A rational review on the effects of sweeteners and sweetness enhancers on appetite, food reward and metabolic/adiposity outcomes in adults

Author(s): Dominic O'Connor ¹ ^, ² ^, ³ ^, ⁴ ^, ⁵ , Michelle Pang ⁶ ^, ⁷ ^, ⁸ ^, ⁹ ^, ¹⁰ , Gabriele Castelnuovo ¹¹ ^, ¹² ^, ¹³ ^, ¹⁴ ^, ¹⁵ , Graham Finlayson ¹ ^, ² ^, ³ ^, ⁴ ^, ⁵ , Ellen Blaak ⁶ ^, ⁷ ^, ⁸ ^, ⁹ ^, ¹⁰ , Catherine Gibbons ¹ ^, ² ^, ³ ^, ⁴ ^, ⁵ , Santiago Navas-Carretero ¹¹ ^, ¹² ^, ¹³ ^, ¹⁴ ^, ¹⁵ , Eva Almiron-Roig ¹¹ ^, ¹² ^, ¹³ ^, ¹⁴ ^, ¹⁵ , Jo Harrold ¹⁶ ^, ¹⁷ ^, ¹⁸ ^, ¹⁹ ^, ⁵ , Anne Raben ¹¹ ^, ²⁰ ^, ²¹ ^, ²² ^, ²³ , J. Alfredo Martinez ¹¹ ^, ¹² ^, ¹³ ^, ¹⁴ ^, ¹⁵

Publication date (Electronic): 2021

Journal: Food & Function

Publisher: Royal Society of Chemistry (RSC)

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Abstract

The review focused on outcomes related to obesity an diabetes as affected by sweeteners and included the following keywords: Food Intake, Subjective Appetite, Food Hedonics/Reward, Body Weight, Energy and Glucose, Metabolism/Adiposity Markers.

Abstract

Numerous strategies have been investigated to overcome the excessive weight gain that accompanies a chronic positive energy balance. Most approaches focus on a reduction of energy intake and the improvement of lifestyle habits. The use of high intensity artificial sweeteners, also known as non-caloric sweeteners (NCS), as sugar substitutes in foods and beverages, is rapidly developing. NCS are commonly defined as molecules with a sweetness profile of 30 times higher or more that of sucrose, scarcely contributing to the individual's net energy intake as they are hardly metabolized. The purpose of this review is first, to assess the impact of NCS on eating behaviour, including subjective appetite, food intake, food reward and sensory stimulation; and secondly, to assess the metabolic impact of NCS on body weight regulation, glucose homeostasis and gut health. The evidence reviewed suggests that while some sweeteners have the potential to increase subjective appetite, these effects do not translate in changes in food intake. This is supported by a large body of empirical evidence advocating that the use of NCS facilitates weight management when used alongside other weight management strategies. On the other hand, although NCS are very unlikely to impair insulin metabolism and glycaemic control, some studies suggest that NCS could have putatively undesirable effects, through various indirect mechanisms, on body weight, glycemia, adipogenesis and the gut microbiota; however there is insufficient evidence to determine the degree of such effects. Overall, the available data suggests that NCS can be used to facilitate a reduction in dietary energy content without significant negative effects on food intake behaviour or body metabolism, which would support their potential role in the prevention of obesity as a complementary strategy to other weight management approaches. More research is needed to determine the impact of NCS on metabolic health, in particular gut microbiota.

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The connection between the gut microbiota and the aetiology of obesity and cardiometabolic disorders is increasingly being recognized by clinicians. Our gut microbiota might affect the cardiometabolic phenotype by fermenting indigestible dietary components and thereby producing short-chain fatty acids (SCFA). These SCFA are not only of importance in gut health and as signalling molecules, but might also enter the systemic circulation and directly affect metabolism or the function of peripheral tissues. In this Review, we discuss the effects of three SCFA (acetate, propionate and butyrate) on energy homeostasis and metabolism, as well as how these SCFA can beneficially modulate adipose tissue, skeletal muscle and liver tissue function. As a result, these SCFA contribute to improved glucose homeostasis and insulin sensitivity. Furthermore, we also summarize the increasing evidence for a potential role of SCFA as metabolic targets to prevent and counteract obesity and its associated disorders in glucose metabolism and insulin resistance. However, most data are derived from animal and in vitro studies, and consequently the importance of SCFA and differential SCFA availability in human energy and substrate metabolism remains to be fully established. Well-controlled human intervention studies investigating the role of SCFA on cardiometabolic health are, therefore, eagerly awaited.

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Evidence is accumulating that the gut microbiome is involved in the aetiology of obesity and obesity-related complications such as nonalcoholic fatty liver disease (NAFLD), insulin resistance and type 2 diabetes mellitus (T2DM). The gut microbiota is able to ferment indigestible carbohydrates (for example, dietary fibre), thereby yielding important metabolites such as short-chain fatty acids and succinate. Numerous animal studies and a handful of human studies suggest a beneficial role of these metabolites in the prevention and treatment of obesity and its comorbidities. Interestingly, the more distal colonic microbiota primarily ferments peptides and proteins, as availability of fermentable fibre, the major energy source for the microbiota, is limited here. This proteolytic fermentation yields mainly harmful products such as ammonia, phenols and branched-chain fatty acids, which might be detrimental for host gut and metabolic health. Therefore, a switch from proteolytic to saccharolytic fermentation could be of major interest for the prevention and/or treatment of metabolic diseases. This Review focuses on the role of products derived from microbial carbohydrate and protein fermentation in relation to obesity and obesity-associated insulin resistance, T2DM and NAFLD, and discusses the mechanisms involved.