Skip to main content

Advertisement

SpringerLink
Log in

Association between maternal exposure to air pollution before conception and sex determination in the city of São Paulo

  • Published:
Air Quality, Atmosphere & Health Aims and scope Submit manuscript

Abstract

It has been widely demonstrated that air pollution can affect human health and that some pollutant gases can have negative impacts on female fertility rates and cause adverse obstetric outcomes, such as premature birth and low birth weight. Few studies have evaluated the impact of maternal exposure to urban air pollution on the number of female births. To evaluate the association between maternal exposure to air pollution during the year before conception and sex determination. This was a prospective study using low-risk pregnant women living in Sao Paulo, Brazil. The pollutants were measured by a fixed station during a 1-year period before conception. Sex was confirmed after birth. We used multiple logistic regression models to evaluate the association between the pollutants and the sex determination and to estimate the odds ratio (OR) and the 95% confidence interval (CI) of being female based on a quantitative increase in pollutant concentration. We evaluated 371 patients. Elevated exposure to nitrogen dioxide (NO2) and particulate matter lower than 10 μm (PM10) prior to conception were associated with increased odds of being female. Each unit increase of NO2 exposure increased the odds of being female by 8% (OR = 1.08, 95% CI = 1.02, 1.15, p = 0.008), and each unit increase of PM10 increased the odds of being female by 14% (OR = 1.14, 95% CI 1.02 to 1.28, p = 0.021). In Sao Paulo, maternal exposure to pollutants was significantly associated with the odds of being female.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

CAPES:

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior

CETESB:

Companhia Ambiental do Estado de São Paulo

CI:

Confidence interval

FAPESP:

São Paulo Research Foundation

NO2 :

Nitrogen dioxide

OR:

Odds ratio

PM:

Particulate matter

PM10 :

PM lower than 10 μg

References

  • Andrade MF, Miranda RM, Fornaro A et al (2012) Vehicle emissions and PM2.5 mass concentrations in six Brazilian cities. Air Qual Atmosphere Health 5(1):79–88

  • Arbex MA, Saldiva PH, Pereira LA, Braga AL (2010) Impact of outdoor biomass air pollution on hypertension hospital admissions. J Epidemiol Community Health 64(7):573–579

    Google Scholar 

  • Beelen R, Stafoggia M, Raaschou-Nielsen O, Andersen ZJ, Xun WW, Katsouyanni K, Dimakopoulou K, Brunekreef B, Weinmayr G, Hoffmann B, Wolf K, Samoli E, Houthuijs D, Nieuwenhuijsen M, Oudin A, Forsberg B, Olsson D, Salomaa V, Lanki T, Yli-Tuomi T, Oftedal B, Aamodt G, Nafstad P, de Faire U, Pedersen NL, Östenson CG, Fratiglioni L, Penell J, Korek M, Pyko A, Eriksen KT, Tjønneland A, Becker T, Eeftens M, Bots M, Meliefste K, Wang M, Bueno-de-Mesquita B, Sugiri D, Krämer U, Heinrich J, de Hoogh K, Key T, Peters A, Cyrys J, Concin H, Nagel G, Ineichen A, Schaffner E, Probst-Hensch N, Dratva J, Ducret-Stich R, Vilier A, Clavel-Chapelon F, Stempfelet M, Grioni S, Krogh V, Tsai MY, Marcon A, Ricceri F, Sacerdote C, Galassi C, Migliore E, Ranzi A, Cesaroni G, Badaloni C, Forastiere F, Tamayo I, Amiano P, Dorronsoro M, Katsoulis M, Trichopoulou A, Vineis P, Hoek G (2014) Long-term exposure to air pollution and cardiovascular mortality: an analysis of 22 European cohorts. Epidemiology. 25(3):368–378

    Google Scholar 

  • Beiguelman B, Franchi-Pinto C, Dal Colletto GM, Krieger H (1995) Annual variation of sex ratio in twin births and in singletons in Brazil. Acta Genet Med Gemellol 44(3–4):163–168

    CAS  Google Scholar 

  • Bruckner TA, Catalano R, Ahern J. Male fetal loss in the U.S. following the terrorist attacks of September 11, 2001. BMC Public Health. 2010;10:273

  • Carvalho MA, Bernardes LS, Hettfleisch K, Pastro LD, Vieira SE, Saldiva SR et al (2016) Associations of maternal personal exposure to air pollution on fetal weight and fetoplacental Doppler: a prospective cohort study. Reprod Toxicol 62:9–17

    CAS  Google Scholar 

  • CETESB. Qualidade do ar no estado de São Paulo 2014. São Paulo2015

  • CETESB. Qualidade do ar no estado de São Paulo 2016a [recurso eletrônico] / CETESB ;. In: Martins CaogMHRB, ramoto CaotcCAM-, al.] EtcMHRBMe, editors. 2017

  • CETESB. CLASSIFICAÇÃO EXPEDITA DA REPRESENTATIVIDADE ESPACIAL DAS ESTAÇÕES DE MONITORAMENTO DA QUALIDADE DO AR DA CETESB NO ESTADO DE SÃO PAULO: TERCEIRA ETAPA. 2016b. p. 1–29

  • Chahnazarian A (1988) Determinants of the sex ratio at birth: review of recent literature. Soc Biol 35(3–4):214–235

    CAS  Google Scholar 

  • Cocco P, Fadda D, Ibba A, Melis M, Tocco MG, Atzeri S, Avataneo G, Meloni M, Monni F, Flore C (2005) Reproductive outcomes in DDT applicators. Environ Res 98(1):120–126

    CAS  Google Scholar 

  • Conceição GM, Miraglia SG, Kishi HS, Saldiva PH, Singer JM (2001) Air pollution and child mortality: a time-series study in São Paulo, Brazil. Environ Health Perspect 109(Suppl 3):347–350

    Google Scholar 

  • Conforti A, Mascia M, Cioffi G, De Angelis C, Coppola G, De Rosa P et al (2018) Air pollution and female fertility: a systematic review of literature. Reprod Biol Endocrinol 16(1):117

    CAS  Google Scholar 

  • Davis DL, Gottlieb MB, Stampnitzky JRReduced ratio of male to female births in seve1998ral industrial countries: a sentinel health indicator? JAMA. 279(13):1018–1023

  • Davis DL, Webster P, Stainthorpe H, Chilton J, Jones L, Doi R (2007) Declines in sex ratio at birth and fetal deaths in Japan, and in U.S. whites but not African Americans. Environ Health Perspect 115(6):941–946

    Google Scholar 

  • Erickson JD (1976) The secondary sex ratio in the United States 1969-71: association with race, parental ages, birth order, paternal education and legitimacy. Ann Hum Genet 40(2):205–212

    CAS  Google Scholar 

  • Estors Sastre B, Bragagnini Rodríguez P, Fernández Atuan R, Delgado Alvira R, Rihuete Heras MA, Gracia RJ (2015) Endocrine disrupting chemicals exposure and other parental factors in hypospadias and cryptorchidism etiology. Cir Pediatr 28(3):128–132

    CAS  Google Scholar 

  • Finger C. Caesarean section rates skyrocket in Brazil. Many women are opting for caesareans in the belief that it is a practical solution. Lancet. 2003;362(9384):628

  • Frutos V, González-Comadrán M, Solà I, Jacquemin B, Carreras R, Checa Vizcaíno MA (2015) Impact of air pollution on fertility: a systematic review. Gynecol Endocrinol 31(1):7–13

    CAS  Google Scholar 

  • Fukuda M, Fukuda K, Shimizu T, Andersen CY, Byskov AG (2002) Parental periconceptional smoking and male: female ratio of newborn infants. Lancet. 359(9315):1407–1408

    Google Scholar 

  • Gloria-Bottini F, Bottini N, La Torre M, Magrini A, Bergamaschi A, Bottini E (2008) The effects of genetic and seasonal factors on reproductive success. Fertil Steril 89(5):1090–1094

    Google Scholar 

  • Gloria-Bottini F, Neri A, Pietropolli A, Bottini E, Magrini A (2013) Ak(1) genetic polymorphism and season of conception. Eur J Obstet Gynecol Reprod Biol 166(2):161–163

    CAS  Google Scholar 

  • Hadlock FP, Harrist RB, Sharman RS, Deter RL, Park SK (1985) Estimation of fetal weight with the use of head, body, and femur measurements--a prospective study. Am J Obstet Gynecol 151(3):333–337

    CAS  Google Scholar 

  • Hadlock FP, Shah YP, Kanon DJ, Lindsey JV (1992) Fetal crown-rump length: reevaluation of relation to menstrual age (5-18 weeks) with high-resolution real-time US. Radiology. 182(2):501–505

    CAS  Google Scholar 

  • Hansen C, Neller A, Williams G, Simpson R. Maternal exposure to low levels of ambient air pollution and preterm birth in Brisbane, Australia. BJOG 2006;113(8):935–941

  • James WH (1984) Seasonality in the sex ratio of US black births. Ann Hum Biol 11(1):67–69

    CAS  Google Scholar 

  • Jongbloet PH. Seasonal fluctuation of pathological and optimum conceptions, maternal sub-fecundity, gender dimorphism and survival. Coll Anthropol; 1999. p. 99–107

  • Jongbloet PH, Groenewoud JM, Zielhuis GA (1996) Further concepts on regulators of the sex ratio in human offspring. Non-optimal maturation of oocytes and the sex ratio. Hum Reprod 11(1):2–7

    CAS  Google Scholar 

  • Koshy G, Delpisheh A, Brabin L, Attia E, Brabin BJ (2010) Parental smoking and increased likelihood of female births. Ann Hum Biol 37(6):789–800

    Google Scholar 

  • Lerchl A (1998) Seasonality of sex ratio in Germany. Hum Reprod 13(5):1401–1402

    CAS  Google Scholar 

  • Lichtenfels AJ, Gomes JB, Pieri PC, El Khouri Miraglia SG, Hallak J, Saldiva PH. Increased levels of air pollution and a decrease in the human and mouse male-to-female ratio in São Paulo, Brazil. Fertil Steril 2007;87(1):230–232

  • Liu S, Krewski D, Shi Y, Chen Y, Burnett RT. Association between gaseous ambient air pollutants and adverse pregnancy outcomes in Vancouver, Canada. Environ Health Perspect 2003;111(14):1773–1778

  • Lummaa V. Seasonality of births in Homo sapiens in pre-industrial Finland: maximisation of offspring survivorship? In: Lemmetyinen R, editor.: J Evol Biol; 1998. p. 147–57

  • Machado CM, Cardoso AA, Allen AG (2008) Atmospheric emission of reactive nitrogen during biofuel ethanol production. Environ Sci Technol 42(2):381–385

    CAS  Google Scholar 

  • Melnikov VN (2015) Seasonal inconstancy of human sex ratio at birth. Early Hum Dev 91(12):817–821

    Google Scholar 

  • Miraglia SG, Veras MM, Amato-Lourenço LF, Rodrigues-Silva F, Saldiva PH. Follow-up of the air pollution and the human male-to-female ratio analysis in Sao Paulo, Brazil: a times series study. BMJ Open. 2013;3(7)

  • Mnatzaganian CL, Pellegrin KL, Miyamura J, Valencia D, Pang L (2015) Association between sugar cane burning and acute respiratory illness on the island of Maui. Environ Health 14:81

    Google Scholar 

  • Nonaka K, Desjardins B, Charbonneau Hea. Seasonality of general births and secondary sex ratio in the 17th and 18th century Canadian population. Triennial Rep; 1991. p. 8–15

  • Parazzini F, Chatenoud L, Maffioletti C, Chiaffarino F, Caserta D (2005) Periconceptional smoking and male:female ratio of newborns. Eur J Pub Health 15(6):613–614

    Google Scholar 

  • Pedersen M, Giorgis-Allemand L, Bernard C, Aguilera I, Andersen AM, Ballester F et al (2013) Ambient air pollution and low birthweight: a European cohort study (ESCAPE). Lancet Respir Med 1(9):695–704

    CAS  Google Scholar 

  • Pires A, de Melo EN, Mauad T, Nascimento Saldiva PH, de Siqueira Bueno HM (2011) Pre- and postnatal exposure to ambient levels of urban particulate matter (PM(2.5)) affects mice spermatogenesis. Inhal Toxicol 23(4):237–245

    CAS  Google Scholar 

  • Quinn A, Koopman P (2012) The molecular genetics of sex determination and sex reversal in mammals. Semin Reprod Med 30(5):351–363

    CAS  Google Scholar 

  • R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

  • Radwan M, Dziewirska E, Radwan P, Jakubowski L, Hanke W, Jurewicz J (2018) Air pollution and human sperm sex ratio. Am J Mens Health 1557988317752608

  • Ruder A (1985) Paternal-age and birth-order effect on the human secondary sex ratio. Am J Hum Genet 37(2):362–372

    CAS  Google Scholar 

  • Ryan JJ, Amirova Z, Carrier G (2002) Sex ratios of children of Russian pesticide producers exposed to dioxin. Environ Health Perspect 110(11):A699–A701

    Google Scholar 

  • Schnorr TM, Lawson CC, Whelan EA, Dankovic DA, Deddens JA, Piacitelli LA, Reefhuis J, Sweeney MH, Connally LB, Fingerhut MA (2001) Spontaneous abortion, sex ratio, and paternal occupational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Environ Health Perspect 109(11):1127–1132

    CAS  Google Scholar 

  • Seade F. http://www.seade.gov.br/produtos/pib/index.php (acessed 13 Ago 2018)

  • Sharpe RM (2010) Environmental/lifestyle effects on spermatogenesis. Philos Trans R Soc Lond Ser B Biol Sci 365(1546):1697–1712

    CAS  Google Scholar 

  • Skakkebaek NE, Rajpert-De Meyts E, Main KM (2001) Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum Reprod 16(5):972–978

    CAS  Google Scholar 

  • Sørensen M, Lühdorf P, Ketzel M, Andersen ZJ, Tjønneland A, Overvad K, Raaschou-Nielsen O (2014) Combined effects of road traffic noise and ambient air pollution in relation to risk for stroke? Environ Res 133:49–55

    Google Scholar 

  • Stuppia L, Franzago M, Ballerini P, Gatta V, Antonucci I (2015) Epigenetics and male reproduction: the consequences of paternal lifestyle on fertility, embryo development, and children lifetime health. Clin Epigenetics 7:120

    Google Scholar 

  • Swan SH, Elkin EP, Fenster L (2000) The question of declining sperm density revisited: an analysis of 101 studies published 1934-1996. Environ Health Perspect 108(10):961–966

    CAS  Google Scholar 

  • Terrell ML. Can environmental or occupational hazards alter the sex ratio at birth? A systematic review. In: Hartnett KP, editor.: Emerging Health Threats Journal; 2011

  • Tragaki A. Temporal and spatial trends in the sex ratio at birth in Greece, 1960–2006: exploring potential environmental factors. In: Lasaridi K, editor.: Popul Environ; 2009. p. 114–28

  • van Larebeke NA, Sasco AJ, Brophy JT, Keith MM, Gilbertson M, Watterson A (2008) Sex ratio changes as sentinel health events of endocrine disruption. Int J Occup Environ Health 14(2):138–143

    Google Scholar 

  • Virtanen HE, Adamsson A (2012) Cryptorchidism and endocrine disrupting chemicals. Mol Cell Endocrinol 355(2):208–220

    CAS  Google Scholar 

  • Williams FL, Lawson AB, Lloyd OL (1992) Low sex ratios of births in areas at risk from air pollution from incinerators, as shown by geographical analysis and 3-dimensional mapping. Int J Epidemiol 21(2):311–319

    CAS  Google Scholar 

  • Yang CY, Tsai SS, Cheng BH, Hsu TY, Wu TN (2000) Sex ratio at birth associated with petrochemical air pollution in Taiwan. Bull Environ Contam Toxicol 65(1):126–131

    CAS  Google Scholar 

Download references

Acknowledgments

The authors acknowledge the following institutions: São Paulo Research Foundation (FAPESP) and CETESB (Companhia Ambiental do Estado de São Paulo).

Funding

This research was supported by grants 2008/57717-6, São Paulo Research Foundation (FAPESP), and by grants 2016/14433-4, FAPESP. This study was also financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001.

Author information

Authors and Affiliations

  1. Faculdade de Medicina FMUSP, Universidade de Sao Paulo, Av. Dr. Enéas de Carvalho Aguiar, Sao Paulo, SP, 05403-900, Brazil

    Mariana Azevedo Carvalho, Karen Hettfleisch, Agatha S Rodrigues, Rossana Pulcineli Vieira Francisco & Lisandra Stein Bernardes

  2. Department of Statistics, Federal University of Espírito Santo, Vitória, ES, Brazil

    Agatha S Rodrigues

  3. Department of Ob-GYN and Reproductive Medecine, Antoine Beclere Hospital, Assistance Publique-Hopitaux de Paris, 92141, Clamart, France

    Alexandra Benachi

  4. Department of Pediatrics, São Paulo University Medical School, 255, Av. Dr. Enéas de Carvalho Aguiar, São Paulo, Brazil

    Sandra Elisabete Vieira

  5. Health Institute, 590, Rua Santo Antônio, São Paulo, Brazil

    Silvia R D M Saldiva

  6. Institute of Advanced Studies, University of São Paulo, 455, Av. Dr Arnaldo, São Paulo, Brazil

    Paulo Hilário N. Saldiva

Authors
  1. Mariana Azevedo Carvalho
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Karen Hettfleisch
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Agatha S Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alexandra Benachi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sandra Elisabete Vieira
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Silvia R D M Saldiva
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Paulo Hilário N. Saldiva
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Rossana Pulcineli Vieira Francisco
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Lisandra Stein Bernardes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lisandra Stein Bernardes.

Ethics declarations

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Carvalho, M.A., Hettfleisch, K., Rodrigues, A.S. et al. Association between maternal exposure to air pollution before conception and sex determination in the city of São Paulo. Air Qual Atmos Health 13, 1203–1210 (2020). https://doi.org/10.1007/s11869-020-00873-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11869-020-00873-z

Keywords

Search

Navigation