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[CANCER RESEARCH 50, 627-631, February 1, 1990]
A Prospective Study of Stomach Cancer and Its Relation to Diet, Cigarettes, andAlcohol Consumption1
Abraham Nomura,2 John S. Grove, Grant N. Stemmermann, and Richard K. Severson
Japan-Hawaii Cancer Study, Kuakini Medical Center, Honolulu, Hawaii 96817
ABSTRACT
From 1965 to 1968 in Hawaii, 7990 American men of Japaneseancestry were interviewed and examined in a cohort study. The intake of20 separate foods in a food frequency questionnaire and the intake ofcarbohydrate and other nutrients, based on a 24-h diet recall history,were recorded. Since then, 150 incident cases of stomach cancer havebeen identified. Although men with stomach cancer (cases) consumedpickles and ham/bacon/sausages more often and fruits and fried vegetables less often than men without cancer (noncases), none of the differenceswas statistically significant. Current cigarette smokers had an increasedrisk (relative risk = 2.7; 95% confidence interval = 1.8 to 4.1) comparedwith nonsmokers, but there was no dose-response effect with heaviercigarette smoking. The consumption of alcohol, either from beer, spirits,or wine, did not affect the incidence of stomach cancer. The failure todetect an association with dietary foods in this study may be due to theomission of many oriental foods in the questionnaire and the limitationsof the 24-h diet recall history.
INTRODUCTION
The major causes of stomach cancer are still unknown, but ithas been hypothesized that the diet plays a principal role in thedevelopment of this disease (1). Foods rich in nitrate or nitriteand their derivatives are strongly suspect as causative agents,but the evidence is not conclusive (1-4). Studies have alsosuggested that a high carbohydrate diet or a high salt dietincreases the risk of gastric cancer, but the findings are notalways consistent (1-3). On the other hand, it is believed thatother foods, mainly fresh vegetables and fruits, may reduce therisk of stomach cancer (1-3). Because the consumption ofvegetables and fruits often increases the intake of vitamin C, itis possible that the antinitrosating properties of this micronu-trient have a protective effect against stomach cancer (2).
As with solid foods, the relation between alcohol intake andgastric cancer is also uncertain. Several researchers have foundthat alcohol drinkers have a greater risk for gastric cancer thannondrinkers (5-9), but others have not supported this observation (10-19). The studies in which a positive association wasobserved did not report a dose-response relationship, suggestingthat the association was not a causal one.
Besides alcohol intake, cigarette smoking has also been studied in relation to gastric cancer risk. Several investigators havefound that cigarette smokers have an elevated risk for stomachcancer compared with nonsmokers (5, 7-10, 20-24). However,these studies usually did not show a dose-response relationship.Other researchers found no association between cigarette smoking and gastric cancer (6, 11, 19).
Because gastric cancer continues to be a significant problemin the United States (25), and because of differences in thefindings of past studies, a prospective study was conducted. It
Received 7/18/89; revised 10/20/89; accepted 10/31/89.The costs of publication of this article were defrayed in part by the payment
of page charges. This article must therefore be hereby marked advertisement inaccordance with 18 U.S.C. Section 1734 solely to indicate this fact.
'Supported by Grant ROI CA 33644 from the National Cancer Institute,
NIH, Bethesda, MD.2To whom requests for reprints should be addreseed, at Japan-Hawaii Cancer
Study, Kuakini Medical Center, 347 N. Kuakini Street, Honolulu. HI 96817.
was done in a cohort of American men of Japanese ancestryliving in Hawaii who have experienced a marked change ingastric cancer risk. Japanese men in Japan have one of thehighest incidence rates of gastric cancer (79.6 cases/100,000population/yr from 1978 to 1981 in Miyagi Prefecture) amongdifferent population groups in the world. Their Japanese counterparts living in Hawaii have a much lower risk for this diseasewith an annual average incidence of 28.9 cases per 100,000men from 1978 to 1982. The average annual rate among whitesin Hawaii is 11.8 cases per 100,000 men (26).
MATERIALS AND METHODS
The subjects for this study were men of Japanese ancestry, bornbetween 1900 and 1919, and residing on the Hawaiian island of Oahu.They were first identified by the Honolulu Heart Program in 1965 withthe use of the comprehensive 1942 Selective Service draft registrationfiles (27). As a result, a brief questionnaire was sent to 12,417 men.This was approximately 2,000 men less than the 14,426 estimated byextrapolation from the 1960 census data to be eligible on Oahu. Of the12,417 men, 1,269 could not be located. Of the remaining 11,148 men,8,006 (71.8%) were interviewed and examined between 1965 and 1968.One hundred eighty (1.6%) died before they could be examined, and2,962 (26.7%) did not participate in the program.
During the interview, the subjects provided information on theircigarette smoking history and alcohol intake patterns. A diet historywas also obtained. First, a food frequency questionnaire was completed,based on the subject's usual dietary practices. Consumption frequency
was recorded for the following 17 food items: table salt/shoyu (soysauce); rice; bread; pastry; udon (flour noodle); miso soup (soup withsoybean base); seaweed; tsukudani (mixed dish of fish, sugar, shoyu,and seaweed); tofu; pickles; fruit; fish; meat; eggs; fried vegetables; milk;and ice cream. Consumption of ham, bacon, or sausage was recordedas a single unit, as was consumption of butter, margarine, or cheese,and candy, jelly, or soda pop. Frequency consumption of these 20 foodswas classified into five categories (almost never, less than 2 times perwk, 2 to 4 times per wk, almost daily, and more than once per day),except for table salt/shoyu and rice. A query was also included in thefood frequency questionnaire in which the subjects were asked if theirpresent diet consisted mostly of oriental, western, or mixed foods.
Next, the subjects completed a diet recall history, based on the 24-hperiod immediately prior to the examination. Their total intake ofcalories, carbohydrates, fat, and protein was estimated from their recallof quantitative amounts of different food items. Food models andserving utensils were used to illustrate portion sizes (28). The methodhas been used by other large-scale dietary studies, such as the Ten StateNutrition Survey of 1968 to 1970 (29) and the First Health andNutrition Examination Survey of 1971-1972 (30). A 7-day diet recordadministered to a sample of the cohort to assess the reliability of the24-h data showed similar levels of nutrient intake for both methods(31).
Alcohol intake was based on the usual monthly intake of beer, spirits(including whiskey, gin, brandy, or other liquor), and wine (includingJapanese sake and fortified wines) among current drinkers. The factorsused to obtain estimates of alcohol content in all beverages consumedwere those used in an earlier analysis (32): 3.7% for beer; 38% forspirits; and 10% for wine.
The subsequent incidence of stomach cancer after examinationamong the men was determined by continuous surveillance of all generalhospitals on Oahu. To reduce the possibility of missing incident cases
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PROSPECTIVE STUDY OF STOMACH CANCER
during the surveillance period, a computer linkage file was establishedwith the Hawaii Tumor Registry, a member of the Surveillance, Epidemiology, and End Results Program of the National Cancer Institute(33). Based on a 19-yr follow-up survey of the study subjects since theirexamination in 1965 to 1968, it was determined that only 1.3% of themen could not be located on Oahu. As a result, the surveillance forincident cases of stomach cancer should be nearly complete.
Each case was confirmed by histológica! examination of tissue obtained by surgery or biopsy. The histological type of stomach cancerwas determined according to the classification of Lauren (34). Forpurposes of presentation, the intestinal-mixed-other type will be referred to as the intestinal type which is separate from the diffuse type.The 16 prevalent cases of stomach cancer at the time of examinationwere excluded from the study.
Each subject's time at risk was computed as the time from his
examination to the histologically confirmed diagnosis of gastric cancer,death, or October 1986, whichever occurred first. Cox's proportional
hazards regression model (35) was used to estimate the relative riskdue to cigarette smoking, alcohol intake, or consumption of variousfoods and nutrients, adjusted by age at examination and other appropriate variables.
RESULTS
Data were available on 7,990 men, representing 140,190person-years at risk after deaths were taken into account. In all,there were 150 incident cases of stomach cancer in the cohort.The age-specific incidence rates per 100,000 person-years atrisk are presented in Table 1. There was an increase in riskwith age for both the intestinal and diffuse histological types ofstomach cancer. An excess in frequency of intestinal over diffusestomach cancer cases was also observed.
In the rest of the data analysis, the findings were comparablefor the two histological types of stomach cancer, so they werecombined. Table 2 shows that current cigarette smokers had anincreased risk for stomach cancer in comparison with never orpast smokers. However, when the current smokers were separated by number of cigarettes smoked per day or by number of
Table 1 Age-specific stomach cancer incidence rates per 100,000 person-years byhistological type
Age at diagnosisof cancer(yr)45-54
55-6465-7475+Intestinal
type10.5(2)°
49.1 (29)127.4(64)150.0(17)Diffuse
type5.2(1)
20.4(12)26.0(13)53.1 (6)All
types15.6(3)74.2
(44)158.8(80)202.4 (23)
" Numbers in parentheses, number of cases.
The histological type of six cases could not be determined.
Table 2 Age-adjusted relative risks and 95% confidence intervals for gastriccancer by cigarette smoking history
CigarettehistoryCigarette
smokingNeverPastCurrentNo.
of cases/noncases29/2377
24/206697/3396Relative
risk1.0
1.02.795%
Confidenceinterval0.6-1.7
1.8-4.1
No. of cigarettes/day forcurrent smokers
Nonsmoker 29/2377 1.01-10 15/451 2.7 1.5-5.111-20 53/1651 2.9 1.9-4.6>20 29/1273 2.4 1.4-4.1
No. of yr of smoking forcurrent smokers
Nonsmoker 29/2377 1.0==25 15/447 3.5 1.9-6.626-35 24/1737 1.5 0.9-2.7>35 58/1199 3.5 2.2-5.6
years of cigarette smoking, there was no indication that the riskprogressively increased with greater exposure.
To analyze the relation between smoking and stomach cancerfurther, the 790 past smokers who quit within 5 yr of theirexaminations were studied separately. They had a relative riskof only 0.9 (95% confidence interval, 0.4 to 2.0) compared withnonsmokers.
Alcohol drinkers had a relative risk of 1.2 for stomach cancercompared with nondrinkers (P = 0.30). Because cigarette smoking was correlated with alcohol intake (r = 0.22), we adjustedfor cigarette smoking status. After adjustment, the relative riskdecreased slightly to 1.1. A detailed look at the relation ofalcohol intake to stomach cancer is presented in Table 3. Inmany instances the relative risk was greater than one, but therewas no suggestion of a progressive increase in gastric cancerrisk by increasing the intake of alcohol from all sources orspecifically from beer, spirits, or wine.
The age-adjusted relative risks of stomach cancer accordingto the intake of the 20 different foods in the food frequencyquestionnaire are listed in Table 4. Pickles and ham/bacon/sausage were consumed more often by cases, and fruits andfried vegetables were consumed less often by cases comparedwith noncases, but none of the differences was statisticallysignificant. The 1144 subjects whose diet consisted mostly oforiental foods had an age-adjusted relative risk of 1.8 (95%confidence interval, 0.8 to 3.8) compared with the 1114 subjectswhose diet was mostly western foods. However, the 5700 subjects who mostly ate a mixture of the two types of foods had arelative risk of 2.1 (95% confidence interval, 1.1 to 4.1).
The dietary data on nutrient intake from the 24-h recallhistory are presented in Table 5. There was no significantassociation between stomach cancer and the consumption oftotal calories or any of the three major nutrients, includingcarbohydrates. Adjustment for the intake of other nutrients didnot affect the results for carbohydrates, protein, or fat.
DISCUSSION
Although there has been much interest in the association ofdiet with stomach cancer, there have been only a few prospectivestudies on this relation (36, 37). Prospective studies have the
Table 3 Relative risks and 95% confidence intervals for gastric cancer by alcoholintake history after adjustment for age and cigarette smoking history
AlcoholhistoryAlcohol
(oz/mo)Nondrinker<55-1415-39a40Beer
(oz/mo)Nondrinker<1010-99100-499iSOOSpirits
(oz/mo)Nondrinker<55-49250Wine
(oz/mo)Nondrinker1>2No.
of cases/noncases51/288124/158125/120423/105723/100464/349610/75417/81928/133728/136586/471029/174026/9258/393124/662913/59111/585Relativerisk1.00.91.21.11.11.00.71.21.11.11.00.91.51.01.01.10.795%
Confidenceinterval0.5-1.40.7-1.90.7-1.90.7-1.90.4-1.40.7-2.10.7-1.80.7-1.70.6-1.41.0-2.20.5-2.10.6-1.90.4-1.3
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Table 4 Age-adjusted relative risks of gastric cancer by dietary items in foodfrequency history questionnaire Table 4—Continued
FooditemTable
salt/shoyuNever-seldomAfter
tastingAlwaysRicesi/daya2/dayBreadsl/wk2-4/wk>5/wkPastrySl/wk2-4/wk=:5/wkUdon<l/wk>2/wkMiso
soup<l/wk2-4/wk=r5/wkNori,
kobu, otherseaweeds<l/wk2-4/wk25/wkTsukudanisl/wk2-4/wk>5/wkTofusl/wk2-4/wk>5/wkHam,
bacon,sausage<l/wk2-4/wk>5/wkPickles<l/wk2-4/wk*5/wkFruit<l/w2-4/w25/wFish£l/w2-4/wi5/wMeatsl/wk2-4/wk>5/wkEggssl/wk2-4/wk;>5/wkFried
vegetablessl/wk>2/wkMilk<l/wk2-4/wk>5/wkNo.
of cases/noncases34/213486/382227/174065/393285/390810/5569/492131/679194/496137/195219/926126/687524/962124/657423/10963/168118/626627/11195/451137/72369/3854/218117/617930/14963/16471/365943/254936/163154/304331/191965/287623/121728/142798/519569/431071/295410/57528/142490/399732/241623/141040/242087/4009141/72309/60880/461516/65954/2564Relativerisk1.01.41.01.01.31.01.21.01.01.01.11.01.41.01.00.91.01.20.61.01.11.01.00.90.71.01.01.31.00.91.21.01.00.81.01.40.91.01.20.81.01.01.31.00.81.01.51.295%
Confidenceinterval0.9-2.10.6-1.61.0-1.90.5-2.80.5-1.90.7-1.50.7-1.80.9-2.10.6-1.60.5-1.30.8-1.90.2-1.40.6-2.20.4-2.60.6-1.40.2-2.30.7-1.40.9-2.00.6-1.50.8-1.70.6-1.70.5-1.31.0-1.90.5-1.80.8-1.80.5-1.30.6-1.70.8-2.00.4-1.60.8-2.50.8-1.6FooditemIce
creamsl/wk2-4/wk>5/wkButter,
margarine,cheesesl/wk2-4/wk=iS/wkCandy,
jelly,sodasl/wk2-4/wk>5/wkNo.
of cases/ Relativenoncasesrisk101/5211
1.031/18740.918/751
1.124/164213/900113/529630/207635/161085/4153.0.1.4.0.5.495%
Confidenceinterval0.6-1.30.7-1.80.5-2.10.9-2.20.9-2.51.0-2.2
Table 5 Relative risks and 95% confidence intervals for stomach cancer bynutrient intake, based on the 24-h dietary recall questionnaire
NutrientsTotal
calories<20002000-2499
>2500Total
carbohydrates (g)<200200-299
>300Total
fat (g)<6565-99
>100Total
protein (g)<7575-99alOONo.
of cases/noncases58/294949/2174
43/271746/2207
63/324641/238754/2544
52/292344/237346/2453
45/242159/2966Relative
risk"1.0
1.3(0.9-1.9)'1.0(0.7-1.5)1.0
1.0(0.7-1.4)0.9(0.6-1.4)1.0
0.9(0.6-1.4)1.1(0.8-1.7)1.0
1.1 (0.7-1.6)1.3(0.8-1.9)Relative
risk"1.0
0.9(0.6-1.4)0.9(0.5-1.4)1.00.9(0.6-1.4)
1.1(0.7-1.9)1.0
1.0(0.7-1.6)1.1 (0.7-1.9)
°Adjusted for age.4 Adjusted for age and other two nutrients in the table.c Numbers in parentheses. 95% confidence interval.
advantage of collecting dietary data earlier in time before thesubjects are subsequently diagnosed with their cancers. The 150incident cases of stomach cancer in this study were followed anaverage of 10.6 yr (range, 3 mo to 18.8 yr) before they werediagnosed with their cancer. However, one limitation of thepresent study was that the dietary questionnaire was originallydesigned for a study of cardiovascular diseases instead of stomach cancer. Nonetheless, it did provide information from a 24-h diet recall history and the frequency of intake of 20 foodsamong 7990 men. Some of the foods, including pickles, ham/bacon/sausage, rice, and fruits and vegetables, have been associated with stomach cancer in past studies (6-8, 11, 15, 23, 38).
The study revealed no statistically significant associationbetween stomach cancer and the intake of any of the 20 foodsin the questionnaire. Two of the foods had a high content ofnitrate or related compounds, ham/bacon/sausage and pickles.Although frequent consumers of these items had an elevatedrisk for stomach cancer, the association was not impressive.Pickles included American pickles, Japanese tsukemono(pickled vegetables), takuwan (pickled turnip), and ume (pickledplum). If we also consider the intake of combinations of foods,the 747 subjects who were frequent consumers (>5 times/wk)of both food categories (ham/bacon/sausage and pickles) had arelative risk of 1.6 (95% confidence interval, 0.9 to 2.9) compared with the infrequent consumers (< once a wk), but theassociation was not statistically significant (P = 0.10).
Past studies have made a strong case that foods high innitrate or related compounds are linked to the occurrence of
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gastric cancer (1-4). However, several studies have not shownthis association (6, 12, 14, 17, 39, 40). 7V-Nitroso compoundswhich can be formed from nitrate or nitrite are potent carcinogens, as shown in experiments with many laboratory animals(41). It is likely that the endogenous formation of nitrite and/V-nitroso compounds (42) contributes to the difficulty in relating exogenous sources of these compounds to stomach cancerrisk.
The intake of fruits and fried vegetables was negatively relatedto stomach cancer, but the magnitude of the association wasnot statistically significant. Earlier studies have been fairlyconsistent in showing a possible protective effect of fruits andvegetables against gastric cancer (3), although they are exceptions (17, 23). Particular attention has been focused on vitaminC which can prevent the formation of /V-nitroso compounds invitro or in vivo (43, 44). Case-control studies have suggestedthat food rich in vitamin C, such as oranges, lettuce, tomatoes,lemons, and citrus fruits, is protective against stomach cancer(7, 10-12, 15, 22, 39). These specific food items were notincluded individually in the study questionnaire.
There was no general pattern in the results to suggest thatoriental foods (rice, udon, miso soup, nori/kobu/other seaweeds, tsukudani, tofu) had a positive association and westernfoods (bread, pastry, meat, ice cream, butter/margarine/cheese)a negative association. Except for rice, each of the other fiveoriental foods was consumed more than once a week by only616 to 1693 (8 to 21%) of the study subjects. The inclusion ofonly a few oriental food items in the questionnaire and therelative infrequency of their consumption could have contributed to the study's inability to identify specific oriental foods
associated with the risk of gastric cancer.When the subjects were asked about their general diet, those
who predominantly ate oriental foods did have a relative riskof 1.8 for gastric cancer compared with subjects whose dietconsisted mostly of western foods. However, the majority ofsubjects (5700 men) said they ate mostly a mixture of the twotypes of foods, and their relative risk was greater than that ofthe oriental food consumers.
An earlier study documented that the Japanese in Hawaiiconsume less carbohydrates than the Japanese in Japan (45). Ifcarbohydrates increase stomach cancer risk, then this observation is consistent with the decrease in stomach cancer amongthe Japanese in Hawaii. However, we did not find that carbohydrate intake, based on the 24-h recall history, was positively
related to gastric cancer risk. The frequent consumers of carbohydrates from oriental sources (rice and udon) had an elevated risk for stomach cancer, but the association was notstatistically significant (P = 0.12 for rice and 0.17 for udon).Overall, the data suggest that there is no relation betweencarbohydrate intake and stomach cancer or that an associationwas not detected due to the limitation of a 24-h diet recallquestionnaire even in a prospective study of almost 8000 subjects.
It is not certain why the present study did not find a significant association between the intake of diet and stomach cancer,as shown in past case-control studies. The possibility exists thatthe format of the food frequency questionnaire was not sensitiveenough to detect meaningful differences in dietary intake, although similar food frequency questionnaires were used byothers (6, 23, 40). The diet history was focused on currentdietary practices which could be a limiting factor. A possibleindication of this limitation is that our study subjects were notfrequent consumers of the few oriental foods in the questionnaire which they might have eaten more regularly when they
were younger. The present study did not specifically include anumber of other food items that have been positively related togastric cancer in past studies, such as broiled fish (37), dried/salted or smoked fish (8, 15, 23), other salted foods (18),potatoes (5, 40), other pickled vegetables (8), and other foodsrich in nitrate-related compounds (7, 22). On this basis, thisstudy does not rule out the possibility that other foods orcombinations of foods may be etiologically related to gastriccancer.
Current cigarette smokers had a strong increase in risk forgastric cancer. However, there was no accentuation in risk withincreased cigarette smoking. In addition, recent past smokersdid not have an elevated risk for gastric cancer. These findingssupport the view that smokers who persist in their habit sharea common characteristic that increases their risk, but it is likelyto be independent of the effects of cigarette smoking. A numberof other studies have also observed that cigarette smokers hadan elevated stomach cancer risk that was not related to amountof cigarettes smoked (7-9, 20, 21, 23, 24). However, threerecent case-control studies have reported a modest, but statistically significant dose-response relation between cigarettesmoking and stomach cancer (5, 10, 22). Subjects who smokedmore than 25 yr had an odds ratio of 2.3 in one study (5), andsmokers who smoked one or more packs a day had an oddsratio of 1.5 in another study (10). These findings are balancedby the observation that three past case-control studies have notfound any association between cigarette smoking and stomachcancer (6, 11, 19).
The evidence in our study of an association between alcoholintake and gastric cancer risk was not compelling. Drinkers hada higher risk than nondrinkers, but the magnitude of the riskwas small. Furthermore, there was no association of risk withincrease in alcohol intake from either beer, spirits, or wine.
Past investigations have reported equivocal findings in studying this association. Several case-control studies have observedthat alcohol drinkers had an elevated risk for stomach cancer(5-9). These studies implicated beer (8), hard liquor (7), redwine (9), or the combined sources of alcohol (5, 6). The magnitude of the relative risk was usually less than 2, and a dose-response relation was either not found or not reported. Two ofthe studies observed the association mainly when alcohol wastaken on an empty stomach (5, 6). Ten previous case-controlstudies have not observed any association between alcoholintake and stomach cancer risk (10-19). The only previousprospective study on this subject did not find any association(18). The weight of evidence thus far does not indicate thatalcohol intake is a strong independent risk factor for gastriccancer.
ACKNOWLEDGMENTS
The authors gratefully acknowledge the following institutions fortheir helpful cooperation: Castle Medical Center; Kaiser Medical Center; Queen's Medical Center; St. Francis Hospital; SträubClinic and
Hospital; Tripler Medical Center; Wahiawa General Hospital; and theHawaii Tumor Registry.
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