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The Effects of Phlorizin on Serum Lipid Profile and Oxidative Stress Parameters in Sheep

Year 2014, Volume: 11 Issue: 1, 29 - 36, 01.03.2014

Abstract

The aim of this study was analyse the effect of phlorizin application on serum lipid prophile and oxidative stres indicators in sheep. Ten non-lactating and non-pregnant sheep were used in this study. Phlorizin was subcutanously injected at a dosage of 100 mg/kg to each animal. Body weight (BW) and subcutaneous fat thickness (SFT) were measured at the beginning and at the end of the study. Hematological, biochemical parameters including lipid prohile, and oxidative stress indicators were analysed in blood samples obtained before (0th hour) and 12., 24., 48., 72. and 120th hours after the study. Urine samples were analysed at the same time intervals. Liver biopsy materials were obtained from two sheep 24 hours before and after the study for histopathological examinations. Results indicate that phlorizin significantly decreased the mean BW, SFT, total leukocyte (WBC), insulin, glucose, blood urea nitrogene (BUN), creatinin, triglyceride (TG), alkaline phosphatase (ALP), lactate dehydrogenase (LDH), total oxidative status (TOS) ve oksidative stres index (OSI) values (p<0.05), and significantly increased the mean platelets (PLT), hemoglobin (Hgb) and non-esterified fatty acids (NEFA) values (p<0.05). Proteinuria and glycosuria were determined in urine samples. Histopathological examinations revealed a progressive decrease in cytoplasmic lipid vacuoles of hepatocytes after phlorizin administration. This study suggests that phlorizin could be proposed as an antihyperglycemic, antihiperlipidemic and antioxidant agent in sheep.

References

  • Aslan V, Aştı RN, Nizamlıoğlu M, Tekeli T, Başoğlu A. Demirci Ü. Postpartum dönem hastalıklarının yağlı karaciğer sendromu ile ilgisi. Selçuk Ü Vet Fak Derg 1989; 4(1): 43-51.
  • Aslan V, Aştı RN, Tiftik AM, Eksen M. Effect of niacin on blood metabolities, rumen protozoa, insulin levels and fatty liver in experimentally induced ketosis in ewes. Selçuk Ü Vet Fak Derg 1988; 4(1): 109-21.
  • Baldisserotto A, Malisardi G, Scalambra E, Andreotti E, Romagnoli C, Vicentini CB, Manfredini S, Vertuani S. Synthesis, antioxidant and antimicrobial activity of a new phloridzin derivative for dermo-cosmetic applications. Molecules 2012; 17(11): 13275-89.
  • Başoğlu A, Turgut K, Eksen M, Traş B, Maden M, Ok M, Baş L, Keskin E. Effect of phlorhizin ınduced ketosis on riboflavin and niacin levels in sheep. Selçuk Üniversitesi Vet Fak Derg 1993; 9(1): 58-63.
  • Boccia MM, Kopf SR, Baratti CM. Phlorizin, a competitive inhibitor of glucose transport, facilitates memory storage in mice. Neurobiol Learn Mem 1999; 71: 104-12.
  • Bradford BJ, Allen MS. Phlorizin induces lipolysis and alters meal patterns in both early and late lactation dairy cows. J Dairy Sci 2007; 90: 1810
  • Burtis CA, Jackson HD, Packett LV, Goetsch GD. Effects of glucagon, glycerol, and insulin on phlorizin induced ketosis in fasted, nonpregnant ewes. Am J Vet Res 1968; 29: 647.
  • Cai O, Li B, Yu F, Lu W, Zhang Z, Yin M, Gao H. Investigation of the protective effects of phlorizin on diabetic cardiomyopathy in db/db mice by quantitative proteomics. J Diabetes Res 2013; 1Cox SD, Jayasinghe KC, Markham JL. Antioxidant activity in Australian native sarsaparilla (Smilax glyciphylla). J Ethnopharmacol 2005; 101(1-3): 162Deng G, Wang J, Zhang Q, He H, Wu F, Feng
  • T, Zhou J, Zou K, Hattori M. Hepatoprotective effects of phlorizdzin on hepatic fibrosis induced by carbon tetrachloride againist oxidative stresstriggered damage and fibrosisin rats. Biol Pharm Bull 2012; 35(7): 1118-25.
  • Dong H, Ning Z, Yu L, Li L, Lin L, Huang J. Preparative separation and ıdentification of the flavonoid phlorhizin from the crude extract of Lithocarpus Polystachyus Rehd. Molecules 2007; 12(3): 552-62.
  • Ehrenkranz JRL, Lewis NG, Kahn CR, Roth J. Phlorizin: a review. Diabetes/ Metab Res Rev 2005; 21: 31-8.
  • Ghanem E, Robaye B, Leal T, Leipziger J, Van Driessche W, Beauwens R, Boeynaems JM. The role of epithelial P2Y(2) and P2Y(4) receptors in the regulation of intestinal chloride secretion. Brit J Pharm 2005; 146: 364-9.
  • Hall JL, Reilly RT, Cottrill KL, Stone WS, Gold PE. Phlorizin enhancement of memory in rats and mice. Pharmacol Biochem Behav 1992; 41(2): 295Herdt TH, Gerloff BJ. Hepatik lipidosis and liver function in 49 cows with displaced abomasum Twelfth World Congress on Diseases of Cattle. September, 7-10, 1984; Amsterdam-Hollanda.
  • Hilt P, Schieber A, Yildirim C, Arnold G, Klaiber I, Conrad JR, Beifuss U, Carle R. Detection of phloridzin in strawberries (Fragaria x ananassa Duch.) by HPLC-PDA-MS/MS and NMR spectroscopy. J Agric Food Chem 2003; 51: 2896Holtenius BK, Holtenius P. Effects of peroral alanine administration in lactating ewes with decreased availability of glucose. Br J Nut 1997; 78: 805-13.
  • Hutchinson A, Taper C, Towers G. Studies of phloridzin in malus. Can J Med Sci 1959; 37(7): 901Janssen SW, Martens GL, Sweep PN, Span PN, Verhofstad AAJ, Hermus ARMM. Phlorizin treatment prevents the decrease in plasma insulin levels but not the progressive histopathological changes in the pancreatic islets during aging of Zucker diabetic fatty rats. J Endocrinol Invest 2003; 26(6): 508-15.
  • Jervis EL, Johnson FR, Sheff MF, Smyth DH. The effect of phlorizin on intestinal absorption and intestinal phosphatase. J Physiol 1956; 134: 675.
  • Kıyıcı Şıklaroğlu R. Deneysel Ketozis Oluşturulan Koyunlarda Parenteral Lipid Emilsiyonlarının Tedavi Edici Etkilerinin Araştırılması. Doktora Tezi. Erciyes Üniv. Sağlık Bilimleri Enstitüsü, Veteriner İç Hastalıkları Programı. Kayseri-Türkiye, 2012.
  • Largis EE, Jacobs FA. Effects of phlorizin on glucose transport into blood and lymph. Biochim Biophys Acta 1971; 255: 301.
  • Lu WD, Li BY, Yu F, Cai Q, Zhang Z, Yin M, Gao HQ. Quantitative proteomics study on the protective mechanism of phlorizin on hepatic damage in diabetic db/db mice. Med Report 2012; 5(5): 1285-94.
  • Lyle RR, de Boer G, Mills SE, Russell RW, Beitz DC, Young JW. Glucose kinetics, plasma metabolites, and endocrine responses during Experimental ketoin in steers, J Dairy Sci 1984; 67(10): 2255-64.
  • Malatiali S, Francis I, Barac NM. Phlorizin prevents glomerular hyperfiltration but not hypertrophy in diabetic rats. Exp Diabetes Res 2008; 2008: 1-7.
  • McCrimmon R, Evans M, Jacob R, Fan X, Zhu Y, Shulman GI, Sherwin RS. AICAR and phlorizin reverse the hypoglycemia-specific defect in glucagon secretion in the diabetic BB rat. Am J Physiol Endocrinol Metab 2002; 283(5): 1076-83.
  • Mills SE, Lyle RR, Beitz DC, Young JW. In vitro hepatic gluconeogenesis during experimental ketosis produced in steers by 1,3-butanediol and phlorizin. J Dairy Sci 1984; 67: 2265-73.
  • Najafian M, Jahromi MZ, Nowroznejhad MJ, Khajeaian P, Kargar MM, Sadeghi M, Arasteh A. Phloridzin reduced blood glucose levels and improves lipids metabolism in streptozotocininduced diabetic rats. Mol Biol Rep 2012; 39: 5299-306.
  • Ohta T, Morinaga H, Yamamoto T, Yamada T. Effect of phlorizin on metabolic abnormalites in spontaneously diabetic torii (STD) rats. J Anim Sci 2012; 2(2): 113-8.
  • Osorio H, Bautista R, Rios A, Franco M, Arellano A, Vargas-Robles H, Romo E, Escalante B. Effect of phlorizin on SGLT2 expression in the kidney of diabetic rats. J Nephrol 2010; 23(5): 541-6.
  • Overton TR, Drackley JK, Otteman-Abbamonte CJ, Beaulieu AD, Clark JH. Metabolic adaptation to experimentally increased glucose demand in ruminants. J Anim Sci 1998; 76: 2938-46.
  • Panayotova-Heiermann M, Loo DDR, Wright EM. Kinetics of steady-state currents and charge movements associated with the rat Na+/glucose cotransporter. J Biol Chem 1995; 270: 2709910
  • Petersen C. Analyse des phloridzins. Ann Acad Sci France 1835; 15: 178. ‘Ehrenkranz JRL, Lewis NG, Kahn CR, Roth J. Phlorizin: a review.
  • Diabetes/ Metab Res Rev 2005; 21: 31-8.’
  • Puel C, Quintin A, Mathey J, Obled C, Davicco MJ, Lebecque P, Kati-Coulibaly S, Horcajada MN, Coxam V. Prevention of bone loss by phloridzin, an apple polyphenol, in ovariectomized rats under inflammation conditions. Calcif Tissue Int 2005; 77: 311-8.
  • Ridgway T, O’Reilly J, West G, Tucker G, Wiseman H. Antioxidant action of novel derivatives of the apple-derived flavonoid phloridzin compared to oestrogen; relevance to potential cardioprotective action. Biochem Soc Trans 1997; 106: 125.
  • Shen L, You BA, Gao HQ, Li BY, Yu F, Pei F. Effects of phlorizin on vascular complications in diabetes db/db mice. Chin Med J (Engl) 2012; 125(20): 3692-6.
  • Ugocsai K, Varga A, Molnar P, Antus S, Molnar J. Effects of selected flavonoids and carotenoids on drug accumulation and apoptosis induction in multidrug-resistant colon cancer cells expressing MDR1/LRP. In Vivo 2005; 19: 433-8.
  • Walle T, Walle UK. The beta-D-glucoside and sodium-dependent glucose transporter 1 (SGLT1)-inhibitor phloridzin is transported by both SGLT1 and multidrug resistance-associated proteins 1/2. Drug Metab Dispos 2003; 31: 12889
  • Van den Berghe G, Wouters P, Weekers F. Intensive insulin therapy in critically ill patients. N Engl J Med 2001; 345: 1359-67.
  • Veeriah S, Kautenburger T, Habermann N, Sauer J, Dietrich H, Will F, Pool-Zobel BL. Apple flavonoids inhibit growth of HT29 human colon cancer cells and modulate expression of genes involved in the biotransformation of xenobiotics. Mol Carcinogen 2006; 45: 164-74.
  • Young JW, Schmidt SP, Akawuah ES, Hess GS,. McGilliard AD. Effects of phlorizin on glucose kinetics in the bovine. J Dairy Sci 1974; 57: 689.
  • Zhao H, Yakar S, Gavrilova O, Sun H, Zhang Y, Kim H, Setser J, Jou W, LeRoith D. Phloridzin improves hyperglisemia but not hepatic insulin resistance in a transgenic mouse model of type 2 diabetes. Diabetes 2004; 53: 2901-9.

Koyunlarda Phlorizinin Serum Lipid Profili ve Oksidatif Stress Parametreleri Üzerine Etkisi

Year 2014, Volume: 11 Issue: 1, 29 - 36, 01.03.2014

Abstract

Bu çalışmanın amacı koyunlarda phlorizin uygulamasının serum lipid profili ve oksidatif stres indikatörleri üzerine etkinliğini araştırmaktı. Çalışmada 10 adet laktasyonda ve gebe olmayan koyun kullanıldı. Phlorizin 100 mg/kg dozunda her koyuna derialtı yolla enjekte edildi. Çalışma öncesi ve sonrasında koyunların canlı ağırlık (CA) ve sırt yağı kalınlığı (SYK) ölçüldü. Çalışmadan önceki (0. saat) ve sonraki 12., 24., 48., 72. ve 120. saatlerde alınan kan örneklerinde hematolojik analizler ve lipid profilini içeren biyokimyasal parametreler ve oksidatif stres indikatörleri analiz edildi. Aynı saatlerde idrar örnekleri de analiz edildi. Histopatolojik muayene için, çalışmadan 24 saat önce ve sonra iki adet koyundan karaciğer biyopsi örnekleri alındı. Çalışma sonucunda, phlorizinin ortalama CA, SYK, total lökosit (WBC), insülin, glukoz, kan üre nitrojen (BUN), kreatinin, trigliserit (TG), alkalen fosfataz (ALP), laktat dehidrogenaz (LDH), total oksidan seviye (TOS) ve oksidatif stres indeksi (OSI) değerlerini önemli ölçüde azalttığı (p<0.05) ve ortalama trombosit (PLT), hemoglobin (Hgb), esterleşmemiş yağ asitleri (NEFA) değerlerini ise önemli oranda artırdığı belirlendi (p<0.05). İdrar örneklerinde proteinüri ve glikozüri tespit edildi. Histopatolojik muayenede, phlorizin uygulamasından sonra hepatositlerin sitoplazmalarındaki yağ vakuollerinin sayısında azalma görüldü. Bu çalışma koyunlarda phlorizinin antihiperglisemik, antihiperlipidemik ve antioksidan olarak önerilebileceğini gösterdi.

References

  • Aslan V, Aştı RN, Nizamlıoğlu M, Tekeli T, Başoğlu A. Demirci Ü. Postpartum dönem hastalıklarının yağlı karaciğer sendromu ile ilgisi. Selçuk Ü Vet Fak Derg 1989; 4(1): 43-51.
  • Aslan V, Aştı RN, Tiftik AM, Eksen M. Effect of niacin on blood metabolities, rumen protozoa, insulin levels and fatty liver in experimentally induced ketosis in ewes. Selçuk Ü Vet Fak Derg 1988; 4(1): 109-21.
  • Baldisserotto A, Malisardi G, Scalambra E, Andreotti E, Romagnoli C, Vicentini CB, Manfredini S, Vertuani S. Synthesis, antioxidant and antimicrobial activity of a new phloridzin derivative for dermo-cosmetic applications. Molecules 2012; 17(11): 13275-89.
  • Başoğlu A, Turgut K, Eksen M, Traş B, Maden M, Ok M, Baş L, Keskin E. Effect of phlorhizin ınduced ketosis on riboflavin and niacin levels in sheep. Selçuk Üniversitesi Vet Fak Derg 1993; 9(1): 58-63.
  • Boccia MM, Kopf SR, Baratti CM. Phlorizin, a competitive inhibitor of glucose transport, facilitates memory storage in mice. Neurobiol Learn Mem 1999; 71: 104-12.
  • Bradford BJ, Allen MS. Phlorizin induces lipolysis and alters meal patterns in both early and late lactation dairy cows. J Dairy Sci 2007; 90: 1810
  • Burtis CA, Jackson HD, Packett LV, Goetsch GD. Effects of glucagon, glycerol, and insulin on phlorizin induced ketosis in fasted, nonpregnant ewes. Am J Vet Res 1968; 29: 647.
  • Cai O, Li B, Yu F, Lu W, Zhang Z, Yin M, Gao H. Investigation of the protective effects of phlorizin on diabetic cardiomyopathy in db/db mice by quantitative proteomics. J Diabetes Res 2013; 1Cox SD, Jayasinghe KC, Markham JL. Antioxidant activity in Australian native sarsaparilla (Smilax glyciphylla). J Ethnopharmacol 2005; 101(1-3): 162Deng G, Wang J, Zhang Q, He H, Wu F, Feng
  • T, Zhou J, Zou K, Hattori M. Hepatoprotective effects of phlorizdzin on hepatic fibrosis induced by carbon tetrachloride againist oxidative stresstriggered damage and fibrosisin rats. Biol Pharm Bull 2012; 35(7): 1118-25.
  • Dong H, Ning Z, Yu L, Li L, Lin L, Huang J. Preparative separation and ıdentification of the flavonoid phlorhizin from the crude extract of Lithocarpus Polystachyus Rehd. Molecules 2007; 12(3): 552-62.
  • Ehrenkranz JRL, Lewis NG, Kahn CR, Roth J. Phlorizin: a review. Diabetes/ Metab Res Rev 2005; 21: 31-8.
  • Ghanem E, Robaye B, Leal T, Leipziger J, Van Driessche W, Beauwens R, Boeynaems JM. The role of epithelial P2Y(2) and P2Y(4) receptors in the regulation of intestinal chloride secretion. Brit J Pharm 2005; 146: 364-9.
  • Hall JL, Reilly RT, Cottrill KL, Stone WS, Gold PE. Phlorizin enhancement of memory in rats and mice. Pharmacol Biochem Behav 1992; 41(2): 295Herdt TH, Gerloff BJ. Hepatik lipidosis and liver function in 49 cows with displaced abomasum Twelfth World Congress on Diseases of Cattle. September, 7-10, 1984; Amsterdam-Hollanda.
  • Hilt P, Schieber A, Yildirim C, Arnold G, Klaiber I, Conrad JR, Beifuss U, Carle R. Detection of phloridzin in strawberries (Fragaria x ananassa Duch.) by HPLC-PDA-MS/MS and NMR spectroscopy. J Agric Food Chem 2003; 51: 2896Holtenius BK, Holtenius P. Effects of peroral alanine administration in lactating ewes with decreased availability of glucose. Br J Nut 1997; 78: 805-13.
  • Hutchinson A, Taper C, Towers G. Studies of phloridzin in malus. Can J Med Sci 1959; 37(7): 901Janssen SW, Martens GL, Sweep PN, Span PN, Verhofstad AAJ, Hermus ARMM. Phlorizin treatment prevents the decrease in plasma insulin levels but not the progressive histopathological changes in the pancreatic islets during aging of Zucker diabetic fatty rats. J Endocrinol Invest 2003; 26(6): 508-15.
  • Jervis EL, Johnson FR, Sheff MF, Smyth DH. The effect of phlorizin on intestinal absorption and intestinal phosphatase. J Physiol 1956; 134: 675.
  • Kıyıcı Şıklaroğlu R. Deneysel Ketozis Oluşturulan Koyunlarda Parenteral Lipid Emilsiyonlarının Tedavi Edici Etkilerinin Araştırılması. Doktora Tezi. Erciyes Üniv. Sağlık Bilimleri Enstitüsü, Veteriner İç Hastalıkları Programı. Kayseri-Türkiye, 2012.
  • Largis EE, Jacobs FA. Effects of phlorizin on glucose transport into blood and lymph. Biochim Biophys Acta 1971; 255: 301.
  • Lu WD, Li BY, Yu F, Cai Q, Zhang Z, Yin M, Gao HQ. Quantitative proteomics study on the protective mechanism of phlorizin on hepatic damage in diabetic db/db mice. Med Report 2012; 5(5): 1285-94.
  • Lyle RR, de Boer G, Mills SE, Russell RW, Beitz DC, Young JW. Glucose kinetics, plasma metabolites, and endocrine responses during Experimental ketoin in steers, J Dairy Sci 1984; 67(10): 2255-64.
  • Malatiali S, Francis I, Barac NM. Phlorizin prevents glomerular hyperfiltration but not hypertrophy in diabetic rats. Exp Diabetes Res 2008; 2008: 1-7.
  • McCrimmon R, Evans M, Jacob R, Fan X, Zhu Y, Shulman GI, Sherwin RS. AICAR and phlorizin reverse the hypoglycemia-specific defect in glucagon secretion in the diabetic BB rat. Am J Physiol Endocrinol Metab 2002; 283(5): 1076-83.
  • Mills SE, Lyle RR, Beitz DC, Young JW. In vitro hepatic gluconeogenesis during experimental ketosis produced in steers by 1,3-butanediol and phlorizin. J Dairy Sci 1984; 67: 2265-73.
  • Najafian M, Jahromi MZ, Nowroznejhad MJ, Khajeaian P, Kargar MM, Sadeghi M, Arasteh A. Phloridzin reduced blood glucose levels and improves lipids metabolism in streptozotocininduced diabetic rats. Mol Biol Rep 2012; 39: 5299-306.
  • Ohta T, Morinaga H, Yamamoto T, Yamada T. Effect of phlorizin on metabolic abnormalites in spontaneously diabetic torii (STD) rats. J Anim Sci 2012; 2(2): 113-8.
  • Osorio H, Bautista R, Rios A, Franco M, Arellano A, Vargas-Robles H, Romo E, Escalante B. Effect of phlorizin on SGLT2 expression in the kidney of diabetic rats. J Nephrol 2010; 23(5): 541-6.
  • Overton TR, Drackley JK, Otteman-Abbamonte CJ, Beaulieu AD, Clark JH. Metabolic adaptation to experimentally increased glucose demand in ruminants. J Anim Sci 1998; 76: 2938-46.
  • Panayotova-Heiermann M, Loo DDR, Wright EM. Kinetics of steady-state currents and charge movements associated with the rat Na+/glucose cotransporter. J Biol Chem 1995; 270: 2709910
  • Petersen C. Analyse des phloridzins. Ann Acad Sci France 1835; 15: 178. ‘Ehrenkranz JRL, Lewis NG, Kahn CR, Roth J. Phlorizin: a review.
  • Diabetes/ Metab Res Rev 2005; 21: 31-8.’
  • Puel C, Quintin A, Mathey J, Obled C, Davicco MJ, Lebecque P, Kati-Coulibaly S, Horcajada MN, Coxam V. Prevention of bone loss by phloridzin, an apple polyphenol, in ovariectomized rats under inflammation conditions. Calcif Tissue Int 2005; 77: 311-8.
  • Ridgway T, O’Reilly J, West G, Tucker G, Wiseman H. Antioxidant action of novel derivatives of the apple-derived flavonoid phloridzin compared to oestrogen; relevance to potential cardioprotective action. Biochem Soc Trans 1997; 106: 125.
  • Shen L, You BA, Gao HQ, Li BY, Yu F, Pei F. Effects of phlorizin on vascular complications in diabetes db/db mice. Chin Med J (Engl) 2012; 125(20): 3692-6.
  • Ugocsai K, Varga A, Molnar P, Antus S, Molnar J. Effects of selected flavonoids and carotenoids on drug accumulation and apoptosis induction in multidrug-resistant colon cancer cells expressing MDR1/LRP. In Vivo 2005; 19: 433-8.
  • Walle T, Walle UK. The beta-D-glucoside and sodium-dependent glucose transporter 1 (SGLT1)-inhibitor phloridzin is transported by both SGLT1 and multidrug resistance-associated proteins 1/2. Drug Metab Dispos 2003; 31: 12889
  • Van den Berghe G, Wouters P, Weekers F. Intensive insulin therapy in critically ill patients. N Engl J Med 2001; 345: 1359-67.
  • Veeriah S, Kautenburger T, Habermann N, Sauer J, Dietrich H, Will F, Pool-Zobel BL. Apple flavonoids inhibit growth of HT29 human colon cancer cells and modulate expression of genes involved in the biotransformation of xenobiotics. Mol Carcinogen 2006; 45: 164-74.
  • Young JW, Schmidt SP, Akawuah ES, Hess GS,. McGilliard AD. Effects of phlorizin on glucose kinetics in the bovine. J Dairy Sci 1974; 57: 689.
  • Zhao H, Yakar S, Gavrilova O, Sun H, Zhang Y, Kim H, Setser J, Jou W, LeRoith D. Phloridzin improves hyperglisemia but not hepatic insulin resistance in a transgenic mouse model of type 2 diabetes. Diabetes 2004; 53: 2901-9.
There are 39 citations in total.

Details

Primary Language Turkish
Journal Section Articles
Authors

İ. Karaca Bekdik

A. C. Onmaz This is me

Publication Date March 1, 2014
Submission Date June 24, 2014
Published in Issue Year 2014 Volume: 11 Issue: 1

Cite

APA Bekdik, İ. K., & Onmaz, A. C. (2014). Koyunlarda Phlorizinin Serum Lipid Profili ve Oksidatif Stress Parametreleri Üzerine Etkisi. Erciyes Üniversitesi Veteriner Fakültesi Dergisi, 11(1), 29-36.
AMA Bekdik İK, Onmaz AC. Koyunlarda Phlorizinin Serum Lipid Profili ve Oksidatif Stress Parametreleri Üzerine Etkisi. Erciyes Üniv Vet Fak Derg. March 2014;11(1):29-36.
Chicago Bekdik, İ. Karaca, and A. C. Onmaz. “Koyunlarda Phlorizinin Serum Lipid Profili Ve Oksidatif Stress Parametreleri Üzerine Etkisi”. Erciyes Üniversitesi Veteriner Fakültesi Dergisi 11, no. 1 (March 2014): 29-36.
EndNote Bekdik İK, Onmaz AC (March 1, 2014) Koyunlarda Phlorizinin Serum Lipid Profili ve Oksidatif Stress Parametreleri Üzerine Etkisi. Erciyes Üniversitesi Veteriner Fakültesi Dergisi 11 1 29–36.
IEEE İ. K. Bekdik and A. C. Onmaz, “Koyunlarda Phlorizinin Serum Lipid Profili ve Oksidatif Stress Parametreleri Üzerine Etkisi”, Erciyes Üniv Vet Fak Derg, vol. 11, no. 1, pp. 29–36, 2014.
ISNAD Bekdik, İ. Karaca - Onmaz, A. C. “Koyunlarda Phlorizinin Serum Lipid Profili Ve Oksidatif Stress Parametreleri Üzerine Etkisi”. Erciyes Üniversitesi Veteriner Fakültesi Dergisi 11/1 (March 2014), 29-36.
JAMA Bekdik İK, Onmaz AC. Koyunlarda Phlorizinin Serum Lipid Profili ve Oksidatif Stress Parametreleri Üzerine Etkisi. Erciyes Üniv Vet Fak Derg. 2014;11:29–36.
MLA Bekdik, İ. Karaca and A. C. Onmaz. “Koyunlarda Phlorizinin Serum Lipid Profili Ve Oksidatif Stress Parametreleri Üzerine Etkisi”. Erciyes Üniversitesi Veteriner Fakültesi Dergisi, vol. 11, no. 1, 2014, pp. 29-36.
Vancouver Bekdik İK, Onmaz AC. Koyunlarda Phlorizinin Serum Lipid Profili ve Oksidatif Stress Parametreleri Üzerine Etkisi. Erciyes Üniv Vet Fak Derg. 2014;11(1):29-36.