Araştırma Makalesi
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Irak'ın Nineveh Vilayetinde Köpek Kardiyak Dirofilariosis Prevalansı

Yıl 2022, Cilt: 17 Sayı: 1, 31 - 34, 29.04.2022

Öz

Kanin kardiyak dirofilariosis, Dirofilaria immitis'in neden olduğu parazitik zoonotik bir hastalıktır. Bu araştırma çalışması, Nineveh Vilayeti'nde (kuzeybatı Irak'ta) sokak ve polis köpeklerinde kardiyak dirofilariosisin hem mikrofilaremik (patent enfeksiyonu) hem de occult formlarının (amikrofilaremik form) prevalansını belirlemeyi amaçlamaktadır. Ekim 2021 - Ocak 2022 tarihleri arasında, 1-11 yaş arası (ortalama: 4,5 yaş) çoğu Belçika Malinois ve Alman Çoban ırkı olmak üzere 45 yerel sokak köpeği ve 45 polis köpeği dahil olmak üzere çeşitli ırklardan doksan köpeğin kanı, dolaşımdaki mikrofilaria'yı saptamak için wet mount, kan smearı acridine orange boyaması ve modifiye Knott testi ile mikroskobik olarak incelendi. Tüm numuneler, ayrıca occult kardiyak dirofilaryozlu köpekleri saptamak için ticari bir enzim bağlantılı immün emici tahlil kiti (Heartworm Ag ELISA kiti, Canine, DRG International Inc., ABD) ile test edildi. Toplam 49 örnek mikrofilaria pozitifti ve prevalans değeri %54.4 idi. İncelenen serumun %27.8'inde D.immitis antijenleri tespit edildi ve genel prevalansı %78.9 idi. Sokak köpekleri, Irak'ın Ninova Vilayeti'ndeki polis köpeklerine kıyasla hem mikrofilaremik hem de occult kardiyak dirofilariyoz formları için daha yüksek prevalans gösterdi. Modifiye Knott testi (Altın standart) ile wet mount, kan smearı acridine orange boyaması ve Cohen'in Kappa indeksi kullanılarak Ag ELISA arasındaki uyum, wet mount (0.030) için hafifti ve Ag ELISA (0,462) ve kan smearı acridine orange boyaması için önemliydi (0.607). Bu çalışmanın bulguları, Irak'ın Nineveh Vilayeti'ndeki köpeklerde (hem sokak hem de polis) kardiyak dirofilariosis prevalansı ve paterni için filogenetik bir analiz gerektiren kanıtlar sunmaktadır.

Kaynakça

  • 1. Atkins C. Overview of Heartworm Disease (Dirofilariasis), Review/Revision. The Merck Veterinary Manual. 2015. Available at www.merckvetmanual.com/mvm/ .
  • 2. Beugnet F, Halos L, Guillot J. Textbook of Clinical Parasitology in dogs and cats. Rhein. Boehringer Ingelheim. 2018; 123-131.
  • 3. Adebayo OO, Akande FA, Adenubi OT. Canine Dirofilariasis: A case report and review of the literature. Folia Veterinaria. 2020; 64(3):75-81. [Crossref]
  • 4. Chalifoux L, Hunt RD. Histochemical differentiation of dirofilaria immitis and dipetalonema reconditum. J. Am. Vet. Med. Assoc. 1971;(5):601–605.
  • 5. Ortega-Mora L.M., Gómez-Bautista M., Rojo-Vázquez F.A. The acid phosphatase activity and morphological characteristics of Dipetalonema dracunculoides (Cobbold, 1870) microfilariae. Vet. Parasitol. 1989; 33:187–190. [Crossref]
  • 6. Toparlak M, Gargili A, Esatgil M, Cetinkaya H. Canine Filariosis Around Istanbul, Turkey Employing Naphtol AS-TR Phosphatase technique. Acta Vet. Brno. 2005;74(2):233-237. [Crossref]
  • 7. Ferreira C, Afonso A, Calado M. Molecular characterization of Dirofilaria spp. circulating in Portugal. Parasit Vectors. 2017; 10(1):250. [Crossref]
  • 8. Hoch H, Strickland K. Canine and feline dirofilariasis: life cycle, pathophysiology, and diagnosis. Compend Contin Educ Vet. 2008;30(3):133-140; quiz 141.
  • 9. Henry LG, Brunson KJ, Walden HS, Wenzlow N, Beachboard S.E, Barr K.L., Long M.T. Comparison of six commercial antigen kits for detection of Dirofilaria immitis infections in canines with necropsy-confirmed heartworm status. Vet. Parasitol. 2018;254:178–182. [Crossref]
  • 10. Genchi M, Rinaldi L, Venco L, Cringoli G, Vismarra A, Kramer L. Dirofilaria immitis and D. repens in dog and cat: a questionnaire study in Italy. Vet. Parasitol. 2019;267:26-31. doi:10.1016/j.vetpar.2019.01.014. [Crossref]
  • 11. Anvari D, Elahe N, Ahmad D, Shahabeddin S, Mahmood M, Hezarjaribi Z, Reza M, Shirzad G. The global status of Dirofilaria immitis in dogs: a systematic review and meta-analysis based on published articles. Res Vet Sci. 2020;131:104–116. doi:10.1016/j.rvsc.2020.04.002. [Crossref]
  • 12. Selim A, Alanazi D, Sazmand A, Otranto D. Seroprevalence and associated risk factors for vector-borne pathogens in dogs from Egypt Abdelfattah. Parasit Vectors. 2021;14(1):175 https://doi.org/10.1186/s13071-021-04670-0. [Crossref]
  • 13. Yildiz K , Yasa D, Yagci BB, Öcal N, Gazyağci AN. Distribution of dirofilaria immitis in dogs in Kırıkkale. Turkish J Parasitol. 2008;32:225-228.
  • 14. Sarı BM , Taşkın G, Kılıç Y. Seroprevalence of dirofilaria immitis, ehrlichia canis and borrelia burgdorferi in dogs in Iğdır province, Turkey. Kafkas Univ Vet Fak Journal. 2013;19:735-739. [Crossref]
  • 15. Sarali H, Bilgic H, Bakirci S, Karagenc T. Prevalence of dirofilaria immitis infection in dogs from Aydin and Izmir Provinces, Turkey. Animal Health Prod and Hyg. 2020;9(2):711 – 715.
  • 16. Omar O, Elamin E, Omer S, Alagaili A, Mohammed O. Serorevalence of Dirofilaria immitis in dogs and cats in Riyadh City, Saudi Arabia, Trop Biomed. 2018;35(2): 531–540.
  • 17. Bamorovat M, Sharifi I, Fasihi Harandi M, Nasibi S, Sadeghi B, Khedri J, Mohammadi MA. Parasitological, serological and molecular study of dirofilariaimmitis in domestic dogs, southeastern Iran. Iran J. Parasitol. 2017;12:260-266.
  • 18. Amall HA. Seroepidemiological study of heartworm Dirofilaria immitis in Baghdad and Karbala provinces. Thesis of PhD. In veterinary medicine \ Parasitology.College of Veterinary Medicine. University of Baghdad / Iraq. 2010.
  • 19. Al-Salihi KA, Al-Dabhawi AH, Al-Rammahi HM, Kareem FA. Dirofilaria immitis infestation in imported police (K-9) dogs in Iraq: clinicopathological and molecular investigations study. Brazil J Vet Res Animal Sci. 2019;56(2):e152987. [Crossref]
  • 20. Alia YY, May HK, Amall HA. Serological study of dirophilaria immitis in human from some village in Al-Hindya part of Karbala governorate. Inter J Sci Natur. 2013;4 (1):185-188.
  • 21. AL-shabbani A. In Iraq, The First Application of Serological SNAP ELISA Technique In Detection of Canine Heartworms (Dirofilaria immitis) In Herder Dogs of Al-Qadisiyah and Dhi-Qar Provinces. Kufa J Vet Med Sci. 2016;7(1)B:192-198.
  • 22. Gary WL, Leland SR, John H. CrossRapid Diagnosis of Brugia malayi and Wuchereria bancrofti Filariasis by an Acridine orange/Microhematocrit Tube Technique. The Journal of Parasit. 1990;76( 2 ): 278-281. Stable URL: http://www.jstor.org/stable/3283035 . [Crossref]
  • 23. Rojas A, Rojas D, Montenegro VM, Baneth G. Detection of Dirofilaria immitis and other arthropod-borne filarioids by an HRM real-time qPCR, blood-concentrating techniques and a serological assay in dogs from Costa Rica. Parasit Vectors. 2015;8:170. [Crossref]
  • 24. Atkins C. Canine heartworm disease. In: Ettinger SJ, Feldman EC, eds. Textbook Vet Internal Med. 6th ed. St. Louis: Elsevier. 2005;1118-1136.
  • 25. Alobaidii W, Zaki Z, Hassan M. Detection of dirofilaria immitis antigen in cats in Mosul city. Iraqi J Vet Sci. 2022;36(1):57-60. [Crossref]
  • 26. Amall HA, Aleia YY. First document on the presence of Iraqi Dirofilaria immitis. Iraqi J Vet Med. 2009;33(1):183-186. [Crossref]
  • 27. Al Salihi KA, Al Zubaydi SQ, Katah, H. Gastrointestinal parasites infestation in military working dogs/ K9 in Al Muthanna Governorate in compare to semi housed dogs. Mirror Res Vet Sci Anim. 2017;6(2):25-38.
  • 28. Montarsi F, Ciocchetta S, Devine G, Ravagnan S, Mutinelli F, Frangipane di Regalbono A, Otranto D, Capelli G. Development of dirofilaria immitis within the mosquito Aedes (Finlaya) koreicus, a new invasive species for Europe. Parasit Vectors. 2015;8:177. [Crossref]
  • 29. Oi M, Yoshikawa S, Ichikawa Y, Nakagaki K, Matsumoto J, Nogami S. Prevalence of dirofilaria immitis among shelter dogs in Tokyo, Japan, after a decade: comparison of 1999-2001 and 2009-2011. Parasite. 2014;21(4):10. [Crossref]
  • 30. Mendoza-Roldan J, Benelli G, Panarese R, Iatta R, Furlanello T, Beugnet F, Zatelli A, Otranto D. leishmania infantum and dirofilaria immitis infections in Italy, 2009–2019: Changing distribution patterns. Parasit Vectors. 2020;13:193. [Crossref]
  • 31. Nguyen C, Koh WL, Casteriano, A. Mosquito-borne heartworm dirofilaria immitis in dogs from Australia. Parasit Vectors. 2016;9: 535. [Crossref]
  • 32. Coles EH. Vet Clin Pathol. 4th ed. Saunders Company, Philadelphia. 1986:203-240.
  • 33. Watanabe Y, Yang CH, Tung KC, Ooi HK. Comparison of microfilaria concentration method for Setaria digitata infection in cattle and for Dirofilaria immitis infection in dogs. J. Vet. Med. Sci. 2004;66: 543–545. [Crossref]
  • 34. Venco L, Genchi, C, Simón F. La filariosis cardiopulmonar (Dirofilaria immitis) en el perro. In La Filariosis en las Especies Domésticas y en el Hombre , Simón F, Genchi C, Venco L, Montoya MN, Eds.; Merial Laboratorios: Barcelona, Spain. 2011:19-60.
  • 35. Laidoudi Y, Ringot D, Watier-Grillot S, Davoust B, Mediannikov OA. Cardiac and subcutaneous canine dirofilariosis outbreak in a kennel in central France. Parasite. 2019;26:72. [Crossref]
  • 36. Ogbaje CI, Abel-Danjuma. Prevalence and risk factors associated with Dirofilaria immitis infection in dogs in Makurdi, Benue State, Nigeria. J Adv Vet Anim Res. 2016i,3(4): 338-344. [Crossref]
  • 37. Ranjbar-Bahadori S, Eslami A, Bokaic S. Evaluation of different methods for diagnosis of dirofilaria immitis. Pak J Biol Sci. 2007;10(11):1938–1940. [Crossref]

Prevalence of Canine Cardiac Dirofilariasis in Nineveh Governorate of Iraq

Yıl 2022, Cilt: 17 Sayı: 1, 31 - 34, 29.04.2022

Öz

Canine cardiac dirofilariasis is a parasitic zoonotic disease caused by Dirofilaria immitis. This research work is aimed to find out the prevalence of both a microfilaremic (patent infection) and occult forms (amicrofilaremic form) of cardiac dirofilariasis in stray and police dogs of Nineveh governorate (in northwestern Iraq). From October 2021 to January 2022, the blood of ninety dogs of various breeds, including 45 local breeds stray dogs and 45 police dogs, mostly of Belgian Malinois and German Shepherd breeds, with an age range of 1 to 11 years (median: 4.5 years), were examined microscopically by wet mount, acridine orange stained blood smears and modified Knott's test to detect circulating microfilaria. All the samples were further tested by a commercial antigen- enzyme-linked immune sorbent assays kit (Heartworm Ag ELISA kit, Canine, DRG International Inc., USA) in order to detect dogs with occult cardiac dirofilariasis. A total of 49 samples were microfilaria positive, giving a prevalence value of 54.4%. D.immitis antigens were detected in 27.8% of the examined sera, with an overall prevalence of 78.9%. Stray dogs showed a higher prevalence for both microfilaremia and occult forms of cardiac dirofilariasis compared to police dogs in Nineveh Governorate of Iraq. The agreement between the modified Knott's test (Gold standard) and wet mount, acridine orange stained blood smears, and Ag ELISA using Cohen’s Kappa index was light for the wet mount (0.030) and substantial for Ag ELISA(0.462), and acridine orange stained blood smears (0.607). The findings of the present study provide evidence for the prevalence and pattern of canine cardiac dirofilariosis in dogs (both stray and police) in Iraq’s Nineveh Governorate, requiring a phylogenetic analysis.

Kaynakça

  • 1. Atkins C. Overview of Heartworm Disease (Dirofilariasis), Review/Revision. The Merck Veterinary Manual. 2015. Available at www.merckvetmanual.com/mvm/ .
  • 2. Beugnet F, Halos L, Guillot J. Textbook of Clinical Parasitology in dogs and cats. Rhein. Boehringer Ingelheim. 2018; 123-131.
  • 3. Adebayo OO, Akande FA, Adenubi OT. Canine Dirofilariasis: A case report and review of the literature. Folia Veterinaria. 2020; 64(3):75-81. [Crossref]
  • 4. Chalifoux L, Hunt RD. Histochemical differentiation of dirofilaria immitis and dipetalonema reconditum. J. Am. Vet. Med. Assoc. 1971;(5):601–605.
  • 5. Ortega-Mora L.M., Gómez-Bautista M., Rojo-Vázquez F.A. The acid phosphatase activity and morphological characteristics of Dipetalonema dracunculoides (Cobbold, 1870) microfilariae. Vet. Parasitol. 1989; 33:187–190. [Crossref]
  • 6. Toparlak M, Gargili A, Esatgil M, Cetinkaya H. Canine Filariosis Around Istanbul, Turkey Employing Naphtol AS-TR Phosphatase technique. Acta Vet. Brno. 2005;74(2):233-237. [Crossref]
  • 7. Ferreira C, Afonso A, Calado M. Molecular characterization of Dirofilaria spp. circulating in Portugal. Parasit Vectors. 2017; 10(1):250. [Crossref]
  • 8. Hoch H, Strickland K. Canine and feline dirofilariasis: life cycle, pathophysiology, and diagnosis. Compend Contin Educ Vet. 2008;30(3):133-140; quiz 141.
  • 9. Henry LG, Brunson KJ, Walden HS, Wenzlow N, Beachboard S.E, Barr K.L., Long M.T. Comparison of six commercial antigen kits for detection of Dirofilaria immitis infections in canines with necropsy-confirmed heartworm status. Vet. Parasitol. 2018;254:178–182. [Crossref]
  • 10. Genchi M, Rinaldi L, Venco L, Cringoli G, Vismarra A, Kramer L. Dirofilaria immitis and D. repens in dog and cat: a questionnaire study in Italy. Vet. Parasitol. 2019;267:26-31. doi:10.1016/j.vetpar.2019.01.014. [Crossref]
  • 11. Anvari D, Elahe N, Ahmad D, Shahabeddin S, Mahmood M, Hezarjaribi Z, Reza M, Shirzad G. The global status of Dirofilaria immitis in dogs: a systematic review and meta-analysis based on published articles. Res Vet Sci. 2020;131:104–116. doi:10.1016/j.rvsc.2020.04.002. [Crossref]
  • 12. Selim A, Alanazi D, Sazmand A, Otranto D. Seroprevalence and associated risk factors for vector-borne pathogens in dogs from Egypt Abdelfattah. Parasit Vectors. 2021;14(1):175 https://doi.org/10.1186/s13071-021-04670-0. [Crossref]
  • 13. Yildiz K , Yasa D, Yagci BB, Öcal N, Gazyağci AN. Distribution of dirofilaria immitis in dogs in Kırıkkale. Turkish J Parasitol. 2008;32:225-228.
  • 14. Sarı BM , Taşkın G, Kılıç Y. Seroprevalence of dirofilaria immitis, ehrlichia canis and borrelia burgdorferi in dogs in Iğdır province, Turkey. Kafkas Univ Vet Fak Journal. 2013;19:735-739. [Crossref]
  • 15. Sarali H, Bilgic H, Bakirci S, Karagenc T. Prevalence of dirofilaria immitis infection in dogs from Aydin and Izmir Provinces, Turkey. Animal Health Prod and Hyg. 2020;9(2):711 – 715.
  • 16. Omar O, Elamin E, Omer S, Alagaili A, Mohammed O. Serorevalence of Dirofilaria immitis in dogs and cats in Riyadh City, Saudi Arabia, Trop Biomed. 2018;35(2): 531–540.
  • 17. Bamorovat M, Sharifi I, Fasihi Harandi M, Nasibi S, Sadeghi B, Khedri J, Mohammadi MA. Parasitological, serological and molecular study of dirofilariaimmitis in domestic dogs, southeastern Iran. Iran J. Parasitol. 2017;12:260-266.
  • 18. Amall HA. Seroepidemiological study of heartworm Dirofilaria immitis in Baghdad and Karbala provinces. Thesis of PhD. In veterinary medicine \ Parasitology.College of Veterinary Medicine. University of Baghdad / Iraq. 2010.
  • 19. Al-Salihi KA, Al-Dabhawi AH, Al-Rammahi HM, Kareem FA. Dirofilaria immitis infestation in imported police (K-9) dogs in Iraq: clinicopathological and molecular investigations study. Brazil J Vet Res Animal Sci. 2019;56(2):e152987. [Crossref]
  • 20. Alia YY, May HK, Amall HA. Serological study of dirophilaria immitis in human from some village in Al-Hindya part of Karbala governorate. Inter J Sci Natur. 2013;4 (1):185-188.
  • 21. AL-shabbani A. In Iraq, The First Application of Serological SNAP ELISA Technique In Detection of Canine Heartworms (Dirofilaria immitis) In Herder Dogs of Al-Qadisiyah and Dhi-Qar Provinces. Kufa J Vet Med Sci. 2016;7(1)B:192-198.
  • 22. Gary WL, Leland SR, John H. CrossRapid Diagnosis of Brugia malayi and Wuchereria bancrofti Filariasis by an Acridine orange/Microhematocrit Tube Technique. The Journal of Parasit. 1990;76( 2 ): 278-281. Stable URL: http://www.jstor.org/stable/3283035 . [Crossref]
  • 23. Rojas A, Rojas D, Montenegro VM, Baneth G. Detection of Dirofilaria immitis and other arthropod-borne filarioids by an HRM real-time qPCR, blood-concentrating techniques and a serological assay in dogs from Costa Rica. Parasit Vectors. 2015;8:170. [Crossref]
  • 24. Atkins C. Canine heartworm disease. In: Ettinger SJ, Feldman EC, eds. Textbook Vet Internal Med. 6th ed. St. Louis: Elsevier. 2005;1118-1136.
  • 25. Alobaidii W, Zaki Z, Hassan M. Detection of dirofilaria immitis antigen in cats in Mosul city. Iraqi J Vet Sci. 2022;36(1):57-60. [Crossref]
  • 26. Amall HA, Aleia YY. First document on the presence of Iraqi Dirofilaria immitis. Iraqi J Vet Med. 2009;33(1):183-186. [Crossref]
  • 27. Al Salihi KA, Al Zubaydi SQ, Katah, H. Gastrointestinal parasites infestation in military working dogs/ K9 in Al Muthanna Governorate in compare to semi housed dogs. Mirror Res Vet Sci Anim. 2017;6(2):25-38.
  • 28. Montarsi F, Ciocchetta S, Devine G, Ravagnan S, Mutinelli F, Frangipane di Regalbono A, Otranto D, Capelli G. Development of dirofilaria immitis within the mosquito Aedes (Finlaya) koreicus, a new invasive species for Europe. Parasit Vectors. 2015;8:177. [Crossref]
  • 29. Oi M, Yoshikawa S, Ichikawa Y, Nakagaki K, Matsumoto J, Nogami S. Prevalence of dirofilaria immitis among shelter dogs in Tokyo, Japan, after a decade: comparison of 1999-2001 and 2009-2011. Parasite. 2014;21(4):10. [Crossref]
  • 30. Mendoza-Roldan J, Benelli G, Panarese R, Iatta R, Furlanello T, Beugnet F, Zatelli A, Otranto D. leishmania infantum and dirofilaria immitis infections in Italy, 2009–2019: Changing distribution patterns. Parasit Vectors. 2020;13:193. [Crossref]
  • 31. Nguyen C, Koh WL, Casteriano, A. Mosquito-borne heartworm dirofilaria immitis in dogs from Australia. Parasit Vectors. 2016;9: 535. [Crossref]
  • 32. Coles EH. Vet Clin Pathol. 4th ed. Saunders Company, Philadelphia. 1986:203-240.
  • 33. Watanabe Y, Yang CH, Tung KC, Ooi HK. Comparison of microfilaria concentration method for Setaria digitata infection in cattle and for Dirofilaria immitis infection in dogs. J. Vet. Med. Sci. 2004;66: 543–545. [Crossref]
  • 34. Venco L, Genchi, C, Simón F. La filariosis cardiopulmonar (Dirofilaria immitis) en el perro. In La Filariosis en las Especies Domésticas y en el Hombre , Simón F, Genchi C, Venco L, Montoya MN, Eds.; Merial Laboratorios: Barcelona, Spain. 2011:19-60.
  • 35. Laidoudi Y, Ringot D, Watier-Grillot S, Davoust B, Mediannikov OA. Cardiac and subcutaneous canine dirofilariosis outbreak in a kennel in central France. Parasite. 2019;26:72. [Crossref]
  • 36. Ogbaje CI, Abel-Danjuma. Prevalence and risk factors associated with Dirofilaria immitis infection in dogs in Makurdi, Benue State, Nigeria. J Adv Vet Anim Res. 2016i,3(4): 338-344. [Crossref]
  • 37. Ranjbar-Bahadori S, Eslami A, Bokaic S. Evaluation of different methods for diagnosis of dirofilaria immitis. Pak J Biol Sci. 2007;10(11):1938–1940. [Crossref]
Toplam 37 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Sağlık Kurumları Yönetimi
Bölüm Araştırma Makaleleri
Yazarlar

Maab Ibrahim Al-farwachi Bu kişi benim 0000-0002-2288-6274

Haneen Badran Al-melachi Bu kişi benim 0000-0001-9493-5867

Yayımlanma Tarihi 29 Nisan 2022
Yayımlandığı Sayı Yıl 2022 Cilt: 17 Sayı: 1

Kaynak Göster

APA Al-farwachi, M. I., & Al-melachi, H. B. (2022). Prevalence of Canine Cardiac Dirofilariasis in Nineveh Governorate of Iraq. Atatürk Üniversitesi Veteriner Bilimleri Dergisi, 17(1), 31-34.
AMA Al-farwachi MI, Al-melachi HB. Prevalence of Canine Cardiac Dirofilariasis in Nineveh Governorate of Iraq. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. Nisan 2022;17(1):31-34.
Chicago Al-farwachi, Maab Ibrahim, ve Haneen Badran Al-melachi. “Prevalence of Canine Cardiac Dirofilariasis in Nineveh Governorate of Iraq”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 17, sy. 1 (Nisan 2022): 31-34.
EndNote Al-farwachi MI, Al-melachi HB (01 Nisan 2022) Prevalence of Canine Cardiac Dirofilariasis in Nineveh Governorate of Iraq. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 17 1 31–34.
IEEE M. I. Al-farwachi ve H. B. Al-melachi, “Prevalence of Canine Cardiac Dirofilariasis in Nineveh Governorate of Iraq”, Atatürk Üniversitesi Veteriner Bilimleri Dergisi, c. 17, sy. 1, ss. 31–34, 2022.
ISNAD Al-farwachi, Maab Ibrahim - Al-melachi, Haneen Badran. “Prevalence of Canine Cardiac Dirofilariasis in Nineveh Governorate of Iraq”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi 17/1 (Nisan 2022), 31-34.
JAMA Al-farwachi MI, Al-melachi HB. Prevalence of Canine Cardiac Dirofilariasis in Nineveh Governorate of Iraq. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. 2022;17:31–34.
MLA Al-farwachi, Maab Ibrahim ve Haneen Badran Al-melachi. “Prevalence of Canine Cardiac Dirofilariasis in Nineveh Governorate of Iraq”. Atatürk Üniversitesi Veteriner Bilimleri Dergisi, c. 17, sy. 1, 2022, ss. 31-34.
Vancouver Al-farwachi MI, Al-melachi HB. Prevalence of Canine Cardiac Dirofilariasis in Nineveh Governorate of Iraq. Atatürk Üniversitesi Veteriner Bilimleri Dergisi. 2022;17(1):31-4.