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Dietary Heterocyclic Aromatic Amine Intake and Cancer Risk: Epidemiological Evidence from Japanese Studies Motoki Iwasaki1* and Shoichiro Tsugane2

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Dietary Heterocyclic Aromatic Amine Intake and Cancer Risk: Epidemiological Evidence from Japanese Studies Motoki Iwasaki1* and Shoichiro Tsugane2 Iwasaki and Tsugane Genes and Environment (2021) 43:33 https://doi.org/10.1186/s41021-021-00202-5 REVIEW Open Access Dietary heterocyclic aromatic amine intake and cancer risk: epidemiological evidence from Japanese studies Motoki Iwasaki1* and Shoichiro Tsugane2 Abstract Heterocyclic aromatic amines (HAAs), which are formed from the reaction of creatine or creatinine, amino acids, and sugars in meat and fish cooked at high temperatures, have been shown to be mutagenic in bacterial assays and carcinogenic in animal models. Following advances in the dietary assessment of HAA intake in epidemiological studies - including development of a validated meat-cooking module and a specialized food composition database - a number of epidemiological studies have specifically examined the association of HAA intake and cancer risk, most of which were conducted in Western countries. Given that dietary habits and cooking methods differ across countries, however, epidemiological investigation of dietary HAA intake requires a population-specific assessment method. Here, we developed a practical method for assessing dietary HAA intake among Japanese using a food frequency questionnaire (FFQ) and evaluated its validity for use in epidemiological studies by comparison with 2- amino-1-methyl-6-phenylimidazo [4,5-b] pyridine (PhIP) levels in human hair. The Japan Public Health Center-based Prospective Study reported that daily intake of HAAs among Japanese was relatively low, and that more than 50% of total intake in mainland Japan was derived from fish. Only four case-control studies in Japan have been reported so far, for colorectal, stomach and prostate cancer, and colorectal adenoma. A statistically significant positive association was found between 2-amino-3,4-dimethylimidazo [4,5-f] quinoline (MeIQ) and the risk of colorectal adenoma and between individual and total HAAs and the risk of prostate cancer. In contrast, no association was observed for colorectal or stomach cancer, or for colorectal adenoma among men. We also found that the limited and inconsistent findings among epidemiological studies are due to the difficulty in assessing exposure levels of HAAs. In addition to further evidence from prospective cohort studies in Japanese based on dietary HAA intake estimated by FFQs, studies using other methods to assess HAA exposure, such as biomarkers, are highly anticipated. Keywords: Heterocyclic aromatic amines, Dietary intake, Food frequency questionnaire, Validity, Colorectal cancer, Colorectal adenoma, Prostate cancer, Epidemiological study * Correspondence: [email protected] 1Division of Epidemiology, Center for Public Health Sciences, National Cancer Center, Tokyo, Japan Full list of author information is available at the end of the article © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Iwasaki and Tsugane Genes and Environment (2021) 43:33 Page 2 of 10 Background namely atka mackerel (“hokke”; salted) for salted fish, Heterocyclic aromatic amines (HAAs), which are formed horse mackerel (“aji”; salted and semi-dried split) for by the reaction of creatine or creatinine, amino acids and semi-dried split fish, salmon (“sake”; raw), horse mack- sugars in meat and fish to cooking at high temperatures, erel (“aji”; raw), sardine (“iwashi”; raw), Pacific saury have been shown to be mutagenic in bacterial assays and (“sanma”; raw), mackerel (“saba”; raw), and eel (“unagi”; carcinogenic in animal models [1–3]. They act through seasoned) [17]. Among three meat items (beef, pork and the formation of DNA adducts after metabolic activation chicken) with five different types of cooking preparation via N-oxidation by cytochrome P-450 1A2 (CYP1A2), (pan-fried and stewed for beef; stir-fried, deep-fried and followed by O-acetylation by N-acetyltransferase 1 stewed for pork; grilled and deep-fried for chicken), (NAT1) and N-acetyltransferase 2 (NAT2) [3, 4]. Al- HAA content was measured for pan-fried beef, stir-fried though over 25 mutagenic HAAs have been identified, the pork, and grilled chicken [17]. We then used the mea- most abundant formed in meats are 2-amino-1-methyl-6- sured values for each food item to develop an HAA phenylimidazo [4,5-b] pyridine (PhIP), 2-amino-3,8- composition table to estimate dietary HAA intake from dimethylimidazo [4,5-f] quinoxaline (MeIQx), and 2- the FFQ (Table 1). For processed meat items, the com- amino-3,4,8-trimethylimidazo [4,5-f] quinoxaline (4,8- position table included published values for bacon. DiMeIQx) [4]. Monographs published in 1993 by the Second, we established a calculation method for diet- International Agency for Research on Cancer (IARC) clas- ary HAA intake using the FFQ and the composition sified PhIP, 2-amino-3,4-dimethylimidazo [4,5-f] quinoline table of HAAs [16]. The FFQ consists of food items with (MeIQ) and MelQx as ‘possible human carcinogens’ nine frequency categories and standard portions/units, (Group 2B) because of a lack of evidence from epidemio- and asks about the usual consumption of listed foods logical studies [5]. Since then, advances in the dietary during the previous year. Daily food intake is calculated assessment of HAA intake in epidemiological studies - by multiplying frequency by standard portion and rela- including development of a validated meat-cooking mod- tive size for each food item. The FFQ includes additional ule and a specialized food composition database [6] - led questions about grilled skin consumption using the five to a number of epidemiological studies that specifically quantity categories of almost none, one-third, half, two- examined the association of HAA intake and cancer risk, thirds, to almost all, and preferred doneness levels (very mainly from Western countries [7–13]. well-done, well-done, medium, medium rare, and rare) The formation of HAAs increases with the for pan-fried and grilled beef. HAA intake from fish con- temperature and duration of cooking and varies with the sumption was estimated based on the proportion of type of meat and cooking method. The highest levels are grilled to total fish consumption, the rate of grilled skin produced by pan-frying, barbecuing, and grilling [4, 14]. consumption, the ratio of skin to flesh, and data on These cooking methods are not equivalent across coun- HAA content in the skin and flesh. HAA intake from tries and populations, however. Japanese generally con- meat consumption was estimated based on preferred sume more fish than animal meat, and the chopped and doneness levels and data on HAA content. stir-fried method of meat preparation is favored as much as the grilled cooking method [15]. Thus, foods contrib- Validity of dietary assessment method uting to HAA intake in Japan probably differ from those Evaluating the validity of the FFQ in estimating dietary consumed in Western countries, which in turn indicates HAA intake requires a reference method which reflects the necessity of population-specific methods to assess long-term exposure to dietary HAA intake. A promising dietary HAA intake in epidemiological studies. In this biomarker of PhIP intake is PhIP accumulation in hu- article, we review Japanese studies from the development man hair [18]. A feeding study among non-smokers of dietary assessment to its application in epidemio- using ground beef cooked to two different levels of logical studies. doneness showed a strong dose-dependent increase in hair PhIP levels [19]. Therefore, we first established an Development of dietary assessment method analytical method for PhIP in human hair using liquid We developed a practical method for assessing dietary chromatography-electrospray ionization/tandem mass HAA intake using a food frequency questionnaire (FFQ) spectrometry (LC-ESI/MS/MS) [20]. We then verified used for the Japan Public Health Center-based Prospect- the quantitative performance of the analytical method ive Study (JPHC study) [16]. First, a composition table of using rat fur samples with a controlled level of exposure HAAs was developed using fish and meat items selected to PhIP by investigating the dose–response relationship from the food list in the FFQ. Among 19 fish items, we between three exposure levels (control, 20 ppm, and 200 selected six which are usually grilled. We then disaggre- ppm) in fur collected at four different times. A positive gated the two of these six which are aggregate items, dose–response relationship was observed between dos- and finally measured HAA content in eight fish species, age and PhIP accumulation in rat fur regardless of the Iwasaki
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