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Parasites & vectors2021; 14(1); 363; doi: 10.1186/s13071-021-04836-w

Risk factors associated with tick infestations on equids in Khyber Pakhtunkhwa, Pakistan, with notes on Rickettsia massiliae detection.

Abstract: Studies on ticks infesting equids are lacking in various parts of the world, including Khyber Pakhtunkhwa (KP), Pakistan. The aim of this study was to investigate the diversity of ticks infesting equids, associated risk factors and rickettsial detection in ticks from equids in KP. Methods: Inspection of 404 equid hosts from November 2018 to October 2019 resulted in the collection of 550 ticks. Data on tick-associated risk factors were collected from equid owners by means of a questionnaire. After morphological identification, partial DNA sequences of the tick mitochondrial 16S rRNA gene were used for taxonomic confirmation of species. Partial sequences of the gltA and ompA genes were used for Rickettsia detection in ticks. Results: A total of 550 tick specimens were collected on 324 (80.2%) of the equids inspected, of which 161 were horses (50%), 145 (45%) were donkeys and 18 were mules (5%). The ticks were identified as belonging to the following five species: Rhipicephalus microplus (341 specimens, 62% of the total ticks), Rh. haemaphysaloides (126, 23%), Rh. turanicus (39, 7%), Rh. sanguineus (s.l.) (33, 6%) and Hyalomma anatolicum (11, 2%). The most prevalent tick life stage was adult females (279, 51%) followed by adult males (186, 34%) and nymphs (85, 15%). Higher tick infestations were observed on male equids (relative risk [RR] 0.7432, P < 0.0005) and adult equids (RR 1.268, P < 0.0020). Ticks were frequently attached to the axial region of horses (55, 21%), sternum of donkeys (44, 21%) and belly of mules (19, 23%) (P < 0.04). Temporal patterns of tick infestation in association with temperature and humidity were highly significant (P < 0.05). Risk factors, such as animal housing (P < 0.0003), living management (P < 0.006), grazing type (P < 0.01) and location in hilly areas (P < 0.02), significantly enhanced the chances for tick infestation. Tick species analyzed in this study were phylogenetically related to species from Afghanistan, China, South Africa and Taiwan. Partial sequences of the gltA and ompA genes obtained from Rh. microplus and Rh. haemaphysaloides were 100% identical to the spotted fever group pathogen Rickettsia massiliae. Conclusions: Equids exposed to significant risk factors were infected by one or more of at least five tick species in KP, Pakistan, and some of the ticks harbored the human pathogen R. massiliae.
© 2021. The Author(s).
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Publication Date: 2021-07-13 PubMed ID: 34256806PubMed Central: PMC8276440DOI: 10.1186/s13071-021-04836-wGoogle Scholar: Lookup
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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 discusses a study conducted to understand the diversity of ticks infesting equids, the risk factors associated with tick infestations, and the detection of a certain bacterium in ticks from equids in Khyber Pakhtunkhwa, Pakistan. The study discovered that certain behaviours and environments significantly increased the risk of tick infestation and found that some of the ticks carried the Rickettsia massiliae, a potentially harmful pathogen to humans.

Methodology

  • The data for the study was collected by inspecting 404 equid hosts from November 2018 to October 2019, resulting in the collection of 550 ticks.
  • A questionnaire was administered to equid owners to collect data on tick-associated risk factors.
  • The collected ticks were morphologically identified and taxonomic confirmation of species was done using partial DNA sequences of the tick mitochondrial 16S rRNA gene.
  • Rickettsia detection in ticks was done using partial sequences of the gltA and ompA genes.

Results

  • Of the 450 ticks collected, 62% were identified as Rhipicephalus microplus, 23% as Rh. haemaphysaloides, 7% as Rh. turanicus, 6% as Rh. sanguineus (s.l.) and 2% as Hyalomma anatolicum.
  • Higher tick infestations were observed on male equids and adult equids. Ticks were mostly attached to the axial region of horses, sternum of donkeys and belly of mules.
  • Temporal patterns of tick infestation in relation with temperature and humidity were significantly high.
  • Lifestyle factors such as animal housing, living management, grazing type and location in hilly areas increased the risk of tick infestation.
  • The detected tick species were found to be related to species from Afghanistan, China, South Africa and Taiwan.
  • Partial sequences of the gltA and ompA genes obtained from Rh. microplus and Rh. haemaphysaloides were 100% identical to the spotted fever group pathogen Rickettsia massiliae, a potentially harmful bacteria to humans.

Conclusions

  • The study concludes that equids exposed to certain risk factors in KP, Pakistan were infected by one or more of at least five tick species some of which carried R. massiliae, potentially posing a health risk to humans.

Cite This Article

APA
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. (2021). Risk factors associated with tick infestations on equids in Khyber Pakhtunkhwa, Pakistan, with notes on Rickettsia massiliae detection. Parasit Vectors, 14(1), 363. https://doi.org/10.1186/s13071-021-04836-w

Publication

Parasites & vectors
ISSN: 1756-3305
NlmUniqueID: 101462774
Country: England
Language: English
Volume: 14
Issue: 1
Pages: 363
PII: 363

Researcher Affiliations

Ali, Abid
  • Department of Zoology, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan. uop_ali@yahoo.com.
Zahid, Hafsa
  • Department of Zoology, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan.
Zeb, Ismail
  • Department of Zoology, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan.
Tufail, Muhammad
  • Department of Zoology, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan.
Khan, Sulaiman
  • Department of Zoology, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan.
Haroon, Muhammad
  • Department of Zoology, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan.
Tufail, Muhammad
  • Department of Zoology, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan.
Bilal, Muhammad
  • Department of Zoology, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan.
Hussain, Majid
  • Department of Zoology, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Pakistan.
Alouffi, Abdulaziz S
  • King Abdulaziz City for Science and Technology, Riyadh, Saudi Arabia.
Muñoz-Leal, Sebastián
  • Departamento de Ciencia Animal, Facultad de Ciencias Veterinarias, Universidad de Concepción, Av. Vicente Méndez 595, casilla 537, Chillán, Ñuble, Chile.
Labruna, Marcelo B
  • Department of Preventive Veterinary Medicine and Animal Health, Faculty of Veterinary Medicine, University of São Paulo, São Paulo, Brazil.

MeSH Terms

  • Animals
  • DNA, Bacterial / genetics
  • Female
  • Horses / parasitology
  • Male
  • Nymph / microbiology
  • Pakistan / epidemiology
  • Phylogeny
  • RNA, Ribosomal, 16S / genetics
  • Rickettsia / genetics
  • Rickettsia / isolation & purification
  • Rickettsia Infections / epidemiology
  • Rickettsia Infections / veterinary
  • Risk Factors
  • Tick Infestations / epidemiology
  • Tick Infestations / veterinary
  • Ticks / classification
  • Ticks / genetics

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

This article includes 51 references
  1. 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.
    doi: 10.1016/j.ttbdis.2015.12.012pubmed: 26723274google scholar: lookup
  2. Labruna MB, Whitworth T, Bouyer DH, McBride J, Camargo LM, Camargo EP, Popov V, Walker DH. Rickettsia bellii and Rickettsia amblyommii in Amblyomma ticks from the State of Rondônia, Western Amazon, Brazil.. J Med Entomol 2004 Nov;41(6):1073-81.
    pubmed: 15605647doi: 10.1603/0022-2585-41.6.1073google scholar: lookup
  3. 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.
    doi: 10.3389/fcimb.2017.00490pmc: PMC5713125pubmed: 29238699google scholar: lookup
  4. 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.
    doi: 10.1016/j.ijpddr.2017.01.004pmc: PMC5302141pubmed: 28189117google scholar: lookup
  5. Estrada-Peña A, Ayllón N, de la Fuente J. Impact of climate trends on tick-borne pathogen transmission.. Front Physiol 2012;3:64.
    doi: 10.3389/fphys.2012.00064pmc: PMC3313475pubmed: 22470348google scholar: lookup
  6. Szabó MP, Pinter A, Labruna MB. Ecology, biology and distribution of spotted-fever tick vectors in Brazil.. Front Cell Infect Microbiol 2013;3:27.
    doi: 10.3389/fcimb.2013.00027pmc: PMC3709097pubmed: 23875178google scholar: lookup
  7. Esser HJ, Mögling R, Cleton NB, van der Jeugd H, Sprong H, Stroo A, Koopmans MPG, de Boer WF, Reusken CBEM. Risk factors associated with sustained circulation of six zoonotic arboviruses: a systematic review for selection of surveillance sites in non-endemic areas.. Parasit Vectors 2019 May 27;12(1):265.
    doi: 10.1186/s13071-019-3515-7pmc: PMC6537422pubmed: 31133059google scholar: lookup
  8. Pietzsch ME, Medlock JM, Jones L, Avenell D, Abbott J, Harding P, Leach S. Distribution of Ixodes ricinus in the British Isles: investigation of historical records.. Med Vet Entomol 2005 Sep;19(3):306-14.
    doi: 10.1111/j.1365-2915.2005.00575.xpubmed: 16134979google scholar: lookup
  9. 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.
    doi: 10.1007/s10493-012-9615-0pubmed: 23015121google scholar: lookup
  10. 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.
    doi: 10.1007/s00436-008-1056-7pubmed: 19030890google scholar: lookup
  11. Egekwu N, Sonenshine DE, Bissinger BW, Roe RM. Transcriptome of the female synganglion of the black-legged tick Ixodes scapularis (Acari: Ixodidae) with comparison between Illumina and 454 systems.. PLoS One 2014;9(7):e102667.
    doi: 10.1371/journal.pone.0102667pmc: PMC4116169pubmed: 25075967google scholar: lookup
  12. James AM, Burdett C, McCool MJ, Fox A, Riggs P. The geographic distribution and ecological preferences of the American dog tick, Dermacentor variabilis (Say), in the U.S.A.. Med Vet Entomol 2015 Jun;29(2):178-88.
    doi: 10.1111/mve.12099pubmed: 25684582google scholar: lookup
  13. 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.0005681pmc: PMC5501686pubmed: 28650978google scholar: lookup
  14. Laus F, Veronesi F, Passamonti F, Paggi E, Cerquetella M, Hyatt D, Tesei B, Fioretti DP. Prevalence of tick borne pathogens in horses from Italy.. J Vet Med Sci 2013;75(6):715-20.
    doi: 10.1292/jvms.12-0449pubmed: 23328633google scholar: lookup
  15. Kamran K, Ali A, Villagra C, Siddiqui S, Alouffi AS, Iqbal A. A cross-sectional study of hard ticks (acari: ixodidae) on horse farms to assess the risk factors associated with tick-borne diseases.. Zoonoses Public Health 2021 May;68(3):247-262.
    doi: 10.1111/zph.12809pubmed: 33522145google scholar: lookup
  16. 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/s13071-017-2138-0pmc: PMC5395890pubmed: 28420420google scholar: lookup
  17. 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.
    pmc: PMC6646419pubmed: 31379587doi: 10.3389/fphys.2019.00793google scholar: lookup
  18. Geevarghese G, Dhanda V. The Indian Hyalomma ticks (Ixodoidea: Ixodidae) New Delhi: ICAR Press; 1987. p. 119.
  19. Walker JB, Keirans JE, Horak IG. The genus Rhipicephalus (Acari, Ixodidae): a guide to the brown ticks of the world. Cambridge: Cambridge University Press; 2005.
  20. Sambrook J, Russell DW. Molecular cloning: a laboratory manual. New York: Cold Spring Harbor Laboratory Press; 2001. pp. 23–44.
  21. Sangioni LA, Horta MC, Vianna MC, Gennari SM, Soares RM, Galvão MA, Schumaker TT, Ferreira F, Vidotto O, Labruna MB. Rickettsial infection in animals and Brazilian spotted fever endemicity.. Emerg Infect Dis 2005 Feb;11(2):265-70.
    doi: 10.3201/eid1102.040656pmc: PMC3320454pubmed: 15752445google scholar: lookup
  22. Mangold AJ, Bargues MD, Mas-Coma S. Mitochondrial 16S rDNA sequences and phylogenetic relationships of species of Rhipicephalus and other tick genera among Metastriata (Acari: Ixodidae).. Parasitol Res 1998 Jun;84(6):478-84.
    doi: 10.1007/s004360050433pubmed: 9660138google scholar: lookup
  23. Regnery RL, Spruill CL, Plikaytis BD. Genotypic identification of rickettsiae and estimation of intraspecies sequence divergence for portions of two rickettsial genes.. J Bacteriol 1991 Mar;173(5):1576-89.
    doi: 10.1128/jb.173.5.1576-1589.1991pmc: PMC207306pubmed: 1671856google scholar: lookup
  24. Roux V, Fournier PE, Raoult D. Differentiation of spotted fever group rickettsiae by sequencing and analysis of restriction fragment length polymorphism of PCR-amplified DNA of the gene encoding the protein rOmpA.. J Clin Microbiol 1996 Sep;34(9):2058-65.
    doi: 10.1128/jcm.34.9.2058-2065.1996pmc: PMC229190pubmed: 8862558google scholar: lookup
  25. 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.
    doi: 10.1016/S0022-2836(05)80360-2pubmed: 2231712google scholar: lookup
  26. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.. Nucleic Acids Res 1994 Nov 11;22(22):4673-80.
    doi: 10.1093/nar/22.22.4673pmc: PMC308517pubmed: 7984417google scholar: lookup
  27. Hall T, Biosciences I, Carlsbad C. BioEdit: an important software for molecular biology.. GERF Bull Biosci 2011;2:60–61.
  28. Nicholas KB. GeneDoc: analysis and visualization of genetic variation.. EMBNEW News 1997;4:14.
  29. 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/msy096pmc: PMC5967553pubmed: 29722887google scholar: lookup
  30. 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/mst197pmc: PMC3840312pubmed: 24132122google scholar: lookup
  31. Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees.. Bioinformatics 2001 Aug;17(8):754-5.
    doi: 10.1093/bioinformatics/17.8.754pubmed: 11524383google scholar: lookup
  32. 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.
    pubmed: 33225403doi: 10.1007/s00436-020-06981-0google scholar: lookup
  33. 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.
    pmc: PMC8170322pubmed: 34095277doi: 10.3389/fvets.2021.664731google scholar: lookup
  34. Swai ES, Mbise AN, Kessy V, Kaaya E, Sanka P, Loomu PM. Farm constraints, cattle disease perception and tick management practices in pastoral Maasai community-Ngorongoro.. Tanzania Livest Res Rural Dev 2005;17(2):17–20.
  35. Mooring MS, Benjamin JE, Harte CR, Herzog NB. Testing the interspecific body size principle in ungulates: the smaller they come, the harder they groom.. Anim Behav 2000 Jul;60(1):35-45.
    doi: 10.1006/anbe.2000.1461pubmed: 10924201google scholar: lookup
  36. Lorusso V, Picozzi K, de Bronsvoort BM, Majekodunmi A, Dongkum C, Balak G, Igweh A, Welburn SC. Ixodid ticks of traditionally managed cattle in central Nigeria: where Rhipicephalus (Boophilus) microplus does not dare (yet?).. Parasit Vectors 2013 Jun 7;6:171.
    doi: 10.1186/1756-3305-6-1pmc: PMC3681633pubmed: 23758913google scholar: lookup
  37. Kemal J, Tamerat N, Tuluka T. Infestation and Identification of Ixodid Tick in Cattle: The Case of Arbegona District, Southern Ethiopia.. J Vet Med 2016;2016:9618291.
    pmc: PMC5220475pubmed: 28105466doi: 10.1155/2016/9618291google scholar: lookup
  38. 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.2017.00506pmc: PMC5732177pubmed: 29322033google scholar: lookup
  39. Labruna MB, Kasai N, Ferreira F, Faccini JL, Gennari SM. Seasonal dynamics of ticks (Acari: Ixodidae) on horses in the state of São Paulo, Brazil.. Vet Parasitol 2002 Apr 19;105(1):65-77.
    doi: 10.1016/S0304-4017(01)00649-5pubmed: 11879967google scholar: lookup
  40. Greenfield BPJ. Environmental parameters affecting tick (Ixodes ricinus) distribution during the summer season in Richmond Park.. London Biosci Horiz 2011;4(2):140–148.
    doi: 10.1093/biohorizons/hzr016google scholar: lookup
  41. Gharbi M, Moussi N, Jedidi M, Mhadhbi M, Sassi L, Darghouth MA. Population dynamics of ticks infesting the one-humped camel (Camelus dromedarius) in central Tunisia.. Ticks Tick Borne Dis 2013 Dec;4(6):488-91.
    doi: 10.1016/j.ttbdis.2013.06.004pubmed: 23999226google scholar: lookup
  42. 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.
    doi: 10.1016/j.ympev.2014.03.017pubmed: 24685498google scholar: lookup
  43. Lv J, Wu S, Zhang Y, Chen Y, Feng C, Yuan X, Jia G, Deng J, Wang C, Wang Q, Mei L, Lin X. Assessment of four DNA fragments (COI, 16S rDNA, ITS2, 12S rDNA) for species identification of the Ixodida (Acari: Ixodida).. Parasit Vectors 2014 Mar 3;7:93.
    doi: 10.1186/1756-3305-7-93pmc: PMC3945964pubmed: 24589289google scholar: lookup
  44. 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.
    doi: 10.1186/s13071-014-0608-1pmc: PMC4482097pubmed: 26104478google scholar: lookup
  45. Ali A, Parizi LF, Ferreira BR, Junior V, Silva I. A revision of two distinct species of Rhipicephalus: R. microplus and R. australis.. Cienc Rural 2016;46:1240–1248.
    doi: 10.1590/0103-8478cr20151416google scholar: lookup
  46. Roy BC, Estrada-Peña A, Krücken J, Rehman A, Nijhof AM. Morphological and phylogenetic analyses of Rhipicephalus microplus ticks from Bangladesh, Pakistan and Myanmar.. Ticks Tick Borne Dis 2018 Jul;9(5):1069-1079.
    doi: 10.1016/j.ttbdis.2018.03.035pubmed: 29661691google scholar: lookup
  47. Eremeeva ME, Zambrano ML, Anaya L, Beati L, Karpathy SE, Santos-Silva MM, Salceda B, MacBeth D, Olguin H, Dasch GA, Aranda CA. Rickettsia rickettsii in Rhipicephalus ticks, Mexicali, Mexico.. J Med Entomol 2011 Mar;48(2):418-21.
    doi: 10.1603/ME10181pubmed: 21485383google scholar: lookup
  48. Abarca K, López J, Acosta-Jamett G, Martínez-Valdebenito C. Rickettsia felis in Rhipicephalus sanguineus from two distant Chilean cities.. Vector Borne Zoonotic Dis 2013 Aug;13(8):607-9.
    doi: 10.1089/vbz.2012.1201pubmed: 23659352google scholar: lookup
  49. Parola P, Paddock CD, Socolovschi C, Labruna MB, Mediannikov O, Kernif T, Abdad MY, Stenos J, Bitam I, Fournier PE, Raoult D. Update on tick-borne rickettsioses around the world: a geographic approach.. Clin Microbiol Rev 2013 Oct;26(4):657-702.
    doi: 10.1128/CMR.00032-13pmc: PMC3811236pubmed: 24092850google scholar: lookup
  50. Wei QQ, Guo LP, Wang AD, Mu LM, Zhang K, Chen CF, Zhang WJ, Wang YZ. The first detection of Rickettsia aeschlimannii and Rickettsia massiliae in Rhipicephalus turanicus ticks, in northwest China.. Parasit Vectors 2015 Dec 10;8:631.
    doi: 10.1186/s13071-014-0608-1pmc: PMC4675064pubmed: 26652857google scholar: lookup
  51. Ortuño A, Sanfeliu I, Nogueras MM, Pons I, López-Claessens S, Castellà J, Antón E, Segura F. Detection of Rickettsia massiliae/Bar29 and Rickettsia conorii in red foxes (Vulpes vulpes) and their Rhipicephalus sanguineus complex ticks.. Ticks Tick Borne Dis 2018 Mar;9(3):629-631.
    doi: 10.1016/j.ttbdis.2018.02.002pubmed: 29433817google scholar: lookup

Citations

This article has been cited 31 times.
  1. 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.
    doi: 10.3389/fmicb.2023.1229950pubmed: 37577446google scholar: lookup
  2. 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
  3. 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).
    doi: 10.3390/ani13091488pubmed: 37174525google scholar: lookup
  4. 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).
    doi: 10.3390/genes14020360pubmed: 36833287google scholar: lookup
  5. Lu M, Tian J, Wang W, Zhao H, Jiang H, Han J, Guo W, Li K. High diversity of Rickettsia spp., Anaplasma spp., and Ehrlichia spp. in ticks from Yunnan Province, Southwest China. Front Microbiol 2022;13:1008110.
    doi: 10.3389/fmicb.2022.1008110pubmed: 36312964google scholar: lookup
  6. 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
  7. 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
  8. 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
  9. 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
  10. 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).
    doi: 10.3390/ani12131708pubmed: 35804607google scholar: lookup
  11. 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
  12. 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
  13. Ullah S, Khan A, Cossío-Bayúgar R, Giantsis IA, Niaz S, Nasreen N, Rahim A, Mahamat OB, Khan A, Salamatullah AM. Molecular detection of Anaplasma Capra and Anaplasma marginale in Rhipicephalus microplus ticks infesting cows. Sci Rep 2025 Oct 2;15(1):34388.
    doi: 10.1038/s41598-025-17263-zpubmed: 41038925google scholar: lookup
  14. 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.
    doi: 10.3389/fvets.2024.1500930pubmed: 39764368google scholar: lookup
  15. 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
  16. Ullah S, Alouffi A, Khan M, Khan M, Tila H, Tanaka T, da Silva Vaz I Jr, Almutairi MM, Ali A. Molecular detection of Rickettsia aeschlimannii, Candidatus Rickettsia shennongii, Rickettsia sp. and Coxiella burnetii in ticks collected from camels. Sci Rep 2024 Sep 27;14(1):22129.
    doi: 10.1038/s41598-024-73663-7pubmed: 39333333google scholar: lookup
  17. 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.
    doi: 10.1186/s12917-024-04259-6pubmed: 39261829google scholar: lookup
  18. Li Y, Li J, Xieripu G, Rizk MA, Macalanda AMC, Gan L, Ren J, Mohanta UK, El-Sayed SAE, Chahan B, Xuan X, Guo Q. Molecular Detection of Theileria ovis, Anaplasma ovis, and Rickettsia spp. in Rhipicephalus turanicus and Hyalomma anatolicum Collected from Sheep in Southern Xinjiang, China. Pathogens 2024 Aug 11;13(8).
    doi: 10.3390/pathogens13080680pubmed: 39204280google scholar: lookup
  19. 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
  20. Qorbani A, Khalili M, Nourollahifard S, Mostafavi E, Farrokhnia M, Esmaeili S. Diversity of Rickettsia species in collected ticks from Southeast Iran. BMC Vet Res 2024 Jun 27;20(1):279.
    doi: 10.1186/s12917-024-04142-4pubmed: 38937767google scholar: lookup
  21. Jamil A, Yu Z, Wang Y, Xin Q, Gao S, Abdul Wahab M, Han X, Chen Z. Tick-borne Rickettsia, Anaplasma, Theileria, and enzootic nasal tumor virus in ruminant, PET, and poultry animals in Pakistan. Front Microbiol 2024;15:1359492.
    doi: 10.3389/fmicb.2024.1359492pubmed: 38596373google scholar: lookup
  22. 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
  23. Zeb I, Parizi LF, Israr M, da Silva Vaz I Jr, Ali A. Cross-species immunoprotective antigens (subolesin, ferritin 2 and P0) provide protection against Rhipicephalus sanguineus sensu lato. Parasit Vectors 2024 Jan 3;17(1):3.
    doi: 10.1186/s13071-023-06079-3pubmed: 38172894google scholar: lookup
  24. 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.
    doi: 10.3389/fmicb.2023.1283814pubmed: 38163073google scholar: lookup
  25. 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
  26. Numan M, Alouffi A, Almutairi MM, Tanaka T, Ahmed H, Akbar H, Rashid MI, Tsai KH, Ali A. First Detection of Theileria sinensis-like and Anaplasma capra in Ixodes kashmiricus: With Notes on cox1-Based Phylogenetic Position and New Locality Records. Animals (Basel) 2023 Oct 17;13(20).
    doi: 10.3390/ani13203232pubmed: 37893956google scholar: lookup
  27. 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).
    doi: 10.3390/vetsci10100628pubmed: 37888580google scholar: lookup
  28. 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
  29. 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.
    doi: 10.3389/fvets.2023.1246871pubmed: 37799410google scholar: lookup
  30. 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.
    doi: 10.3389/fvets.2023.1255482pubmed: 37789871google scholar: lookup
  31. Shehla S, Ullah F, Alouffi A, Almutairi MM, Khan Z, Tanaka T, Labruna MB, Tsai KH, Ali A. Association of SFG Rickettsia massiliae and Candidatus Rickettsia shennongii with Different Hard Ticks Infesting Livestock Hosts. Pathogens 2023 Aug 24;12(9).
    doi: 10.3390/pathogens12091080pubmed: 37764888google scholar: lookup
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