Bartonella Infections in Rodents and Bats in Tropics (Tropical Diseases Due to Bacteria and Viruses) Part 2

Bartonella infections in bats in tropics

Like rodents, bats (Order: Chiroptera) are another group of very abundant, diverse, and geographically dispersed vertebrates on the earth (Simmons, 2005; Calisher et al., 2006). Multiple studies have highlighted that bats may play an important role in serving as natural reservoirs to a variety of pathogens (Schneider et al., 2009). Transmission of pathogenic batborne viruses capable of causing disease with high human mortality has been demonstrated for a number of viruses, including rabies virus and related lyssaviruses, Nipah and Hendra viruses, Marburg virus, Ebola viruses, and the very recently emerged inferred for SARS-CoV-like virus and other coronaviruses and others (Halpin et al., 2000; Li et al., 2005; Williams, 2005; Tang et al., 2006). The high mobility, broad distribution, social behavior (communal roosting, fission-fusion social structure) and longevity of bats make them ideal reservoir hosts and sources of infection for various etiologic agents.

There is very limited information regarding Bartonella infections in bats. In England, detection of Bartonella DNA in bats was reported recently (Concannon et al., 2005). A few studies from Egypt and United States reported presence of Bartonella species in ectoparasites collected from bats (Loftis et al., 2005; Reeves et al., 2005, 2006, & 2007).

From tropic areas, two studies of bartonella infections in bats were conducted in Kenya and Guatemala very recently (Kosoy et al., 2010; Bai et al., 2011). These studies brought large information regarding distribution of bartonellae in bats. Here we present the findings from these two studies. We compare the composition of bat communities, prevalence of bartonella infections in bat populations, genetic diversity of Bartonella strains circulating among the bat populations. We also discuss the epidemiological significance of these findings.

Bat community

Belonging to 28 species, bats collected from these two studies showed large diversity. Species composition was completely different in the two studies. Bats collected from Kenya represented 13 species of 9 genera (Table 2), including Chaerephon sp., Coleura afra, Eidolon helvum, Epomophorus spp., Hipposideros commersoni, Miniopterus spp., Rhinolophus spp., Rousettus aegyptiacus, and Triaenops persicus. Accounted for 32% of all bats, Rousettus aegyptiacus was the most prevalent species in Kenya. The other common species included Eidolon helvum (27%) and Miniopterus spp. (26). Other species only accounted for a very small portion (Table 2).

Table 2. Bartonella in bats, Kenya

Bats collected from Guatemala represented 15 species of 10 genera (Table 3), including Artibeus jamaicensis, Artibeus lituratus, Artibeus toltecus, Carollia castanea, Carollia perspicillata, Desmodus rotundus, Glossophaga soricina, Micronycteris microtis, Myotis elegans, Myotis nigricans, Phyllostomus discolor, Platyrrhinus helleri, Pteronotus davyi, Sturnira lilium, and Sturnira ludovici. Desmodus rotundus comprised 26% of all bats and was the most prevalent species. Glossophaga soricina, Carollia perspicillata, Artibeus jamaicensis, and Sturnira lilium comprised 13%, 12%, 11%, and 10%, respectively, also were frequently found. The other six species comprised a smaller portion (Table 3).

Bartonella prevalence in bats

Although composition of bat species was completely different in the Kenya and Guatemala, interestingly, the overall prevalence of bartonella infection in bats was quite similar: 32% in Kenya and 33% in Guatemala. Such high prevalence may suggest persistent infection of long-lived bats with Bartonella species, similar to their infection with some viruses (Sulkin & Allen, 1974). Nevertheless, large variations of bartonella prevalence were observed among the bat specie. Bartonella species exhibit high, low, or no infectivity depending on the bat species. In Kenya, the bartonella prevalence was 88%, 56%, 44%, 26%, 25%, and 21% for Triaenops persicus bats, Miniopterus spp. bats, Coleura afra bats, Eidolon helvum bats, Hipposideros commersoni bats, and Rousettus aegyptiacus bats, respectively. In Guatemala, Phyllostomus discolor bats, Pteronotus davyi bats, and Desmodus rotundus bats were highly infected with Bartonella species, with prevalence of 89%, 70%, and 48% in each, respectively. Bartonella prevalence was relatively low in Sturnira lilium bats (8%) and Glossophaga sericina bats (13%), and no bartonellae were discovered in some bat species, such as Epomophorus spp., Rhinolophus spp., and Artibeus jamaicensis (Table 2 & Table 3).

Bartonella genetic heterogeneity and relationships with bat species

Genetic analyses of a portion of citrate synthase gene (gltA) demonstrated that the Bartonella strains obtained from bats in both Kenya and Guatemala represent a variety of distinct phylogroups, including 11 from Kenya and 13 from Guatemala. Further characterization is necessary to verify whether the Bartonella strains represent novel Bartonella species. In Kenya, a definite host-specificity was observed for Bartonella strains in bat species. All Bartonella isolates obtained from Rousettus aegyptiacus bats are similar to each other (>96%) and clustered in a monophyletic genogroup that is distant from all other Bartonella species; similarly, Bartonella cultures obtained from Coleura afra bats, Triaenops persicus bats also clearly belonged to the specific Bartonella species group found exclusively in the particular bat species. By contrast, Bartonella cultures obtained from Eidolon helvum bats and Miniopterus bats showed great variation, clustering into three or four clades, each representing a distinct Bartonella phylogroup. Nevertheless, all strains of Bartonella species recovered from Eidolon helvum bats were typical for this species of bats only. Similarly, the gltA sequences from all strains obtained from Miniopterus spp. bats have not been found in bats of other bat genera.

Unlike the discovery in bats in Kenya, host specificity of Bartonella species was not found in bats in Guatemala. In some instances, bats of two or more species may share the same Bartonella strains. For example, one Bartonella strain recovered in Desmodus rotundus bats was also found in Carollia perspicillata bats. Similarly, same Bartonella strain was found in both Glossophaga soricina bats and Pteronotus davyi bats, or both Carollia perspicillata bats and Phyllostomus discolor bats. On the other hand, co-infection with multiple Bartonella strains in the same bat species was observed. For example, Desmodus rotundus bats and Carollia perspicillata bats each were infected with two Bartonella strains; while Pteronotus davyi bats and Phyllostomus discolor bats were infected with four Bartonella strains, respectively. The tendency of some bat species to share roosts, reach large population densities, and roost crowded together creates the potential for dynamic intraspecies and interspecies transmission of infections (Streicker et al., 2010). The observations in the Guatemala study suggested active interspecies transmission of Bartonella species likely occurs among bats in Guatemala, which may have contributed to the lack of host-specificity. Arthropod vectors that parasitize bats may also be partly associated with none host-specificity.

Table 3. Bartonella in bats, Guatemala

Epidemiology significance

Bartonellae were virtually unrecognized as pathogens of humans until 1990s. Identifications of bartonellae as agents of cat-scratch disease, bacillary angiomatosis, urban trench fever, and recent outbreaks of Carrión’s disease have left no doubt about the emerging medical importance of these bacteria. Within the last two decades, new bacteria of the genus of Bartonella were isolated from large number of several mammalian reservoirs, including rodents, cats, dogs, and rabbits, and recognized as emerging zoonotic agents. At least 13 Bartonella species or subspecies have been recognized as emerging human pathogens or zoonotic agents, causing a wide range of syndromes, from a self-limiting to life-threaten endocarditis, myocarditis, and meningoencephalitis. All of these emphasize the concept that inadvertent transmission of known or currently uncharacterized Bartonella spp. from both wild animals and domestic animals occurs in nature.

Although evidence of overt disease in bats caused by Bartonella species has not been demonstrated to date, high incidence of bartonella infection in bats from the studies carried out in Guatemala, Kenya, and other regions suggested that bats may be natural reservoirs in maintaining circulation of Bartonella species in nature. Bats have very long life spans compared to other mammals of similar body size, such as rodents. This may make them serve as reservoirs contributing to the maintenance and transmission of Bartonella to other animals and/or humans. Some bat species have been known to directly transmit infections to humans. For example, the common vampire bat (Desmodus rotundus) has been long recognized to transmit rabies virus to humans by biting throughout Latin America (Schneider et al., 2009). These bats typically feed on the blood of mammals, including domestic animals, such as cattle, horses, pigs, dogs, but also feed on the blood of humans (Turner & Bateson, 1975). Predation of vampire bats on humans is a major problem in Latin America (Schneider et al., 2009). If Bartonella species can be transmitted to humans through the bite of bats, the need for further studies with vampire bats is imperative. Findings of bartonella in bats highlight the need to study whether the bat-originated Bartonella species are responsible for the etiology of local undiagnosed illnesses in humans and domestic animals in tropics.

In addition to the large number of documented reservoir hosts, an increasing number of arthropos vectors, includingbiting flies, fleas, keds, lice, sandflies, and ticks have been confirmed or suspected to be associated with the transmission of Barotellla spp. among animal populations (Billeter et al., 2008). Bartonella species-specific DNA has been detected in ectoparasites collected from bats (Loftis et al., 2005; Reeves et al., 2005 & 2007). Presumably, if Bartonella species are transmitted through a bat ectoparasite vector, some, if not all, bat-associated Bartonella species could be transmitted to humans because bats are frequent hosts to a wide variety of ectoparasites, including bat flies, fleas, soft ticks, and mites. Very recently, two novel Bartonella species, B. tamiae, isolated from febrile Thai patients (Kosoy et al., in press), and B. rochalimae, isolated from an American patient who traveled in Peru and developed fever and splenomegaly after return (Eremeeva et al., 2007). However, the reservoir remains unknown as do the mode of transmission, pathogenesis, and many other characteristics of these organisms. There is the need to identify the animal reservoirs of these novel Bartonella species and to understand their disease ecology. These studies of Bartonella species in bats have enlarged the scope of this zoonotic potential as we search for the reservoirs that harbor novel and known Bartonella species.