Molecular detection of Babesia spp. and Rickettsia spp. in coatis (Nasua nasua) and associated ticks from midwestern Brazil.
Amblyomma dubitatum
Amblyomma sculptum
Babesia sp.
SFG Rickettsia sp.
Tick-borne pathogens
Zoonosis
Journal
Parasitology research
ISSN: 1432-1955
Titre abrégé: Parasitol Res
Pays: Germany
ID NLM: 8703571
Informations de publication
Date de publication:
May 2023
May 2023
Historique:
received:
29
01
2023
accepted:
02
03
2023
medline:
14
4
2023
pubmed:
9
3
2023
entrez:
8
3
2023
Statut:
ppublish
Résumé
Procyonids are reservoirs of many zoonotic infectious diseases, including tick-borne pathogens. The role of coatis (Nasua nasua) in the epidemiology of piroplasmids and Rickettsia has not been fully addressed in Brazil. To molecularly study these agents in coatis and associated ticks, animals were sampled in two urban areas in Midwestern Brazil. Blood (n = 163) and tick (n = 248) DNA samples were screened by PCR assays targeting the 18S rRNA and gltA genes of piroplasmids and Rickettsia spp., respectively. Positive samples were further molecularly tested targeting cox-1, cox-3, β-tubulin, cytB, and hsp70 (piroplasmid) and ompA, ompB, and htrA 17-kDa (Rickettsia spp.) genes, sequenced and phylogenetically analyzed. All coatis' blood samples were negative for piroplasmids, whereas five pools of ticks (2%) were positive for two different sequences of Babesia spp.. The first from Amblyomma sculptum nymphs was close (i.e., ≥ 99% nucleotide identity) to a Babesia sp. previously found in capybaras (Hydrochoerus hydrochaeris); the second from Amblyomma dubitatum nymphs and Amblyomma spp. larvae was identical (100% nucleotide identity) to a Babesia sp. detected in opossums (Didelphis albiventris) and associated ticks. Four samples (0.8%) were positive by PCR to two different Rickettsia spp. sequences, being the first from Amblyomma sp. larva identical to Rickettsia belli and the second from A. dubitatum nymph identical to Rickettsia species from Spotted Fever Group (SFG). The detection of piroplasmids and SFG Rickettsia sp. highlights the importance of Amblyomma spp. in the maintenance of tick-borne agents in urban parks where humans and wild and domestic animals are living in sympatry.
Identifiants
pubmed: 36890298
doi: 10.1007/s00436-023-07815-5
pii: 10.1007/s00436-023-07815-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1151-1158Subventions
Organisme : Fundação de Amparo à Pesquisa do Estado de São Paulo
ID : 2019/15150-4
Organisme : Fundação de Amparo à Pesquisa do Estado de São Paulo
ID : 2020/12037-0
Organisme : NextGenerationEU-MUR PNRR Extended Partnership initiative on Emerging Infectious Diseases
ID : PE00000007
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
ID : 308768/2017-5
Organisme : Conselho Nacional de Desenvolvimento Científico e Tecnológico
ID : 303701/2021-8
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Abdad MY, Abou Abdallah R, Fournier PE, Stenos J, Vasoo S (2018) A concise review of the epidemiology and diagnostics of rickettsioses: Rickettsia and Orientia spp. J Clin Microbiol 56(8):e01728-e1817
pubmed: 29769278
pmcid: 6062794
doi: 10.1128/JCM.01728-17
André MR (2018) Diversity of Anaplasma and Ehrlichia/Neoehrlichia agents in terrestrial wild carnivores worldwide: implications for human and domestic animal health and wildlife conservation. Front Vet Sci 5:293. https://doi.org/10.3389/fvets.2018.00293
doi: 10.3389/fvets.2018.00293
pubmed: 30533417
pmcid: 6265506
Baba K, Kaneda T, Nishimura H, Sato H (2013) Molecular detection of spotted fever group Rickettsia in feral raccoons (Procyon lotor) in the western part of Japan. J Vet Med Sci 75(2):195–197
pubmed: 22986299
doi: 10.1292/jvms.12-0143
Barbieri AR, Romero L, Labruna MB (2012) Rickettsia bellii infecting Amblyomma sabanerae ticks in El Salvador. Pathog Glob Health 106(3):188–189
pubmed: 23265378
pmcid: 4001580
doi: 10.1179/2047773212Y.0000000022
Barbosa AD, Austen J, Portas TJ, Amigo JÁ, Ahlstrom LA, Oskam CL, Irwin PJ (2019) Sequence analyses at mitochondrial and nuclear loci reveal a novel Theileria sp and AID in the phylogenetic resolution of piroplasms from Australian marsupials and ticks. PLoS One 12:e0225822
doi: 10.1371/journal.pone.0225822
Barreto WTG, Herrera HM, de Macedo GC, Rucco AC, de Assis WO, Oliveira-Santos LG, de Oliveira Porfírio GE (2021) Density and survivorship of the South American coati (Nasua nasua) in urban areas in Central-Western Brazil. Hystrix 32(1):82
Bermúdez CSE, Troyo A (2018) A review of the genus Rickettsia in Central America. Res Rep Trop Med 9:103
pubmed: 30050361
pmcid: 6047601
Birkenheuer AJ, Marr HS, Hladio N, Acton AE (2007) Molecular evidence of prevalent dual piroplasma infections in North American raccoons (Procyon lotor). Parasitol 135:33–37
doi: 10.1017/S0031182007003538
Birkenheuer AJ, Levy MG, Breitschwerdt EB (2003) Development and evaluation of a seminested PCR for detection and differentiation of Babesia gibsoni (Asian genotype) and B. canis DNA in canine blood samples. J Clin Microb 41(9): 4172–4177
Black W, Piesman J (1994) Phylogeny of hard-and soft-tick taxa (Acari: Ixodida) based on mitochondrial 16S rDNA sequences. Proc Natl Acad Sci USA 91:10034–10038
pubmed: 7937832
pmcid: 44952
doi: 10.1073/pnas.91.21.10034
Campos JBV, Martins FS, de Oliveira CE, Taveira AA, Oliveira JR, Gonçalves LR, Cordeiro MD, Calchi AC, de Campos BL, Serpa MCA, Barbieri ARM, Labruna MB, Machado RZ, de Andrade GB, André MR, Herrera HM (2021) Tick-borne zoonotic agents infecting horses from an urban area in Midwestern Brazil: epidemiological and hematological features. Trop Anim Health Prod 53(5):475
pubmed: 34553290
pmcid: 8457776
doi: 10.1007/s11250-021-02887-w
Campos JBV, Martins FS, Macedo GC, Barreto WTG, Oliveira CE, Barbieri ARM, Labruna MB, Oliveira-Santos LGR, Herrera HM (2022) Serological exposure of spotted fever group Rickettsia in capybaras (Hydrochoerus hydrochaeris) from urban parks in Campo Grande, Brazilian Midwest. Rev Soc Bras Med Trop 55(e0192):2022. https://doi.org/10.1590/0037-8682-0192-2022.eCollection
doi: 10.1590/0037-8682-0192-2022.eCollection
Castellaw AH, Chenney EF, Varela-Stokes AS (2011) Tick-borne disease agents in various wildlife from Mississippi. Vector-Borne Zoonotic Dis 11(4):439–442
pubmed: 20846016
doi: 10.1089/vbz.2009.0221
Clark K, Savick K, Butler J (2012) Babesia microti in rodents and raccoons from northeast Florida. J Parasitol 98(6):1117–1121
pubmed: 22646851
doi: 10.1645/GE-3083.1
Cleaveland S, Laurenson MK, Taylor LH (2001) Diseases of humans and their domestic mammals: pathogen characteristics, host range and the risk of emergence. Philos Trans R Soc Lond B Biol Sci 356(1411):991–999
pubmed: 11516377
pmcid: 1088494
doi: 10.1098/rstb.2001.0889
Corduneanu A, Hrazdilová K, Sándor AD, Matei IA, Ionică AM, Barti L, Ciocănău MA, Măntoiu DȘ, Coroiu I, Hornok S, Fuehrer HP, Leitner N, Bagó Z, Stefke K, Modrý D, Mihalca AD (2017) Babesia vesperuginis, a neglected piroplasmid: new host and geographical records, and phylogenetic relations. Parasit Vectors 10(1):598
pubmed: 29208011
pmcid: 5718032
doi: 10.1186/s13071-017-2536-3
Criado-Fornelio A, Buling A, Casado N, Gimenez C, Ruas J, Wendt L, Barba-Carretero J (2009) Molecular characterization of arthropod-borne hematozoans in wild mammals from Brazil, Venezuela and Spain. Acta Parasitol 54(3):187–193
doi: 10.2478/s11686-009-0031-5
Dantas-Torres F, Martins TF, Muñoz-Leal S, Onofrio VC, Barros-Battesti DM (2019) Ticks (Ixodida: Argasidae, Ixodidae) of Brazil: updated species checklist and taxonomic keys. Ticks Tick-Borne Dis 10(6):101252
pubmed: 31255534
doi: 10.1016/j.ttbdis.2019.06.012
De Sousa KCM, Fernandes MP, Herrera HM, Freschi CR, Machado RZ, André MR (2018) Diversity of piroplasmids among wild and domestic mammals and ectoparasites in Pantanal wetland. Brazil Ticks Tick-Borne Dis 9(2):245–253
pubmed: 28941935
doi: 10.1016/j.ttbdis.2017.09.010
Emmons L, Helgen K (2016) Nasua nasua. The IUCN Red List of Threatened Species 2016: e.T41684A45216227. https://doi.org/10.2305/IUCN.UK.2016-1.RLTS.T41684A45216227.en
Friedhoff KT (2018) Transmission of Babesia. In: Babesiosis of domestic animals and man 23–52 CRC Press
Garrett KB, Hernandez SM, Balsamo G, Barron H, Beasley JC, Brown JD, Cloherty E, Farid H, Gabriel M, Groves B, Hamer S, Hill J, Lewis M, McManners K, Nemeth N, Oesterle P, Ortiz S, Peshock L, Schnellbacher R, Schott R, Yabsley MJ (2019) Prevalence, distribution, and diversity of cryptic piroplasm infections in raccoons from selected areas of the United States and Canada. Int J Parasitol Paras Wildl 9:224–233
doi: 10.1016/j.ijppaw.2019.05.007
Goethert HK, Telford SR (2003) What is Babesia microti? Parasitol 127(4):301–309
doi: 10.1017/S0031182003003822
Gonçalves LR, Paludo G, Bisol TB, Perles L, de Oliveira LB, de Oliveira CM, André MR (2021) Molecular detection of piroplasmids in synanthropic rodents, marsupials, and associated ticks from Brazil, with phylogenetic inference of a putative novel Babesia sp. from white-eared opossum (Didelphis albiventris). Parasitol Res 20(10):3537–3546
doi: 10.1007/s00436-021-07284-8
Greay TL, Zahedi A, Krige A, Owens JM, Rees RL, Ryan UM, Oskam CL, Irwin PJ (2018) Endemic, exotic and novel apicomplexan parasites detected during a national study of ticks from companion animals in Australia. Parasit Vectors 11:197
pubmed: 29558984
pmcid: 5859549
doi: 10.1186/s13071-018-2775-y
Hersh MH, Tibbetts M, Strauss M, Ostfeld RS, Keesing F (2012) Reservoir competence of wildlife host species for Babesia microti. Emerg Infec Dis 18(12):1951–1957
doi: 10.3201/eid1812.111392
Hildebrand J, Perec-Matysiak A, Popiołek M, Merta D, Myśliwy I, Buńkowska-Gawlik K (2022) A molecular survey of spotted fever group rickettsiae in introduced raccoons (Procyon lotor). Parasit Vect 15(1):1–8
doi: 10.1186/s13071-022-05280-0
Jalovecka M, Hajdusek O, Sojka D, Kopacek P, Malandrin L (2018) The complexity of piroplasms life cycles. Front Cell Infect Microbiol 248:8. https://doi.org/10.3389/fcimb.2018.00248
doi: 10.3389/fcimb.2018.00248
Jalovecka M, Sojka D, Ascencio M, Schnittger L (2019) Babesia life cycle–when phylogeny meets biology. Trends Parasitol 13:356–368. https://doi.org/10.1016/j.pt.2019.01.007
doi: 10.1016/j.pt.2019.01.007
Jefferies R, Ryan UM, Irwin PJ (2007) PCR–RFLP for the detection and differentiation of the canine piroplasm species and its use with filter paper-based technologies. Vet Parasitol 144:20–27
pubmed: 17127005
doi: 10.1016/j.vetpar.2006.09.022
Jinnai M, Kawabuchi-Kurata T, Tsuji M, Nakajima R, Fujisawa K, Nagata S, Ishihara C (2009) Molecular evidence for the presence of new Babesia species in feral raccoons (Procyon lotor) in Hokkaido. Japan Vet Parasitol 162(3–4):241–247
pubmed: 19349121
doi: 10.1016/j.vetpar.2009.03.016
Kawabuchi T, Tsuji M, Sado A, Matoba Y, Asakawa M, Ishihara C (2005) Babesia microti-like parasites detected in feral raccoons (Procyon lotor) captured in Hokkaido. Japan J Vet Med Sci 67(8):825–827
pubmed: 16141672
doi: 10.1292/jvms.67.825
Labruna MB, Whitworth T, Bouyer DH, McBride J, Camargo LMA, Camargo EP, Walker DH (2004a) Rickettsia bellii and Rickettsia amblyommii in Amblyomma ticks from the state of Rondônia, Western Amazon, Brazil. J Med Entomol 41:1073–1081
pubmed: 15605647
doi: 10.1603/0022-2585-41.6.1073
Labruna MB, Whitworth T, Horta MC, Bouyer DH, McBride JW, Pinter A, Walker DH (2004b) Rickettsia species infecting Amblyomma cooperi ticks from an area in the state of Sao Paulo, Brazil, where Brazilian spotted fever is endemic. J Clin Microbiol 42(1):90–98
pubmed: 14715737
pmcid: 321730
doi: 10.1128/JCM.42.1.90-98.2004
Labruna MB, Pacheco RC, Richtzenhain LJ, Szabo MP (2007) Isolation of Rickettsia rhipicephali and Rickettsia bellii from Haemaphysalis juxtakochi ticks in the state of São Paulo. Brazil Appl Environ Microbiol 73(3):869–873
pubmed: 17142361
doi: 10.1128/AEM.02249-06
Labruna MB, Mattar S, Nava S, Bermudez S, Venzal JM, Dolz G, Zavala-Castro J (2011) Rickettsioses in Latin America, Caribbean, Spain and Portugal. MVZ Córdoba 16(2):2435–2457
doi: 10.21897/rmvz.282
Magalhães-Matos PC, de Araújo IM, de Almeida Valim JR, Ogrzewalska M, Guterres A, Cordeiro MD, da Fonseca AH (2022) Detection of Rickettsia spp. in ring-tailed coatis (Nasua nasua) and ticks of the Iguaçu National Park Brazilian Atlantic Rainforest. Ticks Tick-Borne Dis 13(2):101891
pubmed: 34942561
doi: 10.1016/j.ttbdis.2021.101891
Martins TF, Onofrio VC, Barros-Battesti DM, Labruna MB (2010) Nymphs of the genus Amblyomma (Acari: Ixodidae) of Brazil: descriptions, redescriptions, and identification key. Ticks Tick-Borne Dis 1(2):75–99
pubmed: 21771514
doi: 10.1016/j.ttbdis.2010.03.002
McIntosh D, Bezerra RA, Luz HR, Faccini JLH, Gaiotto FA, Giné GAF, Albuquerque GR (2015) Detection of Rickettsia bellii and Rickettsia amblyommii in Amblyomma longirostre (Acari: Ixodidae) from Bahia state, northeast Brazil. Braz J Microbiol 46:879–883
pubmed: 26413074
pmcid: 4568851
doi: 10.1590/S1517-838246320140623
Mehrkens LR, Shender LA, Yabsley MJ, Shock BC, Chinchilla FA, Suarez J, Gilardi KV (2013) White-nosed coatis (Nasua narica) are a potential reservoir of Trypanosoma cruzi and other potentially zoonotic pathogens in Monteverde. Costa Rica J Wildl Dis 49(4):1014–1018
pubmed: 24502732
doi: 10.7589/2013-01-005
Moraes-Filho J, Costa FB, Gerardi M, Soares HS, Labruna MB (2018) Rickettsia rickettsii co-feeding transmission among Amblyomma aureolatum ticks. Emerg Infec Dis 24(11):2041
doi: 10.3201/eid2411.180451
Neves LC, Sousa-Paula LCD, Dias AS, da Silva BBF, Paula WVDF, de Paula LGF, Dantas-Torres F (2023) Detection of an undescribed Babesia sp. in capybaras and Amblyomma ticks in Central-Western Brazil. Animals 13(1):94
pubmed: 36611703
pmcid: 9817508
doi: 10.3390/ani13010094
Otranto D, Cantacessi C, Pfeffer M, Dantas-Torres F, Brianti E, Deplazes P, Genchi C, Guberti V, Capelli G (2015) The role of wild canids and felids in spreading parasites to dogs and cats in Europe: Part I: Protozoa and tick-borne agents. Vet Parasitol 213:12–23
pubmed: 26003669
doi: 10.1016/j.vetpar.2015.04.022
Pacheco RC, Horta MC, Moraes-Filho J, Ataliba AC, Pinter A, Labruna MB (2007) Rickettsial infection in capybaras (Hydrochoerus hydrochaeris) from São Paulo, Brazil: serological evidence for infection by Rickettsia bellii and Rickettsia parkeri. Biomedica 27(3):364–371
pubmed: 18320102
doi: 10.7705/biomedica.v27i3.199
Parola P, Paddock CD, Socolovschi C, Labruna MB, Mediannikov O, Kernif T, Raoult D (2013) Update on tick-borne rickettsioses around the world: a geographic approach. Clin Microbiol Rev 26(4):657–702
pubmed: 24092850
pmcid: 3811236
doi: 10.1128/CMR.00032-13
Perles L, Martins TF, Barreto WTG, Carvalho de Macedo G, Herrera HM, Mathias LA, André MR (2022) Diversity and seasonal dynamics of ticks on ring-tailed coatis Nasua nasua (Carnivora: Procyonidae) in two urban areas from Midwestern Brazil. Animals 12(3):293
pubmed: 35158617
pmcid: 8833741
doi: 10.3390/ani12030293
Polo G, Mera Acosta C, Labruna MB, Ferreira F (2017) Transmission dynamics and control of Rickettsia rickettsii in populations of Hydrochoerus hydrochaeris and Amblyomma sculptum. PLoS Negl Trop Dis 11(6):e0005613
pubmed: 28582429
pmcid: 5472331
doi: 10.1371/journal.pntd.0005613
Rainwater KL, Marchese K, Slavinski S, Humberg LA, Dubovi EJ, Jarvis JA, Calle PP (2017) Health survey of free-ranging raccoons (Procyon lotor) in Central Park, New York, New York, USA: implications for human and domestic animal health. J Wildl Dis 53(2):272–284
pubmed: 28135131
doi: 10.7589/2016-05-096
Regnery RL, Spruill CL, Plikaytis B (1991) Genotypic identification of rickettsiae and estimation of intraspecies sequence divergence for portions of two rickettsial genes. J Bacteriol 173(5):1576–1589
pubmed: 1671856
pmcid: 207306
doi: 10.1128/jb.173.5.1576-1589.1991
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574
pubmed: 12912839
doi: 10.1093/bioinformatics/btg180
Roux V, Raoult D (2000) Phylogenetic analysis of members of the genus Rickettsia using the gene encoding the outer-membrane protein rOmpB (ompB). Int J Syst Evol Microbiol 50(4):1449–1455
pubmed: 10939649
doi: 10.1099/00207713-50-4-1449
Sakai RK, Costa FB, Ueno TE, Ramirez DG, Soares JF, Fonseca AH, Barros-Battesti DM (2014) Experimental infection with Rickettsia rickettsii in an Amblyomma dubitatum tick colony, naturally infected by Rickettsia bellii. Ticks Tick-Borne Dis 5(6):917–923
pubmed: 25108783
doi: 10.1016/j.ttbdis.2014.07.003
Sashika M, Abe G, Matsumoto K, Inokuma H (2010) Molecular survey of rickettsial agents in feral raccoons (Procyon lotor) in Hokkaido Japan. Japanese J Infec Diseases 63(5):353–354
doi: 10.7883/yoken.63.353
Schnittger L, Ganzinelli S, Bhoora R (2022) The Piroplasmida Babesia, Cytauxzoon, and Theileria in farm and companion animals: species compilation, molecular phylogeny, and evolutionary insights. Parasitol Res 121:1207–1245
pubmed: 35098377
doi: 10.1007/s00436-022-07424-8
Soares JF, Girotto A, Brandão PE, Da Silva AS, França RT, Lopes STA, Labruna MB (2011) Detection and molecular characterization of a canine piroplasm from Brazil. Vet Parasitol 180:203–208
pubmed: 21489694
doi: 10.1016/j.vetpar.2011.03.024
Souza CE, Moraes-Filho J, Ogrzewalska M, Uchoa FC, Horta MC, Souza SS, Labruna MB (2009) Experimental infection of capybaras Hydrochoerus hydrochaeris by Rickettsia rickettsii and evaluation of the transmission of the infection to ticks Amblyomma cajennense. Vet Parasitol 161(1–2):116–121
pubmed: 19147293
doi: 10.1016/j.vetpar.2008.12.010
Stöver BC, Müller KF (2010) TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinform 11(1):1–9
doi: 10.1186/1471-2105-11-7
Thompson CS, Mangold AJ, Félix ML, Carvalho L, Armúa-Fernández MT, Venzal JM (2018) Molecular evidence of Babesia species in Procyon cancrivorus (Carnivora, Procyonidae) in Uruguay. Vet Parasitol Reg Stud Rep 13:230–233
Tsuji M, Zamoto A, Kawabuchi T, Kataoka T, Nakajima R, Asakawa M, Ishihara C (2006) Babesia microti-like parasites detected in Eurasian red squirrels (Sciurus vulgaris orientis) in Hokkaido. Japan J Vet Med Sci 68(7):643–646
pubmed: 16891774
doi: 10.1292/jvms.68.643
Tufts DM, Goodman LB, Benedict MC, Davis AD, VanAcker MC, Diuk-Wasser M (2021) Association of the invasive Haemaphysalis longicornis tick with vertebrate hosts, other native tick vectors, and tick-borne pathogens in New York City, USA. Int J Parasitol 51(2–3):149–157
pubmed: 33130214
doi: 10.1016/j.ijpara.2020.08.008
Uilenberg G (2006) Babesia—a historical overview. Vet Parasitol 138(1–2):3–10
pubmed: 16513280
doi: 10.1016/j.vetpar.2006.01.035
Yabsley MJ, Shock BC (2013) Natural history of zoonotic Babesia: role wildlife reservoirs. Int J Parasitol Par Wildl 2:18–31
doi: 10.1016/j.ijppaw.2012.11.003
Zamoto A, Tsuji M, Wei Q, Cho SH, Shin EH, Kim TS, Leonova GN, Hagiwara K, Asakawa M, Kariwa H, Takashima I, Ishihara C (2004) Epizootiologic survey for Babesia microti among small wild mammals in northeastern Eurasia and a geographic diversity in the beta-tubulin gene sequences. J Vet Med Sci 66(7):785–792
pubmed: 15297749
doi: 10.1292/jvms.66.785
Zemtsova G, Killmaster LF, Mumcuoglu KY, Levin ML (2010) Co-feeding as a route for transmission of Rickettsia conorii israelensis between Rhipicephalus sanguineus ticks. Exp Appl Acarol 52(4):383–392
pubmed: 20589416
doi: 10.1007/s10493-010-9375-7