ANTUNES, PAOLA

Carlos Alexandre Sanchez Ferreira

DALL?AGNOL, BRUNO

PADILHA, THAMIRIS

RECK, JOSÉ

SCHOTT, DIOGO

SOUZA, GETÚLIO D.

SOUZA, UGO A.

WEBSTER, ANELISE

Wilderness and Environmental Medicine

Repositório Institucional da PUCRS

WILDERNESS & ENVIRONMENTAL MEDICINE 2019; 30(4): 437e40CASE REPORTClinical Findings Associated with Ornithodoros brasiliensisTick Parasitism in Travelers, Southern BrazilBruno Dall’Agnol, DVM, PhD1; Diogo Schott, MSc1; Thamiris Padilha, DVM1; Paola Antunes, DVM1;Ugo A. Souza, DVM1; Anelise Webster, DVM, PhD1; Getúlio D. Souza, MSc2;Carlos Alexandre S. Ferreira, PhD3; Jose Reck, DVM, PhD11Instituto de Pesquisas Veterinarias Desiderio Finamor (IPVDF), Eldorado do Sul, Brazil; 2Secretaria Estadual da Saúde do Rio Grande do Sul (SES-RS), Porto Alegre, Brazil; 3Pontifícia Universidade Catolica do Rio Grande do Sul, Porto Alegre, BrazilPresented aCarrapatos, OcCorrespondPesquisas Vete6000, Eldoradobruno-dallagnoSubmitted foAccepted foWe report a series of clinical cases associated with parasitism by theOrnithodoros brasiliensis tick in a groupof travelers in the Caxias do Sul municipality, Southern Brazil. These cases draw attention to underdiagnosednoninfectious syndromes caused by ticks with restricted local distributions.Keywords: Argasidae, toxicosis, mouro tick, Caxias do SulIntroductionTicks are blood-feeding parasites that are distributedworldwide.1 They can cause a variety of damage tohuman and animal health, transmit pathogens, or inducesevere injuries directly associated with the tick bite.2 Forinstance, in North America,Dermacentor andersoni (Ixodi-dae) induces cases of paralysis in humans,3 whereasOrnithodoros savignyi (Argasidae) is the causative agentof a severe and often lethal syndrome known as sand tam-pan toxicosis in Africa.4 These syndromes seem to be asso-ciated with salivary toxins rather than infectious agents. Fora comprehensive review of tick toxicoses, see the seminalwork of Mans and colleagues.5 In Southern Brazil, theOrnithodoros brasiliensis (Argasidae) tick is known tocause a noninfectious (toxicosis) syndrome that leads tosystemic changes and severe lesions at the site of the bite.6Data on this tick species are scarce. To date, the knowndistribution ofO brasiliensis is restricted to 2 municipalitiesin Rio Grande do Sul state (RS): S~ao Francisco de Paulaand Jaquirana. Recently, in a study compiling the reportsof ticks on humans between 2004 and 2017 in RS, Brazil,t II Simposio Nacional de Doenças Transmitidas portober 16 and 17, 2017 in Rio de Janeiro, RJ, Brazil.ing author: Bruno Dall’Agnol, DVM, PhD, Instituto derinarias Desiderio Finamor (IPVDF), Estrada do Conde,do Sul, 92990-000, RS, Brazil.; e-mail:l@agricultura.rs.gov.br.r publication January 2019.r publication June 2019.4 cases of human parasitism were reported, with ticksbeing collected directly from victims.7 However, humanparasitism by O brasiliensis seems to be highly underesti-mated and underreported: in 2013, a questionnaire-basedstudy revealed at least 28 retrospective human cases inRS.6 Furthermore, in addition to toxicosis syndrome, thistick species may be linked with pathogen transmission; apotential tick-borne microorganism (Borrelia brasiliensis)was once shown to be associated with O brasiliensisunder laboratory conditions.6,8 Thus, this tick is importantto public health given the apparent high rate of humancases with severe lesions, its potential to produce toxicosis,and its possible role in the epidemiology of Borrelia spp.Here, we report a case series associated with O brasiliensistick parasitism involving 7 travelers after an ecotourismtrail hike in the Southern Brazil highlands.Case descriptionIn April 2017, the travelers spent 1 night in tents at theentrance of a cave close to a waterfall, a tourist attraction inCaxias do Sul municipality (2902'35.7"S 5101'36.4"W;Figure 1A and B). The tourists reported that 7 people fromthe group woke during the night due to several painful bugbites. The guide of the group photographed one of thebugs and collected some specimens (Figure 2A).About 1 wk later, the guide (case 1, a 48-y-old man),who reported having been bitten approximately 50 timesthat night, sought medical attention at a municipal healthcenter in Caxias do Sul. He reported intense pruritus atFigure 1. A, Rio Grande do Sul state, Brazil, and neighboring countries. Gray shading indicates bodies of water; the map-marker indicates the cave fromCaxias do Sul municipality. B, Cave entrance where the tourists camped.Dall’Agnol et al438the bite sites and the formation of blisters. He was pre-scribed betamethasone dipropionate cream, topically.After 2 wk, the patient reported a complete recovery. Theguide delivered the collected bugs to the medical center.The parasites were identified as 2 male specimens ofO brasiliensis.Four of the other 6 people who were bitten sought med-ical attention in their home cities. Cases 2 (a 19-y-oldwoman) and 3 (a 49-y-old woman; Figure 2B) were adaughter and mother bitten by approximately 20 ticks ontheir feet, legs, hands, arms, and neck. About 4 wk afterthe episode, because the symptoms had not resolved, theysought medical attention. They reported severe pruritus,erythema, edema, and blisters at the bite sites. The primarycare physician in their home city told them that the tick biteswere no reason for concern. They sought medical attentionseveral additional times because of this issue. Patients 2 and3 then received dexamethasone (intramuscular, 2 doses)and fexofenadine (oral, once a day, for 7 d). Because ofthe severity of her clinical presentation, patient 3 alsoFigure 2. A, Specimen ofO brasiliensis found attached to the body of case 1,Ornithodoros brasiliensis on the hand of case 3 at 4 wk after tick bites.received systemic antimicrobial therapy. Both patientsreported that the lesions and symptoms remained for >20wk after the episode.Patients 4 and 5 were a couple, a 31-y-old man and a 28-y-oldwoman. Themalewas bitten by 6 ticks, and the femalewas bitten by 3, both on their hands, abdomen, and neck.The female noticed severe pruritus, erythema, and bruisesat the bite sites starting 2 d after the episode and lastingapproximately 8 wk. Her husband noticed the formation ofblisters and a loss of sensation around the bite site; thesymptoms started about 4 d after the tick bites. He soughtmedical attention, and his physician prescribed systemicantimicrobial therapy for 6 d. His symptoms resolved after7 wk. All patients who sought medical attention reportedthat all of their physicians said that they had never treateda victim of tick parasitism or tick-borne diseases, that theyhad never heard about a tick bite lesion lasting for such along time, or that tick bites were no reason for concern.Patient 6 was a 51-y-old man bitten by 35 ticks. Hereported the formation of painful bruises around the tickcollected and photographed by the patient. B, Lesions caused by the bite ofTick Parasitism in Travelers, Brazil 439bites. The symptoms lasted for approximately 4 wk. Case 7was an 18-y-old man bitten by 3 ticks on the torso and neck.He did not report any symptoms associated with the tickbites.About 2 mo after the parasitism episode, we visited thelocal area to search for ticks. A total of 2 females and8 males of O brasiliensis were found. Ticks and patients’blood samples were further submitted to pathogen investi-gation. A set of polymerase chain reaction tests for Borreliaspp and Rickettsia spp.9,10 were performed. All sampleswere negative on analysis.DiscussionLocally known as mouro tick or “bicho mouro,” O brasi-liensis is also designated a ground tick because of its habitof living buried in sand near host habitations, cellars,stables, and even human habitations.11,12 This tick speciesis responsible for severe host reactions in animals13 andhumans,6 such as local pruritus, slowly healing lesions,local edema and erythema, focal skin rash, local pain,blisters, limb edema, malaise, headache, transient fever,and dyspnea.6 However, to date, the salivary compoundsthat induce such lesions are not fully known. O brasilien-sis salivary gland homogenates display potent inhibitionof endothelial cell proliferation, a crucial step in woundhealing.2 In addition, studies in experimental animals(Wistar rats) have shown changes in eosinophil and baso-phil counts and increases in creatine kinase, the creatinekinase MB fraction, and fibrinogen level. Moreover, his-topathologic analysis of bitten rats revealed edema andmuscle degeneration at the tick attachment site.14To the best of our knowledge, this tick species had neverpreviously been reported in the wilderness; it was onlyreported underneath or around human habitations in othermunicipalities of Southern Brazil, S~ao Francisco de Paulaand Jaquirana.6 Herein, we reported the occurrence of Obrasiliensis in a cave from Caxias do Sul municipality,which could be the natural habitat of this tick species, aspreviously observed for other Ornithodoros species.15,16Both domestic and wild animals could act as food sourcesfor O brasiliensis.6 Thus, animals, particularly sinantropicspecies, could act as carriers of ticks, favoring the infesta-tion of human habitations. According to anecdotal informa-tion from local inhabitants, periodically throughout the pastdecades, there have been several reports of people bitten bybugs in this area, which at least suggest that such bites maynot be a recent problem.It is important to note that Caxias do Sul is located in themain tourist region of RS, called “Serra Gaúcha,” popularlyknown for its beautiful scenery and immigrant culture. Italso attracts several thousand foreign tourists each year,highlighting the risk of an emerging issue of importedcases of exotic tick-associated diseases.17 In addition, Cax-ias do Sul is the second largest municipality in the state ofRS, with an estimated population of >500,000 inhabitants.This highlights the risk for novel cases of humanparasitism.Here, we observed a marked difference in the clinicalpresentation among the bitten patients, ranging from nosymptoms to months of medical intervention. Of course,the number of tick bites should be taken into account; how-ever, health practitioners must pay attention to the greatindividual variation in response to O brasiliensis bites andto other tick-induced syndromes.At this time we cannot rule out that at least some of theclinical findings described here may be associated with atick-borne infectious microorganism. We did not findBorrelia spp and Ricketsia spp DNA using the polymer-ase chain reaction analysis of ticks and patients’ blood.However, the blood was collected only 2 mo after thetick bites, and unfortunately only a low number of tickspecimens were tested. Borrelia spp was once found tobe associated with O brasiliensis in 1952,8 but after thisreport, no studies have reported the microbiota of thistick species.Although a toxicosis syndrome associated withO brasi-liensis tick bites has been reported in retrospective studieswith local inhabitants from Southern Brazil, to date, therehave been no case reports describing it in detail.6 Thecase series presented here has particular importancebecause it occurred with travelers. Medical practitionersshould be aware that travelers, especially those returningfrom trails or camping, could present syndromes onlyknown in locally restricted regions. Therefore, additionalstudies on the ecology (domestic and wild hosts, habitat,distribution) and potential pathogenic microorganisms inthis species are peremptory, especially considering thatmedical authorities are usually not aware of human parasit-ism by this tick species.Acknowledgments: We especially thank Mr. Clairton Júlio de Limafrom the company Lob~ao Trilhas e Aventuras for the fundamental supportin the execution of this work and Eduardo Kieling (SES-RS), AdrianaRhoden (Secretaria Municipal de Saúde de Caxias do Sul, Caxias do Sul,Brazil), Bruna F. Leal, Rovaina Doyle, and Fabrício Tibere Jardim(IPVDF) for their valuable help during field work.Author Contributions: Study concept and design (BD, JR); obtainingfunding (BD, JR); acquisition of the data (BD, DS, TP, PA, UAS, AW,GDS); analysis of the data (BD, DS, TP, PA, UAS, AW, GDS, CASF,JR); drafting of the manuscript (BD, JR); critical revision of the manuscript(BD, AW, CASF, JR); approval of final manuscript (BD, DS, TP, PA,UAS, AW, GDS, CASF, JR).Financial/Material Support: This work was supported by the Fundaç~aode Amparo a Pesquisa do Estado do Rio Grande do Sul (FAPERGS),Conselho Nacional de Desenvolvimento Científico e Tecnologico (CNPq),Coordenaç~ao de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)and INCT em Entomologia Molecular.Disclosures: None.Dall’Agnol et al440References1. Nava S, Guglielmone AA, Mangold AJ. An overview of sys-tematics and evolution of ticks. Front Biosci (Landmark Ed).2009;(14):2857e77.2. Reck J, Marks FS, Termignoni C, Guimar~aes JA, Martins JR.Ornithodoros brasiliensis (mouro tick) salivary gland homo-genates inhibit in vivo wound healing and in vitro endothelialcell proliferation. Parasitol Res. 2013;112(4):1749e53.3. Morshed M, Li L, Lee MK, Fernando K, Lo T, Wong Q.A retrospective cohort study of tick paralysis in BritishColumbia. Vector Borne Zoonotic Dis. 2017;17(12):821e4.4. Mans BJ, Steinmann CM, Venter JD, Louw AI, Neitz AW.Pathogenic mechanisms of sand tampan toxicoses induced bythe tick.Ornithodoros Savignyi.Toxicon. 2002;40(7):1007e16.5. Mans BJ, Gothe R, Neitz AW. Biochemical perspectives onparalysis and other forms of toxicoses caused by ticks. Para-sitology. 2004;129(Suppl):S95e111.6. Reck J, Marks FS, Guimar~aes JA, Termignoni C, Martins JR.Epidemiology of Ornithodoros brasiliensis (mouro tick) inthe southern Brazilian highlands and the description ofhuman and animal retrospective cases of tick parasitism.Ticks Tick Borne Dis. 2013;4(1e2):101e9.7. Reck J, Souza U, Souza G, Kieling E, Dall’Agnol B,Webster A, et al. Records of ticks on humans in Rio Grandedo Sul state, Brazil. Ticks Tick Borne Dis. 2018;9(5):1296e301.8. Davis GE. Observations on the biology of the argasid tick,Ornithodoros brasiliensis Arag~ao, 1923; with the recoveryof a spirochete, Borrelia brasiliensis, n. sp. J Parasitol.1952;38(5):473e6.9. Barbieri AM, Venzal JM, Marcili A, Almeida AP,Gonzalez EM, Labruna MB. Borrelia burgdorferi sensu latoinfecting ticks of the Ixodes ricinus complex in Uruguay:first report for the Southern Hemisphere. Vector Borne Zoo-notic Dis. 2013;13(3):147e53.10. Labruna MB, Whitworth T, Horta MC, Bouyer DH,McBride JW, Pinter A, et al. Rickettsia species infectingAmblyomma cooperi ticks from an area in the state of S~aoPaulo, Brazil, where Brazilian spotted fever is endemic.J Clin Microbiol. 2004;42(1):90e8.11. Evans DE, Martins JR, Guglielmone AA. A review of theticks (Acari, ixodida) of Brazil, their hosts and geographic dis-tribution-1. The state of Rio Grande do Sul, southern Brazil.Mem Inst Oswaldo Cruz. 2000;95(4):453e70.12. Martins JR, Doyle RL, Barros-Battesti DM, Onofrio VC,Guglielmone AA. Occurrence of Ornithodoros brasiliensisArag~ao (Acari: Argasidae) in S~ao Francisco de Paula, RS,Southern Brazil. Neotrop Entomol. 2011;40(1):143e4.13. Reck J, Soares JF, Termignoni C, Labruna MB, Martins JR.Tick toxicosis in a dog bitten by Ornithodoros brasiliensis.Vet Clin Pathol. 2011;40(3):356e60.14. Reck J, Bandarra P, Pavarini S, Termignoni C, Driemeier D,Martins JR, et al. Experimentally induced tick toxicosis inrats bitten by Ornithodoros brasiliensis (Chelicerata: Argasi-dae): a clinico-pathological characterization. Toxicon.2014;88:99e106.15. Guzman-Cornejo C, García-Prieto L, Rebollo-Hernandez A,Venzal JM, Nava S, Sanchez-Montes S, et al. 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Clinical Findings Associated with Ornithodoros brasiliensis Tick Parasitism in Travelers, Southern Brazil

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Clinical Findings Associated with Ornithodoros brasiliensis Tick Parasitism in Travelers, Southern Brazil

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