Skip to main content
Top
Published in: Obesity Surgery 7/2021

01-07-2021 | Obesity | Original Contributions

Analysis of the Functional Aspects of Sperm and Testicular Oxidative Stress in Individuals Undergoing Metabolic Surgery

Authors: Roberta Maria Fariello, Renata Cristina de Carvalho, Deborah M. Spaine, Rhayza R. Andretta, Elesiário M. Caetano Jr, Gustavo P. D. Sá, Agnaldo P. Cedenho, Renato Fraietta

Published in: Obesity Surgery | Issue 7/2021

Login to get access

Abstract

Purpose

Metabolic surgery is a recommended treatment for obese patients that results in BMI reduction; however, the observed impact of this therapy on male fertility is inconsistent. This research aimed to study the effects of BMI changes after metabolic surgery on seminal analysis, sex hormonal profile, sperm functional integrity, and the seminal plasma lipid peroxidation levels.

Materials and Methods

A prospective study was performed in 15 patients for whom metabolic surgery was recommended. The patients were evaluated by the techniques proposed in this study before and after the surgical procedure for 12 months. In each analysis, the male sex hormonal profile, semen analysis, sperm functional integrity, and seminal lipid peroxidation levels were assessed.

Results

The surgery resulted in BMI reduction and improvement in seminal characteristics and male sex hormone profile. The semen analysis showed increases in volume, sperm progressive motility, and in sperm morphology and a decrease in immotile sperms. Sperm mitochondrial activity and sperm DNA integrity were improved, and the levels of seminal lipid peroxidation were decreased. The hormonal profile showed lower levels of estradiol and highest levels of luteinizing hormone (LH), sex hormone-binding globulin (SHBG), and testosterone.

Conclusion

BMI changes resulting from this treatment and its metabolic consequences can be associated with changes in the male fertile potential, leading to an improvement in the seminal quality, male sex hormone profile, sperm functional aspects, and levels of seminal lipid peroxidation, thus decreasing the testicular oxidative stress.

Graphical Abstract

Literature
1.
go back to reference World Health Organization. Laboratory manual for the examination of human semen and sperm-cervical mucus interaction. 4th ed. New York: Cambridge University Press; 1999. World Health Organization. Laboratory manual for the examination of human semen and sperm-cervical mucus interaction. 4th ed. New York: Cambridge University Press; 1999.
2.
go back to reference Moschos S, Chan JL, Mantzoros CS. Leptin and reproduction: a review. Fertil Steril. 2002;77(3):433–44.PubMedCrossRef Moschos S, Chan JL, Mantzoros CS. Leptin and reproduction: a review. Fertil Steril. 2002;77(3):433–44.PubMedCrossRef
3.
go back to reference Pasquali R, Pelusi C, Genghini S, et al. Obesity and reproductive disorders in women. Hum Reprod Update. 2003;9(4):359–72.PubMedCrossRef Pasquali R, Pelusi C, Genghini S, et al. Obesity and reproductive disorders in women. Hum Reprod Update. 2003;9(4):359–72.PubMedCrossRef
4.
go back to reference Jensen TK, Andersson A-M, Jørgensen N, et al. Body mass index in relation to semen quality and reproductive hormones among 1,558 Danish men. Fertil Steril. 2004;82(4):863–70.PubMedCrossRef Jensen TK, Andersson A-M, Jørgensen N, et al. Body mass index in relation to semen quality and reproductive hormones among 1,558 Danish men. Fertil Steril. 2004;82(4):863–70.PubMedCrossRef
5.
go back to reference Kort HI, Massey JB, Elsner CW, et al. Impact of body mass index values on sperm quantity and quality. J Androl. 2006;27(3):450–2.PubMedCrossRef Kort HI, Massey JB, Elsner CW, et al. Impact of body mass index values on sperm quantity and quality. J Androl. 2006;27(3):450–2.PubMedCrossRef
6.
go back to reference Hammoud AO, Gibson M, Peterson CM, et al. Impact of male obesity on infertility: a critical review of the current literature. Fertil Steril. 2008;90(4):897–904.PubMedCrossRef Hammoud AO, Gibson M, Peterson CM, et al. Impact of male obesity on infertility: a critical review of the current literature. Fertil Steril. 2008;90(4):897–904.PubMedCrossRef
7.
go back to reference Berga SL, Yen SSC. Reproductive failure due to central nervous system–hypothalamic–pituitary dysfunction. In: Yen and Jaffe’s reproductive endocrinology. 5th ed. Philadelphia: Elsevier; 2004. Berga SL, Yen SSC. Reproductive failure due to central nervous system–hypothalamic–pituitary dysfunction. In: Yen and Jaffe’s reproductive endocrinology. 5th ed. Philadelphia: Elsevier; 2004.
8.
go back to reference Jung A, Schill WB. Male infertility. Current life style could be responsible for infertility. MMW Fortschr Med. 2000;142(37):31–3.PubMed Jung A, Schill WB. Male infertility. Current life style could be responsible for infertility. MMW Fortschr Med. 2000;142(37):31–3.PubMed
9.
go back to reference Kasturi SS, Tannir J, Brannigan RE. The metabolic syndrome and male infertility. J Androl. 2008;29(3):251–9.PubMedCrossRef Kasturi SS, Tannir J, Brannigan RE. The metabolic syndrome and male infertility. J Androl. 2008;29(3):251–9.PubMedCrossRef
10.
go back to reference Agarwal A, Saleh RA. Role of oxidants in male infertility: rationale, significance, and treatment. Urol Clin North Am. 2002;29(4):817–27.PubMedCrossRef Agarwal A, Saleh RA. Role of oxidants in male infertility: rationale, significance, and treatment. Urol Clin North Am. 2002;29(4):817–27.PubMedCrossRef
11.
go back to reference Sharma RK, Agarwal A. Role of reactive oxygen species in male infertility. Urology. 1996;48(6):835–50.PubMedCrossRef Sharma RK, Agarwal A. Role of reactive oxygen species in male infertility. Urology. 1996;48(6):835–50.PubMedCrossRef
12.
go back to reference de Lamirande E, Jiang H, Zini A, et al. Reactive oxygen species and sperm physiology. Rev Reprod. 1997;2(1):48–54.PubMedCrossRef de Lamirande E, Jiang H, Zini A, et al. Reactive oxygen species and sperm physiology. Rev Reprod. 1997;2(1):48–54.PubMedCrossRef
13.
go back to reference Aitken RJ, Clarkson JS. Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. J Reprod Fertil. 1987;81(2):459–69.PubMedCrossRef Aitken RJ, Clarkson JS. Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. J Reprod Fertil. 1987;81(2):459–69.PubMedCrossRef
14.
go back to reference Alvarez JG, Touchstone JC, Blasco L, et al. Spontaneous lipid peroxidation and production of hydrogen peroxide and superoxide in human spermatozoa. Superoxide dismutase as major enzyme protectant against oxygen toxicity. J Androl. 1987;8(5):338–48.PubMedCrossRef Alvarez JG, Touchstone JC, Blasco L, et al. Spontaneous lipid peroxidation and production of hydrogen peroxide and superoxide in human spermatozoa. Superoxide dismutase as major enzyme protectant against oxygen toxicity. J Androl. 1987;8(5):338–48.PubMedCrossRef
15.
go back to reference Ollero M, Gil-Guzman E, Lopez MC, et al. Characterization of subsets of human spermatozoa at different stages of maturation: implications in the diagnosis and treatment of male infertility. Hum Reprod. 2001;16(9):1912–21.PubMedCrossRef Ollero M, Gil-Guzman E, Lopez MC, et al. Characterization of subsets of human spermatozoa at different stages of maturation: implications in the diagnosis and treatment of male infertility. Hum Reprod. 2001;16(9):1912–21.PubMedCrossRef
16.
go back to reference Li K, Shang X, Chen Y. High-performance liquid chromatographic detection of lipid peroxidation in human seminal plasma and its application to male infertility. Clin Chim Acta. 2004;346(2):199–203.PubMedCrossRef Li K, Shang X, Chen Y. High-performance liquid chromatographic detection of lipid peroxidation in human seminal plasma and its application to male infertility. Clin Chim Acta. 2004;346(2):199–203.PubMedCrossRef
17.
go back to reference Santry HP, Gillen DL, Lauderdale DS. Trends in bariatric surgical procedures. JAMA. 2005;294(15):1909–17.PubMedCrossRef Santry HP, Gillen DL, Lauderdale DS. Trends in bariatric surgical procedures. JAMA. 2005;294(15):1909–17.PubMedCrossRef
18.
go back to reference Calle EE, Thun MJ, Petrelli JM, et al. Body-mass index and mortality in a prospective cohort of U.S. adults. N Engl J Med. 1999;341(15):1097–105.PubMedCrossRef Calle EE, Thun MJ, Petrelli JM, et al. Body-mass index and mortality in a prospective cohort of U.S. adults. N Engl J Med. 1999;341(15):1097–105.PubMedCrossRef
19.
go back to reference Fejes I, Koloszár S, Závaczki Z, et al. Effect of body weight on testosterone/estradiol ratio in oligozoospermic patients. Arch Androl. 2006;52(2):97–102.PubMedCrossRef Fejes I, Koloszár S, Závaczki Z, et al. Effect of body weight on testosterone/estradiol ratio in oligozoospermic patients. Arch Androl. 2006;52(2):97–102.PubMedCrossRef
20.
go back to reference Sallmén M, Sandler DP, Hoppin JA, et al. Reduced fertility among overweight and obese men. Epidemiology. 2006;17(5):520–3.PubMedCrossRef Sallmén M, Sandler DP, Hoppin JA, et al. Reduced fertility among overweight and obese men. Epidemiology. 2006;17(5):520–3.PubMedCrossRef
21.
go back to reference Vázquez C, Morejón E, Muñoz C, et al. Nutritional effect of bariatric surgery with Scopinaro operation. Analysis of 40 cases. Nutr Hosp. 2003;18(4):189–93.PubMed Vázquez C, Morejón E, Muñoz C, et al. Nutritional effect of bariatric surgery with Scopinaro operation. Analysis of 40 cases. Nutr Hosp. 2003;18(4):189–93.PubMed
22.
go back to reference di Frega AS, Dale B, Di Matteo L, et al. Secondary male factor infertility after Roux-en-Y gastric bypass for morbid obesity: case report. Hum Reprod. 2005;20(4):997–8.PubMedCrossRef di Frega AS, Dale B, Di Matteo L, et al. Secondary male factor infertility after Roux-en-Y gastric bypass for morbid obesity: case report. Hum Reprod. 2005;20(4):997–8.PubMedCrossRef
23.
24.
go back to reference World Health Organization. WHO laboratory manual for the examination and processing of human semen. 5th ed. Geneva, Switzerland; 2010. World Health Organization. WHO laboratory manual for the examination and processing of human semen. 5th ed. Geneva, Switzerland; 2010.
25.
go back to reference Kruger TF, Menkveld R, Stander FS, et al. Sperm morphologic features as a prognostic factor in in vitro fertilization. Fertil Steril. 1986;46(6):1118–23.PubMedCrossRef Kruger TF, Menkveld R, Stander FS, et al. Sperm morphologic features as a prognostic factor in in vitro fertilization. Fertil Steril. 1986;46(6):1118–23.PubMedCrossRef
26.
27.
go back to reference Fariello RM, Del Giudice PT, Spaine DM, et al. Effect of leukocytospermia and processing by discontinuous density gradient on sperm nuclear DNA fragmentation and mitochondrial activity. J Assist Reprod Genet. 2009;26(2–3):151–7.PubMedPubMedCentralCrossRef Fariello RM, Del Giudice PT, Spaine DM, et al. Effect of leukocytospermia and processing by discontinuous density gradient on sperm nuclear DNA fragmentation and mitochondrial activity. J Assist Reprod Genet. 2009;26(2–3):151–7.PubMedPubMedCentralCrossRef
28.
go back to reference Hrudka F. Cytochemical and ultracytochemical demonstration of cytochrome c oxidase in spermatozoa and dynamics of its changes accompanying ageing or induced by stress. Int J Androl. 1987;10(6):809–28.PubMedCrossRef Hrudka F. Cytochemical and ultracytochemical demonstration of cytochrome c oxidase in spermatozoa and dynamics of its changes accompanying ageing or induced by stress. Int J Androl. 1987;10(6):809–28.PubMedCrossRef
29.
go back to reference Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem. 1979;95(2):351–8.PubMedCrossRef Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem. 1979;95(2):351–8.PubMedCrossRef
30.
go back to reference Oehninger S. Clinical and laboratory management of male infertility: an opinion on its current status. J Androl. 2000;21(6):814–21.PubMed Oehninger S. Clinical and laboratory management of male infertility: an opinion on its current status. J Androl. 2000;21(6):814–21.PubMed
31.
go back to reference Carra E, Sangiorgi D, Gattuccio F, et al. Male infertility and mitochondrial DNA. Biochem Biophys Res Commun. 2004;322(1):333–9.PubMedCrossRef Carra E, Sangiorgi D, Gattuccio F, et al. Male infertility and mitochondrial DNA. Biochem Biophys Res Commun. 2004;322(1):333–9.PubMedCrossRef
33.
go back to reference Ogden CL, Carroll MD, Kit BK, et al. Prevalence of obesity and trends in body mass index among US children and adolescents, 1999-2010. JAMA. 2012;307(5):483–90.PubMedPubMedCentralCrossRef Ogden CL, Carroll MD, Kit BK, et al. Prevalence of obesity and trends in body mass index among US children and adolescents, 1999-2010. JAMA. 2012;307(5):483–90.PubMedPubMedCentralCrossRef
35.
go back to reference World Health Organization. Global database on body mass index. Department of Nutrition for Health and Development. 2006; World Health Organization. Global database on body mass index. Department of Nutrition for Health and Development. 2006;
36.
go back to reference Loret de Mola JR. Obesity and its relationship to infertility in men and women. Obstet Gynecol Clin N Am. 2009;36(2):333–46. ixCrossRef Loret de Mola JR. Obesity and its relationship to infertility in men and women. Obstet Gynecol Clin N Am. 2009;36(2):333–46. ixCrossRef
37.
go back to reference Pasquali R, Vicennati V, Gambineri A. Adrenal and gonadal function in obesity. J Endocrinol Investig. 2002;25(10):893–8.CrossRef Pasquali R, Vicennati V, Gambineri A. Adrenal and gonadal function in obesity. J Endocrinol Investig. 2002;25(10):893–8.CrossRef
39.
go back to reference Hassan MAM, Killick SR. Negative lifestyle is associated with a significant reduction in fecundity. Fertil Steril. 2004;81(2):384–92.PubMedCrossRef Hassan MAM, Killick SR. Negative lifestyle is associated with a significant reduction in fecundity. Fertil Steril. 2004;81(2):384–92.PubMedCrossRef
40.
go back to reference Calderón B, Huerta L, Galindo J, et al. Lack of improvement of sperm characteristics in obese males after obesity surgery despite the beneficial changes observed in reproductive hormones. Obes Surg. 2019;29(7):2045–50.PubMedCrossRef Calderón B, Huerta L, Galindo J, et al. Lack of improvement of sperm characteristics in obese males after obesity surgery despite the beneficial changes observed in reproductive hormones. Obes Surg. 2019;29(7):2045–50.PubMedCrossRef
41.
go back to reference El Bardisi H, Majzoub A, Arafa M, et al. Effect of bariatric surgery on semen parameters and sex hormone concentrations: a prospective study. Reprod BioMed Online. 2016;33(5):606–11.PubMedCrossRef El Bardisi H, Majzoub A, Arafa M, et al. Effect of bariatric surgery on semen parameters and sex hormone concentrations: a prospective study. Reprod BioMed Online. 2016;33(5):606–11.PubMedCrossRef
42.
go back to reference Lee Y, Dang JT, Switzer N, et al. Impact of bariatric surgery on male sex hormones and sperm quality: a systematic review and meta-analysis. Obes Surg. 2019;29(1):334–46.PubMedCrossRef Lee Y, Dang JT, Switzer N, et al. Impact of bariatric surgery on male sex hormones and sperm quality: a systematic review and meta-analysis. Obes Surg. 2019;29(1):334–46.PubMedCrossRef
43.
go back to reference Nielsen TL, Hagen C, Wraae K, et al. Visceral and subcutaneous adipose tissue assessed by magnetic resonance imaging in relation to circulating androgens, sex hormone-binding globulin, and luteinizing hormone in young men. J Clin Endocrinol Metab. 2007;92(7):2696–705.PubMedCrossRef Nielsen TL, Hagen C, Wraae K, et al. Visceral and subcutaneous adipose tissue assessed by magnetic resonance imaging in relation to circulating androgens, sex hormone-binding globulin, and luteinizing hormone in young men. J Clin Endocrinol Metab. 2007;92(7):2696–705.PubMedCrossRef
44.
go back to reference Schneider G, Kirschner MA, Berkowitz R, et al. Increased estrogen production in obese men. J Clin Endocrinol Metab. 1979;48(4):633–8.PubMedCrossRef Schneider G, Kirschner MA, Berkowitz R, et al. Increased estrogen production in obese men. J Clin Endocrinol Metab. 1979;48(4):633–8.PubMedCrossRef
45.
go back to reference Giagulli VA, Kaufman JM, Vermeulen A. Pathogenesis of the decreased androgen levels in obese men. J Clin Endocrinol Metab. 1994;79(4):997–1000.PubMed Giagulli VA, Kaufman JM, Vermeulen A. Pathogenesis of the decreased androgen levels in obese men. J Clin Endocrinol Metab. 1994;79(4):997–1000.PubMed
46.
go back to reference Globerman H, Shen-Orr Z, Karnieli E, et al. Inhibin B in men with severe obesity and after weight reduction following gastroplasty. Endocr Res. 2005;31(1):17–26.PubMedCrossRef Globerman H, Shen-Orr Z, Karnieli E, et al. Inhibin B in men with severe obesity and after weight reduction following gastroplasty. Endocr Res. 2005;31(1):17–26.PubMedCrossRef
47.
go back to reference Fariello RM, Pariz JR, Spaine DM, et al. Association between obesity and alteration of sperm DNA integrity and mitochondrial activity. BJU Int. 2012;110(6):863–7.PubMedCrossRef Fariello RM, Pariz JR, Spaine DM, et al. Association between obesity and alteration of sperm DNA integrity and mitochondrial activity. BJU Int. 2012;110(6):863–7.PubMedCrossRef
48.
go back to reference Samavat J, Cantini G, Lotti F, et al. Massive weight loss obtained by bariatric surgery affects semen quality in morbid male obesity: a preliminary prospective double-armed study. Obes Surg. 2018;28(1):69–76.PubMedCrossRef Samavat J, Cantini G, Lotti F, et al. Massive weight loss obtained by bariatric surgery affects semen quality in morbid male obesity: a preliminary prospective double-armed study. Obes Surg. 2018;28(1):69–76.PubMedCrossRef
49.
go back to reference Reis LO, Zani EL, Saad RD, et al. Bariatric surgery does not interfere with sperm quality--a preliminary long-term study. Reprod Sci. 2012;19(10):1057–62.PubMedCrossRef Reis LO, Zani EL, Saad RD, et al. Bariatric surgery does not interfere with sperm quality--a preliminary long-term study. Reprod Sci. 2012;19(10):1057–62.PubMedCrossRef
50.
go back to reference Moustafa MH, Sharma RK, Thornton J, et al. Relationship between ROS production, apoptosis and DNA denaturation in spermatozoa from patients examined for infertility. Hum Reprod. 2004;19(1):129–38.PubMedCrossRef Moustafa MH, Sharma RK, Thornton J, et al. Relationship between ROS production, apoptosis and DNA denaturation in spermatozoa from patients examined for infertility. Hum Reprod. 2004;19(1):129–38.PubMedCrossRef
51.
go back to reference Smith R, Kaune H, Parodi D, et al. Increased sperm DNA damage in patients with varicocele: relationship with seminal oxidative stress. Hum Reprod. 2006;21(4):986–93.PubMedCrossRef Smith R, Kaune H, Parodi D, et al. Increased sperm DNA damage in patients with varicocele: relationship with seminal oxidative stress. Hum Reprod. 2006;21(4):986–93.PubMedCrossRef
52.
go back to reference Agarwal A, Said TM. Role of sperm chromatin abnormalities and DNA damage in male infertility. Hum Reprod Update. 2003;9(4):331–45.PubMedCrossRef Agarwal A, Said TM. Role of sperm chromatin abnormalities and DNA damage in male infertility. Hum Reprod Update. 2003;9(4):331–45.PubMedCrossRef
53.
go back to reference Sakkas D, Manicardi GC, Bizzaro D. Sperm nuclear DNA damage in the human. Adv Exp Med Biol. 2003;518:73–84.PubMedCrossRef Sakkas D, Manicardi GC, Bizzaro D. Sperm nuclear DNA damage in the human. Adv Exp Med Biol. 2003;518:73–84.PubMedCrossRef
54.
go back to reference Belcheva A, Ivanova-Kicheva M, Tzvetkova P, et al. Effects of cigarette smoking on sperm plasma membrane integrity and DNA fragmentation. Int J Androl. 2004;27(5):296–300.PubMedCrossRef Belcheva A, Ivanova-Kicheva M, Tzvetkova P, et al. Effects of cigarette smoking on sperm plasma membrane integrity and DNA fragmentation. Int J Androl. 2004;27(5):296–300.PubMedCrossRef
55.
go back to reference Kasai T, Ogawa K, Mizuno K, et al. Relationship between sperm mitochondrial membrane potential, sperm motility, and fertility potential. Asian J Androl. 2002;4(2):97–103.PubMed Kasai T, Ogawa K, Mizuno K, et al. Relationship between sperm mitochondrial membrane potential, sperm motility, and fertility potential. Asian J Androl. 2002;4(2):97–103.PubMed
56.
go back to reference Aitken RJ, Irvine DS, Wu FC. Prospective analysis of sperm-oocyte fusion and reactive oxygen species generation as criteria for the diagnosis of infertility. Am J Obstet Gynecol. 1991;164(2):542–51.PubMedCrossRef Aitken RJ, Irvine DS, Wu FC. Prospective analysis of sperm-oocyte fusion and reactive oxygen species generation as criteria for the diagnosis of infertility. Am J Obstet Gynecol. 1991;164(2):542–51.PubMedCrossRef
Metadata
Title
Analysis of the Functional Aspects of Sperm and Testicular Oxidative Stress in Individuals Undergoing Metabolic Surgery
Authors
Roberta Maria Fariello
Renata Cristina de Carvalho
Deborah M. Spaine
Rhayza R. Andretta
Elesiário M. Caetano Jr
Gustavo P. D. Sá
Agnaldo P. Cedenho
Renato Fraietta
Publication date
01-07-2021
Publisher
Springer US
Published in
Obesity Surgery / Issue 7/2021
Print ISSN: 0960-8923
Electronic ISSN: 1708-0428
DOI
https://doi.org/10.1007/s11695-021-05350-9

Other articles of this Issue 7/2021

Obesity Surgery 7/2021 Go to the issue