Table 1.
Summary of included studies.
| Authors | Year | Country | Population | N. | Follow-Up | Vaccine Type | Primary or Secondary A | ROA | Immunization Schedule | Challenging Antigen | Risk of Bias |
|---|---|---|---|---|---|---|---|---|---|---|---|
| Uytdehaag et al. [9] | 1983 | The Netherlands | Healthy, naïve | N/R | 2 or 3 weeks after each vaccination. | DKCV | Secondary | IM | Day 0, 1mo, 6mo | DKCV | Low |
| N/R | 2 or 3 weeks after each vaccination. | DKCV | Secondary | IM | Day 0, 7, 21 | DKCV | |||||
| Celis et al. [10] | 1985 | USA | Immunized | 5 | Incubation. | N/R | Secondary | N/R | N/R | PM | Moderate |
| Celis et al. [11] | 1986 | USA | Immunized (high RVNA titer) |
5 | Maximum 6 mo after last vaccination. Incubation. | HDCV | Secondary | N/R | N/R | PMV | Moderate |
| Celis et al. [12] | 1988 | USA | Healthy | 5 | 7–10 days after last immunization. | HDCV | Secondary | N/R | PrEP (N/S) | PM, CVS, ERA, PV, North American bat (NAB; strain 6014) | Moderate |
| Bunschoten et al. [13] | 1989 | The Netherlands | Naïve | 7 | Incubation. | DKCV | Secondary | IM | Day 0, 7, 21 | PM-DKCV and PMV | Moderate |
| Ueki et al. [14] | 1990 | USA | Healthy, naïve (30–52 years) |
3 | Day -1, 7, 14, 28, 52, 163. | HDCV | Both | ID | Day 0, 7, 21, 142 | ERA | Moderate |
| 1 | Day -1, 7, 14, 28, 52, 163. | HDCV | Both | ID | Day 0, 7, 21 | ERA | |||||
| Herzog et al. [15] | 1991 | France | Healthy, post-exposure, naïve to the vaccine (19–48 years) |
22 | Day 7, 21, 28/35. | PMV | Both | N/R | 2× on day 0, 1× on 7, 21 | CVS, ERA | Moderate |
| Herzog et al. [16] | 1992 | France | Healthy, immunized | 18 | Day 21. | PMV | Secondary | N/R | 2× on day 0, 1x on 7, 21 | ERA, NC | Serious |
| Healthy, immunized | 18 | 1–36 mo after the last vaccination. | PMV | Secondary | N/R | Day 0, 7, 28 + booster each two years | ERA, NC | ||||
| Van der Heijden et al. [17] | 1993 | The Netherlands | Naïve | 25 | Before immunization and variable times. | DKCV | Secondary | N/R | 3 vaccinations | N/R | Serious |
| Thraenhart et al. [18] | 1994 | Germany | Immunized | 18 | After last immunization (2–14 years earlier). Incubation. Cell counts on day 0 and 7. | HDCV or PCECV | Secondary | N/R | N/R | PCECV, Flury LEP, GP, NP, RNP | Moderate |
| Naïve | 18 | N/A | N/A | Primary | N/A | N/A | PCECV, Flury LEP, GP, NP, RNP | ||||
| Ghaffari et al. [19] | 2001 | USA | Healthy, naïve (23–33 years) |
14 | Prior to vaccination, 4 weeks after last vaccination. | HDCV | Secondary | IM | Day 0, 7, 28 | N/R | Low |
| Brinkman et al. [20] | 2003 | The Netherlands | Healthy (19–49 years) |
18 | Day 0, 7, 14, 28, 365 days after 1st vaccination. Day 0, 7, 14, 28 after each booster. | HDCV | Both | IM | Day 0, 3 mo | PM-DKCV | Moderate |
| CID patients (4–13 years) |
5 | Day 0, 7, 14, 28, 365 days after 1st vaccination. Day 0, 7, 14, 28 after each booster. | HDCV | Both | IM | Day 0, 3 mo | PM-DKCV | ||||
| Gomez et al. [21] | 2004 | Austria | Healthy, naïve (<35 years) |
7 | Incubation. Cell counts on day 0 and 7. | N/A | Both | N/A | N/A | HDCV | Moderate |
| Healthy, naïve (>60 years) | 8 | Incubation. Cell counts on day 0 and 7. | N/A | Both | N/A | N/A | HDCV | ||||
| Moore et al. [22] | 2006 | USA | Healthy, naïve | 5 | N/R | N/A | Primary | N/A | N/A | CVS | Moderate |
| Healthy, immunized | 10 | After last immunization (5 mo to 19 years earlier). |
HDCV or PCECV | Secondary | N/A | N/A | CVS | ||||
| Brinkman et al. [23] | 2007 | The Netherlands | JIA or SLE patients (4–15 years) undergoing ASCT |
6 | Day 0, 28 after each vaccination. | HDCV | Both | IM | Day of bone marrow harvest, 6 mo after ASCT | PM-DKCV | Moderate |
| MS patients (23–50 years) undergoing ASCT | 10 | Day 0, 28 after each vaccination. | HDCV | Both | IM | Day of bone marrow harvest, 6 mo after ASCT | PM-DKCV | ||||
| Healthy (19–49 years) | 18 | Day 0, 28 after each vaccination. | HDCV | Both | IM | Day 0, 3 mo | PM-DKCV | ||||
| Blanchard-Rohner et al. [24] | 2009 | UK | Healthy, naïve (18–50 years) |
10 | Before immunization, day 2, 4, 7, 10, 14, 28 after 1st and 3rd vaccination. |
HDCV | Both | IM | Day 0, 28, 56 | N/R | Moderate |
| Healthy, immunized (18–50 years) |
10 | After a single booster. | HDCV | Secondary | IM | Day 0 | N/R | ||||
| Sirikwin et al. [25] | 2009 | Thailand | HIV1 patients, naïve (>15 years) |
27 | Day 0, 3, 7, 14, 30, 90, 180, 365. | PCECV | Both | 8-site ID | Day 0, 3, 7, 14, 30 | N/R | Moderate |
| Horowitz et al. [26] | 2010 | UK | Healthy, naïve (26–31 years) |
30 | Day 0, 21. | HDCV | Both | IM | Day 0, 7, 21 | Inactivated virus | Moderate |
| Vejpongsa et al. [27] (unpublished) | 2011 | Thailand | Immunized (20–55 years) | 41 | Day 0, 14. | PVRV | Secondary | 2-site ID | Day 0 | NR | Moderate |
| Venkataswamy et al. [28] | 2015 | India | Naïve (25–40 years) | 10 | N/A | N/A | Primary | N/A | N/A | HDCV | Low |
| Healthy, immunized (27–58 years) |
10 | Day 7 after the last vaccination. | PCECV | Secondary | ID | Day 0, 7, 28 | HDCV | ||||
| Healthy, immunized (27–58 years) |
20 | Day 7 after the last vaccination. | PCECV | Secondary | ID | Day 0, 7, 28, 180, 183 | HDCV | ||||
| Post-exposure (10–45 years) |
18 | Day 7 after the last vaccination. | PCECV | Secondary | ID | Day 0, 3, 7, 28 | HDCV | ||||
| Post-exposure (10–45 years) |
20 | Day 7 after the last vaccination. | PCECV | Secondary | IM | Day 0, 3, 7, 14, 28 | HDCV |
Abbreviations: N. = number of individuals included in study group. ROA = route of administration. N/R = not reported. DKCV = Dog Kidney Cell Vaccine. IM = intramuscular. Mo = month(s). PM = Pitman–Moore. RVNA = rabies virus neutralizing antibodies. HDCV = Human Diploid Cell Vaccine. PMV = Pittman-Moore strain cultivated in Vero cells. PrEP = Pre-Exposure Prophylaxis. N/S = not specified. CVS = challenge virus strain. PV = Pasteur strain. ID = intradermal. NC = nucleocapsid. PCECV = Purified Chicken Embryo Cell Vaccine. LEP = low egg passage strain. GP = glycoprotein. NP = N protein. RNP = ribonucleoprotein. N/A = not applicable. CID = congenital immunodeficiency. JIA = juvenile idiopathic arthritis. SLE = systemic lupus erythematosus. MS = multiple sclerosis. ASCT = Autologous Stem Cell Transplantation. USA = United States of America. UK = United Kingdom. HIV1 = Human Immunodeficiency Virus 1. PVRV = Purified Vero Rabies Vaccine. A: A primary response is defined as the response to the antigen in (cells of) a naïve individual. After any previous encounter with the antigen, the cells or individual cannot be considered naïve anymore, and, therefore, these responses were defined as secondary or memory responses.