Abstract
Background
Species of the genus Bartonella are facultative intracellular alphaproteobacteria with zoonotic potential. Bartonella infections in humans range from mild with unspecific symptoms to life threatening, and can be transmitted via arthropod vectors or through direct contact with infected hosts, although the latter mode of transmission is rare. Among the small mammals that harbour Bartonella spp., rodents are the most speciose group and harbour the highest diversity of these parasites. Human–rodent interactions are not unlikely as many rodent species live in proximity to humans. However, a surprisingly low number of clinical cases of bartonellosis related to rodent-associated Bartonella spp. have thus far been recorded in humans.
Methods
The main purpose of this review is to determine explanatory factors for this unexpected finding, by taking a closer look at published clinical cases of bartonellosis connected with rodent-associated Bartonella species, some of which have been newly described in recent years. Thus, another focus of this review are these recently proposed species.
Conclusions
Worldwide, only 24 cases of bartonellosis caused by rodent-associated bartonellae have been reported in humans. Possible reasons for this low number of cases in comparison to the high prevalences of Bartonella in small mammal species are (i) a lack of awareness amongst physicians of Bartonella infections in humans in general, and especially those caused by rodent-associated bartonellae; and (ii) a frequent lack of the sophisticated equipment required for the confirmation of Bartonella infections in laboratories that undertake routine diagnostic testing. As regards recently described Bartonella spp., there are presently 14 rodent-associated Candidatus taxa. In contrast to species which have been taxonomically classified, there is no official process for the review of proposed Candidatus species and their names before they are published. This had led to the use of malformed names that are not based on the International Code of Nomenclature of Prokaryotes. Researchers are thus encouraged to propose Candidatus names to the International Committee on Systematics of Prokaryotes for approval before publishing them, and only to propose new species of Bartonella when the relevant datasets allow them to be clearly differentiated from known species and subspecies.
Graphical Abstract
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Background
The genus Bartonella (family Bartonellaceae; order Rhizobiales) comprises facultative intracellular alphaproteobacteria. An increasing number of Bartonella species are recognized as zoonotic pathogens [1]. In humans, bartonellosis can have a variety of mild and unspecific clinical signs and symptoms, but can also be life threatening [2, 3]. Bartonellae can be transmitted to humans indirectly from blood-sucking arthropod vectors through the scratches of an infected reservoir host (e.g. cats) or via contact with infectious faeces of arthropod vectors. Fleas play a major role in the transmission of Bartonella, especially the cat flea (Ctenocephalides felis), one of the most common flea species in central Europe, which is host opportunistic, and thus a common source of infection of Bartonella, and especially Bartonella henselae [4]. Direct transmission through contact with reservoir hosts can not be excluded as a possible transmission path, although it is considered highly unlikely.
A wide variety of mammals are suspected of being reservoir hosts of Bartonella spp. [2]. Among mammals, small mammals, including bat and rodent species, are the group that harbours by far the highest diversity of Bartonella spp. [5]. Moreover, high prevalences of Bartonella spp. have been detected in rodents, the most speciose group of mammals [6]. As many rodent species live in proximity to humans in many parts of the world, human-rodent interactions are not unlikely. Nonetheless, very low numbers of clinical cases of bartonellosis in humans have been reported in the context of rodent-associated Bartonella. Thus, the purpose of this review is to determine explanatory factors for this unexpected finding. Therefore, we decided to explore (i) potential risk factors for humans; (ii) clinical cases described in recent years connected with rodent-associated bartonellae; and, additionally (iii) the growing trend in the scientific literature of newly described Bartonella taxa, including the reporting of a high number of Candidatus species. This review is focussed on rodent, lagomorph and other small mammal species (with the exception of bats) as they may be sympatric and share the same ectoparasites and Bartonella species.
Current knowledge on rodent reservoirs of Bartonella spp.
Global distribution of Bartonella spp. in small mammals
Rodent-associated bartonellae are distributed worldwide and have been the subject of research on almost every continent. For a systematic review of papers describing the detection of Bartonella in small mammal species, the following search engines were used: Google Scholar, PubMed, and Google. The following terms were searched for, solely or in combination: ‘Bartonella’; ‘rodent’; ‘small mammal’; and, in addition [name of any country in the world]; or [name of any continent in the world]. Furthermore, a separate search was conducted with the search term [name of any small mammal genus] in combination with one of the following terms: [Bartonella]; [Bartonellae]; [Bartonellosis]. Only studies published in the English language and in peer-reviewed journals were taken into consideration. In total, 132 studies were included in the analysis, representing research on Bartonella in a total of 231 small mammal species and subspecies (excluding bats). Research on Bartonella in small mammals has been conducted in 67 of the 195 countries (34.4%) of the world. Most of these studies were conducted in North America [in both Canada and the USA (100%)], followed by Europe [25 out of 44 countries (54.6%)] and Asia [19 out of 48 countries (39.6%)]. The continents/regions for which the lowest numbers of studies were reported are as follows: Africa [15 out of 54 countries (27.8%)], Oceania [two out of 14 countries (14.3%)], and Latin America and the Carribean [four out of 33 countries (12.1%)] (Additional file 1: Table S1). Thus, small mammals in a large number of countries have not yet been investigated for the presence of Bartonella spp. Most of these countries are located in Latin America, the Middle East, and Central Africa, and the lack of published data from them might be partly due to their economic and/or political situation. However, it is considered important that studies are especially carried out in countries in Central Africa, as they are among those with the lowest health coverage [7]. People from these areas make up a large proportion of those who most frequently need treatment for neglected tropical diseases [7], and infections with rodent-borne Bartonella spp. can also be expected to occur more frequently in these areas. It is also worth noting that studies were more frequently conducted in some countries than in others (e.g. there were 17 from the USA but only one from Argentina). The studies undertaken in the USA were conducted thoroughly and, in total, reported 25 small mammal species positive for Bartonella (Fig. 1).
The number of Bartonella-positive small mammal species per country (listed in Additional file 1: Table S1)
The most frequently studied genus was Rattus, and in particular the two cosmopolitan species Rattus norvegicus and Rattus rattus. Members of the genera Apodemus, Bandicota, Microtus, Mus, and Myodes were very often associated with Bartonella spp. The most studied rodent species was R. norvegicus (43 studies from four of the seven continents), followed by R. rattus (41 studies), Mus musculus (25 studies) and Clethrionomys glareolus (24 studies). The five Bartonella species most frequently detected in small mammal hosts were Bartonella grahamii (found in 53 small mammal species, and in 31 countries), Bartonella elizabethae (found in 43 small mammal species, and in 34 countries), Bartonella tribocorum (found in 30 small mammal species, and in 27 countries), Bartonella taylorii (found in 27 small mammal species, and in 21 countries), and Bartonella queenslandensis (found in 29 small mammal species, and in 13 countries). Small mammals positive for Bartonella were found in 65 (97.0%) of 67 investigated countries (they were not found in Hungary and Pakistan). The five most frequently listed Bartonella species in Additional file 1: Table S1 may, however, be a distortion as, for example, B. elizabethae is one of the first rodent-associated species to have been described (in 1993) whereas other rodent-associated species such as B. kosoyi were not described until much later (in 2018). Furthermore, it should be noted that various methods were used in the studies, and that not all the published sequences had a homology of 100%.
Clinical cases of bartonellosis in humans in the context of rodent-associated Bartonella spp.
Clinical symptoms/clinical cases, diagnostics, and pathogenicity
The most frequently described Bartonella species pathogenic for humans include the human-specific species Bartonella bacilliformis (transmitted via sand flies), which causes Carrion’s disease in South America; the zoonotic, cat-transmitted species B. henselae, which is responsible for cat scratch disease; and the human-specific species Bartonella quintana (transmitted via body lice), the causative agent of trench fever [8]. Much less is known about human infections with other Bartonella spp. In general, endocarditis, lymphadenopathy and neuroretinitis are common symptoms of severe cases of bartonellosis [9]. A detailed PubMed analysis (performed on 2 October 2021) with the search terms ‘Bartonella [species]’ where the species was one of the 33 Bartonella species given in Table 1 [e.g. (‘B. alsatica’) and (‘infection’)] revealed only 14 publications citing evidence for human infections (see Table 2).
When high diagnostic standards were applied (including direct pathogen detection via culture or PCR), only eight Bartonella species or subspecies (Bartonella vinsonii subsp. arupensis infections, B. elizabethae infections, Bartonella alsatica infections, B. tribocorum or B. vinsonii subsp. vinsonii infections, Bartonella doshiae, B. grahamii, Bartonella rattimassiliensis) were reported (in total, 24 confirmed patient cases; see Table 2).
The analysis of the frequencies of clinical entities showed that 12 patients suffered from acute febrile illness (most likely associated with bacteremia/blood stream infections) (50%), three patients from endocarditis or prosthetic valvular graft infections (12.5%), three patients from lymphadenopathy (12.5%), two from nonspecific symptoms (8.3%), and one each from bacillary angiomatosis, hepatic lesions or neuroretinitis (4.2%). Two of these patients were immunocompromised (human immunodeficiency virus infection, leukemia); no clear association with an underlying comorbidity was reported for the remaining patients. The reported antibiotic therapy regime varied but often included the administration of a macrolide combined with doxycycline for some weeks, which often resulted in clinical improvement.
From a clinical point of view, ‘acute febrile illness’ and ‘endocarditis’ can be classified as ‘bacteremia/blood stream infections’, which 15 of 24 reported patients (62.5%) suffered from. Although these cases were anecdotal, it can be suggested that human infections by rodent-associated Bartonella spp. are rare. To our knowledge, there are several possible reasons for this low number of case reports: (i) physicians are very likely unaware of Bartonella infections (especially when rodent-associated), and thus do not include them in their differential diagnosis; (ii) laboratories may not able to detect these pathogens due to their fastidious nature, and because their diagnostic portfolio does not include PCR tests for the detection of Bartonella spp. or they do not carry out long, sterile microaerophilic incubations for the cultivation of samples from patients. Moreover, (iii) bartonellosis might only cause mild and unspecific symptoms; and (iv) rodent-associated Bartonella infections of humans may simply be rare medical entities. A possible molecular explanation for the latter is the host restriction of Bartonella species mediated by their respective Trw type IV secretion systems (T4SSs) [10]. The Trw T4SS (originally described as a plasmid conjugation system) is crucial for adhesion to erythrocytes and subsequent erythrocyte invasion, and Bartonella with mutations in the trwE gene (signature-tagged mutagenesis) are unable to establish long-lasting bacteremia in certain rodent infection models. It has been demonstrated that the Trw systems of certain Bartonella spp. are responsible for species-specific host-restricted adhesion to erythrocytes. For instance, the Trw T4SS of B. tribocorum mediates a significant bacterial infection in Wistar rats, but infection human erythrocytes is 23 times less efficient. It seems likely that infections of humans by rodent-adapted Bartonella spp. rarely occur because the rodent-pathogen Trw system and human erythrocyte host receptors simply do not match.
Groups at risk of Bartonella infection in the context of rodent-associated Bartonella spp.
Many Bartonella species are pathogenic for humans. However, B. henselae, B. bacilliformis and B. quintana cause most cases of Bartonella disease in humans [8, 11]. Veterinarians, veterinary nurses and people that work with and care for animals seem to be at increased risk of infection as they are particularly exposed to reservoir hosts and vectors of Bartonella spp. [12,13,14]. Oteo et al. [15] found that 11.2–56% of tested veterinary professionals in Spain showed seroreactivity for B. henselae, B. quintana, and/or B. vinsonii berkhoffii. Bartonella spp. were even isolated from 7.9% of the positive individuals, although all of them were asymptomatic [15]. Bartonella henselae is also reported to have possibly contributed to the death of two veterinarians [16]. Cat and dog owners also appear to be at increased risk of infection. Transmission of B. henselae is associated with scratches received from both cats and dogs [17]. Owners of a cat ≤ 12 months old have an increased risk of infection with B. henselae compared to those with a cat > 12 months old [18]. Forest workers and orienteers seem to be the other groups at risk [19, 20]. Furthermore, a higher risk of infection has also been described for homeless people, alcoholics, and drug addicts who administer substances intravenously [21, 22]. Though an intravenous transmission route seems unlikely, one study did show that drug addicts who administered substances intravenously were more at risk of contracting Bartonella spp. [20]. Infestation with ectoparasites such as lice and fleas due to poor hygiene may also lead to bartonellosis, especially in homeless people [23].
The risk factors for rodent-associated Bartonella infections in humans are similar to those mentioned above for Bartonella transmitted via other animals (Table 2). Most of the patients listed in Table 2 were either young, old, pregnant or immunosuppressed. We assume that inclusion in one of these groups is a risk factor for developing clinical symptoms after infection with rodent-associated bartonellae because these groups are associated with an impaired or not yet fully developed immune system. Thus, rodent-associated bartonellosis seems to be opportunistic and might be more likely to develop when a person has a pre-existing medical condition. Furthermore, the studies showed that being homeless [24], abusing drugs [20], or being in contact with animals, e.g. through hunting or animal breeding, may increase the risk of rodent-associated Bartonella infection.
Reservoir role and clinical cases of pet animals infected with rodent-associated Bartonella spp.
Cats are known hosts of B. henselae (and Bartonella clarridgeiae and Bartonella kohlerae) and dogs of Bartonella rochalimae. Thus far, there have only been occasional reports of clinical symptoms in cats and dogs related to Bartonella spp. infection, and even fewer related to rodent-associated bartonellae. Whether bartonellae are primary or opportunistic pathogens for cats and dogs is not entirely clear. Clinical manifestations of bartonellosis are rarely seen in domestic cats, and to the best of our knowledge, there have been no case reports of rodent-associated bartonellosis in them. However, there is one report of a cat which was thought to have transmitted rodent-associated B. grahamii to a human via a scratch [25]. Unlike cats, dogs may develop severe clinical symptoms of bartonellosis that are similar to those displayed by humans [26]. Thus far, rodent-associated B. elizabethae, B. grahamii, B. taylori and a Bartonella volans-like strain have been detected in dogs [27,28,29]. However, only B. elizabethae infections could be linked directly to a canine clinical case. An 8-year-old dog suffering from unspecific symptoms including lethargy, appetite and weight loss was diagnosed with B. elizabethae infection in the blood stream. The dog died immediately before the diagnosis was confirmed, and no other pathogen was detected in the blood [28]. Furthermore, there is one record of a dog with a previously unspecified clinical record which was found to be positive for a strain of B. volans after its death [29]. Bartonella grahamii, B. elizabethae, B. taylorii were found to have a moderate prevalence (9.4%) in stray dogs without a clinical record in Thailand, highlighting the potential reservoir competence of dogs for rodent-associated bartonellae [27].
Current insights into Bartonella taxonomy with a focus on recently discovered small mammal-associated Bartonella spp.
Bartonellae can be divided into eubartonellae and other ancient clades according to their genetic features [5]. Eubartonellae can further be subdivided into four lineages, one of which is the most diverse with regard to potential host species as well as species and subspecies of Bartonella. There are presently 84 known species and subspecies of Bartonella, of which 38 were initially found in specimens belonging to the order Rodentia, followed by 10 species each in specimens of the orders Carnivora and Artiodactyla, and seven in humans. The number of newly described species has been increasing in the past decade [5]. Forty-five new Bartonella species have been proposed and/or published since 2011 (Table 1). Most of these newly described Bartonella species (n = 30) were reported in wild small mammal or specifically rodent species such as Acomys russatus (golden spiny mouse), Mastomys erythroleucus (Guinea multimammate mouse), and Pachyuromys duprasi (fat-tailed gerbil) (Table 1). Out of the 51 proposed or published rodent- or other small mammal-associated species, 19 have Candidatus status.
There is an increasing number of newly discovered, not yet fully characterized, Bartonella species with Candidatus status. Labelling a potentially new species Candidatus is a new concept that began in the 1990s [30] and allows researchers to propose prokaryotic taxa that are well characterized but as yet uncultured. In contrast to official species names, there is no official process for reviewing proposed Candidatus species and their names before they are published (A. Oren, personal communication). Authors are welcome to submit the proposed names to the Judicial Commission on Prokaryote Nomenclature of the International Committee on Systematics of Prokaryotes (ICSP), but they are not obliged to do so. The committee reviews Candidatus species through an extensive literature review, as many Candidatus names have not been qualitatively validated or do not follow the rules of the International Code of Nomenclature of Prokaryotes [31], which explains why many Candidatus names in use for newly described Bartonella species are malformed. However, suggested corrections for these malformed names are regularly published [32]. Nevertheless, due to the large number of new Candidatus taxa being proposed, particularly those with rodents and other small mammals as their origin and likely reservoir hosts, the lists of corrected names are not exhaustive and constantly evolving [31, 32].
Thus, the above should be borne in mind with respect to newly described Candidatus species and their published names. A mandatory submission process for the validation of species names prior to the publication of newly proposed Candidatus species would help to avoid the time-consuming renaming process carried out by the ICSP, and would further help to avoid the circulation in the literature of malformed Candidatus names. For example, the ICSP proposes that ‘Bartonella bandicootii’ should be re-named ‘Bartonella paramelis’ (Table 1). ‘Bandicoot’ is the English name of the animal from which this species of Bartonella was isolated, but the proposed specific epithet ‘bandicootii’ (rather than ‘bandicooti’) is both malformed and in violation of recommendation 6 (3) of the ICNP. The genus name of the host animal, which is Parameles, should be used as the basis for the specific epithet of the Bartonella species rather than the English common name, bandicoot, which is why the current name of this species should be Bartonella paramelis [33].
Furthermore, an increasing number of Bartonella species without Candidatus status have not been validly published according to the ICNP. In total, there are 44 Bartonella species names currently in use that have not been validly published. Of these species, 40 have been described since 2007, and 17 are from rodents or other small mammals (Table 1). As the number of newly described Bartonella species is increasing, in particular with respect to those isolated from rodents and other small mammals, it would be helpful if their names were proposed for approval under the ICNP before they were published, and that these should only be published when the relevant dataset allows these Bartonella species to be clearly differentiated from known species and subspecies of the genus. At present, it is not always easy to define a species or subspecies, but with whole genome sequencing becoming more affordable, it is highly likely that this issue will be resolved in the future through the sufficient description of new Candidatus species through the use of this genetic technique [34].
Further reasons for low numbers of cases of bartonellosis in humans despite high prevalences of Bartonella spp. in rodents and other small mammals
At first glance, it appears to be a phenomenon that Bartonella spp. from small mammals seem to be the least pathogenic for humans and their companion animals, and especially so in the case of rodents, as these comprise the group of small mammals with the highest prevalences and diversities of recorded Bartonella species, are commonly found in urban areas, and are known to harbour and spread disease [35]. Recent work demonstrated that one third of Norway rats in the Belgian region of Flanders harboured B. tribocorum, yet no human cases of infection with this parasite have been reported there [36]. Although it does not seem plausible that there is no transmission of Bartonella spp. from rodents to humans, in particular when taking into consideration the prevalences of Bartonella spp. in rodents and the frequent proximity of the latter to humans, there are several factors that might account for this.
Rodent-associated Bartonella spp. are probably arthropod-borne pathogens, but transmission through rodent scratches or bites (as is often reported for B. henselae infections) cannot be completely ruled out [1, 37]. Several studies have reported possible vertical transmission in naturally infected rodents [37,38,39]. However, a study on infected Clethrionomys glareolus could not experimentally prove transplacental or transovarial transmission of B. taylorii and B. grahamii to the offspring. There is one report of possible vertical transmission of B. birtlesii in BALB/c mice [40]. Most rodent-associated flea species are host specific and do not infest humans, which further limits potential zoonotic transmission of Bartonella spp. However, a few flea species are known to be more host opportunistic [41]. Yersinia pestis, the causative agent of the plague, is known to be transmitted from rats to humans mainly through Xenopsylla cheopis, the oriental rat flea [42], which can cause severe outbreaks of the disease. Xenopsylla cheopis is also known to harbour DNA of zoonotic Bartonella spp. such as B. elizabethae, and it was experimentally shown that X. cheopis can excrete this species over time [43, 44]. Nonetheless, there are, to the best of our knowledge, no reported cases of bartonellosis in humans previously infested with this flea species.
Another possible means of infection is direct contact with a reservoir host. Cats may transmit B. henselae to humans through their scratches [45]. There is even one report of a cat transmitting B. grahamii, which is a rodent-associated pathogen, to its owner [25]. The explanation for this was that the cat came into contact with an infected rodent when it caught it with its paws, which then became infectious. As rodents are not predators of humans and tend to avoid them, direct contact between the two is highly unlikely, with the exception of small mammals kept as pets [46]. However, indirect transmission via a cat is a possible, though unlikely, transmission path [25].
Notwithstanding the cases described above, rodent-associated bartonellae are the principal cause of bartonellosis in humans. However, how and to what extent rodents and their ectoparasites are involved in the zoonotic transmission cycle of Bartonella is not fully understood. Studying the transmission of Bartonella spp. from rodents to humans would help in assessing the potential risk of the former for the latter.
Conclusions
The zoonotic transmission cycle of rodent-associated bartonellae is not fully understood. It is especially unknown whether Bartonella infections in humans arise from direct contact with small mammals or rather indirectly via infestation with a rodent-associated ectoparasite vector. The total number of confirmed human cases of bartonellosis worldwide caused by rodent-associated bartonellae is much lower than expected when taking into account the abundance of Bartonella spp. in rodents, and possible reasons for this have been discussed in this review. Many small mammal species are considered reservoir hosts for the increasing number of newly described Bartonella spp., although some of the latter have yet to be experimentally confirmed. Even though most Bartonella spp. show high adaptation to their hosts, this is not the case for all rodent-associated species. That is why further experimental research is needed to increase our understanding of host–pathogen interactions between rodents and Bartonella species.
Availability of data and materials
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Abbreviations
- ICNP:
-
International Code of Nomenclature of Prokaryotes
- ICSP:
-
International Committee on Systematics of Prokaryotes
- Trw T4SS:
-
Trw type IV secretion system
References
Gutiérrez R, Krasnov B, Morick D, Gottlieb Y, Khokhlova IS, Harrus S. Bartonella infection in rodents and their flea ectoparasites: an overview. Vector Borne Zoonotic Dis. 2015;15:27–39. https://doi.org/10.1089/vbz.2014.1606.
Breitschwerdt EB, Maggi RG, Chomel BB, Lappin MR. Bartonellosis: an emerging infectious disease of zoonotic importance to animals and human beings. J Vet Emerg Crit Care. 2010;20:8–30. https://doi.org/10.1111/j.1476-4431.2009.00496.x.
Garcia-Quintanilla M, Dichter AA, Guerra H, Kempf VAJ. Carrion’s disease: more than a neglected disease. Parasit Vectors. 2019;12:141. https://doi.org/10.1186/s13071-019-3390-2.
Portillo A, Santibáñez S, García-Álvarez L, Palomar AM, Oteo JA. Rickettsioses in Europe. Microbes Infect. 2015;17:834–8. https://doi.org/10.1016/j.micinf.2015.09.009.
Wagner A, Dehio C. Role of distinct type-IV-secretion systems and secreted effector sets in host adaptation by pathogenic Bartonella species. Cell Microbiol. 2019;21: e13004. https://doi.org/10.1111/cmi.13004.
Michaux J, Reyes A, Catzeflis F. Evolutionary history of the most speciose mammals: molecular phylogeny of muroid rodents. Mol Biol Evol. 2001;18:2017–31. https://doi.org/10.1093/oxfordjournals.molbev.a003743.
Report WHO. World health statistics 2021: monitoring health for the SDGs, sustainable development goals. Geneva: WHO; 2021.
Kaiser PO, Riess T, O’Rourke F, Linke D, Kempf VAJ. Bartonella spp.: throwing light on uncommon human infections. Int J Med Microbiol. 2011;301:7–15. https://doi.org/10.1016/j.ijmm.2010.06.004.
Edouard S, Nabet C, Lepidi H, Fournier P-E, Raoult D. Bartonella, a common cause of endocarditis: a report on 106 cases and review. J Clin Microbiol. 2015;53:824–9. https://doi.org/10.1128/JCM.02827-14.
Vayssier-Taussat M, Le Rhun D, Deng HK, Biville F, Cescau S, Danchin A, et al. The Trw type IV secretion system of Bartonella mediates host-specific adhesion to erythrocytes. PLoS Pathog. 2010;6: e1000946. https://doi.org/10.1371/journal.ppat.1000946.
Lamas C, Curi A, Bóia MN, Lemos ERS. Human bartonellosis: seroepidemiological and clinical features with an emphasis on data from Brazil—a review. Mem Inst Oswaldo Cruz. 2008;103:221–35. https://doi.org/10.1590/S0074-02762008000300001.
Oliveira AM, Maggi RG, Woods CW, Breitschwerdt EB. Suspected needle stick transmission of Bartonella vinsonii subspecies berkhoffii to a veterinarian. J Vet Intern Med. 2010;24:1229–32. https://doi.org/10.1111/j.1939-1676.2010.0563.x.
Maggi RG, Mascarelli PE, Pultorak EL, Hegarty BC, Bradley JM, Mozayeni BR, Breitschwerdt EB. Bartonella spp. bacteremia in high-risk immunocompetent patients. Diagn Microbiol Infect Dis. 2011;71:430–7. https://doi.org/10.1016/j.diagmicrobio.2011.09.001.
Lantos PM, Maggi RG, Ferguson B, Varkey J, Park LP, Breitschwerdt EB, Woods CW. Detection of Bartonella species in the blood of veterinarians and veterinary technicians: a newly recognized occupational hazard? Vector Borne Zoonotic Dis. 2014;14:563–70. https://doi.org/10.1089/vbz.2013.1512.
Oteo JA, Maggi R, Portillo A, Bradley J, García-Álvarez L, San-Martín M, et al. Prevalence of Bartonella spp. by culture, PCR and serology, in veterinary personnel from Spain. Parasit Vectors. 2017;10:1–9. https://doi.org/10.1186/s13071-017-2483-z.
Breitschwerdt EB. Did Bartonella henselae contribute to the deaths of two veterinarians? Parasit Vectors. 2015;8:1–11. https://doi.org/10.1186/s13071-015-0920-4.
Keret D, Giladi M, Kletter Y, Wientroub S. Cat-scratch disease osteomyelitis from a dog scratch. J Bone Joint Surg. 1998;80:766–7.
Zangwill KM, Hamilton DH, Perkins BA, Regnery RL, Plikaytis BD, Hadler JL, et al. Cat scratch disease in Connecticut—epidemiology, risk factors, and evaluation of a new diagnostic test. N Engl J Med. 1993;329:8–13. https://doi.org/10.1056/NEJM199307013290102.
Jurke A, Bannert N, Brehm K, Fingerle V, Kempf VAJ, Kömpf D, et al. Serological survey of Bartonella spp., Borrelia burgdorferi, Brucella spp., Coxiella burnetii, Francisella tularensis, spp., Echinococcus, Hanta-, TBE- and XMR-virus infection in employees of two forestry enterprises in North Rhine–Westphalia, Germany, 2011–2013. Int J Med Microbiol. 2015;305:652–62. https://doi.org/10.1016/j.ijmm.2015.08.015.
McGILL S, Hjelm E, Rajs J, Lindquist O, Friman G. Bartonella spp. antibodies in forensic samples from Swedish heroin addicts. Ann N York Acad Sci. 2003;990:409–13. https://doi.org/10.1111/j.1749-6632.2003.tb07402.x.
Jackson LA, Spaeh DH, Kippen DA, Sugg NK, Regnery RL, Sayers MH, Stamm WE. Seroprevalence to Bartonella quintana among patients at a community clinic in downtown Seattle. J Infect Dis. 1996;173:1023–6. https://doi.org/10.1093/infdis/173.4.1023.
Spach DH, Kanter AS, Dougherty MJ, Larson AM, Coyle MB, Brenner DJ, et al. Bartonella (Rochalimaea) quintana bacteremia in inner-city patients with chronic alcoholism. N Engl J Med. 1995;332:424–8. https://doi.org/10.1056/NEJM199502163320703.
Foucault C, Brouqui P, Raoult D. Bartonella quintana characteristics and clinical management. Emerg Infect Dis. 2006;12:217–23. https://doi.org/10.3201/eid1202.050874.
Smith HM, Reporter R, Rood MP, Linscott AJ, Mascola LM, Hogrefe W, Purcell RH. Prevalence study of antibody to ratborne pathogens and other agents among patients using a free clinic in downtown Los Angeles. J Infect Dis. 2002;186:1673–6. https://doi.org/10.1086/345377.
Oksi J, Rantala S, Kilpinen S, Silvennoinen R, Vornanen M, Veikkolainen V, et al. Cat scratch disease caused by Bartonella grahamii in an immunocompromised patient. J Clin Microbiol. 2013;51:2781–4. https://doi.org/10.1128/JCM.00910-13.
Chomel BB, Boulouis H, Maruyama S, Breitschwerdt EB. Bartonella spp. in pets and effect on human health. Emerg Infect Dis. 2006;12:389–94. https://doi.org/10.3201/eid1203.050931.
Bai Y, Kosoy MY, Boonmar S, Sawatwong P, Sangmaneedet S, Peruski LF. Enrichment culture and molecular identification of diverse Bartonella species in stray dogs. Vet Microbiol. 2010;146:314–9. https://doi.org/10.1016/j.vetmic.2010.05.017.
Mexas AM, Hancock SI, Breitschwerdt E. Bartonella henselae and Bartonella elizabethae as potential canine pathogens. J Clin Microbiol. 2002. https://doi.org/10.1128/JCM.40.12.4670-4674.2002.
Pérez C, Maggi RG, Diniz PPVP, Breitschwerdt EB. Molecular and serological diagnosis of Bartonella infection in 61 dogs from the United States. J Vet Intern Med. 2011;25:805–10. https://doi.org/10.1111/j.1939-1676.2011.0736.x.
Murray RG, Stackebrandt E. Taxonomic note: implementation of the provisional status Candidatus for incompletely described procaryotes. Int J Syst Bacteriol. 1995;45:186–7. https://doi.org/10.1099/00207713-45-1-186.
Oren A, Garrity GM, Parker CT, Chuvochina M, Trujillo ME. Lists of names of prokaryotic Candidatus taxa. Int J Syst Evol Microbiol. 2020;70:3956–4042. https://doi.org/10.1099/ijsem.0.003789.
Oren A, Garrity GM. Candidatus list no. 2. Lists of names of prokaryotic Candidatus taxa taxa. Int J Syst Evol Microbiol. 2021. https://doi.org/10.1099/ijsem.0.004671.
Oren A. A plea for linguistic accuracy—also for Candidatus taxa. Int J Syst Evol Microbiol. 2017;67:1085–94. https://doi.org/10.1099/ijsem.0.001715.
Gutiérrez R, Vayssier-Taussat M, Buffet J-P, Harrus S. Guidelines for the isolation, molecular detection, and characterization of Bartonella species. Vector Borne Zoonotic Dis. 2017;17:42–50. https://doi.org/10.1089/vbz.2016.1956.
Himsworth CG, Parsons KL, Jardine C, Patrick DM. Rats, cities, people, and pathogens: a systematic review and narrative synthesis of literature regarding the ecology of rat-associated zoonoses in urban centers. Vector Borne Zoonotic Dis. 2013;13:349–59. https://doi.org/10.1089/vbz.2012.1195.
Krügel M, Pfeffer M, Król N, Imholt C, Baert K, Ulrich RG, Obiegala A. Rats as potential reservoirs for neglected zoonotic Bartonella species in Flanders, Belgium. Parasit Vectors. 2020;13:235. https://doi.org/10.1186/s13071-020-04098-y.
Bown KJ, Bennett M, Begon M. Flea-borne Bartonella grahamii and Bartonella taylorii in bank voles. Emerg Infect Dis. 2004;10:684–7. https://doi.org/10.3201/eid1004.030455.
Kosoy MY, Regnery RL, Kosaya OI, Jones DC, Marston EL, Childs JE. Isolation of Bartonella spp. from embryos and neonates of naturally infected rodents. J Wildl Dis. 1998;34:305–9. https://doi.org/10.7589/0090-3558-34.2.305.
Tołkacz K, Alsarraf M, Kowalec M, Dwużnik D, Grzybek M, Behnke JM, Bajer A. Bartonella infections in three species of Microtus: prevalence and genetic diversity, vertical transmission and the effect of concurrent Babesia microti infection on its success. Parasit Vectors. 2018;11:491. https://doi.org/10.1186/s13071-018-3047-6.
Boulouis HJ, Barrat F, Bermond D, Bernex F, Thibault D, Heller R, et al. Kinetics of Bartonella birtlesii infection in experimentally infected mice and pathogenic effect on reproductive functions. Infect Immun. 2001;69:5313–7. https://doi.org/10.1128/IAI.69.9.5313-5317.2001.
Shenbrot G, Krasnov B, Lu L. Geographical range size and host specificity in ectoparasites: a case study with Amphipsylla fleas and rodent hosts. J Biogeogr. 2007;34:1679–90. https://doi.org/10.1111/j.1365-2699.2007.01736.x.
Miarinjara A, Boyer S. Current perspectives on plague vector control in Madagascar: susceptibility status of Xenopsylla cheopis to 12 insecticides. PLoS Negl Trop Dis. 2016;10: e0004414. https://doi.org/10.1371/journal.pntd.0004414.
Billeter SA, Gundi VAKB, Rood MP, Kosoy MY. Molecular detection and identification of Bartonella species in Xenopsylla cheopis fleas (Siphonaptera: Pulicidae) collected from Rattus norvegicus rats in Los Angeles, California. Appl Environ Microbiol. 2011;77:7850–2. https://doi.org/10.1128/AEM.06012-11.
McKee CD, Osikowicz LM, Schwedhelm TR, Maes SE, Enscore RE, Gage KL, Kosoy MY. Acquisition of Bartonella elizabethae by experimentally exposed oriental rat fleas (Xenopsylla cheopis; Siphonaptera, Pulicidae) and excretion of Bartonella DNA in flea feces. J Med Entomol. 2018;55:1292–8. https://doi.org/10.1093/jme/tjy085.
Chomel BB, Boulouis HJ, Breitschwerdt EB. Cat scratch disease and other zoonotic Bartonella infections. J Am Vet Med Assoc. 2004;224:1270–9. https://doi.org/10.2460/javma.2004.224.1270.
Orellana-Rios J, Verdaguer-Diaz JI, Opazo G, Leong BCS, Zett C, Smith RT, Freund KB. Not cat-scratch disease: Bartonella henselae neuroretinitis associated with non-feline pet mammals. IDCases. 2020;22: e00978. https://doi.org/10.1016/j.idcr.2020.e00978.
Inoue K, Maruyama S, Kabeya H, Hagiya K, Izumi Y, Une Y, Yoshikawa Y. Exotic small mammals as potential reservoirs of zoonotic Bartonella spp. Emerging Infect Dis. 2009;15:526–32. https://doi.org/10.3201/eid1504.081223.
Marciano O, Gutiérrez R, Morick D, King R, Nachum-Biala Y, Baneth G, Harrus S. Detection of Bartonella spp. in wild carnivores, hyraxes, hedgehog and rodents from Israel. Parasitology. 2016;143:1232–42. https://doi.org/10.1017/S0031182016000603.
Morick D, Baneth G, Avidor B, Kosoy MY, Mumcuoglu KY, Mintz D, et al. Detection of Bartonella spp. in wild rodents in Israel using HRM real-time PCR. Vet Microbiol. 2009;139:293–7. https://doi.org/10.1016/j.vetmic.2009.06.019.
Bajer A, Harris PD, Behnke JM, Bednarska M, Barnard CJ, Sherif N, et al. Local variation of haemoparasites and arthropod vectors, and intestinal protozoans in spiny mice (Acomys dimidiatus) from four montane wadis in the St Katherine Protectorate, Sinai, Egypt. J Zool. 2006;270:9–24. https://doi.org/10.1111/j.1469-7998.2006.00089.x.
Sato S, Kabeya H, Fujinaga Y, Inoue K, Une Y, Yoshikawa Y, Maruyama S. Bartonella jaculi sp. nov., Bartonella callosciuri sp. nov., Bartonella pachyuromydis sp. nov. and Bartonella acomydis sp. nov., isolated from wild Rodentia. Int J Syst Evol Microbiol. 2013;63:1734–40. https://doi.org/10.1099/ijs.0.041939-0.
Theonest NO, Carter RW, Amani N, Doherty SL, Hugho E, Keyyu JD, et al. Molecular detection and genetic characterization of Bartonella species from rodents and their associated ectoparasites from northern Tanzania. PLoS ONE. 2019;14: e0223667. https://doi.org/10.1371/journal.pone.0223667.
Hatyoka LM, Brettschneider H, Bennett NC, Kleynhans DJ, Muteka SP, Bastos ADS. Bartonella diversity and zoonotic potential in indigenous Tete Veld rats (Aethomys ineptus) from South Africa. Infect Genet Evol. 2019;73:44–8. https://doi.org/10.1016/j.meegid.2019.04.012.
Pretorius A-M, Beati L, Birtles RJ. Diversity of bartonellae associated with small mammals inhabiting Free State province, South Africa. Int J Syst Evol Microbiol. 2004;54:1959–67. https://doi.org/10.1099/ijs.0.03033-0.
An CH, Chen BB, Lyu W, Nie SM, Li SZ, Fan SP, et al. Bartonella species investigated among rodents from Shaanxi Province of China. Biomed Environ Sci. 2020;33:201–5. https://doi.org/10.3967/bes2020.028.
Rao H, Li S, Lu L, Wang R, Song X, Sun K, et al. Genetic diversity of Bartonella species in small mammals in the Qaidam Basin, western China. Sci Rep. 2021;11:1735. https://doi.org/10.1038/s41598-021-81508-w.
Ying B, Kosoy MY, Maupin GO, Tsuchiya KR, Gage KL. Genetic and ecologic characteristics of Bartonella communities in rodents in southern China. Am J Trop Med Hyg. 2002;66:622–7. https://doi.org/10.4269/ajtmh.2002.66.622.
Jeske K, Herzig-Straschil B, Răileanu C, Kunec D, Tauchmann O, Emirhar D, et al. Zoonotic pathogen screening of striped field mice (Apodemus agrarius) from Austria. Transbound Emerg Dis. 2021. https://doi.org/10.1111/tbed.14015.
Mitkovska V, Dimitrov H, Kunchev A, Chassovnikarova T. Micronucleus frequency in rodents with blood parasites. Acta Zool Bulgarica. 2020:33–41.
Liu Q, Sun J, Lu L, Fu G, Ding G, Song X, et al. Detection of Bartonella species in small mammals from Zhejiang Province, China. J Wildl Dis. 2010;46:179–85. https://doi.org/10.7589/0090-3558-46.1.179.
Qin X-R, Liu J-W, Yu H, Yu X-J. Bartonella species detected in rodents from Eastern China. Vector Borne Zoonotic Dis. 2019;19:810–4. https://doi.org/10.1089/vbz.2018.2410.
Li D-M, Hou Y, Song X-P, Fu Y-Q, Li G-C, Li M, et al. High prevalence and genetic heterogeneity of rodent-borne Bartonella species on Heixiazi Island, China. Appl Environ Microbiol. 2015;81:7981–92. https://doi.org/10.1128/AEM.02041-15.
Tadin A, Tokarz R, Markotić A, Margaletić J, Lipkin WI, Habuš J, et al. Molecular survey of zoonotic agents in rodents and other small mammals in Croatia. Am J Trop Med Hyg. 2016;94:466–73. https://doi.org/10.4269/ajtmh.15-0517.
Silaghi C, Pfeffer M, Kiefer D, Kiefer M, Obiegala A. Bartonella, rodents, fleas and ticks: a molecular field study on host-vector-pathogen associations in Saxony, Eastern Germany. Microb Ecol. 2016;72:965–74. https://doi.org/10.1007/s00248-016-0787-8.
Galfsky D, Król N, Pfeffer M, Obiegala A. Long-term trends of tick-borne pathogens in regard to small mammal and tick populations from Saxony, Germany. Parasit Vectors. 2019;12:131. https://doi.org/10.1186/s13071-019-3382-2.
Obiegala A, Pfeffer M, Kiefer D, Kiefer M, Król N, Silaghi C. Bartonella spp. in small mammals and their fleas in differently structured habitats from Germany. Front Vet Sci. 2020;7:625641. https://doi.org/10.3389/fvets.2020.625641.
Mardosaitė-Busaitienė D, Radzijevskaja J, Balčiauskas L, Bratchikov M, Jurgelevičius V, Paulauskas A. Prevalence and diversity of Bartonella species in small rodents from coastal and continental areas. Sci Rep. 2019;9:12349. https://doi.org/10.1038/s41598-019-48715-y.
Hildebrand J, Paziewska-Harris A, Zaleśny G, Harris PD. PCR Characterization suggests that an unusual range of Bartonella species infect the striped field mouse (Apodemus agrarius) in central Europe. Appl Environ Microbiol. 2013;79:5082–4. https://doi.org/10.1128/AEM.01013-13.
Mediannikov O, Ivanov L, Zdanovskaya N, Vysochina N, Fournier P-E, Tarasevich I, Raoult D. Molecular screening of Bartonella species in rodents from the Russian Far East. Ann N Y Acad Sci. 2005;1063:308–11. https://doi.org/10.1196/annals.1355.049.
Kim KS, Inoue K, Kabeya H, Sato S, Takada T, Pangjai D, et al. prevalence and diversity of Bartonella species in wild small mammals in Asia. J Wildl Dis. 2016;52:10–21. https://doi.org/10.7589/2015-01-015.
Karbowiak G, Stanko M, Fričová J, Wita I, Hapunik J, Peťko B. Blood parasites of the striped field mouse Apodemus agrarius and their morphological characteristics. Biologia. 2009;64:1219–24. https://doi.org/10.2478/s11756-009-0195-3.
Kraljik J, Paziewska-Harris A, Miklisová D, Blaňarová L, Mošanský L, Bona M, Stanko M. Genetic diversity of Bartonella genotypes found in the striped field mouse (Apodemus agrarius) in Central Europe. Parasitology. 2016;143:1437–42. https://doi.org/10.1017/S0031182016000962.
Knap N, Duh D, Birtles R, Trilar T, Petrovec M, Avšič-Županc T. Molecular detection of Bartonella species infecting rodents in Slovenia. FEMS Immunol Med Microbiol. 2007;50:45–50. https://doi.org/10.1111/j.1574-695X.2007.00226.x.
Chae J-S, Yu D-H, Shringi S, Klein TA, Kim H-C, Chong S-T, et al. Microbial pathogens in ticks, rodents and a shrew in northern Gyeonggi-do near the DMZ, Korea. J Vet Sci. 2008;9:285–93. https://doi.org/10.4142/jvs.2008.9.3.285.
Kim C-M, Kim J-Y, Yi Y-H, Lee M-J, Cho M-r, Shah DH, et al. Detection of Bartonella species from ticks, mites and small mammals in Korea. J Vet Sci. 2005;6:327–34.
Polat C, Çelebi B, Irmak S, Karataş A, Çolak F, Matur F, et al. Characterization of Bartonella taylorii strains in small mammals of the Turkish Thrace. EcoHealth. 2020;17:477–86. https://doi.org/10.1007/s10393-021-01518-y.
Szewczyk T, Werszko J, Slivinska K, Laskowski Z, Karbowiak G. Molecular detection of Bartonella spp. in rodents in chernobyl exclusion zone, Ukraine. Acta Parasit. 2021;66:222–7. https://doi.org/10.1007/s11686-020-00276-1.
Inoue K, Maruyama S, Kabeya H, Yamada N, Ohashi N, Sato Y, et al. Prevalence and genetic diversity of Bartonella species isolated from wild rodents in Japan. Appl Environ Microbiol. 2008;74:5086–92. https://doi.org/10.1128/AEM.00071-08.
Inoue K, Kabeya H, Kosoy MY, Bai Y, Smirnov G, McColl D, et al. Evolutional and geographical relationships of Bartonella grahamii isolates from wild rodents by multi-locus sequencing analysis. Microb Ecol. 2009;57:534–41. https://doi.org/10.1007/s00248-009-9488-x.
Inoue K, Kabeya H, Shiratori H, Ueda K, Kosoy MY, Chomel BB, et al. Bartonella japonica sp. nov. and Bartonella silvatica sp. nov., isolated from Apodemus mice. Int J Syst Evol Microbiol. 2010;60:759–63. https://doi.org/10.1099/ijs.0.011528-0.
Kabeya H, Inoue K, Izumi Y, Morita T, Imai S, Maruyama S. Bartonella species in wild rodents and the infested fleas in Japan. J Vet Med Sci. 2011;73:1561–7. https://doi.org/10.1292/jvms.11-0134.
Schmidt S, Essbauer SS, Mayer-Scholl A, Poppert S, Schmidt-Chanasit J, Klempa B, et al. Multiple infections of rodents with zoonotic pathogens in Austria. Vector Borne Zoonotic Dis. 2014;14:467–75. https://doi.org/10.1089/vbz.2013.1504.
Engbaek K, Lawson PA. Identification of Bartonella species in rodents, shrews and cats in Denmark: detection of two B. henselae variants, one in cats and the other in the long-tailed field mouse. APMIS. 2004;112:336–41. https://doi.org/10.1111/j.1600-0463.2004.apm1120603.x.
Tea A, Alexiou-Daniel S, Papoutsi A, Papa A, Antoniadis A. Bartonella species isolated from rodents, Greece. Emerg Infect Dis. 2004;10:963–4. https://doi.org/10.3201/eid1005.030430.
Lipatova I, Paulauskas A, Puraite I, Radzijevskaja J, Balciauskas L, Gedminas V. Bartonella infection in small mammals and their ectoparasites in Lithuania. Microbes Infect. 2015;17:884–8. https://doi.org/10.1016/j.micinf.2015.08.013.
Paziewska A, Harris PD, Zwolinska L, Bajer A, Sinski E. Differences in the ecology of Bartonella infections of Apodemus flavicollis and Myodes glareolus in a boreal forest. Parasitology. 2012;139:881–93. https://doi.org/10.1017/S0031182012000170.
Welc-Faleciak R, Paziewska A, Bajer A, Behnke JM, Siński E. Bartonella spp. infection in rodents from different habitats in the Mazury Lake District, northeast Poland. Vector Borne Zoonotic Dis. 2008;8:467–74. https://doi.org/10.1089/vbz.2007.0217.
Welc-Faleciak R, Bajer A, Behnke JM, Siński E. The ecology of Bartonella spp. infections in two rodent communities in the Mazury Lake District region of Poland. Parasitology. 2010;137:1069–77. https://doi.org/10.1017/S0031182009992058.
Špitalská E, Minichová L, Kocianová E, Škultéty Ľ, Mahríková L, Hamšíková Z, et al. Diversity and prevalence of Bartonella species in small mammals from Slovakia, Central Europe. Parasitol Res. 2017;116:3087–95. https://doi.org/10.1007/s00436-017-5620-x.
Gil H, García-Esteban C, Barandika JF, Peig J, Toledo A, Escudero R, et al. Variability of Bartonella genotypes among small mammals in Spain. Appl Environ Microbiol. 2010;76:8062–70. https://doi.org/10.1128/AEM.01963-10.
Holmberg M, Mills JN, McGill S, Benjamin G, Ellis BA. Bartonella infection in sylvatic small mammals of central Sweden. Epidemiol Infect. 2003;130:149–57. https://doi.org/10.1017/S0950268802008075.
Çelebi B, Karagoz, Alper, Öktem, Mehmet, Çarhan, Ahmet, Matur F, Özkazanc N, Babur C, Kilic S, et al. Bartonella species in wild small mammals in western Black Sea Region of Turkey. Ankara Üniv Vet Fakült Dergisi. 2015;62:183–7. https://doi.org/10.1501/Vetfak_0000002678.
Divari S, Danelli M, Pregel P, Ghielmetti G, Borel N, Bollo E. Biomolecular investigation of Bartonella spp. in wild rodents of two Swiss regions. Pathogens. 2021;10:1331. https://doi.org/10.3390/pathogens10101331.
Buffet J-P, Pisanu B, Brisse S, Roussel S, Félix B, Halos L, et al. Deciphering Bartonella diversity, recombination, and host specificity in a rodent community. PLoS ONE. 2013;8: e68956. https://doi.org/10.1371/journal.pone.0068956.
Harrison A, Bown KJ, Montgomery WI, Birtles RJ. Ixodes ricinus is not an epidemiologically relevant vector of Bartonella species in the wood mouse (Apodemus sylvaticus). Vector Borne Zoonotic Dis. 2012;12:366–71. https://doi.org/10.1089/vbz.2011.0807.
Birtles RJ, Hazel SM, Bennett M, Bown K, Raoult D, Begon M. Longitudinal monitoring of the dynamics of infections due to Bartonella species in UK woodland rodents. Epidemiol Infect. 2001;126:323–9. https://doi.org/10.1017/S095026880100526X.
Telfer S, Clough HE, Birtles LRJ, Bennett M, Carslake D, Helyar S, Begon M. Ecological differences and coexistence in a guild of microparasites: Bartonella in wild rodents. Ecology. 2007;88:1841–9. https://doi.org/10.1890/06-1004.1.
Withenshaw SM, Devevey G, Pedersen AB, Fenton A. Multihost Bartonella parasites display covert host specificity even when transmitted by generalist vectors. J Anim Ecol. 2016;85:1442–52. https://doi.org/10.1111/1365-2656.12568.
Malania L, Bai Y, Osikowicz LM, Tsertsvadze N, Katsitadze G, Imnadze P, Kosoy M. Prevalence and diversity of Bartonella species in rodents from Georgia (Caucasus). Am J Trop Med Hyg. 2016;95:466–71. https://doi.org/10.4269/ajtmh.16-0041.
Meheretu Y, Leirs H, Welegerima K, Breno M, Tomas Z, Kidane D, et al. Bartonella prevalence and genetic diversity in small mammals from Ethiopia. Vector Borne Zoonotic Dis. 2013;13:164–75. https://doi.org/10.1089/vbz.2012.1004.
Gundi VAKB, Kosoy MY, Makundi RH, Laudisoit A. Identification of diverse Bartonella genotypes among small mammals from democratic Republic of Congo and Tanzania. Am J Trop Med Hyg. 2012;87:319–26. https://doi.org/10.4269/ajtmh.2012.11-0555.
Gundi VAKB, Billeter SA, Rood MP, Kosoy MY. Bartonella spp. in rats and zoonoses, Los Angeles, California, USA. Emerg Infect Dis. 2012;18:631–3. https://doi.org/10.3201/eid1804.110816.
Gelling M, Macdonald DW, Telfer S, Jones T, Bown K, Birtles R, Mathews F. Parasites and pathogens in wild populations of water voles (Arvicola amphibius) in the UK. Eur J Wildl Res. 2012;58:615–9. https://doi.org/10.1007/s10344-011-0584-0.
Bitam I, Rolain J-M, Kernif T, Baziz B, Parola P, Raoult D. Bartonella species detected in rodents and hedgehogs from Algeria. Clin Microbiol Infect. 2009;15:102–3. https://doi.org/10.1111/j.1469-0691.2008.02180.x.
Bai Y, Montgomery SP, Sheff KW, Chowdhury MA, Breiman RF, Kabeya H, Kosoy MY. Bartonella strains in small mammals from Dhaka, Bangladesh, related to Bartonella in America and Europe. Am J Trop Med Hyg. 2007;77:567–70. https://doi.org/10.4269/ajtmh.2007.77.567.
Böge I, Pfeffer M, Htwe NM, Maw PP, Sarathchandra SR, Sluydts V, et al. First detection of Bartonella spp. in small mammals from rice storage and processing facilities in Myanmar and Sri Lanka. Microorganisms. 2021;9:658. https://doi.org/10.3390/microorganisms9030658.
Gundi VAKB, Kosoy MY, Myint KSA, Shrestha SK, Shrestha MP, Pavlin JA, Gibbons RV. Prevalence and genetic diversity of Bartonella species detected in different tissues of small mammals in Nepal. Appl Environ Microbiol. 2010;76:8247–54. https://doi.org/10.1128/AEM.01180-10.
Jiyipong T, Jittapalapong S, Morand S, Raoult D, Rolain J-M. Prevalence and genetic diversity of Bartonella spp. in small mammals from Southeastern Asia. Appl Environ Microbiol. 2012;78:8463–6. https://doi.org/10.1128/AEM.02008-12.
Angelakis E, Khamphoukeo K, Grice D, Newton PN, Roux V, Aplin K, et al. Molecular detection of Bartonella species in rodents from the Lao PDR. Clin Microbiol Infect. 2009;15:95–7. https://doi.org/10.1111/j.1469-0691.2008.02177.x.
Bai Y, Kosoy MY, Lerdthusnee K, Peruski LF, Richardson JH. Prevalence and genetic heterogeneity of Bartonella strains cultured from rodents from 17 Provinces in Thailand. Am J Trop Med Hyg. 2009;81:811–6. https://doi.org/10.4269/ajtmh.2009.09-0294.
Castle KT, Kosoy M, Lerdthusnee K, Phelan L, Bai Y, Gage KL, et al. Prevalence and diversity of Bartonella in rodents of northern Thailand: a comparison with Bartonella in rodents from southern China. Am J Trop Med Hyg. 2004;70:429–33. https://doi.org/10.4269/ajtmh.2004.70.429.
Klangthong K, Promsthaporn S, Leepitakrat S, Schuster AL, McCardle PW, Kosoy M, Takhampunya R. The distribution and diversity of Bartonella species in rodents and their ectoparasites across Thailand. PLoS ONE. 2015;10: e0140856. https://doi.org/10.1371/journal.pone.0140856.
Pangjai D, Maruyama S, Boonmar S, Kabeya H, Sato S, Nimsuphan B, et al. Prevalence of zoonotic Bartonella species among rodents and shrews in Thailand. Comp Immunol Microbiol Infect Dis. 2014;37:109–14. https://doi.org/10.1016/j.cimid.2013.12.001.
Saisongkorh W, Wootta W, Sawanpanyalert P, Raoult D, Rolain J-M. “Candidatus Bartonella thailandensis”: a new genotype of Bartonella identified from rodents. Vet Microbiol. 2009;139:197–201. https://doi.org/10.1016/j.vetmic.2009.05.011.
Angelakis E, Lepidi H, Canel A, Rispal P, Perraudeau F, Barre I, et al. Human case of Bartonella alsatica lymphadenitis. Emerg Infect Dis. 2008;14:1951–3. https://doi.org/10.3201/eid1412.080757.
Kosoy M, Mandel E, Green D, Marston E, Childs J. Prospective studies of Bartonella of rodents. Part I. Demographic and temporal patterns in population dynamics. Vector Borne Zoonotic Dis. 2004;4:285–95.
Rizzo MF, Osikowicz L, Cáceres AG, Luna-Caipo VD, Suarez-Puyen SM, Bai Y, Kosoy M. Identification of Bartonella rochalimae in Guinea Pigs (Cavia porcellus) and fleas collected from rural peruvian households. Am J Trop Med Hyg. 2019;101:1276–81. https://doi.org/10.4269/ajtmh.19-0517.
Rubio AV, Ávila-Flores R, Osikowicz LM, Bai Y, Suzán G, Kosoy MY. Prevalence and genetic diversity of Bartonella strains in rodents from northwestern Mexico. Vector Borne Zoonotic Dis. 2014;14:838–45. https://doi.org/10.1089/vbz.2014.1673.
Bai Y, Kosoy MY, Cully JF, Bala T, Ray C, Collinge SK. Acquisition of nonspecific Bartonella strains by the northern grasshopper mouse (Onychomys leucogaster). FEMS Microbiol Ecol. 2007;61:438–48. https://doi.org/10.1111/j.1574-6941.2007.00364.x.
Kamani J, Morick D, Mumcuoglu KY, Harrus S. Prevalence and diversity of Bartonella species in commensal rodents and ectoparasites from Nigeria. West Africa PLOS Negl Trop Dis. 2013;7: e2246. https://doi.org/10.1371/journal.pntd.0002246.
Billeter SA, Borchert JN, Atiku LA, Mpanga JT, Gage KL, Kosoy MY. Bartonella species in invasive rats and indigenous rodents from Uganda. Vector Borne Zoonotic Dis. 2014;14:182–8. https://doi.org/10.1089/vbz.2013.1375.
Mangombi JB, N’dilimabaka N, Lekana-Douki J-B, Banga O, Maghendji-Nzondo S, Bourgarel M, et al. First investigation of pathogenic bacteria, protozoa and viruses in rodents and shrews in context of forest-savannah-urban areas interface in the city of Franceville (Gabon). PLoS ONE. 2021;16:e0248244. https://doi.org/10.1371/journal.pone.0248244.
Diarra AZ, Kone AK, Doumbo Niare S, Laroche M, Diatta G, Atteynine SA, et al. Molecular detection of microorganisms associated with small mammals and their ectoparasites in Mali. Am J Trop Med Hyg. 2020;103:2542–51. https://doi.org/10.4269/ajtmh.19-0727.
Martin-Alonso A, Houemenou G, Abreu-Yanes E, Valladares B, Feliu C, Foronda P. Bartonella spp. in small mammals, Benin. Vector Borne Zoonotic Dis. 2016;16:229–37. https://doi.org/10.1089/vbz.2015.1838.
Halliday JEB, Knobel DL, Agwanda B, Bai Y, Breiman RF, Cleaveland S, et al. Prevalence and diversity of small mammal-associated Bartonella species in rural and urban Kenya. PLoS Negl Trop Dis. 2015;9: e0003608. https://doi.org/10.1371/journal.pntd.0003608.
Bai Y, Kosoy MY, Ray C, Brinkerhoff RJ, Collinge SK. Temporal and spatial patterns of Bartonella infection in black-tailed prairie dogs (Cynomys ludovicianus). Microb Ecol. 2008;56:373–82. https://doi.org/10.1007/s00248-007-9355-6.
de Salvo MN, Hercolini C, Arístegui E, Bruno A, Brambati DF, Cicuttin GL. Bartonella spp. associated with rodents in an urban protected area, Buenos Aires (Argentina). Comp Immunol Microbiol Infect Dis. 2020;72:101515. https://doi.org/10.1016/j.cimid.2020.101515.
Goodrich I, McKee C, Kosoy M. Longitudinal study of bacterial infectious agents in a community of small mammals in New Mexico. Vector Borne Zoonotic Dis. 2020;20:496–508. https://doi.org/10.1089/vbz.2019.2550.
Kosoy M, Murray M, Robert D, Gilmore JR, Bai Y, Gage KL. Bartonella strains from ground squirrels are identical to Bartonella washoensis isolated from a human patient. J Clin Microbiol. 2003;41:645–50. https://doi.org/10.1128/JCM.41.2.645-650.2003.
Gutiérrez R, Morick D, Cohen C, Hawlena H, Harrus S. The effect of ecological and temporal factors on the composition of Bartonella infection in rodents and their fleas. ISME J. 2014;8:1598–608. https://doi.org/10.1038/ismej.2014.22.
Mediannikov O, Aubadie M, Bassene H, Diatta G, Granjon L, Fenollar F. Three new Bartonella species from rodents in Senegal. Int J Infect Dis. 2014;21:335. https://doi.org/10.1016/j.ijid.2014.03.1112.
Kleynhans DJ, Sarli J, Hatyoka LM, Alagaili AN, Bennett NC, Mohammed OB, Bastos ADS. Molecular assessment of Bartonella in Gerbillus nanus from Saudi Arabia reveals high levels of prevalence, diversity and co-infection. Infect Genet Evol. 2018;65:244–50. https://doi.org/10.1016/j.meegid.2018.07.036.
Rocchigiani G, Ebani VV, Nardoni S, Bertelloni F, Bascherini A, Leoni A, et al. Molecular survey on the occurrence of arthropod-borne pathogens in wild brown hares (Lepus europaeus) from Central Italy. Infect Genet Evol. 2018;59:142–7. https://doi.org/10.1016/j.meegid.2018.02.005.
Diagne C, Galan M, Tamisier L, d’Ambrosio J, Dalecky A, Bâ K, et al. Ecological and sanitary impacts of bacterial communities associated to biological invasions in African commensal rodent communities. Sci Rep. 2017;7:14995. https://doi.org/10.1038/s41598-017-14880-1.
Blasdell KR, Perera D, Firth C. High prevalence of rodent-borne Bartonella spp. in urbanizing environments in Sarawak, Malaysian Borneo. Am J Trop Med Hyg. 2019;100:506–9. https://doi.org/10.4269/ajtmh.18-0616.
Gundi VAKB, Taylor C, Raoult D, La Scola B. Bartonella rattaustraliani sp. nov., Bartonella queenslandensis sp. nov. and Bartonella coopersplainsensis sp. nov., identified in Australian rats. Int J Syst Evol Microbiol. 2009;59:2956–61. https://doi.org/10.1099/ijs.0.002865-0.
Obiegala A, Jeske K, Augustin M, Król N, Fischer S, Mertens-Scholz K, et al. Highly prevalent bartonellae and other vector-borne pathogens in small mammal species from the Czech Republic and Germany. Parasit Vectors. 2019;12:332. https://doi.org/10.1186/s13071-019-3576-7.
Kosoy MY, Regnery RL, Tzianabos T, Marston EL, Jones DC, Green D, et al. Distribution, diversity, and host specificity of Bartonella in Rodents from the Southeastern United States. Am J Trop Med Hyg. 1997;57:578–88. https://doi.org/10.4269/ajtmh.1997.57.578.
Karagöz A, Çelebi B, Şisek H, Taner M, Kilic S, Durmaz R, Ertek M. Detection of Bartonella spp. in field mice (Microtus socialis) by culture and PCR. Ankara Üniv Vet Fak Derg. 2013;60:235–9.
Ye X, Li G-w, Yao M-l, Luo W, Su L-q. Study on the prevalence and genotypes of Bartonella species in rodent hosts from Fujian coastal regions. Zhonghua Liu Xing Bing Xue Za Zhi. 2009;30:989–92.
Birtles RJ, Canales J, Ventosilla P, Alvarez E, Guerra H, Llanos-Cuentas A, et al. Survey of Bartonella species infecting intradomicillary animals in the Huayllacallán Valley, Ancash, Peru, a region endemic for human bartonellosis. Am J Trop Med Hyg. 1999;60:799–805. https://doi.org/10.4269/ajtmh.1999.60.799.
Hsieh J-W, Tung K-C, Chen W-C, Lin J-W, Chien L-J, Hsu Y-M, et al. Epidemiology of Bartonella infection in rodents and Shrews in Taiwan. Zoonoses Public Health. 2010;57:439–46. https://doi.org/10.1111/j.1863-2378.2009.01234.x.
Lin EY, Tsigrelis C, Baddour LM, Lepidi H, Rolain JM, Patel R, Raoult D. Candidatus Bartonella mayotimonensis and endocarditis. Emerg Infect Dis. 2010;16:500–3. https://doi.org/10.3201/eid1603.081673.
Márquez FJ, Rodríguez-Liébana JJ, Pachón-Ibáñez ME, Docobo-Pérez F, Hidalgo-Fontiveros A, Bernabeu-Wittel M, et al. Molecular screening of Bartonella species in rodents from south western Spain. Vector Borne Zoonotic Dis. 2008;8:695–700. https://doi.org/10.1089/vbz.2007.0257.
Jardine C, Appleyard G, Kosoy MY, McColl D, Chirino-Trejo M, Wobeser G, Leighton FA. Rodent-associated Bartonella in Saskatchewan, Canada. Vector Borne Zoonotic Dis. 2005;5:402–9. https://doi.org/10.1089/vbz.2005.5.402.
Buffet J-P, Marsot M, Vaumourin E, Gasqui P, Masséglia S, Marcheteau E, et al. Co-infection of Borrelia afzelii and Bartonella spp. in bank voles from a suburban forest. Comp Immunol Microbiol Infect Dis. 2012;35:583–9. https://doi.org/10.1016/j.cimid.2012.07.002.
Matsumoto K, Cook JA, Goethert HK, Telford SR. Bartonella sp. infection of voles trapped from an interior Alaskan site where ticks are absent. J Wildl Dis. 2010;46:173–8. https://doi.org/10.7589/0090-3558-46.1.173.
Morway C, Kosoy M, Eisen R, Montenieri J, Sheff K, Reynolds PJ, Powers N. A longitudinal study of Bartonella infection in populations of woodrats and their fleas. J Vector Ecol. 2008;33:353–64.
Hao L, Yuan D, Guo L, Hou W, Mo X, Yin J, et al. Molecular detection of Bartonella in ixodid ticks collected from yaks and plateau pikas (Ochotona curzoniae) in Shiqu County, China. BMC Vet Res. 2020;16:235. https://doi.org/10.1186/s12917-020-02452-x.
Rao HX, Yu J, Guo P, Ma YC, Liu QY, Jiao M, et al. Bartonella species detected in the plateau pikas (Ochotona curzoiae) from Qinghai Plateau in China. Biomed Environ Sci. 2015;28:674–8. https://doi.org/10.3967/bes2015.094.
Kik MJL, Jaarsma RI, IJzer J, Sprong H, Gröne A, Rijks JM. Bartonella alsatica in wild and domestic rabbits (Oryctolagus cuniculus) in the Netherlands. Microbiol Res. 2021;12:524–7. https://doi.org/10.3390/microbiolres12020036.
Márquez FJ. Molecular detection of Bartonella alsatica in European wild rabbits (Oryctolagus cuniculus) in Andalusia (Spain). Vector Borne Zoonotic Dis. 2010;10:731–4. https://doi.org/10.1089/vbz.2009.0135.
Márquez FJ. Detection of Bartonella alsatica in European wild rabbit and their fleas (Spilopsyllus cuniculi and Xenopsylla cunicularis) in Spain. Parasit Vectors. 2015;8:56. https://doi.org/10.1186/s13071-015-0664-1.
Bai Y, Calisher CH, Kosoy MY, Root JJ, Doty JB. Persistent infection or successive reinfection of deer mice with Bartonella vinsonii subsp. arupensis. Appl Environ Microbiol. 2011;77:1728–31. https://doi.org/10.1128/AEM.02203-10.
Fichet-Calvet E, Jomâa I, Ben Ismail R, Ashford RW. Patterns of infection of haemoparasites in the fat sand rat, Psammomys obesus, in Tunisia, and effect on the host. Ann Trop Med Parasitol. 2000;94:55–68. https://doi.org/10.1080/00034983.2000.11813513.
Tay ST, Mokhtar AS, Zain SNM, Low KC. Isolation and molecular identification of bartonellae from wild rats (Rattus species) in Malaysia. Am J Trop Med Hyg. 2014;90:1039–42. https://doi.org/10.4269/ajtmh.13-0273.
Billeter SA, Colton L, Sangmaneedet S, Suksawat F, Evans BP, Kosoy MY. Molecular detection and identification of Bartonella species in rat fleas from northeastern Thailand. Am J Trop Med Hyg. 2013;89:462–5. https://doi.org/10.4269/ajtmh.12-0483.
Obiegala A, Heuser E, Ryll R, Imholt C, Fürst J, Prautsch L-M, et al. Norway and black rats in Europe: potential reservoirs for zoonotic arthropod-borne pathogens. Pest Manag Sci. 2019;75:1556–63.
Costa F, Porter FH, Rodrigues G, Farias H, de Faria MT, Wunder EA, et al. Infections by Leptospira interrogans, Seoul virus, and Bartonella spp. among Norway rats (Rattus norvegicus) from the urban slum environment in Brazil. Vector Borne Zoonotic Dis. 2014;14:33–40. https://doi.org/10.1089/vbz.2013.1378.
Gundi VAKB, Davoust B, Khamis A, Boni M, Raoult D, La Scola B. Isolation of Bartonella rattimassiliensis sp. nov. and Bartonella phoceensis sp. nov. from European Rattus norvegicus. J Clin Microbiol. 2004;42:3816–8. https://doi.org/10.1128/JCM.42.8.3816-3818.2004.
Winoto IL, Goethert H, Ibrahim IN, Yuniherlina I, Stoops C, Susanti I, et al. Bartonella species in rodents and shrews in the greater Jakarta area. Southeast Asian J Trop Med Public Health. 2005;36:1523–9.
Ellis BA, Regnery RL, Beati L, Bacellar F, Rood M, Glass GG, et al. Rats of the genus Rattus are reservoir hosts for pathogenic Bartonella species: an Old World origin for a New World disease? J Infect Dis. 1999;180:220–4. https://doi.org/10.1086/314824.
Trataris AN, Rossouw J, Arntzen L, Karstaedt A, Frean J. Bartonella spp. in human and animal populations in Gauteng, South Africa, from 2007 to 2009. Onderstepoort J Vet Res. 2012;79:18–25.
Tsai Y-L, Chuang S-T, Chang C-C, Kass PH, Chomel BB. Bartonella species in small mammals and their ectoparasites in Taiwan. Am J Trop Med Hyg. 2010;83:917–23. https://doi.org/10.4269/ajtmh.2010.10-0083.
Dybing NA, Jacobson C, Irwin P, Algar D, Adams PJ. Bartonella species identified in rodent and feline hosts from island and mainland Western Australia. Vector Borne Zoonotic Dis. 2016;16:238–44. https://doi.org/10.1089/vbz.2015.1902.
Harrus S, Bar-Gal GK, Golan A, Elazari-Volcani R, Kosoy MY, Morick D, et al. Isolation and genetic characterization of a Bartonella strain closely related to Bartonella tribocorum and Bartonella elizabethae in Israeli commensal rats. Am J Trop Med Hyg. 2009;81:55–8. https://doi.org/10.4269/ajtmh.2009.81.55.
Brook CE, Bai Y, Yu EO, Ranaivoson HC, Shin H, Dobson AP, et al. Elucidating transmission dynamics and host-parasite-vector relationships for rodent-borne Bartonella spp. in Madagascar. Epidemics. 2017;20:56–66. https://doi.org/10.1016/j.epidem.2017.03.004.
Nesaraj J, Grinberg A, Gedye K, Potter MA, Harrus S. Molecular detection of Bartonella coopersplainsensis and B. henselae in rats from New Zealand. N Zeal Vet J. 2018;66:257–60. https://doi.org/10.1080/00480169.2018.1483781.
Lin J-W, Chen C-Y, Chen W-C, Chomel BB, Chang C-C. Isolation of Bartonella species from rodents in Taiwan including a strain closely related to ‘Bartonella rochalimae’ from Rattus norvegicus. J Med Microbiol. 2008;57:1496–501. https://doi.org/10.1099/jmm.0.2008/004671-0.
Low V, Tan T, Ibrahim J, AbuBakar S, Lim YL. First evidence of Bartonella phoceensis and Candidatus Mycoplasma haemomuris subsp. ratti in synanthropic rodents in Malaysia. Asian Pac J Trop Med. 2020;13:94. https://doi.org/10.4103/1995-7645.275418.
Bown KJ, Ellis BA, Birtles RJ, Durden LA, Lello J, Begon M, Bennett M. New World origins for haemoparasites infecting United Kingdom grey squirrels (Sciurus carolinensis), as revealed by phylogenetic analysis of Bartonella infecting squirrel populations in England and the United States. Epidemiol Infect. 2002;129:647–53. https://doi.org/10.1017/S0950268802007768.
Laakkonen J. Microparasites of three species of shrews from Finnish Lapland. Annal Zoolog Fennici. 2000:37–41.
Jardine C, Waldner C, Wobeser G, Leighton FA. Demographic features of Bartonella infections in Richardson’s ground squirrels (Spermophilus richardsonii). J Wildl Dis. 2006;42:739–49. https://doi.org/10.7589/0090-3558-42.4.739.
Schmitz KM, Foley JE, Kasten RW, Chomel BB, Larsen RS. Prevalence of vector-borne bacterial pathogens in riparian brush rabbits (Sylvilagus bachmani riparius) and their ticks. J Wildl Dis. 2014;50:369–73. https://doi.org/10.7589/2012-11-292.
Bermond D, Heller R, Barrat F, Delacour G, Dehio C, Alliot A, et al. Bartonella birtlesii sp. nov., isolated from small mammals (Apodemus spp.). Int J Syst Evol Microbiol. 2000;50:1973–9. https://doi.org/10.1099/00207713-50-6-1973.
Birtles RJ, Harrison TG, Saunders NA, Molyneux DH. Proposals to unify the genera Grahamella and Bartonella, with descriptions of Bartonella talpae comb. nov., Bartonella peromysci comb. nov., and three new species, Bartonella grahamii sp. nov., Bartonella taylorii sp. nov., and Bartonella doshiae sp. nov. Int J Syst Bacteriol. 1995;45:1–8.
Brenner DJ, O’Connor SP, Winkler HH, Steigerwalt AG. Proposals to unify the genera Bartonella and Rochalimaea, with descriptions of Bartonella quintana comb. nov., Bartonella vinsonii comb. nov., Bartonella henselae comb. nov., and Bartonella elizabethae comb. nov., and to remove the family Bartonellaceae from the order Rickettsiales. Int J Syst Bacteriol. 1993;43:777–86. https://doi.org/10.1099/00207713-43-4-777.
Alsarraf M, Mohallal EM, Mierzejewska EJ, Behnke-Borowczyk J, Welc-Falęciak R, Bednarska M, et al. Description of Candidatus Bartonella fadhilae n. sp. and Candidatus Bartonella sanaae n. sp. (Bartonellaceae) from Dipodillus dasyurus and Sekeetamys calurus (Gerbillinae) from the Sinai Massif (Egypt). Vector Borne Zoonotic Dis. 2017;17:483–94. https://doi.org/10.1089/vbz.2016.2093.
Mangombi JB, N’Dilimabaka N, Medkour H, Banga OL, Tall ML, Ben Khedher M, et al. Bartonella gabonensis sp. nov., a new Bartonella species from savannah rodent Lophuromys sp. in Franceville, Gabon. N Microb N Infect. 2020;38:100796. https://doi.org/10.1016/j.nmni.2020.100796.
Gutiérrez R, Cohen C, Flatau R, Marcos-Hadad E, Garrido M, Halle S, et al. Untangling the knots: co-infection and diversity of Bartonella from wild gerbils and their associated fleas. Mol Ecol. 2018;27:4787–807. https://doi.org/10.1111/mec.14906.
Gutiérrez R, Shalit T, Markus B, Yuan C, Nachum-Biala Y, Elad D, Harrus S. Bartonella kosoyi sp. nov. and Bartonella krasnovii sp. nov., two novel species closely related to the zoonotic Bartonella elizabethae, isolated from black rats and wild desert rodent-fleas. Int J Syst Evol Microbiol. 2020;70:1656–65. https://doi.org/10.1099/ijsem.0.003952.
Breitschwerdt EB, Maggi RG, Cadenas MB, Paiva Diniz PPV, de. A groundhog, a novel Bartonella sequence, and my father’s death. Emerg Infect Dis. 2009;15:2080–6. https://doi.org/10.3201/eid1512.090206.
Dahmani M, Diatta G, Labas N, Diop A, Bassene H, Raoult D, et al. Noncontiguous finished genome sequence and description of Bartonella mastomydis sp. nov. N Microb N Infect. 2018;25:60–70. https://doi.org/10.1016/j.nmni.2018.03.005.
Chomel BB, McMillan-Cole AC, Kasten RW, Stuckey MJ, Sato S, Maruyama S, et al. Candidatus Bartonella merieuxii, a potential new zoonotic Bartonella species in canids from Iraq. PLoS Negl Trop Dis. 2012;6: e1843. https://doi.org/10.1371/journal.pntd.0001843.
Heller R, Riegel P, Hansmann Y, Delacour G, Bermond D, Dehio C, et al. Bartonella tribocorum sp. nov., a new Bartonella species isolated from the blood of wild rats. Int J Syst Bacteriol. 1998;48(4):1333–9. https://doi.org/10.1099/00207713-48-4-1333.
Kordick DL, Swaminathan B, Greene CE, Wilson KH, Whitney AM, O’Connor SP, et al. Bartonella vinsonii subsp. berkhoffii subsp. nov., isolated from dogs; Bartonella vinsonii subsp. vinsonii; and emended description of Bartonella vinsonii. Int J Syst Bacteriol. 1996;46:704–9. https://doi.org/10.1099/00207713-46-3-704.
Schulte Fischedick FB, Stuckey MJ, Aguilar-Setién A, Moreno-Sandoval H, Galvez-Romero G, Salas-Rojas M, et al. Identification of Bartonella species isolated from rodents from Yucatan, Mexico, and isolation of Bartonella vinsonii subsp. yucatanensis subsp. nov. Vector Borne Zoonotic Dis. 2016;16:636–42. https://doi.org/10.1089/vbz.2016.1981.
Bai Y, Kosoy M, Martin A, Ray C, Sheff K, Chalcraft L, Collinge SK. Characterization of Bartonella strains isolated from black-tailed prairie dogs (Cynomys ludovicianus). Vector Borne Zoonotic Dis. 2008;8:1–5. https://doi.org/10.1089/vbz.2007.0136.
Kaewmongkol G, Kaewmongkol S, McInnes LM, Burmej H, Bennett MD, Adams PJ, et al. Genetic characterization of flea-derived Bartonella species from native animals in Australia suggests host–parasite co-evolution. Infect Genet Evol. 2011;11:1868–72. https://doi.org/10.1016/j.meegid.2011.07.021.
Fournier P-E, Taylor C, Rolain J-M, Barrassi L, Smith G, Raoult D. Bartonella australis sp. nov. from kangaroos, Australia. Emerg Infect Dis. 2007;13:1961–2. https://doi.org/10.3201/eid1312.060559.
Celebi B, Anani H, Zgheib R, Carhan A, Raoult D, Fournier P-E. Genomic characterization of the novel Bartonella refiksaydamii sp. isolated from the blood of a Crocidura suaveolens (Pallas, 1811). Vector Borne Zoonotic Dis. 2021. https://doi.org/10.1089/vbz.2020.2626.
Lilley TM, Veikkolainen V, Pulliainen AT. Molecular detection of Candidatus Bartonella hemsundetiensis in bats. Vector Borne Zoonotic Dis. 2015;15:706–8. https://doi.org/10.1089/vbz.2015.1783.
Davoust B, Marié J-L, Dahmani M, Berenger J-M, Bompar J-M, Blanchet D, et al. Evidence of Bartonella spp. in blood and ticks (Ornithodoros hasei) of bats, in French Guiana. Vector Borne Zoonotic Dis. 2016;16:516–9. https://doi.org/10.1089/vbz.2015.1918.
Veikkolainen V, Vesterinen EJ, Lilley TM, Pulliainen AT. Bats as reservoir hosts of human bacterial pathogen, Bartonella mayotimonensis. Emerg Infect Dis. 2014;20:960–7. https://doi.org/10.3201/eid2006.130956.
Qiu Y, Kajihara M, Nakao R, Mulenga E, Harima H, Hang’ombe BM, et al. Isolation of Candidatus Bartonella rousetti and other bat-associated bartonellae from bats and their flies in Zambia. Pathogens. 2020;9:469. https://doi.org/10.3390/pathogens9060469.
Calchi AC, Gaboardi Vultão J, Alves MH, Yogui DR, Desbiez ALJ, Bressianini Amaral R, et al. Multi-locus sequencing reveals a novel Bartonella in mammals from the superorder Xenarthra. Transbound Emerg Dis. 2020;67:2020–33. https://doi.org/10.1111/tbed.13545.
Strong R, Tyzzer EE, Brues CT, Selladors AW, Gastiaburu JC. Verruga peruviana, Oroya fever and uta: preliminary report of the first expedition to South America from the Department of Tropical Medicine of Harvard University. JAMA. 1913;61:1713–6. https://doi.org/10.1001/jama.1913.04350200039013.
Kosoy M, Morway C, Sheff KW, Bai Y, Colborn J, Chalcraft L, et al. Bartonella tamiae sp. nov., a newly recognized pathogen isolated from three human patients from Thailand. J Clin Microbiol. 2008;46:772–5. https://doi.org/10.1128/JCM.02120-07.
Welch DF, Carroll KC, Hofmeister EK, Persing DH, Robison DA, Steigerwalt AG, Brenner DJ. Isolation of a new subspecies, Bartonella vinsonii subsp. arupensis, from a cattle rancher: identity with isolates found in conjunction with Borrelia burgdorferi and Babesia microti among naturally infected mice. J Clin Microbiol. 1999;37:2598–601. https://doi.org/10.1128/JCM.37.8.2598-2601.1999.
Breitschwerdt EB, Kordick DL. Bartonella infection in animals: carriership, reservoir potential, pathogenicity, and zoonotic potential for human infection. Clin Microbiol Rev. 2000;13:428–38. https://doi.org/10.1128/CMR.13.3.428.
Lawson PA, Collins MD. Description of Bartonella clarridgeiae sp. nov. isolated from the cat of a patient with Bartonella henselae septicemia. Med Microbiol Lett. 1996:64–73.
Droz S, Chi B, Horn E, Steigerwalt AG, Whitney AM, Brenner DJ. Bartonella koehlerae sp. nov., isolated from cats. J Clin Microbiol. 1999;37:1117–22. https://doi.org/10.1128/JCM.37.4.1117-1122.1999.
Chomel BB, Molia S, Kasten RW, Borgo GM, Stuckey MJ, Maruyama S, et al. Isolation of Bartonella henselae and Two New Bartonella subspecies, Bartonella koehlerae subspecies boulouisii subsp. nov. and Bartonella koehlerae subspecies bothieri subsp. nov.. from free-ranging Californian mountain lions and bobcats. PLoS ONE. 2016;11:e0148299. https://doi.org/10.1371/journal.pone.0148299.
Eremeeva ME, Gerns HL, Lydy SL, Goo JS, Ryan ET, Mathew SS, et al. Bacteremia, fever, and splenomegaly caused by a newly recognized Bartonella species. N Engl J Med. 2007;356:2381–7. https://doi.org/10.1056/NEJMoa065987.
Mau A, Calchi AC, Bittencourt P, Navarrete-Talloni MJ, Sauvé C, Conan A, et al. Molecular survey and genetic diversity of Bartonella spp. in small Indian mongooses (Urva auropunctata) and their fleas on Saint Kitts, West Indies. Microorganisms. 2021;9:1350. https://doi.org/10.3390/microorganisms9071350.
Bermond D, Boulouis H-J, Heller R, van Laere G, Monteil H, Chomel B, et al. Bartonella bovis Bermond et al. sp. nov. and Bartonella capreoli sp. nov., isolated from European ruminants. Int J Syst Evol Microbiol. 2002;52:383–90. https://doi.org/10.1099/00207713-52-2-383.
Maillard R, Riegel P, Barrat F, Bouillin C, Thibault D, Gandoin C, et al. Bartonella chomelii sp. nov., isolated from French domestic cattle (Bos taurus). Int J Syst Evol Microbiol. 2004;54:215–20. https://doi.org/10.1099/ijs.0.02770-0.
Dahmani M, Sambou M, Scandola P, Raoult D, Fenollar F, Mediannikov O. Bartonella bovis and Candidatus Bartonella davousti in cattle from Senegal. Comp Immunol Microbiol Infect Dis. 2017;50:63–9. https://doi.org/10.1016/j.cimid.2016.11.010.
Rasis M, Rudoler N, Schwartz D, Giladi M. Bartonella dromedarii sp. nov. isolated from domesticated camels (Camelus dromedarius) in Israel. Vector Borne Zoonotic Dis. 2014;14:775–82. https://doi.org/10.1089/vbz.2014.1663.
Maggi RG, Kosoy M, Mintzer M, Breitschwerdt EB. Isolation of Candidatus Bartonella melophagi from human blood. Emerg Infect Dis. 2009;15:66–8. https://doi.org/10.3201/eid1501.081080.
Kosoy M, Bai Y, Enscore R, Rizzo MR, Bender S, Popov V, et al. Bartonella melophagi in blood of domestic sheep (Ovis aries) and sheep keds (Melophagus ovinus) from the southwestern US: cultures, genetic characterization, and ecological connections. Vet Microbiol. 2016;190:43–9. https://doi.org/10.1016/j.vetmic.2016.05.009.
Raya AP, Jaffe DA, Chomel BB, Ota MS, Tsou PM, Davis AZ, et al. Detection of Bartonella species, including Candidatus Bartonella ovis sp. nov., in ruminants from Mexico and lack of evidence of Bartonella DNA in saliva of common vampire bats (Desmodus rotundus) predating on them. Vet Microbiol. 2018;222:69–74. https://doi.org/10.1016/j.vetmic.2018.06.018.
Lozano-Sardaneta YN, Blum-Domínguez S, Huerta H, Tamay-Segovia P, Fernández-Figueroa EA, Becker I, Sánchez-Montes S. Detection of Candidatus Bartonella odocoilei n. sp. in Lipoptena mazamae associated with white-tailed deer in Campeche, Mexico. Med Vet Entomol. 2021. https://doi.org/10.1111/mve.12536.
Dehio C, Lanz C, Pohl R, Behrens P, Bermond D, Piémont Y, et al. Bartonella schoenbuchii sp. nov., isolated from the blood of wild roe deer. Int J Syst Evol Microbiol. 2001;51:1557–65. https://doi.org/10.1099/00207713-51-4-1557.
Laroche M, Berenger J-M, Mediannikov O, Raoult D, Parola P. Detection of a potential new Bartonella species “Candidatus Bartonella rondoniensis” in human biting kissing bugs (Reduviidae; Triatominae). PLoS Negl Trop Dis. 2017;11: e0005297. https://doi.org/10.1371/journal.pntd.0005297.
Medkour H, Lo CI, Anani H, Fenollar F, Mediannikov O. Bartonella massiliensis sp. nov., a new bacterial species isolated from an Ornithodoros sonrai tick from Senegal. N Microb N Infect. 2019;32: 100596. https://doi.org/10.1016/j.nmni.2019.100596.
Kešnerová L, Moritz R, Engel P. Bartonella apis sp. nov., a honey bee gut symbiont of the class Alphaproteobacteria. Int J Syst Evol Microbiol. 2016;66:414–21. https://doi.org/10.1099/ijsem.0.000736.
Mullins KE, Hang J, Jiang J, Leguia M, Kasper MR, Maguiña C, et al. Molecular typing of “Candidatus Bartonella ancashi”, a new human pathogen causing verruga peruana. J Clin Microbiol. 2013;51:3865–8. https://doi.org/10.1128/jcm.01226-13.
Puges M, Ménard A, Berard X, Geneviève M, Pinaquy J-B, Edouard S, et al. An unexpected case of Bartonella alsatica prosthetic vascular graft infection. IDR. 2019;12:2453–6. https://doi.org/10.2147/IDR.S206805.
Jeanclaude D, Godmer P, Leveiller D, Pouedras P, Fournier P-E, Raoult D, Rolain J-M. Bartonella alsatica endocarditis in a French patient in close contact with rabbits. Clin Microbiol Infect. 2009;15(Suppl 2):110–1. https://doi.org/10.1111/j.1469-0691.2008.02187.x.
Raoult D, Roblot F, Rolain J-M, Besnier J-M, Loulergue J, Bastides F, Choutet P. First isolation of Bartonella alsatica from a valve of a patient with endocarditis. J Clin Microbiol. 2006;44:278–9. https://doi.org/10.1128/JCM.44.1.278-279.2006.
Vayssier-Taussat M, Moutailler S, Féménia F, Raymond P, Croce O, La Scola B, et al. Identification of novel zoonotic activity of Bartonella spp., France. Emerg Infect Dis. 2016;22:457–62. https://doi.org/10.3201/eid2203.150269.
Corral J, Manríquez Robles A, Toussaint Caire S, Hernández-Castro R, Moreno-Coutiño G. First report of bacillary angiomatosis by Bartonella elizabethae in an HIV-positive patient. Am J Dermatopathol. 2019;41:750–3. https://doi.org/10.1097/DAD.0000000000001439.
Kosoy M, Bai Y, Sheff K, Morway C, Baggett H, Maloney SA, et al. Identification of Bartonella infections in febrile human patients from Thailand and their potential animal reservoirs. Am J Trop Med Hyg. 2010;82:1140–5. https://doi.org/10.4269/ajtmh.2010.09-0778.
Kandelaki G, Malania L, Bai Y, Chakvetadze N, Katsitadze G, Imnadze P, et al. Human lymphadenopathy caused by ratborne Bartonella, Tbilisi, Georgia. Emerg Infect Dis. 2016;22:544–6. https://doi.org/10.3201/eid2203.151823.
Kerkhoff FT, Bergmans AMC, van DerZee A, Rothova AJCM. Demonstration of Bartonella grahamii DNA in ocular fluids of a patient with neuroretinitis. J Clin Microbiol. 1999;37:4034–8. https://doi.org/10.1128/JCM.37.12.4034-4038.1999.
Breitschwerdt EB, Maggi RG. Bartonella quintana and Bartonella vinsonii subsp. vinsonii bloodstream co-infection in a girl from North Carolina USA. Med Microbiol Immunol. 2019;208:101–7. https://doi.org/10.1007/s00430-018-0563-0.
Bai Y, Kosoy MY, Diaz MH, Winchell J, Baggett H, Maloney SA, et al. Bartonella vinsonii subsp. arupensis in humans, Thailand. Emerg Infect Dis. 2012;18:989–91. https://doi.org/10.3201/eid1806.111750.
Melzi ML, Ferrari GM, D’Adda A, Bovo G, Foresti S, Cavallero A, et al. Hepatic granulomatous lesions caused by systemic Bartonella vinsonii subsp. arupensis infection in a child. Pediatr Infect Dis J. 2015;34:1416–7. https://doi.org/10.1097/INF.0000000000000904.
Fenollar F, Sire S, Raoult D. Bartonella vinsonii subsp. arupensis as an agent of blood culture-negative endocarditis in a human. J Clin Microbiol. 2005;43:945–7. https://doi.org/10.1128/JCM.43.2.945-947.2005.
Acknowledgements
The authors wish to thank Prof. Aharon Oren for providing information on the submission process for Candidatus taxa and updated information on the nomenclatural status of certain Bartonella species.
Funding
VK is funded by the LOEWE Centre DRUID [Novel Drug Targets against Poverty-Related and Neglected Tropical Infectious Diseases (project C2)] and the Robert Koch-Institute, Berlin, Germany (Bartonella Consiliary Laboratory, 1369-354).
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MP and AO organized and drafted the manuscript. AO, MK, VAJK, NK and MP wrote the final version of the manuscript. All the authors read and approved the final manuscript.
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Additional file 1: Table S1.
Worldwide prevalence levels of Bartonella spp. in small mammal species including the detection method.
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Krügel, M., Król, N., Kempf, V.A.J. et al. Emerging rodent-associated Bartonella: a threat for human health?. Parasites Vectors 15, 113 (2022). https://doi.org/10.1186/s13071-022-05162-5
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DOI: https://doi.org/10.1186/s13071-022-05162-5