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Champalimaud Research & Clinical Centre, Champalimaud Centre for the Unknown, Av. de Brasília, Doca de Pedrouços, 1400-038 Lisboa, PortugalLisbon Academic Medical Centre PhD Program, Faculdade de Medicina, Universidade de Lisboa, Avenida Professor Egas Moniz, 1649-028 Lisboa, Portugal
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, PortugalNOVA Medical School, NMS, Universidade Nova de Lisboa, Campo Mártires da Pátria 130, 1169-056 Lisboa, Portugal
Obesity has been associated to altered sensitivity to food reward.
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Sugar triggers brain reward circuitries, encouraging its consumption.
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There is methodological heterogeneity in studies of taste perception in obesity.
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Research on the association between obesity and sweet taste perception is inconclusive.
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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.
]. 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[
], which is thought to be related to changes in reward-related brain neurocircuitry, namely decreased striatal availability of dopamine D2 receptors (D2R)[
]. 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[
] 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[
]. 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[
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[
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[
]. 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. [
], 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)[
]. In addition to informing feeding decisions, this system contributes to the physiological regulation of starch and fat digestion, initiated through salivary secretions[
]. 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[
]. 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[
]. 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)[
]. 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[
]. 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[
]. Regarding salt taste, amiloride-sensitive epithelial sodium channels have been shown to be involved in rodents, although in humans, further research is needed[
]. 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[
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 [
]. 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[
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 [
]). 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 [
] (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. 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
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
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 [
]. 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[
]. 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[
]. Additionally, one of these studies revealed higher electrogustometry (EGM) thresholds in individuals with obesity, despite no correlations with chemical thresholds[
]. 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[
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.
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.
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[
], 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[
], 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[
], 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[
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[
]. 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[
]. 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[
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[
], 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[
]. 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[
]. 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)[
]. 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[
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.
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.
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.
] 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[
]. 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[
]. 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[
]. 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[
]. 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[
]. 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[
]. 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’[
]. 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[
]. 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[
], 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[
], 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[
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[
], 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[
]. 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 [
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[
]. 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.
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.
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