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Tick-borne pathogens in tick species infesting humans in Sibiu County, central Romania

Abstract

Romania has a highly diverse tick fauna. Consequently, a high diversity of tick-transmitted pathogens might be a potential threat to humans. However, only a limited number of tick species regularly infest humans, and pathogens present in such species are therefore of particular interest from a medical perspective. In this study, 297 ticks were collected from humans during 2013 and 2014. Ixodes ricinus was the predominant tick species, accounting for 272 specimens or 91.6% of the ticks in the study. Nevertheless, other tick species were also found to infest humans: Dermacentor marginatus constituted 7% of the ticks found on humans (21/297), Haemaphysalis punctata 1% (3/297), and Haemaphysalis concinna 0.3% (1/297). Ticks were tested by PCR for a wide range of tick-borne pathogens. In total, 11.8% of the ticks carried human pathogenic bacteria, while no viral or protozoan pathogens were detected. The most frequently detected pathogen was Rickettsia spp., occurring in 5.4% of the ticks (16/297) and comprising three species: Rickettsia (R.) raoultii, R. monacensis, and R. helvetica. Borrelia s.l. occurred in 3% (9/297) of the ticks. “Candidatus Neoehrlichia mikurensis” occurred in 1.7% (5/297) and Anaplasma phagocytophilum in 1.3% (4/297). Anaplasma bovis was detected in an H. punctata and Borrelia miyamotoi in an I. ricinus. These results point to the need for further studies on the medical importance of tick-borne pathogens in Romania.

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References

  1. Andersson M, Zaghdoudi-Allan N, Tamba P, Stefanache M, Chitimia L (2014) Co-infection with ‘Candidatus Neoehrlichia mikurensis’ and Borrelia afzelii in an Ixodes ricinus tick that has bitten a human in Romania. Ticks Tick Borne Dis 5:3–5

  2. Andersson M, Tolf C, Tamba P, Stefanache M, Radbea G, Rubel F, Waldenström J, Dobler G, Chitimia-Dobler L (2017a) Babesia, Theileria, and Hepatozoon species in ticks infesting animal hosts in Romania. Parasitol Res 116:2291–2297

  3. Andersson M, Víchová B, Tolf C, Krzyzanowska S, Waldenström J, Karlsson ME (2017b) Co-infection with Babesia divergens and Anaplasma phagocytophilum in cattle (Bos taurus), Sweden. Ticks Tick Borne Dis 8:933–935

  4. Andersson M, Tolf C, Tamba P, Stefanache M, Radbea G, Frangoulidis D, Tomaso H, Waldenström J, Dobler G, Chitimia-Dobler L (2018) Molecular survey of neglected bacterial pathogens reveals an abundant diversity of species and genotypes in ticks collected from animal hosts across Romania. Parasit Vectors 11:1. https://doi.org/10.1186/s13071-018-2756-1

  5. Blanarova L, Stanko M, Miklisová D, Bronislava V, Mosansky L, Kraljik J, Bona M, Derdakova M (2015) Presence of Candidatus Neoehrlichia mikurensis and Babesia microti in rodents and two tick species (Ixodes ricinus and Ixodes trianguliceps) in Slovakia. Ticks Tick Borne Dis 7:319–326. https://doi.org/10.1016/j.ttbdis.2015.11.008

  6. Briciu VT, Titilincu A, Tatulescu DF, Carstina D, Lefkaditis M, Mihalca AD (2011) First survey on hard ticks (Ixodidae) collected from humans in Romania: possible risks for tick-borne diseases. Exp Appl Acarol 54:199–204

  7. Chitimia-Dobler L, Rieß R, Kahl O, Wölfel S, Dobler G, Nava S, Estrada-Peña A (2018) Ixodes inopinatus—occurring also outside the Mediterranean region. Ticks Tick Borne Dis 9:196–200

  8. Coipan EC, Vladimirescu AF (2010) First report of lyme disease spirochetes in ticks from Romania (Sibiu County). Exp Appl Acarol 52:193–197

  9. Cuber P, Andreassen A, Vainio K, Asman M, Dudman S, Szilman P, Szilman E, Ottesen P, Anestad G, Ciesla-Nobis S, Solarz K (2015) Risk of exposure to ticks (Ixodidae) and the prevalence of tick-borne encephalitis virus (TBEV) in tick in Southern Poland. Ticks Tick Borne Dis 6:356–363

  10. Dobler G, Wölfel R (2009) Typhus and other rickettsioses. Dtsch Arztebl Int 106:348–354

  11. Dunaj J, Moniuszko-Malinowska A, Swiecicka I, Andersson M, Czupryna P, Rutkowski K, Zambrowski G, Zajkowska J, Grygorczuk S, Kondrusik M, Świerzbińska R, Pancewicz S (2017) Tick-borne infections and co-infections in patients with non-specific symptoms in Poland. Adv Med Sci 63:167–172

  12. Estrada-Peña A, Jongejan F (1999) Ticks feeding on humans: a review of records on human-biting Ixodoidea with special reference to pathogen transmission. Exp Appl Acarol 23:685–715

  13. Feider Z (1965) Fauna of the Peoples Republic of Romania. Suprafamily Ixodoidea. Ticks. Ed. Acad Rep Pop Romane, Bucharest [In Romanian]

  14. Hügli D, Moret J, Rais O, Moosmann Y, Erard P, Malinverni R, Gern L (2009) Tick bites in a Lyme borreliosis highly endemic area in Switzerland. Int J Med Microbiol 299:155–160

  15. Hildebrandt A, Hunfeld KP, Baier M, Krumbholz A, Saches S, Lorenzen T, Kiehntopf M, Fricke HJ, Straube E (2007) First confirmed autochthonous case of human Babesia microti infection in Europe. Eur J Clin Microbiol Infect Dis 26:595–601

  16. Hornok S, Meli ML, Gönczi E, Hofmann-Lehmann R (2013) First evidence of ‘Candidatus Neoehrlichia mikurensis’ in Hungary. Parasit Vectors 6:267

  17. Ionescu L, Necsulescu M, Alexse A, Ceianu C, Popescu D, Bicheru S, Ordeanu V, Nicolescu G, Vladimirescu A, Postoarca A (2008) The tick-borne encephalitis virus infection in Romania. Rev Rom Med Vet 18:69–79

  18. Ionita M, Mitrea IL, Pfister K, Hamel D, Silaghi C (2013) Molecular evidence for bacterial and protozoan pathogens in hard ticks from Romania. Vet Parasitol 196:71–76

  19. Ionita M, Silaghi C, Mitrea IL, Edouard S, Parola P, Pfister K (2016) Molecular detection of Rickettsia conorii and other zoonotic spotted fever group rickettsiae in ticks, Romania. Ticks Tick Borne Dis 7:150–153

  20. Jado I, Oteo JA, Aldámiz M, Gil H, Escudero R, Ibarra V, Portu J, Portillo A, Lezaun MJ, Garcia-Amil C, Rodriguez-Moreno I, Anda P (2007) Rickettsia monacensis and human disease, Spain. Emerg Infect Dis 13:1405–1407

  21. Kalmár Z, Mihalca AD, Dumitrache MO, Gherman CM, Magdas C, Mircean V, Oltean M, Domsa C, Marcutan DI, Sándor AD, D’Amico G, Pastiu A, Györke A, Gavrea R, Marosi B, Ionica A, Burkhardt E, Toriay H, Cosma V (2013) Geographical distribution and prevalence of Borrelia burgdorferi genospecies in questing Ixodes ricinus from Romania: a countrywide study. Ticks Tick Borne Dis 4:403–408

  22. Kalmár Z, Sprong H, Mihalca AD, Gherman CM, Dumitrache MO, Coipan EC, Fonville M, Cosma V (2016) Borrelia miyamotoi and Candidatus Neoehrlichia mikurensis in Ixodes ricinus ticks, Romania. Emerg Infect Dis 22:550–551

  23. Kawahara M, Rikihisa Y, Lin Q, Isogai E, Tahara K, Itagaki A, Hiramitsu Y, Tajima T (2006) Novel genetic variants of Anaplasma phagocytophilum, Anaplasma bovis, Anaplasma centrale, and a novel Ehrlichia sp. in wild deer and ticks on two major islands in Japan. Appl Environ Microbiol 72:1102–1109

  24. Kim YS, Choi YJ, Lee KM, Ahn KJ, Kim HC, Klein T, Jiang J, Richards A, Park KH, Jang WJ (2017) First isolation of Rickettsia monacensis from a patient in South Korea. Microbiol Immunol 61:258–263

  25. Krücken J, Schreiber C, Maaz D, Kohn M, Demeler J, Beck S, Schein E, Olias P, Richter D, Matuschka FR, Pachnicke S, Krieger K, Kohn B, von Samson-Himmelstjerna G (2013) A novel high-resolution melt PCR assay discriminates Anaplasma phagocytophilum and “Candidatus Neoehrlichia mikurensis”. J Clin Microbiol 51:1958–1961

  26. Lindblom A, Katarina Wallmenius K, Sjöwall J, Fryland L, Wilhelmsson P, Lindgren P-E, Forsberg P, Nilsson K (2016) Prevalence of Rickettsia spp. in ticks and serological and clinical outcomes in tick-bitten individuals in Sweden and on the Åland Islands. PLoS One 11:e0166653

  27. Madeddu G, Mancini F, Caddeo A, Cievo A, Babudieri S, Maida I, Fiori ML, Rezza G, Mura MS (2012) Rickettsia monacensis as cause of mediterranean spotted fever-like illness, Italy. Emerg Infect Dis 18:702–704

  28. Manfredi MT, Dini V, Piacenza S, Genchi C (1999) Tick species parasitizing people in an area endemic for tick-borne diseases in north-western Italy. Parassitologia 41:555–560

  29. Marcutan ID, Kalmár Z, Ionica AM, D’Amico G, Mihalca AD, Vasile C, Sádor AD (2016) Spotted fever group rickettsiae in ticks of migratory birds in Romania. Parasit Vectors 9:294

  30. Matei IA, Kalmár Z, Lupse M, D’Amico G, Ionica AM, Dumitrache MO, Gherman CM, Mihalca AD (2017) The risk of exposure to rickettsial infections and human granulocytic anaplasmosis associated with Ixodes ricinus tick bites in humans in Romania: a multiannual study. Ticks Tick Borne Dis 8:375–378

  31. Matei IA, Kalmár Z, Magdas C, Magdas V, Toriay H, Dumitrache MO, Ionica AM, D’Amico G, Sándor AD, Marcutan DI, Domsa C, Gherman CM, Mihalca AD (2015) Anaplasma phagocytophilum in questing Ixodes ricinus ticks from Romania. Ticks Tick Borne Dis 6:408–413

  32. Mihalca AD, Gherman CM, Magdas C, Dumitrache MO, Györke A, Sándor AD, Domsa C, Oltean M, Mircean V, Marcutan DI, D’Amico G, Paduraru AO, Cozma V (2012) Ixodes ricinus is the dominant questing tick in forest habitats in Romania: the results from a countrywide dragging campaign. Exp Appl Acarol 58:175–182

  33. Moniuszko-Malinowska A, Swiecicka I, Dunaj J, Zajkowska J, Czupryna P, Zambrowski G, Chmielewska-Badora J, Zukiewicz-Sobczak W, Swierzbinska R, Rutkowski K, Garkowski A, Pancewicz S (2016) Infection with Babesia microti in humans with non-specific symptoms in north East Poland. Infect Dis (Auckl) 48:537–543

  34. Mukhacheva TA, Kovalev SY (2014) Borrelia spirochetes in Russia: genospecies differentiation by real-time PCR. Ticks Tick Borne Dis 5:722–726

  35. Nilsson K, Lindquist O, Pahlson C (1999) Association of Rickettsia helvetica with chronic perimyocarditis in sudden cardiac death. Lancet 354:1169–1173

  36. Obiegala A, Silaghi C (2018) Candidatus Neoehrlichia mikurensis—recent insights and future perspectives on clinical cases, vectors, and reservoirs in Europe. Curr Clin Micro Rpt 5:1–9

  37. Ornstein K, Barbour AG (2006) A reverse transcriptase–polymerase chain reaction assay of Borrelia burgdorferi 16S rRNA for highly sensitive quantification of pathogen load in a vector. Vector-Borne Zoonotic Dis 6:103–113

  38. Otranto D, Dantas-Torres F, Giannelli A, Latrofa MS, Cascio A, Cazzin S, Ravagnan S, Montarsi F, Zanzani SA, Manfredi MT, Capelli G (2014) Ticks infesting humans in Italy and associated pathogens. Parasit Vectors 14:328

  39. Palomar AM, Portillo A, Santibáñez P, Mazuelas D, Roncero L, Garcia-Alvarez L, Santibáñez S, Gutiérrez O, Oteo JA (2015) Detection of tick-borne Anaplasma bovis, Anaplasma phagocytophilum and Anaplasma centrale in Spain. Med Vet Entomol 29:349–353

  40. Pangrácová L, Derdáková M, Pekárik L, Hviščová I, Víchová B, Stanko M, Hlavatá H, Petko B (2013) Ixodes ricinus abundance and its infection with the tick-borne pathogens in urban and suburban areas of Eastern Slovakia. Parasit Vectors 6:238

  41. Platonov AE, Karan LS, Kolyasnikova NM, Makhneva NA, Toporkova MG, Malev VV, Fish D, Krause PJ (2011) Humans infected with relapsing fever spirochete Borrelia miyamotoi, Russia. Emerg Infect Dis 17:1816–1823

  42. Ponomareva EP, Mikryukova TP, Gori AV, Kartashov MY, Protopopova EV, Chausov EV, Konovalova SN, Tupota NL, Gheorghita SD, Burlacu VI, Ternovoi VA, Loktev VB (2015) Detection of Far-Eastern subtype of tick-borne encephali tis viral RNA in ticks collected in the Republic of Moldova. J Vector Borne Dis 52:334–336

  43. Raileanu C, Moutailler S, Pavel I, Porea D, Mihalca AD, Savuta G, Vayssier-Taussat M (2017) Borrelia diversity and co-infection with other tick borne pathogens in ticks. Front Cell Infect Microbiol 7:1–12

  44. Rar V, Golovljova I (2011) Anaplasma, Ehrlichia, and ‘Candidatus Neoehrlichia’ bacteria: pathogenicity, biodiversity, and molecular genetic characteristics, a review. Infect Genet Evol 11:1842–1861

  45. Richter D, Kohn C, Matuschka F-R (2013) Absence of Borrelia spp., Candidatus Neoehrlichia mikurensis, and Anaplasma phagocytophilum in questing adult Dermacentor reticulatus ticks. Parasitol Res 112:107–111

  46. Richter D, Matuschka F-R (2012) “Candidatus Neoehrlichia mikurensis”, Anaplasma phagocytophilum and Lyme disease spirochetes in questing European vector ticks and in feeding ticks removed from people. J Clin Microbiol 50:943–947

  47. Salat J, Mihalca AD, Mihaiu M, Modry D, Ruzek D (2017) Tick-borne encephalitis in sheep, Romania. Emerg Infect Dis 23:2065–2067

  48. Schwaiger M, Cassinotti P (2003) Development of a quantitative real-time RT-PCR assay with internal control for the laboratory detection of tick borne encephalitis virus (TBEV) RNA. J Clin Virol 27:136–145

  49. Scoles GA, Papero M, Beati L, Fish D (2001) A relapsing fever group spirochete transmitted by Ixodes scapularis ticks. Vector-Borne Zoonotic Dis 1:21–34

  50. Serban R, Pistol A, Negut M, Cucuiu R (2009) Rickettsia conorii infection in Romania, 2000-2008. Bacteriol Virusol Parazitol Epidemiol 54:177–183

  51. Silaghi C, Beck R, Oteo JA, Pfeffer M, Sprong H (2016) Neoehrlichiosis: an emerging tick-borne zoonosis caused by Candidatus Neoehrlichia mikurensis. Exp Appl Acarol 68:279–297

  52. Sonenshine DE, Mether TN (1994) Ecological dynamics of tick-borne zoonoses. Oxford University Press, Oxford

  53. Welc-Falęciak R, Pawełczyk A, Radkowski M, Pancewicz SA, Zajkowska J, Siński E (2015) First report of two asymptomatic cases of human infection with Babesia microti (Franca, 1910) in Poland. Ann Agric Environ Med 22:51–54

  54. Welinder-Olsson C, Kjellin E, Vaht K, Jacobsson S, Wennerås C (2010) First case of human “Candidatus Neoehrlichia mikurensis” infection in a febrile patient with chronic lymphocytic leukemia. J Clin Microbiol 48:1956–1959

  55. Wennerås C (2015) Infections with the tick-borne bacterium Candidatus Neoehrlichia mikurensis. Clin Microbiol Infect 21:621–630

  56. Wilhelmsson P, Fryland L, Börjesson S, Nordgren J, Bergström S, Ernerudh J, Forsberg P, Lindgren P-E (2010) Prevalence and diversity of Borrelia species in ticks that have bitten humans in Sweden. J Clin Microbiol 48:4169–4176

  57. Wölfel R, Essbauer S, Dobler G (2008) Diagnostics of tick-borne rickettsioses in Germany: a modern concept for a neglected disease. Int J Med Microbiol 298:368–374

  58. Zaharia M, Popescu CP, Florescu SA, Ceausu E, Raoult D, Parola P, Socolovschi C (2016) Rickettsia massiliae infection and SENLAT syndrome in Romania. Ticks Tick Borne Dis 7:759–776

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Acknowledgements

We are sincerely grateful to Richard Robbins for comments on the manuscript.

Funding

This work was funded by the German Center of Infection Research (DZIF), The Royal Swedish Academy of Agriculture and Forestry, The Royal Physiographic Society in Lund, and The Lund Animal Welfare Fund (Lunds djurskyddsfond).

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Correspondence to Lidia Chitimia-Dobler.

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Section Editor: Domenico Otranto

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Andersson, M.O., Marga, G., Banu, T. et al. Tick-borne pathogens in tick species infesting humans in Sibiu County, central Romania. Parasitol Res 117, 1591–1597 (2018). https://doi.org/10.1007/s00436-018-5848-0

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Keywords

  • Humans
  • Ticks
  • Tick-borne diseases
  • Sibiu County
  • Romania