Hum. Reprod. Advance Access originally published online on September 26, 2007
Human Reproduction 2007 22(11):2896-2902; doi:10.1093/humrep/dem260
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Parenting and the psychological development of a representative sample of triplets conceived by assisted reproduction
1 Centre for Family Research, Faculty of Social and Political Sciences, Free School Lane, University of Cambridge, Cambridge CB2 3RF, UK 2 Department of Obstetrics and Gynaecology, Cochin Hospital, Paris, France 3 Follow-Up, Villennes sur Seine, France 4 The Psychometrics Centre, University of Cambridge, UK
5 Correspondence address. Tel: +44-1223-334510; Fax: +44-1223-330574; E-mail: seg42{at}cam.ac.uk
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Abstract |
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BACKGROUND: The aim of the study was to examine the quality of parenting and the psychological development of three-year-old children in IVF/ICSI families with triplets.
METHODS: Comparisons were carried out between a representative sample of 10 families with triplets and matched groups of 15 families with twins and 30 families with singletons. The families were recruited from Follow-Up, a national organization in France that was established to study children conceived by assisted reproduction. Standardized measures of the mother's psychological well-being (parenting stress, depression and quality of marriage) and standardized measures of the child's psychological development (emotional/behavioural problems and general development) were completed by the mother.
RESULTS: Mothers with a multiple birth were found to experience greater difficulties in parenting than mothers of singletons, with no differences between mothers of triplets and mothers of twins. Regarding the children, there were no differences in emotional or behavioural problems between triplets, twins and singletons. However, there were indications of mild delay among triplets and twins in some aspects of language development in comparison with the singleton children.
CONCLUSIONS: The birth of triplets or twins does appear to cause difficulties for parents in the early years, however, the children themselves do not seem to experience markedly raised levels of psychological or developmental problems.
Key words: triplets/twins/ART/parenting/psychological development
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Introduction |
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One of the most dramatic consequences of the introduction of IVF and ICSI has been the high proportion of multiple births that arise from pregnancies produced by these 'high tech' assisted reproduction procedures. Figures for IVF/ICSI treatments initiated in 2002 in Europe show that the multiple delivery rate was 23.2% for twins and 1.3% for triplets (Nyboe Andersen et al., 2006
). Figures from the USA for treatments conducted in 2004 were higher, with a multiple delivery rate of 30% for twins and 3% for triplets (Centres for Disease Control, 2004). In Latin America, the multiple birth rate for assisted reproduction pregnancies in 2000 was 50%, with >13.5% of IVF and ICSI births involving triplets or quadruplets (Zegers-Hochschild, 2002). These figures are in sharp contrast to the multiple birth rate for naturally conceived pregnancies of around 1% (Bergh et al., 1999).
The increased risk of pre-term delivery, low birth weight and disability associated with multiple births (Goldberg and DiVitto, 2002; Olivennes et al., 2002; Helmerhorst et al., 2004; Ronalds et al., 2005; Verstraelen et al., 2005; Ombelet et al., 2006) has raised concerns that children's psychological development may also be adversely affected. Although the psychological development of singleton children conceived by assisted reproduction procedures such as IVF does not appear to differ from that of naturally conceived children (see van Balen, 1998; Golombok, 2006 for reviews), the outcome for assisted reproduction children born as part of a multiple birth remains less clear.
Most of the existing studies of multiple birth families have focused on families with twins rather than families with triplets. For parents, the birth of twins can result in high levels of stress and difficulties in family relationships (Thorpe et al., 1991; Bryan, 1992,2002; Segal, 1999; Lytton and Gallagher, 2002). Regarding the children, investigations of naturally conceived twins have shown that compared with singleton children twins do not show higher levels of emotional or behavioural problems, with the exception of a higher rate of attention problems (Van den Oord et al., 1995; Levy et al., 1996). However, the situation is somewhat different in relation to cognitive and language development. In comparison with singletons, twins have consistently been found to show delayed language development and to obtain lower scores on verbal IQ and reading tests (Hay et al., 1987; Rutter and Redshaw, 1991; Lytton and Gallagher, 2002). A recent, well-controlled study found that the language development of twins at age 3 years lagged 3 months behind that of singleton children, after excluding the most premature twins and those with neurological damage and after adjusting for the gestational age of the twins at birth (Rutter et al., 2003).
Findings relating to naturally conceived twins cannot necessarily be generalized to twins conceived by assisted reproduction as the mothers and fathers of IVF/ICSI twins appear to be more accepting of a multiple birth (Gleicher et al., 1995; Goldfarb et al., 1996; Murdoch, 1997; Ryan et al., 2004) which may have a positive impact on child outcomes. Nevertheless, similar results for IVF/ICSI and naturally conceived twins have been found. In a comparison between the cognitive development of IVF/ICSI twins and IVF/ICSI singletons using the Bayley Scales of Infant Development when the children were 2 years old, the twins obtained significantly lower scores than the singletons (Bonduelle et al., 2003). In addition, Olivennes et al. (2005) examined both the psychological adjustment and cognitive development of IVF/ICSI twins in comparison with a matched group of singletons. There were no differences in the level of emotional or behavioural problems between the twins and singletons. However, twins showed significantly lower levels of cognitive functioning than singletons, particularly in relation to language development and fine motor skills, a finding, i.e. consistent with earlier studies of naturally conceived twins. Thus, the greater acceptance of twins by couples undergoing assisted reproduction does not appear to ameliorate the cognitive delay associated with being a twin.
Although parents of triplets report high levels of stress, exhaustion and feelings of guilt about spending insufficient time with each infant, resulting in emotional distancing from them (Bryan 1992, 2002; Garel and Blondel, 1992; Garel et al., 1995, 1997; Ellison et al., 2005), there has been little systematic research on the psychological development of the triplets themselves, most of whom result from IVF/ICSI. In the only controlled study, 23 sets of triplets were followed up in comparison with 23 sets of twins and 23 singletons across the first 2 years of life. It was found that the task of raising three infants at the same time interfered with the quality of parents' interaction with their triplets at age 3 months as well as the security of the triplets' attachment to their mother at 1 year, and resulted in raised levels of emotional problems at 2 years old (Feldman and Eidelman, 2004). With respect to cognitive development, the triplets showed poorer cognitive competencies at age 1, as measured by the Bayley Scale of Infant Development and a standardized assessment of symbolic play, than did the singletons and twins (Feldman et al., 2004), and the same was also found at age 2 (Feldman and Eidelman, 2005). Similarly, Garel et al. (2001) reported a tendency towards greater cognitive impairment among triplets than singletons with a smaller sample at 7 years old.
The aim of the present study was to contribute to the small but growing literature on the nature and extent of difficulties in parenting and children's psychological development in a representative sample of assisted reproduction families with triplets in comparison with matched groups of assisted reproduction families with twins and assisted reproduction families with singletons. The investigation focused specifically on the psychological well-being of the parents and the socio-emotional and general development of IVF/ICSI children at age 3.
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Materials and Methods |
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Participants
The families were recruited from 'Follow-Up', a national organization in France established to follow-up children conceived by assisted reproduction. At the time of study, the Follow-Up database included >10 000 families recruited from 18 IVF clinics with a cooperation rate of >95%, and thus provided a highly representative sample of assisted reproduction families. The 12 clinics that had been participating for long enough to have children in the required age range were asked to take part in the present investigation. Of these, 10 clinics participated. One of the 12 clinics declined to take part and the other had an insufficient number of children of the required age.
As part of a larger study of 2–5-year-old children (Olivennes et al., 2005), questionnaires were completed by 367 IVF/ICSI families with twins and a comparison group of 958 IVF/ICSI families with a singleton child, representing response rates of 86 and 87%, respectively. For the purposes of the present study, 13 families with IVF/ICSI triplets aged 2–3 years old, representing all of the triplet families with children in that age range, were asked to participate in the research. Of these 13 families, 10 completed questionnaires representing a response rate of 77%. The 10 triplet families were matched to 15 families with twins and 30 families with singletons. Thus there were 30 children in each of the three family types. Matching was conducted on the basis of sex of the child, age of the child, age of the mother, age of the father, educational level of the mother, educational level of the father and number of siblings in the family. Families in which a child had a disability were excluded from the sampling process to avoid the potentially confounding effect of the child's disability on the outcome measures. The families with triplets, twins and singletons will be referred to as 'triplet families', 'twin families' and 'singleton families', respectively, for the sake of simplicity, although many of the target children in each family type had older and/or younger siblings. Ethical approval for the study was obtained from the Scientific Committee of Follow-Up who serve as an IRB.
As shown in Table 1, there were identical proportions of boys (n = 12) and girls (n = 18) in the three family types, and no differences between groups in the age of the children or the number of siblings in the family. The children were aged 3 years 3 months on average and all, but one child in the singleton group had a maximum of one sibling of a different age. In addition, there was no difference in the age of the mothers or the fathers, or in the educational level of the families as assessed by the mother's or the father's highest qualification.
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Measures
A questionnaire booklet comprising structured questions on demographic and family characteristics, standardized measures of the mother's psychological well-being (parenting stress, depression and quality of marriage) and standardized measures of the child's psychological development (emotional/behavioural problems and general development) was sent to mothers by post. Those mothers who had not returned the questionnaire booklet within one month received a reminder letter with a new questionnaire booklet. Fathers were not included as much of the information to be obtained concerned the child/children and such data are most reliably obtained from mothers who spend more time with their children than do fathers. In addition, the response rate for postal questionnaires to fathers is generally markedly lower than for mothers. The standardized measures were translated into French and then back-translated to English by a different translator to ensure that the meaning of the items had not been distorted in the translation process.
Mothers' psychological well-being
The short form (36 items) of the Parenting Stress Index (PSI/SF) (Abidin, 1990) was used to assess stress associated with parenting. The PSI/SF produces a total score, with higher scores reflecting greater parenting stress, as well as subscale scores of parental distress, parent–child difficult interaction and difficult child. A total score of 86 or above represents the 85th percentile. Test-retest reliability is 0.96 over a 1–3 month interval and 0.65 over 1 year. Concurrent and predictive validity have been demonstrated for the full-length questionnaire, and the short form has been reported to correlate very highly with the full-length version. Mothers completed this questionnaire once in relation to all of their children combined and not for each child individually.
The Edinburgh Depression Scale (Thorpe, 1993) was used to assess depression. This 10-item instrument, for which a higher total score represents greater depression, has good reliability and discriminates between clinical and non-clinical groups. A score of 10 or more indicates possible depression. The 10-item short form of the Golombok–Rust Inventory of Marital State (GRIMS) (Rust et al., 1990) was administered to assess the quality of the marital relationship with a higher total score representing poorer marital quality. Split-half reliability for the GRIMS is 0.87, and the GRIMS has been shown to discriminate significantly between couples who are about to separate and those who are not. In the present study, two additional items adapted from the Golombok–Rust Inventory of Sexual Satisfaction (GRISS) (Golombok and Rust, 1986) were included to assess sexual desire (‘I am not interested in sex’) and the frequency of sexual intercourse (‘Since the birth of our child/children we have sex less frequently’), respectively. These items were scored individually with a higher score representing greater sexual problems.
Children's psychological development
The presence of behavioural or emotional problems in the child was measured using the 25-item Strengths and Difficulties Questionnaire (SDQ) (Goodman, 1994, 1997). The SDQ produces a total score as well as subscale scores of emotional problems, conduct problems, hyperactivity, peer problems and prosocial behaviour. This questionnaire has been shown to have good inter-rater and test-retest reliability, and to discriminate well between children with and without psychiatric disorder.
The parental version of the Denver Developmental Screening Test (Denver II) (Frankenburg et al., 1992; Frankenburg and Bresnick, 1998) was completed by mothers to provide an assessment of the child's general development. The questionnaire comprised 20 items of which 11 assessed language development (combines words, names one picture, body parts, points to four pictures, speech half-understandable, names four pictures, knows two actions, knows two adjectives, names one colour, use of two objects and counts one), three assessed gross motor skills (jumps up, broad jump and balances), three assessed fine motor skills (tower of two cubes, imitates vertical line and thumb wiggle) and three assessed personal/social skills (puts on clothing, washes and dries hands and names friend). For each question, the mother reported whether or not her child was able to perform the task described, and a higher total score represented a higher level of development. The Denver II items have been demonstrated to have satisfactory inter-rater and test-retest reliability and good validity at different ages. In the present investigation, internal consistency was found to be 0.90.
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Results |
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Group comparisons of the questionnaire scores were conducted using one-way analyses of variance (ANOVAs). For those questionnaires that produced subscale scores (the PSI, the SDQ and the Denver II), multivariate analyses of variance (MANOVAs) were used to correct for inflated significance. ANOVAs were then performed on the individual subscale scores. Helmert contrasts then were carried out to establish (i) whether the children from a multiple birth differed from the singleton children, and (ii) whether the triplets differed from the twins. Due to the small sample size, non-significant trends in the findings are reported in addition to statistically significant results.
Mothers' measures
As shown in Table 2, there was a non-significant trend between the families for the mother's total score on the PSI (F = 2.72, P < 0.10). Contrast analysis showed a significant difference between the mothers of multiples and the mothers of singletons (P < 0.05) reflecting higher levels of parenting stress among the mothers with a multiple birth. However, the triplet mothers did not differ significantly from the twin mothers in levels of parenting stress. The subscale scores of parental distress, parent-child difficult interaction and difficult child were entered into a MANOVA. Wilks's 
showed a non-significant trend for parental distress (F = 2.49, P < 0.10), indicating a higher level of parent distress among the mothers of multiples than among the mothers of singletons (P < 0.05). There was no group difference for the parent–child difficult interaction or the difficult child subscales, although a non-significant trend towards higher parent–child difficult interaction was reported by the mothers of multiples than by the mothers of singleton children (P < 0.10).
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There was no significant difference between groups for the Edinburgh Depression Scale. Neither was there a difference in marital satisfaction between the family types as assessed by the GRIMS. With respect to the sexual relationship, there was a significant group difference in interest in sex (F = 3.22, P < 0.05), with the mothers of triplets reporting less interest in sex than the mothers of twins (P < 0.05). For frequency of sexual intercourse, there was a non-significant trend (F = 2.83, P < 0.10), reflecting a lower frequency of sexual activity among mothers of triplets and twins than among mothers of singletons.
Children's measures
There was no difference in the level of emotional or behavioural problems shown by triplets, twins and singletons as assessed by the total score of the SDQ (see Table 3). Neither was there a difference between family types in the proportion of children who obtained scores above cut-off for psychological disorder on this measure, with 10.7% of singletons, 10% of twins and 16.7% of triplets obtaining scores above cut-off. These proportions are in line with the expected rate of 10% for the general population and were not significantly different from each other. The subscale scores of emotional symptoms, conduct problems, hyperactivity, peer problems and prosocial behaviour were entered into a MANOVA. Wilks's was not significant.
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One-way ANOVAs showed no difference between family types for any of the individual subscales, although there was a non-significant trend for hyperactivity (F = 2.59, P < 0.01), reflecting greater hyperactivity among the twins than the triplets (P < 0.05).
With respect to general development as assessed by the total score of the Denver Developmental Questionnaire, no significant difference was found between groups. The individual item scores were then entered into a MANOVA and Wilks's showed a non-significant trend (F = 1.47, P < 0.10). One-way ANOVAs showed a significant difference between multiples and singletons for two items, and a non-significant trend for one item, each reflecting lower scores, i.e. poorer performance, among multiples than among singletons. Of these three items, all were language items: names four pictures (F = 3.96, P < 0.05), names one colour (F = 3.50, P < 0.05) and counts one (F = 2.87, P < 0.10).
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Conclusions |
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The findings of this investigation pointed to greater problems in parenting by mothers with a multiple birth than those of singleton children. However, the mothers of triplets and those of twins appeared to experience a similar level of difficulties to each other. Mothers with a multiple birth showed significantly higher levels of parenting stress than those of singletons. Although no differences in depression or marital satisfaction were found between mothers from the three family types, mothers of triplets reported less interest in sex than those of twins, and there was a trend towards a lower frequency of sex among mothers with a multiple birth. Thus greater problems in parenting were experienced by families with a multiple birth than by families with singletons, with no difference between mothers of triplets and mothers of twins, suggesting that a multiple birth produces problems for parents even with two children born at the same time. These findings replicate those of Garel and colleagues (Garel and Blondel, 1992
; Garel et al., 1995,1997) who reported high levels of parenting difficulties in a sample of mothers of triplets conceived by assisted reproduction and Olivennes et al. (2005) who found raised levels of problems associated with parenting in families with IVF/ICSI twins.
With respect to the children themselves, there was no difference in emotional or behavioural problems between triplets, twins or singletons. However, children of a multiple birth showed significantly poorer performance on some items relating to language development than did singleton children, with no differences between triplets and twins. Thus, in line with previous studies of both naturally conceived twins (Hay et al., 1987; Rutter and Redshaw, 1991; Lytton and Gallagher, 2002; Rutter et al., 2003) and IVF/ICSI twins (Olivennes et al., 2005), the children did not show raised levels of psychological problems but did appear to show some evidence of delayed language development. Different theoretical explanations have been proposed for the delayed language development shown by children of a multiple birth. Although biological factors may be involved (Goldberg and DiVitto, 2002), the existing evidence suggests that this results, to some extent at least, from reduced levels of interaction between the mother and each individual child (Rutter et al., 2003).
A limitation of the present investigation is the small sample of triplets studied and the resulting low level of statistical power, a problem associated with all existing studies of triplet families. However, the fact that statistically significant differences were found between families with a multiple birth and families with singleton children with these small sample sizes indicates that these effects are marked, especially as the mothers of multiples may have tended to under-report difficulties in their own or their children's psychological well-being as a result of the difficulties they experienced in becoming parents. It is also conceivable that larger sample sizes would show differences between families with triplets and families with twins. A further constraint of the present study was the reliance on questionnaire measures completed by the mothers regarding their own psychological state and their children's psychological development. Although the measures were selected on the basis of good reliability and validity, more detailed information could be acquired through face-to-face interviews with parents, the direct measurement of the children's socio-emotional and general development, and observational assessment of parent-child relationships. Due to the small sample size, all triplets and twins were included which may have resulted in bias associated with non-independence of the subjects. It is also important to note that only three of the eleven language items on the Denver II indicated language delay, of which only two reached statistical significance. Thus these findings should be taken to indicate possible language delay that warrants further investigation in other samples.
There has been growing pressure in recent years for fertility clinics to replace a maximum of two embryos when conducting IVF/ICSI in order to reduce the multiple birth rate, and there has also been a move towards the use of one embryo only (Geris and Van Royen, 2000; Vayena et al., 2002). The birth of triplets or twins does appear to cause difficulties for parents in the early years, and although the children themselves do not seem to experience raised levels of emotional or behavioural problems, in line with previous studies (e.g. Rutter et al., 2003) there are indications of mild delay in some aspects of language development. Whether or not this language impairment persists or ameliorates as the children grow up remains to be seen. It is important to note that the children in the present study were only 3 years old at the time of assessment. Thus it is essential that IVF/ICSI children born as part of a multiple birth are followed up through childhood to establish the psychological consequences in later years.
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Acknowledgements |
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We are grateful to all of the families who took part in this investigation. We would also like to thank the Follow-Up committee and the following participating clinics: centre Hospitalier, Poissy; Hopital Bichat, Paris; Clinique du Blanc Mesnil, Le Blanc Mesnil; Clinique Cherest, Neuilly; Clinique de la Muette, Paris; CMCO, Schiltigheim; CRES, Lyon; Clinique de la Dhuys, Bagnolet; Hopital les Diaconesses, Paris; Clinique Parly II, Le Chesnay.
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Submitted on December 22, 2006; resubmitted on April 10, 2007; accepted on April 20, 2007.
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