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Sweet taste and obesity

  • Gabriela Ribeiro
    Affiliations
    Champalimaud Research & Clinical Centre, Champalimaud Centre for the Unknown, Av. de Brasília, Doca de Pedrouços, 1400-038 Lisboa, Portugal

    Lisbon Academic Medical Centre PhD Program, Faculdade de Medicina, Universidade de Lisboa, Avenida Professor Egas Moniz, 1649-028 Lisboa, Portugal
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  • Albino J. Oliveira-Maia
    Correspondence
    Corresponding author: Champalimaud Research and Clinical Center, Champalimaud Center for the Unknown, Av. De Brasília, Doca de Pedrouços, 1400-038 Lisboa, Portugal.
    Affiliations
    Champalimaud Research & Clinical Centre, Champalimaud Centre for the Unknown, Av. de Brasília, Doca de Pedrouços, 1400-038 Lisboa, Portugal

    NOVA Medical School, NMS, Universidade Nova de Lisboa, Campo Mártires da Pátria 130, 1169-056 Lisboa, Portugal
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Open AccessPublished:February 13, 2021DOI:https://doi.org/10.1016/j.ejim.2021.01.023

      Highlights

      • Obesity has been associated to altered sensitivity to food reward.
      • Sugar triggers brain reward circuitries, encouraging its consumption.
      • There is methodological heterogeneity in studies of taste perception in obesity.
      • Research on the association between obesity and sweet taste perception is inconclusive.
      • Following bariatric surgery there is limited evidence of changes in sweet taste perception.

      Abstract

      For more than 50 years, there has been evidence for greater consumption of sweet- foods in overweight humans and animals, relative to those that have a normal weight. Furthermore, it has long been suggested that energy deficit resulting from dieting, while moving the individual from a higher weight set point, would result in heightened susceptibility to palatable tastants, namely to sweet tastants. This was the motivation behind the first studies comparing sweet taste perception between individuals with obesity and those of a normal weight. These studies, using direct measures of taste, have been characterized by significant methodological heterogeneity, contributing towards variability in results and conclusions. Nevertheless, some of these findings have been used to support the theory that patients with obesity have decreased taste perception, particularly for sweet tastants. A similar hypothesis has been proposed regarding evidence for reduced brain dopamine receptors in obesity and, in both cases, it is proposed that increased food consumption, and associated weight gain, result from the need to increase sensory and brain stimulation. However, the available literature is not conclusive on the association between obesity and reduced sweet taste perception, with both negative and contradictory findings in comparisons between individuals with obesity and normal weight control subjects, as well as within-subject comparisons before and after bariatric surgery. Nevertheless, following either Roux-en-Y gastric bypass or sleeve gastrectomy, there is evidence of changes in taste perception, particularly for reward-related measures of sweet tastants, that should be further tested and confirmed in large samples, using consensual methodology.

      Keywords

      1. Background

      Obesity is associated with significant morbidity and mortality, and currently represents a global health challenge[
      • Bray G.A.
      • Kim K.K.
      • Wilding J.P.H.
      Obesity: a chronic relapsing progressive disease process. A position statement of the World Obesity Federation.
      ]. While it is associated with complex pathophysiology, increased availability of highly palatable foods and beverages, namely those rich in sugar or fat, is thought to be a major determinant of increasing rates of obesity worldwide[
      • Mullee A.
      • Romaguera D.
      • Pearson-Stuttard J.
      • et al.
      Association between soft drink consumption and mortality in 10 european countries.
      ]. Indeed, individuals with obesity have been shown to have altered sensitivity to food reward[
      • Stice E.
      • Burger K.
      Neural vulnerability factors for obesity.
      ], which is thought to be related to changes in reward-related brain neurocircuitry, namely decreased striatal availability of dopamine D2 receptors (D2R)[
      • Stice E.
      • Burger K.
      Neural vulnerability factors for obesity.
      ]. Sugar, through pleasant taste and postingestive value, triggers brain reward circuitries, stimulating consumption of foods that are rich in sugar[
      • Tan H.-.E.
      • Sisti A.C.
      • Jin H.
      • et al.
      The gut–brain axis mediates sugar preference.
      ,
      • Fernandes A.B.
      • Alves da Silva J.
      • Almeida J.
      • et al.
      Postingestive modulation of food seeking depends on vagus-mediated dopamine neuron activity.
      ,
      • de Araujo I.E.
      • Oliveira-Maia A.J.
      • Sotnikova T.D.
      • et al.
      Food reward in the absence of taste receptor signaling.
      ]. Another important factor is that, while in non-obese subjects striatal D2R availability is inversely associated with sweet preference, in subjects with obesity this association is lacking, through mechanisms that have not yet been clarified[
      • Pepino M.Y.
      • Eisenstein S.A.
      • Bischoff A.N.
      • et al.
      Sweet dopamine: sucrose preferences relate differentially to striatal D2 receptor binding and age in obesity.
      ]. Beyond association between gustatory and reward-related circuits in humans[
      • Oliveira-Maia A.J.
      • Roberts C.D.
      • Simon S.A.
      • Nicolelis M.A.
      Gustatory and reward brain circuits in the control of food intake.
      ], there is also pre-clinical evidence in rodents [
      • Gutierrez R.
      • Fonseca E.
      • Simon S.A.
      The neuroscience of sugars in taste, gut-reward, feeding circuits, and obesity.
      ] and fruit flies [
      • May C.E.
      • Vaziri A.
      • Lin Y.Q.
      • et al.
      High dietary sugar reshapes sweet taste to promote feeding behavior in drosophila melanogaster.
      ] that dietary sugar content influences sweet taste perception. For example, in Drosophila melanogaster a high sugar diet led to decreased response of ‘sweet-taste sensing neurons’, resulting in diminished behavioral responses to sweet tastants[
      • May C.E.
      • Vaziri A.
      • Lin Y.Q.
      • et al.
      High dietary sugar reshapes sweet taste to promote feeding behavior in drosophila melanogaster.
      ]. Importantly, reduction of sweet taste responses through neural manipulation resulted in overfeeding and obesity, further suggesting that sweet taste perception is a driver of obesity[
      • May C.E.
      • Vaziri A.
      • Lin Y.Q.
      • et al.
      High dietary sugar reshapes sweet taste to promote feeding behavior in drosophila melanogaster.
      ].
      Evidence for association between taste, reward and morbid obesity has also been collected in the context of weight loss. Bariatric surgery is broadly accepted as the most efficient treatment for obesity, leading to significant weight loss and maintenance of weight, as well as improvement of obesity related comorbidities[
      • Dicker D.
      • Yahalom R.
      • Comaneshter D.S.
      • Vinker S.
      Long-term outcomes of three types of bariatric surgery on obesity and type 2 diabetes control and remission.
      ,
      • Cătoi A.F.
      • Pârvu A.
      • Mureşan A.
      • Busetto L.
      Metabolic mechanisms in obesity and type 2 diabetes: insights from bariatric/metabolic surgery.
      ,

      Sjostrom L., Narbro K., Sjostrom C.D., et al. Effects of bariatric surgery on mortality in Swedish obese subjects. N Engl J Med.2007;357(8):741–52. doi: 10.1056/NEJMoa066254.

      ]. Several mechanisms have been proposed as determinants of changes in ingestive behavior following bariatric surgery, namely a global reduction of appetite, development of conditioned aversions and changes in reward-related feeding behavior[
      • Nance K.
      • Acevedo M.B.
      • Pepino M.Y.
      Changes in taste function and ingestive behavior following bariatric surgery.
      ], including modulation of taste-related reward[
      • Smith K.R.
      • Papantoni A.
      • Veldhuizen M.G.
      • et al.
      Taste-related reward is associated with weight loss following bariatric surgery.
      ]. Indeed, following Roux-en-Y gastric bypass (RYGB) and sleeve gastrectomy (SG), currently the most commonly performed bariatric procedures, there is substantial evidence of self-reported decrease in consumption, cravings and preference for palatable sugar-rich and/or fat-rich foods (for review see Nance K., et al. [
      • Nance K.
      • Acevedo M.B.
      • Pepino M.Y.
      Changes in taste function and ingestive behavior following bariatric surgery.
      ]). Accordingly, patients report changes in taste perception of sweet foods after surgery[
      • Nance K.
      • Acevedo M.B.
      • Pepino M.Y.
      Changes in taste function and ingestive behavior following bariatric surgery.
      ].
      However, across the several studies exploring taste perception in obesity[
      • Pepino M.Y.
      • Eisenstein S.A.
      • Bischoff A.N.
      • et al.
      Sweet dopamine: sucrose preferences relate differentially to striatal D2 receptor binding and age in obesity.
      ,
      • Rodin J.
      • Moskowitz H.R.
      • Bray G.A.
      Relationship between obesity, weight loss, and taste responsiveness.
      ,
      • Thompson D.A.
      • Moskowitz H.R.
      • Campbell R.G.
      Taste and olfaction in human obesity.
      ,
      • Grinker J.
      Obesity and sweet taste.
      ,
      • Frijters J.E.
      • Rasmussen-Conrad E.L.
      Sensory discrimination, intensity perception, and affective judgment of sucrose-sweetness in the overweight.
      ,
      • Pasquet P.
      • Frelut M.L.
      • Simmen B.
      • Hladik C.M.
      • Monneuse M.O.
      Taste perception in massively obese and in non-obese adolescents.
      ,
      • Pepino M.Y.
      • Finkbeiner S.
      • Beauchamp G.K.
      • Mennella J.A.
      Obese women have lower monosodium glutamate taste sensitivity and prefer higher concentrations than do normal-weight women.
      ,
      • Park D.C.
      • Yeo J.H.
      • Ryu I.Y.
      • Kim S.H.
      • Jung J.
      • Yeo S.G.
      Differences in taste detection thresholds between normal-weight and obese young adults.
      ,
      • Hardikar S.
      • Hochenberger R.
      • Villringer A.
      • Ohla K.
      Higher sensitivity to sweet and salty taste in obese compared to lean individuals.
      ], and its changes following bariatric surgery[
      • Scruggs D.M.
      • Buffington C.
      • Cowan G.S.
      Taste acuity of the morbidly obese before and after gastric bypass surgery.
      ,
      • Burge J.C.
      • Schaumburg J.Z.
      • Choban P.S.
      • DiSilvestro R.A.
      • Flancbaum L.
      Changes in patients’ taste acuity after Roux-en-Y gastric bypass for clinically severe obesity.
      ,
      • Bueter M.
      • Miras A.
      • Chichger H.
      • et al.
      Alterations of sucrose preference after Roux-en-Y gastric bypass.
      ,
      • Pepino M.Y.
      • Bradley D.
      • Eagon J.C.
      • Sullivan S.
      • Abumrad N.A.
      • Klein S.
      Changes in taste perception and eating behavior after bariatric surgery-induced weight loss in women.
      ,
      • Holinski F.
      • Menenakos C.
      • Haber G.
      • Olze H.
      • Ordemann J.
      Olfactory and gustatory function after bariatric surgery.
      ,
      • Altun H.
      • Hanci D.
      • Altun H.
      • et al.
      Improved gustatory sensitivity in morbidly obese patients after laparoscopic sleeve gastrectomy.
      ,
      • Nance K.
      • Eagon J.C.
      • Klein S.
      • Pepino M.Y.
      Effects of sleeve gastrectomy vs. Roux-en-Y gastric bypass on eating behavior and sweet taste perception in subjects with obesity.
      ], there is a notable heterogeneity in methods and results. This has led to considerable difficulties in interpreting the available literature regarding the contribution of taste perception towards obesity. In this review, following an overview of taste physiology and psychophysical assessment of taste in humans, we will focus on studies that used direct measures of taste, using simple tastants rather than mixtures, to compare between patients with obesity and control subjects, as well as studies assessing the impact of bariatric surgery on taste perception.

      2. Neurobiology of taste

      Taste allows for identification and consumption of appetitive substances, like sucrose (sweet), and avoidance of potentially toxic and unpleasant compounds, such as quinine (bitter)[
      • Gutierrez R.
      • Fonseca E.
      • Simon S.A.
      The neuroscience of sugars in taste, gut-reward, feeding circuits, and obesity.
      ]. In addition to informing feeding decisions, this system contributes to the physiological regulation of starch and fat digestion, initiated through salivary secretions[
      • Matsuo R.
      • Carpenter G.H.
      The role of saliva in taste transduction.
      ], as well as to other elements of metabolic regulation through processes such as the cephalic phase of insulin secretion[
      • Gutierrez R.
      • Fonseca E.
      • Simon S.A.
      The neuroscience of sugars in taste, gut-reward, feeding circuits, and obesity.
      ]. In common terms, taste is frequently used as an equivalent for flavor. However, flavor is better defined as the complex perception resulting from converging inputs from taste, texture and olfaction, induced by multisensory stimulation from foods during mastication and swallowing[
      • Snyder D.J.
      • Sims C.A.
      • Bartoshuk L.M.
      Psychophysical measures of human oral sensation.
      ]. This review will focus primarily in taste, rather than flavor perception.
      Taste buds, located in the epithelium of the tongue, palate and epiglottis, are the peripheral organs of gustation[
      • Roper S.D.
      • Chaudhari N.
      Taste buds: cells, signals and synapses.
      ]. They are cell groups shaped similarly to a garlic-bulb, embedded in fungiform, foliate and circumvallate papillae, located on the anterior, lateral, and posterior regions of the tongue, respectively[
      • Gutierrez R.
      • Fonseca E.
      • Simon S.A.
      The neuroscience of sugars in taste, gut-reward, feeding circuits, and obesity.
      ]. The taste receptor cells (TRCs) in taste buds respond to chemical stimuli dissolved in saliva, allowing for the detection of five distinct taste qualities: salt, sweet, bitter, sour (acid) and umami (savory taste of amino acids)[
      • Oliveira-Maia A.J.
      • Roberts C.D.
      • Simon S.A.
      • Nicolelis M.A.
      Gustatory and reward brain circuits in the control of food intake.
      ,
      • Gutierrez R.
      • Fonseca E.
      • Simon S.A.
      The neuroscience of sugars in taste, gut-reward, feeding circuits, and obesity.
      ,
      • Witt M.
      • Reutter K.
      Anatomy of the tongue and taste buds.
      ]. TRCs within taste buds are classified, at least in part, according to their sensory function. In brief, Type II (receptor) cells have, in their apical surface, G-protein coupled receptors (GPCR) that are sensitive to bitter, sweet or umami tastants[
      • Witt M.
      • Reutter K.
      Anatomy of the tongue and taste buds.
      ]. Type III (pre-synaptic) cells have ionotropic receptors to identify acidic stimuli (sour taste) and release GABA, serotonin and norepinephrine in synapses with neurons from cranial nerves[
      • Witt M.
      • Reutter K.
      Anatomy of the tongue and taste buds.
      ]. Type I cells are glia-like [
      • Roper S.D.
      • Chaudhari N.
      Taste buds: cells, signals and synapses.
      ,
      • Witt M.
      • Reutter K.
      Anatomy of the tongue and taste buds.
      ] while type IV (basal) cells are undifferentiated cells located in the base of the taste bud[
      • Witt M.
      • Reutter K.
      Anatomy of the tongue and taste buds.
      ]. Regarding salt taste, amiloride-sensitive epithelial sodium channels have been shown to be involved in rodents, although in humans, further research is needed[
      • Gutierrez R.
      • Fonseca E.
      • Simon S.A.
      The neuroscience of sugars in taste, gut-reward, feeding circuits, and obesity.
      ]. Additional taste qualities have been proposed, such as that occurring via the fatty acid translocase cluster determinant 36 (CD36), that is thought to contribute, with texture perception via the somatosensory system, for identification of fat[
      • Oliveira-Maia A.J.
      • Roberts C.D.
      • Simon S.A.
      • Nicolelis M.A.
      Gustatory and reward brain circuits in the control of food intake.
      ].
      Activation of TRCs leads to neurotransmitter and peptide release onto afferent fiber terminals of cranial nerves VII, IX and X (facial, glossopharyngeal and vagus, respectively) that, in turn convey information to the central nervous system [
      • Small D.M.
      • Faurion A.
      Mapping brain activity in response to taste stimulation.
      ] specifically to the nucleus tractus solitarius, in the brainstem, that then relays neural information to the thalamus and insula[
      • Oliveira-Maia A.J.
      • Roberts C.D.
      • Simon S.A.
      • Nicolelis M.A.
      Gustatory and reward brain circuits in the control of food intake.
      ]. The area of the insula receiving taste sensory information is the primary gustatory cortex, while areas of the orbitofrontal cortex responding to taste stimulation, as well as to other flavor-related sensory information (e.g., texture, temperature, and odor), are sometimes defined as the secondary gustatory cortex[
      • Oliveira-Maia A.J.
      • Roberts C.D.
      • Simon S.A.
      • Nicolelis M.A.
      Gustatory and reward brain circuits in the control of food intake.
      ]. Neurons in the gustatory system also respond to the postingestive effects of food, as well as the homeostatic state[
      • Vincis R.
      • Fontanini A.
      Central taste anatomy and physiology.
      ] (for a review on peripheral and central gustatory processing see Oliveira-Maia AJ et al. 2011 [
      • Oliveira-Maia A.J.
      • Roberts C.D.
      • Simon S.A.
      • Nicolelis M.A.
      Gustatory and reward brain circuits in the control of food intake.
      ]).

      3. Psychophysical measures of taste

      For interpretation of the literature involving taste perception in obesity, it is fundamental to understand the methods used for orosensory assessment. One of the main challenges of such assessment is to capture interindividual variability in perceptions of intensity (e.g., the perception of a soup being too salty or watered down [
      • Snyder D.J.
      • Sims C.A.
      • Bartoshuk L.M.
      Psychophysical measures of human oral sensation.
      ]). There are two main complementary perspectives regarding intensity perception. One perspective treats intensity as a binary concept (i.e., the tastant is identified as absent or present) that is thus measured according to the threshold at which taste stimulation is identified. Both electrical (Fig. 1A) and chemical methods can be used to assess taste thresholds [
      • Snyder D.J.
      • Sims C.A.
      • Bartoshuk L.M.
      Psychophysical measures of human oral sensation.
      ] (see Supplementary Table 1 for details). The other perspective assumes perceived intensity as a continuous construct[
      • Snyder D.J.
      • Sims C.A.
      • Bartoshuk L.M.
      Psychophysical measures of human oral sensation.
      ]. In this case, chemical tests (e.g. Fig. 1B) can be used with suprathreshold scaling, including the general labeled magnitude scale (gLMS) [
      • Green B.G.
      • Dalton P.
      • Cowart B.
      • Shaffer G.
      • Rankin K.
      • Higgins J.
      Evaluating the ‘Labeled Magnitude Scale'for measuring sensations of taste and smell.
      ] which is, currently, the gold standard for this purpose (Fig. 1C; see Supplementary Table 1 for details). The general labeled hedonic scale (gLHS) [
      • Lim J.
      • Wood A.
      • Green B.G.
      Derivation and evaluation of a labeled hedonic scale.
      ], rather than assessing sensory-discriminative domains, assesses the degree of pleasantness, or unpleasantness, of the stimulus [
      • Nance K.
      • Acevedo M.B.
      • Pepino M.Y.
      Changes in taste function and ingestive behavior following bariatric surgery.
      ] (Fig. 1D). A full summary of methods commonly used for oral sensory assessment in humans is provided in Supplementary Table 1, highlighting their complexity and the need to consider methodological specificities in interpretation of the available data.
      Fig. 1
      Fig. 1Examples of methods used for assessment of oral sensations in humans.
      A. Electrogustometer (Rion TR-06; Rion Co. Ltd., Tokyo, Japan). This equipment is commercially available for determination of electric taste thresholds. Stimulus can be applied at durations ranging from 0.5 to 2 s and current ranges from −6 dB to 34 dB, in 21 steps. The electric probe is connected to the left side of the equipment, while a neckband, that completes the circuit is connected to the other side. Reproduced from
      [
      • Hawkes C.
      • Doty R.
      Measurement of Gustation.
      ]
      with permission from Cambridge University Press, through PLSclear.
      B. Taste strips test (Burghart Messtechnik GmbH, Wedel, Germany). This is a commercially available test comprising 16 containers with 4 concentrations of sweet, sour, salt and bitter as well as blank strips (image on the left, provided by Burghart Messtechnik GmbH). The strips are applied on the anterior third of the extended tongue (image on the right, reproduced from
      [
      • Landis B.N.
      • Welge-Luessen A.
      • Brämerson A.
      • Bende M.
      • Mueller C.A.
      • Nordin S.
      • et al.
      “Taste Strips” - a rapid, lateralized, gustatory bedside identification test based on impregnated filter papers.
      ]
      with permission from Springer Nature, through RightsLink.
      C. Examples of labeled scales used for intensity assessment. LMS – Labeled Magnitude Scale; gLMS – general Labeled Magnitude Scale. Adapted from
      [
      • Snyder D.J.
      • Sims C.A.
      • Bartoshuk L.M.
      Psychophysical measures of human oral sensation.
      ]
      with permission from John Wiley & Sons, Inc, through RightsLink.
      D. Examples of labeled hedonic scales. LHS – Labeled Hedonic Scale; gLMS- general Labeled Magnitude Scale. Adapted from
      [
      • Snyder D.J.
      • Sims C.A.
      • Bartoshuk L.M.
      Psychophysical measures of human oral sensation.
      ]
      with permission from John Wiley & Sons, Inc, through RightsLink.

      4. Studies of taste perception in individuals with obesity

      In studies comparing taste perception between individuals with obesity and control subjects, using direct measures of taste, one of the most explored outcomes was detection and/or recognition thresholds. Distinct methods have been used, and overall, the results do not consistently support that individuals with obesity have altered taste sensitivity or require different concentrations of a specific tastant (e.g., sucrose) to detect taste (Table 1). Detailed inspection of the available data shows that 3 studies, using the constant stimuli method (see Supplementary Table 1 for details on this and other methods), did not find differences between individuals with obesity and normal weight control subjects in detection thresholds for sweet taste [
      • Grinker J.
      Obesity and sweet taste.
      ,
      • Frijters J.E.
      • Rasmussen-Conrad E.L.
      Sensory discrimination, intensity perception, and affective judgment of sucrose-sweetness in the overweight.
      ,
      • Bueter M.
      • Miras A.
      • Chichger H.
      • et al.
      Alterations of sucrose preference after Roux-en-Y gastric bypass.
      ]. Another study, using the 3-stimulus drop method, found no differences relating to the presence of obesity for both detection and recognition thresholds for sweet, salt, bitter and sour tastants[
      • Scruggs D.M.
      • Buffington C.
      • Cowan G.S.
      Taste acuity of the morbidly obese before and after gastric bypass surgery.
      ]. Higher detection thresholds (i.e. lower taste sensitivity) in individuals with obesity relative to normal weight controls was reported for salt taste using a derivation of the method of limits among young adults[
      • Park D.C.
      • Yeo J.H.
      • Ryu I.Y.
      • Kim S.H.
      • Jung J.
      • Yeo S.G.
      Differences in taste detection thresholds between normal-weight and obese young adults.
      ], and for umami using the two-alternative forced-choice (2-AFC) staircase procedure in women[
      • Pepino M.Y.
      • Finkbeiner S.
      • Beauchamp G.K.
      • Mennella J.A.
      Obese women have lower monosodium glutamate taste sensitivity and prefer higher concentrations than do normal-weight women.
      ]. These studies found no differences for several other tastants, including sucrose in both cases[
      • Pepino M.Y.
      • Finkbeiner S.
      • Beauchamp G.K.
      • Mennella J.A.
      Obese women have lower monosodium glutamate taste sensitivity and prefer higher concentrations than do normal-weight women.
      ,
      • Park D.C.
      • Yeo J.H.
      • Ryu I.Y.
      • Kim S.H.
      • Jung J.
      • Yeo S.G.
      Differences in taste detection thresholds between normal-weight and obese young adults.
      ], and both quinine and citric acid in one of the studies[
      • Park D.C.
      • Yeo J.H.
      • Ryu I.Y.
      • Kim S.H.
      • Jung J.
      • Yeo S.G.
      Differences in taste detection thresholds between normal-weight and obese young adults.
      ]. Additionally, one of these studies revealed higher electrogustometry (EGM) thresholds in individuals with obesity, despite no correlations with chemical thresholds[
      • Park D.C.
      • Yeo J.H.
      • Ryu I.Y.
      • Kim S.H.
      • Jung J.
      • Yeo S.G.
      Differences in taste detection thresholds between normal-weight and obese young adults.
      ]. While these studies provide limited evidence for higher detection thresholds for salt and umami, but not sweet, bitter or sour tastants, two other studies investigating recognition thresholds with an up-down staircase procedure found that these were lower, rather than higher, among individuals with obesity for sweet and salt, but not for bitter and sour tastants[
      • Pasquet P.
      • Frelut M.L.
      • Simmen B.
      • Hladik C.M.
      • Monneuse M.O.
      Taste perception in massively obese and in non-obese adolescents.
      ,
      • Hardikar S.
      • Hochenberger R.
      • Villringer A.
      • Ohla K.
      Higher sensitivity to sweet and salty taste in obese compared to lean individuals.
      ].
      Table 1Studies that compared individuals with obesity with non-obese controls, using direct measures of taste.
      ReferenceParticipantsMethodologyResults
      Outcome/MethodTaste stimuli/Method of application
      Rodin et al., 1976
      • Rodin J.
      • Moskowitz H.R.
      • Bray G.A.
      Relationship between obesity, weight loss, and taste responsiveness.
      Obese, n=16

      Mildly overweight, n=16

      Normal weight, n=6

      All women
      Intensity (9-point scale)Glucose, 0.125-3 M

      Sip and taste without swallowing
      - No differences were found among weight category groups in intensity ratings.
      Pleasantness (9-point scale)Glucose, 0.125–3 M

      Sip and taste without swallowing
      - Individualswith obesity or who were mildly overweight rated higher concentrations of sweet more pleasantvs. normal weight participants.
      Thompson et al., 1977
      • Thompson D.A.
      • Moskowitz H.R.
      • Campbell R.G.
      Taste and olfaction in human obesity.
      Obese, n=14

      Normal weight, n= 18

      Age matched
      Intensity and pleasantness

      Magnitude estimation
      Sucrose, 0.075-1.5 M

      Sip and taste without swallowing
      - Individuals with obesity did not differ in responses to sucrose vs. normal weight participants.
      Grinker et al., 1978
      • Grinker J.
      Obesity and sweet taste.
      Obese, n=39

      Normal weight, n=13
      Detection threshold

      Constant Stimuli
      Sucrose, 0.175% (w/v) vs. water

      Sip and taste without swallowing
      - Individuals with obesity did not differ in sucrose detection threshold vs. normal weight participants.
      Severely obese, n=39

      Mildly overweight, n=14

      Normal weight, n=13
      Intensity

      Magnitude estimation
      Sucrose, 1.95- 19.5% (w/v)

      Sip and taste without swallowing
      - Individuals with obesity did not differ in intensity estimates vs. normal weight participants.
      Pleasantness

      (-4 to 4-point scale)
      Sucrose, 1.95- 19.5% (w/v)

      Sip and taste without swallowing
      - Individuals with obesity rated higher concentrations of sucrose as less pleasant vs. normal weight.
      Frijters& Rasmussen-Conrad et al., 1982
      • Frijters J.E.
      • Rasmussen-Conrad E.L.
      Sensory discrimination, intensity perception, and affective judgment of sucrose-sweetness in the overweight.
      Overweight, n=13

      Normal weight, n= 12

      All women
      Detection threshold

      Constant stimuli
      Sucrose, 0.0006-0.02 M vs. water

      Sip and taste without swallowing
      - No differences between overweight vs. normal weight participants were found in any parameter.
      Intensity

      Magnitude estimation
      Sucrose, 0.06-1.3 M

      Sip and taste without swallowing
      Liking (170 mm liking scale)Sucrose, 0.06–1.3 M

      Sip and taste without swallowing
      Scruggs et al., 1994
      • Scruggs D.M.
      • Buffington C.
      • Cowan G.S.
      Taste acuity of the morbidly obese before and after gastric bypass surgery.
      Obese, n=6

      Normalweight, n=10

      All women
      Detection and recognition thresholds

      -stimulus drop
      HCL, 0.5-500 mMvs. water

      Urea, 90-5.000 mMvs. water

      Sucrose, 6-5.8000 mMvs. water

      NaCl, 6-6.100 mM vs. water

      Calibrated drops placed on the tongue.
      - Individuals with obesity did not differ in detection or recognition thresholds vs. normal weight participants.
      Pasquet et al., 2007
      • Pasquet P.
      • Frelut M.L.
      • Simmen B.
      • Hladik C.M.
      • Monneuse M.O.
      Taste perception in massively obese and in non-obese adolescents.
      Severe early onset obesity, n=39

      Non-obese, n=48

      Adolescents
      Recognition threshold

      Up-down/staircase
      Sucrose and fructose, 2.0-1000 mM

      Citric acid, 0.40-25mM

      NaCl, 1.77-1000 mM

      Quinine HCl, 0.4-400 mM

      PROP, 0.001-3.2 mM

      Sip and taste without swallowing
      - Adolescents with obesity had significantly lower recognition thresholds for sucrose and NaCl vs. non-obese participants.
      Intensity (9-point scale)Sucrose, 121- 970 mM

      NaCl, 32- 1000 mM

      Sip and taste without swallowing
      -  Adolescents with obesity rated sweet and salty tastants as more intense vs. non-obeseparticipants.
      Pleasantness (9-point scale)Sucrose, 121- 970 mM

      NaCl, 32- 1000 mM

      Sip and taste without swallowing.
      - Adolescents with obesity rated the lowest NaCl solution less pleasant, but not sucrose.
      Pepino et al., 2010
      • Pepino M.Y.
      • Finkbeiner S.
      • Beauchamp G.K.
      • Mennella J.A.
      Obese women have lower monosodium glutamate taste sensitivity and prefer higher concentrations than do normal-weight women.
      Obese, n=23

      Normal-weight, n=34

      All women
      Detection threshold,

      2-AFC staircase
      Sucrose and MSG, 1 - 5.6 × 10−5 M vs. water

      Sip and taste without swallowing
      - Women with obesity had significantly higher detection thresholds for MSG,but not sucrose, when compared to normal-weight participants.
      Intensity (gLMS)Sucrose, 0-1.05 M

      MSG, 0-0.18 M

      Sip and taste without swallowing
      - Women with obesity did not differ in intensity ratings given to MSG or sucrose vs. normal weight participants.
      Preferred concentration

      Two series, forced choice tracking procedure
      Sucrose, 0.09-1.05 M

      MSG, 0.005-0.064 M

      Sip and taste without swallowing
      - Women with obesity preferred higher concentrations of MSG, but not sucrose, when compared to normal-weightparticipants.
      Bueter et al., 2011
      • Bueter M.
      • Miras A.
      • Chichger H.
      • et al.
      Alterations of sucrose preference after Roux-en-Y gastric bypass.
      Obese, n=9

      Normal weight, n=9
      Detection thresholds

      Constant Stimuli
      Sucrose, 2.1-300 mM vs. water

      Sip and taste without swallowing
      - Individuals with obesity did not differed in sucrose detection threshold vs. normal weight participants.
      Park et al., 2015
      • Park D.C.
      • Yeo J.H.
      • Ryu I.Y.
      • Kim S.H.
      • Jung J.
      • Yeo S.G.
      Differences in taste detection thresholds between normal-weight and obese young adults.
      Obese, n=18

      Normalweight, n=23

      Young adults
      Detection thresholds

      Method of limits (derivation)
      Sucrose, 0.05-2.0 g/mL

      NaCl, 0.016-0.9 g/mL

      Quinine HCl, 10−5-0.03 g/mL

      Citric acid, 0.05-0.6 g/mL

      Cotton swab (whole mouth test)
      - Individuals with obesity had significantly higher detection thresholds for NaCl vs.normal weight participants.
      Electrogustometry (EGM)22 possible EGM thresholds(8 dB to 34 dB)were measured on the anterior and posterior tongue, bilaterally.- Individuals with obesity had significantly higher EGM thresholds on both sides of the posterior tongue vs. normal weight participants.
      Holinski et al., 2015
      • Holinski F.
      • Menenakos C.
      • Haber G.
      • Olze H.
      • Ordemann J.
      Olfactory and gustatory function after bariatric surgery.
      Obese, n=44:

      Non-obese, n=23
      Taste acuity (multiple-alternative forced-choice paradigm)

      Taste strips

      Burghart Messtechnik GmbH, Wedel, Germany
      Sucrose, 0.05-0.4 g/mL

      Citric acid, 0.05-0.3 g/mL

      NaCl, 0.016-0.25 g/mL

      Quinine HCl, 0.0004-0.006 g/mL

      Strips were applied to the midline of the anterior third of the tongue.
      - Individualswith obesity had lower overall taste acuity scores vs. non-obese participants.
      Pepino et al., 2016
      • Pepino M.Y.
      • Eisenstein S.A.
      • Bischoff A.N.
      • et al.
      Sweet dopamine: sucrose preferences relate differentially to striatal D2 receptor binding and age in obesity.
      Obese, n=24

      Non-obese, n=20
      Intensity (gLMS)Sucrose, 0.00-1.05 M

      Sip and taste without swallowing
      - Individuals with obesity did not differ in any parameter vs. non-obese participants.
      Preferred concentration

      Two series, forced choice tracking procedure
      Sucrose, 0.09-1.05 M

      Sip and taste without swallowing
      Hardikar et al., 2017
      • Hardikar S.
      • Hochenberger R.
      • Villringer A.
      • Ohla K.
      Higher sensitivity to sweet and salty taste in obese compared to lean individuals.
      Obese, n=23

      Normalweight, n=31
      Recognition thresholds

      Up-down/staircase
      Sucrose, 0.01-20 g/100 mL

      NaCl, 0.01-5 g/100 mL

      Quinine HCL, 0.0001-0.025 g/100 mL

      Citric acid, 0.001-0.9 g/100 mL

      Spray dispenser (0.2 mL bolus of each tastant administered in the anterior part of the tongue).
      - Individuals with obesity had significantly lower recognition thresholds for sucrose and NaCl vs. normal weight participants.
      Intensity (VAS)Sucrose, 0.01–20 g/100 mL

      NaCl, 0.01–5 g/100 mL

      Quinine HCL, 0.0001–0.025 g/100 mL

      Citric acid, 0.001–0.9 g/100 mL

      Spray dispenser (0.2 mL bolus of each tastant administered in the anterior part of the tongue).
      - Individuals with obesity rated the lower concentrations of sucrose, NaCl and citric acid as more intense vs. normal weight participants.
      Pleasantness (VAS)Sucrose, 0.01–20 g/100 mL

      NaCl, 0.01–5 g/100 mL

      Quinine HCL, 0.0001–0.025 g/100 mL

      Citric acid, 0.001–0.9 g/100 mL

      Spray dispenser (0.2 mL bolus of each tastant administered in the anterior part of the tongue).
      - Individuals with obesity rated one of the higher concentrations of sucrose as more pleasantvs. normal weight participants.
      Notes: Sucrose, glucose and fructose are tastants for sweet taste;sodium chloride (NaCl) for salty, citric acid and hydrochloric acid (HCl) for sour, quinine hydrochloride (HCl) and 6-n-propylthiouracil (PROP) for bitter and monosodium glutamate (MSG) for umami.
      Abbreviations: 2-AFC staircase - Two-alternative forced-choice staircase procedure; gLMS - general labeled magnitude scale; VAS - Visual Analogue Scale.
      A study assessing acuity scores for supra-threshold concentrations of salt, bitter and sour tastants, using multiple-alternative forced-choice tests, found lower acuity among individuals with obesity[
      • Holinski F.
      • Menenakos C.
      • Haber G.
      • Olze H.
      • Ordemann J.
      Olfactory and gustatory function after bariatric surgery.
      ]. This is consistent with higher detection thresholds for salt[
      • Park D.C.
      • Yeo J.H.
      • Ryu I.Y.
      • Kim S.H.
      • Jung J.
      • Yeo S.G.
      Differences in taste detection thresholds between normal-weight and obese young adults.
      ], but inconsistent with evidence for unchanged or lower thresholds for salt, bitter and sour, that have also been reported[
      • Pasquet P.
      • Frelut M.L.
      • Simmen B.
      • Hladik C.M.
      • Monneuse M.O.
      Taste perception in massively obese and in non-obese adolescents.
      ,
      • Park D.C.
      • Yeo J.H.
      • Ryu I.Y.
      • Kim S.H.
      • Jung J.
      • Yeo S.G.
      Differences in taste detection thresholds between normal-weight and obese young adults.
      ,
      • Hardikar S.
      • Hochenberger R.
      • Villringer A.
      • Ohla K.
      Higher sensitivity to sweet and salty taste in obese compared to lean individuals.
      ,
      • Scruggs D.M.
      • Buffington C.
      • Cowan G.S.
      Taste acuity of the morbidly obese before and after gastric bypass surgery.
      ], as described above. On the other hand, and in accordance with findings of lower taste recognition thresholds for sweet and salt taste[
      • Pasquet P.
      • Frelut M.L.
      • Simmen B.
      • Hladik C.M.
      • Monneuse M.O.
      Taste perception in massively obese and in non-obese adolescents.
      ,
      • Hardikar S.
      • Hochenberger R.
      • Villringer A.
      • Ohla K.
      Higher sensitivity to sweet and salty taste in obese compared to lean individuals.
      ], the same studies described higher intensity ratings for these taste qualities in individuals with obesity when compared with subjects without obesity. In one of these studies this was shown using a 9-point scale in adolescents with early onset severe obesity[
      • Pasquet P.
      • Frelut M.L.
      • Simmen B.
      • Hladik C.M.
      • Monneuse M.O.
      Taste perception in massively obese and in non-obese adolescents.
      ], and in the other using a Visual Analogue Scale (VAS) in adults, where higher intensity ratings were also described for sour, but not bitter tastants[
      • Hardikar S.
      • Hochenberger R.
      • Villringer A.
      • Ohla K.
      Higher sensitivity to sweet and salty taste in obese compared to lean individuals.
      ]. However, another study also using a 9-point scale[
      • Rodin J.
      • Moskowitz H.R.
      • Bray G.A.
      Relationship between obesity, weight loss, and taste responsiveness.
      ], as well as 3 studies using magnitude estimation [
      • Thompson D.A.
      • Moskowitz H.R.
      • Campbell R.G.
      Taste and olfaction in human obesity.
      ,
      • Grinker J.
      Obesity and sweet taste.
      ,
      • Frijters J.E.
      • Rasmussen-Conrad E.L.
      Sensory discrimination, intensity perception, and affective judgment of sucrose-sweetness in the overweight.
      ] and two studies using the gLMS[
      • Pepino M.Y.
      • Eisenstein S.A.
      • Bischoff A.N.
      • et al.
      Sweet dopamine: sucrose preferences relate differentially to striatal D2 receptor binding and age in obesity.
      ,
      • Pepino M.Y.
      • Finkbeiner S.
      • Beauchamp G.K.
      • Mennella J.A.
      Obese women have lower monosodium glutamate taste sensitivity and prefer higher concentrations than do normal-weight women.
      ], did not find any differences for perceived intensity of sweet taste between weight category groups. One of the gLMS studies also did not find differences for intensity of umami taste[
      • Pepino M.Y.
      • Finkbeiner S.
      • Beauchamp G.K.
      • Mennella J.A.
      Obese women have lower monosodium glutamate taste sensitivity and prefer higher concentrations than do normal-weight women.
      ].
      While, for intensity assessment, studies already differ between reports of higher intensity in obesity relative to no weight-dependent differences, variability in findings for hedonic scaling is even greater, possibly due to higher sensitivity of this measure to heterogeneity of the scales used. In one study using a 9-point pleasantness scale, individuals with excess weight were shown to increase their pleasantness ratings as a factor of increasing concentrations of glucose, in contrast with normal weight individuals that found elevated concentrations of glucose increasingly less pleasant[
      • Rodin J.
      • Moskowitz H.R.
      • Bray G.A.
      Relationship between obesity, weight loss, and taste responsiveness.
      ]. In another study using VAS, individuals with obesity reported higher pleasantness ratings for a ‘relatively high’ sucrose concentration (i.e. three concentration steps above their individual threshold), when compared to normal weight controls[
      • Hardikar S.
      • Hochenberger R.
      • Villringer A.
      • Ohla K.
      Higher sensitivity to sweet and salty taste in obese compared to lean individuals.
      ]. However, it has also been shown that individuals with obesity rate higher sucrose concentrations as less, rather than more, pleasant in a −4 to 4 point scale[
      • Grinker J.
      Obesity and sweet taste.
      ], and several studies failed to find group differences using several distinct methods[
      • Pepino M.Y.
      • Eisenstein S.A.
      • Bischoff A.N.
      • et al.
      Sweet dopamine: sucrose preferences relate differentially to striatal D2 receptor binding and age in obesity.
      ,
      • Thompson D.A.
      • Moskowitz H.R.
      • Campbell R.G.
      Taste and olfaction in human obesity.
      ,
      • Frijters J.E.
      • Rasmussen-Conrad E.L.
      Sensory discrimination, intensity perception, and affective judgment of sucrose-sweetness in the overweight.
      ,
      • Pasquet P.
      • Frelut M.L.
      • Simmen B.
      • Hladik C.M.
      • Monneuse M.O.
      Taste perception in massively obese and in non-obese adolescents.
      ,
      • Pepino M.Y.
      • Finkbeiner S.
      • Beauchamp G.K.
      • Mennella J.A.
      Obese women have lower monosodium glutamate taste sensitivity and prefer higher concentrations than do normal-weight women.
      ]. For other taste qualities, there are reports of lower pleasantness for salt[
      • Pasquet P.
      • Frelut M.L.
      • Simmen B.
      • Hladik C.M.
      • Monneuse M.O.
      Taste perception in massively obese and in non-obese adolescents.
      ], higher pleasantness for umami [
      • Pepino M.Y.
      • Finkbeiner S.
      • Beauchamp G.K.
      • Mennella J.A.
      Obese women have lower monosodium glutamate taste sensitivity and prefer higher concentrations than do normal-weight women.
      ] and no weight-dependent differences for salt, sour or bitter[
      • Hardikar S.
      • Hochenberger R.
      • Villringer A.
      • Ohla K.
      Higher sensitivity to sweet and salty taste in obese compared to lean individuals.
      ].

      5. Changes in taste perception following bariatric surgery

      In studies conducted to test differences in taste perception following bariatric surgery, threshold estimation was also a common outcome, as shown in Table 2. Here, some[
      • Scruggs D.M.
      • Buffington C.
      • Cowan G.S.
      Taste acuity of the morbidly obese before and after gastric bypass surgery.
      ,
      • Burge J.C.
      • Schaumburg J.Z.
      • Choban P.S.
      • DiSilvestro R.A.
      • Flancbaum L.
      Changes in patients’ taste acuity after Roux-en-Y gastric bypass for clinically severe obesity.
      ,
      • Bueter M.
      • Miras A.
      • Chichger H.
      • et al.
      Alterations of sucrose preference after Roux-en-Y gastric bypass.
      ,
      • Altun H.
      • Hanci D.
      • Altun H.
      • et al.
      Improved gustatory sensitivity in morbidly obese patients after laparoscopic sleeve gastrectomy.
      ], but not all studies[
      • Pepino M.Y.
      • Bradley D.
      • Eagon J.C.
      • Sullivan S.
      • Abumrad N.A.
      • Klein S.
      Changes in taste perception and eating behavior after bariatric surgery-induced weight loss in women.
      ,
      • Holinski F.
      • Menenakos C.
      • Haber G.
      • Olze H.
      • Ordemann J.
      Olfactory and gustatory function after bariatric surgery.
      ,
      • Nance K.
      • Eagon J.C.
      • Klein S.
      • Pepino M.Y.
      Effects of sleeve gastrectomy vs. Roux-en-Y gastric bypass on eating behavior and sweet taste perception in subjects with obesity.
      ], revealed an improvement of taste sensitivity after bariatric surgery, but with inconsistent profiles across taste qualities. Specifically, following RYGB, there are reports of lower detection thresholds (i.e. increase in taste sensitivity) for sweet taste, using the constant stimuli method two months after surgery[
      • Bueter M.
      • Miras A.
      • Chichger H.
      • et al.
      Alterations of sucrose preference after Roux-en-Y gastric bypass.
      ], and also for sweet taste, but not for bitter taste, up to 3 months after surgery, using an up-down/ staircase method[
      • Burge J.C.
      • Schaumburg J.Z.
      • Choban P.S.
      • DiSilvestro R.A.
      • Flancbaum L.
      Changes in patients’ taste acuity after Roux-en-Y gastric bypass for clinically severe obesity.
      ]. The latter study also reported unaltered recognition thresholds for both sweet and bitter taste[
      • Burge J.C.
      • Schaumburg J.Z.
      • Choban P.S.
      • DiSilvestro R.A.
      • Flancbaum L.
      Changes in patients’ taste acuity after Roux-en-Y gastric bypass for clinically severe obesity.
      ]. However, another study, using the 3-stimulus drop method, reported reduced detection and recognition thresholds up to 3 months after RYGB for sour and bitter tastants, but not for sweet or salt taste[
      • Scruggs D.M.
      • Buffington C.
      • Cowan G.S.
      Taste acuity of the morbidly obese before and after gastric bypass surgery.
      ]. Furthermore, in two studies using the 2-AFC staircase method, and re-assessing patients after surgery at the point when approximately 20% of weight was lost, changes in detection threshold was not found for sweet, salt or umami taste after RYGB or Laparoscopic Adjustable Gastric Banding (LAGB)[
      • Pepino M.Y.
      • Bradley D.
      • Eagon J.C.
      • Sullivan S.
      • Abumrad N.A.
      • Klein S.
      Changes in taste perception and eating behavior after bariatric surgery-induced weight loss in women.
      ], nor for sweet or salt taste after RYGB or SG[
      • Nance K.
      • Eagon J.C.
      • Klein S.
      • Pepino M.Y.
      Effects of sleeve gastrectomy vs. Roux-en-Y gastric bypass on eating behavior and sweet taste perception in subjects with obesity.
      ]. Finally, somewhat consistently with findings of reduced detection thresholds, taste acuity scores for sour, salt, sweet and bitter tastes improved 3 months after SG in one study[
      • Altun H.
      • Hanci D.
      • Altun H.
      • et al.
      Improved gustatory sensitivity in morbidly obese patients after laparoscopic sleeve gastrectomy.
      ], but remained unaltered 6 months following SG, LAGB or RYGB in another study[
      • Holinski F.
      • Menenakos C.
      • Haber G.
      • Olze H.
      • Ordemann J.
      Olfactory and gustatory function after bariatric surgery.
      ].
      Table 2Studies that followed individuals with obesity before and after bariatric surgeryusing direct measures of taste.
      ReferenceParticipantsSurgery/Follow-upMethodologyResults
      Outcome/MethodTaste stimuli/Method of application
      Scruggs et al., 1994
      • Scruggs D.M.
      • Buffington C.
      • Cowan G.S.
      Taste acuity of the morbidly obese before and after gastric bypass surgery.
      Obese, n=6

      All women
      RYGB

      Pre, 1, 2 and 3 months postoperatively.
      Detection/ Recognition thresholds

      3-stimulus drop
      HCL, 0.5-500 mMvs. water

      Urea, 90-5.000 mMvs. water

      Sucrose, 6-5.8000 mMvs. water

      NaCl, 6-6.100 mM vs. water

      Calibrated drops of the taste solutions/ water were placed on the tongue at identical locations.
      - Following surgery there was a decrease in detection/recognition thresholds for HCL and urea, but not for sucrose or NaCl.
      Burge et al., 1995
      • Burge J.C.
      • Schaumburg J.Z.
      • Choban P.S.
      • DiSilvestro R.A.
      • Flancbaum L.
      Changes in patients’ taste acuity after Roux-en-Y gastric bypass for clinically severe obesity.
      Obese, n=14RYGB

      Pre, 1.5and 3monthspostoperatively.
      Detection/Recognition thresholds

      Up-down/staircase
      Sucrose, 0.01-0.1 mol/L

      Urea, 0.01-0.5 mol/L

      Sip and taste without swallowing
      - Following 1.5 months after surgery, detection thresholds for sucrose significantly decreased and remained so at 3 months.
      Bueter et al., 2011
      • Bueter M.
      • Miras A.
      • Chichger H.
      • et al.
      Alterations of sucrose preference after Roux-en-Y gastric bypass.
      Obese, n=9

      Normal weight, n=9
      RYGB

      1-week pre and 2 months postoperatively.

      Controls were tested at similar time points.
      Detection thresholds

      Constant Stimuli
      Sucrose, 2.1-300 mM vs. water

      Sip and taste without swallowing
      - Following surgery, patients had decreased detection thresholds for the lowest sucrose concentrations vs. controls.
      Obese, n=10

      Normalweight, n=9
      ‘Just about right’ concentration

      (200 mm VAS)
      Sucrose, 0-400 mM

      Sip and taste without swallowing
      - Following surgery there were no changes in the “just about right” concentration of sucrose vs. controls.
      Pepino et al., 2014
      • Pepino M.Y.
      • Bradley D.
      • Eagon J.C.
      • Sullivan S.
      • Abumrad N.A.
      • Klein S.
      Changes in taste perception and eating behavior after bariatric surgery-induced weight loss in women.
      Obese, n=27:

      - RYGB, n=17

      - LAGB, n= 10
      RYGB

      LAGB

      Before surgery and after ∼20% surgically-induced weight loss
      Detection thresholds

      2-AFC staircase
      Sucrose, MSG and NaCl

      All 1-10−4 M vs. water

      Sip and taste without swallowing
      - Following surgery there were no changes in taste thresholdseither in RYGB or LAGB.
      Intensity (gLMS)Sucrose, 0-1.05 M

      Glucose, 0-1.0 M

      NaCl, 0-0.56 M

      MSG, 0-0.18 M

      Sip and taste without swallowing
      - Following surgery there were no changes in suprathreshold intensity ratings for any tastant.
      Preferred concentration

      Two series, forced choice tracking procedure
      Sucrose, 0.09-1.05 M

      MSG, 0.018-0.180 M

      Sip and taste without swallowing
      - Following surgery, both in RYGB and LAGB groups lower concentrations of sucrose were preferred.
      Sweet taste palatibility

      (gLHS and gLMS)
      Sucrose 24% w/v

      Sip and taste without swallowing
      - Following RYGB, but not LAGB, the hedonic value of sucrose (gLHS) changed from pleasant to unpleasant.
      Holinski et al., 2015
      • Holinski F.
      • Menenakos C.
      • Haber G.
      • Olze H.
      • Ordemann J.
      Olfactory and gustatory function after bariatric surgery.
      Obese, n=44:

      - Pre-SG, n=37

      - Pre-LAGB, n=4

      - Pre-RYGB, n=3

      Non-obese, n=23
      LAGB

      SG

      RYGB

      Pre, 0.5, 0.75 and 6 monthspostoperatively.
      Taste acuity

      (multiple-alternative forced-choice paradigm)

      Taste strips

      Burghart Messtechnik GmbH, Wedel, Germany
      Sucrose, 0.05-0.4 g/ml

      Citric acid, 0.05-0.3 g/ml

      NaCl, 0.016-0.25 g/ml

      Quinine HCl, 0.0004-0.006 g/ml

      Strips were applied to the midline of the anterior third of the tongue.
      - Six months after surgery, taste acuity was not significantly different from controls.
      Altun et al., 2016
      • Altun H.
      • Hanci D.
      • Altun H.
      • et al.
      Improved gustatory sensitivity in morbidly obese patients after laparoscopic sleeve gastrectomy.
      Obese, n=52SG

      Pre, 1 and 3 months postoperatively.
      Taste acuity

      (multiple-alternative forced-choice paradigm)

      Taste strips

      Burghart Messtechnik GmbH, Wedel, Germany
      Sucrose, 0.05-0.4 g/ml

      Citric acid, 0.05-0.3 g/ml

      NaCl, 0.016-0.25 g/ml

      Quinine HCl, 0.0004-0.006 g/ml

      Strips were applied tothe anterior region of the tongue.
      - Three months after surgery there was a significant increase in taste acuity for all tastants across the follow-up.
      Nance et al., 2017
      • Nance K.
      • Eagon J.C.
      • Klein S.
      • Pepino M.Y.
      Effects of sleeve gastrectomy vs. Roux-en-Y gastric bypass on eating behavior and sweet taste perception in subjects with obesity.
      Obese, n=31:

      - Pre-RYGB, n=23

      -Pre-SG, n=8

      RYGB

      SG

      Before surgery and after ∼20% surgically-induced weight loss
      Detection thresholds

      2-AFC staircase
      Sucrose, glucose and NaCl, 1 × 10−4-1M vs. water

      Sip and taste without swallowing
      - There wasno changein detection thresholds after RYGB or SG.
      Intensity (gLMS)Sucrose, 0.90-1050 mmol/L

      Glucose, 0.00-1000 mmol/L

      NaCl, 0.00-560 mmol/L

      MSG, 0.00-180 mmol/L

      Sip and taste without swallowing
      - There were no changesin perceived intensities after RYGB or SG.
      Preferred concentration

      Two series, forced choice tracking procedure
      Sucrose, 90-1005 mmol/L

      MSG, 18-180 mmol/L (warmed)

      Sip and taste without swallowing
      - Following surgery, both in RYGB and SG groups lower concentrations of sucrose were preferred.
      Sweet taste palatibility

      (gLHS and gLMS)
      Sucrose 24% w/v

      Sip and taste without swallowing
      - Following both RYGB and SG, the hedonic of sucrose changed from pleasant to unpleasant.
      Notes: Sucrose, and glucose are tastants for sweet taste; sodium chloride (NaCl) for salty, quinine hydrochloride and urea for bitter; citric acid and hydrochloric acid (HCl) for sour and monosodium glutamate (MSG) for umami.
      Abbreviations: 2-AFC staircase - Two-alternative forced-choice staircase procedure; gLHS - general labeled hedonic scale; gLMS - general labeled magnitude scale; LAGB- Laparoscopic Adjustable Gastric Banding; RYGB - Roux-en-Y Gastric Bypass; SG - Sleeve Gastrectomy; VAS - Visual Analogue Scale.
      Very few studies assessed suprathreshold intensity or hedonic assessments after bariatric surgery. Pepino et al. 2014 [
      • Pepino M.Y.
      • Bradley D.
      • Eagon J.C.
      • Sullivan S.
      • Abumrad N.A.
      • Klein S.
      Changes in taste perception and eating behavior after bariatric surgery-induced weight loss in women.
      ] showed that, in patients treated with RYGB or LAGB, following ~20% of surgically-induced weight-loss, there were no significant changes in suprathreshold intensity ratings (gLMS) for sweet, salt or umami tastants, while changes in preferences for sweet, but not umami, tastants did occur, as measured by a two-series, forced choice tracking procedure[
      • Pepino M.Y.
      • Bradley D.
      • Eagon J.C.
      • Sullivan S.
      • Abumrad N.A.
      • Klein S.
      Changes in taste perception and eating behavior after bariatric surgery-induced weight loss in women.
      ]. The authors also found that following RYGB, but not LAGB, the hedonic value of sucrose tasting, as measured by the gLHS, changed from pleasant to unpleasant[
      • Pepino M.Y.
      • Bradley D.
      • Eagon J.C.
      • Sullivan S.
      • Abumrad N.A.
      • Klein S.
      Changes in taste perception and eating behavior after bariatric surgery-induced weight loss in women.
      ]. The same group repeated this experiment in another bariatric group, following either RYGB or SG, confirming no postoperative change in suprathreshold intensity ratings (gLMS) for sweet, salt or umami taste, nor in preference for umami, but with reduction in preference and hedonic scores for sweet taste after both surgery types[
      • Nance K.
      • Eagon J.C.
      • Klein S.
      • Pepino M.Y.
      Effects of sleeve gastrectomy vs. Roux-en-Y gastric bypass on eating behavior and sweet taste perception in subjects with obesity.
      ]. However, in work from another group, assessments of the ‘just about right’ concentration for sucrose, with ratings given on a VAS, did not reveal changes after RYGB[
      • Bueter M.
      • Miras A.
      • Chichger H.
      • et al.
      Alterations of sucrose preference after Roux-en-Y gastric bypass.
      ]. Globally, the available literature does not support changes in the sensory-discriminative component of taste perception induced by bariatric surgery, but provides limited evidence in support of changes of reward-related and hedonic assessments, namely of sweet taste.

      6. Discussion

      In this review we provide perspective on the data available to support, or contradict, the general interpretation that individuals with obesity have reduced sweet taste perception, as is frequently proposed[
      • Gutierrez R.
      • Fonseca E.
      • Simon S.A.
      The neuroscience of sugars in taste, gut-reward, feeding circuits, and obesity.
      ]. This interpretation has typically been framed jointly with the evidence for decreased availability of striatal D2R in individuals with obesity, with both gustatory and dopaminergic factors proposed to contribute towards compensatory food consumption and weight gain[
      • Gutierrez R.
      • Fonseca E.
      • Simon S.A.
      The neuroscience of sugars in taste, gut-reward, feeding circuits, and obesity.
      ]. In fact, in flies there is pre-clinical evidence that a high sugar diet results in diminished sweet perception, via decreased response of ‘sweet-taste sensing neurons’[
      • May C.E.
      • Vaziri A.
      • Lin Y.Q.
      • et al.
      High dietary sugar reshapes sweet taste to promote feeding behavior in drosophila melanogaster.
      ]. Furthermore, in healthy human volunteers, reduction of sugar consumption has been shown to result in increased perception of sweet taste intensity, while pleasantness ratings remained unaltered[
      • Wise P.M.
      • Nattress L.
      • Flammer L.J.
      • Beauchamp G.K.
      Reduced dietary intake of simple sugars alters perceived sweet taste intensity but not perceived pleasantness.
      ]. Finally, a single nucleotide polymorphism, identified in humans, has been associated with higher perceived intensity of several sweet compounds, as well as with consumption of sweet foods[
      • Hwang L.D.
      • Lin C.
      • Gharahkhani P.
      • et al.
      New insight into human sweet taste: a genome-wide association study of the perception and intake of sweet substances.
      ], which may contribute towards interindividual differences in weight. As is shown here, however, the available studies directly assessing pure taste function of individuals with obesity, either comparing with normal weight control subjects, or assessing changes following bariatric surgery, do not clearly support the general interpretation regarding reduced sweet taste perception in obesity.
      Studies comparing sweet taste detection thresholds between participants with and without obesity have found no differences[
      • Grinker J.
      Obesity and sweet taste.
      ,
      • Frijters J.E.
      • Rasmussen-Conrad E.L.
      Sensory discrimination, intensity perception, and affective judgment of sucrose-sweetness in the overweight.
      ,
      • Pepino M.Y.
      • Finkbeiner S.
      • Beauchamp G.K.
      • Mennella J.A.
      Obese women have lower monosodium glutamate taste sensitivity and prefer higher concentrations than do normal-weight women.
      ,
      • Scruggs D.M.
      • Buffington C.
      • Cowan G.S.
      Taste acuity of the morbidly obese before and after gastric bypass surgery.
      ,
      • Bueter M.
      • Miras A.
      • Chichger H.
      • et al.
      Alterations of sucrose preference after Roux-en-Y gastric bypass.
      ]. On the other hand, some[
      • Pasquet P.
      • Frelut M.L.
      • Simmen B.
      • Hladik C.M.
      • Monneuse M.O.
      Taste perception in massively obese and in non-obese adolescents.
      ,
      • Hardikar S.
      • Hochenberger R.
      • Villringer A.
      • Ohla K.
      Higher sensitivity to sweet and salty taste in obese compared to lean individuals.
      ], but not all studies[
      • Scruggs D.M.
      • Buffington C.
      • Cowan G.S.
      Taste acuity of the morbidly obese before and after gastric bypass surgery.
      ], have described reduced recognition thresholds among individuals with obesity, that suggest enhanced, rather than reduced, sweet taste sensitivity. Inconsistently, after bariatric surgery there is limited evidence of reduced sweet taste detection thresholds[
      • Scruggs D.M.
      • Buffington C.
      • Cowan G.S.
      Taste acuity of the morbidly obese before and after gastric bypass surgery.
      ,
      • Burge J.C.
      • Schaumburg J.Z.
      • Choban P.S.
      • DiSilvestro R.A.
      • Flancbaum L.
      Changes in patients’ taste acuity after Roux-en-Y gastric bypass for clinically severe obesity.
      ,
      • Bueter M.
      • Miras A.
      • Chichger H.
      • et al.
      Alterations of sucrose preference after Roux-en-Y gastric bypass.
      ,
      • Pepino M.Y.
      • Bradley D.
      • Eagon J.C.
      • Sullivan S.
      • Abumrad N.A.
      • Klein S.
      Changes in taste perception and eating behavior after bariatric surgery-induced weight loss in women.
      ,
      • Nance K.
      • Eagon J.C.
      • Klein S.
      • Pepino M.Y.
      Effects of sleeve gastrectomy vs. Roux-en-Y gastric bypass on eating behavior and sweet taste perception in subjects with obesity.
      ], thus suggesting enhanced sweet taste sensitivity with weight loss, and no evidence of change in recognition thresholds[
      • Scruggs D.M.
      • Buffington C.
      • Cowan G.S.
      Taste acuity of the morbidly obese before and after gastric bypass surgery.
      ,
      • Burge J.C.
      • Schaumburg J.Z.
      • Choban P.S.
      • DiSilvestro R.A.
      • Flancbaum L.
      Changes in patients’ taste acuity after Roux-en-Y gastric bypass for clinically severe obesity.
      ]. Regarding suprathreshold sweet taste intensity assessments, while most studies find no obesity-dependent [
      • Pepino M.Y.
      • Eisenstein S.A.
      • Bischoff A.N.
      • et al.
      Sweet dopamine: sucrose preferences relate differentially to striatal D2 receptor binding and age in obesity.
      ,
      • Rodin J.
      • Moskowitz H.R.
      • Bray G.A.
      Relationship between obesity, weight loss, and taste responsiveness.
      ,
      • Thompson D.A.
      • Moskowitz H.R.
      • Campbell R.G.
      Taste and olfaction in human obesity.
      ,
      • Grinker J.
      Obesity and sweet taste.
      ,
      • Frijters J.E.
      • Rasmussen-Conrad E.L.
      Sensory discrimination, intensity perception, and affective judgment of sucrose-sweetness in the overweight.
      ,
      • Pepino M.Y.
      • Finkbeiner S.
      • Beauchamp G.K.
      • Mennella J.A.
      Obese women have lower monosodium glutamate taste sensitivity and prefer higher concentrations than do normal-weight women.
      ] or bariatric surgery-dependent [
      • Pepino M.Y.
      • Bradley D.
      • Eagon J.C.
      • Sullivan S.
      • Abumrad N.A.
      • Klein S.
      Changes in taste perception and eating behavior after bariatric surgery-induced weight loss in women.
      ,
      • Nance K.
      • Eagon J.C.
      • Klein S.
      • Pepino M.Y.
      Effects of sleeve gastrectomy vs. Roux-en-Y gastric bypass on eating behavior and sweet taste perception in subjects with obesity.
      ] effects, reports of increased intensity ratings among individuals with obesity are available in two studies[
      • Pasquet P.
      • Frelut M.L.
      • Simmen B.
      • Hladik C.M.
      • Monneuse M.O.
      Taste perception in massively obese and in non-obese adolescents.
      ,
      • Hardikar S.
      • Hochenberger R.
      • Villringer A.
      • Ohla K.
      Higher sensitivity to sweet and salty taste in obese compared to lean individuals.
      ]. For other taste qualities, while there is less evidence that is mostly negative, some studies reveal increased detection thresholds[
      • Pepino M.Y.
      • Finkbeiner S.
      • Beauchamp G.K.
      • Mennella J.A.
      Obese women have lower monosodium glutamate taste sensitivity and prefer higher concentrations than do normal-weight women.
      ,
      • Park D.C.
      • Yeo J.H.
      • Ryu I.Y.
      • Kim S.H.
      • Jung J.
      • Yeo S.G.
      Differences in taste detection thresholds between normal-weight and obese young adults.
      ], reduced recognition thresholds [
      • Pasquet P.
      • Frelut M.L.
      • Simmen B.
      • Hladik C.M.
      • Monneuse M.O.
      Taste perception in massively obese and in non-obese adolescents.
      ,
      • Hardikar S.
      • Hochenberger R.
      • Villringer A.
      • Ohla K.
      Higher sensitivity to sweet and salty taste in obese compared to lean individuals.
      ] or higher intensity ratings [
      • Pasquet P.
      • Frelut M.L.
      • Simmen B.
      • Hladik C.M.
      • Monneuse M.O.
      Taste perception in massively obese and in non-obese adolescents.
      ,
      • Hardikar S.
      • Hochenberger R.
      • Villringer A.
      • Ohla K.
      Higher sensitivity to sweet and salty taste in obese compared to lean individuals.
      ] in individuals with obesity, as well as reduced detection [
      • Scruggs D.M.
      • Buffington C.
      • Cowan G.S.
      Taste acuity of the morbidly obese before and after gastric bypass surgery.
      ] or recognition [
      • Scruggs D.M.
      • Buffington C.
      • Cowan G.S.
      Taste acuity of the morbidly obese before and after gastric bypass surgery.
      ] thresholds after bariatric surgery.
      Regarding the hedonic dimension of taste, comparisons between individuals with obesity and normal-weight controls were mostly inconclusive, with no evidence of differences in sweet taste among participants with obesity in 4 studies[
      • Pepino M.Y.
      • Eisenstein S.A.
      • Bischoff A.N.
      • et al.
      Sweet dopamine: sucrose preferences relate differentially to striatal D2 receptor binding and age in obesity.
      ,
      • Frijters J.E.
      • Rasmussen-Conrad E.L.
      Sensory discrimination, intensity perception, and affective judgment of sucrose-sweetness in the overweight.
      ,
      • Pasquet P.
      • Frelut M.L.
      • Simmen B.
      • Hladik C.M.
      • Monneuse M.O.
      Taste perception in massively obese and in non-obese adolescents.
      ,
      • Pepino M.Y.
      • Finkbeiner S.
      • Beauchamp G.K.
      • Mennella J.A.
      Obese women have lower monosodium glutamate taste sensitivity and prefer higher concentrations than do normal-weight women.
      ], nor in salt, bitter or sour tastes in other studies[
      • Pasquet P.
      • Frelut M.L.
      • Simmen B.
      • Hladik C.M.
      • Monneuse M.O.
      Taste perception in massively obese and in non-obese adolescents.
      ,
      • Hardikar S.
      • Hochenberger R.
      • Villringer A.
      • Ohla K.
      Higher sensitivity to sweet and salty taste in obese compared to lean individuals.
      ]. Other studies, however, revealed increased[
      • Rodin J.
      • Moskowitz H.R.
      • Bray G.A.
      Relationship between obesity, weight loss, and taste responsiveness.
      ,
      • Hardikar S.
      • Hochenberger R.
      • Villringer A.
      • Ohla K.
      Higher sensitivity to sweet and salty taste in obese compared to lean individuals.
      ], or reduced[
      • Grinker J.
      Obesity and sweet taste.
      ], hedonic ratings for sweet taste, reduced hedonic ratings for salt tastants [
      • Pasquet P.
      • Frelut M.L.
      • Simmen B.
      • Hladik C.M.
      • Monneuse M.O.
      Taste perception in massively obese and in non-obese adolescents.
      ] and increased preference for umami taste[
      • Pepino M.Y.
      • Finkbeiner S.
      • Beauchamp G.K.
      • Mennella J.A.
      Obese women have lower monosodium glutamate taste sensitivity and prefer higher concentrations than do normal-weight women.
      ], among individuals with obesity. While studies after bariatric surgery are scarce, two of these studies support adjustments of sweet taste perception leading to lower preferences and hedonic scores[
      • Pepino M.Y.
      • Bradley D.
      • Eagon J.C.
      • Sullivan S.
      • Abumrad N.A.
      • Klein S.
      Changes in taste perception and eating behavior after bariatric surgery-induced weight loss in women.
      ,
      • Nance K.
      • Eagon J.C.
      • Klein S.
      • Pepino M.Y.
      Effects of sleeve gastrectomy vs. Roux-en-Y gastric bypass on eating behavior and sweet taste perception in subjects with obesity.
      ]. However, confidence in the results of available research is limited, given methodological variability between studies, small sample sizes, and lack of adequate controls in longitudinal studies. More studies, with larger patient samples, are needed to address limitations of previous research.
      In fact, we have very recently published results of a multicenter longitudinal cohort, recruiting more than 200 bariatric patients, and showing similar variation in suprathreshold intensity and pleasantness ratings of several tastants, including sweet, between those treated with bariatric surgery and a control group awaiting surgery. While our research is consistent with limited overall effects of bariatric surgery on taste, patients with higher sweet intensity ratings before surgery lost more weight, and reduction of sweet intensity ratings correlated with weight loss [
      • Ribeiro G.
      • Camacho M.
      • Fernandes A.B.
      • Cotovio G.
      • Torres S.
      • Oliveira-Maia A.J.
      Food Reward in Bariatric Surgery Portuguese Study Group
      Reward-related gustatory and psychometric predictors of weight loss following bariatric surgery: a multicenter cohort study.
      ]. These findings, suggesting that associations between taste and bariatric surgery may be better interpreted at the individual, rather than the group level, are consistent with other recent work testing liking ratings for sucrose-sweetened mixtures containing fat, and showing that, in patients receiving RYGB, but not SG, higher preoperative preference for sucrose-sweetened mixtures, as well as activation of the ventral tegmental area by those mixtures, predicted greater weight loss[
      • Smith K.R.
      • Papantoni A.
      • Veldhuizen M.G.
      • et al.
      Taste-related reward is associated with weight loss following bariatric surgery.
      ]. Hypotheses considering interactions between sweet preferences and dopamine-related brain neural activity may thus be relevant for weight-loss induced by bariatric surgery, and should be further assessed in future research .

      7. Conclusions

      Available research suggests that changes of sweet taste with obesity and weight-loss may be more complex than simply considering decreased sweet taste perception. However, there are several indications that sweet taste may be related to weight and, importantly, that it may be a useful marker in the context of bariatric surgery, suggesting the need for further research with refined methods and large sample sizes.

      Declaration of Competing Interest

      Competing interests are not reported by Ribeiro. Oliveira-Maia is recipient of a grant from Schuhfried GmBH for norming and validation of cognitive tests, and national coordinator for Portugal of a Non-interventional Study (EDMS-ERI-143085581, 4.0) to characterize a Treatment-Resistant Depression Cohort in Europe, sponsored by Janssen-Cilag Ltd, and a of a trial of psilocybin therapy for treatment-resistant depression, sponsored by Compass Pathways, Ltd (EudraCT NUMBER: 2017–003288–36).

      Authors Contributions

      Ribeiro conducted the literature search. Ribeiro and Oliveira-Maia wrote the manuscript and approved the final version.

      Funding/Support

      Oliveira-Maia was supported by grants from the BIAL Foundation (176/10), and from Fundação para a Ciência e Tecnologia (FCT) through a Junior Research and Career Development Award from the Harvard Medical School Portugal Program (HMSP/ICJ/0020/2011) and grant PTDC/MED-NEU/31331/2017; and is funded by a Starting Grant from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement No 950357). Ribeiro was funded by doctoral fellowships from Universidade de Lisboa (BD/2015Call) and FCT (SFRH/BD/128783/2017).

      Role of the Funder/Sponsor

      The funding sources did not participate in interpretation of the data, preparation or review of the manuscript.

      Appendix. Supplementary materials

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