Epidemiological Characteristics, Pathogenesis and Clinical Implications of Sinusitis in the Era of COVID-19: A Narrative Review

Introduction

Since the severe acute respiratory syndrome (ARDS) coronavirus 2 (SARS‐CoV‐2) emerged and caused coronavirus disease 2019 (COVID‐19), different reports have indicated the global burden the pandemic caused on the different aspects of the communities and their populations.1,2 In addition, the disease has been associated with not only the development of ARDS but other conditions and complications that might even be life-threatening. In addition, it has been evidenced that COVID-19 can significantly decrease CD8+T and CD4+T cells leading to a remarkable reduction in the immune response and producing a state of immunosuppression.3 Such events can lead to serious conditions, including bacterial and fungal infections. These infections can emerge as hospital-acquired infections or are associated with other pre-existing morbidities, including lung diseases and diabetes.1–3

Epidemiological evidence shows that 5–98% of COVID-19 patients usually suffer from gustatory and olfactory dysfunction.4–8 This might not be very pleasant but is not potentially life-threatening. On the other hand, fungal sinusitis, particularly acute invasive fungal rhinosinusitis (AIFR), can be life-threatening. Furthermore, the condition is usually associated with severe morbidities, as affected patients are usually immunocompromised. Evidence among studies in the literature shows that affected patients with AIFR usually include patients with uncontrolled diabetes, malignancy, immunosuppression, AIDS, the administration of chemotherapy and other immunosuppressive drugs, and COVID-19.9,10

There is an emerging burden of chronic sinusitis during the COVID-19 era, mainly as it can be found in different forms. Therefore, it is essential to study the association between COVID-19 and sinusitis to provide healthcare authorities with a better understanding of these events and establish the best management practice. For that, we conducted this narrative literature review to highlight the association between COVID-19 and sinusitis based on evidence from the available studies in the literature.

Methods

We conducted a thorough literature search to curate all the relevant articles and formulate the best evidence. We searched different databases, including Scopus, PubMed, and Google Scholar. In addition, a manual search was also conducted to find all potentially related articles that could help us formulate our evidence. First, the research team prepared the keywords according to the medical subject headings (MeSH). Then, we searched the articles using the keywords separately and with combinations. The keywords used in the present review article to explore the works of literature were “sinusitis”, “invasive”, “COVID-19”, “risk factors”, “fungal”, “rhinosinusitis”, and “pathogenesis.” The present literature review included only published English-language articles with access to full texts. We excluded the research articles other than in the English language and the published articles without the peer review process. Initially, we searched using keywords and retrieved 285 articles. However, after applying the inclusion and exclusion criteria, the present study used 96 papers for the review related to epidemiological characteristics, pathogenesis, and the association between sinusitis and COVID-19.

COVID-19 and Chronic Sinusitis Association Between Both Conditions

We presented the summary of studies that demonstrated the association between chronic rhinosinusitis (CRS) and COVID – 19 in Table 1.

Table 1 Summary of Studies That Demonstrated the Association Between Chronic Rhinosinusitis (CRS) and COVID – 19

Many previous studies have investigated the association between COVID-19 and chronic rhinosinusitis. For instance, a nested case-control study conducted in Korea by Lee et al11 demonstrated that the rate of COVID-19 infections was higher among patients with chronic rhinosinusitis than among others without it. Lee et al reported that SARS- CoV- 2 infections were significantly higher among CRS patients [Adjusted odds ratio (AOR) = 1.22 and 95% confidence interval (CI) = 1.04–1.42] and COVID-19 patients with CRS had more severe outcomes [AOR = 1.71, 95% of CI = 1.09–2.71] Moreover, the rate of severe COVID-19 outcomes was higher among patients with chronic rhinosinusitis than others (21% versus 13.3%). On the other hand, a cohort study by Wang et al12 reported that the risk of developing severe COVID-19 was not associated with chronic rhinosinusitis. However, it should be noted that the authors mentioned that deceased patients with chronic rhinosinusitis were excluded from the study. These patients could have been patients with severe COVID-19. Therefore, their data might not have been adequately represented. A retrospective study conducted by Sbeih et al13 showed that chronic rhinosinusitis was significantly associated with an increased risk of hospital admission in COVID-19 patients (AOR = 3.19, 95% CI = 1.12–10.68). However, they also reported that this risk was not associated with an increased risk of mortality, mechanical ventilation, or admission to the ICU. The risk of hospitalization in COVID-19 patients with chronic rhinosinusitis is 3.46 times higher than in patients without rhinosinusitis. A more recent case-control study by Workman et al14 showed that the risk of COVID-19 is not associated with having chronic rhinosinusitis. Miller et al15 further demonstrated that the risk of COVID-19 is not associated with the administration of steroid therapy in patients with chronic rhinosinusitis. There have been some concerns regarding the negative impact of steroid therapy on the immune response in patients with chronic rhinosinusitis. However, current evidence does not support these concerns, which need further evaluation in future investigations.

Pathogenesis

Evidence shows that chronic rhinosinusitis is significantly associated with increasing the risk of sepsis, pneumonia, and mortality. This might be attributed to the fact that the presence of sinusitis might lead to a significant reduction in nitric oxide production and can provide a viral or bacterial reservoir, increasing the susceptibility to developing a secondary infection and reducing the functions of the host immune response.16,17 Previous studies also showed different modalities of immune dysfunction with chronic rhinosinusitis, including specific antibody deficiency and epithelial barrier dysfunction.18–20 This can significantly increase the risk of COVID-19 and induce a severe disease.

Different mechanisms and pathogenetic theories have been proposed to justify the association between severe COVID-19 or increased infectivity of SARS-CoV-2 and chronic rhinosinusitis. For instance, chronic rhinosinusitis is usually caused by a viral infection, which increases the risk of other viral co-infections, including SAR-CoV-2. This has been indicated in a previous investigation that compared viral loads in the nasal mucosa and nasal lavage fluids in patients with and without chronic rhinosinusitis. The authors demonstrated that the risk of having viral co-infection was 2.9 times higher among patients with rhinosinusitis. Moreover, it has been shown that the rate of coronavirus infection was 21.6% in these patients.21 Another explanation might be the impairment that affects the functions of the sinonasal epithelial barrier, leading to an increased risk of viral invasion in patients with chronic rhinosinusitis. This happens to be a potential impairment in the mucociliary clearance of viral pathogens. In this context, a previous study demonstrated that patients with chronic rhinosinusitis usually have functional and morphologic changes within sinonasal epithelial cells. These changes involve loss of ciliated cells, goblet cell hyperplasia, and basal cell proliferation.22

Another factor associated with COVID-19 and severe disease is the increased expression of the transmembrane serine protease 2 (TMPRSS2) and receptor-angiotensin converting enzyme II (ACE2) in the nasal cavities of patients with chronic rhinosinusitis due to their significant reported roles in SARS-CoV-2 transmission and entry. In addition, it is well-known that the nasal epithelium and the sinonasal cavity are regions with the highest rate of ACE2 receptors within the respiratory tract.23–25 Accordingly, accelerating SARS-CoV-2 entry can occur secondary to viral retention in patients with chronic rhinosinusitis via viral binding receptors to TMPRSS2 and ACE2. Finally, the susceptibility to COVID-19 can be modulated by the local inflammatory response usually encountered in chronic rhinosinusitis. During inflammation, evidence shows that patients with chronic rhinosinusitis usually suffer from impaired innate immune response to potential viral infections.26

Furthermore, upregulating the expression of ACE2 might also occur during these inflammatory responses secondary to increased expression of proinflammatory cytokines, including interferons.27 Therefore, these events can significantly induce SARS-CoV-2 infection in patients with chronic rhinosinusitis.28 This evidence can be further strengthened by the reports that showed that the severity of COVID-19 in patients with chronic rhinosinusitis could be remarkably reduced by administering an inhibitor of interleukin-13 and 4 (dupilomab).29,30 Accordingly, these discussed factors in patients with chronic rhinosinusitis can significantly increase the risk of SARS-CoV-2 infection and the severity of a pre-existing COVID-19.

Chronic Rhinosinusitis and COVID-19 Symptoms

Some studies have previously used the Sino-Nasal Outcome Test-22 questionnaire to assess the quality of life and severity of chronic rhinosinusitis-related symptoms in patients suffering from COVID-19.31 For example, a cross-sectional study by Akhlaghi et al31 reported no significant differences between patients with and without chronic rhinosinusitis, regarding otologic, nasal, emotional, and sleep domains, according to the Sino-Nasal Outcome Test (SNOT)-22 questionnaire. Therefore, the authors concluded that the presence of COVID-19 in patients with chronic rhinosinusitis does not alter the related manifestations of these patients. Besides, the authors investigated the differences in disease severity among chronic rhinosinusitis patients with and without nasal polyps. It has been shown that no significant differences in COVID-19 severity were noticed between the two groups. However, after one year of the COVID-19 pandemic, the SNOT scores were significantly reduced among the CRS patients (40.1 vs 46.3, p <0.01).31

Olfactory Loss in COVID-19

Official epidemiological reports from the World Health Organization show that olfactory dysfunction can occur in 5% to 85% of patients with COVID-19.5,7,32 In addition, early symptoms of COVID-19 might include sudden olfactory loss with no nasal congestion.33–36 Accordingly, at the time of outbreaks, different countries have adopted the recommendation that patients with sudden olfactory dysfunction should be isolated for being suspected of COVID-19.4,36–38 However, it should be noted that this strategy was not reliable in detecting COVID-19 cases, especially as most cases were based on self-reports.4,39,40

It should be noted that olfactory loss secondary to COVID-19 is usually reversible, and patients gain partial or normal olfactory functions within the first weeks following the viral infection. On the other hand, it has been shown by de Melo et al in their hospital-based cross-sectional study that olfactory dysfunction might persist in some patients for months after the infection and might be permanent in others.41 However, it remains controversial why olfactory dysfunction occurs in COVID-19 patients. Accordingly, various investigations have provided some theories regarding the potential pathogenesis of olfactory dysfunction in these patients.42,43 For example, it might be due to infection of the sustentacular supporting cells and epithelial injury, which is associated with upregulation and overexpression of ACE2 receptors.44,45 Another factor might be obstruction of the olfactory cleft and epithelial edema.

Moreover, neuropilin-1 receptor (NRP1)-mediated injury to the olfactory sensory mucosa might also represent a significant factor that enhances the pathogenesis of the condition as it enhances binding with the spike protein.46,47 Although current evidence through a prospective cohort study supports the claims that endothelial injury to the olfactory mucosa is a significant factor for olfactory dysfunction in COVID-19 patients,48 this mechanism does not adequately represent the characteristics of the phenomenon in these patients. Some of these characteristics include the possible presence of viral particles in olfactory bulbs, neuroimaging changes, the variable duration of olfactory loss in affected patients, and the inverse association between the prevalence of olfactory loss and the severity of COVID-19.

It should be noted that some evidence shows that some of these characteristics can be understood by the potential role of NRP1-mediated viral entry, as the receptor is markedly expressed in neuronal progenitor cells and olfactory neurons.47 This can facilitate damage and loss of neuronal progenitor cells and olfactory functions following viral entry and damaged olfactory neurons. Moreover, these events will lead to axonal transport to the olfactory bulbs, remarkably delaying the recovery of olfactory dysfunction.

Fungal Sinusitis Acute Invasive Fungal Rhinosinusitis (AIFR)

AIFR can be defined by acute fungal tissue invasion, with a clinical course that develops within less than four weeks.49 However, evidence shows that affected patients usually develop the clinical course with days that do not usually exceed a few weeks. Besides, thrombosis and vascular invasion are usually associated.50 Patients usually present with fever, facial pain, and nasal congestion, with frequent extension into the surrounding structures, like the cranial cavity, orbit, and paranasal soft tissues. Attenuation of vision might occur secondary to orbit invasion. Moreover, neurological impairments and proptosis might occur in intracranial or orbit extensions.50,51

It is recommended that the diagnosis and management of AIFR should be conducted urgently as the condition is time-sensitive, might be associated with serious complications, and can even lead to mortality. Furthermore, AIFR represented a major burden even before the COVID-19 era, indicating the present huge burden when many events have been reported in COVID-19 patients. For instance, a 10-year prospective cohort study conducted in Egypt in a pediatric oncology center discovered 45 cases of AIFR. Similar rates were also reported in other countries.52,53 Another investigation reported that an annual number of 5–7 AIFR cases is usually diagnosed in their center. However, during the COVID-19 pandemic, a substantial increase in AIFR cases was noticed in their center.54,55

This has been furtherly indicated in another Egyptian retrospective study, indicating the significant association between COVID-19 and AIFR. However, the authors further demonstrated that the extent of surgical resection and local infection is not associated with COVID-19.56 Ismaiel et al57 also conducted a comparative study between COVID-19 and non-COVID-19 patients and found that the rate of AIFR among COVID-19 patients was higher than in the other group. A more recent investigation in India showed the association between COVID-19 and fungal rhinosinusitis as they included a relatively large number of cases in their study.58 Interestingly, most of the reported cases were of acute onset. On the other hand, a case report by Treviño-Gonzalez et al59 described a case of chronic granulomatous invasive fungal rhinosinusitis in a COVID-19 patient, which was atypical.

The exact incidence of fungal sinusitis in patients with COVID-19 is still unknown. This is because most of the currently published investigations are limited case reports, reporting the clinical sequence and management approaches of a single or a small number of patients.60,61 However, a recent systematic review analyzed the findings of 14 reports that reported cases of AIFR in association with COVID-19. The authors reported that 206 cases were retrieved from these articles, mostly found in India, Egypt, and North America.62 In addition, a large Indian retrospective observational study involving 2826 patients by Sen et al showed that rhino-sinusal mucormycosis (24.6%) was the second most common form of mucormycosis in their COVID-19 patients after rhino-orbital (48.9%).63 Furthermore, a similar prevalence rate was reported in a review of observational studies by Casalini et al,64 as the authors reported that the prevalence of fungal sinusitis was 24.6%.

Intracranial involvement was also reported in different investigations. Many previous studies and case reports also showed the involvement of the cavernous sinus by fungal infection associated with COVID-19.54,65–71 A systematic review of these studies showed a significant association between COVID-19 and the development of these events, with estimated cases of 36/132.72 Moreover, a prospective longitudinal study by El-Kholy et al54 estimated that 2.7% of his population (n = 36) had transverse and sigmoid sinus thrombosis.

Various studies also reported the frequency of involvement of paranasal sinuses. For instance, Arjun et al73 reported that the ethmoid sinus was the most commonly involved paranasal sinus in their population (80%). On the other hand, Bayram et al74 and Nehara et al70 reported prevalence rates of 90.9% and 100% for the involvement of ethmoid sinuses in their population, respectively. Pansinusitis was also frequently reported in many similar investigations. For instance, Pakdal et al65 estimated that their study population was commonly affected with pansinusitis. Bayram et al,74 Sen et al,71 Nehara et al,70 and Ravani et al69 also reported prevalence rates of 90.9%, 100%, 60%, and 77.4%, respectively.

Risk Factors Diabetes Mellitus (DM)

Many studies have implied the association between different factors that might predispose to the development of AIFR before and during the COVID-19 pandemic. For instance, a non-COVID-19 study by Kursun et al75 demonstrated that among patients with AIFR, diabetes mellitus (DM) was the commonest comorbidity. Moreover, the authors reported that chronic kidney disease and hematological malignancies were other associated morbidities. Other studies before the COVID-19 pandemic also demonstrated that DM was the most common morbidity in their AIFR populations.76–81 Furthermore, in 2013, Turner et al82 showed that in their AIFR population, the prevalence of DM was 47.8%.

Moreover, other factors, such as hematological malignancies and corticosteroids, were prevalent in 39% and 27.6% of their population. DM, highly prevalent in Egypt, is also identified as a risk factor for developing fungal infections in the country.83 Bakhshaee et al84 also reported that among patients with AIFR, the commonest associated morbidities were DM and leukemia at 50% and 44.4%. Before the COVID-19 pandemic, evidence from a systematic review demonstrated that the prevalence of DM and hematologic malignancies was 48% and 39% in patients with invasive fungal sinusitis.82 The association between AIFR and DM might be due to the affinity between fungal infection and high glucose concentrations together with the acidotic environment in these patients. Bala et al85 showed that the chance of developing mucormycosis is 7.5 times higher in diabetic patients than in healthy individuals.

Studies that included COVID-19 patients also demonstrated that DM was the commonest risk factor for developing AIFR in these patients. For instance, a prospective longitudinal study by El-Kholy et al54 showed that DM was present in 27.8% of their patients that developed AIFR acutely after COVID-19. This has been furtherly indicated in another Egyptian investigation as the authors showed that COVID-19 is strongly associated with developing DM in previously healthy individuals. DM, in turn, is significantly associated with developing AIFR. Other studies further indicated this. Ismaiel et al57 showed that DM was the commonest predisposing factor for developing AIFR in their population, followed by renal and liver dysfunction due to the negative impact of these conditions on the immune systems of these patients. A recent systematic review of COVID-19-associated AIFR cases also reported that DM and hypertension were the most common risk factors in the population.62 The authors reported that DM was prevalent in 73.3% of their population, while hematologic malignancies were found in 1.5%, which was inconsistent with previous pre-COVID-19 studies that indicated that hematologic malignancies were the second commonest morbidities identified in patients with AIFR. Such findings indicate the huge impact of DM on COVID-19 patients in developing AIFR.

Steroids

Steroid therapy might also be a significant risk factor for developing AIFR during COVID-19. This is because many patients have been administered steroid therapy as a management approach for COVID-19 due to the early reports that suggested the administration of steroids for managing COVID-19. This has been further indicated by Donovan et al62 that steroid use was found in 65% of their COVID-19-associated AIFR population. In addition, in a recent Indian retrospective study by Baghel et al58 demonstrated that HbA1c levels and duration of steroid use in COVID-19 patients were significantly associated with AIFR.

The association between hyperglycemia and diabetes was also investigated in some studies, which might have induced a larger risk of developing AIFR. Evidence shows that patients might have diabetic ketoacidosis secondary to steroid-induced hyperglycemia, contributing to the risk of AIFR during COVID-19.86,87 However, it should be noted that steroid dosing was remarkably variable during the COVID-19 pandemic, explaining why some populations might be at more risk of developing secondary infections and adverse events than others.88,89

COVID-19-Induced Immunosuppression

Moreover, COVID-19 is a significant risk factor for developing an invasive fungal function. This has been indicated according to evidence from the UK National Mycology Reference Laboratory. COVID-19 might dysregulate the immune functions of affected hosts, leading to an impaired immune response and increased incidence of fungal and bacterial infections. However, it should be noted that Ebeid et al56 suggested that the association between COVID-19 and AIFR is not a direct one. In fact, COVID-19 could be responsible for developing other predisposing factors, including DM and impaired immune response, which are usually responsible for the development of AIFR.

It should be noted that some relevant studies reported that the above-mentioned risk factors could be combined in patients with COVID-19 and AIFR, representing the most significant risk for health deterioration in affected patients. For example, Pradhan et al90 reported that DM was present in 96% of their COVID-19 AIFR patients, while a history of using corticosteroids was found in 89% of the total population. This was further indicated in another Indian investigation by Moorthy et al,91 as the authors reported that almost all of their patients had a history of DM and steroid use. A retrospective study by Moorthy et al91 reported that uncontrolled diabetes (p = 0.03) and patients who received steroids at some point of time during the treatment (p = 0.0013) had significantly higher chance of developing the maxillofacial and rhino-cerebro-orbital fungal infections. Similar findings were also reported by other studies and systematic reviews.72,92

Serum Ferritin

Even though uncontrolled diabetes mellitus was one of the critical risk factors for developing mucormycosis, the increased level of serum ferritin associated with mucormycosis among COVID-19 patients was demonstrated by some researchers. A study conducted during the second wave of the COVID-19 pandemic in India by Nayak et al identified increased serum ferritin levels with a mean of 662.01 ng/mL and raised levels of D-Dimer as the associated factor for increased risk of developing mucormycosis.93 A prospective study by Anand et al in 2022 that compared serum ferritin values among COVID-19 and non-COVID patients demonstrated a higher serum ferritin level among COVID-patients, and mucormycosis patients had higher serum ferritin levels, especially among the non-survivors and critically ill patients.94 Similar findings were observed by Rao et al and Bhadania et al.95,96

A summary of studies that demonstrated the risk factors for developing acute invasive fungal rhinosinusitis among COVID – 19 patients are depicted in Table 2.

Table 2 Summary of Studies That Demonstrated the Risk Factors for Developing Acute Invasive Fungal Rhinosinusitis Among COVID – 19 Patients

Conclusion

The current literature review discussed the association between COVID-19 and chronic sinusitis and AIFR. Evidence shows that chronic sinusitis might have a negative impact on COVID-19 outcomes. However, current results are conflicting, and further studies are needed. On the other hand, COVID-19 can also lead to olfactory dysfunction, which is usually temporary. In addition, we found several studies that indicated the association between COVID-19 and AIFR. The condition is usually associated with severe morbidities, as affected patients are usually immunocompromised. Evidence among studies in the literature shows that affected patients with AIFR usually include patients with uncontrolled diabetes, malignancy, immunosuppression, AIDS, the administration of chemotherapy and other immunosuppressive drugs, and COVID-19.

Funding

The present study did not receive any external funding.

Disclosure

The authors declare no conflicts of interest for this work.

References

1. Zhou P, Yang XL, Wang XG, et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature. 2020;579(7798):270–273. doi:10.1038/s41586-020-2012-7

2. Gorbalenya AE, Baker SC, Baric RS. The species severe acute respiratory syndrome-related coronavirus: classifying 2019-nCoV and naming it SARS-CoV-2. Nat Microbiol. 2020;5(4):536–544. doi:10.1038/s41564-020-0695-z

3. Yang W, Cao Q, Qin L, et al. Clinical characteristics and imaging manifestations of the 2019 novel coronavirus disease (COVID-19): a multi-center study in Wenzhou city, Zhejiang, China. J Infect. 2020;80(4):388–393. doi:10.1016/j.jinf.2020.02.016

4. Mullol J, Alobid I, Mariño-Sánchez F, et al. The loss of smell and taste in the COVID-19 outbreak: a tale of many countries. Curr Allergy Asthma Rep. 2020;20(10):61. doi:10.1007/s11882-020-00961-1

5. Lechien JR, Chiesa-Estomba CM, De Siati DR, et al. Olfactory and gustatory dysfunctions as a clinical presentation of mild-to-moderate forms of the coronavirus disease (COVID-19): a multicenter European study. Eur Archiv Oto-Rhino-Laryngol. 2020;277(8):2251–2261. doi:10.1007/s00405-020-05965-1

6. Moein ST, Hashemian SM, Mansourafshar B, Khorram-Tousi A, Tabarsi P, Doty RL. Smell dysfunction: a biomarker for COVID-19. Int Forum Allergy Rhinol. 2020;10(8):944–950. doi:10.1002/alr.22587

7. Izquierdo-Dominguez A, Rojas-Lechuga MJ, Mullol J, Alobid I. Olfactory dysfunction in the COVID-19 outbreak. J Investig Allergol Clin Immunol. 2020;30(5):317–326. doi:10.18176/jiaci.0567

8. Rojas-Lechuga MJ, Izquierdo-Domínguez A, Chiesa-Estomba C, et al. Chemosensory dysfunction in COVID-19 out-patients. Eur Archiv Oto-Rhino-Laryngol. 2021;278(3):695–702. doi:10.1007/s00405-020-06266-3

9. Kim DW, Heo ST, Jeon SY, et al. Invasive paranasal mucormycosis with peripheral eosinophilia in an immunocompetent patient. Med Mycol. 2010;48(2):406–409. doi:10.1080/13693780903177790

10. Fekkar A, Lampros A, Mayaux J, et al. Occurrence of invasive pulmonary fungal infections in patients with severe COVID-19 admitted to the ICU. Am J Respir Crit Care Med. 2021;203(3):307–317. doi:10.1164/rccm.202009-3400OC

11. Lee SW, Kim SY, Moon SY, et al. Estimating COVID-19 infection and severity risks in patients with chronic rhinosinusitis: a Korean nationwide cohort study. J Allergy Clin Immunol Pract. 2021;9(6):2262–2271.e2. doi:10.1016/j.jaip.2021.03.044

12. Wang H, Song J, Pan L, et al. The characterization of chronic rhinosinusitis in hospitalized patients with COVID-19. J Allergy Clin Immunol Pract. 2020;8(10):3597–3599.e2. doi:10.1016/j.jaip.2020.09.013

13. Sbeih F, Gutierrez J, Saieed G, Chaaban MR. Chronic rhinosinusitis is associated with increased risk of COVID-19 hospitalization. Am J Otolaryngol. 2022;43(4):103469. doi:10.1016/j.amjoto.2022.103469

14. Workman AD, Bhattacharyya N. Do patients with chronic rhinosinusitis exhibit elevated rates of covid-19 infection? Laryngoscope. 2022;132(2):257–258. doi:10.1002/lary.29961

15. Miller LE, Bhattacharyya N. Risk of COVID-19 infection among chronic rhinosinusitis patients receiving oral corticosteroids. Otolaryngol Head Neck Surg. 2022;166(1):183–185. doi:10.1177/01945998211006931

16. Deja M, Busch T, Bachmann S, et al. Reduced nitric oxide in sinus epithelium of patients with radiologic maxillary sinusitis and sepsis. Am J Respir Crit Care Med. 2003;168(3):281–286. doi:10.1164/rccm.200207-640OC

17. Huyett P, Rowan NR, Ferguson BJ, Lee S, Wang EW. The relationship of paranasal sinus opacification to hospital-acquired pneumonia in the neurologic intensive care unit patient. J Intensive Care Med. 2019;34(10):844–850. doi:10.1177/0885066617718458

18. Keswani A, Dunn NM, Manzur A, et al. The clinical significance of Specific Antibody Deficiency (SAD) severity in chronic rhinosinusitis (CRS). J Allergy Clin Immunol Pract. 2017;5(4):1105–1111. doi:10.1016/j.jaip.2016.11.033

19. Roland LT, Pinto JM, Naclerio RM. The treatment paradigm of chronic rhinosinusitis with nasal polyps in the COVD-19 era. J Allergy Clin Immunol Pract. 2020;8(8):2492–2494. doi:10.1016/j.jaip.2020.06.029

20. Cho SH, Hamilos DL, Han DH, Laidlaw TM. Phenotypes of chronic rhinosinusitis. J Allergy Clin Immunol Pract. 2020;8(5):1505–1511. doi:10.1016/j.jaip.2019.12.021

21. Cho GS, Moon BJ, Lee BJ, et al. High rates of detection of respiratory viruses in the nasal washes and mucosae of patients with chronic rhinosinusitis. J Clin Microbiol. 2013;51(3):979–984. doi:10.1128/jcm.02806-12

22. Wynne M, Atkinson C, Schlosser RJ, Mulligan JK. Contribution of epithelial cell dysfunction to the pathogenesis of chronic rhinosinusitis with nasal polyps. Am J Rhinol Allergy. 2019;33(6):782–790. doi:10.1177/1945892419868588

23. Kimura H, Francisco D, Conway M, et al. Type 2 inflammation modulates ACE2 and TMPRSS2 in airway epithelial cells. J Allergy Clin Immunol. 2020;146(1):80–88.e8. doi:10.1016/j.jaci.2020.05.004

24. Hou YJ, Okuda K, Edwards CE, et al. SARS-CoV-2 reverse genetics reveals a variable infection gradient in the respiratory tract. Cell. 2020;182(2):429–446.e14. doi:10.1016/j.cell.2020.05.042

25. Sungnak W, Huang N, Bécavin C, et al. SARS-CoV-2 entry factors are highly expressed in nasal epithelial cells together with innate immune genes. Nat Med. 2020;26(5):681–687. doi:10.1038/s41591-020-0868-6

26. Hwang JW, Lee KJ, Choi IH, Han HM, Kim TH, Lee SH. Decreased expression of type I (IFN-β) and type III (IFN-λ) interferons and interferon-stimulated genes in patients with chronic rhinosinusitis with and without nasal polyps. J Allergy Clin Immunol. 2019;144(6):1551–1565.e2. doi:10.1016/j.jaci.2019.08.010

27. Morse JC, Li P, Ely KA, et al. Chronic rhinosinusitis in elderly patients is associated with an exaggerated neutrophilic proinflammatory response to pathogenic bacteria. J Allergy Clin Immunol. 2019;143(3):990–1002.e6. doi:10.1016/j.jaci.2018.10.056

28. Ziegler CGK, Allon SJ, Nyquist SK, et al. SARS-CoV-2 receptor ACE2 is an interferon-stimulated gene in human airway epithelial cells and is detected in specific cell subsets across tissues. Cell. 2020;181(5):1016–1035.e19. doi:10.1016/j.cell.2020.04.035

29. Bachert C, Desrosiers MY, Hellings PW, Laidlaw TM. The role of biologics in chronic rhinosinusitis with nasal polyps. J Allergy Clin Immunol Pract. 2021;9(3):1099–1106. doi:10.1016/j.jaip.2020.11.017

30. Förster-Ruhrmann U, Szczepek AJ, Bachert C, Olze H. COVID-19 in a patient with severe chronic rhinosinusitis with nasal polyps during therapy with dupilumab. J Allergy Clin Immunol. 2020;146(1):218–220.e2. doi:10.1016/j.jaci.2020.05.005

31. Akhlaghi A, Darabi A, Mahmoodi M, et al. The frequency and clinical assessment of COVID-19 in patients with chronic rhinosinusitis. Ear Nose Throat J. 2021;1455613211038070. doi:10.1177/01455613211038070

32. von Bartheld CS, Hagen MM, Butowt R. Prevalence of chemosensory dysfunction in COVID-19 patients: a systematic review and meta-analysis reveals significant ethnic differences. ACS Chem Neurosci. 2020;11(19):2944–2961. doi:10.1021/acschemneuro.0c00460

33. Haehner A, Draf J, Dräger S, de With K, Hummel T. Predictive value of sudden olfactory loss in the diagnosis of COVID-19. ORL. 2020;82(4):175–180. doi:10.1159/000509143

34. Gerkin RC, Ohla K, Veldhuizen MG, et al. Recent smell loss is the best predictor of COVID-19 among individuals with recent respiratory symptoms. Chem Senses. 2021;46. doi:10.1093/chemse/bjaa081

35. Pellegrino R, Cooper KW, Di Pizio A, Joseph PV, Bhutani S, Parma V. Corona viruses and the chemical senses: past, present, and future. Chem Senses. 2020;45:415–422. doi:10.1093/chemse/bjaa031

36. Parma V, Ohla K, Veldhuizen MG, et al. More than smell-COVID-19 is associated with severe impairment of smell, taste, and chemesthesis. Chem Senses. 2020;45(7):609–622. doi:10.1093/chemse/bjaa041

37. Huart C, Philpott C, Konstantinidis I, et al. Comparison of COVID-19 and common cold chemosensory dysfunction. Rhinology. 2020;58(6):623–625. doi:10.4193/Rhin20.251

38. Hannum ME, Ramirez VA, Lipson SJ, et al. 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(9):865–874. doi:10.1093/chemse/bjaa064

39. Landis BN, Hummel T, Hugentobler M, Giger R, Lacroix JS. Ratings of overall olfactory function. Chem Senses. 2003;28(8):691–694. doi:10.1093/chemse/bjg061

40. Lötsch J, Hummel T. Clinical usefulness of self-rated olfactory performance-a data science-based assessment of 6000 patients. Chem Senses. 2019;44(6):357–364. doi:10.1093/chemse/bjz029

41. de Melo GD, Lazarini F, Levallois S, et al. COVID-19-related anosmia is associated with viral persistence and inflammation in human olfactory epithelium and brain infection in hamsters. Sci Transl Med. 2021;13(596). doi:10.1126/scitranslmed.abf8396

42. Hopkins C, Lechien JR, Saussez S. More that ACE2? NRP1 may play a central role in the underlying pathophysiological mechanism of olfactory dysfunction in COVID-19 and its association with enhanced survival. Med Hypotheses. 2021;146:110406. doi:10.1016/j.mehy.2020.110406

43. Butowt R, Meunier N, Bryche B, von Bartheld CS. The olfactory nerve is not a likely route to brain infection in COVID-19: a critical review of data from humans and animal models. Acta Neuropathol. 2021;141(6):809–822. doi:10.1007/s00401-021-02314-2

44. Brann DH, Tsukahara T, Weinreb C, et al. Non-neuronal expression of SARS-CoV-2 entry genes in the olfactory system suggests mechanisms underlying COVID-19-associated anosmia. Sci Adv. 2020;6(31). doi:10.1126/sciadv.abc5801

45. Bilinska K, Jakubowska P, Von Bartheld CS, Butowt R. Expression of the SARS-CoV-2 entry proteins, ACE2 and TMPRSS2, in cells of the olfactory epithelium: identification of cell types and trends with age. ACS Chem Neurosci. 2020;11(11):1555–1562. doi:10.1021/acschemneuro.0c00210

46. Daly JL, Simonetti B, Klein K, et al. Neuropilin-1 is a host factor for SARS-CoV-2 infection. Science. 2020;370(6518):861–865. doi:10.1126/science.abd3072

47. Cantuti-Castelvetri L, Ojha R, Pedro LD, et al. Neuropilin-1 facilitates SARS-CoV-2 cell entry and infectivity. Science. 2020;370(6518):856–860. doi:10.1126/science.abd2985

48. Khan M, Yoo SJ, Clijsters M, et al. Visualizing in deceased COVID-19 patients how SARS-CoV-2 attacks the respiratory and olfactory mucosae but spares the olfactory bulb. Cell. 2021;184(24):5932–5949.e15. doi:10.1016/j.cell.2021.10.027

49. Chakrabarti A, Denning DW, Ferguson BJ, et al. Fungal rhinosinusitis: a categorization and definitional schema addressing current controversies. Laryngoscope. 2009;119(9):1809–1818. doi:10.1002/lary.20520

50. Aribandi M, McCoy VA, Bazan C. Imaging features of invasive and noninvasive fungal sinusitis: a review. Radiographics. 2007;27(5):1283–1296. doi:10.1148/rg.275065189

51. Momeni AK, Roberts CC, Chew FS. Imaging of chronic and exotic sinonasal disease: review. AJR Am J Roentgenol. 2007;189(6 Suppl):S35–S45. doi:10.2214/ajr.07.7031

52. Madney Y, Khedr R, Ahmed N, et al. Overview and outcome of mucormycosis among children with cancer: report from the Children’s Cancer Hospital Egypt. Mycoses. 2019;62(11):984–989. doi:10.1111/myc.12915

53. Prakash H, Chakrabarti A. Global epidemiology of mucormycosis. J Fungi. 2019;5(1):26. doi:10.3390/jof5010026

54. El-Kholy NA, El-Fattah AMA, Khafagy YW. Invasive fungal sinusitis in post COVID-19 patients: a new clinical entity. Laryngoscope. 2021;131(12):2652–2658. doi:10.1002/lary.29632

55. Borrelli M, Nasrollahi T, Ulloa R, Raskin J, Ference E, Tang DM. Invasive fungal sinusitis during active COVID-19 infection. Ear Nose Throat J. 2022;1455613221112337. doi:10.1177/01455613221112337

56. Ebeid K, Gamea M, Allam A, Shehata E. Impact of COVID-19 on acute invasive fungal rhinosinusitis: a comparative study. Egypt J Ear Nose Throat Allied Sci. 2021;22(22):1–7. doi:10.21608/ejentas.2021.76357.1369

57. Ismaiel WF, Abdelazim MH, Eldsoky I, et al. The impact of COVID-19 outbreak on the incidence of acute invasive fungal rhinosinusitis. Am J Otolaryngol. 2021;42(6):103080. doi:10.1016/j.amjoto.2021.103080

58. Baghel SS, Keshri AK, Mishra P, et al. The spectrum of invasive fungal sinusitis in COVID-19 patients: experience from a tertiary care referral center in Northern India. J Fungi. 2022;8(3):223. doi:10.3390/jof8030223

59. Treviño-Gonzalez JL, Santos-Santillana KM, Maldonado-Chapa F, Morales-Del Angel JA, Gomez-Castillo P, Cortes-Ponce JR. ”Chronic granulomatous invasive fungal rhinosinusitis associated with SARS-CoV-2 infection: a case report”. Ann Med Surg. 2021;72:103129. doi:10.1016/j.amsu.2021.103129

60. Mehta S, Pandey A. Rhino-orbital mucormycosis associated with COVID-19. Cureus. 2020;12(9):e10726. doi:10.7759/cureus.10726

61. Werthman-Ehrenreich A. Mucormycosis with orbital compartment syndrome in a patient with COVID-19. Am J Emerg Med. 2021;42:264.e5–264.e8. doi:10.1016/j.ajem.2020.09.032

62. Donovan MR, Miglani A, Lal D, Marino MJ. Factors associated with invasive fungal sinusitis in patients with COVID-19: a systematic review and single-center case series. Laryngosc Investig Otolaryngol. 2022;7:913–919. doi:10.1002/lio2.833

63. Sen M, Honavar SG, Bansal R, et al. Epidemiology, clinical profile, management, and outcome of COVID-19-associated rhino-orbital-cerebral mucormycosis in 2826 patients in India - Collaborative OPAI-IJO Study on Mucormycosis in COVID-19 (COSMIC), report 1. Indian J Ophthalmol. 2021;69(7):1670–1692. doi:10.4103/ijo.IJO_1565_21

64. Casalini G, Giacomelli A, Ridolfo A, Gervasoni C, Antinori S. Invasive fungal infections complicating COVID-19: a narrative review. J Fungi. 2021;7(11):921. doi:10.3390/jof7110921

65. Pakdel F, Ahmadikia K, Salehi M, et al. Mucormycosis in patients with COVID-19: a cross-sectional descriptive multicentre study from Iran. Mycoses. 2021;64(10):1238–1252. doi:10.1111/myc.13334

66. Fouad YA, Abdelaziz TT, Askoura A, et al. Spike in rhino-orbital-cerebral mucormycosis cases presenting to a tertiary care center during the COVID-19 pandemic. Front Med. 2021;8:645270. doi:10.3389/fmed.2021.645270

67. Joshi AR, Muthe MM, Patankar SH, Athawale A, Achhapalia Y. CT and MRI findings of invasive mucormycosis in the setting of COVID-19: experience from a single center in India. AJR. 2021;217(6):1431–1432. doi:10.2214/ajr.21.26205

68. Diwakar J, Samaddar A, Konar SK, et al. First report of COVID-19-associated rhino-orbito-cerebral mucormycosis in pediatric patients with type 1 diabetes mellitus. J Mycol Med. 2021;31(4):101203. doi:10.1016/j.mycmed.2021.101203

69. Ravani SA, Agrawal GA, Leuva PA, Modi PH, Amin KD. Rise of the phoenix: mucormycosis in COVID-19 times. Indian J Ophthalmol. 2021;69(6):1563–1568. doi:10.4103/ijo.IJO_310_21

70. Nehara HR, Puri I, Singhal V, Ih S, Bishnoi BR, Sirohi P. Rhinocerebral mucormycosis in COVID-19 patient with diabetes a deadly trio: case series from the north-western part of India. Indian J Med Microbiol. 2021;39(3):380–383. doi:10.1016/j.ijmmb.2021.05.009

71. Sen M, Lahane S, Lahane TP, Parekh R, Honavar SG. Mucor in a viral land: a tale of two pathogens. Indian J Ophthalmol. 2021;69(2):244–252. doi:10.4103/ijo.IJO_3774_20

72. Bhattacharyya A, Sarma P, Kaur H, et al. COVID-19-associated rhino-orbital-cerebral mucormycosis: a systematic review, meta-analysis, and meta-regression analysis. Indian J Pharmacol. 2021;53(6):499–510. doi:10.4103/ijp.ijp_839_21

73. Arjun R, Felix V, Niyas VKM, et al. COVID-19-associated rhino-orbital mucormycosis: a single-centre experience of 10 cases. QJM. 2022;114(11):831–834. doi:10.1093/qjmed/hcab176

74. Bayram N, Ozsaygılı C, Sav H, et al. Susceptibility of severe COVID-19 patients to rhino-orbital mucormycosis fungal infection in different clinical manifestations. Jpn J Ophthalmol. 2021;65(4):515–525. doi:10.1007/s10384-021-00845-5

75. Kursun E, Turunc T, Demiroglu YZ, Alışkan HE, Arslan AH. Evaluation of 28 cases of mucormycosis. Mycoses. 2015;58(2):82–87. doi:10.1111/myc.12278

76. Vaezi A, Moazeni M, Rahimi MT, de Hoog S, Badali H. Mucormycosis in Iran: a systematic review. Mycoses. 2016;59(7):402–415. doi:10.1111/myc.12474

77. Saedi B, Sadeghi M, Seilani P. Endoscopic management of rhinocerebral mucormycosis with topical and intravenous amphotericin B. J Laryngol Otol. 2011;125(8):807–810. doi:10.1017/s0022215111001289

78. Mohammadi R, Meidani M, Mostafavizadeh K, et al. Case series of rhinocerebral mucormycosis occurring in diabetic patients. Caspian J Intern Med. 2015;6(4):243–246.

79. Ketenci I, Unlü Y, Kaya H, et al. Rhinocerebral mucormycosis: experience in 14 patients. J Laryngol Otol. 2011;125(8):e3. doi:10.1017/s0022215111000843

80. Kermani W, Bouttay R, Belcadhi M, Zaghouani H, Ben Ali M, Abdelkéfi M. ENT mucormycosis. Report of 4 cases. Eur Ann Otorhinolaryngol Head Neck Dis. 2016;133(2):83–86. doi:10.1016/j.anorl.2015.08.027

81. Bellazreg F, Hattab Z, Meksi S, et al. Outcome of mucormycosis after treatment: report of five cases. N Microbes N Infect. 2015;6:49–52. doi:10.1016/j.nmni.2014.12.002

82. Turner JH, Soudry E, Nayak JV, Hwang PH. Survival outcomes in acute invasive fungal sinusitis: a systematic review and quantitative synthesis of published evidence. Laryngoscope. 2013;123(5):1112–1118. doi:10.1002/lary.23912

83. Hegazi R, El-Gamal M, Abdel-Hady N, Hamdy O. Epidemiology of and risk factors for type 2 diabetes in Egypt. Ann Glob Health. 2015;81(6):814–820. doi:10.1016/j.aogh.2015.12.011

84. Bakhshaee M, Bojdi A, Allahyari A, et al. Acute invasive fungal rhinosinusitis: our experience with 18 cases. Eur Archiv Oto-Rhino-Laryngol. 2016;273(12):4281–4287. doi:10.1007/s00405-016-4109-z

85. Bala K, Chander J, Handa U, Punia RS, Attri AK. A prospective study of mucormycosis in north India: experience from a tertiary care hospital. Med Mycol. 2015;53(3):248–257. doi:10.1093/mmy/myu086

86. Tamez-Pérez HE, Quintanilla-Flores DL, Rodríguez-Gutiérrez R, González-González JG, Tamez-Peña AL. Steroid hyperglycemia: prevalence, early detection and therapeutic recommendations: a narrative review. World J Diabetes. 2015;6(8):1073–1081. doi:10.4239/wjd.v6.i8.1073

87. Dallalzadeh LO, Ozzello DJ, Liu CY, Kikkawa DO, Korn BS. Secondary infection with rhino-orbital cerebral mucormycosis associated with COVID-19. Orbit. 2021;2021:1–4.

88. Juneja D, Jain R, Singh O. Practice pattern of critical care physicians in India for use of corticosteroids in COVID-19. J Assoc Physicians India. 2021;69(5):50–55.

89. Jagiasi B, Nasa P, Chanchalani G, et al. Variation in therapeutic strategies for the management of severe COVID-19 in India: a nationwide cross-sectional survey. Int J Clin Pract. 2021;75(10):e14574. doi:10.1111/ijcp.14574

90. Pradhan P, Shaikh Z, Mishra A, et al. Predisposing factors of rhino-orbital-cerebral mucormycosis in patients with COVID 19 infection. Indian J Otolaryngol Head Neck Surg. 2021;2021:1–7.

91. Moorthy A, Gaikwad R, Krishna S, et al. SARS-CoV-2, uncontrolled diabetes and corticosteroids-an unholy trinity in invasive fungal infections of the maxillofacial region? A retrospective, multi-centric analysis. J Maxillofac Oral Surg. 2021;20(3):418–425. doi:10.1007/s12663-021-01532-1

92. Singh AK, Singh R, Joshi SR, Misra A. Mucormycosis in COVID-19: a systematic review of cases reported worldwide and in India. Diabetes Metab Syndr. 2021;15(4):102146. doi:10.1016/j.dsx.2021.05.019

93. Nayak PS, Katyal I, Kumar AD, Prasheetha B, Harugop AS, Reshma R. COVID 19 associated mucormycosis: preventable risk factors leading to a better prognosis: a case series. Indian J Otolaryngol Head Neck Surg. 2022;74(2):3536–3540. doi:10.1007/s12070-022-03163-5

94. Anand CB, Senthilkumar S, Ibrahim PN, et al. Estimation of serum ferritin in mucormycosis patients and prognostication based on the ferritin value. Cureus. 2022;14(4):e24013. doi:10.7759/cureus.24013

95. Rao C. Association of serum iron studies in COVID associated mucormycosis with stage of the disease. J Assoc Physicians India. 2022;70(4):11–12.

96. Bhadania S, Bhalodiya N, Sethi Y, et al. Hyperferritinemia and the extent of mucormycosis in COVID-19 patients. Cureus. 2021;13(12):e20569. doi:10.7759/cureus.20569

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