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Parasites & vectors2020; 13(1); 261; doi: 10.1186/s13071-020-04131-0

Equid infective Theileria cluster in distinct 18S rRNA gene clades comprising multiple taxa with unusually broad mammalian host ranges.

Abstract: Equine theileriosis, a tick-transmitted disease caused by the hemoprotozoan parasites Theileria equi and Theileria haneyi, affects equids throughout tropical and subtropical regions of the world. It is a significant regulatory concern in non-endemic countries, where testing for equine theileriosis is required prior to horse import to prevent parasite entry. Within endemic areas, infection causes significant morbidity and mortality, leading to economic losses. No vaccine for equine theileriosis is available, and current drug treatment protocols are inconsistent and associated with significant side effects. Recent work has revealed substantial genetic variability among equine theileriosis organisms, and analysis of ribosomal DNA from affected animals around the world indicates that the organisms can be grouped into five distinct clades. As these diverse parasites are capable of infecting a wide range of both tick and mammalian hosts, movement of different equine Theileria species between endemic countries, and eventually into non-endemic countries, is a significant concern. Furthermore, the substantial genetic variability of these organisms will likely render currently utilized importation diagnostic tests unable to detect all equine Theileria spp. To this end, more complete characterization of these diverse parasites is critical to the continued global control of equine theileriosis. This review discusses current knowledge of equine Theileria spp. in this context, and highlights new opportunities and challenges for workers in this field.
Publication Date: 2020-05-19 PubMed ID: 32430015PubMed Central: PMC7236219DOI: 10.1186/s13071-020-04131-0Google Scholar: Lookup
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  • Journal Article
  • Review

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research article investigates the genetic variability of the parasites causing equine theileriosis, a disease affecting horses, which has severe economic impact in endemic areas and regulatory implications in non-endemic countries. The researchers discovered five distinct genetic groupings of these parasites, which have a broad host range in ticks and mammals, raising concerns about the disease’s global control.

Background

  • In the study, the researchers sought to provide a deeper understanding of equine theileriosis, a disease that significantly impacts horses in tropical and subtropical regions worldwide. This illness is caused by Theileria equi and Theileria haneyi, tiny parasites transmitted by ticks.
  • Equine theileriosis is not only a veterinary health issue, but it also carries major economic implications. In endemic areas—where the disease is regularly found—it can result in high mortality rates and severe illness, both of which lead to significant economic losses. In non-endemic regions—where the illness is not usually found—there are stringent regulatory restrictions around horse imports to prevent the introduction of the parasites.

Findings

  • The research illuminates the considerable genetic diversity amongst Theileria parasites. Analysis of ribosomal DNA of affected horses worldwide enabled the categorization of these organisms into five distinct genetic clades or groups.
  • This genetic diversity underscores the adaptability of these parasites, which can infect a wide range of ticks and mammals. This versatility also highlights the risk of equine Theileria species spreading from endemic to non-endemic countries.
  • A major issue arises because the genetic variability among these parasites could undermine the current importation diagnostic tests. This means that some species of equine Theileria might not be detected during import procedures.

Implications

  • This study contributes to the body of knowledge surrounding equine Theileria and the disease it causes. The identified genetic diversity and its implications outline the complexity of controlling this disease globally.
  • The discovery of significant genetic diversity could also mean that the development or modification of diagnostic tests and vaccines may have to consider these differences. The robustness of containment strategies and import-level screening procedures could be recalibrated with the insights gained from the study.
  • Finally, the research presents both new challenges and opportunities, as it necessitates novel approaches to manage the disease effectively and mitigates its impact on global horse populations.

Cite This Article

APA
Bishop RP, Kappmeyer LS, Onzere CK, Odongo DO, Githaka N, Sears KP, Knowles DP, Fry LM. (2020). Equid infective Theileria cluster in distinct 18S rRNA gene clades comprising multiple taxa with unusually broad mammalian host ranges. Parasit Vectors, 13(1), 261. https://doi.org/10.1186/s13071-020-04131-0

Publication

ISSN: 1756-3305
NlmUniqueID: 101462774
Country: England
Language: English
Volume: 13
Issue: 1
Pages: 261
PII: 261

Researcher Affiliations

Bishop, Richard P
  • Department of Veterinary Microbiology and Pathology, Washington State University, P.O. Box 647040, Pullman, Washington, 99164, USA.
Kappmeyer, Lowell S
  • Animal Disease Research Unit, Agricultural Research Service, US Department of Agriculture, P.O. Box 646630, Pullman, WA, 99164, USA.
Onzere, Cynthia K
  • Department of Veterinary Microbiology and Pathology, Washington State University, P.O. Box 647040, Pullman, Washington, 99164, USA.
Odongo, David O
  • Biosciences Eastern and Central Africa-International Livestock Research Institute (BecA-ILRI) Hub, P.O. Box 30709, Nairobi, 00100, Kenya.
  • School of Biological Sciences, University of Nairobi, P.O. Box 30197, Nairobi, 00100, Kenya.
Githaka, Naftaly
  • Biosciences Eastern and Central Africa-International Livestock Research Institute (BecA-ILRI) Hub, P.O. Box 30709, Nairobi, 00100, Kenya.
Sears, Kelly P
  • Department of Veterinary Microbiology and Pathology, Washington State University, P.O. Box 647040, Pullman, Washington, 99164, USA.
Knowles, Donald P
  • Department of Veterinary Microbiology and Pathology, Washington State University, P.O. Box 647040, Pullman, Washington, 99164, USA.
Fry, Lindsay M
  • Department of Veterinary Microbiology and Pathology, Washington State University, P.O. Box 647040, Pullman, Washington, 99164, USA. Lindsay.Fry@usda.gov.
  • Animal Disease Research Unit, Agricultural Research Service, US Department of Agriculture, P.O. Box 646630, Pullman, WA, 99164, USA. Lindsay.Fry@usda.gov.

MeSH Terms

  • Animals
  • Genetic Variation
  • Horse Diseases / parasitology
  • Horses
  • Host Specificity
  • Mammals / parasitology
  • Phylogeny
  • RNA, Ribosomal, 18S / genetics
  • Theileria / classification
  • Theileriasis / parasitology

Grant Funding

  • 2090-320000-034-00D / Agricultural Research Service

Conflict of Interest Statement

The authors declare that they have no competing interests.

References

This article includes 57 references
  1. Wise LN, Kappmeyer LS, Mealey RH, Knowles DP. Review of equine piroplasmosis.. J Vet Intern Med 2013 Nov-Dec;27(6):1334-46.
    pubmed: 24033559doi: 10.1111/jvim.12168google scholar: lookup
  2. Scoles GA, Ueti MW. Vector ecology of equine piroplasmosis.. Annu Rev Entomol 2015 Jan 7;60:561-80.
  3. Rothschild CM. Equine piroplasmosis.. J Equine Vet Sci 2013;33:497–508.
  4. Levine N. Phylum II. Apicomplexa Levine, 1970.. In: Lee JJ, Hutner SH, Bovie EC, editors. An illustrated guide to the protozoa. Lawrence: Society for Protozoologists; 1985. pp. 322–374.
  5. Escalante AA, Ayala FJ. Evolutionary origin of Plasmodium and other Apicomplexa based on rRNA genes.. Proc Natl Acad Sci U S A 1995 Jun 20;92(13):5793-7.
    pmc: PMC41587pubmed: 7597031doi: 10.1073/pnas.92.13.5793google scholar: lookup
  6. Sam-Yellowe TY. Rhoptry organelles of the apicomplexa: Their role in host cell invasion and intracellular survival.. Parasitol Today 1996 Aug;12(8):308-16.
    pubmed: 15275182doi: 10.1016/0169-4758(96)10030-2google scholar: lookup
  7. Shaw MK. Cell invasion by Theileria sporozoites.. Trends Parasitol 2003 Jan;19(1):2-6.
    pubmed: 12488213doi: 10.1016/s1471-4922(02)00015-6google scholar: lookup
  8. Kemp LE, Yamamoto M, Soldati-Favre D. Subversion of host cellular functions by the apicomplexan parasites.. FEMS Microbiol Rev 2013 Jul;37(4):607-31.
    pubmed: 23186105doi: 10.1111/1574-6976.12013google scholar: lookup
  9. Carruthers VB, Sibley LD. Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts.. Eur J Cell Biol 1997 Jun;73(2):114-23.
    pubmed: 9208224
  10. Fry LM, Schneider DA, Frevert CW, Nelson DD, Morrison WI, Knowles DP. East Coast Fever Caused by Theileria parva Is Characterized by Macrophage Activation Associated with Vasculitis and Respiratory Failure.. PLoS One 2016;11(5):e0156004.
  11. Tretina K, Gotia HT, Mann DJ, Silva JC. Theileria-transformed bovine leukocytes have cancer hallmarks.. Trends Parasitol 2015 Jul;31(7):306-14.
    pubmed: 25951781doi: 10.1016/j.pt.2015.04.001google scholar: lookup
  12. Knowles DP, Kappmeyer LS, Haney D, Herndon DR, Fry LM, Munro JB, Sears K, Ueti MW, Wise LN, Silva M, Schneider DA, Grause J, White SN, Tretina K, Bishop RP, Odongo DO, Pelzel-McCluskey AM, Scoles GA, Mealey RH, Silva JC. Discovery of a novel species, Theileria haneyi n. sp., infective to equids, highlights exceptional genomic diversity within the genus Theileria: implications for apicomplexan parasite surveillance.. Int J Parasitol 2018 Aug;48(9-10):679-690.
    pubmed: 29885436doi: 10.1016/j.ijpara.2018.03.010google scholar: lookup
  13. Sivakumar T, Hayashida K, Sugimoto C, Yokoyama N. Evolution and genetic diversity of Theileria.. Infect Genet Evol 2014 Oct;27:250-63.
    pubmed: 25102031doi: 10.1016/j.meegid.2014.07.013google scholar: lookup
  14. Schein E, Rehbein G, Voigt WP, Zweygarth E. Babesia equi (Laveran 1901) 1. Development in horses and in lymphocyte culture.. Tropenmed Parasitol 1981 Dec;32(4):223-7.
    pubmed: 7345686
  15. Moltmann UG, Mehlhorn H, Schein E, Rehbein G, Voigt WP, Zweygarth E. Fine structure of Babesia equi Laveran, 1901 within lymphocytes and erythrocytes of horses: an in vivo and in vitro study.. J Parasitol 1983 Feb;69(1):111-20.
    pubmed: 6827432
  16. Mekata H, Minamino T, Mikurino Y, Yamamoto M, Yoshida A, Nonaka N, Horii Y. Evaluation of the natural vertical transmission of Theileria orientalis.. Vet Parasitol 2018 Nov 15;263:1-4.
    pubmed: 30389017doi: 10.1016/j.vetpar.2018.09.017google scholar: lookup
  17. Sant C, d'Abadie R, Pargass I, Basu AK, Asgarali Z, Charles RA, Georges KC. Prospective study investigating transplacental transmission of equine piroplasmosis in thoroughbred foals in Trinidad.. Vet Parasitol 2016 Aug 15;226:132-7.
    pubmed: 27514898doi: 10.1016/j.vetpar.2016.07.008google scholar: lookup
  18. Hammer JF, Jenkins C, Bogema D, Emery D. Mechanical transfer of Theileria orientalis: possible roles of biting arthropods, colostrum and husbandry practices in disease transmission.. Parasit Vectors 2016 Jan 22;9:34.
    pmc: PMC4722681pubmed: 26793977doi: 10.1186/s13071-016-1323-xgoogle scholar: lookup
  19. Yona S, Kim KW, Wolf Y, Mildner A, Varol D, Breker M, Strauss-Ayali D, Viukov S, Guilliams M, Misharin A, Hume DA, Perlman H, Malissen B, Zelzer E, Jung S. Fate mapping reveals origins and dynamics of monocytes and tissue macrophages under homeostasis.. Immunity 2013 Jan 24;38(1):79-91.
  20. Gerstenberg C, Allen W, Phipps L. Mechanical transmission of Babesia equi infection in a British herd of horses.. In: Proceedings of the 8th International Conference of Equine Infectious Diseases, 23–26 March, Dubai, UAE; 1998.
  21. Kappmeyer LS, Thiagarajan M, Herndon DR, Ramsay JD, Caler E, Djikeng A, Gillespie JJ, Lau AO, Roalson EH, Silva JC, Silva MG, Suarez CE, Ueti MW, Nene VM, Mealey RH, Knowles DP, Brayton KA. Comparative genomic analysis and phylogenetic position of Theileria equi.. BMC Genomics 2012 Nov 9;13:603.
    pmc: PMC3505731pubmed: 23137308doi: 10.1186/1471-2164-13-603google scholar: lookup
  22. Ramsay JD, Ueti MW, Johnson WC, Scoles GA, Knowles DP, Mealey RH. Lymphocytes and macrophages are infected by Theileria equi, but T cells and B cells are not required to establish infection in vivo.. PLoS One 2013;8(10):e76996.
  23. Mehlhorn H, Schein E. Redescription of Babesia equi Laveran, 1901 as Theileria equi Mehlhorn, Schein 1998.. Parasitol Res 1998 Jun;84(6):467-75.
    pubmed: 9660136doi: 10.1007/s004360050431google scholar: lookup
  24. McKeever DJ, Taracha EL, Innes EL, MacHugh ND, Awino E, Goddeeris BM, Morrison WI. Adoptive transfer of immunity to Theileria parva in the CD8+ fraction of responding efferent lymph.. Proc Natl Acad Sci U S A 1994 Mar 1;91(5):1959-63.
    pmc: PMC43284pubmed: 8127915doi: 10.1073/pnas.91.5.1959google scholar: lookup
  25. Musoke AJ, Nantulya VM, Buscher G, Masake RA, Otim B. Bovine immune response to Theileria parva: neutralizing antibodies to sporozoites.. Immunology 1982 Apr;45(4):663-8.
    pmc: PMC1555427pubmed: 6802745
  26. Beck R, Vojta L, Mrljak V, Marinculić A, Beck A, Zivicnjak T, Cacciò SM. Diversity of Babesia and Theileria species in symptomatic and asymptomatic dogs in Croatia.. Int J Parasitol 2009 Jun;39(7):843-8.
    pubmed: 19367832doi: 10.1016/j.ijpara.2008.12.005google scholar: lookup
  27. Rosa CT, Pazzi P, Nagel S, McClure V, Christie J, Troskie M, Dvir E. Theileriosis in six dogs in South Africa and its potential clinical significance.. J S Afr Vet Assoc 2014 Aug 20;85(1):1114.
    pubmed: 25685903doi: 10.4102/jsava.v85i1.1114google scholar: lookup
  28. Qablan MA, Sloboda M, Jirků M, Oborník M, Dwairi S, Amr ZS, Hořín P, Lukeš J, Modrý D. Quest for the piroplasms in camels: identification of Theileria equi and Babesia caballi in Jordanian dromedaries by PCR.. Vet Parasitol 2012 May 25;186(3-4):456-60.
    pubmed: 22186193doi: 10.1016/j.vetpar.2011.11.070google scholar: lookup
  29. Da Silveira AW, De Oliveira GG, Menezes Santos L, da Silva Azuaga LB, Macedo Coutinho CR, Echeverria JT, Antunes TR, do Nascimento Ramos CA, Izabel de Souza A. Natural Infection of the South American Tapir ( Tapirus terrestris ) by Theileria equi.. J Wildl Dis 2017 Apr;53(2):411-413.
    pubmed: 28151085doi: 10.7589/2016-06-149google scholar: lookup
  30. Zhang J, Kelly P, Li J, Xu C, Wang C. Molecular Detection of Theileria spp. in Livestock on Five Caribbean Islands.. Biomed Res Int 2015;2015:624728.
    pmc: PMC4689888pubmed: 26783522doi: 10.1155/2015/624728google scholar: lookup
  31. Azmi K, Al-Jawabreh A, Abdeen Z. Molecular Detection of Theileria ovis and Theleiria equi in Livestock from Palestine.. Sci Rep 2019 Aug 9;9(1):11557.
    pmc: PMC6688999pubmed: 31399617doi: 10.1038/s41598-019-47965-0google scholar: lookup
  32. Bishop R, Musoke A, Morzaria S, Gardner M, Nene V. Theileria: intracellular protozoan parasites of wild and domestic ruminants transmitted by ixodid ticks.. Parasitology 2004;129 Suppl:S271-83.
    pubmed: 15938515doi: 10.1017/s0031182003004748google scholar: lookup
  33. Wise LN, Kappmeyer LS, Knowles DP, White SN. Evolution and diversity of the EMA families of the divergent equid parasites, Theileria equi and T. haneyi.. Infect Genet Evol 2019 Mar;68:153-160.
    pubmed: 30576837doi: 10.1016/j.meegid.2018.12.020google scholar: lookup
  34. Pain A, Renauld H, Berriman M, Murphy L, Yeats CA, Weir W, Kerhornou A, Aslett M, Bishop R, Bouchier C, Cochet M, Coulson RM, Cronin A, de Villiers EP, Fraser A, Fosker N, Gardner M, Goble A, Griffiths-Jones S, Harris DE, Katzer F, Larke N, Lord A, Maser P, McKellar S, Mooney P, Morton F, Nene V, O'Neil S, Price C, Quail MA, Rabbinowitsch E, Rawlings ND, Rutter S, Saunders D, Seeger K, Shah T, Squares R, Squares S, Tivey A, Walker AR, Woodward J, Dobbelaere DA, Langsley G, Rajandream MA, McKeever D, Shiels B, Tait A, Barrell B, Hall N. Genome of the host-cell transforming parasite Theileria annulata compared with T. parva.. Science 2005 Jul 1;309(5731):131-3.
    pubmed: 15994557doi: 10.1126/science.1110418google scholar: lookup
  35. El-Sayed SAE, Rizk MA, Terkawi MA, Mousa A, Elsayed G, Fouda M. Cocktail of Theileria equi antigens for detecting infection in equines.. Asian Pac J Trop Biomed 2015;5:977–981.
  36. Silva MG, Graça T, Suarez CE, Knowles DP. Repertoire of Theileria equi immunodominant antigens bound by equine antibody.. Mol Biochem Parasitol 2013 Apr;188(2):109-15.
  37. Zhuang W, Sugimoto C, Matsuba T, Niinuma S, Murata M, Onuma M. Analyses of antigenic and genetic diversities of Theileria sergenti piroplasm surface proteins.. J Vet Med Sci 1994 Jun;56(3):469-73.
    pubmed: 7948375doi: 10.1292/jvms.56.469google scholar: lookup
  38. Onuma M, Kakuda T, Sugimoto C. Theileria parasite infection in East Asia and control of the disease.. Comp Immunol Microbiol Infect Dis 1998 Jul;21(3):165-77.
    pubmed: 9681240doi: 10.1016/s0147-9571(98)00008-3google scholar: lookup
  39. Jenkins C, Bogema DR. Factors associated with seroconversion to the major piroplasm surface protein of the bovine haemoparasite Theileria orientalis.. Parasit Vectors 2016 Feb 25;9:106.
    pmc: PMC4766684pubmed: 26912048doi: 10.1186/s13071-016-1395-7google scholar: lookup
  40. Schein E. Equine babesiosis.. In: Ristic M, editor. Babesiosis of domestic animals and man. Boca Raton: CRC Press; 1988. pp. 197–208.
  41. Friedhoff KT, Tenter AM, Müller I. Haemoparasites of equines: impact on international trade of horses.. Rev Sci Tech 1990 Dec;9(4):1187-94.
    pubmed: 2132711
  42. Bhoora RV, Collins NE, Schnittger L, Troskie C, Marumo R, Labuschagne K, Smith RM, Dalton DL, Mbizeni S. Molecular genotyping and epidemiology of equine piroplasmids in South Africa.. Ticks Tick Borne Dis 2020 Mar;11(2):101358.
    pubmed: 31870636doi: 10.1016/j.ttbdis.2019.101358google scholar: lookup
  43. Peckle M, Pires MS, Silva CBD, Costa RLD, Vitari GLV, Senra MVX, Dias RJP, Santos HA, Massard CL. Molecular characterization of Theileria equi in horses from the state of Rio de Janeiro, Brazil.. Ticks Tick Borne Dis 2018 Feb;9(2):349-353.
    pubmed: 29223587doi: 10.1016/j.ttbdis.2017.11.011google scholar: lookup
  44. Bhoora R, Buss P, Guthrie AJ, Penzhorn BL, Collins NE. Genetic diversity of piroplasms in plains zebra (Equus quagga burchellii) and Cape mountain zebra (Equus zebra zebra) in South Africa.. Vet Parasitol 2010 Nov 24;174(1-2):145-9.
    pubmed: 20833476doi: 10.1016/j.vetpar.2010.08.014google scholar: lookup
  45. Salim B, Bakheit MA, Kamau J, Nakamura I, Sugimoto C. Nucleotide sequence heterogeneity in the small subunit ribosomal RNA gene within Theileria equi from horses in Sudan.. Parasitol Res 2010 Jan;106(2):493-8.
    pubmed: 19953269doi: 10.1007/s00436-009-1691-7google scholar: lookup
  46. Sears KP, Kappmeyer LS, Wise LN, Silva M, Ueti MW, White S, Reif KE, Knowles DP. Infection dynamics of Theileria equi and Theileria haneyi, a newly discovered apicomplexan of the horse.. Vet Parasitol 2019 Jul;271:68-75.
    pubmed: 31303207doi: 10.1016/j.vetpar.2019.06.009google scholar: lookup
  47. Coultous RM, Phipps P, Dalley C, Lewis J, Hammond TA, Shiels BR, Weir W, Sutton DGM. Equine piroplasmosis status in the UK: an assessment of laboratory diagnostic submissions and techniques.. Vet Rec 2019 Jan 19;184(3):95.
    pubmed: 30413675doi: 10.1136/vr.104855google scholar: lookup
  48. Orlando L, Ginolhac A, Zhang G, Froese D, Albrechtsen A, Stiller M, Schubert M, Cappellini E, Petersen B, Moltke I, Johnson PL, Fumagalli M, Vilstrup JT, Raghavan M, Korneliussen T, Malaspinas AS, Vogt J, Szklarczyk D, Kelstrup CD, Vinther J, Dolocan A, Stenderup J, Velazquez AM, Cahill J, Rasmussen M, Wang X, Min J, Zazula GD, Seguin-Orlando A, Mortensen C, Magnussen K, Thompson JF, Weinstock J, Gregersen K, Røed KH, Eisenmann V, Rubin CJ, Miller DC, Antczak DF, Bertelsen MF, Brunak S, Al-Rasheid KA, Ryder O, Andersson L, Mundy J, Krogh A, Gilbert MT, Kjær K, Sicheritz-Ponten T, Jensen LJ, Olsen JV, Hofreiter M, Nielsen R, Shapiro B, Wang J, Willerslev E. Recalibrating Equus evolution using the genome sequence of an early Middle Pleistocene horse.. Nature 2013 Jul 4;499(7456):74-8.
    pubmed: 23803765doi: 10.1038/nature12323google scholar: lookup
  49. Githaka N, Konnai S, Bishop R, Odongo D, Lekolool I, Kariuki E, Gakuya F, Kamau L, Isezaki M, Murata S, Ohashi K. Identification and sequence characterization of novel Theileria genotypes from the waterbuck (Kobus defassa) in a Theileria parva-endemic area in Kenya.. Vet Parasitol 2014 May 28;202(3-4):180-93.
    pubmed: 24690249doi: 10.1016/j.vetpar.2014.02.056google scholar: lookup
  50. Uilenberg G, Gray J, Kahl O. Research on Piroplasmorida and other tick-borne agents: Are we going the right way?. Ticks Tick Borne Dis 2018 May;9(4):860-863.
    pubmed: 29567148doi: 10.1016/j.ttbdis.2018.03.005google scholar: lookup
  51. Smith RM, Bhoora RV, Kotzé A, Grobler JP, Lee Dalton D. Translocation a potential corridor for equine piroplasms in Cape mountain zebra (Equus zebra zebra).. Int J Parasitol Parasites Wildl 2019 Aug;9:130-133.
  52. Hawkins E, Kock R, McKeever D, Gakuya F, Musyoki C, Chege SM, Mutinda M, Kariuki E, Davidson Z, Low B, Skilton RA, Njahira MN, Wamalwa M, Maina E. Prevalence of Theileria equi and Babesia caballi as well as the identification of associated ticks in sympatric Grevy's zebras (Equus grevyi) and donkeys (Equus africanus asinus) in northern Kenya.. J Wildl Dis 2015 Jan;51(1):137-47.
    pubmed: 25380362doi: 10.7589/2013-11-316google scholar: lookup
  53. Woolhouse ME, Thumbi SM, Jennings A, Chase-Topping M, Callaby R, Kiara H, Oosthuizen MC, Mbole-Kariuki MN, Conradie I, Handel IG, Poole EJ, Njiiri E, Collins NE, Murray G, Tapio M, Auguet OT, Weir W, Morrison WI, Kruuk LE, Bronsvoort BM, Hanotte O, Coetzer K, Toye PG. Co-infections determine patterns of mortality in a population exposed to parasite infection.. Sci Adv 2015 Mar;1(2):e1400026.
    pmc: PMC4643819pubmed: 26601143doi: 10.1126/sciadv.1400026google scholar: lookup
  54. Stone NE, Olafson PU, Davey RB, Buckmeier G, Bodine D, Sidak-Loftis LC, Giles JR, Duhaime R, Miller RJ, Mosqueda J, Scoles GA, Wagner DM, Busch JD. Multiple mutations in the para-sodium channel gene are associated with pyrethroid resistance in Rhipicephalus microplus from the United States and Mexico.. Parasit Vectors 2014 Oct 1;7:456.
    pmc: PMC4189684pubmed: 25266983doi: 10.1186/s13071-014-0456-zgoogle scholar: lookup
  55. Eiden AL, Kaufman PE, Oi FM, Allan SA, Miller RJ. Detection of Permethrin Resistance and Fipronil Tolerance in Rhipicephalus sanguineus (Acari: Ixodidae) in the United States.. J Med Entomol 2015 May;52(3):429-36.
    pubmed: 26334817doi: 10.1093/jme/tjv005google scholar: lookup
  56. Aenishaenslin C, Michel P, Ravel A, Gern L, Waaub JP, Milord F, Bélanger D. Acceptability of tick control interventions to prevent Lyme disease in Switzerland and Canada: a mixed-method study.. BMC Public Health 2016 Jan 5;16:12.
    pmc: PMC4700560pubmed: 26733007doi: 10.1186/s12889-015-2629-xgoogle scholar: lookup
  57. Adalja A, Sell TK, McGinty M, Boddie C. Genetically Modified (GM) Mosquito Use to Reduce Mosquito-Transmitted Disease in the US: A Community Opinion Survey.. PLoS Curr 2016 May 25;8.

Citations

This article has been cited 15 times.
  1. Moudgil P, Grakh K, Kumar R, Sharma M, Gupta R, Jindal N. First Molecular Confirmed Outbreak of Malignant Ovine Theileriosis in Sheep from North India. Acta Parasitol 2023 Sep;68(3):527-534.
    doi: 10.1007/s11686-023-00684-zpubmed: 37328625google scholar: lookup
  2. Wang BH, Du LF, Zhang MZ, Xia LY, Li C, Lin ZT, Wang N, Gao WY, Ye RZ, Liu JY, Han XY, Shi WQ, Shi XY, Jiang JF, Jia N, Cui XM, Zhao L, Cao WC. Genomic Characterization of Theileria luwenshuni Strain Cheeloo. Microbiol Spectr 2023 Aug 17;11(4):e0030123.
    doi: 10.1128/spectrum.00301-23pubmed: 37260375google scholar: lookup
  3. Onzere CK, Hulbert M, Sears KP, Williams LBA, Fry LM. Tulathromycin and Diclazuril Lack Efficacy against Theileria haneyi, but Tulathromycin Is Not Associated with Adverse Clinical Effects in Six Treated Adult Horses. Pathogens 2023 Mar 14;12(3).
    doi: 10.3390/pathogens12030453pubmed: 36986375google scholar: lookup
  4. Mongruel ACB, Medici EP, da Costa Canena A, Calchi AC, Perles L, Rodrigues BCB, Soares JF, Machado RZ, André MR. Theileria terrestris nov. sp.: A Novel Theileria in Lowland Tapirs (Tapirus terrestris) from Two Different Biomes in Brazil. Microorganisms 2022 Nov 23;10(12).
  5. Coultous R, Gotić J, McCann M, Sutton D, Beck R, Shiels B. Novel equi merozoite antigen (ema-1) gene heterogeneity in a geographically isolated Theileria equi population in Croatia. Parasit Vectors 2022 Oct 31;15(1):401.
    doi: 10.1186/s13071-022-05484-4pubmed: 36316753google scholar: lookup
  6. Schnittger L, Ganzinelli S, Bhoora R, Omondi D, Nijhof AM, Florin-Christensen M. The Piroplasmida Babesia, Cytauxzoon, and Theileria in farm and companion animals: species compilation, molecular phylogeny, and evolutionary insights. Parasitol Res 2022 May;121(5):1207-1245.
    doi: 10.1007/s00436-022-07424-8pubmed: 35098377google scholar: lookup
  7. Elsawy BSM, Nassar AM, Alzan HF, Bhoora RV, Ozubek S, Mahmoud MS, Kandil OM, Mahdy OA. Rapid Detection of Equine Piroplasms Using Multiplex PCR and First Genetic Characterization of Theileria haneyi in Egypt. Pathogens 2021 Oct 31;10(11).
    doi: 10.3390/pathogens10111414pubmed: 34832570google scholar: lookup
  8. Idoko IS, Edeh RE, Adamu AM, Machunga-Mambula S, Okubanjo OO, Balogun EO, Adamu S, Johnson W, Kappmeyer L, Mousel M, Ueti MW. Molecular and Serological Detection of Piroplasms in Horses from Nigeria. Pathogens 2021 Apr 23;10(5).
    doi: 10.3390/pathogens10050508pubmed: 33922468google scholar: lookup
  9. Bastos RG, Sears KP, Dinkel KD, Kappmeyer L, Ueti MW, Knowles DP, Fry LM. Development of an Indirect ELISA to Detect Equine Antibodies to Theileria haneyi. Pathogens 2021 Feb 27;10(3).
    doi: 10.3390/pathogens10030270pubmed: 33673478google scholar: lookup
  10. Sears K, Knowles D, Dinkel K, Mshelia PW, Onzere C, Silva M, Fry L. Imidocarb Dipropionate Lacks Efficacy against Theileria haneyi and Fails to Consistently Clear Theileria equi in Horses Co-Infected with T. haneyi. Pathogens 2020 Dec 10;9(12).
    doi: 10.3390/pathogens9121035pubmed: 33321715google scholar: lookup
  11. Tirosh-Levy S, Gottlieb Y, Fry LM, Knowles DP, Steinman A. Twenty Years of Equine Piroplasmosis Research: Global Distribution, Molecular Diagnosis, and Phylogeny. Pathogens 2020 Nov 8;9(11).
    doi: 10.3390/pathogens9110926pubmed: 33171698google scholar: lookup
  12. Benitez-Ibalo AP, Debárbora VN, Mangold AJ, Nava S, Sebastian PS. Molecular genotyping of Theileria spp. detected in horses from Corrientes City, Argentina. Vet Res Commun 2024 Dec 24;49(1):54.
    doi: 10.1007/s11259-024-10618-3pubmed: 39718660google scholar: lookup
  13. Mendoza FJ, Pérez-Écija A, Kappmeyer LS, Suarez CE, Bastos RG. New insights in the diagnosis and treatment of equine piroplasmosis: pitfalls, idiosyncrasies, and myths. Front Vet Sci 2024;11:1459989.
    doi: 10.3389/fvets.2024.1459989pubmed: 39205808google scholar: lookup
  14. Zhou B, Yang G, Hu Z, Chen K, Guo W, Wang X, Du C. Development of a Real-Time Quantitative PCR Based on a TaqMan-MGB Probe for the Rapid Detection of Theileria haneyi. Microorganisms 2023 Oct 26;11(11).
  15. Wondim M, Dunaj-Małyszko J, Okrzeja J, Majewski P, Czupryna P, Pancewicz S, Moniuszko-Malinowska A. Detection of Babesia and Theileria species in ticks from North-Eastern Poland. J Travel Med 2023 Jun 23;30(4).
    doi: 10.1093/jtm/taad071pubmed: 37220879google scholar: lookup