The impact of olfactory and gustatory perception on metabolic homeostasis in obese patients
Iu. G. Samoilova,
D. V. Podchinenova,
M. V. Matveeva,
D. A. Kudlay,
O. A. Oleynik,
I. V. Tolmachev,
I. S. Kaverina,
T. D. Vachadze,
M. A. Kovarenko,
O. A. Loginova https://doi.org/10.29413/ABS.2023-8.3.10
Abstract
Obesity is currently a major global public health problem. As a result, in recent decades there has been a growing interest in studying the impact of this disease on the functioning of the central nervous system. One of the least understood aspects is the impact that obesity has on sensory systems.
The olfactory and gustatory systems are closely related to various vital functions, such as the nocifensors activation, the stimulation of digestive reflexes. In addition, these sensory systems are known to play an important role in the mechanisms of food consumption through the regulation of appetite and satiety, influencing food choice and, therefore, they are involved in the development of obesity. A number of clinical studies have shown that obese patients are more likely to suffer from hyposmia compared to lean people of the same age.
The reasons why this relationship exists remain largely unclear. The aim of this review is to assess the available data on this topic and to identify new promising areas for further research. The review was conducted in the PubMed databases for 2017–2023.
About the Authors
Iu. G. Samoilova
Siberian State Medical University
Russian Federation
Russian Federation
Iuliia G. Samoilova – Dr. Sc. (Med.), Professor, Head of the Department of Pediatrics with a Course of Endocrinology
Moskovsky trakt 2, Tomsk 634050, Russian Federation
D. V. Podchinenova
Siberian State Medical University
Russian Federation
Russian Federation
Daria V. Podchinenova – Cand. Sc. (Med.), Associate Professor at the Department of Pediatrics with a Course of Endocrinology
Moskovsky trakt 2, Tomsk 634050, Russian Federation
M. V. Matveeva
Siberian State Medical University
Russian Federation
Russian Federation
Mariia V. Matveeva – Dr. Sc. (Med.), Professor at the Department of Pediatrics with a Course of Endocrinology
Moskovsky trakt 2, Tomsk 634050, Russian Federation
D. A. Kudlay
Institute of Pharmacy, I.M. Sechenov First Moscow State Medical University of the Ministry of Health Care of Russian Federation (Sechenov University); National Research Center – Institute of Immunology, Federal Medical and Biological Agency of Russia
Russian Federation
Russian Federation
Dmitry A. Kudlay – Dr. Sc. (Med.), Corresponding Member of the RAS, Professor at the Department of Pharmacology; Leading Research Officer at the Laboratory of Personalized Medicine and Molecular Immunology No. 71
Trubetskaya str. 8 building 2, Moscow 119991, Russian Federation
Kashirskoe highway 24, Moscow 115522, Russian Federation
O. A. Oleynik
Siberian State Medical University
Russian Federation
Russian Federation
Oxana A. Oleynik – Cand. Sc. (Med.), Associate Professor at the Department of Pediatrics with a Course of Endocrinology
Moskovsky trakt 2, Tomsk 634050, Russian Federation
I. V. Tolmachev
Siberian State Medical University
Russian Federation
Russian Federation
Ivan V. Tolmachev – Cand. Sc. (Med.), Associate Professor at the Department of Medical and Biological Cybernetics
Moskovsky trakt 2, Tomsk 634050, Russian Federation
I. S. Kaverina
Siberian State Medical University
Russian Federation
Russian Federation
Irina S. Kaverina – Research Officer at the Scientific and Educational Laboratory “Bionic Digital Platforms”
Moskovsky trakt 2, Tomsk 634050, Russian Federation
T. D. Vachadze
Siberian State Medical University
Russian Federation
Russian Federation
Tamara D. Vachadze – Resident at the Department of Pediatrics with a Course of Endocrinology
Moskovsky trakt 2, Tomsk 634050, Russian Federation
M. A. Kovarenko
Siberian State Medical University
Russian Federation
Russian Federation
Margarita A. Kovarenko – Cand. Sc. (Med.), Teaching Assistant at the Department of Pediatrics with a Course of Endocrinology
Moskovsky trakt 2, Tomsk 634050, Russian Federation
O. A. Loginova
Siberian State Medical University
Russian Federation
Russian Federation
Olga A. Loginova – Resident at the Department of General Medicine and Outpatient Therapy
Moskovsky trakt 2, Tomsk 634050, Russian Federation
References
1. World Health Organization. WHO European Regional Obesity Report 2022. 2022.
2. Rebolledo Solleiro D, Solleiro Villavicencio H, Velasco M, Roldán Roldán G. Obesidad, síndrome metabólico y percepción olfativa. Revista de Neurología. 2020; 70(02): 53. doi: 10.33588/rn.7002.2019204
3. Lötsch J, Kringel D, Hummel T. Machine learning in human olfactory research. Chem Senses. 2019; 44(1): 11-22. doi: 10.1093/chemse/bjy067
4. Menni C, Valdes AM, Freidin MB, Sudre CH, Nguyen LH, Drew DA, et al. Real-time tracking of self-reported symptoms to predict potential COVID-19. Nat Med. 2020; 26(7): 1037-1040. doi: 10.1038/s41591-020-0916-2
5. Martynov MYu, Bogolepova AN, Yasamanova AN. Endothelial dysfunction in COVID-19 and cognitive impairment. Zhurnal nevrologii i psikhiatrii imeni S.S. Korsakova. 2021; 121(6): 93-99. (In Russ.). doi: 10.17116/jnevro202112106193
6. Asfandiyarova NS. Post-COVID-19 syndrome. Clinical Medicine (Russian Journal). 2021; 99(7-8): 429-435. (In Russ.). doi: 10.30629/0023-2149-2021-99-7-8-429-435
7. Bordin A, Mucignat-Caretta C, Gaudioso P, Pendolino AL, Leoni D, Scarpa B, et al. Comparison of self-reported symptoms and psychophysical tests in coronavirus disease 2019 (COVID-19) subjects experiencing long-term olfactory dysfunction: A 6-month follow-up study. Int Forum Allergy Rhinol. 2021; 11(11): 1592-1595. doi: 10.1002/alr.22828
8. Hummel T, Podlesek D. Clinical assessment of olfactory function. Chem Senses. 2021; 46: bjab053. doi: 10.1093/chemse/bjab053
9. Seubert J, Laukka EJ, Rizzuto D, Hummel T, Fratiglioni L, Bäckman L, et al. Prevalence and correlates of olfactory dysfunction in old age: A population-based study. J Gerontol A Biol Sci Med Sci. 2017; 72(8): 1072-1079. doi: 10.1093/gerona/glx054
10. Goverover Y, Chen MH, Costa SL, Chiaravalloti ND, DeLuca J. Smell as a clinical-marker for functional limitations in multiple sclerosis: A pilot study. Mult Scler Relat Disord. 2020; 46: 102508. doi: 10.1016/j.msard.2020.102508
11. Marin C, Vilas D, Langdon C, Alobid I, López-Chacón M, Haehner A, et al. Olfactory dysfunction in neurodegenerative diseases. Curr Allergy Asthma Rep. 2018; 18(8): 42. doi: 10.1007/s11882-018-0796-4
12. Amital H, Agmon-Levin N, Shoenfeld N, Arnson Y, Amital D, Langevitz P, et al. Olfactory impairment in patients with the fibromyalgia syndrome and systemic sclerosis. Immunol Res. 2014; 60(2-3): 201-207. doi: 10.1007/s12026-014-8573-5
13. Bombini MF, Peres FA, Lapa AT, Sinicato NA, Quental BR, Pincelli Á de SM, et al. Olfactory function in systemic lupus erythematosus and systemic sclerosis. A longitudinal study and review of the literature. Autoimm Rev. 2018; 17(4): 405-412. doi: 10.1016/j.autrev.2018.02.002
14. Spencer AS, da Silva Dias D, Capelas ML, Pimentel F, Santos T, Neves PM, et al. Managing severe dysgeusia and dysosmia in lung cancer patients: A systematic scoping review. Front Oncol. 2021; 11: 774081. doi: 10.3389/fonc.2021.774081
15. Zhou T, Yang K, Thapa S, Liu H, Wang B, Yu S. Differences in symptom burden among cancer patients with different stages of cachexia. J Pain Symptom Manage. 2017; 53(5): 919-926. doi: 10.1016/j.jpainsymman.2016.12.325
16. Falkowski B, Duda-Sobczak A, Araszkiewicz A, Chudzinski M, Urbas M, Gajewska E, et al. Insulin resistance is associated with impaired olfactory function in adult patients with type 1 diabetes: A cross-sectional study. Diabetes Metab Res Rev. 2020; 36(6): e3307. doi: 10.1002/dmrr.3307
17. Catamo E, Tornese G, Concas MP, Gasparini P, Robino A. Differences in taste and smell perception between type 2 diabetes mellitus patients and healthy controls. Nutr Metab Cardiovasc Dis. 2021; 31(1): 193-200. doi: 10.1016/j.numecd.2020.08.025
18. Faour M, Magnan C, Gurden H, Martin C. Olfaction in the context of obesity and diabetes: Insights from animal models to humans. Neuropharmacol. 2022; 206: 108923. doi: 10.1016/j.neuropharm.2021.108923
19. Khan AS, Hichami A, Khan NA. Obesity and COVID-19: Oronaso-sensory perception. J Clin Med. 2020; 9(7): 2158. doi: 10.3390/jcm9072158
20. Singh AK, Gillies CL, Singh R, Singh A, Chudasama Y, Coles B, et al. Prevalence of co-morbidities and their association with mortality in patients with COVID-19: A systematic review and meta-analysis. Diabetes Obes Metab. 2020; 22(10): 1915-1924. doi: 10.1111/dom.14124
21. Kim D, Adeniji N, Latt N, Kumar S, Bloom PP, Aby ES, et al. Predictors of outcomes of COVID-19 in patients with chronic liver disease: US multi-center study. Clin Gastroenterol Hepatol. 2021; 19(7): 1469-1479.e19. doi: 10.1016/j.cgh.2020.09.027
22. Bentsen MA, Mirzadeh Z, Schwartz MW. Revisiting how the brain senses glucose – And why. Cell Metab. 2019; 29(1): 11-17. doi: 10.1016/j.cmet.2018.11.001
23. Caretta A, Mucignat-Caretta C. Not only COVID-19: Involvement of multiple chemosensory systems in human diseases. Front Neural Circuits. 2022; 16: 862005. doi: 10.3389/fncir.2022.862005
24. Ercoli T, Masala C, Pinna I, Orofino G, Solla P, Rocchi L, et al. Qualitative smell/taste disorders as sequelae of acute COVID-19. Neurol Sci. 2021; 42(12): 4921-4926. doi: 10.1007/s10072-021-05611-6
25. Luke L, Lee L, Jegatheeswaran L, Philpott C. Investigations and outcomes for olfactory disorders. Curr Otorhinolaryngol Rep. 2022; 10(4): 377-384. doi: 10.1007/s40136-022-00438-x
26. Zhou T, Matsunami H. Lessons from single-cell transcriptome analysis of oxygen-sensing cells. Cell Tissue Res. 2018; 372(2): 403-415. doi: 10.1007/s00441-017-2682-0
27. Červený K, Janoušková K, Vaněčková K, Zavázalová Š, Funda D, Astl J, et al. Olfactory evaluation in clinical medical practice. J Clin Med. 2022; 11(22): 6628. doi: 10.3390/jcm11226628
28. Maßberg D, Hatt H. Human olfactory receptors: Novel cellular functions outside of the nose. Physiol Rev. 2018; 98(3): 1739-1763. doi: 10.1152/physrev.00013.2017
29. Dalesio NM, Barreto Ortiz SF, Pluznick JL, Berkowitz DE. Olfactory, taste, and photo sensory receptors in non-sensory organs: It just makes sense. Front Physiol. 2018; 9: 1673. doi: 10.3389/fphys.2018.01673
30. Zhang S, Li L, Li H. Role of ectopic olfactory receptors in glucose and lipid metabolism. Br J Pharmacol. 2021; 178(24): 4792-4807. doi: 10.1111/bph.15666
31. Julliard AK, al Koborssy D, Fadool DA, Palouzier-Paulignan B. Nutrient sensing: Another chemosensitivity of the olfactory system. Front Physiol. 2017; 8: 468. doi: 10.3389/fphys.2017.00468
32. Kim LJ, Polotsky VY. Carotid body and metabolic syndrome: Mechanisms and potential therapeutic targets. Int J Mol Sci. 2020; 21(14): 5117. doi: 10.3390/ijms21145117
33. Sacramento JF, Andrzejewski K, Melo BF, Ribeiro MJ, Obeso A, Conde SV. Exploring the mediators that promote carotid body dysfunction in type 2 diabetes and obesity related syndromes. Int J Mol Sci. 2020; 21(15): 5545. doi: 10.3390/ijms21155545
34. Berthoud H, Neuhuber WL. Vagal mechanisms as neuromodulatory targets for the treatment of metabolic disease. Ann N Y Acad Sci. 2019; 1454(1): 42-55. doi: 10.1111/nyas.14182
35. Zwickl H, Zwickl-Traxler E, Pecherstorfer M. Is neuronal histamine signaling involved in cancer cachexia? Implications and perspectives. Front Oncol. 2019; 9: 1409. doi: 10.3389/fonc.2019.01409
36. Antuna-Puente B, Fellahi S, McAvoy C, Fève B, Bastard JP. Interleukins in adipose tissue: Keeping the balance. Mol Cell Endocrinol. 2022; 542: 111531. doi: 10.1016/j.mce.2021.111531
37. Laviano A, Koverech A, Seelaender M. Assessing pathophysiology of cancer anorexia. Curr Opin Clin Nutr Metab Care. 2017; 20(5): 340-345. doi: 10.1097/MCO.0000000000000394
38. Crane JD, Palanivel R, Mottillo EP, Bujak AL, Wang H, Ford RJ, et al. Inhibiting peripheral serotonin synthesis reduces obesity and metabolic dysfunction by promoting brown adipose tissue thermogenesis. Nat Med. 2015; 21(2): 166-172. doi: 10.1038/nm.3766
39. Yabut JM, Crane JD, Green AE, Keating DJ, Khan WI, Steinberg GR. Emerging roles for serotonin in regulating metabolism: New implications for an ancient molecule. Endocr Rev. 2019; 40(4): 1092-1107. doi: 10.1210/er.2018-00283
40. Wilk K, Korytek W, Pelczyńska M, Moszak M, Bogdański P. The effect of artificial sweeteners use on sweet taste perception and weight loss efficacy: A review. Nutrients. 2022; 14(6): 1261. doi: 10.3390/nu14061261
41. Depoortere I. Taste receptors of the gut: Emerging roles in health and disease. Gut. 2014; 63(1): 179-190. doi: 10.1136/gutjnl-2013-305112
42. Raka F, Farr S, Kelly J, Stoianov A, Adeli K. Metabolic control via nutrient-sensing mechanisms: Role of taste receptors and the gut-brain neuroendocrine axis. Am J Physiol Endocrinol Metabol. 2019; 317(4): E559-E572. doi: 10.1152/ajpendo.00036.2019
43. Timasheva YR, Balkhiyarova ZR, Kochetova OV. Current state of the obesity research: Genetic aspects, the role of microbiome, and susceptibility to COVID-19. Problems of Endocrinology. 2021; 67(4): 20-35. (In Russ.) doi: 10.14341/probl12775
44. Daly DM, Park SJ, Valinsky WC, Beyak MJ. Impaired intestinal afferent nerve satiety signalling and vagal afferent excitability in diet induced obesity in the mouse. J Physiol. 2011; 589(11): 2857-2870. doi: 10.1113/jphysiol.2010.204594
45. de Lartigue G, Barbier de la Serre C, Espero E, Lee J, Raybould HE. Diet-induced obesity leads to the development of leptin resistance in vagal afferent neurons. Am J Physiol Endocrinol Metab. 2011; 301(1): E187-E195. doi: 10.1152/ajpendo.00056.2011
46. Covasa M, Ritter RC. Adaptation to high-fat diet reduces inhibition of gastric emptying by CCK and intestinal oleate. Am J Physiol Regul Integr Comp Physiol. 2000; 278(1): R166-R170. doi: 10.1152/ajpregu.2000.278.1.R166
47. Daly DM, Park SJ, Valinsky WC, Beyak MJ. Impaired intestinal afferent nerve satiety signalling and vagal afferent excitability in diet induced obesity in the mouse. J Physiol. 2011; 589(11): 2857-2870. doi: 10.1113/jphysiol.2010.204594
48. Pedersen J, Pedersen NB, Brix SW, Grunddal KV, Rosenkilde MM, Hartmann B, et al. The glucagon-like peptide 2 receptor is expressed in enteric neurons and not in the epithelium of the intestine. Peptides. 2015; 67: 20-28. doi: 10.1016/j.peptides.2015.02.007
49. Grasset E, Puel A, Charpentier J, Collet X, Christensen JE, Tercé F, et al. A specific gut microbiota dysbiosis of type 2 diabetic mice induces GLP-1 resistance through an enteric NO-dependent and gut-brain axis mechanism. Cell Metab. 2017; 25(5): 1075-1090. e5. doi: 10.1016/j.cmet.2017.04.013
50. Shirazi-Beechey SP, Daly K, Al-Rammahi M, Moran AW, Bravo D. Role of nutrient-sensing taste 1 receptor (T1R) family members in gastrointestinal chemosensing. Br J Nutr. 2014; 111(S1): S8-S15. doi: 10.1017/S0007114513002286
51. Steinert RE, Beglinger C. Nutrient sensing in the gut: interactions between chemosensory cells, visceral afferents and the secretion of satiation peptides. Physiol Behav. 2011; 105(1): 62-70. doi: 10.1016/j.physbeh.2011.02.039
52. Doty RL. Measurement of chemosensory function. World J Otorhinolaryngol Head Neck Surg. 2018; 4(1): 11-28. doi: 10.1016/j.wjorl.2018.03.001
53. Tomita H, Ikeda M. Clinical use of electrogustometry: Strengths and limitations. Acta Otolaryngol. 2002; 122(4): 27-38. doi: 10.1080/00016480260046391
54. Doty RL, Crastnopol B. Correlates of chemosensory malingering. Laryngoscope. 2010; 120(4): 707-711. doi: 10.1002/lary.20827
55. Doty RL, Kamath V. The influences of age on olfaction: A review. Front Psychol. 2014; 5: 20. doi: 10.3389/fpsyg.2014.00020
56. Deglaire A, Méjean C, Castetbon K, Kesse-Guyot E, Hercberg S, Schlich P. Associations between weight status and liking scores for sweet, salt and fat according to the gender in adults (The Nutrinet-Santé study). Eur J Clin Nutr. 2015; 69(1): 40-46. doi: 10.1038/ejcn.2014.139
57. Bartoshuk LM, Duffy VB, Hayes JE, Moskowitz HR, Snyder DJ. Psychophysics of sweet and fat perception in obesity: Problems, solutions and new perspectives. Philosoph Trans R Soc Lond B Biol Sci. 2006; 361(1471): 1137-1148. doi: 10.1098/rstb.2006.1853
58. Sarkar S, Kochhar KP, Khan NA. Fat addiction: Psychological and physiological trajectory. Nutrients. 2019; 11(11): 2785. doi: 10.3390/nu11112785
59. Khan AS, Keast R, Khan NA. Preference for dietary fat: From detection to disease. Prog Lipid Res. 2020; 78: 101032. doi: 10.1016/j.plipres.2020.101032
60. Khan AS, Hichami A, Khan NA. Taste perception and its effects on oral nutritional supplements in younger life phases. Curr Opin Clin Nutr Metab Care. 2018; 21(5): 411-415. doi: 10.1097/MCO.0000000000000492
61. Tomassini Barbarossa I, Ozdener MH, Melis M, LoveGregory L, Mitreva M, Abumrad NA, et al. Variant in a common odorant-binding protein gene is associated with bitter sensitivity in people. Behav Brain Res. 2017; 329: 200-204. doi: 10.1016/j.bbr.2017.05.015
62. Patel ZM, DelGaudio JM, Wise SK. Higher body mass index is associated with subjective olfactory dysfunction. Behav Neurol. 2015; 2015: 1-4. doi: 10.1155/2015/675635
63. Ramos-Lopez O, Riezu-Boj JI, Milagro FI, Zulet MA, Santos JL, Martinez JA. Associations between olfactory pathway gene methylation marks, obesity features and dietary intakes. Genes Nutr. 2019; 14(1): 11. doi: 10.1186/s12263-019-0635-9
64. Kaufman A, Choo E, Koh A, Dando R. Inflammation arising from obesity reduces taste bud abundance and inhibits renewal. PLOS Biol. 2018; 16(3): e2001959. doi: 10.1371/journal.pbio.2001959
65. Roura E, Depoortere I, Navarro M. Review: Chemosensing of nutrients and non-nutrients in the human and porcine gastrointestinal tract. Animal. 2019; 13(11): 2714-2726. doi: 10.1017/S1751731119001794
66. Li Y, Cui J, Liu Y, Chen K, Huang L, Liu Y. Oral, tongue-coating microbiota, and metabolic disorders: A novel area of interactive research. Front Cardiovasc Med. 2021; 8: 730203. doi: 10.3389/fcvm.2021.730203
67. Samoilova YuG, Oleynik OA, Kudlay DA, Sagan EV, Denisov NS. Pathogenetic relationship of oral microbiota and obesity in children and adolescents. Rossiyskiy Vestnik Perinatologii i Pediatrii. 2021; 66(5): 38-41. (In Russ.). doi: 10.21508/1027-4065-2021-66-5-38-41
68. Steensels S, Cools L, Avau B, Vancleef L, Farré R, Verbeke K, et al. Supplementation of oligofructose, but not sucralose, decreases high-fat diet induced body weight gain in mice independent of gustducin-mediated gut hormone release. Mol Nutr Food Res. 2017; 61(3): 1600716. doi: 10.1002/mnfr.201600716
69. Pignatelli P, Fabietti G, Ricci A, Piattelli A, Curia MC. How periodontal disease and presence of nitric oxide reducing oral bacteria can affect blood pressure. Int J Mol Sci. 2020; 21(20): 7538. doi: 10.3390/ijms21207538
70. Hsu PC, Wu HK, Huang YC, Chang HH, Lee TC, Chen YP, et al. The tongue features associated with type 2 diabetes mellitus. Medicine. 2019; 98(19): e15567. doi: 10.1097/MD.0000000000015567
Review
For citations:
Samoilova I.G., Podchinenova D.V., Matveeva M.V., Kudlay D.A., Oleynik O.A., Tolmachev I.V., Kaverina I.S., Vachadze T.D., Kovarenko M.A., Loginova O.A. The impact of olfactory and gustatory perception on metabolic homeostasis in obese patients. Acta Biomedica Scientifica. 2023;8(3):96-105. https://doi.org/10.29413/ABS.2023-8.3.10
Views:
3728
.png)
Email this article 
