Abstract
Ticks and fleas are arthropods widely distributed around the world involved in the transmission of various vector-borne diseases (VBDs), including Brazilian Spotted Fever (BSF), Baggio-Yoshinari Syndrome and the plague, with outstanding consequences for the public health. The aim of this study was to investigate the presence of Rickettsia spp., Borrelia spp. and Yersinia pestis in arthropods collected from dogs, cats and horses living in the state of Pernambuco, Northeastern Brazil. From January 2017 to April 2019, ectoparasites were collected, morphologically identified and molecularly analysed through PCR and sequencing. In total 401 specimens were collected from 86 animals, being 68% (n = 273) and 32% (n = 128) from rural and urban areas, respectively. The most commonly detected species were the ticks Dermacentor nitens, Amblyomma sculptum, Rhipicephalus sanguineus sensu lato (s.l.), Rhipicephalus microplus, and Amblyomma ovale, and the fleas Ctenocephalides felis and Ctenocephalides canis. DNA of Rickettsia felis was detected in D. nitens collected from horses, and C. felis, and R. sanguineus s.l. collected from dogs. All samples scored negative for Borrelia spp. and Y. pestis DNA. This study provides valuable data on ectoparasite fauna from domestic animals and identifies the circulation of a zoonotic pathogen (i.e., R. felis) in the population of the arthropods assessed. Therefore, preventive measures should be adopted in order to reduce the risk of occurrence of neglected VBD caused by this pathogen in animal and human hosts.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aguirre AAR, Garcia MV, Costa IND, Csordas BG, Rodrigues VDS, Medeiros JF, Andreotti R (2018) New records of tick-associated spotted fever group Rickettsia in an Amazon savannah ecotone, Brazil. Tick Tick-Borne Dis 9(4):1038–1044. https://doi.org/10.1016/j.ttbdis.2018.03.015
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Angerami RN, Câmara M, Pacola MR, Rezende RCM, Duarte RMR, Nascimento EMM, Colombo S, Santos FCP, Leite RM, Katz G, Silva LJ (2012) Features of Brazilian spotted fever in two different endemic areas in Brazil. Tick Tick-Borne Dis 3(5–6):346–348. https://doi.org/10.1016/j.ttbdis.2012.10.010
Aragão H, Fonseca F (1961) Notas de Ixodologia. VII. Lista e chave para os representantes da fauna ixodológica brasileira. Mem Inst Oswaldo Cruz 59:15–130. https://doi.org/10.1590/S0074-02761961000200001
Ayres M, Ayres Júnior M, Ayres DL, Santos AA (2007) BIOESTAT—Aplicações estatísticas nas áreas das ciências bio-médicas. Ong Mamiraua, Belém, PA
Azad AF, Sacci JB Jr, Nelson WM, Dasch GA, Schmidtmann ET, Carl M (1992) Genetic characterization and transovarial transmission of a typhus-like rickettsia found in cat fleas. Proc Natl Acad Sci USA 89:43–46. https://doi.org/10.1073/pnas.89.1.43
Barker SC, Murrell A (2004) Systematic and evaluation of ticks with a list of valid genus and species names. J Parasitol 129:15–36. https://doi.org/10.1017/s0031182004005207
Brasil (2008) Manual de vigilância e controle da peste. Ministério da Saúde, Brasília
Brasil (2017) Guia de Vigilância em Saúde: volume 3/1ª. ed. atual. Ministério da Saúde, Brasília
Brown LD, Macaluso KR (2016) Rickettsia felis an emerging flea-borne rickettsiosis. Curr Trop Med Rep 3(2):27–39. https://doi.org/10.1007/s40475-016-0070-6
Carranza-Tamayo CO, Costa JNG, Bastos WM (2012) Lyme disease in the state of Tocantins, Brazil: report of the first cases. Braz J Infect Dis 16(6):586–589. https://doi.org/10.1016/j.bjid.2012.07.013
Centers for Disease Control and Prevetion – CDC (2019) Plague worldwide—plague cases by Country 2010–2015. https://www.cdc.gov/plague/maps/index.html Acessed 20 Apr 2020
Del Fiol FS, Junqueira FM, Rocha MCP, Toledo MI, Barberato Filho S (2010) A febre maculosa no Brasil. Rev Panam Salud Pública 27(6):461–466. https://doi.org/10.1590/S1020-49892010000600008
Ehlers J, Poppert S, Ratovonamana RY, Ganzhorn JU, Tappe D, Krüger A (2019) Ectoparasites of endemic and domestic animals in southwest Madagascar. Acta Trop 196:83–92. https://doi.org/10.1016/j.actatropica.2019.05.008
Esch KJ, Petersen CA (2013) Transmission and epidemiology of zoonotic protozoal diseases of companion animals. Clin Microbiol Rev 26(1):58–85. https://doi.org/10.1128/CMR.00067-12
Estrada-Peña A, Ayllón N, De La Fuente J (2012) Impact of climate trends on tick-borne pathogen transmission. Front Physiol 3:64. https://doi.org/10.3389/fphys.2012.00064
Ewald PW (1983) Host-parasite relations vectors and the evolution of disease severity. Annu Rev Ecol Evol Syst 14:465–485. https://doi.org/10.1146/annurev.es.14.110183.002341
Guimarães JH, Tucci CE, Barros-Battesti DM (2001) Ectoparasitos de Importância Veterinária. Plêide/FAPESP, São Paulo, SP
Hinnebusch J, Schwan TG (1993) New method for plague surveillance using polymerase chain reaction to detect Yersinia pestis in fleas. J Clin Microbiol 31(6):1511–1514
Kumsa B, Abiy Y, Abunna F (2019) Ectoparasites infesting dogs and cats in Bishoftu, central Oromia. Ethiopia Vet Parasitol Reg Stud Rep 15:100263. https://doi.org/10.1016/j.vprsr.2019.100263
Labruna MB, Homem VSF, Heinemann MB, Neto JSF (2000) Ticks (Acari: Ixodidae) associated with rural dogs in Uruará, Eastern Amazon, Brazil. J Med Entomol 37:774–776. https://doi.org/10.1603/0022-2585-37.5.774
Labruna MB, Whitworth T, Horta MC, Bouyer DH, McBride JW, Pinter A, Popov V, Gennari SM, Walker DH (2004) Rickettsia species infecting Amblyomma cooperi ticks from an area in the state of São Paulo, Brazil, where Brazilian spotted fever is endemic. J Clin Microbiol 42(1):90–98. https://doi.org/10.1128/JCM.42.1.90-98.2004
Linardi PM (2017) Checklist dos Sifonápteros (Insecta) do Estado do Mato Grosso. Brasil Iheringia Sér Zool 107:e2017148. https://doi.org/10.1590/1678-4766e2017148
Linardi MP, Guimarães LR (2000) Sifonápteros do Brasil. Museu de Zoologia, São Paulo, SP
Moraes-Filho J (2017) Febre maculosa brasileira. Rev Edu Cont Med Vet Zoo CRMV-SP 15:38–45
Ogden NH, Lindsay LR (2016) Effects of climate and climate change on vectors and vector-borne diseases: ticks are different. Trends Parasitol 32(8):646–656. https://doi.org/10.1016/j.pt.2016.04.015
Oliveira RP, Galvão MAM, Mafra CL, Chamone CB, Calic SB, Silva SU, Walker DH (2002) Rickettsia felis in Ctenocephalides spp. fleas, Brazil. Emerg Infect Dis 8(3):317–319. https://doi.org/10.3201/eid0803.010301
Oliveira SV, Pereira SVC, Pinna FV, Fonseca LX, Serra-Freire NM, Cardoso KM, Borsoi ABP, Amorim M, Caldas EP, Gazeta GS (2016) Vigilância de ambientes da febre maculosa: explorando as áreas silenciosas do Brasil. Rev Pan-Amazônica Saúde 7(3):65–72. https://doi.org/10.5123/S2176-62232016000300008
Oliveira SV, Costa RMF, Ferreira G, Pereira SVC, Amorim M, Monteiro MFM, Alves LC, Gazeta GS (2018) Fatal case of spotted fever in a patient from Northeastern Brazil. Rev Inst Med Trop São Paulo 60:e21. https://doi.org/10.1590/S1678-9946201860021
Pacheco RC, Moraes-Filho J, Guedes E, Silveira I, Richtzenhain LJ, Leite RC, Labruna MB (2011) Rickettsial infections of dogs, horses and ticks in Juiz de Fora, southeastern Brazil, and isolation of Rickettsia rickettsii from Rhipicephalus sanguineus ticks. Med Vet Entomol 25(2):148–155. https://doi.org/10.1111/j.1365-2915.2010.00915.x
Pérez-Osorio CE, Zavala-Velázquez JE, Arias-León JJ, Zavala-Castro JE (2008) Rickettsia felis as emergent global threat for humans. Emerg Infect Dis 7:1019–1023. https://doi.org/10.3201/eid1407.071656
Petersen LR, Beard CB, Visser SN (2019) Combatting the increasing threat of vector-borne disease in the United States with a national vector-borne disease prevention and control system. Am J Trop Med Hyg 100(2):242–245. https://doi.org/10.4269/ajtmh.18-0841
Pritt BS, Mead PS, Johnson DKH, Neitzel DF, Respicio-Kingry LB, Davis JP, Schiffman E, Sloan LM, Schriefer ME, Replogle AJ, Paskewitz SM, Ray JA, Bjork J, Steward CR, Deedon A, Lee X, Kingry LC, Miller TK, Feist MA, Theel ES, Patel R, Irish CL, Petersen JM (2016) Identification of a novel pathogenic Borrelia species causing Lyme borreliosis with unusually high spirochaetaemia: a descriptive study. Lancet Infec Dis 16:556–564. https://doi.org/10.1016/S1473-3099(15)00464-8
Ramos RAN, Campbell BE, Whittle A, Lia RP, Montarsi F, Parisi A, Dantas-Torres F, Wall R, Otranto D (2015) Occurrence of Ixodiphagus hookeri (Hymenoptera: Encyrtidae) in Ixodes ricinus (Acari: Ixodidae) in Southern Italy. Tick Tick-Borne Dis 6(3):234–236. https://doi.org/10.1016/j.ttbdis.2015.01.001
Raoult D, La Scola B, Enea M, Fournier P-E, Roux V, Fenollar F, Galvão MA, de Lamballerie X (2001) A flea-associated rickettsia pathogenic for humans. Emerg Infect Dis 7:73–81. https://doi.org/10.3201/eid0701.010112
Rezende J, Lopes FA, Alves FCG, Bruno AR, Moreno SE, Costa IP (2016) Detection of Borrelia burgdorferi sensu lato in Mato Grosso do Sul. Brazil JSM Trop Med Res 1:1003
Rodrigues PCG, Chagas MGS, Silva FBR, Pimentel RMM (2008) Ecologia dos Brejos de Altitude do agreste pernambucano. Rev Geogr 25(3):20–34
Rosa Neto NS, Gauditano G, Yoshinari NH (2014) Chronic lymphomonocytic meningoencephalitis, oligoarthritis and erythema nodosum: report of Baggio-Yoshinari syndrome of long and relapsing evolution. Rev Bras Reumatol 54(2):148–151. https://doi.org/10.1016/j.rbr.2014.03.010
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74(12):5463–5467. https://doi.org/10.1073/pnas.74.12.5463
Santos M, Ribeiro-Rodrigues R, Talhari C, Ferreira LCL, ZelgerB TS (2011) Presence of Borrelia burgdorferi “Sensu Lato” in patients with morphea from the Amazonic region in Brazil. Int J Dermatol 50(11):1373–1378. https://doi.org/10.1111/j.1365-4632.2011.05081.x
Santos LS, Barros Silva HP, Pereira ECG (2014) Cerrado em área disjunta em brejo de altitude no Agreste pernambucano. Brasil Bol Goiano Geogr 34(2):337–353
Semenza JC, Suk JE (2018) Vector-borne diseases and climate change: a European perspective. FEMS Microbiol Lett 1(2):365. https://doi.org/10.1093/femsle/fnx244
Simond PL (1898) La propagation de la peste. Ann Inst Pasteur 10:626–687
Sonenshine DE (2018) Range expansion of tick disease vectors in North America: implications for spread of Tick-borne disease. Int J Environ Res Public Health 15:478. https://doi.org/10.3390/ijerph15030478
Szabó MP, Pinter A, Labruna MB (2013) Ecology, biology and distribution of spotted-fever tick vectors in Brazil. Front Cell Infec Microbiol 3:27. https://doi.org/10.3389/fcimb.2013.00027
Talhari S, Schettini APM, Parreira VJ, Cruz RG, Melo IS, Talhari C (1987) Eritema crônico migrans/Doença de Lyme—Estudo de três casos. In: XLII Congresso Brasileiro de Dermatologia, Goiânia
Talhari S, Souza Santos MN, Talhari C, Lima Ferreira LC, Silva Jr RM, Zelger B, Massone C, Ribeiro RR (2010) Borrelia burgdorferi “sensu lato” in Brazil: occurrence confirmed by immunohistochemistry and focus floating microscopy. Acta Trop 115(3):200–204. https://doi.org/10.1016/j.actatropica.2010.02.017
Tavares C, Aragão AI, Leal NC, Leal-Balbino TC, de Oliveira MBM, de Oliveira Gonçalves Ferreira GM, de Almeida AMP (2012) Plague in Brazil: from now and then. Adv Exp Med Biol 954:69–77. https://doi.org/10.1007/978-1-4614-3561-7_10
Teoh YT, Hii SF, Graves S, Rees R, Stenos J, Traub RJ (2016) Evidence of exposure to Rickettsia felis in Australian patients. One Health 2:95–98. https://doi.org/10.1016/j.onehlt.2016.06.001
Yoshinari N, Spolidorio M, Bonoldi VL, Sotto M (2007) Lyme disease like syndrome associated lymphocytoma: first case report in Brazil. Clinics 62(4):525–526. https://doi.org/10.1590/S1807-59322007000400020
Yoshinari NH, Mantovani E, Bonoldi VLN, Marangoni RG, Gauditano G (2010) Brazilian lyme-like disease or Baggio-Yoshinari syndrome: exotic and emerging Brazilian tick-borne zoonosis. Rev Assoc Med Bras 56(3):363–369. https://doi.org/10.1590/s0104-42302010000300025
Zanela JRC (2016) Zoonoses emergentes e reemergentes e sua importância para saúde e produção animal. Pesq Agropec Bras 51(5):510–519. https://doi.org/10.1590/S0100-204X2016000500011
Acknowledgements
This article is based on the Master dissertation (Postgraduate Program in Animal Bioscience), developed at the Federal Rural University of Pernambuco, supported by a grant from the Fundação de Amparo a Ciência e Tecnologia do Estado de Pernambuco (FACEPE). This work integrates the universal project (420184/2016-3) entitled ‘Diversity of Ixodids and Sifonapters in company animals and its relationship with pathogens of importance in Public Health in the northeast region of Brazil’, funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPQ).
Author information
Authors and Affiliations
Contributions
JCPdO and RANR conceived and designed this study. Material preparation and data collection was performed by JCPdO. Data analysis was conducted by AG, GAdC and LCA. Molecular analysis was performed by JCPdO, GHR and CAdNR. JCPdO and RANR wrote the original draft and all co-authors commented and contributed intellectually on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author declares that they have no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
de Oliveira, J.C.P., Reckziegel, G.H., Ramos, C.A.d. et al. Detection of Rickettsia felis in ectoparasites collected from domestic animals. Exp Appl Acarol 81, 255–264 (2020). https://doi.org/10.1007/s10493-020-00505-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10493-020-00505-2