Review of the Formaldehyde Assessment in the National Toxicology Program 12th Report on Carcinogens (2014)
Chapter: Appendix E: Genotoxicity and Mutagenicity Summary Tables
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.
| 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.
| 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.
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 |
— | ||
| 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.
| 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 | — | — | ||
| 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.
| 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.
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 |
||
| 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.
| 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 |
|
| 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.
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 |
||
| 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.
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