Molecular evidence of Bartonella spp. in tropical wild birds from the Brazilian Pantanal, the largest wetland in South America.
Bartonella henselae
Bartonella machadoae
Bartonellosis
Birds
Journal
Veterinary research communications
ISSN: 1573-7446
Titre abrégé: Vet Res Commun
Pays: Switzerland
ID NLM: 8100520
Informations de publication
Date de publication:
05 Mar 2024
05 Mar 2024
Historique:
received:
05
12
2023
accepted:
26
02
2024
medline:
6
3
2024
pubmed:
6
3
2024
entrez:
5
3
2024
Statut:
aheadofprint
Résumé
Despite the worldwide occurrence of bartonellae in a broad range of mammal species, in which they usually cause a long-lasting erythrocytic bacteremia, few studies reported Bartonella spp. in avian hosts. The present work aimed to investigate the occurrence and molecular identity of Bartonella spp. infecting birds in the Pantanal wetland, central-western Brazil using a multigene approach. For this purpose, blood samples were collected from 517 individuals from 13 avian orders in the states of Mato Grosso and Mato Groso do Sul. DNA was extracted from avian blood and 500/517 (96.7%) samples were positive in a conventional PCR targeting the avian β-actin gene. Nineteen (3.8%) out of 500 avian blood samples were positive in a qPCR assay for Bartonella spp. based on the nuoG gene. Among 19 avian blood DNA samples positive in the qPCR for Bartonella spp., 12 were also positive in the qPCR for Bartonella based on the 16S-23S RNA Intergenic region (ITS). In the PCR assays performed for molecular characterization, one 16S rRNA, three ribC, and one nuoG sequences were obtained. Based on BLASTn results, while 1 nuoG, 2 ribC, and 2 ITS sequences showed high identity to Bartonella henselae, one 16S rRNA and 2 ITS showed high similarity to Bartonella machadoae in the sampled birds. Bartonella spp. related to B. henselae and B. machadoae were detected, for the first time, in wild birds from the Brazilian Pantanal.
Identifiants
pubmed: 38443588
doi: 10.1007/s11259-024-10341-z
pii: 10.1007/s11259-024-10341-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Fundação de Amparo à Pesquisa do Estado de São Paulo
ID : 2020/14948-0
Organisme : Fundação de Amparo à Pesquisa do Estado de São Paulo
ID : 2022/08543-2
Organisme : Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
ID : 001
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
ID : 303701/2021-8
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Nature B.V.
Références
Álvarez-Fernández A, Breitschwerdt EB, Solano-Gallego L (2018) Bartonella infections in cats and dogs including zoonotic aspects. Parasit Vectors 11:1–21. https://doi.org/10.1186/s13071-018-3152-6
doi: 10.1186/s13071-018-3152-6
André MR, Dumler JS, Herrera HM et al (2016) Assessment of a quantitative 5’ nuclease real-time polymerase chain reaction using the nicotinamide adenine dinucleotide dehydrogenase gamma subunit (nuoG) for Bartonella species in domiciled and stray cats in Brazil. J Feline Med Surg 18:783–790. https://doi.org/10.1177/1098612X15593787
doi: 10.1177/1098612X15593787
pubmed: 26138812
André MR, Canola RAM, Braz JB et al (2019a) Aortic valve endocarditis due to Bartonella clarridgeiae in a dog in Brazil. Rev Bras Parasitol Veterinária 28:661–670. https://doi.org/10.1590/S1984-29612019078
doi: 10.1590/S1984-29612019078
André MR, Gutiérrez R, Ikeda P et al (2019b) Genetic diversity of Bartonella spp. in vampire bats from Brazil. Transbound Emerg Dis 66:2329–2341. https://doi.org/10.1111/tbed.13290
doi: 10.1111/tbed.13290
pubmed: 31287942
Anstead GM (2016) The centenary of the discovery of trench fever, an emerging infectious disease of World War 1. Lancet Infect Dis 16:e164–e172
doi: 10.1016/S1473-3099(16)30003-2
pubmed: 27375211
pmcid: 7106389
Battisti JM, Lawyer PG, Minnick MF (2015) Colonization of Lutzomyia verrucarum and Lutzomyia longipalpis Sand Flies (Diptera: Psychodidae) by Bartonella bacilliformis, the Etiologic Agent of Carrión’s Disease. PLoS Negl Trop Dis. https://doi.org/10.1371/journal.pntd.0004128
doi: 10.1371/journal.pntd.0004128
pubmed: 26436553
pmcid: 4593541
Benson DA, Cavanaugh M, Clark K, et al (2018) GenBank
Billeter SA, Diniz PPVP, Battisti JM et al (2009) Infection and replication of Bartonella species within a tick cell line. Exp Appl Acarol 49:193–208. https://doi.org/10.1007/s10493-009-9255-1
doi: 10.1007/s10493-009-9255-1
pubmed: 19242658
pmcid: 4465226
Billeter SA, Gundi VAKB, Rood MP, Kosoy MY (2011) 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 77:7850–7852. https://doi.org/10.1128/AEM.06012-11
doi: 10.1128/AEM.06012-11
pubmed: 21908631
pmcid: 3209143
Birtles RJ, Raoult D (1996) Comparison of partial citrate synthase gene (gltA) sequences for phylogenetic analysis of Bartonella species. Int J Syst Bacteriol 46:891–897. https://doi.org/10.1099/00207713-46-4-891
doi: 10.1099/00207713-46-4-891
pubmed: 8863415
Breitschwerdt EB, Kordick DL, Carolina N (2000) Bartonella infection in animals: carriership, reservoir potential, pathogenicity, and zoonotic potential for human. Infection 13:428–438
Breitschwerdt EB, Maggi RG, Chomel BB, Lappin MR (2010) Bartonellosis: An emerging infectious disease of zoonotic importance to animals and human beings. J Vet Emerg Crit Care 20:8–30
doi: 10.1111/j.1476-4431.2009.00496.x
Buffet JP, Kosoy M, Vayssier-Taussat M (2013) Natural history of Bartonella-infecting rodents in light of new knowledge on genomics, diversity and evolution. Future Microbiol 8:1117–1128
doi: 10.2217/fmb.13.77
pubmed: 24020740
Buhler KJ, Maggi RG, Gailius J et al (2020) Hopping species and borders: detection of Bartonella spp. in avian nest fleas and arctic foxes from Nunavut, Canada. Parasit Vectors 13:469. https://doi.org/10.1186/s13071-020-04344-3
doi: 10.1186/s13071-020-04344-3
pubmed: 32928287
Buhler KJ, Agar B, Galloway T, et al (2022) Arctic fleas are not fussy eaters: Bartonella bacteria may hitchhike between birds and mammals in a tundra ecosystem. Arct Sci. https://doi.org/10.1139/AS-2022-0014/ASSET/IMAGES/AS-2022-0014_F3.JPG
Bustin SA, Benes V, Garson JA et al (2009) The MIQE guidelines: Minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622. https://doi.org/10.1373/clinchem.2008.112797
doi: 10.1373/clinchem.2008.112797
pubmed: 19246619
Chomel BB, Kasten RW, Floyd-Hawkins K et al (1996) Experimental transmission of Bartonella henselae by the cat flea. J Clin Microbiol 34:1952–1956. https://doi.org/10.1088/0022-3727/49/25/254001
doi: 10.1088/0022-3727/49/25/254001
pubmed: 8818889
pmcid: 229161
Chomel BB, Boulouis HJ, Breitschwerdt EB, et al (2009) Ecological fitness and strategies of adaptation of Bartonella species to their hosts and vectors. Vet Res 40. https://doi.org/10.1051/VETRES/2009011
Colborn JM, Kosoy MY, Motin VL et al (2010) Improved detection of Bartonella DNA in mammalian hosts and arthropod vectors by real-time PCR using the NADH dehydrogenase gamma subunit (nuoG). J Clin Microbiol 48:4630–4633. https://doi.org/10.1128/JCM.00470-10
doi: 10.1128/JCM.00470-10
pubmed: 20926707
pmcid: 3008469
Comstedt P, Bergström S, Olsen B et al (2006) Migratory Passerine Birds as Reservoirs of Lyme Borreliosis in Europe. Emerg Infect Dis 12:1087–1102. https://doi.org/10.3201/eid1207.060127
doi: 10.3201/eid1207.060127
pubmed: 16836825
pmcid: 3291064
Cotté V, Bonnet S, Le Rhun D, et al (2008) Transmission of Bartonella henselae by Ixodes ricinus. 14:. https://doi.org/10.3201/eid1407.071110
De Pinho JB, Aragona M, Hakamada KYP, Mâ M (2017) Migration patterns and seasonal forest use by birds in the Brazilian Pantanal. Bird Conserv Int 27:371–387. https://doi.org/10.1017/S0959270916000290
doi: 10.1017/S0959270916000290
de Sena Oliveira MC, Silva PC, Hiromi OkinO C, et al (2018) Extração de DNA por FTA
de Sousa KCM, do Amaral RB, Herrera HM, et al (2018) Genetic Diversity of Bartonella spp. in Wild Mammals and Ectoparasites in Brazilian Pantanal. Microb Ecol 76:544–554 https://doi.org/10.1007/S00248-017-1138-0/FIGURES/4
Dias CM, do Amaral RB, Perles L, et al (2023) Multi-locus Sequencing Typing of Bartonella henselae isolates reveals coinfection with different variants in domestic cats from Midwestern Brazil. Acta Trop https://doi.org/10.1016/j.actatropica.2022.106742
do Amaral RB, Cardozo MV, Varani A de M, et al (2022a) First Report of Bartonella spp. in Marsupials from Brazil, with a Description of Bartonella harrusi sp. nov. and a New Proposal for the Taxonomic Reclassification of Species of the Genus Bartonella. Microorganisms 10:. https://doi.org/10.3390/microorganisms10081609
do Amaral RB, Cardozo MV, Varani A de M, et al (2022b) Bartonella machadoae sp. nov. isolated from wild rodents in the Pantanal wetland. Acta Trop 229:. https://doi.org/10.1016/j.actatropica.2022.106368
Elfving K, Olsen B, Bergström S, et al (2010) Dissemination of spotted fever rickettsia agents in Europe by migrating birds. PLoS One 5:. https://doi.org/10.1371/journal.pone.0008572
Faccini-Martínez ÁA, Márquez AC, Bravo-Estupiñan DM et al (2017) Bartonella quintana and Typhus Group Rickettsiae Exposure among Homeless Persons, Bogotá, Colombia. Emerg Infect Dis 23:1876–1879. https://doi.org/10.3201/eid2311.170341
doi: 10.3201/eid2311.170341
pubmed: 29048284
pmcid: 5652414
Fecchio A, Martins TF, Bell JA et al (2020) Host movement and time of year influence tick parasitism in Pantanal birds. Exp Appl Acarol 82:125–135. https://doi.org/10.1007/s10493-020-00530-1
doi: 10.1007/s10493-020-00530-1
pubmed: 32856170
Gonçalves LR, de Favacho AR, M, Roque ALR, et al (2016) Association of Bartonella species with wild and synanthropic rodents in different Brazilian biomes. Appl Environ Microbiol 82:7154–7164. https://doi.org/10.1128/AEM.02447-16
doi: 10.1128/AEM.02447-16
pubmed: 27736785
pmcid: 5118926
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98. citeulike-article-id:691774
Hamer SA, Goldberg TL, Kitron UD et al (2012) Wild birds and urban ecology of ticks and tick-borne pathogens, Chicago, Illinois, USA, 2005–2010. Emerg Infect Dis 18:1589–1595. https://doi.org/10.3201/eid1810.120511
doi: 10.3201/eid1810.120511
pubmed: 23017244
pmcid: 3471635
Harris MB, Tomas W, Mourão G et al (2005) Safeguarding the pantanal wetlands: Threats and conservation initiatives. Conserv Biol 19:714–720. https://doi.org/10.1111/j.1523-1739.2005.00708.x
doi: 10.1111/j.1523-1739.2005.00708.x
Hatai H, Ochiai K, Murakami M et al (2008) Prevalence of Fowl Glioma-Inducing Virus in Chickens of Zoological Gardens in Japan and Nucleotide Variation in the env Gene. J Vet Med Sci 70:469–474. https://doi.org/10.1292/JVMS.70.469
doi: 10.1292/JVMS.70.469
pubmed: 18525168
Hubert J, Erban T, Kopecky J et al (2017) Comparison of microbiomes between red poultry mite populations (Dermanyssus gallinae): predominance of Bartonella-like bacteria. Microb Ecol 74:947–960. https://doi.org/10.1007/s00248-017-0993-z
doi: 10.1007/s00248-017-0993-z
pubmed: 28534089
Iredell J, Blanckenberg D, Arvand M, et al (2003) Characterization of the Natural Population of Bartonella henselae by Multilocus Sequence Typing. 41:5071–5079 https://doi.org/10.1128/JCM.41.11.5071
Johnson G, Ayers M, Mcclure SCC et al (2003) Detection and Identification of Bartonella species Pathogenic for Humans by PCR Amplification Targeting the Riboflavin Synthase Gene (ribC). J Clin Microbiol 41:1069–1072. https://doi.org/10.1128/JCM.41.3.1069-1072.2003
doi: 10.1128/JCM.41.3.1069-1072.2003
pubmed: 12624031
pmcid: 150319
Kang J-G, Kim H-C, Choi C-Y et al (2013) Molecular detection of Anaplasma, Bartonella, and Borrelia Species in ticks collected from migratory birds from Hong-do Island, Republic of Korea. Vector-Borne Zoonotic Dis 13:215–225. https://doi.org/10.1089/vbz.2012.1149
doi: 10.1089/vbz.2012.1149
pubmed: 23428091
Klangthong K, Promsthaporn S, Leepitakrat S et al (2015) The Distribution and Diversity of Bartonella species in Rodents and Their Ectoparasites across Thailand. PLoS ONE 10:e0140856. https://doi.org/10.1371/journal.pone.0140856
doi: 10.1371/journal.pone.0140856
pubmed: 26484537
pmcid: 4617648
Korobitsyn IG, Moskvitina NS, Tyutenkov OY, et al (2021) Detection of tick-borne pathogens in wild birds and their ticks in Western Siberia and high level of their mismatch. Folia Parasitol (Praha) 68:1–13. https://doi.org/10.14411/FP.2021.024
Kosoy M, Goodrich I (2019) Comparative ecology of Bartonella and Brucella infections in wild carnivores. Front Vet Sci 5:322
doi: 10.3389/fvets.2018.00322
pubmed: 30662899
pmcid: 6328487
Król N, Militzer N, Stöbe E, et al (2021) Evaluating Transmission Paths for Three Different Bartonella spp. in Ixodes ricinus Ticks Using Artificial Feeding. Microorg 2021, Vol 9, Page 901 9:901 https://doi.org/10.3390/MICROORGANISMS9050901
La Scola B, Zeaiter Z, Khamis A, Raoult D (2003) Gene-sequence-based criteria for species definition in bacteriology: The Bartonella paradigm. Trends Microbiol 11:318–321. https://doi.org/10.1016/S0966-842X(03)00143-4
doi: 10.1016/S0966-842X(03)00143-4
pubmed: 12875815
Linardi PM, Costa LJ (2016) Ctenocephalides felis felis vs. Ctenocephalides canis (Siphonaptera: Pulicidae): some issues in correctly identify these species. Rev. Bras. Parasitol. Vet, Cham, pp 139–151
Louni M, Mana N, Bitam I, et al (2018) Body lice of homeless people reveal the presence of several emerging bacterial pathogens in northern Algeria. PLoS Negl Trop Dis 12:. https://doi.org/10.1371/journal.pntd.0006397
Maggi RG, Breitschwerdt EB (2005) Isolation of bacteriophages from Bartonella vinsonii subsp. berkhoffii and the characterization of Pap31 gene sequences from bacterial and phage DNA. J Mol Microbiol Biotechnol 9:44–51. https://doi.org/10.1159/000088145
doi: 10.1159/000088145
pubmed: 16254445
Maggi RG, Richardson T, Breitschwerdt EB, Miller JC (2020) Development and validation of a droplet digital PCR assay for the detection and quantification of Bartonella species within human clinical samples. J Microbiol Methods 176:106022. https://doi.org/10.1016/j.mimet.2020.106022
doi: 10.1016/j.mimet.2020.106022
pubmed: 32795640
Mammeria AB, Bitam I, Boutellis A, Kernif T (2014) First account of arthropods in the nest of the white stork, Ciconia ciconia, in Algeria, including the flea Ctenocephalides felis. Bull La Soc Zool Fr 139:201–215
Mascarelli PE, McQuillan M, Harms CA et al (2014) Bartonella henselae and B. koehlerae DNA in Birds. Emerg Infect Dis 20:490–492. https://doi.org/10.3201/eid2003.130563
doi: 10.3201/eid2003.130563
pubmed: 24589235
Mitsch WJ, Bernal B, Hernandez ME (2015) Ecosystem services of wetlands. Int J Biodivers Sci Ecosyst Serv Manag 11:1–4. https://doi.org/10.1080/21513732.2015.1006250
doi: 10.1080/21513732.2015.1006250
Müller A, Rodríguez E, Walker R et al (2018a) Occurrence and genetic diversity of Bartonella spp. (Rhizobiales: Bartonellaceae) and Rickettsia spp. (Rickettsiales: Rickettsiaceae) in Cat Fleas (Siphonaptera: Pulicidae) From Chile. J Med Entomol 55:1627–1632. https://doi.org/10.1093/jme/tjy124
doi: 10.1093/jme/tjy124
pubmed: 30085290
Müller A, Soto F, Sepúlveda M et al (2018b) Bartonella vinsonii subsp. berkhoffii and B. henselae in dogs. Epidemiol Infect 146:1202–1204. https://doi.org/10.1017/S0950268818001127
doi: 10.1017/S0950268818001127
pubmed: 29729679
Nasereddin A, Risheq A, Harrus S et al (2014) Bartonella species in fleas from Palestinian territories: Prevalence and genetic diversity. J Vector Ecol 39:261–270. https://doi.org/10.1111/jvec.12100
doi: 10.1111/jvec.12100
pubmed: 25424254
Nishide Y, Sugimoto TN, Watanabe K, et al (2022) Genetic variations and microbiome of the poultry red mite Dermanyssus gallinae. Front Microbiol 13:. https://doi.org/10.3389/fmicb.2022.1031535
Norman AF, Regnery R, Jameson P et al (1995) Differentiation of Bartonella-like isolates at the species level by PCR- restriction fragment length polymorphism in the citrate synthase gene. J Clin Microbiol 33:1797–1803. https://doi.org/10.1128/jcm.33.7.1797-1803.1995
doi: 10.1128/jcm.33.7.1797-1803.1995
pubmed: 7545181
pmcid: 228273
Nziza J, Tumushime JC, Cranfield M et al (2019) Fleas from domestic dogs and rodents in Rwanda carry Rickettsia asembonensis and Bartonella tribocorum. Med Vet Entomol 33:177–184. https://doi.org/10.1111/mve.12340
doi: 10.1111/mve.12340
pubmed: 30390316
Okaro U, Addisu A, Casanas B, Anderson B (2017) Bartonella species, an emerging cause of blood-culture-negative endocarditis. Clin Microbiol Rev 30:709–746
doi: 10.1128/CMR.00013-17
pubmed: 28490579
pmcid: 5475225
Oteo JA, Maggi R, Portillo A, et al (2017) Prevalence of Bartonella spp. by culture, PCR and serology, in veterinary personnel from Spain. Parasit Vectors 10:553. https://doi.org/10.1186/s13071-017-2483-z
Paziewska A, Harris PD, Zwolińska L et al (2010) Recombination within and between species of the alpha proteobacterium Bartonella infecting rodents. https://doi.org/10.1007/s00248-010-9735-1
Reed KD, Meece JK, Henkel JS, Shukla SK (2003) Birds, migration and emerging zoonoses: West Nile virus, Lyme disease, Influenza A and enteropathogens. Clin Med Res 1:5–12
doi: 10.3121/cmr.1.1.5
pubmed: 15931279
pmcid: 1069015
Salas LM, Espinoza-Carniglia M, Schmeisser NL et al (2019) Fleas of black rats (Rattus rattus) as reservoir host of Bartonella spp. in Chile. Peerj 2019:e7371. https://doi.org/10.7717/peerj.7371
doi: 10.7717/peerj.7371
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci 74:5463–5467. https://doi.org/10.1073/pnas.74.12.5463
doi: 10.1073/pnas.74.12.5463
pubmed: 271968
pmcid: 431765
Santana M de S, Hoppe EGL, Carraro PE, et al (2022) Molecular detection of vector-borne agents in wild boars (Sus scrofa) and associated ticks from Brazil, with evidence of putative new genotypes of Ehrlichia, Anaplasma, and haemoplasmas. Transbound Emerg Dis 69:e2808–e2831 https://doi.org/10.1111/tbed.14632
Sepúlveda-García P, Rubio A V., Salgado R, et al (2023) Molecular detection and characterization of Bartonella spp. in rodents from central and southern Chile, with emphasis on introduced rats (Rattus spp.). Comp Immunol Microbiol Infect Dis 100:. https://doi.org/10.1016/j.cimid.2023.102026
Sibley CG, Monroe BL (1991) Distribution and taxonomy of birds of the world
Stuckey MJ, Chomel BB, de Fleurieu EC et al (2017) Bartonella, bats and bugs: a review. Comp Immunol Microbiol Infect Dis 55:20–29. https://doi.org/10.1016/j.cimid.2017.09.001
doi: 10.1016/j.cimid.2017.09.001
pubmed: 29127990
Waldenström J, Lundkvist Å, Falk KI et al (2007) Migrating birds and tickborne encephalitis virus. Emerg Infect Dis 13:1215–1218. https://doi.org/10.3201/eid1308.061416
doi: 10.3201/eid1308.061416
pubmed: 17953095
pmcid: 2828075
Wechtaisong W, Bonnet SI, Chomel BB, et al (2021) microorganisms Investigation of Transovarial Transmission of Bartonella henselae in Rhipicephalus sanguineus sensu lato Ticks Using Artificial Feeding. https://doi.org/10.3390/microorganisms9122501
Williams HM, Dittmar K (2020) Expanding our view of Bartonella and its hosts: Bartonella in nest ectoparasites and their migratory avian hosts. Parasit Vectors 13:13. https://doi.org/10.1186/s13071-020-3896-7
doi: 10.1186/s13071-020-3896-7
pubmed: 31924262
pmcid: 6954622
Woolhouse MEJ, Gowtage-Sequeria S (2005) Host range and emerging and reemerging pathogens. Emerg Infect Dis 11:1842–1847. https://doi.org/10.3201/eid1112.050997
doi: 10.3201/eid1112.050997
pubmed: 16485468
pmcid: 3367654