FREE SHIPPING over $40
OVER 10000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Parasitology research2020; 120(1); 15-25; doi: 10.1007/s00436-020-06981-0

Hyalomma anatolicum resistance against ivermectin and fipronil is associated with indiscriminate use of acaricides in southwestern Balochistan, Pakistan.

Abstract: Ivermectin and fipronil have been used regularly to control the hard tick Hyalomma anatolicum (Acari: Ixodidae) in domestic ruminants for more than a half-decade in Balochistan, Pakistan. Inappropriate and indiscriminate use of these acaricides has resulted in the development of resistances in tick species. In this work, acaricides (ivermectin and fipronil) resistance was evaluated in H. anatolicum through in vitro and in vivo bioassays in a horse farm of Quetta, Balochistan province, Pakistan. A participatory epidemiological survey was conducted to assess potential risk factors associated with the development of acaricide resistance in H. anatolicum. The results of the epidemiological survey revealed that the horse keepers did not follow the manufacturer's instructions for the use of acaricides and applied indiscriminate doses of acaricides. The results of in vitro bioassays (adult immersion test and larval immersion test) showed that fipronil and ivermectin have protective efficacy against H. anatolicum. The results of in vivo bioassay (adult-tick mortality assay) revealed that fipronil had a higher efficacy (78.16%) than ivermectin (49.94%). More than 80% of tick mortality was not achieved in any bioassays, even for the highest acaricide concentration (100 ppm), which suggests the development of acaricide resistance against fipronil and ivermectin. This study highlights the urgency to implement a country-wide awareness about resistance monitoring and effective tick control. Graphical abstract.
Get Full Text
Publication Date: 2020-11-22 PubMed ID: 33225403PubMed Central: 3875883DOI: 10.1007/s00436-020-06981-0Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article

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.

The research article investigates the development of resistance in the hard tick species, Hyalomma anatolicum, to commonly used acaricides, ivermectin and fipronil, in Balochistan, Pakistan due to indiscriminate and inappropriate use. The study confirms the resistance and calls for country-wide awareness and effective control.

Objective and Methodology

  • The study aimed to assess the degree of resistance developed by the tick species, Hyalomma anatolicum, against ivermectin and fipronil in Balochistan, Pakistan. The abnormal use of these acaricides over the years has led to this resistance.
  • The resistance was evaluated through in vitro (inside a test tube, culture dish, or elsewhere outside a living organism) and in vivo (within the living) bioassays in a local horse farm in the Balochistan province.
  • Alongside, an epidemiological survey was conducted to identify the risk factors contributing to the resistance.

Findings from the Epidemiological Survey and Bioassays

  • The epidemiological survey results indicated that the resistance could have resulted from horse keepers not following the manufacturers’ instructions while applying the acaricides. They used arbitrary amounts, leading to harmful consequences.
  • The in vitro tests, including the adult and larval immersion tests, confirmed that fipronil and ivermectin provided protection against H. anatolicum.
  • However, the in vivo test, the adult-tick mortality assay, demonstrated that fipronil had a better efficiency (78.16%) than ivermectin (49.94%).
  • Surprisingly, even at the highest concentration of acaricide (100 ppm), none of the bioassays achieved more than 80% tick mortality, backing the theory of developed resistance against these acaricides.

Conclusion and Recommendations

  • The study concluded that the unwarranted use of acaricides, ivermectin, and fipronil, had led to the tick species H. anatolicum developing resistance against them.
  • Given the serious implications of this resistance, the researchers urged the need to raise awareness about resistance monitoring and efficacious control of ticks across the country.

Cite This Article

APA
Kamran K, Ali A, Villagra CA, Bazai ZA, Iqbal A, Sajid MS. (2020). Hyalomma anatolicum resistance against ivermectin and fipronil is associated with indiscriminate use of acaricides in southwestern Balochistan, Pakistan. Parasitol Res, 120(1), 15-25. https://doi.org/10.1007/s00436-020-06981-0

Publication

Parasitology research
ISSN: 1432-1955
NlmUniqueID: 8703571
Country: Germany
Language: English
Volume: 120
Issue: 1
Pages: 15-25

Researcher Affiliations

Kamran, Kashif
  • Department of Zoology, University of Balochistan, Quetta, Pakistan.
Ali, Abid
  • Department of Zoology, Abdul Wali Khan University Mardan, Mardan, Khyber Pakhtunkhwa, Pakistan. uop_ali@yahoo.com.
Villagra, Cristian A
  • Instituto de Entomología, Universidad Metropolitana de Ciencias de la Educación, Santiago, Chile.
Bazai, Zahoor Ahmed
  • Department of Botany, University of Balochistan, Quetta, Pakistan.
Iqbal, Asim
  • Department of Zoology, University of Balochistan, Quetta, Pakistan.
Sajid, Muhammad Sohail
  • Department of Parasitology, University of Agriculture, Faisalabad, Pakistan.
  • Center for Advanced Studies in Agriculture and Food Security (CAS-AFS), University of Agriculture, Faisalabad, Pakistan.

MeSH Terms

  • Acaricides / pharmacology
  • Animals
  • Drug Resistance / physiology
  • Horses
  • Inappropriate Prescribing
  • Ivermectin / pharmacology
  • Ixodidae / drug effects
  • Larva / drug effects
  • Pakistan
  • Pyrazoles / pharmacology
  • Tick Infestations / drug therapy
  • Tick Infestations / veterinary

References

This article includes 56 references
  1. Abbas RZ, Zaman MA, Colwell DD, Gilleard J, Iqbal Z. Acaricide resistance in cattle ticks and approaches to its management: the state of play.. Vet Parasitol 2014 Jun 16;203(1-2):6-20.
    doi: 10.1016/j.vetpar.2014.03.006pubmed: 24709006google scholar: lookup
  2. Abdigoudarzi M. Detection of naturally infected vector ticks (acari: ixodidae) by different species of babesia and theileria agents from three different enzootic parts of iran.. J Arthropod Borne Dis 2013;7(2):164-72.
    pubmed: 24409442pmc: 3875883
  3. Ahmed BM, Taha KM, El Hussein AM. Life cycle of Hyalomma anatolicum Koch, 1844 (Acari: Ixodidae) fed on rabbits, sheep and goats.. Vet Parasitol 2011 May 11;177(3-4):353-8.
    doi: 10.1016/j.vetpar.2010.12.012pubmed: 21277088google scholar: lookup
  4. Ali A, Khan MA, Zahid H, Yaseen PM, Qayash Khan M, Nawab J, Ur Rehman Z, Ateeq M, Khan S, Ibrahim M. Seasonal Dynamics, Record of Ticks Infesting Humans, Wild and Domestic Animals and Molecular Phylogeny of Rhipicephalus microplus in Khyber Pakhtunkhwa Pakistan.. Front Physiol 2019;10:793.
    doi: 10.3389/fphys.2019.00793pubmed: 31379587pmc: 6646419google scholar: lookup
  5. Ali A, Mulenga A, Da Silva Vaz Jr I. Tick and Tick-Borne pathogens: molecular and immune targets for control strategies. Front Physiol .
    doi: 10.3389/fphys.2020.00744google scholar: lookup
  6. Azagi T, Klement E, Perlman G, Lustig Y, Mumcuoglu KY, Apanaskevich DA, Gottlieb Y. Francisella-Like Endosymbionts and Rickettsia Species in Local and Imported Hyalomma Ticks.. Appl Environ Microbiol 2017 Sep 15;83(18).
    doi: 10.1128/AEM.01302-17pubmed: 28710265pmc: 5583492google scholar: lookup
  7. Bardosh K, Waiswa C, Welburn SC. Conflict of interest: use of pyrethroids and amidines against tsetse and ticks in zoonotic sleeping sickness endemic areas of Uganda.. Parasit Vectors 2013 Jul 10;6:204.
    doi: 10.1186/1756-3305-6-204pubmed: 23841963pmc: 3711891google scholar: lookup
  8. Basu A, Charles R. Chapter 1—a general account of ticks. Ticks of Trinidad and Tobago—an overview 1–33.
  9. Becker S, Webster A, Doyle RL, Martins JR, Reck J, Klafke GM. Resistance to deltamethrin, fipronil and ivermectin in the brown dog tick, Rhipicephalus sanguineus sensu stricto, Latreille (Acari: Ixodidae).. Ticks Tick Borne Dis 2019 Aug;10(5):1046-1050.
    doi: 10.1016/j.ttbdis.2019.05.015pubmed: 31175029google scholar: lookup
  10. Beugnet F, Halos L, Larsen D, de Vos C. Efficacy of oral afoxolaner for the treatment of canine generalised demodicosis.. Parasite 2016;23:14.
    doi: 10.1051/parasite/2016014pubmed: 27012161pmc: 4807374google scholar: lookup
  11. Bhagwan J, Kumar A, Kumar R, Goyal L, Goel P, Kumar S. Molecular evidence of Theileria equi infection in Hyalomma anatolicum ticks infested on sero-positive Indian horses.. Acta Parasitol 2015 Jun;60(2):322-9.
    doi: 10.1515/ap-2015-0045pubmed: 26204002google scholar: lookup
  12. Biglari P, Bakhshi H, Chinikar S, Belqeiszadeh H, Ghaffari M, Javaherizadeh S, Faghihi F, Telmadarraiy Z. Hyalomma anatolicum as the Main Infesting Tick in an Important Livestock Rearing Region, Central Area of Iran.. Iran J Public Health 2018 May;47(5):742-749.
    pubmed: 29922618pmc: 6005964
  13. Bouchard C, Aenishaenslin C, Rees EE, Koffi JK, Pelcat Y, Ripoche M, Milord F, Lindsay LR, Ogden NH, Leighton PA. Integrated social-behavioral and ecological risk maps to prioritize local public health responses to Lyme disease. Environ Health Perspect 126:693–699.
    doi: 10.1289/EHP1943google scholar: lookup
  14. Buczek A, Bartosik K, Buczek AM, Buczek W, Kulina D. Abnormal development of Hyalomma marginatum ticks (Acari: Ixodidae) induced by plant cytotoxic substances. Toxins 11:445.
    doi: 10.3390/toxins11080445pmc: 6723890google scholar: lookup
  15. Coles TB, Dryden MW. Insecticide/acaricide resistance in fleas and ticks infesting dogs and cats.. Parasit Vectors 2014 Jan 6;7:8.
    doi: 10.1186/1756-3305-7-8pubmed: 24393426pmc: 3891977google scholar: lookup
  16. Dantas-Torres F, Chomel BB, Otranto D. Ticks and tick-borne diseases: a One Health perspective.. Trends Parasitol 2012 Oct;28(10):437-46.
    doi: 10.1016/j.pt.2012.07.003pubmed: 22902521google scholar: lookup
  17. de Castro JJ. Sustainable tick and tickborne disease control in livestock improvement in developing countries.. Vet Parasitol 1997 Jul 31;71(2-3):77-97.
    doi: 10.1016/S0304-4017(97)00033-2pubmed: 9261972google scholar: lookup
  18. De Meneghi D, Stachurski F, Adakal H. Experiences in Tick Control by Acaricide in the Traditional Cattle Sector in Zambia and Burkina Faso: Possible Environmental and Public Health Implications.. Front Public Health 2016;4:239.
    doi: 10.3389/fpubh.2016.00239pubmed: 27882313pmc: 5101216google scholar: lookup
  19. Dumont P, Chester TS, Gale B, Soll M, Fourie JJ, Beugnet F. Acaricidal efficacy of a new combination of fipronil and permethrin against Ixodes ricinus and Rhipicephalus sanguineus ticks.. Parasit Vectors 2015 Jan 27;8:51.
    doi: 10.1186/s13071-015-0681-0pubmed: 25622698pmc: 4316768google scholar: lookup
  20. El-Ashram S, Aboelhadid SM, Kamel AA, Mahrous LN, Fahmy MM. First report of cattle tick Rhipicephalus (Boophilus) annulatus in Egypt resistant to Ivermectin. Insects 10:404.
    doi: 10.3390/insects10110404pmc: 6921020google scholar: lookup
  21. Finney DJ. Probit analysis: a statistical treatment of the sigmoid response curve. .
  22. Foil LD, Coleman P, Eisler M, Fragoso-Sanchez H, Garcia-Vazquez Z, Guerrero FD, Jonsson NN, Langstaff IG, Li AY, Machila N, Miller RJ, Morton J, Pruett JH, Torr S. Factors that influence the prevalence of acaricide resistance and tick-borne diseases.. Vet Parasitol 2004 Oct 28;125(1-2):163-81.
    doi: 10.1016/j.vetpar.2004.05.012pubmed: 15476966google scholar: lookup
  23. . Resistance management and integrated parasite control in ruminants. Guidelines. .
  24. Hall T, Biosciences I, Carlsbad C. BioEdit: an important software for molecular biology. GERF Bull Biosci 2:60–61.
  25. Hinckley AF, Meek JI, Ray JA, Niesobecki SA, Connally NP, Feldman KA, Jones EH, Backenson PB, White JL, Lukacik G, Kay AB, Miranda WP, Mead PS. Effectiveness of Residential Acaricides to Prevent Lyme and Other Tick-borne Diseases in Humans.. J Infect Dis 2016 Jul 15;214(2):182-8.
    doi: 10.1093/infdis/jiv775pubmed: 26740276google scholar: lookup
  26. Hoogstraal H, Aeschlimann A. Tick-host specificity. 55:5–32.
  27. Iqbal A, Iram S, Gul S, Panezai MA. Analysis of immune response in goats Capra hircus lehri against different doses of cement cone extract antigen taken from ticks (Ixodidae) emulsified with different adjuvants. Pakistan Journal of Zoology 48:1179–1184.
  28. Iqbal A, Sajid MS, Khan MN, Khan MK. Frequency distribution of hard ticks (Acari: Ixodidae) infesting bubaline population of district Toba Tek Singh, Punjab, Pakistan.. Parasitol Res 2013 Feb;112(2):535-41.
    doi: 10.1007/s00436-012-3164-7pubmed: 23086441google scholar: lookup
  29. Jongejan F, de Vos C, Fourie JJ, Beugnet F. A novel combination of fipronil and permethrin (Frontline Tri-Act®/Frontect®) reduces risk of transmission of Babesia canis by Dermacentor reticulatus and of Ehrlichia canis by Rhipicephalus sanguineus ticks to dogs.. Parasit Vectors 2015 Nov 19;8:602.
    doi: 10.1186/s13071-015-1207-5pubmed: 26586365pmc: 4653891google scholar: lookup
  30. Jongejan F, de Vos C, Fourie JJ, Beugnet F. A novel combination of fipronil and permethrin (Frontline Tri-Act®/Frontect®) reduces risk of transmission of Babesia canis by Dermacentor reticulatus and of Ehrlichia canis by Rhipicephalus sanguineus ticks to dogs.. Parasit Vectors 2015 Nov 19;8:602.
    doi: 10.1186/s13071-015-1207-5pubmed: 26586365pmc: 4653891google scholar: lookup
  31. Karim S, Budachetri K, Mukherjee N, Williams J, Kausar A, Hassan MJ, Adamson S, Dowd SE, Apanskevich D, Arijo A, Sindhu ZU, Kakar MA, Khan RMD, Ullah S, Sajid MS, Ali A, Iqbal Z. A study of ticks and tick-borne livestock pathogens in Pakistan.. PLoS Negl Trop Dis 2017 Jun;11(6):e0005681.
    doi: 10.1371/journal.pntd.0005681pubmed: 28650978pmc: 5501686google scholar: lookup
  32. Khalid S, Rehman A, Amir MY, Sarfaraz I, Asif M. Comparative efficacy of ivermectin and fipronil on controlling tick infestation in commercial layers: a randomized controlled trial. Pakistan Journal of Zoology 49:1139–1142.
    doi: 10.17582/journal.pjz/2017.49.3.sc9google scholar: lookup
  33. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms.. Mol Biol Evol 2018 Jun 1;35(6):1547-1549.
    doi: 10.1093/molbev/msy096pubmed: 29722887pmc: 5967553google scholar: lookup
  34. Magnarelli LA. Global importance of ticks and associated infectious disease agents. Clin Microbiol Newsl 31:33–37.
    doi: 10.1016/j.clinmicnews.2009.02.001google scholar: lookup
  35. Manjunathachar HV et al. Identification and characterization of vaccine candidates against Hyalomma anatolicum—Vector of Crimean-Congo haemorrhagic fever virus. 66:422–434.
    doi: 10.1111/tbed.13038google scholar: lookup
  36. Marchiondo AA, Holdsworth PA, Fourie LJ, Rugg D, Hellmann K, Snyder DE, Dryden MW. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) second edition: guidelines for evaluating the efficacy of parasiticides for the treatment, prevention and control of flea and tick infestations on dogs and cats. Vet Parasitol 194:84–97.
    doi: 10.1016/j.vetpar.2013.02.003google scholar: lookup
  37. Ogden NH, Lindsay LR, Beauchamp G, Charron D, Maarouf A, O'Callaghan CJ, Waltner-Toews D, Barker IK. Investigation of relationships between temperature and developmental rates of tick Ixodes scapularis (Acari: Ixodidae) in the laboratory and field.. J Med Entomol 2004 Jul;41(4):622-33.
    doi: 10.1603/0022-2585-41.4.622pubmed: 15311453google scholar: lookup
  38. Okello-Onen J, Ssekitto CMB, Ssentongo YK, Kudamba CAL. Tick situation and control strategies in Uganda. International Journal of Tropical Insect Science 13:657–660.
    doi: 10.1017/S174275840001626Xgoogle scholar: lookup
  39. Ostfeld RS, Price A, Hornbostel VL, Benjamin MA, Keesing F. Controlling ticks and tick-borne zoonoses with biological and chemical agents. BioScience 56:383–394.
    doi: 10.1641/0006-3568(2006)056[0383:Ctatzw]2.0.Co;2google scholar: lookup
  40. Pires MS et al. Amblyomma cajennense infestation on horses in two microregions of the state of Rio de Janeiro, Brazil. Revista Brasileira de Parasitologia Veterinária 22:235-242.
    doi: 10.1590/s1984-29612013005000017google scholar: lookup
  41. Raziq A, Younas M, Rehman ZR. Prospects of livestock production in Balochistan. Pak Vet J 30:181–186.
  42. Rehman A, Nijhof AM, Sauter-Louis C, Schauer B, Staubach C, Conraths FJ. Distribution of ticks infesting ruminants and risk factors associated with high tick prevalence in livestock farms in the semi-arid and arid agro-ecological zones of Pakistan.. Parasit Vectors 2017 Apr 19;10(1):190.
    doi: 10.1186/s13071-017-2138-0pubmed: 28420420pmc: 5395890google scholar: lookup
  43. Rodríguez-Hidalgo R, Pérez-Otáñez X, Garcés-Carrera S, Vanwambeke SO, Madder M, Benítez-Ortiz W. The current status of resistance to alpha-cypermethrin, ivermectin, and amitraz of the cattle tick (Rhipicephalus microplus) in Ecuador.. PLoS One 2017;12(4):e0174652.
    doi: 10.1371/journal.pone.0174652pubmed: 28388639pmc: 5384665google scholar: lookup
  44. Rodriguez-Vivas RI, Ojeda-Chi MM, Trinidad-Martinez I, Pérez de León AA. First documentation of ivermectin resistance in Rhipicephalus sanguineus sensu lato (Acari: Ixodidae).. Vet Parasitol 2017 Jan 15;233:9-13.
    doi: 10.1016/j.vetpar.2016.11.015pubmed: 28043394google scholar: lookup
  45. Sabatini GA, Kemp DH, Hughes S, Nari A, Hansen J. Tests to determine LC50 and discriminating doses for macrocyclic lactones against the cattle tick, Boophilus microplus.. Vet Parasitol 2001 Feb;95(1):53-62.
    doi: 10.1016/s0304-4017(00)00406-4pubmed: 11163698google scholar: lookup
  46. Sajid MS, Iqbal Z, Khan MN, Muhamamd G, Iqbal MU. Effect of Hyalomma ticks (Acari: Ixodidae) on milk production of dairy buffaloes (Bos bubalus bubalis) of Punjab (Pakistan). Ital J Anim Sci 6:939–941.
    doi: 10.4081/ijas.2007.s2.939google scholar: lookup
  47. Sajid MS, Iqbal Z, Khan MN, Muhammad G. In vitro and in vivo efficacies of ivermectin and cypermethrin against the cattle tick Hyalomma anatolicum anatolicum (Acari: Ixodidae).. Parasitol Res 2009 Oct;105(4):1133-8.
    doi: 10.1007/s00436-009-1538-2pubmed: 19562374google scholar: lookup
  48. Sajid MS, Iqbal Z, Khan MN, Muhammad G, Needham G, Khan MK. Prevalence, associated determinants, and in vivo chemotherapeutic control of hard ticks (Acari: Ixodidae) infesting domestic goats (Capra hircus) of lower Punjab, Pakistan.. Parasitol Res 2011 Mar;108(3):601-9.
    doi: 10.1007/s00436-010-2103-8pubmed: 20924608google scholar: lookup
  49. Sellon DC, Long M. Equine infectious diseases E-book. .
  50. Shyma KP, Gupta JP, Singh V, Patel KK. In Vitro Detection of Acaricidal Resistance Status of Rhipicephalus (Boophilus) microplus against Commercial Preparation of Deltamethrin, Flumethrin, and Fipronil from North Gujarat, India.. J Parasitol Res 2015;2015:506586.
    doi: 10.1155/2015/506586pubmed: 26788362pmc: 4691617google scholar: lookup
  51. Tabor AE, Ali A, Rehman G, Rocha Garcia G, Zangirolamo AF, Malardo T, Jonsson NN. Cattle Tick Rhipicephalus microplus-Host Interface: A Review of Resistant and Susceptible Host Responses.. Front Cell Infect Microbiol 2017;7:506.
    doi: 10.3389/fcimb.2017.00506pubmed: 29322033pmc: 5732177google scholar: lookup
  52. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0.. Mol Biol Evol 2013 Dec;30(12):2725-9.
    doi: 10.1093/molbev/mst197pubmed: 24132122pmc: 24132122google scholar: lookup
  53. Thrusfield M. Veterinary epidemiology. .
    doi: 10.1002/9781118280249google scholar: lookup
  54. Tiwari A, Singh NK, Singh H, Jyoti BSA, Rath SS. Prevalence of Theileria annulata infection in Hyalomma anatolicum anatolicum collected from crossbred cattle of Ludhiana, Punjab. Journal of parasitic diseases : official organ of the Indian Society for Parasitology 39:57–61.
    doi: 10.1007/s12639-013-0279-4google scholar: lookup
  55. Vudriko P, Okwee-Acai J, Byaruhanga J, Tayebwa DS, Okech SG, Tweyongyere R, Wampande EM, Okurut ARA, Mugabi K, Muhindo JB, Nakavuma JL, Umemiya-Shirafuji R, Xuan X, Suzuki H. Chemical tick control practices in southwestern and northwestern Uganda.. Ticks Tick Borne Dis 2018 May;9(4):945-955.
    doi: 10.1016/j.ttbdis.2018.03.009pubmed: 29606621google scholar: lookup
  56. Walker AR, Bouattou A, Camicas J-L. Ticks of domestic animals in Africa : a guide to identification of species. Edinburgh, Bioscience.

Citations

This article has been cited 19 times.
  1. Obaid MK, Almutairi MM, Alouffi A, Safi SZ, Tanaka T, Ali A. Assessment of cypermethrin and amitraz resistance and molecular profiling of voltage-gated sodium channel and octopamine tyramine genes of Rhipicephalus microplus. Front Cell Infect Microbiol 2023;13:1176013.
    doi: 10.3389/fcimb.2023.1176013pubmed: 37305408google scholar: lookup
  2. Hussain N, Shabbir RMK, Ahmed H, Afzal MS, Ullah S, Ali A, Irum S, Naqvi SK, Yin J, Cao J. Prevalence of different tick species on livestock and associated equines and canine from different agro-ecological zones of Pakistan. Front Vet Sci 2022;9:1089999.
    doi: 10.3389/fvets.2022.1089999pubmed: 36686198google scholar: lookup
  3. Bonnet SI, Vourc'h G, Raffetin A, Falchi A, Figoni J, Fite J, Hoch T, Moutailler S, Quillery E. The control of Hyalomma ticks, vectors of the Crimean-Congo hemorrhagic fever virus: Where are we now and where are we going?. PLoS Negl Trop Dis 2022 Nov;16(11):e0010846.
    doi: 10.1371/journal.pntd.0010846pubmed: 36395110google scholar: lookup
  4. Numan M, Islam N, Adnan M, Zaman Safi S, Chitimia-Dobler L, Labruna MB, Ali A. First genetic report of Ixodes kashmiricus and associated Rickettsia sp. Parasit Vectors 2022 Oct 19;15(1):378.
    doi: 10.1186/s13071-022-05509-ypubmed: 36261834google scholar: lookup
  5. Kamran K, Akbar A, Naseem M, Samad A, Samiullah, Achakzai JK, Rehman ZU, Sohail Sajid M, Ali A. Participatory appraisal for healthcare and welfare management strategies of donkeys (Equus ascinus) in Balochistan, Pakistan. Front Vet Sci 2022;9:1005079.
    doi: 10.3389/fvets.2022.1005079pubmed: 36118345google scholar: lookup
  6. Alam S, Khan M, Alouffi A, Almutairi MM, Ullah S, Numan M, Islam N, Khan Z, Aiman O, Zaman Safi S, Tanaka T, Ali A. Spatio-Temporal Patterns of Ticks and Molecular Survey of Anaplasma marginale, with Notes on Their Phylogeny. Microorganisms 2022 Aug 17;10(8).
    doi: 10.3390/microorganisms10081663pubmed: 36014081google scholar: lookup
  7. Ullah K, Numan M, Alouffi A, Almutairi MM, Zahid H, Khan M, Islam ZU, Kamil A, Safi SZ, Ahmed H, Tanaka T, Ali A. Molecular Characterization and Assessment of Risk Factors Associated with Theileria annulata Infection. Microorganisms 2022 Aug 9;10(8).
    doi: 10.3390/microorganisms10081614pubmed: 36014032google scholar: lookup
  8. Obaid MK, Islam N, Alouffi A, Khan AZ, da Silva Vaz I Jr, Tanaka T, Ali A. Acaricides Resistance in Ticks: Selection, Diagnosis, Mechanisms, and Mitigation. Front Cell Infect Microbiol 2022;12:941831.
    doi: 10.3389/fcimb.2022.941831pubmed: 35873149google scholar: lookup
  9. Paucar V, Pérez-Otáñez X, Rodríguez-Hidalgo R, Perez C, Cepeda-Bastidas D, Grijalva J, Enríquez S, Arciniegas-Ortega S, Vanwambeke SO, Ron-Garrido L, Saegerman C. The Associated Decision and Management Factors on Cattle Tick Level of Infestation in Two Tropical Areas of Ecuador. Pathogens 2022 Mar 26;11(4).
    doi: 10.3390/pathogens11040403pubmed: 35456078google scholar: lookup
  10. Ali A, Numan M, Khan M, Aiman O, Muñoz-Leal S, Chitimia-Dobler L, Labruna MB, Nijhof AM. Ornithodoros (Pavlovskyella) ticks associated with a Rickettsia sp. in Pakistan. Parasit Vectors 2022 Apr 21;15(1):138.
    doi: 10.1186/s13071-022-05248-0pubmed: 35449077google scholar: lookup
  11. Ali A, Shehla S, Zahid H, Ullah F, Zeb I, Ahmed H, da Silva Vaz I Jr, Tanaka T. Molecular Survey and Spatial Distribution of Rickettsia spp. in Ticks Infesting Free-Ranging Wild Animals in Pakistan (2017-2021). Pathogens 2022 Jan 26;11(2).
    doi: 10.3390/pathogens11020162pubmed: 35215108google scholar: lookup
  12. Ali A, Zahid H, Zeb I, Tufail M, Khan S, Haroon M, Tufail M, Bilal M, Hussain M, Alouffi AS, Muñoz-Leal S, Labruna MB. Risk factors associated with tick infestations on equids in Khyber Pakhtunkhwa, Pakistan, with notes on Rickettsia massiliae detection. Parasit Vectors 2021 Jul 13;14(1):363.
    doi: 10.1186/s13071-021-04836-wpubmed: 34256806google scholar: lookup
  13. Zahid H, Muñoz-Leal S, Khan MQ, Alouffi AS, Labruna MB, Ali A. Life Cycle and Genetic Identification of Argas persicus Infesting Domestic Fowl in Khyber Pakhtunkhwa, Pakistan. Front Vet Sci 2021;8:664731.
    doi: 10.3389/fvets.2021.664731pubmed: 34095277google scholar: lookup
  14. Ullah Z, Khan M, Liaqat I, Kamran K, Alouffi A, Almutairi MM, Tanaka T, Ali A. Unveiling Misconceptions among Small-Scale Farmers Regarding Ticks and Tick-Borne Diseases in Balochistan, Pakistan. Vet Sci 2024 Oct 12;11(10).
    doi: 10.3390/vetsci11100497pubmed: 39453090google scholar: lookup
  15. Alvi MHA, Rehman A, Jamil T, Iqbal MZ, Durrani AZ, Khan AU, Usman M, Sauter-Louis C, Conraths FJ. Impact of Farm Management Practices on Tick Infestation in Punjab's Livestock: A Comprehensive Epidemiological Study. Animals (Basel) 2024 Aug 22;14(16).
    doi: 10.3390/ani14162437pubmed: 39199969google scholar: lookup
  16. Gupta S, Sangwan N, Sangwan AK, Gupta S, Kumar A, Maan S, Kumar A, Kumar S. Acaricide resistance status of deltamethrin and coumaphos in Hyalomma anatolicum ticks collected from different districts of Haryana. Exp Appl Acarol 2024 May;92(4):809-833.
    doi: 10.1007/s10493-023-00894-0pubmed: 38448756google scholar: lookup
  17. Ali A, Khan M, Ullah Z, Numan M, Tsai KH, Alouffi A, Almutairi MM, Tanaka T. First record of Alectorobius coniceps (Ixodoidea: Argasidae) and Dermacentor sp. (Ixodoidea: Ixodidae) in Pakistan. Front Vet Sci 2023;10:1326734.
    doi: 10.3389/fvets.2023.1326734pubmed: 38292134google scholar: lookup
  18. Shehla S, Almutairi MM, Alouffi A, Tanaka T, Chang SC, Chen CC, Ali A. Molecular Survey of Rickettsia raoultii in Ticks Infesting Livestock from Pakistan with Notes on Pathogen Distribution in Palearctic and Oriental Regions. Vet Sci 2023 Oct 29;10(11).
    doi: 10.3390/vetsci10110636pubmed: 37999459google scholar: lookup
  19. Aneela A, Almutairi MM, Alouffi A, Ahmed H, Tanaka T, da Silva Vaz I Junior, Chang SC, Chen CC, Ali A. Molecular Detection of Rickettsia hoogstraalii in Hyalomma anatolicum and Haemaphysalis sulcata: Updated Knowledge on the Epidemiology of Tick-Borne Rickettsia hoogstraalii. Vet Sci 2023 Oct 4;10(10).
    doi: 10.3390/vetsci10100605pubmed: 37888557google scholar: lookup
Subscribe to our newsletter
Join 99,658 horse owners like you who receive our email updates on horse health and nutrition.