TY - JOUR
T1 - Concordance between sites of tumor development in humans and in experimental animals for 111 agents that are carcinogenic to humans
AU - Krewski, Daniel
AU - Rice, Jerry M.
AU - Bird, Michael
AU - Milton, Brittany
AU - Collins, Brian
AU - Lajoie, Pascale
AU - Billard, Melissa
AU - Grosse, Yann
AU - Cogliano, Vincent J.
AU - Caldwell, Jane C.
AU - Rusyn, Ivan I.
AU - Portier, Christopher J.
AU - Melnick, Ronald L.
AU - Baan, Robert A.
AU - Little, Julian
AU - Zielinski, Jan M.
N1 - Funding Information:
Parts of this article appear in Daniel Krewski, Jerry M. Rice, Michael Bird, Brittany Milton, Brian Collins, Pascale Lajoie, Mélissa Billard, Yann Grosse, Vincent J. Cogliano, Jane C. Caldwell, Ivan I. Rusyn, Christopher J. Portier, Ronald L. Melnick, Julian Little, and Jan M. Zielinski in collaboration with other participants in the Workshop on Tumour Site Concordance and Mechanisms of Carcinogenesis. Chapter 21 – Analysis of tumor site concordance. In: Baan, R.A., Stewart, B.W., and Straif, K., editors. Tumor site concordance and mechanisms of carcinogenesis. Lyon, IARC Scientific Publication n°165; 2019 [reproduced here with permission of the IARC]. We are grateful to Abdallah Alami and Nawal Farhat for assistance in the final formatting of this article. Julian Little is the Canada Research Chair in Human Genome Epidemiology at the University of Ottawa. D. Krewski is the Natural Sciences and Engineering Research Council of Canada Chair in Risk Science at the University of Ottawa.
Funding Information:
Parts of this article appear in Daniel Krewski, Jerry M. Rice, Michael Bird, Brittany Milton, Brian Collins, Pascale Lajoie, M?lissa Billard, Yann Grosse, Vincent J. Cogliano, Jane C. Caldwell, Ivan I. Rusyn, Christopher J. Portier, Ronald L. Melnick, Julian Little, and Jan M. Zielinski in collaboration with other participants in the Workshop on Tumour Site Concordance and Mechanisms of Carcinogenesis. Chapter 21?Analysis of tumor site concordance. In: Baan, R.A., Stewart, B.W., and Straif, K., editors. Tumor site concordance and mechanisms of carcinogenesis. Lyon, IARC Scientific Publication n?165; 2019 [reproduced here with permission of the IARC]. We are grateful to Abdallah Alami and Nawal Farhat for assistance in the final formatting of this article. Julian Little is the Canada Research Chair in Human Genome Epidemiology at the University of Ottawa. D. Krewski is the Natural Sciences and Engineering Research Council of Canada Chair in Risk Science at the University of Ottawa.
Publisher Copyright:
© 2019, © 2019 Taylor & Francis.
PY - 2019/11/17
Y1 - 2019/11/17
N2 - Since the inception of the IARC Monographs Programme in the early 1970s, this Programme has developed 119 Monograph Volumes on more than 1000 agents for which there exists some evidence of cancer risk to humans. Of these, 120 agents were found to meet the criteria for classification as carcinogenic to humans (Group 1). Volume 100 of the IARC Monographs, compiled in 2008-2009 and published in 2012, provided a review and update of the 107 Group 1 agents identified as of 2009. These agents were divided into six broad categories: (I) pharmaceuticals; (II) biological agents; (III) arsenic, metals, fibers and dusts; (IV) radiation; (V) personal habits and indoor combustions; and (VI) chemical agents and related occupations. The Group I agents reviewed in Volume 100, as well as five additional Group 1 agents defined in subsequent Volumes of the Monographs, were used to assess the degree of concordance between sites where tumors originate in humans and experimental animals including mice, rats, hamsters, dogs, and non-human primates using an anatomically based tumor nomenclature system, representing 39 tumor sites and 14 organ and tissue systems. This evaluation identified 91 Group 1 agents with sufficient evidence (82 agents) or limited evidence (9 agents) of carcinogenicity in animals. The most common tumors observed in both humans and animals were those of the respiratory system including larynx, lung, and lower respiratory tract. In humans, respiratory system tumors were noted for 31 of the 111 distinct Group 1 carcinogens identified up to and including Volume 109 of the IARC Monographs, comprising predominantly 14 chemical agents and related occupations in category VI; seven arsenic, metals, fibers, and dusts in category III, and five personal habits and indoor combustions in category V. Subsequent to respiratory system tumors, those in lymphoid and hematopoietic tissues (26 agents), the urothelium (18 agents), and the upper aerodigestive tract (16 agents) were most often seen in humans, while tumors in digestive organs (19 agents), skin (18 agents), and connective tissues (17 agents) were frequently seen in animals. Exposures to radiation, particularly X- and gamma-radiation, and tobacco smoke were associated with tumors at multiple sites in humans. Although the IARC Monographs did not emphasize tumor site concordance between animals and humans, substantial concordance was detected for several organ and tissue systems, even under the stringent criteria for sufficient evidence of carcinogenicity used by IARC. Of the 60 agents for which at least one tumor site was identified in both humans and animals, 52 (87%) exhibited tumors in at least one of the same organ and tissue systems in humans and animals. It should be noted that some caution is needed in interpreting concordance at sites where sample size is particularly small. Although perfect (100%) concordance was noted for agents that induce tumors of the mesothelium, only two Group 1 agents that met the criteria for inclusion in the concordance analysis caused tumors at this site. Although the present analysis demonstrates good concordance between animals and humans for many, but not all, tumor sites, limitations of available data may result in underestimation of concordance.
AB - Since the inception of the IARC Monographs Programme in the early 1970s, this Programme has developed 119 Monograph Volumes on more than 1000 agents for which there exists some evidence of cancer risk to humans. Of these, 120 agents were found to meet the criteria for classification as carcinogenic to humans (Group 1). Volume 100 of the IARC Monographs, compiled in 2008-2009 and published in 2012, provided a review and update of the 107 Group 1 agents identified as of 2009. These agents were divided into six broad categories: (I) pharmaceuticals; (II) biological agents; (III) arsenic, metals, fibers and dusts; (IV) radiation; (V) personal habits and indoor combustions; and (VI) chemical agents and related occupations. The Group I agents reviewed in Volume 100, as well as five additional Group 1 agents defined in subsequent Volumes of the Monographs, were used to assess the degree of concordance between sites where tumors originate in humans and experimental animals including mice, rats, hamsters, dogs, and non-human primates using an anatomically based tumor nomenclature system, representing 39 tumor sites and 14 organ and tissue systems. This evaluation identified 91 Group 1 agents with sufficient evidence (82 agents) or limited evidence (9 agents) of carcinogenicity in animals. The most common tumors observed in both humans and animals were those of the respiratory system including larynx, lung, and lower respiratory tract. In humans, respiratory system tumors were noted for 31 of the 111 distinct Group 1 carcinogens identified up to and including Volume 109 of the IARC Monographs, comprising predominantly 14 chemical agents and related occupations in category VI; seven arsenic, metals, fibers, and dusts in category III, and five personal habits and indoor combustions in category V. Subsequent to respiratory system tumors, those in lymphoid and hematopoietic tissues (26 agents), the urothelium (18 agents), and the upper aerodigestive tract (16 agents) were most often seen in humans, while tumors in digestive organs (19 agents), skin (18 agents), and connective tissues (17 agents) were frequently seen in animals. Exposures to radiation, particularly X- and gamma-radiation, and tobacco smoke were associated with tumors at multiple sites in humans. Although the IARC Monographs did not emphasize tumor site concordance between animals and humans, substantial concordance was detected for several organ and tissue systems, even under the stringent criteria for sufficient evidence of carcinogenicity used by IARC. Of the 60 agents for which at least one tumor site was identified in both humans and animals, 52 (87%) exhibited tumors in at least one of the same organ and tissue systems in humans and animals. It should be noted that some caution is needed in interpreting concordance at sites where sample size is particularly small. Although perfect (100%) concordance was noted for agents that induce tumors of the mesothelium, only two Group 1 agents that met the criteria for inclusion in the concordance analysis caused tumors at this site. Although the present analysis demonstrates good concordance between animals and humans for many, but not all, tumor sites, limitations of available data may result in underestimation of concordance.
KW - human tumor sites
KW - animal tumor sites
KW - tumor classification
KW - concordance
KW - overlap
KW - IMMUNOSUPPRESSIVE CYTOTOXIC AGENTS
KW - DIESEL EXHAUST
KW - ADRENAL-TUMORS
KW - CARBON-BLACK
KW - NZBXNZW MICE
KW - INDUCTION
KW - PULMONARY
KW - RATS
KW - EXPOSURE
KW - RADIOSTRONTIUM
U2 - 10.1080/10937404.2019.1642586
DO - 10.1080/10937404.2019.1642586
M3 - (Systematic) Review article
C2 - 31795923
SN - 1093-7404
VL - 22
SP - 203
EP - 236
JO - Journal of Toxicology and Environmental Health-Part B-Critical Reviews
JF - Journal of Toxicology and Environmental Health-Part B-Critical Reviews
IS - 7-8
ER -