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From * Vincent Memorial Obstetrics &
Gynecology Service, Andrology Laboratory and In Vitro Fertilization Unit,
Massachusetts General Hospital, Boston, Massachusetts; and
Environmental Health Department, Occupational
Health Program, Harvard School of Public Health, Boston, Massachusetts.
| Correspondence to: Dr Russ Hauser, Environmental Health Department, Occupational Health Program, Building 1 Room 1405, 665 Huntington Avenue, Boston, MA 02115. |
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Abstract |
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Key words: Epidemiology, sperm concentration, motility, morphology
Semen analysis is frequently used to evaluate male infertility. Assessment of semen quality is based on an evaluation of several parameters, including semen volume, pH, sperm concentration, sperm motility, and sperm morphology.
Seasonal variations in semen parameters have been reported in both fertile and infertile men (Levine et al, 1988; Saint Pol et al, 1989; Centola and Eberly, 1999). Saint Pol and coworkers (1989) found a significant seasonal variation in sperm count, with the highest sperm counts observed in late winter and early spring and the lowest in late summer. In age-adjusted analyses, Centola and Eberly (1999) found significant seasonal variation in the percentage of rapid motile sperm and progressive straight-line velocity, as well as in the percentage of tail defects, immature sperm, and tapered sperm.
Several studies have suggested that an increase in age is associated with a decline in semen parameters (Schwartz et al, 1983; Haidl et al, 1996; Centola and Eberly, 1999; Kidd et al, 2001). However, Paulson and coworkers (2001) identified an inverse association between age and total sperm count, but no age-related decrease in fertilization rate or a decrease in live birth rate in the oocyte donation model was found.
The present study was designed to evaluate seasonal variation and age-related changes in human semen parameters. In this retrospective study we reviewed data that were collected from men who attended the Vincent Memorial Andrology Laboratory of Massachusetts General Hospital (MGH) for semen analysis from 1989 to 2000.
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Materials and Methods |
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Because this was a retrospective review of an existing laboratory database, the subjects were not contacted for informed consent. The MGH Human Subject Committee Institutional Review Board approved this study.
Information was collected retrospectively on 551 semen analyses that were performed from July 1989 to December 2000. The first 4 semen analysis records were retrieved for each month of the study period and comprise the study population. Each record contained the patient's date of birth, date of semen analysis, and semen analysis results (volume, pH, sperm concentration, motility, progressive motility, and morphology). These data were used to derive the patient's age at the time of the semen analysis, as well as the season in which each semen analysis was performed. Winter was defined as December, January, and February; spring as March, April, and May; summer as June, July, and August; and fall as September, October, and November.
All duplicates were eliminated before selecting laboratory records for inclusion in the study database. No demographic information was available from the Vincent Memorial Andrology Laboratory records for this sample population.
Semen volume and pH data were available for 551 records. However, only 408 records had semen analyses performed using a computer-assisted semen analysis (CASA; Hamilton Thorn Research IVOS, Beverly, Mass); 143 records that were manually counted were excluded from the analyses for sperm concentration and motility. The CASA analyzer was used on semen analyses performed from July 1992 to December 2000. In December of 1992, the laboratory implemented the Tygerberg-Kruger strict morphology assessment, thereby changing from the World Health Organization (WHO) criteria for morphology assessment. Therefore, the morphology data were not included before December 1992 because the assessment criteria had been changed. A total of 388 records from December 1992 to December 2000 were included for evaluation of morphology variables. During the study period, 4 technologists performed the semen analyses.
Collection of Semen Samples
Semen was collected by masturbation into a sterile, widemouthed polystyrene
container in a private collection room in the hospital near the laboratory.
The recommended period of abstinence was a minimum of 48 hours but not longer
than 7 days. Semen specimens were allowed to liquefy for at least 20 minutes
in an incubator at 37°C and were analyzed within 60 minutes after the
samples were collected. A routine semen analysis was performed and included
several parameters: semen volume, pH, sperm concentration, sperm motility,
progressive motility, and sperm morphology.
Laboratory Evaluation
Semen Volume and pH—
The samples were well mixed in the original container and were not
vigorously shaken. The volume was determined using a disposable polycarbonate
serologic pipette. The sample color and viscosity were recorded. Semen pH was
measured within 1 hour of ejaculation. A drop of semen was spread evenly onto
pH strips (color pHast indicator strips pH 6.5–10.0; EM Science,
Gibbstown, NJ, made in Germany). This brand of pH strips was the only one used
during the period of data collection. After 30 seconds, the color of the
stained zone of the strip should have been uniform and was compared with the
calibration strip to read the pH. The pH strips were compared with known pH
standards of 7.0, 8.0, 9.0, and 10.0 (Buffer Solution, Fisher Scientific,
Pittsburgh, Pa).
Concentration and Motility—
All fresh samples were analyzed for sperm concentration and motion
parameters by CASA. Sperm concentration, percentage motility, and percentage
of progressive motility were determined. Setting parameters and the definition
of measured sperm motion parameters for CASA were established by
Hamilton-Thorn (frames acquired, 30; frame rate, 60 Hz; straightness
threshold, 80.0%; medium average path velocity cutoff, 25.0 µm/s; and
duration of tracking time, 0.38 seconds). Aliquots of semen samples (5 µL)
were placed into a prewarmed (37°C) Makler counting chamber (Sefi Medical
Instruments, Haifa, Israel). A minimum of 200 spermatozoa from at least 4
different fields was analyzed from each specimen. The percentage of motile
sperm was defined as WHO grades "a" (rapidly progressive 
25
µm/s at 37°C) plus "b" (slow/sluggish progressive with a
velocity 5 µm/s but <25 µm/s).
Morphology— Using the "feathering" method described in the WHO manual (1999), at least 2 slides were made for each fresh semen sample. The resulting thin smear was allowed to air dry for 1 hour before staining, which was carried out using a Diff-Quik staining kit (Dade Behring AG, Düdingen, Switzerland). Morphological assessment was performed with a Nikon microscope using an oil immersion 100x objective (Nikon Company, Tokyo, Japan). As the slide was examined from one microscopic field to another, all spermatozoa were assessed and scored as normal or abnormal. Head defects, midpiece defects, and tail defects were scored. Sperm morphology was determined using the strict criteria described by Kruger et al (1988). A minimum of 200 spermatozoa were counted from 2 slides for each specimen. Results were expressed as the percentage of normal spermatozoa, head defects, midpiece defects, and tail defects.
Statistical Analysis
To investigate whether there were differences in semen parameters across
season and associated with age, we performed regression analyses (SAS version
8.2, SAS Institute, Cary, NC). Winter was used as the reference season. We
also investigated month-to-month variations in semen parameters. For each
semen parameter, a separate multiple regression was performed. Semen analysis
parameters were entered into the models both untransformed and after square
root transformation because of their skewed distribution. Because the square
root–transformed results were similar to the untransformed results and
are simpler to interpret, only the untransformed results are presented. To
explore whether the semen parameters and age relationships were linear, age
was used as both a continuous and categorical variable (less than 30 years, 30
to 40 years, and greater than 40 years of age). P < .05 was
considered statistically significant.
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Results |
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Seasonal variations in semen quality are shown in
Table 2. The mean sperm
concentration in autumn (119.1 million/mL) was significantly lower than in
winter (157.9 million/mL; P < .05). The mean sperm concentrations
in summer (132.9 million/mL) and spring (135.9 million/mL) were also lower
than in winter, although this was not statistically significant. The seasonal
differences remained after adjusting for age as both a continuous and
categorical variable and after square root transformation of semen parameters.
The figure shows the month-to-month median sperm concentration across all 11
years of the study. The interquartile ranges (25th and 75th percentiles) are
used to describe the variability about the median. The spring, summer (except
for June), and fall months had lower median sperm concentrations than winter
months. Total sperm counts were significantly lower in fall than in winter
(Table 2). In addition, total
sperm counts in spring and summer were lower than in winter but this was not
statistically significant.
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There were also seasonal variations in sperm morphology parameters (Table 3). The mean percentage of normal morphology in winter (9.2%) was significantly greater than in spring (7.5%) and summer (7.0%), (P < .05) and nonsignificantly higher than in fall (8.7%). The mean percentage of head defects in summer (72.3%) and fall (74.0%) were significantly higher than in winter (68.6%; P < .05). The mean percentage of midpiece defects was significantly lower in fall (10.4) than in winter (14.0; P < .05. These seasonal differences remained after adjusting for age as both a continuous and categorical variable and after square root transformation of the semen parameters.
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Mean semen volume and pH were similar across seasons. Although the month-to-month median sperm motility was lowest in July and August and in November and December, there was no consistent seasonal pattern.
The relationships between age, which was used as a continuous variable in the regression models, and semen parameters are shown in Table 4. There was a significant age-related decline in volume (-0.38 mL/decade; P = .0002), sperm concentration (-25.4 million/decade; P = .02), total sperm count (-101.1 million/decade; P = .004), motility percentage (-5.12%/decade; P = .02), progressive motility percentage (-4.27%/decade; P = .004), total motile sperm (-36.6 million/decade; P = .001), normal morphology percentage (-1.06%/decade; P = .009), and an increase in percentage of tail defects (+2.46%/decade; P < .0001). Analyses in which age was used as a categorical variable did not show differences between categories for sperm concentration, motility, or morphology. This was not unexpected because the range of ages was narrow and few subjects were over 40 years old.
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Discussion |
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The present study shows a higher sperm concentration and total sperm count in winter than in other seasons and is lowest in fall. A similar finding was reported by Gyllenborg and coworkers (1999), who found lower sperm counts during summer and autumn than in late winter and spring among young Danish men. Two other retrospective studies (Politoff et al, 1989; Saint Pol et al, 1989) found peak sperm concentrations in the winter and spring, whereas the lowest sperm concentrations occurred in summer. A prospective study (Levine et al, 1992) reported reductions in semen quality during summer compared with winter. Levine (1994) conducted a semiquantitative meta-analysis of seasonality in human reproduction. In all 8 studies that reported sperm concentration, the values were lowest during summer. The highest values were noted during winter or spring. This is partially consistent with our findings of highest sperm concentration values in winter, although our study found the lowest values in fall followed by summer. Overall, our data are in agreement with previous reports of seasonal variation in sperm concentration, with winter having the highest concentration.
In the present study, the percentage of sperm with normal morphology was significantly higher in winter than in spring and summer. In addition, the percentage of sperm with abnormal head defects was significantly higher in fall and summer than winter. Centola and Eberly (1999) found similar variations, with a higher percentage of tapered forms in fall than in spring.
The present study is consistent with several other studies (Mortimer et al, 1983; Saint Pol et al, 1989; Centola et al, 1999) in that it did not find seasonal variations in semen volume or motility. In contrast, Reinberg and coworkers (1988) found a peak semen volume during April and May in prevasectomy patients.
The effects of temperature and hours of daylight may partially explain these statistically significant seasonal variations in sperm concentration (Levine 1994). Sperm production in humans is known to decrease when testicular temperature is raised by experimental techniques (Mieusset et al, 1987). Normal spermatogenesis requires a temperature 2–3°C lower than the rectal temperature (Snyder et al, 1990). The effect of higher temperature is manifested at a later time (about 90 days after exposure). This may partially explain why mean sperm concentrations were lowest in the fall but not in summer, and highest in winter. Chia and coworkers (2001) reported no significant month-to-month fluctuations in semen volume and sperm density among men who resided in the tropics, where there are minimal changes in temperature.
In the present study, semen volume, sperm concentration, total sperm count, sperm motility, progressive motility, total motile sperm, and normal morphology decreased as age increased. In addition, tail defects increased significantly as age increased. Significant decreases in semen parameters linked to aging were recognized by Centola and Eberly (1999), Schwartz et al (1983), and Haidl et al (1996). A review of the literature by Kidd et al (2001) on the association between age and semen quality and fertility status suggested that increased age was associated with a decline in semen volume, sperm motility, and sperm morphology, but not with sperm concentration.
The present study has several limitations. Although patients were told to abstain from ejaculation for at least 48 hours and no longer than 7 days before their clinic visit, we were not able to confirm this. Abstinence time data were not retrospectively available. The length of the period of abstinence may confound the relationship between season and semen parameters if, for instance, there was a seasonal variation in the frequency of sexual intercourse. Furthermore, if there was a relationship between age and length of sexual abstinence, the relationship between age and semen parameters may also be biased. However, because older men generally have less frequent intercourse, and therefore longer abstinence times, the relationship between age and semen parameters may by biased toward the null by not adjusting for abstinence time. We also lacked data on smoking history and other lifestyle factors, which may alter semen parameters. For bias to occur, these would need to be related to age or season, and be predictive of the semen parameters.
Although several technologists analyzed the semen samples over the study period, this is unlikely to bias our results. Because season and age-related associations are averaged temporally, intertechnologist variability is unlikely to account for our results. However, for temporal trend analysis of this data, intertechnologist variability may introduce bias. Although the Makler counting chamber was replaced several times during the study period, for the same reasons as noted above, this is also unlikely to account for the seasonal and age-related associations with semen parameters.
Because the study subjects were men who were partners in infertile couples, it may not be possible to generalize the results of the present study to the general population, which includes fertile men. However, if there are seasonal trends among men who attend infertility clinics, this would be important to determine because these men generally represent the subset of the population that is most vulnerable to reproductive insults. The inability to generalize does not alter the internal validity of the study.
In conclusion, the present study found both seasonal and age-related associations with several semen parameters in a sample of subjects from an infertility clinic population. These results are consistent with previously reported results. However, because this was a retrospective review of semen analysis data, we were unable to collect information on potential confounders, including abstinence time and lifestyle factors. Future analysis of a prospectively collected dataset will be used to evaluate seasonal and age related associations with semen parameters.
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Acknowledgments |
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Footnotes |
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References |
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Chia SE, Lim ST, Ho LM, Tay SK. Monthly variation in human semen
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Haidl G, Jung A, Schill WB. Ageing and sperm function. Hum Reprod.1996; 11:558 –560.
Kidd SA, Eskenazi B, Wyrobeck AJ. Effects of male age on semen quality and fertility: a review of the literature. Fertil Steril. 2001;75:237 –248.[Medline]
Kruger TF, Acosta AA, Simmons KF, Swanson RJ, Matta JF, Oehninger S. Predictive value of abnormal sperm morphology in vitro fertilization. Fertil Steril.1988; 49:112 –117.[Medline]
Levine RJ. Male factors contributing to the seasonality of human reproduction. Ann N Y Acad Sci.1994; 18;709 :29–45.
Levine RJ, Bordson BL, Mathew RM, Brown MH, Stanley JM, Starr TB. Deterioration of semen quality during summer in New Orleans. Fertil Steril. 1988;49:900 –907.[Medline]
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