Get 20M+ Full-Text Papers For Less Than $1.50/day. Start a 7-Day Trial for You or Your Team.

Learn More →

Canine Rabies Ecology in Southern Africa

Canine Rabies Ecology in Southern Africa Canine Rabies Ecology in Southern Africa John Bingham* Rabies is a widespread disease in African domestic although their role has been controversial; some studies dogs and certain wild canine populations. Canine rabies indicate that they can support rabies cycles (8), and other became established in Africa during the 20th century, coin- studies indicate that they cannot maintain rabies independ- ciding with ecologic changes that favored its emergence in ently of the disease cycle in dogs (9–12). Although rabies canids. I present a conceptual and terminologic framework is a prominent disease of African canids, the mechanisms for understanding rabies ecology in African canids. The and hosts responsible for sustaining it have not been clear- framework is underpinned by 2 distinct concepts: mainte- ly elucidated. nance and persistence. Maintenance encompasses the I review the ecology of canine rabies in southern Africa, notion of indefinite transmission of infection within a local particularly with the goal of resolving the controversies on population and depends on an average transmission ratio >1. Maintenance in all local populations is inherently unsta- mechanisms of persistence. A conceptual and terminologic ble, and the disease frequently becomes extinct. framework to understand the long-term ecologic survival of Persistence, the notion of long-term continuity, depends on rabies virus in African canine hosts is proposed. the presence of rabies in >1 local population within the canine metapopulation at any time. The implications for Rabies Virus Biology understanding rabies ecology and control are reviewed, as Rabies virus is transmitted in saliva through the bite of are previous studies on rabies ecology in African canids. an infected animal. After gaining entry to the central nerv- ous system by peripheral nerves, it causes encephalitis, he ecologic persistence of pathogenic viruses has been leading to fulminant, progressive neurologic disease, char- Tthe focus of many studies (1–4). Rabies virus, a acterized by excitement, muscular paralysis, impaired lyssavirus that causes a lethal neurotropic infection of responses to social and environmental signals, and other mammals, is a pathogen for which ecologic persistence abnormal neurologic signs. The incubation period is cannot be explained adequately by pathogenetic mecha- unusually variable and can be long; clinical disease and nisms. Death of the host implies that the virus depends on virus shedding are not seen during this period. Infection of transmission to new susceptible hosts to survive. However, the salivary glands during the clinical stage leads to shed- epidemics, a frequent manifestation of rabies, deplete the ding of virions in saliva (13). number of susceptible hosts, which leads to the decline or Rabies virus has a broad mammalian host range. extinction of the virus in the affected population. How, However, in any ecologic zone, a single species, the main- then, does the virus persist? tenance host, is usually principally responsible for support- In southern Africa, rabies virus affects many host ing the virus cycle. The virus variant of the maintenance species, but rabies cycles are sustained by carnivore hosts host is intimately adapted to the host’s physiology and bio- (5,6), particularly by canine species (family Canidae), chemistry to ensure effective transmission (14). which are the focus of this paper, and by mongooses (fam- Maintenance hosts are usually extremely sensitive to their ily Herpestidae) (5,7), which will not be considered here. variant but relatively resistant to rabies virus variants of Domestic dogs (Canis familiaris) are hosts of rabies virus other species. In maintenance hosts, the probability is high in most of Africa; they cause most human rabies cases and that the virus will establish infection, will induce the contacts that require medical intervention. In southern appropriate behavioral changes, such as aggressive biting Africa, jackals (C. adustus, C. mesomelas) are also hosts, behavior, and will prolong the clinical survival period in which salivary virus shedding takes place; all of these fac- tors lead to maximal virus transmission (14). *Commonwealth Scientific and Industrial Research Organisation For a virus cycle to be successfully maintained, the (CSIRO) Australian Animal Health Laboratory, Geelong, Victoria, average transmission ratio (the average number of new Australia Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 9, September 2005 1337 PERSPECTIVE cases caused by each infected host) must be >1. At the susceptible individuals that can replicate, shed, and trans- beginning of an epidemic, this number is expressed math- mit virus efficiently to conspecifics. Maintenance hosts ematically as the basic reproductive number, R , which is live in local populations, which support indefinite trans- defined as the number of new infections generated from an mission of virus independently of other local populations. existing infection, when that infection is introduced into a Individual local populations are unlikely to maintain population composed entirely of susceptible hosts (3,15). rabies continuously because of the inherently high instabil- R is usually treated as a constant that only applies at the ity of the disease in any single local population; the disease beginning of an epidemic, when the ratio of susceptible to is normally reintroduced from other infected local popula- infected hosts is at a maximum. R will not be used in this tions. Persistence encompasses the concept of long-term article, as it precludes variability in space and time (16,17); and continuous presence of disease within a metapopula- the term average transmission ratio, as defined above, will tion. Successful persistence requires that virus is main- generally be used instead. tained in >1 local population at any time. Individuals of species other than the maintenance host Many viral pathogens depend on a constant supply of may also become infected; they are usually dead-end hosts susceptible hosts because the viral infection causes either because of low transmission ratios, which are caused by host death or durable immunity. The unstable pattern factors such as the failure to induce biting behavior, ineffi- caused by depletion and renewal of host local populations cient salivary shedding, and absence of other hosts with is a prominent feature of all carnivore rabies cycles, partic- which to interact. Occasionally, nonmaintenance hosts ularly when studied at a relatively fine geographic resolu- successfully transmit the infection to conspecifics, which tion (6,8,20–24). may lead to the establishment of a new cycle if conditions Mathematical models have shown the importance of for continual, effective transmission to conspecifics are features such as host population heterogeneity and mixing. favorable. The emergence of a new cycle requires some If a spatially heterogeneous host metapopulation experi- genetic adaptation of the virus in the new host. ences a degree of movement between local populations, a Lyssaviruses can probably adapt with relative ease because pathogen can persist over the long term even though it may their broad host range allows adaptive selection to take frequently become extinct in local populations (4,25–28). place, as evidenced by the emergence of many new cycles Metapopulation heterogeneity may be in terms of density, in the last 100 years. A mechanism to explain how such demographic structure, social interactions, and other char- adaptation may arise is the quasispecies concept, where the acteristics that influence transmission ratios. inherently high mutation rates of RNA viruses produce Maintenance and persistence of rabies are affected by variant populations of viruses through which selection can population immunity, which in effect lowers the average act (18). transmission ratio. In carnivores, population immunity against rabies is almost exclusively caused by vaccination Definitions and Concepts rather than natural infection, which is usually fatal. Two working definitions will be cited. A local popula- tion is a “set of individuals that live in the same habitat Canine Rabies in Southern Africa patch and therefore interact with each other” (19). A In addition to the domestic dog, 3 wild canids have metapopulation is a “set of [discrete] local populations been implicated as independent maintenance hosts of within some larger area, where typically migration from rabies in southern Africa: the side-striped jackal (C. adus- one local population to at least some other patches is pos- tus), the black-backed jackal (C. mesomelas), and the bat- sible” (19). The demographic trends of local populations eared fox (Otocyon megalotis) (5,6,8,29). Rabies cases are asynchronous, particularly where migration between have also been reported in other African canids, such as them is relatively low. In this article, the definitions of African wild dogs (Lycaon pictus) (30) and Ethiopian local population and metapopulation may apply to either wolves (C. simensis) (31), but these species do not appear the host or the virus. To use an analogy borrowed from to support extended virus cycles independent of other ecology, the host local population may be viewed as a hosts. resource patch for the pathogen. In Africa, dogs are intimately dependent on humans for Maintenance is the notion of indefinite transmission of food and shelter (32,33), and this association means that virus through members of a host population. (In this con- dog populations can be correlated, in size as well as distri- text “indefinite” transmission does not mean “permanent” bution, with human populations. During the 20th century, but rather denotes an open-ended cycle that is dependent the human population of Africa expanded enormously, and on availability of susceptible hosts.) The average transmis- the dog population expanded in parallel (33). Social sion ratio must be >1 for virus maintenance to be success- changes, such as urbanization, resulted in an increase in ful. A maintenance host is a member of a population of human and dog movement. Rabies persistence would have 1338 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 9, September 2005 Rabies in Southern Africa been enhanced in such a dog metapopulation consisting of tis are closely related but distinct (34). In addition, viruses more numerous local populations and greater movement of all fall within the cosmopolitan lineage that includes many infected dogs. other dog and wild canine virus variants from other regions Such a prediction is borne out by historical records. of the world (35). This finding supports the epidemiologic Rabies in sub-Saharan Africa is a disease of modern times; observations that all present-day dog, jackal, and O. mega- no firm evidence exists of its occurrence before the late lotis rabies viruses in southern Africa stem from a single, 19th century. The first confirmed outbreaks, in South recently introduced virus derived from domestic dogs. Africa in 1893 and Southern Rhodesia (now called However, molecular techniques are not precise enough to Zimbabwe) in 1902, were in domestic dogs, and their ori- indicate which species, dogs or the 3 wildlife species, gin was traced to distant lands (5). The initial outbreaks maintains the virus cycles that are found in wildlife. were temporally and spatially sporadic, and rabies appar- Epidemiologic evidence is required to determine this ently could not become established. These outbreaks were (5,8,29). followed by increasingly frequent, but initially sporadic, outbreaks, until the disease was continuously present in Review of African Canine Rabies Studies national records, as can be seen in the annual reports of the I propose that African canine rabies ecology must be departments of animal health of various African countries understood through the distinct concepts of maintenance from 1892 to 1960. and persistence. An alternative mechanism proposed for Rabies in jackal species appeared in southern and east- rabies persistence in African domestic dogs includes an ern African countries after the introduction of the disease infectious healthy carrier status (10,36). One study pro- in dogs. In Zimbabwean C. adustus populations, rabies poses this mechanism for rabies in spotted hyenas occurred in large, dense, moving epidemics in commercial (Crocuta crocuta, Carnivora: Hyaenidae), on the basis of farming areas (8). The jackal index cases of the epidemics rabies virus RNA detected in saliva of healthy hyenas by were usually associated with cases in dogs, which indi- polymerase chain reaction, although virus isolation, cates that these epidemics were initiated by dog rabies arguably the more important test, was unsuccessful from cycles; once initiated, however, the epidemics were main- these samples (37). A second mechanism by which rabies tained independent of dogs. The moving epidemics termi- may persist is the concept of long incubators, which carry nated at the geographic limits of the C. adustus population infection through quiescent periods to restart epidemics dominance. when the host density has recovered. Long incubators Both jackal species reach high densities in commercial have been reported mainly in humans and other nonmain- farming environments. Jackal rabies occurs predominantly tenance species (38,39). No evidence currently shows that in these areas, but it is virtually absent from most national carrier animals or long incubators play a role in the per- parks, despite substantial jackal populations (8). sistence of rabies cycles in canine hosts, perhaps because Commercial farming practices appear to provide ecologic they do not occur frequently enough to be obvious. conditions that are highly favorable for jackals and jackal Although they should not be ignored, these concepts are rabies. What these conditions are is unclear, but they may difficult to demonstrate scientifically and even more diffi- include abundant resources, increased demographic cult to quantify in terms of their ecologic importance for turnover, and the absence of competitors such as dogs and virus persistence. wild scavengers. Previous studies have questioned the ability of jackals to In southern Africa, rabies in C. mesomelas and O. support rabies virus cycles (9–11). These studies have not megalotis predominantly occurs in the absence of domes- distinguished between the ability of species to support tic dogs or rabies in other carnivores. Given the general pathogen cycles (i.e., maintenance) and the concept of long- lack of associated rabies cases in other species, C. term persistence. Acknowledging this distinction would mesomelas and O. megalotis are likely maintenance host show that local populations of canine species may maintain populations, capable of maintaining the virus cycle inde- epidemics independently and may be free of rabies for peri- pendent of other species. In C. mesomelas and Otocyon ods, often long periods, between epidemics. At the level of populations, the mechanisms of rabies maintenance are the local population, this pattern is essentially similar in poorly understood; because surveillance is scanty, discern- domestic dogs, jackals, and other canids (e.g., African wild ing true spatial and temporal disease patterns is difficult dogs [30]). Domestic dogs may appear to support rabies (5,8,29). infection endemically, whereas jackals do not (11), simply Molecular epidemiology studies have indicated that, in because more numerous discrete local dog populations are Zimbabwe and South Africa, rabies viruses from dogs and within the study area than are jackal populations. jackals are phylogenetically similar and do not fall into Considering rabies ecology through the concepts pre- host-distinguishable lineages, while viruses of O. megalo- sented here would clarify some of the confusion created by Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 9, September 2005 1339 PERSPECTIVE these studies (9–11). For example, a study (11) that used a too low to maintain the chain of infection.” However, the mathematical model concluded that “the side-striped jack- dense moving epidemics, which lasted several years and al population itself does not seem able to support rabies occurred in the absence of cases in other species (8), imply infection endemically, i.e., without frequent reintroduction that host density was not a limiting factor in jackal epi- from outside sources of infection.” While reintroductions demics. Once again, we can resolve this apparent contra- of infection are certainly an important feature in C. adus- diction by considering these populations of jackals to be tus rabies, reintroduction is probably infrequent, given that capable of cycle maintenance but not persistence. most C. adustus cases reported in 46 years followed 5 dog- Transmission is efficient within local populations, but high to-jackal initiation events (8). The contradiction is transmission ratios are transient. The jackal populations of resolved once the concepts of maintenance and persistence Zimbabwe and the rabies viruses they support should not are applied. Hence, C. adustus is capable of maintaining be considered metapopulations because they do not have, rabies cycles independent of other species, but rabies as dog populations do, the spatial separation or interpopu- cycles have not been persistent. lation migration that would be necessary for them to be Terms such as reservoir and endemic do not provide the considered metapopulations. This absence of a metapopu- conceptual clarity necessary to understand rabies ecology lation structure explains the failure of rabies persistence in (10,11). In a study that acknowledges the complexities of jackal populations, and this absence, rather than their defining the term and uses canine rabies as an example, inability to maintain virus, distinguishes jackals from dogs Haydon et al. (12) state that a reservoir is a population “in as hosts of rabies. which the pathogen can be permanently maintained.” However, this definition is problematic because the term Control of Rabies in Africa “permanently maintained” is ambiguous. This study Applying the metapopulation principle to canine rabies implies that dogs, but not jackals, are reservoirs because in Africa reinforces conventional principles of control: they are permanent hosts, yet many dog populations, as employing vaccination or culling in affected host popula- with many jackal populations, do not permanently support tions and minimizing movement of infected hosts. For rabies cycles. Such definitions fail to provide a convincing many decades, controlling rabies in Africa, has been the argument that essential distinctions exist between dogs and mandate of governments. Vaccination programs for dogs jackals in their ability to support rabies cycles. The study generally consisted of periodic visits by a government vac- by Haydon et al. also defines a reservoir in relation to a tar- cination team to communities, which were seen as compli- get population, which is “the population of concern or ant recipients. While in some cases such government- interest to us” and which requires protection. Such anthro- initiated control efforts arguably had some effect on reduc- pocentric definitions of pathogen behavior, although hav- ing rabies, they did not cause any long-term trend in reduc- ing some conceptual value for protecting human health and ing rabies in maintenance hosts or humans. African interests, are unhelpful for understanding the biologic governments have been unable to sustain the level of mechanisms of pathogen emergence and persistence. resource commitment needed to maintain effective levels The scale at which ecologic systems are examined has of vaccination coverage. The metapopulation principle implications, since disease frequency is less stable in local indicates that with increasing dog population density, size, populations than in metapopulations (40). Hence, a farmer and movement, rabies control will require ever-increasing will perceive rabies on his property as epidemic in nature, resources. Traditional methods that have not worked well with intense outbreaks separated by long periods of in the past are likely to be even less effective in the future. absence, while a national epidemiologist may claim that Instead, a completely different approach to controlling the disease is endemic in his country. Both observations rabies is needed. Perhaps this approach should be based on are correct, but observers perceive the epidemiology dif- community-driven initiatives, where the role of govern- ferently because they view the disease frequency at differ- ments focuses on support activities such as surveillance, ent scales. The lump analysis of national rabies case data information dissemination, and legislation. Since dogs are of Zimbabwe (10,11) led to a blending and masking of dis- an integral and dependent part of human communities, ease patterns, giving these researchers the erroneous community-driven initiatives for rabies control may be impression that rabies frequency in dogs was more stable more sustainable than those directed by governments. than it was in jackals. While the transmission ratio, as influenced by host den- Conclusions sity, for example, is the only determinant of maintenance, In recent decades, the frequency of rabies has increased it is not the sole determinant of persistence. In discussing in Africa. Controlling this disease will require a deeper rabies in Zimbabwean jackal populations, Rhodes et al. understanding of its biology. When interpreting rabies case (11) suggest that the “average jackal population density is data for epidemiologic analysis, we must distinguish 1340 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 9, September 2005 Rabies in Southern Africa 11. Rhodes CJ, Atkinson RPD, Anderson RM, Macdonald DW. Rabies in between the concepts of maintenance (the ability of local Zimbabwe: reservoir dogs and the implications for disease control. populations to support a disease cycle) and persistence (the Philos Trans R Soc Lond B Biol Sci. 1998;353:999–1010. presence of >1 infected local population in a host metapop- 12. Haydon DT, Cleaveland S, Taylor LH, Laurenson MK. Identifying ulation). To clearly conceptualize the ecology of canine reservoirs of infection: a conceptual and practical challenge. Emerg Infect Dis. 2002;8:1468–73. rabies, we must use lucid, appropriate definitions for virus- 13. Charlton KM. The pathogenesis of rabies and other lyssaviral infec- host interactions and epidemiologic patterns. tions: recent studies. In: Rupprecht CE, Dietzschold B, Koprowski H, The ecology of many ecosystems has changed dramat- editors. Lyssaviruses. Berlin: Springer-Verlag; 1994. p. 95–119. ically in recent centuries because of the increase in human 14. Wandeler AI, Nadin-Davis SA, Tinline RR, Rupprecht CE. Rabies epidemiology: some ecological and evolutionary perspectives. In: populations, the introduction of large-scale commercial Rupprecht CE, Dietzschold B, Koprowski H, editors. Lyssaviruses. agriculture, urbanization, loss of biodiversity within the Berlin: Springer-Verlag; 1994. p. 297–324. human biosphere, and other changes. The new ecologic 15. Ewalt PW, De Leo G. Alternative transmission modes and the evolu- landscapes have been exploited by species that can adapt tion of virulence. In: Dieckmann U, Metz JAJ, Sabelis MW, Sigmund K, editors. Adaptive dynamics of infectious diseases: in pursuit of vir- favorably to them, including many of the prominent rabies ulence management. Cambridge (UK): Cambridge University Press; maintenance hosts. Rabies viruses have recently become 2002. p. 10–25. prominent in the African ecosystem because of transmis- 16. Keeling MJ, Grenfell BT. Individual-based perspectives on R . J sion in mammals that have exploited ecologic changes that Theor Biol. 2000;203:51–61. have occurred in much of the continent. Such change is set 17. Dieckmann U. Adaptive dynamics of pathogen-host interactions. In: Dieckmann U, Metz JAJ, Sabelis MW, Sigmund K, editors. Adaptive to continue into the future, and those species that can flour- dynamics of infectious diseases: in pursuit of virulence management. ish under the new conditions will be candidate hosts for the Cambridge (UK): Cambridge University Press; 2002. p. 39–59. maintenance of pathogens. 18. Solé RV, Ferrer, R, Gonzalez-Garcia I, Quer J, Domingo E. Red Queen dynamics, competition and critical points in a model of RNA virus quasispecies. J Theor Biol. 1999;198:47–59. Acknowledgments 19. Hanski IA, Simberloff D. The metapopulation approach, its history, I thank Jenny Turton, Ken McColl, and Martyn Jeggo for conceptual domain, and application to conservation. In: Hanski IA, critically reviewing the manuscript. Gilpin ME, editors. Metapopulation biology: ecology, genetics and evolution. San Diego: Academic Press; 1997. p. 5–26. Dr Bingham completed his PhD dissertation on jackal rabies 20. Jennings WL, Schneider NJ, Lewis AL, Scatterday JE. Fox rabies in in Zimbabwe while working at the Central Veterinary Florida. J Wildl Manage. 1960;24:171–9. 21. Verts J, Storm GL. A local study of prevalence of rabies among foxes Laboratories in Harare. His interests include the ecology and evo- and striped skunks. J Wildl Dis. 1966;30:419–21. lution of infectious diseases. 22. Wandeler A, Wachendorfer G, Forster U, Krekel H, Schale W, Muller J, et al. Rabies in wild carnivores in central Europe. I. Epidemiological studies. Zentralbl Veterinarmed B. 1974;21:735–56. References 23. Kappeler A. Die orale Immunisierung von Füchsen gegen Tollwut in der Schweiz [dissertation]. Bern (Germany): University of Bern; 1. Bartlett MS. The critical community size for measles in the United States. J R Stat Soc. 1960;123:37–44. 24. Childs JE, Curns AT, Dey ME, Real LA, Feinstein L, Bjornstad ON, 2. Black FL. Measles endemicity in insular populations: critical com- et al. Predicting the local dynamics of epizootic rabies among rac- munity size and its evolutionary implications. J Theor Biol. coons in the United States. Proc Natl Acad Sci U S A. 1966;11:207–11. 2000;97:13666–71. 3. Anderson RM, May RM. Infectious diseases of humans. New York: 25. Keeling MJ. Modeling the persistence of measles. Trends Microbiol. Oxford University Press; 1991. 1997;5:513–8. 4. Grenfell B, Harwood J. (Meta)population dynamics of infectious dis- 26. Keeling MJ. Multiplicative moments and measures of persistence in eases. Trends Ecol Evol. 1997;12:395–9. ecology. J Theor Biol. 2000;205:269–81. 5. Swanepoel R, Barnard BJH, Meredith CD, Bishop GC, Bruckner GK, 27. Pacala SW, Hassell MP, May RM. Host-parasitoid associations in Foggin CM, et al. Rabies in southern Africa. Onderstepoort J Vet Res. patchy environments. Nature. 1990;344:150–3. 1993;60:325–46. 28. Tinline RR. Persistence of rabies in wildlife. In: Campbell JB, 6. Bingham J, Foggin CM, Wandeler AI, Hill FWG. The epidemiology Charlton KM, editors. Rabies. Boston: Kluwer Academic Publishers; of rabies in Zimbabwe. 1. Rabies in dogs (Canis familiaris). 1988. p. 301–22. Onderstepoort J Vet Res. 1999;66:1–10. 29. Thomson GR, Meredith CD. Rabies in bat-eared foxes in South 7. Nel LH, Sabeta CT, von Teichman B, Jaftha JB, Rupprecht CE, Africa. Onderstepoort J Vet Res. 1993;60:399–403. Bingham J. Mongoose rabies in southern Africa: a re-evaluation 30. Hofmeyr M, Hofmeyr D, Nel L, Bingham J. A second outbreak of based on molecular epidemiology. Virus Res. 2005;109:165–73. rabies in African wild dogs (Lycaon pictus) in Madikwe Game 8. Bingham J, Foggin CM, Wandeler AI, Hill FWG. The epidemiology Reserve, South Africa, demonstrating the efficacy of vaccination of rabies in Zimbabwe. 2. Rabies in jackals (Canis adustus and Canis against natural rabies challenge. Anim Conserv. 2004;7:193–8. mesomelas). Onderstepoort J Vet Res. 1999;66:11–23. 31. Randall DA, Williams SD, Kuzmin IV, Rupprecht CE, Tallents LA, 9. Cumming DHM. A case history of the spread of rabies in an African Tefera Z, et al. Rabies in endangered Ethiopian wolves. Emerg Infect country. S Afr J Sci. 1982;78:443–7. Dis. 2004;10:2214–7. 10. Cleaveland S, Dye C. Maintenance of a microparasite infecting sev- 32. Butler JRA. The ecology of domestic dogs Canis familiaris in the eral host species: rabies in the Serengeti. Parasitology. 1995;111: communal lands of Zimbabwe [dissertation]. Harare (Zimbabwe): S33–47. University of Zimbabwe; 1998. Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 9, September 2005 1341 PERSPECTIVE 33. Brooks R. Survey of the dog population of Zimbabwe and its level of 38. McColl KA, Gould AR, Selleck PW, Hooper PT, Westbury HA, rabies vaccination. Vet Rec. 1990;127:592–6. Smith JS. Polymerase chain reaction and other laboratory techniques 34. Sabeta CT, Bingham J, Nel LH. Molecular epidemiology of canid in the diagnosis of long incubation rabies in Australia. Aust Vet J. rabies in Zimbabwe and South Africa. Virus Res. 2003;91:203–11. 1993;70:84–9. 35. Nadin-Davis SA, Bingham J. Europe as a source of rabies for the rest 39. Bingham J, Hill FWG, Matema R. Rabies incubation in an African of the world. In: King AA, Fooks AR, Aubert M, Wandeler AI, edi- civet (Civettictis civetta). Vet Rec. 1994;134:528. tors. Historical perspectives of rabies in Europe and the 40. Grenfell BT, Bolker BM, Kleczkowski A. Seasonality and extinction Mediterranean basin. Paris: Office International des Épizooties; in chaotic metapopulations. Proc R Soc Lond B Biol Sci. 2004. p. 259–80. 1995;259:97–103. 36. Fekadu M, Shaddock JH, Baer GM. Intermittent excretion of rabies virus in the saliva of a dog two and six months after it had recovered Address for correspondence: John Bingham, CSIRO Australian Animal from experimental rabies. Am J Trop Med Hyg. 1981;30:1113–5. Health Laboratory, Private Bag 24, Geelong, Victoria 3220, Australia; 37. East ML, Hofer H, Cox JH, Wulle U, Wiik H, Pitra C. Regular expo- fax: 61-3-5227-5555; email: [email protected] sure to rabies virus and lack of symptomatic disease in Serengeti spotted hyenas. Proc Natl Acad Sci U S A. 2001;98:15026–31. Search 1342 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 9, September 2005 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Emerging Infectious Diseases Pubmed Central

Canine Rabies Ecology in Southern Africa

Bingham, John
Emerging Infectious Diseases , Volume 11 (9) – Sep 1, 2005
Download PDF
6 pages

Loading next page...
 
/lp/pubmed-central/canine-rabies-ecology-in-southern-africa-qdZt6OpOPx

References (78)

Publisher
Pubmed Central
ISSN
1080-6040
eISSN
1080-6059
DOI
10.3201/eid1109.050172
Publisher site
See Article on Publisher Site

Abstract

Canine Rabies Ecology in Southern Africa John Bingham* Rabies is a widespread disease in African domestic although their role has been controversial; some studies dogs and certain wild canine populations. Canine rabies indicate that they can support rabies cycles (8), and other became established in Africa during the 20th century, coin- studies indicate that they cannot maintain rabies independ- ciding with ecologic changes that favored its emergence in ently of the disease cycle in dogs (9–12). Although rabies canids. I present a conceptual and terminologic framework is a prominent disease of African canids, the mechanisms for understanding rabies ecology in African canids. The and hosts responsible for sustaining it have not been clear- framework is underpinned by 2 distinct concepts: mainte- ly elucidated. nance and persistence. Maintenance encompasses the I review the ecology of canine rabies in southern Africa, notion of indefinite transmission of infection within a local particularly with the goal of resolving the controversies on population and depends on an average transmission ratio >1. Maintenance in all local populations is inherently unsta- mechanisms of persistence. A conceptual and terminologic ble, and the disease frequently becomes extinct. framework to understand the long-term ecologic survival of Persistence, the notion of long-term continuity, depends on rabies virus in African canine hosts is proposed. the presence of rabies in >1 local population within the canine metapopulation at any time. The implications for Rabies Virus Biology understanding rabies ecology and control are reviewed, as Rabies virus is transmitted in saliva through the bite of are previous studies on rabies ecology in African canids. an infected animal. After gaining entry to the central nerv- ous system by peripheral nerves, it causes encephalitis, he ecologic persistence of pathogenic viruses has been leading to fulminant, progressive neurologic disease, char- Tthe focus of many studies (1–4). Rabies virus, a acterized by excitement, muscular paralysis, impaired lyssavirus that causes a lethal neurotropic infection of responses to social and environmental signals, and other mammals, is a pathogen for which ecologic persistence abnormal neurologic signs. The incubation period is cannot be explained adequately by pathogenetic mecha- unusually variable and can be long; clinical disease and nisms. Death of the host implies that the virus depends on virus shedding are not seen during this period. Infection of transmission to new susceptible hosts to survive. However, the salivary glands during the clinical stage leads to shed- epidemics, a frequent manifestation of rabies, deplete the ding of virions in saliva (13). number of susceptible hosts, which leads to the decline or Rabies virus has a broad mammalian host range. extinction of the virus in the affected population. How, However, in any ecologic zone, a single species, the main- then, does the virus persist? tenance host, is usually principally responsible for support- In southern Africa, rabies virus affects many host ing the virus cycle. The virus variant of the maintenance species, but rabies cycles are sustained by carnivore hosts host is intimately adapted to the host’s physiology and bio- (5,6), particularly by canine species (family Canidae), chemistry to ensure effective transmission (14). which are the focus of this paper, and by mongooses (fam- Maintenance hosts are usually extremely sensitive to their ily Herpestidae) (5,7), which will not be considered here. variant but relatively resistant to rabies virus variants of Domestic dogs (Canis familiaris) are hosts of rabies virus other species. In maintenance hosts, the probability is high in most of Africa; they cause most human rabies cases and that the virus will establish infection, will induce the contacts that require medical intervention. In southern appropriate behavioral changes, such as aggressive biting Africa, jackals (C. adustus, C. mesomelas) are also hosts, behavior, and will prolong the clinical survival period in which salivary virus shedding takes place; all of these fac- tors lead to maximal virus transmission (14). *Commonwealth Scientific and Industrial Research Organisation For a virus cycle to be successfully maintained, the (CSIRO) Australian Animal Health Laboratory, Geelong, Victoria, average transmission ratio (the average number of new Australia Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 9, September 2005 1337 PERSPECTIVE cases caused by each infected host) must be >1. At the susceptible individuals that can replicate, shed, and trans- beginning of an epidemic, this number is expressed math- mit virus efficiently to conspecifics. Maintenance hosts ematically as the basic reproductive number, R , which is live in local populations, which support indefinite trans- defined as the number of new infections generated from an mission of virus independently of other local populations. existing infection, when that infection is introduced into a Individual local populations are unlikely to maintain population composed entirely of susceptible hosts (3,15). rabies continuously because of the inherently high instabil- R is usually treated as a constant that only applies at the ity of the disease in any single local population; the disease beginning of an epidemic, when the ratio of susceptible to is normally reintroduced from other infected local popula- infected hosts is at a maximum. R will not be used in this tions. Persistence encompasses the concept of long-term article, as it precludes variability in space and time (16,17); and continuous presence of disease within a metapopula- the term average transmission ratio, as defined above, will tion. Successful persistence requires that virus is main- generally be used instead. tained in >1 local population at any time. Individuals of species other than the maintenance host Many viral pathogens depend on a constant supply of may also become infected; they are usually dead-end hosts susceptible hosts because the viral infection causes either because of low transmission ratios, which are caused by host death or durable immunity. The unstable pattern factors such as the failure to induce biting behavior, ineffi- caused by depletion and renewal of host local populations cient salivary shedding, and absence of other hosts with is a prominent feature of all carnivore rabies cycles, partic- which to interact. Occasionally, nonmaintenance hosts ularly when studied at a relatively fine geographic resolu- successfully transmit the infection to conspecifics, which tion (6,8,20–24). may lead to the establishment of a new cycle if conditions Mathematical models have shown the importance of for continual, effective transmission to conspecifics are features such as host population heterogeneity and mixing. favorable. The emergence of a new cycle requires some If a spatially heterogeneous host metapopulation experi- genetic adaptation of the virus in the new host. ences a degree of movement between local populations, a Lyssaviruses can probably adapt with relative ease because pathogen can persist over the long term even though it may their broad host range allows adaptive selection to take frequently become extinct in local populations (4,25–28). place, as evidenced by the emergence of many new cycles Metapopulation heterogeneity may be in terms of density, in the last 100 years. A mechanism to explain how such demographic structure, social interactions, and other char- adaptation may arise is the quasispecies concept, where the acteristics that influence transmission ratios. inherently high mutation rates of RNA viruses produce Maintenance and persistence of rabies are affected by variant populations of viruses through which selection can population immunity, which in effect lowers the average act (18). transmission ratio. In carnivores, population immunity against rabies is almost exclusively caused by vaccination Definitions and Concepts rather than natural infection, which is usually fatal. Two working definitions will be cited. A local popula- tion is a “set of individuals that live in the same habitat Canine Rabies in Southern Africa patch and therefore interact with each other” (19). A In addition to the domestic dog, 3 wild canids have metapopulation is a “set of [discrete] local populations been implicated as independent maintenance hosts of within some larger area, where typically migration from rabies in southern Africa: the side-striped jackal (C. adus- one local population to at least some other patches is pos- tus), the black-backed jackal (C. mesomelas), and the bat- sible” (19). The demographic trends of local populations eared fox (Otocyon megalotis) (5,6,8,29). Rabies cases are asynchronous, particularly where migration between have also been reported in other African canids, such as them is relatively low. In this article, the definitions of African wild dogs (Lycaon pictus) (30) and Ethiopian local population and metapopulation may apply to either wolves (C. simensis) (31), but these species do not appear the host or the virus. To use an analogy borrowed from to support extended virus cycles independent of other ecology, the host local population may be viewed as a hosts. resource patch for the pathogen. In Africa, dogs are intimately dependent on humans for Maintenance is the notion of indefinite transmission of food and shelter (32,33), and this association means that virus through members of a host population. (In this con- dog populations can be correlated, in size as well as distri- text “indefinite” transmission does not mean “permanent” bution, with human populations. During the 20th century, but rather denotes an open-ended cycle that is dependent the human population of Africa expanded enormously, and on availability of susceptible hosts.) The average transmis- the dog population expanded in parallel (33). Social sion ratio must be >1 for virus maintenance to be success- changes, such as urbanization, resulted in an increase in ful. A maintenance host is a member of a population of human and dog movement. Rabies persistence would have 1338 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 9, September 2005 Rabies in Southern Africa been enhanced in such a dog metapopulation consisting of tis are closely related but distinct (34). In addition, viruses more numerous local populations and greater movement of all fall within the cosmopolitan lineage that includes many infected dogs. other dog and wild canine virus variants from other regions Such a prediction is borne out by historical records. of the world (35). This finding supports the epidemiologic Rabies in sub-Saharan Africa is a disease of modern times; observations that all present-day dog, jackal, and O. mega- no firm evidence exists of its occurrence before the late lotis rabies viruses in southern Africa stem from a single, 19th century. The first confirmed outbreaks, in South recently introduced virus derived from domestic dogs. Africa in 1893 and Southern Rhodesia (now called However, molecular techniques are not precise enough to Zimbabwe) in 1902, were in domestic dogs, and their ori- indicate which species, dogs or the 3 wildlife species, gin was traced to distant lands (5). The initial outbreaks maintains the virus cycles that are found in wildlife. were temporally and spatially sporadic, and rabies appar- Epidemiologic evidence is required to determine this ently could not become established. These outbreaks were (5,8,29). followed by increasingly frequent, but initially sporadic, outbreaks, until the disease was continuously present in Review of African Canine Rabies Studies national records, as can be seen in the annual reports of the I propose that African canine rabies ecology must be departments of animal health of various African countries understood through the distinct concepts of maintenance from 1892 to 1960. and persistence. An alternative mechanism proposed for Rabies in jackal species appeared in southern and east- rabies persistence in African domestic dogs includes an ern African countries after the introduction of the disease infectious healthy carrier status (10,36). One study pro- in dogs. In Zimbabwean C. adustus populations, rabies poses this mechanism for rabies in spotted hyenas occurred in large, dense, moving epidemics in commercial (Crocuta crocuta, Carnivora: Hyaenidae), on the basis of farming areas (8). The jackal index cases of the epidemics rabies virus RNA detected in saliva of healthy hyenas by were usually associated with cases in dogs, which indi- polymerase chain reaction, although virus isolation, cates that these epidemics were initiated by dog rabies arguably the more important test, was unsuccessful from cycles; once initiated, however, the epidemics were main- these samples (37). A second mechanism by which rabies tained independent of dogs. The moving epidemics termi- may persist is the concept of long incubators, which carry nated at the geographic limits of the C. adustus population infection through quiescent periods to restart epidemics dominance. when the host density has recovered. Long incubators Both jackal species reach high densities in commercial have been reported mainly in humans and other nonmain- farming environments. Jackal rabies occurs predominantly tenance species (38,39). No evidence currently shows that in these areas, but it is virtually absent from most national carrier animals or long incubators play a role in the per- parks, despite substantial jackal populations (8). sistence of rabies cycles in canine hosts, perhaps because Commercial farming practices appear to provide ecologic they do not occur frequently enough to be obvious. conditions that are highly favorable for jackals and jackal Although they should not be ignored, these concepts are rabies. What these conditions are is unclear, but they may difficult to demonstrate scientifically and even more diffi- include abundant resources, increased demographic cult to quantify in terms of their ecologic importance for turnover, and the absence of competitors such as dogs and virus persistence. wild scavengers. Previous studies have questioned the ability of jackals to In southern Africa, rabies in C. mesomelas and O. support rabies virus cycles (9–11). These studies have not megalotis predominantly occurs in the absence of domes- distinguished between the ability of species to support tic dogs or rabies in other carnivores. Given the general pathogen cycles (i.e., maintenance) and the concept of long- lack of associated rabies cases in other species, C. term persistence. Acknowledging this distinction would mesomelas and O. megalotis are likely maintenance host show that local populations of canine species may maintain populations, capable of maintaining the virus cycle inde- epidemics independently and may be free of rabies for peri- pendent of other species. In C. mesomelas and Otocyon ods, often long periods, between epidemics. At the level of populations, the mechanisms of rabies maintenance are the local population, this pattern is essentially similar in poorly understood; because surveillance is scanty, discern- domestic dogs, jackals, and other canids (e.g., African wild ing true spatial and temporal disease patterns is difficult dogs [30]). Domestic dogs may appear to support rabies (5,8,29). infection endemically, whereas jackals do not (11), simply Molecular epidemiology studies have indicated that, in because more numerous discrete local dog populations are Zimbabwe and South Africa, rabies viruses from dogs and within the study area than are jackal populations. jackals are phylogenetically similar and do not fall into Considering rabies ecology through the concepts pre- host-distinguishable lineages, while viruses of O. megalo- sented here would clarify some of the confusion created by Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 9, September 2005 1339 PERSPECTIVE these studies (9–11). For example, a study (11) that used a too low to maintain the chain of infection.” However, the mathematical model concluded that “the side-striped jack- dense moving epidemics, which lasted several years and al population itself does not seem able to support rabies occurred in the absence of cases in other species (8), imply infection endemically, i.e., without frequent reintroduction that host density was not a limiting factor in jackal epi- from outside sources of infection.” While reintroductions demics. Once again, we can resolve this apparent contra- of infection are certainly an important feature in C. adus- diction by considering these populations of jackals to be tus rabies, reintroduction is probably infrequent, given that capable of cycle maintenance but not persistence. most C. adustus cases reported in 46 years followed 5 dog- Transmission is efficient within local populations, but high to-jackal initiation events (8). The contradiction is transmission ratios are transient. The jackal populations of resolved once the concepts of maintenance and persistence Zimbabwe and the rabies viruses they support should not are applied. Hence, C. adustus is capable of maintaining be considered metapopulations because they do not have, rabies cycles independent of other species, but rabies as dog populations do, the spatial separation or interpopu- cycles have not been persistent. lation migration that would be necessary for them to be Terms such as reservoir and endemic do not provide the considered metapopulations. This absence of a metapopu- conceptual clarity necessary to understand rabies ecology lation structure explains the failure of rabies persistence in (10,11). In a study that acknowledges the complexities of jackal populations, and this absence, rather than their defining the term and uses canine rabies as an example, inability to maintain virus, distinguishes jackals from dogs Haydon et al. (12) state that a reservoir is a population “in as hosts of rabies. which the pathogen can be permanently maintained.” However, this definition is problematic because the term Control of Rabies in Africa “permanently maintained” is ambiguous. This study Applying the metapopulation principle to canine rabies implies that dogs, but not jackals, are reservoirs because in Africa reinforces conventional principles of control: they are permanent hosts, yet many dog populations, as employing vaccination or culling in affected host popula- with many jackal populations, do not permanently support tions and minimizing movement of infected hosts. For rabies cycles. Such definitions fail to provide a convincing many decades, controlling rabies in Africa, has been the argument that essential distinctions exist between dogs and mandate of governments. Vaccination programs for dogs jackals in their ability to support rabies cycles. The study generally consisted of periodic visits by a government vac- by Haydon et al. also defines a reservoir in relation to a tar- cination team to communities, which were seen as compli- get population, which is “the population of concern or ant recipients. While in some cases such government- interest to us” and which requires protection. Such anthro- initiated control efforts arguably had some effect on reduc- pocentric definitions of pathogen behavior, although hav- ing rabies, they did not cause any long-term trend in reduc- ing some conceptual value for protecting human health and ing rabies in maintenance hosts or humans. African interests, are unhelpful for understanding the biologic governments have been unable to sustain the level of mechanisms of pathogen emergence and persistence. resource commitment needed to maintain effective levels The scale at which ecologic systems are examined has of vaccination coverage. The metapopulation principle implications, since disease frequency is less stable in local indicates that with increasing dog population density, size, populations than in metapopulations (40). Hence, a farmer and movement, rabies control will require ever-increasing will perceive rabies on his property as epidemic in nature, resources. Traditional methods that have not worked well with intense outbreaks separated by long periods of in the past are likely to be even less effective in the future. absence, while a national epidemiologist may claim that Instead, a completely different approach to controlling the disease is endemic in his country. Both observations rabies is needed. Perhaps this approach should be based on are correct, but observers perceive the epidemiology dif- community-driven initiatives, where the role of govern- ferently because they view the disease frequency at differ- ments focuses on support activities such as surveillance, ent scales. The lump analysis of national rabies case data information dissemination, and legislation. Since dogs are of Zimbabwe (10,11) led to a blending and masking of dis- an integral and dependent part of human communities, ease patterns, giving these researchers the erroneous community-driven initiatives for rabies control may be impression that rabies frequency in dogs was more stable more sustainable than those directed by governments. than it was in jackals. While the transmission ratio, as influenced by host den- Conclusions sity, for example, is the only determinant of maintenance, In recent decades, the frequency of rabies has increased it is not the sole determinant of persistence. In discussing in Africa. Controlling this disease will require a deeper rabies in Zimbabwean jackal populations, Rhodes et al. understanding of its biology. When interpreting rabies case (11) suggest that the “average jackal population density is data for epidemiologic analysis, we must distinguish 1340 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 9, September 2005 Rabies in Southern Africa 11. Rhodes CJ, Atkinson RPD, Anderson RM, Macdonald DW. Rabies in between the concepts of maintenance (the ability of local Zimbabwe: reservoir dogs and the implications for disease control. populations to support a disease cycle) and persistence (the Philos Trans R Soc Lond B Biol Sci. 1998;353:999–1010. presence of >1 infected local population in a host metapop- 12. Haydon DT, Cleaveland S, Taylor LH, Laurenson MK. Identifying ulation). To clearly conceptualize the ecology of canine reservoirs of infection: a conceptual and practical challenge. Emerg Infect Dis. 2002;8:1468–73. rabies, we must use lucid, appropriate definitions for virus- 13. Charlton KM. The pathogenesis of rabies and other lyssaviral infec- host interactions and epidemiologic patterns. tions: recent studies. In: Rupprecht CE, Dietzschold B, Koprowski H, The ecology of many ecosystems has changed dramat- editors. Lyssaviruses. Berlin: Springer-Verlag; 1994. p. 95–119. ically in recent centuries because of the increase in human 14. Wandeler AI, Nadin-Davis SA, Tinline RR, Rupprecht CE. Rabies epidemiology: some ecological and evolutionary perspectives. In: populations, the introduction of large-scale commercial Rupprecht CE, Dietzschold B, Koprowski H, editors. Lyssaviruses. agriculture, urbanization, loss of biodiversity within the Berlin: Springer-Verlag; 1994. p. 297–324. human biosphere, and other changes. The new ecologic 15. Ewalt PW, De Leo G. Alternative transmission modes and the evolu- landscapes have been exploited by species that can adapt tion of virulence. In: Dieckmann U, Metz JAJ, Sabelis MW, Sigmund K, editors. Adaptive dynamics of infectious diseases: in pursuit of vir- favorably to them, including many of the prominent rabies ulence management. Cambridge (UK): Cambridge University Press; maintenance hosts. Rabies viruses have recently become 2002. p. 10–25. prominent in the African ecosystem because of transmis- 16. Keeling MJ, Grenfell BT. Individual-based perspectives on R . J sion in mammals that have exploited ecologic changes that Theor Biol. 2000;203:51–61. have occurred in much of the continent. Such change is set 17. Dieckmann U. Adaptive dynamics of pathogen-host interactions. In: Dieckmann U, Metz JAJ, Sabelis MW, Sigmund K, editors. Adaptive to continue into the future, and those species that can flour- dynamics of infectious diseases: in pursuit of virulence management. ish under the new conditions will be candidate hosts for the Cambridge (UK): Cambridge University Press; 2002. p. 39–59. maintenance of pathogens. 18. Solé RV, Ferrer, R, Gonzalez-Garcia I, Quer J, Domingo E. Red Queen dynamics, competition and critical points in a model of RNA virus quasispecies. J Theor Biol. 1999;198:47–59. Acknowledgments 19. Hanski IA, Simberloff D. The metapopulation approach, its history, I thank Jenny Turton, Ken McColl, and Martyn Jeggo for conceptual domain, and application to conservation. In: Hanski IA, critically reviewing the manuscript. Gilpin ME, editors. Metapopulation biology: ecology, genetics and evolution. San Diego: Academic Press; 1997. p. 5–26. Dr Bingham completed his PhD dissertation on jackal rabies 20. Jennings WL, Schneider NJ, Lewis AL, Scatterday JE. Fox rabies in in Zimbabwe while working at the Central Veterinary Florida. J Wildl Manage. 1960;24:171–9. 21. Verts J, Storm GL. A local study of prevalence of rabies among foxes Laboratories in Harare. His interests include the ecology and evo- and striped skunks. J Wildl Dis. 1966;30:419–21. lution of infectious diseases. 22. Wandeler A, Wachendorfer G, Forster U, Krekel H, Schale W, Muller J, et al. Rabies in wild carnivores in central Europe. I. Epidemiological studies. Zentralbl Veterinarmed B. 1974;21:735–56. References 23. Kappeler A. Die orale Immunisierung von Füchsen gegen Tollwut in der Schweiz [dissertation]. Bern (Germany): University of Bern; 1. Bartlett MS. The critical community size for measles in the United States. J R Stat Soc. 1960;123:37–44. 24. Childs JE, Curns AT, Dey ME, Real LA, Feinstein L, Bjornstad ON, 2. Black FL. Measles endemicity in insular populations: critical com- et al. Predicting the local dynamics of epizootic rabies among rac- munity size and its evolutionary implications. J Theor Biol. coons in the United States. Proc Natl Acad Sci U S A. 1966;11:207–11. 2000;97:13666–71. 3. Anderson RM, May RM. Infectious diseases of humans. New York: 25. Keeling MJ. Modeling the persistence of measles. Trends Microbiol. Oxford University Press; 1991. 1997;5:513–8. 4. Grenfell B, Harwood J. (Meta)population dynamics of infectious dis- 26. Keeling MJ. Multiplicative moments and measures of persistence in eases. Trends Ecol Evol. 1997;12:395–9. ecology. J Theor Biol. 2000;205:269–81. 5. Swanepoel R, Barnard BJH, Meredith CD, Bishop GC, Bruckner GK, 27. Pacala SW, Hassell MP, May RM. Host-parasitoid associations in Foggin CM, et al. Rabies in southern Africa. Onderstepoort J Vet Res. patchy environments. Nature. 1990;344:150–3. 1993;60:325–46. 28. Tinline RR. Persistence of rabies in wildlife. In: Campbell JB, 6. Bingham J, Foggin CM, Wandeler AI, Hill FWG. The epidemiology Charlton KM, editors. Rabies. Boston: Kluwer Academic Publishers; of rabies in Zimbabwe. 1. Rabies in dogs (Canis familiaris). 1988. p. 301–22. Onderstepoort J Vet Res. 1999;66:1–10. 29. Thomson GR, Meredith CD. Rabies in bat-eared foxes in South 7. Nel LH, Sabeta CT, von Teichman B, Jaftha JB, Rupprecht CE, Africa. Onderstepoort J Vet Res. 1993;60:399–403. Bingham J. Mongoose rabies in southern Africa: a re-evaluation 30. Hofmeyr M, Hofmeyr D, Nel L, Bingham J. A second outbreak of based on molecular epidemiology. Virus Res. 2005;109:165–73. rabies in African wild dogs (Lycaon pictus) in Madikwe Game 8. Bingham J, Foggin CM, Wandeler AI, Hill FWG. The epidemiology Reserve, South Africa, demonstrating the efficacy of vaccination of rabies in Zimbabwe. 2. Rabies in jackals (Canis adustus and Canis against natural rabies challenge. Anim Conserv. 2004;7:193–8. mesomelas). Onderstepoort J Vet Res. 1999;66:11–23. 31. Randall DA, Williams SD, Kuzmin IV, Rupprecht CE, Tallents LA, 9. Cumming DHM. A case history of the spread of rabies in an African Tefera Z, et al. Rabies in endangered Ethiopian wolves. Emerg Infect country. S Afr J Sci. 1982;78:443–7. Dis. 2004;10:2214–7. 10. Cleaveland S, Dye C. Maintenance of a microparasite infecting sev- 32. Butler JRA. The ecology of domestic dogs Canis familiaris in the eral host species: rabies in the Serengeti. Parasitology. 1995;111: communal lands of Zimbabwe [dissertation]. Harare (Zimbabwe): S33–47. University of Zimbabwe; 1998. Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 9, September 2005 1341 PERSPECTIVE 33. Brooks R. Survey of the dog population of Zimbabwe and its level of 38. McColl KA, Gould AR, Selleck PW, Hooper PT, Westbury HA, rabies vaccination. Vet Rec. 1990;127:592–6. Smith JS. Polymerase chain reaction and other laboratory techniques 34. Sabeta CT, Bingham J, Nel LH. Molecular epidemiology of canid in the diagnosis of long incubation rabies in Australia. Aust Vet J. rabies in Zimbabwe and South Africa. Virus Res. 2003;91:203–11. 1993;70:84–9. 35. Nadin-Davis SA, Bingham J. Europe as a source of rabies for the rest 39. Bingham J, Hill FWG, Matema R. Rabies incubation in an African of the world. In: King AA, Fooks AR, Aubert M, Wandeler AI, edi- civet (Civettictis civetta). Vet Rec. 1994;134:528. tors. Historical perspectives of rabies in Europe and the 40. Grenfell BT, Bolker BM, Kleczkowski A. Seasonality and extinction Mediterranean basin. Paris: Office International des Épizooties; in chaotic metapopulations. Proc R Soc Lond B Biol Sci. 2004. p. 259–80. 1995;259:97–103. 36. Fekadu M, Shaddock JH, Baer GM. Intermittent excretion of rabies virus in the saliva of a dog two and six months after it had recovered Address for correspondence: John Bingham, CSIRO Australian Animal from experimental rabies. Am J Trop Med Hyg. 1981;30:1113–5. Health Laboratory, Private Bag 24, Geelong, Victoria 3220, Australia; 37. East ML, Hofer H, Cox JH, Wulle U, Wiik H, Pitra C. Regular expo- fax: 61-3-5227-5555; email: [email protected] sure to rabies virus and lack of symptomatic disease in Serengeti spotted hyenas. Proc Natl Acad Sci U S A. 2001;98:15026–31. Search 1342 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 9, September 2005

Journal

Emerging Infectious Diseases – Pubmed Central

Published: Sep 1, 2005

There are no references for this article.