Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Association of decreased spermatozoa omega-3 fatty acid levels and increased oxidative DNA damage with varicocele in infertile men: a case control study

Li-Xin Tang A B F , Dong-Juan Yuan C D , Qi-Ling Wang A B , Fang Jiang A B , Jian Guo C , Yun-Ge Tang A B , Li-Xin Zheng A B and Jing X. Kang E F
+ Author Affiliations
- Author Affiliations

A Key Laboratory of Male Reproduction and Genetics, National Health and Family Planning Commission of China, Guangzhou 510000, China.

B Department of Andrology, Guangdong Family Planning Science and Technology Institute, Guangzhou 510030, China.

C Department of Biochemistry and Molecular Biology, Guangdong Medical College, Zhanjiang 524023, China.

D School of Light Industry and Food Sciences, South China University of Technology, Guangzhou 510630, China.

E Laboratory for Lipid Medicine and Technology, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02129, USA.

F Corresponding authors. Emails: tang-lixin@126.com; kang.jing@mgh.harvard.edu

Reproduction, Fertility and Development 28(5) 648-654 https://doi.org/10.1071/RD14276
Submitted: 30 July 2014  Accepted: 16 September 2014   Published: 19 November 2014

Abstract

Varicocele is commonly associated with male infertility because it impairs normal sperm morphology and activity. Polyunsaturated fatty acids (PUFA) are important determinants of sperm cell structure and function, but their relationship with varicocele remains unclear. The aim of the present study was to investigate the PUFA composition in spermatozoa of infertile men with varicocele and to evaluate the potential relationship between PUFA and varicocele. This case control study recruited 92 infertile men with varicocele, 99 infertile men without varicocele and 95 fertile male control subjects. Semen morphology and activity parameters were assessed and seminal plasma 8-hydroxy-2-deoxyguanosine (8-OHdG) content was determined by ELISA. Sperm concentrations of omega-3 and omega-6 fatty acids were measured by gas chromatography. Infertile men with varicocele had lower concentrations of omega-3 PUFA, higher omega-6 : omega-3 PUFA ratios and greater oxidative DNA damage in spermatozoa compared with infertile men without varicocele and normal subjects. The degree of varicocele and DNA damage was associated with decreased omega-3 PUFA concentrations and semen quality in infertile men with varicocele. The findings suggest that omega-3 PUFA deficiency could be implicated in varicocele-associated infertility, and highlight the need for intervention trials to test the usefulness of omega-3 supplementation in reducing sperm abnormalities in infertile men with varicocele.

Additional keywords: 8-hydroxy-2-deoxyguanosine, infertility, omega-6 fatty acids.


References

Agarwal, A., Hamada, A., and Esteves, S. C. (2012). Insight into oxidative stress in varicocele-associated male infertility: part 1. Nat. Rev. Urol. 9, 678–690.
Insight into oxidative stress in varicocele-associated male infertility: part 1.CrossRef | 23165403PubMed |

Barbieri, E. R., Hidalgo, M. E., Venegas, A., Smith, R., and Lissi, E. A. (1999). Varicocele-associated decrease in antioxidant defenses. J. Androl. 20, 713–717.
Varicocele-associated decrease in antioxidant defenses.CrossRef | 1:STN:280:DC%2BD3c%2FlslKjuw%3D%3D&md5=405ec607e4bd2d2e28941a903d109279CAS | 10591609PubMed |

Calamera, J., Buffone, M., Ollero, M., Alvarez, J., and Doncel, G. F. (2003). Superoxide dismutase content and fatty acid composition in subsets of human spermatozoa from normozoospermic, asthenozoospermic, and polyzoospermic semen samples. Mol. Reprod. Dev. 66, 422–430.
Superoxide dismutase content and fatty acid composition in subsets of human spermatozoa from normozoospermic, asthenozoospermic, and polyzoospermic semen samples.CrossRef | 1:CAS:528:DC%2BD3sXovFClurk%3D&md5=80e264ded8dcdb4ca50b86b8e05331d8CAS | 14579418PubMed |

Comhaire, F. H., Christophe, A. B., Zalata, A. A., Dhooge, W. S., Mahmoud, A. M., and Depuydt, C. E. (2000). The effects of combined conventional treatment, oral antioxidants and essential fatty acids on sperm biology in subfertile men. Prostaglandins Leukot. Essent. Fatty Acids 63, 159–165.
The effects of combined conventional treatment, oral antioxidants and essential fatty acids on sperm biology in subfertile men.CrossRef | 1:CAS:528:DC%2BD3cXnslGisbc%3D&md5=7b27c350c118b19a575321922612b584CAS | 10991774PubMed |

Conquer, J. A., Martin, J. B., Tummon, I., Watson, L., and Tekpetey, F. (1999). Fatty acid analysis of blood serum, seminal plasma, and spermatozoa of normozoospermic vs. asthenozoospermic males. Lipids 34, 793–799.
Fatty acid analysis of blood serum, seminal plasma, and spermatozoa of normozoospermic vs. asthenozoospermic males.CrossRef | 1:CAS:528:DyaK1MXmtFKisL8%3D&md5=790be43c21c2b7a59627e6d8831501b2CAS | 10529089PubMed |

Gulaya, N. M., Margitich, V. M., Govseeva, N. M., Klimashevsky, V. M., Gorpynchenko, I. I., and Boyko, M. I. (2001). Phospholipid composition of human sperm and seminal plasma in relation to sperm fertility. Arch. Androl. 46, 169–175.
Phospholipid composition of human sperm and seminal plasma in relation to sperm fertility.CrossRef | 1:CAS:528:DC%2BD3MXjslKksLc%3D&md5=17faaeefd17459aec0d705ab57f13a1fCAS | 11339641PubMed |

Hossain, S., Tareq, K. M. A., Hammano, K., and Tsujii, H. (2007). Effect of fatty acids on boar sperm motility, viability and acrosome reaction. Reprod. Med. Biol. 6, 235–239.
Effect of fatty acids on boar sperm motility, viability and acrosome reaction.CrossRef |

Kang, J. X., and Wang, J. (2005). A simplified method for analysis of polyunsaturated fatty acids. BMC Biochem. 6, 5.
A simplified method for analysis of polyunsaturated fatty acids.CrossRef | 15790399PubMed |

Lenzi, A., Picardo, M., Gandini, L., and Dondero, F. (1996). Lipids of the sperm plasma membrane: from polyunsaturated fatty acids considered as markers of sperm function to possible scavenger therapy. Hum. Reprod. Update 2, 246–256.
Lipids of the sperm plasma membrane: from polyunsaturated fatty acids considered as markers of sperm function to possible scavenger therapy.CrossRef | 1:CAS:528:DyaK1cXotVGgtLw%3D&md5=da894eb10bf61e089364003f7a87d5dbCAS | 9079417PubMed |

Mazza, M., Pomponi, M., Janiri, L., Bria, P., and Mazza, S. (2007). Omega-3 fatty acids and antioxidants in neurological and psychiatric diseases: an overview. Prog. Neuropsychopharmacol. Biol. Psychiatry 31, 12–26.
Omega-3 fatty acids and antioxidants in neurological and psychiatric diseases: an overview.CrossRef | 1:CAS:528:DC%2BD2sXht1agug%3D%3D&md5=da6b7e17617b1b3704196af2c8098dbdCAS | 16938373PubMed |

Mostafa, T., Anis, T., El Nashar, A., Imam, H., and Osman, I. (2012). Seminal plasma reactive oxygen species–antioxidants relationship with varicocele grade. Andrologia 44, 66–69.
Seminal plasma reactive oxygen species–antioxidants relationship with varicocele grade.CrossRef | 1:CAS:528:DC%2BC38XhtVKlu7k%3D&md5=2b4366fc2618f7864138a5b74ab37cb4CAS | 21651600PubMed |

Nagler, H. M., Luntz, R. K., and Martinis, F. G. (1997). Varicocele. In ‘Infertility in the Male’. (Eds L. I. Lipshultz and S. S. Howards.) pp. 336–359. (Mosby Year Book: St. Louis, MO.)

Safarinejad, M. R., and Safarinejad, S. (2012). The roles of omega-3 and omega-6 fatty acids in idiopathic male infertility. Asian J. Androl. 14, 514–515.
The roles of omega-3 and omega-6 fatty acids in idiopathic male infertility.CrossRef | 22659579PubMed |

Safarinejad, M. R., Hosseini, S. Y., Dadkhah, F., and Asgari, M. A. (2010). Relationship of omega-3 and omega-6 fatty acids with semen characteristics, and anti-oxidant status of seminal plasma: a comparison between fertile and infertile men. Clin. Nutr. 29, 100–105.
Relationship of omega-3 and omega-6 fatty acids with semen characteristics, and anti-oxidant status of seminal plasma: a comparison between fertile and infertile men.CrossRef | 1:CAS:528:DC%2BC3cXhs1antLc%3D&md5=20fc027c5dc56ae20a8d49ebffdd143dCAS | 19666200PubMed |

Saleh, R. A., Agarwal, A., Sharma, R. K., Said, T. M., Sikka, S. C., and Thomas, A. J. (2003). Evaluation of nuclear DNA damage in spermatozoa from infertile men with varicocele. Fertil. Steril. 80, 1431–1436.
Evaluation of nuclear DNA damage in spermatozoa from infertile men with varicocele.CrossRef | 14667879PubMed |

Sinclair, S. (2000). Male infertility: nutritional and environmental considerations. Altern. Med. Rev. 5, 28–38.
| 1:STN:280:DC%2BD3c7mtFSgsQ%3D%3D&md5=99f3fcc802a3d3c8d45cad9d5afdb12cCAS | 10696117PubMed |

Smith, R., Kaune, H., Parodi, D., Madariaga, M., Rios, R., Morales, I., and Castro, A. (2006). Increased sperm DNA damage in patients with varicocele: relationship with seminal oxidative stress. Hum. Reprod. 21, 986–993.
Increased sperm DNA damage in patients with varicocele: relationship with seminal oxidative stress.CrossRef | 1:CAS:528:DC%2BD28XivVOnsbs%3D&md5=fd537f1e39e389a154da8d974ce57116CAS | 16361286PubMed |

Tavilani, H., Doosti, M., Abdi, K., Vaisiraygani, A., and Joshaghani, H. R. (2006). Decreased polyunsaturated and increased saturated fatty acid concentration in spermatozoa from asthenozoospermic males as compared with normozoospermic males. Andrologia 38, 173–178.
Decreased polyunsaturated and increased saturated fatty acid concentration in spermatozoa from asthenozoospermic males as compared with normozoospermic males.CrossRef | 1:CAS:528:DC%2BD28XhtlSltbbK&md5=796b20ed44feab63929c03cf5a4fe49fCAS | 16961570PubMed |

Valavanidis, A., Vlachogianni, T., and Fiotakis, C. (2009). 8-Hydroxy-2-deoxyguanosine (8-OHdG): a critical biomarker of oxidative stress and carcinogenesis. J. Environ. Sci. Health C. Environ. Carcinog. Ecotoxicol. Rev. 27, 120–139.
8-Hydroxy-2-deoxyguanosine (8-OHdG): a critical biomarker of oxidative stress and carcinogenesis.CrossRef | 1:CAS:528:DC%2BD1MXlsVeqtrc%3D&md5=87e1dd080a9c439ad7eef23583a1ab32CAS | 19412858PubMed |

World Health Organization (WHO) (2000). ‘Manual for the Standardized Investigation and Diagnosis and Management of the Infertile Male.’ (Cambridge University Press: Cambridge, UK.)

World Health Organization (WHO) (2010a). ‘WHO Laboratory Manual for the Examination of Human Semen and Sperm–Cervical Mucus Interaction.’ (Cambridge University Press: Cambridge, UK.)

World Health Organization (WHO) (2010b). ‘WHO Laboratory Manual for the Examination and Processing of Human Semen.’ 5th ed. (World Health Organization: Geneva.)

Zalata, A. A., Christophe, A. B., Depuydt, C. H. E., Schoonjans, F., and Comhaire, F. H. (1998). The fatty acid composition of phospholipids of spermatozoa from infertile patients. Mol. Hum. Reprod. 4, 111–118.
The fatty acid composition of phospholipids of spermatozoa from infertile patients.CrossRef | 1:CAS:528:DyaK1cXitlamurY%3D&md5=f14ac13dc89df371fe8b45315dc4a1f8CAS | 9542967PubMed |



Rent Article (via Deepdyve) Export Citation Cited By (1)

View Altmetrics