Association of H. pylori infection with gastric carcinoma: A meta analysis

Fu-Bo Xue; Yong-Yong Xu; Yi Wan; Bo-Rong Pan; Jun Ren; Dai-Ming Fan

doi:10.3748/wjg.v7.i6.801

. 2001 Dec 15;7(6):801–804. doi: 10.3748/wjg.v7.i6.801

Association of H. pylori infection with gastric carcinoma: A meta analysis

Fu-Bo Xue ^1,^2,³, Yong-Yong Xu ^1,^2,³, Yi Wan ^1,^2,³, Bo-Rong Pan ^1,^2,³, Jun Ren ^1,^2,³, Dai-Ming Fan ^1,^2,³

PMCID: PMC4695598 PMID: 11854905

Abstract

AIM: To follow the principles of evidence based medicine to reach the integrated results of these studies.

METHODS: Twenty-one papers of case-control studies were selected, including 11 on gastric cancer, 7 on precancerous lesion of stomach and 3 on lymphoma of stomach. Meta analysis was used to sum up the odds ratios (OR) of these studies.

RESULTS: H. pylori vsgastric cancer (intestinal and diffuse type): the odds ratio from the fixed effect model is 3.0016 (95% CI: 2.4197-3.7234, P < 0.001). H. pylori vs precancerous lesion of stomach: a random effect model was used to calculate the summary odds ratio and its value is 2.5635 (95% CI: 1.8477-3.5566, P < 0.01). H. pylori vs lymphoma of stomach: though the quantity of literature is too small to make Meta analysis, the data of these 3 studies show that lymphoma of stomach is highly associated with H. pylori infections.

CONCLUSION: Since it had been revealed that H. pylori infection pre-exists in gastric carcinoma and precancerous lesions, the results of Meta analysis present a strong evidence to support the conclusion that H. pylori infection is a risk factor for gastric carcinoma.

Keywords: Helicobacter pylori, Helicobacter infections, stomach neoplasms/microbiology, evidence-based medicine, meta-analysis

INTRODUCTION

Since H. pylori was founded in 1983, the association of H. pylori with H. pylori related diseases has become the hot spot of gastroenterological studies. Gastric carcinoma is the most important disease among H. pylori related diseases. It is believed that H. pylori is one of the important causes of gastric carcinoma. But there is still lack of the final conclusion and the definite mechanisms of their association.

In China, malignant tumor is the second death cause of men and the third death cause of women according to the investigation of death cause in 29 provinces, municipalities and autonomous regions conducted from 1973 to 1975. The annual average mortality rate of gastric carcinoma is as high as 16 per 10 0 thousand, which is the leading death cause among malignant tumors, and the rates of H. pylori infection are higher than 50 percent in the mainland of China[1]. In the past two decades, Chinese medical researchers and clinical workers have done much a great amount of studies to reveal the relationship and the mechanisms of the association of H. pylori with gastric carcinoma. Most of them agree to the opinion that H. pylori is a risk factor for gastric carcinoma, but a certain number of them hold different points of view[2-19].

Eslick et al[20] have worked out the summary odds ratio of 2.04 of those same studies made in Western countries. In this paper, we reviewed all the literatures of studies in China on the relationship between H. pylori and gastric carcinoma as well as precancerous lesions of stomach published from 1995 in order to reach a summary conclusion using statistical methods.

MATERIALS AND METHODS

Literature

A CBM (Chinese Biomedical Database) search for articles published from 1995 was performed with the MeSH headings “Helicobacter pylori,” “gastric carcinoma (cancer),” “precancerous lesion of stomach” and “lymphoma of stomach.” More than 100 papers were retrieved. Since most of them had no appropriate controls or their data did not meet the requirements of Meta analysis, only 21 papers of case-control studies were selected, including 11 about gastric cancer (Table 1), 7 on precancerous lesions of stomach (Table 2) and 3 on lymphoma of stomach (Table 3).

Table 1.

Eleven case-control studies of H. pylori vs. gastric cancer[21-31]

No.	Cases		Controls		OR	95%CI	χ²	P value
No.	Hp (+)	Hp (-)	Hp (+)	Hp (-)	OR	95%CI	χ²	P value
1	61	13	49	25	2.394	1.110～5.163	4.284	0.038
2	13	3	78	68	3.778	1.033～13.818	3.475	0.062
3	71	21	46	46	3.381	1.791～6.384	13.52	0.000
4	99	23	6	8	5.793	1.841～18.155	8.400	0.004
5	35	16	34	87	5.597	2.746～11.408	22.873	0.000
6	101	35	6236	4628	2.142	1.455～3.151	14.959	0.000
7^*	16	9	32	43	2.389	0.937～6.092	2.618	0.106
8^*	21	19	3	12	4.421	1.080～18.093	3.457	0.063
9^*	55	21	12	10	2.183	0.821～5.805	1.75	0.186
10	90	13	89	50	3.889	1.977～7.653	15.500	0.000
11	60	25	35	50	3.429	1.815～6.475	13.743	0.000
Summary	622	198	6620	5027	3.0016	2.4197～3.7234	99.9483	0.000

Open in a new tab

^*the literatures that did not attain significant results.

Table 2.

Seven case-control studies of H. pylori vs. precancerous lesion of stomach[32-38]

No.	Cases		Controls		OR	95%CI	χ²	P value
No.	Hp (+)	Hp (-)	Hp (+)	Hp (-)	OR	95%CI	χ²	P value
1	344	194	1467	1311	1.585	1.309～1.918	22.089	0.000
2	67	29	175	180	2.376	1.466～3.851	11.955	0.000
3	103	38	26	53	5.525	3.036～10.056	31.988	0.000
4	427	252	992	892	1.524	1.273～1.824	20.736	0.000
5	99	41	12	28	5.634	2.614～12.144	20.128	0.000
6	134	35	272	201	2.829	1.870～4.282	24.490	0.000
7	188	27	332	135	2.831	1.805～4.442	20.836	0.000
Summary	1362	616	3276	2800	2.5635	1.8477～3.5566	31.7540	0.000

Open in a new tab

Table 3.

Three case-control studies of H. pylori vs. lymphoma of stomach[39-41]

No.	Cases		Controls		OR	95%CI	χ²	P value
No.	Hp (+)	Hp (-)	Hp (+)	Hp (-)	OR	95%CI	χ²	P value
1	24	5	13	16	5.908	1.762～19.810	7.465	0.006
2	15	0	36	24	10.811	1.347～86.798	5.692	0.017
3	34	5	31	23	5.045	1.709～14.896	8.176	0.004

Open in a new tab

Data

Eleven case-control studies on the relationship between H. pylori infection and gastric cancer (intestinal and diffuse type) included totally 820 patients and 11-647 controls. Among them, 7 attained significant results, and 4 did not (Table 1).

Seven case-control studies on the relationship between H. pylori infection and precancerous lesions of stomach included totally 1978 patients and 6076 controls. All of them had significant results (Table 2).

Three case-control studies on the relationship between H. pylori infection and lymphoma of the stomach included totally 83 patients and 143 controls. All of them had significant results (Table 3).

Methods

In the statistical analysis, Meta analysis method with fixed effect model and random effect model was used to reach the integrated conclusion[42].

RESULTS

H. pylori infection vs gastric cancer

All 11 odds ratios were statistically homogenous (P > 0.05). Summary odds ratio for gastric cancer related to H. pylori infection was 3.0016 using fixed effect model (95% CI 2.41 97-3.7234, Table 1). Figure 1 shows the summary odds ratio and odds ratios and their 95%CI of 11 case-control studies on the relationship between H. pylori infection and gastric cancer.

Odds ratios and summary odds ratio with 95%CI of 11 case-control studies.

H. pylori infection vs precancerous lesion of stomach

Since 7 odds ratios were not statistically homogenous (P < 0.05), random effect model was used to calculate the summary odds ratio. The summary odds ratio for precancerous lesions of stomach related to H. pylori infection was 2.5635 (95% CI 1.8477-3.5566, Table 2). Figure 2 shows the summary odds ratio and odds ratios and their 95%CI of 7 case-control studies on the relationship between H. pylori and precancerous lesions of the stomach.

Odds ratios and summary odds ratio with 95%CI of 7 case-control studies.

H. pylori vs lymphoma of stomach

Though the quantity of literature is too small to make Meta analysis, the data of these 3 studies show that lymphoma of the stomach was highly associated with H. pylori infections. Figure 3 shows the odds ratios and their 95%CI of 3 case-control studies on the relationship between H. pylori infection and lymphoma of the stomach.

Odds ratios with 95%CI of 3 case-control studies.

DISCUSSION

Since it had been revealed that H. pylori infection pre-exists in gastric carcinoma and precancerous lesions, the result of the Meta analysis present a strong evidence to support the conclusion that H. pylori infection is a risk factor for gastric carcinoma.

The following statements might explain the association of H. pylori infection with gastric carcinoma: ① gastric carcinoma is caused by H. pylori infection; ② H. pylori infection is caused by gastric carcinoma; ③ there are some certain factors for H. pylori infection and gastric carcinoma[9]. As we all know that H. pylori infections also exist in the gastric mucosa of nearly normal persons, it is impossible that H. pylori infection is caused by gastric carcinoma. Numerous studies support the point that H. pylori infection exist before the occurrence of gastric carcinoma[43-48], indicating that H. pylori infection is not a secondary infection but a primary infection. It was reported that. Mongolia gerbils have been infected with H. pylori through mouth route, which is implanted in their stomach for a long time. Twenty-six weeks after the infection, severe chronic active gastritis, ulcer and intestinal metaplasia occurred in the stomachs of the gerbils. And 37% of the gerbils involved in the study were attacked with gastric adenocarcinoma 62 wk after the infection[10].

The development and occurrence of gastric carcinoma is a long-lasting process and the effect of multiple factors. It is accepted by numerous scholars that H. pylori is an important risk factor for gastric carcinoma. In addition to the studies that support the association of H. pylori with gastric carcinoma, some researchers investigated the relationship between H. pylori and other kinds of carcinoma such as cancer of the colon, rectum, esophagus etc. and they made a negative conclusion, which proved the effect of H. pylori in gastric carcinoma in the other directions. However, H. pylori is not the unique etiological factor for gastric carcinoma. The association of the occurrence of gastric carcinoma with H. pylori infection should be considered from the angle of the multi-agent compound etiological theory[49-62].

According to the studies that support the opinion of association of H. pylori with gastric carcinoma, It can be assumed that the canceration of gastric mucosa took place under the action of H. pylori in the following process: H. pylori related gastritis of antrum→ atrophic gastritis → intestinal metaplasia → gastric carcinoma.

There are many problems we are going to face. The infection rate of H. pylori is very high in the population surveys. But why most of those with H. pylori infection were not attacked with gastric carcinoma. What are the other factors acting together with H. pylori to cause gastric carcinoma How do they act We must do more prospective interventional trial to answer these questions. It will be more helpful to do random interventional trial of eradication of H. pylori infection among the high-risk groups of gastric carcinoma and precancerous lesions to observe if their incidence rate of gastric carcinoma will decrease. In China, though very few of this kind of prospective studies have been made, an interventional trial of eradication of H. pylori is being made in Shandong and Fujian provinces. It will be of great help in revealing the exact mechanism of H. pylori in the process of gastric mucosa canceration.

Footnotes

Edited by Ma JY

Supported by Funds for University Key Teachers by the Ministry of Education, No. 2000-65

References

1.Zhao ZQ. Association of H. pylori infection with gastroduodenal diseases. Tiedao Yixue. 1998;26:212–214. [Google Scholar]
2.Gao XH, Pan BR. Helicobacter pylori infection and gastric cancer. Xin Xiaohuabingxue Zazhi. 1995;3:223–224. [Google Scholar]
3.Zhang WD, Xu KQ. Progress in research of the role of Helicobacter pylori in the process of occurrence of gastric cancer. Xin Xiaohuabingxue Zazhi. 1997;5(Suppl 6):9–11. [Google Scholar]
4.Zu Y, Shu J, Yang CM, Zhong ZF, Dai HY, Wang X, Qin GM. Study on relation between H. pylori infection and risk of gastric cancer. Huaren Xiaohua Zazhi. 1998;6:367–368. [Google Scholar]
5.Wang JY. Recent development of studies on relation between H. pylori infection and gastric cancer. Huaren Xiaohua Zazhi. 1998;6:829–830. [Google Scholar]
6.Xiao SD. H. pylori and gastric cancer. Huaren Xiaohua Zazhi. 1998;6(Suppl 7):4. [Google Scholar]
7.Qin GLZB, Wang JM. Relationship between H. pylori infection and gastric cancer. Huaren Xiaohua Zazhi. 1998:6 (Suppl 7): 421. [Google Scholar]
8.Hu PJ. H. pylori and gastric cancer: challenge in the research. Shijie Huaren Xiaohua Zazhi. 1999;7:1–2. [Google Scholar]
9.Quan J, Fan XG. Progress in experimental research of H. pylori infection and gastric carcinoma. Shijie Huaren Xiaohua Zazhi. 1999;7:1068–1069. [Google Scholar]
10.Wang PX, Zhang XR, Yin YF. 10 years’ retrospective analysis of correlation of gastric cancer and precancerosis withH. pylori in Muslim, Tibet and Han population in China. Shijie Huaren Xiaohua Zazhi. 2000;8:368. [Google Scholar]
11.Wang PX, Zhang XR, Yin YF, Wan DJ. Epidemiological relationship between H. pylori infection and gastric cancer in minority population in western China. Shijie Huaren Xiaohua Zazhi. 2000;8:1444. [Google Scholar]
12.Zhou LJ, Tang JX, Chen XQ, Chen J. Relationship between H. pylori infection and gastric cancer. Shijie Huaren Xiaohua Zazhi. 2000;8(Suppl 8):67. [Google Scholar]
13.Gu JZ, Hou TW, Wang XX. Cross-sectional study of precancerosis of gastric mucosa caused by H. pylori. Shijie Huaren Xiaohua Zazhi. 2001;9:111. [Google Scholar]
14.Li YY, Hu PJ, Lin HL, Zhao SM. H. pylori and gastric cancer: An endoscopic survey in low and high risk areas for gastric cancer. Linchuang Xiaohua Zazhi. 1996;8:145–147. [Google Scholar]
15.Liang HJ, Liu WW, Fang DC, Wang ZH, Zhou ZC, Xu Z, Gao JH. Study on the relationship between H. pylori infection and risk of gastric cancer. Zhonghua Xiaohua Neijing Zazhi. 1997;14:15–17. [Google Scholar]
16.Yang F. Relationship between H. pylori infection and gastric precancerosis. Zhongguo Neijing Zazhi. 1999;5:46–47. [Google Scholar]
17.Qiu H. Epidemiological analysis of relationship between gastric precancerosis and H. pylori infection. Xin Xiaohuabingxue Zazhi. 1997;5(Suppl 6):154. [Google Scholar]
18.Yu XE, Zhao AX, Wei DL, Du JZ. Relationship between H. pylori and gastric cancer. Huaren Xiaohua Zazhi. 1998;6(Suppl 7):367. [Google Scholar]
19.Zhuang XQ, Lin SR. Progress in research on the relationship between H. pylori and gastric cancer. Shijie Huaren Xiaohua Zazhi. 2000;8:206–207. [Google Scholar]
20.Eslick GD, Lim LL, Byles JE, Xia HH, Talley NJ. Association of Helicobacter pylori infection with gastric carcinoma: a meta-analysis. Am J Gastroenterol. 1999;94:2373–2379. doi: 10.1111/j.1572-0241.1999.01360.x. [DOI] [PubMed] [Google Scholar]
21.Xu SP, Wan MW, You WD. Study of correlation of H. pylori infection and human gastric cancer. Zhonghua Xiaohua Zazhi. 1997;17:211–212. [Google Scholar]
22.Yang RK, Lin SR, Lei DN, Ye SM, Chen WH, Li YH, Li YN, Zhou LY, Wang RT. Relationship between Helicobacter pylori infection and gastric cancer. Zhonghua Xiaohua Zazhi. 1997;17:251–253. [Google Scholar]
23.Li DG, Gao XH, Guan HW. [Relationship between Helicobacter pylori infection other factors and diffuse-and intestinal type stomach carcinomas] Zhonghua Liu Xing Bing Xue Za Zhi. 1995;16:299–302. [PubMed] [Google Scholar]
24.Yu DH, Ye HP, Wang P, Yao M, Ding RP. Relationship between malignent t um or of stomach and H. pylori infection of Ltype. Zhongguo Renshougonghuanbing Zazhi. 1997;13:7–9. [Google Scholar]
25.Wang JL, Dong ZY. Relationship between gastric canc er and H. pylori infection. Zhonghua Shiyong Neike Zazhi. 1998;18:87. [Google Scholar]
26.Chen SY, Wang JY, Liu TS. H. pylori infection and gastric cancer, a Case-control study. Weichangbingxue He Ganbingxue Zazhi. 1998;7:227–229. [Google Scholar]
27.Yang W C, Li XL, Zhao WX, Zou JX. A study of relationship between H. pylori infection and proliferating cell nuclear antigen as well as apoptosis of gastric mucosa. Zhonghua Xiaohua Neijing Zazhi. 1997;14:337–340. [Google Scholar]
28.Hu FL, Guo F, Jia BQ. A study of correlation between H. pylori toxin and the occurrence of gastric canc er. Zhonghua Neike Zazhi. 1998;37:620–621. [Google Scholar]
29.Guo TM. Association of H. pylori with lesion of gastric mucosa. New Journal of Digestive Diseases. 1997;5:127. [Google Scholar]
30.Liu JY. Risk of occurrence of gastric cancer for patients with Cag A positive or negative H. pylori infection. Guowai Yixue. 1998;18:113–114. [Google Scholar]
31.Cao NY, Du HR. Gastric adenocarcinoma in differen t sites vs. H. pylori infection. Zhonghua Xiaohua Neijing Zazhi. 1998;15:147–149. [Google Scholar]
32.Zhong WR, Huang YX. A study of relationship between H. pylori infection and intestinal metaplasia of gastric mucosa. Zhonghua Xiaohua Zazhi. 1995;15:232–233. [Google Scholar]
33.Jiang HX, Chen ZN, Chen Z, Chen YN, Nong ZX, Wei ZP, Deng TC. Relationship between H. pylori infection and precancerous lesion of stomach. Zhonghua Shiyong Neike Zazhi. 1996;16:21–22. [Google Scholar]
34.Liang HJ, Liu WW, Fang DC, Shi CM, Xu QW, Wang JR. H. pylori infection vs. atrophy and intestinal metaplasia of gastric mucosa. Zhonghua Shiyong Neike Zazhi. 1996;16:406–407. [Google Scholar]
35.Ruan HJ, Shi MH, Lin X. Trying to find out the relationship bet ween H. pylori infection and precancerous lesion of stomach. Xin Yixue. 1997;28:464. [Google Scholar]
36.Zhang JB. Relationship between cytotoxin productive H. pylori infection and intestinal metaplasia of gastric mucosa. Xin Yixue. 1999;30:315–316. [Google Scholar]
37.Ch en JX, Song Y, Chen LP. Test and analysis of H. pylori of 642 cases with intestin al metaplasia. Zhejiang Medicine. 1997;19:193–194. [Google Scholar]
38.Liao LP, Chen FT, Zhang JN. Investigation of the relation between intestinal metaplasia of gastric mucosa and H. pylori infection. Zhonghua Xiaohua Neijing Zazhi. 1998;15:171–172. [Google Scholar]
39.Li XH, Zhu RM, Shi QL, Zhang ZH. H. pylori infection vs. primaryly mphoma of stomach. Xin Xiaohuabingxue Zazhi. 1997;5:502–503. [Google Scholar]
40.Han SX, Chen HP, Wen J, Yang H. Gastric mucosa-associated lymphoid tissue lymphoma vs.H. pylori infection. Zhonghua Neike Zazhi. 1997;36:253–254. [Google Scholar]
41.Yi ZH, Ouya ng Q, Li GD, Bu H. Trying to find out the correlation between primary malignant lymphoma of stomach and H. pylori infection. Zhonghua Neike Zazhi. 1997;36:44 2–445. [Google Scholar]
42.Li LS. Principle and Method for Study in Clinical medicine, Practi cal Clinical Epidemiology. Shanxi science and technology press. 2000. pp. 357–372. [Google Scholar]
43.Zhang SL, Chen HY. Relationship between H. pylori and histology of gastric cancer. Xin Xiaohuabingxue Zazhi. 1997;5:51. [Google Scholar]
44.Lu SY, Pan XZ, Peng XW, Shi ZL, Lin L, Chen MH. Study on mechanism of higher risk of gastric cancer caused by H. pylori. Shijie Huaren Xiaohua Zazhi. 2000;8(Suppl 8):80. [Google Scholar]
45.Li W, Wang XC, Li X. Pathologic observation of relation between the carcinoma of stomach and the infection of Helicobacter pylori. Zhongliu Fangzhi Yanjiu. 1996;23:135–136. [Google Scholar]
46.Liang HJ, Liu WW, Liu W, Fang DC, Shi CM, Xu QW. Effect of concentrated Helicobacter pylori cult ure supernatant on cell kinetics and unscheduled DNA synthesis in rat pyloric mucosa. Xin Xiaohuabingxue Zazhi. 1995;3:132–133. [Google Scholar]
47.Zhang MW, Du XL, Chen SB. Hel icobacter pylori infection and serum gastrin level in patients with gastric canc er. Xin Xiaohuabingxue Zazhi. 1996;4:82–83. [Google Scholar]
48.Wu Y, Zhang WD, Yang HT, Wu HD. R elationship between H. pylori infection and the locations and histological types of gastric carcinoma. Xin Xiaohuabingxue Zazhi. 1997;5:524–525. [Google Scholar]
49.Wang XH, Zhang WD, Zhang YL, Zeng JZ, Sun Y. Relationship between Hp infection and oncogene and tumor suppressor gene expressions in gastric cancer and precancerosis. Shijie Huaren Xiaohua Zazhi. 1998;6:516–518. [Google Scholar]
50.Lv ZW, Wang YX, Du YJ, Xu J. Role of the free radical in gastric cancer caused by H. pylori. Huaren Xiaohua Zazhi. 1998;6(Suppl 7):371. [Google Scholar]
51.Xia HX, Zhang GS. Apoptosis and proliferation in gastric cancer caused by Hp infection. Shijie Huaren Xiaohua Zazhi. 1999;7:740–742. [Google Scholar]
52.Zu Y, S hu J, Yang CM, Zhong ZF, Dai HY, Tang ZG, Wang X. Relationship between H. pylori infection and expression of oncogene protein in gastric cancer and precancerosis. Shijie Huaren Xiaohua Zazhi. 2000;8:582–583. [Google Scholar]
53.Wang RQ, Fang DC, Liu WW, Luo YH. Relationship between H. pylori infection and expression of MUC1 ane MUC6 in gastric cancer and precancerosis. Shijie Huaren Xiaohua Zazhi. 2000;8:584–58 5. [Google Scholar]
54.Guan JL, Zhang JP, Zhou TH. Relationship between telomerase Helicobact er pylori and stomach cacner. Shijie Huaren Xiaohua Zazhi. 2000;8:910–911. [Google Scholar]
55.Gao G, Zhou CY, Lin ZY. Relationship between gastric cancer and H. pylori infection and expression of c-myc and p53. Shijie Huaren Xiaohua Zazhi. 2000;8:941–943. [Google Scholar]
56.Huang MF, Zhu YQ, Zhang CX, Liu C, Huang X, Deng CS. Effect of H. pylori infection to proliferation, content of DNA and oncogene expression of gastric mucosa. Shijie Huaren Xiaohua Zazhi. 2000;8:1057–1059. [Google Scholar]
57.Lu HP, Zheng YB. H. pylori infection in tissues of intestinal metaplasia and gastric cancer and expression of ras. Shijie Huaren Xiaohua Zazhi. 2001;9:218–219. [Google Scholar]
58.Zhong HM, Song J, Yao P, Yin CC. Sig nificance of expression of p53 and Fas in gastric cancer with H. pylori infection. Shijie Huaren Xiaohua Zazhi. 2001;9:456–457. [Google Scholar]
59.Guan JL, Zhou TH, Xue M, Fan M Z, Li XQ, Cao SL, Shi GM, Han CL. Telomerase activated H. pylori infection and gastric cancer. Shijie Huaren Xiaohua Zazhi. 2000;8(Suppl 8):104. [Google Scholar]
60.Chen JX, Song Y, Fang ZQ. A study of expression of P21 in H. pylori infection and gastric cancer and precancerosis. Zhongliu Fangzhi Yanjiu. 1996;23:149–150. [Google Scholar]
61.Si JL, Liu JY, Qi YQ. A study on relationship between H. pylori infection and activity of telomerase in gastric mucosa. Shijie Huaren Xiaohua Zazhi. 1999;7:429–430. [Google Scholar]
62.Wang RQ, Fang DC, Liu WW, Luo YH. Relationship between H. pylori infection and express ion of MUC5AC in gastric cancer and paracancerous tissue. Shijie Huaren Xiaohua Zazhi. 1999;7:546. [Google Scholar]

[B1] 1.Zhao ZQ. Association of H. pylori infection with gastroduodenal diseases. Tiedao Yixue. 1998;26:212–214. [Google Scholar]

[B2] 2.Gao XH, Pan BR. Helicobacter pylori infection and gastric cancer. Xin Xiaohuabingxue Zazhi. 1995;3:223–224. [Google Scholar]

[B3] 3.Zhang WD, Xu KQ. Progress in research of the role of Helicobacter pylori in the process of occurrence of gastric cancer. Xin Xiaohuabingxue Zazhi. 1997;5(Suppl 6):9–11. [Google Scholar]

[B4] 4.Zu Y, Shu J, Yang CM, Zhong ZF, Dai HY, Wang X, Qin GM. Study on relation between H. pylori infection and risk of gastric cancer. Huaren Xiaohua Zazhi. 1998;6:367–368. [Google Scholar]

[B5] 5.Wang JY. Recent development of studies on relation between H. pylori infection and gastric cancer. Huaren Xiaohua Zazhi. 1998;6:829–830. [Google Scholar]

[B6] 6.Xiao SD. H. pylori and gastric cancer. Huaren Xiaohua Zazhi. 1998;6(Suppl 7):4. [Google Scholar]

[B7] 7.Qin GLZB, Wang JM. Relationship between H. pylori infection and gastric cancer. Huaren Xiaohua Zazhi. 1998:6 (Suppl 7): 421. [Google Scholar]

[B8] 8.Hu PJ. H. pylori and gastric cancer: challenge in the research. Shijie Huaren Xiaohua Zazhi. 1999;7:1–2. [Google Scholar]

[B9] 9.Quan J, Fan XG. Progress in experimental research of H. pylori infection and gastric carcinoma. Shijie Huaren Xiaohua Zazhi. 1999;7:1068–1069. [Google Scholar]

[B10] 10.Wang PX, Zhang XR, Yin YF. 10 years’ retrospective analysis of correlation of gastric cancer and precancerosis withH. pylori in Muslim, Tibet and Han population in China. Shijie Huaren Xiaohua Zazhi. 2000;8:368. [Google Scholar]

[B11] 11.Wang PX, Zhang XR, Yin YF, Wan DJ. Epidemiological relationship between H. pylori infection and gastric cancer in minority population in western China. Shijie Huaren Xiaohua Zazhi. 2000;8:1444. [Google Scholar]

[B12] 12.Zhou LJ, Tang JX, Chen XQ, Chen J. Relationship between H. pylori infection and gastric cancer. Shijie Huaren Xiaohua Zazhi. 2000;8(Suppl 8):67. [Google Scholar]

[B13] 13.Gu JZ, Hou TW, Wang XX. Cross-sectional study of precancerosis of gastric mucosa caused by H. pylori. Shijie Huaren Xiaohua Zazhi. 2001;9:111. [Google Scholar]

[B14] 14.Li YY, Hu PJ, Lin HL, Zhao SM. H. pylori and gastric cancer: An endoscopic survey in low and high risk areas for gastric cancer. Linchuang Xiaohua Zazhi. 1996;8:145–147. [Google Scholar]

[B15] 15.Liang HJ, Liu WW, Fang DC, Wang ZH, Zhou ZC, Xu Z, Gao JH. Study on the relationship between H. pylori infection and risk of gastric cancer. Zhonghua Xiaohua Neijing Zazhi. 1997;14:15–17. [Google Scholar]

[B16] 16.Yang F. Relationship between H. pylori infection and gastric precancerosis. Zhongguo Neijing Zazhi. 1999;5:46–47. [Google Scholar]

[B17] 17.Qiu H. Epidemiological analysis of relationship between gastric precancerosis and H. pylori infection. Xin Xiaohuabingxue Zazhi. 1997;5(Suppl 6):154. [Google Scholar]

[B18] 18.Yu XE, Zhao AX, Wei DL, Du JZ. Relationship between H. pylori and gastric cancer. Huaren Xiaohua Zazhi. 1998;6(Suppl 7):367. [Google Scholar]

[B19] 19.Zhuang XQ, Lin SR. Progress in research on the relationship between H. pylori and gastric cancer. Shijie Huaren Xiaohua Zazhi. 2000;8:206–207. [Google Scholar]

[B20] 20.Eslick GD, Lim LL, Byles JE, Xia HH, Talley NJ. Association of Helicobacter pylori infection with gastric carcinoma: a meta-analysis. Am J Gastroenterol. 1999;94:2373–2379. doi: 10.1111/j.1572-0241.1999.01360.x. [DOI] [PubMed] [Google Scholar]

[B21] 21.Xu SP, Wan MW, You WD. Study of correlation of H. pylori infection and human gastric cancer. Zhonghua Xiaohua Zazhi. 1997;17:211–212. [Google Scholar]

[B22] 22.Yang RK, Lin SR, Lei DN, Ye SM, Chen WH, Li YH, Li YN, Zhou LY, Wang RT. Relationship between Helicobacter pylori infection and gastric cancer. Zhonghua Xiaohua Zazhi. 1997;17:251–253. [Google Scholar]

[B23] 23.Li DG, Gao XH, Guan HW. [Relationship between Helicobacter pylori infection other factors and diffuse-and intestinal type stomach carcinomas] Zhonghua Liu Xing Bing Xue Za Zhi. 1995;16:299–302. [PubMed] [Google Scholar]

[B24] 24.Yu DH, Ye HP, Wang P, Yao M, Ding RP. Relationship between malignent t um or of stomach and H. pylori infection of Ltype. Zhongguo Renshougonghuanbing Zazhi. 1997;13:7–9. [Google Scholar]

[B25] 25.Wang JL, Dong ZY. Relationship between gastric canc er and H. pylori infection. Zhonghua Shiyong Neike Zazhi. 1998;18:87. [Google Scholar]

[B26] 26.Chen SY, Wang JY, Liu TS. H. pylori infection and gastric cancer, a Case-control study. Weichangbingxue He Ganbingxue Zazhi. 1998;7:227–229. [Google Scholar]

[B27] 27.Yang W C, Li XL, Zhao WX, Zou JX. A study of relationship between H. pylori infection and proliferating cell nuclear antigen as well as apoptosis of gastric mucosa. Zhonghua Xiaohua Neijing Zazhi. 1997;14:337–340. [Google Scholar]

[B28] 28.Hu FL, Guo F, Jia BQ. A study of correlation between H. pylori toxin and the occurrence of gastric canc er. Zhonghua Neike Zazhi. 1998;37:620–621. [Google Scholar]

[B29] 29.Guo TM. Association of H. pylori with lesion of gastric mucosa. New Journal of Digestive Diseases. 1997;5:127. [Google Scholar]

[B30] 30.Liu JY. Risk of occurrence of gastric cancer for patients with Cag A positive or negative H. pylori infection. Guowai Yixue. 1998;18:113–114. [Google Scholar]

[B31] 31.Cao NY, Du HR. Gastric adenocarcinoma in differen t sites vs. H. pylori infection. Zhonghua Xiaohua Neijing Zazhi. 1998;15:147–149. [Google Scholar]

[B32] 32.Zhong WR, Huang YX. A study of relationship between H. pylori infection and intestinal metaplasia of gastric mucosa. Zhonghua Xiaohua Zazhi. 1995;15:232–233. [Google Scholar]

[B33] 33.Jiang HX, Chen ZN, Chen Z, Chen YN, Nong ZX, Wei ZP, Deng TC. Relationship between H. pylori infection and precancerous lesion of stomach. Zhonghua Shiyong Neike Zazhi. 1996;16:21–22. [Google Scholar]

[B34] 34.Liang HJ, Liu WW, Fang DC, Shi CM, Xu QW, Wang JR. H. pylori infection vs. atrophy and intestinal metaplasia of gastric mucosa. Zhonghua Shiyong Neike Zazhi. 1996;16:406–407. [Google Scholar]

[B35] 35.Ruan HJ, Shi MH, Lin X. Trying to find out the relationship bet ween H. pylori infection and precancerous lesion of stomach. Xin Yixue. 1997;28:464. [Google Scholar]

[B36] 36.Zhang JB. Relationship between cytotoxin productive H. pylori infection and intestinal metaplasia of gastric mucosa. Xin Yixue. 1999;30:315–316. [Google Scholar]

[B37] 37.Ch en JX, Song Y, Chen LP. Test and analysis of H. pylori of 642 cases with intestin al metaplasia. Zhejiang Medicine. 1997;19:193–194. [Google Scholar]

[B38] 38.Liao LP, Chen FT, Zhang JN. Investigation of the relation between intestinal metaplasia of gastric mucosa and H. pylori infection. Zhonghua Xiaohua Neijing Zazhi. 1998;15:171–172. [Google Scholar]

[B39] 39.Li XH, Zhu RM, Shi QL, Zhang ZH. H. pylori infection vs. primaryly mphoma of stomach. Xin Xiaohuabingxue Zazhi. 1997;5:502–503. [Google Scholar]

[B40] 40.Han SX, Chen HP, Wen J, Yang H. Gastric mucosa-associated lymphoid tissue lymphoma vs.H. pylori infection. Zhonghua Neike Zazhi. 1997;36:253–254. [Google Scholar]

[B41] 41.Yi ZH, Ouya ng Q, Li GD, Bu H. Trying to find out the correlation between primary malignant lymphoma of stomach and H. pylori infection. Zhonghua Neike Zazhi. 1997;36:44 2–445. [Google Scholar]

[B42] 42.Li LS. Principle and Method for Study in Clinical medicine, Practi cal Clinical Epidemiology. Shanxi science and technology press. 2000. pp. 357–372. [Google Scholar]

[B43] 43.Zhang SL, Chen HY. Relationship between H. pylori and histology of gastric cancer. Xin Xiaohuabingxue Zazhi. 1997;5:51. [Google Scholar]

[B44] 44.Lu SY, Pan XZ, Peng XW, Shi ZL, Lin L, Chen MH. Study on mechanism of higher risk of gastric cancer caused by H. pylori. Shijie Huaren Xiaohua Zazhi. 2000;8(Suppl 8):80. [Google Scholar]

[B45] 45.Li W, Wang XC, Li X. Pathologic observation of relation between the carcinoma of stomach and the infection of Helicobacter pylori. Zhongliu Fangzhi Yanjiu. 1996;23:135–136. [Google Scholar]

[B46] 46.Liang HJ, Liu WW, Liu W, Fang DC, Shi CM, Xu QW. Effect of concentrated Helicobacter pylori cult ure supernatant on cell kinetics and unscheduled DNA synthesis in rat pyloric mucosa. Xin Xiaohuabingxue Zazhi. 1995;3:132–133. [Google Scholar]

[B47] 47.Zhang MW, Du XL, Chen SB. Hel icobacter pylori infection and serum gastrin level in patients with gastric canc er. Xin Xiaohuabingxue Zazhi. 1996;4:82–83. [Google Scholar]

[B48] 48.Wu Y, Zhang WD, Yang HT, Wu HD. R elationship between H. pylori infection and the locations and histological types of gastric carcinoma. Xin Xiaohuabingxue Zazhi. 1997;5:524–525. [Google Scholar]

[B49] 49.Wang XH, Zhang WD, Zhang YL, Zeng JZ, Sun Y. Relationship between Hp infection and oncogene and tumor suppressor gene expressions in gastric cancer and precancerosis. Shijie Huaren Xiaohua Zazhi. 1998;6:516–518. [Google Scholar]

[B50] 50.Lv ZW, Wang YX, Du YJ, Xu J. Role of the free radical in gastric cancer caused by H. pylori. Huaren Xiaohua Zazhi. 1998;6(Suppl 7):371. [Google Scholar]

[B51] 51.Xia HX, Zhang GS. Apoptosis and proliferation in gastric cancer caused by Hp infection. Shijie Huaren Xiaohua Zazhi. 1999;7:740–742. [Google Scholar]

[B52] 52.Zu Y, S hu J, Yang CM, Zhong ZF, Dai HY, Tang ZG, Wang X. Relationship between H. pylori infection and expression of oncogene protein in gastric cancer and precancerosis. Shijie Huaren Xiaohua Zazhi. 2000;8:582–583. [Google Scholar]

[B53] 53.Wang RQ, Fang DC, Liu WW, Luo YH. Relationship between H. pylori infection and expression of MUC1 ane MUC6 in gastric cancer and precancerosis. Shijie Huaren Xiaohua Zazhi. 2000;8:584–58 5. [Google Scholar]

[B54] 54.Guan JL, Zhang JP, Zhou TH. Relationship between telomerase Helicobact er pylori and stomach cacner. Shijie Huaren Xiaohua Zazhi. 2000;8:910–911. [Google Scholar]

[B55] 55.Gao G, Zhou CY, Lin ZY. Relationship between gastric cancer and H. pylori infection and expression of c-myc and p53. Shijie Huaren Xiaohua Zazhi. 2000;8:941–943. [Google Scholar]

[B56] 56.Huang MF, Zhu YQ, Zhang CX, Liu C, Huang X, Deng CS. Effect of H. pylori infection to proliferation, content of DNA and oncogene expression of gastric mucosa. Shijie Huaren Xiaohua Zazhi. 2000;8:1057–1059. [Google Scholar]

[B57] 57.Lu HP, Zheng YB. H. pylori infection in tissues of intestinal metaplasia and gastric cancer and expression of ras. Shijie Huaren Xiaohua Zazhi. 2001;9:218–219. [Google Scholar]

[B58] 58.Zhong HM, Song J, Yao P, Yin CC. Sig nificance of expression of p53 and Fas in gastric cancer with H. pylori infection. Shijie Huaren Xiaohua Zazhi. 2001;9:456–457. [Google Scholar]

[B59] 59.Guan JL, Zhou TH, Xue M, Fan M Z, Li XQ, Cao SL, Shi GM, Han CL. Telomerase activated H. pylori infection and gastric cancer. Shijie Huaren Xiaohua Zazhi. 2000;8(Suppl 8):104. [Google Scholar]

[B60] 60.Chen JX, Song Y, Fang ZQ. A study of expression of P21 in H. pylori infection and gastric cancer and precancerosis. Zhongliu Fangzhi Yanjiu. 1996;23:149–150. [Google Scholar]

[B61] 61.Si JL, Liu JY, Qi YQ. A study on relationship between H. pylori infection and activity of telomerase in gastric mucosa. Shijie Huaren Xiaohua Zazhi. 1999;7:429–430. [Google Scholar]

[B62] 62.Wang RQ, Fang DC, Liu WW, Luo YH. Relationship between H. pylori infection and express ion of MUC5AC in gastric cancer and paracancerous tissue. Shijie Huaren Xiaohua Zazhi. 1999;7:546. [Google Scholar]

PERMALINK

Association of H. pylori infection with gastric carcinoma: A meta analysis

Fu-Bo Xue

Yong-Yong Xu

Yi Wan

Bo-Rong Pan

Jun Ren

Dai-Ming Fan

Abstract

INTRODUCTION