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    Risk Factors and Outcomes Associated With a ShortUmbilical Cord

    Paula Krakowiak, MS, Erin N. Smith, BS, Guy de Bruyn, MBBCH, andMona T. Lydon-Rochelle, PhD, MPH

    OBJECTIVE: To identify risk factors and outcomes associ-ated with a short umbilical cord.

    METHODS: We conducted a population-based case-con-trol study using linked Washington State birth certificate

    hospital discharge data for singleton live births from 1987 to1998 to assess the association between maternal, pregnancy,delivery, and infant characteristics and short umbilicalcord. Cases (n 3,565) were infants diagnosed with a shortumbilical cord. Controls (n 14,260) were randomly selectedfrom among births without a diagnosis of short umbilicalcord.

    RESULTS: Case mothers were less likely to be overweight(body mass index 25 or more, odds ratio [OR] 0.7; 95%confidence interval [CI] 0.6, 0.8) and more likely to beprimiparous (OR 1.4; 95% CI 1.3, 1.6). Case infants weremore likely to be female (OR 1.3; 95% CI 1.2, 1.4), have acongenital malformation (OR 1.6; 95% CI 1.4, 1.8), and besmall for their gestational age (risk ratio [RR] 1.6; 95% CI1.4, 1.9). A short cord was associated with increased risk formaternal labor and delivery complications, including re-

    tained placenta (RR 1.6; 95% CI 1.2, 2.3) and operativevaginal delivery (RR 1.4; 95% CI 1.3, 1.5). Adverse fetaland infant outcomes in cases included fetal distress (RR1.8; 95% CI 1.6, 2.1) and death within the first year of lifeamong term infants (RR 2.4; 95% CI 1.2, 4.6).

    CONCLUSION: Modifiable risk factors associated with thedevelopment of a short cord were not identified. Casemothers and infants are more likely to experience la-bor and delivery complications. Term case infants had a2-fold increased risk of death, which suggests closer post-partum monitoring of these infants. (Obstet Gynecol

    2004;103:119 127. 2004 by The American College ofObstetricians and Gynecologists.)

    LEVEL OF EVIDENCE: II-2

    Short umbilical cords occur in approximately 6% ofpregnancies.1The presence of a short umbilical cord hasbeen associated with antepartum abnormalities and risk

    factors for complications of labor and delivery. Fewstudies have investigated both risk factors and outcomesassociated with this relatively rare condition. A shortumbilical cord has been associated with various intra-uterine conditions and exposures that may impact inutero development and activity of the fetus, includingoligohydramnios, amnion rupture, and uterine struc-tural anomalies,2,3 as well as substances such as alcoholand-blockers.46 The pathogenesis of short umbilicalcords remains unclear. One prominent hypothesis toexplain the ontogeny of the umbilical cord is the stretchhypothesis, which attributes the development of a short

    umbilical cord to intrauterine constraint.24

    Previousstudies contain conflicting results on the relationship ofexposures, such as parity79 and sex of the fetus,1,1012 toshort umbilical cords. Similarly, previous studies reportinconsistent associations between outcomes, such as neo-natal resuscitation and short umbilical cords.1,13 How-ever, past studies have consistently reported selectedlabor and delivery complications associated with the

    presence of short cords, including abruptio placenta,prolonged labor,1, and fetal distress.7,13 Therefore, anassessment of exposures is important and would providenew information about the possible etiology of short

    umbilical cords and its association with adverse neonataloutcomes.

    We used maternally linked birth records to deter-mine risk factors for a short umbilical cord, to examinethe risk of selected labor and delivery outcomes attribut-able to short umbilical cords, and to identify the risk ofselected fetal and infant outcomes attributable to shortumbilical cords among women delivering singleton live

    births.

    From the Department of Epidemiology, School of Public Health and CommunityMedicine, Molecular and Cellular Biology Program, Division of Allergy andInfectious Diseases, School of Medicine, Department of Family and Child Nursing,School of Nursing, and Department of Health Services, School of Public Healthand Community Medicine, University of Washington, Seattle, Washington; andDivisions of Human Biology and Clinical Research and Program in InfectiousDiseases, Fred Hutchinson Cancer Research Center, Seattle, Washington.

    This work was in part supported by grants from the National Institutes of Health(NCI T32 CA80416 and RO1 DE12925-02).

    The authors thank William OBrien for data linkage and management support.

    VOL. 103, NO. 1, JANUARY 2004119 2004 by The American College of Obstetricians and Gynecologists. 0029-7844/04/$30.00

    Published by Lippincott Williams & Wilkins. doi:10.1097/01.AOG.0000102706.84063.C7

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    MATERIALS AND METHODS

    We conducted a population-based retrospective studyusing data obtained from the Washington State BirthEvents Records Database. This database links more than95% of birth certificate records to maternal and infanthospital discharge records for deliveries that occur in allnonfederal hospitals in Washington.14 Birth records arealso linked to death certificate data for infant deaths thatoccurred within 12 months of delivery.

    Subjects were selected from among all singleton live-born infants from 1987 through 1998 (n 17,825).Cases (n 3,565) consisted of all births with a diagnosisof a short umbilical cord (International Classification ofDiseases, Ninth Revision, Clinical Modification [ICD-9-CM] code 663.4).15 Controls (n 14,260) were ran-domly selected from among the remaining singleton

    births that occurred during the same years (frequencywas matched on the year of delivery) in a 4:1 ratio. The

    Human Subjects Protection Review Boards at the Uni-versity of Washington and the Washington State De-

    partment of Health approved this study.To evaluate potential risk factors that may be associ-

    ated with the development of a short umbilical cord, weselected characteristics that have been reported in previ-ous studies as well as several new characteristics. Thesecharacteristics included body mass index; smoking andalcohol intake during pregnancy; various maternal med-ical conditions; reproductive history, including parity,

    prior fetal loss, and previous preterm or small-for-gesta-tional-age (SGA) infant; prenatal procedures; various

    pregnancy complications; and fetal characteristics.We identified the presence of risk factors and congen-

    ital anomalies using birth certificates and hospital dis-charge data. A risk factor or congenital malformation wasconsidered present if either or both data sources indicateditspresence. Thefollowing risk factors were identified fromhospital discharge ICD-9-CM codes or birth certificates:anemia (280285), cardiac disease (429), diabetes mellitus(250), hypertension (401405), epilepsy (345), genital her-

    pes (054.1), oligohydramnios (761.2), hydramnios (761.3),incompetent cervix (761.0), placenta previa (762.0, 641.0,

    641.1), gestational diabetes (648.8), preeclampsia (642.4,642.5), and eclampsia (642.6). We classified congenitalmalformations into groups with similar characteristicsand used ICD-9-CM codes along with birth certificatesto identify the various congenital defects: any malforma-tions (740759), chromosomal (758), gastrointestinal(750751), circulatory/respiratory (745748), integu-ment (757), musculoskeletal (754756), genitourinary(752753), central nervous system (740742), and othermalformations (743,744,749,759). All remaining mater-

    nal characteristics and risk factors not listed above weretaken from birth certificates only.

    Maternal labor and delivery outcomes included mal-position (breech [652.2], transverse [652.3], other malpo-sition [652.0, 652.4, 652.5, 652.6, 652.7, 652.8, 652.9]),induced labor, stimulated labor, abruptio placenta(641.2), prolonged labor (662), prolonged second stage

    (662.2), third- and fourth-degree perineal lacerations(664.2, 664.3), retained placenta (667), postpartum hem-orrhage (666.0, 666.1), and delivery method (spontane-ous vaginal delivery, operative vaginal delivery, andcesarean section). Fetal and infant outcomes includedgestational age, SGA,16 birth weight, 5-minute Apgarscore, asphyxia (768.5, 768.6, 768.9), hypoxic-ischemicencephalopathy (348.1, 997.01, 767.0, 770.8), birth in-

    jury (767), fetal distress (656.3, 768.2, 768.3, 768.4),meconium aspiration (770.1), presence of moderate/heavy meconium, assisted ventilation, and infant death(within the first year of life).

    The associations between selected maternal character-istics, medical conditions, reproductive history, prenatal

    procedures, pregnancy complications, and fetal factorsand the presence of a short umbilical cord were esti-mated by using Mantel-Haenszel stratified analysis toobtain estimates of the odds ratio (OR) and test-based95% confidence intervals (CIs) using SAS 8.2 softwarefor Windows (SAS Institute, Cary, NC). To assess theassociation between short umbilical cord and adverselabor and delivery outcomes and to assess adverse fetaland infant outcome association with short umbilicalcord, we used Mantel-Haenszel estimates of the relative

    risk (RR) and 95% CIs. Delivery and fetal and infantoutcomes were restricted to cases and controls withoutcongenital malformations, because we wanted to exam-ine the impact of a short umbilical cord on labor anddelivery without including outcomes that may be relatedto congenital defects.

    We chose several variables a priori to be assessed aspotential confounders or effect modifiers, including ma-ternal age, payment method, the trimester when prenatalcare began, body mass index, parity, previous pregnancylosses, presence of malformations, sex of infant, gesta-tional age in weeks, and birth weight (in grams). The OR

    or RR was adjusted for a potential confounder(s) if theadjusted RR differed from the crude measure of risk by10% or more. All risk factors and outcomes were as-sessed on an individual basis. To evaluate effect modifi-cation, we applied the Breslow-Day test for homogene-ity17 to test for differences between all strata, usingP.05 to denote statistical significance.

    We examined birth outcomes for vaginal deliveriesalone to eliminate the possibility that short cords may bedifferentially reported during a cesarean delivery. We

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    also assessed outcomes in term deliveries by restrictingone analysis to those who delivered between 37 and 42weeks of gestation, because prematurity of the infant mayinfluence the outcomes of interest. For comparability, weadjusted variables for the same confounders that we de-tected in outcomes under unrestricted conditions. How-ever, if the RR did not differ by more than 10% from theadjusted risk estimatein a subanalysis, we reported only thecrude RR. Both subanalyses were also restricted to infants

    born without congenital malformations.

    RESULTS

    From 1987 to 1998, 3,565 cases of short umbilical cordwere reported among 901,775 live singleton births, giv-ing an overall incidence of 4 per 1,000 live births. Mater-nal characteristics of women with short cords were gen-erally similar to those that did not have short cords(Table 1). However, women with short cordinfantstended to be more educated and less likely to have usedMedicaid insurance.

    Mothers with short cordinfants were less likely to beoverweight (OR 0.7; 95% CI 0.6, 0.8; Table 2). Primip-arous women were at an elevated risk for having a shortcordinfant compared with those with 1 previous deliv-ery (OR 1.4; 95% CI 1.3, 1.6). Among women with a

    previous pregnancy, mothers of short cordinfants weresimilar to controls in their history of having a previousfetal loss or previous preterm infant. Although there wasno significant association with amniocentesis, womenwith short cordinfants were 20% less likely to have had

    ultrasound (OR 0.8; 95% CI 0.7, 0.9). Women withshort cordinfants did not differ from mothers of controlinfants regarding likelihood of pregnancy complications.Infants with short cords were more likely to be female(OR 1.3; 95% CI 1.2, 1.4) and to have a congenitalmalformation (OR 1.6; 95% CI 1.4, 1.8).

    After subdividing by major class of malformation, wefound that short cordinfants had at least twice the riskof having chromosomal (OR 5.3; 95% CI 3.2, 8.6),gastrointestinal (OR 2.8; 95% CI 1.6, 4.8), and circula-

    Table 1. Selected Characteristics of Mothers Delivering Infants With Short Umbilical Cords Compared With MothersDelivering Infants Without Short Umbilical Cords, Washington State, 19871998

    Short cord (N 3,565)* No short cord (N 14,260)*

    Mothers age (y)20 394 (11.1) 1579 (11.1)2024 901 (25.3) 3572 (25.1)2529 1120 (31.4) 4220 (29.6)3034 823 (23.1) 3284 (23.0)35 325 (9.1) 1597 (11.2)

    EducationLess than high school 318 (15.4) 1630 (19.7)High school 631 (30.5) 2722 (32.9)Some college 1120 (54.1) 3935 (47.5)

    Marital statusMarried 2654 (74.8) 10530 (74.0)Not married 896 (25.2) 3703 (26.0)

    Race/ethnicityWhite 2768 (80.6) 10797 (77.7)Asian/Pacific Islander 216 (6.3) 845 (6.1)Black 91 (2.7) 471 (3.4)Hispanic 303 (8.8) 1449 (10.4)Native American 55 (1.6) 325 (2.3)

    Other 0 (0.0) 5 (0.0)Payment method

    Medicaid 964 (27.0) 4661 (32.7)Health maintenance organization 562 (15.8) 2201 (15.4)Commercial insurance 1003 (28.1) 3572 (25.1)Self-pay/charity 209 (5.9) 774 (5.4)Other 827 (23.2) 3050 (21.4)

    Trimester in which prenatal care beganNone 19 (0.6) 107 (0.8)First 2752 (83.6) 10796 (81.0)Second 433 (13.2) 1985 (14.9)Third 87 (2.6) 442 (3.3)

    Values are presented asn(%).* Column figures may not add up to the total because of missing values.

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    tory/respiratory (OR 2.3; 95% CI 1.7, 3.1) malforma-tions (Table 3).

    Delivery and fetal and infant outcomes analysis wasrestricted to infants without congenital malformations(n 16,583) to prevent spurious associations with neg-ative outcomes due to malformations (Table 4). Basedon the Breslow-Day test of homogeneity, significant ef-fect modification was found for prolonged labor and

    prolonged second stage of labor, both of which werealtered by parity; the presence of postpartum hemor-rhage and hypoxic-ischemic encephalopathy both dif-fered by birth weight strata; fetal distress was modified

    by sex of the infant; and risk of infant death was found tobe contingent on weeks of gestation.

    Overall, short cordinfants were less likely to presentin breech (RR 0.6; 95% CI 0.5, 0.8) or transverse (RR

    Table 2. Selected Risk Factors and Characteristics Associated With the Presence of Short Umbilical Cords, Washington

    State, 19871998

    Short cord (N 3,565)* No short cord (N 14,260)* cOR 95% CI aOR 95% CI

    Maternal characteristics andbehaviors

    Body mass index18.5 91 (6.3) 282 (5.1) 1.1 0.9, 1.418.524.9 (ref) 975 (66.8) 3360 (61.1) 1.025.0 393 (26.9) 1860 (33.8) 0.7 0.6, 0.8

    Smoking 602 (18.0) 2464 (18.3) 1.0 0.9, 1.1Alcohol 78 (2.9) 310 (2.8) 1.0 0.8, 1.3

    Maternal medical conditionsAnemia 178 (5.0) 814 (5.7) 0.9 0.7, 1.0Cardiac disease 3 (0.1) 35 (0.3) 0.3 0.1, 1.1Diabetes mellitus 0 (0.0) 43 (0.3)Hypertension 20 (0.6) 122 (0.9) 0.7 0.4, 1.1Epilepsy 1 (0.0) 14 (0.1) 0.3 0.0, 2.2Genital herpes 88 (2.5) 385 (2.7) 0.9 0.7, 1.2

    Reproductive historyParity

    1 1911 (54.8) 5961 (42.6) 1.4 1.3, 1.62 (ref) 1014 (29.1) 4543 (32.4) 1.0

    3 565 (16.2) 3498 (25.0) 0.7 0.6, 0.8Among women with prior

    pregnanciesPrior fetal loss 627 (31.0) 3082 (32.2) 1.0 0.9, 1.1Previous preterm infant 31 (1.9) 195 (2.5) 0.8 0.5, 1.1

    Prenatal proceduresAmniocentesis

    Not done (ref) 3289 (96.5) 13063 (95.5) 1.0 1.0

    First or second trimester 82 (2.4) 457 (3.3) 0.7 0.6, 0.9 0.8 0.6, 1.0Third trimester 36 (1.1) 155 (1.1) 0.9 0.6, 1.3 1.0 0.7, 1.4

    Ultrasound 1560 (52.1) 6956 (57.9) 0.8 0.7, 0.9Pregnancy complications

    First-trimester bleeding 27 (0.9) 120 (1.0) 0.9 0.6, 1.4Oligohydramnios 46 (1.3) 130 (0.9) 1.4 1.0, 2.0

    Polyhydramnios 21 (0.6) 60 (0.4) 1.4 0.9, 2.3Incompetent cervix 3 (0.1) 25 (0.2) 0.5 0.1, 1.6Placenta previa 13 (0.4) 95 (0.7) 0.5 0.3, 1.0Gestational diabetes 29 (2.0) 154 (2.9) 0.7 0.5, 1.0 0.8 0.5, 1.1Preeclampsia 162 (4.5) 794 (5.6) 0.8 0.7, 1.0Eclampsia 3 (0.1) 57 (0.4) 0.3 0.1, 1.4 0.4 0.1, 1.5

    Fetal factorsFemale 1979 (55.5) 6956 (48.8) 1.3 1.2, 1.4Any malformation 340 (9.5) 902 (6.3) 1.6 1.4, 1.8

    cOR crude odds ratio; CI confidence intervals; aOR adjusted odds ratio; ref referent category.Values are presented asn(%).* Column figures may not add up to the total because of missing values. See text for explanation of variables for which adjustment was to be carried out.Adjusted for parity.Adjusted for body mass index.

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    0.4; 95% CI 0.2, 0.8) positions. Case women were alsoless likely to have induced labor (RR 0.8; 95% CI 0.7,0.9). Significantly higher risks of prolonged labor and

    prolonged second-stage labor were found among secun-diparous case women (RR 1.9; 95% CI 1.3, 2.7 and RR

    2.2; 95% CI 1.4, 3.6, respectively). Case women were60% more likely to experience retained placenta duringdelivery (95% CI 1.2, 2.3), and if they delivered a mac-rosomic infant, case mothers were twice as likely tosuffer postpartum hemorrhage (RR 2.4; 95% CI 1.4,4.0). Finally, women with short cordinfants were 40%more likely to have an assisted vaginal delivery (95% CI1.3, 1.5) than controls and 50% less likely to have acesarean delivery (95% CI 0.4, 0.5) even after adjustingfor parity.

    After adjustment for birth weight, infants with shortcords were similar to controls in gestational age distribu-

    tion. However, short cordinfants were more likely to beSGA (RR 1.6; 95% CI 1.4, 1.9), to have hypoxic-isch-emic encephalopathy (RR 1.4; 95% CI 1.2, 1.8), and tohave fetal distress (RR 1.8; 95% CI 1.6, 2.1). The risk ofhypoxic-ischemic encephalopathy was especially highamong infants weighing 2,5003,999 g compared withother birth weight categories (RR 1.7; 95% CI 1.3, 2.2).Finally, although the overall risk estimate was not signif-icant, term case infants had higher rates of infant death inthe first year of life (RR 2.4; 95% CI 1.2, 4.6).

    To exclude the possibility of underreported cases in acesarean delivery, we repeated our analysis shown in

    Table 4 for vaginal deliveries only (in addition to exam-ining only infants without any malformations); however,the changes in RRs comparably were not substantialenough to report separately. Similarly, to exclude deliv-ery and infant outcomes that were due to complicationsfrom having a preterm infant, we repeated the analysisshown in Table 4 for infants born between 37 and 42weeks of gestation. The majority of delivery and infantoutcomes was similar after this restriction except thatcase women were significantly more likely to have ab-

    ruptio placenta (RR 1.6; 95% CI 1.2, 2.3; results notshown in table).

    DISCUSSION

    In this population-based study, the incidence of shortumbilical cord was 4 cases per 1,000 live births, with nosignificant variation in incidence year to year in the11-year study period. We found no association with

    potentially modifiable risk factors, such as timing ofinitiation of prenatal care or chronic maternal medicalconditions, which have not been examined previously.However, we demonstrated that short umbilical cordsconferred a heightened risk of complications during la-

    bor and delivery to both mother and infant, some ofwhich have been reported in previous studies.1,7,9,11,13,18

    Notably, we found an increased risk of death among

    infants with a short cord, which was doubled amongterm infants without congenital malformations.

    Our findings confirm previous observations of theassociation of several factors with short umbilical cords.Seminal observations reported by Naeye1 and Mills10

    used data on more than 35,000 singleton pregnanciesfrom different areas within the United States participat-ing in the Collaborative Perinatal Study of the NationalInstitutes of Neurological and Communicative Disor-ders and Stroke. These studies demonstrated that femaleinfants have shorter cords than male infants, which isconsistent with our findings. Second, a positive correla-

    tion between umbilical cord length and parity has beenreported.9 By extension, we demonstrated that a diagno-sis of short cord was more common among primiparas.

    Third, socioeconomic status has been associated withcord length,1 and in the current study, we found differ-ences in insurance coverage and maternal education,suggesting minor disparities in socioeconomic status be-tween cases and controls. However, differences in insur-ance payer do not explain the magnitude of differences inthe use of ultrasound between cases and controls. Last,

    Table 3. Selected Congenital Malformations and Anomalies of Infants Diagnosed With a Short Umbilical Cord Compared

    With Infants Without a Short Umbilical Cord, Washington State, 19871998

    Short cord (N 3,565) No short cord (N 14,260) OR 95% CI

    Chromosomal 30 (0.8) 23 (0.2) 5.3 3.2, 8.6Gastrointestinal 21 (0.6) 30 (0.2) 2.8 1.6, 4.8Circulatory/respiratory 70 (2.0) 122 (0.9) 2.3 1.7, 3.1Integument 110 (3.1) 280 (2.0) 1.6 1.3, 2.0Musculoskeletal 76 (2.1) 202 (1.4) 1.5 1.2, 2.0Genitourinary 52 (1.5) 146 (1.0) 1.4 1.0, 2.0Central nervous system 6 (0.2) 26 (0.2) 0.9 0.4, 2.2Other malformations 28 (0.8) 69 (0.5) 1.6 1.1, 2.5

    OR crude odds ratio; CI confidence intervals.Values are presented atn(%).

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    Table 4. Delivery and Fetal and Infant Characteristics Associated With the Presence of a Short Umbilical Cord Among

    Infants Without Any Congenital Malformations, Washington State, 19871998

    OutcomesShort cord

    (N 3,225)*No short cord

    (N 13,358)* cRR 95% CI aRR 95% CI

    DeliveryMalposition

    Breech 72 (2.2) 490 (3.7) 0.6 0.5, 0.8Transverse 7 (0.2) 75 (0.6) 0.4 0.2, 0.8Other 87 (2.7) 328 (2.5) 1.1 0.9, 1.4No malposition (ref) 3059 (94.9) 12465 (93.3) 1.0

    Induced labor 396 (12.7) 2076 (16.0) 0.8 0.7, 0.9Stimulated labor 490 (15.9) 1860 (14.5) 1.1 1.0, 1.2

    Abruptio placenta 59 (1.8) 177 (1.3) 1.4 1.0, 1.8Prolonged labor (EM) 198 (6.3) 682 (5.2) 1.2 1.0, 1.4 1.0 0.9, 1.2

    Primiparas 150 (8.7) 522 (9.4) 0.9 0.8, 1.1Secundiparas 38 (4.1) 95 (2.2) 1.9 1.3, 2.7Multiparas 10 (2.0) 65 (2.0) 1.0 0.5, 1.9

    Prolonged 2nd stage (EM) 118 (3.7) 354 (2.7) 1.4 1.1, 1.7 1.2 0.9, 1.4Primiparas 93 (5.4) 289 (5.2) 1.0 0.8, 1.3Secundiparas 23 (2.5) 48 (1.1) 2.2 1.4, 3.6Multiparas 2 (0.4) 17 (0.5) 0.8 0.2, 3.3

    Third/fourth degree lacerations 293 (9.3) 878 (6.7) 1.4 1.2, 1.6 1.0 0.9, 1.1Retained placenta 43 (1.3) 109 (0.8) 1.6 1.2, 2.3Postpartum hemorrhage (g, EM) 100 (3.1) 419 (3.1) 1.0 0.8, 1.21500 0 (0.0) 0 (0.0)15002499 3 (1.6) 13 (3.0) 0.5 0.1, 1.825003999 81 (2.9) 336 (3.1) 0.9 0.7, 1.24000 16 (9.0) 70 (3.8) 2.4 1.4, 4.0

    Delivery methodSpontaneous vaginal (ref) 2107 (66.8) 8722 (66.5) 1.0 1.0

    Operative vaginal 799 (25.4) 1871 (14.3) 1.6 1.4, 1.7 1.4 1.3, 1.5Cesarean delivery 247 (7.8) 2524 (19.2) 0.5 0.4, 0.5 0.4 0.4, 0.5

    Fetal and infantGestational age (wk)

    1832 17 (0.6) 86 (0.7) 0.8 0.5, 1.4 1.0 0.6, 1.53336 132 (4.2) 403 (3.1) 1.4 1.1, 1.7 1.0 0.8, 1.23742 (ref) 2913 (93.9) 12324 (94.8) 1.0 1.0

    4345 41 (1.3) 185 (1.4) 0.9 0.7, 1.3 0.9 0.7, 1.3Size for gestational age

    Small 279 (9.6) 673 (5.4) 1.6 1.4, 1.9Average (ref) 2484 (85.1) 10297 (82.3) 1.0Large 157 (5.4) 1533 (12.3) 0.5 0.4, 0.5

    Birth weight (g)1500 8 (0.3) 71 (0.5) 0.4 0.2, 0.9 0.9 0.6, 1.515002499 191 (6.2) 419 (3.2) 1.7 1.5, 2.0 1.5 1.3, 1.825003999 (ref) 2732 (88.0) 10694 (82.3) 1.0 1.04000 172 (5.5) 1814 (14.0) 0.4 0.4, 0.5 0.4 0.4, 0.5

    5-minute Apgar 54 (1.7) 180 (1.4) 1.2 0.9, 1.7Asphyxia 76 (2.4) 262 (2.0) 1.2 0.9, 1.5Hypoxic-ischemic encephalopathy (EM) 109 (3.4) 318 (2.4) 1.4 1.2, 1.81500 5 (50.0) 30 (38.5) 1.3 0.7, 2.615002499 18 (9.3) 61 (14.2) 0.7 0.4, 1.125003999 83 (2.9) 186 (1.7) 1.7 1.3, 2.24000 3 (1.7) 39 (2.1) 0.8 0.3, 2.6

    Birth injury 229 (7.3) 640 (4.9) 1.5 1.3, 1.7 1.2 1.0, 1.3Fetal distress (EM) 330 (10.2) 753 (5.6) 1.8 1.6, 2.1

    Male 195 (13.7) 427 (6.3) 2.2 1.9, 2.6Female 135 (7.5) 326 (5.0) 1.5 1.2, 1.8

    Meconium aspiration 21 (0.7) 69 (0.5) 1.3 0.8, 2.1Meconium moderate/heavy 137 (5.2) 659 (6.0) 0.9 0.7, 1.0

    Assisted ventilation 60 (2.3) 247 (2.3) 1.0 0.8, 1.3Infant death (wk, EM) 15 (0.5) 46 (0.4) 1.4 0.8, 2.4 1.7 1.0, 2.9

    2432 0 (0.0) 21 (24.4)3336 1 (0.8) 2 (0.5) 1.5 0.1, 16.7 1.3 0.1, 13.63742 14 (0.5) 22 (0.2) 2.7 1.4, 5.3 2.4 1.2, 4.64345 0 (0.0) 1 (0.5)

    cRR crude risk ratio; CI confidence intervals; aRR adjusted risk ratio; ref referent category; EM effect modification.Values are presented asn(%).* Column figures may not add up to the total because of missing values. See text for explanation of variables for which adjustment was to be carried out.Adjusted for parity.Adjusted for parity and assisted delivery.Adjusted for birth weight.Adjusted for gestational age.

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    in common with a previous study,1 we found no associ-ation of short umbilical cords with maternal smoking oralcohol intake.

    Several studies2,3,12 have implicated a relationship be-tween the presence of oligohydramnios during preg-nancy and the subsequent development of a short um-

    bilical cord. Miller et al2,3 hypothesized that the umbilical

    cord grows in response to tensile forces exerted on thecord by fetal movements. Moessinger et al12 showed thatin the presence of oligohydramnios, the umbilical cordsof rat fetuses were 65% of control length. We did notdetect an association between oligohydramnios or hy-dramnios and a greater or lesser likelihood of being acase, respectively. Likewise, more recent studies4,5 usinganimal models have argued against the stretch hypoth-esis, stating that the umbilical cord continues to growthroughout pregnancy in an almost linear fashion. In-stead, these studies have proposed a multifactorial expla-nation for the occurrence of short cords.

    Indeed, in this study, no single factor accounted forthe occurrence of all short cords, suggesting a multifac-torial etiology. Surprisingly, fewer than 10% of caseinfants were reported as having congenital anomalies.Our data suggest an association of short cords with

    particular malformation sequences, particularly thosecaused by chromosomal anomalies. Other importantsequences may be those affecting gastrointestinal andcirculatory-respiratory systems. Previous studies of theassociation of short cords with malformation sequencesand fetal problems have defined several groups of suchsequences and problems among infants including still-

    borns and those who died shortly after birth due tomultiple severe anomalies. These include ADAM se-quence, cyllosomus/pleurosomus, acephalus-acardia,

    presumed primary defect of the umbilical cord and ab-dominal wall formation, schisis association, and reducedfetal movement.3,19 Such anomalies are usually multisys-tem disorders, although they principally involve thecentral nervous system, limbs, and cardiovascular sys-tem or are associated with defects in the formation of theanterior abdominal wall. Of interest, in our study, mal-formations of the central nervous system were not asso-ciated with the occurrence of short cords, and the asso-

    ciation of musculoskeletal malformations was modest.Such associations, if present, would have supported thestretch hypothesis for the lengthening of the cord andindeed formed the basis of some previous arguments2,3

    in favor of the stretch hypothesis. Miller et al3 statedthat extremes of decreased fetal movement occur in casesof amelia, acardia, arthrogryposis, and atrophy of spinalmuscles. Moessinger et al12 suppressed fetal movement

    by curarization, which led to the development of shortercords among rat fetuses. By extension, severe central

    nervous system malformations also would reduce fetalactivity.

    Our findings of increased risk of prolonged second-stage1 and operative vaginal delivery13 is consistent with

    previous studies. However, our findings of increased riskof retained placenta and postpartum hemorrhage amongwomen with short umbilical cords have not been previ-

    ously reported. Finally, we found increased likelihood ofimportant fetal and infant outcomes, including beingSGA, having hypoxic-ischemic encephalopathy, fetaldistress, and infant death, among case infants thancontrols. Our most striking finding was the 2-foldincrease in risk of death among term infants born withshort cords. Clausson et al20 reported a 3-fold increasein infant deaths among term SGA infants withoutcongenital malformations in a population-based studyof 510,029 singleton term and postterm births re-corded in the Swedish Birth Registry, but they did notspecifically examine cord length. In addition, our find-

    ings are consistent with previous studies, which re-ported low birth weight7 and fetal distress13,18 amonginfants with short cords.

    The major limitation of this study is the potential formisclassification of case status, because we identifiedcases by ICD-9-CM codes, whereas previous studiesadopted an absolute cord length as a case defini-tion.1,7,8,18,19 Underreporting of short umbilical cordcases would be present if neonates with umbilical cordsclose to the normal length were noted with a lowerfrequency. In this instance, we would expect the riskestimates to be closer to the null. Nonetheless, differen-tial misclassification can also be present if newborns withshort cords were noted as having a short cord morereadily in the presence of other adverse outcomes. Ourfindings did confirm previous reports regarding shortumbilical cords, such as low socioeconomic status andfetal distress,13,18 suggesting that differential misclassifi-cation was minimal. We restricted all outcome analysesand subanalyses to newborns without malformationsunder the assumption that, in the presence of any mal-formation, the short umbilical cord may be missed. Inaddition, we attempted to assess potential misclassifica-

    tion of the short cord in cesarean deliveries by examiningoutcomes in vaginal deliveries only but found no differ-ences in the outcomes. Finally, gestational age or the

    presence of congenital anomalies could potentially leadto differential recognition of cord anomalies, resulting indifferential misclassification of case status. We addressedthe concern by restricting delivery and fetal and infantoutcome analyses to infants without recognized malfor-mations. The potential effect of misclassification by ges-tational age also is unlikely to have had a significant

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    impact on the associations we report as 94% of caseswere term deliveries.

    Although reference standards for cord length havebeen reported,10 variation exists in the definition of shortcord.1,7,8,18,19 Naeye1 adopted a cord length of 40 cm,whereas Nnatu et al8 used a measurement of less than 46cm. Other studies7,18,19 defined short cords as less than

    or equal to 35 cm in length. Their reported prevalence ofshort cords ranged from 2%7 to 6%1,18 to 10%,8 contrast-ing with our incidence of 0.4%. However, most of the

    previous studies were not population based;7,8,18,19 hadrestrictive exclusion criteria, including gestation less than37 weeks, malposition, and cases of umbilical cord trau-mas;1,7,18 or examined a high-risk population,8 whichmay account for our lower incidence of short cord. Inaddition, the prevalence of short umbilical cords wasconsistent between years 1987 and 1998 in the State of

    Washington.Although we were able use both birth certificate and

    hospital discharge data for the majority of risk factorsand outcomes, giving us greater likelihood of identifyingthese factors, some factors were only provided in the

    birth certificate data. Underreporting or failure to recordrisk factors, such as smoking and alcohol intake, is

    possible, and bias may have been introduced if casemothers reported these risk factors with a differing accu-racy compared with control mothers. As such, we wouldexpect our findings to result in a null risk estimate.

    Despite these limitations, our study has severalstrengths. We identified a large number of cases, lendinggreater precision and power to our analyses than had been

    possible with previous studies. Selection bias was unlikelybecause we included all identified cases and a large sampleof randomly selected controls. The availability of linkeddata enabled us to more accurately identify variables thanthrough use of either of the data sources alone. In addition,the definitions and classifications of risk factors and out-comes remained consistent between 1987 and 1998 be-cause the ICD-9 codes and birth certificate standardizeddefinitions had not changed.

    In summary, we demonstrated that case infants hadgreater odds of having certain organ or chromosomalmalformations, which suggest that there may be a spe-

    cific sequence association. Although we did not identifyany modifiable risks that would predispose infants to thedevelopment of a short cord, several previously unre-

    ported complications of labor and delivery in both moth-ers and infants were identified. Because antenatal andintrapartum screening or diagnoses for short cords donot exist at present, preventive measures are unavail-able. Most importantly, we recognized a 2-fold increasein infant death among term cases, which suggests closermonitoring of infants born with a short cord after birth.

    Moreover, the presence of a short cord at delivery mayindicate an important surveillance marker for infants inthe first year of life. However, the relationship betweenshort cords and first year of life mortality among terminfants should be further addressed in future studies.

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    Address reprint requests to: Mona T. Lydon-Rochelle, PhD,

    MPH, CNM, University of Washington, Box 357262, Seattle,Washington 981957762; Phone: (206) 221 6576, Fax: (206)5436656, e-mail: [email protected].

    Received May 23, 2003. Received in revised form September 17, 2003.

    Accepted September 26, 2003.

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