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Keywords:

  • Chiroptera;
  • infectious agents;
  • enteric bacteria;
  • Salmonella ;
  • Yersinia ;
  • Pasteurella ;
  • Leptospira ;
  • arthropod-borne;
  • antimicrobial resistance;
  • wildlife;
  • zoonosis

Summary

  1. Top of page
  2. Summary
  3. Impacts
  4. Introduction
  5. Enteric Pathogens
  6. Arthropod-Borne Bacterial Pathogens
  7. Bacteria of the Genus Leptospira
  8. Pasteurella Infections in Bats
  9. Bacteria with Antibiotic Resistance
  10. Implications on Bats as Carriers of Pathogenic Bacteria
  11. Conclusions
  12. Acknowledgements
  13. References

The occurrence of emerging infectious diseases and their relevance to human health has increased the interest in bats as potential reservoir hosts and vectors of zoonotic pathogens. But while previous and ongoing research activities predominantly focused on viral agents, the prevalence of pathogenic bacteria in bats and their impact on bat mortality have largely neglected. Enteric pathogens found in bats are often considered to originate from the bats’ diet and foraging habitats, despite the fact that little is known about the actual ecological context or even transmission cycles involving bats, humans and other animals like pets and livestock. For some bacterial pathogens common in human and animal diseases (e.g. Pasteurella, Salmonella, Escherichia and Yersinia spp.), the pathogenic potential has been confirmed for bats. Other bacterial pathogens (e.g. Bartonella, Borrelia and Leptospira spp.) provide evidence for novel species that seem to be specific for bat hosts but might also be of disease importance in humans and other animals. The purpose of this review is to summarize the current knowledge of bacterial pathogens identified in bats and to consider factors that might influence the exposure and susceptibility of bats to bacterial infection but could also affect bacterial transmission rates between bats, humans and other animals.


Impacts

  1. Top of page
  2. Summary
  3. Impacts
  4. Introduction
  5. Enteric Pathogens
  6. Arthropod-Borne Bacterial Pathogens
  7. Bacteria of the Genus Leptospira
  8. Pasteurella Infections in Bats
  9. Bacteria with Antibiotic Resistance
  10. Implications on Bats as Carriers of Pathogenic Bacteria
  11. Conclusions
  12. Acknowledgements
  13. References
  •  Despite the multitude of publications on infectious agents detected in bat species worldwide, little is known about the presence of bacterial pathogens in bats.
  •  The purpose of this review is to provide an overview of main bacterial pathogens isolated from bats, which have the potential to cause disease in bats and humans.
  •  Furthermore, specific characteristics of bats as carriers of pathogenic bacteria are discussed to identify areas that could be rewarding for further research.

Introduction

  1. Top of page
  2. Summary
  3. Impacts
  4. Introduction
  5. Enteric Pathogens
  6. Arthropod-Borne Bacterial Pathogens
  7. Bacteria of the Genus Leptospira
  8. Pasteurella Infections in Bats
  9. Bacteria with Antibiotic Resistance
  10. Implications on Bats as Carriers of Pathogenic Bacteria
  11. Conclusions
  12. Acknowledgements
  13. References

The order Chiroptera is the most diverse and geographically distributed mammalian taxon found on all continents except Antarctica (Schipper et al., 2008). Bats are unique among mammals in their capability to fly and cover long distances during seasonal migrations, and their potential for very large, colonial populations. These characteristics together with their long lifespan and their ability to inhabit a multitude of diverse ecological niches make bats among the most successful species on earth but have also increased the global interest in bats as potential reservoir hosts and vectors of zoonotic pathogens (Calisher et al., 2006; Wong et al., 2007; Kuzmin et al., 2011; Wang et al., 2011). Their role in disease epidemiology is even more important as bats are susceptible to a multitude of different microorganisms that include viruses, bacteria, fungi and parasites (Whitaker et al., 2009; Wibbelt et al., 2009). Several of these infectious agents are common to humans and domestic animals.

Many studies investigated the presence of infectious agents in bats, in particular those that have a zoonotic potential for humans. However, the knowledge regarding the impact of microorganisms on bat hosts is limited for the majority of microbial species detected (Mühldorfer et al., 2011a,b). In addition, the knowledge of the natural microflora of bats is sparse. Because of limitations in sample collection and preservation, bacteriological investigations in bats are largely restricted to the gastrointestinal bacterial flora (e.g. Klite, 1965a; Heard et al., 1997; Gordon and FitzGibbon, 1999; Di Bella et al., 2003), serology (e.g. Choi and Lee, 1996; Reeves et al., 2006; Zetun et al., 2009; D’Auria et al., 2010) and bacterial detection by genetic methods from blood (e.g. Cox et al., 2005; Bessa et al., 2010; Kosoy et al., 2010) and ectoparasite samples (e.g. Reeves et al., 2005, 2007; Schwan et al., 2009).

The present review provides an overview of available information on bacteria isolated from bats with a particular emphasis on main bacterial pathogens, which have the potential to cause disease in bats and humans. In addition, factors likely to affect the susceptibility and exposure of bats to bacterial pathogens were considered. Some of these factors also draw attention to relationships by which bats may act as vectors of pathogenic bacteria.

Enteric Pathogens

  1. Top of page
  2. Summary
  3. Impacts
  4. Introduction
  5. Enteric Pathogens
  6. Arthropod-Borne Bacterial Pathogens
  7. Bacteria of the Genus Leptospira
  8. Pasteurella Infections in Bats
  9. Bacteria with Antibiotic Resistance
  10. Implications on Bats as Carriers of Pathogenic Bacteria
  11. Conclusions
  12. Acknowledgements
  13. References

The majority of information regarding the normal gastrointestinal bacterial flora of bats and the presence or absence of bacterial enteropathogens comes from traditional microbiological studies (e.g. Klite, 1965a,b; Arata et al., 1968; Heard et al., 1997; Gordon and FitzGibbon, 1999; Di Bella et al., 2003; Adesiyun et al., 2009). Most of these studies have so far concentrated on bacterial species that may present a potential health threat to humans or domestic animals (e.g. Arata et al., 1968; Adesiyun et al., 2009; Reyes et al., 2011). Enteric pathogens such as Salmonella, Shigella, Yersinia and Campylobacter species have occasionally been found in bats (Table 1).

Table 1. Enteropathogenic bacteria isolated from apparently healthy and diseased bats
Family of batsBacteria na SourceLocationReference
  1. All enteropathogenic bacteria have been isolated from bats by traditional culture methods except for Salmonella spp. of reference Reyes et al. (2011), which were detected by PCR.

  2. aNumber of positive bats/total number of bats sampled.

  3. bSalmonella isolates named by the respective serotype of Salmonella enterica ssp. enterica.

Vespertilionidae Campylobacter jejuni 17/634Faecesthe Netherlands Hazeleger et al. (2010)
Clostridium perfringens 11/76FaecesCzech Republic Hajkova and Pikula (2007)
Clostridium sordellii 1/486IntestineGermany Mühldorfer et al. (2011a)
Listeria spp.1/149Rectal swabsPoland Różalska et al. (1998)
Salmonella spp.2/46IntestinePhilippines Reyes et al. (2011)
Salmonella group Db1/73Heart bloodUK Daffner (2001)
Salmonella Enteritidisb, Salmonella Typhimuriumb3/486Organ samplesGermany Mühldorfer et al. (2011a)
Shigella flexneri 5/149Rectal swabsPoland Różalska et al. (1998)
Vibrio spp.1/486Organ samplesGermany Mühldorfer et al. (2011a)
Yersinia enterocolitica, Yersinia spp.31/149Rectal swabsPoland Różalska et al. (1998)
Yersinia enterocolitica, Y. pseudotuberculosis2/486Organ samplesGermany Mühldorfer et al. (2010)
Molossidae Clostridium spp.3/20Intestine Klite (1965a)
Listeria monocytogenes 2/234IntestineTogo Höhne et al. (1975)
Salmonella Caracasb, Salmonella group I2/37Gastrointestinal tractTrinidad Adesiyun et al. (2009)
Salmonella Anatumb, S. Blockleyb2/184Intestinal/rectal swabsColombia Arata et al. (1968)
Salmonella Enteritidisb, Salmonella O48b10/88FaecesMadagascar Cassel-Béraud and Richard (1988)
Shigella boydii-21/184Intestinal/rectal swabsColombia Arata et al. (1968)
Mormoopidae Clostridium spp.5/20Intestine Klite (1965a)
Phyllostomidae
 Desmodontinae Salmonella Typhimuriumb9/100FaecesBrazil Moreno et al. (1975)
Shigella sonnei 1/113FaecesBrazil de Souza et al. (2002)
 Carolliinae Clostridium spp.9/20Intestine Klite (1965a)
 Glossophaginae Salmonella Saintpaulb, S. Typhimurium var. Copenhagenb1/6FaecesPanama Klite (1965b)
 Stenodermatinae Salmonella Llandoffb, S. Sandiegob2/967Intestinal/rectal swabsColombia Arata et al. (1968)
Pteropodidae
 Epomophorinae Listeria monocytogenes 1/2IntestineTogo Höhne et al. (1975)
 Pteropodinae Salmonella Typhib, Salmonella Typhimuriumb58/481Heart blood, organ samplesMadagascar Brygoo et al. (1971)
S. flexneri, S. sonnei17/481Intestine, bileMadagascar Brygoo et al. (1971)
Nectarivorous Salmonella sp.1/47FaecesBrazil de Souza et al. (2002)
Noctilionidae Salmonella Moladeb, Salmonella Rubislawb1/11Gastrointestinal tractTrinidad Adesiyun et al. (2009)

Salmonellosis is a major cause of gastroenteritis in both humans and animals and a global bacterial disease of public health concern and economic importance in industrial livestock (Brenner et al., 2000; Sanchez et al., 2002; Foley and Lynne, 2008). Livestock species and wild birds are considered as an important reservoir of human-pathogenic Salmonella serotypes (Sanchez et al., 2002; Tizard, 2004). However, many domestic and wild animals are colonized by Salmonella, harbouring the bacteria in their gastrointestinal tracts without apparent clinical signs (Sanchez et al., 2002; Hoelzer et al., 2011). A variety of different Salmonella serotypes have been isolated from apparently healthy and diseased bats (Table 1). Almost all of them are serotypes with a broad-host-range (Hoelzer et al., 2011). In particular, Salmonella Enteritidis and Salmonella Typhimurium have been frequently identified, which belong to a small group of Salmonella serotypes mainly associated with disease in humans and animals (Sanchez et al., 2002; Foley and Lynne, 2008; Hoelzer et al., 2011). Both serotypes have been isolated from organ tissues of three individual bats of the family Vespertilionidae that were found dead or severely injured near human habitation (Mühldorfer et al., 2011a,b). Histo-pathologic examination revealed inflammatory lesions in multiple organs of these bats, including interstitial pneumonia and purulent meningitis. Other non-typhoidal Salmonella serotypes have been isolated only once from the intestine of bats. Among these, Salmonella serotypes Anatum, Blockley, Rubislaw, Saintpaul and Sandiego are widespread in livestock and companion animals and of medical importance to humans (CDC, 2009; Hoelzer et al., 2011). However, Salmonella Caracas and Salmonella Llandoff have rarely been identified from human salmonellosis cases (CDC, 2009). In contrast to broad-host-range Salmonella serotypes found in bats, Salmonella Typhi is the causative agent of typhoid fever and almost exclusively associated with disease in humans (Uzzau et al., 2000). Interestingly, this serotype was isolated from heart blood, internal organs and bile of 58 Pteropus rufus from Madagascar (Brygoo et al., 1971), which again provide some evidence for systemic bacterial infection possibly stress-induced by capture and handling of bats inapparently infected with Salmonella Typhi.

Shigellosis is a highly contagious foodborne disease of humans that is caused by four different species of Shigella: S. dysenteriae (group A), S. flexneri (group B), S. boydii (group C) and S. sonnei (group D) (Edwards, 1999; Weir, 2002). The disease symptoms range from mild gastroenteritis to severe dysentery and are restricted to higher primates. In developing countries, Shiga toxin-producing S. dysenteriae are responsible for epidemics of fatal shigellosis in humans (Edwards, 1999; Weir, 2002). Animals may act as asymptomatic carriers but Shigella bacteria are rarely detected in wild or domestic animals other than primates (Edwards, 1999). Shigella strains of serogroups B to D have been isolated from mega- and microbats of diverse feeding habitats (Table 1). Shigella flexneri in particular was detected in more than 3% of bats investigated (Brygoo et al., 1971; Różalska et al., 1998). Together with S. sonnei, it accounts for the majority of human shigellosis cases worldwide (Edwards, 1999; Weir, 2002).

The wide distribution and host range of enteropathogenic Yersinia species, Y. enterocolitica and Y. pseudotuberculosis, and the potential zoonotic risk of human health make yersiniosis a significant bacterial disease. Both bacterial species have frequently been isolated from a wide variety of wild and domestic animals (Mair, 1968, 1973; Blobel and Schließer, 1982; Neubauer et al., 2001). However, the occurrence of enteropathogenic Yersinia species and their impact on bats are largely unknown. A study reported high prevalence of different Yersinia species (∼35%) in the faeces of 70 insectivorous Myotis myotis collected from natural populations in Poland (Różalska et al., 1998). Most of the Yersinia species isolated from bats are widely distributed in the environment and rarely associated with disease in mammals and birds (Shayegani et al., 1986; Bottone et al., 2005). In contrast, Y. pseudotuberculosis often causes enteric or systemic disease in wild mammals induced by stress of cold and humid weather or starvation (Baskin, 1980). A similar case of systemic Y. pseudotuberculosis infection has been described once in an adult insectivorous bat (M. myotis) found dead in Germany after hibernation (Mühldorfer et al., 2010). As diagnostic investigations in bats are markedly impaired by fast decomposition of dead animals, the importance of pathogenic Yersinia species might be underestimated, especially in hibernating bats. Outbreaks of Y. pseudotuberculosis infection have occasionally been observed in closed colonies of captive flying foxes (Williams, 2004; Child-Sanford et al., 2009), which supports the pathogenic potential of Y. pseudotuberculosis strains for bats.

Few studies on bacterial pathogens in chiropteran species investigated the presence of Campylobacter but predominantly failed to isolate bacteria of this genus from bats of diverse feeding habitats (Daffner, 2001; Duignan et al., 2003; Adesiyun et al., 2009). The negative results may reflect a lack of exposure of bats to Campylobacter species (Daffner, 2001; Adesiyun et al., 2009). In wild birds, for example, which are considered as important reservoir of human-pathogenic Campylobacter strains (Kapperud and Rosef, 1983), the presence of these enteropathogens seems to be influenced by their feeding habitats, with the majority of insectivores and granivores rarely tested positive for Campylobacter species (Waldenström et al., 2002). However, insectivorous bats could acquire bacteria from livestock environments (Rosef et al., 1983; Wales et al., 2010), which might explain the presence of human-pathogenic Campylobacter jejuni strains in faecal samples collected from vespertilionid bats in the Netherlands (Hazeleger et al., 2010).

A wide variety of further Gram-negative and Gram-positive bacteria have been isolated from bats often considered as intestinal commensals in relation to their diets (Müller et al., 1980; Pinus and Müller, 1980; Cassel-Béraud and Richard, 1988). Several of these bacterial species (i.e. Escherichia coli, Vibrio spp. and Clostridium spp.) are also known as enteropathogens and are able to cause disease in bats. For example, Clostridium perfringens and C. sordellii have been identified as primary cause of haemorrhagic diarrhoea in European vespertilionid species (Hajkova and Pikula, 2007; Mühldorfer et al., 2011a). Clostridium sordellii was isolated from a traumatized whiskered bat (Myotis mystacinus) found moribund in close proximity to humans (Mühldorfer et al., 2011a). Furthermore, C. perfringens was identified in a group of Nyctalus noctula kept in captivity for medical treatment (Hajkova and Pikula, 2007). Other enteropathogenic bacteria such as E. coli and Vibrio species have been described to cause extra-intestinal bacterial disease in bats (Mühldorfer et al., 2011a,b). For example, E. coli was identified as the causative agent of ascending urinary tract infection in two individual bats of the family Vespertilionidae (Mühldorfer et al., 2011b). Additionally, apparently virulent non-sorbitol fermenting and/or haemolytic E. coli strains have been isolated from the gastrointestinal tract of bat species in Trinidad (Adesiyun et al., 2009) and Brazil (Moreno et al., 1975).

Arthropod-Borne Bacterial Pathogens

  1. Top of page
  2. Summary
  3. Impacts
  4. Introduction
  5. Enteric Pathogens
  6. Arthropod-Borne Bacterial Pathogens
  7. Bacteria of the Genus Leptospira
  8. Pasteurella Infections in Bats
  9. Bacteria with Antibiotic Resistance
  10. Implications on Bats as Carriers of Pathogenic Bacteria
  11. Conclusions
  12. Acknowledgements
  13. References

Several Borrelia and Bartonella species and the causative agent of Potomac horse fever disease Neorickettsia risticii have been detected in blood and organ tissues of bats (Table 2). The majority of infected animals appear to be healthy, only two vespertilionid bats (Pipistrellus sp. and Natalus tumidirostris) revealed severe borrelial spirochetaemia (Marinkelle and Grose, 1968; Evans et al., 2009). Phylogenetic analyses of Bartonella strains derived from bats identified several distinct phylogroups indicating the presence of a variety of novel Bartonella species in bats (Concannon et al., 2005; Kosoy et al., 2010; Bai et al., 2011; Lin et al., 2012). It is notable that bats of the same species (Kosoy et al., 2010) as well as bats of the same geographic origin and ecological niche (i.e. Desmodus rotundus, members of the family Vespertilionidae) shared closely related strains of Bartonella (Kosoy et al., 2010; Bai et al., 2011; Lin et al., 2012).

Table 2. Arthropod-borne bacteria identified in apparently healthy and diseased bats
Family of batsBacteria na SourceDetection methodLocationReference
  1. aNumber of positive bats/total number of bats sampled.

  2. bOral cavity, anus, perianal area, genitalia.

Vespertilionidae Bartonella spp.6/53BloodCulture, PCRTaiwan Lin et al. (2012)
Bartonella spp.49/87BloodCultureKenya Kosoy et al. (2010)
Bartonella spp.5/60HeartPCRCornwall, UK Concannon et al. (2005)
Borrelia spp.1/1LiverPCRCornwall, UK Evans et al. (2009)
Borrelia spp.3/3SwabsbCultureUSA Hanson (1970)
Grahamella spp.2/111Blood smearsMicroscopyCzech Republic Šebek (1975)
Neorickettsia risticii 23/53Blood, organs, trematodePCRPennsylvania, USA Gibson et al. (2005)
Hipposideridae Bartonella spp.8/12BloodCultureKenya Kosoy et al. (2010)
Mormoopidae Bartonella spp.7/10BloodCultureGuatemala Bai et al. (2011)
Natalidae Borrelia spp.1/512Blood smearsMicroscopyColumbia Marinkelle and Grose (1968)
Emballonuridae Bartonella spp.4/9BloodCultureKenya Kosoy et al. (2010)
Phyllostomidae
 Desmodontinae Bartonella spp.15/31BloodCultureGuatemala Bai et al. (2011)
 Carolliinae Bartonella spp.4/14BloodCultureGuatemala Bai et al. (2011)
 Glossophaginae Bartonella spp.2/152BloodCultureGuatemala Bai et al. (2011)
 Phyllostominae Bartonella spp.9/12BloodCultureGuatemala Bai et al. (2011)
 Stenodermatinae Bartonella spp.2/13BloodCultureGuatemala Bai et al. (2011)
Pteropodidae
 Pteropodinae Bartonella spp.23/88BloodCultureKenya Kosoy et al. (2010)
 Rousettinae Bartonella spp.22/105BloodCultureKenya Kosoy et al. (2010)

Blood-feeding arthropods are important vectors of bacterial pathogens common in humans and animals, picking up the bacteria while feeding on infected hosts (Wales et al., 2010; Fleer et al., 2011). Soft ticks (family Argasidae) and other ectoparasites commonly found on bats or in bat habitats have been found to be infected with Bartonella, Borrelia and Rickettsia species (Loftis et al., 2005; Reeves et al., 2005, 2007; Gill et al., 2008; Schwan et al., 2009; Blott, 2010; Billeter et al., 2012; Hornok et al., 2012), posing a potential risk of intra- and interspecies transmission cycles between bats, humans and domestic animals (D’Auria et al., 2010). Host-switching and variations in host-specificity of ectoparasites are significant factors in arthropod-borne diseases that increase the spread of pathogenic microorganisms (Kampen, 2009). Bats can also carry the bacteria in their bloodstream (Marinkelle and Grose, 1968; Gibson et al., 2005; Kosoy et al., 2010; Bai et al., 2011), which allow them to enter local ectoparasite populations at other roosting sites.

Antibodies reactive for the causative agent of scrub typhus Orienta tsutsugamushi (formerly genus Rickettsia), for a relapsing fever Borrelia species (B. hermsii), and for several Rickettsia species of the spotted fever group (R. conorii, R. rickettsii, R. parkeri, R. amblyommii and R. rhipicephali) have been detected in blood serum samples of bats (range 1.1–12.9%) from Korea, Brazil, and the U.S. state of Georgia (Choi and Lee, 1996; Reeves et al., 2006; D’Auria et al., 2010). Most of these bats belong to the families Vespertilionidae and Molossidae, indicating that insectivorous bats are exposed to human-pathogenic Borrelia, Orienta and Rickettsia species. In addition, a novel spirochete detected in a pipistrelle bat from the United Kingdom was found to be closely related to known human-pathogenic Borrelia species of the relapsing fever group (Evans et al., 2009).

Bacteria of the Genus Leptospira

  1. Top of page
  2. Summary
  3. Impacts
  4. Introduction
  5. Enteric Pathogens
  6. Arthropod-Borne Bacterial Pathogens
  7. Bacteria of the Genus Leptospira
  8. Pasteurella Infections in Bats
  9. Bacteria with Antibiotic Resistance
  10. Implications on Bats as Carriers of Pathogenic Bacteria
  11. Conclusions
  12. Acknowledgements
  13. References

Leptospirosis is a globally re-emerging bacterial disease of importance for humans and animals (Cruz et al., 2009). Members of the genus Leptospira include saprophytic, intermediate and pathogenic strains that are capable of surviving in moist and warm environments (Monahan et al., 2009). The bacteria colonize the renal tubules of their hosts and are excreted via urine into the environment. Thus, transmission of Leptospira to humans and animals usually occurs through contact with urine-contaminated soil or water (Monahan et al., 2009). Rodents are recognized as most important carriers of leptospires (Plank and Dean, 2000); however, a variety of pathogenic Leptospira species have also been identified in bats of diverse feeding habitats (Table 3). The prevalence of leptospiral infections in bats varied from almost 2% to 35% depending on the sample size of the respective study (Fennestad and Borg-Petersen, 1972; Bunnell et al., 2000; Cox et al., 2005; Matthias et al., 2005; Bessa et al., 2010). Species-specific variations in bacterial infection rates may indicate that some species of bats are more exposed or even more susceptible to Leptospira (Fennestad and Borg-Petersen, 1972; Matthias et al., 2005; Bessa et al., 2010). The family Phyllostomidae comprised the majority of microbats infected with Leptospira, whereas in obligate insectivorous species (i.e. families Vespertilionidae and Molossidae) leptospiral infection with pathogenic strains has occasionally been found (Matthias et al., 2005; Bessa et al., 2010). However, a study from Denmark reported high prevalence of Leptospira-like bacteria in three of eight different species of vespertilionid bats (i.e. Myotis daubentonii, Pipistrellus pipistrellus and Nyctalus noctula) that apparently differed in their growth requirements and their pathogenicity from known leptospiral agents (Fennestad and Borg-Petersen, 1972). The bacteria were identified in urine and kidney suspensions of 31 bats by dark-field microscopy, while subsequent efforts to isolate leptospires from these samples were not successful. In addition, intraperitoneal inoculation of laboratory animals (i.e. newborn rodents, rabbits and chicken) as well as of vespertilionid bats resulted only in bats in infection and leptospiruria (Fennestad and Borg-Petersen, 1972). Some bacterial strains identified in bats of the family Phyllostomidae formed separate monophyletic groups and may also represent novel species of the genus Leptospira (Matthias et al., 2005).

Table 3. Leptospira identified in bats
Family of bats na SourceDetection methodLocationReference
  1. aNumber of positive bats/total number of bats sampled.

Vespertilionidae 1/3KidneyCulture, PCRPeru Matthias et al. (2005)
31/166Kidney, urineDark-field microscopyDenmark Fennestad and Borg-Petersen (1972)
Molossidae 1/2KidneyCulture, PCRPeru Matthias et al. (2005)
Phyllostomidae
 Desmodontinae 1/2KidneyCulture, PCRPeru Matthias et al. (2005)
 Carolliinae 3/203KidneyCulture, PCRPeru Matthias et al. (2005)
 2/3KidneyPCRPeru Bunnell et al. (2000)
 Glossophaginae 4/82KidneyPCRBrazil Bessa et al. (2010)
 4/33KidneyCulture, PCRPeru Matthias et al. (2005)
 Phyllostominae 3/69KidneyCulture, PCRPeru Matthias et al. (2005)
 Stenodermatinae 2/43KidneyPCRBrazil Bessa et al. (2010)
 7/274KidneyCulture, PCRPeru Matthias et al. (2005)
 5/17KidneyPCRPeru Bunnell et al. (2000)
Pteropodidae
 Pteropodinae19/173KidneyPCRAustralia Cox et al. (2005)
18/46UrinePCRAustralia Cox et al. (2005)

Habitat preference and geographic origin are factors that could influence the colonization of bats with leptospires. In particular, microbats found in forest habitats revealed higher infection rates of pathogenic Leptospira species than animals collected in areas with increased human activity (Fennestad and Borg-Petersen, 1972; Matthias et al., 2005; Bessa et al., 2010). This suggests that microbats not serve as important vectors of human Leptospira infections (Bessa et al., 2010), but might play a possible role in the maintenance of leptospires in the environment (Everard et al., 1983). In contrast, native flying fox populations (genus Pteropus) in Australia are considered as important carriers of pathogenic Leptospira responsible for infections in humans and other animals because of high bacterial detection rates in kidney (11%) and urine samples (39%) (Cox et al., 2005) as well as high seroprevalences (18%, 28%) (Emanuel et al., 1964; Smythe et al., 2002).

Pasteurella Infections in Bats

  1. Top of page
  2. Summary
  3. Impacts
  4. Introduction
  5. Enteric Pathogens
  6. Arthropod-Borne Bacterial Pathogens
  7. Bacteria of the Genus Leptospira
  8. Pasteurella Infections in Bats
  9. Bacteria with Antibiotic Resistance
  10. Implications on Bats as Carriers of Pathogenic Bacteria
  11. Conclusions
  12. Acknowledgements
  13. References

The genus Pasteurella comprises bacterial pathogens of wide distribution and host range (Boyce et al., 2004). Members of this genus (i.e. P. multocida, P. pneumotropica and Pasteurella species B) have been identified as primary pathogens in bats responsible for a variety of localized and systemic infections in European bat species (Simpson, 2000; Daffner, 2001; Hajkova and Pikula, 2007; Mühldorfer et al., 2011a,b,c). In addition, a novel Pasteurella-like bacterium was found as the causative agent of severe pneumonia and subcutaneous abscesses in captive flying foxes (Helmick et al., 2004).

Several pathogenic Pasteurella species are commensals of the oropharyngeal flora of carnivores; hence, wound infections following bites from domestic cats and dogs play an important role in bacterial transmission (Smit et al., 1980; Ganiere et al., 1993; Talan et al., 1999). Bite wounds also appear to be the most likely source of Pasteurella infections in European bats, as the majority of animals dying of pasteurellosis had traumatic injuries suggestive of cat predation (Routh, 2003; Mühldorfer et al., 2011b,c). Accordingly, bat species roosting in human habitations were primarily affected by pasteurellosis (Routh, 2003; Mühldorfer et al., 2011b). On the basis of the results of genetic characterization, most Pasteurella strains isolated from organ tissues of 29 vespertilionid bats represented P. multocida ssp. septica (85%) and capsular type A (75%) (Mühldorfer et al., 2011c). Such strains have been described as predominant P. multocida in the oral cavity of domestic cats (Kuhnert et al., 2000; Ewers et al., 2006).

Bacteria with Antibiotic Resistance

  1. Top of page
  2. Summary
  3. Impacts
  4. Introduction
  5. Enteric Pathogens
  6. Arthropod-Borne Bacterial Pathogens
  7. Bacteria of the Genus Leptospira
  8. Pasteurella Infections in Bats
  9. Bacteria with Antibiotic Resistance
  10. Implications on Bats as Carriers of Pathogenic Bacteria
  11. Conclusions
  12. Acknowledgements
  13. References

Antimicrobial resistance is of increasing concern in human and veterinary medicine in both pathogenic and opportunistic bacteria. Antimicrobial-resistant bacteria have been reported in the absence of antibiotic therapy, for example, in wild animals (e.g. Mare, 1968; Pagano et al., 1985; Gilliver et al., 1999; Costa et al., 2008; Guenther et al., 2010a,b; Molina-Lopez et al., 2011) and insects (Rahuma et al., 2005). Bacteria resistant to antimicrobial substances are also found in environmental samples (e.g. Pagano et al., 1985; Jones et al., 1986; Kaspar et al., 1990; Shears et al., 1995), where their occurrence is almost certainly linked to the use of antibiotics in humans and livestock. Likewise, bats that inhabit urban and rural ecosystems can acquire microorganisms from insect and environmental sources and might serve as a reservoir of antibiotic-resistant bacteria and genetic determinants. But while many research efforts are focussed on the prevalence of antimicrobial resistance in wildlife, information on bats is limited. Souza et al. (1999) analysed 202 E. coli strains obtained from 81 mammalian species of different continents and found 41% of the Mexican strains resistant against at least one antimicrobial agent. Among these, E. coli (n = 11) isolated from bats of both urban and wilderness areas (i.e. insectivores, sanguivores and nectarivores) tended to have a much higher prevalence of antibiotic resistance (i.e. neomycin 15%, ampicillin 46% and streptomycin 100%) than bacterial strains obtained from other mammalian species (Souza et al., 1999). Another study on enteropathogens in bats from Trinidad found increased prevalence of antimicrobial resistance in E. coli against streptomycin (26.5%) and tetracycline (16.3%) with 8% of bacterial strains resistant to both antimicrobial agents (Adesiyun et al., 2009). In contrast to these results, the prevalence of resistant E. coli strains in wild mammals from Australia was generally low (9.6%, range 0.2–3.1%), with the exception of spectinomycin (55.2%) (Souza et al., 1999; Sherley et al., 2000). However, Sherley et al. (2000) found location and host-dependent resistance profiles in Australian bacterial strains indicating that Enterobacteriaceae isolated from bats (family Vespertilionidae), potoroos (family Potoridae) and rodents (family Muridae) shared similar patterns of antimicrobial resistance. Finally, during routine microbiological examination, a methicillin-resistant Staphylococcus aureus (MRSA) was isolated from an infected wound of a bat in Germany (Walther et al., 2008).

Implications on Bats as Carriers of Pathogenic Bacteria

  1. Top of page
  2. Summary
  3. Impacts
  4. Introduction
  5. Enteric Pathogens
  6. Arthropod-Borne Bacterial Pathogens
  7. Bacteria of the Genus Leptospira
  8. Pasteurella Infections in Bats
  9. Bacteria with Antibiotic Resistance
  10. Implications on Bats as Carriers of Pathogenic Bacteria
  11. Conclusions
  12. Acknowledgements
  13. References

A wide variety of intrinsic (e.g. sex, age, reproductive status, social status and body condition) and extrinsic factors (i.e. environmental and anthropogenic stressors) can influence the immune competence and disease susceptibility of a wildlife host or can even increase the exposure and transmission rate of microbial pathogens (Hawley and Altizer, 2011; Hofer and East, 2012). The majority of data on infection dynamics in bats originate from virology or parasitology studies. Certain features of bats that may contribute to the viral richness encountered in these animals (Calisher et al., 2006; Kuzmin et al., 2011; Wang et al., 2011) can also facilitate bacterial infection. It is beyond the limit of this article to discuss these aspects in detail, but few examples should be mentioned here.

Of particular importance is the aggregation behaviour of bats within their roosts, as this dense clustering enhances the potential for bacterial transmission between individuals via direct bat-to-bat contact. Other behavioural characteristics, such as frequent intra- and inter-roost movements and long distance migrations, can increase transmission between bat species and different colonies and with this the exchange of bacterial pathogens within different bat populations (Smythe et al., 2002; D’Auria et al., 2010).

Many bat species hibernate to sustain winter. Like in other mammals, it is assumed that the reduced metabolic rate of bats under hibernation may suppress their immune responses to microbial infection (Bouma et al., 2010). Psychrophilic bacteria, such as enteropathogenic Yersinia, can still grow at lowered body temperatures (Morita, 1975; Luis and Hudson, 2006) and may provoke systemic disease in bats during hibernation arousal cycles (Mühldorfer et al., 2010, 2011a).

The feeding ecology of bats appears to be another key determinant of both bacterial acquisition and transmission, because it provides ample opportunities for bats to share infectious agents with other hosts (Wong et al., 2007; Kuzmin et al., 2011). Bats have a remarkable range of dietary habits and some species cover long distances between their roosting and foraging sites. In their search for food, several species of bats come into close contact with humans and other animals (Wong et al., 2007; Kuzmin et al., 2011). Additionally, predatory species (i.e. insectivores, carnivores or sangivores) can possibly acquire infectious agents from their prey (Wong et al., 2007; Johnson et al., 2010). Several insects have been found to harbour harmful bacteria common in human and animal diseases, including Salmonella, Yersinia or Campylobacter species (Rahuma et al., 2005; Vallet-Gely et al., 2008; Wales et al., 2010). Therefore, it seems likely that prey insects may act as passive vectors of enteric pathogens found in insect-eating bats (Adesiyun et al., 2009; Hazeleger et al., 2010; Mühldorfer et al., 2010; Reyes et al., 2011). Similarly, contaminated fruits (Kuzmin et al., 2011) or water (Mühldorfer et al., 2010; Reyes et al., 2011) might also be possible sources of bacteria identified in bats.

As mentioned, there are more characteristics of bats to consider while such data are sparse and almost limited to virus–host interactions only. Because viral transmission differs from bacterial transmission in several ways, this review is aimed to stimulate research in this area.

Conclusions

  1. Top of page
  2. Summary
  3. Impacts
  4. Introduction
  5. Enteric Pathogens
  6. Arthropod-Borne Bacterial Pathogens
  7. Bacteria of the Genus Leptospira
  8. Pasteurella Infections in Bats
  9. Bacteria with Antibiotic Resistance
  10. Implications on Bats as Carriers of Pathogenic Bacteria
  11. Conclusions
  12. Acknowledgements
  13. References

With regard to the emergence of novel infectious diseases in wildlife, it is of public and scientific interest to determine whether bats act as carriers of pathogenic bacteria or whether they are affected by bacterial diseases that could also be relevant for conservation issues. The present review shows that bats are vulnerable to several infectious agents common in bacterial diseases of humans and domestic animals like enteric (e.g. Salmonella, Shigella, Yersinia and Campylobacter spp.) and arthropod-borne bacterial pathogens (Bartonella, Borrelia spp. and members of the family Rickettsiales) and pathogenic Leptospira species. Some of these bacterial agents are also associated with pathological lesions and systemic disease in bats themselves. The review further indicates that bats carry different bacteria of unknown pathogenic importance. The utilization and continuous development of molecular investigation methods, rather than traditional cultural methods, will prove invaluable for studying the complexity of the microflora of bats as well as for the detection of novel bacterial pathogens.

As bats can acquire various infectious agents through their diet and from environmental sources in human and livestock habitats, the awareness of possible bacterial transmission routes in different species of bats could serve as model for other infectious organisms like zoonotic pathogens.

Acknowledgements

  1. Top of page
  2. Summary
  3. Impacts
  4. Introduction
  5. Enteric Pathogens
  6. Arthropod-Borne Bacterial Pathogens
  7. Bacteria of the Genus Leptospira
  8. Pasteurella Infections in Bats
  9. Bacteria with Antibiotic Resistance
  10. Implications on Bats as Carriers of Pathogenic Bacteria
  11. Conclusions
  12. Acknowledgements
  13. References

I am grateful to G. Wibbelt for her dedicated help in manuscript editing. I also thank G. Wibbelt and S. Speck for all their work on bat diseases; as well as G.-A. Czirják, M. Grobbel and two anonymous reviewers for helpful suggestions and comments on earlier drafts of this review. Work from my own laboratory that is cited in this review was supported by the Adolf and Hildegard Isler-Stiftung, the FAZIT-Stiftung and the Klara Samariter-Stiftung.

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  2. Summary
  3. Impacts
  4. Introduction
  5. Enteric Pathogens
  6. Arthropod-Borne Bacterial Pathogens
  7. Bacteria of the Genus Leptospira
  8. Pasteurella Infections in Bats
  9. Bacteria with Antibiotic Resistance
  10. Implications on Bats as Carriers of Pathogenic Bacteria
  11. Conclusions
  12. Acknowledgements
  13. References
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