Advertisement

Hepatitis B virus vaccine immune response and mortality in dialysis patients: a meta-analysis

  • Suwasin Udomkarnjananun
  • Kullaya Takkavatakarn
  • Kearkiat Praditpornsilpa
  • Claudia Nader
  • Somchai Eiam-Ong
  • Bertrand L. Jaber
  • Paweena SusantitaphongEmail author
Original Article
  • 12 Downloads

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.

Keywords

Systematic review Meta-analysis HBV vaccine Seroresponsiveness Dialysis Mortality 

Notes

Acknowledgements

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.

Author contributions

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.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest related to this article. The results presented in this paper have not been published previously in whole or part, except in abstract format.

Ethical approval

The Institutional Review Board of the Faculty of Medicine, Chulalongkorn University, Bangkok, Thailand, has exempted this study in compliance with the International guidelines for human research protection as Declaration of Helsinki, The Belmont Report, CIOMS Guideline, International Conference on Harmonization in Good Clinical Practice (ICP-GCP) and 45CFR 46.101(b). (IRB No. 432/62).

Human/animal rights statement

This study did not directly involve with human participants or animal subjects.

Supplementary material

40620_2019_668_MOESM1_ESM.docx (192 kb)
Supplementary material 1 (DOCX 192 kb)

References

  1. 1.
    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):638–643PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Di Bisceglie AM (2009) Hepatitis B and hepatocellular carcinoma. Hepatology 49(5 Suppl):S56–S60PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Polaris Observatory Collaborators (2018) Global prevalence, treatment, and prevention of hepatitis B virus infection in 2016: a modelling study. Lancet Gastroenterol Hepatol 3(6):383–403CrossRefGoogle Scholar
  4. 4.
    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):1325PubMedCrossRefPubMedCentralGoogle Scholar
  5. 5.
    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):e0150499PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Namgyal P (2003) Impact of hepatitis B immunization, Europe and worldwide. J Hepatol 39(Suppl 1):S77–S82PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    Fabrizi F, Martin P (2000) Hepatitis B virus infection in dialysis patients. Am J Nephrol 20(1):1–11PubMedCrossRefPubMedCentralGoogle Scholar
  8. 8.
    Courouce AM, Jungers P, Benhamou E, Laplanche A, Crosnier J (1984) Hepatitis B vaccine in dialysis patients. N Engl J Med 311(23):1515–1516PubMedCrossRefPubMedCentralGoogle Scholar
  9. 9.
    Cohen G, Horl WH (2012) Immune dysfunction in uremia-an update. Toxins (Basel) 4(11):962–990CrossRefGoogle Scholar
  10. 10.
    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):1526–1533PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Geerlings SE, Hoepelman AI (1999) Immune dysfunction in patients with diabetes mellitus (DM). FEMS Immunol Med Microbiol 26(3–4):259–265PubMedCrossRefPubMedCentralGoogle Scholar
  12. 12.
    Lord JM (2013) The effect of ageing of the immune system on vaccination responses. Hum Vaccine Immunother 9(6):1364–1367CrossRefGoogle Scholar
  13. 13.
    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):815–821PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    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):1053–1062PubMedCrossRefPubMedCentralGoogle Scholar
  15. 15.
    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):2615–2617PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    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):239–245PubMedCrossRefPubMedCentralGoogle Scholar
  17. 17.
    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–S160PubMedPubMedCentralGoogle Scholar
  18. 18.
    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):814–820PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    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):97PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    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:b2700PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    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):136–143PubMedPubMedCentralGoogle Scholar
  22. 22.
    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):1080–1088PubMedPubMedCentralGoogle Scholar
  23. 23.
    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):497–506PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    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):344–349CrossRefGoogle Scholar
  25. 25.
    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):27–30PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Walz G, Kunzendorf U, Haller H et al (1989) Factors influencing the response to hepatitis B vaccination of hemodialysis patients. Nephron 51(4):474–477PubMedCrossRefPubMedCentralGoogle Scholar
  27. 27.
    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):385–387PubMedCrossRefPubMedCentralGoogle Scholar
  28. 28.
    Fleming SJ, Moran DM, Cooksley WG, Faoagali JL (1991) Poor response to a recombinant hepatitis B vaccine in dialysis patients. J Infect 22(3):251–257PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    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):121–128PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Lombardi M, Pizzarelli F, Righi M et al (1992) Hepatitis B vaccination in dialysis patients and nutritional status. Nephron 61(3):266–268PubMedCrossRefGoogle Scholar
  31. 31.
    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):60–65PubMedCrossRefGoogle Scholar
  32. 32.
    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):1930–1934PubMedGoogle Scholar
  33. 33.
    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 12:315–317PubMedGoogle Scholar
  34. 34.
    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):536–543PubMedCrossRefGoogle Scholar
  35. 35.
    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):1559–1563PubMedCrossRefGoogle Scholar
  36. 36.
    Khan AN, Bernardini J, Rault RM, Piraino B (1996) Low seroconversion with hepatitis B vaccination in peritoneal dialysis patients. Perit Dial Int 16(4):370–373PubMedPubMedCentralGoogle Scholar
  37. 37.
    Mitwalli A (1996) Responsiveness to hepatitis b vaccine in immunocompromised patients by doubling the dose scheduling. Nephron 73(3):417–420PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    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):95–97PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    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):629–636PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    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):1982–1987PubMedCrossRefGoogle Scholar
  41. 41.
    Kovacic V, Sain M, Vukman V (2002) Efficient haemodialysis improves the response to hepatitis B virus vaccination. Intervirology 45(3):172–176PubMedCrossRefGoogle Scholar
  42. 42.
    Chin AI (2003) Hepatitis B virus vaccine response in hemodialysis: baseline patient characteristics. Hemodial Int 7(4):296–303PubMedCrossRefGoogle Scholar
  43. 43.
    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):3963–3967PubMedCrossRefGoogle Scholar
  44. 44.
    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–c72PubMedCrossRefGoogle Scholar
  45. 45.
    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):1136–1141PubMedCrossRefGoogle Scholar
  46. 46.
    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):3957–3960PubMedCrossRefGoogle Scholar
  47. 47.
    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):242–245PubMedCrossRefGoogle Scholar
  48. 48.
    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–c93PubMedCrossRefGoogle Scholar
  49. 49.
    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):1953–1957PubMedPubMedCentralGoogle Scholar
  50. 50.
    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):15–19Google Scholar
  51. 51.
    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):65–71PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Ramezani A, Velayati AA, Eslamifar A et al (2008) Persistence of hepatitis B vaccine immunity in hemodialysis patients. Ther Apher Dial 12(2):143–146PubMedCrossRefGoogle Scholar
  53. 53.
    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):798–803PubMedGoogle Scholar
  54. 54.
    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):5865–5869PubMedCrossRefGoogle Scholar
  55. 55.
    Bock M, Barros E, Veronese FJ (2009) Hepatitis B vaccination in haemodialysis patients: a randomized clinical trial. Nephrology (Carlton). 14(3):267–272PubMedCrossRefGoogle Scholar
  56. 56.
    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):415–420PubMedGoogle Scholar
  57. 57.
    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):394–397PubMedCrossRefGoogle Scholar
  58. 58.
    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):2303–2309PubMedCrossRefGoogle Scholar
  59. 59.
    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):276–279PubMedCrossRefGoogle Scholar
  60. 60.
    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):9618–9623PubMedCrossRefGoogle Scholar
  61. 61.
    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):1559–1562PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    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):1501–1506PubMedCrossRefGoogle Scholar
  63. 63.
    Afsar B (2013) The relationship between erythropoietin resistance and antibody response to hepatitis B vaccine in hemodialysis patients. Nephrourol Mon 5(3):806–812PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    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):185–191CrossRefGoogle Scholar
  65. 65.
    Ayub MA, Bacci MR, Fonseca FL, Chehter EZ (2014) Hemodialysis and hepatitis B vaccination: a challenge to physicians. Int J Gen Med 7:109–114PubMedGoogle Scholar
  66. 66.
    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):315–318PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    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):584–592PubMedCrossRefGoogle Scholar
  68. 68.
    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):567–573PubMedCrossRefGoogle Scholar
  69. 69.
    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):1063–1074PubMedCrossRefGoogle Scholar
  70. 70.
    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):67–71PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Almueilo SH (2017) Evaluation of response to hepatitis B vaccination in chronic hemodialysis patients. Saudi J Med Med Sci 5(3):218–223PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Asan A, Demirhan H, Sorkun HC et al (2017) Factors affecting responsiveness to hepatitis B immunization in dialysis patients. Int Urol Nephrol 49(10):1845–1850PubMedCrossRefPubMedCentralGoogle Scholar
  73. 73.
    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):27–37PubMedPubMedCentralGoogle Scholar
  74. 74.
    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):141–145PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    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 42:5–8PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    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):557–562CrossRefGoogle Scholar
  77. 77.
    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):151–158PubMedCrossRefPubMedCentralGoogle Scholar
  78. 78.
    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):947–953PubMedCrossRefGoogle Scholar
  79. 79.
    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):791–796Google Scholar
  80. 80.
    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):530–536PubMedCrossRefPubMedCentralGoogle Scholar
  81. 81.
    Higgins JP, Altman DG, Gotzsche PC et al (2011) The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ 343:d5928PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    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):1–7PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    Lisowska-Myjak B (2014) Uremic toxins and their effects on multiple organ systems. Nephron Clin Pract 128(3–4):303–311PubMedCrossRefPubMedCentralGoogle Scholar
  84. 84.
    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):e73141PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Vaziri ND, Pahl MV, Crum A, Norris K (2012) Effect of uremia on structure and function of immune system. J Ren Nutr 22(1):149–156PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    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):717–722PubMedCrossRefPubMedCentralGoogle Scholar
  87. 87.
    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):2807–2810PubMedCrossRefPubMedCentralGoogle Scholar
  88. 88.
    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–S205PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    Janus N, Vacher L-V, Karie S, Ledneva E, Deray G (2007) Vaccination and chronic kidney disease. Nephrol Dial Transplant 23(3):800–807PubMedCrossRefPubMedCentralGoogle Scholar
  90. 90.
    Alwarawrah Y, Kiernan K, MacIver NJ (2018) Changes in nutritional status impact immune cell metabolism and function. Front Immunol 9:1055PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Sayarlioglu H, Erkoc R, Demir C et al (2006) Nutritional status and immune functions in maintenance hemodialysis patients. Mediat Inflamm 2006(1):20264Google Scholar
  92. 92.
    Prendergast AJ (2015) Malnutrition and vaccination in developing countries. Philos Trans R Soc Lond B Biol Sci 370(1671):20140141PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    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):45–51PubMedCrossRefPubMedCentralGoogle Scholar
  94. 94.
    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):113–119PubMedCrossRefPubMedCentralGoogle Scholar
  95. 95.
    Schulman G (2004) The dose of dialysis in hemodialysis patients: impact on nutrition. Semin Dial 17(6):479–488PubMedCrossRefPubMedCentralGoogle Scholar
  96. 96.
    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):250–257Google Scholar
  97. 97.
    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) PubMedPubMedCentralGoogle Scholar
  98. 98.
    Montecino-Rodriguez E, Berent-Maoz B, Dorshkind K (2013) Causes, consequences, and reversal of immune system aging. J Clin Investig 123(3):958–965PubMedCrossRefPubMedCentralGoogle Scholar
  99. 99.
    Goronzy JJ, Weyand CM (2013) Understanding immunosenescence to improve responses to vaccines. Nat Immunol 14(5):428–436PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    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):9825PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Lee SK, Ding JL (2013) A perspective on the role of extracellular hemoglobin on the innate immune system. DNA Cell Biol 32(2):36–40PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    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):579–583PubMedCrossRefPubMedCentralGoogle Scholar
  103. 103.
    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):1339–1346PubMedCrossRefPubMedCentralGoogle Scholar
  104. 104.
    Bishlawy IM (1999) Red blood cells, hemoglobin and the immune system. Med Hypotheses 53(4):345–346PubMedCrossRefPubMedCentralGoogle Scholar
  105. 105.
    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):1–59Google Scholar
  106. 106.
    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 CrossRefGoogle Scholar
  107. 107.
    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):332–336PubMedCrossRefPubMedCentralGoogle Scholar
  108. 108.
    Shurtz-Swirski R, Shkolnik T, Shasha SM (1995) Parathyroid hormone and the cellular immune system. Nephron 70(1):21–24PubMedCrossRefPubMedCentralGoogle Scholar
  109. 109.
    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):299–312PubMedCrossRefPubMedCentralGoogle Scholar
  110. 110.
    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):1950–1956PubMedCrossRefPubMedCentralGoogle Scholar
  111. 111.
    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):165–170PubMedPubMedCentralGoogle Scholar
  112. 112.
    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):100–104PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    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):2690–2697PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Stern LJ, Calvo-Calle JM (2009) HLA-DR: molecular insights and vaccine design. Curr Pharm Des 15(28):3249–3261PubMedPubMedCentralCrossRefGoogle Scholar
  115. 115.
    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):9–14PubMedCrossRefPubMedCentralGoogle Scholar
  116. 116.
    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):495–502PubMedCrossRefPubMedCentralGoogle Scholar
  117. 117.
    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):1770–1787PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Rubinow KB, Rubinow DR (2017) In immune defense: redefining the role of the immune system in chronic disease. Dialogues Clin Neurosci 19(1):19–26PubMedPubMedCentralGoogle Scholar
  119. 119.
    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):2295–2300PubMedCrossRefPubMedCentralGoogle Scholar
  120. 120.
    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):730–737PubMedCrossRefPubMedCentralGoogle Scholar
  121. 121.
    Imam MH (2017) The accelerated hepatitis B virus vaccination schedule among hemodialysis patients, does it work? A randomized controlled trial. J Nephrol 30(6):803–809PubMedCrossRefPubMedCentralGoogle Scholar
  122. 122.
    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):668–674PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Italian Society of Nephrology 2019

Authors and Affiliations

  1. 1.Division of Nephrology, Department of Medicine, Faculty of Medicine, King Chulalongkorn Memorial HospitalChulalongkorn UniversityBangkokThailand
  2. 2.Department of MedicineSt. Elizabeth’s Medical CenterBostonUSA
  3. 3.Department of MedicineTufts University School of MedicineBostonUSA
  4. 4.Research Unit for Metabolic Bone Disease in CKD Patients, Faculty of MedicineChulalongkorn UniversityBangkokThailand

Personalised recommendations