Skip to main content
Top
Published in: Journal of Assisted Reproduction and Genetics 5/2011

01-05-2011 | Goanadal Physiology and Disease

The effects of male aging on semen quality, sperm DNA fragmentation and chromosomal abnormalities in an infertile population

Authors: Sonia Brahem, Meriem Mehdi, Hatem Elghezal, Ali Saad

Published in: Journal of Assisted Reproduction and Genetics | Issue 5/2011

Login to get access

Abstract

Purpose

To investigate the effects of male aging on semen quality, DNA fragmentation and chromosomal abnormalities in the spermatozoa of infertile patients and fertile men.

Methods

Semen samples of 140 infertile patients (24–76 years) and 50 men with proven fertility (25–65 years) were analyzed according to WHO guidelines. DNA fragmentation was detected by TUNEL assay, while aneuploidy was assessed by FISH.

Results

In the patient group, semen volume and vitality of spermatozoa decreased significantly with age, while sperm concentration showed a statistically significant increase with age. DNA fragmentation as well as disomy of sex chromosomes and disomy 8 did not show a statistically significant change with age. However, the diploidy rate was significantly increased with patient’s age. In the control group, conventional semen parameters as well as DNA fragmentation and chromosomal abnormalities did not show a statistically significant with age.

Conclusion

Increased age in infertile men is associated with an increase in sperm concentration and diploidy, as well as a decline in semen volume and sperm vitality. However motility, morphology and DNA fragmentation are not affected by male age.
Literature
1.
go back to reference Kidd SA, Eskenazi B, Wyrobek AJ. Effects of male age on semen quality and fertility: a review of the literature. Fertil Steril. 2001;75:237–48.PubMedCrossRef Kidd SA, Eskenazi B, Wyrobek AJ. Effects of male age on semen quality and fertility: a review of the literature. Fertil Steril. 2001;75:237–48.PubMedCrossRef
2.
go back to reference Eskenazi B, Wyrobek AJ, Sloter E, Kidd SA, Moore L, Young S, et al. The association of age and semen quality in healthy men. Hum Reprod. 2003;18:447–54.PubMedCrossRef Eskenazi B, Wyrobek AJ, Sloter E, Kidd SA, Moore L, Young S, et al. The association of age and semen quality in healthy men. Hum Reprod. 2003;18:447–54.PubMedCrossRef
3.
go back to reference Lewis SE, Aitken RJ. DNA damage to spermatozoa has impacts on fertilization and pregnancy. Cell Tissue Res. 2005;322:33–41.PubMedCrossRef Lewis SE, Aitken RJ. DNA damage to spermatozoa has impacts on fertilization and pregnancy. Cell Tissue Res. 2005;322:33–41.PubMedCrossRef
4.
go back to reference Benchaib M, Lornage J, Mazoyer C, Lejeune H, Salle B, François Guerin J. Sperm deoxyribonucleic acid fragmentation as a prognostic indicator of assisted reproductive technology outcome. Fertil Steril. 2007;87:93–100.PubMedCrossRef Benchaib M, Lornage J, Mazoyer C, Lejeune H, Salle B, François Guerin J. Sperm deoxyribonucleic acid fragmentation as a prognostic indicator of assisted reproductive technology outcome. Fertil Steril. 2007;87:93–100.PubMedCrossRef
5.
go back to reference Bungum M, Humaidan P, Axmon A, Spano M, Bungum L, Erenpreiss J, et al. Sperm DNA integrity assessment in prediction of assisted reproduction technology outcome. Hum Reprod. 2007;22:174–9.PubMedCrossRef Bungum M, Humaidan P, Axmon A, Spano M, Bungum L, Erenpreiss J, et al. Sperm DNA integrity assessment in prediction of assisted reproduction technology outcome. Hum Reprod. 2007;22:174–9.PubMedCrossRef
6.
go back to reference Vagnini L, Baruffi RL, Mauri AL, Petersen CG, Massaro FC, Pontes A, et al. The effects of male age on sperm DNA damage in an infertile population. Reprod Biomed Online. 2007;15:514–9.PubMedCrossRef Vagnini L, Baruffi RL, Mauri AL, Petersen CG, Massaro FC, Pontes A, et al. The effects of male age on sperm DNA damage in an infertile population. Reprod Biomed Online. 2007;15:514–9.PubMedCrossRef
7.
go back to reference Spano M, Kolstad AH, Larsen SB, Cordelli E, Leter G, Giwercman A, et al. The applicability of the flow cytometric sperm chromatin structure assay in epidemiological studies. Hum Reprod. 1998;13:2495–505.PubMedCrossRef Spano M, Kolstad AH, Larsen SB, Cordelli E, Leter G, Giwercman A, et al. The applicability of the flow cytometric sperm chromatin structure assay in epidemiological studies. Hum Reprod. 1998;13:2495–505.PubMedCrossRef
8.
go back to reference Wyrobek AJ, Eskenazi B, Young S, Arnheim N, Tiemann-Boege I, Jabs EW, et al. Advancing age has differential effects on DNA damage, chromatin integrity, gene mutations, and aneuploidies in sperm. Proc Natl Acad Sci USA. 2006;103:9601–6.PubMedCrossRef Wyrobek AJ, Eskenazi B, Young S, Arnheim N, Tiemann-Boege I, Jabs EW, et al. Advancing age has differential effects on DNA damage, chromatin integrity, gene mutations, and aneuploidies in sperm. Proc Natl Acad Sci USA. 2006;103:9601–6.PubMedCrossRef
9.
go back to reference Morris ID, Ilott S, Dixon L, Brison DR. The spectrum of DNA damage in human sperm assessed by single cell gel electrophoresis (Comet assay) its relationship fertilization embryo development. Hum Reprod. 2002;17:990–8.PubMedCrossRef Morris ID, Ilott S, Dixon L, Brison DR. The spectrum of DNA damage in human sperm assessed by single cell gel electrophoresis (Comet assay) its relationship fertilization embryo development. Hum Reprod. 2002;17:990–8.PubMedCrossRef
10.
go back to reference Colin A, Barroso G, Gomez-Lopez N, Duran EH, Oehninger S. The effect of age on the expression of apoptosis biomarkers in human spermatozoa. Fertil Steril 2010 (in press). Colin A, Barroso G, Gomez-Lopez N, Duran EH, Oehninger S. The effect of age on the expression of apoptosis biomarkers in human spermatozoa. Fertil Steril 2010 (in press).
11.
go back to reference Schmid TE, Eskenazi B, Baumgartner A, Marchetti F, Young S, Weldon R, et al. The effects of male age on sperm DNA damage in healthy non-smokers. Hum Reprod. 2007;22:180–7.PubMedCrossRef Schmid TE, Eskenazi B, Baumgartner A, Marchetti F, Young S, Weldon R, et al. The effects of male age on sperm DNA damage in healthy non-smokers. Hum Reprod. 2007;22:180–7.PubMedCrossRef
12.
go back to reference 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;26:41–6.PubMedCrossRef 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;26:41–6.PubMedCrossRef
13.
go back to reference Hook EB, Schreinemachers DM, Willey AM, Cross PK. Rates of mutant structural chromosome rearrangements in human foetuses: data from prenatal cytogenetic studies and associations with maternal age and parental mutagen exposure. Am J Hum Genet. 1983;35:96–109.PubMed Hook EB, Schreinemachers DM, Willey AM, Cross PK. Rates of mutant structural chromosome rearrangements in human foetuses: data from prenatal cytogenetic studies and associations with maternal age and parental mutagen exposure. Am J Hum Genet. 1983;35:96–109.PubMed
14.
go back to reference Nicolaidis P, Petersen MB. Origin and mechanisms of nondisjunction in human autosomal trisomies. Hum Reprod. 1998;13:313–9.PubMedCrossRef Nicolaidis P, Petersen MB. Origin and mechanisms of nondisjunction in human autosomal trisomies. Hum Reprod. 1998;13:313–9.PubMedCrossRef
15.
go back to reference Sloter ED, Marchetti F, Eskenazi B, Weldon RH, Nath J, Cabreros D, et al. Frequency of human sperm carrying structural aberrations of chromosome 1 increases with advancing age. Fertil Steril. 2007;87:1077–86.PubMedCrossRef Sloter ED, Marchetti F, Eskenazi B, Weldon RH, Nath J, Cabreros D, et al. Frequency of human sperm carrying structural aberrations of chromosome 1 increases with advancing age. Fertil Steril. 2007;87:1077–86.PubMedCrossRef
16.
go back to reference Luetjens CM, Rolf C, Gassner P, Werny JE, Nieschlag E. Sperm aneuploidy rates in younger and older men. Hum Reprod. 2002;17:1826–32.PubMedCrossRef Luetjens CM, Rolf C, Gassner P, Werny JE, Nieschlag E. Sperm aneuploidy rates in younger and older men. Hum Reprod. 2002;17:1826–32.PubMedCrossRef
17.
go back to reference World Health O. WHO laboratory manual for the examination of human semen and sperm-cervical mucus interaction. 4th ed. Cambridge, UK, Published on behalf of the World Health Organization by Cambridge University Press; 1999. World Health O. WHO laboratory manual for the examination of human semen and sperm-cervical mucus interaction. 4th ed. Cambridge, UK, Published on behalf of the World Health Organization by Cambridge University Press; 1999.
18.
go back to reference David G. Editorial: sperm banks in France. Arch Fr Pediatr. 1975;5:401–4. David G. Editorial: sperm banks in France. Arch Fr Pediatr. 1975;5:401–4.
19.
go back to reference Schwartz D, Mayaux MJ, Spria A, Moscato ML, Jouannet P, Czyglik F, et al. Semen characteristics as a function of age in 833 fertile men. Fertil Steril. 1983;39:530–5.PubMed Schwartz D, Mayaux MJ, Spria A, Moscato ML, Jouannet P, Czyglik F, et al. Semen characteristics as a function of age in 833 fertile men. Fertil Steril. 1983;39:530–5.PubMed
20.
go back to reference Levitas E, Lunenfeld E, Weisz N, Friger M, Potashnik G. Relationship between age and semen parameters in men with normal sperm concentration: analysis of 6, 022 semen samples. Andrologia. 2007;39:45–50.PubMedCrossRef Levitas E, Lunenfeld E, Weisz N, Friger M, Potashnik G. Relationship between age and semen parameters in men with normal sperm concentration: analysis of 6, 022 semen samples. Andrologia. 2007;39:45–50.PubMedCrossRef
21.
go back to reference Rolf C, Behre HM, Nieschlag E. Reproductive parameters of older couples compared to younger men of infertile couples. Int J Androl. 1996;19:135–42.PubMedCrossRef Rolf C, Behre HM, Nieschlag E. Reproductive parameters of older couples compared to younger men of infertile couples. Int J Androl. 1996;19:135–42.PubMedCrossRef
22.
go back to reference Rolf C, Kenkel S, Nieschlag E. Age-related disease pattern in infertile men: increasing incidence of infections in older patients. Andrologia. 2002;34:209–17.PubMedCrossRef Rolf C, Kenkel S, Nieschlag E. Age-related disease pattern in infertile men: increasing incidence of infections in older patients. Andrologia. 2002;34:209–17.PubMedCrossRef
23.
go back to reference Andolz P, Bielsa MA, Vila J. Evolution of semen quality in northeastern Spain: a study in 22 759 infertile men over a 36 year period. Hum Reprod. 1999;14:731–5.PubMedCrossRef Andolz P, Bielsa MA, Vila J. Evolution of semen quality in northeastern Spain: a study in 22 759 infertile men over a 36 year period. Hum Reprod. 1999;14:731–5.PubMedCrossRef
24.
go back to reference Mladenovic I, Micic S, Papic N, Genbacev O, Marinkovic B. Sperm morphology and motility in different age populations. Arch Androl. 1994;32:197–205.PubMedCrossRef Mladenovic I, Micic S, Papic N, Genbacev O, Marinkovic B. Sperm morphology and motility in different age populations. Arch Androl. 1994;32:197–205.PubMedCrossRef
25.
go back to reference Auger J, Kunstmann JM, Czyglik F, Jouannet P. Decline in semen quality among fertile men in Paris during the past 20 years. N Engl J Med. 1995;332:281–5.PubMedCrossRef Auger J, Kunstmann JM, Czyglik F, Jouannet P. Decline in semen quality among fertile men in Paris during the past 20 years. N Engl J Med. 1995;332:281–5.PubMedCrossRef
26.
go back to reference Fisch H, Goluboff ET, Olson JH, Feldshuh J, Broder SJ, Barad DH. Semen analysis in 1, 283 men from the United States over a 25-year period: no decline in quality. Fertil Steril. 1996;65:1009–14.PubMed Fisch H, Goluboff ET, Olson JH, Feldshuh J, Broder SJ, Barad DH. Semen analysis in 1, 283 men from the United States over a 25-year period: no decline in quality. Fertil Steril. 1996;65:1009–14.PubMed
27.
go back to reference Bujan L, Mansat A, Pontonnier F, Mieusset R. Time series analysis of sperm concentration in fertile men in Toulouse, France between 1977 and 1992. BMJ. 1996;312:471–2.PubMed Bujan L, Mansat A, Pontonnier F, Mieusset R. Time series analysis of sperm concentration in fertile men in Toulouse, France between 1977 and 1992. BMJ. 1996;312:471–2.PubMed
28.
go back to reference 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. BMJ. 1996;312:467–71.PubMed 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. BMJ. 1996;312:467–71.PubMed
29.
go back to reference Plastira K, Msaouel P, Angelopoulou R, Zanioti K, Plastiras A, Pothos A, et al. The effects of age on DNA fragmentation, chromatin packaging and conventional semen parameters in spermatozoa of oligoasthenoteratozoospermic patients. J Assist Reprod Genet. 2007;24:437–43.PubMedCrossRef Plastira K, Msaouel P, Angelopoulou R, Zanioti K, Plastiras A, Pothos A, et al. The effects of age on DNA fragmentation, chromatin packaging and conventional semen parameters in spermatozoa of oligoasthenoteratozoospermic patients. J Assist Reprod Genet. 2007;24:437–43.PubMedCrossRef
30.
go back to reference Sailer BL, Jost LK, Evenson DP. Mammalian sperm DNA susceptibility to in situ denaturation associated with the presence of DNA strand breaks as measured by the terminal desoxynucleotidyl transferase assay. J Androl. 1995;16:80–7.PubMed Sailer BL, Jost LK, Evenson DP. Mammalian sperm DNA susceptibility to in situ denaturation associated with the presence of DNA strand breaks as measured by the terminal desoxynucleotidyl transferase assay. J Androl. 1995;16:80–7.PubMed
31.
go back to reference Zini A, Libman J. Sperm DNA damage: clinical significance in the era of assisted reproduction. CMAJ. 2006;175:495–500.PubMedCrossRef Zini A, Libman J. Sperm DNA damage: clinical significance in the era of assisted reproduction. CMAJ. 2006;175:495–500.PubMedCrossRef
32.
go back to reference Agarwal A, Saleh RA. Utility of oxidative stress test in the male infertility clinic. Zhonghua Nan Ke Xue. 2002;8:1–9.PubMed Agarwal A, Saleh RA. Utility of oxidative stress test in the male infertility clinic. Zhonghua Nan Ke Xue. 2002;8:1–9.PubMed
33.
34.
go back to reference Sakkas D, Mariethoz E, Manicardi G, Bizzaro D, Bianchi PG, Bianchi U. Origin of DNA damage in ejaculated human spermatozoa. Rev Reprod. 1999;4:31–7.PubMedCrossRef Sakkas D, Mariethoz E, Manicardi G, Bizzaro D, Bianchi PG, Bianchi U. Origin of DNA damage in ejaculated human spermatozoa. Rev Reprod. 1999;4:31–7.PubMedCrossRef
35.
go back to reference Singh NP, Muller CH, Berger RE. Effects of age on DNA double-strand breaks and apoptosis in human sperm. Fertil Steril. 2003;80:1420–30.PubMedCrossRef Singh NP, Muller CH, Berger RE. Effects of age on DNA double-strand breaks and apoptosis in human sperm. Fertil Steril. 2003;80:1420–30.PubMedCrossRef
36.
go back to reference Sati L, Ovari L, Bennett D, Simon SD, Demir R, Huszar G. Double probing of human spermatozoa for persistent histones, surplus cytoplasm, apoptosis and DNA fragmentation. Reprod Biomed Online. 2008;16:570–9.PubMedCrossRef Sati L, Ovari L, Bennett D, Simon SD, Demir R, Huszar G. Double probing of human spermatozoa for persistent histones, surplus cytoplasm, apoptosis and DNA fragmentation. Reprod Biomed Online. 2008;16:570–9.PubMedCrossRef
37.
go back to reference Moskovtsev SI, Willis J, Mullen JB. Age-related decline in sperm deoxyribonucleic acid integrity in patients evaluated for male infertility. Fertil Steril. 2006;85:496–9.PubMedCrossRef Moskovtsev SI, Willis J, Mullen JB. Age-related decline in sperm deoxyribonucleic acid integrity in patients evaluated for male infertility. Fertil Steril. 2006;85:496–9.PubMedCrossRef
38.
go back to reference Moskovtsev SI, Willis J, White J, Mullen JB. Sperm DNA damage: correlation to severity of semen abnormalities. Urology. 2009;74:789–93.PubMedCrossRef Moskovtsev SI, Willis J, White J, Mullen JB. Sperm DNA damage: correlation to severity of semen abnormalities. Urology. 2009;74:789–93.PubMedCrossRef
39.
go back to reference Bosch M, Rajmil O, Martinez-Pasarell O, Egozcue J, Templado C. Linear increase of diploidy in human sperm with age: a four-colour FISH study. Eur J Hum Genet. 2001;9:533–8.PubMedCrossRef Bosch M, Rajmil O, Martinez-Pasarell O, Egozcue J, Templado C. Linear increase of diploidy in human sperm with age: a four-colour FISH study. Eur J Hum Genet. 2001;9:533–8.PubMedCrossRef
40.
go back to reference Bosch M, Rajmil O, Egozcue J, Templado C. Linear increase of structural and numerical chromosome 9 abnormalities in human sperm regarding age. Eur J Hum Genet. 2003;11:754–9.PubMedCrossRef Bosch M, Rajmil O, Egozcue J, Templado C. Linear increase of structural and numerical chromosome 9 abnormalities in human sperm regarding age. Eur J Hum Genet. 2003;11:754–9.PubMedCrossRef
41.
go back to reference Griffin DK, Abruzzo MA, Millie EA, Sheean LA, Feingold E, Sherman SL, et al. Non-disjunction in human sperm: evidence for an effect of increasing paternal age. Hum Mol Gen. 1995;4:2227–32.PubMedCrossRef Griffin DK, Abruzzo MA, Millie EA, Sheean LA, Feingold E, Sherman SL, et al. Non-disjunction in human sperm: evidence for an effect of increasing paternal age. Hum Mol Gen. 1995;4:2227–32.PubMedCrossRef
42.
go back to reference Robbins WA, Baulch JE, Moore DI, Weire HU, Blakey D, Wyrobek AJ. Three-probe fluorescence in situ hybridization to assess chromosome X, Y, and 8 aneuploidy in sperm of 14 men from two healthy groups: evidence for a paternal age effect on sperm aneuploidy. Reprod Fertil Dev. 1995;7:799–809.PubMedCrossRef Robbins WA, Baulch JE, Moore DI, Weire HU, Blakey D, Wyrobek AJ. Three-probe fluorescence in situ hybridization to assess chromosome X, Y, and 8 aneuploidy in sperm of 14 men from two healthy groups: evidence for a paternal age effect on sperm aneuploidy. Reprod Fertil Dev. 1995;7:799–809.PubMedCrossRef
43.
go back to reference Martin RH, Spriggs E, Ko E, Rademaker AW. The relationship between paternal age, sex ratios, and aneuploidy frequencies in human sperm, as assessed by multicolor FISH. Am J Hum Gen. 1995;57:1395–9. Martin RH, Spriggs E, Ko E, Rademaker AW. The relationship between paternal age, sex ratios, and aneuploidy frequencies in human sperm, as assessed by multicolor FISH. Am J Hum Gen. 1995;57:1395–9.
44.
go back to reference Kinakin B, Rademaker A, Martin R. Paternal age effect of YY aneuploidy in human sperm, as assessed by fluorescence in situ hybridization. Cytogenet Cell Genet. 1997;78:116–9.PubMedCrossRef Kinakin B, Rademaker A, Martin R. Paternal age effect of YY aneuploidy in human sperm, as assessed by fluorescence in situ hybridization. Cytogenet Cell Genet. 1997;78:116–9.PubMedCrossRef
45.
go back to reference Asada H, Sueoka K, Hashiba T, Kuroshima M, Kobayashi N, Yoshimura Y. The effects of age and abnormal sperm count on the nondisjunction of spermatozoa. J Assist Reprod Genet. 2000;17:51–9.PubMedCrossRef Asada H, Sueoka K, Hashiba T, Kuroshima M, Kobayashi N, Yoshimura Y. The effects of age and abnormal sperm count on the nondisjunction of spermatozoa. J Assist Reprod Genet. 2000;17:51–9.PubMedCrossRef
46.
go back to reference Guttenbach M, Kohn FM, Engel W, Schmid M. Meiotic nondisjunction of chromosomes 1, 17, 18, X, and Y in men more than 80 years of age. Biol Reprod. 2000;63:1727–9.PubMedCrossRef Guttenbach M, Kohn FM, Engel W, Schmid M. Meiotic nondisjunction of chromosomes 1, 17, 18, X, and Y in men more than 80 years of age. Biol Reprod. 2000;63:1727–9.PubMedCrossRef
47.
go back to reference Lowe X, Eskenazi B, Nelson DO, Kidd S, Alme A, Wyrobek AJ. Frequency of XY sperm increases with age in fathers of boys with Klinefelter syndrome. Am J Hum Genet. 2001;69:1046–54.PubMedCrossRef Lowe X, Eskenazi B, Nelson DO, Kidd S, Alme A, Wyrobek AJ. Frequency of XY sperm increases with age in fathers of boys with Klinefelter syndrome. Am J Hum Genet. 2001;69:1046–54.PubMedCrossRef
Metadata
Title
The effects of male aging on semen quality, sperm DNA fragmentation and chromosomal abnormalities in an infertile population
Authors
Sonia Brahem
Meriem Mehdi
Hatem Elghezal
Ali Saad
Publication date
01-05-2011
Publisher
Springer US
Published in
Journal of Assisted Reproduction and Genetics / Issue 5/2011
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-011-9537-5

Other articles of this Issue 5/2011

Journal of Assisted Reproduction and Genetics 5/2011 Go to the issue