Graphical abstract

Introduction

The novel coronavirus disease 2019 (COVID-19) has rapidly evolved into a global crisis, posing a significant challenge to public health due to its swift spread and high mortality rate. Initially identified in December 2019 in China’s Hubei Province, the disease quickly spread across the globe. By March 2020, the World Health Organization (WHO) had declared it a ‘pandemic emergency’. As of April 2023, the outbreak has resulted in over 762,201,169 confirmed cases and 6,893,190 deaths worldwide [1]. The disease’s incubation period spans from 1 to 14 days, with the most frequently observed symptoms being fever, cough, shortness of breath or difficulty breathing, and fatigue. Other less common symptoms, such as headache, loss of taste or smell, sore throat, diarrhea, and nausea or vomiting, may also manifest [2]. The severity of these symptoms can vary greatly among individuals, as it is influenced by factors such as the timing of exposure to the virus, the patient’s age and gender, and any pre-existing health conditions.

Research has shown that the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infiltrates human cells using receptors known as angiotensin-converting enzyme 2 (ACE2) and transmembrane protease serine 2 (also referred to as transmembrane serine protease or TMPRSS2) [3]. Of these 2, the ACE2 receptor is primarily located in the cells of the lungs, liver, kidneys, and gastrointestinal (GI) tract, as well as the salivary glands and the dorsum of the tongue within the oral cavity [4]. These cells, equipped with the receptors, serve as host cells for the virus. The virus penetrates these cells and triggers an inflammatory response in the affected organs [4].

Previously, COVID-19 was not thought to have oral symptoms, unlike other viral rash. However, the subsequent detection of SARS-CoV-2 in patients’ saliva suggested that oral manifestations could indeed be clinical characteristics of the disease [3]. The presence of the ACE2 receptor in specific oral organs, such as the tongue and salivary glands, further supports the potential involvement of the oral cavity in COVID-19 infection [3]. The prevalence of oral manifestations among COVID-19 patients is currently unknown, but several studies have attempted to determine their incidence and prevalence [5−10]. A large-scale study by Nuno-Gonzalez et al. [5] involving 666 patients found oral cavity findings in 25.65% of cases. The most frequently observed oral symptoms, as reported in a case series by Sinadinos and Shelswell [6], were blisters, ulcerations, and desquamative gingivitis. Within the oral cavity, the palate and tongue are the sites most commonly affected by COVID-19, followed by the gums and lips [7]. On the tongue, ulcerations are particularly common, especially on the dorsal surface or sides. However, only 15% of patients develop ulcerations on the ventral surface. Other possible tongue symptoms include multiple pinpoint yellowish ulcers and white plaque [3]. The presence of white plaque on the tongue’s dorsal surface is often due to fungal infections, another common oral manifestation of SARS-CoV-2, likely resulting from reduced immunity. Dima et al. [8] reported a case of a neonate with COVID-19 who developed oral cavity candidiasis. These oral symptoms are often painful, with 75% of patients reporting discomfort [7]. In another study, 25% of patients reported taste impairment, 15% experienced burning sensations, and 20% had difficulty swallowing. Taste disorders were observed in 24% of patients (ageusia), 35% (hypogeusia), and 38% (dysgeusia). These taste disorders were more prevalent in women than in men [9].

It is crucial for dentists to understand the oral manifestations of COVID-19, as this knowledge aids in early disease diagnosis and consequently, prevents transmission. This systematic review aims to summarize the findings from existing literature on the oral manifestations of COVID-19, highlighting the role of the dentist in mitigating the severity of this deadly pandemic.

Materials and Methods

A systematic assessment and description of the currently reported cases and studies related to oral manifestations associated with SARS-CoV-2 infection was conducted. This review adhered to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines [10].

Eligibility Criteria

We conducted a search for clinical evidence in the form of original, peer-reviewed journal articles. These included observational and cross-sectional studies that investigated the prevalence of oral disorders in patients with COVID-19. In addition to these, we also incorporated case reports and case series into our systematic review. The data publication range was restricted from January 1, 2020 to June 30, 2022. We further updated our research on March 31, 2023 across these databases. We did not utilize conference papers, book reviews, book chapters, letters to the editor and replies, newspaper and newsletter articles, expert opinions, or theses and dissertations. Any articles not published in English were also excluded.

Data Sources and Search Strategy

We carried out a comprehensive search of various electronic bibliographic databases, including PubMed, Scopus, Science Direct, and Litcovid. We gathered all articles published between January 1, 2020, and March 31, 2023. We then screened observational cross-sectional, case-control and cohort studies, case reports/series that reported on multisystem inflammatory syndrome in children, as well as letters to the editor. The 2 independent reviewers (A.G. and K.S.) conducted an electronic search of all cross-sectional studies, case reports, and case series up until March 31, 2023. They used a combination of relevant keywords, appropriately linked by Boolean operators. (1) COVID-19 OR SARS-CoV-2 OR Coronavirus disease 2019 OR novel coronavirus; (2) AND oral manifestations OR oral involvement OR oral lesions; (3) AND cross-sectional studies OR case reports OR case series.

Selection Process

The inclusion of studies was done in 2 phases. During the first phase, the titles of all studies were initially screened, followed by a review of their abstracts using the established inclusion and exclusion criteria. Two authors (A.G. and K.S.) independently performed this screening. If a title and abstract appeared to meet the criteria, the full article was then read and assessed for eligibility by these same 2 authors (A.G. and K.S.). Any disagreements between the authors were resolved through discussion and consensus, with the involvement of a third author (A.A.) if necessary. Duplicates were removed and irrelevant articles were excluded from the systematic review. We obtained and evaluated the full-text articles of all potentially relevant studies. In the second phase, we screened the references of all the included studies, case reports, and case series once more to identify any additional potentially eligible studies.

Data Collection

Three authors (A.G., K.S., and A.P.) independently extracted data from the eligible studies. In the event of disagreements, a 4th author (A.A.) was included to facilitate consensus through discussion. We included all studies that reported orofacial manifestations in patients with COVID-19. To systematically review these studies, we assessed the included studies based on demographic details such as author, year, country, study type, sample size, gender, age, study duration, medical history, intensive care unit (ICU) admission, and disease severity. In addition, we recorded details related to oral manifestations, including the affected site, onset of orofacial manifestations, general symptoms, any special investigations conducted, treatment of oral lesions, and disease outcome. The flow diagram for article inclusion is depicted in Figure 1.

Assessment of Risk of Bias of the Included Studies

The Joanna Briggs Institute (JBI) Critical Appraisal Tools for use in systematic reviews of cross-sectional studies, case-control studies, case reports, and case series were used to assess the risk of bias and the individual quality of the selected studies [11]. Each type of study was assessed using its respective checklist, with each question offering 3 possible responses: yes, no, or unclear. Two blinded reviewers (A.G. and K.S.) evaluated the risk of bias in each study, using a scoring system agreed upon by all reviewers. Following the assessment, studies were categorized based on their scores: high bias (if the study scored up to 49% “yes”), moderate bias (if the study scored between 50% and 69% “yes”), and low bias (if the study scored more than 70% “yes”).

Statistical Analysis

Qualitative data were reorganized by grouping and comparing the information reported in the studies. Conditions affecting the oral and mucosal areas were summarized using schematic diagrams. The primary outcome of interest was the prevalence of oral symptoms in COVID-19 patients. The prevalence of oral lesions was categorized into subgroups such as taste alteration, red and white lesions, vesiculobullous lesions, xerostomia, ulceration, burning sensation, and salivary gland disorders. A meta-analysis of the combined prevalence was then conducted using Jamovi ver. 2.3 (2022; https://www.jamovi.org). To evaluate heterogeneity between studies, the I² and Q statistics were utilized, with p-values less than 0.01 considered statistically significant. The analyses were conducted using a random model. Oral lesions in COVID-19 patients, as reported in case reports and case series, were not included in the meta-analysis.

Results

After conducting the initial search, a total of 275 articles were found. Of these, 79 articles were selected for inclusion in the final analysis [5,6,8,9,12−86].

Characteristics of the Studies

The demographic characteristics of the populations in the studies included in our analysis (n=79) are detailed in Table 1. We extracted data from these 79 studies [5,6,8,9,12−86], which encompassed a total of 13,252 patients. The individual sample sizes within these studies varied, ranging from as few as 14 [47] to as many as 1,172 [35] patients. All of the studies (n=79) were published between the years 2020 [6,8,9,12−27,56−69] and 2023 [83−86]. The majority of these studies (n=33) were published in 2020, followed by 2021 (n=31), 2022 (n=15), and 2023 (n=4).

The 79 articles analyzed presented data from various countries worldwide. Italy accounted for the most articles, with 14 studies [16,19,20,22,23,28,29,36,37,58,66,72,81,86]. This was followed by India with 8 studies [17,33,44,45,50,55,80,83], United States with 7 studies [21,25,,30,31,54,62,79], Brazil with 7 studies [9,47,49,52,56,75,77], and both Egypt and Turkey with 5 studies each [34,38,41,68,71] and [26,39,42,48,64], respectively. Iran [5,53,59,60], Iraq [12,43,84,85], and Spain [27,57,65,67] contributed to 4 studies each. Saudi Arabia was represented by 3 studies [40,46,51], while China [15,35] and Israel each [13,74] had 2 studies. Two studies contain data from multiple European countries [18,70]. The remaining countries—Denmark [14], France [24], Qatar [32], Romania [8], the United Kingdom [6], Colombia [61], Norway [63], Indonesia [69], Afghanistan [73], the Czech Republic [76], Ukraine [78], and Poland [82]—each contributed 1 study, respectively.

Most of the 79 studies were cross-sectional studies (n=41) [5,12−26,29−31,33,34,37−46,48−51,53−55,84−86] followed by case reports (n=20) [9,61−75,78−81], case series (n=11) [6,8,56−60,76,77,82,83], retrospective studies (n=6) [27,28,35,36,47,52], and case-control studies (n=1) [32].

The studies contained data from 13,252, of whom 7,509 (56.6%) were females. In most of the studies (n=40), the mean age of the patients was 58.26±11.50 years followed by 41.42±17.32 years (23 studies) and 26.18±18.42 years (12 studies). Three studies did not report the patients’ ages [5,34,35] and 1 study was conducted among newborns [8].

Only 34 studies have documented patients’ medical history. The majority of these studies documented a history of hypertension (n=26), followed by diabetes (n=20), respiratory diseases and asthma (n=7), cardiovascular disease (n=6), allergies (n=4), and other conditions. Twenty-one studies indicated that patients with COVID-19 were admitted to the hospital. Additionally, 11 studies reported that patients were hospitalized in the ICU, with 5 studies revealing that the patients required ventilation.

Oral signs and symptoms can be broadly categorized into the following: oral ulcerations, redness and burning sensation, xerostomia, red and white lesions, vesiculobullous lesions, morphological changes of the tongue, taste alteration, gingival and periodontal lesions, and salivary gland disorders. Many patients exhibited multiple signs and symptoms affecting various parts of the oral cavity. Therefore, we have assessed each oral manifestation individually. The most prevalent oral manifestation, observed in 23.8% (n=3,157) of patients, was taste alteration (46 studies). This was followed by oral ulceration in 8.1% (n=1,082 patients in 41 studies), redness and burning sensation in 2.2% (n=297 patients in 33 studies), xerostomia in 12.7% (1,694 patients in 24 studies), red and white lesions in 2.4% (326 patients in 18 studies), vesiculobullous lesions in 0.55% (n=73 patients in 13 studies), morphological changes of the tongue in 2.7% (n=360 patients in 27 studies), gingival and periodontal changes in 3.2% (n=430 patients in 12 studies), and salivary gland disorder in 1.07% (n=143 patients in 3 studies). In the majority of patients (23.6%), the tongue was the most commonly affected area, followed by the oral mucosa (14.7%), lips (4.9%), gingiva and periodontium (3.2%), palate (1.9%), and salivary glands (1.1%).

Risk of Bias Assessment

JBI critical appraisal checklists were utilized to assess the risk of bias in cross-sectional studies, case-control studies, case reports, and case series. Of the 79 studies evaluated, 50 (63.7%) demonstrated a low risk of bias, while 23 (29.3%) exhibited moderate bias, and a mere 6 studies (7%) showed a high risk of bias (Table 1) [5,6,8,9,12−86]. The detailed computation of the risk of bias, using the JBI Critical Appraisal Tools, is presented in Tables S1-S4 [5,6,8,9,12−86].

Descriptive Characteristics of the Oral Lesions

Taste disorders and tongue manifestation

The prevalence of taste disorders and tongue manifestations was evaluated using data from 46 and 27 studies, respectively. We further subdivided the taste disorders into additional categories. These include complete loss of taste, or ageusia, as reported in 22 studies [12,14,20,23,35,40−42,44,49,53,55,56,58,63,65,67,70,72,74,85], taste alteration or dysfunction, as reported in 19 studies [5,13,16−19,21,22,29,36,38,46,51,54,66,78,84−86], dysgeusia, as reported in 7 studies [24,28,37,50,54,59,60], and amblygeustia, as reported in only one study [15].

Xerostomia

Xerostomia was noted in 22 cross-sectional studies [13,15,22,28,34,37,38,40−42,44−46,48,50−55,84,85] and 2 case reports [60,78].

Vesiculobullous lesions

Thirteen studies, comprising case reports and case series, reported vesiculobullous lesions [6,9,24,26,29,50,57,59,61,62,70,77,81].

Ulceration

Ulceration was reported in 41 studies [5,6,24,27−29,31,33,34,37,39−51,53,55,56,61,64,69,73,75−85].

Red and white lesions

Eighteen studies reported red and white lesions in COVID-19-positive patients [8,24−26,29,33,36,37,39,43,49,51,53,57,61,68,80,82].

Periodontal involvement

Twelve studies described the involvement of gingiva and periodontium among patients with COVID-19 [6,26,29,32,38,39,42,44,51,55,59,78].

Redness and burning sensation

In total, 33 studies reported patients who complained of redness and burning sensation [5,6,22,26,28,30,31,33,34,38−44,46,48,50−55,57,59,60,69,78,79,81,82,85].

Salivary gland involvement

Salivary gland disorders [37,38,52] were found in 3 studies.

The latency time between the emergence of systemic symptoms and oral lesions ranged from 2 weeks prior to 10 days following the onset of systemic symptoms. In the majority of the studies (n=14), systemic symptoms occurred after the appearance of oral symptoms (Table 2) [5,6,8,9,12−86].

The general treatment protocol, as well as the specific treatment for oral lesions in COVID-19 patients, is outlined in Table S5 [6,8,9,29,43,47,56,57,59−61,64,65,67−71,73,75,77,79,80,82]. Oral lesions typically healed between 7 and 21 days post-emergence. Depending on the severity and cause of the oral lesions, various therapies were prescribed. These included chlorhexidine mouthwash, nystatin, oral fluconazole, topical or systemic corticosteroids, systemic antibiotics, systemic acyclovir, artificial saliva, and photobiomodulation therapy.

Results of the Meta-Analysis

Data from 48 studies were meta-analyzed to determine the prevalence of taste alteration, xerostomia, red and white lesions, vesiculobullous lesions, ulceration, burning sensation, and salivary gland involvement.

Among the prevalence studies, 28 separate studies [12−14,16−20,22−24,28,29,35,36,38,40−44,46,51,53−55,85,86] investigated the occurrence of taste alteration in a total of 3,157 COVID-19 patients. The meta-analysis of these studies revealed a combined prevalence rate of 48% (95% confidence interval [CI], 39%–57%). The heterogeneity of these studies was assessed using Cochran Q test and the I² index, indicating a high degree of heterogeneity with an I² value of 98.7 (Figure 2).

A total of 327 COVID-19 patients from 14 different studies reported experiencing red and white lesions [5,13,24,25,29,36,37,39,43,48,51−53,84]. These studies revealed a pooled prevalence of these symptoms at 17% (95% CI, 9%–26%), with an I² value of 98.2% (Figure 3).

Xerostomia was reported in 22 studies [13,15,22,28,34,37,38,40−42,44−46,48,50−55,84,85] involving 1,694 COVID-19 patients, showing a pooled prevalence of 35% (95% CI, 26%–44%) and I²=98.7% (Figure 4).

Ulceration was reported in 23 studies [5,24,27−29,31,33,34,37,39−48,50,51,53,85] involving 1,086 patients, with a a prevalence of 21% (95% CI, 12%–30%) and I² of 99.62% (Figure 5).

The pooled prevalence of a burning sensation was reported to be 12% (95% CI, 6%–18%) with I²=98.3%; this symptom was found in 297 patients in 11 studies [5,22,33,38,42−44,53,55,84,85] (Figure 6).

Vesiculobullous lesions were reported by 73 participants from 5 studies [26,29,36,50,51], with a pooled prevalence of 10% (95% CI, 5%–16%) and an I² of 98.5% (Figure 7A).

Salivary gland involvement was reported only in 3 studies [37,38,52] involving 193 patients, showing a pooled prevalence of 32% (95% CI, 22%–41%) and I²=98.7% (Figure 7B).

Funnel plots demonstrated asymmetry, indicating the presence of high publication bias in the studies (Figure 8).

Discussion

COVID-19 has emerged as a global public health issue. Initially, it was believed that the absence of oral mucosa involvement distinguished COVID-19 from other viral infections. However, in April 2020, a case report by Chaux-Bodard et al. [87] demonstrated a link between COVID-19 and oral mucosa. The report detailed a 45-year-old woman who experienced painful inflammation of the tongue’s papilla, which eventually healed into an asymptomatic ulcer within 10 days, leaving no scar. This patient also developed a skin lesion on her toe and tested positive for COVID-19 on the eighth day. Since this report, numerous observational studies and case reports have been published, highlighting the involvement of oral mucosa in COVID-19 patients. This systematic review was undertaken to determine the prevalence of oral manifestations in patients with COVID-19.

SARS-CoV-2 infiltrates human cells in the lower respiratory system using receptors known as ACE2 and transmembrane protease serine 2 [3]. Of these 2, the ACE2 receptor is primarily located in the cells of the lung, liver, kidney, GI tract, and even in the cells of the nasal epithelium and oral mucosa [4]. These cells serve as host cells for the virus, which invades these body cells and triggers an inflammatory response in these organs. This response, in turn, leads to early smell and taste dysfunctions during the disease’s progression [15]. Therefore, the development of oral lesions can occur directly through the effects of the virus replicating in these cells (resulting in SARS-CoV-2-specific lesions) and indirectly as a consequence of potential drug reactions that may occur during the latency period, viral exanthem, due to the physical and psychological stress of COVID-19 or its treatment, or co-infection with other bacterial infections that exacerbate the severity of COVID-19 [59,88]. The involvement of the oral cavity becomes a unique characteristic of COVID-19 [89]. According to Amorim dos Santos et al. [4], the general health deterioration of COVID-19 patients, coupled with extended hospitalization periods and numerous treatment procedures, also increases the likelihood of oral lesions. Chaux-Bodard et al. [87] proposed that oral lesions might emerge as a result of various inflammatory reactions that induce vascular inflammation. Previous reports from Italy and the United Kingdom have noted a temporary association between pediatric inflammatory multisystem syndrome and SARS-COV-2 cases [90]. Certain diseases, such as Kawasaki disease and erythema multiforme, can predispose individuals to oral manifestations. Consequently, we have excluded such conditions from our systematic review.

Regarding oral lesions, the tongue was the most frequently affected area (n=65), followed by the oral mucosa (n=37), and then the lips (n=19). de Sousa and Paradella [7] identified the palate and tongue, followed by the gums and lips, as the areas most commonly affected in COVID-19 patients. The oral manifestations among COVID-19 patients are described below:

Taste Disorders

Numerous studies have indicated that alterations in smell and taste can serve as early signs of COVID-19 infection, playing a crucial role in early diagnosis and decision-making. While these symptoms are not life-threatening, they can significantly impact a patient’s quality of life. Professor C. Hopkins, President of the British Rhinological Society, has noted that the loss of smell or taste may be the sole symptom of COVID-19 [91]. Several public health surveillance organizations, including the European Centre for Disease Prevention and Control, the Centers for Disease Control and Prevention, the WHO [92], and Public Health England, have incorporated the sudden onset of anosmia, ageusia, or dysgeusia into their primary clinical criteria for defining a COVID-19 case [93]. The present systematic review also found that general symptoms typically follow oral symptoms, particularly the loss of taste. The likely reason for taste alteration in COVID-19 patients is the higher expression of the ACE2 receptor in the tongue than in the buccal and gingival tissues. This results in damage to the mucosal epithelial cells of the oral cavity [94,95].

In the present systematic review, the pooled prevalence of taste alteration was 48%. A recent review by Scotto et al. [89] indicated that the prevalence of taste disorders varied widely across studies, ranging from 1.0% to 93.0%. In a cross-sectional study by Al-Zaidi and Badr [12], 83.08% of COVID-19 patients experienced taste dysfunction. For 50% of these patients, taste returned within a week, while for 25% it took less than a week, for 18.75% it took within 2 weeks, and for 6.25% it took within 3 weeks. In their living systematic review (LSR), Amorim dos Santos et al. [4] identified taste disorders as the most common oral symptom in this population, with a prevalence of 45%. However, in their subsequent LSR, the prevalence dropped to 38%. They noted that the prevalence of taste disorders among COVID-19 patients varies geographically, from 14% in Africa to 49% in Europe [96]. Yan et al. [21] reported taste loss in 71% of COVID-19-positive subjects, and found a strong association between taste loss and COVID-19 positivity (odds ratio, 10.2; 95% CI, 4.74–22.1). In a study by Biadsee et al. [13], 52% of participants reported changes in taste sensation, with 52 patients noting a change in spicy taste perception, 54 in salty taste, 53 in sour taste, and 61 in sweet taste. Bodnia and Katzenstein [14] found that 70% of patients experienced a total loss of taste, which resolved within 1 to 3 weeks for 78% of patients and within 3 to 6 weeks for 22%. A meta-analysis by Tong et al. [97] revealed that 43.93% of individuals noted changes in taste. Another meta-analysis by Nijakowski et al. [98] estimated the prevalence of taste alterations to be around 54.73% (95% CI, 46.28%–63.04%).

Three studies in our systematic review, conducted by Favia et al. [29], Bardellini et al. [36], and Binmadi et al. [51], reported geographic tongue. Bardellini et al. [36] carried out a retrospective cohort study on pediatric patients and identified the most common oral lesions as oral pseudomembranous candidiasis (n=2), coated tongue (n=2), taste alteration (n=3), and geographic tongue (n=1). Notably, the occurrence of geographic tongue coincided with a high fever, as reported by the patient's mother. The etiopathogenesis of geographic tongue remains unclear, but some researchers have suggested a link with several non-genetic multifactorial factors, including viral infections [99].

Vesiculobullous Lesions and Ulceration

Thirteen studies, encompassing both case reports and case series [6,9,24,26,29,50,57,59,61,62,70,77,81], documented vesiculobullous lesions. Among these, 5 cross-sectional studies revealed a combined prevalence of 10%.

Ulceration was reported by 23 studies [5,24,27−29,31,33,34,37,39−48,50,51,53,85], involving 1,086 patients with a pooled prevalence of 21%. This is slightly higher than the value reported in the meta-analysis by Aragoneses et al. [100] (10%). Favia et al. [29] provided a detailed description of the histological aspects of oral SARS-CoV-2-related lesions, identifying ulcers as the most common oral manifestation, in 52.8% of patients. Martin Carreras-Presas et al. [59] reported 3 cases of ulcers, 1 of which was confirmed to be infected with SARS-CoV-2, while the other 2 were suspected cases. These lesions were similar in appearance to herpes simplex infection, but this was not confirmed by biopsy. Halboub et al. [101] conducted a review and found that painful oral ulcers were the most common orofacial manifestation in patients with COVID-19. Bullous lesions on the palate and oral mucosa were found by Cruz Tapia et al. [57] and Dalipi et al. [70], respectively. Orilisi et al. [102] conducted a systematic review and reported that oral ulcers, cheilitis, and tongue lesions were more common in patients prior to hospitalization. In contrast, perioral pressure ulcers, macroglossia, blisters, and oral candidiasis were more frequently observed in patients during their hospital stay.

The mechanism behind ulcer formation is thought to involve an elevated level of tumor necrosis factor-α in COVID-19 patients, which can trigger the chemotaxis of neutrophils to the oral mucosa, leading to the development of aphthous-like lesions. Other potential causes for these lesions in COVID-19 patients could be stress and immunosuppression, both secondary effects of the infection [9].

Red and white lesions

Eighteen studies have reported the presence of red and white lesions in patients who tested positive for COVID-19, with a pooled prevalence of 17% [8,24−26,29,33,36,37,39,43,49,51,53,57,61,68,80,82]. The variety of red and white lesions documented in these studies include cheilitis and oral lichenoid reactions [24], white plaques on the inner oral mucous layer [25,37,43,68,80], rashes and erythema [26], candidiasis [9,29,36,49,51,53], reddish-white spots on the palate [33,57], erythema and lichen planus [39], angular cheilitis [53,82], and reddish plaques on the lower lip [61].

Xerostomia

Xerostomia was observed in 22 cross-sectional studies [13,15,22,28,34,37,38,40−42,44−46,48,50−55,84,85] and 2 case reports [60,78]. These studies reported a combined prevalence of 35%, a figure slightly lower than the 44% prevalence (95% CI, 36%–52%) found in a recent meta-analysis by Aragoneses et al. [100]. In research conducted by Biadsee et al. [13], 56% of patients reported experiencing xerostomia, as determined by the question, “Do you feel the need to drink more (dry mouth)?”. In the revised version of the LSR by Amorim Dos Santos et al. [96], xerostomia was the most frequently reported oral symptom in COVID-19 patients, whereas tassate disturbances were the primary feature in the original LSR [4]. In a meta-analysis by Nijakowski et al. [98], xerostomia was prevalent in 37.58% (95% CI, 26.35%–49.53%) of COVID-19 patients.

Gingival and periodontal involvement

Twelve studies (15%) [6,26,29,32,38,39,42,44,51,55,59,78] reported the prevalence of gingivitis and periodontitis. The gingival symptoms identified in COVID-19 patients from our systematic review included gingivitis [29], desquamative gingivitis [6,59], ulceronecrotic gingivitis [29], and gingival bleeding [6,38,42,44,55,78]. Two studies reported instances of periodontitis [32] and necrotizing periodontal disease [51].

Other findings

Red and/or swollen lips was observed by Halepas et al. [30] in 48.9% of patients. Other findings related to lip involvement in COVID-19 patients included pale lips [33], reddish plaques on the lower lip [61], nodules on the lower lip [10], and reddish macules [42]. In terms of palatal findings among COVID-19 patients, there were reddish-white spots on the palate [33], palate ulcerations [6,39,56,59,60,81,82], a white coating on the palate [43,68], bullae on both the left and right palatal mucosa [57], an erythematous surface on the hard palate [64], and an angioma-type lesion on the right side of the palate [82].

Limitations

Although we have attempted to summarize the findings of studies that report oral manifestations in COVID-19 patients, a significant limitation of this systematic review is the absence of a temporal dimension. We cannot definitively state that these oral manifestations are directly linked to COVID-19, or if they are indirect manifestations of other factors such as stress, immunosuppression, and/or medications. Another limitation is the absence of a definitive diagnosis, as most of the cases included in the review did not undergo a biopsy to confirm the diagnosis.

Conclusion

Our systematic review showed a relatively high prevalence of oral manifestations, specifically taste alteration (48%), followed by dry mouth (35%), ulceration (21%), and red and white lesions (17%). These patients exhibit a variety of oral symptoms that could aid clinicians in the early detection of the disease. It is crucial to recognize the signs and symptoms of COVID-19 for a prompt diagnosis and an improved prognosis. Dental practitioners can play a significant role not only in preventing the transmission of COVID-19 but also in interrupting the disease's progression. Increasing awareness of these symptoms is vital for the early diagnosis and treatment of this deadly disease.

HIGHLIGHTS

• The present systematic review shows a higher prevalence of oral manifestations among COVID-19 patients, specifically taste alterations, followed by xerostomia, ulceration, and red and white lesions.

• COVID-19 patients show various oral manifestations that may help clinicians detect the disease early in its course.

• Identifying the oral signs and symptoms of COVID-19 is crucial for initiating early diagnosis and treatment of this deadly disease; therefore, increasing awareness of these symptoms is important.

Supplementary Material

Article information

Ethics Approval

Not applicable.

Conflicts of Interest

The authors have no conflicts of interest to declare.

Funding

None.

Availability of Data

The datasets are not publicly available but are available from the corresponding author upon reasonable request.

Authors’ Contributions

Conceptualization: AG, KS, AP; Data curation: AG, AA; Formal analysis: AG, AP; Investigation: AG, KS, AA; Methodology: AG, KS, AA, AP, RC; Project administration: AG, KS; Software: AG, AP; Supervision: AG, AA; Validation: AG, AP; Visualization: AG, RC; Writing–original draft: AG; Writing–review & editing: authors. All authors read and approved the final manuscript.

Figure 1.

Flow diagram of literature search and selection criteria of the included studies (n=79).

Figure 2.

Forest plot showing the pooled prevalence of taste disorders in patients with COVID-19 (28 studies). RE, random effects.

Figure 3.

Forest plot showing the pooled prevalence of red and white lesions in patients with COVID-19 (14 studies). RE, random effects.

Figure 4.

Forest plot showing the pooled prevalence of xerostomia in patients with COVID-19 (22 studies). RE, random effects.

Figure 5.

Forest plot showing the pooled prevalence of ulceration in patients with COVID-19 (23 studies). RE, random effects.

Figure 6.

Forest plot showing the pooled prevalence of burning sensation in patients with COVID-19 (11 studies). RE, random effects.

Figure 7.

Forest plot showing the pooled prevalence of (A) vesiculobullous lesions (5 studies) and (B) salivary gland involvement (3 studies) in patients with COVID-19. RE, random effects.

Figure 8.

Funnel plot of studies on the prevalence of (A) taste alteration, (B) xerostomia, (C) red and white lesions, (D) vesiculobullous lesions, (E) ulceration, and (F) burning sensation.

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