Public Health Significance of Urban Pests
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tant for people residing in the areas affected. A number of cities in central Colorado and nearby Cheyenne, Wyoming, also have experienced occasional plague epizootics among
fox squirrel populations that live in the urban deciduous forests found in these cities, and a single human plague case was associated with these animals in Denver, Colorado
Hudson et al., 1971. It is believed that fox squirrels, which are not native to the region, acquire plague bacteria from rock squirrels or other native species that are common hosts
of plague in this region. In another report, a gray squirrel kept as a pet was implicated as the source of an infectious bite that resulted in a human tularaemia case in Arkansas
Magee et al., 1989. Acute T. gondii infections have caused fatalities among gray squir- rels, but the epidemiological significance of this observation is unknown Roher et al.,
1981. Gray squirrels also were found naturally infected with LB spirochetes in the United Kingdom Craine et al., 1997. Another report suggested that five patients in
Kentucky had contracted spongiform encephalopathy as a result of eating the brains of tree squirrels species not given that perhaps contained a prion-like agent Berger,
Weisman Weisman, 1997. American red squirrels in western North America have been implicated as important hosts for a soft tick O. hermsi that transmits relapsing
fever spirochetes B. hermsii to people. These same squirrels also are susceptible to infec- tion with B. hermsii and are thought to be sources of infection for feeding O. hermsi
Burgdorfer Mavros 1970; Burgdorfer 1976. Although rarely reported in rodents, a case of rabies was identified in a fox squirrel Cappucci, Emmons Sampson, 1972.
13.4.4.2. Flying squirrels
In North America, the southern flying squirrel was implicated as a source of typhus cau- sed by a R. prowazekii-like agent. Transmission of this rickettsial agent to people, presu-
mably occurred through the bites of flying squirrel ectoparasites fleas or lice, which can be found on these squirrels and in the nests they build in attics or wall spaces McDade
et al., 1980.
13.4.4.3. Ground squirrels and antelope ground squirrels
Numerous ground squirrel species Spermophilus spp. and white-tailed antelope ground squirrels have been implicated as hosts of Y. pestis, the causative agent of plague in North
America Gage, Ostfeld Olson, 1995. Among the most important of these species are the rock squirrel and the closely related Beechey California ground squirrel. Both spe-
cies occur frequently in peridomestic environments, and Beechey ground squirrels are common in many recreational sites in California and nearby areas. Rock squirrels and
Beechey ground squirrels are considered the most significant sources of Y. pestis infection in people in the United States, due both to their presence in peridomestic environments
and to one of their common fleas, O. montana formerly Diamanus montanus, which is the primary vector of plague in people in this country. Other western ground squirrels
Spermophilus spp. have been reported to be infected with Y. pestis or F. tularensisHopla, 1974; Jellison, 1974; Barnes, 1982. Probably the most important among these is the gol-
den-mantled ground squirrel, which is often mistaken for a large chipmunk and fre- quently digs its burrows near home sites or recreational sites in mountainous areas of
western North America. Yersinia pestis-positive samples have been reported frequently from these ground squirrels, and in certain California mountain ranges they have been
implicated as likely sources of infectious fleabites for human cases of plague. The white-
Non-commensal rodents and lagomorphs
446
gone splenectomies. The taxonomical and etiological status of these B. microti-like agents is currently a topic of much debate, but there seems to be general agreement that this
complex of parasitic protozoa poses a risk to people in certain tick-infested areas, inclu- ding those undergoing urbanization. The primary vectors of these agents are various
ticks of the genus Ixodes, including the castor bean tick in Europe and the deer tick and the western black-legged tick in North America. Because these same vectors also trans-
mit LB and HGA, areas at risk for these last two diseases also are likely to be at risk for babesiosis caused by B. microti or closely related agents. The major rodent hosts for B.
microti
-like agents in Europe are various voles primarily Microtus spp. and Apodemus mice; North American hosts include voles primarily Microtus spp. and Peromyscus mice.
13.4.3.4. Echinococci
Alveolar echinococcosis is a rare, but severe zoonosis due to the hepatic development of the fox tapeworm. The definitive hosts are various carnivores, including wild foxes. The
intermediate hosts are various rodents, including voles, lemmings and mice. Viel and col- leagues 1999 demonstrated that densities of water voles are a risk factor for human
alveolar echinococcosis in France. Domestic dogs and cats can be sources of human infec- tion, if these animals are allowed to hunt and consume non-commensal rodents infected
with cysts bearing the larval stages of E. multilocularis.
13.4.3.5. Capillaria
Capillaria hepatica is a nematode that affects a wide range of mammal hosts, including
humans. In people, it causes a rare, but potentially fatal infestation of the liver that typi- cally manifests as acute hepatitis hepatic capillariasis with marked eosinophilia.
Capillaria hepatica has been found nearly worldwide, primarily as a parasite of the hepa-
tic parenchyma of a number of rodent species. In the Canton of Geneva, Switzerland, Reperant Deplazes 2005 trapped 664 rodents that belonged to five non-commensal
species and found a significant cluster of C. hepatica infections in three rodent species in rural and urbanized areas in the northern part of the canton. These rodents included the
yellow-necked mouse, in which the overall prevalence of infestations was 7, while in some sites prevalences reached 20 in the bank vole and the northern water vole.
13.4.4. Disease associations with particular types of rodents
The following subsections list certain noteworthy risks of disease posed by the rodent groups listed in section 13.2 of this chapter.
13.4.4.1. Tree squirrels
Several cases of leptospirosis, rickettsial infections and TBE have been reported in various tree squirrels, but these animals usually do not play important roles as reservoirs for these
infections. Squirrels can also carry many species of ticks, mites and fleas, but their tree- dwelling habits prevent them from exchanging ectoparasites with most ground-dwel-
ling rodents. With the few exceptions noted below, tree squirrels rarely have been repor- ted to be involved in epizootics or to serve as sources of disease agents that infected people.
One report noted that tularaemia infections in Siberia had spread from hares to red squir- rels, causing deaths among the latter, a situation that could be epidemiologically impor-
Public Health Significance of Urban Pests
449
Pasteurella , as well as helminth species, that cause alveolar echinococcosis, clonorchiasis
and other ailments Monzingo Hibler, 1987; Marquardt, Demaree Grieve, 2000; Dunlap Thies, 2002; Jordan et al., 2005; Lawson et al., 2005. An outbreak of blasto-
mycosis in Wisconsin was associated with children having contact with a beaver lodge and picking up soil associated with the lodge Klein et al., 1986; Gaus, Baumgardner
Paretsky, 1996.
13.4.4.6. Voles and other microtine rodents
Voles and other microtine rodents are important hosts of many zoonotic and vector-borne diseases. Species of Microtusvoles have been found infected with F. tularensis, Y. pestis, Y.
pseudotuberculosis , R. rickettsii, L. monocytogenes, Bordetella bronchiseptica, Pneumocystis
carinii , Pasteurella spp., Brucella spp., Salmonella spp. and Streptococcus spp. Hopla, 1974;
Gage, Ostfeld Olson, 1995; Soveri et al., 2000. Voles are particularly important as hosts of tularaemia, which has been detected in Microtus spp. in Austria, Belgium, the Czech
Republic, France, Norway, Poland, Romania, the Russian Federation, Slovakia and Turkey Olsuf’ev Dunaeva, 1960. Common voles are very sensitive to tularaemia and
can die 4–10 days after being inoculated with only a few F. tularensis organisms. The high level of bacteraemia 10
7
–10
8
F. tularensis ml of blood commonly experienced by
infected voles also enables these animals to serve as sources for infecting feeding tick vec- tors. During winter epizootics, F. tularensis can be transmitted between voles through
cannibalism. Microtusvoles infected with Y. pestis have been identified near human habi- tations in California. Other voles, especially the meadow vole, are considered important
hosts of the etiological agents of tularaemia F. tularensis and RMSF R. rickettsii. Meadow voles also are common hosts of larval and nymphal American dog ticks and
wood ticks, which are primary vectors of both tularaemia and RMSF in different regions of North America. Northern water voles also are important hosts of tularaemia in
Europe, including the former Union of Soviet Socialist Republics Hopla, 1974. Finally, muskrats frequently have been found infected with F. tularensis holarctica type B tula-
raemia strains in Europe and North America Hopla, 1974.
Other pathogens have been discovered in microtine rodents in Europe and North America. Among common voles in Europe, the prevalences of Listeria, Y. pseudotuber-
culosis and erysipeloid bacteria were 0.6–1.6, 0.1–0.5, and 0.3–2.2, respectively. The
common vole was infected predominantly with the grippotyphosa serotype of Leptospira interrogans
90, and the root vole carried a variety of L. interrogans serotypes, inclu- ding javanica, pomona, hebdomadis and grippotyphosa Karaseva, 1963, 1971; Rosicky
Sebek, 1974. Viel and colleagues 1999 also demonstrated that population densities of northern water voles are a risk factor for alveolar echinococcosis in people. Other micro-
tine rodents, including Microtus voles and lemmings Lemmus spp., can also serve as intermediate hosts for E. multilocularis, the agent that causes alveolar echinococcosis. In
Alberta, Canada, southern red-backed voles, meadow voles and long-tailed voles were found to be infected with Giardia spp. Wallis et al., 1984. Microtine rodents are also
commonly infected with the causative agent of yersiniosis Y. pseudotuberculosis. Notably, the prevalence of Y. pseudotuberculosis in voles in urban and suburban areas was higher
than that observed in commensal rodents Iushchenko, 1970. Recently, a number of out- breaks of yersiniosis, primarily in the Russian Federation, have been linked to eating raw
Non-commensal rodents and lagomorphs
448
tailed antelope ground squirrel, which can be abundant near the homes of people in the south-western United States, is commonly infected with Y. pestis and carries fleas, parti-
cularly Thrassis bacchi, that can transmit plague bacteria to people Montman, Barnes Maupin, 1986. Recently, B. washoensis was isolated from Beechey ground squirrels in
the Sierra Nevada mountains of western Nevada Kosoy et al., 2003. Prior to this report, B. washoensis
had been reported only in a man with myocarditis, and it was suggested that this bacterium might have been the cause of his illness and might represent the etio-
logical agent of a previously unrecognized zoonosis that is maintained in ground squir- rels. Richardson’s ground squirrels and prairie dogs also have been reported to harbour
Bartonella spp. Stevenson et al., 2003; Jardine et al., 2005.
13.4.4.4. Chipmunks
