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ORIGINAL RESEARCH |
From the Division of Feto-Maternal Medicine and Center for Reproductive Medicine, Department of Obstetrics and Gynecology, Academisch Ziekenhuis VUB, Vrije Universiteit Brussel, Brussels, Belgium.
Address reprint requests to: Luc De Catte, MD, Academisch Ziekenhuis Vrije Universiteit, Feto-Maternal Medicine, Department of Obstetrics and Gynecology, Laarbeeklaan 101, 1090 Brussels, Belgium; E-mail: luc.decatte{at}az.vub.ac.be.
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ABSTRACT |
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 ABSTRACT METHODSRESULTSDISCUSSIONREFERENCES |
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METHODS: Data charts of all patients with multifetal (
3) pregnancies referred for fetal reduction over the last 10 years were reviewed for the presence of monochorionic twin pairs or triplets.
RESULTS: Twenty-nine of 239 high-order multiple pregnancies contained a monochorionic component (12.1%), eight of which were monochorionic triplets. Half of all naturally conceived pregnancies contained a monochori-onic component. High-order multiple pregnancies with a monochorionic component resulted significantly more frequently from natural conceptions (7 of 29) than multichorionic pregnancies (7 of 210) (P = .001). Fetal reduction of the monochorionic twin pair in 21 pregnancies resulted in eight twin and 13 singleton pregnancies; mean gestational age at delivery was, respectively, 34.3 ± 2.9 and 39.2 ± 1.4 weeks. Pregnancy loss rate was one of 21 (4.8%). In the remaining eight multiple pregnancies with a monochorionic triplet present, three were complicated by a twin reversed arterial perfusion sequence, and two couples requested a first trimester termination of pregnancy. Fetal reduction of the monochorionic triplet in a dichorionic quadruplet pregnancy resulted in a normal pregnancy outcome. In two monochorionic triplet pregnancies, fetal reduction to monochorionic twin pregnancies with bipolar coagulation of the umbilical cord resulted in a favorable pregnancy outcome.
CONCLUSION: Monochorionic twins or triplets are frequently part of naturally conceived high-order multiple pregnancies. Reduction of the monochorionic twin pairs improves pregnancy outcome. Monochorionic triplet pregnancies show a high complication rate, but may benefit from fetal reduction by cord coagulation.
Assisted reproduction dramatically changed the incidence of multiple pregnancies in the last 15 years. In Flanders, Belgium, there is one twin pregnancy for nearly every 50 pregnancies. The estimated number of spontaneously conceived triplet pregnancies would be one in 8000–9000, yet the incidence has increased almost ten-fold. Seventy-five percent of this increase has been related to ovulation induction and the transfer of more than two embryos.1 Only a small number is related to the rising maternal age at spontaneous conception. It could be assumed that the majority of triplet pregnancies therefore would be multizygotic and multichorionic.
According to Allen, 4.5% of all triplet pregnancies are monozygotic, but the fraction of monochorionic triplets remains unknown.2 Assisted reproductive technologies may result in dichorionic or even monochorionic triplets if one of the embryonic disks splits after the third day after fertilization. Monochorionic twin pregnancies appear 7 to 8 times more frequently after assisted reproduction3,4 than after spontaneous conception, and are especially associated with ovulation induction,5 in vitro fertilization with blastocyst transfer,6 and assisted hatching techniques.7 However, among multiple pregnancies, the frequency of naturally conceived multiple pregnancies with a monochorionic component is much higher than in multiple pregnancies established with assisted reproductive technologies.3,8 Between 5% and 10% of multiple pregnancies after assisted reproductive technologies have monochorionic pairs.8,9 In triplet pregnancies, the presence of a monochorionic twin may jeopardize the perinatal outcome. Early spontaneous loss and pregnancy complications related to twin–twin transfusion syndrome rather than the number of fetuses complicate nearly 30% of dichorionic triplet pregnancies.10
We report the sonographic findings and obstetric outcomes in 29 monochorionic pregnancies of higher order (3).
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METHODS |
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3) between 1990 and 2000 were reviewed. There were two octuplet, two septuplet, six sextuplets, eight quintuplet, 44 quadruplet, and 177 triplet pregnancies. All patients were referred for first trimester multifetal reduction with or without prenatal diagnosis. For that purpose, chorionicity and amnionicity was meticulously determined by counting the number of placental disks, evaluating the lambda sign and the thickness of the dividing membranes, and counting the number of amniotic cavities and yolk sacs per gestational sac. All pregnancies were divided into two groups: group 1 contained multiple pregnancies with a monochorionic component or pregnancies being completely monochorionic (n = 29), whereas group 2 consisted of pregnancies where the chorionicity matched the number of fetuses (n = 210). The mode of conception was categorized in four groups: natural; by ovulation induction; by artificial reproduction techniques, including in vitro fertilization (IVF) and intracytoplasmic sperm injection; or unknown. The number of embryos transferred in utero was compared with the chorionicity of the resulting pregnancies.
Obstetric outcome was studied in terms of mean gestational age at delivery, mean birth weight, congenital malformations related to monochorionicity, perinatal loss rates, and baby take-home rate.
Statistical analysis involved Mann-Whitney test, Fisher exact test, and 
2 test when appropriate at significance level of P 
.05. Relative risks (RRs) and confidence intervals (CIs) for estimated proportions were added.
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RESULTS |
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3) was studied between 1990 and 2000. Mean maternal age and mean gestational age at the time of referral did not differ significantly between groups 1 and 2 (Table 1
). Fourteen patients conceived naturally (5.9%), and of the remaining 225 patients, 105 pregnancies were established after induction of ovulation (43.9%), and 86 needed assisted reproductive technologies (36.0%). In 34 patients, the way of conception was unknown (14.2%), nine of these patients had quadruplet or quintuplet pregnancies, most likely as a result of assisted reproductive technologies. Seven of the 14 naturally conceived high-order multiple pregnancies contained a monochorionic component (0.5; 95% CI 0.23, 0.77), in contrast with 21 of 191 (0.11; 95% CI 0.07, 0.16) pregnancies established after infertility treatment (P < .001). Of these 21, seven were obtained after ovulation induction, and 14 after assisted reproductive technologies (Table 2). Ovulation induction resulted more frequently in a multichorionic pregnancy (28 of 105) than in a pregnancy with monochorionic component (7 of 105 (P = .03; RR = 0.52; 95% CI 0.27, 1.0).
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and 4. In 21 patients (Table 3), including 13 bichorionic triamniotic triplet pregnancies, seven trichorionic quadramniotic quadruplet pregnancies, and one sextuplet pregnancy, the monochorionic twin pairs were selectively reduced resulting in 13 singleton pregnancies and eight bichorionic twin pregnancies. One pregnancy was completely lost at 19 weeks. Mean gestational age at delivery and mean birth weight in singleton and twin pregnancies was 39.2 ± 1.4 weeks and 3105 ± 430.6 g, and 34.3 ± 2.9 weeks, and 2083 ± 426.6 g and 2124 ± 405.4 g, respectively. The baby take-home rate was 27 of 29 or 93.1%.
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. Three of eight cases showed a monochorionic triplet pregnancy and a twin reversed arterial perfusion sequence, none of which reached viability. The acardiac fetus and its related pump twin were monoamniotic in two of the three cases. One patient was initially managed conservatively, but fetal death and preterm prelabor rupture of membranes at 19 weeks led to a termination of pregnancy. In the second pregnancy, a dilation and curettage was performed for a missed abortion, and in the third patient with a twin reversed arterial perfusion sequence, the couple requested a termination of pregnancy. Of the five remaining patients, two opted for a termination of pregnancy for psychologic reasons. In both cases, the monochorionicity was confirmed by pathologic examination. In one dichorionic quadramniotic quadruplet pregnancy, the selective feticide of the monochorionic triplet resulted in an uneventful pregnancy and a normal obstetric outcome. Two patients requested a bipolar coagulation of the cord of one of the fetuses at 18 weeks, resulting in a monochorionic diamniotic twin pregnancy. At 37 weeks, one patient delivered two healthy girls weighing 2700 and 2650 g, the other patient, at 34 weeks, delivered two healthy girls weighing 1545 and 1640 g. They all had an uneventful neonatal course. The baby take-home rate is five of 18 or 27.7%. |
DISCUSSION |
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Multiple pregnancies of higher order established after infertility treatment are usually multizygotic and multi-chorionic. Machin and Bamforth found six monozy-gotic, seven dizygotic, and two trizygotic sets of triplets among 15 consecutive spontaneously conceived triplet pregnancies.14 Allen2 conceived a formula by which the number of monozygotic triplet pregnancies could be calculated in a triplet population, considering the number of like-sex triplets, the number of dizygotic triplets, and the number of unlike-sex triplets, and estimated the number of monozygotic triplets pregnancies in a triplet population at 4.5%. The incidence of monochorionic multiples of higher order must even be lower. Obstetric outcome and clinical management of multiple pregnancies relies on chorionicity. Unfortunately, the few studies having evaluated the perinatal outcome in triplet pregnancies rarely mention the type of placentation, assuming trichorionicity in all cases.15–19
The investigation of third trimester fetal death among 89 triplet pregnancies by Børlum20 demonstrated the association of a mono- or dichorionic placenta in ten of the 15 stillbirths, confirming the observations by Gonen et al21 and Cherouny et al.22 Prenatal findings on chorionicity in triplet pregnancies are scarce and almost exclusively provided by fetal reduction programs. Sepulveda et al23 documented chorionicity in 48 triplet pregnancies by ultrasonographic examination of the epsilon zone. Although the majority of triplet gestations were trichorionic (81%), eight were dichorionic (17%), and one (2%) was monochorionic. Monteagudo et al revealed six monochorionic pregnancies of 148 patients (4%) with high-order multiples: two dichorionic triamniotic and four trichorionic quadramniotic pregnancies.24 Only one of six pregnancies was conceived spontaneously. Of 239 consecutive high-order multiple pregnancies (at least a triplet pregnancy) amenable for fetal reduction, we found 29 patients (12%) with a monochorionic twin or triplet pregnancy. Seventy-two percent (21 of 29) of these pregnancies were the results of different fertility treatment protocols.
Of the high-order multiple pregnancies conceived in a natural way, 50% contained a monochorionic component (seven of 14). Although these results may be biased by the way the patients were recruited, they indicate that multichorionicity in naturally conceived pregnancies should not be considered obvious. Unfortunately, 33 patients in the nonmonochorionic group and one in the monochorionic group lacked data on the way of conception. Although these differences were not statistically significant, the majority of the 33 nonmonochorionic pregnancies could be naturally conceived, as only nine of them were quadruplet of higher-order multiple pregnancies. However, if we assume that all 33 cases were conceived naturally, 15% of these pregnancies still yielded a monochorionic component, which is certainly higher than the expected rate of less than 4.5%.2 This rate has also been reported by Chasen et al;10 in 14 cases of dichorionic triplet pregnancies, two patients conceived naturally (14.3%).
Monozygotic multichorionic triplet pregnancies result from embryonic splitting in the first 3 days after fertilization; after this, they become monochorionic. Establishing chorionicity and amnionicity in multiple pregnancies by early sonographic examination relies on counting the number of gestational sacs, identifying the number of heartbeats and yolk sacs within each gestational sac, and identifying the number of amniotic membranes.24 The highest accuracy is obtained at 8–10 weeks’ gestation. Monochorionicity is linked with a higher morbidity and mortality rate caused by complications particularly related to interfetal vascular anastomoses in the single placental disk: twin–twin transfusion syndrome, twin reversed arterial perfusion sequence, and fetal death of one fetus.25 Feto-feto-fetal triplet transfusion syndrome with normal survival of only the fetus after early preterm cesarean delivery has been reported.26 The incidence of the twin reversed arterial perfusion sequence in triplet pregnancies is much higher than the expected rate of one in 30.27 Monoamnionicity would still further increase that risk. In our small series, three of eight monochorionic multiples showed a twin reversed arterial perfusion sequence, and two cases were monoamniotic.
Patients seeking reduction in multifetal pregnancies containing a monochorionic component should be advised in view of the hidden mortality of the monochorionic component to have this part of their pregnancy reduced.25 Analysis of the outcomes of 14 dichorionic triplets by Chasen et al,10 revealed a nearly 30% pregnancy loss rate. Two of these 14 pregnancies (14%) were terminated because of a severe twin–twin transfusion syndrome, whereas two other patients lost their pregnancy completely before viability at 21 and 22 weeks. Fetal reduction of 21 monochorionic twins and one monochorionic triplet resulted in only one pregnancy loss of 22 (4.5%). In addition, mean gestational age at birth and mean birth weight were comparable with normal twin and singleton pregnancies. Although the presence of monochorionicity was not specified in the 10-year multicenter overview of multifetal pregnancy reductions,28 our data compare well with the reported outcome of multifetal pregnancies reduced to twins or singletons. Multifetal reduction carries a low pregnancy loss rate in experienced hands, and perinatal risk after the reduction is reduced to levels of pregnancies with the same number of fetuses.
Interfetal placental vascular anastomoses prohibit traditional fetal reduction techniques in monochorionic fetuses. Exclusion of the fetus from the common vascular bed of the monochorionic placenta can be achieved by cord ligation, the use of histoacryl or pure ethanol, ultrasound-guided monopolar coagulation of the thoraco-abdominal vasculature, or bipolar coagulation of the umbilical cord, or even fetoscopic neodymium yttrium aluminum garnet laser cord occlusion. Although successful fetal reductions have been reported with each of these techniques, pregnancy loss rates remain much higher than for classical fetal reductions.29 Therefore, these techniques are used only exceptionally in cases where pregnancy loss would otherwise be inevitable, or in cases where one of the fetuses presents a severe congenital malformation most likely leading to fetal death. However, as with trichorionic triplet pregnancies, couples are not always able to cope with a high-order monochorionic multiple gestation with a high perinatal morbidity and mortality. In two patients, we successfully reduced a "sonographically normal" triamnionic triplet to a biamnionic twin pregnancy. Although the reduction does not eliminate the risk for twin–twin transfusion syndrome, it is considered a valid alternative to termination of pregnancy in cases of longstanding infertility treatment. Termination of pregnancy in two of the eight first trimester uncomplicated monochorionic triplet pregnancies can be supported by the fact that these women conceived spontaneously and were primigravidas. They judged the unpredictable outcome of their pregnancy to be psychologically worse than making a new start.
In conclusion, our data indicate a high incidence of complete or partially monochorionic pregnancies among high-order multiple pregnancies, especially after a spontaneous conception. Multifetal reduction of the monochorionic component in a multifetal pregnancy leads to favorable pregnancy outcome. Patients carrying a complete monochorionic pregnancy after assisted reproductive technologies may benefit from cord coagulation techniques to reduce the twin transfusion syndrome–associated perinatal risks. In spontaneously conceived complete monochorionic gestations, a termination of pregnancy is acceptable.
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Footnotes |
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Received October 25, 2001. Received in revised form February 20, 2002. Accepted March 21, 2002.
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REFERENCES |
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2. Allen G. A differential method for estimation of type frequencies in triplets and quadruplets. Am J Hum Genet 1960;12:210.[Medline]
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