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Association of Schizophrenia With Low Maternal Body Mass Index, Small Size at Birth, and Thinness During Childhood
Kristian Wahlbeck, MD, MScD;
Tom Forsén, MD, MScD;
Clive Osmond, PhD;
David J. P. Barker, FRS;
Johan G. Eriksson, MD, MScD
Arch Gen Psychiatry. 2001;58:48-52.
ABSTRACT
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Background Nutritional factors in early life may contribute to the neurodevelopmental
deficit in schizophrenia. This study explores the influence of maternal body
size, size at birth, and childhood growth on future risk for schizophrenia.
Subjects and Methods This population-based cohort study comprised births at Helsinki University
Central Hospital in Helsinki, Finland, from 1924 to 1933. Prospective data
from birth and school health records of 7086 individuals were collected and
linked to the Finnish Hospital Discharge Register.
Results Schizophrenia or schizoaffective disorder had been diagnosed in 114
individuals. A lower late-pregnancy maternal body mass index (BMI) increased
the risk (odds ratio [OR], 1.09 per kilogram/meter2; 95% confidence
interval [CI], 1.02-1.17) for schizophrenia among the offspring. The risk
of schizophrenia increased with low birth weight (OR, 1.48 per kilogram; 95%
CI, 1.03-2.13), shortness at birth (OR, 1.12 per centimeter; 95% CI, 1.03-1.22),
and low placental weight (OR, 1.22 per 100 g; 95% CI, 1.04-1.43). Schizophrenia
cases were thinner than comparison subjects from 7 to 15 years of age. In
a joint model comprising late-pregnancy maternal BMI, body size at birth,
and childhood BMI, childhood BMI was an independent predictor of schizophrenia,
whereas other factors exhibited attenuated effects.
Conclusion Indicators of intrauterine and childhood undernutrition are associated
with an increased lifetime risk of schizophrenia.
INTRODUCTION
SCHIZOPHRENIA IS a severe syndrome with a prevalence of approximately
1.3% in the Finnish adult population.1 Although
the etiopathogenesis of schizophrenia is inconclusive, the evidence supports
genetic predisposition and disturbed early neurodevelopmental processes as
important underlying factors.2 Published data
indicate that an array of adverse pregnancy and perinatal factors are related
to subsequent schizophrenia,3 including infections
during the second trimester of pregnancy,4 starvation
in utero,5 and obstetric complications.6 Preeclampsia, which is associated with a reduced nutritional
supply to the fetus, is the obstetric complication most strongly associated
with schizophrenia.7 Delayed motor development
and lower childhood educational achievements in people who later develop the
syndrome8 indicate that schizophrenia originates
long before the onset of evident illness.
An association between low birth weight (<2500 g) and schizophrenia
has been reported in a retrospective case-control study9
and replicated in a recent population-based prospective study from northern
Finland,10 which found that low birth weight
and the combination of low birth weight and short gestation (<37 weeks)
were more common among schizophrenic subjects. However, that study did not
find a connection between schizophrenia and low weight for gestational age.10 In a Swedish population-based cohort, small birth
size for gestational age and a low ponderal index (birth weight/length3) were associated with increased risk of schizophrenia, but only among
men.11 However, both cohort studies were restricted
to prenatal and perinatal risk factors and had a follow-up only until subjects
were in their 20s, which excluded later cases of schizophrenia from the analyses.
In the British 1946 birth cohort with 30 schizophrenia cases, no evidence
of differences between cases and controls in birth weight or in height and
weight at ages 7 and 11 years was found.8
We assembled a cohort of 7086 men and women who were born at Helsinki
University Central Hospital in Helsinki, Finland, between 1924 and 1933. The
aim of the study was to clarify the effects of fetal and childhood nutrition,
as reflected in late-pregnancy maternal body mass index (BMI), size at birth,
and growth during childhood, on lifetime risk of developing psychoses in the
broad schizophrenia group.
SUBJECTS AND METHODS
SAMPLE
The risk set originated from 27 068 men and women born at the public
Helsinki University Central Hospital between 1924 and 1933. The hospital served
both people living within Helsinki (population 221 524 in 1933) and people
living outside the city in southern Finland. This study included children
who went to primary schools in the city of Helsinki. Both birth and school
health records were available for 8580 subjects. School health records of
subjects born at the Helsinki hospital but who lived outside the city and
went to rural primary schools were not included.
We used birth and school health records to trace 7086 subjects who still
lived in Finland in 1971.12, 13 At
that time, a unique personal identification number was assigned to all residents
by the Finnish Population Register.
RISK FACTORS
Data on mothers' height, weight in late pregnancy, age, parity, and
the date of the last menstrual period were extracted from birth records together
with data on the newborns' length, weight, head circumference, and placental
weight.14 Using the father's occupation, the
subjects were grouped according to a social classification used by the Central
Statistical Office of Finland.15 Overall, 78%
of the fathers were laborers, and 10% were lower middle class. Together these
constitute the lower social class as opposed to the upper social class, which
is subdivided into upper middle class (2%) and self-employed (2%). The social
status of 8% could not be classified.
For each subject, height and weight were measured during school medical
examinations twice a year from ages 6 to 16 years.12, 13
The number of household inhabitants and the number of rooms in the home had
been recorded when the child first began school.
IDENTIFICATION OF CASES
Using the unique personal identification number, the individuals were
linked with the Finnish Hospital Discharge Register (HDR). The HDR was founded
in 1967 and covers all psychiatric and general hospitals. It contains data
on primary diagnosis and up to 3 subsidiary diagnoses on both discharges and
deaths of inpatients, regardless of length of hospitalization. The HDR is
a valid and reliable tool for epidemiological research.16
Accuracy of primary diagnoses in the HDR is acceptable; a 96.3% agreement
between HDR data and case notes has been reported in a schizophrenia sample.17 The predictive power of an HDR diagnosis in a broad
schizophrenia spectrum is 0.93 when compared with a "gold standard" consensus
diagnosis made against clinical records by 2 senior research psychiatrists
using the Diagnostic and Statistical Manual of Mental Disorders,
Revised Third Edition (DSM-III-R) criteria.17
Diagnoses have been entered in the HDR according to the International Classification of Diseases, Eighth Revision (ICD-8) until
1986, according to ICD-9 using the DSM-III-R criteria between 1987 and 1995, and according to ICD-10 criteria from 1996 onward. The first 3 digits from the cause
of admission were used to identify the occurrence of schizophrenia, schizophreniform
disorder, or schizoaffective disorder: 295 in ICD-8
and ICD-9 and F20 and F25 in ICD-10.
STATISTICAL ANALYSES
In this study, any individual found in the HDR with a primary or subsidiary
diagnosis as defined previously until December 1996 was assigned to the schizophrenia
group. This group of broad schizophrenia was compared with the remainder of
the risk set. We used multiple logistic regression analysis to calculate odds
ratios (ORs) for schizophrenia, adjusting for sex. Odds ratios are reported
with 95% confidence intervals (CIs). The independent variables we included
were maternal, neonatal, and childhood growth measurements. We assessed the
joint effect of variables in this sequence by including them simultaneously
in a multiple regression analysis. Childhood heights, weights, and BMIs were
all converted to age- and sex-specific z scores using the method of Royston.18 We interpolated between successive z scores with a
piecewise linear function and obtained a z score at each birthday from age
7 years to age 15 years. We then converted back these z scores to obtain the
corresponding height, weight, and BMI at each age.
RESULTS
In the cohort, 114 cases with a hospital diagnosis of broad schizophrenia
were identified, which indicates a cumulative incidence of 1.6% (1.3% in men
and 1.9% in women). A primary diagnosis of schizoaffective disorder was found
in 16 cases, and the remainder were diagnosed with schizophrenia. None had
a diagnosis of schizophreniform disorder. The occurrence of schizophrenia
was not related to year of birth.
The mean ± SD age of mothers in the cohort was 27.6 ±
5.7 years, and the mean ± SD parity was 2.3 ± 1.8. The mothers
of schizophrenic subjects were similar to the other mothers regarding their
age and parity.
In the unaffected control group (n = 6972), mean ± SD maternal
BMI was 26.8 ± 3.2 kg/m2, mean birth weight was 3383 ±
508 g, mean birth length was 50.0 ± 2.0 cm, and average BMI at age
7 years was 15.3 ± 1.2 kg/m2.
MATERNAL BODY SIZE
Table 1 presents ORs for
schizophrenia associated with a unit decrease in late-pregnancy body size.
Mothers' late-pregnancy BMI was significantly related to the occurrence of
schizophrenia in their offspring. Table 2 indicates that this finding depended mainly on an increased risk
with late-pregnancy BMIs of 30 or less. Mothers' heights were not related
to schizophrenia in offspring.
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Table 1. Odds Ratios for Schizophrenia Associated With a Unit Decrease
in Body Size in 7086 Men and Women in Helsinki, Finland*
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Table 2. Odds Ratios for Schizophrenia According to Late-Pregnancy
Maternal, Neonatal, and Childhood Body Size in 7086 Men and Women in Helsinki,
Finland*
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BIRTH SIZE
Men and women who were born small had an increased risk of schizophrenia.
Both low birth weight and a short length at birth increased the risk (Table 1 and Table 2). Schizophrenia was not associated with head circumference
at birth or with ponderal index (birth weight/length3). Length
of gestation (days) was not associated with increased risk of schizophrenia
(OR, 1.01; 95% CI, 0.99-1.02). There was no difference in the proportion of
preterm births (  37 weeks) in the schizophrenia group (11.2% of births)
when compared with the rest of the cohort (10.9% of births) ( 21 = 0.008, P = .93). A low placental weight
was associated with an increased risk of schizophrenia. As expected, size
at birth was related to mothers' late-pregnancy BMI (r
= 0.23 with birth length P<.001). In a simultaneous
regression, both shortness at birth (OR, 1.11; 95% CI, 1.01-1.22; P = .03) and low late-pregnancy maternal BMI (OR, 1.07; 95% CI, 1.00-1.15; P = .05) were related to schizophrenia.
CHILDHOOD GROWTH
Table 1 indicates that at
age 7 years, boys and girls who later developed schizophrenia had below-average
weight and BMI. These differences were statistically significant and remained
so at each age up to 15 years (Figure 1).
The height of boys and girls who developed schizophrenia did not differ significantly
from the average between ages 7 and 15 years. Table 3 presents the simultaneous effect of birth length and BMI
at 7 years on risk of schizophrenia. The highest risk was in people who were
short at birth and thin in childhood. In a simultaneous regression with mothers'
late-pregnancy BMI, birth length, and offspring's BMI at age 7 years, only
lower BMI at age 7 years remained significantly associated with schizophrenia
(OR, 1.37; 95% CI, 1.13-1.66; P = .001). Shortness
at birth was of borderline significance (OR, 1.10; 95% CI, 1.00-1.20; P = .06), and lower late-pregnancy maternal BMI was not
significant (OR, 1.05; 95% CI, 0.97-1.12; P = .22).
Findings in men and women were similar.
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Body mass index (BMI) during childhood for 114 girls and boys who
later developed schizophrenia in comparison with rest of cohort.
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Table 3. Odds Ratios (95% Confidence Intervals) for Schizophrenia According
to Tertiles of Birth Weight and Length, and Body Mass Index (BMI) at Age 7
Years, in 7086 Subjects*
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CHILDHOOD SOCIOECONOMIC CIRCUMSTANCES
The average number of inhabitants in the homes where the boys and girls
grew up was 5 (range, 1-27). The average number of rooms in the house was
2 (range, 1-14), and 47% lived in homes with only 1 room. As in previous studies,12, 13 we used the ratio of the number of
inhabitants to the number of rooms as an index of crowding. Families living
in less crowded conditions were of higher social class, and the children were
taller and weighed more between ages 7 and 15 years.12, 13
However, the level of crowding in the household during childhood was not related
to the risk of broad schizophrenia (OR, 0.93; 95% CI, 0.58-1.47), nor was
risk related to social class at birth, defined by the father's occupation
(OR, 1.38; 95% CI, 0.91-2.09).
COMMENT
Schizophrenia is a disorder with a multifactorial pathogenesis. The
importance of pregnancy and delivery factors has been highlighted in previous
studies. The present study is unique in combining maternal, birth, and childhood
growth characteristics. Our results indicate that in a semiurban setting,
small infants who are born to lean mothers and become thin in childhood are
at increased risk for schizophrenia. Leanness during childhood seems to be
an independent, additive risk factor to small size at birth. Thus, our results
support the role of early life and childhood influence in the pathogenesis
of schizophrenia.
Our study was restricted to men and women born at Helsinki University
Central Hospital. About 60% of Helsinki births occurred at this hospital.
The fathers of 78% of the cohort subjects were classified as laborers. The
subjects may be unrepresentative of all people living in Helsinki, although
we know that in 1930, around 60% of the city's men were laborers. This would
introduce a bias only if the associations between maternal, neonatal, and
childhood body size and schizophrenia differed between people born in the
hospital and those born in other places.
Subjects who died before 1971 and subjects who never went to primary
school, such as severely mentally retarded children, are excluded from our
cohort. Some subjects were lost because of early mortality; infant mortality
was 6.5% during the period between 1924 and 1933.19
Therefore, the associations in our study are representative of a population
that has reached middle age. One can assume that adverse maternal, pregnancy,
and childhood factors exert their maximum effect early in life,20
and thus the possible bias arising from selective loss of people who died
before middle age is more likely to lead to an underestimation of the associations
between early risk factors and schizophrenia than to an overestimation.
We were able to trace 92% of the people originally identified through
birth and school records. Our findings gain strength from the prospectively
collected growth data and the occurrence and coverage of the HDR. Results
from retrospective case-control studies on schizophrenia may be distorted
or inflated because of bias in case selection or ascertainment of risk factor
information. However, in the present population- and register-based study,
all data on risk factors for schizophrenia were ascertained before an outcome
was known.
One limitation of our study is that it excluded both schizophrenia subjects
who were never hospitalized and those hospitalized in young adulthood only
before 1971. In an extensive cross-sectional health survey of a representative
sample of the Finnish adult population between 1978 and 1980, 86% of those
with psychosis were currently receiving treatment.21
In Finland, treatment of schizophrenia almost always includes hospitalization.
The cumulative incidence of 1.6% in our cohort, born between 1924 and 1933,
is compatible with the findings of a declining incidence of schizophrenia
in Finnish birth cohorts22 and the 1-month prevalence
of schizophrenia of 1.3% in the population study from 1978 to 1980.1
Like another population-based cohort study,11
we failed to replicate the finding of small head circumference at birth made
in retrospective case-control studies of clinical samples.23, 24
Those studies may include more severely ill patients, with a stronger connection
to premorbid brain abnormalities. A similar discrepancy between cohort and
case-control studies has been described concerning obstetric complications
as a risk factor for schizophrenia.6 Together
these observations may indicate a true difference between clinical- and population-based
samples, and they suggest the need for caution when interpreting findings
from retrospective case-control studies.
The association between small birth size and schizophrenia was not due
to shortened gestation and must therefore be caused by reduced rates of growth.
We suggest that the associations with reduced fetal growth, small placental
size, and late-pregnancy maternal thinness indicate that schizophrenia may
originate through fetal undernutrition. This conclusion is strengthened by
findings among people who were conceived during the height of the Dutch famine
in 1945, whose risk for a schizophrenia-spectrum disorder was increased almost
threefold.25 Although there was no acute food
shortage in Finland during the years of cohort birth, the nutritional situation
of the lower classes was not good. About half of an average blue-collar worker's
wages was spent on food, and food shortage was common in working-class families
with many children. The primary source of protein was cereal products, mainly
bread.26
In a previous analysis of this semiurban cohort, we found that high
maternal BMI in late pregnancy was associated with a high rate of coronary
heart disease in men.14 We now find that low
late-pregnancy maternal BMI increased the child's risk of subsequent schizophrenia.
Mothers' late-pregnancy BMI reflects both weight gain during pregnancy and
BMI before pregnancy. Body mass index in late pregnancy is highly correlated
with BMI before pregnancy (r = 0.86; Keith Malcolm
Godfrey, BM, PhD, MRCP, unpublished data, 1991-1992, 1994-1995).
In a later Finnish general-population cohort of subjects born in 1966,
when the socioeconomic circumstances in Finland had improved, a high prepregnancy
maternal BMI was associated with schizophrenia. In a secondary analysis of
that cohort, the heaviest fifth percentile (BMI  29) of mothers had a doubled
risk of offspring with schizophrenia when compared with the middle 90%, but
the finding was not statistically significant.10
The differing findings between our study and the later Finnish cohort may
reflect societal changes. A low BMI in the late 1920s or early 1930s, in a
society without developed welfare structures, was linked to malnutrition or
illness, whereas in 1966, when the population's nutritional status was good,
it was more a matter of choice. In current Western populations, a high rather
than low maternal BMI is more likely to be associated with adverse outcomes,27 such as late fetal death,28
neural tube defects,29 and other congenital
malformations.30 However, it does protect against
the delivery of an infant that is small for its gestational age. We suggest
that our cohort's independent association between thinness in childhood and
schizophrenia may reflect childhood undernutrition. Our data indicate that
children with a length of 49 cm or less at birth, and who were below the lowest
BMI tertile at age 7 years, had a fourfold risk of developing schizophrenia
when compared with children who were above upper BMI tertile at age 7 years
and were longer at birth (Table 3).
In 1932, only 29% of children were offered meals in primary schools. The cohort
experienced a food shortage during adolescence in 1942, but there was no wartime
famine in Finland because of organized food rationing.26
In the Dutch famine study,25 periconceptional
famine was associated with an increased risk of schizophrenia. The current
study associates indicators of continued undernutrition with schizophrenia.
Epidemiologic studies have found that schizophrenic patients usually
belong to lower socioeconomic groups. However, the classic study by Goldberg
and Morrison31 found that the social class distribution
of the fathers of schizophrenic subjects did not differ from that of the general
population, which indicates that the excess of persons with schizophrenia
in the lowest socioeconomic group may be more the result of a downward drift,
or a decrease in social status, than of a socioeconomic causative factor.
In the present study, those original findings were replicated: we found no
significant difference between groups in socioeconomic distribution according
to fathers' occupation. Schizophrenia developed in 1.5% of children of laborers
and in 2% of children of nonlaborers. A similar trend of association between
schizophrenia and high social class at birth was reported in the British 1946
cohort.8 Thus, the association with nutritional
status does not seem to be mediated by socioeconomic status of the family.
In conclusion, low late-pregnancy maternal BMI, small placental size,
and small size at birth, possibly indicating fetal undernutrition, are associated
with increased lifetime risk of schizophrenia. Subjects who subsequently developed
schizophrenia remained lean during childhood, which may indicate continued
malnutrition.
AUTHOR INFORMATION
Accepted for publication July 20, 2000.
This study was supported in part by the British Heart Foundation, London,
England (Dr Barker), and the Wilhelm and Else Stockmann Foundation, Helsinki,
Finland (Dr Wahlbeck).
From the Department of Psychiatry, University of Helsinki (Dr Wahlbeck),
and the National Public Health Institute (Drs Forsén and Eriksson),
Helsinki, Finland; and the Medical Research Council Environmental Epidemiology
Unit, University of Southampton, Southampton, England (Drs Osmond and Barker).
Corresponding author: Kristian Wahlbeck, MD, MScD, Department of
Psychiatry, University of Helsinki, Lappviksvägen, PO Box 320, FIN-00029,
Helsinki, Finland (e-mail: kristian.wahlbeck{at}helsinki.fi).
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