Abstract
(1) The objective of this study is to analyze differences in smell–taste capacity between females in extreme weight/eating conditions (EWC) and (2) to explore the interaction between smell/taste capacity, gastric hormones, eating behavior and body mass index (BMI). The sample comprised 239 females in EWC [64 Anorexia nervosa (AN) and 80 age-matched healthy-weight controls, and 59 obese and 36 age-matched healthy-weight controls]. Smell and taste assessments were performed through “Sniffin’ Sticks” and “Taste Strips,” respectively. The assessment measures included the eating disorders inventory-2, the symptom check list 90-revised, and The Dutch Eating Behavior Questionnaire, as well as peptides from the gastrointestinal tract [Ghrelin, peptide YY, cholecystokinin]. Smell capacity was differentially associated across EWC groups. Smell was clearly impaired in obese participants and increased in AN (hyposmia in Obesity was 54.3 and 6.4 % in AN), but taste capacity did not vary across EWC. Ghrelin levels were significantly decreased in obese subjects and were related to smell impairment. EWC individuals showed a distinct smell profile and circulating ghrelin levels compared to controls. Smell capacity and ghrelin may act as moderators of emotional eating and BMI.
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A.B. Fagundo, R. de la Torre, S. Jiménez-Murcia, Z. Agüera, R. Granero, S. Tárrega, C. Botella, R. Baños, J.M. Fernández-Real, R. Rodríguez, L. Forcano, G. Frühbeck, J. Gómez-Ambrosi, F.J. Tinahones, J.C. Fernández-García, F.F. Casanueva, F. Fernández-Aranda, Executive functions profile in extreme eating/weight conditions: from anorexia nervosa to obesity. PLoS ONE 7, e43382 (2012)
L. Claes, F. Fernández-Aranda, S. Jimenez-Murcia, C. Botella, F.F. Casanueva, R. de la Torre, J.M. Fernández-Real, G. Frühbeck, F.J. Tinahones, N. Vilarrasa, M. Montserrat-Gil de Bernabé, R. Granero, Z. Agüera, C. Sancho, J. Muehlenkamp, J.M. Menchón, Co-occurrence of non-suicidal self-injury and impulsivity in extreme weight conditions. Personal. Individ. Differ. 54, 137–140 (2013)
C. Villarejo, S. Jiménez-Murcia, E. Álvarez-Moya, R. Granero, E. Penelo, J. Treasure, N. Vilarrasa, M. Gil-Montserrat De Bernabé, F.F. Casanueva, F.J. Tinahones, J.M. Fernández-Real, G. Frühbeck, R. De La Torre, C. Botella, Z. Agüera, J.M. Menchõn, F. Fernández-Aranda, Loss of control over eating: a description of the eating disorder/obesity spectrum in women. Eur. Eat. Disord. Rev. 22, 25–31 (2014)
C. Villarejo, F. Fernández-Aranda, S. Jiménez-Murcia, E. Peñas-Lledó, R. Granero, E. Penelo, F.J. Tinahones, C. Sancho, N. Vilarrasa, M. Montserrat-Gil de Bernabé, F.F. Casanueva, J.M. Fernández-Real, G. Frühbeck, R. De laTorre, J. Treasure, C. Botella, J.M. Menchón, F. Fernandez-Aranda, S. Jimenez-Murcia, E. Penas-Lledo, M. Montserrat-Gil de Bernabe, J.M. Fernandez-Real, G. Fruhbeck, J.M. Menchon, Lifetime obesity in patients with eating disorders: increasing prevalence, clinical and personality correlates. Eur. Eat. Disord. Rev 20, 250–254 (2012)
S. Jacquemont, A. Reymond, F. Zufferey, L. Harewood, R.G. Walters, Z. Kutalik, D. Martinet, Y. Shen, A. Valsesia, N.D. Beckmann, G. Thorleifsson, M. Belfiore, S. Bouquillon, D. Campion, N. de Leeuw, B.B. de Vries, T. Esko, B.A. Fernandez, F. Fernández-Aranda, J.M. Fernández-Real, M. Gratacòs, A. Guilmatre, J. Hoyer, M.R. Jarvelin, R.F. Kooy, A. Kurg, C. Le Caignec, K. Männik, O.S. Platt, D. Sanlaville, M.M. Van Haelst, S. Villatoro Gomez, F. Walha, B.L. Wu, Y. Yu, A. Aboura, M.C. Addor, Y. Alembik, S.E. Antonarakis, B. Arveiler, M. Barth, N. Bednarek, F. Béna, S. Bergmann, M. Beri, L. Bernardini, B. Blaumeiser, D. Bonneau, A. Bottani, O. Boute, H.G. Brunner, D. Cailley, P. Callier, J. Chiesa, J. Chrast, L. Coin, C. Coutton, J.M. Cuisset, J.C. Cuvellier, A. David, B. de Freminville, B. Delobel, M.A. Delrue, B. Demeer, D. Descamps, G. Didelot, K. Dieterich, V. Disciglio, M. Doco-Fenzy, S. Drunat, B. Duban-Bedu, C. Dubourg, J.S. El-Sayed Moustafa, P. Elliott, B.H. Faas, L. Faivre, A. Faudet, F. Fellmann, A. Ferrarini, R. Fisher, E. Flori, L. Forer, D. Gaillard, M. Gerard, C. Gieger, S. Gimelli, G. Gimelli, H.J. Grabe, A. Guichet, O. Guillin, A.L. Hartikainen, D. Heron, L. Hippolyte, M. Holder, G. Homuth, B. Isidor, S. Jaillard, Z. Jaros, S. Jiménez-Murcia, G.J. Helas, P. Jonveaux, S. Kaksonen, B. Keren, A. Kloss-Brandstätter, N.V. Knoers, D.A. Koolen, P.M. Kroisel, F. Kronenberg, A. Labalme, E. Landais, E. Lapi, V. Layet, S. Legallic, B. Leheup, B. Leube, S. Lewis, J. Lucas, K.D. MacDermot, P. Magnusson, C. Marshall, M. Mathieu-Dramard, M.I. McCarthy, T. Meitinger, M.A. Mencarelli, G. Merla, A. Moerman, V. Mooser, F. Morice-Picard, M. Mucciolo, M. Nauck, N.C. Ndiaye, A. Nordgren, L. Pasquier, F. Petit, R. Pfundt, G. Plessis, E. Rajcan-Separovic, G.P. Ramelli, A. Rauch, R. Ravazzolo, A. Reis, A. Renieri, C. Richart, J.S. Ried, C. Rieubland, W. Roberts, K.M. Roetzer, C. Rooryck, M. Rossi, E. Saemundsen, V. Satre, C. Schurmann, E. Sigurdsson, D.J. Stavropoulos, H. Stefansson, C. Tengström, U. Thorsteinsdóttir, F.J. Tinahones, R. Touraine, L. Vallée, E. van Binsbergen, N. Van der Aa, C. Vincent-Delorme, S. Visvikis-Siest, P. Vollenweider, H. Völzke, A.T. Vulto-van Silfhout, G. Waeber, C. Wallgren-Pettersson, R.M. Witwicki, S. Zwolinksi, J. Andrieux, X. Estivill, J.F. Gusella, O. Gustafsson, A. Metspalu, S.W. Scherer, K. Stefansson, A.I. Blakemore, J.S. Beckmann, P. Froguel, Mirror extreme BMI phenotypes associated with gene dosage at the chromosome 16p11.2 locus. Nature 478(7367), 97–102 (2011)
G.K.W. Frank, J.R. Reynolds, M.E. Shott, L. Jappe, T.T. Yang, J.R. Tregellas, R.C. O’Reilly, Anorexia nervosa and obesity are associated with opposite brain reward response. Neuropsychopharmacology. 37, 2031–2046 (2012)
K. Aschenbrenner, N. Scholze, P. Joraschky, T. Hummel, Gustatory and olfactory sensitivity in patients with anorexia and bulimia in the course of treatment. J. Psychiatr. Res. 43, 129–137 (2008)
K.J. Burdach, R.L. Doty, The effects of mouth movements, swallowing, and spitting on retronasal odor perception. Physiol. Behav. 41, 353–356 (1987)
F. Dazzi, S.De Nitto, G. Zambetti, C. Loriedo, A. Ciofalo, Alterations of the olfactory-gustatory functions in patients with eating disorders. Eur. Eat. Disord. Rev. 21, 382–385 (2013)
N. Rapps, K.E. Giel, E. Söhngen, A. Salini, P. Enck, S.C. Bischoff, S. Zipfel, Olfactory deficits in patients with anorexia nervosa. Eur. Eat. Disord. Rev. 18, 385–389 (2010)
D. Stein, R. Gross-Isseroff, R. Besserglick, A. Ziv, G. Mayer, A. Yaroslavsky, A. Toledano, H. Voet, A. Weizman, H. Hermesh, Olfactory function and alternation learning in eating disorders. Eur. Neuropsychopharmacol. 22, 615–624 (2012)
G. Goldzak-Kunik, R. Friedman, M. Spitz, L. Sandler, M. Leshem, Intact sensory function in anorexia nervosa. Am. J. Clin. Nutr. 95, 272–282 (2012)
L.C. Kopala, K. Good, E.M. Goldner, C.L. Birmingham, Olfactory identification ability in anorexia nervosa. J. Psychiatry Neurosci. 20, 283–286 (1995)
G.K. Frank, M.E. Shott, J.O. Hagman, V.A. Mittal, Alterations in brain structures related to taste reward circuitry in ill and recovered anorexia nervosa and in bulimia nervosa. Am. J. Psychiatry 170, 1152–1160 (2013)
T.A. Oberndorfer, G.K.W. Frank, A.N. Simmons, A. Wagner, D. McCurdy, J.L. Fudge, T.T. Yang, M.P. Paulus, W.H. Kaye, Altered insula response to sweet taste processing after recovery from anorexia and bulimia nervosa. Am. J. Psychiatry 170, 1143–1151 (2013)
B.E. Richardson, E.A. Vander Woude, R. Sudan, J.S. Thompson, D.A. Leopold, Altered olfactory acuity in the morbidly obese. Obes. Surg. 14, 967–969 (2004)
U. Simchen, C. Koebnick, S. Hoyer, S. Issanchou, H.-J.F. Zunft, Odour and taste sensitivity is associated with body weight and extent of misreporting of body weight. Eur. J. Clin. Nutr. 60, 698–705 (2006)
F. Sartor, L.F. Donaldson, D.A. Markland, H. Loveday, M.J. Jackson, H.P. Kubis, Taste perception and implicit attitude toward sweet related to body mass index and soft drink supplementation. Appetite. 57, 237–246 (2011)
H.-R. Berthoud, C. Morrison, The Brain, Appetite, and Obesity. Annu. Rev. Psychol. 59, 55–92 (2008)
C.B. Saper, Hypothalamic connections with the cerebral cortex. Prog. Brain Res. 126, 39–48 (2000)
J.V. Verhagen, The neurocognitive bases of human multimodal food perception: consciousness. Brain Res. Rev. 53, 271–286 (2007)
M.S.La Sala, M.D. Hurtado, A.R. Brown, D.V. Bohórquez, R.A. Liddle, H. Herzog, S. Zolotukhin, C.D. Dotson, Modulation of taste responsiveness by the satiation hormone peptide YY. FASEB J. 27, 5022–5033 (2013)
B. Palouzier-Paulignan, M.-C. Lacroix, P. Aimé, C. Baly, M. Caillol, P. Congar, K.A. Julliard, K. Tucker, D.A. Fadool, Olfaction under metabolic influences. Chem. Senses 37, 769–797 (2012)
P. Monteleone, F. Piscitelli, P. Scognamiglio, A.M. Monteleone, B. Canestrelli, V. Di Marzo, M. Maj, Hedonic eating is associated with increased peripheral levels of ghrelin and the endocannabinoid 2-arachidonoyl-glycerol in healthy humans: a pilot study. J. Clin. Endocrinol. Metab. 97, E917–E924 (2012)
L.M. Seoane, O. Al-Massadi, J.E. Caminos, S.A. Tovar, C. Dieguez, F.F. Casanueva, Sensory stimuli directly acting at the central nervous system regulate gastric ghrelin secretion. an ex vivo organ culture study. Endocrinology 148, 3998–4006 (2007)
APA, Diagnostic and Statistical Manual of Mental Disorders: DSM-5 (American Psychiatric Association, Washington, DC, 2013)
First, M.B. et, Spitzer, R.L., Gibbon, M., Williams, J.B.W.: Structured Clinical Interview for DSM-IV Axis I Disorders, Clinician Version (SCID-CV). (1997)
D.M. Garner, Eating Disorder Inventory-2 (Psychological Assessment Resources, Odessa, 1991)
L.R. Derogatis, SCL-90-R Symptom Checklist-90-R. Administration, Scoring and Procedures Manual (National Computer System, Minneapolis, 1994)
T. Van Strien, J.E. Frijters, G. Bergers, P.B. Defares, The Dutch Eating Behavior Questionnaire (DEBQ) for assessment of restrained, emotional, and external eating behavior. Int. J. Eat. Disord. 5(2), 295–315 (1986)
G. Kobal, T. Hummel, B. Sekinger, S. Barz, S. Roscher, S. Wolf, “Sniffin” Sticks’: screening of olfactory performance. Rhinology. 34, 222–226 (1996)
T. Hummel, B. Sekinger, S.R. Wolf, E. Pauli, G. Kobal, “Sniffin” sticks’. Olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. Chem. Senses 22, 39–52 (1997)
A. Haehner, C. Tosch, M. Wolz, L. Klingelhoefer, M. Fauser, A. Storch, H. Reichmann, T. Hummel, Olfactory training in patients with Parkinson’s disease. PLoS ONE 8, e61680 (2013)
C. Mueller, S. Kallert, B. Renner, K. Stiassny, A.F.P. Temmel, T. Hummel, G. Kobal, Quantitative assessment of gustatory function in a clinical context using impregnated “taste strips”. Rhinology. 41, 2–6 (2003)
R.B. Kline, Principles and practice of structural equation modeling (The Guilford Press, New York, 2010)
S. Trellakis, S. Tagay, C. Fischer, A. Rydleuskaya, A. Scherag, K. Bruderek, S. Schlegl, J. Greve, A.E. Canbay, S. Lang, S. Brandau, Ghrelin, leptin and adiponectin as possible predictors of the hedonic value of odors. Regul. Pept. 167, 112–117 (2011)
M.R. Druce, M.A. Wren, J.A. Park, J.E. Milton, M. Patterson, G. Frost, M.A. Ghatei, C. Small, S.R. Bloom, Ghrelin increases food intake in obese as well as lean subjects. Int. J. Obes. (Lond). 29, 1130–1136 (2005)
M. Tschöp, C. Weyer, P.A. Tataranni, V. Devanarayan, E. Ravussin, M.L. Heiman, Circulating ghrelin levels are decreased in human obesity. Diabetes 50, 707–709 (2001)
N. Thiebaud, M.C. Johnson, J.L. Butler, G.A. Bell, K.L. Ferguson, A.R. Fadool, J.C. Fadool, A.M. Gale, D.S. Gale, D.A. Fadool, Hyperlipidemic diet causes loss of olfactory sensory neurons, reduces olfactory discrimination, and disrupts odor-reversal learning. J. Neurosci. 34, 6970–6984 (2014)
B.E. Richardson, E.A. Vander Woude, D.A. Leopold, J.S. Thompson, Gastric bypass does not influence olfactory function in obese patients. Obes. Surg. 22, 283–286 (2012)
J.D. Cameron, G.S. Goldfield, É. Doucet, Fasting for 24 h improves nasal chemosensory performance and food palatability in a related manner. Appetite. 58, 978–981 (2012)
I.C. Fedoroff, S.A. Stoner, A.E. Andersen, R.L. Doty, B.J. Rolls, Olfactory dysfunction in anorexia and bulimia nervosa. Int. J. Eat. Disord. 18, 71–77 (1995)
J. Mullol, I. Alobid, F. Mariño-Sánchez, L. Quintó, J. de Haro, M. Bernal-Sprekelsen, A. Valero, C. Picado, C. Marin, Furthering the understanding of olfaction, prevalence of loss of smell and risk factors: a population-based survey (OLFACAT study). BMJ Open. 2, e001256 (2012)
H.I. Davidson, R.M. Pattison, R.A. Richardson, Clinical undernutrition states and their influence on taste. Proc. Nutr. Soc. 57, 633–638 (1998)
J. Rodin, L. Bartoshuk, C. Peterson, D. Schank, Bulimia and taste: possible interactions. J. Abnorm. Psychol. 99, 32–39 (1990)
C.M. Vicario, Altered insula response to sweet taste processing in recovered anorexia and bulimia nervosa: a matter of disgust sensitivity? Am. J. Psychiatry 170, 1497 (2013)
A.B. Maliphol, D.J. Garth, K.F. Medler, Diet-induced obesity reduces the responsiveness of the peripheral taste receptor cells. PLoS ONE 8, e79403 (2013)
A. Tortorella, F. Brambilla, M. Fabrazzo, U. Volpe, A.M. Monteleone, D. Mastromo, P. Monteleone, Central and peripheral peptides regulating eating behaviour and energy homeostasis in anorexia nervosa and bulimia nervosa: a literature review. Eur. Eat. Disord. Rev. 22, 307–320 (2014)
J.H. Baker, C.L. Sisk, L.M. Thornton, H. Brandt, S. Crawford, M.M. Fichter, K.A. Halmi, C. Johnson, I. Jones, A.S. Kaplan, J.E. Mitchell, M. Strober, J. Treasure, D.B. Woodside, W.H. Berrettini, W.H. Kaye, C.M. Bulik, K.L. Klump, Primary amenorrhea in anorexia nervosa: impact on characteristic masculine and feminine traits. Eur. Eat. Disord. Rev. 22, 32–38 (2014)
Acknowledgments
This manuscript was supported by grants from Instituto de Salud Carlos III (Fondo de Investigación Sanitaria FIS PI11/210, FIS PI14/290 and CIBERobn) and Fondo Europeo de Desarrollo Regional (FEDER). CIBERObn is an initiative of ISCIII. Jose C. Fernández-García is recipient of a ‘Rio Hortega’ contract from ‘Instituto de Salud Carlos III,’ Madrid, Spain (CM12/00059). L. Garrido-Sánchez is supported by a fellowship from the Fondo de Investigación Sanitaria (FIS) “Miguel Servet I” MS13/00188-CP13/00188. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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Fernández-Aranda, F., Agüera, Z., Fernández-García, J.C. et al. Smell–taste dysfunctions in extreme weight/eating conditions: analysis of hormonal and psychological interactions. Endocrine 51, 256–267 (2016). https://doi.org/10.1007/s12020-015-0684-9
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DOI: https://doi.org/10.1007/s12020-015-0684-9