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- W3087334866 abstract "Vaccines vary in their efficacy and can be categorized as conferring waning, binary, or partial immunity. Some imperfect vaccines may indirectly increase parasite transmission or virulence.Target vaccine coverage depends on wildlife disease control objectives, for example, spillover prevention or conservation.Understanding the ecological drivers of variation in exposure (e.g., trait-based behaviors) and physiological response to vaccination (e.g., species identity, age class, genotype) is critical to developing efficient vaccine deployment strategies.Features of vaccine or host–parasite biology should drive the choice of modeling framework between classic compartment models versus individual-based models (IBMs). Susceptible-infected-resistant (SIR) models are useful for modeling binary imperfection, but IBMs are better for vaccines with partial imperfection. Wildlife vaccination is of urgent interest to reduce disease-induced extinction and zoonotic spillover events. However, several challenges complicate its application to wildlife. For example, vaccines rarely provide perfect immunity. While some protection may seem better than none, imperfect vaccination can present epidemiological, ecological, and evolutionary challenges. While anti-infection and antitransmission vaccines reduce parasite transmission, antidisease vaccines may undermine herd immunity, select for increased virulence, or promote spillover. These imperfections interact with ecological and logistical constraints that are magnified in wildlife, such as poor control and substantial trait variation within and among species. Ultimately, we recommend approaches such as trait-based vaccination, modeling tools, and methods to assess community- and ecosystem-level vaccine safety to address these concerns and bolster wildlife vaccination campaigns. Wildlife vaccination is of urgent interest to reduce disease-induced extinction and zoonotic spillover events. However, several challenges complicate its application to wildlife. For example, vaccines rarely provide perfect immunity. While some protection may seem better than none, imperfect vaccination can present epidemiological, ecological, and evolutionary challenges. While anti-infection and antitransmission vaccines reduce parasite transmission, antidisease vaccines may undermine herd immunity, select for increased virulence, or promote spillover. These imperfections interact with ecological and logistical constraints that are magnified in wildlife, such as poor control and substantial trait variation within and among species. Ultimately, we recommend approaches such as trait-based vaccination, modeling tools, and methods to assess community- and ecosystem-level vaccine safety to address these concerns and bolster wildlife vaccination campaigns. Vaccination, the process of exposing the immune system to an antigen to induce pathogen resistance, is a powerful tool for controlling disease. The benefits of vaccination are twofold: recipients are directly protected against infection and unvaccinated hosts are indirectly protected through herd immunity (see Glossary), which reduces transmission and parasite-mediated harm to host populations [1.Anderson R.M. May R.M. Vaccination and herd immunity to infectious diseases.Nature. 1985; 318: 323-329Crossref PubMed Scopus (507) Google Scholar]. Vaccination has been vastly successful for humans and livestock [2.Rappuoli R. et al.Vaccines, new opportunities for a new society.Proc. Natl. Acad. Sci. U. S. A. 2014; 111: 12288-12293Crossref PubMed Scopus (175) Google Scholar,3.de Swart R.L. et al.Rinderpest eradication: lessons for measles eradication?.Curr. Opin. Virol. 2012; 2: 330-334Crossref PubMed Scopus (38) Google Scholar]. Successful vaccination campaigns against rabies in raccoons (Procyon lotor), red foxes (Vulpes vulpes), gray foxes (Urocyon cinereoargenteus), and coyotes (Canis latrans) suggest that vaccination efforts could be directed towards emerging infectious diseases (EIDs) that cause devastating host declines, for example, amphibian chytridiomycosis, white nose syndrome, Tasmanian devil facial-tumor disease, and Ebola [4.Gilbert A.T. Chipman R.B. Rabies control in wild carnivores.in: Fooks A.R. Jackson A.C. Rabies: Scientific Basis of the Disease and Its Management. 4th edn. Elsevier, 2020: 605-654Crossref Scopus (2) Google Scholar, 5.MacInnes C.D. et al.Elimination of rabies from red foxes in Eastern Ontario.J. Wildl. Dis. 2001; 37: 119-132Crossref PubMed Scopus (159) Google Scholar, 6.Slate D. et al.Oral rabies vaccination in North America: opportunities, complexities, and challenges.PLoS Negl. Trop. Dis. 2009; 3e549Crossref PubMed Scopus (193) Google Scholar, 7.Scheele B.C. et al.Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity.Science. 2019; 363: 1459-1463Crossref PubMed Scopus (627) Google Scholar, 8.Hoyt J.R. et al.Long-term persistence of Pseudogymnoascus destructans, the causative agent of white-nose syndrome, in the absence of bats.EcoHealth. 2015; 12: 330-333Crossref PubMed Scopus (52) Google Scholar, 9.Flies A.S. et al.An oral bait vaccination approach for the Tasmanian devil facial tumor diseases.Expert Rev. Vaccines. 2020; 19: 1-10Crossref PubMed Scopus (16) Google Scholar, 10.Leendertz S.A.J. et al.Ebola in great apes – current knowledge, possibilities for vaccination, and implications for conservation and human health.Mammal Rev. 2017; 47: 98-111Crossref Scopus (32) Google Scholar]. The success of vaccination in human and livestock populations, the pressing need for disease-control tools in wildlife conservation, and the ever-increasing threat of zoonotic spillover events support a clear need to develop vaccination as an intervention tool for wildlife disease control. However, several outstanding challenges and questions remain before vaccination can emerge as a reliable tool for wildlife disease control. We argue that accounting for the limitations of imperfect vaccines, host and non-host ecology, and individual physiology in the development of vaccination campaigns is vital for harnessing the potential of wildlife vaccines successfully. Biodiversity conservation and the prevention of pathogen spillover are two urgent concerns of wildlife disease control. Emerging diseases of wildlife threaten population and species persistence and contribute significantly to the ongoing loss of biodiversity [11.Smith K.F. et al.Evidence for the role of infectious disease in species extinction and endangerment.Conserv. Biol. 2006; 20: 1349-1357Crossref PubMed Scopus (371) Google Scholar]. Additionally, wildlife populations are reservoir hosts for many zoonotic pathogens such as rabies, Nipah virus, and coronaviruses that threaten the health of humans [12.Letko M. et al.Bat-borne virus diversity, spillover and emergence.Nat. Rev. Microbiol. 2020; 18: 461-471Crossref PubMed Scopus (193) Google Scholar]. Controlling disease in wildlife reservoir populations can reduce spillover transmission, but complete prevention of spillover risk from a known pathogen requires elimination or eradication of a parasite within a reservoir host to prevent zoonotic transmission. Vaccines may be able to achieve this objective, but given the inherent antigenic specificity of all known vaccines they will not prevent novel pathogen emergence. Theory underlying eradication often identifies a critical level of vaccine coverage, which drives the effective reproductive ratio (Reff) of a pathogen below the threshold value of one [1.Anderson R.M. May R.M. Vaccination and herd immunity to infectious diseases.Nature. 1985; 318: 323-329Crossref PubMed Scopus (507) Google Scholar]. Combating rinderpest virus reintroduction during the eradication campaign exemplifies the intense effort needed for eradication [3.de Swart R.L. et al.Rinderpest eradication: lessons for measles eradication?.Curr. Opin. Virol. 2012; 2: 330-334Crossref PubMed Scopus (38) Google Scholar]. By contrast, vaccination for conservation aims to maximize the persistence of host populations and communities by decreasing the risk of disease-induced extinction, rather than through achieving parasite elimination. Wildlife populations can generally withstand small-scale disease outbreaks, and so conservation-motivated vaccination does not always require pathogen eradication [13.Haydon D.T. et al.Low-coverage vaccination strategies for the conservation of endangered species.Nature. 2006; 443: 692-695Crossref PubMed Scopus (142) Google Scholar]. Thus, vaccination coverage required for conservation-motivated disease control tends to be lower than that required for spillover prevention. For example, modeling estimates suggest that maintaining low vaccination coverage, between 20% and 40%, will stave off rabies-induced extinction of Ethiopian wolves (Canis simensis) [13.Haydon D.T. et al.Low-coverage vaccination strategies for the conservation of endangered species.Nature. 2006; 443: 692-695Crossref PubMed Scopus (142) Google Scholar]. Despite their potential for controlling wildlife disease, vaccines rarely provide perfect immunity, which can compromise herd immunity or contribute to the evolution of increased parasite virulence [14.Plumb G. et al.Vaccination in conservation medicine.Rev. Sci. Tech. Int. Off. Epizoot. 2007; 26: 229-241Crossref PubMed Scopus (22) Google Scholar]. For example, a prototype vaccine partially protects amphibians from Batrachochytrium dendrobatidis; vaccination decreases, but does not eliminate, parasite proliferation [15.McMahon T.A. et al.Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression.Nature. 2014; 511: 224-227Crossref PubMed Scopus (166) Google Scholar]. By contrast, a theoretically perfect vaccine would provide permanent and complete resistance to infection for all recipients, but vaccines considered for wildlife often fall short of this definition [14.Plumb G. et al.Vaccination in conservation medicine.Rev. Sci. Tech. Int. Off. Epizoot. 2007; 26: 229-241Crossref PubMed Scopus (22) Google Scholar]. Three broad aspects of vaccine imperfection are often discussed in the literature: waning, leaky, and partial immunity. However, 'leaky' immunity is used inconsistently and imprecisely, generating confusion. One reason for this is that modeling frameworks, such as susceptible-infected-resistant (SIR) compartment models can make it difficult to incorporate some types of vaccine imperfections. Therefore, we suggest a clarified categorization based on waning, binary, and partial immunity. Importantly, these categories are not mutually exclusive, and we discuss the impacts of these varying levels of immunity on wildlife populations, vaccine efficacy, and modeling frameworks. Waning describes the loss of resistance to infection over time. Individuals can vary in their waning rate, and immunity can be restored by subsequent exposures, that is, 'boosters'. Vaccine-induced immunity often wanes faster than immunity generated from natural infection, which can leave vaccinated individuals at higher risk during recurrent or cyclical epidemics [16.Heffernan J.M. Keeling M.J. Implications of vaccination and waning immunity.Proc. R. Soc. B Biol. Sci. 2009; 276: 2071-2080Crossref PubMed Scopus (70) Google Scholar]. For example, eastern equine encephalitis virus vaccination in sandhill cranes (Grus americana) and whooping cranes (Grus canadensis) waned rapidly, requiring booster vaccination within 30 days [17.Clark G.G. et al.Antibody response of Sandhill and Whooping cranes to an Eastern Equine Encephalities virus vaccine.J. Wildl. Dis. 1987; 23: 539-544Crossref PubMed Scopus (19) Google Scholar]. Life history traits, immune boosting sources, and waning rate interact to determine vaccine utility [18.Morris S.E. et al.Demographic buffering: titrating the effects of birth rate and imperfect immunity on epidemic dynamics.J. R. Soc. Interface. 2015; 1220141245Crossref PubMed Scopus (18) Google Scholar]. Waning immunity is routinely and relatively easily incorporated into SIR compartment models by allowing resistant individuals to re-enter the susceptible class. Binary immunity occurs when vaccination does not induce immunity in all recipients [19.Heininger U. et al.The concept of vaccination failure.Vaccine. 2012; 30: 1265-1268Crossref PubMed Scopus (61) Google Scholar]. This generates a binary outcome, wherein hosts are either resistant or susceptible, with no intermediate outcome. Binary outcomes of immunization have also been described as an 'all-or-nothing qualitative response' [20.Gandon S. Michalakis Y. Evolution of parasite virulence against qualitative or quantitative host resistance.Proc. R. Soc. Lond. B Biol. Sci. 2000; 267: 985-990Crossref PubMed Scopus (137) Google Scholar]. For example, high rates of binary vaccine outcomes for the varicella vaccine in humans prompted the recommendation for a second dose within months of the first [21.Michalik D.E. et al.Primary vaccine failure after 1 dose of varicella vaccine in healthy children.J. Infect. Dis. 2008; 197: 944-949Crossref PubMed Scopus (110) Google Scholar]. Differences in vaccine immunogenicity, adjuvants, vaccine storage, dosage, administration, host infection status, competence of the host’s immune system, and host genetics can all shape binary immunity [19.Heininger U. et al.The concept of vaccination failure.Vaccine. 2012; 30: 1265-1268Crossref PubMed Scopus (61) Google Scholar,22.Mentzer A.J. et al.Searching for the human genetic factors standing in the way of universally effective vaccines.Philos. Trans. R. Soc. B Biol. Sci. 2015; 37020140341Crossref PubMed Scopus (33) Google Scholar]. Random binary immunization outcomes are often incorporated into SIR models by effectively lowering vaccination coverage by the proportion of binary failures [23.Fine P. et al.'Herd immunity': a rough guide.Clin. Infect. Dis. 2011; 52: 911-916Crossref PubMed Scopus (739) Google Scholar]. However, if certain host types are more prone to vaccine failure, then it might be critical to address how these different failure rates among different host classes affect disease dynamics [24.te Kamp V. et al.Responsiveness of various reservoir species to oral rabies vaccination correlates with differences in vaccine uptake of mucosa associated lymphoid tissues.Sci. Rep. 2020; 10: 2919Crossref PubMed Scopus (12) Google Scholar]. In contrast to binary efficacy, which assumes that a vaccine either succeeds in inducing an acquired immune response or fails, vaccines that provide partial immunity may not completely prevent infection, disease symptoms, or transmission in an immunized host. Partial immunity allows for vaccine efficacy to be measured on a proportional gradient from 0 to 1, rather than as a qualitative all-or-nothing response [25.De Roode J.C. et al.Virulence evolution in response to anti-infection resistance: toxic food plants can select for virulent parasites of monarch butterflies: Resistance and virulence evolution.J. Evol. Biol. 2011; 24: 712-722Crossref PubMed Scopus (36) Google Scholar,26.Miller I.F. Metcalf C.J.E. Evolving resistance to pathogens.Science. 2019; 363: 1277-1278Crossref PubMed Scopus (5) Google Scholar]. One critical complication is that partial immunity may impact a number of infection outcomes, such as resistance to infection, disease attributed to infection, and infectiousness [27.Miller I.F. Metcalf C.J. Vaccine-driven virulence evolution: consequences of unbalanced reductions in mortality and transmission and implications for pertussis vaccines.J. R. Soc. Interface. 2019; 1620190642Crossref PubMed Scopus (11) Google Scholar]. The functional consequences of these changes are detailed below. Partial immunity is less easily incorporated into SIR-type models and has therefore been relatively neglected compared with other modes of imperfection. Individual-based models (IBMs), which explicitly track individual traits and histories, may be much better suited to investigate this vaccine imperfection. Different resistance responses to imperfect vaccines have unique ecological and evolutionary consequences. Imperfect immunization can confer the following three phenotypic types of resistance response: (i) antidisease, (ii) anti-infection, and (iii) antitransmission (Figure 1). These are also not mutually exclusive, and they can be assessed using either binary (qualitative) or partial (quantitative) metrics [26.Miller I.F. Metcalf C.J.E. Evolving resistance to pathogens.Science. 2019; 363: 1277-1278Crossref PubMed Scopus (5) Google Scholar,28.Gandon S. et al.Imperfect vaccines and the evolution of pathogen virulence.Nature. 2001; 414: 6Crossref Scopus (462) Google Scholar,29.Read A.F. et al.Imperfect vaccination can enhance the transmission of highly virulent pathogens.PLoS Biol. 2015; 13e1002198Crossref PubMed Scopus (239) Google Scholar]. Because the majority of vaccines are imperfect, anticipating and addressing their potential deleterious consequences is a priority in determining vaccination feasibility in a wildlife context. For example, the imperfect-vaccine hypothesis postulates that partial immunity upon vaccination could drive the evolution of increased pathogen virulence, and the risk of vaccine-driven virulence evolution is dependent on the vaccination phenotype and efficacy [29.Read A.F. et al.Imperfect vaccination can enhance the transmission of highly virulent pathogens.PLoS Biol. 2015; 13e1002198Crossref PubMed Scopus (239) Google Scholar]. Antidisease vaccines reduce virulence (i.e., increase host tolerance) without necessarily reducing the risk of infection or subsequent transmission. Therefore, these vaccines directly benefit recipients, but can counteract herd immunity if the infectious period is lengthened. Studies on Marek’s disease in poultry, and helminth and tuberculosis coinfections in African buffalo, show that interventions which reduce the mortality of infected hosts, without decreasing infection or transmission rates, increase parasite transmission in populations by extending the infectious period [29.Read A.F. et al.Imperfect vaccination can enhance the transmission of highly virulent pathogens.PLoS Biol. 2015; 13e1002198Crossref PubMed Scopus (239) Google Scholar,30.Ezenwa V.O. Jolles A.E. Opposite effects of anthelmintic treatment on microbial infection at individual versus population scales.Science. 2015; 347: 175-177Crossref PubMed Scopus (120) Google Scholar]. Despite this potential for increased transmission, antidisease vaccines may still be effective for conservation if their net effect reduces total parasite-induced mortality or reproductive costs. A prototype anti-Chlamydia pecorum vaccine for koala (Phascolarctos cinereus) conservation offers potential as a therapeutic vaccine as it reduces disease in unexposed and infected koalas, with some reduction in infection incidence and loads [31.Waugh C. et al.A prototype recombinant-protein based Chlamydia pecorum vaccine results in reduced chlamydial burden and less clinical disease in free-ranging koalas (Phascolarctos cinereus).PLoS ONE. 2016; 11e0146934Crossref PubMed Scopus (36) Google Scholar]. However, antidisease vaccines are unlikely to reduce spillover risk, precisely because they can promote transmission. Evolutionarily, lengthening the infectious period through antidisease vaccination is theorized to relax selection against high virulence [27.Miller I.F. Metcalf C.J. Vaccine-driven virulence evolution: consequences of unbalanced reductions in mortality and transmission and implications for pertussis vaccines.J. R. Soc. Interface. 2019; 1620190642Crossref PubMed Scopus (11) Google Scholar,29.Read A.F. et al.Imperfect vaccination can enhance the transmission of highly virulent pathogens.PLoS Biol. 2015; 13e1002198Crossref PubMed Scopus (239) Google Scholar]. This prediction, derived from the transmission-virulence trade-off hypothesis, arises because limiting host death allows for otherwise highly virulent genotypes to persist and even be favored by selection [29.Read A.F. et al.Imperfect vaccination can enhance the transmission of highly virulent pathogens.PLoS Biol. 2015; 13e1002198Crossref PubMed Scopus (239) Google Scholar]. While experimental evidence explicitly demonstrating increased virulence driven by vaccination is lacking, a recent study on house finches (Haemorhous mexicanus) parasitized by the bacterium Mycoplasma gallisepticum demonstrated that an antidisease phenotype conferred by a natural primary infection facilitated a twofold increase in the fitness advantage of a high-virulence strain during secondary infections [32.Fleming-Davies A.E. et al.Incomplete host immunity favors the evolution of virulence in an emergent pathogen.Science. 2018; 359: 1030-1033Crossref PubMed Scopus (36) Google Scholar]. However, antidisease vaccines that vary in degree of protection among immunized individuals may be less risky for vaccine-driven virulence evolution, as variance in host protection will not uniformly favor the evolution of increased parasite virulence [27.Miller I.F. Metcalf C.J. Vaccine-driven virulence evolution: consequences of unbalanced reductions in mortality and transmission and implications for pertussis vaccines.J. R. Soc. Interface. 2019; 1620190642Crossref PubMed Scopus (11) Google Scholar]. Vaccines that prevent or reduce parasite establishment in an immunized host are considered anti-infection vaccines. Antitransmission vaccines, on the other hand, may permit infection but prevent or reduce onward transmission from the recipient. Both phenotypes contribute to herd immunity, and epidemiological models predict that parasite elimination can be achieved with high rates of coverage and efficacy [28.Gandon S. et al.Imperfect vaccines and the evolution of pathogen virulence.Nature. 2001; 414: 6Crossref Scopus (462) Google Scholar]. Thus, both anti-infection and antitransmission vaccines can be effective for spillover prevention and conservation. The Mycobacterium bovis bacille Calmette–Guérin (BCG) vaccine, used to prevent spillover of M. bovis into livestock, confers anti-infection resistance in Australian brushtail possums (Trichosurus vulpecula), and the transmission-reducing prototype B. dendrobatidis vaccine offers promise for use in amphibian conservation [15.McMahon T.A. et al.Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression.Nature. 2014; 511: 224-227Crossref PubMed Scopus (166) Google Scholar,33.Buddle B.M. et al.Efficacy and safety of BCG vaccine for control of tuberculosis in domestic livestock and wildlife.Front. Vet. Sci. 2018; 5: 259Crossref PubMed Scopus (63) Google Scholar]. The evolutionary consequences of these vaccines depend crucially on the mode of imperfection. Binary anti-infection or antitransmission vaccines do not favor virulence evolution and can, at times, even reduce selection for parasite virulence, by preventing coinfections for example [28.Gandon S. et al.Imperfect vaccines and the evolution of pathogen virulence.Nature. 2001; 414: 6Crossref Scopus (462) Google Scholar,34.Choisy M. de Roode J.C. Mixed infections and the evolution of virulence: effects of resource competition, parasite plasticity, and impaired host immunity.Am. Nat. 2010; 175: E105-E118Crossref PubMed Scopus (93) Google Scholar]. Conversely, partial anti-infection or antitransmission vaccines can select for increased virulence [25.De Roode J.C. et al.Virulence evolution in response to anti-infection resistance: toxic food plants can select for virulent parasites of monarch butterflies: Resistance and virulence evolution.J. Evol. Biol. 2011; 24: 712-722Crossref PubMed Scopus (36) Google Scholar]. Partial anti-infection and antitransmission phenotypes effectively increase the exposure dose required for establishment (i.e., the infectious dose), which can select for increases in parasite reproduction rate [25.De Roode J.C. et al.Virulence evolution in response to anti-infection resistance: toxic food plants can select for virulent parasites of monarch butterflies: Resistance and virulence evolution.J. Evol. Biol. 2011; 24: 712-722Crossref PubMed Scopus (36) Google Scholar,28.Gandon S. et al.Imperfect vaccines and the evolution of pathogen virulence.Nature. 2001; 414: 6Crossref Scopus (462) Google Scholar]. Theory suggests that this type of anti-infection resistance favors virulence evolution by encouraging the increase in intrinsic parasite reproduction for successful infection establishment [25.De Roode J.C. et al.Virulence evolution in response to anti-infection resistance: toxic food plants can select for virulent parasites of monarch butterflies: Resistance and virulence evolution.J. Evol. Biol. 2011; 24: 712-722Crossref PubMed Scopus (36) Google Scholar]. Vaccines have strong potential to achieve disease control in wildlife. However, imperfect vaccines must also overcome physiological, behavioral, and ecological factors to succeed. Thus, complications arise from two primary factors: vaccine imperfections and vaccine administration. Lack of control and intraspecific, interspecific, and environmental heterogeneity are central sources of uncertainty in vaccine delivery, uptake, and response (Box 1). Vaccination success hinges on high coverage of doses that induce a durable immune response without harming recipients [1.Anderson R.M. May R.M. Vaccination and herd immunity to infectious diseases.Nature. 1985; 318: 323-329Crossref PubMed Scopus (507) Google Scholar]. In complex ecological communities, indirect deployment (i.e., oral baiting) campaigns risk simultaneously over- and under-dosing many organisms because wildlife can vary in (i) the amount of inoculum consumed or encountered, and (ii) their physiological response to a given dose.Box 1Canid Rabies Vaccination Campaigns: Limitations to ControlRabies vaccination of canids has been used to both prevent spillover transmission into human populations and protect endangered wildlife [51.WHO Expert Consultation on Rabies: Third Report. World Health Organization, 2018Google Scholar]. Rabies vaccination of domestic dogs, stray dogs, and wild canids demonstrates vaccination across a gradient of control and wildness (Figure I). Globally, domestic dogs are the main source of rabies transmission to humans [52.Hampson K. et al.Estimating the global burden of endemic canine rabies.PLoS Negl. Trop. Dis. 2015; 9e0003709Crossref PubMed Scopus (957) Google Scholar]. Consequently, owned-dog vaccination is used to interrupt dog-to-human transmission and, largely due to the control afforded by ownership, has been successful in eliminating enzootic canine rabies in the USA [53.Velasco-Villa A. et al.Successful strategies implemented towards the elimination of canine rabies in the Western Hemisphere.Antivir. Res. 2017; 143: 1-12Crossref PubMed Scopus (67) Google Scholar]. However, the unconstrained movement of stray dogs allows contact with wildlife, owned dogs, and humans, amplifying their importance in rabies transmission [54.Hampson K. et al.Transmission dynamics and prospects for the elimination of canine rabies.PLoS Biol. 2009; 7e1000053Crossref Scopus (321) Google Scholar]. Difficulty catching stray dogs contributed to poor coverage, and hence failure, in a mass rabies vaccination campaign in Bangkok, Thailand [55.Kasempimolporn S. et al.Prevalence of rabies virus infection and rabies antibody in stray dogs: A survey in Bangkok, Thailand.Prev. Vet. Med. 2007; 78: 325-332Crossref PubMed Scopus (25) Google Scholar]. Furthermore, high population growth, turnover, and translocation rates of stray dogs intensifies the challenge of achieving and maintaining vaccination coverage sufficient for herd immunity [54.Hampson K. et al.Transmission dynamics and prospects for the elimination of canine rabies.PLoS Biol. 2009; 7e1000053Crossref Scopus (321) Google Scholar, 55.Kasempimolporn S. et al.Prevalence of rabies virus infection and rabies antibody in stray dogs: A survey in Bangkok, Thailand.Prev. Vet. Med. 2007; 78: 325-332Crossref PubMed Scopus (25) Google Scholar, 56.Randall D.A. et al.An integrated disease management strategy for the control of rabies in Ethiopian wolves.Biol. Conserv. 2006; 131: 151-162Crossref Scopus (87) Google Scholar]. Combining vaccination with neutering can combat these challenges [57.Taylor L.H. et al.The role of dog population management in rabies elimination – a review of current approaches and future opportunities.Front. Vet. Sci. 2017; 4: 109Crossref PubMed Scopus (86) Google Scholar].Vaccination of wildlife against rabies, to prevent spillover into humans and domestic animals, has also involved hugely successful campaigns – locally eliminating rabies in red foxes and coyotes, while decreasing its prevalence in gray foxes [4.Gilbert A.T. Chipman R.B. Rabies control in wild carnivores.in: Fooks A.R. Jackson A.C. Rabies: Scientific Basis of the Disease and Its Management. 4th edn. Elsevier, 2020: 605-654Crossref Scopus (2) Google Scholar, 5.MacInnes C.D. et al.Elimination of rabies from red foxes in Eastern Ontario.J. Wildl. Dis. 2001; 37: 119-132Crossref PubMed Scopus (159) Google Scholar, 6.Slate D. et al.Oral rabies vaccination in North America: opportunities, complexities, and challenges.PLoS Negl. Trop. Dis. 2009; 3e549Crossref PubMed Scopus (193) Google Scholar]. This success is undoubtedly driven by the advent of oral bait vaccines, which can be distributed across large geographic scale [6.Slate D. et al.Oral rabies vaccination in North America: opportunities, complexities, and challenges.PLoS Negl. Trop. Dis. 2009; 3e549Crossref PubMed Scopus (193) Google Scholar]. Yet, although oral vaccination reduces the need for wildlife control via capture and handling, and increases the geographic scale of administration, successful oral vaccination requires ecological knowledge of target and non-target foraging behaviors and home ranges for baiting, population turnover" @default.
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- W3087334866 title "Ecological and Evolutionary Challenges for Wildlife Vaccination" @default.
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