Abstract
Background
Clarification of the putative etiologic role of heterocyclic aromatic amines (HAAs) in the development of cancer requires a validated assessment tool for dietary HAAs. This study primarily aimed to evaluate the validity of a food frequency questionnaire (FFQ) in estimating HAA intake, using 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) level in human hair as the reference method.
Methods
We first updated analytical methods of PhIP using liquid chromatography-electrospray ionization/tandem mass spectrometry (LC-ESI/MS/MS) and measured 44 fur samples from nine rats from a feeding study as part-verification of the quantitative performance of LC-ESI/MS/MS. We next measured PhIP level in human hair samples from a validation study of the FFQ (n = 65). HAA intake from the FFQ was estimated using information on intake from six fish items and seven meat items and data on HAA content in each food item. Correlation coefficients between PhIP level in human hair and HAA intake from the FFQ were calculated.
Results
The animal feeding study of PhIP found a significant dose–response relationship between dosage and PhIP in rat fur. Mean level was 53.8 pg/g hair among subjects with values over the limit of detection (LOD) (n = 57). We found significant positive correlation coefficients between PhIP in human hair and HAA intake from the FFQ, with Spearman rank correlation coefficients of 0.35 for all subjects, 0.21 for subjects with over LOD values, and 0.34 for subjects with over limit of quantification.
Conclusion
Findings from the validation study suggest that the FFQ is reasonably valid for the assessment of HAA intake.
Similar content being viewed by others
Abbreviations
- CV:
-
Coefficients of variation
- CI:
-
Confidence interval
- 7,8-DiMeIQx:
-
2-Amino-3,7,8-trimethylimidazo[4,5-f]quinoxaline
- 4,8-DiMeIQx:
-
2-Amino-3,4,8-trimethylimidazo[4,5-f]quinoxaline
- dG-C8-PhIP:
-
N 2-(deoxyguanosine-8-yl)-2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine
- DR:
-
Dietary record
- ESI:
-
Electrospray ionization
- FFQ:
-
Food frequency questionnaire
- HAAs:
-
Heterocyclic aromatic amines
- IQ:
-
2-Amino-3-methylimidazo[4,5-f]quinoline
- LC-ESI/MS:
-
Liquid chromatography-electrospray ionization/mass spectrometry
- LC-ESI/MS/MS:
-
Liquid chromatography-electrospray ionization/tandem mass spectrometry
- LC/MS/MS:
-
Liquid chromatography tandem mass spectrometry
- LOD:
-
Limit of detection
- LOQ:
-
Limit of quantification
- MeIQ:
-
2-Amino-3,4-dimethylimidazo[4,5-f]quinoline
- MeIQx:
-
2-Amino-3,8-dimethylimidazo[4,5-f]quinoxaline
- MRM:
-
Multiple reaction monitoring
- PhIP:
-
2-Amino-1-methyl-6-phenylimidazo[4,5-b]pyridine
- psi:
-
Pound per square inch
- SPE:
-
Solid phase extraction
- Trp-P-1:
-
3-Amino-1,4-dimethyl-5H-pyrido[4,3-b]indole
References
Sugimura T, Wakabayashi K, Nakagama H, Nagao M (2004) Heterocyclic amines: mutagens/carcinogens produced during cooking of meat and fish. Cancer Sci 95:290–299
Hasegawa R, Sano M, Tamano S et al (1993) Dose-dependence of 2-amino-1-methyl-6-phenylimidazo[4,5-b]-pyridine (PhIP) carcinogenicity in rats. Carcinogenesis 14:2553–2557
Shirai T, Sano M, Tamano S et al (1997) The prostate: a target for carcinogenicity of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) derived from cooked foods. Cancer Res 57:195–198
Sinha R, Peters U, Cross AJ et al (2005) Meat, meat cooking methods and preservation, and risk for colorectal adenoma. Cancer Res 65:8034–8041
Wu K, Giovannucci E, Byrne C et al (2006) Meat mutagens and risk of distal colon adenoma in a cohort of U.S. men. Cancer Epidemiol Biomarkers Prev 15:1120–1125
Ollberding NJ, Wilkens LR, Henderson BE, Kolonel LN, Le Marchand L (2012) Meat consumption, heterocyclic amines and colorectal cancer risk: the Multiethnic Cohort Study. Int J Cancer 131:E1125–E1133
Cross AJ, Peters U, Kirsh VA et al (2005) A prospective study of meat and meat mutagens and prostate cancer risk. Cancer Res 65:11779–11784
Daniel CR, Cross AJ, Graubard BI et al (2012) Large prospective investigation of meat intake, related mutagens, and risk of renal cell carcinoma. Am J Clin Nutr 95:155–162
Skog KI, Johansson MA, Jagerstad MI (1998) Carcinogenic heterocyclic amines in model systems and cooked foods: a review on formation, occurrence and intake. Food Chem Toxicol 36:879–896
Iwasaki M, Kataoka H, Ishihara J et al (2010) Heterocyclic amines content of meat and fish cooked by Brazilian methods. J Food Compost Anal 23:61–69
Kobayashi M, Hanaoka T, Hashimoto H, Tsugane S (2005) 2-Amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) level in human hair as biomarkers for dietary grilled/stir-fried meat and fish intake. Mutat Res 588:136–142
Bessette EE, Yasa I, Dunbar D, Wilkens LR, Le Marchand L, Turesky RJ (2009) Biomonitoring of carcinogenic heterocyclic aromatic amines in hair: a validation study. Chem Res Toxicol 22:1454–1463
Hashimoto H, Hanaoka T, Kobayashi M, Tsugane S (2004) Analytical method of 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine in human hair by column-switching liquid chromatography-mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 803:209–213
Kobayashi M, Hanaoka T, Tsugane S (2007) Validity of a self-administered food frequency questionnaire in the assessment of heterocyclic amine intake using 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) levels in hair. Mutat Res 630:14–19
Tsugane S, Sasaki S, Kobayashi M, Tsubono Y, Sobue T (2001) Dietary habits among the JPHC study participants at baseline survey. Japan Public Health Center-based Prospective Study on Cancer and Cardiovascular Diseases. J Epidemiol 11:S30–S43
Sasaki S, Kobayashi M, Tsugane S (2003) Validity of a self-administered food frequency questionnaire used in the 5-year follow-up survey of the JPHC Study Cohort I: comparison with dietary records for food groups. J Epidemiol 13:S57–S63
Kobayashi M, Hanaoka T, Nishioka S, Kataoka H, Tsugane S (2002) Estimation of dietary HCA intakes in a large-scale population-based prospective study in Japan. Mutat Res 506–507:233–241
Otani T, Iwasaki M, Ikeda S et al (2006) Serum triglycerides and colorectal adenoma in a case–control study among cancer screening examinees (Japan). Cancer Causes Control 17:1245–1252
Yamaji T, Iwasaki M, Sasazuki S, Sakamoto H, Yoshida T, Tsugane S (2012) Association between plasma 25-hydroxyvitamin D and colorectal adenoma according to dietary calcium intake and vitamin D receptor polymorphism. Am J Epidemiol 175:236–244
Takachi R, Ishihara J, Iwasaki M et al (2011) Validity of a self-administered food frequency questionnaire for middle-aged urban cancer screenees: comparison with 4-day weighed dietary records. J Epidemiol 21:447–458
Goodenough AK, Schut HA, Turesky RJ (2007) Novel LC-ESI/MS/MS(n) method for the characterization and quantification of 2′-deoxyguanosine adducts of the dietary carcinogen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine by 2-D linear quadrupole ion trap mass spectrometry. Chem Res Toxicol 20:263–276
Steffensen IL, Janak K, Hegstad S et al (2003) Incorporation of the food mutagen 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) into fur and correlation with intestinal tumourigenesis in Min/+mice. Pharmacol Toxicol 92:131–136
Voutsinas J, Wilkens LR, Franke A et al (2013) Heterocyclic amine intake, smoking, cytochrome P450 1A2 and N-acetylation phenotypes, and risk of colorectal adenoma in a multiethnic population. Gut 62:416–422
Kataoka H, Nishioka S, Kobayashi M, Hanaoka T, Tsugane S (2002) Analysis of mutagenic heterocyclic amines in cooked food samples by gas chromatography with nitrogen-phosphorus detector. Bull Environ Contam Toxicol 69:682–689
Hegstad S, Reistad R, Haug LS, Alexander J (2002) Eumelanin is a major determinant for 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP) incorporation into hair of mice. Pharmacol Toxicol 90:333–337
Acknowledgments
We thank Dr. Loic Le Marchand (Cancer Research Center of Hawaii, University of Hawaii), Dr. Robert J. Turesky (New York State Department of Health), Dr. Hiroyuki Kataoka (School of Pharmacy, Shujitsu University), and Dr. Hiroaki Itoh (Juntendo University Faculty of Medicine) for their helpful advice on the assay of HAA in hair. This study was supported by National Cancer Centre Research and Development Fund, a Grant-in-Aid for Scientific Research (C) (24501366) from the Japan Society for the Promotion of Science, and a Grant-in-Aid for the Third-Term Comprehensive Ten-Year Strategy for Cancer Control from the Ministry of Health, Labour and Welfare of Japan.
Conflict of interest
The authors have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
10552_2014_401_MOESM2_ESM.ppt
Supplementary figure 1. Typical liquid chromatography-electrospray ionization/tandem mass spectrometry chromatograms of rat colon sample in multiple reaction monitoring mode, and fragmentation pattern of N 2-(deoxyguanosine-8-yl)-2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (dG-C8-PhIP)(21). (PPT 379 kb)
Rights and permissions
About this article
Cite this article
Iwasaki, M., Mukai, T., Takachi, R. et al. Validity of a self-administered food frequency questionnaire in the estimation of heterocyclic aromatic amines. Cancer Causes Control 25, 1015–1028 (2014). https://doi.org/10.1007/s10552-014-0401-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10552-014-0401-7