Overview of Hepatitis B Vaccine Non-Response and Associated B Cell Amnesia: A Sco** Review
Abstract
:1. Introduction
2. Methods
2.1. Search
2.2. Eligibility Criteria
3. Results
3.1. Hepatitis B Vaccine Non-Response Prevalence and Risk Factors
3.1.1. Chronic Hepatitis C
3.1.2. Chronic Kidney Disease (CKD) and Haemodialysis
3.1.3. Celiac Disease
3.1.4. Latent HBV Infection
3.1.5. Inflammatory Bowel Disease
3.1.6. Other Conditions
3.2. Mechanisms Involved in Hepatitis B Vaccine Non-Response
3.2.1. Pattern Recognition Receptors
3.2.2. Involvement of Helper T Cells (Th)
3.2.3. The Role of Regulatory B Cells
3.3. Genetic Variation in Hepatitis B Vaccine Non-Response
3.3.1. Antigen Processing and Presentation Genes
3.3.2. T Cell Regulation Genes
3.3.3. Genetic Polymorphism in Markers of the Immune System
3.4. B Cell Amnesia-Associated Hepatitis B Vaccination Non-Response
3.5. Strategies in Addressing HBV Non-Response
3.5.1. Revaccination/Booster Dose
3.5.2. Use of Intradermal Route for Vaccine Administration
3.5.3. Use of Adjuvants
3.5.4. Strategies in Chronic Kidney Disease (CKD) Patients
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- WHO. Global Progress Report on HIV, Viral Hepatitis and Sexually Transmitted Infections, 2021: Accountability for the Global Health Sector Strategies 2016–2021: Actions for Impact; World Health Organization: Geneva, Switzerland, 2021.
- Li, Q.; Cao, M.; Lei, L.; Yang, F.; Li, H.; Yan, X.; He, S.; Zhang, S.; Teng, Y.; **, W. The effects of TLR3 up-regulation on Th1/Th2 cytokines in CBMCs of infants with non/hypo response to hepatitis B vaccine. Chin. J. Diseas Control. Prev. 2020, 24, 711–715. [Google Scholar]
- Wu, L.; Fu, G.; Xu, X.; Yi, L.; Yao, T.; Wan, H.; Li, J.; Wang, B.; Feng, S.; Feng, Y. Decreased placental TLR3 is associated with hepatitis B virus vaccine responsiveness in infants born to HBsAg-positive mothers. Transl. Pediatr. 2023, 12, 1204. [Google Scholar] [CrossRef]
- Smolnikova, M.V.; Tereshchenko, S.Y. Proteins of the lectin pathway of the complement system activation: Immunobiological functions, genetics and involvement in the pathogenesis of human diseases. Russ. J. Infect. Immun. 2022, 12, 209–221. [Google Scholar] [CrossRef]
- Chong, W.P.; To, Y.F.; Ip, W.K.; Yuen, M.F.; Poon, T.P.; Wong, W.H.; Lai, C.L.; Lau, Y.L. Mannose-binding lectin in chronic hepatitis B virus infection. Hepatology 2005, 42, 1037–1045. [Google Scholar] [CrossRef]
- Tong, H.V.; Toan, N.L.; Song, L.H.; Ouf, E.A.; Bock, C.-T.; Kremsner, P.G.; Kun, J.F.; TP, V. Ficolin-2 levels and FCN2 haplotypes influence hepatitis B infection outcome in Vietnamese patients. PLoS ONE 2011, 6, e28113. [Google Scholar] [CrossRef]
- Xu, H.-d.; Zhao, M.-f.; Wan, T.-h.; Song, G.-z.; He, J.-l.; Chen, Z. Association between Mannose-binding lectin gene polymorphisms and hepatitis B virus infection: A meta-analysis. PLoS ONE 2013, 8, e75371. [Google Scholar] [CrossRef]
- Ruseva, M.; Kolev, M.; Dagnaes-Hansen, F.; Hansen, S.B.; Takahashi, K.; Ezekowitz, A.; Thiel, S.; Jensenius, J.C.; Gadjeva, M. Mannan-binding lectin deficiency modulates the humoral immune response dependent on the genetic environment. Immunology 2009, 127, 279–288. [Google Scholar] [CrossRef]
- Davila, S.; Froeling, F.; Tan, A.; Bonnard, C.; Boland, G.; Snippe, H.; Hibberd, M.; Seielstad, M. New genetic associations detected in a host response study to hepatitis B vaccine. Genes Immun. 2010, 11, 232–238. [Google Scholar] [CrossRef] [PubMed]
- Fourati, S.; Cristescu, R.; Loboda, A.; Talla, A.; Filali, A.; Railkar, R.; Schaeffer, A.K.; Favre, D.; Gagnon, D.; Peretz, Y. Pre-vaccination inflammation and B-cell signalling predict age-related hyporesponse to hepatitis B vaccination. Nat. Commun. 2016, 7, 10369. [Google Scholar] [CrossRef]
- Böcher, W.O.; Herzog-Hauff, S.; Schlaak, J.; zum Büschenfelde, K.-H.M.; Löhr, H.F. Kinetics of Hepatitis B Surface Antigen-Specific Immune Responses in Acute and Chronic Hepatitis B or After Hbs Vaccination: Stimulation of The In Vitro Antibody Response by Interferon Gamma. Hepatology 1999, 29, 238–244. [Google Scholar] [CrossRef] [PubMed]
- Crotty, S. T follicular helper cell differentiation, function, and roles in disease. Immunity 2014, 41, 529–542. [Google Scholar] [CrossRef] [PubMed]
- Doedée, A.; Kannegieter, N.; Öztürk, K.; van Loveren, H.; Janssen, R.; Buisman, A.-M. Higher numbers of memory B-cells and Th2-cytokine skewing in high responders to hepatitis B vaccination. Vaccine 2016, 34, 2281–2289. [Google Scholar] [CrossRef]
- Pan, L.; Zhang, W.; Liang, Z.; Wu, X.; Zhu, X.; Li, J.; Li, T.; Wang, L.; Li, H.; Liu, Y. Association between polymorphisms of the cytokine and cytokine receptor genes and immune response to hepatitis B vaccination in a Chinese Han population. J. Med. Virol. 2012, 84, 26–33. [Google Scholar] [CrossRef]
- Kardar, G.; Jeddi-Tehrani, M.; Shokri, F. Diminished Th1 and Th2 cytokine production in healthy adult nonresponders to recombinant hepatitis B vaccine. Scand. J. Immunol. 2002, 55, 311–314. [Google Scholar] [CrossRef]
- Sabry, R.; Mohamed, Z.A.Z.; Abdallah, A.M. Relationship between Th1 and Th2 cytokine serum levels and immune response to Hepatitis B vaccination among Egyptian health care workers. J. Immunoass. Immunochem. 2018, 39, 496–508. [Google Scholar] [CrossRef]
- Honorati, M.C.; Dolzani, P.; Mariani, E.; Piacentini, A.; Lisignoli, G.; Ferrari, C.; Facchini, A. Epitope specificity of Th0/Th2 CD4+ T-lymphocyte clones induced by vaccination with rHBsAg vaccine. Gastroenterology 1997, 112, 2017–2027. [Google Scholar] [CrossRef] [PubMed]
- Wataya, M.; Sano, T.; Kamikawaji, N.; Tana, T.; Yamamoto, K.; Sasazuki, T. Comparative analysis of HLA restriction and cytokine production in hepatitis B surface antigen-specific T cells from low-and high-antibody responders in vaccinated humans. J. Hum. Genet. 2001, 46, 197–206. [Google Scholar] [CrossRef] [PubMed]
- Velu, V.; Saravanan, S.; Nandakumar, S.; Shankar, E.M.; Vengatesan, A.; Jadhav, S.S.; Kulkarni, P.S.; Thyagarajan, S.P. Relationship between T-lymphocyte cytokine levels and sero-response to hepatitis B vaccines. World J. Gastroenterol. 2008, 14, 3534. [Google Scholar] [CrossRef] [PubMed]
- Jogdand, G.M.; Mohanty, S.; Devadas, S. Regulators of Tfh cell differentiation. Front. Immunol. 2016, 7, 520. [Google Scholar] [CrossRef] [PubMed]
- Sage, P.T.; Sharpe, A.H. T follicular regulatory cells in the regulation of B cell responses. Trends Immunol. 2015, 36, 410–418. [Google Scholar] [CrossRef] [PubMed]
- Chevalier, N.; Jarrossay, D.; Ho, E.; Avery, D.T.; Ma, C.S.; Yu, D.; Sallusto, F.; Tangye, S.G.; Mackay, C.R. CXCR5 expressing human central memory CD4 T cells and their relevance for humoral immune responses. J. Immunol. 2011, 186, 5556–5568. [Google Scholar] [CrossRef] [PubMed]
- Morita, R.; Schmitt, N.; Bentebibel, S.-E.; Ranganathan, R.; Bourdery, L.; Zurawski, G.; Foucat, E.; Dullaers, M.; Oh, S.; Sabzghabaei, N. Human blood CXCR5+ CD4+ T cells are counterparts of T follicular cells and contain specific subsets that differentially support antibody secretion. Immunity 2011, 34, 108–121. [Google Scholar] [CrossRef]
- Bentebibel, S.-E.; Khurana, S.; Schmitt, N.; Kurup, P.; Mueller, C.; Obermoser, G.; Palucka, A.K.; Albrecht, R.A.; Garcia-Sastre, A.; Golding, H. ICOS+ PD-1+ CXCR3+ T follicular helper cells contribute to the generation of high-avidity antibodies following influenza vaccination. Sci. Rep. 2016, 6, 26494. [Google Scholar] [CrossRef] [PubMed]
- Xu, X.; Li, Y.; Liang, Y.; Yin, M.; Yu, Z.; Zhang, Y.; Huang, L.; Ni, J. MiR-18a and miR-17 are positively correlated with circulating PD-1+ICOS+ follicular helper T cells after hepatitis B vaccination in a chinese population. BMC Immunol. 2018, 19, 25. [Google Scholar] [CrossRef]
- Aghbash, P.S.; Hemmat, N.; Nahand, J.S.; Shamekh, A.; Memar, M.Y.; Babaei, A.; Baghi, H.B. The role of Th17 cells in viral infections. Int. Immunopharmacol. 2021, 91, 107331. [Google Scholar] [CrossRef]
- Mills, K.H. IL-17 and IL-17-producing cells in protection versus pathology. Nat. Rev. Immunol. 2023, 23, 38–54. [Google Scholar] [CrossRef]
- Zhang, Y.; Cobleigh, M.A.; Lian, J.Q.; Huang, C.X.; Booth, C.J.; Bai, X.F.; Robek, M.D. A proinflammatory role for interleukin-22 in the immune response to hepatitis B virus. Gastroenterology 2011, 141, 1897–1906. [Google Scholar] [CrossRef]
- Pati, N.T.; Hissar, S.; Agrawal, K.; Rani, R.; Sarin, S.K. Decrease in CD4+ T lymphocyte proliferation responses and enhanced CD150 cell expression in health care workers non-responsive to HBV vaccine. Vaccine 2007, 25, 1848–1855. [Google Scholar] [CrossRef]
- Lu, L.-R.; Wang, X.-Y.; Li, D.-C.; Huang, Z.-L.; Liu, J.; Lin, C.-S. A preliminary study of CD150 expression in responders and non-responders to the Hepatitis B vaccine. Biomed. Res. 2014, 25, 149–152. [Google Scholar]
- Borzooy, Z.; Streinu-Cercel, A.; Mirshafiey, A.; Khamseh, A.; Mahmoudie, M.K.; Navabi, S.S.; Nosrati, M.; Najafi, Z.; Hosseini, M.; Jazayeri, S.M. IL-17 and IL-22 genetic polymorphisms in HBV vaccine non-and low-responders among healthcare workers. Germs 2016, 6, 14. [Google Scholar] [CrossRef]
- Hsiao, H.-W.; Liu, W.-H.; Wang, C.-J.; Lo, Y.-H.; Wu, Y.-H.; Jiang, S.-T.; Lai, M.-Z. Deltex1 is a target of the transcription factor NFAT that promotes T cell anergy. Immunity 2009, 31, 72–83. [Google Scholar] [CrossRef]
- **e, B.; Zhang, P.; Liu, M.; Zeng, W.; Yang, J.; Liu, H. Deltex1 Polymorphisms Are Associated with Hepatitis B Vaccination Non-Response in Southwest China. PLoS ONE 2016, 11, e0149199. [Google Scholar] [CrossRef]
- Zhang, X.; Sun, X.; Li, M.; Zhou, Z.; Gao, Y. A promoter polymorphism (rs3806798) of interleukin-15 gene is associated with chronic hepatitis B virus infection in the C hinese H an population. Int. J. Immunogenet. 2014, 41, 298–305. [Google Scholar] [CrossRef]
- Chekol Abebe, E.; Asmamaw Dejenie, T.; Mengie Ayele, T.; Dagnew Baye, N.; Agegnehu Teshome, A.; Tilahun Muche, Z. The role of regulatory B cells in health and diseases: A systemic review. J. Inflamm. Res. 2021, 2021, 75–84. [Google Scholar] [CrossRef] [PubMed]
- Rosser, E.C.; Blair, P.A.; Mauri, C. Cellular targets of regulatory B cell-mediated suppression. Mol. Immunol. 2014, 62, 296–304. [Google Scholar] [CrossRef] [PubMed]
- Yang, M.; Rui, K.; Wang, S.; Lu, L. Regulatory B cells in autoimmune diseases. Cell. Mol. Immunol. 2013, 10, 122–132. [Google Scholar] [CrossRef]
- Bolther, M.; Andersen, K.L.D.; Tolstrup, M.; Visvanathan, K.; Woolley, I.; Skinner, N.; Millen, R.; Warner, N.; Østergaard, L.; Jensen-Fangel, S. Levels of regulatory B cells do not predict serological responses to hepatitis B vaccine. Hum. Vaccines Immunother. 2018, 14, 1483–1488. [Google Scholar] [CrossRef]
- Garner-Spitzer, E.; Wagner, A.; Paulke-Korinek, M.; Kollaritsch, H.; Heinz, F.X.; Redlberger-Fritz, M.; Stiasny, K.; Fischer, G.F.; Kundi, M.; Wiedermann, U. Tick-borne encephalitis (TBE) and hepatitis B nonresponders feature different immunologic mechanisms in response to TBE and influenza vaccination with involvement of regulatory T and B cells and IL-10. J. Immunol. 2013, 191, 2426–2436. [Google Scholar] [CrossRef]
- Körber, N.; Pohl, L.; Weinberger, B.; Grubeck-Loebenstein, B.; Wawer, A.; Knolle, P.A.; Roggendorf, H.; Protzer, U.; Bauer, T. Hepatitis B Vaccine Non-Responders Show Higher Frequencies of CD24highCD38high Regulatory B Cells and Lower Levels of IL-10 Expression Compared to Responders. Front. Immunol. 2021, 12, 713351. [Google Scholar] [CrossRef]
- Posteraro, B.; Pastorino, R.; Di Giannantonio, P.; Ianuale, C.; Amore, R.; Ricciardi, W.; Boccia, S. The link between genetic variation and variability in vaccine responses: Systematic review and meta-analyses. Vaccine 2014, 32, 1661–1669. [Google Scholar] [CrossRef]
- Cardell, K.; Lindblom, B.; Frydén, A. Hepatitis B Vaccination in Relatives to Known Non-Responders: A Family Study; Stockholm University: Stockholm, Sweden, 2009. [Google Scholar]
- Qiu, S.; He, P.; Fang, X.; Tong, H.; Lv, J.; Liu, J.; Zhang, L.; Zhai, X.; Wang, L.; Hu, Z. Significant transcriptome and cytokine changes in hepatitis B vaccine non-responders revealed by genome-wide comparative analysis. Hum. Vaccines Immunother. 2018, 14, 1763–1772. [Google Scholar] [CrossRef]
- **on, Y.; Chen, S.; Chen, R.; Lin, W.; Ni, J. Association between microRNA polymorphisms and humoral immunity to hepatitis B vaccine. Hum. Vaccines Immunother. 2013, 9, 1673–1678. [Google Scholar] [CrossRef]
- Bartholomeus, E.; De Neuter, N.; Meysman, P.; Suls, A.; Keersmaekers, N.; Elias, G.; Jansens, H.; Hens, N.; Smits, E.; Van Tendeloo, V. Transcriptome profiling in blood before and after hepatitis B vaccination shows significant differences in gene expression between responders and non-responders. Vaccine 2018, 36, 6282–6289. [Google Scholar] [CrossRef]
- Loureiro, J.; Ploegh, H.L. Antigen presentation and the ubiquitin-proteasome system in host–pathogen interactions. Adv. Immunol. 2006, 92, 225–305. [Google Scholar] [PubMed]
- Pishesha, N.; Harmand, T.J.; Ploegh, H.L. A guide to antigen processing and presentation. Nat. Rev. Immunol. 2022, 22, 751–764. [Google Scholar] [CrossRef] [PubMed]
- Berry, A.; Kapelus, D.; Singh, P.; Groome, M.; de Assis Rosa, D. ABO blood types, but not Secretor or Lewis blood types, influence strength of antibody response to Hepatitis B vaccine in Black South African children. Vaccine 2023, 41, 3617–3626. [Google Scholar] [CrossRef]
- Alper, C.A.; Kruskall, M.S.; Marcus-Bagley, D.; Craven, D.E.; Katz, A.J.; Brink, S.J.; Dienstag, J.L.; Awdeh, Z.; Yunis, E.J. Genetic Prediction of Nonresponse to Hepatitis B Vaccine. New Engl. J. Med. 1989, 321, 708–712. [Google Scholar] [CrossRef]
- Zhao, M.; Wang, C.; Li, P.; Sun, T.; Wang, J.; Zhang, S.; Ma, Q.; Ma, F.; Shi, W.; Shi, M. Single-cell RNA sequencing reveals the transcriptomic characteristics of peripheral blood mononuclear cells in hepatitis B vaccine non-responders. Front. Immunol. 2023, 14, 1091237. [Google Scholar] [CrossRef]
- Lin, H.H.; Liao, H.W.; Lin, S.K.; Wang, L.Y. HLA and response to booster hepatitis B vaccination in anti-HBs-seronegative adolescents who had received primary infantile vaccination. Vaccine 2008, 26, 3414–3420. [Google Scholar] [CrossRef]
- Wang, L.-Y.; Chen, C.-F.; Wu, T.-W.; Lai, S.-K.; Chu, C.-C.; Lin, H.H. Response to hepatitis B vaccination is co-determined by HLA-DPA1 and-DPB1. Vaccine 2019, 37, 6435–6440. [Google Scholar] [CrossRef]
- Li, Z.-K.; Nie, J.-J.; Li, J.; Zhuang, H. The effect of HLA on immunological response to hepatitis B vaccine in healthy people: A meta-analysis. Vaccine 2013, 31, 4355–4361. [Google Scholar] [CrossRef]
- Mineta, M.; Tanimura, M.; Tana, T.; Yssel, H.; Kashiwagi, S.; Sasazuki, T. Contribution of HLA class I and class II alleles to the regulation of antibody production to hepatitis B surface antigen in humans. Int. Immunol. 1996, 8, 525–531. [Google Scholar] [CrossRef]
- Wang, C.; Tang, J.; Song, W.; Lobashevsky, E.; Wilson, C.M.; Kaslow, R.A. HLA and cytokine gene polymorphisms are independently associated with responses to hepatitis B vaccination. Hepatology 2004, 39, 978–988. [Google Scholar] [CrossRef]
- Desombere, I.; Willems, A.; Leroux-Roels, G. Response to hepatitis B vaccine: Multiple HLA genes are involved. Tissue Antigens 1998, 51, 593–604. [Google Scholar] [CrossRef] [PubMed]
- Amirzargar, A.A.; Mohseni, N.; Shokrgozar, M.A.; Arjang, Z.; Ahmadi, N.; Yousefi Behzadi, M.; Amanzadeh, A.; Shokri, F. HLA-DRB1, DQA1 and DQB1 Alleles and Hap-lotypes Frequencies in Iranian Healthy Adult Responders and Non-Responders to Recombi-nant Hepatitis B Vaccine. Iran. J. Immunol. 2008, 5, 92–99. [Google Scholar] [PubMed]
- Yoon, J.H.; Shin, S.; won In, J.; Chang, J.Y.; Song, E.Y.; Roh, E.Y. Association of HLA alleles with the responsiveness to hepatitis B virus vaccination in Korean infants. Vaccine 2014, 32, 5638–5644. [Google Scholar] [CrossRef] [PubMed]
- Höhler, T.; Reuss, E.; Evers, N.; Dietrich, E.; Rittner, C.; Freitag, C.M.; Vollmar, J.; Schneider, P.M.; Fimmers, R. Differential genetic determination of immune responsiveness to hepatitis B surface antigen and to hepatitis A virus: A vaccination study in twins. Lancet 2002, 360, 991–995. [Google Scholar] [CrossRef] [PubMed]
- Jilin, Z.; Yuguo, S. The effect of HLA-DRB1 alleles in immune response to hepatitis B vaccine. In Proceedings of the 2011 International Conference on Human Health and Biomedical Engineering, Jilin, China, 19–22 August 2011; pp. 554–557. [Google Scholar]
- Milich, D.R.; Leroux-Roels, G.G. Immunogenetics of the response to HBsAg vaccination. Autoimmun. Rev. 2003, 2, 248–257. [Google Scholar] [CrossRef] [PubMed]
- Sakai, A.; Noguchi, E.; Fukushima, T.; Tagawa, M.; Iwabuchi, A.; Kita, M.; Kakisaka, K.; Miyasaka, A.; Takikawa, Y.; Sumazaki, R. Identification of amino acids in antigen-binding site of class II HLA proteins independently associated with hepatitis B vaccine response. Vaccine 2017, 35, 703–710. [Google Scholar] [CrossRef] [PubMed]
- Höhler, T.; Stradmann-Bellinghausen, B.; Starke, R.; Sänger, R.; Victor, A.; Rittner, C.; Schneider, P.M. C4A deficiency and nonresponse to hepatitis B vaccination. J. Hepatol. 2002, 37, 387–392. [Google Scholar] [CrossRef] [PubMed]
- De Silvestri, A.; Pasi, A.; Martinetti, M.; Belloni, C.; Tinelli, C.; Rondini, G.; Salvaneschi, L.; Cuccia, M. Family study of non-responsiveness to hepatitis B vaccine confirms the importance of HLA class III C4A locus. Genes Immun. 2001, 2, 367–372. [Google Scholar] [CrossRef] [PubMed]
- Xu, B.; Zhu, D.; Bi, Y.; Wang, Y.; Hu, Y.; Zhou, Y.-H. Minimal association of alleles of human leukocyte antigen class II gene and long-term antibody response to hepatitis B vaccine vaccinated during infancy. Vaccine 2017, 35, 2457–2462. [Google Scholar] [CrossRef] [PubMed]
- Wu, T.W.; Chen, C.F.; Lai, S.K.; Lin, H.H.; Chu, C.C.; Wang, L.Y. SNP rs7770370 in HLA-DPB 1 loci as a major genetic determinant of response to booster hepatitis B vaccination: Results of a genome-wide association study. J. Gastroenterol. Hepatol. 2015, 30, 891–899. [Google Scholar] [CrossRef] [PubMed]
- Okada, Y.; Uno, N.; Sato, S.; Mori, S.; Sasaki, D.; Kaku, N.; Kosai, K.; Morinaga, Y.; Hasegawa, H.; Yanagihara, K. Strong influence of human leukocyte antigen-DP variants on response to hepatitis B vaccine in a Japanese population. Vaccine 2017, 35, 5662–5665. [Google Scholar] [CrossRef]
- Yu, L.; Cheng, Y.-j.; Cheng, M.-l.; Yao, Y.-m.; Zhang, Q.; Zhao, X.-k.; Liu, H.-j.; Hu, Y.-x.; Mu, M.; Wang, B. Quantitative assessment of common genetic variations in HLA-DP with hepatitis B virus infection, clearance and hepatocellular carcinoma development. Sci. Rep. 2015, 5, 14933. [Google Scholar] [CrossRef]
- Pan, L.; Zhang, L.; Zhang, W.; Wu, X.; Li, Y.; Yan, B.; Zhu, X.; Liu, X.; Yang, C.; Xu, J. A genome-wide association study identifies polymorphisms in the HLA-DR region associated with non-response to hepatitis B vaccination in Chinese Han populations. Hum. Mol. Genet. 2014, 23, 2210–2219. [Google Scholar] [CrossRef]
- Roh, E.Y.; Yoon, J.H.; In, J.W.; Lee, N.; Shin, S.; Song, E.Y. Association of HLA-DP variants with the responsiveness to Hepatitis B virus vaccination in Korean Infants. Vaccine 2016, 34, 2602–2607. [Google Scholar] [CrossRef]
- Duan, Z.; Chen, X.; Liang, Z.; Zeng, Y.; Zhu, F.; Long, L.; McCrae, M.A.; Zhuang, H.; Shen, T.; Lu, F. Genetic polymorphisms of CXCR5 and CXCL13 are associated with non-responsiveness to the hepatitis B vaccine. Vaccine 2014, 32, 5316–5322. [Google Scholar] [CrossRef]
- Zhuo, Y.; Yang, Y.; Zhang, M.; Xu, Y.; Chen, Z.; Mu, L.; Tang, X.; Zhong, Z.; Chen, J.; Zhou, L. Single nucleotide polymorphisms in IFN-γ signaling pathway associated with risk of hepatitis B virus infection in Chinese children. Can. J. Infect. Dis. Med. Microbiol. 2020, 2020, 8121659. [Google Scholar] [CrossRef]
- Amirpour-Rostami, S.; Kazemi Arababadi, M. IL-18 and IL-1β gene polymorphisms: The plausible risk factors for chronic hepatitis B. Viral Immunol. 2019, 32, 208–213. [Google Scholar] [CrossRef]
- Chen, J.; Liang, Z.; Lu, F.; Fang, X.; Liu, S.; Zeng, Y.; Zhu, F.; Chen, X.; Shen, T.; Li, J. Toll-like receptors and cytokines/cytokine receptors polymorphisms associate with non-response to hepatitis B vaccine. Vaccine 2011, 29, 706–711. [Google Scholar] [CrossRef]
- Çiftdoǧan, D.Y.; Onay, H.; Tosun, S.; Özdemir, T.R.; Özkinay, F.; Vardar, F. IFNG and IFNGR1 gene polymorphisms in children with nonresponse to the hepatitis B vaccine. Future Virol. 2014, 9, 123–130. [Google Scholar] [CrossRef]
- Burton, A.R.; Maini, M.K. Human antiviral B cell responses: Emerging lessons from hepatitis B and COVID-19. Immunol. Rev. 2021, 299, 108–117. [Google Scholar] [CrossRef]
- Pondé, R.A.d.A. Expression and detection of anti-HBs antibodies after hepatitis B virus infection or vaccination in the context of protective immunity. Arch. Virol. 2019, 164, 2645–2658. [Google Scholar] [CrossRef]
- Khodadadi, L.; Cheng, Q.; Radbruch, A.; Hiepe, F. The maintenance of memory plasma cells. Front. Immunol. 2019, 10, 721. [Google Scholar] [CrossRef]
- Van Damme, P.; Dionne, M.; Leroux-Roels, G.; Van Der Meeren, O.; Di Paolo, E.; Salaun, B.; Surya Kiran, P.; Folschweiller, N. Persistence of HB sAg-specific antibodies and immune memory two to three decades after hepatitis B vaccination in adults. J. Viral Hepat. 2019, 26, 1066–1075. [Google Scholar] [CrossRef] [PubMed]
- Rosado, M.M.; Scarsella, M.; Pandolfi, E.; Cascioli, S.; Giorda, E.; Chionne, P.; Madonne, E.; Gesualdo, F.; Romano, M.; Ausiello, C.M. Switched memory B cells maintain specific memory independently of serum antibodies: The hepatitis B example. Eur. J. Immunol. 2011, 41, 1800–1808. [Google Scholar] [CrossRef]
- Samandari, T.; Fiore, A.E.; Negus, S.; Williams, J.L.; Kuhnert, W.; McMahon, B.J.; Bell, B.P. Differences in response to a hepatitis B vaccine booster dose among Alaskan children and adolescents vaccinated during infancy. Pediatrics 2007, 120, e373–e381. [Google Scholar] [CrossRef] [PubMed]
- Coursaget, P.; Leboulleux, D.; Soumare, M.; le Cann, P.; Yvonnet, B.; Chiron, J.-P.; Coll-Seck, A.-M.; Diop-Mar, I. Twelve-year follow-up study of hepatitis B immunization of Senegalese infants. J. Hepatol. 1994, 21, 250–254. [Google Scholar] [CrossRef] [PubMed]
- Zaffina, S.; Marcellini, V.; Santoro, A.P.; Scarsella, M.; Camisa, V.; Vinci, M.R.; Musolino, A.M.; Nicolosi, L.; Rosado, M.M.; Carsetti, R. Repeated vaccinations do not improve specific immune defenses against Hepatitis B in non-responder health care workers. Vaccine 2014, 32, 6902–6910. [Google Scholar] [CrossRef] [PubMed]
- Valats, J.; Tuaillon, E.; Funakoshi, N.; Hoa, D.; Brabet, M.; Bollore, K.; Ducos, J.; Vendrell, J.; Blanc, P. Investigation of memory B cell responses to hepatitis B surface antigen in health care workers considered as non-responders to vaccination. Vaccine 2010, 28, 6411–6416. [Google Scholar] [CrossRef]
- Karimi, S.; Mehdipour, F.; Sarvari, J.; Ataollahi, M.R.; Ramezani, A.; Meri, S.; Kalantar, K. Investigation of the frequencies of various B cell populations in non-responder healthcare workers in comparison with responders to hepatitis B virus vaccination. Trans. R. Soc. Trop. Med. Hyg. 2023, 117, 628–636. [Google Scholar] [CrossRef]
- Zhang, L.; Liu, J.; Lu, J.; Yan, B.; Song, L.; Li, L.; Cui, F.; Zhang, G.; Wang, F.; Liang, X. Antibody response to revaccination among adult non-responders to primary Hepatitis B vaccination in China. Hum. Vaccines Immunother. 2015, 11, 2716–2722. [Google Scholar] [CrossRef]
- Raven, S.F.; Hoebe, C.J.; Vossen, A.C.; Visser, L.G.; Hautvast, J.L.; Roukens, A.H.; van Steenbergen, J.E. Serological response to three alternative series of hepatitis B revaccination (Fendrix, Twinrix, and HBVaxPro-40) in healthy non-responders: A multicentre, open-label, randomised, controlled, superiority trial. Lancet Infect. Dis. 2020, 20, 92–101. [Google Scholar] [CrossRef]
- Hoebe, C.J.; Vermeiren, A.P.; Dukers-Muijrers, N.H. Revaccination with Fendrix® or HBVaxPro® results in better response rates than does revaccination with three doses of Engerix-B® in previous non-responders. Vaccine 2012, 30, 6734–6737. [Google Scholar] [CrossRef]
- Grazzini, M.; Arcangeli, G.; Mucci, N.; Bonanni, P.; Bini, C.; Bechini, A.; Boccalini, S.; Tiscione, E.; Paolini, D. High chance to overcome the non-responder status to hepatitis B vaccine after a further full vaccination course: Results from the extended study on healthcare students and workers in Florence, Italy. Hum. Vaccines Immunother. 2020, 16, 949–954. [Google Scholar] [CrossRef]
- Li, J.; Meng, F.; Zheng, J.; Liang, Q.; Li, H.; Li, J.; Zhang, L.; Gan, J.; Zhu, F. Immune persistence induced by three doses of 60 μg hepatitis B vaccine in non-responders following standard primary vaccination in Chinese adults. Hum. Vaccines Immunother. 2021, 17, 2762–2767. [Google Scholar] [CrossRef] [PubMed]
- Pan, H.-X.; Zeng, Y.; Song, X.-F.; Zhang, Y.-J.; Xu, K.; Liang, Z.-L.; Zhu, F.-C. Immune response to hepatitis B vaccine with high antigen content in non-responders after standard primary vaccination in Chinese adults. Vaccine 2014, 32, 3706–3712. [Google Scholar] [CrossRef] [PubMed]
- Shooshtari, M.H.S.; Makvandi, M.; Rasti, M.; Neisi, N.; Rastegarvand, N.; Pouremamali, A.; Haj, M.S.; Ghaedi, F. Evaluation of hepatitis B surface antibody and specific gamma interferon response in health care workers after vaccination. Jundishapur J. Microbiol. 2015, 8, e13801. [Google Scholar] [CrossRef] [PubMed]
- Saraceni, C.; Birk, J. A review of hepatitis B virus and hepatitis C virus immunopathogenesis. J. Clin. Transl. Hepatol. 2021, 9, 409. [Google Scholar] [CrossRef] [PubMed]
- Fabrizi, F.; Cerutti, R.; Dixit, V.; Ridruejo, E. Hepatitis B virus vaccine and chronic kidney disease. The advances. Nefrologia 2021, 41, 115–122. [Google Scholar] [CrossRef] [PubMed]
- Koc, Ö.M.; Damoiseaux, J.; van Loo, I.H.; Masquillier, H.I.; Lashof, A.M.O. Case report of delayed seroprotection rather than non-response after primary three-dose hepatitis B vaccination. Vaccine 2020, 38, 112–114. [Google Scholar] [CrossRef] [PubMed]
- Madhavan, A.; Palappallil, D.S.; Balakrishnapanicker, J.; Asokan, A. Immune response to hepatitis B vaccine: An evaluation. Perspect. Clin. Res. 2021, 12, 209. [Google Scholar] [PubMed]
- Hanif, F.; Mehmood, N.; Majid, Z.; Luck, N.; Laeeq, S.; Tasneem, A.; Ul Haque, M. Successful response of intradermal hepatitis B vaccine in nonresponders of intramuscular hepatitis B vaccine in general and hemodialysis population. Saudi J. Gastroenterol. 2020, 26, 306–311. [Google Scholar] [CrossRef]
- Leonardi, S.; Praticò, A.D.; Lionetti, E.; Spina, M.; Vitaliti, G.; La Rosa, M. Intramuscular vs intradermal route for hepatitis B booster vaccine in celiac children. World J. Gastroenterol. 2012, 18, 5729. [Google Scholar] [CrossRef]
- Dhillon, S.; Moore, C.; Li, S.; Aziz, A.; Kakar, A.; Dosanjh, A.; Beesla, A.; Murphy, L.; Van Thiel, D. Efficacy of high-dose intra-dermal hepatitis B virus vaccine in previous vaccination non-responders with chronic liver disease. Dig. Dis. Sci. 2012, 57, 215–220. [Google Scholar] [CrossRef] [PubMed]
- Filippelli, M.; Lionetti, E.; Gennaro, A.; Lanzafame, A.; Arrigo, T.; Salpietro, C.; La Rosa, M.; Leonardi, S. Hepatitis B vaccine by intradermal route in non responder patients: An update. World J. Gastroenterol. 2014, 20, 10383–10394. [Google Scholar] [CrossRef] [PubMed]
- Rosenbaum, P.; Tchitchek, N.; Joly, C.; Rodriguez Pozo, A.; Stimmer, L.; Langlois, S.; Hocini, H.; Gosse, L.; Pejoski, D.; Cosma, A. Vaccine inoculation route modulates early immunity and consequently antigen-specific immune response. Front. Immunol. 2021, 12, 645210. [Google Scholar] [CrossRef] [PubMed]
- Niu, L.; Chu, L.Y.; Burton, S.A.; Hansen, K.J.; Panyam, J. Intradermal delivery of vaccine nanoparticles using hollow microneedle array generates enhanced and balanced immune response. J. Control. Release 2019, 294, 268–278. [Google Scholar] [CrossRef] [PubMed]
- Menon, I.; Bagwe, P.; Gomes, K.B.; Bajaj, L.; Gala, R.; Uddin, M.N.; D’souza, M.J.; Zughaier, S.M. Microneedles: A new generation vaccine delivery system. Micromachines 2021, 12, 435. [Google Scholar] [CrossRef] [PubMed]
- Goel, A.; Aggarwal, A.; Aggarwal, R. Hepatitis B vaccine: Using skin when muscle does not work. J. Gastroenterol. Hepatol. 2016, 31, 524–526. [Google Scholar] [CrossRef] [PubMed]
- Erstad, B.L.; Barletta, J.F. Implications of obesity for drug administration and absorption from subcutaneous and intramuscular injections: A primer. Am. J. Health-Syst. Pharm. 2022, 79, 1236–1244. [Google Scholar] [CrossRef] [PubMed]
- Liang, Z. Effect of Aluminum Adjuvant on the Structure of Recombinant Hepatitis B Core Antigen. Front. Soc. Sci. Technol. 2020, 2, 27–38. [Google Scholar]
- Wang, Z.; Li, S.; Shan, P.; Wei, D.; Hao, S.; Zhang, Z.; Xu, J. Improved aluminum adjuvants eliciting stronger immune response when mixed with hepatitis B virus surface antigens. ACS Omega 2022, 7, 34528–34537. [Google Scholar] [CrossRef]
- Tajiri, K.; Shimizu, Y. Unsolved problems and future perspectives of hepatitis B virus vaccination. World J. Gastroenterol. 2015, 21, 7074. [Google Scholar] [CrossRef]
- Tanwar, S.; Thursz, M. Granulocyte colony-stimulating factor as a novel adjunct to improve hepatitis B vaccination. World J. Hepatol. 2010, 2, 136. [Google Scholar] [CrossRef] [PubMed]
- Singh, N.; Mandal, S.; Thakur, A.; Kapoor, D.; Anuradha, S.; Prakash, A.; Kohli, R.; Agarwal, S. Efficacy of GM-CSF as an adjuvant to hepatitis B vaccination in patients with chronic renal failure—Results of a prospective, randomized trial. Ren. Fail. 2003, 25, 255–266. [Google Scholar] [CrossRef] [PubMed]
- das Graças Sasaki, M.; Foccacia, R.; de Messias-Reason, I.J. Efficacy of granulocyte-macrophage colony-stimulating factor (GM-CSF) as a vaccine adjuvant for hepatitis B virus in patients with HIV infection. Vaccine 2003, 21, 4545–4549. [Google Scholar]
- Lin, C.; Zhu, J.; Zheng, Y.; Chen, Y.; Wu, Z.; Chong, Y.; Gao, Z. Effect of GM-CSF in combination with hepatitis B vaccine on revacination of healthy adult non-responders. J. Infect. 2010, 60, 264–270. [Google Scholar] [CrossRef] [PubMed]
- Chou, H.Y.; Lin, X.Z.; Pan, W.Y.; Wu, P.Y.; Chang, C.M.; Lin, T.Y.; Shen, H.H.; Tao, M.H. Hydrogel-delivered GM-CSF overcomes nonresponsiveness to hepatitis B vaccine through the recruitment and activation of dendritic cells. J. Immunol. 2010, 185, 5468–5475. [Google Scholar] [CrossRef]
- Brunel, F.; Darbouret, A.; Ronco, J. Cationic lipid DC-Chol induces an improved and balanced immunity able to overcome the unresponsiveness to the hepatitis B vaccine. Vaccine 1999, 17, 2192–2203. [Google Scholar] [CrossRef]
- Shouval, D.; Roggendorf, H.; Roggendorf, M. Enhanced immune response to hepatitis B vaccination through immunization with a Pre-S1/Pre-S2/S vaccine. Med. Microbiol. Immunol. 2015, 204, 57–68. [Google Scholar] [CrossRef] [PubMed]
- Krawczyk, A.; Ludwig, C.; Jochum, C.; Fiedler, M.; Heinemann, F.M.; Shouval, D.; Roggendorf, M.; Roggendorf, H.; Lindemann, M. Induction of a robust T- and B-cell immune response in non- and low-responders to conventional vaccination against hepatitis B by using a third generation PreS/S vaccine. Vaccine 2014, 32, 5077–5082. [Google Scholar] [CrossRef] [PubMed]
- Rendi-Wagner, P.; Shouval, D.; Genton, B.; Lurie, Y.; Rümke, H.; Boland, G.; Cerny, A.; Heim, M.; Bach, D.; Schroeder, M. Comparative immunogenicity of a PreS/S hepatitis B vaccine in non-and low responders to conventional vaccine. Vaccine 2006, 24, 2781–2789. [Google Scholar] [CrossRef] [PubMed]
- Mizrahi, M.; Lalazar, G.; Ben Ya’acov, A.; Livovsky, D.M.; Horowitz, Y.; Zolotarov, L.; Adler, R.; Shouval, D.; Ilan, Y. Beta-glycoglycosphingolipid-induced augmentation of the anti-HBV immune response is associated with altered CD8 and NKT lymphocyte distribution: A novel adjuvant for HBV vaccination. Vaccine 2008, 26, 2589–2595. [Google Scholar] [CrossRef]
- Lindemann, M.; Zaslavskaya, M.; Fiedler, M.; Wilde, B.; Heinemann, F.; Heinold, A.; Horn, P.; Witzke, O. Humoral and Cellular Responses to a Single Dose of Fendrix in Renal Transplant Recipients with Non-response to Previous Hepatitis B Vaccination. Scand. J. Immunol. 2017, 85, 51–57. [Google Scholar] [CrossRef]
- Babu, T.M.; Kotton, C.N. Immunizations in chronic kidney disease and kidney transplantation. Curr. Treat. Options Infect. Dis. 2021, 13, 47–65. [Google Scholar] [CrossRef]
- Bauer, T.; Günther, M.; Bienzle, U.; Neuhaus, R.; Jilg, W. Vaccination against hepatitis B in liver transplant recipients: Pilot analysis of cellular immune response shows evidence of HBsAg-specific regulatory T cells. Liver Transplant. 2007, 13, 434–442. [Google Scholar] [CrossRef] [PubMed]
- Michaelides, K.; Prasanna, M.; Badhan, R.; Mohammed, A.-U.-R.; Walters, A.; Howard, M.K.; Dulal, P.; Al-Khattawi, A. Single administration vaccines: Delivery challenges, in vivo performance, and translational considerations. Expert Rev. Vaccines 2023, 22, 579–595. [Google Scholar] [CrossRef] [PubMed]
- Cardell, K.; Akerlind, B.; Sällberg, M.; Frydén, A. Excellent response rate to a double dose of the combined hepatitis A and B vaccine in previous nonresponders to hepatitis B vaccine. J. Infect. Dis. 2008, 198, 299–304. [Google Scholar] [CrossRef]
- Shahidi, S.; Ghareghani, N.N.; Mortazavi, M.; Sadeghi, S.; Adeli, R. The evaluation of Tetanus-diphtheria (Td) vaccine impacts on immune response to hepatitis B (HB) vaccine in non-responder dialysis patients. J. Res. Med. Sci. Off. J. Isfahan Univ. Med. Sci. 2011, 16, 598. [Google Scholar]
- Haghighat, A.; Moafi, M.; Sharifian, J.; Salehi, H.; Taleban, R.; Kalbasi, N.; Salehi, M.; Salehi, M.M.; Salehi, M. Effect of tetanus-diphtheria vaccine on immune response to Hepatitis b vaccine in low-responder individuals. Int. J. Prev. Med. 2016, 7, 94. [Google Scholar]
- Sönmez, E.; Sönmez, A.S.; Bayindir, Y.; Coskun, D.; Aritürk, S. Antihepatitis B response to hepatitis B vaccine administered simultaneously with tetanus toxoid in nonresponder individuals. Vaccine 2002, 21, 243–246. [Google Scholar] [CrossRef]
- Fabrizi, F.; Ganeshan, S.; Dixit, V.; Martin, P. Meta-analysis: The adjuvant role of granulocyte macrophage-colony stimulating factor on immunological response to hepatitis B virus vaccine in end-stage renal disease. Aliment. Pharmacol. Ther. 2006, 24, 789–796. [Google Scholar] [CrossRef]
- Saade, F.; Honda-Okubo, Y.; Trec, S.; Petrovsky, N. A novel hepatitis B vaccine containing Advax™, a polysaccharide adjuvant derived from delta inulin, induces robust humoral and cellular immunity with minimal reactogenicity in preclinical testing. Vaccine 2013, 31, 1999–2007. [Google Scholar] [CrossRef]
- Ramezani, A.; Eslamifar, A.; Banifazl, M.; Ahmadi, F.; Maziar, S.; Razeghi, E.; Kalantar, E.; Amirkhani, A.; Aghakhani, A. Efficacy and long-term immunogenicity of hepatitis B vaccine in haemodialysis patients. Int. J. Clin. Pract. 2009, 63, 394–397. [Google Scholar] [CrossRef] [PubMed]
- Fabrizi, F.; Dixit, V.; Messa, P.; Martin, P. Intradermal vs intramuscular vaccine against hepatitis B infection in dialysis patients: A meta-analysis of randomized trials. J. Viral Hepat. 2011, 18, 730–737. [Google Scholar] [CrossRef] [PubMed]
- Christodoulou, M.; Aspray, T.J.; Schoenmakers, I. Vitamin D supplementation for patients with chronic kidney disease: A systematic review and meta-analyses of trials investigating the response to supplementation and an overview of guidelines. Calcif. Tissue Int. 2021, 109, 157–178. [Google Scholar] [CrossRef] [PubMed]
- Vingerhoets, J.; Vanham, G.; Kestens, L.; Penne, G.; Leroux-Roels, G.; Gigase, P. Deficient T-cell responses in non-responders to hepatitis B vaccination: Absence of TH1 cytokine production. Immunol. Lett. 1994, 39, 163–168. [Google Scholar] [CrossRef] [PubMed]
- Jarrosson, L.; Kolopp-Sarda, M.; Aguilar, P.; Bene, M.; Lepori, M.; Vignaud, M.; Faure, G.; Kohler, C. Most humoral non-responders to hepatitis B vaccines develop HBV-specific cellular immune responses. Vaccine 2004, 22, 3789–3796. [Google Scholar] [CrossRef]
- Hsu, Y.-C.; Huang, D.Q.; Nguyen, M.H. Global burden of hepatitis B virus: Current status, missed opportunities and a call for action. Nat. Rev. Gastroenterol. Hepatol. 2023, 20, 524–537. [Google Scholar] [CrossRef]
Characteristic | HBVaxPRO-40 | Fendrix | Engerix | Twinrix | HBVaxPRO-10 | Third-Generation Vaccines |
---|---|---|---|---|---|---|
Effectiveness in Non-responders | High | High | Moderate | Moderate | Moderate | High |
Dose | Up to 60 µg (booster) | 40 µg (chronic kidney) | Variable (10 µg standard) | Variable (combination) | 10 µg | S, preS1/S2 antigens |
Frequency | Booster/three doses | Increased frequency | Standard/booster doses | Standard/booster doses | Standard/booster doses | Variable (dependent on patient condition) |
Administration Route | Intramuscular | Intramuscular | Intramuscular | Intramuscular | Intramuscular | Intramuscular or with adjuvant systems |
Special Conditions | High immunogenicity | High response in kidney disease | Moderate response in general population | Moderate response in general population | Moderate response in general population | Enhanced immunogenicity in specific conditions |
Use of Adjuvants | No | Yes (MPL) | No | No | No | Yes (e.g., GM-CSF, MPL, liposomes, PreS1/S2 proteins) |
Side Effects | Mild to moderate | Mild | Mild | Mild | Mild | Mild injection site reactions |
Additional Notes | Suitable for higher-risk non-responders | Effective in chronic kidney disease | Commonly used; standard vaccine | Combination vaccine (Hepatitis A and B) | Commonly used; standard vaccine | More robust T and B cell responses, used in immunocompromised patients |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Bello, N.; Hudu, S.A.; Alshrari, A.S.; Imam, M.U.; Jimoh, A.O. Overview of Hepatitis B Vaccine Non-Response and Associated B Cell Amnesia: A Sco** Review. Pathogens 2024, 13, 554. https://doi.org/10.3390/pathogens13070554
Bello N, Hudu SA, Alshrari AS, Imam MU, Jimoh AO. Overview of Hepatitis B Vaccine Non-Response and Associated B Cell Amnesia: A Sco** Review. Pathogens. 2024; 13(7):554. https://doi.org/10.3390/pathogens13070554
Chicago/Turabian StyleBello, Nura, Shuaibu A. Hudu, Ahmed S. Alshrari, Mustapha U. Imam, and Abdulgafar O. Jimoh. 2024. "Overview of Hepatitis B Vaccine Non-Response and Associated B Cell Amnesia: A Sco** Review" Pathogens 13, no. 7: 554. https://doi.org/10.3390/pathogens13070554