Neuromotor, cognitive, language and behavioural outcome
in children born following IVF or ICSI–a systematic review
K.J. Middelburg1,5, M.J. Heineman2,3, A.F. Bos4and M. Hadders-Algra1
1Department of Paediatrics, Division of Developmental Neurology, University Medical Center Groningen, Hanzeplein 1, 9713 GZ
Groningen, The Netherlands;2Department of Obstetrics and Gynaecology, University Medical Center Groningen, Groningen, The
Netherlands;3Department of Obstetrics and Gynaecology, Academic Medical Center, Amsterdam, The Netherlands;4Department of
Paediatrics, Division of Neonatology, University Medical Center Groningen, Groningen, The Netherlands
5Correspondence address. Tel: þ31-50-3614247; Fax: þ31-50-3615918; E-mail: firstname.lastname@example.org
BACKGROUND: The effect of in vitro fertilization (IVF) or intracytoplasmic sperm injection (ICSI) on the
developing human brain is unclear. The objective of this study is to evaluate neurodevelopmental (ND) outcome
of children born following these techniques. METHODS: This systematic review includes studies which compare
a group of children born following IVF/ICSI to children born after natural conception by assessing outcome in
terms of neuromotor development, cognition, speech/language and behaviour. Specific attention is paid to the
studies’ methodological quality based on study design, attrition, blinding of the assessor, validity of ND tests used,
confounders included and group size or power analysis. RESULTS: Twenty-three out of 59 studies had a good meth-
odological quality including 9 register-based (RB) and 14 controlled studies. RB studies suggested that IVF/ICSI per
se does not increase the risk for severe cognitive impairment (i.e. mental retardation) or neuromotor handicaps such
as cerebral palsy (CP), the association of IVF/ICSI and CP being brought about by the association of assisted con-
ception with risk factors, like preterm birth. In general, controlled studies of good quality did not report an excess of
ND disorders in IVF/ICSI-children. However, the majority of studies followed the children during infancy only,
thereby precluding pertinent conclusions on the risk of ND disorders that come to the expression at older ages,
such as fine manipulative disability or dyslexia. CONCLUSIONS: A negative effect of assisted conception on the
developing human brain is not identified; however, further research of high methodological quality in children
beyond pre-school age is needed.
Keywords: children; follow-up; ICSI; IVF; neurodevelopmental outcome
The effect of assisted conception on the developing human brain is
still not clear, notwithstanding the fact that in vitro fertilization
(IVF) and intracytoplasmic sperm injection (ICSI) have been
introduced more than 25 and 15 years ago, respectively (Steptoe
and Edwards, 1978; Palermo et al., 1992). Since then many
studies have been conducted on neurodevelopmental outcome
(an umbrella term covering neuromotor, cognitive, speech/
language and behavioural outcome) of children born following
these techniques but hitherto uncertainties persist. For instance,
contradicting results have been reported considering the associ-
ation between assisted conception and cerebral palsy (CP), which
is a neuromotor disorder that is attributed to non-progressive dis-
turbances in the developing brain (Bax et al., 2005). Some studies
report an association between assisted conception and CP (Ericson
et al., 2002; Lidegaard et al., 2005; Stro ¨mberg et al., 2002),
whereas others could not demonstrate such association (Pinborg
et al., 2004; Ka ¨lle ´n et al., 2005; Hvidtjørn et al., 2006; Klemetti
et al., 2006). The lack of clarity on potential neurodevelopmental
risk after IVF/ICSI is worrying for multiple reasons. First, the
number of pregnancies obtained by an assisted reproductive tech-
nology (ART) is steadily increasing. In Europe, up to 3.9% of
national births are infants born after ART (Nyboe Andersen
et al., 2007). Moreover, new and more invasive techniques are
introduced at a rapid pace and are not always accompanied by
extensive follow-up programmes.
Furthermore, there might be reasons to suppose that IVF/ICSI
is associated with an increase in neurodevelopmental problems.
Early development of the human nervous system is a comp-
lex and neatly orchestrated process which can be affected easily
by external influences (De Graaf-Peters and Hadders-Algra,
2006). It has already been established that perinatal outcome of
singletons born after assisted conception is worse than that of
naturally conceived singletons. Artificially conceived singleton
pregnancies end significantly more often preterm and with
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Human Reproduction Update, Vol.14, No.3 pp. 219–231, 2008
Advance Access publication March 26, 2008
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low birth weight (Schieve et al., 2002; Helmerhorst et al., 2004;
Jackson et al., 2004) and perinatal mortality and neonatal
intensive care admission are increased (Helmerhorst et al., 2004;
Jackson et al., 2004).
The lack of consensus about neurodevelopmental risk after
IVF/ICSI largely stems from the fact that the results of the
various follow-up studies often are difficult to interpret
because of methodological shortcomings. Previous reviews
mentioned methodological drawbacks but lacked a thorough
methodologicalevaluation (Van Balen, 1998; Buitendijk,
1999; Tarlatzis and Grimbizis, 1999; Olivennes et al., 2002;
Sutcliffe and Ludwig, 2007). Others focused on subgroups of
children, e.g. twins (Pinborg, 2005), children born following
ICSI (Van Steirteghem et al., 2002; Leslie, 2004), or children
born following cryopreservation of embryos (Sutcliffe, 2000;
Wennerholm, 2000), or took into account only a part of
neurodevelopmental outcome, such as psychosocial well being
(Hahn, 2001; Colpin, 2002; Golombok and MacCallum, 2003;
Gibson and McMahon, 2004). Therefore, the aim of the
present review is to evaluate in a systematic manner studies
on neurodevelopmental outcome of children born following
IVF or ICSI compared to naturally conceived children. We
restricted ourselves to the techniques of IVF and ICSI as the
character of these procedures is invasive and a substantial
number of follow-up studies have been reported. For the still
more invasive techniques, such as preimplantation genetic
screening and in vitro maturation, follow-up information is
almost completely lacking. We first evaluated the methodologi-
cal quality of the studies in a strict and standardized way.
The identified studies of good methodological quality are
summarized and the results are presented and discussed in an
An extensive literature search was performed for relevant studies
on neurodevelopmental outcome of children born following IVF
or ICSI. We searched for articles published between 1978 and 5
December 2007 in Medline, Embase (since its first coverage
year: 1989), PsycINFO and the Cochrane library. A computer
based search strategy with multiple combinations of terms was
entered into the databases. This search strategy consisted of all
combinations of (i) IVF OR ICSI OR reproductive techniques,
assisted OR fertilization in vitro AND (ii) child development
OR abnormalities OR morbidity OR psychomotor performance
OR motor skills OR intelligence OR child psychology OR child
behaviour OR developmental disabilities OR nervous system dis-
eases OR CP AND (iii) infant(s) OR child(ren) OR adolescent(s)
OR twins OR triplets. Note that the terms were adapted to termi-
nology used in the various databases. In addition, the reference
lists of all identified studies and review articles were reviewed
for additional articles.
Inclusion and exclusion criteria
We searched for all studies which assessed neurodevelopmental
outcome, i.e. neuromotor development, cognition, speech/language
and behaviour as a primary outcome measure in IVF or ICSI
children and a naturally conceived comparison group. Excluded
from the study were studies (i) which did not include a naturally
conceived control group, (ii) with a study group size of less than
25 children, (iii) in which the follow-up did not extend beyond
the neonatal period, (iv) in which the study group included more
than 10% of children born following ovulation induction only
(without IVF or ICSI), (v) which compared outcome of children
born following IVF or ICSI to children born from donor gametes,
adopted children or children born from surrogate mothers and
(vi) not published in English. The decision to exclude studies
with a group size of less than 25 children was based on preliminary
results which revealed that a small group size virtually always was
only included when a substantial part of the study was devoted to
the child’s neurodevelopmental outcome.
The search strategy yielded 1131 publications in Medline and
Embase, 213 in PsycINFO and 181 in the Cochrane library.
These were supplemented with articles found in reference lists.
On the basis of abstract and title, 115 potentially relevant articles
were identified and screened for retrieval. Fig. 1 shows a flow-
diagram of the in and excluded studies, with reasons for exclusion.
The manuscripts of the studies included in the systematic review
were read in full by two independent reviewers (M.H-A. and
K.J.M.). Study characteristics, data qualifying methodology and
data on outcome were extracted and discussed until consensus
Studies evaluating outcome after IVF/ICSI do not allow for a ran-
domized clinical trial (Buck Louis et al.,2005). The best option for
a clinical trial is the design which evaluates outcome in prospec-
tive cohorts of consecutively born IVF/ICSI children and natu-
rally conceived controls, both recruited pre- or perinatally. Next
best approaches are studies in which IVF/ICSI children are
studied prospectively as a cohort, but the naturally conceived
controls are matched retrospectively at nursery- or school age.
In order to enhance the ability to fine grade the quality of
IVF/ICSI studies, we therefore made the differentiation between
prospective- and retrospective-cohort studies (respectively, PC
and RC) according to the enrollment of the control children.
Studies, which included IVF/ICSI children whose selection was
not clearly defined, i.e. studies in which it was not clear whether
the children studied represented the entire population of a region
or a centre, were classified as retrospective cohort. Studies
which included children with a disorder or disease (e.g. CP) and
evaluated the mode of conception of children in the diseased
and non-diseased groups were classified as case–control (CC).
The effect of IVF/ICSI has not only been studied in clinical
trials, but also in studies based on nation-wide registers. These
register-based (RB) studies are in particular valuable to detect dis-
orders of low incidence, like CP. Hierarchically, RB studies were
considered as having the same level of evidence as the PC studies.
Attrition is an important problem in follow-up studies. We
classified studies according to their degree of post-natal attrition.
This means that attrition due to perinatal mortality is not taken
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January 17, 2008
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