Seasonal Dynamics, Record of Ticks Infesting Humans, Wild and Domestic Animals and Molecular Phylogeny of Rhipicephalus microplus in Khyber Pakhtunkhwa Pakistan.
Abstract: Although ticks prevalent in various agro-systems of Pakistan are associated with economic losses, information is still missing about the tick's diversity, hosts they infest, seasonal dynamics and molecular phylogeny of in Khyber Pakhtunkhwa (KP) Pakistan. This study for the first time enlisted ticks infesting diverse hosts including humans in various regions of KP. A total of 8,641 ticks were collected across the northern, southern and central regions of KP and were morpho-taxonomically categorized into six genera comprising 17 species, ( = 3,584, 42%), ( = 2,253, 27%) ( = 1,342, 16%), ( = 586, 7%) ( = 161, 2%), ( = 142, 2%), ( = 132, 2%), ( = 123, 1.4%), ( = 110, 1.3%), ( = 34, 0.4%), and ( = 31, 0.4%). Ticks infesting wild animals included , , and , while ticks collected from humans included , , and . The overall prevalence of ticks infesting domestic animals was 69.4% (536/772). Among animal hosts, cattle were found highly infested (87.2%, 157/180) followed by buffalos (79%, 91/114), domestic fowls (74.7%, 112/150), goats (68.3%, 82/120), dogs (66.7%, 32/48), horses (61.3%, 49/80), and sheep (16.3%, 13/80). Analysis revealed that the tick burden significantly differed among domestic animals and was found to be high in cattle, followed by buffalos, goats, sheep, domestic fowl, dogs, and horses. Seasonal patterns of ticks distribution showed highest prevalance in July, August, and September due to the prevailing high temperature and humidity during these months. The phylogenetic analysis of cattle tick based on partial mitochondrial cytochrome oxidase subunit I (COX1), 16S ribosomal RNA (16S rRNA) and internal transcribed spacer 2 (ITS2) sequences, revealed that prevalent in this region belongs to clade C which include ticks originating from Bangladesh, Malaysia, and India. Further large scale studies across the country are necessary to explore the molecular and cross breeding aspects at the geographical overlapping of various tick species and their associated pathogens to facilitate designing control strategies as well as awareness against tick infestation in the region.
Publication Date: 2019-07-16 PubMed ID: 31379587PubMed Central: PMC6646419DOI: 10.3389/fphys.2019.00793Google 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.
- 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.
This research investigates the diversity, prevalence, seasonal dynamics, and molecular phylogeny of ticks in Khyber Pakhtunkhwa, Pakistan, for the first time cataloging tick species on various hosts including humans. The study found a high prevalence of tick infestation in domestic animals, especially cattle, and revealed seasonal patterns and local molecular phylogeny, mapping the ticks to a clade that includes ticks from Bangladesh, Malaysia, and India.
Tick Diversity and Prevalence
- This research took place across the northern, southern, and central regions of Khyber Pakhtunkhwa (KP) Pakistan.
- A total of 8,641 ticks were collected and morphologically classified into six genera and 17 species.
- The ticks were found infesting a range of creatures, including humans, wild and domestic animals.
- The overall prevalence of ticks infesting domestic animals was high at 69.4%.
Host-Specific Infestations
- Among the infested animals observed, cattle suffered a particularly high level of infestation (87.2%), followed by buffalos (79%), domestic fowls (74.7%), goats (68.3%), dogs (66.7%), horses (61.3%), and sheep (16.3%).
- Tick burden was found to vary significantly among different species of domesticated animals.
- Tick species found on human hosts were different from those found on wild animals, implying species-host specificity.
Seasonal Dynamics
- The study also found a clear seasonal pattern in tick prevalence, with the highest numbers encountered in the warmer months of July, August and September.
- This seasonal pattern is likely related to climatic factors such as temperature and humidity, which are known to affect tick survival and activity.
Molecular Phylogeny
- The molecular phylogeny study on a specific species of cattle tick (Rhipicephalus microplus) based on partial mitochondrial cytochrome oxidase subunit I (COX1), 16S ribosomal RNA (16S rRNA), and internal transcribed spacer 2 (ITS2) sequences, established that these ticks belong to clade C, a group that also includes ticks from Bangladesh, Malaysia, and India.
- This result provides key information about the genetic origin and spread of this tick species, which could guide future research and control strategies.
Conclusions and Future Research
- This study emphasizes the need for further, large-scale studies to explore the molecular and cross-breeding aspects at the geographical overlapping of various tick species and their associated pathogens.
- From practical perspectives, the findings may inform design of control strategies against tick infestation and disease transmission, and raise public awareness about ticks in the region.
Cite This Article
APA
Ali A, Khan MA, Zahid H, Yaseen PM, Qayash Khan M, Nawab J, Ur Rehman Z, Ateeq M, Khan S, Ibrahim M.
(2019).
Seasonal Dynamics, Record of Ticks Infesting Humans, Wild and Domestic Animals and Molecular Phylogeny of Rhipicephalus microplus in Khyber Pakhtunkhwa Pakistan.
Front Physiol, 10, 793.
https://doi.org/10.3389/fphys.2019.00793 Publication
Researcher Affiliations
- Department of Zoology, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan.
- Department of Zoology, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan.
- Department of Zoology, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan.
- Department of Zoology, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan.
- Department of Zoology, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan.
- Department of Environmental Sciences, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan.
- Department of Microbiology, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan.
- Department of Chemistry, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan.
- Department of Environmental Sciences, University of Peshawar, Khyber Pakhtunkhwa, Pakistan.
- Department of Chemistry, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan.
References
This article includes 76 references
- Ali A, Parizi L F, Ferreira B R, Junior V, da Silva I. A revision of two distinct species of Rhipicephalus: R. microplus and R. australis.. Cienc. Rural 46 1240–1248.
- Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool.. J Mol Biol 1990 Oct 5;215(3):403-10.
- Apanaskevich D A, Horak I G. The genus Hyalomma. II The taxonomic status of H. (Euhyalomma) anatolicum Koch 1844 and H. (Euhyalomma) excavatum Koch 1844 with the redescription of all stages.. Acarina 13 181–197.
- Apanaskevich D A, Horak I G. The genus Hyalomma Koch, 1844: V. Re-evaluation of the taxonomic rank of taxa comprising the H. (Euhyalomma) marginatum Koch complex of species (Acari: Ixodidae) with redescription of all parasitic stages and notes on biology.. Int. J. Acarol. 34 13–42.
- Apanaskevich DA, Horak IG. The genus Hyalomma Koch, 1844. IX. Redescription of all parasitic stages of H. (Euhyalomma) impeltatum Schulze & Schlottke, 1930 and H. (E.) somalicum Tonelli Rondelli, 1935 (Acari: Ixodidae).. Syst Parasitol 2009 Jul;73(3):199-218.
- Bakirci S, Aysul N, Eren H, Unlu A H, Karagenc T. Diversity of ticks biting humans in Aydın province of Turkey.. Ank Univ Vet Fak Derg 61 93–98.
- Barker SC, Walker AR. Ticks of Australia. The species that infest domestic animals and humans.. Zootaxa 2014 Jun 18;(3816):1-144.
- Baron S, van der Merwe NA, Maritz-Olivier C. The genetic relationship between R. microplus and R. decoloratus ticks in South Africa and their population structure.. Mol Phylogenet Evol 2018 Dec;129:60-69.
- Brahma RK, Dixit V, Sangwan AK, Doley R. Identification and characterization of Rhipicephalus (Boophilus) microplus and Haemaphysalis bispinosa ticks (Acari: Ixodidae) of northeast India by ITS2 and 16S rDNA sequences and morphological analysis.. Exp Appl Acarol 2014 Feb;62(2):253-65.
- Briciu VT, Titilincu A, Tăţulescu DF, Cârstina D, Lefkaditis M, Mihalca AD. First survey on hard ticks (Ixodidae) collected from humans in Romania: possible risks for tick-borne diseases.. Exp Appl Acarol 2011 Jun;54(2):199-204.
- Burger TD, Shao R, Barker SC. Phylogenetic analysis of mitochondrial genome sequences indicates that the cattle tick, Rhipicephalus (Boophilus) microplus, contains a cryptic species.. Mol Phylogenet Evol 2014 Jul;76:241-53.
- Cabezas-Cruz A, Allain E, Ahmad AS, Saeed MA, Rashid I, Ashraf K, Yousfi L, Shehzad W, Indjein L, Rodriguez-Valle M, Estrada-Peña A, Obregón D, Jabbar A, Moutailler S. Low genetic diversity of Ehrlichia canis associated with high co-infection rates in Rhipicephalus sanguineus (s.l.).. Parasit Vectors 2019 Jan 7;12(1):12.
- Caetano RL, Vizzoni VF, Bitencourth K, Carriço C, Sato TP, Pinto ZT, De Oliveira SV, Amorim M, Voloch CM, Gazeta GS. Ultrastructural Morphology and Molecular Analyses of Tropical and Temperate "Species" of Rhipicephalus sanguineus sensu lato (Acari: Ixodidae) in Brazil.. J Med Entomol 2017 Sep 1;54(5):1201-1212.
- Cheng T, Halper B, Siebert J, Cruz-Martinez L, Chapwanya A, Kelly P, Ketzis JK, Vessell J, Köster L, Yao C. Parasites of small Indian mongoose, Herpestes auropunctatus, on St. Kitts, West Indies.. Parasitol Res 2018 Apr;117(4):989-994.
- Coimbra-Dores MJ, Maia-Silva M, Marques W, Oliveira AC, Rosa F, Dias D. Phylogenetic insights on Mediterranean and Afrotropical Rhipicephalus species (Acari: Ixodida) based on mitochondrial DNA.. Exp Appl Acarol 2018 May;75(1):107-128.
- Csordas BG, Garcia MV, Cunha RC, Giachetto PF, Blecha IM, Andreotti R. New insights from molecular characterization of the tick Rhipicephalus (Boophilus) microplus in Brazil.. Rev Bras Parasitol Vet 2016 Jul-Sep;25(3):317-26.
- Dantas-Torres F. Climate change, biodiversity, ticks and tick-borne diseases: The butterfly effect.. Int J Parasitol Parasites Wildl 2015 Dec;4(3):452-61.
- Dantas-Torres F, Latrofa MS, Ramos RAN, Lia RP, Capelli G, Parisi A, Porretta D, Urbanelli S, Otranto D. Biological compatibility between two temperate lineages of brown dog ticks, Rhipicephalus sanguineus (sensu lato).. Parasit Vectors 2018 Jul 9;11(1):398.
- de la Fuente J, Antunes S, Bonnet S, Cabezas-Cruz A, Domingos AG, Estrada-Peña A, Johnson N, Kocan KM, Mansfield KL, Nijhof AM, Papa A, Rudenko N, Villar M, Alberdi P, Torina A, Ayllón N, Vancova M, Golovchenko M, Grubhoffer L, Caracappa S, Fooks AR, Gortazar C, Rego ROM. Tick-Pathogen Interactions and Vector Competence: Identification of Molecular Drivers for Tick-Borne Diseases.. Front Cell Infect Microbiol 2017;7:114.
- De La Fuente J, Rodríguez M, García-García JC. Immunological control of ticks through vaccination with Boophilus microplus gut antigens.. Ann N Y Acad Sci 2000;916:617-21.
- Estrada-Peña A. Climate, niche, ticks, and models: what they are and how we should interpret them.. Parasitol Res 2008 Dec;103 Suppl 1:S87-95.
- Estrada-Peña A, Gray JS, Kahl O, Lane RS, Nijhof AM. Research on the ecology of ticks and tick-borne pathogens--methodological principles and caveats.. Front Cell Infect Microbiol 2013;3:29.
- Estrada-Peña A, Jongejan F. Ticks feeding on humans: a review of records on human-biting Ixodoidea with special reference to pathogen transmission.. Exp Appl Acarol 1999 Sep;23(9):685-715.
- Estrada-Peña A, Venzal JM, Nava S, Mangold A, Guglielmone AA, Labruna MB, de la Fuente J. Reinstatement of Rhipicephalus (Boophilus) australis (Acari: Ixodidae) with redescription of the adult and larval stages.. J Med Entomol 2012 Jul;49(4):794-802.
- Fernández-Soto P, Pérez-Sánchez R, Alamo-Sanz R, Encinas-Grandes A. Spotted fever group rickettsiae in ticks feeding on humans in northwestern Spain: is Rickettsia conorii vanishing?. Ann N Y Acad Sci 2006 Oct;1078:331-3.
- García-García JC, Gonzalez IL, González DM, Valdés M, Méndez L, Lamberti J, D'Agostino B, Citroni D, Fragoso H, Ortiz M, Rodríguez M, de la Fuente J. Sequence variations in the Boophilus microplus Bm86 locus and implications for immunoprotection in cattle vaccinated with this antigen.. Exp Appl Acarol 1999 Nov;23(11):883-95.
- Ghosh HS, Misra KK. Scanning electron microscope study of a snake tick, Amblyomma gervaisi (Acari: Ixodidae).. J Parasit Dis 2012 Oct;36(2):239-50.
- Gondard M, Cabezas-Cruz A, Charles RA, Vayssier-Taussat M, Albina E, Moutailler S. Ticks and Tick-Borne Pathogens of the Caribbean: Current Understanding and Future Directions for More Comprehensive Surveillance.. Front Cell Infect Microbiol 2017;7:490.
- Gratz NG. Emerging and resurging vector-borne diseases.. Annu Rev Entomol 1999;44:51-75.
- Guglielmone A A, Robbins R G. Hard Ticks (Acari: Ixodida: Ixodidae) Parasitizing Humans. New York, NY: Springer; 314.
- Guglielmone A A, Robbins R G, Apanaskevich D A, Petney T N, Estrada-Peña A, Horak I G. The hard ticks of the world.. Dordrecht: Springer.
- Hall T, Biosciences I, Carlsbad C. BioEdit: an important software for molecular biology.. GERF Bull. Biosci. 2 60–61.
- Hanson BA, Frank PA, Mertins JW, Corn JL. Tick paralysis of a snake caused by Amblyomma rotundatum (Acari: Ixodidae).. J Med Entomol 2007 Jan;44(1):155-7.
- Hoogstraal H. Identity, distribution, and hosts of Haemaphysalis (Rhipistoma) indica Warburton (resurrected) (Ixodoidea: Ixodidae), a carnivore parasite of the Indian subregion.. J. Parasitol. 56 1013–1022.
- HOOGSTRAAL H. Haemaphysalis nepalensis sp. n. from a Himalayan rodent and man, and description of the male of H. aponommoides Warburton (n. comb.) (Ixodoidea, Ixodidae). J Parasit 48:195-203, Apr 62 and Pakistan (Ixodoidea, Ixodidae).. J Parasitol 1962 Apr;48:185-94.
- Hoogstraal H, Wassef H Y. Haemaphysalis (Ornithophysalis) kadarsani sp. n. (Ixodoidea: Ixodidae), a rodent parasite of virgin lowland forests in Sulawesi (Celebes).. J. Parasitol. 63 1103–1109.
- Horak IG, Chaparro F, Beaucournu JC, Louw JP. Parasites of domestic and wild animals in South Africa. XXXVI. Arthropod parasites of yellow mongooses, Cynictis penicillata (G. Cuvier, 1829).. Onderstepoort J Vet Res 1999 Mar;66(1):33-8.
- Horak IG, Fourie LJ, Braack LE. Small mammals as hosts of immature ixodid ticks.. Onderstepoort J Vet Res 2005 Sep;72(3):255-61.
- Jabbar A, Abbas T, Sandhu ZU, Saddiqi HA, Qamar MF, Gasser RB. Tick-borne diseases of bovines in Pakistan: major scope for future research and improved control.. Parasit Vectors 2015 May 22;8:283.
- Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P. Global trends in emerging infectious diseases.. Nature 2008 Feb 21;451(7181):990-3.
- Jore S, Vanwambeke SO, Viljugrein H, Isaksen K, Kristoffersen AB, Woldehiwet Z, Johansen B, Brun E, Brun-Hansen H, Westermann S, Larsen IL, Ytrehus B, Hofshagen M. Climate and environmental change drives Ixodes ricinus geographical expansion at the northern range margin.. Parasit Vectors 2014 Jan 8;7:11.
- Kaiser M N, Hoogstraal H. The Hyalomma ticks (Ixodoidea, Ixodidae) of Pakistan, India, and Ceylon, with keys to subgenera and species.. Acarologia 6 257–286.
- Kar S, Yilmazer N, Akyildiz G, Gargili A. The human infesting ticks in the city of Istanbul and its vicinity with reference to a new species for Turkey.. Syst. Appl. Acarol. 22 2245–2256.
- 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.
- 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.
- Labruna MB, Jorge RS, Sana DA, Jácomo AT, Kashivakura CK, Furtado MM, Ferro C, Perez SA, Silveira L, Santos TS Jr, Marques SR, Morato RG, Nava A, Adania CH, Teixeira RH, Gomes AA, Conforti VA, Azevedo FC, Prada CS, Silva JC, Batista AF, Marvulo MF, Morato RL, Alho CJ, Pinter A, Ferreira PM, Ferreira F, Barros-Battesti DM. Ticks (Acari: Ixodida) on wild carnivores in Brazil.. Exp Appl Acarol 2005;36(1-2):149-63.
- Labruna MB, McBride JW, Bouyer DH, Camargo LM, Camargo EP, Walker DH. Molecular evidence for a spotted fever group Rickettsia species in the tick Amblyomma longirostre in Brazil.. J Med Entomol 2004 May;41(3):533-7.
- Labruna MB, Naranjo V, Mangold AJ, Thompson C, Estrada-Peña A, Guglielmone AA, Jongejan F, de la Fuente J. Allopatric speciation in ticks: genetic and reproductive divergence between geographic strains of Rhipicephalus (Boophilus) microplus.. BMC Evol Biol 2009 Feb 25;9:46.
- Léger E, Vourc'h G, Vial L, Chevillon C, McCoy KD. Changing distributions of ticks: causes and consequences.. Exp Appl Acarol 2013 Feb;59(1-2):219-44.
- Lempereur L, Geysen D, Madder M. Development and validation of a PCR-RFLP test to identify African Rhipicephalus (Boophilus) ticks.. Acta Trop 2010 Apr;114(1):55-8.
- 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.
- Lew-Tabor AE, Rodriguez Valle M. A review of reverse vaccinology approaches for the development of vaccines against ticks and tick borne diseases.. Ticks Tick Borne Dis 2016 Jun;7(4):573-85.
- Low VL, Tay ST, Kho KL, Koh FX, Tan TK, Lim YA, Ong BL, Panchadcharam C, Norma-Rashid Y, Sofian-Azirun M. Molecular characterisation of the tick Rhipicephalus microplus in Malaysia: new insights into the cryptic diversity and distinct genetic assemblages throughout the world.. Parasit Vectors 2015 Jun 24;8:341.
- Lv J, Wu S, Zhang Y, Zhang T, Feng C, Jia G, Lin X. Development of a DNA barcoding system for the Ixodida (Acari: Ixodida).. Mitochondrial DNA 2014 Apr;25(2):142-9.
- Madder M, Horak I, Stoltsz H. Tick Identification.. Pretoria: Faculty of veterinary Science University of Pretoria, 58.
- Manan A, Khan Z, Ahmad B. Prevalence and identification of ixodid tick genera in frontier region Peshawar.. J. Agric. Biol. Sci. 37 173–176.
- Marcus L C. Veterinary Biology and Medicine of Captive Amphibians and Reptiles.. Philadelphia, PA: Lea and Febiger.
- Nowak-Chmura M. Teratological changes in tick morphology in ticks feeding on exotic reptiles.. J. Nat. Hist. 46 911–921.
- Okino T, Ushirogawa H, Matoba K, Hatsushika R. Bibliographical studies on human cases of hard tick (Acarina: Ixodidae) bites in Japan (5) cases of Ixodes acutitarsus and I. turdus infestation.. Kawasaki Med. J. 36 115–120.
- Paddock CD, Childs JE. Ehrlichia chaffeensis: a prototypical emerging pathogen.. Clin Microbiol Rev 2003 Jan;16(1):37-64.
- Papa A, Karabaxoglou D, Kansouzidou A. Acute West Nile virus neuroinvasive infections: cross-reactivity with dengue virus and tick-borne encephalitis virus.. J Med Virol 2011 Oct;83(10):1861-5.
- Parola P, Raoult D. Ticks and tickborne bacterial diseases in humans: an emerging infectious threat.. Clin Infect Dis 2001 Mar 15;32(6):897-928.
- 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.
- Robertson RG, Wiseman CL Jr, Traub R. Tick-borne rickttsiae of the spotted fever group in West Pakistan. I. Isolation of strains from ticks in different habitats.. Am J Epidemiol 1970 Dec;92(6):382-94.
- Roy BC, Krücken J, Ahmed JS, Majumder S, Baumann MP, Clausen PH, Nijhof AM. Molecular identification of tick-borne pathogens infecting cattle in Mymensingh district of Bangladesh reveals emerging species of Anaplasma and Babesia.. Transbound Emerg Dis 2018 Apr;65(2):e231-e242.
- Santos-Silva MM, Beati L, Santos AS, De Sousa R, Núncio MS, Melo P, Santos-Reis M, Fonseca C, Formosinho P, Vilela C, Bacellar F. The hard-tick fauna of mainland Portugal (Acari: Ixodidae): an update on geographical distribution and known associations with hosts and pathogens.. Exp Appl Acarol 2011 Sep;55(1):85-121.
- Schorderet-Weber S, Noack S, Selzer PM, Kaminsky R. Blocking transmission of vector-borne diseases.. Int J Parasitol Drugs Drug Resist 2017 Apr;7(1):90-109.
- Serra-Freire NM. Occurrence of ticks (Acari: Ixodidae) on human hosts, in three municipalities in the State of Pará, Brazil.. Rev Bras Parasitol Vet 2010 Jul-Sep;19(3):141-7.
- Sherrard-Smith E, Chadwick E, Cable J. Abiotic and biotic factors associated with tick population dynamics on a mammalian host: Ixodes hexagonus infesting otters, Lutra lutra.. PLoS One 2012;7(10):e47131.
- Stenos J, Graves SR, Unsworth NB. A highly sensitive and specific real-time PCR assay for the detection of spotted fever and typhus group Rickettsiae.. Am J Trop Med Hyg 2005 Dec;73(6):1083-5.
- Stephen S, Achyutha Rao KN. Q fever in South Kanara district: natural occurrence of Coxiella burnetii in the tick (Aponomma gervaisi)--preliminary report.. Indian J Med Res 1979 Feb;69:244-6.
- Tadesse F, Abadfaji G, Girma S, Jibat T. Identification of tick species and their preferred site on cattles body in and around Mizan Teferi, Southwestern Ethiopia.. Vet. Med. Anim. Health 4 1–5.
- 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.
- Tenderio J. Alguns dados sobre as stirpes de Coxiella burneti isoladas na Guine Portugusea.. Bol. Cult. Guine Port. 8 69–87.
- Walker A R, Bouattour A, Camicas J L, Estrada-Peña A, Horak I G, Latif A A. Ticks of Domestic Animals in Africa: A Guide to Identification of Species.. Edinburgh: Bioscience Reports.
- Yu Z, Wang H, Wang T, Sun W, Yang X, Liu J. Tick-borne pathogens and the vector potential of ticks in China.. Parasit Vectors 2015 Jan 14;8:24.
Citations
This article has been cited 58 times.- Ali A, Obaid MK, Almutairi MM, Alouffi A, Numan M, Ullah S, Rehman G, Islam ZU, Khan SB, Tanaka T. Molecular detection of Coxiella spp. in ticks (Ixodidae and Argasidae) infesting domestic and wild animals: with notes on the epidemiology of tick-borne Coxiella burnetii in Asia. Front Microbiol 2023;14:1229950.
- 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.
- Ullah S, Alouffi A, Almutairi MM, Islam N, Rehman G, Ul Islam Z, Ahmed H, Júnior IDSV, Labruna MB, Tanaka T, Ali A. First Report of Rickettsia conorii in Hyalomma kumari Ticks. Animals (Basel) 2023 Apr 27;13(9).
- Khan SM, Khan M, Alouffi A, Almutairi MM, Numan M, Ullah S, Obaid MK, Islam ZU, Ahmed H, Tanaka T, Ali A. Phylogenetic Position of Haemaphysalis kashmirensis and Haemaphysalis cornupunctata, with Notes on Rickettsia spp. Genes (Basel) 2023 Jan 30;14(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.
- Zeb J, Song B, Senbill H, Aziz MU, Hussain S, Khan MA, Qadri I, Cabezas-Cruz A, de la Fuente J, Sparagano OA. Ticks Infesting Dogs in Khyber Pakhtunkhwa, Pakistan: Detailed Epidemiological and Molecular Report. Pathogens 2023 Jan 6;12(1).
- Zeb I, Almutairi MM, Alouffi A, Islam N, Parizi LF, Safi SZ, Tanaka T, da Silva Vaz I Jr, Ali A. Low Genetic Polymorphism in the Immunogenic Sequences of Rhipicephalus microplus Clade C. Vaccines (Basel) 2022 Nov 11;10(11).
- Lu M, Meng C, Gao X, Sun Y, Zhang J, Tang G, Li Y, Li M, Zhou G, Wang W, Li K. Diversity of Rickettsiales in Rhipicephalus microplus Ticks Collected in Domestic Ruminants in Guizhou Province, China. Pathogens 2022 Sep 27;11(10).
- 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.
- Iqbal Z, Kayani AR, Akhter A, Qayyum M. Prevalence and Distribution of Hard Ticks and Their Associated Risk Factors in Sheep and Goats from Four Agro-Climatic Zones of Khyber Pakhtunkhwa (KPK), Pakistan. Int J Environ Res Public Health 2022 Sep 17;19(18).
- 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.
- 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).
- 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).
- Chen Z, Liu J. A review of argasid ticks and associated pathogens of China. Front Vet Sci 2022;9:865664.
- Zaheer T, Kandeel M, Abbas RZ, Khan SR, Rehman TU, Aqib AI. Acaricidal Potential and Ecotoxicity of Metallic Nano-Pesticides Used against the Major Life Stages of Hyalomma Ticks. Life (Basel) 2022 Jun 29;12(7).
- 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.
- Sultan S, Zeb J, Ayaz S, Rehman SU, Khan S, Hussain M, Senbill H, Husain S, Sparagano OA. Epidemiologic profile of hard ticks and molecular characterization of Rhipicephalus microplus infesting cattle in central part of Khyber Pakhtunkhwa, Pakistan. Parasitol Res 2022 Sep;121(9):2481-2493.
- Khan Z, Shehla S, Alouffi A, Kashif Obaid M, Zeb Khan A, Almutairi MM, Numan M, Aiman O, Alam S, Ullah S, Zaman Safi S, Tanaka T, Ali A. Molecular Survey and Genetic Characterization of Anaplasma marginale in Ticks Collected from Livestock Hosts in Pakistan. Animals (Basel) 2022 Jul 1;12(13).
- Nasirian H. Detailed new insights about tick infestations in domestic ruminant groups: a global systematic review and meta-analysis. J Parasit Dis 2022 Jun;46(2):526-601.
- Khan A, Ahmed Muhammed A, Nasreen N, Iqbal F, Cossio-Bayugar R, Ali Sha SS, Alanazi AD, Zajac Z. Tick-borne haemoparasitic diseases in small ruminants in Pakistan: Current knowledge and future perspectives. Saudi J Biol Sci 2022 Apr;29(4):2014-2025.
- 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.
- 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).
- Mattos C, Andrade J, Salarini Peixoto B, Tavares Moraes NL, da Cunha Veloso MC, Alves Romeiro G, Folly EDC. Acaricidal Properties of Bio-Oil Derived From Slow Pyrolysis of Crambe abyssinica Fruit Against the Cattle Tick Rhipicephalus microplus (Acari: Ixodidae). Front Physiol 2021;12:768522.
- Ullah R, Shams S, Khan MA, Ayaz S, Akbar NU, Din QU, Khan A, Leon R, Zeb J. Epidemiology and molecular characterization of Theileria annulata in cattle from central Khyber Pakhtunkhwa, Pakistan. PLoS One 2021;16(9):e0249417.
- Rooman M, Assad Y, Tabassum S, Sultan S, Ayaz S, Khan MF, Khan SN, Ali R. A cross-sectional survey of hard ticks and molecular characterization of Rhipicephalus microplus parasitizing domestic animals of Khyber Pakhtunkhwa, Pakistan. PLoS One 2021;16(8):e0255138.
- 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.
- 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.
- Hussain S, Hussain A, Ho J, Li J, George D, Rehman A, Zeb J, Sparagano O. An Epidemiological Survey Regarding Ticks and Tick-Borne Diseases among Livestock Owners in Punjab, Pakistan: A One Health Context. Pathogens 2021 Mar 18;10(3).
- Iatta R, Sazmand A, Nguyen VL, Nemati F, Ayaz MM, Bahiraei Z, Zafari S, Giannico A, Greco G, Dantas-Torres F, Otranto D. Vector-borne pathogens in dogs of different regions of Iran and Pakistan. Parasitol Res 2021 Dec;120(12):4219-4228.
- Kamran K, Ali A, Villagra CA, Bazai ZA, Iqbal A, Sajid MS. Hyalomma anatolicum resistance against ivermectin and fipronil is associated with indiscriminate use of acaricides in southwestern Balochistan, Pakistan. Parasitol Res 2021 Jan;120(1):15-25.
- Ghafar A, Abbas T, Rehman A, Sandhu ZU, Cabezas-Cruz A, Jabbar A. Systematic Review of Ticks and Tick-Borne Pathogens of Small Ruminants in Pakistan. Pathogens 2020 Nov 11;9(11).
- Pacheco I, Acevedo P, Prado E, Mihalca AD, de la Fuente J. Targeting the Exoskeleton Elementome to Track Tick Geographic Origins. Front Physiol 2020;11:572758.
- Ghafar A, Khan A, Cabezas-Cruz A, Gauci CG, Niaz S, Ayaz S, Mateos-Hernández L, Galon C, Nasreen N, Moutailler S, Gasser RB, Jabbar A. An Assessment of the Molecular Diversity of Ticks and Tick-Borne Microorganisms of Small Ruminants in Pakistan. Microorganisms 2020 Sep 17;8(9).
- Hernandez EP, Shimazaki K, Niihara H, Umemiya-Shirafuji R, Fujisaki K, Tanaka T. Expression analysis of glutathione S-transferases and ferritins during the embryogenesis of the tick Haemaphysalis longicornis. Heliyon 2020 Mar;6(3):e03644.
- Ghafar A, Cabezas-Cruz A, Galon C, Obregon D, Gasser RB, Moutailler S, Jabbar A. Bovine ticks harbour a diverse array of microorganisms in Pakistan. Parasit Vectors 2020 Jan 3;13(1):1.
- Lalawmpuii K, Jacob SS, Tolenkhomba TC, Behera P, Lalmuanpuia J, Lalremsanga HT, Lalrintluanga K, Lalchhandama C, Biakzuala L, Lalrinkima H. Mitochondrial and Nuclear DNA Analyses of Rhipicephalus microplus from Mizoram, Northeast India: Insights into Genetic Diversity and Endosymbiont. Genes (Basel) 2025 Oct 15;16(10).
- Obaid MK, Luo J, Zhao S, Tian Z, Ullah S, Zeb J, Liu G, Luo J, Yin H, Rashid M, Ren Q, Guan G. Molecular Profiling of Ticks and Associated Pathogens: First Report of Rickettsia sibirica, Rickettsia slovaca, and Babesia microti in Ticks From Pakistan. Transbound Emerg Dis 2025;2025:3157047.
- Pandey GS, Pathak CR, Sadaula A, Manandhar P, Bastakoti R, Kwak ML, Hayashi N, Nonaka N, Nakao R. Molecular characterization of Rhipicephalus microplus and tick-borne pathogens in cattle in Nepal. Vet Res Commun 2025 Oct 4;49(6):346.
- Luciano A, Jallow BJJ, Liu M, Ma Y, Miambo RD, Meng F. Distribution of Rhipicephalus microplus and Hyalomma lusitanicum, and the pathogens they are carrying: A systematic review. Parasite Epidemiol Control 2025 Aug;30:e00437.
- Jamil L, Li C, Wang Y, Jamil J, Tian W, Zhao D, Shen S, Sun Y, Zhao L, Cao W. High Diversity and Low Coinfections of Pathogens in Ticks from Ruminants in Pakistan. Microorganisms 2025 May 30;13(6).
- Ciarma M, Melis S, Bisaglia B, Batisti Biffignandi G, Sunny GS, Vumbaca M, Epis S, Arshad M, Ahmed H, Sassera D, Castelli M. Survey of tick-borne pathogens in Rhipicephalus microplus ticks from livestock in the Northern Punjab Province, Pakistan. Curr Res Parasitol Vector Borne Dis 2025;7:100275.
- Hussain S, Hussain A, Aziz MU, Song B, Zeb J, Moutailler S, Foucault-Simonin A, Smith RL, Cabezas-Cruz A, George D, Sparagano O. Exploring the Coinfection and Genetic Diversity of Multiple Tick-Borne Pathogens in Livestock Population of Punjab, Pakistan. Transbound Emerg Dis 2024;2024:9958535.
- Yean S, Prasetyo DB, Ren T, Krib D, Sen S, Chea B, Tum S, Sorn S, Sum S, Boyer S. Seasonal dynamic of ticks infesting cattle (Bos indicus) farms in two provinces in Cambodia. PLoS One 2025;20(4):e0320879.
- Ullah Z, Liaqat I, Khan M, Alouffi A, Almutairi MM, Apanaskevich DA, Tanaka T, Ali A. Investigation of Hyalomma turanicum and Hyalomma asiaticum in Pakistan, with notes on the detection of tickborne Rickettsiales. Front Vet Sci 2024;11:1500930.
- Abbas MZ, Ghafoor M, Hussain MH, Alvi MA, Jamil T, Sajid MS, Aslam M, Hassan A, Hussain S, Hafeez MA, Ullah MI, Khan I, Ashfaq K, Muhammad G, Mertens-Scholz K, Neubauer H, El-Adawy H, Saqib M. A Cross-Sectional Serological Study to Assess the Prevalence and Risk Factors of Anaplasmosis in Dromedary Camels in Punjab, Pakistan. Vet Sci 2024 Dec 16;11(12).
- 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).
- Khan Z, Ullah F, Ullah S, Ibrahim M, Khan M, Rehman G, Tanaka T, Almutairi MM, Alouffi A, Ali A. Molecular detection of Anaplasma bovis, Candidatus Anaplasma boleense and Rickettsia spp. in ticks infesting small ruminants. BMC Vet Res 2024 Sep 11;20(1):408.
- Ali S, Ahmad AS, Ashraf K, Khan JA, Rashid MI. Insights into the involvement of male Hyalomma anatolicum ticks in transmitting Anaplasma marginale, lumpy skin disease virus and Theileria annulata. Trop Anim Health Prod 2024 May 18;56(5):167.
- Obaid MK, Shehla S, Guan G, Rashid M, Shams S. Genotyping of ticks: first molecular report of Hyalomma asiaticum and molecular detection of tick-borne bacteria in ticks and blood from Khyber Pakhtunkhwa, Pakistan. Front Cell Infect Microbiol 2024;14:1346595.
- Deng YP, Li R, Zhang XL, Yi XL, Liu GH. The complete mitochondrial genome of cattle tick clade C reveals the genetic relationship within Rhipicephalus microplus complex. Parasitol Res 2024 Mar 22;123(3):168.
- Majid A, Almutairi MM, Alouffi A, Tanaka T, Yen TY, Tsai KH, Ali A. First report of spotted fever group Rickettsia aeschlimannii in Hyalomma turanicum, Haemaphysalis bispinosa, and Haemaphysalis montgomeryi infesting domestic animals: updates on the epidemiology of tick-borne Rickettsia aeschlimannii. Front Microbiol 2023;14:1283814.
- 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).
- Nasirian H. Hard Tick Species Parasitism Levels in Domestic Ruminants with Their Distribution and Role as Vectors: A Detailed Global Meta-analysis and Systematic Review. Acta Parasitol 2024 Mar;69(1):1-105.
- Zahid H, Alouffi A, Almutairi MM, Ateeq M, Tanaka T, Chang SC, Chen CC, Ali A. Argas persicus and Carios vespertilionis Ticks Infesting Ducks, Domestic Fowls and Bats in Pakistan: First Report on Molecular Survey and Phylogenetic Position of Borrelia anserina. Vet Sci 2023 Oct 20;10(10).
- 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).
- Krausser L, Chauvaux E, Van Dyck-Lippens M, Yssouf A, Assoumani Y, Tortosa P, de Jong BC, Braet SM. Ticks are unlikely to play a role in leprosy transmission in the Comoros (East Africa) as they do not harbour M. leprae DNA. Front Med (Lausanne) 2023;10:1238914.
- Ali A, Ullah S, Numan M, Almutairi MM, Alouffi A, Tanaka T. First report on tick-borne pathogens detected in ticks infesting stray dogs near butcher shops. Front Vet Sci 2023;10:1246871.
- Tila H, Khan M, Almutairi MM, Alouffi A, Ahmed H, Tanaka T, Tsai KH, Ali A. First report on detection of Hepatozoon ayorgbor in Rhipicephalus haemaphysaloides and Hepatozoon colubri in Haemaphysalis sulcata and Hyalomma anatolicum: risks of spillover of Hepatozoon spp. from wildlife to domestic animals. Front Vet Sci 2023;10:1255482.
Use Nutrition Calculator
Check if your horse's diet meets their nutrition requirements with our easy-to-use tool Check your horse's diet with our easy-to-use tool
Talk to a Nutritionist
Discuss your horse's feeding plan with our experts over a free phone consultation Discuss your horse's diet over a phone consultation
Submit Diet Evaluation
Get a customized feeding plan for your horse formulated by our equine nutritionists Get a custom feeding plan formulated by our nutritionists