Ultrasound Obstet Gynecol 2011; 37: 290–295 Published online in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/uog.8882
Neurodevelopmental outcome following prenatal diagnosis of an isolated anomaly of the corpus callosum R. MANGIONE*, N. FRIES*, P. GODARD*, C. CAPRON†‡, V. MIRLESSE*§, D. LACOMBE¶ and M. DUYME†‡ *Coll`ege Fran¸cais d’Echographie Fœtale (CFEF), France; †University of Montpellier 3, Montpellier, France; ‡CNRS, University of Montpellier1-Nˆımes, Montpellier, France; §Maternity Bichat, Paris, France; ¶Department of Medical Genetics, University of Bordeaux 2, CHU Bordeaux, Bordeaux, France
K E Y W O R D S: corpus callosum anomaly; neurological development; outcome; parental questionnaire; prenatal diagnosis
ABSTRACT Objectives To assess the ability of prenatal ultrasound and magnetic resonance imaging (MRI) to diagnose isolated anomalies of the corpus callosum (ACC) and to further document the long-term prognosis following diagnosis. Methods This was a prospective case–control study carried out between 1999 and 2004. Diagnosis was made by a combination of ultrasound and MRI. All infants were examined by a neuropediatrician and parents consented to answer questionnaires (CDI, Ireton’s Child Developmental Inventory) in 22 cases, which were matched with 44 control infants. The CDI was used to assess neurodevelopmental outcome in cases and controls. Mean DQ-CDI (development quotient calculated from CDI) values and frequencies of abnormal results were compared between groups, and a meta-analysis of previous studies was performed. Results The diagnosis of ACC was made prenatally and confirmed postnatally in 175 cases. The diagnosis was thought to be isolated ACC in 88/175 (50%) cases. Sixty of these 88 cases (68%) underwent termination of pregnancy and one died in utero. Twenty-seven were liveborn, of which 26 were followed up for a median of 50 (range, 30–74) months. Additional anomalies were diagnosed postnatally in four (15%) of these 26 neonates. The control group was significantly better (P < 0.05) compared with the cases diagnosed prenatally with isolated ACC with respect to gross motor, fine motor, language comprehension, numbers and general development, and it was marginally better for letters (P = 0.066). Seven of 26 (27%) (95% CI, 13–46%) infants with ACC over the age of 30 months had
neurodevelopmental delay, compared with only one case with borderline developmental delay among the 44 controls (P = 0.006). Conclusion Prenatal diagnosis of ACC by a combination of ultrasound and MRI is reliable. However, the isolated nature of the anomaly could only be assessed in 85% of our cases. Since counseling is provided at the time of prenatal diagnosis, our population of isolated ACC included the cases that were missed prenatally as being ACC with associated anomalies. A meta-analysis of nine studies suggests that the development of children diagnosed prenatally with isolated ACC is normal in up to 70% (CI 95%, 56–83%) of cases. This means that the prospective risk of neurodevelopmental delay for a fetus with ACC described as isolated prenatally is 27%, compared with 15% for an infant whose diagnosis of isolated ACC is confirmed postnatally. Copyright 2011 ISUOG. Published by John Wiley & Sons, Ltd.
INTRODUCTION The corpus callosum (CC) is the main interhemispheric commissure and is responsible for the transfer of motor, sensorial and cognitive information between the two brain hemispheres. Anomalies of the CC (ACC) include complete and partial agenesis as well as hypoplasia1 . The prevalence of ACC, which is difficult to assess in the general population due to recruiting bias, ranges from 1.8 to 7 per 10 000 births within population-based registries of birth defects, but is up to 2–3% in neuropediatric populations2 – 5 . ACC can be isolated or associated with other cerebral and extracerebral abnormalities, including chromosomal anomalies and genetic syndromes. They
Correspondence to: Dr R. Mangione, Polyclinique Bordeaux Nord Aquitaine, Department of Women Imaging, 15 rue Claude Boucher, 33000 Bordeaux, France (e-mail:
[email protected]) Accepted: 27 October 2010
Copyright 2011 ISUOG. Published by John Wiley & Sons, Ltd.
ORIGINAL PAPER
Anomaly of corpus callosum and neurodevelopment could also result from fetal infections or in-utero exposure to teratogens3 – 7 . ACC may be amenable to prenatal diagnosis based on direct and indirect signs on prenatal ultrasound from 20 weeks onwards7,8 . The prenatal diagnosis of hypoplasia and partial agenesis is more difficult than that of complete agenesis, but is feasible by targeted sonography9 . Although each type of ACC is likely to reflect a distinct malformative spectrum, they seem to share the same neurodevelopmental prognosis when they are isolated6,9 . In the presence of associated anomalies, the prognosis depends largely on these anomalies and whether they lead to severe mental and psychomotor retardation4,6,10 – 12 . However, even in isolated ACC a wide range of outcomes has been reported, from completely normal4,13,14 to severely impaired7,12 neurodevelopment, through to epilepsy or behavioral disorders15,16 . This heterogeneity can be explained at least in part by the difficulty in confirming the isolated nature of ACC prenatally, the small size of usually retrospective studies and the lack of standardization in the follow-up of affected infants7,8,17,18 . The reported percentage of liveborn children with ACC and with a normal outcome varies, therefore, between 25% and 100% (Table 1). We aimed to assess the ability of prenatal ultrasound and magnetic resonance imaging (MRI) to diagnose isolated ACC and to further document the long-term prognosis following diagnosis. We reviewed the neurodevelopmental outcome of affected children between 30 months and 6 years of age in order to contribute further to the cumulative but still limited evidence in the literature (Table 1)4,6 – 8,14,17,19 – 21.
SUBJECTS AND METHODS This prospective case–control study was carried out between 1999 and 2004 by the Coll`ege Fran¸cais d’´echographie Fœtale (CFEF). The CFEF is a national network of perinatal ultrasonologists, each of whom performs more than 1000 prenatal examinations every year. There were 37 participating centers which, during the study period, reported prospectively into a central database all cases of ACC suspected antenatally as well as pre- and postnatal management of these cases. The diagnosis was made by a combination of ultrasound from 20 weeks’ onwards and prenatal MRI performed at around 32 weeks of gestation in all cases continuing with the pregnancy. The diagnosis was reassessed postnatally by transfontanellar ultrasound. The isolated nature of the ACC was defined by the absence of other neurological (including ventriculomegaly > 15 mm) and extraneurological anomalies observed on a detailed prenatal morphological ultrasound examination, as well as on MRI carried out at around 32 weeks and standard karyotype testing. Postnatally, we considered that the ACC was isolated when there was no morphological, chromosomal or genetic anomaly discovered during the examination carried out just after birth. All infants were examined by a neuropediatrician and parents consented to answering questionnaires (French
Copyright 2011 ISUOG. Published by John Wiley & Sons, Ltd.
291
translation of the CDI, Ireton’s Child Developmental Inventory22 ) in 22 cases. In addition, each of these infants was matched postnatally for age, gender and socioeconomic status with two control infants. This control group consisted of children who did not present with any pre- or postnatal anomaly, selected from a national population-based study focusing on child neurodevelopment using the CDI22 . The control group was created during the same period as that during which the ACC cases were being collected22 .
Outcome measures The CDI23,24 is one of the parental questionnaires recommended by the American Academy of Pediatrics25 , and has both high sensitivity (80–100%) and high specificity (94–96%) for screening for severe as well as borderline neuropsychological disorders26 – 28 . In addition, the CDI is an assessment level tool designed to be used in children whose neuropsychological development is either questionable or delayed24 . From it, a development quotient, the DQ-CDI, is calculated. The French version of the CDI has a sensitivity of 84% and specificity of 92%, and the DQ-CDI correlates well with the IQ WPPSI test (Wechlser preschool and primary scale of intelligence, intelligence quotient) (r = 0.85)22 . The CDI consists of a set of statements describing the child’s behavior. The parent must tick ‘Yes’ or ‘No’ for each statement in the answer grid according to what his child does or does not do. Each ‘Yes’ answer scores 1 point, and the score obtained for each scale is calculated by totalling the number of points. Scores were then transformed into developmental age according to French normal values22 and then into the DQ-CDI, defined as development age/chronological age × 100. As for the IQ WIPPSI29 , the average was 100 and the SD was 15 for the general population. The 10th percentile for the DQ-CDI was 80. Developmental delay was defined as DQ-CDI < 79, with borderline retardation defined as DQ-CDI between 79 and 70 and mental retardation defined as DQ-CDI < 7029 .
Statistical analysis Mean DQ-CDI values were compared between the ACC and control groups by ANOVA (analysis of variance) and the Yates corrected chi-square test was used for comparisons of frequencies of abnormal results. A metaanalysis of previous studies was carried out using Stats Direct software (version 2.7.3) (StatsDirect Ltd, Cheshire, UK) (Table 1).
RESULTS During the study period, the diagnosis of ACC was suspected prenatally in 175 cases on ultrasound and MRI; their outcome is summarized in Figure 1. The diagnosis was confirmed postnatally in all cases by transfontanellar
Ultrasound Obstet Gynecol 2011; 37: 290–295.
Mangione et al. 5/7; 71 (29–96) 23/27; 85 (48–98) 1/4; 25 (8–90) 13/16; 81 (30–92) 6/9†; 66 4/7; 57 6/8; 75 (35–97) 6/6; 100 (56–100) 3/3; 100 (56–100) 3/7; 43 (10–81) 11/20; 55 (31–77) 19/26; 73 (54–86) 0 5 0 By 2 years: 1 By 4 years: 8 By 6 years: 10 1 0 0 8 0 0 2 y (6 m–8 y) 29 m (birth–11 y) 4 y (2–7 y) 4 y (2–8 y)
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0 0 0 19 NA 60 19 1 0 When necessary 16 27 9 6 3 15 20 27 Volpe et al.8 (2006) Pisani et al.4 (2006) Ramelli et al.14 (2006) Fratelli et al.7 (2007) Chadie et al.6 (2008) This study
19 9 3 117 20 175
1 0 0 0 4 4
NA NA 14 17 7 30 4 17 14 70 14 17 Vergani et al.20 (1994) Gupta and Lilford21 (1995)* Rapp et al.17 (2002) Moutard et al.19 (2003)
Reference
Liveborn
2 3 2 0
Prenatal MRI performed ( n) Diagnosed non-isolated postnatally Total ACC ( n)
Prenatal diagnosis isolated ACC (n)
Table 1 Prenatal prognosis of isolated anomalies of the corpus callosum: review of the literature
3 y (1–6 y) 5 y (2–16 y) 5 y (2–10 y) 3 y (2–5 y) 6 y (3–16 y) 4 y (30–74 m)
Copyright 2011 ISUOG. Published by John Wiley & Sons, Ltd.
0 4 4 NA
ACC have been amenable to prenatal ultrasound diagnosis for at least 15 years12,19 . The neurodevelopmental outcome of ACC associated with other anomalies is generally described as dismal, while that of isolated ACC is considered to be better, although not consistently normal. However, there have been only relatively few cases reported over the last 15 years that document reliably the performance of prenatal diagnosis using a combination of ultrasound and fetal MRI to confirm the isolated nature of ACC and to predict the outcome of cases with isolated ACC (Table 1).
TOP ACC isolated ( n)
*Includes the study by Pilu et al.18 (1993), 11 children aged 6 months to 11 years, 9 (82%) of whom were normal. †Used for meta-analysis. MRI, magnetic resonance imaging; NA, not available; m, months; TOP, termination of pregnancy; y, years.
Normal evolution (n; % (95% CI)) Lost to follow-up ( n) Duration of follow-up (median (range))
292 175 fetuses with ACC
88 isolated - 53 complete agenesis - 23 partial agenesis - 12 hypoplasia
1 IUFD
27 liveborn
26 followed up
60 TOP
1 excluded∗
87 with associated anomalies - 59 complete agenesis - 14 partial agenesis - 14 hypoplasia
3 IUFD
5 neonatal deaths
14 liveborn
2 lost to follow-up
70 TOP
7 followed up
Figure 1 Outcome of pregnancies with fetal anomalies of the corpus callosum (ACC). IUFD, intrauterine fetal death; TOP, termination of pregnancy. * Excluded because age 14 months at assessment.
ultrasound examination. The diagnosis was thought to be isolated ACC, including normal karyotype, in 88/175 (50%) cases prenatally. Of these, 27 cases were liveborn. One child of less than 30 months at the time of evaluation was excluded from long-term follow-up analysis; 26 (30%) were followed up to a median age of 50 (range, 30–74) months. In four of the 26 (15%) liveborn neonates thought prenatally to have isolated ACC, additional anomalies were diagnosed postnatally (Table 2). All infants with isolated ACC diagnosed prenatally were examined by a neuropediatrician and in 22 cases the parents consented to answering questionnaires. These cases were matched postnatally for age, gender and socioeconomic status with 44 control infants and DQ-CDIs were calculated for both groups. Significant differences (P < 0.05) were found between cases diagnosed prenatally with isolated ACC and controls for gross motor, fine motor, language comprehension, numbers and general development DQs (Table 3). Among the 26 infants diagnosed with isolated ACC antenatally, seven (27%) (95% CI, 13–46%) had neurodevelopmental delay, including three of the four children wrongly diagnosed with isolated ACC prenatally and then diagnosed as non-isolated ACC postnatally. In contrast, only one of the 44 control children had borderline developmental delay (P = 0.006; odds ratio, 15.84 (95% CI, 1.82–138).
DISCUSSION
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293
Table 2 Characteristics of children with a prenatal diagnosis of isolated anomalies of the corpus callosum (ACC) ACC type Gender
Prenatal diagnosis
Postnatal diagnosis
Associated deformities diagnosed postnatally
Developmental assessment
Age at assessment (months)
F M
Complete Complete
Complete Complete
No No
112 77
59 48
104 100 116
Normal Borderline development Normal Normal Normal Normal Retarded Normal Normal Normal Normal Normal Borderline development Normal Normal N/A*
M F F F M M M F M M M
Complete Complete Complete Complete Complete Complete Complete Complete Complete Complete Complete
Complete Complete Complete Complete Complete Complete Complete Complete Complete Complete Partial
No No No No No No No No No No No
85 97 89 107 47 104 95 NPE NPE NPE 76
M F M
Complete Complete Partial
Hypoplasia Partial Complete
No No No
F F
Partial Partial
Partial Partial
No No
134 93
Normal Normal
35 44
F
Partial
Partial
No
100
Normal
66
M M M
Partial Hypoplasia Hypoplasia
Complete Hypoplasia Hypoplasia
No No No
NPE 108 91
Retarded Normal Normal
60 57 45
F
Hypoplasia
Hypoplasia
No
108
Normal
66
M
Complete
Complete
28
Retarded
58
M
Complete
Complete
63
Retarded
51
F
Partial
Partial
20
Retarded
71
F
Complete
Complete
Congenital torticollis Congenital torticollis, LV over 15 mm Non-ketotic, hyperglycinemia Peter’s anomaly
111
Normal
72
DQ-CDI
74 50 33 30 32 55 39 36 48 60 47 57 56 14
Comments Convulsions
Squinting Squinting Prematurity (33 weeks) Squinting Squinting
Difficulty in swallowing
Persistence of right umbilical vein PROM at 6 months, prematurity (33 weeks) umbilical cord prolapse 33 weeks premature, pre-eclampsia
Neonatal respiratory distress, hypotonia Moderate IUGR, myopia Swallowing disorder, squinting, autism
Severe fixed encephalopathy
*Under 30 months at time of evaluation; excluded from long-term follow-up analysis. Complete, complete agenesis; DQ-CDI, development quotient from Child Developmental Inventory; F, female; IUGR, intrauterine growth restriction; LV, lateral ventricles; M, male; N/A, not applicable; NPE, neuropediatric examination without parental questionnaire; Partial, partial agenesis; PROM, premature rupture of membranes.
The aims of our study were: first, to review the ability of a combination of antenatal ultrasound and MRI to diagnose isolated forms of ACC, and second, to contribute to knowledge of the long-term prognosis of isolated ACC diagnosed prenatally, in a prospective population-based study performed within a national network of multidisciplinary centers for prenatal diagnosis. Overall, 15% of cases thought to be isolated proved to be associated with other abnormalities after birth. The severity of the anomaly diagnosed as well as the uncertainty regarding associated anomalies led to termination of over two thirds of cases. Prenatal counseling should take into account this uncertainty
Copyright 2011 ISUOG. Published by John Wiley & Sons, Ltd.
surrounding the diagnosis of associated anomalies, with reports of between 5 and 20% of cases diagnosed prenatally with isolated ACC proving to be nonisolated cases3,6,17 (Table 1). In the neurodevelopmental assessment of this population, we therefore deliberately took into account cases of ACC with associated anomalies that were thought to have been isolated prenatally because counseling is provided at the time of prenatal diagnosis. The meta-analysis of nine previously published studies (Table 1) suggests that the development of children diagnosed prenatally with isolated ACC is normal in up to 70% (95% CI, 56–83%) of cases. Including our series suggests it is normal in 71% (95% CI, 63–79%) of cases.
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Mangione et al.
294 Table 3 Development quotient (DQ) scores according to developmental area DQ score (mean (SD)) Developmental area Social Autonomy Gross motor Fine motor Expressive language Language comprehension Letters* Numbers General development†
Prenatal isolated ACC group (n = 22)
Control group (n = 44)
P
96.0 (33.3) 97.4 (36.0) 88.9 (27.6) 88.4 (26.4) 93.0 (33.9) 85.9 (26.2) 88.8 (31.0) 86.9 (27.1) 88.5 (27.7)
104.4 (23.0) 99.8 (16.7) 100.3 (18.2) 99.5 (10.8) 103.0 (21.4) 101.3 (21.7) 100.0 (12.9) 102.5 (14.6) 100.4 (9.9)
0.233 0.706 0.049‡ 0.018‡ 0.148 0.014‡ 0.066 0.003‡ 0.013‡
*For letters, test valid only for children above 38 months; number of subjects for this variable was 18 for ACC group and 36 for control group. †Six children in ACC group and one control had a general DQ score < 80 (Yates corrected chi-square = 6.40, d.f. = 1, P = 0.01). ‡Significant.
Our study found that the risk of neurodevelopmental delay in a fetus with ACC described prenatally as being isolated was 27%, whereas it was 15% for an infant whose diagnosis of isolated ACC was confirmed postnatally. Although the heterogeneity of the populations studied should favor center-based statistics at the time of prenatal counseling, in very few centers could sufficient numbers of these rare cases be gathered, and these overall figures might prove useful for counseling in these difficult cases. Our series reports on children up to the age of 6 years, whereas some psychopathological or cognitive disorders can only be evaluated later in life. Several studies evoked the hypothesis that subtle problems or deficits in neurodevelopment might appear with increased age15,19,30 – 33 . Furthermore, it is possible that using more specific psychometric tools to explore the interhemispheric relationship, focusing on visuospatial or verbal difficulties, might highlight certain types of specific deficit which do not hinder general development. Research on genome restructuring using the comparative genomic hybridization array technique should, in the near future, make it possible to characterize further anomalies that are not amenable to prenatal imaging34 . In our series, eye abnormalities in a case of Peter’s syndrome (OMIM #148 300), subtle and progressive anomalies of the cornea not amenable to prenatal diagnosis, were missed in one case that was diagnosed in utero as being isolated. This emphasizes that the diagnosis of isolated ACC calls for thorough genetic counseling, which may in turn lead to further prenatal investigations to confirm whether ACC is, in fact, isolated.
ACKNOWLEDGMENTS Thanks are due to Micheline Bisaro (psychologist), for her contribution and her help with this study, Teresa Sawyers, for translation, and all sonographers who participated in this study: C. Talmant, M. Althuser, D. Moeglin, B. Maugey, J.G. Martin, C. Courtiol, M. Aubron, J.P. Bault,
Copyright 2011 ISUOG. Published by John Wiley & Sons, Ltd.
B. Laplanche, E. Bensa¨ıd, G. Haddad, N. Bigi, F. Atger, H. Laurichesse, G. Gerves, B. Jouitteau, O. Castaing, O. Buisson, E. Julien, M. P. Legac, P. Morcel, F. Rauch, E. Vidalo, C. Lepinard, A. Sauvadet, M. Yvinec, C. Massias, T. Tomasella, S. Chouchene, A. Laurent, F. Poisson, D. Marchal, G. Neveux, M. Moulis, M. H. Vignelongue, M. Wetzel, B. Picard and D. Leduff.
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