COVID-19 Induced Taste Dysfunction and Recovery: Association with Smell Dysfunction and Oral Health Behaviour

Georgia Catton, Alexander Gardner, Georgia Catton, Alexander Gardner

Abstract

Background and Objectives: Disruption to taste and smell are common symptoms of COVID-19 infection. The current literature overlooks taste symptoms and tends to focus on the sense of smell. Persisting cases (>28 days) of taste dysfunction are increasingly recognised as a major future healthcare challenge. This study focuses on the severity and recovery of COVID-19 induced taste loss and association with olfactory symptoms, lifestyle and oral health factors. Materials and Methods: This study was a cross-sectional survey comparing 182 rapid taste recovery participants (≤28 days) with 47 participants with prolonged taste recovery >28 days. Analyses of taste loss in association with smell loss, age, sex, illness severity, diet, BMI, vitamin-D supplementation, antidepressants, alcohol use, smoking, brushing frequency, flossing, missing teeth, appliances and number of dental restorations were conducted. Differences in the severity of the loss of sour, sweet, salt, bitter and umami tastes were explored. Results: Both the severity and the duration of taste and smell loss were closely correlated (p < 0.001). Salt taste was significantly less affected than all other taste qualities (p < 0.001). Persisting taste loss was associated with older age (mean ± 95% CI = 31.73 ± 1.23 years vs. 36.66 ± 3.59 years, p < 0.001) and reduced likelihood of using floss (odds ratio ± 95% CI = 2.22 (1.15−4.25), p = 0.047). Conclusions: Smell and taste loss in COVID-19 are closely related, although a minority of individuals can experience taste or smell dysfunction in the absence of the other. The taste of salt may be less severely affected than other taste qualities and future work exploring this finding objectively is indicated. The association of flossing with rapid taste recovery adds to the growing evidence of a link between good periodontal health and favourable COVID-19 outcomes.

Keywords: COVID-19; dental care; oral health; taste dysfunction.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Comparison of total publications on either smell or taste loss and COVID-19 infection since the pandemic began. Data generated by searching the Web of Science using the terms “COVID taste OR COVID gustatory NOT smell NOT olfactory” and “COVID smell OR COVID olfactory NOT taste NOT gustatory” in the title field.
Figure 2
Figure 2
(a) Bubble plot showing the relationship between taste and smell loss severity, n = 421. (b) Plot indicating the differential time for resolution of taste and smell loss, n = 207. (c) Recovery curve for both taste and smell loss, n = 207.
Figure 3
Figure 3
Comparison of intensity of taste sensation loss for the five primary taste modalities. p-values are for Friedman test with Bonferroni-adjusted post hoc pairwise comparisons between all groups, n = 384.

References

    1. Menni C., Valdes A.M., Freidin M.B., Ganesh S., El-Sayed Moustafa J.S., Visconti A., Hysi P., Bowyer R.C.E., Mangino M., Falchi M., et al. Loss of smell and taste in combination with other symptoms is a strong predictor of COVID-19 infection. medRxiv. 2020 doi: 10.1101/2020.04.05.20048421.
    1. Sudre C.H., Keshet A., Graham M.S., Joshi A.D., Shilo S., Rossman H., Murray B., Molteni E., Klaser K., Canas L.D. Anosmia, ageusia, and other COVID-19-like symptoms in association with a positive SARS-CoV-2 test, across six national digital surveillance platforms: An observational study. Lancet Digit. Health. 2021;3:e577–e586. doi: 10.1016/S2589-7500(21)00115-1.
    1. George B., McGee J., Giangrasso E., Finkelstein S., Wu S., Glatt A.E. What Is the Predictive Value of a Single Nasopharyngeal SARS-CoV-2 PCR Swab Test in a Patient With COVID-Like Symptoms and/or Significant COVID-19 Exposure? Open Forum Infect. Dis. 2020;7:ofaa399. doi: 10.1093/ofid/ofaa399.
    1. Haehner A., Draf J., Dräger S., de With K., Hummel T. Predictive Value of Sudden Olfactory Loss in the Diagnosis of COVID-19. ORL J. Otorhinolaryngol. Relat. Spec. 2020;82:175–180. doi: 10.1159/000509143.
    1. Sedaghat A.R., Gengler I., Speth M.M. Olfactory Dysfunction: A Highly Prevalent Symptom of COVID-19 With Public Health Significance. Otolaryngol. Neck Surg. 2020;163:12–15. doi: 10.1177/0194599820926464.
    1. Callejon-Leblic M.A., Moreno-Luna R., Del Cuvillo A., Reyes-Tejero I.M., Garcia-Villaran M.A., Santos-Peña M., Maza-Solano J.M., Martín-Jimenez D.I., Palacios-Garcia J.M., Fernandez-Velez C., et al. Loss of Smell and Taste Can Accurately Predict COVID-19 Infection: A Machine-Learning Approach. J. Clin. Med. 2021;10:570. doi: 10.3390/jcm10040570.
    1. Lechien J.R., Chiesa-Estomba C.M., Hans S., Barillari M.R., Jouffe L., Saussez S. Loss of smell and taste in 2013 European patients with mild to moderate COVID-19. Ann. Intern. Med. 2020;173:672–675. doi: 10.7326/M20-2428.
    1. Lee Y., Min P., Lee S., Kim S.-W. Prevalence and Duration of Acute Loss of Smell or Taste in COVID-19 Patients. J. Korean Med. Sci. 2020;35:e174. doi: 10.3346/jkms.2020.35.e174.
    1. Boscolo-Rizzo P., Tirelli G., Meloni P., Hopkins C., Madeddu G., De Vito A., Gardenal N., Valentinotti R., Tofanelli M., Borsetto D., et al. Coronavirus disease 2019 (COVID-19)-related smell and taste impairment with widespread diffusion of severe acute respiratory syndrome-coronavirus-2 (SARS-CoV-2) Omicron variant. Int. Forum Allergy Rhinol. 2022 doi: 10.1002/alr.22995. Early View .
    1. Gardner A., Carpenter G.H. Anatomical stability of human fungiform papillae and relationship with oral perception measured by salivary response and intensity rating. Sci. Rep. 2019;9:9759. doi: 10.1038/s41598-019-46093-z.
    1. Roper S.D., Chaudhari N. Taste buds: Cells, signals and synapses. Nat. Rev. Neurosci. 2017;18:485. doi: 10.1038/nrn.2017.68.
    1. Gilbertson A.T., Damak S., Margolskee R.F. The molecular physiology of taste transduction. Curr. Opin. Neurobiol. 2000;10:519–527. doi: 10.1016/S0959-4388(00)00118-5.
    1. Pinto J.M. Olfaction. Proc. Am. Thorac. Soc. 2011;8:46–52. doi: 10.1513/pats.201005-035RN.
    1. Kinnamon S.C., Margolskee R. Mechanisms of taste transduction. Curr. Opin. Neurobiol. 1996;6:506–513. doi: 10.1016/S0959-4388(96)80057-2.
    1. Rinaldi A. The scent of life. The exquisite complexity of the sense of smell in animals and humans. EMBO Rep. 2007;8:629–633. doi: 10.1038/sj.embor.7401029.
    1. Bushdid C., Magnasco M.O., Vosshall L.B., Keller A. Humans Can Discriminate More than 1 trillion Olfactory Stimuli. Science. 2014;343:1370–1372. doi: 10.1126/science.1249168.
    1. Castro J.B., Ramanathan A., Chennubhotla C.S. Categorical Dimensions of Human Odor Descriptor Space Revealed by Non-Negative Matrix Factorization. PLoS ONE. 2013;8:e73289. doi: 10.1371/journal.pone.0073289.
    1. Eshraghi A.A., Mirsaeidi M., Davies C., Telischi F.F., Chaudhari N., Mittal R. Potential Mechanisms for COVID-19 Induced Anosmia and Dysgeusia. Front. Physiol. 2020;11:1039. doi: 10.3389/fphys.2020.01039.
    1. Lozada-Nur F., Chainani-Wu N., Fortuna G., Sroussi H. Dysgeusia in COVID-19: Possible Mechanisms and Implications. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. 2020;130:344–346. doi: 10.1016/j.oooo.2020.06.016.
    1. Tsuchiya H. Oral Symptoms Associated with COVID-19 and Their Pathogenic Mechanisms: A Literature Review. Dent. J. 2021;9:32. doi: 10.3390/dj9030032.
    1. Hannum E.M., Ramirez A.V., Lipson S.J., Herriman R.D., Toskala A.K., Lin C., Joseph P.V., Reed D.R. Objective sensory testing methods reveal a higher prevalence of olfactory loss in COVID-19–positive patients compared to subjective methods: A systematic review and meta-analysis. Chem. Senses. 2020;45:865–874. doi: 10.1093/chemse/bjaa064.
    1. Risso D., Drayna D., Morini G. Alteration, Reduction and Taste Loss: Main Causes and Potential Implications on Dietary Habits. Nutrients. 2020;12:3284. doi: 10.3390/nu12113284.
    1. Printza A., Katotomichelakis M., Valsamidis K., Metallidis S., Panagopoulos P., Panopoulou M., Petrakis V., Constantinidis J. Smell and Taste Loss Recovery Time in COVID-19 Patients and Disease Severity. J. Clin. Med. 2021;10:966. doi: 10.3390/jcm10050966.
    1. Lechien J.R., Journe F., Hans S., Chiesa-Estomba C.M., Mustin V., Beckers E., Vaira L.A., De Riu G., Hopkins C., Saussez S. Severity of anosmia as an early symptom of COVID-19 infection may predict lasting loss of smell. Front. Med. 2020;7:582802. doi: 10.3389/fmed.2020.582802.
    1. Catton G., Gardner A. Relationship between Recovery from COVID-19-Induced Smell Loss and General and Oral Health Factors. Medicina. 2022;58:283. doi: 10.3390/medicina58020283.
    1. Song J., Deng Y.-K., Wang H., Wang Z.-C., Liao B., Ma J., He C., Pan L., Liu Y., Alobid I., et al. Self-reported Taste and Smell Disorders in Patients with COVID-19: Distinct Features in China. Curr. Med. Sci. 2021;41:14–23. doi: 10.1007/s11596-021-2312-7.
    1. Boscolo-Rizzo P., Guida F., Polesel J., Marcuzzo A.V., Antonucci P., Capriotti V., Sacchet E., Cragnolini F., D’Alessandro A., Zanelli E., et al. Self-reported smell and taste recovery in coronavirus disease 2019 patients: A one-year prospective study. Eur. Arch. Oto-Rhino-Laryngol. 2021;279:515–520. doi: 10.1007/s00405-021-06839-w.
    1. Nguyen N.N., Hoang V.T., Lagier J.-C., Raoult D., Gautret P. Long-term persistence of olfactory and gustatory disorders in COVID-19 patients. Clin. Microbiol. Infect. 2021;27:931–932. doi: 10.1016/j.cmi.2020.12.021.
    1. Niklassen A.S., Draf J., Huart C., Hintschich C., Bocksberger S., Trecca E.M.C., Klimek L., Le Bon S.D., Altundag A., Hummel T. COVID-19: Recovery from chemosensory dysfunction. a multicentre study on smell and taste. Laryngoscope. 2021;131:1095–1100. doi: 10.1002/lary.29383.
    1. Alwan N.A., Johnson L. Defining long COVID: Going back to the start. Medicine. 2021;2:501–504. doi: 10.1016/j.medj.2021.03.003.
    1. Burges Watson D.L., Campbell M., Hopkins C., Smith B., Kelly C., Deary V. Altered smell and taste: Anosmia, parosmia and the impact of long Covid-19. PLoS ONE. 2021;16:e0256998. doi: 10.1371/journal.pone.0256998.
    1. Alshakhs A., AlMomen A., Alyaeesh I., AlOmairin A., Almutairi A.A., Alammar Z., AlMomen H., AlMomen Z. The Association of Smell and Taste Dysfunction with COVID19, and Their Functional Impacts. Indian J. Otolaryngol. Head Neck Surg. 2021:1–6. doi: 10.1007/s12070-020-02330-w.
    1. Islam M.R. Sample size and its role in Central Limit Theorem (CLT) Comput. Appl. Math. J. 2018;4:1–7.
    1. Ciofalo A., Cavaliere C., Masieri S., Di Chicco A., Fatuzzo I., Re F.L., Baroncelli S., Begvarfaj E., Adduci A., Mezzaroma I., et al. Long-Term Subjective and Objective Assessment of Smell and Taste in COVID-19. Cells. 2022;11:788. doi: 10.3390/cells11050788.
    1. Ali G., Akhter N., Akram R., Kazmi S.A.J., Khan M.S., Iqbal S. The Loss of Smell and Taste in the COVID-19 Outbreak, a Cross Sectional Study. Haya Saudi J. Life Sci. 2022;7:24–28. doi: 10.36348/sjls.2022.v07i01.005.
    1. Cecchetto C., Di Pizio A., Genovese F., Calcinoni O., Macchi A., Dunkel A., Ohla K., Spinelli S., Farruggia M.C., Joseph P.V., et al. Assessing the extent and timing of chemosensory impairments during COVID-19 pandemic. Sci. Rep. 2021;11:17504. doi: 10.1038/s41598-021-96987-0.
    1. Coelho D.H., Reiter E.R., Budd S.G., Shin Y., Kons Z.A., Costanzo R.M. Predictors of smell recovery in a nationwide prospective cohort of patients with COVID-19. Am. J. Otolaryngol. 2021;43:103239. doi: 10.1016/j.amjoto.2021.103239.
    1. Speth M.M., Singer-Cornelius T., Oberle M., Gengler I., Brockmeier S.J., Sedaghat A.R. Olfactory dysfunction and sinonasal symptomatology in COVID-19: Prevalence, severity, timing, and associated characteristics. Otolaryngol. Head Neck Surg. 2020;163:114–120. doi: 10.1177/0194599820929185.
    1. D’Amico C., Bocchieri S., De Stefano R., Gorassini F., Surace G., Amoroso G., Scoglio C., Mastroieni R., Gambino D., Amantia E.M., et al. Dental Office Prevention of Coronavirus Infection. Eur. J. Dent. 2020;14:S146–S151. doi: 10.1055/s-0040-1715923.
    1. Asadi M.M., Shankayi Z., Bahrami F., Mohammadzadeh T., Amini H., Naderi M. Quantitative analysis of taste disorder in COVID-19 patients, the hypersensitivity to salty quality. New Microbes New Infect. 2021;43:100919. doi: 10.1016/j.nmni.2021.100919.
    1. Konstantinidis I., Delides A., Tsakiropoulou E., Maragoudakis P., Sapounas S., Tsiodras S. Short-Term Follow-Up of Self-Isolated COVID-19 Patients with Smell and Taste Dysfunction in Greece: Two Phenotypes of Recovery. ORL J. Otorhinolaryngol. Relat. Spec. 2020;82:295–303. doi: 10.1159/000511436.
    1. Mazzatenta A., Neri G., D’Ardes D., De Luca C., Marinari S., Porreca E., Cipollone F., Vecchiet J., Falcicchia C., Panichi V., et al. Smell and Taste in Severe CoViD-19: Self-Reported vs. Testing. Front. Med. 2020;7:589409. doi: 10.3389/fmed.2020.589409.
    1. Hintschich C.A., Niv M.Y., Hummel T. The taste of the pandemic—Contemporary review on the current state of research on gustation in coronavirus disease 2019 (COVID-19) Int. Forum Allergy Rhinol. 2021;12:210–216. doi: 10.1002/alr.22902.
    1. Santos R.E.A., da Silva M.G., Barbosa D.A.M., Gomes A.L.D.V., Galindo L.C.M., Aragão R.D.S., Ferraz-Pereira K.N. Onset and duration of symptoms of loss of smell/taste in patients with COVID-19: A systematic review. Am. J. Otolaryngol. 2021;42:102889. doi: 10.1016/j.amjoto.2020.102889.
    1. Marouf N., Cai W., Said K.N., Daas H., Diab H., Chinta V.R., Hssain A.A., Nicolau B., Sanz M., Tamimi F. Association between periodontitis and severity of COVID-19 infection: A case-control study. J. Clin. Periodontol. 2021;48:483–491. doi: 10.1111/jcpe.13435.
    1. Kamel A.H.M., Basuoni A., Salem Z.A., AbuBakr N. The impact of oral health status on COVID-19 severity, recovery period and C-reactive protein values. Br. Dent. J. 2021:1–7. doi: 10.1038/s41415-021-2656-1.
    1. Juzikis E., Klimenko J., Žilinskas J., Ivanauskienė E. The effect of new acrylic full removable dentures on food taste. Stomatologija. 2021;23:48–50.
    1. Kaur K., Sculley D., Veysey M., Lucock M., Wallace J., Beckett E.L. Bitter and sweet taste perception: Relationships to self-reported oral hygiene habits and oral health status in a survey of Australian adults. BMC Oral Health. 2021;21:553. doi: 10.1186/s12903-021-01910-8.
    1. Neyraud E., Morzel M. Biological films adhering to the oral soft tissues: Structure, composition, and potential impact on taste perception. J. Texture Stud. 2018;50:19–26. doi: 10.1111/jtxs.12363.
    1. Worthington H.V., MacDonald L., Poklepovic Pericic T., Sambunjak D., Johnson T.M., Imai P., Clarkson J.E. Home use of interdental cleaning devices, in addition to toothbrushing, for preventing and controlling periodontal diseases and dental caries. Cochrane Database Syst. Rev. 2019;4:1–159. doi: 10.1002/14651858.CD012018.pub2.
    1. Quirynen M., Avontroodt P., Soers C., Zhao H., Pauwels M., Van Steenberghe D. Impact of tongue cleansers on microbial load and taste. J. Clin. Periodontol. 2004;31:506–510. doi: 10.1111/j.0303-6979.2004.00507.x.
    1. Hyde R., Feller R., Sharon I. Tongue Brushing, Dentifrice, and Age Effects on Taste and Smell. J. Dent. Res. 1981;60:1730–1734. doi: 10.1177/00220345810600100101.
    1. Matsuda S., Saito T., Yoshida H., Yoshimura H., Sano K. Prevalence of Tongue Cleaning Using a Toothbrush: A Questionnaire Survey in Fukui Prefecture, Japan. BioMed Res. Int. 2019;2019:6320261. doi: 10.1155/2019/6320261.
    1. Madiloggovit J., Chotechuang N., Trachootham D. Impact of self-tongue brushing on taste perception in Thai older adults: A pilot study. Geriatr. Nurs. 2015;37:128–136. doi: 10.1016/j.gerinurse.2015.11.004.
    1. Elibol E., Baran H. The relation between serum D-dimer, ferritin and vitamin D levels, and dysgeusia symptoms, in patients with coronavirus disease 2019. J. Laryngol. Otol. 2021;135:45–49. doi: 10.1017/S0022215120002765.
    1. Cheng W.A., Turner L., Ruiz C.J.M., Tanaka M.L., Congrave-Wilson Z., Lee Y., Jumarang J., Perez S., Peralta A., Pannaraj P.S. Clinical manifestations of COVID-19 differ by age and obesity status. Influ. Other Respir. Viruses. 2021;16:255–264. doi: 10.1111/irv.12918.
    1. Andrews P.J., Pendolino A.L., Ottaviano G., Scarpa B., Grant J., Gaudioso P., Bordin A., Marchese-Ragona R., Leoni D., Cattelan A. Olfactory and taste dysfunction among mild-to-moderate symptomatic COVID-19 positive health care workers: An international survey. Laryngoscope Investig. Otolaryngol. 2020;5:1019–1028. doi: 10.1002/lio2.507.
    1. Henin D., Pellegrini G., Carmagnola D., Attisano G.C.L., Lopez G., Ferrero S., Amendola A., De Angelis D., Tanzi E., Dellavia C. Morphological and Immunopathological Aspects of Lingual Tissues in COVID-19. Cells. 2022;11:1248. doi: 10.3390/cells11071248.
    1. Lyoo K.-S., Kim H.M., Lee B., Che Y.H., Kim S.-J., Song D., Hwang W., Lee S., Park J.-H., Na W. Direct neuronal infection of SARS-CoV-2 reveals cellular and molecular pathology of chemosensory impairment of COVID-19 patients. Emerg. Microbes Infect. 2022;11:406–411. doi: 10.1080/22221751.2021.2024095.
    1. Sinjari B., D’Ardes D., Santilli M., Rexhepi I., D’Addazio G., Di Carlo P., Chiacchiaretta P., Caputi S., Cipollone F. SARS-CoV-2 and Oral Manifestation: An Observational, Human Study. J. Clin. Med. 2020;9:3218. doi: 10.3390/jcm9103218.
    1. Graves R.C., Disney J.A., Stamm J.W. Comparative Effectiveness of Flossing and Brushing in Reducing Interproximal Bleeding. J. Periodontol. 1989;60:243–247. doi: 10.1902/jop.1989.60.5.243.
    1. Carroll G.C., Sebor R.J. Dental Flossing, and Its Relationship to Transient Bacteremia. J. Periodontol. 1980;51:691–692. doi: 10.1902/jop.1980.51.12.691.
    1. Gupta S., Mohindra R., Chauhan P., Singla V., Goyal K., Sahni V., Gaur R., Verma D., Ghosh A., Soni R. SARS-CoV-2 detection in gingival crevicular fluid. J. Dent. Res. 2021;100:187–193. doi: 10.1177/0022034520970536.
    1. Cazzolla A.P., Lovero R., Muzio L.L., Testa N.F., Schirinzi A., Palmieri G., Pozzessere P., Procacci V., Di Comite M., Ciavarella D., et al. Taste and Smell Disorders in COVID-19 Patients: Role of Interleukin-6. ACS Chem. Neurosci. 2020;11:2774–2781. doi: 10.1021/acschemneuro.0c00447.
    1. Shimada Y., Komatsu Y., Ikezawa-Suzuki I., Tai H., Sugita N., Yoshie H. The effect of periodontal treatment on serum leptin, interleukin-6, and C-reactive protein. J. Periodontol. 2010;81:1118–1123. doi: 10.1902/jop.2010.090741.
    1. Attin T., Hornecker E. Tooth brushing and oral health: How frequently and when should tooth brushing be performed? Oral Health Prev. Dent. 2005;3:135–140.
    1. Zimmermann H., Zimmermann N., Hagenfeld D., Veile A., Kim T.-S., Becher H. Is frequency of tooth brushing a risk factor for periodontitis? A systematic review and meta-analysis. Community Dent. Oral Epidemiol. 2014;43:116–127. doi: 10.1111/cdoe.12126.
    1. Saniasiaya J., Islam A., Abdullah B. Prevalence and Characteristics of Taste Disorders in Cases of COVID-19: A Meta-analysis of 29,349 Patients. Otolaryngol. Neck Surg. 2020;165:33–42. doi: 10.1177/0194599820981018.
    1. Seok J., Shim Y.J., Rhee C.-S., Kim J.-W. Correlation between olfactory severity ratings based on olfactory function test scores and self-reported severity rating of olfactory loss. Acta Oto-Laryngol. 2017;137:750–754. doi: 10.1080/00016489.2016.1277782.
    1. Le Bon S.-D., Payen L., Prunier L., Steffens Y., Horoi M., Vaira L.A., Hopkins C., Lechien J.R., Saussez S. Making scents of loss of taste in COVID-19: Is self-reported loss of taste due to olfactory dysfunction? A prospective study using psychophysical testing. Int. Forum Allergy Rhinol. 2021;11:1504–1507. doi: 10.1002/alr.22815.

Source: PubMed

3
Předplatit