A classification framework and practical guidance for establishing a mode of action for chemical carcinogens

Regulatory Toxicology and Pharmacology

Volumn 45, Issue 1, 2006, Pages 9-23

  Butterworth, Byron E ^a  

^a Butterworth Consulting   (United States)

Author keywords

Cancer risk assessment; Chemical carcinogenesis; Framework for assigning a mode of action; Genetic toxicology testing; Genotoxic carcinogens; Mode of action; Nongenotoxic carcinogens

Indexed keywords

CARCINOGEN; CHLOROFORM; NAPHTHALENE;

ARTICLE; BIOASSAY; CANCER RISK; CARCINOGEN TESTING; CARCINOGENESIS; CARCINOGENICITY; CELL ASSAY; CELL PROLIFERATION; CELL REGENERATION; CHROMOSOME ANALYSIS; CYTOTOXICITY; DNA DETERMINATION; DNA REPAIR; GENETIC TOXICOLOGY; GENOTOXICITY; HUMAN; LETHALITY; MICRONUCLEUS TEST; MUTAGENIC ACTIVITY; MUTAGENICITY; NONHUMAN; OUTCOME ASSESSMENT; PRACTICE GUIDELINE; PRIORITY JOURNAL; RELIABILITY; RISK ASSESSMENT;

ANIMALS; CARCINOGENICITY TESTS; CARCINOGENS; ENDPOINT DETERMINATION; GUIDELINES; HUMANS; MUTAGENICITY TESTS; NEOPLASMS; RISK ASSESSMENT; UNITED STATES; UNITED STATES ENVIRONMENTAL PROTECTION AGENCY;

ANIMALIA; BACTERIA (MICROORGANISMS); RODENTIA;

EID: 33646086476     PISSN: 02732300     EISSN: 10960295     Source Type: Journal    
DOI: 10.1016/j.yrtph.2006.01.011     Document Type: Article

References (90)

1. Ashby J., and Tennant R.W. Definitive relationships among chemical structure, carcinogenicity and mutagenicity for 301 chemicals tested by the U.S. NTP. Mutat. Res. 257 (1991) 229-306
2. Belinsky S.A., Walker V.E., Maronpot R.R., Swenberg J.A., and Anderson M.W. Molecular dosimetry of DNA adduct formation and cell toxicity in rat nasal mucosa following exposure to the tobacco specific nitrosamine 4-(N-methyl-N-nitroamino)-1-(3-pyridyl)-1-butanone and their relationship to induction of neoplasia. Cancer Res. 47 (1987) 6058-6065
3. Bermudez E., Tillery D., and Butterworth B.E. The effect of 2,4-diaminotoluene and isomers of dinitrotoluene on unscheduled DNA synthesis in primary rat hepatocytes. Environ. Mutagen. 1 (1979) 391-398
4. Bolt H.M., Foth H., Hengstler J.G., and Dengen G.H. Carcinogenicity categorization of chemicals-new aspects to be considered in a European perspective. Toxicol. Lett. 151 (2004) 29-41
5. Borgert C.T. EPA's new guidance for assessing cancer risks from early life exposures: genotoxic mode of action and implications for human health-based standards. Regul. Toxicol. Pharmacol. 42 (2005) 245-248
6. Bridges, B., Butterworth, B.E., Weinstein, I.B. (Eds.), 1982 "Indicators of Genotoxic Exposure," Banbury Report 13, Cold Spring Harbor Laboratory, p. 580.
7. Buckpitt A., Boland B., Isbell M., Morin D., Shultz M., Baldwin R., Chan K., Karlsson A., Lin C., Taff A., West J., Fanucci M., Van Winkle L., and Plopper C. Naphthalene-induced respiratory tract toxicity: metabolic mechanisms of toxicity. Drug Metab. Rev. 34 (2002) 791-820
8. Butterworth, B.E., 2004. Expert Opinion on the Genotoxicity and Carcinogenicity of Naphthalene. Submitted to the U.S. EPA as public comment on the Toxicological Review of Naphthalene (CAS No. 91-20-3) In support of summary information on the Integrated Risk Information System (IRIS).
9. Butterworth B.E., Ashby J., Bermudez E., Casciano D., Mirsalis J., Probst G., and Williams G. A protocol and guide for the in vitro rat hepatocyte DNA repair assay. Mutat. Res. 189 (1987) 113-121
10. Butterworth B.E., Ashby J., Bermudez E., Casciano D., Mirsalis J., Probst G., and Williams G. A protocol and guide for the in vivo rat hepatocyte DNA repair assay. Mutat. Res. 189 (1987) 123-133
11. Butterworth B.E., and Bogdanffy M.S. A comprehensive approach for integration of toxicity and cancer risk assessments. Regul. Toxicol. Pharmacol. 29 (1999) 23-36
12. Butterworth B.E., Conolly R.B., and Morgan K.T. A strategy for establishing mode of action of chemical carcinogens as a guide for approaches to risk assessments. Cancer Lett. 93 (1995) 129-146
13. Butterworth, B.E., Doolittle, D.J., Working, P.K., Strom, S.C., Jirtle, R.L., Michalopoulos, G., 1982. Chemically-induced DNA repair in rodent and human cells. In: Bridges, B.A, Butterworth, B.E., Weinstein, I.B. (Eds.), "Indicators of Genotoxic Exposure," Banbury Report 13, Cold Spring Harbor Laboratory, New York, pp. 101-114.
14. Butterworth, B.E., Popp, J.A., Conolly, R.B., Goldsworthy, T.L., 1992. Chemically-induced cell proliferation in carcinogenesis. In: Vainio, H., Magee, P.N., McGregor, D.B., McMichael, A.J. (Eds.), Mechanisms of Carcinogenesis in Risk Identification. IARC Scientific Publication Number 116, pp. 279-305.
15. Butterworth B.E., Smith-Oliver T., Earle L., Loury D., White R.D., Doolittle D., Working P., Cattley R.C., Jirtle R., Michalopoulos G., and Strom S. Use of primary cultures of human hepatocytes in toxicology studies. Cancer Res. 49 (1989) 1075-1084
16. Carmichael P.L., Crooks N., Schenk M., Gardner I., Kenna J.G., and Caldwell J. A comparison of immunochemical and postlabeling methodologies for the detection of DNA adducts formed by methyleugenol. Hum. Exp. Toxicol. 18 (1999) 55
17. Cohen S.M., and Ellwein L.B. Cell proliferation in carcinogenesis. Science 249 (1990) 1007-1011
18. Cohen S.M., Purtilo D.T., and Ellwein L.B. Pivotal role of increased cell proliferation in human carcinogenesis. Mod. Pathol. 4 (1991) 371-375
19. Columbano A., Rajalakshmi S., and Sarma D.S.R. Requirement of cell proliferation for the initiation of liver carcinogenesis as assayed by three different procedures. Cancer Res. 41 (1981) 2079-2083
20. Collins A.R. The comet assay for DNA damage and repair. Mol. Biotechnol. 26 (2004) 249-261
21. 1 mice. Toxicol. Sci. 66 (2002) 201-208
22. Constan A.A., Sprankle C.S., Peters J.M., Kedderis G.L.., Everitt J.I., Wong B.A., Gonzalez F.L., and Butterworth B.E. Metabolism of chloroform by cytochrome P450 2E1 is required for induction of toxicity in the liver, kidney, and nose of male mice. Toxicol. Appl. Pharmacol. 160 (1999) 120-126
23. Craddock V.M. Cell proliferation and experimental liver cancer. In: Cameron H.M., Linsell C.A., and Warwick G.P. (Eds). Liver Cell Cancer (1976), Elsevier/North-Holland Biomedical Press, Amsterdam 153-201
24. Dearfield K.L., Auletta A.E., Mimino M.C., et al. Considerations in the U.S. Environmental Protection Agency's testing approach for mutagenicity. Mutat. Res. 258 (1991) 259-283
25. 2u-globulin is necessary for d-limonene promotion of male rat kidney tumors. Cancer Res. 51 (1991) 3512-3521
26. Doolittle D.J., Bermudez E., Working P.K., and Butterworth B.E. Measurement of genotoxic activity in multiple tissues following inhalation exposure to dimethylnitrosamine. Mutat. Res. 141 (1984) 123-127
27. Doolittle D.J., Sherrill J.M., and Butterworth B.E. The influence of intestinal bacteria, sex of the animal, and position of the nitro group on the hepatic genotoxicity of nitrotoluene isomers in vivo. Cancer Res. 43 (1983) 2836-2842
28. Ellwein L.B., and Cohen S.M. The health risks of saccharin revisited. Crit. Rev. Toxicol. 20 (1990) 311-326
29. Flamm G.W., and Lehman-McKeeman L.D. The human relevance of the renal tumor-inducing potential of d-limonene in male rats: implications for risk assessment. Regulat. Toxicol. Pharmacol. 13 (1991) 70-86
30. Galloway S.M. Cytotoxicity and chromosome aberrations in vitro: experience in industry and the case for an upper limit on toxicity in the aberration assay. Environ. Mol. Mutagen 35 (2000) 191-201
31. Galloway S.M., Aardema M.J., Ishidate Jr. M., Ivett J.L., Kirkland D.J., Morita T., Mosesso P., and Sofuni T. Report from working group on in vitro tests for chromosomal aberrations. Mutat. Res. 312 (1994) 241-261
32. Hard G.C., Boorman G.A., and Wolf D.C. Re-evaluation of the 2-year chloroform drinking water carcinogenicity bioassay in Osborne-Mendel rats supports chronic renal tubule injury as the mode of action underlying the renal tumor response. Toxicol. Sci. 53 (2000) 237-244
33. Heck, H. d'A., 1987. Bladder stones and bladder cancer: a review of the toxicology of terephthalic acid. In: Butterworth, B.E., Slaga, T.J. (Eds.), Nongenotoxic Mechanisms in Carcinogenesis. Cold Spring Harbor Laboratory, [Banbury Report 25], Cold Spring Harbor, NY, pp. 233-243.
34. Howes A.J., Chan V.S., and Caldwell J. Structure-specificity of the genotoxicity of some naturally occurring alkenylbenzenes determined by the unscheduled DNA synthesis assay in rat hepatocytes. Food Chem. Toxicol. 28 (1990) 537-542
35. Hozier J., Sawyer J., Moore M., Howard B., and Clive D. Cytogenetic analysis of the L5178Y tk+/-, tk-/- mouse lymphoma mutagenesis assay system. Mutat. Res. 84 (1981) 169-175
36. IARC Monographs Evaluating Carcinogenic Risks to Humans, 2002. Vol. 82, Naphthalene, pp. 367-435.
37. International Conference on Harmonization (ICH)., 1995. Guidance on Specific aspects of regulatory genotoxicity tests for pharmaceuticals-ICH Harmonized Tripartite Guideline S2A. Federal Register, vol. 61, p. 18199, April 24, 1996.
38. International Conference on Harmonization (ICH)., 1997. Genotoxicity: A Standard Battery for Genotoxicity Testing of Pharmaceuticals-ICH Harmonized Tripartite Guideline S2B. Federal Register, November 21, 1997.
39. International Life Sciences Institute (ILSI), 1997. An Evaluation of EPA's Proposed Guidelines for Carcinogen Risk Assessment Using Chloroform and Dichloroacetate As Case Studies: Report of an Expert Panel." International Life Sciences Institute, 1126 Sixteenth St., N.W., Washington, DC.
40. International Programme on Chemical Safety (IPCS). (1994). Environmental Health Criteria 163: Chloroform, World Health Organization, Geneva, Switzerland, p. 174.
41. International Programme on Chemical Safety (IPCS), 1999. IPCS Workshop on Developing a Conceptual Framework for Cancer Risk Assessment." February 16-18, 1999, Lyon, France. IPCS/99.6 World Health Organizations Geneva, Switzerland.
42. International Programme on Chemical Safety (IPCS), 2000. Environmental Health Criteria 216: Disinfectants and Disinfectant By-Products, World Health Organization, Geneva, Switzerland, p. 210.
43. International Programme on Chemical Safety (IPCS) INCHEM Review of Eugenol. WHO Food Additives Series 14. , Accessed September 9, 2005.
44. 1 mice. Fundam. Appl. Toxicol. 5 (1985) 760-769
45. Lambert I.B., Singer T.M., Boucher S.E., and Douglas G.R. Detailed review of transgenic rodent mutation assays. Mutat. Res. 590 (2005) 1-280
46. 1 mice. Environ. Mol. Mutagen. 23 (1994) 132-136
47. 1 mice: comparison of administration by gavage in corn oil vs. ad libitum in drinking water. Fundam. Appl. Toxicol. 22 (1994) 90-102
48. Lohman P.H., Mendelsohn M.L., Moore D.H., Waters M.D., Brusick D.J., Ashby J., and Lohman W.J. International Commission for Protection Against Environmental Mutagens and Carcinogens. A method for comparing and combining short-term genotoxicity test data: the basic system. Mutat. Res. 266 (1992) 7-25
49. McCann J., Choi E., Yamasaki E., and Ames B.N. Detection of carcinogens as mutagens in the Salmonella/microsome test: assay of 300 chemicals. Proc. Natl. Acad. Sci. USA 72 (1975) 5135-5139
50. Meek M.E., Bucher J.R., Cohen S.M., Dellarco V., Hill R.N., Lehman-McKeeman L.D., Longfellow D.G., Pastoor T., Seed J., and Patton D.E. A framework for human relevance analysis of information on carcinogenic modes of action. Crit. Rev. Toxicol. 33 (2003) 591-653
51. Mendelsohn M.L., Moore D.H., and Lohman P.H. International Commission for Protection Against Environmental Mutagens and Carcinogens. A method for comparing and combining short-term genotoxicity test data: results and interpretation. Mutat. Res. 266 (1992) 43-60
52. Mirsalis J.C., and Butterworth B.E. Detection of unscheduled DNA synthesis in hepatocytes isolated from rats treated with genotoxic agents: an in vivo-in vitro assay for potential carcinogens and mutagens. Carcinogenesis 1 (1980) 621-625
53. Mirsalis J.C., and Butterworth B.E. Induction of unscheduled DNA synthesis in rat hepatocytes following in vivo treatment with dinitrotoluene. Carcinogenesis 3 (1982) 241-245
54. Mirsalis J.C., Hamm Jr. T.E., Sherrill M., and Butterworth B.E. The role of gut flora in the genotoxicity of dinitrotoluenes. Nature 295 (1982) 322-323
55. Mirsalis J.C., Tyson K.C., and Butterworth B.E. The detection of genotoxic carcinogens in the in vivo-in vitro hepatocyte DNA repair assay. Environ. Mutagen. 4 (1982) 553-562
56. Morgan K.T. Nasal dosimetry, lesion distribution, and the toxicologic pathologist: a brief review. Inhal. Toxicol. 6 (1995) 41-57
57. Muller L., and Kasper P. Human biological relevance and the use of threshold-arguments in regulatory genotoxicity assessment: experience with pharmaceuticals. Mutat. Res. 464 (2000) 19-34
58. Muller L., and Sofuni T. Appropriate levels of cytotoxicity for genotoxicity tests using mammalian cells in vitro. Environ. Mol. Mutagen 35 (2000) 202-205
59. National Cancer Institute (NCI), 1976. Report on Carcinogenesis Bioassay of Chloroform, Accession No. PB-264 018. National Technical Information Service, Springfield, VA, p. 60.
60. National Toxicology Program (NTP), 1992. Technical Report on the Toxicology and Carcinogenesis Studies of Naphthalene (CAS No. 91-20-3) in B6C3F1 Mice (inhalation studies). Rockville, MD: DHHS, PHS, Tech. Rep. Ser. 410. NIH Publ. No. 92-3141.
61. National Toxicology Program (NTP), 2000a. NTP Technical Report 491 (TR 491) Toxicology and Carcinogenesis Studies of Methyleugenol (CAS NO. 93-15-2) in F344/N Rats and B6C3F1 Mice (Gavage Studies). July 2000. National Toxicology Program, National Institutes of Health, p. 396.
62. National Toxicology Program (NTP), 2000b. Technical report on the toxicology and carcinogenesis studies of naphthalene (CAS No. 91-20-3) in F344/N rats (inhalation studies). Rockville, MD: DHHS, PHS, Tech. Rep. Ser. 500.
63. Phillips D.H. Further evidence that eugenol does not bind to DNA in vivo. Mutat. Res. 245 (1990) 23-26
64. Putman D.L., Gudi R., Wagner V.O., San R.C., and Jacobson-Kram D. Genetic toxicology. In: Jacobson-Kram D., and Keller K.A. (Eds). Toxicology Testing Handbook: Principles, Applications, and Data Interpretation (2000), Marcel Dekker 127-194
65. Richardson F.C., Boucheron J.A., Dyroff M., Popp J.A., and Swenberg J.A. Biochemical and morphological studies of heterogeneous lobe responses in hepatocarcinogenesis. Carcinogenesis 7 (1986) 247-251
66. Rickert D.E., Butterworth B.E., and Popp J.A. Dinitrotoluene: Acute Toxicity, Oncogenicity, Genotoxicity, and Metabolism. Critical Reviews in Toxicology 13 (1983), CRC Press, Boca Raton, FL 217-234
67. Schreiner C. Genetic toxicity of naphthalene: a review. J. Toxicol. Environ. Health Part B 6 (2003) 161-183
68. Shelby M.D. The genetic toxicity of human carcinogens and its implications. Mutat. Res. 204 (1988) 3-15
69. Shelby M.D., Erexson G.L., Hook G.J., and Tice R.R. Evaluation of a three-exposure mouse bone marrow micronucleus protocol: results with 49 chemicals. Environ. Mol. Mutagen. 21 (1993) 160-179
70. Shelby M.D., and Witt K.L. Comparison of results from mouse bone marrow chromosome aberration and micronucleus tests. Environ. Mol. Mutagen. 25 (1995) 302-313
71. Short B., Hamilton C., Zimmermann D., Hart R., Wier P., Mirsalis J., and Schwartz L. Effect of SK&F 105809 on hepatocellular proliferation, foci, and DNA repair in the rat. Toxicologist 14 (1994) 252
72. Swiger R.R., Cosentino L., Shima N., Bielas J., Cruz-Munoz W., and Helddle J.A. The cII locus in the MutaMouse system. Environ. Mol. Mutagen. 34 (1999) 201-207
73. Tennant R.W. Stratification of rodent carcinogenicity bioassay results to reflect relative human hazard. Mutat. Res. 286 (1993) 111-118
74. Tennant R.W., Margolin B.H., Shelby M.D., Zeiger E., Haseman J.K., Spalding J., Caspary W., Stasiewicz S., and Anderson B. Prediction of chemical carcinogenicity in rodents from in vitro genetic toxicity assays. Science 236 (1987) 933-941
75. Tice R.R., Agurell E., Anderson D., Burlinson B., Hartman A., Kobayashi H., Miyamae Y., Rojas E., Ryu J.-C., and Sasaki Y.F. Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ. Mol. Mutagen. 35 (2000) 206-221
76. U.S. Court of Appeals (2000), District of Columbia Circuit, Argued February 11, 2000, Decided March 31, 2000, No. 98-1627, Chlorine Chemistry Council and Chemical Manufactures Association Petitioners vs. Environmental Protection Agency, Respondent, On petitions for review of an order of the Environmental Protection Agency.
77. U.S. Environmental Protection Agency (U.S. EPA), 1986. Guidelines for Mutagenicity Risk Assessment, EPA/630/R-98/003, September 24, 1986, U.S. Environmental Protection Agency, Federal Register, vol. 51. Washington, DC, pp. 34006-34012.
78. U.S. Environmental Protection Agency (U.S. EPA), 1998a. National Primary Drinking Water Regulations: Disinfectants and Disinfection Byproducts Notice of Data Availability. March 31, 1998, Fed. Regist, vol. 63, pp. 15674-15692.
79. U.S. Environmental Protection Agency (U.S. EPA), 1998b. National Primary Drinking Water Regulations: Disinfectants and Disinfection Byproducts; Final Rule, December 16, 1998, Fed. Regist. 63, pp. 69390-69396.
80. U.S. Environmental Protection Agency (U.S. EPA), 2004a. Toxicological Review of Naphthalene (CAS No. 91-20-3) In Support of Summary Information on the Integrated Risk Information System (IRIS). NECA-S-1707, June 2004, U.S. Environmental Protection Agency, Washington, DC.
81. U.S. Environmental Protection Agency (U.S. EPA), 2004b. Summary Information on the Integrated Risk Information System (IRIS) for Naphthalene (CAS No. 91-20-3). June 2004, U.S. Environmental Protection Agency, Washington, DC.
82. U.S. Environmental Protection Agency (U.S. EPA), 2005a. Supplemental Guidance for Assessing Susceptibility from Early-Life Exposure to Carcinogens. EPA/630/R-03/003F, March 2005, Risk Assessment Forum, U.S. Environmental Protection Agency, Washington, DC.
83. U.S. Environmental Protection Agency (U.S. EPA), 2005b. Guidelines for Carcinogen Risk Assessment, EPA/630/P-03/00F, March 2005, U.S. Environmental Protection Agency, Washington, DC.
84. U.S. Environmental Protection Agency (U.S. EPA), 2005c. IRIS: Integrated Risk Information System. Database on chloroform. Accessed September 2, 2005.
85. U.S. Food and Drug Administration (U.S. FDA), 2006. Guidance for Industry, Recommended Approaches to Integration of Genetic Toxicology Study Results. CDER/FDA website. Accessed January 21, 2006.
86. Waters M.D., Stack H.F., Garrett N.E., and Jackson M.A. The genetic activity profile database. Environ. Health Perspect. 96 (1991) 41-45
87. Waters, M.D., Stack, H.F., Jackson, M.A., 1999. Short-term tests for defining mutagenic carcinogens. In: McGregor, D.B., Rice, J.M., Venitt, S. (Eds). The use of short term tests for carcinogens and data on genetic effects in carcinogenic hazard evaluation. Lyon, France: IARC Publication No. 146 pp. 499-536.
88. Williams G.M. Carcinogen induced DNA repair in primary rat liver cell cultures: a possible screen for chemical carcinogens. Cancer Lett. 1 (1976) 231-236
89. Working P.K., and Butterworth B.E. An assay to detect chemically-induced DNA repair in rat spermatocytes. Environ. Mutagen. 6 (1984) 273-286
90. Zeiger E., Haseman J.K., Shelby M.D., Margolin B.H., and Tennant R.W. Evaluation of four in vitro genetic toxicity tests for predicting rodent carcinogenicity: confirmation of earlier results with 41 additional chemicals. Environ. Mol. Mutagen. 16 Suppl. 18 (1990) 1-14