Advanced search
1,633
Views
11
CrossRef citations to date
0
Altmetric
Research Communications

Seasonal variation of human sperm cells among 4,422 semen samples: A retrospective study in Turkey

, , , , , & show all
Pages 379-386
Received 27 Mar 2016
Accepted 21 Jun 2016
Published online: 09 Sep 2016

ABSTRACT

We aimed to assess the possible presence of a seasonal pattern in three parameters of semen analysis: sperm concentration, morphology, and motility as a function of the time of ejaculation and sperm production (spermatogenesis) in normal and oligozoospermic men. This retrospective study included a consecutive series of 4,422 semen samples that were collected from patients as a part of the basic evaluation of the infertile couples attending the Reproductive Endocrine Outpatient Clinic of a tertiary women’s hospital in Ankara, Turkey, between January 1, 2012 and December 31, 2013. The samples were classified according to sperm concentration: ≥15 x106/mL as normozoospermic samples and 4 -14.99 x106/mL as oligozoospermic samples and seasonal analysis of the semen samples were carried out separately. When the data was analyzed according to the season of semen production, there was no seasonal effect on the sperm concentration. A gradual and consistent decrease in the rate of sperm with fast forward motility was observed from spring to fall with a recovery noticed during the winter. The percentage of sperms with normal morphology was found to be statistically significantly higher in the spring samples compared with the summer samples (p=0.001). Both normozoospermic and oligozoospermic semen samples appeared to have better sperm parameters in spring and winter. The circannual variation of semen parameters may be important in diagnosis and treatment desicions.

Abbreviations: WHO: World Health Organization; mRNA:messenger ribonucleic acid

Introduction

The impact of male factor on infertility has been widely studied over the last 20 years. Seasonal variations in conception and birth rates have drawn attention to the relationship between seasonal changes in sperm parameters. Changes in temperature and photoperiod were suggested to be partially responsible for the circannual variations observed in sperm parameters by various researchers [Chik et al.1992; Politoff et al.1989; Levine 1994].

Studies in rhesus monkeys implied that the seasonal variations in semen quality may be driven by a mechanism associated with the length of daylight [Wickings and Nieschlag 1980]. Melatonin regulation is related to the variations of the length of daylight and its positive effect on sperm motility [Ortiz et al. 2011]. As melatonin levels are low during the daytime, it shows a relatively high concentration during the winter days when exposure to daylight is short. Abnormally high levels of nocturnal melatonin were found in adult men with hypogonadism and oligoazoospermia [Wurtman et al. 1986]. Testes volume and thus plasma testosterone increases during short winter days most probably due to the shortened exposure to sunlight [Levine 1999]. Another factor influencing seasonal variations is speculated to be temperature changes. Normally, the temperature is at about 35°C inside the scrotum where the testes are located. This comparatively cool environment is necessary for the production of spermatozoa. When the testes are exposed to warm or cold ambient temperatures, scrotal skin provides temperature adjustments by contraction and relaxation via pampiniform plexus which controls the heat liberation and conservation mechanism.

In the animal kingdom, the breeding pattern is under the influence of seasonal rotation but data on humans concerning seasonal sperm variations remain controversial [Andolz et al. 2001; Chen et al. 2004; Menge and Beitner 1989; Ombelet et al. 1996]. Another important factor that leads to conflicting results is the parameter(s) selected for evaluation by different researchers. These mainly include sperm count, morphology, and motility. Moreover, individual habits such as hours of sleep affect the duration to exposure to daylight [Chik et al. 1992]. As a result, although seasonal variations in semen parameters have been reported in both infertile and fertile men there is no consensus on the season that is related with optimal sperm parameters [Levine et al. 1988; Centola and Eberly 1999]. Determining seasonal variation of sperm might be important for the management of couples with male related infertility who had unsuccessful and prolonged treatments. Therefore, defining a pattern of seasonal sperm quality may help to determine the optimal time frame for initiating infertility treatment in order to increase the chance of conception. After initiation of spermatogenesis it takes approximately 72 days for the sperm to reach the caudal epididymis where it is stored until ejaculation. The effect of seasonal changes at the time of sperm production (spermatogenesis) is not widely evaluated.

In this study, we assessed the possible presence of a seasonal pattern in sperm concentration, morphology, and motility. These three parameters of semen analysis were measured at the time of both ejaculation (semen production) and sperm production (spermatogenesis) in normal and oligozoospermic men.

Results

A total of 5,800 sperm samples were initially included in the study of which a total of 1,378 were excluded. The remaining 4,422 semen specimens were analyzed and 3,735 semen specimens were classified as normozoospermic. The mean age for the normozoospermic patients was 31.86±6.42 years. Sperm concentration did not exhibit a seasonal effect nor did age (p = 0.585). Total sperm motility was found to be the highest in the fall samples, but this value was only statistically significantly higher than the winter values (60.65 ± 20.28 vs. 58.54 ± 19.29 p = 0.026) but not statistically significant when compared with the summer and spring values. The overall increase in the percentage of total sperm motility during the fall was due to the increase in the percent of slow motility sperm from a low value of 12.17 ± 5.93% during the spring to a peak value of 36.01 ± 25.71% during the fall months. In the normozoospermic group, an increase of one year of age was correlated with a 1.03 fold decrease in percent fast forward motility sperm while the age had no effect on fast forward motility of the oligozoospermic group.

In the analysis of the data, a gradual and consistent decrease in the rate of sperm with fast forward motility was observed from spring to fall. The 930 spring produced sperm samples showed an average ± SD fast motility of 48.05 ± 18.29% whereas the 1,003 fall produced samples presented a mean value of 24.65 ± 20.03% (p = 0.001), with a recovery of fast sperm motility to 43.07 ± 19.70% observed in the 999 winter samples (Table 1). Similar to this change in the rate of sperms with fast forward motility, the percentage of sperms with normal morphology was found to be statistically significantly higher in the spring samples with a value of 15.55 ± 9.07 compared with fall samples (8.94 ± 7.73, p = 0.001) (Figure 1).When the data was analyzed by season of spermatogenesis (70 days before giving the sample), there was no significant difference between age and sperm production seasons (p = 0.117) and there was no seasonal effect on sperm concentration and total motility. Although, total sperm motility was similar between summer and winter samples, the rate of slow motility sperm was found to be significantly higher during summer compared with winter at the same time an inverse gradual drop was observed for the mean ± SD percent of fast motility sperm. This fell from a peak value of 46.69 ± 18.33% during the winter to 25.36 ± 25.47% (p = 0.001) in the summer period. The morphological evaluation of the normozoospermic samples showed similar trends as fast motility, the value of mean ± SD percent normal morphology was found to be higher among the 935 winter samples with a value of 15.05 ± 9.09% compared with 894 summer specimens with a value of 9.16 ± 7.87% (p = 0.001) (Table 2).

Table 1. Seasonal variations in normozoospermic sperm samples by the day of semen collection.

Table 2. Seasonal variations in normozoospermic sperm samples by the day of spermatogenesis.

Figure 1. The trends of sperm parameters in different seasons by the day of collection. In the normozoospermic group, the total sperm motility was found to be the highest in the fall samples and this value was only statistically significantly higher than the winter values, the percentage of sperms with normal morphology was found to be statistically significantly higher in the spring samples compared with the fall samples. In the oligozoospermic group, total motility was not affected by seasonal variations and the percentage of normal morphology reached a peak value during the spring and dropped during fall months and recovered during the winter.

The 687 oligozoospermic semen specimens were also analyzed according to the season of the semen production. The mean age for the oligozoospermic patients was 32.11 ± 6.22 years (Table 3). There was no significant difference between age and sperm production seasons (p = 0.333). Total motility was not affected by seasonal variation and the incidence of sperm with fast motility was highest during spring and winter (30.14 ± 16.67% and 24.59 ± 16.62%, respectively) and lowest during fall (13.08 ± 18.49%; p = 0.001). The percentage of sperm with slow motility showed similar trends in both oligo and normozoospermic groups as slow motile sperm reached peak values during fall, i.e., 35.07 ± 21.03% and 36.01 ± 25.71% vs. spring values of 20.45 ± 12.51% and 12.17 ± 5.93% (p = 0.001), respectively. Similarly, the percentage of normal morphology according to Kruger criteria results reached a peak value of 9.14 ± 7.02 during the spring, dropped to 5.06 ± 5.99 (p = 0.001) during fall months and recovered to 7.63 ± 6.02 during winter (Figure 2).

Table 3. Seasonal variations in oligozoospermic sperm samples by the day of semen collection.

Figure 2. The trends of sperm parameters in different seasons by the day of spermatogenesis. No seasonal effect was observed on total sperm motility both in normozoospermic and oligozoospermic samples. The morphological evaluation of the normozoospermic samples was found to be higher among the winter samples compared with summer specimens. In the oligozoospermic group, sperm with normal morphology were statistically significantly high in the winter samples.

When the oligozoospermic samples were evalauted according to the season of sperm production (spermatogenesis), there was no significant difference between age and sperm production seasons (p = 0.946). No seasonal effect was observed on sperm concentration and total sperm motility. The rate of fast forward motile sperm and sperm with normal morphology were statistically significantly higher in the winter samples (p < 0.001) while the percentage of slow moving sperm was highest in the summer samples (p<0.001) (Table 4).

Table 4. Seasonal variations in oligozoospermic sperm samples by the day of spermatogenesis.

A total of 31,096 deliveries have been recorded between January 1, 2012 and December 31, 2013 at the Etlik Zübeyde Hanım Women’s Health Teaching and Training Hospital, Ankara, Turkey. The highest number of deliveries, 9,264, was registered during summer whereas the lowest delivery rate, namely, 7,019, was noticed during winter months. There was a significant statistical difference between seasonal birth numbers (p = 0.001) (Figure 3).

Figure 3. Seasonal distrubution of deliveries during 2012–2013 at a tertiary women’s hospital in Ankara. A total of 31,096 deliveries have been registered between January 1, 2012 and December 31, 2013 at the Etlik Zübeyde Hanım Women’s Health Teaching and Training Hospital, Ankara, Turkey. The highest number of deliveries was recorded during the summer months demonstrating a highest conception rate during the previous fall whereas the lowest delivery rate was recorded during the winter months compatible with spring conceptions (p = 0.001). The columns represented 12 mounts of the year. Spring (March, April, May), Summer (June, July, August), Fall (September, October, November), and Winter (December, January, February).

Logistic regression analysis was performed for the 3,735 normozoospermic and 687 oligozoospermic samples using variables such as patient’s age and the season corresponding to the day of semen production. In both groups, a significant improvement of sperm parameters such as sperm morphology and fast forward motility was found during the spring and winter seasons compared with the summer season (Tables 5 and 6).

Table 5. Logistic regression analysis performed on 3,735 normozoospermic samples using variables such as patient’s age and the four seasons on the day of semen collection.

Table 6. Logistic regression analysis performed on 687 oligozoospermic samples using variables such as patient’s age and the four seasons on the day of semen collection.

Discussion

In the above study, we aimed to investigate the seasonal variations of sperm quality in a Mediterranean country and determine whether there is a circannual pattern. To our knowledge this is the first study to analyze the seasonal variations of semen parameters in Turkey. Moreover, seasonal variations in both normal and suboptimal semen samples were analyzed separately in order to reduce the possibility of bias related to the low sperm concentration.

In our study, sperm volume on the day of semen sample collection was significantly affected by the seasonal variations for both normozoospermic and oligozoospermic groups as peak volume was observed during winter. When the data was analyzed according to the season of sperm production (spermatogenesis), a peak sperm volume was observed in fall for both groups. Similarly, Reinberg et al. [1988] demonstrated a peak volume during spring.However, Centola and Eberly [1999] did not demonstrate a seasonal variation in semen volume, whereas Chen et al. [2004] reported no seasonal effect on the semen volume in accordance with the studies published by Levitas et al. [2013] and De Giorgi et al. [2015].

Some of the published studies reported a peak mean sperm concentration during the spring months [Andolz et al. 2001; Chen et al. 2004; Paraskevaides et al. 1988; Gyllenborg et al. 1999] and a lowest sperm count in summer [Krause and Krause 2002]. These researchers speculated that the changes in sperm count might be related to changes in the temperature and photoperiod as a temperature 2-3°C below the rectal temperature is required for normal spermatogenesis and sperm production is inhibited by increased temperature in the testes [Snyder 1990; Hermo and Clermont 1995]. The study of Yang et al. [2010], on gene expression profiles of remnant messenger ribonucleic acid (mRNA) in the summer and winter seasons confirmed molecular mechanisms of thermal effect on spermatogenesis but their functions in spermatogenesis are not clearly understood. However, Krause and Krause [2002] did not demonstrate a correlation with the sperm concentration and the increase in the temperature after analyzing the summer and winter sperm concentrations. In our study, the sperm concentrations did not show a season related significant change.

The results of the studies on seasonal variations in sperm motility are inconsistent [Centola and Eberly 1999; Saint Pol et al. 1989; Mortimer et al. 1983; Henkel et al. 2001]. One the one hand, Mortimer et al. [1983] showed no seasonal variation in sperm motility. On the other hand, Levitas at al. [2013] demonstrated a rhytmic circannual pattern for total sperm motility; the peak sperm motility was observed in summer while the lowest values were recorded in the winter months. Interestingly, the increase in total motile sperm cells in summer was attributed to the increase in the slow motile cells. In accordance with this study, DiGeorgi et al. [2015] found a higher sperm motility during summer. In another study, Centola and Eberly [1999] reported that the total sperm motility was highest in the fall and winter seasons. In our study, the total sperm motility was highest in fall and spring, namely, 60.65 ± 20.28% and 60.23 ± 19.16%, respectively, followed by summer and winter 59.56 ± 20.26% and 58.54 ± 19.29%, respectively; and similar to the study by Levine [1999], the highest value of total sperm motility in fall was attributed to the increase in slow motility sperm values. However, the study presented above also showed that fast motility sperm which may reflect an increase in fecundability was found to be significantly increased in the spring and winter samples.

In some studies, investigators reported no statistically significant seasonal changes in sperm morphology [Centola and Eberly 1999; Di Giorgi et al. 2015; Chen et al. 2003]. Chen et al. [2003] showed a higher median percentage of normal sperm morphology in winter as compared to spring. Levitas et al. [2013] also showed that the mean percent normal sperm morphology was the highest among the winter and spring samples and lowest in fall.

In the study presented above, the peak percent mean sperm morphology was present in spring followed by the winter season (p = 0.001) and our data also supported a seasonal pattern compatible with impaired sperm morphology during the fall months and a gradual increase in the samples given during the winter and spring months when the data were analyzed by the season of semen production. Besides the percentage of sperm with normal morphology, sperm with fast motility were also found to be higher in the spring and winter samples. This finding might imply the possibility of a higher success rate in infertility treatment during spring and winter.

To our knowledge, few publications analyzed the normal and subnormal sperm concentration samples separately to determine the seasonal effects. Levitas at al. [2013] found that oligozoospermic semen samples are different in some aspects from the normozoospermic sperm samples. While the highest percent mean sperm morphology were present in winter in normozoospermic samples, the oligozoospermic semen samples demonstrated the highest percent mean sperm morphology in spring and fall. Unlike normozoospermic samples, oligozoospermic sperm samples presented the highest values of all three motility parameters in the fall. However, there was no statistical difference between the percentage of fast motility sperm during different seasons in oligozoospermic samples

In contrast with Levitas et al. [2013], we found that both normozoospermic and oligozoospermic samples showed similar trends in sperm parameters such as percent mean fast motility and percent mean morphology. Both groups presented the highest percent mean sperm morphology (15.55 ± 9.07% and 9.14 ± 7.02%) (p = 0.001) and peak percent mean fast motility (48.05 ± 18.29% and 30.14 ± 16.67%) (p = 0.001) in spring. In accordance with these findings, analysis of the sperm parameters during the spermatogenesis period presented the highest mean sperm morphology and peak mean fast motility in winter. The association of seasonal variation between births and fecundity is not clear. Roenneberg and Aschoff [1990] defined circannual rhythmic phenomenon for human birth rates throughout the world. To test this hypothesis of seasonal fecundability, we analyzed the birth registry. A total of 31,096 deliveries have been recorded between January 1, 2012 and December 31, 2013 at the Etlik Zübeyde Hanım Women’s Health Teaching and Training Hospital, Ankara, Turkey. There was a significant statistical difference between seasonal births numbers (p = 0.001) (Figure 3). It has been reported that peak human fecundity is observed in late spring in many human populations around the world [Chen et al. 2004]. However, in this study, the delivery rate (N: 9,264, 30.78 %) was recorded during the summer months. Accordingly the highest conception rate occurred during the previous fall whereas the lowest delivery rate was recorded during the winter months compatible with spring conceptions (p = 0.001). Although the data support the view of seasonal variation of the sperm parameters in both normozoospermic and oligozoospermic samples, we found that there was no relation between seasonal pattern of sperm parameters and human conception. However, the seasonal effects, i.e., the circannual variation in sperm parameters on sperm parameters are different in normozoospermic and oligozoospermic individuals. The circannual variation of semen parameters may be important in diagnosis and treatment. Although both normozoospermic and oligozoospermic semen samples had better sperm parameters in spring and winter, further studies are required to determine whether a higher treatment success rate will be achieved for infertile patients during these seasons.

Materials and methods

This retrospective study includes a consecutive series of 4,422 semen samples that were collected from patients as a part of the basic evaluation of the infertile couples between January 1, 2012 and December 31, 2013 at the Etlik Zübeyde Hanım Women’s Health Teaching and Training Hospital Reproductive Endocrine Outpatient Clinic, Ankara, Turkey.

This study was approved by the Institutional Review Board and written informed consent was obtained from all patients for the use of data for scientific reporting purposes at the beginning of examination. Samples were obtained in privacy by masturbation into a sterile plastic container after a standard abstinence time of three days. Specimens were delivered to the laboratory within 15 min. The semen analyses were carried out using the Makler counting chamber (Sefi-Medical Instrument Ltd., Haifa, Israel) by the same laboratory technician to eliminate interobserver variation. After liquefaction, samples were put into the Makler counting chamber, the evaluation of the sperm parameters such as semen volume, sperm concentration, and percentage of total motility and also the evaluation of the percent fast and slow motility sperm were based on World Health Organization [WHO 2010] guidelines. Sperm morphological criteria were directly assessed by SQA-Vision (Medical Electronic Systems, LLC, Los Angeles, CA, USA) system automatically, in agreement with the strict criteria by Kruger-Tygerberg [Kruger 1988]. In order to prevent underlying unknown effects causing severe oligozoospermia interfering with the results, samples with a sperm concentration below 4 million/mL were excluded. The samples were classified according to sperm concentration: ≥15 x106/mL as normozoospermic samples and 4 -14.99 x106/mL as oligozoospermic samples. Seasonal time periods were grouped as follows: March-May as spring, June-August as summer, September-November as fall, and December-February as winter. Seasonal analyses of the semen samples were done separately for the two groups (normozoospermic and oligozoospermic). We collected only one sample from each patient. The two group morphological features of sperm samples were also examined using two different seasonal variables: the season on the day of obtaining the semen by masturbation and the season in which the sperm production (spermatogenesis) was presumed to initiate which is accepted as 70 d before the actual date of obtaining the sample.

Statistical evaluation

The Kruskal Wallis test was used to assess differences in semen parameters among four different groups and Mann-Whitney U test was performed to test the significance of pairwise differences using Bonferroni correction to adjust or multiple comparisons. Logistic regression analysis was performed to prevent a derangement of the results by confounding factors such as age of the patients and evaluate the effect of seasonal variations on the sperm parameters adjusted to the age. Summer was used as the reference season. Statistical analyses were performed using Statistical Programs for the Social Sciences (version 22.0; SPSS Inc, Chicago, IL, USA) software programs. p < 0.05 was assumed as statistically significant.

Declaration of interests

There is no conflict of interest.

Additional information

Notes on contributors

Runa Ozelci

Protocol development: RO, SY, SD; Manuscript writing: RO, BD; Project development: RO, SY; Data collection: FA, AO, DAC.

Saynur Yılmaz

Protocol development: RO, SY, SD; Manuscript writing: RO, BD; Project development: RO, SY; Data collection: FA, AO, DAC.

Berna Dilbaz

Protocol development: RO, SY, SD; Manuscript writing: RO, BD; Project development: RO, SY; Data collection: FA, AO, DAC.

Funda Akpınar

Protocol development: RO, SY, SD; Manuscript writing: RO, BD; Project development: RO, SY; Data collection: FA, AO, DAC.

Derya Akdag Cırık

Protocol development: RO, SY, SD; Manuscript writing: RO, BD; Project development: RO, SY; Data collection: FA, AO, DAC.

Serdar Dilbaz

Protocol development: RO, SY, SD; Manuscript writing: RO, BD; Project development: RO, SY; Data collection: FA, AO, DAC.

Aslı Ocal

Protocol development: RO, SY, SD; Manuscript writing: RO, BD; Project development: RO, SY; Data collection: FA, AO, DAC.

References

  • Andolz, P., Bielsa, A., Andolz, A. (2001) Circannual variation in human semen parameters. Int J Androl 24: 266271. [Crossref], [PubMed], [Web of Science ®][Google Scholar]
  • Chen, Z., Toth, T., Godfrey-Bailey, L., Mercedat N., Schiff I., Hauser, R. (2003) Seasonal variation and age-related changes in human semen parameters. J Androl 24:226-231. [Google Scholar]
  • Chen Z., Godfrey-Bailey L., Schiff I., Hauser, R. (2004) Impact of seasonal variation, age and smoking on human semen parameters: The Massachusetts General Hospital experience. J Exp Clin Assist Reprod 1:2. [Google Scholar]
  • Centola, G.M., Eberly, S. (1999) Seasonal variations and age related changes in human sperm count, motiliy, motion parameters, morphologyand white blood cell concentration. Fertil Steril 72:803-808. [Crossref], [PubMed], [Web of Science ®][Google Scholar]
  • Chik, C.L., Almeida, O.F., Libre, E.A., Booth, J.D., Renquist, D., Merriam, G.R. (1992) Photoperiod-driven changes inreproductive function in male rhesus monkeys. J Clin Endocrinol Metab 74:1068-1074. [PubMed], [Web of Science ®][Google Scholar]
  • De Giorgi, A., Volpi, R., Tiseo, R., Pala, M., Manfredini, R., Fabbian, F. (2015) Seasonal variation of human semen parameters: A retrospective study in Italy. Chronobiol Int 32(5):711-716. [Web of Science ®][Google Scholar]
  • Gyllenborg, J., Skakkebaek, N.E., Nielsen, N.C., Keiding, N., Giwercman, A. (1999) Secular and seasonal changes in semen quality among young Danishmen: a statistical analysis of semen samples from 1927 donor candidates during 1977-1995. Int J Androl 22:28-36. [Crossref], [PubMed][Google Scholar]
  • Henkel, R., Menkveld, R., Klein, M., Schill, W.B. (2001) Seasonal changes in human sperm chromatin condensation. J Assist Reprod Genet 18:371-377. [Crossref], [PubMed], [Web of Science ®][Google Scholar]
  • Hermo, L., Clermont, Y. (1995) How are germ cells produced and what factors control their production? In Handbook of Andrology. ed. Robaire, B., Pryor, J., Trasler, J. Allen Press, Lawrence, KS. pp. 1315. [Google Scholar]
  • Krause, A., Krause, W. (2002) Seasonal variations in human seminal parameters. Eur J Obstet Gynecol Reprod Biol 101:175–178. [Crossref], [PubMed], [Web of Science ®][Google Scholar]
  • Kruger, T.F., Acosta, A.A., Simmons, K.F., Swanson, R.J., Matta, J.F., Oehninger, S. (1988) Predictive value of abnormal sperm morphology in in vitro fertilization. Fertil Steril 49:112-117. [Crossref], [PubMed], [Web of Science ®][Google Scholar]
  • Levine, R.J., Bordson, B.L., Mathew, R.M., Brown, M.H., Stanley, J. M., Star, T.B. (1988) Deterioration of semen quality during summer in New Orleans. Fertil and Steril 49: 900907. [Crossref], [PubMed], [Web of Science ®][Google Scholar]
  • Levine, R.J. (1994) Male factors contributing to the seasonality of human reproduction. Ann N Y Acad Sci 709:29-45. [Crossref], [PubMed], [Web of Science ®][Google Scholar]
  • Levine, R.J. (1999) Seasonal variation of semen quality and fertility. Scand J Work Environ Health 25:34–37; discussion 7678. [Google Scholar]
  • Levitas, E., Lunenfeld, E., Weisz, N., Friger, Michael., Vardi, I.H. (2013) Seasonal variations of human sperm cells among 6455 semen samples: a plausible explanation of a seasonal birth pattern. Am J Obstet Gynecol 208:406. [Web of Science ®][Google Scholar]
  • Menge, A.C., Beitner, O. (1989) Interrelationships among semen characteristics, antisperm antibodies, and cervical mucus penetration assays in infertile human couples. Fertil Steril 51:486-492. [Crossref], [PubMed], [Web of Science ®][Google Scholar]
  • Mortimer, D., Templeton, A.A., Lenton, E.A., Coleman, R.A. (1983) Annual patterns of human sperm production and sperm quality. Arch Androl 10:1-5. [Taylor & Francis Online][Google Scholar]
  • Ombelet, W., Maes, M., Vandeput, H., Janssen M., Pollet, H., Fourie, F.L., et al. (1996) Chronobiological fluctuations in semen parameters with a constant abstinence period. Arch Andrology 37: 9196. [Taylor & Francis Online][Google Scholar]
  • Ortiz, A., Espino, J., Bejarano, I, Lozano, G.M., Monllor, F.,Garcia, J.F., et al. (2011) High endogenous melatonin concentrations enhance sperm quality and short-term in vitro exposure to melatonin improves aspects of sperm motility. J Pineal Res 50:132–139. [PubMed], [Web of Science ®][Google Scholar]
  • Paraskevaides, E.C., Pennington, G.W., Naik, S. (1988) Seasonal distribution in conceptions achieved by artificial insemination by donor. Br Med J 297:1309-1310. [Crossref], [PubMed], [Web of Science ®][Google Scholar]
  • Politoff, L., Birkhauser, M., Almendral, A., Zorn, A. (1989) New data confirming a circannual rhythm in spermatogenesis. Fertil Steril 52:486-489. [Crossref], [PubMed], [Web of Science ®][Google Scholar]
  • Reinberg, A., Smolensky, M.H., Hallek, M., Smith, K.D., Steinberger, E. (1988) Annual variation in semen characteristics and plasma hormone levels in men undergoing vasectomy. Fertil Steril 49:309–315. [Crossref], [PubMed], [Web of Science ®][Google Scholar]
  • Roenneberg, T., Aschoff, J. (1990) Annual rhythm of human reproduction. I. Biology, sociology, or both? Biol Rhythms 5:195–216. [Google Scholar]
  • Saint Pol, P., Beuscart, R., Leroy-Martin, B., Hermand, E., Jablonski, W. (1989) Circannual rhythms of sperm parameters of ferile men. Fertil Steril 51:1030-1033. [PubMed], [Web of Science ®][Google Scholar]
  • Snyder, P.J. (1990) Fewer sperm in the summer-it’s not heat,it’s... N Engl J Med 323:54-56. [Web of Science ®][Google Scholar]
  • WHO (2010) Laboratory Manual for the Examination and Processing of Human Semen, 5th ed. Geneva: World Health Organization. [Google Scholar]
  • Wickings, E.J., Nieschlag, E. (1980) Seasonality in endocrine and exocrine testicular function of the adult rhesus monkey (Macaca mulatta) maintained in a controlled laboratory environment. Int J Androl 3:87-104. [Crossref], [PubMed][Google Scholar]
  • Wurtman, R.J. (1986) Melatonin in humans. J Neural Transm Suppl 21:18. [PubMed][Google Scholar]
  • Yang, S.C.C, Lin, Y.S., Hsu, C.C., Tsai, M.H., Wu, S.C., Cheng, W.T.K. (2010) Seasonal effect on sperm messenger RNA profile of domestic swine (Sus Scrofa). Anim Reprod Sci 119:76–84. [Crossref], [Web of Science ®][Google Scholar]
 

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.