International Journal of Epidemiology 2003;32:248-256
© International Epidemiological Association 2003
Special Theme: Cancer |
Birth characteristics and brain cancers in young children
California Department of Health Services, Environmental Health Investigations Branch Oakland, CA 94612, USA.
Correspondence: Julie Von Behren, California Department of Health Services, Environmental Health Investigations Branch 1515 Clay Street, Suite 1700, Oakland, CA 94612, USA. E-mail: jvonbehr{at}dhs.ca.gov
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Abstract |
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Background High birthweight is a potential risk factor for childhood brain tumours, particularly astrocytomas. We investigated several birth characteristics in relationship to brain cancers in young children.
Methods We obtained 849 invasive central nervous system (CNS) cancer cases, ages 0–4 years, from California’s population-based cancer registry for 1988–1997. We matched 746 (88%) of these cases to a California live birth certificate. We randomly selected two control birth certificates for each case, matched on date of birth and gender. We used conditional logistic regression to obtain odds ratios (OR) and 95% CI. The birth characteristics examined included birthweight, gestational age, race, parental age, and parental education.
Results Analysing all CNS tumours combined, we found that children of other racial/ ethnic groups had OR below one compared with non-Hispanic white children. When adjusted for gestational age, race/ethnicity, and mother’s place of birth, the OR for high birthweight (
4000 g) was 1.05 (95% CI: 0.79–1.38) compared with children with birthweights of 2500–3999 g. For astrocytomas (313 cases), the adjusted OR for high birthweight was 1.40 (95% CI: 0.90–2.18). When parental education was included in the model (available for only a subset of the birth years), the adjusted OR was 1.71 (95% CI: 1.01–2.90). High birthweight did not appear to be a risk factor for primitive neuroectodermal tumours (PNET).
Conclusions We found high birthweight associated with increased risk of astrocytomas, but not PNET, in young children.
Keywords Brain cancer, child birthweight, parents’ education, parents age, social class, age factors, astrocytoma, race, ethnicity
Accepted 7 November 2002
Brain and other central nervous system (CNS) cancers account for 22% of all childhood malignancies in the US.1 These cancers continue to have poorer survival rates than the other most common childhood cancers, leukaemias and lymphomas.1 The causes of CNS malignancies are generally unknown. Between 1973 and 1994, the incidence rate of childhood CNS cancer increased by 35% in the US.2 The cause of this increase has been debated, with some researchers implicating environmental factors, though none has been conclusively identified.3 Others have suggested the rise was due to increased detection through improved medical imaging technology, rather than a true increase in incidence.2
Several studies have investigated the potential relationships between childhood CNS tumours and parental characteristics and birth characteristics. High birthweight has been identified as a potential risk factor for brain tumours, particularly astrocytomas.4–8 However, many other studies have investigated birthweight and found no significant differences between cases and controls.9–13 Other birth characteristics, including maternal age, birth order, and previous fetal loss, have been investigated but the results have been conflicting and inconsistent.14,15
We investigated birth characteristics in relationship to the diagnosis of CNS cancers before age 5 years among California children. Because of the relatively large number of cases available, more than in most previous studies, we analysed astrocytomas and primitive neuroectodermal tumours (PNET) separately, as well as looking at all tumours combined. Cancer registry data and birth certificate records were linked to conduct this records-based case-control study.
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Methods |
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A total of 849 cases of invasive CNS cancers, ages 0–4 years, were obtained from California’s population-based statewide cancer registry for 1988–1997. The CNS cancers were defined by the International Classification of Childhood Cancer (ICCC) diagnostic group III and included gliomas and other intracranial and intraspinal neoplasms.16 Using probabilistic record linkage,17,18 we matched 746 (88%) of these cases to a California live birth certificate (birth years 1983–1997). From the same birth certificate file, two controls were randomly selected for each case, matched on date of birth and gender. Control births were selected among mothers who were California residents at the time of delivery. The birth certificates of the controls were then matched to the California Birth Cohort files, which contain linked birth and death records for infants in the first year of life. Seven controls who died in the first year of life were excluded and replaced by the next eligible live birth certificate in the file (again matched for birth date and gender). One control was later dropped because we determined that the maternal residence address was not a California location.
The California birth certificates contained information on the age, race, and Hispanic ethnicity of both the mother and father. Maternal pregnancy history was also collected, including number of pregnancies, live births, prior pregnancy losses (spontaneous abortions and stillbirths), and time since last live birth. Information was also available about prenatal care, method of delivery, and complications during pregnancy and delivery. Data on the infants included gender, birthweight, gestational age, and whether a single or multiple birth. Maternal and paternal education were added to the birth certificate starting in 1989, so analyses including education could only be performed on births occurring in that year or later. We determined the highest level of education from the mother or the father to construct a parental education variable.
Odds ratios (OR) and 95% CI were obtained from conditional logistic regression models, which take into account the matched nature of the cases and controls. All analyses were performed in SAS.19 The multivariate models were restricted to those case-control sets where the case and at least one control were singletons. We entered birthweight and gestational age, a factor closely related to birthweight, into all multivariate models. We also included variables that were statistically significant in the univariate analyses. We stratified models by sex to look for differential effects, as reported in the previous literature by Emerson et al.6 Analyses were performed on the cases and controls for of all CNS cancers combined and separately for astrocytomas and PNET.
The study protocol was reviewed and approved by the California Health and Human Services Agency, Committee for the Protection of Human Subjects.
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Results |
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Among the 746 cases of CNS cancer, the most common type was astrocytoma, with 313 cases (42%). There were 238 PNET (32%), 91 ependymomas (12%), 73 other gliomas (10%), and 31 miscellaneous and unspecified intracranial and intraspinal neoplams (4%). There were 421 boys with a CNS cancer (56%) and 325 girls (44%). Among the astrocytoma cases, 54% were boys. The proportion of males was slightly higher in the cases of PNET and ependymomas (63% and 57% respectively).
All central nervous system tumours
The number of cases and controls for all the CNS tumours are shown in Table 1
. The univariate OR are also shown for each birth characteristic examined. Most of the CI included one, except for parental education, mother’s birthplace, and race/ethnicity of the child. The OR for 16 years of parental education was 1.69 (95% CI: 1.25–2.30) compared with parents who did not complete high school. Children whose mothers were born outside the US appeared to have reduced risk of CNS tumours (OR = 0.66, 95% CI: 0.55–0.80). Children of other race/ethnicity groups had OR below one when compared with non-Hispanic white children.
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The results from the multivariate model are shown in Table 2
. The OR for each race/ethnicity group remained below one. The OR for black children was 0.69 (95% CI: 0.49–0.98), the OR for Hispanics was 0.64 (95% CI: 0.50–0.82), and the OR for Asians/ others was 0.77 (95% CI: 0.53–1.14) when compared with non-Hispanic whites. The adjusted OR for foreign-born mothers was 0.79 (95% CI: 0.61–1.01). The adjusted OR for high birthweight (4000 g) was 1.17 (95% CI: 0.85–1.62) as compared with children with birthweights between 2500 and 3900 g. The OR for parental education were reduced appreciably in the multivariate model. The OR for college education of one or more parent was 1.19 (95% CI: 0.80–1.76) in the multivariate model compared with 1.69 in the univariate analysis. In this population, parental education was highly correlated with race/ethnicity, which was strongly related to case status. Over 41% of the non-Hispanic white children had a parent with a college education compared with about 20% for black children and only 8% for Hispanics. However, the proportion of Asian/other children whose parents had a college degree was about the same as that for non-Hispanic whites (42%).
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Astrocytomas
The number of cases and controls for astrocytomas are shown in Table 3
. The univariate OR are also shown for each birth characteristic examined. Children whose mothers were born outside the US appeared to have reduced risk (OR = 0.46, 95% CI: 0.34–0.63). When compared with non-Hispanic whites, children of the other race/ethnicity groups had OR below one. The OR for high birthweight (4000 g) was elevated at 1.67 (95% CI: 1.11–2.50) whereas the OR for low birthweight was below one (0.74, 95% CI: 0.35–1.56) when compared with the referent group (birthweight 2500–3999 g). The test for trend across the three birthweight categories was statistically significant (P = 0.01). The OR for 16 years of parental education was 2.68 (95% CI: 1.61–4.48) when compared with children whose parents did not complete high school.
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The results of the multivariate analysis are shown in Table 4
. The reduced OR for blacks, Hispanics, and foreign-born mothers persisted in this model. The risk for high birthweight for the full time period was still elevated at 1.40 though the CI included one (95% CI: 0.90–2.18). For the abbreviated time period for which education information was available, 1989–1997, the adjusted OR was 1.70 (95% CI: 1.01–2.90). The unadjusted OR for this time period was also higher (OR = 1.91) than for the full time period (OR = 1.67).
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Although no evidence of a differential effect for birthweight by sex was observed for all CNS tumours combined, a substantial difference was observed for boys and girls for the astrocytomas. Among boys, the adjusted OR for high birthweight and astrocytomas was 1.05 (95% CI: 0.58–1.88). However, in girls the OR was 2.21 (95% CI: 1.08–4.49).
In the analysis of the later birth years (where education information was available), the increased risk for advanced parental education (OR = 1.31 for college graduates, 95% CI: 0.68–2.51) was greatly reduced compared with the univariate analysis results (OR = 2.68). Among the astrocytoma cases and controls, parental education was strongly related to race/ethnicity. The non-Hispanic whites, who had a higher risk for astrocytoma than the other racial/ethnic groups, had the highest percentage of parents with a college degree (45%). Only 16% of the parents of the black children and 9% of the parents of Hispanic children had a college education. The proportion of Asian/other children whose parents had a college degree was higher, 35%, but still less than that of the non-Hispanic whites.
Primitive neuroectodermal tumours
The number of cases and controls for PNET are shown in Table 5. The univariate OR are also shown for each birth characteristic examined. The point estimates were close to one for most of the birth characteristics examined and the CI included one. High birthweight did not appear to be associated with PNET risk as it was for astrocytoma. The race/ethnicity differences appeared less pronounced for PNET than for all CNS tumours and astrocytomas.
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A multivariate model for PNET was run with mother’s age, infant race/ethnicity, birthweight, and gestational age. All of the point estimates were close to one except for the Asian/other race category. The OR for this group was 0.48 (95% CI: 0.22–1.05) compared with non-Hispanic whites. The OR for Hispanic children was 1.01 (95% CI: 0.70–1.46) and for blacks the OR was 0.86 (95% CI: 0.43–1.72). The adjusted OR for high birthweight was 1.03 (95% CI: 0.64–1.65) and for late gestational age was 1.14 (95% CI: 0.69–1.89). In addition, we did not observe the same differential effect by sex for high birthweight and PNET, as we did for astrocytomas.
Infants
Because many infant cancers exhibit unique epidemiological features,20,21 we examined selected birth characteristics and CNS tumours in children under one year of age (99 cases and 198 controls). Older parental age was associated with increased risk for infant CNS tumours. The OR for maternal age 35 years was 1.76 (95% CI: 0.87–3.55) as compared with mothers under age 35. The OR for paternal age 35 years was 1.75 (95% CI: 0.97–3.14) as compared with fathers under age 35. The OR for all race/ethnic groups were below one (but CI included one). The OR for birthweight 4000 g was 0.72 (95% CI: 0.32–1.64) compared with the referent group (birthweight 2500–3999 g). We also looked at the birth characteristics for astrocytomas, the most common tumour type (41 cases). Though based on small numbers the OR were still elevated for both older maternal and paternal age (for mother’s age OR = 4.16, 95% CI: 1.29–13.44). Firstborn children were at decreased risk (OR = 0.30, 95% CI: 0.13–0.70) and the OR for all race/ethnic groups were below one again, as they were for all tumour types combined. The OR for high birthweight was 1.80 (95% CI: 0.57–5.69).
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Discussion |
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This investigation found that high birthweight was associated with increased risk of astrocytomas in young children. Several previous studies have found no birthweight difference between cases and controls,9–13,22 but these studies did not differentiate by tumour subtype. In the study on brain tumours in Swedish children, Linet et al. reported findings by detailed histological types.5 They reported elevated OR for astrocytomas, especially high-grade astrocytoma, and high birthweights, but the OR was not significantly elevated for all tumours combined. Two other studies done in the US have found increased risk of astrocytoma with high birthweight.6,7 Because of the rarity of CNS tumours, most studies have not had sufficient numbers of cases to examine histological sub-types. It is possible that high birthweight is related to increased risk of astrocytomas but not other types of CNS tumours, which could explain the lack of findings in some previous studies.
High birthweight has been associated with increased risk of other childhood cancers, including leukaemia,23 neuroblastoma,10 and Wilms’ tumour.15 Birthweight is a crude proxy for hormone levels during pregnancy and high birthweight is associated with high oestrogen levels.24 Markers of high in utero oestrogen exposure have been associated with breast cancer, prostate cancer, and testicular cancer, possibly due to oestrogen’s growth promotion or genotoxic effects.25 High birthweight may be an indicator of increased cell division and fast growth. Insulin-like growth factor (IGF) is positively related to birthweight and high levels of IGF may stimulate the proliferation of both normal and malignant cells.23 The rapid proliferation of cells may lead to increased vulnerability to carcinogens and increased mutations.4 Alternatively, high birthweight may be a marker of other conditions, such as maternal diabetes.10
The present study showed that high birthweight was a risk factor for astrocytoma in girls but not boys. In a methodologically similar study done in Washington State, the risk for high birthweight and astrocytoma was also more pronounced in girls than boys.6 However, the authors reported several other significant differences that we did not see, including increased risk for prior fetal loss among boys and older maternal age with firstborn children. It is unclear why high birthweight would be a risk factor among girls but not boys.
The California data showed increased risk with older parental age in infants. Also, firstborn infants appeared at decreased risk for astrocytomas. These findings on infant tumours are based on very small numbers but may be useful for hypothesis generation about the aetiology of CNS tumours in this special age group. The early onset of these cancers is more suggestive of a prenatal origin and genetic factors may be especially important.26
California’s population of children is extremely diverse in terms of race and ethnicity, which allowed us the unique opportunity to examine these factors in relation to this rare cancer. white, non-Hispanic children are at higher risk than all other groups. However, this difference was less pronounced for PNET. Nationally, white children and teenagers have an 18% higher incidence rate of CNS cancers than blacks.27 In a recent study of California childhood cancer incidence rates, Glazer et al. reported significantly lower incidence rates of astrocytomas in Hispanics compared with non-Hispanic white children.28
Education is a proxy for socioeconomic status (SES), which in turn may be a proxy for certain disease risk factors. However, there are few known risk factors for CNS cancer in children and no well-established hypothesis about SES in relation to this disease. In our study of very young children, those whose parents had a college education appeared to have a higher risk of CNS cancer, especially for astrocytoma, than those whose parents did not complete high school. However, the OR for college education was greatly reduced once adjusted for race/ ethnicity, maternal birthplace, and birthweight (from 2.68 to 1.31 for astrocytoma). Socioeconomic status has been examined in a few other CNS cancer studies. Two occupational studies have found increased risk for CNS cancer in children of parents in white collar or managerial/professional occupations.29,30 An ecological study of childhood brain tumours in Scotland found that incidence was greatest in the most affluent areas.31 Two previous case-control studies that examined CNS risk and education have reported decreased risk for higher education. These studies both relied on volunteers for the control interviews, which resulted in women of higher social classes agreeing to participate more than other women.11,12
The occupational exposures hypothesized to increase brain cancer risk in offspring include pesticides, hydrocarbons, and N-nitroso compounds found in rubber, leather, metal, and chemical industries and in mining.15 Highly educated people are more likely to hold managerial and professional jobs, which usually have few known carcinogenic exposures.30 However, children of parents with a high level of education may have better access to diagnostic screening services and therefore be more likely to have their brain cancer detected, or at least detected earlier, than other children. In the US, the use of diagnostic imaging technology, such as magnetic resonance imaging (MRI) increased dramatically during the mid-1980s and is believed to be responsible for the rise in incidence of this disease observed during that time.2
This analysis was restricted to information available from the birth certificates. The data on birth certificates may not always be accurate or complete. We examined the percentage of missing data for each factor of interest and found a high level of completeness for most data elements. For example, mother’s age and birthweight were available for all subjects. Most missing data were on paternal factors. Eight per cent of the births were missing information on father’s age. Certain data elements such as complications during pregnancy and delivery and abnormal conditions present in the infant, including Down’s syndrome, are most likely incompletely reported. On the other hand, the accuracy of birth certificate data may be quite high for some factors of interest, such as birthweight and race. Birthweight is measured and recorded at the time of the birth. A recent analysis of the validity of race and Hispanic ethnicity information on the California birth certificate found that the information is a valid measure for all groups except Native Americans.32 Data on other birth characteristics, such as gestational age33 and birth defects,34 have not been reported to be as reliable.
Another potential limitation of this study is that the cases were limited to children who were both diagnosed and born in California, excluding highly mobile subjects. However, we did not see any differences in the distribution of unmatched and matched cases by race/ethnicity.
One of the main advantages of this study was that the use of vital records diminishes the problem of recall bias since the data were not self-reported after knowledge of disease status. In addition, the controls were randomly selected from state birth files, eliminating participation bias. The cases were drawn from the statewide, population-based cancer registry which has estimated 99% completeness of ascertainment.35 Also, this study focused on early childhood cancer which has a relatively short latency period and which may have a stronger relationship to perinatal factors than later cancers. With over 700 cases, this is one of the largest childhood CNS case-control studies to date. The relatively large number of cases allowed us to look at specific types of CNS tumours for which there appear to be different risk factors.
Because CNS tumours in children are rare, the literature to date on birth characteristics is limited. This study provided a large sample size with analysis by tumour subtype, an ethnically diverse population, and equivalent data collection for both cases and controls. The risk factors identified in this population, especially high birthweight for astrocytomas which has been observed in some other studies, may provide clues as to the aetiology of these rare but often deadly malignancies.
KEY MESSAGES
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Acknowledgments |
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This study was funded by grant number R01 CA71745 from the National Cancer Institute. The authors thank the staff of the California Cancer Registry and the staff of the Office of Vital Records. Thanks to Eric Elkin and Susan Hurley for conducting the record linkages. Theresa Saunders assisted with manuscript preparation. The ideas and opinions expressed are those of the authors and no endorsement by the California Department of Health Services should be inferred.
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