The Relationship Between Widespread Pollution Exposure and Oxidized Products of Nucleic Acids in Seminal Plasma and Urine in Males Attending a Fertility Center.


Journal

International journal of environmental research and public health
ISSN: 1660-4601
Titre abrégé: Int J Environ Res Public Health
Pays: Switzerland
ID NLM: 101238455

Informations de publication

Date de publication:
13 03 2020
Historique:
received: 27 01 2020
revised: 04 03 2020
accepted: 05 03 2020
entrez: 19 3 2020
pubmed: 19 3 2020
medline: 23 9 2020
Statut: epublish

Résumé

In recent decades, there has been an increase in male infertility, and in many cases, the etiology remains unclear. Several studies relate male hypo-fertility to xenobiotic exposure, even if no data exist about multiple exposure at the environmental level. The study involved 86 males with diagnosis of idiopathic male infertility (IMI), and 46 controls with no alteration in sperm characteristics. Seminal plasma (SP) and urine samples were analyzed by liquid chromatography tandem mass spectrometry (LC-MS/MS) to quantify biomarkers of exposure (the main metabolites of benzene, toluene, 1,3-butadiene, 3-monochloropropanediol, styrene, and naphthol) and effect (oxidized products of nucleic acids). Biomarker concentrations were similar in subjects with IMI and controls even if a stronger correlation between biomarkers of exposure and effects were observed in SP. Data show that, both in SP and urine, most metabolites were inter-correlated, indicating a simultaneous co-exposure to the selected substances at the environmental level. Principal component analysis showed in SP the clustering of mercapturic acids indicating a preferential metabolic pathway with Glutathione (GSH) depletion and, consequently, an increase of oxidative stress. This result was also confirmed by multivariable analysis through the development of explanatory models for oxidized products of nucleic acids. This study highlights how oxidative stress on the male reproductive tract can be associated with a different representation of metabolic pathways making the reproductive tract itself a target organ for different environmental pollutants. Our results demonstrate that SP is a suitable matrix to assess the exposure and evaluate the effects of reproductive toxicants in environmental/occupational medicine. The statistical approach proposed in this work represents a model appropriate to study the relationship between multiple exposure and effect, applicable even to a wider variety of chemicals.

Sections du résumé

BACKGROUND
In recent decades, there has been an increase in male infertility, and in many cases, the etiology remains unclear. Several studies relate male hypo-fertility to xenobiotic exposure, even if no data exist about multiple exposure at the environmental level.
METHODS
The study involved 86 males with diagnosis of idiopathic male infertility (IMI), and 46 controls with no alteration in sperm characteristics. Seminal plasma (SP) and urine samples were analyzed by liquid chromatography tandem mass spectrometry (LC-MS/MS) to quantify biomarkers of exposure (the main metabolites of benzene, toluene, 1,3-butadiene, 3-monochloropropanediol, styrene, and naphthol) and effect (oxidized products of nucleic acids).
RESULTS
Biomarker concentrations were similar in subjects with IMI and controls even if a stronger correlation between biomarkers of exposure and effects were observed in SP. Data show that, both in SP and urine, most metabolites were inter-correlated, indicating a simultaneous co-exposure to the selected substances at the environmental level. Principal component analysis showed in SP the clustering of mercapturic acids indicating a preferential metabolic pathway with Glutathione (GSH) depletion and, consequently, an increase of oxidative stress. This result was also confirmed by multivariable analysis through the development of explanatory models for oxidized products of nucleic acids.
CONCLUSIONS
This study highlights how oxidative stress on the male reproductive tract can be associated with a different representation of metabolic pathways making the reproductive tract itself a target organ for different environmental pollutants. Our results demonstrate that SP is a suitable matrix to assess the exposure and evaluate the effects of reproductive toxicants in environmental/occupational medicine. The statistical approach proposed in this work represents a model appropriate to study the relationship between multiple exposure and effect, applicable even to a wider variety of chemicals.

Identifiants

pubmed: 32183208
pii: ijerph17061880
doi: 10.3390/ijerph17061880
pmc: PMC7143937
pii:
doi:

Substances chimiques

Biomarkers 0
Environmental Pollutants 0
Nucleic Acids 0
Benzene J64922108F

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Déclaration de conflit d'intérêts

The authors declare no conflict of interest.

Références

Proc Natl Acad Sci U S A. 2005 Aug 16;102(33):11722-7
pubmed: 16085710
Nicotine Tob Res. 2016 Sep;18(9):1886-94
pubmed: 27113015
World J Mens Health. 2014 Apr;32(1):1-17
pubmed: 24872947
Int J Occup Med Environ Health. 2009;22(4):305-29
pubmed: 20053623
Environ Int. 2019 May;126:134-144
pubmed: 30798194
Biomarkers. 2012 Jun;17(4):343-51
pubmed: 22458326
Int J Hyg Environ Health. 2018 Jun;221(5):809-815
pubmed: 29739653
J Chromatogr A. 1999 Jun 25;847(1-2):9-17
pubmed: 10431347
Anal Bioanal Chem. 2015 Jun;407(16):4823-7
pubmed: 25862474
Hum Reprod. 2019 Mar 1;34(3):558-567
pubmed: 30576495
Mol Cell Endocrinol. 2012 May 22;355(2):221-30
pubmed: 22138051
Gynecol Obstet Fertil. 2009 Jun;37(6):529-35
pubmed: 19481966
Int J Hyg Environ Health. 2007 May;210(3-4):201-28
pubmed: 17376741
Biochim Biophys Acta. 2014 Feb;1840(2):801-8
pubmed: 23791936
Nat Rev Urol. 2017 Feb;14(2):120-130
pubmed: 28050014
Environ Health Perspect. 2009 Jun;117(6):923-7
pubmed: 19590684
Andrology. 2016 Jul;4(4):648-61
pubmed: 27230702
Toxicol Lett. 2006 Apr 10;162(2-3):202-10
pubmed: 16260099
Sci Rep. 2017 Nov 14;7(1):15570
pubmed: 29138449
Fertil Steril. 2001 Feb;75(2):237-48
pubmed: 11172821
Environ Toxicol Pharmacol. 2017 Apr;51:56-70
pubmed: 28292651
J Endocrinol. 2011 Jun;209(3):337-51
pubmed: 21471187
Free Radic Biol Med. 2000 Feb 15;28(4):529-36
pubmed: 10719234
Scand J Urol Nephrol. 2003;37(1):38-42
pubmed: 12745742
Reprod Biol Endocrinol. 2019 Jan 6;17(1):4
pubmed: 30611299
Nat Rev Urol. 2017 Aug;14(8):470-485
pubmed: 28508879
Free Radic Biol Med. 2016 Oct;99:385-391
pubmed: 27585947
Toxicol In Vitro. 2016 Aug;34:1-7
pubmed: 26922907
J Environ Sci (China). 2019 Mar;77:210-217
pubmed: 30573085
Ther Adv Urol. 2016 Oct;8(5):302-318
pubmed: 27695529
Bioessays. 2004 May;26(5):533-42
pubmed: 15112233
Environ Res. 2008 Nov;108(3):280-8
pubmed: 18801480
J Biomed Biotechnol. 2006;2006(3):82323
pubmed: 17047315
Hum Exp Toxicol. 2018 Mar;37(3):247-255
pubmed: 28413887
Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11456-61
pubmed: 11572992
Environ Health Perspect. 2000 Sep;108(9):803-13
pubmed: 11017884
Reprod Biol Endocrinol. 2018 Dec 23;16(1):109
pubmed: 30579357
J Proteomics. 2018 Mar 1;174:85-100
pubmed: 29288815
J Toxicol Environ Health A. 2001 Jul 20;63(6):437-58
pubmed: 11482799
Fertil Steril. 2016 Oct;106(5):1070-1075
pubmed: 27460460
Ecotoxicol Environ Saf. 2019 Apr 30;171:475-483
pubmed: 30639874
Environ Res. 2016 Jul;148:154-163
pubmed: 27060750
Clin Chem. 1986 Mar;32(3):446-52
pubmed: 3948388
BMC Urol. 2012 Mar 19;12:6
pubmed: 22429816
Anal Bioanal Chem. 2010 Aug;397(8):3563-74
pubmed: 20556363
J Toxicol Environ Health A. 2004 Dec;67(23-24):2001-11
pubmed: 15513898
J Chromatogr B Analyt Technol Biomed Life Sci. 2015 Oct 1;1002:123-9
pubmed: 26319305
Asian Pac J Cancer Prev. 2015;16(16):6967-72
pubmed: 26514476
Biomarkers. 2010 May;15(3):221-31
pubmed: 19958079
Toxicol Lett. 2008 Sep;181(1):25-30
pubmed: 18640250
J Toxicol Environ Health B Crit Rev. 2014;17(1):45-61
pubmed: 24597909
Free Radic Biol Med. 2011 Jan 15;50(2):254-61
pubmed: 21075202
Curr Pharm Des. 2017 Nov 28;23(30):4438-4450
pubmed: 27774895
Hum Reprod Update. 2008 May-Jun;14(3):233-42
pubmed: 18281240
Andrologia. 2018 Apr;50(3):
pubmed: 29124782
Cancer Epidemiol Biomarkers Prev. 2008 Jan;17(1):3-14
pubmed: 18199707
Mol Cell Biochem. 1994 Nov 9;140(1):1-22
pubmed: 7877593
Epidemiology. 2006 Sep;17(5):520-3
pubmed: 16837825
J Androl. 2009 May-Jun;30(3):287-97
pubmed: 19059903
Int J Androl. 2011 Aug;34(4):369-78
pubmed: 20633195
Toxicol Lett. 2010 Jan 15;192(1):40-4
pubmed: 20117324
Andrology. 2016 Mar;4(2):270-6
pubmed: 26789272
Br Med Bull. 2000;56(3):630-42
pubmed: 11255550
FASEB J. 2003 Jul;17(10):1195-214
pubmed: 12832285

Auteurs

Diana Poli (D)

Department of Occupational and Environmental Medicine, Epidemiology and Hygiene, INAIL Research, Via Fontana Candida1, 00078 Monte Porzio Catone, Rome, Italy.

Roberta Andreoli (R)

Department of Medicine and Surgery, University of Parma, via A. Gramsci 14, 43126 Parma, Italy.
Centre for Research in Toxicology (CERT), University of Parma, via A. Gramsci 14, 43126 Parma, Italy.

Lucia Moscato (L)

Center of Reproductive Infertility (CIR), University Hospital of Parma, via A. Gramsci 14, 43126 Parma, Italy.

Giovanna Pelà (G)

Department of Medicine and Surgery, University of Parma, via A. Gramsci 14, 43126 Parma, Italy.
University Hospital of Parma, via A. Gramsci 14, 43126 Parma, Italy.

Giuseppe de Palma (G)

Department of Medicine, Surgery, Radiological Sciences, Public Health and Human Sciences Unit, University of Brescia, 25121 Brescia, Italy.

Delia Cavallo (D)

Department of Occupational and Environmental Medicine, Epidemiology and Hygiene, INAIL Research, Via Fontana Candida1, 00078 Monte Porzio Catone, Rome, Italy.

Marta Petyx (M)

Department of Occupational and Environmental Medicine, Epidemiology and Hygiene, INAIL Research, Via Fontana Candida1, 00078 Monte Porzio Catone, Rome, Italy.

Giorgio Pelosi (G)

Centre for Research in Toxicology (CERT), University of Parma, via A. Gramsci 14, 43126 Parma, Italy.
Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area delle Scienze 11/a, 43124 Parma, Italy.

Massimo Corradi (M)

Department of Medicine and Surgery, University of Parma, via A. Gramsci 14, 43126 Parma, Italy.
Centre for Research in Toxicology (CERT), University of Parma, via A. Gramsci 14, 43126 Parma, Italy.
University Hospital of Parma, via A. Gramsci 14, 43126 Parma, Italy.

Matteo Goldoni (M)

Department of Medicine and Surgery, University of Parma, via A. Gramsci 14, 43126 Parma, Italy.
Centre for Research in Toxicology (CERT), University of Parma, via A. Gramsci 14, 43126 Parma, Italy.

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