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Carcinogenesis Advance Access originally published online on January 7, 2006
Carcinogenesis 2006 27(7):1391-1397; doi:10.1093/carcin/bgi334
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© The Author 2006. Published by Oxford University Press. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

A past history of gastric ulcers and Helicobacter pylori infection increase the risk of gastric malignant lymphoma

Takeshi Suzuki 1, 3, Keitaro Matsuo 1, *, Hidemi Ito 1, Kaoru Hirose 1, Kenji Wakai 1, Toshiko Saito 1, Shigeki Sato 3, Yasuo Morishima 2, Shigeo Nakamura 4, Ryuzo Ueda 3 and Kazuo Tajima 1

1 Division of Epidemiology and Prevention, Aichi Cancer Center Research Institute, 1-1 Kanokoden, Chikusa-ku, Nagoya 464-8681, Japan, 2 Department of Hematology and Cell Therapy, Aichi Cancer Center Hospital, Nagoya, Japan, 3 Department of Internal Medicine and Molecular Science, Nagoya City University Graduate School of Medical Science, Nagoya, Japan and 4 Department of Clinical Pathophysiology, Nagoya University Graduate School of Medicine, Nagoya, Japan

* To whom correspondence should be addressed. Tel: +81 52 762 6111; Fax: +81 52 763 5233; Email: kmatsuo{at}aichi-cc.jp


   Abstract
Top
 Abstract
Introduction
 Materials and methods
 Result
 Discussion
 References
 
Helicobacter pylori (H. pylori) is a causative agent for peptic ulcers as well as some types of gastric lymphoma; however, the relationship between a peptic ulcer history in combination with H. pylori infection and the risk of gastric lymphoma has not been fully evaluated. To examine this point, we conducted a case-control study with 645 patients histologically diagnosed as having malignant lymphomas and 3225 non-cancer controls. Plasma H. pylori IgG status was assessed for subgroups for which blood samples were available (116 cases and 114 controls). An association with a history of gastric, but not duodenal ulcers was found for gastric lymphoma [odds ratio (OR) = 5.41, 95% confidence interval (CI): 3.12–9.39]. In the examination according to histological subtype, the OR was high for both gastric mucous-associated lymphoid tissue (MALT) lymphoma (OR = 5.54, 95% CI: 2.56–12.01) and diffuse large B-cell lymphoma (DLBCL) (OR = 7.23, 95% CI: 2.62–19.90). In the analysis of H. pylori antibody, the risk of total gastric lymphoma was associated with H. pylori infection (OR = 5.34, 95% CI: 1.42–20.05). A high prevalence of H. pylori infection was also found for both gastric MALT lymphoma (8 out of 10: 80.0%) and DLBCL (8 out of 9: 88.9%). Further, in subgroup analysis of subjects with H. pylori infection, gastric ulcer history, but not duodenal ulcer history was associated with the risk of gastric lymphoma (OR = 4.15, 95% CI: 1.02–16.89). In conclusion, we found a positive association with a past history of gastric ulcer and H. pylori infection for gastric lymphoma, while duodenal ulcer history was no association. These results suggested the risk of gastric lymphoma increased by interaction between H. pylori infection and gastric ulcer history. Further studies are warranted.

Abbreviations: CI, confidence interval; DLBCL, diffuse large B-cell lymphoma; HERPACC, Hospital-based Epidemiologic Research Program at Aichi Cancer Center; MALT, mucous-associated lymphoid tissue; ML, malignant lymphoma; OR, odds ratio


   Introduction
Top
 Abstract
 Introduction
Materials and methods
 Result
 Discussion
 References
 
Malignant lymphoma (ML) is a rapidly increasing malignancy in developed countries, including Japan (1–3) and the risk factors require elucidation. These include several medical conditions featuring chronic local inflammation, especially with extra-nodal ML (2,3). Of note are reports of increased risk of gastric lymphoma with chronic infection with Helicobacter pylori (H. pylori) in the stomach (4,5).

Infection with H. pylori has in fact been shown to have a pivotal role in gastric lymphoma development, particularly of the mucous-associated lymphoid tissue (MALT) type (4), a prospective study demonstrating 6-fold increase with H. pylori seropositivity (5). Although H. pylori is also recognized to play an important role in formation of peptic ulcers (6), little is known about interactions between these two and gastric lymphoma. One epidemiological study conducted in Italy suggested that a peptic ulcer history is a risk factor for gastric MALT lymphoma (7), but the situation was less clear regarding the diffuse large B-cell lymphoma (DLBCL). In addition, the study was limited in that the H. pylori status was not examined.

To evaluate associations between ML risk and peptic ulcer history along with H. pylori infection status, we conducted the present case-control study with patients from a single institution in Japan.


   Materials and methods
Top
 Abstract
 Introduction
 Materials and methods
Result
 Discussion
 References
 
Study subjects
Cases and controls were selected from a database of the Hospital-based Epidemiologic Research Program at Aichi Cancer Center (HERPACC) conducted at Aichi Cancer Center Hospital (ACCH). Details of the HERPACC study have been described elsewhere (8,9). In brief, we have conducted the first version of HERPACC study (HERPACC-I) between January 1988 and December 2000, with information on lifestyle factors collected from all first-visit outpatients, using a self-administered questionnaire checked by a trained interviewer. Following HERPACC-I, the second version of HERPACC (HERPACC-II) was launched in 2001 and is still on-going, asking all first-visit outpatients to provide 7 ml of blood as well as information on lifestyle factors. In both studies, questionnaire data were loaded into the HERPACC database and periodically linked with the hospital cancer registry system to update the data on cancer incidence. In HERPACC case-control studies, subjects having been diagnosed as incident cancer are used as cases and those without cancer are applied as controls. Our previous study showed lifestyle patterns of first visit outpatients to be accordant with those in the general population randomly selected from the Nagoya City (10).

Figure 1 shows subject enrollment in HERPACC-I and -II as well as selection process of current study. In total of 91 870 patients (between January 1988 and December 2000) and 28 068 patients (between January 2001 and December 2004) visited ACCH as first-visit outpatients. Among them, 8228 and 5637 patients, respectively, were not enrolled due to refusal, age ineligibility (younger than 18 years), interviewers' absence, or other miscellaneous reasons. The questionnaire was ultimately administered to 83 642 and 22 431 patients, respectively. Finally, 82 552 (98.7%) and 22 249 (98.7%) subjects completed the questionnaire adequately and enrolled in HERPACC-I and -II study, respectively.


Figure 1
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  		Fig. 1. Overview of subjects enrollment and selection in this study.

 
Among them, 645 cases (452 from HERPACC-I and 193 from HERPACC-II) that were aged 18–79 years with having no prior history of cancer and histopathologically diagnosed as having ML were eligible for the analysis. We randomly selected five controls for each case from among the 79 090 individuals who diagnosed as cancer-free and have no prior history of cancer, with matching for age and sex. Eventually, 3225 controls (HERPACC-I 2260, HERPACC-II 965) were included in data set 1.

To analyze H. pylori status, we selected cases and controls from HERPACC-II study. Blood samples were available for 116 out of 193 ML patients. We attempted to select one controls for each case from among the 965 controls population randomly, with matching for age and sex, but 2 of 116 controls had no blood sample (data set 2).

Subjects in this study provided written informed consent for participation in HERPACC study. This study was approved by Institutional Ethical Committee at Aichi Cancer Center.

Past history of peptic ulcer and other exposure data
The HERPACC questionnaire included items on demographic characteristics, family history, height and weight, exercise, smoking and drinking habits, and consumption of foods as well as past history. Past history, including gastric ulcer and duodenal ulcer, was obtained from the baseline self-administered questionnaire, with simple yes or no answers. We also obtained information about smoking and drinking habits and body mass index (BMI). BMI at baseline was calculated from reported height and weight: BMI = (weight in kg)/(height in m)2.

H. pylori infection
An H. pylori IgG antibody test, the High-Molecular weight Campylobacter- Associated-Protein-Japan (HM-CAP-J) ELISA (‘Detaminor H. pylori antibody’, Enteric Products Inc., Westbury, NY), which has been established as routine measurement of the IgG antibody in Japan, was used for the identification of H. pylori infected participants using plasma samples. HM-CAP-J provided 95.5% sensitivity and 81.9% specificity with 92.3% accuracy in Japan (11). A value of 2.3 or over was regarded as positive for H. pylori infection.

Statistical analyses
The effect of past history of peptic ulcer was assessed in terms of the odds ratios (ORs) and 95% confidence interval (CIs) calculated with conditional logistic regression model using data set 1. For the subgroup analysis for H. pylori infection, unconditional logistic regression was applied to avoid loss of cases due to lack of matched control using data set 2. All ORs and 95% CIs were adjusted for age, sex, smoking status (never smokers, former smokers or current smokers who daily consumed <20, 20–39 or ≥40 cigarettes), drinking status [never drinkers, former drinkers, or current drinkers who daily consumed <1.0, 1.0–1.9 or ≥2.0 Japanese drinks (one Japanese drink is equivalent to 23g of ethanol)], BMI (<20.0, 20.0–24.9 or ≥25.0 kg/m2) and referral pattern to our hospital (one's own accord, family-recommendation, referral from other clinics, secondary screening after primary screening, or others). Former smokers and drinkers were defined as persons who had quit smoking or drinking at least 1 year previously. All P-values were two-sided, and all the analyses were performed using Stata version 8 (Stata, College Station, TX).


   Result
Top
 Abstract
 Introduction
 Materials and methods
 Result
Discussion
 References
 
Data from 645 ML cases and 3225 controls were available for analysis of peptic ulcer history and ML risk. Among 645 cases with a confirmed histological diagnosis of ML, 48 (7.4%) were diagnosed as having Hodgkin's lymphomas (HL), 235 (36.4%) with DLBCL, 114 (17.7%) with follicular lymphomas, 96 (14.9%) with MALT lymphomas, 64 (9.9%) with NK/T-cell lymphomas, and 88 (13.6%) with the other non-Hodgkin's lymphomas (NHLs). Table I shows the distribution of cases and controls by background characteristics; age and sex were exactly matched between cases and controls. Compared with the control group, the proportion of never drinkers in case group was higher and current drinkers who daily consumed less than 1.0 Japanese drinks was lower (P < 0.01). In referral pattern to our hospital, referral from other clinics was higher, and one's own accord and secondary screening after primary screening were lower among case group than control group (P < 0.01). Other characteristics, including smoking status and BMI, were similarly distributed in cases and controls.


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  		Table I. Characteristic of malignant lymphoma cases and controls from data set 1

 
Rate of gastric and duodenal ulcer history in control group was 9.6% (308/3225) and 6.9% (222/3225), respectively. Table II shows ORs and 95%CIs associated with gastric and duodenal ulcer history for ML subtypes. Gastric ulcer history was significantly associated with the risk of all lymphoma and NHL, but no association was found for HL. An association with gastric ulcer history was observed for gastric lymphoma (OR = 5.41, 95% CI: 3.12–9.39), while no association was found for nodal lymphoma and non-gastric lymphoma in extranodal lymphoma. In analysis of histological subtype of gastric lymphoma, the ORs for gastric ulcer history were significantly elevated for both gastric MALT lymphomas (OR = 5.54, 95% CI: 2.56–12.01) and DLBCL (OR = 7.23, 95% CI: 2.62–19.90), but no association was found for other gastric lymphoma. A duodenal ulcer history showed no consistent link among all subtypes of ML.


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  		Table II. Adjusted ORs relating associations with peptic ulcer history for risk of malignant lymphoma subtypes

 
To evaluate the risk of gastric lymphoma with reference to the H. pylori status, we examined the cases with blood samples (n = 116) and matched controls (n = 114) within the HERPACC-II study. Table III presents the prevalence of H. pylori according to basic characteristics among cases and controls. Anti-H. pylori antibodies were detected in 59% of all lymphoma cases and 54% of the controls. In control group, H. pylori prevalence differed by sex and age, with male and old age subjects having higher prevalence as compared with female and young age categories. No association with H. pylori prevalence was observed for smoking and drinking status. High prevalence of H. pylori was observed among controls with past history of gastric or duodenal ulcer.


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  		Table III. H. pylori prevalence by different characteristics among case and control subjects from data set 2

 
H. pylori infection was not associated with an increased risk of all lymphoma (Table IV). Among several histological subtypes of lymphoma, H. pylori infection showed a significantly increased risk of MALT, but not of other histological subtypes. In analyses of lymphoma by primary site, a significantly increased risk of gastric lymphoma with H. pylori infection was observed (19 out of 22: 86.4%, OR = 5.34, 95% CI: 1.42–20.05). Although not significant, H. pylori infection showed increased risk of each subtype of gastric lymphoma. Higher prevalence of H. pylori was noted for both gastric MALT lymphoma (8 out of 10: 80.0%) and DLBCL (8 out of 9: 88.9%) compared with control group. No association was found for nodal lymphoma and extranodal non-gastric lymphoma. To further examine an impact of peptic ulcer history, subgroup analysis for those with anti-H. pylori positive subjects were conducted (Table V). Adjusted OR indicated that history of gastric ulcer was associated with significantly increased risk of gastric lymphoma (OR = 4.15, 95% CI: 1.02–16.89), while such association was not observed with duodenal ulcer.


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  		Table IV. Distribution of H. pylori antibody prevalence and ORs among malignant lymphoma subtypes

 

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  		Table V. ORs relating associations with peptic ulcer history for risk of gastric lymphoma among H. pylori infection subjects

 

   Discussion
Top
 Abstract
 Introduction
 Materials and methods
 Result
 Discussion
References
 
In this study, we found that a history of gastric ulcer was associated with the risk of gastric DLBCL as well as MALT lymphoma, but not with a history of duodenal ulcer. An increased risk was observed with H. pylori infection for total gastric lymphoma as well as each subtype of gastric lymphoma. Moreover, a history of gastric ulcer was significantly associated with increased risk of gastric lymphoma among those with H. pylori.

Concerning a past history of peptic ulcers, only few epidemiological studies have been published (7,12,13). Our finding that a past history of gastric ulcer increased the risk of gastric lymphoma development is compatible with results published by Vineis et al. (7). Here we detected an association with a past history of gastric ulcer for both gastric MALT lymphomas, in line with an earlier report (7), and also gastric DLBCL, for the first time to our knowledge. In contrast with a history of gastric ulcer, a past history of duodenal ulcer was not associated with an elevated risk of gastric lymphoma. Similar discrepancy between two subtypes of peptic ulcer is recognized for the risk of gastric adenocarcinoma (14).

Clinical observations indicate that the pattern and distribution of gastritis and H. pylori infection correlate with the risk of gastric or duodenal ulcers, gastric adenocarcinoma or lymphoma (15). H. pylori is usually acquired in childhood (16,17) and clinical course of H. pylori related diseases are highly variable and depend on bacterial and host factors (18). Patients with antral-predominant gastritis are predisposed to duodenal ulcers (19), and suggested mechanism behind this phenomenon is gastrin-mediated acid stimulation by H. pylori (20). On the other hand, patients with gastritis in the corpus are predisposed to gastric ulcer, gastric cancer (21–23) and lymphoma (24) but not to duodenal ulcer, suggesting that potential role of H. pylori in corpus dominant gastritis mainly owes to inflammation rather than acid secretion. Considering these findings in mind, our observation might indicate a common carcinogenic story between gastric lymphoma and carcinoma.

In this study, we observed increased risk of gastric lymphoma for those with H. pylori positive subjects (OR = 5.34). This was consistent with results in a former prospective study (5). We also observed high prevalence of anti-H. pylori antibody among two main subtypes of gastric lymphoma, gastric MALT lymphoma and DLBCL. This is consistent with the literature suggesting that H. pylori is a potential causative factor for gastric DLBCL as well as gastric MALT lymphoma (25,26).

Gastric and duodenal ulcers are commonly predisposed with H. pylori infection (6), and such association was consistently observed in our control group in data set 2. Taken this fact in consideration along with our observations where a history of gastric ulcer as well as H. pylori infection showed significant increased risk of gastric lymphoma, it is interesting to see whether there is an interaction between a history of gastric ulcer and H. pylori infection. Results in an analysis limited to H. pylori positive subjects indicated that gastric ulcer might have some additional role in gastric lymphomagenesis. Further evaluation was clearly warranted.

We found that current low amount drinkers in whole lymphoma cases were significantly less frequent than in controls. Recent pooled analysis suggested that current drinkers might have a lower risk of NHL than non- or former drinkers; however, risk did not decrease in a dose-dependent manner (27). These finding is consistent with our result in which dose of alcohol did not show clear association. The potential protective effects of light to moderate alcohol use is suggested to be its immunomodulatory effects, however, a background mechanism remains to be elucidated (28).

Several methodological limitations in this study must be considered. First, in our study a self-administered questionnaire was performed to obtain information on a past history of peptic ulcers. It has been suggested that the association with gastric ulcer for risk of gastric lymphoma may be due to detection bias. This is an unlikely explanation for finding of this study, because duodenal ulcer was not associated with an increased risk of gastric lymphoma. Further, past history of other gastrointestinal diseases (e.g. gastritis and other benign gastric diseases) were also not associated with an increased risk of gastric lymphoma in the HERPACC-I study (data not shown). Secondly, a substantial misclassification in self-report of gastric and duodenal ulcer is possible. However, the associations found in this study could not be attributed to such misclassification, because it is guessed that any possible misclassification of gastric and duodenal ulcers is most likely non-differential in cases and controls groups. In addition, gastric and duodenal ulcer ratio among controls in this study was 1.38 (308/222), this figure is approximately in agreement with that of prospective study conducted in Japan (23). Thirdly, because ulcerated lesion on endoscopic appearance is reported in 30–50% of gastric lymphoma (29,30), diagnosis bias is need to consider. In our study, the information on data of gastric ulcer diagnosed was unavailable unfortunately, however, each patient was asked about lifestyles, including past history of peptic ulcer when healthy or prior to assessment of their symptoms and all information was collected before clinical diagnoses were made. Additionally, it is thought that there were few patients who were referred to our hospital being diagnosed as gastric ulcer though true disease was gastric lymphoma, because our hospital is cancer center, and differs from a general hospital. Fourthly, the estimates of association with H. pylori infection for the risk of gastric lymphoma subtypes were unstable, because a small number of gastric MALT lymphoma and DLBCL had an available blood sample in this study. To enhance the consistency of association with H. pylori infection for the risk of both subtypes of gastric lymphoma, future larger scale studies were need. Fifthly, H. pylori detected rate of control group is smaller than most previous studies from Japan (31), but the ELISA kits used in this study modified their kits to better detect H. pylori strains and high sensitivity was reported among Japanese population (11). In addition, because higher positive rate of H. pylori antibody was found among control group with history of gastric or duodenal ulcer, comparing with non-peptic ulcer history control group, we consider that the reliability of this device was established.

Lastly, internal validity of this hospital-based study is a potential threaten for causal inference in this population. We applied non-cancer patients at ACCH as controls because it is reasonable to assume our cases arise within this population base. Notable point of our control population is its similarity to general population in terms of exposure of interest, here past history. We have compared lifestyle characteristics between outpatients in ACCH and the 1231 individuals randomly selected from the general population, and confirmed that they are not substantially different (10). Medical background of controls is another potential source of bias; however, our previous study focusing on females demonstrated a limited impact (32). With men, the circumstance is similar. This situation is very different from that in other developed countries, where people visit local general clinics first, and are then referred to hospitals which function as secondary and/or specific facilities for further medical treatment. Further, to best take the difference between cases and controls into consideration, we adjusted for referral pattern to our hospital. We therefore conclude that it is feasible to use non-cancer outpatients as referents in HERPACC type epidemiological studies. Another limitation is possible misclassification of past history of peptic ulcers because self-report past history was applied in this study. This could be potential source of bias, therefore, interpretation needs caution. Limitations of this study may be cleared in the future prospective cohort studies with detailed examination of medical history.

In conclusion, the present study showed a significantly increased risk of gastric MALT lymphoma and DLBCL development with a past history of gastric ulcers, but not with duodenal ulcer. Interaction between gastric ulcer history and H. pylori infection for the risk of gastric lymphoma was suggested, however, it remains to be examined in future studies.


   Acknowledgments
 
The study was supported by a Grant-in Aid for Scientific Research from the Ministry of Education, Science, Sports, Culture and Technology of Japan and a Grant-in-Aid for the Third Term Comprehensive 10-Year-Strategy for Cancer Control from the Ministry of Health, Labour and Welfare of Japan.

Conflict of Interest Statement: None declared.


   References
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 Abstract
 Introduction
 Materials and methods
 Result
 Discussion
 References
 

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Received November 11, 2005; revised December 20, 2005; accepted December 24, 2005.


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