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Prevalence, epidemiology, seasonality, and phylogeny of Anaplasma marginale in blood samples of goats collected from Punjab, Pakistan

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Abstract

Purpose

In Pakistan, a major constrain to goat farming is the tick and tick-borne diseases that results in financial losses to livestock farmers. This study was conducted to report the molecular prevalence of Anaplasma (A.) marginale in goat blood samples collected during four seasons from Khanewal district in Punjab (Pakistan).

Methods and results

The mps1 gene of A. marginale was targeted in 900 blood samples that were collected on seasonal basis (n = 225 per season) and 6.6% (61/900) goats were found positive with A. marginale. Anaplasma marginale positive PCR products were sequenced and submitted to the GenBank. Prevalence of A. marginale varied with sampling season (P = 0.002) and it was highest in the summer (11.5%) followed by the autumn (7.6%), spring (5.3%), and winter seasons (2.7%) respectively. Anaplasma marginale prevalence varied significantly between goat breeds during the autumn (p = 0.01) and summer seasons (p = 0.02). Goats more than 2 years old and livestock farms where only goats were kept and dogs were associated with herds were risk factors for ovine anaplasmosis during different seasons. White and red blood cell counts and parameters associated with their counts were affected in A. marginale infected goats while studied serum parameters remained unaffected.

Conclusion

PCR is a reliable tool for the detection of A. marginale in goat blood samples. A relatively low prevalence of A. marginale in goats of Khanewal district was observed and the parasite prevalence in goats was higher in the summer (May until September) and autumn (October and November) seasons. Control measures are required to prevent tick-borne diseases in ruminants from Pakistan.

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Data availability

All the epidemiological data associated with this project are presented in this manuscript.

References

  • Abid K, Bukhari S, Asif M, Sattar A, Arshad M, Aktas M, Ozubek S, Shaikh RS, Iqbal F (2021) Molecular detection and prevalence of Theileria ovis and Anaplasma marginale in sheep blood samples collected from district Layyah in Punjab Pakistan. Trop Anim Health Prod https://doi.org/10.1007/s11250-021-02870-5

    Article  PubMed  Google Scholar 

  • Abubakar M, Manzoor S and Ali Q (2015) Evaluating the role of vaccine to combat peste des petits ruminants outbreak in endemic disease situation. J Anim Sci Technol 57:2-7.

    Article  Google Scholar 

  • Akhter G, Hasan M (2016) Determination of aquifer parameters using geoelectrical sounding and pumping test data in Khanewal District, Pakistan. Open Geosci 8(1):630-638.

    Google Scholar 

  • Ameen KAH, Abdullah BA, Abdul-Razaq RA (2012) Seroprevalence of Babesia bigemina and Anaplasma marginale in domestic animals in Erbil, Iraq. Iraqi J Vet Sci 26(3):109-114.

    Article  Google Scholar 

  • Asif M, Parveen A, Ashraf S, Hussain M, Aktas M, Ozubek S, Shaikh RS, Iqbal F (2019) First report regarding the simultaneous molecular detection of Anaplasma marginale and Theileria annulata in equine blood samples collected from Southern Punjab in Pakistan. Acta Parasitol 65:259-263

    Article  Google Scholar 

  • Atif FA (2015) Anaplasma marginale and Anaplasma phagocytophilum: Rickettsiales pathogens of veterinary and public health significance. Parasitol Res 114(11):3941-3957.

    Article  Google Scholar 

  • Ahmadi-Hamedani M, Khaki Z, Rahbari S, Kazemi B, Bandehpour M (2009) Molecular identification of anaplasmosis in goats using a new PCR- RFLP method. Iran J Vet Res 10:367-372.

    Google Scholar 

  • Alessandra T, Santo C (2012) Tick-borne diseases in sheep and goats: Clinical and diagnostic aspects. Small Rumin Res106:S6–S11.

    Article  Google Scholar 

  • Ashraf S, Parveen A, Awais M.M, Gillani Q, Aktas M, Ozubek S, Iqbal F (2021) A Report on molecular detection and phylogenetic evaluation of Anaplasma marginale in ticks and blood samples collected from cattle in district Layyah in Punjab (Pakistan). Curr Microbiol 78(1):274-28.

    Article  CAS  Google Scholar 

  • Boyazoglu J, Hatziminaoglou I, Morand-Fehr P (2005) The role of the goat in society: Past, present and perspectives for the future. Small Rumin Res 60(1-2):13-23.

    Article  Google Scholar 

  • Coskun A, Ekici OD, Guzelbektes H, Aydogdu U, Sen I (2012) Acute phase proteins, clinical, hematological and biochemical parameters in dairy cows naturally infected with Anaplasma marginale. Kafkas Univ Vet Fak Derg 18(3):497–502.

    Google Scholar 

  • De la Fuente J, Atkinson MW, Naranjo V, de Mera, IGF, Mangold AJ, Keating KA, Kocan KM (2007) Sequence analysis of the msp4 gene of Anaplasma ovis strains. Vet Microbiol 119:375–381.

    Article  Google Scholar 

  • Escareno L, Salinas-González H, Wurzinger M, Iñiguez L, Solkner J, Meza-Herrera C (2012) Dairy goat production systems. Tropi Anim Health Prod 45:17-34.

    Article  Google Scholar 

  • Ghaffar A, Ijaz M, Ali A, Farooqi SH, Rehman A, Ali MM, Zafar MZ, Naeem MA (2020) First report on molecular characterization of anaplasmosis in small ruminants in Pakistan. J Parasitol 106(3):360–368.

    Article  Google Scholar 

  • George N, Bhandari V, Sharma P (2017) Phylogenetic relationship and genotypic variability in Anaplasma marginale strains causing anaplasmosis in India. Infect Genet Evol 48:71-5.

    Article  Google Scholar 

  • Hussain M, Junaid A, Gul R, Jamal MA, Ahmed I, Talpur MZ, Rahim K, Fatima M, Munir S (2017) First detection on prevalence of Anaplasma marginale in sheep and goat in Karak District, Pakistan. Asian Pac J Trop Dis 7(9):531-535.

    Article  Google Scholar 

  • Iqbal A, Siddique F, Mahmood M.S, Shamim A, Zafar T, Rasheed I, Saleem I, Ahmad W (2014) Prevalence and impacts of ectoparasitic fauna infesting goats (Capra hircus) of district Toba Tek Singh, Punjab, Pakistan. Glob Vet 12:158–164.

    Google Scholar 

  • Jabbar A, Abbas T, Sandhu ZD, Saddiqi HA, Qamar MF, Gasser RB (2015) Tick-borne diseases of bovines in Pakistan: Major scope for future research and improved control. Para Vect 8:283.

    Article  Google Scholar 

  • Jukes TH, Cantor, CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian Protein Metabolism, Academic Press, New York, pp. 21-132.

    Chapter  Google Scholar 

  • Kashif M, Ahmad MS (2014) Seroprevalence of Anaplasma sp. In sheep (Ovis aries) by ELISA in Peshawar, Pakistan. Int J Curr Res 6(1):4502–04.

  • Khaki Z, Jalali SM, Kazemi B, Jalali MR, Yasini SP (2015) A study of hematological changes in sheep naturally infected with Anaplasma spp. and Theileria ovis: Molecular diagnosis. Iran J Vet Med 9(1):19–26.

  • Khan A, Nasreen N, Mitchell RD, Niaz S, Ayaz S, Khattak I, Naeem H, PérezdeLeón AA Zaman MA (2019) Seroprevalence of Anaplasma spp. among sheep and goats in Charsadda District, Pakistan. Small Rumin Res 165: 5-10.

    Article  Google Scholar 

  • Khan A, Khan MR, Tufail MG, Saleem MG, Masood S (2015) Pathogenesis of anaplasmosis in bulkhi sheep and their confirmation with polymerase chain reaction. Scholar’s Adv Anim Vet Res 2(2):107-114.

    Article  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2017) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger data sets. Mol Biol Evol 33:1870–1874.

    Article  Google Scholar 

  • Miranda EA, Han SW, Cho YK, Choi KS, Chae JS (2021) Co-Infection with Anaplasma species and novel genetic variants detected in cattle and goats in the republic of Korea. Path 10:28.

    CAS  Google Scholar 

  • Molad T, Mazuz ML, Fleiderovitz L, Fish L, Savitsky I, Krigel Y, Leibovitz B, Molloy J, Jongejan F, Shkap V (2006) Molecular and serological detection of A. centrale- and A. marginale-infected cattle grazing within an endemic area. Vet Microbiol 113(1–2): 55–62.

  • Mustafa I, Shabbir RMK, Subhani M, Ahmad I, Aleem R, Jamil S, Muqaddas H, Shabbir RG, Ghani A, Mahmood T (2014) Seasonal activity of tick infestation in goats and buffalo of Punjab province (district Sargodha), Pakistan. Kafkas Univ Vet Fak Derg 20:655–662.

    Google Scholar 

  • Nasreen A, Saeed K, Khan A, Niaz S, Akhtar N (2016) Sero-diagnosis and haematological effect of anaplasmosis in goats and sheep of district Mardan, Khyber Pakhtunkhwa, Pakistan. World J Zool 11(2):67-80.

    Google Scholar 

  • Parveen A, Ashraf S, Khan A, Asif M, Iqbal F. 2021. Epidemiology of Tick-Borne Diseases. In: Kumar S, Bayugar RC, Sharma AK, Miranda EM, Chaubey AK (eds) The Entomological Guide to Rhipicephalus. Nova Science Publishers, New York, USA.

  • Ramos RAN, Ramos CAN, Araújo FR, Melo ESP, Tembue ASM, Faustino MAG, Soares CO (2008) Detection of antibodies against Anaplasma sp. in small ruminants from the semi-arid region against Pernambuco State, Brazil. Rev Bras Parasitol Vet 17(2):115–7

  • Razmi GR, Dastjerdi K, Hossieni H, Naghibi A, Barati F, Aslan MR (2006) An epidemiological study on Anaplasma infection in cattle, sheep, and goats in Mashhad Suburb, Khorasan Province, Iran. Ann NY Acad Sci 1078:479–481.

    Article  CAS  Google Scholar 

  • da Silva NB, Taus NS, Johnson WS, Mira A, Schnittger L, Valente JDM, Vidotto O, Masterson HE, Vieira TSWJ, Ueti MW, Vieira RFC (2018) First report of Anaplasma marginale infection in goats, Brazil. PLOS ONEE. https://doi.org/10.1371/journal.pone.0202140

  • Tahir D, Meyer l, Fourie J, Jongejan F, Mather T, Choumet V, Blagburn B, Straubinger RK, Varloud M (2020) Interrupted blood feeding in ticks: causes and consequences. Microorg 8(6):910-917

    Article  CAS  Google Scholar 

  • Yasini S, Khaki Z, Rahbari S, Kazemi B, Amoli JS, Gharabaghi A, Jalali S (2012) Hematologic and clinical aspects of experimental ovine anaplasmosis caused by Anaplasma ovis in Iran. Iran J parasitol 7:91.

    PubMed  PubMed Central  Google Scholar 

  • Yousefi A, Rahbari S, Shayan P, Sadeghi-dehkordi Z, Bahonar A (2017) Molecular detection of Anaplasma marginale and Anaplasma ovis in sheep and goat in west highland pasture of Iran. Asia Pac J Trop Biomed 7(5):455-459.

    Article  Google Scholar 

  • Zhou M, Cao S, Sevinc F, Sevinc M, Ceylan O, Ekici S, Xuan X (2017) Molecular detection and genetic characterization of Babesia, Theileria and Anaplasma amongst apparently healthy sheep and goats in the central region of Turkey. Tick Tick Born Dis 8(2):246-52.

    Article  Google Scholar 

Download references

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Author notes

  1. Muhammad Naveed Aziz and Muhammad Irfan Equal contribution towards this manuscript

Authors and Affiliations

  1. Institute of Molecular Biology and Biotechnology, Bahauddin Zakariya University, Multan, 60800, Pakistan

    Muhammad Naveed Aziz, Muhammad Irfan, Muhammad Asif & Rana Khalid Iqbal

  2. Zoology Division, Institute of Pure and Applied Biology, Bahauddin Zakariya University, Multan, 60800, Pakistan

    Asia Parveen, Maryam Ijaz, Sadia Mumtaz & Furhan Iqbal

  3. Department of Parasitology, Veterinary Faculty, University of Firat, 23119, Elazig, Turkey

    Sezayi Ozubek & Munir Aktas

Authors
  1. Muhammad Naveed Aziz
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  2. Muhammad Irfan
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  3. Asia Parveen
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  4. Muhammad Asif
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  5. Maryam Ijaz
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  7. Sezayi Ozubek
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  8. Munir Aktas
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  9. Rana Khalid Iqbal
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  10. Furhan Iqbal
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Contributions

FI and RKI had designed and supervised this study. MNA, MI, and MA had collected blood and epidemiological data from goats. MNA, MI, and SM had extracted DNA from the blood samples and performed PCRs. AP had purified PCR products and analyzed DNA sequences. MA and SO had constructed phylogenetic trees and analyzed the data. All these authors contributed in manuscript writing and approved the final version of the manuscript.

Corresponding authors

Correspondence to Rana Khalid Iqbal or Furhan Iqbal.

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Ethics approval

Ethical Research Committee of the Institute of Molecular Biology and Biotechnology at Bahauddin Zakariya University Multan (Pakistan) approved all the experimental procedures and protocols applied in this study via letter number IMBB/Ethics/2018–47.

Consent to participate

Informed consent was obtained from livestock owners before including their animals in this study.

Conflict of interest

The authors declare no competing interests.

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Aziz, M.N., Irfan, M., Parveen, A. et al. Prevalence, epidemiology, seasonality, and phylogeny of Anaplasma marginale in blood samples of goats collected from Punjab, Pakistan. Trop Anim Health Prod 54, 74 (2022). https://doi.org/10.1007/s11250-022-03080-3

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