Analysis for the prevalence of global bat-borne Bartonella

doi:10.17520/biods.2023166

Abstract

Abstract:

Background & Aim Bartonellae is a worldwide group of bacteria that causes a variety of zoonoses. Their hosts include carnivores, ruminants, rodents, and even mammals such as marine whales. Recently, it has been discovered that Bartonellae can infect bats, one of the important host animals for Bartonellae, worldwide. This review summarizes studies of bat-borne Bartonella worldwide since 2005 to illustrate the prevalence of Bartonellae in bats.

Context & Conclusions Bartonellae has been detected in 106 bat species in 31 countries and regions around the world, indicating that bats are major animal hosts. The feeding habit of bats does not affect whether they can carry Bartonellae, which has been found in bats with multiple feeding habits. The phylogenetic tree based on gltA sequences of bat-borne Bartonella displayed that most bat-borne Bartonella sequences are distant from other host-derived Bartonella and constituted a bat-origin Bartonella group. Bat-borne Bartonella, which has spread with bats worldwide, is host-specific to a certain extent. It is hinted that there is coevolution between Bartonellae and bat hosts.

Key words: Bartonella, bat, bacteria, genetic diversity, phylogenetic analysis, coevolution

Qingduo Li, Dongmei Li. Analysis for the prevalence of global bat-borne Bartonella[J]. Biodiv Sci, 2023, 31(9): 23166.

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URL: https://www.biodiversity-science.net/EN/10.17520/biods.2023166

https://www.biodiversity-science.net/EN/Y2023/V31/I9/23166

Figures/Tables 3

References 48

[1]	André MR, Gutiérrez R, Ikeda P, Amaral RB, Sousa KCM, Nachum-Biala Y, Lima L, Teixeira MMG, Machado RZ, Harrus S (2019) Genetic diversity of Bartonella spp. in vampire bats from Brazil. Transboundary and Emerging Diseases, 66, 2329-2341. DOI URL
[2]	Anh PH, Van Cuong N, Son NT, Tue NT, Kosoy M, Woolhouse MEJ, Baker S, Bryant JE, Thwaites G, Carrique-Mas JJ, Rabaa MA (2015) Diversity of Bartonella spp. in bats, southern Vietnam. Emerging Infectious Diseases, 21, 1266-1267. DOI URL
[3]	Bai Y (2011) Bartonella spp. in bats, Guatemala. Emerging Infectious Diseases, 17, 1269-1272. DOI URL
[4]	Bai Y, Gómez J, Kosoy MY, Recuenco S, Osikowicz LM, Rupprecht C, Gilbert AT (2012) Prevalence and diversity of Bartonella spp. in bats in Peru. The American Journal of Tropical Medicine and Hygiene, 87, 518-523. DOI URL
[5]	Bai Y, Osinubi MOV, Osikowicz L, McKee C, Vora NM, Rizzo MR, Recuenco S, Davis L, Niezgoda M, Ehimiyein AM, Kia GSN, Oyemakinde A, Adeniyi OS, Gbadegesin YH, Saliman OA, Ogunniyi A, Ogunkoya AB, Kosoy MY (2018) Human exposure to novel Bartonella species from contact with fruit bats. Emerging Infectious Diseases, 24, 2317-2323. DOI URL
[6]	Bai Y, Urushadze L, Osikowicz L, McKee C, Kuzmin I, Kandaurov A, Babuadze G, Natradze I, Imnadze P, Kosoy M (2017) Molecular survey of bacterial zoonotic agents in bats from the country of Georgia (Caucasus). PLoS ONE, 12, e171175.
[7]	Becker DJ, Bergner LM, Bentz AB, Orton RJ, Altizer S, Streicker DG (2018) Genetic diversity, infection prevalence, and possible transmission routes of Bartonella spp. in vampire bats. PLoS Neglected Tropical Diseases, 12, e0006786.
[8]	Breitschwerdt EB (2017) Bartonellosis, One Health and all creatures great and small. Veterinary Dermatology, 28, 96-e21.
[9]	Brook CE, Bai Y, Dobson AP, Osikowicz LM, Ranaivoson HC, Zhu QY, Kosoy MY, Dittmar K (2015) Bartonella spp. in fruit bats and blood-feeding ectoparasites in Madagascar. PLoS Neglected Tropical Diseases, 9, e0003532.
[10]	Chomel BB, Obregón-Morales C, Olave-Leyva JI, Aréchiga-Ceballos N, Stuckey MJ, Moreno-Sandoval H, Aguilar-Setién A, Salas-Rojas M, Galvez-Romero G (2017) Bartonella infection in hematophagous, insectivorous, and phytophagous bat populations of central Mexico and the Yucatan Peninsula. The American Journal of Tropical Medicine and Hygiene, 97, 413-422. DOI URL
[11]	Cicuttin GL, De Salvo MN, La Rosa I, Dohmen FEG (2017) Neorickettsia risticii, Rickettsia sp. and Bartonella sp. in Tadarida brasiliensis bats from Buenos Aires, Argentina. Comparative Immunology, Microbiology and Infectious Diseases, 52, 1-5. DOI URL
[12]	Concannon R, Wynn-Owen K, Simpson VR, Birtles RJ (2005) Molecular characterization of haemoparasites infecting bats (Microchiroptera) in Cornwall, UK. Parasitology, 131, 489-496. PMID
[13]	Davoust B, Marié JL, Dahmani M, Berenger JM, Bompar JM, Blanchet D, Cheuret M, Raoult D, Mediannikov O (2016) Evidence of Bartonella spp. in blood and ticks (Ornithodoros hasei) of bats, in French Guiana. Vector-Borne and Zoonotic Diseases, 16, 516-519. DOI URL
[14]	Dietrich M, Tjale MA, Weyer J, Kearney T, Seamark ECJ, Nel LH, Monadjem A, Markotter W (2016) Diversity of Bartonella and Rickettsia spp. in bats and their blood-feeding ectoparasites from South Africa and Swaziland. PLoS ONE, 11, e0152077. DOI URL
[15]	Ferreira MS, Guterres A, Rozental T, Novaes RLM, Vilar EM, Oliveira RC, Fernandes J, Forneas D, Junior AA, Brandão ML, Cordeiro JLP, Del Valle Alvarez MR, Althoff SL, Moratelli R, Cordeiro-Estrela P, Silva RCD, Lemos ERS (2018) Coxiella and Bartonella spp. in bats (Chiroptera) captured in the Brazilian Atlantic Forest biome. BMC Veterinary Research, 14, 279. DOI
[16]	Gonçalves-Oliveira J, Rozental T, Guterres A, Teixeira BR, Elise Andrade-Silva B, da Costa-Neto SF, Furtado MC, Moratelli R, D’Andrea PS, Lemos ERS (2020) Investigation of Bartonella spp. in Brazilian mammals with emphasis on rodents and bats from the Atlantic Forest. International Journal for Parasitology: Parasites and Wildlife, 13, 80-89. DOI PMID
[17]	Han HJ, Li ZM, Li X, Liu JX, Peng QM, Wang R, Gu XL, Jiang Y, Zhou CM, Li D, Xiao X, Yu XJ (2022) Bats and their ectoparasites (Nycteribiidae and Spinturnicidae) carry diverse novel Bartonella genotypes, China. Transboundary and Emerging Diseases, 69, e845-e858.
[18]	Han HJ, Wen HL, Zhao L, Liu JW, Luo LM, Zhou CM, Qin XR, Zhu YL, Zheng XX, Yu XJ (2017) Novel Bartonella species in insectivorous bats, northern China. PLoS ONE, 12, e0167915.
[19]	Hou SL, Koh FX, Nuryana I, Sitam FT, Tay ST (2018) Molecular detection of Bartonella spp. in Malaysian small flying foxes (Pteropus hypomelanus). Tropical Biomedicine, 35, 293-299. PMID
[20]	Ikeda P, Marinho Torres J, Perles L, Lourenço EC, Herrera HM, de Oliveira CE, Zacarias Machado R, André MR (2020) Intra- and inter-host assessment of Bartonella diversity with focus on non-hematophagous bats and associated ectoparasites from Brazil. Microorganisms, 8, 1822. DOI URL
[21]	Ikeda P, Seki MC, Carrasco AOT, Rudiak LV, Miranda JMD, Gonçalves SMM, Hoppe EGL, Albuquerque ACA, Teixeira MMG, Passos CE, Werther K, Machado RZ, André MR (2017) Evidence and molecular characterization of Bartonella spp. and hemoplasmas in neotropical bats in Brazil. Epidemiology and Infection, 145, 2038-2052. DOI PMID
[22]	Judson SD, Frank HK, Hadly EA (2015) Bartonellae are prevalent and diverse in Costa Rican bats and bat flies. Zoonoses and Public Health, 62, 609-617. DOI PMID
[23]	Kaiser PO, Riess T, O’Rourke F, Linke D, Kempf VAJ (2011) Bartonella spp.: Throwing light on uncommon human infections. International Journal of Medical Microbiology, 301, 7-15. DOI URL
[24]	Kamani J, Baneth G, Mitchell M, Mumcuoglu KY, Gutiérrez R, Harrus S (2014) Bartonella species in bats (Chiroptera) and bat flies (Nycteribiidae) from Nigeria, West Africa. Vector Borne and Zoonotic Diseases, 14, 625-632. DOI URL
[25]	Kosoy M, Bai Y, Lynch T, Kuzmin IV, Niezgoda M, Franka R, Agwanda B, Breiman RF, Rupprecht CE (2010) Bartonella spp. in bats, Kenya. Emerging Infectious Diseases, 16, 1875-1881. DOI URL
[26]	Li DM, Yang WH, Li QD, Han X, Song XP, Pan H, Feng Y (2021) High prevalence and genetic variation of Bartonella species inhabiting the bats in southwestern Yunnan. Biodiversity Science, 29, 1245-1255. (in Chinese with English abstract) DOI URL
	[栗冬梅, 杨卫红, 李庆多, 韩茜, 宋秀平, 潘虹, 冯云 (2021) 巴尔通体在滇西南蝙蝠中高度流行并具有丰富的遗传变异特征. 生物多样性, 29, 1245-1255.]
[27]	Lilley TM, Veikkolainen V, Pulliainen AT (2015) Molecular detection of Candidatus Bartonella hemsundetiensis in bats. Vector-Borne and Zoonotic Diseases, 15, 706-708. DOI URL
[28]	Lilley TM, Wilson CA, Bernard RF, Willcox EV, Vesterinen EJ, Webber QM, Kurpiers L, Prokkola JM, Ejotre I, Kurta A, Field KA, Reeder DM, Pulliainen AT (2017) Molecular detection of Candidatus Bartonella mayotimonensis in north American bats. Vector-Borne and Zoonotic Diseases, 17, 243-246. DOI URL
[29]	Lin J, Hsu Y, Chomel BB, Lin L, Pei J, Wu S, Chang C (2012) Identification of novel Bartonella spp. in bats and evidence of Asian gray shrew as a new potential reservoir of Bartonella. Veterinary Microbiology, 156, 119-126. DOI URL
[30]	McKee CD, Kosoy MY, Bai Y, Osikowicz LM, Franka R, Gilbert AT, Boonmar S, Rupprecht CE, Peruski LF (2017) Diversity and phylogenetic relationships among Bartonella strains from Thai bats. PLoS ONE, 12, e0181696.
[31]	Mitchell MM, Vicente-Santos A, Rodríguez-Herrera B, Corrales-Aguilar E, Gillespie TR (2022) Genetic diversity of Bartonella spp. in cave-dwelling bats and bat flies, Costa Rica, 2018. Emerging Infectious Diseases, 28, 488-491. DOI PMID
[32]	Mühldorfer K (2013) Bats and bacterial pathogens: A review. Zoonoses and Public Health, 60, 93-103. DOI PMID
[33]	Müller A, Sepúlveda P, Di Cataldo S, Cevidanes A, Lisón F, Millán J (2020) Molecular investigation of zoonotic intracellular bacteria in Chilean bats. Comparative Immunology, Microbiology and Infectious Diseases, 73, 101541. DOI URL
[34]	Nabeshima K, Sato S, Brinkerhoff RJ, Amano M, Kabeya H, Itou T, Maruyama S (2023) Prevalence and genetic diversity of Bartonella spp. in northern bats (Eptesicus nilssonii) and their blood-sucking ectoparasites in Hokkaido, Japan. Microbial Ecology, 85, 298-306. DOI
[35]	Nabeshima K, Sato S, Kabeya H, Kato C, Suzuki K, Maruyama S (2020) Isolation and genetic properties of Bartonella in eastern bent-wing bats (Miniopterus fuliginosus) in Japan. Infection, Genetics and Evolution, 83, 104354. DOI URL
[36]	Noguchi H, Battistini TS (1926) Etiology of Oroya fever: I. Cultivation of Bartonella bacilliformis. Journal of Experimental Medicine, 43, 851-864. DOI PMID
[37]	Olival KJ, Dittmar K, Bai Y, Rostal MK, Lei BR, Daszak P, Kosoy M (2015) Bartonella spp. in a Puerto Rican bat community. Journal of Wildlife Diseases, 51, 274-278. DOI PMID
[38]	Oren A, Garrity GM (2021) Valid publication of the names of forty-two phyla of prokaryotes. International Journal of Systematic and Evolutionary Microbiology, 71, 005056.
[39]	Parte AC, Sardà Carbasse J, Meier-Kolthoff JP, Reimer LC, Göker M (2020) List of Prokaryotic names with standing in Nomenclature (LPSN) moves to the DSMZ. International Journal of Systematic and Evolutionary Microbiology, 70, 5607-5612. DOI URL
[40]	Poofery J, Narapakdeesakul D, Riana E, Arnuphapprasert A, Nugraheni YR, Ngamprasertwong T, Wangthongchaicharoen M, Soisook P, Bhodhibundit P, Kaewthamasorn M (2022) Molecular identification and genetic diversity of Bartonella spp. in 24 bat species from Thailand. Transboundary and Emerging Diseases, 69, e717-e733.
[41]	Qiu YJ, Kajihara M, Nakao R, Mulenga E, Harima H, Hang’ombe BM, Eto Y, Changula K, Mwizabi D, Sawa H, Higashi H, Mweene A, Takada A, Simuunza M, Sugimoto C (2020) Isolation of Candidatus Bartonella rousetti and other bat-associated Bartonellae from bats and their flies in Zambia. Pathogens, 9, 469. DOI URL
[42]	Reeves WK, Beck J, Orlova MV, Daly JL, Pippin K, Revan F, Loftis AD (2016) Ecology of bats, their ectoparasites, and associated pathogens on Saint Kitts Island. Journal of Medical Entomology, 53, 1218-1225. DOI PMID
[43]	Stuckey MJ, Boulouis HJ, Cliquet F, Picard-Meyer E, Servat A, Aréchiga-Ceballos N, Echevarría JE, Chomel BB (2017) Potentially zoonotic Bartonella in bats from France and Spain. Emerging Infectious Diseases, 23, 539-541. DOI URL
[44]	Szentiványi T, Markotter W, Dietrich M, Clément L, Ançay L, Brun L, Genzoni E, Kearney T, Seamark E, Estók P, Christe P, Glaizot O (2020) Host conservation through their parasites: Molecular surveillance of vector-borne microorganisms in bats using ectoparasitic bat flies. Parasite, 27, 72. DOI PMID
[45]	Szubert-Kruszyńska A, Stańczak J, Cieniuch S, Podsiadły E, Postawa T, Michalik J (2019) Bartonella and Rickettsia infections in Haematophagous Spinturnix myoti mites (Acari: Mesostigmata) and their bat host, Myotis myotis (Yangochiroptera: Vespertilionidae), from Poland. Microbial Ecology, 77, 759-768. DOI PMID
[46]	Urushadze L, Bai Y, Osikowicz L, McKee C, Sidamonidze K, Putkaradze D, Imnadze P, Kandaurov A, Kuzmin I, Kosoy M (2017) Prevalence, diversity, and host associations of Bartonella strains in bats from Georgia (Caucasus). PLoS Neglected Tropical Diseases, 11, e0005428.
[47]	Veikkolainen V, Vesterinen EJ, Lilley TM, Pulliainen AT (2014) Bats as reservoir hosts of human bacterial pathogen, Bartonella mayotimonensis. Emerging Infectious Diseases, 20, 960-967. DOI PMID
[48]	Wray AK, Olival KJ, Morán D, Lopez MR, Alvarez D, Navarrete-Macias I, Liang E, Simmons NB, Lipkin WI, Daszak P, Anthony SJ (2016) Viral diversity, prey preference, and Bartonella prevalence in Desmodus rotundus in Guatemala. Ecohealth, 13, 761-774. PMID

洲和国家(参考文献) Continents and countries studied (References)				感染巴尔通体的蝙蝠 Bats infected with Bartonellae			感染率 Infection rates (%)	调查方法(目标基因) Investigation methods (target genes)
非洲 Africa	南非 South Africa (Dietrich et al, 2016)			韦氏颈囊果蝠 Epomophorus wahlbergi 长翼蝠 Miniopterus natalensis 埃及果蝠 Rousettus aegyptiacus			15.5	PCR (gltA)
	斯威士兰 Swaziland (Dietrich et al, 2016)			非洲凹脸蝠 Nycteris thebaica			2.7	PCR (gltA)
	尼日利亚 Nigeria (Kamani et al, 2014; Bai et al, 2018)			黄毛果蝠 Eidolon helvum Epomophorus sp. Micropterus sp. 埃及果蝠 Rousettus aegyptiacus 菊头蝠属一种 Rhinolophus sp.			12.4-15.5	分离培养 Isolation & culture, PCR (gltA)
	赞比亚 Zambia (Qiu et al, 2020)			埃及果蝠 Rousettus aegyptiacus Hipposideros vittatus			16.7	分离培养 Isolation & culture, PCR (gltA)
	马达加斯加 Madagascar (Brook et al, 2015)			Eidolon dupreanum			23.6	PCR (gltA)
	肯尼亚 Kenya (Kosoy et al, 2010)			南鞘尾蝠 Coleura afra 黄毛果蝠 Eidolon helvum 康氏蹄蝠 Hipposideros commersoni 长翼蝠属一种 Miniopterus sp. 埃及果蝠 Rousettus aegyptiacus 波斯叶鼻蝠 Triaenops persicus			32.0	分离培养 Isolation & culture, PCR (gltA)
欧洲 Europe	芬兰 Finland (Veikkolainen et al, 2014; Lilley et al, 2015)			水鼠耳蝠 Myotis daubentonii 圆形叶口蝠 Desmodus rotundus 北棕蝠 Eptesicus nilssonii			33.3-37.1	PCR (gltA, rpoB)
	英国 Britain (Concannon et al, 2005)			翼蝠属一种 Pipistrellus sp.			8.3	PCR (gltA)
	法国 France (Stuckey et al, 2017)			水鼠耳蝠 Myotis daubentonii 须鼠耳蝠 Myotis mystacinus 褐山蝠 Nyctalus noctula 纳氏伏翼蝠 Pipistrellus nathusii			10.1	PCR (gltA)
	意大利 Italy (Szentiványi et al, 2020)			普通长翼蝠 Miniopterus schreibersii			25.0	PCR (gltA)
	匈牙利 Hungary (Szentiványi et al, 2020)			普通长翼蝠 Miniopterus schreibersii			33.3	PCR (gltA)
	波兰 Poland (Szubert-Kruszyńska et al, 2019)			大鼠耳蝠 Myotis myotis			25.4	PCR (gltA)
	西班牙 Spain (Stuckey et al, 2017)			未鉴定 Unidentified			3.8	PCR (gltA)
亚洲 Asia	马来西亚 Malaysia (Hou et al, 2018)			小狐蝠 Pteropus hypomelanus			6.7	分离培养 Isolation & culture, PCR (gltA)
	日本 Japan (Nabeshima et al, 2020, 2023)			亚洲长翼蝠 Miniopterus fuliginosus 北棕蝠 Eptesicus nilssonii			24.0-26.0	分离培养 Isolation & culture, PCR (gltA)
	中国 China (Han et al, 2017, 2022; Li et al, 2021; Lin et al, 2012)			普通长翼蝠 Miniopterus schreibersii 毛腿鼠耳蝠 Myotis fimbriatus 北京鼠耳蝠 Myotis pequinius 大足鼠耳蝠 Myotis ricketti 小菊头蝠 Rhinolophus pusillus 马铁菊头蝠 Rhinolophus ferrumequinum 中菊头蝠 Rhinolophus affinis 棕果蝠 Rousettus leschenaultii 小鼠耳蝠 Myotis davidii 郝氏鼠耳蝠 Myotis adversus			10.3-56.4	PCR (gltA), qPCR (ssrA)
	越南 Vietnam (Anh et al, 2015)			大蹄蝠 Hipposideros armiger Hipposideros larvatui 印度假吸血蝠 Megaderma lyra 马来假吸血蝠 Megaderma spasma 泰国无尾果蝠 Megaerops niphanae 大角菊头蝠 Rhinolophus acuminatus Rhinolophus chaseli 中华菊头蝠 Rhinolophus sinicus			35.0	PCR (gltA)
	泰国 Thailand (Mckee et al, 2017; Poofery et al, 2022)	无尾长鼻蝠 Anoura geoffroyi 中蹄蝠 Hipposideros larvatus 黑髯墓蝠 Taphozous melanopogon 圆形叶口蝠 Desmodus rotundus 大耳蹄蝠 Hipposideros fulvus 大蹄蝠 Hipposideros armiger Craseonycteris thonglongyai Rhinolophus coelophyllus Hipposideros kunzi Hipposideros gentilis 喜山鼠耳蝠 Myotis muricola 小蹄蝠 Hipposideros cineraceus 马来假吸血蝠 Megaderma spasma 马来菊头蝠 Rhinolophus malayanus 皮氏菊头蝠 Rhinolophus pearsonii 高颅鼠耳蝠 Myotis siligorensis			25.5-36.6			分离培养 Isolation & culture, PCR (gltA, 16S rRNA gene)
	格鲁吉亚 Georgia (Bai et al, 2017; Urushadze et al, 2017)	棕蝠 Eptesicus serotinus 普通长翼蝠 Miniopterus schreibersii 尖耳鼠耳蝠 Myotis blythii 佐氏鼠耳蝠 Myotis emarginatus Pipistrellus pygmaeus 地中海菊头蝠 Rhinolophus euryale 马铁菊头蝠 Rhinolophus ferrumequinum			35.3-49.5			PCR (ITS (16S-23S internal transcribed spacer locus), gltA)
美洲 America	美国 United States of America (Lilley et al, 2017)	灰鼠耳蝠 Myotis grisescens 小棕蝠 Myotis lucifugus			9.8			PCR (gltA)
	圣基茨和尼维斯 Saint Kitts and Nevis (Reeves et al, 2016)	牙买加果蝠 Artibeus jamaicensis Artibeus fimbriatus 艾氏短尾叶鼻蝠 Carollia castanea			36.9			PCR (gltA)
	哥斯达黎加 Costa Rica (Judson et al, 2015; Mitchell et al, 2022)	Micronycteris microtus Myotis keaysei Chaerephon plicatus Artibeus obscurus 大食果蝠 Artibeus lituratus Platyrrhinus vittatus Vampyressa thyone 昭短尾叶鼻蝠 Carollia perspicillata 毛足黄肩蝠 Sturnira mordax 苍白矛吻蝠 Phyllostomus discolor 美洲林蝠 Ardops nichollsi 黄肩蝠 Sturnira lilium			10.7-33.3			PCR (gltA)
	危地马拉 Guatemala (Bai, 2011; Wray et al, 2016)	中美果蝠 Artibeus toltecus 昭短尾叶鼻蝠 Carollia perspicillata 圆形叶口蝠 Desmodus rotundus 鼩形长舌蝠 Glossophaga soricina 美洲大耳蝠 Micronycteris microtis 苍白矛吻蝠 Phyllostomus discolor 裸背蝠 Pteronotus davyi 黄肩蝠 Sturnira lilium			33.1-39.3			PCR (gltA)
	墨西哥 Mexico (Chomel et al, 2017)	牙买加果蝠 Artibeus jamaicensis 襞兜翼蝠 Balantiopteryx plicata 圆形叶口蝠 Desmodus rotundus 红斑裸背蝠 Pteronotus parnellii 黄肩蝠属一种 Sturnira sp.			22.7			PCR (gltA)
	秘鲁 Peru (Bai et al, 2012; Becker et al, 2018)	Artibeus obscurus 扁吻美洲果蝠 Artibeus planirostris 短尾叶鼻蝠 Carollia brevicauda 昭短尾叶鼻蝠 Carollia perspicillata 圆形叶口蝠 Desmodus rotundus 鼩形长舌蝠 Glossophaga soricina 鼠耳蝠属一种 Myotis sp. 苍白矛吻蝠 Phyllostomus discolor 矛吻蝠 Phyllostomus hastatus			24.1-67.3			PCR (gltA)
			黄肩蝠 Sturnira lilium Vampyriscus bidens
	法属圭亚那 French Guiana (Davoust et al, 2016)		垂耳真蝠 Eumops auripendulus Noctilio albiventris 红斑裸背蝠 Pteronotus parnellii			13.6		PCR (gltA)
	伯利兹 Belize (Becker et al, 2018)		圆形叶口蝠 Desmodus rotundus			45.0		PCR (gltA)
	巴西 Brazil (Ikeda et al, 2017, 2020; Ferreira et al, 2018; André et al, 2019; Gon?alves-Oliveira et al, 2020)		昭短尾叶鼻蝠 Carollia perspicillata 牙买加果蝠 Artibeus jamaicensis 小叶吻蝠 Rhinophylla pumilio 狭叶蝠 Brachyphylla cavernarum 毛腿吸血蝠 Diphylla ecaudata 黄肩蝠 Sturnira lilium 大蹄蝠 Hipposideros armiger 大食果蝠 Artibeus lituratus 苍白矛吻蝠 Phyllostomus discolor 扁吻美洲果蝠 Artibeus planirostris Platyrrhinus lineatus Natalus espiritosantensis 鼩形长舌蝠 Glossophaga soricina Carollia sowelii 圆形叶口蝠 Desmodus rotundus			4.3-24.5		PCR (gltA, nuoG (NADH dehydrogenase gamma subunit gene)), qPCR (ITS)
	阿根廷 Argentina (Cicuttin et al, 2017)		巴西犬吻蝠 Tadarida brasiliensis			4.9		PCR (gltA)
	波多黎各 Puerto Rico (Olival et al, 2015)		牙买加果蝠 Artibeus jamaicensis 狭叶蝠 Brachyphylla cavernarum 牙买加长舌蝠 Monophyllus redmani			17.6		PCR (gltA)
	智利 Chile (Müller et al, 2020)		智利鼠耳蝠 Myotis chiloensis Histiotus montanus Histiotus macrotus 巴西犬吻蝠 Tadarida brasiliensis			38.1		PCR (gltA)

洲和国家(参考文献) Continents and countries studied (References)				感染巴尔通体的蝙蝠 Bats infected with Bartonellae			感染率 Infection rates (%)	调查方法(目标基因) Investigation methods (target genes)
非洲 Africa	南非 South Africa (Dietrich et al, 2016)			韦氏颈囊果蝠 Epomophorus wahlbergi 长翼蝠 Miniopterus natalensis 埃及果蝠 Rousettus aegyptiacus			15.5	PCR (gltA)
	斯威士兰 Swaziland (Dietrich et al, 2016)			非洲凹脸蝠 Nycteris thebaica			2.7	PCR (gltA)
	尼日利亚 Nigeria (Kamani et al, 2014; Bai et al, 2018)			黄毛果蝠 Eidolon helvum Epomophorus sp. Micropterus sp. 埃及果蝠 Rousettus aegyptiacus 菊头蝠属一种 Rhinolophus sp.			12.4-15.5	分离培养 Isolation & culture, PCR (gltA)
	赞比亚 Zambia (Qiu et al, 2020)			埃及果蝠 Rousettus aegyptiacus Hipposideros vittatus			16.7	分离培养 Isolation & culture, PCR (gltA)
	马达加斯加 Madagascar (Brook et al, 2015)			Eidolon dupreanum			23.6	PCR (gltA)
	肯尼亚 Kenya (Kosoy et al, 2010)			南鞘尾蝠 Coleura afra 黄毛果蝠 Eidolon helvum 康氏蹄蝠 Hipposideros commersoni 长翼蝠属一种 Miniopterus sp. 埃及果蝠 Rousettus aegyptiacus 波斯叶鼻蝠 Triaenops persicus			32.0	分离培养 Isolation & culture, PCR (gltA)
欧洲 Europe	芬兰 Finland (Veikkolainen et al, 2014; Lilley et al, 2015)			水鼠耳蝠 Myotis daubentonii 圆形叶口蝠 Desmodus rotundus 北棕蝠 Eptesicus nilssonii			33.3-37.1	PCR (gltA, rpoB)
	英国 Britain (Concannon et al, 2005)			翼蝠属一种 Pipistrellus sp.			8.3	PCR (gltA)
	法国 France (Stuckey et al, 2017)			水鼠耳蝠 Myotis daubentonii 须鼠耳蝠 Myotis mystacinus 褐山蝠 Nyctalus noctula 纳氏伏翼蝠 Pipistrellus nathusii			10.1	PCR (gltA)
	意大利 Italy (Szentiványi et al, 2020)			普通长翼蝠 Miniopterus schreibersii			25.0	PCR (gltA)
	匈牙利 Hungary (Szentiványi et al, 2020)			普通长翼蝠 Miniopterus schreibersii			33.3	PCR (gltA)
	波兰 Poland (Szubert-Kruszyńska et al, 2019)			大鼠耳蝠 Myotis myotis			25.4	PCR (gltA)
	西班牙 Spain (Stuckey et al, 2017)			未鉴定 Unidentified			3.8	PCR (gltA)
亚洲 Asia	马来西亚 Malaysia (Hou et al, 2018)			小狐蝠 Pteropus hypomelanus			6.7	分离培养 Isolation & culture, PCR (gltA)
	日本 Japan (Nabeshima et al, 2020, 2023)			亚洲长翼蝠 Miniopterus fuliginosus 北棕蝠 Eptesicus nilssonii			24.0-26.0	分离培养 Isolation & culture, PCR (gltA)
	中国 China (Han et al, 2017, 2022; Li et al, 2021; Lin et al, 2012)			普通长翼蝠 Miniopterus schreibersii 毛腿鼠耳蝠 Myotis fimbriatus 北京鼠耳蝠 Myotis pequinius 大足鼠耳蝠 Myotis ricketti 小菊头蝠 Rhinolophus pusillus 马铁菊头蝠 Rhinolophus ferrumequinum 中菊头蝠 Rhinolophus affinis 棕果蝠 Rousettus leschenaultii 小鼠耳蝠 Myotis davidii 郝氏鼠耳蝠 Myotis adversus			10.3-56.4	PCR (gltA), qPCR (ssrA)
	越南 Vietnam (Anh et al, 2015)			大蹄蝠 Hipposideros armiger Hipposideros larvatui 印度假吸血蝠 Megaderma lyra 马来假吸血蝠 Megaderma spasma 泰国无尾果蝠 Megaerops niphanae 大角菊头蝠 Rhinolophus acuminatus Rhinolophus chaseli 中华菊头蝠 Rhinolophus sinicus			35.0	PCR (gltA)
	泰国 Thailand (Mckee et al, 2017; Poofery et al, 2022)	无尾长鼻蝠 Anoura geoffroyi 中蹄蝠 Hipposideros larvatus 黑髯墓蝠 Taphozous melanopogon 圆形叶口蝠 Desmodus rotundus 大耳蹄蝠 Hipposideros fulvus 大蹄蝠 Hipposideros armiger Craseonycteris thonglongyai Rhinolophus coelophyllus Hipposideros kunzi Hipposideros gentilis 喜山鼠耳蝠 Myotis muricola 小蹄蝠 Hipposideros cineraceus 马来假吸血蝠 Megaderma spasma 马来菊头蝠 Rhinolophus malayanus 皮氏菊头蝠 Rhinolophus pearsonii 高颅鼠耳蝠 Myotis siligorensis			25.5-36.6			分离培养 Isolation & culture, PCR (gltA, 16S rRNA gene)
	格鲁吉亚 Georgia (Bai et al, 2017; Urushadze et al, 2017)	棕蝠 Eptesicus serotinus 普通长翼蝠 Miniopterus schreibersii 尖耳鼠耳蝠 Myotis blythii 佐氏鼠耳蝠 Myotis emarginatus Pipistrellus pygmaeus 地中海菊头蝠 Rhinolophus euryale 马铁菊头蝠 Rhinolophus ferrumequinum			35.3-49.5			PCR (ITS (16S-23S internal transcribed spacer locus), gltA)
美洲 America	美国 United States of America (Lilley et al, 2017)	灰鼠耳蝠 Myotis grisescens 小棕蝠 Myotis lucifugus			9.8			PCR (gltA)
	圣基茨和尼维斯 Saint Kitts and Nevis (Reeves et al, 2016)	牙买加果蝠 Artibeus jamaicensis Artibeus fimbriatus 艾氏短尾叶鼻蝠 Carollia castanea			36.9			PCR (gltA)
	哥斯达黎加 Costa Rica (Judson et al, 2015; Mitchell et al, 2022)	Micronycteris microtus Myotis keaysei Chaerephon plicatus Artibeus obscurus 大食果蝠 Artibeus lituratus Platyrrhinus vittatus Vampyressa thyone 昭短尾叶鼻蝠 Carollia perspicillata 毛足黄肩蝠 Sturnira mordax 苍白矛吻蝠 Phyllostomus discolor 美洲林蝠 Ardops nichollsi 黄肩蝠 Sturnira lilium			10.7-33.3			PCR (gltA)
	危地马拉 Guatemala (Bai, 2011; Wray et al, 2016)	中美果蝠 Artibeus toltecus 昭短尾叶鼻蝠 Carollia perspicillata 圆形叶口蝠 Desmodus rotundus 鼩形长舌蝠 Glossophaga soricina 美洲大耳蝠 Micronycteris microtis 苍白矛吻蝠 Phyllostomus discolor 裸背蝠 Pteronotus davyi 黄肩蝠 Sturnira lilium			33.1-39.3			PCR (gltA)
	墨西哥 Mexico (Chomel et al, 2017)	牙买加果蝠 Artibeus jamaicensis 襞兜翼蝠 Balantiopteryx plicata 圆形叶口蝠 Desmodus rotundus 红斑裸背蝠 Pteronotus parnellii 黄肩蝠属一种 Sturnira sp.			22.7			PCR (gltA)
	秘鲁 Peru (Bai et al, 2012; Becker et al, 2018)	Artibeus obscurus 扁吻美洲果蝠 Artibeus planirostris 短尾叶鼻蝠 Carollia brevicauda 昭短尾叶鼻蝠 Carollia perspicillata 圆形叶口蝠 Desmodus rotundus 鼩形长舌蝠 Glossophaga soricina 鼠耳蝠属一种 Myotis sp. 苍白矛吻蝠 Phyllostomus discolor 矛吻蝠 Phyllostomus hastatus			24.1-67.3			PCR (gltA)
			黄肩蝠 Sturnira lilium Vampyriscus bidens
	法属圭亚那 French Guiana (Davoust et al, 2016)		垂耳真蝠 Eumops auripendulus Noctilio albiventris 红斑裸背蝠 Pteronotus parnellii			13.6		PCR (gltA)
	伯利兹 Belize (Becker et al, 2018)		圆形叶口蝠 Desmodus rotundus			45.0		PCR (gltA)
	巴西 Brazil (Ikeda et al, 2017, 2020; Ferreira et al, 2018; André et al, 2019; Gon?alves-Oliveira et al, 2020)		昭短尾叶鼻蝠 Carollia perspicillata 牙买加果蝠 Artibeus jamaicensis 小叶吻蝠 Rhinophylla pumilio 狭叶蝠 Brachyphylla cavernarum 毛腿吸血蝠 Diphylla ecaudata 黄肩蝠 Sturnira lilium 大蹄蝠 Hipposideros armiger 大食果蝠 Artibeus lituratus 苍白矛吻蝠 Phyllostomus discolor 扁吻美洲果蝠 Artibeus planirostris Platyrrhinus lineatus Natalus espiritosantensis 鼩形长舌蝠 Glossophaga soricina Carollia sowelii 圆形叶口蝠 Desmodus rotundus			4.3-24.5		PCR (gltA, nuoG (NADH dehydrogenase gamma subunit gene)), qPCR (ITS)
	阿根廷 Argentina (Cicuttin et al, 2017)		巴西犬吻蝠 Tadarida brasiliensis			4.9		PCR (gltA)
	波多黎各 Puerto Rico (Olival et al, 2015)		牙买加果蝠 Artibeus jamaicensis 狭叶蝠 Brachyphylla cavernarum 牙买加长舌蝠 Monophyllus redmani			17.6		PCR (gltA)
	智利 Chile (Müller et al, 2020)		智利鼠耳蝠 Myotis chiloensis Histiotus montanus Histiotus macrotus 巴西犬吻蝠 Tadarida brasiliensis			38.1		PCR (gltA)