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ORIGINAL RESEARCH |
From the Neonatal Pediatrics Division, Department of Obstetrics and Gynaecology, Reproductive Care Program of Nova Scotia, and Perinatal Epidemiology Research Unit, IWK Health Centre, Halifax, Nova Scotia, Canada.
Address reprint requests to: Samawal Lutfi, MD, CABP, Neonatal Pediatrics Division, IWK Health Centre, 5980 University Avenue, Halifax, NS, B3J 3G9; e-mail: samawal_lutfi{at}yahoo.com.
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ABSTRACT |
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 ABSTRACT METHODSRESULTSDISCUSSIONREFERENCES |
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METHODS: A population-based cohort study of all monochorionic diamniotic twin pregnancies of 20 weeks of gestation or longer born to Nova Scotia (Canada) residents between 1988 and 2000 was examined. The effect of gestational age adjustment and birth weight discordancy of more than 20% on mortality and 1-year survival was studied. Other outcomes studied included birth depression, respiratory distress syndrome, chronic lung disease, interventricular hemorrhage, periventricular leukomalacia, acute renal failure, and congestive heart failure.
RESULTS: Of 404 monochorionic-diamniotic twin pregnancies examined, 48 were identified with twin–twin transfusion syndrome. Total mortality rates per pregnancy were significantly greater in the twin–twin transfusion syndrome group than in the remainder of our monochorionic diamniotic population (P < .01). However, when adjusted for gestational age, mortality failed to achieve statistical significance. Similarly, no differences were noted for 1-year survival and other outcomes of liveborn infants after gestational age adjustment. Discordance in birth weight predicted a higher incidence of morbid outcomes per pregnancy, but this effect was lost after gestational age adjustment.
CONCLUSION: Increased morbidity and mortality of twins with twin–twin transfusion syndrome is likely to be due to a higher incidence of preterm birth. Birth weight discordancy was not found to be an independent predictor of mortality after controlling for gestational age and twin-twin transfusion syndrome.
LEVEL OF EVIDENCE: II-2
Studies conducted on placentae after birth suggest that these abnormal shifts occur because of deep arteriovenous vascular connections within the placental cotyledon in association with little or no superficial arterioarterial vascular communication.2,11–13 The imbalance of blood flow in the communicating vessels between the cotwins, as well as the final expression of twin–twin transfusion syndrome, may be influenced by placental expansion with advancing gestation, fetal cardiac tolerance,14,15 or the fetal renin-angiotensin system, atrial natriuretic peptide, and vasopressin.16–20
Although discordance in fetal or birth weight, amniotic fluid volumes, and fetal or neonatal hemoglobin concentrations are consistent features in twin–twin transfusion syndrome, they are by no means pathognomonic for the syndrome.5,21–23 Therefore, the dependability of most diagnostic criteria proposed to date has been subject to considerable criticism.24,25 Advanced Doppler ultrasonographic confirmation of the abnormal imbalanced flow of blood across vascular anastomotic connections in a monochorionic twin placenta exhibiting the above signs is diagnostic but not feasible in many centers.26,27
Antenatal predictors for the development of twin–twin transfusion syndrome include ultrasound identification of discordant nuchal translucency at 10–14 weeks of gestation,28 quantifying placental vascular angioarchitecture using Doppler sonography,27,29 or evidence of velamentous cord insertion.30 Predictors of mortality in twin–twin transfusion syndrome include significant weight discordance between twins,31 the gestational age at diagnosis,32,33 and the presence of hydrops fetalis.10
The heterogeneity in the literature in defining twin–twin transfusion syndrome results in a range of disease incidence as well as differing outcome measures of morbidity and mortality rates. Furthermore, most studies employed data from hospital-based cohorts that may not reflect unbiased population-based outcomes. The strength of this study is that it is a complete, geographic, population-based cohort using the Nova Scotia Atlee Perinatal Database. The objectives of this study include defining the incidence of twin–twin transfusion syndrome and the outcome and report predictors (maternal, demographical, and newborn) for morbidity and mortality in twins born with twin–twin transfusion syndrome in Nova Scotia (Canada).
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METHODS |
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The Nova Scotia Atlee Perinatal Database was used to identify all cases meeting the inclusion criteria of twin pregnancies of 20 weeks or more of gestation of Nova Scotia residents in the years 1988–2000, where placentation was established as being monochorionic and diamniotic. The period 1988–2000 included twin–twin transfusion syndrome diagnosed by both obstetrical and neonatal criteria. Obstetrical ultrasonographic criteria include confirming monochorionic placental mass using absence of the twin peak sign, oligo- or anhydramnios in the donor using amniotic fluid pocket measurements (defined as a vertical fluid pocket < 2 cm or an amniotic fluid index < 5 cm) and the absence of fetal bladder, hydramnios (defined by a vertical pocket > 8 cm or an amniotic fluid index > 20 cm) in the recipient, and signs of significant fetal cardiac decompensation, cardiac hypertrophy, tricuspid insufficiency, and hydrops. Doppler evaluation of the umbilical arteries in the assessment of twin–twin transfusion syndrome has been used in Nova Scotia since 1995, whereas Doppler evaluation of middle cerebral artery has been in use since 1999.
Neonatal criteria include monochorionic-diamniotic twins with 30% discordance in hemoglobin and more than 20% discordance in birth weight. All cases where twin–twin transfusion syndrome was diagnosed or where the individual clinical signs were noted were retrieved from the database. If an ambiguity was noted such that the individual clinical signs had been coded but the diagnosis of twin–twin transfusion syndrome had not been assigned, charts were reviewed and a diagnostic decision was made (by S.L.).
Chorionicity in this population is identified by ultrasonography and confirmed by postpartum histopathology. All twin placentas, irrespective of ultrasound diagnosis, are sent for pathologic assessment (and chorionicity), not just those associated with adverse outcome.
Twins diagnosed with the syndrome made up the study group, and the remaining monochorionic-diamniotic twins without twin–twin transfusion syndrome formed the comparison group. The primary outcomes of interest were total mortality and 1-year survival. The total mortality included fetal mortality (death before birth), neonatal mortality (death within the first 28 days of life), and infant mortality (death between 28 days and 1 year of life).
Secondary outcomes of interest included birth-depressed infants who required mask resuscitation of more than 1 minute or required endotracheal tube placement at birth. Respiratory distress syndrome includes all infants with signs of distress requiring oxygen supplementation or ventilatory support beyond 6 hours of age and infants with a pathological diagnosis of hyaline membrane disease. Chronic lung disease was defined by any 2 of the following: abnormal chest X-ray not typical of other disease, clinical respiratory distress lasting more than 2 weeks or PCO2 more than 60 mm Hg on 2 or more occasions after 1 week of age with no other obvious cause. Interventricular hemorrhage (includes grade I–IV as defined by Papile et al35), periventricular leukomalacia (evidenced by cystic brain lesions on imaging studies or cortical atrophy), congestive heart failure, hydrops fetalis, persistent pulmonary hypertension of the newborn, acute renal failure, and any minor or major congenital anomalies were other outcomes of interest.
Other variables extracted from the database included demographic descriptions of the mother such as age, family status (single parent versus dual parent home), history of infertility, use of tobacco, pregnancy and delivery history, and infant characteristics such as gestational age at birth, birth weight, and gender. For measure of high socioeconomic status, a proxy variable was used (defined as the top 40% of quintile of annual household income per person equivalent). Differences in outcomes between twins with discordance of birth weight more than 20% were also analyzed in both study and comparison groups. Percentage discordance was calculated by dividing the birth weight of the smaller twin by that of the larger and multiplying by 100.
Crude differences in incidence rates were assessed with the 
2 test and the Fisher exact test where appropriate. Median values were compared by Mann-Whitney test. Logistic regression analysis was used to obtain gestational age-adjusted estimates of odds ratios of total mortality and 1-year survival of liveborn infants. Statistical analysis was conducted using SPSS 10 (SPSS Inc, Chicago, IL). Infant outcomes in a twin pregnancy tend to be correlated, leading to a violation of the assumption of independence between observations. Therefore, the examination of the relationship between twin–twin transfusion syndrome and survival to 1 year, controlling for the influence of potential confounders, was made using the procedure of general estimating equations. This procedure adjusts the variance estimates for the correlation in outcome between the births in a single twin pregnancy. SAS software (PROC GENMOD) was used for this analysis (SAS 8.2, SAS Institute, Cary, NC).
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RESULTS |
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Maternal and infant characteristics are shown in Table 1. Infants in the twin–twin transfusion syndrome group were more likely to be born prematurely (P < .001) compared with those in the comparison group. This difference is consistent with administration of maternal antenatal steroids (P = .002), as well as a lower birth weight (P < .001). There were no significant differences between study and comparison groups in maternal age, maternal obstetrical history, or type and method of delivery. The increase in female twins in the study group was not statistically significant (P = .23).
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Of 808 infants born to 404 mothers, there were 74 (9%) total mortalities, of which 18 were from the study group and 56 were from the comparison group. Figure 2 charts the numbers of fetal, neonatal, and infant deaths per pregnancy. The total mortality rate/pregnancy was significantly different between the study group and the comparison group as determined by univariate analysis (P = .01). The neonatal mortality/pregnancy in the twin–twin transfusion syndrome group was significantly higher than in the comparison group (P = .003); however, the fetal and infant mortality between the 2 groups was not different.
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Overall, the difference between groups in the number of pregnancies where both twins died (total mortality) approached statistical significance (odds ratio [OR] 2.7, 95% confidence interval [CI] 1.0–7.1, P = .05). However, no difference was found in the rate for 1 twin death per pregnancy between the 2 groups. In the twin-twin transfusion syndrome group, 4 of 6 pregnancies with 1 twin dying were donors and the other 2 were recipients.
After excluding all pregnancies with 1 or 2 fetal mortalities, outcomes in liveborn infants in both study and comparison groups are shown in Table 2. There was a significantly lower 1-year survival in the twin–twin transfusion syndrome group by univariate analysis (P = .004). Infants in the twin–twin transfusion syndrome group were more likely to be born depressed or to develop respiratory distress syndrome, chronic lung disease, interventricular hemorrhage, acute renal failure, and congestive heart failure. Periventricular leukomalacia and major or minor congenital anomalies, however, were not found to be different between the 2 groups.
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Both twins were liveborn in 42 twin pairs from the study group and in 332 pairs from the comparison group. A birth weight discordance of more than 20% was noted in 16 of 42 (38%) of the twin–twin transfusion syndrome group and 46 of 332 (15%) of the comparison group (OR 3.8, 95% CI 2.3–6.3, P < .001). A comparison of outcomes per pregnancies with and without discordance in birth weight in both twin–twin transfusion syndrome and comparison groups is shown in Table 3. No difference in survival at 1 year was noted between discordant and nondiscordant twins of both twin–twin transfusion syndrome (P = .15) and comparison (P = .14) groups. There was a significantly higher incidence of birth depression, respiratory distress syndrome, chronic lung disease, interventricular hemorrhage, acute renal failure, and congestive heart failure in twins discordant for birth weight within the twin–twin transfusion syndrome group. There were no significant differences in morbid outcomes between the discordant and nondiscordant twins of the comparison group. In comparing the discordant study group with the discordant comparison group, we found significant differences in birth depression, respiratory distress syndrome, chronic lung disease, interventricular hemorrhage, acute renal failure, and congestive heart failure; these outcomes were much higher among the discordant twin–twin transfusion syndrome group than among the discordant comparison group (Table 3).
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The percentage of added risk of mortality or morbidity for one or both infants per pregnancy with a weight discordancy of more than 20% in the study group was estimated by calculating the estimated rate difference within each group. Discordance of birth weight increased the risk of birth depression by 47% (95% CI 18–76%), of respiratory distress syndrome by 50% (95% CI 19–80%), of chronic lung disease by 38% (95% CI 16–69%), of interventricular hemorrhage by 50% (95% CI 26–74%), of acute renal failure by 19% (95% CI 3–35%), and of congestive heart failure by 21% (95% CI 1–41%) in twins with twin–twin transfusion syndrome (Table 4). In the comparison group, discordance of birth weight had little or no effect on morbid outcomes.
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A regression model in which survival at 1 year is the dependent variable, which was adjusted for gestational age and the diagnosis of twin–twin transfusion syndrome, showed chronic lung disease was significantly higher (OR 47.85, 95% CI 2.97–770.31, P = .001) in 1-year survivors. Discordance in birth weight, however, did not predict a lower survival (OR 0.29, 95% CI 0.07–1.28, P = .07) (Table 4).
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DISCUSSION |
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The incidence of twin–twin transfusion syndrome in Nova Scotia is 0.03% of all pregnancies of 20 or more weeks of gestation, 2.9% of twin births, and 10.6% of monochorionic twins. This is similar to the 0.02% of pregnancies and 1.7% of twin birth incidence Dickinson and Evans32 extrapolated from a West Australian population database. Our incidence however, is much lower than that quoted in a hospital-based cohort studied by Cincotta et al8 (15% of monochorionic twins), Sebire et al5 (6.9% of all twins), or Seng and Rajadurai4 (6.2% of all twins). The differences in incidence may be explained by the criteria used to diagnose twin–twin transfusion syndrome. Seng and Rajadurai4 based their diagnosis on neonatal criteria, whereas Dickinson and Evans,32 Cincotta et al,8 and Sebire et al5 relied on ultrasound criteria for diagnosis of twin–twin transfusion syndrome.
Treatment options for twin–twin transfusion syndrome have changed with time and include expectant management, therapeutic amnioreduction, and laser ablation.14 In Nova Scotia, uncomplicated dichorionic twins undergo growth assessment every 4 weeks, whereas uncomplicated monochorionic twins undergo growth assessment every 3 weeks. When a complicated twin pregnancy is identified (small for gestational age, discordant growth, structural abnormalities, amniotic fluid volume discordance), these serial ultrasound examinations are performed more frequently. In addition ultrasound fetal surveillance is performed weekly from 32 to 34 weeks.
There was no significant difference in the incidence of premature rupture of membranes noted in this study. Gire et al36 looked upon rupture of membranes as a predictor of favorable outcome. In this study, however, premature rupture of membranes did not influence the gestational age–adjusted outcomes of liveborn infants when forced into the model (data not shown).
The incidence of adverse perinatal outcomes per infant seen in our study was lower than that of Dickinson and Cincotta and comparable to Sebire's rates (Table 5). Although these differences could in part be explained by the variations in gestational age and antenatal or neonatal management of the different institutes, the diagnostic criteria used may also contribute to observed differences in outcome rates.
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In our opinion, the different diagnostic criteria may help to identify a select proportion of twin gestations suffering from the twin–twin transfusion syndrome. Almost all monochorionic twins have some degree of abnormal vascular communication. The expression of this syndrome can encompass a spectrum from asymptomatic twin pregnancies with a balanced equilibrium in the net sharing of blood and nutrients to twin pregnancies with a severely and chronically unbalanced intrauterine environment–associated morbidity and mortality. It may be that the most important diagnostic criteria is establishing the presence of the vascular anastomoses, either by antenatal doppler ultrasonography or by postnatal placental histopathology.
In this study we have shown that the increase in perinatal mortality and morbidity is largely due to a higher incidence in preterm birth in the study group. A higher neonatal and infant mortality rate in the study group is also affected by the higher preterm birth. Neonatal and infant mortality in the twin–twin transfusion syndrome group occurred in those born at less than 30 weeks of gestation. Dickinson and Evans32 also showed a clear gestational age influence on survival. This is emphasized by Asztalos et al,3 who looked at a 2-year cohort of twins born at 30 weeks or less of gestation and found no differences in neurodevelopmental morbidity at 18–24 months or mortality between monochorionic and dichorionic twins (38.9% versus 24.6%, P = .17), or between twins and singletons (29.7% versus 22.8%, P = .34).
The death of 1 twin is associated with a significantly higher morbidity in the surviving twin.4,9 In the twin–twin transfusion syndrome group, 4 of 6 such twin deaths were donors. A higher proportion of donor versus recipient deaths is also noted in other studies.26,29,32 The discordance in estimated fetal weight or birth weight has also moved from a diagnostic criterion to a predictor of poor outcome.31 In this study, 20% discordance in birth weight did not predict a lower survival per pregnancy, but it was significantly associated with an added risk of birth depression, respiratory distress syndrome, chronic lung disease, interventricular hemorrhage, acute renal failure, congestive heart failure, or hydrops. Shah and Chaffin37 did not find weight discordancy to be a factor in perinatal mortality. Their study sampled extremely premature twins, born between 24 and 28 weeks of gestation, and set the discordance level to 15%. The higher chronic lung disease rate among survivors is a reflection of a higher perinatal mortality rate that occurred before the onset of the disease; chronic lung disease could only occur in those who survive long enough.
The Nova Scotia Atlee Perinatal Database contains outcome variables up to and including 1 year of life; therefore, we are unable, at present, to provide any measure of a long-term outcome differences between the 2 groups. Because this is a database study, we are limited to pregnancies of at least 20 weeks in duration; therefore, the impact of twin–twin transfusion syndrome on fetal death before 20 weeks is beyond the scope of this study. In this study twin–twin transfusion syndrome diagnosed by obstetrical criteria and neonatal criteria constituted approximately 55% and 45% of the study group, respectively. Because of the small sample size, a subgroup analysis would not provide meaningful results.
Based on this study, the higher mortality of twins born with twin–twin transfusion syndrome is influenced by their higher incidence of preterm birth. Moreover, twins with twin–twin transfusion syndrome and a discordant birth weight of more than 20% have a significantly increased morbidity compared with nondiscordant twins. However, in this cohort of monochorionic-diamniotic twins, birth weight discordancy was not found to be an independent predictor of mortality after controlling for gestational age and twin–twin transfusion syndrome.
As a final note, it has been suggested that the incidence of monoamniotic twins is 1–2% of all twin pregnancies.38 In the Nova Scotia population, we have identified 2.9% of our twin population as monoamniotic. Wensinger39 gave an incidence of 5% of monozygotic twins. More recently Umur et al40 has identified by placental microscopy 24 monoamniotic twins in a population of 224 monochorionic twins, giving a similar incidence of 10%.
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Footnotes |
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Received April 22, 2004. Received in revised form July 14, 2004. Accepted August 5, 2004.
doi:10.1097/01.AOG.0000143828.41271.6c
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REFERENCES |
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2. Denbow ML, Cox P, Taylor M, Hammal DM, Fisk NM. Placental angioarchitecture in monochorionic twin pregnancies: relationship to fetal growth, fetofetal transfusion syndrome, and pregnancy outcome. Am J Obstet Gynecol 2000;182:417–26.[Medline]
3. Asztalos E, Barrett JF, Lacy M, Luther M. Evaluating 2 year outcome in twins 
30 weeks gestation at birth: a regional perinatal unit's experience. Twin Res 2001;4:431–8.[Medline]
4. Seng YC, Rajadurai VS. Twin-twin transfusion syndrome: a five year review. Arch Dis Child Fetal Neonatal Ed 2000;83:F168–70.
5. Sebire NJ, Snijders RJ, Hughes K, Sepulveda W, Nicolaides KH. The hidden mortality of monochorionic twin pregnancies. Br J Obstet Gynaecol 1997;104:1203–7.[Medline]
6. Strong SJ, Corney G: The placenta in twin pregnancy. 1st ed. Oxford (UK): Pergamon Press, 1967.
7. Corney G, Aherne W. The placental transfusion syndrome in monozygous twins. Arch Dis Child 1965;40:264–70.
8. Cincotta RB, Gray PH, Phythian G, Rogers YM, Chan FY. Long term outcome of twin-twin transfusion syndrome. Arch Dis Child Fetal Neonatal Ed 2000;83:F171–6.
9. Mari G, Detti L, Oz U, Abuhamad AZ. Long-term outcome in twin-twin transfusion syndrome treated with serial aggressive amnioreduction. Am J Obstet Gynecol 2000;183:211–7.[Medline]
10. Hayakawa M, Oshiro M, Mimura S, Katou Y, Takahashi R, Nishikawa H, et al. Twin-to-twin transfusion syndrome with hydrops: a retrospective analysis of ten cases. Am J Perinatol 1999;16:263–7.[Medline]
11. Machin G, Still K, Lalani T. Correlations of placental vascular anatomy and clinical outcomes in 69 monochorionic twin pregnancies. Am J Med Genet 1996;61:229–36.[Medline]
12. 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]
13. Umur A, van Gemert MJ, Nikkels PG, Ross MG. Monochorionic twins and twin-twin transfusion syndrome: the protective role of arterio-arterial anastomoses. Placenta 2002;23:201–9.[Medline]
14. Wee LY, Fisk NM. The twin-twin transfusion syndrome. Semin Neonatol 2002;7:187–202.[Medline]
15. van Gemert MJ, Umur A, Tijssen JG, Ross MG. Twin-twin transfusion syndrome: etiology, severity and rational management. Curr Opin Obstet Gynecol 2001;13:193–206.[Medline]
16. Mahieu-Caputo D, Muller F, Joly D, Gubler MC, Lebidois J, Fermont L, et al. Pathogenesis of twin-twin transfusion syndrome: the renin-angiotensin system hypothesis. Fetal Diagn Ther 2001;16:241–4.[Medline]
17. Mahieu-Caputo D, Dommergues M, Delezoide AL, Lacoste M, Cai Y, Narcy F, et al. Twin-to-twin transfusion syndrome. Role of the fetal renin-angiotensin system. Am J Pathol 2000;156:629–36.
18. Bajoria R, Ward S, Chatterjee R. Natriuretic peptides in the pathogenesis of cardiac dysfunction in the recipient fetus of twin-twin transfusion syndrome. Am J Obstet Gynecol 2002;186:121–7.[Medline]
19. Bajoria R, Ward S, Sooranna SR. Atrial natriuretic peptide mediated polyuria: pathogenesis of polyhydramnios in the recipient twin of twin-twin transfusion syndrome. Placenta. 2001;22:716–24.[Medline]
20. Bajoria R, Ward S, Sooranna SR. Influence of vasopressin in the pathogenesis of oligohydramnios-polyhydramnios in monochorionic twins. Eur J Obstet Gynecol Reprod Biol. 2004;113:49–55.[Medline]
21. Lees CC, Schwarzler P, Ville Y, Campbell S. Stuck twin syndrome without signs of twin-to-twin transfusion. Ultrasound Obstet Gynecol 1998;12:211–4.[Medline]
22. Danskin FH, Neilson JP. Twin-to-twin transfusion syndrome: what are appropriate diagnostic criteria? Am J Obstet Gynecol. 1989;161:365–9.[Medline]
23. Mari G, Detti L, Levi-D'Ancona R, Kern L. "Pseudo" twin-to-twin transfusion syndrome and fetal outcome. J Perinatol 1998;18:399–403.[Medline]
24. Bruner JP, Rosemond RL. Twin-to-twin transfusion syndrome: a subset of the twin oligohydramnios-polyhydramnios sequence. Am J Obstet Gynecol. 1993;169:925–30.[Medline]
25. Fisk NM, Borrell A, Hubinont C, Tannirandorn Y, Nicolini U, Rodeck CH. Fetofetal transfusion syndrome: do the neonatal criteria apply in utero? Arch Dis Child. 1990;65:657–61.[Abstract]
26. Quintero RA, Morales WJ, Allen MH, Bornick PW, Johnson PK, Kruger M. Staging of twin-twin transfusion syndrome. Perinatol 1999;19:550–5.
27. Taylor MJ, Denbow ML, Tanawattanacharoen S, Gannon C, Cox PM, Fisk NM. Doppler detection of arterio-arterial anastomoses in monochorionic twins: feasibility and clinical application. Hum Reprod 2000;15:1632–6.
28. Sebire NJ, Talbert D, Fisk NM. Twin-to-twin transfusion syndrome results from dynamic asymmetrical reduction in placental anastomosis: a hypothesis. Placenta 2001;22:383–91.[Medline]
29. Taylor MJ, Denbow ML, Duncan KR, Overton TG, Fisk NM. Antenatal factors at diagnosis that predict outcome in twin-twin transfusion syndrome. Am J Obstet Gynecol 2000;184:1023–8.
30. Fries MH, Goldstein RB, Kilpatrick SJ, Golbus MS, Callen PW, Filly RA. The role of velamentous cord insertion in the etiology of twin-twin transfusion syndrome. Obstet Gynecol 1993;81:569–74.
31. Amaru RC, Bush MC, Berkowitz RL, Lapinski RH, Gaddipati S. Is discordant growth in twins an independent risk factor for adverse neonatal outcome? Obstet Gynecol 2004;103:71–6.
32. Dickinson JE, Evans SF. Obstetric and perinatal outcomes from the Australian and New Zealand twin-twin transfusion syndrome registry. Am J Obstet Gynecol 2000;182:706–12.[Medline]
33. Mari G, Roberts A, Detti L, Kovanci E, Stefos T, Bahado-Singh RO, et al. Perinatal morbidity and mortality rates in severe twin-twin transfusion syndrome: results of the International Amnioreduction Registry. Am J Obstet Gynecol 2001;185:708–15.[Medline]
34. Fair M, Cyr M, Allen AC, Wen SW, Guyon G, MacDonald RC. An assessment of the validity of a computer system for probabilistic record linkage of birth and infant death records in Canada. The Fetal and Infant Health Study Group. Chronic Dis Can 2000;21:8–13.[Medline]
35. Papile LA, Burstein J, Burstein R, Koffler H. Incidence and evolution of subependymal and intraventricular hemorrhage: a study of infants with birth weights less than 1,500 gm. J Pediatr 1978;92:529–34.[Medline]
36. Gire C, Nicaise C, ShoJai R, Chau C, Boubli L, d'Ercole C. Preterm premature rupture of membrane and twin-to-twin transfusion syndrome before 20 weeks: a favourable outcome. Fetal Diagn Ther 2002;17:252–4.[Medline]
37. Shah DM, Chaffin D. Perinatal outcome in very preterm births with twin-twin transfusion syndrome. Am J Obstet Gynecol 1989;161:1111–3.[Medline]
38. Benirschke K, Kaufmann P. Pathology of the human placenta. 3rd ed. New York (NY): Springer-Verlag; 1995.
39. Weinsinger JADF. Monoamniotic twins. Am J Obstet Gynecol 1961;81:323–30.[Medline]
40. Umur A, van Gemert MJ, Nikkels PG. Monoamniotic-versus diamniotic-monochorionic twin placentas: anastomoses and twin-twin transfusion syndrome. Am J Obstet Gynecol 2003;189:1325–9.[Medline]
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