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Abstrakt

The aim of this study was to evaluate the antioxidative/oxidative status of spermatozoa and prostatic fluid in dogs with benign prostatic hyperplasia (BPH) by the determination of total antioxidant capacity and protein peroxidation markers. Study was conducted on 40 intact dogs of various breeds. The dogs were assigned to two groups: BPH group (n=20) and non-affected group (n=20). The second and third fractions of the ejaculate were collected separately by digital manipulation. Total antioxidant capacity (TAC) and the concentrations of SH-groups in sperm and prostatic fluid were determined spectrophotometrically, the concentrations of bityrosine and formylkynurenine were determined using spectrofluorimetric methods. The mean values of TAC in spermatozoa and prostatic fluid were significantly lower (p<0.05), whereas the mean contents of biotyrosine and formylkinurenine were significantly higher (p<0.05) in BPH dogs compared to control dogs. There was no statistically significant difference in the content of SH group between dogs with BPH and control dogs (p>0.05). In conclusion, the results indicate that BPH in dogs is associated with reduced total antioxidant capacity and increased protein oxidation in the prostatic fluid and spermatozoa, and suggest the importance of oxidative stress in the pathogenesis of this condition. The potential role of antioxidants in the prevention and therapy of canine BPH requires further studies.
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Bibliografia

1. Al Smadi MA, Hammadeh ME, Batiha O, Al Sharu E, Altalib MM, Jahmani MY, Mahdy A, Amor H (2021) Elevated seminal protein carbonyl concentration is correlated with asthenozoospermia and affects adversely the laboratory intracytoplasmic sperm injection (ICSI) outcomes. Andrologia 53: e14232.
2. Angrimani DS, Brito MM, Rui BR, Nichi M, Vannucchi CI (2020) Reproductive and endocrinological effects of Benign Prostatic Hy-perplasia and finasteride therapy in dogs. Sci Rep 10: 14834.
3. Aquino-Cortez A, Pinheiro BQ, Lima DB, Silva HV, Mota-Filho AC, Martins JA, Rodriguez-Villamil P, Moura AA, Silva LD (2017) Proteomic characterization of canine seminal plasma. Theriogenology 95: 178-186.
4. Aydin A, Arsova-Sarafinovska Z, Sayal A, Eken A, Erdem O, Erten K, Ozgok Y, Dimovski A (2006) Oxidative stress and antioxidant status in non-metastatic prostate cancer and benign prostatic hyperplasia. Clin Biochem 39: 176-179.
5. Barsanti JA, Finco DR (1986) Canine prostatic diseases. Vet Clin North Am Small Anim Pract 16: 587-599.
6. Benzie IF, Strain JJ (1996) The ferric reducing ability of plasma (FRAP) as a measure of „antioxidant power”: The FRAP assay. Anal Biochem 239: 70-76.
7. Bergsma AT, Li HT, Eliveld J, Bulthuis ML, Hoek A, van Goor H, Bourgonje AR, Cantineau AE (2022) Local and systemic oxidative stress biomarkers for male infertility: The ORION study. Antioxidants (Basel) 11: 1045.
8. Berry SJ, Strandberg JD, Saunders WJ, Coffey DS (1986) Development of canine benign prostatic hyperplasia with age. Prostate 9: 363-373.
9. Castleton PE, Deluao JC, Sharkey DJ, McPherson NO (2022) Measuring reactive oxygen species in semen for male preconception care: A scientist perspective. Antioxidants (Basel) 11: 264.
10. Cunto M, Ballotta G, Zambelli D (2022) Benign prostatic hyperplasia in the dog. Anim Reprod Sci 247: 107096.
11. Da Rocha AA, da Cunha ICN, Ederli BB, Albernaz AP, Quirino CR (2009) Effect of daily food supplementation with essential fatty ac-ids on canine semen quality. Reprod Dom Anim 44, (Suppl 2): 313-315.
12. Dearakhshandeh N, Mogheiseh A, Nazifi S, Ahrari Khafi MS, Abbaszadeh Hasiri M, Golchin-Rad K (2019) Changes in the oxidative stress factors and inflammatory proteins following the treatment of BPH-induced dogs with an anti-proliferative agent called tadalafil. J Vet Pharmacol Ther 42: 665-672.
13. De Souza FF, Barreto CS, Lopes MD (2007) Characteristics of seminal plasma proteins and their correlation with canine semen analysis. Theriogenology 68: 100-106.
14. Domosławska A, Zdunczyk S (2020) Clinical and spermatological findings in male dogs with acquired infertility: A retrospective analy-sis. Andrologia 52: e13802.
15. Domoslawska A, Zdunczyk S, Franczyk M, Kankofer M, Janowski T (2018) Selenium and vitamin E supplementation enhances the an-tioxidant status of spermatozoa and improves semen quality in male dogs with lowered fertility. Andrologia 50: e13023
16. Domosławska A, Zdunczyk S, Franczyk M, Kankofer M, Janowski T (2019) Total antioxidant capacity and protein peroxidation inten-sity in seminal plasma of infertile and fertile dogs. Reprod Domest Anim 54: 252-257.
17. Domosławska A, Zduńczyk S, Kankofer M, Bielecka A (2022) Oxidative stress biomarkers in dogs with benign prostatic hyperplasia. Ir Vet J 75: 21.
18. Ferré-Dolcet L, Frigotto L, Contiero B, Bedin S, Romagnoli S (2022) Prostatic fluid composition and semen quality in dogs with benign prostatic hyperplasia undergoing treatment with osaterone acetate. Reprod Domest Anim 57: 72-79.
19. Fontbonne A (2011) Infertility in male dogs: recent advances. Rev Bras Reprod Anim 35: 266-273.
20. Gandaglia G, Briganti A, Gontero P, Mondaini N, Novara G, Salonia A, Sciarra A, Montorsi F (2013) The role of chronic prostatic in-flammation in the pathogenesis and progression of benign prostatic hyperplasia (BPH). BJU Int 112: 432-441.
21. Ghiselli A, Serafini M, Natella F, Scaccini C (2000) Total antioxidant capacity as a tool to assess redox status: critical view and experi-mental data. Free Radic Biol Med 29: 1106-1114.
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24. Kankofer M (2001) Protein peroxidation processes in bovine retained and not-retained placenta. J Vet Med A Physiol Pathol Clin Med 48: 207-2212.
25. Kawakami E, Kobayashi M, Hori T, Kaneda T (2015) Therapeutic effects of vitamin E in 4 dogs with poor semen quality and low su-peroxide dismutase activity in seminal plasma. J Vet Med Sci 77: 1711-1714.
26. Lévy X, Niżański W, von Heimendahl A, Mimouni P (2014) Diagnosis of common prostatic conditions in dogs: an update. Reprod Domest Anim 49 (Suppl 2): 50-57.
27. Linde-Forsberg C (1991) Achieving canine pregnancy by using frozen or chilled extended semen. Vet Clin North Am Small Anim Pract 21: 467-485.
28. Meikle AW, Collier ES, Stringham JD, Fang SM, Taylor GN (1981) Elevated intranuclear dihydrotestosterone in prostatic hyperplasia of aging dogs. J Steroid Biochem 14: 331-335.
29. Memon MA (2007) Common causes of male dog infertility. Theriogenology 68: 322-328.
30. Minciullo PL, Inferrera A, Navarra M, Calapai G, Magno C, Gangemi S (2015) Oxidative stress in benign prostatic hyperplasia: a sys-tematic review. Urol Int 94: 249-254.
31. Mitsunari K, Miyata Y, Matsuo T, Mukae Y, Otsubo A, Harada J, Kondo T, Matsuda T, Ohba K, Sakai H (2021) Pharmacological Ef-fects and Potential Clinical Usefulness of Polyphenols in Benign Prostatic Hyperplasia. Molecules 26: 450.
32. Morielli T, O’Flaherty C (2015) Oxidative stress impairs function and increases redox protein modifications in human spermatozoa. Re-production 149: 113-23.
33. Nowicka-Bauer K, Lepczynski A, Ozgo M, Kamieniczna M, Fraczek M, Stanski L, Olszewska M, Malcher A, Skrzypczak W, Kurpisz MK (2018) Sperm mitochondrial dysfunction and oxidative stress as possible reasons for isolated asthenozoospermia. J Physiol Phar-macol 69.
34. Pace G, Di Massimo C, De Amicis D, Corbacelli C, Di Renzo L, Vicentini C, Miano L, Tozzi Ciancarelli MG (2010) Oxidative stress in benign prostatic hyperplasia and prostate cancer. Urol Int 85: 328-333.
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36. Roumeguère T, Sfeir J, El Rassy E, Albisinni S, Van Antwerpen P, Boudjeltia KZ, Farès N, Kattan J, Aoun F (2017) Oxidative stress and prostatic diseases. Mol Clin Oncol 7: 723-728.
37. Schäfer-Somi S (2023) Diseases of the Canine Prostate Gland. IntechOpen. Doi: 10.5772/intechopen.105835.
38. Smith J (2008) Canine prostatic disease: a review of anatomy, pathology, diagnosis, and treatment. Theriogenology 70: 375-383.
39. Srivastava DS, Mittal RD (2005) Free radical injury and antioxidant status in patients with benign prostate hyperplasia and prostate can-cer. Indian J Clin Biochem 20: 162-165.
40. Stadtman ER, Levine RL (2000) Protein oxidation. Ann N Y Acad Sci 899: 191-208.
41. Stewart KL, Lephart ED (2023) Overview of BPH: Symptom Relief with Dietary Polyphenols, Vitamins and Phytochemicals by Nutraceutical Supplements with Implications to the Prostate Microbiome. Int J Mol Sci 24: 5486.
42. Strzeżek R, Koziorowska-Gilun M, Kowalówka M, Strzeżek J (2009) Characteristics of antioxidant system in dog semen. Pol J Vet Sci 12: 55-60.
43. Tong Y, Zhou RY (2020) Review of the roles and interaction of androgen and inflammation in benign prostatic hyperplasia. Mediators Inflamm 2020: 7958316.
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45. Vital P, Castro P, Ittmann M (2016) Oxidative stress promotes benign prostatic hyperplasia. Prostate 76: 58-67.
46. Worobiej E, Klepacka M (2003) Degradation changes induced by hydroxyl radicals in bean (Phaseolus vulgaris) and pea (Pisum sa-tivum) proteins. Pol J Food Nutr Sci 53: 13-17.
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Autorzy i Afiliacje

A. Domosławska
1
S. Zduńczyk
1
A. Bielecka
2
M. Kankofer
2

  1. Department of Animal Reproduction with Clinic, University of Warmia and Mazury, 10-719 Olsztyn, Oczapowskiego 14, Poland
  2. Department of Biochemistry, Faculty of Veterinary Medicine, University of Life Sciences, 20-033 Lublin, Akademicka 12, Lublin, Poland
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Abstrakt

The aim of this study was to evaluate the effect of benign prostatic hyperplasia (BPH) on nitric oxide (NO) production by spermatozoa and sperm parameters in dogs. The study was conducted on 40 intact dogs of various breeds. The dogs were assigned to two groups: BPH group (n=20) and non-affected group (n=20). The sperm concentration and motility parameters of spermatozoa were assessed using computer-assisted sperm analysis. For the assessment of sperm morphology monochromatic Diff-Quick stain was used. Plasma membrane integrity, mitochondrial membrane potential and the spermatozoa producing nitric oxide and with apoptotic-like changes were determined using fluorescent stain methods. The percentages of motile sperm, sperm with progressive motility and normal sperm were statistically significantly (p<0.05) lower in dogs with BPH than in non-affected dogs. The proportion of sperm in motility subcategory RAPID was statistically significantly (p<0.05) lower in dogs with BPH than in control dogs, whereas in the STATIC motility subcategory the proportion was significantly (p<0.05) higher in dogs with BPH. The percentage of spermatozoa producing NO was significantly (p<0.05) higher in dogs with BPH than in control dogs. In conclusion, the results of this study showed that BPH adversely affects semen quality, especially motility, in dogs. The decreased semen quality was associated with an increased proportion of spermatozoa generating NO. Further research is needed to clarify the mechanisms by which BPH affects semen quality.
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Bibliografia

1. Agarwal A, Virk G, Ong C, du Plessis SS (2014) Effect of oxidative stress on male reproduction. World J Mens Health 32: 1-17.
2. Angrimani DS, Brito MM, Rui BR, Nichi M, Vannucchi CI (2020) Reproductive and endocrinological effects of Benign Prostatic Hy-perplasia and finasteride therapy in dogs. Sci Rep 10: 14834.
3. Aquino-Cortez A, Pinheiro BQ, Lima DB, Silva HV, Mota-Filho AC, Martins JAM Rodriguez-Villamil P, Moura AA, Silva LD (2017) Proteomic characterization of canine seminal plasma. Theriogenology 95: 178-186.
4. Balercia G, Moretti S, Vignini A, Magagnini M, Mantero F, Boscaro M, Ricciardo-Lamonica G, Mazzanti L (2004) Role of nitric oxide concentrations on human sperm motility. J Androl 25: 245-249.
5. Berry SJ, Strandberg JD, Saunders WJ, Coffey DS (1986) Development of canine benign prostatic hyperplasia with age. Prostate 9: 363-73.
6. Carson C 3rd, Rittmaster R (2003) The role of dihydrotestosterone in benign prostatic hyperplasia. Urology 61 (4 Suppl 1): 2-7.
7. Cochran RC, Ewing LL, Niswender GD (1981) Serum levels of follicle stimulating hormone, luteinizing hormone, prolactin, testos-terone, 5 alpha-dihydrotestosterone, 5 alpha-androstane-3 alpha, 17 beta-diol, 5 alpha-androstane-3 beta, 17 beta-diol, and 17 be-ta-estradiol from male beagles with spontaneous or induced benign prostatic hyperplasia. Invest Urol 19: 142-147.
8. Cunto M, Ballotta G, Zambelli D (2022) Benign prostatic hyperplasia in the dog. Anim Reprod Sci 247: 107096.
9. Dearakhshandeh N, Mogheiseh A, Nazifi S, Ahrari Khafi MS, Abbaszadeh Hasiri M, Golchin-Rad K (2019) Changes in the oxidative stress factors and inflammatory proteins following the treatment of BPH induced dogs with an anti-proliferative agent called tadalafil. J Vet Pharmacol Ther 42: 665–672.
10. Domosławska A, Zduńczyk S, Kankofer M, Bielecka A (2022) Oxidative stress biomarkers in dogs with benign prostatic hyperplasia. Ir Vet J 75: 21.
11. Domosławska A, Zduńczyk S, Niżański W, Janowski T (2013) Assessment of semen quality in infertile dogs using computer-assisted sperm analysis by the Hamilton-Thorne Semen Analyser. Bull Vet Inst Pulawy 57: 429-432.
12. Doshi SB, Khullar K, Sharma RK, Agarwal A (2012) Role of reactive nitrogen species in male infertility. Reprod Biol Endocrinol 10: 109.
13. Fafula RV, Iefremova UP, Onufrovych OK, Maksymyuk HV, Besedina AS, Nakonechnyi IA, Vorobets DZ, Vorobets ZD (2018) Al-terations in Arginase-NO-synthase System of Spermatozoa in Human Subjects with Different Fertility Potential. J Med Biochem 37: 134-140.
14. Ferré-Dolcet L, Frigotto L, Contiero B, Bedin S, Romagnoli S (2022) Prostatic fluid composition and semen quality in dogs with benign prostatic hyperplasia undergoing treatment with osaterone acetate. Reprod Domest Anim 57: 72-79.
15. Flores RB, Angrimani D, Rui BR, Brito MM, Abreu RA, Vannucchi CI (2017) The influence of benign prostatic hyperplasia on sperm morphological features and sperm DNA integrity in dogs. Repro Domest Anim 52 (Suppl 2): 310-315.
16. Fontbonne A (2011) Infertility in male dogs: recent advances. Rev Bras Reprod Anim 35: 266-273.
17. Fraser L, Lecewicz M, Strzeżek J (2002) Fluorometric assessments of viability and mitochondrial status of boar spermatozoa following liquid storage. Pol J Vet Sci 5: 85-92.
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20. Krakowski L, Wąchocka A, Brodzki P, Wrona Z, Piech T, Wawron W, Chałabis-Mazurek A (2015) Sperm quality and selected bio-chemical parameters of seminal fluid in dogs with benign prostatic hyperplasia. Anim Reprod Sci 160: 20-125.
21. Lampiao F, Huussen J, du Plessis SS (2014) Effects of nitric oxide exposure on human sperm function and apoptosis markers. Open Reprod Sci J 6: 17-20.
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23. Lévy X, Niżański W, von Heimendahl A, Mimouni P (2014) Diagnosis of common prostatic conditions in dogs: an update. Reprod Domest Anim 49 (Suppl 2): 50-57.
24. Linde-Forsberg C (1991) Achieving canine pregnancy by using frozen or chilled extended semen. Vet Clin North Am Small Anim Pract 21: 467-485.
25. Luo Y, Zhu Y, Basang W, Wang X, Li C, Zhou X (2021) Roles of Nitric Oxide in the Regulation of Reproduction: A Review. Front Endocrinol (Lausanne) 12: 52410.
26. Minciullo PL, Inferrera A, Navarra M, Calapai G, Magno C, Gangemi S (2015) Oxidative stress in benign prostatic hyperplasia: a sys-tematic review. Urol Int 94: 249-254.
27. Niżański W, Eberhardt M, Ochota M, Fontaine C, Levy X, Pasikowska J (2022) A Comparative Study of the Effects of Osaterone Ace-tate and Deslorelin Acetate on Sperm Kinematics and Morpho-Functional Parameters in Dogs. Animals (Basel) 12: 1548.
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33. Rosselli M, Dubey RK, Imthurn B, Macas E, Keller PJ (1995) Effects of nitric oxide on human spermatozoa: evidence that nitric oxide decreases sperm motility and induces sperm toxicity. Hum Reprod 10: 1786-1790.
34. Ruel Y, Barthez PY, Mailles A, Begon D (1998) Ultrasonographic evaluation of the prostate in healthy intact dogs. Vet Radiol Ultra-sound 39: 212-6.
35. Smith J (2008) Canine prostatic disease: a review of anatomy, pathology, diagnosis, and treatment. Theriogenology 70: 375-383.
36. Strzeżek R, Szemplińska K, Filipowicz K, Kordan W (2015) Semen characteristics and selected biochemical markers of canine seminal plasma in various seasons of the year. Pol J Vet Sci 18: 13-18.
37. Thomas CA, Garner DL, DeJarnette JM, Marshall CE (1998) Effect of cryopreservation of bovine sperm organelle function and viability as determined by flow cytometry. Biol Reprod 58: 786-793.
38. Tong Y, Zhou RY (2020) Review of the roles and interaction of androgen and inflammation in benign prostatic hyperplasia. Mediators Inflamm 2020: 7958316.
39. Trzcińska M, Bryła M (2015) Apoptotic-like changes of boar spermatozoa in freezing media supplemented with different antioxidants. Pol J Vet Sci 18: 473-480.
40. Uribe P, Boguen R, Treulen F, Sánchez R, Villegas JV (2015) Peroxynitrite-mediated nitrosative stress decreases motility and mitochon-drial membrane potential in human spermatozoa. Mol Hum Reprod 21: 237-243.
41. Vital P, Castro P, Ittmann M (2016) Oxidative stress promotes benign prostatic hyperplasia. Prostate 76: 58-67.
42. Volpe S, Leoci R, Aiudi G, Lacalandra GM (2009) Relationship between motility and mitochondrial functional status in canine sperma-tozoa. Reprod Domest Anim 44 (Suppl 2): 275-278.
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Autorzy i Afiliacje

A. Domoslawska-Wyderska
1
A. Orzołek
2
S. Zduńczyk
1
A. Rafalska
1

  1. Department of Animal Reproduction with Clinic, University of Warmia and Mazury, Oczapowskiego 14, 10-719 Olsztyn, Poland
  2. Department of Animal Biochemistry and Biotechnology, University of Warmia and Mazury, Oczapowskiego 5, 10-719 Olsztyn, Poland

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