Nutr Res Pract. 2018 Feb;12(1):52-60. English.
Published online Jan 22, 2018.
©2018 The Korean Nutrition Society and the Korean Society of Community Nutrition
Original Article

Development of quantitative index evaluating anticancer or carcinogenic potential of diet: the anti-cancer food scoring system 1.0

Chai Hong Rim
    • Department of Radiation Oncology, Ansan Hospital, Korea University Medical College, 123, Jeokgeum ro, Danwon-gu, Gyeonggi 15355, Korea.
Received October 23, 2017; Revised December 31, 2017; Accepted January 02, 2018.

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

BACKGROUND/OBJECTIVE

Cancer is closely related to diet. One of the most reliable reports of the subject is the expert report from the World Cancer Research Fund & American Institute of Cancer Research (WCRF&AICR). However, majority of the studies including above were written with academic terms and in English. The aim of this study is to create a model, named Anti-Cancer Food Scoring System (ACFS), to provide a simple index of the anticancer potential of food.

SUBJECTS/METHODS

We created ACFS codes of various food groups. The evidence of the ACFS codes was provided by the literature at a level comparable to that suggested in the WCRF&AICR report or from the WCRF&AICR report. The ACFS grade was calculated considering food group, cooking, and normalization. Application was performed for Koreans' 20 common meals, which encompass multinational recipes.

RESULT

We calculated the ACFS grades of Koreans' 20 common meals. The results were not significantly different from the WCRF&AICR guidelines or information from the National Cancer Information Center of Korea. The grades were briefly interpreted as follows: grade S. ideal for cancer prevention; grade A. good for cancer prevention; grade B, might have anticancer potential; grade C, difficult to be regarded as preventive or carcinogenic; grade D, might against cancer prevention; grade E, probably against cancer prevention.

CONCLUSIONS

The ACFS provides a simple index of anticancer potential of diets. This indicator can be useful for the people without expertise, and is effective in evaluating the diets including Asian foods. The ACFS can help design of future clinical or nutritional studies of cancer prevention.

Keywords
Cancer; diet; prevention

INTRODUCTION

Cancer is a disease that might cause death and is a serious social health burden. In 2015, Approximately 90.5 million people worldwide experienced cancer, and it has led to 8.8 million deaths, accounting for 15.7% of all mortalities [1]. The risk of cancer increases with population aging, and is a more serious health problem in developed countries [2]. In the United States, cancer was the second leading cause of death following heart disease, and cancer was the leading cause of death in Japan and Korea, the East Asian countries [3, 4, 5].

The cause of cancer is deeply related to lifestyle including food consumed, and 30–35% of cancer is known to be related to diet [6]. World Cancer Research Fund (WCRF) and Ameican Institute of Cancer Research (AICR) published the second expert report in 2007, which is one of the most comprehensive literature about the association between food, nutrition, physical activity and cancer prevention [7]. In a recent prospective trial, adherence to the WCRF/AICR cancer prevention guideline was related with 61% lower cancer specific mortality [8].

The WCRF/AICR second expert report and its updated online version, which is called Continuous Updated Project (CUP) [9], are comprehensive and evidence-based. However, they contain many academics terms of medical and nutritional aspects, and the volume of reports is so large that it is difficult to understand by those who do not have medical expertise and fluency in English. The report also lacks the ability to analyze a wide range of Asian foods, with the most of the analysis taking place only on Western and some Chinese foods.

The relationship between food and cancer is well-known in common knowledge; for example, vegetable and fruits are known to prevent cancer and meat is to occur cancer. However, relying on common knowledge has risk of biased nutrition, and being shifted by commercial information without evidence. The US's healthy eating index [10] for general health promotion, and the dietary inflammatory index [11] for prevention of cardiovascular disease are examples of indexes that scientifically classified nutritional evidence and providing easy reference. However, there is no simple index that can easily understand the cancer potential of diets.

Food is produced and consumed by people of all socioeconomic classes in all countries. Therefore, we need a simple index of anti-cancer diet that allows to analyze as many regions' diet, but which is also available for those without expertise. The aim of this study is to develop a model, named Anti-Cancer Food Scoring System (ACFS), that can provide a simple index quantitatively evaluating the anticancer or carcinogenic potential of diets.

SUBJECTS AND METHODS

Development of the ACFS codes and normalization

The ACFS codes were developed by modifying the factors in the WCRF/AICR second report [7], excluding the factors related to lifestyle rather than diet (e.g. physical activity, lactation, and sedentary living) and adding more diet related factors to assess wider range of foods including them from Asian regions. The codes were composed of 22 food groups, which were: whole grain (WG), red meat (RM), green leafy salad (GLS), fish (FISH), garlic (Ga), soy food (SF), cruciferous vegetable (CV), allium vegetable (AV), cheese (Ch), seeweed (SW), fruit (FR), non-starchy vegetable (NSV), white meat (WM), carotene-rich vegetable (CRV), processed meat (PM), selenium-rich food (SRF), milk (Mi), egg (Egg), refined grain (RG), legume (Le), Chilli (Chilli), and potato (Pot).

Each code was given cancer-specific grades (CSG) associated with its anticancer or carcinogenic potential. The CSG were assigned in five types of cancers, which have been global health burden with high mortality rates and are the cancers largely affected by diet [6, 10]. These include lung, breast, colorectal, stomach, and liver cancers. The CSG was developed based on the 4 criteria for grading evidence from the WCRF/AICR second expert report; convincing, probable, limited-suggestive, and limited-no conclusion [12]. In ACFS, the evidence levels which is equal or higher than probable level from WCRF/AICR report, which briefly means the evidences supported from ≥ 2 cohort studies or ≥ 5 case control studies (which have good qualities) without substantial unexplained heterogeneity with biological plausibility, were regarded as CSG A. CSG B in ACFS was correlated with limited-suggestive level of WCRF/AICR report, which briefly means the evidences supported from ≥ 2 cohort studies or ≥ 5 case control studies with general consistency and biological plausibility. CSG C in ACFS meant the same level of evidence as the limited-no conclusion level of the WCRF/AICR report.

When CSG was A, B, and C, scores of 10, 5, and 2 were given, respectively. When CSG was related to carcinogenic potential, negative score was given. The CSGs were added for each code, and the summed code points ranged from −20 (RM) to 32 (Fr) points. These summed points were simplified and divided into five code grades; > 21 for code grade A, 11 to 20 for B, 0 to 10 for C, −1 to −10 for D, and −11 to −20 for E. Theoretically, a summed code point can range from −50 to 50, but an extreme score like 50 or −50 is hard to be found in practice. CSG grading is designed considering above, distribution of summed code points, nutritional common knowledge, simplicity and ease of application. Further calculation was performed with the code grades, rather than summed code point. Above process was described in Table 1.

Table 1
Anti-cancer food scoring system code table

Evidence preparation of CSGs

We developed CSGs based on literature evidences. The main reference was the WCRF/AICR second expert report [7] and its updated online version [9].

The preventive effect of the whole grain (ACFS code: WG) for stomach cancer was supported by at least a prospective study [13] and several case-control studies with general consistency [14, 15, 16, 17, 18, 19, 20, 21]. The fiber in the grain is potentially countering the harmful effect of N-nitroso compounds [22, 23]. The relationship was considered as CSG B.

The carcinogenic effect of red meat (ACFS code: RM) consumption for liver cancer, was supported by at least 3 prospective studies [24, 25, 26], but there was heterogeneity among case-control studies [27, 28, 29, 30, 31, 32]. Thus it was regarded as CSG C. The protective effect of fish (ACFS code: FISH) consumption for liver cancer was supported by at least 4 prospective studies [25, 26, 33, 34], and heterogeneity among case-control studies was not substantial [28, 29, 31, 32, 35, 36]. Meta-analysis was performed and risk ratio of high fish intake for liver cancer was 0.78 (95% CI: 0.63–0.90) [37]. Biological plausibility was supported by studies including them about anti-inflammatory effect of poly-unsaturated fatty acids (PUFA) [38]. Therefore, protective effect of fish consumption for liver cancer was regarded as CSG B. The anticancer effect of white meat (ACFS code: WM) consumption for liver cancer was supported by at least 4 prospective and 4 case-control studies [24, 25, 26, 27, 28, 29, 32, 34]. There was no substantial heterogeneity. The anti-inflammatory effect of PUFA also contributes to liver cancer prevention of white meat [39]. The CSG B was allotted for the anticancer effect of white meat for liver cancer.

The association between anticancer effect of soy food (ACFS code: SF) consumption and colorectal cancer was supported by at least 2 prospective studies [40, 41]. A prospective study by Akhter et al. [42] showed no relationship, and the other prospective study by Oba et al. [43]. showed difference of effect according to gender. Case-control studies generally suggested protective effect [44, 45, 46, 47, 48, 49, 50, 51]. The biological plausibility is still not robust [52]. Therefore, the CSG was regarded as C. When discussing the relationship between soy food and stomach cancer, we excluded miso soup or bean paste among the soy foods. Because they often contains significant amounts of salt, miso soup is usually served in the form of hot liquid, and salt and hot beverages are well-known risk factors for gastric cancer [9, 53]. The preventive effect was supported by at least 3 prospective studies [54, 55, 56], and the result of case-control studies were generally consistent [18, 46, 50, 57, 58, 59, 60, 61]. The mechanisms are explained by many hypotheses, including anti-inflammatory and antioxidative effects [62], inhibition of H.pylori growth [63], and inhibition of angiogenesis and increased apoptosis [64]. Therefore, the preventive effect of soy food on stomach cancer, except for miso soup and bean paste, was considered to be CSG B.

The relationship between soy foods and breast cancer is one of the most extensively studied areas. Biological plausibility is well known; soy isoflavone, which is a phytoestrogen of soy food similar to 17-β estradiol in structure but with weaker estrogenic effect, acts as antagonist to the cancer development of endogenous estrogens [65]. In a recent meta-analysis, a total of 35 studies including 12 prospective studies were analyzed [66]. In this study, soy food intake is preventive for breast cancer regardless of menopausal status in Asian women. The cancer preventive effect of soy food in premenopausal Asian women is supported by at least two prospective studies [67, 68], and that in Asian postmenopausal women is also supported by at least two prospective studies [68, 69]. The breast cancer preventive effects of soy foods in premenopausal and postmenopausal Asian women are supported by more than 10 retrospective studies respectively [66]. There is controversy about the breast cancer preventive potential of soy foods in Westerners. However, the amount of soy food intake in the studies of Western women is far lower than that of Asians. In a meta-analysis by Wu et al. [65], the quartile consuming the soy food the most in studies of Asian women was > 20 mg per day and the least consumed quartile was < 5 mg per day. In the studies of Western Women, the highest quartile of intake was > 0.8 mg per day and the lowest quartile was < 0.15 mg per day. The 0.8 mg of isoflavone is the amount of soy milk in < 10 cc. Considering that the soy food intake was too low in studies of Western women, a large number of studies on Asians supported the preventive effect of soy food, and biological plausibility was evident, the breast cancer preventability of soy food was classified as CSG B.

Seaweed (ACFS code: SW) is consumed as food only in limited countries, including Korea and Japan. But it is a very common food in Korea and Japan. Seaweed contains beta-carotene, fucoxanthin, and chlorophyll, which seem to be effective in preventing breast cancer [70, 71]. Also, dietary fiber and digestible algae polysaccharides are abundant, which can be helpful for preventing colorectal cancer [72, 73]. Many other mechanisms and possibilities of cancer prevention were suggested, but large clinical trials are warranted to draw more robust conclusion [74]. We cautiously allotted CSG C for anticancer effect of seaweed for breast and colon cancer.

The references of evidence of other CSGs are summarized in Supplement 1.

Application

Application was performed with 20 commonly consumed meals of Koreans; the composition and food exchange units (FEU) [75] of the ingredients were identified by referring to the Korean Nutrition Society database [76]. Korean lifestyle has been influenced by Asian countries such as China and Japan, and Western countries including the United States. Therefore, common meals of Korean include Chinese, Japanese, and Western food as well as Korean food. The reason for using the FEU other than the weight of the ingredient is that the former is the unit of the concept most similar to the serving, which was the more commonly used measurement than weight in reference studies.

RESULTS

Calculation of the ACFS grade

The ACFS grade, which is the objective index reflecting anticancer or carcinogenic potential of the meals, is calculated in the following steps:

1) Allocate the ACFS code corresponding to the components of the meals. Auxiliary materials for cooking, including salt and cooking oil, are not considered in this step.

2) The FEU of the components given the ACFS code is summed up, and the fraction of the FEU of each component is calculated as a percentile.

3) Multiply the FEU percentage of each component calculated above and the point assigned to the code grade. The point assigned to the code grade is 5 for code grade A, 4 for B, 3 for C, 2 for E, and 1 for E.

4) Sum all the values of components calculated in step 3. This value is called ingredient score.

5) Theoretically, the ingredient score can range from as low as 100 to as high as 500 points. The score of > 400 is classified as grade S, 301 to 400 as A, 251 to 300 as B, 201 to 250 as D, and ≤ 200 as E. The categorization was performed considering distribution of the ingredient scores, common nutritional knowledge, simplicity and ease of use.

6) Finally, two harmful cooking factors [high salt (HS) and high fat (HF)] are used to account for the influence of the cooking method. If > 2 g of salt or > 20 g of oil was used in the cooking process, it is regarded as harmful cooking and the grade is lowered by one level.

The definition of high salt food (2 grams of salt) is made to ensure that the salt intake does not exceed the WHO recommendation (< 5 grams per day) with three meals. The definition of high fat diet was made with reference to the ‘high in fat’ category of Food Standard Agency of US [≥ 21 g of fat per serving (≥ 250 g)] [77] and the Coronary Prevention Group (49.5 kcal from fat/ 100 kcal of food) [78] and considering the composition of 20 Korean common meals. The example of calculating ACFS grade is described in Table 2.

Table 2
Examples of ingredient score calculation

Application of ACFS grades

The final result including ACFS grade of 20 common meals sampled are described in Table 3. Ingredient score ranged from 122 to 449.5. After consideration of harmful cooking method, the ACFS grades of 20 common meals are as follows:

Table 3
Application and ACFS codes of Koreans' common meals

Grade S: designed breakfast, lunch, and dinner

Grade A: fish soup and rice, Maki roll

Grade B: Chinese-style noodles with vegetables and seafood, vegetable and minced meat dumpling, Hand-pulled dough soup, Bibimbap, Sushi, Soybean paste stew and rice

Grade C: kimchi stew and rice, noodle with black soybean sauce, fried rice in thin omelette, Chinese-style fried rice, cold buckwheat noodles, knife-cut noodle soup

Grade D: pork cutlet and rice, ox bone soup and rice, bulgogi

Grade E: instant noodle, sweet and sour fried pork, grilled pork belly

The food exchange list considering the food items in 20 Korean recipes that we have used is listed in Table 4 [75].

Table 4
Foods in the ACFS 1.0 development and the amount corresponding exchange unit

Designed meals were recipes that made ideally for cancer prevention in consideration of ACFS. This designed meal basically refers to the composition of the meal planning as exemplified by the Korean Diabetes Association [75], takes into consideration the cancer preventive potential of ACFS, and has a variety of foods to make the meal enjoyable. The details are as follows:

Designed breakfast: steamed multi-grain rice 1.5 FEU; shredded and seasoned radish 0.5 FEU; seasoned spinach 0.5 FEU; boiled and marinated mackerel pike 2 FEU; kimchi 2.5 FEU

Designed lunch: steamed multi-grain rice 2.5 FEU; boiled tofu 1.5 FEU; white kimchi 0.5 FEU; walnuts and peanuts 1.0 FEU; boiled and marinated anchovy 0.5 FEU; tomato 0.5 FEU; broccoli 0.5 FEU; onion 0.5 FEU

Designed dinner: whole-grain bread 2.0 FEU; steamed salmon 2.0 FEU; lettuce and bokchoi salad 2.0 FEU

ACFS grades interpretation

Grade S: ideal for cancer prevention in terms of composition and cooking method.

Grade A: good for cancer prevention in terms of composition and cooking method.

Grade B: might have cancer prevention potential and some modification can be helpful.

Grade C: difficult to be regarded to have anticancer or carcinogenic potential. Modification is recommended.

Grade D: might be against cancer prevention. Modification is highly recommended.

Grade E: probably against cancer prevention.

DISCUSSION

Dolls & Peto estimated that about one-third of cancer causes are related to food [79]. Recently, the association of diets with cancer is clinically proven beyond estimation. In a recent large prospective studies, the risk of colorectal cancer and breast cancer was reduced by up to 58% and 60%, respectively, in patients who were well adhered the guidelines provided by WCRF & AICR [8, 80]. These guidelines refer to diet, obesity, and lifestyle, and diet account for a significant portion. Since the ACFS model referred much of the principles from WCRF & AICR expert report, ACFS might be expected to have predictive potential for cancer prevention.

The types of cancer that occur in Asian and Western countries are very different. This might be due to racial differences, but is also largely influenced by difference in food intake. For example, it is reported that the stomach cancer, which is prevalent in East Asians countries, is associated with salt-preserved foods; and larger consumptions of soy and fish were reported to prevent cancers including breast or gastrointestinal cancer [7, 36, 37, 41]. We systematically searched the literature and developed the ACFS code to broaden the scope of food analysis than the WCRF & AICR expert report. This will especially help to analyze Asian foods which use a wide variety of ingredients.

To our knowledge, no model has yet been published that quantifies the anticancer and carcinogenic potential of diet. We analyzed 20 Koreans' common meals encompass Korean, Chinese, Japanese, or Western styled foods, and the calculated ACFS grade was in good agreement with the generally recommended diet for cancer prevention [7, 81]. The ACFS model provides estimates from calculations, but its strength is providing the grades that can be understood at a glance. Previously, in order to know the relationship between cancer prevention and diet, a comprehensive understanding of the various studies and guidelines with help of expertise was needed. With the ACFS grade, people without expertise can easily understand the relationship between diet and cancer. The ACFS will develop businesses of catering services or health food products related to cancer prevention, and evolve the cancer prevention business to more evidence-based field.

This study has several limitations. Since the ACFS is a computational estimate, it should be used for reference purposes with other nutritional epidemiologic studies and should be reinforced by future clinical studies. Because the ACFS is a model developed by an oncologist, it has limitation in terms of subjectivity. Cooperation with nutritionists, nurses, and engineers is essential to increase its reliability and utilization. The ACFS currently validates only 20 common meals, and it is necessary to analyze the diverse foods of various countries in the future to increase the reliability.

The ACFS provides a quantitative index of anticancer and carcinogenic potential of diets. This indicator is particularly useful for people without expertise, and is also effective in assessing the diets including Asian foods. This indicator should prove its effectiveness in future clinical studies. We sincerely hope that the ACFS will be able to reduce the fears and suffering caused by malignant cancer.

SUPPLEMENTARY MATERIAL

Supplement Table S1

The reference of all the other Cancer Specific Grades (CSGs) are based on the World Cancer Research Fund (WCRF)/American Institute of Cancer Research (AICR) 2nd expert report [7] and its updated online version (continuous updated project, CUP) [9]. Of note, the evidence level of “limited-no conclusion” in the WCRF/AIRF 2nd expert report or CUP does not necessarily mean that the expert panel judged that there is no evidence of relationship; with further good research, a component of this grade might be shown to increase or decrease cancer risk in the future. If there is a sufficient level of evidence that the component has no relationship with cancer development, it is categorized as “substantial effect on risk unlikely” [12].

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Notes

This study was supported by research grant of Korea University Ansan Hospital.

CONFLICT OF INTEREST:The authors declare no potential conflicts of interests.

References

    1. GBD 2015 Mortality and Causes of Death Collaborators. Global, regional, and national life expectancy, all-cause mortality, and cause-specific mortality for 249 causes of death, 1980-2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet 2016;388:1459–1544.
    1. Stewart B, Wild CP. In: World Cancer Report 2014. Lyon: International Agency for Research on Cancer; 2014.
    1. National Center for Health Statistics (US). Health, United States, 2016: with Chartbook on Long-term Trends in Health. Hyattsville (MD): National Center for Health Statistics; 2017.
    1. Statistics Korea. Cause of death statistics [Internet]. Daejeon: Statistics Korea; 2016 [cited 2017 September 14].
    1. Nagao M, Tsugane S. Cancer in Japan: prevalence, prevention and the role of heterocyclic amines in human carcinogenesis. Genes Environ 2016;38:16.
    1. Anand P, Kunnumakkara AB, Sundaram C, Harikumar KB, Tharakan ST, Lai OS, Sung B, Aggarwal BB. Cancer is a preventable disease that requires major lifestyle changes. Pharm Res 2008;25:2097–2116.
    1. World Cancer Research Fund. American Institute for Cancer Research. Food, Nutrition, Physical Activity, and the Prevention of Cancer: a Global Perspective. Washington, D.C.: AICR; 2007.
    1. Hastert TA, Beresford SA, Sheppard L, White E. Adherence to the WCRF/AICR cancer prevention recommendations and cancer-specific mortality: results from the Vitamins and Lifestyle (VITAL) Study. Cancer Causes Control 2014;25:541–552.
    1. World Cancer Research Fund International (GB). Continuous update project (CUP) [Internet]. London: World Cancer Research Fund International; 2017 [cited 2017 September 14].
    1. Guenther PM, Casavale KO, Reedy J, Kirkpatrick SI, Hiza HA, Kuczynski KJ, Kahle LL, Krebs-Smith SM. Update of the healthy eating index: HEI-2010. J Acad Nutr Diet 2013;113:569–580.
    1. Cavicchia PP, Steck SE, Hurley TG, Hussey JR, Ma Y, Ockene IS, Hébert JR. A new dietary inflammatory index predicts interval changes in serum high-sensitivity C-reactive protein. J Nutr 2009;139:2365–2372.
    1. World Cancer Research Fund. American Institute for Cancer Research. Food, Nutrition, Physical Activity, and the Prevention of Cancer: a Global Perspective. Washington, D.C.: AICR; 2007. pp. 60.
    1. M A M, Pera G, Agudo A, Bueno-de-Mesquita HB, Palli D, Boeing H, Carneiro F, Berrino F, Sacerdote C, Tumino R, Panico S, Berglund G, Manjer J, Johansson I, Stenling R, Martinez C, Dorronsoro M, Barricarte A, Tormo MJ, Quiros JR, Allen N, Key TJ, Bingham S, Linseisen J, Kaaks R, Overvad K, Jensen M, Olsen A, Tjønneland A, Peeters PH, Numans ME, Ocké MC, Clavel-Chapelon F, Boutron-Ruault MC, Trichopoulou A, Lund E, Slimani N, Jenab M, Ferrari P, Riboli E, González CA. Cereal fiber intake may reduce risk of gastric adenocarcinomas: the EPIC-EURGAST study. Int J Cancer 2007;121:1618–1623.
    1. Mayne ST, Risch HA, Dubrow R, Chow WH, Gammon MD, Vaughan TL, Farrow DC, Schoenberg JB, Stanford JL, Ahsan H, West AB, Rotterdam H, Blot WJ, Fraumeni JF Jr. Nutrient intake and risk of subtypes of esophageal and gastric cancer. Cancer Epidemiol Biomarkers Prev 2001;10:1055–1062.
    1. González CA, Riboli E, Badosa J, Batiste E, Cardona T, Pita S, Sanz JM, Torrent M, Agudo A. Nutritional factors and gastric cancer in Spain. Am J Epidemiol 1994;139:466–473.
    1. Chen H, Tucker KL, Graubard BI, Heineman EF, Markin RS, Potischman NA, Russell RM, Weisenburger DD, Ward MH. Nutrient intakes and adenocarcinoma of the esophagus and distal stomach. Nutr Cancer 2002;42:33–40.
    1. De Stefani E, Boffetta P, Deneo-Pellegrini H, Mendilaharsu M, Carzoglio JC, Ronco A. Carbohydrates and risk of stomach cancer in Uruguay. Int J Cancer 1999;82:618–621.
    1. Ji BT, Chow WH, Yang G, McLaughlin JK, Zheng W, Shu XO, Jin F, Gao RN, Gao YT, Fraumeni JF Jr. Dietary habits and stomach cancer in Shanghai, China. Int J Cancer 1998;76:659–664.
    1. Kaaks R, Tuyns AJ, Haelterman M, Riboli E. Nutrient intake patterns and gastric cancer risk: a case-control study in Belgium. Int J Cancer 1998;78:415–420.
    1. López-Carrillo L, López-Cervantes M, Ward MH, Bravo-Alvarado J, Ramírez-Espitia A. Nutrient intake and gastric cancer in Mexico. Int J Cancer 1999;83:601–605.
    1. Harrison LE, Zhang ZF, Karpeh MS, Sun M, Kurtz RC. The role of dietary factors in the intestinal and diffuse histologic subtypes of gastric adenocarcinoma: a case-control study in the U.S. Cancer 1997;80:1021–1028.
    1. Møller ME, Dahl R, Bøckman OC. A possible role of the dietary fibre product, wheat bran, as a nitrite scavenger. Food Chem Toxicol 1988;26:841–845.
    1. Jakszyn P, Bingham S, Pera G, Agudo A, Luben R, Welch A, Boeing H, Del Giudice G, Palli D, Saieva C, Krogh V, Sacerdote C, Tumino R, Panico S, Berglund G, Simán H, Hallmans G, Sanchez MJ, Larrañaga N, Barricarte A, Chirlaque MD, Quirós JR, Key TJ, Allen N, Lund E, Carneiro F, Linseisen J, Nagel G, Overvad K, Tjonneland A, Olsen A, Bueno-de-Mesquita HB, Ocké MO, Peeters PH, Numans ME, Clavel-Chapelon F, Trichopoulou A, Fenger C, Stenling R, Ferrari P, Jenab M, Norat T, Riboli E, Gonzalez CA. Endogenous versus exogenous exposure to N-nitroso compounds and gastric cancer risk in the European Prospective Investigation into Cancer and Nutrition (EPIC-EURGAST) study. Carcinogenesis 2006;27:1497–1501.
    1. Freedman ND, Cross AJ, McGlynn KA, Abnet CC, Park Y, Hollenbeck AR, Schatzkin A, Everhart JE, Sinha R. Association of meat and fat intake with liver disease and hepatocellular carcinoma in the NIH-AARP cohort. J Natl Cancer Inst 2010;102:1354–1365.
    1. Fedirko V, Trichopolou A, Bamia C, Duarte-Salles T, Trepo E, Aleksandrova K, Nöthlings U, Lukanova A, Lagiou P, Boffetta P, Trichopoulos D, Katzke VA, Overvad K, Tjønneland A, Hansen L, Boutron-Ruault MC, Fagherazzi G, Bastide N, Panico S, Grioni S, Vineis P, Palli D, Tumino R, Bueno-de-Mesquita HB, Peeters PH, Skeie G, Engeset D, Parr CL, Jakszyn P, Sánchez MJ, Barricarte A, Amiano P, Chirlaque M, Quirós JR, Sund M, Werner M, Sonestedt E, Ericson U, Key TJ, Khaw KT, Ferrari P, Romieu I, Riboli E, Jenab M. Consumption of fish and meats and risk of hepatocellular carcinoma: the European Prospective Investigation into Cancer and Nutrition (EPIC). Ann Oncol 2013;24:2166–2173.
    1. Kurozawa Y, Ogimoto I, Shibata A, Nose T, Yoshimura T, Suzuki H, Sakata R, Fujita Y, Ichikawa S, Iwai N, Fukuda K, Tamakoshi A. Dietary habits and risk of death due to hepatocellular carcinoma in a large scale cohort study in Japan. Univariate analysis of JACC study data. Kurume Med J 2004;51:141–149.
    1. Huang YS, Chern HD, Wu JC, Chao Y, Huang YH, Chang FY, Lee SD. Polymorphism of the N-acetyltransferase 2 gene, red meat intake, and the susceptibility of hepatocellular carcinoma. Am J Gastroenterol 2003;98:1417–1422.
    1. Kanazir M, Boricic I, Delic D, Tepavcevic DK, Knezevic A, Jovanovic T, Pekmezovic T. Risk factors for hepatocellular carcinoma: a case-control study in Belgrade (Serbia). Tumori 2010;96:911–917.
    1. Yu SZ, Huang XE, Koide T, Cheng G, Chen GC, Harada K, Ueno Y, Sueoka E, Oda H, Tashiro F, Mizokami M, Ohno T, Xiang J, Tokudome S. Hepatitis B and C viruses infection, lifestyle and genetic polymorphisms as risk factors for hepatocellular carcinoma in Haimen, China. Jpn J Cancer Res 2002;93:1287–1292.
    1. Tavani A, La Vecchia C, Gallus S, Lagiou P, Trichopoulos D, Levi F, Negri E. Red meat intake and cancer risk: a study in Italy. Int J Cancer 2000;86:425–428.
    1. Srivatanakul P, Parkin DM, Khlat M, Chenvidhya D, Chotiwan P, Insiripong S, L'Abbé KA, Wild CP. Liver cancer in Thailand. II. A case-control study of hepatocellular carcinoma. Int J Cancer 1991;48:329–332.
    1. Talamini R, Polesel J, Montella M, Dal Maso L, Crispo A, Tommasi LG, Izzo F, Crovatto M, La Vecchia C, Franceschi S. Food groups and risk of hepatocellular carcinoma: a multicenter case-control study in Italy. Int J Cancer 2006;119:2916–2921.
    1. Sawada N, Inoue M, Iwasaki M, Sasazuki S, Shimazu T, Yamaji T, Takachi R, Tanaka Y, Mizokami M, Tsugane S. Japan Public Health Center-Based Prospective Study Group. Consumption of n-3 fatty acids and fish reduces risk of hepatocellular carcinoma. Gastroenterology 2012;142:1468–1475.
    1. Daniel CR, Cross AJ, Graubard BI, Hollenbeck AR, Park Y, Sinha R. Prospective investigation of poultry and fish intake in relation to cancer risk. Cancer Prev Res (Phila) 2011;4:1903–1911.
    1. Fernandez E, Chatenoud L, La Vecchia C, Negri E, Franceschi S. Fish consumption and cancer risk. Am J Clin Nutr 1999;70:85–90.
    1. Wang MP, Thomas GN, Ho SY, Lai HK, Mak KH, Lam TH. Fish consumption and mortality in Hong Kong Chinese--the LIMOR study. Ann Epidemiol 2011;21:164–169.
    1. Luo J, Yang Y, Liu J, Lu K, Tang Z, Liu P, Liu L, Zhu Y. Systematic review with meta-analysis: meat consumption and the risk of hepatocellular carcinoma. Aliment Pharmacol Ther 2014;39:913–922.
    1. Endres S, Ghorbani R, Kelley VE, Georgilis K, Lonnemann G, van der Meer JW, Cannon JG, Rogers TS, Klempner MS, Weber PC, Schaefer EJ, Wolff SM, Dinarello CA. The effect of dietary supplementation with n-3 polyunsaturated fatty acids on the synthesis of interleukin-1 and tumor necrosis factor by mononuclear cells. N Engl J Med 1989;320:265–271.
    1. Ferguson LR. Meat and cancer. Meat Sci 2010;84:308–313.
    1. Yang G, Shu XO, Li H, Chow WH, Cai H, Zhang X, Gao YT, Zheng W. Prospective cohort study of soy food intake and colorectal cancer risk in women. Am J Clin Nutr 2009;89:577–583.
    1. Wang L, Lee IM, Zhang SM, Blumberg JB, Buring JE, Sesso HD. Dietary intake of selected flavonols, flavones, and flavonoid-rich foods and risk of cancer in middle-aged and older women. Am J Clin Nutr 2009;89:905–912.
    1. Akhter M, Inoue M, Kurahashi N, Iwasaki M, Sasazuki S, Tsugane S. Japan Public Health Center-Based Prospective Study Group. Dietary soy and isoflavone intake and risk of colorectal cancer in the Japan public health center-based prospective study. Cancer Epidemiol Biomarkers Prev 2008;17:2128–2135.
    1. Oba S, Nagata C, Shimizu N, Shimizu H, Kametani M, Takeyama N, Ohnuma T, Matsushita S. Soy product consumption and the risk of colon cancer: a prospective study in Takayama, Japan. Nutr Cancer 2007;57:151–157.
    1. Budhathoki S, Joshi AM, Ohnaka K, Yin G, Toyomura K, Kono S, Mibu R, Tanaka M, Kakeji Y, Maehara Y, Okamura T, Ikejiri K, Futami K, Maekawa T, Yasunami Y, Takenaka K, Ichimiya H, Terasaka R. Soy food and isoflavone intake and colorectal cancer risk: the Fukuoka Colorectal Cancer Study. Scand J Gastroenterol 2011;46:165–172.
    1. Ramadas A, Kandiah M. Food intake and colorectal adenomas: a case-control study in Malaysia. Asian Pac J Cancer Prev 2009;10:925–932.
    1. Huang XE, Hirose K, Wakai K, Matsuo K, Ito H, Xiang J, Takezaki T, Tajima K. Comparison of lifestyle risk factors by family history for gastric, breast, lung and colorectal cancer. Asian Pac J Cancer Prev 2004;5:419–427.
    1. Nishi M, Yoshida K, Hirata K, Miyake H. Eating habits and colorectal cancer. Oncol Rep 1997;4:995–998.
    1. Le Marchand L, Hankin JH, Wilkens LR, Kolonel LN, Englyst HN, Lyu LC. Dietary fiber and colorectal cancer risk. Epidemiology 1997;8:658–665.
    1. Inoue M, Tajima K, Hirose K, Hamajima N, Takezaki T, Hirai T, Kato T, Ohno Y. Subsite-specific risk factors for colorectal cancer: a hospital-based case-control study in Japan. Cancer Causes Control 1995;6:14–22.
    1. Hoshiyama Y, Sasaba T. A case-control study of stomach cancer and its relation to diet, cigarettes, and alcohol consumption in Saitama Prefecture, Japan. Cancer Causes Control 1992;3:441–448.
    1. Kono S, Imanishi K, Shinchi K, Yanai F. Relationship of diet to small and large adenomas of the sigmoid colon. Jpn J Cancer Res 1993;84:13–19.
    1. Yu Y, Jing X, Li H, Zhao X, Wang D. Soy isoflavone consumption and colorectal cancer risk: a systematic review and meta-analysis. Sci Rep 2016;6:25939.
    1. Chen Y, Tong Y, Yang C, Gan Y, Sun H, Bi H, Cao S, Yin X, Lu Z. Consumption of hot beverages and foods and the risk of esophageal cancer: a meta-analysis of observational studies. BMC Cancer 2015;15:449.
    1. Wada K, Tsuji M, Tamura T, Konishi K, Kawachi T, Hori A, Tanabashi S, Matsushita S, Tokimitsu N, Nagata C. Soy isoflavone intake and stomach cancer risk in Japan: from the Takayama study. Int J Cancer 2015;137:885–892.
    1. Ko KP, Park SK, Yang JJ, Ma SH, Gwack J, Shin A, Kim Y, Kang D, Chang SH, Shin HR, Yoo KY. Intake of soy products and other foods and gastric cancer risk: a prospective study. J Epidemiol 2013;23:337–343.
    1. Kweon SS, Shu XO, Xiang Y, Cai H, Yang G, Ji BT, Li H, Gao YT, Zheng W, Epplein M. Intake of specific nonfermented soy foods may be inversely associated with risk of distal gastric cancer in a Chinese population. J Nutr 2013;143:1736–1742.
    1. Lee JK, Park BJ, Yoo KY, Ahn YO. Dietary factors and stomach cancer: a case-control study in Korea. Int J Epidemiol 1995;24:33–41.
    1. You WC, Blot WJ, Chang YS, Ershow AG, Yang ZT, An Q, Henderson B, Xu GW, Fraumeni JF Jr, Wang TG. Diet and high risk of stomach cancer in Shandong, China. Cancer Res 1988;48:3518–3523.
    1. Inoue M, Tajima K, Hirose K, Kuroishi T, Gao CM, Kitoh T. Life-style and subsite of gastric cancer--joint effect of smoking and drinking habits. Int J Cancer 1994;56:494–499.
    1. Gao CM, Takezaki T, Ding JH, Li MS, Tajima K. Protective effect of allium vegetables against both esophageal and stomach cancer: a simultaneous case-referent study of a high-epidemic area in Jiangsu Province, China. Jpn J Cancer Res 1999;90:614–621.
    1. Ko KP, Park SK, Park B, Yang JJ, Cho LY, Kang C, Kim CS, Gwack J, Shin A, Kim Y, Kim J, Yang HK, Kang D, Chang SH, Shin HR, Yoo KY. Isoflavones from phytoestrogens and gastric cancer risk: a nested case-control study within the Korean Multicenter Cancer Cohort. Cancer Epidemiol Biomarkers Prev 2010;19:1292–1300.
    1. Sakai T, Kogiso M. Soy isoflavones and immunity. J Med Invest 2008;55:167–173.
    1. Verdrengh M, Collins LV, Bergin P, Tarkowski A. Phytoestrogen genistein as an anti-staphylococcal agent. Microbes Infect 2004;6:86–92.
    1. Yang ZP, Zhao Y, Huang F, Chen J, Yao YH, Li J, Wu XN. Equol inhibits proliferation of human gastric carcinoma cells via modulating Akt pathway. World J Gastroenterol 2015;21:10385–10399.
    1. Wu AH, Yu MC, Tseng CC, Pike MC. Epidemiology of soy exposures and breast cancer risk. Br J Cancer 2008;98:9–14.
    1. Chen M, Rao Y, Zheng Y, Wei S, Li Y, Guo T, Yin P. Association between soy isoflavone intake and breast cancer risk for pre- and post-menopausal women: a meta-analysis of epidemiological studies. PLoS One 2014;9:e89288
    1. Lee SA, Shu XO, Li H, Yang G, Cai H, Wen W, Ji BT, Gao J, Gao YT, Zheng W. Adolescent and adult soy food intake and breast cancer risk: results from the Shanghai Women's Health Study. Am J Clin Nutr 2009;89:1920–1926.
    1. Yamamoto S, Sobue T, Kobayashi M, Sasaki S, Tsugane S. Japan Public Health Center-Based Prospective Study on Cancer Cardiovascular Diseases Group. Soy, isoflavones, and breast cancer risk in Japan. J Natl Cancer Inst 2003;95:906–913.
    1. Wu AH, Koh WP, Wang R, Lee HP, Yu MC. Soy intake and breast cancer risk in Singapore Chinese Health Study. Br J Cancer 2008;99:196–200.
    1. Teas J. The consumption of seaweed as a protective factor in the etiology of breast cancer. Med Hypotheses 1981;7:601–613.
    1. Yamamoto I, Maruyama H, Moriguchi M. The effect of dietary seaweeds on 7,12-dimethyl-benz[a]anthracene-induced mammary tumorigenesis in rats. Cancer Lett 1987;35:109–118.
    1. Ohigashi H, Sakai Y, Yamaguchi K, Umezaki I, Koshimizu K. Possible anti-tumor promoting properties of marine algae and in vivo activity of Wakame seaweed extract. Biosci Biotechnol Biochem 1992;56:994–995.
    1. Moore MA, Park CB, Tsuda H. Soluble and insoluble fiber influences on cancer development. Crit Rev Oncol Hematol 1998;27:229–242.
    1. Tokudome S, Kuriki K, Moore MA. Seaweed and cancer prevention. Jpn J Cancer Res 2001;92:1008–1009.
    1. Korean Diabetes Association. Korean food exchange lists. 3rd edition [Internet]. Seoul: Korean Diabetes Association; 2010 [cited 2017 December 29].
    1. The Korean Nutrition Society Database [Internet]. Seoul: The Korean Nutrition Society; 2017 [cited 2017 September 19].
      Available from: http://www.kns.or.kr/.
    1. Food Standards Agency (GB). Signpost labeling: board paper FSA 06/06/03 (Annex 6) [Internet]. London: Food Standards Agency; 2006 [cited 2017 February 1].
    1. Rayner M, Scarborough P, Stockley L. In: Nutrient Profiles: Options for Definitions for Use in Relation to Food Promotion and Children's Diets. London: British Heart Foundation Health Promotion Research Group, Department of Public Health, University of Oxford; 2004.
    1. Doll R, Peto R. The causes of cancer: quantitative estimates of avoidable risks of cancer in the United States today. J Natl Cancer Inst 1981;66:1191–1308.
    1. Hastert TA, Beresford SA, Patterson RE, Kristal AR, White E. Adherence to WCRF/AICR cancer prevention recommendations and risk of postmenopausal breast cancer. Cancer Epidemiol Biomarkers Prev 2013;22:1498–1508.
    1. National Cancer Information Center of Korea [Internet]. Goyang: National Cancer Information Center; [cited 2017 September 19].

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