This web only provides the extract of this article. If you want to read the figures and tables, please reference the PDF full text on Blackwell Synergy. Thank you.
- Original Article -
Seminal characteristics and sexual behavior in men of different age groups: is there an aging effect?
Panayiotis M. Zavos1, Khalied Kaskar1, Juan R. Correa2, Suresh C. Sikka3
1Andrology Institute of America, Lexington, Kentucky 40523, USA
2 Centre de Fertilidad del Caribe, Rio Piedras, Puerto Rico 00923, USA
3Department of Urology, Tulane University School of Medicine, New Orleans, Louisiana 70118, USA
Abstract
Aim: To assess the seminal characteristics as well as the sexual behavior of men of various age groups to establish the
presence of an aging effect on those characteristics.
Methods: Semen samples were collected from men
(n=792) undergoing in vitro fertilization or intrauterine insemination in cases of female factor infertility only. Samples were
collected using a seminal collection device at intercourse and evaluated manually according to World Health
Organization (WHO) standards. Men were divided into four groups according to their ages: (i) 20-30, (ii) 31-40, (iii) 41-50
and (iv) 51-60 years, and their seminal characteristics and responses to a sexual behavior questionnaire were
compared. Results: The data showed statistically significant differences in the seminal characteristics tested, most notably in the
sperm concentration, motility, grade of motility, hypo-osmotic swelling and normal sperm morphology. Furthermore,
the decline in normal sperm morphology with age was more pronounced when using strict criteria rather than WHO
standards. There were also differences in total sperm count, total motile sperm and total functional sperm fraction
(assessed by both WHO and strict criteria). Significant differences were also observed in the sexual behavior patterns
in older men in terms of the number of years they have been trying to conceive, sexual frequency and sexual satisfaction. Conclusion: The data clearly illustrate an aging effect on semen characteristics and sexual behavior in men as they
age. It is suggested that the aging effect be taken into consideration when proposing normal standard values for
semen characteristics in routine semen analysis as outlined by WHO standards. (Asian J Androl 2006 May; 8: 337-341)
Keywords: seminal parameters; male; aging effect; fertility; sexual behavior; semen quality; male factor infertility
Correspondence to: Dr Panayiotis M. Zavos, Andrology Institute of America, P. O. Box 23777, Lexington, Kentucky 40523, USA.
Tel/Fax: +859-278-6806
E-mail: zavos@zavos.org
Received 2004-11-15 Accepted 2006-12-23
1 Introduction
It has been established that aging in women significantly reduces the potential to produce oocytes and achieve
conception. Female fecundity starts to decline after 30 years of age and is more pronounced after 40 years of age,
thereby making maternal age the main limiting factor in the treatment of infertility [1, 2]. However, very little data
show similar trends in men, possibly because of the fact that spermatogenesis can continue throughout life. It has
been shown that in bulls, spermatozoal production increases from puberty to sexual maturity and declines again in
older men [3]. Also, young rats show higher sexual frequency and number of erections than middle-aged rats. Such
decline was correlated to decline in sex hormones [4].
Older men have been shown to have decreased sexual frequency [5], ejaculate volume [5, 6], motility [5-7] and
normal morphology [6] as compared to younger men. However, in a study comparing seminal characteristics of
proven fertile fathers aged 60-88 years and those aged 24-37 years, the older men showed higher sperm density and
lower sperm motility with no difference in seminal volume and normal sperm morphology [7].
Changes in the biochemistry of human semen have been reported with aging, showing decreases in the
concentrations of fructose [7], kallikrein and prostate specific antigen (PSA), and elevated liquefaction times [8]. These
alterations could cause age-related declines in sperm motility and fertilizing ability.
Ford et al. [9] showed that increasing paternal age is associated with delayed conception in a large population of
fertile couples. Watanabe et al. [10] showed a negative correlation between the fertilization rate in an oocyte donor
program and paternal age. The fertilization rate was lower for men over 39 years of age (51.3%) compared to those
younger than 39 years (60.2%). Recently, it has also been shown that both paternal and maternal aging has a deleterious
effect on in vitro fertilization (IVF) and gamete intrafallopian tube transfer (GIFT) outcomes [11].
On a structural level, advanced age has been associated with an increase in sperm double stranded DNA damage
[12]. Genetic disease has been shown be positively associated with increasing paternal age and this could be a result
of an increase in sperm genetic abnormalities [13]. Furthermore, an increase in aneuploid sperm has been reported for
oligoasthenozoospermic men when compared to fertile controls [14]. However, the aneuploidy rate for men under
30 years of age was not significantly different from men over 60 years [13].
The aim of the present study was to assess the seminal characteristics as well as the sexual behavior of men of
various age groups to establish the presence of an aging effect on those characteristics.
2 Materials and methods
2.1 Patient profile
Seven hundred and ninety-two couples undergoing infertility evaluation at our facilities (Andrology Institute of
America, Lexington, Kentucky, USA) participated in the current study. Only couples with female factor infertility and
no male factor infertility as determined by routine semen analyses were included in the study. Men were divided into
four groups according to their ages: (i) 20-30, (ii) 31-40, (iii) 41-50 and (iv) 51-60 years.
2.2 Semen collection and evaluation
All ejaculates were produced during intercourse using Male Factor Pak (ZDL, Lexington, KY, USA) after
3-4days of abstinence [15, 16]. The experimental protocol of the current study was reviewed and approved by the
Institutional Review Board at the Andrology Instiute of America. After semen samples were produced and
liquefied (within 15-30min), each specimen was evaluated manually according to standard procedures recommended by the
World Health Organization (WHO) using a phase-contrast microscope [17]. Semen measures included volume, sperm
concentration per mL, percentage sperm motility, grade of sperm motility (scale of 0-4) and normal sperm morphology,
and hypo-osmotic swelling. Sperm morphology was also assessed using strict criteria
[18]. Derivative parameters, such as total motile sperm (TMS, total sperm count×percentage motility), total functional sperm fraction (TFSF; total motile
sperm×percentage normal morphology as assessed by WHO guidelines) and the critical total functional sperm fraction
(total motile sperm×percentage normal morphology as assessed by strict criteria, as described above) were also calculated.
2.3 Measurement of sexual satisfaction
During the first visit, each couple was asked to complete a questionnaire pertaining to their clinical profile and sexual
history in the presence of each other. The requested information included: age of the husband and wife, number of years
of marriage, years trying to conceive, sexual frequency per month and sexual satisfaction/rating (0-10; 0=poor and
10=extremely satisfactory).
2.4 Statistical evaluation
Men were divided into four groups according to their ages: (i) 20-30, (ii) 31-40, (iii) 41-50 and (iv) 51-60 years,
and their seminal characteristics and responses to the sexual behavior questionnaire were compared. The results
obtained were analyzed statistically with the use of the unpaired
t-test, as appropriate. P<0.05 was considered statistically significant.
3 Results
The results obtained in the present study are shown in Tables1 and 2. The data showed statistically significant
differences in the seminal characteristics tested, most notably in the sperm concentration, motility, grade of motility,
hypo-osmotic swelling and normal sperm morphology. There were also differences in total sperm count, total motile
sperm and total functional sperm fraction (as assessed by both WHO and strict criteria). Significant differences were
also observed in the sexual behavior patterns of older men in terms of the number of years they have been trying to
conceive, sexual frequency and sexual satisfaction.
Most noticeably, there was a significant increase in almost all of the parameters assessed in the 31-40-year age group
versus the younger 20-30-year age group, after which there was a significant decrease in the 41-50 and 51-60-year age
groups. A marked but not significant increase was noted in the seminal volume in the 31-40-year age group, resulting in
corresponding increases in total sperm count, TMS and TFSF. There was a consistent decrease in the percentage
normal sperm morphology as assessed by WHO guidelines with increasing age. More noticeably, this decrease in the
percentage normal sperm morphology was more pronounced when using strict criteria for morphology evaluation
(Figure1).
Significant differences were also observed in the sexual behavior patterns of older men in terms of the number of
years they have been trying to conceive, sexual frequency and sexual satisfaction. There was a significant decline in
the sexual frequency of men as age increased (Table2). Sexual satisfaction rated on a scale of 0-10 showed a
significant decline in men over 40 years of age. However, the overall satisfaction in all the age groups remained high
despite the decline.
4 Discussion
The data clearly illustrate an effect on semen characteristics and sexual behavior in men as they age. Although
semen quality declined with age, in the group of normospermic men, the semen parameters were still above normal
levels according to WHO standards. The decline in sperm quality along with the decreasing sexual frequency noted in
the present study could cumulatively have a negative effect on fecundity. It is suggested that the aging effect be taken
into consideration when proposing normal standard values for semen characteristics in routine semen analysis as
outlined by the WHO standards. The cut-off values for normal semen characteristics might be too strict when
evaluating older men and, thereby, classifying them as subfertile when in fact their sperm characteristics might be
within normal limits for their age group. This will be of significant clinical importance when advising the patient
regarding his potential for natural conception prior to pursuing assisted reproductive technologies.
Increasing paternal age was associated with delayed conception in fertile couples, especially after the age of
25 years [1]. The published literature suggested various causes for the decline in conception. Johnson
et al. [19] reported that older men (aged 51-84 years) have significantly reduced testicular weight, length of tubules, volume of
seminiferous tubule and daily sperm production, when compared to men between 20 and 29 years of age. They also
showed that the daily sperm production per testes was 30% lower in older men [20].
Upon closer inspection of the various sperm characteristics in the current study, we have shown significant
differences in almost all the semen parameters tested between each of the age groups. Of interest, there was a significant
increase in semen characteristics in patients in the
31-40-year age group as compared to the 20-30-year group, after
which the qualitative and quantitative sperm characteristics declined significantly for the 41-50-year and 51-60-year
age groups. This trend is also noted by Schwartz
et al. [21]. However, they found that the only parameter
significantly different between the age groups was the percentage normal morphology.
The deficiencies noted in older patients do not affect the ability of sperm to fertilize oocytes
in vitro [22, 23], presumably because during IVF the number of normal, motile sperm is standardized to eliminate such variations. In
addition, subsequent embryo development and implantation was not affected by the age of the man providing the
semen sample [22]. In contrast, Watanabe
et al. [10] showed a negative correlation between the fertilization rate in an
oocyte donor program and paternal age. The fertilization rate is lower for men over 39 years of age (51.3%)
compared to those below 39 years (60.2%). However, no difference is noted in the clinical pregnancy rate between these
two groups. Recently, aging, both paternal and maternal, has been associated with deleterious effects on IVF and
GIFT outcomes, as evidenced by pregnancy and live birth rates [11].
The aging effect on men is further demonstrated in sexual behavior patterns in terms of the number of years they
have been trying to conceive, sexual frequency and sexual satisfaction. We showed in the present study that sexual
frequency declined significantly in each of the age groups tested. Similarly, the degree of sexual satisfaction
decreased significantly after 40 years of age. Ford
et al. [9] adjusted for the age of the woman, and found that the
likelihood of conception within 6-12months was lower in older men.
The data obtained in the present study clearly illustrate an aging effect on semen characteristics and sexual behavior in
men as they age. Although semen quality declined with age, in this group of normospermic men, the semen parameters
were still above normal levels according to WHO standards. In cases of male factor infertility, this aging effect on semen
quantity could be significant enough to impact on sperm function. The decline in sperm quality along with decreasing sexual
frequency could have a negative effect on these couples¡¯s overall fecundity. Given the results generated in the present study,
it is suggested that the aging effect be taken into consideration when proposing normal standard values for semen
characteristics during routine semen analysis to standardize the population and to eliminate any bias that might be associated with
advanced age. References
1 Hull MG, Fleming CF, Hughes AO, McDermott A. The age-related decline in female fecundity: a quantitative controlled study of
implanting capacity and survival of individual embryos after
in vitro fertilization. Fertil Steril 1996; 65: 783-90.
2 Spandorfer SD, Avrech OM, Colombero LT, Palermo GD, Rosenwaks Z. Effect of parental age on fertilization and pregnancy
characteristics in couples treated by intracytoplasmic sperm injection. Hum Reprod 1998; 13: 334-8.
3 Foote RH, Seidel GE Jr, Hahn J, Berndtson WE, Coulter GH. Seminal quality, spermatozoal output and testicular changes in growing
Holstein bulls. J Dairy Sci 1977; 60: 85-8.
4 Gray GD, Smith ER, Damassa DA, Ehrenkranz JR, Davidson JM. Neuroendocrine mechanisms mediating the suppression of
circulating testosterone levels associated with chronic stress in male rats. Neuroendocrinology 1978; 25: 247-56.
5 Rolf C, Behre HM, Nieschlag E. Reproductive parameters of older compared to younger men of infertile couples. Int J Androl 1996;
19: 135-42.
6 Kuhnert B, Nieschlag E. Reproductive functions of the ageing male. Hum Reprod Update 2004; 10: 327-39.
7 Nieschlag E, Lammers U, Freischem CW, Langer K, Wickings EJ. Reproductive functions in young fathers and grandfathers. J Clin
Endocrinol Metab 1982; 55: 676-81.
8 Matsuda Y, Shimokawa KI, Katayama M, Shimuzu H, Chiba R. Action of physiologically active materials in human semen during
aging. Arch Androl 2004; 50: 131-7.
9 Ford WC, North K, Taylor H, Farrow A, Hull MG, Golding J. Increasing paternal age is associated with delayed conception in a large
population of fertile couples: evidence for declining fecundity in older men. The ALSPAC Study Team (Avon Longitudinal Study of
Pregnancy and Childhood). Hum Reprod 2000; 15: 1703-8.
10 Watanabe Y, Cornet D, Merviel J, Mandelbaum J, Antoine JM, Uzan S. Influence of husband's age on outcome of a shared oocyte
donation program. Fertil Steril 2000; 74: S78-9.
11 Klonoff-Cohen HS, 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: 507-14.
12 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.
13 Luetjens CM, Rolf C, Gassner P, Werny JE, Nieschlag E. Sperm aneuploidy rates in younger and older men. Hum Reprod 2002; 17:
1826-32.
14 Vegetti W, Van Assche E, Frias A, Verheyen A, Bianchi G, Bonduelle MM,
et al. Correlation between semen parameters and sperm
aneuploidy rates investigated by fluorescence
in-situ hybridization in infertile men. Hum Reprod 2000; 15: 351-65.
15 Zavos PM. Characteristics of human ejaculates collected via masturbation and a new Silastic seminal fluid collection device (SCD).
Fertil Steril 1985; 43: 49l-2.
16 Zavos PM, Goodpasture JC. Clinical improvements of specific seminal deficiencies via intercourse with a seminal collection device
versus masturbation. Fertil Steril 1985; 51:190-3.
17 World Health Organization. WHO laboratory manual for the examination of human semen and semencervical mucus interaction.
Cambridge: Cambridge University Press: 1999.
18 Kruger TF, Menkveld R, Stander FS, Lombard CJ, van der Merwe JP, van Zyl JA,
et al. Sperm morphologic features as a prognostic
factor in in vitro fertilization. Fertil Steril 1986; 46: 1118-23.
19 Johnson L, Abdo JG, Petty CS, Neaves WB. Effect of age on the composition of seminiferous tubular boundary tissue and on the
volume of each component in humans. Fertil Steril 1988; 49: 104551.
20 Johnson L, Petty CS, Neaves WB. Influence of age on sperm production and testicular weights in men. J Reprod Fertil 1984; 70:
2118.
21 Schwartz D, Mayaux MJ, Spira 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.
22 Gallardo E, Simon C, Levy M, Guanes PP, Remohi J, Pellicer A. Effect of age on sperm fertility potential: oocyte donation as a model.
Fertil Steril 1996; 66: 260-4.
23 Paulson RJ, Milligan RC, Sokol RZ. The lack of influence of age on male fertility. Am J Obstet Gynecol 2001; 184: 818-24.
|