Asian Pac J Trop Biomed 2014; 4(10): 757-767 757

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Document heading doi:10.12980/APJTB.4.2014C742 2014 by the Asian Pacific Journal of Tropical Biomedicine. All rights reserved. 襃 species in small mammals and their potential vectors in Asia

1,4,5,6 2,6 3,7 1 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

PEER REVIEW ABSTRACT

Peer reviewer Bartonella In this article, authors review the current knowledge of infection in small mammals Dr. Hossein Ghalehnoei, University of including rodents,Bartonella insectivores, bats and exotic small mammal pets and their vectors in Asia. Medical Science, Tehran, Iran. Species of are Gram-negative intracellular that infect erythrocytes of various +989385518026 Tel: , E-mail: hossein. mammalian and non-mammalianBartonella animals and mainly transmitted by blood sucking arthropod 58 ghalehnoei @gmail.com vectors. The genus includesBartonella several species of important human diseases with C M C S o-reviewers:é isael hinchilla, an severe clinical signs. Several new speciesBartonella were isolated from rodents and other small Jos , Costa Rica, mammals, and from human patients in Asia. species are identified using standard ( A Comments polymerase chain reaction amplification and a sequencing targeting two housekeeping genes glt and rpoB) and the internal transcribed spacer fragment. Authors also discuss the implications in This is a good research about the term of potential emerging zoonotic diseases. presenceBartonella of various species of 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. KEYWORDS Bartonella Diagnostic tests referred in this article , Small mammals, Rodents, Shrews, Asia are very useful. Details on Page 764

1. Introduction B. bacilliformis ( ) is the causative ( ) Bartonella agentBartonella of Oroya quintana fever andB. quintanaverruga peruana Peruvian wart ; ( ) Member of the genus are fastidious, is theB. henselaecausative agent hemotropic, Gram-negative and aerobic bacilli bacteria of ; ( ) is the belonging to the class . Several species causative agent of cat-scratch disease[1-3]. Additionally, have been implicated in causing human diseases, ranging several species have been describedBartonella as alsatica coincident B. alsaticazoonotic ( ) with short-term fever to severe endocarditis. Five species infectionBartonella agents koehlerae including B. koehlerae Bartonella vinsonii are known to be causative of significant human diseases: [4], ( )[5],

C J M R R * orresponding author: ean- arc olain, esearch unit on infectiousé andé emerging Article history: tropical diseases (URMITE) CNRS-IRD-INSERM UMR 7278, IHU M diterran e Infection, Received 28 Dec 2013 Faculty of Medicine and Pharmacy, Aix-Marseille-University, Marseille, France. Received in revised form 20 Feb, 2nd revised form 3 Apr, 3rd revised form 20 Apr 2014 E-mail: [email protected] Accepted 20 May 2014 Foundation Project: Supported by the French ANR CERoPath project (number ANR Available online 14 Sep 2014 07 BDIV 012) and the French ANR BiodivHealthSEA project (number ANR 11 CPEL 002). Tawisa Jiyipong et al./Asian Pac J Trop Biomed 2014; 4(10): 757-767 758 berkhoffii B. vinsonii berkhoffii Bartonella ( )[6,7] tamiaesubsp. B. tamiae Bartonella subsp. rochalimae B. ,rochalimae or mild diseases or severe indiseases. vitro Bacteria from this ( )[8] ( ) Bartonella washoensis, B. washoensis Candidatus genus are fastidious to grow . The culture on blood [9], ( )[10] and agar requires 7 to 45 d in primary isolation. Microscopically, Bartonella mayotimonensis[11] Bartonella Bartonella . Bartonellathe species are Gram-negativeB. bacilliformis bacilli. B.Several bovis species parasitize the erythrocytes, endothelial species are flagellate, , [12,13] B. clarridgeiae[22,23] cells, monocytesBartonella and dendritic cells of mammals . and . Additionally, a species has been described in Table 1 [14] Bartonella Bartonella. loggerhead sea turtle . Bacteria of the genus List of the currently known described species of Bartonella are widespread in domestic and wild animals and are species First detection Country Reference B. alsatica Wild rabbit France [59] transmitted by a great variety of bloodsucking arthropods B. australis [15,16] Gray kangaroo Australia [60] including , , sand flies and ticks . Since 1990s, B. bacilliformis Human Europe [61] numerous studies have demonstrated that several mammals B. birtlesii Mouse German [62] such as cats, dogs, rabbits and rodents are potential reservoir B. bovis Bartonella Cow France [62] B. capreoli hosts of . Until now, new host species such as Deer France [63] B. chomelii insectivores, bats and exotic pets are continually added in Domestic cattle France [64] ’ B. clarridgeiae T Cat USA [65] the reservoir hosts list. his review provides an update of B. coopersplainsensis Rat Australia [66] reservoir host species focusing on small mammals, their B. doshiae Bartonella Field vole United Kingdom [67] potential vectors and case reports of infection in B. durdenii S USA Asia, a hotspot of emerging infectious diseases[17,18]. Hosts quirrel unpublished data B. elizabethae Human USA [68] B. grahamii such as cats, dogs, and rabbits have been excluded from Bank vole United Kingdom [67] B. henselae this review since several review articles have been already Cat USA [69] B. japonica written on these reservoir hosts[19,20]. Mouse Japan [70] B. koehlerae Cat USA [71] B. melophagi Sheep unpublished data B merieuxii 2. and bacteriology of Bartonella Canid Irak [72] B. peromysci Mouse [67] B. phoceensis Wild rat France [73] Bartonella B. queenslandensis Bacteria of the genus belong to the Rat Australia [66] B. quintana family Bartonellaceae, order Rhizobiales, class Human [74] Bartonella B. rattaustraliani Rat Australia [66] Alphaproteobacteria, and phylum . B. rattimassiliensis Brucella Agrobacterium Rat France [73] are closely related with species and B. rochalimae tumefaciens Bartonella Human USA [9] . genus includes a large diversity of B. schoenbuchensis Bartonella Deer German [75] B. silvatica species, which were identified from different Mouse Japan [70] B. silvicola host species. Since the development of more efficient Bat unpublished data B. talpae molecular tools for detection, genetic criteria and species Mole [59] B. tamiae [21] Human Thailand [6] identification are greatly improved , and the description B. taylorii Bartonella Mouse United Kingdom [67] of new species has rapidly increased over the B. tribocorum Rat France [76] last 10 years and is still continually growing. The genus B. vinsonii arupensis subsp. Cattle [77,78] 30 3 B. vinsonii berkhoffii currently contains more than species and subspecies subsp. Dog [79] B. alsatica Bartonella australis B. bacilliformis B vinsonii vinsonii including , , , . subsp. Vole [80] Bartonella birtlesii B. birtlesii Bartonella bovis B. bovis B. volans ( ), ( ), Squirrel USA unpublished data Bartonella capreoli B. capreoli Bartonella chomelii B. washoensis ( ) H USA Bartonella coopersplainsensis B., coopersplainsensis , uman unpublished data ( ) Bartonella clarridgeiae B. clarridgeiae Bartonella, ( ) doshiae B. doshiae Bartonella durdenii, Bartonella ( ) grahamii B. grahamii, B. henselae Bartonella, japonica B. 3. Bartonella ( ) ( japonica B. koehlerae, Bartonella, melophagi Bartonella ) phoceensis, B. phoceensis, Bartonella queenslandensis, Bartonella ( ) B. queenslandensis Bartonella, quintana B. quintana The sizes ofBartonella species range fromB. ( ) ( ) 1 5 2 5 Bartonella rattaustraliani, B. rattaustraliani Bartonella, bacilliformis. to . Mb.B. S everalbirtlesii B. clarridgeae speciesB. includinggrahamii B. ( ) rattimassiliensis B. rattimassiliensis B. rochalimae, henselae B. quintana, B. ,rattimassiliensis , B. rattaustraliani, ( ) Bartonella schoenbuchensis Bartonella, silvatica B., B. tribocorum, , , ( silvatica Bartonella silvicola, B. tamiae, Bartonella and B. grahamii were completelyB. tribocorum sequenced and two ) ( ) taylorii B., taylorii , , B. tribocorum , species and containB. henselae plasmid. ( ) ( ) Bartonella vinsonii arupensis B. vinsonii B.The quintana first genomes have been described for and ( 1 9 1 6 [24] arupensis , B. vinsonii subsp. berkhoffii Bartonella vinsoniisubsp. with . and . Mb, respectivelyB. bacilliformis, followed ) (1 4 vinsonii B. vinsonii subsp. vinsonii, B. washoensis by the sequencing of the genomes of . ( ) ) ( ) Candidatussubsp. Bartonella antechini subsp. Candidatus, Bartonella, MB.b clarridgeiae the Institute for GenomicB. grahamiiResearch, unpublishedB., (1 5 )[25] (2 3 )[26] mayotimonensis Candidatus Bartonella, thailandensis tribocorum . MbB. rattismassiliensis, . Mb , B. ( (2 6 )[27] (2 0 )[28] , Table rattaustraliani. Mb , B. birtlesii . Mb , B. 1). Of these, several species may cause either asymptomatic (2.1 Mb)[29], (1.8 Mb)[30] and Tawisa Jiyipong et al./Asian Pac J Trop Biomed 2014; 4(10): 757-767 759 quintina (1 6 )[31] [19,33] Bartonella. Mb among others. The guanine-cytosineB. bats, insectivores and rodents . content of species range from 38.5 mol% for quintana B. vinsonii 4.1. Rodents to 41.1 mol% for [2]. Additionally, some B. bacilliformis B. henselae B. quintana species such as , , B. vinsonii berkhoffii and subsp. have been shown to contain Wild rodents are known to be important reservoir hosts B. bacilliformis B. of various pathogens, which are causative of human phage[32]. The phage particles from and vinsonii . berkhoffii illnesses including . Of the current species of subsp were tailed, whereas those from Bartonella B. birtlesii B. henselae B. quintana the genus , fifteen species including , and lacked tails, but all contained (B. elizabethae) B. coopersplainsensis , , 14 kb linear, double-stranded DNA, packaged in a round to B. doshiae B. grahamii B. japonica B. phoceensis B. , , , , head. queenslandensis B. rattaustraliani B. rattimassiliensis Bartonella , , , To date, species are identified using standard B. silvatica B. taylorii B. tribocorum B. vinsonii , , , subsp. polymerase chain reaction (PCR) amplification and a arupensis, B. vinsonii vinsonii B. washoensis subsp. , have sequencing targeting two housekeeping genes (gltA and B. been isolated from various rodent species[2]. Of these, rpoB) and the internal transcribed spacer fragment[2]. birtlesii B. elizabethae B. grahamii B. washoensis , , , and are causative agent of human illnesses.Bartonella 4. Hosts and reservoirs In Asia, the occurrence of infection in rodent populations have been reported in several countries Bartonella including China, Japan, Taiwan, Lao PDR, Cambodia, species may show either low specificity with Bartonella Thailand, Indonesia, Bangladesh and Israel. some species infecting several different host species, while is present in most surveyed rodent populations, with an some other species show high specificity by infecting a B. bovis overall prevalence in the sites investigated ranging from single host. For example, generally infects only 6% in Korea[34] to 47% in China[35]. Table 2 summarizes one species and is seldom associated with other Bartonella Bartonella species, host species and geographic distribution animals. The prevalence of in both wild and Bartonella Bartonella of in Asia. infections are highly domestic mammals has been studied in many different prevalent in rodents in China, Korea, Japan, Russia and countries. To date, several animal species have been Rattus Taiwan ranging from 8.6% to 82.3%. Several species reported as a potential reservoir hosts, such as cats, dogs, have been found as highly infected including the house rabbits, , monkeys, marsupials, marine mammals, Rattus tanezumi (R. tanezumi) rat . Several species of the Table 2 Bartonella infection and host species in East Asia. Bartonella Diagnostic test Type of animal Country infection Host species and prevalence of each species Reference PCR Culture Rodent Shrew Bat Exotic pet B. elizabethae Rattus tanezumi flavipectus China + + subsp. , 41.4% (24/58) + ---[35] B. grahamii Rattus norvegicus + + , 42.9% (3/7) + ---[35] B. tribocorum Apodemus chevrieri + + , 62.5% (20/32) + ---[35] Apodemus draco , 33.3% (2/6) + ---[35] Apodemus latronum , 71.4% (5/7) + ---[35] Eothenomys miletus , 18.8% (3/16) + ---[35] B. grahamii R. rattus + - , 28.6% (2/7) + ---[81] Bartonella Rattus losea unknown species + - , 31% (14/45) + ---[81] Rattus norvegicus , 30% (7/23) + ---[81] Suncus murinus , 16% (7/43) + ---[81] Niviventer confucianus , 4% (1/28) + ---[81] Apodemus agrarius , 46.8% (90/192) + ---[81] Apodemus peninsulae , 28.6% (2/7) + ---[81] Eothenomys melanogaster , 24% (9/37) + ---[81] Microtus fortis , 22% (2/9) + ---[81] B. grahamii Apodemus speciosus Japan + + , 51.2% (116/224) + ---[82] Apodemus argenteus , 37.1% (13/35) B. phoceensis R. rattus, + + 3.7% (11/297) + ---[82] B. rattimassiliensis R. rattus, + + 1.0% (3/297) + ---[82] B. taylorii Apodemus speciosus + + , 8.9% (2/224) + ---[82] Myodes rufocanus bedfordiae subsp. , 23.5% (4/17) B. tribocorum Apodemus speciosus + + , 1.8% (4/224) + ---[82] Apodemus argenteus , 5.7% (2/35) R. rattus , 2.0% (6/297) Apodemus speciosus, Unknown species + + 8.0% (18/224) + ---[82] Apodemus argenteus , 11.4% (4/35) B. clarridgeiae Spermophilus dauricus + + , 40% (4/10) --- + [48] B. elizabethae Sciurus vulgaris orientis + + subsp. , 20% (2/10) --- + [48] B. grahamii Tamias sibiricus + + , 41.4% (12/29) --- + [48] Tawisa Jiyipong et al./Asian Pac J Trop Biomed 2014; 4(10): 757-767 760 continued Table 2 B. washoensis Pteromys volans + + , 50% (5/10) --- + [48] Callosciurus notatus , 63.3% (19/30) --- + [48] Tamiasciurus hudosonicus , 16.7% (3/18) --- + [48] Glaucomys volans , 60% (6/10) --- + [48] Pachyuromys duprasi , 72.2% (13/18) --- + [48] Acomys cahirinus , 9.7% (3/31) --- + [48] Acomys russatus , 61.5% (8/13) --- + [48] Psammomys obesus , 60% (6/10) --- + [48] Sekeetamys calurus , 100% (10/10) --- + [48] Gerbillus pyramidum , 90% (9/10) --- + [48] Jaculus orientalis , 81.3% (13/16) --- + [48] Jaculus jaculus ,75% (6/8) --- + [48] B. elizabethae Apodemus agrarius Korea + - , 14.2% (53/373) + ---[43] Eothenomys melanogaster , 11.1% (1/9) + ---[43] Crocidura lasiura , 12.1% (4/33) - + --[43] B. elizabethae Apodemus agrarius + + , 6.7% (24/358) + ---[34] B. elizabethae R. rattus Taiwan + - , 33.3% (1/3) + ---[73] B. tribocorum Rattus norvegicus + - , 9.4% (5/53) + ---[73] B. elizabethae R. tanezumi R. rattus + + ( ), 20% (1/5) + ---[42] B. queenslandensis Rattus norvegicus + + , 36% (22/61) + ---[42] B. phoceensis Sciurus murinus + + , 20% (4/20) - + --[42] B. rattimassiliensis + + [42] B. tribocorum + + [42] B. elizabethae R. rattus + + , 10% (1/10) + ---[74] B. grahamii Rattus norvegicus + + , 52.7% (89/169) + ---[74] B. phoceensis Rattus losea + + , 66.7% (2/3) + ---[74] B. rattimassiliensis Sattus murinus + + , 28.6% (36/126) ----[74] B. tribocorum + + [74] B. elizabethae Miniopterus schreibersii + + , 42.9% (6/14) -- + -[47] B. grahamii Rattus coxinga niviventer + + , 100% (1/1) + ---[47] B. rattimassiliensis Crocidura attenuata tanakae + + , 77.8% (7/9) - + --[47] B. tribocorum + + [47] unknown species + + [47] B. grahamii Myodes rutilus Western + - , 14.1% (11/78) + ---[85] B. taylorii Myodes glareolus Siberia + - , 16% (4/25) + ---[85] Bartonella Russia unknown species + - [85] Apodemus Eothenomys Mus Myodes 4.2. Shrews genera , Bartonella, and have alsoBartonella been shown to host . A high diversity of B. species elizabethae was observedB. grahamii from B.rodents queenslandensis in this regionB. Several shrew species live in the domestic areas or peri- including , , , domestic environments such as agricultural areas. Isolation phoceensis B. rattimassiliensis B. taylorii, B. tribocorum Bartonella , , and of from shrews has been carried out in Asia and unknown species. Bartonella Bartonella North America. In Asia, most infections in shrews In Southeast Asia, species have been have been described in East Asia (Korea and Taiwan) and investigated from rodents in Indonesia, Lao PDR, Cambodia South Asia (Bangladesh and Nepal)[41-43]. In Southeast Asia, [36-40] Rattus Bartonella and Thailand (Table 3). Again, the genus appears the prevalence of in shrews has been reported Sattus murinus to be the more prevalent rodent genus followed by the in in Indonesia[37] (Table 3). Potential new Bandicota Mus Bartonella Sattus genera and . In South and West Asia, studies species of has been recently observed in Bartonella murinus of in rodents are more limited (Table 4). [36] B. coopersplainsensis in Cambodia . Altogether, it appears that is mainly Sattus murinus Bandicota Bandicota indica B. indica Finally, it appears that is a main host found in species [ ( ) and B. elizabethae B. phoceensis B. rattimassiliensis Bandicota savilei B. savilei R. tanezumi B. elizabethae for , , and ( )] and ; B. tribocorum Crocidura attenuata Apodemus agrarius Rattus Rattus rattus R. , although is found in and species [ ( B. rattimassiliensis B. rattus R. tanezumi B. grahamii Rattus norvegicus infected with high prevalence by and ) and ]; in ; tribocorum B. queenslandensis Mus Mus cookii M. cookii . in species [ ( ), B. phoceensis R. tanezumi B. rattimassiliensis M. in , in 4.3. Bats cookii R. tanezumi B. rochalimae Mus cervicolor and ; in ; B. silvatica Clethrionomys rufocanus B. taylorii C. in ; in Bartonella rufocanus B. tribocorum Apodemus A. chevrieri The knowledge of in bats is still scarce, ; in species ( , A. latronum Rattus R. tanezumi Rattus with only few studies published concerning bats from ) and in species ( , [44] norvegicus B. washoensis Pachyuromys duprasi Asia . Studies on bats and their arthropod vectors have ); in . Tawisa Jiyipong et al./Asian Pac J Trop Biomed 2014; 4(10): 757-767 761 Table 3 Bartonella infection and host species in Southeast Asia. Bartonella Diagnostic test Type of animal Country infection Host species and prevalence of each species Reference PCR Culture Rodent Shrew Bat Exotic pet B. coopersplainsensis B. savilei Cambodia + + , 9.5% (7/74) + ---[36] B. elizabethae Berylmys berdmorei + + , 9.1% (1/11) + ---[36] B. queenslandensis Maxomys surifer + + , 1.1% (1/92) + ---[36] B. rattimassiliensis Niviventer fulvescens, + + 10% (1/10) + ---[36] B. tribocorum Rattus argentiventer + + , 9.5% (4/42) + ---[36] Rattus exulans Unknown new species + + , 3.5% (4/115) + ---[36] R. tanzumi phylogenetic R3 + + , 24.8%(29/117) + ---[36] Sciurus murinus + + , 5.1% (2/39) - + --[36] B. phoceensis R. tanezumi R. rattus Indonesia + - ( ), 10.3% (8/78) + ---[37] B. rattimassiliensis Rattus norvegicus + - , 2% (1/49) + ---[37] S. murinus , 4.8% (4/83) - + --[37] B. elizabethae R. tanezumi R. rattus Laos + - ( ), 16% (61/381) + ---[38] B. phoceensis Rattus exulans + - , 21.5% (17/79) + ---[38] B. tribocorum Cannomys badius + - , 50% (1/2) + ---[38] Mus cervicolor , 1.4% (1/71) + ---[38] Mus caroli , 33.3% (1/3) + ---[38] B. coopersplainsensis B. savilei + + , 7.1% (1/14) + ---[36] B. elizabethae Berylmys berdmorei, + + 20% (1/5) + ---[36] B. queenslandensis Mus caroli, + + 4.8% (1/23) + ---[36] B. rattimassiliensis M. cookii + + , 30.9% (17/55) + ---[36] B. tribocorum Rattus andamanensis + + , 40% (2/5) + ---[36] R. tanezumi Unknown new species + + , 21.8% (17/78) + ---[36] B. queenslandensis B. savilei Thailand + - , 6.1% (2/33) + ---[39] B. coopersplainsensis R. tanezumi R. rattus + - ( ), 8.2% (4/49) + ---[39] B. phoceensis Rattus exulans + - , 1.5% (1/69) + ---[39] B. rochalimae Mus cervicolor + - , 50% (1/2) + ---[39] Candidatus Bartonella Berylmys berdmorei + + , 25% (5/20) + ---[39] thailandensis Maxomys surifer + + , 24.3% (8/33) + ---[39] B. elizabethae B. indica + + , 8.1% (12/147) + ---[40] B. grahamii R. tanezumi R. rattus + + ( ), 12.5% (3/24) + ---[40] Rattus losea , 18% (2/11) + ---[40] B. coopersplainsensis B. indica + + , 32.6% (15/46) + ---[86] B. elizabethae B. savilei + + , 57.1% (4/7) + ---[86] B. phoceensis R. tanezumi R. rattus + + ( ), 65.2% (88/135) + ---[86] B. rattimassiliensis Rattus exulans + + , 3.2% (3/95) + ---[86] B. tribocorum Rattus losea + + , 33.3% (1/3) + ---[86] R. norvegicus + + , 86.4% (19/22) + ---[86] Rattus argentiventer + + , 66.7% (2/3) + ---[86] Rattus remotus + + , 50% (1/2) + ---[86] Mus cervicolor + + , 42.9% (3/7) + ---[86] Berylmys berdmorei + + , 100% (1/1) + ---[86] B. coopersplainsensis B. indica + + , 7.7% (5/65) + ---[36] B. elizabethae Berylmys berdmorei + + , 13.3% (2/15) + ---[36] B. phoceensis Mus caroli + + , 8% (2/26) + ---[36] B. queenslandensis M. cookii + + , 17.1% (6/35) + ---[36] B. rattimassiliensis Mus cervicolor + + , 20.8% (10/48) + ---[36] B. tribocorum Mus + + sp., 75% (3/4) + ---[36] Niviventer fulvescens + + , 12.5% (1/8) + ---[36] Rattus exulans + + , 4.2% (6/142) + ---[36] R. tanezumi + + , 31.6% (12/38) + ---[36] R. tanezumi R3 + + , 20.7% (6/29) + ---[36] 4.4. Exotic pets demonstrated that bats were infected with unknown Bartonella species[45]. Another study found new putative species in bats from Kenya[46]. In Asia, reports are even Exotic pets are wildlife that are traded around the Bartonella scarcer. infection in bat has been described in world, with important illegal trafficking, and have been Miniopterus schreibersii Taiwan[47]. Six blood samples of (and still being) imported into many countries. The illegal Bartonella were positive with new putative spp. with high trade without quarantine may cause the dissemination prevalence (42.9%, Table 2). of infectious diseases. However, there are little data on Tawisa Jiyipong et al./Asian Pac J Trop Biomed 2014; 4(10): 757-767 762 Table 4 Bartonella infection and host species in South and West Asia. Bartonella Diagnostic test Type of animal Country infection Host species Reference PCR Culture Rodent Shrew Bat Exotic pet B. elizabethae Bandicota bengalensis Bangladesh + + , 63.2% (48/76) + ---[37] B. tribocorum R. rattus + + , 32.3% (32/99) + ---[37] Sciurus murinus , 42.9% (6/14) - + --[37] B. elizabethae B. bengalensis Nepal + - , 26.3% (10/38) + ---[87] B. queenslandensis R. rattus brunneusculus + - , 43.3% (39/90) + ---[87] B. phoceensis Sciurus murinus + - , 64.1% (59/92) - + --[87] B. rochalimae + - [87] B. rattimassiliensis + - [87] B. tribocorum + - [87] B. elizabethae R. rattus Israel + + , 16% (10/62) + ---[88] B. tribocorum + + [88] B. elizabethae Apodemus cahirinus + - , 25% (1/4) + ---[89] B. tribocorum R. rattus + - , 24% (19/79) + ---[89]

Table 5 Bartonella Species of detected on arthropod vectors from rodents and shrews in Asia. Bartonella Diagnostic Type of Country Vector species Host reservoirs Ref infection test vector B. elizabethae Xenopsylla cheopis Cricetulus migratorius Afghanistan PCR [90] B. dosiae Xenopsylla cheopis Meriones lybicus PCR flea (gerbil) [90] B. koehlerae Xenopsylla cheopis Mus PCR flea spp. [90] B. quintana Xenopsylla cheopis Rattus PCR flea spp. [90] B. taylorii Xenopsylla cheopis PCR flea [90] Xenopsylla cheopis Rattus tanezumi flavipectus China B. tribocorum PCR flea subsp. [91] Ctenophthalmus lushuiensis Eothenomys PCR flea spp. [91] Bartonella Haemaphysalis longicornis Korea spp. PCR tick Wild rodents [34] Haemaphysalis flava PCR tick Unidentified species [34] Ixodes nipponensis PCR tick [34] Ixodes turdus PCR tick [34] Ixodes persulcatus PCR tick [34] Ixodes PCR spp. tick [34] Apodemus agrarius Crocidura lasiura Microtus fortis Myodes regulus Micromys minutus Ctenophthalmus congeneroides , , , , , PCR flea Mus musculus [92]

Stenoponia sidimi PCR flea [92] Bartonella Xenopsylla cheopis R. rattus Israel sp. PCR flea [93] Leptopsylla algira Mus musculus PCR flea [93] Xenopsylla ramesis Meriones tristrami PCR flea [93] Synosternus cleopatrae Gerbillus andersoni allenbyi PCR flea [93] Gerbillus pyramidum PCR [93] Meriones sacramenti PCR [93] Bartonella Laelaps Apodemus cahirinus Taiwan spp. PCR spp. [42] Laelaps echianinus Rattus norvegicus PCR mite [42] Xenopsylla cheopis R. rattus PCR flea [42] Polyplax spinulosa Sciurus murinus PCR lice [42] Dermacentor PCR spp. tick [42] Ixodes PCR spp. tick [42] Bartonella Nosopsyllus fasciatus Rattus surifer Thailand PCR flea [94] BNfRs B. tamiae Leptotrombidium Rattus argentiventer PCR spp. mite [49] Schoengastia R. rattus PCR spp. mite [49] Blankarrtia B. indica PCR spp. mite [49] Haemaphysalis B. savilei PCR spp. tick [49] Mus cervicolor PCR [49] Bartonella prevalence of infection with spp. from exotic sandflies and ticks have been reported as potential vectors Bartonella small mammal pets in Asia (Table 2). Among them, a study transmitting among animals and between animals reported that several exotic species in Japan were infected and humans. Bartonella [48] Of the several blood-sucking arthropods, fleas are the with spp. with quite high prevalence . Bartonella key vectors of infection. Several studies have 4.5. Vectors Xenopsylla cheopis suggested that fleas, especially , are potential vectors in rodents (Table 5). Ticks, mites and Bartonella Several blood-sucking arthropods including fleas, mites, lice are also potential vectors for infections in Tawisa Jiyipong et al./Asian Pac J Trop Biomed 2014; 4(10): 757-767 763 Table 6 Bartonella Case reports of infection in Asia. Bartonella Country infection Diagnostic test Clinical sign Patient Ref B. quintana India Culture, serology endocarditis endocarditis patients [95] B. henselae Japan Culture, PCR endocarditis 77- year-old, male [96] B. quintana Serology fever, headache, anorexia, history of body lice and homeless people, male and female [97] fleas infestation B. quintana Culture, PCR endocarditis 70- year-old, female [98] B. quintana Culture, PCR endocarditis 66-year-old, male [99] B. quintana Jordan Serology, PCR None (Seroprevalence among Jordanian children) None [100] B. henselae Serology, PCR None [100] B. henselae Korea Gram staining, PCR fever, enlargement of axillary lymph nodes 8-year-old, girl [101] B. henselae Serology cervical lymphadenitis 25- year-old, female [101] B. elizabethae Nepal Serology headache, fever, myalgia ranging from 9 to 70 years, both male [53] and female B. quintana Serology headache, fever, myalgia [53] B. tamiae Serology headache, fever, myalgia [53] B. vinsonii arupensis Serology headache, fever, myalgia [53] B. elizabethae ° ≥ Thailand Serology febrile patients, fever > 38 C for < 2 weeks febrile patients, 7 years old [52] B. henselae ≥ Serology non-febrile patients, (unidentified) non-febrile patients, 14 years old [52] B. quintana Serology [52] B. henselae Culture, PCR fever, pharyngitis, meningitis febrile patients [50] B. henselae Culture, PCR having symptomatic HIV infection 40 year-old [102] B. tamiae Culture, PCR fatigue, myalgia, fever, headache 38 year-old [8] B. tamiae Culture, PCR pterygium in each eye 41 year-old [8] B. tamiae Culture, PCR fever, fatigue, myalgia, a headache 12 year-old [8] B. vinsonii Culture, PCR headache, myalgias, dizziness, and fatigue 11 to 56 year-old [59]

Bartonella 7. Perspectives rodents. Epidemiological surveys of infection in ticks, mites and lice have been done in Korea, Taiwan and Bartonella Thailand[16,34,42,49]. The diversity of species is far from being known et al as the recent study of Jiyipong . emphasized on three [36] I S A 6. Zoonotic diseases and case reports in Asia new putative species . ndeed, outheast sia is a hotspot of mammal species[54] and a diversification centre for several rodent families. Two-thirds of living rodent species Bartonella species are important zoonotic bacteria with belongs to the family Muridae[55], which also represents most increasing array of emerging infections in humans and of the rodents found in Southeast Asia with 35 species[56]. It animals. Bartonellosis has been described in Asia. Possible appears that less than 50% of these murid species have been Bartonella routes of transmission are contacts with infected animals or investigated for the presence of species (Table Bartonella blood-sucking arthropod via their feces. Four 3). The knowledge is even poorer for shrews and bats. This B. henselae B. quintana B. elizabethae species including , , emphasizes the need to increase the screening, detection B. tamiae Bartonella and have been reported as causative agents of and characterization of in small mammals[57]. Bartonella several human diseases in Asia (Table 6). However, few Since species may be transmitted to humans Bartonella Bartonella cases of human infections with bacteria of rodent by ticks, fleas and lice, surveys of distribution Bartonella origins have been reported. The first case of within arthropods are needed. In particular, the population Bartonella endocarditis in Thailand was found in a 57-year-old male changes of these vectors of in relation to the poultry farmer in Khon Kaen province, where the source of impacts of habitat and land-use changes should be better B. tamiae pathogen was a cat. was isolated from three febrile investigated[57]. patients in Thailand[8]. In another report, several farmers Rodents, shrews and bats live in a wide range of habitats were supposed to be exposed to infected rodents at home that are frequented by humans[58], which warrants further Bartonella or fields[50]. Recently, four patients were found infected by investigations on the transmission ecology of B. vinsonii Bartonella in Northern and Northeastern Thailand, with in order to improve prevention of infections. dogs and rats supposed to be reservoirs[51]. Additional Identification of risky habitats for human transmission is Bartonella serological studies evidenced exposure to rodent needed to develop a surveillance strategy, which could spp. in Thailand but also in Nepal[52,53]. However, to date, be done only after the improvement of our knowledge on B. elizabethae Bartonella only was found in rodent surveys, where the the diversity of in small mammals and in their Apodemus most common rodents were murid from spp. and arthropod vectors. Rattus R. rattus R. spp. (and particularly the commensal and This review by giving up-to-date list of reservoirs will tanezumi ). help develop a strategy of reservoirs, vectors and habitats Tawisa Jiyipong et al./Asian Pac J Trop Biomed 2014; 4(10): 757-767 764 Bartonella Applications prone to be sources of outbreaks and/or emerging infections in humans. This review article surveys prevalence of various species Bartonella of in different areas of Asia. Informations Conflict of interest statement offered in this article can be useful for more studies in future. Peer review We declare that we have no conflict of interest. This is a good research about the presence of various Bartonella Acknowledgements species of and its role at causing different infections. The consideration of authors to various reservoirs of this bacteria in animals that a little have been The study was supported by the French ANR CERoPath already surveyed is interesting. Diagnostic tests referred in project (number ANR 07 BDIV 012) (www.ceropath.org), the this article are very useful. French ANR BiodivHealthSEA project (number ANR 11 CPEL 002) ( ) I S www.biodivhealthsea.org , the nfectiopole ud and the References Center of Excellence on Agricultural Biotechnology (Science and Technology Postgraduate Education and Research Development Office, Office of Higher Education Commission, [1] B oulouis HJ, Chang CC, Henn JB, Kasten RW, Chomel BB. 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