Original Article
Differences in the Quality of Semen in Outdoor Workers during Summer and Winter
N Engl J Med 1990; 323:12-16July 5, 1990
- Abstract
- Abstract
Background and Methods.
In warm climates throughout the world, there is a deficit of births during the spring season. To determine whether this deficit might reflect a deleterious effect of heat on the male reproductive capacity during the previous summer, we obtained semen specimens in summer and winter from normal men who worked outdoors in the vicinity of San Antonio, Texas, and we performed automated semen analyses with an image-analysis system.
Results.
Pairwise comparisons among 131 men without azoospermia who contributed specimens in both summer and winter revealed significant reductions during the summer in sperm concentration, total sperm count per ejaculate, and concentration of motile sperm. The mean decreases in these values after adjustment for potential confounding characteristics were 32 percent (95 percent confidence limits, 28 and 44 percent), 24 percent (95 percent confidence limits, 18 and 43 percent), and 28 percent (95 percent confidence limits, 24 and 44 percent), respectively (P<0.0001). The lower a subject's average sperm concentration and motile-sperm concentration, the greater the reduction. We found no correlation, however, between the number of hours per day spent working during summer in settings without air conditioning and either the summer sperm concentration or the difference in concentration between summer and winter. Among the children of the men in the study whose wives were living near San Antonio during the year before they gave birth, a disproportionately low number were born during the spring.
Conclusions.
Semen quality deteriorates during the summer. This phenomenon may account at least in part for the reduction in the birth rate during the spring in regions with warm climates. (N Engl J Med 1990; 323:12–6.)
Media in This Article
Figure 1
Adjusted Births in Each Season, as a Percentage of Adjusted Total Births in All Seasons.Table 1
Characteristics of Seminal-Fluid Samples Obtained from 131 Men in Summer and Winter.*Article Activity
- Article
Demographers have repeatedly noted reductions in the birth rate during spring in nonequatorial regions with warm climates.1 2 3 4 Could summer heat nine months earlier have caused the quality of semen to deteriorate and result in a diminished rate of conception? Whereas homeostatic mechanisms should afford the female reproductive organs maximal protection against temperature changes in the environment, the thermoregulatory capacity of the scrotum is limited.5 Even mild scrotal warming can temporarily diminish the number of sperm ejaculated after two to three weeks.6 A decreased frequency of sexual intercourse could explain a reduced rate of conception during the summer, but the available evidence suggests that this does not occur.5 , 7 8 9
Retrospective studies in Houston of presumably fertile men before vasectomy10 and in New Orleans of men attending infertility clinics5 have indicated that the quality of semen may vary with the season. The highest values for sperm concentration and related measures were found in winter, and the lowest values in summer. To confirm and extend these findings and evaluate the role of potential confounding factors, we undertook a prospective study of semen quality during August 1986 and February 1987 among outdoor workers in San Antonio, Texas (average maximal daily temperatures, 35.9°C in July and August 1986 and 17.7°C in January and February 1987).11
Methods
Subjects
Men who worked outdoors at least four hours daily during the summer were recruited in the summer of 1986 through newspaper advertisements and asked to visit a medical clinic once or twice that summer (August) and twice the following winter (February). At each visit the men were interviewed, and they provided fresh semen specimens by masturbation into sterile plastic containers. A second visit was scheduled 7 to 14 days after the first visit in each season. Of 159 men enrolled during the summer of 1986, 135 (85 percent) returned (he following winter. The study protocol was approved by an institutional review committee, and each man gave informed consent for the study and was paid for his participation.
Questionnaires
At all clinic visits, the subjects were asked how long it had been since their most recent ejaculation (less than 24 hours or a specific number of days), whether during the past three months they bad had any febrile illness or used any medications or drugs (including recreational drugs), and whether they had collected their specimens Completely. To enhance the truthfulness of the reports about abstinence before the specimen collection, no instructions were given to the study subjects about what duration of abstinence might be considered desirable. At the first clinic visit of each season (summer and winter), information was also obtained about the type of work the man performed, the duration of employment, the number of hours per day spent outdoors on the job within the past three months, the presence of any urethral discharge or dysuria within the past month or any testicular pain within the past three months, and the ingestion of alcoholic beverages during that season. Information about the subjects' smoking and marital histories, the birth dates of all biologic children, and the place of residence of their wives during the year before the birth of each child was obtained during the winter clinic visits.
Laboratory Methods
The semen specimens were placed in an incubator at 37°C immediately after collection. After they were liquefied, the volume of seminal fluid was measured with wide-bore 5-ml or 1-ml pipettes. A 7-μl aliquot was pipetted into a warmed Makler chamber (SefiMedical instruments, Haifa, Israel) and transferred to a computer-assisted semen analyzer (CellSoft CASA, Cryo Resources, New York City). The sample was kept at 37°C on a warming stage while the prescribed microscopical fields were videotaped by one of two laboratory technicians. To minimize the opportunity for bias in the selection of fields, videotaping was begun above the upper right corner of the central grid, proceeding clockwise around the grid, and defocusing between fields.
A computerized analysis of the videotapes was performed with the following CellSoft index settings: 20 frames analyzed per field at an image-sampling frequency of 30 Hz; minimal sampling, 1 frame for percentage of motile sperm, 4 frames for sperm velocity and linearity of path (distance traveled in a straight line divided by the sum of the distances between each successive frame on the actual cell track and multiplied by 10), 7 frames for amplitude of lateral head displacement (displacement of the sperm head from the main path of the cell) and beat/cross frequency (flagellar beat frequency, as inferred from the rate at which the sperm head crosses the mean cell path); threshold velocity, 8 μm per second for velocity and percentage of motile sperm, 18 μm per second for amplitude of lateral head displacement and beat/cross frequency; maximal velocity, 110 μm per second; minimal linearity for amplitude of lateral head displacement and measurements of beat/cross frequency, 3.5; and permissible range of cell size, 5 to 25 pixels at a scale of 0.688 μm per pixel. A sufficient number of fields were analyzed in 84 percent of the specimens to provide results based on at least 200 sperm. For only 5.7 percent of specimens were fewer than 100 sperm analyzed.
When a subject provided two specimens in the same season, on average they were found to have virtually identical values for measures related to concentration if they were videotaped by the same technician, but not if they were videotaped by different technicians. For other measures, when such differences existed, they did not depend on the technician.12 Additional details of the equipment, the procedures used, and the reproducibility of the analyses have been published elsewhere.12 , 13
Statistical Analysis
Specimens from which videotapes were prepared more than two hours after the time of collection were not used in the analysis of the amplitude of lateral head displacement or beat/cross frequency. In addition, for the analysis of amplitude of lateral head displacement, two specimens with extreme values were excluded. Measurements of velocity and linear velocity for samples that were processed after a lapse of more than three hours were also excluded.12
Of the 135 men who contributed at least one specimen in summer and one in winter, 2 men who were azoospermic (i.e., without detectable sperm) in both seasons were excluded. Only specimens provided in summer and winter by the same man and videotaped by the same laboratory technician were compared, since the values obtained for the concentration-related measures of semen quality differed systematically between the two laboratory technicians who produced the videotapes.12 Among such specimens, those from 65 men (including 1 man with four specimens) were videotaped by one technician, and those from 2 men by the other. An additional 64 men who provided two samples in each season had had pairs of specimens videotaped by both technicians. The specimens from the two remaining men were videotaped by different technicians in summer and winter and were therefore excluded. At this point 442 specimens from 131 men remained for analysis. When two specimens were provided by an individual man in a season, the results were averaged.
Paired t-tests and analyses of variance were employed to assess the significance of any effect of season on semen quality within subjects. The cube-root transformations of the sperm concentration, the total sperm count per ejaculate, and the motile-sperm concentration were used to normalize these measures and stabilize their variance. Nonparametric analyses using Wilcoxon's signed-rank test were also performed on the original, untransformed variables. Since these led to the same conclusions as the parametric tests, only the results of the latter are reported.
In order to control for potential confounding characteristics, the analyses of variance were enhanced by the addition of measures of possible confounding. The following continuous variables were added as covariates: abstinence (specific number of days, or a half day if less than 24 hours) in the inverse scale, smoking (packs of cigarettes per day, or zero for nonsmokers and exsmokers), and drinking (number of drinks per month, or zero for nondrinkers). The following categorical measures were added as dummy variables according to season-specific yes-or-no categories: incomplete specimen collection, fever, symptoms of possible urogenital disease (urethral discharge, dysuria, and testicular pain), and drug and medication use.
Two-sided 95 percent confidence limits were obtained for the difference between the summer and winter values for each measure of semen quality, with use of standard errors obtained from the analyses of variance.14 , 15 Each confidence limit was then expressed as a percentage of the mean value for the measure in winter. For the analyses conducted in the cube-root scale, the confidence limits were reported after retransformation to the natural scale. The point estimates were always computed in the natural scale, however; thus, the confidence intervals for measures analyzed in the cuberoot scale may appear to be highly asymmetric around the point estimates.
A chi-square test with one degree of freedom was used to assess the significance of the proportion of spring births.
Results
A total of 442 semen specimens from 131 men without azoospermia were used in the analysis of the effect of season on semen quality. Sixty-five subjects contributed two summer and two winter specimens; 40 subjects, two specimens in the summer and one in the winter; 10 subjects, two in the winter and one in the summer; and 16 subjects, one specimen in each season. Of the 131 men, 126 were white, 4 were black, and I was Asian; 45 men (all white) had Spanish surnames. They ranged from 20 to 58 years of age (mean, 32). The study subjects were more likely than adult American men in general to be current smokers (49 percent vs. 32 percent) and to consume two or more drinks per day of beer, wine, or spirits (22 percent vs. 13 percent).16 During the summer of 1986, the subjects spent an average of eight hours per day on the job outdoors or in settings that were not air-conditioned. The most prevalent occupational categories were construction-related activities (33 percent), landscaping work (17 percent), driving a motor vehicle (8 percent), and maintenance work (6 percent).
The seasonal characteristics of the seminal-fluid samples from the 131 men are shown in Table 1Table 1
Characteristics of Seminal-Fluid Samples Obtained from 131 Men in Summer and Winter.*. The sperm concentration, total sperm count per ejaculate, and motile-sperm concentration for individual men were all significantly lower (P<0.0001) in summer than in winter (mean values for summer, 29, 23, and 26 percent lower, respectively, than those for winter). Reductions of similar magnitude were found among the specimens videotaped by each of the two laboratory technicians. The volume of seminal fluid, percentage of motile sperm, characteristics of sperm movement (velocity, linearity, linear velocity, mean amplitude of lateral head displacement, and beat/ cross frequency), and length of abstinence did not differ significantly between seasons.The values obtained in winter for sperm concentration, total sperm count per ejaculate, and motile-sperm concentration exceeded the summer values in 101 (77 percent), 79 (60 percent), and 94 (72 percent) of the 131 men, respectively. In the case of sperm concentration, the percentage difference between summer and winter ranged from an increase of 153 percent in summer to a decrease of 92 percent, with first-quartile, median, and third-quartile decreases of 4, 36, and 56 percent. The proportion of men with sperm concentrations under 20 million per milliliter increased from 1 of 131 (1 percent) in winter to 13 of 131 (10 percent) in summer.
Adjustments were made with linear models for the confounding influence of length of abstinence, incomplete specimen collection, cigarette smoking, consumption of alcoholic beverages, symptoms of possible urogenital disease (urethral discharge, dysuria, and testicular pain), fever, and drug and medication use, considered jointly. The magnitude of the reduction in sperm concentration and related measures during summer was altered little after such adjustments (Table 1). Analyses of variance with or without confounding variables revealed no significant correlation between the number of hours per day spent on the job during the summer in settings without air conditioning and the summer sperm concentration or the difference in sperm concentration between summer and winter.
When the season and potential confounding factors were entered into a linear model to assess their influence on semen quality, the season was the only significant predictor of concentration-related measures for an individual subject other than abstinence. When it was added to a model that already contained all other factors of interest, the season accounted for 21, 6, and 10 percent of the conditional variance in the untransformed sperm concentration, total sperm count per ejaculate, and motile-sperm concentration, respectively. The corresponding values for abstinence were 2, 6, and 4 percent. No other variable explained more than 1 percent of the conditional within-subject variance for these measures.
The extent of the summer decline in sperm concentration, total sperm count per ejaculate, and motile-sperm concentration was evaluated with respect to the mean of a man's summer and winter values, defined as his base line.17 The differences between summer (S) and winter (W), expressed as a percentage of the winter value ([S - W)/W] X 100%), were regressed against linear and nonlinear functions of the base line. These analyses confirmed the existence of a significant decline in summer for each concentration-related measure at all base-line values. In addition, they revealed a significant but weak trend toward increasing decline during summer with decreasing base-line sperm concentration and motile-sperm concentration.
Among the biologic children of the subjects, 73 had been born to subjects' wives who had resided within 250 miles of San Antonio during the year before child-birth. A histogram was constructed of the percentage of births occurring in each season, after the number of births was adjusted to account for the unequal length of the seasons (winter, 89.25 days beginning December 22; spring, 92 days beginning March 21; summer, 94 days beginning June 21; and fall, 90 days beginning September 23). In the absence of differences between seasons, approximately one quarter of the adjusted total births should have occurred during each season, assuming that temporal trends in fertility and migrations were negligible. Instead, as shown in Figure 1Figure 1
Adjusted Births in Each Season, as a Percentage of Adjusted Total Births in All Seasons., there was a notable but nonsignificant decline in the number of spring births (P = 0.06, one-sided).Discussion
Pairwise analyses of the semen specimens obtained in summer and winter from men who worked outdoors during the summer in the vicinity of San Antonio revealed substantial reductions in sperm concentration, total sperm count per ejaculate, and motile-sperm concentration during the summer. These reductions could not be explained by potential confounding factors. Moreover, they were observed despite the tendency of computer-assisted semen analysis to moderate extreme values for concentrations and thereby minimize the differences in concentration between summer and winter.18 , 19 Of a number of factors tested, the season was the only significant predictor of concentration-related measures of semen quality other than abstinence. It explained much of the conditional variance of sperm concentration within subjects, whereas abstinence did not, perhaps because the changes in the duration of abstinence for each man in our study tended to be small.
The deficit in spring births that occurs in non-equatorial warm climates worldwide was duplicated among the study subjects, linking the seasonal variation in the birth rate to a reduction in sperm concentration during the summer. The deterioration of semen quality in a population may affect fertility rales by increasing the time to pregnancy20 as well as the chance that pregnancy will not occur. In this study, the number of men with sperm concentrations below 20 million per milliliter and hence at higher risk of infertility21 was considerably larger during summer.
Prospective and retrospective studies of several populations in warm climates in the United States —San Antonio, Houston,10 and New Orleans5 — have demonstrated significant summer reductions in sperm concentration. Similar findings have been published recently from Lille, France,22 and Basel, Switzerland.23 Together with an earlier report from Edinburgh, Scotland,24 these latter studies suggest that sperm concentrations may be lower in the summer in cooler climates and make it less likely that heat alone can explain the entire phenomenon. Furthermore, since the birth rale is at its peak during the spring in northern Europe,2 , 25 not at its lowest point, as it is in the southern United States, the relation in Europe between the diminished summer sperm concentration and spring births is not immediately apparent. Seasonal variation in the social or psychological factors that influence the frequency of coitus9 , 26 may predominate in northern Europe, obscuring the effect of the reduced sperm concentration in summer on springtime births.
If environmental stimuli such as heat and light are causative factors, a summer decline in the sperm concentration might be expected to be most evident in men who are outdoors in summer during the middle of the day. Indeed, among 61 men attending a New Orleans fertility clinic, substantial deterioration in semen quality during the summer was identified only in those men whose workplaces were probably not air-conditioned — i.e., those who worked mostly outdoors.5 In our study we found no correlation between the number of hours per day spent on the job during summer in settings without air conditioning and the summer-time sperm concentrations or the differences in concentration between summer and winter. Since the study subjects worked outdoors at least four hours daily, they may have received sufficient environmental exposure to elicit a maximal biologic response.
There can no longer be any doubt that concentration-related measures of semen quality are reduced during summer. Like abstinence, the season is a significant predictor of sperm concentration, total sperm count per ejaculate, and motile-sperm concentration, and it should be taken into account in both the design and the analysis of clinical and epidemiologic studies.
We are indebted to the staff of Medical Research Associates, San Antonio, for assistance and the use of clinic facilities and to Yvonne A. Rokahr, R.N., for important contributions to the success of the field study.
Source Information
From the Chemical Industry Institute of Toxicology, Research Triangle Park, N.C. (R.J.L., R.M.M., M.H.B., M.E.H., K.S.B., K.L.M., P.K.W.); Medical Research Associates, San Antonio (C.B.C); the Haskell Laboratory for Toxicology and Industrial Medicine, E.I. du Pont de Nemours & Co., Newark, Del. (M.E.H., K.S.B.); and the Department of Safety Evaluation, Genentech, South San Francisco (P.K.W.). Address reprint requests to Dr. Levine at the Chemical Industry Institute of Toxicology, P.O. Box 12137, Research Triangle Park, NC 27709.
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Full Text37
Jnyder, Peter J., . (1990) Fewer Sperm in the Summer. New England Journal of Medicine 323:1, 54-56
Full Text
- Letters
