Taste-related reward is associated with weight loss following bariatric surgery

BACKGROUNDBariatric surgeries are the most effective treatments for successful and sustained weight loss, but individuals vary in treatment response. Understanding the neurobiological and behavioral mechanisms accounting for this variation could lead to the development of personalized therapeutic ap...

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Veröffentlicht in:The Journal of clinical investigation 2020-08, Vol.130 (8), p.4370-4381
Hauptverfasser: Smith, Kimberly R, Papantoni, Afroditi, Veldhuizen, Maria G, Kamath, Vidyulata, Harris, Civonnia, Moran, Timothy H, Carnell, Susan, Steele, Kimberley E
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container_end_page 4381
container_issue 8
container_start_page 4370
container_title The Journal of clinical investigation
container_volume 130
creator Smith, Kimberly R
Papantoni, Afroditi
Veldhuizen, Maria G
Kamath, Vidyulata
Harris, Civonnia
Moran, Timothy H
Carnell, Susan
Steele, Kimberley E
description BACKGROUNDBariatric surgeries are the most effective treatments for successful and sustained weight loss, but individuals vary in treatment response. Understanding the neurobiological and behavioral mechanisms accounting for this variation could lead to the development of personalized therapeutic approaches and improve treatment outcomes. The primary objectives of this study were to investigate changes in taste preferences and taste-induced brain responses after Roux-en-Y gastric bypass (RYGB) and vertical sleeve gastrectomy (VSG) and to identify potential taste-related predictors of weight loss.METHODSFemales, ages 18 to 55, with a body mass index greater than or equal to 35 kg/m2, and approved for bariatric surgery at the Johns Hopkins Center for Bariatric Surgery were recruited for participation. Demographics, anthropometrics, liking ratings, and neural responses to varying concentrations of sucrose plus fat mixtures were assessed before and after surgery via visual analog scales and functional MRI.RESULTSBariatric surgery produced decreases in liking for sucrose-sweetened mixtures. Greater preference for sucrose-sweetened mixtures before surgery was associated with greater weight loss in RYGB, but not VSG. In the RYGB group only, individuals who showed lower taste-induced activation in the ventral tegmental area (VTA) before surgery and greater changes in taste-induced VTA activation 2 weeks following surgery experienced increased weight loss.CONCLUSIONThe anatomical and/or metabolic changes associated with RYGB may more effectively "reset" the neural processing of reward stimuli, thereby rescuing the blunted activation in the mesolimbic pathway found in patients with obesity. Further, these findings suggest that RYGB may be particularly effective in patients with a preference for sweet foods.FUNDINGNIH K23DK100559 and Dalio Philanthropies.
doi_str_mv 10.1172/JCI137772
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Understanding the neurobiological and behavioral mechanisms accounting for this variation could lead to the development of personalized therapeutic approaches and improve treatment outcomes. The primary objectives of this study were to investigate changes in taste preferences and taste-induced brain responses after Roux-en-Y gastric bypass (RYGB) and vertical sleeve gastrectomy (VSG) and to identify potential taste-related predictors of weight loss.METHODSFemales, ages 18 to 55, with a body mass index greater than or equal to 35 kg/m2, and approved for bariatric surgery at the Johns Hopkins Center for Bariatric Surgery were recruited for participation. Demographics, anthropometrics, liking ratings, and neural responses to varying concentrations of sucrose plus fat mixtures were assessed before and after surgery via visual analog scales and functional MRI.RESULTSBariatric surgery produced decreases in liking for sucrose-sweetened mixtures. Greater preference for sucrose-sweetened mixtures before surgery was associated with greater weight loss in RYGB, but not VSG. In the RYGB group only, individuals who showed lower taste-induced activation in the ventral tegmental area (VTA) before surgery and greater changes in taste-induced VTA activation 2 weeks following surgery experienced increased weight loss.CONCLUSIONThe anatomical and/or metabolic changes associated with RYGB may more effectively "reset" the neural processing of reward stimuli, thereby rescuing the blunted activation in the mesolimbic pathway found in patients with obesity. Further, these findings suggest that RYGB may be particularly effective in patients with a preference for sweet foods.FUNDINGNIH K23DK100559 and Dalio Philanthropies.</description><identifier>ISSN: 0021-9738</identifier><identifier>EISSN: 1558-8238</identifier><identifier>DOI: 10.1172/JCI137772</identifier><identifier>PMID: 32427584</identifier><language>eng</language><publisher>United States: American Society for Clinical Investigation</publisher><subject>Adolescent ; Adult ; Bariatric surgery ; Biomedical research ; Body mass index ; Body weight loss ; Care and treatment ; Clinical Medicine ; Demographics ; Demography ; Dopamine ; Female ; Food ; Food preferences ; Functional magnetic resonance imaging ; Gastrectomy ; Gastric Bypass ; Gastroesophageal reflux ; Gastrointestinal surgery ; Health aspects ; Humans ; Information processing ; Mesolimbic system ; Middle Aged ; Obesity ; Obesity - physiopathology ; Obesity - surgery ; Patients ; Preferences ; Ratings &amp; rankings ; Reinforcement ; Sucrose ; Surgery ; Sweet taste ; Taste ; Taste preferences ; Ventral tegmentum ; Weight control ; Weight Loss ; Weight loss maintenance</subject><ispartof>The Journal of clinical investigation, 2020-08, Vol.130 (8), p.4370-4381</ispartof><rights>COPYRIGHT 2020 American Society for Clinical Investigation</rights><rights>Copyright American Society for Clinical Investigation Aug 2020</rights><rights>2020 American Society for Clinical Investigation 2020 American Society for Clinical Investigation</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c607t-715e6420028b2243c1a13275ad44249b6f2e949ef2aeb5eaa13d21a92b32093f3</citedby><cites>FETCH-LOGICAL-c607t-715e6420028b2243c1a13275ad44249b6f2e949ef2aeb5eaa13d21a92b32093f3</cites><orcidid>0000-0001-5096-6549 ; 0000-0001-8375-7719 ; 0000-0001-6539-095X ; 0000-0001-7711-3597</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7410047/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7410047/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32427584$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Smith, Kimberly R</creatorcontrib><creatorcontrib>Papantoni, Afroditi</creatorcontrib><creatorcontrib>Veldhuizen, Maria G</creatorcontrib><creatorcontrib>Kamath, Vidyulata</creatorcontrib><creatorcontrib>Harris, Civonnia</creatorcontrib><creatorcontrib>Moran, Timothy H</creatorcontrib><creatorcontrib>Carnell, Susan</creatorcontrib><creatorcontrib>Steele, Kimberley E</creatorcontrib><title>Taste-related reward is associated with weight loss following bariatric surgery</title><title>The Journal of clinical investigation</title><addtitle>J Clin Invest</addtitle><description>BACKGROUNDBariatric surgeries are the most effective treatments for successful and sustained weight loss, but individuals vary in treatment response. Understanding the neurobiological and behavioral mechanisms accounting for this variation could lead to the development of personalized therapeutic approaches and improve treatment outcomes. The primary objectives of this study were to investigate changes in taste preferences and taste-induced brain responses after Roux-en-Y gastric bypass (RYGB) and vertical sleeve gastrectomy (VSG) and to identify potential taste-related predictors of weight loss.METHODSFemales, ages 18 to 55, with a body mass index greater than or equal to 35 kg/m2, and approved for bariatric surgery at the Johns Hopkins Center for Bariatric Surgery were recruited for participation. Demographics, anthropometrics, liking ratings, and neural responses to varying concentrations of sucrose plus fat mixtures were assessed before and after surgery via visual analog scales and functional MRI.RESULTSBariatric surgery produced decreases in liking for sucrose-sweetened mixtures. Greater preference for sucrose-sweetened mixtures before surgery was associated with greater weight loss in RYGB, but not VSG. In the RYGB group only, individuals who showed lower taste-induced activation in the ventral tegmental area (VTA) before surgery and greater changes in taste-induced VTA activation 2 weeks following surgery experienced increased weight loss.CONCLUSIONThe anatomical and/or metabolic changes associated with RYGB may more effectively "reset" the neural processing of reward stimuli, thereby rescuing the blunted activation in the mesolimbic pathway found in patients with obesity. Further, these findings suggest that RYGB may be particularly effective in patients with a preference for sweet foods.FUNDINGNIH K23DK100559 and Dalio Philanthropies.</description><subject>Adolescent</subject><subject>Adult</subject><subject>Bariatric surgery</subject><subject>Biomedical research</subject><subject>Body mass index</subject><subject>Body weight loss</subject><subject>Care and treatment</subject><subject>Clinical Medicine</subject><subject>Demographics</subject><subject>Demography</subject><subject>Dopamine</subject><subject>Female</subject><subject>Food</subject><subject>Food preferences</subject><subject>Functional magnetic resonance imaging</subject><subject>Gastrectomy</subject><subject>Gastric Bypass</subject><subject>Gastroesophageal reflux</subject><subject>Gastrointestinal surgery</subject><subject>Health aspects</subject><subject>Humans</subject><subject>Information processing</subject><subject>Mesolimbic system</subject><subject>Middle Aged</subject><subject>Obesity</subject><subject>Obesity - physiopathology</subject><subject>Obesity - surgery</subject><subject>Patients</subject><subject>Preferences</subject><subject>Ratings &amp; rankings</subject><subject>Reinforcement</subject><subject>Sucrose</subject><subject>Surgery</subject><subject>Sweet taste</subject><subject>Taste</subject><subject>Taste preferences</subject><subject>Ventral tegmentum</subject><subject>Weight control</subject><subject>Weight Loss</subject><subject>Weight loss maintenance</subject><issn>0021-9738</issn><issn>1558-8238</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BEC</sourceid><sourceid>BENPR</sourceid><recordid>eNqNkl1rFDEUhoNY7Fq98A_IgCB6MTVfs5m5Ecrix5bCglZvQyZzZiYlm9Qk49p_b_rhtlv2QnIROOc5b95wXoReEXxMiKAfThdLwoQQ9Amakaqqy5qy-imaYUxJ2QhWH6LnMV5gTDiv-DN0yCinoqr5DK3OVUxQBrAqQVcE2KjQFSYWKkavzU1xY9JYbMAMYyqsj7HovbV-Y9xQtCpkJhhdxCkMEK5eoINe2Qgv7-4j9OPzp_PF1_Js9WW5ODkr9RyLVApSwZzTbLBuKeVME0VYtqQ6zilv2nlPoeEN9FRBW4HK3Y4S1dCWUdywnh2hj7e6l1O7hk6DS0FZeRnMWoUr6ZWRux1nRjn431JwgjEXWeDdnUDwvyaISa5N1GCtcuCnKCnHFcOC8Sajbx6hF34KLn8vU4zUrMKY3VODsiCN631-V1-LypM5Y4IIjkmmyj3UAA6ySe-gN7m8wx_v4fPpYG303oH3OwOZSfAnDWqKUS6_f_t_dvVzl337gB1B2TRGb6dkvIt7RXXIWQnQb5dCsLyOq9zGNbOvH25xS_7LJ_sLrk_f7Q</recordid><startdate>20200801</startdate><enddate>20200801</enddate><creator>Smith, Kimberly R</creator><creator>Papantoni, Afroditi</creator><creator>Veldhuizen, Maria G</creator><creator>Kamath, Vidyulata</creator><creator>Harris, Civonnia</creator><creator>Moran, Timothy H</creator><creator>Carnell, Susan</creator><creator>Steele, Kimberley E</creator><general>American Society for Clinical Investigation</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7RV</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BEC</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB0</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>NAPCQ</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>S0X</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-5096-6549</orcidid><orcidid>https://orcid.org/0000-0001-8375-7719</orcidid><orcidid>https://orcid.org/0000-0001-6539-095X</orcidid><orcidid>https://orcid.org/0000-0001-7711-3597</orcidid></search><sort><creationdate>20200801</creationdate><title>Taste-related reward is associated with weight loss following bariatric surgery</title><author>Smith, Kimberly R ; 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rankings</topic><topic>Reinforcement</topic><topic>Sucrose</topic><topic>Surgery</topic><topic>Sweet taste</topic><topic>Taste</topic><topic>Taste preferences</topic><topic>Ventral tegmentum</topic><topic>Weight control</topic><topic>Weight Loss</topic><topic>Weight loss maintenance</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Smith, Kimberly R</creatorcontrib><creatorcontrib>Papantoni, Afroditi</creatorcontrib><creatorcontrib>Veldhuizen, Maria G</creatorcontrib><creatorcontrib>Kamath, Vidyulata</creatorcontrib><creatorcontrib>Harris, Civonnia</creatorcontrib><creatorcontrib>Moran, Timothy H</creatorcontrib><creatorcontrib>Carnell, Susan</creatorcontrib><creatorcontrib>Steele, Kimberley E</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Nursing &amp; 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Understanding the neurobiological and behavioral mechanisms accounting for this variation could lead to the development of personalized therapeutic approaches and improve treatment outcomes. The primary objectives of this study were to investigate changes in taste preferences and taste-induced brain responses after Roux-en-Y gastric bypass (RYGB) and vertical sleeve gastrectomy (VSG) and to identify potential taste-related predictors of weight loss.METHODSFemales, ages 18 to 55, with a body mass index greater than or equal to 35 kg/m2, and approved for bariatric surgery at the Johns Hopkins Center for Bariatric Surgery were recruited for participation. Demographics, anthropometrics, liking ratings, and neural responses to varying concentrations of sucrose plus fat mixtures were assessed before and after surgery via visual analog scales and functional MRI.RESULTSBariatric surgery produced decreases in liking for sucrose-sweetened mixtures. Greater preference for sucrose-sweetened mixtures before surgery was associated with greater weight loss in RYGB, but not VSG. In the RYGB group only, individuals who showed lower taste-induced activation in the ventral tegmental area (VTA) before surgery and greater changes in taste-induced VTA activation 2 weeks following surgery experienced increased weight loss.CONCLUSIONThe anatomical and/or metabolic changes associated with RYGB may more effectively "reset" the neural processing of reward stimuli, thereby rescuing the blunted activation in the mesolimbic pathway found in patients with obesity. Further, these findings suggest that RYGB may be particularly effective in patients with a preference for sweet foods.FUNDINGNIH K23DK100559 and Dalio Philanthropies.</abstract><cop>United States</cop><pub>American Society for Clinical Investigation</pub><pmid>32427584</pmid><doi>10.1172/JCI137772</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0001-5096-6549</orcidid><orcidid>https://orcid.org/0000-0001-8375-7719</orcidid><orcidid>https://orcid.org/0000-0001-6539-095X</orcidid><orcidid>https://orcid.org/0000-0001-7711-3597</orcidid><oa>free_for_read</oa></addata></record>
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subjects Adolescent
Adult
Bariatric surgery
Biomedical research
Body mass index
Body weight loss
Care and treatment
Clinical Medicine
Demographics
Demography
Dopamine
Female
Food
Food preferences
Functional magnetic resonance imaging
Gastrectomy
Gastric Bypass
Gastroesophageal reflux
Gastrointestinal surgery
Health aspects
Humans
Information processing
Mesolimbic system
Middle Aged
Obesity
Obesity - physiopathology
Obesity - surgery
Patients
Preferences
Ratings & rankings
Reinforcement
Sucrose
Surgery
Sweet taste
Taste
Taste preferences
Ventral tegmentum
Weight control
Weight Loss
Weight loss maintenance
title Taste-related reward is associated with weight loss following bariatric surgery
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