Original Article
Helicobacter pylori Infection and Gastric Carcinoma among Japanese Americans in Hawaii
N Engl J Med 1991; 325:1132-1136October 17, 1991
- Abstract
- Abstract
Background.
Helicobacter pylori are gram-negative spiral bacteria that are associated with chronic gastritis, a known precursor of gastric carcinoma. Persons at high risk for gastric carcinoma have been shown to have a high prevalence of H. pylori infection.
Methods.
We studied the relation of H. pylori infection and gastric carcinoma in a cohort of Japanese American men living in Hawaii. The 5908 men were enrolled and examined from 1967 to 1970. By 1989, 109 cases of pathologically confirmed gastric carcinoma had been identified. The stored serum of each patient with gastric carcinoma and of each matched control subject was tested for the presence of serum lgG antibody to H. pylori.
Results.
Ninety-four percent of the men with gastric carcinoma and 76 percent of the matched control subjects had a positive test for H. pylori antibodies, for an odds ratio of 6.0 (95 percent confidence interval, 2.1 to 17.3). As the level of antibody to H. pylori increased, there was a progressive increase in the risk of gastric carcinoma (P for trend = 0.0009). The association was strong even for men in whom the diagnosis was made 10 or more years after the serum sample was obtained (odds ratio, 10.5; 95 percent confidence interval, 2.5 to 44.8).
Conclusions.
Infection with H. pylori is strongly associated with an increased risk of gastric carcinoma. However, most persons infected with H. pylori will never have gastric carcinoma. Therefore, other factors that increase the risk of gastric carcinoma among persons infected with H. pylori need to be identified. (N Engl J Med 1991; 325:1132–6.)
Article Activity
- Article
GASTRIC carcinoma is one of the most frequently diagnosed malignant diseases worldwide,1 and in the United States it was the leading cause of death due to cancer in 1930.2 Since then, the mortality rate for gastric carcinoma has fallen steadily in the United States. Although the reasons for this decline are not known, epidemiologic data indicate that exposure to environmental factors is important in the pathogenesis of gastric carcinoma.3 , 4
Helicobacter pylori are gram-negative microaerophilic spiral bacteria that have been identified and cultured only in the past decade.5 They can colonize the gastric mucosa for years,6 , 7 and their presence is strongly associated with chronic, diffuse, superficial gastritis of the fundus and antrum.8 10 As a result, they are now believed to have an etiologic role in gastritis.11 , 12 Recent evidence suggests that H. pylori gastritis may progress over several decades to chronic atrophic (type B) gastritis,13 , 14 a lesion that is a precursor of gastric carcinoma.15 17
The epidemiologic features of gastric carcinoma and H. pylori infection are similar,18 , 19 and recent studies suggest that H. pylori infection may be a risk factor for gastric carcinoma.20 23 We conducted a prospective study of H. pylori infection in a relatively homogeneous population — American men of Japanese ancestry in Hawaii — that has a high rate of gastric carcinoma.1
Methods
Study Population
The study population consisted of Japanese American men born from 1900 to 1919 who were identified by the Honolulu Heart Program in 1965 with use of the comprehensive 1942 Selective Service draft-registration files.24 Of 11,148 eligible men, 8006 (72 percent) were interviewed and examined from 1965 to 1968, 180 (2 percent) died before they could be examined, and 2962 (26 percent) did not participate in the program. The data collected on these men included birthplace, marital status, history of alcohol use, blood pressure, and body-mass index (the weight in kilograms divided by the square of the height in meters). Serum cholesterol values were determined by the AutoAnalyzer N-24A method, and serum glucose values were determined one hour after a 50-g glucose load had been given by the AutoAnalyzer N-2B method.25
A total of 7498 (94 percent) of the men returned for a second examination between 1967 and 1970, at which time a serum specimen was obtained. Blood samples from a random sample of 20 percent of the men were sent to the U.S. Public Health Service Hospital in San Francisco, whereas samples from the remaining 5924 men were stored at —20°C at the study site. Sixteen of the 5924 men had stomach cancer at the time of examination and were thus excluded from the study.
Surveillance Methods
To identify cases of stomach cancer occurring in the cohort during the study, discharge records of all general hospitals on Oahu were monitored. To reduce the possibility of missing diagnosed cases, a computer linkage file was established with the Hawaii Tumor Registry, a member of the Surveillance, Epidemiology and End Results Program of the National Cancer Institute.26 The data should be nearly complete, because only 1.3 percent of the men could not be located on Oahu during a survey conducted by mail 19 years later.
There were 137 cases of gastric carcinoma diagnosed from 1968 to 1989 and confirmed by examination of tissue obtained surgically or by biopsy. An additional seven cases were diagnosed clinically but were not confirmed histologically and thus were excluded from the study. Twenty-six of the 137 men with histologically confirmed cases had an insufficient amount of stored serum, and they were also excluded from the study. The histologic type of carcinoma was determined according to the classification of Lauren.27 For purposes of presentation, the intestinal-mixed-other type will be referred to as the intestinal type, which is separate from the diffuse type.28 There were 81 cases of intestinal-type cancer, 25 cases of diffuse-type cancer, and 5 cases whose type was unknown. The staging of the cancer at the time of diagnosis was based on the system of the American Joint Committee for Staging and End Results Reporting.29
Selection of Control Subjects
Each case patient was matched with one control subject from the study cohort according to age at examination (49 to 70 years) and date of serum collection. If a potential control subject had had a gastrectomy before the serum was obtained or had been given a diagnosis of peptic ulcer disease according to hospital records before or after the serum was obtained, he was excluded from the study. As a result, 739 subjects (13 percent) were removed from the control pool of 5764 men. This was done because of the reported association between H. pylori infection and peptic ulcer disease11 , 12 and because we plan to study the subjects with peptic ulcer disease separately. In addition, 336 men (6 percent) were excluded because they had cardiovascular disease or some other type of cancer at enrollment, and 1532 (27 percent) were excluded because cardiovascular disease or cancer was diagnosed after the serum collection. This was done because the serum samples from these men were being used for other studies. Of 3157 men remaining in the pool of control subjects, 111 (4 percent) were matched to patients with gastric carcinoma. Each control subject was alive at the time his respective case patient was given the diagnosis of gastric carcinoma.
Serologic Methods
The presence of serum IgG antibodies to H. pylori was determined by enzyme-linked immunosorbent assay (ELISA) with the Pyloristat kit (Whittaker Bioproducts, Walkersville, Md.). As validated by the manufacturer, the results of this assay closely mirror the results of an IgG ELISA, as previously described.9 , 30 33 In brief, the serum samples were diluted 1:20 for use in the kit, and serum IgG levels were determined according to the manufacturer's instructions. The serum specimens were coded so that the laboratory technician could not identify their source. A ratio of 1.00 or more was considered positive, below 0.80 considered negative, and 0.80 to 0.99 considered indeterminate, as calibrated in the kit. Two men with gastric carcinoma had indeterminate values, so they and their matched controls were excluded from the study.
Statistical Analysis
The t-test for paired samples was used for the comparison of means, and McNemar's test was used for the comparison of the distribution of various characteristics between patients and control subjects. Odds ratios for stomach cancer, based on the results of the H. pylori IgG-antibody test, were derived from conditional logistic-regression methods.34 When the odds ratios for stomach cancer were indeterminate, because there were no matched pairs in which the patient had a negative test and the control had a positive test, approximate confidence intervals were determined by the method of Breslow and Day.34 Tests for linear trend in the logit of risk were derived from conditional logistic-regression models through the use of grouped H. pylori test results (coded as 1, 2, 3, or 4). All models of conditional logistic regression were fitted by using iterative maximum-likelihood methods and a special application of the proportional-hazards regression model.35 The estimate of the attributable risk of gastric carcinoma related to a positive H. pylori antibody test was based on the method of Walter.36
Results
The characteristics of the 109 patients with gastric carcinoma and their matched controls are shown in Table 1Table 1
Characteristics of Patients with Gastric Carcinoma and Control Subjects.. The two groups of men were similar with respect to demographic characteristics and laboratory values.Ninety-four percent of the men with gastric carcinoma (103 of 109) and 76 percent of the control subjects had a positive test for H. pylori—specific IgG antibody (Table 2Table 2
Odds Ratios for the Association of Gastric Carcinoma with H. pylori Seropositivity, According to the Histologic Type of Cancer.). Subjects with a positive test had an odds ratio of 6.0 (P = 0.0009) for gastric carcinoma. Because of the strength of the association, the population-attributable risk of gastric carcinoma due to H. pylori infection (as indicated by a positive antibody test) was also calculated. It was estimated that 63 percent (95 percent confidence interval, 37 to 89) of the gastric carcinoma in this cohort was attributable to H. pylori infection.When the cases were separated according to histologic type, the association was statistically significant for intestinal-type cancer and for diffuse-type cancer. Because none of the patients with diffuse-type disease had a negative antibody test, their odds ratio was indeterminate. If we arbitrarily assigned 1 of the 23 patients with a positive antibody test to the group with negative antibody tests, then the odds ratio for those with diffuse-type cancer would be 6.0.
Thirty-one of the patients with gastric carcinoma also had peptic ulcer, cardiovascular disease, or some other type of cancer, as documented by hospital records. If these patients had been excluded from the study (as were potential control subjects with these diseases), 78 patients would have remained in the study. Ninety-six percent of these 78 patients and 74 percent of the controls had a positive H. pylori antibody test. The odds ratio of gastric carcinoma was 9.5 (95 percent confidence interval, 2.2 to 40.8) in this group of subjects.
When the patients with cancer and positive antibody tests were separated into tertile groupings, according to the distribution of antibody levels among the control subjects, there was a linear trend in their odds ratios (Table 3Table 3
Odds Ratios for Gastric Carcinoma, According to H. pylori Test Results and Antibody Levels.). Thus, as the level of H. pylori antibody increased, there was a progressive increase in the risk of stomach cancer.The average (±SD) time from phlebotomy to diagnosis was 13±5 years for the 109 patients with histologically confirmed cases of gastric carcinoma. We examined the association of antibody positivity and cancer in relation to the interval from phlebotomy to diagnosis (Table 4Table 4
Odds Ratios for the Association of Gastric Carcinoma with H. pylori Seropositivity, According to the Time from Phlebotomy to Diagnosis.). Patients whose disease was diagnosed 10 to 14 years or 15 or more years after phlebotomy had a significantly increased risk of gastric carcinoma. When both groups were combined, their odds ratio was 10.5 (95 percent confidence interval, 2.5 to 44.8).Next, the participants were separated into two birth-year cohorts, as shown in Table 5Table 5
Odds Ratios for the Association of Gastric Carcinoma with H. pylori Seropositivity, According to Birth-Year Cohort.. Among the control subjects, the frequency of a positive H. pylori antibody test decreased from 82 percent in those born from 1900 to 1909 to 72 percent in those born from 1910 to 1919. As a result, the odds ratio for gastric carcinoma was higher in the younger cohort.The distribution of the cases of stomach cancer according to the stage of disease at the time of diagnosis was as follows: 20 percent were classified as stage 1 to 2, 39 percent as stage 3, and 40 percent as stage 4; the stage was unknown in 1 percent of the cases. The odds ratios for gastric carcinoma were similar according to the stage of disease: 6.0 for stage 1 to 2, 7.0 for stage 3, and 5.5 for stage 4.
The cancers were located in the antrum or body of the stomach in 104 patients and in the cardia in 5 patients. Although the number of cases of cancer of the cardia was small, only 2 of the 5 were antibody-positive, as compared with 101 of the 104 cases of noncardia cancer, a difference that was statistically significant (P = 0.0009 by Fisher's exact test). When the 5 cases of cancer of the cardia were excluded, the odds ratio associated with positive antibody tests for the remaining 104 noncardia cases was 12.0 (95 percent confidence interval, 2.8 to 50.8).
Discussion
This study used a nested case–control design to analyze prospective data. Both the patients and the control subjects were from a single cohort of men. The appropriateness of the selection of controls is evidenced by their similarity to the patients in regard to factors that were unrelated to the risk of gastric carcinoma, such as marital status, body-mass index, diastolic blood pressure, and serum cholesterol levels.
Potential control subjects who had peptic ulcer disease were excluded from the study. As a result, the odds ratio for H. pylori infection may have been overestimated. However, just 13 percent of the subjects in the control pool had gastric or duodenal ulcer. If they had been included in the study, then about 13 percent, or 14, of the 109 controls would have had peptic ulcer. If all 14 had had a positive test for H. pylori antibody, then 86 instead of 83 controls would have had positive results, but the association between H. pylori positivity and gastric carcinoma would have remained significant. The exclusion of subjects with cardiovascular disease or other types of cancer from the control group also did not affect the odds ratios observed in this study.
Because the serum samples had been stored for more than 20 years, some of the specimens had been used for other studies over the years. Forty-seven of the serum specimens from men with gastric carcinoma had never been thawed before the study began, 27 had been thawed once, and 35 had been thawed at least twice. The respective numbers for the control subjects were 51, 54, and 4. Analysis of the matched patients and control subjects according to the frequency of thawing indicated that thawing did not affect the results in this study. We have previously reported that multiple cycles of freezing and thawing do not affect the results of H. pylori serologic determinations.37
There is strong evidence that H. pylori infection is associated with the subsequent development of gastric carcinoma. Ninety-four percent of the patients with gastric carcinoma had H. pylori— specific IgG antibody present in serum obtained an average of 13 years before diagnosis. If data for patients with cancers originating in the cardia were excluded, then 97 percent of the remaining patients had a positive H. pylori antibody test. There was no indication that the strength of the association waned as the interval between the collection of the serum specimen and the diagnosis lengthened. The positive association was still significant for the 43 patients whose cancer was diagnosed 15 or more years after phlebotomy.
In this study population, the intestinal type of gastric carcinoma was diagnosed more commonly than the diffuse type,28 but the association with H. pylori was present for both types. A recent serologic study reported similar results.22 Another study reported that H. pylori infection was detected more frequently with the intestinal type of gastric carcinoma than with the diffuse type, but the investigation was based on the identification of the organism in gastric-tissue specimens at the time of the diagnosis.38 Because of the difficulty in culturing and visualizing the bacteria in tissue, serologic analysis may be the best diagnostic technique since it can be considered to be an assay of the entire stomach.11 Serologic assays for specific IgG antibodies have been documented to be accurate for the diagnosis of H. pylori infection.30 , 33 , 39
The increasing association of cancer with increased levels of specific IgG antibodies is of interest. H. pylori infection is closely associated with active gastric inflammation,8 11 and in vitro studies indicate that soluble H. pylori products activate macrophages.40 The height of the IgG immune response to infection may be related to the extent of gastric inflammation.41 Chronic inflammation may lead to mutagenesis42 and thus to cancer. This is analogous to the association between the severity of inflammation in ulcerative colitis and the risk of colorectal carcinoma.43
The association with gastric carcinoma was greater in the younger cohort of subjects than the older cohort because of the decrease in the frequency of a positive antibody test among the younger control subjects. This decrease in seropositivity could be related to the decline in the incidence of gastric carcinoma in this population since 1960.1 , 44
Although the incidence of adenocarcinoma of the cardia is increasing in the United States,45 in our study only five of the Japanese American men in Hawaii had such tumors. Nevertheless, H. pylori infection was diagnosed significantly less often in men with cancer of the cardia than in those with cancer of the body of the stomach or antrum, confirming studies in which specimens were obtained at the time of diagnosis.20 , 46 Cancers arising in the cardia more closely resemble esophageal adenocarcinomas than other gastric adenocarcinomas in their epidemiologic and pathologic features.45 Consequently, it is not surprising that the H. pylori antibody status may differ between these types of gastric carcinoma.
Several lines of evidence indicate that chronic diffuse superficial gastritis is caused by H.pylori.11 Voluntary ingestion of H. pylori has led to gastritis on two occasions.6 , 47 Antimicrobial therapy that eliminated the infection also cleared the gastritis, but with the recurrence of infection, gastritis recurred.48 Experimental challenge with H. pylori has also led to the development of chronic gastritis in infected animals.49 That this gastritis may progress to chronic atrophic gastritis involving the antrum (type B) has been suggested.13 , 14 Earlier reports have shown that chronic atrophic gastritis is a precursor lesion of gastric carcinoma.15 17 Thus, it is biologically plausible that H. pylori may be a cause of chronic atrophic gastritis that predisposes patients to gastric carcinoma.
In spite of the evidence that an H. pylori infection commonly precedes the diagnosis of gastric carcinoma, we found that 76 percent of the population-based control subjects in our study were also infected with these bacteria. Thus far, only 2.3 percent of the 5908 subjects have been found to have gastric carcinoma. Of the 1540 deaths that have occurred in this cohort, 6.0 percent were due to gastric carcinoma. Consequently, it appears that most of the H. pylori—infected subjects will not have gastric carcinoma. Adult populations in a number of developing countries also have a high prevalence (75 to 90 percent) of H. pylori infection,50 , 51 but gastric carcinoma will develop in only a relatively small percentage. These data indicate that other factors besides H. pylori have an important role in gastric carcinogenesis. Future studies should be directed at identifying other environmental factors that increase the risk of gastric carcinoma among persons infected with H. pylori.
Supported in part by a grant (R01-CA-33644) from the National Cancer Institute, by the Medical Research Service of the Department of Veterans Affairs, and by the Procter & Gamble Company.
Drs. Blaser and Perez-Perez have a royalty interest in the Pyloristat kit (Whittaker Bioproducts, Inc.).
We are indebted to the Honolulu Heart Program for the use of its data and to the following institutions for their helpful cooperation: Castle Medical Center, Kaiser Medical Center, Pali Momi Medical Center, Queen's Medical Center, St. Francis Hospital, Straub Clinic and Hospital, Tripler Medical Center, Wahiawa General Hospital, and the Hawaii Tumor Registry.
Source Information
From the Japan—Hawaii Cancer Study, Kuakini Medical Center, Honolulu (A.N.,G.N.S., P.-H.C., I.K.);and the Division of Infectious Diseases, Vander bilt University School of Medicine (G.I.P.-P., M.J.B.), and the Veterans Affairs Medical Center (M.J.B.), both in Nashville. Address reprint requests to Dr. Nomura at the Japan–Hawaii Cancer Study, Kuakini Medical Center, 347 N. Kuakini St., Honolulu, HI 96817.
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