The Role of Peridomestic Rodents as Reservoirs for Zoonotic Foodborne Pathogens

Abstract

Although rodents are well-known reservoirs and vectors for a number of zoonoses, the functional role that peridomestic rodents serve in the amplification and transmission of foodborne pathogens is likely underappreciated. Clear links have been identified between commensal rodents and outbreaks of foodborne pathogens throughout Europe and Asia; however, comparatively little research has been devoted to studying this relationship in the United States. In particular, regional studies focused on specific rodent species and their foodborne pathogen reservoir status across the diverse agricultural landscapes of the United States are lacking. We posit that both native and invasive species of rodents associated with food-production pipelines are likely sources of seasonal outbreaks of foodborne pathogens throughout the United States. In this study, we review the evidence that identifies peridomestic rodents as reservoirs for foodborne pathogens, and we call for novel research focused on the metagenomic communities residing at the rodent-agriculture interface. Such data will likely result in the identification of new reservoirs for foodborne pathogens and species-specific demographic traits that might underlie seasonal enteric disease outbreaks. Moreover, we anticipate that a One Health metagenomic research approach will result in the discovery of new strains of zoonotic pathogens circulating in peridomestic rodents. Data resulting from such research efforts would directly inform and improve upon biosecurity efforts, ultimately serving to protect our food supply.

Introduction

Foodborne illnesses are a major threat to human health, and it is estimated that foodborne pathogens sicken at least 48 million in the United States annually, causing upwards of $70 billion USD in health-related costs (Scallan et al. 2011, Scharff 2012, Hoffman et al. 2015, Hoffmann and Scallan 2017). Moreover, ∼64% of hospitalization and deaths associated with foodborne pathogens in the United States are caused by zoonotic bacteria, including nontyphoidal Salmonella enterica, Campylobacter spp., Clostridium spp., Shiga-toxin producing Escherichia coli (STEC), and Listeria monocytogenes (Scallan et al. 2011).

The direct environmental point source for many of the zoonotic enteric pathogens that enter our food supply is typically difficult to determine; however, wildlife distributed throughout local environments associated with a given outbreak are frequently implicated in spreading zoonosis (Atwill et al. 2012, Himsworth et al. 2013, Greig et al. 2015, Sellers et al. 2018, Ayyal et al. 2019). When considering putative reservoirs and vectors for the major zoonotic foodborne pathogens that underlie human disease, a critically important and uniting feature is that each is associated with peridomestic rodent hosts (Backhans et al. 2011, Himsworth et al. 2015, Ayyal et al. 2019, Bondo et al. 2019, Tan et al. 2019) (Table 1).

Table 1.

Zoonotic Foodborne Pathogens Associated with Rodent Reservoirs

Foodborne pathogens	Known rodent reservoirs	References
Campylobacter spp.	Apodemus sylvaticus (Wood mouse), Microtus agrestis (Field vole), Microtus longicaudus (Longtail vole), Microtus richardsoni (Water vole), Mus musculus (House mouse), Myodes glareolus (Bank vole), Peromyscus maniculatus (Deer mouse), Rattus norvegicus (Norway rat), Zapu princeps (Western jumping mouse)	Fernie and Park (1977), Rosef et al. (1983), Pacha et al. (1987), Meerburg et al. (2006), Viswanathan et al. (2017)
Clostridium spp.	A. sylvaticus, Microtus arvalis (Common vole), Micromys minutus (Eurasian harvest mouse), M. musculus, R. norvegicus, Rattus rattus (Black rat)	Burt et al. (2012), Jardine et al. (2013), Himsworth et al. (2014), Krijger et al. (2019)
Coxiella burnetii Cryptosporidium spp.	Akodon cursor (Cursor grass mouse), Allactaga elater (Small five-toed jerboa), Apodemus agrarius (Striped field mouse), Apodemus flavicollis (Yellow-necked mouse), Aeschynanthus speciosus, Arvicola terrestris (European water vole), Callospermophilus lateralis (Golden-mantled ground squirrel), Clethrionomys gapperi (Southern Red-backed voles), Cricetulus migratorius (Gray hamster), Dipodomys heermanni (Heermann's kangaroo rat), Dipodomys microps (Chisel-toothed kangaroo rat), Dipodomys ordii (Ord's kangaroo rat), Eliomys quercinus (Garden dormouse), Eutamias amoenus (Yellow pine chipmunk), Eutamias sibiricus (Siberian Chipmunk), Glaucomys sabrinus (Northern flying squirrel), Lemniscomys barbarus (Zebra mouse), Meriones shawi (Shaw's jird), M. arvalis, Microtus californicus (Meadow mouse), Microtus fortis (Reed vole), M. musculus, Myocastor coypus (Nutria), M. glareolus, Myodes rutilus (Northern red-backed vole), Napaeozapus insignis (Woodland jumping mice), Neotoma cinerea (Bushy-tailed woodrat or packrat), Neotoma fuscipes (Dusky-footed woodrat), Neotamias minimus (Least chipmunk), Neotamias sonomae (Sonoma chipmunk), Oligoryzomys nigripes (Black-footed pygmy rice rat), Ondatra zibethicus (Muskrat), Onychomys leucogaster (Northern grasshopper mouse), Otospermophilus beecheyi (Beechy ground squirrel), Oxymycterus dasytrichus (Atlantic Forest hocicudo), Peromyscus boylii (Brush mouse), P. maniculatus, Peromyscus truei (Pinyon mouse), Proechimys cayenne (Cayenne spiny rat), Physalaemus cuvieri (Cuvier's spiny rat), R. norvegicus, R. rattus, Reithrodontomys megalotis (Harvest mouse), Rhombomys opimus (Great gerbil), Sciurus griseus (Western gray squirrel), Spermophilus relictus (Relict ground squirrel), Tamiasciurus hudsonicus (North American red squirrels) A. agrarius, Apodemus chejuensis (Jeju striped field mouse), M. musculus, Peromyscus californicus (California mouse), P. maniculatus, Rattus argentiventer (Rice-field rat), R. norvegicus, R. exulans (Pacific rat), R. rattus, Rattus tanezumi (Asian house rat), Rattus tiomanicus (Malayan field rat)	Blanc et al. (1947), Perez Gallordo et al. (1952), Zhmaeva et al. (1955), Blanc and Bruneau (1956), Syrůček and Raška (1956), Orsborn et al. (1959), Stoenner et al. (1959), Yevdoshenko and Proreshnaya (1961), Burgdorfer et al. (1963), Enright et al. (1969), Enright et al. (1971), Riemann et al. (1979), Ejercito et al. (1993), Gardon et al. (2001), Meerburg and Reusken (2011), Reusken et al. (2011), Thompson et al. (2012), Liu et al. (2013), Foronda et al. (2015), Bolaños-Rivero et al. (2017), Rozental et al. (2017) Kilonzo et al. (2013), Song et al. (2015), Saki et al. (2016), Tan et al. (2019)
Escherichia coli (STEC and multiple AMR strains)	A. agrarius, A. flavicollis, A. sylvaticus, Arvicola amphibius (European water vole), M. minutus, M. agrestis, M. arvalis, Microtus pennsylvanicus (Meadow vole), Monodus subterraneus (European pine vole), M. musculus, M. glareolus, P. californicus, P. maniculatus, R. norvegicus, Tamius striatus (Eastern chipmunk)	Čížek et al. (1999) Nielsen et al. (2004), Ulrich et al. (2008), Guenther et al. (2010), Allen et al. (2011), Allen et al. (2013), Kilonzo et al. (2013)
Francisella tularensis Giardia spp.	A. agrarius, A. flavicollis, A. peninsulae, A. sylvaticus, A. amphibius, A. terrestris, Callithrix jacchus (Common marmosets), Castor canadensis (American beaver), Cricetus migratorius (European hamster), Cynomys ludovicianus (Black-tailed prairie dog), E. sibiricus, Meriones lybicus (Libyan jird), M. agrestis, M. arvalis, M. pennsylvanicus, Microtus montebelli (Japanese grass vole), M. musculus, M. glareolus, M. rufocanus (Gray-sided vole), O. zibethicus, R. norvegicus, R. rattus, Sciurus carolinensis (Eastern gray squirrel), S. griseus, Sciurus niger (fox squirrel), Spermophilus dauricus (Daurian ground squirrels), Tscherskia triton (Greater Long-tailed Hamster), Urocitellus richardsonii (Richardson's ground squirrel) A. agrarius, A. flavicollis, A. sylvaticus, Bandicota indica (Greater bandicoot rat), Maxomys surifer (Red spiny rat), M. agrestis, M. arvalis, M. glareolus, P. californicus, P. maniculatus, R. argentiventer, R. norvegicus, R. exulans, R. rattus, R. tanezumi, R. tiomanicus	Bell and Stewart (1975), Bruce (1978), Magee et al. (1989), Gurycova et al. (2001), Avashia et al. (2002), Berrada et al. (2006), Friend (2006), Zhang et al. (2006), Splettstoesser et al. (2007), Kaysser et al. (2008), Williams and Barker (2008), Gyuranecz et al. (2010), Nelson et al. (2014), Rossow et al. (2014), Sharma et al. (2014) Pacha et al. (1987), Kilonzo et al. (2013), Masakul et al. (2016), Helmy et al. (2018), Tan et al. (2019)
Hepatitis E virus Leptospira spp.	A. sylvaticus, Bandicota bengalensis (Lesser bandicoot rat), M. musculus, P. maniculatus, Rattus exulans, R. norvegicus, Rattus pyctoris (Turkestan rat), R. rattus, R. tanezumi, Sigmodon hispidus (Cotton rat) R. norvegicus, S. niger	Karetnyĭ et al. (1993), Kabrane-Lazizi et al. (1999), Favorov et al. (2000), Arankalle et al. (2001), He et al. (2002), Hirano et al. (2003), Vitral et al. (2005), Johne et al. (2010), Purcell et al. (2011), Kanai et al. (2012), Lack et al. (2012), Depamede et al. (2013), De Sabato et al. (2020) Bharti et al. (2003), Dirsmith et al. (2013), Allen et al. (2014)
Listeria monocytogenes	A. agrarius, A. chevrieri (Chevrier's field mouse), A. peninsulae (Korean field mouse), Callosciurus (Beautiful squirrels), Niviventer confucianus (Chinese white-bellied rat), Rattus lossea, R. norvegicus, R. rattus, T. triton	Inoue et al. (1992), Lesley et al. (2016), Wang et al. (2017), Cao et al. (2019)
Norovirus (multiple strains)	R. Norvegicus	Wolf et al. (2013), Summa et al. (2018)
Salmonella spp.	A. sylvaticus, M. agrestis, M. musculus, M. glareolus, P. californicus, P. maniculatus, R. norvegicus, S. carolinensis	Shimi et al. (1979), Singh et al. (1980), Henzler and Opitz (1992), Guard-Petter et al. (1997), Pocock et al. (2001), Hilton et al. (2002), Davies and Breslin (2003), Garber et al. (2003), Meerburg et al. (2006), Jijón et al. (2007), Kilonzo et al. (2013)
Staphylococcus aureus	A. flavicollis, M. agrestis, M. musculus, M. glareolus, R. norvegicus, R. rattus	Van de Giessen et al. (2009), Mrochen et al. (2017), Lee et al. (2019)
Toxoplasma gondii	A. sylvaticus, M. arvalis, Mastomys erythroleucus (Guinea multimammate mouse), Mastomys natalensis (Natal multimammate mouse), M. musculus domesticus (Western European house mouse), Peromyscus sp?, R. norvegicus, R. rattus	Dubey et al. (1995), Weigel et al. (1995), Kijlstra et al. (2008), Meerburg et al. (2012), Ruffolo et al. (2016), Khademvatan et al. (2017), Brouat et al. (2018)
Trichinella spp.	A. agrarius, A. flavicollis, A. sylvaticus, B. bengalensis, M. natalensis, M. musculus, Meriones persicus (Persian Jird), Peromyscus leucopus (White-footed mouse), P. maniculatus, R. norvegicus, R. rattus	Martin et al. (1968), Sadighian et al. (1973), Shaikenov and Boev (1983), Loutfy et al. (1999), Dick and Pozio (2001), Larrieu et al. (2004), Stojcevic et al. (2004), Pozio (2005), Kanai et al. (2007), Pozio et al. (2009), Ribicich et al. (2010)
Yersinia spp.	A. agrarius, A. argenteus (Geisha mice), A. flavicollis, A. speciosus (Woods mice), Ashizomys andersoni (Oriental voles), A. niigatae (Oriental voles), Clethrionomys rufocanus bedfordiae (Large red-backed mice), C. rutilus (Redbacked mice), Eothenomys kageus (Oriental voles), M. minutus, M. agrestis, M. levis (Sibling vole), M. montebelli (Japanese grass vole), M. musculus, M. glareolus, R. norvegicus, R. rattus, Tamias sibiricus (Asiatic chipmunks), T. striatus	Pokorná and Aldová (1977), Kaneko and Hashimoto (1981), Shayegani et al. (1986), Iinuma et al. (1992), Backhans et al. (2011), Joutsen et al. (2017)

AMR, antimicrobial resistance; STEC, Shiga-toxin producing E. coli.

Rodents are the most specious group of mammals in the world with over 2000 species recognized, and they are well known for harboring a plethora of zoonotic pathogens of human health concern (e.g., Hantaviruses, Lassa fever virus, Giardia, Borrelia, and so on) (Han et al. 2015). Commensal and peridomestic rodent species are of special interest to the global One Health initiative, as regionally invasive and native species of mice and rats have benefitted from human activities, especially agricultural systems. Commensal rodents are a common component of the agricultural landscape, and these animals are known to transmit foodborne pathogens to livestock, poultry, and raw produce by contaminating the overall farm environment (Rodriguez et al. 2006, Meerburg 2010, Backhans and Fellström 2012, Kilonzo et al. 2013). This transmission is largely due to the amplification of foodborne pathogens through the daily deposition of urine and fecal pellets into the production environment, and a clear example of this rodent-based amplification is found with Salmonella (Fig. 1).

FIG. 1.

Salmonella amplification by a rodent host. (A) Approximately 15 Salmonella bacteria are required to establish infection within a rodent. (B) After colonization, ∼230,000 Salmonella are shed in a single mouse fecal pellet. (C) One rodent can produce 100 fecal pellets in 24 h. Thus, at least 23 million Salmonella can be introduced into a barn environment by a single rodent pest. This process contributes to outbreaks of enteric disease due to contaminated food or water resources.

Fifteen Salmonella Enteritidis cells can successfully infect a mouse (Mus musculus), and the infection can be maintained for over 10 months (Trampel et al. 2014). During active shedding, one mouse fecal pellet can contain up to 230,000 Salmonella cells, and the rodent can output more than 100 fecal pellets in a day (Fig. 1). Thus, a single rodent within a barn or food-production facility can introduce upwards of 23 million Salmonella bacteria into production pipelines within 24 h (Davies and Wray 1995, Trampel et al. 2014). In particular, the poultry industry is especially susceptible to rodent-driven Salmonella outbreaks as poultry preferentially consume rodent fecal pellets (see Salmonella section below), and as little as 100 Salmonella bacteria are required to successfully infect young chicks (sustained doses of 10⁶ colony-forming units [CFUs] required for maintaining infections [Van Immerseel et al. 2004]).

Despite a growing list of examples that document strong links between rodents on farms and outbreaks of foodborne pathogens in Europe and Asia (Berndtson et al. 1996, Burt et al. 2012, Lapuz et al. 2012, Espinosa et al. 2018, Camba et al. 2020), comparatively little research on the rodent-agriculture interface has occurred in the United States (Henzler and Opitz 1992, Kilonzo et al. 2013). Moreover, studies investigating this interface frequently lack specific knowledge of the rodent species involved and refer to rodents simply as “mice” or “rats,” therefore preventing the identification of species-specific patterns with respect to reservoir status, demographic trends, etc. (Hancock et al. 1998, Hiett et al. 2002). For these reasons, the role of peridomestic rodents as reservoirs or vectors of zoonotic foodborne pathogens in the United States is not well defined, and there is a great need to fill this epidemiological knowledge gap.

We review select rodent species and bacterial foodborne pathogens that are routinely linked to rodent reservoirs. Our intent is to bring awareness to the rodent species diversity that must be considered when examining environmental sources of foodborne pathogens; these data can ultimately inform public health policies and species-specific biosecurity measures in food production operations.

Primary Species of the Rodent-Agriculture Interface Across the Midwestern United States

In this study, we summarize some of the rodent species that are likely at the heart of the rodent-agriculture interface in the Midwestern United States (i.e., Iowa, Michigan, Minnesota, Missouri, Nebraska, North Dakota, Ohio, South Dakota, and Wisconsin), one of the most agriculturally productive regions of the world. Importantly, the species we highlight represent a regional example and are not exhaustive; these are species that are commonly observed on farms throughout the Midwest and they include both North American native species and invasive species.

Native Species

White-footed mouse

The White-footed Mouse (Peromyscus leucopus) is a relatively small rodent in the genus Peromyscus that has a distribution extending from Canada to Mexico, including the eastern and midwestern United States, as far west as Arizona (Fig. 2) (Lackey et al. 1985). White-footed mice are semiarboreal, but also occur in agricultural areas (Drickamer 1970, Cummings and Vessey 1994); and their diet consists of seeds, green vegetation, insects, and arthropods (Lackey et al. 1985, Wolff et al. 1985). Cummings and Vessey (1994) reported that P. leucopus could be found in nearly all areas trapped across the farmsteads of Ohio and was second in abundance only to the invasive house mouse (M. musculus; see below). White-footed mice are of special concern to One Health because they have been positively identified as vectors for not only hantavirus (Cummings and Vessey 1994) but also for other pathogens causing Lyme disease, human babesiosis, and human granulocytic ehrlichiosis (Stafford et al. 1999). When considering foodborne zoonoses, multiple pathogens have been identified within Peromyscus hosts (Table 1).

FIG. 2.

Geographic distributions of native rodent species highlighted herein. (A) Deer Mouse (Peromyscus maniculatus), White-footed Mouse (Peromyscus leucopus), Meadow Vole (Microtus pennsylvanicus). (B) Thirteen-lined Ground Squirrel (Ictidomys tridecemlineatus), Eastern Chipmunk (Tamias striatus), (C) Fox Squirrel (Sciurus niger), Eastern Gray Squirrel (Sciurus carolinensis).

Deer mouse

A close relative to the White-footed Mouse is the Deer Mouse (Peromyscus maniculatus) from the same genus, Peromyscus. The Deer Mouse is a common rodent species that is distributed throughout North America, including Canada, nearly all the United States, and southward into Mexico (American Society of Mammalogists and King 1968). Similar to the White-footed mouse, deer mice feed on seeds, vegetation, and arthropods (Jameson 1952, Wolff et al. 1985). Deer mice are well adapted to different environments, including grasslands, prairies, and agricultural lands (Beckwith 1954), and have been reported to prefer indoor granaries when living in a farm setting, especially during winter months (Bovet 1970). Peromyscus maniculatus is a known reservoir for many zoonotic pathogens, including Sin Nombre Virus (Madhav et al. 2007), Cryptosporidium and Giardia (Kilonzo et al. 2017), and Coxiella burnetii and Pasteurella pestis (Yersinia pestis) (Orsborn et al. 1959). This species is also associated with several foodborne pathogens (Table 1).

Meadow vole

The Meadow Vole (Microtus pennsylvanicus) can be distinguished from Peromyscus species by a darker pelage and shorter tail (Reich 1981). It has a large range compared to other voles in the genus Microtus. The Meadow Vole occurs throughout Canada, the north and eastern parts of the United States, and extending southward into Mexico (Reich 1981). This species has been known to frequent farm settings in the Midwest and is associated with dense grassland habitats (American Society of Mammalogists and Tamarin 1985). Meadow voles are mainly herbivores, although they have been found to eat insects and scavenge on animal remains (Zimmerman 1965, Reich 1981). Microtus pennsylvanicus has been implicated as a reservoir for Borrelia burgdorferi (causative agent of Lyme disease) (Markowski et al. 1998) and Rickettsia responsible for Rocky Mountain Spotted fever (Gould and Miesse 1954). Multiple species of voles (Microtus) have been implicated as reservoirs for Campylobacter sp., E. coli, and Listeria sp. (Table 1).

Thirteen-lined ground squirrel

The Thirteen-lined Ground Squirrel (Ictidomys tridecemlineatus) is recognizable by its slender body and distinctly alternating light-colored longitudinal stripes and rows of spots (Lawlor 1982). The distribution for the thirteen-lined ground squirrel extends from Canada to Texas, east of the Rocky Mountains to the Great Lakes region (Streubel and Fitzgerald 1978). This species is considered carnivorous, mainly feeding on grasshoppers, although seeds and other vegetation have been found in their stomach contents (Fitzpatrick 1925, Whitaker 1972). Thirteen-lined ground squirrels have adapted well to farms and urban areas (Streubel and Fitzgerald 1978), thus increasing the risk of zoonotic disease transfer. For instance, Cloud-Hansen et al. (2007) reported multidrug resistant bacteria from wild-caught thirteen-lined ground squirrels (Morganella morganii and Stenotrophomonas maltophilia). Furthermore, thirteen-lined ground squirrels have been implicated as potential transmitters of avian influenza viruses (Vandalen et al. 2009). Very little research has focused on the putative pathogens that thirteen-lined ground squirrels carry despite the species being a common resident on farms and in urban areas throughout the Midwest.

Eastern chipmunk

The Eastern Chipmunk (Tamias striatus) is heavier-set than the thirteen-lined ground squirrel and has prominent white dorsal stripes flanked by darker stripes and no spots (as seen in the thirteen-lined ground squirrel). The Eastern Chipmunk is distributed throughout eastern North America, including Canada and southward to the Gulf states, but is absent from the coastal plain (Snyder 1982). Eastern chipmunks are omnivorous, and their diet includes seeds, nuts, insects, fungi, frogs, snakes, birds, and small mammals (Elliott 1978, Snyder 1982). Tamias striatus has been associated with West Nile Virus (Gómez et al. 2008) and was implicated as an amplifier host for La Crosse Virus (Hanson et al. 1975). Furthermore, isolates of E. coli have been found in chipmunks (Maldonado et al. 2005). Other datasets showing putative links to foodborne pathogens are lacking.

Eastern gray and fox squirrels

The Eastern Gray Squirrel (Sciurus carolinensis) is distributed throughout the eastern United States and northward into Canada. Several introductions have occurred in the western United States and Europe (Koprowski 1994a). The Fox Squirrel's (Sciurus niger) range overlaps with much of the Eastern Gray Squirrel's range, but extends further west in the United States and Canada (Koprowski 1994b). The Eastern Gray Squirrel is distinguishable from the Fox Squirrel by its silver/white hair on the ventral side (belly) compared to the Fox Squirrel's reddish-orange ventral hair. Nuts are the main food source for both species, including acorns, pecans, and walnuts (Koprowski 1994a, 1994b). The Eastern Gray and Fox squirrels are a common component of urban and rural areas. Viruses and bacteria associated with these species include West Nile Virus (Kiupel et al. 2003) and Leptospira (Dirsmith et al. 2013) in fox squirrels and Salmonella from eastern gray squirrels (Jijón et al. 2007). Despite co-occurring with humans and agricultural animals at relatively high densities, little to no research investigates the role of tree squirrels in harboring foodborne pathogens or zoonotic diseases.

Invasive Species

House mouse

The ancestral range for the House Mouse (M. musculus) was most likely India; however, this species readily colonized worldwide as an invasive species due to their close proximity to humans (Boursot et al. 1993, Phifer-Rixey and Nachman 2015). Wild M. musculus are distinguishable from white-footed mice and deer mice by their shorter pelage, smaller eyes, and scaly tail (Schmidly and Bradley 2016). House mice are commonly found in urban and agricultural areas, although feral populations do exist in the wild (Phifer-Rixey and Nachman 2015). Wild M. musculus is heavily studied, and this species has been shown to be a vector for many human diseases and is frequently implicated as reservoir for foodborne pathogens (including multiple pathogenic Salmonella serovars, E. coli, Clostridium difficile, and so on) and other zoonotic pathogens (e.g., avian influenza) of special interest to agricultural production systems (Table 1) (Shimi et al. 1979, Henzler and Opitz 1992, Allen et al. 2011, Burt et al. 2012).

Norway rat

The Norway Rat (Rattus norvegicus), also known as the Brown Rat, is native to China and Mongolia but now has a worldwide distribution as its range expanded alongside humans, facilitated in large part to global trade (Frittelli 2008, Puckett et al. 2016). Like house mice, Norway rats are a common component of both rural and urban environments across the United States, especially on farms. Indeed, the authors of this review personally witnessed an active infestation of hundreds of R. norvegicus on a single farm in southern Minnesota in 2019. Norway rats have connections to several of zoonotic diseases and foodborne pathogens, including Hepatitis E virus (Kanai et al. 2012), C. burnetii (Reusken et al. 2011), Salmonella (Hilton et al. 2002), and C. difficile (Himsworth et al. 2014), among others (Table 1). The ability of these two invasive species, the house mouse and the Norway rat, to adapt to any environment and their quick reproductive cycles make them especially important to understand and document as reservoirs of foodborne pathogens.

Black rat

Also known as the Roof Rat or Ship Rat, the Black Rat (Rattus rattus) is native to Southeast Asia. As in the case of the Norway Rat, the Black Rat is commensal with humans and is now cosmopolitan due to human travel. This species is a major vector for numerous pathogens across the globe, including Y. pestis (plague), Bartonella spp. (Ellis et al. 1999), Trypanosoma cruzi (Panti-May et al. 2017), and several foodborne pathogens (Table 1). The current distribution of the Back Rat in the United States is primarily associated with coastal regions, and data regarding established R. rattus populations in the central United States are limited (Lack et al. 2013). It is likely that R. rattus first colonized North America alongside Columbus in 1492 and established populations in the continental United States by the 1500s (Armitage 1993). However, R. rattus populations across the United States have dwindled, possibly a direct result of being extirpated by the larger and more aggressive R. norvegicus (reviewed in Lack et al. 2013). Given the paucity of data regarding R. rattus within the Midwestern United States, and potential for misidentification with R. norvegicus, we recommend field-based studies aimed to better understand the extent to which R. rattus is distributed on Midwestern farms, especially near shipping ports and railway hubs (e.g., the Great Lakes region, Mississippi and Missouri Rivers, and so on).

Major Bacterial Foodborne Pathogens Linked to Rodents

STEC, nontyphoidal S. enterica, Campylobacter spp., Clostridium spp., and L. monocytogenes are classified as major zoonotic foodborne pathogens in the United States (Scallan et al. 2011). From a global perspective, these zoonoses have well-documented rodent reservoirs, yet there are clear knowledge gaps regarding the interplay between these zoonoses and rodents in the United States. Thus, we focus on the following for our review:

STEC and multidrug resistant generic E. coli

STEC, also known as verocytotoxigenic E. coli (VTEC), is an important foodborne zoonotic pathogen that causes illness ranging from mild diarrhea to hemorrhagic colitis and life-threatening hemolytic uremic syndrome (HUS) (Tarr 1995, Karmali 2004). Cattle and other ruminants are considered to be natural reservoirs for STEC; however, STEC strains have been isolated from other domestic species, as well as wild animals (e.g., goats, sheep, pigs, cats, dogs, deer, wild rabbits, birds, and rodents) (Espinosa et al. 2018). For example, in 2011 a large outbreak of E. coli O157:H7 was traced back to fresh strawberries contaminated with deer feces (Laidler et al. 2013).

With respect to rodent-specific analyses, several studies have identified STEC strains circulating in peridomestic species on both agricultural and urban landscapes, including the Norway Rat (R. norvegicus), Black Rat (R. rattus), and House Mouse (M. musculus) (Čížek et al. 1999, Blanco Crivelli et al. 2012, Himsworth et al. 2015, Williams et al. 2018). In particular, Nielsen et al. reported the isolation of a STEC strain from a Norway Rat (R. norvegicus) identical to a cattle isolate from the corresponding farm with respect to serotype, virulence profile, and pulsed-field gel electrophoresis type (Nielsen et al. 2004). Moreover, in a Czech cattle farm, E. coli O157 was isolated from 40% of Norway rats, emphasizing the importance of rodents as potential vectors of pathogenic E. coli in cattle productions (Čížek et al. 1999).

In pathogen survival studies, it was shown that E. coli O157 could survive for up to 9 months in the feces of experimentally infected rodents, whereas in ruminant feces the pathogen survived for up to 18 weeks (Fukushima et al. 1999, Guenther et al. 2013). This finding suggests that rodent mobility and longer survival periods of the pathogen in rodent feces may make rodents competent vectors of such pathogens particularly when they have access to livestock production farms. In addition, limited or no data exist with respect to STEC screening of populations of native rodent species occurring on farms across the Midwestern states (e.g., Peromyscus spp., Microtus spp., Sciurus spp.; see above); thus, additional research is required to investigate the role of these rodents in spreading or harboring strains of STEC.

Nonspecific E. coli strains with antibiotic resistance or multidrug resistance (MDR) are also of great health concern, as MDR infections are complicated to treat and, in worst case scenarios, are completely without antibiotic treatment options. Moreover, MDR bacteria can greatly contribute to the dissemination of antibiotic resistance genes through horizontal gene transfer to other bacteria.

MDR bacteria have been found at high prevalence in the intestinal bacteria of wild rodents living in close proximity to livestock. For example, one study reported 71% MDR E. coli positive samples (cecum) from 49 wild house mice (M. musculus) captured from swine farms (Allen et al. 2013). Furthermore, Allen et al. (2011) studied antimicrobial resistance in generic E. coli from wild small mammals (e.g., mouse, vole, shrew) living in swine farms, residential areas, landfills, and natural environments in Ontario, Canada. They observed the highest (48%) resistant E. coli population isolated from the small mammals living in swine farms compared to other areas (Allen et al. 2011). A study by Guenther et al. (2010) reported low (5.5%) prevalence of antibiotic resistance among 188 E. coli isolated from rodents captured from rural areas in Germany, which also suggests transmission of resistant bacteria from livestock or farm environment to wild rodents. With respect to species-specific behavioral traits, it was suggested by Himsworth et al. (2015) that Black Rats (R. rattus) are less likely to carry E. coli than Norway Rats (R. norvegicus) as the latter species is a ground dweller and thus experiences more fecal exposure than the upper level dweller. Moreover, Kozak et al. (2009) found that rodents residing in swine farms were five times more likely to carry tetracycline and multidrug resistant E. coli than rodents living in natural areas. Interestingly, 83% of the swine population in the specified farms also carried tetracycline resistant E. coli. However, the direction of transmission of these resistant pathogens remains unclear.

Nontyphoidal S. enterica

Salmonellosis is a common foodborne illness worldwide, caused by the bacteria Salmonella that has over 2500 serotypes making this pathogen very challenging to control. In the United States, nontyphoidal Salmonella bacteria cause 11% of all foodborne illness, 35% of all foodborne illness related hospitalization, and 28% of all foodborne illness related death (Scallan et al. 2011). In addition, 95% of all nontyphoidal Salmonella cases are foodborne, suggesting an origin from food animals or contaminated food products derived from food animals and fresh produce (Hoelzer et al. 2011).

Many studies have isolated Salmonella at higher rates from farm environments, indicating that the overall farm environment is an important Salmonella reservoir (Bondo et al. 2016). Both wildlife and companion animals represent potential sources of human salmonellosis, as Salmonella can cause disease in these animals and some animals can be asymptomatic carriers as well (Rodriguez et al. 2006). Rodents are effective amplifiers of Salmonella (see above, Fig. 1) with the capacity to output millions of Salmonella bacteria into a particular environment. Such rodent-associated Salmonella output is within the reported infective doses for poultry and livestock (e.g., pigs and cattle), which range from 10⁶ to 10⁸ CFUs (Barrow et al. 1987, Gast and Holt 1998, Silva et al. 2008, Hill et al. 2016).

Poultry will preferentially feed on rodent fecal pellets if present in feed or housing facilities, which is highly suggestive of commensal rodents being a critical risk factor in production operations (Davies and Wray 1995). Umali et al. (2012) showed an important connection between persistent Salmonella infection in layer chicken houses and rodents, where R. rattus intermittently shed Salmonella up to 24 weeks, thus reintroducing the pathogen to replacement flocks after cleaning and disinfection. Camba et al. (2020) report that continual fecal shedding by R. rattus inhabiting commercial layer farms in Japan likely played an important role in shifting the predominant Salmonella serotypes identified on layer farms. Over a sampling period from 2008 to 2017, the authors describe an initial identification of Salmonella Infantis in farm-collected R. rattus; however, over time the rat-associated serotypes changed to Salmonella Corvallis in 2013 followed by Salmonella Potsdam and Salmonella Mbandaka in 2017, which became the predominant on-farm serotypes (Camba et al. 2020). Thus, rodents associated with poultry farms are a serious public health concern (Antunes et al. 2016, Nidaullah et al. 2017, Camba et al. 2020).

Several other studies reported the isolation of highly similar strains of Salmonella from food animals (chickens, pigs) and rodents (R. rattus and an undefined species) circulating in the same farm environment (Lapuz et al. 2012, Andrés-Barranco et al. 2014). Moreover, Andrés-Barranco et al. (2014) suggested a greater role of rodents compared to wild birds in maintaining S. enterica in a farm environment, where the associated livestock population was a major source of Salmonella contamination.

There are a growing number of examples documenting the relationship between rodents and Salmonella outbreaks. Although not occurring in a wild or agricultural setting, a 2004 multistate outbreak of S. enterica serovar Typhimurium was traced to hamsters, rats, and mice sold in pet shops across the United States (Hoelzer et al. 2011). Studies investigating the contamination of chicken and pork sausage by Salmonella have implicated poor rodent-control measures within processing facilities (Trimoulinard et al. 2017). It is likely that rodent-related Salmonella outbreaks occur seasonally, coinciding with key demographic and/or climatic shifts that influence rodent behavior (e.g., reproductive cycles, seeking of indoor shelter with lower autumn nightly temperatures, seeking novel food sources during periods of drought, and so on). Given the strong connection between rodents and Salmonella, we recommend renewed and proactive monitoring of rodents associated with food animal farms and food production facilities.

Campylobacter spp.

Campylobacter are major pathogens that cause significant episodes of foodborne illness and hospitalization across the global human population (Scallan et al. 2011). Campylobacter jejuni and Campylobacter coli are the species most commonly associated with human campylobacteriosis; other less frequently reported species causing infection include Campylobacter fetus, Campylobacter lari, and Campylobacter upsaliensis (Meerburg and Kijlstra 2007). Campylobacteriosis typically causes symptoms of gastroenteritis, including vomiting, diarrhea, and fever (Franco 1988). The majority of Campylobacter infections are self-limiting; however, in the case of immunocompromised individuals, hospitalization and treatment are required. Thus, antibiotic resistant strains of Campylobacter pose a great threat to public health. Poultry, contaminated retail meat, and dairy products have largely been associated with campylobacteriosis cases (Scallan et al. 2011).

Poultry and other food animals are thought to be the primary reservoir of Campylobacter spp.; however, wildlife surrounding farm environments are a potential source (Wilson et al. 2008). Viswanathan et al. (2017) studied the prevalence of Campylobacter in livestock (i.e., beef cattle, dairy cattle, and swine) and wildlife, including rodents (i.e., meadow voles (M. pennsylvanicus), house mice (M. musculus), species of Peromyscus, and Norway rats (R. norvegicus)), and identified Campylobacter across their samples (Table 1). Importantly, the presence of rodents in poultry farms has been identified as a significant risk factor for Campylobacter colonization in turkeys and broilers (Agunos et al. 2014). Hiett et al. (2002) conducted molecular subtyping analyses of Campylobacter spp. from Arkansas and California poultry operations. They isolated identical strains of Campylobacter from broiler feces and from a mouse (undefined species) captured from the same farm. Similarly, other studies have reported greater prevalence of antimicrobial resistant strains of Campylobacter from wildlife living in or surrounding farms (Agunos et al. 2014).

Several studies have investigated the role of rodents as potential reservoirs of Campylobacter spp., showing an association between the presence of rodents on farms and an increased risk for flocks to become infected with Campylobacter (Berndtson et al. 1996, Adhikari et al. 2004, Meerburg and Kijlstra 2007). These studies collectively indicate that rodents are a risk factor for the transmission of Campylobacter on food animal operations, and additional studies are required to better understand these transmission dynamics.

Clostridium spp.

The Centers for Disease Control and Prevention (CDC) estimates that ∼1 million cases of foodborne illnesses each year are linked to Clostridium species (Grass et al. 2013). The most common species causing these foodborne illnesses include C. perfringens, C. difficile, and C. botulinum. Clostridia are anaerobic, spore-forming bacteria and produce enterotoxin that can cause mild diarrhea to fatal colitis and death of humans (Keessen et al. 2011, Silva et al. 2014). Over 90% of Clostridium outbreaks are associated with meat products (e.g., beef, pork, and poultry) (Grass et al. 2013). However, very limited information is known about animal or environmental reservoirs for Clostridium spp., information that could be crucial for implementing biological control measures at animal production farms and processing facilities (McClane 2007).

Companion and food animals have been considered as potential sources of Clostridium infection (Rodriguez et al. 2017); however, only a few studies have investigated the presence of Clostridium species in peridomestic rodents despite having clear connections (Hensgens et al. 2012, Himsworth et al. 2013). Himsworth et al. (2014) reported an overall prevalence of 13.1% of C. difficile across 724 rodents (R. rattus, R. norvegicus) collected in Vancouver, Canada. Another study in the Netherlands stated high prevalence (66%) of C. difficile in house mice (M. musculus) from a swine farm, indicating the potential role of these rodents in the maintenance and transmission of the pathogen (Burt et al. 2012). Many studies have established rodents as reservoirs for C. difficile (Burt et al. 2012, 2018, Himsworth et al. 2014). In addition, Krijger et al. (2019) reported six ribotypes of C. difficile associated with human infections that were isolated from rodents captured from swine and dairy farms in the Netherlands. A study by Andrés-Lasheraset al. (2017) in Spain observed that the odds of finding C. difficile from environmental rodent (Rattus sp., M. musculus) fecal pellets were 10 times higher than from swine fecal samples, suggesting that rodents can transmit the pathogen on farms. Another study reported the isolation of identical clonal types of C. difficile from rodents (R. rattus, M. musculus) and piglets from two swine farms in Brazil, suggesting that rodents were introducing the pathogen to the piglets (de Oliveira et al. 2018). Overall, these studies suggest that on-farm rodents are potential C. difficile reservoirs.

Listeria monocytogenes

Another important foodborne pathogen is L. monocytogenes, which causes significant hospitalization and is a leading cause of death by foodborne illness (Scallan et al. 2011). Listeriosis is less commonly reported, perhaps due to its long incubation period and/or because the bacteria are not detected by routine stool culture (Smith et al. 2018). However, listeriosis can cause severe conditions, including stillbirths, abortions, septicemia, and meningitis in high risk groups such as pregnant women, elderly, young children, and immune compromised individuals (Montero et al. 2015).

L. monocytogenes can be found naturally in the environment (e.g., soil, water) and, consequently, in fresh produce, livestock, and wild animals (Weis and Seeliger 1975, Lyautey et al. 2007). Fecal carriage of L. monocytogenes is common and widely documented in food animals (cattle, goat, sheep, swine) and wildlife (mammals, birds) (Weber et al. 1995, Yoshida et al. 2000, Kalorey et al. 2006). The specific reservoir status of farm-associated rodents for Listeria spp. is poorly understood; nevertheless, a few studies have reported varying levels of Listeria presence in rodents. For example, Ayyal et al. (2019) reported 5% prevalence of Listeria spp. among 120 black rats within an urban setting in Baghdad, Iraq. Lesley et al. (2016) conducted a study in Kubah National Park (Sarawak, Malaysia) to detect the prevalence and antibiotic resistance of L. monocytogenes from wild animals (bats, rats, and shrews) and water samples. They reported 33% prevalence of L. monocytogenes from the samples collected and found the isolates to be uniformly resistant to tetracycline and erythromycin.

Another species, Listeria ivanovii, also causes listeriosis, and Cao et al. (2019) described 3.7% prevalence of the bacteria in wild rodents collected from six regions of China, suggesting that wild rodents might be a long-term host of the pathogen. Inoue et al. (1992) captured 254 wild rats, including 41 R. rattus and 126 R. norvegicus in buildings from six different areas in Kanto, Japan, and they observed high prevalence of Listeria (up to 77.8%). These same authors also reported frequent isolation of L. monocytogenes from R. rattus inhabiting Tokyo restaurants (Inoue et al. 1991). Trimoulinard et al. (2017) investigated contamination of chicken and pork sausage by L. monocytogenes, and their findings suggested a positive association with fresh rodent droppings. Additional studies are required to describe the epidemiology of Listeria spp. from commensal rodents inhabiting farms and to assess the public health risk.

Conclusions

At present, many epidemiological studies of zoonotic foodborne pathogen outbreaks in humans focus almost entirely on the role and risk factors of food animals in transmission dynamics. There remains limited published research on the role that individual species of peridomestic rodents play in the transmission of these pathogens to humans, food animals, and within food production systems of the United States. Despite the connections between rodents and zoonotic foodborne pathogens highlighted above, there is a lack of research on this subject across the diverse agricultural landscape of the United States. In light of this paucity of data, we recommend novel research that focuses on the rodent-agriculture interface and that leverages modern metagenomic approaches. For example, high-throughput metagenomic analyses are ideally suited for investigating the rodent-agriculture interface, and such approaches could elucidate the origins of zoonotic foodborne pathogens (Koskela et al. 2017, Sekse et al. 2017, Andersen and Hoorfar 2018, Carleton et al. 2019). Moreover, mammalogists must be engaged in this research to appropriately identify those rodent species that are associated with food production pipelines in the United States. This is important for several reasons, especially when considering that species-specific behaviors and natural history traits (as described above) can influence pest control measures (e.g., avoidance of poison baits), facilitating large on-farm populations.

When considering native rodent species, the local habitat and ecology surrounding farms are important for understanding seasonal population densities, as local environmental conditions can directly influence behavior and on-farm population density. Knowing the resident rodent species composition associated with our food production facilities would allow for the development of sophisticated predictive modeling of rodent populations and the implementation of species-specific biosecurity measures.

There is an undeniable connection between peridomestic rodents and agriculture that has existed since the dawn of civilization. This connection is ongoing and should not be ignored when investigating the source and/or spread of zoonotic foodborne pathogens. Therefore, we recommend the formation of multidisciplinary One Health research teams consisting of farmers, veterinarians, epidemiologists, microbiologists, and mammalogists to focus on this area of research. It is likely that such efforts will identify novel reservoirs for emerging zoonotic foodborne pathogens and will ultimately help to secure food production systems across the United States.

Footnotes

Acknowledgment

The authors thank the University of Minnesota Agricultural Research, Education, Extension and Technology Transfer program for startup funds awarded to PAL.

Author Disclosure Statement

No conflicting financial interests exist.

Funding Information

This study was supported by discretionary funds awarded to PAL.

References

Adhikari

, Connolly

, Madie

, Davies

. Prevalence and clonal diversity of Campylobacter jejuni from dairy farms and urban sources. N Z Vet J, 2004; 52:378–383.

Agunos

, Waddell

, Léger

, Taboada

. A systematic review characterizing on-farm sources of Campylobacter spp. for broiler chickens. PLoS One, 2014; 9:e104905.

Allen

, Boerlin

, Janecko

, Lumsden

, et al. Antimicrobial resistance in generic Escherichia coli isolates from wild small mammals living in swine farm, residential, landfill, and natural environments in Southern Ontario, Canada. Appl Environ Microbiol, 2011; 77:882–888.

Allen

, Janecko

, Pearl

, Boerlin

, et al. Comparison of Escherichia coli recovery and antimicrobial resistance in cecal, colon, and fecal samples collected from wild house mice (Mus musculus). J Wildl Dis, 2013; 49:432–436.

Allen

, Ojkic

, Jardine

. Prevalence of antibodies to Leptospira in wild mammals trapped on livestock farms in Ontario, Canada. J Wildl Dis, 2014; 50:666–670.

American Society of

Mammalogists

, King

. Biology of Peromyscus (Rodentia)/Edited by John A. King. Stillwater, OK: American Society of Mammalogists, 1968.

American Society of

Mammalogists

, Tamarin

. Biology of New World Microtus/edited by Robert H. Tamarin. Stillwater, OK: American Society of Mammalogists, 1985.

Andersen

, Hoorfar

. Surveillance of foodborne pathogens: Towards diagnostic metagenomics of fecal samples. Genes, 2018; 9:14.

Andrés-Barranco

, Vico

, Garrido

, Samper

, et al. Role of wild bird and rodents in the epidemiology of subclinical Salmonellosis in finishing pigs. Foodborne Pathog Dis, 2014; 11:689–697.

10.

Andrés-Lasheras

, Bolea

, Mainar-Jaime

, Kuijper

, et al. Presence of Clostridium difficile in pig faecal samples and wild animal species associated with pig farms. J Appl Microbiol, 2017; 122:462–472.

11.

Antunes

, Mourão

, Campos

, Peixe

. Salmonellosis: The role of poultry meat. Clin Microbiol Infect, 2016; 22:110–121.

12.

Arankalle

, Joshi

, Kulkarni

, Gandhe

, et al. Prevalence of anti-hepatitis E virus antibodies in different Indian animal species. J Viral Hepat, 2001; 8:223–227.

13.

Armitage

PL.

Commensal rats in the New World, 1492-1992. Biologist, 1993; 40:174–178.

14.

Atwill

, Jay-Russell

, Li

, Vivas

, et al. Wildlife, livestock, and companion animals. Proceedings of the Vertebrate Pest Conference, 2012.

15.

Avashia

, Petersen

, Lindley

, Schriefer

, et al. First reported prairie dog–to-human tularemia transmission, Texas, 2002. Emerg Infect Dis, 2004; 10:483.

16.

Ayyal

, Abbas

, Karim

, Abbas

, et al. Bacterial isolation from internal organs of rats (Rattus rattus) captured in Baghdad city of Iraq. Vet World, 2019; 12:119–125.

17.

Backhans

, Fellström

. Rodents on pig and chicken farms—A potential threat to human and animal health. Infect Ecol Epidemiol, 2012; 2:17093.

18.

Backhans

, Fellström

, Lambertz

. Occurrence of pathogenic Yersinia enterocolitica and Yersinia pseudotuberculosis in small wild rodents. Epidemiol Infect, 2011; 139:1230–1238.

19.

Barrow

, Huggins

, Lovell

, Simpson

. Observations on the pathogenesis of experimental Salmonella Typhimurium infection in chickens. Res Vet Sci, 1987; 42:194–199.

20.

Beckwith

SL.

Ecological succession on abandoned farm lands and its relationship to wildlife management. Ecol Monogr, 1954; 24:349–376.

21.

Bell

, Stewart

. Chronic shedding tularemia nephritis in rodents: Possible relation to occurrence of Francisella tularensis in lotic waters. J Wildl Dis, 1975; 11:421–430.

22.

Berndtson

, Emanuelson

, Engvall

, Danielsson-Tham

M-L

. A 1-year epidemiological study of campylobacters in 18 Swedish chicken farms. Prev Vet Med, 1996; 26:167–185.

23.

Berrada

, Goethert

, Telford III

. Raccoons and skunks as sentinels for enzootic tularemia. Emerg Infect Dis, 2006; 12:1019.

24.

Bharti

, Nally

, Ricaldi

, Matthias

, et al. Leptospirosis: A zoonotic disease of global importance. Lancet Infect Dis, 2003; 3:757–771.

25.

Blanc

, Bruneau

. Isolement du virus de Q fever de deux rongeurs sauvages provenant de la forêt de Nefifik (Maroc). Bull Soc Pathol Exot, 1956; 49:431–434.

26.

Blanc

, Martin

, Maurica

. Présence du virus de la ‘Q fever'dans le Maroc méridional. Bull l'Acad Natl Méd (Paris), 1947; 131:138–143.

27.

Blanco Crivelli

, Rumi

, Carfagnini

, Degregorio

, et al. Synanthropic rodents as possible reservoirs of shigatoxigenic Escherichia coli strains. Front Cell Inf Microbiol, 2012; 2:134.

28.

Bolaños-Rivero

, Carranza-Rodríguez

, Rodríguez

, Gutiérrez

, et al. Detection of Coxiella burnetii DNA in peridomestic and wild animals and ticks in an endemic region (Canary Islands, Spain). Vector-Borne and Zoonotic Diseases, 2017; 17:630–634.

29.

Bondo

, Pearl

, Jaecko

, Boerlin

, et al. Impact of season, demographic and environmental factors on Salmonella occurrence in Raccoons (Procyon lotor) from swine farms and conservation areas in Southern Ontario. PLoS One, 2016, 11e0161497.

30.

Bondo

, Pearl

, Janecko

, Reid-Smith

, et al. Salmonella, Campylobacter, Clostridium difficile, and anti-microbial resistant Escherichia coli in the faeces of sympatric mesomammals in southern Ontario, Canada. Zoonoses Public Health, 2019; 66:406–416.

31.

Boursot

, Auffray

J-C

, Britton-Davidian

, Bonhomme

. The evolution of house mice. Annu Rev Ecol Syst, 1993; 24:119–152.

32.

Bovet

Sedentariness of Peromyscus maniculatus in Alberta Granaries. J Mammal, 1970; 51:632.

33.

Brouat

, Diagne

, Ismaïl

, Aroussi

, et al. Seroprevalence of Toxoplasma gondii in commensal rodents sampled across Senegal, West Africa. Parasite, 2018; 25:32.

34.

Bruce

DL.

Tularemia in Canada: Francisella tularensis agglutinins in Alberta ground squirrel sera. Can J Public Health, 1978:49–53.

35.

Burgdorfer

, Pickens

, Newhouse

, Lackman

. Isolation of Coxiella burnetii from rodents in western Montana. J Infect Dis, 1963:181–186.

36.

Burt

, Meijer

, Burggraaff

, Kamerich

, et al. Wild mice in and around the city of Utrecht, the Netherlands, are carriers of Clostridium difficile but not ESBL-producing Enterobacteriaceae, Salmonella spp. or MRSA. Lett Appl Microbiol, 2018; 67:513–519.

37.

Burt

, Siemeling

, Kuijper

, Lipman

LJA

. Vermin on pig farms are vectors for Clostridium difficile PCR ribotypes 078 and 045. Vet Microbiol, 2012; 160:256–258.

38.

Camba

, Del Valle

, Umali

, Soma

, et al. The expanded role of Roof-Rats (Rattus rattus) in Salmonella spp. contamination of a commercial layer farm in east Japan. Avian Dis, 2020; 64:46–52.

39.

Cao

, Wang

, Li

, et al. Prevalence and characteristics of Listeria ivanovii strains in wild rodents in China. Vector-Borne Zoonotic Dis, 2019; 19:8–15.

40.

Carleton

, Besser

, Williams-Newkirk

, Huang

, Trees

, Gerner-Smidt

. Metagenomic approaches for public health surveillance of foodborne infections: Opportunities and challenges. Foodborne Pathog Dis, 2019; 16:474–479.

41.

Čížek

, Alexa

, Literák

, Hamřík

, et al. Shiga toxin-producing Escherichia coli O157 in feedlot cattle and Norwegian rats from a large-scale farm. Lett Appl Microbiol, 1999; 28:435–439.

42.

Cloud-Hansen

, Villiard

, Handelsman

, Carey

. Thirteen-lined ground squirrels (Spermophilus tridecemlineatus) harbor multiantibiotic-resistant bacteria. Am Assoc Lab Animal Sci, 2007; 46:21–23.

43.

Cummings

, Vessey

. Agricultural influences on movement patterns of white-footed mice (Peromyscus leucopus). Am Midl Nat, 1994; 132:209.

44.

Davies

, Breslin

. Observations on Salmonella contamination of commercial laying farms before and after cleaning and disinfection. Vet Rec, 2003; 152:283–287.

45.

Davies

, Wray

. Mice as carriers of Salmonella Enteritidis on persistently infected poultry units. Vet Rec, 1995; 137:337–341.

46.

de Oliveira

, de Paula Gabardo

, Guedes

RMC

, Poncet

, et al. Rodents are carriers of Clostridioides difficile strains similar to those isolated from piglets. Anaerobe, 2018; 51:61–63.

47.

Depamede

, Sriasih

, Takahashi

, Nagashima

, et al. Frequent detection and characterization of hepatitis E virus variants in wild rats (Rattus rattus) in Indonesia. Arch Virol, 2013; 158:87–96.

48.

De Sabato

, Ianiro

, Monini

, De Lucia

, et al. Detection of hepatitis E virus RNA in rats caught in pig farms from Northern Italy. Zoonoses Public Health, 2020; 67:62–69.

49.

Dick

, Pozio

. Trichinella spp. and trichinellosis. Paras Dis Wild Mammals, 2001; 2:380–396.

50.

Dirsmith

, VanDalen

, Fry

, Charles

, et al. Leptospirosis in fox squirrels (Sciurus niger) of Larimer county, Colorado, USA. J Wildl Dis, 2013; 49:641–645.

51.

Drickamer

LC.

Seed Preferences in wild caught Peromyscus maniculatus bairdii and Peromyscus leucopus noveboracensis . J Mammal, 1970; 51:191–194.

52.

Dubey

, Weigel

, Siegel

, Thulliez

, et al. Sources and reservoirs of Toxoplasma gondii infection on 47 swine farms in Illinois. J Parasitol, 1995; 723–729.

53.

Ejercito

, Cai

, Htwe

, Taki

, et al. Serological evidence of Coxiella burnetii infection in wild animals in Japan. J Wildl Dis, 1993; 29:481–484.

54.

Elliott

Social behavior and foraging ecology of the eastern chipmunk (Tamias striatus) in the Adirondack Mountains. Smithson Contrib Zool, 1978:1–107.

55.

Ellis

, Regnery

, Beati

, Bacellar

, et al. Rats of the Genus Rattus are reservoir hosts for pathogenic Bartonella species: An old world origin for a new world disease?. J Infect Dis, 1999; 180:220–224.

56.

Enright

, Franti

, Behymer

, Longhurst

, et al. Coxiella burnetii in a wildlife-livestock environment: Distribution of Q fever in wild mammals. Am J Epidemiol, 1971; 94:79–90.

57.

Enright

, Longhurst

, Franti

, Wright

, et al. Some observations on domestic sheep and wildlife relationships in Q-fever. Bull Wildl Dis Assoc, 1969; 5:276–283.

58.

Espinosa

, Gray

, Duffy

, Fanning

, et al. A scoping review on the prevalence of Shiga-toxigenic Escherichia coli in wild animal species. Zoonoses Public Health, 2018; 65:911–920.

59.

Favorov

, Kosoy

, Tsarev

, Childs

, et al. Prevalence of antibody to hepatitis E virus among rodents in the United States. J Infect Dis, 2000; 181:449–455.

60.

Fernie

, Park

RWA

. The isolation and nature of campylobacters (microaerophilic vibrios) from laboratory and wild rodents. J Med Microbiol, 1977; 10:325–330.

61.

Fitzpatrick

FL.

The Ecology and Economic Status of Citellus tridecemlineatus. Iowa City, Iowa: University of Iowa Studies in Natural History,, 1925; (New Series No. 86. 11:3–40).

62.

Foronda

, Plata-Luis

, del Castillo-Figueruelo

, Fernández-Álvarez Á, et al. Serological survey of antibodies to Toxoplasma gondii and Coxiella burnetii in rodents in north-western African islands (Canary Islands and Cape Verde). Onderstepoort J Vet Res, 2015; 82:01–4.

63.

Franco

DA.

Campylobacter species: Considerations for controlling a foodborne pathogen. J Food Prot, 1988; 51:145–153.

64.

Friend

Tularemia. US Geological Survey, 2006. Reston, VA: xi, 67p. doi:10.3133/cir1297. https://doi.org/10.3133/cir1297

65.

Frittelli

JF.

Port and Maritime Security. New York, NY: Nova Publishers, 2008.

66.

Fukushima

, Hoshina

, Gomyoda

. Long-term survival of shiga toxin-producing Escherichia coli O26, O111, and O157 in bovine feces. Appl Environ Microbiol, 1999; 65:5177–5181.

67.

Garber

, Smeltzer

, Fedorka-Cray

, Ladely

, et al. Salmonella enterica serotype Enteritidis in table egg layer house environments and in mice in US layer houses and associated risk factors. Avian Dis, 2003; 47:134–142.

68.

Gardon

, Héraud

, Laventure

, Ladam

, et al. Suburban transmission of Q fever in French Guiana: Evidence of a wild reservoir. J Infect Dis, 2001; 184:278–284.

69.

Gast

, Holt

. Persistence of Salmonella Enteritidis from one day of age until maturity in experimentally infected layer chickens. Poult Sci, 1998; 77:1759–1762.

70.

Gómez

, Kilpatrick

, Kramer

, Dupuis

, et al. Land use and West Nile Virus seroprevalence in wild mammals. Emerg Infect Dis, 2008; 14:962–965.

71.

Gould

, Miesse

. Recovery of a Rickettsia of the Spotted Fever group from Microtus pennsylvanicus from Virginia. Exp Biol Med, 1954; 85:558–561.

72.

Grass

, Gould

, Mahon

. Epidemiology of foodborne disease outbreaks caused by Clostridium perfringens, United States, 1998–2010. Foodborne Pathog Dis, 2013; 10:131–136.

73.

Greig

, Rajić A, Young I, Mascarenhas M, et al. A scoping review of the role of wildlife in the transmission of bacterial pathogens and antimicrobial resistance to the food chain. Zoonoses Public Health, 2015; 62:269–284.

74.

Guard-Petter

, Henzler

, Rahman

, Carlson

. On-farm monitoring of mouse-invasive Salmonella enterica serovar Enteritidis and a model for its association with the production of contaminated eggs. Appl Environ Microbiol, 1997; 63:1588–1593.

75.

Guenther

, Grobbel

, Heidemanns

, Schlegel

, et al. First insights into antimicrobial resistance among faecal Escherichia coli isolates from small wild mammals in rural areas. Sci Total Environ, 2010; 408:3519–3522.

76.

Guenther

, Wuttke

, Bethe

, Vojtěch

, et al. Is fecal carriage of extended-spectrum-β-lactamase-producing Escherichia coli in urban rats a risk for public health?. Antimicrob Agents Chemother, 2013; 57:2424–2425.

77.

Gurycova

, Výrosteková V, Khanakah G, Kocianova E, et al. Importance of surveillance of tularemia natural foci in the known endemic area of Central Europe, 1991–1997. Wien Klin Wochenschr, 2001; 113:433–438.

78.

Gyuranecz

, Dénes

, Dán Á

RigóK

. , et al. Susceptibility of the common hamster (Cricetus cricetus) to Francisella tularensis and its effect on the epizootiology of tularemia in an area where both are endemic. J Wildl Dis, 2010; 46:1316–1320.

79.

Han

, Schmidt

, Bowden

, Drake

. Rodent reservoirs of future zoonotic diseases. PNAS, 2015; 112:7039–7044.

80.

Hancock

, Besser

, Rice

, Ebel

, et al. Multiple sources of Escherichia coli O157 in feedlots and dairy farms in the Northwestern USA. Prev Vet Med, 1998; 35:11–19.

81.

Hanson

, Gauld

, Sinha

, Yuill

. Isolation of La Crosse Virus (California Encephalitis Group) from the chipmunk (Tamias striatus), an Amplifier Host*. Am J Trop Med Hyg, 1975; 24:999–1005.

82.

, Innis

, Shrestha

, Clayson

, et al. Evidence that rodents are a reservoir of hepatitis E virus for humans in Nepal. J Clin Microbiol, 2002; 40:4493–4498.

83.

Helmy

, Spierling

, Schmidt

, Rosenfeld

, et al. Occurrence and distribution of Giardia species in wild rodents in Germany. Paras Vectors, 2018; 11:213.

84.

Hensgens

MPM

, Keessen

, Squire

, Riley

, et al. Clostridium difficile infection in the community: A zoonotic disease?. Clin Microbiol Infect, 2012; 18:635–645.

85.

Henzler

, Opitz

. The role of mice in the epizootiology of Salmonella Enteritidis infection on chicken layer farms. Avian Dis, 1992; 625–631.

86.

Hiett

, Stern

, Fedorka-Cray

, Cox

, et al. Molecular subtype analyses of Campylobacter spp. from Arkansas and California poultry operations. Appl Environ Microbiol, 2002; 68:6220–6236.

87.

Hill

, Simons

, Kelly

, Snary

. A farm transmission model for Salmonella in pigs, applicable to EU Member States. Risk Anal, 2016; 36:461–481.

88.

Hilton

, Willis

, Hickie

. Isolation of Salmonella from urban wild brown rats (Rattus norvegicus) in the West Midlands, UK. Int J Environ Health Res, 2002; 12:163–168.

89.

Himsworth

, Parsons

, Jardine

, Patrick

. Rats, cities, people, and pathogens: A systematic review and narrative synthesis of literature regarding the ecology of rat-associated zoonoses in urban centers. Vector-Borne Zoonotic Dis, 2013; 13:349–359.

90.

Himsworth

, Patrick

, Mak

, Jardine

, et al. Carriage of Clostridium difficile by wild urban Norway rats (Rattus norvegicus) and black rats (Rattus rattus). Appl Environ Microbiol, 2014; 80:1299–1305.

91.

Himsworth

, Zabek

, Desruisseau

, Parmley

, et al. Prevalence and characteristics of Escherichia coli and Salmonella spp. in the feces of wild urban Norway and black rats (Rattus norvegicus and Rattus rattus) from an inner-city neighborhood of Vancouver, Canada. J Wildl Dis, 2015; 51:589–600.

92.

Hirano

, Ding

, Li

, Takeda

, et al. Evidence for widespread infection of hepatitis E virus among wild rats in Japan. Hepatol Res, 2003; 27:1–5.

93.

Hoelzer

, Moreno Switt

, Wiedmann

. Animal contact as a source of human non-typhoidal salmonellosis. Vet Res, 2011; 42:34.

94.

Hoffman

, Maculloch

, Batz

Economic burden of major foodborne illnesses acquired in the United States. Economic Information Bulletin, Number 140; 10.22004/ag.econ.205081. AgEcon Search 2015.

95.

Hoffmann

, Scallan

. Chapter 2—Epidemiology, cost, and risk analysis of foodborne disease. In: Dodd

CER

, Aldsworth

, Stein

, Cliver

, Riemann

, eds. Foodborne Diseases, 3rd ed. Cambridge, MA: Academic Press; 2017. p. 31–63.

96.

Iinuma

, Hayashidani

, Kaneko

, Ogawa

, et al. Isolation of Yersinia enterocolitica serovar O8 from free-living small rodents in Japan. J Clin Microbiol, 1992; 30:240–242.

97.

Inoue

, Iida

, Tanikawa

, Maruyama

, et al. Isolation of Listeria monocytogenes from roof rats (Rattus rattus) in buildings in Tokyo. J Vet Med Sci, 1991; 53:521–522.

98.

Inoue

, Tanikawa

, Kawaguchi

, Iida

, et al. Prevalence of Listeria (spp.) in wild rats captured in the Kanto area of Japan. J Vet Med Sci, 1992; 54:461–463.

99.

Jameson

EW.

Food of Deer mice, Peromyscus maniculatus and P. boylei, in the Northern Sierra Nevada, California. J Mammal, 1952; 33:50.

100.

Jardine

, Reid-Smith

, Rousseau

, Weese

. Detection of Clostridium difficile in small and medium-sized wild mammals in Southern Ontario, Canada. J Wildl Dis, 2013; 49:418–421.

101.

Jijón

, Wetzel

, LeJeune

. Salmonella enterica isolated from wildlife at two Ohio rehabilitation centers. J Zoo Wildl Med, 2007; 38:409–413.

102.

Johne

, Heckel

, Plenge-Bönig

, Kindler

, et al. Novel hepatitis E virus genotype in Norway rats, Germany. Emerg Infect Dis, 2010; 16:1452.

103.

Joutsen

, Laukkanen-Ninios

, Henttonen

, Niemimaa

, et al. Yersinia spp. in wild rodents and shrews in Finland. Vector-Borne Zoonotic Dis, 2017; 17:303–311.

104.

Kabrane-Lazizi

, Fine

, Elm

, Glass

, et al. Evidence for widespread infection of wild rats with hepatitis E virus in the United States. Am J Trop Med Hyg, 1999; 61:331–335.

105.

Kalorey

, Kurkure

, Warke

, Rawool

, et al. Isolation of pathogenic Listeria monocytogenes in faeces of wild animals in captivity. Comp Immunol Microbiol Infect Dis, 2006; 29:295–300.

106.

Kanai

, Inoue

, Mano

, Nonaka

, et al. Epizootiological survey of Trichinella spp. infection in carnivores, rodents and insectivores in Hokkaido, Japan. Jpn J Vet Res, 2007; 54:175–182.

107.

Kanai

, Miyasaka

, Uyama

, Kawami

, et al. Hepatitis E virus in Norway rats (Rattus norvegicus) captured around pig farms. BMC Res Notes, 2012; 5:4.

108.

Kaneko

, Hashimoto

. Occurrence of Yersinia enterocolitica in wild animals. Appl Environ Microbiol, 1981; 41:635–638.

109.

Karetnyĭ IU, Dzhumalieva DI, Usmanov RK, Titova IP, et al.. The possible involvement of rodents in the spread of viral hepatitis E. Zh Mikrobiol Epidemiol Immunobiol, 1993:52–56.

110.

Karmali

MA.

Infection by Shiga toxin-producing Escherichia coli . Mol Biotechnol, 2004; 26:117–122.

111.

Kaysser

, Seibold

, Mätz-Rensing

, Pfeffer

, et al. Re-emergence of tularemia in Germany: Presence of Francisella tularensis in different rodent species in endemic areas. BMC Infect Dis, 2008; 8:157.

112.

Keessen

, Gaastra

, Lipman

LJA

. Clostridium difficile infection in humans and animals, differences and similarities. Vet Microbiol, 2011; 153:205–217.

113.

Khademvatan

, Foroutan

, Hazrati-Tappeh

, Dalvand

, et al. Toxoplasmosis in rodents: A systematic review and meta-analysis in Iran. J Infect Public Health, 2017; 10:487–493.

114.

Kijlstra

, Meerburg

, Cornelissen

, De Craeye

, et al. The role of rodents and shrews in the transmission of Toxoplasma gondii to pigs. Vet Parasitol, 2008; 156:183–190.

115.

Kilonzo

, Li

, Vivas

, Jay-Russell

, et al. Fecal shedding of zoonotic foodborne pathogens by wild rodents in a major agricultural region of the Central California Coast. Appl Environ Microbiol, 2013; 79:6337–6344.

116.

Kilonzo

, Li

, Vodoz

, Xiao

, et al. Quantitative shedding of multiple genotypes of Cryptosporidium and Giardia by Deer mice (Peromyscus maniculatus) in a major agricultural region on the California Central Coast. J Food Prot, 2017; 80:819–828.

117.

Kiupel

, Simmons

, Fitzgerald

, Wise

, et al. West Nile Virus infection in eastern fox squirrels (Sciurus niger). Vet Pathol, 2003; 40:703–707.

118.

Koprowski

JL.

Sciurus carolinensis. Mamm Species, 1994a:1.

119.

Koprowski

JL.

Sciurus niger. Mamm Species, 1994b:1.

120.

Koskela

, Kalin-Mänttäri

, Hemmilä H, Smura T, et al. Metagenomic evaluation of bacteria from voles. Vector-Borne Zoonotic Dis, 2017; 17:123–133.

121.

Kozak

, Boerlin

, Janecko

, Reid-Smith

, et al. Antimicrobial resistance in Escherichia coli isolates from swine and wild small mammals in the proximity of swine farms and in natural environments in Ontario, Canada. Appl Environ Microbiol, 2009; 75:559–566.

122.

Krijger

, Meerburg

, Harmanus

, Burt

. Clostridium difficile in wild rodents and insectivores in the Netherlands. Lett Appl Microbiol, 2019; 69:35–40.

123.

Lack

, Hamilton

, Braun

, Mares

, et al. Comparative phylogeography of invasive Rattus rattus and Rattus norvegicus in the U.S. reveals distinct colonization histories and dispersal. Biol Invasions, 2013; 15:1067–1087.

124.

Lack

, Volk

, Van Den Bussche

. Hepatitis E virus genotype 3 in wild rats, United States. Emerg Infect Dis, 2012; 18:1268.

125.

Lackey

, Huckaby

, Ormiston

. Peromyscus leucopus. Mamm Species, 1985:1.

126.

Laidler

, Tourdjman

, Buser

, Hostetler

, et al. Escherichia coli O157:H7 infections associated with consumption of locally grown strawberries contaminated by deer. Clin Infect Dis, 2013; 57:1129–1134.

127.

Lapuz

RRSP

, Umali

, Suzuki

, Shirota

, et al. Comparison of the prevalence of Salmonella infection in layer hens from commercial layer farms with high and low rodent densities. Avian Dis, 2012; 56:29–34.

128.

Larrieu

, Molina

, Albarracín

, Mancini

, et al. Porcine and rodent infection with Trichinella, in the Sierra Grande area of Río Negro province, Argentina. Ann Trop Med Parasitol, 2004; 98:725–731.

129.

Lawlor

, Hall

. The mammals of North America. 2nd ed. John Wiley and Sons, New York. J Mammal, 1982; 63:718–719.

130.

Lee

, Byers

, Donovan

, Zabek

, et al. Methicillin-resistant Staphylococcus aureus in urban Norway rat (Rattus norvegicus) populations: Epidemiology and the impacts of kill-trapping. Zoonoses Public Health, 2019; 66:343–348.

131.

Lesley

, Velnetti

, Fazira

, Kasing

, et al. Detection and antibiotic susceptibility profiles of Listeria monocytogenes in wildlife and water samples in Kubah National Park, Sarawak, Malaysia. Int Food Res J, 2016; 23.

132.

Liu

, Baoliang

, Yingqun

, Ming

, et al. Coxiella burnetii in rodents on Heixiazi Island at the Sino-Russian Border. Am J Trop Med Hyg, 2013; 88:770–773.

133.

Loutfy

, Awad

, El-Masry

, Kandil

. Study on rodents infestation in Alexandria and prevalence of Trichinella spiralis infection among them. J Egypt Soc Parasitol, 1999; 29:897.

134.

Lyautey

, Hartmann

, Pagotto

, Tyler

, et al. Characteristics and frequency of detection of fecal Listeria monocytogenes shed by livestock, wildlife, and humans. Can J Microbiol, 2007; 53:1158–1167.

135.

Madhav

, Wagoner

, Douglass

, Mills

. Delayed density-dependent prevalence of Sin Nombre virus antibody in Montana deer mice (Peromyscus maniculatus) and implications for human disease risk. Vector-Borne Zoonotic Dis, 2007; 7:353–364.

136.

Magee

, Steele

, Kelly

, Jacobs

. Tularemia transmitted by a squirrel bite. Pediatr Infect Dis J, 1989; 8:123–125.

137.

Maldonado

, Fiser

, Nakatsu

, Bhunia

. Cytotoxicity potential and genotypic characterization of Escherichia coli isolates from environmental and food sources. Appl Environ Microbiol, 2005; 71:1890–1898.

138.

Markowski

, Ginsberg

, Hyland

, Hu

. Reservoir competence of the meadow vole (Rodentia: Cricetidae) for the Lyme disease spirochete Borrelia burgdorferi . J Med Entomol, 1998; 35:804–808.

139.

Martin

, Schnurrenberger

, Andersen

, Hsu

. Prevalence of Trichinella spiralis in wild animals on two Illinois swine farms. J Parasitol, 1968; 1:108–111.

140.

Masakul

, Thaprathom

, Chaisiri

, Karnchanabanthoeng

, et al. Infection rates of Giardia duodenalis associated with diversity of rodents in Thailand. Agricultural Innovation for Global Value Chain, Proceedings of 54th Kasetsart University Annual Conference, 2-5 February 2016, Kasetsart University, Thailand Vol 1, Plants, Animals, Veterinary Medicine, Fisheries, Agricultural Extension and Home Economics,, 2016:523–530.

141.

McClane

BA.

Clostridium perfringens in Food Microbiology Fundamentals and Frontiers. Doyle MP, Beuchat LR, eds. Washington DC: ASM Press, 2007.

142.

Meerburg

, De Craeye

, Dierick

, Kijlstra

. Neospora caninum and Toxoplasma gondii in brain tissue of feral rodents and insectivores caught on farms in the Netherlands. Vet Parasitol, 2012; 184:317–320.

143.

Meerburg

, Jacobs-Reitsma

, Wagenaar

, Kijlstra

. Presence of Salmonella and Campylobacter spp. in wild small mammals on organic farms. Appl Environ Microbiol, 2006; 72:960–962.

144.

Meerburg

, Kijlstra

. Role of rodents in transmission of Salmonella and Campylobacter . J Sci Food Agric, 2007; 87:2774–2781.

145.

Meerburg

, Reusken

. The role of wild rodents in spread and transmission of Coxiella burnetii needs further elucidation. Wildl Res, 2011; 38:617–625.

146.

Meerburg

BG.

Rodents are a risk factor for the spreading of pathogens on farms. Vet Microbiol, 2010; 142:464–465.

147.

Montero

, Bodero

, Riveros

, Lapierre

, et al. Molecular epidemiology and genetic diversity of Listeria monocytogenes isolates from a wide variety of ready-to-eat foods and their relationship to clinical strains from listeriosis outbreaks in Chile. Front Microbiol, 2015; 6:384.

148.

Mrochen

, Schulz

, Fischer

, Jeske

, et al. Wild rodents and shrews are natural hosts of Staphylococcus aureus . Int J Med Microbiol, 2017; 308:590–597.

149.

Nelson

, Haldorson

, Stanton

, Noh

, et al. Francisella tularensis infection without lesions in gray tree squirrels (Sciurus griseus): A diagnostic challenge. J Vet Diagn Invest, 2014; 26:312–315.

150.

Nidaullah

, Abirami

, Shamila-Syuhada

, Chuah

L-O

, et al. Prevalence of Salmonella in poultry processing environments in wet markets in Penang and Perlis, Malaysia. Vet World, 2017; 10:286–292.

151.

Nielsen

, Skov

, Madsen

, Lodal

, et al. Verocytotoxin-producing Escherichia coli in wild birds and rodents in close proximity to farms. Appl Environ Microbiol, 2004; 70:6944–6947.

152.

Orsborn

, Lackman

, Holdenried

, Stoenner

. The occurrence of Coxiella burnetii, Brucella, and other pathogens among fauna of the Great Salt Lake Desert in Utah. Am J Trop Med Hyg, 1959; 8:590–596.

153.

Pacha

, Clark

, Williams

, Carter

, et al. Small rodents and other mammals associated with mountain meadows as reservoirs of Giardia spp. and Campylobacter spp. Appl Environ Microbiol, 1987; 53:1574–1579.

154.

Panti-May

, De Andrade

RRC

, Gurubel-Gonzalez

, Palomo-Arjona

, et al. A survey of zoonotic pathogens carried by house mouse and black rat populations in Yucatan, Mexico. 2017. Epidemiol Infect, 2017; 145:2287–2295.

155.

Perez

, Clavero

, Hernandez

. Investigations on the epidemiology of Q fever in Spain; mountain rabbits and dormouses as a reservoir of Coxiella burnetii . Rev Sanid Hig Publica, 1952; 26:81–87.

156.

Phifer-Rixey

, Nachman

. Insights into mammalian biology from the wild house mouse Mus musculus . eLife, 2015; 4:e05959.

157.

Pocock

MJO

, Searle

, Betts

, White

PCL

. Patterns of infection by Salmonella and Yersinia spp. in commensal house mouse (Mus musculus domesticus) populations. J Appl Microbiol, 2001; 90:755–760.

158.

Pokorná. V, Aldová E. Finding of Yersinia enterocolitica in Rattus rattus . J Hyg Epidemiol Microbiol Immunol, 1977; 21:104–105.

159.

Pozio

The broad spectrum of Trichinella hosts: From cold-to warm-blooded animals. Vet Parasitol, 2005; 132:3–11.

160.

Pozio

, Rinaldi

, Marucci

, Musella

, et al. Hosts and habitats of Trichinella spiralis and Trichinella britovi in Europe. Int J Parasitol, 2009; 39:71–79.

161.

Puckett

, Park

, Combs

, Blum

, et al. Global population divergence and admixture of the brown rat (Rattus norvegicus). Proc R Soc B, 2016; 283:20161762.

162.

Purcell

, Engle

, Rood

, Kabrane-Lazizi

, et al. Hepatitis e virus in rats, Los Angeles, California, USA. Emerg Infect Dis, 2011; 17:2216.

163.

Reich

LM.

Microtus pennsylvanicus. Mamm Species, 1981:1.

164.

Reusken

, van der Plaats

, Opsteegh

, de Bruin

, et al. Coxiella burnetii (Q fever) in Rattus norvegicus and Rattus rattus at livestock farms and urban locations in the Netherlands; could Rattus spp. represent reservoirs for (re)introduction?. Prev Vet Med, 2011; 101:124–130.

165.

Ribicich

, Gamble

, Bolpe

, Scialfa

, et al. Trichinella infection in wild animals from endemic regions of Argentina. Parasitol Res, 2010; 107:377–380.

166.

Riemann

, Behymer

, Franti

, Crabb

, et al. Survey of Q-fever agglutinins in birds and small rodents in Northern California, 1975–76. J Wildl Dis, 1979; 15:515–523.

167.

Rodriguez

, Pangloli

, Richards

, Mount

, et al. Prevalence of Salmonella in diverse environmental farm samples. J Food Prot, 2006; 69:2576–2580.

168.

Rodriguez

, Hakimi

D-E

, Vanleyssem

, Taminiau

, et al. Clostridium difficile in beef cattle farms, farmers and their environment: Assessing the spread of the bacterium. Vet Microbiol, 2017; 210:183–187.

169.

Rosef

, Gondrosen

, Kapperud

, Underdal

. Isolation and characterization of Campylobacter jejuni and Campylobacter coli from domestic and wild mammals in Norway. Appl Environ Microbiol, 1983; 46:855–859.

170.

Rossow

, Sissonen

, Koskela

, Kinnunen

, et al. Detection of Francisella tularensis in voles in Finland. Vector-Borne Zoonotic Dis, 2014; 14:193–198.

171.

Rozental

, Ferreira

, Guterres

, Mares-Guia

, et al. Zoonotic pathogens in Atlantic Forest wild rodents in Brazil: Bartonella and Coxiella infections. Acta Trop, 2017; 168:64–73.

172.

Ruffolo

, Toledo

, Martins

, Bugni

, et al. Isolation and genotyping of Toxoplasma gondii in seronegative urban rats and presence of antibodies in communicating dogs in Brazil. Rev Inst Med Trop São Paulo, 2016; 58.

173.

Sadighian

, Arfaa

, Movafagh

. Trichinella spiralis in carnivores and rodents in Isfahan, Iran. J Parasitol, 1973; 59:986.

174.

Saki

, Foroutan-Rad

, Asadpouri

. Molecular characterization of Cryptosporidium spp. in wild rodents of Southwestern Iran using 18s rRNA gene nested-PCR-RFLP and sequencing techniques. J Trop Med, 2016; 2016:1–6.

175.

Scallan

, Hoekstra

, Angulo

, Tauxe

, et al. Foodborne illness acquired in the United States—major pathogens. Emerg Infect Dis, 2011; 17:7–15.

176.

Scharff

RL.

Economic burden from health losses due to foodborne illness in the United States. J Food Prot, 2012; 75:123–131.

177.

Schmidly

, Bradley

. The Mammals of Texas. Austin, TX: University of Texas Press, 2016.

178.

Sekse

, Holst-Jensen

, Dobrindt

, Johannessen

, et al. High throughput sequencing for detection of foodborne pathogens. Front Microbol, 2017; 8:2029.

179.

Sellers

, Long

, Jay-Russell

, Li

, et al. Impact of field-edge habitat on mammalian wildlife abundance, distribution, and vectored foodborne pathogens in adjacent crops. Crop Prot, 2018; 108:1–11.

180.

Shaikenov

, Boev

. Distribution of Trichinella species in the Old World. Wiadomości Parazyt, 1983; 29:596–608.

181.

Sharma

, Hotta

, Yamamoto

, Uda

, et al. Serosurveillance for Francisella tularensis among wild animals in Japan using a newly developed competitive enzyme-linked immunosorbent assay. Vector-Borne Zoonotic Dis, 2014; 14:234–239.

182.

Shayegani

, Stone

, DeForge

, Root

, et al. Yersinia enterocolitica and related species isolated from wildlife in New York State. Appl Environ Microbiol, 1986; 52:420–424.

183.

Shimi

, Keyhani

, Hedayati

. Studies on salmonellosis in the house mouse, Mus musculus . Lab Anim, 1979; 13:33–34.

184.

Silva

, Silva

, Fagliari

, Ávila

, et al. Clinical evaluation of experimental calf infection with Salmonella Dublin . Braz Arch Vet Med Anim Sci, 2008; 60:251–255.

185.

Silva

, D'Elia

, Teixeira ÉP, Pereira

, et al. Clostridium difficile and Clostridium perfringens from wild carnivore species in Brazil. Anaerobe, 2014; 28:207–211.

186.

Singh

, Sethi

, Sharma

. The occurrence of salmonellae in rodent, shrew, cockroach and ant. Int J Zoonoses, 1980; 7:58–61.

187.

Smith

, Moorhouse

, Monaghan

, Taylor

, et al. Sources and survival of Listeria monocytogenes on fresh, leafy produce. J Appl Microbiol, 2018; 125:930–942.

188.

Snyder

DP.

Tamias striatus. Mamm Species, 1982:1.

189.

Song

, Kim

C-Y

, Chang

S-N

, Abdelkader

, et al. Detection and molecular characterization of Cryptosporidium spp. from wild rodents and insectivores in South Korea. Korean J Parasitol, 2015; 53:737–743.

190.

Splettstoesser

, Mätz-Rensing

, Seibold

, Tomaso

, et al. Re-emergence of Francisella tularensis in Germany: Fatal tularaemia in a colony of semi-free-living marmosets (Callithrix jacchus). Epidemiol Infect, 2007; 135:1256–1265.

191.

Stafford

, Massung

, Magnarelli

, Ijdo

, et al. Infection with agents of human granulocytic ehrlichiosis, lyme Disease, and babesiosis in wild white-footed mice (Peromyscus leucopus) in Connecticut. J Clin Microbiol, 1999; 37:2887–2892.

192.

Stoenner

, Holdenried

, Lackman

, Orsborn Jr

. The occurrence of Coxiella burnetii, Brucella, and other pathogens among fauna of the Great Salt Lake Desert in Utah. Am J Trop Med Hyg, 1959; 8:590–596.

193.

Stojcevic

, Zivicnjak

, Marinculic

, Marucci

, et al. The epidemiological investigation of Trichinella infection in brown rats (Rattus norvegicus) and domestic pigs in Croatia suggests that rats are not a reservoir at the farm level. J Parasitol, 2004; 90:666–670.

194.

Streubel

, Fitzgerald

. Spermophilus tridecemlineatus. Mamm Species, 1978:1.

195.

Summa

, Henttonen

, Maunula

. Human noroviruses in the faeces of wild birds and rodents—New potential transmission routes. Zoonoses Public Health, 2018; 65:512–518.

196.

Syrůček

, Raška

. Q fever in domestic and wild birds. Bull World Health Org, 1956; 15:329.

197.

Tan

, Low

, Ng

, Ibrahim

, et al. Occurrence of zoonotic Cryptosporidium and Giardia duodenalis species/genotypes in urban rodents. Parasitol Int, 2019; 69:110–113.

198.

Tarr

PI.

Escherichia coli O157: H7: Clinical, diagnostic, and epidemiological aspects of human infection. Clin InfectDis, 1995; 20:1–8.

199.

Thompson

, Mykytczuk

, Gooderham

, Schulte-Hostedde

. Prevalence of the bacterium Coxiella burnetii in wild rodents from a Canadian natural environment park. Zoonoses Public Health, 2012; 59:553–560.

200.

Trampel

, Holder

, Gast

. Integrated farm management to prevent Salmonella Enteritidis contamination of eggs. J Appl Poult Res, 2014; 23:353–365.

201.

Trimoulinard

, Beral

, Henry

, Atiana

, et al. Contamination by Salmonella spp., Campylobacter spp. and Listeria spp. of most popular chicken and pork-sausages sold in Reunion Island. Int J Food Microbiol, 2017; 250:68–74.

202.

Ulrich

, Schmidt-Chanasit

, Schlegel

, Jacob

, et al. Network “Rodent-borne pathogens” in Germany: Longitudinal studies on the geographical distribution and prevalence of hantavirus infections. Parasitol Res, 2008; 103:121.

203.

Umali

, Lapuz

RRSP

, Suzuki

, Shirota

, et al. Transmission and shedding patterns of Salmonella in naturally infected captive wild roof rats (Rattus rattus) from a Salmonella contaminated layer farm. Avian Dis, 2012; 56:288–294.

204.

Vandalen

, Shriner

, Sullivan

, Root

, et al. Monitoring exposure to avian influenza viruses in wild mammals. Mamm Rev, 2009; 39:167–177.

205.

Van de Giessen

, van Santen-Verheuvel

, Hengeveld

, Bosch

, et al. Occurrence of methicillin-resistant Staphylococcus aureus in rats living on pig farms. Prev Vet Med, 2009; 91:270–273.

206.

Van Immerseel

, De Buck

, Pasmans

, Bohez

, et al. Intermittent long-term shedding and induction of carrier birds after infection of chickens early posthatch with a low or high dose of Salmonella Enteritidis. Poult Sci, 2004; 83:1911–1916.

207.

Viswanathan

, Pearl

, Taboada

, Parmley

, et al. Molecular and statistical analysis of Campylobacter spp. and antimicrobial-resistant Campylobacter carriage in wildlife and livestock from Ontario farms. Zoonoses Public Health, 2017; 64:194–203.

208.

Vitral

, Pinto

, Lewis-Ximenez

, Khudyakov

, et al. Serological evidence of hepatitis E virus infection in different animal species from the Southeast of Brazil. Mem Inst Oswaldo Cruz, 2005; 100:117–122.

209.

Wang

, Lu

, Lan

, Salazar

, et al. Isolation and characterization of Listeria species from rodents in natural environments in China. Emerg Microb Infect, 2017; 6:1–6.

210.

Weber

, Potel

, Schäfer-Schmidt

, Prell

, et al. Studies on the occurrence of Listeria monocytogenes in fecal samples of domestic and companion animals. Zentralbl Hyg Umweltmed, 1995; 198:117–123.

211.

Weigel

, Dubey

, Siegel

, Kitron

, et al. Risk factors for transmission of Toxoplasma gondii on swine farms in Illinois. J Parasitol, 1995:736–741.

212.

Weis

, Seeliger

. Incidence of Listeria monocytogenes in nature. Appl Microbiol, 1975; 30:29–32.

213.

Whitaker

JO.

Food and external parasites of Spermophilus tridecemlineatus in Vigo county, Indiana. J Mammal, 1972; 53:644–648.

214.

Williams

, Barker

, eds. Infectious Diseases of Wild Mammals. New York, NY: John Wiley & Sons, 2008.

215.

Williams

, Che

, Paulick

, Guo

, et al. New York city house mice (Mus musculus) as potential reservoirs for pathogenic bacteria and antimicrobial resistance determinants. mBio, 2018; 9:e00624-18.

216.

Wilson

, Gabriel

, Leatherbarrow

AJH

, Cheesbrough

, et al. Tracing the source of Campylobacteriosis. PLoS Genet, 2008; 4:e1000203.

217.

Wolf

, Reetz

, Johne

, Heiberg

A-C

, et al. The simultaneous occurrence of human norovirus and hepatitis E virus in a Norway rat (Rattus norvegicus). Arch Virol, 2013; 158:1575–1578.

218.

Wolff

, Dueser

, Berry

. Food habits of sympatric Peromyscus leucopus and Peromyscus maniculatus . J Mammal, 1985; 66:795–798.

219.

Yevdoshenko

, Proreshnaya

. Natural infection of wild animals of Northern Kirghizia with Rickettsia burnetii . Prob Virol, 1961; 6:656–660.

220.

Yoshida

, Sugimoto

, Sato

, Hirai

. Incidence of Listeria monocytogenes in wild animals in Japan. J Vet Med Sci, 2000; 62:673–675.

221.

Zhang

, Liu

, Chu

, He

, et al. Francisella tularensis in Rodents, China. Emerg Infect Dis, 2006; 12:994–996.

222.

Zhmaeva

, Pchelkina

, Mishchenko

, Karulin

. The epidemiological importance of ectoparasites of birds in a natural focus of Q fever in the south of central Asia. Doklady Akademii Nauk SSSR, 1955; 101:387–389.

223.

Zimmerman

EG.

A comparison of habitat and food of two species of Microtus . J Mammal, 1965; 46:605–612.