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A Histopathological and Biochemical Investigation of the Wound Healing and Oxidative Stress Effect on the Wound Model of the Achillea millefolium in Rats

Yıl 2017, Cilt: 28 Sayı: 3, 157 - 163, 20.12.2017

Öz

The aim of current study is to evaulate of histopathological and
biochemical effects of Achillea
millefolium
(Civanperçemi-CP) on the wound healing in the rats skin. In
this study, 24 Wistar albino rats were divided to three groups, Control (K),
Madecassol® (M) and Achillea millefolium
(CP). A wound was created with a punch under the anesthesia in the back region
of the rats in all groups. Achillea
millefolium
and madecassol pomad have been administered to study groups per
day and serum physiologic solution has been administered to K group locally as
placebo. In order to evaulate by histopathological and immunohistochemical and
biochemical on 7th and 15th days were taken the blood and skin tissue. Compared
with the K group, the topical application of Achillea millefolium has a positive effect on epithelialization,
fibroblastic activity and collagenization in the CP group. As a result of
immunohistochemical investigation, Glutathione peroxidase 1 (GPx1)
immunoreactivity in the CP group was stronger than in the K group. Biochemical
examination of skin and blood tissue revealed that fluctuated antioxidant
defence system constituents levels were restored in CP and M groups. In
conclusion, Achillea millefolium
increased connective tissue formation and reduced the time needed to complete
epithelization and was also found that wound healing was accelerated by this
occasion.

Kaynakça

  • Adamson B, Schwarz D, Klugston P, GilmontR, Perry L, Fisher J, Rees R (1996). Oxidant stress: the role of the glutathione redox cycle in skin preconditioning. J Surg Res, 62, 159-164. Adetutu, A, Morgan, W, Corcoran O (2011). Ethnopharmacological survey and in vitro evaluation of wound-healing plants used in South-western Nigeria. J Ethnopharmacol, 137, 50-56. Agarwal JP, Ogilvie M (2005). Vacuum-assisted closure for sternal wounds: a first-line therapeutic management approach. Plast Reconstr Surg, 116, 4, 1035-1040. Aksoy H, Özakpınar ÖB. (2014). Yara iyileşmesi ve oksidatif stres. Marmara Pharm J, 18, 153-158. Aydın S, Çağlıkülekçi M, Çolak T, Dirlik M, Öcal K, Akça T (2002). Washington Cerrahi El Kitabı, Nobel Tıp Kitabevleri. Calvin M (1998). Cutaneous wound healing. Wounds, 10, 1, 12-32. Candan İ (2003). Medikal Tedavi. Cilt 1. Antıp Yayınları. Ankara. 361-365. Czuczejko J, Zachara BA, Staubach-Topczewska E, Halota W, Kedziora J (2003). Selenium, glutathione and glutathione peroxidases in blood of patients with chronic liver diseases. Acta Biochim Pol, 50, 1147–1154. Çavdar C, Sifil, A, Çamsarı, T (1997). Reaktif oksijen türleri ve antioksidan savunma. Turk Neph Dial Transpl, 3, 92-95. Duarte T, Cooke M, Jones G (2009). Gene expression profiling reveals new protective rolesfor vitamin C in human skin cells. Adv Free Radical Bio, 46, 78– 87. Engin A (2004). Yara iyileşmesi In: Temel Cerrahi. Edited by Sayek, İ., 3. Baskı, pp: 266-277, Güneş Kitabevi, Ankara. Flanagan M (1994). Wound care. Assessment criteria. Nurs Times, 90, (45):77. 9-15 Gálvez M, Cordero CM, Lázaro, ML, Cortés F, Ayuso, MJ (2003). Cytotoxic effect of Plantago spp. on cancer cell lines. J Ethnopharmacol, 88, 125-130 . Grey JE, Enoch S, Harding KG (2006). Wound assessment. BMJ, 4, 332 (7536), 285-8. Güneş ÜY (2007). Kronik yaraların değerlendirilmesi. CÜ Hemşirelik Yüksekokulu Derg, 11 (3), 38-44. Hedlund CS (2002). Surgey of the integumentary system. In: Small Animal Surgery, 2th Edition, Edited by Fossum, T.W. Mosby, Printed in China, pp: 134-137 Heinze CD, Clem MF (1988). Wound healing and tissue repair. In: Textbook of Large Animal Surgery.2nd Ed., Edited by Oehme, F.W., pp:141-153 Williams& Wilkins USA. Herbette S, Roeckel-Drevet P, Drevet JR (2007). Seleno-independent glutathione peroxidases. More than simple antioxidant scavengers. FEBS J, 274, 2163–2180. Jain V, Prasad V, Pandey RS (2006). Wound healing activity of Desmodium gangeticum in Different Wound Model. J Plant Sci, 1(3), 247-253. Jurjus, A, Atiyeh BS, Abdallah IM, Jurjus RA, Hayek SN, Jaoude MA, Gerges A, Tohme RA (2007). Pharmacological modulation of wound healing in experimental burns. Burns, 33, 892-907. Kapan M, Aslanmirza MY, Karip AB, Bozkurt Y, Evsen MS, Sak E, Öngören AU (2008). Lokal fenitoin ve üre uygulamasının yara iyileşmesi üzerine olan etkilerinin karşılaştırılması. Yeni Tıp Derg, 25, 209-212. Kirsner, RS, Eaglsterin WH (1993). The wound healing process. Dermatol Clin, 11, 4, 629-640 Lakshmi T, Geetha R, Roy A, Aravind Kumar S (2011). Yarrow (Achillea Millefolium Linn) A Herbal Medicinal Plant with Broad Therapeutic Use–A Review. Int J Pharm Sci Rev Res, 9, 136-144. Munz B, Frank S, Hübner G, Olsen E, Werner S (1997). A novel type of glutathione peroxidase:expression and regulation during wound repair. Biochem J, 326, 579-85. Murnigsih T, Subeki H, Matsuura K, Takahashi M, Yamasaki O, Yamato Y, Maede K, Katakura M, Suzuki S, Kobayashi C, Yoshihara T (2005). Evaluation of the inhibitory activities of the extracts of Indonesian traditional medicinal plants against Plasmodium falciparum and Babesia gibsoni. J Vet Med Sci, 67, 829–831. Mustoe T (2004). Understanding chronic wounds: a unifying hypothesis on their pathogenesis and implications for therapy. Am J Surg, 187, 65–70. Özkorkmaz E, Özay Y (2009). Yara iyileşmesi ve yara iyileşmesinde kullanılan bazı bitkiler. Türk Bilimsel Derlemeler Dergisi 2, 63-67. Özler M, Şimşek K, Topal T, Öter Ş, Korkmaz A (2010). Pinealektomili ratlarda yara iyileşmesi. Gulhane Med J, 52, 181-184. Passalacqua N, Guarrera P, De Fine G (2007). Contribution to the knowledge of the folk plant medicine in Calabria region (Southern Italy). Fitoterapia, 78: 52-68. Pires JM, Mendes FR, Negri G, Duarte-Almeida JM, Carlini EA (2009). Anti noci-ceptive peripheral effect of Achillea millefolium L. and Artemisia vulgaris L, both plants known popularly by brand names of analgesic drugs. Phytother Res, 23, 212–219. Regan MC, Barbul A (1994). The cellular biology of wound healing. In: Wound Healing. Editedby Schlag, G., Redl, H. Vol:1 pp: 3-17 Springer-VerlagBerlin Heidelberg. Printed in Germany. Rigler DJ (1997). Inflamation and repair. In Veterinary Pathology, 6nd Ed., Edited by Jones, T.C.,Hunt, R.D., King, N.W., pp: 150-157, Williams &Wilkins, Pennsylvania. Rodrigues HG, Vinolo MA, Magdalon J, Vitzel K, Nachbar RT, Pessoa AF, dos Santos MF, Hatanaka E, Calder PC, Curi R (2012). Oral administration of oleic or linoleic acid accelerates the inflammatory phase of wound healing. J Invest Dermatol, 132, 1, 208-215. Saarialho-Kere UK (1992). Patterns of matrix metalloproteinase and TİMP expressionin chronic ulcers. Arch Dermatol Res, 290, 47-54. Sen CK, Roy S (2008). Redox signals in wound healing. Biochim Biophys Acta, 1780, 1348–1361. Souza de P, Gasparotto Jr. A, Crestania S, Stefanello MEA, Marques MCA, Silva-Santos JE, Kassuyaa CAL (2011). Hypotensive mechanism of the extracts and artemetin isolated from Achillea millefolium L.(Asterace) in rats. Phytomedicine, 18, 819–825. Stashak TS (1991). Principles of wound healing. In: Equine Wound Management, pp: 1-15, Lea&Febiger, Malvern, Pennsylvania. Steiling H, Munz B, Werner S, Brauchle M (1999). Different types of ROS scavenging enzymes are expressed during cutaneous wound repair. Exp Cell Res, 247, 484-94. Stojanović G, Radulović N, Hashimoto T, Palić R (2005). In vitro antimicrobial activity of extracts of four Achillea species, The composition of Achillea clavennae L. (Asteraceae) extract. J Ethnopharmacol, 101, 185–190. Swaim SF, Henderson RA (1990). Wound healing. In: Small Animal Wound Management. pp: 1-8,Lea & Febiger, Malvern, Pennsylvania. Theoret CL (2004). Update on wound repair, Clin Tech Equine Pract, 3, 110-122. Thomas AC, Wysocki AB (1990) The healing wound: a comparison of three clinically useful methods of measurement. Decubitus, 3,1,18-20, 24-5. Van Rijswijk L, Braden BJ (1999) Pressure ulcer patient and wound assessment: an AHCPR clinical practice guideline update. Ostomy Wound Manage, 45:56S-67S; quiz 68S-69S. Yaeesh S, Jamal Q, Khan AU, Gilani AH (2006). Studies on hepatoprotective, anti-spasmodic and calcium antagonist activities of the aqueous-methanol extract of Achillea millefolium. Phytother Res, 20, 546–551. Yager DR, Kulina RA, Gilman LA (2007). Wound fluids: a window into the wound environment? Int J Low Extrem Wounds, 6, 4, 262-272.

Ratlarda Deneysel Olarak Oluşturulan Yara Modelinde Civanperçemi (Achillea millefolium) Bitkisinin Yara İyileşmesi ve Oksidatif Stres Üzerine Etkisinin Histopatolojik ve Biyokimyasal Olarak Araştırılması

Yıl 2017, Cilt: 28 Sayı: 3, 157 - 163, 20.12.2017

Öz

Bu çalışmada Civanperçemi’nin (Achillea millefolium) (CP) ratlarda yara iyileşmesi
üzerine histopatolojik ve biyokimyasal etkisi araştırıldı. Çalışmada 24 adet
Wistar albino ırkı rat kullanıldı. Ratlar; Kontrol (K),
CP ve
Madecassol (M) grubu olmak üzere üç gruba ayrıldı. Tüm gruplardaki ratların
sırt bölgesi derisinde anestezi altında punch cihazı ile yara oluşturuldu.
CP grubu ratların
yara bölgelerine
CP ekstraktından elde edilen pomat uygulanırken, M grubu ratların yara
bölgelerine ise ticari bir preparat olan madecassol kremi uygulandı. Denemenin
7. günü ile deneme sonu olan 15. günde anestezi altında kan ve deri doku
örnekleri alındı. Histopatolojik incelemelerde, K grubu ile
karşılaştırıldığında CP grubunda yangı ve ödemin azaldığı, epitelizasyon,
fibroblastik aktivite ve kollajenizayonda pozitif bir etki görüldü.
İmmunohistokimyasal olarak
CP grubunda Glutathione peroxidase 1
(GPx1) immunoreaktivitesi K grubundan daha güçlü idi. Deri ve kan dokusunun
biyokimyasal incelemelerinde K grubuna göre M ve
CP grubunda antioksidan
savunma sistemi enzim düzeyleri daha yüksek idi.
Sonuç olarak CP’nin bağ
doku oluşumunu arttırdığı ve epitelizasyonun tamamlanması için gerekli zamanı
azalttığı, bu vesile ile yara iyileşmesini hızlandırdığı görülmüştür.

Kaynakça

  • Adamson B, Schwarz D, Klugston P, GilmontR, Perry L, Fisher J, Rees R (1996). Oxidant stress: the role of the glutathione redox cycle in skin preconditioning. J Surg Res, 62, 159-164. Adetutu, A, Morgan, W, Corcoran O (2011). Ethnopharmacological survey and in vitro evaluation of wound-healing plants used in South-western Nigeria. J Ethnopharmacol, 137, 50-56. Agarwal JP, Ogilvie M (2005). Vacuum-assisted closure for sternal wounds: a first-line therapeutic management approach. Plast Reconstr Surg, 116, 4, 1035-1040. Aksoy H, Özakpınar ÖB. (2014). Yara iyileşmesi ve oksidatif stres. Marmara Pharm J, 18, 153-158. Aydın S, Çağlıkülekçi M, Çolak T, Dirlik M, Öcal K, Akça T (2002). Washington Cerrahi El Kitabı, Nobel Tıp Kitabevleri. Calvin M (1998). Cutaneous wound healing. Wounds, 10, 1, 12-32. Candan İ (2003). Medikal Tedavi. Cilt 1. Antıp Yayınları. Ankara. 361-365. Czuczejko J, Zachara BA, Staubach-Topczewska E, Halota W, Kedziora J (2003). Selenium, glutathione and glutathione peroxidases in blood of patients with chronic liver diseases. Acta Biochim Pol, 50, 1147–1154. Çavdar C, Sifil, A, Çamsarı, T (1997). Reaktif oksijen türleri ve antioksidan savunma. Turk Neph Dial Transpl, 3, 92-95. Duarte T, Cooke M, Jones G (2009). Gene expression profiling reveals new protective rolesfor vitamin C in human skin cells. Adv Free Radical Bio, 46, 78– 87. Engin A (2004). Yara iyileşmesi In: Temel Cerrahi. Edited by Sayek, İ., 3. Baskı, pp: 266-277, Güneş Kitabevi, Ankara. Flanagan M (1994). Wound care. Assessment criteria. Nurs Times, 90, (45):77. 9-15 Gálvez M, Cordero CM, Lázaro, ML, Cortés F, Ayuso, MJ (2003). Cytotoxic effect of Plantago spp. on cancer cell lines. J Ethnopharmacol, 88, 125-130 . Grey JE, Enoch S, Harding KG (2006). Wound assessment. BMJ, 4, 332 (7536), 285-8. Güneş ÜY (2007). Kronik yaraların değerlendirilmesi. CÜ Hemşirelik Yüksekokulu Derg, 11 (3), 38-44. Hedlund CS (2002). Surgey of the integumentary system. In: Small Animal Surgery, 2th Edition, Edited by Fossum, T.W. Mosby, Printed in China, pp: 134-137 Heinze CD, Clem MF (1988). Wound healing and tissue repair. In: Textbook of Large Animal Surgery.2nd Ed., Edited by Oehme, F.W., pp:141-153 Williams& Wilkins USA. Herbette S, Roeckel-Drevet P, Drevet JR (2007). Seleno-independent glutathione peroxidases. More than simple antioxidant scavengers. FEBS J, 274, 2163–2180. Jain V, Prasad V, Pandey RS (2006). Wound healing activity of Desmodium gangeticum in Different Wound Model. J Plant Sci, 1(3), 247-253. Jurjus, A, Atiyeh BS, Abdallah IM, Jurjus RA, Hayek SN, Jaoude MA, Gerges A, Tohme RA (2007). Pharmacological modulation of wound healing in experimental burns. Burns, 33, 892-907. Kapan M, Aslanmirza MY, Karip AB, Bozkurt Y, Evsen MS, Sak E, Öngören AU (2008). Lokal fenitoin ve üre uygulamasının yara iyileşmesi üzerine olan etkilerinin karşılaştırılması. Yeni Tıp Derg, 25, 209-212. Kirsner, RS, Eaglsterin WH (1993). The wound healing process. Dermatol Clin, 11, 4, 629-640 Lakshmi T, Geetha R, Roy A, Aravind Kumar S (2011). Yarrow (Achillea Millefolium Linn) A Herbal Medicinal Plant with Broad Therapeutic Use–A Review. Int J Pharm Sci Rev Res, 9, 136-144. Munz B, Frank S, Hübner G, Olsen E, Werner S (1997). A novel type of glutathione peroxidase:expression and regulation during wound repair. Biochem J, 326, 579-85. Murnigsih T, Subeki H, Matsuura K, Takahashi M, Yamasaki O, Yamato Y, Maede K, Katakura M, Suzuki S, Kobayashi C, Yoshihara T (2005). Evaluation of the inhibitory activities of the extracts of Indonesian traditional medicinal plants against Plasmodium falciparum and Babesia gibsoni. J Vet Med Sci, 67, 829–831. Mustoe T (2004). Understanding chronic wounds: a unifying hypothesis on their pathogenesis and implications for therapy. Am J Surg, 187, 65–70. Özkorkmaz E, Özay Y (2009). Yara iyileşmesi ve yara iyileşmesinde kullanılan bazı bitkiler. Türk Bilimsel Derlemeler Dergisi 2, 63-67. Özler M, Şimşek K, Topal T, Öter Ş, Korkmaz A (2010). Pinealektomili ratlarda yara iyileşmesi. Gulhane Med J, 52, 181-184. Passalacqua N, Guarrera P, De Fine G (2007). Contribution to the knowledge of the folk plant medicine in Calabria region (Southern Italy). Fitoterapia, 78: 52-68. Pires JM, Mendes FR, Negri G, Duarte-Almeida JM, Carlini EA (2009). Anti noci-ceptive peripheral effect of Achillea millefolium L. and Artemisia vulgaris L, both plants known popularly by brand names of analgesic drugs. Phytother Res, 23, 212–219. Regan MC, Barbul A (1994). The cellular biology of wound healing. In: Wound Healing. Editedby Schlag, G., Redl, H. Vol:1 pp: 3-17 Springer-VerlagBerlin Heidelberg. Printed in Germany. Rigler DJ (1997). Inflamation and repair. In Veterinary Pathology, 6nd Ed., Edited by Jones, T.C.,Hunt, R.D., King, N.W., pp: 150-157, Williams &Wilkins, Pennsylvania. Rodrigues HG, Vinolo MA, Magdalon J, Vitzel K, Nachbar RT, Pessoa AF, dos Santos MF, Hatanaka E, Calder PC, Curi R (2012). Oral administration of oleic or linoleic acid accelerates the inflammatory phase of wound healing. J Invest Dermatol, 132, 1, 208-215. Saarialho-Kere UK (1992). Patterns of matrix metalloproteinase and TİMP expressionin chronic ulcers. Arch Dermatol Res, 290, 47-54. Sen CK, Roy S (2008). Redox signals in wound healing. Biochim Biophys Acta, 1780, 1348–1361. Souza de P, Gasparotto Jr. A, Crestania S, Stefanello MEA, Marques MCA, Silva-Santos JE, Kassuyaa CAL (2011). Hypotensive mechanism of the extracts and artemetin isolated from Achillea millefolium L.(Asterace) in rats. Phytomedicine, 18, 819–825. Stashak TS (1991). Principles of wound healing. In: Equine Wound Management, pp: 1-15, Lea&Febiger, Malvern, Pennsylvania. Steiling H, Munz B, Werner S, Brauchle M (1999). Different types of ROS scavenging enzymes are expressed during cutaneous wound repair. Exp Cell Res, 247, 484-94. Stojanović G, Radulović N, Hashimoto T, Palić R (2005). In vitro antimicrobial activity of extracts of four Achillea species, The composition of Achillea clavennae L. (Asteraceae) extract. J Ethnopharmacol, 101, 185–190. Swaim SF, Henderson RA (1990). Wound healing. In: Small Animal Wound Management. pp: 1-8,Lea & Febiger, Malvern, Pennsylvania. Theoret CL (2004). Update on wound repair, Clin Tech Equine Pract, 3, 110-122. Thomas AC, Wysocki AB (1990) The healing wound: a comparison of three clinically useful methods of measurement. Decubitus, 3,1,18-20, 24-5. Van Rijswijk L, Braden BJ (1999) Pressure ulcer patient and wound assessment: an AHCPR clinical practice guideline update. Ostomy Wound Manage, 45:56S-67S; quiz 68S-69S. Yaeesh S, Jamal Q, Khan AU, Gilani AH (2006). Studies on hepatoprotective, anti-spasmodic and calcium antagonist activities of the aqueous-methanol extract of Achillea millefolium. Phytother Res, 20, 546–551. Yager DR, Kulina RA, Gilman LA (2007). Wound fluids: a window into the wound environment? Int J Low Extrem Wounds, 6, 4, 262-272.
Toplam 1 adet kaynakça vardır.

Ayrıntılar

Birincil Dil Türkçe
Bölüm Makaleler
Yazarlar

Ahmet Uyar

Turgut Akyol Bu kişi benim

Turan Yaman

Ömer Faruk Keleş

Yayımlanma Tarihi 20 Aralık 2017
Gönderilme Tarihi 13 Kasım 2017
Kabul Tarihi 18 Aralık 2018
Yayımlandığı Sayı Yıl 2017 Cilt: 28 Sayı: 3

Kaynak Göster

APA Uyar, A., Akyol, T., Yaman, T., Keleş, Ö. F. (2017). Ratlarda Deneysel Olarak Oluşturulan Yara Modelinde Civanperçemi (Achillea millefolium) Bitkisinin Yara İyileşmesi ve Oksidatif Stres Üzerine Etkisinin Histopatolojik ve Biyokimyasal Olarak Araştırılması. Van Veterinary Journal, 28(3), 157-163.
AMA Uyar A, Akyol T, Yaman T, Keleş ÖF. Ratlarda Deneysel Olarak Oluşturulan Yara Modelinde Civanperçemi (Achillea millefolium) Bitkisinin Yara İyileşmesi ve Oksidatif Stres Üzerine Etkisinin Histopatolojik ve Biyokimyasal Olarak Araştırılması. Van Vet J. Aralık 2017;28(3):157-163.
Chicago Uyar, Ahmet, Turgut Akyol, Turan Yaman, ve Ömer Faruk Keleş. “Ratlarda Deneysel Olarak Oluşturulan Yara Modelinde Civanperçemi (Achillea Millefolium) Bitkisinin Yara İyileşmesi Ve Oksidatif Stres Üzerine Etkisinin Histopatolojik Ve Biyokimyasal Olarak Araştırılması”. Van Veterinary Journal 28, sy. 3 (Aralık 2017): 157-63.
EndNote Uyar A, Akyol T, Yaman T, Keleş ÖF (01 Aralık 2017) Ratlarda Deneysel Olarak Oluşturulan Yara Modelinde Civanperçemi (Achillea millefolium) Bitkisinin Yara İyileşmesi ve Oksidatif Stres Üzerine Etkisinin Histopatolojik ve Biyokimyasal Olarak Araştırılması. Van Veterinary Journal 28 3 157–163.
IEEE A. Uyar, T. Akyol, T. Yaman, ve Ö. F. Keleş, “Ratlarda Deneysel Olarak Oluşturulan Yara Modelinde Civanperçemi (Achillea millefolium) Bitkisinin Yara İyileşmesi ve Oksidatif Stres Üzerine Etkisinin Histopatolojik ve Biyokimyasal Olarak Araştırılması”, Van Vet J, c. 28, sy. 3, ss. 157–163, 2017.
ISNAD Uyar, Ahmet vd. “Ratlarda Deneysel Olarak Oluşturulan Yara Modelinde Civanperçemi (Achillea Millefolium) Bitkisinin Yara İyileşmesi Ve Oksidatif Stres Üzerine Etkisinin Histopatolojik Ve Biyokimyasal Olarak Araştırılması”. Van Veterinary Journal 28/3 (Aralık 2017), 157-163.
JAMA Uyar A, Akyol T, Yaman T, Keleş ÖF. Ratlarda Deneysel Olarak Oluşturulan Yara Modelinde Civanperçemi (Achillea millefolium) Bitkisinin Yara İyileşmesi ve Oksidatif Stres Üzerine Etkisinin Histopatolojik ve Biyokimyasal Olarak Araştırılması. Van Vet J. 2017;28:157–163.
MLA Uyar, Ahmet vd. “Ratlarda Deneysel Olarak Oluşturulan Yara Modelinde Civanperçemi (Achillea Millefolium) Bitkisinin Yara İyileşmesi Ve Oksidatif Stres Üzerine Etkisinin Histopatolojik Ve Biyokimyasal Olarak Araştırılması”. Van Veterinary Journal, c. 28, sy. 3, 2017, ss. 157-63.
Vancouver Uyar A, Akyol T, Yaman T, Keleş ÖF. Ratlarda Deneysel Olarak Oluşturulan Yara Modelinde Civanperçemi (Achillea millefolium) Bitkisinin Yara İyileşmesi ve Oksidatif Stres Üzerine Etkisinin Histopatolojik ve Biyokimyasal Olarak Araştırılması. Van Vet J. 2017;28(3):157-63.

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