Emerging Infectious Diseases Volume 11 Issue 9

2005·7.9 MB·English

by  CDC

APeer-Reviewed Journal Tracking and Analyzing Disease Trends pages 1337–1502
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D. PeterDrotman
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Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 9, September 2005
A Peer-Reviewed Journal Tracking and Analyzing Disease Trends Vol. 11, No. 9, September 2005
On the Cover Dead Crow Density and
Jackson Pollock (1912–1956) West Nile Virus Monitoring . . . . . .1370
Autumn Rhythm (Number 30) (1950) M. Eidson et al.
Enamel on canvas Persons in counties of New York State with high
(266.7 cm × 525.8 cm) dead crow densities had elevated risk for disease.
The Metropolitan Museum of Art,
George A. Hearn Fund, 1957 (57.92) Dengue Virus Type 3,
Photograph copyright 1998 Brazil, 2002 . . . . . . . . . . . . . . . . . . .1376
The Metropolitan Museum of Art
R.M.R. Nogueira et al.
About the Cover p. 1500 An explosive epidemic of DENV-3 in 2002 was the
most severe dengue epidemic reported in Brazil
since dengue viruses were introduced.
Perspective
Trypanosomiasis Control,
Rabies in Southern Africa . . . . . . .1337
Democratic Republic of Congo . .1382
J. Bingham
P. Lutumba et al.
Understanding the persistence of rabies in multiple
Efforts to control human trypanosomiasis, which
canine hosts in southern Africa requires applying
sharply reduced disease incidence, must be
the principles of metapopulation biology.
sustained.
Synopsis
Staphylococcus epidermidis
and Clarithromycin . . . . . . . . . . . .1389
Mosquitoborne Disease and
M. Sjölund et al.
Hydrologic Monitoring . . . . . . . . . .1343
Short course of antimicrobial therapy can select
J. Shaman and J.F. Day
resistant bacteria that persist for 4 years or longer.
West Nile virus transmission in Florida can be
monitored by using modeled hydrology.
Simulated Anthrax Attacks
and Syndromic Surveillance . . . . .1394
Research p. 1347
J.D. Nordin et al.
Bioterrorism surveillance systems can be assessed
Variant Creutzfeldt-Jakob
using modeling to simulate real-world attacks.
Disease . . . . . . . . . . . . . . . . . . . . . .1351
E.D. Belay et al. West Nile Virus–infected
Reports of secondary bloodborne transmission of
Mosquitoes, Louisiana, 2002 . . . .1399
vCJD add to the uncertainty about the future of the
M.S. Godsey, Jr. et al.
vCJD outbreak.
Culex quinquefasciatuswas identified as probable
p. 1352
vector.
Antiviral Drug Use during
Influenza Pandemic . . . . . . . . . . . .1355
Legionellosis from Legionella
R. Gani et al.
pneumophila Serogroup 13 . . . . .1405
Impact of different antiviral drug treatment strategies
B. Faris et al.
on hospitalizations during an influenza pandemic is
L. pneumophilaserogroup 13 may be
evaluated.
underrecognized.
Fluoroquinolone-resistant
Malaria Attributable to
Escherichia coli . . . . . . . . . . . . . . .1363
the HIV-1 Epidemic . . . . . . . . . . . . .1410
K. Kuntaman et al.
E.L. Korenromp et al.
High prevalence may be due to clonal spread and
HIV-1 has substantially increased malaria in
emergence of resistant strains.
southern Africa.
Molecular Epidemiology of
SARS-associated Coronavirus . . .1420
W. Cao et al.
A Peer-Reviewed Journal Tracking and Analyzing Disease Trends Vol. 11, No. 9, September 2005
Viral adaptation to the host may be occurring under
selective immune pressure.
1473 Human Infection with Rickettsia
Historical Review honei, Thailand
J. Jiang et al.
Malaria in Kenya’s 1476 Pediatric Bacterial Carriage,
Western Highlands . . . . . . . . . . . . .1425 Vaccination Implications
G.D. Shanks et al. S.H. Factor et al.
Reemergence of epidemics in tea plantations will p. 1426 1480 Human Herpesvirus 8 and
likely result in antimalarial-drug resistance.
Pulmonary Hypertension
E. Nicastri et al.
Dispatches
1483 Surveillance for Early Anthrax
Detection
1433 Protective Behavior and West Nile
E.M. Begier et al.
Virus Risk
M. Loeb et al.
Commentary
1437 West Nile Virus Detection
O.A. Ohajuruka et al.
1487 Syndromic Surveillance in
1440 Tularemia Outbreak, Sweden, 2003 Bioterrorist Attacks
L. Payne et al. A.F. Kaufmann et al.
1443 Chromobacterium violaceum,
Brazil Letters
I.C. de Siqueira et al.
1446 HIV and Simian Immunodeficiency 1489 Telithromycin-resistant
Virus Surveillance Streptococcus pneumoniae
A. Schaefer et al. 1490 Human-Animal Disease
1449 West Nile Virus Isolation in Human Surveillance
and Mosquitoes, Mexico 1491 VanB-VanC1 Enterococcus
D. Elizondo-Quiroga et al.
gallinarum, Italy
1453 Cyclosporiasis Outbreak,
1493 Empyema Thoracis from
Indonesia
SalmonellaCholeraesuis
M.C.A. Blans et al.
1494 Asymptomatic Yersinia pestis
1456 Plague from Eating Raw Camel
Infection
Liver p. 1443
A.A. Bin Saeed et al. 1496 Sporotrichosis, Plain of Jars, Lao
1458 Melioidosis, Northeastern Brazil 1497 West Nile Virus Antibodies in
D.B. Rolim et al. Colombian Horses
1461 Multidrug-resistant Tuberculosis 1498 Wild Poliovirus Type 1, Central
Detection, Latvia African Republic
G. Skenders et al.
1464 ββ-Lactam Resistance and
News & Notes
Enterobacteriaceae
J.M. Whichard et al.
About the Cover
1467 Perinatal Group B Streptococcal 1500 Oneness, Complexity, and the
Disease Prevention Distribution of Disease
C.A. Morin et al.
1470 Characterizing Vancomycin-
EID Online:
resistant Enterococci
As of January 2005, summaries of
C.R. Sherer et al.
emerging infectious disease conferences
are published online only.
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
notion of indefinite transmission of infection within a local I review the ecology of canine rabies in southern Africa,
population and depends on an average transmission ratio particularly with the goal of resolving the controversies on
>1. Maintenance in all local populations is inherently unsta- mechanisms of persistence. Aconceptual 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,
The ecologic persistence of pathogenic viruses has been leading to fulminant, progressive neurologic disease, char-
the 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-
0
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
0
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
0
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. Alocal 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 tisare 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 RNAdetected 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). Asecond 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. adustuspopulation 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
tusrabies, reintroduction is probably infrequent, given that capable of cycle maintenance but not persistence.
most C. adustuscases 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
between the concepts of maintenance (the ability of local 11. Rhodes CJ, Atkinson RPD, Anderson RM, Macdonald DW. Rabies in
populations to support a disease cycle) and persistence (the Zimbabwe: reservoir dogs and the implications for disease control.
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
rabies, we must use lucid, appropriate definitions for virus- Infect Dis. 2002;8:1468–73.
host interactions and epidemiologic patterns. 13. Charlton KM. The pathogenesis of rabies and other lyssaviral infec-
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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
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Laboratories in Harare. His interests include the ecology and evo- 21. Verts J, Storm GL. Alocal study of prevalence of rabies among foxes
lution of infectious diseases. and striped skunks. J Wildl Dis. 1966;30:419–21.
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J, et al. Rabies in wild carnivores in central Europe. I.
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