Oral vaccination of dogs: a well-studied and undervalued tool for achieving human and dog rabies elimination

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diarrhea 10300 during hunting [[38]]. Reported gastrointestinal signs (e.g., vomiting, inappetence, constipation or diarrhea ) were probably related to the ingestion of the aluminium/polyvinyl chloride sachet and behavioral signs
rabies 116 Veterinary ResearchOral vaccination of dogs: a well-studied and undervalued tool for achieving human and dog rabies eliminationFlorence CliquetAnne-Laure GuiotMichel AubertEmmanuelle RobardetCharles E. RupprechtFrançois-Xavier
rabies 398 (pmc-release): 7/2018Publication date (ppub): /2018AbstractThe mass vaccination of dogs is a proven tool for rabies prevention. Besides parenteral delivery of inactivated vaccines, over the past several decades, several
rabies 659 modified-live, attenuated and recombinant viruses, have been evaluated for the oral vaccination of dogs against rabies . Vaccines are included within an attractive bait for oral consumption by free-ranging dogs. Due to the
rabies 1440 Health context, OVD should be considered as part of a holistic plan for the global elimination of canine rabies .Electronic supplementary materialThe online version of this article (10.1186/s13567-018-0554-6) contains
rabies 1679 which is available to authorized users.IntroductionMore than a century after Louis Pasteur developed a rabies vaccine, the disease remains endemic worldwide. This acute progressive encephalitis causes approximately
rabies 2095 (which incorporates both premature mortality and disability). The vast majority of these estimated human rabies cases occurs in Africa (36.4%) and Asia (59.6%) [[1]]. More than 99% of all rabies human cases are transmitted
rabies 2178 estimated human rabies cases occurs in Africa (36.4%) and Asia (59.6%) [[1]]. More than 99% of all rabies human cases are transmitted by dog bites. Forty percent of people bitten by suspect rabid animals are
rabies 2453 vaccination programs associated with strict prophylactic measures have been effective in eliminating rabies in dogs in all developed countries, but prevention, control and eventually elimination of canine rabies
rabies 2557 rabies in dogs in all developed countries, but prevention, control and eventually elimination of canine rabies has not been achieved in most developing countries. Low priority due to a lack of awareness of the rabies
rabies 2663 has not been achieved in most developing countries. Low priority due to a lack of awareness of the rabies burden, epidemiological constraints, inaccessibility of some subpopulations of dogs to parenteral vaccination
rabies 2907 inactivated vaccines and limited resources were identified as some of the main obstacles for effective canine rabies prevention and control [[3]].Rabies prevention by oral vaccination of wildlife with live vaccines has
rabies 3063 oral vaccination of wildlife with live vaccines has proven a powerful tool to eliminate or control rabies in multiple countries in Europe and North America [[4], [5]].This approach has been proposed as a complementary
rabies 3720 vaccination of dogs (OVD) with the objective to promote the development and use of safe and effective rabies vaccines and baits. Guidelines were issued for the evaluation of candidate vaccines for efficacy and
rabies 4270 renewed interest for OVD [[15]]. The OIE now endorses the concept of OVD, which is now included in the rabies chapter of the OIE Manual of Diagnostic Tests and Vaccines for Terrestrial Animals [[16]]. Additionally,
rabies 4572 [[17]], giving recommendations on various aspects of preventing human deaths and controlling animal rabies , including OVD [[18]].The objective of this manuscript is to review the main studies conducted to evaluate
rabies 5444 for OVDSeveral types of modified-live, attenuated or recombinant vaccines were evaluated for the oral rabies vaccination of dogs (OVD). SAD (Street-Alabama-Dufferin) Bern is a modified-live virus vaccine, cell-adapted
rabies 5777 from the SAD Bern by selection [[20], [21]]. SAG2 (SAD Avirulent Gif) is a modified-live, attenuated rabies virus vaccine, selected from the SAD Bern strain in a two-step process of amino acid mutation using
rabies 5943 two-step process of amino acid mutation using neutralizing monoclonal antibodies [[22]–[24]]. Vaccinia rabies glycoprotein (V-RG) is an attenuated (“modified-live”) recombinant vaccinia virus vector vaccine
rabies 6066 (V-RG) is an attenuated (“modified-live”) recombinant vaccinia virus vector vaccine expressing the rabies virus glycoprotein gene [[25]–[27]]. AdRG1.3 is a human adenovirus-vectored recombinant vaccine containing
rabies 6224 human adenovirus-vectored recombinant vaccine containing a glycoprotein gene sequence from the ERA rabies virus strain [[28]]. CAV-2-E3Δ-RGP is a canine adenovirus-vectored recombinant vaccine with the rabies
rabies 6328 rabies virus strain [[28]]. CAV-2-E3Δ-RGP is a canine adenovirus-vectored recombinant vaccine with the rabies virus glycoprotein [[29], [30]]. rERAG333E is a recombinant ERA rabies virus strain containing a mutation
rabies 6399 recombinant vaccine with the rabies virus glycoprotein [[29], [30]]. rERAG333E is a recombinant ERA rabies virus strain containing a mutation from Arg to Glu at G333 position [[31]]. Other live-attenuated recombinant
rabies 6516 strain containing a mutation from Arg to Glu at G333 position [[31]]. Other live-attenuated recombinant rabies virus vaccines (RV SN10-333; RV SPBN-Cyto c; RV SPBNGAS; RV SPBNGAS-GAS; VRC-RZ2) were also tested in
rabies 9940 intramuscularly, PFU: plaque forming units, TCID50: median tissue culture infectious doses.During the oral rabies vaccination campaigns in Finland from 2011 to 2014, 160 000 to 360 000 SAG2 vaccine baits were distributed
rabies 11368 animals, V-RG (tested on mice and cats) did not induce adverse events [[5]]. In contrast, SAD B19 induced rabies in nude mice (2 out of 6 mice) [[39]]. Residual pathogenicity of SAD B19 was also reported in wild rodents
rabies 11551 also reported in wild rodents (5.7% of wild rodents receiving orally a field concentration died of rabies ), as described [[39]]. In addition, adverse events were observed after administration of SAD Bern to
rabies 13960 [[13]]. Humans accidentally in contact with the vaccine (by mouth, nose, eye or wound) should receive rabies post-exposure prophylaxis, except for V-RG for which pre-exposure or post-exposure rabies vaccination
rabies 14050 should receive rabies post-exposure prophylaxis, except for V-RG for which pre-exposure or post-exposure rabies vaccination is not recommended, since this vaccine does not include infectious rabies virus [[6]].During
rabies 14136 post-exposure rabies vaccination is not recommended, since this vaccine does not include infectious rabies virus [[6]].During small scale studies in Tunisia, human exposure risks differed according to the mode
rabies 15394 [[48]]. SAD Bern elicited a strong antibody response in vaccinated dogs and complete protection against rabies after direct instillation into the mouth, but safety concerns in wild rodents [[40]] and non-human primates
rabies 15887 street virus of dog origin (ideally of salivary gland material). A concentration sufficient to cause rabies in at least 80% of controls should be administered. Immunogenicity measured by antibody response is
rabies 16310 (vaccine-in-bait efficacy). Moreover, efficacy of vaccine baits should be studied in the field [[6]].Different rabies vaccine candidates were shown to induce rabies virus neutralising antibodies (VNA) when administered
rabies 16357 baits should be studied in the field [[6]].Different rabies vaccine candidates were shown to induce rabies virus neutralising antibodies (VNA) when administered orally to dogs: SAG2 [[22]–[24]], V-RG [[25]–[27],
rabies 16618 AdRG1.3 [[28]], CAV-2-E3Δ-RGP [[30]], rERAG333E [[31]], and different live-attenuated recombinant rabies virus vaccines (RV SN10-333; RV SPBN-Cyto c; RV SPBNGAS; RV SPBNGAS-GAS) [[26], [32]].Efficacy, as defined
rabies 16930 [[22], [23]], V-RG [[25]], SAD Bern [[19]], SAD B19 [[20]], and different live-attenuated recombinant rabies virus vaccines (RV SN10-333; RV SPBN-Cyto c; RV SPBNGAS; RV SPBNGAS-GAS) [[26]].Some vaccine strains
rabies 17065 RV SPBN-Cyto c; RV SPBNGAS; RV SPBNGAS-GAS) [[26]].Some vaccine strains induced protection against rabies virus challenge after administration into a bait (Additional file 1). Most studies have been conducted
rabies 17425 post-baiting [[22]–[24], [34], [44], [50]]. This vaccine has been registered for the control of canine rabies in India in 2006 [[24]] and is, to our knowledge, the sole oral rabies vaccine registered for dogs and
rabies 17496 registered for the control of canine rabies in India in 2006 [[24]] and is, to our knowledge, the sole oral rabies vaccine registered for dogs and wildlife. When administered into baits used for oral immunisation of
rabies 17646 When administered into baits used for oral immunisation of wildlife, V-RG induced protection against rabies in laboratory dogs [[27]]. SAD B19 distributed with Köfte baits or boiled intestine baits to free-roaming
rabies 17870 Turkish dogs induced protection [[20], [21]]. CAV-2-E3Δ-RGP induced a complete protection against rabies 15 weeks after administration in a bait to indigenous Chinese dogs [[30]].Lastly, WHO recommends evaluation
rabies 18848 2 years (CAV-2-E3Δ-RGP [[30]]) after vaccine bait administration.Efficacy studies have confirmed that rabies VNA are a critical immune effector and generally correlated with protection. However, resistance to
rabies 18955 VNA are a critical immune effector and generally correlated with protection. However, resistance to rabies virus challenge was reported in some dogs despite any detectable VNA after vaccination with SAG2 [[23],
rabies 19123 detectable VNA after vaccination with SAG2 [[23], [24], [44]], V-RG [[26], [27]] and different recombinant rabies virus vaccines [[26]]. An anamnestic response was evident after rabies virus challenge in most dogs
rabies 19194 [27]] and different recombinant rabies virus vaccines [[26]]. An anamnestic response was evident after rabies virus challenge in most dogs vaccinated with SAG2, V-RG and SAD B19, including dogs which did not develop
rabies 19424 vaccination [[21], [23], [26]]. The lack of detectable antibodies in a fraction of dogs after oral rabies vaccination may cause recurring problems in the field, because there is still no reliable predictive
rabies 19793 immunised orally developed VNA, which persisted for 2 years in 80% of dogs. All 10 of 10 dogs survived a rabies virus challenge performed 2 years after their vaccination [[30]]. However, Wright et al. showed that
rabies 20017 antibodies against CAV, naturally occurring in South Africa, inhibited the development of VNA against rabies in dogs immunized with CAV-2-E3Δ-RGP. All dogs, except one which received prior vaccination against
rabies 20191 received prior vaccination against CAV and were then immunized with CAV-2-E3Δ-RGP orally, developed rabies after challenge [[52]].Bait development and evaluation of preferencesBait candidates should be tested
rabies 25101 would however necessitate modifications of regulation on the delivery and application of veterinary rabies vaccines currently enforced in many countries. Door to door baiting enables safe administration of vaccine
rabies 25572 vaccination of free-roaming and feral dogs which represent a potentially higher risk group in terms of rabies virus transmission [[6], [69]]. In WIM model, baits should be preferably distributed in late afternoon/early
rabies 26717 night cats took up to 27% of the baits. In addition, free-roaming owned dogs already vaccinated against rabies by the parenteral route can compete for distributed baits [[71]]. In contrast, the risk of unintentional
rabies 27383 methods of distribution requires adaptation to the local situation and should be incorporated in the rabies control programme as a complement to parenteral vaccination. Factors that help determine the most appropriate
rabies 29081 vaccination coverage should reach at least 70% of the total dog population to successfully eliminate rabies [[73], [74]]. Different studies showed that overall vaccination coverage was increased to levels assumed
rabies 29215 studies showed that overall vaccination coverage was increased to levels assumed to stop the spread of rabies through the use of OVD. In Sri Lanka, the vaccination coverage obtained after a parenteral vaccination
rabies 29798 84% [[75]]. In another study in the Philippines, none of the owned dogs had been vaccinated against rabies previously, and all, except one dog, were free-roaming. During the vaccination campaign, only 8% of
rabies 31099 significant overall benefits to the mass vaccination used routinely towards the elimination of canine rabies on a global basis, there are a number of potential issues that are quite distinct between the two strategies.
rabies 31337 become technically more feasible in the future to provide purified, highly immunogenic antigens for oral rabies vaccination, currently all biologics involved in the OVD are self-replicating agents. As such, the relative
rabies 32223 biologics used thus far for OVD. To date, all countries that have eliminated the transmission of canine rabies virus have used mass parenteral vaccination only [[76]]. The more routine use of OVD on large scales
rabies 32587 advantages.ConclusionsOral vaccination has the potential to become an important adjunct to traditional rabies prevention and control measures, such as parenteral vaccination of dogs, control of stray dog populations,
rabies 32728 such as parenteral vaccination of dogs, control of stray dog populations, public education and human rabies prophylaxis [[23]]. Many vaccine strains have been thoroughly evaluated for OVD, and at least two (SAG2
rabies 33517 free-roaming owned and ownerless dogs playing an important role in the disease maintenance and spread in rabies infected areas (qualitative effect) [[75]]. Safety for target and non-target species, including humans,
rabies 34883 increase in the immunisation coverage resulting from the wise application of OVD may be crucial to achieve rabies elimination.Cost-wise, countries should realize that when targeting certain high risk components of
rabies 35503 applications. Table 2 proposes a list of the main criteria that should be considered for assessing oral rabies vaccines for use in dogs.Table 2Prerequisites and criteria for oral vaccines in dogsEfficacy of the
rabies 36443 free-roaming owned dogsThermostabilitySeveral countries, especially those which have been fighting canine rabies for decades and are today close to achieving the goal of elimination (such as Thailand, Sri Lanka, Mexico,
rabies 37151 application of OVD in developing countries to help achieve the Global initiative Zero human case of rabies by 2030 [[77]].Additional filesAdditional file 1.Efficacy studies. This table contains compiled information
rabies 37300 file 1.Efficacy studies. This table contains compiled information summarizing efficacy data in oral rabies vaccines for dogs studies.Additional file 2.Attractiveness studies. This table contains compiled information
rabies 37456 2.Attractiveness studies. This table contains compiled information summarizing attractiveness data on oral rabies vaccines for dogs studies
vaccinia 6021 [[22]–[24]]. Vaccinia rabies glycoprotein (V-RG) is an attenuated (“modified-live”) recombinant vaccinia virus vector vaccine expressing the rabies virus glycoprotein gene [[25]–[27]]. AdRG1.3 is a human
vaccinia 14945 or domestic animals [[5]]. Only two human exposures, from contact with vaccinated dogs, resulted in vaccinia virus infections in a pregnant woman with epidermolytic hyperkeratosis and in a woman receiving immunosuppressive

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