bmj open · date submitted by the author: 25-apr-2014 complete list of authors: miranda, rafael;...
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Electromyographic activity of preterm children in kangaroo care: a cohort study
Journal: BMJ Open
Manuscript ID: bmjopen-2014-005560
Article Type: Research
Date Submitted by the Author: 25-Apr-2014
Complete List of Authors: Miranda, Rafael; Instituto de Medicina Integral Prof. Fernando Fiqueira, Pós-graduação Cabral Filho, José; Instituto de Medicina Integral Prof. Fernando Fiqueira, Pós-graduação Diniz, Kaísa; Instituto de Medicina Integral Prof. Fernando Fiqueira, Pós-graduação Lima, Geisy Maria; Instituto de Medicina Integral Prof. Fernando Fiqueira, Unidade Canguru Vasconcelos, Danilo; Instituto de Medicina Integral Prof. Fernando Fiqueira, Pós-graduação
<b>Primary Subject Heading</b>:
Paediatrics
Secondary Subject Heading: Public health
Keywords: PAEDIATRICS, Developmental neurology & neurodisability < PAEDIATRICS, Community child health < PAEDIATRICS
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Electromyographic activity of preterm children in kangaroo care: a cohort study
Rafael Moura Miranda1; José Eulálio Cabral Filho
2; Kaísa Trovão Diniz
3; Geisy Maria
Souza Lima4; Danilo de Almeida Vasconcelos
5.
Affiliations: 1,2,3,5
Post Graduate Program of Instituto de Medicina Integral Prof.
Fernando Figueira (IMIP) – Recife – Brasil. 4Instituto de Medicina Integral Prof.
Fernando Figueira (IMIP) – Recife – Brasil.
Address correspondence to: Rafael Moura Miranda. Rua: Paula Batista, 270, Edifício
Morada Paula Batista, apto 203. Recife-PE/ Brasil; CEP: 51030-080.
Key-words: Kangaroo-Mother Care Method, Muscle Tonus, Electromyography, Child
Development, Motor Activity.
Word count: 2214
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ABSTRACT
Aim: The aim of this study was to compare the electromyographic activity in preterm
newborns placed or not in kangaroo care.
Methods: A cohort study was carried out at the Instituto de Medicina Integral Prof.
Fernando Figueira (IMIP), Recife, Brazil. Children were included if they were preterm
(38 newborns) with a gestational age of 27 to 34 weeks, and a corrected age of 35 weeks
at the time of the first electromyographic examination and had not been previously in
kangaroo care or term newborns (26 newborns) with a gestational age of 38 to 41
weeks. Surface electromyography (EMGs) was used to investigate muscle activity in
the brachial biceps at rest. The mean values for the groups and intervals were analyzed
using analysis of variance for repeated measurements and multiple comparisons.
Results: The RMS values for all the evaluations showed significant differences (F(5,108)=
56.69; p<0.001). The multiple comparisons showed that, in the preterm group in
kangaroo care, the RMS was greater at 48h compared to 0h, but not in the group not in
kangaroo care. The RMS in the term equivalent aged group in kangaroo care was also
greater when compared to the term group.
Conclusions: The kangaroo position increases electromyographic activity in the
brachial biceps of preterm newborns and those who have reached an age equivalent to
term. One limitation of the present study is the absence of a group of preterm newborns
not in kangaroo care followed up to age equivalent to term.
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Strengths and limitations of this study
▪ The results of the study add new information about the effects of kangaroo care for the
preterm.
▪ The early initiation of the kangaroo position may, like other early intervention
programs, have a positive influence on the motors responses of the child, thereby
making it possible to influence the motor development of the preterm newborn.
It is important to point out the innovative nature of this study, since there is a lack of
studies specifically evaluating electromyographic activity in children in kangaroo care.
▪ The sample size lower than the estimate is a factor that may diminish the reliability of
our findings. However with a sample power of 90%, the large differences found
between the means and the statistically significant figures may support our inference.
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INTRODUCTION
The Kangaroo Method (KM) is an intervention that aims to improve the health
of preterm low-weight newborns.1 There is evidence that the method provides various
benefits. These include an increase in body temperature,2,3
stabilization of cardio-
respiratory frequency,3,4
improved oxygenation of the brain,5
improved behavior (crying
and sleep),6-8
a reduction in pain4,9,10
and greater adherence to and duration of
breastfeeding.11-13
The method is also associated with a reduction in morbidity and
mortality,14,15
infections14
and the duration of hospitalization.15
The main feature of the method is the kangaroo position, whereby the child
remains in a vertical position supported on its stomach with limbs flexed, dressed in
light clothes, maintaining skin-to-skin contact with the adult’s thorax1. This position
allows the child to receive sensory, vestibular and postural stimuli and its effect on
motor responses in the newborns has thus aroused some interest among investigators.16
Recently, some studies16,17
have shown an increase in electromyographic activity in
preterms after different periods of time in kangaroo care (up to 96h) and that this
increase persists until an age equivalent to term. These results were pioneering, although
no study has yet been conducted in which these responses are compared with those of
preterm newborns not in kangaroo care and those of term newborns. The aim of this
study was thus to compare electromyographic activity in preterm newborns in kangaroo
care and newborns not placed in this position.
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METHODS
Participants
A cohort study was carried out, between July 2012 and January 2013, at the
Instituto de Medicina Integral Prof. Fernando Figueira (IMIP), in Recife, Brazil, with 64
newborns, 38 preterm hospitalized in the Kangaroo Unit and 26 term in the IMIP
nursery.
The IMIP’s Kangaroo Unit covers a surface-area of 600 m2
and has a ward with
22 beds for clinically stable preterm newborns (with a respiratory frequency of between
30–60 inspirations per minute, a heart rate of between 120–160 beats per minute,
peripheric oxygen saturation of over 89%, absence of signs of respiratory distress,
absence of cyanosis or pallor and pain.) The newborns had to tolerate food, to breathe
without the use of an apparatus and to weigh more than 1,250 grams.
The Kangaroo Unit provides medical and nursing services and also speech
therapy and physiotherapy. In this unit, the newborns, when referred by the medical
services, are evaluated and undergo an early stimulation program.
Newborns were included in the preterm group if they had a gestational age of 27
to 34 weeks and a corrected age of 35 weeks at the time of the first electromyographic
examination, and had not previously been in kangaroo care. Children were included in
the group of term newborns if they had a gestational age of 38-41 weeks. The exclusion
factors for all the newborns were: Apgar lower than 7 after 5 minutes, a history of grade
III or IV intracranial hemorrhage (diagnosed by way of transfontanelar ultra-sound and
included in medical records), convulsions, congenital infections (cytomegalovirus,
rubella, toxoplasmosis, syphilis and vertically transmitted HIV), malformations of the
Central Nervous System (hydrocephaly and genetic syndromes), infections of the
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central nervous system (meningitis or encephalitis), congenital cardiopathy, traumas
during delivery (injuries to the brachial plexus, dislocation of the hip and pelvis
fractures) and gastro-esophageal reflux disorder.
All these inclusion and exclusion factors were evaluated using data collected
from the medical records of patients evaluated by neonatologists at the Neonatal
Intensive Care Unit, the Kangaroo Unit and the IMIP nursery.
A non-probabilistic convenient sample of newborns was selected, the size of the
sample being based on a previous study 17
that found variance of 2.6 in
electromyographic activity and estimated the minimum difference between means to be
2 µV. With an alpha error of 0.05 and power of 90%, 21 individuals were calculated for
each group.
The project for this study was submitted to the IMIP’s Ethics Committee for
Research involving Human Beings and was approved (Nº 1,902). The parents or
guardians who agreed to participate signed terms of free informed consent.
Collection procedure
The electromyographic signal was obtained using a Miotool 400 ®
electromyograph (Miotec Equipamentos Biomédicos – Brazil). A system of self-
adhering Ag/AgCl channels and electrodes (Meditrace 100®
) was used to connect the
equipment to the body of the child under examination. The electromyograph was
connected to a laptop with Myographic 2.0 software (Miotec Equipamentos Biomédicos
- Brazil) to process the myoelectrical records. The sampling frequency was 2000 Hz and
the electromyograms were amplified 2000 times.
The electromyographic signal was captured using two electrodes placed on the
central portion of the left brachial bíceps muscle, between the motor point and the
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myotendinous junction, parallel to the muscle fibers, as recommended by the SENIAM
(Surface Electromyography for the Non-Invasive Assessment of Muscles) project.18
The
electrodes were adjusted to ensure the distance between them did not exceed 20 mm and
the reference electrode was always placed on the lateral malleolus contralateral to the
muscle under evaluation.
When the measurements were made, the child was placed on a small wedge-
shaped cushion at angle of 30° relative to the horizontal plane. Electromyographic
activity was captured with the children in Brazelton state 4 or 5 (inactive alert or alert
with activity) respectively.19
Three groups were drawn up: 1) preterm newborns in kangaroo care (PT –
KAN); 2) preterm newborns not in kangaroo care (PT – NKAN); and 3) term newborns
(T). In the PT – KAN group, electromyographic activity was measured before being in
kangaroo care (0h). Immediately after taking the first reading, the children were placed
for the first time in the Kangaroo Position. The Kangaroo Position adopted was that
recommended by the Kangaroo Unit, in which the newborn is positioned against the
adult’s chest, face down, wrapped in a strip of flexible cloth. Subsequent readings were
taken after 48h of the Kangaroo Position and, finally, at term-equivalent age (40 ± 1
weeks). In the PT – NKAN group the measurements were made at 0h and 48h. In the T
group electromyographic activity was measured only once, at a chronological age of
24h. The newborns were kept in the kangaroo position for 8-12 hours per day, until the
evaluation after 48h.
During data collection, the researchers asked the Kangaroo Unit not to give the
newborns physiotherapy. The newborns did not, therefore, undergo any kind of early
motor stimulation during data collection, except for oral stimulation by speech
therapists, when necessary.
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Treatment of Data and Statistical analysis
For analysis of muscle activity the signal was transformed into the Root Mean
Square (RMS) and normalized.20,21
For normalization, 100% corresponding to the peak
electromyographic signal was taken as a reference. The signal was captured for 30s,
with a window of 10s before the next measurement.
Comparison of the means of the groups was carried out after establishing the
normality of the distribution (Kolmogorov-Smirnov Test) and the homogeneity of
variance (Levene Test), by analysis of variance for repeated measurements, followed by
multiple comparisons (Holm-Sidak’s post hoc test) to test for the differences between
the two groups. The alpha error for rejection of the null hypothesis was 0.05.
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RESULTS
The clinical and biological characteristics of the newborns in each group can be
seen in Table 1.
Table 1: Clinical and Biological Characteristics of Newborns.
PT-KAN
(n= 25)
PT-NKAN
(n=13)
T
(n=26)
Variables relating to newborn
Gestational age, weeks 31.06 (2.24) 31.21 (1.68) 39.27 (0.92)
Birthweight, grams 1314 (391.66) 1433.08 (349.72) 3191.36 (476.06)
Apgar score after 5’, Md (min-
max)
9 (7-10)
9 (7-9)
9 (8-10)
Corrected age on first
measurement (0h), weeks
34.86 (1.66)
33.93 (1.17)
39.84 (0.85)
For continuous variables the mean (SD) are given; for ordinal variables (Apgar) the median (min-max).
Comparison of the RMS between measurements (Table 2) shows them to be
different to a statistically significant extent: (F(5,108)= 56.69; p<0.001). The post hoc
multiple comparisons (Holm-Sidak Method) showed that in the PT-KAN the RMS was
greater at 48h (p=0.004) and at an age equivalent to term (p=0.004) compared with the
measurement at 0h, although there is no statistically significant difference between the
measurements at 48h and at age equivalent to term. In the PT-NKAN group no
significant difference was found between 0h and 48h.
The RMS in the PT-KAN group at age equivalent to term was greater than in T
(p=0.004).
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Table 2: Electromyographic activity (RMS normalized) of the left brachial biceps
muscle in preterm newborns in kangaroo care or not and in term newborns.
Intervals between
measurements
Groups
PT-KAN
(��± DP)
PT-NKAN
(��± DP)
T
(��± DP)
0h
31.85±6.93
37.59±4.42
-
48h
49.30±4.91
38.17±3.10
-
IET/IAT
48.03±5.56
-
27.12±5.70
RMS: Root Mean Square. PT-KAN: group of preterm newborns in kangaroo care. PT-NKAN: group of preterm
newborns not in kangaroo care. T: group of term newborns. IET: age equivalent to term (for PT-KAN group).
IAT: age on term (for T group). *Analysis of variance for repeated measurements: F(5,108)= 56.69; p<0.001.
Multiple comparisons (Holm-Sidak Test): in the PT-KAN group: 0h x 48h (p=0.004), 0h x IET (p=0.004).
Between PT-KAM and T groups: IET x IAT (p=0.004).
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DISCUSSION
The results of this study showed an increase in electromyographic activity of the
brachial biceps muscle in preterm newborns placed for 48h in kangaroo care, which did
not occur in the control group. These data suggest that the kangaroo position changes
myoelectrical activity in these children, at least in the case of the flexor muscle
evaluated here.
A similar result was observed in a previous study.17
Preterm newborns placed for
24h in kangaroo care saw an increase in the myoelectrical activity of flexor muscles and
this increase persisted even after 24h out of this position.
Later, Diniz et al16
observed a growing increase in electromyographic activity in
the brachial biceps muscle during 96h in kangaroo care. As in our study, these authors
observed this effect 48h after being placed in kangaroo care. However, it is important to
note the presence of a control group in our study which gives added weight to our
results. Also in accordance with the findings of Diniz et al16
, the effect on
electromyographic activity remained constant until an age equivalent to term.
It is worth noting that the electromyographic activity in the PT-KAM group, at an
age equivalent to term, was significantly greater than that in term children. This finding
may be associated with the fact that preterm children received extra-uterine stimuli up
to age equivalent to term, especially those provided by the kangaroo position. However,
the term children to not have the opportunity to receive such stimuli.
The effect of the kangaroo position on inducing a more flexed posture in preterm
neonates is already known,22,23
and this also suggest a specific effect of the kangaroo
position on flexor muscles.
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Recently Schneider et al24
using Transcranial Magnetic Stimulation, showed that
preterm newborns undergoing the kangaroo method had better connectivity and
synaptic efficacy of the motor routes in the brain in adolescence. Another study25
provides electroencephalic evidence to the effect that the kangaroo interventions makes
the brain mature faster in health preterm children. These findings are relevant, since
changes in the myoelectrical parameter in response to the kangaroo position found in
our study may be associated with faster maturation of the brain and better performance
of cerebral motor activity. The mechanism behind this central motor activation on the
peripheral myoelectrical response is still a matter of debate, but it corroborates the
conclusion that the kangaroo position has an effect on muscle response.
Delays in neuropsychomotor development are frequent in preterm newborns
owing to insufficient organization of their nervous systems.8,24
However, a recent meta-
analysis26
concluded that early intervention programs for premature babies have a
positive influence on motor development and there is evidence that tactile, synesthesic
and vestibular stimuli may influence the motor abilities of newborns.27,28
We suggest, then, that early initiation of the kangaroo position may, like other
early intervention programs, have a positive influence on the motor development of the
child. This hypothesis may be sustained by the characteristics of the kangaroo position,
which provide different stimuli for the newborn. However, given that, in the kangaroo
position, the preterm newborn remains in skin-to-skin contact with the adult chest, with
its limbs flexed, in a vertical position1 receiving various environmental inputs, the
sensory, postural and vestibular stimuli furnished when in this position16
may cause a
considerable increase in motor activity.
This evidence suggests that the kangaroo position has a positive influence on
motor activity in newborns that is physiologically represented by an alteration in
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myoelectrical parameters as observed here. Moreover, myoelectrical alterations in a
flexor muscle is a relevant physiological response, since the kangaroo position involves
maintaining a flexed posture.
One limitation of the present study is the absence of a group of preterm newborns
not in kangaroo care followed up to age equivalent to term, as this would shed light on
whether the increase in electromyographic activity in the preterm children at age
equivalent to term is only related to the growth and development of the child and not the
influence of the kangaroo position. However, the reduced myoelectrical response in
group T suggests that it is the kangaroo position and not the growth of the child per se
that is responsible for the changes in electromyographic activity observed here. Apart
from the this limitation, the sample size lower than the estimate is a factor that may
diminish the reliability of our findings. However with a sample power of 90%, the large
differences found between the means and the statistically significant figures may
support our inference.
In conclusion, the results of this study provide evidence that the kangaroo
position in the short term causes an increase in myoelectrical activity in preterm
newborns that persists until an age equivalent to term. In addition, it may be that the fact
that electromyographic activity in premature children at age equivalent to term is greater
than that of term newborns is related to the different stimuli (tactile, synesthetic and
vestibular) that they receive. It is thus suggested that this intervention induces changes
in the flexor function of the muscle (flexor tonus), thereby making it possible to
influence the motor development of the newborn. The age to which (in the long term)
these effects persist and whether they are positive effects need to be examined in further
studies.
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It is important to point out the innovative nature of this study, since there is a
lack of studies specifically evaluating electromyographic activity in children in
kangaroo care. It is suggested that further research be carried out to investigate the
electromyographic effect of the kangaroo position on other muscles involved in the
postural system, in both term and preterm newborns.
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Acknowledgements: We wish to thank the babies, parents and, especially, thank the
nursing technicians of the Kangaroo Unit at the Instituto de Medicina Integral Prof.
Fernando Figueira (IMIP), Recife – Brazil.
Contributors: RMM – Preparation of the study project, data collection and supervision
thereof, statistical analysis, research articles in the database, preparation of the article;
and approved the final manuscript as submitted; JECF – Guidance for the preparation of
the study project, supervision of data collection, statistical analysis, research articles in
the database; guidance and preparation of the article; and approved the final manuscript
as submitted; KTD – Preparation of the study project, data collection and supervision
thereof, data processing, statistical analysis, research articles in the database,
preparation of the article; and approved the final manuscript as submitted; GMSL –
Preparation of the study project, data collection and supervision thereof; and approved
the final manuscript as submitted; DAV: Preparation of the study project, supervision of
data collection, data processing; and approved the final manuscript as submitted;
Funding Source: Fundação de Amparo à Ciência e Tecnologia do Estado de
Pernambuco – FACEPE (APQ – 0552–4.08/100).
Financial Disclosure: Miranda RM was supported by post graduate scholarship from
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Diniz KT
was supported by post graduate scholarship from Fundação de Amparo à Ciência e
Tecnologia do Estado de Pernambuco (FACEPE).
Conflict of Interest: the authors declare that they have no competing interests.
Ethics approval: IMIP’s Ethics Committee for Research involving Human Beings (Nº
1,902)
Data sharing statement: no additional data available.
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REFERENCES
1. Nyqvist KH , Anderson GC, Bergman N, et al. Towards universal Kangaroo Mother
Care: recommendations and report from the First European conference and Seventh
International Workshop on Kangaroo Mother Care. Acta Paediatr 2010;99:820-6.
2. Mori R, Khanna R, Pledge D, et al. Meta-analysis of physiological effects of skin-to-
skin contact for newborns and mothers. Pediatr Int 2010;52:161-70.
3. Almeida CM, Almeida AFN, Forti EMP. Effects of kangaroo mother care on the vital
signs of low-weight preterm newborns. Rev bras fisioter 2007;11:1-5.
4. Cong X, Cusson RM, Hussain N, et al. Kangaroo care and behavioral and physiologic
pain responses in very-low-birth-weight twins: a case study. Pain Manag
Nurs 2012;13:127-38.
5. Begum EA, Bonno M, Ohtani N, et al. Cerebral oxygenation responses
during kangaroo care in low birth weight infants. BMC Pediatr 2008;51:1-9.
6. Ferber SG, Makhoul IR. The Effect of Skin-to-Skin Contact (Kangaroo Care) Shortly
After Birth on the Neurobehavioral Responses of the Term Newborn: A Randomized,
Controlled Trial. Pediatrics 2004;113:858-65.
7. Lamy Filho F, Silva AA, Lamy ZC, et al. Evaluation of the neonatal outcomes of
the kangaroo mother method in Brazil. J Pediatr (Rio J) 2008; 84:428-35.
8. Ludington-Hoe SM, Johnson MW, Morgan K, et al. Neurophysiologic assessment of
neonatal sleep organization: preliminary results of a randomized, controlled trial of skin
contact with preterm infants. Pediatrics 2006; 117:e909-23.
9. Saeidi R, Asnaashari Z, Amirnejad M, et al. Use of "kangaroo care" to alleviate the
intensity of vaccination pain in newborns. Iran J Pediatr 2011;21:99-102.
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10. Nimbalkar SM, Chaudhary NS, Gadhavi KV, et al. Kangaroo Mother Care in
reducing pain in preterm neonates on heel prick. Indian J Pediatr 2013;80:6-10.
11. Moore ER, Anderson GC, Bergman N, et al. Early skin-to-skin contact for mothers
and their healthy newborn infants. Cochrane Database Syst Rev 2013;(6): CD003519.
12. Mahmood I, Jamal M, Khan N. Effect of mother-infant early skin-to-skin contact on
breastfeeding status: a randomized controlled trial. J Coll Physicians Surg Pak 2011;
21:601-5.
13. Nagai S, Yonemoto N, Rabesandratana N, et al. Long-term effects of earlier
initiated continuous Kangaroo Mother Care (KMC) for low-birth-weight (LBW) infants
in Madagascar. Acta Paediatr 2011;100:e241-7.
14. Conde-Agudelo A, Belizán JM, Diaz-Rossello J. Kangaroo mother care to reduce
morbidity and mortality in low birthweight infants. Cochrane Database Syst
Rev 2013;(6):CD002771.
15. Lawn JE, Mwansa-Kambafwile J, Horta BL, et al. Kangaroo mother care to prevent
neonatal deaths due to preterm birth complications. Int J Epidemiol 2010;39:i144–54.
16. Diniz KT, Cabral-Filho JE, Miranda RM, et al. Effect of the kangaroo position on
the electromyographic activity of preterm children: a follow-up study. BMC Pediatr
2013; 13:79.
17. Barradas J: Kangaroo position effect on the flexor muscle tone of newborn preterm.
Fernando Figueira: Dissertation. Post Graduate Department the Institute of Integrated
Medicine Prof; 2010.
18. Hermens HJ, Freriks B, Disselhorst-Klug C, et al. Development of
recommendations for SEMG sensors and sensor placement procedures. J Electromyogr
Kinesiol 2000;10:361-74.
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19. Als H, Tronick E, Lester BM, et al. The Braselton neonatal behavioral assessment
scale (BNBAS). J Abnorm Child Psychol 1977;5:215-29.
20. Bolgla LA, Uhl TL. Reliability of electromyographic normalization methods for
evaluating the hip musculature. J Electromyogr Kinesiol 2007;17:102–111.
21. Lehman GJ, McGill SM. The importance of normalization in the interpretation of
surface electromyography: a proof of principle. J Manipulative Physiol Ther 1999;
22:444–46.
22. Barradas J, Fosceca A, Guimarães CLN, et al. Relationship between positioningof
premature infants in kangaroo mother care and early neuromotor development. J Pediatr
(Rio J) 2006;82:475–80.
23. Ferber SG, Makhoul IR. The effect of skin-to-skin contact (kangaroo care) shortly
after birth on the neurobehavioral responses of the term newborn: a randomized.
Controlled Trial. Pediatrics 2004;113:858–65.
24. Schneider C, Charpak N, Ruiz-Peláez JG, et al. Cerebral motor function in very
premature-at-birth adolescents: a brain stimulation exploration of kangaroo mother care
effects. Acta Paediatr 2012;101:1045-53.
25. Kaffashi F, Scher MS, Ludington-Hoe SM, et al. An analysis of
the kangaroo care intervention using neonatal EEG complexity: a preliminary study.
Clin Neurophysiol 2013;124:238-46.
26. Spittle A, Orton J, Anderson P, et al. Early developmental intervention programmes
post-hospital discharge to prevent motor and cognitive impairments in preterm infants.
Cochrane Database Syst Rev 2013;(6):CD005495.
27. Field TM, Schanberg SM, Scafidi F, et al. Tactile/kinesthetic stimulation effects on
preterm neonates. Pediatrics 1986; 77:654–58.
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28. Symington AJ, Pinelli J. Developmental care for promoting development and
preventing morbidity in preterm infants. Cochrane Database Syst Rev 2013;(6):CD
001814.
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Electromyographic activity of preterm newborns in kangaroo position: a cohort study
Journal: BMJ Open
Manuscript ID: bmjopen-2014-005560.R1
Article Type: Research
Date Submitted by the Author: 14-Jul-2014
Complete List of Authors: Miranda, Rafael; Instituto de Medicina Integral Prof. Fernando Fiqueira, Pós-graduação Cabral Filho, José; Instituto de Medicina Integral Prof. Fernando Fiqueira, Pós-graduação Diniz, Kaísa; Instituto de Medicina Integral Prof. Fernando Fiqueira, Pós-graduação Lima, Geisy Maria; Instituto de Medicina Integral Prof. Fernando Fiqueira, Unidade Canguru Vasconcelos, Danilo; Instituto de Medicina Integral Prof. Fernando Fiqueira, Pós-graduação
<b>Primary Subject Heading</b>:
Paediatrics
Secondary Subject Heading: Public health
Keywords: PAEDIATRICS, Developmental neurology & neurodisability < PAEDIATRICS, Community child health < PAEDIATRICS
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1
Electromyographic activity of preterm newborns in kangaroo position: a cohort
study
Rafael Moura Miranda1; José Eulálio Cabral Filho
2; Kaísa Trovão Diniz
3; Geisy Maria
Souza Lima4; Danilo de Almeida Vasconcelos
5.
Affiliations: 1,2,3,5
Post Graduate Program of Instituto de Medicina Integral Prof.
Fernando Figueira (IMIP) – Recife – Brasil. 4Instituto de Medicina Integral Prof.
Fernando Figueira (IMIP) – Recife – Brasil.
Address correspondence to: Rafael Moura Miranda. Rua: Paula Batista, 270, Edifício
Morada Paula Batista, apto 203. Recife-PE/ Brasil; CEP: 51030-080.
Key-words: Kangaroo-Mother Care Method, Muscle Tonus, Electromyography, Child
Development, Motor Activity.
Word count: 3628
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ABSTRACT
Aim: to compare the electromyographic activity of preterm newborns placed in
kangaroo position with the same activity of newborns not placed in this position.
Methods: A cohort study was carried out at the Instituto de Medicina Integral Prof.
Fernando Figueira (IMIP), Recife, Brazil. Surface electromyography (EMGs) was used
to investigate muscle activity in the brachial biceps at rest. Three groups were designed:
1) preterm newborns in kangaroo position (PT – KAN), its electromyographic activity
being recorded at 0h (immediately before starting this position), and then at 48h from
beginning the position (but newborns being kept in the kangaroo position for 8-12 hours
per day) and at term equivalent age (40 ± 1 weeks); 2) preterm newborns not in
kangaroo position (PT – NKAN), the measurements being made at 0h and 48h; and 3)
term newborns (T), in which measurements were made at 24h of chronological age.
Statistical comparisons were made by analysis of variance for repeated measurements
followed by the multiple comparisons tests (Holm-Sidak’s).
Results: The RMS values showed significant differences among the groups (F(5,108)=
56.69; p<0.001). The multiple comparisons showed that, RMS was greater at 48h
compared to 0h in the preterm group in kangaroo position, but not in the group not
submitted to kangaroo position. The RMS in the term equivalent aged group in
kangaroo position was also greater when compared to the term group.
Conclusions: The kangaroo position increases electromyographic activity in the
brachial biceps of preterm newborns and those who have reached the age equivalent to
term. One limitation of the present study is the absence of a group of preterm newborns
not in kangaroo position followed up to age equivalent to term.
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Strengths and limitations of this study
▪ The results of the study add new information about the effects of Kangaroo-Mother
Care for the preterm.
▪ The early initiation of the kangaroo position may, like other early intervention
programs, have a positive influence on the motor responses of the neonate, thereby
making it possible to influence the motor development of the preterm newborn.
It is important to point out the innovative nature of this study, since there is a lack of
studies specifically evaluating electromyographic activity in newborn in kangaroo
position.
▪ The sample size lower than the estimate in one of the Groups (PT-NKAN) is a factor
that may diminish the reliability of our findings. However the sample power of 90%, the
large differences found between the means and the statistically significant figures may
support our inference.
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INTRODUCTION
The Kangaroo Method (KM) is an intervention that aims to improve the health
of preterm low-weight newborns.1 There is evidence that the method provides various
benefits. These include an increase in body temperature,2,3
stabilization of cardio-
respiratory frequency,3,4
improved oxygenation of the brain,5
improved behavior (crying
and sleep),6-8
a reduction in pain4,9,10
and greater adherence to and duration of
breastfeeding.11-13
The method is also associated with a reduction in morbidity and
mortality,14,15
infections14
and the duration of hospitalization.15
The main feature of the method is the kangaroo position, whereby the newborn
remains in a vertical position supported on its stomach with limbs flexed, dressed in
light clothes, maintaining skin-to-skin contact with the adult’s thorax1. This position
allows the neonates to receive sensory, vestibular and postural stimuli and its effect on
motor responses in the newborns has thus aroused some interest among investigators.16
Recently, some studies16,17
have shown an increase in electromyographic activity in
preterm newborns after different periods of time in kangaroo position (up to 96h) and
that this increase persists until an age equivalent to term. These results were pioneering,
although no study has yet been conducted in which these responses are compared with
those of preterm newborns not in kangaroo position and those of term newborns. The
aim of this study was thus to compare electromyographic activity in preterm newborns
in kangaroo position and newborns not placed in this position.
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METHODS
Participants
A cohort study was carried out, between July 2012 and January 2013, at the
Instituto de Medicina Integral Prof. Fernando Figueira (IMIP), in Recife, Brazil, with 64
hospitalized newborns, from which 38 preterm in the Kangaroo Unit sector and 26 term
in the Nursery sector of the IMIP hospital.
The IMIP’s Kangaroo Unit covers a surface-area of 600 m2
and has a ward with
22 beds for clinically stable preterm newborns (with a respiratory frequency of between
30–60 inspirations per minute, a heart rate of between 120–160 beats per minute,
peripheric oxygen saturation of over 89%, absence of signs of respiratory distress,
absence of cyanosis or pallor and pain.) The newborns had to tolerate food, to breathe
without the use of an apparatus and to weigh more than 1,250 grams.
The Kangaroo Unit provides medical and nursing services and also speech
therapy and physiotherapy. In this unit, the newborns, when referred by the medical
services, are evaluated and undergo an early stimulation program.
Newborns were included in the preterm groups if they had a gestational age of
27 to 34 weeks and a corrected age until 35 weeks at the time of the first
electromyographic examination, and had not previously been in kangaroo position.
Neonates were included in the group of term if they had a gestational age of 38-41
weeks. Neonates were included only when their Brazelton state during
electromyographic recording was 4 or 5 (inactive alert or alert with activity).
The exclusion factors for all the newborns were: Apgar lower than 7 in the 5th
minute, a history of grade III or IV intracranial hemorrhage (diagnosed by way of
transfontanelar ultra-sound and included in medical records), convulsions, congenital
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infections (cytomegalovirus, rubella, toxoplasmosis, syphilis and vertically transmitted
HIV), malformations of the Central Nervous System (hydrocephaly and genetic
syndromes), infections of the central nervous system (meningitis or encephalitis),
congenital cardiopathy, traumas during delivery (injuries to the brachial plexus,
dislocation of the hip and pelvis fractures) and gastro-esophageal reflux disorder.
All these inclusion and exclusion factors were evaluated using data collected
from the medical records of patients evaluated by neonatologists at the Neonatal
Intensive Care Unit, the Kangaroo Unit sector and the Nursery sector.
A non-probabilistic convenient sample of newborns was selected, the size of the
sample being based on a previous study 17
that found variance of 2.6 in
electromyographic activity and estimated the minimum difference between means to be
2 µV. With an alpha error of 0.05 and power of 90%, 21 individuals were calculated for
each group.
The project for this study was submitted to the IMIP’s Ethics Committee for
Research involving Human Beings and was approved (protocol no. 1902). The parents
or guardians who agreed to participate signed terms of free informed consent.
Collection procedure
The electromyographic signal was obtained using a Miotool 400 ®
electromyograph (Miotec Equipamentos Biomédicos – Brazil). A system of channels
and self-adhesive 4.2 mm diameter Ag/AgCl electrodes (Meditrace 100®
) was used to
connect the equipment to the body of the newborn under examination. The
electromyograph was connected to a laptop with Myographic 2.0 software (Miotec
Equipamentos Biomédicos - Brazil) to process the myoelectrical records. The sampling
frequency was 2000 Hz and the electromyograms were amplified 2000 times.
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The electromyographic signal was captured using two surface electrodes placed
on the central portion of the left brachial bíceps muscle, between the motor point and
the myotendinous junction, parallel to the muscle fibers, as recommended by the
SENIAM (Surface Electromyography for the Non-Invasive Assessment of Muscles)
project.18
The electrodes were adjusted to ensure the distance between them did not
exceed 20 mm and the reference electrode was always placed on the lateral malleolus
contralateral to the muscle under evaluation.
When the measurements were made, the newborn was placed on a small wedge-
shaped cushion at angle of 30° relative to the horizontal plane. Electromyographic
activity was captured with the newborn in Brazelton state 4 or 5 (inactive alert or alert
with activity) respectively.19
Three groups were designed: Group 1 (n=25): preterm newborns in kangaroo
position (PT – KAN); 2) Group 2 (n=13): preterm newborns not in kangaroo position
(PT – NKAN); and 3) Group 3 (n=16): term newborns (T).
In the PT – KAN group, electromyographic activity was first recorded before
neonate being in kangaroo position (0h). Immediately after taking this record, the
neonates were placed for the first time in the kangaroo position. The kangaroo position
adopted was that recommended by the Kangaroo Unit, in which the newborn is
positioned against the adult’s chest, face down, wrapped in a strip of flexible cloth.
Subsequent recordings were taken immediately after 48h of the kangaroo position and,
finally, at term-equivalent age (40 ± 1 weeks). The newborns were kept in the kangaroo
position for 8-12 hours per day, until the evaluation after 48h.
In the PT – NKAN group the measurements were made at 0h and 48h. In the T
group electromyographic activity was measured only once, at a chronological age until
24h.
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During data collection, the researchers asked the Kangaroo Unit not to give the
newborns physiotherapy. The newborns did not, therefore, undergo any kind of early
motor stimulation during data collection, except for oral stimulation by speech
therapists, when necessary.
Treatment of Data and Statistical analysis
For analysis of muscle activity the signal was transformed into the Root Mean
Square (RMS) and normalized.20,21
For normalization, 100% corresponding to the
maximum peak electromyographic signal was taken as a reference. A period of 10s of
the total electromyographic reading (30s) was used.
Comparison of the means of the groups was carried out after verifying the
normality of the distribution (Kolmogorov-Smirnov Test) and the homogeneity of
variance (Levene Test), by analysis of variance for repeated measurements, followed by
multiple comparisons (Holm-Sidak’s post hoc test) to test for the differences between
each two groups. The alpha error for rejection of the null hypothesis was 0.05.
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RESULTS
The clinical and biological characteristics of the newborns in each group can be
seen in Table 1.
Table 1: Clinical and Biological Characteristics of Newborns.
PT-KAN
(n= 25)
PT-NKAN
(n=13)
T
(n=26)
Variables relating to newborn
Gestational age, weeks 31.06 (2.24) 31.21 (1.68) 39.27 (0.92)
Birthweight, grams 1314 (391.66) 1433.08 (349.72) 3191.36 (476.06)
Apgar score after 5’, Md (min-
max)
9 (7-10)
9 (7-9)
9 (8-10)
Corrected age on first
measurement (0h), weeks
34.86 (1.66)
33.93 (1.17)
39.84 (0.85)
For continuous variables the mean (SD) are given; for ordinal variables (Apgar) the median (min-max).
Variances analyses comparison of the RMS among measurements (Table 2)
demonstrated a significant difference (F(5,108)= 56.69; p<0.001). The post hoc multiple
comparisons (Holm-Sidak Method) showed that in the PT-KAN Group the RMS was
greater at 48h (p=0.004) and at age equivalent to term (p=0.004) compared with the
measurement at 0h, but there is no statistically significant difference between the
measurements at 48h and at age equivalent to term. In the PT-NKAN group no
significant difference was found between 0h and 48h.
The RMS in the PT-KAN group at age equivalent to term was greater than in the
T Group (p=0.004).
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Table 2: Electromyographic activity (RMS normalized) of the left brachial biceps
muscle in preterm newborns in kangaroo position or not and in term newborns.
Intervals between
measurements
Groups
PT-KAN
(��± DP)
PT-NKAN
(��± DP)
T
(��± DP)
0h
31.85±6.93
37.59±4.42
-
48h
49.30±4.91
38.17±3.10
-
TEA and TA
48.03±5.56
-
27.12±5.70
RMS: Root Mean Square. PT-KAN: group of preterm newborns in kangaroo care. PT-NKAN: group of preterm
newborns not in kangaroo position. T: group of term newborns. TEA: term equivalent age (for PT-KAN group).
TA: term age (for T group). *Analysis of variance for repeated measurements: F(5,108)= 56.69; p<0.001. Multiple
comparisons (Holm-Sidak Test): in the PT-KAN group: 0h x 48h (p=0.004), 0h x TEA (p=0.004). Between PT-
KAN and T groups: TEA x TA (p=0.004).
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DISCUSSION
The results of this study showed an increase in electromyographic activity of the
brachial biceps muscle in preterm newborns maintained in a kangaroo care environment
for 48h even when placed on kangaroo position during only to 8 – 12h by day, which
did not occur in the control group. These data suggest that the kangaroo position
changes myoelectrical activity in these newborn, at least in the case of the flexor muscle
evaluated here.
A similar result was observed in a previous study.17
Preterm newborns placed for
24h in kangaroo position saw an increase in the myoelectrical activity of flexor muscles
and this increase persisted even after 24h out of this position.
Later, Diniz et al16
observed a growing increase in electromyographic activity in
the brachial biceps muscle during 96h in kangaroo position. As in our study, these
authors observed this effect 48h after being placed in kangaroo position. However, it is
important to note the presence of a control group in our study which gives added weight
to our results. Also in accordance with the findings of Diniz et al16
, the effect on
electromyographic activity remained constant until an age equivalent to term.
It is worth noting that the electromyographic activity in the PT-KAN group, at an
age equivalent to term, was significantly greater than that in term newborns, although a
similarity between them was expected. This increased electromyographic activity might
be associated with the fact that preterm newborns received extra-uterine stimuli up to
age equivalent to term, especially those provided by the kangaroo position. However,
the term newborns to not have the opportunity to receive such stimuli.
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The effect of the kangaroo position on inducing a more flexed posture in preterm
neonates is already known,22,23
and this also suggest a specific effect of the kangaroo
position on flexor muscles.
Recently Schneider et al24
using transcranial magnetic stimulation, showed that
preterm newborns undergoing the kangaroo method had better connectivity and
synaptic efficacy of the motor routes in the brain in adolescence. Another study25
provides electroencephalic evidence to the effect that the kangaroo interventions makes
the brain mature faster in health preterm newborns. These findings are relevant, since
changes in the myoelectrical parameter in response to kangaroo position found in our
study may be associated with faster maturation of the brain and better performance of
the cerebral structures controlling motor activity. The mechanism behind this central
motor activation on the peripheral myoelectrical response is still a matter of debate, but
it corroborates the conclusion that the kangaroo position has an effect on muscle
response.
Delays in neuropsychomotor development are frequent in preterm newborns
owing to insufficient organization of their nervous systems.8,24
However, a recent meta-
analysis26
concluded that early intervention programs for premature babies have a
positive influence on motor development and there is evidence that tactile, synesthesic
and vestibular stimuli may influence the motor abilities of newborns.27,28
We suggest, then, that early initiation of the kangaroo position may, like other
early intervention programs, have a positive influence on the motor development of the
preterm newborns. This hypothesis may be sustained by the characteristics of the
kangaroo position, which provide different stimuli for the newborn. However, given
that, in the kangaroo position, the preterm newborn remains in skin-to-skin contact with
the adult chest, with its limbs flexed, in a vertical position1 receiving various
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environmental inputs, the sensory, postural and vestibular stimuli furnished when in this
position16
may cause a considerable increase in motor activity. This evidence suggests
that the kangaroo position has a positive influence on motor activity in newborns that is
physiologically represented by an alteration in myoelectrical parameters as observed
here. Moreover, myoelectrical alterations in a flexor muscle are a relevant physiological
response, since the kangaroo position involves maintaining a flexed posture.
One limitation of the present study is the absence of a group of preterm newborns
not in kangaroo care followed up to age equivalent to term, as this would shed light on
whether the increase in electromyographic activity in the preterm newborns at age
equivalent to term is only related to the growth and development of the neonates and not
the influence of the kangaroo position. However, the reduced myoelectrical response in
group T suggests that it is the kangaroo position and not the growth of the newborns per
se that is responsible for the changes in electromyographic activity observed here. Apart
from this limitation, the sample size was lower than the estimate so it is a factor that
may diminish the reliability of our findings. However with a sample power of 90%, the
large differences found between the means and the statistically significant figures may
support our inferences.
In conclusion, although this is a preliminary study their results provide evidence
that the kangaroo position in the short term induces an increase in myoelectrical activity
in preterm newborns which persists until the age equivalent to term. In addition, it may
be that the fact that electromyographic activity in premature newborn at age equivalent
to term is greater than that of term newborns is related to the different stimuli (tactile,
synesthetic and vestibular) that they receive. It is thus suggested that this intervention
induces changes in the flexor function of the muscle (flexor tonus), thereby making it
possible to influence the motor development of the newborn. The age to which (in the
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long term) these effects persist and whether they are positive effects need to be
examined in further studies.
It is important to point out the innovative nature of this study, although
preliminary, since there is a lack of studies specifically evaluating electromyographic
activity in newborn in kangaroo position. It is suggested that further research be carried
out to investigate the electromyographic effect of the kangaroo position on other
muscles involved in the postural system, in both term and preterm newborns.
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Acknowledgements: We wish to thank the babies, parents and, especially, thank the
nursing technicians of the Kangaroo Unit at the Instituto de Medicina Integral Prof.
Fernando Figueira (IMIP), Recife – Brazil.
Contributors: RMM – Preparation of the study project, data collection and supervision
thereof, statistical analysis, research articles in the database, preparation of the article;
and approved the final manuscript as submitted; JECF – Guidance for the preparation of
the study project, supervision of data collection, statistical analysis, research articles in
the database; guidance and preparation of the article; and approved the final manuscript
as submitted; KTD – Preparation of the study project, data collection and supervision
thereof, data processing, statistical analysis, research articles in the database,
preparation of the article; and approved the final manuscript as submitted; GMSL –
Preparation of the study project, data collection and supervision thereof; and approved
the final manuscript as submitted; DAV: Preparation of the study project, supervision of
data collection, data processing; and approved the final manuscript as submitted;
Funding Source: Fundação de Amparo à Ciência e Tecnologia do Estado de
Pernambuco – FACEPE (APQ – 0552–4.08/100).
Financial Disclosure: Miranda RM was supported by post graduate scholarship from
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Diniz KT
was supported by post graduate scholarship from Fundação de Amparo à Ciência e
Tecnologia do Estado de Pernambuco (FACEPE).
Conflict of Interest: the authors declare that they have no competing interests.
Ethics approval: IMIP’s Ethics Committee for Research involving Human Beings
(protocol no.1902)
Data sharing statement: no additional data available.
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REFERENCES
1. Nyqvist KH , Anderson GC, Bergman N, et al. Towards universal Kangaroo Mother
Care: recommendations and report from the First European conference and Seventh
International Workshop on Kangaroo Mother Care. Acta Paediatr 2010;99:820-6.
2. Mori R, Khanna R, Pledge D, et al. Meta-analysis of physiological effects of skin-to-
skin contact for newborns and mothers. Pediatr Int 2010;52:161-70.
3. Almeida CM, Almeida AFN, Forti EMP. Effects of kangaroo mother care on the vital
signs of low-weight preterm newborns. Rev bras fisioter 2007;11:1-5.
4. Johnston C, Campbell-Yeo M, Fernandes A, et al. Skin-to-skin care for procedural
pain in neonates. Cochrane Database Syst Rev. 2014 (4):CD008435.
5. Begum EA, Bonno M, Ohtani N, et al. Cerebral oxygenation responses
during kangaroo care in low birth weight infants. BMC Pediatr 2008;51:1-9.
6. Ferber SG, Makhoul IR. The Effect of Skin-to-Skin Contact (Kangaroo Care) Shortly
After Birth on the Neurobehavioral Responses of the Term Newborn: A Randomized,
Controlled Trial. Pediatrics 2004;113:858-65.
7. Lamy Filho F, Silva AA, Lamy ZC, et al. Evaluation of the neonatal outcomes of
the kangaroo mother method in Brazil. J Pediatr (Rio J) 2008; 84:428-35.
8. Ludington-Hoe SM, Johnson MW, Morgan K, et al. Neurophysiologic assessment of
neonatal sleep organization: preliminary results of a randomized, controlled trial of skin
contact with preterm infants. Pediatrics 2006; 117:e909-23.
9. Saeidi R, Asnaashari Z, Amirnejad M, et al. Use of "kangaroo care" to alleviate the
intensity of vaccination pain in newborns. Iran J Pediatr 2011;21:99-102.
10. Nimbalkar SM, Chaudhary NS, Gadhavi KV, et al. Kangaroo Mother Care in
reducing pain in preterm neonates on heel prick. Indian J Pediatr 2013;80:6-10.
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11. Moore ER, Anderson GC, Bergman N, et al. Early skin-to-skin contact for mothers
and their healthy newborn infants. Cochrane Database Syst Rev 2013;(6): CD003519.
12. Mahmood I, Jamal M, Khan N. Effect of mother-infant early skin-to-skin contact on
breastfeeding status: a randomized controlled trial. J Coll Physicians Surg Pak 2011;
21:601-5.
13. Nagai S, Yonemoto N, Rabesandratana N, et al. Long-term effects of earlier
initiated continuous Kangaroo Mother Care (KMC) for low-birth-weight (LBW) infants
in Madagascar. Acta Paediatr 2011;100:e241-7.
14. Conde-Agudelo A, Belizán JM, Diaz-Rossello J. Kangaroo mother care to reduce
morbidity and mortality in low birthweight infants. Cochrane Database Syst
Rev 2013;(6):CD002771.
15. Lawn JE, Mwansa-Kambafwile J, Horta BL, et al. Kangaroo mother care to prevent
neonatal deaths due to preterm birth complications. Int J Epidemiol 2010;39:i144–54.
16. Diniz KT, Cabral-Filho JE, Miranda RM, et al. Effect of the kangaroo position on
the electromyographic activity of preterm children: a follow-up study. BMC Pediatr
2013; 13:79.
17. Barradas J: Kangaroo position effect on the flexor muscle tone of newborn preterm.
Fernando Figueira: Dissertation. Post Graduate Department the Institute of Integrated
Medicine Prof; 2010.
18. Hermens HJ, Freriks B, Disselhorst-Klug C, et al. Development of
recommendations for SEMG sensors and sensor placement procedures. J Electromyogr
Kinesiol 2000;10:361-74.
19. Als H, Tronick E, Lester BM, et al. The Braselton neonatal behavioral assessment
scale (BNBAS). J Abnorm Child Psychol 1977;5:215-29.
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20. Bolgla LA, Uhl TL. Reliability of electromyographic normalization methods for
evaluating the hip musculature. J Electromyogr Kinesiol 2007;17:102–111.
21. Lehman GJ, McGill SM. The importance of normalization in the interpretation of
surface electromyography: a proof of principle. J Manipulative Physiol Ther 1999;
22:444–46.
22. Barradas J, Fosceca A, Guimarães CLN, et al. Relationship between positioningof
premature infants in kangaroo mother care and early neuromotor development. J Pediatr
(Rio J) 2006;82:475–80.
23. Ferber SG, Makhoul IR. The effect of skin-to-skin contact (kangaroo care) shortly
after birth on the neurobehavioral responses of the term newborn: a randomized.
Controlled Trial. Pediatrics 2004;113:858–65.
24. Schneider C, Charpak N, Ruiz-Peláez JG, et al. Cerebral motor function in very
premature-at-birth adolescents: a brain stimulation exploration of kangaroo mother care
effects. Acta Paediatr 2012;101:1045-53.
25. Kaffashi F, Scher MS, Ludington-Hoe SM, et al. An analysis of
the kangaroo care intervention using neonatal EEG complexity: a preliminary study.
Clin Neurophysiol 2013;124:238-46.
26. Spittle A, Orton J, Anderson P, et al. Early developmental intervention programmes
post-hospital discharge to prevent motor and cognitive impairments in preterm infants.
Cochrane Database Syst Rev 2013;(6):CD005495.
27. Field TM, Schanberg SM, Scafidi F, et al. Tactile/kinesthetic stimulation effects on
preterm neonates. Pediatrics 1986; 77:654–58.
28. Symington AJ, Pinelli J. Developmental care for promoting development and
preventing morbidity in preterm infants. Cochrane Database Syst Rev 2013;(6):CD
001814.
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Electromyographic activity of preterm newborns in kangaroo position: a cohort
study
Rafael Moura Miranda1; José Eulálio Cabral Filho
2; Kaísa Trovão Diniz
3; Geisy Maria
Souza Lima4; Danilo de Almeida Vasconcelos
5.
Affiliations: 1,2,3,5
Post Graduate Program of Instituto de Medicina Integral Prof.
Fernando Figueira (IMIP) – Recife – Brasil. 4Instituto de Medicina Integral Prof.
Fernando Figueira (IMIP) – Recife – Brasil.
Address correspondence to: Rafael Moura Miranda. Rua: Paula Batista, 270, Edifício
Morada Paula Batista, apto 203. Recife-PE/ Brasil; CEP: 51030-080.
Key-words: Kangaroo-Mother Care Method, Muscle Tonus, Electromyography, Child
Development, Motor Activity.
Word count: 3628
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ABSTRACT
Aim: to compare the electromyographic activity of preterm newborns placed in
kangaroo position with the same activity of newborns not placed in this position.
Methods: A cohort study was carried out at the Instituto de Medicina Integral Prof.
Fernando Figueira (IMIP), Recife, Brazil. Surface electromyography (EMGs) was used
to investigate muscle activity in the brachial biceps at rest. Three groups were designed:
1) preterm newborns in kangaroo position (PT – KAN), its electromyographic activity
being recorded at 0h (immediately before starting this position), and then at 48h from
beginning the position (but newborns being kept in the kangaroo position for 8-12 hours
per day) and at term equivalent age (40 ± 1 weeks); 2) preterm newborns not in
kangaroo position (PT – NKAN), the measurements being made at 0h and 48h; and 3)
term newborns (T), in which measurements were made at 24h of chronological age.
Statistical comparisons were made by analysis of variance for repeated measurements
followed by the multiple comparisons tests (Holm-Sidak’s).
Results: The RMS values showed significant differences among the groups (F(5,108)=
56.69; p<0.001). The multiple comparisons showed that, RMS was greater at 48h
compared to 0h in the preterm group in kangaroo position, but not in the group not
submitted to kangaroo position. The RMS in the term equivalent aged group in
kangaroo position was also greater when compared to the term group.
Conclusions: The kangaroo position increases electromyographic activity in the
brachial biceps of preterm newborns and those who have reached the age equivalent to
term. One limitation of the present study is the absence of a group of preterm newborns
not in kangaroo position followed up to age equivalent to term.
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Strengths and limitations of this study
▪ The results of the study add new information about the effects of Kangaroo-Mother
Care for the preterm.
▪ The early initiation of the kangaroo position may, like other early intervention
programs, have a positive influence on the motor responses of the neonate, thereby
making it possible to influence the motor development of the preterm newborn.
It is important to point out the innovative nature of this study, since there is a lack of
studies specifically evaluating electromyographic activity in newborn in kangaroo
position.
▪ The sample size lower than the estimate in one of the Groups (PT-NKAN) is a factor
that may diminish the reliability of our findings. However the sample power of 90%, the
large differences found between the means and the statistically significant figures may
support our inference.
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INTRODUCTION
The Kangaroo Method (KM) is an intervention that aims to improve the health
of preterm low-weight newborns.1 There is evidence that the method provides various
benefits. These include an increase in body temperature,2,3
stabilization of cardio-
respiratory frequency,3,4
improved oxygenation of the brain,5
improved behavior (crying
and sleep),6-8
a reduction in pain4,9,10
and greater adherence to and duration of
breastfeeding.11-13
The method is also associated with a reduction in morbidity and
mortality,14,15
infections14
and the duration of hospitalization.15
The main feature of the method is the kangaroo position, whereby the newborn
remains in a vertical position supported on its stomach with limbs flexed, dressed in
light clothes, maintaining skin-to-skin contact with the adult’s thorax1. This position
allows the neonates to receive sensory, vestibular and postural stimuli and its effect on
motor responses in the newborns has thus aroused some interest among investigators.16
Recently, some studies16,17
have shown an increase in electromyographic activity in
preterm newborns after different periods of time in kangaroo position (up to 96h) and
that this increase persists until an age equivalent to term. These results were pioneering,
although no study has yet been conducted in which these responses are compared with
those of preterm newborns not in kangaroo position and those of term newborns. The
aim of this study was thus to compare electromyographic activity in preterm newborns
in kangaroo position and newborns not placed in this position.
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METHODS
Participants
A cohort study was carried out, between July 2012 and January 2013, at the
Instituto de Medicina Integral Prof. Fernando Figueira (IMIP), in Recife, Brazil, with 64
hospitalized newborns, from which 38 preterm in the Kangaroo Unit sector and 26 term
in the Nursery sector of the IMIP hospital.
The IMIP’s Kangaroo Unit covers a surface-area of 600 m2
and has a ward with
22 beds for clinically stable preterm newborns (with a respiratory frequency of between
30–60 inspirations per minute, a heart rate of between 120–160 beats per minute,
peripheric oxygen saturation of over 89%, absence of signs of respiratory distress,
absence of cyanosis or pallor and pain.) The newborns had to tolerate food, to breathe
without the use of an apparatus and to weigh more than 1,250 grams.
The Kangaroo Unit provides medical and nursing services and also speech
therapy and physiotherapy. In this unit, the newborns, when referred by the medical
services, are evaluated and undergo an early stimulation program.
Newborns were included in the preterm groups if they had a gestational age of
27 to 34 weeks and a corrected age until 35 weeks at the time of the first
electromyographic examination, and had not previously been in kangaroo position.
Neonates were included in the group of term if they had a gestational age of 38-41
weeks. Neonates were included only when their Brazelton state during
electromyographic recording was 4 or 5 (inactive alert or alert with activity).
The exclusion factors for all the newborns were: Apgar lower than 7 in the 5th
minute, a history of grade III or IV intracranial hemorrhage (diagnosed by way of
transfontanelar ultra-sound and included in medical records), convulsions, congenital
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infections (cytomegalovirus, rubella, toxoplasmosis, syphilis and vertically transmitted
HIV), malformations of the Central Nervous System (hydrocephaly and genetic
syndromes), infections of the central nervous system (meningitis or encephalitis),
congenital cardiopathy, traumas during delivery (injuries to the brachial plexus,
dislocation of the hip and pelvis fractures) and gastro-esophageal reflux disorder.
All these inclusion and exclusion factors were evaluated using data collected
from the medical records of patients evaluated by neonatologists at the Neonatal
Intensive Care Unit, the Kangaroo Unit sector and the Nursery sector.
A non-probabilistic convenient sample of newborns was selected, the size of the
sample being based on a previous study 17
that found variance of 2.6 in
electromyographic activity and estimated the minimum difference between means to be
2 µV. With an alpha error of 0.05 and power of 90%, 21 individuals were calculated for
each group.
The project for this study was submitted to the IMIP’s Ethics Committee for
Research involving Human Beings and was approved (protocol no. 1902). The parents
or guardians who agreed to participate signed terms of free informed consent.
Collection procedure
The electromyographic signal was obtained using a Miotool 400 ®
electromyograph (Miotec Equipamentos Biomédicos – Brazil). A system of channels
and self-adhesive 4.2 mm diameter Ag/AgCl electrodes (Meditrace 100®
) was used to
connect the equipment to the body of the newborn under examination. The
electromyograph was connected to a laptop with Myographic 2.0 software (Miotec
Equipamentos Biomédicos - Brazil) to process the myoelectrical records. The sampling
frequency was 2000 Hz and the electromyograms were amplified 2000 times.
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The electromyographic signal was captured using two surface electrodes placed
on the central portion of the left brachial bíceps muscle, between the motor point and
the myotendinous junction, parallel to the muscle fibers, as recommended by the
SENIAM (Surface Electromyography for the Non-Invasive Assessment of Muscles)
project.18
The electrodes were adjusted to ensure the distance between them did not
exceed 20 mm and the reference electrode was always placed on the lateral malleolus
contralateral to the muscle under evaluation.
When the measurements were made, the newborn was placed on a small wedge-
shaped cushion at angle of 30° relative to the horizontal plane. Electromyographic
activity was captured with the newborn in Brazelton state 4 or 5 (inactive alert or alert
with activity) respectively.19
Three groups were designed: Group 1 (n=25): preterm newborns in kangaroo
position (PT – KAN); 2) Group 2 (n=13): preterm newborns not in kangaroo position
(PT – NKAN); and 3) Group 3 (n=16): term newborns (T).
In the PT – KAN group, electromyographic activity was first recorded before
neonate being in kangaroo position (0h). Immediately after taking this record, the
neonates were placed for the first time in the kangaroo position. The kangaroo position
adopted was that recommended by the Kangaroo Unit, in which the newborn is
positioned against the adult’s chest, face down, wrapped in a strip of flexible cloth.
Subsequent recordings were taken immediately after 48h of the kangaroo position and,
finally, at term-equivalent age (40 ± 1 weeks). The newborns were kept in the kangaroo
position for 8-12 hours per day, until the evaluation after 48h.
In the PT – NKAN group the measurements were made at 0h and 48h. In the T
group electromyographic activity was measured only once, at a chronological age until
24h.
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During data collection, the researchers asked the Kangaroo Unit not to give the
newborns physiotherapy. The newborns did not, therefore, undergo any kind of early
motor stimulation during data collection, except for oral stimulation by speech
therapists, when necessary.
Treatment of Data and Statistical analysis
For analysis of muscle activity the signal was transformed into the Root Mean
Square (RMS) and normalized.20,21
For normalization, 100% corresponding to the
maximum peak electromyographic signal was taken as a reference. A period of 10s of
the total electromyographic reading (30s) was used.
Comparison of the means of the groups was carried out after verifying the
normality of the distribution (Kolmogorov-Smirnov Test) and the homogeneity of
variance (Levene Test), by analysis of variance for repeated measurements, followed by
multiple comparisons (Holm-Sidak’s post hoc test) to test for the differences between
each two groups. The alpha error for rejection of the null hypothesis was 0.05.
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RESULTS
The clinical and biological characteristics of the newborns in each group can be
seen in Table 1.
Table 1: Clinical and Biological Characteristics of Newborns.
PT-KAN
(n= 25)
PT-NKAN
(n=13)
T
(n=26)
Variables relating to newborn
Gestational age, weeks 31.06 (2.24) 31.21 (1.68) 39.27 (0.92)
Birthweight, grams 1314 (391.66) 1433.08 (349.72) 3191.36 (476.06)
Apgar score after 5’, Md (min-
max)
9 (7-10)
9 (7-9)
9 (8-10)
Corrected age on first
measurement (0h), weeks
34.86 (1.66)
33.93 (1.17)
39.84 (0.85)
For continuous variables the mean (SD) are given; for ordinal variables (Apgar) the median (min-max).
Variances analyses comparison of the RMS among measurements (Table 2)
demonstrated a significant difference (F(5,108)= 56.69; p<0.001). The post hoc multiple
comparisons (Holm-Sidak Method) showed that in the PT-KAN Group the RMS was
greater at 48h (p=0.004) and at age equivalent to term (p=0.004) compared with the
measurement at 0h, but there is no statistically significant difference between the
measurements at 48h and at age equivalent to term. In the PT-NKAN group no
significant difference was found between 0h and 48h.
The RMS in the PT-KAN group at age equivalent to term was greater than in the
T Group (p=0.004).
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Table 2: Electromyographic activity (RMS normalized) of the left brachial biceps
muscle in preterm newborns in kangaroo position or not and in term newborns.
Intervals between
measurements
Groups
PT-KAN
(��± DP)
PT-NKAN
(��± DP)
T
(��± DP)
0h
31.85±6.93
37.59±4.42
-
48h
49.30±4.91
38.17±3.10
-
TEA and TA
48.03±5.56
-
27.12±5.70
RMS: Root Mean Square. PT-KAN: group of preterm newborns in kangaroo care. PT-NKAN: group of preterm
newborns not in kangaroo position. T: group of term newborns. TEA: term equivalent age (for PT-KAN group).
TA: term age (for T group). *Analysis of variance for repeated measurements: F(5,108)= 56.69; p<0.001. Multiple
comparisons (Holm-Sidak Test): in the PT-KAN group: 0h x 48h (p=0.004), 0h x TEA (p=0.004). Between PT-
KAN and T groups: TEA x TA (p=0.004).
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DISCUSSION
The results of this study showed an increase in electromyographic activity of the
brachial biceps muscle in preterm newborns maintained in a kangaroo care environment
for 48h even when placed on kangaroo position during only to 8 – 12h by day, which
did not occur in the control group. These data suggest that the kangaroo position
changes myoelectrical activity in these newborn, at least in the case of the flexor muscle
evaluated here.
A similar result was observed in a previous study.17
Preterm newborns placed for
24h in kangaroo position saw an increase in the myoelectrical activity of flexor muscles
and this increase persisted even after 24h out of this position.
Later, Diniz et al16
observed a growing increase in electromyographic activity in
the brachial biceps muscle during 96h in kangaroo position. As in our study, these
authors observed this effect 48h after being placed in kangaroo position. However, it is
important to note the presence of a control group in our study which gives added weight
to our results. Also in accordance with the findings of Diniz et al16
, the effect on
electromyographic activity remained constant until an age equivalent to term.
It is worth noting that the electromyographic activity in the PT-KAN group, at an
age equivalent to term, was significantly greater than that in term newborns, although a
similarity between them was expected. This increased electromyographic activity might
be associated with the fact that preterm newborns received extra-uterine stimuli up to
age equivalent to term, especially those provided by the kangaroo position. However,
the term newborns to not have the opportunity to receive such stimuli.
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The effect of the kangaroo position on inducing a more flexed posture in preterm
neonates is already known,22,23
and this also suggest a specific effect of the kangaroo
position on flexor muscles.
Recently Schneider et al24
using transcranial magnetic stimulation, showed that
preterm newborns undergoing the kangaroo method had better connectivity and
synaptic efficacy of the motor routes in the brain in adolescence. Another study25
provides electroencephalic evidence to the effect that the kangaroo interventions makes
the brain mature faster in health preterm newborns. These findings are relevant, since
changes in the myoelectrical parameter in response to kangaroo position found in our
study may be associated with faster maturation of the brain and better performance of
the cerebral structures controlling motor activity. The mechanism behind this central
motor activation on the peripheral myoelectrical response is still a matter of debate, but
it corroborates the conclusion that the kangaroo position has an effect on muscle
response.
Delays in neuropsychomotor development are frequent in preterm newborns
owing to insufficient organization of their nervous systems.8,24
However, a recent meta-
analysis26
concluded that early intervention programs for premature babies have a
positive influence on motor development and there is evidence that tactile, synesthesic
and vestibular stimuli may influence the motor abilities of newborns.27,28
We suggest, then, that early initiation of the kangaroo position may, like other
early intervention programs, have a positive influence on the motor development of the
preterm newborns. This hypothesis may be sustained by the characteristics of the
kangaroo position, which provide different stimuli for the newborn. However, given
that, in the kangaroo position, the preterm newborn remains in skin-to-skin contact with
the adult chest, with its limbs flexed, in a vertical position1 receiving various
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environmental inputs, the sensory, postural and vestibular stimuli furnished when in this
position16
may cause a considerable increase in motor activity. This evidence suggests
that the kangaroo position has a positive influence on motor activity in newborns that is
physiologically represented by an alteration in myoelectrical parameters as observed
here. Moreover, myoelectrical alterations in a flexor muscle are a relevant physiological
response, since the kangaroo position involves maintaining a flexed posture.
One limitation of the present study is the absence of a group of preterm newborns
not in kangaroo care followed up to age equivalent to term, as this would shed light on
whether the increase in electromyographic activity in the preterm newborns at age
equivalent to term is only related to the growth and development of the neonates and not
the influence of the kangaroo position. However, the reduced myoelectrical response in
group T suggests that it is the kangaroo position and not the growth of the newborns per
se that is responsible for the changes in electromyographic activity observed here. Apart
from this limitation, the sample size was lower than the estimate so it is a factor that
may diminish the reliability of our findings. However with a sample power of 90%, the
large differences found between the means and the statistically significant figures may
support our inferences.
In conclusion, although this is a preliminary study their results provide evidence
that the kangaroo position in the short term induces an increase in myoelectrical activity
in preterm newborns which persists until the age equivalent to term. In addition, it may
be that the fact that electromyographic activity in premature newborn at age equivalent
to term is greater than that of term newborns is related to the different stimuli (tactile,
synesthetic and vestibular) that they receive. It is thus suggested that this intervention
induces changes in the flexor function of the muscle (flexor tonus), thereby making it
possible to influence the motor development of the newborn. The age to which (in the
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long term) these effects persist and whether they are positive effects need to be
examined in further studies.
It is important to point out the innovative nature of this study, although
preliminary, since there is a lack of studies specifically evaluating electromyographic
activity in newborn in kangaroo position. It is suggested that further research be carried
out to investigate the electromyographic effect of the kangaroo position on other
muscles involved in the postural system, in both term and preterm newborns.
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Acknowledgements: We wish to thank the babies, parents and, especially, thank the
nursing technicians of the Kangaroo Unit at the Instituto de Medicina Integral Prof.
Fernando Figueira (IMIP), Recife – Brazil.
Contributors: RMM – Preparation of the study project, data collection and supervision
thereof, statistical analysis, research articles in the database, preparation of the article;
and approved the final manuscript as submitted; JECF – Guidance for the preparation of
the study project, supervision of data collection, statistical analysis, research articles in
the database; guidance and preparation of the article; and approved the final manuscript
as submitted; KTD – Preparation of the study project, data collection and supervision
thereof, data processing, statistical analysis, research articles in the database,
preparation of the article; and approved the final manuscript as submitted; GMSL –
Preparation of the study project, data collection and supervision thereof; and approved
the final manuscript as submitted; DAV: Preparation of the study project, supervision of
data collection, data processing; and approved the final manuscript as submitted;
Funding Source: Fundação de Amparo à Ciência e Tecnologia do Estado de
Pernambuco – FACEPE (APQ – 0552–4.08/100).
Financial Disclosure: Miranda RM was supported by post graduate scholarship from
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Diniz KT
was supported by post graduate scholarship from Fundação de Amparo à Ciência e
Tecnologia do Estado de Pernambuco (FACEPE).
Conflict of Interest: the authors declare that they have no competing interests.
Ethics approval: IMIP’s Ethics Committee for Research involving Human Beings
(protocol no.1902)
Data sharing statement: no additional data available.
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REFERENCES
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11. Moore ER, Anderson GC, Bergman N, et al. Early skin-to-skin contact for mothers
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13. Nagai S, Yonemoto N, Rabesandratana N, et al. Long-term effects of earlier
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14. Conde-Agudelo A, Belizán JM, Diaz-Rossello J. Kangaroo mother care to reduce
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16. Diniz KT, Cabral-Filho JE, Miranda RM, et al. Effect of the kangaroo position on
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17. Barradas J: Kangaroo position effect on the flexor muscle tone of newborn preterm.
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19. Als H, Tronick E, Lester BM, et al. The Braselton neonatal behavioral assessment
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20. Bolgla LA, Uhl TL. Reliability of electromyographic normalization methods for
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21. Lehman GJ, McGill SM. The importance of normalization in the interpretation of
surface electromyography: a proof of principle. J Manipulative Physiol Ther 1999;
22:444–46.
22. Barradas J, Fosceca A, Guimarães CLN, et al. Relationship between positioningof
premature infants in kangaroo mother care and early neuromotor development. J Pediatr
(Rio J) 2006;82:475–80.
23. Ferber SG, Makhoul IR. The effect of skin-to-skin contact (kangaroo care) shortly
after birth on the neurobehavioral responses of the term newborn: a randomized.
Controlled Trial. Pediatrics 2004;113:858–65.
24. Schneider C, Charpak N, Ruiz-Peláez JG, et al. Cerebral motor function in very
premature-at-birth adolescents: a brain stimulation exploration of kangaroo mother care
effects. Acta Paediatr 2012;101:1045-53.
25. Kaffashi F, Scher MS, Ludington-Hoe SM, et al. An analysis of
the kangaroo care intervention using neonatal EEG complexity: a preliminary study.
Clin Neurophysiol 2013;124:238-46.
26. Spittle A, Orton J, Anderson P, et al. Early developmental intervention programmes
post-hospital discharge to prevent motor and cognitive impairments in preterm infants.
Cochrane Database Syst Rev 2013;(6):CD005495.
27. Field TM, Schanberg SM, Scafidi F, et al. Tactile/kinesthetic stimulation effects on
preterm neonates. Pediatrics 1986; 77:654–58.
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STROBE Statement—checklist of items that should be included in reports of observational studies
Item
No Recommendation
Title and abstract 1 The study’s design with a commonly used term in the title: Electromyographic
activity of preterm newborns in kangaroo position: a cohort study.
The abstract has an informative and balanced summary of what was done and what
was found in the search.
Introduction
Background/rationale 2 A scientific and rational background for the research reported was used.
Objectives 3 Specific objectives and were prespecified hypotheses: The aim of this study was thus
to compare electromyographic activity in preterm newborns in kangaroo position with
the activity of newborns not placed in this position.
Methods
Study design 4 A cohort study was carried out.
Setting 5 Been described in the setting, locations / dates, including periods of recruitment,
exposure, follow-up and data collection
Participants 6 Cohort study - have been described: the eligibility criteria, and the sources and
methods of selection of participants; yet the methods of follow-up.
Variables 7 Were all clearly defined outcomes, exposures, predictors, potential confounders and
effect modifiers.
Data sources/
measurement
8 Surface electromyography (EMGs) was used to investigate muscle activity in the
brachial biceps at rest. Three groups were designed: 1) preterm newborns in kangaroo
position (PT – KAN), its electromyographic activity being recorded at 0h
(immediately before starting this position), and then at 48h from beginning the
position (but newborns being kept in the kangaroo position for 8-12 hours per day)
and at term equivalent age (40 ± 1 weeks); 2) preterm newborns not in kangaroo
position (PT – NKAN), the measurements being made at 0h and 48h; and 3) term
newborns (T), in which measurements were made at 24h of chronological age.
Bias 9 However, the reduced myoelectrical response in group T suggests that it is the
kangaroo position and not the growth of the newborns per se that is responsible for the
changes in electromyographic activity observed here. Apart from this limitation, the
sample size was lower than the estimate so it is a factor that may diminish the
reliability of our findings. However with a sample power of 90%, the large differences
found between the means and the statistically significant figures may support our
inferences.
Study size 10 A non-probabilistic convenient sample of newborns was selected, the size of the
sample being based on a previous study 17 that found variance of 2.6 in
electromyographic activity and estimated the minimum difference between means to
be 2 µV. With an alpha error of 0.05 and power of 90%, 21 individuals were
calculated for each group.
Quantitative variables 11 For analysis of muscle activity the signal was transformed into the Root Mean Square
(RMS) and normalized.20,21
For normalization, 100% corresponding to the maximum
peak electromyographic signal was taken as a reference. A period of 10s of the total
electromyographic reading (30s) was used.
Statistical methods 12 Comparison of the means of the groups was carried out after verifying the normality
of the distribution (Kolmogorov-Smirnov Test) and the homogeneity of variance
(Levene Test), by analysis of variance for repeated measurements, followed by
multiple comparisons (Holm-Sidak’s post hoc test) to test for the differences between
each two groups. The alpha error for rejection of the null hypothesis was 0.05.
Continued on next page
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Results
Participants 13 A cohort study was carried out, between July 2012 and January 2013, at the Instituto de
Medicina Integral Prof. Fernando Figueira (IMIP), in Recife, Brazil, with 64 hospitalized
newborns, from which 38 preterm in the Kangaroo Unit sector and 26 term in the Nursery
sector of the IMIP hospital.
Three groups were designed: Group 1 (n=25): preterm newborns in kangaroo position (PT –
KAN); 2) Group 2 (n=13): preterm newborns not in kangaroo position (PT – NKAN); and 3)
Group 3 (n=16): term newborns (T).
Descriptive data 14 The clinical and biological characteristics of the newborns in each group can be seen in
Table 1.
The newborns were kept in the kangaroo position for 8-12 hours per day, until the evaluation
after 48h.
Outcome data 15 In the PT – KAN group, electromyographic activity was first recorded before neonate being
in kangaroo position (0h). Immediately after taking this record, the neonates were placed for
the first time in the kangaroo position. The kangaroo position adopted was that
recommended by the Kangaroo Unit, in which the newborn is positioned against the adult’s
chest, face down, wrapped in a strip of flexible cloth. Subsequent recordings were taken
immediately after 48h of the kangaroo position and, finally, at term-equivalent age (40 ± 1
weeks). The newborns were kept in the kangaroo position for 8-12 hours per day, until the
evaluation after 48h.
In the PT – NKAN group the measurements were made at 0h and 48h. In the T group
electromyographic activity was measured only once, at a chronological age until 24h.
Main results and
Other analyses
16 Variances analyses comparison of the RMS among measurements (Table 2) demonstrated a
significant difference (F(5,108)= 56.69; p<0.001). The post hoc multiple comparisons (Holm-
Sidak Method) showed that in the PT-KAN Group the RMS was greater at 48h (p=0.004)
and at age equivalent to term (p=0.004) compared with the measurement at 0h, but there is
no statistically significant difference between the measurements at 48h and at age equivalent
to term. In the PT-NKAN group no significant difference was found between 0h and 48h.
The RMS in the PT-KAN group at age equivalent to term was greater than in the T Group
(p=0.004).
Discussion
Key results 17 The results were discussed based on current references.
Limitations 18 One limitation of the present study is the absence of a group of preterm newborns not in
kangaroo care followed up to age equivalent to term, as this would shed light on whether the
increase in electromyographic activity in the preterm newborns at age equivalent to term is
only related to the growth and development of the neonates and not the influence of the
kangaroo position. However, the reduced myoelectrical response in group T suggests that it
is the kangaroo position and not the growth of the newborns per se that is responsible for the
changes in electromyographic activity observed here. Apart from this limitation, the sample
size was lower than the estimate so it is a factor that may diminish the reliability of our
findings. However with a sample power of 90%, the large differences found between the
means and the statistically significant figures may support our inferences.
Interpretation 19 An overall cautious interpretation of the results was performed, considering objectives,
limitations, multiplicity of analyzes, results from similar studies, and other relevant evidence.
Generalisability 20 The generalization (external validity) of study results was discussed
Other information
Funding 21 The source of funding and the role of the funders for the study is described in the article.
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Electromyographic activity of preterm newborns in kangaroo position: a cohort study
Journal: BMJ Open
Manuscript ID: bmjopen-2014-005560.R2
Article Type: Research
Date Submitted by the Author: 02-Sep-2014
Complete List of Authors: Miranda, Rafael; Instituto de Medicina Integral Prof. Fernando Fiqueira, Pós-graduação Cabral Filho, José; Instituto de Medicina Integral Prof. Fernando Fiqueira, Pós-graduação Diniz, Kaísa; Instituto de Medicina Integral Prof. Fernando Fiqueira, Pós-graduação Lima, Geisy Maria; Instituto de Medicina Integral Prof. Fernando Fiqueira, Unidade Canguru Vasconcelos, Danilo; Instituto de Medicina Integral Prof. Fernando Fiqueira, Pós-graduação
<b>Primary Subject Heading</b>:
Paediatrics
Secondary Subject Heading: Public health
Keywords: PAEDIATRICS, Developmental neurology & neurodisability < PAEDIATRICS, Community child health < PAEDIATRICS
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1
Electromyographic activity of preterm newborns in kangaroo position: a cohort
study
Rafael Moura Miranda1; José Eulálio Cabral Filho
2; Kaísa Trovão Diniz
3; Geisy Maria
Souza Lima4; Danilo de Almeida Vasconcelos
5.
Affiliations: 1,2,3,5
Post Graduate Program of Instituto de Medicina Integral Prof.
Fernando Figueira (IMIP) – Recife – Brasil. 4Instituto de Medicina Integral Prof.
Fernando Figueira (IMIP) – Recife – Brasil.
Address correspondence to: Rafael Moura Miranda. Rua: Paula Batista, 270, Edifício
Morada Paula Batista, apto 203. Recife-PE/ Brasil; CEP: 51030-080.
Key-words: Kangaroo-Mother Care Method, Muscle Tonus, Electromyography, Child
Development, Motor Activity.
Word count: 3676
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ABSTRACT
Objective: to compare the electromyographic activity of preterm newborns placed in
kangaroo position with the activity of newborns not placed in this position.
Design: A cohort study.
Setting: A Kangaroo Unit sector and Nursery sector in a secondary and tertiary care at a
mother-child hospital in Recife, Brazil.
Participants: Preterm infants of gestational age of 27 to 34 weeks (n=38) and term
infants (n=39).
Primary and secondary outcome measures: Surface electromyography (EMGs) was
used to investigate muscle activity in the brachial biceps at rest. Three groups were
designed: 1) preterm newborns in kangaroo position (PT – KAN), whereas the newborn
remains in a vertical position, lying face down, with limbs flexed, dressed in light
clothes, maintaining skin-to-skin contact with the adult’s thorax. Her electromyographic
activity was recorded at 0h (immediately before starting this position), and then at 48h
after the beginning of the position (but newborns were kept in the kangaroo position for
8-12 hours per day) and at term equivalent age (40 ± 1 weeks); 2) preterm newborns not
in kangaroo position (PT – NKAN), the measurements were made at 0h and 48h; and 3)
term newborns (T), in which measurements were made at 24h of chronological age.
Results: The Root Mean Square (RMS) values showed significant differences among
the groups (F(5,108)= 56.69; p<0.001). The multiple comparisons showed that, RMS was
greater at 48h compared to 0h in the preterm group in kangaroo position, but not in the
group not submitted to kangaroo position. The RMS in the term equivalent aged group
in the kangaroo position was also greater when compared those at the term group.
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Conclusions: The kangaroo position increases electromyographic activity in the
brachial biceps of preterm newborns and those who have reached the age equivalent to
term.
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Strengths and limitations of this study
▪ The results of the study add new information about the effects of Kangaroo-Mother
Care for the preterm.
▪ The early initiation of the kangaroo position may, like other early intervention
programs, have a positive influence on the motor responses of the neonate, thereby
making it possible to influence the motor development of the preterm newborn.
It is important to point out the innovative nature of this study, since there is a lack of
studies specifically evaluating electromyographic activity in newborn in kangaroo
position.
▪ The sample size lower than the estimate in one of the Groups (PT-NKAN) is a factor
may diminish the reliability of our findings. However the sample power of 90%, the
large differences found between the means and the statistically significant results may
support our inference.
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INTRODUCTION
The Kangaroo Method (KM) is a kind of intervention that aims to improve the
health of low-weight preterm newborns.1 There is evidence that the method provides
various benefits. These benefits include an increase in body temperature,2,3
stabilization
of cardio-respiratory frequency,3,4
improved brain oxygenation,5
behavior improvement
(crying and sleep),6-8
pain reduction4,9,10
and greater adherence and duration of
breastfeeding.11-13
The method is also associated with a reduction in morbidity and
mortality,14,15
infections14
and hospital stay.15
The main feature of the method is the kangaroo position, whereby the newborn
remains in a vertical position, with limbs flexed, dressed in light clothes, maintaining
skin-to-skin contact and the face on with the adult’s thorax1. This position allows the
neonates to receive sensory, vestibular and postural stimuli and the effects on the motor
responses in the newborns has thus aroused some interest among investigators.16
Recently, some studies16,17
have shown an increase in electromyographic activity in
preterm newborns after different periods of time in the kangaroo position (up to 96h)
and this increase persists until an age equivalent to term. These results were pioneering,
although no study has yet been conducted in which these responses have been compared
with those of preterm newborns not in kangaroo position and those of term newborns.
The aim of the present study was thus to compare electromyographic activity in preterm
newborns in kangaroo position and the activity of newborns not placed in this position.
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METHODS
Participants
This cohort study was carried out between July 2012 and January 2013, at the
Instituto de Medicina Integral Prof. Fernando Figueira (IMIP), in Recife, Brazil, with 64
hospitalized newborns, 38 preterm were in the Kangaroo Unit sector and 26 terms were
in the Nursery sector at IMIP hospital.
The IMIP’s Kangaroo Unit covers a surface-area of 600 m2
and has a ward with
22 beds for clinically stable preterm newborns (with a respiratory frequency of between
30–60 inspirations per minute, a heart rate of between 120–160 beats per minute,
peripheric oxygen saturation of over 89%, absence of signs of respiratory distress, signs
cyanosis or pallor and pain) The newborns had to tolerate food, to breathe without the
use of any equipment and weigh more than 1,250 grams.
The Kangaroo Unit provides medical and nursing services and also speech
therapy and physiotherapy. In this unit, the newborns, referred to medical services, are
evaluated and undergo to an early stimulation program.
Newborns were included in the preterm groups if they had a gestational age of
27 to 34 weeks and a corrected age of until 35 weeks at the time of the first
electromyographic examination, and had not previously been in the kangaroo position.
Neonates were included in the group of term if they had a gestational age of 38-41
weeks. Neonates were only included when their Brazelton state during
electromyographic recording was 4 or 5 (inactive alert or alert with activity).
The exclusion factors for all the newborns were: Apgar lower than 7 in the 5th
minute, a history of grade III or IV intracranial hemorrhage (diagnosed by way of
transfontanelar ultra-sound and included in the medical records), seizures, congenital
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infections (cytomegalovirus, rubella, toxoplasmosis, syphilis and vertically transmitted
HIV), malformations of the Central Nervous System (hydrocephaly and genetic
syndromes), infections of the central nervous system (meningitis or encephalitis),
congenital cardiopathy, traumas during delivery (injuries to the brachial plexus,
dislocation of the hip and pelvis fractures) and gastro-esophageal reflux disorder.
All these inclusion and exclusion factors were evaluated using collected data
from patients’ medical records evaluated by neonatologists at the Neonatal Intensive
Care Unit, the Kangaroo Unit sector and the Nursery sector.
A convenient non-probabilistic sequential sample was obtained from the
newborns. The size of the sample was calculated based on a previous study 17
that found
variance of 2.6 in the electromyographic activity and estimated the minimum difference
between means of 2 µV. With an alpha error of 0.05 and the power of 90%, the sample
size result was 21 individuals for each group.
The project for this study was submitted to the IMIP’s Ethics Committee for
Research involving Human Beings and was approved (protocol number 1902). The
parents or guardians who agreed to participate in the study signed the free informed
consent.
Collection procedure
The electromyographic signal was obtained using a Miotool 400 ®
electromyograph (Miotec Equipamentos Biomédicos – Brazil). A system of channels
and a self-adhesive 4.2 mm diameter Ag/AgCl electrode (Meditrace 100®
) were used to
connect the equipment to the newborn’s body at examination. The electromyograph was
connected to a laptop using Myographic 2.0 software (Miotec Equipamentos
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Biomédicos - Brazil) to process the myoelectrical records. The sampling frequency was
2000 Hz and the electromyograms were amplified 2000 times.
The electromyographic signal was captured using two surface electrodes placed
on the central portion of the left brachial bíceps muscle, between the motor point and
the myotendinous junction, parallel to the muscle fibers, as recommended by the
SENIAM (Surface Electromyography for the Non-Invasive Assessment of Muscles)
project.18
The electrodes were adjusted to ensure the distance between them could not
exceed more than 20 mm and the reference electrode was always placed on the lateral
malleolus contralateral to the muscle under evaluation.
Before the measurements were performed, the newborn was placed on a small
wedge-shaped cushion at an angle of 30° relative to the horizontal plane. The
electromyographic activity captured the newborns in Brazelton state 4 or 5 (inactive
alert or alert with activity), respectively.19
There were three designed groups: Group 1 (n=25): preterm newborns in the
kangaroo position (PT – KAN); 2) Group 2 (n=13): preterm newborns not submitted in
kangaroo position (PT – NKAN); and 3) Group 3 (n=16): term newborns (T).
In the PT – KAN group, electromyographic activity was first recorded before the
neonates were in the kangaroo position (0h). Immediately after taking this record, the
neonates were placed for the first time in the kangaroo position. The kangaroo position
adopted was as recommended by the Kangaroo Unit, in which the newborn is
positioned in the adult’s breasts, face down, should be dressed in light clothes and
wrapped in a flexible cloth. Subsequent recordings were taken immediately after 48h of
the kangaroo position and, finally, at term-equivalent age (40 ± 1 weeks). The newborns
were kept in the kangaroo position for 8-12 hours per day until the evaluation after
48h. The newborns were removed from the Kangaroo Position (and placed on a soft
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cushion) for short intervals when the mothers would go to the restroom or to take a
shower, during breastfeeding or other forms of feeding.
The measurements in the PT – NKAN group were made at 0h and 48h. In the T
group of electromyographic activity was measured only once at a chronological age of
until 24h.
During data collection, the researchers asked the Kangaroo Unit not to give the
newborns physiotherapy. The newborns did not, therefore, undergo any kind of early
motor stimulation during data collection, except for oral stimulation done by speech
therapists, when it was necessary.
Treatment of Data and Statistical analysis
The muscle activity analysis signal was transformed to the Root Mean Square
(RMS) and normalized.20,21
For normalization, 100% corresponded to the maximum
peak of the electromyographic signal was taken as a reference. A period of 10s of total
electromyographic reading (30s) was used.
The comparison of means of the groups was carried out after verifying the
normality of the distribution (Kolmogorov-Smirnov Test) and the homogeneity of
variance (Levene Test), by repeated measurements analysis of variance, followed by
multiple comparisons (Holm-Sidak’s post hoc test) to test for the differences between
each two groups. The alpha error for rejection of the null hypothesis was 0.05.
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RESULTS
The clinical and biological characteristics of the newborns in each group are
presented in Table 1.
Table 1: Clinical and Biological Characteristics of Newborns.
PT-KAN
(n= 25)
PT-NKAN
(n=13)
T
(n=26)
Variables relating to newborn
Gestational age, weeks 31.06 (2.24) 31.21 (1.68) 39.27 (0.92)
Birthweight, grams 1314 (391.66) 1433.08 (349.72) 3191.36 (476.06)
Apgar score after 5’, Md (min-
max)
9 (7-10)
9 (7-9)
9 (8-10)
Corrected age on first
measurement (0h), weeks
34.86 (1.66)
33.93 (1.17)
39.84 (0.85)
For continuous variables, the mean (SD) is given; for ordinal variables (Apgar), the median (min-max).
The comparison on variances analyses of the RMS among measurements (Table
2) demonstrated a significant difference (F(5,108)= 56.69; p<0.001). The post hoc
multiple comparisons (Holm-Sidak Method) showed that in the PT-KAN Group, the
RMS was greater at 48h (p=0.004) and age equivalent to term measurement was
(p=0.004) compared with the measurement at 0h, but there is no statistically significant
difference between the measurements at 48h and age equivalent to term. In the PT-
NKAN group no significant difference was found between 0h and 48h.
The RMS in the PT-KAN group at age equivalent to term was greater than in the
T Group (p=0.004).
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Table 2: Electromyographic activity (RMS normalized) of the left brachial biceps
muscle in preterm newborns in the kangaroo position or not and in term
newborns.
Intervals between
measurements
Groups
PT-KAN
(��± DP)
PT-NKAN
(��± DP)
T
(��± DP)
0h
31.85±6.93
37.59±4.42
-
48h
49.30±4.91
38.17±3.10
-
TEA and TA
48.03±5.56
-
27.12±5.70
RMS: Root Mean Square. PT-KAN: preterm newborns in the kangaroo position. PT-NKAN: preterm newborns
not in the kangaroo position. T: term newborns. TEA: term equivalent age (for PT-KAN group). TA: term age (for
T group). *Analysis of variance for repeated measurements: F(5,108)= 56.69; p<0.001. Multiple comparisons
(Holm-Sidak Test): in the PT-KAN group: 0h x 48h (p=0.004), 0h x TEA (p=0.004). Between PT-KAN and T
groups: TEA x TA (p=0.004).
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DISCUSSION
The results of this study showed an increase in electromyographic activity of the
brachial biceps muscle in preterm newborns maintained at a kangaroo care environment
for 48h even when placed in the kangaroo position during 8 – 12h per day, which this
did not occur in the control group. These data suggest that the kangaroo position
changes myoelectrical activity in these newborns, at least in the flexor muscle case
evaluated here.
A similar result was observed in a previous study.17
Preterm newborns placed for
24h in the kangaroo position had an increase in the myoelectrical activity of flexor
muscles and this increase persisted even after 24h out of this position.
In later study, Diniz et al16
observed a growing increase in electromyographic
activity in the brachial biceps muscle during 96h in the kangaroo position. As in our
study, was observed this effect 48h after being placed in kangaroo position. However, it
is important to note the presence of the control group in our study which added weight
to our results. Also in accordance to of Diniz et al16
findings, the effect on
electromyographic activity remained constant until an age equivalent to term.
It is worth noting that the electromyographic activity in the PT-KAN group, at an
age equivalent to term, was significantly greater than in term newborns, although a
similarity between them was expected. This increased electromyographic activity might
be associated to the fact that preterm newborns received extra-uterine stimuli at age
equivalent to term, especially those provided by the kangaroo position. However, the
term newborns do not have the opportunity to receive such stimuli.
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The effect of the kangaroo position in inducing a more flexed posture in preterm
neonates is already known,22,23
and this also suggests a specific effect of the kangaroo
position on flexor muscles.
Recently Schneider et al24
used transcranial magnetic stimulation, showing that
preterm newborns underwent the kangaroo method had better connectivity and synaptic
efficacy of the motor routes in the brain at adolescence. Another study25
provided
electroencephalic evidence to the effect that the kangaroo interventions makes the brain
mature faster in healthy preterm newborns. These findings are relevant, since changes in
the myoelectrical parameter in response to the kangaroo position found in our study
may be associated with faster maturation of the brain and better performance of the
cerebral structures controlling motor activity. The mechanism behind this central motor
activation on the peripheral myoelectrical response is still a matter to study, but it
corroborates the conclusion that the kangaroo position has an effect on the muscle
response.
Delays in neuropsychomotor development are frequent in preterm newborns
owing to insufficient organization of their nervous systems.8,24
However, a recent meta-
analysis26
concluded that early intervention programs for premature babies have a
positive influence on motor development and there is evidence that tactile, synesthesic
and vestibular stimuli may influence the motor abilities of the newborns.27,28
We suggest, then, that early initiation of the kangaroo position may, like other
early intervention programs, have a positive influence on the motor development of the
preterm newborns. This hypothesis may be sustained by the characteristics on the
kangaroo position, which provide different stimuli for the newborn. Therefore,
considering that, in the kangaroo position the preterm newborn remains in skin-to-skin
contact with the adult breast, with its limbs flexed, in a vertical position1 and receiving
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various environmental inputs, such as sensory, postural and vestibular stimuli, the
kangaroo position16
may causing a considerable increase in motor activity. This
evidence suggests that the kangaroo position has a positive influence on the motor
activity in newborns that is physiologically represented by an alteration in the
myoelectrical parameters as observed here. Moreover, the myoelectrical alterations in
the flexor muscle are a relevant physiological response, since the kangaroo position
maintains a flexed posture.
One limitation on this present study is the absence of PT-NKAN (preterm
newborns not submitted in kangaroo position) followed up to age equivalent to term.
Such fact could clarify whether the increased electromyographic activity in PT-KAN
(preterm newborns in the kangaroo position) group at age equivalent to term is only
related to the growth and development of the neonates or the influence of the kangaroo
position. However, the reduced myoelectrical response in T group suggests that it is the
kangaroo position and not the growth of the newborns per se that is responsible for the
changes in the electromyographic activity observed here. Apart from this limitation, the
sample size was lower than the estimate so it is a factor that may diminish the reliability
of our findings. However with a sample power of 90%, the large differences found
between the means and statistically significant results may support our inferences.
In conclusion, although this is a preliminary study resulting to provide evidence
that the kangaroo position in short term induces an increase in the myoelectrical activity
in the preterm newborns which persists until the age equivalent to term. In addition, it
may be the fact that electromyographic activity in premature newborn at age equivalent
to term is greater than the term newborns and related to the different stimuli (tactile,
synesthetic and vestibular) that they have received. It is suggested that this intervention
induces changes in the flexor muscle function (flexor tonus), thereby making it possible
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to influence the motor development of the newborns. The age to which (in long terms)
these effects persist and whether they have positive effects need to be examined in
further studies.
It is important to point out the innovative nature of this study, although
preliminary, since there is a lack of studies specifically evaluating electromyographic
activity in newborns in the kangaroo position. It is suggested that further research
should be carried out to investigate the electromyographic effect of the kangaroo
position on other muscles involved in the postural system, both in newborns preterms
such as in term newborns.
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Acknowledgements: We wish to thank the babies, parents and, especially, the nursing
technicians at the Kangaroo Unit at the Instituto de Medicina Integral Prof. Fernando
Figueira (IMIP), Recife – Brazil.
Contributors: RMM – Preparation of the study project, data collection and supervision
thereof, statistical analysis, research articles in the database, preparation of the article;
and approved the final manuscript as submitted; JECF – Guidance for the preparation of
the study project, supervision of data collection, statistical analysis, research articles in
the database; guidance and preparation of the article; and approved the final manuscript
as submitted; KTD – Preparation of the study project, data collection and supervision
thereof, data processing, statistical analysis, research articles in the database,
preparation of the article; and approved the final manuscript as submitted; GMSL –
Preparation of the study project, data collection and supervision thereof; and approved
the final manuscript as submitted; DAV: Preparation of the study project, supervision of
data collection, data processing; and approved the final manuscript as submitted;
Acknowledgements: We wish to thank the babies, parents and, especially, the
nursing technicians at the Kangaroo Unit at the Instituto de Medicina Integral Prof.
Fernando Figueira (IMIP), Recife – Brazil. We would also like to thank the
translators Patricia Ferraz and Peter Ratclisse (Sharing English Traduções) , by
editing the text in the English language.
Funding Source: Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco –
FACEPE (APQ – 0552–4.08/100) and Fundo de Apoio à Pesquisa e Ensino do IMIP (FAPE-IMIP).
Financial Disclosure: Miranda RM was supported by the post graduate scholarship
from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and
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Diniz KT was supported by the post graduate scholarship from Fundação de Amparo à
Ciência e Tecnologia do Estado de Pernambuco (FACEPE).
Conflict of Interest: the authors declare that they have no competing interests.
Ethics approval: Ethics Committee for Research involving Human Beings at IMIP
(protocol number1902)
Data sharing statement: no additional data available.
REFERENCES
1. Nyqvist KH , Anderson GC, Bergman N, et al. Towards universal Kangaroo Mother
Care: recommendations and report from the First European conference and Seventh
International Workshop on Kangaroo Mother Care. Acta Paediatr 2010;99:820-6.
2. Mori R, Khanna R, Pledge D, et al. Meta-analysis of physiological effects of skin-to-
skin contact for newborns and mothers. Pediatr Int 2010;52:161-70.
3. Almeida CM, Almeida AFN, Forti EMP. Effects of kangaroo mother care on the vital
signs of low-weight preterm newborns. Rev bras fisioter 2007;11:1-5.
4. Johnston C, Campbell-Yeo M, Fernandes A, et al. Skin-to-skin care for procedural
pain in neonates. Cochrane Database Syst Rev. 2014 (4):CD008435.
5. Begum EA, Bonno M, Ohtani N, et al. Cerebral oxygenation responses
during kangaroo care in low birth weight infants. BMC Pediatr 2008;51:1-9.
6. Ferber SG, Makhoul IR. The Effect of Skin-to-Skin Contact (Kangaroo Care) Shortly
After Birth on the Neurobehavioral Responses of the Term Newborn: A Randomized,
Controlled Trial. Pediatrics 2004;113:858-65.
7. Lamy Filho F, Silva AA, Lamy ZC, et al. Evaluation of the neonatal outcomes of
the kangaroo mother method in Brazil. J Pediatr (Rio J) 2008; 84:428-35.
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8. Ludington-Hoe SM, Johnson MW, Morgan K, et al. Neurophysiologic assessment of
neonatal sleep organization: preliminary results of a randomized, controlled trial of skin
contact with preterm infants. Pediatrics 2006; 117:e909-23.
9. Saeidi R, Asnaashari Z, Amirnejad M, et al. Use of "kangaroo care" to alleviate the
intensity of vaccination pain in newborns. Iran J Pediatr 2011;21:99-102.
10. Nimbalkar SM, Chaudhary NS, Gadhavi KV, et al. Kangaroo Mother Care in
reducing pain in preterm neonates on heel prick. Indian J Pediatr 2013;80:6-10.
11. Moore ER, Anderson GC, Bergman N, et al. Early skin-to-skin contact for mothers
and their healthy newborn infants. Cochrane Database Syst Rev 2013;(6): CD003519.
12. Mahmood I, Jamal M, Khan N. Effect of mother-infant early skin-to-skin contact on
breastfeeding status: a randomized controlled trial. J Coll Physicians Surg Pak 2011;
21:601-5.
13. Nagai S, Yonemoto N, Rabesandratana N, et al. Long-term effects of earlier
initiated continuous Kangaroo Mother Care (KMC) for low-birth-weight (LBW) infants
in Madagascar. Acta Paediatr 2011;100:e241-7.
14. Conde-Agudelo A, Belizán JM, Diaz-Rossello J. Kangaroo mother care to reduce
morbidity and mortality in low birthweight infants. Cochrane Database Syst
Rev 2013;(6):CD002771.
15. Lawn JE, Mwansa-Kambafwile J, Horta BL, et al. Kangaroo mother care to prevent
neonatal deaths due to preterm birth complications. Int J Epidemiol 2010;39:i144–54.
16. Diniz KT, Cabral-Filho JE, Miranda RM, et al. Effect of the kangaroo position on
the electromyographic activity of preterm children: a follow-up study. BMC Pediatr
2013; 13:79.
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17. Barradas J: Kangaroo position effect on the flexor muscle tone of newborn preterm.
Fernando Figueira: Dissertation. Post Graduate Department the Institute of Integrated
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18. Hermens HJ, Freriks B, Disselhorst-Klug C, et al. Development of
recommendations for SEMG sensors and sensor placement procedures. J Electromyogr
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19. Als H, Tronick E, Lester BM, et al. The Braselton neonatal behavioral assessment
scale (BNBAS). J Abnorm Child Psychol 1977;5:215-29.
20. Bolgla LA, Uhl TL. Reliability of electromyographic normalization methods for
evaluating the hip musculature. J Electromyogr Kinesiol 2007;17:102–111.
21. Lehman GJ, McGill SM. The importance of normalization in the interpretation of
surface electromyography: a proof of principle. J Manipulative Physiol Ther 1999;
22:444–46.
22. Barradas J, Fosceca A, Guimarães CLN, et al. Relationship between positioningof
premature infants in kangaroo mother care and early neuromotor development. J Pediatr
(Rio J) 2006;82:475–80.
23. Ferber SG, Makhoul IR. The effect of skin-to-skin contact (kangaroo care) shortly
after birth on the neurobehavioral responses of the term newborn: a randomized.
Controlled Trial. Pediatrics 2004;113:858–65.
24. Schneider C, Charpak N, Ruiz-Peláez JG, et al. Cerebral motor function in very
premature-at-birth adolescents: a brain stimulation exploration of kangaroo mother care
effects. Acta Paediatr 2012;101:1045-53.
25. Kaffashi F, Scher MS, Ludington-Hoe SM, et al. An analysis of
the kangaroo care intervention using neonatal EEG complexity: a preliminary study.
Clin Neurophysiol 2013;124:238-46.
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26. Spittle A, Orton J, Anderson P, et al. Early developmental intervention programmes
post-hospital discharge to prevent motor and cognitive impairments in preterm infants.
Cochrane Database Syst Rev 2013;(6):CD005495.
27. Field TM, Schanberg SM, Scafidi F, et al. Tactile/kinesthetic stimulation effects on
preterm neonates. Pediatrics 1986; 77:654–58.
28. Symington AJ, Pinelli J. Developmental care for promoting development and
preventing morbidity in preterm infants. Cochrane Database Syst Rev 2013;(6):CD
001814.
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Electromyographic activity of preterm newborns in kangaroo position: a cohort
study
Rafael Moura Miranda1; José Eulálio Cabral Filho
2; Kaísa Trovão Diniz
3; Geisy Maria
Souza Lima4; Danilo de Almeida Vasconcelos
5.
Affiliations: 1,2,3,5
Post Graduate Program of Instituto de Medicina Integral Prof.
Fernando Figueira (IMIP) – Recife – Brasil. 4Instituto de Medicina Integral Prof.
Fernando Figueira (IMIP) – Recife – Brasil.
Address correspondence to: Rafael Moura Miranda. Rua: Paula Batista, 270, Edifício
Morada Paula Batista, apto 203. Recife-PE/ Brasil; CEP: 51030-080.
Key-words: Kangaroo-Mother Care Method, Muscle Tonus, Electromyography, Child
Development, Motor Activity.
Word count: 3676
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ABSTRACT
Objective: to compare the electromyographic activity of preterm newborns placed in
kangaroo position with the activity of newborns not placed in this position.
Design: A cohort study.
Setting: A Kangaroo Unit sector and Nursery sector in a secondary and tertiary care at a
mother-child hospital in Recife, Brazil.
Participants: Preterm infants of gestational age of 27 to 34 weeks (n=38) and term
infants (n=39).
Primary and secondary outcome measures: Surface electromyography (EMGs) was
used to investigate muscle activity in the brachial biceps at rest. Three groups were
designed: 1) preterm newborns in kangaroo position (PT – KAN), whereas the newborn
remains in a vertical position, lying face down, with limbs flexed, dressed in light
clothes, maintaining skin-to-skin contact with the adult’s thorax. Her electromyographic
activity was recorded at 0h (immediately before starting this position), and then at 48h
after the beginning of the position (but newborns were kept in the kangaroo position for
8-12 hours per day) and at term equivalent age (40 ± 1 weeks); 2) preterm newborns not
in kangaroo position (PT – NKAN), the measurements were made at 0h and 48h; and 3)
term newborns (T), in which measurements were made at 24h of chronological age.
Results: The Root Mean Square (RMS) values showed significant differences among
the groups (F(5,108)= 56.69; p<0.001). The multiple comparisons showed that, RMS was
greater at 48h compared to 0h in the preterm group in kangaroo position, but not in the
group not submitted to kangaroo position. The RMS in the term equivalent aged group
in the kangaroo position was also greater when compared those at the term group.
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Conclusions: The kangaroo position increases electromyographic activity in the
brachial biceps of preterm newborns and those who have reached the age equivalent to
term.
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Strengths and limitations of this study
▪ The results of the study add new information about the effects of Kangaroo-Mother
Care for the preterm.
▪ The early initiation of the kangaroo position may, like other early intervention
programs, have a positive influence on the motor responses of the neonate, thereby
making it possible to influence the motor development of the preterm newborn.
It is important to point out the innovative nature of this study, since there is a lack of
studies specifically evaluating electromyographic activity in newborn in kangaroo
position.
▪ The sample size lower than the estimate in one of the Groups (PT-NKAN) is a factor
may diminish the reliability of our findings. However the sample power of 90%, the
large differences found between the means and the statistically significant results may
support our inference.
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INTRODUCTION
The Kangaroo Method (KM) is a kind of intervention that aims to improve the
health of low-weight preterm newborns.1 There is evidence that the method provides
various benefits. These benefits include an increase in body temperature,2,3
stabilization
of cardio-respiratory frequency,3,4
improved brain oxygenation,5
behavior improvement
(crying and sleep),6-8
pain reduction4,9,10
and greater adherence and duration of
breastfeeding.11-13
The method is also associated with a reduction in morbidity and
mortality,14,15
infections14
and hospital stay.15
The main feature of the method is the kangaroo position, whereby the newborn
remains in a vertical position, with limbs flexed, dressed in light clothes, maintaining
skin-to-skin contact and the face on with the adult’s thorax1. This position allows the
neonates to receive sensory, vestibular and postural stimuli and the effects on the motor
responses in the newborns has thus aroused some interest among investigators.16
Recently, some studies16,17
have shown an increase in electromyographic activity in
preterm newborns after different periods of time in the kangaroo position (up to 96h)
and this increase persists until an age equivalent to term. These results were pioneering,
although no study has yet been conducted in which these responses have been compared
with those of preterm newborns not in kangaroo position and those of term newborns.
The aim of the present study was thus to compare electromyographic activity in preterm
newborns in kangaroo position and the activity of newborns not placed in this position.
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METHODS
Participants
This cohort study was carried out between July 2012 and January 2013, at the
Instituto de Medicina Integral Prof. Fernando Figueira (IMIP), in Recife, Brazil, with 64
hospitalized newborns, 38 preterm were in the Kangaroo Unit sector and 26 terms were
in the Nursery sector at IMIP hospital.
The IMIP’s Kangaroo Unit covers a surface-area of 600 m2
and has a ward with
22 beds for clinically stable preterm newborns (with a respiratory frequency of between
30–60 inspirations per minute, a heart rate of between 120–160 beats per minute,
peripheric oxygen saturation of over 89%, absence of signs of respiratory distress, signs
cyanosis or pallor and pain) The newborns had to tolerate food, to breathe without the
use of any equipment and weigh more than 1,250 grams.
The Kangaroo Unit provides medical and nursing services and also speech
therapy and physiotherapy. In this unit, the newborns, referred to medical services, are
evaluated and undergo to an early stimulation program.
Newborns were included in the preterm groups if they had a gestational age of
27 to 34 weeks and a corrected age of until 35 weeks at the time of the first
electromyographic examination, and had not previously been in the kangaroo position.
Neonates were included in the group of term if they had a gestational age of 38-41
weeks. Neonates were only included when their Brazelton state during
electromyographic recording was 4 or 5 (inactive alert or alert with activity).
The exclusion factors for all the newborns were: Apgar lower than 7 in the 5th
minute, a history of grade III or IV intracranial hemorrhage (diagnosed by way of
transfontanelar ultra-sound and included in the medical records), seizures, congenital
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infections (cytomegalovirus, rubella, toxoplasmosis, syphilis and vertically transmitted
HIV), malformations of the Central Nervous System (hydrocephaly and genetic
syndromes), infections of the central nervous system (meningitis or encephalitis),
congenital cardiopathy, traumas during delivery (injuries to the brachial plexus,
dislocation of the hip and pelvis fractures) and gastro-esophageal reflux disorder.
All these inclusion and exclusion factors were evaluated using collected data
from patients’ medical records evaluated by neonatologists at the Neonatal Intensive
Care Unit, the Kangaroo Unit sector and the Nursery sector.
A convenient non-probabilistic sequential sample was obtained from the
newborns. The size of the sample was calculated based on a previous study 17
that found
variance of 2.6 in the electromyographic activity and estimated the minimum difference
between means of 2 µV. With an alpha error of 0.05 and the power of 90%, the sample
size result was 21 individuals for each group.
The project for this study was submitted to the IMIP’s Ethics Committee for
Research involving Human Beings and was approved (protocol number 1902). The
parents or guardians who agreed to participate in the study signed the free informed
consent.
Collection procedure
The electromyographic signal was obtained using a Miotool 400 ®
electromyograph (Miotec Equipamentos Biomédicos – Brazil). A system of channels
and a self-adhesive 4.2 mm diameter Ag/AgCl electrode (Meditrace 100®
) were used to
connect the equipment to the newborn’s body at examination. The electromyograph was
connected to a laptop using Myographic 2.0 software (Miotec Equipamentos
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Biomédicos - Brazil) to process the myoelectrical records. The sampling frequency was
2000 Hz and the electromyograms were amplified 2000 times.
The electromyographic signal was captured using two surface electrodes placed
on the central portion of the left brachial bíceps muscle, between the motor point and
the myotendinous junction, parallel to the muscle fibers, as recommended by the
SENIAM (Surface Electromyography for the Non-Invasive Assessment of Muscles)
project.18
The electrodes were adjusted to ensure the distance between them could not
exceed more than 20 mm and the reference electrode was always placed on the lateral
malleolus contralateral to the muscle under evaluation.
Before the measurements were performed, the newborn was placed on a small
wedge-shaped cushion at an angle of 30° relative to the horizontal plane. The
electromyographic activity captured the newborns in Brazelton state 4 or 5 (inactive
alert or alert with activity), respectively.19
There were three designed groups: Group 1 (n=25): preterm newborns in the
kangaroo position (PT – KAN); 2) Group 2 (n=13): preterm newborns not submitted in
kangaroo position (PT – NKAN); and 3) Group 3 (n=16): term newborns (T).
In the PT – KAN group, electromyographic activity was first recorded before the
neonates were in the kangaroo position (0h). Immediately after taking this record, the
neonates were placed for the first time in the kangaroo position. The kangaroo position
adopted was as recommended by the Kangaroo Unit, in which the newborn is
positioned in the adult’s breasts, face down, should be dressed in light clothes and
wrapped in a flexible cloth. Subsequent recordings were taken immediately after 48h of
the kangaroo position and, finally, at term-equivalent age (40 ± 1 weeks). The newborns
were kept in the kangaroo position for 8-12 hours per day until the evaluation after
48h. The newborns were removed from the Kangaroo Position (and placed on a soft
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cushion) for short intervals when the mothers would go to the restroom or to take a
shower, during breastfeeding or other forms of feeding.
The measurements in the PT – NKAN group were made at 0h and 48h. In the T
group of electromyographic activity was measured only once at a chronological age of
until 24h.
During data collection, the researchers asked the Kangaroo Unit not to give the
newborns physiotherapy. The newborns did not, therefore, undergo any kind of early
motor stimulation during data collection, except for oral stimulation done by speech
therapists, when it was necessary.
Treatment of Data and Statistical analysis
The muscle activity analysis signal was transformed to the Root Mean Square
(RMS) and normalized.20,21
For normalization, 100% corresponded to the maximum
peak of the electromyographic signal was taken as a reference. A period of 10s of total
electromyographic reading (30s) was used.
The comparison of means of the groups was carried out after verifying the
normality of the distribution (Kolmogorov-Smirnov Test) and the homogeneity of
variance (Levene Test), by repeated measurements analysis of variance, followed by
multiple comparisons (Holm-Sidak’s post hoc test) to test for the differences between
each two groups. The alpha error for rejection of the null hypothesis was 0.05.
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RESULTS
The clinical and biological characteristics of the newborns in each group are
presented in Table 1.
Table 1: Clinical and Biological Characteristics of Newborns.
PT-KAN
(n= 25)
PT-NKAN
(n=13)
T
(n=26)
Variables relating to newborn
Gestational age, weeks 31.06 (2.24) 31.21 (1.68) 39.27 (0.92)
Birthweight, grams 1314 (391.66) 1433.08 (349.72) 3191.36 (476.06)
Apgar score after 5’, Md (min-
max)
9 (7-10)
9 (7-9)
9 (8-10)
Corrected age on first
measurement (0h), weeks
34.86 (1.66)
33.93 (1.17)
39.84 (0.85)
For continuous variables, the mean (SD) is given; for ordinal variables (Apgar), the median (min-max).
The comparison on variances analyses of the RMS among measurements (Table
2) demonstrated a significant difference (F(5,108)= 56.69; p<0.001). The post hoc
multiple comparisons (Holm-Sidak Method) showed that in the PT-KAN Group, the
RMS was greater at 48h (p=0.004) and age equivalent to term measurement was
(p=0.004) compared with the measurement at 0h, but there is no statistically significant
difference between the measurements at 48h and age equivalent to term. In the PT-
NKAN group no significant difference was found between 0h and 48h.
The RMS in the PT-KAN group at age equivalent to term was greater than in the
T Group (p=0.004).
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Table 2: Electromyographic activity (RMS normalized) of the left brachial biceps
muscle in preterm newborns in the kangaroo position or not and in term
newborns.
Intervals between
measurements
Groups
PT-KAN
(��± DP)
PT-NKAN
(��± DP)
T
(��± DP)
0h
31.85±6.93
37.59±4.42
-
48h
49.30±4.91
38.17±3.10
-
TEA and TA
48.03±5.56
-
27.12±5.70
RMS: Root Mean Square. PT-KAN: preterm newborns in the kangaroo position. PT-NKAN: preterm newborns
not in the kangaroo position. T: term newborns. TEA: term equivalent age (for PT-KAN group). TA: term age (for
T group). *Analysis of variance for repeated measurements: F(5,108)= 56.69; p<0.001. Multiple comparisons
(Holm-Sidak Test): in the PT-KAN group: 0h x 48h (p=0.004), 0h x TEA (p=0.004). Between PT-KAN and T
groups: TEA x TA (p=0.004).
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DISCUSSION
The results of this study showed an increase in electromyographic activity of the
brachial biceps muscle in preterm newborns maintained at a kangaroo care environment
for 48h even when placed in the kangaroo position during 8 – 12h per day, which this
did not occur in the control group. These data suggest that the kangaroo position
changes myoelectrical activity in these newborns, at least in the flexor muscle case
evaluated here.
A similar result was observed in a previous study.17
Preterm newborns placed for
24h in the kangaroo position had an increase in the myoelectrical activity of flexor
muscles and this increase persisted even after 24h out of this position.
In later study, Diniz et al16
observed a growing increase in electromyographic
activity in the brachial biceps muscle during 96h in the kangaroo position. As in our
study, was observed this effect 48h after being placed in kangaroo position. However, it
is important to note the presence of the control group in our study which added weight
to our results. Also in accordance to of Diniz et al16
findings, the effect on
electromyographic activity remained constant until an age equivalent to term.
It is worth noting that the electromyographic activity in the PT-KAN group, at an
age equivalent to term, was significantly greater than in term newborns, although a
similarity between them was expected. This increased electromyographic activity might
be associated to the fact that preterm newborns received extra-uterine stimuli at age
equivalent to term, especially those provided by the kangaroo position. However, the
term newborns do not have the opportunity to receive such stimuli.
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The effect of the kangaroo position in inducing a more flexed posture in preterm
neonates is already known,22,23
and this also suggests a specific effect of the kangaroo
position on flexor muscles.
Recently Schneider et al24
used transcranial magnetic stimulation, showing that
preterm newborns underwent the kangaroo method had better connectivity and synaptic
efficacy of the motor routes in the brain at adolescence. Another study25
provided
electroencephalic evidence to the effect that the kangaroo interventions makes the brain
mature faster in healthy preterm newborns. These findings are relevant, since changes in
the myoelectrical parameter in response to the kangaroo position found in our study
may be associated with faster maturation of the brain and better performance of the
cerebral structures controlling motor activity. The mechanism behind this central motor
activation on the peripheral myoelectrical response is still a matter to study, but it
corroborates the conclusion that the kangaroo position has an effect on the muscle
response.
Delays in neuropsychomotor development are frequent in preterm newborns
owing to insufficient organization of their nervous systems.8,24
However, a recent meta-
analysis26
concluded that early intervention programs for premature babies have a
positive influence on motor development and there is evidence that tactile, synesthesic
and vestibular stimuli may influence the motor abilities of the newborns.27,28
We suggest, then, that early initiation of the kangaroo position may, like other
early intervention programs, have a positive influence on the motor development of the
preterm newborns. This hypothesis may be sustained by the characteristics on the
kangaroo position, which provide different stimuli for the newborn. Therefore,
considering that, in the kangaroo position the preterm newborn remains in skin-to-skin
contact with the adult breast, with its limbs flexed, in a vertical position1 and receiving
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various environmental inputs, such as sensory, postural and vestibular stimuli, the
kangaroo position16
may causing a considerable increase in motor activity. This
evidence suggests that the kangaroo position has a positive influence on the motor
activity in newborns that is physiologically represented by an alteration in the
myoelectrical parameters as observed here. Moreover, the myoelectrical alterations in
the flexor muscle are a relevant physiological response, since the kangaroo position
maintains a flexed posture.
One limitation on this present study is the absence of PT-NKAN (preterm
newborns not submitted in kangaroo position) followed up to age equivalent to term.
Such fact could clarify whether the increased electromyographic activity in PT-KAN
(preterm newborns in the kangaroo position) group at age equivalent to term is only
related to the growth and development of the neonates or the influence of the kangaroo
position. However, the reduced myoelectrical response in T group suggests that it is the
kangaroo position and not the growth of the newborns per se that is responsible for the
changes in the electromyographic activity observed here. Apart from this limitation, the
sample size was lower than the estimate so it is a factor that may diminish the reliability
of our findings. However with a sample power of 90%, the large differences found
between the means and statistically significant results may support our inferences.
In conclusion, although this is a preliminary study resulting to provide evidence
that the kangaroo position in short term induces an increase in the myoelectrical activity
in the preterm newborns which persists until the age equivalent to term. In addition, it
may be the fact that electromyographic activity in premature newborn at age equivalent
to term is greater than the term newborns and related to the different stimuli (tactile,
synesthetic and vestibular) that they have received. It is suggested that this intervention
induces changes in the flexor muscle function (flexor tonus), thereby making it possible
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to influence the motor development of the newborns. The age to which (in long terms)
these effects persist and whether they have positive effects need to be examined in
further studies.
It is important to point out the innovative nature of this study, although
preliminary, since there is a lack of studies specifically evaluating electromyographic
activity in newborns in the kangaroo position. It is suggested that further research
should be carried out to investigate the electromyographic effect of the kangaroo
position on other muscles involved in the postural system, both in newborns preterms
such as in term newborns.
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Acknowledgements: We wish to thank the babies, parents and, especially, the nursing
technicians at the Kangaroo Unit at the Instituto de Medicina Integral Prof. Fernando
Figueira (IMIP), Recife – Brazil.
Contributors: RMM – Preparation of the study project, data collection and supervision
thereof, statistical analysis, research articles in the database, preparation of the article;
and approved the final manuscript as submitted; JECF – Guidance for the preparation of
the study project, supervision of data collection, statistical analysis, research articles in
the database; guidance and preparation of the article; and approved the final manuscript
as submitted; KTD – Preparation of the study project, data collection and supervision
thereof, data processing, statistical analysis, research articles in the database,
preparation of the article; and approved the final manuscript as submitted; GMSL –
Preparation of the study project, data collection and supervision thereof; and approved
the final manuscript as submitted; DAV: Preparation of the study project, supervision of
data collection, data processing; and approved the final manuscript as submitted;
Funding Source: Fundação de Amparo à Ciência e Tecnologia do Estado de
Pernambuco – FACEPE (APQ – 0552–4.08/100).
Financial Disclosure: Miranda RM was supported by the post graduate scholarship
from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and
Diniz KT was supported by the post graduate scholarship from Fundação de Amparo à
Ciência e Tecnologia do Estado de Pernambuco (FACEPE).
Conflict of Interest: the authors declare that they have no competing interests.
Ethics approval: Ethics Committee for Research involving Human Beings at IMIP
(protocol number1902)
Data sharing statement: no additional data available.
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REFERENCES
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skin contact for newborns and mothers. Pediatr Int 2010;52:161-70.
3. Almeida CM, Almeida AFN, Forti EMP. Effects of kangaroo mother care on the vital
signs of low-weight preterm newborns. Rev bras fisioter 2007;11:1-5.
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6. Ferber SG, Makhoul IR. The Effect of Skin-to-Skin Contact (Kangaroo Care) Shortly
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11. Moore ER, Anderson GC, Bergman N, et al. Early skin-to-skin contact for mothers
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14. Conde-Agudelo A, Belizán JM, Diaz-Rossello J. Kangaroo mother care to reduce
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16. Diniz KT, Cabral-Filho JE, Miranda RM, et al. Effect of the kangaroo position on
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17. Barradas J: Kangaroo position effect on the flexor muscle tone of newborn preterm.
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19. Als H, Tronick E, Lester BM, et al. The Braselton neonatal behavioral assessment
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20. Bolgla LA, Uhl TL. Reliability of electromyographic normalization methods for
evaluating the hip musculature. J Electromyogr Kinesiol 2007;17:102–111.
21. Lehman GJ, McGill SM. The importance of normalization in the interpretation of
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22. Barradas J, Fosceca A, Guimarães CLN, et al. Relationship between positioningof
premature infants in kangaroo mother care and early neuromotor development. J Pediatr
(Rio J) 2006;82:475–80.
23. Ferber SG, Makhoul IR. The effect of skin-to-skin contact (kangaroo care) shortly
after birth on the neurobehavioral responses of the term newborn: a randomized.
Controlled Trial. Pediatrics 2004;113:858–65.
24. Schneider C, Charpak N, Ruiz-Peláez JG, et al. Cerebral motor function in very
premature-at-birth adolescents: a brain stimulation exploration of kangaroo mother care
effects. Acta Paediatr 2012;101:1045-53.
25. Kaffashi F, Scher MS, Ludington-Hoe SM, et al. An analysis of
the kangaroo care intervention using neonatal EEG complexity: a preliminary study.
Clin Neurophysiol 2013;124:238-46.
26. Spittle A, Orton J, Anderson P, et al. Early developmental intervention programmes
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Cochrane Database Syst Rev 2013;(6):CD005495.
27. Field TM, Schanberg SM, Scafidi F, et al. Tactile/kinesthetic stimulation effects on
preterm neonates. Pediatrics 1986; 77:654–58.
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STROBE Statement—checklist of items that should be included in reports of observational studies
Item
No Recommendation
Title and abstract 1 The study’s design with a commonly used term in the title: Electromyographic
activity of preterm newborns in kangaroo position: a cohort study.
The abstract has an informative and balanced summary of what was done and what
was found in the search.
Introduction
Background/rationale 2 A scientific and rational background for the research reported was used.
Objectives 3 Specific objectives and were prespecified hypotheses: The aim of this study was thus
to compare electromyographic activity in preterm newborns in kangaroo position with
the activity of newborns not placed in this position.
Methods
Study design 4 A cohort study was carried out.
Setting 5 Been described in the setting, locations / dates, including periods of recruitment,
exposure, follow-up and data collection
Participants 6 Cohort study - have been described: the eligibility criteria, and the sources and
methods of selection of participants; yet the methods of follow-up.
Variables 7 Were all clearly defined outcomes, exposures, predictors, potential confounders and
effect modifiers.
Data sources/
measurement
8 Surface electromyography (EMGs) was used to investigate muscle activity in the
brachial biceps at rest. Three groups were designed: 1) preterm newborns in kangaroo
position (PT – KAN), its electromyographic activity being recorded at 0h
(immediately before starting this position), and then at 48h from beginning the
position (but newborns being kept in the kangaroo position for 8-12 hours per day)
and at term equivalent age (40 ± 1 weeks); 2) preterm newborns not in kangaroo
position (PT – NKAN), the measurements being made at 0h and 48h; and 3) term
newborns (T), in which measurements were made at 24h of chronological age.
Bias 9 However, the reduced myoelectrical response in group T suggests that it is the
kangaroo position and not the growth of the newborns per se that is responsible for the
changes in electromyographic activity observed here. Apart from this limitation, the
sample size was lower than the estimate so it is a factor that may diminish the
reliability of our findings. However with a sample power of 90%, the large differences
found between the means and the statistically significant figures may support our
inferences.
Study size 10 A non-probabilistic convenient sample of newborns was selected, the size of the
sample being based on a previous study 17 that found variance of 2.6 in
electromyographic activity and estimated the minimum difference between means to
be 2 µV. With an alpha error of 0.05 and power of 90%, 21 individuals were
calculated for each group.
Quantitative variables 11 For analysis of muscle activity the signal was transformed into the Root Mean Square
(RMS) and normalized.20,21
For normalization, 100% corresponding to the maximum
peak electromyographic signal was taken as a reference. A period of 10s of the total
electromyographic reading (30s) was used.
Statistical methods 12 Comparison of the means of the groups was carried out after verifying the normality
of the distribution (Kolmogorov-Smirnov Test) and the homogeneity of variance
(Levene Test), by analysis of variance for repeated measurements, followed by
multiple comparisons (Holm-Sidak’s post hoc test) to test for the differences between
each two groups. The alpha error for rejection of the null hypothesis was 0.05.
Continued on next page
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Results
Participants 13 A cohort study was carried out, between July 2012 and January 2013, at the Instituto de
Medicina Integral Prof. Fernando Figueira (IMIP), in Recife, Brazil, with 64 hospitalized
newborns, from which 38 preterm in the Kangaroo Unit sector and 26 term in the Nursery
sector of the IMIP hospital.
Three groups were designed: Group 1 (n=25): preterm newborns in kangaroo position (PT –
KAN); 2) Group 2 (n=13): preterm newborns not in kangaroo position (PT – NKAN); and 3)
Group 3 (n=16): term newborns (T).
Descriptive data 14 The clinical and biological characteristics of the newborns in each group can be seen in
Table 1.
The newborns were kept in the kangaroo position for 8-12 hours per day, until the evaluation
after 48h.
Outcome data 15 In the PT – KAN group, electromyographic activity was first recorded before neonate being
in kangaroo position (0h). Immediately after taking this record, the neonates were placed for
the first time in the kangaroo position. The kangaroo position adopted was that
recommended by the Kangaroo Unit, in which the newborn is positioned against the adult’s
chest, face down, wrapped in a strip of flexible cloth. Subsequent recordings were taken
immediately after 48h of the kangaroo position and, finally, at term-equivalent age (40 ± 1
weeks). The newborns were kept in the kangaroo position for 8-12 hours per day, until the
evaluation after 48h.
In the PT – NKAN group the measurements were made at 0h and 48h. In the T group
electromyographic activity was measured only once, at a chronological age until 24h.
Main results and
Other analyses
16 Variances analyses comparison of the RMS among measurements (Table 2) demonstrated a
significant difference (F(5,108)= 56.69; p<0.001). The post hoc multiple comparisons (Holm-
Sidak Method) showed that in the PT-KAN Group the RMS was greater at 48h (p=0.004)
and at age equivalent to term (p=0.004) compared with the measurement at 0h, but there is
no statistically significant difference between the measurements at 48h and at age equivalent
to term. In the PT-NKAN group no significant difference was found between 0h and 48h.
The RMS in the PT-KAN group at age equivalent to term was greater than in the T Group
(p=0.004).
Discussion
Key results 17 The results were discussed based on current references.
Limitations 18 One limitation of the present study is the absence of a group of preterm newborns not in
kangaroo care followed up to age equivalent to term, as this would shed light on whether the
increase in electromyographic activity in the preterm newborns at age equivalent to term is
only related to the growth and development of the neonates and not the influence of the
kangaroo position. However, the reduced myoelectrical response in group T suggests that it
is the kangaroo position and not the growth of the newborns per se that is responsible for the
changes in electromyographic activity observed here. Apart from this limitation, the sample
size was lower than the estimate so it is a factor that may diminish the reliability of our
findings. However with a sample power of 90%, the large differences found between the
means and the statistically significant figures may support our inferences.
Interpretation 19 An overall cautious interpretation of the results was performed, considering objectives,
limitations, multiplicity of analyzes, results from similar studies, and other relevant evidence.
Generalisability 20 The generalization (external validity) of study results was discussed
Other information
Funding 21 The source of funding and the role of the funders for the study is described in the article.
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