Pecans and Its Polyphenols Prevent Obesity, Hepatic Steatosis and Diabetes by Reducing Dysbiosis, Inflammation, and Increasing Energy Expenditure in Mice Fed a High-Fat Diet

Delgadillo-Puga, Claudia; Torre-Villalvazo, Ivan; Noriega, Lilia G.; Rodríguez-López, Leonardo A.; Alemán, Gabriela; Torre-Anaya, Erik A.; Cariño-Cervantes, Yonatan Y.; Palacios-Gonzalez, Berenice; Furuzawa-Carballeda, Janette; Tovar, Armando R.; Cisneros-Zevallos, Luis

doi:10.3390/nu15112591

Open AccessArticle

Pecans and Its Polyphenols Prevent Obesity, Hepatic Steatosis and Diabetes by Reducing Dysbiosis, Inflammation, and Increasing Energy Expenditure in Mice Fed a High-Fat Diet

by

Claudia Delgadillo-Puga

^1,*,†

,

Ivan Torre-Villalvazo

^2,†

,

Lilia G. Noriega

²

,

Leonardo A. Rodríguez-López

²,

Gabriela Alemán

²,

Erik A. Torre-Anaya

²,

Yonatan Y. Cariño-Cervantes

¹,

Berenice Palacios-Gonzalez

³,

Janette Furuzawa-Carballeda

⁴

,

Armando R. Tovar

²

and

Luis Cisneros-Zevallos

^5,*

¹

Departamento de Nutrición Animal Dr. Fernando Pérez-Gil Romo, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán (INCMNSZ), Mexico City 14080, Mexico

²

Departamento de Fisiología de la Nutrición, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán (INCMNSZ), Mexico City 14080, Mexico

³

Unidad de Vinculación Científica Facultad de Medicina, Instituto Nacional de Medicina Genómica (INMEGEN), Mexico City 16080, Mexico

⁴

Departamento de Cirugía Experimental, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán (INCMNSZ), Mexico City 14080, Mexico

⁵

Department of Horticultural Sciences, Texas A&M University, College Station, TX 77843-2133, USA

^*

Authors to whom correspondence should be addressed.

^†

These authors contributed equally to this work.

Nutrients 2023, 15(11), 2591; https://doi.org/10.3390/nu15112591

Submission received: 11 March 2023 / Revised: 30 May 2023 / Accepted: 30 May 2023 / Published: 31 May 2023

(This article belongs to the Section Phytochemicals and Human Health)

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Abstract

Pecans (Carya illinoinensis) are considered a functional food due to the high content of polyunsaturated fatty acids, dietary fiber and polyphenols. To determine the effect of whole pecans (WP) or a pecan polyphenol (PP) extract on the development of metabolic abnormalities in mice fed a high-fat (HF) diet, we fed C57BL/6 mice with a Control diet (7% fat), HF diet (23% fat), HF containing 30% WP or an HF diet supplemented with 3.6 or 6 mg/g of PP for 18 weeks. Supplementation of an HF diet with WP or PP reduced fat mass, serum cholesterol, insulin and HOMA-IR by 44, 40, 74 and 91%, respectively, compared to the HF diet. They also enhanced glucose tolerance by 37%, prevented pancreatic islet hypertrophy, and increased oxygen consumption by 27% compared to the HF diet. These beneficial effects were associated with increased thermogenic activity in brown adipose tissue, mitochondrial activity and AMPK activation in skeletal muscle, reduced hypertrophy and macrophage infiltration of subcutaneous and visceral adipocytes, reduced hepatic lipid content and enhanced metabolic signaling. Moreover, the microbial diversity of mice fed WP or PP was higher than those fed HF, and associated with lower circulating lipopolysaccharides (~83–95%). Additionally, a 4-week intervention study with the HF 6PP diet reduced the metabolic abnormalities of obese mice. The present study demonstrates that WP or a PP extract prevented obesity, liver steatosis and diabetes by reducing dysbiosis, inflammation, and increasing mitochondrial content and energy expenditure. Pecan polyphenols were mainly condensed tannin and ellagic acid derivatives including ellagitannins as determined by LC-MS. Herein we also propose a model for the progression of the HF diet-mediated metabolic disorder based on early and late events, and the possible molecular targets of WP and PP extract in preventive and intervention strategies. The body surface area normalization equation gave a conversion equivalent to a daily human intake dose of 2101–3502 mg phenolics that can be obtained from 110–183 g pecan kernels/day (22–38 whole pecans) or 21.6–36 g defatted pecan flour/day for an average person of 60 kg. This work lays the groundwork for future clinical studies.

Keywords: pecans; polyphenols; obesity; dysbiosis; insulin resistance; mitochondrial activity; functional food; bioactive compounds

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MDPI and ACS Style

Delgadillo-Puga, C.; Torre-Villalvazo, I.; Noriega, L.G.; Rodríguez-López, L.A.; Alemán, G.; Torre-Anaya, E.A.; Cariño-Cervantes, Y.Y.; Palacios-Gonzalez, B.; Furuzawa-Carballeda, J.; Tovar, A.R.; et al. Pecans and Its Polyphenols Prevent Obesity, Hepatic Steatosis and Diabetes by Reducing Dysbiosis, Inflammation, and Increasing Energy Expenditure in Mice Fed a High-Fat Diet. Nutrients 2023, 15, 2591. https://doi.org/10.3390/nu15112591

AMA Style

Delgadillo-Puga C, Torre-Villalvazo I, Noriega LG, Rodríguez-López LA, Alemán G, Torre-Anaya EA, Cariño-Cervantes YY, Palacios-Gonzalez B, Furuzawa-Carballeda J, Tovar AR, et al. Pecans and Its Polyphenols Prevent Obesity, Hepatic Steatosis and Diabetes by Reducing Dysbiosis, Inflammation, and Increasing Energy Expenditure in Mice Fed a High-Fat Diet. Nutrients. 2023; 15(11):2591. https://doi.org/10.3390/nu15112591

Chicago/Turabian Style

Delgadillo-Puga, Claudia, Ivan Torre-Villalvazo, Lilia G. Noriega, Leonardo A. Rodríguez-López, Gabriela Alemán, Erik A. Torre-Anaya, Yonatan Y. Cariño-Cervantes, Berenice Palacios-Gonzalez, Janette Furuzawa-Carballeda, Armando R. Tovar, and et al. 2023. "Pecans and Its Polyphenols Prevent Obesity, Hepatic Steatosis and Diabetes by Reducing Dysbiosis, Inflammation, and Increasing Energy Expenditure in Mice Fed a High-Fat Diet" Nutrients 15, no. 11: 2591. https://doi.org/10.3390/nu15112591

APA Style

Delgadillo-Puga, C., Torre-Villalvazo, I., Noriega, L. G., Rodríguez-López, L. A., Alemán, G., Torre-Anaya, E. A., Cariño-Cervantes, Y. Y., Palacios-Gonzalez, B., Furuzawa-Carballeda, J., Tovar, A. R., & Cisneros-Zevallos, L. (2023). Pecans and Its Polyphenols Prevent Obesity, Hepatic Steatosis and Diabetes by Reducing Dysbiosis, Inflammation, and Increasing Energy Expenditure in Mice Fed a High-Fat Diet. Nutrients, 15(11), 2591. https://doi.org/10.3390/nu15112591

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Pecans and Its Polyphenols Prevent Obesity, Hepatic Steatosis and Diabetes by Reducing Dysbiosis, Inflammation, and Increasing Energy Expenditure in Mice Fed a High-Fat Diet

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