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Chinyere Nsonwu-Anyanwu, A., Raymond Ekong, E., Jeremiah Offor, S., Francis Awusha, O., Chukwuma Orji, O., Idiongo Umoh, E., Aleruchim Owhorji, J., Rowland Emetonjor, F., & Adanna Opara Usoro, C. (2019). Heavy metals, biomarkers of oxidative stress and changes in sperm function: A case-control study. International Journal of Reproductive BioMedicine (IJRM), 17(3). https://doi.org/10.18502/ijrm.v17i3.4515
https://doi.org/10.18502/ijrm.v17i3.4515
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- Cited by 15 articles
authors
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Augusta Chinyere Nsonwu-Anyanwu
No author data available.
-
Eworo Raymond Ekong
No author data available.
-
Sunday Jeremiah Offor
No author data available.
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Ogar Francis Awusha
No author data available.
-
Oliver Chukwuma Orji
No author data available.
-
Ediang Idiongo Umoh
No author data available.
-
Jennifer Aleruchim Owhorji
No author data available.
-
Faith Rowland Emetonjor
No author data available.
-
Chinyere Adanna Opara Usoro
No author data available.
Published Date
- May 29, 2019
Heavy metals, biomarkers of oxidative stress and changes in sperm function: A case-control study
Abstract
Background: Heavy metal-induced oxidative stress has been implicated in abnormal sperm functions and male infertility.
Objective: Serum and seminal levels of heavy metals and biomarkers of oxidative stress were compared in fertile and infertile men.
Materials and Methods: A total of 130 men aged 20–60 yr comprising 30 azoospermic, 50 oligozoospermic, and 50 normozoospermic men were studied. Semen analysis was done by world health organization guidelines, biomarkers of oxidative stress (total antioxidant capacity (TAC), total plasma peroxidase (TPP), oxidative stress index (OSI), vitamin C (vit C) and nitric oxide (NO)) and fructose by colorimetry and serum and seminal heavy metals (zinc (Zn), selenium (Se), cadmium (Cd) and lead (Pb)) by atomic absorption spectrophotometry.
Results: Azoospermic and oligozoospermic men had higher serum and seminal peroxides (TPP, p = 0.00), higher serum heavy metals (Zn, Se, Pb, and Cd (p = 0.01)) and lower sperm concentration, %motility, serum and seminal antioxidants (vit C, TAC, NO, GSH (p = 0.01)) compared to normozoospermic men. Higher seminal peroxides (TPP, p = 0.001), heavy metals (Pb and Cd (p = 0.03)) and lower sperm concentration, %motility, and seminal antioxidants (TAC and NO (p = 0.00)) were also observed in azoospermic men compared to oligozoospermic men. Negative correlations were observed between seminal fructose and seminal vit C (r = -0.535, p = 0.015), GSH (r =-0.734, p = 0.000), NO (r = -0.714, p = 0.000), Zn (r = -0.774, p = 0.000) and Se (r = -0.719, p = 0.000) only in azoospermic men.
Conclusion: Elevated heavy metal levels, increased lipid peroxidation and antioxidant depletion is associated with abnormal sperm functions in men studied.
Key words: Heavy metals, Antioxidants, Lipid peroxidation, Oxidative stress, Sperm function.
References
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[5] Agarwal A, Virk G, Ong C, du Plessis SS. Effect of oxidative stress on male reproduction. World J Mens Health 2014; 32: 1–17.
[6] Venkatesh S, Deecaraman M, Kumar R, Shamsi MB, Dada R. Role of reactive oxygen species in the pathogenesis of mitochondrial DNA (mtDNA) mutations in male infertility. Indian J Med Res 2009; 129: 127–137.
[7] Atig F, Raffa M, Habib BA, Kerkeni A, Saad A, Ajina M. Impact of seminal trace element and glutathione levels on semen quality of Tunisian infertile men. BMC Urol 2012; 12: 6–14.
[8] Al-Azzawie HF, Naeim M, Saleman ED, Hasan FAl. Evaluation of enzymatic and non-enzymatic antioxidant status in seminal plasma of Iraqi infertile men. Int J Adv Res 2014, 2: 158–167.
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[10] National Collaborating Centre for Women’s and Children’s Health (UK). Fertility: assessment and treatment for people with fertility problems. National Institute for Health and Clinical Excellence: Guidance; 2004.
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[13] Everson ME. Spectrophotometric techniques, In Tietz Textbook of Clinical Chemistry, CA Burtis and ER Ashwood, Eds., 3rd Ed. W. B. Saunders, Philadelphia, Pa, USA, 1999: 75–93.
[14] Koracevic D, Koracevic G, Djordjevic V, Andrejevic S, Cosic V. Method for the measurement of antioxidant activity in human fluids. J Clin Pathol 2001; 54: 356–361.
[15] Miyazawa T. Determination of phospholipid hydroperoxides in human blood plasma by a chemiluminescenceHPLC assay. Free Radic Biol Med 1989; 7: 209–217.
[16] Miranda KM, Espey MG, Wink DA. A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 2001; 5: 62–71.
[17] Bulaj G, Kortemme T, Goldenberg DP. Ionization-reactivity relationships for cysteine thiols in polypeptides. Biochemistry 1998; 37: 8965–8972.
[18] World Health Organisation. WHO laboratory manual for the Examination and processing of human semen. 5th Ed. Cambridge University Press, Cambridge, UK, 2010.
[19] Roe JH, Kuether CA. The Determination of Ascorbic Acid in whole blood and urine through the 2, 4-dinitrophenylhydrazine derivative of dehydroascorbic Acid. J Biol Chem. 1943; 147: 399–402.
[20] Agarwal A, Prabakaran SA. Mechanism, measurement, and prevention of oxidative stress in male reproductive physiology. Indian J Exp Biol 2005; 43: 963–974.
[21] Aitken RJ, Baker MA. Causes and consequences of apoptosis in spermatozoa; contributions to infertility and impacts on development. Int J Dev Biol 2013; 57: 265–272.
[22] Yousefniapasha Y, Jorsaraei G, Gholinezhadchari M, Mahjoub S, Hajiahmadi M, Farsi M. Nitric oxide levels and total antioxidant capacity in the seminal plasma of infertile smoking men. Cell J 2015; 17: 129–136.
[23] Khatoon F, Batool S, Omer S, Balouch Z, Mushtaq M. Correlation and reproductive hormone and fructose with sperm count and motility in infertile males. J Multidisciplinary Res 2014; 3: 171–179.
[24] Aumuller G, Riva A. Morphology and functions of the human seminal vesicle. Andrologia 1992; 24: 183–196.
[25] Amidu N, Owiredu WKBA, Bekoe MAT, Quaye L. The impact of seminal zinc and fructose concentration on human sperm characteristic. J Med Biomed Sci 2012; 1: 14–20.
[26] Angulo C, Maldonado R, Pulgar E, Mancilla H, Córdova1 A, Villarroel F, et al. Vitamin C and oxidative stress in the seminiferous epithelium. Biol Res 2011; 44: 169–180.
[27] Young SS, Eskenazi B, Marchetti FM, Block G, Wyrobek AJ. The association of folate, zinc and antioxidant intake with sperm aneuploidy in healthy non-smoking men. Hum Reprod 2008, 23: 1014–1022.
[28] Miraglia E, De Angelis F, Gazzano E, Hassanpour H, Bertagna A, Aldieri E, et al. Nitric oxide stimulates human sperm motility via activation of the cyclic GMP/protein kinase G signaling pathway. Reproduction 2011; 141: 47–54.
[29] Amiri I, Sheikh N, Najafi R. Nitric oxide level in seminal plasma and its relation with sperm DNA damages. Iran Biomed J 2007; 11: 259–264.
[30] Badade ZG, More KM, Narshetty JG, Badade VZ, Yadav BK. Human seminal oxidative stress: correlation with antioxidants and sperm quality parameters. Ann Biol Res 2011; 2: 351–359.
[31] Kumar D, Salian SR, Kalthur G, Uppangala S, Kumari S, Challapalli S, et al. Association between sperm DNA integrity and seminal plasma antioxidant levels in health workers occupationally exposed to ionizing radiation. Environ Res 2014; 132: 297–304.
[32] Naher ZU, Biswas SK, Mollah FH, Ali M, Arslan MI. Role of Glutathione in Male Infertility. Bangladesh J Med Biochem 2011; 4: 20–25.
[33] Akinloye O, Abbiyesuku FM, Oguntibeju OO, Arowojolu AO, Truter EJ. The impact of blood and seminal plasma zinc and copper concentrations on spermogram and hormonal changes in infertile Nigerian men. Reprod Biol 2011; 11: 83–98.
[34] Colagar AH, Marzony ET, Chaichi MJ. Zinc levels in seminal plasma are associated with sperm quality in fertile and infertile men. Nutr Res 2009; 29: 82–88.
[35] Akinloye O, Arowojolu AO, Shittu OB, Adejuwon CA, Osotimehin B. Selenium status of idiopathic infertile Nigerian males. Biol Trace Elem Res 2005, 104; 9–18.
[36] Marzec-Wróblewska U, Kamiński P, Łakota P. Influence of chemical elements on mammalian spermatozoa. Folia Biol (Praha) 2012; 58: 7–15.
[37] Kasperczyk A, Kasperczyk S, Horak S, Ostałowska A, Grucka-Mamczar E, Romuk E, et al. Assessment of semen function and lipid peroxidation among lead exposed men. Toxicol Appl Pharmacol 2008; 228: 378–384.
[38] Ghaffari MA, Motlagh B. In vitro effect of lead, silver, tin, mercury, indium and bismuth on human sperm creatine kinase activity: a presumable mechanism for men infertility. Iran Biomed J 2011; 15: 38–43.
Basic Clin Reprod Sci 2015; 4: 45–53.
[2] World Health Organisation. Laboratory manual for the examination of human semen and sperm-cervical mucus interaction. 4th Ed. Cambridge University Press, 1999: 30–31.
[3] Nabil H, Moemen LA, Abu Elela MH. Studying the levels of malondialdehyde and antioxidant parameters in normal and abnormal human seminal plasma. Aust J Basic Appl Sci 2008; 2: 773–778.
[4] Benoff S, Jacob A, Hurley IR. Male infertility and environmental exposure to lead and cadmium. Hum Reprod Update 2000; 6: 107–121.
[5] Agarwal A, Virk G, Ong C, du Plessis SS. Effect of oxidative stress on male reproduction. World J Mens Health 2014; 32: 1–17.
[6] Venkatesh S, Deecaraman M, Kumar R, Shamsi MB, Dada R. Role of reactive oxygen species in the pathogenesis of mitochondrial DNA (mtDNA) mutations in male infertility. Indian J Med Res 2009; 129: 127–137.
[7] Atig F, Raffa M, Habib BA, Kerkeni A, Saad A, Ajina M. Impact of seminal trace element and glutathione levels on semen quality of Tunisian infertile men. BMC Urol 2012; 12: 6–14.
[8] Al-Azzawie HF, Naeim M, Saleman ED, Hasan FAl. Evaluation of enzymatic and non-enzymatic antioxidant status in seminal plasma of Iraqi infertile men. Int J Adv Res 2014, 2: 158–167.
[9] The Practice Committee of the American Society for Reproductive Medicine. Definition of "infertility". Fertil Steril 2004; 82:S206.
[10] National Collaborating Centre for Women’s and Children’s Health (UK). Fertility: assessment and treatment for people with fertility problems. National Institute for Health and Clinical Excellence: Guidance; 2004.
[11] World Health Organization (WHO). Laboratory Manual for the Examination of Human Semen and Semen-Cervical Mucus Interaction, 5th Ed. Cambridge University Press, Cambridge, UK, 1992: 23.
[12] Comhaire F, Vermeulen L. Human semen analysis. Hum Reprod Update 1995; 1: 343–362.
[13] Everson ME. Spectrophotometric techniques, In Tietz Textbook of Clinical Chemistry, CA Burtis and ER Ashwood, Eds., 3rd Ed. W. B. Saunders, Philadelphia, Pa, USA, 1999: 75–93.
[14] Koracevic D, Koracevic G, Djordjevic V, Andrejevic S, Cosic V. Method for the measurement of antioxidant activity in human fluids. J Clin Pathol 2001; 54: 356–361.
[15] Miyazawa T. Determination of phospholipid hydroperoxides in human blood plasma by a chemiluminescenceHPLC assay. Free Radic Biol Med 1989; 7: 209–217.
[16] Miranda KM, Espey MG, Wink DA. A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 2001; 5: 62–71.
[17] Bulaj G, Kortemme T, Goldenberg DP. Ionization-reactivity relationships for cysteine thiols in polypeptides. Biochemistry 1998; 37: 8965–8972.
[18] World Health Organisation. WHO laboratory manual for the Examination and processing of human semen. 5th Ed. Cambridge University Press, Cambridge, UK, 2010.
[19] Roe JH, Kuether CA. The Determination of Ascorbic Acid in whole blood and urine through the 2, 4-dinitrophenylhydrazine derivative of dehydroascorbic Acid. J Biol Chem. 1943; 147: 399–402.
[20] Agarwal A, Prabakaran SA. Mechanism, measurement, and prevention of oxidative stress in male reproductive physiology. Indian J Exp Biol 2005; 43: 963–974.
[21] Aitken RJ, Baker MA. Causes and consequences of apoptosis in spermatozoa; contributions to infertility and impacts on development. Int J Dev Biol 2013; 57: 265–272.
[22] Yousefniapasha Y, Jorsaraei G, Gholinezhadchari M, Mahjoub S, Hajiahmadi M, Farsi M. Nitric oxide levels and total antioxidant capacity in the seminal plasma of infertile smoking men. Cell J 2015; 17: 129–136.
[23] Khatoon F, Batool S, Omer S, Balouch Z, Mushtaq M. Correlation and reproductive hormone and fructose with sperm count and motility in infertile males. J Multidisciplinary Res 2014; 3: 171–179.
[24] Aumuller G, Riva A. Morphology and functions of the human seminal vesicle. Andrologia 1992; 24: 183–196.
[25] Amidu N, Owiredu WKBA, Bekoe MAT, Quaye L. The impact of seminal zinc and fructose concentration on human sperm characteristic. J Med Biomed Sci 2012; 1: 14–20.
[26] Angulo C, Maldonado R, Pulgar E, Mancilla H, Córdova1 A, Villarroel F, et al. Vitamin C and oxidative stress in the seminiferous epithelium. Biol Res 2011; 44: 169–180.
[27] Young SS, Eskenazi B, Marchetti FM, Block G, Wyrobek AJ. The association of folate, zinc and antioxidant intake with sperm aneuploidy in healthy non-smoking men. Hum Reprod 2008, 23: 1014–1022.
[28] Miraglia E, De Angelis F, Gazzano E, Hassanpour H, Bertagna A, Aldieri E, et al. Nitric oxide stimulates human sperm motility via activation of the cyclic GMP/protein kinase G signaling pathway. Reproduction 2011; 141: 47–54.
[29] Amiri I, Sheikh N, Najafi R. Nitric oxide level in seminal plasma and its relation with sperm DNA damages. Iran Biomed J 2007; 11: 259–264.
[30] Badade ZG, More KM, Narshetty JG, Badade VZ, Yadav BK. Human seminal oxidative stress: correlation with antioxidants and sperm quality parameters. Ann Biol Res 2011; 2: 351–359.
[31] Kumar D, Salian SR, Kalthur G, Uppangala S, Kumari S, Challapalli S, et al. Association between sperm DNA integrity and seminal plasma antioxidant levels in health workers occupationally exposed to ionizing radiation. Environ Res 2014; 132: 297–304.
[32] Naher ZU, Biswas SK, Mollah FH, Ali M, Arslan MI. Role of Glutathione in Male Infertility. Bangladesh J Med Biochem 2011; 4: 20–25.
[33] Akinloye O, Abbiyesuku FM, Oguntibeju OO, Arowojolu AO, Truter EJ. The impact of blood and seminal plasma zinc and copper concentrations on spermogram and hormonal changes in infertile Nigerian men. Reprod Biol 2011; 11: 83–98.
[34] Colagar AH, Marzony ET, Chaichi MJ. Zinc levels in seminal plasma are associated with sperm quality in fertile and infertile men. Nutr Res 2009; 29: 82–88.
[35] Akinloye O, Arowojolu AO, Shittu OB, Adejuwon CA, Osotimehin B. Selenium status of idiopathic infertile Nigerian males. Biol Trace Elem Res 2005, 104; 9–18.
[36] Marzec-Wróblewska U, Kamiński P, Łakota P. Influence of chemical elements on mammalian spermatozoa. Folia Biol (Praha) 2012; 58: 7–15.
[37] Kasperczyk A, Kasperczyk S, Horak S, Ostałowska A, Grucka-Mamczar E, Romuk E, et al. Assessment of semen function and lipid peroxidation among lead exposed men. Toxicol Appl Pharmacol 2008; 228: 378–384.
[38] Ghaffari MA, Motlagh B. In vitro effect of lead, silver, tin, mercury, indium and bismuth on human sperm creatine kinase activity: a presumable mechanism for men infertility. Iran Biomed J 2011; 15: 38–43.