One Health is an initiative aiming to bring together human, animal, and environmental health and plays a significant role in zoonosis prevention and control . The increasingly close health relationship between humans and their domestic animals, especially cats, is conspicuous. According to the Brazilian Association of Pet Products Industry, the cat population has shown an accelerated annual growth in Brazil. Based on these facts, zoonosis studies have become ever more important. From a public health perspective, cats are a major reservoir host for at least three zoonotic Bartonella species (B. henselae, B. clarridgeiae, and B. koehlerae) and they are commonly infested by C. felis fleas, which also represent the great majority of fleas observed in peoples’ homes . To the best of our knowledge, this is the first study in Brazil to investigate Bartonella DNA in shelter cats and their ectoparasites.
The overall prevalence of Bartonella DNA was 47.5% in cat blood, 18.3% in fleas, 13.3% in flea egg pools, and 12.5% in lice pools. The occurrence of Bartonella DNA was higher than previously reported, especially in shelter cats [19–25]. However, a previous study reported 97.3% positivity in one shelter in Rio de Janeiro, Brazil . Risk factors which appear to influence the occurrence of bacteremia in cats includes age, flea infestation status, neutering status, historic of fights, outdoor access and multiple cat households [25, 27–29]. Flea infestation status is particularly important as all cats in this study had ectoparasites on their body surface. Bartonella DNA detected in C. felis fleas varies worldwide, with prevalence ranging from 7.3–75.6% [10, 20, 30–32]. Bartonella DNA was not detected in R. sanguineus ticks or F. subrostratus lice collected from shelter cats in Taiwan .
This study confirmed Bartonella henselae, Bartonella clarridgeiae, and Bartonella koehlerae single infection as well as coinfection by B. henselae and B. clarridgeiae in feline blood samples. Occurrence of concurrent infection by two or more Bartonella species are uncommon in the literature, being documented in low percentages of cats or being absent [5, 31, 33]. The Bartonella species encountered in the present study in cat fleas (B. henselae and B. clarridgeiae) have also been detected in cat fleas in previous studies [20, 34–36].
In all shelters, Bartonella spp. were detected in fleas and their hosts. In one shelter, the Bartonella species detected in fleas and their eggs were different from those in their respective hosts. However, the discrepant bacteria species was detected in other cats sharing the same environment. For such non coincident cases, it is possible that fleas previously fed on different bacteremic cats from the one on which they were collected.
Interestingly, bacteria DNA was detected in fleas collected from non-bacteremic hosts and detected in cats harboring negative fleas. It is noteworthy that in this study, fleas collected from cats represent a sample of the real flea population present on cats and in the local environment. Thus, newly emerged or not yet infected fleas may have been collected. Examples of different bacterial species in fleas and cat hosts has been documented previously [31, 36–39].
The presence of Bartonella DNA in C. felis fleas collected in bacteremic cats also suggests that these ectoparasites play an essential role in the transmission of Bartonella species to cats. A study has shown C. felis to be a potential vector for Bartonella species including those for which cats serve as natural reservoir, such as B. henselae and B. clarridgeiae . In fact, there is a positive correlation between previous or current flea infestation and Bartonella bacteremia in shelter cats . Although there was no statistical association, cats infested by fleas have at least twice the chance of becoming infected by Bartonella species. Similarly, previous studies found no apparent correlation [37, 39].
To the best of the authors’ knowledge, Bartonella DNA was detected for the first time in lice collected from bacteremic cat. This cat was infested with lice at the time of collection, had historic of flea infestation and lived at shelter 6, where Bartonella species DNA was also detected in fleas and contactant cats. Considering the flea importance on Bartonella transmission between cats [9, 25] and the absent link of lice infestation to Bartonella infection in cats in this and previous studies [25, 30], it is necessary to be cautious to infer that the louse was responsible for the transmission of bacteria to the cat in the present study. In order to analyse the importance of the lice as a vector of Bartonella spp. to cats, one must invest on further studies.
The possibility of vertical Bartonella spp. transmission among fleas remains as a hypothesis. In our study, B. henselae DNA was detected in naturally infected fleas and their respective eggs. Consistent with our findings, Bartonella DNA was detected in reproductive tissues (ovary) of flea species collected from several mammals, suggesting that transovarian transmission of this organism among fleas may be is possible . However, no Bartonella DNA was amplified in eggs laid by infected fleas, but the authors concluded that their results cannot be extended to natural conditions . Knowledge of Bartonella behavior and dispersal in fleas is limited and the question of whether fleas can acquire Bartonella by mechanisms other than ingestion of infected blood remains. Additional studies are needed to validate the vertical transmission hypothesis. According to a study evaluating ticks as a possible bacterial vector, transovarian transmission was not supported because no bacterial amplification was obtained in larvae even though B. henselae DNA was detected in the respective egg pools laid by female ticks that had fed on infected blood .
This study shows that three distinct Bartonella species occur in shelter cats in metropolitan region of Rio de Janeiro and that B. henselae and B. clarridgeiae circulate among fleas collected from them, reinforcing the importance of this ectoparasite in bacterial transmission between cats. For public health purposes, it is important to note that Bartonella species identified in ectoparasites and their host cats are agents associated with human disease. Thus, ectoparasites control measures should be implemented to prevent flea infestation and, consequently, Bartonella infection in cats and the humans with whom they have close contact.