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ORIGINAL RESEARCH |
From the Department of Obstetrics and Gynecology, Fundacion Valle de Lili, Cali, Colombia; Department of Obstetrics and Gynecology, Hospital de San Luis Potosi, San Luis Potosi, Mexico; and the Division of Maternal-Fetal Medicine, Toledo Hospital, Toledo, Ohio.
Address reprint requests to: Fernando Arias, MD, PhD Center for Women’s Health The Toledo Hospital Toledo, OH 43606 E-mail: fernandoariasmd{at}promedica.org
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Abstract |
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Methods: We studied retrospectively a cohort of 382 twin pregnancies with gestational ages that ranged from 24 to 40 weeks. Pregnancies were classified as dichorionic or monochorionic by histologic examination of placentas. Infants were subdivided into concordant (less than 5% difference in birth weight), mildly discordant (5–25% difference), and severely discordant groups (more than 25% difference), and their clinical characteristics and findings at placental examination were analyzed and compared.
Results: Severe discordance occurred significantly more often in monochorionic than in dichorionic twins and was associated with significantly more deliveries before 36 weeks and more newborns remaining more than 10 days in the neonatal intensive care unit. Severely discordant monochorionic and dichorionic twins had significantly worse perinatal mortality and morbidity than mildly discordant and concordant twins. The weight of the placenta of the smaller fetus in severely discordant dichorionic twins with separate placentas and the total placental weight in severely discordant monochorionic twins were significantly smaller than the weights of the placentas in their concordant and mildly discordant counterparts. The umbilical cords of the smaller fetuses in both dichorionic and monochorionic pregnancies exhibited significantly more velamentous insertions and single umbilical arteries than in concordant or mildly discordant twins of similar chorionicity.
Conclusion: Severe discordance is more frequent and has greater morbidity in monochorionic than dichorionic twins. The most frequent findings in the placentas of severely discordant twins were small placental weight and umbilical cord abnormalities.
Unequal size of fetuses, a frequent complication of multifetal gestations, is associated with increased perinatal mortality and morbidity.1,2 The birth weight discordance must be at least 25% to cause poor perinatal outcome.1 This degree of discordance is associated with preterm birth, perinatal asphyxia, abnormal labor presentation, and prolonged stay in the neonatal intensive care unit (NICU).3,4 Potential long-term complications include small stature and reduced intelligence.5,6
Most studies of discordance1–6 did not separate twins by chorionicity. It is not clear whether the incidence, mechanism of disease, and perinatal outcomes of discordant dichorionic and monochorionic twins are similar, and there is little information about the placental abnormalities associated with discordance. We analyzed all monochorionic and dichorionic twins delivered in a community hospital during 3 years and related pregnancy outcomes and placental pathology to the severity of birth weight discordance.
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Materials and Methods |
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Gestational age at delivery was estimated from last menstrual period if confirmed by ultrasound examination before 20 weeks. When menstrual histories were unreliable, gestational age was calculated from ultrasound examinations done before 20 weeks. Preeclampsia was diagnosed by sustained blood pressure elevation at or above 140 mmHg systolic or 90 mmHg diastolic plus proteinuria of at least 300 mg/24 hours or 2+ in qualitative urine examinations. Polyhydramnios was diagnosed if the amniotic fluid index was 25 cm or more or if a single amniotic fluid pocket was at least 12 cm. Discordance was defined as difference in birth weight of the twins and was expressed as a percentage of the weight of the larger twin. Twins were divided into three groups by the severity of discordance. Twins with less than 5% difference in birth weight were concordant. Those with 5–25% discordance were considered mildly discordant, and those with more than 25% discordance were defined as severely discordant. Twin-twin transfusion syndrome was diagnosed by a weight difference of at least 15%; polyhydramnios in the recipient twin; oligohydramnios in the donor twin; plethoric appearance of one twin and pale appearance of the other, with hemoglobin difference greater than 5 g/L; and significant differences in the appearance of the maternal surface of the placenta, showing a normal red color in the domain of the plethoric twin and pale and bulky appearance in the domain of the anemic twin.7 Perinatal mortality was defined as fetal or neonatal death during the hospital stay and was corrected for congenital defects incompatible with life. Neonatal morbidity was assessed by the number of days newborns remained in the NICU.
Placentas were placed in plastic bags after delivery and kept at 0C until processed, usually within 24 hours of delivery. Pathologists who examined the placentas had access to the clinical information. The placentas were placed on a clean surface, adherent clots were removed, and the membranes and umbilical cords were excised before they were weighed. Microscopic examination involved the assessment of at least nine sections of each twin placenta. From the pathology report, we extracted information about chorionicity, which was determined by gross and microscopic characteristics of the intertwin membrane, umbilical cord insertion (central, marginal, or velamentous), number of vessels present, and, in monochorionic placentas, by the description of intertwin vascular anastomoses. The presence of vascular-thrombotic lesions (infarcts, abruptio placentae, decidual vasculopathy, fetal vessel thrombosis, and intraplacental hematomas) was also recorded. There was no systematic approach to attribute placental mass to each twin in dichorionic fused and monochorionic placentas, so only the total placental weight was recorded.
The differences between proportions according to the degree of discordance were assessed by 
2 testing. Differences between continuous variables with normal distribution were tested by analysis of variance, followed by Tukey test with pregnancies as the units of analysis. A dependent-proportions analysis was done to compare neonatal outcomes with newborns as the units of analysis. A stepwise logistic regression analysis was used to determine strength of the association between perinatal mortality and variables believed to be clinically relevant (maternal age, poor obstetric history, chorionicity, gestational age at delivery, severity of discordance, and birth weight of the smaller infant), using pregnancies as the units of analysis. Statistical analysis was done with software from Epistat Services (Richardson, TX).
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Results |
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Sex distribution of the newborns was 370 males and 384 females. Eleven twin pairs had identical birth weights. Among the remaining pairs, a significantly larger number of second-born twins were smaller than first-born ones (194 of 366 [53%] versus 164 of 366 [46.9%]; odds ratio [OR] 1.38; 95% confidence interval [CI] 1.02, 1.87; P = .03). After classification by degree of discordance, 81 of 288 (28.1%) dichorionic and 20 of 89 (22.4%) monochorionic pregnancies were concordant; 185 of 288 (64.2%) dichorionic and 51 of 89 (57.3%) monochorionic pregnancies were mildly discordant, and 22 of 288 (7.6%) dichorionic and 18 of 89 (20.2%) monochorionic pregnancies were severely discordant. The incidence of severe discordance was significantly larger in monochorionic twins than in dichorionic twins (OR 3.06; 95% CI 1.47, 6.33; P < .01).
Monochorionic twins had worse outcomes than dichorionic twins, and significantly more of them delivered before 30 weeks (11 of 89 [12.3%] versus 14 of 288 [4.6%]; OR 2.7; 95% CI 1.11, 6.77; P = .02), remained more than 10 days in the NICU (73 of 118 [40.4%] versus 137 of 576 [23.7%]; OR 2.27; 95% CI 1.53, 3.22; P < .01), and remained more than 30 days in the NICU (25 of 178 [14%] versus 37 of 576 [6.4%]; OR 2.38; 95% CI 1.34, 4.20; P < .01). There were no significant differences between monochorionic and dichorionic twins in delivery before 36 weeks, incidence of cesarean deliveries, and development of polyhydramnios and preeclampsia (Table 1
). Delivery before 36 weeks was spontaneous in 25 of 40 (62.5%) monochorionic and in 78 of 106 (73.5%) dichorionic pregnancies, a nonsignificant difference. The most frequent reasons for indicated delivery were non-reassuring tests of fetal well-being (abnormal nonstress test plus abnormal umbilical and cerebral artery Doppler or biophysical profile score less than four in monochorionic twins (eight of 15; 53.3%) and preeclampsia in dichorionic twins (13 of 24; 54.1%).
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). There were three stillborn infants and six neonatal deaths in the dichorionic group, and four stillborn infants and three neonatal deaths in the monochorionic group. Two of the monochorionic neonatal deaths excluded from analysis were in twins with similar severe congenital abnormalities of the central nervous system. Stepwise logistic regression analysis was used to identify independent risk factors associated with corrected perinatal mortality, and it was found that birth weight of the smaller twin was the strongest predictor (Table 3).
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The neonatal outcomes of severely discordant dichorionic and monochorionic twins were significantly worse than the outcomes of concordant and mildly discordant twins of the same chorionicity (Table 2
). When severely discordant monochorionic and dichorionic twins were compared, delivery before 36 weeks (14 of 18 [77.7%] versus nine of 22 [40.9%]; OR 5.05; 95% CI 1.05, 27.22; P = .04) and more than 10 days’ stay in the NICU (25 of 36 [69.4%] versus 18 of 44 [40.9%]; OR 3.28; 95% CI 1.17, 9.30; P = .02) occurred significantly more often in severely discordant monochorionic twins.
One hundred fifty of 288 dichorionic placentas were fused and 138 were separate. One hundred thirty-eight of 150 fused (92.0%), 268 of 276 separated (97.1%), and 77 of 89 monochorionic placentas (86.5%) were examined pathologically. Weights of placentas of the smaller fetuses in severely discordant dichorionic twins with separate placentas were significantly less than weights of placentas of the smaller concordant and mildly discordant twins (Table 4). Weights of placentas of severely discordant smaller twins were significantly less than weights of placentas of larger twins (238 ± 128 g, versus 358 ± 104 g; P = .01). The total placental weights of severely discordant monochorionic twins were significantly less than the total placental weights of concordant and mildly discordant twins. No significant differences were seen in total placental weights among dichorionic twins with fused placentas and different degrees of discordance.
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). There were no significant differences in the number of placental vascular-thrombotic lesions in relation to the degree of discordance in dichorionic twins.
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). There was no statistically significant difference in the numbers of superficial vascular anastomoses associated with increased severity of discordance in monochorionic twins.
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Discussion |
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Different genetic potential, crowding in utero, unequal sharing of placental mass, and placental insufficiency are explanations for discordant fetal growth in dichorionic twins.13–15 Hemodynamic imbalance caused by placental vascular anastomoses is commonly cited as the cause in monochorionic gestations.13–15 Eberle et al13 found that birth weight discordance was related in dichorionic twins to placental vascular-thrombotic lesions and in monochorionic twins to placental vascular anastomoses. Rizzo et al14 found Doppler evidence that suggested placental insufficiency in dichorionic discordant twins and fetal anemia in monochorionic twins. More recently, Blickstein et al16 suggested that discordance was a function of the uterine capacity to carry twins and was dependent on the birth order.
We found that decreased placental weight and increased umbilical cord abnormalities were the most common placental findings associated with severe discordance in dichorionic and monochorionic twins. Smaller and larger severely discordant dichorionic twins had smaller placentas than their concordant and mildly discordant counterparts, suggesting that growth restriction affects placental and fetal growth of both twins but with different degrees of severity. The finding of smaller total placental mass in severely discordant monochorionic twins also suggests that placental insufficiency is a mechanism of severe discordance in these types of twins, but the lack of an accurate estimation of placental mass distribution weakens that conclusion.
The association of a small placental mass with severe discordance in dichorionic twins with separate placentas is not surprising because there is a well-accepted relation between placental weight and fetal size,17 and hypoplastic placentas are common in newborns with severe fetal growth restriction (FGR).18 Abnormalities of the umbilical cord, particularly velamentous insertion, also are more frequent in twin than singleton gestations and are associated with preterm delivery, twin-twin transfusion, and FGR.19 Single UA is three to four times more frequent in twins than singletons and is usually associated with the smaller of discordant pairs.20
Vascular-thrombotic lesions, particularly infarcts, acute atherosis of spiral arteries, thrombosis of fetal vessels, intraplacental hematomas, and perivillous fibrin deposition, are common in the placentas of growth-restricted fetuses.21 We found that this was the case in the placentas of smaller, severely discordant monochorionic twins. However, many of the placentas were not examined in the fresh state and placental-bed biopsies were not obtained, so the incidence of decidual vasculopathy is probably grossly underestimated.
We found superficial vascular anastomosis in 51.1% of monochorionic placentas, an incidence lower than the 76–98% reported in the literature.22 Our lower rate of detection of anastomosis in this study might be due to the lack of placental perfusion studies, which allow a more accurate evaluation of the number and nature of vascular communications. Another consequence of the lack of perfusion studies was our inability to determine the presence and frequency of deep vascular anastomosis.
Our incidence of twin-twin transfusion syndrome of 5.6% is consistent with the 5–10% incidence reported in the literature.23 As described by other investigators,24 we found few superficial vascular anastomoses in the placentas of twins with twin-twin transfusion syndrome. Pathologic evidence indicates that fetuses with twin-twin transfusion share one or more placental cotyledons with the arterial supply from one and the venous return going to the other (third circulation). Superficial anastomoses are a mechanism to compensate for the continuous blood loss from the twin on the arterial side to the twin on the venous side of the shared cotyledon. According to this concept, absence of super-ficial anastomoses is one of the fundamental anatomic features leading to the twin-twin transfusion syndrome.
In contrast to the results of Eberle et al,13 we found an increased incidence of severe discordance in monochorionic twins and a clear association between reduced placental weight and growth discordance in dichorionic twins. In addition, our findings do not support their conclusion that the most important cause of discordance in monochorionic twins is superficial vascular anastomoses and in dichorionic twins is vascular-thrombotic lesions. Although there are differences in the number of cases, definition of severe discordance, and methodology in analyses of the placental lesions, the reasons for the inconsistencies between their findings and ours need further investigation.
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Footnotes |
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Received March 27, 2000. Received in revised form September 22, 2000. Accepted October 5, 2000.
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References |
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2. Sonntag J, Waltz S, Schollmeyer T, Schuppler U, Schroeder H, Weisner D. Morbidity and mortality of discordant twins up to 34 weeks of gestational age. Eur J Pediatr 1996;155:224–9.[Medline]
3. Fraser D, Picard R, Picard E, Leiberman JR. Birth weight discordance, intrauterine growth retardation and perinatal outcomes in twins. J Reprod Med 1994;39:504–8.[Medline]
4. Hollier LM, McIntire DD, Leveno KJ. Outcome of twin pregnancies according to intrapair birth weight differences. Obstet Gynecol 1999;94:1006–10.
5. Babson SG, Phillips DS. Growth and development of twins dissimilar in size at birth. N Engl J Med 1973;289:937–40.
6. Rydhstroem H. The relationship of birth weight and birth weight discordance to cerebral palsy or mental retardation later in life for twins weighing less than 2500 grams. Am J Obstet Gynecol 1995;173:680–6.[Medline]
7. Fox H. Pathology of the placenta. 2nd ed. Philadelphia: WB Saunders, 1997.
8. Baldwin VJ. Pathology of multiple pregnancy. New York: Springer-Verlag, 1994:231–4.
9. Minakami H, Honma Y, Matsubara S, Uchida A, Shiraishi H, Sato I. Effects of placental chorionicity on outcome in twin pregnancies. J Reprod Med 1999;44:595–600.[Medline]
10. Sebire N, Snijders R, Hughes K, Sepulveda W, Nicolaides KH. The hidden mortality of monochorionic twin pregnancies. Br J Obstet Gynaecol 1997;104:1203–7.[Medline]
11. Bajoria R, Kingdom J. The case for routine determination of chorionicity and zygosity in multiple pregnancy. Prenat Diagn 1997;17:1207–25.[Medline]
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17. Bonds DR, Gabbe SG, Kumar S, Taylor T. Fetal weight/placental weight ratio and perinatal outcome. Am J Obstet Gynecol 1984; 149:195–200.[Medline]
18. Thomson AM, Billewickz WZ, Hytten FR. The weight of the placenta in relation to birth weight. J Obstet Gynaecol Br Commonw 1969;76:865–72.[Medline]
19. Eddleman KA, Lockwood CJ, Berkowitz GS, Lapinski RH, Berkowitz RL. Clinical significance and sonographic diagnosis of velamentous umbilical cord insertion. Am J Perinatol 1992;9:123–6.[Medline]
20. Heifetz SA. Single umbilical artery. A statistical analysis of 237 autopsy cases and review of the literature. Perspect Pediatr Pathol 1984;8:345–78.[Medline]
21. Fox H. Placentation in intrauterine growth retardation. Fetal and Maternal Medicine Review 1997;9:61–71.
22. Robertson EG, Neer KJ. Placental injection studies in twin gestation. Am J Obstet Gynecol 1983;147:170–5.[Medline]
23. Benirschke K. Twin placenta in perinatal mortality. N Y State J Med 1961;61:1499–508.
24. Bajoria R, Wigglesworth J, Fisk NM. Angioarchitecture of monochorionic placentas in relation to the twin-twin transfusion syndrome. Am J Obstet Gynecol 1995;172:856–63.[Medline]
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