{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,14]],"date-time":"2026-09-14T07:55:08Z","timestamp":1789372508055,"version":"build-2803163510"},"reference-count":105,"publisher":"Wiley","issue":"6","license":[{"start":{"date-parts":[[2003,6,26]],"date-time":"2003-06-26T00:00:00Z","timestamp":1056585600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Intl Journal of Cancer"],"published-print":{"date-parts":[[2003,10,10]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>At an individual level<jats:italic>Helicobacter pylori<\/jats:italic>was associated with the occurrence of gastric cancer but in some African and Asian countries its prevalence runs with low gastric cancer rates, the so\u2010called African and Asian enigmas. We assessed whether the association between gastric cancer and<jats:italic>H. pylori<\/jats:italic>prevalence at an area level is modified by the level of exposure to fruits and vegetables, alcohol or tobacco. Regression models were fitted to data from 58 countries using as dependent variable log transformed gastric cancer rates and as independent covariables the<jats:italic>H. pylori<\/jats:italic>prevalence, fruits and vegetables consumption, cigarette smoking, alcohol intake and interaction terms. The levels of alcohol consumption or cigarette smoking modified the association between gastric cancer and<jats:italic>H. pylori<\/jats:italic>infection. Models including<jats:italic>H. pylori<\/jats:italic>prevalence, alcohol consumption, cigarette smoking and the interaction terms<jats:italic>H. pylori<\/jats:italic>\u00d7 alcohol or<jats:italic>H. pylori<\/jats:italic>\u00d7 tobacco were used to compute gastric cancer incidence multiplying regression coefficients by a<jats:italic>H. pylori<\/jats:italic>prevalence of 85% (the approximate median in African countries) and the median figures observed in each continent for alcohol and tobacco availability. The expected gastric cancer incidence per 100,000 would be 5.7 assuming the alcohol and tobacco availability in African countries, 7.0 in Asia and Oceania, 16.0 in America and 26.0 in Europe. The interaction between<jats:italic>H. pylori<\/jats:italic>and cigarette or alcohol consumption may contribute to further explain the international variation in gastric cancer and the so\u2010called African and Asian enigmas. \u00a9 2003 Wiley\u2010Liss, Inc.<\/jats:p>","DOI":"10.1002\/ijc.11306","type":"journal-article","created":{"date-parts":[[2003,8,11]],"date-time":"2003-08-11T13:45:48Z","timestamp":1060609548000},"page":"953-960","source":"Crossref","is-referenced-by-count":76,"title":["<i>Helicobacter pylori<\/i>infection and gastric cancer: Facing the enigmas"],"prefix":"10.1002","volume":"106","author":[{"given":"Nuno","family":"Lunet","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Henrique","family":"Barros","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2003,8,6]]},"reference":[{"key":"e_1_2_6_2_2","unstructured":"World Health Statistics Annual.World Health Organization Databank. Geneva Switzerland. Last updated: November2001. Available from: URL:http:\/\/www.dep.iarc.fr\/who\/menu.htm. Accessed July 15 2002."},{"key":"e_1_2_6_3_2","volume-title":"GLOBOCAN 2000: cancer incidence, mortality and prevalence worldwide. version 1.0. IARC CancerBase No. 5.","author":"Ferlay J","year":"2001"},{"key":"e_1_2_6_4_2","doi-asserted-by":"publisher","DOI":"10.1093\/oxfordjournals.epirev.a036288"},{"key":"e_1_2_6_5_2","doi-asserted-by":"publisher","DOI":"10.1056\/NEJMoa001999"},{"key":"e_1_2_6_6_2","doi-asserted-by":"publisher","DOI":"10.4269\/ajtmh.1999.61.37"},{"key":"e_1_2_6_7_2","doi-asserted-by":"crossref","first-page":"1870","DOI":"10.1128\/jcm.27.8.1870-1873.1989","article-title":"Seroepidemiology of Campylobacter pylori infection in various populations","volume":"27","author":"M\u00e9graud F","year":"1989","journal-title":"J Clin Microbiol"},{"key":"e_1_2_6_8_2","first-page":"944","article-title":"Prevalence of Helicobacter (formally Campylobacter) pylori infection in Saudi Arabia and comparison of those with and without upper gastrointestinal symptoms","volume":"85","author":"Al\u2010Moagel MA","year":"1990","journal-title":"Am J Gastroenterol"},{"key":"e_1_2_6_9_2","doi-asserted-by":"publisher","DOI":"10.1093\/infdis\/161.6.1237"},{"key":"e_1_2_6_10_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF01297451"},{"key":"e_1_2_6_11_2","first-page":"28","article-title":"H. pylori, the most common bacterial infection in Africa: a random serological study","volume":"87","author":"Holcombe C","year":"1992","journal-title":"Am J Gastroenterol"},{"key":"e_1_2_6_12_2","first-page":"1313","article-title":"Helicobacter pylori seroprevalence in the African population of the Cape Peninsula","volume":"89","author":"Sitas F","year":"1994","journal-title":"Am J Gastroenterol"},{"key":"e_1_2_6_13_2","doi-asserted-by":"publisher","DOI":"10.2188\/jea.7.251"},{"key":"e_1_2_6_14_2","doi-asserted-by":"publisher","DOI":"10.1097\/00042737-199804000-00007"},{"key":"e_1_2_6_15_2","doi-asserted-by":"publisher","DOI":"10.1136\/gut.33.4.429"},{"key":"e_1_2_6_16_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1572-0241.2002.05663.x"},{"key":"e_1_2_6_17_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0140-6736(75)90498-5"},{"key":"e_1_2_6_18_2","first-page":"148","volume-title":"World Cancer Research Fund, American Institute for Cancer Research. Food, nutrition and the prevention of cancer: a global perspective","author":"World Cancer Research Fund, American Institute for Cancer Research","year":"1997"},{"key":"e_1_2_6_19_2","doi-asserted-by":"publisher","DOI":"10.1002\/(SICI)1097-0215(19970807)72:4<565::AID-IJC3>3.0.CO;2-O"},{"key":"e_1_2_6_20_2","series-title":"Alcohol drinking IARC monographs on the evaluation of carcinogenic risks to humans","author":"IARC","year":"1988"},{"key":"e_1_2_6_21_2","doi-asserted-by":"publisher","DOI":"10.1054\/bjoc.2001.2140"},{"key":"e_1_2_6_22_2","series-title":"Monographs on the evaluation of carcinogenic risks to humans. Schistosomes, liver flukes and Helicobacter pylori","author":"IARC","year":"1994"},{"key":"e_1_2_6_23_2","doi-asserted-by":"publisher","DOI":"10.1097\/00008469-199512002-00001"},{"key":"e_1_2_6_24_2","doi-asserted-by":"publisher","DOI":"10.1301\/002966402760240345"},{"key":"e_1_2_6_25_2","doi-asserted-by":"publisher","DOI":"10.1097\/00042737-200012050-00004"},{"key":"e_1_2_6_26_2","doi-asserted-by":"publisher","DOI":"10.1093\/jn\/128.9.1450"},{"key":"e_1_2_6_27_2","doi-asserted-by":"publisher","DOI":"10.1080\/003655201750065988"},{"key":"e_1_2_6_28_2","doi-asserted-by":"publisher","DOI":"10.1002\/ijc.10201"},{"key":"e_1_2_6_29_2","doi-asserted-by":"publisher","DOI":"10.1080\/01635589109514118"},{"key":"e_1_2_6_30_2","doi-asserted-by":"publisher","DOI":"10.1002\/ijc.2910560407"},{"key":"e_1_2_6_31_2","doi-asserted-by":"publisher","DOI":"10.1093\/jnci\/83.23.1734"},{"key":"e_1_2_6_32_2","doi-asserted-by":"publisher","DOI":"10.3109\/00365529709028150"},{"key":"e_1_2_6_33_2","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1080\/003655299750026353","article-title":"Helicobacter pylori infection and risk of cardia cancer and non\u2010cardia gastric cancer. A nested case\u2010control study","volume":"33","author":"Hansen S","year":"1999","journal-title":"Scand J Gastroenterol"},{"key":"e_1_2_6_34_2","unstructured":"World Health Organization. World Health Organization Global Report on Alcohol Consumption 1999. Available from: URL:http:\/\/www.who.int. Accessed July 15 2002."},{"key":"e_1_2_6_35_2","unstructured":"Food and Agriculture Organization of the United Nations. FAO food balance sheets. Available from: URL:http:\/\/www.fao.org. Accessed July 15 2002."},{"key":"e_1_2_6_36_2","unstructured":"World Health Organization. Tobacco and health: a global status report. Country profiles by region 1997. Available from: URL:http:\/\/www.cdc.gov\/tobacco\/who\/whofirst.htm. Accessed July 15 2002."},{"key":"e_1_2_6_37_2","unstructured":"National Tobacco Information Online System (NATIONS). Country data. Available from URL:http:\/\/apps.nccd.cdc.gov\/nations. Accessed July 15 2002."},{"key":"e_1_2_6_38_2","series-title":"STATA reference manual","author":"STATA","year":"2001"},{"key":"e_1_2_6_39_2","first-page":"459","volume-title":"Modern epidemiology","author":"Morgenstern H","year":"1998"},{"key":"e_1_2_6_40_2","doi-asserted-by":"publisher","DOI":"10.1097\/00042737-199412000-00005"},{"key":"e_1_2_6_41_2","doi-asserted-by":"publisher","DOI":"10.1155\/1999\/132197"},{"key":"e_1_2_6_42_2","doi-asserted-by":"publisher","DOI":"10.1093\/infdis\/168.1.222"},{"key":"e_1_2_6_43_2","first-page":"189","article-title":"Serologic response to Helicobacter pylori among children and teenagers in Northern Chile","volume":"49","author":"Russell RG","year":"1993","journal-title":"Am J Hyg"},{"key":"e_1_2_6_44_2","doi-asserted-by":"publisher","DOI":"10.1136\/gut.34.12.1672"},{"key":"e_1_2_6_45_2","doi-asserted-by":"publisher","DOI":"10.1093\/oxfordjournals.aje.a117070"},{"key":"e_1_2_6_46_2","doi-asserted-by":"publisher","DOI":"10.1093\/oxfordjournals.aje.a117725"},{"key":"e_1_2_6_47_2","first-page":"398","volume-title":"World Cancer Research Fund, American Institute for Cancer Research. Food, nutrition and the prevention of cancer: a global perspective","author":"World Cancer Research Fund, American Institute for Cancer Research","year":"1997"},{"key":"e_1_2_6_48_2","doi-asserted-by":"publisher","DOI":"10.1289\/ehp.02110479"},{"key":"e_1_2_6_49_2","doi-asserted-by":"publisher","DOI":"10.1016\/0140-6736(93)90938-D"},{"key":"e_1_2_6_50_2","doi-asserted-by":"publisher","DOI":"10.1002\/(SICI)1097-0215(19970729)72:3<453::AID-IJC13>3.0.CO;2-D"},{"key":"e_1_2_6_51_2","doi-asserted-by":"publisher","DOI":"10.1177\/030089168907500503"},{"key":"e_1_2_6_52_2","doi-asserted-by":"publisher","DOI":"10.1002\/1097-0142(19901215)66:12<2569::AID-CNCR2820661220>3.0.CO;2-I"},{"key":"e_1_2_6_53_2","doi-asserted-by":"publisher","DOI":"10.1002\/ijc.2910460410"},{"key":"e_1_2_6_54_2","first-page":"449","article-title":"Antibodies to Helicobacter pylori and pepsinogen levels in children from Costa Rica: comparison of two areas with different risks for stomach cancer","volume":"1","author":"Sierra R","year":"1992","journal-title":"Cancer Epidemiol Biomarkers Prev"},{"key":"e_1_2_6_55_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF00051332"},{"key":"e_1_2_6_56_2","first-page":"37","article-title":"Helicobacter pylori antibodies in areas of Italy at varying gastric cancer risk","volume":"2","author":"Palli D","year":"1993","journal-title":"Cancer Epidemiol Biomarkers Prev"},{"key":"e_1_2_6_57_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF00051331"},{"key":"e_1_2_6_58_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF02065425"},{"key":"e_1_2_6_59_2","first-page":"754","article-title":"Is there a link between the variation in gastric cancer mortality and differences in Helicobacter pylori prevalence in different regions of France?","volume":"23","author":"Broutet N","year":"1999","journal-title":"Gastroenterol Clin Biol"},{"key":"e_1_2_6_60_2","first-page":"113","article-title":"Risk factors for stomach cancer in sixty\u2010five Chinese Counties","volume":"1","author":"Kneller RW","year":"1992","journal-title":"Cancer Epidemiol Biomarkers Prev"},{"key":"e_1_2_6_61_2","doi-asserted-by":"publisher","DOI":"10.1038\/75015"},{"key":"e_1_2_6_62_2","doi-asserted-by":"publisher","DOI":"10.1038\/35006081"},{"key":"e_1_2_6_63_2","doi-asserted-by":"publisher","DOI":"10.1093\/jnci\/94.22.1680"},{"key":"e_1_2_6_64_2","doi-asserted-by":"publisher","DOI":"10.1093\/ije\/25.3.494"},{"key":"e_1_2_6_65_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0016-5085(99)70122-8"},{"key":"e_1_2_6_66_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0016-5085(99)70065-X"},{"key":"e_1_2_6_67_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1523-5378.2001.00044.x"},{"key":"e_1_2_6_68_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1572-0241.2002.07031.x"},{"key":"e_1_2_6_69_2","doi-asserted-by":"publisher","DOI":"10.1128\/JCM.39.4.1323-1327.2001"},{"key":"e_1_2_6_70_2","doi-asserted-by":"publisher","DOI":"10.1097\/00004836-200007000-00008"},{"key":"e_1_2_6_71_2","first-page":"3","article-title":"Epidemiology of Helicobacter pylori in Barbados","volume":"46","author":"Edwards CN","year":"1997","journal-title":"West Indian Med J"},{"key":"e_1_2_6_72_2","doi-asserted-by":"publisher","DOI":"10.1590\/S0074-02761998000200006"},{"key":"e_1_2_6_73_2","doi-asserted-by":"publisher","DOI":"10.1093\/infdis\/169.2.434"},{"key":"e_1_2_6_74_2","doi-asserted-by":"crossref","first-page":"122","DOI":"10.25100\/cm.v31i.3.164","article-title":"Seroprevalencia de anticuerpos anti\u2010Helicobacter pylori en donantes de sangre de regiones colombianas con diferencias en la mortalidad por c\u00e1ncer g\u00e1strico","volume":"31","author":"Bravo LE","year":"2000","journal-title":"Colomb M\u00e9d"},{"key":"e_1_2_6_75_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1365-3156.1999.00480.x"},{"key":"e_1_2_6_76_2","doi-asserted-by":"publisher","DOI":"10.1086\/515663"},{"key":"e_1_2_6_77_2","doi-asserted-by":"publisher","DOI":"10.1086\/315384"},{"key":"e_1_2_6_78_2","first-page":"961","article-title":"Helicobacter pylori and stomach cancer: a case\u2010control study in Venezuela","volume":"9","author":"Plummer M","year":"2000","journal-title":"Cancer Epidemiol Biomarkers Prev"},{"key":"e_1_2_6_79_2","doi-asserted-by":"publisher","DOI":"10.1097\/00042737-199305000-00007"},{"key":"e_1_2_6_80_2","doi-asserted-by":"publisher","DOI":"10.2739\/kurumemedj.47.25"},{"key":"e_1_2_6_81_2","doi-asserted-by":"publisher","DOI":"10.1097\/00042737-200102000-00014"},{"key":"e_1_2_6_82_2","unstructured":"MitchellHM FlynnPJ KhinM BuckleyM BolinTD. Epidemiology ofHelicobacterin Myanmar.European Helicobacter Study Group. Abstracts from Strasbourg Workshop 2001. Available from: URL:http:\/\/www.helicobacter.org\/ehpsh_abstracts_stras_6.htm. Accessed July 15 2002."},{"key":"e_1_2_6_83_2","doi-asserted-by":"publisher","DOI":"10.1097\/00042737-199801000-00009"},{"key":"e_1_2_6_84_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1440-1746.2001.02568.x"},{"key":"e_1_2_6_85_2","doi-asserted-by":"publisher","DOI":"10.1136\/pgmj.75.883.316e"},{"key":"e_1_2_6_86_2","doi-asserted-by":"publisher","DOI":"10.1055\/s-2007-1009067"},{"key":"e_1_2_6_87_2","first-page":"139","article-title":"[Distribution of Helicobacter pylori infection in the adult population of Croatia]","volume":"119","author":"Babus V","year":"1997","journal-title":"Lijec Vjesn"},{"key":"e_1_2_6_88_2","first-page":"132","article-title":"[Prevalence of Helicobacter pylori infection in the Czech Republic\u2010the South Moravia region]","volume":"44","author":"Dite P","year":"1998","journal-title":"Vnitr Lek"},{"key":"e_1_2_6_89_2","first-page":"1313","article-title":"Seroprevalence of Helicobacter pylori infection in an unselected Danish population","volume":"89","author":"Rosenstock SJ","year":"1994","journal-title":"Am J Gastroenterol"},{"key":"e_1_2_6_90_2","doi-asserted-by":"publisher","DOI":"10.1097\/00042737-199406000-00014"},{"key":"e_1_2_6_91_2","doi-asserted-by":"publisher","DOI":"10.3109\/00365528909092247"},{"key":"e_1_2_6_92_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1572-0241.2001.03686.x"},{"key":"e_1_2_6_93_2","first-page":"1387","article-title":"[Epidemiology of Helicobacter pylori infection in Hungary (comparative sero\u2010epidemiologic study)]","volume":"136","author":"Tamassy K","year":"1995","journal-title":"Orv Hetil"},{"key":"e_1_2_6_94_2","doi-asserted-by":"publisher","DOI":"10.3109\/00365529609036904"},{"key":"e_1_2_6_95_2","doi-asserted-by":"publisher","DOI":"10.1097\/00042737-199805000-00004"},{"key":"e_1_2_6_96_2","unstructured":"KupcinskasL MiciulevicieneJ KiudelisG KucinskieneR JonaitisLV. Trends in decreasing ofHelicobacter pylori(HP) prevalence in Lithuania.European Helicobacter Study Group. Abstracts from Strasbourg Workshop 2001. Available from: URL:http:\/\/www.helicobacter.org\/ehpsg_abstracts_stras_6.htm. Accessed July 15 2002."},{"key":"e_1_2_6_97_2","doi-asserted-by":"publisher","DOI":"10.1136\/gut.33.4.452"},{"key":"e_1_2_6_98_2","doi-asserted-by":"publisher","DOI":"10.1136\/bmj.304.6837.1276"},{"key":"e_1_2_6_99_2","first-page":"723","article-title":"Epidemiological study on Helicobacter pylori infection and extra gastroduodenal disorders in Polish population","volume":"50","author":"Bielanski W","year":"1999","journal-title":"J Physiol Pharmacol"},{"key":"e_1_2_6_100_2","doi-asserted-by":"publisher","DOI":"10.1097\/00008469-199412002-00012"},{"key":"e_1_2_6_101_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1523-5378.1996.tb00015.x"},{"key":"e_1_2_6_102_2","doi-asserted-by":"publisher","DOI":"10.1023\/A:1007480625665"},{"key":"e_1_2_6_103_2","doi-asserted-by":"publisher","DOI":"10.1159\/000007799"},{"key":"e_1_2_6_104_2","first-page":"267","article-title":"The prevalence of Helicobacter pylori infection in a defined healthy population in Turkey","volume":"6","author":"\u00d6zden A","year":"1992","journal-title":"Hellenic J Gastroenterol"},{"key":"e_1_2_6_105_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1440-1746.1998.tb00677.x"},{"key":"e_1_2_6_106_2","first-page":"657","article-title":"Seroepidemiology of Campylobacter pyloridis","volume":"99","author":"Morris A","year":"1986","journal-title":"NZ Med J"}],"container-title":["International Journal of Cancer"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1002%2Fijc.11306","content-type":"unspecified","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/ijc.11306","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,12,13]],"date-time":"2024-12-13T13:28:08Z","timestamp":1734096488000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1002\/ijc.11306"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2003,8,6]]},"references-count":105,"journal-issue":{"issue":"6","published-print":{"date-parts":[[2003,10,10]]}},"alternative-id":["10.1002\/ijc.11306"],"URL":"https:\/\/doi.org\/10.1002\/ijc.11306","archive":["Portico"],"relation":{},"ISSN":["0020-7136","1097-0215"],"issn-type":[{"value":"0020-7136","type":"print"},{"value":"1097-0215","type":"electronic"}],"subject":[],"published":{"date-parts":[[2003,8,6]]}}}