Objective
To compare the different sperm parameters according to season of the year on sperm production day and the season 70 days prior (during spermatogenesis).
Study Design
Retrospective Andrology Laboratory data comparison. A total of 6455 consecutive semen samples were collected as part of the basic fertility evaluation of 6447 couples. According to sperm concentration, the samples were classified as Normozoospermic or Oligozoospermic and analyzed in relation to the season.
Results
The sperm concentration and percentage of fast motility showed a significant decrease from spring toward summer and fall ( P < .001) with recovery noticed during the winter. As well, the highest percentage of normal sperm morphology was observed during the winter months.
Conclusion
Seasonal sperm pattern seems to be a circannual-rhythmic phenomenon. The winter and spring semen patterns are compatible with increased fecundability and may be a plausible explanation of the peak number of deliveries during the fall.
Male factor-related infertility is a rising phenomenon among infertile couples. There is an increasing effort to understand the factors that affect sperm quality expressed mainly by the standard semen analysis as it is defined by World Health Organization (WHO) guidelines. Apparently, the alterations in sperm analysis can be related to such physiologic factors as racial, seasonal, or even diurnal variations. Factors related to habits such as sedentary life style, obesity, smoking, alcohol, and drug intake, as well as the frequency of sexual intercourse, are known to be inversely related to sperm percent motility and normal morphology. Environmental hazards as well as occupational exposure have been mentioned as important factors acting to decrease sperm quality. Although pathologic findings such as varicocele or cryptorchidism are most probably related to abnormal sperm parameters, the major reasons leading to male infertility are not well defined.
Rotation of seasons as a phenomenon affecting breeding patterns in the animal world is well known. In humans, data regarding seasonal sperm variations were controversial. Andolz et al and Chen et al have found seasonal variations of sperm analysis, whereas others did not. Even though seasonal variations were noticed, there was no consensus on what season has the optimal sperm parameters.
Discovery of seasonal sperm variations may be of paramount importance, especially in couples with male-related infertility struggling with unsuccessful and prolonged infertility treatments. Hence, defining a seasonal sperm quality pattern may direct the fertility treatment to the optimal time frame, thereby increasing the chances of conception.
Therefore, we have undertaken the present study to undercover any possible seasonal sperm variation pattern, although taking into consideration as many semen parameters as we could, using a large computerized data base including a uniform sperm population aiming to diminish bias caused by possible underlying unknown pathologies that could affect the study results.
Materials and Methods
Study subjects
The study was performed between January 2006 and July 2009. It was approved by the institutional review board and is based on the computerized data base from the Clinical Andrology Laboratory at Soroka University Medical Center in Beer-Sheva, Israel, which is constantly under external quality assessment by UK NEQAS, SubFertility Laboratory, Saint Mary’s Hospital, Manchester, UK.
The 6455 semen samples included in the study were collected as part of the basic evaluation of 6447 couples referred to the Infertility Clinic at Soroka University Medical Center.
To avoid any possible derangement of the study results by underlying unknown effects causing severe oligozoospermia, the samples with sperm concentration below 4 million/mL as well as patients under hormonal treatments were excluded from the study. Therefore, the samples were classified according to sperm concentration: ≥20 × 10 6 /mL – Normozoospermic samples (4960) and 4–19.99 × 10 6 /mL – Oligozoospermic samples (1495). The results were analyzed separately for the Normozoospermic and the Oligozoospermic semen samples.
Because the warm Mediterranean climate can be roughly divided into a hot season: May–October, and a cold season: November–April, the Normozoospermic and Oligozoospermic groups of samples were examined by the season on the day of semen specimen production and again by the season 70 days before the sperm production day, which is during spermatogenesis.
At the final stage of the study evaluation and to explore the finest seasonal variations in human sperm, the Normozoospermic and the Oligozoospermic samples were analyzed according to the 4 classical seasons: spring (March, April, May); summer (June, July, Aug.); fall (Sept., Oct., Nov.); and winter (Dec., Jan., Feb.).
Laboratory analysis
Patients were advised to abstain from sexual activity for 1–3 days before the semen analysis, and the exact abstinence period was recorded on arrival at the laboratory. Samples were produced privately by masturbation into a sterile plastic container supplied by the pharmacy or the Andrology Laboratory and the specimens delivered to the laboratory between 30 and 60 minutes thereafter.
All sperm samples were analyzed using the Makler counting chamber (Sefi-Medical Instruments, Haifa, Israel) by the same laboratory technician for the following routine parameters: semen volume, sperm concentration, and percentage of total motility according to WHO guidelines. The analysis of the samples was completed by evaluation of the percent fast and slow motility sperm.
Sperm morphology was evaluated by a laboratory technician dedicated mainly to methodologic examination according to the strict Kruger-Tygerberg criteria. In addition, for some of the samples the evaluation of the acrosome index was performed using Menkeveld criteria. Both morphology and acrosome index were investigated among 100 stained sperm (Spermatic stain; FertilPro N.V., Beernem, Belgium) using a magnification of 1000. According to Menkeveld et al, a normal acrosome is clearly visible and well defined with a smooth oval configuration comprising 40% to 70% of the sperm head. The acrosome index is the percent of spermatozoa with a normal acrosome; the suggested cutoff is ≥10% of sperm with a normal acrosome.
Statistical evaluation
Univariate analysis was performed using χ 2 , Fisher exact test, Wilcoxon matched-pairs signed-ranks test, and 1 way analysis when appropriate.
Logistic regression analysis was performed to evaluate the effect of seasonal variations on the sperm parameters adjusted to the different confounding factors such as abstinence duration and age. Summer was used as the reference season.
Statistical analyses were performed using Statistical Programs for the Social Sciences (version 11.0; SPSS Inc, Chicago, IL) software programs. P < .05 was assumed as statistically significant.
Results
Only 6.6% of the Normozoospermic and 4.2% of the Oligozoospermic patients included in the study were above 45 years of age. The mean age (± standard deviation [SD]) for the Normozoospermic and the Oligozoospermic patients was 30.36 ± 6.68 and 29.72 ± 6.53 years, respectively.
To determine whether the seasonal sperm variations are related to the season on sperm production day or the season during spermatogenesis, we analyzed the data by season on sperm production day, and the data were reanalyzed according to the season 70 days before the sperm production day, to discover a possible seasonal effect on spermatogenesis.
Normozoospermic sample analysis
Among 4960 Normozoospermic semen specimens analyzed by the season on the day of sperm production, there was no seasonal effect on the semen volume, but the sperm concentration was found to be significantly higher ( P = .02) for the 2733 samples produced during the cold season vs the 2227 specimens produced during the hot season. Although the mean ± SD percent total motility was increased during the hot season compared with the cold season, namely 49.29 ± 18.88% and 39.64 ± 21.24% ( P < .0001), respectively, the increase was totally attributed to the slow motility sperm, ie, 30.03 ± 18.13% and 22.21 ± 18.12%. The percent ± SD of fast motility sperm was found to be significantly reduced during the hot season, ie, 3.93 ± 4.59% vs 4.83 ± 5.08% ( P < .0001) for the hot and cold season samples, respectively. As well, the mean percent (± SD) normal sperm morphology seems to improve during the cold season compared with the hot season, ie, 8.81 ± 6.06% and 8.24 ± 5.63% ( P < .01), respectively. Even if less noticeable, the above observed trends for the season-related differences in sperm parameters were preserved when the data were analyzed by the season of spermatogenesis.
Data analyzed by the season on sperm production day ( Table 1 ) revealed a gradual but consistent decrease in the values of sperm concentration from spring toward fall.
| Variable | Spring | Summer | Fall | Winter | P value |
|---|---|---|---|---|---|
| Volume, mL | 3.3 ± 1.68 (1152) | 3.27 ± 1.62 (1163) | 3.29 ± 1.63 (1145) | 3.25 ± 1.68 (1498) | NS |
| Concentration, 10 6 /mL | 71.95 ± 43.82 (1153) | 68.06 ± 40.67 (1163) | 64.66 ± 38.93 (1145) | 70.21 ± 42.29 (1499) | .001 |
| Motility total, % | 44.00 ± 21.49 (1153) | 49.34 ± 18.37 (1163) | 47.77 ± 19.31 (1145) | 36.88 ± 21.07 (1499) | .0001 |
| Motility fast, % | 4.03 ± 4.68 (468) | 3.45 ± 4.58 (448) | 4.92 ± 4.62 (526) | 5.03 ± 5.31 (730) | .0001 |
| Motility slow, % | 25.03 ± 18.89 (468) | 30.02 ± 17.71 (448) | 29.36 ± 18.62 (526) | 20.35 ± 17.45 (730) | .0001 |
| Morphology, % | 8.54 ± 5.61 (1140) | 8.30 ± 5.64 (1156) | 8.37 ± 5.83 (1136) | 8.91 ± 6.28 (1460) | .03 |
| Acrosome index, % | 8.75 ± 3.80 (463) | 9.22 ± 4.30 (449) | 8.83 ± 3.86 (453) | 8.90 ± 3.95 (647) | NS |
| Sexual abstinence, d | 4.89 ± 4.88 (1115) | 4.93 ± 3.74 (1134) | 4.97 ± 4.11 (1088) | 4.99 ± 5.70 (1450) | NS |
The 1153 spring produced samples demonstrated an average ± SD concentration of 71.95 ± 43.82 M/mL whereas the 1145 fall produced samples presented a mean value of 64.66 ± 38.93 M/mL ( P < .001), with a recovery of sperm concentration to 70.21 ± 42.29 M/mL observed among the 1499 winter samples.
The average ± SD percent of total sperm motility was found to be the highest among the summer and fall samples, namely, 49.34 ± 18.37% and 47.77 ± 19.31%, respectively. An abrupt and statistically significant reduction in total sperm motility to 36.88 ± 21.07% ( P < .0001) ensued during the winter months, whereas a recovery to 44 ± 21.49% was observed during the spring months. Interestingly, the dramatic increase in percent total sperm motility during the summer was entirely attributed to a gradual increase in the mean ± SD percent of slow motility sperm from a nadir value of 20.35 ± 17.45% during the winter to a peak value of 30.02 ± 17.71% ( P < .0001) during the summer months. At the same time, an inverse gradual process was observed for the mean ± SD percent of fast motility sperm, which drops from a peak value of 5.03 ± 5.31% during the winter to 3.45 ± 4.58% ( P < .0001) in the summer period. Sperm morphology was evaluated in 4892 of 4960 Normozoospermic samples ( Table 1 ). Similarly to the fast motility, the value of mean ± SD percent normal morphology was found to be higher among the 1460 winter samples with a value of 8.91 ± 6.28% compared with 1156 summer specimens with a value of 8.30 ± 5.64% ( P = .03).
Data analyzed according to the 4 seasons during spermatogenesis showed similar trends in all semen parameters, emphasizing even more the significantly higher mean ± SD percent of fast motility during the fall and winter months, ie, 5.21 ± 5.23% and 4.30 ± 4.91%, respectively, vs 3.76 ± 4.78% during the spring and 4.08 ± 4.17% during the summer months ( P < .001). In addition, an increased mean ± SD percent normal morphology during the winter compared with the spring values was noticed, ie, 8.84 ± 5.84% vs 8.07 ± 5.54% ( P < .001), respectively.
Oligozoospermic sperm sample analysis
The 1495 Oligozoospermic sperm samples were analyzed separately from the Normozoospermic sperm samples. Albeit the differences between the hot and cold season sperm parameters on the day of sperm production are less distinct, the trend of higher mean ± SD percent total sperm motility observed for the Normozoospermic samples during the hot season compared withthe cold season is preserved in the Oligozoospermic samples, ie, 31.23 ± 26.18% and 26.18 ± 18.93% ( P < .001), respectively. As detected for the Normozoospermic samples, the mean ± SD percent slow motility is increased during the hot season and reaches statistical significance in the samples by “Season during spermatogenesis”, ie, 14.16 ± 15.04% and 12.36 ± 13.44% ( P < .01) for the hot and cold seasons, respectively. Other parameters, such as percent fast motility and percent normal morphology, were not significantly affected by seasonal variations although showing higher values of normal morphology during the cold season.
When analyzed by 4 classical seasons: spring, summer, fall, and winter, the mean ± SD percent total motility was highest during the summer and fall ( Table 2 ), namely, 29.96 ± 19.28% and 32.29 ± 18.97%, respectively, and lowest during the winter: 24.06 ± 18.93% ( P < .0001). The mean ± SD percent low motility sperm reached peak values during the fall, ie, 16.61 ± 15.71% vs winter values of 11.38 ± 14.34%, but in contrast with the Normozoospermic samples, the variations in mean percent fast motility did not reach statistical significance. The percent ± SD normal morphology has reached peak value of 6.78 ± 5.82% during the spring, dropped to 5.61 ± 5.13% ( P = .02) during summer months, and recovered to 6.25 ± 5.07% during the fall. Similarly, the percent average ± SD acrosome index greatly resembled the above mentioned percent morphology pattern: ie, 7.80 ± 3.74% vs 6.69 ± 3.89% ( P = .002) for spring and summer months, respectively.
| Variable | Spring | Summer | Fall | Winter | P value |
|---|---|---|---|---|---|
| Volume, mL | 3.36 ± 1.88 (353) | 3.30 ± 1.81 (362) | 3.24 ± 1.78 (385) | 3.51 ± 1.92 (395) | NS |
| Concentration, 10 6 /mL | 10.98 ± 4.34 (353) | 10.92 ± 4.62 (362) | 10.93 ± 4.57 (385) | 11.21 ± 4.57 (395) | NS |
| Motility total, % | 28.52 ± 19.07 (353) | 29.96 ± 19.28 (362) | 32.29 ± 18.97 (385) | 24.06 ± 18.93 (395) | .0001 |
| Motility fast, % | 3.49 ± 3.61 (153) | 4.06 ± 4.71 (141) | 4.29 ± 4.(3175) | 3.91 ± 4.34 (213) | NS |
| Motility slow, % | 12.88 ± 14.30 (154) | 12.68 ± 13.03 (141) | 16.61 ± 15.71 (175) | 11.38 ± 14.34 (213) | .004 |
| Morphology, % | 6.78 ± 5.82 (346) | 5.61 ± 5.13 (360) | 6.25 ± 5.07 (385) | 5.88 ± 5.08 (386) | .02 |
| Acrosome index, % | 7.80 ± 3.74 (138) | 6.69 ± 3.89 (147) | 7.44 ± 3.90 (172) | 6.80 ± 3.65 (211) | .02 |
| Sexual abstinence, d | 4.03 ± 4.07 (340) | 4.39 ± 4.47 (353) | 4.29 ± 4.73 (367) | 4.23 ± 3.75 (384) | NS |
When analyzed by season of spermatogenesis, the noticed variations of sperm parameters were less statistically significant, showing an improved percent mean ± SD total motility during summer months, namely, 32.49 ± 19.13% and again an increased percent slow motility cells, ie, 16.05 ± 14.5%.
Logistic regression analysis
The logistic regression analysis performed on the study Normozoospermic samples using variables on the day of sperm production, such as patient’s age, days of abstinence, and the 4 seasons, has reaffirmed the significant improvement of fast motility ( Table 3 ) and sperm morphology during the winter season compared with the summer.
