The Prevalence of Helicobacter pylori Infection in Korean Patients with Inflammatory Bowel Disease, a Multicenter Study

Min Jun Song; Dong Il Park; Sang Jun Hwang; Eun-Ran Kim; Young-Ho Kim; Byeong Ik Jang; Suck Ho Lee; Jeong Seon Ji; Sung Jae Shin

doi:10.4166/kjg.2009.53.6.341

Journal List > Korean J Gastroenterol > v.53(6) > 1006556

Go to TopGo to Top Go to BottomGo to Bottom

TOOLS

Song, Park, Hwang, Kim, Kim, Jang, Lee, Ji, and Shin: The Prevalence of Helicobacter pylori Infection in Korean Patients with Inflammatory Bowel Disease, a Multicenter Study

Original Article

Korean J Gastroenterol 2009;53(6):341-347.

Published online: 21 February 2009

DOI: https://doi.org/10.4166/kjg.2009.53.6.341

The Prevalence of Helicobacter pylori Infection in Korean Patients with Inflammatory Bowel Disease, a Multicenter Study

Min Jun Song, M.D., Dong Il Park, M.D., Sang Jun Hwang, M.D., Eun-Ran Kim, M.D.^∗, Young-Ho Kim, M.D.^∗, Byeong Ik Jang, M.D.^†, Suck Ho Lee, M.D.^‡, Jeong Seon Ji, M.D.^§, Sung Jae Shin, M.D.^∥

Department of Internal Medicine, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, Korea

^∗Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea

^†Yeungnam University College of Medicine, Daegu, Korea

^‡Soonchunhyang University College of Medicine, Cheonan, Korea

^§The Catholic University of Korea College of Medicine, Suwon, Korea

^¶Ajou University School of Medicine, Suwon, Korea

Received 13 October 2008 Accepted 16 October 2008

Abstract

Background/Aims

The prevalence of Helicobacter pylori (H. pylori) infection has been reported to be lower in individuals with inflammatory bowel disease (IBD) in some Western countries. We investigated H. pylori infection in Korean patients with IBD and any possible associations of H. pylori infection with drug therapy for IBD and the phenotype of Crohn's disease (CD).

Methods

We studied 316 unselected patients with IBD, including 169 ulcerative colitis (UC) patients and 147 with CD, and the control group consisted of 316 age- and gen-der-matched healthy people who received a comprehensive medical examination for a regular checkup purpose. Infection rates of H. pylori as detected by the urea breath test were compared between the IBD patients and the controls.

Results

A statistically significant difference in H. pylori infection rate was noticed between the IBD patients (25.3%) and the controls (52.5%; p＜0.001), and between UC (32.0%) and CD patients (17.7%; p=0.04). Among the IBD patients, the age group of ＜60 and individuals with a history of taking metronidazole (13.0%; p=0.038) or ciprofloxacin (6.7%; p=0.001) were found to have a meaningfully lower infection rate, but those who did not take antibiotics still showed H. pylori infection rate significantly lower than the controls (CD 22.0% vs. UC 33.8% vs. Control 52.5%, p＜0.001). With an exception of age, phenotypic characteristics showed no significant relations with H. pylori infection rate in CD patients.

Conclusions

Korean patients with IBD, particularly CD, were found to have a significantly lower H. pylori infection rate than the controls. This association was more evident in those ＜60 years old, which suggested that H. pylori infection might be deemed to lower possible risks of IBD in younger adults.

Keywords: Helicobacter pylori, Ulcerative colitis, Crohn's disease

REFERENCES

1. El-Omar E, Penman I, Cruikshank G, Dover S, Banerjee S, Williams C. Low prevalence of Helicobacter pylori in inflammatory bowel disease: association with sulfasalazine. Gut. 1994; 35:1385–1388.

2. Halme L, Kä rkkä inen P, Rautelin H, Kosunen T, Sipponen P. High frequency of Helicobacter pylori negative gastritis in patients with Crohn's disease. Gut. 1996; 38:379–383.

3. Halme L, Rautelin H, Leidenius M, Kosunen TU. Inverse correlation between Helicobacter pylori infection and inflammatory bowel disease. J Clin Pathol. 1996; 49:65–67.

4. De Reuck M, Brad M, Otero J, Cozzoli A, Denis P, De Koster E. H. pylori prevalence in IBD patients: role of IBD treatment. Gut. 1996; 39(suppl 2):A89–90.

5. Parente F, Molteni P, Bollani S, Maconi G, Vago L, Duga PG. Prevalence of Helicobacter pylori infection and related upper gastrointestinal lesions in patients with inflammatory bowel disease. A cross-sectional study with matching. Scand J Gastroenterol. 1997; 32:1140–1146.

6. Masato M, Toshiyuki M, Sadamune H, et al. Prevalence of Helicobacter pylori infection and correlation between severity of upper gastrointestinal lesions and H. pylori infection in Japanese patients with Crohn's disease. J Gastroenterol. 2001; 36:740–747.

7. Sousa LS, Santos AM, Macedo TC, et al. Prevalence of H. pylori infection in inflammatory bowel disease: a controlled study. Gut. 1996; 39(suppl 2):A94–95.

8. Loftus EV Jr. Clinical epidemiology of inflammatory bowel disease: incidence, prevalence, and environmental influences. Gastroenterology. 2004; 126:1504–1517.

9. Patrizia D, Stefano B, Anna RD, et al. Familial clustering of Helicobacter pylori infection: population based study. BMJ. 1999; 319:537–541.

10. Guillermo I, Perez-Perez , Dietrich R, Hermann B. Epidemiology of Helicobacter pylori infection. Helicobacter. 2004; 9(suppl 1):1–6.

11. Marion R, Leslie D, Marian V, Anna H, Billy B, Brendan D. Age-specific incidence of Helicobacter pylori. Gastroenterology. 2006; 130:65–72.

12. Kim JH, Kim HY, Kim NY, et al. Seroprevalence of Helicobacter pylori infection in asymptomatic people in Korea. Korean J Intern Med. 2000; 59:388–397.

13. Yang SK, Hong WS, Min YI, et al. Incidence and prevalence of ulcerative colitis in the Songpa-Kangdong District, Seoul, Korea, 1986-1997. J Gastroenterol Hepatol. 2000; 15:1037–1042.

14. Song IS, Chang DK, Kim CY. Current status of Crohn's disease in Korea. Korean J Intern Med. 1998; 55:158–168.

15. Andreas P, Clemens D, Georg O, et al. Influence of Helicobacter pylori infection on the phenotype of Crohn's disease. Am J Gastroenterol. 1999; 94:3239–3244.

16. László P, László S, Zsuzsa O, Pá l M, Zsolt T. Lower prevalence of Helicobacter pylori infection in patients with inflammatory bowel disease but not with chronic obstructive pulmonary disease-antibiotic use in the history does not play a significant role. Helicobacter. 2004; 9:278–283.

17. Gasche C, Scholmerich J, Brynskov J, et al. A simple classification of Crohn's disease: report of the Working Party for the World Congresses of Gastroenterology, Vienna 1998. Inflamm Bowel Dis. 2000; 6:8–15.

18. Kim MH, Kim MK, Choi BY, Shin YJ. Educational dis-parities in the metabolic syndrome in a rapidly changing soci-ety-the case of South Korea. Int J Epidemiol. 2005; 34:1266–1273.

19. Nishise Y, Fukao A, Takahashi T. Risk factors for Helicobacter pylori infection among a rural population in Japan: relation to living environment and medical history. J Epidemiol. 2003; 13:266–273.

20. Mendall M, Goggin PM, Molineaux N, et al. Childhood living conditions and Helicobacter pylori seropositivity in adult life. Lancet. 1992; 339:896–897.

21. Mitchell JD, Mitchell HM, Tobias V. Acute Helicobacter pylori in an infant, associated with gastric ulceration and sero-logical evidence of intra- familial transmission. Am J Gastroenterol. 1992; 87:382–386.

22. Gent AE, Hellier MD, Grace RH, Swarbrick ET, Coggon D. Inflammatory bowel disease and domestic hygiene in infancy. Lancet. 1994; 343:766–767.

23. Montgomery SM, Pounder RE, Wakefield AJ. Infant mortality and the incidence of inflammatory bowel disease. Lancet. 1997; 349:472–473.

24. Duggan AE, Usmani I, Neal KR, Logan RF. Appendicecto-my, childhood hygiene, Helicobacter pylori status, and risk of inflammatory bowel disease: a case control study. Gut. 1998; 43:494–498.

25. Gent AE, Hellier MD, Grace RH, et al. Inflammatory bowel disease and domestic hygiene in infancy. Lancet. 1994; 343:766–767.

26. Bach JF. The effect of infections and susceptibility to autoimmune and allergic diseases. N Engl J Med. 2002; 347:911–920.

27. Christelle B, John H, Alexandra B, Dino V, Stuart B. Are Helicobacter species and Enterotoxigenic Bacteroides fragilis involved in inflammatory bowel disease. Dig Dis Sci. 2004; 49:1425–1432.

28. Fiocchi C. Microbial factors in the pathogenesis of IBD. Biosci Microflora. 2003; 22:5–14.

29. Guarner F, Malagelada JR. Gut flora in health and disease. Lancet. 2003; 361:512–519.

30. Tursi A. Onset of Crohn's disease after Helicobacter pylori eradication. Inflamm Bowel Dis. 2006; 12:1008–1009.

31. Jovanovic IR, Miloslavljevic TN, Jankovic GP, et al. Clinical onset of the Crohn's disease after eradication therapy of Helicobacter pylori infection. Does Helicobacter pylori inter-act with natural history of inflammatory bowel diseases? Med Sci Monit. 2001; 7:137–141.

Fig. 1.

The prevalence of Helicobacter pylori infection in the IBD patients and controls. IBD, inflammatory bowel disease; UC, ulcerative colitis; CD, Crohn's disease.

Table 1.

Clinical Characteristics of the IBD Patients and Controls

	CD	UC	Control	p
Number	147	169	316
Mean age (years)^∗	33.5±14.5	44.7±14.0	40.7±14.2	＜0.001
Male/Female	99/48	107/62	206/110	N.S.
Education (years) n	(%)			＜0.001
≤9	46	57	73
	(31.3%)	(33.7%)	(23.1%)
＞9	101	112	243
	(68.7%)	(66.3%)	(76.9%)
Prevalence of	17.7	32.0	52.5	＜0.001
Hp＋ (%)

^∗ Expressed as means± SD (95% confidence interval). Data are numbers of patients unless otherwise specified. IBD, inflammatory bowel disease; CD, Crohn's disease; UC, ulcerative colitis; Hp＋, H. pylori positive.

Table 2.

Prevalence of Helicobacter pylori Infection in the IBD Patients and Controls by Age

	Number	Prevalence of Hp infection (%)
	Number	Control (n=316)	IBD (n=316)	CD (n=147)	UC (n=169)
＜30	167	31/72 (43.1%)	14/95 (14.7%)^∗	8/70 (11.4%)^∗	6/25 (24.0%)
30-44	247	77/135 (57%)	26/112 (23.2%)^∗	6/45 (13.3%)^∗	20/67 (29.9%)^∗
45-59	143	40/74 (54.1%)	21/69 (30.4%)^∗	8/22 (36.4%)	13/47 (27.7%)^∗
≥60	75	13/35 (51.4%)	19/40 (47.5%)	4/10 (40.0%)	15/30 (50%)

^∗ p＜0.05, vs. control. IBD, inflammatory bowel disease; Hp, Helicobacter pylori; UC, ulcerative colitis; CD, Crohn's disease.

Table 3.

Prevalence of H. pylori Infection in the IBD Patients according to Drug History

	Prevalence of Hp infection (%)		p
	User	Non-user	p
Sulfasalazine	11/59 (18.6%)	69/244 (28.3%)	N.S.
5-ASA	65/261 (24.9%)	15/55 (27.3%)	N.S.
Steroid	32/139 (23.0%)	48/177 (27.1%)	N.S.
Azathioprine	9/55 (16.4%)	71/261 (27.2%)	N.S.
Metronidazole	6/46 (13.0%)	74/270 (27.4%)	0.038
Ciprofloxacin	3/45 (6.7%)	77/271 (28.4%)	0.001

5-ASA, 5-aminosalicylic acid; Hp, Helicobacter pylori.

Table 4.

Preva Phenotype alence of H. pylori In nfection a according to IBD

	Subgroup	Number	Prevalence of Hp infection (%)
Crohn's disease
	Age^∗
	A1, ＜40 years	114	14.7%
	A2, ≥40 years	33	33.3%
	Location
	L1, terminal ileum	27	28.0%
	L2, colon	39	25.0%
	L3, ileocolon	74	14.9%
	L4, upper GI	7	0%
	Behavior
	B1, non-stricturing	95	20.0%
	non-penetrating
	B2, stricturing	33	16.7%
	B3, penetrating	19	17.6%
Ulcerative colitis
	Proctitis	65	29.4%
	Left colitis	53	31.7%
	Pancolitis	51	35.0%

^∗ p＜0.05. Hp, Helicobacter pylori.

TOOLS

Similar articles