Molecular Detection and Differentiation of Theileria lestoquardi, T. ovis and T. annulata in Blood of Goats and Ticks in Kermanshah Province, Iran
,
Abstract
Background: This study was carried out to identify Theileria spp. infections in goats and ticksin Kermanshah Province, western Iran from May–Sep 2015.
Methods: For differentiation of different Theileria spp. both blood and tick samples were examined by nested PCR-RFLP.
Results: Light microscopy of blood smears revealed Theileria spp. infection in 22 (5.5%), while 68 (17%) of blood samples were positive using nested PCR. Out of 68 positive samples, 85.3% (58/68) and 11.7% (8/68) were respectively positive for Theileria ovis and T. lestoquardi. Mixed infection was detected in 3% (2/68) cases. Overall, 420 ixodid ticks belong to seven different hard ticks species were collected from goats. Rhipicephalus turanicus 112 (26.7%), R. sanguineus 95 (22.6%), R. bursa, 91(21.7%), Hyalomma anatolicum, 55(13.1%), H. excavatum 27(6.4%), H. marginatum, 22(5.3%) and Dermacentor marginatus, 18(4.2%) were the main tick species infesting goats. The PCR products obtained from ticks were subjected to the differentiation of Theileria species. Respectively, 2 and 8 pools of H. marginatum and R. turanicus salivary glands were infected with T. ovis and T. lestoquardi. In addition, T. annulata and T. lestoquardi infection weredetected in three pools of H. anatolicum.
Conclusion: This is the first report of goats and collected ticks to Theileria spp infection in Iran. The results suggest that T. ovis has a higher prevalence than T. lestoquardi. It is also postulated H. marginatum, R. turanicus and H. anatolicum might play an important role in the field as a vector of Theileria spp in this area.
1. Niu Q, Luo J, Guan G, Ma M, Liu Z, Liu A, Dang Z, Gao J, Ren Q, Li Y, Liu J, Yin H (2009) Detection and differenti-ation of ovine Theileria and Babesia by reverse line blotting in China. Para-sitol Res. 104: 1417–1423.
2. Yin H, Schnittger L, Luo JX, Ulrike Seit-zer, Ahmed J (2007) Ovine theileriosis in China: a new look at an old story. Parasitol Res. 101: 191–195.
3. Hashemi-Fesharaki R (1997) Tick-borne diseases of sheep and goats and their related vectors in Iran. Parasitol. 39: 115–117.
4. Zaeemi M, Haddadzadeh H, Khazraiinia P, Kazemi B, Bandehpou M (2011) Identification of different Theileria species (Theileria lestoquardi, Theil-eria ovis, and Theileria annulata) in naturally infected sheep using nested PCR-RFLP. Parasitol Res. 108: 837–843.
5. Tavassoli M, Tabatabaei M, Mohammadi M, Esmaeilnejad B, Mohamadpour H (2011) PCR-based detection of Babe-sia spp. infection in collected ticks from cattle in west and north-west of Iran. J Arthropod Borne Dis. 7: 132–138.
6. Telmadarraiy Z, Oshaghi MA, Hosseini- Vasoukolaei N, Yaghoobi Ershadi MR, Babamahmoudi F, Mohtarami F (2012) First molecular detection of Theileria ovis in Rhipicephalus san-guineus tick in Iran. Asian Pac J Trop Med. 5: 29–32.
7. Taha KM, Elhussein AM (2010) Experi-mental transmission of Theileria lestoquardi by developmental stages of Hyalomma anatolicum ticks. Parasi-tol Res. 107: 1009–1012.
8. Aktas M (2014) A survey of ixodid tick species and molecular identification of tick-borne pathogens. Vet Parasitol. 200: 276–283.
9. Shayan P, Rahbari S (2005) Simultaneous differentiation between Theileria spp. and Babesia spp. on stained blood smear using PCR. Parasitol Res. 97: 281–286.
10. Altay K, Dumanli N, Aktas M (2007) Molecular identification, genetic di-versity and distribution of Theileria and Babesia species infecting small rumi-nants. Vet Parasitol. 147: 161–165.
11. Heidarpour-Bami M, Khazraiinia P, Haddadzadeh HR, Kazemi B (2010) Identification of Theileria species in sheep in the eastern half of Iran using nest-ed PCR-RFLP and microscopic tech-niques. Iranian J Vet Res. 11: 262–266.
12. Razmi GR, Hossieni M, Aslani MR (2003) Identification of vector ticks of ovine theileriosis in an endemic region of Iran. Vet Parasitol. 116: 1–6.
13. Rashidi A, Razmi G (2013) Molecular detection of Theileria spp. in sheep and vector ticks in the North Khorasan Province, Iran. Trop Anim Health Prod. 45: 299–303.
14. Razmi G, Yaghfoori S (2013) Molecular surveillance of Theileria ovis, Theil-eria lestoquardi and Theileria annula-ta infection in sheep and ixodid ticks in Iran. Onderstepoort J Vet Res. 80: 635.
15. Hegab AA, Fahmy MM, Mahdy OA, Wahba AA (2016) Parasitological and molecular identification of Theileria Spe-cies by PCR-RFLP Method in Sheep, Egypt. Int J Adv Res Biol Sci. 3: 48–55.
16. Esmaeilnejad B, Tavassoli M, Asri-Rezaei S, Dalir-Naghadeh B, Mardani K, Golabi M, Arjmand J, Kazemnia A, Jalilzadeh G (2015) Determination of prevalence and risk factors of infection with Babesia ovis in small ruminants from West Azerbaijan Province, Iran by Polymer-ase Chain Reaction. J Arthropod Borne Dis. 9: 246–248.
17. Walker AR, Bouattour A, Camicas JL, Estrand-Perna A, Horak IG, Latif AA, Pegram RG, Preston MM (2003) Ticks of domestic animals in Africa: A guide to identification of species. Bio-science Reports, Edinburgh Scotland, U.K. Available at: http://www.alanrwalker.com/assets/PDF/tickguide-africa.pdf
18. Estrada-Pena A, Bouattour A, Camicas JL, Walker AR (2004) Ticks of do-mestic animals in the Mediterranean region: a guide to identification of species. University of Zaragoza, Spain.
19. Alsaad KM, Al-obaidi QT, Esmaeel SA (2009) Hematological and biochemi-cal study on the effect some common blood parasites in native goats in Mo-sul area. Vet Med Mosul. 23: 101–106.
20. Zangana IK, Naqid IA (2011) Prevalence of piroplasmosis (Theileriosis and Babesi-osis) among goats in Duhok Governorate. Al-Anbar J Vet Sci. 4: 50–57.
21. Altay K, Aktas M, Dumanli N (2007) Theil-eria infections in small ruminants in the East and Southeast Anatolia. Tü-rkiye Parazitol Derg. 31: 268–271.
22. Sayin K, Nalbantoğlu S, Yukari BA, Cakmak A, Zafer Karaer Z (2009) Epi-demiological studies on sheep and goat Theileria infection. Ankara. Univ Vet Fak Derg. 56: 127–129.
23. Aydin MF, Aktas M, Dumanli N (2013) Molecular identification of Theileria and Babesia in sheep and goats in the Black Sea region in Turkey. Parasitol Res. 112: 2817–2824.
24. Irshad MN, Qayyum M, Hussain QM, Qasim Khan M (2010) Prevalence of tick infestation and Theileriosis in sheep and
goats. Pak Vet J. 30: 178–180.
25. Alessandra T, Santo C (2012) Tick-borne diseases in sheep and goats: Clinical and diagnostic aspects. Small Rum Res. 106: 6–11.
26. Aghamohammad Hassan M, Raoofi A, Lotfollahzadeh S, Javanbakht J (2015) Clinical and cytological characteris-tics and prognostic implications on sheep and goat Theileria infection in north of Iran. J Parasit Dis. 39: 190–193.
27. Hoosmand-Rad P, Hawa NY (1973) Ma-lignant theileriosis of sheep and goats. Trop Anim Health Prod. 5: 97–102.
28. Kirvar E, Ilhan T, Katzer F, Wilkie G, Hooshmand-Rad P, Brown CGD (1998) Detection of Theileria lestoquardi (hirci) in ticks, sheep and goats using the polymerase chain reac-tion. Annals New York. Sci. 29: 52–62.
29. Schnittger L, Yin H, Qi B, Gubbels MJ, Beyer D, Niemann S, Jongejan F, Ah-med JS (2004) Simultaneously detec-tion and differentiation of Theileria and Babesia parasite infection in small ru-minants by reverse line blotting. Par-asitol Res. 92: 189–196.
30. Latif BMA, Hawa NJ, Bakir FA (1997) Incidence of malignant theileriosis (Theil-eria hirci) of sheep in Iraq. Iraq J Vet Med. 1: 29–37.
31. Al-Amery M, Hasso SA (2002) Labora-tory diagnosis of novel species of Theileria hirci, Eimeria caprovina and Eimeria pallid in goats in Iraq. Small Rum Res. 44: 163–166.
32. Morel P (1989) Tick-borne diseases of live-stock in Africa. In: Fischer M, Ralph S (Eds.), Manual of Tropical Veterinary Parasitology. CAB International, Wallingford, p. 473.
33. Bell-Sakyi L, Koney EBM, Dogbey O, Walker AR (2004) Incidence and prev-alence of tick-borne haemoparasites in domestic ruminants in Ghana. Vet Par-asitol. 124: 25–42.
34. Dhaim YA, A'aiz NN (2014) Prevalence of theileriosis in sheep in Wasit prov-ince ALQadisiya. J Vet Med Sci. 13: 14–18.
35. Sappenfield E, Jamieson DJ, Kourtis AP (2013) Pregnancy and Susceptibility to Infectious Diseases. Infect Dis Obstet Gyneco. 2013: 1–8.
36. Redman IGH, El Kelesh EA (2009) Iden-tification Theileria species in sheep and goats by the polymerase chain re-action (PCR). Vet Med J. 1: 460–473.
37. Inci A, İCA A, Yildirim A, Onder Duzlu O (2010) Identification of Babesia and Theileria species in small ruminants in Central Anatolia (Turkey) via re-verse line blotting. Turk J Vet Anim Sci. 34: 205–210.
38. Alyasino Y, Greiner M (1999) Serosur-vey on theileriosis in Awassi sheepin Syria. Vet Parasitol. 81: 275–280.
39. M’ghirbi Y, Ros-García A, Iribar P, Rhaim A, Hurtado A, Bouattour A (2013) A molecular study of tick-borne haemoprotozoan parasites (Theileria and Babesia) in small ruminants in Northern Tunisia. Vet Parasitol. 198: 72–77.
40. Omer OH (2012) Note on life cycle of Hyalomma anatolicum anatolicum (Acar: Ixodidae) on rabbit, and goats. J Agri-cul Vet Sci. 5: 53–57.
41. Haddadzadeh HR, Rahbari S, Khazraiinia P, Nabian S (2004) New concept on limiting factors of ovine and caprine malig-nantn Theileriosis. Iran J Vet Res. 5: 43–46.
42. Ghashgai O, Yakhchali M, Sohrabi S (2015) PCR-RELP for detecting of Theil-eria annulata infection in cattle and Hyalomma species in Kermanshah Province, Iran. Archiv Razi Instit. 70: 7–12.
43. Brown CG, Ilhan T, Kirvar E, Thomas M, Wilkie G, Leemans I, Leemans I, Hooshmand-Rad P (1998) Theileria lestoquardi and T. annulata in cattle, sheep and goats. Ann New Acad Sci. 29: 44–51.
44. Sohrabi S, Yakhchali M, Ghashghai O (2013) Hard ticks (Acarina: Ixodidae) diversity in the natural habitat of Ira-nian domestic ruminants: A provincial study in Kermanshah. J Vet Res. 68: 39–46.
45. Hasson RH, Al-Zubaidi HH (2012) Sheep and goats tick's infestation in Wasit's districts. Proceeding of the Eleventh Veterinary Scientific Confer-ence, pp. 299–305.
46. Shabestari BA, Davoodi J (2010) Study on goats tick fauna and seasonal varia-tions of tick population in Zanjan Province. J Azad Uni Garmsar. 5: 135–140.
47. Abdigoudarzi M (2013) Detection of naturally infected vectors ticks (Acari: Ixidiadae) by different species of Babesia and Theileria agents from three different enzootic parts of Iran. J Arthropod Borne Dis. 7: 164–172.
48. Aydin MF, Aktas M, Dumanli N (2015) Molecular identification of Theileria and Babesia in ticks collected from sheep and goats in the Black Sea region of Turkey. Parasitol Res. 114: 65–69.
49. Shayan P, Hooshmand E, Rahbari S, Na-bian S (2007) Determination of Rhipicephalus spp. as vectors for Babesia ovis in Iran. Parasitol Res. 101: 1029–1033.
50. Young AS, Leitch BL, Staff DA, Dolan TA (1983) Identification of Theileria in-fection in living salivary glands of ticks. Parasitol. 86: 519–528.
2. Yin H, Schnittger L, Luo JX, Ulrike Seit-zer, Ahmed J (2007) Ovine theileriosis in China: a new look at an old story. Parasitol Res. 101: 191–195.
3. Hashemi-Fesharaki R (1997) Tick-borne diseases of sheep and goats and their related vectors in Iran. Parasitol. 39: 115–117.
4. Zaeemi M, Haddadzadeh H, Khazraiinia P, Kazemi B, Bandehpou M (2011) Identification of different Theileria species (Theileria lestoquardi, Theil-eria ovis, and Theileria annulata) in naturally infected sheep using nested PCR-RFLP. Parasitol Res. 108: 837–843.
5. Tavassoli M, Tabatabaei M, Mohammadi M, Esmaeilnejad B, Mohamadpour H (2011) PCR-based detection of Babe-sia spp. infection in collected ticks from cattle in west and north-west of Iran. J Arthropod Borne Dis. 7: 132–138.
6. Telmadarraiy Z, Oshaghi MA, Hosseini- Vasoukolaei N, Yaghoobi Ershadi MR, Babamahmoudi F, Mohtarami F (2012) First molecular detection of Theileria ovis in Rhipicephalus san-guineus tick in Iran. Asian Pac J Trop Med. 5: 29–32.
7. Taha KM, Elhussein AM (2010) Experi-mental transmission of Theileria lestoquardi by developmental stages of Hyalomma anatolicum ticks. Parasi-tol Res. 107: 1009–1012.
8. Aktas M (2014) A survey of ixodid tick species and molecular identification of tick-borne pathogens. Vet Parasitol. 200: 276–283.
9. Shayan P, Rahbari S (2005) Simultaneous differentiation between Theileria spp. and Babesia spp. on stained blood smear using PCR. Parasitol Res. 97: 281–286.
10. Altay K, Dumanli N, Aktas M (2007) Molecular identification, genetic di-versity and distribution of Theileria and Babesia species infecting small rumi-nants. Vet Parasitol. 147: 161–165.
11. Heidarpour-Bami M, Khazraiinia P, Haddadzadeh HR, Kazemi B (2010) Identification of Theileria species in sheep in the eastern half of Iran using nest-ed PCR-RFLP and microscopic tech-niques. Iranian J Vet Res. 11: 262–266.
12. Razmi GR, Hossieni M, Aslani MR (2003) Identification of vector ticks of ovine theileriosis in an endemic region of Iran. Vet Parasitol. 116: 1–6.
13. Rashidi A, Razmi G (2013) Molecular detection of Theileria spp. in sheep and vector ticks in the North Khorasan Province, Iran. Trop Anim Health Prod. 45: 299–303.
14. Razmi G, Yaghfoori S (2013) Molecular surveillance of Theileria ovis, Theil-eria lestoquardi and Theileria annula-ta infection in sheep and ixodid ticks in Iran. Onderstepoort J Vet Res. 80: 635.
15. Hegab AA, Fahmy MM, Mahdy OA, Wahba AA (2016) Parasitological and molecular identification of Theileria Spe-cies by PCR-RFLP Method in Sheep, Egypt. Int J Adv Res Biol Sci. 3: 48–55.
16. Esmaeilnejad B, Tavassoli M, Asri-Rezaei S, Dalir-Naghadeh B, Mardani K, Golabi M, Arjmand J, Kazemnia A, Jalilzadeh G (2015) Determination of prevalence and risk factors of infection with Babesia ovis in small ruminants from West Azerbaijan Province, Iran by Polymer-ase Chain Reaction. J Arthropod Borne Dis. 9: 246–248.
17. Walker AR, Bouattour A, Camicas JL, Estrand-Perna A, Horak IG, Latif AA, Pegram RG, Preston MM (2003) Ticks of domestic animals in Africa: A guide to identification of species. Bio-science Reports, Edinburgh Scotland, U.K. Available at: http://www.alanrwalker.com/assets/PDF/tickguide-africa.pdf
18. Estrada-Pena A, Bouattour A, Camicas JL, Walker AR (2004) Ticks of do-mestic animals in the Mediterranean region: a guide to identification of species. University of Zaragoza, Spain.
19. Alsaad KM, Al-obaidi QT, Esmaeel SA (2009) Hematological and biochemi-cal study on the effect some common blood parasites in native goats in Mo-sul area. Vet Med Mosul. 23: 101–106.
20. Zangana IK, Naqid IA (2011) Prevalence of piroplasmosis (Theileriosis and Babesi-osis) among goats in Duhok Governorate. Al-Anbar J Vet Sci. 4: 50–57.
21. Altay K, Aktas M, Dumanli N (2007) Theil-eria infections in small ruminants in the East and Southeast Anatolia. Tü-rkiye Parazitol Derg. 31: 268–271.
22. Sayin K, Nalbantoğlu S, Yukari BA, Cakmak A, Zafer Karaer Z (2009) Epi-demiological studies on sheep and goat Theileria infection. Ankara. Univ Vet Fak Derg. 56: 127–129.
23. Aydin MF, Aktas M, Dumanli N (2013) Molecular identification of Theileria and Babesia in sheep and goats in the Black Sea region in Turkey. Parasitol Res. 112: 2817–2824.
24. Irshad MN, Qayyum M, Hussain QM, Qasim Khan M (2010) Prevalence of tick infestation and Theileriosis in sheep and
goats. Pak Vet J. 30: 178–180.
25. Alessandra T, Santo C (2012) Tick-borne diseases in sheep and goats: Clinical and diagnostic aspects. Small Rum Res. 106: 6–11.
26. Aghamohammad Hassan M, Raoofi A, Lotfollahzadeh S, Javanbakht J (2015) Clinical and cytological characteris-tics and prognostic implications on sheep and goat Theileria infection in north of Iran. J Parasit Dis. 39: 190–193.
27. Hoosmand-Rad P, Hawa NY (1973) Ma-lignant theileriosis of sheep and goats. Trop Anim Health Prod. 5: 97–102.
28. Kirvar E, Ilhan T, Katzer F, Wilkie G, Hooshmand-Rad P, Brown CGD (1998) Detection of Theileria lestoquardi (hirci) in ticks, sheep and goats using the polymerase chain reac-tion. Annals New York. Sci. 29: 52–62.
29. Schnittger L, Yin H, Qi B, Gubbels MJ, Beyer D, Niemann S, Jongejan F, Ah-med JS (2004) Simultaneously detec-tion and differentiation of Theileria and Babesia parasite infection in small ru-minants by reverse line blotting. Par-asitol Res. 92: 189–196.
30. Latif BMA, Hawa NJ, Bakir FA (1997) Incidence of malignant theileriosis (Theil-eria hirci) of sheep in Iraq. Iraq J Vet Med. 1: 29–37.
31. Al-Amery M, Hasso SA (2002) Labora-tory diagnosis of novel species of Theileria hirci, Eimeria caprovina and Eimeria pallid in goats in Iraq. Small Rum Res. 44: 163–166.
32. Morel P (1989) Tick-borne diseases of live-stock in Africa. In: Fischer M, Ralph S (Eds.), Manual of Tropical Veterinary Parasitology. CAB International, Wallingford, p. 473.
33. Bell-Sakyi L, Koney EBM, Dogbey O, Walker AR (2004) Incidence and prev-alence of tick-borne haemoparasites in domestic ruminants in Ghana. Vet Par-asitol. 124: 25–42.
34. Dhaim YA, A'aiz NN (2014) Prevalence of theileriosis in sheep in Wasit prov-ince ALQadisiya. J Vet Med Sci. 13: 14–18.
35. Sappenfield E, Jamieson DJ, Kourtis AP (2013) Pregnancy and Susceptibility to Infectious Diseases. Infect Dis Obstet Gyneco. 2013: 1–8.
36. Redman IGH, El Kelesh EA (2009) Iden-tification Theileria species in sheep and goats by the polymerase chain re-action (PCR). Vet Med J. 1: 460–473.
37. Inci A, İCA A, Yildirim A, Onder Duzlu O (2010) Identification of Babesia and Theileria species in small ruminants in Central Anatolia (Turkey) via re-verse line blotting. Turk J Vet Anim Sci. 34: 205–210.
38. Alyasino Y, Greiner M (1999) Serosur-vey on theileriosis in Awassi sheepin Syria. Vet Parasitol. 81: 275–280.
39. M’ghirbi Y, Ros-García A, Iribar P, Rhaim A, Hurtado A, Bouattour A (2013) A molecular study of tick-borne haemoprotozoan parasites (Theileria and Babesia) in small ruminants in Northern Tunisia. Vet Parasitol. 198: 72–77.
40. Omer OH (2012) Note on life cycle of Hyalomma anatolicum anatolicum (Acar: Ixodidae) on rabbit, and goats. J Agri-cul Vet Sci. 5: 53–57.
41. Haddadzadeh HR, Rahbari S, Khazraiinia P, Nabian S (2004) New concept on limiting factors of ovine and caprine malig-nantn Theileriosis. Iran J Vet Res. 5: 43–46.
42. Ghashgai O, Yakhchali M, Sohrabi S (2015) PCR-RELP for detecting of Theil-eria annulata infection in cattle and Hyalomma species in Kermanshah Province, Iran. Archiv Razi Instit. 70: 7–12.
43. Brown CG, Ilhan T, Kirvar E, Thomas M, Wilkie G, Leemans I, Leemans I, Hooshmand-Rad P (1998) Theileria lestoquardi and T. annulata in cattle, sheep and goats. Ann New Acad Sci. 29: 44–51.
44. Sohrabi S, Yakhchali M, Ghashghai O (2013) Hard ticks (Acarina: Ixodidae) diversity in the natural habitat of Ira-nian domestic ruminants: A provincial study in Kermanshah. J Vet Res. 68: 39–46.
45. Hasson RH, Al-Zubaidi HH (2012) Sheep and goats tick's infestation in Wasit's districts. Proceeding of the Eleventh Veterinary Scientific Confer-ence, pp. 299–305.
46. Shabestari BA, Davoodi J (2010) Study on goats tick fauna and seasonal varia-tions of tick population in Zanjan Province. J Azad Uni Garmsar. 5: 135–140.
47. Abdigoudarzi M (2013) Detection of naturally infected vectors ticks (Acari: Ixidiadae) by different species of Babesia and Theileria agents from three different enzootic parts of Iran. J Arthropod Borne Dis. 7: 164–172.
48. Aydin MF, Aktas M, Dumanli N (2015) Molecular identification of Theileria and Babesia in ticks collected from sheep and goats in the Black Sea region of Turkey. Parasitol Res. 114: 65–69.
49. Shayan P, Hooshmand E, Rahbari S, Na-bian S (2007) Determination of Rhipicephalus spp. as vectors for Babesia ovis in Iran. Parasitol Res. 101: 1029–1033.
50. Young AS, Leitch BL, Staff DA, Dolan TA (1983) Identification of Theileria in-fection in living salivary glands of ticks. Parasitol. 86: 519–528.
| Files | ||
| Issue | Vol 13 No 3 (2019) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v13i3.1539 | |
| Keywords | ||
| Theileria; Tick; Goat; Nested PCR-RFLP; Iran | ||
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How to Cite
1.
Rahmani-Varmale M, Tavassoli M, Esmaeilnejad B. Molecular Detection and Differentiation of Theileria lestoquardi, T. ovis and T. annulata in Blood of Goats and Ticks in Kermanshah Province, Iran. J Arthropod Borne Dis. 2019;13(3):297-309.
