Rabies as a threat to wildlife.

The impact of infectious disease may become progressively more harmful to a species' survival as a wild population approaches an 'extinction vortex'. This risk is especially relevant for pathogens that spread rapidly and result in high mortality rates. Rabies, a virus that infects many mammalian species, can be efficiently transmitted through infected saliva, and is fatal without prior vaccination or rapid post-exposure prophylaxis (in humans). The authors conducted an extensive literature review to identify all wild mammal species reported to have been infected with rabies virus. They found reports of infection in 190 mammalian species, including 16 with elevated risk of extinction and two for which rabies is a direct conservation threat: the Ethiopian wolf (Canis simensis) and the African wild dog (Lycaon pictus). This paper discusses selected examples in which rabies has contributed to the population decline of a species of conservation concern. In addition, the authors note the importance of the transmission of rabies virus (RABV) from domestic dogs to wildlife, and the many challenges associated with the vaccination of wild animals. With this in mind, they present potential solutions to reduce the burden of rabies on wildlife. Once stable control of RABV is achieved in domestic dogs, remaining rabies threats to wildlife conservation can be addressed more effectively.

L'impact des maladies infectieuses peut constituer une menace croissante pour la survie d'espèces animales sauvages dès lors que leurs populations sont entraînées dans la « spirale de l'extinction ¼. Ce risque se pose plus particulièrement lorsqu'il s'agit d'agents pathogènes qui se propagent rapidement et induisent un taux de mortalité élevé. Le virus de la rage affecte un grand nombre d'espèces de mammifères et se transmet facilement par contact avec de la salive infectée ; l'infection virale entraîne la mort en l'absence d'une vaccination préalable ou, chez l'être humain, d'une prophylaxie post-exposition administrée rapidement. Les auteurs ont procédé à un examen exhaustif de la littérature afin d'inventorier les espèces de mammifères sauvages chez qui l'infection rabique a été rapportée. Des cas ont été notifiés chez 190 espèces de mammifères, dont 16 présentant un risque élevé d'extinction et deux directement menacées d'extinction en raison de la rage : le loup d'Abyssinie (Canis simensis) et le lycaon (Lycaon pictus). Les auteurs apportent des précisions sur un nombre choisi d'espèces vulnérables ou en danger dont le déclin des populations est en partie imputé à la rage. En outre, ils soulignent l'importance de la transmission du virus de la rage des chiens domestiques aux animaux sauvages et décrivent les nombreuses difficultés liées à la vaccination de la faune sauvage. Ces éléments établis, ils présentent quelques solutions envisageables pour réduire le fardeau de la rage dans la faune sauvage. Une fois le virus de la rage contrôlé de manière pérenne chez le chien domestique il sera possible de lutter plus efficacement contre les autres menaces que la rage fait peser sur la conservation de la faune.

Una enfermedad infecciosa puede tener efectos cada vez más dañinos en la supervivencia de una especie a medida que una población silvestre se va aproximando a un «vórtice de extinción¼. Este riesgo tiene especial importancia en el caso de patógenos que se propagan con rapidez y causan elevadas tasas de mortalidad. La rabia, enfermedad provocada por un virus que infecta a muchas especies de mamíferos y puede transmitirse eficazmente a través de saliva infectada, resulta letal en ausencia de vacunación previa o de rápidas medidas de profilaxis tras la exposición (en el ser humano). Los autores realizaron un amplio estudio bibliográfico para determinar todas aquellas especies de mamíferos silvestres en que se hubiera descrito una infección por el virus de la rabia. Encontraron infecciones descritas en 190 especies de mamíferos, de las que 16 presentan un elevado riesgo de extinción y dos cuya conservación se ve directamente amenazada por la rabia: el lobo etíope (Canis simensis) y el licaón, o perro salvaje africano (Lycaon pictus). Los autores exponen una serie de ejemplos en los que la rabia ha contribuido al declive demográfico de una especie cuya pervivencia está en mayor o menor peligro. Los autores señalan además la importancia que reviste la transmisión del virus de la rabia de los perros domésticos a la fauna silvestre y los numerosos problemas que presenta la vacunación de los animales silvestres. Teniendo presente esta dificultad, exponen posibles soluciones para reducir la carga de rabia en la fauna silvestre. Una vez se logre estabilizar el control del virus rábico en el perro doméstico, será posible combatir más eficazmente la amenaza que representa para la conservación de las especies silvestres.

Rabies outbreak in Greece during 2012-2014: use of Geographical Information System for analysis, risk assessment and control.

The objectives of this work were (i) geographical analysis of the 2012-2014 outbreak of rabies in Greece using GIS and (ii) comparative analysis of animal cases with data of potential human exposure to rabies together with environmental data, in order to provide information for risk assessment, effective monitoring and control. Most animal cases (40/48) involved red foxes, while domestic animals were also diagnosed with rabies. Overall, 80% of the cases were diagnosed in central northern Greece; 75% of the cases were diagnosed in low altitudes (<343·5 m), within a distance of 1 km from human settlements. Median distance from livestock farms was 201·25 m. Most people potentially exposed to rabies (889/1060) presented with dog bite injuries. Maximum entropy analysis revealed that distance from farms contributed the highest percentage in defining environmental niche profiles for rabid foxes. Oral vaccination programmes were implemented in 24 administrative units of the country during 2013 and 2014, covering a total surface area of ~60 000 km2. Rabies re-occurrence in Greece emphasizes the need for ongoing surveillance in cross-border areas and in areas with intense human activity.

The relationship between socioeconomic indices and potentially zoonotic pathogens carried by wild Norway rats: a survey in Rhône, France (2010-2012).

Leptospira interrogans, hantaviruses (particularly Seoul virus), hepatitis E virus (HEV), and Toxoplasma gondii are rat-associated zoonoses that are responsible for human morbidity and mortality worldwide. This study aimed to describe the infection patterns of these four pathogens in wild rats (Rattus norvegicus) across socioeconomic levels in neighbourhoods in Lyon, France. The infection or exposure status was determined using polymerase chain reaction or serology for 178 wild rats captured in 23 locations; additionally, confirmatory culture or mouse inoculation was performed. Multivariate logistic regression analyses were used to investigate whether morphological and socioeconomic data could predict the infection status of the rats. This study revealed that the rat colony's age structure may influence the prevalence of L. interrogans, hantavirus, and HEV. In addition, areas with high human population densities and low incomes may be associated with a greater number of infected rats and an increased risk of disease transmission.

The status of tularemia in Europe in a one-health context: a review.

The bacterium Francisella tularensis causes the vector-borne zoonotic disease tularemia, and may infect a wide range of hosts including invertebrates, mammals and birds. Transmission to humans occurs through contact with infected animals or contaminated environments, or through arthropod vectors. Tularemia has a broad geographical distribution, and there is evidence which suggests local emergence or re-emergence of this disease in Europe. This review was developed to provide an update on the geographical distribution of F. tularensis in humans, wildlife, domestic animals and vector species, to identify potential public health hazards, and to characterize the epidemiology of tularemia in Europe. Information was collated on cases in humans, domestic animals and wildlife, and on reports of detection of the bacterium in arthropod vectors, from 38 European countries for the period 1992-2012. Multiple international databases on human and animal health were consulted, as well as published reports in the literature. Tularemia is a disease of complex epidemiology that is challenging to understand and therefore to control. Many aspects of this disease remain poorly understood. Better understanding is needed of the epidemiological role of animal hosts, potential vectors, mechanisms of maintenance in the different ecosystems, and routes of transmission of the disease.

Sustainable control of zoonotic pathogens in wildlife: how to be fair to wild animals?

Wildlife may harbour infectious pathogens that are of zoonotic concern. However, culling such reservoir populations to mitigate or control the transmission of these pathogens to humans has proved disappointingly inefficient. Alternatives are still in an experimental stage of development. They include vaccination, medication, contraception and environmental manipulation, including fencing and biosecurity measures. This review examines the general concepts involved in the control of wildlife diseases and presents relevant case studies. Since wildlife disease control inevitably involves interfering with wildlife ecology, this is a complex goal whose attempts at realisation should be supervised by a scientific organisation. Most approaches within natural ecosystems should first be carefully tested in trials that are progressively extended to a larger scale. Finally, all measures that aim to prevent infection in humans (such as personal hygiene or vaccination) or that encourage us to avoid infectious contacts with wildlife should be recommended.

Outbreaks of highly pathogenic avian influenza in Europe: the risks associated with wild birds.

The infection of wild birds by highly pathogenic strains of avian influenza (Al) virus was virtually unknown--apart from one instance of the disease appearing in common terns in South Africa in 1961--before the Asian strain of highly pathogenic AI virus (AIV), H5N1, began to expand across the world. Outbreaks of clinical disease in Eurasia have resulted in visible mortality among populations of free-ranging wild birds in a multitude of species. The circulation pattern of influenza viruses in natural ecosystems results from a selection pressure towards strains which are indirectly transmitted by droppings from water birds and contaminated fomites, and which exhibit low pathogenicity. Some of these viruses, of the subtypes H5 or H7, can mutate into highly pathogenic strains after being introduced into domestic poultry farms. The maintenance of highly pathogenic AIV (HPAIV) H5N1 in several parts of the world exposes wild birds to infected poultry, resulting in long-distance virus transmission. There is great concern that these wild birds may, in turn, propagate these HPAIV or introduce them into domestic birds. Rigorous disease control and biosecurity measures to protect poultry farms are the only solution presently available to mitigate such a risk.

What is the future of wildlife rabies control in Europe?

Over the last fifteen years or so, classical rabies in terrestrial wildlife has been eliminated from large areas of Western Europe. Over the next few years, terrestrial rabies is likely to occur only east of a line from the Baltic Sea to the Black Sea; the overall aim is to eliminate terrestrial rabies from the whole European Union. Elimination of rabies from the less rich countries of Eastern Europe, and the protection of Europe against a resurgence of rabies in the longer term requires modifications to existing OIE and WHO strategies. Here we discuss the options available to eliminate rabies in wildlife while taking account of financial cost, and how to maintain a 'cordon sanitaire' along the eastern boundary of the EU in order to protect the rabies-free areas from rabies incursion. Minimising financial costs at the national level is obviously essential, considering the competing priorities for development and health. This could be achieved either by increasing external funding (for example by the EU) and/or by changing the currently agreed vaccination strategy to reduce costs; any such change must not substantially reduce the chances of rabies elimination. A cordon sanitaire might be placed outside the economic area of the EU, to protect the whole of the EU, or it might be placed within the easternmost countries to ensure logistical consistency of vaccination. Policy must also anticipate an emergency due to rabies breaking out in a previously freed region. Strategic planning may be complicated by the increasing range and abundance of the raccoon dog, an introduced species that is increasingly important as a host for fox rabies. It is argued here that models help to evaluate altemative strategies, exploring options for optimising costs by minimising bait density and frequency or by reducing the vaccination area.

[Wildlife and emerging diseases]. / La faune sauvage et les maladies émergentes.

This article reviews the conditions that allow an infectious or parasitic pathogen to migrate from a wild reservoir to domestic animals and/or humans, and examines the possibility of a new disease emerging as a result. The review presents epidemiological mechanisms grouped into three principal models, illustrating them with examples: the intentional or accidental release of the reservoir host or pathogen; the exceeding of a numerical, ecological or behavioural threshold in the host populations and/or increased exposure of humans and domestic animals due to changes in behaviour; and lastly, an "adaptive" leap that ensures that a new host species finally succumbs to the pathogen and that it spreads among the conquered population. The authors examine the lessons to be drawn from such occurrences in terms of surveillance, prophylaxis and prevention.

A modelling approach to vaccination and contraception programmes for rabies control in fox populations.

In a previous study, three of the authors designed a one-dimensional model to simulate the propagation of rabies within a growing fox population; the influence of various parameters on the epidemic model was studied, including oral-vaccination programmes. In this work, a two-dimensional model of a fox population having either an exponential or a logistic growth pattern was considered. Using numerical simulations, the efficiencies of two prophylactic methods (fox contraception and vaccination against rabies) were assessed, used either separately or jointly. It was concluded that far lower rates of administration are necessary to eradicate rabies, and that the undesirable side-effects of each programme disappear, when both are used together.

Retroviruses and sexual size dimorphism in domestic cats (Felis catus L.).

Hochberg and co-workers have predicted that an increase in host adult mortality due to parasites is balanced by an earlier age at first reproduction. In polygynous species we hypothesize that such a pattern would lead to diverging selection pressure on body size between sexes and increased sexual size dimorphism. In polygynous mammals, male body size is considered to be an important factor for reproductive success. Thus, under the pressure of a virulent infection, males should be selected for rapid growth and/or higher body size to be able to compete successfully as soon as possible with opponents. In contrast, under the same selection pressure, females should be selected for lighter adult body size or rapid growth to reach sexual maturity earlier. We investigated this hypothesis in the domestic cat Felis catus. Orange cats have greater body size dimorphism than non-orange cats. Orange females are lighter than non-orange females, and orange males are heavier than non-orange males. Here, we report the extent to which orange and non-orange individuals differ in infection prevelance for two retroviruses, feline immunodeficiency virus (FIV) and feline leukaemia virus (FeLV). FIV is thought to be transmitted almost exclusively through aggressive contacts between individuals, whereas FeLV transmission occurs mainly through social contacts. The pattern of infection of both diseases is consistent with the higher aggressiveness of orange cats. In both sexes, orange cats are significantly more infected by FIV, and tend to be less infected by FeLV than other cats. The pattern of infection is also consistent with an earlier age at first reproduction in orange than in non-orange cats, at least for females. These results suggest that microparasitism may have played an important role in the evolution of sexual size dimorphism of domestic cats.

Efficacy of three oral rabies vaccine-baits in the red fox: a comparison.

The three commercial vaccine-baits currently available in western Europe were fed to caged red foxes. The vaccines were: SADB19, Bundesforschunganstalt für Viruskrankheiten der Tiere-Tübingen, Germany: a live attenuated rabies strain; SAG1 VIRBAC, France: low pathogenicity mutant of the SAD strain and "Raboral", Rhône-Mérieux, France: a vaccinia rabies glycoprotein recombinant (V-RG). Protection rates conferred by the vaccine-baits were respectively 7 of 15 (SADB19), 5 of 9 (SAG1) and 6 of 12 (V-RG) when the vaccinated foxes were challenged intramuscularly with 10(4.7) Mice Intra-Cerebral Lethal Doses 50% (MICLD50) of rabies virus which killed all of 6 unvaccinated control foxes.

Oral immunization of foxes with avirulent rabies virus mutants.

SAG1, a rabies virus strain bearing one mutation which abolishes virulence for adult animals, was constructed from the SADBern strain of rabies virus which has previously been used as live vaccine for oral immunization of foxes. SAG1 also bears an antigenic mutation which serves as an additional marker of the strain. Studies on mice and four species of wild rodents showed that SAG1 is totally avirulent whereas SADBern is still pathogenic after intracerebral, intramuscular or oral inoculation and thus could cause cases of rabies. Trials of oral vaccination performed on foxes with SAG1 indicate that it is as effective as SADBern. The SAG1 strain represents a significant progress in the search for an efficient and safe live rabies for the oral immunization of wild animals.

Use of vaccinia rabies recombinant for oral vaccination of wildlife.

A vaccinia rabies recombinant virus was constructed and shown to induce the synthesis of rabies virus glycoprotein in infected cells and to induce rabies virus neutralizing antibodies and protection in susceptible animals. Active when orally administered, this recombinant is a good candidate for the development of vaccines for wild animal rabies vectors. This recombinant was found stable, safe for target and non-target animal species, and protective for most of the rabies vectors. After extensive experimental studies conducted under controlled conditions, it as used in limited field trials and in an extensive open field trial. The preliminary results confirmed its basic properties and potential for rabies eradication.

[Population (age and sex) structure of foxes in rabies-free and invaded areas]. / Structure des populations (age et sexe) de renards en zones indemnes ou atteintes de rage.

Post mortem analysis of 1259 foxes from all over France, between 1976 and 1980, allowed comparison of age-structure of fox populations from long-time invaded areas (enzootic situation) or rabies-free areas. Heads received for rabies diagnosis have been aged by the cementum annulation technique, the sex of 650 of these foxes was known or fixed by examination of cells of the brain tissue for sex chromatin (found only in females). Results led to the generalization that young foxes (5-13 months) contracted rabies less frequently than did other ones. Consequently in rabies enzootic areas the age-structure of the fox population was lowered. The effect of 'gazage des terriers' (i.e. shooting foxes bolted from their holes with tear gas), which killed four females for each male, probably reduced the proportion of vixen in the population. No other obvious differences existed between sex-ratios. Consequently rabies does not seem to exercise any influence on this second parameter. The consequence of these results on the fox-culling is discussed.

[Radio-tracking of rabid foxes]. / Radio-pistage de renards enrages.

Three wild foxes were trapped, inoculated with rabid fox salivary glands virus and radio-tracked straightaway for about three weeks until the death of the animal. Comparison of movements between incubation and clinical period indicate principally no obvious alteration of the activity area; an important increase in movement, especially during the day-time and lastly some variable changes in the activity pattern according to the individual. A common characteristic was a long period of immobility, before death, near the border of the usual activity area. In connection with these remarks, many sub-cutaneous lesions were observed from bites on the body of one of these three foxes, after necropsy. Epidemiological consequences of these first results were argued, especially as far as transmission of rabies from one fox to another is concerned.

Managing problem wildlife in the 'Old World': a veterinary perspective.

This paper focuses on mammalian pest species mainly in Europe and Africa and on implications for animal health, human safety, wildlife management and animal welfare. Three examples of problem species are presented: the wild boar (Sus scrofa), the stray dog (Canis familiaris) and the red fox, (Vulpes vulpes). Several species are reservoirs or vectors of transmissible diseases of man and of economically valuable domestic species. The control of these and other infections and the limitation of the nuisance or damage caused by these pest species involves lethal or non-lethal methods which are briefly reviewed. Some control measures require veterinary expertise, and veterinary involvement in managing problem species is likely to increase. With regard to fertility control, methods are considered which will allow an appropriate choice of the best technique for the management of problem animals in various habitats. For desirable native species, traditional methods of control, especially hunting in the case of game species, is preferable to contraception. For exotic or feral species, control of fertility seems to be a worthwhile option.

A discrete-event computer model of feline herpes virus within cat populations.

The purpose of this work was to study the epidemiology of feline herpes virus (FHV), which causes a respiratory disease within natural populations of domestic cats. A stochastic model was constructed using discrete-events simulation. Two habitats (rural vs. urban) were simulated, featuring different demographic, spatial and social patterns. The evolution of immunity in individuals was reproduced, allowing for the random recrudescence of latent infections (influenced by environment and reproduction). Hypotheses concerning the circulation of FHV were examined regarding the role of host density and the possibility of reinfection of host. Uncertainty analyses were performed on the basis of replicated Monte Carlo sampling. The results were in good agreement with serologic data from a long-term study conducted on five populations in France. The model satisfactorily reproduced the variability of natural immunity, and the epidemic features observed. The simulations have shown that FHV can persist in small populations (because of its capacity of reactivation leading to epidemics). However, the impact on demography was not dramatic. The most important parameters in determining change in epidemiology of FHV were: transmission rate corresponding to 'friendly' contacts, and the recrudescence rate of FHV. However, an interaction between these two parameters did not allow estimation of their values.

Control of infectious diseases of wildlife in Europe.

During the last 30 years, new epidemiological patterns have emerged as free-ranging wildlife have become progressively more involved in the epidemiology of both common and emerging infectious diseases of humans and domestic animals. This has been seen in rabies, bovine tuberculosis and more recently in wild-boar classical swine fever. Emerging diseases are of interest to veterinarians as well as public health officials but attempts to control these diseases have not always been successful as in wildlife populations control of either host or pathogen can present particular problems. Lessons should be learnt from previous experiences to help in the management of new emerging diseases in the future.

Epidemiology of contagious diseases, ecology of mammals, health, management and conservation biology: concluding remarks.

In conclusion to the Proceedings of the Symposium on the Health and management of free-ranging mammals (held in Nancy, France, in 1991), the author presents a review of the literature on the ecology of diseases of wild mammals. This discipline involves the ecology of both pathogens and hosts. The ecology of a pathogen may be considered as a synonym of epidemiology, i.e. the mode of transmission and circulation of parasites, their origin, invasion and persistence. The ecology of the host deals with the outcome of infection within different geographical and time scales: a) the impact on population density and communities within the time scale of the "observer" b) the effect of infection on the co-evolution of hosts and pathogens within the evolutionary time scale. This account is illustrated by numerous examples from field studies, as well as mathematical models, and concludes by examining the effect of pathogens on biodiversity, human health and the health of domestic animals.

[Experimental infection of sheep with a rabies virus of canine origin: study of the pathogenicity for that species]. / Infección experimental de ovinos por un virus de la rabia de origen canino: estudio del poder patógeno para esta especie.

The effects of the inoculation of a canine strain of rabies virus in sheep were studied using ten animals which received different amounts of this virus. Two subjects, inoculated with 10(5.4) mouse intracerebral lethal doses 50% (MICLD50), died from rabies after 19 and 40 days of incubation. Clinical signs were anorexia, emaciation, nervous reactions and prostration before death. The virus was recovered from different parts of the central nervous system and salivary glands with high titres. Only three animals showed an antibody response, at very low levels.