Original Article
Helicobacter pylori Infection and Gastric Lymphoma
N Engl J Med 1994; 330:1267-1271May 5, 1994
- Abstract
Background
Helicobacter pylori infection is a risk factor for gastric adenocarcinoma. We examined whether this infection is also a risk factor for primary gastric non-Hodgkin's lymphoma.
Methods
This nested case-control study involved two large cohorts (230,593 participants). Serum had been collected from cohort members and stored, and all subjects were followed for cancer. Thirty-three patients with gastric non-Hodgkin's lymphoma were identified, and each was matched to four controls according to cohort, age, sex, and date of serum collection. For comparison, 31 patients with nongastric non-Hodgkin's lymphoma from one of the cohorts were evaluated, each of whom had been previously matched to 2 controls. Pathological reports and specimens were reviewed to confirm the histologic type of the tumor. Serum samples from all subjects were tested for H. pylori IgG by an enzyme-linked immunosorbent assay.
Results
Thirty-three cases of gastric non-Hodgkin's lymphoma occurred a median of 14 years after serum collection. Patients with gastric lymphoma were significantly more likely than matched controls to have evidence of previous H. pylori infection (matched odds ratio, 6.3; 95 percent confidence interval, 2.0 to 19.9). The results were similar in both cohorts. Among the 31 patients with nongastric lymphoma, a median of six years had elapsed between serum collection and the development of disease. No association was found between nongastric non-Hodgkin's lymphoma and previous H. pylori infection (matched odds ratio, 1.2; 95 percent confidence interval, 0.5 to 3.0).
Conclusions
Non-Hodgkin's lymphoma affecting the stomach, but not other sites, is associated with previous H. pylori infection. A causative role for the organism is plausible, but remains unproved.
Media in This Article
Table 1
Characteristics of the Patients with Gastric or Nongastric Non-Hodgkin's Lymphoma.Table 2
Odds Ratios and 95 Percent Confidence Intervals for the Association of H. pylori Infection with Gastric Non-Hodgkin's Lymphoma and Nongastric Non-Hodgkin's Lymphoma.Article Activity
- Article
Primary non-Hodgkin's lymphoma of the stomach is an uncommon cancer, accounting for only 10 percent of lymphomas and 3 percent of gastric neoplasms1. According to U.S. tumor-registry data from 1985, there were only 7.1 cases of gastric non-Hodgkin's lymphoma per million population per year2. Gastric non-Hodgkin's lymphoma remains, however, the most common extranodal form of this lymphoma, accounting for 20 percent of primary extranodal disease3. The majority of the tumors are diffuse, large-cell lymphomas when classified according to the cytomorphologic criteria of the working formulation4. Immunohistochemical studies have shown most tumors to be of B-cell lineage5-7.
Circumstantial evidence suggests that infection with a bacterium, Helicobacter pylori, may increase the risk of gastric non-Hodgkin's lymphoma. Sixty percent of gastric non-Hodgkin's lymphomas evolve from chronic gastritis, a lesion usually caused by H. pylori8. In a study of adenocarcinoma, an unexpected link between H. pylori infection and the subsequent development of gastric non-Hodgkin's lymphoma was identified, although this association was not statistically significant9. Furthermore, a region in Europe with a high incidence of gastric non-Hodgkin's lymphoma had a higher rate of H. pylori infection than a region with a low incidence10. A possible association between H. pylori and non-Hodgkin's lymphoma was also seen in a large multiregion study in China, although the primary sites of the lymphomas were not identified11. Two studies have demonstrated high rates of H. pylori infection in patients with gastric non-Hodgkin's lymphoma12,13; one linked infection to a specific type of tumor derived from mucosa-associated lymphoid tissue (MALT lymphomas)13.
To address the association of H. pylori with primary gastric non-Hodgkin's lymphoma, we conducted a nested case-control study within two very large cohorts using a serologic marker for infection with the bacterium. Because we hypothesized that any association of H. pylori with lymphoma should be specific to gastric sites, we also evaluated the association of H. pylori with nongastric lymphomas.
Methods
Subjects
A case of gastric non-Hodgkin's lymphoma was defined as lymphoma restricted to the stomach and adjacent lymph nodes. Patients with gastric non-Hodgkin's lymphoma were identified in two large cohorts. The Kaiser-Orentreich cohort consisted of 128,992 members of a health maintenance organization (the Kaiser Permanente Medical Group) who had provided serum between 1964 and 1969 as part of a routine multiphasic health evaluation. Since 1980, these serum samples have been catalogued and maintained at -40 °C by the Orentreich Foundation (Cold Spring, N.Y.)14. Members of the cohort in whom gastric non-Hodgkin's lymphoma subsequently developed were identified by linkage with computerized tumor-registry and hospitalization data. The Janus cohort included 170,000 persons who donated blood and participated in various health screening programs in Norway from 1973 to 199115,16; of these, 101,601 were eligible for selection as case patients or controls, since both cancer-registry data and serum samples were available. Members of the cohort in whom gastric non-Hodgkin's lymphoma developed through 1990 were identified by linkage with the Norwegian Cancer Registry.
Nineteen patients with gastric non-Hodgkin's lymphoma were identified in the Kaiser-Orentreich cohort and 13 in the Janus cohort. The medical records of these patients were reviewed, and pathological specimens were reexamined by pathologists at Stanford University to confirm the histologic type of the tumor. Lesions were classified according to the cytomorphologic criteria of the working formulation4. Low-grade MALT lymphomas were defined according to the criteria of Isaacson17. In cases in which there were differences in the histologic interpretation between the original and reviewing pathologists, immunohistochemical studies were performed18,19.
Patients identified as having gastric non-Hodgkin's lymphoma were matched according to cohort, date of birth (in the Kaiser-Orentreich cohort the controls were obtained from the same five-year birth cohort; in the Janus cohort the controls were matched for the date of birth plus or minus six months), sex, and date and site of serum collection to four randomly chosen control subjects in whom cancer had not developed as of the year gastric non-Hodgkin's lymphoma was diagnosed in the case patient. Case patients from the Kaiser-Orentreich cohort were also matched according to racial or ethnic group. There are no corresponding data on the predominantly white Janus cohort.
To identify a group of patients with nongastric non-Hodgkin's lymphoma for comparative purposes, serum samples were obtained from a previous nested case-control study of this lymphoma in the Kaiser-Orentreich cohort20. In this earlier study, 44 patients with non-Hodgkin's lymphoma had each been matched to 2 controls as described above. Two of these patients had gastric lymphoma and were also identified by our computerized analysis of the Kaiser-Orentreich cohort. All 12 controls for these 2 patients (4 each from the recent linkage analysis and 2 each from the previous analysis) were included in the analysis. On review of the histopathological information, an additional patient with gastric lymphoma was identified who was not identified by computerized analysis of the Kaiser-Orentreich cohort. This patient and two matched controls were also included in the matched analysis of gastric non-Hodgkin's lymphoma.
Of the 41 remaining patients who were identified in the earlier study of non-Hodgkin's lymphoma, 6 had no pathological specimens available for review and in 3 others the diagnosis of lymphoma could not be confirmed. These nine patients were excluded. An additional patient was found to have widely disseminated disease involving the stomach. Because the primary site of cancer could not be confirmed, this patient was also excluded. One patient had only one control because there were no serum samples remaining for the other control. Thus, a total of 31 patients with nongastric non-Hodgkin's lymphoma and 61 matched controls were evaluated. The histologic analyses of lymphoma had previously been confirmed by pathologists at Harvard University, Stanford University, or both. Seventeen were primary tumors of the lymph nodes. The remaining tumors were widely disseminated without gastric involvement (three) or were primary cancers of the mesentery, omentum, or intestine (four); nasopharynx or thyroid (two each); or larynx, parotid gland, or retroperitoneum (one each).
Serologic Assays
All serum samples had been maintained at -20 °C or lower14,15. The aliquots were coded and sent to Stanford University, where they were tested by workers who were unaware of the case or control status of the specimens. Titers of anti-H. pylori IgG were assayed by a serum enzyme-linked immunosorbent assay (ELISA) as previously described9. The antigens included the high-molecular-weight, cell-associated proteins of three H. pylori strains. Dominant bands elicited by sodium dodecyl sulfate-polyacrylamide-gel electrophoresis included proteins at 66, 57, and 29 kd. Other bands occurred at 83, 53, and 26 kd. These antigens, which include the urease subunits and the cytotoxin, are similar to those described for other H. pylori ELISAs21. Any subject with a serum titer higher than 3 SD above the mean of 15 negative control standards was considered to have been infected with H. pylori at the time of serum collection. This assay had a sensitivity of 96 percent and a specificity of 76 percent for active gastric infection, on the basis of an analysis of 124 biopsy-confirmed serum samples from the United States, Latin America, and Asia (75 positive and 49 negative). Because biopsy specimens may not include tissue from an active site of a patchy infection, the calculated specificity is most likely an underestimate of the true specificity22. Serologic tests accurately reflect the presence or absence of active H. pylori infection, except in the very elderly, in whom titers may be falsely negative23,24. A positive titer therefore strongly supports the presence of an ongoing, rather than past, infection.
Statistical Analysis
Data were entered and analyzed with EpiInfo (Centers for Disease Control and Prevention, Atlanta) and Egret (Statistics and Epidemiology Research Corporation, Seattle) computer programs. The relative risk of H. pylori infection and subsequent lymphoma was determined by the odds ratio with conditional logistic regression25. Statistical tests of the regression coefficients were based on the chi-square approximation for the likelihood-ratio statistic, with confidence intervals estimated by Wald's test. Combined effects of risk factors on the development of gastric lymphoma were explored with statistical tests for interaction. The median values of continuous variables were compared with the Wilcoxon rank-sum test26. Attributable risk was estimated as previously described27.
Results
There were a total of 33 patients with gastric non-Hodgkin's lymphoma (20 from the Kaiser-Orentreich cohort and 13 from the Janus cohort) with 134 matched controls and a total of 31 patients with nongastric non-Hodgkin's lymphoma with 61 matched controls (Table 1Table 1
Characteristics of the Patients with Gastric or Nongastric Non-Hodgkin's Lymphoma.). Patients with gastric lymphoma from the Kaiser-Orentreich cohort were significantly older at the time of diagnosis than those from the Janus cohort and were somewhat more likely to be female. These patients were also older at diagnosis than the patients with nongastric lymphoma from the Kaiser-Orentreich cohort. The median interval from serum donation to the diagnosis of cancer was similar in the two groups of patients with gastric lymphoma but was significantly shorter in the group with nongastric lymphoma.Patients with gastric non-Hodgkin's lymphoma were substantially more likely to have had immunologic evidence of prior H. pylori infection than were matched controls (odds ratio, 6.3; 95 percent confidence interval, 2.0 to 19.9) (Table 2Table 2
Odds Ratios and 95 Percent Confidence Intervals for the Association of H. pylori Infection with Gastric Non-Hodgkin's Lymphoma and Nongastric Non-Hodgkin's Lymphoma.). Sixty-six percent of gastric lymphomas could be attributed to H. pylori infection in this population. No association was found between nongastric non-Hodgkin's lymphoma and prior H. pylori infection (odds ratio, 1.2; 95 percent confidence interval, 0.5 to 3.0) (Table 2).There was one mismatch between patients and controls with respect to racial or ethnic classification; one Hispanic patient was matched to four Asian controls. This case-control group was completely discordant: the patient had evidence of H. pylori antibodies, but all four controls did not. When this group was excluded from the analysis, evidence of prior H. pylori infection remained linked to gastric non-Hodgkin's lymphoma (odds ratio, 5.5; 95 percent confidence interval, 1.8 to 17.4).
The analysis of the group of patients with gastric lymphoma was also stratified according to cohort, sex, age at diagnosis, and the interval between serum collection and diagnosis. The odds ratio for prior H. pylori infection was elevated in all subgroups (Table 3Table 3
Adjusted Odds Ratio and 95 Percent Confidence Intervals for the Association of Gastric Non-Hodgkin's Lymphoma with H. pylori Infection.). There were no statistically significant differences among these subgroups.Three patients with gastric non-Hodgkin's lymphoma were identified as having low-grade MALT lymphoma. This number was too small to assess reliably; 2 of the 3 patients were infected with H. pylori, as compared with 5 of 12 controls (odds ratio, 2.8; 95 percent confidence interval, 0.2 to 28.5). Another patient had a small lymphocytic lymphoma with plasmacytoid features that had no other features indicative of a MALT lymphoma; this patient did not have H. pylori antibodies. The tumors in the remaining 29 patients were classified as diffuse large-cell lymphomas according to the criteria of the working formulation4. In this subgroup, the odds ratio for prior H. pylori infection was 7.4 (95 percent confidence interval, 2.1 to 27.0).
Discussion
In this study, patients with gastric non-Hodgkin's lymphoma were substantially more likely than matched controls to have immunologic evidence of prior infection with H. pylori. This association between cancer and infection was found in two large cohorts from different continents. The observed odds ratio probably underestimated the true risk, since a misclassification bias attributable to an imperfect serologic assay would tend to minimize true associations28. Had the ELISA for H. pylori been 100 percent sensitive and 100 percent specific, the odds ratio of lymphoma would have been approximately 25 percent higher.
Studies of Epstein-Barr virus suggest that an aberrant antibody response to infection may occur years before a tumor appears. Such a response is unlikely to explain our findings20. There was no link between nongastric lymphoma and previous infection. Therefore, the finding of an increased risk is not due solely to an abnormal immune response in patients with lymphoma before the disease is diagnosed. Infection with H. pylori was specifically linked to lymphomas of gastric tissue, suggesting that any deleterious effect of this infection is exerted locally.
H. pylori infects approximately half the world's population. Although this infection has been linked to the development of duodenal ulcer, gastric ulcer, hypertrophic gastropathy, and gastric adenocarcinoma, the majority of infected persons remain asymptomatic throughout their lives. Gastric and duodenal ulcers are thought to be caused, at least in part, by H. pylori infection, since the eradication of this microorganism prevents recurrences of these diseases29,30. It remains possible that H. pylori does not cause cancer but merely signals exposure to other risk factors. Since H. pylori infection is associated with lower socioeconomic status, household crowding, and diminished hygiene,31 a different causative factor could be involved rather than the infection itself.
Despite this possibility, we believe that H. pylori is a highly plausible initiator or promoter of gastric lymphoma. Small intestinal lymphomas that develop from immunoproliferative small intestinal disease have previously been linked to bacterial infection32. Other extranodal lymphomas (i.e., thyroid and salivary gland) have been linked to chronic inflammatory processes17. Furthermore, the stomach, unlike the intestine, is not functionally a lymphoid organ33. In infancy and early childhood, the stomach is devoid of lymphocytes and plasma cells. With age, however, chronic inflammation can develop, leading lymphocytes to accumulate in the submucosa and gradually increase their depth of penetration. H. pylori infection causes the vast majority of cases of chronic gastritis34. With the eradication of this microorganism, chronic inflammation decreases and the density of submucosal lymphocytes dramatically declines24. Since most gastric non-Hodgkin's lymphomas arise in areas of chronic inflammation,8 it seems likely that prior H. pylori infection and this lymphoma are linked.
A recent European study provides evidence that H. pylori has a role in causing a subgroup of gastric lymphomas, low-grade MALT lymphomas35. MALT lymphomas are B-cell lymphomas that arise from lymphoid aggregates in the lamina propria. In that study, MALT lymphomas regressed in response to the treatment of H. pylori infection; in five of six patients, the tumors completely disappeared with the eradication of infection. In a separate investigation, B cells from MALT tumors proliferated in response to H. pylori antigens when incubated in the presence of H. pylori-specific T cells36. Although only 20 to 30 percent of gastric lymphomas appear to arise from clinically evident MALT lymphomas, these few cases may represent a model for H. pylori-related antigenic stimulation, lymphoproliferation, and lymphomagenesis37.
In disrupting the normal physiologic and immunologic processes within the stomach, H. pylori establishes an environment in which proliferation of cells and oxidative damage of DNA may occur in both epithelial and hematopoietic cells. This disruption may manifest itself differently in different persons, perhaps accounting for the variation in risk for H. pylori-related diseases. Differences in response may relate to host factors (age at infection or genetic or immunologic factors), variations between strains (cytotoxin production), or dietary or environmental cofactors (nutritional intake or viral exposure). Therefore, attention should be focused on individual differences in the inflammatory response to H. pylori infection and on factors that influence this response.
The incidence of non-Hodgkin's lymphoma is rising in industrialized countries38. The tumor, however, is not a uniform disease with uniform initiating events. This is particularly true of extranodal non-Hodgkin's lymphoma, of which many cases have been linked to localized inflammatory processes. Studies of the epidemiology and risk factors for non-Hodgkin's lymphoma might best address specific types of tumor and disease locations rather than view these lymphomas as a single entity.
Supported in part by an Ortho Pharmaceutical Corporation Young Investigator Award in Infectious Diseases (to Dr. Parsonnet) and by grants (R35CA49761, CA33119, and CA34233) from the National Cancer Institute (to Dr. Friedman, Dr. Gelb, and Dr. Warnke).
We are indebted to Dr. Nancy Mueller of the Harvard School of Public Health for providing serum from the patients with non-Hodgkin's lymphoma and the controls in the previously studied Kaiser-Orentreich cohort; to Marilyn Replogle, Shufang Yang, and Sandra Chen for technical support; and to Nancy P. Durr for her review of the manuscript.
Source Information
From the Departments of Medicine and Health Research and Policy (J.P., L.R.) and the Department of Pathology (A.B.G., R.A.W.), Stanford University School of Medicine, Stanford, Calif.; the Cancer Registry of Norway, Oslo (S.H.); the Janus Committee, Norwegian Cancer Society, Oslo (E.J.); the Orentreich Foundation for the Advancement of Science, Cold Spring, N.Y. (N.O., J.H.V.); and the Division of Research, Kaiser Permanente Medical Care Program, Oakland, Calif. (G.D.F.).
Address reprint requests to Dr. Parsonnet at HRP Bldg., Rm. 225, Stanford University, Stanford, CA 94305.
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