Hostname: page-component-6bf8c574d5-rwnhh Total loading time: 0 Render date: 2025-02-15T19:05:21.313Z Has data issue: false hasContentIssue false
  • English
  • Français

What is Babesia microti?

Published online by Cambridge University Press:  17 October 2003

H. K. GOETHERT  and
S. R. TELFORD
H. K. GOETHERT
Affiliation:
Department of Immunology and Infectious Diseases, 665 Huntington Avenue, Harvard School of Public Health, Boston, Massachusetts 02115, USA
S. R. TELFORD
Affiliation:
Department of Immunology and Infectious Diseases, 665 Huntington Avenue, Harvard School of Public Health, Boston, Massachusetts 02115, USA
Get access Rights & Permissions [Opens in a new window]

Abstract

Babesia microti (Apicomplexa: Piroplasmida) has historically been considered a common parasite of Holarctic rodents. However, human babesiosis due to this species has generally been limited to the northeastern seaboard of the United States and Minnesota and Wisconsin. The absence of reports of B. microti babesiosis from sites where the agent is enzootic, such as in western Europe, remains unexplained. Previous work focusing on the 18S rDNA demonstrates little sequence diversity among samples from allopatric host populations across a wide geographical area. It may be that genetic diversity is underestimated due to sample size or the gene analysed. Accordingly, we collected blood or spleen samples from American or Eurasian animals with parasites that were morphologically consistent with B. microti, amplified the 18S rDNA and beta-tubulin gene, and conducted phylogenetic analysis. Surprisingly, what was considered to be ‘B. microti’ by microscopy appears to be a diverse species complex. We identify 3 distinct clades within this complex, including parasites from non-rodent hosts. Rodent parasites comprise 2 clades, one representing zoonotic isolates, and the other apparently maintained in microtine rodents, and therefore their morphological detection within animals from a site does not necessarily imply a risk to public health.

Keywords

Babesia microtiphylogenetic analysispiroplasmrodentbeta-tubulin
Type
Research Article
Information
Parasitology , Volume 127 , Issue 4 , October 2003 , pp. 301 - 309
Copyright
2003 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

ALLSOPP, M. T. E. P., CAVALIER-SMITH, T., DE WAAL, D. T. & ALLSOPP, B. A. (1994). Phylogeny and evolution of the piroplasms. Parasitology 108, 147–152.CrossRefGoogle Scholar
ARMSTRONG, P. M., KATAVOLOS, P., CAPORALE, D. A., SMITH, R. P., SPIELMAN, A. & TELFORD, S. R., 3rd (1998). Diversity of Babesia infecting deer ticks (Ixodes dammini). American Journal of Tropical Medicine and Hygiene 58, 739–742.CrossRefGoogle Scholar
BAJER, A., PAWELCZYK, A., BEHNKE, J. M., GILERT, F. S. & SINSKI, E. (2001). Factors affecting the compent community structure of haemoparasites in bank voles (Clethrionomys glareolus) from the Mazury Lake District region of Poland. Parasitology 122, 43–54.CrossRefGoogle Scholar
BROOKS, D. R. & HOBERG, E. P. (2000). Triage for the biosphere: the need and rationale for taxonomic inventories and phylogenetic studies of parasites. Comparative Parasitology 67, 1–25.Google Scholar
BURKOT, T. R., SCHNEIDER, B. S., PIENIAZEK, N. J., HAPP, C. M., RUTHERFORD, J. S., SLEMENDA, S. B., HOFFMEISTER, E., MAUPIN, G. O. & ZEIDNER, N. S. (2000). Babesia microti and Borrelia bissettii transmission by Ixodes spinipalpis ticks among pine voles Microtus ochrogaster in Colorado. Parasitology 121, 595–599.Google Scholar
CACCIO, S., CAMMA, C., ONUMA, M. & SEVERINI, C. (2000). The beta-tubulin gene of Babesia and Theileria parasites is an informative marker for species discrimination. International Journal for Parasitology 30, 1181–1185.CrossRefGoogle Scholar
CACCIO, S., HOMAN, W., VANDIJK, K. & POZIO, E. (1999). Genetic polymorphism at the beta-tubulin locus among human and animal isolates of Cryptosporidium parvum. FEMS Microbiology Letters 170, 173–179.CrossRefGoogle Scholar
CACCIO, S., LAROSA, G. & POZIO, E. (1997). The beta-tubulin gene of Cryptosporidium parvum. Molecular and Biochemical Parasitology 89, 307–311.Google Scholar
CAMACHO, A. T., PALLAS, E., GESTAL, J. J., GUITIAN, F. J., OLMEDA, A. S., GOETHERT, H. K. & TELFORD, S. R., 3rd (2001). Infection of dogs in north-west Spain with a Babesia microti-like agent. The Veterinary Record 149, 552–555.CrossRefGoogle Scholar
COLLINS, N. E. & ALLSOPP, B. A. (1999). Theileria parva ribosomal internal transcribed spacer sequences exhibit extensive polymorphism and mosaic evolution: application to the characterization of parasites from cattle and buffalo. Parasitology 118, 541–551.CrossRefGoogle Scholar
CONROY, C. J. & COOK, J. A. (1999). MtDNA evidence for repeated pulses of speciation within arvicoline and murid rodents. Journal of Mammalian Evolution 6, 221–245.CrossRefGoogle Scholar
CORREDOR, V. & ENEA, V. (1994). The small ribosomal subunit of RNA isoforms in Plasmodium cynomolgi. Genetics 136, 857–865.Google Scholar
DALRYMPLE, B. P. (1990). Cloning and characterization of the rRNA genes and flanking regions from Babesia bovis: use of the genes as strain discriminating probes. Molecular and Biochemical Parasitology 43, 117–124.CrossRefGoogle Scholar
DUH, D., PETROVEC, M. & AVSIC-ZUPANC, T. (2001). Diversity of Babesia infecting european sheep ticks (Ixodes ricinus). Journal of Clinical Microbiology 39, 3395–3397.CrossRefGoogle Scholar
FAHRENHOLZ, H. (1913). Ectoparasitien und Abstammungslehre. Zoologische Anzeiger 132, 254–262.Google Scholar
FAY, F. G. & RAUSCH, R. L. (1969). Parasitic organisms in the blood of arvicoline rodents in Alaska. Journal of Parasitology 55, 1258–1265.CrossRefGoogle Scholar
FOPPA, I. M., KRAUSE, P. J., SPIELMAN, A., GOETHERT, H. K., GERN, L., BRAND, B. & TELFORD, S. R., 3rd (2002). Entomologic and serologic evidence of zoonotic transmission of Babesia microti in eastern Switzerland. Emerging Infectious Diseases 8, 722–726.CrossRefGoogle Scholar
FRANCA, C. (1910). Sur la classification des piroplasmes et description des deux formes de ces parasites. Archives of the Royal Institute of Bacteriology Camara Pestana Lisbon, Portugal 3, 11.Google Scholar
GOETHERT, H. K., LUBELCYZK, C., LACOMBE, E., HOLMAN, M., RAND, P., SMITH, R. P., Jr & TELFORD, S. R., 3rdEnzootic Babesia microti in Maine. Journal of Parasitology (in the Press).
GORENFLOT, A., MOUBRI, K., PRECIGOUT, E., CARCY, B. & SCHETTERS, T. P. M. (1998). Human babesiosis. Annals of Tropical Medicine and Parasitology 92, 489–501.CrossRefGoogle Scholar
GRAY, J., VON STEDINGK, L. V., GURTELSCHMID, M. & GRANSTROM, M. (2002). Transmission studies of Babesia microti in Ixodes ricinus ticks and gerbils. Journal of Clinical Microbiology 40, 1259–1263.CrossRefGoogle Scholar
GUBBELS, M., HONG, Y., VANDERWEIDE, M., QI, B., NIJMAN, I. J., GUANGYUAN, L. & JONGEJAN, F. (2000). Molecular characterization of the Theileria buffeli/orientalis group. International Journal for Parasitology 30, 943–952.CrossRefGoogle Scholar
HAWKING, F. (1972). Entopolypoides macaci, a Babesia-like parasite in Cercopithecus monkeys. Parasitology 65, 89.CrossRefGoogle Scholar
HEALING, T. D. (1981). Infections with blood parasites in the small British rodents Apodemus sylvaticus, Clethrionomys glareolus, and Microtus agrestis. Parasitology 83, 179–189.CrossRefGoogle Scholar
HOBERG, E. P., MONSEN, K., KUTZ, S. & BLOUIN, M. (1999). Structure, biodiversity, and historical biogeography of nematode faunas in Holarctic ruminants: morphological and molecular diagnoses for Teladorsagia boreoarcticus sp.n. (Nematoda: Ostertagiinae) a dimorphic cryptic species in muskoxen (Ovibos moschatus). Journal of Parasitology 85, 910–934.Google Scholar
HUGHES, W. T. & OZ, H. S. (1995). Successful prevention and treatment of babesiosis with atovaquone. Journal of Infectious Diseases 172, 1042–1046.CrossRefGoogle Scholar
HUNFELD, K. P., LAMBERT, A., KAMPEN, H., ALBERT, S., EPE, C., BRADE, V. & TENTER, A. M. (2002). Seroprevalence of Babesia infections in humans exposed to ticks in midwestern Germany. Journal of Clinical Microbiology 40, 2431–2436.CrossRefGoogle Scholar
HUSSEIN, H. S. (1980). Ixodes trianguliceps: seasonal abundance and role in the epidemiology of Babesia microti infection in north-western England. Annals of Tropical Medicine and Parasitology 74, 531–539.CrossRefGoogle Scholar
INTERNATIONAL TRUST FOR ZOOLOGICAL NOMENCLATURE (2000). International Code of Zoological Nomenclature, 4th Edn. London, UK.
KARBOWIAK, G., STANKO, M., RYCHLIK, L., NOWAKOWSKI, W. & SIUDA, K. (1999). The new data about zoonotic reservoir of Babesia microti in small mammals in Poland. Acta Parasitologica 44, 142–144.Google Scholar
KILLICK-KENDRICK, R. (1974). Parasitic protozoa of the blood of rodents II. Hemogregarines, malaria parasites and piroplasms of rodents: an annotated check list and host index. Acta Tropica 31, 29–69.Google Scholar
KJEMTRUP, A. M., ROBINSON, T. & CONRAD, P. A. (2001). Description and epidemiology of Theileria youngi n. sp. from a northern Californian dusky-footed woodrat (Neotoma fuscipes) population. Journal of Parasitology 87, 373–378.Google Scholar
KJEMTRUP, A. M., THOMFORD, J., ROBINSON, T. & CONRAD, P. A. (2000). Phylogenetic relationships of human and wildlife piroplasm isolates in the western U.S. inferred from 18S nuclear small subunit RNA gene. Parasitology 120, 487–493.Google Scholar
KRAMPITZ, H. E. (1979). Babesia microti: morphology, distribution and host relationship in Germany. Zentralblatt fur Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene 244, 411–415.Google Scholar
LEVINE, N. D. (1971). Taxonomy of piroplasms. Transactions of the American Microscopical Society 90, 2–33.CrossRefGoogle Scholar
LEVINE, N. D. (1984). Nomenclatural Corrections and New Taxa in the Apicomplexan Protozoa. Transactions of the American Microscopical Society 103, 195–204.CrossRefGoogle Scholar
McCUTCHAN, T. F., LI, J., McCONKEY, G. A., ROGERS, M. J. & WATERS, A. P. (1995). The cytoplasmic ribosomal RNAs of Plasmodium spp. Parasitology Today 11, 134–138.CrossRefGoogle Scholar
NAGEL, S. D. & BOOTHROYD, J. C. (1988). The alpha and beta tubulins of Toxoplasma gonii are encoded by single copy genes containing multiple introns. Molecular and Biochemical Parasitology 29, 261–274.CrossRefGoogle Scholar
NICHOLAS, K. B. & NICHOLAS, H. B., Jr. (1997). GeneDoc: A tool for editing and anotating multiple sequence alignments. Distributed by the author.
OZ, H. S. & HUGHES, W. T. (1996). Acute fulminating babesiosis in hamsters infected with Babesia microti. International Journal for Parasitology 26, 667–670.CrossRefGoogle Scholar
POSADA, D. & CRANDALL, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle Scholar
RANDOLPH, S. E. (1994). Quantifying parameters in the transmission of Babesia microti by the tick Ixodes trianguliceps amongst voles (Clethrionomys gareolus). Parasitology 10, 287–295.Google Scholar
REDDY, G. R., CHAKRABARTI, D., YOWELL, C. A. & DAME, J. B. (1991). Sequence microheterogeneity of the three small subunit ribosomal RNA genes of Babesia bigemina: expression in erthrocyte culture. Nucleic Acids Research 19, 3641–3645.CrossRefGoogle Scholar
ROSE, T. M., SCHULTZ, E. R., HENIKOFF, J. G., PIETROKOVSKI, S., McCALLUM, C. M. & HENIKOFF, S. (1998). Consensus-degenerate hybrid oligonucleotide primers for amplification of distantly-related sequences. Nucleic Acids Research 26, 1628–1635.CrossRefGoogle Scholar
ROZAS, J. & ROZAS, R. (2000). DNA Sequence Polymorphism. Universitat de Barcelona, Barcelona.
SHIH, C. M., LIU, L. P., CHUNG, W. C., ONG, S. J. & WANG, C. C. (1997). Human babesiosis in Taiwan: asymptomatic infection with a Babesia microti-like organism in a Taiwanese woman. Journal of Clinical Microbiology 35, 450–454.Google Scholar
SPIELMAN, A., ETKIND, P., PIESMAN, J., RUEBUSH, T. K., Jr., JURANEK, D. D. & JACOBS, M. S. (1981). Reservoir hosts of human babesiosis on Nantucket Island Massachusetts, USA. American Journal of Tropical Medicine and Hygiene 30, 560–565.CrossRefGoogle Scholar
SWOFFORD, D. (1998). Phylogenetic Analysis using Parsimony, paup4d61.ppc.ed. Smithsonian Institution, Washington DC, 1998.
TELFORD, S. R., 3rd, GORENFLOT, A., BRASSEUR, P. & SPIELMAN, A. (1993). Babesial infections in humans and wildlife. In Parasitic Protozoa, vol. 5 (ed. Kreier, J. P.), pp. 1–47. Academic Press, San Diego, CA, USA.
TELFORD, S. R., 3rd, KORENBERG, E. I., GOETHERT, H. K., KOVALEVSKY, Y. V., GORELOVA, N. B. & SPIELMAN, A. (2002). Detection of natural foci of Babesiosis and granulocytic ehrlichiosis in Russia. Journal of Microbiology Epidemiology and Immunology 6, 21–25.Google Scholar
TELFORD, S. R., 3rd & MAGUIRE, J. H. (1999). Babesiosis. In Tropical Infectious Diseases: Principles, Pathogens, and Practice, vol. 1 (ed. Guerrant, R. L., Walker, D. H. & Weller, P. F.), pp. 767–773. Churchill Livingstone, London, UK.
TELFORD, S. R., 3rd, MATHER, T. N., ADLER, G. H. & SPIELMAN, A. (1990). Short-tailed shrews as reservoirs of the agents of Lyme disease and human babesiosis. Journal of Parasitology 76, 681–683.Google Scholar
TELFORD, S. R., 3rd & SPIELMAN, A. (1993). Reservoir competence of white-footed mice for Babesia microti. Journal of Medical Entomology 30, 223–227.CrossRefGoogle Scholar
TSUJI, M., WEI, Q., ZAMOTO, A., MORITA, C., ARAI, S., SHIOTA, T., FUJIMAGARI, M., ITAGAKI, A., FUJITA, H. & ISHIHARA, C. (2001). Human babesiosis in Japan: epizootiologic survey of rodent reservoir and isolation of new type of Babesia microti-like parasite. Journal of Clinical Microbiology 39, 4316–4322.CrossRefGoogle Scholar
TSUR, I., HADANI, A. & PIPANO, E. (1960). Nuttallia danii n. sp. a hemoprotozoan from the gerbil (Meriones tristami shawi). Refuah Veterinary 17, 234–236.Google Scholar
VAN PEENEN, P. F., CHANG, S. J., BANKNIEDER, A. R. & SANTANA, F. J. (1977). Piroplasms from Taiwanese rodents. Journal of Protozoology 24, 310–312.CrossRefGoogle Scholar
WESSELING, J. G., DIRKS, R., SMITS, M. A. & SCHOENMAKERS, J. G. G. (1989). Nucleotide sequence and expression of a beta tubulin gene from Plasmodium falciparum a malarial parasite of man. Gene 83, 301–309.CrossRefGoogle Scholar
WIDMER, G., TCHACK, L., CHAPPELL, C. L. & TZIPORI, S. (1998). Sequence polymorphism in the beta-tubulin gene reveals heterogeneous and variable population structure in Cryptosporidium parvum. Applied and Environmental Microbiology 64, 4477–4481.Google Scholar
YOUNG, A. S. (1970). Investigations on the epidemiology of blood parasites of small mammals with special reference to piroplasms. Ph.D. thesis, Univeristy of London.
ZAHLER, M., RINDER, H. & GOTHE, R. (2000 a). Genotypic status of Babesia microti within the piroplasms. Parasitology Research 86, 642–646.Google Scholar
ZAHLER, M., RINDER, H., SCHEIN, E. & GOTHE, R. (2000 b). Detection of a new pathogenic Babesia microti-like species in dogs. Veterinary Parasitology 89, 241–248.Google Scholar