Abstract
Background
Patients with chronic kidney disease (CKD) typically show a diminished immune response to hepatitis B virus (HBV) vaccine compared with individuals with intact kidney function. A number of inherited or acquired factors have been implicated in this suboptimal response. Patients with chronic kidney disease frequently have a compromised nutritional status; however, the impact of malnutrition on the immune response to hepatitis B virus vaccine in chronic kidney disease patients remains unclear.
Aim
To evaluate the influence of nutrition status on the immune response to HBV vaccine in CKD population by performing a systematic review of the literature with a meta-analysis of clinical studies.
Methods
Study-specific relative risks were weighted by the inverse of their variance to obtain fixed- and random-effects pooled estimates of impaired vaccine response across the published studies. The risk of poor serological response to HBV vaccine in chronic kidney disease population according to nutritional parameters was regarded as the most reliable outcome end-point. Only studies performing multivariate analysis in order to make adjustments for potential confounders were included.
Results
We identified seven studies (15,172 unique patients with CKD). The serum protection rate after a full course of recombinant or plasma-derived vaccine towards HBV ranged between 40 and 86%. Aggregation of study results showed an independent and adverse effect of poor nutrition status, as mostly detected by serum albumin levels, on the protection rate after HBV vaccine course; the summary estimate for adjusted RR was 1.50 with a 95% confidence interval (CI) of 1.02, 2.21; R i = 0.01 (random-effects model). The P value for study heterogeneity was significant (Q = 0.0001). In the subgroup of patients who received HBV recombinant vaccine, the relative risk of impaired serological response after HBV vaccination was 1.63 (95% CI, 1.08, 2.45), R i = 0.90, Q = 0.00001, with poor nutritional parameters at baseline.
Conclusions
An increased risk exists of impaired serologic response to HBV vaccine response among chronic kidney disease patients having poor nutrition status. Additional studies are needed to understand better the mechanisms underlying the relationship between nutritional status and serological response to HBV vaccine among patients with CKD.
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References
Labriola L, Jadoul M. The decades-long fight against HBV transmission to dialysis patients: slow but definite progress. Nephrol Dial Transplant. 2010;25:2047–2049.
Finelli L, Miller JT, Tokars JI, Alter MJ, Arduino MJ. National surveillance of dialysis-associated diseases in the United States. Semin Dial. 2005;18:52–61.
Thompson ND, Perez JF, Moorman AC, Holmberg SD. Nonhospital health-care associated hepatitis B and C virus transmission: United States, 1998–2008. Ann Intern Med. 2009;150:33–39.
Burdick RA, Bragg-Gresham JL, Woods JD, et al. Patterns of hepatitis B prevalence and seroconversion in haemodialysis units from three continents: the DOPPS. Kidney Int. 2003;63:2222–2229.
Rangel M, Coronado V, Euler G, Strikas R. For the Advisor Committee on Immunization Practices and the American Academy of Pediatrics. Vaccine recommendations for patients on chronic dialysis. Semin Dial. 2002;13:101–107.
Chandra RK. Cellular and molecular basis of nutrition-immunity interactions. Adv Exp Med Biol. 1990;262:13–18.
Takkouche B, Cadarso-Suarez C, Spiegelman D. Evaluation of old and new tests for heterogeneity in epidemiologic meta-analysis. Am J Epidemiol. 1999;150:206–215.
DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7:177–188.
Costa-Bouzas J, Takkouche B, Cadarso-Suarez C, Spiegelman D. HepiMA: software for the identification of heterogeneity in meta-analysis. Comput Methods Progr Biomed. 2001;64:101–107.
DaRoza G, Loewen A, Djurdjev O, et al. Stage of chronic kidney disease predicts seroconversion after hepatitis B immunization: earlier is better. Am J Kidney Dis. 2003;42:1184–1192.
Chin A. Hepatitis B virus vaccine response in haemodialysis: baseline patient characteristics. Hemodial Int. 2003;7:296–303.
Weinstein T, Chagnac A, Boaz M, et al. Improved immunogenicity of a novel third-generation recombinant hepatitis B vaccine in patients with end-stage renal disease. Nephron Clin Pract. 2004;97:c67–c72.
Lacson E, Teng M, Ong J, Vienneau L, Ofsthun N, Lazarus J. Antibody response to Engerix-B and Recombivax-HB hepatitis B vaccination in end-stage renal disease. Hemodial Int. 2005;9:367–375.
Chow K, Law M, Leung C, Szeto C, Li P. Antibody response to hepatitis B vaccine in end-stage renal disease patients. Nephron Clin Pract. 2006;103:c89–c93.
Liu J, Liu Y, Lin H, et al. Intravenous iron attenuates post-vaccination anti-HBsAg titers after quadruple hepatitis B vaccination in dialysis patients with erythropoietin therapy. Int J Clin Pract. 2009;63:387–393.
Afsar B, Elsurer R, Eyileten T, Yilmaz M, Caglar K. Antibody response following hepatitis B vaccination in dialysis patients: does depression and life quality matter? Vaccine. 2009;27:5865–5869.
Fernandez E, Betriu M, Gomez R, Montoliu J. Response to the hepatitis B virus vaccine in haemodialysis patients: influence of malnutrition and its importance as a risk factor for morbidity and mortality. Nephrol Dial Transplant. 1996;11:1559–1563.
Morais E, Resende M, Oliveira A, et al. Intradermal hepatitis B vaccination in patients with advanced chronic renal failure: immunogenicity and follow-up. Aliment Pharmacol Ther. 2007;25:849–855.
Fabrizi F, Di Filippo S, Marcelli D, et al. Recombinant hepatitis B vaccine use in chronic haemodialysis patients. Nephron. 1996;72:536–543.
Kara I, Yilmaz M, Suner A, Kadiroglu A, Isikoglu B. The evaluation of immune responses that occur after HBV infection and HBV vaccination in haemodialysis patients. Vaccine. 2004;22:3963–3967.
Lombardi M, Pizzarelli F, Righi M, et al. Hepatitis B vaccination in dialysis patients and nutritional status. Nephron. 1992;61:266–268.
Vagelli G, Calabrese G, Mazzotta A, Pratesi G, Gonella M. More about response to hepatitis B vaccine in haemodialysis patients. Nephron. 1988;49:171.
Chow K, Lo S, Szeto C, et al. Extra-high-dose hepatitis B vaccination does not confer longer seroprotection in peritoneal dialysis patients: a randomized controlled trial. Nephrol Dial Transplant. 2010;25:2303–2309.
Radziszewski A, Gajda M, Pituch-Noworolska A, et al. The evaluation of the effectiveness of multiple dose intradermal hepatitis B re-vaccination in haemodialysis patients not responding to standard method of immunization. Prezegl Lek. 2007;64:470–475.
Verkade M, Druningen C, op de Hoek C, Weimar W, Betjes M. Decreased antigen-specific T-cell proliferation by moDC among hepatitis B vaccine non-responders on haemodialysis. Clin Exp Med. 2007;7:65–71.
Mak R, Ikizler A, Kovesdy C, Raj D, Stenvinkel P, Kalantar-Zadeh K. Wasting in chronic kidney disease. J Cachexia Sarcopenia Muscle. 2011;2:9–25.
Liu Y, Kao M, Huang C. A comparison of responsiveness to hepatitis B vaccination in patients on haemodialysis and peritoneal dialysis. Vaccine. 2005;23:3957–3960.
Peces R, de la Torre M, Alcazar R, Urra J. Prospective analysis of the factors influencing the antibody response to hepatitis B vaccine in haemodialysis patients. Am J Kidney Dis. 1997;29:239–245.
Elwell R, Neumann M, Bailie G. Factors associated with long-term antibody production induced by hepatitis B vaccine in patients undergoing haemodialysis: a retrospective cohort study. Pharmacotherapy. 2003;23:1558–1563.
Navarro J, Teruel J, Mateos M, Marcen R, Ortuno J. Antibody level after hepatitis B vaccination in haemodialysis patients: influence of hepatitis C virus infection. Am J Nephrol. 1996;16:95–97.
Acknowledgment
The authors’ work is supported in part by the grant ‘Project Glomerulonephritis’; in memory of Pippo Neglia.
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The authors of this manuscript have no conflicts of interest to disclose.
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Fabrizi, F., Dixit, V., Martin, P. et al. Meta-Analysis: The Impact of Nutritional Status on the Immune Response to Hepatitis B Virus Vaccine in Chronic Kidney Disease. Dig Dis Sci 57, 1366–1372 (2012). https://doi.org/10.1007/s10620-011-1987-1
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DOI: https://doi.org/10.1007/s10620-011-1987-1