Consistent age-dependent declines in human semen quality: A systematic review and meta-analysis

Ageing Research Reviews

Volumn 19, Issue , 2015, Pages 22-33

  Johnson, Sheri L ^a   Dunleavy, Jessica ^a   Gemmell, Neil J ^a   Nakagawa, Shinichi ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Fertility; Male aging; Meta regression; Paternal age; Quantitative synthesis; Sperm performance

Indexed keywords

AGING; DNA FRAGMENTATION; EJACULATION; GROUPS BY AGE; HUMAN; META ANALYSIS; MORPHOLOGY; PATERNAL AGE; PREGNANCY OUTCOME; PROGENY; PUBLISHING; REGRESSION ANALYSIS; REVIEW; SEMEN ANALYSIS; SENSITIVITY ANALYSIS; SPERM QUALITY; SPERMATOZOON COUNT; SPERMATOZOON DENSITY; SPERMATOZOON MOTILITY; SYSTEMATIC REVIEW; ADOLESCENT; ADULT; AGE; AGED; MALE; MIDDLE AGED; PHYSIOLOGY; SPERM; SPERMATOZOON; VERY ELDERLY; YOUNG ADULT;

ADOLESCENT; ADULT; AGE FACTORS; AGED; AGED, 80 AND OVER; AGING; HUMANS; MALE; MIDDLE AGED; SEMEN; SEMEN ANALYSIS; SPERM COUNT; SPERMATOZOA; YOUNG ADULT;

EID: 84912095085     PISSN: 15681637     EISSN: 18729649     Source Type: Journal    
DOI: 10.1016/j.arr.2014.10.007     Document Type: Review

References (177)

1. *Aboulghar M., Mansour R., Al-Inany H., Abou-Setta A.M., Aboulghar M., Mourad L., Serour G. Paternal age and outcome of intracytoplasmic sperm injection. Reprod. Biomed. Online 2007, 14:588-592.
2. Agarwal A., Makker K., Sharma R. Clinical relevance of oxidative stress in male factor infertility: an update. Am. J. Reprod. Immunol. 2008, 59:2-11.
3. Aitken R.J. The role of free oxygen radicals and sperm function. Int. J. Androl. 1989, 12:95-97.
4. Aitken R.J. Age, the environment and our reproductive future: bonking baby boomers and the future of sex. Reproduction 2014, 147:S1-S11.
5. Aitken R.J., De Iuliis G.N. On the possible origins of DNA damage in human spermatozoa. Mol. Hum. Reprod. 2010, 16:3-13.
6. Aitken R.J., De Iuliis G.N., Finnie J.M., Hedges A., McLachlan R.I. Analysis of the relationships between oxidative stress. DNA damage and sperm vitality in a patient population: development of diagnostic criteria. Hum. Reprod. 2010, 25:2415-2426.
7. Aitken R.J., De Iuliis G.N., McLachlan R.I. Biological and clinical significance of DNA damage in the male germ line. Int. J. Androl. 2009, 32:46-56.
8. Aitken R.J., Koopman P., Lewis S.E.M. Seeds of concern. Nature 2004, 432:48-52.
9. *Alam W., Khan M.S., Akhtar J., Bibi R., Shabbir A., Naeem M., Qazi B.M. Trend of fertility potentials with increasing age in Pakistani males. J. Postgrad. Med. Instit. 2011, 25:9-13.
10. *Aleisa N.A.S. Semen characteristics of fertile and subfertile men in a fertility clinic and correlation with age. J. King Saud Univ. Sci. 2013, 25:63-71.
11. *Alshahrani S., Sharma R., Gupta S., Durairajanayagam D., Sabanegh E., Agarwal A. The effect of advancing paternal age on semen parameters and seminal oxidative stress markers in infertile men. Fertil. Steril. 2013, 1:S440-S441.
12. Archer N.P., Langlois P.H., Suarez L., Brender J., Shanmugam R. Association of paternal age with prevalence of selected birth defects. Birt. Defects Res. A: Clin. Mol. Teratol. 2007, 79:27-34.
13. Armstrong J.S., Rajasekaran M., Chamulitrat W., Gatti P., Hellstrom W.J., Sikka S.C. Characterization of reactive oxygen species induced effects on human spermatozoa movement and energy metabolism. Free Radic. Biol. Med. 1999, 26:869-880.
14. *Auger J., Kunstmann J.M., Czyglik F., Jouannet P. Decline in semen quality among fertile men in Paris during the past 20 years. N. Engl. J. Med. 1995, 332:281-285.
15. Belloc S., Cohen-Bacrie P., Benkhalifa M., Cohen-Bacrie M., De Mouzon J., Hazout A., Menezo Y. Effect of maternal and paternal age on pregnancy and miscarriage rates after intrauterine insemination. Reprod. Biomed. Online 2008, 17:392-397.
16. *Bellver J., Garrido N., Remohi J., Pellicer A., Meseguer M. Influence of paternal age on assisted reproduction outcome. Reprod. Biomed. Online 2008, 17:595-604.
17. Bonde J.P. Male reproductive organs are at risk from environmental hazards. Asian J. Androl. 2010, 12:152-156.
18. Borenstein M., Hedges L.V., Higgins J.P.I., Rothstein H.R. Introduction to Meta-analysis 2009, Wiley, Chichester.
19. *Brahem S., Mehdi M., Elghezal H., Saad A. The effects of male aging on semen quality, sperm DNA fragmentation and chromosomal abnormalities in an infertile population. J. Assist. Reprod. Genet. 2011, 28:425-432.
20. *Bujan L., Mansat A., Pontonnier F., Mieusset R. Time series analysis of sperm concentration in fertile men in Toulouse, France between 1977 and 1992. Br. Med. J. 1996, 312:471-472.
21. *Bujan L., Mieusset R., Mondinat C., Mansat A., Pontonnier F. Sperm morphology in fertile men and its age related variation. Andrologia 1988, 20:121-128.
22. Buuren S., Groothuis-Oudshoorn K. MICE: multivariate imputation by chained equations in R. J. Stat. Softw. 2011, 45:1-67.
23. *Cardona Maya W., Berdugo J., Cadavid Jaramillo N. The effects of male age on semen parameters: analysis of 1364 men attending an andrology center. Aging Male 2009, 12:100-103.
24. Carlsen E., Giwercman A., Keiding N., Skakkebæk N.E. Evidence for decreasing quality of semen during past 50 years. Br. Med. J. 1992, 305:609-613.
25. *Carlsen E., Swan S.H., Petersen J.H., Skakkebaek N.E. Longitudinal changes in semen parameters in young Danish men from the Copenhagen area. Hum. Reprod. 2005, 20:942-949.
26. *Centola G.M., Eberly S. Seasonal variations and age-related changes in human sperm count, motility, motion parameters, morphology, and white blood cell concentration. Fertil. Steril. 1999, 72:803-808.
27. *Chen Z.Y., Toth T., Godfrey-Bailey L., Mercedat N., Schiff I., Hauser R. Seasonal variation and age-related changes in human semen parameters. J. Androl. 2003, 24:226-231.
28. Choi J.-Y., Lee K.-M., Park S.K., Noh D.-Y., Ahn S.-H., Yoo K.-Y., Kang D. Association of paternal age at birth and the risk of breast cancer in offspring: a case control study. BMC Cancer 2005, 5:143.
29. *Cocuzza M., Athayde K.S., Agarwal A., Sharma R., Pagani R., Lucon A.M., Srougi M., Hallak J. Age-related increase of reactive oxygen species in neat semen in healthy fertile men. Urology 2008, 71:490-494.
30. Cohen J. Statistical Power Analysis for the Behavioral Sciences 1988, L. Erlbaum Associates, Hillsdale, New Jersey.
31. *Cohen-Bacrie P., Belloc S., Menezo Y.J.R., Clement P., Hamidi J., Benkhalifa M. Correlation between DNA damage and sperm parameters: a prospective study of 1,633 patients. Fertil. Steril. 2009, 91:1801-1805.
32. *Colin A., Barroso G., Gomez-Lopez N., Duran E.H., Oehninger S. The effect of age on the expression of apoptosis biomarkers in human spermatozoa. Fertil. Steril. 2010, 94:2609-2614.
33. Cooper T.G., Handelsman D.J. Falling sperm counts and global oestrogenic pollution: postscript. Asian J. Androl. 2013, 15:208.
34. Cooper T.G., Noonan E., Von Eckardstein S., Auger J., Baker H.G., Behre H.M., Haugen T.B., Kruger T., Wang C., Mbizvo M.T. World Health Organization reference values for human semen characteristics. Hum. Reprod. Update 2010, 16:231-245.
35. Crow J.F. The origins, patterns and implications of human spontaneous mutation. Nat. Rev. Genet. 2000, 1:40-47.
36. *Das M., Al-Hathal N., San-Gabriel M., Phillips S., Kadoch I.J., Bissonnette F., Holzer H., Zini A. High prevalence of isolated sperm DNA damage in infertile men with advanced paternal age. J. Assist. Reprod. Genet. 2013, 30:843-848.
37. De Jonge C., LaFromboise M., Bosmans E., Ombelet W., Cox A., Nijs M. Influence of the abstinence period on human sperm quality. Fertil. Steril. 2004, 82:57-65.
38. de La Rochebrochard E., de Mouzon J., Thépot F., Thonneau P. Fathers over 40 and increased failure to conceive: the lessons of in vitro fertilization in France. Fertil. Steril. 2006, 85:1420-1424.
39. de La Rochebrochard E., Thonneau P. Paternal age and maternal age are risk factors for miscarriage results of a multicentre European study. Hum. Reprod. 2002, 17:1649-1656.
40. De Meyer T., Rietzschel E.R., De Buyzere M.L., De Bacquer D., Van Criekinge W., De Backer G.G., Gillebert T.C., Van Oostveldt P., Bekaert S. Paternal age at birth is an important determinant of offspring telomere length. Hum. Mol. Genet. 2007, 16:3097-3102.
41. *Diao R., Fok K.L., Zhao L., Chen H., Tang H., Chen J., Zheng A., Zhang X., Gui Y., Chan H.C., Cai Z. Decreased expression of cystic fibrosis transmembrane conductance regulator impairs sperm quality in aged men. Reproduction 2013, 146:637-645.
42. *Duarte Filho O.B., Tso L.O., Oliveira B.S., Busso C.E., Antunes Junior N., Glina S. Relationship between the male age and the results of intrauterine insemination cycles in couples with goodreproductive prognosis. Fertil. Steril. 2013, (1):S449.
43. Egger M., Smith G.D., Schneider M., Minder C. Bias in meta-analysis detected by a simple, graphical test. Br. Med. J. 1997, 315:629-634.
44. Eisenberg D.T., Hayes M.G., Kuzawa C.W. Delayed paternal age of reproduction in humans is associated with longer telomeres across two generations of descendants. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:10251-10256.
45. *Elzanaty S. Association between age and epididymal and accessory sex gland function and their relation to sperm motility. Arch. Androl. 2007, 53:149-156.
46. *Eskenazi B., Wyrobek A.J., Sloter E., Kidd S.A., Moore L., Young S., Moore D. The association of age and semen quality in healthy men. Hum. Reprod. 2003, 18:447-454.
47. Evenson D., Jost L., Marshall D., Zinaman M., Clegg E., Purvis K., De Angelis P., Claussen O. Utility of the sperm chromatin structure assay as a diagnostic and prognostic tool in the human fertility clinic. Hum. Reprod. 1999, 14:1039-1049.
48. *Ferreira R.C., Braga D., Bonetti T.C.D., Pasqualotto F.F., Iaconelli A., Borges E. Negative influence of paternal age on clinical intracytoplasmic sperm injection cycle outcomes in oligozoospermic patients. Fertil. Steril. 2010, 93:1870-1874.
49. Fisch H., Braun S.R. Trends in global semen parameter values. Asian J. Androl. 2013, 15:169-173.
50. Fisch H., Hyun G., Golden R., Hensle T.W., Olsson C.A., Liberson G.L. The influence of paternal age on Down syndrome. J. Urol. 2003, 169:2275-2278.
51. Ford W., North K., Taylor H., Farrow A., Hull M., Golding J. Increasing paternal age is associated with delayed conception in a large population of fertile couples: evidence for declining fecundity in older men. Hum. Reprod. 2000, 15:1703-1708.
52. *Frattarelli J.L., Miller K.A., Miller B.T., Elkind-Hirsch K., Scott R.T. Male age negatively impacts embryo development and reproductive outcome in donor oocyte assisted reproductive technology cycles. Fertil. Steril. 2008, 90:97-103.
53. *Freour T., Jean M., Mirallie S., Barriere P. Computer-assisted sperm analysis parameters in young fertile sperm donors and relationship with age. Syst. Biol. Reprod. Med. 2012, 58:102-106.
54. *Gallardo E., Simon C., Levy M., Guanes P.P., Remohi J., Pellicer A. Effect of age on sperm fertility potential: oocyte donation as a model. Fertil. Steril. 1996, 66:260-264.
55. *Gao J., Gao E.S., Yang Q., Walker M., Wu J.Q., Zhou W.J., Wen S.W. Semen quality in a residential, geographic and age representative sample of healthy Chinese men. Hum. Reprod. 2007, 22:477-484.
56. *Girsh E., Katz N., Genkin L., Girtler O., Bocker J., Bezdin S., Barr I. Male age influences oocyte-donor program results. J. Assist. Reprod. Genet. 2008, 25:137-143.
57. *Gregoire A.T., Moran M.J., Quintero R., O'Connell K. The pregnancy rate, duration of infertility, months of treatment, and semen characteristics expressed in age-specific groups of couples attending a fertility service. Fertil. Steril. 1972, 23:894-897.
58. *Grunewald S., Glander H.J., Paasch U., Kratzsch J. Age-dependent inhibin B concentration in relation to FSH and semen sample qualities: a study in 2448 men. Reproduction 2013, 145:237-244.
59. Guryev V., Koudijs M.J., Berezikov E., Johnson S.L., Plasterk R.H.A., van Eeden F.J.M., Cuppen E. Genetic variation in the zebrafish. Genome Res. 2006, 16:491-497.
60. *Haidl G., Jung A., Schill W.B. Ageing and sperm function. Hum. Reprod. 1996, 11:558-560.
61. *Hammiche F., Laven J.S., Boxmeer J.C., Dohle G.R., Steegers E.A., Steegers-Theunissen R.P. Sperm quality decline among men below 60 years of age undergoing IVF or ICSI treatment. J. Androl. 2011, 32:70-76.
62. Harlap S., Paltiel O., Deutsch L., Knaanie A., Masalha S., Tiram E., Caplan L.S., Malaspina D., Friedlander Y. Paternal age and preeclampsia. Epidemiology 2002, 13:660-667.
63. Harrell F.E. Regression Modeling Strategies: With Applications to Linear Models, Logistic Regression, and Survival Analysis 2001, Springer-Verlag, New York.
64. Hassan M.A.M., Killick S.R. Effect of male age on fertility: evidence for the decline in male fertility with increasing age. Fertil. Steril. 2003, 79:1520-1527.
65. Hector K.L., Nakagawa S. Quantitative analysis of compensatory and catch-up growth in diverse taxa. J. Anim. Ecol. 2012, 81:583-593.
66. Hedges L.V., Pigott T.D. The power of statistical tests in meta-analysis. Psychol. Methods 2001, 6:203-217.
67. *Hellstrom W.J.G., Overstreet J.W., Sikka S.C., Denne J., Ahuja S., Hoover A.M., Sides G.D., Cordell W.H., Harrison L.M., Whitaker J.S. Semen and sperm reference ranges for men 45 years of age and older. J. Androl. 2006, 27:421-428.
68. *Henkel R., Bittner J., Weber R., Hüther F., Miska W. Relevance of zinc in human sperm flagella and its relation to motility. Fertil. Steril. 1999, 71:1138-1143.
69. *Henkel R., Maass G., Schuppe H.C., Jung A., Schubert J., Schill W.B. Molecular aspects of declining sperm motility in older men. Fertil. Steril. 2005, 84:1430-1437.
70. Higgins J.P., Thompson S.G., Deeks J.J., Altman D.G. Measuring inconsistency in meta-analyses. Br. Med. J. 2003, 327:557.
71. *Hossain M.M., Fatima P., Rahman D., Hossain H.B. Semen parameters at different age groups of male partners of infertile couples. Mymensingh Med. J. 2012, 21:306-315.
72. Hultman C., Sandin S., Levine S., Lichtenstein P., Reichenberg A. Advancing paternal age and risk of autism: new evidence from a population-based study and a meta-analysis of epidemiological studies. Mol. Psychiatry 2010, 16:1203-1212.
73. Humm K.C., Sakkas D. Role of increased male age in IVF and egg donation: is sperm DNA fragmentation responsible?. Fertil. Steril. 2013, 99:30-36.
74. *Irvine S., Cawood E., Richardson D., MacDonald E., Aitken J. Evidence of deteriorating semen quality in the United Kingdom: Birth Cohort Study in 577 men in Scotland over 11 years. Br. Med. J. 1996, 312:467-471.
75. *Itoh N., Kayama F., Tatsuki T.J., Tsukamoto T. Have sperm counts deteriorated over the past 20 years in healthy, young Japanese men? Results from the Sapporo area. J. Androl. 2001, 22:40-44.
76. Johnson S.L., Gemmell N.J. Are old males still good males and can females tell the difference?. Bioessays 2012, 34:609-619.
77. *Jung A., Schuppe H.C., Schill W.B. Comparison of semen quality in older and younger men attending an andrology clinic. Andrologia 2002, 34:116-122.
78. Kidd S.A., Eskenazi B., Wyrobek A.J. Effects of male age on semen quality and fertility: a review of the literature. Fertil. Steril. 2001, 75:237-248.
79. Klonoff-Cohen H., Lam-Kruglick P., Gonzalez C. Effects of maternal and paternal alcohol consumption on the success rates of in vitro fertilization and gamete intrafallopian transfer. Fertil. Steril. 2003, 79:330-339.
80. Klonoff-Cohen H.S., Natarajan L. The effect of advancing paternal age on pregnancy and live birth rates in couples undergoing in vitro fertilization or gamete intrafallopian transfer. Am. J. Obstet. Gynecol. 2004, 191:507-514.
81. Kong A., Frigge M.L., Masson G., Besenbacher S., Sulem P., Magnusson G., Gudjonsson S.A., Sigurdsson A., Jonasdottir A., Jonasdottir A. Rate of de novo mutations and the importance of father's age to disease risk. Nature 2012, 488:471-475.
82. Koppers A.J., De Iuliis G.N., Finnie J.M., McLaughlin E.A., Aitken R.J. Significance of mitochondrial reactive oxygen species in the generation of oxidative stress in spermatozoa. J. Clin. Endocrinol. Metab. 2008, 93:3199-3207.
83. Kühnert B., Nieschlag E. Reproductive functions of the ageing male. Hum. Reprod. Update 2004, 10:327-339.
84. *Kumtepe Y., Yakin K., Kahraman S., Sertyel S., Vanlioglu F., Cengiz S., Donmez E. Male age is not an independent factor to affect the outcome of assisted reproductive techniques. Int. J. Androl. 2003, 26:161-165.
85. *Lackner J., Schatzl G., Waldhor T., Resch K., Kratzik C., Marberger M. Constant decline in sperm concentration in infertile males in an urban population: experience over 18 years. Fertil. Steril. 2005, 84:1657-1661.
86. *Lemcke B., Behre H.M., Nieschlag E. Frequently subnormal semen profiles of normal volunteers recruited over 17 years. Int. J. Androl. 1997, 20:144-152.
87. *Levitas E., Lunenfeld E., Weisz N., Friger M., Potashnik G. Relationship between age and semen parameters in men with normal sperm concentration: analysis of 6022 semen samples. Andrologia 2007, 39:45-50.
88. Li Y., Lin H., Li Y., Cao J. Association between socio-psycho-behavioral factors and male semen quality: systematic review and meta-analyses. Fertil. Steril. 2011, 95:116-123.
89. *Li Y.F., Lin H., Ma M.F., Li L.B., Cai M., Zhou N.Y., Han X., Bao H.Q., Huang L.P., Zhu C.Z., Li C.H., Yang H., Rao Z.L., Xiang Y., Cui Z.H., Ao L., Zhou Z.Y., Xiong H.Y., Cao J. Semen quality of 1346 healthy men, results from the Chongqing area of southwest China. Hum. Reprod. 2009, 24:459-469.
90. Lipsey M.W., Wilson D.B. Practical Meta Analysis. Applied Social Research Methods Series 2001, vol. 49. Sage, Thousand Oaks, CA.
91. *Luna M., Finkler E., Barritt J., Bar-Chama N., Sandler B., Copperman A.B., Grunfeld L. Paternal age and assisted reproductive technology outcome in ovum recipients. Fertil. Steril. 2009, 92:1772-1775.
92. Maheshwari A., Hamilton M., Bhattacharya S. Effect of female age on the diagnostic categories of infertility. Hum. Reprod. 2008, 23:538-542.
93. *Marimuthu P., Kapilashrami M.C., Misro M.M., Singh G. Evaluation of trend in semen analysis for 11 years in subjects attending a fertility clinic in India. Asian J. Androl. 2003, 5:221-225.
94. Mathieu C., Ecochard R., Bied V., Lornage J., Czyba J.C. Cumulative conception rate following intrauterine artificial insemination with husbands spermatozoa - influence of husbands age. Hum. Reprod. 1995, 10:1090-1097.
95. May-Panloup P., Chretien M.F., Savagner F., Vasseur C., Jean M., Malthiery Y., Reynier P. Increased sperm mitochondrial DNA content in male infertility. Hum. Reprod. 2003, 18:550-556.
96. *Mladenovic I., Micic S., Papic N., Genbacev O., Marinkovlc B. Sperm morphology and motility in different age populations. Syst. Biol. Reprod. Med. 1994, 32:197-205.
97. Moher D., Liberati A., Tetzlaff J., Altman D.G. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann. Intern. Med. 2009, 151:264-269.
98. *Molina R.I., Martini A.C., Tissera A., Olmedo J., Senestrari D., De Cuneo M.F., Ruiz R.D. Semen quality and aging: analysis of 9.168 samples in Cordoba, Argentina. Arch. Esp. Urol. 2010, 63:214-222.
99. Moreno S.G., Sutton A.J., Ades A., Stanley T.D., Abrams K.R., Peters J.L., Cooper N.J. Assessment of regression-based methods to adjust for publication bias through a comprehensive simulation study. BMC Med. Res. Methodol. 2009, 9:2.
100. Moreno-Loshuertos R., Acin-Perez R., Fernandez-Silva P., Movilla N., Perez-Martos A., de Cordoba S.R., Gallardo M.E., Enriquez J.A. Differences in reactive oxygen species production explain the phenotypes associated with common mouse mitochondrial DNA variants. Nat. Genet. 2006, 38:1261-1268.
101. *Moskovtsev S.I., Mullen J.B., Lecker I., Jarvi K., White J., Roberts M., Lo K.C. Frequency and severity of sperm DNA damage in patients with confirmed cases of male infertility of different aetiologies. Reprod. Biomed. Online 2010, 20:759-763.
102. *Moskovtsev S.I., Willis J., Mullen J.B.M. Age-related decline in sperm deoxyribonucleic acid integrity in patients evaluated for male infertility. Fertil. Steril. 2006, 85:496-499.
103. *Moskovtsev S.I., Willis J., White J., Mullen J.B. Sperm DNA damage: correlation to severity of semen abnormalities. Urology 2009, 74:789-793.
104. *Moskovtsev S.I., Willis J., White J., Mullen J.B.M. Sperm survival relationship to age-related sperm DNA integrity in infertile men. Arch. Androl. 2007, 53:29-32.
105. *Mukhopadhyay D., Varghese A.C., Pal M., Banerjee S.K., Bhattacharyya A.K., Sharma R.K., Agarwal A. Semen quality and age-specific changes: a study between two decades on 3,729 male partners of couples with normal sperm count and attending an andrology laboratory for infertility-related problems in an Indian city. Fertil. Steril. 2010, 93:2247-2254.
106. Murtaugh P.A. Journal quality, effect size, and publication bias in meta-analysis. Ecology 2002, 83:1162-1166.
107. Nakagawa S., Cuthill I.C. Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol. Rev. 2007, 82:591-605.
108. Nakagawa S., Santos E.S. Methodological issues and advances in biological meta-analysis. Evol. Ecol. 2012, 26:1253-1274.
109. *Ng K.K., Donat R., Chan L., Lalak A., Di Pierro I., Handelsman D.J. Sperm output of older men. Hum. Reprod. 2004, 19:1811-1815.
110. *Nicopoullos J.D.M., Gilling-Smith C., Almeida P.A., Homa S., Norman-Taylor J.Q., Ramsay J.W.A. Sperm DNA fragmentation in subfertile men: the effect on the outcome of intracytoplasmic sperm injection and correlation with sperm variables. BJU Int. 2008, 101:1553-1560.
111. *Nijs M., De Jonge C., Cox A., Janssen M., Bosmans E., Ombelet W. Correlation between male age, WHO sperm parameters. DNA fragmentation, chromatin packaging and outcome in assisted reproduction technology. Andrologia 2011, 43:174-179.
112. Nybo Andersen A.-M., Hansen K.D., Andersen P.K., Smith G.D. Advanced paternal age and risk of fetal death: a cohort study. Am. J. Epidemiol. 2004, 160:1214-1222.
113. *Paasch U., Grunewald S., Kratzsch J., Glander H.J. Obesity and age affect male fertility potential. Fertil. Steril. 2010, 94:2898-2901.
114. Pacey A.A. Are sperm counts declining? Or did we just change our spectacles?. Asian J. Androl. 2013, 15:187-190.
115. *Pasqualotto F.F., Sobreiro B.P., Hallak J., Pasqualotto E.B., Lucon A.M. Sperm concentration and normal sperm morphology decrease and follicle-stimulating hormone level increases with age. BJU Int. 2005, 96:1087-1091.
116. *Paulson R.J., Milligan R.C., Sokol R.Z. The lack of influence of age on male fertility. Am. J. Obstet. Gynecol. 2001, 184:818-824.
117. Pellestor F., Girardet A., Andreo B. Effect of long abstinence periods on human sperm quality. Int. J. Fertil. Menopausal Stud. 1994, 39:278-282.
118. Pinheiro J.C., Bates D.M. Mixed Effects Models in S and S-PLUS 2000, Springer-Verlag.
119. Plas E., Berger P., Hermann M., Pflüger H. Effects of aging on male fertility?. Exp. Gerontol. 2000, 35:543-551.
120. *Plastira K., Msaouel P., Angelopoulou R., Zanioti K., Plastiras A., Pothos A., Bolaris S., Paparisteidis N., Mantas D. The effects of age on DNA fragmentation, chromatin packaging and conventional semen parameters in spermatozoa of oligoasthenoteratozoospermic patients. J. Assist. Reprod. Genet. 2007, 24:437-443.
121. Povey A., Clyma J.-A., McNamee R., Moore H., Baillie H., Pacey A., Cherry N. Modifiable and non-modifiable risk factors for poor semen quality: a case-referent study. Hum. Reprod. 2012, 27:2799-2806.
122. *Rehan N. Semen characteristics of fertile Pakistani men. J. Pak. Med. Assoc. 1994, 44:62-64.
123. *Rehan N., Sobrero A.J., Fertig J.W. The semen of fertile men: statistical analysis of 1300 men. Fertil. Steril. 1975, 26:492-502.
124. Reinhardt K. Evolutionary consequences of sperm cell aging. Q. Rev. Biol. 2007, 82:375-393.
125. Rochebrochard E., Thonneau d.L.P. Paternal age≥ 40 years: an important risk factor for infertility. Am. J. Obstet. Gynecol. 2003, 189:901-905.
126. *Rolf C., Behre H.M., Nieschlag E. Reproductive parameters of older compared to younger men of infertile couples. Int. J. Androl. 1996, 19:135-142.
127. Ruiz-Pesini E., Lapeòa A.-C., Dìez-sánchez C., Pèrez-Martos A., Montoya J., Alvarez E., Dìaz M., Urriès A., Montoro L., LÛpez-Pèrez M.J., Enrìquez J.A. Human mtDNA haplogroups associated with high or reduced spermatozoa motility. Am. J. Hum. Genet. 2000, 67:682-696.
128. *Rybar R., Kopecka V., Prinosilova P., Markova P., Rubes J. Male obesity and age in relationship to semen parameters and sperm chromatin integrity. Andrologia 2011, 43:286-291.
129. Saidi J.A., Chang D.T., Goluboff E.T., Bagiella E., Olsen G., Fisch H. Declining sperm counts in the United States? A critical review. J. Urol. 1999, 161:460-462.
130. Sakkas D., Alvarez J.G. Sperm DNA fragmentation: mechanisms of origin, impact on reproductive outcome, and analysis. Fertil. Steril. 2010, 93:1027-1036.
131. Sartorius G.A., Nieschlag E. Paternal age and reproduction. Hum. Reprod. Update 2010, 16:65-79.
132. Schielzeth H. Simple means to improve the interpretability of regression coefficients. Method Ecol. Evol. 2010, 1:103-113.
133. *Schmid T.E., Eskenazi B., Baumgartner A., Marchetti F., Young S., Weldon R., Anderson D., Wyrobek A.J. The effects of male age on sperm DNA damage in healthy non-smokers. Hum. Reprod. 2007, 22:180-187.
134. *Schwartz D., Mayaux M.J., Spira A. Semen characteristics as a function of age in 833 fertile men. Fertil. Steril. 1983, 39:530-535.
135. *Schwartz D., Mayaux M.J., Spira A., Moscato M.L., Jouannet P., Czyglik F., David G. Study of a group of 484 fertile men. Part II: relation between age (20-59) and semen characteristics. Int. J. Androl. 1981, 4:450-465.
136. Sergerie M., Laforest G., Bujan L., Bissonnette F., Bleau G. Sperm DNA fragmentation: threshold value in male fertility. Hum. Reprod. 2005, 20:3446-3451.
137. Sharma R.K., Sabanegh E., Mahfouz R., Gupta S., Thiyagarajan A., Agarwal A. TUNEL as a test for sperm DNA damage in the evaluation of male infertility. Urology 2010, 76:1380-1386.
138. *Siddighi S., Chan C.A., Patton W.C., Jacobson J.D., Chan P.J. Male age and sperm necrosis in assisted reproductive technologies. Urol. Int. 2007, 79:231-234.
139. *Silva L.F.I., Oliveira J.B.A., Petersen C.G., Mauri A.L., Massaro F.C., Cavagna M., Baruffi R.L.R., Franco J.G. The effects of male age on sperm analysis by motile sperm organelle morphology examination (MSOME). Reprod. Biol. Endocrinol. 2012, 10:19.
140. Simon L., Proutski I., Stevenson M., et al. Sperm DNA damage has a negative association with live bith rates after IVF. Reprod. BioMed. Online 2013, 26:68-78.
141. *Singh N.P., Muller C.H., Berger R.E. Effects of age on DNA double-strand breaks and apoptosis in human sperm. Fertil. Steril. 2003, 80:1420-1430.
142. Sipos A., Rasmussen F., Harrison G., Tynelius P., Lewis G., Leon D.A., Gunnell D. Paternal age and schizophrenia: a population based cohort study. Br. Med. J. 2004, 329:1070.
143. Siva-Jothy M.T. The young sperm gambit. Ecol. Lett. 2000, 3:172-174.
144. Slama R., Bouyer J., Windham G., Fenster L., Werwatz A., Swan S.H. Influence of paternal age on the risk of spontaneous abortion. Am. J. Epidemiol. 2005, 161:816-823.
145. Sloter E., Schmid T.E., Marchetti F., Eskenazi B., Nath J., Wyrobek A.J. Quantitative effects of male age on sperm motion. Hum. Reprod. 2006, 21:2868-2875.
146. *Smit M., Romijn J.C., Wildhagen M.F., Weber R.F., Dohle G.R. Sperm chromatin structure is associated with the quality of spermatogenesis in infertile patients. Fertil. Steril. 2010, 94:1748-1752.
147. *Sobreiro B.P., Lucon A.M., Pasqualotto F.F., Hallak J., Athayde K.S., Arap S. Semen analysis in fertile patients undergoing vasectomy: reference values and variations according to age, length of sexual abstinence, seasonality, smoking habits and caffeine intake. Sao Paulo Med. J. 2005, 123:161-166.
148. *Sobrero A.J., Naghma-Rehan E. The semen of fertile men. II. Semen characteristics of 100 fertile men. Fertil. Steril. 1975, 26:1048-1056.
149. Song G.J., Lewis V. Mitochondrial DNA integrity and copy number in sperm from infertile men. Fertil. Steril. 2008, 90:2238-2244.
150. *Spandorfer S.D., Avrech O.M., Colombero L.T., Palermo G.D., Rosenwaks Z. Effect of parental age on fertilization and pregnancy characteristics in couples treated by intracytoplasmic sperm injection. Hum. Reprod. 1998, 13:334-338.
151. Spiropoulos J., Turnbull D.M., Chinnery P.F. Can mitochondrial DNA mutations cause sperm dysfunction?. Mol. Hum. Reprod. 2002, 8:719-721.
152. *Stone B.A., Alex A., Werlin L.B., Marrs R.P. Age thresholds for changes in semen parameters in men. Fertil. Steril. 2013, 100:952-958.
153. Swan S.H., Elkin E.P., Fenster L. Have sperm densities declined? A reanalysis of global trend data. Environ. Health Perspect. 1997, 105:1228-1232.
154. Swan S.H., Elkin E.P., Fenster L. The question of declining sperm density revisited: an analysis of 101 studies published 1934-1996. Environ. Health Perspect. 2000, 108:961-966.
155. *Tandara M., Bajic A., Tandara L., Sunj M., Jurisic Z., Jukic M. Correlation between proportions of sperm with DNA fragmentation assessed by Halosperm test and values of standard quality parameters of semen and possible impact on embryo quality. Zdravniski Vestnik 2013, 82:298-307.
156. *Teijon M.L., Garcia F., Serra O., Moragas M., Rabanal A., Olivares R., Alvarez J.G. Semen quality in a population of volunteers from the province of Barcelona. Reprod. Biomed. Online 2007, 15:434-444.
157. *Telisman S., Cvitkovic P., Jurasovic J., Pizent A., Gavella M., Rocic B. Semen quality and reproductive endocrine function in relation to biomarkers of lead, cadmium, zinc, and copper in men. Environ. Health Perspect. 2000, 108:45-53.
158. Trikalinos T.A., Ioannidis J.P.A. Assessing the evolution of effect sizes over time. Publication Bias in Meta-analysis: Publication Bias in Meta-Analysis: Prevention, Assessment, and Adjustments 2006, 241-259. Wiley, Chichester. R. Hannah, A.J.S. Rothstein, Michael Borenstein (Eds.).
159. *Vagnini L., Baruffi R.L.R., Mauri A.L., Petersen C.G., Massaro F.C., Pontes A., Oliveira J.B.A., Franco J.G. The effects of male age on sperm DNA damage in an infertile population. Reprod. Biomed. Online 2007, 15:514-519.
160. *Varshini J., Srinag B.S., Kalthur G., Krishnamurthy H., Kumar P., Rao S.B.S., Adiga S.K. Poor sperm quality and advancing age are associated with increased sperm DNA damage in infertile men. Andrologia 2012, 44:642-649.
161. Viechtbauer W. Conducting meta-analyses in R with the metafor package. J. Stat. Softw. 2010, 36:1-48.
162. *Vierula M., Niemi M., Keiski A., Saaranen M., Saarikoski S., Suominen J. High and unchanged sperm counts of Finnish men. Int. J. Androl. 1996, 19:11-17.
163. *Vivas-Acevedo G., Lozano J.R., Camejo M.I. Effect of varicocele grade and age on seminal parameters. Urol. Int. 2010, 85:194-199.
164. *Wang C., Chan S.Y., Leung A., Ng R.P., Ng M., Tang L.C., Ma H.K., Tsoi W.L., Kwan M. Cross-sectional study of semen parameters in a large group of normal Chinese men. Int. J. Androl. 1985, 8:257-274.
165. *Whitcomb B.W., Turzanski-Fortner R., Richter K.S., Kipersztok S., Stillman R.J., Levy M.J., Levens E.D. Contribution of male age to outcomes in assisted reproductive technologies. Fertil. Steril. 2011, 95:147-151.
166. WHO WHO Laboratory Manual for the Examination of Human Semen and Sperm-Cervical Mucus Interaction 1999, 128. Cambridge University Press. 4th ed.
167. WHO WHO Laboratory Manual for the Examination and Processing of Human Semen 2010, World Health Organization, Geneva.
168. *Winkle T., Rosenbusch B., Gagsteiger F., Paiss T., Zoller N. The correlation between male age, sperm quality and sperm DNA fragmentation in 320 men attending a fertility center. J. Assist. Reprod. Genet. 2009, 26:41-46.
169. *Wogatzky J., Wirleitner B., Stecher A., Vanderzwalmen P., Neyer A., Spitzer D., Schuff M., Schechinger B., Zech N.H. The combination matters - distinct impact of lifestyle factors on sperm quality: a study on semen analysis of 1683 patients according to MSOME criteria. Reprod. Biol. Endocrinol. 2012, 10:115.
170. *Wyrobek A.J., Eskenazi B., Young S., Arnheim N., Tiemann-Boege I., Jabs E.W., Glaser R.L., Pearson F.S., Evenson D. Advancing age has differential effects on DNA damage, chromatin integrity, gene mutations, and aneuploidies in sperm. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:9601-9606.
171. Yang Q., Wen S., Leader A., Chen X., Lipson J., Walker M. Paternal age and birth defects: how strong is the association?. Hum. Reprod. 2007, 22:696-701.
172. Yip B.H., Pawitan Y., Czene K. Parental age and risk of childhood cancers: a population-based cohort study from Sweden. Int. J. Epidemiol. 2006, 35:1495-1503.
173. *Zavos P.M., Kaskar K., Correa J.R., Sikka S.C. Seminal characteristics and sexual behavior in men of different age groups: is there an aging effect?. Asian J. Androl. 2006, 8:337-341.
174. *Zhu Q.X., Meads C., Lu M.L., Wu J.Q., Zhou W.J., Gao E.S. Turning point of age for semen quality: a population-based study in Chinese men. Fertil. Steril. 2011, 96:572-576.
175. Zini A., Sigman M. Are tests of sperm dna damage clinically useful? Pros and cons. J. Androl. 2009, 30:219-229.
176. *Zorn B., Golob B., Ihan A., Kopitar A., Kolbezen M. Apoptotic sperm biomarkers and their correlation with conventional sperm parameters and male fertility potential. J. Assist. Reprod. Genet. 2012, 29:357-364.
177. *Zou Z.K., Hu H.X., Song M.S., Shen Y.L., Guo X.H., McElreavey K., Bittles A.H., Wang W. Semen quality analysis of military personnel from six geographical areas of the People's Republic of China. Fertil. Steril. 2011, 95:2018-2184.