Human Exposure to Novel Bartonella Species From Contact With Fruit Bats

Ying Bai; Modupe O.V. Osinubi; Lynn Osikowicz; Clifton McKee; Neil M. Vora; Maria Rosales Rizzo; Sergio Recuenco; Lora Davis; Mike Niezgoda; Ajoke M. Ehimiyein; Grace S.N. Kia; Akin Oyemakinde; Olufunmilayo Sanni Adeniyi; Yemi H. Gbadegesin; Olugbon A. Saliman; Abiodun Ogunniyi; Albert B. Ogunkoya; Michael Y. Kosoy; Idanre Bat Festival Investigation Team

Disclosures

Emerging Infectious Diseases. 2018;24(12):2317-2323. 

In This Article

Discussion

We made several observations during this investigation. First, Egyptian fruit bats carry a unique Bartonella strain that probably represents a new species, for which we propose the name Bartonella rousetti. Second, bat flies, the common ectoparasites of bats, carry this same strain of Bartonella. Because this organism was detected by PCR only, the presence of the DNA does not necessarily indicate that the organism is viable. Last, persons from the communities surrounding the bat caves were exposed to this particular Bartonella strain, which might cause human infection.

Since 2010, several reports have described finding diverse Bartonella genotypes in bats of many species.[25,27–30] The relationships between Bartonella genotypes and bat species that harbored these bacteria are not always simple. The same Bartonella species may circulate among different bat species, showing no specific relationship between the bats and the Bartonella species.[27] Sometimes, multiple Bartonella species are associated with bats of only 1 species. For example, 6 Bartonella species have been identified in straw-colored fruit bats (Eidolon helvum) in Africa.[16,29] Our study indicates that Egyptian fruit bats carry a specific Bartonella strain that has not been identified in bats of other species.

Similarly, we found that the most prevalent Bartonella species found in bat flies parasitizing Egyptian fruit bats is B. rousetti. The ectoparasite bat flies E. africana are predominantly associated with Egyptian fruit bats.[17,31,32] Although sequences matching other Bartonella species were identified in the bat flies, these genogroups may be primarily associated with arthropods and not mammals. One sequence from a bat fly was identified as B. tamiae. The presence of B. tamiae in bat flies from Algeria has been recorded,[33] and the bacterium reportedly has been identified in chigger mites collected from rodents in Thailand.[34] It is possible that Bartonella species found only in arthropods and not their associated mammal hosts may represent facultative symbionts that are uniquely adapted to live in the arthropod gut or other body system.[35,36] The risks posed to humans by these primarily arthropod-associated Bartonella species are still unclear, although B. tamiae is a reported human pathogen that may cause febrile illness and other clinical signs and symptoms.[37]

Detection of antibodies against B. rousetti in serum samples from several study participants indicates their exposure to the bacteria. However, with serologic results, cross-reactivity is a concern. For example, phylogenetically closely related B. henselae and B. quintana (the causative agents of cat-scratch disease and trench fever, respectively) exhibit a high level of serologic cross-reactivity.[26,38,39] We tested the positive human serum samples for 3 other Bartonella species (B. henselae, B. quintana, and B. elizabethae) that circulate in Africa, and we did not detect any positive results. Given that immunofluorescence assays have good discriminatory ability for a wide range of antigens,[40–42] the results lead us to conclude that the antibodies in these participants were indeed reactive with B. rousetti but not the other Bartonella species tested, although cross-reactivity with other non-Bartonella agents cannot be ruled out.

Our study is not the first attempt to identify antibodies against bat-associated Bartonella in humans. Mannerings et al.[43] conducted a serologic survey of 335 volunteers from Ghana for antibodies against 6 species of Bartonella, including Bartonella strains isolated from straw-colored fruit bats. In that study, only 2 serum samples were positive for B. henselae antibodies at low titers, whereas none was positive against the bat strains.

All known species of Bartonella are transmitted between natural animal hosts by arthropods.[29,44] The presence of B. rousetti DNA in E. africana bat flies parasitizing Egyptian fruit bats suggests that these ectoparasites may act as vectors for the transmission of Bartonella infection among bats, but it is unclear how bat flies would play a role in transmitting the bacterium to humans because bat flies do not commonly bite humans (C. McKee, unpub. data). Instead, human exposure may potentially occur via other routes, such as 1) directly by bat bites or scratches, which is similar to how humans acquire infections with B. henselae through cat scratches;[10,45] 2) indirectly by contamination of open wounds with blood or other materials (e.g., saliva, urine, feces) of infected bats; or 3) indirectly by contamination of open wounds with bat fly excreta. Several studies have reported detecting Bartonella DNA in bat feces,[12,46,47] and Dietrich et al.[47] detected Bartonella DNA in bat saliva and urine, providing support for routes 1 and 2 above, although no attempts have been made to culture viable bacteria from these fluids. However, viable Bartonella bacteria have been cultured from experimentally infected ectoparasites, including fleas and bedbugs,[48,49] although such studies have yet to be performed for bat flies. Nevertheless, evidence is accumulating that Bartonella could spread from infected mammalian hosts through multiple routes. Therefore, it may not be necessary for humans to interact directly with live bats to be exposed to bat-associated Bartonella. Persons might be at risk when interacting with bat carcasses, guano, or other contaminated products. Of note, we do not provide definitive evidence of the route of exposure for any of the 8 seropositive participants. Indeed, 3 of these participants reported no interactions at all with bats.

Future studies should continue to evaluate the relative correlations of exposure routes, the pathobiology of batborne B. rousetti in humans, and vector competency of bat flies for transmitting Bartonella. Results should provide guidance to communities for mitigating the risks to humans interacting with animals and their arthropod vectors.

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