Home | Archive | AJA @ Nature | Online Submission | News & Events | Subscribe | APFA | Society | Links | Contact Us | 中文版 |
 |
Seasonality in human semen quality of smokers and non-smokers: effect of temperature
Robert Knzle1, Michael D. Mueller1, Alexander W. Huber1, Heinz Drescher2, Nick A. Bersinger1
1Department of Obstetrics and Gynaecology,
University of Berne, Berne, CH-3010, Switzerland
2MCL Laboratories, Dudingen, Switzerland
Asian J Androl 2004 Sep; 6: 243-247
Keywords: sperm quality; seasonal temperature; fertility; smoking
Abstract
Aim: To analyse the possible effect of seasonal variation on semen parameters. Methods: The participants consisted of 1688 men attending the andrology laboratory between 1991 and 1997 for reduced fertility in the couple. Semen analysis was performed according to the WHO manual. The 84 individual months of the study period were each assigned to one of the three groups according to the average monthly outside temperature; Group A (temperature <4.4 ), Group B (4.4 - 13.3 ) and Group C (>13.3 ). Results: When comparing the different sperm parameters, the morphology was significantly better in Group C. However, when the smokers were analysed separately, this difference disappeared and significant seasonal variations were found in sperm density, total sperm count, motility and total motile sperm; they were deteriorated in the warmer season. In non-smokers, no such negative effect of increased temperature was observed. Conclusion: Sperm quality is influenced by seasonal factors. Increased environmental temperature, (maybe also light exposure) has an additional negative effect on the spermatogenesis in smokers, leading to reduced sperm quality in men with borderline fertility.
1 Introduction
Assessment of semen quality is based on the evaluation of several parameters, including semen volume, sperm density, total sperm count, sperm motility and sperm morphology. It is now accepted that these parameters can be influenced by various factors such as smoking [1-3], lifestyle [4] and high scrotal temperature[5], and may be also seasons of the year. Most studies performed in temperate climates showed a minimum of the sperm count in summer and higher densities in winter or spring [6-9]. However no significant differences in other semen parameters could be observed as a function of the month of the year in other studies. Chia et al [10] did not see a significant seasonal variation in semen volume and density of men who live in the tropics. Ombelet et al [11] examined seasonal variation in sperm count, motility and morphology without observing any differences in these parameters, neither did others find a circannian rhythm except a reduced motility in the spring [12]. Nevertheless, fluctuations in testicular temperature or changes in daily exposure to light may be responsible for seasonal variations of sperm quality, which could be induced by an endogenous biological clock occurring annually by changes in the length of daylight. The causal mechanisms of this process are far from being fully understood .
Seasonal variation in sperm quality may result in lower conception rates in summer as one of the possible factors being responsible for a reduced birth rate in spring[13]. In this study we aimed to investigate whether semen quality was subject to circannian rhythmicity and if smoking habits had an effect on this variability in a part of the world with a temperate climate, but with a wide range of temperatures, such as Western Europe.
2 Materials and methods
2.1 Participants and sample collection
Men attending the andrology laboratory between 1991 and 1997 for reduced fertility in the couple were included in this retrospective study. Only the first sperm evaluation was taken into account in this analysis and samples from patients with azoospermia or having had vasectomy or vasovasostomy were excluded. Semen samples were collected by ejaculation into a special sterile container (Telast SA, Prverenges, Switzerland) after two to seven days of sexual abstinence. Most ejaculates were collected at the laboratory, but some at home and delivered immediately to the laboratory without allowing to cool. All analyses were performed within two hours.
A total of 1688 samples, with clinical data and smoking behaviour on record, fulfilled the criteria and were included in the study. All analyses were performed in the same laboratory (MCL) and no methodological changes were made during the study period.
2.2 Semen analysis
The semen analysis consisted in the determination of sample volume, sperm density, total sperm count, progressive motility, vitality and morphology as described by the WHO [14]. Total sperm count and total motile sperm were calculated from the observed data.
The sperm motility was assessed by computer assisted sperm analysis (CASA), using an ATS 20-J.C. analyser (Diffusion International, Fresnele, France) based on the principle of negative phase contrast microscopy. Oligozoospermic samples were manually analysed with a Makler chamber using an Olympus BH-2 microscope (Japan). The morphology was assessed under the microscope after staining with a kit based on fast green, eosin and thiacin (Diff-Quick, Dade Diagnostica, Switzerland). The laboratory continuously takes part in multicentre quality control trials.
2.3 Statistical analyses
The 84 individual months of the study period (1991 to 1997) were assigned to three groups according to the average monthly temperature in Berne, obtained retrospectively from the Swiss National Bureau of Meteorology (Liebefeld, Berne, Switzerland). Table 1 shows the average monthly temperatures observed during the collection period. The following temperature cut-offs between the groups were calculated in order to obtain three groups of an identical total time span (28 months each): Group A, less than 4.4 ; Group B, 4.4 - 13.3 ; and Group C, more than 13.3 .
Table 1. Average monthly temperature in during the study period (July 1991 to May 1997).
| Year |
1991 |
1992 |
1993 |
1994 |
1995 |
1996 |
1997 |
| January |
- |
-2.2 |
2.4 |
2.4 |
-0.4 |
0.1 |
-1.3 |
| February |
- |
1.0 |
-0.8 |
2.3 |
4.4 |
-0.5 |
4.0 |
| March |
- |
5.7 |
4.0 |
8.9 |
3.5 |
3.2 |
7.2 |
| April |
- |
8.3 |
9.7 |
6.7 |
8.7 |
9.0 |
7.8 |
| May |
- |
14.2 |
13.9 |
13.2 |
12.5 |
12.3 |
13.5 |
| June |
- |
15.2 |
16.5 |
16.5 |
14.8 |
16.9 |
- |
| July |
19.3 |
18.4 |
17.1 |
21.0 |
20.5 |
17.1 |
- |
| August |
19.3 |
20.4 |
17.8 |
19.5 |
17.6 |
16.7 |
- |
| September |
16.0 |
14.1 |
12.9 |
13.5 |
11.8 |
10.9 |
- |
| October |
8.0 |
7.8 |
7.7 |
9.4 |
120 |
9.3 |
- |
| November |
3.6 |
6.1 |
1.9 |
7.2 |
3.7 |
4.3 |
- |
| December |
-1.0 |
0.6 |
3.6 |
3.0 |
-0.1 |
-0.1 |
- |
Data were analysed by Student's t-test or, in case of significantly different standard deviations (predominantly for total sperm count), with the Welch's approximate test. A P value of 0.05 or less indicated a significant difference between two seasonal groups.
3 Results
The study sample consisted of 1688 participants of whom 1064 (63 %) were non-smokers. Group A (cold) consisted of 635 semen samples, Group B (medium), 522 samples and Group C (warm), 531 samples. The fraction of smokers was 38.5 % (n=240), 30.4 % (n=190) and 31.1 % (n=194) in temperature groups A, B and C, respectively. No significant associations were found between smoking habits and temperature groups.
When analysing the mean values of different sperm parameters as a function of the 3 groups, only the morphology showed significant differences (A vs. C and B vs. C) with higher values in Group C (Table 2). A similar trend was seen when comparing the non-smokers alone between these groups, with a significantly better morphology in Group C than in the others. When the smokers were analysed separately, the morphology was not significantly different, while significant seasonal variations were found for sperm density (A vs. C), total sperm count (A vs. C and B vs. C), motility (B vs. C) and total motile sperm (A vs. C) with lower values in C. Non-smoker semen donors in warmer months (C) were significantly younger than those recruited during the cold period (A) (Table2).
Table 2. Sperm parameters as a function of temperature. Group A (<4.4 ), B (4.4 - 13.3 ) and C (>13.3 ) in the total population, smokers and non-smokers. Data in meanSD.a Total motile sperm = total sperm countprogressive motility/100. bP<0.05 compared to smokers. eP <0.05, Group A versus Group C; hP<0.05, Group B versus Group C.
Characteristics
|
|
Total |
Non-Smokers |
Smokers |
| Number
(n) |
A |
635 |
395 |
240 |
| Age |
A |
|
33.9
5.7 b |
32.2
6.0 |
| Sperm
density |
A |
81.85.6 |
86.079.7 |
74.967.9 |
| Sample
volume |
A |
3.6
1.7 |
3.71.7 |
3.61.6 |
| Total
sperm count |
A |
282.2
278.4 |
295.9275.4 |
259.7
283.0 |
| Progressive
motility |
A |
39.5
16.3 |
39.716.1 |
39.116.7 |
| Total
motile sperma
(106) |
A |
111.4
45.4 |
135.7
148.5 |
119.5
146.4 |
| Morphology |
A |
23.0
14.7 |
23.815.1 |
21.2
14.0 |
| Vitality
(%) |
A |
46.1
18.5 |
46.318.5 |
45.818.4 |
Hence, a deleterious effect on sperm quality associated with the warmer season was observed in smokers only, i.e. sperm samples collected in the summer months were of a significantly reduced quality in the smoking population. This effect cannot be attributed to age, since the non-smokers were slightly older.
4 Discussion
A number of biological rhythms are known to exist in man, such as the rhythm of the pituitary response to luteinising hormone-releasing hormone (LHRH) and the circadian rhythm in the excretion of prolactin or steroid hormones. Some studies describe a chronobiological fluctuation in semen parameters with a decrease in semen quality during the summer months and an increase in winter and spring [7, 8, 15]. This seasonal rhythmicity may be induced by an endogenous clock which is influenced by seasonal changes in temperature or light exposure [13]; however the causal relations and mechanisms are not understood and the reported results are contradictory to some extent. Other studies did not find any seasonal variation in semen parameters [9, 11]. The lack of significant periodicity in these studies may be explained by the large variation in individual semen parameters in the population, which could also be influenced by external factors, such as length of abstinence, different smoking habits [1, 3], sedentary working style [5], varying age [7, 16] or different daily light exposure [13]. Details on these factors, which could be potential confounders, are not available, but we do not think that bias could have been introduced by them since the large number of samples is likely to be randomly distributed.
Politoff et al
[15] demonstrated a circannual rhythm in spermatogenesis using 2697 spermiograms
from fertile and subfertile men, with the lowest sperm parameter values
observed in July, August, September, and December , and the highest in
February and November. Statistical significance (P = 0.017) was
reached for the month of September. In the normal spermiogram population
alone, a similar rhythmicity was found, with sperm densities between 20
106/mL
and 250106/mL (first spermiograms
) and a minimum value again in September but which did not quite reach
statistical significance (P =
0.076). This seasonal pattern was confirmed in a recent paper focusing
on donor sperm quality for IVF [17]. On the other hand, the mean monthly
densities in patients with borderline semen quality or oligozoospermia
(< 20106/mL)
also displayed a distinct fall (P = 0.004) in August. Our study
examined the seasonal variation in different semen parameters in smokers,
non-smokers and in the total population of the study group (Table 2).
A rhythmicity with a significant decrease in semen quality (sperm density,
total sperm count and total motile sperm) in the summer months was observed
only in semen samples collected from smokers (Group C). This seasonal
summer reduction in semen quality confirms the observation of others [6-8,15].
Apart from sperm morphology, no statistically significant seasonal variation
was noted when comparing sperm parameters in the total or the entirely
non-smoking population depending on environmental temperature. However,
the results obtained are paradoxical to some extent. Chen et al
[7] found a seasonal variation in sperm density and morphology with a
greater percentage of sperm with normal morphology in winter than in spring
and summer, whereas in this study, we have observed an improved morphology
in the warmer seasons, at least in the overall and the non-smoking group.
Our non-smokers in Group C were significantly younger than those in the
cold period (A). Advanced age has been associated with decreased semen
volume, motility and morphology [16], which could thus explain our observation
together with the disappearance of this improved morphology in the total
population where the smokers with their negative contribution to the result
are included. Other studies did not find any seasonal variation in semen
parameters, but no differentiation between smokers and non-smokers was
made [9,11]. Another explanation for the seasonal variation could be the
daily exposure to light. Chia et al [10] analysed a total of 7
656 semen samples from men who reside in the tropics and no variations
in semen volume and density were observed; this may have been related
to the comparatively constant light exposure for all participants in these
latitudes. A differentiation in smoking habits was not done in this study.
When comparing smokers and non-smokers with respect to the environmental
tempe-rature, a decreased semen quality (sperm density, total sperm count,
motility and total motile sperm) in smokers of Group C (summer months)
was noted (Table 2). The association between cigarette smoking and altered
semen quality is well accepted [1, 3] and it could be possible that the
decrease in sperm quality in smokers during summer is the result of an
increased tobacco consumption in this period of the year. No data, however,
on tobacco consumption versus the season could be found. No difference
between the temperate (B) and the cold (A) season was observed in either
smokers or non-smokers.
One could hypothesize that in patients with an already reduced sperm quality such as smokers, the effects of environmental temperature and maybe light and lifestyle would have an additional deleterious influence on the spermatogenesis. This would also be in agreement with Politoff et al [15] who found a more pronounced decrease in sperm density in a population with oligozoospermia than in the control population during the summer.
In conclusion, sperm quality is influenced by a number of external factors, of which some are seasonal. Environmental factors such as temperature and light could have an additional negative effect on spermatogenesis and sperm quality in men with borderline fertility.
References
[1]
Zhang JP, Meng QY, Wang Q, Zhang
LJ, Mao YL, Sun ZX. Effect of smoking on semen quality of infertile men
in Shandong, China. Asian J Androl 2000; 2: 143-6.
[2] Vine MF, Tse CK, Hu P, Truong KY. Cigarette smoking and semen quality.
Fertil Steril 1996; 65: 835-42.
[3] Kunzle R, Mueller MD, Hanggi W, Birkhauser MH, Drescher H, Bersinger
NA. Semen quality of male smoker and nonsmoker in infertile couples. Fertil
Steril 2003; 79: 287-91.
[4] Auger J, Eustache F, Andersen AG, Irvine DS, Jorgensen N, Skakkebaek
NE, et al. Sperm morphological defects related to environment,
lifestyle and medical history of 1001 male partners of pregnant women
from four European cities. Hum Reprod 2001; 16: 2710-7.
[5] Hjollund NH, Storgaard L, Ernst E, Bonde JP, Olsen J. Impact of diurnal
scrotal temperature on semen quality. Reprod Toxicol 2002; 16: 215-21.
[6] Andolz P, Bielsa A, Andolz A. Circannual variation in human semen
parameters. Int J Androl 2001; 24: 266-71.
[7] Chen Z, Toth T, Godfrey-Bailey L, Mercedat N, Schiff I, Hauser R.
Seasonal variation and age-related changes in human semen parameters.
J Androl 2003; 24: 226-31.
[8] Gyllenborg J, Skakkebaek NE, Nielsen NC, Keiding N, Giwercman A. Secular
and seasonal changes in semen quality among young Danish men: a statistical
analysis of semen samples from 1927 donor candidates during 1977-1995.
Int J Androl 1999; 22: 28-36.
[9] Saint Pol P, Beuscart R, Leroy-Martin B, Hermand E, Jablonski W. Circannual
rhythms of sperm parameters of fertile men. Fertil Steril 1989; 51: 1030-3.
[10] Chia SE, Lim ST, Ho LM, Tay SK. Monthly variation in human semen
quality in male partners of infertile women in the tropics. Hum Reprod
2001; 16: 277-81.
[11] Ombelet W, Maes M, Vandeput H, Cox A, Janssen M, Pollet H, et
al. Chronobiological fluctuations in semen parameters with a constant
abstinence period. Arch Androl 1996; 37: 91-6.
[12] Centola GM, Eberly S. Seasonal variations and age-related changes
in human sperm count, motility, motion parameters, morphology, and white
blood cell concentration. Fertil Steril 1999; 72: 803-8.
[13] Levine RJ. Seasonal variation of semen quality and fertility. Scand
J Work Environ Health 1999; 25 Suppl 1: 34-8.
[14] WHO laboratory manual for the examination of human semen and semen-cervical
mucus interaction, 3rd ed. Cambridge (UK): Cambridge University Press;
1992.
[15] Politoff L, Birkhauser M, Almendral A, Zorn A. New data confirming
a circannual rhythm in spermatogenesis. Fertil Steril 1989; 52: 486-9.
[16] Kidd SA, Eskenazi B, Wyrobek AJ. Effects of male age on semen quality
and fertility: a review of the literature. Fertil Steril 2001; 75: 237-48.
[17] Yogev L, Kleiman S, Shabtai E, Botchan A, Gamzu R, Paz G, et al.
Seasonal variations in pre-and post-thaw donor sperm quality. Hum Reprod
2004; 19: 880-5.
Correspondence to:
Nick A. Bersinger, Ph.D., University
Department of Clinical Research, Inselspital KKL G3-825, Berne, CH-3010,
Switzerland.
Tel: +41-31-632 1358, Fax: +41-31-632 1199
Email: nick.bersinger@dkf.unibe.ch
Received 2003-12-18 Accepted
2004-06-14
