An overview of studies on psychological well-being in children born following assisted reproductive technologies

An overview of studies on psychological well-being in children born following assisted reproductive technologies first-author corresp ‡Corresponding Author ‡Corresponding Author †E-mail:jinfan@zju.edu.cn †E-mail:jinfan@zju.edu.cn jinfan@zju.edu.cn Department of Reproductive Endocrinology, Women’s Hospital, School of Medicine, Zhejiang University, Hangzhou 310006, China Department of Reproductive Endocrinology, Women’s Hospital, School of Medicine, Zhejiang University, Hangzhou 310006, China Over the course of the past 35 years, assisted reproductive technologies (ARTs) have been increasingly used worldwide, while debates on their safety have been generated. Birth defects and imprinting disorders were reported in previous research. Thus, the psychological development of children born following ARTs has become a major concern nowadays. This review gives a systematic view of psychological well-being of children conceived by different types of ART, including in vitro fertilization, intracytoplasmic sperm injection (ICSI), preimplantation genetic diagnosis/screening, and in vitro maturation. The previous studies are analyzed in three sections: (1) cognitive, motor, and language developments, (2) behavior problems and socio-emotional development, and (3) parent-child relationship. We conclude that although the majority of the studies on cognitive, motor, and language developments reported comparable achievements in the ART group vs. the naturally conceived group, lower intelligence quotient (IQ) scores, worse visual-motor ability or locomotor development, and delayed receptive language competence were found in the ART group. The results on the socio-emotional development were reassuring. As for the behavior problems, a higher prevalence of behavior problems existed in ART children; moreover, ICSI children were found to be at a higher risk of autism than the general population. Meanwhile, ART parents tended to have positive parental attitudes and be more protective of their children. Some suggestions for further research are also given in this review. Assisted reproductive technologies Psychological well-being Behavior problems Parent-child relationship Introduction 1 Worldwide, couples view infertility as “a tragedy which carries social, economic, and psychological consequences” (World Health Organization, 2010 2010 ). Since the first child conceived by in vitro fertilization (IVF) was born in Britain in 1978 (Steptoe and Edwards, 1978 1978 ), assisted reproductive technologies (ARTs), which cover IVF, intracytoplasmic sperm injection (ICSI), preimplantation genetic diagnosis/screening (PGD/PGS), in vitro maturation (IVM), and other technologies, have become widely-accepted medical treatments for human infertility. These interventions are scientifically innovative, and they have revolutionized concepts of generational identity, family, and human reproductive potential. According to the data from the Centers for Disease Control and Prevention of USA, the number of pregnancies obtained by ARTs has been steadily increasing. A total of 61 426 ART infants, over 1% of all infants, were born in the United States (Centers for Disease Control and Prevention et al., 2010 2010 ), but these children were not always accompanied by extensive follow-up programs. Thus, the clarity on potential psychological disorders after ARTs was in need of further evaluation. ARTs are supposed to be accompanied with an increase in psychological developmental problems for several reasons in our paper. Firstly, early development of the human nervous system is a complex and neatly orchestrated process which can be affected easily by invasive interventions like ARTs (de Graaf-Peters and Hadders-Algra, 2006 2006 ). Secondly, ARTs carry a significantly increased risk of multiple pregnancies, which are associated with a higher rate of prematurity and low birth weights, and carry increased neonatal intensive care admissions (Schieve et al., 2002 2002 ; Helmerhorst et al., 2004 2004 ; Jackson et al., 2004 2004 ; Fauser et al., 2005 2005 ; Basatemur and Sutcliffe, 2008 2008 ; Lu et al., 2013 2013 ). Thirdly, imprinted disorders, including Beckwith-Wiedemann syndrome, Angelman syndrome and Prader-Willi syndrome, and hyperthyrotropinemia tended to happen more frequently in the ART group than in the natural conception (NC) group (Cox et al., 2002 2002 ; DeBaun et al., 2003 2003 ; Gicquel et al., 2003 2003 ; Maher et al., 2003 2003 ; Halliday et al., 2004 2004 ; Chang et al., 2005 2005 ; Sutcliffe et al., 2006 2006 ). Previous reviews focused on subgroups of children, such as only on children born following IVF, or took into account only a part of the psychological development, e.g., neurodevelopment. Therefore, the aim of the present review is to try to give a systematic evaluation of psychological development of ART children. Here, we restricted ourselves to the techniques of IVF, ICSI, PGD/PGS, and IVM as a substantial number of follow-up studies had been reported before in these areas. In order to identify relevant articles, we conducted an extensive search using the databases PsycINFO, PubMed, and Web of Science, with the terms “assisted reproduction OR IVF OR ICSI OR PGD/PGS OR IVM” and “child development OR child psychology OR cognition OR language OR psychomotor OR motor skills OR intelligence OR behavior OR parenting”, which were chosen on the basis of preliminary exploratory literature searches and keywords in published studies. Potentially relevant studies were identified and screened based on title and abstract. We searched for articles published between 1995 and Oct. 9, 2012. Excluded from the search results were studies (1) which did not include a naturally conceived control group, (2) in which the follow-up did not figure out the conception type of ART; (3) not published in English. Two authors of this paper assessed titles, abstracts, full articles, and quality of the articles independently. Sample size, age of the children at evaluation, methods used in the assessments, and outcomes were also recorded. The scope of this research is broken down into three sections: (1) cognitive, motor, and language developments, (2) behavior problems and socio-emotional development, and (3) environment for development. Cognitive, motor, language developments 1 There are 21 reports of early psychological functioning in children born after assisted reproduction (Table 1 1 ), 14 of this reported data from ICSI children, 7 from IVF children, and 3 from children born after PGD which was developed for couples at the high risk of having a child with genetic disease. A=C, no statistically significant differences between ART group and control group; A>C, higher scores in ART group than in control group; A<C, lower scores in ART group than in control group Study Age of children ART group(s) Control group Method Outcome Banerjee et al., 2008 2008 4 years 49 PGD 66 Griffiths Scales of Mental Development (0‒8 years) (Griffiths, 1996 1996 ) Griffiths quotient: A=C; locomotor development: A < C ( p =0.0001); hearing language: A > C ( p =0.03) Gibson et al., 1998 1998 1 year 65 IVF 63 Bayley Scales of Infant Development, 2nd edition (BSID II) (Bayley, 1993 1993 ); Receptive-Expressive Emergent Language Test, 2nd edition (REEL-2) (Bzoch and League, 1991 1991 ) Mental & psychomotor development: A=C; competence of receptive language: A < C ( p =0.006) Golombok et al., 1996 1996 4‒9 years 116 IVF 120 Pictorial Scale of Perceived Competence & Social Acceptance for Young Children (Harter and Pike, 1984 1984 ) Cognitive competence: A=C Knoester et al., 2008 2008 5‒8 years 86 ICSI 85 Revised Amsterdam Child Intelligence Test (RAKIT; short form) (Bleichrodt et al., 1987 1987 ) Intelligence quotient (IQ): A < C ( p < 0.05) Koivurova et al., 2003 2003 1‒3 years 299 IVF 558 Age-Related Psychomotor Developmental Milestones Psychomotor development: A=C Leslie et al., 2003 2003 5 years 97 ICSI; 80 IVF 110 Wechsler Preschool and Primary Scales of Intelligence-Revised (WPPSI-R) (Wechsler, 1989 1989 ) IQ (full, verbal & performance): A=C Leunens et al., 2006 2006 8 years 151 ICSI 153 Wechsler Intelligence Scale for Children-Revised (WISC-R) (Wechsler, 1974 1974 ; van der Steene et al., 1986 1986 ); Movement Assessment Battery for Children (ABC) (Henderson and Sugden, 1998 1998 ) IQ (full, verbal & performance): A > C ( p < 0.05); motor development: A=C Leunens et al., 2008 2008 10 years 109 ICSI 90 WISC-R (Wechsler, 1974 1974 ; van der Steene et al., 1986 1986 ); Movement ABC (Henderson and Sugden, 1998 1998 ) IQ: A=C; balance skill: A > C ( p =0.044) Ludwig et al., 2009a 2009a 5.5 years 276 ICSI 273 Zimmer/Volkamer Motor Test (MOT; 4–6 years) (Zimmer and Volkamer, 1987 1987 ); Kaufman-Assessment Battery for Children (K-ABC) (Kaufman, 2001 2001 ) Neuromotor development: A=C; intelligence: A=C Mu et al., 2006 2006 6‒24 months 21 IVM 21 A general physical & neurological examination; BSID II (Bayley, 1993 1993 ) Growth: A=C; mental & psychomotor development: A=C Nekkebroeck et al., 2008a 2008a 2 years 70 PGD; 70 ICSI 70 BSID II (Dutch version) (van der Meulen et al., 2002 2002 ) Mental & psychomotor development: A=C Nekkebroeck et al., 2008b 2008b 3 years 41 PGD/S; 35 ICSI 53 McArthur Communicative Development Inventories (M-CDI) (Zink and Lejaegere, 2003 2003 ) Language development: A=C Papaligoura et al., 2004 2004 12 months 34 ICSI 29 BSID II (Bayley, 1993 1993 ) Mental & psychomotor development: A=C Place and Englert, 2003 2003 0‒5 years 66 ICSI 59 Standardized interviews with mother; Revised Brunet-Lézine Scale (Josse, 1997 1997 ); WPPSI-R (Wechsler, 1995 1995 ) Psychomotor & intellectual development: A=C Ponjaert-Kristoffersen et al., 2004 2004 5 years 296 ICSI 259 WPPSI-R (Wechsler, 1990 1990 ; 1999 1999 ); Peabody Developmental Motor Scales (PDMS) (Folio and Fewell, 2000 2000 ) IQ (full, verbal & performance): A=C; motor development: A < C ( p < 0.05) Ponjaert-Kristoffersen et al., 2005 2005 6 years 511 ICSI; 424 IVF 488 WPPSI-R (Wechsler, 1990 1990 ); McCarthy Scales of Children’s Abilities Motor Scale (MSCA) (McCarthy, 1972 1972 ) IQ (full, verbal & performance): A (IVF & ICSI)=C; motor development: A=C Sutcliffe et al., 1999 1999 12‒24 months 123 ICSI 123 Griffiths Scales of Mental Development-Revised (UK version) (Huntley, 1996 1996 ) Griffiths quotient: A=C; eye-hand coordination: A < C ( p < 0.05) Sutcliffe et al., 2001 2001 17 months 208 ICSI 221 Griffiths Scales of Mental Development-Revised (UK version) (Huntley, 1996 1996 ) Neurodevelopment: A=C Sutcliffe et al., 2003 2003 13‒15 months 58 ICSI 38 Griffiths Scales of Mental Development-Revised (UK version) (Huntley, 1996 1996 ) Neurodevelopment: A=C Wagenaar et al., 2008a 2008a 8‒18 years 233 IVF 233 The levels of the Dutch school system; a national test of educational achievement (CITO) School functioning: A=C Wagenaar et al., 2009b 2009b 9‒18 years 139 IVF 143 A national test of educational achievement (CITO); Trailmaking Test (Reitan, 1979 1979 ); Amsterdam Neuropsychological Tasks (ANT) (de Sonneville, 1999 1999 ); Beery-Buktenica Test for Visual Motor Integration, Visual Perception & Motor Coordination (Beery, 1989 1989 ; Beery and Buktenica, 1989 1989 ) General cognitive ability: A=C; information processing, attention: A=C; visual-motor function (visual perception, Purdue pegboard, & tapping task): A < C ( p < 0.05) Cognitive development 2 Children must find a way to understand, to remember, to solve problems, and to organize their environment. The method that leads to the maturation of their mental activity constitutes cognitive development. Cognition was assessed in 19 studies, and it was conceptualized most often in terms of the intelligence quotient (IQ), Griffiths quotient, mental or intellectual development, and cognitive competence. Most studies used standardized scales, and some used structured interviews (Table 1 1 ). Through an age-matched study, Knoester et al. ( 2008 2008 ) observed a slightly but significantly reduced IQ in 5- to 8-year-old children born after ICSI, though the mean IQ was within the normal range. Leunens et al. ( 2006 2006 ) also found a difference of IQ in 8-year-old ICSI children. However, their results are significantly increased for IQ compared with natural controls. In contrast, the follow-up study by Leunens et al. ( 2008 2008 ) revealed that the previously reported difference of cognitive development between children born after ICSI and NC had disappeared when they reached the age of 10 years. The result probably indicates that the effect of the maternal educational level or home environment decreased in the ICSI group over time. Similarly, there was no indication of a lower Griffiths quotient in ART vs. NC children in four papers (Sutcliffe et al., 1999 1999 ; 2001 2001 ; 2003 2003 ; Banerjee et al., 2008 2008 ) using the Griffiths Scales of Mental Development (Griffiths, 1996 1996 ; Huntley, 1996 1996 ). By means of the Bayley Scales of Infant Development (BSID) (Bayley, 1993 1993 ; van der Meulen et al., 2002 2002 ) or the Wechsler Intelligence Scales (WIS) (Wechsler, 1974 1974 ; 1989 1989 ; 1990 1990 ; 1995 1995 ; van der Steene et al., 1986 1986 ), neither delayed mental development nor worsening IQ scores between the ART children and the control group were found (Gibson et al., 1998 1998 ; Leslie et al., 2003 2003 ; Place and Englert, 2003 2003 ; Papaligoura et al., 2004 2004 ; Ponjaert-Kristoffersen et al., 2004 2004 ; 2005 2005 ; Mu et al., 2006 2006 ; Nekkebroeck et al., 2008a 2008a ). In addition, another four studies (Golombok et al., 1996 1996 ; Wagenaar et al., 2008a 2008a ; 2009b 2009b ; Ludwig et al., 2009a 2009a ) focusing on cognitive abilities found comparable achievement between the ART and NC groups by using the standardized test. The conclusion drawn is that there was only one report that presented a lower IQ score in the ART group, and the majority of the investigations showed similar cognitive development between the ART children and the control group. One possible reason for the different findings might be evaluation measurements, that is, the Revised Amsterdam Child Intelligence Test (RAKIT) (Bleichrodt et al., 1987 1987 ) was used by Knoester et al. ( 2008 2008 ), while the more widely-used scales such as BSID and WIS were used in other investigations. Sample size might also account for the different results as well. In the research of Knoester et al. ( 2008 2008 ), the sample size of ICSI children was relatively small, while in the research of Ponjaert-Kristoffersen ( 2005 2005 ), which used a well-matched and controlled design, the large sample size of ICSI children might potentially induce more reliable findings. Motor development 2 Two skills, locomotion and handedness, are acquired throughout the motor development process. Locomotion is the ability to navigate the environment, while handedness is the ability to reach and grasp objects (Benjamin et al., 2009 2009 ). Fourteen studies reported findings on motor development being assessed in terms of locomotor, psychomotor, neuromotor, balance skill, eye-hand coordination, and motor skills, with the help of common inventories, such as the Griffiths Scales of Mental Development (Griffiths, 1996 1996 ; Huntley, 1996 1996 ), BSID, and the Movement Assessment Battery for Children (ABC) (Henderson and Sugden, 1998 1998 ) (Table 1 1 ). On one hand, 10-year-old ICSI children were identified by Leunens et al. ( 2008 2008 ) to have higher balance skills than naturally conceived children. On the other hand, lower scores on eye-hand coordination in ICSI children and worsened visual-motor competence in IVF adolescents were observed, although these scores were still within the normal range (Sutcliffe et al., 1999 1999 ; Wagenaar et al., 2009b 2009b ). Ponjaert-Kristoffersen et al. ( 2004 2004 ) additionally presented a trend indicating that ICSI children did worse on motor development than spontaneously conceived children when they were at the age of 5 years, though selection bias, educational level, age of the mother, and cultural differences might account for the differences that were found. With regard to PGD children, worse achievement on locomotor was also found when they were at age of 4 years (Banerjee et al., 2008 2008 ). However, four investigations (Gibson et al., 1998 1998 ; Papaligoura et al., 2004 2004 ; Mu et al., 2006 2006 ; Nekkebroeck et al., 2008a 2008a ) found no differences of psychomotor development between the ART and NC groups by means of BSID. Similarly, Koivurova et al. ( 2003 2003 ) using the psychomotor developmental milestones and Place and Englert ( 2003 2003 ) using the Revised Brunet-Lézine Scale (Josse, 1997 1997 ) presented no differences between the ART and NC groups for psychomotor development. In another three reports (Ponjaert-Kristoffersen et al., 2005 2005 ; Leunens et al., 2006 2006 ; Ludwig et al., 2009a 2009a ) on motor development of ICSI children, there were also no worsening performances. In summary, worse visual-motor competence or delayed locomotor development was observed in the ART group, although more than half of the studies showed that motor development in the assisted group was similar to that in the natural group. The worse performance at early ages, but not at adolescence, might be induced by the higher rating of premature and lower birth weight in the ART group. Selection bias like educational level, age of the mother, and cultural differences might also partially account for the differences. Language development 2 Language refers to the ability to communicate as well as the capacity to use symbolic thought in the speech process, that is, to produce sounds and words. There have only been three investigations of the language development in the children born after ART (Table 1 1 ). The study of Gibson (1998) presented lower scores on receptive language skills in IVF infants. However, Banerjee et al. ( 2008 2008 ) reported higher hearing language development in children born following PGD. Another investigation (Nekkebroeck et al., 2008b 2008b ) found no differences between the two ART groups (PGD and ICSI) and the spontaneously control group, and both the ART groups were within the normal range. We can conclude that previous studies presented no worse performance on language development in the ART group as compared to the NC group, except for worse receptive language competence in IVF infants. Conception after embryo biopsy in the case of PGD and PGS had no adverse impact on language development compared with the natural control group. In general, lower IQ scores in the ICSI group were reported in one study, but fortunately, the majority of studies reported comparable achievement on cognitive development in the ART group vs. the NC group. Meanwhile, worse visual-motor competence or locomotor development was reported in the ART children, and delayed receptive language competence was found only in IVF infants. The higher rating of premature and lower birth weight in the ART group might accout for the worse performance, and the higher educational level and decent home environment might contribute to the better achievement. Based on the results in Table 1 1 , studies on motor and language developments only followed the children up to middle childhood, and long-term follow-up research is still in need as disorders may become more obvious after middle childhood. Socio-emotional development and behavior problems 1 There are 15 reports in children born after assisted reproduction in this section, 12 of these reports concerning IVF children, 5 concerning ICSI children, and 1 concerning PGD (Table 2 2 ). A=C, no statistically significant differences between ART group and control group; A>C, higher scores in ART group than in control group; A<C, lower scores in ART group than in control group Study Age of children ART group(s) Control group Method Outcome Barnes et al., 2004 2004 5 years 514 ICSI; 424 IVF 488 Difficult Child Subscale (DC) (Abidin, 1990 1990 ); Child Behavior Checklist (CBCL/4–18) (Achenbach, 1991a 1991a ) DC & CBCL: A (ICSI=IVF)=C Colpin and Bossaert, 2008 2008 15‒16 years 24 IVF 21 CBCL/4–18 (Achenbach, 1991a 1991a ); Youth Self-Report (YSR/11–18) (Achenbach, 1991b 1991b ) CBCL: A=C; psychosocial adjustment: A=C Colpin and Soenen, 2002 2002 8‒9 years 27 IVF 23 CBCL/4–18 (Achenbach, 1991a 1991a ); Teacher’s Report Form (TRF) (Achenbach, 1991b 1991b ) CBCL: A=C; total problem behavior from teachers: A > C ( p =0.06) Gibson et al., 1998 1998 1 year 65 IVF 63 Vineland Adaptive Behavior Scales (Sparrow et al., 1984 1984 ); Bayley Behavior Rating Scale (BRS) (Bayley, 1993 1993 ); Behavior Checklist (BCL) (Richman et al., 1982 1982 ) Social development: A=C; test-taking behavior: A=C; behavior problems: A > C ( p =0.005) Golombok et al., 1995 1995 4‒8 years 41 IVF 43 A standardized interview with the mother (Graham and Rutter, 1968 1968 ) Social and emotional adjustment: A=C Golombok et al., 1996 1996 4‒9 years 116 IVF 120 Rutter “A” Scale & “B” Scale (Rutter et al., 1970 1970 ; 1975 1975 ; Goodman, 1994 1994 ); Pictorial Scale of Perceived Competence and Social Acceptance for Young Children (Harter and Pike, 1984 1984 ) Socio-emotional development: A=C Golombok et al., 2001 2001 12 years 34 IVF 38 A standardized interview with the mother; Strengths and Difficulties Questionnaire (SDQ) (Goodman, 1994 1994 ; 1997 1997 ); Social Adjustment Inventory for Children and Adolescents (SAICA) (John et al., 1987 1987 ) School functioning: A=C; social and emotional adjustment: A=C Golombok et al., 2002 2002 11‒12 years 102 IVF 102 Child and Adolescent Functioning and Environment Schedule (CAFÉ) (John and Quinton, 1991 1991 ); SDQ (Goodman, 1994 1994 ; 1997 1997 ); SAICA (John et al., 1987 1987 ) School functioning: A=C; social and emotional adjustment: A=C; physical aggression: A < C ( p < 0.05) Golombok et al., 2009 2009 18 years 26 IVF 56 CAFÉ (John and Quinton, 1991 1991 ); Inventory of Peer and Parent Attachment (IPPA) (Armsden and Greenberg, 1987 1987 ); Symptoms Checklist-90-Revised (SCL-90-R) (Derogatis, 1994 1994 ); Self Perception Profile for College Students (Neemann and Harter, 1986 1986 ) Peer relationships: A=C; psychological problems: A=C; physical aggression: A > C ( p < 0.05); suspended or expelled from school: A > C ( p < 0.05); self-esteem: A < C ( p < 0.01) Knoester et al., 2007 2007 5‒8 years 87 ICSI; 92 IVF 85 CBCL/4–18 (Achenbach, 1991a 1991a ) Behavior disorders: ICSI=C; ICSI=IVF; autism: ICSI>general population Ludwig et al., 2009a 2009a 5.5 years 276 ICSI 273 Kaufman-Assessment Battery for Children (K-ABC) (Kaufman, 2001 2001 ) Emotional & behavioral development: A=C Nekkebroeck et al., 2008b 2008b 2 years 41 PGD/S; 35 ICSI 53 CBCL (Achenbach and Rescorla, 2000 2000 ) CBCL total problem & external problem: A < C ( p < 0.05) Ponjaert-Kristoffersen et al., 2004 2004 5 years 296 ICSI 259 CBCL (Achenbach and Edelbrock, 1983 1983 ; Verhulst et al., 1996 1996 ); DC (Abidin, 1990 1990 ) CBCL total problem & external problem: A < C ( p < 0.05); DC: A < C ( p < 0.05) Wagenaar et al., 2009a 2009a 9‒18 years 139 IVF 143 CBCL, TRF (Achenbach and Rescorla, 2001 2001 ) CBCL external and syndrome scale (thought problems & aggressive behavior): A < C ( p < 0.05); TRF: A=C Wagenaar et al., 2011 2011 11‒18 years 86 IVF 97 YSR (Achenbach and Rescorla, 2001 2001 ) Behavior problems & socio-emotional development: A=C Socio-emotional development 2 Once children have formed a sense of self, they can think about and interpret their experiences in other situations. That is the process of social development. Nine studies aimed to provide insight into the socio-emotional development of ART children compared with the spontaneously conceived control group (Table 2 2 ). There was only one report (Golombok et al., 2009 2009 ) that found lower self-esteem in adolescents born following IVF than in the control group. And the difference of self-esteem was not from a general tendency in IVF adolescents, as the result was not significant when excluding two outliers. The socio-emotional development was also assessed in terms of psychosocial adjustment and peer relationship in the other eight studies. All of the eight studies were in line with each other, in which the authors reported no differences between the groups. Taken together, the results were reassuring, that is, there were no significant differences between the ART children and control children regarding their socio-emotioanl development. Behavior problems 2 Behavior problems mainly include the internal and the external aspects. Problems such as withdrawn, somatic complaints, and anxious or depressed states comprise the internalizing aspect, and behaviors like rule breaking and aggression belong to the externalizing aspect. Thirteen studies reported on behavioral problems (Table 2 2 ). On one hand, a lower prevalence of behavioral problems, especially external problems, in the ART-conceived children were reported (Golombok et al., 2002 2002 ; Nekkebroeck et al., 2008b 2008b ; Wagenaar et al., 2009a 2009a ) according to Child Behavior Checklist (CBCL) (Achenbach and Rescorla, 2000 2000 ; Achenbach and Rescorla, 2001 2001 ) or Strengths and Difficulties Questionnaire (SDQ) (Goodman, 1994 1994 ; 1997 1997 ). Ponjaert-Kristoffersen et al. ( 2004 2004 ) found similar results indicating less problematic behavior in the ICSI group. However, variables such as cultural differences and selection bias were not excluded in the study. On the other hand, Gibson et al. ( 1998 1998 ) indicated that IVF mothers tended to report more children’s behavioral problems. The follow-up research performed by Golombok et al. ( 2009 2009 ) also revealed higher incidences of physical aggression and higher rates of being suspended or expelled from school in IVF adolescents than in the matched control group, which did not occur when they were teenagers (Golombok et al., 2002 2002 ). For further analysis of this research, the above described change in adolescence largely resulted from the behavior of two outliers rather than from the general performance of the IVF adolescents (Golombok et al., 2009 2009 ). In Colpin and Soenen ( 2002 2002 )’s research, marginally significant behavior problems were reported according to the Teacher’s Report Form (TRF) (Achenbach, 1991b 1991b ) in IVF children vs. the control group. However, according to the CBCL, the scores were similar in the two groups. It was interesting to consider why teachers’ ratings tended to show slight differences from parents’ ratings. First, social desirability might prevent IVF parents from observing or reporting disorders; second, it was possible that the IVF children had problems that manifested at school, but not at home. In addition, Knoester et al. ( 2007 2007 ) reported a higher prevalence of autism in ICSI-conceived children vs. the general population (3.4% vs. the general population ±0.3%) (Williams et al., 2006 2006 ). On the contrary, Barnes et al. ( 2004 2004 ), Colpin and Bossaert ( 2008 2008 ), and Wagenaar et al. ( 2011 2011 ) found no differences in self- or parent-reported behavioral problems between the ART children and NC children according to the CBCL or Youth Self-Report (YSR/11–18) (Achenbach, 1991b 1991b ). Meanwhile, neither Golombok et al. ( 2001 2001 ) nor Ludwig et al. ( 2009a 2009a ) reported any higher prevalence of behavioral problems in the ART children. In summary, there were two studies that reported more behavioral problems in the ART group than in the control group, and the majority of those studies found that the ART children perform similarly or were even less likely to be physically aggressive than the NC children. Additionally, a higher prevalence of autism in ICSI children was found, which warrants more research of high methodological quality and long-term follow-up. Overall, ART children were functioning well and did not differ from the NC children on the measures of socio-emotional development. Two studies found a higher prevalence of behavioral problems in ART children, but fortunately, most of the studies did not report more behavioral problems in the ART group vs. the control group. Meanwhile, ICSI children were reported to be at a higher risk of autism than the general population. Since the birth of the first ICSI child in 1992, children born after ICSI have just reached their adulthood. Follow-up research of ICSI-conceived children, consequently, becomes an urgent need. Environment for development 1 The home environment of ART families was assessed in 14 studies in terms of parent-child interaction, parent-child relationship, parenting style, and attachment. Eleven of these studies provided data on IVF families, 3 on ICSI families, and 1 on a PGD family (Table 3 3 ). A=C, no statistically significant differences between ART group and control group; A>C, perform significantly better or more in ART group than in control group; A<C, perform significantly worse or less in ART group than in control group Study Age of children ART group(s) Control group Method Outcome Banerjee et al., 2008 2008 4 years 49 PGD 66 Parental Acceptance Rejection Questionnaire (Rohner and Khaleque, 2005 2005 ) Warmth-affection to child: A > C ( p =0.042); aggression-hostility and rejection: A < C ( p =0.03) Barnes et al., 2004 2004 5 years 514 ICSI 488 Parent-Child Dysfunctional Interaction Subscale (P-CDI) (Abidin, 1990 1990 ); Parental Acceptance-Rejection Questionnaire (PARQ) (Rohner, 1999 1999 ) Difficulties in the relationship: A=C; mother’s negative feeling to child: A < C ( p =0.0001); father’s response: A=C Colpin et al., 1995 1995 24‒30 months 31 IVF 31 Rating Scales for Structured Tasks (Erickson et al., 1985 1985 ); Questionnaire for Parental Attitudes and Emotions (Engfer and Schneewind, 1976 1976 ) Parent-child relationship: A=C Colpin and Bossaert, 2008 2008 15‒16 years 24 IVF 21 Louvain Adolescent Perceived Parenting Scale (LAPPS) (Soenens et al., 2004 2004 ) Parenting style: A=C Colpin and Soenen, 2002 2002 8‒9 years 27 IVF 23 Nijmegen Child-Rearing Questionnaire-adapted version (NCRQ) (Gerris et al., 1996 1996 ); Questionnaire Parenting Goals (QPG) (Gerris et al., 1993 1993 ) Parenting goal of adjustment: A > C ( p =0.03) Knoester et al., 2007 2007 5‒8 years 87 ICSI; 92 IVF 85 Dutch Children TON AZL Quality of Life questionnaire (Dux 25); TNO AZL Child Quality of Life questionnaire (TACQoL) (Theunissen et al., 1998 1998 ; Vogels et al., 1998 1998 ; Verrips et al., 1999 1999 ) Quality of life: A=C Gibson et al., 2000 2000 1 year 65 IVF 61 Strange Situation procedure (SS) (Ainsworth et al., 1978 1978 ); Emotional Availability Scales (Biringen et al., 1993 1993 ) Attachment: A=C; mother-child interaction: A=C Golombok et al., 1995 1995 4‒8 years 41 IVF 43 A standardized interview with the mother (Graham and Rutter, 1968 1968 ); questionnaire for parents Mother’s warmth to child & emotional involvement: A > C ( p < 0.01); parent-child interaction: A > C ( p < 0.05) Golombok et al., 1996 1996 4‒9 years 116 IVF 120 A standardized interview with the mother (Quinton and Rutter, 1988 1988 ); Family Relations Test (Bene and Anthony, 1985 1985 ) Mother’s warmth & emotional involvement: A > C ( p < 0.01); father-child interaction: A > C ( p < 0.01); quality of family relationship & parenting: A=C Golombok et al., 2001 2001 12 years 34 IVF 38 A standardized interview with parents; Child and Adolescent Functioning and Environment Schedule (CAFÉ) (John and Quinton, 1991 1991 ); Expression of Affection Inventory (EAI) (Hetherington, 1992 1992 ); Conflict Tactics Scale (CTS) (Straus, 1979 1979 ) Warmth: A > C ( p < 0.05) Golombok et al., 2002 2002 11‒12 years 102 IVF 102 A standardized interview with parents; CAFÉ (John and Quinton, 1991 1991 ); EAI (Hetherington, 1992 1992 ); CTS (Straus, 1980 1980 ) Warmth: A > C ( p < 0.01); criticism & discipline: A < C ( p < 0.05) Golombok et al., 2009 2009 18 years 26 IVF 56 CAFÉ (John and Quinton, 1991 1991 ); Inventory of Peer and Parent Attachment (IPPA) (Armsden and Greenberg, 1987 1987 ) Warmth & control: A=C Owen and Golombok, 2009 2009 18 years 26 IVF 63 A standardized interview; parent-adolescent warmth scale Mother’s warmth: A > C ( p < 0.05); mother’s control & discipline: A < C ( p < 0.05); father’s response: A=C Ponjaert-Kristoffersen et al., 2004 2004 5 years 296 ICSI 259 P-CDI (Abidin, 1990 1990 ) Parent-child dysfunctional interaction: A < C ( p < 0.05) In the research of Banerjee et al. ( 2008 2008 ) and Golombok et al. ( 2001 2001 ; 2002 2002 ), ART parents showed more positive feeling (i.e., warmth and affection to children) and less negative feeling (i.e., aggression and hostility to children) than naturally conceived children’s parents. It was notable that these feelings were especially true for mothers (Golombok et al., 1995 1995 ; 1996 1996 ; Barnes et al., 2004 2004 ; Owen and Golombok, 2009 2009 ). Moreover, a lower rating of discipline in IVF parents vs. NC parents was reported (Golombok et al., 2002 2002 ; Owen and Golombok, 2009 2009 ). Nevertheless, ART parents expected their children, more than naturally conceived children’s parents, to adjust to their own and others’ expectations (Colpin and Soenen, 2002 2002 ). As for the parent-child interaction, more healthy interactions in IVF families and less dysfunctional interactions in ICSI families were indicated vs. their control group (Golombok et al., 1995 1995 ; 1996 1996 ; Ponjaert-Kristoffersen et al., 2004 2004 ). In contrast, neither Gibson et al. ( 2000 2000 ) nor Golombok et al. ( 2009 2009 ) reported that warmth to child or attachment in IVF families differed from that in NC families. Quality of life, parent-child relationship, or parenting style of the ART families was also similar to that of NC families. The explanation for the absence of differences might be that, nowadays, for some couples, NC is also as heavily planned as assisted conception; meanwhile, ART has become a widely used and accepted reproduction technique. In brief, the parent-child relationship serves as the first context for the developments of cognition, language, social, and moral values. The vast majority of the data above suggested that ART parents, especially ART mothers, showed positive parental attitudes and more protection to their children throughout their development. Duncan and Edwards ( 1999 1999 ) also identified that ICSI mothers, but not fathers, were more committed to being a parent than the naturally conceived children’s mothers, which, to a certain extent, explained the mothers’ performances. In addition, reviews of issues on psychological impact of ART suggested that firstly the inability to conceive children was experienced as a stressful situation by individuals and couples, and secondly, parents who conceived using ART experienced additional stress and anxiety during the assisted conception procedure (Cousineau and Domar, 2007 2007 ; Basatemur and Sutcliffe, 2008 2008 ). Either of them might affect adaptation to the parental role, influence how parents view their children, and then affect the child-parent relationship and child development. Conclusions 1 First of all, although the majority of the studies on cognitive, motor, and language developments reported comparable achievement in the ART group vs. the NC group, different performances between the two groups also existed. Lower IQ scores in the ICSI group were reported in one study, and worse visual-motor ability or locomotor development and delayed receptive language competence were found in the ART group as well. Then, the results on socio-emotional development were reassuring. With regard to behavioral problems, two studies found a higher prevalence of behavioral problems in ART children; moreover, ICSI children were found to be at a higher risk of autism than the general population. Finally, the vast majority of the data on home environment suggest that ART parents, especially ART mothers, show positive parental attitudes and more protection of their children throughout their development. Suggestions in further researches 1 Previous reviews stated that potential problems of ART children perhaps emerged during adolescence, and therefore, continuing follow-up is undoubtedly recommended to make sure that ART children continue to do well (Basatemur and Sutcliffe, 2008 2008 ; Izat and Goldbeck, 2008 2008 ; Middelburg et al., 2008 2008 ; Wagenaar et al., 2008b 2008b ). Some studies have been conducted to estimate the psychological well-being of IVF children who were close to their 18th birthday (Wagenaar et al., 2008a 2008a ; 2009a 2009a ; 2009b 2009b ; Golombok et al., 2009 2009 ; Owen and Golombok, 2009 2009 ), but, till now, few have focused on adolescent born following other technologies, such as ICSI, PGD/PGS, or IVM. Besides, the higher risk of autism reported in ICSI children calls for more research and long-term follow-up. It was estimated that the blinded examiners in ART studies could intuit the mode of conception in three out of four children. 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Y2100822 and LZ13H040001) 2013-04-04 2013-10-22 2013-07-14 2022-01-05 Copyright © Zhejiang University and Springer-Verlag Berlin Heidelberg 2013 2013 Journal of Zhejiang University-SCIENCE B (Biomedicine and Biotechnology) 11 14