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Viruses, chemicals and co-carcinogenesis

Abstract

The etiology of cancers appears to be complex and multifactorial. Peyton Rous and others demonstrated the process of co-carcinogenesis by exposing rabbits to a virus and tars. Epidemiologists have proposed virus–chemical interactions to cause several cancers. For example, one might propose that the etiology of cervical cancer results from a complex interplay between oncogenic viruses and cervical tar exposures through tar-based vaginal douching, cigarette smoking, and/or long-term cooking over wood-burning stoves in poorly ventilated kitchens. Hepatocellular carcinoma may result from the joint effects of viruses and hepatotoxic chemical carcinogens. Kaposi's sarcoma might happen following reciprocal actions of human herpes virus-8 infection, immunosuppression, and chemical exposures, such as nitrite radicals and alumino-silicates. Use of Koch's postulates will not help one prove or disprove a multifactorial causation of disease; new criteria are needed. Delineating the web of causation may lead to additional strategies for prevention and treatment of several cancers.

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References

  • Armstrong BK, Munoz N and Bosch FX . (1992). Epidemiology of Cancer of the Cervix Coppleson M (ed). Gynecologic Oncology, 2nd edn Churchill Livingstone: Edinburgh, pp. 11–28.

    Google Scholar 

  • Anonymous . (1996). NIH Consensus Conference April 1–3, Vol. 14, pp. 1–29.

  • Barre-Sinoussi F, Chermann JC, Rey F, Nugeyre MT, Chamaret S, Gruest J, Dauguet C, Axler-Blin C, Vezinet-Brun F, Rouzioux C, Rozenbaum W and Montagnier L . (1983). Science, 220, 868–871.

  • Beasley RP, Hwang LY, Lin C-C and Chien CS . (1981). Lancet, 11, 1128–1133.

  • Beers FG . (1973). Br. J. Cancer, 27, 473–484.

  • Beral V, Peterman TA, Berkelman RL and Jaffe HW . (1990). Lancet, 335, 123–128.

  • Berenblum I . (1954). Adv. Cancer Res., 2, 129–175.

  • Bosch FX, Manos MM, Munoz N, Sherman M, Jansen AM and Peto J . (1995). J. Natl. Cancer Inst., 87, 796–802.

  • Bosch FX, Munoz N, De Sanjose S, Izarzugaza I, Gili M, Viladiu P, Tormo MJ, Moreo P, Ascunce N and Gonzalez LC . (1992). Int. J. Cancer, 52, 750–758.

  • Boshart M, Gissmann L, Ikenberg H, Kleinheinz A, Scheurlen W and zur Hausen H . (1984). EMBO J., 3, 1151–1157.

  • Cannon MJ, Dollard SC, Black JB, Edlin BR, Hannah C, Hogan SE, Patel MM, Jaffe HW, Offermann MK, Spira TJ, Pellett PE and Gunthel CJ . (2003). AIDS, 17, 215–222.

  • Carbone M, Pass HI, Miele L and Bocchetta M . (2003). Oncogene, 22, 5173–5180.

  • Castle PE, Wacholder S, Lorincz AT, Scott DR, Sherman ME, Glass AG, Rush BB, Schussler JE and Schiffman M . (2002). J. Natl. Cancer Inst., 94, 1406–1414.

  • Chang M-H, Chen C-J, Lai M-S, Hsu H-M, Wu T-C, Kong M-S, Liang D-C, Shau W-Y and Chen D-S . (1997). N. Engl. J. Med., 336, 1855–1859.

  • Chang Y, Cesarman E, Pessin MS, Lee F, Culpepper J, Knowles DM and Moore PS . (1994). Science, 266, 1865–1869.

  • Chen C-J and Chen D-S . (2002). Hepatology, 36, 1046–1049.

  • Chen C-J, Yu M-W and Liaw Y-F . (1997). J. Gastroenterol. Hepatol., 12 (Suppl), S294–S308.

  • Daling JR, Madeleine MM, McKnight B, Carter JJ, Wipf GC, Ashley R, Ashley R, Schwartz SM, Beckmann AM, Hagensee ME, Mandelson MT and Galloway DA . (1996). Cancer Epidemiol. Biomarkers Prev., 5, 541–548.

  • Dal Maso L, Serraino D and Franceschi S . (2001). Eur. J. Cancer, 37, 1188–1201.

  • Day GL, Blot WJ, McLaughlin JK and Fraumeni Jr JF . (1994). Int. J. Cancer, 59, 319–321.

  • Drotman DP, Peterman TA and Friedman-Kien AE . (1995). Dermatol. Clin., 13, 575–582.

  • Duran-Reynals F . (1957). Texas Rep. Biol. Med., 15, 306–333.

  • Durst M, Gissmann L, Ikenberg H and zur Hausen H . (1983). Proc. Natl. Acad. Sci., 80, 3812–3815.

  • Evans AS . (1982). Yale J. Biol. Med., 55, 193–199.

  • Evans AS and Mueller NE . (1990). Ann. Epidemiol., 1, 71–92.

  • Ferlay J, Bray R, Pisani P and Parkin DM . (2001). Globocan 2000: Cancer Incidence, Mortality and Prevalence Worldwide. World Health Organization. IARC Press: Lyon.

    Google Scholar 

  • Ferrera A, Velema JP, Figueroa M, Bulnes R, Toro LA, de Barahona O and Melchers WJ . (2000). Int. J. Epidemiol., 29, 817–825.

  • Frenkel N, Roizman B, Cassai E and Nahmias A . (1972). Proc. Natl. Acad. Sci. USA, 69, 3784–3789.

  • Friedman-Kien AE . (1989). Color Atlas of AIDS. WB Saunders Co: Philadelphia.

    Google Scholar 

  • Galloway DA . (2003). Lancet Infect. Dis., 3, 469–475.

  • Garrett LR, Perez-Reyes N, Smith PP and McDougall JK . (1993). Carcinogenesis, 14, 329–332.

  • Gillison M and Shah KV . (2003). J. Natl. Cancer Inst. Monogr., 31, 57–65.

  • Hassan MM, Hwang LY, Hatten CJ, Swaim M, Li D, Abbruzzese JI, Beasley P and Patt YZ . (2002). Hepatology, 36, 1206–1213.

  • Haverkos HW . (1996). Biomed. Pharmacother., 50, 318–319.

  • Haverkos HW and Curran JW . (1982). Ca-A Cancer J. Clin., 32, 330–339.

  • Haverkos HW and Drotman DP . (1995). Genetica, 95, 157–164.

  • Haverkos HW, Kopstein AN, Wilson H and Drotman P . (1994). Environ. Health Perspect., 102, 858–861.

  • Haverkos HW, Pinsky PF, Drotman DP and Bregman DJ . (1985). Sex Transm. Dis., 12, 203–208.

  • Haverkos H, Rohrer M and Pickworth W . (2000). Biomed. Pharmacother., 54, 54–59.

  • Haverkos HW, Soon G, Steckley SL and Pickworth W . (2003). Biomed. Pharmacother., 57, 67–77.

  • Hildesheim A, Herrero R, Castle PE, Wacholder S, Bratti MC, Sherman ME, Lorincz AT, Burk RD, Morales J, Rodriguez AC, Helgesen K, Alfaro M, Hutchinson M, Balmaceda I, Greenberg M and Schiffman M . (2001). Br. J. Cancer, 84, 1219–1226.

  • Hildesheim A, Mann V, Brinton LS, Szklo M, Reeves WC and Rawls WE . (1991). Int. J. Cancer, 49, 335–340.

  • Ho GY, Bierman R, Beardsley L, Chang CJ and Burk RD . (1998). N. Engl. J. Med., 338, 423–428.

  • Ho GYF, Burk RD, Klein S, Kadish AS, Chang CJ, Palan P, Basu J, Tachezy R, Lewis R and Romney S . (1995). J. Natl. Cancer Inst., 87, 1365–1371.

  • Holly EA, Lele C and Bracci PM . (1998). Am. J. Public Health, 88, 1767–1773.

  • Huang MH, Chen C-J, Lai M-S, Hsu M-H, Wu T-C, Kong M-S, Liang D-C, Shau W-Y and Chen D-S . (1997). N. Engl. J. Med., 336, 1855–1859.

  • Kew MC . (2002). Toxicology, 181–182, 35–38.

  • Koutsky LA, Holmes KK, Critchlow CW, Stevens CE, Paavonen J, Beckman AM, DeRouen TA, Galloway DA, Vernon D and Kiviat NB . (1992). N. Engl. J. Med., 327, 1272–1278.

  • Lombard HL and Potter EA . (1950). Cancer, 3, 960–968.

  • Martin CM, Magnusson S, Goscienski PJ and Hansen GF . (1961). Science, 134, 1985–1986.

  • Mendis LN, Best JM and Banatvala JE . (1981). Int. J. Cancer, 27, 669–677.

  • Ming L, Thorgeirsson SS, Gail MH, Lu P, Harris CC, Wang N, Shao Y, Wu Z, Liu G, Wang X and Sun A . (2002). Hepatology, 36, 1214–1220.

  • Mirvish SS, Williamson J, Babcook D and Chen SC . (1993). Environ. Mol. Mutagen., 21, 247–252.

  • Moore PS and Chang YC . (1995). N. Engl. J. Med., 332, 1181–1185.

  • Osmond DH, Buchbinder S, Cheng A, Graves A, Vittinghoff E, Cossen CK, Forghani B and Martin JN . (2002). JAMA, 287, 221–225.

  • Papanicolaou GN and Traut HF . (1941). Am. J. Obstet. Gynecol., 42, 193–205.

  • Popovic M, Sarngadharan MC, Read E and Gallo RC . (1984). Science, 224, 497–500.

  • Prokopczyk B, Cox JE, Hoffmann D and Waggoner SE . (1997). J. Natl. Cancer Inst., 89, 868–873.

  • Rogers S and Rous P . (1951). J. Exp. Med., 93, 459–486.

  • Root-Bernstein RS . (1993). Rethinking AIDS: The Tragic Cost of Premature Consensus. The Free Press: New York, pp. 104–109.

    Google Scholar 

  • Rothman N, Cantor KP, Blair A, Bush D, Brock JW, Helzlsouer K, Zahm SH, Needham LL, Pearson GR, Hoover RN, Comstock GW and Strickland PT . (1997). Lancet, 350, 240–244.

  • Rotkin ID . (1967). Am. J. Public Health Nations Health, 57, 815–829.

  • Rous P . (1911). JAMA, 56, 198.

  • Rous P . (1965). Nature, 207, 457–458.

  • Rous P and Beard JW . (1934). J. Exp. Med., 60, 741–766.

  • Rous P and Kidd JG . (1938). J. Exp. Med., 67, 399–428.

  • Rowe PC, Valle D and Brusilow SW . (1988). JAMA, 260, 3167–3170.

  • Rowson KE, Roe FJ, Ball JK and Salaman MH . (1961). Nature, 191, 893–895.

  • Salaman MH and Roe FJ . (1964). Br. Med. Bull., 20, 139–144.

  • Smith FR . (1931). Am. J. Obstet. Gynecol., 21, 18–25.

  • Smith JS, Herrero R, Bosetti C, Munoz N, Bosch FX, Eluf-Neto J, Castellsague X, Meijer CJ, Van den Brule AJ, Franceschi S, Ashley R and International Agency for Research on Cancer Multicentric Cervical Cancer Study Group. (2002). J. Natl. Cancer Inst., 94, 1604–1613.

  • Southam CM . (1963). Cancer Res., 23, 1105–1115.

  • Steckley SL, Pickworth WB and Haverkos HW . (2003). Biomed. Pharmacother., 57, 78–83.

  • Stoker M . (1963). Nature, 200, 756–758.

  • Sun ZT, Lu PX, Gail MH, Pee D, Zhang QN, Ming LH, Wang NJ, Wu Y, Liu G, Wu Y and Zhu Y . (1999). Hepatology, 30, 379–383.

  • Sylla A, Diallo MS, Categnaro J and Wild CP . (1999). Mutat. Res., 428, 187–196.

  • Tanaka S and Southam CM . (1962). J. Nat. Cancer Inst., 29, 711–722.

  • Tanaka S and Southam CM . (1965). J. Nat. Cancer Inst., 34, 441–451.

  • Tran-Thanh D, Provencher D, Koushik A, Duarte-Franco E, Kessous A, Drouin P, Wheeler CM, Dubuc-Lissoir J, Gauthier P, Allaire G, Vauclair R, Dipaolo JA, Gravitt P, Franco E and Coutlee F . (2003). Am. J. Obstet. Gynecol., 188, 129–134.

  • Uetake S, Yamauchi M, Itoh S, Kawashima O, Takeda K and Ohata M . (2003). Alcohol Clin. Exp. Res., 27 (8 Suppl), 47S–51S.

  • Velema JP, Ferrera A, Figueroa M, Bulnes R, Toro LS, de Barahona O, Claros JM and Melchers WJ . (2002). Int. J. Cancer, 97, 536–541.

  • Whitby D, Howard MR, Tenant-Flowers M, Brink NS, Copas A, Boshoff C, Hatzioannou T, Suggett FE, Aldam DM and Denton AS . (1995). Lancet, 346, 799–802.

  • Winkelstein Jr W, Sacks ST, Ernster VL and Selvin S . (1977). Am. J. Epidemiol., 105, 407–409.

  • Winkelstein Jr W . (1977). Am. J. Epidemiol., 106, 257.

  • Ziegler JL, Newton R, Katongole-Mbidde E, Mbulataiye S, DeCock K, Wabinga H, Mugerwa J, Katabira E, Jaffe H, Parkin DM, Reeves G, Weiss R and Beral V . (1997). AIDS, 11, 1619–1626.

  • Ziegler JL, Simonart T and Snoeck R . (2001). J. Clin. Virol., 20, 127–130.

  • Ziegler JL . (1993). Lancet, 342, 1348–1351.

  • zur Hausen H . (1975). Biophys. Biochim. Acta., 417, 25–53.

  • zur Hausen H . (1976). Cancer Res., 36, 530.

  • zur Hausen H . (1982). Lancet, 2, 1370–1372.

  • zur Hausen H, Gissman L, Steiner W, Dippold W and Dreger J . (1975). Bibl. Haematol., 43, 569–571.

  • zur Hausen H, Meinhof W, Schreiber W and Bornkamm GW . (1974). Int. J. Cancer, 13, 650–656.

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Acknowledgements

To Drs Lynne Haverkos, Nara Battula, Lalji Mishra, Stanka Kukich, and Peter Drotman for comments on a draft paper.

Disclaimer: No official support or endorsement of this article by the Department of the Army, the Department of Defense, or the Food and Drug Administration is intended or should be inferred.

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Haverkos, H. Viruses, chemicals and co-carcinogenesis. Oncogene 23, 6492–6499 (2004). https://doi.org/10.1038/sj.onc.1207822

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