综述

代谢性疾病与嗅觉改变及其机制进展

  • 吴倩 ,
  • 李华婷
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  • 1.上海交通大学医学院附属第六人民医院内分泌代谢科,上海市糖尿病研究所,上海市糖尿病重点实验室,上海市糖尿病临床医学中心,上海 200233
    2.上海交通大学医学院,上海 200025
吴 倩(1998—),女,硕士生;电子信箱:wuqian2021@sjtu.edu.cn
李华婷,电子信箱:huarting99@sjtu.edu.cn

收稿日期: 2023-05-31

  录用日期: 2023-12-05

  网络出版日期: 2024-01-28

基金资助

国家自然科学基金优秀青年科学基金(82022012);上海交通大学医学院“双百人”项目(20191830);上海市高水平地方高校创新团队(SHSMU-ZDCX20212700);上海市内分泌与代谢疾病研究中心(2022ZZ01002);2021年度教育信息化教学应用实践共同体项目

Progress of olfactory changes in metabolic diseases and the mechanisms

  • Qian WU ,
  • Huating LI
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  • 1.Department of Endocrinology and Metabolism, Shanghai Sixth People′s Hospital, Shanghai Jiao Tong University School of Medicine; Shanghai Diabetes Institute; Shanghai Key Laboratory of Diabetes Mellitus; Shanghai Clinical Center for Diabetes, Shanghai 200233, China
    2.Shanghai Jiao Tong University School of Medicine, Shanghai 200025, China
LI Huating, E-mail: huarting99@sjtu.edu.cn.

Received date: 2023-05-31

  Accepted date: 2023-12-05

  Online published: 2024-01-28

Supported by

National Natural Science Foundation of China for Excellent Young Scholars(82022012);"Two-hundred Talents" Program of Shanghai Jiao Tong University School of Medicine(20191830);Innovative Research Team of High-Level Local Universities in Shanghai(SHSMU-ZDCX20212700);Shanghai Municipal Key Clinical Specialty, Shanghai Research Center for Endocrine and Metabolic Diseases(2022ZZ01002);Educational Informatization Teaching Practice Community Project in 2021

摘要

代谢性疾病发病机制复杂,其患病率逐年上升且发病趋向年轻化,已成为全球重要的公共卫生问题。嗅觉是一种重要的感觉功能,在个体的营养和生活质量方面发挥着重要作用。肥胖与嗅觉功能可以相互影响,嗅觉功能受到营养状况的影响,同时在食物摄入、能量消耗和脂质代谢的调节过程中也发挥重要作用,而2型糖尿病、阻塞性睡眠呼吸暂停综合征等代谢性疾病患者也存在嗅觉功能障碍。代谢性疾病出现嗅觉改变的机制包括高血糖、胰岛素抵抗等代谢状态的改变,这些改变可引起肽类激素、脂肪细胞因子和神经递质的调节异常,这些中介分子可能在代谢性疾病和嗅觉功能障碍之间发挥作用;代谢性疾病所产生的血管与神经病变也会引起嗅觉神经的直接损伤或神经传导异常;代谢性疾病导致的肠道菌群紊乱也是引起嗅觉功能障碍的潜在机制。同时,认知功能障碍是代谢性疾病的重要并发症,嗅觉功能障碍是代谢性疾病出现认知障碍的前驱临床表现,有助于疾病的早期识别和评估。该文对代谢性疾病与嗅觉变化之间的关系及其潜在机制的研究现状作一综述。

本文引用格式

吴倩 , 李华婷 . 代谢性疾病与嗅觉改变及其机制进展[J]. 上海交通大学学报(医学版), 2024 , 44(1) : 131 -136 . DOI: 10.3969/j.issn.1674-8115.2024.01.015

Abstract

Metabolic disorders, characterized by a complex pathogenesis, are experiencing a rising prevalence globally and a trend toward younger populations, making them a significant public health concern. Olfaction, a crucial sensory function, plays a pivotal role in an individual′s nutrition and quality of life. There is a bidirectional relationship between obesity and olfactory function. Olfaction is influenced by nutritional status; simultaneously, it plays a vital role in the regulation of food intake, energy expenditure, and lipid metabolism. Moreover, individuals with metabolic disorders such as type 2 diabetes and obstructive sleep apnea syndrome exhibit olfactory dysfunction. Mechanisms underlying olfactory changes in metabolic disorders involve alterations in metabolic states such as hyperglycemia and insulin resistance. These changes can lead to dysregulation of peptide hormones, adipocyte factors, and neurotransmitters, which may potentially act as mediators between metabolic disorders and olfactory dysfunction. Vascular and neural alterations resulting from metabolic disorders can directly damage olfactory nerves or induce abnormal neural transmission. Furthermore, dysbiosis in the gut microbiota induced by metabolic disorders is a potential mechanism for olfactory dysfunction. Cognitive dysfunction is a significant complication of metabolic disorders. Olfactory dysfunction can serve as an early clinical manifestation of cognitive impairment and contributes to early identification and assessment of diseases. This article reviews recent researches on the relationship between metabolic diseases and olfactory changes and the potential mechanisms.

参考文献

1 The Lancet Diabetes Endocrinology. Obesity in China: time to act[J]. Lancet Diabetes Endocrinol, 2021, 9(7): 407.
2 WANG L M, PENG W, ZHAO Z P, et al. Prevalence and treatment of diabetes in China, 2013?2018[J]. JAMA, 2021, 326(24): 2498-2506.
3 BOESVELDT S, DE GRAAF K. The differential role of smell and taste for eating behavior[J]. Perception, 2017, 46(3/4): 307-319.
4 DOTY R L. Olfactory dysfunction in Parkinson disease[J]. Nat Rev Neurol, 2012, 8(6): 329-339.
5 LAFAILLE-MAGNAN M E, POIRIER J, ETIENNE P, et al. Odor identification as a biomarker of preclinical AD in older adults at risk[J]. Neurology, 2017, 89(4): 327-335.
6 ZHANG Z, ZHANG B, WANG X, et al. Olfactory dysfunction mediates adiposity in cognitive impairment of type 2 diabetes: insights from clinical and functional neuroimaging studies[J]. Diabetes Care, 2019, 42(7): 1274-1283.
7 FIRESTEIN S. How the olfactory system makes sense of scents[J]. Nature, 2001, 413(6852): 211-218.
8 THIEBAUD N, JOHNSON M C, BUTLER J L, et al. Hyperlipidemic diet causes loss of olfactory sensory neurons, reduces olfactory discrimination, and disrupts odor-reversal learning[J]. J Neurosci, 2014, 34(20): 6970-6984.
9 CAMPOLO J, CORRADI E, RIZZARDI A, et al. Correlates of olfactory impairment in middle-aged non-diabetic Caucasian subjects with stage Ⅰ?Ⅱ obesity[J]. Eur Arch Otorhinolaryngol, 2021, 278(6): 2047-2054.
10 PENG M, COUTTS D, WANG T, et al. Systematic review of olfactory shifts related to obesity[J]. Obes Rev, 2019, 20(2): 325-338.
11 VELLUZZI F, DELEDDA A, ONIDA M, et al. Relationship between olfactory function and BMI in normal weight healthy subjects and patients with overweight or obesity[J]. Nutrients, 2022, 14(6): 1262.
12 HOLINSKI F, MENENAKOS C, HABER G, et al. Olfactory and gustatory function after bariatric surgery[J]. Obes Surg, 2015, 25(12): 2314-2320.
13 HANCI D, ALTUN H, ALTUN H, et al. Laparoscopic sleeve gastrectomy improves olfaction sensitivity in morbidly obese patients[J]. Obes Surg, 2016, 26(3): 558-562.
14 MAKARONIDIS J M, NEILSON S, CHEUNG W H, et al. Reported appetite, taste and smell changes following Roux-en-Y gastric bypass and sleeve gastrectomy: effect of gender, type 2 diabetes and relationship to post-operative weight loss[J]. Appetite, 2016, 107: 93-105.
15 ZERRWECK C, ZURITA L, áLVAREZ G, et al. Taste and olfactory changes following laparoscopic gastric bypass and sleeve gastrectomy[J]. Obes Surg, 2016, 26(6): 1296-1302.
16 ZERRWECK C, GALLARDO V C, CALLEJA C, et al. Gross olfaction before and after laparoscopic gastric bypass[J]. Obes Surg, 2017, 27(11): 2988-2992.
17 GUYOT E, DOUGKAS A, ROBERT M, et al. Food preferences and their perceived changes before and after bariatric surgery: a cross-sectional study[J]. Obes Surg, 2021, 31(7): 3075-3082.
18 RIERA C E, TSAOUSIDOU E, HALLORAN J, et al. The sense of smell impacts metabolic health and obesity[J]. Cell Metab, 2017, 26(1): 198-211.e5.
19 STAFFORD L D, WHITTLE A. Obese individuals have higher preference and sensitivity to odor of chocolate[J]. Chem Senses, 2015, 40(4): 279-284.
20 KINDLEYSIDES S, BECK K L, WALSH D C I, et al. Fat sensation: fatty acid taste and olfaction sensitivity and the link with disinhibited eating behaviour[J]. Nutrients, 2017, 9(8): 879.
21 POESSEL M, MORYS F, BREUER N, et al. Brain response to food odors is not associated with body mass index and obesity-related metabolic health measures[J]. Appetite, 2022, 168: 105774.
22 LE FLOCH J P, LE LIèVRE G, LABROUE M, et al. Smell dysfunction and related factors in diabetic patients[J]. Diabetes Care, 1993, 16(6): 934-937.
23 WEINSTOCK R S, WRIGHT H N, SMITH D U. Olfactory dysfunction in diabetes mellitus[J]. Physiol Behav, 1993, 53(1): 17-21.
24 CATAMO E, TORNESE G, CONCAS M P, et al. Differences in taste and smell perception between type 2 diabetes mellitus patients and healthy controls[J]. Nutr Metab Cardiovasc Dis, 2021, 31(1): 193-200.
25 RASMUSSEN V F, VESTERGAARD E T, HEJLESEN O, et al. Prevalence of taste and smell impairment in adults with diabetes: a cross-sectional analysis of data from the National Health and Nutrition Examination Survey (NHANES)[J]. Prim Care Diabetes, 2018, 12(5): 453-459.
26 KAYA K S, MAZ? E E, DEMIR S T, et al. Relationship between progression of type 2 diabetes mellitus and olfactory function[J]. Am J Otolaryngol, 2020, 41(2): 102365.
27 MOZZANICA F, FERRULLI A, VUJOSEVIC S, et al. Olfactory disfunction and diabetic complications in type 2 diabetic patients: a pilot study[J]. Endocrine, 2022, 75(3): 760-767.
28 LI J, LI M Y, ZHANG J J, et al. Associations between taste and smell alterations and diabetes-related comorbidities among US adults: the National Health and Nutrition Examination Surveys 2011?2014[J]. Acta Diabetol, 2022, 59(3): 429-433.
29 BOREL A L. Sleep apnea and sleep habits: relationships with metabolic syndrome[J]. Nutrients, 2019, 11(11): 2628.
30 MAGLIULO G, DE VINCENTIIS M, IANNELLA G, et al. Olfactory evaluation in obstructive sleep apnoea patients[J]. Acta Otorhinolaryngol Ital, 2018, 38(4): 338-345.
31 ARNOLD S E, ARVANITAKIS Z, MACAULEY-RAMBACH S L, et al. Brain insulin resistance in type 2 diabetes and Alzheimer disease: concepts and conundrums[J]. Nat Rev Neurol, 2018, 14(3): 168-181.
32 BOSCO D, PLASTINO M, CRISTIANO D, et al. Dementia is associated with insulin resistance in patients with Parkinson′s disease[J]. J Neurol Sci, 2012, 315(1/2): 39-43.
33 DE LA MONTE S M, WANDS J R. Alzheimer′s disease is type 3 diabetes: evidence reviewed[J]. J Diabetes Sci Technol, 2008, 2(6): 1101-1113.
34 PONSEN M M, STOFFERS D, BOOIJ J, et al. Idiopathic hyposmia as a preclinical sign of Parkinson′s disease[J]. Ann Neurol, 2004, 56(2): 173-181.
35 TAHERI S, MAHMOODI M, OPACKA-JUFFRY J, et al. Distribution and quantification of immunoreactive orexin A in rat tissues[J]. FEBS Lett, 1999, 457(1): 157-161.
36 ZAGHLOUL H, PALLAYOVA M, AL-NUAIMI O, et al. Association between diabetes mellitus and olfactory dysfunction: current perspectives and future directions[J]. Diabet Med, 2018, 35(1): 41-52.
37 KOSSE C, GONZALEZ A, BURDAKOV D. Predictive models of glucose control: roles for glucose-sensing neurones[J]. Acta Physiol, 2015, 213(1): 7-18.
38 POESSEL M, FREIHERR J, WIENCKE K, et al. Insulin resistance is associated with reduced food odor sensitivity across a wide range of body weights[J]. Nutrients, 2020, 12(8): 2201.
39 FIGLEWICZ D P, IKEDA H, HUNT T R, et al. Brain insulin binding is decreased in Wistar Kyoto rats carrying the 'fa' gene[J]. Peptides, 1986, 7(1): 61-65.
40 EDWIN THANARAJAH S, HOFFSTALL V, RIGOUX L, et al. The role of insulin sensitivity and intranasally applied insulin on olfactory perception[J]. Sci Rep, 2019, 9(1): 7222.
41 MURATA K, KINOSHITA T, FUKAZAWA Y, et al. GABAergic neurons in the olfactory cortex projecting to the lateral hypothalamus in mice[J]. Sci Rep, 2019, 9(1): 7132.
42 VáRKONYI T, K?REI A, PUTZ Z, et al. Olfactory dysfunction in diabetes: a further step in exploring central manifestations of neuropathy?[J]. Angiology, 2014, 65(10): 857-860.
43 DUDA-SOBCZAK A, ARASZKIEWICZ A, URBAS M, et al. Impaired olfactory function is related to the presence of neuropathy in adults with type 1 diabetes[J]. Diab Vasc Dis Res, 2017, 14(2): 139-143.
44 PALOUZIER-PAULIGNAN B, LACROIX M C, AIMé P, et al. Olfaction under metabolic influences[J]. Chem Senses, 2012, 37(9): 769-797.
45 FERNANDEZ-GARCIA J C, ALCAIDE J, SANTIAGO-FERNANDEZ C, et al. An increase in visceral fat is associated with a decrease in the taste and olfactory capacity[J]. PLoS One, 2017, 12(2): e0171204.
46 UYGUN B, KIYICI S, OZMEN S, et al. The association between olfaction and taste functions with serum ghrelin and leptin levels in obese women[J]. Metab Syndr Relat Disord, 2019, 17(9): 452-457.
47 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[J]. Endocrine, 2016, 51(2): 256-267.
48 MUTLU A S, GAO S M, ZHANG H N, et al. Olfactory specificity regulates lipid metabolism through neuroendocrine signaling in Caenorhabditis elegans[J]. Nat Commun, 2020, 11(1): 1450.
49 FAN Y, PEDERSEN O. Gut microbiota in human metabolic health and disease[J]. Nat Rev Microbiol, 2021, 19(1): 55-71.
50 WONG A C N, WANG Q P, MORIMOTO J, et al. Gut microbiota modifies olfactory-guided microbial preferences and foraging decisions in Drosophila[J]. Curr Biol, 2017, 27(15): 2397-2404.e4.
51 FRAN?OIS A, GREBERT D, RHIMI M, et al. Olfactory epithelium changes in germfree mice[J]. Sci Rep, 2016, 6: 24687.
52 NAUDON L, FRAN?OIS A, MARIADASSOU M, et al. First step of odorant detection in the olfactory epithelium and olfactory preferences differ according to the microbiota profile in mice[J]. Behav Brain Res, 2020, 384: 112549.
53 O'DONNELL M P, FOX B W, CHAO P H, et al. A neurotransmitter produced by gut bacteria modulates host sensory behaviour[J]. Nature, 2020, 583(7816): 415-420.
54 CANI P D, BIBILONI R, KNAUF C, et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice[J]. Diabetes, 2008, 57(6): 1470-1481.
55 BIESSELS G J, DESPA F. Cognitive decline and dementia in diabetes mellitus: mechanisms and clinical implications[J]. Nat Rev Endocrinol, 2018, 14(10): 591-604.
56 TANAKA H, GOURLEY D D, DEKHTYAR M, et al. Cognition, brain structure, and brain function in individuals with obesity and related disorders[J]. Curr Obes Rep, 2020, 9(4): 544-549.
57 JUNG H J, SHIN I S, LEE J E. Olfactory function in mild cognitive impairment and Alzheimer′s disease: a meta-analysis[J]. Laryngoscope, 2019, 129(2): 362-369.
58 SANKE H, MITA T, YOSHII H, et al. Relationship between olfactory dysfunction and cognitive impairment in elderly patients with type 2 diabetes mellitus[J]. Diabetes Res Clin Pract, 2014, 106(3): 465-473.
59 YULUG B, SAATCI O, I?IKLAR A, et al. The association between HbA1c levels, olfactory memory and cognition in normal, pre-diabetic and diabetic persons[J]. Endocr Metab Immune Disord Drug Targets, 2020, 20(2): 198-212.
60 SANKE H, MITA T, YOSHII H, et al. Olfactory dysfunction predicts the development of dementia in older patients with type 2 diabetes[J]. Diabetes Res Clin Pract, 2021, 174: 108740.
61 MARTINS I V A, RIVERS-AUTY J, ALLAN S M, et al. Mitochondrial abnormalities and synaptic loss underlie memory deficits seen in mouse models of obesity and Alzheimer′s disease[J]. J Alzheimers Dis, 2017, 55(3): 915-932.
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