Endocrine disrupting pesticides: A leading cause of cancer among rural people in Pakistan

Experimental Oncology

Volumn 26, Issue 2, 2004, Pages 98-105

  Ejaz, Sohail ^a   Akram, Waseem ^a   Lim, Chae Woong ^a   Lee, Jong Jin ^a   Husain, Imtiaz ^b  

^a Chonbuk National University   (South Korea)

^b Basic Health Unit   (Pakistan)

Author keywords

Cancer; Endocrine disruptors; Farmer; Pesticides

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; CHLORPHENOTANE; ORGANOCHLORINE PESTICIDE; PHTHALIC ACID BIS(2 ETHYLHEXYL) ESTER; POLYCHLORINATED BIPHENYL; TRIAZINE DERIVATIVE; TRIBUTYLTIN; CARCINOGEN; ENDOCRINE DISRUPTOR; HERBICIDE; PESTICIDE;

AGRICULTURAL WORKER; BREAST CANCER; CANCER; CANCER RESEARCH; CANCER RISK; CARCINOGENESIS; ENDOCRINE FUNCTION; ENVIRONMENTAL EXPOSURE; HORMONE DEPENDENCE; HUMAN; NONHUMAN; OCCUPATIONAL EXPOSURE; OVARY CANCER; PAKISTAN; PROSTATE CANCER; REVIEW; RURAL AREA; TESTIS CANCER; THYROID CANCER; ACUTE DISEASE; ARTICLE; CHRONIC DISEASE;

AGRICULTURE; ENDOCRINE SYSTEM; HUMANS; NEOPLASMS; OCCUPATIONAL EXPOSURE; PAKISTAN; PESTICIDES; RISK FACTORS; RURAL POPULATION;

EID: 3242777060     PISSN: 02043564     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (98)

1. Pimentel D. Green revolution agriculture and chemical hazards. Sci Total Eviron 1996; 1: 86-98.
2. Fleming LE, Bean JA, Rudolph M, Hamilton K. Mortality in a cohort of licensed pesticide applicators in Florida. Occup Environ Med 1999; 56: 14-21.
3. Perry MJ, Layde PM. Sources, routes, and frequency of pesticide exposure among farmers. JOEM 1998; 40: 697-701.
4. Martin SAJr, Sandler DP, Harlow SD, Shore DL, Rowland AS, Alavanja MC. Pesticide use and pesticide-related symptoms among black farmers in the Agricultural Health Study. Am J Int Med 2002; 41: 202-9.
5. Veil JF. Public health impact of pesticides used in agriculture, Geneva, Switzerland. WHO (World Health Organization), 1990.
6. Smith C. Pesticide exports from US ports, 1997-2000. Int J Occup Environ Health 2001; 7: 266-74.
7. Birnbaum LS, Fenton SE. Cancer and developmental exposure to endocrine disruptors. Environ Health Perspect 2003; 111: 389-94.
8. Mathur V, Bhatnagar P, Sharma RG, Acharya V, Sexana R. Breast cancer incidence and exposure to pesticides among women originating from Jaipur. Environ Int 2002; 28: 331-6.
9. Alomar MA, Abbas AK, Alobaidy AS. Combined effect of exposure to lead and chlordane on the testicular tissues of swiss mice. Toxicol Lett 2000; 115: 1-8.
10. Bounias M. Etiological factors and mechanism involved in relationships between pesticide exposure and cancer. J Environ Biol 2003; 24: 1-8.
11. Potti A, Panwalkar AW, Langness E. Prevalence of pesticide exposure in young males with adenocarcinoma of the prostate. J Carcinog 2003; 2: 4.
12. US Environmental Protection Agency: special report on environmental endocrine disruption: an effects assessment and analysis, EPA, Washington, 1997, EPA Report No. EPA/630/R-96/012.
13. Barry P, Paul H. Overview of the endocrine disrupters. Issues in environmental science and technology No. 12. Endocrine disrupting chemicals. The Royal Society of Chemistry, 1999.
14. Silbergeld EK, Flaws JA, Brown KM. Organizational and activational effects of estrogenic endocrine disrupting chemicals. Cad Saude Publica 2002; 18: 495-504.
15. Kannan K, Tanabe S, Tatsukawa R. Geographical distribution and accumulation features of organochlorine residues in fish of tropical Asia and Oceania. Environ Sci Technol 1995; 26: 73-83.
16. Heberer T, Dunnbier U. DDT metabolite bis(chlorophenyl)acetic acid: the neglected environmental contaminant. Environ Sci Technol 1999; 33: 2346-51.
17. Gong ZM, Tao S, Xu FL, Dawson R, Liu WX, Cui YH, Cao J, Wang XJ, Shen WR, Zhang WJ, Qing BP, Sun R. Level and distribution of DDT in surface soils from Tianjin, China. Chemosphere 2004; 54: 1247-53.
18. Agency for Toxic Substances and Disease Registry, US Department of Health and Human Services, 2000. Toxicological Profile for DDT, DDE and DDD (update): draft for public comment.
19. IARC monographs on the evaluation of carcinogenic risks to humans. Polychlorinated dibenzo-para-dioxins and polychlorinated dibenzofurans. Lyon: IARC 1997; 69:333-44.
20. Tsuda H, Moore MA, Fukushima S, Nakae D, Imaida K, Tatematsu M. Value of GST-P positive preneoplastic hepatic foci in dose-response studies of hepatocarcinogenesis: evidence for thresholds with both genotoxic and non-genotoxic carcinogens. Toxicol Pathol 2003; 31: 80-6.
21. Lopez-Cervantes M, Torres-Sanchez L, Tobias A, Lopez-Carrillo L. Dichlorodiphenyldichloroethane burden and breast cancer risk: a meta-analysis of the epidemiologic evidence. Environ Health Perspect 2004; 112: 207-14.
22. Pavuk M, Cerhan JR, Lynch CF, Schecter A, Petrik J, Chovancova J, Kocan A. Environmental exposure to PCBs and cancer incidence in eastern Slovakia. Chemosphere 2004; 54: 1509-20.
23. Bounias M. Etiological factors and mechanism involved in relationships between pesticide exposure and cancer. J Environ Biol 2003; 24: 1-8.
24. Tabb MM, Kholodovych V, Grun F, Zhou C, Welsh WJ, Blumberg B. Highly chlorinated PCBs inhibit the human xenobiotic response mediated by the steroid and xenobiotic receptor (SXR). Environ Health Perspect 2004; 112: 163-9.
25. Tharappel JC, Lee EY, Robertson LW, Spear BT, Glauert HP. Regulation of cell proliferation, apoptosis and transcription factor activities during the promotion of liver carcinogenesis by polychlorinated biphenyls. Toxicol Appl Pharmacol 2002; 179: 172-84.
26. Nakanishi Y, Bai F, Inoue K, Takayama K, Pei XH, Harada T. Polychlorinated biphenyls promotes 1-nitropyrene-induced lung tumorigenesis without the induction of K-ras gene mutation in A/J mice. Teratog Carcinog Mutagen 2001; 21: 395-403.
27. Whysner J, Wang CX. Hepatocellular iron accumulation and increased cell proliferation in polychlorinated biphenyl-exposed Sprague-Dawley rats and the development of hepatocarcinogenesis. Toxicol Sci 2001; 62: 36-45.
28. Desaulniers D, Leingartner K, Russo J, Perkins G, Chittim BG, Archer MC. Modulatory effects of neonatal exposure to TCDD or a mixture of PCBs, p,p′-DDT and p,p′-DDE, on methylnitrosourea-induced mammary tumor development in the rat. Environ Health Perspect 2001; 109: 739-47.
29. Negri E, Bosetti C, Fattore E, La Vecchia C. Environmental exposure to polychlorinated biphenyls (PCBs) and breast cancer: a systematic review of the epidemiological evidence. Eur J Cancer Prev 2003; 12: 509-16.
30. Vreugdenhil HJ, Mulder PG, Emmen HH, Weisglas-Kuperus N. Effects of perinatal exposure to PCBs on neuropsychological functions in the rotterdam cohort at 9 years of age. Neuropsychology 2004; 18: 185-93.
31. Woolcott CG, Aronson KJ, Hanna WM, Sengupta SK, McCready DR, Stems EE, Miller AB. Organochlorines and breast cancer risk by receptor status, tumor size and grade (Canada). Cancer Causes Control 2001; 12: 395-404.
32. Pohjanvirta R, Tuomisto J. Short-term toxicity of 2,3,7,8- tetrachlorodibenzo-p-dioxin in laboratory animals: effects, mechanisms, and animal models. Pharmacol Rev 1994; 46: 483-549.
33. Ushinohama K, Son D, Roby KF, Rozman KK, Terranova PF. Impaired ovulation by 2,3,7,8 tetrachlorodibenzo-p-dioxin (TCDD) in immature rats treated with equine chorionic gonadotropin. Reprod Toxicol 2001; 15: 275-80.
34. Guo SW. The link between exposure to dioxin and endometriosis: a critical reappraisal of primate data. Gynecol Obstet Invest 2004; 57: 157-73.
35. IARC monographs on the evaluation of carcinogenic risks to humans. Polychlorinated dibenzo-para-dioxins and polychlorinated dibenzofurans. Lyon: IARC 1997; 69: 33-44.
36. Fenton SE, Hamm JT, Birnbaum LS, Youngblood GL. Persistent abnormalities in the rat mammary gland following gestational and lactational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Toxicol Sci 2002; 67: 63-74.
37. Teraoka H, Dong W, Ogawa S, Tsukiyama S, Okuhara Y, Niiyama M, Ueno N, Peterson RE, Hiraga T. 2,3,7,8-tetrachlorodibenzo-p-dioxin toxicity in the zebrafish embryo: altered regional blood flow and impaired lower jaw development. Toxicol Sci 2002; 65: 192-9.
38. Partanen AM, Kiukkonen A, Sahlberg C, Alaluusua S, Thesleff I, Pohjanvirta R, Lukinmaa PL. Developmental toxicity of dioxin to mouse embryonic teeth in vitro: arrest of tooth morphogenesis involves stimulation of apoptotic program in the dental epithelium. Toxicol Appl Pharmacol 2004; 194: 24-33.
39. Alaluusua S, Lukinmaa PL, Torppa J, Tuomisto J, Vartiainen T. Developing teeth as biomarker of dioxin exposure. Lancet 1999; 353: 206.
40. Tuomisto JT, Pekkanen J, Kiviranta H, Tukiainen E, Vartiainen T, Tuomisto J. Soft-tissue sarcoma and dioxin: a case-control study. Int J Cancer 2004; 108: 893-900.
41. IARC Monographs on the evaluation of carcinogenic risks to humans. Overall evaluations of carcinogenicity. Supplement 7. Lyon, France: IARC, 1987; 440.
42. Ito N, Fukushima S, Tamano S, Hirose M, Hagiwara A. Dose response in butylated hydroxyanisole induction of forestomach carcinogenesis in F344 rats. J Natl Cancer Inst 1986; 77: 1261-5.
43. Clayson DB, Iverson F, Nera EA, Lok E. Early indicators of potential neoplasia produced in the rat forestomach by non-genotoxic agents: the importance of induced cellular proliferation. Mutat Res 1991; 248: 321-31.
44. Nera EA, Iverson F, Lok E, Armstrong CL, Karpinski K, Clayson DB. A carcinogenesis reversibility study of the effects of butylated hydroxyanisole on the forestomach and urinary bladder in male Fischer 344 rats. Toxicology 1988; 53: 251-68.
45. Schroeder JC, Olshan AF, Baric R, Dent GA, Weinberg CR, Yount B. Agricultural risk factors for (14; 18) subtypes of non-Hodgkin's lymphoma. Epidemiology 2001; 12: 701-9.
46. Hopenhayn-Rich C, Stump ML, Browning SR. Regional assessment of atrazine exposure and incidence of breast and ovarian cancers in Kentucky. Arch Environ Contam Toxicol 2002; 42: 127-36.
47. Pinter A, Torok G, Borzsonyi M, Surjan A, Csik M, Kelecsenyi Z. Long-term carcinogenicity bioassay of the herbicide atrazine in F344 rats. Neoplasma 1990; 37: 533-44.
48. Donna A, Betta PG, Robutti F, Bellingeri D. Carcinogenicity testing of atrazine: preliminary report on a 13-month study on male Swiss albino mice treated by intraperitoneal administration. G Ital Med Lav 1986; 8: 119-21.
49. Agency for Toxic Substances and Disease Registry. Toxicological profile for di(2-ethylhexyl) phthalate. Update. (Draft for public comment). Atlanta, GA: ATSDR, Public Health Service, U.S. Department of Health and Human Services, 2000; 287.
50. IARC monographs on the evaluation of carcinogenic risks to humans. Some industrial chemicals and dye-stuffs. Lyon: IARC 1982; 29: 257-68.
51. IARC monographs on the evaluation of the carcinogenic risk of chemicals to humans. Some industrial chemicals. Lyon, France: IARC, 2000; 77: 564.
52. Melnick RL. Is peroxisome proliferation an obligatory precursor step in the carcinogenicity of di(2-ethylhexyl) phthalate (DEHP)? Environ Health Perspect 2001; 109: 437-42.
53. Hoch M, Alonso-Azcarate J, Lischick M. Assessment of adsorption behavior of dibutyltin (DBT) to clay-rich sediments in comparison to the highly toxic tributyltin (TBT). Environ Pollut 2003; 123: 217-27.
54. Manseuto C, Villa L, Agati PD, Marciano V, Pellerito C, Fiore T, Scopelliti M, Nagy L, Pellerito L. Effect of tributyltin (IV) chloride on the fertilization of Styela Plicata (Ascidiacea: Tunicata): II. Scaning and transmission electron microscopy studies. Appl Organometal Chem 2003; 17: 553-60.
55. Kannan K, Guruge KS, Thomas NJ, Tanabe S, Giesy JP. Butyltin residues in southern sea otters (Enhydra lutris nereis) found dead along California coastal waters. Environ Sci Technol 1998; 32: 1169-75.
56. Anderson RS, Unger MA, Burreson EM. Enhancement of Perkinsus marinus disease progression in TBT-exposed oysters (Crossostrea virginica). Mar Environ Res 1996; 42: 177-80.
57. Ghoneum M, Hussein AE, Gill G, Alfred LJ. Suppression of murine natural killer cell activity by tributyltin: in vivo and in vitro assessment. Environ Res 1990; 52: 178-86.
58. Hanna M. Expression of metastatic potential of tumor cells in young nude mice is correlated with low levels of naturalkiller-cell mediated cytotoxicity. Int J Cancer 1989; 26: 675-90.
59. Whalen MM, Green SA, Loganathan BG. Brief butyltin exposure induces irreversible inhibition of the cytotoxic function on human natural killer cells, in vitro. Environ Res 2002; 88: 19-29.
60. Baloch UK. Problems associated with the use of chemicals by agricultural workers. Basic Life Sci 1985; 34: 63-78.
61. Economic Survey, Govt of Pakistan. 1999-2000.
62. Technical bulletin, Directorate of pest warning and quality control of pesticides, Punjab 2000.
63. Wesseling C, Antich D, Hogstedt C, Rodriguez AC, Ahlbom A. Geographical differences of cancer in Costa Rica in relation to environmental and occupational pesticide exposure. Int J Epidemiology 1999; 28: 365-74.
64. Krawinkel MB, Plehn G, Kruse H, Kasi AM. Organochlorine residues in Baluchistan/Pakistan: blood and fat concentrations in humans. Bull Environ Contam Toxicol 1989; 43: 821-6.
65. Cancer registry, Shaukat khanum memorial cancer hospital and research centre. 1994-2002.
66. Starek A. Estrogens and organochlorine xenoestrogens and breast cancer risk. Int J Occup Med Environ Health 2003; 16: 113-24.
67. Muscat JE, Britton JA, Djordjevic MV, Citron ML, Kemeny M, Busch-Devereaux E, Pittman B, Stellman SD. Adipose concentrations of organochlorine compounds and breast cancer recurrence in Long Island, New York. Cancer Epidemiol Biomarkers Prev 2003; 12: 1474-8.
68. Bounias M. Etiological factors and mechanism involved in relationships between pesticide exposure and cancer. Environ Biol 2003; 24: 1-8.
69. Zou E, Matsumura F. Long-term exposure to beta-hexachlorocyclohexane (beta-HCH) promotes transformation and invasiveness of MCF-7 human breast cancer cells. Biochem Pharmacol 2003; 66: 831-40.
70. Cabello G, Juarranz A, Botella LM, Calaf GM. Organophosphorous pesticides in breast cancer progression. J Submicrosc Cytol Pathol 2003; 35: 1-9.
71. Birnbaum LS, Fenton SE. Cancer and developmental exposure to endocrine disruptors. Environ Health Perspect 2003; 111: 389-94.
72. Daly M, Obrams GI. Epidemiology and risk assessment for ovarian cancer. Seminars in Oncology 1998; 25: 255-64.
73. Donna A, Crosignani P, Robutti F, Betta PG, Bocca R, Mariani N, Ferrario F, Fissi R, Berrino F. Triazine herbicides and ovarian epithelial neoplasms. Scand J Work Environ Health 1989; 15: 47-53.
74. Koifman S, Koifman RJ, Meyer A. Human reproductive system disturbances and pesticide exposure in Brazil. Cad Saude Publica 2002; 18: 435-45.
75. Dich J, Zahm SH, Hanberg A, Adami HO. Pesticides and cancer. Cancer Causes Control 1997; 8: 420-43.
76. Mettlin CJ, Murphy GP, Rosenthal DS, Menck HR. The National Cancer Data Base report on prostate carcinoma after the peak in incidence rates in the U.S. The American College of Surgeons Commission on Cancer and the American Cancer Society. Cancer 1998; 83: 1679-84.
77. Satariano WA, Ragland KE, Van Den Eeden SK. Cause of death in men diagnosed with prostate carcinoma. Cancer 1998; 83: 1180-8.
78. Fleming LE, Bean JA, Rudolph M, Hamilton K. Mortality in a cohort of licensed pesticide applicators in Florida. Occup Environ Med 1999, 56: 14-21.
79. Morrison H, Savitz D, Semenciw R, Hulka B, Mao Y, Morison D, Wigle D. Farming and prostate cancer mortality. Am J Epidemiol 1993; 137: 270-80.
80. Fleming LE, Bean JA, Rudolph M, Hamilton K. Cancer incidence in a cohort of licensed pesticide applicators in Florida. J Occup Environ Med 1999; 41: 279-88.
81. Fleming LE, Bean JA, Rudolph M, Hamilton K. Mortality in a cohort of licensed pesticide applicators in Florida. J Occup Environ Med 1999; 56: 14-21.
82. Potti A, Panwalkar AW, Langness E. Prevalence of pesticide exposure in young males (
83. Devesa SS, Blot WJ, Stone BJ, Miller BA, Tarone RE, Fraumeni JFJr. Recent cancer trends in the United States. J Natl Cancer Inst 1995; 87: 175-82.
84. Bergstrom R, Adami HO, Mohner M, Zatonski W, Storm H, Ekbom A, Tretli S, Teppo L, Akre O, Hakulinen T. Increase in testicular cancer incidence in six European countries: a birth cohort phenomenon. J Natl Cancer Inst 1996; 88: 727-33.
85. Gray LEJr. Xenoendocrine disrupters: laboratory studies on male reproductive effects. Toxicol Lett 1998; 28: 102-3.
86. Weir HK, Marrett LD, Kreiger N, Darlington GA, Sugar L. Pre-natal and peri-natal exposures and risk of testicular germ-cell cancer. Int J Cancer 2000; 87: 438-43.
87. Kristensen P, Andersen A, Irgens LM, Bye AS, Vagstad N. Testicular cancer and parental use of fertilizers in agriculture. Cancer Epidem Biomark Prev 1996; 5: 3-9.
88. Murakami M, Hosokawa S, Yamada T, Harakawa M, Ito M, Koyama Y, Kimura J, Yoshitake A, Yamada H. Species-specific mechanism in rat Leydig cell tumorigenesis by procymidone. Toxicol Appl Pharmacol 1995; 131: 244-52.
89. Fowler KA, Gill K, Kirma N, Dillehay DL, Tekmal RR. Overexpression of aromatase leads to development of testicular Leydig cell tumors: an in vivo model for hormone-mediated testicular cancer. Am J Pathol 2000; 156: 347-53.
90. Banu SK, Govindarajulu P, Aruldhas MM. Testosterone and estradiol differentially regulate TSH-induced thyrocyte proliferation in immature and adult rats. Steroids 2002; 67: 573-9.
91. Cheek AO, Kow K, Chen J, McLachlan JA. Potential mechanisms of thyroid disruption in humans: interaction of organochlorine compounds with thyroid receptor, transthyretin, and thyroid-binding globulin. Environ Health Perspect 1999; 107; 273-8.
92. Kohn MC, Sewall CH, Lucier GW, Poriter CJ. A mechanistic model of effects of dioxin on thyroid hormones in the rat. Toxicol Appl Pharmacol 1996; 136: 29-48.
93. Calvert GM, Sweeney MH, Deddens J, Wall DK. Evaluation of diabetes mellitus, serum glucose, and thyroid function among United States workers exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Occup Environ Med 1999; 56: 270-6.
94. Zhou LX, Dehal SS, Kupfer D, Morrell S, McKenzie BA, Eccleston EDJr, Holtzman JL. Cytochrome P450 catalyzed covalent binding of methoxychlor to rat hepatic, microsomal iodothyronine 5′-monodeiodinase, type I: does exposure to methoxychlor disrupt thyroid hormone metabolism? Arch Biochem Biophys 1995; 322: 390-94.
95. Wilson AG, Thake DC, Heydens WE, Brewster DW, Hotz KJ. Mode of action of thyroid tumor formation in the male Long-Evans rat administered high doses of alachlor. Fund Appl Toxicol 1996; 33: 16-23.
96. Pavuk M, Cerhan JR, Lynch CF, Schecter A, Petrik J, Chovancova J, Kocan A. Environmental exposure to PCBs and cancer incidence in eastern Slovakia. Chemosphere 2004; 54: 1509-20.
97. Hurley PM. Mode of carcinogenic action of pesticides inducing follicular cell tumors in rodents. Environ Health Persp 1998; 106: 437-45.
98. rd ed, Zenz C, Dickerson OB, Horvath JrEP, ed. St Louis: Mosby-Year Book, Inc, 1994; 836-69.