Short-term hypercaloric carbohydrate loading increases surgical stress resilience by inducing FGF21

Thomas Agius, Raffaella Emsley, Arnaud Lyon, Michael R. MacArthur, Kevin Kiesworo, Anna Faivre, Louis Stavart, Martine Lambelet, David Legouis, Sophie Seigneux, Déla Golshayan, Francois Lazeyras, Heidi Yeh, James F. Markmann, Korkut Uygun, Alejandro Ocampo, Sarah J. Mitchell, Florent Allagnat, Sébastien Déglise and Alban Longchamp ()
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Thomas Agius: University Hospital of Lausanne (CHUV)
Raffaella Emsley: University Hospital of Lausanne (CHUV)
Arnaud Lyon: University Hospital of Lausanne (CHUV)
Michael R. MacArthur: Princeton University
Kevin Kiesworo: University Hospital of Lausanne (CHUV)
Anna Faivre: University of Geneva
Louis Stavart: University of Lausanne (UNIL)
Martine Lambelet: University Hospital of Lausanne (CHUV)
David Legouis: University of Geneva
Sophie Seigneux: University of Geneva
Déla Golshayan: University of Lausanne (UNIL)
Francois Lazeyras: University of Geneva
Heidi Yeh: Harvard Medical School
James F. Markmann: Harvard Medical School
Korkut Uygun: Harvard Medical School
Alejandro Ocampo: University of Lausanne
Sarah J. Mitchell: Princeton University
Florent Allagnat: University Hospital of Lausanne (CHUV)
Sébastien Déglise: University Hospital of Lausanne (CHUV)
Alban Longchamp: University Hospital of Lausanne (CHUV)

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: Abstract Dietary restriction promotes resistance to surgical stress in multiple organisms. Counterintuitively, current medical protocols recommend short-term carbohydrate-rich drinks (carbohydrate loading) prior to surgery, part of a multimodal perioperative care pathway designed to enhance surgical recovery. Despite widespread clinical use, preclinical and mechanistic studies on carbohydrate loading in surgical contexts are lacking. Here we demonstrate in ad libitum-fed mice that liquid carbohydrate loading for one week drives reductions in solid food intake, while nearly doubling total caloric intake. Similarly, in humans, simple carbohydrate intake is inversely correlated with dietary protein intake. Carbohydrate loading-induced protein dilution increases expression of hepatic fibroblast growth factor 21 (FGF21) independent of caloric intake, resulting in protection in two models of surgical stress: renal and hepatic ischemia-reperfusion injury. The protection is consistent across male, female, and aged mice. In vivo, amino acid add-back or genetic FGF21 deletion blocks carbohydrate loading-mediated protection from ischemia-reperfusion injury. Finally, carbohydrate loading induction of FGF21 is associated with the induction of the canonical integrated stress response (ATF3/4, NF-kB), and oxidative metabolism (PPARγ). Together, these data support carbohydrate loading drinks prior to surgery and reveal an essential role of protein dilution via FGF21.

Date: 2024
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DOI: 10.1038/s41467-024-44866-3

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