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The Journal of Clinical Endocrinology & Metabolism Vol. 89, No. 9 4397-4402
Copyright © 2004 by The Endocrine Society

Reproductive Function during Summer and Winter in Norwegian Men Living North and South of the Arctic Circle

Gunilla Malm, Trine B. Haugen, Trine Henrichsen, Cathrine Bjørsvik, Tom Grotmol, Thomas Sæther, Johan Malm, Yngve Figenschau, Lars Hagmar, Lars Rylander, Richard J. Levine and Aleksander Giwercman

Fertility Centre (G.M., A.G.), Scanian Andrology Centre, University Hospital MAS, Malmö, SE 205 02 Sweden; Andrology Laboratory (T.B.H., T.H., C.B., T.S.), Department of Gynaecology and Obstetrics, Rikshospitalet University Hospital, N-0027 Oslo, Norway; The Cancer Registry of Norway (T.G.), Institute of Population-Based Cancer Research, N-0310 Oslo, Norway; Department of Clinical Chemistry (J.M.), University Hospital MAS, SE 205 02 Malmö, Sweden; Department of Clinical Chemistry (Y.F.), University Hospital of North Norway, N-9038 Tromsoe, Norway; Department of Occupational and Environmental Medicine (L.H., L.R.), Lund University Hospital, Sweden; and Department of Health and Human Services (R.J.L.), National Institute of Child Health and Human Development, Bethesda, Maryland 20892

Address all correspondence and requests for reprints to: Aleksander Giwecman, M.D., Fertility Center, Scanian Andrology Centre, Malmö University Hospital, SE 205 02, Malmö, Sweden. E-mail: aleksander.giwercman{at}kir.mas.lu.se.


   Abstract
Top
 Abstract
Introduction
 Subjects and Methods
 Results
 Discussion
 References
 
Seasonal, daylight-dependent variation in human spermatozoa counts, with lowest values during summer, has been suggested. To test this hypothesis, we performed a longitudinal study of semen quality and reproductive hormone levels in Norwegian men living north and south of the Arctic Circle. An ejaculate and a serum specimen were obtained both in summer and in winter from 92 volunteers in Tromsoe (69° north latitude) and 112 in Oslo (60° north latitude). Semen analyses were performed, and serum was assayed for FSH and inhibin B. The median spermatozoa concentration in Tromsoe after adjustment for abstinence period length was 49 x 106/ml in summer and 54 x 106/ml in winter. Corresponding values for Oslo were 59 x 106/ml and 54 x 106/ml. The seasonal differences in spermatozoa concentration were not statistically significant, nor were significant differences observed in median total spermatozoa count, semen volume, percentage progressive motile spermatozoa, or FSH. In Tromsoe, but not Oslo, inhibin B concentration was slightly, but significantly (P = 0.02) higher in winter than summer (229 ng/liter vs. 223 ng/liter).

The length of the daylight period may have a slight impact on hormonal markers of spermatogenesis but does not cause substantial changes in spermatozoa numbers and motility.


   Introduction
Top
 Abstract
 Introduction
Subjects and Methods
 Results
 Discussion
 References
 
A SECULAR TREND for deterioration in male reproductive function over the past 50 yr, including declining sperm counts, has been suggested (1, 2, 3). Factors related to the environment, lifestyle, and genes may have a significant impact on semen parameters and thereby on the fertility of the male (4). Elucidation of these factors is of clinical as well as epidemiological importance. In the Western world, infertility is experienced by 15% of couples (5, 6). A better understanding of mechanisms controlling male reproductive function is crucial for diagnosis and treatment of male infertility (7) and for proper evaluation of semen data in epidemiological studies (8).

Several reports have indicated that spermatozoa concentration is subject to significant seasonal variation, with highest spermatozoa counts during winter and early spring and lowest spermatozoa number in summer and early autumn (9, 10). The assumption of circannual variation in spermatozoa output has been based mainly on cross-sectional retrospective studies (11, 12). Two prospective studies in which samples were delivered by the same individual in different seasons (9, 13) concluded that spermatozoa counts are lower during summer compared with winter. It has, therefore, been suggested that, similar to the animal world, in humans a variation is driven by an inherent circannual clock reset annually by seasonal changes in the length of daylight (14, 15). An important role in this regulatory mechanism has been assigned to the light-controlled secretion of melatonin (15).

Studies on seasonal variation in human semen quality have been conducted in the Northern Hemisphere, south of the Arctic Circle but not north of it where there are approximately two months of total darkness during winter and a corresponding period of 24 h daylight during summer. If spermatozoa production is directly related to the length of the daylight period, a higher degree of seasonal variation in spermatozoa counts is expected to be found in men living north of the Arctic Circle. To test the hypothesis of daylight-dependent seasonal variation in semen quality, we performed a study of reproductive function in Norwegian men living in Tromsoe (69° north latitude), 348 km north of the Arctic Circle (67° north latitude) and Oslo (60° north latitude) 739 km south of the Arctic Circle. Furthermore, because semen parameters are subject to considerable intra-individual variation, two serum markers of spermatogenesis that are less variable, FSH and inhibin B, were also measured.


   Subjects and Methods
Top
 Abstract
 Introduction
 Subjects and Methods
Results
 Discussion
 References
 
Subjects

The participants were recruited by advertising on radio and in local newspapers. Individuals who were 19–40 yr old, had lived in the respective area for a minimum of 1 yr before the start of the study and were to remain in that area during the year of the study (except for 5 wk holiday), were included. A total of 207 men were recruited, 93 from Tromsoe and 114 from Oslo (Fig. 1Go). Among those who delivered the first semen sample, 92 in Tromsoe and 112 in Oslo delivered a second ejaculate. Semen sample collections periods were based on the time of sunrise and sunset in the respective area, i.e. 2–3 months after the first day of the polar night (November 28) and polar day (May 18) in Tromsoe and a corresponding number of days after the solstices in Oslo (December 21 and June 21). The first sample collection period was in summer and the second in winter: in Tromsoe, July 30 to August 10, 2001, and January 21to February 1, 2002 (73–84 d and 55–66 d after the first polar day and the first polar night, respectively), and in Oslo, September 3 to September 14, 2001, and March 4 to March 15, 2002 (74–85 d and 73–84 d after summer and winter solstices, respectively) (Fig. 2Go). This delay was included to account for the duration of spermatogenesis and epididymal spermatozoa maturation.



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  		FIG. 1. A map showing the location of Tromsoe and Oslo in relation to the Arctic Circle.

 


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  		FIG. 2. Timing of the semen sampling in relation to the distribution of daylight hours in Oslo and in Tromsoe. The semen sampling periods are indicated by squares: T1 and T2, Tromsoe; O1 and O2, Oslo.

 
Blood samples drawn between 0800 and 1000 h were obtained for analysis of FSH and inhibin B. Because these two hormones are markers of early stages of spermatogenesis, the blood samples were drawn 50–60 d before obtaining the ejaculate, which means at the time of polar day and polar night in Tromsoe and within 2 wk after the solstices in Oslo.

The subjects were included after having given a written informed consent. They received 300 NOK (approximately 37 Euro) after delivering the first semen sample and 700 NOK after giving the second ejaculate. All filled in a questionnaire concerning reproductive history (e.g. infertility, proven fertility, and genital disorders), smoking habits, and chronic or endocrine diseases that could influence their reproductive function. At the time of blood sample collection, we obtained information from each subject regarding the average time spent outdoors between 1300 and 1800 h (minutes per week) during the past 3 months (Table 1Go).


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  		TABLE 1. Background characteristics of subjects in Oslo and in Tromsoe

 
The study was approved by the Ethical committee of Lund University, Sweden, and Regional Committee for Medical Research Ethics, Southern Norway.

Semen analysis

A period of 2–3 d sexual abstinence was recommended before delivering a semen sample. The reported length of the abstinence period was recorded in each case. The samples were obtained at the laboratory by masturbation and analyzed according to recommendations of the World Health Organization (16). The volume of semen was estimated by weighing. The spermatozoa concentration was determined with an improved Neubauer hemocytometer after dilution of the ejaculate using positive displacement pipettes.

For motility assessment, a drop of ejaculate was placed on a slide mounted on a heated stage (37 C). The movements of 200 spermatozoa were scored as rapid progressive motility (A), slow or sluggish progressive motility (B), nonprogressive motility (C), and immotility (D) (16). Two laboratory technicians performed examination of the ejaculates both in Tromsoe and Oslo. In each case, the same technician examined summer and winter samples obtained from a particular subject. The interobserver coefficient of variation was 9% for concentration and 5% for the motility assessment.

Hormone analysis

Circulating levels of FSH were measured on an automated fluorescence detection system. Intra- and interassay variation was less than 4.0 and 7.5%, respectively. Inhibin B levels were assessed using a specific immunometric assay (17), with a detection limit of 15 ng/liter and intra and interassay variation coefficients of less than 7%. All samples were measured in the same assay.

Background characteristics

The men were between 19 and 40 yr old. The median (interquartile range) age was 26 (24, 25, 26, 27, 28, 29, 30, 31, 32) yr in Oslo and 30 (26, 27, 28, 29, 30, 31, 32, 33, 34) yr in Tromsoe. The median length of the abstinence period was 3.0 d (range, 0.5–10). More detailed background characteristics are given in Table 1Go.

Statistical analysis

The appropriate number of participants in each of the two cities was, by an a priori power analysis, calculated to be 100. This sample size provided a statistical power of 0.80 to detect, at each of the two locations, a seasonal change in spermatozoa concentration of 10 x 106/ml, with a statistical significance of 0.05 (two-sided). The SD of the expected seasonal difference in either of the two cities was set equal to 25 x 106/ml based on repetitive sampling of 12 spermatozoa donor candidates at the Malmö University Hospital.

To control for the variation in the abstinence period, various multiple regression models based on different transformations of the semen variables were explored. However, a satisfactory fulfillment of the assumptions, assessed by residual analysis and partial regression plots, was difficult to achieve. Therefore, previous recordings of spermatozoa samples from 548 healthy young men from Norway and Sweden (18, 19), were classified (groups 1–4) according to their abstinence period and categorized as follows: ≤2 d, >2 and ≤3 d, >3 and ≤4 d, and >4 d. Within each category, the median values of semen volume, spermatozoa concentration, and spermatozoa count were used to establish the respective category’s relationship to the abstinence period, using period 2 (>2 and ≤3 d) as reference (=1.00). For spermatozoa concentration, the estimated relative values were 0.72, 1.28, and 1.56 for groups 1, 3, and 4, respectively. For total spermatozoa count, the corresponding values were 0.72, 1.28, and 1.55. Finally, the correction factors for semen volume were 0.97, 1.01, and 1.01. By means of these independent correction factors, the spermatozoa concentration, spermatozoa count, and semen volume values of group 1 were adjusted upward, whereas those of groups 3 and 4 were adjusted downward.

Seasonal differences in both regions were evaluated by means of the Wilcoxon signed rank test, each individual serving as his own control. Spearman’s rank correlation coefficient was applied to estimate the association between average afternoon time spent outdoors during the past 3 months (minutes per week) and the reproductive parameters. Separate calculations were performed for summer and winter samples. Seasonal differences were also evaluated for the quartiles of subjects with the greatest or least afternoon time spent outdoors. All tests were two sided, and a P value < 0.05 was considered as statistically significant.


   Results
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
Discussion
 References
 
Semen characteristics

The median (range) spermatozoa concentration among men living in Tromsoe after adjustment for abstinence was 49 (3.0–240) x 106/ml in summer and 54 (0.0–210) x 106/ml in winter. The corresponding values for Oslo were 59 (2.0–290) x 106/ml in summer and 54 (3.0–280) x 106/ml in winter. Summer-winter differences were not statistically significant at either location, nor were they significant when subjects from both cities were analyzed as a single group (data not shown). Summer and winter levels of semen volume, total spermatozoa count, and motility also did not differ significantly at both locations (Table 2Go).


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  		TABLE 2. Median (range) values for reproductive parameters in summer and winter in 112 subjects from Oslo and 92 subjects from Tromsoe

 
Hormone levels

In Tromsoe, the median (range) concentration of inhibin B was 223 (41.0–458) ng/liter in summer and 229 (54.0–494) in winter (P = 0.02). Seasonal differences in inhibin B concentration in Oslo were not significant, nor were the seasonal differences in FSH levels in any of the cities.

Impact of outdoors stay

In Tromsoe at summer sampling, the number of minutes an individual had stayed outdoors between 1300 and 1800 h during the past 3 months was negatively correlated to the serum level of inhibin B ({rho} = –0.24; P = 0.02) but not to any other serum or semen parameter. In Oslo, during both sample collection periods, and in Tromsoe, during the winter sampling, no statistically significant correlations were found between the number of outdoor minutes and any of the reproductive parameters. There was in neither Oslo nor Tromsoe any significant summer-winter differences in semen parameters, when the quartiles of subjects with the highest and the lowest outdoors stay during the summer time were compared (data not shown).


   Discussion
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
References
 
This study was designed to investigate whether extreme differences in the length of daylight affect semen quality in humans. No significant seasonal variation in spermatozoa concentration, total spermatozoa count, semen volume, or spermatozoa motility was found in men living either north or south of the Arctic Circle. The insignificant effect of daylight on spermatogenesis was supported by hormone analyses showing only slightly higher inhibin B values during wintertime in Tromsoe but no summer-winter difference in FSH levels at this location or for any of the two hormones in the Oslo study group.

An important question is whether the timing of sampling was appropriate to detect daylight-dependent seasonal variation in spermatozoa characteristics. The periods for semen sample collection were based on the results of previous cross-sectional studies that indicated that the maxima and minima in the spermatozoa counts occurred 2–3 months after solstices (20). Because spermatogenesis and subsequent epididymal maturation require approximately 11 wk, the timing of spermatozoa count peaks and troughs might indicate that the length of daylight affects the early stages of spermatogenesis. Apart from assessing semen parameters, we therefore measured levels of FSH and inhibin B, markers of early stages of spermatogenesis that have been shown to correlate with the concentration of spermatozoa (21). However, our study design should have permitted detection of daylight-dependent differences even if later stages of spermatozoa production were affected. Thus a seasonal difference in spermatozoa concentration should have been seen at least in Tromsoe, because during the entire 11-wk period before sample collection, the daylight period was at least 19 h longer in summer than in winter.

Despite extreme variations in the light conditions, as seen in Tromsoe, we could not detect any strong effect on spermatozoa count. Our sample size of approximately 100 men in both cities was sufficient to detect, with 80% probability, a difference of at least 10 x 106/ml between summer and winter. Previous studies, performed in locations with less extreme seasonal variation in the length of daylight, reported a circannual variation in spermatozoa concentration of approximately 20 x 106/ml (11, 12, 22, 23, 24, 25, 26). However, our results do not exclude a less pronounced seasonal variation in spermatozoa numbers. In contrast to the results obtained in Oslo, the median concentration in Tromsoe, although not statistically significant, was 10% higher during wintertime. This small difference was in accordance with a statistically significant but subtle increase in inhibin B concentration.

Potential confounders related to the methodology of seminal analysis and to selection in the subject recruitment should be taken into consideration. Spermatozoa concentration is highly dependent on the length of the abstinence period (27). In our analysis, all spermatozoa numbers and volume were adjusted for the actual period of abstinence. We attempted to recruit males representing the general population, but it has been shown that control populations recruited for occupational and environmental studies of male reproductive function may have an overrepresentation of men suffering subfertility (8). Because of the low percentage of dropouts, and because each individual served as his own control, such selection bias is less likely to have affected the results of the study. Furthermore, the prevalence of infertility problems among the included subjects was at the same level as reported for the Western countries (5), and their sperm count levels were comparable with those of the general Norwegian population (19).

Using the same laboratory equipment in both Oslo and Tromsoe minimized the importance of interlaboratory variation. The same two technicians examined the samples in both cities, and the same technician examined both semen samples from each individual.

The previous assumption of seasonal variation in spermatozoa characteristics is based on a number of cross-sectional and two longitudinal studies, all performed at the Northern Hemisphere, south of the Arctic Circle (9, 13, 25, 28). Spermatogenesis is a highly temperature-sensitive process, which is why it was hypothesized that heat might account for the reduction in spermatozoa counts during summer (3, 13, 24). However, because the summer-winter gradient was as pronounced in outdoor workers as in subjects working in air-conditioned environments, the length of daylight was thought to be a more plausible explanatory factor (13). Our results do not fit with this hypothesis. Looking for an explanation for this discrepancy, it should be kept in mind that not all cross-sectional studies were able to show a seasonal variation in spermatozoa characteristics (19, 29). The data collection in most previous studies was not originally aimed at disclosing such variation, but the surveys were performed for other reasons, with seasonal variation being a chance finding (11, 25). One can therefore not exclude some publication bias toward reporting on the season-related data, if a statistically significant variation was found. Furthermore, unlike this study, the majority of previous reports have included subjects selected either because of infertility (10) or because they were proven fertile as partners of pregnant females (31) or vasectomy candidates (26). Interestingly, in two recent studies of Danish men, a seasonal variation was found in partners to pregnant females (31) but not in military conscripts, representing the general male population (19).

Other potential confounders are the intensity of indoor illumination and seasonal variation in lifestyle. Most data on the effect of indoor illumination on the endocrine system are related to melatonin secretion. Although not completely conclusive, it seems obvious that indoor illumination has far less effect than daylight on melatonin secretion (32). Furthermore, men living under normal conditions in Tromsoe were found to have the highest mean levels of melatonin in January and the lowest in June (33). These findings demonstrate the effect of changes in the length of the daylight period on the endocrine system despite exposure to indoor illumination. We also found a negative correlation between afternoon time spent outdoors and inhibin B levels during summer in Tromsoe. There was, however, no difference in seminal parameters in subgroups with greatest or least afternoon exposure to daylight, indicating that variation in the length of the time period outdoors plays only a minor role for sperm characteristics.

Furthermore, we cannot exclude the possibility of an adaptation to the extreme conditions of light and dark to which their study groups are exposed, which might mask the endogenous circannual pattern apparent in men living in areas with lesser light variation. However, there are no data in the literature to support such a hypothesis. Additionally, the fact that a slight (but statistically significant) increase in the winter levels of inhibin B was seen in Tromsoe and not in Oslo seems to contradict such hypothesis.

Because of the longitudinal design, each individual served as his own control. No corrections were made for possible seasonal intra-individual variation in lifestyle. The association between semen parameters and cigarette smoking or alcohol consumption, unless excessive, is very weak (34, 35), if indeed it exists. A recent cross-sectional study from Tromsoe indicated no annual variation in smoking habits and suggested that peak alcohol consumption occurred in May (36). Given that alcohol consumption has detrimental effects on semen quality and assuming peak sperm concentrations in winter, such circannual variation in alcohol consumption would tend to increase, not decrease, a summer-winter difference in sperm concentration

Two longitudinal studies reporting on declining spermatozoa counts during summer (9, 13) were performed in Texas and Louisiana. Their results fitted well with the seasonal variations in birth rates in these regions. Because spermatozoa concentration is an important determinant of male fertility (37), the circannual variation in spermatozoa counts might be mirrored in corresponding fluctuations in birth rates 9 months later. However, even such a link could not be confirmed by our study. In Oslo and in Tromsoe, the highest numbers of births are reported during the spring and summer (data from Statistics Norway, Oslo, Norway), which should correspond to the highest sperm counts in the summer and fall. Therefore, we cannot exclude the possibility of regional trends in the seasonality of male reproductive function, regulated by genetic, environmental, social, and/or nutritional factors.

Our findings should also be seen from an evolutionary perspective. Thus, although season-dependent variation in semen parameters has been well documented in other primates such as rhesus monkeys (38) and in other seasonal breeders such as rams (39), it does not seem to be a universal phenomenon in humans.

In conclusion, in a longitudinal study of 204 men living north or south of the Arctic Circle, we did not observe differences in semen volume, spermatozoa counts, or motility of spermatozoa between summer and winter. This indicates that even this large seasonal variation in the length of the daylight period does not affect human sperm characteristics.


   Acknowledgments
 
We gratefully acknowledge Statistics Norway and Department of Clinical Research, University Hospital of North Norway, Tromsoe, for valuable information and help.


   Footnotes
 
This study was supported by grants from Swedish Research Council (Grant 521-2002-3907) University Hospital MAS Foundation in Malmö, Gunnar Nilssons Cancer Fund, Crafoordska Fund, Ove Tulefjords Fund, Swedish governmental funding for clinical research, and Foundation for Urological Research.

Received March 2, 2004.

Accepted June 16, 2004.


   References
Top
 Abstract
 Introduction
 Subjects and Methods
 Results
 Discussion
 References
 

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Hum. Reprod., July 1, 2005; 20(7): 1921 - 1927.
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