Environmental exposure to industrial air pollution is associated with decreased male fertility

Joemy M. Ramsay; Kiarad Fendereski; Joshua J. Horns; James A. VanDerslice; Heidi A. Hanson; Benjamin R. Emery; Joshua A. Halpern; Kenneth I. Aston; Elisabeth Ferlic; James M. Hotaling

doi:10.1016/j.fertnstert.2023.05.143

Environmental exposure to industrial air pollution is associated with decreased male fertility

Joemy M. Ramsay
, Kiarad Fendereski
, Joshua J. Horns
, James A. VanDerslice
, Heidi A. Hanson
, Benjamin R. Emery
, Joshua A. Halpern
, Kenneth I. Aston
, Elisabeth Ferlic
, James M. Hotaling

Biostatistics and Biomedical Informatics

Research output: Contribution to journal › Article › peer-review

32 Scopus citations

Abstract

Objective: To understand how chronic exposure to industrial air pollution is associated with male fertility through semen parameters. Design: Retrospective cohort study. Patients: Men in the Subfertility, Health, and Assisted Reproduction cohort who underwent a semen analysis in the two largest healthcare systems in Utah from 2005–2017 with ≥1 measured semen parameter (N = 21,563). Intervention(s): Residential histories for each man were constructed using locations from administrative records linked through the Utah Population Database. Industrial facilities with air emissions of nine endocrine-disrupting compound chemical classes were identified from the Environmental Protection Agency Risk-Screening Environmental Indicators microdata. Chemical levels were linked with residential histories for the 5 years before each semen analysis. Main Outcome Measures: Semen analyses were classified as azoospermic or oligozoospermic (< 15 M/mL) using World Health Organization cutoffs for concentration. Bulk semen parameters such as concentration, total count, ejaculate volume, total motility, total motile count, and total progressive motile count were also measured. Multivariable regression models with robust standard errors were used to associate exposure quartiles for each of the nine chemical classes with each semen parameter, adjusting for age, race, and ethnicity, as well as neighborhood socioeconomic disadvantage. Results: After adjustment for demographic covariates, several chemical classes were associated with azoospermia and decreased total motility and volume. For exposure in the 4th relative to 1st quartile, significant associations were observed for acrylonitrile (β_{total motility} = −0.87 pp), aromatic hydrocarbons (odds ratio [OR]_azoospermia = 1.53; β_volume = −0.14 mL), dioxins (OR_azoospermia = 1.31; β_volume = −0.09 mL; β_{total motility} = −2.65 pp), heavy metals (β_{total motility} = −2.78pp), organic solvents (OR_azoospermia = 1.75; β_volume = −0.10 mL), organochlorines (OR_azoospermia = 2.09; β_volume = −0.12 mL), phthalates (OR_azoospermia = 1.44; β_volume = −0.09 mL; β_{total motility} = −1.21 pp), and silver particles (OR_azoospermia = 1.64; β_volume = −0.11 mL). All semen parameters significantly decreased with increasing socioeconomic disadvantage. Men who lived in the most disadvantaged areas had concentration, volume, and total motility of 6.70 M/mL, 0.13 mL, and 1.79 pp lower, respectively. Count, motile count, and total progressive motile count all decreased by 30–34 M. Conclusion(s): Several significant associations between chronic low-level environmental exposure to endocrine-disrupting compound air pollution from industrial sources and semen parameters were observed. The strongest associations were seen for increased odds of azoospermia and declines in total motility and volume. More research is needed to further explore additional social and exposure factors as well as expand on the risk posed to male reproductive health by the studied chemicals.

Original language	English
Pages (from-to)	637-647
Number of pages	11
Journal	Fertility and Sterility
Volume	120
Issue number	3
DOIs	https://doi.org/10.1016/j.fertnstert.2023.05.143
State	Published - Sep 2023

Funding

With thanks to the Pedigree and Population Resource of the Huntsman Cancer Institute , the University of Utah (funded in part by the Huntsman Cancer Foundation ) for its role in the ongoing collection, maintenance, and support of the Utah Population Database (UPDB). We also acknowledge partial support for the UPDB through grant P30 CA2014 from the National Cancer Institute , the University of Utah , and the University of Utah’s program in personalized health and the Center for Clinical and Translational Science . Supported by GEMS: Genomic approach to connecting Elevated germline Mutation rates with male infertility and Somatic health (NICHD: R01 HD106112). The University of Utah Center for Clinical and Translational Science (funded by NIH Clinical and Translational Science Awards), the Pedigree and Population Resource, University of Utah Information Technology Services, and Biomedical Informatics Core for establishing the Master Subject Index between the Utah Population Database, the University of Utah Health Sciences Center, and Intermountain Healthcare . The research was also supported by the NCRR grant “Sharing Statewide Health Data for Genetic Research” (R01 RR021746, G. Mineau, PI), with additional support from the Utah Department of Health and Human Services and the University of Utah . With thanks to the Pedigree and Population Resource of the Huntsman Cancer Institute, the University of Utah (funded in part by the Huntsman Cancer Foundation) for its role in the ongoing collection, maintenance, and support of the Utah Population Database (UPDB). We also acknowledge partial support for the UPDB through grant P30 CA2014 from the National Cancer Institute, the University of Utah, and the University of Utah's program in personalized health and the Center for Clinical and Translational Science. The University of Utah Center for Clinical and Translational Science (funded by NIH Clinical and Translational Science Awards), the Pedigree and Population Resource, University of Utah Information Technology Services, and Biomedical Informatics Core for establishing the Master Subject Index between the Utah Population Database, the University of Utah Health Sciences Center, and Intermountain Healthcare. The research was also supported by the NCRR grant “Sharing Statewide Health Data for Genetic Research” (R01 RR021746, G. Mineau, PI), with additional support from the Utah Department of Health and Human Services and the University of Utah.

Keywords

Male fertility
air pollution
endocrine-disrupting compounds
environmental exposure
semen analysis

Access to Document

10.1016/j.fertnstert.2023.05.143

Cite this

@article{21941e1791144d11be8adc1fd877335d,

title = "Environmental exposure to industrial air pollution is associated with decreased male fertility",

abstract = "Objective: To understand how chronic exposure to industrial air pollution is associated with male fertility through semen parameters. Design: Retrospective cohort study. Patients: Men in the Subfertility, Health, and Assisted Reproduction cohort who underwent a semen analysis in the two largest healthcare systems in Utah from 2005–2017 with ≥1 measured semen parameter (N = 21,563). Intervention(s): Residential histories for each man were constructed using locations from administrative records linked through the Utah Population Database. Industrial facilities with air emissions of nine endocrine-disrupting compound chemical classes were identified from the Environmental Protection Agency Risk-Screening Environmental Indicators microdata. Chemical levels were linked with residential histories for the 5 years before each semen analysis. Main Outcome Measures: Semen analyses were classified as azoospermic or oligozoospermic (< 15 M/mL) using World Health Organization cutoffs for concentration. Bulk semen parameters such as concentration, total count, ejaculate volume, total motility, total motile count, and total progressive motile count were also measured. Multivariable regression models with robust standard errors were used to associate exposure quartiles for each of the nine chemical classes with each semen parameter, adjusting for age, race, and ethnicity, as well as neighborhood socioeconomic disadvantage. Results: After adjustment for demographic covariates, several chemical classes were associated with azoospermia and decreased total motility and volume. For exposure in the 4th relative to 1st quartile, significant associations were observed for acrylonitrile (βtotal motility = −0.87 pp), aromatic hydrocarbons (odds ratio [OR]azoospermia = 1.53; βvolume = −0.14 mL), dioxins (ORazoospermia = 1.31; βvolume = −0.09 mL; βtotal motility = −2.65 pp), heavy metals (βtotal motility = −2.78pp), organic solvents (ORazoospermia = 1.75; βvolume = −0.10 mL), organochlorines (ORazoospermia = 2.09; βvolume = −0.12 mL), phthalates (ORazoospermia = 1.44; βvolume = −0.09 mL; βtotal motility = −1.21 pp), and silver particles (ORazoospermia = 1.64; βvolume = −0.11 mL). All semen parameters significantly decreased with increasing socioeconomic disadvantage. Men who lived in the most disadvantaged areas had concentration, volume, and total motility of 6.70 M/mL, 0.13 mL, and 1.79 pp lower, respectively. Count, motile count, and total progressive motile count all decreased by 30–34 M. Conclusion(s): Several significant associations between chronic low-level environmental exposure to endocrine-disrupting compound air pollution from industrial sources and semen parameters were observed. The strongest associations were seen for increased odds of azoospermia and declines in total motility and volume. More research is needed to further explore additional social and exposure factors as well as expand on the risk posed to male reproductive health by the studied chemicals.",

keywords = "Male fertility, air pollution, endocrine-disrupting compounds, environmental exposure, semen analysis",

author = "Ramsay, \{Joemy M.\} and Kiarad Fendereski and Horns, \{Joshua J.\} and VanDerslice, \{James A.\} and Hanson, \{Heidi A.\} and Emery, \{Benjamin R.\} and Halpern, \{Joshua A.\} and Aston, \{Kenneth I.\} and Elisabeth Ferlic and Hotaling, \{James M.\}",

note = "Publisher Copyright: {\textcopyright} 2023 American Society for Reproductive Medicine",

year = "2023",

month = sep,

doi = "10.1016/j.fertnstert.2023.05.143",

language = "English",

volume = "120",

pages = "637--647",

journal = "Fertility and Sterility",

issn = "0015-0282",

number = "3",

}

TY - JOUR

T1 - Environmental exposure to industrial air pollution is associated with decreased male fertility

AU - Ramsay, Joemy M.

AU - Fendereski, Kiarad

AU - Horns, Joshua J.

AU - VanDerslice, James A.

AU - Hanson, Heidi A.

AU - Emery, Benjamin R.

AU - Halpern, Joshua A.

AU - Aston, Kenneth I.

AU - Ferlic, Elisabeth

AU - Hotaling, James M.

PY - 2023/9

Y1 - 2023/9

N2 - Objective: To understand how chronic exposure to industrial air pollution is associated with male fertility through semen parameters. Design: Retrospective cohort study. Patients: Men in the Subfertility, Health, and Assisted Reproduction cohort who underwent a semen analysis in the two largest healthcare systems in Utah from 2005–2017 with ≥1 measured semen parameter (N = 21,563). Intervention(s): Residential histories for each man were constructed using locations from administrative records linked through the Utah Population Database. Industrial facilities with air emissions of nine endocrine-disrupting compound chemical classes were identified from the Environmental Protection Agency Risk-Screening Environmental Indicators microdata. Chemical levels were linked with residential histories for the 5 years before each semen analysis. Main Outcome Measures: Semen analyses were classified as azoospermic or oligozoospermic (< 15 M/mL) using World Health Organization cutoffs for concentration. Bulk semen parameters such as concentration, total count, ejaculate volume, total motility, total motile count, and total progressive motile count were also measured. Multivariable regression models with robust standard errors were used to associate exposure quartiles for each of the nine chemical classes with each semen parameter, adjusting for age, race, and ethnicity, as well as neighborhood socioeconomic disadvantage. Results: After adjustment for demographic covariates, several chemical classes were associated with azoospermia and decreased total motility and volume. For exposure in the 4th relative to 1st quartile, significant associations were observed for acrylonitrile (βtotal motility = −0.87 pp), aromatic hydrocarbons (odds ratio [OR]azoospermia = 1.53; βvolume = −0.14 mL), dioxins (ORazoospermia = 1.31; βvolume = −0.09 mL; βtotal motility = −2.65 pp), heavy metals (βtotal motility = −2.78pp), organic solvents (ORazoospermia = 1.75; βvolume = −0.10 mL), organochlorines (ORazoospermia = 2.09; βvolume = −0.12 mL), phthalates (ORazoospermia = 1.44; βvolume = −0.09 mL; βtotal motility = −1.21 pp), and silver particles (ORazoospermia = 1.64; βvolume = −0.11 mL). All semen parameters significantly decreased with increasing socioeconomic disadvantage. Men who lived in the most disadvantaged areas had concentration, volume, and total motility of 6.70 M/mL, 0.13 mL, and 1.79 pp lower, respectively. Count, motile count, and total progressive motile count all decreased by 30–34 M. Conclusion(s): Several significant associations between chronic low-level environmental exposure to endocrine-disrupting compound air pollution from industrial sources and semen parameters were observed. The strongest associations were seen for increased odds of azoospermia and declines in total motility and volume. More research is needed to further explore additional social and exposure factors as well as expand on the risk posed to male reproductive health by the studied chemicals.

AB - Objective: To understand how chronic exposure to industrial air pollution is associated with male fertility through semen parameters. Design: Retrospective cohort study. Patients: Men in the Subfertility, Health, and Assisted Reproduction cohort who underwent a semen analysis in the two largest healthcare systems in Utah from 2005–2017 with ≥1 measured semen parameter (N = 21,563). Intervention(s): Residential histories for each man were constructed using locations from administrative records linked through the Utah Population Database. Industrial facilities with air emissions of nine endocrine-disrupting compound chemical classes were identified from the Environmental Protection Agency Risk-Screening Environmental Indicators microdata. Chemical levels were linked with residential histories for the 5 years before each semen analysis. Main Outcome Measures: Semen analyses were classified as azoospermic or oligozoospermic (< 15 M/mL) using World Health Organization cutoffs for concentration. Bulk semen parameters such as concentration, total count, ejaculate volume, total motility, total motile count, and total progressive motile count were also measured. Multivariable regression models with robust standard errors were used to associate exposure quartiles for each of the nine chemical classes with each semen parameter, adjusting for age, race, and ethnicity, as well as neighborhood socioeconomic disadvantage. Results: After adjustment for demographic covariates, several chemical classes were associated with azoospermia and decreased total motility and volume. For exposure in the 4th relative to 1st quartile, significant associations were observed for acrylonitrile (βtotal motility = −0.87 pp), aromatic hydrocarbons (odds ratio [OR]azoospermia = 1.53; βvolume = −0.14 mL), dioxins (ORazoospermia = 1.31; βvolume = −0.09 mL; βtotal motility = −2.65 pp), heavy metals (βtotal motility = −2.78pp), organic solvents (ORazoospermia = 1.75; βvolume = −0.10 mL), organochlorines (ORazoospermia = 2.09; βvolume = −0.12 mL), phthalates (ORazoospermia = 1.44; βvolume = −0.09 mL; βtotal motility = −1.21 pp), and silver particles (ORazoospermia = 1.64; βvolume = −0.11 mL). All semen parameters significantly decreased with increasing socioeconomic disadvantage. Men who lived in the most disadvantaged areas had concentration, volume, and total motility of 6.70 M/mL, 0.13 mL, and 1.79 pp lower, respectively. Count, motile count, and total progressive motile count all decreased by 30–34 M. Conclusion(s): Several significant associations between chronic low-level environmental exposure to endocrine-disrupting compound air pollution from industrial sources and semen parameters were observed. The strongest associations were seen for increased odds of azoospermia and declines in total motility and volume. More research is needed to further explore additional social and exposure factors as well as expand on the risk posed to male reproductive health by the studied chemicals.

KW - Male fertility

KW - air pollution

KW - endocrine-disrupting compounds

KW - environmental exposure

KW - semen analysis

UR - https://www.scopus.com/pages/publications/85165699320

U2 - 10.1016/j.fertnstert.2023.05.143

DO - 10.1016/j.fertnstert.2023.05.143

M3 - Article

C2 - 37196750

AN - SCOPUS:85165699320

SN - 0015-0282

VL - 120

SP - 637

EP - 647

JO - Fertility and Sterility

JF - Fertility and Sterility

IS - 3

ER -

Environmental exposure to industrial air pollution is associated with decreased male fertility

Abstract

Funding

Keywords

Access to Document

Other files and links

Fingerprint

Cite this