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Avoiding multiple pregnancies in ART: Double trouble: yes a twin pregnancy is an adverse outcome

Avoiding multiple pregnancies in ART: Double trouble: yes a twin pregnancy is an adverse outcome The frequency of twins has increased by 30% between 1972 and 1990 in France, USA and England (Tuppin et al., 1993; Luke et al., 1994; Dunn et al., 1996). Twin pregnancies represented a mean of 24.7% of IVF pregnancies as reported in the last World Collaborative Report on IVF (De Mouzon and Lancaster, 1997). In some IVF centres this rate can be as high as 40–50% as seen regularly in meeting presentations. Almost no large scale data are available to assess with precision the exact rate of twins in ovarian stimulation outside IVF. A study carried in France in 1993, showed that 63% of twin pregnancies originated from ovarian stimulation, 19.5% after IVF and 43.5% without IVF (Blondel et al., 1996). Triplet pregnancies (or pregnancies of higher order) are clearly considered as the major adverse outcome of assisted reproductive technologies (ART). Selective embryo reduction is proposed as an alternative to reduce the rank of the pregnancy, even though progress in neonatal care of premature babies has recently questioned the obstetric benefits of this ethically controversial procedure in triplet pregnancies (Khadel et al., 1998). Embryo reduction often proposes to reduce these high rank pregnancies to twins. Twins are rarely considered as an adverse outcome. It is even considered some times as a good way `to make up for lost time', in fact `a nice way to have two children in one pregnancy'. However, it should be underlined that twin pregnancies carry a significantly higher risk of maternal morbidity and mortality, of adverse perinatal outcome, child handicap and psychological difficulties for the parents. Couples should be informed of these indisputable facts and doctors might need to be convinced. Some data available on multiple pregnancies do not always separate twins from other multiples. As far as data on spontaneous pregnancies, figures obtained solely on twins are rare, but data obtained in multiple pregnancies are mainly concerning twins, considering the rarity of spontaneous pregnancies of a higher order. Maternal morbidity and mortality Maternal morbidity and mortality is increased in multiple pregnancies (among which twins represent a large majority) as demonstrated in a recent review (Senat et al., 1998). Higher maternal mortality In France, in 1994, the maternal mortality rate (per 100 000 live births) was 10.2 in multiple pregnancies versus 4.4 in singleton. For Europe as a whole, these figures were 14.9 and 5.2 respectively. The risk of death is, therefore, three times higher in multiple pregnancies (Senat et al., 1998). Higher maternal morbidity For hypertension, a major complication of pregnancy, the odds ratio in twins vary from 1.8 to 3.4, according to the different published studies (Senat et al., 1998). The risk of developing severe hypertension is 2–3 times greater in twins compared with singletons (Senat et al., 1998). The risk of post-partum haemorrhage is 3–4.5 times higher in multiple pregnancies, even if specific data on twins are not presented. The rate of Caesarean section is three times higher (Senat et al., 1998). Multiple pregnancy is an independent factor, and has a 2.3 odds ratio, for a women to be admitted in an intensive care unit (Bouviet et al., 1997). In a 1995 French national perinatal survey, the risk of being transferred to an intensive care unit in women giving birth to twins was 15.5 times higher than for singletons (Senat et al., 1998). Perinatal outcome As well as the fact that maternal morbidity can influence the neonates' health, adverse perinatal outcome of twin pregnancies is clearly demonstrated. Greater prematurity In a French national survey carried out in 1995, the prematurity rate (<37 weeks of amenorrhoea) was 39.2% in twins versus 4.5% in singletons (Blondel et al., 1996). In the same study, the authors showed that 31.5% of very premature births (<33 weeks of amenorrhoea) were related to ovarian stimulation. In a French study of 1263 IVF pregnancies, the prematurity rate (<37 weeks of amenorrhoea) in twins was 43.8% compared with 12.2% in singletons, the corresponding figures were 13.9 and 2.9% for extreme prematurity (<33 weeks of amenorrhoea; Rufat et al., 1994). In the USA, the National Natality Files report that 3.1% of the singletons and 11% of the twins were born at <32 weeks gestation (Kiely, 1998). In a recent study on extreme prematurity in France, the authors estimated that 7% of all extremely premature children (<31 weeks of amenorrhoea) were born following the use of assisted reproductive technologies (Expertise collective, 1997). Lower birth weight Apart from prematurity, twins are exposed to higher rate of low birth weight and small for gestational age (SFGA). In a study carried out in France in 1993, the respective rate of children weighing <2500 g was 47.5% in twins versus 4.6% in singletons (Blondel et al., 1996). In USA, between 1991 and 1995, very low birth weight (<1500 g) was 10 times more frequent in twins than in singleton (1.1 versus 10.1) and the rate for SFGA was four times higher (9.4 versus 35.6) (Alexander et al., 1998). The same results were found in a study carried out on a large group of IVF pregnancies in which twins were SFGA in 49.6% of the cases compared with 14.3% in singletons (Rufat et al., 1994). Higher neonatal mortality Although an increasing body of evidence suggests that the survival rate of twins occurs at an earlier gestational age than singletons (Buekens and Wilcox, 1993; Kiely, 1998), extreme prematurity can affect the survival rate of the children and their potential handicaps. The higher rates of low birth weight and prematurity is, of course, reflected in perinatal mortality rates. In England and Wales in 1991, all mortality parameters (per 1000 live births) were higher in twins than in singletons. The stillbirth rate was 14.2 versus 4.4, the early neonatal mortality rate was 22.8 versus 2.9, the late neonatal mortality rate was 3.9 versus 0.8, the post-natal mortality rate was 6.3 versus 2.4 and the infant mortality rate was 33.0 versus 6.1 (Doyle, 1996). Despite a decrease in recent years (related to medical progress), the mortality rates remain high in twins (Glinianaia et al., 1998). Greater number of handicaps Prematurity and low birth weight are the two main determinants of perinatal mortality and handicap. This is confirmed by the higher risk of cerebral palsy observed in twins. Twins were found to have an odd ratios of 10.2 of having cerebral palsy compared with singletons (Petridou et al., 1996). In the USA, it was observed that twins had a 1.7 times higher risk of severe handicap than singletons (Luke and Keith, 1992). An Australian group reported a five-fold higher risk of cerebral palsy compared with singletons (Petterson, 1993). Other studies confirmed these higher risks of handicap in twins (Pharoah and Cooke, 1996; Williams et al., 1996). More malformations Finally, the rate of malformation is increased in twins compared with singletons, even when taking into account the number of children (Kallen, 1986; Mastroiacovo et al., 1999). Specific malformations (neural tube defects, and structural malformation of the gastro–intestinal tract) have been found to be increased in twins (Doyle et al., 1991). Psychological consequences The prevalence of depression in parents of twins has been found to be higher than in parents of singletons (Thorpe et al., 1991). The same group found that women expecting twins experienced a poorer physical well-being but not poorer emotional well-being (Thorpe et al., 1995). The extent of maternal difficulties (economic, social, psychological) in the immediate period following the birth of twins was demonstrated (Robin et al., 1991, 1996). Such difficulties can lead to child abuse and studies have demonstrated an increased risk of child abuse in twins (Groothuis et al., 1982). Although earlier studies had highlighted a delay in the development of twins, especially in language, recent data do not support this hypothesis and the development of twins has not been found to be significantly lower than that of singletons (Silva and Crosado, 1985; Dezoete and MacArthur, 1996) Conclusions Twin pregnancies have a higher rate of obstetric, perinatal and even post-natal complications, in comparison with singletons. Of course these adverse outcomes are not of the same magnitude when compared with higher order pregnancies. This is probably why twins are `well accepted' by the majority of the ART teams. The point of view of this short paper is not to condemn the fact that twins occur after ART. The poor implantation rate of IVF-produced embryos encourages multiple embryo transfer to increase pregnancy rates. In ovarian stimulation without IVF, the number of mature follicles is correlated with the success rate and the frequency of twins increases with pregnancy rates. However, there is a clear trend towards reducing the proportion of multiple pregnancies when possible. In IVF, a reduction in the number of transferred embryos is advocated by many teams in selected indications (Hazenkamp et al., 2000). Triplet pregnancies are the main target of this transfer policy. But twins should be also considered, as demonstrated in this very brief summary of their complications. There is a clear paradox in regularly obtaining an average of 10 embryos and deciding more and more frequently to transfer only two embryos and even one of them (Gerris et al., 1999). Reducing the number of transferred embryos will also very soon promote less intense stimulation protocols: a more `friendly IVF′ (Olivennes and Frydman, 1998). 1 To whom correspondence should be addressed at: Hôpital A.Béclère, 157 Rue de la Porte de Trivaux, 92140 Clamart, France. E-mail: [email protected] This debate was previously published on Webtrack, May 17, 2000 I would like to thank Drs E.Bryan and B.Blondel for their help and fruitful advice. References Alexander, G., Kogan M., Martin, J. and Papiernik, E. ( 1998) What are the fetal growth pattern of singletons, twins and triplets in the United States. Clin. Obstet. Gynecol. , 41, 115–125. Google Scholar Blondel, B., Du Mazaubrun, C. and Bréart, G. ( 1996) Risque perinatal et prise en charge des grossesses gemellaires, enquete nationale perinatale 1995. Arch. Public Health , 53 (Suppl. 1), 22. Google Scholar Bouvier-Colle, M.H., Varnoux, N., Salanave, B. et al. ( 1997) Case-control study of risk factors for obstetric patients' admission to intensive care units. Eur. J. Obstet. Gynecol. Reprod. Biol. , 74, 173–177. Google Scholar Buekens, P. and Wilcox, A. ( 1993) Why do small twins have a lower mortality rate than singletons? Am. J. Obstet. Gynecol. , 168, 937–941. Google Scholar De Mouzon, and Lancaster, P. ( 1997) World Collaborative Report on IVF preliminary data for 1995. J. Assist. Reprod. Genet. , 14S, 251–265. Google Scholar Dezoete, J.A. and MacArthur, B.A. ( 1996) Cognitive development and behaviour in very low birthweight twins at four years. Acta Genet. Med. Gemellol. , 45, 325–332. Google Scholar Doyle, P., Beral, V., Botting, B. and Wale, C. ( 1991) Congenital malformations in twins in England and Wales. J. Epidemiol. Community Health , 45, 43–48. Google Scholar Doyle, P. ( 1996) The outcome of multiple pregnancy. Hum. Reprod. , 11 (Suppl. 4), 110–117. Google Scholar Dunn, A. and McFarlane, A. ( 1996) Recent trends in the incidence of multiple births and associated mortality in England in Wales. Arch. Dis. Child. , 75, F10–F19. Google Scholar Expertise collective (1997) Influence des grossesses multiples in Grande prématurité. Dépistage et prévention du risque. Edition INSERM, Paris, France. Google Scholar Gerris, J., De Neubourg, D., Mangelschots, K. et al. ( 1999) Prevention of twin pregnancy after in-vitro fertilization or intracytoplasmic sperm injection based on strict embryo criteria: a prospective randomized clinical trial. Hum. Reprod. , 14, 2581–2587. Google Scholar Glinianaia, S.V., Rankin, J. and Renwick, M. ( 1998) Time trends in twin perinatal mortality in northern England, 1982–94. Northern Region Perinatal Mortality Survey Steering Group. Twin Res. , 1, 189–195. Google Scholar Groothuis, J.R., Altemeier, W.A., Robarge, J.P. et al. ( 1982) Increased child abuse in families of twins. Pediatrics , 70, 769–773. Google Scholar Hazekamp, J., Bergh, C., Wennerhold, U.-B. et al. ( 2000) Avoiding multiple pregnancies in ART: consideration of new strategies. Hum. Reprod. , 15, 1217–1219. Google Scholar Kadhel, P., Olivennes, F., Fernandez, H. et al. ( 1998) Are there still obstetric and perinatal benefits for selective embryo reduction of triplet pregnancies? Hum. Reprod. , 13, 3555–3559. Google Scholar Kallen, B. ( 1986) Congenital malformation in twins a population study. Acta Genet. Med. Gemellol. , 35, 167–178. Google Scholar Kiely, J. ( 1998) What is the population-based risk of preterm birth among twins and other multiples? Clin. Obstet. Gynecol. , 41, 3–11. Google Scholar Luke, B. ( 1994) The changing pattern of multiple births in the United States: maternal and infant characteristics, 1973 and 1990. Obstet. Gynecol. , 84, 101–106. Google Scholar Luke, B. and Keith, L.G. ( 1992) The contribution of singletons, twins and triplets to low birth weight, infant mortality and handicap in the United States. J. Reprod. Med. , 37, 661–665. Google Scholar Mastroiacovo, P., Castilla, E.E., Arpino, C. et al. ( 1999) Congenital malformation in twins: an international study. Am. J. Med. Genet. , 83, 117–124. Google Scholar Olivennes, F. and Frydman, R. ( 1998) Friendly IVF the way of the future. Hum. Reprod. , 13, 1121–1124. Google Scholar Petterson, B., Nelson, K.B., Watson, L. and Stanley, F. ( 1993) Twins, Triplets and cerebral palsy in births in Western Australia in the 1980s. Br. Med. J. , 307, 1239–1243. Google Scholar Petridou, E., Koussouri, M. and Toupadaki, N. ( 1996) Risk factors for cerebral palsy: a case control study in Greece. Scand. J. Soc. Med. , 24, 14–26. Google Scholar Pharoa, P and Cooke, T. ( 1996) Cerebral palsy and multiple births. Arch. Dis. Child. , 75, F174–F177. Google Scholar Robin, M., Josse, D. and Tourette, C. ( 1991) Forms of family reorganization following the birth of twins. Acta Genet. Med. Gemellol. , 40, 53–61. Google Scholar Robin, M., Corroyer, D. and Casati, I. ( 1996) Childcare patterns of mothers of twins during the first year. J. Child Psychol. Psychiat. , 37, 453–460. Google Scholar Rufat, P., Olivennes, F., De Mouzon, J. et al. ( 1994) Task force report on the outcome of pregnancies and children conceived by in-vitro-fertilization (France: 1987–1989). Fertil. Steril. , 61, 324–330. Google Scholar Senat, M.V., Ancel, P.Y., Bouvier-Colle, M.H. and Bréart, G. ( 1998) How does multiple pregnancy affect maternal mortality and morbidity. Clin. Obstet. Gynecol. , 41, 79–83. Google Scholar Silva, P.A. and Crosado, B. ( 1985) The growth and development of twins compared with singletons at ages 9 and 11. Aust. Paediatr. J. , 21, 265–267. Google Scholar Thorpe, K., Golding, J., Macgillivray, I. and Greenwood, R. ( 1991) Comparison of prevalence of depression in mothers of twins and mothers of singletons. Br. Med. J. , 302, 875–878. Google Scholar Thorpe, K., Greenwood, R. and Goodenough, T. ( 1995) Does twin pregnancy have a greater impact on physical and emotional well-being than singleton pregnancy? Birth , 22, 148–152. Google Scholar Tuppin, P., Blondel, B. and Kaminski, M. ( 1993) Trends in multiple deliveries and infertility treatments in France. Br. J. Obstet. Gynaecol. , 100, 383–385. Google Scholar Williams, K., Henessy, E. and Alberman, E. ( 1996) Cerebral palsy: effects of twining, birthweight and gestational age. Arch. Dis. Child. , 75, F178–F182. Google Scholar © European Society of Human Reproduction and Embryology http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Human Reproduction Oxford University Press

Avoiding multiple pregnancies in ART: Double trouble: yes a twin pregnancy is an adverse outcome

Olivennes, François
Human Reproduction , Volume 15 (8) – Aug 1, 2000
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Oxford University Press
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© European Society of Human Reproduction and Embryology
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0268-1161
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1460-2350
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10.1093/humrep/15.8.1663
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Abstract

The frequency of twins has increased by 30% between 1972 and 1990 in France, USA and England (Tuppin et al., 1993; Luke et al., 1994; Dunn et al., 1996). Twin pregnancies represented a mean of 24.7% of IVF pregnancies as reported in the last World Collaborative Report on IVF (De Mouzon and Lancaster, 1997). In some IVF centres this rate can be as high as 40–50% as seen regularly in meeting presentations. Almost no large scale data are available to assess with precision the exact rate of twins in ovarian stimulation outside IVF. A study carried in France in 1993, showed that 63% of twin pregnancies originated from ovarian stimulation, 19.5% after IVF and 43.5% without IVF (Blondel et al., 1996). Triplet pregnancies (or pregnancies of higher order) are clearly considered as the major adverse outcome of assisted reproductive technologies (ART). Selective embryo reduction is proposed as an alternative to reduce the rank of the pregnancy, even though progress in neonatal care of premature babies has recently questioned the obstetric benefits of this ethically controversial procedure in triplet pregnancies (Khadel et al., 1998). Embryo reduction often proposes to reduce these high rank pregnancies to twins. Twins are rarely considered as an adverse outcome. It is even considered some times as a good way `to make up for lost time', in fact `a nice way to have two children in one pregnancy'. However, it should be underlined that twin pregnancies carry a significantly higher risk of maternal morbidity and mortality, of adverse perinatal outcome, child handicap and psychological difficulties for the parents. Couples should be informed of these indisputable facts and doctors might need to be convinced. Some data available on multiple pregnancies do not always separate twins from other multiples. As far as data on spontaneous pregnancies, figures obtained solely on twins are rare, but data obtained in multiple pregnancies are mainly concerning twins, considering the rarity of spontaneous pregnancies of a higher order. Maternal morbidity and mortality Maternal morbidity and mortality is increased in multiple pregnancies (among which twins represent a large majority) as demonstrated in a recent review (Senat et al., 1998). Higher maternal mortality In France, in 1994, the maternal mortality rate (per 100 000 live births) was 10.2 in multiple pregnancies versus 4.4 in singleton. For Europe as a whole, these figures were 14.9 and 5.2 respectively. The risk of death is, therefore, three times higher in multiple pregnancies (Senat et al., 1998). Higher maternal morbidity For hypertension, a major complication of pregnancy, the odds ratio in twins vary from 1.8 to 3.4, according to the different published studies (Senat et al., 1998). The risk of developing severe hypertension is 2–3 times greater in twins compared with singletons (Senat et al., 1998). The risk of post-partum haemorrhage is 3–4.5 times higher in multiple pregnancies, even if specific data on twins are not presented. The rate of Caesarean section is three times higher (Senat et al., 1998). Multiple pregnancy is an independent factor, and has a 2.3 odds ratio, for a women to be admitted in an intensive care unit (Bouviet et al., 1997). In a 1995 French national perinatal survey, the risk of being transferred to an intensive care unit in women giving birth to twins was 15.5 times higher than for singletons (Senat et al., 1998). Perinatal outcome As well as the fact that maternal morbidity can influence the neonates' health, adverse perinatal outcome of twin pregnancies is clearly demonstrated. Greater prematurity In a French national survey carried out in 1995, the prematurity rate (<37 weeks of amenorrhoea) was 39.2% in twins versus 4.5% in singletons (Blondel et al., 1996). In the same study, the authors showed that 31.5% of very premature births (<33 weeks of amenorrhoea) were related to ovarian stimulation. In a French study of 1263 IVF pregnancies, the prematurity rate (<37 weeks of amenorrhoea) in twins was 43.8% compared with 12.2% in singletons, the corresponding figures were 13.9 and 2.9% for extreme prematurity (<33 weeks of amenorrhoea; Rufat et al., 1994). In the USA, the National Natality Files report that 3.1% of the singletons and 11% of the twins were born at <32 weeks gestation (Kiely, 1998). In a recent study on extreme prematurity in France, the authors estimated that 7% of all extremely premature children (<31 weeks of amenorrhoea) were born following the use of assisted reproductive technologies (Expertise collective, 1997). Lower birth weight Apart from prematurity, twins are exposed to higher rate of low birth weight and small for gestational age (SFGA). In a study carried out in France in 1993, the respective rate of children weighing <2500 g was 47.5% in twins versus 4.6% in singletons (Blondel et al., 1996). In USA, between 1991 and 1995, very low birth weight (<1500 g) was 10 times more frequent in twins than in singleton (1.1 versus 10.1) and the rate for SFGA was four times higher (9.4 versus 35.6) (Alexander et al., 1998). The same results were found in a study carried out on a large group of IVF pregnancies in which twins were SFGA in 49.6% of the cases compared with 14.3% in singletons (Rufat et al., 1994). Higher neonatal mortality Although an increasing body of evidence suggests that the survival rate of twins occurs at an earlier gestational age than singletons (Buekens and Wilcox, 1993; Kiely, 1998), extreme prematurity can affect the survival rate of the children and their potential handicaps. The higher rates of low birth weight and prematurity is, of course, reflected in perinatal mortality rates. In England and Wales in 1991, all mortality parameters (per 1000 live births) were higher in twins than in singletons. The stillbirth rate was 14.2 versus 4.4, the early neonatal mortality rate was 22.8 versus 2.9, the late neonatal mortality rate was 3.9 versus 0.8, the post-natal mortality rate was 6.3 versus 2.4 and the infant mortality rate was 33.0 versus 6.1 (Doyle, 1996). Despite a decrease in recent years (related to medical progress), the mortality rates remain high in twins (Glinianaia et al., 1998). Greater number of handicaps Prematurity and low birth weight are the two main determinants of perinatal mortality and handicap. This is confirmed by the higher risk of cerebral palsy observed in twins. Twins were found to have an odd ratios of 10.2 of having cerebral palsy compared with singletons (Petridou et al., 1996). In the USA, it was observed that twins had a 1.7 times higher risk of severe handicap than singletons (Luke and Keith, 1992). An Australian group reported a five-fold higher risk of cerebral palsy compared with singletons (Petterson, 1993). Other studies confirmed these higher risks of handicap in twins (Pharoah and Cooke, 1996; Williams et al., 1996). More malformations Finally, the rate of malformation is increased in twins compared with singletons, even when taking into account the number of children (Kallen, 1986; Mastroiacovo et al., 1999). Specific malformations (neural tube defects, and structural malformation of the gastro–intestinal tract) have been found to be increased in twins (Doyle et al., 1991). Psychological consequences The prevalence of depression in parents of twins has been found to be higher than in parents of singletons (Thorpe et al., 1991). The same group found that women expecting twins experienced a poorer physical well-being but not poorer emotional well-being (Thorpe et al., 1995). The extent of maternal difficulties (economic, social, psychological) in the immediate period following the birth of twins was demonstrated (Robin et al., 1991, 1996). Such difficulties can lead to child abuse and studies have demonstrated an increased risk of child abuse in twins (Groothuis et al., 1982). Although earlier studies had highlighted a delay in the development of twins, especially in language, recent data do not support this hypothesis and the development of twins has not been found to be significantly lower than that of singletons (Silva and Crosado, 1985; Dezoete and MacArthur, 1996) Conclusions Twin pregnancies have a higher rate of obstetric, perinatal and even post-natal complications, in comparison with singletons. Of course these adverse outcomes are not of the same magnitude when compared with higher order pregnancies. This is probably why twins are `well accepted' by the majority of the ART teams. The point of view of this short paper is not to condemn the fact that twins occur after ART. The poor implantation rate of IVF-produced embryos encourages multiple embryo transfer to increase pregnancy rates. In ovarian stimulation without IVF, the number of mature follicles is correlated with the success rate and the frequency of twins increases with pregnancy rates. However, there is a clear trend towards reducing the proportion of multiple pregnancies when possible. In IVF, a reduction in the number of transferred embryos is advocated by many teams in selected indications (Hazenkamp et al., 2000). Triplet pregnancies are the main target of this transfer policy. But twins should be also considered, as demonstrated in this very brief summary of their complications. There is a clear paradox in regularly obtaining an average of 10 embryos and deciding more and more frequently to transfer only two embryos and even one of them (Gerris et al., 1999). Reducing the number of transferred embryos will also very soon promote less intense stimulation protocols: a more `friendly IVF′ (Olivennes and Frydman, 1998). 1 To whom correspondence should be addressed at: Hôpital A.Béclère, 157 Rue de la Porte de Trivaux, 92140 Clamart, France. E-mail: [email protected] This debate was previously published on Webtrack, May 17, 2000 I would like to thank Drs E.Bryan and B.Blondel for their help and fruitful advice. References Alexander, G., Kogan M., Martin, J. and Papiernik, E. ( 1998) What are the fetal growth pattern of singletons, twins and triplets in the United States. Clin. Obstet. Gynecol. , 41, 115–125. Google Scholar Blondel, B., Du Mazaubrun, C. and Bréart, G. ( 1996) Risque perinatal et prise en charge des grossesses gemellaires, enquete nationale perinatale 1995. Arch. Public Health , 53 (Suppl. 1), 22. Google Scholar Bouvier-Colle, M.H., Varnoux, N., Salanave, B. et al. ( 1997) Case-control study of risk factors for obstetric patients' admission to intensive care units. Eur. J. Obstet. Gynecol. Reprod. Biol. , 74, 173–177. Google Scholar Buekens, P. and Wilcox, A. ( 1993) Why do small twins have a lower mortality rate than singletons? Am. J. Obstet. Gynecol. , 168, 937–941. Google Scholar De Mouzon, and Lancaster, P. ( 1997) World Collaborative Report on IVF preliminary data for 1995. J. Assist. Reprod. Genet. , 14S, 251–265. Google Scholar Dezoete, J.A. and MacArthur, B.A. ( 1996) Cognitive development and behaviour in very low birthweight twins at four years. Acta Genet. Med. Gemellol. , 45, 325–332. Google Scholar Doyle, P., Beral, V., Botting, B. and Wale, C. ( 1991) Congenital malformations in twins in England and Wales. J. Epidemiol. Community Health , 45, 43–48. Google Scholar Doyle, P. ( 1996) The outcome of multiple pregnancy. Hum. Reprod. , 11 (Suppl. 4), 110–117. Google Scholar Dunn, A. and McFarlane, A. ( 1996) Recent trends in the incidence of multiple births and associated mortality in England in Wales. Arch. Dis. Child. , 75, F10–F19. Google Scholar Expertise collective (1997) Influence des grossesses multiples in Grande prématurité. Dépistage et prévention du risque. Edition INSERM, Paris, France. Google Scholar Gerris, J., De Neubourg, D., Mangelschots, K. et al. ( 1999) Prevention of twin pregnancy after in-vitro fertilization or intracytoplasmic sperm injection based on strict embryo criteria: a prospective randomized clinical trial. Hum. Reprod. , 14, 2581–2587. Google Scholar Glinianaia, S.V., Rankin, J. and Renwick, M. ( 1998) Time trends in twin perinatal mortality in northern England, 1982–94. Northern Region Perinatal Mortality Survey Steering Group. Twin Res. , 1, 189–195. Google Scholar Groothuis, J.R., Altemeier, W.A., Robarge, J.P. et al. ( 1982) Increased child abuse in families of twins. Pediatrics , 70, 769–773. Google Scholar Hazekamp, J., Bergh, C., Wennerhold, U.-B. et al. ( 2000) Avoiding multiple pregnancies in ART: consideration of new strategies. Hum. Reprod. , 15, 1217–1219. Google Scholar Kadhel, P., Olivennes, F., Fernandez, H. et al. ( 1998) Are there still obstetric and perinatal benefits for selective embryo reduction of triplet pregnancies? Hum. Reprod. , 13, 3555–3559. Google Scholar Kallen, B. ( 1986) Congenital malformation in twins a population study. Acta Genet. Med. Gemellol. , 35, 167–178. Google Scholar Kiely, J. ( 1998) What is the population-based risk of preterm birth among twins and other multiples? Clin. Obstet. Gynecol. , 41, 3–11. Google Scholar Luke, B. ( 1994) The changing pattern of multiple births in the United States: maternal and infant characteristics, 1973 and 1990. Obstet. Gynecol. , 84, 101–106. Google Scholar Luke, B. and Keith, L.G. ( 1992) The contribution of singletons, twins and triplets to low birth weight, infant mortality and handicap in the United States. J. Reprod. Med. , 37, 661–665. Google Scholar Mastroiacovo, P., Castilla, E.E., Arpino, C. et al. ( 1999) Congenital malformation in twins: an international study. Am. J. Med. Genet. , 83, 117–124. Google Scholar Olivennes, F. and Frydman, R. ( 1998) Friendly IVF the way of the future. Hum. Reprod. , 13, 1121–1124. Google Scholar Petterson, B., Nelson, K.B., Watson, L. and Stanley, F. ( 1993) Twins, Triplets and cerebral palsy in births in Western Australia in the 1980s. Br. Med. J. , 307, 1239–1243. Google Scholar Petridou, E., Koussouri, M. and Toupadaki, N. ( 1996) Risk factors for cerebral palsy: a case control study in Greece. Scand. J. Soc. Med. , 24, 14–26. Google Scholar Pharoa, P and Cooke, T. ( 1996) Cerebral palsy and multiple births. Arch. Dis. Child. , 75, F174–F177. Google Scholar Robin, M., Josse, D. and Tourette, C. ( 1991) Forms of family reorganization following the birth of twins. Acta Genet. Med. Gemellol. , 40, 53–61. Google Scholar Robin, M., Corroyer, D. and Casati, I. ( 1996) Childcare patterns of mothers of twins during the first year. J. Child Psychol. Psychiat. , 37, 453–460. Google Scholar Rufat, P., Olivennes, F., De Mouzon, J. et al. ( 1994) Task force report on the outcome of pregnancies and children conceived by in-vitro-fertilization (France: 1987–1989). Fertil. 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Journal

Human Reproduction – Oxford University Press

Published: Aug 1, 2000

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