{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,18]],"date-time":"2026-03-18T16:13:14Z","timestamp":1773850394356,"version":"3.50.1"},"reference-count":35,"publisher":"Oxford University Press (OUP)","license":[{"start":{"date-parts":[[2023,2,17]],"date-time":"2023-02-17T00:00:00Z","timestamp":1676592000000},"content-version":"vor","delay-in-days":47,"URL":"https:\/\/academic.oup.com\/pages\/standard-publication-reuse-rights"}],"funder":[{"DOI":"10.13039\/100000199","name":"United States Department of Agriculture","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000199","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009633","name":"NICHD","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100009633","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100005825","name":"National Institute of Food and Agriculture","doi-asserted-by":"publisher","award":["698-991"],"award-info":[{"award-number":["698-991"]}],"id":[{"id":"10.13039\/100005825","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100005825","name":"National Institute of Food and Agriculture","doi-asserted-by":"publisher","award":["HD070855"],"award-info":[{"award-number":["HD070855"]}],"id":[{"id":"10.13039\/100005825","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2023,1,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Wolfram syndrome is a rare disease characterized by diabetes, neurodegeneration, loss of vision, and audition. We recently found, in a young sample of participants (mean age 15 years), that Wolfram syndrome was associated with impairment in smell identification with normal smell sensitivity and whole-mouth taste function. However, these senses were assessed separately, and it is unknown whether smell\u2013taste interactions are altered in Wolfram syndrome, which was the focus of this study. Participants with Wolfram syndrome (n = 36; 18.2 \u00b1 6.8 years) and sex\u2013age-equivalent healthy controls (n = 34) were assessed with a battery of sensory tests. Using sip-and-spit methods, participants tasted solutions containing gustatory and olfactory stimuli (sucrose with strawberry extract, citric acid with lemon extract, sodium chloride in vegetable broth, and coffee) with and without nose clips, and rated perceived taste and retronasal smell intensities using the generalized Labeled Magnitude Scale. Participants also completed n-butanol detection thresholds and the University of Pennsylvania Smell Identification Test (UPSIT). Retronasal smell increased taste intensity of sucrose, sodium chloride, and coffee solutions similarly in both groups (P values &amp;lt;0.03). Compared with the control group, participants in the Wolfram group had lower UPSIT scores and reduced smell sensitivity, retronasal intensity, and saltiness (P values &amp;lt;0.03), but rated other taste intensities similarly when wearing the nose clip. Despite impairments in orthonasal smell identification, odor-induced taste enhancement was preserved in participants with Wolfram syndrome who still had some peripheral olfactory function. This finding suggests that odor-induced taste enhancement may be preserved in the presence of reduced olfactory intensity.<\/jats:p>","DOI":"10.1093\/chemse\/bjad004","type":"journal-article","created":{"date-parts":[[2023,2,17]],"date-time":"2023-02-17T06:08:50Z","timestamp":1676614130000},"source":"Crossref","is-referenced-by-count":6,"title":["Enhancement of taste by retronasal odors in patients with Wolfram syndrome and decreased olfactory function"],"prefix":"10.1093","volume":"48","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6719-8045","authenticated-orcid":false,"given":"Raul","family":"Alfaro","sequence":"first","affiliation":[{"name":"Department of Food Science and Human Nutrition, University of Illinois at Urbana-Champaign , Urbana, IL , United States"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5340-9016","authenticated-orcid":false,"given":"Jessica G","family":"Nicanor-Carre\u00f3n","sequence":"additional","affiliation":[{"name":"Division of Nutritional Sciences, University of Illinois at Urbana-Champaign , Urbana, IL , United States"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7621-2072","authenticated-orcid":false,"given":"Tasha","family":"Doty","sequence":"additional","affiliation":[{"name":"Department of Psychiatry, School of Medicine, Washington University , St. Louis, MO , United States"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7917-5545","authenticated-orcid":false,"given":"Heather","family":"Lugar","sequence":"additional","affiliation":[{"name":"Department of Psychiatry, School of Medicine, Washington University , St. Louis, MO , United States"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7549-0698","authenticated-orcid":false,"given":"Tamara","family":"Hershey","sequence":"additional","affiliation":[{"name":"Department of Psychiatry, School of Medicine, Washington University , St. Louis, MO , United States"},{"name":"Department of Radiology, School of Medicine, Washington University , St. Louis, MO , United States"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2381-1095","authenticated-orcid":false,"given":"Marta Yanina","family":"Pepino","sequence":"additional","affiliation":[{"name":"Department of Food Science and Human Nutrition, University of Illinois at Urbana-Champaign , Urbana, IL , United States"},{"name":"Division of Nutritional Sciences, University of Illinois at Urbana-Champaign , Urbana, IL , United States"},{"name":"Department of Biomedical and Translational Sciences, Carle Illinois College of Medicine, University of Illinois at Urbana-Champaign , Urbana, IL , United States"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2023,2,17]]},"reference":[{"key":"2024021710502510500_CIT0001","doi-asserted-by":"crossref","first-page":"100535","DOI":"10.1016\/j.ijgfs.2022.100535","article-title":"Neurocognitive mechanisms of odor-induced taste enhancement: a systematic review","volume":"28","author":"Ai","year":"2022","journal-title":"Int J Gastron Food Sci"},{"key":"2024021710502510500_CIT0002","doi-asserted-by":"crossref","first-page":"bjab026","DOI":"10.1093\/chemse\/bjab026","article-title":"Taste and smell function in head and neck cancer survivors","volume":"46","author":"Alfaro","year":"2021","journal-title":"Chem Senses"},{"issue":"1","key":"2024021710502510500_CIT0003","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1186\/s13023-020-1335-7","article-title":"Taste and smell function in Wolfram syndrome","volume":"15","author":"Alfaro","year":"2020","journal-title":"Orphanet J Rare Dis"},{"issue":"4","key":"2024021710502510500_CIT0004","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1086\/520961","article-title":"A homozygous mutation in a novel zinc-finger protein, ERIS, is responsible for Wolfram syndrome 2","volume":"81","author":"Amr","year":"2007","journal-title":"Am J Hum Genet"},{"issue":"10","key":"2024021710502510500_CIT0005","doi-asserted-by":"crossref","first-page":"838","DOI":"10.1136\/jmg.34.10.838","article-title":"Wolfram (DIDMOAD) syndrome","volume":"34","author":"Barrett","year":"1997","journal-title":"J Med Genet"},{"issue":"Pt 6","key":"2024021710502510500_CIT0006","doi-asserted-by":"crossref","first-page":"882","DOI":"10.1038\/eye.1997.226","article-title":"Optic atrophy in Wolfram (DIDMOAD) syndrome","volume":"11","author":"Barrett","year":"1997","journal-title":"Eye (Lond)"},{"issue":"1","key":"2024021710502510500_CIT0007","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1016\/j.physbeh.2004.02.033","article-title":"Valid across-group comparisons with labeled scales: the gLMS versus magnitude matching","volume":"82","author":"Bartoshuk","year":"2004","journal-title":"Physiol Behav"},{"issue":"9","key":"2024021710502510500_CIT0008","doi-asserted-by":"crossref","first-page":"1003","DOI":"10.1037\/amp0000577","article-title":"What Aristotle didn\u2019t know about flavor","volume":"74","author":"Bartoshuk","year":"2019","journal-title":"Am Psychol"},{"key":"2024021710502510500_CIT0009","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1186\/s13023-015-0282-1","article-title":"Selective cognitive and psychiatric manifestations in Wolfram Syndrome","volume":"10","author":"Bischoff","year":"2015","journal-title":"Orphanet J Rare Dis"},{"issue":"5","key":"2024021710502510500_CIT0010","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1089\/chi.2017.0023","article-title":"Personal variation in preference for sweetness: effects of age and obesity","volume":"13","author":"Bobowski","year":"2017","journal-title":"Child Obes"},{"key":"2024021710502510500_CIT0011","doi-asserted-by":"crossref","first-page":"S20","DOI":"10.1212\/WNL.0b013e3182872e38","article-title":"Gustation assessment using the NIH Toolbox","volume":"80","author":"Coldwell","year":"2013","journal-title":"Neurology"},{"key":"2024021710502510500_CIT0012","volume-title":"The Smell Identification Test\u2122 Administration Manual","author":"Doty","year":"2013","edition":"3"},{"issue":"3","key":"2024021710502510500_CIT0013","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1016\/0031-9384(84)90269-5","article-title":"Development of the University of Pennsylvania Smell Identification Test: a standardized microencapsulated test of olfactory function","volume":"32","author":"Doty","year":"1984","journal-title":"Physiol Behav"},{"issue":"1","key":"2024021710502510500_CIT0014","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s12078-013-9140-5","article-title":"Effects of stimulus intensity on odor enhancement by taste","volume":"6","author":"Fujimaru","year":"2013","journal-title":"Chemosens Percept"},{"issue":"23","key":"2024021710502510500_CIT0015","doi-asserted-by":"crossref","DOI":"10.3390\/jcm10235637","article-title":"Olfactory dysfunction: a complication of diabetes or a factor that complicates glucose metabolism? A narrative review","volume":"10","author":"Gouveri","year":"2021","journal-title":"J Clin Med"},{"issue":"3","key":"2024021710502510500_CIT0016","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1093\/chemse\/21.3.323","article-title":"Evaluating the \u2018Labeled Magnitude Scale\u2019 for measuring sensations of taste and smell","volume":"21","author":"Green","year":"1996","journal-title":"Chem Senses"},{"issue":"1","key":"2024021710502510500_CIT0017","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1093\/chemse\/bjr068","article-title":"Enhancement of retronasal odors by taste","volume":"37","author":"Green","year":"2012","journal-title":"Chem Senses"},{"issue":"3","key":"2024021710502510500_CIT0018","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1007\/s00405-006-0173-0","article-title":"Normative data for the \u201cSniffin\u2019 Sticks\u201d including tests of odor identification, odor discrimination, and olfactory thresholds: an upgrade based on a group of more than 3,000 subjects","volume":"264","author":"Hummel","year":"2007","journal-title":"Eur Arch Otorhinolaryngol"},{"issue":"1","key":"2024021710502510500_CIT0019","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1093\/chemse\/22.1.39","article-title":"\u2018Sniffin\u2019 sticks\u2019: olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold","volume":"22","author":"Hummel","year":"1997","journal-title":"Chem Senses"},{"issue":"2","key":"2024021710502510500_CIT0020","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1038\/2441","article-title":"A gene encoding a transmembrane protein is mutated in patients with diabetes mellitus and optic atrophy (Wolfram syndrome)","volume":"20","author":"Inoue","year":"1998","journal-title":"Nat Genet"},{"issue":"1","key":"2024021710502510500_CIT0021","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1186\/s13023-018-0852-0","article-title":"Longitudinal hearing loss in Wolfram syndrome","volume":"13","author":"Karzon","year":"2018","journal-title":"Orphanet J Rare Dis"},{"issue":"7","key":"2024021710502510500_CIT0022","doi-asserted-by":"crossref","first-page":"1629","DOI":"10.1002\/lary.28258","article-title":"Retronasal olfactory function in patients with smell loss but subjectively normal flavor perception","volume":"130","author":"Liu","year":"2020","journal-title":"Laryngoscope"},{"issue":"1","key":"2024021710502510500_CIT0023","doi-asserted-by":"crossref","first-page":"6010","DOI":"10.1038\/s41598-019-42447-9","article-title":"Evidence for altered neurodevelopment and neurodegeneration in Wolfram syndrome using longitudinal morphometry","volume":"9","author":"Lugar","year":"2019","journal-title":"Sci Rep"},{"key":"2024021710502510500_CIT0024","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1186\/1750-1172-8-64","article-title":"Phenotypic characteristics of early Wolfram syndrome","volume":"8","author":"Marshall","year":"2013","journal-title":"Orphanet J Rare Dis"},{"issue":"11","key":"2024021710502510500_CIT0025","doi-asserted-by":"crossref","first-page":"496","DOI":"10.3758\/BF03210253","article-title":"Variability in gustatory quality identification","volume":"2","author":"Meiselman","year":"1967","journal-title":"Percept Psychophys"},{"issue":"7","key":"2024021710502510500_CIT0026","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1016\/j.foodqual.2011.05.001","article-title":"Cross-modal interactions between taste and smell: odour-induced saltiness enhancement depends on salt level","volume":"22","author":"Nasri","year":"2011","journal-title":"Food Qual Prefer"},{"issue":"6","key":"2024021710502510500_CIT0027","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1093\/chemse\/bjz027","article-title":"Quality of life in patients with olfactory loss is better predicted by flavor identification than by orthonasal olfactory function","volume":"44","author":"Oleszkiewicz","year":"2019","journal-title":"Chem Senses"},{"issue":"7","key":"2024021710502510500_CIT0028","doi-asserted-by":"crossref","first-page":"1918","DOI":"10.3390\/nu12071918","article-title":"Relationship between sucrose taste detection thresholds and preferences in children, adolescents, and adults","volume":"12","author":"Petty","year":"2020","journal-title":"Nutrients"},{"issue":"9","key":"2024021710502510500_CIT0029","doi-asserted-by":"crossref","first-page":"1599","DOI":"10.1093\/hmg\/ddx060","article-title":"A novel CISD2 mutation associated with a classical Wolfram syndrome phenotype alters Ca2+ homeostasis and ER-mitochondria interactions","volume":"26","author":"Rouzier","year":"2017","journal-title":"Hum Mol Genet"},{"issue":"(3\u20134","key":"2024021710502510500_CIT0030","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1007\/s00221-005-2376-9","article-title":"Odor\/taste integration and the perception of flavor","volume":"166","author":"Small","year":"2005","journal-title":"Exp Brain Res"},{"key":"2024021710502510500_CIT0031","doi-asserted-by":"crossref","first-page":"104393","DOI":"10.1016\/j.foodqual.2021.104393","article-title":"Factors affecting odour-induced taste enhancement","volume":"96","author":"Spence","year":"2022","journal-title":"Food Qual Prefer"},{"issue":"6","key":"2024021710502510500_CIT0032","doi-asserted-by":"crossref","first-page":"627","DOI":"10.1093\/chemse\/24.6.627","article-title":"Confusing tastes and smells: how odours can influence the perception of sweet and sour tastes","volume":"24","author":"Stevenson","year":"1999","journal-title":"Chem Senses"},{"issue":"1","key":"2024021710502510500_CIT0033","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1093\/chemse\/bjx063","article-title":"Interactions of lemon, sucrose and citric acid in enhancing citrus, sweet and sour flavors","volume":"43","author":"Veldhuizen","year":"2017","journal-title":"Chem Senses"},{"issue":"2","key":"2024021710502510500_CIT0034","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1002\/lary.26229","article-title":"Patterns of olfactory impairment reflect underlying disease etiology","volume":"127","author":"Whitcroft","year":"2017","journal-title":"Laryngoscope"},{"issue":"10","key":"2024021710502510500_CIT0035","doi-asserted-by":"crossref","first-page":"3847","DOI":"10.1007\/s00405-021-06687-8","article-title":"Validation study of a novel approach for assessment of retronasal olfactory function with combination of odor thresholds and identification","volume":"278","author":"Yoshino","year":"2021","journal-title":"Eur Arch Otorhinolaryngol"}],"container-title":["Chemical Senses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/chemse\/advance-article-pdf\/doi\/10.1093\/chemse\/bjad004\/49233892\/bjad004.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/chemse\/article-pdf\/doi\/10.1093\/chemse\/bjad004\/49449673\/bjad004.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/chemse\/article-pdf\/doi\/10.1093\/chemse\/bjad004\/49449673\/bjad004.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,2,17]],"date-time":"2024-02-17T10:50:55Z","timestamp":1708167055000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/chemse\/article\/doi\/10.1093\/chemse\/bjad004\/7043567"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,1,1]]},"references-count":35,"URL":"https:\/\/doi.org\/10.1093\/chemse\/bjad004","relation":{},"ISSN":["0379-864X","1464-3553"],"issn-type":[{"value":"0379-864X","type":"print"},{"value":"1464-3553","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2023,1,1]]},"published":{"date-parts":[[2023,1,1]]},"article-number":"bjad004"}}