Occupations of Parents of Children with Retinoblastoma: a Report from the Children's Cancer Study Group1

[CANCER RESEARCH 50, 7129-7133. November 15. 1990] Occupations of Parents of Children with Retinoblastoma: A Report from the Children's Cancer Study Group1

Greta R. Bunin, Alena Petrakova, Anna T. Meadows, Beverly S. Emanuel, Jonathan D. Buckley, William G. Woods, and G. Denman Hammond The Children 's Hospital of Philadelphia and the University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania I9I04 Â¡Ci.R.B., A. T. M., B. S. E.]; Charles University, Faculty of Pediatrics, Prague, Czechoslovakia [A. P.]; University of Southern California School of Medicine, Los Angeles, California 90033 fJ. D. B., G. D. H.]; and University of Minnesota Health Sciences Center, Minneapolis, Minnesota 55455 [W. G. W.Â¡

ABSTRACT childhood cancer, only the paternal occupation of television or A matched case-control study was conducted by the Children's Cancer radio repairman has been associated specifically with retino blastoma (5). We investigated occupations and exposures that Study Group to investigate the role of parental occupation in the etiology of sporadic heritable and nonheritable retinoblastoma. Eligible cases had been associated with other embryonal or nervous system were those patients with retinoblastoma diagnosed in 1982-1985 at any cancers (6-14). The results of exploratory analyses also are of the Children's Cancer Study Group member hospitals. Telephone reported here because this was one of the first case-control interviews of 201 parents of cases and their pair-matched controls se studies of retinoblastoma. lected by random digit dialing were completed. Of the 201 cases, 19 were At the time this study was conducted, the paternal origin of familial, 67 were sporadic heritable, and 115 were nonheritable. The 19 most new germinal mutations was not known. We hypothesized familial cases were excluded from the analysis. Paternal employment in that events during the grandmother's pregnancy with the the military |odds ratio (OR) 2.8, 95% confidence interval (CI) 1.1-8.8, mother might result in a germinal mutation because DNA P = 0.041 and in the metal industry (OR Â»,95% CI 1.4-Â», P = 0.02) replication occurs in utero in the female. The results of the was associated with sporadic heritable retinoblastoma ( Y = 67). For nonheritable retinoblastoma (.V = 115), a significant association was analysis of maternal grandparental occupation are reported. observed for a job cluster consisting mostly of welders and machinists (OR 4.0, 95% CI 1.1-22.1, P = 0.04). Occupations of maternal grand MATERIALS AND METHODS parents were also studied and an association was observed with farming The study has been described in detail elsewhere (15) and will be and nonheritable retinoblastoma (OR 10.0, 95% CI 1.4-433, P = 0.02). summarized here. Eligible cases were those patients with retinoblas toma diagnosed between 1982 and 1985 at one of the 34 Children's Many comparisons were made and the number of significant findings did not exceed that expected by chance. Thus, the results need to be inter Cancer Study Group member hospitals or their affiliates. Additional preted very cautiously. However, the findings related to metal exposure eligibility criteria were: biological mother English speaking and avail corroborate observations on other childhood cancers. able for interview, telephone in household, and residence at the time of diagnosis and interview in the United States or Canada. Of 373 cases identified, 314 met all eligibility criteria. INTRODUCTION Permission for an interview was obtained first from the case's phy Two forms of retinoblastoma, heritable and nonheritable, are sician and then from the parents. Of the 314 eligible cases, 201 were known to occur. The timing of causal events as postulated by interviewed and matched to a control. The reasons for not being the "two-hit" theory of carcinogenesis and clinical features interviewed or not being matched to a control were physician refusal (W = 5), insufficient information from hospital (A' = 24), inability to distinguish the forms (1). From an epidemiological viewpoint, locate family (N = 29), parental refusal (N = 27), inability to interview exposures of parents before the child's conception could influ parents before study ended (A' = 20), and inability to find a control (A1 ence the development of sporadic heritable retinoblastoma. = 8). These cases occur in the absence of a positive family history Cases were classified as familial, sporadic heritable, or nonheritable, and are believed to result from new germinal mutations. The based on family history information, tumor laterality, and cytogenetic vast majority of new germinal mutations in the retinoblastoma analysis, which was available for 75% of cases. The 201 cases were gene occur in the gene derived from the father (2-4). Thus, classified as follows: 19 (9%) familial, 67 (33%) sporadic heritable, and preconception exposures of the father but not the mother are 115 (57%) nonheritable. Four unilateral cases were included in the likely to be important in most instances. Since 95% of those sporadic heritable category based on the results of cytogenetic analyses with the retinoblastoma gene develop the disease, postconcep- as previously reported (16). The 25% of cases for whom cytogenetic analysis was not available were classified on the basis of family history tion exposures are unlikely to play a significant role. For and laterality. Analyses of occupational factors are reported for the 67 nonheritable retinoblastoma. however, postconception expo sporadic heritable cases and their controls and for the 115 nonheritable sures may be of etiological importance because the events cases and their controls. The 19 familial cases were excluded from leading to this form of retinoblastoma occur after conception. analysis. Parental occupation before and after the child's conception Controls were selected by random digit dialing and were pair- was investigated in a case-control study in order to explore matched to cases on telephone area code and the next five digits of the potential etiological factors for both forms of retinoblastoma. telephone number, date of birth (Â±1year), and race. The random digit- Although studies have investigated parental occupation and dialing procedure has been described previously (17). For 151 (75%) of the cases, the first eligible control identified completed the interview. Received 12/13/89; accepted 8/14/90. Controls for 43 (21 %) cases were the second eligible control identified. The costs of publication of this article were defrayed in part by the payment Participating controls for the remaining 7 cases were either the third of page charges. This article must therefore be hereby marked advertisement in or fourth eligible control identified. In all, 259 eligible control families accordance with 18 U.S.C. Section 1734 solely to indicate this fact. ' Partial support for this study was provided by a grant from the National were identified of which 201 (78%) participated. Institutes of Health (CA 36222). Contributing Children's Cancer Study Group A complete occupational history was obtained from both parents. If investigators, institutions, and grant numbers are given in the Appendix. Grant the father refused to participate or was unavailable, the mother prov ided support from the Division of Cancer Treatment, National Cancer Institute. a proxy interview. For each job held for at least 6 months, information National Institutes of Health. Department of Health and Human Services. A. P. was supported by the International Research and Exchanges Board while working was collected on the employer, job title, specific duties, and start and on this project. Address reprint requests to the Children's Cancer Study Group. termination dates. Fathers also were asked about military service, 199 North Lake Avenue. Third Floor. Pasadena. CA 91101. specifically in Vietnam, and exposure to herbicides. Mothers provided 7129

Downloaded from cancerres.aacrjournals.org on September 28, 2021. © 1990 American Association for Cancer Research. PARENTAL OCCUPATION AND RETINOBI.ASTOMA the industry and job title for the jobs that their parents, the index Table 1 Distribution of job characteristic.'! for cases and controls byform of child's maternal grandparents, held at the time of the mother's birth. retinohlastoma In addition to occupational history, parents provided information on Sporadic heritable Nonheritable medications. X-rays, life-style exposures, and family medical history. Cases C'ontrols Cases C'ontrols The results for nonoccupational factors have been reported previously (14). No. No. No. % No. % A. General job categories Job titles and industries were coded using the scheme of Hoar et al. Maternal grandfather's occu (18) which is based on the Standard Industrial Classification Manual pation (19) and the Dictionary of Occupational Titles (20). Jobs with similar Blue collar 361082114381464181446412213714511039121665259258182463141731861143865 71 68 exposures were grouped into 30 clusters according to the scheme of White collar 14 22 21 Hsieh et al. (21). Analyses were performed for ever versus never em Professional, managerial, 18 9 9 ployment in jobs, industries, and clusters of interest. The analyses of technical Student, unemployed 3 3 3 parental occupation were performed separately for mothers and fathers, No information 10 for preconception and postconception exposure, and for sporadic her Father's occupation itable and nonheritable cases. In addition, analysis of the preconception Blue collar 53 64 56 period was done considering all jobs and considering only jobs held full White collar 12 21 18 Professional, managerial. 33 30 26 time for at least 2 years. The results of the two analyses were compared technical to assess the possibility of recall bias concerning short-term jobs held Student, unemployed 3 0 20 B. Other characteristics of fa in the somewhat distant past. The results for all jobs and jobs lasting 2 thers' jobs or more years in the preconception period differed little and only results Proxy interviews of father 14 21 22 33 25 22 31 27 for the latter are reported. Occupations of maternal grandparents were Jobs (mean) analyzed separately for sporadic heritable and nonheritable cases. For Preconception 2.8 2.7 2.8 2.6 about one-quarter of the matched pairs, information on the maternal Postconception 1.1 1.1 1.2 1.1 grandparents was missing for either the case or the control or both. Age at first reported job 18.5 19.1 18.9 19.4 (mean yr) Because of the reduced sample size, only job clusters were analyzed. Few mothers or grandmothers had jobs with chemical or physical exposures. Their jobs were analyzed, but no significant associations were observed. 95% CI 0.7-277. P = 0.13; Table 2). Significantly more cases Job titles were also grouped into the general categories of blue collar, than controls in the nonheritable group had maternal grand white collar, and professional, technical, or managerial. The distribu tion of fathers' and grandfathers' jobs among these categories was fathers who were farmers (cluster 13) (OR 10.0, 95% CI 1.4- 433, P = 0.02). In the analysis of grandpaternal occupations, 1 compared in the sporadic heritable and nonheritable groups to investi gate possible case-control differences in socioeconomic status. of 15 case-control comparisons was statistically significant. Parental Occupation. Results for both pre- and postconcep- Odds ratios for matched pairs were calculated for potential risk factors and the corresponding two-sided P values computed using tion occupation are reported for both forms of retinoblastoma McNemar's test. Demographic characteristics of cases and controls to allow assessment of the specificity of the associations. Table were compared by x2 and McNemar's tests. For odds ratios based on 3 presents selected results of these analyses which are described 25 or fewer discordant pairs, 95% confidence intervals were calculated below. In the analysis of father's occupation, 104 comparisons by the exact method (22). Otherwise, approximate confidence intervals were made and four were statistically significant. Of 37 com were calculated (22). Statistical significance was defined at the 5% level. parisons made for mother's occupation, none were significant. We performed conditional multiple logistic regression to adjust for Sporadic Heritable Group. Significantly more case than con demographic differences between cases and controls and for associa trol fathers had a preconception job in the metal industry (OR tions among risk factors. Adjustment for other occupational risk fac oc,95% CI 1.4-3C, p â€”0.02). In the postconception period, the tors, nonoccupational risk factors described earlier (15), and other factors, such as general job category and proxy status of father's case excess remained (OR <*,95% CI 0.7-oo, P = 0.13). Case interview, did not substantially affect the results. fathers were significantly more likely than control fathers to have served in the military (OR 2.8, 95% CI 1.1-8.8, P = 0.04). When the timing was known, military service occurred with RESULTS one exception in the preconception period; the timing was General Job-related Factors. For both maternal grandfathers' unknown for three subjects. Seven case and five control fathers and fathers' occupations, the distribution of occupations among had served in Southeast Asia; only 2 case fathers and 1 control blue collar, white collar, and professional, managerial, or tech father reported exposure to Agent Orange or other herbicides; nical categories did not differ significantly (Table \A). Never 4 case fathers and 1 control father reported taking malaria theless, these nonsignificant differences were adjusted for in prophylaxis. other analyses. Information on 21% of case fathers and 29% of Using the classification schemes described in previous studies control fathers was provided by proxy interview of the mother of childhood cancer, we observed no significant associations for (P = 0.09). The age at first reported job, the number of jobs of exposure to hydrocarbons (23), lead (13), electromagnetic field 6 months or more reported in the preconception period, and (11), or ionizing radiation (5) or with employment as mechanics the number of jobs reported for the postconception period were or machinists (9), television or radio repairmen (5), paper mill similar for case and control fathers (Table IÃŸ)and for case and workers (9), painters (7, 8), aircraft workers (10), Air Force control mothers. workers (5), metal workers (12), or electronics workers (11). Maternal Grandparental Occupation. In the sporadic heritable However, nonsignificant case excesses were observed for elec group, nonsignificantly more case than control maternal grand tromagnetic field exposure (9 cases and 3 controls), for electric fathers had jobs in a cluster which include welders, machinists, and electronics manufacturing workers (3 cases, 0 controls), and paper-processing occupations (cluster 6 of Hsieh et al. (21) and for Air Force members (3 cases, 1 control). One case and referred to hereafter as the welder-machinist cluster) (OR2 6.0, two control fathers held jobs as television or radio repairmen, the only job category for which an association specific for 2The abbreviations used are: OR. odds ratio; CI. confidence interval. retinoblastoma has been previously reported (5).

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Table 2 Occupation of maternal grandfather and retinohlastoma: selected results heritable (/V= 48; 19 missing)Exact (N = 90; 25missing)RatioExact

Cluster"Description6 Ratio*CI6:1 95% CI5:2 95% Machinists, welders, metal workers 0.7-277 0.4-26.2 13 Farmers, farm workersOR6.0 1.0Sporadic 3:3 0.1-7.5OR2.5 10.0'Nonheritable10:1 1.4-433 Â°Asdefined by Hsieh et al. (21). Ratio of case exposed-control unexposed to case unexposed-control exposed pairs. c P = 0.02.

Table 3 Paternal occupation and retinoblastoma: selected results industry"Sporadic Metal-manufacturing cluster*OR2.3and machinists occupation'OR0.9

95%CI1.4-000.7-000.2-9.1 95%CI0.5-14.0 95%CI0.3-2.6 heritable (A' = 67) Preconception Postconception 4:04:3 1.74.0' S312:3 0.3-10.71.1-22.1 1.03.013.3Ratio8:97:715:50.3-3.31.0-10.5 Nonheritable (A' =115) Preconception PostconceptionORoo'OD1.34.0Ratio"7:0 4:1Exact 0.4-19.5Welders 5.0'Ratio7:3 10:2Exact 1.1-46.8Metal-related 10.3Exact 0.9-18.8 " Industry 6 as defined by Hoar et al. (18). * Cluster 6 as defined by Hsieh et al. (21). ' As defined by Wilkins and Koutras (12). d Ratio of case exposed-control unexposed to case unexposed-control exposed pairs.

Nonheritable Group. Significantly elevated odds ratios of 4.0 heritable retinoblastoma were more likely than controls to have (95% CI 1.1-22.1, P = 0.04) and 5.0 (95% CI 1.1-46.8, P = fathers who had served in the military and fathers employed in 0.04) were observed for paternal employment in jobs in the the metal-manufacturing industry. For the nonheritable form welder-machinist cluster before and after conception, respec of the disease, more cases than controls had fathers employed tively. Case fathers with jobs in this cluster included 5 welders, in the welder-machinist cluster and maternal grandfathers who 4 machinists, 2 metal workers, and 1 paper-manufacturing were farmers. Another significant finding, the association of worker. The association with military service observed in the preconception employment in a metal-related occupation and sporadic heritable group was absent in the nonheritable group nonheritable retinoblastoma, did not fit our original hypotheses (OR 0.6, 95% CI 0.3-1.2, P = 0.12). of timing of exposure and form of the disease. The five signifi The occupational groups found to be associated with child cant findings arose from 156 comparisons. Given the propor hood cancers in previous studies were analyzed for the nonher tion of significant findings, any or all of them may have occurred itable cases in an identical manner as for the sporadic heritable by chance. However, we believe that the metal-manufacturing cases. A significantly increased risk was observed for metal- and welder-machinist findings are less likely to be chance related occupation prior to conception (OR 3.0, 95% CI 1.1- associations because they corroborate some previous observa 10.5, P = 0.04); the odds ratio for postconception exposure was tions. similar (OR 3.3, 95% CI 0.9-18.8, P = 0.10). This metal- Associations with metal exposures have been reported for related category includes 90% of occupations in the welder- other childhood cancers. Wilms' tumor has been associated machinist cluster, as well as other occupations. We also ob with jobs in the welder-machinist cluster in one study (6) and served a slightly and nonsignificantly elevated odds ratio for with welding (14) in another. Childhood brain tumors have electromagnetic field exposure (preconception OR 1.6, 95% CI been associated with paternal employment in metal-related jobs 0.5-5.1, P = 0.48; postconception OR 1.8, 95% CI 0.5-7.5, P (12), and acute nonlymphocytic leukemia and hepatoblastoma = 0.42), which was completely explained by the case excess of have been associated with maternal exposure to metals (24, 25). welders. Reported associations of childhood cancer and parental metal- related industry and occupation are summarized in Table 4. Biological plausibility is suggested by the carcinogenicity of two DISCUSSION metals, nickel and hexavalent chromium (26). In this study, we observed five significant associations be The epidemiological findings on metals are intriguing but by tween occupation and retinoblastoma. Children with sporadic their nature do not suggest mechanisms by which occupational

Table 4 Metal-related parental industry and occupation: reported associations with childhood cancers

CancerWilms' occupationWelderor ratio"3.2-5.04.0-8.21.64.54/0-7/04.0-5.0Ref.6141224This tumorWilms' clusterWelderMetal-relatedand machinist tumorBrain tumorAcute occupationMetal-manufacturing leukemiaSporadicnonlymphocytic industryMetal-manufacturing retinoblastomaNonheritableheritable industryWelder studyThis retinoblastomaParentFatherFatherFatherMotherFatherFatherIndustryand machinist clusterOdds study flAll studies cited were case-control studies. The odds ratios from Ref. 14 did not reach statistical significance at the 0.05 level. For all other studies, at least one odds ratio in the range cited was statistically significant at the 0.05 level. 7131

Downloaded from cancerres.aacrjournals.org on September 28, 2021. © 1990 American Association for Cancer Research. PARENTAL OCCUPATION AND RETINOBLASTOMA exposures of parents might cause cancer in children. For ma ing relatively weak associations in the nonheritable group but, ternal exposure, direct exposure of the fetus seems like a more importantly, by reducing the sample size and power in plausible mechanism. Paternal exposure before the child's con the heritable group. ception might induce a germinal mutation that predisposes to Recall bias is a concern of case-control interview studies. We cancer. In sporadic heritable retinoblastoma, about 90% of new considered the possibility of recall bias resulting from case- germinal mutations are of paternal origin (2-4). Thus, paternal control differences in the proportion of fathers' interviews exposures before the child's conception may indeed play a role conducted by proxy, the number of reported jobs, and the in the etiology of sporadic heritable retinoblastoma, and the reporting of short-term jobs in the preconception period. For association reported here with paternal preconception employ each potential source of recall bias either no case-control dif ment in metal manufacturing is biologically plausible. Because ference was observed or adjustment for such a difference did nonheritable cases are believed to have a postconception origin, not affect the results. Thus, we believe that recall bias is unlikely any effect of paternal occupation would have to occur by ex to explain the results. posure during gestation or infancy. Substances might be Selection bias was also considered because nonparticipation brought home on the father's clothes or body or perhaps be rates for both cases and controls were substantial. Selection on absorbed and transmitted through semen. Exposure of children socioeconomic status would be perhaps most likely to affect a via soiled work clothes of their parents can occur and result in study of occupational factors. Differences in parents' education, elevated blood levels of occupational substances or clinical and more importantly, general job categories, were generally illness (27, 28). Whether this route of exposure affects fetuses small and were adjusted for in the analyses. Although selection is unknown. bias cannot be ruled out, it is difficult to imagine a bias that Whether maternal grandparental exposures play a role in the produces an effect for some blue collar occupations but not etiology of childhood cancer is a matter of speculation. When others. Selection bias might, however, have obscured real as the study began we hypothesized that exposures of maternal sociations. Our random digit-dialing method matched on the grandparents increased the risk of the sporadic heritable form cases' telephone exchange and therefore, probably to at least of retinoblastoma, by causing a new germinal mutation in one some degree, on socioeconomic status. This may have led to of the mother's eggs while the eggs were developing in utero. some overmatching on occupation and may explain some of Since then molecular biologists have determined that nearly all the negative findings. new germinal mutations in the retinoblastoma gene are derived Associations with metal-related occupation or industry oc from the father (2-4). Thus, the analyses of maternal grand curred for both forms of retinoblastoma. Although the inter parents' occupations are somewhat anachronistic. However, pretation of these findings is not clear, they require further these analyses revealed a strong association between maternal study because they corroborate reported associations with other grandfathers who were farmers and nonheritable retinoblas childhood cancers. toma. One might speculate that women whose fathers were farmers would have been exposed to pesticides while growing APPENDIX up on a farm. Because some pesticides can be stored for long APPENDIX periods of time in human fat (29), these women might reach Principal Investigators Children's Cancer Study Group reproductive age with a greater body burden of pesticides than other women. Perhaps this greater body burden would affect Institution Investigator Grant the fetus adversely after conception. Group Operations Office: University Dcnman Hammond. M.D. CA 13539 of Southern California Comprehen John Weiner. Dr.P.H. We hypothesized that preconception exposures increase the sive Cancer Center. Los Angeles. CA Harland Sather. Ph.D. risk of sporadic heritable retinoblastoma and postconception Richard Sposto. Ph.D. exposures increase the risk of nonheritable retinoblastoma. Mark Krailo. Ph.D. Jonathan Buckley. However, since fathers often had one job that began before the M.B.B.S. Ph.D. child's conception and continued afterward, the results for both Madeline Bauer. Ph.D. University of Michigan Medical Raymond Hutchinson. 02971 time periods were similar and we were not able to distinguish Center. Ann Arbor, Ml M.D. between pre- and postconception effects. University of California Medical ArthurM.D.Paul Ablin, CA17829CA We considered whether misclassification of form of retino Center, San Francisco. CA University of Wisconsin Hospital. M.D.RonaldGaynon, 05436CA blastoma may have affected our results. If the form of retino Madison. \VI blastoma (nonheritable versus sporadic heritable) was misclas- Children's Hospital and Medical M.D.SusanChard. 10382CA sified for a substantial proportion of cases, associations for each Center. Seattle. WA Rainbow Babies and Children's M.D.GregoryShurin. 20320CA form might be obscured. Cytogenetic analysis in addition to Hospital. Cleveland, OH laterality and family history information was used to classify Children's Hospital National Medical M.D.EdwardReaman. 03888CA Center. Washington. DC form. All cases classified as sporadic heritable are likely to be Childrens Memorial Hospital. M.D.JorgeBaum, 07431CA correctly classified according to current knowledge. The non- Chicago. IL Children's Hospital of Los Angeles. heritable group, however, might contain some unrecognized M.D.FrederickOrtega. 02649CA heritable cases. A small proportion, 10-15%, of unilateral cases Los Angeles, CA Children's Hospital of Columbus. M.D.SergioRuymann. 03750CA are believed to be sporadic heritable cases in whom only one Columbus. OH tumor occurred. Of the 119 unilateral cases (115 nonheritable Babies Hospital. New York. NY Piomelli. M.D. 03526 Children's Hospital of Pittsburgh. M.D.JohnVincent Albo. CA36015CA cases plus the four unilateral classified as heritable because of Pittsburgh. PA Vanderbill I'imersity School of a 13q abnormality), 12-18 would be expected to be heritable. M.D.RobertLukens. 26270CA We detected and reclassified four of these. Thus, 8-14 (7-12%) Medicine. Nashville. TN Doernbecher Memorial Hospital for M.D.WilliamNeerhout. 26044CA of the 115 nonheritable cases are likely to be misclassified Children. Portland, OR sporadic heritable cases. The actual number of sporadic herit University of Minnesota Health M.D.ThomasWoods. 07306C'A Sciences Center. Minneapolis. MN able cases would be 75-81 rather than 67. Misclassification of 36004 University of Texas Health Sciences Williams, M.D.CA form of retinoblastoma may have affected this study by obscur Center. San Antonio. TX 7132

APPENDIXâ€”continued 7. Wilkins, J. R.. Ill, and Sinks, T. H., Jr. Paternal occupation and Wilms' Principal Investigators Children's Cancer Study Group tumor in offspring. J. Epidemiol. Community Health. 38: 7-11. 1984. 8. Hemminki, K.. Saloniemi. I.. Salonen. T.. Partanen. T.. and Vainio, H. InstitutionChildren's Childhood cancer and parental occupation in Finland. J. Epidemiol. Com Philadelphia.Philadelphia,Hospital of M.D.PeterMeadows. 11796CA munity Health, 35: 11-15, 1981. PAMemorial 9. Kwa. S-L., and Fine, L. J. The association between parental occupation and CancerCenter.Sloan-Kettering M.D.RobertSteinherz, 42764CA childhood malignancy. J. Occup. Med.. 22: 792-794. 1980. NYJames New York. 10. Peters, J. M., Preston-Martin. S., and Yu, M. C. Brain tumors in children and occupational exposure of parents. Science (Washington, DC). 213: 235- forChildren.Whitcomb Riley Hospital M.D.MarkWeetman, 13809CA INHospital Indianapolis. 237, 1981. Toronto.Ontario.for Sick Children, MBCHBRichardGreenberg. 11. Spitz, M. R., and Johnson. C. C. Neuroblastoma and paternal occupation: a case-control analysis. Am. J. Epidemiol., 121: 924-929. 1985. CanadaUniversity Center.Saltof Utah Medical M.D.PaulO'Brien, 10198CA 12. Wilkins, J. R.. III. and Koutras. R. A. Paternal occupation and brain cancer UTUniversityLake City. in off-spring: a mortality-based case-control study. Am. J. Ind. Med.. 14: Columbia.Vancouver.of British M.D.BeatriceRogers, 29013C 299-318, 1988. 13. Kantor. A. F., Curnen, M. G. M., Meigs. J. W., and Flannery, J. T. Columbia.CanadaChildren'sBritish Occupation of fathers of patients with Wilms' tumour. J. Epidemiol. Com Center.Cincinnati.Hospital Medical M.D.JerryLampkin. A26I26CA munity Health. 33: 253-256. 1979. 14. Olshan. A. F.. Breslow. N. E.. Daling. J. R.. Palletta. J. M.. Grufferman. S.. OHHarbor/UCLA Robison, L. L., Waskerwitz, M., and Hammond. G. D. 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Downloaded from cancerres.aacrjournals.org on September 28, 2021. © 1990 American Association for Cancer Research. Occupations of Parents of Children with Retinoblastoma: A Report from the Children's Cancer Study Group

Greta R. Bunin, Alena Petrakova, Anna T. Meadows, et al.

Cancer Res 1990;50:7129-7133.

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