Abstract
Spermatogenesis is a temperature-dependent process, and high summer temperatures have been linked to lower sperm concentration and count. However, reports describing the association between other meteorological variables and semen quality are scarce. This study evaluated the association between semen quality and temperature, humidity, pressure, apparent temperature (AT), temperature-humidity index (THI), simplified wet-bulb global temperature (sWBGT), and sunshine duration. Semen samples were obtained at the Laboratorio de Andrología y Reproducción (LAR, Argentina), from men undergoing routine andrology examination (n=11657) and computer-assisted sperm analysis (n=4705) following WHO 2010 criteria. Meteorological variables readings were obtained from the Sistema Meteorológico Nacional. Sperm quality parameters were negatively affected in summer when compared to winter. Additionally, there was a significant decrease in sperm kinematics between winter and spring. Branch and bound variable selection followed by multiple regression analysis revealed a significant association between semen quality and meteorological variables. Specifically, changes in sunshine duration and humidity reinforced the prognosis of semen quality. Highest/lowest sunshine duration and humidity quantiles resulted in decreased sperm concentration, count, motility, vitality and membrane competence, nuclear maturity, and sperm kinematics associated to highest sunshine duration and lowest humidity. Findings from this report highlight the relevance of environmental studies for predicting alterations in male reproductive health associated to variations in meteorological variables, especially considering the current climate changes around the planet due to global warming and its consequences for human health.
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References
Agarwal A, Mulgund A, Hamada A, Chyatte MR (2015) A unique view on male infertility around the globe. Reprod Biol Endocrinol 13:37. https://doi.org/10.1186/s12958-015-0032-1
Amann RP (2008) The cycle of the seminiferous epithelium in humans: a need to revisit? J Androl 29:469–487. https://doi.org/10.2164/jandrol.107.004655
Barreca A, Deschenes O, Guldi M (2018) Maybe Next Month? Temperature shocks and dynamic adjustments in birth rates. Demography 55:1269–1293. https://doi.org/10.1007/s13524-018-0690-7
Barrett B, Charles JW, Temte JL (2015) Climate change, human health, and epidemiological transition. Prev Med 70:69–75. https://doi.org/10.1016/j.ypmed.2014.11.013
Bedford JM (2015) The epididymis re-visited: a personal view. Asian J Androl 17:693–698. https://doi.org/10.4103/1008-682X.153297
Bellastella G, Pane E, Iorio S, De Bellis A, Sinisi AA (2013) Seasonal variations of plasma gonadotropin, prolactin, and testosterone levels in primary and secondary hypogonadism: evidence for an independent testicular role. J Endocrinol Investig 36:339–342. https://doi.org/10.3275/8620
Bohmanova J, Misztal I, Cole JB (2007) Temperature-humidity indices as indicators of milk production losses due to heat stress. J Dairy Sci 90:1947–1956. https://doi.org/10.3168/jds.2006-513
Brito LF, Silva AE, Barbosa RT, Kastelic JP (2004) Testicular thermoregulation in Bos indicus, crossbred and Bos taurus bulls: relationship with scrotal, testicular vascular cone and testicular morphology, and effects on semen quality and sperm production. Theriogenology 61:511–528. https://doi.org/10.1016/s0093-691x(03)00231-0
Bujan L, Daudin M, Charlet JP, Thonneau P, Mieusset R (2000) Increase in scrotal temperature in car drivers. Hum Reprod 15:1355–1357. https://doi.org/10.1093/humrep/15.6.1355
Carlsen E, Petersen JH, Andersson AM, Skakkebaek NE (2004) Effects of ejaculatory frequency and season on variations in semen quality. Fertil Steril 82:358–366. https://doi.org/10.1016/j.fertnstert.2004.01.039
Chen Z, Toth T, Godfrey-Bailey L, Mercedat N, Schiff I, Hauser R (2003) Seasonal variation and age-related changes in human semen parameters. J Androl 24:226–231. https://doi.org/10.1186/1743-1050-1-2
De Giorgi A, Volpi R, Tiseo R, Pala M, Manfredini R, Fabbian F (2015) Seasonal variation of human semen parameters: A retrospective study in Italy. Chronobiol Int 32:711–716. https://doi.org/10.3109/07420528.2015.1024315
Demir A, Mehmet U, Arslan OE (2016) The effect of seasonal variation on sexual behaviors in males and its correlation with hormone levels: a prospective clinical trial. Cent European J Urol 69:285–289. https://doi.org/10.5173/ceju.2016.793
Ding GL, Liu Y, Liu ME, Pan JX, Guo MX, Sheng JZ, Huang HF (2015) The effects of diabetes on male fertility and epigenetic regulation during spermatogenesis. Asian J Androl 17:948–953. https://doi.org/10.4103/1008-682X.150844
Durairajanayagam D, Agarwal A, Ong C (2015) Causes, effects and molecular mechanisms of testicular heat stress. Reprod BioMed Online 30:14–27. https://doi.org/10.1016/j.rbmo.2014.09.018
Frungieri MB, Calandra RS, Rossi SP (2017) Local actions of melatonin in somatic cells of the testis. Int J Mol Sci 18:E1170. https://doi.org/10.3390/ijms18061170
Furnival GM, Wilson RW (1974) Regressions by leaps and bounds. Technometrics 16:499–511. https://doi.org/10.2307/1267601
Garolla A, Torino M, Sartini B, Cosci I, Patassini C, Carraro U, Foresta C (2013) Seminal and molecular evidence that sauna exposure affects human spermatogenesis. Hum Reprod 28:877–885. https://doi.org/10.1093/humrep/det020
Garolla A, Torino M, Miola P, Caretta N, Pizzol D, Menegazzo M, Bertoldo A, Foresta C (2015) Twenty-four-hour monitoring of scrotal temperature in obese men and men with a varicocele as a mirror of spermatogenic function. Hum Reprod 30:1006–1013. https://doi.org/10.1093/humrep/dev057
Goldie J, Alexander L, Lewis SC, Sherwood S (2017) Comparative evaluation of human heat stress indices on selected hospital admissions in Sydney, Australia. Aust N Z J Public Health 41:381–387. https://doi.org/10.1111/1753-6405.12692
Golher DM, Kumaresan A, Saraf KK, Chhillar S, Nayak S, Tripathi UK, Bhaskar CN, Lathwal SS, Mohanty TK (2018) Influence of season and climatic variables on testicular cytology, semen quality and melatonin concentrations in crossbred bucks reared under subtropical climate. Int J Biometeorol 62:1709–1719. https://doi.org/10.1007/s00484-018-1571-x
Gyllenborg J, Skakkebaek NE, Nielsen NC, Keiding N, Giwercman A (1999) 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 22:28–36. https://doi.org/10.1046/j.1365-2605.1999.00137.x
Hand DJ (1981) Branch and bound in statistical data analysis. Statistician 30:1–13. https://doi.org/10.2307/2987699
Heller CG, Clermont Y (1963) Spermatogenesis in man: an estimate of its duration. Science 140:184–186. https://doi.org/10.1126/science.140.3563.184
Hossain MZ, Bambrick H, Wraith D, Tong S, Khan AF, Hore SK, Hu W (2019) Sociodemographic, climatic variability and lower respiratory tract infections: a systematic literature review. Int J Biometeorol 63:209–219. https://doi.org/10.1007/s00484-018-01654-1
Ilacqua A, Izzo G, Emerenziani GP, Baldari C, Aversa A (2018) Lifestyle and fertility: the influence of stress and quality of life on male fertility. Reprod Biol Endocrinol 16:115. https://doi.org/10.1186/s12958-018-0436-9
Ivell R (2007) Lifestyle impact and the biology of the human scrotum. Reprod Biol Endocrinol 5:15. https://doi.org/10.1186/1477-7827-5-15
Jenkins TG, Aston KI, Carrell DT (2018) Sperm epigenetics and aging. Transl Androl Urol 7:S328–S335. https://doi.org/10.21037/tau.2018.06.10
Jung A, Leonhardt F, Schill WB, Schuppe HC (2005) Influence of the type of undertrousers and physical activity on scrotal temperature. Hum Reprod 20:1022–1027. https://doi.org/10.1093/humrep/deh697
Jung A, Strauss P, Lindner HJ, Schuppe HC (2008) Influence of heating car seats on scrotal temperature. Fertil Steril 90:335–339. https://doi.org/10.1016/j.fertnstert.2007.06.053
Kastelic JP, Rizzoto G, Thundathil J (2018) Review: Testicular vascular cone development and its association with scrotal thermoregulation, semen quality and sperm production in bulls. Animal. 12:s133–s141. https://doi.org/10.1017/S1751731118001167
Kastelic JP, Wilde RE, Bielli A, Genovese P, Rizzoto G, Thundathil J (2019) Hyperthermia is more important than hypoxia as a cause of disrupted spermatogenesis and abnormal sperm. Theriogenology. 131:177–181. https://doi.org/10.1016/j.theriogenology.2019.03.040
Krausz C, Riera-Escamilla A (2018) Genetics of male infertility. Nat Rev Urol 15:369–384. https://doi.org/10.1038/s41585-018-0003-3
Künzle R, Mueller MD, Huber AW, Drescher H, Bersinger NA (2004) Seasonality in human semen quality of smokers and non-smokers: effect of temperature. Asian J Androl 6:243–247
Lam D, Miron J (1996) The effects of temperature on human fertility. Demography 33:291–305
Leaver RB (2016) Male infertility: an overview of causes and treatment options. Br J Nurs 25:S35–S40. https://doi.org/10.12968/bjon.2016.25.18.S35
Lerchl A, Keck C, Spiteri-Grech J, Nieschlag E (1993) Diurnal variations in scrotal temperature of normal men and patients with varicocele before and after treatment. Int J Androl 16:195–200. https://doi.org/10.1111/j.1365-2605.1993.tb01179.x
Levine RJ (1999) Seasonal variation of semen quality and fertility. Scand J Work Environ Health 25:34–37 discussion 76-78
Levine H, Jørgensen N, Martino-Andrade A, Mendiola J, Weksler-Derri D, Mindlis I, Pinotti R, Swan SH (2017) Temporal trends in sperm count: a systematic review and meta-regression analysis. Hum Reprod Update 23:646–659. https://doi.org/10.1093/humupd/dmx022
Levitas E, Lunenfeld E, Weisz N, Friger M, Har-Vardi I (2013) Seasonal variations of human sperm cells among 6455 semen samples: a plausible explanation of a seasonal birth pattern. Am J Obstet Gynecol 208:406 e1–406 e6. https://doi.org/10.1016/j.ajog.2013.02.010
Llamas Luceño N, de Souza Ramos Angrimani D, de Cássia BL, Szymańska KJ, Van Poucke M, Demeyere K, Meyer E, Peelman L, Mullaart E, Broekhuijse MLWJ, Soom AV (2020) Exposing dairy bulls to high temperature-humidity index during spermatogenesis compromises subsequent embryo development in vitro. Theriogenology 141:16–25. https://doi.org/10.1016/j.theriogenology.2019.08.034
Lymperi S, Giwercman A (2018) Endocrine disruptors and testicular function. Metabolism 86:79–90. https://doi.org/10.1038/s41598-019-53919-3
Malm G, Haugen TB, Henrichsen T, Bjørsvik C, Grotmol T, Saether T, Malm J, Figenschau Y, Hagmar L, Rylander L, Levine RJ, Giwercman A (2004) Reproductive function during summer and winter in Norwegian men living north and south of the Arctic circle. J Clin Endocrinol Metab 89:4397–4402. https://doi.org/10.1210/jc.2004-0427
Marcho C, Oluwayiose OA, Pilsner JR (2020) The preconception environment and sperm epigenetics. Andrology 8:924–9424. https://doi.org/10.1111/andr.12753
Menegassi SRO, Pereira GR, Bremm C, Koetz C Jr, Lopes FG, Fiorentini EC, McManus C, Dias EA, da Rocha MK, Lopes RB, Barcellos JOJ (2016) Effects of ambient air temperature, humidity, and wind speed on seminal traits in Braford and Nellore bulls at the Brazilian Pantanal. Int J Biometeorol 60:1787–1794. https://doi.org/10.1007/s00484-016-1167-2
Meriggiola MC, Noonan EA, Paulsen CA, Bremner WJ (1996) Annual patterns of luteinizing hormone, follicle stimulating hormone, testosterone and inhibin in normal men. Hum Reprod 11:248–252. https://doi.org/10.1093/humrep/11.2.248
Morabito M, Crisci A, Messeri A, Capecchi V, Modesti PA, Gensini GF, Orlandini S (2014) Environmental temperature and thermal indices: what is the most effective predictor of heat-related mortality in different geographical contexts? Sci World J 2014:961750–961715. https://doi.org/10.1155/2014/961750
Neto FT, Bach PV, Najari BB, Li PS, Goldstein M (2016) Spermatogenesis in humans and its affecting factors. Semin Cell Dev Biol 59:10–26. https://doi.org/10.1016/j.semcdb.2016.04.009
Ozelci R, Yılmaz S, Dilbaz B, Akpınar F, Akdag Cırık D, Dilbaz S, Ocal A (2016) Seasonal variation of human sperm cells among 4,422 semen samples: A retrospective study in Turkey. Syst Biol Reprod Med 62:379–386. https://doi.org/10.1080/19396368.2016.1225322
Pawlowski B, Sorokowski P (2008) Men's attraction to women's bodies changes seasonally. Perception. 37:1079–1085. https://doi.org/10.1068/p5715
Ramasamy R, Armstrong JM, Lipshultz LI (2015) Preserving fertility in the hypogonadal patient: an update. Asian J Androl 17:197–200. https://doi.org/10.4103/1008-682X.142772
Rizzoto G, Kastelic JP (2020) A new paradigm regarding testicular thermoregulation in ruminants? Theriogenology. 147:166–175. https://doi.org/10.1016/j.theriogenology.2019.11.019
Ruhayel Y, Malm G, Haugen TB, Henrichsen T, Bjørsvik C, Grotmol T, Saether T, Malm J, Figenschau Y, Rylander L, Levine RJ, Giwercman A (2007) Seasonal variation in serum concentrations of reproductive hormones and urinary excretion of 6-sulfatoxymelatonin in men living north and south of the Arctic Circle: a longitudinal study. Clin Endocrinol 67:85–92. https://doi.org/10.1111/j.1365-2265.2007.02843.x
Sailer BL, Sarkar LJ, Bjordahl JA, Jost LK, Evenson DP (1997) Effects of heat stress on mouse testicular cells and sperm chromatin structure. J Androl 18:294–301
Santi D, Magnani E, Michelangeli M, Grassi R, Vecchi B, Pedroni G, Roli L, De Santis MC, Baraldi E, Setti M, Trenti T, Simoni M (2018) Seasonal variation of semen parameters correlates with environmental temperature and air pollution: A big data analysis over 6 years. Environ Pollut 235:806–813. https://doi.org/10.1016/j.envpol.2018.01.021
Sheynkin Y, Jung M, Yoo P, Schulsinger D, Komaroff E (2005) Increase in scrotal temperature in laptop computer users. Hum Reprod 20:452–455. https://doi.org/10.1093/humrep/deh616
Skinner JD, Louw GN (1966) Heat stress and spermatogenesis in Bos indicus and Bos taurus cattle. J Appl Physiol 21:1784–1790. https://doi.org/10.1152/jappl.1966.21.6.1784
Smolensky MH, Reinberg A, Bicakova-Rocher A, Sanford J (1981) Chronoepidemiological search for circannual changes in the sexual activity of human males. Chronobiologia 8:217–230
Sood S, Reghunandanan R, Singh U, Reghunandanan V, Singh PI (1993) Circanual variation of sperm count and motility in men. Indian J Med Sci 47:197–200
Spira A (1984) Seasonal variations of sperm characteristics. Arch Androl 12:23–28
Srinivasan AK, Freyle J, Gitlin JS, Palmer LS (2007) Climatic conditions and the risk of testicular torsion in adolescent males. J Urol 178:2585–2588. https://doi.org/10.1016/j.juro.2007.08.049
Steadman RG (1984) The determination of degree days for the heating, cooling and dehumidification of buildings: its application to arid-zone development. Int J Biometeorol 28:33–42
Suriyasomboon A, Lundeheim N, Kunavongkrit A, Einarsson S (2005) Effect of temperature and humidity on sperm morphology in duroc boars under different housing systems in Thailand. J Vet Med Sci 67:777–785. https://doi.org/10.1292/jvms.67.777
Verón GL, Tissera AD, Bello R, Beltramone F, Estofan G, Molina RI, Vazquez-Levin MH (2018) Impact of age, clinical conditions, and lifestyle on routine semen parameters and sperm kinematics. Fertil Steril 110:68–75.e4. https://doi.org/10.1016/j.fertnstert.2018.03.016
Wang C, Cui YG, Wang XH, Jia Y, Sinha Hikim A, Lue YH, Tong JS, Qian LX, Sha JH, Zhou ZM, Hull L, Leung A, Swerdloff RS (2007) Transient scrotal hyperthermia and levonorgestrel enhance testosterone-induced spermatogenesis suppression in men through increased germ cell apoptosis. J Clin Endocrinol Metab 92:3292–3304. https://doi.org/10.1210/jc.2007-0367
Wehr TA (2001) Photoperiodism in Humans and Other Primates: Evidence and Implications. J Biol Rhythm 16:348–364. https://doi.org/10.1177/074873001129002060
Winters BR, Walsh TJ (2014) The epidemiology of male infertility. Urol Clin North Am 41:195–204. https://doi.org/10.1016/j.ucl.2013.08.006
Yaeram J, Setchell BP, Maddocks S (2006) Effect of heat stress on the fertility of male mice in vivo and in vitro. Reprod Fertil Dev 18:647–653. https://doi.org/10.1071/rd05022
Yogev L, Kleiman S, Shabtai E, Botchan A, Gamzu R, Paz G, Yavetz H, Hauser R (2004) Seasonal variations in pre- and post-thaw donor sperm quality. Hum Reprod 19:880–885. https://doi.org/10.1093/humrep/deh165
Zhang XZ, Liu JH, Sheng HQ, Wu HJ, Wu Y, Yao KS, Lu JC, Zhang FB (2013) Seasonal variation in semen quality in China. Andrology 1:639–643. https://doi.org/10.1111/j.2047-2927.2013.00092.x
Lauritsen JL, White N (2014) Seasonal patterns in criminal victimization trends. U.S. Department of Justice Office of Justice Programs Bureau of Justice Statistics NCJ 245959:1-21.
World Health Organization, Department of Reproductive Health and Research (2010). WHO laboratory manual for the examination and processing of human semen. Fifth edition. Geneve, Switzerland. ISBN: 978 92 4 154778 9
Funding
Studies were supported by funds from the LAR to RM and from Consejo Nacional de Investigaciones Científicas y Técnicas de Argentina (CONICET) (PIP2015#887) to MVL. Special thanks to Fundación R. Barón and Fundación Williams for institutional (IBYME) support.
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Verón, G.L., Tissera, A.D., Bello, R. et al. Association between meteorological variables and semen quality: a retrospective study. Int J Biometeorol 65, 1399–1414 (2021). https://doi.org/10.1007/s00484-021-02112-1
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DOI: https://doi.org/10.1007/s00484-021-02112-1