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Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens (2014)

Chapter: Appendix E: Genotoxicity and Mutagenicity Summary Tables

« Previous: Appendix D: Literature-Search Strategies Completed in Support of the Committee's Independent Assessment of Formaldehyde
Suggested Citation:"Appendix E: Genotoxicity and Mutagenicity Summary Tables." National Research Council. 2014. Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens. Washington, DC: The National Academies Press. doi: 10.17226/18948.
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Appendix E

Genotoxicity and Mutagenicity Summary Tables

The committee undertook a comprehensive review of scientific peer-reviewed literature on formaldehyde genotoxicity and mutagenicity. The review included studies that were available to the National Toxicology Program at the time the12th Report on Carcinogens was published and new literature published since July 10, 2011 (see the description of the literature search strategy, including the dates of the search, in Appendix D). The tables in this appendix provide information on the following outcomes: DNA adducts (Table E-1), DNA–DNA cross-links (Table E-2), DNA–protein cross-links (Table E-3), DNA strand breaks (Table E-4), mutations (Table E-5), sister-chromatid exchanges (Table E-6), micronuclei (Table E-7), and chromosomal aberrations (Table E-8). The evidence is organized by cell-free systems; nonmammalian model organisms; mammalian in vitro systems in the rodent, primate, and human; mammalian in vivo systems showing portal-of-entry effects in the rodent, primate, and human; and mammalian in vivo systems showing systemic effects in the rodent, primate, and human. The studies are categorized as either positive (the effect studied was statistically significant for the outcome of interest) or negative (the effect was studied, but no statistically significant change in the outcome of interest was observed). Table 3-9 summarizes the evidence.

Suggested Citation:"Appendix E: Genotoxicity and Mutagenicity Summary Tables." National Research Council. 2014. Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens. Washington, DC: The National Academies Press. doi: 10.17226/18948.
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TABLE E-1 DNA Adducts

Positive Studies Negative Studies
Cell-free systems Von Hippel and Wong 19711
Beland et al. 19841
Snyder and Van Houten 19861
Zhong and Que Hee 2004a, 20051
Cheng et al. 20081
Lu et al. 20091
Nonmammalian model organisms
Mammalian in vitro Rodent Beland et al. 19841
Human Zhong and Que Hee 2004b1
Lu et al. 20122
Mammalian in vivo: portal-of-entry effects Rodent Lu et al. 2010a1
Lu et al. 20112
Primate Moeller et al. 20112
Human
Mammalian in vivo: systemic effects* Rodent Lu et al. 2010a1
Primate Moeller et al. 20112
Human Bono et al. 20102,#

*The committee acknowledges that although most investigators consider the effects on circulating blood mononucleated cells systemic because cells for the analyses were collected from the systemic circulation, it is also plausible that these cells may have been exposed to formaldehyde in the nose through lymphoid tissue in the mucosa.
#M1G adduct has been postulated to be the result of secondary DNA damage from formaldehyde-associated oxidative stress.
1The study was identified from the background document or the substance profile for formaldehyde in the National Toxicology Program 12th Report on Carcinogens (NTP 2010, 2011).
2The study was identified from the committee’s new literature search (see Appendix D).
Source: Committee generated.

Suggested Citation:"Appendix E: Genotoxicity and Mutagenicity Summary Tables." National Research Council. 2014. Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens. Washington, DC: The National Academies Press. doi: 10.17226/18948.
×

TABLE E-2 DNA–DNA Cross-Links

Positive Studies Negative Studies
Cell-free systems Chaw et al. 19801
Huang et al. 19921
Huang and Hopkins 19931
Nonmammalian model organisms
Mammalian in vitro Rodent
Human
Mammalian in vivo: portal-of-entry effects Rodent
Primate
Human
Mammalian in vivo: systemic effects Rodent
Primate
Human

1The study was identified from the background document or the substance profile for formaldehyde in the National Toxicology Program 12th Report on Carcinogens (NTP 2010, 2011).
Source: Committee generated.

Suggested Citation:"Appendix E: Genotoxicity and Mutagenicity Summary Tables." National Research Council. 2014. Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens. Washington, DC: The National Academies Press. doi: 10.17226/18948.
×

TABLE E-3 DNA–Protein Cross-Links

Positive Studies Negative Studies
Cell-free systems Kuykendall and Bogdanffy 19922
Lu et al. 20084
Lu et al. 2010b4
Nonmammalian model organisms
Mammalian in vitro Rodent Ross and Shipley 19801
Ross et al. 19811
Swenberg et al. 1983b3
O'Connor and Fox 19871
Cosma et al. 1988a1
Zhitkovich and Costa 19921
Olin et al. 19961
Casanova and Heck 19971
Casanova et al. 19971
Merk and Speit 1998, 19991
Speit et al. 2007a1
Garcia et al. 20091
She et al. 20133
Human Fornace et al. 19821
Grafström et al. 1984
Saladino et al. 19851
Grafström et al. 19861
Craft et al. 19871
Grafström 19901
Olin et al. 19961
Shaham et al. 1996a1
Costa et al. 19971
Blasiak et al. 20001
Andersson et al. 20033
Emri et al. 20041
Suggested Citation:"Appendix E: Genotoxicity and Mutagenicity Summary Tables." National Research Council. 2014. Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens. Washington, DC: The National Academies Press. doi: 10.17226/18948.
×
Saito et al. 20051
Liu et al. 20061
Schmid and Speit 20071
Speit et al. 2008b
Neuss et al. 2010a,b3
Speit et al. 20103
Duan 20113
Zeller et al. 2011a3
Wong et al. 20123
Ren et al. 20133
Mammalian in vivo: portal-of-entry effects Rodent Casanova-Schmitz et al. 1984a1
Lam et al. 19851
Casanova and Heck 19871
Heck et al. 1986, 19891
Cosma et al. 1988b1
Casanova et al. 1989, 19941
Primate Heck et al. 19891
Casanova et al. 19911
Human
Mammalian in vivo: systemic effects Rodent Ke et al. 20123
Ye et al. 20133
Casanova-Schmitz et al. 1984a1
Casanova and Heck 19871
Primate Heck et al. 19891
Casanova et al. 19911
Human Shaham et al. 1996a, 20031
Lin et al. 20133

1The study was identified from the background document or the substance profile for formaldehyde in the National Toxicology Program 12th Report on Carcinogens (NTP 2010, 2011).
2The study was identified from IARC 2006 or IARC 2012.
3The study was identified from the committee’s new literature search (see Appendix D).
4The study was identified through additional ad hoc searches or from the reference list of other studies.
Source: Committee generated.

Suggested Citation:"Appendix E: Genotoxicity and Mutagenicity Summary Tables." National Research Council. 2014. Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens. Washington, DC: The National Academies Press. doi: 10.17226/18948.
×

TABLE E-4 DNA Strand Breaks

Positive Studies Negative Studies
Cell-free systems
Nonmammalian model organisms Poverenny et al. 19752
Wilkins and Macleod 19762
Magana-Schwencke et al. 19781
Magana-Schwencke and Ekert 19782
Magana-Schwencke and Moustacchi 19802
Le Curieux et al. 19932
Mammalian in vitro Rodent Ross and Shipley 19801
O'Connor and Fox 19871
Cosma et al. 1988a1
Demkowicz-Dobrzanski and Castonguay 19921
Kumari et al. 20123
She et al. 20133
Ross et al. 19811
Speit et al. 2007a1
Human Fornace et al. 19821
Grafström et al. 19841
Saladino et al. 19851
Grafström et al. 19861
Snyder and Van Houten 19861
Grafström 19901
Vock et al. 19991
Liu et al. 20061
Mammalian in vivo: portal-of-entry effects Rodent Neuss et al. 2010c3
Primate
Human
Suggested Citation:"Appendix E: Genotoxicity and Mutagenicity Summary Tables." National Research Council. 2014. Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens. Washington, DC: The National Academies Press. doi: 10.17226/18948.
×
Mammalian in vivo: systemic effects Rodent Im et al. 20061
Wang and Liu 20061
Speit et al. 20091
Primate
Human Yu et al. 20051
Jiang et al. 20061
Jiang et al. 20063
Tong et al. 20061
Costa et al. 20081
Jiang et al. 20103
Costa et al. 20114
Gomaa et al. 20123
Lin et al. 20133
Zeller et al. 2011b3
Aydin et al. 20134

1The study was identified from the background document or the substance profile for formaldehyde in the National Toxicology Program 12th Report on Carcinogens (NTP 2010, 2011).
2The study was identified from IARC 2006 or IARC 2012.
3The study was identified from the committee’s new literature search (see Appendix D).
4The study was identified through additional ad hoc searches or from the reference list of other studies.
Source: committee-generated.

Suggested Citation:"Appendix E: Genotoxicity and Mutagenicity Summary Tables." National Research Council. 2014. Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens. Washington, DC: The National Academies Press. doi: 10.17226/18948.
×

TABLE E-5 Mutations

Positive Studies Negative Studies
Cell-free systems
Nonmammalian model organisms Reviewed in IARC (2006)2: largely positive (with and without S9) for point mutations in bacteria (Salmonella typhimurium, Escherichia coli) and nonmammalian eukaryotes (Neurospora crassa, Drosophila melanogaster, Caenorhabditis elegans) Reviewed in IARC (2006)2: largely negative for frame-shift mutations in S. typhimurium
Mammalian in vitro Rodent Grafstrom et al. 19931
Mackerer et al. 19961
Speit and Merk 20021
Merk and Speit 1998, 19991
Human Goldmacher and Thilly 19831
Grafström et al. 19851
Craft et al. 19871
Crosby et al. 19881
Liber et al. 19891
Grafström 19901
Mammalian in vivo: portal-of-entry effects Rodent Recio et al. 19921 Meng et al. 20101
Primate
Human
Mammalian in vivo: systemic effects Rodent Liu et al. 2009b1
Primate
Human

1The study was identified from the background document or the substance profile for formaldehyde in the National Toxicology Program 12th Report on Carcinogens (NTP 2010, 2011).
2The study was identified from IARC 2006 or IARC 2012.
Source: Committee generated.

Suggested Citation:"Appendix E: Genotoxicity and Mutagenicity Summary Tables." National Research Council. 2014. Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens. Washington, DC: The National Academies Press. doi: 10.17226/18948.
×

TABLE E-6 Sister-Chromatid Exchanges

Positive Studies Negative Studies
Cell-free systems
Nonmammalian model organisms
Mammalian in vitro Rodent Obe and Beek 19791
Natarajan et al. 19831
Basler et al. 19851
Galloway et al. 19851
Merk and Speit 1998, 19991
Speit et al. 2007a1
Garcia et al. 20091
She et al. 20132
Human Obe and Beek 19791
Kreiger and Garry 19831
Schmid et al. 19861
Schmid and Speit 20071
Neuss and Speit 2008
Zeller et al. 2011a2
Mammalian in vivo: portal-of-entry effects Rodent
Primate
Human
Mammalian in vivo: systemic effects Rodent Kligerman et al. 19841
Speit et al. 20091
Primate
Human Yager et al. 19861
Shaham et al. 1997, 20021
He et al. 19981
Thomson et al. 19841
Bauchinger and Schmid 19851
Chebotarev et al. 19861
Suruda et al. 19931
Suggested Citation:"Appendix E: Genotoxicity and Mutagenicity Summary Tables." National Research Council. 2014. Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens. Washington, DC: The National Academies Press. doi: 10.17226/18948.
×
Positive Studies Negative Studies
Ye et al. 20051 Ying et al. 19991
Costa et al. 20081 Pala et al. 20081
Costa et al. 20132 Jakab et al. 20102
Zeller et al. 2011b, 20122

1The study was identified from the background document or the substance profile for formaldehyde in the National Toxicology Program 12th Report on Carcinogens (NTP 2010, 2011).
2The study was identified from the committee’s new literature search (see Appendix D).
Source: committee-generated.

Suggested Citation:"Appendix E: Genotoxicity and Mutagenicity Summary Tables." National Research Council. 2014. Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens. Washington, DC: The National Academies Press. doi: 10.17226/18948.
×

TABLE E-7 Micronuclei

Positive Studies Negative Studies
Cell-free systems
Nonmammalian model organisms
Mammalian in vitro Rodent Merk and Speit 19981
Speit et al. 2007a1
Ji et al. 20133
She et al. 20133
Human Speit et al. 20001
Schmid and Speit 20071
Speit et al. 2011a3
Ren et al. 20133
Mammalian in vivo: portal-of-entry effects Rodent Migliore et al. 19891 Neuss et al. 2010c3
Speit et al. 2011b3
Primate
Human Ballarin et al. 19921
Suruda et al. 19931
Kitaeva et al. 19961
Titenko-Holland et al. 19961
Ying et al. 19971
Burgaz et al. 2001,20021
Ye et al. 20051
Ladeira et al. 2011, 20133
Viegas et al. 20133
Titenko-Holland et al. 19961
Speit et al. 2007b1
Zeller et al. 2011b3
Mammalian in vivo: systemic effects Rodent Zhao et al. 20044
Gao et al. 20084
Gao et al. 20093
Katsnelson et al. 20134
Gocke et al. 19811
Natarajan et al. 19831
Kim et al. 19914
Morita et al. 19971
Speit et al. 20091
Suggested Citation:"Appendix E: Genotoxicity and Mutagenicity Summary Tables." National Research Council. 2014. Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens. Washington, DC: The National Academies Press. doi: 10.17226/18948.
×
Positive Studies Negative Studies
Primate
Human Suruda et al. 19931
Kitaeva et al. 19961
He et al. 19981
Yu et al. 20052
Orsiere et al. 20061
Iarmarcovai et al. 20071
Costa et al. 20081
Jiang et al. 20103
Viegas et al. 20104
Brahem et al. 20113
Costa et al. 20114
Ladeira et al. 2011, 20133
Bouraoui et al. 20133
Costa et al. 20133
Lin et al. 20133
Viegas et al. 20133
Souza and Devi 20143
Ying et al. 19971
Pala et al. 20081
Zeller et al. 2011b3

1The study was identified from the background document or the substance profile for formaldehyde in the National Toxicology Program 12th Report on Carcinogens (NTP 2010, 2011).
2The study was identified from IARC 2006 or IARC 2012.
3The study was identified from the committee’s new literature search (see Appendix D).
4The study was identified through additional ad hoc searches or from the reference list of other studies.
Source: Committee-generated.

Suggested Citation:"Appendix E: Genotoxicity and Mutagenicity Summary Tables." National Research Council. 2014. Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens. Washington, DC: The National Academies Press. doi: 10.17226/18948.
×

TABLE E-8 Chromosomal Aberrations

Positive Studies Negative Studies
Cell-free systems
Nonmammalian model organisms
Mammalian in vitro Rodent Ishidate et al. 19811
Natarajan et al. 19831
Galloway et al. 19851
Hikiba et al. 20051
Hagiwara et al. 2006
Human Miretskaya and Shvartsman 19821
Levy et al. 19831
Schmid et al. 19861
Dresp and Bauchinger 19881
Pongsavee 20112
Ren et al. 20132
Kuehner et al. 20122
Ji et al. 20132
Mammalian in vivo: portal-of-entry effects Rodent Dallas et al. 19921
Primate
Human
Mammalian in vivo: systemic effects Rodent Kitaeva et al. 19901
Gomaa et al. 20122
Fontignie-Houbrechts 19811
Natarajan et al. 19831
Kligerman et al. 19841
Dallas et al. 19921
Speit et al. 20091
Primate
Human Bauchinger and Schmid 19851
Chebotarev et al. 19861
Kitaeva et al. 19961
He et al. 19981
Lazutka et al. 19991
Fleig et al. 19821
Thomson et al. 19841
Vargova et al. 19921
Vasudeva and Anand 19961
Pala et al. 20081
Suggested Citation:"Appendix E: Genotoxicity and Mutagenicity Summary Tables." National Research Council. 2014. Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens. Washington, DC: The National Academies Press. doi: 10.17226/18948.
×
Positive Studies Negative Studies
Neri et al. 20061
Jakab et al. 20102
Zhang et al. 2010b1
Santovito et al. 20112
Gomaa et al. 20122
Musak et al. 20132

1The study was identified from the background document or the substance profile for formaldehyde in the National Toxicology Program 12th Report on Carcinogens (NTP 2010, 2011).
2The study was identified from the committee’s new literature search (see Appendix D).
Source: committee-generated.

Suggested Citation:"Appendix E: Genotoxicity and Mutagenicity Summary Tables." National Research Council. 2014. Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens. Washington, DC: The National Academies Press. doi: 10.17226/18948.
×

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Suggested Citation:"Appendix E: Genotoxicity and Mutagenicity Summary Tables." National Research Council. 2014. Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens. Washington, DC: The National Academies Press. doi: 10.17226/18948.
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Suggested Citation:"Appendix E: Genotoxicity and Mutagenicity Summary Tables." National Research Council. 2014. Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens. Washington, DC: The National Academies Press. doi: 10.17226/18948.
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Suggested Citation:"Appendix E: Genotoxicity and Mutagenicity Summary Tables." National Research Council. 2014. Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens. Washington, DC: The National Academies Press. doi: 10.17226/18948.
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Suggested Citation:"Appendix E: Genotoxicity and Mutagenicity Summary Tables." National Research Council. 2014. Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens. Washington, DC: The National Academies Press. doi: 10.17226/18948.
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Suggested Citation:"Appendix E: Genotoxicity and Mutagenicity Summary Tables." National Research Council. 2014. Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens. Washington, DC: The National Academies Press. doi: 10.17226/18948.
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Many people in the United States are exposed to formaldehyde. Exposure can occur from environmental sources (for example, combustion processes, building materials, and tobacco smoke) or in occupational settings (for example, the furniture, textile, and construction industries). Formaldehyde exposure also has endogenous sources--it is produced intracellularly as a component of the one carbon pool intermediary metabolism pathway. Scientists have studied formaldehyde for decades to determine whether exogenous formaldehyde exposure may be associated with cancer in humans. In 1981, The National Toxicology Program (NTP) first listed formaldehyde in the 2nd Report on Carcinogens as "reasonably anticipated to be a human carcinogen". In 2011, NTP upgraded the listing of formaldehyde to "known to be a human carcinogen". Following the new listing, Congress directed the Department of Health and Human Services to arrange for the National Academy of Sciences to independently review formaldehyde's substance profile and listing. This report presents the findings and conclusions of the committee formed in response to the congressional request.

Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens concurs with NTP that there is sufficient evidence in studies that had adequate characterization of relevant exposure metrics to enable a strong conclusion about the association between formaldehyde exposure and cancer in humans. Additionally, the authoring committee independently reviewed the scientific evidence from studies in humans, experimental animals, and other studies relevant to the mechanisms of carcinogenesis and made level-of-evidence conclusions. This report finds clear and convincing epidemiologic evidence of an association between formaldehyde exposure and nasopharyngeal and sinonasal cancers in humans.

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