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Ameliorating effects of exercise on disrupted epididymal sperm parameters in high fat diet-induced obese rats

Yıl 2019, Cilt: 32 Sayı: 1, 14 - 19, 29.01.2019
https://doi.org/10.5472/marumj.518732

Öz

Objective: Obesity causes male infertility problems and affects
the sperm quality. Recent studies have shown that exercise has
positive effects on male fertility. The present study aimed to show
the effects of swimming exercise on the epididymal sperm number,
motility and morphology in hight fat diet (HFD)-induced obese
rats.
Materials and Methods: Four experimental groups (n=8 in
each group) were formed. Standard (STD) and STD+Exercise
(STD+EXC) groups were fed with standard rat diet (6% of calories
as fat); HFD and HFD+Exercise (HFD+EXC) groups were fed
with high fat diet (45% of calories as fat) for 18 weeks. The rats
in STD+EXC and HFD+EXC groups were trained by swimming
sessions (1 h per day for 5 days a week) during the last 6 weeks of
the experiment. The left caudal epididymis was prepared to evaluate
the number, motility and morphology of the spermatozoa. The right
epididymal samples were processed for histological evaluation.
Results: Normospermic parameters were seen in STD and
STD+EXC groups. Sperm number and motility decreased and
spermatozoa with abnormal morphology increased significantly in
HFD group when compared with STD group. A large number of
spermatozoa in the epididymal duct lumen and regular morphology
of the fibromuscular connective tissue were observed in STD
and STD+EXC groups. Most of the epididymal ducts consisted
of decreased amount of spermatozoal accumulation in the HFD
group. Degenerated pseudostratified columnar epithelium with
vacuole formation were additional findings in this group. On the
other hand, swimming exercise had an enhancement effect on
sperm parameters with prominent spermatozoal accumulation in
the ducts of epididymis in HFD induced obese rats.
Conclusion: This study shows that HFD-induced obesity
decreased the number and motility of spermatozoa, increased
abnormal spermatozoa and caused disrupted epididymal
morphology. We hypothesize that exercise enhanced HFD-induced
spermatogenic and epididymal damages by the regulation of scrotal
heat and possible inhibition of oxidative damage in the epididymis.

Kaynakça

  • 1. Roumaud P, Martin LJ. Roles of leptin, adiponectin and resistin in the transcriptional regulation of steroidogenic genes contributing to decreased Leydig cells function in obesity. Horm Mol Biol Clin Investig 2015;24:25-45. doi: 10.1515/hmbci-2015-0046.
  • 2. Palmer NO, Bakos HW, Fullston T, Lane M. Impact of obesity on male fertility, sperm function and molecular composition. Spermatogenesis 2012;2:253-63. doi: 10.4161/spmg.21362.
  • 3. Ramlau-Hansen CH, Hansen M, Jensen CR, Olsen J, Bonde JP, Thulstrup AM. Semen quality and reproductive hormones according to birthweight and body mass index in childhood and adult life: two decades of follow-up. Fertil Steril 2010;94:610-8. doi: 10.1016/j.fertnstert.2009.01.142.
  • 4. Palmer NO, Bakos HW, Owens JA, Setchell BP, Lane M. Diet and exercise in an obese mouse fed a high-fat diet improve metabolic health and reverse perturbed sperm function. Am J Physiol Endocrinol Metab 2012;302:E768-80. doi: 10.1152/ ajpendo.00401.2011.
  • 5. Nguyen RH, Wilcox AJ, Skjaerven R, Baird DD. Men’s body mass index and infertility. Hum Reprod 2007;22:2488-93. doi: 10.1093/humrep/dem139.
  • 6. Fan Y, Liu Y, Xue K, et al. Diet-induced obesity in male C57BL/6 mice decreases fertility as a consequence of disrupted blood-testis barrier. PLoS One 2015;10:e0120775. doi: 10.1371/journal.pone.0120775.
  • 7. Ghanayem BI, Bai R, Kissling GE, Travlos G, Hoffler U. Diet-induced obesity in male mice is associated with reduced fertility and potentiation of acrylamide-induced reproductive toxicity. Biol Reprod 2010;82:96-104. doi: 10.1095/ biolreprod.109.078915.
  • 8. Bedford JM. Human spermatozoa and temperature: the elephant in the room. Biol Reprod 2015;93:97. doi: 10.1095/ biolreprod.115.130658.
  • 9. Robinson D, Rock J, Menkin MF. Control of human spermatogenesis by induced changes of intrascrotal temperature. JAMA 1968;204:290-7.
  • 10. Paul C, Melton DW, Saunders PT. Do heat stress and deficits in DNA repair pathways have a negative impact on male fertility? Mol Hum Reprod 2008;14:1-8. doi: 10.1093/ molehr/gam089.
  • 11. Shiraishi K, Takihara H, Matsuyama H. Elevated scrotal temperature, but not varicocele grade, reflects testicular oxidative stress-mediated apoptosis. World J Urol 2010;28:359-64. doi: 10.1007/s00345.009.0462-5.
  • 12. Garolla A, Torino M, Miola P, et al. Twenty-four-hour monitoring of scrotal temperature in obese men and men with a varicocele as a mirror of spermatogenic function. Hum Reprod 2015;30:1006-13. doi: 10.1093/humrep/dev057.
  • 13. Vigueras-Villasenor RM, Rojas-Castaneda JC, Chavez- Saldana M, et al. Alterations in the spermatic function generated by obesity in rats. Acta Histochem 2011;113:214- 20. doi: 10.1016/j.acthis.2009.10.004.
  • 14. Dandona P, Aljada A, Chaudhuri A, Mohanty P, Garg R. Metabolic syndrome: a comprehensive perspective based on interactions between obesity, diabetes, and inflammation. Circulation 2005;111:1448-54. doi: 10.1161/01. CIR.000.015.8483.13093.9D.
  • 15. Du Plessis SS, Cabler S, McAlister DA, Sabanegh E, Agarwal A. The effect of obesity on sperm disorders and male infertility. Nat Rev Urol 2010;7:153-61. doi: 10.1038/ nrurol.2010.6.
  • 16. Hammoud AO, Wilde N, Gibson M, Parks A, Carrell DT, Meikle AW. Male obesity and alteration in sperm parameters. Fertil Steril 2008;90:2222-5. doi: 10.1016/j. fertnstert.2007.10.011.
  • 17. MacDonald AA, Herbison GP, Showell M, Farquhar CM. The impact of body mass index on semen parameters and reproductive hormones in human males: a systematic review with meta-analysis. Hum Reprod Update 2010;16:293-311. doi: 10.1093/humupd/dmp047.
  • 18. Atilgan D, Parlaktas BS, Uluocak N, et al. Weight loss and melatonin reduce obesity-induced oxidative damage in rat testis. Adv Urol 2013;2013:836121. doi: 10.1155/2013/836121.
  • 19. Ickin Gulen M, Guven Bagla A, Yavuz O, Hismiogullari AA. Histopathological changes in rat pancreas and skeletal muscle associated with high fat diet induced insulin resistance. Biotech Histochem 2015;90:495-505. doi: 10.3109/10520.295.2015.1021380.
  • 20. Sallmen M, Sandler DP, Hoppin JA, Blair A, Baird DD. Reduced fertility among overweight and obese men. Epidemiology 2006;17:520-3. doi: 10.1097/01. ede.000.022.9953.76862.e5.
  • 21. Chavarro JE, Toth TL, Wright DL, Meeker JD, Hauser R. Body mass index in relation to semen quality, sperm DNA integrity, and serum reproductive hormone levels among men attending an infertility clinic. Fertil Steril 2010;93:2222-31. doi: 10.1016/j.fertnstert.2009.01.100.
  • 22. Bakos HW, Mitchell M, Setchell BP, Lane M. The effect of paternal diet-induced obesity on sperm function and fertilization in a mouse model. Int J Androl 2011;34(5 Pt 1):402-10. doi: 10.1111/j.1365-2605.2010.01092.x.
  • 23. Fernandez CD, Bellentani FF, Fernandes GS, et al. Dietinduced obesity in rats leads to a decrease in sperm motility. Reprod Biol Endocrinol 2011;9:32. doi: 10.1186/1477-7827- 9-32.
  • 24. Liu Y, Ding Z. Obesity, a serious etiologic factor for male subfertility in modern society. Reproduction 2017;154:R123-R31. doi: 10.1530/REP-17-0161.
  • 25. Ng SF, Lin RC, Laybutt DR, Barres R, Owens JA, Morris MJ. Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 2010;467(7318):963-6. doi: 10.1038/nature09491.
  • 26. Kasturi SS, Tannir J, Brannigan RE. The metabolic syndrome and male infertility. J Androl 2008;29:251-9. doi: 10.2164/ jandrol.107.003731.
  • 27. La Vignera S, Condorelli RA, Vicari E, Calogero AE. Negative effect of increased body weight on sperm conventional and nonconventional flow cytometric sperm parameters. J Androl 2012;33:53-8. doi: 10.2164/jandrol.110.012120.
  • 28. Akishita M, Fukai S, Hashimoto M, et al. Association of low testosterone with metabolic syndrome and its components in middle-aged Japanese men. Hypertens Res 2010;33:587-91. doi: 10.1038/hr.2010.43.
  • 29. Haring R, Volzke H, Felix SB, et al. Prediction of metabolic syndrome by low serum testosterone levels in men: results from the study of health in Pomerania. Diabetes 2009;58:2027-31. doi: 10.2337/db09-0031.
  • 30. Kupelian V, Page ST, Araujo AB, Travison TG, Bremner WJ, McKinlay JB. Low sex hormone-binding globulin, total testosterone, and symptomatic androgen deficiency are associated with development of the metabolic syndrome in nonobese men. J Clin Endocrinol Metab 2006;91:843-50. doi: 10.1210/jc.2005-1326.
  • 31. Sermondade N, Faure C, Fezeu L, Levy R, Czernichow S, Obesity-Fertility Collaborative G. Obesity and increased risk for oligozoospermia and azoospermia. Arch Intern Med 2012;172:440-2. doi: 10.1001/archinternmed.2011.1382.
  • 32. Shayeb AG, Harrild K, Mathers E, Bhattacharya S. An exploration of the association between male body mass index and semen quality. Reprod Biomed Online 2011;23:717-23. doi: 10.1016/j.rbmo.2011.07.018.
  • 33. Vaamonde D, Da Silva-Grigoletto ME, Garcia-Manso JM, Barrera N, Vaamonde-Lemos R. Physically active men show better semen parameters and hormone values than sedentary men. Eur J Appl Physiol 2012;112:3267-73. doi: 10.1007/ s00421.011.2304-6.
  • 34. Hajizadeh Maleki B, Tartibian B. Long-term low-to-intensive cycling training: Impact on semen parameters and seminal cytokines. Clin J Sport Med 2015;25:535-40. doi: 10.1097/ JSM.000.000.0000000122.

Yüksek yağlı diyetle indüklenmiş obez sıçanların bozulmuş epididimal sperm parametreleri üzerine egzersizin iyileştirici etkisi

Yıl 2019, Cilt: 32 Sayı: 1, 14 - 19, 29.01.2019
https://doi.org/10.5472/marumj.518732

Öz

Amaç: Obezite erkek infertilite problemlerine neden olur ve sperm

kalitesini etkiler. Egzersizin erkek fertilitesi üzerine olumlu etkileri

olduğu çeşitli çalışmalar ile gösterilmiştir. Bu çalışmanın amacı,

yüksek yağlı diyetle (YYD) indüklenmiş obez sıçanlarda yüzme

egzersizinin epididimal sperm sayısı, motilitesi ve epididimis

morfolojisi üzerine etkilerini göstermektir.

Gereçler ve Yöntemler: Bu çalışmada dört deney grubu

(her grupta n=8) oluşturuldu. Standart (STD) ve STD+Egzersiz

(STD+EGZ) gruplarındaki sıçanlar standart sıçan diyeti ile

(kalorisinde %6 yağ içeren); YYD ve YYD+Egzersiz (YYD+EGZ)

grubundaki sıçanlar da yüksek yağlı diyet ile (kalorisinde %45 yağ

içeren) 18 hafta beslendiler. STD+EGZ ve YYD+EGZ grubundaki

sıçanlara deneyin son 6 haftasında haftada 5 gün, günde 1 saat yüzme

egzersizi yaptırıldı. Deney sonunda sol kaudal epididimis sperm

sayısı, motilitesi ve morfolojisinin incelenmesi için hazırlandı. Sağ

epididimis dokusu da histolojik inceleme için hazırlandı.

Bulgular: STD ve STD+EGZ gruplarında normospermik

parametreler gözlendi. STD grubu ile kıyaslandığında YYD

grubunda sperm sayısı ve motilitesinin anlamlı olarak azaldığı

ve morfolojik anomaliye sahip sperm sayısının arttığı gözlendi.

STD ve STD+EGZ gruplarında epididimal kanal spermatozoa

ile doluydu ve fibromusküler bağ dokusu düzenli morfolojide

gözlendi. YYD grubunda epididimal kanalların çoğu azalmış

sayıda spermatozoa kümesinden oluşuyordu. Ayrıca, epididimisin

stereosilyalı yalancı çok katlı silindirik epitelinde yer yer vakuol

oluşumları gözlendi. Egzersizin ise YYD ile indüklenmiş obez

sıçanlarda sperm parametrelerini ve epididimis kanalındaki sperm

kümesini arttırdığı gözlendi.

Sonuç: Bu çalışma, obezitenin sperm sayısını ve motilitesini

azalttığını, anomalili sperm sayısını arttırdığını ve epididimis

morfolojisini bozduğunu göstermektedir. Egzersizin ise, skrotal

ısıyı dengeleyerek ve epididimisteki olası oksidan hasarı

engelleyerek YYD ile indüklenmiş spermatogenik ve epididimal

hasarı iyileştirdiği düşünülmektedir.

Kaynakça

  • 1. Roumaud P, Martin LJ. Roles of leptin, adiponectin and resistin in the transcriptional regulation of steroidogenic genes contributing to decreased Leydig cells function in obesity. Horm Mol Biol Clin Investig 2015;24:25-45. doi: 10.1515/hmbci-2015-0046.
  • 2. Palmer NO, Bakos HW, Fullston T, Lane M. Impact of obesity on male fertility, sperm function and molecular composition. Spermatogenesis 2012;2:253-63. doi: 10.4161/spmg.21362.
  • 3. Ramlau-Hansen CH, Hansen M, Jensen CR, Olsen J, Bonde JP, Thulstrup AM. Semen quality and reproductive hormones according to birthweight and body mass index in childhood and adult life: two decades of follow-up. Fertil Steril 2010;94:610-8. doi: 10.1016/j.fertnstert.2009.01.142.
  • 4. Palmer NO, Bakos HW, Owens JA, Setchell BP, Lane M. Diet and exercise in an obese mouse fed a high-fat diet improve metabolic health and reverse perturbed sperm function. Am J Physiol Endocrinol Metab 2012;302:E768-80. doi: 10.1152/ ajpendo.00401.2011.
  • 5. Nguyen RH, Wilcox AJ, Skjaerven R, Baird DD. Men’s body mass index and infertility. Hum Reprod 2007;22:2488-93. doi: 10.1093/humrep/dem139.
  • 6. Fan Y, Liu Y, Xue K, et al. Diet-induced obesity in male C57BL/6 mice decreases fertility as a consequence of disrupted blood-testis barrier. PLoS One 2015;10:e0120775. doi: 10.1371/journal.pone.0120775.
  • 7. Ghanayem BI, Bai R, Kissling GE, Travlos G, Hoffler U. Diet-induced obesity in male mice is associated with reduced fertility and potentiation of acrylamide-induced reproductive toxicity. Biol Reprod 2010;82:96-104. doi: 10.1095/ biolreprod.109.078915.
  • 8. Bedford JM. Human spermatozoa and temperature: the elephant in the room. Biol Reprod 2015;93:97. doi: 10.1095/ biolreprod.115.130658.
  • 9. Robinson D, Rock J, Menkin MF. Control of human spermatogenesis by induced changes of intrascrotal temperature. JAMA 1968;204:290-7.
  • 10. Paul C, Melton DW, Saunders PT. Do heat stress and deficits in DNA repair pathways have a negative impact on male fertility? Mol Hum Reprod 2008;14:1-8. doi: 10.1093/ molehr/gam089.
  • 11. Shiraishi K, Takihara H, Matsuyama H. Elevated scrotal temperature, but not varicocele grade, reflects testicular oxidative stress-mediated apoptosis. World J Urol 2010;28:359-64. doi: 10.1007/s00345.009.0462-5.
  • 12. Garolla A, Torino M, Miola P, et al. Twenty-four-hour monitoring of scrotal temperature in obese men and men with a varicocele as a mirror of spermatogenic function. Hum Reprod 2015;30:1006-13. doi: 10.1093/humrep/dev057.
  • 13. Vigueras-Villasenor RM, Rojas-Castaneda JC, Chavez- Saldana M, et al. Alterations in the spermatic function generated by obesity in rats. Acta Histochem 2011;113:214- 20. doi: 10.1016/j.acthis.2009.10.004.
  • 14. Dandona P, Aljada A, Chaudhuri A, Mohanty P, Garg R. Metabolic syndrome: a comprehensive perspective based on interactions between obesity, diabetes, and inflammation. Circulation 2005;111:1448-54. doi: 10.1161/01. CIR.000.015.8483.13093.9D.
  • 15. Du Plessis SS, Cabler S, McAlister DA, Sabanegh E, Agarwal A. The effect of obesity on sperm disorders and male infertility. Nat Rev Urol 2010;7:153-61. doi: 10.1038/ nrurol.2010.6.
  • 16. Hammoud AO, Wilde N, Gibson M, Parks A, Carrell DT, Meikle AW. Male obesity and alteration in sperm parameters. Fertil Steril 2008;90:2222-5. doi: 10.1016/j. fertnstert.2007.10.011.
  • 17. MacDonald AA, Herbison GP, Showell M, Farquhar CM. The impact of body mass index on semen parameters and reproductive hormones in human males: a systematic review with meta-analysis. Hum Reprod Update 2010;16:293-311. doi: 10.1093/humupd/dmp047.
  • 18. Atilgan D, Parlaktas BS, Uluocak N, et al. Weight loss and melatonin reduce obesity-induced oxidative damage in rat testis. Adv Urol 2013;2013:836121. doi: 10.1155/2013/836121.
  • 19. Ickin Gulen M, Guven Bagla A, Yavuz O, Hismiogullari AA. Histopathological changes in rat pancreas and skeletal muscle associated with high fat diet induced insulin resistance. Biotech Histochem 2015;90:495-505. doi: 10.3109/10520.295.2015.1021380.
  • 20. Sallmen M, Sandler DP, Hoppin JA, Blair A, Baird DD. Reduced fertility among overweight and obese men. Epidemiology 2006;17:520-3. doi: 10.1097/01. ede.000.022.9953.76862.e5.
  • 21. Chavarro JE, Toth TL, Wright DL, Meeker JD, Hauser R. Body mass index in relation to semen quality, sperm DNA integrity, and serum reproductive hormone levels among men attending an infertility clinic. Fertil Steril 2010;93:2222-31. doi: 10.1016/j.fertnstert.2009.01.100.
  • 22. Bakos HW, Mitchell M, Setchell BP, Lane M. The effect of paternal diet-induced obesity on sperm function and fertilization in a mouse model. Int J Androl 2011;34(5 Pt 1):402-10. doi: 10.1111/j.1365-2605.2010.01092.x.
  • 23. Fernandez CD, Bellentani FF, Fernandes GS, et al. Dietinduced obesity in rats leads to a decrease in sperm motility. Reprod Biol Endocrinol 2011;9:32. doi: 10.1186/1477-7827- 9-32.
  • 24. Liu Y, Ding Z. Obesity, a serious etiologic factor for male subfertility in modern society. Reproduction 2017;154:R123-R31. doi: 10.1530/REP-17-0161.
  • 25. Ng SF, Lin RC, Laybutt DR, Barres R, Owens JA, Morris MJ. Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 2010;467(7318):963-6. doi: 10.1038/nature09491.
  • 26. Kasturi SS, Tannir J, Brannigan RE. The metabolic syndrome and male infertility. J Androl 2008;29:251-9. doi: 10.2164/ jandrol.107.003731.
  • 27. La Vignera S, Condorelli RA, Vicari E, Calogero AE. Negative effect of increased body weight on sperm conventional and nonconventional flow cytometric sperm parameters. J Androl 2012;33:53-8. doi: 10.2164/jandrol.110.012120.
  • 28. Akishita M, Fukai S, Hashimoto M, et al. Association of low testosterone with metabolic syndrome and its components in middle-aged Japanese men. Hypertens Res 2010;33:587-91. doi: 10.1038/hr.2010.43.
  • 29. Haring R, Volzke H, Felix SB, et al. Prediction of metabolic syndrome by low serum testosterone levels in men: results from the study of health in Pomerania. Diabetes 2009;58:2027-31. doi: 10.2337/db09-0031.
  • 30. Kupelian V, Page ST, Araujo AB, Travison TG, Bremner WJ, McKinlay JB. Low sex hormone-binding globulin, total testosterone, and symptomatic androgen deficiency are associated with development of the metabolic syndrome in nonobese men. J Clin Endocrinol Metab 2006;91:843-50. doi: 10.1210/jc.2005-1326.
  • 31. Sermondade N, Faure C, Fezeu L, Levy R, Czernichow S, Obesity-Fertility Collaborative G. Obesity and increased risk for oligozoospermia and azoospermia. Arch Intern Med 2012;172:440-2. doi: 10.1001/archinternmed.2011.1382.
  • 32. Shayeb AG, Harrild K, Mathers E, Bhattacharya S. An exploration of the association between male body mass index and semen quality. Reprod Biomed Online 2011;23:717-23. doi: 10.1016/j.rbmo.2011.07.018.
  • 33. Vaamonde D, Da Silva-Grigoletto ME, Garcia-Manso JM, Barrera N, Vaamonde-Lemos R. Physically active men show better semen parameters and hormone values than sedentary men. Eur J Appl Physiol 2012;112:3267-73. doi: 10.1007/ s00421.011.2304-6.
  • 34. Hajizadeh Maleki B, Tartibian B. Long-term low-to-intensive cycling training: Impact on semen parameters and seminal cytokines. Clin J Sport Med 2015;25:535-40. doi: 10.1097/ JSM.000.000.0000000122.
Toplam 34 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Klinik Tıp Bilimleri
Bölüm Makaleler
Yazarlar

Merve Açıkel Elmas Bu kişi benim

Serap Arbak Bu kişi benim

Feriha Ercan Bu kişi benim

Yayımlanma Tarihi 29 Ocak 2019
Yayımlandığı Sayı Yıl 2019 Cilt: 32 Sayı: 1

Kaynak Göster

APA Açıkel Elmas, M., Arbak, S., & Ercan, F. (2019). Ameliorating effects of exercise on disrupted epididymal sperm parameters in high fat diet-induced obese rats. Marmara Medical Journal, 32(1), 14-19. https://doi.org/10.5472/marumj.518732
AMA Açıkel Elmas M, Arbak S, Ercan F. Ameliorating effects of exercise on disrupted epididymal sperm parameters in high fat diet-induced obese rats. Marmara Med J. Ocak 2019;32(1):14-19. doi:10.5472/marumj.518732
Chicago Açıkel Elmas, Merve, Serap Arbak, ve Feriha Ercan. “Ameliorating Effects of Exercise on Disrupted Epididymal Sperm Parameters in High Fat Diet-Induced Obese Rats”. Marmara Medical Journal 32, sy. 1 (Ocak 2019): 14-19. https://doi.org/10.5472/marumj.518732.
EndNote Açıkel Elmas M, Arbak S, Ercan F (01 Ocak 2019) Ameliorating effects of exercise on disrupted epididymal sperm parameters in high fat diet-induced obese rats. Marmara Medical Journal 32 1 14–19.
IEEE M. Açıkel Elmas, S. Arbak, ve F. Ercan, “Ameliorating effects of exercise on disrupted epididymal sperm parameters in high fat diet-induced obese rats”, Marmara Med J, c. 32, sy. 1, ss. 14–19, 2019, doi: 10.5472/marumj.518732.
ISNAD Açıkel Elmas, Merve vd. “Ameliorating Effects of Exercise on Disrupted Epididymal Sperm Parameters in High Fat Diet-Induced Obese Rats”. Marmara Medical Journal 32/1 (Ocak 2019), 14-19. https://doi.org/10.5472/marumj.518732.
JAMA Açıkel Elmas M, Arbak S, Ercan F. Ameliorating effects of exercise on disrupted epididymal sperm parameters in high fat diet-induced obese rats. Marmara Med J. 2019;32:14–19.
MLA Açıkel Elmas, Merve vd. “Ameliorating Effects of Exercise on Disrupted Epididymal Sperm Parameters in High Fat Diet-Induced Obese Rats”. Marmara Medical Journal, c. 32, sy. 1, 2019, ss. 14-19, doi:10.5472/marumj.518732.
Vancouver Açıkel Elmas M, Arbak S, Ercan F. Ameliorating effects of exercise on disrupted epididymal sperm parameters in high fat diet-induced obese rats. Marmara Med J. 2019;32(1):14-9.