Semen characteristics of fertile and subfertile men in a fertility clinic and correlation with age

1 Introduction

Semen quality is one of the most valuable indications of male reproductive health where semen analysis plays a critical role in the diagnosis and treatment of male infertility. Semen analysis is widely undertaken applying the reference values for normal semen measurements published by the World Health Organization (WHO, 1999).

Several studies during the last decades have highlighted the concern of a time-related decrease in the semen quality worldwide (Miyamoto et al., 2012). They provided the evidences of a decreasing trend in sperm count and percentage of sperm motility or normal sperm morphology over the last decades, from France (Auger et al., 1995), Scotland (Irvine et al., 1996), Italy (Bilotta et al., 1999), Denmark (Andersen et al., 2000; Jensen et al., 2002), India (Adiga et al., 2008), and Tunisia (Feki et al., 2009).

These findings are of an important concern since men with sperm count <40 × 10⁶/ml were indicated to experience reduced fecundity (Bonde et al., 1998). However, in contradiction, other studies reported nonsignificant change in human semen quality (Bujan et al., 1996; Fisch et al., 1996; Rasmussen et al., 1997; Andolz et al., 1999; Acacio et al., 2000; Swan et al., 2000; Marimuthu et al., 2003; Axelsson et al., 2011). Hence, the global temporal trend in semen quality is still on debate.

Regional differences in semen quality have been reported for some areas in the USA (Fisch et al., 1996), Europe (Jørgensen et al., 2001; Jørgensen et al., 2002), Japan (Iwamoto et al., 2006), India (Adiga et al., 2008), and China (Gao et al., 2007). The European study of fertile men showed that sperm concentration of Danish men was 74% of that of Finnish men and 82% of the Scottish men (Jørgensen et al., 2001). In Southwest China, Li et al. (2009) showed that the semen parameters’ values of men were markedly different from those reported for the other Chinese, USA or Europeans. Japanese fertile men had a semen quality level similar to Danish men that reported to have the lowest values among the investigated men in Europe (Iwamoto et al., 2006).

Nevertheless, some studies suggested that a decline in semen parameters is associated with increased age (Kidd et al., 2001; Chen et al., 2003; Eskenazi et al., 2003; Maya et al., 2009).

However, others showed no such association (Chen et al., 2004; Seo et al., 2000; Li et al., 2009).

In Saudi Arabia, the WHO reference values have been used to assess the reproductive health of Saudi men and there are no available data for the semen parameters in different cities, neither in other Arabic countries, except those reported for subfertile Tunisian men by Feki et al. (2009).

This study aimed to evaluate the semen characteristics of Saudi fertile, subfertile men, and men of unproven fertility in a fertility clinic in Riyadh city and to investigate the relationship between age and semen parameters.

2 Methods

3 Results

3.4

3.4 Correlation of semen parameters with age

The results of age correlation with each of the semen parameters in the different groups (Figs. 1 and 2) were as follow:

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Figure 1

Scatter plots with regression lines of semen volume versus age for the pooled data and the different study groups.

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Figure 2

Scatter plots with regression lines of sperm motility versus age for the pooled data and the different study groups.

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3.4.1

3.4.1 Fertile men

The age range of men in this group 23–53 years, the median was 37 (31.5–40.5) years. The age was positively correlated with most of the semen parameters but was only significant with the sperm concentration (r = 0.304, P= 034).

3.4.2

3.4.2 Subfertile men

The age range was 21–74 years, the median was 34 (29–40) years. There was an inverse correlation between age and each of the semen parameters but there was significant negative correlation with sperm motility (r = −0.235, P= 0.01).

3.4.3

3.4.3 Unproven fertility men

The age range was 20–44 years; the median was 27 (25–30) years. There was negative correlation with sperm motility (r = −0.318, P= 0.009).

3.4.4

3.4.4 Pooled data

The age range of all men was 20–74 years, the median was 32 (28–39) years. There was a significant negative correlation between age and semen volume (r = −0.152, P= 0.011) and sperm motility (r = −0.149, P= 0.023).

4 Discussion

This is the first study conducted, as a pilot one, to characterize the semen parameters in Saudi men in Riyadh city. The number of men of proven fertility was lower than the subfertile men due to the difficulty in collecting semen samples from men of general population as it is an embarrassing process unless they have to collect semen for analysis in the fertility clinics.

The social parameters of the fertile and subfertile groups were in the same range regarding age, duration of unprotected intercourse, and the occupation in each group. Hence the two groups were well matched, the social parameters of the unproven fertility men were also in the same range as the other two groups except age. Age was lower in the last group compared with other groups, as most of these men were single, due to the social customs and traditions of the Saudi society that encourage men to get married at young age.

The differences in the median values of the main semen characteristics between the fertile and subfertile groups were in consistence with those reported by Nallella et al. (2006) and Guzick et al. (2001). The values of semen parameters of each of fertile and subfertile men were compared with those reported in other populations; USA (Acacio et al., 2000; Guzick et al., 2001; Nallella et al., 2006), Europe (Auger et al., 1995; Bilotta et al., 1999; Andolz et al., 1999; Jørgensen et al., 2001; Lackner et al., 2005; Sripada et al., 2007), China (Li et al., 2009), Japan (Iwamoto et al., 2006), india (Marimuthu et al., 2003; Adiga et al., 2008) and Korea (Seo et al., 2000) (Tables 4 and 5).

Sperm concentration of the fertile men was nearly two times higher than that recorded for the Americans or Danish fertile men and was also higher than the values reported for other populations, such as French, Scottish, Finnish, Italian, and Chinese men; whereas, Japanese men had the lowest sperm concentration.

Sperm motility was lower than that reported in different populations, i.e. American fertile men, Danish, Scottish and Finnish, Japanese and Italian men, but was similar to the results reported in French.

The percentage of sperm normal morphology was lower than that reported for the European populations, but higher than Japanese and in men in Cleveland (USA).

These differences could be due to endocrine, ethnic, geographical, environmental, nutritional, or life style variations. Specifically, the higher temperatures during most of the year in Riyadh city may affect sperm motility. In addition, genetic factors may be a factor where differences are due to different polymorphisms in the genes involved in influencing these parameters.

In subfertile men; sperm concentration was significantly higher than that the WHO (1999) reference (<20 × 10⁶/ml) that could be due to the high percentage of the subfertile men (∼50%) categorized as subfertile for reasons other than the sperm concentration (normal: 99.27 × 10⁶/ml and asthenospermia: 73.28 × 10⁶/ml). Nallella et al. (2006) reported a large group of patients with male factor infertility that presented higher sperm concentration. This average value was also higher than that reported for subfertile men in South India and Vienna (Austria), and lower than that of American subfertile men.

Sperm motility of subfertile Saudis was lower than reported for subfertile men of other population such as in South India, Northeast of Scotland and USA, but not that reported in Vienna (Austria). These variations could be due to the relatively lower sperm motility in the general population of our study compared with other populations.

Around one third of the subfertile men were asthenozoospermic, and one fifth were oligoasthenozoospermic. This shows a relatively high percentage (∼57%) of Saudi subfertile men with abnormal sperm motility that was similar to the percentage reported in Los Angeles and Munirka (India). That percentage, followed by around 27% of the Saudi subfertile men who had sperm concentration <20 × 10⁶/ml (5.7% oligozoospermic and 21.5% oligoasthenozoospermic). This percentage was higher than that reported for men in Los Angeles.

In comparison with other studies (Table 6), the prevalence of azoospermia (26%) was higher than that reported for subfertile men in South India, Los Angeles (USA), Northeast Spain, and Korea. Acacio et al. (2000), and Andolz et al. (1999) demonstrated that 4% and 6%, respectively, of the subjects were azoospermic. The subjects of their studies were of subfertile relationship so they were not diagnosed as subfertile men, and were also of unknown age. Adiga et al. (2008) recruited a population of subfertile men of undefined age of whom 7.2% were azoospermic. Seo et al. (2000) investigated a population that is similar to that in our study (subfertile men; 32 years) reporting that 19% of the population was azoospermic. This value was closer to the value reported in the present study.

There was a significant correlation between age and the sperm concentration only in fertile men group that was not observed in other groups. This could be due to the lower variability in the age range and the small sample size of fertile group, of whom 57% fell in the age range of 30–40 years old, 13% were >45 years, and the oldest man was 53 years. The sample size of the subfertile group was higher, the age range was wider (50% were in the 30–40 years range), 13% were >45 years and the oldest man was 74 year. In the group of unproven fertility men, the sample size was higher than the fertile group, and they were younger with 26% in the age range 30–39 year old and the oldest was 39 years. Other studies (Table 7) agreed with the finding of this study suggesting no impact of age on sperm concentration (Cavalcante et al., 2008; Li et al., 2009; Seo et al., 2000). However, others were in disagreement with our results (Maya et al., 2009). Chen et al. (2004), reported nonsignificant impact of age on semen parameters in a sample size of 306, whereas Chen et al. (2003) reported an inverse relationship between age and semen parameters when the sample size and the age range were larger.

There was an inverse correlation between age and sperm motility and semen volume in almost all groups in agreement with Kidd et al. (2001) suggesting that advanced age was associated with a decrease in semen volume, sperm motility, and sperm morphology but not sperm concentration. Cavalcante et al. (2008) showed an inverse effect of age on semen volume but not on other semen parameters. Maya et al. (2009) showed an inverse relationship between age and the main semen parameters. In contrast, some studies reported no impact of age on semen parameters (Li et al., 2009; Chen et al., 2004).

The contradiction between these studies could be due to differences in the age-range and the number of participated individuals, in addition, to other confounder factors such as ethnics, genetics, geographical location and the surrounding environment.

The relatively low sperm motility in the general population and the relatively high prevalence of azoospermia are of important implications with respect to infertility and further studies using large number of fertile and subfertile subjects with additional information on their smoking, socioeconomic condition, and life- style related factors are recommended.

In conclusion, our findings suggest that the values of sperm parameters were, in agreement with WHO criteria, significantly different in normal fertile from that of the subfertile Saudi men. Age has no effect on sperm concentration, viscosity, and morphology, but an inverse effect of age was observed on sperm motility and semen volume. As Riyadh city has the highest population (18.5%) among other Saudi cities, due to diverse socioeconomic factors, it is important to assess the semen quality in its different parts for further validation of the statement. In addition, further studies in other regions of Saudi Arabia are also needed.

5 Ethical statement

After IRB approval, all participants were asked to sign an informed consent form if they agreed to take part in this study.