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American Journal of Epidemiology Advance Access originally published online on December 12, 2006
American Journal of Epidemiology 2007 165(5):486-495; doi:10.1093/aje/kwk041
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American Journal of Epidemiology Copyright © 2006 by the Johns Hopkins Bloomberg School of Public Health All rights reserved; printed in U.S.A.

ORIGINAL CONTRIBUTIONS

Birth Characteristics and Risk of Neuroblastoma in Young Children

Kevin Y. Urayama1, Julie Von Behren2 and Peggy Reynolds2

1 Division of Epidemiology, School of Public Health, University of California, Berkeley, CA
2 Northern California Cancer Center, Berkeley, CA

Correspondence to Dr. Peggy Reynolds, Northern California Cancer Center, 2001 Center Street, Suite 700, Berkeley, CA 94704 (e-mail: preynolds{at}nccc.org).

Received for publication September 20, 2005. Accepted for publication July 26, 2006.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
The peak incidence of neuroblastoma during infancy suggests that certain prenatal or perinatal factors may be etiologically important. In this population-based study, California birth certificates were identified for 508 (86%) neuroblastoma cases diagnosed at less than 5 years of age between 1988 and 1997. For each case, two controls, matched on date of birth and gender, were randomly selected from the statewide birth registry. Results of multivariate analyses showed a reduced risk for children of Hispanic (odds ratio (OR) = 0.57, 95% confidence interval (CI): 0.43, 0.76) and "other" (OR = 0.56, 95% CI: 0.37, 0.85) race/ethnicity, compared with non-Hispanic Whites. Postterm/high birth weight delivery was associated with an increased risk of neuroblastoma compared with term/normal birth weight delivery among infants (OR = 6.99, 95% CI: 1.07, 45.55), while preterm birth appeared suggestive of a reduced risk among children 1–4 years of age. For children in this age group, the risk of neuroblastoma was elevated for cesarean delivery compared with vaginal delivery (OR = 1.72, 95% CI: 1.21, 2.47), and, for infants, the risk was reduced if the mother had had multiple previous pregnancies (OR = 0.39, 95% CI: 0.22, 0.69). These data suggest that etiologic factors associated with the prenatal and perinatal periods may be specific to age at neuroblastoma diagnosis.

birth certificates; birth weight; case-control studies; gestational age; neuroblastoma; risk factors

Abbreviations: CI, confidence interval; OR, odds ratio


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Neuroblastoma is an embryonal tumor derived from primordial neural crest cells that develop into the sympathetic nervous system and adrenal medulla. It is the most common cancer in infants (children less than 1 year of age), at 64 per million per year, and the third most common, after acute leukemia and tumors of the central nervous system, to affect children less than 5 years of age in the United States (1). Incidence is highly age dependent, peaking during infancy and rapidly declining with older age. Children less than 5 years of age account for nearly 90 percent of all neuroblastoma diagnoses in a given year (1).

An increased biologic and clinical understanding of neuroblastoma, together with advances in noninvasive screening technology during the past 20 years, have resulted in improved survival rates and identification of factors that influence prognosis (2, 3). In contrast, analyses of cancer surveillance data from several countries have shown marked increases in neuroblastoma incidence, particularly among infants (1, 4–6). This trend may have been influenced by implementation of mass screening programs among infants and the growing use of routine prenatal ultrasonography that has effectively led to an increase in antenatally detected neuroblastomas that would have otherwise spontaneously regressed with time (7). However, this factor does not appear to entirely explain the rising incidence, since increasing rates were reported in earlier studies, including those from the United States prior to these screening programs (6) and the United Kingdom, where screening has not been implemented (4, 5).

Because neuroblastoma is a disease of early childhood, prenatal and perinatal factors have been hypothesized to play an important role in its pathogenesis, serving as etiologically important events or markers for these events. The current epidemiologic literature reporting on these associations is relatively limited and has been largely inconsistent. Several studies have reported associations with gestational age and/or birth weight, but the direction of risk is conflicting and the association remains controversial (8–13). Other factors that have been associated with an increased risk of neuroblastoma include congenital anomalies in the child as well as maternal and delivery factors, including greater number of prior pregnancies, history of spontaneous and induced abortions, use of anesthesia during labor, and cesarean sections (8, 9, 11, 12, 14).

In this large, statewide, population-based case-control study, we used information provided by the California Cancer Registry and California birth certificate files to evaluate the influence of various parental and newborn characteristics and maternal obstetric factors on risk of neuroblastoma in children.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Study subjects
Using California's statewide cancer registry (the California Cancer Registry), we identified 594 cases of neuroblastoma in children 0–4 years of age diagnosed between 1988 and 1997. Using probabilistic record linkage (15–17), we located California birth certificates for 508 (86 percent) of these cases (birth years 1983–1997). From the same birth certificate files, we randomly selected two controls for each case, matched on date of birth and gender. To be consistent with our case selection criteria, we chose controls whose mothers were California residents at the time of delivery. We then cross-checked the birth certificates of our controls against the California Birth Cohort files, which link birth and death records for infants in the first year of life. Controls who had died in infancy were replaced if their death occurred at an age younger than the corresponding case's age at diagnosis. We later excluded one control because we determined that the mother's residential address at delivery was outside California. Because this was a records-based study, we were not required to obtain informed consent from study subjects. However, our use of human subjects data was reviewed by the California Health and Human Services Agency, Committee for the Protection of Human Subjects.

Birth certificate information
California birth certificates served as our main data source, providing demographic information, pregnancy history, and children's birth characteristics. Birth certificate information available for each child included date of birth, place of birth, gender, race/ethnicity, birth weight, gestational age, birth order, abnormal conditions and clinical procedures related to the newborn, and whether the birth was single or multiple (twins, triplets, etc.). Parental information included age, race/ethnicity, and place of birth. Starting in 1989, California began collecting information on educational level for each parent on birth certificates. Available information on maternal pregnancy history included numbers of pregnancies, livebirths, and pregnancy losses (spontaneous abortions and stillbirths); and time since last livebirth. The birth certificates also provided information about prenatal care, pregnancy complications, and delivery method for each case and control.

Census data
The mother's residential address at the time of each child's birth was abstracted from all case and control birth certificates. Ninety-eight percent of residences were assigned an address-level latitude and longitude coordinate using a geographic information system. Using 1990 US Census information (18), we assigned each address to a US Census block group and used the block group's median family income and percentage of the adult population with a college degree as measures of the family's socioeconomic status.

Statistical analysis
To account for the matched study design, we used conditional logistic regression models in a matched analysis to calculate odds ratios and 95 percent confidence intervals. The initial inclusion of variables in the multivariate model was based on prior knowledge of the importance of certain variables, univariate risk estimates, and consideration of collinearity between variables. The transformed likelihood value (–2log[L]) served as the relative measure of goodness of fit for the full and nested models and was used to determine the relative importance of the explanatory variables. The multivariate models were restricted to those case-control sets in which the case and at least one control were singletons.

To alleviate collinearity and interpretation issues of including highly correlated variables in a multivariate model, a combined nine-category index for gestational age and birth weight was created. Children were considered preterm, term, and postterm if born at less than 37, 37–41, and 42 weeks or more, respectively. Children were considered low, normal, and high birth weight if born weighing less than 2,500 g, 2,500–3,999 g, and 4,000 g or more, respectively. Dichotomous (yes/no) variables were created for abnormal conditions of the newborn and pregnancy complications. Specific conditions and complications were evaluated only when sufficient sample sizes were available. Because of the age-dependent nature of this disease, a stratified analysis by child's age (≤12 months vs. 1–4 years of age) was conducted based on the hypothesis that these two groups may be associated with different risk factors. We did not attempt to impute data that were missing. We performed all statistical analyses by using SAS, version 8 software (19).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Our analysis included 508 neuroblastoma cases diagnosed between 1988 and 1997 in California and 1,015 controls matched on date of birth and gender. Cases less than 5 years of age constitute nearly 90 percent of all neuroblastomas diagnosed in California during this time period (20). Approximately 45 percent (228 of 508) of the diagnoses in children less than 5 years of age occurred during the first year of life, with less than half as many (102 of 508) occurring in the second year.

Table 1 shows results from our univariate analyses examining the association between neuroblastoma and selected birth certificate characteristics. Neuroblastoma incidence appeared to be slightly higher in males (59 percent) than in females and varied considerably by age. Children classified as Hispanic and "other" (includes Asians, Pacific Islanders, and Native Americans) race/ethnicity had roughly half the risk of neuroblastoma compared with that for non-Hispanic White children (odds ratio (OR) = 0.51, 95 percent confidence interval (CI): 0.40, 0.65 for Hispanic children; OR = 0.57, 95 percent CI: 0.39, 0.84 for children of "other" race/ethnicity). Neuroblastoma cases appeared more likely to be firstborn (OR = 1.25, 95 percent CI: 1.00, 1.59) and have some type of abnormality noted at birth (OR = 1.77, 95 percent CI: 1.09, 2.88). The data were too sparse to evaluate risks associated with specific abnormalities. Neither birth weight nor gestational age appeared to be significantly associated with neuroblastoma. Among births after 1988, children of more highly educated mothers (OR = 2.11, 95 percent CI: 1.47, 3.04 for children of mothers with ≥16 vs. <12 years of education) and fathers (OR = 1.85, 95 percent CI: 1.28, 2.68 for children of fathers with ≥16 vs. < 12 years of education) appeared to have an increased risk. Consistent with this result, higher median annual household income and percentage with a college degree, according to the 1990 US Census block group data, were associated with a positive trend toward an increased risk of neuroblastoma (OR = 1.52, 95 percent CI: 1.09, 2.13 for children born in the highest vs. the lowest category of median household income; OR = 1.87, 95 percent CI: 1.36, 2.58 for children born in a neighborhood with the highest vs. the lowest percentage of adults with a college degree).


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  		TABLE 1. Distribution of newborn and parental characteristics and maternal obstetric factors and corresponding effect estimates in relation to neuroblastoma risk in young children in California diagnosed between 1988 and 1997

 
Some characteristics related to the pregnancy and delivery of the child and maternal pregnancy history seemed to be associated with neuroblastoma risk. Initiation of prenatal care during the later trimesters, compared with the first trimester, was significantly associated with a reduced risk (OR = 0.70, 95 percent CI: 0.53, 0.94). An elevated risk was observed for children delivered by cesarean section (OR = 1.55, 95 percent CI: 1.22, 1.97), with primary and repeat cesarean delivery showing similarly elevated risks when evaluated as separate categories. Two correlated variables—greater number of previous livebirths (p for trend < 0.001) and prior pregnancies (p for trend = 0.002)—were associated with a reduced risk of neuroblastoma. Neither pregnancy complications overall nor any specific complications (e.g., preeclampsia, diabetes, and genital herpes) appeared to be associated with risk.

Table 2 presents the results estimated from a multivariate conditional logistic regression model including birth characteristics that, according to the model fit, best characterized the data. In the multivariate analysis, child's race/ethnicity remained statistically significant, where Hispanic and "other" race/ethnicity was associated with a reduced risk of neuroblastoma compared with that for non-Hispanic White race/ethnicity (OR = 0.57, 95 percent CI: 0.43, 0.76 for Hispanic race/ethnicity; OR = 0.56, 95 percent CI: 0.37, 0.85 for "other" race/ethnicity). The risk associated with delivery by cesarean section continued to be elevated compared with vaginal delivery (OR = 1.43, 95 percent CI: 1.10, 1.87), and children born to mothers who had had three or more previous livebirths had a reduced risk (OR = 0.63, 95 percent CI: 0.44, 0.91). Greater percentage with a college degree appeared suggestive of an increased risk of neuroblastoma (OR = 1.41, 95 percent CI: 0.97, 2.04 for 33 percent with a college degree vs. <10 percent with a college degree).


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  		TABLE 2. Multivariate analysis of select birth certificate characteristics in relation to neuroblastoma risk in California children diagnosed between 1988 and 1997

 
Table 3 shows the results of multivariate analyses that evaluated birth characteristics and risk of neuroblastoma in infants (≤12 months of age) separate from children 1–4 years of age. This stratified analysis showed that, among infants, postterm/high birth weight delivery, compared with term/normal birth weight delivery, was significantly associated with an increased risk of neuroblastoma (OR = 6.99, 95 percent CI: 1.07, 45.55). This association was not evident among children diagnosed at later ages. However, among older children only, preterm delivery—either low birth weight or normal birth weight—compared with term/normal birth weight delivery, was suggestive of a reduced risk of neuroblastoma (OR = 0.56, 95 percent CI: 0.19, 1.60 for preterm/low birth weight; OR = 0.56, 95 percent CI: 0.27, 1.17 for preterm/normal birth weight). The risk of neuroblastoma associated with cesarean section appeared to affect mostly older children (OR = 1.72, 95 percent CI: 1.21, 2.47). Infants born to women who had had three or more prior pregnancies had a statistically significant reduced odds compared with that for infants born to women with no prior pregnancies (OR = 0.39, 95 percent CI: 0.22, 0.69), an association not evident among older children. Finally, this stratified analysis suggests that there may be a larger effect of socioeconomic status on risk among older children compared with infants (OR = 1.59, 95 percent CI: 1.01, 2.51 for 20–32 percent with a college degree vs. <10 percent with a college degree).


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  		TABLE 3. Multivariate analysis of select birth certificate characteristics in relation to neuroblastoma risk among infants (≤12 months of age) and children 1–4 years of age in California diagnosed between 1988 and 1997

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
The early presentation of neuroblastoma suggests that certain prenatal and perinatal factors may play a role in the pathogenesis of this disease. In this large, population-based, case-control study, we observed associations with a number of birth characteristics, including child's race/ethnicity, gestational age/birth weight, cesarean section delivery, and maternal pregnancy history. Notably, estimates of associations between certain characteristics (preterm and postterm/high birth weight births, cesarean delivery, and maternal gravidity) and neuroblastoma risk differed between earlier- and later-diagnosed children.

The ethnic diversity of California's population offered us the opportunity to evaluate the risk of neuroblastoma associated with child's race and Hispanic ethnicity. In our analyses of children less than 5 years of age, compared with non-Hispanic White children, Hispanics and those of "other" race/ethnicity (largely, Asians and Pacific Islanders) were at a significantly reduced risk of neuroblastoma. This finding is consistent with cancer registry data showing that the average annual age-specific (0–4 years) incidence of sympathetic nervous system tumors is lowest among these two groups of children in California (20). Among the limited number of studies that could evaluate an association with race/ethnicity, the Children's Oncology Group study reported no convincing evidence of an association with maternal race (21). Their predominately White study population (approximately 80 percent) and age criterion of less than 19 years may account for the inconsistency. According to data reported by the Surveillance, Epidemiology, and End Results Program, incidence rates of neuroblastoma appeared to differ by race/ethnicity among infants, but not among older children, suggesting that this association may be age dependent (1). Our stratified analysis by child's age, however, suggested a similar effect of race/ethnicity among infants and older children.

Previous reports of international comparisons have shown incidence rates of neuroblastoma to be highest among the developed countries of Europe and North America and lowest among the developing countries of Africa, Asia, and South America (22). These observations suggest potential risk factors unique to certain socioeconomic conditions, as well as an influence of race-specific genetic susceptibility. Although this pattern is consistent with the results of this current study showing an increased risk associated with higher socioeconomic status, some earlier studies have suggested neuroblastoma to be more common among groups of lower socioeconomic status (23, 24).

The rapidly declining incidence with increasing age suggests that neuroblastoma presenting at younger and older ages may be associated with different preconceptional, gestational, and/or early postnatal risk factors and highlights the critical nature of the timing of certain exposures. A study was conducted in Denmark based on a hypothesis that factors associated with elevated risks of paternal germ line mutations would be more common in neuroblastomas presenting during the first year of life, while neuroblastomas diagnosed later would be more commonly associated with factors related to or occurring during pregnancy (initiating somatic mutation) (25). Their results were not completely supportive of these hypotheses but did show evidence of differing risk factors between younger- and older-diagnosed patients. We found a few notable differences in risk between infants and older children, primarily gestational age/birth weight, type of delivery, and mother's number of prior pregnancies.

The Children's Oncology Group study and other studies have evaluated the association of gestational age and birth weight with risk of neuroblastoma (8–10, 12, 13); however, results of these studies have been inconsistent. In our analyses, we categorized children based on the combination of two highly correlated variables—gestational age and birth weight—and found some suggestion of a reduced risk associated with preterm delivery and an increased risk associated with postterm/high birth weight delivery. Interestingly, when we stratified our data by age at diagnosis, postterm/high birth weight delivery was associated with a markedly increased risk of neuroblastoma among infants only, and preterm delivery, either low birth weight or normal birth weight, remained suggestive of a reduced risk among older children. These results are consistent with an early study that showed a reduced risk associated with preterm births (<37 weeks' gestation) independent of birth weight and ethnic group (10). However, in contrast to our study, these authors also observed a trend toward an increasing risk with lower birth weight among term births. The authors of the study proposed a mechanism indicative of an in utero stimulus (oncogenic initiator or promoter) that occurs in the last month of pregnancy, a period of possible increased susceptibility of the fetal nervous system to transplacental insults, and suggested that weight may play a role in susceptibility to this factor. In their study, cases included all children less than 15 years of age who died of neuroblastoma. Because higher survival rates have been observed among children diagnosed during infancy, the authors noted that younger children may have been underrepresented in their case series, which provides greater support for the results of this current study showing an effect among the older age group only.

The Children's Oncology Group study found a marginally significant reduced risk associated with a preterm gestation of 33–35 weeks and an imprecise, but elevated, risk estimate associated with gestation of less than 33 weeks (9). However, in contrast to our results and to this proposed mechanism, in an age-stratified analysis, the study observed a suggestive increased risk of preterm delivery among children 1–4 years of age. Birth weight was not found to be statistically significant, but it provided some evidence of an increased risk associated with extremely low birth weight (<1,500 g). A German study similarly reported statistically significant increased risks for shorter gestational duration and lower birth weight (12). In a study conducted in New York State, no association was found with birth weight, but a reduced risk was observed for both preterm and postterm delivery, making interpretation difficult (8).

The hypothesis of an in utero oncogenic stimulus during the last month of pregnancy suggests that children born after a longer than normal gestational period could potentially be at increased risk of developing neuroblastoma. Our results of an increased risk associated with postterm/high birth weight delivery supports this hypothesis. Two other US studies specifically examining the influence of birth weight on risk of childhood cancers have reported increased risks associated with high birth weight (13, 26). In the larger of the two studies, the association was confined to only those children less than 2 years of age (26). Since neither of the two studies examined gestational age, it is difficult to conclude whether these associations confer risk independently of gestational age. In our study, no association was observed for term/high birth weight delivery compared with term/normal birth weight, suggesting that gestational age likely is an important factor in the increased risk found for postterm/high birth weight among infants. Finally, in a relatively smaller study conducted in Minnesota, no associations were observed for either birth weight or gestational age (11).

Our results show an increased risk of neuroblastoma in children delivered by cesarean section compared with those delivered vaginally, particularly those in the age group 1–4 years. The Children's Oncology Group study reported an increased risk associated with cesarean delivery but, in contrast, observed the effect primarily among children less than 1 year of age (9). The investigators suggested that cesarean delivery may be a marker for anesthesia use. Their study also found anesthetic epidural to be associated with an increased risk of neuroblastoma (9). However, the New York State study showed an increased risk for repeat cesarean deliveries but not primary cesarean deliveries, which argues against a role of anesthesia use during labor and delivery on risk, since repeat cesarean deliveries are usually scheduled and performed in a manner that ensures minimal exposure of the fetus to anesthetic agents (8). Neuroblastoma risk may be associated with cesarean delivery through a relation of the delivery procedure, such as with anesthesia use or through another mechanism possibly related to some surrogate of pregnancy complication.

The reduced risk associated with a higher number of prior maternal pregnancies observed in this study has been suggested in the New York State study (8) but conflicts with the findings from the Children's Oncology Group study (9). The epidemiologic association with gravidity is not consistent, nor is there a biologic explanation that supports a reason for an association. Our stratified analyses showed gravidity to be important in neuroblastomas presenting at an early age only. Although the data were too sparse to perform valid statistical tests to evaluate risks associated with specific abnormalities, there did appear to be an overrepresentation of cases with abnormalities of the circulatory system and genitourinary system compared with controls. These observations support the findings from a recent report from the Children's Oncology Group study that showed an increased risk associated with increasing number of congenital anomalies, specifically genitourinary and cardiac anomalies (14). Investigators in a recent study conducted in Massachusetts performed an echocardiographic review of neuroblastoma cases and controls to detect congenital cardiovascular malformations; they found a significantly larger proportion of cases (20 percent) with these anomalies compared with controls (3.6 percent) (27). Other types of congenital anomalies, including anomalies of the face and digestive system, have also been previous associated with neuroblastoma risk (28, 29).

A disadvantage of conducting this purely records-based study is that we lacked potentially important information on personal behavior, environmental exposures, and genetic susceptibility factors. In addition, it is sometimes possible for birth certificate data to be inaccurate or incomplete. However, in examining the percentage of missing birth certificate data for each factor of interest, we noted at least 99 percent completeness for all data elements except father's age, gestational age, and time since last livebirth. Parental education information was available for only recent births, resulting in missing data for approximately 30 percent of subjects. In addition to examining individual indicators of educational status for this subset, we assigned all subjects measures of neighborhood (block group) socioeconomic status, based on US Census median household income and percentage of the adult population with a college degree for their residence at birth. Birth certificate data are thought to be reliable for many factors recorded at the time of birth, such as birth weight and race/ethnicity. A recent validity analysis of race and Hispanic ethnicity data on the California birth certificate found that the information was a valid measure for all groups except Native Americans (30).

To our knowledge, this is the largest case-control study of neuroblastoma in young children conducted to date. We designed our two-to-one matching scheme to optimize power for examining associations between neuroblastoma and the birth characteristics of interest. Our study's strengths lie in its population-based subject ascertainment, reduced selection and information biases, and case-control study design. We drew our cases from the statewide, population-based cancer registry, which has an estimated 99 percent ascertainment completeness (31). Although we limited our cases to children who were both diagnosed and born in California, probably excluding highly mobile subjects, our selection included most California cases diagnosed within our study time frame. We eliminated participation bias by randomly selecting controls from the California birth files rather than using volunteer recruits. The records-based nature of our study minimized the potential information biases common to many epidemiologic studies that use questionnaires or interviews to obtain data.

The literature to date examining prenatal and perinatal risk factors for neuroblastoma is limited and highly inconsistent. Although it is the most common cancer in infants, the overall rarity of neuroblastoma introduces challenges to conducting epidemiologic studies. In this relatively large and ethnically diverse population-based study, we demonstrated that certain perinatal factors may be of etiologic importance to the pathogenesis of neuroblastoma and that earlier- and later-diagnosed disease may be associated with different risk factors.


   ACKNOWLEDGMENTS
 
This study was funded by grant 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. They also thank Eric Elkin and Susan Hurley for conducting the record linkages and Theresa Saunders for assisting with manuscript preparation.

The ideas and opinions expressed herein are those of the authors, and no endorsement by the National Cancer Institute should be inferred.

Conflict of interest: none declared.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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