BioDrugs

https://doi.org/10.1007/s40259-018-0329-7

LEADING ARTICLE

Current Ebola Virus Vaccine Progress

Andrea Marzi1 · Chad E. Mire2

© Springer Nature Switzerland AG 2019

Abstract
Over 40 years since the discovery of Ebola virus, the anti-Ebola virus vaccine efforts of the past 2 decades have culminated
in over 12 different vaccine candidates that have been placed into a number of clinical trial phases, past and present. Of
these 12 vaccines, four candidates are up to or in phase II clinical trials, and only one has completed the phase III clinical
trial stage. While remarkable progress toward a national regulatory agency-approved vaccine for Ebola virus has been made,
there remain unanswered questions on issues such as, but not limited to, vaccine protective immunity and duration of that
immunity, and the appropriate vaccination strategy for those at risk of Ebola virus infection.

Key Points  EBOV vaccine in a nonhuman primate (NHP) EBOV-medi-

Over six Ebola virus vaccine candidates have undergone
testing in human clinical trials.
Two Ebola vaccine candidates have been submitted to
the WHO for Emergency Use Assessment and Listing
(EUAL) approval.
Currently there is one Ebola vaccine candidate that is
part of the WHO Expanded Access protocol in response
to Ebola virus outbreaks.
1 Introduction
Currently, there are no national regulatory agency (NRA)-
licensed vaccines against Zaire ebolavirus (Ebola virus:
EBOV; historically EBOZ or ZEBOV) that have been sub-
mitted to the World Health Organization (WHO) for assess-
ment by the Strategic Advisory Group of Experts (SAGE)
on immunization. The first preclinical data for a successful
* Chad E. Mire
chmire@utmb.edu
1
Laboratory of Virology, Division of Intramural Research,
National Institute of Allergy and Infectious Diseases,
National Institutes of Health, Hamilton, MO, USA
2
Galveston National Laboratory, and Department
of Microbiology and Immunology, University of Texas
Medical Branch, Galveston, TX, USA
ated disease model were published in 2000 [1]. These data
were based on DNA vaccines expressing a number of ebola-
virus glycoproteins with a final boost using the replication
defective recombinant human adenovirus serotype 5 (rAd5)
vaccine expressing the EBOV glycoprotein (GP) as the sole
immunogen for EBOV. Since this publication, there has been
multifaceted progress in the EBOV vaccine field regarding
preclinical data in the NHP model; from the number of vac-
cine vectors developed with success against EBOV-mediated
disease in NHP studies [2], the dosing regimens required for
successful immunity [2], and even the timing of the immu-
nity after vaccination [3]. Even with these successes over
the past 18 years and the initial encouraging human phase
I clinical trials with the DNA and rAd5 vector regimens
[4, 5], authors opining on the subject of EBOV vaccines
still have to write that there are no United States Food and
Drug Administration (FDA)-approved vaccines for EBOV.
However, there are EBOV vaccines licensed for human use
in Russia and China [6]. While there are a multitude of rea-
sons for why there is no FDA-approved vaccine for EBOV,
the fact remains that there was no approved vaccine to use
before or during the EBOV epidemic that started in Guinea
in December 2013 and lasted until 2016.

Vol.:(0123456789)

2 Current Status of Ebola Virus (EBOV)
Vaccines
2.1 Licensure of an EBOV Vaccine Approved
by the WHO
Before the 2013–2016 EBOV epidemic, the number of
confirmed human cases in EBOV outbreaks was relatively
low, with no more than an estimated 425 cases per out-
break that occurred from 1976 to 2009 [7] compared with
the estimated 28,646 cases that occurred from 2013 to
2016 [8]. The previous EBOV outbreaks could be con-
tained by intervention strategies that employed isolation
at home of patients who were identified early, monitor-
ing of new EBOV cases through contact tracing and iso-
lation of any of those contacts who showed symptoms,
and implementation of safe burial practices that reduced
transmission through close contact with the bodies to be
buried. Regardless of the reasons or circumstances, these
interventions were either not fully implemented or were
not enough to contain the EBOV epidemic of 2013–2016,
resulting in the ‘world’s eye’ directed toward West Africa
and asking questions such as, “Why are there no vaccines
or medicines for EBOV?”. This should naturally then lead
to the question of “How does a vaccine get to a point of
being used in humans?”.
For a vaccine to make it into the arms of people there
are processes through NRAs that are mandatory and usu-
ally these depend on human clinical trials that go from
phase I to phase IV (http://www.fda.gov). Phase I studies
typically evaluate the safety (including adverse events)
and immunogenicity of different vaccine doses in human
groups that are small in number. For phase II studies, the
numbers in the groups are larger and here the vaccines are
evaluated for immunogenicity and any adverse reactions
that may occur after vaccination. While all human clini-
cal trial phases are important toward getting a vaccine to
licensure, a phase III clinical trial is often the major and
critical hurdle since the efficacy of the vaccine against the
disease or pathogen in question is a large part of the evalu-
ation. However, for sporadically occurring viral diseases
like EBOV disease, the FDA implemented the ‘animal
rule’, under which a countermeasure can be licensed with
phase I and phase II clinical trials and animal efficacy data
[9]. In phase IV clinical trials, the safety and immuno-
genicity are further evaluated in larger cohorts of humans,
but this is typically after the vaccine has received licensure
and after all the data are evaluated from the first three
phases. Human vaccine clinical trials as described above
require a massive amount of resources, time, and money
and generally have the support of a big pharmaceutical
company. These companies manufacture the vaccine as
A. Marzi, C. E. Mire
they have experience in producing large amounts of prod-
uct that are in a formulation safe for human use and pro-
vide the know-how to bring a product to market through
NRA licensure.
There are a number of reasons that have held back an
EBOV vaccine making it to licensure, such as the sporadic
and limited nature of previous EBOV outbreaks; the enor-
mous effort (often said to take 10–20 years) and money to
bring a vaccine to licensure; the willingness/ability of key
players (governments of non-affected and/or affected coun-
tries) to pay for the licensed vaccines; and the overall lack of
efficacy data of EBOV vaccine candidates in humans. Thus,
the potential for an EBOV vaccine to be licensed by the FDA
was previously small at best. However, the nature of the
2013–2016 EBOV epidemic accelerated phase I–III human
clinical trials on a number of EBOV vaccine candidates that
had previously been shown to have efficacy in EBOV NHP
models [2]. The vaccines in these trials included a non-
exhaustive list of rAd5-EBOV [10–13], rVSV-EBOV (also
known as rVSVΔG-EBOV GP or rVSV-ZEBOV) [14–23], a
combination prime-boost vaccination of rVSV-EBOV prime
followed by rAd5-EBOV boost [24], rChAd3-EBOV with
or without MVA-BN-Filo boost [25–28], and rAd26-EBOV
prime with MVA-BN-Filo boost [29, 30] (http://www.Clini​
calTr​ials.gov; http://www.pactr​.org). Each of these vaccines
generated good immunogenicity to the EBOV GP antigen
and, for the modified vaccinia Ankara (MVA) studies, the
immunogenicity was also measured for the nucleoprotein
of multiple ebolavirus species (Table 1). Along with being
immunogenic, the vaccines in the phase I/II trials lacked
any serious adverse events; however, temporary arthritis
was documented at one trial site with high-dose vaccination
using rVSV-EBOV [14] but was not reported at any other
site [15–17]. The single vaccine trials with rChAd3-EBOV
reported no arthritic events, although arthralgia was docu-
mented in the phase I rChAd3-EBOV prime and MVA-BN-
Filo boost trial [28].
As described above, there are many check points that must
be met in order for a phase III clinical trial to take place for a
vaccine. Unlike AIDS, where phase III clinical trials can be
run at any time as there are many new infections annually,
EBOV vaccine efficacy trials are more difficult to conduct
as there are only few and sporadic outbreaks. However, the
2013–2016 EBOV epidemic lasted long enough to get pro-
tocols in place and for at least one of the registered phase
III clinical trials (http://www.Clinic​ alTri​ als.gov; http://www.
pactr​.org; see Table 1) to be conducted and provide efficacy
results with significant enough numbers that were able to be
analyzed and reported. This trial was the rVSV-EBOV ring
vaccination, open-label, cluster-randomized phase III trial in
Guinea [16, 17]. The phase III clinical trial study reported
statistically significant protection against EBOV-mediated
disease and no new cases reported in either randomized
Current Ebola Virus Vaccine Progress

Table 1  Clinical trials of Ebola virus vaccines

Vaccine Study ID Location Phase Cohort Efficacy References

rVSV-EBOV NCT02269423 USA I 39 [15]

NCT02280408 USA I 39 [15]
NCT02283099 Guinea I 30 [15]
NCT02374385 Canada I 40 [19]
NCT02287480 Switzerland I/II 115 [14, 18, 33]
NCT02296983 Kenya I 40 [14, 33]
NCT02314923 USA I 512 [21]
NCT02344407 Liberia II 1500 [23]
PACTR201503001057193 Guinea III 8851 100% [16, 17]
(95% CI
68.9–100)
NCT02378753 PACTR201502001027220 Sierra Leone II/III 8651
NCT02503202 Canada, Spain, USA III 1198 [19]
PACTR201411000919191 Gabon I 155 [14, 22, 33]
NCT02718469 USA I 38
NCT02788227 USA II 18
NCT02933931 Switzerland 100 [33]
NCT02876328 PACTR201712002760250 Guinea, Liberia II 5500
NCT03031912 Canada II 200
NCT03161366 Uganda III 500
rVSV-EBOV + rAd5-EBOV No. ­495a Russia I/II 84 [24]
NCT02911415 Russia I 60
NCT02911428 Russia I 60
NCT03072030 PACTR201702002053400 Guinea, Russia IV 2000
NCT03333538 Russia I/II 120
rAd5-EBOV NCT02326194/NCT02533791 China I 120 [10, 11]
PACTR201509001259869 Sierra Leone II 500 [13]
NCT02575456
NCT02401373 China I 61 [12]
rChAd3-EBOV NCT02231866 USA I 50 [25, 26]
NCT02289027 Switzerland I/II 120 [27]
NCT02344407 Liberia II 1500
NCT02485301 Cameroon, Mali, II 3024
Nigeria, Senegal
NCT02548078 Mali, Senegal II 600
b
PACTR201412000957310 Uganda IB
rChAd3-EBOV + MVA BN-Filo NCT02240875 UK I 92 [28]
NCT02267109 Mali I 91 [26]
NCT02354404 Uganda I 90
NCT02408913 USA I 64
NCT02368119 Mali I 60
NCT02451891 UK I 38
NCT02485912 Senegal I 40
rAd26 EBOV + MVA BN-Filo NCT02313077 UK I 87 [29, 30]
c
NCT02509494 Sierra Leone III
a
 Registered in Russia
b
 Not yet recruiting
c
 Recruiting started when outbreak declined

or non-randomized clusters of contacts around confirmed
EBOV virus disease patients. While these results are very
promising, to date the rVSV-EBOV vaccine is not licensed
by an NRA on its own. However, Russia has recently
licensed an rVSV-EBOV prime with rAd5-EBOV boost
regimen through phase I, II [24], and IV studies (Table 1),
with limited preclinical efficacy data and without any effi-
cacy data in humans. In a similar vein, China also licensed
the rAd5-EBOV vaccine with limited preclinical and phase
I/II data, without efficacy data in humans [10]. The circum-
stances and standards applied for licensure and the efficacy
of the licensed vaccines remains questionable. We could not
find any information about the process. It remains to be seen
if the rVSV-EBOV vaccine will receive licensure by other
NRAs in EBOV non-endemic and endemic countries. In the
US it should be possible to license an EBOV vaccine without
human efficacy data; that is why the FDA implemented the
‘animal rule’ [9]. The combination of preclinical efficacy
data in an established animal model recapitulating human
disease (like the EBOV macaque model) and human phase
I and II clinical data should make it possible for the FDA
to approve a vaccine candidate. In November 2018, it was
announced that Merck has initiated the submission of a roll-
ing Biologics License Application to the US FDA for its
vaccine V920 (rVSV-EBOV).
2.2 Current WHO Recommendation on EBOV
Vaccine Usage During an Outbreak
In April 2017, the SAGE convened to discuss vaccines for
polio virus, cholera, diphtheria, and EBOV [31] and what
follows summarizes the EBOV portion of this meeting. At
this SAGE meeting it was acknowledged that the rVSV-
EBOV vaccine candidate had received Priority Medicine
(PRIME) designation through the European Medicine
Agency (EMA) and Breakthrough Therapy designation by
the FDA because of its human efficacy data, and along with
the rAd26-EBOV prime and MVA-BN-Filo boost vaccine,
has been submitted for WHO Emergency Use Assessment
and Listing (EUAL) approval. Almost 1 year later, no EBOV
vaccine has been prequalified by the WHO nor has a vaccine
been through the complete EUAL procedure. While there
are NRA-licensed vaccines in China and Russia, these have
yet to be submitted to the EUAL process for consideration
of use by the WHO in the prevention of EBOV outbreaks.
In light of these considerations, the SAGE recommen-
dation, should more EBOV outbreaks occur, was to imple-
ment the rVSV-EBOV vaccine within the confines of the
Expanded Access framework, employing informed con-
sent and in compliance with good clinical practice. This
Expanded Access study protocol has the potential for coor-
dination between 13 African Member States and Médecins
Sans Frontières (MSF), the vaccine manufacturer, and any
A. Marzi, C. E. Mire
other partners involved after confirmation of EBOV infec-
tion. Intriguingly, it was revealed that the Global Alliance
for Vaccines and Immunizations (GAVI) Alliance had
ordered/purchased 300,000 doses of rVSV-EBOV. While
not officially licensed by any NRA to date, the rVSV-
EBOV vaccine was well positioned for human use if there
happened to be another EBOV outbreak. And indeed, this
did not come too early; since August 2018 the Democratic
Republic of the Congo (DRC) [32] is fighting to stop its
largest EBOV outbreak on record, which is still ongoing in
the North Kivu region [33]. The rVSV-EBOV is currently
being used to help interrupt the ongoing human transmis-
sion chains in the affected area [34]; over 28,000 people
have received the vaccine [35].
3 Further EBOV Vaccine Considerations
Beyond the thoughts of EBOV vaccine researchers 5 years
ago, there has been remarkable progress with regard to the
rVSV-EBOV vaccine—it met the check points for human
use in clinical trial settings to prevent EBOV disease. It
has successfully been through phase I, II, and III clini-
cal trials showing safety, immunogenicity, and efficacy in
humans, and is currently being used in the ongoing largest
outbreak of EBOV in the DRC and neighboring Uganda,
where healthcare workers are being prophylactically vac-
cinated [36]. Since this vaccine received important EMA
and FDA designations to be used in compassionate use
situations and has been put into an Expanded Access
protocol with doses purchased by the GAVI Alliance, it
was ready for use in the ongoing outbreak. These were
all hurdles/obstacles that were presented above as being
what was holding back a WHO-approved NRA-licensed
EBOV vaccine and these have mostly been met with suc-
cess. However, for rVSV-EBOV, and all the other vac-
cine candidates for that matter, the long-term durability
of the immune response to vaccination (up to 2 years to
date for rVSV-EBOV [37, 38]) and the efficacy associ-
ated with this long-term immune response are in question
(only 90 samples at the 2-year mark for the trial described
in [32]) and not easily answered. For now, there is good
data suggesting rVSV-EBOV works well in an emergency
ring vaccination strategy as the human efficacy data sug-
gest. Therefore, the rVSV-EBOV vaccine is fulfilling its
primary purpose as it was developed as an emergency vac-
cine with the focus on a short time to immunity, whereas
durable immunity was of lower importance. It is the best
the field can hope for right now during an outbreak until
the answers of durability and efficacy for the other vaccine
platforms are answered, when one may envision more of a
population-based approach to vaccination against EBOV.
Current Ebola Virus Vaccine Progress

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