Bats and human.pdf

SPECIAL ISSUE – BATS
Bats and Bacterial Pathogens: A Review
K. Mühldorfer
Research Group of Wildlife Diseases, Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany
Impacts
• 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
The order Chiroptera is the most diverse and geographi-
cally distributed mammalian taxon found on all conti-
nents 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 char-
acteristics together with their long lifespan and their abil-
ity 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 patho-
gens (Calisher et al., 2006; Wong et al., 2007; Kuzmin
et al., 2011; Wang et al., 2011). Their role in disease epi-
demiology 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
Keywords:
Chiroptera; infectious agents; enteric bacteria;
Salmonella; Yersinia; Pasteurella; Leptospira;
arthropod-borne; antimicrobial resistance;
wildlife; zoonosis
Correspondence:
K. Mühldorfer. Research Group of Wildlife
Diseases, Leibniz Institute for Zoo and Wildlife
Research, Alfred-Kowalke-Str. 17, 10315
Berlin, Germany. Tel.: +49 30 5168246;
Fax: +49 30 5126104;
E-mail: muehldorfer@izw-berlin.de
Received for publication January 24, 2012
doi: 10.1111/j.1863-2378.2012.01536.x
Summary
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 pre-
dominantly focused on viral agents, the prevalence of pathogenic bacteria in
bats and their impact on bat mortality have largely neglected. Enteric patho-
gens 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 ecologi-
cal context or even transmission cycles involving bats, humans and other ani-
mals 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 fac-
tors 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.
Zoonoses and Public Health
ª 2012 Blackwell Verlag GmbH 93
Zoonoses and Public Health, 2013, 60, 93–103

microflora of bats is sparse. Because of limitations in
sample collection and preservation, bacteriological investi-
gations 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 ectopara-
site 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 particu-
lar emphasis on main bacterial pathogens, which have the
potential to cause disease in bats and humans. In addi-
tion, 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
The majority of information regarding the normal gastro-
intestinal bacterial flora of bats and the presence or
absence of bacterial enteropathogens comes from tradi-
tional 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).
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 indus-
trial 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-path-
ogenic 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 intersti-
tial 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 iso-
lated 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 Shi-
gella: 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; Ró_
zalska et al.,
1998). Together with S. sonnei, it accounts for the major-
ity of human shigellosis cases worldwide (Edwards, 1999;
Weir, 2002).
The wide distribution and host range of enteropatho-
genic Yersinia species, Y. enterocolitica and Y. pseudotuber-
culosis, and the potential zoonotic risk of human health
make yersiniosis a significant bacterial disease. Both bac-
terial 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). How-
ever, the occurrence of enteropathogenic Yersinia species
and their impact on bats are largely unknown. A study
reported high prevalence of different Yersinia species
Bats and Bacterial Pathogens K. Mühldorfer
94 ª 2012 Blackwell Verlag GmbH

(35%) in the faeces of 70 insectivorous Myotis myotis
collected from natural populations in Poland (Ró_
zalska
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. pseudotu-
berculosis 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. pseudotu-
berculosis infection have occasionally been observed in
closed colonies of captive flying foxes (Williams, 2004;
Child-Sanford et al., 2009), which supports the patho-
genic potential of Y. pseudotuberculosis strains for bats.
Few studies on bacterial pathogens in chiropteran spe-
cies investigated the presence of Campylobacter but pre-
dominantly 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
Table 1. Enteropathogenic bacteria isolated from apparently healthy and diseased bats
Family of bats Bacteria na
Source Location Reference
Vespertilionidae Campylobacter jejuni 17/634 Faeces the Netherlands Hazeleger et al. (2010)
Clostridium perfringens 11/76 Faeces Czech Republic Hajkova and Pikula (2007)
Clostridium sordellii 1/486 Intestine Germany Mühldorfer et al. (2011a)
Listeria spp. 1/149 Rectal swabs Poland Ró_
zalska et al. (1998)
Salmonella spp. 2/46 Intestine Philippines Reyes et al. (2011)
Salmonella group Db
1/73 Heart blood UK Daffner (2001)
Salmonella Enteritidisb
, Salmonella
Typhimuriumb
3/486 Organ samples Germany Mühldorfer et al. (2011a)
Shigella flexneri 5/149 Rectal swabs Poland Ró_
Vibrio spp. 1/486 Organ samples Germany Mühldorfer et al. (2011a)
Yersinia enterocolitica, Yersinia spp. 31/149 Rectal swabs Poland Ró_
Yersinia enterocolitica,
Y. pseudotuberculosis
2/486 Organ samples Germany Mühldorfer et al. (2010)
Molossidae Clostridium spp. 3/20 Intestine – Klite (1965a)
Listeria monocytogenes 2/234 Intestine Togo Höhne et al. (1975)
Salmonella Caracasb
, Salmonella group I 2/37 Gastrointestinal tract Trinidad Adesiyun et al. (2009)
Salmonella Anatumb
, S. Blockleyb
2/184 Intestinal/rectal swabs Colombia Arata et al. (1968)
Salmonella Enteritidisb
, Salmonella O48b
10/88 Faeces Madagascar Cassel-Béraud and
Richard (1988)
Shigella boydii-2 1/184 Intestinal/rectal swabs Colombia Arata et al. (1968)
Mormoopidae Clostridium spp. 5/20 Intestine – Klite (1965a)
Phyllostomidae
Desmodontinae Salmonella Typhimuriumb
9/100 Faeces Brazil Moreno et al. (1975)
Shigella sonnei 1/113 Faeces Brazil de Souza et al. (2002)
Carolliinae Clostridium spp. 9/20 Intestine – Klite (1965a)
Glossophaginae Salmonella Saintpaulb
, S. Typhimurium
var. Copenhagenb
1/6 Faeces Panama Klite (1965b)
Stenodermatinae Salmonella Llandoffb
, S. Sandiegob
2/967 Intestinal/rectal swabs Colombia Arata et al. (1968)
Pteropodidae
Epomophorinae Listeria monocytogenes 1/2 Intestine Togo Höhne et al. (1975)
Pteropodinae Salmonella Typhib
, Salmonella
Typhimuriumb
58/481 Heart blood,
organ samples
Madagascar Brygoo et al. (1971)
S. flexneri, S. sonnei 17/481 Intestine, bile Madagascar Brygoo et al. (1971)
Nectarivorous Salmonella sp. 1/47 Faeces Brazil de Souza et al. (2002)
Noctilionidae Salmonella Moladeb
, Salmonella
Rubislawb
1/11 Gastrointestinal tract Trinidad Adesiyun et al. (2009)
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.
a
Number of positive bats/total number of bats sampled.
b
Salmonella isolates named by the respective serotype of Salmonella enterica ssp. enterica.
K. Mühldorfer Bats and Bacterial Pathogens

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 entero-
pathogens seems to be influenced by their feeding habi-
tats, with the majority of insectivores and granivores
rarely tested positive for Campylobacter species (Wald-
enström et al., 2002). However, insectivorous bats could
acquire bacteria from livestock environments (Rosef et al.,
1983; Wales et al., 2010), which might explain the pres-
ence 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 trauma-
tized 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 bac-
teria 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 Vespertili-
onidae (Mühldorfer et al., 2011b). Additionally, appar-
ently 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
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 spirocheta-
emia (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.,
Table 2. Arthropod-borne bacteria identified in apparently healthy and diseased bats
Family of bats Bacteria na
Source Detection method Location Reference
Vespertilionidae Bartonella spp. 6/53 Blood Culture, PCR Taiwan Lin et al. (2012)
Bartonella spp. 49/87 Blood Culture Kenya Kosoy et al. (2010)
Bartonella spp. 5/60 Heart PCR Cornwall, UK Concannon et al. (2005)
Borrelia spp. 1/1 Liver PCR Cornwall, UK Evans et al. (2009)
Borrelia spp. 3/3 Swabsb
Culture USA Hanson (1970)
Grahamella spp. 2/111 Blood smears Microscopy Czech Republic Šebek (1975)
Neorickettsia risticii 23/53 Blood, organs,
trematode
PCR Pennsylvania, USA Gibson et al. (2005)
Hipposideridae Bartonella spp. 8/12 Blood Culture Kenya Kosoy et al. (2010)
Mormoopidae Bartonella spp. 7/10 Blood Culture Guatemala Bai et al. (2011)
Natalidae Borrelia spp. 1/512 Blood smears Microscopy Columbia Marinkelle and Grose (1968)
Emballonuridae Bartonella spp. 4/9 Blood Culture Kenya Kosoy et al. (2010)
Phyllostomidae
Desmodontinae Bartonella spp. 15/31 Blood Culture Guatemala Bai et al. (2011)
Carolliinae Bartonella spp. 4/14 Blood Culture Guatemala Bai et al. (2011)
Glossophaginae Bartonella spp. 2/152 Blood Culture Guatemala Bai et al. (2011)
Phyllostominae Bartonella spp. 9/12 Blood Culture Guatemala Bai et al. (2011)
Stenodermatinae Bartonella spp. 2/13 Blood Culture Guatemala Bai et al. (2011)
Pteropodidae
Pteropodinae Bartonella spp. 23/88 Blood Culture Kenya Kosoy et al. (2010)
Rousettinae Bartonella spp. 22/105 Blood Culture Kenya Kosoy et al. (2010)
a
b
Oral cavity, anus, perianal area, genitalia.

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).
Blood-feeding arthropods are important vectors of bac-
terial 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 Argasi-
dae) and other ectoparasites commonly found on bats or
in bat habitats have been found to be infected with Barto-
nella, 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 varia-
tions 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
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 environ-
ment. Thus, transmission of Leptospira to humans and
animals usually occurs through contact with urine-con-
taminated 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 lep-
tospiral 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
Table 3. Leptospira identified in bats
Family of bats na
Source Detection method Location Reference
Vespertilionidae 1/3 Kidney Culture, PCR Peru Matthias et al. (2005)
31/166 Kidney, urine Dark-field microscopy Denmark Fennestad and Borg-
Petersen (1972)
Molossidae 1/2 Kidney Culture, PCR Peru Matthias et al. (2005)
Phyllostomidae
Desmodontinae 1/2 Kidney Culture, PCR Peru Matthias et al. (2005)
Carolliinae 3/203 Kidney Culture, PCR Peru Matthias et al. (2005)
2/3 Kidney PCR Peru Bunnell et al. (2000)
Glossophaginae 4/82 Kidney PCR Brazil Bessa et al. (2010)
4/33 Kidney Culture, PCR Peru Matthias et al. (2005)
Phyllostominae 3/69 Kidney Culture, PCR Peru Matthias et al. (2005)
Stenodermatinae 2/43 Kidney PCR Brazil Bessa et al. (2010)
7/274 Kidney Culture, PCR Peru Matthias et al. (2005)
5/17 Kidney PCR Peru Bunnell et al. (2000)
Pteropodidae
Pteropodinae 19/173 Kidney PCR Australia Cox et al. (2005)
18/46 Urine PCR Australia Cox et al. (2005)
a

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 Phyllos-
tomidae formed separate monophyletic groups and may
also represent novel species of the genus Leptospira
(Matthias et al., 2005).
Habitat preference and geographic origin are factors
that could influence the colonization of bats with lepto-
spires. 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 fly-
ing fox populations (genus Pteropus) in Australia are con-
sidered 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
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. pneumotropic-
a and Pasteurella species B) have been identified as pri-
mary 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 Pasteu-
rella-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 sug-
gestive of cat predation (Routh, 2003; Mühldorfer et al.,
2011b,c). Accordingly, bat species roosting in human hab-
itations 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 repre-
sented 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
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; Guen-
ther 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 cer-
tainly linked to the use of antibiotics in humans and live-
stock. 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 preva-
lence 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 resis-
tant 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). How-
ever, Sherley et al. (2000) found location and host-depen-
dent 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 microbio-
logical 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
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 encoun-
tered 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 behaviour-
al 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 die-
tary 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 pas-
sive 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
With regard to the emergence of novel infectious diseases
in wildlife, it is of public and scientific interest to deter-
mine 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 mem-
bers 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
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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