Ambient temperature-related sex ratio at birth in historical urban populations: the example of the city of Poznań, 1848-1900.
Climate
Conception
Nineteenth century
Pregnancy
Secondary sex ratio
Temperature stress
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
18 Jun 2024
18 Jun 2024
Historique:
received:
14
03
2024
accepted:
13
06
2024
medline:
19
6
2024
pubmed:
19
6
2024
entrez:
18
6
2024
Statut:
epublish
Résumé
This study examines whether exposure to ambient temperature in nineteenth-century urban space affected the ratio of boys to girls at birth. Furthermore, we investigate the details of temperature effects timing upon sex ratio at birth. The research included 66,009 individual births, aggregated in subsequent months of births for the years 1847-1900, i.e. 33,922 boys and 32,087 girls. The statistical modelling of the probability of a girl being born is based on logistic GAM with penalized splines and automatically selected complexity. Our research emphasizes the significant effect of temperature in the year of conception: the higher the temperature was, the smaller probability of a girl being born was observed. There were also several significant temperature lags before conception and during pregnancy. Our findings indicate that in the past, ambient temperature, similar to psychological stress, hunger, malnutrition, and social and economic factors, influenced the viability of a foetus. Research on the effects of climate on the sex ratio in historical populations may allow for a better understanding of the relationship between environmental factors and reproduction, especially concerning historical populations since due to some cultural limitations, they were more prone to stronger environmental stressors than currently.
Identifiants
pubmed: 38890431
doi: 10.1038/s41598-024-64799-7
pii: 10.1038/s41598-024-64799-7
doi:
Types de publication
Journal Article
Historical Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
14001Subventions
Organisme : Narodowe Centrum Nauki
ID : No. UMO-2020/39/O/HS3/00524
Informations de copyright
© 2024. The Author(s).
Références
Bonell, A. et al. A protocol for an observational cohort study of heat strain and its effect on fetal wellbeing in pregnant farmers in The Gambia. Wellcome Open Res. 31(5), 32. https://doi.org/10.12688/wellcomeopenres.15731.2 (2020).
doi: 10.12688/wellcomeopenres.15731.2
Rekha, S., Nalini, S. J., Bhuvana, S., Kanmani, S. & Vidhya, V. A. Comprehensive review on hot ambient temperature and its impacts on adverse pregnancy outcomes. J. Mother Child 27(1), 10–20. https://doi.org/10.34763/jmotherandchild.20232701.d-22-00051 (2023).
doi: 10.34763/jmotherandchild.20232701.d-22-00051
pubmed: 37368943
pmcid: 10298495
Flouris, A. D., Spiropoulos, Y., Sakellariou, G. J. & Koutedakis, Y. Effect of seasonal programming on fetal development and longevity: Links with environmental temperature. Am. J. Hum. Biol. 21(2), 214–216. https://doi.org/10.1002/ajhb.20818 (2009).
doi: 10.1002/ajhb.20818
pubmed: 19194861
Basu, R. & Sarovar, V. Association between high ambient temperature and risk of stillbirth in California. Am. J. Epidemiol. 183(10), 894–901. https://doi.org/10.1093/aje/kwv295 (2016).
doi: 10.1093/aje/kwv295
pubmed: 27037268
Rylander, C., Odland, J. Ø. & Sandanger, T. M. Climate change and environmental impacts on maternal and newborn health with focus on Arctic populations. Glob. Health Action 4(1), 8452. https://doi.org/10.3402/gha.v4i0.8452 (2011).
doi: 10.3402/gha.v4i0.8452
Auger, N., Naimi, A. I., Smargiassi, A., Lo, E. & Kosatsky, T. Extreme heat and risk of early delivery among preterm and term pregnancies. Epidemiology 25(3), 344–350. https://doi.org/10.1097/EDE.0000000000000074 (2014).
doi: 10.1097/EDE.0000000000000074
pubmed: 24595396
Kuehn, L. & McCormick, S. Heat exposure and maternal health in the face of climate change. Int. J. Environ. Res Public Health 14(8), 853. https://doi.org/10.3390/ijerph14080853 (2017).
doi: 10.3390/ijerph14080853
pubmed: 28758917
pmcid: 5580557
Shashar, S. et al. Temperature and preeclampsia: Epidemiological evidence that perturbation in maternal heat homeostasis affects pregnancy outcome. PLoS One 15(5), e0232877. https://doi.org/10.1371/journal.pone.0232877 (2020).
doi: 10.1371/journal.pone.0232877
pubmed: 32421729
pmcid: 7234374
Kasdorf, E. & Perlman, J. M. Hyperthermia, inflammation, and perinatal brain injury. Pediatr. Neurol. 49(1), 8–14. https://doi.org/10.1016/j.pediatrneurol.2012.12.026 (2013).
doi: 10.1016/j.pediatrneurol.2012.12.026
pubmed: 23683657
Asamoah, B., Kjellstrom, T. & Östergren, P.-O. Is ambient heat exposure levels associated with miscarriage or stillbirths in hot regions? A cross-sectional study using survey data from the Ghana Maternal Health Survey 2007. Int. J. Biometeorol. 62(3), 319–330. https://doi.org/10.1007/s00484-017-1402-5 (2018).
doi: 10.1007/s00484-017-1402-5
pubmed: 28748383
Rahman, J., Fakhruddin, S., Rahman, A. F. & Halim, M. Environmental heat stress among young working women: A pilot study. Ann Glob. Health 82(5), 760–767. https://doi.org/10.1016/j.aogh.2016.07.007 (2016).
doi: 10.1016/j.aogh.2016.07.007
pubmed: 28283126
Vicedo-Cabrera, A. M., Olsson, D. & Forsberg, B. Exposure to seasonal temperatures during the last month of gestation and the risk of preterm birth in Stockholm. Int. J. Environ. Res. Public Health 12(4), 3962–3396. https://doi.org/10.3390/ijerph120403962 (2015).
doi: 10.3390/ijerph120403962
pubmed: 25867199
pmcid: 4410227
Rooney, C., McMichael, A., Kovats, R. & Coleman, M. Excess mortality in England and Wales, and in Greater London, during the 1995 heat wave. J. Epidemiol. Commun. Health 52(8), 482–486. https://doi.org/10.1136/jech.52.8.482 (1998).
doi: 10.1136/jech.52.8.482
Kysely, J. & Kim, J. Mortality during heat waves in South Korea, 1991 to 2005: How exceptional was the 1994 heat wave?. Clim. Res. 38, 105–116. https://doi.org/10.3354/cr00775 (2009).
doi: 10.3354/cr00775
Basagña, X. et al. Heat waves and cause-specific mortality at all ages. Epidemiology 22(6), 765–772. https://doi.org/10.1097/EDE.0b013e31823031c5 (2011).
doi: 10.1097/EDE.0b013e31823031c5
Nitschke, M. et al. Impact of two recent extreme heat episodes on morbidity and mortality in Adelaide, South Australia: A case series analysis. Environ. Health 42, 1–10. https://doi.org/10.1186/1476-069X-10-42 (2011).
doi: 10.1186/1476-069X-10-42
Lawlor, D. A., Leon, D. A. & Smith, G. D. The association of ambient outdoor temperature throughout pregnancy and offspring birthweight: Findings from the Aberdeen Children of the 1950s cohort. BJOG1 12(5), 647–657 https://doi.org/10.1111/j.1471-0528.2004.00488.x (2005).
Murray, L. J. et al. Season and outdoor ambient temperature: Effects on birth weight. Obstet. Gynecol. 96, 689–695. https://doi.org/10.1016/s0029-7844(00)01022-x (2000).
doi: 10.1016/s0029-7844(00)01022-x
pubmed: 11042302
Cavalli-Sforza, L. L. & Bodmer, W. F. The Genetics of Human Populations (Freeman, 1971).
Catalano, R., Bruckner, T. & Smith, K. R. Ambient temperature predicts sex ratios and male longevity. PNAS 105(6), 2244–2247. https://doi.org/10.1073/pnas.0710711104 (2008).
doi: 10.1073/pnas.0710711104
pubmed: 18250336
pmcid: 2538905
Lerchl, A. Sex ratios at birth and environmental temperatures. Naturwissenschaften 86, 340–342. https://doi.org/10.1007/s001140050630 (1999).
doi: 10.1007/s001140050630
pubmed: 10451858
McLachlan, J. C. & Storey, H. Hot male: Can sex in humans be modified by temperature?. J. Theor. Biol. 222(1), 71–72. https://doi.org/10.1016/s0022-5193(03)00014-6 (2003).
doi: 10.1016/s0022-5193(03)00014-6
pubmed: 12699735
Grech, V., Savona-Ventura, C. & Vassallo-Agius, P. Unexplained differences in sex ratios at birth in Europe and North America. BMJ 324, 1010. https://doi.org/10.1136/bmj.324.7344.1010 (2002).
doi: 10.1136/bmj.324.7344.1010
pubmed: 11976243
pmcid: 102777
Helle, S., Helama, S. & Jokela, J. Temperature-related birth sex ratio bias in historical Sami: Warm years bring more sons. Biol. Lett. 4, 60–62. https://doi.org/10.1098/rsbl.2007.0482 (2008).
doi: 10.1098/rsbl.2007.0482
pubmed: 18042510
Murray, J. D., Deeming, D. C. & Ferguson, M. W. J. Size-dependent pigmentation-pattern formation in embryos of alligator mississippiensis: Time of initiation of pattern generation mechanism. Proc. R. Soc. B. Biol. Sci. 239(1296), 279–293 http://www.jstor.org/stable/49461 (1990).
Grech, V., Vassallo-Agius, P. & Savona-Ventura, C. Declining male births with increasing geographical latitude in Europe. J. Epidemiol. Commun. Health 54(4), 244–246. https://doi.org/10.1136/jech.54.4.244 (2000).
doi: 10.1136/jech.54.4.244
Schmahl, J. & Capel, B. Cell proliferation is necessary for the determination of male fate in the gonad. Dev. Biol. 258(2), 264–276. https://doi.org/10.1016/S0012-1606(03)00122-2 (2000).
doi: 10.1016/S0012-1606(03)00122-2
Piprek, R. P. & Kubiak, J. Z. Historia badań nad determinacją płci. Kosmos 68, 523–533. https://doi.org/10.36921/kos.2019_2516 (2019).
doi: 10.36921/kos.2019_2516
McLaren, Z. & Wide, J. The Effect of Ambient Temperature during Pregnancy on Human Sex Ratios at Birth. https://paa.confex.com/paa/2017/mediafile/ExtendedAbstract/Paper16645/McLaren_Wilde_Temperature_Gender_9292016.pdf . Accessed 1 March 2024 (2016).
Hajdu, T. & Hajdu, G. Temperature, climate change, and human conception rates: Evidence from Hungary. J. Popul. Econ. 35(4), 1751–1776. https://doi.org/10.1007/s00148-020-00814-1 (2022).
doi: 10.1007/s00148-020-00814-1
Rutledge, J. J., Monson, R. L., Northey, D. L. & Leibfried-Rutledge, M. L. Seasonality of cattle embryo production in a temperate region. Theriogenology 51, 330. https://doi.org/10.1016/S0093-691X(99)91889-7 (1999).
doi: 10.1016/S0093-691X(99)91889-7
De Rensis, F. & Scaramuzzi, R. J. Heat stress and seasonal effects on reproduction in the dairy cow—A review. Theriogenology 60(6), 1139–1151. https://doi.org/10.1016/S0093-691X(03)00126-2 (2003).
doi: 10.1016/S0093-691X(03)00126-2
pubmed: 12935853
Wolfenson, D., Roth, Z. & Meidan, R. Impaired reproduction in heat-stressed cattle: Basic and applied aspects. Anim. Reprod. Sci. 2(60–61), 535–547. https://doi.org/10.1016/s0378-4320(00)00102-0 (2000).
doi: 10.1016/s0378-4320(00)00102-0
Edwards, M. J., Saunders, R. D. & Shiota, K. Effects of heat on embryos and foetuses. Int. J. Hyperthermia 19(3), 295–324. https://doi.org/10.1080/0265673021000039628 (2003).
doi: 10.1080/0265673021000039628
pubmed: 12745973
van Zutphen, A. R., Lin, S., Fletcher, B. A. & Hwang, S.-A. A population based case–control study of extreme summer temperature and birth defects. Environ. Health Perspect. 120(10), 1443–1449. https://doi.org/10.1289/ehp.1104671 (2012).
doi: 10.1289/ehp.1104671
pubmed: 23031822
pmcid: 3491926
Fukuda, M., Fukuda, K., Shimizu, T. & Møller, H. Decline in sex ratio at birth after Kobe earthquake. Hum. Reprod. 13(8), 2321–2322. https://doi.org/10.1093/humrep/13.8.2321 (1998).
doi: 10.1093/humrep/13.8.2321
pubmed: 9756319
Fukuda, M., Fukuda, K., Shimizu, T., Yomu-Ra, W. & Shimizu, S. Kobe earthquake and reduced sperm motility. Hum. Reprod. 11, 1244–1246. https://doi.org/10.1093/oxfordjournals.humrep.a019365 (1996).
doi: 10.1093/oxfordjournals.humrep.a019365
pubmed: 8671433
Gomendio, M. et al. Male fertility and sex ratio at birth in red deer. Science 314(5804), 1445–1447. https://doi.org/10.1126/science.1133064 (2006).
doi: 10.1126/science.1133064
pubmed: 17138900
Paul, C., Murray, A. A., Spears, N. & Saunders, P. T. K. A single, mild, transient scrotal heat stress causes DNA damage, subfertility and impairs formation of blastocysts in mice. Reproduction 136, 73–84. https://doi.org/10.1530/REP-08-0036 (2008).
doi: 10.1530/REP-08-0036
pubmed: 18390691
Yaeram, J., Setchell, B. P. & Maddocks, S. 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 (2006).
doi: 10.1071/RD05022
pubmed: 16930511
Brito, L. F. C., Silva, A. E. D. F., Barbosa, R. T., Unanian, M. M. & Kastelic, J. P. Effects of scrotal insulation on sperm production, semen quality, and testicular echotexture in Bos indicus and Bos indicus × Bos taurus bulls. Anim. Reprod. Sci. 79, 1–15. https://doi.org/10.1016/S0378-4320(03)00082-4 (2003).
doi: 10.1016/S0378-4320(03)00082-4
pubmed: 12853175
Garcia-Oliveros, L. N. et al. Heat stress effects on bovine sperm cells: A chronological approach to early findings. Int. J. Biometeorol. 64, 1367–1378. https://doi.org/10.1007/s00484-020-01917-w (2020).
doi: 10.1007/s00484-020-01917-w
pubmed: 32388687
Pérez-Crespo, M., Pintado, B. & Gutiérrez-Adán, A. Scrotal heat stress effects on sperm viability, sperm DNA integrity, and the offspring sex ratio in mice. Mol. Reprod. Dev. 75, 40–47. https://doi.org/10.1002/mrd.20759 (2008).
doi: 10.1002/mrd.20759
pubmed: 17474098
Boklage, C. E. Survival probability of human conceptions from fertilization to term. Int. J. Fertil. 35(2), 75, 79–80, 81–94 (1990).
pubmed: 1970983
Macklon, N. S., Geraedts, J. P. & Fauser, B. C. Conception to ongoing pregnancy: The “black box” of early pregnancy loss. Hum. Reprod. 8(4), 333–343. https://doi.org/10.1093/humupd/8.4.333 (2002).
doi: 10.1093/humupd/8.4.333
Wilcox, A. J. et al. Incidence of early loss of pregnancy. N. Engl. J. Med. 319, 189–194. https://doi.org/10.1056/NEJM198807283190401 (1988).
doi: 10.1056/NEJM198807283190401
pubmed: 3393170
Trivers, R. L. & Willard, D. E. Natural selection of parental ability to vary the sex ratio of offspring. Science 191(249–263), 1973. https://doi.org/10.1126/science.179.4068.90 (1973).
doi: 10.1126/science.179.4068.90
Klimada 2.0. https://klimada2.ios.gov.pl/ . Accessed 4 Mar 2024 (2024).
Kundzewicz, Z. W. Climate changes, their reasons and effects—Observations and projections. Landform Anal. 15, 39–49. http://yadda.icm.edu.pl/baztech/element/bwmeta1.element.baztech-article-BUJ5-0052-0052 . Accessed 4 Mar 2024 (2011).
Błażejczyk, K., Baranowski, J. & Błażejczyk, A. Wpływ Klimatu na Stan Zdrowia w Polsce: Stan Aktualny Oraz Prognoza do 2100 Roku (Wydawnictwo Akademickie SEDNO, 2015).
Grzeszczuk-Brendel, H. Miasto do Mieszkania. Zagadnienia Reformy Mieszkaniowej na Przełomie XIX i XX Wieku i jej Wprowadzenie w Poznaniu w Pierwszej Połowie XX Wieku (Wydawnictwo Politechniki Poznańskiej, 2012).
Trzeciakowski, L. Społeczeństwo, jego życie codzienne i kultura materialna. In Dzieje Poznania w Latach 1793–1945 (Topolski, J., Trzeciakowski, L. eds.). 296–320 (Wydawnictwo Naukowe PWN, 1994).
Die Gemeinden und Gutsbezirke des Preussischen Staates und ihre Bevölkerung. 4, Die Gemeinden und Gutsbezirke der Provinz Posen und ihre Bevölkerung: Nach den Urmaterialien der Allgemeinen Volkszählung vom 1. December 1871 (Verlag des Königlichen Statistischen Bureaus, 1874).
Łuczak, C. Życie Gospodarczo-Społeczne w Poznaniu 1815–1918 (Wydawnictwo Poznańskie, 1965).
Szulc, W. Położenie Klasy Robotniczej w Wielkopolsce w Latach 1871–1914 (Wydawnictwo Naukowe UAM, 1970).
Smosarski, W. Temperatura i Opady w Wielkopolsce (Ministerstwo Wyznań Religijnych i Oświecenia Publicznego, 1925).
Kolendowicz, K. et al. Homogenization of air temperaturę and its long-term trends in Poznan (Poland) for the period 1848–2016. Theor. Appl. Climatol. 136, 1357–1370. https://doi.org/10.1007/s00704-018-2560-z (2019).
doi: 10.1007/s00704-018-2560-z
Cunningham, J. M. et al. The frequency of hereditary defective mismatch repair in a prospective series of unselected colorectal carcinomas. Am. J. Hum. Genet. 69(5), 1160. https://doi.org/10.1086/323658 (2001).
doi: 10.1086/323658
Bhat, R. A. & Kushtagi, P. A re-look at the duration of human pregnancy. Singap. Med. J. 12(47), 1044–1048 (2006).
Hastie, T. J. & Tibshirani, R. J. Generalized Additive Models. https://doi.org/10.1201/9780203753781 (Boca Raton, 1990).
Wood, S. N. Generalized Additive Models: An Introduction with R. 2nd ed. https://doi.org/10.1201/9781315370279 (Boca Raton, 2017).
Wood, S. N., Pya, N. & Saefken, B. Smoothing parameter and model selection for general smooth models (with discussion). J. Am. Stat. Asoc. 111(516), 1548–1575. https://doi.org/10.1080/01621459.2016.1180986 (2016).
doi: 10.1080/01621459.2016.1180986
Almon, Sh. The distributed lag between capital appropriations and net expenditures. Econometrica 33, 178–196. https://doi.org/10.2307/1911894 (1965).
doi: 10.2307/1911894
Brabec, M. Semiparametric Model for Short Term Effects of Air Pollution Upon Asthma Symptoms Exacerbations 26–30 (Joint ISCB/ASC Meeting, 2018).
Judge, G. G., Griffiths, W. E., Hill, R. C. & Lee, T.-C. The Theory and Practice of Econometrics (Wiley, 1980).
R Core Team. R: A Language and Environment for Statistical Computing. https://www.r-project.org/ (R Foundation for Statistical Computing, 2023).
Rocznik Demograficzny 2023 (Główny Urząd Statystyczny, 2023). https://stat.gov.pl/obszary-tematyczne/roczniki-statystyczne/roczniki-statystyczne/rocznik-demograficzny-2023,3,17.html . Accessed 16 June 2024 (2023).
Weng, Y. H., Yang, C. Y. & Chiu, Y. W. Neonatal outcomes in relation to sex differences: A national cohort survey in Taiwan. Biol. Sex Differ. 6, 30. https://doi.org/10.1186/s13293-015-0052-8 (2015).
doi: 10.1186/s13293-015-0052-8
pubmed: 26664663
pmcid: 4675056
Bohn, C. et al. Birth weight increases with birth order despite decreasing maternal pregnancy weight gain. Acta Paediatr. 110, 1218–1224. https://doi.org/10.1111/apa.15598 (2021).
doi: 10.1111/apa.15598
pubmed: 32981144
Chahnazarian, A. Determinants of the sex ratio at birth: Review of recent literature. Soc. Biol. 35(3–4), 214–235. https://doi.org/10.1080/19485565.1988.9988703 (1988).
doi: 10.1080/19485565.1988.9988703
pubmed: 3071849
Liczbińska, G. & Sobkowiak, A. Did the sex ratio at birth reflect social and economic inequalities? A pilot study of the Province of Poznań, 1875–1913. Poland’s Demogr.Past (Przeszłość Demograficzna Polski) 42, 95–121. https://doi.org/10.18276/pdp.2020.42-04 (2020).
doi: 10.18276/pdp.2020.42-04
Ruckstuhl, K. E., Colijn, G. P., Amiot, V. & Vinish, E. Mother’s occupation and sex ratio at birth. BMC Pub. Health 10, 269. https://doi.org/10.1186/1471-2458-10-269 (2010).
doi: 10.1186/1471-2458-10-269