Abstract
Background:
Ludwig's angina (LA) is a diffuse cellulitis of the submandibular space and adjacent tissues. During the coronavirus disease 2019 (COVID-19) pandemic, odontogenic treatments were often delayed because of the implementation of safety measures to avoid the spread of the virus. We hypothesized that delayed odontogenic treatments associated with the onset of the COVID-19 pandemic would be associated with an increase in the incidence of LA and worse outcomes related to these infections.
Patients and Methods:
Patients from June 2018 to June 2022 with computed tomography images suggestive of LA and confirmed by ear, nose, throat (ENT) consult were included. We abstracted demographics, outcomes, clinical management, and microbiology. Patients were stratified into pre-COVID and COVID-onset. Our primary outcome, incidence of LA, was defined as: (new LA cases) ÷ (ED evaluations of oral or dental infections × 1.5 years).
Results:
In the pre-COVID group, we identified 32 of 1,301 patients with LA for an incidence of 0.02 per year. The COVID-onset group consisted of 41 of 641 patients, with an incidence of 0.04 per year. In the COVID-onset group, progression to necrotizing fasciitis was more likely (0% vs. 15%; p < 0.024), and they returned to the operating room for repeated debridement (3% vs. 22%; p < 0.020). Likewise, hospital length of stay, intensive care unit (ICU) length of stay, and ventilator days were higher (4.3 ± 3.5 vs. 9.5 ± 11.3; 1.1 ± 1.2 vs. 9.5 ± 7.1; 0.3 ± 1 vs. 3.6 ± 7.1; p < 0.001).
Conclusions:
Although the prognosis for dental infections diagnosed early is generally favorable, we observed a notable increase in the incidence of LA after the onset of the COVID-19 pandemic. Moreover, complications stemming from these infections became more severe in the COVID-onset era. Specifically, the likelihood of necrotizing fasciitis showed a substantial increase, accompanied by an increased risk of respiratory failure and mediastinitis.
Keywords: COVID-19, incidence, Ludwig's angina, outcomes
Ludwig's angina (LA) is a diffuse cellulitis of the submandibular, sublingual, and submental spaces. Even though there is a wide range of etiologies associated with this condition, it commonly originates from dental infections, usually involving the second or third mandibular molar teeth.1 Symptoms of LA often include oral pain, fever, drooling, and dysphagia. As the infection progresses, patients may present with shortness of breath. For this reason, early recognition and treatment of LA is paramount to avoid complications such as obstruction of the airway because of the rapid and aggressive spread of the infection to adjacent tissues.2–4 Mortality in untreated LA with airway compromise is reported to be as high as 50%; this risk lowers to 8% in patients who receive prompt and adequate treatment.5 Severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2), a new coronavirus commonly referred as coronavirus disease 2019 (COVID-19) first appeared in December 2019 with a series of cases of “viral pneumonia” in Wuhan, China. Since then, the world and health systems have been engaged in curbing the transmission and dealing with the challenge of treatment and appeasing complications.
The first case of COVID-19 was reported in the United States in January 2020. In March of the same year, lockdowns began to be implemented with the intention of preventing the spread of the virus. During the pandemic, odontogenic treatments were often delayed because of these mandatory lockdowns, mask mandates, and the uncertainty of the novel coronavirus. In the United States, the American Dental Association recommended in March 2020 that dental professionals postpone elective procedures and provide only emergency dental care. An electronic survey conducted by Moffat et al.6 in April 2020 aimed to study the perceptions of susceptibility to contracting COVID-19 in a dental setting indicated agreement in perceived susceptibility and risk of contracting COVID-19 during dental appointments.7
This study aimed to evaluate whether a correlation exists between delayed odontogenic treatments associated with the onset of the COVID-19 pandemic. We hypothesized an increase in both the incidence of LA and the worsening of outcomes related to these infections because of the pandemic.
Patients and Methods
After obtaining an Institutional Review Board approval, we retrospectively queried our Acute and Critical Care Surgery database at Barnes-Jewish Hospital in St. Louis, Missouri, spanning June 2018 to June 2022 for patients >18 years old admitted with computed tomography images suggestive of LA (loss of fat planes, fluid, edema, soft tissue gas, and or thickening). We only included patients whose diagnosis was confirmed by otolaryngology consult. Afterward, patients were stratified into two groups according to COVID-19 onset. The pre-COVID group consisted of patients admitted from June 1, 2018 to December 31, 2019; and the COVID-onset group of patients admitted from January 1, 2021 to June 30, 2022. The year 2020 was excluded from the analysis. This exclusion was based on how we would model the progression of dental disease with loss of primary care; we would not expect an immediate change within the first several months of lockdown, with this in mind we purposely incorporated a delay to allow these problems to become severe.
We subsequently proceeded to calculate the incidence of LA for each period. This was our primary outcome and we defined incidence as (new LA cases) ÷ (emergency department evaluations of oral or dental infections × 1.5 years).
We abstracted demographics including age, gender, race, body mass index (BMI), and past medical history; specifically obesity, diabetes mellitus (DM), smoking, and hypertension. We abstracted clinical care management details such as drainage (evacuation of accumulated material through incision), antibiotic therapy, tracheostomy, microbiology results, and COVID-19 coinfection in the COVID-onset group. Our secondary outcome was aimed at assessing the following: radiologic worsening (defined as aggravating edema), hospital length of stay, intensive care unit length of stay, ventilator days, and mortality. Furthermore, we measured complications. We defined complications as additional medical problems arising directly from the LA. These complications include airway compromise, sepsis, osteomyelitis, respiratory failure, mediastinitis, and necrotizing fasciitis. Clinician assessment was used for diagnosis, relying on symptoms, radiological studies and microbiology when suitable.
Continuous variables are presented as median and interquartile range, categorical variables as counts and proportions. We subsequently analyzed the groups using χ2 and Student t-test when applicable in SPSS Statistics (IBM Corp, Armonk, NY). We considered p values <0.05 to be statistically significant.
Results
We identified 1,942 patients admitted to the emergency department with the chief complaint of oral or dental infections. During the pre-COVID time lapse 1,301 patients were admitted with these complaints; and in the COVID-onset group, only 641 patients presented to the emergency department. In the pre-COVID group, we identified 32 patients with a confirmed diagnosis of LA. The COVID-onset group consisted of 41 patients. Incidence for the pre-COVID period was 0.02 per year; the COVID-onset group had an incidence of LA of 0.04 per year.
The pre-COVID group was in majority females (53%) with a median age of 52.5 years (interquartile range [IQR], 27.5). The COVID-onset group was predominantly male (66%), with a median age of 52 years (IQR, 31). Both groups were predominantly white (56%) followed by African American (40%). We found no significant differences in gender, age, or race (p = 0.104, p = 0.923, and p = 0.355, respectively). Likewise, there was no difference in BMI (27 kg/m2, IQR, 9 vs. 27 kg/m2, IQR, 9.5, p = 0.158) between the groups. From the total cohort, 18% of patients had a history of DM (38% vs. 37%, p = 0.295), 43% hypertension (44% vs. 42%, p = 0.845), and 52% were active smokers (59% vs. 46%, p = 0.269), no significant difference was found between both groups (Table 1).
Table 1.
Cohort Demographics and Past Medical History
| |
Total |
|
Pre-COVID |
|
COVID-onset |
|
|
|---|---|---|---|---|---|---|---|
| Variables | n = 73 | % | n = 32 | % | n = 41 | % | p |
| Age | 52 (IQR, 29.5) | 52.5 (IQR, 27.5) | 52 (IQR, 31) | 0.923 | |||
| Gender | 0.104 | ||||||
| Male | 42 | 57.5 | 15 | 46.9 | 27 | 65.9 | |
| Female | 31 | 42.5 | 17 | 53.1 | 14 | 34.1 | |
| Race | 0.355 | ||||||
| White | 41 | 56.2 | 21 | 65.6 | 20 | 48.8 | |
| Black | 29 | 39.7 | 10 | 31.3 | 19 | 46.3 | |
| Other/Unknown | 3 | 4.1 | 1 | 3.1 | 2 | 4.9 | |
| Body mass index | 27 (IQR, 8.5) | 27 (IQR, 9) | 27 (IQR, 9.5) | 0.158 | |||
| Obesity | 27 | 37 | 12 | 37.5 | 15 | 36.6 | 0.936 |
| Diabetes mellitus | 13 | 18 | 4 | 12.5 | 9 | 22 | 0.295 |
| Current smoker | 38 | 52.1 | 19 | 59.4 | 19 | 46.3 | 0.269 |
| Hypertension | 31 | 42.5 | 14 | 43.8 | 17 | 41.5 | 0.845 |
Pre-Covid = January 2018 to December 2019; COVID onset = January 2021 to June 2022; COVID = coronavirus disease 2019; IQR = interquartile range.
Clinical management between the groups was very similar. Treatment consisted primarily of intravenous antibiotic agents and incision and drainage in 64% of cases (66% vs. 63%; p = 0.845), performed either in the operating room or bedside. The most common antibiotic used was intravenous ampicillin-sulbactam, followed by intravenous vancomycin and intravenous clindamycin (42%, 33%, and 31%, respectively). Furthermore, inpatient antibiotic therapy in the pre-COVID group was shorter, with a median of 4 days (IQR, 4); in the COVID-onset group antibiotic therapy was continued for a median of six days (IQR, 8.5; p < 0.001). Likewise, patients in the COVID-onset group were more likely to return to the operating room for unplanned repeated drainage or debridement (3% vs. 22%; p < 0.020). There was no statistical difference in tracheostomy rate between the groups (9% vs. 17%; p = 0.343) (Table 2).
Table 2.
Clinical Management
| |
Total |
|
Pre-COVID |
|
Post-COVID |
|
|
|---|---|---|---|---|---|---|---|
| Variables | n = 73 | % | n = 32 | % | n = 41 | % | p |
| Tracheostomy | 10 | 13.7 | 3 | 9.4 | 7 | 17.1 | 0.343 |
| Incision and drainage | 47 | 64.4 | 21 | 65.6 | 26 | 63.4 | 0.845 |
| Unplanned return to the OR | 10 | 27 | 1 | 3.1 | 9 | 21.9 | 0.020 |
| Inpatient antibiotic | |||||||
| Ampicilin-sulbactam – IV | 42 | 57.5 | 12 | 37.5 | 30 | 73.2 | |
| Vancomycin – IV | 33 | 45.2 | 12 | 37.5 | 21 | 51.2 | |
| Clindamycin – IV | 31 | 42.5 | 18 | 56.25 | 13 | 32 | |
| Antibiotic days - inpatient | 5 (IQR, 6.5) | 4 (IQR, 4) | 6 (IQR, 8.5) | < 0.001 | |||
| Antibiotic days - outpatient | 10 (IQR, 7) | 10 (IQR, 7) | 10 (IQR, 3) | 0.016 | |||
| Outpatient antibiotic | 67 | 91.2 | 31 | 96.9 | 36 | 87.8 | 0.162 |
| Amoxicillin-clavulanic acid – PO | 39 | 58.2 | 26 | 83.9 | 13 | 36.1 | 0.053 |
| Clindamycin – PO | 17 | 25.4 | 12 | 38.7 | 5 | 12.2 | 0.011 |
| Ceftriaxone – IV | 3 | 4.5 | 3 | 9.7 | 0 | 0.045 | |
Pre-Covid = January 2018 to December 2019; COVID onset = January 2021 to June 2022; COVID = coronavirus disease 2019; OR = operating room; IV = intravenous; PO = oral; IQR = interquartile range.
The most common isolated microbe pre-COVID was viridans streptococci (56%), followed by polymicrobial infections with mixed upper respiratory organisms (39%), Peptostreptococcus (11%), methicillin-sensitive Staphylococcus aureus (MSSA) (6%), and Streptococcus pyogenes (6%). In the COVID-onset group, this trend was inverted with polymicrobial infections being more common (69%), followed by viridans streptococci (19%), MSSA (15%), coagulase-negative staphylococci (4%), and Bacteroides (4%; Table 3). In the COVID-onset group, only two patients (5%) were found to be COVID-19 positive.
Table 3.
Isolated Micro-Organisms
| |
Total |
|
Pre-COVID |
|
Post-COVID |
|
|---|---|---|---|---|---|---|
| Variables | n = 73 | % | n = 32 | % | n = 41 | % |
| Positive culture | 44 | 60.3 | 18 | 56.3 | 26 | 63.4 |
| Mixed upper respiratory organisms | 25 | 56.8 | 7 | 38.9 | 18 | 69.2 |
| Viridans streptococci | 15 | 34.1 | 10 | 55.5 | 5 | 19.2 |
| MSSA | 5 | 11.4 | 1 | 5.6 | 4 | 15.4 |
| Peptostreptococcus | 2 | 4.5 | 2 | 11.1 | 0 | |
| Streptococcus pyogenes | 1 | 2.3 | 1 | 5.6 | 0 | |
| Coagulase-negative staphylococci | 1 | 2.3 | 0 | 1 | 3.8 | |
| Bacteroides | 1 | 2.3 | 0 | 1 | 3.8 | |
| Antibiotic resistance | 6 | 13.6 | 4 | 22.2 | 2 | 7.7 |
| Erythromycin | 6 | 13.6 | 4 | 22.2 | 2 | 7.7 |
| Clindamycin | 4 | 9.1 | 3 | 16.7 | 1 | 3.8 |
Pre-Covid = January 2018 to December 2019; COVID onset = January 2021 to June 2022; COVID = coronavirus disease 2019; MSSA = methicillin-sensitive Staphylococcus aureus.
Regarding complications, airway compromise had an incidence of 19%; interestingly, the rate in the pre-COVID group was 28%, in the COVID-onset group, the rate was 12% (p = 0.086). Sepsis and osteomyelitis of the jaw were more common in the pre-COVID group (9% vs. 7%; p = 0.751 and 6% vs. 2%; p = 0.416, respectively). There was a rate of respiratory failure of 10% and mediastinitis of 7% in the COVID-onset group (p = 0.069 and p = 0.118, respectively). There were no cases of either in the pre-COVID era. However, none of these complication rates were significantly different. Nonetheless, development of necrotizing fasciitis was more likely in the COVID-onset group (0% vs. 15%; p < 0.024). In accordance with previous statistics, mortality had a 4% rate in the entire cohort. In the pre-COVID group, mortality had a rate of 3% versus the COVID-onset where mortality had a rate of 5% (p = 0.708).
Hospital length of stay (3.5 [IQR, 4] vs. 6 [IQR, 10.5] ; p < 0.001), ICU length of stay (0 [IQR, 0] vs. 2 [IQR, 4.5]; p < 0.001), and ventilator days (0 [IQR, 0] vs. 0 [IQR, 4]; p < 0.001) were also significantly increased in the COVID-onset group (Table 4).
Table 4.
Hospital Outcomes
| |
Total |
|
Pre-COVID |
|
Post-COVID |
|
|
|---|---|---|---|---|---|---|---|
| Variables | n = 73 | % | n = 32 | % | n = 41 | % | p |
| Complications | 22 | 30.3 | 9 | 28.1 | 13 | 31.7 | 0.741 |
| Airway compromise | 14 | 19.2 | 9 | 28.1 | 5 | 12.2 | 0.086 |
| Sepsis | 6 | 8.2 | 3 | 9.4 | 3 | 7.3 | 0.751 |
| Necrotizing fasciitis | 6 | 8.2 | 0 | 6 | 15 | 0.024 | |
| Respiratory failure | 4 | 5.5 | 0 | 4 | 9.8 | 0.069 | |
| Osteomyelitis | 3 | 4.1 | 2 | 6.3 | 1 | 2.4 | 0.416 |
| Mediastinitis | 3 | 4.1 | 0 | 3 | 7.3 | 0.118 | |
| Radiologic worsening | 12 | 16.4 | 5 | 15.6 | 7 | 17.1 | 0.868 |
| Hospital LOS | 5 (IQR, 6) | 3.5 (IQR, 4) | 6 (IQR, 10.5) | < 0.001 | |||
| ICU LOS | 0 (IQR, 3.5) | 0 (IQR, 2) | 2 (IQR, 4.5) | < 0.001 | |||
| Vent days | 0 (IQR, 2) | 0 (IQR, 0) | 0 (IQR, 4) | < 0.001 | |||
| Mortality | 3 | 4.1 | 1 | 3.1 | 2 | 4.8 | 0.708 |
Pre-Covid = January 2018 to December 2019; COVID onset = January 2021 to June 2022; COVID = coronavirus disease 2019; IQR = Interquartile range.
Discussion
Our study examines the impact of the COVID-19 pandemic on the incidence and outcomes of LA, a serious infection of the submandibular, sublingual, and submental spaces. Other studies have explored the relation between delayed treatment and progression of LA1,5,8,9 as well as some implications for patient outcomes.10 However, our study offers comparison between the pre-COVID and COVID-onset eras, illustrating how the patters of complications shifted as a result of the pandemic.
During the onset of the COVID-19 pandemic, non-emergent dental procedures were considered high-risk for the spread of COVID-19. As stated by Kahraman et al.11: “the oral mucosa examination has been neglected during the pandemic on reasonable grounds.” The public health measures during this extraordinary time forced patients to remain in isolation. A retrospective study in England by Dawoud et al.12 comparing healthcare services from March to June 2020, to the same months the previous year, reported the time between symptom onset and presentation to the emergency department increased by a mean of 3.6 days.
The SARS-Cov-2 pandemic was an unprecedented event that affected health care services to an extent that have not been fully described. When comparing our results with existing literature, we observe consistent patterns that emphasize the need for early intervention.13–15 Chen et al.16 suggested that delay in treatment influenced the development of life-threatening neck infections. In circumstances in which hospitals are in high demand, such as a pandemic, it is vitally important that primary care systems be maintained to ease the flow of patients to emergency departments with conditions easily manageable if treated early.
With respect to complications, we found the most frequent in our cohort to be airway compromise, sepsis, necrotizing fasciitis, respiratory failure, osteomyelitis, and mediastinitis. Airway compromise, sepsis, and osteomyelitis of the jaw were more common in the pre-COVID group. A possible explanation for this may be these patients had a less aggressive treatment from admission because of milder disease. Among patients in the COVID-onset group, respiratory failure, mediastinitis, and necrotizing fasciitis were observed, which were not seen in the pre-COVID era. These complications underscore the seriousness of disease after the pandemic onset.
Previous studies have reported necrotizing fasciitis as a rare extension of LA.10,17,18 In our study, we found this to be true in the pre-COVID era; however, in the COVID-onset group there was a higher rate of necrotizing fasciitis affecting 15% of patients.
Appropriate treatment of an early diagnosed LA includes primarily antibiotic therapy. The predominant bacteria in head and neck infections are often aerobic and anaerobic. In our study, there was a predominance in viridans streptococci, mixed upper respiratory tract organisms, and MSSA. The correct choice of antimicrobial agents is imperative for an effective treatment. According to previous studies β-lactam antibiotic agents, and fluoroquinolones have been stablished as the most common drugs used to treat head and neck infections.19 Ampicillin-sulbactam, vancomycin, and clindamycin were the drugs of choice in our institution. The duration of treatment must be individualized depending on clinical response. In our study, the COVID-onset group had longer inpatient treatment periods but shorter outpatient antibiotic continuation. We suspect that longer inpatient treatment and repeated drainage procedures decreased the need of prolonged outpatient treatment continuation. Even though total duration of treatment (inpatient + outpatient) in both groups were similar, longer inpatient treatment suggest the infections of the COVID-onset group were more severe, as we could see by the higher number of tracheostomies performed in this group. We find this to be highly relevant, despite not reaching statistical significance, possibly due to a small sample size.
In some cases of LA, surgical drainage is also required as co-adjuvant to antimicrobial therapy. In our study, the COVID-onset group required multiple unplanned trips to the operating room due to ongoing incision and drainage when compared to the pre-COVID group. As well as with the antimicrobial therapy, we attribute this to the more critical illness seen in the COVID-onset group.
In the COVID-onset group, the longer hospital and intensive care unit length of stay, taken together with a higher number of inpatient antibiotic days, and ventilator days, suggest that patients after the COVID-19 pandemic onset had overall worse outcomes due to infectious complications. It is worth highlighting that out of the two patients who were diagnosed with COVID-19, only one required mechanical ventilation for less than 48 hours because of airway management. Thus, we do not believe that the presence of COVID-19 infection had a direct impact on the complicated clinical course of the COVID-onset group.
This study has some limitations. Because LA is an uncommon disorder, our sample size is small. The retrospective nature of our study should also be taken into consideration because this design must rely on others for accurate recordkeeping. Perhaps the most important limitation of our study is the lack of data on the duration of symptoms prior to presentation and whether the patients presented to the emergency department after failing outpatient antibiotic agents. However, given the evidence from previous studies demonstrating that people felt vulnerable to contracting COVID-19 during dental visits, it is likely that patients may have delayed seeking medical attention and subsequently presented to the emergency department. Also, assessment of the complications was made by clinicians; we count this as a limitation because we did not set criteria for diagnosis specific to each complication.
Conclusions
Most odontogenic infections are generally localized and if diagnosed early have an excellent prognosis and low complication rates. Conversely, delayed treatment associated with COVID-19 resulted in a higher incidence of LA and overall worse outcomes in our study population. Our study emphasizes the critical importance of early diagnosis and intervention, especially during periods of healthcare disruption. Future research should delve deeper into the specific factors contributing to delayed health-care–seeking behaviors and explore potential strategies to mitigate their impact on patient outcomes.
Authors' Contributions
Data curation: Canas, Fonseca, De Filippis, Diaz, Afzal, Day. Formal analysis: Canas, Fonseca. Investigation: Canas, Fonseca, De Filippis, Diaz, Afzal. Writing—original draft: Canas, Fonseca. Writing—review and editing: Canas. Visualization: Canas, Leonard. Conceptualization: J. Leonard, G.V. Bochicchio, Hoofnagle. Methodology: Leonard, Hoofnagle. Validation: Leonard, Hoofnagle. Supervision: Leonard, K. Bochicchio, G.V. Bochicchio, Hoofnagle. Project administration: K. Bochicchio. Visualization: G.V. Bochicchio, Hoofnagle.
Funding Information
The authors have no funding to report.
Author Disclosure Statement
The authors have no conflict of interest to report.
References
- 1. Boscolo-Rizzo P, Da Mosto MC. Submandibular space infection: A potentially lethal infection. Int J Infect Dis 2009;13(3):327–333; doi: 10.1016/j.ijid.2008.07.007 [DOI] [PubMed] [Google Scholar]
- 2. Pak S, Cha D, Meyer C, et al. Ludwig's angina. Cureus 2017;9(8):e1588; doi: 10.7759/cureus.1588 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3. An J, Maddeo J, Singhal M. StatPearls Publishing [Internet]. Ludwig Angina. Treasure Island (FL); 2023; Available from: https://www.ncbi.nlm.nih.gov/books/NBK482354/ [Last accessed: May 25, 2023]. [Google Scholar]
- 4. Parhiscar AH-E, G. Deep neck abscess: A retrospective review of 210 cases. Ann Otol Rhinol Laryngol 2001;110(11):1051–1054; doi: 10.1177/000348940111001111 [DOI] [PubMed] [Google Scholar]
- 5. Bridwell R, Gottlieb M, Koyfman A, et al. Diagnosis and management of Ludwig's angina: An evidence-based review. Am J Emerg Med 2021;41:1–5; doi: 10.1016/j.ajem.2020.12.030 [DOI] [PubMed] [Google Scholar]
- 6. Moffat RC, Yentes CT, Crookston BT, et al. Patient perceptions about professional dental services during the COVID-19 pandemic. JDR Clin Trans Res 2021;6(1):15–23; doi: 10.1177/2380084420969116 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7. Altintas E. Complications of dental infections due to diagnostic delay during COVID-19 pandemic. BMJ Case Rep 2022;15(4):e247553; doi: 10.1136/bcr-2021-247553 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8. McDonnough JA, Ladzekpo DA, Yi I, et al. Epidemiology and resource utilization of Ludwig's angina ED visits in the United States 2006–2014. Laryngoscope 2019;129(9):2041–2044; doi: 10.1002/lary.27734 [DOI] [PubMed] [Google Scholar]
- 9. Kovalev V. A Severe Case of Ludwig's Angina with a complicated clinical course. Cureus 2020;12(4):e7695; doi: 10.7759/cureus.7695 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10. Blanchard A, Garcia LG, Palacios E, et al. Ludwig angina progressing to fatal necrotizing fasciitis. Ear Nose Throat J 2013;92(3):102–104; doi: 10.1177/014556131309200306 [DOI] [PubMed] [Google Scholar]
- 11. Cebeci Kahraman F, Caskurlu H. Mucosal involvement in a COVID-19–positive patient: A case report. Dermatol Ther 2020;33(4):e13797; doi: 10.1111/dth.13797 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12. Dawoud BES, Kent P, Ho MWS. Impacts of lockdown during the SARS-CoV-2 pandemic on patients presenting with cervicofacial infection of odontogenic origin: A comparative study. Br J Oral Maxillofac Surg 2021;59(3):e109–e113; doi: 10.1016/j.bjoms.2020.09.014 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13. Uittamo J, Lofgren M, Hirvikangas R, et al. Severe odontogenic infections: Focus on more effective early treatment. Br J Oral Maxillofac Surg 2020;58(6):675–680; doi: 10.1016/j.bjoms.2020.04.004 [DOI] [PubMed] [Google Scholar]
- 14. Rusu LC, Ardelean LC, Tigmeanu CV, et al. COVID-19 and its repercussions on oral health: A review. Medicina (Kaunas) 2021;57(11):1189; doi: 10.3390/medicina57111189 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15. Nardi GM, Grassi R, Grassi FR, et al. How did the COVID-19 pandemic effect dental patients? An Italian observational survey study. Healthcare (Basel) 2021;9(12)L1748; doi: 10.3390/healthcare9121748 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16. Chen MK, Wen YS, Chang CC, et al. Predisposing Factors of life-threatening deep neck infection: Logistic regression analysis of 214 cases. J Otolaryngol 1998;27(3):141–144. [PubMed] [Google Scholar]
- 17. Chueng K, Clinkard DJ, Enepekides D, et al. An unusual presentation of ludwig's angina complicated by cervical necrotizing fasciitis: A case report and review of the literature. Case Rep Otolaryngol 2012;2012:931350; doi: 10.1155/2012/931350 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18. Kavarodi AM. Necrotizing fasciitis in association with Ludwig's angina: A case report. Saudi Dent J 2011;23(3):157–160; doi: 10.1016/j.sdentj.2011.03.003 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19. Brook I. Microbiology and principles of antimicrobial therapy for head and neck infections. Infect Dis Clin North Am 2007;21(2):355–391, vi; doi: 10.1016/j.idc.2007.03.014 [DOI] [PubMed] [Google Scholar]