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Validity of a self-administered food frequency questionnaire in the estimation of heterocyclic aromatic amines

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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.

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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

  1. 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

    Article  CAS  PubMed  Google Scholar 

  2. 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

    Article  CAS  PubMed  Google Scholar 

  3. 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

    CAS  PubMed  Google Scholar 

  4. 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

    Article  CAS  PubMed  Google Scholar 

  5. 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

    Article  CAS  PubMed  Google Scholar 

  6. 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  7. 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

    Article  CAS  PubMed  Google Scholar 

  8. 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. 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

    Article  CAS  PubMed  Google Scholar 

  10. 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. 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

    Article  CAS  PubMed  Google Scholar 

  12. 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. 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

    Article  CAS  PubMed  Google Scholar 

  14. 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

    Article  CAS  PubMed  Google Scholar 

  15. 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

    Article  CAS  PubMed  Google Scholar 

  16. 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

    Article  PubMed  Google Scholar 

  17. 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

    Article  PubMed  Google Scholar 

  18. 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

    Article  PubMed  Google Scholar 

  19. 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

    Article  PubMed  Google Scholar 

  20. 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

    Article  PubMed Central  PubMed  Google Scholar 

  21. 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. 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

    Article  CAS  PubMed  Google Scholar 

  23. 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

    Article  CAS  PubMed  Google Scholar 

  24. 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

    Article  CAS  PubMed  Google Scholar 

  25. 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

    Article  CAS  PubMed  Google Scholar 

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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.

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The authors have no conflict of interest.

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Correspondence to Motoki Iwasaki.

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Supplementary material 1 (DOCX 64 kb)

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)

Supplementary material 3 (XLSX 19 kb)

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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

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  • DOI: https://doi.org/10.1007/s10552-014-0401-7

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