Abstract
Background
We performed a systematic review and meta-analysis to examine factors associated with HBV immune response in dialysis patients, and the association between the immune response to the HBV vaccine and mortality.
Methods
Electronic databases were searched for studies of dialysis patients that compared the characteristics of HBV vaccine responders and non-responders. Mortality was also analyzed according to the vaccine immune response (defined by hepatitis B surface antibody titer > 10 mIU/mL). Random-effects model meta-analyses were performed to compute a weighted mean difference (WMD), a pooled odds ratio (OR), and a pooled risk ratio (RR) between groups.
Results
We identified 61 studies with a total of 6628 dialysis patients who completed the course of HBV vaccination, 4582 responders (69%) and 2046 non-responders (31%). By meta-analysis, relative to non-responders, HBV vaccine responders had a higher dialysis adequacy as measured by Kt/V (WMD 0.08, P < 0.001), a higher serum albumin (WMD 0.12 gm/dL, P < 0.001), a higher normalized protein catabolic rate (WMD 0.12 gm/kg/day, P = 0.001), a higher hemoglobin (WMD 0.15 gm/L, P = 0.03), and a higher parathyroid hormone level (WMD 44 pg/mL, P = 0.004). HBV vaccine responders were younger (WMD − 4.68 years, P < 0.001), had been on dialysis for longer (WMD 2.60 months, P < 0.001), were less likely to have diabetes mellitus (pooled OR 0.65, P < 0.001), and were less likely to carry the human leukocyte antigen (HLA) DR3 (pooled OR 0.38, P = 0.01). Compared to non-responders, HBV vaccine responders had lower risk for all-cause mortality (pooled RR 0.64, P < 0.001), and lower risk for cardiovascular-related mortality (pooled RR 0.74, P = 0.02).
Conclusion
In dialysis patients, the lack of immune response to the HBV vaccine is associated with older age, diabetes mellitus, HLA-DR3 status, shorter time on dialysis, lower nutritional status, lower hemoglobin, lower PTH level, and lower dialysis adequacy. Tackling some of these modifiable factors might improve the HBV vaccine immune response.
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References
Poh Z, Goh BB, Chang PE, Tan CK (2015) Rates of cirrhosis and hepatocellular carcinoma in chronic hepatitis B and the role of surveillance: a 10-year follow-up of 673 patients. Eur J Gastroenterol Hepatol 27(6):638–643
Di Bisceglie AM (2009) Hepatitis B and hepatocellular carcinoma. Hepatology 49(5 Suppl):S56–S60
Polaris Observatory Collaborators (2018) Global prevalence, treatment, and prevention of hepatitis B virus infection in 2016: a modelling study. Lancet Gastroenterol Hepatol 3(6):383–403
Ujiie M, Sasaki K, Yoshikawa N, Enami T, Shobayashi T (2016) Introduction of a hepatitis B vaccine into the national routine immunisation programme of Japan. Lancet Infect Dis. 16(12):1325
Posuwan N, Wanlapakorn N, Sa-Nguanmoo P et al (2016) The success of a universal hepatitis B immunization program as part of Thailand’s EPI after 22 years’ implementation. PLoS One 11(3):e0150499
Namgyal P (2003) Impact of hepatitis B immunization, Europe and worldwide. J Hepatol 39(Suppl 1):S77–S82
Fabrizi F, Martin P (2000) Hepatitis B virus infection in dialysis patients. Am J Nephrol 20(1):1–11
Courouce AM, Jungers P, Benhamou E, Laplanche A, Crosnier J (1984) Hepatitis B vaccine in dialysis patients. N Engl J Med 311(23):1515–1516
Cohen G, Horl WH (2012) Immune dysfunction in uremia-an update. Toxins (Basel) 4(11):962–990
Kato S, Chmielewski M, Honda H et al (2008) Aspects of immune dysfunction in end-stage renal disease. Clin J Am Soc Nephrol 3(5):1526–1533
Geerlings SE, Hoepelman AI (1999) Immune dysfunction in patients with diabetes mellitus (DM). FEMS Immunol Med Microbiol 26(3–4):259–265
Lord JM (2013) The effect of ageing of the immune system on vaccination responses. Hum Vaccine Immunother 9(6):1364–1367
Fabrizi F, Dixit V, Martin P, Messa P (2011) Meta-analysis: the impact of diabetes mellitus on the immunological response to hepatitis B virus vaccine in dialysis patients. Aliment Pharmacol Ther 33(7):815–821
Fabrizi F, Martin P, Dixit V, Bunnapradist S, Dulai G (2004) Meta-analysis: the effect of age on immunological response to hepatitis B vaccine in end-stage renal disease. Aliment Pharmacol Ther 20(10):1053–1062
Ozdemir FN, Micozkadioglu H, Arat Z, Turan M, Gulmus S, Haberal M (2004) The importance of A3 allele in response to hepatitis B vaccine in end-stage renal disease patients. Transplant Proc 36(9):2615–2617
Peces R, de la Torre M, Alcazar R, Urra JM (1997) Prospective analysis of the factors influencing the antibody response to hepatitis B vaccine in hemodialysis patients. Am J Kidney Dis 29(2):239–245
Caillat-Zucman S, Gimenez JJ, Albouze G et al (1993) HLA genetic heterogeneity of hepatitis B vaccine response in hemodialyzed patients. Kidney Int Suppl 41:S157–S160
Zitt E, Hafner-Giessauf H, Wimmer B et al (2017) Response to active hepatitis B vaccination and mortality in incident dialysis patients. Vaccine 35(5):814–820
Lin SY, Liu JH, Wang SM et al (2012) Association of response to hepatitis B vaccination and survival in dialysis patients. BMC Nephrol. 13(1):97
Liberati A, Altman DG, Tetzlaff J et al (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ 339:b2700
Mulley WR, Le ST, Ives KE (2017) Primary seroresponses to double-dose compared with standard-dose hepatitis B vaccination in patients with chronic kidney disease: a systematic review and meta-analysis. Nephrol Dial Transplant 32(1):136–143
Yousaf F, Gandham S, Galler M, Spinowitz B, Charytan C (2015) Systematic review of the efficacy and safety of intradermal versus intramuscular hepatitis B vaccination in end-stage renal disease population unresponsive to primary vaccination series. Ren Fail 37(7):1080–1088
Fabrizi F, Dixit V, Magnini M, Elli A, Martin P (2006) Meta-analysis: intradermal vs. intramuscular vaccination against hepatitis B virus in patients with chronic kidney disease. Aliment Pharmacol Ther 24(3):497–506
von Elm E, Altman DG, Egger M, Pocock SJ, Gotzsche PC, Vandenbroucke JP (2008) The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. J Clin Epidemiol 61(4):344–349
Regenstein FG, Perrillo RP, Bodicky C, Stern K, Zelman S (1985) Clinical and immunologic features of chronic dialysis patients who fail to respond to hepatitis B vaccine. Vaccine 3(1):27–30
Walz G, Kunzendorf U, Haller H et al (1989) Factors influencing the response to hepatitis B vaccination of hemodialysis patients. Nephron 51(4):474–477
Pol S, Legendre C, Mattlinger B, Berthelot P, Kreis H (1990) Genetic basis of nonresponse to hepatitis B vaccine in hemodialyzed patients. J Hepatol 11(3):385–387
Fleming SJ, Moran DM, Cooksley WG, Faoagali JL (1991) Poor response to a recombinant hepatitis B vaccine in dialysis patients. J Infect 22(3):251–257
Sennesael JJ, Van Der Niepen P, Verbeelen DL (1991) Treatment with recombinant human erythropoietin increases antibody titers after hepatitis B vaccination in dialysis patients. Kidney Int 40(1):121–128
Lombardi M, Pizzarelli F, Righi M et al (1992) Hepatitis B vaccination in dialysis patients and nutritional status. Nephron 61(3):266–268
Stachowski J, Kramer J, Fust G, Maciejewski J, Baldamus CA, Petranyi GG (1995) Relationship between the reactivity to hepatitis B virus vaccination and the frequency of MHC class I, II and III alleles in haemodialysis patients. Scand J Immunol 42(1):60–65
Waite NM, Thomson LG, Goldstein MB (1995) Successful vaccination with intradermal hepatitis B vaccine in hemodialysis patients previously nonresponsive to intramuscular hepatitis B vaccine. J Am Soc Nephrol 5(11):1930–1934
Dacko C, Holley JL (1996) The influence of nutritional status, dialysis adequacy, and residual renal function on the response to hepatitis B vaccination in peritoneal dialysis patients. Adv Perit Dial 12:315–317
Fabrizi F, Di Filippo S, Marcelli D et al (1996) Recombinant hepatitis B vaccine use in chronic hemodialysis patients. Long-term evaluation and cost-effectiveness analysis. Nephron 72(4):536–543
Fernandez E, Betriu MA, Gomez R, Montoliu J (1996) 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 11(8):1559–1563
Khan AN, Bernardini J, Rault RM, Piraino B (1996) Low seroconversion with hepatitis B vaccination in peritoneal dialysis patients. Perit Dial Int 16(4):370–373
Mitwalli A (1996) Responsiveness to hepatitis b vaccine in immunocompromised patients by doubling the dose scheduling. Nephron 73(3):417–420
Navarro JF, Teruel JL, Mateos ML, Marcen R, Ortuno J (1996) Antibody level after hepatitis B vaccination in hemodialysis patients: influence of hepatitis C virus infection. Am J Nephrol 16(2):95–97
Jha R, Lakhtakia S, Jaleel MA, Narayan G, Hemlatha K (2001) Granulocyte macrophage colony stimulating factor (GM-CSF) induced sero-protection in end stage renal failure patients to hepatitis B in vaccine non-responders. Ren Fail 23(5):629–636
Eardley KS, Jones HE, Osman H, Smith SA (2002) Efficacy of the accelerated hepatitis B vaccination schedule used in haemodialysis patients post-exposure to virus: a single-centre experience. Nephrol Dial Transplant 17(11):1982–1987
Kovacic V, Sain M, Vukman V (2002) Efficient haemodialysis improves the response to hepatitis B virus vaccination. Intervirology 45(3):172–176
Chin AI (2003) Hepatitis B virus vaccine response in hemodialysis: baseline patient characteristics. Hemodial Int 7(4):296–303
Kara IH, Yilmaz ME, Suner A, Kadiroglu AK, Isikoglu B (2004) The evaluation of immune responses that occur after HBV infection and HBV vaccination in hemodialysis patients. Vaccine 22(29–30):3963–3967
Weinstein T, Chagnac A, Boaz M et al (2004) Improved immunogenicity of a novel third-generation recombinant hepatitis B vaccine in patients with end-stage renal disease. Nephron Clin Pract 97(2):c67–c72
Ahuja TS, Kumar S, Mansoury H, Rodriguez H, Kuo YF (2005) Hepatitis B vaccination in human immunodeficiency virus-infected adults receiving hemodialysis. Kidney Int 67(3):1136–1141
Liu YL, Kao MT, Huang CC (2005) A comparison of responsiveness to hepatitis B vaccination in patients on hemodialysis and peritoneal dialysis. Vaccine 23(30):3957–3960
Roozbeh J, Moini M, Lankarani KB, Sagheb MM, Shahpoori S, Bastani B (2005) Low dose intradermal versus high dose intramuscular hepatitis B vaccination in patients on chronic hemodialysis. ASAIO J 51(3):242–245
Chow KM, Man CL, Chi BL, Cheuk CS, Li PKT (2006) Antibody response to hepatitis B vaccine in end-stage renal disease patients. Nephron Clin Pract 103(3):c89–c93
Ibrahim S, el-Din S, Bazzal I (2006) Antibody level after hepatitis-B vaccination in hemodialysis patients: impact of dialysis adequacy, chronic inflammation, local endemicity and nutritional status. J Natl Med Assoc 98(12):1953–1957
Sit D, Kadiroglu AK, Kayabasi H, Yilmaz Z, Yilmaz ME (2007) The effect of inflammatory reactions on antibody unresponsiveness to hepatitis B vaccine in hemodialysis patients. Hepat Mon 7(1):15–19
Verkade MA, van Druningen CJ, Op de Hoek CT, Weimar W, Betjes MG (2007) Decreased antigen-specific T-cell proliferation by moDC among hepatitis B vaccine non-responders on haemodialysis. Clin Exp Med 7(2):65–71
Ramezani A, Velayati AA, Eslamifar A et al (2008) Persistence of hepatitis B vaccine immunity in hemodialysis patients. Ther Apher Dial 12(2):143–146
Sorkhi H, Roushan MR, Al Hashemi GH, Dooki MR, Bai S (2008) Response to hepatitis B virus vaccination in haemodialysis patients with and without hepatitis C infection. East Mediterr Health J 14(4):798–803
Afsar B, Elsurer R, Eyileten T, Yilmaz MI, Caglar K (2009) Antibody response following hepatitis B vaccination in dialysis patients: does depression and life quality matter? Vaccine. 27(42):5865–5869
Bock M, Barros E, Veronese FJ (2009) Hepatitis B vaccination in haemodialysis patients: a randomized clinical trial. Nephrology (Carlton). 14(3):267–272
Pin M, Compte MT, Angelet P, Gállego C, Gutiérrez C, Vea AM (2009) Long-term assessment of the immunological response to hepatitis B vaccines in 136 haemodialysis patients. Nefrologia 29(5):415–420
Ramezani A, Eslamifar A, Banifazl M et al (2009) Efficacy and long-term immunogenicity of hepatitis B vaccine in haemodialysis patients. Int J Clin Pract 63(3):394–397
Chow KM, Lo SH, Szeto CC et al (2010) Extra-high-dose hepatitis B vaccination does not confer longer serological protection in peritoneal dialysis patients: a randomized controlled trial. Nephrol Dial Transplant 25(7):2303–2309
Brown CM, Donlon S, O’Kelly P et al (2011) A prospective study of hepatitis B vaccination—a comparison of responders versus nonresponders. Ren Fail 33(3):276–279
Chaves SS, Daniels D, Cooper BW et al (2011) Immunogenicity of hepatitis B vaccine among hemodialysis patients: effect of revaccination of non-responders and duration of protection. Vaccine 29(52):9618–9623
Dervisoglu E, Simsek M, Yilmaz A (2011) Antibody response following hepatitis B vaccination in peritoneal dialysis patients: does normalized urea clearance matter? Clinics 66(9):1559–1562
Sari F, Taskapan H (2012) Good response to HBsAg vaccine in dialysis patients is associated with high CD4+/CD8+ ratio. Int Urol Nephrol 44(5):1501–1506
Afsar B (2013) The relationship between erythropoietin resistance and antibody response to hepatitis B vaccine in hemodialysis patients. Nephrourol Mon 5(3):806–812
Al Saran K, Sabry A, Al Halawany Z, Ismail M (2014) Factors affecting response to hepatitis B vaccine among hemodialysis patients in a large Saudi Hemodialysis Center. Saudi J Kidney Dis Transplant 25(1):185–191
Ayub MA, Bacci MR, Fonseca FL, Chehter EZ (2014) Hemodialysis and hepatitis B vaccination: a challenge to physicians. Int J Gen Med 7:109–114
El-Charabaty E, Saifan C, Samarneh MM, El-Sayegh S (2015) Variability in response to hepatitis B vaccine in hemodialysis patients. J Clin Med Res 7(5):315–318
Fabrizi F, Tarantino A, Castelnovo C, Martin P, Messa P (2015) Recombinant hepatitis B vaccine adjuvanted with AS04 in dialysis patients: a prospective cohort study. Kidney Blood Press Res 40(6):584–592
Patel N, Assimon MM, Bruni E, McNutt LA, Mason DL (2015) Incidence and clinical predictors of nonresponse to hepatitis B vaccination among patients receiving hemodialysis: importance of obesity. South Med J 108(9):567–573
Grzegorzewska AE, Świderska MK, Warchoł W (2016) Antibodies to hepatitis B virus surface antigen and survival of hemodialysis patients—a prospective study. Expert Rev Vaccines 15(8):1063–1074
Jhorawat R, Jain S, Pal A et al (2016) Effect of vitamin D level on the immunogenicity to hepatitis B vaccination in dialysis patients. Indian J Gastroenterol 35(1):67–71
Almueilo SH (2017) Evaluation of response to hepatitis B vaccination in chronic hemodialysis patients. Saudi J Med Med Sci 5(3):218–223
Asan A, Demirhan H, Sorkun HC et al (2017) Factors affecting responsiveness to hepatitis B immunization in dialysis patients. Int Urol Nephrol 49(10):1845–1850
Cordova E, Miglia I, Festuccia F et al (2017) Hepatitis B vaccination in haemodialysis patients: an underestimated problem. Factors influencing immune responses in ten years of observation in an Italian haemodialysis centre and literature review. Ann Ig 29(1):27–37
Ferreira TMB, Guimaraes TGS, Fontenele AMM, Salgado NF, Ferreira ASP, Costa APM (2017) Does infection by the hepatitis C virus decrease the response of immunization against the hepatitis B virus in individuals undergoing dialysis? J Bras Nefrol 39(2):141–145
Kauke T, Link M, Rentsch M et al (2017) Antibody response to HBV vaccination on dialysis does not correlate with the development of deNovo anti-HLA antibodies after renal transplantation. Transpl Immunol 42:5–8
Shamshirian A, Alikhani S, Alipoor R, Jafarpour H, Espahbodi F, Azizi S (2017) Evaluation of immunogenicity of hepatitis B vaccine in hemodialysis patients at Mazandaran Heart Center, Iran. Biomed Pharmacol J 10(2):557–562
Elhanan E, Boaz M, Schwartz I et al (2018) A randomized, controlled clinical trial to evaluate the immunogenicity of a PreS/S hepatitis B vaccine Sci-B-Vac, as compared to Engerix B((R)), among vaccine naive and vaccine non-responder dialysis patients. Clin Exp Nephrol 22(1):151–158
Grzegorzewska AE, Frycz BA, Winnicka H, Warchol W, Jagodzinski PP (2018) Relative indoleamine 2,3-dioxygenase transcript level concerning anti-HBs titers in response to HBV vaccination in hemodialysis patients. Expert Rev Vaccines 17(10):947–953
Huzmeli C, Candan F, Bagci G et al (2018) Vitamin d receptor taqi polymorphism is associated with higher immune response to hepatitis b vaccination in turkish dialysis patients. Acta Medica Mediterranea 34(3):791–796
Erdogdu HI, Atalay E, Gursoy G et al (2019) Factors affecting inadequate response to HBV vaccine in hemodialysis patients: northeast anatolia survey with six hemodialysis centers. Clin Exp Nephrol 23(4):530–536
Higgins JP, Altman DG, Gotzsche PC et al (2011) The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ 343:d5928
Fabrizi F, Dixit V, Messa P, Martin P (2015) Transmission of hepatitis B virus in dialysis units: a systematic review of reports on outbreaks. Int J Artif Organs 38(1):1–7
Lisowska-Myjak B (2014) Uremic toxins and their effects on multiple organ systems. Nephron Clin Pract 128(3–4):303–311
Mansouri L, Paulsson JM, Moshfegh A, Jacobson SH, Lundahl J (2013) Leukocyte proliferation and immune modulator production in patients with chronic kidney disease. PLoS One 8(8):e73141
Vaziri ND, Pahl MV, Crum A, Norris K (2012) Effect of uremia on structure and function of immune system. J Ren Nutr 22(1):149–156
Ruiz P, Gomez F, Schreiber AD (1990) Impaired function of macrophage Fc gamma receptors in end-stage renal disease. N Engl J Med 322(11):717–722
Girndt M, Sester U, Sester M, Kaul H, Kohler H (1999) Impaired cellular immune function in patients with end-stage renal failure. Nephrol Dial Transplant 14(12):2807–2810
Jaber BL, Cendoroglo M, Balakrishnan VS, Perianayagam MC, King AJ, Pereira BJ (2001) Apoptosis of leukocytes: basic concepts and implications in uremia. Kidney Int Suppl 78:S197–S205
Janus N, Vacher L-V, Karie S, Ledneva E, Deray G (2007) Vaccination and chronic kidney disease. Nephrol Dial Transplant 23(3):800–807
Alwarawrah Y, Kiernan K, MacIver NJ (2018) Changes in nutritional status impact immune cell metabolism and function. Front Immunol 9:1055
Sayarlioglu H, Erkoc R, Demir C et al (2006) Nutritional status and immune functions in maintenance hemodialysis patients. Mediat Inflamm 2006(1):20264
Prendergast AJ (2015) Malnutrition and vaccination in developing countries. Philos Trans R Soc Lond B Biol Sci 370(1671):20140141
Teixeira Nunes F, de Campos G, Xavier de Paula SM et al (2008) Dialysis adequacy and nutritional status of hemodialysis patients. Hemodial Int 12(1):45–51
Azar AT, Wahba K, Mohamed AS, Massoud WA (2007) Association between dialysis dose improvement and nutritional status among hemodialysis patients. Am J Nephrol 27(2):113–119
Schulman G (2004) The dose of dialysis in hemodialysis patients: impact on nutrition. Semin Dial 17(6):479–488
Ghamar-Chehreh ME, Agah S, Khedmat H, Aghaei A, Alavian SM (2017) Serum albumin level as an indicator of response to hepatitis B vaccination in dialysis patients: a systematic review and meta-analysis. Casp J Intern Med 8(4):250–257
Harford R, Clark MJ, Norris KC, Yan G (2016) Relationship between age and pre-end stage renal disease care in elderly patients treated with maintenance hemodialysis. Nephrol Nurs J 43(2):101–107 (quiz 8)
Montecino-Rodriguez E, Berent-Maoz B, Dorshkind K (2013) Causes, consequences, and reversal of immune system aging. J Clin Investig 123(3):958–965
Goronzy JJ, Weyand CM (2013) Understanding immunosenescence to improve responses to vaccines. Nat Immunol 14(5):428–436
Wagner A, Garner-Spitzer E, Jasinska J et al (2018) Age-related differences in humoral and cellular immune responses after primary immunisation: indications for stratified vaccination schedules. Sci Rep 8(1):9825
Lee SK, Ding JL (2013) A perspective on the role of extracellular hemoglobin on the innate immune system. DNA Cell Biol 32(2):36–40
Ekiz C, Agaoglu L, Karakas Z, Gurel N, Yalcin I (2005) The effect of iron deficiency anemia on the function of the immune system. Hematol J. 5(7):579–583
Roman RM, Lobo PI, Taylor RP et al (2004) Prospective study of the immune effects of normalizing the hemoglobin concentration in hemodialysis patients who receive recombinant human erythropoietin. J Am Soc Nephrol 15(5):1339–1346
Bishlawy IM (1999) Red blood cells, hemoglobin and the immune system. Med Hypotheses 53(4):345–346
Kidney Disease: Improving Global Outcomes (KDIGO) CKD-MBD Update Work Group (2017) KDIGO 2017 clinical practice guideline update for the diagnosis, evaluation, prevention, and treatment of chronic kidney disease-mineral and bone disorder (CKD-MBD). Kidney Int Suppl (2011) 7(1):1–59
Geara AS, Castellanos MR, Bassil C et al (2010) Effects of parathyroid hormone on immune function. Clin Dev Immunol. 2010;418695. https://doi.org/10.1155/2010/418695
Yasunaga C, Nakamoto M, Matsuo K, Nishihara G, Yoshida T, Goya T (1999) Effects of a parathyroidectomy on the immune system and nutritional condition in chronic dialysis patients with secondary hyperparathyroidism. Am J Surg 178(4):332–336
Shurtz-Swirski R, Shkolnik T, Shasha SM (1995) Parathyroid hormone and the cellular immune system. Nephron 70(1):21–24
Garrett G, Sardiwal S, Lamb EJ, Goldsmith DJ (2013) PTH–a particularly tricky hormone: why measure it at all in kidney patients? Clin J Am Soc Nephrol 8(2):299–312
Cavalier E, Delanaye P, Vranken L et al (2012) Interpretation of serum PTH concentrations with different kits in dialysis patients according to the KDIGO guidelines: importance of the reference (normal) values. Nephrol Dial Transplant 27(5):1950–1956
Gallieni M, Cucciniello E, D’Amaro E et al (2002) Calcium, phosphate, and PTH levels in the hemodialysis population: a multicenter study. J Nephrol 15(2):165–170
Feroze U, Molnar MZ, Dukkipati R, Kovesdy CP, Kalantar-Zadeh K (2011) Insights into nutritional and inflammatory aspects of low parathyroid hormone in dialysis patients. J Ren Nutr 21(1):100–104
Schillie SF, Spradling PR, Murphy TV (2012) Immune response of hepatitis B vaccine among persons with diabetes: a systematic review of the literature. Diabetes Care 35(12):2690–2697
Stern LJ, Calvo-Calle JM (2009) HLA-DR: molecular insights and vaccine design. Curr Pharm Des 15(28):3249–3261
Mert G, Sengul A, Gul HC, Karakas A, Eyigun CP (2014) The role of human leukocyte antigen tissue groups in hepatitis B virus vaccination in Turkey. J Microbiol Immunol Infect 47(1):9–14
Kruskall MS, Alper CA, Awdeh Z, Yunis EJ, Marcus-Bagley D (1992) The immune response to hepatitis B vaccine in humans: inheritance patterns in families. J Exp Med 175(2):495–502
Singh R, Kaul R, Kaul A, Khan K (2007) A comparative review of HLA associations with hepatitis B and C viral infections across global populations. World J Gastroenterol 13(12):1770–1787
Rubinow KB, Rubinow DR (2017) In immune defense: redefining the role of the immune system in chronic disease. Dialogues Clin Neurosci 19(1):19–26
Fabrizi F, Dixit V, Messa P, Martin P (2012) Hepatitis B virus vaccine in chronic kidney disease: improved immunogenicity by adjuvants? A meta-analysis of randomized trials. Vaccine 30(13):2295–2300
Fabrizi F, Dixit V, Messa P, Martin P (2011) Intradermal vs intramuscular vaccine against hepatitis B infection in dialysis patients: a meta-analysis of randomized trials. J Viral Hepat 18(10):730–737
Imam MH (2017) The accelerated hepatitis B virus vaccination schedule among hemodialysis patients, does it work? A randomized controlled trial. J Nephrol 30(6):803–809
Jackson S, Lentino J, Kopp J et al (2018) Immunogenicity of a two-dose investigational hepatitis B vaccine, HBsAg-1018, using a toll-like receptor 9 agonist adjuvant compared with a licensed hepatitis B vaccine in adults. Vaccine 36(5):668–674
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The authors thank the staff of the medical library of the Faculty of Medicine at Chulalongkorn University, Bangkok, Thailand. The librarians provided support by obtaining the original articles for the purpose of the systematic review.
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Suwasin Udomkarnjananun, M.D.; suwasin.u@gmail.com: first author, study design, review of citations and articles, manuscript preparation and draft. Kullaya Takkavatakarn, M.D.; koykullaya@hotmail.com: review of citations and articles. Kearkiat Praditpornsilpa, M.D.; kearkiat@hotmail.com: study design. Claudia Nader, M.D.; Claudia.nader@steward.org: manuscript review and edits. Somchai Eiam-Ong, M.D.; somchai80754@yahoo.com: manuscript review and edits. Bertrand L. Jaber, M.D., M.S.; bertrand.Jaber@steward.org: study design, manuscript review and edits. Paweena Susantitaphong, M.D., Ph.D.; pesancerinus@hotmail.com: corresponding author, review of citations and articles, study design, manuscript review and edits.
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Udomkarnjananun, S., Takkavatakarn, K., Praditpornsilpa, K. et al. Hepatitis B virus vaccine immune response and mortality in dialysis patients: a meta-analysis. J Nephrol 33, 343–354 (2020). https://doi.org/10.1007/s40620-019-00668-1
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DOI: https://doi.org/10.1007/s40620-019-00668-1