Bartonella species in small mammals and their potential vectors in Asia

Tawisa Jiyipong, Sathaporn Jittapalapong, Serge Morand, Jean-Marc Rolain

1Research Unit on Infectious and Emerging Tropical Diseases (URMITE), CNRS-IRD-INSERM UMR 7278, IHU Méditerranée Infection, Faculty of Medicine and Pharmacy, Aix-Marseille-University, Marseille, France

2Department of Parasitology, Faculty of Veterinary Medicine, Kasetsart University, Bangkok, Thailand

3Institut Sciences of Evolution, UMR 5554 CNRS-IRD-UM2, CC65, Université de Montpellier 2, F-34095, Montpellier, France

4Center for Agricultural Biotechnology (AG-BIO/PEDRO-CHE), Kasetsart University, Kamphaeng Saen Campus, Nakhon Pathom, 73140, Thailand

5Center of Excellence on Agricultural Biotechnology (AG-BIO/PERDO-CHE), Bangkok 10900, Thailand

6Center of Advanced Studies for Agriculture and Food, KU Institute for Advanced Studies, Kasetsart University, Bangkok 10900, Thailand (CASAF, NRU-KU, Thailand)

7Walai Rukhavej Botanical Research Institute, Mahasarakham University, Mahasrakham, Thailand

Bartonella species in small mammals and their potential vectors in Asia

Tawisa Jiyipong1,4,5,6, Sathaporn Jittapalapong2,6, Serge Morand3,7, Jean-Marc Rolain1*

1Research Unit on Infectious and Emerging Tropical Diseases (URMITE), CNRS-IRD-INSERM UMR 7278, IHU Méditerranée Infection, Faculty of Medicine and Pharmacy, Aix-Marseille-University, Marseille, France

2Department of Parasitology, Faculty of Veterinary Medicine, Kasetsart University, Bangkok, Thailand

3Institut Sciences of Evolution, UMR 5554 CNRS-IRD-UM2, CC65, Université de Montpellier 2, F-34095, Montpellier, France

4Center for Agricultural Biotechnology (AG-BIO/PEDRO-CHE), Kasetsart University, Kamphaeng Saen Campus, Nakhon Pathom, 73140, Thailand

5Center of Excellence on Agricultural Biotechnology (AG-BIO/PERDO-CHE), Bangkok 10900, Thailand

6Center of Advanced Studies for Agriculture and Food, KU Institute for Advanced Studies, Kasetsart University, Bangkok 10900, Thailand (CASAF, NRU-KU, Thailand)

7Walai Rukhavej Botanical Research Institute, Mahasarakham University, Mahasrakham, Thailand

PEER REVIEW

Peer reviewer

Dr. Hossein Ghalehnoei, University of Medical Science, Tehran, Iran.

Tel: +989385518026, E-mail: hossein. ghalehnoei58@gmail.com

Co-reviewers: Misael Chinchilla, San José, Costa Rica,

Comments

This is a good research about the presence of various species of Bartonella and its role at causing different infections. The consideration of authors to various reservoirs of this bacteria in animals that a little have been already surveyed is interesting. Diagnostic tests referred in this article are very useful.

Details on Page 764

In this article, authors review the current knowledge of Bartonella infection in small mammals including rodents, insectivores, bats and exotic small mammal pets and their vectors in Asia. Species of Bartonella are Gram-negative intracellular bacteria that infect erythrocytes of various mammalian and non-mammalian animals and mainly transmitted by blood sucking arthropod vectors. The genus Bartonella includes several species of important human diseases with severe clinical signs. Several new Bartonella species were isolated from rodents and other small mammals, and from human patients in Asia. Bartonella species are identified using standard polymerase chain reaction amplification and a sequencing targeting two housekeeping genes (gltA and rpoB) and the internal transcribed spacer fragment. Authors also discuss the implications in term of potential emerging zoonotic diseases.

Bartonella, Small mammals, Rodents, Shrews, Asia

1. Introduction

Member of the genusBartonellaare fastidious, hemotropic, Gram-negative and aerobic bacilli bacteria belonging to the class Alphaproteobacteria. Several species have been implicated in causing human diseases, ranging with short-term fever to severe endocarditis. Five species are known to be causative of significant human diseases:Bartonella bacilliformis(B. bacilliformis) is the causative agent of Oroya fever and verruga peruana (Peruvian wart);Bartonella quintana(B. quintana) is the causative agent of trench fever;Bartonella henselae(B. henselae) is the causative agent of cat-scratch disease[1-3]. Additionally, several species have been described as coincident zoonotic infection agents includingBartonella alsatica(B. alsatica) [4],Bartonella koehlerae(B. koehlerae)[5],Bartonella vinsoniisubsp.berkhoffii(B. vinsoniisubsp.berkhoffii)[6,7],Bartonella tamiae(B. tamiae)[8],Bartonella rochalimae(B. rochalimae) [9],Bartonella washoensis(B. washoensis)[10] andCandidatus Bartonella mayotimonensis[11].

Bartonellaspecies parasitize the erythrocytes, endothelial cells, monocytes and dendritic cells of mammals[12,13]. Additionally, aBartonellaspecies has been described in loggerhead sea turtle[14]. Bacteria of the genusBartonellaare widespread in domestic and wild animals and are transmitted by a great variety of bloodsucking arthropods including fleas, mites, sand flies and ticks[15,16]. Since 1990s, numerous studies have demonstrated that several mammals such as cats, dogs, rabbits and rodents are potential reservoir hosts ofBartonella. Until now, new host species such as insectivores, bats and exotic pets are continually added in the reservoir hosts’ list. This review provides an update of reservoir host species focusing on small mammals, their potential vectors and case reports ofBartonellainfection in Asia, a hotspot of emerging infectious diseases[17,18]. Hosts such as cats, dogs, and rabbits have been excluded from this review since several review articles have been already written on these reservoir hosts[19,20].

2. Taxonomy and bacteriology of Bartonella

Bacteria of the genusBartonellabelong to the family Bartonellaceae, order Rhizobiales, class Alphaproteobacteria, and phylum Proteobacteria.Bartonellaare closely related withBrucellaspecies andAgrobacterium tumefaciens.Bartonellagenus includes a large diversity ofBartonellaspecies, which were identified from different host species. Since the development of more efficient molecular tools for detection, genetic criteria and species identification are greatly improved[21], and the description of newBartonellaspecies has rapidly increased over the last 10 years and is still continually growing. The genus currently contains more than 30 species and 3 subspecies includingB. alsatica,Bartonella australis,B. bacilliformis,Bartonella birtlesii(B. birtlesii),Bartonella bovis(B. bovis),Bartonella capreoli(B. capreoli),Bartonella chomelii,Bartonella coopersplainsensis(B. coopersplainsensis),Bartonella clarridgeiae(B. clarridgeiae),Bartonella doshiae(B. doshiae),Bartonella durdenii,Bartonella grahamii(B. grahamii),B. henselae,Bartonella japonica(B. japonica),B. koehlerae,Bartonella melophagi,Bartonella phoceensis(B. phoceensis),Bartonella queenslandensis(B. queenslandensis),Bartonella quintana(B. quintana),Bartonella rattaustraliani(B. rattaustraliani),Bartonella rattimassiliensis(B. rattimassiliensis),B. rochalimae,Bartonella schoenbuchensis,Bartonella silvatica(B. silvatica),Bartonella silvicola,B. tamiae, Bartonella taylorii(B. taylorii), Bartonella tribocorum(B. tribocorum), Bartonella vinsoniisubsp.arupensis(B. vinsoniisubsp.arupensis), B. vinsoniisubsp.berkhoffii,Bartonella vinsoniisubsp.vinsonii(B. vinsoniisubsp.vinsonii),B. washoensis,CandidatusBartonella antechini,Candidatus Bartonella mayotimonensis,CandidatusBartonella thailandensis(Table 1). Of these, several species may cause either asymptomatic or mild diseases or severe diseases. Bacteria from this genus are fastidious to growin vitro. The culture on blood agar requires 7 to 45 d in primary isolation. Microscopically, theBartonellaspecies are Gram-negative bacilli. SeveralBartonellaspecies are flagellate,B. bacilliformis,B. bovisandB. clarridgeiae[22,23].

Table 1 List of the currently known described species of Bartonella.

3. Bartonella genomes

The genome sizes ofBartonellaspecies range from 1.5 to 2.5 Mb. SeveralBartonellaspecies includingB. bacilliformis,B. birtlesii,B. clarridgeae,B. grahamii,B. henselae,B. quintana,B. rattimassiliensis,B. rattaustralianiandB. tribocorumwere completely sequenced and two species (B. grahamiiandB. tribocorum) contain plasmid. The first genomes have been described forB. henselaeandB. quintanawith 1.9 and 1.6 Mb, respectively[24], followed by the sequencing of the genomes ofB. bacilliformis(1.4 Mb) (the Institute for Genomic Research, unpublished),B. clarridgeiae(1.5 Mb)[25],B. grahamii(2.3 Mb)[26],B. tribocorum(2.6 Mb)[27],B. rattismassiliensis(2.0 Mb)[28],B. rattaustraliani(2.1 Mb)[29],B. birtlesii(1.8 Mb)[30] andB.quintina(1.6 Mb)[31] among others. The guanine-cytosine content ofBartonellaspecies range from 38.5 mol% forB. quintanato 41.1 mol% forB. vinsonii[2]. Additionally, some species such asB. bacilliformis,B. henselae,B. quintanaandB. vinsoniisubsp.berkhoffiihave been shown to contain phage[32]. The phage particles fromB. bacilliformisandB. vinsoniisubsp. berkhoffiiwere tailed, whereas those fromB. henselaeandB. quintanalacked tails, but all contained 14 kb linear, double-stranded DNA, packaged in a round to head.

To date,Bartonellaspecies are identified using standard polymerase chain reaction (PCR) amplification and a sequencing targeting two housekeeping genes (gltA and rpoB) and the internal transcribed spacer fragment[2].

4. Hosts and reservoirs

Bartonellaspecies may show either low specificity with some species infecting several different host species, while some other species show high specificity by infecting a single host. For example,B. bovisgenerally infects only one ruminant species and is seldom associated with other animals. The prevalence ofBartonellain both wild and domestic mammals has been studied in many different countries. To date, several animal species have been reported as a potential reservoir hosts, such as cats, dogs, rabbits, ruminants, monkeys, marsupials, marine mammals, bats, insectivores and rodents[19,33].

4.1. Rodents

Wild rodents are known to be important reservoir hosts of various pathogens, which are causative of human illnesses including Bartonellosis. Of the current species of the genusBartonella, fifteen species includingB. birtlesii,Bartonella elizabethae (B. elizabethae),B. coopersplainsensis,B. doshiae,B. grahamii,B. japonica,B. phoceensis,B. queenslandensis,B. rattaustraliani,B. rattimassiliensis,B. silvatica,B. taylorii,B. tribocorum,B. vinsoniisubsp.arupensis, B. vinsoniisubsp.vinsonii,B. washoensishave been isolated from various rodent species[2]. Of these,B. birtlesii,B. elizabethae,B. grahamii, andB. washoensisare causative agent of human illnesses.

In Asia, the occurrence ofBartonellainfection in rodent populations have been reported in several countries including China, Japan, Taiwan, Lao PDR, Cambodia, Thailand, Indonesia, Bangladesh and Israel.Bartonellais present in most surveyed rodent populations, with an overall prevalence in the sites investigated ranging from 6% in Korea[34] to 47% in China[35]. Table 2 summarizesBartonellaspecies, host species and geographic distribution ofBartonellain Asia.Bartonellainfections are highly prevalent in rodents in China, Korea, Japan, Russia and Taiwan ranging from 8.6% to 82.3%. SeveralRattusspecies have been found as highly infected including the house ratRattus tanezumi (R. tanezumi). Several species of thegeneraApodemus,Eothenomys,MusandMyodeshave also been shown to hostBartonella. A high diversity ofBartonellaspecies was observed from rodents in this region includingB. elizabethae,B. grahamii,B. queenslandensis,B. phoceensis,B. rattimassiliensis,B. taylorii, B. tribocorumand unknown species.

Table 2 Bartonella infection and host species in East Asia.

continued Table 2

In Southeast Asia,Bartonellaspecies have been investigated from rodents in Indonesia, Lao PDR, Cambodia and Thailand[36-40] (Table 3). Again, the genusRattusappears to be the more prevalent rodent genus followed by the generaBandicotaandMus. In South and West Asia, studies ofBartonellain rodents are more limited (Table 4).

Altogether, it appears thatB. coopersplainsensisis mainly found inBandicotaspecies [Bandicota indica(B. indica) andBandicota savilei(B. savilei)] andR. tanezumi;B. elizabethaeinApodemus agrariusandRattusspecies [Rattus rattus(R. rattus) andR. tanezumi];B. grahamiiinRattus norvegicus;B. queenslandensisinMusspecies [Mus cookii(M. cookii),B. phoceensisinR. tanezumi,B. rattimassiliensisinM. cookiiandR. tanezumi;B. rochalimaeinMus cervicolor;B. silvaticainClethrionomys rufocanus;B. tayloriiinC. rufocanus;B. tribocoruminApodemusspecies (A. chevrieri,A. latronum) and inRattusspecies (R. tanezumi,Rattus norvegicus);B. washoensisinPachyuromys duprasi.

4.2. Shrews

Several shrew species live in the domestic areas or peridomestic environments such as agricultural areas. Isolation ofBartonellafrom shrews has been carried out in Asia and North America. In Asia, mostBartonellainfections in shrews have been described in East Asia (Korea and Taiwan) and South Asia (Bangladesh and Nepal)[41-43]. In Southeast Asia, the prevalence ofBartonellain shrews has been reported inSattus murinusin Indonesia[37] (Table 3). Potential new species ofBartonellahas been recently observed inSattus murinusin Cambodia[36].

Finally, it appears thatSattus murinusis a main host forB. elizabethae,B. phoceensis,B. rattimassiliensisandB. tribocorum, althoughCrocidura attenuatais found infected with high prevalence byB. rattimassiliensisandB. tribocorum.

4.3. Bats

The knowledge ofBartonellain bats is still scarce, with only few studies published concerning bats from Asia[44]. Studies on bats and their arthropod vectors havedemonstrated that bats were infected with unknownBartonellaspecies[45]. Another study found new putative species in bats from Kenya[46]. In Asia, reports are even scarcer.Bartonellainfection in bat has been described in Taiwan[47]. Six blood samples ofMiniopterus schreibersiiwere positive with new putativeBartonellaspp. with high prevalence (42.9%, Table 2).

Table 3 Bartonella infection and host species in Southeast Asia.

4.4. Exotic pets

Exotic pets are wildlife that are traded around the world, with important illegal trafficking, and have been (and still being) imported into many countries. The illegal trade without quarantine may cause the dissemination of infectious diseases. However, there are little data onprevalence of infection withBartonellaspp. from exotic small mammal pets in Asia (Table 2). Among them, a study reported that several exotic species in Japan were infected withBartonellaspp. with quite high prevalence[48].

Table 4 Bartonella infection and host species in South and West Asia.

Table 5 Species of Bartonella detected on arthropod vectors from rodents and shrews in Asia.

4.5. Vectors

Several blood-sucking arthropods including fleas, mites, sandflies and ticks have been reported as potential vectors transmittingBartonellaamong animals and between animals and humans.

Of the several blood-sucking arthropods, fleas are the key vectors ofBartonellainfection. Several studies have suggested that fleas, especiallyXenopsylla cheopis, are potential vectors in rodents (Table 5). Ticks, mites and lice are also potential vectors forBartonellainfections inrodents. Epidemiological surveys ofBartonellainfection in ticks, mites and lice have been done in Korea, Taiwan and Thailand[16,34,42,49].

Table 6 Case reports of Bartonella infection in Asia.

6. Zoonotic diseases and case reports in Asia

Bartonellaspecies are important zoonotic bacteria with increasing array of emerging infections in humans and animals. Bartonellosis has been described in Asia. Possible routes of transmission are contacts with infected animals or blood-sucking arthropod via their feces. FourBartonellaspecies includingB. henselae,B. quintana,B. elizabethaeandB. tamiaehave been reported as causative agents of several human diseases in Asia (Table 6). However, few cases of human infections withBartonellabacteria of rodent origins have been reported. The first case ofBartonellaendocarditis in Thailand was found in a 57-year-old male poultry farmer in Khon Kaen province, where the source of pathogen was a cat.B. tamiaewas isolated from three febrile patients in Thailand[8]. In another report, several farmers were supposed to be exposed to infected rodents at home or fields[50]. Recently, four patients were found infected byB. vinsoniiin Northern and Northeastern Thailand, with dogs and rats supposed to be reservoirs[51]. Additional serological studies evidenced exposure to rodentBartonellaspp. in Thailand but also in Nepal[52,53]. However, to date, onlyB. elizabethaewas found in rodent surveys, where the most common rodents were murid fromApodemusspp. andRattusspp. (and particularly the commensalR. rattusandR. tanezumi).

7. Perspectives

The diversity ofBartonellaspecies is far from being known as the recent study of Jiyiponget al. emphasized on three new putative species[36]. Indeed, Southeast Asia is a hotspot of mammal species[54] and a diversification centre for several rodent families. Two-thirds of living rodent species belongs to the family Muridae[55], which also represents most of the rodents found in Southeast Asia with 35 species[56]. It appears that less than 50% of these murid species have been investigated for the presence ofBartonellaspecies (Table 3). The knowledge is even poorer for shrews and bats. This emphasizes the need to increase the screening, detection and characterization ofBartonellain small mammals[57].

SinceBartonellaspecies may be transmitted to humans by ticks, fleas and lice, surveys ofBartonelladistribution within arthropods are needed. In particular, the population changes of these vectors ofBartonellain relation to the impacts of habitat and land-use changes should be better investigated[57].

Rodents, shrews and bats live in a wide range of habitats that are frequented by humans[58], which warrants further investigations on the transmission ecology ofBartonellain order to improve prevention ofBartonellainfections. Identification of risky habitats for human transmission is needed to develop a surveillance strategy, which could be done only after the improvement of our knowledge on the diversity ofBartonellain small mammals and in their arthropod vectors.

This review by giving up-to-date list of reservoirs will help develop a strategy of reservoirs, vectors and habitatsprone to be sources of outbreaks and/or emergingBartonellainfections in humans.

Conflict of interest statement

We declare that we have no conflict of interest.

Acknowledgements

The study was supported by the French ANR CERoPath project (number ANR 07 BDIV 012) (www.ceropath.org), the French ANR BiodivHealthSEA project (number ANR 11 CPEL 002) (www.biodivhealthsea.org), the Infectiopole Sud and the Center of Excellence on Agricultural Biotechnology (Science and Technology Postgraduate Education and Research Development Office, Office of Higher Education Commission, Ministry of Education) (AG-BIO/PERDO-CHE). Part of this research was also funded by the Center of Advanced Studies for Agriculture and Food, Institute for Advanced Studies, Kasetsart University. We thank the editor and a reviewer for helpful comments.

Comments

Background

Bartonellais an important bacteria that can make various infections in different animals specially humans. This bacteria has various hosts and it is transmitted by several vectors. Species ofBartonellaare Gram-negative intracellular bacteria that infects erythrocytes of various mammalian and non-mammalian animals and mainly transmitted by blood-sucking arthropod vectors.

Research frontiers

This is a review article aboutBartonellainfection in small mammals including rodents, insectivores, bats and exotic small mammal pets and their vectors in Asia. This article dicusses the present species ofBartonellain animals cited.

Related reports

This is a review article and it is based on various reports that are already reported. Various articles mentioned role of different species ofBartonellain making infections in animals (mammals and non-mammals).Bartonellain different animals have been recognized.

Innovations and breakthroughs

This review article investigates various species ofBartonellain animals that already a little have been studied and can offer good information about the role ofBartonellaat causing infection in animals cited.

Applications

This review article surveys prevalence of various species ofBartonellain different areas of Asia. Informations offered in this article can be useful for more studies in future.

Peer review

This is a good research about the presence of various species ofBartonellaand its role at causing different infections. The consideration of authors to various reservoirs of this bacteria in animals that a little have been already surveyed is interesting. Diagnostic tests referred in this article are very useful.

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10.12980/APJTB.4.2014C742

*Corresponding author: Jean-Marc Rolain, Research unit on infectious and emerging tropical diseases (URMITE) CNRS-IRD-INSERM UMR 7278, IHU Méditerranée Infection, Faculty of Medicine and Pharmacy, Aix-Marseille-University, Marseille, France.

E-mail: jean-marc.rolain@univ-amu.fr

Foundation Project: Supported by the French ANR CERoPath project (number ANR 07 BDIV 012) and the French ANR BiodivHealthSEA project (number ANR 11 CPEL 002).

Article history:

Received 28 Dec 2013

Received in revised form 20 Feb, 2nd revised form 3 Apr, 3rd revised form 20 Apr 2014

Accepted 20 May 2014

Available online 14 Sep 2014