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Risk Factors and Outcomes Associated With a Short

Umbilical Cord
Paula Krakowiak, MS, Erin N. Smith, BS, Guy de Bruyn, MBBCH, and
Mona T. Lydon-Rochelle, PhD, MPH
OBJECTIVE: To identify risk factors and outcomes associated with a short umbilical cord.

2004;103:119 127. 2004 by The American College of


Obstetricians and Gynecologists.)

METHODS: We conducted a population-based case-control study using linked Washington State birth certificate
hospital discharge data for singleton live births from 1987 to
1998 to assess the association between maternal, pregnancy,
delivery, and infant characteristics and short umbilical
cord. Cases (n 3,565) were infants diagnosed with a short
umbilical cord. Controls (n 14,260) were randomly selected
from among births without a diagnosis of short umbilical
cord.

LEVEL OF EVIDENCE: II-2

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 be
primiparous (OR 1.4; 95% CI 1.3, 1.6). Case infants were
more likely to be female (OR 1.3; 95% CI 1.2, 1.4), have a
congenital malformation (OR 1.6; 95% CI 1.4, 1.8), and be
small for their gestational age (risk ratio [RR] 1.6; 95% CI
1.4, 1.9). A short cord was associated with increased risk for
maternal labor and delivery complications, including retained placenta (RR 1.6; 95% CI 1.2, 2.3) and operative
vaginal delivery (RR 1.4; 95% CI 1.3, 1.5). Adverse fetal
and infant outcomes in cases included fetal distress (RR
1.8; 95% CI 1.6, 2.1) and death within the first year of life
among term infants (RR 2.4; 95% CI 1.2, 4.6).
CONCLUSION: Modifiable risk factors associated with the
development of a short cord were not identified. Case
mothers and infants are more likely to experience labor and delivery complications. Term case infants had a
2-fold increased risk of death, which suggests closer postpartum monitoring of these infants. (Obstet Gynecol
From the Department of Epidemiology, School of Public Health and Community
Medicine, Molecular and Cellular Biology Program, Division of Allergy and
Infectious Diseases, School of Medicine, Department of Family and Child Nursing,
School of Nursing, and Department of Health Services, School of Public Health
and Community Medicine, University of Washington, Seattle, Washington; and
Divisions of Human Biology and Clinical Research and Program in Infectious
Diseases, 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 2004
2004 by The American College of Obstetricians and Gynecologists.
Published by Lippincott Williams & Wilkins.

Short umbilical cords occur in approximately 6% of


pregnancies.1 The presence of a short umbilical cord has
been associated with antepartum abnormalities and risk
factors for complications of labor and delivery. Few
studies have investigated both risk factors and outcomes
associated with this relatively rare condition. A short
umbilical cord has been associated with various intrauterine conditions and exposures that may impact in
utero development and activity of the fetus, including
oligohydramnios, amnion rupture, and uterine structural anomalies,2,3 as well as substances such as alcohol
and -blockers.4 6 The pathogenesis of short umbilical
cords remains unclear. One prominent hypothesis to
explain the ontogeny of the umbilical cord is the stretch
hypothesis, which attributes the development of a short
umbilical cord to intrauterine constraint.2 4 Previous
studies contain conflicting results on the relationship of
exposures, such as parity79 and sex of the fetus,1,10 12 to
short umbilical cords. Similarly, previous studies report
inconsistent associations between outcomes, such as neonatal resuscitation and short umbilical cords.1,13 However, past studies have consistently reported selected
labor and delivery complications associated with the
presence of short cords, including abruptio placenta,
prolonged labor,1, and fetal distress.7,13 Therefore, an
assessment of exposures is important and would provide
new information about the possible etiology of short
umbilical cords and its association with adverse neonatal
outcomes.
We used maternally linked birth records to determine risk factors for a short umbilical cord, to examine
the risk of selected labor and delivery outcomes attributable to short umbilical cords, and to identify the risk of
selected fetal and infant outcomes attributable to short
umbilical cords among women delivering singleton live
births.

0029-7844/04/$30.00
doi:10.1097/01.AOG.0000102706.84063.C7

119

MATERIALS AND METHODS


We conducted a population-based retrospective study
using data obtained from the Washington State Birth
Events Records Database. This database links more than
95% of birth certificate records to maternal and infant
hospital discharge records for deliveries that occur in all
nonfederal hospitals in Washington.14 Birth records are
also linked to death certificate data for infant deaths that
occurred within 12 months of delivery.
Subjects were selected from among all singleton liveborn infants from 1987 through 1998 (n 17,825).
Cases (n 3,565) consisted of all births with a diagnosis
of a short umbilical cord (International Classification of
Diseases, Ninth Revision, Clinical Modification [ICD-9CM] code 663.4).15 Controls (n 14,260) were randomly selected from among the remaining singleton
births that occurred during the same years (frequency
was matched on the year of delivery) in a 4:1 ratio. The
Human Subjects Protection Review Boards at the University of Washington and the Washington State Department of Health approved this study.
To evaluate potential risk factors that may be associated with the development of a short umbilical cord, we
selected characteristics that have been reported in previous studies as well as several new characteristics. These
characteristics included body mass index; smoking and
alcohol intake during pregnancy; various maternal medical conditions; reproductive history, including parity,
prior fetal loss, and previous preterm or small-for-gestational-age (SGA) infant; prenatal procedures; various
pregnancy complications; and fetal characteristics.
We identified the presence of risk factors and congenital anomalies using birth certificates and hospital discharge data. A risk factor or congenital malformation was
considered present if either or both data sources indicated
its presence. The following risk factors were identified from
hospital discharge ICD-9-CM codes or birth certificates:
anemia (280 285), cardiac disease (429), diabetes mellitus
(250), hypertension (401 405), epilepsy (345), genital herpes (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 congenital
malformations into groups with similar characteristics
and used ICD-9-CM codes along with birth certificates
to identify the various congenital defects: any malformations (740 759), chromosomal (758), gastrointestinal
(750 751), circulatory/respiratory (745748), integument (757), musculoskeletal (754 756), genitourinary
(752753), central nervous system (740 742), and other
malformations (743,744,749,759). All remaining mater-

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Krakowiak et al

Short Umbilical Cords

nal characteristics and risk factors not listed above were


taken from birth certificates only.
Maternal labor and delivery outcomes included malposition (breech [652.2], transverse [652.3], other malposition [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 hemorrhage (666.0, 666.1), and delivery method (spontaneous vaginal delivery, operative vaginal delivery, and
cesarean section). Fetal and infant outcomes included
gestational age, SGA,16 birth weight, 5-minute Apgar
score, asphyxia (768.5, 768.6, 768.9), hypoxic-ischemic
encephalopathy (348.1, 997.01, 767.0, 770.8), birth injury (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 characteristics, medical conditions, reproductive history, prenatal
procedures, pregnancy complications, and fetal factors
and the presence of a short umbilical cord were estimated by using Mantel-Haenszel stratified analysis to
obtain estimates of the odds ratio (OR) and test-based
95% confidence intervals (CIs) using SAS 8.2 software
for Windows (SAS Institute, Cary, NC). To assess the
association between short umbilical cord and adverse
labor and delivery outcomes and to assess adverse fetal
and infant outcome association with short umbilical
cord, we used Mantel-Haenszel estimates of the relative
risk (RR) and 95% CIs. Delivery and fetal and infant
outcomes were restricted to cases and controls without
congenital malformations, because we wanted to examine the impact of a short umbilical cord on labor and
delivery without including outcomes that may be related
to congenital defects.
We chose several variables a priori to be assessed as
potential confounders or effect modifiers, including maternal age, payment method, the trimester when prenatal
care began, body mass index, parity, previous pregnancy
losses, presence of malformations, sex of infant, gestational age in weeks, and birth weight (in grams). The OR
or RR was adjusted for a potential confounder(s) if the
adjusted RR differed from the crude measure of risk by
10% or more. All risk factors and outcomes were assessed on an individual basis. To evaluate effect modification, we applied the Breslow-Day test for homogeneity17 to test for differences between all strata, using P
.05 to denote statistical significance.
We examined birth outcomes for vaginal deliveries
alone to eliminate the possibility that short cords may be
differentially reported during a cesarean delivery. We

OBSTETRICS & GYNECOLOGY

Table 1. Selected Characteristics of Mothers Delivering Infants With Short Umbilical Cords Compared With Mothers
Delivering Infants Without Short Umbilical Cords, Washington State, 19871998
Short cord (N 3,565)*

No short cord (N 14,260)*

394 (11.1)
901 (25.3)
1120 (31.4)
823 (23.1)
325 (9.1)

1579 (11.1)
3572 (25.1)
4220 (29.6)
3284 (23.0)
1597 (11.2)

318 (15.4)
631 (30.5)
1120 (54.1)

1630 (19.7)
2722 (32.9)
3935 (47.5)

2654 (74.8)
896 (25.2)

10530 (74.0)
3703 (26.0)

2768 (80.6)
216 (6.3)
91 (2.7)
303 (8.8)
55 (1.6)
0 (0.0)

10797 (77.7)
845 (6.1)
471 (3.4)
1449 (10.4)
325 (2.3)
5 (0.0)

964 (27.0)
562 (15.8)
1003 (28.1)
209 (5.9)
827 (23.2)

4661 (32.7)
2201 (15.4)
3572 (25.1)
774 (5.4)
3050 (21.4)

19 (0.6)
2752 (83.6)
433 (13.2)
87 (2.6)

107 (0.8)
10796 (81.0)
1985 (14.9)
442 (3.3)

Mothers age (y)


20
2024
2529
3034
35
Education
Less than high school
High school
Some college
Marital status
Married
Not married
Race/ethnicity
White
Asian/Pacific Islander
Black
Hispanic
Native American
Other
Payment method
Medicaid
Health maintenance organization
Commercial insurance
Self-pay/charity
Other
Trimester in which prenatal care began
None
First
Second
Third

Values are presented as n (%).


* Column figures may not add up to the total because of missing values.

also assessed outcomes in term deliveries by restricting


one analysis to those who delivered between 37 and 42
weeks of gestation, because prematurity of the infant may
influence the outcomes of interest. For comparability, we
adjusted variables for the same confounders that we detected in outcomes under unrestricted conditions. However, if the RR did not differ by more than 10% from the
adjusted risk estimate in a subanalysis, we reported only the
crude RR. Both subanalyses were also restricted to infants
born without congenital malformations.
RESULTS
From 1987 to 1998, 3,565 cases of short umbilical cord
were reported among 901,775 live singleton births, giving an overall incidence of 4 per 1,000 live births. Maternal characteristics of women with short cords were generally similar to those that did not have short cords
(Table 1). However, women with short cordinfants
tended to be more educated and less likely to have used
Medicaid insurance.

VOL. 103, NO. 1, JANUARY 2004

Mothers with short cordinfants were less likely to be


overweight (OR 0.7; 95% CI 0.6, 0.8; Table 2). Primiparous women were at an elevated risk for having a short
cordinfant compared with those with 1 previous delivery (OR 1.4; 95% CI 1.3, 1.6). Among women with a
previous pregnancy, mothers of short cordinfants were
similar to controls in their history of having a previous
fetal loss or previous preterm infant. Although there was
no significant association with amniocentesis, women
with short cordinfants were 20% less likely to have had
ultrasound (OR 0.8; 95% CI 0.7, 0.9). Women with
short cordinfants did not differ from mothers of control
infants 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 congenital
malformation (OR 1.6; 95% CI 1.4, 1.8).
After subdividing by major class of malformation, we
found that short cordinfants had at least twice the risk
of having chromosomal (OR 5.3; 95% CI 3.2, 8.6),
gastrointestinal (OR 2.8; 95% CI 1.6, 4.8), and circula-

Krakowiak et al

Short Umbilical Cords

121

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 and
behaviors
Body mass index
18.5
18.524.9 (ref)
25.0
Smoking
Alcohol
Maternal medical conditions
Anemia
Cardiac disease
Diabetes mellitus
Hypertension
Epilepsy
Genital herpes
Reproductive history
Parity
1
2 (ref)
3
Among women with prior
pregnancies
Prior fetal loss
Previous preterm infant
Prenatal procedures
Amniocentesis
Not done (ref)
First or second trimester
Third trimester
Ultrasound
Pregnancy complications
First-trimester bleeding
Oligohydramnios
Polyhydramnios
Incompetent cervix
Placenta previa
Gestational diabetes
Preeclampsia
Eclampsia
Fetal factors
Female
Any malformation

91 (6.3)
975 (66.8)
393 (26.9)
602 (18.0)
78 (2.9)

282 (5.1)
3360 (61.1)
1860 (33.8)
2464 (18.3)
310 (2.8)

1.1
1.0
0.7
1.0
1.0

0.9, 1.4

178 (5.0)
3 (0.1)
0 (0.0)
20 (0.6)
1 (0.0)
88 (2.5)

814 (5.7)
35 (0.3)
43 (0.3)
122 (0.9)
14 (0.1)
385 (2.7)

0.9
0.3

0.7, 1.0
0.1, 1.1

0.7
0.3
0.9

0.4, 1.1
0.0, 2.2
0.7, 1.2

1911 (54.8)
1014 (29.1)
565 (16.2)

5961 (42.6)
4543 (32.4)
3498 (25.0)

1.4
1.0
0.7

1.3, 1.6

627 (31.0)
31 (1.9)

3082 (32.2)
195 (2.5)

1.0
0.8

0.9, 1.1
0.5, 1.1

3289 (96.5)
82 (2.4)
36 (1.1)
1560 (52.1)

13063 (95.5)
457 (3.3)
155 (1.1)
6956 (57.9)

1.0
0.7
0.9
0.8

0.6, 0.9
0.6, 1.3
0.7, 0.9

27 (0.9)
46 (1.3)
21 (0.6)
3 (0.1)
13 (0.4)
29 (2.0)
162 (4.5)
3 (0.1)

120 (1.0)
130 (0.9)
60 (0.4)
25 (0.2)
95 (0.7)
154 (2.9)
794 (5.6)
57 (0.4)

0.9
1.4
1.4
0.5
0.5
0.7
0.8
0.3

0.6, 1.4
1.0, 2.0
0.9, 2.3
0.1, 1.6
0.3, 1.0
0.5, 1.0
0.7, 1.0
0.1, 1.4

1979 (55.5)
340 (9.5)

6956 (48.8)
902 (6.3)

1.3
1.6

1.2, 1.4
1.4, 1.8

0.6, 0.8
0.9, 1.1
0.8, 1.3

0.6, 0.8

1.0
0.8
1.0

0.6, 1.0
0.7, 1.4

0.8

0.5, 1.1

0.4

0.1, 1.5

cOR crude odds ratio; CI confidence intervals; aOR adjusted odds ratio; ref referent category.
Values are presented as n (%).
* 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.

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


Delivery and fetal and infant outcomes analysis was
restricted to infants without congenital malformations
(n 16,583) to prevent spurious associations with negative outcomes due to malformations (Table 4). Based
on the Breslow-Day test of homogeneity, significant effect modification was found for prolonged labor and

122

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Short Umbilical Cords

prolonged second stage of labor, both of which were


altered by parity; the presence of postpartum hemorrhage and hypoxic-ischemic encephalopathy both differed by birth weight strata; fetal distress was modified
by sex of the infant; and risk of infant death was found to
be contingent on weeks of gestation.
Overall, short cordinfants were less likely to present
in breech (RR 0.6; 95% CI 0.5, 0.8) or transverse (RR

OBSTETRICS & GYNECOLOGY

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
Chromosomal
Gastrointestinal
Circulatory/respiratory
Integument
Musculoskeletal
Genitourinary
Central nervous system
Other malformations

Short cord (N 3,565)

No short cord (N 14,260)

OR

95% CI

30 (0.8)
21 (0.6)
70 (2.0)
110 (3.1)
76 (2.1)
52 (1.5)
6 (0.2)
28 (0.8)

23 (0.2)
30 (0.2)
122 (0.9)
280 (2.0)
202 (1.4)
146 (1.0)
26 (0.2)
69 (0.5)

5.3
2.8
2.3
1.6
1.5
1.4
0.9
1.6

3.2, 8.6
1.6, 4.8
1.7, 3.1
1.3, 2.0
1.2, 2.0
1.0, 2.0
0.4, 2.2
1.1, 2.5

OR crude odds ratio; CI confidence intervals.


Values are presented at n (%).

0.4; 95% CI 0.2, 0.8) positions. Case women were also


less 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 secundiparous case women (RR 1.9; 95% CI 1.3, 2.7 and RR
2.2; 95% CI 1.4, 3.6, respectively). Case women were
60% more likely to experience retained placenta during
delivery (95% CI 1.2, 2.3), and if they delivered a macrosomic infant, case mothers were twice as likely to
suffer 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% CI
1.3, 1.5) than controls and 50% less likely to have a
cesarean delivery (95% CI 0.4, 0.5) even after adjusting
for parity.
After adjustment for birth weight, infants with short
cords were similar to controls in gestational age distribution. However, short cordinfants were more likely to be
SGA (RR 1.6; 95% CI 1.4, 1.9), to have hypoxic-ischemic encephalopathy (RR 1.4; 95% CI 1.2, 1.8), and to
have fetal distress (RR 1.8; 95% CI 1.6, 2.1). The risk of
hypoxic-ischemic encephalopathy was especially high
among infants weighing 2,500 3,999 g compared with
other birth weight categories (RR 1.7; 95% CI 1.3, 2.2).
Finally, although the overall risk estimate was not significant, term case infants had higher rates of infant death in
the first year of life (RR 2.4; 95% CI 1.2, 4.6).
To exclude the possibility of underreported cases in a
cesarean delivery, we repeated our analysis shown in
Table 4 for vaginal deliveries only (in addition to examining only infants without any malformations); however,
the changes in RRs comparably were not substantial
enough to report separately. Similarly, to exclude delivery and infant outcomes that were due to complications
from having a preterm infant, we repeated the analysis
shown in Table 4 for infants born between 37 and 42
weeks of gestation. The majority of delivery and infant
outcomes was similar after this restriction except that
case women were significantly more likely to have ab-

VOL. 103, NO. 1, JANUARY 2004

ruptio placenta (RR 1.6; 95% CI 1.2, 2.3; results not


shown in table).
DISCUSSION
In this population-based study, the incidence of short
umbilical cord was 4 cases per 1,000 live births, with no
significant variation in incidence year to year in the
11-year study period. We found no association with
potentially modifiable risk factors, such as timing of
initiation of prenatal care or chronic maternal medical
conditions, which have not been examined previously.
However, we demonstrated that short umbilical cords
conferred a heightened risk of complications during labor and delivery to both mother and infant, some of
which 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 among
term infants without congenital malformations.
Our findings confirm previous observations of the
association of several factors with short umbilical cords.
Seminal observations reported by Naeye1 and Mills10
used data on more than 35,000 singleton pregnancies
from different areas within the United States participating in the Collaborative Perinatal Study of the National
Institutes of Neurological and Communicative Disorders and Stroke. These studies demonstrated that female
infants have shorter cords than male infants, which is
consistent with our findings. Second, a positive correlation between umbilical cord length and parity has been
reported.9 By extension, we demonstrated that a diagnosis of short cord was more common among primiparas.
Third, socioeconomic status has been associated with
cord length,1 and in the current study, we found differences in insurance coverage and maternal education,
suggesting minor disparities in socioeconomic status between cases and controls. However, differences in insurance payer do not explain the magnitude of differences in
the use of ultrasound between cases and controls. Last,

Krakowiak et al

Short Umbilical Cords

123

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
Outcomes
Delivery
Malposition
Breech
Transverse
Other
No malposition (ref)
Induced labor
Stimulated labor
Abruptio placenta
Prolonged labor (EM)
Primiparas
Secundiparas
Multiparas
Prolonged 2nd stage (EM)
Primiparas
Secundiparas
Multiparas
Third/fourth degree lacerations
Retained placenta
Postpartum hemorrhage (g, EM)
1500
15002499
25003999
4000
Delivery method
Spontaneous vaginal (ref)
Operative vaginal
Cesarean delivery
Fetal and infant
Gestational age (wk)
1832
3336
3742 (ref)
4345
Size for gestational age
Small
Average (ref)
Large
Birth weight (g)
1500
15002499
25003999 (ref)
4000
5-minute Apgar
Asphyxia
Hypoxic-ischemic encephalopathy (EM)
1500
15002499
25003999
4000
Birth injury
Fetal distress (EM)
Male
Female
Meconium aspiration
Meconium moderate/heavy
Assisted ventilation
Infant death (wk, EM)
2432
3336
3742
4345

Short cord
(N 3,225)*

No short cord
(N 13,358)*

72 (2.2)
7 (0.2)
87 (2.7)
3059 (94.9)
396 (12.7)
490 (15.9)
59 (1.8)
198 (6.3)
150 (8.7)
38 (4.1)
10 (2.0)
118 (3.7)
93 (5.4)
23 (2.5)
2 (0.4)
293 (9.3)
43 (1.3)
100 (3.1)
0 (0.0)
3 (1.6)
81 (2.9)
16 (9.0)

cRR

95% CI

490 (3.7)
75 (0.6)
328 (2.5)
12465 (93.3)
2076 (16.0)
1860 (14.5)
177 (1.3)
682 (5.2)
522 (9.4)
95 (2.2)
65 (2.0)
354 (2.7)
289 (5.2)
48 (1.1)
17 (0.5)
878 (6.7)
109 (0.8)
419 (3.1)
0 (0.0)
13 (3.0)
336 (3.1)
70 (3.8)

0.6
0.4
1.1
1.0
0.8
1.1
1.4
1.2
0.9
1.9
1.0
1.4
1.0
2.2
0.8
1.4
1.6
1.0

0.5, 0.8
0.2, 0.8
0.9, 1.4
0.7, 0.9
1.0, 1.2
1.0, 1.8
1.0, 1.4
0.8, 1.1
1.3, 2.7
0.5, 1.9
1.1, 1.7
0.8, 1.3
1.4, 3.6
0.2, 3.3
1.2, 1.6
1.2, 2.3
0.8, 1.2

0.5
0.9
2.4

0.1, 1.8
0.7, 1.2
1.4, 4.0

2107 (66.8)
799 (25.4)
247 (7.8)

8722 (66.5)
1871 (14.3)
2524 (19.2)

1.0
1.6
0.5

1.4, 1.7
0.4, 0.5

17 (0.6)
132 (4.2)
2913 (93.9)
41 (1.3)

86 (0.7)
403 (3.1)
12324 (94.8)
185 (1.4)

0.8
1.4
1.0
0.9

0.5, 1.4
1.1, 1.7

279 (9.6)
2484 (85.1)
157 (5.4)

673 (5.4)
10297 (82.3)
1533 (12.3)

1.6
1.0
0.5

1.4, 1.9

8 (0.3)
191 (6.2)
2732 (88.0)
172 (5.5)
54 (1.7)
76 (2.4)
109 (3.4)
5 (50.0)
18 (9.3)
83 (2.9)
3 (1.7)
229 (7.3)
330 (10.2)
195 (13.7)
135 (7.5)
21 (0.7)
137 (5.2)
60 (2.3)
15 (0.5)
0 (0.0)
1 (0.8)
14 (0.5)
0 (0.0)

71 (0.5)
419 (3.2)
10694 (82.3)
1814 (14.0)
180 (1.4)
262 (2.0)
318 (2.4)
30 (38.5)
61 (14.2)
186 (1.7)
39 (2.1)
640 (4.9)
753 (5.6)
427 (6.3)
326 (5.0)
69 (0.5)
659 (6.0)
247 (2.3)
46 (0.4)
21 (24.4)
2 (0.5)
22 (0.2)
1 (0.5)

0.4
1.7
1.0
0.4
1.2
1.2
1.4
1.3
0.7
1.7
0.8
1.5
1.8
2.2
1.5
1.3
0.9
1.0
1.4

0.2, 0.9
1.5, 2.0

1.5
2.7

0.7, 1.3

aRR

95% CI

1.0

0.9, 1.2

1.2

0.9, 1.4

1.0

0.9, 1.1

1.0
1.4
0.4

1.3, 1.5
0.4, 0.5

1.0
1.0
1.0
0.9

0.6, 1.5
0.8, 1.2

0.9
1.5
1.0
0.4

0.6, 1.5
1.3, 1.8

1.2

1.0, 1.3

1.7

1.0, 2.9

0.7, 1.3

0.4, 0.5

0.4, 0.5
0.9, 1.7
0.9, 1.5
1.2, 1.8
0.7, 2.6
0.4, 1.1
1.3, 2.2
0.3, 2.6
1.3, 1.7
1.6, 2.1
1.9, 2.6
1.2, 1.8
0.8, 2.1
0.7, 1.0
0.8, 1.3
0.8, 2.4
0.1, 16.7
1.4, 5.3

1.3
2.4

0.4, 0.5

0.1, 13.6
1.2, 4.6

cRR crude risk ratio; CI confidence intervals; aRR adjusted risk ratio; ref referent category; EM effect modification.
Values are presented as n (%).
* 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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OBSTETRICS & GYNECOLOGY

in common with a previous study,1 we found no association of short umbilical cords with maternal smoking or
alcohol intake.
Several studies2,3,12 have implicated a relationship between the presence of oligohydramnios during pregnancy and the subsequent development of a short umbilical cord. Miller et al2,3 hypothesized that the umbilical
cord grows in response to tensile forces exerted on the
cord by fetal movements. Moessinger et al12 showed that
in the presence of oligohydramnios, the umbilical cords
of rat fetuses were 65% of control length. We did not
detect an association between oligohydramnios or hydramnios and a greater or lesser likelihood of being a
case, respectively. Likewise, more recent studies4,5 using
animal models have argued against the stretch hypothesis, stating that the umbilical cord continues to grow
throughout pregnancy in an almost linear fashion. Instead, these studies have proposed a multifactorial explanation for the occurrence of short cords.
Indeed, in this study, no single factor accounted for
the occurrence of all short cords, suggesting a multifactorial etiology. Surprisingly, fewer than 10% of case
infants were reported as having congenital anomalies.
Our data suggest an association of short cords with
particular malformation sequences, particularly those
caused by chromosomal anomalies. Other important
sequences may be those affecting gastrointestinal and
circulatory-respiratory systems. Previous studies of the
association of short cords with malformation sequences
and fetal problems have defined several groups of such
sequences and problems among infants including stillborns and those who died shortly after birth due to
multiple severe anomalies. These include ADAM sequence, cyllosomus/pleurosomus, acephalus-acardia,
presumed primary defect of the umbilical cord and abdominal wall formation, schisis association, and reduced
fetal movement.3,19 Such anomalies are usually multisystem disorders, although they principally involve the
central nervous system, limbs, and cardiovascular system or are associated with defects in the formation of the
anterior abdominal wall. Of interest, in our study, malformations of the central nervous system were not associated with the occurrence of short cords, and the association of musculoskeletal malformations was modest.
Such associations, if present, would have supported the
stretch hypothesis for the lengthening of the cord and
indeed formed the basis of some previous arguments2,3
in favor of the stretch hypothesis. Miller et al3 stated
that extremes of decreased fetal movement occur in cases
of amelia, acardia, arthrogryposis, and atrophy of spinal
muscles. Moessinger et al12 suppressed fetal movement
by curarization, which led to the development of shorter
cords among rat fetuses. By extension, severe central

VOL. 103, NO. 1, JANUARY 2004

nervous system malformations also would reduce fetal


activity.
Our findings of increased risk of prolonged secondstage1 and operative vaginal delivery13 is consistent with
previous studies. However, our findings of increased risk
of retained placenta and postpartum hemorrhage among
women with short umbilical cords have not been previously reported. Finally, we found increased likelihood of
important fetal and infant outcomes, including being
SGA, having hypoxic-ischemic encephalopathy, fetal
distress, and infant death, among case infants than
controls. Our most striking finding was the 2-fold
increase in risk of death among term infants born with
short cords. Clausson et al20 reported a 3-fold increase
in infant deaths among term SGA infants without
congenital malformations in a population-based study
of 510,029 singleton term and postterm births recorded in the Swedish Birth Registry, but they did not
specifically examine cord length. In addition, our findings are consistent with previous studies, which reported low birth weight7 and fetal distress13,18 among
infants with short cords.
The major limitation of this study is the potential for
misclassification of case status, because we identified
cases by ICD-9-CM codes, whereas previous studies
adopted an absolute cord length as a case definition.1,7,8,18,19 Underreporting of short umbilical cord
cases would be present if neonates with umbilical cords
close to the normal length were noted with a lower
frequency. In this instance, we would expect the risk
estimates to be closer to the null. Nonetheless, differential misclassification can also be present if newborns with
short cords were noted as having a short cord more
readily in the presence of other adverse outcomes. Our
findings did confirm previous reports regarding short
umbilical cords, such as low socioeconomic status and
fetal distress,13,18 suggesting that differential misclassification was minimal. We restricted all outcome analyses
and subanalyses to newborns without malformations
under the assumption that, in the presence of any malformation, the short umbilical cord may be missed. In
addition, we attempted to assess potential misclassification of the short cord in cesarean deliveries by examining
outcomes in vaginal deliveries only but found no differences in the outcomes. Finally, gestational age or the
presence of congenital anomalies could potentially lead
to differential recognition of cord anomalies, resulting in
differential misclassification of case status. We addressed
the concern by restricting delivery and fetal and infant
outcome analyses to infants without recognized malformations. The potential effect of misclassification by gestational age also is unlikely to have had a significant

Krakowiak et al

Short Umbilical Cords

125

impact on the associations we report as 94% of cases


were term deliveries.
Although reference standards for cord length have
been reported,10 variation exists in the definition of short
cord.1,7,8,18,19 Naeye1 adopted a cord length of 40 cm,
whereas Nnatu et al8 used a measurement of less than 46
cm. Other studies7,18,19 defined short cords as less than
or equal to 35 cm in length. Their reported prevalence of
short cords ranged from 2%7 to 6%1,18 to 10%,8 contrasting with our incidence of 0.4%. However, most of the
previous studies were not population based;7,8,18,19 had
restrictive exclusion criteria, including gestation less than
37 weeks, malposition, and cases of umbilical cord traumas;1,7,18 or examined a high-risk population,8 which
may account for our lower incidence of short cord. In
addition, the prevalence of short umbilical cords was
consistent 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 factors
and outcomes, giving us greater likelihood of identifying
these factors, some factors were only provided in the
birth certificate data. Underreporting or failure to record
risk factors, such as smoking and alcohol intake, is
possible, and bias may have been introduced if case
mothers reported these risk factors with a differing accuracy compared with control mothers. As such, we would
expect our findings to result in a null risk estimate.
Despite these limitations, our study has several
strengths. We identified a large number of cases, lending
greater precision and power to our analyses than had been
possible with previous studies. Selection bias was unlikely
because we included all identified cases and a large sample
of randomly selected controls. The availability of linked
data enabled us to more accurately identify variables than
through use of either of the data sources alone. In addition,
the definitions and classifications of risk factors and outcomes remained consistent between 1987 and 1998 because the ICD-9 codes and birth certificate standardized
definitions had not changed.
In summary, we demonstrated that case infants had
greater odds of having certain organ or chromosomal
malformations, which suggest that there may be a specific sequence association. Although we did not identify
any modifiable risks that would predispose infants to the
development of a short cord, several previously unreported complications of labor and delivery in both mothers and infants were identified. Because antenatal and
intrapartum screening or diagnoses for short cords do
not exist at present, preventive measures are unavailable. Most importantly, we recognized a 2-fold increase
in infant death among term cases, which suggests closer
monitoring of infants born with a short cord after birth.

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Short Umbilical Cords

Moreover, the presence of a short cord at delivery may


indicate an important surveillance marker for infants in
the first year of life. However, the relationship between
short cords and first year of life mortality among term
infants 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)
543 6656, e-mail: minot@u.washington.edu.

Received May 23, 2003. Received in revised form September 17, 2003.
Accepted September 26, 2003.

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127