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Perigestational exposure of a combination of a high-fat diet and pesticide impacts the metabolic and microbiotic status of dams and pups; a preventive strategy based on prebiotics

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Abstract

Purpose

Metabolic changes during the perinatal period are known to promote obesity and type-2 diabetes in adulthood via perturbation of the microbiota. The risk factors for metabolic disorders include a high-fat diet (HFD) and exposure to pesticide residues. The objective of the present study was to evaluate the effects of perigestational exposure to a HFD and chlorpyrifos (CPF) on glycemia, lipid profiles, and microbial populations in Wistar dams and their female offspring. We also tested a preventive strategy based on treatment with the prebiotic inulin.

Methods

From 4 months before gestation to the end of the lactation period, six groups of dams were exposed to either a standard diet, a HFD alone, CPF alone, a combination of a HFD and CPF, and/or inulin supplementation. All female offspring were fed a standard diet from weaning to adulthood. We measured the impacts of these exposures on glycemia, the lipid profile, and the microbiota (composition, metabolite production, and translocation into tissues).

Results

HFD exposure and CPF + HFD co-exposure induced dysmetabolism and an imbalance in the gut flora in both the dams and the female offspring. Inulin mitigated the impact of exposure to a HFD alone but not that of CPF + HFD co-exposure.

Conclusion

Our results provide a better understanding of the complex interactions between environmental pollutants and diet in early life, including in the context of metabolic diseases.

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Data availability

Data is available on demand by email to the corresponding author.

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Acknowledgements

We thank Professor Jérôme Ausseil (Biochemistry Laboratory, Amiens University Medical Center, at the time of the work) for assistance with the metabolite assays. We also thank David Fraser PhD (Biotech Communication SARL, Ploudalmézeau, France) for copy-editing assistance.

Funding

The study was funded by the French Ministry of Higher Education, Research and the Hauts-de-France region via the 2017 “Fédératif Hospitalo-Universitaire 1000 Days for Health Proghomeo” program.

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Authors and Affiliations

  1. Laboratoire PeriTox UMR_I 01, Centre Universitaire de Recherche en Santé, CURS-UPJV, University of Picardy Jules Verne, 80054, Amiens cedex 1, France

    Narimane Djekkoun, Marion Guibourdenche, Hiba El Khayat Et Sabbouri, Aurélie Corona, Jerome Gay-Queheillard, Maurice Biendo, Véronique Bach & Hafida Khorsi-Cauet

  2. Laboratoire de Biologie Cellulaire Et Moléculaire, Mentouri Brothers University of Constantine 1, 2500, Constantine, Algeria

    Narimane Djekkoun & Leila Rouabah

  3. Transformations Et Agro-Ressources ULR7519, Institut Polytechnique UniLaSalle - Université d’Artois, 60026, Beauvais, France

    Flore Depeint & Larbi Rhazi

  4. Service Endocrinologie-Diabétologie et Nutrition, CHU Amiens-Picardie, 80000, Amiens, France

    Abdallah Al-Salameh & Jean-Daniel Lalau

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  1. Narimane Djekkoun
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Contributions

Data curation: ND; investigation; ND, FD, MG, HEKES, AC, LR, JGQ, MB, AAS; formal analysis: ND, VB; visualization: ND, VB, HKC; methodology: ND, MG, HEKES, LR, LR, MB, AAS, HKC; writing—original draft; writing—review and editing: ND, FD, JDL, VB, HKC; validation: FD, HKC; supervision: JGQ, VB, HKC; funding acquisition: JGQ, HKC; conceptualization: HKC; project administration: HKC. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Hafida Khorsi-Cauet.

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Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported here.

Ethical approval

The study protocol was approved by the Regional Directorate for Health, Animal Protection and the Environment (Amiens, France) and the French Ministry of Research (reference: APAFIS # 8207-2016121322563594 v2, September 5th, 2017). All animals were treated in accordance with the European Union Directive 2010/63 and monitored daily for well-being.

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Djekkoun, N., Depeint, F., Guibourdenche, M. et al. Perigestational exposure of a combination of a high-fat diet and pesticide impacts the metabolic and microbiotic status of dams and pups; a preventive strategy based on prebiotics. Eur J Nutr 62, 1253–1265 (2023). https://doi.org/10.1007/s00394-022-03063-y

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