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Hum. Reprod. Advance Access published online on August 24, 2007
Human Reproduction, doi:10.1093/humrep/dem191
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© The Author 2007. Published by Oxford University Press on behalf of the European Society of Human Reproduction and Embryology. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Umbilical cord anomalies are more frequent in twins after assisted reproduction

I. Delbaere1,5, S. Goetgeluk2, C. Derom3, D. De Bacquer4, P. De Sutter1 and M. Temmerman1

1 Department of Obstetrics and Gynaecology, Ghent University, De Pintelaan 185, B-9000 Gent, Belgium 2 Department of Applied Mathematics and Informatics, Ghent University, Krijgslaan 281 S9, B-9000 Gent, Belgium 3 Department of Human Genetics, Katholieke Universiteit Leuven, Belgium 4 Department of Public Health, Ghent University, De Pintelaan 185, B-9000 Gent, Belgium

5 Correspondence address. Tel: +32 9 240 48 53; Fax: +32 9 240 38 31; E-mail: ilse.delbaere{at}ugent.be


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Data collection
 Definitions
 Statistical analysis
 Results
 Discussion
 Acknowledgements
 References
 
BACKGROUND: The objective of this study is to analyse differences in cord characteristics between naturally conceived twins and twins born after assisted reproduction.

METHODS: Between 1985 and 2004, the East Flanders Prospective Twin Survey (EFPTS) registered 4159 twin pairs. We compared cord characteristics between 2119 naturally conceived dizygotic (DZ) twin members and 2243 DZ twin members originating from assisted reproductive technologies (ART). Data were adjusted for intra-twin correlation, year of birth, maternal age, gestational age, parity, sex of the child and number of placentas.

RESULTS: Marginal cord insertion, velamentous cord insertion and single umbilical artery (SUA) occur more frequently in twins following infertility treatment (P < 0.001). The incidence of velamentous cord insertion increases proportionate with ‘invasiveness’ of reproductive techniques: 3.6% in naturally conceived twins versus 5% in twins after artificial induction of ovulation (AIO) [odds ratio (OR) 1.45; 95% confidence interval (CI) 0.99–2.11], 7.4% in twins after IVF (OR 1.49; 95% CI 1.26–1.77) and 10.4% in twins after ICSI (OR 1.31; 95% CI 1.14–1.51). SUA has the highest incidence in twins after AIO: 1.9% compared with 0.6% in naturally conceived twins (OR 3.19; 95% CI 1.66–6.11).

CONCLUSIONS: Umbilical cords of twins born after ART have more pathologic characteristics when compared with cords of naturally conceived twins.

Key words: umbilical cord/assisted reproduction/implantation/multiple pregnancy


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Data collection
 Definitions
 Statistical analysis
 Results
 Discussion
 Acknowledgements
 References
 
Both multiple pregnancy and assisted reproduction have been demonstrated to affect the incidence of abnormal cord insertion (Jauniaux et al., 1990Go; Benirschke, 1995Go; Daniel et al., 1999Go; Victoria et al., 2001Go). The most preponderant and favourable position for umbilical cord insertion is near the centre of the placenta (Benirschke and Kaufman, 2006Go). A cord insertion more towards the edge of the placenta is called a marginal insertion and occurs in 7–10% of term singleton placentas (Robinson et al., 1983Go; Benirschke and Kaufman, 2006Go), while the incidence of insertion on the membranes, i.e. velamentous insertion, is estimated at 1% (Robinson et al., 1983Go; Jauniaux et al., 1990Go; Benirschke and Kaufman, 2006Go). Next to abnormal cord insertion, single umbilical artery (SUA) occurs in ~1% of singleton pregnancies (Bardawil et al., 1988Go) and in 3 to 4% of twin pregnancies (Heifetz, 1984Go; Victoria et al., 2001Go; Benirschke and Kaufman, 2006Go).

Cord insertion anomalies, particularly velamentous insertion, have been associated with preterm delivery (McLennan, 1968Go; Heinonen et al., 1996Go; Victoria et al., 2001Go), low birth weight (Eddleman et al., 1992Go; Heinonen et al., 1996Go; Victoria et al., 2001Go), fetal growth retardation (Bjoro et al., 1985Go; Victoria et al., 2001Go) and deformational defects (Robinson et al., 1983Go; Nerlich et al., 1992Go). In almost 50% of the cases, SUA is associated with other anomalies,(Benirschke and Kaufman, 2006Go) most frequently of the genitourinary system (renal anomalies; Macpherson, 1991Go; Cristina et al., 2005Go). SUA is furthermore correlated with placental abnormalities (Benirschke and Kaufman 2006Go) and with adverse pregnancy outcome, namely preterm delivery, low birth weight, perinatal mortality and growth retardation (Bjoro et al., 1985Go; Gornall et al., 2003Go).

The relationship between mode of conception (spontaneous conception versus conception after IVF) and abnormal cord insertion in both singletons and twins has been investigated only in small populations (n < 100; Englert et al., 1987Go; Jauniaux et al., 1990Go; Gavriil et al., 1993Go; Daniel et al., 2001Go; Narine et al., 2003Go), whereas the association between assisted reproductive technologies (ART) and SUA has so far escaped research. The availability of the population-based East Flanders Prospective Twin Survey (EFPTS) with data on > 6000 twin pairs encouraged us to analyse cord insertion differences between naturally conceived twins and twins born after assisted reproduction. Since the latter have been suggested to fare worse in terms of pregnancy outcome (Pinborg et al., 2004Go; Verstraelen et al., 2005Go) and cord anomalies have been correlated to unfavourable outcome as well, it is of interest to consider the association between cord characteristics and assisted reproduction in twins.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Data collection
 Definitions
 Statistical analysis
 Results
 Discussion
 Acknowledgements
 References
 
Study population
Since 1964, all multiple births in the East Flanders province of Belgium have been registered in the EFPTS. Because assisted reproduction was rather rare until the mid-80s, we analysed twins born in the time span 1985–2004, in which at least one twin had a birth weight of 500 g. For the analysis of placental characteristics between naturally conceived twins and twins as a result of infertility treatment, only dizygotic (DZ) twins were included since the absolute majority of infertility treatment twins are of this type. Characteristics of each child were analysed separately, but the analysis includes adjustment for possible intra-twin correlations.


   Data collection
Top
 Abstract
 Introduction
 Materials and Methods
 Data collection
Definitions
 Statistical analysis
 Results
 Discussion
 Acknowledgements
 References
 
For a detailed description of the data collection, we refer to a previous paper (Loos et al., 1998Go). In brief, staff of all 19 maternity units of East Flanders collaborated to record a defined set of obstetric and perinatal data in twin deliveries. Within 48 h after delivery, the placentas were collected and examined in a standardized manner by a trained midwife. Zygosity was determined through sequential analysis in live- and stillbirths based on sex, fetal membranes, umbilical cord blood groups, placental alkaline phosphatase and, since 1985, DNA fingerprinting. However, due to financial stringency, DNA fingerprints could not be determined systematically on all twin pairs. Therefore, in this study, only same-sexed dichorionic twins with the same markers reaching a probability of 0.95 or more, were considered monozygotic. The remaining same-sex dichorionic twins were classified as ‘unknown’.


   Definitions
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 Abstract
 Introduction
 Materials and Methods
 Data collection
 Definitions
Statistical analysis
 Results
 Discussion
 Acknowledgements
 References
 
Within the EFPTS database, a central or eccentric insertion of the umbilical cord in a particular twin member was registered as an insertion respectively, in the centre or near the centre of the collective placenta or placenta part belonging to the concerned twin member. An insertion at < 2 cm from the edge was defined as marginal insertion, whereas an insertion on the membranes was classified as velamentous insertion.

Because the degree of manipulation in assisted reproduction may have an effect on placental characteristics, different types of reproductive techniques were analysed separately. All women who conceived in vivo after stimulation of ovulation without a subsequent in vitro procedure were included in the artificial induction of ovulation (AIO) group. The IVF group consisted of women who conceived after an in vitro procedure (generally also after stimulation of ovulation), without the direct injection of the prepared spermatozoon in the oocyte in order to facilitate fertilization. The ICSI group included all women who became pregnant by an in vitro procedure with direct injection of the spermatozoon in the oocyte.


   Statistical analysis
Top
 Abstract
 Introduction
 Materials and Methods
 Data collection
 Definitions
 Statistical analysis
Results
 Discussion
 Acknowledgements
 References
 
Differences in prevalence rates were assessed by linear and logistic regression models. As is recommended in literature, we adjusted for parity, maternal age and fetal sex (Heifetz, 1984Go; Heinonen et al., 1996Go). In addition, we adjusted for number of placentas, birth year, duration of gestation and intra-twin correlation by means of mixed models. Analyses were done with SPSS 12.0 and SAS 8.02 statistical software.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Data collection
 Definitions
 Statistical analysis
 Results
Discussion
 Acknowledgements
 References
 
Characteristics of naturally conceived twins were compared with those of twins originating from AIO, IVF or ICSI (Table 1). Mean maternal age, mean gestational age and number of previous children were significantly different depending on mode of conception. Table 2 demonstrates that all types of umbilical cord pathology assessed were found to be significantly more frequent in twins conceived through infertility treatment. The incidence of velamentous cord insertion doubled in twins conceived by IVF and tripled in twins originating from ICSI in comparison with naturally conceived twins. SUA was found to be more than twice as frequent in twins after assisted reproduction compared with naturally conceived twins. When different subtypes of ART were considered for this parameter, AIO seemed to bring about the greatest risk, with an incidence of 1.9%. In twins originating from IVF and ICSI, an incidence of 1.2% was found for SUA which was considerably higher than the incidence found in naturally conceived twins (0.6%). However, this difference was not found to be statistically significant, possibly due to lack of power.


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  		Table 1: Characteristics of DZ twins in the EFPTS—database, according to mode of conception (1985–2004)

 

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  		Table 2: The incidence of central/eccentric cord insertion and abnormal umbilical cord in DZ twins of the EFPTS—population 1985–2004, according to mode of conception and adjusted for maternal age, gestational age, parity, year of birth and fetal sex

 
Extensive research of correlations between umbilical cord anomalies and outcome parameters are beyond the scope of this paper. However, explorative univariate analyses on our database show that mean gestational age and mean birth weight are highest in twins with central insertion of the umbilical cord and when both umbilical arteries are present (see Table 3). Twins with marginally inserted cords were born on average almost 4 days earlier (P < 0.001) and weighed 114 g less (P < 0.001) than those with centrally inserted cords. Although we found no significant difference in gestational age between twins with centrally inserted cords and those with velamentous cord insertion (P = 0.266), the latter weighed an average of 87 grams less (P < 0.001).


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  		Table 3: Differences in mean gestational age and mean birth weight according to type of cord insertion (EFPTS—population 1985–2004)

 
Table 4 shows that twins with SUA were born an average of 9 days earlier (P < 0.001) and weighed 232.6 g less (P < 0.001) than those with two umbilical arteries.


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  		Table 4: Differences in mean gestational age and mean birth weight according to number of umbilical arteries (EFPTS—population 1985–2004)

 
As we found lower mean gestational ages (Table 1) and higher incidences of cord anomalies (Table 2) in twins born after infertility treatment in comparison with those born after natural conception, we examined the impact of cord anomalies in the pathway between mode of conception and gestational age. Analyses showed that marginal insertion of the cord explains some, but not all of the difference in gestational age between naturally conceived twins and twins after infertility treatment. SUA, on the other hand, was found to be a more important confounder in this relationship.


   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Data collection
 Definitions
 Statistical analysis
 Results
 Discussion
Acknowledgements
 References
 
The results obtained indicate that twins born after infertility treatment are at higher risk for cord anomalies, particularly for velamentous insertion and SUA, which have been assessed to engender adverse pregnancy outcomes (Robinson et al., 1983Go; Macpherson, 1991Go; Heinonen et al., 1996Go; Benirschke and Kaufman, 2006Go). This is of interest since previous studies have reported less advantageous outcomes in these types of twins, whereby the pathway to these outcomes is not yet fully defined (Pinborg et al., 2004Go; Verstraelen et al., 2005Go).

We found abnormal cord insertions to be more frequent in all DZ twins compared with earlier reported incidences in singletons (Victoria et al., 2001Go; Benirschke and Kaufman, 2006Go), however, the incidence of all cord anomalies are much higher in twins after infertility treatment. Marginal cord insertion occurred in 10.5% of all twins, which is a slightly higher incidence than the earlier reported incidence in singletons (7–10%; Robinson et al., 1983Go; Benirschke and Kaufman, 2006Go). A marginally inserted cord was found in 8.7% of naturally conceived DZ twins, which is a similar incidence to that which has been found for the singleton population. Velamentous cord insertion, on the other hand, was found to be much more frequent in our twin population, compared with the earlier described incidence in singletons. Approximately 1% of singletons have cords inserted on the membranes (Robinson et al., 1983Go; Jauniaux et al., 1990Go; Benirschke and Kaufman, 2006Go), whereas 3.6% of naturally conceived DZ twins and not < 7% of twins born after infertility treatment manifest this characteristic. Surprisingly, the naturally conceived DZ twins of the EFPTS-population have a lower incidence of SUA compared with the incidence in singletons that has been described in literature (Bardawil et al., 1988Go). The incidence of SUA in twins after infertility treatment is nonetheless double the rate of the incidence in singletons.

The higher incidence of abnormal cord insertion in ART—populations has been previously observed in smaller sample sizes (Englert et al., 1987Go; Jauniaux et al., 1990Go). We compared cord anomalies according to different types of artificial techniques in the same fashion as Daniel et al. (2001)Go. However, the latter study identified more abnormal umbilical cord insertions in singleton ART pregnancies, but found no difference according to the applied technique, thus suggesting that the non-physiological hormonal milieu in ART pregnancies or the embryo transfer procedure are responsible for the cord anomalies. The present study observed an increase in the incidence of velamentous insertion along with the invasiveness of the reproductive procedure. However, SUA was found to be more frequent in twins originating from assisted induction of ovulation.

As stated earlier, velamentous cord insertion has often been correlated with deformational defects in children (Robinson et al., 1983Go). Since placental development is completed only after the teratogenic period, velamentous cord insertion is not held responsible for other structural defects; both phenomena are rather considered secondary to a disturbed nidation process (Benirschke and Kaufman 2006Go). Mechanical factors such as uterine malformations, uterine myomata and multiple gestation (Daniel et al., 2001Go) are likely to result in uterine crowding and competition for space between the fetus(es) and the placenta (Robinson, 1983Go). Hence, the placenta may expand from unfavourable areas towards positions with better nourishment conditions. However, in this laterally growing placental tissue, the umbilical cord remains at its original location, turning an initially centrally inserted cord into a marginal or velamentous insertion (Robinson, 1983Go; Heinonen et al., 1996Go; Bruner et al., 1998Go; Loos et al., 2001Go; Benirschke and Kaufman, 2006Go). Evidence for this trophotropism theory is also found in the occasional migration of an early diagnosed placenta praevia to higher situated places in the uterus while the opposite never occurs (Benirschke and Kaufman, 2006Go).

Next to this theory, there is also a ‘polarity theory’ in which it is hypothesized that an oblique orientation of the blastocyst at the nidation is responsible for marginal or velamentous cord insertion. If the embryo does not face the implantation base, the vessels in the vascular stalk have to extend in order to reach the endometrium. In this way, vessels can be located at marginal or membranous locations (McLennan, 1968Go; Gavriil et al., 1993Go).

The above established higher incidence of abnormal cord insertion in ART pregnancies is more supportive of the trophotropism hypothesis, since the exact chronological succession of biological events, necessary for proper blastocyst implantation, is disturbed at more than one phase in the case of assisted reproduction. Ovulation stimulation protocols engender high levels of estrogen and progesterone, effecting in a thicker endometrium; while embryo transfer encompasses the passage of often more than one embryo through the uterine cervix with an entrance in the uterine cavity 2 days earlier than in physiological conditions (Daniel et al., 2001Go; Romundstad et al., 2006Go). Particularly in ICSI, there is an important interference in physiological conditions, in that both gametes are manipulated before replacement (Van Steirteghem et al., 2002Go), although how this would affect the implantation process is unclear. Furthermore, it is reported that 80% of embryos implant in the area they are transferred in, which is not automatically the most favourable location (Baba et al., 2000Go).

To the best of our knowledge, no earlier studies assessed incidences of cord insertion and SUA in twins in relation to different techniques of assisted reproduction on a considerably high sample size. This study is limited in that for 1453 DZ twins with unlike sex, cord parameters were missing. However, it is unlikely that this has affected our results, since we adjusted for fetal sex and this parameter was not found to be of significant interest.

This account confirms that cord anomalies associated with poor pregnancy outcome are more frequently observed in multiple pregnancies after infertility treatment than after natural conception. Since these types of twins have previously been established to fare worse than naturally conceived DZ twins (Sherer, 2001Go; Pinborg et al., 2004Go; Verstraelen et al., 2005Go), it would be of interest to adjust for cord anomalies in future studies analysing obstetrical and perinatal outcome after ART. It is our contention that cord and placenta pathology may interfere in the pathway between assisted reproduction and pregnancy outcome. Investigations into the effect of cord anomalies in twin pregnancies after infertility treament may further our understanding of the underlying mechanisms responsible for adverse outcomes after ART.


   Acknowledgements
Top
 Abstract
 Introduction
 Materials and Methods
 Data collection
 Definitions
 Statistical analysis
 Results
 Discussion
 Acknowledgements
References
 
Petra De Sutter is holder of a fundamental clinical research mandate by the Flemish Foundation for Scientific Research (FWO-Vlaanderen). The authors wish to acknowledge Professor Robert Derom as founder and driving force of the East Flanders Prospective Twin Survey.


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Data collection
 Definitions
 Statistical analysis
 Results
 Discussion
 Acknowledgements
 References
 
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Submitted on February 6, 2007; resubmitted on May 8, 2007; accepted on May 17, 2007.


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