Abstract
The goal of this study was to investigate the potential for selection bias in published case–control studies on household exposure to pesticides and childhood acute leukemia; most studies have reported positive findings. Items to evaluate the potential for selection bias were first developed. They focused on the source populations that gave rise to cases and controls, the probabilistic selection of subjects from the source, and the losses of the subjects actually selected. A quantitative assessment of bias was also carried out. Potential sources of selection bias were found in all the studies, but none of them were observed across all the studies. Main sources of potential bias were a non-concurrent selection of controls with respect to cases, the use of control diagnoses possibly caused by pesticide exposure in hospital-based studies, and non-participation of selected eligible subjects. A quantitative assessment of bias concluded that non-participation alone could not explain the reported positive associations. We conclude that overall, selection bias, as a likely source of bias in these studies, does not seem to explain their positive findings. Our analysis provides arguments strengthening the conclusions on associations reported in earlier studies.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 6 print issues and online access
$259.00 per year
only $43.17 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Adgate J.L., Kukowski A., Stroebel C., Shubat P.J., Morrell S., and Quackenboss J.J., et al. Pesticide storage and use patterns in Minnesota households with children. J Expo Anal Environ Epidemiol 2000: 10: 159–167.
Alderton L.E., Spector L.G., Blair C.K., Roesler M., Olshan A.F., and Robison L.L., et al. Child and maternal household chemical exposure and the risk of acute leukemia in children with Down's syndrome: a report from the Children's Oncology Group. Am J Epidemiol 2006: 164: 212–221.
Anderson J.E., Nelson D.E., and Wilson R.W. Telephone coverage and measurement of health risk indicators: data from the National Health Interview Survey. Am J Public Health 1998: 88: 1392–1395.
Belson M., Kingsley B., and Holmes A. Risk factors for acute leukemia in children: a review. Environ Health Perspect 2007: 115: 138–145.
Berkowitz G.S., Obel J., Deych E., Lapinski R., Godbold J., and Liu Z., et al. Exposure to indoor pesticides during pregnancy in a multiethnic, urban cohort. Environ Health Perspect 2003: 111: 79–84.
Borghouts J.A., Koes B.W., and Bouter L.M. The clinical course and prognostic factors of non-specific neck pain: a systematic review. Pain 1998: 77: 1–13.
Buckley J.D., Robison L.L., Swotinsky R., Garabrant D.H., LeBeau M., and Manchester P., et al. Occupational exposures of parents of children with acute nonlymphocytic leukemia: a report from the Childrens Cancer Study Group. Cancer Res 1989: 49: 4030–4037.
Cloarec N., and Victor P. Le marché des télécommunications en 2002. Insee première 2004: 968: 1–4.
Galea S., and Tracy M. Participation rates in epidemiologic studies. Ann Epidemiol 2007: 17: 643–653.
Greenberg E.R. Random digit dialing for control selection. A review and a caution on its use in studies of childhood cancer. Am J Epidemiol 1990: 131: 1–5.
Greenland S. Basic methods for sensitivity analysis of biases. Int J Epidemiol 1996: 25: 1107–1116.
Greenland S. Multiple-bias modelling for analysis of observational data. J R Stat Soc Ser A 2005: 168: 267–291.
Hatch E.E., Kleinerman R.A., Linet M.S., Tarone R.E., Kaune W.T., and Auvinen A., et al. Do confounding or selection factors of residential wiring codes and magnetic fields distort findings of electromagnetic fields studies? Epidemiology 2000: 11: 189–198.
Infante-Rivard C., Labuda D., Krajinovic M., and Sinnett D. Risk of childhood leukemia associated with exposure to pesticides and with gene polymorphisms. Epidemiology 1999: 10: 481–487.
Infante-Rivard C., and Jacques L. Empirical study of parental recall bias. Am J Epidemiol 2000: 152: 480–486.
Infante-Rivard C., and Scott Weichenthal S. Pesticides and childhood cancer: an update of Zahm and Ward's 1998 Review. J Toxicol Environ Health B 2007: 10: 81–99.
Kaatsch P., Kaletsch U., Krummenauer F., Meinert R., Miesner A., and Haaf G., et al. Case control study on childhood leukemia in Lower Saxony, Germany. Basic considerations, methodology, and summary of results. Klin Padiatr 1996: 208: 179–185.
Karabelas A.J., Plakas K.V., Solomou ESDrossou V., and Sarigiannis D.A. Impact of European legislation on marketed pesticides—a view from the standpoint of health impact assessment studies. Environ Int 2009: 35: 1096–1107.
Kleinbaum D.G., Morgenstern H., and Kupper L.L. Selection bias in epidemiologic studies. Am J Epidemiol 1981: 113: 452–463.
Leiss J.K., and Savitz D.A. Home pesticide use and childhood cancer: a case-control study. Am J Public Health 1995: 85: 249–252.
Lowengart R.A., Peters J.M., Cicioni C., Buckley J., Bernstein L., and Preston-Martin S., et al. Childhood leukemia and parents' occupational and home exposures. J Natl Cancer Inst 1987: 79: 39–46.
Lu C., Knutson D.E., Fisker-Andersen J., and Fenske R.A. Biological monitoring survey of organophosphorus pesticide exposure among pre-school children in the Seattle metropolitan area. Environ Health Perspect 2001: 109: 299–303.
Ma X., Buffler P.A., Gunier R.B., Dahl G., Smith M.T., and Reinier K., et al. Critical windows of exposure to household pesticides and risk of childhood leukemia. Environ Health Perspect 2002: 110: 955–960.
Macfarlane T.V., Glenny A.M., and Worthington H.V. Systematic review of population-based epidemiological studies of oro-facial pain. J Dent 2001: 29: 451–467.
Meinert R., Kaatsch P., Kaletsch U., Krummenauer F., Miesner A., and Michaelis J. Childhood leukaemia and exposure to pesticides: results of a case-control study in northern Germany. Eur J Cancer 1996: 32A: 1943–1948.
Meinert R., Schuz J., Kaletsch U., Kaatsch P., and Michaelis J. Leukemia and non-Hodgkin's lymphoma in childhood and exposure to pesticides: results of a register-based case-control study in Germany. Am J Epidemiol 2000: 151: 639–646.
Menegaux F., Baruchel A., Bertrand Y., Lescoeur B., Leverger G., and Nelken B., et al. Household exposure to pesticides and risk of childhood acute leukaemia. Occup Environ Med 2006: 63: 131–134.
Mezei G., and Kheifets L. Selection bias and its implications for case-control studies: a case study of magnetic field exposure and childhood leukaemia. Int J Epidemiol 2006: 35: 397–406.
Mezei G., Spinelli J.J., Wong P., Borugian M., and McBride M.L. Assessment of selection bias in the Canadian case-control study of residential magnetic field exposure and childhood leukemia. Am J Epidemiol 2008: 167: 1504–1510.
Miettinen O.S. The “case-control” study: valid selection of subjects. J Chronic Dis 1985: 38: 543–548.
Mitchell A.A., Cottler L.B., and Shapiro S. Effect of questionnaire design on recall of drug exposure in pregnancy. Am J Epidemiol 1986: 123: 670–676.
Nguyen Q.V., Bezemer P.D., Habets L., and Prahl-Andersen B. A systematic review of the relationship between overjet size and traumatic dental injuries. Eur J Orthod 1999: 21: 503–515.
Perrillat F., Clavel J., Auclerc M.F., Baruchel A., Leverger G., and Nelken B., et al. Day-care, early common infections and childhood acute leukaemia: a multicentre French case-control study. Br J Cancer 2002: 86: 1064–1069.
Pocock S.J., Collier T.J., Dandreo K.J., de Stavola B.L., Goldman M.B., and Kalish L.A., et al. Issues in the reporting of epidemiological studies: a survey of recent practice. BMJ 2004: 329: 883–887.
Pombo-de-Oliveira M.S., and Koifman S. Infant acute leukemia and maternal exposures during pregnancy. Cancer Epidemiol Biomarkers Prev 2006: 15: 2336–2341.
Poole C. Invited commentary: evolution of epidemiologic evidence on magnetic fields and childhood cancers. Am J Epidemiol 1996: 143: 129–132.
Richiardi L., Boffetta P., and Merletti F. Analysis of nonresponse bias in a population-based case-control study on lung cancer. J Clin Epidemiol 2002: 55: 1033–1040.
Robbins P., Polderman A., and Birkenholtz T. Lawns and toxins—an ecology of the city. Cities 2001: 18: 369–380.
Robbins P., and Sharp J.T. Producing and consuming chemicals: the moral economy of the American lawn. Econ Geogr 2003: 79: 425–451.
Rudant J., Menegaux F., Leverger G., Baruchel A., Nelken B., and Bertrand Y., et al. Household exposure to pesticides and risk of childhood hematopoietic malignancies: the ESCALE study (SFCE). Environ Health Perspect 2007: 115: 1787–1793.
Sanderson S., Tatt I.D., and Higgins J.P. Tools for assessing quality and susceptibility to bias in observational studies in epidemiology: a systematic review and annotated bibliography. Int J Epidemiol 2007: 36: 666–676.
Savitz D.A. Selection bias in case-control studies. In: Savitz D.A. (Ed.). Interpreting Epidemiologic Evidence: Strategies for Study Design and Analysis. Oxford University Press, Oxford, 2003, pp. 81–114.
Savitz D.A., Wachtel H., Barnes F.A., John E.M., and Tvrdik J.G. Case-control study of childhood cancer and exposure to 60-Hz magnetic fields. Am J Epidemiol 1988: 128: 21–38.
Schwartzbaum J.A., George S.L., Pratt C.B., and Davis B. An exploratory study of environmental and medical factors potentially related to childhood cancer. Med Pediatr Oncol 1991: 19: 115–121.
Shen M., Cozen W., Huang L., Colt J., De Roos A.J., and Severson R.K., et al. Census and geographic differences between respondents and nonrespondents in a case-control study of non-Hodgkin lymphoma. Am J Epidemiol 2008: 167: 350–361.
Steer C.D., and Grey C.N. Socio-demographic characteristics of UK families using pesticides and weed-killers. J Expo Sci Environ Epidemiol 2006: 16: 251–263.
Teschke K., Kennedy S.M., and Olshan A.F. Effect of different questionnaire formats on reporting of occupational exposures. Am J Ind Med 1994: 26: 327–337.
Teschke K., Smith J.C., and Olshan A.F. Evidence of recall bias in volunteered vs. prompted responses about occupational exposures. Am J Ind Med 2000: 38: 385–388.
Von Elm E., Altman D.G., Egger M., Pocock S.J., Gotzsche P.C., and Vandenbroucke J.P. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Epidemiology 2007: 18: 800–804.
Wacholder S., Silverman D.T., McLaughlin J.K., and Mandel J.S. Selection of controls in case-control studies. II. Types of controls. Am J Epidemiol 1992: 135: 1029–1041.
Wartenberg D. The potential impact of bias in studies of residential exposure to magnetic fields and childhood leukemia. Bioelectromagnetics 2001: (Suppl 5): S32–S47.
Whyatt R.M., Camann D.E., Kinney P.L., Reyes A., Ramirez J., and Dietrich J., et al. Residential pesticide use during pregnancy among a cohort of urban minority women. Environ Health Perspect 2002: 110: 507–514.
Acknowledgements
This work was supported by a grant from the Association pour la Recherche sur le Cancer (ARC) and was partially carried out while Jérémie Rudant was on post-doctoral training with Claire Infante-Rivard in the Department of Epidemiology, Biostatistics and Occupational Health, Faculty of Medicine, McGill University, Canada.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no conflict of interest.
Appendix 1. Calculation of the prevalence of exposure among all the eligible controls who were selected (the method is similar for the cases).
Appendix 1. Calculation of the prevalence of exposure among all the eligible controls who were selected (the method is similar for the cases).
Let PRControls denotes the participation rate in controls, PEPartControls the prevalence of exposure in participating controls, PENPartControls the prevalence of exposure in non-participating controls, PEControls the prevalence of exposure among all the eligible controls who were selected and ORExpPartControls the odds ratio for association between household exposure to pesticides and participation status in controls.
PENPartControls is related to PEPartControls and ORExpPartControls by
ORExpPartControls=[PEPartControls * (1−PENPartControls)]/[(1−PEPartControls) * PENPartControls]
and hence, PENPartControls=1/[1+(ORExpPartControls * (1−PEPartControls)/PEPartControls)]
Then, PEControls is obtained by the following equation:
PEControls=PEPartControls * PRControls+PENPartControls *(1−PRControls)
Rights and permissions
About this article
Cite this article
Rudant, J., Clavel, J. & Infante-Rivard, C. Selection bias in case–control studies on household exposure to pesticides and childhood acute leukemia. J Expo Sci Environ Epidemiol 20, 299–309 (2010). https://doi.org/10.1038/jes.2009.61
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/jes.2009.61