Public Health Significance of Urban Pests
451
Another important group of sigmodontine rodents are the wood rats Neotoma spp., which occur throughout much of North America. A number of species in the western
United States are commonly found to be infected with Y. pestis and act as significant hosts for this bacterium and certain species of fleas that transmit it Gage, Ostfeld Olson,
1995. Wood rats are also hosts of a recently recognized arenavirus Whitewater Arroyo virus, which is of unknown significance to human health Fulhorst et al., 1996; Kosoy
et al., 1996. Moreover, these rats are important hosts in the far western United States for the immature stages of western black-legged ticks, which transmit LB spirochetes B.
burgdorferi
, as well as the HGA agent A. phagocytophilum Piesman, 2002. Borrelia bis- setti,
another spirochete, which was initially confused with B. burgdorferi s.s., occurs in wood rats, but at present its importance to human health is uncertain Maupin et al., 1994;
Eisen et al., 2003. Wood rats have also been found seropositive for hepatitis E virus in New Mexico Favorov et al., 2000. Finally, wood rats have been reported to serve as hosts
for the protozoon parasite Trypanosoma cruzi that causes Chagas disease. Trypanosoma cruzi
is transmitted by a type of reduviid bug that can be found living within the large stick nests built by these animals Peterson et al., 2002.
Four species of cotton rats occur in the temperate regions of North America, but only one of these, the hispid cotton rat, is likely to pose a significant threat to human health. Hispid
cotton rats can occur near human habitations and are extremely abundant in much of the south-eastern and south-central United States, including some largely urban areas with
appropriate habitat and other sites undergoing urbanization. In some regions they are the major hosts of the immature American dog tick, the primary vector of the RMSF agent
R. rickettsii in the eastern United States Gage, Burgdorfer Hopla, 1990; Gage, Hopla Schwan, 1992. Recently, Kosoy and colleagues 1997, 1999, 2004a,b reported that cotton
rats are hosts to four uncharacterized Bartonella genogroups. Hispid cotton rats also are known to be susceptible to infection with B. burgdorferi Burgdorfer Gage, 1987.
13.4.4.10. Rabbits and hares
Tularaemia, which is often referred to as rabbit fever, is frequently found in rabbits and hares, and these animals are common sources of human infection Hopla, 1974; Jellison,
1974; Hopla Hopla, 1994; Petersen Schriefer, 2005. In the United States, rabbits are the source of tularaemia infection in 90 of human cases, 70 of which result from
contact with the genus Sylvilagus. Jackrabbits also are an important source of infection in some areas of the United States, but are a minor factor nationally, and exposure to snows-
hoe hares Lepus americanus account for less than 1 of cases of human tularaemia in the United States.
In Europe, tularaemia has been detected in brown hares Lepus europaeus, mountain hares Lepus timidus, and rabbits such as the European rabbit. High rates of mortality were
usually observed among all these species, with death occurring 7–19 days after exposure. In Europe, die-offs of hares often followed epizootics in small rodents Borg et al., 1969.
Rabbits have often been found to be naturally infected with Y. pestis in North America, and numerous human plague cases have been associated with handling these animals
Kartman, 1960; von Reyn et al., 1976. In most instances, these cases have occurred in
Non-commensal rodents and lagomorphs
450
vegetables contaminated with Y. pseudotuberculosis-infected rodent urine Daiter, Polotskii Tsareva, 1987. Microtusvoles also are reported as hosts of L. interroganssero-
types in Bulgaria, the Czech Republic, Denmark, Germany, Hungary, the Netherlands, Poland, the Russian Federation, Slovakia and Switzerland.
13.4.4.7. Old World mice
Species of Apodemus are particularly important hosts for many tick-borne pathogens, and at least 23 species of ticks are reported on the wood mouse. The most epidemiologically
important of these ticks is the castor bean tick, which is the primary vector of LB and TBE in Europe Humair Gern, 2000; Huegli et al., 2002; Charrel et al., 2004. Among
the pathogens associated with wood mice are those that cause LB, TBE, Omsk haemor- rhagic fever, Q fever, tularaemia, leptospirosis, bartonellosis, toxoplasmosis, salmonello-
sis and infections with hantaviruses. Yellow-necked mice also serve as hosts for the patho- gens that cause leptospirosis, TBE, lymphocytic choriomeningitis, toxoplasmosis and a
severe form of HFRS caused by Dobrava virus. The yellow-necked mouse also is a host of B. garinii Huegli et al., 2002, a genospecies that has been cultivated frequently from
the cerebrospinal fluid of LB patients from Denmark, Germany, the Netherlands and Slovenia. These mice also are important hosts of larval and nymphal castor-bean ticks.
13.4.4.8. Dormice
Although less important as hosts of rodent-related disease agents than the voles or Old World mice, the edible or fat dormouse has been implicated as the source of F. tularensis
infection for a human tularaemia case in which the person was bitten on the finger by an infected dormouse Friedl, Heinzer Fankhauser, 2005. Garden dormice also are hosts
of a recently described spirochete B. spielmani that reportedly causes LB in people Richter et al., 2004. Others have proposed that dormice might act as hosts for the murine
typhus agent R. typhi, after this rickettsia was identified in fleas Monopsyllus sciurorum sciurorum
taken from the nests of these animals Trilar, Radulovic Walker, 1994.
13.4.4.9. N ew World rats and mice
Although many species of rats and mice exist in the New World murine subfamily Sigmodontinae, only a few are likely to be found near human habitations or to pose a
significant risk of disease to people. Notable among these are various species of native mice Peromyscus spp., wood rats Neotoma spp. and cotton rats Sigmodon spp.. Among
the species of Peromyscus, the deer mouse and the white-footed mouse are widespread and particularly important. The deer mouse is the major source of SNV infection in peo-
ple Childs et al., 1994 and often is considered to be a significant enzootic host of plague. The white-footed mouse is the major host of the LB spirochete B. burgdorferi and its
primary tick vector the deer tick throughout the north-eastern and much of the upper Midwestern United States, as well as parts of south-eastern Canada Piesman, 2002. It
is also an important host for the HGA agent A. phagocytophilum, which is also trans- mitted by deer ticks Parola Raoult, 2001; Strle, 2004; Parola, Davoust Raoult, 2005.
Moreover, Peromyscus mice are important hosts of the immature stages of the American dog tick, the primary tick vector of the RMSF agent R. rickettsii in the eastern United
States.
Public Health Significance of Urban Pests
453
dry region. As a result of the large rainfalls, plant growth increased dramatically; in turn, this led to an increased availability of rodent food sources such as vegetation, seeds, fruits
and insects and a tremendous eruption in the region’s deer mouse population Engelthaler et al., 1999; Hjelle Glass, 2000; Glass et al., 2002, which was followed by
an increase in hantavirus prevalence among these mice. As deer mouse populations increased, so did the frequency at which peridomestic environments, including homes,
were invaded – a factor that greatly increased the risk of exposing people to hantavirus- infected animals or their excreta. Based on a study by Kuenzi and colleagues 2001,
which demonstrated that the breeding season of deer mice in peridomestic sites was about two months longer than in naturally occurring habitats, Mills 2005 suggested that this
factor could influence the risk of exposure of people living in these sites.
Human plague in the south-western United States largely occurs in peridomestic envi- ronments located in formerly rural areas that are rapidly undergoing urbanization. The
risk of people acquiring plague in these areas is likely to be influenced by environmen- tal factors, such as yearly variations in climatic variables, that affect rodent and vector
abundance. Parmenter and colleagues 1999 also noted that increased cool season preci- pitation was associated with an increased risk of human plague in New Mexico. They
proposed that the increased risk was linked to the positive effects of precipitation increa- ses on the availability of rodent food sources; this, in turn, led to increased populations of
the rodent hosts of plague and probably the flea vectors that feed on these animals. These ideas were further expanded by Enscore and colleagues 2002, who demonstrated that
the frequencies of human plague cases in a given onset year in a region of the south-wes- tern United States were associated positively with late winter precipitation and relatively
cool summers, findings believed to be related to rodent population dynamics and survi- val of vector fleas, respectively.
The incidence of LB also can be affected by changing ecological parameters, including the availability of food for rodents. Jones and colleagues 1998 proposed that increased oak
masts acorn crops can lead to increased populations of rodents, particularly white-foo- ted mice, that serve as hosts and sources of spirochetal infection for the immature stages
of the deer tick, which is the primary vector of LB in the eastern United States and sou- thern Canada.
13.6. The impacts of anthropogenic transformations
Although complete urbanization can result in the elimination of non-commensal species, the transition from rural to suburban environments often results in a mosaic of human
development interspersed with largely natural areas that can harbour sizeable non-com- mensal rodent populations. Human activities often disturb landscapes, causing major
alterations of rodent habitats, as well as significant changes in the composition of local rodent and lagomorph populations that serve as hosts for various disease agents Barnes,
1982; Maupin et al., 1991; Gage, Ostfeld Olsen, 1995; Gage et al., 2000; Randolf, 2001; Piesman, 2002. In some instances these landscape disturbances result in the loss of cer-
tain rodent species from the area affected, particularly when those species are highly spe-
Non-commensal rodents and lagomorphs
452
hunters and others who have skinned infected carcasses. Cottontail rabbits, however, also occur frequently in urbanized environments, and rabbit carcasses positive for Y. pestis
have been found in such areas, suggesting a possible risk for people who might come into contact with infected rabbits or their fleas in these areas.
Other bacterial or rickettsial disease agents reported from lagomorphs include those that cause pasteurellosis, brucellosis, yersiniosis, listeriosis, rickettsioses Rickettsia spp., C.
burnetii , Anaplasma spp., salmonelloses and leptospirosis Dunaeva, 1979; Dumler, 1994;
Williams Sanchez, 1994; Gage, Ostfeld Olson, 1995; Goethert Telford, 2003a, although no known cases of human infection with these agents have been traced to
contact with wild rabbits or hares. Lagomorphs also carry endoparasites, such as hel- minths Trichostrongylus spp., Passalurus ambiguus and Graphidium strigosum in hares,
tapeworms Taenia pisiformis, Taenia serialis and Echinococcus granulosus in rabbits; Cittotaenia ctenoides
in rabbits; and Protostrongylus spp. in hares. Finally, rabbits and hares can carry protozoan parasites, including T. gondii, Encephalitozoon cuniculi and coccidia
Eimeria spp. Dunaeva, 1979; Marquardt, Demaree Grieve, 2000. Although lago- morphs harbour viruses, such as myxoma virus, snowshoe hare virus, herpesvirus and
the virus that causes European brown hare syndrome, these agents do not appear to be important causes of illness in people Dunaeva, 1979.
13.5. Risk factors for rodent- and lagomorph-related diseases
In general, the risk of acquiring rodent- or lagomorph-related disease agents is linked to the likelihood of coming into close proximity to the rodent carriers of these diseases, their
wastes or the disease-transmitting ectoparasites they carry. Even in the absence of chan- ges induced by people, the risk rarely remains steady over time, but tends to fluctuate,
depending on the status of various ecological factors, including climatic variables, qua- lity of natural habitat and available food supplies Gage Kosoy, 2005; Mills, 2005, all
of which can affect the survival and reproduction of rodents and lagomorphs through their impacts on the availability of food. Although the effects of various ecological factors
on eruptions of rodent or lagomorph populations have been much debated Begon, Harper Townsend, 1996, any factors that causes populations of these animals to
increase above certain threshold levels is likely to lead to an increased spread of disease among these populations Davis et al., 2004. Also, it is likely to lead to heightened risks
of exposure for people, particularly when infected animals invade their home sites, recrea- tional areas or workplaces where good rodent sanitation practices are lacking or inade-
quate Childs et al., 1995; Zeitz et al., 1995; Enscore et al., 2002. The following para- graphs provide some examples of how the risk of disease in people can be affected by
environmental factors that influence rodent population dynamics. These paragraphs also provide examples of the likelihood that these animals will move into close contact with
people.
The 1993 HPS outbreak caused by SNV in the south-western United States occurred after a strong El Niño event that resulted in extremely high precipitation in this normally
