TY - JOUR
AU1 - Spector, Alan, C
AU2 - Kapoor,, Natasha
AU3 - Price, Ruth, K
AU4 - Pepino, M, Yanina
AU5 - Livingstone, M Barbara, E
AU6 - Le Roux, Carel, W
AB - Abstract This article provides a summary of the topics discussed at the symposium titled “Bariatric Surgery and Its Effects on Taste and Food Selection,” which was held at the Fortieth Annual Meeting of the Association for Chemoreception Sciences. Bariatric surgery such as Roux-en-Y gastric bypass (RYGB) is currently one of the most effective treatments available for weight loss and Type 2 diabetes. For this reason, it is of great interest to clinicians as well as to basic scientists studying the controls of feeding and energy balance. Despite the commonly held view by clinicians that RYGB patients change their food preferences away from fats and sugars in favor of less energy dense alternatives such as vegetables, the empirical support for this claim is equivocal. It is currently thought that the taste and palatability of fats and sugars are affected by the surgery. Some key preclinical and clinical findings addressing these issues were evaluated in this symposium. food choice, gustatory, nutrition, Roux-en-Y gastric bypass, taste aversions, taste preferences On 18 April 2018, a symposium titled “Bariatric Surgery and Its Effects on Taste and Food Selection” was held at the Fortieth Annual Meeting of the Association for Chemoreception Sciences in Bonita Springs, FL. This article provides a summary of the major points discussed by the speakers. The prevailing views on bariatric surgery regarding the effects on taste and food selection (Carel W. le Roux and Natasha Kapoor) Obesity is a complex and chronic brain disease. Diet, exercise, medications, and surgical treatments are options for intentional weight loss (AMA; CMA; Mingrone et al. 2015). Approximately 15–30% bodyweight loss can be achieved by surgery and is usually sustained long term (Sjöström 2013). There are different types of bariatric procedures, and the decision that operations will be used depends on the metabolic benefits, surgical risks related to each patient, geographical preferences, and surgeons’ experience. This symposium deals with one of the most common bariatric surgeries practised today, Roux-en-Y gastric bypass (RYGB). Roux-en-Y gastric bypass RYGB was first performed in 1967 (Alden 1977) and is one of the most effective and commonly performed procedures resulting in weight loss that is maintained (Buchwald and Oien 2013). The procedure involves anatomical rearrangement of the gastrointestinal tract with the stomach being divided into 2 parts—the gastric pouch 15–30 ml in volume and the remnant stomach that has no contact with food. The small gastric pouch is anastomosed to the mid-jejunum. The duodenum and proximal limb of the jejunum is anastomosed to the lower jejunum for the continuity of the intestine. Contrary to popular belief, this procedure does not work through restriction as food is transferred straight to the small intestine due to the absence of a sphincter between the stomach and small bowel. The gastric and biliopancreatic secretions proceed down the biliopancreatic limb and join food distal to the jejunojejunostomy. Food mixes with the gastric and biliopancreatic juices in the common channel that is usually between 2 and 5 m long (Olbers et al. 2003). Eating behavior and gut hormones The weight loss associated with RYGB in humans is not due to caloric malabsorption as energy content of feces remains unchanged (Carswell et al. 2014). Rather, the weight loss appears to be due to a combination of an increase in energy expenditure and, importantly, with respect to the topic of this symposium, a reduction in caloric intake. The latter is associated with symptoms of reduced hunger and increased satiation. The desire to acquire and eat food can be defined as hunger, whereas satiation is the satisfaction resulting at the end of the eating period (Blundell 1991). Both hunger and satiation are partly under the control of hormonal signals. Enteroendocrine cells in the small intestine release satiation hormones in response to direct contact with nutrients (Chambers et al. 2014). These endocrine signals can activate vagal nerve endings or stimulate the target of vagal afferents, the nucleus tractus solitarius, directly. The changes in the gut after surgery cause nutrients to arrive at the distal bowel sooner, initiating earlier secretion of satiation hormones PYY, GLP-1, and oxyntomodulin (Melissas et al. 2008; Chambers et al. 2014; Vigneshwaran et al. 2016). The earlier and exaggerated rise of postprandial satiation gut hormones after RYGB is proportionate with the weight loss after surgery. When these satiation gut hormones are blocked in humans and rats using octreotide, it results in increased food intake (le Roux et al. 2007; Goldstone et al. 2016). All of these potential mechanisms may contribute to the effects of RYGB, but the relative contribution of each, for every individual, remains to be understood. RYGB and food preferences Some studies have found that food preferences appear to change after RYGB, but these are, for the most part, based on measures dependent on verbal report (see Dr. Barbara Livingstone’s section) (Mathes and Spector 2012). It has been suggested that some patients have a reduction in preference for high-fat and sugary foods after RYGB. In an attempt to understand the putative change in food preference studies were conducted to evaluate changes in taste. A psychophysical study by le Roux et al. (2011) found a small leftward shift (i.e., increased sensitivity) in the taste detection of sucrose (~0.2 log10), whereas Pepino et al. (2014) found no change in taste detection of sucrose (or glucose, sodium chloride [NaCl], and monosodium glutamate [MSG]). This is reminiscent of prior disparities regarding taste sensitivity changes caused by RYGB (Scruggs et al. 1994; Burge et al. 1995). The difference between the outcomes of these studies probably stems from significant variation in the methodology employed. Nevertheless, when changes in taste sensitivity have been found, they have been relatively small. Appetitive behavior, however, has been shown in some cases to be significantly reduced after RYGB. Miras et al. (2012), using a progressive ratio task before and within 8 weeks after surgery, showed a reduction by 50% in the amount of effort the subjects were prepared to exert (breakpoint) to obtain the reward of a sugary foods. Studies using functional magnetic resonance imaging have also suggested a reduction in blood flow to areas of the brain associated with processing reward when pictures of calorie-dense foods are shown to patients after RYGB, in comparison to patients with equivalent weight loss with gastric banding (Scholtz et al. 2014). In contrast to Miras et al., a study in patients who were in the weight maintenance phase showed the breakpoint of a progressive ratio task to be similar in controls and patients after RYGB. When octreotide was used to block the satiation gut hormone response in these patients, an increase in both the breakpoint in the progressive ratio task and the brain “reward” response for palatable food was seen (Goldstone et al. 2016). Potential explanations include that the breakpoint may be different in when subjects are in a steep negative energy balance in comparison to when energy balance has been achieved after weight loss but that gut hormones may contribute to appetitive behavior. Attempts are now underway to use direct measures of behavior such as directly quantifying macronutrient content from ad libitum meals during a buffet lunch. Early data suggest that in a group of 60 patients having either RYGB or vertical sleeve gastrectomy (SG), no major shifts in preferences have been observed 6 months after surgery (Nielsen et al. 2017). Longer follow-up data and subgroup analyses are awaited. Conclusion Bariatric surgery results in weight loss, and the combined contribution of hormonal, neural, and other visceral signal plays an important role. The putative changes in food preferences and reward after surgery could potentially contribute toward the decrease in calorie intake. Understanding the nature and causes of changes in food preferences after RYGB may allow surgery to be utilized more effectively and may also facilitate the development of new weight-loss therapies. The effects of Roux-en-Y gastric bypass on food selection and taste-related motivation (Alan C. Spector) Introduction to the problem My laboratory has adopted a rat model of RYGB with an eye toward identifying the effects of this remarkable reorganization of the alimentary tract on food selection and taste-related motivation. Ultimately, we, like other groups, hope to exploit the accessibility of the rat model to further uncover the physiological and neural mechanisms underlying the surgically induced changes in taste-driven ingestive behavior. Indeed, our studies have been conceptually coordinated with those of some of the other speakers in this symposium in an effort to enhance the translational relevance of our experimental outcomes while providing some guidance to the human work. Here, I would like to briefly review some of the key findings from our studies and provide a glimpse of the future directions we plan to follow. High-fat diet avoidance One of the most consistent findings regarding food intake from laboratories that have adopted a rodent model of RYGB is the postsurgical decline in preference for a high-fat diet (HFD) (Zheng et al. 2009; le Roux et al. 2011; Shin et al. 2011; Saeidi et al. 2012; Seyfried et al. 2013; Wilson-Pérez et al. 2013). After RYGB, in addition to lowering their total caloric intake, animals will decrease their relative intake of a diet that is high in fat when a low-fat alternative, such as common laboratory chow, is simultaneously available. For example, Figure 1 provides unpublished intake data during the postoperative (PO) recovery period from a study we published (Mathes, Bohnenkamp, le Roux, et al. 2015) a few years ago in which some rats had access to both HFD and laboratory chow before and after either sham surgery (SHAM) or RYGB. When the diets were reintroduced on PO day 3, initially there was no difference between the groups with respect to their relative ingestion of the 2 foods, but over days, the rats in the RYGB group decreased their preference for the HFD in contrast to the stable and high preference displayed by the SHAM rats. This decline in mean HFD preference was progressive and never dropped below indifference during the test period. This suggested that the change in HFD intake relative to chow after RYGB is dependent on experience and that animals still take a reasonably high proportion of their total calories from the food; in other words, the avoidance could be learned and does not necessarily represent an absolute rejection of the HFD. Figure 1. View largeDownload slide High-fat diet (HFD) preference versus laboratory chow (calculated from calories) in rats after Roux-en-Y gastric bypass (RYGB) or sham surgery (SHAM) across postoperative (PO) days. The animals had been exposed to HFD presurgically along with chow. HFD was returned on PO day 3. Two-way mixed repeated-measures ANOVA results: Surgical Group, F1,15 = 10.93, P = 0.005; Days, F11,165 = 6.16, P < 0.001; Surgical Group × Day, F11,165 = 2.02, P = 0.03. These represent the unpublished recovery data that were from rats in a published study (Mathes, Bohnenkamp, Blonde, et al. 2015). Figure 1. View largeDownload slide High-fat diet (HFD) preference versus laboratory chow (calculated from calories) in rats after Roux-en-Y gastric bypass (RYGB) or sham surgery (SHAM) across postoperative (PO) days. The animals had been exposed to HFD presurgically along with chow. HFD was returned on PO day 3. Two-way mixed repeated-measures ANOVA results: Surgical Group, F1,15 = 10.93, P = 0.005; Days, F11,165 = 6.16, P < 0.001; Surgical Group × Day, F11,165 = 2.02, P = 0.03. These represent the unpublished recovery data that were from rats in a published study (Mathes, Bohnenkamp, Blonde, et al. 2015). Two-bottle preference When a fat emulsion is pitted against water in long-term (usually ~24 h) 2-bottle intake tests, SHAM rats will increase their fat preference in a concentration-dependent manner, but RYGB rats show severely blunted increases in fat preference (le Roux et al. 2011). Similar results have been obtained with sucrose as the test stimulus (Bueter et al. 2011). Interestingly, the preference/avoidance functions from 2-bottle tests with compounds representing other basic taste qualities such as NaCl (“salty”), quinine (“bitter”), and citric acid (“sour”) are unaffected by the surgery (Bueter et al. 2011). Moreover, the preference for fat or sucrose solutions relative to water never drops much below indifference (i.e., 50% preference). Thus, a complete avoidance of intake of these solutions is not observed. It is important to remember that these animals do not need to drink the test solutions for sustenance because they have laboratory chow and water freely available. Brief access test The results showing that rats display a decreased preference for fats and sugars after RYGB are consistent with some reports (mostly using indirect measures) in the clinical literature (Mathes and Spector 2012). However, does this change in preference represent a fundamental shift in the orosensory motivational properties of these types of foods and fluids? In simple terms, is there a decrease of the unconditioned palatability of fats and sugars after RYGB? It is well documented that the intake in 2-bottle preference tests can be influenced by nontaste factors of a postoral origin (McCleary 1953; Shuford 1959; Stellar 1967; Rabe and Corbit 1973; Weingarten and Watson 1982; Grill et al. 1987; Nissenbaum and Sclafani 1987). One way that investigators can overcome the interpretive limitations of the 2-bottle test to assess orosensory-driven ingestive motivation is to use a procedure appropriately called the brief access test (Young and Madsen 1963; Davis 1973; Smith et al. 1992; Spector et al. 1993, 1996; Smith 2001; Glendinning et al. 2002). In this procedure, animals are given randomized trials during which, for a very brief period of time, usually on the order of seconds, a taste stimulus is available for sampling, and the licking response is measured. The facts that the trial duration is so short and animals can only ingest a very small amount minimize the influence of postingestive events on the licking response. Mathes et al. (2012) used this procedure to assess unconditioned responsiveness to sucrose in SHAM and RYGB rats. To our surprise, we found that concentration-dependent licking to sucrose was not attenuated by RYGB regardless of whether the animals were tested fasted or not. In fact, when nondeprived, rats actually had a leftward shift in the sucrose concentration–response function indicating greater responsiveness as assessed by this test. Moreover, the RYGB rats initiated ~2–3 more trials compared with the SHAM controls regardless of fasting state. In contrast, other groups have reported some degree of decline in sucrose responsiveness after RYGB as assessed by a brief access test (Hajnal et al. 2010; Shin et al. 2011; Tichansky et al. 2011), but there were significant methodological differences between those studies and the Mathes et al.’s study that could have contributed to the disparity in the results. Regardless, the Mathes et al.’s results clearly show that a decrease in concentration-dependent licking to sucrose in a brief access test in RYGB rats is not universally observed. le Roux et al. (2011) found no difference in the licking responsiveness to a range of concentrations of the fat emulsion Intralipid between RYGB and SHAM rats as assessed in a brief access test. Progressive ratio Another way to assess the motivational potency of a taste stimulus is to use it as a reinforcer in an operant-conditioning schedule called a progressive ratio (Hodos 1961). In this task, a given response (e.g., pressing a lever, licking a dry drinking spout) is reinforced with a very small amount of a taste stimulus that is normally preferred in drinking tests. After each reinforcer delivery, the response demand increases. At some point, referred to as the breakpoint, the animal quits responding; the higher the breakpoint, the more effective the reinforcer is at driving responding. The breakpoint is thought to be a proxy of the motivational potency of the taste stimulus serving as the reinforcer under the test conditions present. The task is used to minimize the influence of satiation on responding in the assessment of the efficacy of a reinforcer (e.g., “reward”) and thus is well suited for studies on the effect of RYGB on taste-driven motivation. Mathes et al. trained rats before surgery to lick a dry drinking spout 10 times to receive a small amount (~75 µl) of 1.0 M sucrose. After each sucrose delivery, the response requirement increased by 10 licks (10, 20, 30, 40…). There was no difference in the mean breakpoint between RYGB and SHAM rats before or after surgery. Similar results were obtained for other reinforcers such as the fluid emulsion Intralipid (Mathes, Bohnenkamp, Blonde, et al. 2015). These progressive ratio results from the rat model are in contrast with those from a human study. Miras et al. (2012) instructed obese humans and normal-weight controls to press a computer mouse key to eat a single piece of chocolate candy. The response demand started at 10 clicks and then progressed geometrically by a factor of 2 (10, 20, 40, 80…). Interestingly, there was no difference in the willingness for the 2 groups of subjects to press the mouse key (i.e., breakpoints) for the chocolate reinforcer. However, when the obese subjects were tested 8 weeks after RYGB and the control subjects were tested after a comparable time interval, the RYGB patients significantly decreased their median breakpoint by half, whereas the control subjects were stable. Interestingly there was a significant correlation (r > 0.80) between the postsurgical drop in body mass index and the decrease in breakpoint in the RYGB patients. The basis of disparity between the rat and human progressive ratio findings remains to be resolved. Of course, the explicit features of the method differed between the studies as well such as the specific reinforcer and the exact schedule of reinforcement used (linear vs. geometric), to name a couple of possibilities. Another possibility is that the patients were tested, while they were in the early stage of the dynamic phase of body mass loss, whereas the rats were tested when they were relatively weight stable. A subsequent human study found that the breakpoints for RYGB patients 28.4 months postoperatively on average did not differ from those measured in normal-weight controls for a chocolate reinforcer even though the somatostatin analogue, octreotide, an inhibitor of gut peptide release, was effective at raising the breakpoint for the patients (Goldstone et al. 2016). It could also be that within the first few months after surgery, some patients are quite compliant with the nutritional advice they receive and are thus reluctant to work for a reinforcer that they feel is unhealthy; the behavior of the rats is not subject to nutritional counseling. Microstructure of ingestion Another way to assess the motivational potency of a taste stimulus is to do so in the context of feeding and drinking. Rats will drink by initiating bursts of licks. The time between licks within bursts is relatively fixed and is called the interlick interval. The pauses between bursts, however, is quite variable as is the size of the bursts themselves. This burst-pause pattern of drinking is referred to the microstructure of intake, and when the fluid contains nutrients and calories, it can be considered eating. The microstructure of ingestion is a syntax of sorts for the way that various factors contribute to the control of intake such as the orosensory properties of the solution, the physiological state of the animal, and the attendant postoral events (Davis 1989; Davis and Smith 1992; Davis and Perez 1993; Davis 1996; Spector et al. 1998; Spector and St John 1998). Mathes et al. used this approach to assess the intake of various nutrient solutions in sham-operated (SHAM) and RYGB rats for 60-min single-bottle sessions (Mathes, Bohnenkamp, le Roux, et al. 2015). The results with 5% Intralipid were quite revealing. On the first day, the nondeprived RYGB and SHAM rats drank comparable amounts of the fat emulsion. Over the next several days, however, the RYGB rats decreased their intake and the SHAM rats increased such that the former was drinking roughly half as much as the latter. This progressive decrease in intake was reminiscent of the decrease in HFD preference described earlier, suggesting that experience is important. When the first-minute lick rate and the size of the first burst were analyzed, there was no difference between the 2 groups. Moreover, both measures increased across days in both groups. These early meal microstructural measures are thought to be indicative of the motivational potency of orosensory signals preceding any significant postoral accumulation of the stimulus. It would thus appear that the decrease in Intralipid intake by the RYGB group across days did not indicate a drop in the palatability of the stimulus. Cafeteria diet We wanted to assess food selection and preference in a context that more closely resembled the choices that humans confront daily. We thus searched for food items in the local supermarket that varied in their macronutrient content, would not spoil overnight, would not excessively spill, and would allow us to accurately measure intake. We settled on refried beans (low fat, low sugar), creamy peanut butter (high fat, low sugar), low-fat yogurt (low fat, high sugar), and a “sugar fat whip,” which we made from corn oil, shortening, powdered sugar and whey protein (high fat, high sugar). The animals were habituated to each item for several days alone with chow available and then were given an 8-day 5-item choice test (chow was included). The last 2 days served as the baseline. After that, roughly half the animals received RYGB and half received sham surgery. We then quantified the PO change in the relative percentage of calories taken from each macronutrient category as well as for sugar alone irrespective of the total calories ingested (which expectedly decreased after RYGB). Initially, both groups displayed no difference from their presurgical baseline. However, although the sham-operated rats maintained this profile of macronutrient ingestion, the RYGB progressively decreased the proportion of calories they ingested from fat over days and progressively increased the proportion of calories they ingested from carbohydrate accompanied by a slight but significant increase in the proportion of calories taken from protein. The increase in relative carbohydrate intake could not be explained by an increase in sugar intake because the latter stayed the same (or actually slightly decreased) and thus is attributable to an elevation in the ingestion of complex carbohydrates. Whether this occurs in humans or not remains somewhat unclear. Although there appears to be a widely held view in the medical community that humans decrease their relative consumption of fats and sugars after RYGB, a review of the literature by Mathes and Spector (2012) found that the reported changes in relative macronutrient intake after RYGB in humans are small and transient if they occur at all, but those studies were all based on verbal report that is vulnerable to inaccuracies (see Dr. Barbara Livingstone’s section). A recent Danish study found that at 6 months post-RYGB, patients did not change their relative intake of macronutrients during a test meal with choices that varied in their nutrient composition (Nielsen et al. 2017). Future plans As the results presented above attest, although RYGB has clear effects on the relative intake of and preference for sugar and fat by rats when they are given alternative options, there is no strong evidence that taste-motivated responses to these nutrients have been changed. We plan to continue to comprehensively test the possibility that the neural processing of orosensory signals, as assessed importantly by behavioral means, is altered by RYGB in a rat model (see Dr. Yanina Pepino’s section on human testing). In addition, we have developed a home-cage feeding monitor that can provide moment-by-moment recording of the ingestion from 5 food cups in a linear array as well as lick-by-lick records of 2 solutions over a 24-h period. We hope to exploit the temporal resolution of this device to provide insight into the evolution of altered macronutrient feeding patterns. Finally, we will continue to coordinate with and learn from our colleagues in the Republic of Ireland and in Northern Ireland, Dr. Carel le Roux, Dr. Barbara Livingstone, Dr. Ruth Price and their coworkers, who are conducting experiments that employ direct measures of food selection and intake in patients before and after RYGB and controls. Free-living versus laboratory assessment of food selection and intake in bariatric research (M. Barbara E. Livingstone and Ruth K. Price) Background It is now widely accepted that there are multiple mediators involved in weight loss following bariatric surgery that cannot be explained by purely restrictive and malabsorptive mechanisms. Although a decrease in energy intake (EI) is the main driver of weight loss, the literature in the area presents a complex and inconsistent picture of the consequences of bariatric surgery on macronutrient intake, food selection, taste sensitivity, and food reward/aversion processes, all of which have been implicated to a greater or lesser extent in the diminution in EI. There are a number of possible reasons for this lack of clarity, but from a methodological standpoint, there are 2 plausible explanations. In the first place, it is not always fully appreciated that food intake is likely to transition over the time period when body weight is decreasing, then stabilizing, and perhaps even rebounding following surgery. Unfortunately, there has been a paucity of follow-up studies with sufficiently robust methodology to account for these changes. Hence, the conclusions drawn from single time-point observations are unlikely to be insightful and may even be misleading regarding the dynamics of food intake following bariatric surgery. Second, most of the studies have placed overwhelming and unquestioning reliance on the validity self-reported food intake data (Mathes and Spector 2012). Free-living dietary assessment: a complex and challenging undertaking Various methods of measuring food intake at the individual level have been developed (Thompson et al. 2015; Cade et al. 2017), of which the most commonly used methods in bariatric research include food frequency questionnaires (FFQ); either single or repeated 24-h recalls; and food records or diaries that are administered for a variable number of days and are either weighed or nonweighed. Different methods for portion size estimation are used and include standardized or population averaged portion sizes (often used for FFQs), household measures, pictures, and food models. Other dietary assessment methods employed include the diet history and diet checklists. More recently, research has focused on harnessing new applications of information and communication technologies (ICT), especially mobile phone and internet applications as a viable solution to current methodological shortcomings (Ngo et al. 2009; Gemming et al. 2015; Boushey et al. 2017; Cade 2017). Certainly, ICT has the potential to reduce researcher and respondent burden, improve adherence and communication, automate and standardize coding, and upgrade data quality, consistency, and completeness. However, although the evidence base on the efficacy of ICT in dietary assessment is growing, it presents a very mixed picture. A popular misconception is that these new technologies in dietary assessment are also methodologically new (Illner et al. 2012). In fact, most of them are hostage to the same shortcomings as conventional methods of assessment and their adoption and integration into bariatric research is unlikely to bring resolution to the inherent individual bias related to self-reported data. Unfortunately, all techniques for dietary assessment in current use are fraught with inherent and extrinsic methodological problems making accurate measurements of food intake under free-living conditions extremely challenging. Critically, they all share the same fundamental weakness: they are entirely subjective and the validity of the data ultimately depends on the ability and/or motivation of respondents to faithfully report and recall what they have eaten. Misreporting in dietary assessment: a fact of life Up until the late 1980s, it was widely assumed that errors in dietary assessment were random, and in the absence of objective and independent markers of food intake, dietary data were tacitly assumed to provide valid measures of usual food intake. However, the advent of the doubly labeled water (DLW) method of measuring total energy expenditure (Schoeller 2002) as an independent marker of EI led to the universal recognition and acceptance that most EI data are fundamentally and systematically flawed by misreporting, particularly under-reporting (Trabulsi and Schoeller 2001; Westerterp and Goris 2002; Livingstone and Black 2003). DLW validation studies have revealed that although under-reporting is endemic in all dietary surveys and occurs in all ages, both sexes, and at all levels of energy expenditure, obesity and dieting have been identified as having the most robust associations with under-reporting of EI. Moreover, under-reporting is not specific to any one method of dietary assessment, whereas subject-specific bias, whether over time or to different assessment methods, has been observed (Black and Cole 2001; Subar et al. 2003). The source of bias in the reporting of food intake in obese individuals remains poorly understood but involves a complex interplay of cognitive and behavioral processes that operate in different ways in different individuals (Macdiarmid and Blundell 1997, 1998; Mela and Aaron 1997). Under-reporting may be the consequence of one or more of the following: a conscious failure to record/report food eaten to achieve a self-presentation goal of eating a “healthy” diet; a conscious failure to record because it is time consuming and inconvenient; a subconscious failure to record due to memory lapse across all or selected food items; accurate and honest recording of atypical intakes during the reporting period; and an alteration of habitual intake such as avoidance of snacks, to simplify reporting. Conscious and subconscious inhibitions may be particularly strong in people with obesity due to negative social attitudes toward overweight and consequent guilt about either the quantities or types of food that they are consuming. Thus, self-deception may play a significant role in under-reporting, rather than a conscious desire to deceive the researcher. The under-reporting of EI implies an under-reporting of dietary factors that may be food and/or macronutrient specific. However, the question of whether there is distortion in macronutrient reporting has not been fully answered and indeed difficult to prove given that macronutrients are highly interrelated when expressed as % energy. With the caveat that it is difficult to draw definitive conclusions from studies using different dietary assessment methods and criteria for defining under-reporters, the available evidence shows that under-reporters of EI tend to report a diet with a higher proportion of energy from protein, whereas fat intake tends to be under-reported, particularly by individuals with obesity. Total carbohydrate shows variable associations with under-reporting but, where the intakes of sugars have been separately identified, a consistently lower percentage of energy from sugars has been observed. Alcohol intakes are consistently under-reported (Goris et al. 2000; Heitmann et al. 2000; Livingstone and Black 2003). The consequence of this differential reporting of macronutrients is a complex pattern of partly inaccurate information where some foods are over-reported and others under-reported—but which ones and by how much are largely unknown. A logical conclusion is that foods with negative health connotations (e.g., cakes biscuits, confectionary, fried foods, alcohol) are more likely to be under-reported, whereas the intake of those with a positive health image (e.g., fruits and vegetables) are likely to be exaggerated. Direct measurement of food intake: a priority in bariatric research The conclusion is inescapable; despite best efforts to refine existing methodology, particularly exploiting the potential of innovative technologies for data capture, one of the most intractable problems facing nutrition research is our inability to accurately assess the dietary intake of free-living individuals (Subar et al. 2015). Whether this issue will ever be fully understood or resolved is debatable, but for now, all data on self-reported food intake in weight-loss studies are literally incredible. Given the vagaries and heterogeneity of free-living measurements of food intake, the priority in bariatric research must be to measure appetite and eating behavior under strictly controlled laboratory conditions. Certainly, although these cannot replicate the free-living situation, it can legitimately be argued that this is not their intention. Rather, laboratory studies permit the isolation and systematic testing of specific variables associated with appetite and eating behavior free from the constraints of external influences which are an inevitable part of a free-living scenario. Working in collaboration with Dr. Alan Spector (Florida State University) and Dr. Carel le Roux (University College, Dublin) and funded by the US-Ireland R&D Partnership Programme, Ulster University (Dr. Barbara Livingstone, Dr. Ruth Price) are now objectively exploring changes in meal patterns, food selection, and gut hormone responses in 32 RYGB patients and 32 time-matched normal-weight controls. The transition in food intake behavior during a very dynamic phase of weight change in bariatric patients is being captured by covert and direct tracking of food intake at 4 × 36 h time points: 1 month pre-surgery and 3, 12, and 24 months post-surgery. To ensure the highest degree of sensitivity and control over intervention and outcome variables, all measurements are being made under fully residential conditions. Thus, although the study design represents a compromise between the demands of external and internal validity, it may help to fill a critical void in our understanding of the dynamics of food selection and intake following bariatric surgery, which, hitherto, has suffered from over-reliance on, and uncritical acceptance of, the integrity of self-reported food intake data. Effects of bariatric surgery on ingestive behavior and sweet taste perception in subjects with obesity (M. Yanina Pepino) Bariatric surgery As mentioned in the introduction section, there are different types of bariatric surgical procedures. At present, the most popular procedures performed worldwide are RYGB, SG, and laparoscopic adjustable gastric banding (LAGB) (Angrisani et al. 2017). All 3 procedures decrease gastric volume and result in weight loss, but unlike LAGB, in which the anatomy of the intestine and stomach remains intact, RYGB and SG alter the anatomy of the digestive system. RYGB and SG surgery cause greater weight loss than does LAGB (Angrisani et al. 2017). The precise mechanism(s) responsible for this difference are incompletely understood, but it is now known that they go beyond restriction and malabsorption of nutrients. Data from several studies support the hypothesis that one potential mechanism contributing to RYGB and SG clinical effectiveness is surgically induced changes in flavor perception and brain reward, which affect ingesting behavior and help patients adopt healthier diets (Miras and le Roux 2010). Following RYGB and SG, the majority of patients report changes in appetite and “taste” Multiple studies that survey patients agree on the finding that the majority of patients report changes in their sense of taste and smell after weight-loss surgery (Tichansky et al. 2006; Graham et al. 2014; Makaronidis et al. 2016). However, few studies have evaluated changes in taste function in these patients using validated sensory techniques (Scruggs et al. 1994; Burge et al. 1995; Bueter et al. 2011; El Labban et al. 2016). Of note, the majority of these studies measured changes in taste thresholds. Threshold sensitivity refers to the lowest concentration of a tastant that can be detected as different from water (i.e., detection thresholds), or recognized as a quality (i.e., recognition threshold) at least 50% of the time (Bartoshuk 1978). Although it may seem reasonable to speculate that gustatory sensitivity derived from threshold data predicts gustatory sensitivity above threshold concentrations, this is rarely the case (Bartoshuk 1978; Keast and Roper 2007; Pepino et al. 2010). My laboratory has systematically examined whether these different weight-loss surgical procedures (i.e., RYGB, SG, LAGB) induce changes in taste sensitivity and in the pleasure/displeasure derived from tasting sweetness, at least in the short term (i.e., within the first year from surgery). We assessed threshold (i.e., detection) and suprathreshold (i.e., perception of taste intensity at concentrations of taste stimuli that represent the range of concentrations daily experienced in food) sensitivity to basic taste stimuli. In our study designs, we included the LAGB group as a weight-loss control group to separate changes in taste perception and ingestive behavior that are caused by anatomical alteration of the digestive system from those that could be caused by changes in the diet and weight loss itself. Accordingly, we evaluated the sensory-discriminative and hedonic components of taste perception, and eating behavior, in women with obesity before and after they lost ~20% of their body weight induced by either RYGB, SG or LAGB surgery (Pepino et al. 2014; Nance et al. 2017). We found that overall, sensitivity to different concentrations of sucrose, glucose (for sweetness), NaCl (for saltiness), and MSG (for “umaminess” or savoriness) remained remarkably unchanged after RYGB, SG, and LAGB surgery (Pepino et al. 2014; Nance et al. 2017). However, convergent with some, but not all (see Dr. Alan C. Spector’s section), findings from preclinical (Hajnal et al. 2010; Shin et al. 2011) and clinical studies (Miras and le Roux 2010; Ochner et al. 2011; Scholtz et al. 2014), we found that RYGB had weight-loss-independent effects in the hedonic dimension of sweet taste perception in people (Pepino et al. 2014). RYGB, but not LAGB, shifted sweetness palatability from pleasant to unpleasant when repetitively tasting sucrose. We also observed that patients who underwent SG, similar to patients who underwent RYGB, perceive less pleasantness when tasting sweetness after surgery compared with before surgery (Nance et al. 2017). However, the small sample size in our study with SG patients (8 women evaluated before and after surgery) warrants further investigation. At first, our results may seem at contrast with preclinical data presented by Dr. Spector’s section of this review. However, it is important to highlight that in our studies we evaluated all subjects within the first few months of their surgery. Whether the observed changes in the hedonic value of sweetness are transient and an epiphenomenon of surgery, or long lasting and directly related to the success of these surgeries is unknown and the focus of some of our current research. Bypassing sweets for alcohol and future studies In contrast to the beneficial effect of RYGB surgery on food preferences, a growing body of evidence indicates that RYGB surgery is associated with an increased risk to develop an alcohol use disorder (AUD) in patients who had no history of having an AUD before surgery (King et al. 2012, 2017; Ostlund et al. 2013). Interestingly, the idea of performing gastric bypass surgeries to treat obesity originated from the observation that patients with gastric resections (to treat peptic ulcers and gastric cancers) would lose weight and remain thin (Mason and Ito 1969). However, the observation that undergoing total or partial gastrectomy surgeries increased the risk of developing alcoholism, abundantly documented in the literature for more than half a century (Soeder 1957; Navratil 1959), was forgotten, and the association between RYGB and AUD has been acknowledged recently as a new phenomenon. Recent studies show a 2-fold increase in prevalence of AUD after RYGB compared with after LAGB (King et al. 2012, 2017; Ostlund et al. 2013). Perhaps due to its recency, less is known about the potential long-term side effects of SG—this weight-loss surgery procedure was not used until 2008, but it is markedly increasing in prevalence (Angrisani et al. 2017). Because both partial and total gastrectomy surgeries are associated with an increased risk of developing an AUD, SG may also increase the risk, but currently, there are no data available on whether SG has an impact on AUD. We are currently studying several potential mechanisms that could underlie the increased risk for AUD after gastric surgery. Because it is well known that the faster a drug of abuse is delivered to the brain, the higher is its addiction potential (de Wit et al. 1992), it is possible that RYGB-induced AUD is related to surgically induced changes in alcohol pharmacokinetics. Our data show that SG surgery, similar to RYGB surgery, causes faster and higher blood alcohol concentrations (BAC). When people drink alcohol after these surgeries, they experience a peak BAC within a few minutes of ingestion that is 2-fold higher than that reached after drinking the same amount before surgery (Pepino et al. 2015; Acevedo et al. 2018). Our data, combined with data from others (Klockhoff et al. 2002; Steffen et al. 2013), underscore the need to make patients aware of the alterations in alcohol metabolism that occur after these surgical procedures to help reduce the risk of potential serious consequences of moderate alcohol consumption. In our future studies, we plan to continue our research efforts on the effects of bariatric surgery-induced weight loss on ingestive behavior. We found this area of research important not only because of the direct impact of advancing knowledge for this clinical population, but also because we see these surgeries as powerful experimental tools to elucidate the intricate physiology of appetite and reward. Final remarks (Alan C. Spector) It should be clear from the paragraphs above that although there are very clear consequences of RYGB on body weight and overall caloric intake, its effects on food selection and taste remain to be fully understood. There are notable differences between the outcomes of experiments aiming to test the same phenomenon. Some of these disparities may be due to species differences (rodent vs. human), and some may be due to key methodological features of experiments. In fact, arguably, similar inconsistencies plague the obesity literature in toto. My colleagues and I have championed the application of more direct measures that can be applied to preclinical and clinical experimental inquiries with the hope that this may provide some clarity. Nevertheless, all of the speakers in this symposium agree that further work on the role of taste on food choice is essential to gain a comprehensive understanding of the causes and effects of obesity and the bases of the therapeutic properties of bariatric surgery. Funding A.C.S.: This work was supported in part by the National Institute of Diabetes and Digestive and Kidney Diseases of the National Institutes of Health under Award Number R01-DK106112. M.Y.P.: This work is being supported in part by the National Institute on Alcohol Abuse and Alcoholism under Award Number R01-AA024103 and USDA National Institute of Food and Agriculture Hatch Project number 698–921. 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TI - Proceedings from the 2018 Association for Chemoreception Annual Meeting Symposium: Bariatric Surgery and Its Effects on Taste and Food Selection
JF - Chemical Senses
DO - 10.1093/chemse/bjy076
DA - 2019-03-11
UR - https://www.deepdyve.com/lp/oxford-university-press/proceedings-from-the-2018-association-for-chemoreception-annual-zESRpesSxK
SP - 155
VL - 44
IS - 3
DP - DeepDyve
ER -