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MOLECULAR INVESTIGATION OF CANINE HEPATOZOONOSIS IN BATMAN AND VAN PROVINCES OF TÜRKİYE

Year 2022, , 50 - 56, 26.07.2022

Bekir Oğuz , Mustafa Serdar Değer , Saeed El-ashram

https://doi.org/10.18036/estubtdc.1052090

Abstract

Canine hepatozoonosis is a tick-borne protozoan disease spread by hard ticks of the Ixodidae family. Although this illness has been seen in numerous locations in Türkiye, its existence in the Batman and Van provinces has yet to be confirmed. The purpose of this research was to look into canine hepatozoonosis in stray dogs from two distinct areas in Türkiye using conventional polymerase chain reaction (PCR). Between 2019 and 2021, blood samples were collected from 197 stray dogs in Batman and Van provinces in Türkiye. A unique 486–520 bp segment of the 18S rRNA gene of Hepatozoon spp. was amplified using PCR. According to the PCR findings, none of the 197 stray dogs tested positive for Hepatozoon spp. This research offers epidemiological data on the prevalence of canine hepatozoonosis in Türkiye, which may be useful in future studies with larger sample sizes and dogs of varied origins.

Keywords

Batman Canine hepatozoonosis PCR Stray dogs Van Türkiye

Thanks

We thank Prof. Armagan Erdem UTUK and Assist. Prof. Ufuk EROL for providing positive DNA of Hepatozoon spp. The authors also thank Veterinarians Onur KILIC and Omer SELCIN for kind help during sample collection.

References

  • [1] Aydin MF, Sevinc F, Sevinc M. Molecular detection and characterization of Hepatozoon spp. in dogs from the Central part of Turkey. Ticks Tick Borne Dis, 2015; 6(3): 388-392.
  • [2] Murata T, Inoue M, Taura Y, Nakayama S, Abe H, Fujisaki K. Detection of Hepatozoon canis oocyst from ticks collected from the infected dogs. J Vet Med Sci, 1995; 57(1): 111-112.
  • [3] Forlano M, Scofield A, Elisei C, Fernandes KR, Ewing SA, Massard CL. Diagnosis of Hepatozoon spp. in Amblyomma ovale and its experimental transmission in domestic dogs in Brazil. Vet Parasitol, 2005; 134(1-2): 1-7.
  • [4] Baneth G. Perspectives on canine and feline hepatozoonosis. Vet Parasitol, 2011; 181(1): 3-11.
  • [5] de Miranda RL, de Castro JR, Olegário MM, Beletti ME, Mundim AV, O’Dwyer LH, Eyal O, Talmi-Frank D, Cury MC, Baneth G. Oocysts of Hepatozoon canis in Rhipicephalus (Boophilus) microplus collected from a naturally infected dog. Vet Parasitol, 2011; 177(3-4): 392-396.
  • [6] Giannelli A, Lia RP, Annoscia G, Buonavoglia C, Lorusso E, Dantas-Torres F, Baneth G, Otranto D. Rhipicephalus turanicus, a new vector of Hepatozoon canis. Parasitology, 2017; 144 (Suppl 6): 730-737. [7] Orkun O, Nalbantoglu S. Hepatozoon canis in Turkish red foxes and their ticks. Vet Parasitol Reg Stud Reports, 2018; 13: 35-37.
  • [8] Léveillé AN, Baneth G, Barta JR. Next generation sequencing from Hepatozoon canis (Apicomplexa: Coccidia: Adeleorina): complete apicoplast genome and multiple mitochondrion-associated sequences. Int J Parasitol, 2019; 49: 375-387
  • [9] Mathew JS, Ewing SA, Panciera RJ, Woods JP. Experimental transmission of Hepatozoon americanum Vincent-Johnson et al., 1997 to dogs by the Gulf Coast tick, Amblyomma maculatum Koch. Vet Parasitol, 1998; 80: 1-14.
  • [10] Inci A, Duzlu O. Vectors and Vector-Borne Diseases. Erciyes Üniv Vet Fak Derg, 2009; 6(1): 53-63.
  • [11] Aktas M, Ozubek S, Sayın Ipek DN. Molecular investigations of Hepatozoon species in dogs and developmental stages of Rhipicephalus sanguineus. Parasitol Res, 2013; 112: 2381-2385.
  • [12] Aktas M. A survey of ixodid tick species and molecular identification of tick-borne pathogens. Vet Parasitol, 2014; 200(3-4): 276-283.
  • [13] Aktas M, Ozubek S. A survey of canine haemoprotozoan parasites from Turkey, including molecular evidence of an unnamed Babesia. Comp Immunol Microbiol Infect Dis, 2017; 52: 36-42.
  • [14] Kramer. Canine hepatozoonosis-a summary for the practitioner. CVBD World Forum, 2009; 6: 1-12.
  • [15] Tuzdil AN. Biz de ilk defa görülen bir Hepatozoon canis vakası. Türk Bay Cem Mec, 1933; 13: 35.
  • [16] Voyvoda H, Pasa S, Uner A. Clinical Hepatozoon canis infection in a dog in Turkey. J Small Anim Pract, 2004; 45: 613-617.
  • [17] Karagenc TI, Pasa S, Kirli G, Hosgor M, Bilgic HB, Ozon YH, Atasoy A, Eren H. A parasitological, molecular and serological survey of Hepatozoon canis infection in dogs around the Aegean coast of Turkey. Vet Parasitol, 2006; 135: 113-119.
  • [18] Duzlu O, Inci A, Yildirim A, Onder Z, Ciloglu A. The investigation of some tick-borne protozoon and rickettsial infections in dogs by Real Time PCR and the molecular characterizations of the detected isolates. Ankara Univ Vet Fak Derg, 2014; 61: 275-282.
  • [19] Aktas M, Ozubek S, Altay K, Balkaya I, Utuk AE, Kırbas A, Simsek S, Dumanli, N. A molecular and parasitological survey of Hepatozoon canis in domestic dogs in Turkey. Vet Parasitol, 2015; 209: 264-267.
  • [20] Bolukbas CS, Pekmezci D, Gurler AT, Pekmezci GZ, Guzel M, Acici M, Umur S. Molecular survey of Hepatozoon canis in dogs from Samsun Province of Northern part of Turkey. J Etlik Vet Microbiol, 2016; 27: 104-107.
  • [21] Guo H, Sevinc F, Ceylan O, Sevinc M, Ince E, Gao Y, Moumouni PFA, Liu M, Efstratiou A, Wang G, Cao S, Zhou M, Jirapattharasate C, Ringo AE, Zhenh W, Xuan X. A PCR survey of vector-borne pathogens in different dogpopulations from Turkey. Acta Parasitol, 2017; 62: 533-540.
  • [22] Guven E, Avcioglu H, Cengiz S, Hayirli A. Vector-borne pathogens in stray dogs in Northeastern Turkey. Vector Borne Zoonotic Dis, 2017; 17(8): 610-617.
  • [23] Orkun O, Nafiye K, Sursal N, Cakmak A, Nalbantoglu S, Karaer Z. Molecular characterization of tick-borne blood protozoa in stray dogs from central Anatolia region of Turkey with a high-rate Hepatozoon infection. Kafkas Univ Vet Fak, 2018; 24(2): 227-232.
  • [24] Aslantas O, Celebi B, Usluca S. Investigation of vector-borne diseases in dogs. Harran Üniv Vet Fak Derg, 2020; 9(2): 154-160.
  • [25] Erol U, Altay K, Ataş AD, Özkan E, Şahin ÖF. Molecular Prevalence of Canine Hepatozoonosis in Owned-Dogs in Central Part of Turkey. Isr J Vet Med, 2021; 76(2): 71-76.
  • [26] Attipa C, Hicks CAE, Barker EN, Christodoulou V, Neofytou K, Mylonakis ME, Siarkou VI, Vingopoulou EI, Soutter F, Chochlakis D, Psaroulaki A, Papasouliotis K, Tasker S. Canine tick-borne pathogens in Cyprus and a unique canine case of multiple co-infections. Ticks Tick Borne Dis, 2017; 8(3): 341-346.
  • [27] Casati, SS, Sager, HH, Gern, LL, Piffaretti, JCJ-C. Presence of potentially pathogenic Babesia sp for human in Ixodes ricinus in Switzerland. Ann Agric Environ Med, 2006; 13(1): 65.
  • [28] Gökçe T. Investigations of hard tick species (Acari:Ixodidae) parasitizing in Corum region and presence of Babesia in these ticks.Msc, Hitit Üniversitesi, Çorum, Turkey, 2017.
  • [29] Andersson MO, Tolf C, Tamba P, Stefanache M, Waldenström J, Dobler G, Chițimia-Dobler L. Canine tick-borne diseases in pet dogs from Romania. Parasit Vectors, 2017; 10(1): 155.
  • [30] Maggi RG., Krämer F. A review on the occurrence of companion vector-borne diseases in pet animals in Latin America. Parasites Vectors, 2019; 12: 145.
  • [31] Dantas-Torres F, Otranto D. Hepatozoonosis. In: Marcondes CB, editors. Arthropod Borne Diseases. Springer; Cham, Switzerland: 2017; 215–222.
  • [32] Nguyen VL, Colella V, Greco G. et al. Molecular detection of pathogens in ticks and fleas collected from companion dogs and cats in East and Southeast Asia. Parasites Vectors, 2020; 13: 420.
  • [33] Alaeddinoglu F. The Functional Characteristics and Primary Problems of the Batman City. Eastern Geography Review, 2011; 15(24): 19-42 .
  • [34] Kalelioglu E. Characteristics of the climate of Van Plain (Van Ovasının iklim özellikleri). Ankara Üniv. Dil Tarih-Coğrafya Fakültesi Dergisi, 1991; 35, 155-166.
  • [35] Dantas-Torres F, Latrofa MS, Weigl S, Tarallo VD, Lia RP, Otranto D. Hepatozoon canis infection in ticks during spring and summer in Italy. Parasitol Res, 2012; 110 (Suppl 2): 695-698
  • [36] Pacifico L, Braff J, Buono F. et al. Hepatozoon canis in hunting dogs from Southern Italy: distribution and risk factors. Parasitol Res, 2020; 119: 3023-3031.
  • [37] Deger MS, Bicek K, Oguz B. Infestation rate and distribution of hard ticks on cattle in the Eastern Anatolia Region of Turkey. Sci Parasitol, 2016; 17: 76-82.
  • [38] Smith TG. The genus hepatozoon (Apicomplexa: Adeleina). J Parasitol, 1996; 82: 565-585.
  • [39] Taylor MA, Coop RL, Wall RL. Veterinary Parasitology. 4th. ed. Blackwell Publishing, Oxford, 2016.

MOLECULAR INVESTIGATION OF CANINE HEPATOZOONOSIS IN BATMAN AND VAN PROVINCES OF TÜRKİYE

Year 2022, , 50 - 56, 26.07.2022

Bekir Oğuz , Mustafa Serdar Değer , Saeed El-ashram

https://doi.org/10.18036/estubtdc.1052090

Abstract

Canine hepatozoonosis is a tick-borne protozoan disease spread by hard ticks of the Ixodidae family. Although this illness has been seen in numerous locations in Türkiye, its existence in the Batman and Van provinces has yet to be confirmed. The purpose of this research was to look into canine hepatozoonosis in stray dogs from two distinct areas in Türkiye using conventional polymerase chain reaction (PCR). Between 2019 and 2021, blood samples were collected from 197 stray dogs in Batman and Van provinces in Türkiye. A unique 486–520 bp segment of the 18S rRNA gene of Hepatozoon spp. was amplified using PCR. According to the PCR findings, none of the 197 stray dogs tested positive for Hepatozoon spp. This research offers epidemiological data on the prevalence of canine hepatozoonosis in Türkiye, which may be useful in future studies with larger sample sizes and dogs of varied origins.

Keywords

Batman Canine hepatozoonosis PCR Stray dogs Van Türkiye

References

  • [1] Aydin MF, Sevinc F, Sevinc M. Molecular detection and characterization of Hepatozoon spp. in dogs from the Central part of Turkey. Ticks Tick Borne Dis, 2015; 6(3): 388-392.
  • [2] Murata T, Inoue M, Taura Y, Nakayama S, Abe H, Fujisaki K. Detection of Hepatozoon canis oocyst from ticks collected from the infected dogs. J Vet Med Sci, 1995; 57(1): 111-112.
  • [3] Forlano M, Scofield A, Elisei C, Fernandes KR, Ewing SA, Massard CL. Diagnosis of Hepatozoon spp. in Amblyomma ovale and its experimental transmission in domestic dogs in Brazil. Vet Parasitol, 2005; 134(1-2): 1-7.
  • [4] Baneth G. Perspectives on canine and feline hepatozoonosis. Vet Parasitol, 2011; 181(1): 3-11.
  • [5] de Miranda RL, de Castro JR, Olegário MM, Beletti ME, Mundim AV, O’Dwyer LH, Eyal O, Talmi-Frank D, Cury MC, Baneth G. Oocysts of Hepatozoon canis in Rhipicephalus (Boophilus) microplus collected from a naturally infected dog. Vet Parasitol, 2011; 177(3-4): 392-396.
  • [6] Giannelli A, Lia RP, Annoscia G, Buonavoglia C, Lorusso E, Dantas-Torres F, Baneth G, Otranto D. Rhipicephalus turanicus, a new vector of Hepatozoon canis. Parasitology, 2017; 144 (Suppl 6): 730-737. [7] Orkun O, Nalbantoglu S. Hepatozoon canis in Turkish red foxes and their ticks. Vet Parasitol Reg Stud Reports, 2018; 13: 35-37.
  • [8] Léveillé AN, Baneth G, Barta JR. Next generation sequencing from Hepatozoon canis (Apicomplexa: Coccidia: Adeleorina): complete apicoplast genome and multiple mitochondrion-associated sequences. Int J Parasitol, 2019; 49: 375-387
  • [9] Mathew JS, Ewing SA, Panciera RJ, Woods JP. Experimental transmission of Hepatozoon americanum Vincent-Johnson et al., 1997 to dogs by the Gulf Coast tick, Amblyomma maculatum Koch. Vet Parasitol, 1998; 80: 1-14.
  • [10] Inci A, Duzlu O. Vectors and Vector-Borne Diseases. Erciyes Üniv Vet Fak Derg, 2009; 6(1): 53-63.
  • [11] Aktas M, Ozubek S, Sayın Ipek DN. Molecular investigations of Hepatozoon species in dogs and developmental stages of Rhipicephalus sanguineus. Parasitol Res, 2013; 112: 2381-2385.
  • [12] Aktas M. A survey of ixodid tick species and molecular identification of tick-borne pathogens. Vet Parasitol, 2014; 200(3-4): 276-283.
  • [13] Aktas M, Ozubek S. A survey of canine haemoprotozoan parasites from Turkey, including molecular evidence of an unnamed Babesia. Comp Immunol Microbiol Infect Dis, 2017; 52: 36-42.
  • [14] Kramer. Canine hepatozoonosis-a summary for the practitioner. CVBD World Forum, 2009; 6: 1-12.
  • [15] Tuzdil AN. Biz de ilk defa görülen bir Hepatozoon canis vakası. Türk Bay Cem Mec, 1933; 13: 35.
  • [16] Voyvoda H, Pasa S, Uner A. Clinical Hepatozoon canis infection in a dog in Turkey. J Small Anim Pract, 2004; 45: 613-617.
  • [17] Karagenc TI, Pasa S, Kirli G, Hosgor M, Bilgic HB, Ozon YH, Atasoy A, Eren H. A parasitological, molecular and serological survey of Hepatozoon canis infection in dogs around the Aegean coast of Turkey. Vet Parasitol, 2006; 135: 113-119.
  • [18] Duzlu O, Inci A, Yildirim A, Onder Z, Ciloglu A. The investigation of some tick-borne protozoon and rickettsial infections in dogs by Real Time PCR and the molecular characterizations of the detected isolates. Ankara Univ Vet Fak Derg, 2014; 61: 275-282.
  • [19] Aktas M, Ozubek S, Altay K, Balkaya I, Utuk AE, Kırbas A, Simsek S, Dumanli, N. A molecular and parasitological survey of Hepatozoon canis in domestic dogs in Turkey. Vet Parasitol, 2015; 209: 264-267.
  • [20] Bolukbas CS, Pekmezci D, Gurler AT, Pekmezci GZ, Guzel M, Acici M, Umur S. Molecular survey of Hepatozoon canis in dogs from Samsun Province of Northern part of Turkey. J Etlik Vet Microbiol, 2016; 27: 104-107.
  • [21] Guo H, Sevinc F, Ceylan O, Sevinc M, Ince E, Gao Y, Moumouni PFA, Liu M, Efstratiou A, Wang G, Cao S, Zhou M, Jirapattharasate C, Ringo AE, Zhenh W, Xuan X. A PCR survey of vector-borne pathogens in different dogpopulations from Turkey. Acta Parasitol, 2017; 62: 533-540.
  • [22] Guven E, Avcioglu H, Cengiz S, Hayirli A. Vector-borne pathogens in stray dogs in Northeastern Turkey. Vector Borne Zoonotic Dis, 2017; 17(8): 610-617.
  • [23] Orkun O, Nafiye K, Sursal N, Cakmak A, Nalbantoglu S, Karaer Z. Molecular characterization of tick-borne blood protozoa in stray dogs from central Anatolia region of Turkey with a high-rate Hepatozoon infection. Kafkas Univ Vet Fak, 2018; 24(2): 227-232.
  • [24] Aslantas O, Celebi B, Usluca S. Investigation of vector-borne diseases in dogs. Harran Üniv Vet Fak Derg, 2020; 9(2): 154-160.
  • [25] Erol U, Altay K, Ataş AD, Özkan E, Şahin ÖF. Molecular Prevalence of Canine Hepatozoonosis in Owned-Dogs in Central Part of Turkey. Isr J Vet Med, 2021; 76(2): 71-76.
  • [26] Attipa C, Hicks CAE, Barker EN, Christodoulou V, Neofytou K, Mylonakis ME, Siarkou VI, Vingopoulou EI, Soutter F, Chochlakis D, Psaroulaki A, Papasouliotis K, Tasker S. Canine tick-borne pathogens in Cyprus and a unique canine case of multiple co-infections. Ticks Tick Borne Dis, 2017; 8(3): 341-346.
  • [27] Casati, SS, Sager, HH, Gern, LL, Piffaretti, JCJ-C. Presence of potentially pathogenic Babesia sp for human in Ixodes ricinus in Switzerland. Ann Agric Environ Med, 2006; 13(1): 65.
  • [28] Gökçe T. Investigations of hard tick species (Acari:Ixodidae) parasitizing in Corum region and presence of Babesia in these ticks.Msc, Hitit Üniversitesi, Çorum, Turkey, 2017.
  • [29] Andersson MO, Tolf C, Tamba P, Stefanache M, Waldenström J, Dobler G, Chițimia-Dobler L. Canine tick-borne diseases in pet dogs from Romania. Parasit Vectors, 2017; 10(1): 155.
  • [30] Maggi RG., Krämer F. A review on the occurrence of companion vector-borne diseases in pet animals in Latin America. Parasites Vectors, 2019; 12: 145.
  • [31] Dantas-Torres F, Otranto D. Hepatozoonosis. In: Marcondes CB, editors. Arthropod Borne Diseases. Springer; Cham, Switzerland: 2017; 215–222.
  • [32] Nguyen VL, Colella V, Greco G. et al. Molecular detection of pathogens in ticks and fleas collected from companion dogs and cats in East and Southeast Asia. Parasites Vectors, 2020; 13: 420.
  • [33] Alaeddinoglu F. The Functional Characteristics and Primary Problems of the Batman City. Eastern Geography Review, 2011; 15(24): 19-42 .
  • [34] Kalelioglu E. Characteristics of the climate of Van Plain (Van Ovasının iklim özellikleri). Ankara Üniv. Dil Tarih-Coğrafya Fakültesi Dergisi, 1991; 35, 155-166.
  • [35] Dantas-Torres F, Latrofa MS, Weigl S, Tarallo VD, Lia RP, Otranto D. Hepatozoon canis infection in ticks during spring and summer in Italy. Parasitol Res, 2012; 110 (Suppl 2): 695-698
  • [36] Pacifico L, Braff J, Buono F. et al. Hepatozoon canis in hunting dogs from Southern Italy: distribution and risk factors. Parasitol Res, 2020; 119: 3023-3031.
  • [37] Deger MS, Bicek K, Oguz B. Infestation rate and distribution of hard ticks on cattle in the Eastern Anatolia Region of Turkey. Sci Parasitol, 2016; 17: 76-82.
  • [38] Smith TG. The genus hepatozoon (Apicomplexa: Adeleina). J Parasitol, 1996; 82: 565-585.
  • [39] Taylor MA, Coop RL, Wall RL. Veterinary Parasitology. 4th. ed. Blackwell Publishing, Oxford, 2016.
There are 38 citations in total.

Details

Primary Language English
Subjects Microbiology
Journal Section Articles
Authors

Bekir Oğuz 0000-0001-8720-3940

Mustafa Serdar Değer 0000-0001-9651-6957

Saeed El-ashram This is me 0000-0003-0389-1980

Publication Date July 26, 2022
Published in Issue Year 2022

Cite

APA Oğuz, B., Değer, M. S., & El-ashram, S. (2022). MOLECULAR INVESTIGATION OF CANINE HEPATOZOONOSIS IN BATMAN AND VAN PROVINCES OF TÜRKİYE. Eskişehir Teknik Üniversitesi Bilim Ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji, 11(2), 50-56. https://doi.org/10.18036/estubtdc.1052090
AMA Oğuz B, Değer MS, El-ashram S. MOLECULAR INVESTIGATION OF CANINE HEPATOZOONOSIS IN BATMAN AND VAN PROVINCES OF TÜRKİYE. Eskişehir Teknik Üniversitesi Bilim ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji. July 2022;11(2):50-56. doi:10.18036/estubtdc.1052090
Chicago Oğuz, Bekir, Mustafa Serdar Değer, and Saeed El-ashram. “MOLECULAR INVESTIGATION OF CANINE HEPATOZOONOSIS IN BATMAN AND VAN PROVINCES OF TÜRKİYE”. Eskişehir Teknik Üniversitesi Bilim Ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji 11, no. 2 (July 2022): 50-56. https://doi.org/10.18036/estubtdc.1052090.
EndNote Oğuz B, Değer MS, El-ashram S (July 1, 2022) MOLECULAR INVESTIGATION OF CANINE HEPATOZOONOSIS IN BATMAN AND VAN PROVINCES OF TÜRKİYE. Eskişehir Teknik Üniversitesi Bilim ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji 11 2 50–56.
IEEE B. Oğuz, M. S. Değer, and S. El-ashram, “MOLECULAR INVESTIGATION OF CANINE HEPATOZOONOSIS IN BATMAN AND VAN PROVINCES OF TÜRKİYE”, Eskişehir Teknik Üniversitesi Bilim ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji, vol. 11, no. 2, pp. 50–56, 2022, doi: 10.18036/estubtdc.1052090.
ISNAD Oğuz, Bekir et al. “MOLECULAR INVESTIGATION OF CANINE HEPATOZOONOSIS IN BATMAN AND VAN PROVINCES OF TÜRKİYE”. Eskişehir Teknik Üniversitesi Bilim ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji 11/2 (July 2022), 50-56. https://doi.org/10.18036/estubtdc.1052090.
JAMA Oğuz B, Değer MS, El-ashram S. MOLECULAR INVESTIGATION OF CANINE HEPATOZOONOSIS IN BATMAN AND VAN PROVINCES OF TÜRKİYE. Eskişehir Teknik Üniversitesi Bilim ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji. 2022;11:50–56.
MLA Oğuz, Bekir et al. “MOLECULAR INVESTIGATION OF CANINE HEPATOZOONOSIS IN BATMAN AND VAN PROVINCES OF TÜRKİYE”. Eskişehir Teknik Üniversitesi Bilim Ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji, vol. 11, no. 2, 2022, pp. 50-56, doi:10.18036/estubtdc.1052090.
Vancouver Oğuz B, Değer MS, El-ashram S. MOLECULAR INVESTIGATION OF CANINE HEPATOZOONOSIS IN BATMAN AND VAN PROVINCES OF TÜRKİYE. Eskişehir Teknik Üniversitesi Bilim ve Teknoloji Dergisi - C Yaşam Bilimleri Ve Biyoteknoloji. 2022;11(2):50-6.