Hepatitis B and A vaccination in HIV-infected adults: A review

Figures & data

Figure 1. Search strategy and selection criteria of articles included in the review.

Table 1. Studies assessing the immunological response after HBV vaccination in adults in the HAART era

Author / Year	Study design	Vaccine manufacturer and schedule	Baseline immunological status of participants	Response rate (%)	Main findings
Sasaki Md et al.^58 2003	RCT	Engerix-B, (a) 40 μg at 0,1,6 months vs. (b) 40 μg at 0,1,6 months plus 20 μg rh GM-CSF at first visit	(a) CD4 count median=462 cells/mm^3 (b) CD4 count median=487 cells/mm^3 (a+b) 90% on HAART	(a) 60.0% (24/40) (b) 72.5% (29/40)	GM-CSF increases the immunogenicity of recombinant HBV vaccine
Fonseca et al.^46 2005	RCT	Engerix-B, (a) 20 μg at 0,1,6 months vs. (b) 40 μg at 0,1,6 months	CD4 count mean=429 cells/mm^3 86% on HAART	Overall: 40.6% (78/192) (a) 34.0% (32/94) (b) 46.9% (46/98)	Protective antibody response was associated with 40μg dose compared with the standard dose for patients with CD4 cell counts ≥ 350 cells/mm^3. 40 μg-schedule also improved seroconversion compared with standard dose for patients with HIV viral load <10,000 copies/mL
Overton et al.^55 2005	Retrospective	Engerix-B,10 μg at 0,1,6 months	Responders: CD4 count mean=449 cells/mm^3 at baseline 85% on HAART Non-responders: CD4 count mean=415 cells/mm^3 at baseline 82% on HAART	17.5% (34/194)	A plasma HIV RNA level of <400 copies/mL was associated with a protective antibody response
Cornejo-Juarez et al. ^57 2006	RCT	Recombivax HB, (a) 10 μg at 0,1,6 months vs. (b) 40 μg at 0,1,6 months	(a) CD4 count mean = 245 cells/mm^3 (b) CD4 count mean = 225 cells/mm^3 (a+b) 65% on HAART	(a) 61.5% (24/39) (b) 60.0% (29/40)	Protective antibody response was associated with being female and having a higher CD4 count
Veiga et al. ^59 2006	Prospective observational	EUVAX B, 40 μg at 0,1,6 months	Responders: CD4 count median = 452 cells/mm^3 at baseline Non-responders: CD4 count median = 359 cells/mm^3 at baseline 91% on HAART	63.8% (30/47)	Protective antibody response was associated with higher CD4 count and lower plasma HIV RNA
Ungulkraiwit et al. ^47 2007	Prospective observational	Engerix-B, 20 μg at 0,1,6 months	CD4 count mean = 345 cells/mm^3 88% on HAART	46.2% (30/65)	Protective antibody response was associated with younger age and higher CD4 cell count
de Vries-Sluijs et al. ^67 2008	Prospective observational	HBVAXPRO,10 μg at 0,1,2 months Re-vac: 20 μg, at 0,1,2 months	CD4 count median = 360 cells/mm^3 67% on HAART	Overall (after one or 2 series): 50.7% (73/144)	Protective antibody response was associated with female sex. For patients with a detectable HIV RNA load, serological response at revaccination was lower in those ≥in those ts w
Kim et al. ^48 2008	Retrospective	Twinrix or Engerix-B, 20 μg at 0,1,6 months	CD4 count mean = 325 cells/mm^3 31% on HAART	44.3%(43/97)	Protective antibody response was associated with age < 40 years, not alcohol abuse, CD4 nadir >200, HIV RNA<400 copies/ml and not African-American race
Bailey et al.^49 2008	Retrospective	Engerix-B or Recombivax HB, 20 μg at 0,1,6 months	Responders: CD4 count median = 502 cells/mm^3 at baseline 81% on HAART Non-responders: CD4 count median = 346 cells/mm^3 at baseline 74% on HAART	47.2% (59/125)	Protective antibody response was associated with HIV RNA<10,000 copies/ml
Cruciani et al.^66 2009	Prospective observational	HBVAXPRO, 40 μg at 0,1,2 months Re-vac: 1 to 3 doses	CD4 count median = 533 cells/mm^3 (excluding CD4 count <200) 80% on HAART	Overall: 89.2% (58/65) After primary schedule: 60.0% (39/65) Re-vac: 1 to 3 doses: 73.1% (19/26) After one year, 70.6% (41/58) and after 2 years, 32.7% (19/58) had persistence of anti-HBs	Protective antibody response was associated with female sex, higher CD4 count, and HIV viral load <1,000 copies. Anti-HBs titres after 1–3 booster dose/s significantly lower in non-responders than in responders to primary vaccination. Persistence of anti-HBs may be related to antibody titres after immunization.
Potsch et al.^60 2010	Prospective observational	EUVAX B, 40 μg at 0,1,2,6 months	CD4 count median = 402 cells/mm^3 79% on HAART	89% (42/47)	Protective antibody response was associated with undetectable HIV RNA load.
Psevdos et al.^Citation50 2010	Retrospective	Recombivax HB, 20 μg, at 0,1,6 months. Re-vac: 1 to 5 additional doses of 20 μg or with 3 to 8 additional doses of 40 μg	CD4 count median = 380 cells/mm^3 90% on HAART	After primary schedule: 34.7%(126/363) Re-vac: after additional 20 μg dose/s: 59.0% (36/61); after additional 40 μg doses: 85.0% (34/40)	Protective antibody response at re-vaccination was associated with HAART use and CD4 cell counts ≥ 200 cells/mm^3, as was 40 μg HBV revaccination dosage
Overton et al.^63 2010	RCT	Recombivax HB, (a) 40 μg at 0,1,3 months vs. (b) 40 μg plus 250 μg GM-CSF at 0,1,3 months	CD4 count median = 446 cells/mm^3 77% on HAART	Overall: 59.1% (26/44) (a) 65.2% (15/23) (b) 52.4% (11/21)	GM-CSF as an adjuvant did not improve the anti-HBs titres or the development of protective immunity. Subjects who developed immunity were significantly younger than those who did not
Pettit et al.^51 2010	Retrospective	Engerix-B or Twinrix, 20 μg at 0,1,6 months Re-vac: Engerix-B 40 μg at 0,1,6 months	CD4 count mean = 420 cells/mm^3 66% on HAART	After primary schedule: 46.5% (100/215) Re-vac: 66.7%(20/30)	Protective antibody response associated after primary schedule with younger age, higher CD4 count and receipt of Twinrix vs. Engerix-B.
Overton et al. ^130 2011	RCT	One booster dose in previous non-responders: Recombivax HB, (a) 40 μg vs. (b) 40 μg plus 250 μg GM-CSF	(a) CD4 count median = 375 cells/mm^3 (b) CD4 count median = 425 cells/mm^3 70% on HAART	Overall: 42% (24/57) (a) 50.0% (14/28) (b) 34.5% (10/29)	GM-CSF failed to improve responses to the booster HBV vaccination
de Vries-Sluijs et al.^Citation56 2011	Randomized non-inferiority trial	HBVAXPRO, (a) 10 μg at 0,1,3 weeks vs. at (b) 10 μg at 0,1,6 months	CD4 count median = 440 cells/mm^3 71% on HAART	(a) 38.7%(142/367) (b) 50.0% (197/394)	The efficacy of an accelerated schedule was non-inferior in those with CD4 cell count >500 cells/mm^3
Launay et al.^52 2011	RCT	(a) GenHevac B, 20 μg i.m at 0,1,6 months vs. (b) 40 μg i.m at 0,1,2,6 months vs (c) 4 μg i.d at 0,1,2,6 months	CD4 count median = (a) 516, (b) 509, (c) 482 cells/mm^3 (a) 86%, (b) 80%, (c) 86% on HAART	(a) 64.5%(91/141) (b) 82.1%(119/145) (c) 77.1%(108/140)	Both the 4 intramuscular double-dose regimen and the 4 intradermal low-dose regimen improved serological response compared with the standard HBV vaccine regimen. Protective antibody response was associated with higher CD4 count, undetectable HIV RAN viral load, younger age and no smoking
Kim et al.^Citation65 2012	Retrospective	Non-responders after a standard schedule: Re-vac: Recombivax HB, 40 μg at 0,1,2 months	CD4 count median = 433 cells/mm^3 91% on HAART	Re-vac: 81.5% (44/54) 57.6% (19/33) had persistent protective anti-HBs titres 12 months later	Protective anti-HB titres may decrease over time after successful 40 μg HBV rescue vaccination in HIV-infected patients. HIV viral load suppression could improve the persistence of anti-HB titres.
Mena et al.^62 2012	Retrospective	Engerix-B, HBVAXPRO or Twinrix, 20 or 40 μg at (a) 0,1,6 months vs. (b) 0,1,2 months vs. (c) 0,7,14–21 d Re-vac schedules also included.	CD4 count median = 488 cells/mm^3 62% on HAART	Overall: 60.3% (286/474) (a) 69.2% (157/235) (b) 58.1% (93/160) (c) 50.0% (14/28)	Protective antibody response was associated with lower HIV RNA viral load and CD4 count ≥350 cells. Patients receiving less than 3 doses of vaccine or 3 doses of the rapidly accelerated schedule had a lower probability of response in comparison with those receiving 3 doses of an accelerated schedule
Potsch et al.^61 2012	Retrospective	EUVAX B, 40 μg at 0,1,2,6 months	CD4 count median = 385 cells/mm^3 80% on HAART	After the third dose: 83.4% (136/163) After the fourth dose: 90.8% (148/163)	Strong protective antibody response was associated with undetectable HIV-1 viral load and higher CD4 count after 4 doses. Patients with undetectable HIV viral load were almost 3 times more likely to have anti-HBs titres above 100 mIU/mL than those with detectable viral load
Chaiklang et al.^53 2013	RCT	Hepavax-Gene, (a) 20 μg at 0,1,6 months vs. (b) 20 μg at 0,1,2,6 months vs. (c) 40 μg at 0,1,2,6 months	CD4 count median = (a) 400, (b,c) 544 cells/mm^3 100% on HAART	(a) 86.6% (39/44) (b) 93.2% (41/44) (c) 95.5% (42/44)	The standard 3 dose HBV vaccination in HIV infected adults with CD4+ cell counts >200 cells/mm3 and undetectable plasma HIV-1 RNA is highly effective. Although regimens of 4 injections of either standard or double doses could not significantly increase the response rate, these regimens may induce higher levels of virus antibodies
Irungu et al.^64 2013	Prospective observational	EUVAX-B, REVACC-B or SHANVAC-B at 0,1 to 3, and 6 months. Re-vac: 0,1,6 months.	557 cells/μL 0% on HAART (5 participants initiated HAART during the study period)	After the third dose: 64,2% (199/310) Re-vac: 83.3% (88/102)	Protective antibody response to initial vaccination was associated with higher CD4 count and female sex. Higher body mass index, lower plasma HIV-1 RNA levels, and shorter time to revaccination predicted protective response to re-vaccination
Rock el al.^54 2013	Retrospective	Engerix-B 20 μg at 0,1,6 months. Re-vac: 40 μg at 0,1,6 months	Responders to a primary schedule: CD4 count mean = 544 cells/mm^3 56% on HAART Non-responders to a primary schedule: CD4 count mean = 430 cells/mm^3 51% on HAART	47.3% (147/226) Re-vac: 70%(48/69)	Protective antibody response to initial vaccination was associated with higher absolute numbers and percentages of CD4 cells and responders were more likely to be receiving HAART

ˆ Inclusion and exclusion criteria: Appendix 1.

* Protective titre: Anti-HBs ≥ 10 UI/L.

# Associated factors in a multivariate analysis / Factors at baseline.

-RCT: Randomized Controlled Trial. RDBCT: Randomized Double-Blind Controlled Trial. GMT: Geometric Mean Titre. HAART: Highly active antiretroviral therapy. GM-CSF: Granulocyte Macrophage Colony-Stimulating Factor.

Table 3. Studies assessing the immunological response after HAV vaccination in adults in the HAART era

Author / Year	Study design	Vaccine manufacturer and schedule	Baseline immunological status of participants	Response rate (%)	Main findings
Kemper et al. ^1202003	RBDCT	HAVRIX 1440 EIU, Two doses, 6 months apart	CD4 count mean = 376 cells/mm^3	After the 1st dose: 11.1% (5/45) After the 2nd dose: 52.1% (25/48)	Protective antibody response to vaccination was associated with CD4 count ≥ 200 cells/mm^3
Wallace et al.^108 2004	RDBCT	VAQTA 50 IU, Two doses, 6 months apart	CD4 count mean = 458 cells/mm^3 76% on HAART	One month after the 1st dose: 61.0% (33/54) One month after the 2nd dose: 93.9% (46/49)	Protective antibody response to vaccination was associated with CD4 count ≥300 cells/mm^3
Weissman et al.^109 2006	Retrospective	HAVRIX 1440 EIU, Two doses, 6–12 months apart	85% on HAART	After the 2nd dose: 48.5% (67/138)	Protective antibody response to vaccination was associated with female sex and higher CD4 count
Rimland D and Guest J.L.^110 2005	Retrospective	HAVRIX 1440 EIU, Two doses	No data	After the 2nd dose: 60.7% (130/214)	Protective antibody response to vaccination was associated with higher CD4 count, especially if > 200 cells/mm^3
Overton et al.^111 2007	Retrospective	HAVRIX 1440 EIU, Two doses	CD4 count mean = 447 cells/mm^3 68% on HAART	After the 1st or the 2nd dose: 49.6% (133/238) After the 2nd dose: 52.2% (94/180)	Protective antibody response to vaccination was associated with male sex and HIV viral RNA load <1000 copies/ml
Launay et al. ^112 2008	RCT	HAVRIX 1440 EIU, (a) 2 doses (6 months apart) vs. (b) 3 doses (0,1 and 6 months)	CD4 count median = 355 cells/mm^3 95% on HAART	(a) After the 1st dose: 37.9% After the 2nd dose: 69.4%(34/49) (b) After the 3rd dose: 82.6% (38/46)	The 3-dose group induced a significantly higher antibody titer. Protective antibody response to vaccination was associated with not smoking
Crum-Cianflone et al.^113 2011	Retrospective	VAQTA 50 IU or HAVRIX 1440 EIU, Two doses (6–18 months apart)	CD4 count median = 461cells/mm3 62% on HAART	After the 2nd dose: 89% (116/130)	Younger age was associated with a higher initial GMC, with a trend to lower log10 plasma HIV RNA levels with better response.
Kourkounti et al.^114 2012	Prospective observational	HAVRIX 1440 EIU or VAQTA 50 IU. Two doses, 6–12 months apart	CD4 count median=564 cells/mm^3	After the 2nd dose: 74.4% (260/351)	Protective antibody response to vaccination was associated with higher CD4 count. A higher response rate and higher GMTs were observed in patients with CD4 counts ≥ 500 cells/mm^3
Mena et al.^119 2013	Retrospective	HAVRIX 1440 EIU, (a) One dose vs. (b) Two doses (6 months apart) vs. (c) Twinrix (720 EIU) at 0,7,14–21 d	CD4 count median=631 461cells/mm3 64% on HAART	(a) 60.0% (48/80) (b) 80.7% (130/161) (c) 70.7% (29/41)	Protective antibody response to vaccination was associated with female sex, not HCV co-infection and a higher CD4/CD8 ratio. Higher response was associated with reception of 2 doses of standard schedule (in comparison with those receiving only one of those of the same schedule)
Tseng et al.^115 2013	Prospective observational	HAVRIX 1440 EIU, (a) Two doses, 6 months apart vs. (b) 3 doses at 0,1 and 6 months	All participants were MSM (a) CD4 count mean = 538 cells/mm3 at baseline. 67% on HAART (b) CD4 count mean = 452 cells/mm3 at baseline. 58% on HAART	At week 24 after the first dose: (a) 88.6% (109/123) (b) 89.2% (182/204)	The GMC of anti-HAV antibody for 3-dose subjects were significantly higher than for 2-dose subjects, but was lower than HIV-uninfected subjects. Protective antibody response to vaccination was associated higher CD4 counts and undetectable plasma HIV RNA load
Jimenez et al.^116 2013	Retrospective	(a) HAVRIX 1440 EIU, Two doses, 6 months apart vs. (b) Twinrix 720 EIU, at 0,1, and 6 months	(a) HAVRIX Responders: CD4 count median = 401 cells/mm^3 Non-Responders: CD4 count median = 362 cells/mm^3 (b) Twinrix Responders: CD4 count median = 511 cells/mm^3 Non-Responders: CD4 count median = 378 cells/mm^3	(a) 54% (67/125) (b) 53% (54/101)	Protective antibody response to vaccination was associated wit higher baseline median CD4 counts and lower median HIV RNA levels. Patients with CD4 counts ≥ 350 cells/mm^3 were more likely to respond than those with CD4 counts <200 cells/mm^3. Responders were more likely to be virologically suppressed. Twinrix receivers were less likely to respond if vaccination series was not completed
Kourkounti et al. ^117 2013	Prospective observational	HAVRIX 1440 EIU or VAQTA 50 IU. Two doses, 6–12 months apart	CD4 count median = 570 cells/mm^3 56% on HAART	After the second dose: 77.0%(87/113)	Protective antibody response to vaccination was associated wit higher baseline median CD4 count at vaccination. The count of other immune cells or the administration of antiretroviral therapy did not predict response to HAV vaccine in HIV patients with baseline CD4 count >200 cells/mm^3
Jablonowska et al.^118 2014	Prospective observational	HAVRIX 1440 EIU. Two doses, 6 months apart	CD4 count median = 450 cells/mm^3 40% on HAART	79.5% (66/83) Five years after vaccination: 75.5% (37/49)	Protective antibody response to vaccination was associated with the absence of HCV antibodies. Most HIV-infected adults with high CD4 counts had a durable response even up to 5 y after vaccination.

ˆ Inclusion and exclusion criteria: Appendix 2.

* Protective titre: Anti-HAV ≥ 10 IU/L: Wallace et al., Crum-Cianflone et al.; ≥ 18 IU/L: Weissman et al.; ≥ 20 IU/L: Rimland and Guest, Launay et al., Kourkounti et al., Mena et al., Tseng et al. Kourkounti et al., Jablonowska et al.; ≥ 33 IU/L: Kemper et al.; Not reported: Overton et al.; Jimenez et al.

# Associated factors in a multivariate analysis / Factors at baseline.

-RCT: Randomized Controlled Trial. RDBCT: Randomized Double-Blind Controlled Trial. GMT: Geometric Mean Titre. EIU: ELISA units. Anti-HAV: Antibody against hepatitis A virus.

Table 2. Key issues in hepatitis B vaccination in adults living with HIV

• Viral hepatitis-related liver failure remains the most common main specific cause of liver-related deaths in people living with HIV.

• Reciprocal interactions between HIV and HBV leads to an increased risk for serious, life-threatening complications.

• Higher levels of HBV replication not only increase the risk of HBV transmission but also result in faster progression of liver fibrosis, with a higher risk of cirrhosis and end-stage liver disease, especially in patients with low CD4+ cell nadir counts.

• A diminished response to HBV vaccination in immunocompromised adults has been repeatedly shown. This includes HIV-infected subjects.

• Undetectable or minimum HIV RNA viral load and higher CD4+ cell count at baseline are the factors most-frequently associated with a successful response to HBV vaccination in both RCT and observational studies.

• Younger age and female sex were also repeatedly found to be independent factors for HBV vaccine responsiveness in HIV-infected subjects.

• A higher number of shots and HBsAg dosage have also been shown to play a significant role in anti-HBs seroconversion in HIV-infected patients.

• HIV RNA suppression at vaccination has been associated with the persistence of protective levels of anti-HBs.

• HBV vaccination of HIV-infected and non-HIV infected subjects shows a similar safety profile.

• The BHIVA and the US Guidelines for prevention and treatment of opportunistic infections in HIV-Infected adults and adolescents maintain the need for annual serological testing in immunocompromised individuals who have previously responded after one or 2 series of vaccination.

• Primary vaccination with alternative frequencies of administration, a higher number of doses, a higher concentration of HBsAg per dose, and different routes of administration have not been recommended by any of the guidelines or institutions mentioned in this review.

Table 3. Key issues in hepatitis A vaccination in adults living with HIV

• After infection, the HAV load is higher, the duration of viremia is longer and faecal excretion is prolonged in the case of concurrent HIV infection.

• The immune response to HAV vaccination is reduced in immunocompromised patients, with seroconversion rates ranging from 48.5% to 93.9%.

• Higher CD4 counts are associated with a better vaccine response. Likewise, low HIV RNA viral loads lead to better vaccine response in HIV-infected adults.

• Male sex and HCV co-infection were found to be independent factors for HBV vaccine non-responsiveness in HIV-infected subjects.

• Studies comparing the vaccine response according to whether recipients received 2 or 3 doses of inactivated HAV vaccine found that both the proportion of responders and the GMT of HAV antibodies were higher after the third dose.

• The duration of protection has been associated with suppressed HIV RNA levels at time of vaccination.

• No serious adverse events are usually reported after HAV vaccination regardless of the number of doses or the immunological status, and vaccination has no effect on the course of HIV infection.

• The CDC and WHO recommend vaccinating these subjects if any other medical, behavioral, epidemiological or occupational condition is added to HIV infection. The EACS recommends periodic controls of antibody titres in vaccinated immunocompromised subjects.

• The EACS recommends periodic controls of antibody titres in vaccinated immunocompromised subjects.

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