Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Biologia




More options …
Volume 65, Issue 6

Issues

Granulocytic anaplasmosis — emerging tick-borne disease of humans and animals

Mária Nováková / Bronislava Víchová
Published Online: 2010-10-15 | DOI: https://doi.org/10.2478/s11756-010-0119-2

Abstract

Granulocytic anaplasmoses represent a group of emerging tick-borne infectious diseases caused by the obligate intracellular gram-negative bacterium, Anaplasma phagocytophilum (Rickettsiales) that infects granulocytes. It has been known as a ruminant pathogen in Europe since 1932, however, recently it has emerged as a pathogen of humans and domestic animals such as dogs and horses in the Northern Hemisphere, including United States and Europe. Rodents and game animals (especially deer) are presumed to play a crucial role in the maintenance of A. phagocytophilum in natural foci and serve as competent reservoirs. Up to now, the presence of bacterial DNA has been confirmed by molecular methods in a number of domestic and wildlife animals. Circulation of several genotypes has been confirmed in natural foci but the vector competence and the host spectrum involved in its circulation is still under investigation. Human granulocytic anaplasmosis (HGA) typically occurs in spring or summer and clinical manifestations range from mild or self-limiting to severe disease, especially in elderly patients with up to 50% requiring hospitalization and 7% intensive care. So far, no confirmed A. phagocytophilum infections of humans have been reported in Slovakia despite the fact that the presence of anti-anaplasma antibodies has been detected in investigated patients sera. This fact could be explained by non-specific clinical signs of the infection or lack of information in physicians and underdiagnosed or misdiagnosed cases. The purpose of this review is to present biology, ecology and life cycle of A. phagocytophilum and introduce clinical symptoms, diagnosis and treatment of the infection caused by this pathogenic bacterium.

Keywords: Anaplasma phagocytophilum; human granulocytic anaplasmosis; tick-transmitted infections; Ixodes ricinus, Ticks

  • [1] Aguero-Rosenfeld M.E. 2003. Laboratory aspects of tick-borne diseases: Lyme, human granulocytic ehrlichiosis and babesiosis. Mt. Sinai. J. Med. 70: 197–203. Google Scholar

  • [2] Alberti A., Addis M.F., Sparagano O., Zobba R., Chessa B., Cubeddu T., Parpaglia M.L.P., Ardu M. & Pittau M. 2005. Anaplasma phagocytophilum, Sardinia, Italy. Emerg. Infect. Dis. 11: 1322–1323. CrossrefGoogle Scholar

  • [3] Alberdi M.P., Walker A.R. & Urquhart K.A. 2004. Field evidence that roe deer (Capreolus capreolus) are a natural host for Ehrlichia phagocytophila. Epidemiol. Infect. 124: 315–323. http://dx.doi.org/10.1017/S0950268899003684CrossrefGoogle Scholar

  • [4] Arnez M., Petrovec M., Lotric-Furlan S., Avsic Zupanc T. & Strle F. 2001. First European pediatric case of human granulocytic ehrlichiosis. J. Clin. Microbiol. 39: 4591–4592. DOI: 10.1128/JCM.39.12.4591-4592.2001 http://dx.doi.org/10.1128/JCM.39.12.4591-4592.2001CrossrefGoogle Scholar

  • [5] Bakken J.S., Krueth J., Tilden R.L., Asanovich K., Walls J.J. & Dumler J.S. 1997. Duration of IFA serologic response in humans infected with the agent of human granulocytic ehrlichiosis. Clin. Infect. Dis. 25: 368. Google Scholar

  • [6] Barbet A.F., Lundgren A.M., Alleman A.R., Stuen S., Bjöersdorff A., Brown R.N., Drazenovich N.L. & Foley J.E. 2006. Structure of the expression site reveals global diversity in MSP2 (P44) variants in Anaplasma phagocytophilum. Infect. Immun. 74: 6429–6437. DOI: 10.1128/IAI.00809-06 http://dx.doi.org/10.1128/IAI.00809-06CrossrefGoogle Scholar

  • [7] Blanco J.R. & Oteo J.A. 2002. Human granulocytic ehrlichiosis in Europe. Clin. Microbiol. Infect. Dis. 8: 763–772. http://dx.doi.org/10.1046/j.1469-0691.2002.00557.xCrossrefGoogle Scholar

  • [8] Bock R.E., DeVos A.J., Kingston T.G. & Carter P.D. 2003. Assessment of a low virulence Australian isolate of Anaplasma marginale for pathogenicity, immunogenicity and transmissibility by Boophilus microplus. Vet. Parasitol. 118: 121–131. DOI: 10.1016/j.natpar.2003.08.011 http://dx.doi.org/10.1016/j.vetpar.2003.08.011CrossrefGoogle Scholar

  • [9] Bown K.J., Begon M., Bennett M., Birtles M.J., Burthe S., Lambin X., Telfer S., Woldehiwet Z. & Ogden N.H. 2006. Sympatric Ixodes trianguliceps and Ixodes ricinus ticks feeding on field voles (Microtus agrestis): potential for increased risk of Anaplasma phagocytophilum in the United Kingdom? Vector Borne Zoonotic Dis. 6: 404–410. http://dx.doi.org/10.1089/vbz.2006.6.404CrossrefGoogle Scholar

  • [10] Bown K.J., Lambin X., Ogden N.H., Begon M., Telford G., Woldehiwet Z. & Birtles R.J. 2009. Delineating Anaplasma phagocytophilum ecotypes in coexisting, discrete enzootic cycles. Emerg. Infect. Dis. 15: 1948–1954. DOI: 10.3201/eid1512.09 0178 http://dx.doi.org/10.3201/eid1512.090178CrossrefGoogle Scholar

  • [11] Brouqui P. 1999. Ehrlichiosis in Europe, pp. 220–232. In: Raoult D. & Brouqui P. (eds), Rickettsiae and rickettsial diseases at the turn of the third millenium. Elsevier, Paris. Google Scholar

  • [12] Brouqui P., Bacellar F., Baranton G., Birtles R.J., Bjoërsdorff A., Blanco J.R., Caruso G., Cinco M., Fournier P.E., Francavilla E., Jensenius M., Kazar J., Laferl H., Lakos A., Lotric Furlan S., Maurin M., Oteo J.A., Parola P., Perez-Eid C., Peter O., Postic D., Raoult D., Tellez A., Tselentis Y. & Wilske B. 2004. Guidelines for the diagnosis of tick-borne bacterial diseases in Europe. Clin. Microbiol. Infect. 10: 1108–1132. http://dx.doi.org/10.1111/j.1469-0691.2004.01019.xCrossrefGoogle Scholar

  • [13] Buller R.S., Arens M., Hmiel S.P., Paddock C.D., Sumner J.W., Rikihisa Y., Unver A., Gaudreault-Keener M., Manian F.A., Liddell A.M., Schmulewitz N. & Storch G.A. 1999. Ehrlichia ewingii, a newly recognized agent of human ehrlichiosis. N. Engl. J. Med. 341: 148–155. http://dx.doi.org/10.1056/NEJM199907153410303CrossrefGoogle Scholar

  • [14] Chen S.M., Dumler J.S., Bakken J.S. & Walker D.H. 1994. Identification of a granulocytotropic Ehrlichia species as the etiologic agent of human disease. J. Clin. Microbiol. 32: 589–595. Google Scholar

  • [15] De Castro M.B., Machado R.Z., de Aquino L.P., Alessi A.C. & Costa M.T. 2004. Experimental acute canine monocytic ehrlichiosis: clinicopathological and immunopathological findings. Vet. Parasitol. 119: 73–86. DOI: 10.1016/j.natpar.2003.10.012 http://dx.doi.org/10.1016/j.vetpar.2003.10.012CrossrefGoogle Scholar

  • [16] De La Fuente J., Atkinson M.W., Hogg J.T., Miller D.S., Naranjo V., Almazán C., Anderson N. & Kocan K.M. 2006. Genetic characterization of Anaplasma ovis strains from bighorn sheep in Montana. J. Wildl. Dis. 42: 381–385. Google Scholar

  • [17] De La Fuente J., Naranjo V., Ruiz-Fons F., Höfle U., De Mera IG F., Villanúa D., Almazán C., Torina A., Caracappa S., Kocan K.M. & Gortázar C. 2005. Potential vertebrate reservoir hosts and invertebrate vectors of Anaplasma marginale and A. phagocytophilum in central Spain. Vector Borne Zoonotic Dis. 5: 390–401. http://dx.doi.org/10.1089/vbz.2005.5.390CrossrefGoogle Scholar

  • [18] Derdáková M., Halanová M., Stanko M., Štefančíková A., Čisláková L. & Pet’ko B. 2003. Molecular evidence for Anaplasma phagocytophilum and Borrelia burgdorferi sensu lato in Ixodes ricinus ticks from eastern Slovakia. Ann. Agric. Environ. Med. 10: 269–271. Google Scholar

  • [19] Dumler J.S., Barbet A.F., Bekker C.P.J., Dasch G.A., Palmer G.H., Ray S.C., Rikihisa Y. & Rurangiwra F.R. 2001. Reorganization of genera in the families Rickettsiaceae and Anaplasmataceae in the order Rickettsiales: unification of some species of Ehrlichia with Anaplasma, Cowdria with Ehrlichia and Ehrlichia with Neorickettsia, descriptions of six new species combinations and designation of Ehrlichia equi and “HGE agent” as subjective synonyms of Ehrlichia phagocytophila. Int. J. Syst. Evol. Microbiol. 51: 2145–2165. Google Scholar

  • [20] Dumler J.S., Choi K.S., Garcia-Garcia J.C., Barat N.S., Scorpio D.G., Garyu J.W., Grab D.J. & Bakken J.S. 2005. Human granulocytic anaplasmosis and Anaplasma phagocytophilum. Emerg. Infect. Dis. 11: 1828–1834. CrossrefGoogle Scholar

  • [21] Foley J.E., Foley P. & Madigan J.E. 2001. Spatial distribution of seropositivity to the causative agent of granulocytic ehrlichiosis in dogs in California. Am. J. Vet. Res. 62: 1599–1605. http://dx.doi.org/10.2460/ajvr.2001.62.1599CrossrefGoogle Scholar

  • [22] Harvey J.W., Simpson C.F. & Gaskin J.M. 1978. Cyclic thrombocytopenia induced by a Rickettsia-like agent in dogs. J. Infect. Dis. 137: 182–188. CrossrefGoogle Scholar

  • [23] Hulínska D., Langerova K., Pejčoch M. & Pavlásek I. 2004. Detection of Anaplasma phagocytophilum in animals by real-time polymerase chain reaction. APMIS. 112: 239–247. http://dx.doi.org/10.1111/j.1600-0463.2004.apm11204-0503.xCrossrefGoogle Scholar

  • [24] Kawahara M., Rikihisa Y., Isogai E., Takahashi M., Misumi H., Suto C., Shibata S., Zhang C. & Tsuji M. 2004. Ultrastructure and phylogenetic analysis of “Candidatus Neoehrlichia mikurensis” in the family Anaplasmataceae, isolated from wild rats and found in Ixodes ovatus ticks. Int. J. Syst. Evol. Microbiol. 54: 1837–1843. http://dx.doi.org/10.1099/ijs.0.63260-0CrossrefGoogle Scholar

  • [25] Kawahara M., Suto C., Rikihisa Y., Yamamoto S. & Tsuboi Y. 1993. Characterization of ehrlichial organisms isolated from a wild mouse. J. Clin. Microbiol. 31: 89–96. Google Scholar

  • [26] Kocan K.M., De la Fuente J., Blouin E.F. & Garcia-Garcia J.C. 2004. Anaplasma marginale (Rickettsiales: Anaplasmataceae): recent advances in defining host-pathogen adaptations of a tick-borne rickettsia. Parasitology 129: 285–300. http://dx.doi.org/10.1017/S0031182003004700CrossrefGoogle Scholar

  • [27] Kocianová E., Blaškovič D., Smetanová K., Schwarzová K., Boldiš V., Košťanová Z., Müllerová D. & Barák I. 2008a. Comparison of an oligo-chip based assay with PCR method to measure the prevalence of tick-borne pathogenic bacteria in Central Slovakia. Biologia 63: 34–37. http://dx.doi.org/10.2478/s11756-008-0007-1CrossrefGoogle Scholar

  • [28] Kocianová E., Košťanová Z., Štefanidesová K., Špitalská E., Boldiš V., Hučková D. & Stanek G. 2008b. Serologic evidence of Anaplasma phagocytophilum infections in patients with a history of tick bite in central Slovakia. Wien. Klin. Wochenschr. 120: 427–431. http://dx.doi.org/10.1007/s00508-008-1000-yCrossrefGoogle Scholar

  • [29] Krier J.P. & Ristic M. 1963. Anaplasmosis. VII. Experimental Anaplasma ovis infection in white-tailed deer (Dama virginiana). Am. J. Vet. Res. 24: 567–572. Google Scholar

  • [30] Kuttler K.L. 1984. Anaplasma infections in wild and domestic ruminants: a review. J. Wildl. Dis. 20: 12–20. Google Scholar

  • [31] Levin M.L., Nicholson W.L., Massung R.F., Sumner J.W. & Fish D. 2002. Comparison of the reservoir competence of mediumsized mammals and Peromyscus leucopus for Anaplasma phagocytophilum in Connecticut. Vector Borne Zoonotic Dis. 2: 125–136. http://dx.doi.org/10.1089/15303660260613693CrossrefGoogle Scholar

  • [32] Lewis G.E., Jr., Ristic M., Smith R.D., Lincoln T. & Stephenson E.H. 1977. The brown dog tick Rhipicephalus sanguineus and the dog as experimental hosts of Ehrlichia canis. Am. J. Vet. Res. 38: 1953–1955. Google Scholar

  • [33] Liz J.S., Anderes L., Sumner J.W., Massung R.F., Gern L., Rutti B. & Brossard, M. 2000. PCR detection of granulocytic ehrlichiae in Ixodes ricinus ticks and wild small mammals in western Switzerland. J. Clin. Microbiol. 38: 1002–1007. Google Scholar

  • [34] Liz J.S., Sumner J.W., Pfister K. & Brossard M. 2002. PCR detection and serological evidence of granulocytic ehrlichial infection in roe deer (Capreolus capreolus) and chamois (Rupicapra rupicapra). J. Clin. Microbiol. 40: 892–897. DOI: 10.1128/JCM.40.3.892-897.2002 http://dx.doi.org/10.1128/JCM.40.3.892-897.2002CrossrefGoogle Scholar

  • [35] Loebermann M., Fingerle V., Lademann M., Fritzsche C. & Reisinger E.C. 2006. Borrelia burgdorferi and Anaplasma phagocytophilum coinfection. Emerg. Infect. Dis. 12: 353–355. CrossrefGoogle Scholar

  • [36] Madigan J.E. 1993. Equine ehrlichiosis. Vet. Clin. North. Am. Equine. Pract. 9: 423–428. Google Scholar

  • [37] Maeda K., Markowitz N., Hawley R.C., Ristic M., Cox D. & McDate J.E. 1987. Human infection with Ehrlichia canis, a leukocytic rickettsia. N. Engl. J. Med. 316: 853–856. http://dx.doi.org/10.1056/NEJM198704023161406CrossrefGoogle Scholar

  • [38] Massung R. F., Mather T.N. & Levin M.L. 2006. Reservoir competency of goats for the Ap-Variant 1 Strain of Anaplasma phagocytophilum. Infect. Immun. 74: 1373–1375. DOI: 10.1128/IAI.74.2.1373-1375.2006 http://dx.doi.org/10.1128/IAI.74.2.1373-1375.2006CrossrefGoogle Scholar

  • [39] Massung R.F., Mauel M.J., Owens J.H., Allan N., Courtney J.W., Stafford III K.C. & Mather T.N. 2002. Genetic variants of Ehrlichia phagocytophila Rhode Island and Connecticut. Emerg. Infect. Dis. 8: 467–472. CrossrefGoogle Scholar

  • [40] Misic-Majerus L.J., Bujic N., Madjaric V. & Janes-Poje, V. 2000. First description of the human granulocytic ehrlichiosis in Croatia. Clin. Microbiol. Infect. 6: 194. Google Scholar

  • [41] Nakamura Y., Kawazu S. & Minami T. 1991. Analysis of protein comaprisons and surface protein epitopes of Anaplasma marginale and Anaplasma centrale. J. Vet. Med. Sci. 53: 73–79. CrossrefGoogle Scholar

  • [42] Nováková M., Víchová B., Majláthová V., Lesňáková A., Pochybová M. & Peťko B. 2010. First case of human granulocytic anaplasmosis from Slovakia. Ann. Agric. Environ. Med. 17: 129–133. Google Scholar

  • [43] Ogden N.H., Casey A.N.J., French N.P., Bown K.J., Adams J.D.W. & Woldehiwet Z. 2002. Natural Ehrlichia phagocytophila transmission coefficients from sheep ‘carriers’ to Ixodes ricinus ticks vary with the numbers of feeding ticks. Parasitology 124: 127–136. Google Scholar

  • [44] Petrovec M., Lotric-Furlan S., Avsic Zupanc T., Strle F., Brouqui P., Roux V. & Dumler J.S. 1997. Human disease in Europe caused by a granulocytic Ehrlichia species. J. Clin. Microbiol. 35: 1556–1559. Google Scholar

  • [45] Polin H., Hufnagl P., Haunschmid R., Gruber F. & Ladurner G. 2004. Molecular evidence of Anaplasma phagocytophilum in Ixodes ricinus ticks and wild animals in Austria. J. Clin. Microbiol. 42: 2285–2286. DOI: 10.1128/JCM.42.5.2285-2286.2004 http://dx.doi.org/10.1128/JCM.42.5.2285-2286.2004CrossrefGoogle Scholar

  • [46] Reubel G.H., Kimsey R.B., Barlough J.E. & Madigan J.E. 1998. Experimental transmission of Ehrlichia equi to horses through naturally infected ticks (Ixodes pacificus) from Northern California. J. Clin. Microbiol. 36: 2132–2134. Google Scholar

  • [47] Richter P.J., Kimsey R.B., Madigan J.E., Barlough J.E., Dumler J.S. & Brooks D.L. 1996. Ixodes pacificus (Acari: Ixodidae) as a vector of Ehrlichia equi (Rickettsiales: Ehrlichieae). J. Med. Entomol. 33: 1–5. Google Scholar

  • [48] Rikihisa Y. 1991. The tribe Ehrlichieae and ehrlichial diseases. Clin. Microbiol. Rev. 4: 286–308. Google Scholar

  • [49] Schouls L.M., Van de Pol I., Rijpkema S.G.T. & Schot C.S. 1999. Detection and identification of Ehrlichia, Borrelia burgdorferi sensu lato, and Bartonella species in dutch Ixodes ricinus ticks. J. Clin. Microbiol. 37: 2215–2222. Google Scholar

  • [50] Scoles G.A., Ueti M.W., Noh S.M., Knowles D.P. & Palmer G.H. 2007. Conservation of transmission phenotype of Anaplasma marginale (Rickettsiales: Anaplasmataceae) strains among Dermacentor and Rhipicephalus ticks (Acari: Ixodidae). J. Med. Entomol. 44: 484–491. http://dx.doi.org/10.1603/0022-2585(2007)44[484:COTPOA]2.0.CO;2Google Scholar

  • [51] Skotarczak B., Rymaszewska A., Wodecka B., Sawczuk M., Adamska M. & Maciejewska A. 2006. PCR detection of granulocytic Anaplasma and Babesia in Ixodes ricinus ticks and birds in west-central Poland. Ann. Agric. Environ. Med. 13: 21–23. Google Scholar

  • [52] Smetanová K., Boldiš V., Kocianová E. & Špitalská E. 2007. Detection of Ehrlichia muris in a yellow-necked mouse (Apodemus flavicollis) in Central Slovakia. Acta Virol. 51: 65–67. Google Scholar

  • [53] Smetanová K., Schwarzová K. & Kocianová, E. 2006. Detection of Anaplasma phagocytophilum, Coxiella burnetti, Rickettsia spp., and Borrelia burgdorferi s.l. in ticks, and wild-living animals in western and middle Slovakia. Ann. N. Y. Acad. Sci. 1078: 312–315. http://dx.doi.org/10.1196/annals.1374.058CrossrefGoogle Scholar

  • [54] Sphynov S., Fournier P.E., Rudakov N., Tarasevich I. & Raoult D. 2006. Detection of the members of the genera Rickettsia, Anaplasma, and Ehrlichia in ticks collected in the Asiatic part of Russia. Ann. N.Y. Acad. Sci. 1078: 378–383. http://dx.doi.org/10.1196/annals.1374.075CrossrefGoogle Scholar

  • [55] Stiller D., Kocan K.M., Edwards W., Ewing S.A. & Barron J.A. 1989. Detection of colonies of Anaplasma marginale in salivary glands of three Dermacentor spp. infected as nymphs or adults. Am. J. Vet. Res. 50: 1381–1385. Google Scholar

  • [56] Strle F. 2004. Human granulocytic ehrlichiosis in Europe. Int. J. Med. Microbiol. 293: 27–35. Google Scholar

  • [57] Stuen S. 2007. Anaplasma phagocytophilum — the most widespread tick-borne infection in animals in Europe. Vet. Res. Commun. 31: 79–84. http://dx.doi.org/10.1007/s11259-007-0071-yCrossrefGoogle Scholar

  • [58] Špitalská E. & Kocianová E. 2002. Agents of Ehrlichia phagocytophila group and other microorganisms co-infecting ticks in southwestern Slovakia. Acta Virol. 46: 49–50. Google Scholar

  • [59] Špitalská E. & Kocianová E. 2003. Tick-borne microorganisms in Southwestern Slovakia. Ann. N. Y. Acad. Sci. 990: 196–200. http://dx.doi.org/10.1111/j.1749-6632.2003.tb07362.xCrossrefGoogle Scholar

  • [60] Špitalská E., Literák I., Sparagano O.A.E., Golovchenko M. & Kocianová E. 2006. Ticks (Ixodidae) from passarine birds in the Carpathian region. Wien. Klin. Wochenschr. 118: 759–764. http://dx.doi.org/10.1007/s00508-006-0729-4CrossrefGoogle Scholar

  • [61] Štefančíková A., Derdáková M., Lenčáková D., Ivanová R., Stanko M., Čisláková L. & Peťko B. 2008. Serological and molecular detection of Borrelia bugdorferi sensu lato and Anaplasmataceae in rodents. Folia Microbiol. 53: 493–499. http://dx.doi.org/10.1007/s12223-008-0077-zCrossrefGoogle Scholar

  • [62] Štefančíková A., Derdáková M., Majláthová V., Lenčáková D., Boldižár M., Stanko M. & Peťko B. 2005. Coincidence of Borrelia burgdorferi sensu lato and Anaplasma in free-living, domestic and farm animals from eastern Slovakia, pp. 51–57. In: Venglovský J. (eds), Ecology and Veterinary Medicine VI., Proceeding, Košice. Google Scholar

  • [63] Štefanidesová K., Kocianová E., Boldiš V., Košťanová Z., Kanka P., Nemethová D. & Špitalská E. 2008. Evidence of Anaplasma phagocytophilum and Rickettsia helvetica infection in free-ranging ungulates in central Slovakia. Eur. J. Wildl. Res. 54: 519–524. DOI: 10.1007/s10344-007-0161-8 http://dx.doi.org/10.1007/s10344-007-0161-8CrossrefGoogle Scholar

  • [64] Thomas R.J., Dumler J.S. & Carlyon J.A. 2009. Current management of human granulocytic anaplasmosis, human monocytic ehrlichiosis and E. ewingii ehrlichiosis. Expert Rev. Anti. Infect. Ther. 7: 709–722. http://dx.doi.org/10.1586/eri.09.44CrossrefGoogle Scholar

  • [65] Víchová B., Majláthová V., Nováková M., Straka M. & Peťko B. 2009. First molecular detection of Anaplasma phagocytophilum in European brown bear (Ursus arctos). Vector Borne Zoonotic Dis. 10: 1–3. Google Scholar

  • [66] Zaugg J.L. 1988. Experimental anaplasmosis in mule deer: persistence of infection of Anaplasma marginale and susceptibility to A. ovis. J. Wildl. Dis. 24: 120–126. Google Scholar

  • [67] Zeman P. & Jahn P. 2009. An entropy-optimized multilocus approach for characterizing the strains of Anaplasma phagocytophilum infecting horses in the Czech Republic. J. Med. Microbiol. 58: 423–429. http://dx.doi.org/10.1099/jmm.0.007831-0CrossrefGoogle Scholar

  • [68] Zeman P. & Pecha M. 2008. Segregation of genetic variants of Anaplasma phagocytophilum circulating among wild ruminants within a Bohemian forest (Czech Republic). Int. J. Med. Microbiol. 298: 203–210. http://dx.doi.org/10.1016/j.ijmm.2008.03.003CrossrefGoogle Scholar

About the article

Published Online: 2010-10-15

Published in Print: 2010-12-01


Citation Information: Biologia, Volume 65, Issue 6, Pages 925–931, ISSN (Online) 1336-9563, ISSN (Print) 0006-3088, DOI: https://doi.org/10.2478/s11756-010-0119-2.

Export Citation

© 2010 Slovak Academy of Sciences. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

[1]
Martin O. Andersson, Conny Tolf, Paula Tamba, Mircea Stefanache, Gabriel Radbea, Dimitrios Frangoulidis, Herbert Tomaso, Jonas Waldenström, Gerhard Dobler, and Lidia Chitimia-Dobler
Parasites & Vectors, 2018, Volume 11, Number 1
[2]
Martin O. Andersson, Conny Tolf, Paula Tamba, Mircea Stefanache, Jonas Waldenström, Gerhard Dobler, and Lidia Chițimia-Dobler
Parasites & Vectors, 2017, Volume 10, Number 1
[3]
Ana J. Ribeiro, Luís Cardoso, José M. Maia, Teresa Coutinho, and Mário Cotovio
Parasitology Research, 2013, Volume 112, Number 7, Page 2611

Comments (0)

Please log in or register to comment.
Log in