Sixty-seven percent of all respondents engaged in at least 1 practice to protect themselves and their families from potentially hazardous environmental exposures (eg, pesticides, cleaning products, organic foods, plastics, etc.). Fellows were significantly less likely to report participating in behaviors in their own home that might avoid exposures to chemicals associated with health risks than were nurse practitioners or attending physicians (P<0.001) (Table 4). Those who attempted to avoid exposures at home were more likely to agree or strongly agree that environmental exposures are important contributors to the development of childhood leukemia (69%; SD, 8%; P=0.001). Among those providers who attempted to avoid home exposures and also agreed or strongly agreed that environmental factors are important contributors to childhood cancers, only 53% were somewhat or very comfortable discussing these issues with their patients.
This survey found that a majority of clinicians agreed that environmental exposures were important contributors to childhood cancers, but remained inconsistent in their history taking for these events. Although most practitioners routinely received questions about the relationship between environmental exposures and disease, few were entirely comfortable addressing these issues. Over 90% of respondents believed they would benefit from more information on this topic.
Previous surveys of the general public in the United States indicate widespread beliefs that the environment plays an important role in various health problems, and that parents would like more information from their pediatricians regarding environmental health topics.44,45 The findings of our survey support these previous results. Many respondents (48%) reported being frequently asked about environmental exposures to potential carcinogens by patients or their families. Greater familiarity with the emerging research on environmental contributions to childhood cancer would allow clinicians to be more responsive to these questions.
Providers with 5 or fewer years of experience were more likely to highlight genetics as a cause of childhood leukemia compared with providers with more experience, perhaps reflecting differences in curriculum and training that highlight more recent genetic studies. This group was also less likely to incorporate environmental health questions into their routine patient histories. Generational differences might account for this difference, as the more experienced clinicians were educated and trained during the height of the environmental movement, which could lead to greater awareness of environmental impacts on health.46,47
Our survey results indicate that clinical hematologists and oncologists engage in a variety of environmental history-taking practices. Many participants reported frequently asking about parental occupation, but not about any specific environmental hazards associated with that occupation. Anecdotal evidence and survey results suggest that clinicians have reservations about the appropriateness of asking the patients’ families questions related to environmental exposures and other carcinogens. One factor contributing to this perception may be the notion that clinicians do not have a major role in assessing etiology, and that such questions could raise the parents’ anxiety and guilt with little benefit to treatment outcomes. Although anticipation of negative parental reaction has been similarly cited by pediatricians as a common barrier to intervening with parents who smoke, the vast majority of smoking parents show strong support for addressing smoking at office visits.48,49
Twenty-five percent of clinicians did not ask about any of the environmental factors mentioned in our survey, whereas 75% routinely asked at least some questions related to assessing environmental exposures. For both groups, a better grounding in the literature could ensure that responses to questions from patients and families regarding environmental hazards are addressed promptly and accurately. This assumption is supported by our result that providers uniformly believed that more information on environmental health research relevant to childhood cancer would be helpful.
Historically, alert clinicians have recognized environmental exposure trends in their patient populations, and brought them to the attention of public health authorities. This was seen in cases of mesothelioma and lung cancer in asbestos workers, and vaginal adenocarcinoma in women born to diethylstilbestrol-exposed mothers, among others.50–52 Investigations of these cancer clusters led to the identification of previously unrecognized human carcinogens. By bringing an awareness of potential environmental etiologies to their oncology practice, clinicians can play an important role in raising issues in the research community and assisting investigators and public health officials in deciding potential areas of study.
Further illustration of this point can be seen in a recent case report, where the authors identified 4 cases of congenital fibrosarcoma linked to prenatal exposure to petroleum derivatives.52 Through the use of a routine pediatric environmental health history questionnaire, the authors were able to compare case histories with toxicological databases and identify exposures in each case to compounds associated with the development of fibrosarcoma in animals.52 Although this case series does not establish a causal association, it may form the hypothesis for a full-scale study.
Health professionals use peer-reviewed journals, consultations with peers, and conference attendance as their primary sources of reliable information for clinical decision making.53,54 We reviewed abstracts from the 2011 and 2012 American Society of Pediatric Hematology/Oncology (ASPHO) meetings to select those that examined causation or environmental risk factors (characterized broadly to include factors like diet and infectious agents). Of 569 abstracts, 8% dealt with questions of causation, and only 1% mentioned any environmental risk factors. During the same 2-year period, a PubMed search showed that 48 papers were published specifically on the topic of childhood cancers and environmental risk factors. However, these papers appeared primarily in nonclinical journals, such as Environmental Health Perspectives, American Journal of Epidemiology, and Cancer Causes & Control. It is likely that nonclinical journals do not have a widespread readership among busy clinicians.55
We reviewed federal funding to assess the proportion of resources devoted to studying environmental causes of childhood cancers. During 2010 and 2011, the National Institutes of Health awarded 3% to 7% of its total funding for childhood leukemia research to studies evaluating environmental etiologies. (A broad definition of environment was used to include factors such as diet and infection, together with more traditional factors. Only projects that focused on cancer as the primary endpoint were considered. Projects exclusively focusing on adult populations were excluded, as well as those that investigated mechanisms that might be broadly implicated in cancer development.) The majority of funding for this research comes from the National Institute for Environmental Health Sciences (NIEHS). The National Cancer Institute contributed around 1% of its funding for all childhood cancer toward environmental risk research.56,57 Despite an evolving understanding of environmental exposures associated with leukemia, funding for research that might inform activities aimed at prevention of childhood cancer remains limited.
Although this is a relatively small survey, it is the first characterization of pediatric hematology-oncology practitioners’ current perception of the importance of environmental exposures to their patient care responsibilities. Surveys, as a research tool, have disadvantages with respect to the data collected and representativeness of the sample. In our survey design, participants were restricted to specific responses, limiting the potential details collected. Two questions allowed for open-ended responses, which increased the depth of our investigation.
Our survey response rate of 45% may introduce bias in our results, as no information about the nonresponders was collected. For example, if those who had a higher concern for environmental associations were more likely to respond to the survey, these perspectives would have been overestimated in our sample. Email surveys of general practitioners have reported response rates similar to ours,58 however a study found response rates among specialty-fellows to be lower than nonspecialists.59 In general, email surveys have significantly lower response rates than mailed questionnaires.60,61 We aimed to increase the response rate and ensure more representativeness of the sample by sending a reminder email to participants. The survey was distributed to clinicians at selected institutions and does not comprise a representative sample of all practitioners in this field. This may affect the generalizability of our results if clinicians at these institutions differ substantially in their attitudes and practices from their counterparts across the country.
This survey identifies an opportunity for improved training in and awareness of environmental health research among attending physicians, fellows, and nurse practitioners working in the field of pediatric hematology/oncology. To help bridge this gap, environmental health researchers and epidemiologists should publish their relevant findings in journals that are widely read by pediatric hematologists/oncologists and nurse practitioners.
Educational opportunities should also be made available at national meetings, as our survey revealed significant interest in increasing baseline knowledge of environmental factors contributing to cancer. Training in environmental history taking, introduction of basic environmental history questions into the electronic medical record, and implementation of self-administered patient questionnaires during medical visits that address environmental exposures may aid in simplifying the collection of relevant information in the medical records of children with cancer. Moreover, the self-administered questionnaire may address the hesitancy of some clinicians to ask these questions during history taking. Ultimately, having gained a better understanding of current research findings, practitioners will utilize this information in ways appropriate to their particular practice setting.
Our results highlight the need for better integration of environmental health awareness in pediatric oncology practice and training. The translation of rigorous environmental health research findings to clinicians would potentially improve provider-patient communications, enhance data collection, and promote the role of alert clinicians in identifying sentinel events. With the convergence of research from CLIC and other groups, the body of evidence supporting environmental associations with childhood cancers is growing. Hazards, such as those mentioned in the Introduction section, have already gained a significant body of supporting information. As the environment continues to change and more hazards are identified, there is an ever-present need for pediatric oncologists to keep pace with this emerging research.
In memory of Pat Buffler who guided this work and made epidemiology important in our lifetime. She strongly motivated others to get involved and never saw a reason to fail. The authors would also like to acknowledge Yang Wang, Pagan Morris, and Sandra Luna-Fineman for their contributions.
2. Howlader N, Noone AM, Karapcho M, et al.. National Cancer Institute. SEER cancer statistics review, 1975-2008. Based on November 2010 SEER data submission. 2011. Available at: http://seer.cancer.gov/csr/1975_2008/
. Accessed February 27, 2013.
5. Boice JD Jr, Miller RW. Childhood and adult cancer after intrauterine exposure to ionizing radiation. Teratology. 1999;59:227–233.
6. Chokkalingam AP, Bartley K, Wiemels JL, et al.. Haplotypes of DNA repair and cell cycle control genes, x-ray exposure, and risk of childhood acute lymphoblastic leukemia. Cancer Causes Control. 2011;22:1721–1730.
7. Infante-Rivard C, Mathonnet G, Sinnett D. Risk of childhood leukemia associated with diagnostic irradiation and polymorphisms in DNA repair genes. Environ Health Perspect. 2000;108:495–498.
8. Moysich KB, Menezes RJ, Michalek AM. Chernobyl-related ionising radiation exposure and cancer risk: an epidemiological review. Lancet Oncol. 2002;3:269–279.
9. Doll R, Wakeford R. Risk of childhood cancer from fetal irradiation. Br J Radiol. 1997;70:130–139.
10. Pearce MS, Salotti JA, Little MP, et al.. Radiation exposure from CT scans in childhood and subsequent risk of leukaemia and brain tumours: a retrospective cohort study. Lancet. 2012;380:499–505.
11. Reynolds P, Von Behren J, Gunier RB, et al.. Childhood cancer incidence rates and hazardous air pollutants in California: an exploratory analysis. Environ Health Perspect. 2003;111:663–668.
12. Scelo G, Metayer C, Zhang L, et al.. Household exposure to paint and petroleum solvents, chromosomal translocations, and the risk of childhood leukemia. Environ Health Perspect. 2009;117:133–139.
13. Steffen C, Auclerc MF, Auvrignon A, et al.. Acute childhood leukaemia and environmental exposure to potential sources of benzene and other hydrocarbons; a case-control study. Occup Environ Med. 2004;61:773–778.
14. Vinceti M, Rothman KJ, Crespi CM, et al.. Leukemia risk in children exposed to benzene and PM10 from vehicular traffic: a case-control study in an Italian population. Eur J Epidemiol. 2012;27:781–790.
15. Ward MH, Colt JS, Metayer C, et al.. Residential exposure to polychlorinated biphenyls and organochlorine pesticides and risk of childhood leukemia. Environ Health Perspect. 2009;117:1007–1013.
16. Turner MC, Wigle DT, Krewski D. Residential pesticides and childhood leukemia: a systematic review and meta-analysis. Environ Health Perspect. 2010;118:33–41.
17. Infante-Rivard C, Labuda D, Krajinovic M, et al.. Risk of childhood leukemia associated with exposure to pesticides and with gene polymorphisms. Epidemiology. 1999;10:481–487.
18. Infante-Rivard C, Weichenthal S. Pesticides and childhood cancer: an update of Zahm and Ward’s 1998 review. J Toxicol Environ Health B Crit Rev. 2007;10:81–99.
19. Zahm SH, Ward MH. Pesticides and childhood cancer. Environ Health Perspect. 1998;106(suppl 3):893–908.
20. Rull RP, Gunier R, Von Behren J, et al.. Residential proximity to agricultural pesticide applications and childhood acute lymphoblastic leukemia. Environ Res. 2009;109:891–899.
21. Wigle DT, Turner MC, Krewski D. A systematic review and meta-analysis of childhood leukemia and parental occupational pesticide exposure. Environ Health Perspect. 2009;117:1505–1513.
22. Ma X, Buffler PA, Gunier RB, et al.. Critical windows of exposure to household pesticides and risk of childhood leukemia. Environ Health Perspect. 2002;110:955–960.
23. Wigle DT, Arbuckle TE, Turner MC, et al.. Epidemiologic evidence of relationships between reproductive and child health outcomes and environmental chemical contaminants. J Toxicol Environ Health B Crit Rev. 2008;11:373–517.
24. US Department of Health and Human Services. Chapter five: reproductive and developmental effects from exposure to secondhand smoke. The Health Consequences of Involuntary Exposure to Tobacco Smoke: A Report of the Surgeon General. Atlanta, GA: Centers for Disease Control and Prevention, Coordinating Center for Health Promotion, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health; 2006:165–256.
26. Cogliano VJ, Baan R, Straif K, et al.. Preventable exposures associated with human cancers. J Natl Cancer Inst. 2011;103:1827–3189.
27. Metayer C, Zhang L, Wiemels JL, et al.. Tobacco smoke exposure and the risk of childhood acute lymphoblastic and myeloid leukemias by cytogenetic subtype. Cancer Epidemiol Biomarkers Prev. 2013;22:1600–1611.
28. Ward MH, Colt JS, Deziel NC, et al.. Residential levels of polybrominated diphenyl ethers and risk of childhood acute lymphoblastic leukemia in California. Environ Health Perspect. 2014;122:1110–1116.
29. Metayer C, Milne E, Clavel J, et al.. The childhood leukemia International Consortium. Cancer Epidemiol. 2013;37:336–347.
30. Brown RC, Dwyer T, Kasten C, et al.. Cohort profile: the International Childhood Cancer Cohort Consortium (I4C). Int J Epdemiol. 2007;36:724–730.
31. Greaves MF. Infection, immune responses and the aetiology of childhood leukaemia. Nat Rev Cancer. 2006;6:193–203.
32. Urayama KY, Buffler PA, Gallagher ER, et al.. A meta-analysis of the association between day-care attendance and childhood acute lymphoblastic leukaemia. Int J Epidemiol. 2010;9:718–732.
33. Ma X, Buffler PA, Wiemels JL, et al.. Ethnic difference in daycare attendance, early infections, and risk of childhood acute lymphoblastic leukemia. Cancer Epidemiol Biomarkers Prev. 2005;14:1928–1934.
34. Kilpatrick N, Frumkin H, Trowbridge J, et al.. The environmental history in pediatric practice: a study of pediatricians’ attitudes, beliefs, and practices. Environ Health Perspect. 2002;110:823–827.
35. Trasande L, Newman N, Long L, et al.. Translating knowledge about environmental health to practitioners: are we doing enough? Mt Sinai J Med. 2010;77:114–123.
36. McCurdy LE, Roberts J, Rogers B, et al.. Incorporating environmental health into pediatric medical and nursing education. Environ Health Perspect. 2004;112:1755–1760.
37. Institute of Medicine. Role of the Primary Care Physicians in Occupational and Environmental Medicine. Washington, DC: National Academies Press; 1988.
38. Roberts JR, Gitterman BA. Pediatric environmental health education: a survey of US pediatric residency programs. Ambul Pediatr. 2003;3:57–59.
39. Schenk M, Popp SM, Neale AV, et al.. Environmental medicine content in medical school curricula. Acad Med. 1996;71:499–501.
40. Bellack JP, Musham C, Hainer A, et al.. Environmental health competencies: a survey of US nurse practitioner programs. J Nurs Educ. 1996;35:74–81.
41. Wilborne-Davis P, Kirkland KH, Mulloy KB. A model for physician education and consultation in pediatric environmental health—the Pediatric Environmental Health Specialty Units (PEHSU) program. Pediatr Clin North Am. 2007;54:1–13.
44. Centers for Disease Control and Prevention. Public opinion about public health—United States, 1999. MMWR Morb Mortal Wkly Rep. 2003;49:258–260.
45. Stickler GB, Simmons PS. Pediatricians’ preferences for anticipatory guidance topics compared with parental anxieties. Clin Pediatr (Phila). 1995;34:384–387.
46. Torgler B, García Valiñas MA, Macintyre A. Differences in preferences towards the environment: The impact of a gender, age and parental effect. Nota di lavoro, Fondazione Eni Enrico Mattei: CCMP, Climate change modeling and policy. 2008. Available at: http://hdl.handle.net/10419/40684
. Accessed July 8, 2013.
48. Cluss PA, Moss D. Parent attitudes about pediatricians addressing parental smoking. Ambul Pediatr. 2002;2:485–488.
49. Moss D, Cluss PA, Mesiano M, et al.. Accessing adult smokers in the pediatric setting: what do parents think? Nicotine Tob Res. 2006;8:67–75.
50. Fowler PBS, Sloper JC, Warner EC. Exposure to asbestos and mesothelioma of the pleura. Br Med J. 1964;2:211–213.
51. Herbst AL, Ulfelder H, Poskanzer DC. Adenocarcinoma of the vagina: association of maternal stilbestrol therapy with tumor appearance in young women. N Engl J Med. 1971;284:878–881.
52. Ortega-García JA, Soldin OP, López-Hernández FA, et al.. Congenital fibrosarcoma and history of prenatal exposure to petroleum derivatives. Pediatrics. 2012;130:e1019–e1025.
53. Schein M, Paladugu R, Sutija VG, et al.. What American surgeons read: a survey of a thousand Fellows of the American College of Surgeons. Current Surg. 2000;57:252–258.
54. Stinson ER, Mueller DA. Survey of health professionals’ information habits and needs. Conducted through personal interviews. JAMA. 1980;243:140–143.
55. McKibbon KA, Haynes RB, McKinlay RJ, et al.. Which journals do primary care physicians and specialists access from an online service? J Med Libr Assoc. 2007;95:246–254.
56. US Department of Health and Human Services. National Institutes of Health. National Cancer Institute. NCI Funded Research Portfolio database. Available at: http://fundedresearch.cancer.gov/nciportfolio/
. Accessed January 28, 2013.
57. US Department of Health and Human Services. National Institutes of Health. Estimates of Funding for Various Research Condition, and Disease Categories (RCDC). 2013. Available at: http://report.nih.gov/categorical_spending.aspx
. Accessed May 18, 2013.
58. Braithwaite D, Emery J, de Lusignan S, et al.. Using the Internet to conduct surveys of health professionals: a valid alternative? Fam Pract. 2003;20:545–551.
59. Cull WL, O’Connor KG, Sharp S, et al.. Response rates and response bias for 50 surveys of pediatricians. Health Serv Res. 2005;40:213–226.
60. VanGeest JB, Johnson TP, Welch VL. Methodologies for improving response rates in surveys of physicians: a systematic review. Eval Health Prof. 2007;30:303–321.
61. McMahon SR, Iwamoto M, Massoudi MS, et al.. Comparison of e-mail, fax, and postal surveys of pediatricians. Pediatrics. 2003;111:299–303.