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Cancer Causes & Control

, Volume 28, Issue 3, pp 177–190 | Cite as

Pesticide exposure and liver cancer: a review

  • Trang VoPhamEmail author
  • Kimberly A. Bertrand
  • Jaime E. Hart
  • Francine Laden
  • Maria M. Brooks
  • Jian-Min Yuan
  • Evelyn O. Talbott
  • Darren Ruddell
  • Chung-Chou H. Chang
  • Joel L. Weissfeld
Review article

Abstract

Purpose

To review the epidemiologic literature examining pesticide exposure and liver cancer incidence.

Methods

A search of the MEDLINE and Embase databases was conducted in October 2015. Eligibility criteria included examining hepatocellular carcinoma (HCC) or primary liver cancer, pesticides as an exposure of interest, and individual-level incidence. The review was performed according to Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines.

Results

Forty-eight papers were assessed for eligibility and 15 studies were included in the review. The majority of studies were conducted in China and Egypt (n = 8), used a case–control design (n = 14), and examined HCC (n = 14). Most studies showed no association between self-reported and/or occupational exposure to pesticides and liver cancer risk. Six studies demonstrated statistically significant positive associations, including three biomarker-based studies (two using pre-diagnostic sera) that reported higher serum levels of dichlorodiphenyltrichloroethane (DDT) were associated with increased HCC risk. Studies indirectly measuring pesticide exposure using self-reported exposure, occupation, job-exposure matrices, or geographic residence demonstrated inconsistent results. These studies were limited by exposure assessment methods, lack of confounder information, minimal case confirmation, selection bias, and/or over-adjustment.

Conclusions

There is mixed evidence suggesting a possible association between specific pesticides and HCC risk, with the strongest evidence observed in biomarker-based studies. In particular, organochlorine pesticides, including DDT, may increase HCC risk. Future research should focus on improved pesticide exposure assessment methods, potentially incorporating multiple approaches including biomonitoring while considering the chemicals of interest, historical exposure to address latency periods, and examining specific chemicals and exposure pathways.

Keywords

Liver cancer Hepatocellular carcinoma Pesticides Epidemiology Review 

Notes

Acknowledgments

The authors declare no conflicts of interest. Dr. VoPham is supported by the National Institutes of Health (NIH) National Cancer Institute (NCI) Training Program in Cancer Epidemiology (T32 CA009001). Dr. Hart is supported by the NIH National Institute of Environmental Health Sciences (NIEHS) P30 ES000002.

References

  1. 1.
    Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin D, Forman D, Bray F (2013) GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11 [Internet]. International Agency for Research on Cancer. http://globocan.iarc.fr. Accessed 11 Aug 2015
  2. 2.
    Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61(2):69–90. doi: 10.3322/caac.20107 PubMedCrossRefGoogle Scholar
  3. 3.
    McGlynn KA, Petrick JL, London WT (2015) Global epidemiology of hepatocellular carcinoma: an emphasis on demographic and regional variability. Clin Liver Dis 19(2):223–238. doi: 10.1016/j.cld.2015.01.001 PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Carr BI (2010) Hepatocellular carcinoma: diagnosis and treatment, 2nd edn. Humana Press, PhiladelphiaCrossRefGoogle Scholar
  5. 5.
    El-Serag HB (2007) Epidemiology of hepatocellular carcinoma in USA. Hepatology Res 37(Suppl 2):S88–S94. doi: 10.1111/j.1872-034X.2007.00168.x CrossRefGoogle Scholar
  6. 6.
    Surveillance, Epidemiology, End Results (SEER) Program, (http://www.seer.cancer.gov) SEER*Stat Database: Incidence—SEER 18 Regs Research Data + Hurricane Katrina Impacted Louisiana Cases, Nov 2014 Sub (2000–2012) <Katrina/Rita Population Adjustment>—Linked To County Attributes - Total U.S., 1969–2013 Counties, National Cancer Institute, DCCPS, Surveillance Research Program, Surveillance Systems Branch, released April 2015, based on the November 2014 submission.
  7. 7.
    El-Serag HB, Kanwal F (2014) Epidemiology of hepatocellular carcinoma in the United States: where are we? Where do we go? Hepatology 60(5):1767–1775. doi: 10.1002/hep.27222 PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Yu MC, Yuan JM (2004) Environmental factors and risk for hepatocellular carcinoma. Gastroenterology 127(5 Suppl 1):S72–S78. doi: 10.1016/j.gastro.2004.09.018 PubMedCrossRefGoogle Scholar
  9. 9.
    Turati F, Galeone C, Rota M, Pelucchi C, Negri E, Bagnardi V, Corrao G, Boffetta P, La Vecchia C (2014) Alcohol and liver cancer: a systematic review and meta-analysis of prospective studies. Annu Oncol 25(8):1526–1535. doi: 10.1093/annonc/mdu020 CrossRefGoogle Scholar
  10. 10.
    Jinjuvadia R, Patel S, Liangpunsakul S (2014) The association between metabolic syndrome and hepatocellular carcinoma: systemic review and meta-analysis. J Clin Gastroenterol 48(2):172–177. doi: 10.1097/MCG.0b013e3182a030c4 PubMedCrossRefGoogle Scholar
  11. 11.
    Bravi F, Bosetti C, Tavani A, Gallus S, La Vecchia C (2013) Coffee reduces risk for hepatocellular carcinoma: an updated meta-analysis. Clin Gastroenterol Hepatol 11(11):1413–1421. doi: 10.1016/j.cgh.2013.04.039 (e1411) PubMedCrossRefGoogle Scholar
  12. 12.
    Duan XY, Zhang L, Fan JG, Qiao L (2014) NAFLD leads to liver cancer: do we have sufficient evidence? Cancer Lett 345(2):230–234. doi: 10.1016/j.canlet.2013.07.033 PubMedCrossRefGoogle Scholar
  13. 13.
    FonSing M, Yang WS, Gao S, Gao J, Xiang YB (2011) Epidemiological studies of the association between tea drinking and primary liver cancer: a meta-analysis. Eur J Cancer Prev 20(3):157–165. doi: 10.1097/CEJ.0b013e3283447497 CrossRefGoogle Scholar
  14. 14.
    Larsson S, Wolk A (2007) Overweight, obesity and risk of liver cancer: a meta-analysis of cohort studies. Br J Cancer 97(7):1005–1008. doi: 10.1038/sj.bjc.6603932 PubMedPubMedCentralGoogle Scholar
  15. 15.
    Lee YC, Cohet C, Yang YC, Stayner L, Hashibe M, Straif K (2009) Meta-analysis of epidemiologic studies on cigarette smoking and liver cancer. Int J Epidemiol 38(6):1497–1511. doi: 10.1093/ije/dyp280 PubMedCrossRefGoogle Scholar
  16. 16.
    Wang C, Wang X, Gong G, Ben Q, Qiu W, Chen Y, Li G, Wang L (2012) Increased risk of hepatocellular carcinoma in patients with diabetes mellitus: a systematic review and meta-analysis of cohort studies. Int J Cancer 130(7):1639–1648. doi: 10.1002/ijc.26165 PubMedCrossRefGoogle Scholar
  17. 17.
    Alavanja MC, Hoppin JA, Kamel F (2004) Health effects of chronic pesticide exposure: cancer and neurotoxicity. Annu Rev Public Health 25:155–197. doi: 10.1146/annurev.publhealth.25.101802.123020 PubMedCrossRefGoogle Scholar
  18. 18.
    Centers for Disease Control and Prevention (2009) Fourth National Report on Human Exposure to Environmental Chemicals. http://www.cdc.gov/exposurereport/pdf/fourthreport.pdf. Accessed 01 Oct 14
  19. 19.
    Franklin C, Worgan J (2005) Occupational and residential exposure assessment for pesticides. Wiley, HobokenCrossRefGoogle Scholar
  20. 20.
    Rull RP, Ritz B (2003) Historical pesticide exposure in California using pesticide use reports and land-use surveys: an assessment of misclassification error and bias. Environ Health Perspect 111(13):1582–1589. doi: 10.1289/ehp.6118 PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Deziel NC, Friesen MC, Hoppin JA, Hines CJ, Thomas K, Freeman LE (2015) A review of nonoccupational pathways for pesticide exposure in women living in agricultural areas. Environ Health Perspect 123(6):515–524. doi: 10.1289/ehp.1408273 PubMedPubMedCentralGoogle Scholar
  22. 22.
    Dich J, Zahm SH, Hanberg A, Adami HO (1997) Pesticides and cancer. Cancer Causes Control 8 (3):420–443. doi: 10.1023/A:1018413522959 PubMedCrossRefGoogle Scholar
  23. 23.
    Gomaa AI, Khan SA, Toledano MB, Waked I, Taylor-Robinson SD (2008) Hepatocellular carcinoma: epidemiology, risk factors and pathogenesis. World J Gastroenterol 14(27):4300–4308. doi: 10.3748/wjg.14.4300 PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Jin X, Chen M, Song L, Li H, Li Z (2014) The evaluation of p, p’-DDT exposure on cell adhesion of hepatocellular carcinoma. Toxicology 322:99–108. doi: 10.1016/j.tox.2014.05.002 PubMedCrossRefGoogle Scholar
  25. 25.
    Jin XT, Song L, Zhao JY, Li ZY, Zhao MR, Liu WP (2014) Dichlorodiphenyltrichloroethane exposure induces the growth of hepatocellular carcinoma via Wnt/beta-catenin pathway. Toxicol Lett 225(1):158–166. doi: 10.1016/j.toxlet.2013.12.006 PubMedCrossRefGoogle Scholar
  26. 26.
    Rossi L, Barbieri O, Sanguineti M, Cabral JR, Bruzzi P, Santi L (1983) Carcinogenicity study with technical-grade dichlorodiphenyltrichloroethane and 1,1-dichloro-2,2-bis(p-chlorophenyl)ethylene in hamsters. Cancer Res 43(2):776–781PubMedGoogle Scholar
  27. 27.
    Turusov VS, Day NE, Tomatis L, Gati E, Charles RT (1973) Tumors in CF-1 mice exposed for six consecutive generations to DDT. J Natl Cancer Inst 51(3):983–997. doi: 10.1093/jnci/51.3.983 PubMedCrossRefGoogle Scholar
  28. 28.
    Cohn BA, Wolff MS, Cirillo PM, Sholtz RI (2007) DDT and breast cancer in young women: new data on the significance of age at exposure. Environ Health Perspect 115(10):1406–1414. doi: 10.1289/ehp.10260 PubMedPubMedCentralGoogle Scholar
  29. 29.
    Cocco P, Blair A, Congia P, Saba G, Ecca AR, Palmas C (1997) Long-term health effects of the occupational exposure to DDT. A preliminary report. Ann NY Acad Sci 837:246–256. doi: 10.1111/j.1749-6632.1997.tb56878.x PubMedCrossRefGoogle Scholar
  30. 30.
    Cocco P, Fadda D, Billai B, D’Atri M, Melis M, Blair A (2005) Cancer mortality among men occupationally exposed to dichlorodiphenyltrichloroethane. Cancer Res 65(20):9588–9594. doi: 10.1158/0008-5472.CAN-05-1487 PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Cocco P, Kazerouni N, Zahm SH (2000) Cancer mortality and environmental exposure to DDE in the United States. Environ Health Perspect 108(1):1–4. doi: 10.1289/ehp.001081 PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Evans AA, Chen G, Ross EA, Shen FM, Lin WY, London WT (2002) Eight-year follow-up of the 90,000-person Haimen City cohort: I. Hepatocellular carcinoma mortality, risk factors, and gender differences. Cancer Epidemiol Biomark Prev 11(4):369–376Google Scholar
  33. 33.
    Hardell L, Bengtsson NO, Jonsson U, Eriksson S, Larsson LG (1984) Aetiological aspects on primary liver cancer with special regard to alcohol, organic solvents and acute intermittent porphyria–an epidemiological investigation. Br J Cancer 50(3):389–397. doi: 10.1038/bjc.1984.188 PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Kauppinen T, Riala R, Seitsamo J, Hernberg S (1992) Primary liver cancer and occupational exposure. Scand J Work Environ Health 18(1):18–25. doi: 10.5271/sjweh0.1616 PubMedCrossRefGoogle Scholar
  35. 35.
    London WT, Evans AA, McGlynn K, Buetow K, An P, Gao L, Lustbader E, Ross E, Chen G, Shen F (1995) Viral, host and environmental risk factors for hepatocellular carcinoma: a prospective study in Haimen City, China. Intervirology 38(3–4):155–161PubMedGoogle Scholar
  36. 36.
    Stemhagen A, Slade J, Altman R, Bill J (1983) Occupational risk factors and liver cancer. A retrospective case–control study of primary liver cancer in New Jersey. Am J Epidemiol 117(4):443–454PubMedCrossRefGoogle Scholar
  37. 37.
    Suarez L, Weiss NS, Martin J (1989) Primary liver cancer death and occupation in Texas. Am J Ind Med 15(2):167–175. doi: 10.1002/ajim.4700150205 PubMedCrossRefGoogle Scholar
  38. 38.
    Moher D, Liberati A, Tetzlaff J, Altman DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 6(7):e1000097. doi: 10.1371/journal.pmed.1000097 PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Szklo M, Nieto FJ (2007) Epidemiology Beyond the Basics, 2nd edn. Jones and Bartlett, SudburyGoogle Scholar
  40. 40.
    Austin H, Delzell E, Grufferman S, Levine R, Morrison AS, Stolley PD, Cole P (1987) Case–control study of hepatocellular carcinoma, occupation, and chemical exposures. J Occup Med 29(8):665–669PubMedGoogle Scholar
  41. 41.
    Badawi AF, Michael MS (1999) Risk factors for hepatocellular carcinoma in Egypt: the role of hepatitis-B viral infection and schistosomiasis. Anticancer research 19(5C):4565–4569PubMedGoogle Scholar
  42. 42.
    Chang CK, Astrakianakis G, Thomas DB, Seixas NS, Ray RM, Gao DL, Wernli KJ, Fitzgibbons ED, Vaughan TL, Checkoway H (2006) Occupational exposures and risks of liver cancer among Shanghai female textile workers–a case-cohort study. Int J Epidemiol 35(2):361–369. doi: 10.1093/ije/dyi282 PubMedCrossRefGoogle Scholar
  43. 43.
    Cordier S, Le TB, Verger P, Bard D, Le CD, Larouze B, Dazza MC, Hoang TQ, Abenhaim L (1993) Viral infections and chemical exposures as risk factors for hepatocellular carcinoma in Vietnam. International journal of cancer Journal international du cancer 55(2):196–201. doi: 10.1002/ijc.2910550205 PubMedCrossRefGoogle Scholar
  44. 44.
    Dossing M, Petersen KT, Vyberg M, Olsen JH (1997) Liver cancer among employees in Denmark. Am J Ind Med 32(3):248–254. doi: 10.1002/(SICI)1097-0274(199709)32:33.0.CO;2-V PubMedCrossRefGoogle Scholar
  45. 45.
    Ezzat S, Abdel-Hamid M, Eissa SA, Mokhtar N, Labib NA, El-Ghorory L, Mikhail NN, Abdel-Hamid A, Hifnawy T, Strickland GT, Loffredo CA (2005) Associations of pesticides, HCV, HBV, and hepatocellular carcinoma in Egypt. Int J Hyg Environ Health 208(5):329–339. doi: 10.1016/j.ijheh.2005.04.003 PubMedCrossRefGoogle Scholar
  46. 46.
    Ferrand JF, Cenee S, Laurent-Puig P, Loriot MA, Trinchet JC, Degos F, Bronovicky JP, Pelletier G, Stucker I (2008) Hepatocellular carcinoma and occupation in men: a case–control study. J Occup Environ Med 50(2):212–220. doi: 10.1097/JOM.0b013e31815d88e2 PubMedCrossRefGoogle Scholar
  47. 47.
    Heinemann K, Willich SN, Heinemann LA, DoMinh T, Mohner M, Heuchert GE (2000) Occupational exposure and liver cancer in women: results of the Multicentre International Liver Tumour Study (MILTS). Occup Med (Lond) 50(6):422–429. doi: 10.1093/occmed/50.6.422 CrossRefGoogle Scholar
  48. 48.
    McGlynn KA, Abnet CC, Zhang M, Sun XD, Fan JH, O’Brien TR, Wei WQ, Ortiz-Conde BA, Dawsey SM, Weber JP, Taylor PR, Katki H, Mark SD, Qiao YL (2006) Serum concentrations of 1,1,1-trichloro-2,2-bis(p-chlorophenyl)ethane (DDT) and 1,1-dichloro-2,2-bis(p-chlorophenyl)ethylene (DDE) and risk of primary liver cancer. J Natl Cancer Inst 98(14):1005–1010. doi: 10.1093/jnci/djj266 PubMedCrossRefGoogle Scholar
  49. 49.
    Persson EC, Graubard BI, Evans AA, London WT, Weber JP, Leblanc A, Chen G, Lin W, McGlynn KA (2012) Dichlorodiphenyltrichloroethane and risk of hepatocellular carcinoma. Int J Cancer J int du Cancer 131(9):2078–2084. doi: 10.1002/ijc.27459 CrossRefGoogle Scholar
  50. 50.
    Porru S, Placidi D, Carta A, Gelatti U, Ribero ML, Tagger A, Boffetta P, Donato F (2001) Primary liver cancer and occupation in men: a case–control study in a high-incidence area in Northern Italy. Int J Cancer J Int du Cancer 94(6):878–883. doi: 10.1002/ijc.1538 CrossRefGoogle Scholar
  51. 51.
    Schiefelbein E, Zekri A-R, Newton D, Soliman G, Banerjee M, Hung C-W, Seifeldin I, Lo A-C, Soliman A (2012) Hepatitis C virus and other risk factors in hepatocellular carcinoma. Acta Virol 56(3):235PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Soliman AS, Hung CW, Tsodikov A, Seifeldin IA, Ramadan M, Al-Gamal D, Schiefelbein EL, Thummalapally P, Dey S, Ismail K (2010) Epidemiologic risk factors of hepatocellular carcinoma in a rural region of Egypt. Hepatol Int 4(4):681–690. doi: 10.1007/s12072-010-9187-1 PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    VoPham T, Brooks MM, Yuan JM, Talbott EO, Ruddell D, Hart JE, Chang CC, Weissfeld JL (2015) Pesticide exposure and hepatocellular carcinoma risk: a case–control study using a geographic information system (GIS) to link SEER-Medicare and California pesticide data. Environ Res 143(Pt A):68–82. doi: 10.1016/j.envres.2015.09.027 PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Zhao B, Shen H, Liu F, Liu S, Niu J, Guo F, Sun X (2012) Exposure to organochlorine pesticides is an independent risk factor of hepatocellular carcinoma: a case–control study. J Expo Sci Environ Epidemiol 22(6):541–548. doi: 10.1038/jes.2011.29 PubMedCrossRefGoogle Scholar
  55. 55.
    Fernandez-Cornejo J, Nehring R, Osteen C, Wechsler S, Martin A, Vialou A (2014) Pesticide use in US agriculture: 21 selected crops, 1960–2008, EIB-124. US Department of Agriculture, Economic Research ServiceGoogle Scholar
  56. 56.
    Environmental Protection Agency (2011) Pesticides Industry Sales and Usage: 2006 and 2007 Market Estimates. http://www.epa.gov/sites/production/files/2015-10/documents/market_estimates2007.pdf. Accessed 12 Jan 15
  57. 57.
    Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418(6898):671–677. doi: 10.1038/nature01014 PubMedCrossRefGoogle Scholar
  58. 58.
    Li Y, Zhang C, Yin Y, Cui F, Cai J, Chen Z, Jin Y, Robson MG, Li M, Ren Y, Huang X, Hu R (2014) Neurological effects of pesticide use among farmers in China. Int J Environ Res Public Health 11(4):3995–4006. doi: 10.3390/ijerph110403995 PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Dasgupta S, Meisner C, Wheeler D, Xuyen K, Thi Lam N (2007) Pesticide poisoning of farm workers-implications of blood test results from Vietnam. Int J Hyg Environ Health 210(2):121–132. doi: 10.1016/j.ijheh.2006.08.006 PubMedCrossRefGoogle Scholar
  60. 60.
    Peyre L, Zucchini-Pascal N, de Sousa G, Rahmani R (2012) Effects of endosulfan on hepatoma cell adhesion: epithelial-mesenchymal transition and anoikis resistance. Toxicology 300(1–2):19–30. doi: 10.1016/j.tox.2012.05.008 PubMedCrossRefGoogle Scholar
  61. 61.
    Galloway T, Handy R (2003) Immunotoxicity of organophosphorous pesticides. Ecotoxicology 12(1–4):345–363. doi: 10.1023/A:1022579416322 PubMedCrossRefGoogle Scholar
  62. 62.
    Voccia I, Blakley B, Brousseau P, Fournier M (1999) Immunotoxicity of pesticides: a review. Toxicol Ind Health 15(1–2):119–132. doi: 10.1177/074823379901500110 PubMedCrossRefGoogle Scholar
  63. 63.
    Longnecker MP, Rogan WJ, Lucier G (1997) The human health effects of DDT (dichlorodiphenyltrichloroethane) and PCBS (polychlorinated biphenyls) and an overview of organochlorines in public health. Annu Rev Public Health 18:211–244. doi: 10.1146/annurev.publhealth.18.1.211 PubMedCrossRefGoogle Scholar
  64. 64.
    Zhang Y, Han S, Liang D, Shi X, Wang F, Liu W, Zhang L, Chen L, Gu Y, Tian Y (2014) Prenatal exposure to organophosphate pesticides and neurobehavioral development of neonates: a birth cohort study in Shenyang, China. PloS one 9(2):e88491. doi: 10.1371/journal.pone.0088491 PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Wells J (2011) Pesticide Use Trends in California Agriculture. Environmental Solutions GroupGoogle Scholar
  66. 66.
    Environmental Protection Agency (2015) Persistent Organic Pollutants: A Global Issue, A Global Response. http://www.epa.gov/international-cooperation/persistent-organic-pollutants-global-issue-global-response. Accessed 21 Dec 2015
  67. 67.
    Faroon O, Harris MO, Llados F, Swarts S, Sage G, Citra M, Gefell D (2002) Toxicological profile for DDT, DDE, and DDD. ATSDR (Agency for Toxic Substances and Disease Registry)Google Scholar
  68. 68.
    Befeler AS, Di Bisceglie AM (2002) Hepatocellular carcinoma: diagnosis and treatment. Gastroenterology 122(6):1609–1619PubMedCrossRefGoogle Scholar
  69. 69.
    Chevrier J, Dewailly E, Ayotte P, Mauriege P, Despres J, Tremblay A (2000) Body weight loss increases plasma and adipose tissue concentrations of potentially toxic pollutants in obese individuals. International journal of obesity 24(10):1272–1278PubMedCrossRefGoogle Scholar
  70. 70.
    Angerer J, Bird MG, Burke TA, Doerrer NG, Needham L, Robison SH, Sheldon L, Zenick H (2006) Strategic biomonitoring initiatives: moving the science forward. Toxicol Sci 93(1):3–10PubMedCrossRefGoogle Scholar
  71. 71.
    Nasca PC, Pastides H (2008) Fundamentals of cancer epidemiology, 2nd edn. Jones and Bartlett Publishers, SudburyGoogle Scholar
  72. 72.
    Koutros S, Silverman DT, Alavanja MC, Andreotti G, Lerro CC, Heltshe S, Lynch CF, Sandler DP, Blair A, Freeman LEB (2015) Occupational exposure to pesticides and bladder cancer risk. Int J Epidemiol:dyv195Google Scholar
  73. 73.
    Wolff MS, Anderson HA, Britton JA, Rothman N (2007) Pharmacokinetic variability and modern epidemiology—the example of dichlorodiphenyltrichloroethane, body mass index, and birth cohort. Cancer Epidemiol Biomark Prev 16 (10):1925–1930CrossRefGoogle Scholar
  74. 74.
    Sobus J, Morgan M, Pleil J, Barr D (2010) Biomonitoring: uses and considerations for assessing non-occupational human exposure to pesticides. In: Krieger R (ed) Hayes’ Handbook of Pesticide Toxicology. Oxford, pp 1021–1036Google Scholar
  75. 75.
    NIH Research Portfolio Online Reporting Tools (2015) 5R01ES014662-03 Serum organochlorine levels and primary liver cancer: a nested case–control study. https://projectreporter.nih.gov/. Accessed 12 Jan 2015

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Trang VoPham
    • 1
    • 2
    Email author
  • Kimberly A. Bertrand
    • 3
  • Jaime E. Hart
    • 2
    • 4
  • Francine Laden
    • 1
    • 2
    • 4
  • Maria M. Brooks
    • 5
  • Jian-Min Yuan
    • 5
    • 6
  • Evelyn O. Talbott
    • 5
  • Darren Ruddell
    • 7
  • Chung-Chou H. Chang
    • 8
  • Joel L. Weissfeld
    • 5
    • 6
  1. 1.Department of EpidemiologyHarvard T. H. Chan School of Public HealthBostonUSA
  2. 2.Channing Division of Network MedicineBrigham and Women’s Hospital and Harvard Medical SchoolBostonUSA
  3. 3.Slone Epidemiology CenterBoston UniversityBostonUSA
  4. 4.Department of Environmental HealthHarvard T. H. Chan School of Public HealthBostonUSA
  5. 5.Department of Epidemiology, Graduate School of Public HealthUniversity of PittsburghPittsburghUSA
  6. 6.Division of Cancer Control and Population SciencesUniversity of Pittsburgh Cancer InstitutePittsburghUSA
  7. 7.Spatial Sciences InstituteUniversity of Southern CaliforniaLos AngelesUSA
  8. 8.Division of General Internal MedicineUniversity of Pittsburgh School of MedicinePittsburghUSA

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