bmj openhave explored the postterm effect on maternal mental health.[26-30] blom et al....

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For peer review only A PROSPECTIVE STUDY OF 33 PRETERM MOTHER-INFANT (<33 GA) INTERACTIONS AT SIX AND 18 MONTHS AND THE IMPACT OF MATERNAL MENTAL HEALTH REACTIONS, PREGNANCY AND BIRTH COMPLICATIONS Journal: BMJ Open Manuscript ID: bmjopen-2015-009699 Article Type: Research Date Submitted by the Author: 12-Aug-2015 Complete List of Authors: Misund, Aud R; University College of Oslo and Akershus, Health science Bråten, Stein; University of Oslo, Dept. of Sociology and Human Geography Nerdrum, Per; University College of Oslo and Akershus, Health science Pripp, Are; Oslo University Hospital, Department of Biostatistics, Epidemiology & Health Economy Diseth, Trond; Oslo University Hospital and University of Oslo, Department of Clinical Neurosciences for Children, Women and Children’s Division and Department of Medicine <b>Primary Subject Heading</b>: General practice / Family practice Secondary Subject Heading: Mental health, Obstetrics and gynaecology, Reproductive medicine, Paediatrics Keywords: Neonatal intensive & critical care < INTENSIVE & CRITICAL CARE, MENTAL HEALTH, Maternal medicine < OBSTETRICS, PERINATOLOGY, TRAUMA MANAGEMENT, Child & adolescent psychiatry < PSYCHIATRY For peer review only - http://bmjopen.bmj.com/site/about/guidelines.xhtml BMJ Open on March 16, 2020 by guest. Protected by copyright. http://bmjopen.bmj.com/ BMJ Open: first published as 10.1136/bmjopen-2015-009699 on 4 May 2016. Downloaded from

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Page 1: BMJ Openhave explored the postterm effect on maternal mental health.[26-30] Blom et al. interestingly reported that certain perinatal complications such as preeclampsia, hospitalization,

For peer review only

A PROSPECTIVE STUDY OF 33 PRETERM MOTHER-INFANT

(<33 GA) INTERACTIONS AT SIX AND 18 MONTHS AND THE

IMPACT OF MATERNAL MENTAL HEALTH REACTIONS,

PREGNANCY AND BIRTH COMPLICATIONS

Journal: BMJ Open

Manuscript ID: bmjopen-2015-009699

Article Type: Research

Date Submitted by the Author: 12-Aug-2015

Complete List of Authors: Misund, Aud R; University College of Oslo and Akershus, Health science Bråten, Stein; University of Oslo, Dept. of Sociology and Human Geography Nerdrum, Per; University College of Oslo and Akershus, Health science Pripp, Are; Oslo University Hospital, Department of Biostatistics, Epidemiology & Health Economy Diseth, Trond; Oslo University Hospital and University of Oslo, Department of Clinical Neurosciences for Children, Women and Children’s Division and Department of Medicine

<b>Primary Subject Heading</b>:

General practice / Family practice

Secondary Subject Heading: Mental health, Obstetrics and gynaecology, Reproductive medicine, Paediatrics

Keywords: Neonatal intensive & critical care < INTENSIVE & CRITICAL CARE, MENTAL HEALTH, Maternal medicine < OBSTETRICS, PERINATOLOGY, TRAUMA MANAGEMENT, Child & adolescent psychiatry < PSYCHIATRY

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BMJ Open on M

arch 16, 2020 by guest. Protected by copyright.

http://bmjopen.bm

j.com/

BM

J Open: first published as 10.1136/bm

jopen-2015-009699 on 4 May 2016. D

ownloaded from

Page 2: BMJ Openhave explored the postterm effect on maternal mental health.[26-30] Blom et al. interestingly reported that certain perinatal complications such as preeclampsia, hospitalization,

For peer review only

1

A PROSPECTIVE STUDY OF 33 PRETERM MOTHER-INFANT (<33

GA) INTERACTIONS AT SIX AND 18 MONTHS AND THE IMPACT

OF MATERNAL MENTAL HEALTH REACTIONS, PREGNANCY AND

BIRTH COMPLICATIONS

Aud R. Misund1 Stein Bråten

Per Nerdrum

Are Hugo Pripp

Trond H. Diseth

ABSTRACT

Objective:

Pregnancy, birth and health complications, maternal mental health reactions following

preterm birth and their possible impact on early mother-infant interaction at six and 18

months postterm age (PA) were explored. Predictors of mother-infant interaction at 18 months

PA were identified.

Design and methods:

This prospective longitudinal and observational study included 33 preterm mother-infant (<33

GA) interactions at six and 18 months PA from a socio-economic low risk middle class

sample. The parent-child early relational assessment scale (PCERA) was used to assess the

mother-infant interaction.

Results:

Mothers with clinical important case scores in the Impact of Event Scale, the General Health

Questionnaire, and PTSR/PTSD diagnosis at two weeks postpartum (PP) showed significant

better outcome scores than the mothers without clinical case scores in five PCERA subscales

at six months and in two PCERA subscales at 18 months PA.

1 Faculty of Health Sciences, University College of Oslo and Akershus and Department of Medicine, Institute of

Clinical Medicine, University of Oslo, adr: PO Box. 4 St. Olavs plass, N-0130 Oslo, Norway e-mail:

[email protected]

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“Bleeding in pregnancy” predicted lower quality in preterm mother-infant interaction in six

PCERA scales, while high “Maternal trait anxiety” predicted higher interactional quality in

two PCERA scales at 18 months PA.

Conclusions:

Our study detected a correspondence between early pregnancy complications and lower

quality of preterm mother-infant interaction, and an association between high levels of

maternal mental health problems and better quality in preterm mother-infant interaction.

Strengths and limitations of this study:

The longitudinal design, the high response rate and the use of well validated psychometric

instruments (IES, GHQ and STAI) and interactional assessment tool (PCERA) are strengths

in this study.

Ethical considerations called for a referral procedure to meet need for psychological treatment

among the attending preterm women and it is a limitation that we could not assess the extent

to which our results were influenced by the psychological treatment.

The present study describes a small preterm group and one should be cautious about

generalising from this study.

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INTRODUCTION

Early parent-infant relationships that are well functioning seem to be critical to

preterm children. Preterm children face severe risk of cognitive, learning, and behavioural

disorders from early cerebral injuries,[1-6] and show more psychiatric symptoms in

adolescence.[7] Early parent-infant relationships that are well functioning seem to prevent and

restore some of these difficulties in preterm children.[8, 9]

Good quality in mother-child interactions have been reported to facilitate the infant’s

emotional, behavioural, cognitive, and neurobehavioral development.[10-15] The

interactional quality is also found to be related to the child’s physical health.[16, 17]

The maternal stress reaction following preterm birth has been highlighted as a risk

factor in preterm dyads in several studies.[18-23] Postpartum depression has been identified

as predictor for interactional difficulties in term dyads[24] and reported as a risk factor for

difficulties in preterm mother-infant dyads.[25] Only a limited number of studies, however,

have explored the nature of mothers’ mental health reactions following preterm birth with

psychometric tools, and their impact on mother-infant interaction. Several studies, however,

have explored the postterm effect on maternal mental health.[26-30] Blom et al. interestingly

reported that certain perinatal complications such as preeclampsia, hospitalization, emergency

caesarean, and fetal distress predicted higher depression outcomes in a normal population

sample. An unaddressed trauma reaction is known to predispose for posttraumatic stress

disorder (PTSD) with long term effects on mothers’ mental health. The effect of mothers

postpartum PTSD on mother-infant interaction and infant’s development is less explored.[31]

In addition only a limited number of studies have explored the maternal posttraumatic stress

responses following preterm birth,[32-39] and their impact on mother-infant interactions.[36,

40, 41]

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The results from preterm mother-infant interaction research are contradictory.

Different measurements and definitions being used, as well as the complexity of mother-

infant interactional studies may have contributed to these differences. Some studies have

reported that preterm mothers showed more stimulating behaviour and were emotionally

withdrawn, as well as non-synchronous in their interaction with the child,[40, 42-48] and

others have found no interactional differences between preterm and full term dyads.[40, 49-

54] Korja et al. detected that caregivers’ physical closeness with the infant was more

important to interactional quality than infants’ prematurity.[52] Finally, it is interesting that

several studies have shown that mothers are intensifying their efforts to be available and

supportive to their premature babies’ needs.[55-60] The need for further exploration of the

complexity of factors influencing the early mother-infant relationship long-term in preterm

dyads seems essential.[6, 61]

The focus of this longitudinal study is broad and explorative. We have examined the

possible influence of physical complications and maternal mental health reactions following

preterm birth, assessed at four time points, and their impact on early mother-infant interaction

at six months PA and 18 months PA. To our knowledge, these associations have not been

explored in other studies. Psychometric tools and tentative psychiatric diagnosis (anxiety,

depression, and PTSR/PTSD) were used to assess maternal mental health reactions following

preterm birth.

It should be noted that this paper is an extension of our previous studies of short- and

long-term maternal mental health reactions following preterm birth.[38, 39]

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METHOD

Participants

From June 2005 to July 2008 over two periods of 8 and 10 months, the psychological

responses of 29 consecutive mothers of 35 premature children born before 33rd week of

pregnancy were assessed at a high-specialized neonatal intensive care unit (NICU) at Oslo

University Hospital, Norway. The data collection was performed as soon as the mothers were

able to attend an interview following preterm childbirth: within two weeks postpartum (T0)

median 11 days (4-30); then within two weeks after hospitalization (T1), median time

postpartum 2.7 months (0.2-4.7); then at the infant’s six months postterm age (T2), median

time postpartum 8.5 months (7.6-10.4); and at the infant’s 18 months postterm age (T3),

median time following birth 20.6 months (19.2-23.4). Data collection of mother-infant

interaction was collected only at T2 and T3. Mothers of severely ill babies with uncertain

survival and non-native speakers were not included (Figure 1).

FIGURE 1 ABOUT HERE

Semi-structured interviews and standardized mental health screening questionnaires

were used to collect data about socio-demographics, the pregnancy and birth, child’s health

status, and mothers’ mental health reactions. Medical charts were used to double-check the

data of child’s health status, and pregnancy and birth. The studied sample was homogeneous

regarding high scores on socio-demographic variables such as education, income, and housing

standard. Most mothers were giving first time birth late in their twenties or early thirties. All

lived with the child’s father and none reported any relationship problems (Table 1).

The participating mothers’ mental health reactions following preterm birth have

been assessed at T0, T1, T2, T3 and methods and results are described in detail in our earlier

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papers.[38, 39] Maternal mental health problems were assessed at every time points (T0, T1,

T2, T3) by standardized psychometric methods with well-established reliability and validity:

Impact of Event Scale (IES), one of the key psychometric assessment methods in traumatic

stress research,[62, 63] the General Health Questionnaire (GHQ) 30-item version, a widely

used screening instrument for assessing the presence of distress, psychopathology and overall

well-being,[64, 65] and the State/Trait Anxiety Inventory (STAI-X1/X2)[66] is widely used to

assess maternal anxiety. Scores above the threshold for identifying a psychiatric case is

referred to as a clinical important case score.

Based on all information available in a clinical perusal of the psychometric self-reports

IES, GHQ and STAI of each of the 29 preterm mothers, and blinded to the physical and socio-

demographic characteristics of the mothers and their children, a tentative clinical diagnosis

was made where appropriate based on the clinical descriptions and diagnostic guidelines in

the ICD-10 Classification of mental and behavioural disorders, and was assessed by a

psychiatrist (last author).

A prevalence of maternal posttraumatic stress responses/disorders (PTSR/PTSD) two

weeks postpartum (T0) of 52% and maternal PTSD at 18 months postterm age (T3) of 23%

was revealed. On the other hand, depression was detected among 24 % of the mothers two

weeks postpartum and among 8% of the mothers at T3. Anxiety decreased from 7% at two

weeks postpartum to zero at T3.

Fourteen of the mothers received psychological support at the hospital during their

infants’ NICU stay. Eleven of these mothers were referred for further psychological treatment

after discharge from the hospital. Altogether, 20 mothers that met the criteria of clinical

diagnoses were referred for adequate psychological treatments such as psychotherapy,

psychopharmacology treatment, and mother-infant interactional treatment. Five of the

mothers refused the referral for psychological treatment, and only one of them filled the

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criteria for a tentative clinical diagnosis (PTSD/Depression) at T3. The prevalence of

pregnancy and birth complications and maternal mental health reactions following preterm

birth are reported in earlier papers.[38, 39]

Data collected at 2 weeks postpartum (T0) about sociodemographics, physical

complications and maternal mental health reactions following preterm birth are presented in

Table 1.

TABLE 1 ABOUT HERE

Measures

Mother–infant interaction in a free-play situation was video recorded at six and 18

months PA. According to Clark (1985) by six months of age, dyadic mutuality and dyadic

regulatory processes are perceptible while at 18 months, the infant's own communication

skills are easier to identify in interaction [67]. The interaction situation was recorded in a

consultation room at the psychiatric clinic for children and families situated in the same

building as the hospital the children were born in, except for four video recordings at 18

months PA that were recorded in their homes. The recordings were performed when child was

awaken and interested in a play session with mother. Recordings were stopped and performed

later when child became too distressed or sleepy to play. A therapist (first author) instructed

the mothers about the procedure. For the video recording, the mother and the infant were

placed on a soft mat with age-appropriate toys. Instructions by the investigators given to the

mother prior to the video recording were: ‘This is a free-play time with your child. You can

use the toys, or you can play without the toys. Try to play or be with your infant as you

usually would be”. Video recordings were obtained from all mother-infant pairs.

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The recordings were five minutes long. The mother-infant interaction in the free-play

situation was analysed using the Parent-Child Early Relational Assessment (PCERA)

method.[67] The PCERA is developed to assess affective and behavioural aspects that both

the parent and infant bring into the interaction,[67] and the validity of the free play situation

has been established.[68, 69] Video recordings allows thoroughly analysis of the interactions

several times and in short and slow sections that can identify areas of strength and of concern

in the mother-infant interplay. The PCERA consists of 29 parental items, 28 infant items and

eight dyadic items. The assessment rates the frequency, duration and intensity of the infant's,

parent's and dyad's behaviour. The parental items comprise the parent's positive and negative

affect, expressed attitude toward the infant, sensitivity and contingent response to the infant's

cues, mirroring the infant's feeling, capacity to structure, behavioural involvement and

parental style. The infant items comprise expressed positive and negative affect and

characteristic mood, behaviour/adaptive abilities, activity level and communication skills. The

dyadic items comprise affective quality of interaction and mutuality of interaction.

All items were rated on a 5-point “Likert” scale. The scores 1 and 2 describe an area of

concern, the score 3 describes an area of some concern and the scores 4 and 5 describe an area

of strength. A trained coder made the assessment. The coder was unaware of the infant's

background and clinical status. Additionally, to estimate the interrater reliability from the

study data, 20% of all assessments were double-scored by another trained coder. The study

data was assessed by calculating the mean of the agreement percentage of the raters' overall

agreement. Agreement equal or above 80% is considered good, 50-80% is considered

moderate, and lower than 50% is considered poor. The mean of interrater agreements was

80.3% in six months PA and 81% in 18 months PA.

The PCERA items were organized in eight scales according to Clark [67] before the

data analysis: “Maternal positive affective involvement PS1”, “Maternal negative affect &

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behaviour PS2”, “Maternal intrusiveness PS3”, “Infant positive affect PS4”, “Infant quality

of play PS5”, “Infant dysregulation PS6”, “Dyadic mutuality & reciprocity PS7”, and “Dyadic

disorganization & tension PS8”. PCERA high scores (4-5) always indicate positive affect and

behaviour or lack of negative affect and behaviour. The Cronbach alpha coefficients for

calculating the internal consistency of PCERA subscales in our study were satisfactorily and

were .95,.86,.86, .90,.87,.85,.80,.86 for PS1-PS8 at six months PA (T2), and

.89,.81,.82,.92,.89,.75,.73,.79 for PS1-PS8 at 18 months PA (T3).

The PCERA scale has been used in several studies to explore the quality of preterm

mother-infant interactions.[25, 70-74]

Statistical methods

Values of continuous variables are presented as means (SD) or if skewed, as median

and range. Categorical variables are given as proportions and percentages. Paired-sample t-

test was used for comparison of the PCERA means scores at T2 and T3. Differences in the

quality of mother-infant interactions measured by the PCERA scales were explored with

independent-samples t-test. As grouping variable we used mothers’ clinical important case

scores (0=no, 1=yes) in IES, GHQ, STAI and the tentative diagnostic assessments at four time

points; two weeks PP (T0), two weeks after hospitalization (T1), six months PA (T2), and 18

months PA (T3) (Figure 2). A more detailed description of mothers’ clinical important case

scores in IES, GHQ, STAI and the tentative diagnostic assessments are available in our earlier

papers.[38, 39]

The correlations between normally distributed and continuous variables at T3 in

correlation analysis were measured using Pearson’s correlation coefficient or Spearman’s

correlation coefficient when the variables had a skewed distribution (Table 2).

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Forward linear regression analysis was used to identify possible predictors of the PCERA

results at T3 (Table 3). The three variables at T3 with the strongest bivariate associations

(<0.05) were included in the multivariable linear regression model. A careful check of the

model assumptions, including an investigation of residual plots, did not reveal any violation

of the assumptions. All analyses were performed in SPSS version 20. Two-sided statistical

tests were applied and a 5 % statistical significance level was chosen.

Ethics

Written informed consent was obtained from participants prior to the study start. The

study protocol was approved in 5 May 2005 and 19 April 2007 by the National Committee for

Research Ethics (S-05068 and S-07096b) and 1 April 2005 and 12 March 2007 by the Data

Inspectorate (12360 and 07/1088). The study protocol was carried out in accordance with the

Declaration of Helsinki.

For ethical reasons the mothers that reported clinically important mental health

problems were assessed and referred for adequate psychological treatment. In this study, we

looked for clinically important mental health problems in mothers at four points from the time

of birth to two years postpartum. A no referral procedure could have caused unnecessary

suffering for both mothers and children.

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RESULTS

Mother-Infant Interaction

The paired sample t-test of the results of the PCERA showed no significant difference

for the PCERA mean scores from six months to 18 months postterm age (PA). For that reason

the presented results are based only on the mean scores from 18 months PA. The results of the

PCERA revealed mean scores in three of the scales in the area of moderate concern and five

scales in the area of no concern (Table 2).

Differences in the quality of mother-infant interaction at T2 and T3 between mothers with or

without clinically important case scores at T0, T1, T2, and T3

The results of the independent-samples t-test showed significant group differences at

T2 and T3 between the mothers with clinically important case scores compared to mothers

without case scores in IES, GHQ, and tentative PTSR diagnosis at T0 (Figure 2). Mothers’

with clinical case scores at T3 in GHQ also showed significant better results at the .05 level

(2-tailed)* in two PCERA scales at T3; PS7 Dyadic mutuality and reciprocity (N0/N1=24/8,

mean 3.1/3.7*), and PS8 Dyadic disorganization and tension (N0/N1=24/8, mean 3.9/4.4*).

Most unexpectedly, the mothers with clinically important case scores (1=yes) at T0 showed

significantly better quality in mother-infant interaction in seven of the PCERA subscales at T3

than mothers with no (0=no) clinically important case scores (Figure 2). Tentative depression

or anxiety diagnosis (0=no, 1=yes) as a grouping variable showed no significant group

differences regarding the quality of the mother-infant interaction.

FIGURE 2 ABOUT HERE

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Psychometric means correlation with mother-infant interactional quality

In the bivariate correlation analyses, we revealed a positive correlation between better

interactional quality measured by PCERA and higher levels of maternal mental health

reactions measured by psychometric means at T3. High levels of GHQ Likert and clinical

case scores correlated with high levels of PCERA scores in three scales and GHQ case sum

scores correlated with two scales. High levels of STAI-X2 sum scores were associated with

high levels of PCERA scores in two scales and clinical case scores correlated with three

scales (Table 2).

Maternal and infant physical variables correlation with mother-infant interactional quality

Three maternal variables correlated with two of the PCERA scales. Parity (number of

previous births with child survival) and the scale “Maternal intrusiveness, intensity and

inconsistency (PS3)” were positively correlated. Family size (number of children in the

family) and the “Infant dysregulation and irritability (PS6)” scale inversely correlated. “Acute

caesarean” correlated positively with high scores on the same scale.

Two infant complications were correlated with two of the PCERA scales. Infant health

scores at the infant’s “Apgar scores at 5 minutes postpartum” correlated positively with the

“Infant quality of play, interest, and attention (PS5)” scale. Infant stroke by “Intraventricular

Haemorrhage grade 1 or 2 (IVH)” closely following birth” correlated inversely with the

“Maternal negative affect and behaviour (PS2)” scale (Table 2).

The strongest correlations were inversely and found between a pregnancy

complication “Bleeding in pregnancy” and the following six PCERA scales: “Maternal

negative affect and behaviour (PS2), Maternal intrusiveness, intensity, and inconsistency

(PS3), Infant positive affect, communicative, and social skills (PS4), Infant quality of play,

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interest, and attention (PS5), Dyadic mutuality and reciprocity (PS7), and Dyadic

disorganization and tension (PS8)”.

TABLE 2 ABOUT HERE

Predictors of preterm mother-infant interactional quality

In the multiple linear regression analyses we revealed that the pregnancy complication

variable “Bleeding in pregnancy” was a significant predictor (p<0.01) of lower scores in

preterm mother-infant interaction in six of the PCERA domains, including both of the Dyadic

scales (Table 3). Trait anxiety (STAI-X2) clinically important case and sum score are

significant predictors for higher quality in preterm mother-infant interaction in the “Maternal

positive affect domain (PS1)” (p<0.01) and in the “Maternal intrusiveness (PS3)” domain

(p<0.05), consecutively. Higher “Number of children in the family” predicts lower interaction

quality in the “Infant dysregulation and irritability (PS6)” scale (p<0.05). Adjusted R2 showed

that the predictors explain from 17 to 39 % of the variance in different PCERA scales.

TABLE 3 ABOUT HERE

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DISCUSSION

The study revealed significant associations between pregnancy and birth

complications, maternal postpartum mental health, and the quality of preterm mother-infant

interaction. The most surprising results in our study were the detection of “Bleeding in

pregnancy” as a predictor of lower quality in preterm mother-infant interaction in six of eight

PCERA scales and the association between high levels of maternal mental health problems

and better mother-infant interactional quality.

The predictor “Bleeding in pregnancy” is profoundly interesting. No other study has,

to our knowledge, revealed a physical complication in pregnancy that predicts the quality of

the preterm mother-infant interaction. In a previous paper, we detected that “Bleeding in

pregnancy” was a predictor of low levels in maternal mental health reactions, while

“Preeclampsia”, which is a sudden complication later in pregnancy, predicted high levels of

maternal mental health reactions following preterm birth. “Bleeding in pregnancy” could be

experienced as an early warning sign for possible pregnancy complications as it usually

occurs before 22 weeks of pregnancy.

Two questions now arise: is it possible to provide an existential explanation of why “Bleeding

in pregnancy” contributes to low levels of PCERA scores in preterm mother-infant

interaction? Could it be that the mother-to-be feels “Bleeding in pregnancy” as a near-loss

experience leaving her with the frightening impression that her child is at risk (in which case

the preterm birth confirms the fear of loss)? Given such an enduring threatening impression,

the mother can be expected to be anxious and alert, preventing her from relaxing and taking

pleasure in the mother-infant interaction, and rather inviting negative affect and intrusiveness

which may also entail dyadic disorganization and tension.

A mother experiencing a sudden preterm birth with infant survival and no serious early

warning signs is likely to have been quite “undisturbed” in her transition process to prepare

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for motherhood. A preterm birth may represent a very dangerous situation for both mother

and child where both may have risked death. When mother experiences hope for survival, we

may assume that a prior “undisturbed” transition process into motherhood is likely to increase

her efforts to attain the very best mother-infant interaction.

Most unexpectedly, our results showed that high levels of maternal mental health

problems following preterm birth were associated with better quality in preterm mother-infant

interaction. In regression analysis, we found that high levels of maternal trait anxiety (STAI-

X2) scores predicted better scores in two PCERA scales at T3. In the independent-samples t-

test, we revealed that mothers with clinically important case scores on IES, GHQ, STAI and

the tentative diagnoses of PTSR/PTSD at 2 weeks postpartum (T0) showed significantly

better quality in mother-infant interaction on six PCERA scales at six months (T2) and on five

PCERA scales at 18 months postterm age (T3). The STAI trait’s association with general

psychological distress following preterm birth has been reported in our previous papers.[38,

39] In addition, the STAI trait’s association with posttraumatic stress following term birth has

also been reported by another study.[75]

It is theoretically interesting that our results imply that high levels of maternal mental

distress improve the preterm mother–infant interaction. At first glance, this result seems to

contradict the well-known connection between high levels of maternal depression and high

risk mother-infant interactions.[25, 76-78] It should be noted that we found quite low

prevalence of depression among the mothers participating in this study.[38, 39] Instead, we

found high levels of posttraumatic stress reactions. PTSD following childbirth is

acknowledged by several researchers to be potentially different from PTSD following other

traumatic incidences.[31] The culturally positive connotation of giving birth, the mother-child

connection, the transition from pregnancy to birth, and the formal care setting the birth

incident takes place in are all matters that may have an impact on PTSD following preterm

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birth. Several studies have reported that many people experience positive psychological

growth after struggling with trauma.[79] Maternal posttraumatic stress reaction following

preterm birth is characterized by a prior physical trauma where survival of the mother and the

baby may be at risk. Is it possible that maternal posttraumatic stress reactions following

preterm birth helps the mother to focus her attention towards her premature baby’s wellbeing?

Our results may imply that the posttraumatic stress response activates and helps the mother

cope over time with a tremendously stressful situation, and furthermore helps her stimulate

the prematurely born child’s healthy development. Several studies support our view.[56-58,

60] Other studies that have explored maternal mental health reactions following preterm birth

and preterm mother-child interactions have reported results that contrast with our own.[36, 46,

73, 80] Studies that have used the PCERA scale in studying preterm dyads, however, did not

find depression to be a significant predictor of PCERA outcome at six, 12, or16 months

PA.[25, 71] On the other hand, they reported that high infant heart rate variety (HVR) after

feeding,[72] and higher frequency of naps had a positive impact on preterm mother-infant

interaction.[74]

The socio-demographic variable “Number of children in the family” predicted low

interactional quality in one of the PCERA scales. In our study, the mothers with preterm

babies that had siblings showed significantly lower scores in the “Infant dysregulation scale

(PS6)” in the PCERA. Our result is supported by two studies in the 1970’s and 1980’s that

found the preterm infant’s birth-order to affect the mother-child interaction.[81, 82] An

explanation for their results was the mother’s divided attention between the infant and other

siblings.

Strength/limitations

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The participants in this study came from well-defined geographic areas and both single

and multiple births were included consecutively in the study, thus minimizing selection bias.

Our sample was homogeneous in socio-economic background (SES).The mothers had higher

educational attainments, greater age and higher socioeconomic status, higher number of twins

and higher rate of previous psychological treatment than would be found in a typical

population of mothers who deliver preterm in our country. In this sample we found no

indication of significant differences in parental challenges between participants with

singletons or twins that needed to be addressed in the analysis. Besides the high prevalence of

earlier psychological treatment among the mothers in our sample, we found no other

indication of mental distress that had an impact on their psychosocial function in everyday life

before the actual preterm birth incident. Regarding research on quality of the preterm mother-

infant interaction, it has been considered that risk factors other than preterm birth itself may

have created bias / been sources of bias in many studies [40, 44, 83]. In our study, we have

controlled for high risk socio-economic backgrounds.

It is a limitation that the video-procedure of PCERA could not be followed for the four

dyads that were recorded in their homes and not in the clinic, as were the others. On the other

hand, these dyads would not have participated if the recordings were not made in their homes.

It is a limitation that interrater reliability was not checked for tentative clinical diagnosis. The

prediction model used in this study needs further validation by future studies.

CONCLUSIONS

Our results imply that pregnancy complications occurring early in the pregnancy may

affect the bonding process between the mother and her preterm infant long term. Early

intervention programs should be offered to mothers with early pregnancy complications to

support mother-infant interaction.

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Acknowledgements

The authors would like to thank the families that participated in the study, the staff of the

maternity ward at the neonatal intensive care unit at the National Hospital, Oslo and Sari

Ahlqvist-Björkroth who coded and Tanja Lipasti who recoded the PCERA data. In particular,

we want to thank the parents who participated in the study.

Contributorship statement

ARM initiated the study, collected, and organized the data. ARM and AHP performed the

statistical analyses. ARM, PN, SB, AHP and THD wrote the article.

Competing interests

We have no information of disclosure of interests.

Funding

This work was supported by the Centre for Child and Adolescent Mental Health, Eastern and

Southern Norway and the University College of Oslo and Akershus.

Data sharing statement

All authors have read and approved the final manuscript and have given their consent for

publication in BMJ Open.

Word count 3983

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adults. Acta Psychiatrica Scandinavica, 1989. 80: p. 103-112.

66. Spielberger, C.D., R.L. Goursch, and R.E. Luschene, STAI Manual for the State-Trait Anxiety

Inventory. 1970, California: Palo Alto: Consulting Psychologists Press.

67. Clark, R., The parent-child early relational assessment: Instrument and manual. Madison:

University of Wisconsin Medical School, Department of Psychiatry, 1985.

68. Clark, R., et al., Length of Maternity Leave and Quality of Mother-Infant Interactions. Child

Development, 1997. 68(2): p. 364-383.

69. Clark, R., The Parent-Child Early Relational Assessment: A Factorial Validity Study. Educational

and Psychological Measurement, 1999. 59(5): p. 821-846.

70. Korja, R., et al., Relations between maternal attachment representations and the quality of

mother-infant interaction in preterm and full-term infants. Infant Behavior & Development,

2010. 33(3): p. 330-336.

71. McManus, B. and J. Poehlmann, Parent–child interaction, maternal depressive symptoms and

preterm infant cognitive function. Infant behavior & development, 2012. 35(3): p. 489.

72. Schwichtenberg, A., et al., Daytime sleep and parenting interactions in infants born preterm.

Journal of Developmental and Behavioral Pediatrics, 2011. 32(1): p. 8-17.

73. Shah, P.E., M. Clements, and J. Poehlmann, Maternal Resolution of Grief After Preterm Birth:

Implications for Infant Attachment Security. Pediatrics, 2011. 127(2): p. 284-292.

74. Poehlmann, J., et al., Emerging self-regulation in toddlers born preterm or low birth weight:

Differential susceptibility to parenting. Development and Psychopathology, 2011. 23(1): p.

177-193.

75. Czarnocka, J. and P. Slade, Prevalence and predictors of post-traumatic stress symptoms

following childbirth. British journal of clinical psychology, 2000. 39(1): p. 35-51.

76. Downey, G., Children of depressed parents: an integrative review. Psychological bulletin,

1990. 108(1): p. 50.

77. Goodman, S.H., Risk for psychopathology in the children of depressed mothers: a

developmental model for understanding mechanisms of transmission. Psychological review,

1999. 106(3): p. 458.

78. Lovejoy, M.C., et al., Maternal depression and parenting behavior: A meta-analytic review.

Clinical Psychology Review, 2000. 20(5): p. 561-592.

79. Tedeschi, R.G., C.L. Park, and L.G. Calhoun, Posttraumatic growth: Conceptual issues, in

Posttraumatic growth: Positive changes in the afternath of crisis, R.G. Tedeschi, C.L. Park, and

L.G. Calhoun, Editors. 1998, Earlbaum: Mahwah, NJ. p. 1-22.

80. Feeley, N., L. Gottlieb, and P. Zelkowitz, Infant, Mother, and Contextual Predictors of Mother-

Very Low Birth Weight Infant Interaction at 9 Months of Age. Journal of Developmental &

Behavioral Pediatrics, 2005. 26(1): p. 24-33.

81. Bendersky, M. and M. Lewis, The impact of birth order on mother–infant interactions in

preterm and sick infants. Journal of developmental and behavioral pediatrics, 1986. 7(4): p.

242-246.

82. Cohen, S.E. and L. Beckwith, Caregiving Behaviors and Early Cognitive Development as

Related to Ordinal Position in Preterm Infants. Child Development, 1977. 48(1): p. 152-157.

83. Wille, D.E., Relation of preterm birth with quality of infant--mother attachment at one year.

Infant Behavior and Development, 1991. 14(2): p. 227-240.

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For peer review only

5 mothers with 5 infants refused to

participate

*4 mothers out of lack of energy or

mental capacity or lack of time.

*1 mother refused to be videotaped

1 mother with 1 infant refused to

participate at T3 due to her working load

2 mothers with 2 infants refused to

participate at T1

*1 mother started to work

*1 mother and infant were

transferred to another Hospital

34 mothers with 40 infants assessed for

eligibility

29 mothers with 35 infants included at 2

weeks postpartum (T0) and examined for maternal mental health problems.

26 mothers with 32 infants included at 18

months post term age (T3) and examined for maternal mental health problems and

for dyadic interaction.

27 mothers with 33 infants included at 2

weeks after discharge from hospital (T1) and examined for maternal mental health

problems.

27 mothers with 33 infants included at 6

months post term age (T2) and examined for maternal mental health problems and

for dyadic interaction.

Figure 1. Inclusion and exclusion of mothers of preterm born babies

Page 23 of 30

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For peer review only

[Skriv her]

Figure 2. Differences in the quality of mother – infant interaction at T2; 6 months post term age (PA) and T3; 18 moths PA for mothers with (N1) and mothers without (N0) case scores in

psychometric means of IES, GHQ, and STAI, and tentative PTSR diagnosis at T0; 2 weeks

postpartum. Interaction quality is measured by the mean values in the PCERA subscales.

2.9

3.4

3.9

4.4

6 months PA

(T2) Case

18 months PA

(T3) Case

6 months PA

(T2) No Case

18 months PA

(T3) No Case

Mean PCERA subscale score in (PS1) Parental

Positive Affctive Involvement and

Verbalization for Mothers with or without

Case Score in IES, GHQ, STAI, and with or

without PTSR diagnosis at T0.

IES, T2(T3):N1=17(16), N0=16(16) T3*

GHQ, T2(T3):N1=27(27), N0=6(5) T2*

STAI-X1, T2(T3):N1=23(22), N0=10(10)

STAI-X2, T2(T3):N1=31(30), N0=2(2)

PTSR, T2(T3):N1=17(16), N0=16(16) T3*

3.6

4.1

4.6

6 months PA

(T2) Case

18 months PA

(T3) Case

6 months PA

(T2) No Case

18 months PA

(T3) No Case

Mean PCERA subscale score in (PS2) Parental

Negative Affctive Involvement and

Verbalization for Mothers with or without

Case Score in IES, GHQ, STAI, and with or

without PTSR diagnosis at T0.

IES, T2(T3):N1=17(16), N0=16(16)

GHQ, T2(T3):N1=27(27), N0=6 (5)

STAI-X1, T2(T3):N1=23(22), N0=10 (10)

STAI-X2, T2(T3):N1=31(30), N0=2(2) T2***

PTSR, T2(T3):N1=17(16), N0=16(16)

2.8

3.3

3.8

4.3

6 months PA

(T2) Case

18 months PA

(T3) Case

6 months PA

(T2) No Case

18 months PA

(T3) No Case

Mean PCERA subscale score in (PS3) Parental

Intrusiveness, Intensitivity, and Inconsistency

for Mothers with or without Case Score in IES,

GHQ, STAI, and with or without PTSR

diagnosis at T0.

IES, T2(T3):N1=17(16), N0=16(16)

GHQ, T2(T3):N1=27(27), N0=6 (5)

STAI-X1, T2(T3) N1=23(22), N0=10 (10)

STAI-X2, T2(T3):N1=31(30), N0=2(2) T2**

PTSR, T2(T3):N1=17(16), N0=16(16) T2*

2

2.5

3

3.5

6 months PA

(T2) Case

18 months PA

(T3) Case

6 months PA

(T2) No Case

18 months PA

(T3) No Case

Mean PCERA subscale score in (PS4) Infant

Positive Affect Communicative and Social

Skills for Mothers with or without Case Score

in IES, GHQ, STAI, and with or without PTSR

diagnosis at T0.

IES, T2(T3):N1=17(16), N0=16(16)

GHQ, T2(T3):N1=27(27), N0=6 (5) T2**

STAI-X1, T2(T3):N1=23(22), N0=10 (10)

STAI-X2, T2(T3):N1=31(30), N0=2(2)

PTSR, T2(T3):N1=17(16), N0=16(16)

2.9

3.1

3.3

3.5

3.7

3.9

4.1

6 months PA

(T2) Case

18 months PA

(T3) Case

6 months PA

(T2) No Case

18 months PA

(T3) No Case

Mean PCERA subscale score in (PS5) Infant

Quality of Play and Relatedness for Mothers

with or without Case Score in IES, GHQ, STAI,

and with or without PTSR diagnosis at T0.

IES, T2(T3):N1=17(16), N0=16(16)

GHQ, T2(T3):N1=27(27), N0=6 (5)

STAI-X1, T2(T3):N1=23(22), N0=10 (10)

STAI-X2, T2(T3):N1=31(30), N0=2(2) T3*

PTSR, T2(T3):N1=17(16), N0=16(16)

3.6

3.8

4

4.2

4.4

4.6

4.8

6 months PA

(T2) Case

18 months PA

(T3) Case

6 months PA

(T2) No Case

18 months PA

(T3) No Case

Mean PCERA subscale score in (PS6) Infant

Dysregulation and Irritability for Mothers with

or without Case Score in IES, GHQ, STAI, and

with or without PTSR diagnosis at T0.

IES, T2(T3):N1=17(16), N0=16(16)

GHQ, T2(T3):N1=27(27), N0=6 (5)

STAI-X1, T2(T3):N1=23(22), N0=10 (10)

STAI-X2, T2(T3): N1=31(30), N0=2(2)

PTSR, T2(T3):N1=17(16), N0=16(16)

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For peer review only

[Skriv her]

N0 = the number of mothers without case scores in IES, GHQ, STAI and PTSR diagnosis at T0.

N1= the number of mothers with case scores in IES; GHQ; STAI and PTSR diagnosis.

*Significant difference at the .05 level (2-tailed) at the time referred to as T2 (6 months PA) or T3 (18 months PA).

**Significant difference at the .01 level (2-tailed) at the time referred to as T2 (6 months PA) or T3 (18 months PA).

*** Significant difference at the .001 level (2-tailed) at the time referred to as T2 (6 months PA) or T3 (18 months PA).

2.1

2.3

2.5

2.7

2.9

3.1

3.3

3.5

6 months PA

(T2) Case

18 months PA

(T3) Case

6 months PA

(T2) No Case

18 months PA

(T3) No Case

Mean PCERA subscale score in (PS7) Dyadic

Mutuality and Reciprocity for Mothers with or

without Case Score in IES, GHQ, STAI, and with

or without PTSR diagnosis at T0.

IES, T2(T3):N1=17(16), N0=16(16)

GHQ, T2(T3):N1=27(27), N0=6 (5) T2**

STAI-X1, T2(T3):N1=23(22), N0=10 (10)

STAI-X2, T2(T3):N1=31(30), N0=2(2)

PTSR, T2(T3):N1=17(16), N0=16(16)

2.5

2.7

2.9

3.1

3.3

3.5

3.7

3.9

4.1

4.3

6 months PA

(T2) Case

18 months PA

(T3) Case

6 months PA

(T2) No Case

18 months PA

(T3) No Case

Mean PCERA subscale score in (PS8) Dyadic

Disorganization and Tension for Mothers

with or without Case Score in IES, GHQ, STAI,

and with or without PTSR diagnosis at T0.

IES, T2(T3):N1=17(16), N0=16(16)

GHQ, T2(T3):N1=27(27), N0=6 (5)

STAI-X1, T2(T3):N1=23(22), N0=10 (10)

STAI-X2, T2(T3):N1=31(30), N0=2(2) T2*

PTSR, T2(T3):N1=17(16), N0=16(16)

Page 25 of 30

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For peer review only

Table 1. Socio-demographic, physical characteristics, and mental health variables in mothers

giving preterm birth and their children at two weeks postpartum (T0).

Mothers n=29

Age; mean (SD) 33.7 (4.3)

Education > 12 years; n (%) 26 (89.7)

Single parent; n (%) 0 (0)

Unemployed; n (%) 4 (13.8)

Previous psychological treatment; n (%)

8 (27.6)

Chronic illness; n (%) 2 (6.9)

Tot. no. of children; mean (SD) 1.7 (.8)

Previous pregnancies; mean (SD) 1.1 (1.5)

Previous childbirths; mean (SD) .5 (.7)

First time mothers; n (%) 18 (62.1)

IVFa pregnancy; n (%) 8 (27.6)

Bleeding in pregnancy; n (%) 19 (65.5)

Preeclampsia; n (%) 4 (14.3)

Caesarean; n (%) 17 (58.6)

Mental Health Variables:b

IES total (0-75); mean (SD) 19.7 (10.8)

IES Clinically significant case score >18; n (%) 13 (44.8)

GHQ Likert (0-90); n (%) 40 (15.4)

GHQ case (0-30): n (%) 12.8 (7.5)

GHQ Clinically important case score >5; n (%) 23 (79.3)

STAI-X1 (0-40); mean (SD) 21.5 (2.8)

STAI-X1 Clinically important case score >19; n (%) 20 (69)

STAI-X2 (0-80); mean (SD) 44.0 (4)

STAI-X2 Clinically important case score >39; n (%) 27 (93.1)

PTSR/PTSD Clinical diagnosis; n (%) 15 (51.7)

Children n=35

Girl; n (%) 17 (48.6)

Boy; n (%) 18 (51.4)

Twinc; n (%) 14 (40)

Gestational age (weeks);

Median (range)

Mean (SD)

29 (24-32)

28.5 (2.6)

Birth weight (kg);

Median (range)

Mean (SD)

1.2 (.6-2.0)

1.2 (.4)

Apgar score at 1 minute; median (SD) 6.3 (2.3)

Apgar score at 5 minutes; median (SD) 7.6 (2.0)

Apgar score at 10 minutes; median (SD) 8.3 (1.0)

Oxygen supply > 28 days; n (%) 19 (54)

IVHd; n (%) 7 (20.0)

a In vitro fertilization/Assisted fertilization.

bThe Impact of Event Scale (IES), The General Health Questionnaire (GHQ), The Spielberger State Trait Anxiety Inventory (STAI-X1/X2),

Tentative Clinical Diagnosis: Posttraumatic Stress Responses (PTSR), Posttraumatic Stress Disorder (PTSD).

cTwo of the twins were raised as singleton as their twin sibling were stillborn.

dIntraventricular hemorrhage grade 1-4 following birth.

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For peer review only

Table 2. Bivariate correlations at T3 (18 months post term age) between the PCERA scales, the maternal psychometric means, and the individual characteristics of the

mothers and infants. Pearson’s correlation coefficients (p<.05) are reported. (N=32). Mean values for PCERA subscales and 95% confidence interval for mean, are

reported in the last row of this table.

PCERA PS1

Maternal

Positive

affective

involvement

PCERA PS2

Maternal

Negative

affect &

behavior

PCERA PS3

Maternal

Intrusiveness

Insensitivity

Inconsistency

PCERA PS4

Infant

Positive affect

Communica-

tive & social

skills

PCERA PS5

Infant

Quality of

play

Interest

Attention

PCERA PS6

Infant

Dys-

regulation

Irritability

PCERA PS7

Dyadic

Mutuality

Reciprocity

PCERA PS8

Dyadic

Dis-

organization

Tension

GHQ Likert

sum score

.39*

.37*

.35* .16 .12 .05 .30 .28

GHQ case

sum score

.36* .36* .06 .12 .07 .17 .26 .31

GHQ

case > 5

.26 .40* .30 .33 .29 .21 .41* .43*

STAI-X2

sum score

.46** .21 .39*

.09 -.03 .08 .25 .19

STAI-X2

case > 39

.48* .36* .57** .19 .06 .07 .32 .32

Parity

.07

.18 .39* .24 .10

.01

.31 .33

CH< grade 3a

-.21 -.28 -.35* -.20 -.23 -.15 -.30 -.35

Apgar

at 5 minutes

-.01 .09 .20 .22 .35* -.12 .18 .19

Bleedings in

pregnancy

-.22 -.45** -.56** -.53** -.55** -.33 -.46** -.52**

Family sizeb

-.09 -.12 .07 -.02 -.16 -.45* .01 .00

Acute

Caesarean

.14 .14 .13 .01 .03 .39* .07 .22

Mean values

1-5 c(95% CI)

3.8 (3.6–4.1) 4.6 (4.4–4.8) 4.2 (4.0–4.4) 3.2 (2.9–3.5) 4.0 (3.7–4.2) 4.5 (4.4–4.7) 3.3 (3.0–3.5) 4.0 (3.8–4.2)

*Correlation is significant at the .05 level (2-tailed). **Correlation is significant at the .01 level (2-tailed). a CH< grade 3 refers to Cerebral Hemorrhage grade 1 or 2 closely after birth.

b Family size refers to the number of children in the family.

c Rates 1 and 2 in PCERA subscale; “Area of concern”. Rate 3 in PCERA subscale; “Area of moderate concern”. Rates 4 and 5 in PCERA subscale; “Area of no concern”.

Page 27 of 30

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on March 16, 2020 by guest. Protected by copyright. http://bmjopen.bmj.com/ BMJ Open: first published as 10.1136/bmjopen-2015-009699 on 4 May 2016. Downloaded from

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For peer review only

Table 3. Forward entry multiple regression analyses predicting mother-child interaction

outcomes for PCERA in preterm mother–child dyads at T3 (18 months post term age).

Unstandardized (B) and standardized (Beta) regression coefficients. (N=32)

Predicting variable B CI Beta P-

value

R2

adj.

PCERA:

Maternal positive aff-

ective involvement PS1

STAI-X2 clinical

important case score

.53 (.17, .89) .48 .005 .21

Maternal negative

affect & behavior PS2

Bleeding in pregnancy -.21 (-.37, -.06) -.45 .009 .18

Maternal intrusiveness

PS3

Bleeding in pregnancy

STAI-X2 total sum

-.29

.03

(-.45, -.13)

(.01, 06)

-.53

.35

.001

.017

.39

Infant positive affect

PS4

Bleeding in pregnancy -.43 (-.68, -.17) -.53 .002 .26

Infant quality of play

PS5

Bleeding in pregnancy -.35 (-.56, -.15) -.55 .001 .27

Infant dysregulation

PS6

Number of children in

the family

-.24

(-.42, -.06)

-.45

.011

.17

Dyadic mutuality &

reciprocity PS7

Bleeding in pregnancy

-.33

(-.56, -.09)

-.33

.008

.21

Dyadic disorganization

& tension PS8

Bleeding in pregnancy

-.32

(-.51, -.12)

-.52

.002

.25

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For peer review only

STROBE 2007 (v4) Statement—Checklist of items that should be included in reports of cohort studies

Section/Topic Item

# Recommendation Reported on page #

Title and abstract 1 (a) Indicate the study’s design with a commonly used term in the title or the abstract 1

(b) Provide in the abstract an informative and balanced summary of what was done and what was found 1

Introduction

Background/rationale 2 Explain the scientific background and rationale for the investigation being reported 3-4

Objectives 3 State specific objectives, including any prespecified hypotheses 4

Methods

Study design 4 Present key elements of study design early in the paper 5

Setting 5 Describe the setting, locations, and relevant dates, including periods of recruitment, exposure, follow-up, and data

collection

5

Participants 6 (a) Give the eligibility criteria, and the sources and methods of selection of participants. Describe methods of follow-up 5

(b) For matched studies, give matching criteria and number of exposed and unexposed

Variables 7 Clearly define all outcomes, exposures, predictors, potential confounders, and effect modifiers. Give diagnostic criteria, if

applicable

5-9

Data sources/

measurement

8* For each variable of interest, give sources of data and details of methods of assessment (measurement). Describe

comparability of assessment methods if there is more than one group

5-9

Bias 9 Describe any efforts to address potential sources of bias 5 -9

Study size 10 Explain how the study size was arrived at 5

Quantitative variables 11 Explain how quantitative variables were handled in the analyses. If applicable, describe which groupings were chosen and

why

9-10

Statistical methods 12 (a) Describe all statistical methods, including those used to control for confounding 9-10

(b) Describe any methods used to examine subgroups and interactions 9-10

(c) Explain how missing data were addressed

(d) If applicable, explain how loss to follow-up was addressed

(e) Describe any sensitivity analyses

Results

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Participants 13* (a) Report numbers of individuals at each stage of study—eg numbers potentially eligible, examined for eligibility, confirmed

eligible, included in the study, completing follow-up, and analysed

5

(b) Give reasons for non-participation at each stage 5

(c) Consider use of a flow diagram 5

Descriptive data 14* (a) Give characteristics of study participants (eg demographic, clinical, social) and information on exposures and potential

confounders

5-7

(b) Indicate number of participants with missing data for each variable of interest

(c) Summarise follow-up time (eg, average and total amount) 5

Outcome data 15* Report numbers of outcome events or summary measures over time 5-9

Main results 16 (a) Give unadjusted estimates and, if applicable, confounder-adjusted estimates and their precision (eg, 95% confidence

interval). Make clear which confounders were adjusted for and why they were included

11-13

(b) Report category boundaries when continuous variables were categorized

(c) If relevant, consider translating estimates of relative risk into absolute risk for a meaningful time period

Other analyses 17 Report other analyses done—eg analyses of subgroups and interactions, and sensitivity analyses 11-13

Discussion

Key results 18 Summarise key results with reference to study objectives 14

Limitations

Interpretation 20 Give a cautious overall interpretation of results considering objectives, limitations, multiplicity of analyses, results from

similar studies, and other relevant evidence

2 and 16

Generalisability 21 Discuss the generalisability (external validity) of the study results 2

Other information

Funding 22 Give the source of funding and the role of the funders for the present study and, if applicable, for the original study on

which the present article is based

18

*Give information separately for cases and controls in case-control studies and, if applicable, for exposed and unexposed groups in cohort and cross-sectional studies.

Note: An Explanation and Elaboration article discusses each checklist item and gives methodological background and published examples of transparent reporting. The STROBE

checklist is best used in conjunction with this article (freely available on the Web sites of PLoS Medicine at http://www.plosmedicine.org/, Annals of Internal Medicine at

http://www.annals.org/, and Epidemiology at http://www.epidem.com/). Information on the STROBE Initiative is available at www.strobe-statement.org.

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For peer review only

A NORWEGIAN PROSPECTIVE STUDY OF PRETERM MOTHER-

INFANT INTERACTIONS AT SIX AND 18 MONTHS AND THE

IMPACT OF MATERNAL MENTAL HEALTH REACTIONS,

PREGNANCY AND BIRTH COMPLICATIONS

Journal: BMJ Open

Manuscript ID bmjopen-2015-009699.R1

Article Type: Research

Date Submitted by the Author: 19-Oct-2015

Complete List of Authors: Misund, Aud R; University College of Oslo and Akershus, Health science Bråten, Stein; University of Oslo, Dept. of Sociology and Human Geography Nerdrum, Per; University College of Oslo and Akershus, Health science Pripp, Are; Oslo University Hospital, Department of Biostatistics, Epidemiology & Health Economy Diseth, Trond; Oslo University Hospital and University of Oslo, Department of Clinical Neurosciences for Children, Women and Children’s Division and Department of Medicine

<b>Primary Subject Heading</b>:

General practice / Family practice

Secondary Subject Heading: Mental health, Obstetrics and gynaecology, Reproductive medicine, Paediatrics

Keywords: Neonatal intensive & critical care < INTENSIVE & CRITICAL CARE, MENTAL HEALTH, Maternal medicine < OBSTETRICS, PERINATOLOGY, TRAUMA MANAGEMENT, Child & adolescent psychiatry < PSYCHIATRY

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1

A NORWEGIAN PROSPECTIVE STUDY OF PRETERM MOTHER-

INFANT INTERACTIONS AT SIX AND 18 MONTHS AND THE

IMPACT OF MATERNAL MENTAL HEALTH REACTIONS,

PREGNANCY AND BIRTH COMPLICATIONS

Aud R. Misund

1 Stein Bråten

Per Nerdrum

Are Hugo Pripp

Trond H. Diseth

ABSTRACT

Objective:

Pregnancy, birth and health complications, maternal mental health reactions following

preterm birth and their possible impact on early mother-infant interaction at six and 18

months corrected age (CA) were explored. Predictors of mother-infant interaction at 18

months CA were identified.

Design and methods:

This prospective longitudinal and observational study included 33 preterm mother-infant (<33

GA) interactions at six and 18 months CA from a socio-economic low risk middle class

sample. The parent-child early relational assessment scale (PCERA) was used to assess the

mother-infant interaction.

Results:

Mothers with case scores in the Impact of Event Scale, the General Health Questionnaire, the

Spielberger State/Trait Anxiety Inventory and PTSR/PTSD diagnosis at two weeks

postpartum (PP) showed significant better outcome than mothers without case scores in six

and two PCERA subscales at six months and 18 months CA, respectively.

“Bleeding in pregnancy” predicted lower quality in preterm mother-infant interaction in six

PCERA scales, while high “Maternal trait anxiety” predicted higher interactional quality in

1 Faculty of Health Sciences, University College of Oslo and Akershus and Department of Medicine, Institute of

Clinical Medicine, University of Oslo, adr: PO Box. 4 St. Olavs plass, N-0130 Oslo, Norway e-mail:

[email protected]

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two PCERA scales and “Family size” predicted lower interactional quality in one PCERA

scale at 18 months CA.

Conclusions:

Our study detected a correspondence between early pregnancy complications and lower

quality of preterm mother-infant interaction, and an association between high levels of

maternal mental health problems and better quality in preterm mother-infant interaction.

Strengths and limitations of this study:

The longitudinal design, the high response rate and the use of well-validated psychometric

instruments and interactional assessment tool are strengths in this study.

Fifty percent of the attending women received psychological treatment during the study and it

is a limitation that the influence of the psychological treatment on our study results was not

assessed.

The present study and describes a small preterm group and one should be cautious about

generalising from this study.

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INTRODUCTION

Early parent-infant relationships that are well functioning seem to be critical to

preterm children. Preterm children face severe risk of cognitive, emotional, and behavioural

disorders ,[1-8] and show more psychiatric symptoms in adolescence.[9] Early parent-infant

relationships that are well functioning seem to prevent and restore some of these difficulties in

preterm children.[10, 11]

Good quality in mother-child interactions have been reported to facilitate the infant’s

emotional, behavioural, cognitive, and neurobehavioral development.[12-17] The

interactional quality is also found to be related to the child’s physical health.[18, 19]

Compared with infants born at term the preterm infants are likely to show vague signals that

are difficult to read and respond to and are in need of extended care and support to gain self-

regulation. [20, 21] These traits, as well as parent’s psychiatric disease are known as risk

factors for good quality parent-infant interactions.[22, 23] Research detected significant

higher mental health reactions following preterm birth than term birth.[24-26]

The maternal stress reaction following preterm birth has been highlighted as a risk

factor in preterm dyads in several studies.[24-29] Postpartum depression has been identified

as predictor for interactional difficulties in term dyads[30] and reported as a risk factor for

difficulties in preterm mother-infant dyads.[31] Only a limited number of studies, however,

have explored the nature of mothers’ mental health reactions following preterm birth with

psychometric tools, and their impact on mother-infant interaction. Several studies, however,

have explored the postterm effect on maternal mental health.[32-36] Blom et al. interestingly

reported that certain perinatal complications such as preeclampsia, hospitalization, emergency

caesarean, and fetal distress predicted higher depression outcomes in a normal population

sample. An unaddressed trauma reaction is known to predispose for posttraumatic stress

disorder (PTSD) with long term effects on mothers’ mental health. The effect of mothers

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postpartum PTSD on mother-infant interaction and infant’s development is less explored.[37]

In addition only a limited number of studies have explored the maternal posttraumatic stress

responses following preterm birth[38-45] and their impact on mother-infant interactions.[20,

42, 46]

The results from preterm mother-infant interaction research are contradictory.

Different measurements and definitions being used, as well as the complexity of mother-

infant interactional studies may have contributed to these differences. Some studies have

reported that preterm mothers showed more stimulating behaviour and were emotionally

withdrawn, as well as non-synchronous in their interaction with the child,[20, 47-53] and

others have found no interactional differences between preterm and full term dyads.[20, 54-

59] Korja et al. detected that caregivers’ physical closeness with the infant was more

important to interactional quality than infants’ prematurity.[57] Finally, it is interesting that

several studies have shown that mothers are intensifying their efforts to be available and

supportive to their premature babies’ needs.[60-65] Preterm birth is reported to influence the

interaction between mother and infant.[20, 66, 67] The knowledge of risk factors that may

affect preterm mother-infant interaction is limited. [31, 68-70]The need for further exploration

of the complexity of factors influencing the early mother-infant relationship long-term in

preterm dyads seems essential.[6, 71]

The aim of our longitudinal study was to explore the possible influence of maternal

mental health reactions following preterm birth, pregnancy and birth complications, and their

impact on early preterm mother-infant interaction at six months PA and 18 months CA.

The first aim of our longitudinal study was to explore the associations between maternal

mental health reactions following preterm birth, pregnancy and birth complications, and early

preterm mother-infant interaction at six months PA (T2) and 18 months CA (T3). The second

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aim of the study was to identify predictors of early mother-infant interaction quality at T2 and

T3.

To our knowledge, these associations have not been explored in other studies.

Psychometric tools and tentative psychiatric diagnosis (anxiety, depression, and PTSR/PTSD)

were used to assess maternal mental health reactions following preterm birth.

It should be noted that this paper is an extension of our previous studies of short- and

long-term maternal mental health reactions following preterm birth.[44, 45]

METHOD

Participants

Data were collected in two periods: June 2005-January 2006 and October 2007-July

2008. The psychological responses of 29 consecutive mothers of 35 premature children born

before 33rd week of pregnancy were assessed at a high-specialized neonatal intensive care unit

(NICU) at Oslo University Hospital, Norway. Mothers of severely ill babies that the medical

staff estimated to have poor chance of survival, and non-Norwegian speakers were not

included. The participants stayed in NICU till they were discharged for home. The parents

could participate in the caring of the infant during hospitalisation. The data collection was

performed as soon as the mothers were able to attend an interview following preterm

childbirth: within two weeks postpartum (T0) median 11 days (4-30); then within two weeks

after hospitalization (T1), median time postpartum 2.7 months (0.2-4.7); then at the infant’s

six months corrected age (T2), median time postpartum 8.5 months (7.6-10.4); and at the

infant’s 18 months corrected age (T3), median time following birth 20.6 months (19.2-23.4).

Data collection of mother-infant interaction was collected only at T2 and T3. Mothers of

severely ill babies with uncertain survival and non-native speakers were not included (Figure

1).

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FIGURE 1 ABOUT HERE

Semi-structured interviews and standardized mental health screening questionnaires

were used to collect data about socio-demographics, the pregnancy and birth, child’s health

status, and mothers’ mental health reactions. Medical charts were used to double-check the

data of child’s health status, and pregnancy and birth. The studied sample was homogeneous

regarding high scores on socio-demographic variables such as education, income, and housing

standard. Most mothers were giving first time birth late in their twenties or early thirties. All

lived with the child’s father and none reported any relationship problems (Table 1).

The participating mothers’ mental health reactions following preterm birth have

been assessed at T0, T1, T2, T3 and methods and results are described in detail in our earlier

papers.[44, 45] Maternal mental health problems were assessed at every time points (T0, T1,

T2, T3) by standardized psychometric methods with well-established reliability and validity:

Impact of Event Scale (IES) 15-item version, one of the key psychometric assessment

methods in traumatic stress research,[72, 73] the General Health Questionnaire (GHQ) 30-

item version, a widely used screening instrument for assessing the presence of distress,

psychopathology and overall well-being,[74, 75] and the State/Trait Anxiety Inventory

(STAI-X1/X2)[76] is widely used to assess maternal anxiety. STAI-X1 measures state anxiety

levels reflecting subjective feelings of tension, apprehension, nervousness and worry. STAI-

X2 is a measure of trait anxiety that refers to individual differences in anxiety proneness, i.e.

in the tendency to see the world as dangerous and threatening, and the frequency with which

anxiety states are experienced. Scores above the threshold for identifying a psychiatric case is

referred to as a case score.

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Based on all information available in a clinical perusal of the psychometric self-reports

IES, GHQ and STAI of each of the 29 preterm mothers, and blinded to the physical and socio-

demographic characteristics of the mothers and their children, a tentative clinical diagnosis

was made where appropriate based on the clinical descriptions and diagnostic guidelines in

the ICD-10 Classification of mental and behavioural disorders, and was assessed by a

psychiatrist (last author).

A prevalence of maternal posttraumatic stress responses/disorders (PTSR/PTSD) two

weeks postpartum (T0) of 52% and maternal PTSD at 18 months corrected age (T3) of 23%

was revealed. On the other hand, depression was detected among 24 % of the mothers two

weeks postpartum and among 8% of the mothers at T3. Anxiety decreased from 7% at two

weeks postpartum to zero at T3.

Fourteen of the mothers received psychological support at the hospital during their

infants’ NICU stay. Eleven of these mothers were referred for further psychological treatment

after discharge from the hospital. Altogether, 20 mothers that met the criteria of clinical

diagnoses were referred for adequate psychological treatments such as psychotherapy,

psychopharmacology treatment, and mother-infant interactional treatment. Five of the

mothers refused the referral for psychological treatment, and only one of them filled the

criteria for a tentative clinical diagnosis (PTSD/Depression) at T3. The prevalence of

pregnancy and birth complications and maternal mental health reactions following preterm

birth are reported in earlier papers.[44, 45]

Data collected at 2 weeks postpartum (T0) about sociodemographics, physical

complications and maternal mental health reactions following preterm birth are presented in

Table 1.

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Table 1. Socio-demographic, physical characteristics, and mental health variables in mothers

giving preterm birth and their children at two weeks postpartum (T0).

Mothers n=29

Age; mean (SD) 33.7 (4.3)

Education > 12 years; n (%) 26 (89.7)

Single parent; n (%) 0 (0)

Unemployed; n (%) 4 (13.8)

Previous psychological treatment; n (%)

8 (27.6)

Chronic illness; n (%) 2 (6.9)

Tot. no. of children; median (quartile low,upper) 2 (1,2)

Previous pregnancies; median (quartile low,upper) 1 (0,2)

Previous childbirths; median (quartile low,upper) 0 (0,1)

First time mothers; n (%) 18 (62.1)

IVFa pregnancy; n (%) 8 (27.6)

Bleeding in pregnancy; n (%) 19 (65.5)

Preeclampsia; n (%) 4 (14.3)

Caesarean; n (%) 17 (58.6)

Mental Health Variables:b

IES total (0-75); median (quartile low,upper) 18 (11,30)

IES case score >18; n (%) 13 (44.8)

GHQ Likert score (0-90); n (%) 40 (15.4)

GHQ case (0-30): n (%) 12.8 (7.5)

GHQ case score >5; n (%) 23 (79.3)

STAI-X1 (0-40); mean (SD) 21.5 (2.8)

STAI-X1 case score >19; n (%) 20 (69)

STAI-X2 (0-80); mean (SD) 44.0 (4)

STAI-X2 case score >39; n (%) 27 (93.1)

PTSR Tentative clinical diagnosis; n (%) 15 (51.7)

Children n=35

Girl; n (%) 17 (48.6)

Boy; n (%) 18 (51.4)

Twinc; n (%) 14 (40)

Gestational age (weeks);

Median (range)

Mean (SD)

29 (24-32)

28.5 (2.6)

Birth weight (g);

Median (range)

Mean (SD)

1185(623-2030)

1222(423)

Apgar score at 1 minute; mean (SD) 6,3 (2.3)

Apgar score at 5 minute; mean (SD) 7.6 (2.0)

Apgar score at 10 minute; mean (SD) 8.3 (1.0)

Oxygen supply > 28 days; n (%) 19 (54)

IVHd; n (%) 7 (20.0) a In vitro fertilization/Assisted fertilization.

bThe Impact of Event Scale (IES) 15 item with scoring range 0(not at all) to 5 (very much), The General Health Questionnaire (GHQ)30 items

Likert scores with weights 0-1-2-3 and case scores with weights 0-0-1-1, The Spielberger State/Trait Anxiety Inventory (STAI-X1/X2) 10

item/20 item with scoring range 1-2-3-4. The STAI-X1 10 item was constructed since both STAI-X1 12 item and 20 item had been used and

only 10 items overlapped. Tentative Clinical Diagnosis: Posttraumatic Stress Responses (PTSR). cTwo of the twins were raised as singleton as their twin sibling were stillborn.

dIntraventricular hemorrhage grade 1-4 following birth.

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Measures

Mother–infant interaction in a free-play situation was video recorded at six and 18

months CA. According to Clark (1985) by six months of age, dyadic mutuality and dyadic

regulatory processes are perceptible while at 18 months, the infant's own communication

skills are easier to identify in interaction [77]. The interaction situation was recorded in a

consultation room at the psychiatric clinic for children and families situated in the same

building as the hospital the children were born in, except for four video recordings at 18

months CA that were recorded in their homes. The recordings were performed when child

was awaken and interested in a play session with mother. Recordings were stopped and

performed later when child became too distressed or sleepy to play. A therapist (first author)

instructed the mothers about the procedure. For the video recording, the mother and the infant

were placed on a soft mat with age-appropriate toys. Instructions by the investigators given to

the mother prior to the video recording were: ‘This is a free-play time with your child. You

can use the toys, or you can play without the toys. Try to play or be with your infant as you

usually would be”. Video recordings were obtained from all mother-infant pairs.

The recordings were five minutes long. The mother-infant interaction in the free-play

situation was analysed using the Parent-Child Early Relational Assessment (PCERA)

method.[77] The PCERA is developed to assess affective and behavioural aspects that both

the parent and infant bring into the interaction,[77] and the validity of the free play situation

has been established.[78, 79] Video recordings allows thoroughly analysis of the interactions

several times and in short and slow sections that can identify areas of strength and of concern

in the mother-infant interplay. The PCERA consists of 29 parental items, 28 infant items and

eight dyadic items. The assessment rates the frequency, duration and intensity of the infant's,

parent's and dyad's behaviour. The parental items comprise the parent's positive and negative

affect, expressed attitude toward the infant, sensitivity and contingent response to the infant's

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cues, mirroring the infant's feeling, capacity to structure, behavioural involvement and

parental style. The infant items comprise expressed positive and negative affect and

characteristic mood, behaviour/adaptive abilities, activity level and communication skills. The

dyadic items comprise affective quality of interaction and mutuality of interaction.

All items were rated on a 5-point “Likert” scale. The scores 1 and 2 describe an area of

concern, the score 3 describes an area of some concern and the scores 4 and 5 describe an area

of strength. A trained coder made the assessment. The coder was unaware of the infant's

background and clinical status. Additionally, to estimate the interrater reliability from the

study data, 20% of all assessments were double-scored by another trained coder. The study

data was assessed by calculating the mean of the agreement percentage of the raters' overall

agreement. Agreement equal or above 80% is considered good, 50-80% is considered

moderate, and lower than 50% is considered poor. The mean of interrater agreements was

80.3% in six months CA and 81% in 18 months CA.

The PCERA items were organized in eight scales according to Clark [77] before the

data analysis: “Maternal positive affective involvement PS1”, “Maternal negative affect &

behaviour PS2”, “Maternal intrusiveness PS3”, “Infant positive affect PS4”, “Infant quality

of play PS5”, “Infant dysregulation PS6”, “Dyadic mutuality & reciprocity PS7”, and “Dyadic

disorganization & tension PS8”. PCERA high scores (4-5) always indicate positive affect and

behaviour or lack of negative affect and behaviour. The Cronbach alpha coefficients for

calculating the internal consistency of PCERA subscales in our study were satisfactorily and

were .95,.86,.86, .90,.87,.85,.80,.86 for PS1-PS8 at six months CA (T2), and

.89,.81,.82,.92,.89,.75,.73,.79 for PS1-PS8 at 18 months CA (T3).

The PCERA scale has been used in several studies to explore the quality of preterm

mother-infant interactions.[31, 80-84]

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Statistical methods

Values of continuous variables are presented as means (SD) or if skewed, as median

and range. Categorical variables are given as proportions and percentages. Paired-sample t-

test was used for comparison of the PCERA means scores at T2 and T3. Differences in the

quality of mother-infant interactions measured by the PCERA scales were explored with

independent-samples t-test. As grouping variable we used mothers’ case scores (0=no, 1=yes)

in IES, GHQ, STAI and the tentative diagnostic assessments at four time points; two weeks

PP (T0), two weeks after hospitalization (T1), six months CA (T2), and 18 months CA (T3)

(Figure 2). A more detailed description of mothers’ case scores in IES, GHQ, STAI and the

tentative diagnostic assessments are available in our earlier papers.[44, 45]

The correlations between normally distributed and continuous variables at T3 in

correlation analysis were measured using Pearson’s correlation coefficient or Spearman’s

correlation coefficient when the variables had a skewed distribution (Table 2).

Forward linear regression analysis was used to identify possible predictors of the PCERA

results at T3 (Table 3). The three variables at T3 with the strongest bivariate associations

(<0.05) were included in the multivariable linear regression model; PS1 (STAI-X2 case,

STAI-X2 sum, GHQ Likert), PS2 (Bleeding in pregnancy, GHQ case, GHQ Likert), PS3

(STAI-X2 case, Bleeding in pregnancy, Parity/STAI-X2 sum), PS4 (Bleeding in pregnancy),

PS5 (Bleeding in pregnancy, Apgar 5 min), PS6 (Family size, Acute Caesarean), PS7

(Bleeding in pregnancy, GHQ case), and PS8 (Bleeding in pregnancy, GHQ case). A careful

check of the model assumptions, including an investigation of residual plots, did not reveal

any violation of the assumptions. All analyses were performed in SPSS version 20. Two-sided

statistical tests were applied and a 5 % statistical significance level was chosen.

Ethics

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Written informed consent was obtained from participants prior to the study start. The

study protocol was approved in 5 May 2005 and 19 April 2007 by the National Committee for

Research Ethics (S-05068 and S-07096b) and 1 April 2005 and 12 March 2007 by the Data

Inspectorate (12360 and 07/1088). The study protocol was carried out in accordance with the

Declaration of Helsinki.

For ethical reasons the mothers that reported mental health problems and had case

scores above the threshold for identifying a psychiatric case in IES, GHQ and STAI were

assessed and referred for adequate psychological treatment. In this study, we looked for

mental health problems in mothers at four points from the time of birth to two years

postpartum. A no referral procedure could have caused unnecessary suffering for both

mothers and children.

RESULTS

Associations between maternal mental health reactions following preterm birth,

pregnancy and birth complications, and early preterm mother-infant interaction at six

months PA (T2) and 18 months CA (T3)

The paired sample t-test of the results of the PCERA showed no significant difference

for the PCERA mean scores from six months to 18 months corrected age (CA). For that

reason the presented results from correlation and regression analysis are based only on the

mean scores from 18 months CA. The results of the PCERA revealed mean scores in three of

the scales in the area of moderate concern and five scales in the area of no concern. The

results of the PCERA is presented in Table 2.

Group differences in mother – infant interaction quality at T2 and T3 for mothers with and

without psychometric case scores at T0, T1, T2, and T3

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The results of the independent-samples t-test showed significant group differences at

T2 and T3 between the mothers with case scores above the threshold for identifying a

psychiatric case compared to mothers without case scores in IES, GHQ, and tentative PTSR

diagnosis at T0 (Figure 2). Mothers’ with case scores at T3 in GHQ also showed significant

better results at the .05 level (2-tailed)* in two PCERA scales at T3; PS7 Dyadic mutuality

and reciprocity (N0/N1=24/8, mean 3.1/3.7*), and PS8 Dyadic disorganization and tension

(N0/N1=24/8, mean 3.9/4.4*). Most unexpectedly, the mothers with case scores (1=yes) at T0

showed significantly better quality in mother-infant interaction in six (T2) and two (T3)

subscales of the PCERA than mothers with no (0=no) case scores (Figure 2). Tentative

depression or anxiety diagnosis (0=no, 1=yes) as a grouping variable showed no significant

group differences regarding the quality of the mother-infant interaction.

FIGURE 2 ABOUT HERE

Associations between maternal mental health reactions and mother-infant interactional

quality at T3

In the bivariate correlation analyses, we revealed a positive correlation between better

interactional quality measured by PCERA and higher levels of maternal mental health

reactions measured by psychometric means at T3. High levels of GHQ Likert and case scores

correlated with high levels of PCERA scores in three scales and GHQ case sum scores

correlated with two scales. High levels of STAI-X2 sum scores were associated with high

levels of PCERA scores in two scales and case scores correlated with three scales (Table 2).

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Associations between pregnancy/ birth complications, maternal variables and mother-infant

interactional quality at T3

The strongest correlations were inversely and found between a pregnancy

complication “Bleeding in pregnancy” and the following six PCERA scales: “Maternal

negative affect and behaviour (PS2), Maternal intrusiveness, intensity, and inconsistency

(PS3), Infant positive affect, communicative, and social skills (PS4), Infant quality of play,

interest, and attention (PS5), Dyadic mutuality and reciprocity (PS7), and Dyadic

disorganization and tension (PS8)”.

Two infant complications following birth were correlated with two of the PCERA

scales. Infant health scores at the infant’s “Apgar scores at 5 minutes postpartum” correlated

positively with the “Infant quality of play, interest, and attention (PS5)” scale. Infant stroke by

“Intraventricular Haemorrhage grade 1 or 2 (IVH)” closely following birth” correlated

inversely with the “Maternal negative affect and behaviour (PS2)” scale (Table 2).

Three maternal variables correlated with two of the PCERA scales. Parity (number of

previous births with child survival) and the scale “Maternal intrusiveness, intensity and

inconsistency (PS3)” were positively correlated. Family size (number of children in the

family) and the “Infant dysregulation and irritability (PS6)” scale inversely correlated. “Acute

caesarean” correlated positively with high scores on the same scale.

Associations between exposure variables, e.g. IVF treatment, pre-and postnatal

maternal health problems and pregnancy and birth/ postnatal complications, were not

significant.

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Table 2. Bivariate correlations at T3 (18 months corrected age) between the PCERA scales, the maternal

psychometric means, and the individual characteristics of the mothers and infants. Pearson’s correlation

coefficients (p<.05) are reported. (N=32). Mean values, range scores and minimum and maximum scores

for PCERA subscales are reported in the last row of this table.

PCERA

PS1

Maternal

Positive

affective

involve-

ment

PCERA

PS2

Maternal

Neg.

affect &

behav.

PCERA

PS3

Maternal

Intrusive-

ness

In-

sensitivit

y

Inconsist

-ency

PCERA

PS4

Infant

Positive

affect

Commun-

icative

& social

skills

PCERA

PS5

Infant

Quality of

play

Interest

Attention

PCERA

PS6

Infant

Dysregu-

lation

Irritabil-

ity

PCERA

PS7

Dyadic

Mutuali

ty

Reci-

procity

PCERA

PS8

Dyadic

Disorgan

-ization

Tension

GHQ Likert

sum score

.39*

.37*

.35* .16 .12 .05 .30 .28

GHQ case

sum score

.36* .36* .06 .12 .07 .17 .26 .31

GHQ

case > 5

.26 .40* .30 .33 .29 .21 .41* .43*

STAI-X2

sum score

.46** .21 .39*

.09 -.03 .08 .25 .19

STAI-X2

case > 39

.48* .36* .57** .19 .06 .07 .32 .32

Parity

.07

.18 .39* .24 .10

.01

.31 .33

CH< grade

3a

-.21 -.28 -.35* -.20 -.23 -.15 -.30 -.35

Apgar

at 5

minutes

-.01 .09 .20 .22 .35* -.12 .18 .19

Bleeding in

pregnancy

-.22 -.45** -.56** -.53** -.55** -.33 -.46** -.52**

Family

sizeb

-.09 -.12 .07 -.02 -.16 -.45* .01 .00

Acute

Caesarean

.14 .14 .13 .01 .03 .39* .07 .22

Mean/

Range c (Min-Max)

3.8/2.5

(2.3-4.8)

4.6/1.6

(3.4–5.0)

4.2/2.0

(3.0–5.0)

3.2/3.0

(1.9–4.9)

4.0/2.2

(2.7–4.9)

4.5/1.3

(3.7–5.0)

3.3/2.8

(2.0–

4.8)

4.0/2.0

(3.0–

5.0)

*Correlation is significant at the .05 level (2-tailed). **Correlation is significant at the .01 level (2-tailed). a CH< grade 3 refers to Cerebral Hemorrhage grade 1 or 2 closely after birth.

b Family size refers to the number

of children in the family. c Rates 1 and 2 in PCERA subscale; “Area of concern”. Rate 3 in PCERA subscale; “Area of moderate concern”.

Rates 4 and 5 in PCERA subscale; “Area of no concern”.

Predictors of mother-infant interactional quality at T3

In the multiple linear regression analyses we revealed that the pregnancy complication

variable “Bleeding in pregnancy” was a significant predictor (p<0.01) of lower scores in

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preterm mother-infant interaction in six of the PCERA domains, including both of the Dyadic

scales (Table 3). Trait anxiety (STAI-X2) case and sum score are significant predictors for

higher quality in preterm mother-infant interaction in the “Maternal positive affect domain

(PS1)” (p<0.01) and in the “Maternal intrusiveness (PS3)” domain (p<0.05), consecutively.

Higher “Number of children in the family” predicts lower interaction quality in the “Infant

dysregulation and irritability (PS6)” scale (p<0.05). Adjusted R2 showed that the predictors

explain from 17 to 39 % of the variance in different PCERA scales.

Table 3. Forward entry multiple regression analyses predicting mother-child interaction

outcomes for PCERA in preterm mother–child dyads at T3 (18 months corrected age).

Unstandardized (B) and standardized (Beta) regression coefficients. (N=32)

Predicting variable B CI Beta P-

value

R2

adj.

PCERA subscales:

PS1 (Maternal positive

affective involvement)

STAI-X2 case .53 (.17, .89) .48 .005 .21

PS2 (Maternal negative

affect & behavior)

Bleeding in pregnancy -.21 (-.37, -.06) -.45 .009 .18

PS3 (Maternal

intrusiveness)

Bleeding in pregnancy

STAI-X2 sum score

-.29

.03

(-.45, -.13)

(.01, 06)

-.53

.35

.001

.017

.39

PS4 (Infant positive

affect)

Bleeding in pregnancy -.43 (-.68, -.17) -.53 .002 .26

PS5 (Infant quality of

play)

Bleeding in pregnancy -.35 (-.56, -.15) -.55 .001 .27

PS6 (Infant

dysregulation)

Family size

-.24

(-.42, -.06)

-.45

.011

.17

PS7 (Dyadic mutuality &

reciprocity )

Bleeding in pregnancy

-.33

(-.56, -.09)

-.33

.008

.21

PS8 (Dyadic dis-

organization & tension)

Bleeding in pregnancy

-.32

(-.51, -.12)

-.52

.002

.25

PCERA subscales were used as dependent variables (Three variables with strongest bivariate association (<0.05) was used as

independent variables);

PS1 (STAI-X2 case, STAI-X2 sum score, GHQ Likert sum score), PS2 (Bleeding in pregnancy, GHQ case, GHQ Likert sum

score),PS3 (STAI-X2 case, Bleeding in pregnancy, Parity/STAI-X2 sum score), PS4 (Bleeding in pregnancy),

PS5 (Bleeding in pregnancy, Apgar at 5 minutes), PS6 (Family size, Acute Caesarean),

PS7 (Bleeding in pregnancy, GHQ case), PS8 (Bleeding in pregnancy, GHQ case).

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DISCUSSION

The study revealed significant associations between pregnancy and birth

complications, maternal postpartum mental health, and the quality of preterm mother-infant

interaction. The most surprising results in our study were the detection of “Bleeding in

pregnancy” as a predictor of lower quality in preterm mother-infant interaction in six of eight

PCERA scales, and the association between high levels of maternal mental health problems

and better mother-infant interactional quality. We should keep in mind that the results from a

small and explorative study have low statistical power. In most studies there also is a

possibility that confounding variables are not included in the analysis that should have been.

In our study that could have been assessment of mothers’ attachment patterns, the effect of

psychological assessment and referral procedure and an assessment of the comforting

conditions for mother-infant interactions in the hospital for instance. However, our study

results may be of value for future research that will systematically explore the complexity of

factors influencing early preterm mother-infant interaction in a broader sense.

The predictor “Bleeding in pregnancy” is profoundly interesting. No other study has,

to our knowledge, revealed a physical complication in pregnancy that predicts the quality of

the preterm mother-infant interaction. In a previous paper, we detected that “Bleeding in

pregnancy” was a predictor of low levels in maternal mental health reactions, while

“Preeclampsia”, which is a sudden complication later in pregnancy, predicted high levels of

maternal mental health reactions following preterm birth. “Bleeding in pregnancy” could be

experienced as an early warning sign for possible pregnancy complications as it usually

occurs before 22 weeks of pregnancy. “Bleeding in pregnancy” may therefore affect how

mother relates to her unborn child and how her transition into motherhood alternates.

Two questions now arise; is it possible to provide an existential explanation of why “Bleeding

in pregnancy” contributes to low levels of PCERA scores in preterm mother-infant

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interaction? Could it be that the mother-to-be feels “Bleeding in pregnancy” as a near-loss

experience leaving her with the frightening impression that her child is at risk (in which case

the preterm birth confirms the fear of loss)? Given such an enduring threatening impression,

the mother can be expected to be anxious and alert, preventing her from relaxing and taking

pleasure in the mother-infant interaction, and rather inviting negative affect and intrusiveness

which may also entail dyadic disorganization and tension. The greatest responsibility nature

has given us is to secure survival of our offspring Daniel Stern argues.[85]

A mother experiencing a sudden preterm birth with infant survival and no serious early

warning signs is likely to have been quite “undisturbed” in her transition process to prepare

for motherhood. A preterm birth may represent a very dangerous situation for both mother

and child where both may have risked death. When mother experiences hope for survival, we

may assume that a prior “undisturbed” transition process into motherhood is likely to increase

her efforts to attain the very best mother-infant interaction.

Attachment theory supports our hypothesis that loss or possible loss can be seen as serious

threats to attachment.[86] Attachment theory may also contribute with an alternative

explanation of our results. There is a growing number of research that show that mothers’

attachment pattern is associated with the mother-infant interaction.[87, 88] In our study,

however, attachment assessment were not explored.

Most unexpectedly, our results showed that high levels of maternal mental health

problems following preterm birth were associated with better quality in preterm mother-infant

interaction. In regression analysis, we found that high levels of maternal trait anxiety (STAI-

X2) scores predicted better scores in two PCERA scales at T3. In the independent-samples t-

test, we revealed that mothers with case scores on IES, GHQ, STAI and the tentative

diagnoses of PTSR/PTSD at 2 weeks postpartum (T0) showed significantly better quality in

mother-infant interaction on six PCERA scales at six months (T2) and on two PCERA scales

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at 18 months corrected age (T3). The STAI trait’s association with general psychological

distress following preterm birth has been reported in our previous papers.[44, 45] In addition,

the STAI trait’s association with posttraumatic stress following term birth has also been

reported by another study.[89]

It is theoretically interesting that our results imply that high levels of maternal mental

distress improve the preterm mother–infant interaction. At first glance, this result seems to

contradict the well-known connection between high levels of maternal depression and high

risk mother-infant interactions.[31, 90-92] It should be noted that we found quite low

prevalence of depression among the mothers participating in this study.[44, 45] Instead, we

found high levels of posttraumatic stress reactions. PTSD following childbirth is

acknowledged by several researchers to be potentially different from PTSD following other

traumatic incidences.[37] The culturally positive connotation of giving birth, the mother-child

connection, the transition from pregnancy to birth, and the formal care setting the birth

incident takes place in are all matters that may have an impact on PTSD following preterm

birth. Several studies have reported that many people experience positive psychological

growth after struggling with trauma.[93] Maternal posttraumatic stress reaction following

preterm birth is characterized by a prior physical trauma where survival of the mother and the

baby may be at risk. Is it possible that maternal posttraumatic stress reactions following

preterm birth helps the mother to focus her attention towards her premature baby’s wellbeing?

Our results may imply that the posttraumatic stress response activates and helps the mother

cope over time with a tremendously stressful situation, and furthermore helps her stimulate

the prematurely born child’s healthy development. Several studies support our view.[61-63,

65] Other studies that have explored maternal mental health reactions following preterm birth

and preterm mother-child interactions have reported results that contrast with our own.[42, 51,

83, 94] Studies that have used the PCERA scale in studying preterm dyads, however, did not

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find depression to be a significant predictor of PCERA outcome at six, 12, or16 months

CA.[31, 81] On the other hand, they reported that high infant heart rate variety (HVR) after

feeding,[82] and higher frequency of naps had a positive impact on preterm mother-infant

interaction.[84]

The socio-demographic variable “Family size” predicted low interactional quality in

one of the PCERA scales. In our study, the mothers with preterm babies that had siblings

showed significantly lower scores in the “Infant dysregulation scale (PS6)” in the PCERA.

Our result is supported by two studies in the 1970’s and 1980’s that found the preterm infant’s

birth-order to affect the mother-child interaction.[95, 96] An explanation for their results was

the mother’s divided attention between the infant and other siblings.

Strength/limitations

The participants in this study came from well-defined geographic areas and both single

and multiple births were included consecutively in the study, thus minimizing selection bias.

Our sample was homogeneous in socio-economic background (SES).The mothers had higher

educational attainments, greater age and higher socioeconomic status, higher number of twins

and higher rate of previous psychological treatment than would be found in a typical

population of mothers who deliver preterm in our country. In this sample we found no

indication of significant differences in parental challenges between participants with

singletons or twins that needed to be addressed in the analysis. Besides the high prevalence of

earlier psychological treatment among the mothers in our sample, no other collected data

gave indication for mental distress having an impact on their psychosocial function in

everyday life before the actual preterm birth incident. Regarding research on quality of the

preterm mother-infant interaction, it has been considered that risk factors other than preterm

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birth itself may have created bias / been sources of bias in many studies [20, 49, 97]. In our

study, we have controlled for high risk socio-economic backgrounds.

It is a limitation that the video-procedure of PCERA could not be followed for the four

dyads that were recorded in their homes and not in the clinic, as were the others. On the other

hand, these dyads would not have participated if the recordings were not made in their homes.

It is a limitation that interrater reliability was not checked for tentative clinical diagnosis. The

prediction model used in this study needs further validation by future studies.

CONCLUSIONS

Our results imply that pregnancy complications occurring early in the pregnancy may

affect the bonding process between the mother and her preterm infant long term. Early

intervention programs should be offered to mothers with early pregnancy complications to

support mother-infant interaction.

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Acknowledgements

The authors would like to thank the families that participated in the study, the staff of the

maternity ward at the neonatal intensive care unit at the National Hospital, Oslo and Sari

Ahlqvist-Björkroth who coded and Tanja Lipasti who recoded the PCERA data. In particular,

we want to thank the parents who participated in the study.

Contributorship statement

ARM initiated the study, collected, and organized the data. ARM and AHP performed the

statistical analyses. ARM, PN, SB, AHP and THD wrote the article.

Competing interests

We have no information of disclosure of interests.

Funding

This work was supported by the Centre for Child and Adolescent Mental Health, Eastern and

Southern Norway and the University College of Oslo and Akershus.

Data sharing statement

The full dataset is available from the corresponding author Aud R.

Misund([email protected]).

REFERENCES

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209x297mm (300 x 300 DPI)

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209x297mm (300 x 300 DPI)

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209x297mm (300 x 300 DPI)

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STROBE 2007 (v4) Statement—Checklist of items that should be included in reports of cohort studies

Section/Topic Item

# Recommendation Reported on page #

Title and abstract 1 (a) Indicate the study’s design with a commonly used term in the title or the abstract 1

(b) Provide in the abstract an informative and balanced summary of what was done and what was found 1

Introduction

Background/rationale 2 Explain the scientific background and rationale for the investigation being reported 3-4

Objectives 3 State specific objectives, including any prespecified hypotheses 4

Methods

Study design 4 Present key elements of study design early in the paper 5

Setting 5 Describe the setting, locations, and relevant dates, including periods of recruitment, exposure, follow-up, and data

collection

5

Participants 6 (a) Give the eligibility criteria, and the sources and methods of selection of participants. Describe methods of follow-up 5

(b) For matched studies, give matching criteria and number of exposed and unexposed

Variables 7 Clearly define all outcomes, exposures, predictors, potential confounders, and effect modifiers. Give diagnostic criteria, if

applicable

5-9

Data sources/

measurement

8* For each variable of interest, give sources of data and details of methods of assessment (measurement). Describe

comparability of assessment methods if there is more than one group

5-9

Bias 9 Describe any efforts to address potential sources of bias 5 -9

Study size 10 Explain how the study size was arrived at 5

Quantitative variables 11 Explain how quantitative variables were handled in the analyses. If applicable, describe which groupings were chosen and

why

9-10

Statistical methods 12 (a) Describe all statistical methods, including those used to control for confounding 9-10

(b) Describe any methods used to examine subgroups and interactions 9-10

(c) Explain how missing data were addressed

(d) If applicable, explain how loss to follow-up was addressed

(e) Describe any sensitivity analyses

Results

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Participants 13* (a) Report numbers of individuals at each stage of study—eg numbers potentially eligible, examined for eligibility, confirmed

eligible, included in the study, completing follow-up, and analysed

5

(b) Give reasons for non-participation at each stage 5

(c) Consider use of a flow diagram 5

Descriptive data 14* (a) Give characteristics of study participants (eg demographic, clinical, social) and information on exposures and potential

confounders

5-7

(b) Indicate number of participants with missing data for each variable of interest

(c) Summarise follow-up time (eg, average and total amount) 5

Outcome data 15* Report numbers of outcome events or summary measures over time 5-9

Main results 16 (a) Give unadjusted estimates and, if applicable, confounder-adjusted estimates and their precision (eg, 95% confidence

interval). Make clear which confounders were adjusted for and why they were included

11-13

(b) Report category boundaries when continuous variables were categorized

(c) If relevant, consider translating estimates of relative risk into absolute risk for a meaningful time period

Other analyses 17 Report other analyses done—eg analyses of subgroups and interactions, and sensitivity analyses 11-13

Discussion

Key results 18 Summarise key results with reference to study objectives 14

Limitations

Interpretation 20 Give a cautious overall interpretation of results considering objectives, limitations, multiplicity of analyses, results from

similar studies, and other relevant evidence

2 and 16

Generalisability 21 Discuss the generalisability (external validity) of the study results 2

Other information

Funding 22 Give the source of funding and the role of the funders for the present study and, if applicable, for the original study on

which the present article is based

18

*Give information separately for cases and controls in case-control studies and, if applicable, for exposed and unexposed groups in cohort and cross-sectional studies.

Note: An Explanation and Elaboration article discusses each checklist item and gives methodological background and published examples of transparent reporting. The STROBE

checklist is best used in conjunction with this article (freely available on the Web sites of PLoS Medicine at http://www.plosmedicine.org/, Annals of Internal Medicine at

http://www.annals.org/, and Epidemiology at http://www.epidem.com/). Information on the STROBE Initiative is available at www.strobe-statement.org.

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A NORWEGIAN PROSPECTIVE STUDY OF PRETERM MOTHER-

INFANT INTERACTIONS AT SIX AND 18 MONTHS AND THE

IMPACT OF MATERNAL MENTAL HEALTH PROBLEMS,

PREGNANCY AND BIRTH COMPLICATIONS

Journal: BMJ Open

Manuscript ID bmjopen-2015-009699.R2

Article Type: Research

Date Submitted by the Author: 09-Dec-2015

Complete List of Authors: Misund, Aud R; University College of Oslo and Akershus, Health science Bråten, Stein; University of Oslo, Dept. of Sociology and Human Geography Nerdrum, Per; University College of Oslo and Akershus, Health science Pripp, Are; Oslo University Hospital, Department of Biostatistics, Epidemiology & Health Economy; University College of Oslo and Akershus, Faculty of Health Sciences Diseth, Trond; Oslo University Hospital and University of Oslo, Department of Clinical Neurosciences for Children, Women and Children’s Division and Department of Medicine

<b>Primary Subject Heading</b>:

General practice / Family practice

Secondary Subject Heading: Mental health, Obstetrics and gynaecology, Reproductive medicine, Paediatrics

Keywords: Neonatal intensive & critical care < INTENSIVE & CRITICAL CARE, MENTAL HEALTH, Maternal medicine < OBSTETRICS, PERINATOLOGY, TRAUMA MANAGEMENT, Child & adolescent psychiatry < PSYCHIATRY

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BMJ Open on M

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1

A NORWEGIAN PROSPECTIVE STUDY OF PRETERM MOTHER-

INFANT INTERACTIONS AT SIX AND 18 MONTHS AND THE

IMPACT OF MATERNAL MENTAL HEALTH PROBLEMS,

PREGNANCY AND BIRTH COMPLICATIONS

Aud R. Misund

1 Stein Bråten

Per Nerdrum

Are Hugo Pripp

Trond H. Diseth

ABSTRACT

Objective:

Pregnancy, birth and health complications, maternal mental health problems following

preterm birth and their possible impact on early mother-infant interaction at six and 18 months

corrected age (CA) were explored. Predictors of mother-infant interaction at 18 months CA

were identified.

Design and methods:

This prospective longitudinal and observational study included 33 preterm mother-infant (<33

GA) interactions at six and 18 months CA from a socio-economic low risk middle class

sample. The parent-child early relational assessment scale (PCERA) was used to assess the

mother-infant interaction.

Results:

“Bleeding in pregnancy” predicted lower quality in preterm mother-infant interaction in six

PCERA scales, while high “Maternal trait anxiety” predicted higher interactional quality in

two PCERA scales and “Family size” predicted lower interactional quality in one PCERA

scale at 18 months CA.

1 (Corresponding Author) Faculty of Health Sciences, University College of Oslo and Akershus and

Department of Medicine, Institute of Clinical Medicine, University of Oslo, adr: PO Box. 4 St. Olavs

plass, N-0130 Oslo, Norway e-mail:

[email protected]

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Mothers with symptoms of posttraumatic stress reactions, general psychological distress and

anxiety at two weeks postpartum (PP) showed significant better outcome than mothers

without symptoms in six PCERA subscales at six months CA and two PCERA subscales at18

months CA.

Conclusions:

Our study detected a correspondence between early pregnancy complications and lower

quality of preterm mother-infant interaction, and an association between high levels of

maternal mental health problems and better quality in preterm mother-infant interaction.

Strengths and limitations of this study:

The longitudinal design, the high response rate and the use of well-validated psychometric

instruments and interactional assessment tool are the strengths in this study.

Fifty percent of the attending women received psychological treatment during the study, and it

is a limitation that the influence of the psychological treatment on our study results was not

assessed.

The present study describes a small preterm group and one should be cautious about

generalising from this study.

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INTRODUCTION

Early parent-infant relationships that are well functioning seem to be critical to preterm

children. Preterm children face severe risk of cognitive, emotional, and behavioural disorders

,[1-8] and show more psychiatric symptoms in adolescence.[9] Early parent-infant

relationships that are well functioning seem to prevent and restore some of these difficulties in

preterm children.[10, 11] Good quality in mother-child interactions have been reported to

facilitate the infant’s emotional, behavioural, cognitive, and neurobehavioral

development.[12-17] The interactional quality is also found to be related to the child’s

physical health.[18, 19] Compared with infants born at term the preterm infants are likely to

show vague signals that are difficult to read and respond to and are in need of extended care

and support to gain self-regulation.[20, 21] These traits, as well as parent’s psychiatric disease

are known as risk factors for good quality parent-infant interactions.[22, 23] Research

detected significant higher mental health problems following preterm birth than term

birth.[24-26]

The maternal stress reaction following preterm birth has been highlighted as a risk

factor in preterm dyads in several studies.[24-29] Postpartum depression has been identified

as predictor for interactional difficulties in term dyads,[30] and reported as a risk factor for

difficulties in preterm mother-infant dyads.[31] Only a limited number of studies, however,

have explored the nature of mothers’ mental health problems following preterm birth with

psychometric tools, and their impact on mother-infant interaction. Several studies, however,

have explored the post-term effect on maternal mental health.[32-36] Blom et al. interestingly

reported that certain perinatal complications such as preeclampsia, hospitalization, emergency

caesarean, and fetal distress predicted higher depression outcomes in a normal population

sample.[36] An unaddressed trauma reaction is known to predispose for posttraumatic stress

disorder (PTSD) with long term effects on mothers’ mental health. The effect of mothers

postpartum PTSD on mother-infant interaction and infant’s development is less explored.[37]

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In addition only a limited number of studies have explored the maternal posttraumatic stress

responses following preterm birth,[38-45] and their impact on mother-infant interactions.[20,

42, 46]

The results from preterm mother-infant interaction research are contradictory.

Different measurements and definitions being used, as well as the complexity of mother-

infant interactional studies may have contributed to these differences. Some studies have

reported that preterm mothers showed more stimulating behaviour and were emotionally

withdrawn, as well as non-synchronous in their interaction with the child,[20, 21, 47-52] and

others have found no interactional differences between preterm and full term dyads.[20, 53-

58] Korja et al. detected that caregivers’ physical closeness with the infant was more

important to interactional quality than infants’ prematurity.[56] Finally, it is interesting that

several studies have shown that mothers are intensifying their efforts to be available and

supportive to their premature babies’ needs.[59-64] Preterm birth is reported to influence the

interaction between mother and infant.[20, 49, 65] The knowledge of risk factors that may

affect preterm mother-infant interaction is limited.[31, 66-68] The need for further exploration

of the complexity of factors influencing the early mother-infant relationship long-term in

preterm dyads seems essential.[6, 69]

The first aim of our longitudinal study was to explore the associations between

maternal mental health problems following preterm birth, pregnancy and birth complications,

and early preterm mother-infant interaction at six months CA (T2) and 18 months CA (T3).

The second aim of the study was to identify predictors of early mother-infant interaction

quality at T2 and T3.

To our knowledge, these associations have not been explored in other studies.

Psychometric tools and tentative psychiatric diagnosis (anxiety, depression, and PTSR/PTSD)

were used to assess maternal mental health problems following preterm birth.

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It should be noted that this paper is an extension of our previous studies of short- and

long-term maternal mental health problems following preterm birth.[44, 45]

METHOD

Participants

Data were collected in two periods: June 2005-January 2006 and October 2007-July

2008. The psychological responses of 29 consecutive mothers of 35 premature children born

before 33rd week of pregnancy were assessed at a high-specialized neonatal intensive care unit

(NICU) at Oslo University Hospital, Norway. Mothers of severely ill babies that the medical

staff estimated to have poor chance of survival, and non-Norwegian speakers were not

included. The participants stayed in NICU until they were discharged for home. The parents

could participate in the caring of the infant during hospitalisation. The data collection was

performed as soon as the mothers were able to attend an interview following preterm

childbirth: within two weeks postpartum (T0) median 11 days (4-30); then within two weeks

after hospitalization (T1), median time postpartum 2.7 months (0.2-4.7); then at the infant’s

six months corrected age (T2), median time postpartum 8.5 months (7.6-10.4); and at the

infant’s 18 months corrected age (T3), median time following birth 20.6 months (19.2-23.4).

Data collection of mother-infant interaction was collected only at T2 and T3. Mothers of

severely ill babies with uncertain survival and non-native speakers were not included (Figure

1).

Semi-structured interviews and standardized mental health screening questionnaires

were used to collect data about socio-demographics, the pregnancy and birth, child’s health

status, and mothers’ mental health problems. Medical charts were used to double-check the

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data of child’s health status, and pregnancy and birth. The studied sample was homogeneous

regarding high scores on socio-demographic variables such as education, income, and housing

standard. Most mothers were giving first time birth late in their twenties or early thirties. All

lived with the child’s father and none reported any relationship problems (Table 1). The

participating mothers’ mental health problems following preterm birth have been assessed at

T0, T1, T2, T3 and methods and results are described in detail in our earlier papers.[44, 45]

Maternal mental health problems were assessed at every time points (T0, T1, T2, T3) by

standardized psychometric methods with well-established reliability and validity: Impact of

Event Scale (IES) 15-item version, one of the key psychometric assessment methods in

traumatic stress research,[70, 71] the General Health Questionnaire (GHQ) 30item version, a

widely used screening instrument for assessing the presence of distress, psychopathology and

overall well-being,[72, 73] and the State/Trait Anxiety Inventory (STAI-X1/X2)[74] is widely

used to assess maternal anxiety. STAI-X1 measures state anxiety levels reflecting subjective

feelings of tension, apprehension, nervousness and worry. STAIX2 is a measure of trait

anxiety that refers to individual differences in anxiety proneness, i.e. in the tendency to see the

world as dangerous and threatening, and the frequency with which anxiety states are

experienced. Scores above the threshold for identifying a psychiatric case is referred to as a

case score.

Based on all information available in a clinical perusal of the psychometric self-reports

IES, GHQ and STAI of each of the 29 preterm mothers, and blinded to the physical and

sociodemographic characteristics of the mothers and their children, a tentative clinical

diagnosis was made where appropriate based on the clinical descriptions and diagnostic

guidelines in the ICD-10 Classification of mental and behavioural disorders, and was assessed

by a psychiatrist (last author).

A prevalence of maternal posttraumatic stress responses/disorders (PTSR/PTSD) two

weeks postpartum (T0) of 52% and maternal PTSD at 18 months corrected age (T3) of 23%

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was revealed. On the other hand, depression was detected among 24 % of the mothers two

weeks postpartum and among 8% of the mothers at T3. Anxiety decreased from 7% at two

weeks postpartum to zero at T3.

Fourteen of the mothers received psychological support at the hospital during their

infants’ NICU stay. Eleven of these mothers were referred for further psychological treatment

after discharge from the hospital. Altogether, 20 mothers that met the criteria of clinical

diagnoses were referred for adequate psychological treatments such as psychotherapy,

psychopharmacology treatment, and mother-infant interactional treatment. Five of the mothers

refused the referral for psychological treatment, and only one of them filled the criteria for a

tentative clinical diagnosis (PTSD/Depression) at T3. The prevalence of pregnancy and birth

complications and maternal mental health problems following preterm birth are reported in

earlier papers.[44, 45]

Data collected at 2 weeks postpartum (T0) about sociodemographics, physical

complications and maternal mental health problems following preterm birth are presented in

Table 1.

Table 1. Socio-demographic, physical characteristics, and mental health variables in mothers

giving preterm birth and their children at two weeks postpartum (T0).

Mothers n=29

Age; mean (SD) 33.7 (4.3)

Education > 12 years; n (%) 26 (89.7)

Single parent; n (%) 0 (0)

Unemployed; n (%) 4 (13.8)

Previous psychological treatment; n (%)

8 (27.6)

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Chronic illness; n (%) 2 (6.9)

Tot. no. of children; median (quartile low,upper) 2 (1,2)

Previous pregnancies; median (quartile low,upper) 1 (0,2)

Previous childbirths; median (quartile low,upper) 0 (0,1)

First time mothers; n (%) 18 (62.1)

IVFa pregnancy; n (%) 8 (27.6)

Bleeding in pregnancy; n (%) 19 (65.5)

Preeclampsia; n (%) 4 (14.3)

Caesarean; n (%) 17 (58.6)

Mental Health Variables:b

IES total (0-75); median (quartile low,upper) 18 (11,30)

IES case score >18; n (%) 13 (44.8)

GHQ Likert score (0-90); n (%) 40 (15.4)

GHQ case (0-30): n (%) 12.8 (7.5)

GHQ case score >5; n (%) 23 (79.3)

STAI-X1 (0-40); mean (SD) 21.5 (2.8)

STAI-X1 case score >19; n (%) 20 (69)

STAI-X2 (0-80); mean (SD) 44.0 (4)

STAI-X2 case score >39; n (%) 27 (93.1)

PTSR Tentative clinical diagnosis; n (%) 15 (51.7)

Children n=35

Girl; n (%) 17 (48.6)

Boy; n (%) 18 (51.4)

Twinc; n (%) 14 (40)

Gestational age (weeks);

Median (range)

Mean (SD)

29 (24-32)

28.5 (2.6)

Birth weight (g);

Median (range)

Mean (SD)

1185(623-2030)

1222(423)

Apgar score at 1 minute; mean (SD) 6,3 (2.3)

Apgar score at 5 minute; mean (SD) 7.6 (2.0)

Apgar score at 10 minute; mean (SD) 8.3 (1.0)

Oxygen supply > 28 days; n (%) 19 (54)

IVHd; n (%) 7 (20.0)

a In vitro fertilization/Assisted fertilization.

bThe Impact of Event Scale (IES) 15 item with scoring range 0(not at all) to 5 (very much), The General Health Questionnaire (GHQ)30 items

Likert scores with weights 0-1-2-3 and case scores with weights 0-0-1-1, The Spielberger State/Trait Anxiety Inventory (STAI-X1/X2) 10

item/20 item with scoring range 1-2-3-4. The STAI-X1 10 item was constructed since both STAI-X1 12 item and 20 item had been used and

only 10 items overlapped. Tentative Clinical Diagnosis: Posttraumatic Stress Responses (PTSR). cTwo of the twins were raised as singleton as their twin sibling were stillborn.

dIntraventricular hemorrhage grade 1-4 following birth.

Measures

Mother–infant interaction in a free-play situation was video recorded at six and 18

months CA. According to Clark (1985) by six months of age, dyadic mutuality and dyadic

regulatory processes are perceptible while at 18 months, the infant's own communication

skills are easier to identify in interaction.[75] The interaction situation was recorded in a

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consultation room at the psychiatric clinic for children and families situated in the same

building as the hospital the children were born in, except for four video recordings at 18

months CA that were recorded in their homes. The recordings were performed when child was

awaken and interested in a play session with mother. Recordings were stopped and performed

later when child became too distressed or sleepy to play. A therapist (first author) instructed

the mothers about the procedure. For the video recording, the mother and the infant were

placed on a soft mat with age-appropriate toys. Instructions by the investigators given to the

mother prior to the video recording were: “This is a free-play time with your child. You can

use the toys, or you can play without the toys. Try to play or be with your infant as you

usually would be”. Video recordings were obtained from all mother-infant pairs.

The recordings were five minutes long. The mother-infant interaction in the free-play

situation was analysed using the Parent-Child Early Relational Assessment (PCERA)

method.[75] The PCERA is developed to assess affective and behavioural aspects that both

the parent and infant bring into the interaction,[75] and the validity of the free play situation

has been established.[76, 77] Video recordings allows thoroughly analysis of the interactions

several times and in short and slow sections that can identify areas of strength and of concern

in the mother-infant interplay. The PCERA consists of 29 parental items, 28 infant items and

eight dyadic items. The assessment rates the frequency, duration and intensity of the infant's,

parent's and dyad's behaviour. The parental items comprise the parent's positive and negative

affect, expressed attitude toward the infant, sensitivity and contingent response to the infant's

cues, mirroring the infant's feeling, capacity to structure, behavioural involvement and

parental style. The infant items comprise expressed positive and negative affect and

characteristic mood, behaviour/adaptive abilities, activity level and communication skills. The

dyadic items comprise affective quality of interaction and mutuality of interaction.

All items were rated on a 5-point “Likert” scale. The scores 1 and 2 describe an area of

concern, the score 3 describes an area of some concern and the scores 4 and 5 describe an area

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of strength. A trained coder made the assessment. The coder was unaware of the infant's

background and clinical status. Additionally, to estimate the interrater reliability from the

study data, 20% of all assessments were double-scored by another trained coder. The study

data was assessed by calculating the mean of the agreement percentage of the raters' overall

agreement. Agreement equal or above 80% is considered good, 50-80% is considered

moderate, and lower than 50% is considered poor. The mean of interrater agreements was

80.3% in six months CA and 81% in 18 months CA.

The PCERA items were organized in eight scales according to Clark,[75] before the

data analysis: “Maternal positive affective involvement PS1”, “Maternal negative affect &

behaviour PS2”, “Maternal intrusiveness PS3”, “Infant positive affect PS4”, “Infant quality

of play PS5”, “Infant dysregulation PS6”, “Dyadic mutuality & reciprocity PS7”, and “Dyadic

disorganization & tension PS8”. PCERA high scores (4-5) always indicate positive affect and

behaviour or lack of negative affect and behaviour. The Cronbach alpha coefficients for

calculating the internal consistency of PCERA subscales in our study were satisfactorily and

were .95,.86,.86, .90,.87,.85,.80,.86 for PS1-PS8 at six months CA (T2), and

.89,.81,.82,.92,.89,.75,.73,.79 for PS1-PS8 at 18 months CA (T3).

The PCERA scale has been used in several studies to explore the quality of preterm

mother-infant interactions.[31, 78-82]

Statistical methods

Continuous variables are presented as means (SD) or if skewed, as median and range.

Categorical variables are given as proportions and percentages. Paired-sample t-test was used

for comparison of the PCERA means scores at T2 and T3. Differences in the quality of

mother-infant interactions measured by the PCERA scales were explored with independent-

samples t-test. As grouping variable we used mothers’ case scores above threshold for

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identifying psychiatric symptoms (0=no, 1=yes) in IES, GHQ, STAI and the tentative

diagnostic assessments at four time points; two weeks

PP (T0), two weeks after hospitalization (T1), six months CA (T2), and 18 months CA (T3)

(Figure 2). A more detailed description of mothers’ case scores in IES, GHQ, STAI and the

tentative diagnostic assessments are available in our earlier papers.[44, 45]

The association between variables at T3 were assessed using Pearson’s correlation

coefficient (Table 2).

Stepwise regression analysis with a forward selection method was used to identify possible

predictors of the PCERA results at T3 (Table 3). At most three variables at T3 with the

strongest bivariate associations above 0.3 were included in the multivariable linear regression

model; PS1 (STAI-X2 case, STAI-X2 sum, GHQ Likert), PS2 (Bleeding in pregnancy, GHQ

case, GHQ Likert), PS3 (STAI-X2 case, Bleeding in pregnancy, Parity/STAI-X2 sum), PS4

(Bleeding in pregnancy, GHQ case), PS5 (Bleeding in pregnancy, Apgar 5 min), PS6 (Family

size, Acute Caesarean, Bleeding in pregnancy), PS7 (Bleeding in pregnancy, GHQ case,

STAI-X2 case), and PS8 (Bleeding in pregnancy, GHQ case, CH<grade 3). A careful check of

the model assumptions, including an investigation of residual plots, did not reveal any

violation of the assumptions. All analyses were performed in SPSS version 20. Two-sided

statistical tests were applied and a 5 % statistical significance level was chosen.

Ethics

Written informed consent was obtained from participants prior to the study start. The

study protocol was approved in 5 May 2005 and 19 April 2007 by the National Committee for

Research Ethics (S-05068 and S-07096b) and 1 April 2005 and 12 March 2007 by the Data

Inspectorate (12360 and 07/1088). The study protocol was carried out in accordance with the

Declaration of Helsinki.

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For ethical reasons the mothers that reported mental health problems and had case

scores above the threshold for identifying psychiatric symptoms in IES, GHQ and STAI were

assessed and referred for adequate psychological treatment. In this study, we looked for

mental health problems in mothers at four points from the time of birth to two years

postpartum. A no referral procedure could have caused unnecessary suffering for both

mothers and children.

RESULTS

Associations between maternal mental health problems following preterm birth,

pregnancy and birth complications, and early preterm mother-infant interaction at six

months CA (T2) and 18 months CA (T3)

The paired sample t-test of the results of the PCERA showed no significant difference

for the PCERA mean scores from six months to 18 months corrected age (CA). For that

reason the presented results from correlation and regression analysis are based only on the

mean scores from 18 months CA. The results of the PCERA revealed mean scores in three of

the scales in the area of moderate concern and five scales in the area of no concern. The

results of the PCERA is presented in Table 2.

Group differences in mother – infant interaction quality at T2 and T3 for mothers with and

without psychometric case scores at T0, T1, T2, and T3

The results of the independent-samples t-test showed significant group differences at

T2 and T3 between the mothers with case scores above the threshold for identifying a

psychiatric case compared to mothers without case scores in IES, GHQ, and tentative PTSR

diagnosis at T0 (Figure 2). Mothers’ with case scores at T3 in GHQ also showed significant

better results at the .05 level (2-tailed)* in two PCERA scales at T3; PS7 Dyadic mutuality

and reciprocity (N0/N1=24/8, mean 3.1/3.7*), and PS8 Dyadic disorganization and tension

(N0/N1=24/8, mean 3.9/4.4*). Unexpectedly, the mothers with case scores (1=yes) at T0

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showed significantly better quality in mother-infant interaction in six (T2) and two (T3)

subscales of the PCERA than mothers with no (0=no) case scores (Figure 2). Tentative

depression or anxiety diagnosis (0=no, 1=yes) as a grouping variable showed no significant

group differences regarding the quality of the mother-infant interaction.

Associations between maternal mental health problems and mother-infant interactional

quality at T3

In the bivariate correlation analyses, we revealed a positive correlation between better

interactional quality measured by PCERA and higher levels of maternal mental health

problems measured by psychometric means at T3. High levels of GHQ Likert and case scores

correlated with high levels of PCERA scores in three scales and GHQ case sum scores

correlated with two scales. High levels of STAI-X2 sum scores were associated with high

levels of PCERA scores in two scales and case scores correlated with three scales (Table 2).

Associations between pregnancy/ birth complications, maternal variables and mother-infant

interactional quality at T3

The strongest correlations were inversely and found between a pregnancy complication

“Bleeding in pregnancy” and the following six PCERA scales: “Maternal negative affect and

behaviour (PS2), Maternal intrusiveness, intensity, and inconsistency (PS3), Infant positive

affect, communicative, and social skills (PS4), Infant quality of play, interest, and attention

(PS5), Dyadic mutuality and reciprocity (PS7), and Dyadic disorganization and tension

(PS8)”.

Two infant complications following birth were correlated with two of the PCERA

scales. Infant health scores at the infant’s “Apgar scores at 5 minutes postpartum” correlated

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positively with the “Infant quality of play, interest, and attention (PS5)” scale. Infant stroke by

“Intraventricular Haemorrhage grade 1 or 2 (IVH)” closely following birth” correlated

inversely with the “Maternal negative affect and behaviour (PS2)” scale (Table 2).

Three maternal variables correlated with two of the PCERA scales. Parity (number of

previous births with child survival) and the scale “Maternal intrusiveness, intensity and

inconsistency (PS3)” were positively correlated. Family size (number of children in the

family) and the “Infant dysregulation and irritability (PS6)” scale inversely correlated. “Acute

caesarean” correlated positively with high scores on the same scale.

Associations between exposure variables, e.g. IVF treatment, pre-and postnatal

maternal health problems and pregnancy and birth/postnatal complications, were not

significant.

Table 2. Pearson correlations coefficients at T3 (18 months corrected age) between the PCERA scales, the

maternal psychometric means, and the individual characteristics of the mothers and infants. (N=32). Mean

values, range scores and minimum and maximum scores for PCERA subscales are reported in the last

row of this table.

PCERA

PS1

Maternal Positive

affective

involvement

PCERA

PS2

Maternal

Negative

affect &

Behavior

PCERA PS3

Maternal Intrusiveness

Insensitivity

Inconsistency

PCERA PS4

Infant Positive affect Communicative

& Social skills

PCERA

PS5 Infant Quality of

play

Interest Attention

PCERA

PS6

Infant Dysregu -lation

Irritability

PCERA

PS7

Dyadic Mutuality

Reciprocity

PCERA

PS8

Dyadic Disorganization

Tension

GHQ Likert

sum score

.39*

.37*

.35* .16 .12 .05 .30 .28

GHQ case

sum score

.36* .36* .06 .12 .07 .17 .26 .31

GHQ

case > 5

.26 .40* .30 .33 .29 .21 .41* .43*

STAI-X2

sum score

.46** .21 .39*

.09 -.03 .08 .25 .19

STAI-X2

case > 39

.48* .36* .57** .19 .06 .07 .32 .32

Parity

.07

.18 .39* .24 .10

.01

.31 .33

CH< grade

3a

-.21 -.28 -.35* -.20 -.23 -.15 -.30 -.35

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Apgar

at 5

min.

-.01 .09 .20 .22 .35* -.12 .18 .19

Bleeding in

pregnancy

-.22 -.45** -.56** -.53** -.55** -.33 -.46** -.52**

Family

sizeb

-.09 -.12 .07 -.02 -.16 -.45* .01 .00

Acute

Caesarean

.14 .14 .13 .01 .03 .39* .07 .22

Mean/

Range c

(Min-Max)

3.8/2.5

(2.3-4.8)

4.6/1.6

(3.4–5.0)

4.2/2.0

(3.0–5.0)

3.2/3.0

(1.9–4.9)

4.0/2.2

(2.7–4.9)

4.5/1.3

(3.7–

5.0)

3.3/2.8

(2.0–4.8)

4.0/2.0

(3.0–5.0)

*Correlation is significant at the .05 level (2-tailed). **Correlation is significant at the .01 level (2-tailed). a CH< grade 3 refers to Cerebral Hemorrhage grade 1 or 2 closely after birth.

b Family size refers to the number

of children in the family. c Rates 1 and 2 in PCERA subscale; “Area of concern”. Rate 3 in PCERA subscale; “Area

of moderate concern”. Rates 4 and 5 in PCERA subscale; “Area of no concern”.

Predictors of mother-infant interactional quality at T3

In the multivariable linear regression analyses we revealed that the pregnancy

complication variable “Bleeding in pregnancy” was a significant predictor (p<0.01) of lower

scores in preterm mother-infant interaction in six of the PCERA domains, including both of

the Dyadic scales (Table 3). Trait anxiety (STAI-X2) case and sum score are significant

predictors for higher quality in preterm mother-infant interaction in the “Maternal positive

affect domain (PS1)” (p<0.01) and in the “Maternal intrusiveness (PS3)” domain (p<0.05),

consecutively. Higher “Number of children in the family” predicts lower interaction quality in

the “Infant dysregulation and irritability (PS6)” scale (p<0.05). Adjusted R2 showed that the

predictors explain from 17 to 39 % of the variance in different PCERA scales.

Table 3. Significant results of the multivariable regression analyses with the selected

independent variables to predict mother-child interaction following preterm birth at T3 (18

months corrected age). Unstandardized (B) and standardized (Beta) regression coefficients.

(N=32)

Predicting variable B CI Beta P value R2

adj.

PCERA subscales:

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PS1 (Maternal positive

affective involvement)

STAI-X2 case .53 (.17, .89) .48 .005 .21

PS2 (Maternal negative

affect & behavior)

Bleeding in pregnancy -.21 (-.37, -.06) -.45 .009 .18

PS3 (Maternal

intrusiveness)

Bleeding in pregnancy

STAI-X2 sum score

-.29

.03

(-.45, -.13)

(.01, 06)

-.53

.35

.001

.017

.39

PS4 (Infant positive

affect)

Bleeding in pregnancy -.43 (-.68, -.17) -.53 .002 .26

PS5 (Infant quality of

play)

Bleeding in pregnancy -.35 (-.56, -.15) -.55 .001 .27

PS6 (Infant

dysregulation)

Family size

-.24

(-.42, -.06)

-.45

.011

.17

PS7 (Dyadic mutuality &

reciprocity )

Bleeding in pregnancy

-.33

(-.56, -.09)

-.33

.008

.21

PS8 (Dyadic

disorganization &

tension)

Bleeding in pregnancy

-.32

(-.51, -.12)

-.52

.002

.25

PCERA subscales were used as dependent variables (At most three variables with strongest bivariate association above 0.3 were used as

independent variables); PS1 (STAI-X2 case, STAI-X2 sum score, GHQ Likert sum score), PS2 (Bleeding in pregnancy, GHQ case, GHQ Likert sum score),PS3

(STAI-X2 case, Bleeding in pregnancy, Parity/STAI-X2 sum score), PS4 (Bleeding in pregnancy), PS5 (Bleeding in pregnancy, Apgar at 5 minutes), PS6 (Family size, Acute Caesarean), PS7 (Bleeding in pregnancy, GHQ case), PS8 (Bleeding in pregnancy, GHQ case).

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DISCUSSION

The study revealed significant associations between pregnancy and birth

complications, maternal postpartum mental health, and the quality of preterm mother-infant

interaction. The most surprising results in our study were the detection of 1; “Bleeding in

pregnancy” as a predictor of lower quality in preterm mother-infant interaction in six of eight

PCERA scales, and 2; the association between high levels of maternal mental health problems

and better mother-infant interactional quality.

The predictor “Bleeding in pregnancy” is interesting. No other study has, to our

knowledge, revealed a physical complication in pregnancy that predicts a possible weaker

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quality of the mother-infant interaction following preterm birth. With reference to our

previous papers, “Bleeding in pregnancy”, was detected as a predictor of low levels in

maternal mental health symptoms, while, a sudden complication later in pregnancy

“Preeclampsia”, predicted high levels of maternal mental health problems following preterm

birth.[44, 45] As “Bleeding in pregnancy” usually occurs before 22 weeks of pregnancy it

may be experienced as an early warning sign for possible pregnancy complications by the

mother. A possible hypothesis may be that early complications in pregnancy and

complications late in pregnancy influence the mother differently in the way she relates to her

unborn child and how her transition into motherhood alternates. Early bleeding in pregnancy

could leave the mother-to-be with the impression that her child is at risk and when preterm

birth becomes reality, it may confirm her fear of loss. Given such an enduring threatening

impression, the mother can be expected to be anxious and alert, preventing her from relaxing

and taking pleasure in the mother-infant interaction, and rather initiating negative affect and

intrusiveness which may also entail dyadic disorganization and tension.

On the other hand, the mother without prior early warning signs is likely to have been

quite “undisturbed” in her transition process to prepare for motherhood until later in her

pregnancy. “Preeclampsia” and a sudden preterm birth induces a serious situation for both

mother and child and both may risk non-survival. When mother experiences hope for infant

survival, we may assume that a prior “undisturbed” transition process into motherhood is

likely to increase her efforts to attain the very best mother-infant interaction.

Attachment theory supports our hypothesis that loss or possible loss can be seen as

serious threats to attachment.[83] A growing number of research show that mothers’

attachment pattern is associated with the mother-infant interaction,[84, 85] and an assessment

of mothers’ attachment pattern would possibly have given a valuable perspective to our

results.

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Unexpectedly, our results showed that high levels of maternal mental health problems

following preterm birth were significantly associated with better quality in preterm mother-

infant interaction. In regression analysis, we found that high levels of maternal anxiety

measured by STAI-X2 predicted better mother-infant interaction in two PCERA scales at T3.

In our previous studies we found an association between STAI-X2 and general psychological

distress outcomes following preterm birth,[44, 45] and another study revealed an association

between STAI-X2 and posttraumatic stress outcomes following term birth.[86] With reference

to these studies we may suggest that there is an significant association between high levels of

mental health problems following preterm birth and better quality in two PCERA scales at T3.

In the independent-samples t-test, we also found that mothers with symptoms of posttraumatic

stress, general psychological distress and anxiety at 2 weeks postpartum (T0) showed

significantly better quality in mother-infant interaction on six PCERA scales at six months

(T2) and on two PCERA scales at 18 months corrected age (T3).

It is theoretically interesting that our results imply that high levels of maternal mental

distress improve the preterm mother–infant interaction. At first glance, this result seems to

contradict the well-known connection between high levels of maternal depression and high

risk mother-infant interactions.[31, 87-89] It should be noted that we found quite low

prevalence of depression among the mothers participating in this study.[44, 45] Instead, we

found high levels of posttraumatic stress reactions. PTSD following childbirth is

acknowledged by several researchers to be potentially different from PTSD following other

traumatic incidences.[37] The culturally positive connotation of giving birth, the mother-child

connection, the transition from pregnancy to giving birth, and the formal care setting the birth

incident takes place in are all matters that may have an impact on PTSD following preterm

birth. Several studies have reported that many people experience positive psychological

growth after struggling with trauma.[90, 91] Maternal posttraumatic stress reaction following

preterm birth is characterized by a prior physical trauma where survival of the mother and the

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baby may be at risk. Is it possible that maternal posttraumatic stress reactions following

preterm birth helps the mother to focus her attention towards her premature baby’s wellbeing?

Our findings may imply that the posttraumatic stress response activates and helps the mother

cope over time with a tremendously stressful situation, and furthermore helps her stimulate

the prematurely born child’s healthy development. Several studies support our view.[60-62,

64] However, other studies that have explored maternal mental health problems following

preterm birth and preterm mother-child interactions have reported results that contradict with

our findings.[42, 50, 81, 92] Studies that have used the PCERA scale in studying preterm

dyads, however, did not find depression to be a significant predictor of PCERA outcome at

six, 12, or 16 months CA.[31, 79] The socio-demographic variable “Family size” predicted

low interactional quality in one of the PCERA scales. In our study, the mothers with preterm

babies that had siblings showed significantly lower scores in the “Infant dysregulation scale

(PS6)” in the PCERA. Our result is supported by two studies in the 1970’s and 1980’s that

found the preterm infant’s birth-order to affect the mother-child interaction.[93, 94] An

explanation for their results was the mother’s divided attention between the infant and other

siblings.

Strength/limitations

The results from a small and explorative study have low statistical power and low

external validity,[95] and one should be cautious about generalising from the study. In most

studies there is also a possibility that confounding variables are not included in the analysis

that should have been. In our study such factors could have been assessment of mothers’

attachment patterns, the effect of psychological assessment and referral procedure and an

assessment of the comforting conditions for mother-infant interactions in the hospital.

However, our study results may still be of value for future research that will systematically

explore the complexity of factors influencing early preterm mother-infant interaction in a

broader sense.

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The participants in this study were included consecutively and both single and multiple

births were included, thus minimizing selection bias. Our sample was homogeneous in socio-

economic background (SES). However, the mothers had higher educational attainments,

greater age and higher socioeconomic status, higher number of twins and higher rate of

previous psychological treatment than would be found in a typical population of mothers who

deliver preterm in our country. In this sample we found no indication of significant

differences in parental challenges between participants with singletons or twins that needed to

be controlled for. Besides high prevalence of earlier psychological treatment among the

mothers in our sample, no other collected data indicated that mental distress had impact on

their psychosocial function in everyday life before the actual preterm birth incident.

Regarding research on quality of the preterm mother-infant interaction, it has been considered

that risk factors other than preterm birth itself have been sources of bias in many studies.[20,

48, 96] In our study, we have controlled for high risk socio-economic backgrounds.

It is a limitation that the video-procedure of PCERA could not be followed for the four

dyads that were recorded in their homes and not in the clinic, as were the others. On the other

hand, these dyads would not have participated if the recordings were not made in their homes.

It is a limitation that interrater reliability was not checked for tentative clinical diagnosis. The

prediction model used in this study needs further validation by future studies.

CONCLUSIONS

Our study detected a correspondence between early pregnancy complications and

lower quality of preterm mother-infant interaction, and an association between high levels of

maternal mental health problems and better quality in preterm mother-infant interaction.

Early intervention programs should be considered to mothers who give preterm birth to

support mother-infant interaction.

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Acknowledgements

The authors would like to thank the families that participated in the study, the staff of the

maternity ward at the neonatal intensive care unit at the National Hospital, Oslo and Sari

Ahlqvist-Björkroth who coded and Tanja Lipasti who recoded the PCERA data. In particular,

we want to thank the parents who participated in the study.

Contributorship statement

ARM initiated the study, collected, and organized the data. ARM and AHP performed the

statistical analyses. ARM, PN, SB, AHP and THD wrote the article.

Competing interests

We have no information of disclosure of interests.

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Funding

This work was supported by the Centre for Child and Adolescent Mental Health, Eastern and

Southern Norway and the University College of Oslo and Akershus.

Data sharing statement

The full data set is available from the corresponding author Aud R.

Misund([email protected]

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209x297mm (300 x 300 DPI)

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209x297mm (300 x 300 DPI)

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STROBE 2007 (v4) Statement—Checklist of items that should be included in reports of cohort studies

Section/Topic Item

# Recommendation Reported on page #

Title and abstract 1 (a) Indicate the study’s design with a commonly used term in the title or the abstract 1

(b) Provide in the abstract an informative and balanced summary of what was done and what was found 1

Introduction

Background/rationale 2 Explain the scientific background and rationale for the investigation being reported 3-4

Objectives 3 State specific objectives, including any prespecified hypotheses 4

Methods

Study design 4 Present key elements of study design early in the paper 5

Setting 5 Describe the setting, locations, and relevant dates, including periods of recruitment, exposure, follow-up, and data

collection

5

Participants 6 (a) Give the eligibility criteria, and the sources and methods of selection of participants. Describe methods of follow-up 5

(b) For matched studies, give matching criteria and number of exposed and unexposed

Variables 7 Clearly define all outcomes, exposures, predictors, potential confounders, and effect modifiers. Give diagnostic criteria, if

applicable

5-9

Data sources/

measurement

8* For each variable of interest, give sources of data and details of methods of assessment (measurement). Describe

comparability of assessment methods if there is more than one group

5-9

Bias 9 Describe any efforts to address potential sources of bias 5 -9

Study size 10 Explain how the study size was arrived at 5

Quantitative variables 11 Explain how quantitative variables were handled in the analyses. If applicable, describe which groupings were chosen and

why

9-10

Statistical methods 12 (a) Describe all statistical methods, including those used to control for confounding 9-10

(b) Describe any methods used to examine subgroups and interactions 9-10

(c) Explain how missing data were addressed

(d) If applicable, explain how loss to follow-up was addressed

(e) Describe any sensitivity analyses

Results

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For peer review only

Participants 13* (a) Report numbers of individuals at each stage of study—eg numbers potentially eligible, examined for eligibility, confirmed

eligible, included in the study, completing follow-up, and analysed

5

(b) Give reasons for non-participation at each stage 5

(c) Consider use of a flow diagram 5

Descriptive data 14* (a) Give characteristics of study participants (eg demographic, clinical, social) and information on exposures and potential

confounders

5-7

(b) Indicate number of participants with missing data for each variable of interest

(c) Summarise follow-up time (eg, average and total amount) 5

Outcome data 15* Report numbers of outcome events or summary measures over time 5-9

Main results 16 (a) Give unadjusted estimates and, if applicable, confounder-adjusted estimates and their precision (eg, 95% confidence

interval). Make clear which confounders were adjusted for and why they were included

11-13

(b) Report category boundaries when continuous variables were categorized

(c) If relevant, consider translating estimates of relative risk into absolute risk for a meaningful time period

Other analyses 17 Report other analyses done—eg analyses of subgroups and interactions, and sensitivity analyses 11-13

Discussion

Key results 18 Summarise key results with reference to study objectives 14

Limitations

Interpretation 20 Give a cautious overall interpretation of results considering objectives, limitations, multiplicity of analyses, results from

similar studies, and other relevant evidence

2 and 16

Generalisability 21 Discuss the generalisability (external validity) of the study results 2

Other information

Funding 22 Give the source of funding and the role of the funders for the present study and, if applicable, for the original study on

which the present article is based

18

*Give information separately for cases and controls in case-control studies and, if applicable, for exposed and unexposed groups in cohort and cross-sectional studies.

Note: An Explanation and Elaboration article discusses each checklist item and gives methodological background and published examples of transparent reporting. The STROBE

checklist is best used in conjunction with this article (freely available on the Web sites of PLoS Medicine at http://www.plosmedicine.org/, Annals of Internal Medicine at

http://www.annals.org/, and Epidemiology at http://www.epidem.com/). Information on the STROBE Initiative is available at www.strobe-statement.org.

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A NORWEGIAN PROSPECTIVE STUDY OF PRETERM MOTHER-

INFANT INTERACTIONS AT SIX AND 18 MONTHS AND THE

IMPACT OF MATERNAL MENTAL HEALTH PROBLEMS,

PREGNANCY AND BIRTH COMPLICATIONS

Journal: BMJ Open

Manuscript ID bmjopen-2015-009699.R3

Article Type: Research

Date Submitted by the Author: 12-Jan-2016

Complete List of Authors: Misund, Aud R; University College of Oslo and Akershus, Health science Bråten, Stein; University of Oslo, Dept. of Sociology and Human Geography Nerdrum, Per; University College of Oslo and Akershus, Health science Pripp, Are; Oslo University Hospital, Department of Biostatistics, Epidemiology & Health Economy; University College of Oslo and Akershus, Faculty of Health Sciences Diseth, Trond; Oslo University Hospital and University of Oslo, Department of Clinical Neurosciences for Children, Women and Children’s Division and Department of Medicine

<b>Primary Subject Heading</b>:

General practice / Family practice

Secondary Subject Heading: Mental health, Obstetrics and gynaecology, Reproductive medicine, Paediatrics

Keywords: Neonatal intensive & critical care < INTENSIVE & CRITICAL CARE, MENTAL HEALTH, Maternal medicine < OBSTETRICS, PERINATOLOGY, TRAUMA MANAGEMENT, Child & adolescent psychiatry < PSYCHIATRY

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BMJ Open on M

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1

A NORWEGIAN PROSPECTIVE STUDY OF PRETERM MOTHER-

INFANT INTERACTIONS AT SIX AND 18 MONTHS AND THE

IMPACT OF MATERNAL MENTAL HEALTH PROBLEMS,

PREGNANCY AND BIRTH COMPLICATIONS

Aud R. Misund

1 Stein Bråten

Per Nerdrum

Are Hugo Pripp

Trond H. Diseth

ABSTRACT

Objective:

Pregnancy, birth and health complications, maternal mental health problems following

preterm birth and their possible impact on early mother-infant interaction at six and 18 months

corrected age (CA) were explored. Predictors of mother-infant interaction at 18 months CA

were identified.

Design and methods:

This prospective longitudinal and observational study included 33 preterm mother-infant (<33

GA) interactions at six and 18 months CA from a socio-economic low risk middle class

sample. The parent-child early relational assessment scale (PCERA) was used to assess the

mother-infant interaction.

Results:

“Bleeding in pregnancy” predicted lower quality in preterm mother-infant interaction in six

PCERA scales, while high “Maternal trait anxiety” predicted higher interactional quality in

two PCERA scales and “Family size” predicted lower interactional quality in one PCERA

scale at 18 months CA.

1 Faculty of Health Sciences, University College of Oslo and Akershus and Department of Medicine,

Institute of Clinical Medicine, University of Oslo, adr: PO Box. 4 St. Olavs plass, N-0130 Oslo,

Norway e-mail:

[email protected]

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Mothers with symptoms of posttraumatic stress reactions, general psychological distress and

anxiety at two weeks postpartum (PP) showed significant better outcome than mothers

without symptoms in six PCERA subscales at six months CA and two PCERA subscales at18

months CA.

Conclusions:

Our study detected a correspondence between early pregnancy complications and lower

quality of preterm mother-infant interaction, and an association between high levels of

maternal mental health problems and better quality in preterm mother-infant interaction.

Strengths and limitations of this study:

The longitudinal design, the high response rate and the use of well-validated psychometric

instruments and interactional assessment tool are the strengths in this study.

Fifty percent of the attending women received psychological treatment during the study, and it

is a limitation that the influence of the psychological treatment on our study results was not

assessed.

The present study describes a small preterm group and one should be cautious about

generalising from this study.

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INTRODUCTION

Early parent-infant relationships that are well functioning seem to be critical to preterm

children. Preterm children face severe risk of cognitive, emotional, and behavioural disorders

,[1-8] and show more psychiatric symptoms in adolescence.[9] Early parent-infant

relationships that are well functioning seem to prevent and restore some of these difficulties in

preterm children.[10, 11] Good quality in mother-child interactions have been reported to

facilitate the infant’s emotional, behavioural, cognitive, and neurobehavioral

development.[12-17] The interactional quality is also found to be related to the child’s

physical health.[18, 19] Compared with infants born at term the preterm infants are likely to

show vague signals that are difficult to read and respond to and are in need of extended care

and support to gain self-regulation.[20, 21] These traits, as well as parent’s psychiatric disease

are known as risk factors for good quality parent-infant interactions.[22, 23] Research

detected significant higher mental health problems following preterm birth than term

birth.[24-26]

The maternal stress reaction following preterm birth has been highlighted as a risk

factor in preterm dyads in several studies.[24-29] Postpartum depression has been identified

as predictor for interactional difficulties in term dyads,[30] and reported as a risk factor for

difficulties in preterm mother-infant dyads.[31] Only a limited number of studies, however,

have explored the nature of mothers’ mental health problems following preterm birth with

psychometric tools, and their impact on mother-infant interaction. Several studies, however,

have explored the post-term effect on maternal mental health.[32-36] Blom et al. interestingly

reported that certain perinatal complications such as preeclampsia, hospitalization, emergency

caesarean, and fetal distress predicted higher depression outcomes in a normal population

sample.[36] An unaddressed trauma reaction is known to predispose for posttraumatic stress

disorder (PTSD) with long term effects on mothers’ mental health. The effect of mothers

postpartum PTSD on mother-infant interaction and infant’s development is less explored.[37]

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In addition only a limited number of studies have explored the maternal posttraumatic stress

responses following preterm birth,[38-45] and their impact on mother-infant interactions.[20,

42, 46]

The results from preterm mother-infant interaction research are contradictory.

Different measurements and definitions being used, as well as the complexity of mother-

infant interactional studies may have contributed to these differences. Some studies have

reported that preterm mothers showed more stimulating behaviour and were emotionally

withdrawn, as well as non-synchronous in their interaction with the child,[20, 21, 47-52] and

others have found no interactional differences between preterm and full term dyads.[20, 53-

58] Korja et al. detected that caregivers’ physical closeness with the infant was more

important to interactional quality than infants’ prematurity.[56] Finally, it is interesting that

several studies have shown that mothers are intensifying their efforts to be available and

supportive to their premature babies’ needs.[59-64] Preterm birth is reported to influence the

interaction between mother and infant.[20, 49, 65] The knowledge of risk factors that may

affect preterm mother-infant interaction is limited.[31, 66-68] The need for further exploration

of the complexity of factors influencing the early mother-infant relationship long-term in

preterm dyads seems essential.[6, 69]

The first aim of our longitudinal study was to explore the associations between

maternal mental health problems following preterm birth, pregnancy and birth complications,

and early preterm mother-infant interaction at six months CA (T2) and 18 months CA (T3).

The second aim of the study was to identify predictors of early mother-infant interaction

quality at T2 and T3.

To our knowledge, these associations have not been explored in other studies.

Psychometric tools and tentative psychiatric diagnosis (anxiety, depression, and PTSR/PTSD)

were used to assess maternal mental health problems following preterm birth.

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It should be noted that this paper is an extension of our previous studies of short- and

long-term maternal mental health problems following preterm birth.[44, 45]

METHOD

Participants

Data were collected in two periods: June 2005-January 2006 and October 2007-July

2008. The psychological responses of 29 consecutive mothers of 35 premature children born

before 33rd week of pregnancy were assessed at a high-specialized neonatal intensive care unit

(NICU) at Oslo University Hospital, Norway. Mothers of severely ill babies that the medical

staff estimated to have poor chance of survival, and non-Norwegian speakers were not

included. The participants stayed in NICU until they were discharged for home. The parents

could participate in the caring of the infant during hospitalisation. The data collection was

performed as soon as the mothers were able to attend an interview following preterm

childbirth: within two weeks postpartum (T0) median 11 days (4-30); then within two weeks

after hospitalization (T1), median time postpartum 2.7 months (0.2-4.7); then at the infant’s

six months corrected age (T2), median time postpartum 8.5 months (7.6-10.4); and at the

infant’s 18 months corrected age (T3), median time following birth 20.6 months (19.2-23.4).

Data collection of mother-infant interaction was collected only at T2 and T3. Mothers of

severely ill babies with uncertain survival and non-native speakers were not included (Figure

1).

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Semi-structured interviews and standardized mental health screening questionnaires

were used to collect data about socio-demographics, the pregnancy and birth, child’s health

status, and mothers’ mental health problems. Medical charts were used to double-check the

data of child’s health status, and pregnancy and birth. The studied sample was homogeneous

regarding high scores on socio-demographic variables such as education, income, and housing

standard. Most mothers were giving first time birth late in their twenties or early thirties. All

lived with the child’s father and none reported any relationship problems (Table 1). The

participating mothers’ mental health problems following preterm birth have been assessed at

T0, T1, T2, T3 and methods and results are described in detail in our earlier papers.[44, 45]

Maternal mental health problems were assessed at every time points (T0, T1, T2, T3) by

standardized psychometric methods with well-established reliability and validity: Impact of

Event Scale (IES) 15-item version, one of the key psychometric assessment methods in

traumatic stress research,[70, 71] the General Health Questionnaire (GHQ) 30item version, a

widely used screening instrument for assessing the presence of distress, psychopathology and

overall well-being,[72, 73] and the State/Trait Anxiety Inventory (STAI-X1/X2)[74] is widely

used to assess maternal anxiety. STAI-X1 measures state anxiety levels reflecting subjective

feelings of tension, apprehension, nervousness and worry. STAIX2 is a measure of trait

anxiety that refers to individual differences in anxiety proneness, i.e. in the tendency to see the

world as dangerous and threatening, and the frequency with which anxiety states are

experienced. Scores above the threshold for identifying a psychiatric case is referred to as a

case score.

Based on all information available in a clinical perusal of the psychometric self-reports

IES, GHQ and STAI of each of the 29 preterm mothers, and blinded to the physical and

sociodemographic characteristics of the mothers and their children, a tentative clinical

diagnosis was made where appropriate based on the clinical descriptions and diagnostic

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guidelines in the ICD-10 Classification of mental and behavioural disorders, and was assessed

by a psychiatrist (last author).

A prevalence of maternal posttraumatic stress responses/disorders (PTSR/PTSD) two

weeks postpartum (T0) of 52% and maternal PTSD at 18 months corrected age (T3) of 23%

was revealed. On the other hand, depression was detected among 24 % of the mothers two

weeks postpartum and among 8% of the mothers at T3. Anxiety decreased from 7% at two

weeks postpartum to zero at T3.

Fourteen of the mothers received psychological support at the hospital during their

infants’ NICU stay. Eleven of these mothers were referred for further psychological treatment

after discharge from the hospital. Altogether, 20 mothers that met the criteria of clinical

diagnoses were referred for adequate psychological treatments such as psychotherapy,

psychopharmacology treatment, and mother-infant interactional treatment. Five of the mothers

refused the referral for psychological treatment, and only one of them filled the criteria for a

tentative clinical diagnosis (PTSD/Depression) at T3. The prevalence of pregnancy and birth

complications and maternal mental health problems following preterm birth are reported in

earlier papers.[44, 45]

Data collected at 2 weeks postpartum (T0) about sociodemographics, physical

complications and maternal mental health problems following preterm birth are presented in

Table 1.

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Table 1. Socio-demographic, physical characteristics, and mental health variables in mothers

giving preterm birth and their children at two weeks postpartum (T0).

Mothers n=29

Age; mean (SD) 33.7 (4.3)

Education > 12 years; n (%) 26 (89.7)

Single parent; n (%) 0 (0)

Unemployed; n (%) 4 (13.8)

Previous psychological treatment; n (%)

8 (27.6)

Chronic illness; n (%) 2 (6.9)

Tot. no. of children; median (quartile low,upper) 2 (1,2)

Previous pregnancies; median (quartile low,upper) 1 (0,2)

Previous childbirths; median (quartile low,upper) 0 (0,1)

First time mothers; n (%) 18 (62.1)

IVFa pregnancy; n (%) 8 (27.6)

Bleeding in pregnancy; n (%) 19 (65.5)

Preeclampsia; n (%) 4 (14.3)

Caesarean; n (%) 17 (58.6)

Mental Health Variables:b

IES total (0-75); median (quartile low,upper) 18 (11,30)

IES case score >18; n (%) 13 (44.8)

GHQ Likert score (0-90); n (%) 40 (15.4)

GHQ case (0-30): n (%) 12.8 (7.5)

GHQ case score >5; n (%) 23 (79.3)

STAI-X1 (0-40); mean (SD) 21.5 (2.8)

STAI-X1 case score >19; n (%) 20 (69)

STAI-X2 (0-80); mean (SD) 44.0 (4)

STAI-X2 case score >39; n (%) 27 (93.1)

PTSR Tentative clinical diagnosis; n (%) 15 (51.7)

Children n=35

Girl; n (%) 17 (48.6)

Boy; n (%) 18 (51.4)

Twinc; n (%) 14 (40)

Gestational age (weeks);

Median (range)

Mean (SD)

29 (24-32)

28.5 (2.6)

Birth weight (g);

Median (range)

Mean (SD)

1185(623-2030)

1222(423)

Apgar score at 1 minute; mean (SD) 6,3 (2.3)

Apgar score at 5 minute; mean (SD) 7.6 (2.0)

Apgar score at 10 minute; mean (SD) 8.3 (1.0)

Oxygen supply > 28 days; n (%) 19 (54)

IVHd; n (%) 7 (20.0)

a In vitro fertilization/Assisted fertilization.

bThe Impact of Event Scale (IES) 15 item with scoring range 0(not at all) to 5 (very much), The General Health Questionnaire (GHQ)30 items

Likert scores with weights 0-1-2-3 and case scores with weights 0-0-1-1, The Spielberger State/Trait Anxiety Inventory (STAI-X1/X2) 10

item/20 item with scoring range 1-2-3-4. The STAI-X1 10 item was constructed since both STAI-X1 12 item and 20 item had been used and

only 10 items overlapped. Tentative Clinical Diagnosis: Posttraumatic Stress Responses (PTSR).

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cTwo of the twins were raised as singleton as their twin sibling were stillborn.

dIntraventricular hemorrhage grade 1-4 following birth.

Measures

Mother–infant interaction in a free-play situation was video recorded at six and 18

months CA. According to Clark (1985) by six months of age, dyadic mutuality and dyadic

regulatory processes are perceptible while at 18 months, the infant's own communication

skills are easier to identify in interaction.[75] The interaction situation was recorded in a

consultation room at the psychiatric clinic for children and families situated in the same

building as the hospital the children were born in, except for four video recordings at 18

months CA that were recorded in their homes. The recordings were performed when child was

awaken and interested in a play session with mother. Recordings were stopped and performed

later when child became too distressed or sleepy to play. A therapist (first author) instructed

the mothers about the procedure. For the video recording, the mother and the infant were

placed on a soft mat with age-appropriate toys. Instructions by the investigators given to the

mother prior to the video recording were: “This is a free-play time with your child. You can

use the toys, or you can play without the toys. Try to play or be with your infant as you

usually would be”. Video recordings were obtained from all mother-infant pairs.

The recordings were five minutes long. The mother-infant interaction in the free-play

situation was analysed using the Parent-Child Early Relational Assessment (PCERA)

method.[75] The PCERA is developed to assess affective and behavioural aspects that both

the parent and infant bring into the interaction,[75] and the validity of the free play situation

has been established.[76, 77] Video recordings allows thoroughly analysis of the interactions

several times and in short and slow sections that can identify areas of strength and of concern

in the mother-infant interplay. The PCERA consists of 29 parental items, 28 infant items and

eight dyadic items. The assessment rates the frequency, duration and intensity of the infant's,

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parent's and dyad's behaviour. The parental items comprise the parent's positive and negative

affect, expressed attitude toward the infant, sensitivity and contingent response to the infant's

cues, mirroring the infant's feeling, capacity to structure, behavioural involvement and

parental style. The infant items comprise expressed positive and negative affect and

characteristic mood, behaviour/adaptive abilities, activity level and communication skills. The

dyadic items comprise affective quality of interaction and mutuality of interaction.

All items were rated on a 5-point “Likert” scale. The scores 1 and 2 describe an area of

concern, the score 3 describes an area of some concern and the scores 4 and 5 describe an area

of strength. A trained coder made the assessment. The coder was unaware of the infant's

background and clinical status. Additionally, to estimate the interrater reliability from the

study data, 20% of all assessments were double-scored by another trained coder. The study

data was assessed by calculating the mean of the agreement percentage of the raters' overall

agreement. Agreement equal or above 80% is considered good, 50-80% is considered

moderate, and lower than 50% is considered poor. The mean of interrater agreements was

80.3% in six months CA and 81% in 18 months CA.

The PCERA items were organized in eight scales according to Clark,[75] before the

data analysis: “Maternal positive affective involvement PS1”, “Maternal negative affect &

behaviour PS2”, “Maternal intrusiveness PS3”, “Infant positive affect PS4”, “Infant quality

of play PS5”, “Infant dysregulation PS6”, “Dyadic mutuality & reciprocity PS7”, and “Dyadic

disorganization & tension PS8”. PCERA high scores (4-5) always indicate positive affect and

behaviour or lack of negative affect and behaviour. The Cronbach alpha coefficients for

calculating the internal consistency of PCERA subscales in our study were satisfactorily and

were .95,.86,.86, .90,.87,.85,.80,.86 for PS1-PS8 at six months CA (T2), and

.89,.81,.82,.92,.89,.75,.73,.79 for PS1-PS8 at 18 months CA (T3).

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The PCERA scale has been used in several studies to explore the quality of preterm

mother-infant interactions.[31, 78-82]

Statistical methods

Continuous variables are presented as means (SD) or if skewed, as median and range.

Categorical variables are given as proportions and percentages. Paired-sample t-test was used

for comparison of the PCERA means scores at T2 and T3. Differences in the quality of

mother-infant interactions measured by the PCERA scales were explored with independent-

samples t-test. As grouping variable we used mothers’ case scores above threshold for

identifying psychiatric symptoms (0=no, 1=yes) in IES, GHQ, STAI and the tentative

diagnostic assessments at four time points; two weeks PP (T0), two weeks after

hospitalization (T1), six months CA (T2), and 18 months CA (T3) (Figure 2a and 2b). A more

detailed description of mothers’ case scores in IES, GHQ, STAI and the tentative diagnostic

assessments are available in our earlier papers.[44, 45]

The association between variables at T3 were assessed using Pearson’s correlation

coefficient (Table 2).

Stepwise regression analysis with a forward selection method was used to identify possible

predictors of the PCERA results at T3 (Table 3). At most three variables at T3 with the

strongest bivariate associations above 0.3 were included in the multivariable linear regression

model; PS1 (STAI-X2 case, STAI-X2 sum, GHQ Likert), PS2 (Bleeding in pregnancy, GHQ

case, GHQ Likert), PS3 (STAI-X2 case, Bleeding in pregnancy, Parity/STAI-X2 sum), PS4

(Bleeding in pregnancy, GHQ case), PS5 (Bleeding in pregnancy, Apgar 5 min), PS6 (Family

size, Acute Caesarean, Bleeding in pregnancy), PS7 (Bleeding in pregnancy, GHQ case,

STAI-X2 case), and PS8 (Bleeding in pregnancy, GHQ case, CH<grade 3). A careful check of

the model assumptions, including an investigation of residual plots, did not reveal any

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violation of the assumptions. All analyses were performed in SPSS version 20. Two-sided

statistical tests were applied and a 5 % statistical significance level was chosen.

Ethics

Written informed consent was obtained from participants prior to the study start. The

study protocol was approved in 5 May 2005 and 19 April 2007 by the National Committee for

Research Ethics (S-05068 and S-07096b) and 1 April 2005 and 12 March 2007 by the Data

Inspectorate (12360 and 07/1088). The study protocol was carried out in accordance with the

Declaration of Helsinki.

For ethical reasons the mothers that reported mental health problems and had case

scores above the threshold for identifying psychiatric symptoms in IES, GHQ and STAI were

assessed and referred for adequate psychological treatment. In this study, we looked for

mental health problems in mothers at four points from the time of birth to two years

postpartum. A no referral procedure could have caused unnecessary suffering for both

mothers and children.

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RESULTS

Associations between maternal mental health problems following preterm birth,

pregnancy and birth complications, and early preterm mother-infant interaction at six

months CA (T2) and 18 months CA (T3)

The paired sample t-test of the results of the PCERA showed no significant difference

for the PCERA mean scores from six months to 18 months corrected age (CA). For that

reason the presented results from correlation and regression analysis are based only on the

mean scores from 18 months CA. The results of the PCERA revealed mean scores in three of

the scales in the area of moderate concern and five scales in the area of no concern. The

results of the PCERA is presented in Table 2.

Group differences in mother – infant interaction quality at T2 and T3 for mothers with and

without psychometric case scores at T0, T1, T2, and T3

The results of the independent-samples t-test showed significant group differences at

T2 and T3 between the mothers with case scores above the threshold for identifying a

psychiatric case compared to mothers without case scores; in IES that measure symptoms of

posttraumatic stress following preterm childbirth, in GHQ which measure symptoms of

general psychological distress, and in tentative PTSR diagnosis at T0 (Figure 2a and 2b).

Mothers’ identified with case scores of general psychological distress (GHQ) at T3 also

showed significant better results at the .05 level (2-tailed)* in two PCERA scales at T3; PS7

Dyadic mutuality and reciprocity (N0/N1=24/8, mean 3.1/3.7*), and PS8 Dyadic

disorganization and tension (N0/N1=24/8, mean 3.9/4.4*). Unexpectedly, the mothers with

case scores (1=yes) at T0 showed significantly better quality in mother-infant interaction in

six (T2) and two (T3) subscales of the PCERA than mothers with no (0=no) case scores

(Figure 2a and 2b). Tentative depression or anxiety diagnosis (0=no, 1=yes) as a grouping

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variable showed no significant group differences regarding the quality of the mother-infant

interaction.

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Associations between maternal mental health problems and mother-infant interactional

quality at T3

In the bivariate correlation analyses, we revealed a positive correlation between better

interactional quality measured by PCERA and higher levels of maternal mental health

problems measured by psychometric means at T3. High levels of maternal psychological

distress measured by GHQ Likert and case scores correlated with high levels of PCERA

scores in three scales and maternal psychological distress measured by GHQ case sum scores

correlated with two scales. High levels of maternal trait anxiety measured by STAI-X2 sum

scores were associated with high levels of PCERA scores in two scales and maternal trait

anxiety measured by STAI-X2 case scores correlated with three scales (Table 2).

Associations between pregnancy/ birth complications, maternal variables and mother-infant

interactional quality at T3

The strongest correlations were inversely and found between a pregnancy complication

“Bleeding in pregnancy” and the following six PCERA scales: “Maternal negative affect and

behaviour (PS2), Maternal intrusiveness, intensity, and inconsistency (PS3), Infant positive

affect, communicative, and social skills (PS4), Infant quality of play, interest, and attention

(PS5), Dyadic mutuality and reciprocity (PS7), and Dyadic disorganization and tension

(PS8)”.

Two infant complications following birth were correlated with two of the PCERA

scales. Infant health scores at the infant’s “Apgar scores at 5 minutes postpartum” correlated

positively with the “Infant quality of play, interest, and attention (PS5)” scale. Infant stroke by

“Intraventricular Haemorrhage grade 1 or 2 (IVH)” closely following birth” correlated

inversely with the “Maternal negative affect and behaviour (PS2)” scale (Table 2).

Three maternal variables correlated with two of the PCERA scales. Parity (number of

previous births with child survival) and the scale “Maternal intrusiveness, intensity and

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inconsistency (PS3)” were positively correlated. Family size (number of children in the

family) and the “Infant dysregulation and irritability (PS6)” scale inversely correlated. “Acute

caesarean” correlated positively with high scores on the same scale.

Associations between exposure variables, e.g. IVF treatment, pre-and postnatal

maternal health problems and pregnancy and birth/postnatal complications, were not

significant.

Table 2. Pearson correlations coefficients at T3 (18 months corrected age) between the PCERA scales, the

maternal psychometric means, and the individual characteristics of the mothers and infants. (N=32). Mean

values, range scores and minimum and maximum scores for PCERA subscales are reported in the last

row of this table.

PCERA

PS1

Maternal Positive

affective

involvement

PCERA

PS2

Maternal

Negative

affect &

Behavior

PCERA PS3

Maternal Intrusiveness

Insensitivity

Inconsistency

PCERA PS4

Infant Positive affect Communicative

& Social skills

PCERA

PS5 Infant Quality of

play

Interest Attention

PCERA

PS6

Infant Dysregu -lation

Irritability

PCERA

PS7

Dyadic Mutuality

Reciprocity

PCERA

PS8

Dyadic Disorganization

Tension

GHQ Likert

sum score .39*

.37*

.35* .16 .12 .05 .30 .28

GHQ case

sum score

.36* .36* .06 .12 .07 .17 .26 .31

GHQ

case > 5

.26 .40* .30 .33 .29 .21 .41* .43*

STAI-X2

sum score

.46** .21 .39*

.09 -.03 .08 .25 .19

STAI-X2

case > 39

.48* .36* .57** .19 .06 .07 .32 .32

Parity

.07

.18 .39* .24 .10

.01

.31 .33

CH< grade

3a

-.21 -.28 -.35* -.20 -.23 -.15 -.30 -.35

Apgar

at 5

min.

-.01 .09 .20 .22 .35* -.12 .18 .19

Bleeding in

pregnancy

-.22 -.45** -.56** -.53** -.55** -.33 -.46** -.52**

Family

sizeb

-.09 -.12 .07 -.02 -.16 -.45* .01 .00

Acute

Caesarean

.14 .14 .13 .01 .03 .39* .07 .22

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Mean/

Range c

(Min-Max)

3.8/2.5

(2.3-4.8)

4.6/1.6

(3.4–5.0)

4.2/2.0

(3.0–5.0)

3.2/3.0

(1.9–4.9)

4.0/2.2

(2.7–4.9)

4.5/1.3

(3.7–

5.0)

3.3/2.8

(2.0–4.8)

4.0/2.0

(3.0–5.0)

*Correlation is significant at the .05 level (2-tailed). **Correlation is significant at the .01 level (2-tailed).

a CH< grade 3 refers to Cerebral Hemorrhage grade 1 or 2 closely after birth.

b Family size refers to the number of children in the family.

c Rates 1 and 2 in PCERA subscale; “Area of concern”. Rate 3 in PCERA subscale; “Area of moderate concern”. Rates 4 and 5 in PCERA

subscale; “Area of no concern”.

Predictors of mother-infant interactional quality at T3

In the multivariable linear regression analyses we revealed that the pregnancy

complication variable “Bleeding in pregnancy” was a significant predictor (p<0.01) of lower

scores in preterm mother-infant interaction in six of the PCERA domains, including both of

the Dyadic scales (Table 3). Trait anxiety (STAI-X2) case and sum score are significant

predictors for higher quality in preterm mother-infant interaction in the “Maternal positive

affect domain (PS1)” (p<0.01) and in the “Maternal intrusiveness (PS3)” domain (p<0.05),

consecutively. Higher “Number of children in the family” predicts lower interaction quality in

the “Infant dysregulation and irritability (PS6)” scale (p<0.05). Adjusted R2 showed that the

predictors explain from 17 to 39 % of the variance in different PCERA scales.

Table 3. Significant results of the multivariable regression analyses with the selected

independent variables to predict mother-child interaction following preterm birth at T3 (18

months corrected age). Unstandardized (B) and standardized (Beta) regression coefficients.

(N=32)

Predicting variable B CI Beta P value R2

adj.

PCERA subscales:

PS1 (Maternal positive

affective involvement)

STAI-X2 case .53 (.17, .89) .48 .005 .21

PS2 (Maternal negative

affect & behavior)

Bleeding in pregnancy -.21 (-.37, -.06) -.45 .009 .18

PS3 (Maternal

intrusiveness)

Bleeding in pregnancy

STAI-X2 sum score

-.29

.03

(-.45, -.13)

(.01, 06)

-.53

.35

.001

.017

.39

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PS4 (Infant positive

affect)

Bleeding in pregnancy -.43 (-.68, -.17) -.53 .002 .26

PS5 (Infant quality of

play)

Bleeding in pregnancy -.35 (-.56, -.15) -.55 .001 .27

PS6 (Infant

dysregulation)

Family size

-.24

(-.42, -.06)

-.45

.011

.17

PS7 (Dyadic mutuality &

reciprocity )

Bleeding in pregnancy

-.33

(-.56, -.09)

-.33

.008

.21

PS8 (Dyadic

disorganization &

tension)

Bleeding in pregnancy

-.32

(-.51, -.12)

-.52

.002

.25

PCERA subscales were used as dependent variables (At most three variables with strongest bivariate association above 0.3 were used as

independent variables):

PS1 (STAI-X2 case, STAI-X2 sum score, GHQ Likert sum score), PS2 (Bleeding in pregnancy, GHQ case, GHQ Likert sum score),PS3 (STAI-X2

case, Bleeding in pregnancy, Parity/STAI-X2 sum score), PS4 (Bleeding in pregnancy), PS5 (Bleeding in pregnancy, Apgar at 5 minutes), PS6

(Family size, Acute Caesarean), PS7 (Bleeding in pregnancy, GHQ case), PS8 (Bleeding in pregnancy, GHQ case).

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DISCUSSION

The study revealed significant associations between pregnancy and birth

complications, maternal postpartum mental health, and the quality of preterm mother-infant

interaction. The most surprising results in our study were the detection of 1; “Bleeding in

pregnancy” as a predictor of lower quality in preterm mother-infant interaction in six of eight

PCERA scales, and 2; the association between high levels of maternal mental health problems

and better mother-infant interactional quality.

The predictor “Bleeding in pregnancy” is interesting. No other study has, to our

knowledge, revealed a physical complication in pregnancy that predicts a possible weaker

quality of the mother-infant interaction following preterm birth. With reference to our

previous papers, “Bleeding in pregnancy”, was detected as a predictor of low levels in

maternal mental health symptoms, while, a sudden complication later in pregnancy

“Preeclampsia”, predicted high levels of maternal mental health problems following preterm

birth.[44, 45] As “Bleeding in pregnancy” usually occurs before 22 weeks of pregnancy it

may be experienced as an early warning sign for possible pregnancy complications by the

mother. A possible hypothesis may be that early complications in pregnancy and

complications late in pregnancy influence the mother differently in the way she relates to her

unborn child and how her transition into motherhood alternates. Early bleeding in pregnancy

could leave the mother-to-be with the impression that her child is at risk and when preterm

birth becomes reality, it may confirm her fear of loss. Given such an enduring threatening

impression, the mother can be expected to be anxious and alert, preventing her from relaxing

and taking pleasure in the mother-infant interaction, and rather initiating negative affect and

intrusiveness which may also entail dyadic disorganization and tension.

On the other hand, the mother without prior early warning signs is likely to have been

quite “undisturbed” in her transition process to prepare for motherhood until later in her

pregnancy. “Preeclampsia” and a sudden preterm birth induces a serious situation for both

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mother and child and both may risk non-survival. When mother experiences hope for infant

survival, we may assume that a prior “undisturbed” transition process into motherhood is

likely to increase her efforts to attain the very best mother-infant interaction.

Attachment theory supports our hypothesis that loss or possible loss can be seen as

serious threats to attachment.[83] A growing number of research show that mothers’

attachment pattern is associated with the mother-infant interaction,[84, 85] and an assessment

of mothers’ attachment pattern would possibly have given a valuable perspective to our

results.

Unexpectedly, our results showed that high levels of maternal mental health problems

following preterm birth were significantly associated with better quality in preterm mother-

infant interaction. In regression analysis, we found that high levels of maternal anxiety

measured by STAI-X2 predicted better mother-infant interaction in two PCERA scales at T3.

In our previous studies we found an association between STAI-X2 and general psychological

distress outcomes following preterm birth,[44, 45] and another study revealed an association

between STAI-X2 and posttraumatic stress outcomes following term birth.[86] With reference

to these studies we may suggest that there is an significant association between high levels of

mental health problems following preterm birth and better quality in two PCERA scales at T3.

In the independent-samples t-test, we also found that mothers with symptoms of posttraumatic

stress, general psychological distress and anxiety at 2 weeks postpartum (T0) showed

significantly better quality in mother-infant interaction on six PCERA scales at six months

(T2) and on two PCERA scales at 18 months corrected age (T3).

It is theoretically interesting that our results imply that high levels of maternal mental

distress improve the preterm mother–infant interaction. At first glance, this result seems to

contradict the well-known connection between high levels of maternal depression and high

risk mother-infant interactions.[31, 87-89] It should be noted that we found quite low

prevalence of depression among the mothers participating in this study.[44, 45] Instead, we

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found high levels of posttraumatic stress reactions. PTSD following childbirth is

acknowledged by several researchers to be potentially different from PTSD following other

traumatic incidences.[37] The culturally positive connotation of giving birth, the mother-child

connection, the transition from pregnancy to giving birth, and the formal care setting the birth

incident takes place in are all matters that may have an impact on PTSD following preterm

birth. Several studies have reported that many people experience positive psychological

growth after struggling with trauma.[90, 91] Maternal posttraumatic stress reaction following

preterm birth is characterized by a prior physical trauma where survival of the mother and the

baby may be at risk. Is it possible that maternal posttraumatic stress reactions following

preterm birth helps the mother to focus her attention towards her premature baby’s wellbeing?

Our findings may imply that the posttraumatic stress response activates and helps the mother

cope over time with a tremendously stressful situation, and furthermore helps her stimulate

the prematurely born child’s healthy development. Several studies support our view.[60-62,

64] However, other studies that have explored maternal mental health problems following

preterm birth and preterm mother-child interactions have reported results that contradict with

our findings.[42, 50, 81, 92] Studies that have used the PCERA scale in studying preterm

dyads, however, did not find depression to be a significant predictor of PCERA outcome at

six, 12, or 16 months CA.[31, 79] The socio-demographic variable “Family size” predicted

low interactional quality in one of the PCERA scales. In our study, the mothers with preterm

babies that had siblings showed significantly lower scores in the “Infant dysregulation scale

(PS6)” in the PCERA. Our result is supported by two studies in the 1970’s and 1980’s that

found the preterm infant’s birth-order to affect the mother-child interaction.[93, 94] An

explanation for their results was the mother’s divided attention between the infant and other

siblings.

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Strength/limitations

The results from a small and explorative study have low statistical power and low

external validity,[95] and one should be cautious about generalising from the study. In most

studies there is also a possibility that confounding variables are not included in the analysis

that should have been. In our study such factors could have been assessment of mothers’

attachment patterns, the effect of psychological assessment and referral procedure and an

assessment of the comforting conditions for mother-infant interactions in the hospital.

However, our study results may still be of value for future research that will systematically

explore the complexity of factors influencing early preterm mother-infant interaction in a

broader sense.

The participants in this study were included consecutively and both single and multiple

births were included, thus minimizing selection bias. Our sample was homogeneous in socio-

economic background (SES). However, the mothers had higher educational attainments,

greater age and higher socioeconomic status, higher number of twins and higher rate of

previous psychological treatment than would be found in a typical population of mothers who

deliver preterm in our country. In this sample we found no indication of significant

differences in parental challenges between participants with singletons or twins that needed to

be controlled for. Besides high prevalence of earlier psychological treatment among the

mothers in our sample, no other collected data indicated that mental distress had impact on

their psychosocial function in everyday life before the actual preterm birth incident.

Regarding research on quality of the preterm mother-infant interaction, it has been considered

that risk factors other than preterm birth itself have been sources of bias in many studies.[20,

48, 96] In our study, we have controlled for high risk socio-economic backgrounds.

It is a limitation that the video-procedure of PCERA could not be followed for the four

dyads that were recorded in their homes and not in the clinic, as were the others. On the other

hand, these dyads would not have participated if the recordings were not made in their homes.

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It is a limitation that interrater reliability was not checked for tentative clinical diagnosis. The

prediction model used in this study needs further validation by future studies.

CONCLUSIONS

Our study detected a correspondence between early pregnancy complications and

lower quality of preterm mother-infant interaction, and an association between high levels of

maternal mental health problems and better quality in preterm mother-infant interaction.

Early intervention programs should be considered to mothers who give preterm birth to

support mother-infant interaction.

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Acknowledgements

The authors would like to thank the families that participated in the study, the staff of the

maternity ward at the neonatal intensive care unit at the National Hospital, Oslo and Sari

Ahlqvist-Björkroth who coded and Tanja Lipasti who recoded the PCERA data. In particular,

we want to thank the parents who participated in the study.

Contributorship statement

ARM initiated the study, collected, and organized the data. ARM and AHP performed the

statistical analyses. ARM, PN, SB, AHP and THD wrote the article.

Competing interests

We have no information of disclosure of interests.

Funding

This work was supported by the Centre for Child and Adolescent Mental Health, Eastern and

Southern Norway and the University College of Oslo and Akershus.

Data sharing statement

The full dataset is available from the corresponding author Aud R.

Misund([email protected]).

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209x297mm (300 x 300 DPI)

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STROBE 2007 (v4) Statement—Checklist of items that should be included in reports of cohort studies

Section/Topic Item

# Recommendation Reported on page #

Title and abstract 1 (a) Indicate the study’s design with a commonly used term in the title or the abstract 1

(b) Provide in the abstract an informative and balanced summary of what was done and what was found 1

Introduction

Background/rationale 2 Explain the scientific background and rationale for the investigation being reported 3-4

Objectives 3 State specific objectives, including any prespecified hypotheses 4

Methods

Study design 4 Present key elements of study design early in the paper 5

Setting 5 Describe the setting, locations, and relevant dates, including periods of recruitment, exposure, follow-up, and data

collection

5

Participants 6 (a) Give the eligibility criteria, and the sources and methods of selection of participants. Describe methods of follow-up 5

(b) For matched studies, give matching criteria and number of exposed and unexposed

Variables 7 Clearly define all outcomes, exposures, predictors, potential confounders, and effect modifiers. Give diagnostic criteria, if

applicable

5-9

Data sources/

measurement

8* For each variable of interest, give sources of data and details of methods of assessment (measurement). Describe

comparability of assessment methods if there is more than one group

5-9

Bias 9 Describe any efforts to address potential sources of bias 5 -9

Study size 10 Explain how the study size was arrived at 5

Quantitative variables 11 Explain how quantitative variables were handled in the analyses. If applicable, describe which groupings were chosen and

why

9-10

Statistical methods 12 (a) Describe all statistical methods, including those used to control for confounding 9-10

(b) Describe any methods used to examine subgroups and interactions 9-10

(c) Explain how missing data were addressed

(d) If applicable, explain how loss to follow-up was addressed

(e) Describe any sensitivity analyses

Results

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For peer review only - http://bmjopen.bmj.com/site/about/guidelines.xhtml

BMJ Open

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Page 137: BMJ Openhave explored the postterm effect on maternal mental health.[26-30] Blom et al. interestingly reported that certain perinatal complications such as preeclampsia, hospitalization,

For peer review only

Participants 13* (a) Report numbers of individuals at each stage of study—eg numbers potentially eligible, examined for eligibility, confirmed

eligible, included in the study, completing follow-up, and analysed

5

(b) Give reasons for non-participation at each stage 5

(c) Consider use of a flow diagram 5

Descriptive data 14* (a) Give characteristics of study participants (eg demographic, clinical, social) and information on exposures and potential

confounders

5-7

(b) Indicate number of participants with missing data for each variable of interest

(c) Summarise follow-up time (eg, average and total amount) 5

Outcome data 15* Report numbers of outcome events or summary measures over time 5-9

Main results 16 (a) Give unadjusted estimates and, if applicable, confounder-adjusted estimates and their precision (eg, 95% confidence

interval). Make clear which confounders were adjusted for and why they were included

11-13

(b) Report category boundaries when continuous variables were categorized

(c) If relevant, consider translating estimates of relative risk into absolute risk for a meaningful time period

Other analyses 17 Report other analyses done—eg analyses of subgroups and interactions, and sensitivity analyses 11-13

Discussion

Key results 18 Summarise key results with reference to study objectives 14

Limitations

Interpretation 20 Give a cautious overall interpretation of results considering objectives, limitations, multiplicity of analyses, results from

similar studies, and other relevant evidence

2 and 16

Generalisability 21 Discuss the generalisability (external validity) of the study results 2

Other information

Funding 22 Give the source of funding and the role of the funders for the present study and, if applicable, for the original study on

which the present article is based

18

*Give information separately for cases and controls in case-control studies and, if applicable, for exposed and unexposed groups in cohort and cross-sectional studies.

Note: An Explanation and Elaboration article discusses each checklist item and gives methodological background and published examples of transparent reporting. The STROBE

checklist is best used in conjunction with this article (freely available on the Web sites of PLoS Medicine at http://www.plosmedicine.org/, Annals of Internal Medicine at

http://www.annals.org/, and Epidemiology at http://www.epidem.com/). Information on the STROBE Initiative is available at www.strobe-statement.org.

Page 38 of 38

For peer review only - http://bmjopen.bmj.com/site/about/guidelines.xhtml

BMJ Open

123456789101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960

on March 16, 2020 by guest. Protected by copyright. http://bmjopen.bmj.com/ BMJ Open: first published as 10.1136/bmjopen-2015-009699 on 4 May 2016. Downloaded from