The COVID-19 Pandemic: Impact on Oral Health

The COVID-19 Pandemic: Impact on Oral Health

COVID-19 was declared a global emergency on January 30, 2020, by the World Health Organization.1Zarocostas J. What next for the coronavirus response? Lancet. 2020;395(10222):401. The subsequent pandemic was announced in March 2020, disrupted life as we knew it, and has resulted in devastating consequences to health and societies.2WHO. Coronavirus disease (COVID-19) Weekly Epidemiological Update and Weekly Operational Update. Available at: https://www.who.int/emergencies/diseases/novel-coronavirus-2019/situation-reports. The impact of COVID-19 on oral health was also reported shortly after the pandemic began. Dysgeusia (loss of taste) became recognized as one of the first symptoms of COVID-19, and first oral symptom, in a significant number of patients.3Agyeman AA, Chin KL, Landersdorfer CB, et al. Smell and Taste Dysfunction in Patients With COVID-19: A Systematic Review and Meta-analysis. Mayo Clin Proc 2020;95(8):1621-31. doi:10.1016/j.mayocp.2020.05.030. Since then, reports have addressed the impact of COVID-19 on the oral health of infected individuals and suffering from symptomatic disease, and medication-related adverse effects. Additionally, an association has been proposed for periodontal disease and COVID-19. The longer-term impact on oral health is now also being reported as societies are reopening, including the effect of reduced access to care or desire to seek care during the pandemic. In this article, we will look at findings and implications for oral health.

Oral manifestations in patients with COVID-19

Initially, fever, dry cough, dyspnea, myalgia, and gastrointestinal upsets were recognized as signs and symptoms of COVID-19.3Agyeman AA, Chin KL, Landersdorfer CB, et al. Smell and Taste Dysfunction in Patients With COVID-19: A Systematic Review and Meta-analysis. Mayo Clin Proc 2020;95(8):1621-31. doi:10.1016/j.mayocp.2020.05.030.^,4Rothan H A, Byrareddy S N. The epidemiology and pathogenesis of coronavirus disease (COVID-19) outbreak. J Autoimmun 2020; doi:10.1016/j.jaut.2020.102433. It was soon realized that taste and/or smell dysfunction (loss or absence of) and other symptoms are possible. (Table 1) In a systematic review published in August 2020 with more than 8000 patients with confirmed COVID-19 across 24 studies, it was concluded that 38% and 41% of patients, respectively, experienced taste and smell dysfunction.3Agyeman AA, Chin KL, Landersdorfer CB, et al. Smell and Taste Dysfunction in Patients With COVID-19: A Systematic Review and Meta-analysis. Mayo Clin Proc 2020;95(8):1621-31. doi:10.1016/j.mayocp.2020.05.030. In a second systematic review with 31 studies, taste dysfunction occurred in 45% of patients overall, with symptoms including loss of taste, reduced taste sensation and other taste disturbances.5Amorim Dos Santos J, Normando AGC, Carvalho da Silva RL, et al. Oral manifestations in patients with COVID-19: a living systematic review. J Dent Res 2021;100:141-154. https://doi.org/10.1177/0022034520957289. Furthermore, in a recent cross-sectional study, it was found that more than 50% of patients with COVID-19 experienced smell or taste dysfunction.6Pérula de Torres LÁ, González-Lama J, Jiménez García C, et al; EPICOVID Collaborative Group. Frequency and predictive validity of olfactory and taste dysfunction in patients with SARS-CoV-2 infection. Med Clin (Engl Ed) 2021;156(12):595-601. doi: 10.1016/j.medcle.2020.12.024. It is also suggested that these manifestations may offer predictive value for COVID-19 infection. The reasons for dysgeusia are still not clear, while there are several hypotheses.7Samaranayake L, Fakhruddin KS, Bandara N. Oral Manifestations of Coronavirus Disease 2019 (COVID-19): An Overview. Dental Update May 2021;48:5. Available at: https://doi.org/10.12968/denu.2021.48.5.418. These include targeting by the SARS-CoV-2 virus of the many ACE-2 receptors in salivary glands and taste buds, with SARS-CoV-2 entering the body after its spike protein binds to ACE-2 receptors. (Figure 1) Other hypotheses include a neurological impact, damage to chemoreceptors, and an inflammatory response when the virus enters taste bud epithelial cells.7Samaranayake L, Fakhruddin KS, Bandara N. Oral Manifestations of Coronavirus Disease 2019 (COVID-19): An Overview. Dental Update May 2021;48:5. Available at: https://doi.org/10.12968/denu.2021.48.5.418.

Dry mouth: Salivary flow and quality
Dry mouth is one of the initial symptoms that may occur with COVID-19 infection.8Chen L, Zhao J, Peng J, et al. Detection of SARS-CoV-2 in saliva and characterization of oral symptoms in COVID-19 patients. Cell Prolif 2020 Dec;53(12):e12923. doi: 10.1111/cpr.12923. (Table 1) Salivary gland dysfunction, causing both reduced salivary flow and reduced salivary quality, is reported. This is believed to be the result of SARS-CoV-2 entering the salivary glands by binding to the high level of ACE-2 receptors present.7Samaranayake L, Fakhruddin KS, Bandara N. Oral Manifestations of Coronavirus Disease 2019 (COVID-19): An Overview. Dental Update May 2021;48:5. Available at: https://doi.org/10.12968/denu.2021.48.5.418. Dry mouth associated with COVID-19 may also be related to systemic inflammation, a neurological pathway, a hyperinflammatory response or cardiovascular dysfunction.9Gherlone EF, Polizzi E, Tetè G, et al. Frequent and Persistent Salivary Gland Ectasia and Oral Disease After COVID-19. Journal of Dental Research. 2021;100(5):464-471. doi:10.1177/0022034521997112. In two studies, 32% and 45% of patients with COVID-19 experienced dry mouth.10Freni F, Meduri A, Gazia F, et al. Symptomatology in head and neck district in coronavirus disease (COVID-19): A possible neuroinvasive action of SARS-CoV-2. Am J Otolaryngol 2020;41(5):102612. doi: 10.1016/j.amjoto.2020.102612. ^,11Fantozzi PJ, Pampena E, Di Vanna D, et al. Xerostomia, gustatory and olfactory dysfunctions in patients with COVID-19. Am J Otolaryngol 2020;41(6),102721. doi: 10.1016/j.amjoto.2020.102721. In addition, sialadenitis (salivary gland infection) was found to be a possible early manifestation of COVID-19 and it is suggested that chronic sialadenitis may occur following recovery from COVID-19.12Chern A, Famuyide AO, Moonis G, Lalwani AK. Sialadenitis: a possible early manifestation of COVID-19. Laryngoscope 2020;130(111):2595-2597. doi:10.1002/lary.29083.^,13Wang C, Wu H, Ding X, et al. Does infection of 2019 novel coronavirus cause acute and/or chronic sialadenitis? Med Hypotheses 2020;140:109789. doi:10.1016/j.mehy.2020.109789. Medications used to treat COVID-19 include drugs with dry mouth as a side effect, including agents such as remdesivir, other anti-viral agents, and interferons with some extending dry mouth after recovery from COVID-19.14Dziedzic A, Wojtyczka R. The impact of coronavirus infectious disease 19 (COVID-19) on oral health. Oral Dis 2020;27(S3):703-706. In addition, oral health suffers in patients in intensive care units.

Other Oral manifestations
In one article on findings in more than 650 patients in a Spanish field hospital, temporary glossitis was reported in a quarter of patients, while papillitis, glossitis with scalloping and aphthous stomatitis was reported in 11.5%, 6.6% and 6.9% of patients.15Nuno-Gonzalez A, Martin-Carrillo P, Magaletsky K, et al. Prevalence of mucocutaneous manifestations in 666 patients with COVID-19 in a field hospital in Spain: oral and palmoplantar findings. Br J Dermatol 2021;184(1):184-185. doi:10.1111/bjd.19564. Other less frequent complaints included mucositis and ‘burning mouth.’ While reports from dental professionals have noted oral manifestations on the tongue potentially associated with COVID-19, it is also acknowledged that these may not be related to COVID-19 since they are not uncommon and more research is needed on the potential association with COVID-19.16American Dental Association. Trio of organizations agree more research needed on COVID-19’s effect on oral health. ADA News, February 2021. Available at: https://www.ada.org/en/publications/ada-news/2021-archive/february/research-needed-on-covid-effect-on-oral-health. Other reported oral manifestations include but are not limited to ulcers, vesicle and bullous formation, herpetiform and aphthous-like lesions, and spontaneous bleeding.7Samaranayake L, Fakhruddin KS, Bandara N. Oral Manifestations of Coronavirus Disease 2019 (COVID-19): An Overview. Dental Update May 2021;48:5. Available at: https://doi.org/10.12968/denu.2021.48.5.418. (Table 1) These seem to occur more frequently in older patients.

Societal Impact of COVID-19, Mental Health and Oral Conditions

COVID-19 severely impacted both societal and economic conditions, with isolation, physical distancing, and the disruption of everyday life.17National Institute of Mental Health. One Year In: COVID-19 and Mental Health, April 9, 2021. Available at: https://www.nimh.nih.gov/about/director/messages/2021/one-year-in-covid-19-and-mental-health. This has resulted in impaired mental health, with individuals experiencing stress, anxiety, depression and insomnia.17National Institute of Mental Health. One Year In: COVID-19 and Mental Health, April 9, 2021. Available at: https://www.nimh.nih.gov/about/director/messages/2021/one-year-in-covid-19-and-mental-health. ^,18Berg-Weger M, Morley JE. Editorial: Loneliness and Social Isolation in Older Adults during the COVID-19 Pandemic: Implications for Gerontological Social Work. J Nutr Health Aging 2020;24(5):456-458. doi:10.1007/s12603-020-1366-8.^,19Ettman CK, Abdalla SM, Cohen GH, et al. Prevalence of Depression Symptoms in US Adults Before and During the COVID-19 Pandemic. JAMA Netw Open 2020;3(9):e2019686. doi:10.1001/jamanetworkopen.2020.19686. Stress in and of itself can result in negative emotions, appetite changes, cause physical reactions, difficulty sleeping and concentrating, and worsening of chronic health and mental health problems.20CDC. COVID-19. Coping with Stress. Available at: https://www.cdc.gov/coronavirus/2019-ncov/daily-life-coping/managing-stress-anxiety.html. By the end of June 2020, it was estimated that the number of individuals in the US surveyed who reported anxiety/depression, stress-related disorders and suicidal ideation had increased two-fold, reaching 31%, 26% and 11%, respectively.21Czeisler MÉ , Lane RI, Petrosky E, et al. Mental Health, Substance Use, and Suicidal Ideation During the COVID-19 Pandemic — United States, June 24–30, 2020. MMWR Morb Mortal Wkly Rep 2020;69:1049-1057. doi: http://dx.doi.org/10.15585/mmwr.mm6932a1. (Figure 2) In addition, increased use of substances such as alcohol and tobacco and substance abuse can occur.20CDC. COVID-19. Coping with Stress. Available at: https://www.cdc.gov/coronavirus/2019-ncov/daily-life-coping/managing-stress-anxiety.html. Older adults have also been disproportionately affected by the pandemic.22Kasar KS, Karaman E. Life in lockdown: Social isolation, loneliness and quality of life in the elderly during the COVİD-19 pandemic: A scoping review. Ger Nursing 2021;ISSN 0197-4572. https://doi.org/10.1016/j.gerinurse.2021.03.010. The pandemic has also resulted in more severe mental illness in those already experiencing impaired mental health.17National Institute of Mental Health. One Year In: COVID-19 and Mental Health, April 9, 2021. Available at: https://www.nimh.nih.gov/about/director/messages/2021/one-year-in-covid-19-and-mental-health. Impaired mental health as a result of the pandemic has resulted in increased use of anti-depressants, anxiolytics, other medications, and alcohol misuse.23WHO. Mental health & COVID-19. Available at: https://www.who.int/teams/mental health-and-substance-use/covid-19.^,24Rabeea SA, Merchant HA, Khan MU, et al. Surging trends in prescriptions and costs of antidepressants in England amid COVID-19. Daru 2021;29(1):217-221. doi:10.1007/s40199-021-00390-z.^,25Pesce NL. Anti-anxiety medication prescriptions have spiked 34% during the coronavirus pandemic. May 26, 2020. Available at: https://www.marketwatch.com/story/anti-anxiety-medication-prescriptions-have-spiked-34-during-the-coronavirus-pandemic-2020-04-16.^,26Hendrie D. Anxiety and depression medication rates spike amid ongoing uncertainty. July 8, 2020. Available at: https://www1.racgp.org.au/newsgp/clinical/use-of-anxiety-and-depression-medication-spikes-as

Dry mouth is a common side effect for medications, including anti-depressants, anxiolytics and sleep medication.27Scully C. Drug effects on salivary glands: Dry mouth. Oral Dis 2003;9:165-176. Stress may also cause dry mouth.28Gholami N, Hosseini Sabzvari B, Razzaghi A, Salah S. Effect of stress, anxiety and depression on unstimulated salivary flow rate and xerostomia. J Dent Res Dent Clin Dent Prospects 2017;11(4):247-52. doi:10.15171/joddd.2017.043. Individuals with dry mouth experience discomfort and an increased risk for dental caries, dental erosion, oral infections and halitosis.29Amerongen AN, Veerman E. Saliva – the defender of the oral cavity. Oral Dis 2002;8:12-22. https://doi.org/10.1034/j.1601-0825.2002.1o816.x. In addition, a risk of dry mouth has been noted in association with mouth breathing and reduced fluid intake when wearing masks for extended periods of time. Reports have also noted an increase in bruxism among patients since the pandemic began, associated with stress, with a higher occurrence of clenching, grinding and cracked teeth.30Chen T. A dentist sees more cracked teeth. What’s going on? The New York Times. September 11, 2020. Accessed December 20, 2020. https://www.nytimes.com/2020/09/08/well/live/dentists-tooth-teeth-cracks-fractures-coronavirus-stress-grinding.html.^,31Dadnam C, Dadnam D, Al-Safar H. Pandemic bruxism. Letters to the Editor. Br Dent J 2021;230(5):271.^,32Emodi-Perlman A, Eli I, Smardz J, et al. Temporomandibular disorders and bruxism outbreak as a possible factor of orofacial pain worsening during the COVID-19 pandemic – concomitant research in two countries. J Clin Med 2020;9:3250. A higher incidence of temporomandibular joint disorder has also been reported.32Emodi-Perlman A, Eli I, Smardz J, et al. Temporomandibular disorders and bruxism outbreak as a possible factor of orofacial pain worsening during the COVID-19 pandemic – concomitant research in two countries. J Clin Med 2020;9:3250.

Periodontitis and COVID-19

Recent reports have highlighted potential associations between periodontal and mucosal conditions, and the occurrence and severity of COVID-19.33ADA. COVID-19 and Oral Health Conditions, February 12, 2021. Available at: https://www.ada.org/en/press-room/news-releases/2021-archives/february/covid-19-and-oral-health-conditions. In a case-control study conducted between February and July 2020 using Qatari national electronic health records for more than 500 patients, the potential relationship between severe COVID-19 complications and periodontitis was evaluated.34Marouf N, Cai W, Said KN, et al. Association between periodontitis and severity of COVID-19 infection: A case–control study. J Clin Periodontol 2021;48(4):483-491. Available at: https://onlinelibrary.wiley.com/doi/10.1111/jcpe.13435. Compared to patients released without severe COVID-19 complications, the risk of severe complications (including death) was eight-fold for individuals with periodontitis, and more than three- and four-fold respectively for admission to an intensive care unit (ICU) and assisted ventilation. (Figure 3) In addition, inflammatory markers were higher in this patient cohort. It was concluded that periodontitis may be a risk factor for severe COVID-19, and the importance of a healthy periodontium was highlighted by the results.34Marouf N, Cai W, Said KN, et al. Association between periodontitis and severity of COVID-19 infection: A case–control study. J Clin Periodontol 2021;48(4):483-491. Available at: https://onlinelibrary.wiley.com/doi/10.1111/jcpe.13435.

Figure 3. Increase in risk for patients with periodontitis34Marouf N, Cai W, Said KN, et al. Association between periodontitis and severity of COVID-19 infection: A case–control study. J Clin Periodontol 2021;48(4):483-491. Available at: https://onlinelibrary.wiley.com/doi/10.1111/jcpe.13435.

Severe complications (8-fold)
Assisted ventilation (4-fold)
ICU admission (3-fold)

In a second study, the UK BioBank database was used to obtain data on patients who had taken COVID-19 tests between March and June 2020.35Larvin H, Wilmott S, Wu J, Kang J. The Impact of Periodontal Disease on Hospital Admission and Mortality During COVID-19 Pandemic. Front Med (Lausanne) 2020;7:604980. doi: 10.3389/fmed.2020.604980. Of these individuals, more than 1600 were positive for COVID-19. In this study, an almost two-fold risk (OR 1.71) for death was found for patients who had self-reported painful or bleeding gums. However, no increase in risk compared to COVID-negative patients was found for individuals reporting loose teeth. It was concluded that while there was not sufficient evidence for a link to risk of infection, there was a higher mortality rate. Some limitations of this study were self-reporting of signs and symptoms associated with periodontal disease, as well as no findings on causality.35Larvin H, Wilmott S, Wu J, Kang J. The Impact of Periodontal Disease on Hospital Admission and Mortality During COVID-19 Pandemic. Front Med (Lausanne) 2020;7:604980. doi: 10.3389/fmed.2020.604980.

Several theories are proposed for a potential association between periodontitis and severity of COVID-19. High levels of interleukin-6 (IL-6) and other pro-inflammatory mediators are believed to play a role in the severity of COVID-19 by creating a cytokine storm.34Marouf N, Cai W, Said KN, et al. Association between periodontitis and severity of COVID-19 infection: A case–control study. J Clin Periodontol 2021;48(4):483-491. Available at: https://onlinelibrary.wiley.com/doi/10.1111/jcpe.13435. ^,36Molayem S, Pontes CC. The Mouth-COVID Connection: IL-6 Levels in Periodontal Disease ― Potential Role in COVID-19-Related Respiratory Complications. Calif Dent Assoc J, October 2020. Available at: https://issuu.com/cdapublications/docs/cdapubs_journal_2020_october/s/11067174. Treatment for COVID-19 has also included immunosuppression using monoclonal antibody therapy to target the IL-6 receptor.14Dziedzic A, Wojtyczka R. The impact of coronavirus infectious disease 19 (COVID-19) on oral health. Oral Dis 2020;27(S3):703-706. In addition, it is suggested that the oral bacterial load may result in bronchial and systemic co-infection and may influence outcomes for COVID-19 infection in patients with periodontitis.35Larvin H, Wilmott S, Wu J, Kang J. The Impact of Periodontal Disease on Hospital Admission and Mortality During COVID-19 Pandemic. Front Med (Lausanne) 2020;7:604980. doi: 10.3389/fmed.2020.604980.^,37Sampson V, Kamona N, Sampson A. Could there be a link between oral hygiene and the severity of SARS-CoV-2 infections?. Br Dent J 2020;228:971-975. https://doi.org/10.1038/s41415-020-1747-8.

Implications for Oral Care

Given the initial findings on a potential association between periodontitis and the severity of COVD-19, oral hygiene interventions have been recommended to reduce the intraoral bacterial load and inflammatory response, and periodontal care to decrease IL-6 levels.34Marouf N, Cai W, Said KN, et al. Association between periodontitis and severity of COVID-19 infection: A case–control study. J Clin Periodontol 2021;48(4):483-491. Available at: https://onlinelibrary.wiley.com/doi/10.1111/jcpe.13435. Dental professionals can advise patients on the potential relationship as well as the confirmed associations for periodontal disease and other systemic disease and emphasize oral hygiene measures. Twice-daily brushing with an antimicrobial toothpaste, daily interdental cleaning and the use of antimicrobial mouth rinses can be recommended. In addition, the need for treatment should be communicated in the case of individuals with periodontal disease. For individuals at increased risk of disease due to substance abuse, advice can include counselling on alcohol/drug use and, as necessary, a referral should be provided.

The findings in several studies related to patients with COVID-19 as well as the psychological impact of the pandemic show an increased risk for oral disease. For patients with oral manifestations of COVID-19, depending on the lesions, management may include use of antimicrobial rinses, corticosteroids and other medications.7Samaranayake L, Fakhruddin KS, Bandara N. Oral Manifestations of Coronavirus Disease 2019 (COVID-19): An Overview. Dental Update May 2021;48:5. Available at: https://doi.org/10.12968/denu.2021.48.5.418. However, it should be noted that it is not yet known whether antimicrobial rinses actually reduce the impact and frequency of oral manifestations.7Samaranayake L, Fakhruddin KS, Bandara N. Oral Manifestations of Coronavirus Disease 2019 (COVID-19): An Overview. Dental Update May 2021;48:5. Available at: https://doi.org/10.12968/denu.2021.48.5.418. An increased risk for dry mouth occurs as a result of COVID-19, treatment for COVID-19, and with the use of anti-depressant and other medications used to manage mental health impairment associated with the pandemic. Patients should be counselled on the risks to oral health and provided with recommendations on saliva substitutes and advice on other methods to relieve discomfort associated with dry mouth.38American Dental Association. Oral Health Topics. Xerostomia (Dry Mouth). Available at: https://www.ada.org/en/member-center/oral-health-topics/xerostomia#:~:text=The%20ADA%20Seal%20of%20Acceptance,symptoms%2C%20when%20used%20as%20directed. In addition, due to the increased risk for dental caries and dental erosion, periodic in-office application of 5% sodium fluoride varnish and home use of high-level prescription fluoride pastes can be recommended.39Weyant RJ, Tracy SL, Anselmo TT, et al; American Dental Association Council on Scientific Affairs Expert Panel on Topical Fluoride Caries Preventive Agents. Topical fluoride for caries prevention: executive summary of the updated clinical recommendations and supporting systematic review. J Am Dent Assoc 2013;144(11):1279-1291. doi: 10.14219/jada.archive.2013.0057.^,40Magalhães AC, Wiegand A, Rios D, Buzalaf MAR, Lussi A. Fluoride in dental erosion. Monogr Oral Sci 2011;22:158-170. doi: 10.1159/000325167. Risk for bruxism and tooth fracture should also be determined,31Dadnam C, Dadnam D, Al-Safar H. Pandemic bruxism. Letters to the Editor. Br Dent J 2021;230(5):271. with advice and treatment provided for affected individuals.

Conclusions

The COVID-19 pandemic has impacted oral health in individuals with and without COVID-19 infection. More research is needed on the potential link between periodontitis and COVID-19, causality, and on the effect of periodontal treatment.34Marouf N, Cai W, Said KN, et al. Association between periodontitis and severity of COVID-19 infection: A case–control study. J Clin Periodontol 2021;48(4):483-491. Available at: https://onlinelibrary.wiley.com/doi/10.1111/jcpe.13435. ^,35Larvin H, Wilmott S, Wu J, Kang J. The Impact of Periodontal Disease on Hospital Admission and Mortality During COVID-19 Pandemic. Front Med (Lausanne) 2020;7:604980. doi: 10.3389/fmed.2020.604980. In addition, research is needed on the management of oral complications of COVID-19, notably oral manifestations.7Samaranayake L, Fakhruddin KS, Bandara N. Oral Manifestations of Coronavirus Disease 2019 (COVID-19): An Overview. Dental Update May 2021;48:5. Available at: https://doi.org/10.12968/denu.2021.48.5.418. In the meantime, dental professionals can reassure patients on the safety of dental care and educate patients on potential complications to oral health and the potential association between periodontal disease and COVID-19 severity. An assessment of risk for oral disease informs recommendations for preventive care, while patients should be encouraged to perform thorough oral hygiene and to receive indicated treatment.

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