Using follicular fluid metabolomics to investigate the association between air pollution and oocyte quality
Background and aim: Our objective was to use metabolomics in a toxicological-relevant target tissue to gain insight into the biological processes that may underlie the negative association between air pollution exposure and oocyte quality. Methods: Our study included 125 women undergoing in vitro fe...
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Elsevier
2022-11-01
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Series: | Environment International |
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Online Access: | http://www.sciencedirect.com/science/article/pii/S0160412022004792 |
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author | Sueyoun Hwang Robert B. Hood Russ Hauser Joel Schwartz Francine Laden Dean Jones Donghai Liang Audrey J. Gaskins |
author_facet | Sueyoun Hwang Robert B. Hood Russ Hauser Joel Schwartz Francine Laden Dean Jones Donghai Liang Audrey J. Gaskins |
author_sort | Sueyoun Hwang |
collection | DOAJ |
description | Background and aim: Our objective was to use metabolomics in a toxicological-relevant target tissue to gain insight into the biological processes that may underlie the negative association between air pollution exposure and oocyte quality. Methods: Our study included 125 women undergoing in vitro fertilization at an academic fertility center in Massachusetts, US (2005–2015). A follicular fluid sample was collected during oocyte retrieval and untargeted metabolic profiling was conducted using liquid chromatography with ultra-high-resolution mass spectrometry and two chromatography columns (C18 and HILIC). Daily exposure to nitrogen dioxide (NO2), ozone, fine particulate matter, and black carbon was estimated at the women’s residence using spatiotemporal models and averaged over the period of ovarian stimulation (2-weeks). Multivariable linear regression models were used to evaluate the associations between the air pollutants, number of mature oocytes, and metabolic feature intensities. A meet-in-the-middle approach was used to identify overlapping features and metabolic pathways. Results: Of the air pollutants, NO2 exposure had the largest number of overlapping metabolites (C18: 105; HILIC: 91) and biological pathways (C18: 3; HILIC: 6) with number of mature oocytes. Key pathways of overlap included vitamin D3 metabolism (both columns), bile acid biosynthesis (both columns), C21-steroid hormone metabolism (HILIC), androgen and estrogen metabolism (HILIC), vitamin A metabolism (HILIC), carnitine shuttle (HILIC), and prostaglandin formation (C18). Three overlapping metabolites were confirmed with level-1 or level-2 evidence. For example, hypoxanthine, a metabolite that protects against oxidant-induced cell injury, was positively associated with NO2 exposure and negatively associated with number of mature oocytes. Minimal overlap was observed between the other pollutants and the number of mature oocytes. Conclusions: Higher exposure to NO2 during ovarian stimulation was associated with many metabolites and biologic pathways involved in endogenous vitamin metabolism, hormone synthesis, and oxidative stress that may mediate the observed associations with lower oocyte quality. |
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language | English |
last_indexed | 2024-04-12T09:31:26Z |
publishDate | 2022-11-01 |
publisher | Elsevier |
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series | Environment International |
spelling | doaj.art-851b4e7661ec41d19fc02b211805eedb2022-12-22T03:38:21ZengElsevierEnvironment International0160-41202022-11-01169107552Using follicular fluid metabolomics to investigate the association between air pollution and oocyte qualitySueyoun Hwang0Robert B. Hood1Russ Hauser2Joel Schwartz3Francine Laden4Dean Jones5Donghai Liang6Audrey J. Gaskins7Department of Epidemiology, Emory University Rollins School of Public Health, Atlanta, GA, United StatesDepartment of Epidemiology, Emory University Rollins School of Public Health, Atlanta, GA, United StatesDepartment of Environmental Health, Harvard T.H. Chan School of Public Health, Boston, MA, United States; Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, United StatesDepartment of Environmental Health, Harvard T.H. Chan School of Public Health, Boston, MA, United States; Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, United States; Channing Division of Network Medicine, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, United StatesDepartment of Environmental Health, Harvard T.H. Chan School of Public Health, Boston, MA, United States; Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, United States; Channing Division of Network Medicine, Harvard Medical School and Brigham and Women’s Hospital, Boston, MA, United StatesDivision of Pulmonary, Allergy, & Critical Care Medicine, Emory University School of Medicine, Atlanta, GA, United StatesGangarosa Department of Environmental Health, Emory University Rollins School of Public Health, Atlanta, GA, United StatesDepartment of Epidemiology, Emory University Rollins School of Public Health, Atlanta, GA, United States; Corresponding author at: Sc.D., 1518 Clifton Road, CNR 3017, Atlanta, GA 30322, United States.Background and aim: Our objective was to use metabolomics in a toxicological-relevant target tissue to gain insight into the biological processes that may underlie the negative association between air pollution exposure and oocyte quality. Methods: Our study included 125 women undergoing in vitro fertilization at an academic fertility center in Massachusetts, US (2005–2015). A follicular fluid sample was collected during oocyte retrieval and untargeted metabolic profiling was conducted using liquid chromatography with ultra-high-resolution mass spectrometry and two chromatography columns (C18 and HILIC). Daily exposure to nitrogen dioxide (NO2), ozone, fine particulate matter, and black carbon was estimated at the women’s residence using spatiotemporal models and averaged over the period of ovarian stimulation (2-weeks). Multivariable linear regression models were used to evaluate the associations between the air pollutants, number of mature oocytes, and metabolic feature intensities. A meet-in-the-middle approach was used to identify overlapping features and metabolic pathways. Results: Of the air pollutants, NO2 exposure had the largest number of overlapping metabolites (C18: 105; HILIC: 91) and biological pathways (C18: 3; HILIC: 6) with number of mature oocytes. Key pathways of overlap included vitamin D3 metabolism (both columns), bile acid biosynthesis (both columns), C21-steroid hormone metabolism (HILIC), androgen and estrogen metabolism (HILIC), vitamin A metabolism (HILIC), carnitine shuttle (HILIC), and prostaglandin formation (C18). Three overlapping metabolites were confirmed with level-1 or level-2 evidence. For example, hypoxanthine, a metabolite that protects against oxidant-induced cell injury, was positively associated with NO2 exposure and negatively associated with number of mature oocytes. Minimal overlap was observed between the other pollutants and the number of mature oocytes. Conclusions: Higher exposure to NO2 during ovarian stimulation was associated with many metabolites and biologic pathways involved in endogenous vitamin metabolism, hormone synthesis, and oxidative stress that may mediate the observed associations with lower oocyte quality.http://www.sciencedirect.com/science/article/pii/S0160412022004792Air pollutionFertilityMetabolomicsOvaryAssisted reproductionFollicular fluid |
spellingShingle | Sueyoun Hwang Robert B. Hood Russ Hauser Joel Schwartz Francine Laden Dean Jones Donghai Liang Audrey J. Gaskins Using follicular fluid metabolomics to investigate the association between air pollution and oocyte quality Environment International Air pollution Fertility Metabolomics Ovary Assisted reproduction Follicular fluid |
title | Using follicular fluid metabolomics to investigate the association between air pollution and oocyte quality |
title_full | Using follicular fluid metabolomics to investigate the association between air pollution and oocyte quality |
title_fullStr | Using follicular fluid metabolomics to investigate the association between air pollution and oocyte quality |
title_full_unstemmed | Using follicular fluid metabolomics to investigate the association between air pollution and oocyte quality |
title_short | Using follicular fluid metabolomics to investigate the association between air pollution and oocyte quality |
title_sort | using follicular fluid metabolomics to investigate the association between air pollution and oocyte quality |
topic | Air pollution Fertility Metabolomics Ovary Assisted reproduction Follicular fluid |
url | http://www.sciencedirect.com/science/article/pii/S0160412022004792 |
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