Jump to ContentJump to Main Navigation

Biologia

12 Issues per year


IMPACT FACTOR increased in 2013: 0.696
5-year IMPACT FACTOR: 0.751

SCImago Journal Rank (SJR): 0.306
Source Normalized Impact per Paper (SNIP): 0.555

VolumeIssuePage

Issues

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

1Slovak Academy of Sciences

© 2010 Versita Warsaw. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. (CC BY-NC-ND 3.0)

Citation Information: Biologia. Volume 65, Issue 6, Pages 925–931, ISSN (Online) 1336-9563, ISSN (Print) 0006-3088, DOI: 10.2478/s11756-010-0119-2, October 2010

Publication History

Published Online:
2010-10-15

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.

  • [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. [CrossRef]

  • [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/S0950268899003684 [CrossRef]

  • [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.39.12.4591-4592.2001 [CrossRef]

  • [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.

  • [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.00809-06 [CrossRef]

  • [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.x [CrossRef]

  • [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.2003.08.011 [CrossRef]

  • [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.2006.6.404 [CrossRef]

  • [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/eid1512.090178 [CrossRef]

  • [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.

  • [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.x [CrossRef]

  • [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/NEJM199907153410303 [CrossRef]

  • [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.

  • [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.2003.10.012 [CrossRef]

  • [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.

  • [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.2005.5.390 [CrossRef]

  • [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.

  • [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.

  • [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. [CrossRef]

  • [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.2001.62.1599 [CrossRef]

  • [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. [CrossRef]

  • [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.x [CrossRef]

  • [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.0.63260-0 [CrossRef]

  • [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.

  • [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/S0031182003004700 [CrossRef]

  • [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/s11756-008-0007-1 [CrossRef]

  • [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-y [CrossRef]

  • [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.

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

  • [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/10.1089/15303660260613693 [CrossRef]

  • [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.

  • [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.

  • [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.40.3.892-897.2002 [CrossRef]

  • [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. [CrossRef]

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

  • [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/NEJM198704023161406 [CrossRef]

  • [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.74.2.1373-1375.2006 [CrossRef]

  • [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. [CrossRef]

  • [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.

  • [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. [CrossRef]

  • [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.

  • [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.

  • [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.

  • [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.42.5.2285-2286.2004 [CrossRef]

  • [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.

  • [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.

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

  • [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.

  • [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;2

  • [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.

  • [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.

  • [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.1374.058 [CrossRef]

  • [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.1374.075 [CrossRef]

  • [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.

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

  • [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-y [CrossRef]

  • [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.

  • [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.x [CrossRef]

  • [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/s00508-006-0729-4 [CrossRef]

  • [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-z [CrossRef]

  • [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.

  • [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/s10344-007-0161-8 [CrossRef]

  • [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.09.44 [CrossRef]

  • [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.

  • [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.

  • [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.0.007831-0 [CrossRef]

  • [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.2008.03.003 [CrossRef]

Comments (0)

Please log in or register to comment.