European Journal of Obstetrics & Gynecology and

Reproductive Biology 96 (2001) 150157

Umbilical cord morphology and pregnancy outcome

Edoardo Di Naroa,*, Fabio Ghezzib, Luigi Raioc,
Massimo Franchib, Vincenzo D'Addarioa
a
Department of Obstetrics and Gynecology, University of Bari, Bari, Italy
Department of Obstetrics and Gynecology, University of Insubria, Varese, Italy
c
Department of Obstetrics and Gynecology, University of Bern, Bern, Switzerland
b

Received 21 April 2000; received in revised form 13 July 2000; accepted 1 August 2000

Abstract
Traditionally, the prenatal assessment of the umbilical cord (UC) is limited to the assessment of the number of vessels and to the
evaluation of umbilical artery blood ow parameters. Morphologic aspects of the UC have usually been studies by pathologists and
retrospectively correlated with the perinatal outcome. The introduction of more sophisticated imaging techniques have offered the
possibility to investigate the UC characteristics during fetal life from early to late gestation. A number of investigations have demonstrated
that an altered structure of the UC can be associated with pathologic conditions (i.e. Preeclampsia, fetal growth restriction, diabetes, fetal
demise). Nomograms of the various UC components have been generated and allow the identication of lean or large umbilical cords,
entities frequently associated with fetal growth abnormalities and diabetes. A Wharton's jelly reduction has also been invoked as a possible
cause of fetal death in the presence of single umbilical artery. Prenatal morphometric UC characteristics as well as arterial and venous blood
ow parameters in normal and pathologic conditions will be discussed. # 2001 Elsevier Science Ireland Ltd. All rights reserved.
Keywords: Umbilical cord; Nomograms; Umbilical artery; Lean umbilical cord

1. Introduction
The umbilical cord, a structure vital to the growth and
well-being of the fetus, is 5060 cm long at term gestation
and its three blood vessels course through Wharton's jelly in
a helical fashion, completing 1011 coils between the fetal
and placental insertion site [1]. Although the umbilical cord
is most probably the only organ that dies when life begins, it
is one of the most important parts of the feto-placental unit,
playing a role in determining the manner in which extrauterine life will begin.
For several decades, the morphological and morphometric
aspects of the umbilical cord have been studied and retrospectively correlated with the perinatal outcome by pathologists after delivery [16]. The reason for this was mainly
due to the limited resolution of the ultrasound equipment
used for obstetrical ultrasonography in most institutions.
Traditionally, the prenatal assessment of the umbilical
cord is limited to the ultrasonographic evaluation of the
vessels' number and to the investigation of the resistance to
blood ow in the umbilical arteries by Doppler analysis
[711]. However, an increasing body of clinical and experi*
Corresponding author. Tel.: 39-80-501-4648; fax: 39-80-547-8928.
E-mail address: edoardodinaro@hotmail.com (E. Di Naro).

mental evidence shows that the morphology and constitution

of the umbilical cord can inuence the pregnancy course and
the neonatal outcome [1217]. The introduction of more
sophisticated imaging techniques and an increasing interest
in the umbilical cord and placenta ultrastructure have led to a
better understanding of the mechanisms which regulate the
development of the fetus. Recently, a number of investigations have demonstrated that altered composition and metabolism of the umbilical cord are frequently observed in
certain diseases occurring in pregnancy (i.e. fetal growth
restriction [13], preeclampsia [18], diabetes [19], fetal
demise [20]) and during labor (i.e. fetal distress [21],
meconium [14], fetal heart rate disturbances [14]).
We undertook the present review to clarify the association
between antenatal antrophometric characteristics of the
umbilical cord and perinatal outcome. Although several
umbilical cord malformations (i.e. cysts, hematomas, aneurysms, tumors) have been reported in the literature [22,23], a
comprehensive report of these conditions is beyond the
purpose of this article.
2. Antenatal umbilical cord morphology
The evaluation of the umbilical cord can be accomplished
either from the long-axis view (Fig. 1) or from a cross-

0301-2115/01/$ see front matter # 2001 Elsevier Science Ireland Ltd. All rights reserved.
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151

Fig. 1. Ultrasonographic long-axis view of the umbilical cord.

sectional view (Fig. 2). We believe that the latter method is

more appropriate because it allows a quantication not only
of the umbilical vessels' size but also of the amount of the
Wharton's jelly. It is preferable to obtain measurements in at

least three different parts of the umbilical cord to minimize

the risk of considering an isolated altered portion of the cord.
Nomograms for the diameter of the umbilical vessels,
obtained from 368 healthy pregnant women, have been

Fig. 2. Ultrasonographic cross-sectional view of the umbilical cord.

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Fig. 3. Umbilical cord diameter according to gestational age. The lines

represent the 10th, 50th and 90th percentiles.

Fig. 4. Umbilical cord area according to gestational age. The lines

represent the 10th, 50th and 90th percentiles.

Table 1
Umbilical cord diameter and area according to gestational age
Week of gestation (weeks days)
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
37
38
39
40
41

010
011
012
013
014
015
016
017
018
019
020
021
022
023
024
025
026
027
028
029
030
031
032
033
034
035
036
037
038
039
040
042

6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
6
0

Cases (n)
6
8
8
12
13
15
24
21
18
25
20
18
23
12
20
20
18
15
13
22
23
21
21
22
24
21
20
22
18
17
9
8

S.D.: standard deviation of the mean.

Umbilical cord diameter

Umbilical cord area

Mean (mm)

S.D.a (mm)

Mean (mm2)

S.D.a (mm2)

3.19
3.65
3.68
4.37
5.10
5.95
6.47
7.23
7.87
8.68
9.47
10.73
10.93
12.23
13.14
13.44
14.34
14.06
14.34
16.25
16.24
16.45
16.59
16.72
16.72
16.27
16.53
16.01
15.85
14.48
15.59
14.42

0.40
0.41
0.53
0.43
0.39
0.73
0.81
0.79
0.74
1.07
1.48
1.55
1.58
1.62
1.72
1.74
1.80
1.99
2.07
2.01
2.12
2.21
2.42
2.49
2.57
2.67
2.30
1.99
1.82
1.60
1.41
1.50

8.11
11.40
11.70
15.10
20.50
26.62
33.04
38.96
49.12
55.39
65.01
80.54
87.45
104.54
127.88
128.00
139.03
143.02
143.40
186.36
186.65
187.5
187.95
189.98
192.53
182.65
181.70
181.56
163.07
149.44
146.77
139.07

2.06
4.87
3.16
2.77
3.00
7.35
10.58
9.81
12.90
15.07
18.13
21.04
22.96
22.23
24.33
27.32
38.44
44.99
40.95
49.26
44.56
43.17
51.66
48.20
49.15
47.04
42.02
42.48
39.30
37.11
35.66
24.64

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reported by Weissman et al. [24]. The diameter of the

umbilical arteries increases from 1:2  0:4 mm at 16 weeks
to 4:2  0:4 mm at term gestation and the umbilical vein
diameter varies from 2:0  0:6 mm at 16 weeks of gestation
to 8:2  0:8 mm at term of gestation.
Recently, our group has generated nomograms for the
sonographic diameter and cross-sectional area of the umbilical cord obtained from 557 uncomplicated pregnancies
(Figs. 3 and 4, Table 1) [25]. The sonographic umbilical cord
diameter and area increase as a function of gestational age.
The progressive increase in the umbilical cord diameter and
area up to 32 weeks of gestation followed by a reduction of
umbilical cord size can be explained by the reduction of the
water content of Wharton's jelly towards the end of the
pregnancy [24].
Raio et al. [25] have reported a signicant relationship
between umbilical cord diameter and cross-sectional area
and fetal anthropometric parameters (biparietal diameter,
femur length, abdominal circumference). This nding is in
accordance with that of Gill and Jarjoura [27] who reported
that infants born to women with higher prepregnancy
weight, male infant and those who are heavier at birth have
an advantage with regard to the quantity of Wharton's jelly
wrapped around their umbilical cord vessels [27]. Moreover,
a correlation between Wharton's jelly content, umbilical
cord diameter and estimated fetal weight has been reported
in non-macrosomic fetuses of mothers diagnosed to have
gestational diabetes [19].
3. ``Lean'' umbilical cord
Pathologic studies and case reports demonstrated that a
lean umbilical cord is associated with adverse pregnancy
outcome [2832]. A lean umbilical cord at birth has also
been associated with oligohydramnios and fetal distress.
Silver et al. [33] reported that, in post-term pregnancies, the
umbilical cord diameter is smaller in patients with oligohydramnios than in those with normal amniotic uid. In
addition, these authors found a higher incidence of antepartum variable decelerations in patients with a small umbilical cord diameter than in those with a normal umbilical
cord.
Raio et al. [13] found an association between the presence
of a ``lean'' umbilical cord (cross-sectional area < 10th
centile) and the delivery of a small for gestational age infant
(SGA). Patients with a ``lean'' umbilical cord after 20 weeks
of gestation had a 4.4-fold higher risk (95% condence
interval, 2.168.85) of having an SGA infant than those with
a normal umbilical cord. If the analysis is restricted to
women who underwent an ultrasound at or after 25 weeks
of gestation, the risk of having an SGA infant was 12.4-fold
higher (95% condence interval, 4.3734.67) when the
umbilical cord was ``lean'' than when it was of normal size.
Bruch et al. [12] reported that growth-retarded fetuses with
or without Doppler abnormalities of umbilical arteries have

153

a smaller umbilical cord cross-sectional area at delivery than

normal healthy fetuses. These authors found that growthretarded fetuses with normal Doppler waveforms of umbilical arteries have a reduction in the total umbilical cord area
when compared to that of healthy infants. However, no
modications were observed in the total lumen area of both
arteries, suggesting that the difference in the cross-sectional
area of the umbilical cord between IUGR and normal fetuses
is mainly due to Wharton's jelly diminution and umbilical
vein reduction.
Wharton's jelly appears to serve the function of adventitia, which the umbilical cord lacks, binding and encasing
the umbilical vessels. It has been speculated that the cells of
Wharton's jelly may participate in the regulation of umbilical blood ow and that, at least in some cases, the reduction
in fetal growth could be the consequence of Wharton's jelly
diminution leading to hypoplasia of the umbilical vessels
[12,34].
Although prospective longitudinal studies to assess the
clinical value of the presence of an ultrasonographic lean
umbilical cord in the second half of gestation have not been
conducted, cumulative evidence suggests that an umbilical
cord <10 centile for gestational age is a simple and an early
marker for the delivery of an SGA infant and the occurrence
of intrapartum complications [12,13,28,33].
4. Large umbilical cord
Several reports in the literature have described a large
umbilical cord associated with other fetal structural anomalies such as umbilical cord tumor, urachal cysts, umbilical
cord mucoid degeneration and omphalomesenteric cysts
[1,35,36]. Generally, in these conditions, the morphology
is altered in a limited portion of the umbilical cord.
However, a consistent association between an ultrasonographic large umbilical cord (diameter > 95% confidence
interval) and the presence of a gestational diabetes mellitus
has been reported by Weissman and Jakobi [37]. The
increase in umbilical cord size was already evident at 24
weeks of gestation. Of note is the fact that this increase was
independent of factors such as macrosomia or uncontrolled
diabetes. These authors postulated that other mechanisms
(hemodynamic, biochemical, etc.) are responsible for an
increase in Wharton's jelly or its water content.
Therefore, it can be speculated that an abnormally large
umbilical cord might serve as an additional parameter that
can help to identify fetuses of a mother with some kind of
glucose intolerance during pregnancy. Further studies are,
however, needed to conrm it.
5. Discordant umbilical artery
Discordance between the umbilical arteries is considered
to be present when the difference between the diameter of

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E. Di Naro et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 96 (2001) 150157

Fig. 5. Cross-sectional view of an umbilical cord with discordant umbilical artery.

the two arteries is at least 1 mm in three different portions of

the umbilical cord in both transverse and longitudinal sections [38,39] (Fig. 5).
Raio et al. [39] in the largest study in this eld reported
that morphologic placental alterations (placenta bipartita,
placenta succenturiata, absence of the Hyrtl anastomosis)
and anomalous placental insertion (marginal, velamentous)
of the umbilical cord are often present in cases of discordant
umbilical arteries. These placental anomalies are similar to
those frequently seen in cases of single umbilical artery
(SUA) supporting the theory that the presence of a single
artery represents the greatest expression of umbilical artery
discordance [4,40]. The absence of the Hyrtl anastomosis, a
communicating vessel between the umbilical arteries
usually located within 1.5 cm of the placental end of the
umbilical cord, has been proposed to be responsible for
secondary atrophy or atresia of one of the umbilical arteries
because of different blood pressure in the two placental
territories supplied by the two vessels [41,42]. The difference in the impedance between discordant arteries is of
clinical relevance. Indeed, it has been reported that the
resistance to blood ow between discordant umbilical
arteries is signicantly different, and that, in a relevant
proportion of cases, the resistance index of the smaller
artery is above 2 S.D. of the mean for gestational age
[39]. Therefore, the information provided by Doppler velocimetry of the smaller umbilical artery should be taken with
caution [43], because the signicance of high-resistance
patterns observed in other populations seems to represent

a more benign condition in patients with discordant umbilical arteries.

From a clinical point of view, the presence of discordant
umbilical artery seems to be a benign condition that does not
affect the development of the fetus.
6. Single umbilical artery
The incidence of SUA is reported to be 0.52.5% in
uncomplicated neonates, but is higher in aborted (1.5
7%) and aneuploid fetuses (911%) [4]. Multiple gestations
have a three- to sevenfold increased risk of SUA [4]. Fetuses
whose umbilical cord has a single artery (Fig. 6) are at
increased risk of intrauterine and intrapartum death, regardless of the presence or not of congenital or chromosomal
malformations [4].
Most cases of SUA are diagnosed in the late second
trimester. Despite the apparently easy recognition of
SUA, a low sensitivity of ultrasound (65%) is reported
[44,45]. Color Doppler imaging allows earlier and more
condent diagnosis of SUA, but its apparent efcacy has to
be proven [46]. The patent artery is usually larger than
normal and it may approximate to the vein diameter [47].
The most important clinical implication of SUA is its
possible association with prenatal complications, such as
fetal anomalies, aneuploidies, fetal growth restriction and
placental abnormalities [48]. It has been estimated that the
risk of anomalies is seven times greater than in infant with a

E. Di Naro et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 96 (2001) 150157

155

Fig. 6. Cross-sectional view of an umbilical cord with a single umbilical artery.

three-vessel cord [4]. The list of anomalies identied to be

associated with SUA is long. Persutte and Hobbins [40]
divided the reported abnormalities into three groups: (1)
those believed to be identiable with prenatal ultrasonography; (2) those believed to be difcult to be identied and (3)
those believed to be unidentiable. Using these criteria, they
conclude that prenatal ultrasonography can consistently
identify only 37% of fetal anomalies associated with
SUA. This low accuracy should well be kept in mind when
counseling a patient with a fetus affected by SUA.
The prognosis of SUA infants is mainly related to the
associated fetal structural or chromosomal anomalies and to
the frequently present intrauterine growth retardation [4].
However, this does not explain the increased proportion of
intrauterine or intrapartum death among otherwise normal
fetuses with a SUA [4]. Recently, Raio et al. [49] reported
that the amount of Wharton's jelly of 22 fetuses with SUA
and without congenital or chromosomal abnormalities was
below 2 S.D. from the mean for gestational age. We speculate that the lower amount of Wharton's jelly present in
two-vessel cords in comparison with that of normal umbilical cords could be responsible of a higher vulnerability of
the umbilical cord during the third trimester of pregnancy
and during labor. The elevated incidence of fetal death
towards the end of pregnancy in patients with a single artery
may be in part explained by the cumulative effect of the
relative Wharton's jelly reduction that occurs physiologically in the third trimester of pregnancy [26], acting on a
``constitutional'' deciency of jelly in umbilical cord with a

single artery. It is likely that the amount of Wharton's jelly at

earlier stages of pregnancy exerts a sufcient protection to
the vessels without affecting blood ow, and therefore, fetal
growth.
7. Hypocoiled umbilical cord
The most obvious characteristic of the umbilical cord is
the spiral course of its component blood vessels. Hypocoiled
or non-coiled umbilical cords at delivery have been reported
to be more frequently present in the case of adverse perinatal
outcome [14,15,21]. Strong et al. [21] reported that the
presence of a hypocoiled umbilical cord is responsible for
an increased rate of intrapartum complication and interventional delivery for fetal distress. Rana et al. [14] described a
higher proportion of low cord blood pH and fetal heart rate
disturbances in fetuses with a hypocoiled cord than in those
with a normal umbilical cord. The explanation for the
association between hypocoiled cord and adverse pregnancy
outcome is still controversial. A correlation between the
umbilical coiling index, dened as the number of vascular
coils in a given cord, and the umbilical vein blood ow has
been reported by Degani et al. [50]. In keeping with this
nding, we have recently demonstrated that a signicant
correlation exists between the umbilical vein blood ow per
minute normalized for fetal weight and the umbilical coiling
index (r 0:67, P < 0:001) [51]. These ndings support the
hypothesis proposed by Reynolds [52] that the umbilical

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E. Di Naro et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 96 (2001) 150157

cord is a pistonless pulsometer pumping system. The fetal

blood ows through the umbilical vein pumped by slight but
denite decreases and increases in venous pressure that is
generated from the force of the rising limb of the arterial
pressure pulse. The presence of arterial coils that surround
the vein along the length of the cord provides multiple
variations in an additive fashion. Therefore, a reduced
number of coils in lean umbilical cords could be responsible
for a reduced umbilical blood ow which in turn leads to a
fetal growth impairment. Indeed, Barbera et al. [16] demonstrated a signicant correlation between the umbilical vein
blood ow per kilogram, measured between 20 and 38
weeks of gestation, and anthropometric fetal measurements
such as head circumference and abdominal circumference.
Although the calculation of the umbilical coiling index is
feasible in utero [50], it might be easier to measure the
umbilical vein blood ow with the introduction of new
ultrasound machine softwares which allow an immediate
quantication of the blood ow per minute [51]. Recently, it
has been reported that the measure of umbilical blood ow
has acceptable intra- and interobserver variability, does not
require extreme skill or specialized ultrasound apparatus,
and is not particularly time-intensive [53].
The observation of hypocoiled and lean umbilical cord at
delivery is not an uncommon nding among SGA neonates
and among fetuses who had fetal distress in labor. We have
recently demonstrated that fetuses with a lean cord have a
signicantly lower umbilical coiling index (0:18  0:08
versus 0:29  0:09, P < 0:005) and a reduced umbilical
vein blood normalized for fetal weight (93:7  17:8 versus
126:0  23:4 ml=kg=min, P < 0:001) in comparison with
normal-sized umbilical cords.
Therefore, increasing clinical evidence suggests that the
quantication of umbilical vein blood ow may be useful in
pathological conditions such as intrauterine growth restriction or rhesus isoimmunization [50,54,55].

[3]
[4]
[5]
[6]
[7]
[8]
[9]

[10]
[11]

[12]

[13]

[14]
[15]
[16]

8. Conclusion
Considering that the visualization of the umbilical cord is
easy and fast to obtain with the majority of the ultrasound
machines currently available, we suggest that a target ultrasound of the umbilical cord be performed during the routine
scans in pregnancy. The identication of an abnormally
small or large umbilical cord, the absence of an umbilical
artery or the presence of a discordance between umbilical
arteries should prompt the physician to a more strict monitoring of the pregnancy.

[17]
[18]

[19]
[20]
[21]

References
[1] Benirschke K, Kaufmann P. Pathology of the human placenta. 3rd ed.
New York: Springer, 1995.
[2] Bacsich P, Smout CFV. Some observations on the foetal vessels of the

[22]
[23]

human placenta with an account of the corrosion technique. J Anat

1938;72:35864.
Malpas P, Symonds EM. Observations on the structure of the human
umbilical cord. Surg Gynecol Obstet 1966;123:74650.
Heifetz SA. Single umbilical artery. A statistical analysis of 237
autopsy cases and review of the literature. Perspect Pediatr Pathol
1984;8:34578.
Otsubo Y, Yoneyama Y, Suzuki S, Sawa R, Araki T. Sonographic
evaluation of umbilical cord insertion with umbilical coiling index. J
Clin Ultrasound 1999;27:3414.
Ercal T, Lacin S, Altunyurt S, Saygili U, Cinar O, Mumcu A.
Umbilical coiling index: is it a marker for the foetus at risk? Br Clin
Pract 1996;50:2546.
Wu MH, Chang FM, Shen MR, Yao BL, Chang CH, Yu CH, Hsu CC,
Huang KE. Prenatal sonographic diagnosis of single umbilical artery.
J Clin Ultrasound 1997;26:42530.
Persutte WH, Lenke RR. Transverse umbilical arterial diameter:
technique for the prenatal diagnosis of single umbilical artery. J
Ultrasound Med 1994;13:7636.
Goffinet F, Paris J, Heim H, Nisard J, Breat G. Predictive value of
Doppler umbilical artery velocimetry in a low risk population with
normal fetal biometry. A prospective study of 2016 women. Eur J
Obstet Gynecol Reprod Biol 1997;71:149.
Bartha JL, Comino-Delgado R, Gonzales-Mena C, Lopez I, Arrabal
J. Umbilical blood flow and neonatal morphometry: a multivariate
analysis. Eur J Obstet Gynecol Reprod Biol 1998;79:2733.
Scorza WE, Nardi D, Vintziles AM, Fleming AD, Rodis JF,
Campbell WA. The relationship between umbilical artery Doppler
velocimetry and fetal biometry. Am J Obstet Gynecol
1991;165:10139.
Bruch JF, Sibony O, Benali K, Challier C, Blot P, Nessmann C.
Computerized microscope morphometry of umbilical vessels from
pregnancies with intrauterine growth retardation and abnormal
umbilical artery Doppler. Hum Pathol 1997;28:113945.
Raio L, Ghezzi F, Di Naro E, Franchi M, Maymon E, Mueller MD,
Bruhwiler H. Prenatal diagnosis of a ``lean'' umbilical cord: a simple
marker for fetuses at risk of being small for gestational age at birth.
Ultrasound Obstet Gynecol 1999;13:17680.
Rana J, Ebert GA, Kenneth AK. Adverse perinatal outcome in
patients with an abnormal umbilical coiling index. Obstet Gynecol
1995;85:5737.
Strong TH, Elliott JP, Radin TG. Non-coiled umbilical blood vessels:
a new marker for the fetus at risk. Obstet Gynecol 1993;81:40911.
Barbera A, Galan HL, Ferrazzi E, Rigano S, Jozwik M, Battaglia FC,
Pardi G. Relationship of umbilical vein blood flow to growth
parameters in the human fetus. Am J Obstet Gynecol 1999;181:174
9.
Pawlicka E, Bankowski E, Jaworski S. Elastin of the umbilical cord
arteries and its alterations in EPH gestosis (preeclampsia). Biol
Neonate 1999;75:916.
Bankowski E, Sobolewski K, Romanowicz L, Chyczewski L,
Jawosrski S. Collagen and glycosaminoglycans of Wharton's jelly
and their alterations in EPH-gestosis. Eur J Obstet Gynecol Reprod
Biol 1996;66:10917.
Weissman A, Jakobi P. Sonographic measurements of the umbilical
cord in pregnancies complicated by gestational diabetes. J Ultrasound
Med 1997;16:6914.
Hill LM, DiNofrio DM, Guzick D. Sonographic determination of first
trimester umbilical cord length. J Clin Ultrasound 1994;22:4358.
Strong TH, Finberg HJ, Mattox JH. Antepartum diagnosis of
noncoiled umbilical cords. Am J Obstet Gynecol 1994;170:172933.
Sherer DM, Manning FA. Prenatal ultrasonographic morphologic
assessment of the umbilical cord: a review. Part I. Obstet Gynecol
Surv 1997;52:50614.
Sherer DM, Manning FA. Prenatal ultrasonographic morphologic
assessment of the umbilical cord: a review. Part II. Obstet Gynecol
Surv 1997;52:51523.

E. Di Naro et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 96 (2001) 150157
[24] Weissman A, Jakobi P, Bronshtein M, Goldstein I. Sonographic
measurements of the umbilical cord and vessels during normal
pregnancies. J Ultrasound Med 1994;13:114.
[25] Raio L, Ghezzi F, Di Naro E, Gomez R, Mueller MD, Maymon E,
Mazor M. Sonographic measurements of the umbilical cord and fetal
anthropometric parameters. Eur J Obstet Gynecol Reprod Biol
1999;83:13545.
[26] Sloper KS, Brown RS, Baum JD. The water content of the human
umbilical cord. Early Hum Dev 1979;3:20510.
[27] Gill P, Jarjoura D. Wharton's jelly in the umbilical cord. A study of
its quantitative variations and clinical correlates. J Reprod Med
1993;38:6124.
[28] Goodlin RC. Fetal dysmaturity, ``lean cord'', and fetal distress. Am J
Obstet Gynecol 1987;156:716.
[29] Hall PK. The thin cord syndrome. A review with a report of two
cases. Obstet Gynecol 1961;18:5079.
[30] Sun Y, Arbuckle S, Hocking G, Billson V. Umbilical cord stricture
and intrauterine fetal death. Pediatr Pathol Lab Med 1985;15:72332.
[31] Qureshi F, Jacques SM. Marked segmental thinning of the umbilical
cord vessels. Arch Pathol Lab Med 1994;118:82630.
[32] Clausen I. Umbilical cord anomalies and antenatal fetal deaths.
Obstet Gynecol Surv 1989;44:8415.
[33] Silver RK, Dooley SL, Tamura RK, Depp R. Umbilical cord size and
amniotic fluid volume in prolonged pregnancy. Am J Obstet Gynecol
1987;157:71620.
[34] Gebrane-Younes J, Minh HN, Orcel L. Ultrastructure of human
umbilical vessels: a possible role in amniotic fluid formation?
Placenta 1986;7:17385.
[35] Chantler C, Baum JD, Wigglesworth JS, Scopes JW. Giant umbilical
cord associated with a patent urachus and fused umbilical arteries. J
Obstet Gynecol Br Cwlth 1969;76:2734.
[36] Iaccarino M, Baldi F, Persico O, Palagiano A. Ultrasonographic and
pathologic study of mucoid degeneration of umbilical cord. J Clin
Ultrasound 1986;14:1279.
[37] Weissman A, Jakobi P. Sonographic measurements of the umbilical
cord in pregnancies complicated by gestational diabetes. J Clin
Ultrasound 1997;16:6914.
[38] Dolkart LA, Reimers FT, Kuonen CA. Discordant umbilical arteries:
ultrasonographic and Doppler analysis. Obstet Gynecol 1992;79:59
63.
[39] Raio L, Ghezzi F, Di Naro E, Gomez R, Saile G, Bruhwiler H. The
clinical significance of antenatal detection of discordant umbilical
arteries. Obstet Gynecol 1998;91:8691.
[40] Persutte WH, Hobbins J. Single umbilical artery: a clinical enigma in
modern prenatal diagnosis. Ultrasound Obstet Gynecol 1995;6:216
9.

157

[41] Raio L, Ghezzi F, Di Naro E, Franchi M, Bruhwiler H. Prenatal

identification of the Hyrtl anastomosis and its functional evaluation.
Hum Reprod 1999;14:18903.
[42] Hitschold T, Braun S, Weiss E, Berle P, Beck T, Muntefering H. A
case of discordant flow velocity waveforms in nonanastomoting
umbilical arteries: a morphometric analysis. J Matern Fetal Invest
1992;2:2159.
[43] Predanic M, Kolli J, Yousefzadeh P, Pennisi J. Disparate blood flow
patterns in parallel umbilical arteries. Obstet Gynecol 1998;91:757
80.
[44] Jones TB, Sorokin Y, Bhatia R, Zador I, Bottom SF. Single umbilical
artery: accurate diagnosis? Am J Obstet Gynecol 1993;169:35860.
[45] Catanzarite VA, Hendricks SK, Maida C, Westbrook C, Cousins L,
Schrimmer D. Prenatal diagnosis of two vessels cord: implications
for patients counseling and obstetrics management. Ultrasound
Obstet Gynecol 1995;5:98105.
[46] Jauniaux E, Campbell S, Vyas S. The use of color Doppler imaging
for prenatal diagnosis of umbilical cord abnormalities: report of three
cases. Am J Obstet Gynecol 1989;161:11956.
[47] Persutte WH, Lenke RR. Transverse umbilical arterial diameter: a
new technique for the prenatal diagnosis of single umbilical artery. J
Ultrasound Med 1994;13:7636.
[48] Lilja M. Infants with single umbilical artery studied in a national
registry. 2. Survival and malformations in infants with single
umbilical artery. Paediatr Perinat Epidemiol 1992;6:41622.
[49] Raio L, Ghezzi F, Di Naro E, Franchi M, Bruhwiler H, Luscher KP.
Prenatal assessment of Wharton's jelly in umbilical cords with single
artery. Ultrasound Obstet Gynecol 1999;14:426.
[50] Degani S, Lewinsky RM, Berger H, Spiegel D. Sonographic
estimation of umbilical coiling index and correlation with Doppler
flow characteristics. Obstet Gynecol 1995;86:9903.
[51] Di Naro E, Ghezzi F, Raio L, Franchi M, D'Addario V, Lanzillotti G,
Schneider H. Umbilical vein blood flow in fetuses with normal and
lean umbilical cord. Ultrasound Obstet Gynecol, in press.
[52] Reynolds SRM. Mechanisms of placentofetal blood flow. Obstet
Gynecol 1978;51:2459.
[53] Lees C, Albaiges G, Deane C, Parra M, Nicolaides KH. Assessment
of umbilical arterial and venous flow using color Doppler. Ultrasound
Obstet Gynecol 1999;14:2505.
[54] Gill RW, Kossoff G, Warren PS, Garrett WJ. Umbilical venous flow
in normal and complicated pregnancy. Ultrasound Med Biol
1984;10:34963.
[55] Challis DE, Warren PS, Gill RW. The significance of high umbilical
and venous blood flow measurements in a high-risk population. J
Ultrasound Med 1995;14:90712.