Chronic low BPS exposure through diet impairs in vitro embryo production parameters according to metabolic status in the ewe

Desmarchais, Alice; Têteau, Ophélie; Kasal-Hoc, Nathalie; Cognié, Juliette; Lasserre, Olivier; Papillier, Pascal; Lacroix, Marlène Z.; Vignault, Claire; Jarrier-Gaillard, Peggy; Maillard, Virginie; Binet, Aurélien; Pellicer-Rubio, Maria-Teresa; Fréret, Sandrine; Elis, Sébastien

doi:10.1016/j.ecoenv.2021.113096

Cited by 13 publications

(18 citation statements)

References 52 publications

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“…Our data, therefore, suggest that the BPS-induced impairment in progesterone secretion in restricted ewes could be detrimental to oocyte quality and, consequently, fertility. This is in line with our previous results that suggest that the effects of BPS on oocyte quality assessed by in vitro embryo production after ovum pick-up also vary according to metabolic status ( 13 ).…”

Section: Discussionsupporting

confidence: 93%

“…In June, i.e. at least 3 months before sample collection, ewes with similar age, body weight (BW) and body condition score (BCS) were allotted into two diet groups, as previously described ( 13 ). Briefly, the diet consisted of straw added with dietary supplement (AXEREAL Elevage, saint Germain de salles, France) composed of wheat (60%), alfalfa, sugar cane treacle and vitamins with nutritional values of 1.5 Mcal of net energy and 72 g of metabolisable protein per kilogram of dry matter and straw ad libitum .…”

Section: Methodsmentioning

confidence: 99%

“…Plasma (n = 80) and follicular fluid (< 6 mm follicles, therefore, not the preovulatory follicles, n = 20, 5 ewes per experimental groups) BPS and BPS-g concentrations of individual ewes were determined as previously described ( 13 ). Briefly, BPS and BPS-g concentrations were quantified using liquid chromatography-mass spectrometry with an Acquity U-HPLC device coupled to a Xevo-TQ triple quadrupole mass spectrometer (Waters, Saint-Quentin-en-Yvelines, France) operated with positive electrospray ionization and MRM mode.…”

Section: Methodsmentioning

confidence: 99%

“…Because metabolic status can regulate steroidogenesis, we hypothesize that the effects of BPS on steroid concentrations could vary according to the metabolic status of the animal, as reported for ovine oocyte quality ( 13 ). The objective of the present study was, therefore, to characterize the effects of BPS on all detectable steroid hormones in the preovulatory follicle fluid, oviduct fluid and plasma of adult ewes exhibiting contrasted metabolic status (restricted or well-fed).…”

Section: Introductionmentioning

confidence: 98%

“…Bisphenols can also bind to corticoid receptors and alter adrenal hormone secretion ( 2 ). Furthermore, chronic low exposure of ewes to BPS through the diet has been shown to impair oocyte quality and embryo production in vitro ( 13 ). However, whether BPS affects steroid hormone synthesis and secretion in vivo remains to be explored.…”

Section: Introductionmentioning

confidence: 99%

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Bisphenol S Alters the Steroidome in the Preovulatory Follicle, Oviduct Fluid and Plasma in Ewes With Contrasted Metabolic Status

et al. 2022

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Bisphenol A (BPA), a plasticizer and endocrine disruptor, has been substituted by bisphenol S (BPS), a structural analogue that had already shown adverse effects on granulosa cell steroidogenesis. The objective of this study was to assess the effect of chronic exposure to BPS, a possible endocrine disruptor, on steroid hormones in the ovary, oviduct and plasma using the ewe as a model. Given the interaction between steroidogenesis and the metabolic status, the BPS effect was tested according to two diet groups. Eighty adult ewes were allotted to restricted (R) and well-fed (WF) groups, that were further subdivided into two subgroups. Ewes were exposed to 50 µg BPS/kg/day in their diet (R50 and WF50 groups) or were unexposed controls (R0 and WF0 groups). After at least 3 months of BPS exposure, preovulatory follicular fluid, oviduct fluid and plasma were collected and steroid hormones were analyzed by gas chromatography coupled with tandem mass spectrometry (GC-MS/MS). A deleterious effect of restricted diet on the volume of oviduct fluid and numbers of pre-ovulatory follicles was observed. Exposure to BPS impaired estradiol concentrations in both follicular and oviduct fluids of well-fed ewes and progesterone, estradiol and estrone concentrations in plasma of restricted ewes. In addition, a significant interaction between metabolic status and BPS exposure was observed for seven steroids, including estradiol. In conclusion, BPS acts in ewes as an endocrine disruptor with differential actions according to metabolic status.

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Section: Discussionsupporting

confidence: 93%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 98%

Section: Introductionmentioning

confidence: 99%

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Bisphenol S Alters the Steroidome in the Preovulatory Follicle, Oviduct Fluid and Plasma in Ewes With Contrasted Metabolic Status

et al. 2022

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Exposure to bisphenol A and its analogs and polycystic ovarian syndrome in women of childbearing age: A multicenter case-control study

et al. 2023

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Impact of Bisphenol A and its alternatives on oocyte health: a scoping review

Peters,

Ford,

Roman

et al. 2024

Human Reproduction Update

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BACKGROUND Bisphenol A (BPA) is an endocrine disrupting chemical released from plastic materials, including food packaging and dental sealants, persisting in the environment and ubiquitously contaminating ecosystems and human populations. BPA can elicit an array of damaging health effects and, alarmingly, ‘BPA-free’ alternatives mirror these harmful effects. Bisphenol exposure can negatively impact female fertility, damaging both the ovary and oocytes therein. Such damage can diminish reproductive capacity, pregnancy success, and offspring health. Despite global government regulations in place to indicate ‘safe’ BPA exposure levels, these policies have not considered the effects of bisphenols on oocyte health. OBJECTIVE AND RATIONALE This scoping review was conducted to evaluate evidence on the effects of BPA and BPA alternatives on standardized parameters of oocyte health. In doing so, this review addresses a critical gap in the literature providing a comprehensive, up-to-date synthesis of the effects of bisphenols on oocyte health. SEARCH METHODS This scoping review was conducted in accordance with PRISMA guidelines. Four databases, Medline, Embase, Scopus, and Web of Science, were searched twice (23 February 2022 and 1 August 2023) to capture studies assessing mammalian oocyte health post-bisphenol exposure. Search terms regarding oocytes, ovarian follicles, and bisphenols were utilized to identify relevant studies. Manuscripts written in English and reporting the effect of any bisphenol on mammalian oocyte health from all years were included. Parameters for toxicological studies were evaluated, including the number of bisphenol concentrations/doses tested, dosing regimen, biological replicates and/or animal numbers, and statistical information (for human studies). Standardized parameters of oocyte health including follicle counts, oocyte yield, oocyte meiotic capacity, morphology of oocyte and cumulus cells, and oocyte meiotic spindle integrity were extracted across the studies. OUTCOMES After screening 3147 studies, 107 studies of either humans or mammalian animal models or humans were included. Of the in vitro exposure studies, 96.3% (26/27) and 94.1% (16/17) found at least one adverse effect on oocyte health using BPA or BPA alternatives (including BHPF, BPAF, BPB, BPF, and BPS), respectively. These included increased meiotic cell cycle arrest, altered morphology, and abnormal meiotic spindle/chromosomal alignment. In vivo, 85.7% (30/35) of studies on BPA and 92.3% (12/13) on BPA alternatives documented adverse effects on follicle development, morphology, or spindle/chromosome alignment. Importantly, these effects were recorded using levels below those deemed ‘safe’ for human exposure. Over half (11/21) of all human observational studies showed associations between higher urinary BPA levels and reduced antral follicle counts or oocyte yield in IVF patients. Recommendations are presented based on the identified shortcomings of the current evidence, incorporating elements of FDA requirements for future research in the field. WIDER IMPLICATIONS These data highlight the detrimental impacts of low-level BPA and BPA alternative exposure, contributing to poor oocyte quality and reduced fertility. These outcomes are valuable in promoting the revision of current policies and guidelines pertaining to BPA exposure internationally. This study serves as a valuable resource to scientists, providing key recommendations on study design, reporting elements, and endpoint measures to strengthen future studies. Ultimately, this review highlights oocyte health as a fundamentally important endpoint in reproductive toxicological studies, indicating an important direction for future research into endocrine disrupting chemicals to improve fertility outcomes.

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Chronic low BPS exposure through diet impairs in vitro embryo production parameters according to metabolic status in the ewe

Cited by 13 publications

References 52 publications

Bisphenol S Alters the Steroidome in the Preovulatory Follicle, Oviduct Fluid and Plasma in Ewes With Contrasted Metabolic Status

Bisphenol S Alters the Steroidome in the Preovulatory Follicle, Oviduct Fluid and Plasma in Ewes With Contrasted Metabolic Status

Exposure to bisphenol A and its analogs and polycystic ovarian syndrome in women of childbearing age: A multicenter case-control study

Impact of Bisphenol A and its alternatives on oocyte health: a scoping review

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