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Glifosat Bazlı Herbisite Maruz Kalan Sıçanlarda N-Asetilsisteinin Testis Oksidatif Hasarı, Spermatolojik Parametreler ve DNA Hasarı Üzerindeki Koruyucu Etkisi

Yıl 2018, , 292 - 300, 01.09.2018
https://doi.org/10.30607/kvj.435112

Öz

Bu çalışmanın amacı,
N-asetilsisteinin (NAC) sıçanlarda Glifosat (GLF) 'nin neden olduğu testiküler
oksidatif hasar, spermatolojik parametreler ve DNA hasarı üzerindeki koruyucu
etkisini incelemektir. Toplam yirmi sekiz Wistar erkek sıçan, eşit bir şekilde
dört gruba ayrılarak değerlendirildi. Kontrol grubunu olan grup I'deki
sıçanlar, GLF veya NAC olmaksızın normal diyetle beslendiler, grup II’deki
hayvanlara 160 mg / kg / günlük NAC içeren normal rat diyeti uygulandı, grup
III’deki hayvanlara 375 mg / kg / günlük GLF içeren normal rat diyeti verildi
ve grup IV’deki hayvanlara 160 mg / kg / günlük NAC + 375 mg / kg / günlük GLF
içeren normal rat diyeti uygulandı. GLF uygulaması sıçanların testis dokusunda
spermatozoon motilitesini, anormal spermatozoon oranını, spermatozoon plazma
membran bütünlüğünü, glutatyon ve süperoksit dismutaz düzeyini azaltmıştır.
Diğer taraftan GLF uygulanan grupta yüksek malondialdehid düzeyi ve DNA hasarı
saptandı. Ayrıca histopatolojik olarak testis dokusunda spermatozoon
konsantrasyonunda azalma ve sertoli hücrelerin dejenerasyonu belirlendi. NAC ve
NAC + GLF uygulaması, lipid peroksidasyonunu ve GLF tarafından indüklenen DNA
hasarını, sıçanların testislerinde antioksidan enzimlerin aktivitesini ve hücre
bütünlüğünü tersine çevirdi. Yukarıda belirtilen bulgular, NAC'nin GLF'nin
neden olduğu lipit peroksidasyonunu azalttığını, antioksidan savunma
mekanizmasını geliştirdiğini ve sıçanların testislerinde doku hasarını rejenere
ettiğini göstermektedir.

Kaynakça

  • Aebi, H. Catalase in vitro. Methods Enzymol. 1984; 105: 121–126.
  • Aitken RJ, Buckingham D, Harris D. Use of a xanthine oxidase oxidant generating system to investigate the cytotoxic effects of reactive oxygen species on human spermatozoa. J Reprod Fertil. 1993; 97: 441-450.
  • Akiyama M. In vivo scavenging effect of ethylcysteine on reactive oxygen species in human semen]. Nippon Hinyokika Gakkai Zasshi. 1999; 90: 421-428.
  • Arı UÇ, Kulaksız R, Öztürkler Y, Lehimcioğlu NC, Yıldız S. Effect of N-Acetylcysteine (NAC) on Post-thaw Semen Quality of Tushin Rams. Kafkas Üniv Vet Fak Derg. 2016; 22(6): 883-887.
  • Baker GHW, Brindle J, Irvine SD, Aitken RJ. Protective effect of antioxidants on the impairment of sperm motility by activated polymorphonuclear leukocytes. Fertil Steril. 1996; 65: 411–419.
  • Beutler E, Duron O, Kelly BM. Improved method for the determination of blood glutathione. J Lab Clin Med. 1963; 61: 882–888.
  • Bhide MB. Report on Effect of Pesticides on Reproductive Process – Segment IV – Three Generation Reproduction Study with Albino Rats Using Glyphosate Technical of Excel Industries Ltd. 1988; Bombay. BVL-2328485: TOX955.
  • Bohm GM, Genovese MI, Pigosso G, Trichez V, Rombaldi CV. Residues of glyphosate and aminomethylphosphonic acid and levels of isoflavones in BRS 244 RR and BRS 154 soybean. Food Sci. Technol. 2008; 28: 192-197.
  • Çiftci H, Verit A, Savaş M, Yeni E, Erel O. Effects of N-acetylcysteine on Semen Parameters and Oxidative/Antioxidant Status. Urology. 2009; 74: 73–76.
  • Clair E, Mesnage R, Travert C, Séralini GE. A glyphosate-based herbicide induces necrosis and apoptosis in mature rat testicular cells in vitro and testosterone decrease at lower levels. Toxicol. InVitro. 2012; 26: 269–279.
  • Cocco T, Sgobbo P, Clemente M, Lopriore B, Grattagliano I, Di Paola M, et al. Tissue-specific changes of mitochondrial functions in aged rats: effect of a long-term dietary treatment with Nacetylcysteine. Free Radic Biol Med. 2005; 38: 796–805.
  • Dallegrave E, Mantese FD, Oliveira RT, Andrade AJ, Dalsenter PR. Langeloh APre-and postnatal toxicity of the commercial glyphosate formulationin Wistar rats. Arch. Toxicol. 2007; 81: 665–673.
  • De Liz Oliveira Cavalli VL, Cattani D, Elise Heinz Rieg C, Pierozan P, Zanatta L, Benedetti Parisotto E, Wilhelm Filho D, Regina Mena Barreto Silva F, Pessoa- Pureur R, Zamoner A. Roundup disrupted male reproductive functions by triggering calcium-mediated cell death in rat testis and sertoli cells. Free Radic. Biol. Med. 2013; 65: 335-346.
  • Ducci M, Gaazano A, Villani C, Cela V, Artini PG, Martelli F, Genazzani AR. Membrane integrity evaluation in rabbit spermatozoa. Eur. J. Obstet. Gynaecol. Reprod. Biol. 2002; 102: 53-56.
  • Erkkila K, Hirvonen V, Wuokko E, Parvinen M, Dunkel L. N-Acetyl-L-Cysteine inhibits apoptosis in human male germ cells in vitro. Journal of Clinical Endocrinology and Metabolism. 1998; 83(7): 2523-2531.
  • Farombi EO, Ugwuezunmba MC, Ezenwadu TT, Oyeyemi MO, Ekor M. Tetracycline-induced reproductive toxicity in male rats: Effects of vitamin C and N-acetylcysteine. Experimental and Toxicologic Pathology. 2008; 60: 77–85.
  • Feron VJ, Cassee FR, Groten JP, van Vliet PW, van Zorge JA. International issues on human health effects of exposure to chemical mixtures. Environ. Health Perspect. 2002; 110: 893–899.
  • Fukui Y, Togawa M, Abe N, Takano Y, Asada M, Okada A, Iida K, Ishikawa H, Ohsumi S. Validation of sperm quality analyzer and the hypo-osmotic swelling test for frozen-thawed ram and minke whale (Balaenoptera bonarensi) spermatozoa. J. of Reprod. And Dev. 2004; 50: 147-154.
  • Gehin A, Guyon C, Nicod L. Glyphosate-induced antioxidant imbalance in HaCaT: the protective effect of vitamins C and E. Environ.Toxicol.Pharmacol. 2006; 22: 27–34.
  • Gündoğan M, Yeni D, Avdatek F, Fidan AF. Influence of sperm concentration on the motility, morphology, membrane and DNA integrity along with oxidative stress parameters of ram sperm during liquid storage. Animal Reproduction Science. 2010; 122: 200–207.
  • Hancock JL. The Morphology of Bull Spermatozoa. J Exp Biol. 1952; 29: 445–53.
  • Jasper R., Locatelli GO, Pilati C, Locatelli C. Evaluation of biochemical, hematological and oxidative parameters in mice exposed to the herbicide glyphosate Roundup® . Interdiscip. Toxicol. 2012; 5(3): 133–140.
  • Küçükkurt I, Ince S, Fidan AF, Özdemir A. The effects of dietary supplementation of different amount of Yucca schidigera powder (Sarsaponin 30) on blood and tissue antioxidant defense systems and lipid peroxidation in rats. J Anim Vet Adv. 2008; 7: 1413–1417.
  • Kumaravel TS, Jha AN. Reliable Comet assay measurements for detecting DNA damage induced by ionising radiation and chemicals. Mutat Res. 2006; 605: 7–16.
  • Li Ji Y, Wang H, Zhang C, Zhang Y, Zhao M, Chen YH, Xu DX. N-acetylcysteine protects against cadmium-induced germ cell apoptosis by inhibiting endoplasmic reticulum stress in testes. Asian Journal of Andrology. 2013; 15: 290–296.
  • Lopes FM, Varela Juniora AS, Corcini CD, Cardoso da Silva A, Guazzelli VG, Tavares G, Eduardo da Rosaa C. Effect of glyphosate on the sperm quality of zebrafish Danio rerio. Aquatic Toxicology. 2014; 155: 322–326.
  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951; 193: 265–275. Mansour MM. Modification of hypo-osmotic swelling test to evaluate the integrity of stallion sperm plasma membrane. Glob. Vet. 2009; 3: 302-307.
  • Martha T, Majed AA, Tanuja B, et al. Effect of aqueous extract of onion on the liver and lung of rats. J Ethnopharmacol. 1998; 61(2): 91-99.
  • Meister A. Glutathione deficiency produced by inhibition of its synthesis, andits reversal; applications in research and therapy, Pharmacol. Ther. 1991; 51: 155–194.
  • Michael AJ, Alexopoulos C, Pontiki EA, Hadjipavlou-Litina DJ, Saratsis P, Ververidis HN, et al. Effect of antioxidant supplementation in semen extenders on semen quality and reactive oxygen species of chilled canine spermatozoa. Anim Reprod Sci. 2009; 112: 119–35.
  • Nithya R, Elango V. Pesticide effect in male hormones and antioxidant status in male albino rats. J. Acad. Ind. Res. 2015; 4(4): 140–143.
  • Oeda T, Henkel R, Ohmori H. et al. Scavenging effect of N-acetyl-L-cysteine against reactive oxygen species in human semen: a possible therapeutic modality for male factor infertility? Andrologia. 1997; 29: 125-131.
  • Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem, 1979; 95: 351–358.
  • Partyka A, Niżański W, Bratkowska M, Maślikowski P. Effects of N-acetyl-L-cysteine and catalase on the viability and motility of chicken sperm during liquid storage. Reproductive Biology. 2015; 15: 126-129.
  • Raina R, Verma PK, Pankaj NK, Kant V. Ameliorative effect of alpha tocopherol on cypermethrin‑induced oxidative stress and lipid peroxidation in Wistar rats. Int J Med Med Sci. 2009a; 1: 396‑9.
  • Raina R, Verma PK, Pankaj NK, Prawez S. Induction of oxidative stres and lipid peroxidation in rats chronically exposed to cypermethrin through dermal application. J Vet Sci. 2009b; 10: 257‑9.
  • Reddy PS, Rani GP, Sainath SB, Meena R, Supriya Ch. Protective effects of N-acetylcysteine against arsenic-induced oxidative stres and reprotoxicity in male mice. Journal of Trace Elements in Medicine and Biology. 2011; 25: 247– 253.
  • Richard S, Moslemi S, Sipahutar H, Benachour N, Séralini GE. Differential effects of glyphosate and Roundup on human placental cells and aromatase. Environ. Health Perspect. 2005; 113: 716–720.
  • Romano RM, Romano MA, Bernardi MM, Furtado P, Oliveira CA. Prepubertal exposure to commercial formulation of the herbicide glyphosatealters testosterone levels and testicular morphology. Arch. Toxicol. 2010; 84: 309–317.
  • Sönmez M, Türk G, Yüce A. The effect of ascorbic acid supplementation on sperm quality, lipid peroxidation and testosterone levels of male Wistar rats. Theriogenology. 2005; 63: 2063–72.
  • Sun Y, Oberley LW, Li Y. A simple method for clinical assay of superoxide dismutase. Clin Chem. 1988; 34: 497–500.
  • Takahashi M, Horie M, Aoba N. Analysis of glyphosate and its metabolite, aminomethylphosphonic acid, in agricultural products by HPLC. Shokuhin Eiseigaku Zasshi. 2001; 42: 304–308.
  • Whitaker BD, Casey SJ, Taupier R. N-acetyl-L-cysteine Supplementation Improves Boar Spermatozoa Characteristics and Subsequent Fertilization and Embryonic Development. Reprod Dom Anim. 2012; 47: 263–268.
  • Yıldız S, Öztürkler Y, Arı UÇ, Lehimcioğlu NC, Atakişi E, Kulaksız R. The effects of L-ergothioneine, N-acetylcystein and cystein on freezing of ram semen. Kafkas Univ Vet Fak Derg. 2015; 21: 81-86.

Protective Effect of N-Acetylcysteine on Testicular Oxidative Damage, Spermatological Parameters and DNA Damage in Glyphosate-Based Herbicide-Exposed Rats

Yıl 2018, , 292 - 300, 01.09.2018
https://doi.org/10.30607/kvj.435112

Öz

The aim of this
study was to examine the protective effect of N-acetylcysteine (NAC) on
testicular oxidative damage, spermatological parameters and DNA damage caused
by Glyphosate (GLF) in rats.
In
total, twenty-eight
Wistar male
rats were evaluated by being separated into four groups in an equal way. Rats
in group I, which represented the control
group, were fed normal diet without GLF
or NAC, group II received normal feed containing
160 mg/kg/daily NAC, group III received normal feed containing 375 mg/kg/daily
GLF, and group IV received normal feed containing 160 mg/kg/daily NAC + 375
mg/kg/daily GLF. GLF administration decreased sperm motility, abnormal
sperm rate, sperm plasma membrane integrity,
glutathione level and superoxide dismutase in the rats’ testicular tissue. On
the other hand, high malondialdehyde level and DNA damage were detected in the
group administered with GLF. Besides, in histopathological terms, a decrease in
sperm concentration and degeneration of sertoli cells were determined in the
testicular tissue. NAC and NAC+GLF administration reversed lipid peroxidation
and DNA damage induced by GLF, the activity
of antioxidant enzymes and cell integrity in rats’ testis. The above-mentioned
findings indicate that NAC reduces lipid peroxidation caused by GLF, improves
the antioxidant defense mechanism and regenerates tissue damage in rats’
testis.

Kaynakça

  • Aebi, H. Catalase in vitro. Methods Enzymol. 1984; 105: 121–126.
  • Aitken RJ, Buckingham D, Harris D. Use of a xanthine oxidase oxidant generating system to investigate the cytotoxic effects of reactive oxygen species on human spermatozoa. J Reprod Fertil. 1993; 97: 441-450.
  • Akiyama M. In vivo scavenging effect of ethylcysteine on reactive oxygen species in human semen]. Nippon Hinyokika Gakkai Zasshi. 1999; 90: 421-428.
  • Arı UÇ, Kulaksız R, Öztürkler Y, Lehimcioğlu NC, Yıldız S. Effect of N-Acetylcysteine (NAC) on Post-thaw Semen Quality of Tushin Rams. Kafkas Üniv Vet Fak Derg. 2016; 22(6): 883-887.
  • Baker GHW, Brindle J, Irvine SD, Aitken RJ. Protective effect of antioxidants on the impairment of sperm motility by activated polymorphonuclear leukocytes. Fertil Steril. 1996; 65: 411–419.
  • Beutler E, Duron O, Kelly BM. Improved method for the determination of blood glutathione. J Lab Clin Med. 1963; 61: 882–888.
  • Bhide MB. Report on Effect of Pesticides on Reproductive Process – Segment IV – Three Generation Reproduction Study with Albino Rats Using Glyphosate Technical of Excel Industries Ltd. 1988; Bombay. BVL-2328485: TOX955.
  • Bohm GM, Genovese MI, Pigosso G, Trichez V, Rombaldi CV. Residues of glyphosate and aminomethylphosphonic acid and levels of isoflavones in BRS 244 RR and BRS 154 soybean. Food Sci. Technol. 2008; 28: 192-197.
  • Çiftci H, Verit A, Savaş M, Yeni E, Erel O. Effects of N-acetylcysteine on Semen Parameters and Oxidative/Antioxidant Status. Urology. 2009; 74: 73–76.
  • Clair E, Mesnage R, Travert C, Séralini GE. A glyphosate-based herbicide induces necrosis and apoptosis in mature rat testicular cells in vitro and testosterone decrease at lower levels. Toxicol. InVitro. 2012; 26: 269–279.
  • Cocco T, Sgobbo P, Clemente M, Lopriore B, Grattagliano I, Di Paola M, et al. Tissue-specific changes of mitochondrial functions in aged rats: effect of a long-term dietary treatment with Nacetylcysteine. Free Radic Biol Med. 2005; 38: 796–805.
  • Dallegrave E, Mantese FD, Oliveira RT, Andrade AJ, Dalsenter PR. Langeloh APre-and postnatal toxicity of the commercial glyphosate formulationin Wistar rats. Arch. Toxicol. 2007; 81: 665–673.
  • De Liz Oliveira Cavalli VL, Cattani D, Elise Heinz Rieg C, Pierozan P, Zanatta L, Benedetti Parisotto E, Wilhelm Filho D, Regina Mena Barreto Silva F, Pessoa- Pureur R, Zamoner A. Roundup disrupted male reproductive functions by triggering calcium-mediated cell death in rat testis and sertoli cells. Free Radic. Biol. Med. 2013; 65: 335-346.
  • Ducci M, Gaazano A, Villani C, Cela V, Artini PG, Martelli F, Genazzani AR. Membrane integrity evaluation in rabbit spermatozoa. Eur. J. Obstet. Gynaecol. Reprod. Biol. 2002; 102: 53-56.
  • Erkkila K, Hirvonen V, Wuokko E, Parvinen M, Dunkel L. N-Acetyl-L-Cysteine inhibits apoptosis in human male germ cells in vitro. Journal of Clinical Endocrinology and Metabolism. 1998; 83(7): 2523-2531.
  • Farombi EO, Ugwuezunmba MC, Ezenwadu TT, Oyeyemi MO, Ekor M. Tetracycline-induced reproductive toxicity in male rats: Effects of vitamin C and N-acetylcysteine. Experimental and Toxicologic Pathology. 2008; 60: 77–85.
  • Feron VJ, Cassee FR, Groten JP, van Vliet PW, van Zorge JA. International issues on human health effects of exposure to chemical mixtures. Environ. Health Perspect. 2002; 110: 893–899.
  • Fukui Y, Togawa M, Abe N, Takano Y, Asada M, Okada A, Iida K, Ishikawa H, Ohsumi S. Validation of sperm quality analyzer and the hypo-osmotic swelling test for frozen-thawed ram and minke whale (Balaenoptera bonarensi) spermatozoa. J. of Reprod. And Dev. 2004; 50: 147-154.
  • Gehin A, Guyon C, Nicod L. Glyphosate-induced antioxidant imbalance in HaCaT: the protective effect of vitamins C and E. Environ.Toxicol.Pharmacol. 2006; 22: 27–34.
  • Gündoğan M, Yeni D, Avdatek F, Fidan AF. Influence of sperm concentration on the motility, morphology, membrane and DNA integrity along with oxidative stress parameters of ram sperm during liquid storage. Animal Reproduction Science. 2010; 122: 200–207.
  • Hancock JL. The Morphology of Bull Spermatozoa. J Exp Biol. 1952; 29: 445–53.
  • Jasper R., Locatelli GO, Pilati C, Locatelli C. Evaluation of biochemical, hematological and oxidative parameters in mice exposed to the herbicide glyphosate Roundup® . Interdiscip. Toxicol. 2012; 5(3): 133–140.
  • Küçükkurt I, Ince S, Fidan AF, Özdemir A. The effects of dietary supplementation of different amount of Yucca schidigera powder (Sarsaponin 30) on blood and tissue antioxidant defense systems and lipid peroxidation in rats. J Anim Vet Adv. 2008; 7: 1413–1417.
  • Kumaravel TS, Jha AN. Reliable Comet assay measurements for detecting DNA damage induced by ionising radiation and chemicals. Mutat Res. 2006; 605: 7–16.
  • Li Ji Y, Wang H, Zhang C, Zhang Y, Zhao M, Chen YH, Xu DX. N-acetylcysteine protects against cadmium-induced germ cell apoptosis by inhibiting endoplasmic reticulum stress in testes. Asian Journal of Andrology. 2013; 15: 290–296.
  • Lopes FM, Varela Juniora AS, Corcini CD, Cardoso da Silva A, Guazzelli VG, Tavares G, Eduardo da Rosaa C. Effect of glyphosate on the sperm quality of zebrafish Danio rerio. Aquatic Toxicology. 2014; 155: 322–326.
  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951; 193: 265–275. Mansour MM. Modification of hypo-osmotic swelling test to evaluate the integrity of stallion sperm plasma membrane. Glob. Vet. 2009; 3: 302-307.
  • Martha T, Majed AA, Tanuja B, et al. Effect of aqueous extract of onion on the liver and lung of rats. J Ethnopharmacol. 1998; 61(2): 91-99.
  • Meister A. Glutathione deficiency produced by inhibition of its synthesis, andits reversal; applications in research and therapy, Pharmacol. Ther. 1991; 51: 155–194.
  • Michael AJ, Alexopoulos C, Pontiki EA, Hadjipavlou-Litina DJ, Saratsis P, Ververidis HN, et al. Effect of antioxidant supplementation in semen extenders on semen quality and reactive oxygen species of chilled canine spermatozoa. Anim Reprod Sci. 2009; 112: 119–35.
  • Nithya R, Elango V. Pesticide effect in male hormones and antioxidant status in male albino rats. J. Acad. Ind. Res. 2015; 4(4): 140–143.
  • Oeda T, Henkel R, Ohmori H. et al. Scavenging effect of N-acetyl-L-cysteine against reactive oxygen species in human semen: a possible therapeutic modality for male factor infertility? Andrologia. 1997; 29: 125-131.
  • Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem, 1979; 95: 351–358.
  • Partyka A, Niżański W, Bratkowska M, Maślikowski P. Effects of N-acetyl-L-cysteine and catalase on the viability and motility of chicken sperm during liquid storage. Reproductive Biology. 2015; 15: 126-129.
  • Raina R, Verma PK, Pankaj NK, Kant V. Ameliorative effect of alpha tocopherol on cypermethrin‑induced oxidative stress and lipid peroxidation in Wistar rats. Int J Med Med Sci. 2009a; 1: 396‑9.
  • Raina R, Verma PK, Pankaj NK, Prawez S. Induction of oxidative stres and lipid peroxidation in rats chronically exposed to cypermethrin through dermal application. J Vet Sci. 2009b; 10: 257‑9.
  • Reddy PS, Rani GP, Sainath SB, Meena R, Supriya Ch. Protective effects of N-acetylcysteine against arsenic-induced oxidative stres and reprotoxicity in male mice. Journal of Trace Elements in Medicine and Biology. 2011; 25: 247– 253.
  • Richard S, Moslemi S, Sipahutar H, Benachour N, Séralini GE. Differential effects of glyphosate and Roundup on human placental cells and aromatase. Environ. Health Perspect. 2005; 113: 716–720.
  • Romano RM, Romano MA, Bernardi MM, Furtado P, Oliveira CA. Prepubertal exposure to commercial formulation of the herbicide glyphosatealters testosterone levels and testicular morphology. Arch. Toxicol. 2010; 84: 309–317.
  • Sönmez M, Türk G, Yüce A. The effect of ascorbic acid supplementation on sperm quality, lipid peroxidation and testosterone levels of male Wistar rats. Theriogenology. 2005; 63: 2063–72.
  • Sun Y, Oberley LW, Li Y. A simple method for clinical assay of superoxide dismutase. Clin Chem. 1988; 34: 497–500.
  • Takahashi M, Horie M, Aoba N. Analysis of glyphosate and its metabolite, aminomethylphosphonic acid, in agricultural products by HPLC. Shokuhin Eiseigaku Zasshi. 2001; 42: 304–308.
  • Whitaker BD, Casey SJ, Taupier R. N-acetyl-L-cysteine Supplementation Improves Boar Spermatozoa Characteristics and Subsequent Fertilization and Embryonic Development. Reprod Dom Anim. 2012; 47: 263–268.
  • Yıldız S, Öztürkler Y, Arı UÇ, Lehimcioğlu NC, Atakişi E, Kulaksız R. The effects of L-ergothioneine, N-acetylcystein and cystein on freezing of ram semen. Kafkas Univ Vet Fak Derg. 2015; 21: 81-86.
Toplam 44 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Bölüm ARAŞTIRMA MAKALESİ
Yazarlar

Fatih Avdatek 0000-0003-2345-8826

Ruhi Türkmen

Hasan Hüseyin Demirel Bu kişi benim

Yavuz Osman Birdane

Yayımlanma Tarihi 1 Eylül 2018
Kabul Tarihi 14 Temmuz 2018
Yayımlandığı Sayı Yıl 2018

Kaynak Göster

APA Avdatek, F., Türkmen, R., Demirel, H. H., Birdane, Y. O. (2018). Protective Effect of N-Acetylcysteine on Testicular Oxidative Damage, Spermatological Parameters and DNA Damage in Glyphosate-Based Herbicide-Exposed Rats. Kocatepe Veterinary Journal, 11(3), 292-300. https://doi.org/10.30607/kvj.435112
AMA Avdatek F, Türkmen R, Demirel HH, Birdane YO. Protective Effect of N-Acetylcysteine on Testicular Oxidative Damage, Spermatological Parameters and DNA Damage in Glyphosate-Based Herbicide-Exposed Rats. kvj. Eylül 2018;11(3):292-300. doi:10.30607/kvj.435112
Chicago Avdatek, Fatih, Ruhi Türkmen, Hasan Hüseyin Demirel, ve Yavuz Osman Birdane. “Protective Effect of N-Acetylcysteine on Testicular Oxidative Damage, Spermatological Parameters and DNA Damage in Glyphosate-Based Herbicide-Exposed Rats”. Kocatepe Veterinary Journal 11, sy. 3 (Eylül 2018): 292-300. https://doi.org/10.30607/kvj.435112.
EndNote Avdatek F, Türkmen R, Demirel HH, Birdane YO (01 Eylül 2018) Protective Effect of N-Acetylcysteine on Testicular Oxidative Damage, Spermatological Parameters and DNA Damage in Glyphosate-Based Herbicide-Exposed Rats. Kocatepe Veterinary Journal 11 3 292–300.
IEEE F. Avdatek, R. Türkmen, H. H. Demirel, ve Y. O. Birdane, “Protective Effect of N-Acetylcysteine on Testicular Oxidative Damage, Spermatological Parameters and DNA Damage in Glyphosate-Based Herbicide-Exposed Rats”, kvj, c. 11, sy. 3, ss. 292–300, 2018, doi: 10.30607/kvj.435112.
ISNAD Avdatek, Fatih vd. “Protective Effect of N-Acetylcysteine on Testicular Oxidative Damage, Spermatological Parameters and DNA Damage in Glyphosate-Based Herbicide-Exposed Rats”. Kocatepe Veterinary Journal 11/3 (Eylül 2018), 292-300. https://doi.org/10.30607/kvj.435112.
JAMA Avdatek F, Türkmen R, Demirel HH, Birdane YO. Protective Effect of N-Acetylcysteine on Testicular Oxidative Damage, Spermatological Parameters and DNA Damage in Glyphosate-Based Herbicide-Exposed Rats. kvj. 2018;11:292–300.
MLA Avdatek, Fatih vd. “Protective Effect of N-Acetylcysteine on Testicular Oxidative Damage, Spermatological Parameters and DNA Damage in Glyphosate-Based Herbicide-Exposed Rats”. Kocatepe Veterinary Journal, c. 11, sy. 3, 2018, ss. 292-00, doi:10.30607/kvj.435112.
Vancouver Avdatek F, Türkmen R, Demirel HH, Birdane YO. Protective Effect of N-Acetylcysteine on Testicular Oxidative Damage, Spermatological Parameters and DNA Damage in Glyphosate-Based Herbicide-Exposed Rats. kvj. 2018;11(3):292-300.

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