Infection

, Volume 41, Issue 6, pp 1057–1072 | Cite as

Human Babesiosis in Europe: what clinicians need to know

Review

Abstract

Although best known as an animal disease, human babesiosis is attracting increasing attention as a worldwide emerging zoonosis. Humans are commonly infected by the bite of ixodid ticks. Rare ways of transmission are transplacental, perinatal and transfusion-associated. Infection of the human host can cause a very severe host-mediated pathology including fever, and hemolysis leading to anemia, hyperbilirubinuria, hemoglobinuria and possible organ failure. In recent years, apparently owing to increased medical awareness and better diagnostic methods, the number of reported cases in humans is rising steadily worldwide. Hitherto unknown zoonotic Babesia spp. are now being reported from geographic areas where babesiosis was not previously known to occur and the growing numbers of travelers and immunocompromised individuals suggest that the frequency of cases in Europe will also continue to rise. Our review is intended to provide clinicians with practical information on the clinical management of this rare, but potentially life-threatening zoonotic disease. It covers epidemiology, phylogeny, diagnostics and treatment of human babesiosis and the potential risk of transfusion-transmitted disease with a special focus on the European situation.

Keywords

Babesia Ticks Zoonosis Europe Phylogeny Human disease Blood transfusion IFAT PCR Diagnostics Treatment Prevention 

References

  1. 1.
    Telford SR 3rd, Spielman A. Reservoir competence of white-footed mice for Babesia microti. J Med Entomol. 1993;30:223–7.PubMedGoogle Scholar
  2. 2.
    Skrabalo Z, Deanovic Z. Piroplasmosis in man; report of a case. Doc Med Geogr Trop. 1957;9:11–6.PubMedGoogle Scholar
  3. 3.
    Homer MJ, Aguilar-Delfin I, Telford SR 3rd, Krause PJ, Persing DH. Babesiosis. Clin Microbiol Rev. 2000;13:451–69.PubMedGoogle Scholar
  4. 4.
    Herwaldt BL, Linden JV, Bosserman E, Young C, Olkowska D, Wilson M. Transfusion-associated babesiosis in the United States: a description of cases. Ann Intern Med. 2011;155:509–19. doi:10.1059/0003-4819-155-8-201110180-00362.PubMedGoogle Scholar
  5. 5.
    Vannier E, Krause PJ. Human babesiosis. N Engl J Med. 2012;366:2397–407. doi:10.1056/NEJMra1202018.PubMedGoogle Scholar
  6. 6.
    Hunfeld KP, Hildebrandt A, Gray JS. Babesiosis: recent insights into an ancient disease. Int J Parasitol. 2008;38:1219–37. doi:10.1016/j.ijpara.2008.03.001.PubMedGoogle Scholar
  7. 7.
    Gray J, Zintl A, Hildebrandt A, Hunfeld KP, Weiss L. Zoonotic babesiosis: overview of the disease and novel aspects of pathogen identity. Ticks Tick Borne Dis. 2010;1:3–10. doi:10.1016/j.ttbdis.2009.11.003.PubMedGoogle Scholar
  8. 8.
    Zahler M, Rinder H, Schein E, Gothe R. Detection of a new pathogenic Babesia microti-like species in dogs. Vet Parasitol. 2000;89:241–8.PubMedGoogle Scholar
  9. 9.
    Cho SH, Kim TS, Lee HW, Tsuji M, Ishihara C, Kim JT, Wee SH, Lee CG. Identification of newly isolated Babesia parasites from cattle in Korea by using the Bo-RBC-SCID mice. Korean J Parasitol. 2002;40:33–40.PubMedGoogle Scholar
  10. 10.
    Herwaldt BL, Cacció S, Gherlinzoni F, Aspöck H, Slemenda SB, Piccaluga P, Martinelli G, Edelhofer R, Hollenstein U, Poletti G, Pampiglione S, Löschenberger K, Tura S, Pieniazek NJ. Molecular characterization of a non-Babesia divergens organism causing zoonotic babesiosis in Europe. Emerg Infect Dis. 2003;9:942–8.PubMedGoogle Scholar
  11. 11.
    Herwaldt BL, de Bruyn G, Pieniazek NJ, Homer M, Lofy KH, Slemenda SB, Fritsche TR, Persing DH, Limaye AP. Babesia divergens-like infection, Washington State. Emerg Infect Dis. 2004;10:622–9.PubMedGoogle Scholar
  12. 12.
    Conrad PA, Kjemtrup AM, Carreno RA, Thomford J, Wainwright K, Eberhard M, Quick R, Telford SR 3rd, Herwaldt BL. Description of Babesia duncani n.sp. (Apicomplexa: Babesiidae) from humans and its differentiation from other piroplasms. Int J Parasitol. 2006;36:779–89. doi:10.1016/j.ijpara.2006.03.008.PubMedGoogle Scholar
  13. 13.
    Kjemtrup AM, Wainwright K, Miller M, Penzhorn BL, Carreno RA. Babesia conradae, sp. Nov., a small canine Babesia identified in California. Vet Parasitol. 2006;138:103–11. doi:10.1016/j.vetpar.2006.01.044.PubMedGoogle Scholar
  14. 14.
    Häselbarth K, Tenter AM, Brade V, Krieger G, Hunfeld KP. First case of human babesiosis in Germany - Clinical presentation and molecular characterisation of the pathogen. Int J Med Microbiol. 2007;297:197–204. doi:10.1016/j.ijmm.2007.01.002.PubMedGoogle Scholar
  15. 15.
    Kim JY, Cho SH, Joo HN, Tsuji M, Cho SR, Park IJ, Chung GT, Ju JW, Cheun HI, Lee HW, Lee YH, Kim TS. First case of human babesiosis in Korea: detection and characterization of a novel type of Babesia sp. (KO1) similar to ovine babesia. J Clin Microbiol. 2007;45:2084–7. doi:10.1128/JCM.01334-06.PubMedGoogle Scholar
  16. 16.
    Michael SA, Morsy TA, Montasser MF. A case of human babesiosis (preliminary case report in Egypt). J Egypt Soc Parasitol. 1987;17:409–10.PubMedGoogle Scholar
  17. 17.
    Bush JB, Isaäcson M, Mohamed AS, Potgieter FT, de Waal DT. Human babesiosis-a preliminary report of 2 suspected cases in South Africa. S Afr Med J. 1990;78:699.PubMedGoogle Scholar
  18. 18.
    Shih CM, Liu LP, Chung WC, Ong SJ, Wang CC. Human babesiosis in Taiwan: asymptomatic infection with a Babesia microti-like organism in a Taiwanese woman. J Clin Microbiol. 1997;35:450–4.PubMedGoogle Scholar
  19. 19.
    Ríos L, Alvarez G, Blair S. Serological and parasitological study and report of the first case of human babesiosis in Colombia. Rev Soc Bras Med Trop. 2003;36:493–8.PubMedGoogle Scholar
  20. 20.
    Marathe A, Tripathi J, Handa V, Date V. Human babesiosis-a case report. Indian J Med Microbiol. 2005;23:267–9.PubMedGoogle Scholar
  21. 21.
    El-Bahnasawy MM, Morsy TA. Egyptian human babesiosis and general review. J Egypt Soc Parasitol. 2008;38:265–72.PubMedGoogle Scholar
  22. 22.
    Qi C, Zhou D, Liu J, Cheng Z, Zhang L, Wang L, Wang Z, Yang D, Wang S, Chai T. Detection of Babesia divergens using molecular methods in anemic patients in Shandong Province, China. Parasitol Res. 2011;109:241–5. doi:10.1007/s00436-011-2382-8.PubMedGoogle Scholar
  23. 23.
    Senanayake SN, Paparini A, Latimer M, Andriolo K, Dasilva AJ, Wilson H, Xayavong MV, Collignon PJ, Jeans P, Irwin PJ. First report of human babesiosis in Australia. Med J Aust. 2012;196:350–2.PubMedGoogle Scholar
  24. 24.
    Martinot M, Zadeh MM, Hansmann Y, Grawey I, Christmann D, Aguillon S, Jouglin M, Chauvin A, De Briel D. Babesiosis in immunocompetent patients, Europe. Emerg Infect Dis. 2011;17:114–6. doi:10.3201/eid1701.100737.PubMedGoogle Scholar
  25. 25.
    Hildebrandt A, Hunfeld KP, Baier M, Krumbholz A, Sachse S, Lorenzen T, Kiehntopf M, Fricke HJ, Straube E. First confirmed autochthonous case of human Babesia microti infection in Europe. Eur J Clin Microbiol Infect Dis. 2007;26:595–601. doi:10.1007/s10096-007-0333-1.PubMedGoogle Scholar
  26. 26.
    Baumann D, Pusterla N, Péter O, Grimm F, Fournier PE, Schar G, Bossart W, Lutz H, Weber R. Fever after a tick bite: clinical manifestations and diagnosis of acute tick bite-associated infections in northeastern Switzerland. Dtsch Med Wochenschr. 2003;128:1042–7. doi:10.1055/s-2003-39103.PubMedGoogle Scholar
  27. 27.
    Nohýnková E, Kubek J, Mĕst’ánková O, Chalupa P, Hubálek Z. A case of Babesia microti imported into the Czech Republic from the USA. Cas Lek Cesk. 2003;142:377–81.PubMedGoogle Scholar
  28. 28.
    Ramharter M, Walochnik J, Lagler H, Winkler S, Wernsdorfer WH, Stoiser B, Graninger W. Clinical and molecular characterization of a near fatal case of human babesiosis in Austria. J Travel Med. 2010;17:416–8. doi:10.1111/j.1708-8305.2010.00446.x.PubMedGoogle Scholar
  29. 29.
    Poisnel E, Ebbo M, Berda-Haddad Y, Faucher B, Bernit E, Carcy B, Piarroux R, Harlé JR, Schleinitz N. Babesia microti: an unusual travel-related disease. BMC Infect Dis. 2013;13:99. doi:10.1186/1471-2334-13-99.PubMedGoogle Scholar
  30. 30.
    Berens-Riha N, Zechmeister M, Hirzmann J, Draenert R, Bogner J, Löscher T. Babesiose bei einem splenektonierten Reisenden aus den USA - Nach Deutschland importierte Infektion durch Zecken. Flugmedizin Tropenmedizin Reisemedizin - FTR. 2012;19:113–5.Google Scholar
  31. 31.
    Jablonska J, Zarnowska-Prymek H, Stanczak J, Kozlowska J, Wiercinska-Drapalo A (2013) Symptomatic co-infection with Babesia microti and Borrelia burgdorferi in Polish immuncompetent patient. in review process.Google Scholar
  32. 32.
    Haapasalo K, Suomalainen P, Sukura A, Siikamaki H, Jokiranta TS. Fatal babesiosis in man, Finland, 2004. Emerg Infect Dis. 2010;16:1116–8. doi:10.3201/eid1607.091905.PubMedGoogle Scholar
  33. 33.
    Andrić B, Golubović M, Terzic D, Dupanovic B, Icevic M. First diagnostic cases of human babesiosis in Montenegro. Braz J Infect Dis. 2012;16:498–9. doi:10.1016/j.bjid.2012.04.001.Google Scholar
  34. 34.
    Centeno-Lima S, do Rosário V, Parreira R, Maia AJ, Freudenthal AM, Nijhof AM, Jongejan F. A fatal case of human babesiosis in Portugal: molecular and phylogenetic analysis. Trop Med Int Health. 2003;8:760–4.PubMedGoogle Scholar
  35. 35.
    Welc-Falęciak R, Hildebrandt A, Siński E. Co-infection with Borrelia species and other tick-borne pathogens in humans: two cases from Poland. Ann Agric Environ Med. 2010;17:309–13.PubMedGoogle Scholar
  36. 36.
    Zahler M, Rinder H, Gothe R. Genotypic status of Babesia microti within the piroplasms. Parasitol Res. 2000;86:642–6.PubMedGoogle Scholar
  37. 37.
    Humiczewska M, Kuźna-Grygiel W. A case of imported human babesiosis in Poland. Wiad Parazytol. 1997;43:227–9.PubMedGoogle Scholar
  38. 38.
    Meer-Scherrer L, Adelson M, Mordechai E, Lottaz B, Tilton R. Babesia microti infection in Europe. Curr Microbiol. 2004;48:435–7. doi:10.1007/s00284-003-4238-7.PubMedGoogle Scholar
  39. 39.
    Moreno Giménez JC, Jiménez Puya R, Galàn Gutiérrez M, Ortega Salas R, Dueñas Jurado JM. Erythema figuratum in septic babesiosis. J Eur Acad Dermatol Venereol. 2006;20:726–8. doi:10.1111/j.1468-3083.2006.01492.x.
  40. 40.
    Falagas ME, Klempner MS. Babesiosis in patients with AIDS: a chronic infection presenting as fever of unknown origin. Clin Infect Dis. 1996;22:809–12.PubMedGoogle Scholar
  41. 41.
    Karp CL, Auwaerter PG. Coinfection with HIV and tropical infectious diseases. I. Protozoal pathogens. Clin Infect Dis. 2007;45:1208–13. doi:10.1086/522181.PubMedGoogle Scholar
  42. 42.
    Krause PJ, Gewurz BE, Hill D, Marty FM, Vannier E, Foppa IM, Furman RR, Neuhaus E, Skowron G, Gupta S, McCalla C, Pesanti EL, Young M, Heiman D, Hsue G, Gelfand JA, Wormser GP, Dickason J, Bia FJ, Hartman B, Telford SR 3rd, Christianson D, Dardick K, Coleman M, Girotto JE, Spielman A. Persistent and relapsing babesiosis in immunocompromised patients. Clin Infect Dis. 2008;46:370–6. doi:10.1086/525852.PubMedGoogle Scholar
  43. 43.
    Hunfeld KP, Allwinn R, Peters S, Kraiczy P, Brade V. Serologic evidence for tick-borne pathogens other than Borrelia burgdorferi (TOBB) in Lyme borreliosis patients from midwestern Germany. Wien Klin Wochenschr. 1998;110:901–8.PubMedGoogle Scholar
  44. 44.
    Hunfeld KP, Lambert A, Kampen H, Albert S, Epe C, Brade V, Tenter AM. Seroprevalence of Babesia infections in humans exposed to ticks in midwestern Germany. J Clin Microbiol. 2002;40:2431–6.PubMedGoogle Scholar
  45. 45.
    Chmielewska-Badora J, Moniuszko A, Żukiewicz-Sobczak W, Zwoliński J, Piątek J, Pancewicz S. Serological survey in persons occupationally exposed to tick-borne pathogens in cases of co-infections with Borrelia burgdorferi, Anaplasma phagocytophilum, Bartonella spp. and Babesia microti. Ann Agric Environ Med. 2012;19:271–4.PubMedGoogle Scholar
  46. 46.
    Foppa IM, Krause PJ, Spielman A, Goethert H, Gern L, Brand B, Telford SR 3rd. Entomologic and serologic evidence of zoonotic transmission of Babesia microti, eastern Switzerland. Emerg Infect Dis. 2002;8:722–6.PubMedGoogle Scholar
  47. 47.
    Leiby DA. Transfusion-transmitted Babesia spp.: bull’s-eye on Babesia microti. Clin Microbiol Rev. 2011;24:14–28. doi:10.1128/CMR.00022-10.PubMedGoogle Scholar
  48. 48.
    Vannier E, Gewurz BE, Krause PJ. Human babesiosis. Infect Dis Clin North Am. 2008;22:469–88, viii–ix. doi:10.1016/j.idc.2008.03.010.
  49. 49.
    Hildebrandt A, Tenter AM, Straube E, Hunfeld KP. Human babesiosis in Germany: Just overlooked or truly new? Int J Med Microbiol 2008;298:336–46.Google Scholar
  50. 50.
    Wójcik-Fatla A, Bartosik K, Buczek A, Dutkiewicz J. Babesia microti in adult Dermacentor reticulatus ticks from eastern Poland. Vector Borne Zoonotic Dis. 2012;12:841–3. doi:10.1089/vbz.2011.0904.PubMedGoogle Scholar
  51. 51.
    Walter G. Transmission of Babesia microti by nymphs of Dermacentor marginatus, D. reticulatus, Haemaphysalis punctata, Rhipicephalus sanguineus and Ixodes hexagonus. Z Parasitenkd. 1982;66:353–4.PubMedGoogle Scholar
  52. 52.
    Skotarczak B, Cichocka A. Isolation and amplification by polymerase chain reaction DNA of Babesia microti and Babesia divergens in ticks in Poland. Ann Agric Environ Med. 2001;8:187–9.PubMedGoogle Scholar
  53. 53.
    Hartelt K, Oehme R, Frank H, Brockmann SO, Hassler D, Kimmig P. Pathogens and symbionts in ticks: prevalence of Anaplasma phagocytophilum (Ehrlichia sp.), Wolbachia sp., Rickettsia sp., and Babesia sp. in Southern Germany. Int J Med Microbiol. 2004;293:86–92.PubMedGoogle Scholar
  54. 54.
    Halos L, Jamal T, Maillard R, Beugnet F, Le Menach A, Boulouis HJ, Vayssier-Taussat M. Evidence of Bartonella sp. in questing adult and nymphal Ixodes ricinus ticks from France and co-infection with Borrelia burgdorferi sensu lato and Babesia sp. Vet Res. 2005;36:79–87. doi:10.1051/vetres:2004052.PubMedGoogle Scholar
  55. 55.
    Casati S, Sager H, Gern L, Piffaretti JC. Presence of potentially pathogenic Babesia sp. for human in Ixodes ricinus in Switzerland. Ann Agric Environ Med. 2006;13:65–70.PubMedGoogle Scholar
  56. 56.
    Piccolin G, Benedetti G, Doglioni C, Lorenzato C, Mancuso S, Papa N, Pitton L, Ramon MC, Zasio C, Bertiato G. A study of the presence of B. burgdorferi, Anaplasma (previously Ehrlichia) phagocytophilum, Rickettsia, and Babesia in Ixodes ricinus collected within the territory of Belluno, Italy. Vector Borne Zoonotic Dis. 2006;6:24–31. doi:10.1089/vbz.2006.6.24.PubMedGoogle Scholar
  57. 57.
    Wielinga PR, Fonville M, Sprong H, Gaasenbeek C, Borgsteede F, van der Giessen JW. Persistent detection of Babesia EU1 and Babesia microti in Ixodes ricinus in the Netherlands during a 5-year surveillance: 2003–2007. Vector Borne Zoonotic Dis. 2009;9:119–22. doi:10.1089/vbz.2008.0047.PubMedGoogle Scholar
  58. 58.
    Reye AL, Hübschen JM, Sausy A, Muller CP. Prevalence and seasonality of tick-borne pathogens in questing Ixodes ricinus ticks from Luxembourg. Appl Environ Microbiol. 2010;76:2923–31. doi:10.1128/AEM.03061-09.PubMedGoogle Scholar
  59. 59.
    Cassini R, Bonoli C, Montarsi F, Tessarin C, Marcer F, Galuppi R. Detection of Babesia EU1 in Ixodes ricinus ticks in northern Italy. Vet Parasitol. 2010;171:151–4. doi:10.1016/j.vetpar.2010.03.009.PubMedGoogle Scholar
  60. 60.
    Hildebrandt A, Franke J, Schmoock G, Pauliks K, Kramer A, Straube E. Diversity and coexistence of tick-borne pathogens in central Germany. J Med Entomol. 2011;48:651–5.PubMedGoogle Scholar
  61. 61.
    Franke J, Hildebrandt A, Meier F, Straube E, Dorn W. Prevalence of Lyme disease agents and several emerging pathogens in questing ticks from the German Baltic coast. J Med Entomol. 2011;48:441–4.PubMedGoogle Scholar
  62. 62.
    Gigandet L, Stauffer E, Douet V, Rais O, Moret J, Gern L. Prevalence of three zoonotic Babesia species in Ixodes ricinus (Linne, 1758) nymphs in a suburban forest in Switzerland. Vector Borne Zoonotic Dis. 2011;11:363–6. doi:10.1089/vbz.2010.0195.PubMedGoogle Scholar
  63. 63.
    Schorn S, Pfister K, Reulen H, Mahling M, Silaghi C. Occurrence of Babesia spp., Rickettsia spp. and Bartonella spp. in Ixodes ricinus in Bavarian public parks, Germany. Parasit Vectors. 2011;4:135. doi:10.1186/1756-3305-4-135.PubMedGoogle Scholar
  64. 64.
    Lempereur L, De Cat A, Caron Y, Madder M, Claerebout E, Saegerman C, Losson B. First molecular evidence of potentially zoonotic Babesia microti and Babesia sp. EU1 in Ixodes ricinus ticks in Belgium. Vector Borne Zoonotic Dis. 2011;11:125–30. doi:10.1089/vbz.2009.0189.PubMedGoogle Scholar
  65. 65.
    Reis C, Cote M, Paul RE, Bonnet S. Questing ticks in suburban forest are infected by at least six tick-borne pathogens. Vector Borne Zoonotic Dis. 2011;11:907–16. doi:10.1089/vbz.2010.0103.PubMedGoogle Scholar
  66. 66.
    Egyed L, Elő P, Sréter-Lancz Z, Széll Z, Balogh Z, Sréter T. Seasonal activity and tick-borne pathogen infection rates of Ixodes ricinus ticks in Hungary. Ticks Tick Borne Dis. 2012;3:90–4. doi:10.1016/j.ttbdis.2012.01.002.PubMedGoogle Scholar
  67. 67.
    Lommano E, Bertaiola L, Dupasquier C, Gern L. Infections and coinfections of questing Ixodes ricinus ticks by emerging zoonotic pathogens in Western Switzerland. Appl Environ Microbiol. 2012;78:4606–12. doi:10.1128/AEM.07961-11.PubMedGoogle Scholar
  68. 68.
    Øines Ø, Radzijevskaja J, Paulauskas A, Rosef O. Prevalence and diversity of Babesia spp. in questing Ixodes ricinus ticks from Norway. Parasit Vectors. 2012;5:156. doi:10.1186/1756-3305-5-156.
  69. 69.
    Blaschitz M, Narodoslavsky-Gföller M, Kanzler M, Stanek G, Walochnik J. Babesia species occurring in Austrian Ixodes ricinus ticks. Appl Environ Microbiol. 2008;74:4841–6. doi:10.1128/AEM.00035-08.PubMedGoogle Scholar
  70. 70.
    Franke J, Fritzsch J, Tomaso H, Straube E, Dorn W, Hildebrandt A. Coexistence of pathogens in host-seeking and feeding ticks within a single natural habitat in Central Germany. Appl Environ Microbiol. 2010;76:6829–36. doi:10.1128/AEM.01630-10.PubMedGoogle Scholar
  71. 71.
    Hildebrandt A, Franke J, Meier F, Sachse S, Dorn W, Straube E. The potential role of migratory birds in transmission cycles of Babesia spp., Anaplasma phagocytophilum, and Rickettsia spp. Ticks Tick Borne Dis. 2010;1:105–7. doi:10.1016/j.ttbdis.2009.12.003.
  72. 72.
    Hasle G, Leinaas HP, Røed KH, Øines Ø. Transport of Babesia venatorum-infected Ixodes ricinus to Norway by northward migrating passerine birds. Acta Vet Scand. 2011;53:41. doi:10.1186/1751-0147-53-41.PubMedGoogle Scholar
  73. 73.
    Movila A, Reye AL, Dubinina HV, Tolstenkov OO, Toderas I, Hübschen JM, Muller CP, Alekseev AN. Detection of Babesia sp. EU1 and members of spotted fever group rickettsiae in ticks collected from migratory birds at Curonian Spit, North-Western Russia. Vector Borne Zoonotic Dis. 2011;11:89–91. doi:10.1089/vbz.2010.0043.PubMedGoogle Scholar
  74. 74.
    Skotarczak B, Rymaszewska A, Wodecka B, Sawczuk M. Molecular evidence of coinfection of Borrelia burgdorferi sensu lato, human granulocytic ehrlichiosis agent, and Babesia microti in ticks from northwestern Poland. J Parasitol. 2003;89:194–6. doi:10.1645/0022-3395(2003)089[0194:MEOCOB]2.0.CO;2.Google Scholar
  75. 75.
    Wójcik-Fatla A, Szymańska J, Wdowiak L, Buczek A, Dutkiewicz J. Coincidence of three pathogens (Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum and Babesia microti) in Ixodes ricinus ticks in the Lublin macroregion. Ann Agric Environ Med. 2009;16:151–8.PubMedGoogle Scholar
  76. 76.
    Hildebrandt A, Fritzsch J, Franke J, Sachse S, Dorn W, Straube E. Co-circulation of emerging tick-borne pathogens in Middle Germany. Vector Borne Zoonotic Dis. 2011;11:533–7. doi:10.1089/vbz.2010.0048.PubMedGoogle Scholar
  77. 77.
    Sytykiewicz H, Karbowiak G, Hapunik J, Szpechciński A, Supergan-Marwicz M, Golawska S, Sprawka I, Czerniewicz P. Molecular evidence of Anaplasma phagocytophilum and Babesia microti co-infections in Ixodes ricinus ticks in central-eastern region of Poland. Ann Agric Environ Med. 2012;19:45–9.PubMedGoogle Scholar
  78. 78.
    Hunfeld KP, Brade V. Zoonotic Babesia: possibly emerging pathogens to be considered for tick-infested humans in Central Europe. Int J Med Microbiol. 2004;293:93–103.PubMedGoogle Scholar
  79. 79.
    Esernio-Jenssen D, Scimeca PG, Benach JL, Tenenbaum MJ. Transplacental/perinatal babesiosis. J Pediatr. 1987;110:570–2.PubMedGoogle Scholar
  80. 80.
    New DL, Quinn JB, Qureshi MZ, Sigler SJ. Vertically transmitted babesiosis. J Pediatr. 1997;131:163–4.PubMedGoogle Scholar
  81. 81.
    Sethi S, Alcid D, Kesarwala H, Tolan RW Jr. Probable congenital babesiosis in infant, new jersey, USA. Emerg Infect Dis. 2009;15:788–91. doi:10.3201/eid1505.070808.PubMedGoogle Scholar
  82. 82.
    Aderinboye O, Syed SS. Congenital babesiosis in a four-week-old female infant. Pediatr Infect Dis J. 2010;29:188. doi:10.1097/INF.0b013e3181c3c971.PubMedGoogle Scholar
  83. 83.
    Joseph JT, Purtill K, Wong SJ, Munoz J, Teal A, Madison-Antenucci S, Horowitz HW, Aguero-Rosenfeld ME, Moore JM, Abramowsky C, Wormser GP. Vertical transmission of Babesia microti, United States. Emerg Infect Dis. 2012;18:1318–21. doi:10.3201/eid1808.110988.PubMedGoogle Scholar
  84. 84.
    Mylonakis E. When to suspect and how to monitor babesiosis. Am Fam Physician. 2001;63:1969–74.PubMedGoogle Scholar
  85. 85.
    Telford SR, 3rd, Maguire JH. Babesiosis. In: Guerrant RL, Walker DH, Weller PF editors. Tropical infectious diseases: principles, pathogens, and practice. Oxford: Churchill Livingstone. 2006. p. 1063–71.Google Scholar
  86. 86.
    Benach JL, Habicht GS, Hamburger MI. Immunoresponsiveness in acute babesiosis in humans. J Infect Dis. 1982;146:369–80.PubMedGoogle Scholar
  87. 87.
    Kjemtrup AM, Conrad PA. Human babesiosis: an emerging tick-borne disease. Int J Parasitol. 2000;30:1323–37.PubMedGoogle Scholar
  88. 88.
    Hatcher JC, Greenberg PD, Antique J, Jimenez-Lucho VE. Severe babesiosis in Long Island: review of 34 cases and their complications. Clin Infect Dis. 2001;32:1117–25. doi:10.1086/319742.PubMedGoogle Scholar
  89. 89.
    Pantanowitz L, Cannon ME. Extracellular Babesia microti parasites. Transfusion. 2001;41:440.PubMedGoogle Scholar
  90. 90.
    Gubernot DM, Nakhasi HL, Mied PA, Asher DM, Epstein JS, Kumar S. Transfusion-transmitted babesiosis in the United States: summary of a workshop. Transfusion. 2009;49:2759–71. doi:10.1111/j.1537-2995.2009.02429.x.PubMedGoogle Scholar
  91. 91.
    Krause PJ, Telford SR 3rd, Spielman A, Sikand V, Ryan R, Christianson D, Burke G, Brassard P, Pollack R, Peck J, Persing DH. Concurrent Lyme disease and babesiosis. Evidence for increased severity and duration of illness. JAMA. 1996;275:1657–60.PubMedGoogle Scholar
  92. 92.
    Swanson SJ, Neitzel D, Reed KD, Belongia EA. Coinfections acquired from ixodes ticks. Clin Microbiol Rev. 2006;19:708–27. doi:10.1128/CMR.00011-06.PubMedGoogle Scholar
  93. 93.
    Krause PJ, Spielman A, Telford SR 3rd, Sikand VK, McKay K, Christianson D, Pollack RJ, Brassard P, Magera J, Ryan R, Persing DH. Persistent parasitemia after acute babesiosis. N Engl J Med. 1998;339:160–5. doi:10.1056/NEJM199807163390304.PubMedGoogle Scholar
  94. 94.
    Leiby DA. Babesiosis and blood transfusion: flying under the radar. Vox Sang. 2006;90:157–65. doi:10.1111/j.1423-0410.2006.00740.x.PubMedGoogle Scholar
  95. 95.
    Gray JS, Weiss LM. Babesia microti. In: Khan NA, editor. Emerging Protozoan Pathogens. Abingdon: Taylor and Francis. 2008. p. 303–49.Google Scholar
  96. 96.
    Saito-Ito A, Tsuji M, Wei Q, He S, Matsui T, Kohsaki M, Arai S, Kamiyama T, Hioki K, Ishihara C. Transfusion-acquired, autochthonous human babesiosis in Japan: isolation of Babesia microti-like parasites with hu-RBC-SCID mice. J Clin Microbiol. 2000;38:4511–6.PubMedGoogle Scholar
  97. 97.
    Vannier E, Krause PJ. Update on babesiosis. Interdiscip Perspect Infect Dis. 2009;2009:984568. doi:10.1155/2009/984568.PubMedGoogle Scholar
  98. 98.
    Gorenflot A, Moubri K, Precigout E, Carcy B, Schetters TP. Human babesiosis. Ann Trop Med Parasitol. 1998;92:489–501.PubMedGoogle Scholar
  99. 99.
    Zintl A, Mulcahy G, Skerrett HE, Taylor SM, Gray JS. Babesia divergens, a bovine blood parasite of veterinary and zoonotic importance. Clin Microbiol Rev. 2003;16:622–36.PubMedGoogle Scholar
  100. 100.
    Bruckner DA, Garcia LS, Shimizu RY, Goldstein EJ, Murray PM, Lazar GS. Babesiosis: problems in diagnosis using autoanalyzers. Am J Clin Pathol. 1985;83:520–1.PubMedGoogle Scholar
  101. 101.
    Krause PJ, Telford SR 3rd. Babesiosis. In: Gilles HM, editor. Protozoal Diseases. Arnold: London; 1999. p. 236–48.Google Scholar
  102. 102.
    Teal AE, Habura A, Ennis J, Keithly JS, Madison-Antenucci S. A new real-time PCR assay for improved detection of the parasite Babesia microti. J Clin Microbiol. 2012;50:903–8. doi:10.1128/JCM.05848-11.PubMedGoogle Scholar
  103. 103.
    Persing DH, Mathiesen D, Marshall WF, Telford SR, Spielman A, Thomford JW, Conrad PA. Detection of Babesia microti by polymerase chain reaction. J Clin Microbiol. 1992;30:2097–103.PubMedGoogle Scholar
  104. 104.
    Thomford JW, Conrad PA, Telford SR 3rd, Mathiesen D, Bowman BH, Spielman A, Eberhard ML, Herwaldt BL, Quick RE, Persing DH. Cultivation and phylogenetic characterization of a newly recognized human pathogenic protozoan. J Infect Dis. 1994;169:1050–6.PubMedGoogle Scholar
  105. 105.
    Persing DH, Conrad PA. Babesiosis: new insights from phylogenetic analysis. Infect Agents Dis. 1995;4:182–95.PubMedGoogle Scholar
  106. 106.
    Johnson ST, Cable RG, Leiby DA. Lookback investigations of Babesia microti-seropositive blood donors: seven-year experience in a Babesia-endemic area. Transfusion. 2012;52:1509–16. doi:10.1111/j.1537-2995.2011.03345.x.PubMedGoogle Scholar
  107. 107.
    Bloch EM, Lee TH, Krause PJ, Telford SR 3rd, Montalvo L, Chafets D, Usmani-Brown S, Lepore TJ, Busch MP. Development of a real-time polymerase chain reaction assay for sensitive detection and quantitation of Babesia microti infection. Transfusion. 2013;. doi:10.1111/trf.12098.Google Scholar
  108. 108.
    Espy MJ, Uhl JR, Sloan LM, Buckwalter SP, Jones MF, Vetter EA, Yao JD, Wengenack NL, Rosenblatt JE, Cockerill FR 3rd, Smith TF. Real-time PCR in clinical microbiology: applications for routine laboratory testing. Clin Microbiol Rev. 2006;19:165–256. doi:10.1128/CMR.19.1.165-256.2006.PubMedGoogle Scholar
  109. 109.
    Mosqueda J, Olvera-Ramirez A, Aguilar-Tipacamu G, Canto GJ. Current advances in detection and treatment of babesiosis. Curr Med Chem. 2012;19:1504–18.PubMedGoogle Scholar
  110. 110.
    Johnson N, Voller K, Phipps LP, Mansfield K, Fooks AR. Rapid molecular detection methods for arboviruses of livestock of importance to northern Europe. J Biomed Biotechnol. 2012;2012:719402. doi:10.1155/2012/719402.PubMedGoogle Scholar
  111. 111.
    Krause PJ, Telford S 3rd, Spielman A, Ryan R, Magera J, Rajan TV, Christianson D, Alberghini TV, Bow L, Persing D. Comparison of PCR with blood smear and inoculation of small animals for diagnosis of Babesia microti parasitemia. J Clin Microbiol. 1996;34:2791–4.PubMedGoogle Scholar
  112. 112.
    Herwaldt BL, McGovern PC, Gerwel MP, Easton RM, MacGregor RR. Endemic babesiosis in another eastern state: New Jersey. Emerg Infect Dis. 2003;9:184–8.PubMedGoogle Scholar
  113. 113.
    Krause PJ, Telford SR 3rd, Ryan R, Conrad PA, Wilson M, Thomford JW, Spielman A. Diagnosis of babesiosis: evaluation of a serologic test for the detection of Babesia microti antibody. J Infect Dis. 1994;169:923–6.PubMedGoogle Scholar
  114. 114.
    Gelfand JA. Babesia. In: Mandell GL, Douglas RG, Bennett JE, Dolin R, editors. Mandell, Douglas, and Bennett’s Principles and Practice of Infectious Diseases. 5th ed. Churchill Livingstone: New York; 2000. p. 2899–902.Google Scholar
  115. 115.
    Gabrielli S, Galuppi R, Marcer F, Marini C, Tampieri MP, Moretti A, Pietrobelli M, Cancrini G. Development of culture-based serological assays to diagnose Babesia divergens infections. Vector Borne Zoonotic Dis. 2012;12:106–10. doi:10.1089/vbz.2011.0706.PubMedGoogle Scholar
  116. 116.
    WHO. World Health Organisation Veterinary Public Health Unit: WHO Workshop on Lyme Borreliosis Diagnosis and Surveillance. Document No. WHO/CDS/VPH/95.141. Geneva: World Health Organization 1995.Google Scholar
  117. 117.
    Palmer GH, McElwain TF. Molecular basis for vaccine development against anaplasmosis and babesiosis. Vet Parasitol. 1995;57:233–53.PubMedGoogle Scholar
  118. 118.
    Musoke AJ, Palmer GH, McElwain TF, Nene V, McKeever D. Prospects for subunit vaccines against tick-borne diseases. Br Vet J. 1996;152:621–39.PubMedGoogle Scholar
  119. 119.
    Priest JW, Moss DM, Won K, Todd CW, Henderson L, Jones CC, Wilson M. Multiplex assay detection of immunoglobulin G antibodies that recognize Babesia microti antigens. Clin Vaccine Immunol. 2012;19:1539–48. doi:10.1128/CVI.00313-12.PubMedGoogle Scholar
  120. 120.
    Homer MJ, Lodes MJ, Reynolds LD, Zhang Y, Douglass JF, McNeill PD, Houghton RL, Persing DH. Identification and characterization of putative secreted antigens from Babesia microti. J Clin Microbiol. 2003;41:723–9.PubMedGoogle Scholar
  121. 121.
    Wormser GP, Dattwyler RJ, Shapiro ED, Halperin JJ, Steere AC, Klempner MS, Krause PJ, Bakken JS, Strle F, Stanek G, Bockenstedt L, Fish D, Dumler JS, Nadelman RB. The clinical assessment, treatment, and prevention of lyme disease, human granulocytic anaplasmosis, and babesiosis: clinical practice guidelines by the Infectious Diseases Society of America. Clin Infect Dis. 2006;43:1089–134. doi:10.1086/508667.PubMedGoogle Scholar
  122. 122.
    Gelfand JA Vannier E. Clinical manifestations, diagnosis, treatment, and prevention of babesiosis. http://wwwuptodatecom/contents/clinical-manifestations-diagnosis-treatment-and-prevention-of-babesiosis#H1. Accessed online 11 Sept 2013.
  123. 123.
    Vial HJ, Gorenflot A. Chemotherapy against babesiosis. Vet Parasitol. 2006;138:147–60. doi:10.1016/j.vetpar.2006.01.048.PubMedGoogle Scholar
  124. 124.
    Krause PJ, Lepore T, Sikand VK, Gadbaw J Jr, Burke G, Telford SR 3rd, Brassard P, Pearl D, Azlanzadeh J, Christianson D, McGrath D, Spielman A. Atovaquone and azithromycin for the treatment of babesiosis. N Engl J Med. 2000;343:1454–8. doi:10.1056/NEJM200011163432004.PubMedGoogle Scholar
  125. 125.
    Wittner M, Lederman J, Tanowitz HB, Rosenbaum GS, Weiss LM. Atovaquone in the treatment of Babesia microti infections in hamsters. Am J Trop Med Hyg. 1996;55:219–22.PubMedGoogle Scholar
  126. 126.
    Marley SE, Eberhard ML, Steurer FJ, Ellis WL, McGreevy PB, Ruebush TK 2nd. Evaluation of selected antiprotozoal drugs in the Babesia microti-hamster model. Antimicrob Agents Chemother. 1997;41:91–4.PubMedGoogle Scholar
  127. 127.
    Rowin KS, Tanowitz HB, Wittner M. Therapy of experimental babesiosis. Ann Intern Med. 1982;97:556–8.PubMedGoogle Scholar
  128. 128.
    Wittner M, Rowin KS, Tanowitz HB, Hobbs JF, Saltzman S, Wenz B, Hirsch R, Chisholm E, Healy GR. Successful chemotherapy of transfusion babesiosis. Ann Intern Med. 1982;96:601–4.PubMedGoogle Scholar
  129. 129.
    Weiss LM. Babesiosis in humans: a treatment review. Expert Opin Pharmacother. 2002;3:1109–15. doi:10.1517/14656566.3.8.1109.PubMedGoogle Scholar
  130. 130.
    Brasseur P, Lecoublet S, Kapel N, Favennec L, Ballet JJ. Quinine in the treatment of Babesia divergens infections in humans. Eur J Clin Microbiol Infect Dis. 1996;15:840–1.PubMedGoogle Scholar
  131. 131.
    Denes E, Rogez JP, Dardé ML, Weinbreck P. Management of Babesia divergens babesiosis without a complete course of quinine treatment. Eur J Clin Microbiol Infect Dis. 1999;18:672–3.PubMedGoogle Scholar
  132. 132.
    Corpelet C, Vacher P, Coudore F, Laurichesse H, Conort N, Souweine B. Role of quinine in life-threatening Babesia divergens infection successfully treated with clindamycin. Eur J Clin Microbiol Infect Dis. 2005;24:74–5. doi:10.1007/s10096-004-1270-x.PubMedGoogle Scholar
  133. 133.
    Pudney M, Gray JS. Therapeutic efficacy of atovaquone against the bovine intraerythrocytic parasite, Babesia divergens. J Parasitol. 1997;83:307–10.PubMedGoogle Scholar
  134. 134.
    Gorenflot A, Bazin C, Ambroise-Thomas P. Human babesiosis. Treatment of severe forms. Presse Med. 1987;16:1099.PubMedGoogle Scholar
  135. 135.
    Weiss LM, Wittner M, Wasserman S, Oz HS, Retsema J, Tanowitz HB. Efficacy of azithromycin for treating Babesia microti infection in the hamster model. J Infect Dis. 1993;168:1289–92.PubMedGoogle Scholar
  136. 136.
    Gray JS, Pudney M. Activity of atovaquone against Babesia microti in the Mongolian gerbil, Meriones unguiculatus. J Parasitol. 1999;85:723–8.PubMedGoogle Scholar
  137. 137.
    Meldrum SC, Birkhead GS, White DJ, Benach JL, Morse DL. Human babesiosis in New York State: an epidemiological description of 136 cases. Clin Infect Dis. 1992;15:1019–23.PubMedGoogle Scholar
  138. 138.
    Wormser GP, Prasad A, Neuhaus E, Joshi S, Nowakowski J, Nelson J, Mittleman A, Aguero-Rosenfeld M, Topal J, Krause PJ. Emergence of resistance to azithromycin-atovaquone in immunocompromised patients with Babesia microti infection. Clin Infect Dis. 2010;50:381–6. doi:10.1086/649859.PubMedGoogle Scholar
  139. 139.
    Spencer AM, Goethert HK, Telford SR 3rd. Holman PJ. In vitro host erythrocyte specificity and differential morphology of Babesia divergens and a zoonotic Babesia sp. from eastern cottontail rabbits (Sylvilagus floridanus). J Parasitol. 2006;92:333–40. doi:10.1645/GE-662R.1.PubMedGoogle Scholar
  140. 140.
    Kogut SJ, Thill CD, Prusinski MA, Lee JH, Backerson PB, Coleman JL, Anand M, White DJ. Babesia microti, upstate New York. Emerg Infect Dis. 2005;11:476–8.PubMedGoogle Scholar
  141. 141.
    Stramer SL, Hollinger FB, Katz LM, Kleinman S, Metzel PS, Gregory KR, Dodd RY. Emerging infectious disease agents and their potential threat to transfusion safety. Transfusion. 2009;49:1S–29S. doi:10.1111/j.1537-2995.2009.02279.x.PubMedGoogle Scholar
  142. 142.
    Pantanowitz L, Aufranc S 3rd, Monahan-Earley R, Dvorak A, Telford SR 3rd. Transfusion medicine illustrated. Morphologic hallmarks of Babesia. Transfusion. 2002;42:1389.PubMedGoogle Scholar
  143. 143.
    Grabowski EF, Giardina PJ, Goldberg D, Masur H, Read SE, Hirsch RL, Benach JL. Babesiosis transmitted by a transfusion of frozen-thawed blood. Ann Intern Med. 1982;96:466–7.PubMedGoogle Scholar
  144. 144.
    Zhao Y, Love KR, Hall SW, Beardell FV. A fatal case of transfusion-transmitted babesiosis in the State of Delaware. Transfusion. 2009;49:2583–7. doi:10.1111/j.1537-2995.2009.02454.x.PubMedGoogle Scholar
  145. 145.
    Setty S, Khalil Z, Schori P, Azar M, Ferrieri P. Babesiosis. Two atypical cases from Minnesota and a review. Am J Clin Pathol. 2003;120:554–9. doi:10.1309/N3DP-9MFP-NUJD-4XJY.PubMedGoogle Scholar
  146. 146.
    Matsui T, Inoue R, Kajimoto K, Tamekane A, Okamura A, Katayama Y, Shimoyama M, Chihara K, Saito-Ito A, Tsuji M. First documentation of transfusion-associated babesiosis in Japan. Rinsho Ketsueki. 2000;41:628–34.PubMedGoogle Scholar
  147. 147.
    Piesman J, Eisen L. Prevention of tick-borne diseases. Annu Rev Entomol. 2008;53:323–43. doi:10.1146/annurev.ento.53.103106.093429.PubMedGoogle Scholar
  148. 148.
    Siński E, Welc-Falęciak R, Pogłód R. Babesia spp. infections transmitted through blood transfusion. Wiad Parazytol. 2011;57:77–81.PubMedGoogle Scholar
  149. 149.
    White DJ, Talarico J, Chang HG, Birkhead GS, Heimberger T, Morse DL. Human babesiosis in New York State: review of 139 hospitalized cases and analysis of prognostic factors. Arch Intern Med. 1998;158:2149–54.PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Medical University Laboratories, Institute of Medical MicrobiologyFriedrich-Schiller-University JenaJenaGermany
  2. 2.UCD School of Biology and Environmental ScienceUniversity College DublinDublin 4Ireland
  3. 3.Institute of Laboratory Medicine, Microbiology and Infection ControlNorthwest Medical CentreFrankfurt/MainGermany

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