Skip to main content

Advertisement

Log in

Smell–taste dysfunctions in extreme weight/eating conditions: analysis of hormonal and psychological interactions

  • Original Article
  • Published:
Endocrine Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. 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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. 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)

    Article  Google Scholar 

  3. 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)

    Article  PubMed  Google Scholar 

  4. 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)

    Article  PubMed  PubMed Central  Google Scholar 

  5. 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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. 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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. 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)

    Article  PubMed  Google Scholar 

  8. K.J. Burdach, R.L. Doty, The effects of mouth movements, swallowing, and spitting on retronasal odor perception. Physiol. Behav. 41, 353–356 (1987)

    Article  CAS  PubMed  Google Scholar 

  9. 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)

    Article  PubMed  Google Scholar 

  10. 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)

    Article  PubMed  Google Scholar 

  11. 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)

    Article  CAS  PubMed  Google Scholar 

  12. 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)

    Article  CAS  PubMed  Google Scholar 

  13. L.C. Kopala, K. Good, E.M. Goldner, C.L. Birmingham, Olfactory identification ability in anorexia nervosa. J. Psychiatry Neurosci. 20, 283–286 (1995)

    CAS  PubMed  PubMed Central  Google Scholar 

  14. 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)

    Article  PubMed  PubMed Central  Google Scholar 

  15. 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)

    Article  PubMed  PubMed Central  Google Scholar 

  16. 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)

    Article  PubMed  Google Scholar 

  17. 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)

    Article  CAS  PubMed  Google Scholar 

  18. 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)

    Article  PubMed  Google Scholar 

  19. H.-R. Berthoud, C. Morrison, The Brain, Appetite, and Obesity. Annu. Rev. Psychol. 59, 55–92 (2008)

    Article  PubMed  Google Scholar 

  20. C.B. Saper, Hypothalamic connections with the cerebral cortex. Prog. Brain Res. 126, 39–48 (2000)

    Article  CAS  PubMed  Google Scholar 

  21. J.V. Verhagen, The neurocognitive bases of human multimodal food perception: consciousness. Brain Res. Rev. 53, 271–286 (2007)

    Article  PubMed  PubMed Central  Google Scholar 

  22. 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)

    Article  PubMed  PubMed Central  Google Scholar 

  23. 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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. 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)

    Article  CAS  PubMed  Google Scholar 

  25. 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)

    Article  CAS  PubMed  Google Scholar 

  26. APA, Diagnostic and Statistical Manual of Mental Disorders: DSM-5 (American Psychiatric Association, Washington, DC, 2013)

    Google Scholar 

  27. 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)

  28. D.M. Garner, Eating Disorder Inventory-2 (Psychological Assessment Resources, Odessa, 1991)

    Google Scholar 

  29. L.R. Derogatis, SCL-90-R Symptom Checklist-90-R. Administration, Scoring and Procedures Manual (National Computer System, Minneapolis, 1994)

    Google Scholar 

  30. 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)

    Article  Google Scholar 

  31. G. Kobal, T. Hummel, B. Sekinger, S. Barz, S. Roscher, S. Wolf, “Sniffin” Sticks’: screening of olfactory performance. Rhinology. 34, 222–226 (1996)

    CAS  PubMed  Google Scholar 

  32. 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)

    Article  CAS  PubMed  Google Scholar 

  33. 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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. 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)

    CAS  PubMed  Google Scholar 

  35. R.B. Kline, Principles and practice of structural equation modeling (The Guilford Press, New York, 2010)

    Google Scholar 

  36. 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)

    Article  CAS  PubMed  Google Scholar 

  37. 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)

    Article  CAS  Google Scholar 

  38. 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)

    Article  PubMed  Google Scholar 

  39. 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)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. 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)

    Article  PubMed  Google Scholar 

  41. 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)

    Article  PubMed  Google Scholar 

  42. 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)

    Article  CAS  PubMed  Google Scholar 

  43. 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)

    Article  PubMed  PubMed Central  Google Scholar 

  44. H.I. Davidson, R.M. Pattison, R.A. Richardson, Clinical undernutrition states and their influence on taste. Proc. Nutr. Soc. 57, 633–638 (1998)

    Article  CAS  PubMed  Google Scholar 

  45. J. Rodin, L. Bartoshuk, C. Peterson, D. Schank, Bulimia and taste: possible interactions. J. Abnorm. Psychol. 99, 32–39 (1990)

    Article  CAS  PubMed  Google Scholar 

  46. 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)

    Article  PubMed  Google Scholar 

  47. 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)

    Article  PubMed  PubMed Central  Google Scholar 

  48. 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)

    Article  PubMed  Google Scholar 

  49. 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)

    Article  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Fernando Fernández-Aranda or Felipe F. Casanueva.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest associated with this manuscript.

Human and Animal Rights and Informed Consent

All procedures performed were in accordance with the ethical standards of the Ethics Committee of all the institutions involved and with the 1964 Helsinki Declaration and its later amendments. Informed consent was obtained from all individual participants included in the study.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 133 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12020-015-0684-9

Keywords

Navigation