Submitted:
19 December 2024
Posted:
19 December 2024
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Abstract
Keywords:
1. Introduction
2. Materials and Methods
3. Results
3.1.1. Demographic Results
3.1.2. Confounder and Time Window Selection
3.1.3. Seasonal Analysis
3.1.4. Subgroup Analysis of Motility
4. Discussion
4.1. Limitations
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Appendix A


| (a) Relative effect of exposure to top 25th percent of maximum daily temperatures in summer months on percent motile sperm | |||
| Subgroup | Effect on Motility (%), 95% CI | P value | |
| Total | -0.62% (-3.96, 2.83) | 0.721 | |
| Sperm status | |||
| Normal Motility Range | 0.17% (-1.45, 1.81) | 0.842 | |
| Abnormal Motility Range | -5.38% (-13.02, 2.92) | 0.197 | |
| Ethnicity | |||
| Jewish | -0.4% (-4.34, 3.71) | 0.856 | |
| Arab | -0.1% (-6.11, 6.31) | 0.975 | |
| SES | |||
| Low | -5.92%% (-12.74, 1.43) | 0.112 | |
| Mid | 0.82% (-3.58, 5.41) | 0.721 | |
| High | 2.23% (-4.86, 9.84) | 0.547 | |
| Age | |||
| Below 40 years | -1.52% (-5.05, 2.13) | 0.409 | |
| Above 40 years | 4.43% (-4.82, 14.58) | 0.360 | |
| Smoking status | |||
| Non-smokers | -0.28% (-5.16, 4.86) | 0.913 | |
| Smokers | -1.79% (-6.72, 3.40) | 0.491 | |
| Co-morbidities | |||
| None | -0.2% (-6.43, 6.45) | 0.951 | |
| Some | -0.56% (-4.46, 3.50) | 0.782 | |
| (a) Relative effect of exposure to bottom 25th percent of minimum daily temperatures in winter months on percent motile sperm | |||
| Subgroup | Effect on Motility (%), 95% CI | P value | |
| Total | -5.52% (-8.9, -1.9) | 0.003 | |
| Sperm status | |||
| Normal Motility Range | -1.46% (-3.1, 0.1) | 0.072 | |
| Abnormal Motility Range | -3.58% (-9.9, 3.2) | 0.201 | |
| Ethnicity | |||
| Jewish | -6.53% (-10.6, -2.3) | 0.002 | |
| Arab | -3.74% (-10.0, 2.9) | 0.366 | |
| SES | |||
| Low | -5.58% (-12.5, 1.87) | 0.138 | |
| Mid | -6.03% (-10.56, -1.26) | 0.013 | |
| High | -4.14% (-11.86, 4.26) | 0.323 | |
| Age | |||
| Below 40 years | -4.87% (-8.66, -0.91) | 0.016 | |
| Above 40 years | -6.81% (-15.0, 2.18) | 0.133 | |
| Smoking status | |||
| Non-smokers | -6.26% (-11.20, -1.05) | 0.019 | |
| Smokers | -6.55% (-11.76, -1.02) | 0.021 | |
| Co-morbidities | |||
| None | 0.73% (-6.36, 8.36) | 0.844 | |
| Some | -7.35% (-11.27, -3.25) | <0.001 | |
References
- Marx, W.; Haunschild, R.; Bornmann, L. Heat waves: a hot topic in climate change research. Theor Appl Climatol. 2021, 146, 781–800. [Google Scholar] [CrossRef] [PubMed]
- Meehl, G.A.; Tebaldi, C. More intense, more frequent, and longer lasting heat waves in the 21st century. Science. 2004, 305, 994–997. [Google Scholar] [CrossRef] [PubMed]
- Jouannet, P.; Wang, C.; Eustache, F.; Kold-Jensen, T.; Auger, J. Semen quality and male reproductive health: the controversy about human sperm concentration decline. APMIS. 2001, 109, 333–344. [Google Scholar] [CrossRef] [PubMed]
- Nelson, C.M.K.; Bunge, R.G. Semen Analysis: Evidence for Changing Parameters of Male Fertility Potential. Fertility and Sterility. 1974, 25, 503–507. [Google Scholar] [CrossRef] [PubMed]
- Swan, S.H.; Elkin, E.P.; Fenster, L. The question of declining sperm density revisited: an analysis of 101 studies published 1934-1996. Environ Health Perspect. 2000, 108, 961–966. [Google Scholar] [CrossRef] [PubMed]
- Ravitsky, V.; Kimmins, S. The forgotten men: rising rates of male infertility urgently require new approaches for its prevention, diagnosis and treatment. Biology of Reproduction. 2019, 101, 872–874. [Google Scholar] [CrossRef] [PubMed]
- Lv, M.Q.; Ge, P.; Zhang, J.; Yang, Y.Q.; Zhou, L.; Zhou, D.X. Temporal trends in semen concentration and count among 327 373 Chinese healthy men from 1981 to 2019: a systematic review. Hum Reprod. 2021, 36, 1751–1775. [Google Scholar] [CrossRef] [PubMed]
- Mann, U.; Shiff, B.; Patel, P. Reasons for worldwide decline in male fertility. Current Opinion in Urology. 2020, 30, 296–301. [Google Scholar] [CrossRef] [PubMed]
- Levine H, Jørgensen N, Martino-Andrade A, Mendiola J, Weksler-Derri D, Mindlis I, et al. Temporal trends in sperm count: a systematic review and meta-regression analysis. Hum Reprod Update. 2017, 23, 646–659.
- Levine H, Jørgensen N, Martino-Andrade A, Mendiola J, Weksler-Derri D, Jolles M, et al. Temporal trends in sperm count: a systematic review and meta-regression analysis of samples collected globally in the 20th and 21st centuries. Human Reproduction Update. 2022 Nov 15;dmac035.
- WHO laboratory manual for the examination and processing of human semen. Available online: https://apps.who.int/iris/handle/10665/44261 (accessed on 1 October 2022).
- Wang X, Tian X, Ye B, Zhang Y, Zhang X, Huang S, et al. The association between ambient temperature and sperm quality in Wuhan, China. Environ Health. 2020, 19, 44.
- Appell, R.A.; Evans, P.R.; Blandy, J.P. The effect of temperature on the motility and viability of sperm. Br J Urol. 1977, 49, 751–756. [Google Scholar] [CrossRef] [PubMed]
- Sperm in hot water: direct and indirect thermal challenges interact to impact on brown trout sperm quality | Journal of Experimental Biology | The Company of Biologists. Available online: https://journals.biologists.com/jeb/article/220/14/2513/18616/Sperm-in-hot-water-direct-and-indirect-thermal (accessed on 11 September 2022).
- Kandeel, F.R.; Swerdloff, R.S. Role of temperature in regulation of spermatogenesis and the use of heating as a method for contraception. Fertil Steril. 1988, 49, 1–23. [Google Scholar] [PubMed]
- Shadmehr, S.; Fatemi Tabatabaei, S.R.; Hosseinifar, S.; Tabandeh, M.R.; Amiri, A. Attenuation of heat stress-induced spermatogenesis complications by betaine in mice. Theriogenology. 2018, 106, 117–126. [Google Scholar] [CrossRef] [PubMed]
- Hamilton TR dos S, Mendes CM, de Castro LS, de Assis PM, Siqueira AFP, Delgado J de C, et al. Evaluation of Lasting Effects of Heat Stress on Sperm Profile and Oxidative Status of Ram Semen and Epididymal Sperm. Oxid Med Cell Longev. 2016, 2016, 1687657.
- Santi D, Vezzani S, Granata AR, Roli L, De Santis MC, Ongaro C, et al. Sperm quality and environment: A retrospective, cohort study in a Northern province of Italy. Environ Res. 2016, 150, 144–153.
- Reimer-Benaim, A. The use of time-dynamic patterns of temperature and flexible generalized models to clarify the relations between temperature and semen quality – PubMed. Available online: https://pubmed.ncbi.nlm.nih.gov/39025153/ (accessed on 27 August 2024).
- Momen, M.N.; Ananian, F.B.; Fahmy, I.M.; Mostafa, T. Effect of high environmental temperature on semen parameters among fertile men. Fertility and Sterility. 2010, 93, 1884–1886. [Google Scholar] [CrossRef] [PubMed]
- Wang C, McDonald V, Leung A, Superlano L, Berman N, Hull L, et al. Effect of increased scrotal temperature on sperm production in normal men. Fertil Steril. 1997, 68, 334–339.
- Hotter Summers Kill Thousands in a Europe With Scant Air Conditioning - WSJ. Available online: https://www.wsj.com/world/europe/hotter-summers-kill-thousands-in-a-europe-with-scant-air-conditioning-9c8ab5d8 (accessed on 14 September 2023).
- Heat-related mortality in Europe during the summer of 2022 | Nature Medicine. Available online: https://www.nature.com/articles/s41591-023-02419-z (accessed on 14 September 2023).



| Patients’ characteristics | Total (N= 21,331) |
Jewish | Arab | Normal | Abnormal |
|---|---|---|---|---|---|
| (N=13,192) | (N=7,134) | (N=10,043) | (N=10,288) | ||
|
Age, years Mean±SD (n) Median |
32.7 ± 8.4 (21,331) 31 |
32.7±7.9 (13,192) 32 |
32.2±9.1(7,134) 30 |
31.9±7.7 (10,043) 31 |
33.2±8.9 (10,288) 32 |
|
SES (0-10) Mean±SD (n) Median |
4.5 ± 2.8 (21,331) 5 |
4.8±2.5 (13,192) 5 |
1.6± 2.5 (7,134) 1 |
3.9±2.9 (10,043) 4 |
3.4±2.9 (10,288) 3 |
| Smoking, % (n/N) | 40.4 (8,617/21,331) | 45.0 (4,913/13,192) | 48.7 (3,605/7,134) | 45.3 (4,549/10,043) | 47.4 (4,876/10,288) |
| Comorbidities(%, n/N) | |||||
| Diabetes | 7.2 (1,535/21,331) | 5.4 (733/13,192) | 9.9 (803/7,134) | 4.7 (472/10,043) | 9.2 (946/10,288) |
| Hyperlipidemia | 19.0 (4,052/21,331) | 18.6 (2,529/13,192) | 21.1 (1,685/7,134) | 16.6 (1,667/10,043) | 22.3 (2,294/10,288) |
| Obesity | 18.5 (3,946/21,331) | 16.8 (2,268/13,192) | 21.3 (1,641/7,134) | 16.6 (1,677/10,043) | 19.9 (2,047/10,288) |
| Hypertension | 5.6 (1,194/21,331) | 5.2 (712/13,192) | 6.0 (483/7,134) | 3.9 (391/10,043) | 7.0 (720/10,288) |
| Sperm Quality | |||||
|
Motility, % Mean±SD (n) Median |
52.2 ± 22.1 (14,385) 56 |
53.3±21.0 (9,225) 57 |
50.0±23.7 (5,160) 53 |
63.4±13.0 (10,399) 63 |
22.7±10.9 (3,986) 24 |
|
Progressive Motility, % Mean±SD (n) Median |
43.8 ± 21.4 (14,686) 46 |
45.3±20.9 (9,552) 47 |
41.1±22.1 (5,154) 42 |
55.0±13.7 (10,355) 54 |
17.1±9.4 (4,331) 18 |
|
Normal Cell Count, 106 per ejaculate Mean±SD (n) Median |
3.7 ± 2.2 (13,455) 3 |
3.8±2.2 (8,974) 4 |
3.3±1.9 (4,481) 3 |
NA | NA |
|
Sperm Concentration, 106 per ml Mean±SD (n) Median |
53.1 ± 47.9 (14,852) 40 |
58.9 ± 49.6 (9,226) 50 |
42.3±41.9 (5,163) 30 |
65.0±43.4 (11,170) 55 |
6.2±4.4 (3,168) 6 |
|
Semen Volume, ml Mean±SD (n) Median |
2.5 ± 1.5 (19,558) 2 |
2.6 ± 1.7 (12,261) 2 |
2.4 ± 1.6 (7,291) 2 |
2.5±1.02 (14,248)2 | 0.6±1.5 (3,512) 1 |
| Yearlong (Bottom 25th percentile) | Yearlong (Top 25th percentile) |
Winter (Bottom 25th percentile) | Summer (Top 25th percentile) | |
|---|---|---|---|---|
| Motility (% Change, p-value, N) | -11.19 (<0.001) (N=14,849) |
6.21 (<0.001) (N=14,849) |
-5.52 0.003 (N=5,251) |
-0.62 0.721 (N=4,257) |
| Progressive motility (% Change, p-value, N) | -13.54 (<0.001) (N=14,686) |
6.21 (<0.001) (N=14,686) |
-7.07 0.001 (N=5,249) |
0.59 0.767 (N=4,246) |
| Sperm concentration (% change, in 106 cells/ml, p-value, N) | 4.01 (0.015) (N=14,852) |
-6.34 (<0.001) (N=14,852) |
-4.65 (0.135) (N=5,252) |
-1.59 (0.674) (N=4,255) |
| Normal cells (% change, in 106 per ejaculate, p-value, N) | 4.48 (<0.001) (N=13,460) |
-6.20 (<0.001) (N=13,460) |
2.63 (0.202) (N=4,746) |
-5.80 (<0.001) (N=4,232) |
| Semen Volume (% change, in ml, p-value, N) | 0.20 (0.895) (N=19,558) |
-0.94 (0.525) (N=19,558) |
-0.64 (0.754) (N=6,649) |
1.74 (0.532) (N=6,649) |
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