Skip to main content
SpringerLink
Log in

Epidemiological research in stomach cancer: progress over the last ten years

  • Guest Editorial
  • Clinical Oncology
  • Published:
Journal of Cancer Research and Clinical Oncology Aims and scope Submit manuscript

Summary

In this paper the progress of epidemiological research in stomach cancer during 1980–1990 is reviewed in respect to regional variation, etiology, and formation of carcinogens. The evaluation of 4 cohort and 16 case-control studies revealed a consistently inverse relationship of stomach cancer risk with raw vegetables, fruit, and wholemeal bread consumption and with vitamin C and carotene intake. Milk, cooked vegetables and vitamins A and E were not consistently found to be related to stomach cancer risk. Positive associations of increasing consumption with stomach cancer risk were occasionally found for processed or particularly prepared meat and fish, and for nitrite. Dietary nitrate intake did not appear to be related to stomach cancer risk in these studies. This latter observation is also supported by metabolic studies in high- and low-risk areas for stomach cancer. Consistently among studies, increased risk for stomach cancer was also found for later availability of refrigeration facilities in the household, non-centralized water supply (especially well water), and high salt intake. Prospective studies agreed in an increased risk for stomach cancer for cigarette smoking, but not for alcohol drinking, whereas case-control studies showed divergent results on these factors. Recent metabolic studies in high- and low-risk areas for stomach cancer or in groups with precursor lesions, with theN-nitrosoproline test as a marker for endogenous nitrosation, revealed inconsistent results. Higher nitrite concentration and increased pH in stomach juice were found to be associated with precursor conditions for stomach cancer. It is still not clear whether intake of preformed carcinogens or endogenous formation in the stomach with or without the inclusion of nitrite is the most important source of tumor-initiating or-promoting substances. Preservation or preparation of meat and fish may play an important role in this process, and vitamin C may be an inhibiting substance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Abbreviations

CI:

confidence interval

References

  • American Cancer Society (1990) Cancer facts and figures 1990. American Cancer Society Inc, Atlanta

    Google Scholar 

  • Armijo R, Gonzales A, Orellana M, Coulson AH, Sayre JW, Detels R (1981) Epidemiology of gastric cancer in Chile: II. Nitrate exposures and stomach cancer frequency. Int J Epidermiol 10:57–62

    Google Scholar 

  • Bartsch H, Ohshima H, Pignatelli B, Calmels S (1989) Human exposure to endogenousN-nitroso compounds: quantitative estimates in subjects at high risk for cancer of the oral cavity, oesophagus, stomach and urinary bladder. Cancer Surv 8:335–362

    Google Scholar 

  • Becker N, Frentzel-Beyme R, Wagner G (1984) Krebsatlas der Bundesrepublik Deutschland. Atlas of cancer mortality in the Federal Republic of Germany. Springer, Berlin Heidelberg New York Tokyo

    Google Scholar 

  • Belman S (1983) Onion and garlic oil inhibits tumor promotion. Carcinogenesis 4:1063–1065

    Google Scholar 

  • Boeing H, Frentzel-Beyme R, Berger M, Berndt V, Göres W, Körner M, Lohmeier R, Menarcher A, Männl HFK, Meinhardt M, Müller R, Ostermeier H, Paul F, Schwemmle K, Wagner KH, Wahrendorf J (1991) Case-control study on stomach cancer in Germany. Int J Cancer 47 (in press)

  • Bramwell NH (1989) The prevalence ofCampylobacter Pylori gastritis among asymptomatic adults. Can Med Assoc J 140:276

    Google Scholar 

  • Buiatti E, Palli D, Decarli A, Amadori D, Avellini C, Bianchi S, Biserni R, Cipriani F, Cocco P, Giacosa A, Marubini E, Puntoni R, Vindigni C, Fraumeni J, Blot W (1989) A case-control study of gastric cancer and diet in Italy. Int J Cancer 44:611–616

    Google Scholar 

  • Buiatti E, Palli D, Decarli A, Amadori D, Avellini C, Bianchi S, Bonaguri C, Cipriani F, Cocco P, Giacosa A, Marubini E, Minacci C, Puntoni R, Russo A, Vindigni C, Fraumeni JF, Blot WJ (1990) A case-control study of gastric cancer and diet in italy: II. Associations with nutrients. Int J Cancer 45:896–901

    Google Scholar 

  • Byers T, Graham S (1984) The epidemiology of diet and cancer. Adv Cancer Res 41:1–69

    Google Scholar 

  • Byers TE, Graham S, Haughey BP, Marshall JR, Swanson MK (1987) Diet and lung cancer risk: findings from the Western New York Diet Study. Am J Epidemiol 125:351–363

    Google Scholar 

  • Chen CS (1989) (Investigation of nitrosamine in drinking water in Huang Shi — a high-risk area of stomach cancer in Fujian province). Chung Hua Liu Hsing Ping Hsueh Tsa Chih 10:359–362

    Google Scholar 

  • Chen J, Ohshima H, Yang H, Li J, Campbell TC, Peto R, Bartsch H (1987) A correlation study on urinary excretion ofN-nitroso compounds and cancer mortality in China. Interim results. IARC Sci Publ 84:503–506

    Google Scholar 

  • Chen VW, Abu-Elyazeed RR, Zavala DE, Ktsanes VK, Haenszel W, Cuello C, Montes G, Correa P (1990a) Risk factors of gastric precancerous lesions in a high-risk Colombian population. I. Salt. Nutr Cancer 13:59–65

    Google Scholar 

  • Chen VW, Abu-Elyazzed RR, Zavala DE, Haenszel W, Ktsanes VK, Rice J, Cuello C, Montes G, Correa P (1990b) Risk factor of gastric precancerous lesions in a high-risk Colombian population. II. Nitrate and nitrite. Nutr Cancer 13:67–72

    Google Scholar 

  • Coggon D, Barker DJ, Cole RB, Nelson M (1989) Stomach cancer and food storage. J Natl Cancer Inst 81:1178–1182

    Google Scholar 

  • Colditz GA, Branch LG, Lipnick RJ, Willett WC, Rosner B, Posner BM, Hennekens CH (1985) Increased green and yellow vegetable intake and lowered cancer deaths in an elderly population. Am J Clin Nutr 41:32–36

    Google Scholar 

  • Correa P (1988) A human model of gastric carcinogenesis. Cancer Res 48:3554–3560

    Google Scholar 

  • Correa P, Fontham E, Pickle LW, Chen V, Lin Y, Haenszel W (1985) Dietary determinants of gastric cancer in South Louisiana inhabitants. J Natl Cancer Inst 75:645–654

    Google Scholar 

  • Craver L (1932) A clinical study of etiology of gastric and esophageal carcinoma. Am J Cancer 16:68–102

    Google Scholar 

  • Cuello C, Correa P, Haenszel W, Gordillo G, Brown C, Archer M, Tannenbaum S (1976) Gastric cancer in Colombia: I. Cancer risk and suspect environmental agents. J Natl Cancer Inst 57:1015–1020

    Google Scholar 

  • Demirer T, Icli F, Uzunalimoglu O, Kucuk O (1990) Diet and stomach cancer incidence. A case-control study in Turkey. Cancer 65:2344–2348

    Google Scholar 

  • Denk W, Hansluwka H, Karrer K (1967) Zur Epidemiologie des Carcinoms: III. Regionale Unterschiede in der Häufigkeit des Magenkrebses in Österreich. Z Krebsforsch Klin Onkol 70:13–30

    Google Scholar 

  • Dooley CP, Cohen H (1988) The clinical significance ofCampylobacter pylori. An Intern Med 108:70–79

    Google Scholar 

  • Editorial Commitee (1979) Atlas of cancer mortality in the People's Republic of China. China Map Press

  • Fontham E, Zavala D, Correa P, Rodriguez E, Hunter F, Haenszel W, Tannenbaum SR (1986) Diet and chronic atrophic gastritis: a case-control study. J Natl Cancer Inst 76:621–627

    Google Scholar 

  • Forman D (1987) Dietary exposure toN-nitroso compounds and the risk of human cancer. Cancer Surv 6:719–738

    Google Scholar 

  • Forman D, Al-Dabbagh S, Doll R (1985) Nitrates, nitrites and gastric cancer in Great Britain. Nature 313:620–625

    Google Scholar 

  • Frentzel-Beyme (1988) Stomach cancer as a subject for epidemiological investigation for etiology and prevention. Saude Publica 5:9–26

    Google Scholar 

  • Gao ZQ (1989a) (Unscheduled DNA synthesis (UDS) in human lymphocytes induced by drinking water in high risk areas of stomach cancer) Chung Hua Liu Hsing Ping Hsueh Tsa Chih 18:171–174

    Google Scholar 

  • Gao ZQ (1989b) (Study on the effect of micronucleus with drinking water in the high risk area of stomach cancer). Chung Hua Yu Fang I Hsueh Tsa Chih 23:308–310

    Google Scholar 

  • Graham S, Haughey B, Marshall J, Brasure J, Zielezney M, Freudenheim J, West D, Nolan J, Wilkinson G (1990) Diet in the epidemiology of gastric cancer. Nutr Cancer 13:19–34

    Google Scholar 

  • Haenszel W (1982) Migrant studies. In: Schottenfeld D, Fraumeni JF (eds) Cancer epidemiology and prevention. Saunders, Philadelphia, pp 194–207

    Google Scholar 

  • Haenszel W, Kurihara M, Locke FB, Shimuzu K, Segi M (1976) Stomach cancer in Japan. J Natl Cancer Inst 56:265–278

    Google Scholar 

  • Hammond EC (1966) Smoking in relation to the death rates of 1 million men and women. Natl Cancer Inst Monogr 19:127–204

    Google Scholar 

  • Herbert WE, Bruske JS (1936) Etiology of cancer of the stomach. Guy's Hospital Rep 86:301–308

    Google Scholar 

  • Hirayama T (1990) Life style and mortality. Karger, Basel

    Google Scholar 

  • Hoey J, Montvermay C, Lambert R (1981) Wine and tobacco: risk factors for gastric cancer in France. Am J Epidemiol 113:668–674

    Google Scholar 

  • Houghton PW, Leach S, Owen RW, McC Mortensen NJ, Hill MJ, Williamson RC (1989) Use of a modifiedN-nitrosoproline test to show intragastric nitrosation in patients at risk of gastric cancer. Br J Cancer 60:231–234

    Google Scholar 

  • Howson CP, Hirayama T, Wynder EL (1986) The decline in gastric cancer: epidemiology of an unplanned triumph. Epidemiol Rev 8:1–27

    Google Scholar 

  • Hu JF, Zhang SF, Jia EM, Wang QQ, Liu SD, Liu YY, Wu YP, Cheng YT (1988) Diet and cancer of the stomach: a case-control study in China. Int J Cancer 41:331–335

    Google Scholar 

  • Ikeda M, Yoshimoto K, Yoshimura T, Kono S, Kato H, Kuratsune M (1983) A cohort study on the possible association between broiled fish intake and cancer. Gann 74:640–648

    Google Scholar 

  • Jedrychowski W, Wahrendorf J, Popiela T, Rachtan J (1986) A case-control study of dietary factors and stomach cancer risk in Poland. Int J Cancer 37:837–842

    Google Scholar 

  • Joossens JV, Geboers J (1981) Nutrition and gastric cancer. Nutr Cancer 2:250–261

    Google Scholar 

  • Joossens JV, Geboers J (1987) Dietary salt and risks to health. Am J Clin Nutr 45:1277–1288

    Google Scholar 

  • Kamiyama S, Ohshima H, Shimada A, Saito N, Bourgade MC, Ziegler P, Bartsch H (1987) Urinary excretion ofN-nitrosamine acids and nitrate by inhabitants in high- and low-risk areas for stomach cancer in northern Japan. IARC Sci Publ 84:497–502

    Google Scholar 

  • Kodama M, Kodama T, Suzuki H, Kondo K (1984) Effect of rice and salty rice diets on the structure of mouse stomach. Nutr Cancer 6:135–147

    Google Scholar 

  • Kono S, Ikeda M, Tokudome S, Kuratsune M (1988) A case-control study of gastric cancer and diet in northern Kyushu, Japan. Jpn J Cancer Res 79:1067–1074

    Google Scholar 

  • Lauren P (1965) The two histological main types of gastric carcinoma: diffuse and so-called intestinal-type carcinoma. Acta Pathol Microbiol Scan 64:31–49

    Google Scholar 

  • La Vecchia C, Negri E, Decarli A, D'Avanzo B, Franceschi S (1987) A case-control study of diet and gastric cancer in northern Italy. Int J Cancer 40:484–489

    Google Scholar 

  • Levi F, La Vecchia C, Te VC (1990) Descriptive epidemiology of adenocarcinomas of the cardia and distal stomach in the Swiss Canton of Vaud. Tumori 76:167–171

    Google Scholar 

  • Li JY, Ershow AG, Chen ZJ, Wacholder S, Li GY, Guo W, Li B, Blot WJ (1989) A case-control study of cancer of the esophagus and gastric cardia in Linixian. Int. J Cancer 43:755–761

    Google Scholar 

  • McLaughlin JK, Gridley G, Block G, Winn DM, Preston-Martin, S. Schoenberg JB, Greenberg RS, Stemhagen A, Austin DF, Ershow AG, Blot W, Fraumeni JF (1988) Dietary factors in oral and pharyngeal cancer. J Natl Cancer Inst 80:1237–1243

    Google Scholar 

  • McLaughlin JK, Hrubec Z, Blot WJ, Fraumeni JF Jr (1990) Stomach cancer and cigarette smoking among US veterans, 1954–1980 (Letter). Cancer Res 50:3804

    Google Scholar 

  • Mirvish SS (1983) The etiology of gastric cancer. Intragastric nitrosamide formation and other theories. J Natl Cancer Inst 71:629–647

    Google Scholar 

  • Mirvish SS (1986) Effects of vitamins C and E onN-nitroso compound formation, carcinogenesis, and cancer. Cancer 58:1842–1850

    Google Scholar 

  • Moller ME, Dahl R, Bockman OC (1988) A possible role of the dietary fibre product, wheat bran, as a nitrite scavenger. Food Chem Toxicol 26:841–845

    Google Scholar 

  • Nomura A (1982) Stomach. In: Schottenfeld D, Fraumeni JF (eds) Cancer epidemiology and prevention. Saunders, Philadelphia, pp 624–637

    Google Scholar 

  • Nomura A, Grove JS, Stemmermann GN, Severson RK (1990) A prospective study of stomach cancer and its relation to diet, cigarettes, and alcohol consumption. Cancer Res 50:627–631

    Google Scholar 

  • Notani PN, Jayant K (1987) Role of diet in upper aerodigestive tract cancers. Nutr Cancer 10:103–113

    Google Scholar 

  • Ohshima H, Bartsch H (1981) Quantitative estimation of endogenous nitrosation in humans by monitoringN-nitrosoproline excreted in the urine. Cancer Res 41:3658–3662

    Google Scholar 

  • Ohshima H, Friesen M, Malaveille C, Brouet I, Hautefeuille A, Bartsch H (1989a) Formation of direct-acting genotoxic substances in nitrosated smoked fish and meat products: identification of simple phenolic precursors and phenyldiazonium ions as reactive products. Food Chem Toxicol 27:193–203

    Google Scholar 

  • Ohshima H, Furihata C, Matsushima T, Bartsch H (1989b) Evidence of potential tumour-initiating and tumour-promoting activities of hickory smoke condensate when given alone or with nitrite to rats. Food Chem Toxicol 27:511–516

    Google Scholar 

  • Parkin DM, Läärä E, Muir CS (1988) Estimates of the worldwide frequency of sixteen major cancers in 1980. Int J Cancer 41:184–197

    Google Scholar 

  • Pisani P, Berrino F, Macaluso M, Pastorino U, Crosignani P, Baldasseroni A (1986) Carrots, green vegetables and lung cancer: a case-control study. Int J Epidemiol 15:463–468

    Google Scholar 

  • Risch HA, Jain M, Choi NW, Fodor JG, Pfeiffer CJ, Howe GR, Harrison LW, Craib KJP, Miller AB (1985) Dietary factors and the incidence of cancer of the stomach. Am J Epidemiol 122:947–959

    Google Scholar 

  • Rojas-Campos N, Sigaran MF, Bravo AV, Jimenez-Ulate F, Correa P (1990) Salt enhances the mutagenicity of nitrosated black beans. Nutr Cancer 14:1–3

    Google Scholar 

  • Sato T, Fukuyama T, Urata G, Suzuki T (1959a) Studies of the causation of gastric cancer: 1. Bleeding in the glandular stomach of mice by feeding with highly salted foods, and a comment on salted foods in Japan. Bull Inst Publ Health (Tokyo) 8:10–13

    Google Scholar 

  • Sato T, Fukujama T, Suzuki T, Takayanagi J, Murakami T, Shiotsuki N, Tanaka R, Tsuji R (1959b) Studies of the causation of gastric cancer: 2. The relation between gastric cancer mortality rate and salted food intake in several places in Japan. Bull Inst Publ Helth (Tokyo) 8:187–198

    Google Scholar 

  • Smans M, Boyle P, Muir CS (1989) Cancer mortality atlas of the European Economic Community. Recent Results Cancer Research 114:253–268

    Google Scholar 

  • Sobala GM, Schorah CJ, Sanderson M, Dixon MF, Tompkins DS, Godwin P, Axon ATR (1989) Ascorbic acid in the human stomach. Gastroenterology 97:357–363

    Google Scholar 

  • Stanley K, Stjernswaerd J, Koroltchouk V (1988) Cancers of the stomach, lung and breast: mortality trends and control strategies. World Health Stat Q 41:107–114

    Google Scholar 

  • Stehr PA, Gloninger MF, Kuller LH, Marsh GM, Radford EP, Weinberg GB (1985) Dietary vitamin A deficiencies and stomach cancer. Am J Epidemiol 121:65–70

    Google Scholar 

  • Stocks P, Karn MA (1933) A cooperative study on the habits, home life, dietary and family histories of 450 cancer patients and of equal number of control patients. Ann Eugen (Lond) 5:237–280

    Google Scholar 

  • Stuehr DJ, Marletta MA (1987) Further studies on murine macrophage synthesis of nitrite and nitrate. IARC Sci Publ 84:335–344

    Google Scholar 

  • Sugimura T, Fujimura S (1967) Tumor production in glandular stomach of rat byN-methyl-N′-nitro-N-nitrosoguanidine. Nature 216:943–944

    Google Scholar 

  • Tajima K, Tominaga S (1985) Dietary habits and gastro-intestinal cancers: a comparative case-control study of stomach and large intestinal cancers in Nogoya, Japan. Jpn J Cancer Res 76:705–716

    Google Scholar 

  • Tannenbaum SR, Wishnok JS, Leaf CD (1990) Cell-mediated nitrosation. J Cancer Res Clin Oncol 116 [Suppl]:1115

    Google Scholar 

  • Tatematsu M, Takahashi M, Fukushima S, Hananouchi M, Shirai T (1975) Effects in rats of sodium chloride on experimental gastric cancers induced byN-methyl-N-nitro-N-nitrosoguanidine or 4-nitroquinoline-1-oxide. J Natl Cancer Inst 55:101–106

    Google Scholar 

  • Trichopoulos D, Ouranos G, Day NE, Tzonou A, Manousos O, Papadimitriou CH, Trichopoulos A (1985) Diet and cancer of the stomach: a case-control study in Greece. Int J Cancer 36:291–297

    Google Scholar 

  • Trock B, Lanza E, Greenwald P (1990) Dietary fiber, vegetables, and colon cancer; critical review and meta-analyses of the epidemiologic evidence. J Natl Cancer Inst 82:650–661

    Google Scholar 

  • Tuyns AJ (1988) Salt and gastrointestinal cancer. Nutr Cancer 11:229–232

    Google Scholar 

  • Ursin G, Bjelke E, Heuch I, Vollset SE (1990) Milk consumption and cancer incidence: a Norwegian prospective study. Br J Cancer 61:456–459

    Google Scholar 

  • Vogelstein B, Fearon ER, Hamilton SR, Kern SE, Preisinger AC, Leppert M, Nakamura Y, White R, Smits AMM, Bos JL (1988) Genetic alterations during colorectal-tumor development. N Engl J Med 319:525–532

    Google Scholar 

  • Wargovich MJ (1987) Diallyl sulfide, a flavor component of garlic (Allium sativum) inhibits Dimethylhydrazine-induced colon cancer. Carcinogenesis 8:487–489

    Google Scholar 

  • Wishnok JS, Richardson DP (1979) Interaction of wheat bran with nitrosamines and with amines during nitrosation. J Agric Food Chem 27:1132–1134

    Google Scholar 

  • Wolff G (1989) Alkoholwirkung am Magen (Effect of alcohol on the stomach). Gastroenterology J 49:45–49

    Google Scholar 

  • Wu-Williams AH, Yu MC, Mack TM (1990) Life-style, workplace, and stomach cancer by subsite in young men of Los Angeles County. Cancer Res 50:2569–2576

    Google Scholar 

  • Yang PC, Davis S (1988) Epidemiological characteristics of adenocarcinoma of the gastric cardia and distal stomach in the United States, 1973–1982. Int J Epidemiol 17:293–297

    Google Scholar 

  • You WC, Blot WJ, Chang YS, Ershow AG, Yang ZT, An Q, Henderson B, Xu GW, Fraumeni JF Jr, Wang TG (1988) Diet and high risk of stomach cancer in Shandong, China. Cancer Res 48:3518–3523

    Google Scholar 

  • Zatonski W, Ohshima H, Przewozniak K, Drosik K, Mierzwinska J, Krygier M, Chmielarczyk W, Bartsch H (1989) Urinary excretion of N-nitrosamino acids and nitrate by inhabitants of high- and low-risk areas for stomach cancer in Poland. Int J Cancer 44:823–827

    Google Scholar 

  • Zentralinstitut für Krebsforschung. Bereich Nationales Krebsregister und Krebsstatistik (Institute of Cancer Research. Section National Cancer Registry and Cancer Statistics) (1981) Krebsinzidenz in der DDR 1978 (Cancer incidence in the GDR 1978). Akademie der Wissenschaften, Berlin

    Google Scholar 

  • Zentralinstitut für Krebsforschung. Bereich Nationales Krebsregister und Krebsstatistik (Institute of Cancer Research. Section National Cancer Registry and Cancer Statistics) (1989) Krebsinzidenz in der DDR 1986 (Cancer incidence in the GDR, 1986). Akademie der Wissenschaften, Berlin

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Epidemiology and Biometry, German Cancer Research Center, Im Neuenheimer Feld 280, W-6900, Heidelberg, Federal Republic of Germany

    H. Boeing

Authors
  1. H. Boeing
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

The “Journal of Cancer Research and Clinical Oncology” publishes in loose succession “Editorials” and “Guest editorials” on current and/ or controversial problems in experimental and clinical oncology. These contributions represent exclusively the personal opinion of the autor The Editors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Boeing, H. Epidemiological research in stomach cancer: progress over the last ten years. J Cancer Res Clin Oncol 117, 133–143 (1991). https://doi.org/10.1007/BF01613137

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01613137

Key words

Search

Navigation