Yonsei Med J.  2013 Jul;54(4):832-838. 10.3349/ymj.2013.54.4.832.

Association of Helicobacter pylori with Elevated Blood Ammonia Levels in Cirrhotic Patients: A Meta-Analysis

Affiliations
  • 1Department of Gastroenterology, the First Affiliated Hospital of Guangxi Medical University, Nanning, Guangxi, PR China. luckydoc123@qq.com
  • 2Jiangsu University Affiliated Yixing People's Hospital, Yixing, Jiangsu, PR China.
  • 3Guangxi Information Institute, Nanning, Guangxi, PR China.

Abstract

PURPOSE
The association between Helicobacter pylori (H. pylori) and blood ammonia levels in cirrhotic patients is controversial. We aimed to clarify this controvercy by performing a meta-analysis of published studies.
MATERIALS AND METHODS
We searched PubMed, EMBASE and Cochrane library for studies which explored the association between H. pylori and blood ammonia levels in cirrhotic patients before May 2012. Six cohort studies involved in 632 H. pylori positive and 396 H. pylori negative cirrhotic patients were eligible for our analysis. The summary estimates were presented as standard means differences (SMD) and 95% confidence intervals (CI) from individual studies.
RESULTS
Overall, there was significant association between H. pylori infection and the elevated blood ammonia levels in cirrhotic patients (SMD=0.34, 95% CI=0.21-0.47, I2=42.1%). Sensitivity analysis further confirmed this association. Subgroup analysis showed that the association was found only in Asian ethnicity, but not in Caucasian ethnicity.
CONCLUSION
H. pylori infection is associated with elevated blood ammonia levels in cirrhotic patients, and more large scale studies and stratify analysis are warranted in order to further evaluate this association.

Keyword

Helicobacter pylori; blood; ammonia; meta-analysis

MeSH Terms

Ammonia/blood
Asian Continental Ancestry Group
European Continental Ancestry Group
Helicobacter Infections/*blood
Helicobacter pylori/pathogenicity
Humans
Liver Cirrhosis/*blood/*microbiology
Publication Bias
Regression Analysis
Ammonia

Figure

  • Fig. 1 Flow diagram of the study selection process.

  • Fig. 2 Meta-analysis of nine included studies. SMD, standard means differences; CI, confidence intervals.

  • Fig. 3 Funnel Plot of the Meta-Analysis (Begg's test). SMD, standard means differences.


Reference

1. Souba WW. Interorgan ammonia metabolism in health and disease: a surgeon's view. JPEN J Parenter Enteral Nutr. 1987; 11:569–579.
Article
2. LeVeen HH, LeVeen EG, LeVeen RF. Awakenings to the pathogenicity of urease and the requirement for continuous long term therapy. Biomed Pharmacother. 1994; 48:157–166.
Article
3. Demirtürk L, Yazgan Y, zci O, Ozel M, Toğrol E, Gültepe M, et al. The effect of Helicobacter pylori eradication on gastric juice and blood ammonia concentrations and on visual evoked potentials in cirrhotics. Helicobacter. 2001; 6:325–330.
Article
4. Queiroz DM, Rocha AM, Rocha GA, Cinque SM, Oliveira AG, Godoy A, et al. Association between Helicobacter pylori infection and cirrhosis in patients with chronic hepatitis C virus. Dig Dis Sci. 2006; 51:370–373.
Article
5. Chakrabarti P, Zullo A, Hassan C, Pandit A, Chowdhury A, Santra A, et al. Helicobacter pylori, gastric juice, and arterial ammonia levels in patients with cirrhosis. J Clin Gastroenterol. 2002; 34:578–581.
Article
6. Dasani BM, Sigal SH, Lieber CS. Analysis of risk factors for chronic hepatic encephalopathy: the role of Helicobacter pylori infection. Am J Gastroenterol. 1998; 93:726–731.
Article
7. Miyaji H, Ito S, Azuma T, Ito Y, Yamazaki Y, Ohtaki Y, et al. Effects of Helicobacter pylori eradication therapy on hyperammonaemia in patients with liver cirrhosis. Gut. 1997; 40:726–730.
Article
8. Chen SJ, Wang LJ, Zhu Q, Cai JT, Chen T, Si JM. Effect of H pylori infection and its eradication on hyperammo-nemia and hepatic encephalopathy in cirrhotic patients. World J Gastroenterol. 2008; 14:1914–1918.
Article
9. Abdel-Hady H, Zaki A, Badra G, Lotfy M, Selmi C, Giorgini A, et al. Helicobacter pylori infection in hepatic encephalopathy: relationship to plasma endotoxins and blood ammonia. Hepatol Res. 2007; 37:1026–1033.
Article
10. Vásconez C, Elizalde JI, Llach J, Ginès A, de la Rosa C, Fernández RM, et al. Helicobacter pylori, hyperammonemia and subclinical portosystemic encephalopathy: effects of eradication. J Hepatol. 1999; 30:260–264.
Article
11. Zullo A, Hassan C, Morini S. Helicobacter pylori infection in patients with liver cirrhosis: facts and fictions. Dig Liver Dis. 2003; 35:197–205.
Article
12. Zullo A, Rinaldi V, Efrati C, Hassan C, Caroli S, Riggio O, et al. Zinc, ammonia, and Helicobacter pylori infection in liver cirrhosis. Dig Liver Dis. 2000; 32:836–838.
Article
13. Miquel J, Barcena R, Boixeda D, Fernández J, SanRoman AL, Martín-de-Argila C, et al. Role of Helicobacter pylori infection and its eradication in patients with subclinical hepatic encephalopathy. Eur J Gastroenterol Hepatol. 2001; 13:1067–1072.
Article
14. Moher D, Liberati A, Tetzlaff J, Altman DG. PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009; 6:e1000097.
Article
15. Group CEPaOoC. EPOC resources for review authors. accessed on 2011 July 5. Available at: http://epoc.cochrane.org/epoc-resources.
16. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986; 7:177–188.
Article
17. Higgins JPT, Green S. Cochrane Handbook for Systematic Reviews of Interventions Version 5.0.1. 2008. The Cochrane Callaboration. Available at: http://www.cochrane-handbook.org.
18. Normand SL. Meta-analysis: formulating, evaluating, combining, and reporting. Stat Med. 1999; 18:321–359.
Article
19. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997; 315:629–634.
Article
20. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994; 50:1088–1101.
Article
21. Kini D, Aggarwal R, Saraswat VA, Naik SR. Role of Helicobacter pylori infection in hyperammonemia and subclinical hepatic encephalopathy in cirrhosis of liver. Indian J Gastroenterol. 2001; 20:237–240.
22. Yang CS, Cao SY, He XJ, Wang YX, Zhang YL. [Study of correlation between Helicobacter pylori infection and hyperammonemia and hepatic encephalopathy in cirrhotic patients]. Zhongguo Wei Zhong Bing Ji Jiu Yi Xue. 2007; 19:422–424.
23. Dunn BE, Campbell GP, Perez-Perez GI, Blaser MJ. Purification and characterization of urease from Helicobacter pylori. J Biol Chem. 1990; 265:9464–9469.
Article
24. Turbett GR, Nandapalan N, Campbell IG, Nikoletti SM, Mee BJ. Characterisation of the urease from Helicobacter pylori and comparison with the ureases from related spiral gastric bacteria. FEMS Microbiol Immunol. 1991; 3:19–24.
25. Neithercut WD, Rowe PA, el Nujumi AM, Dahill S, McColl KE. Effect of Helicobacter pylori infection on intragastric urea and ammonium concentrations in patients with chronic renal failure. J Clin Pathol. 1993; 46:544–547.
Article
26. Evans WB, Aoyagi T, Summerskill WH. Gastrointestinal urease in man. II. Urea hydrolysis and ammonia absorption in upper and lower gut lumen and the effect of neomycin. Gut. 1966; 7:635–639.
Article
27. Conn HO. Studies of the source and significance of blood ammonia. IV. Early ammonia peaks after ingestion of ammonium salts. Yale J Biol Med. 1972; 45:543–549.
28. Rudman D, DiFulco TJ, Galambos JT, Smith RB 3rd, Salam AA, Warren WD. Maximal rates of excretion and synthesis of urea in normal and cirrhotic subjects. J Clin Invest. 1973; 52:2241–2249.
Article
29. Huber M, Rössle M, Siegerstetter V, Ochs A, Haag K, Kist M, et al. Helicobacter pylori infection does not correlate with plasma ammonia concentration and hepatic encephalopathy in patients with cirrhosis. Hepatogastroenterology. 2001; 48:541–544.
30. DuBois S, Eng S, Bhattacharya R, Rulyak S, Hubbard T, Putnam D, et al. Breath ammonia testing for diagnosis of hepatic encephalopathy. Dig Dis Sci. 2005; 50:1780–1784.
Article
31. Calvet X, Nogueras C, Roqué M, Sanfeliu I. Helicobacter pylori is not a risk factor for hepatic encephalopathy. Dig Liver Dis. 2001; 33:414–419.
Article
32. Webberley MJ, Webberley JM, Newell DG, Lowe P, Melikian V. Seroepidemiology of Helicobacter pylori infection in vegans and meat-eaters. Epidemiol Infect. 1992; 108:457–462.
Article
33. Nardone G, Coscione P, D'Armiento FP, Del Pezzo M, Pontillo M, Mossetti G, et al. Cirrhosis negatively affects the efficiency of serologic diagnosis of Helicobacter pylori infection. Ital J Gastroenterol. 1996; 28:332–336.
34. Taylor-Robinson SD, Jackson N, Buckley C. Helicobacter pylori, ammonia and the brain. Gut. 1997; 40:805–806.
Article
35. Johnston SC. Identifying confounding by indication through blinded prospective review. Am J Epidemiol. 2001; 154:276–284.
Article
Full Text Links
  • YMJ
Actions
Cited
CITED
export Copy
Close
Share
  • Twitter
  • Facebook
Similar articles
Copyright © 2024 by Korean Association of Medical Journal Editors. All rights reserved.     E-mail: koreamed@kamje.or.kr