The Incidence and Characteristics of Oral Candidiasis in Patients Hospitalized for SARS-CoV-2 Infection During the Circulation of Alpha, Beta, and Delta Variants
Abstract
1. Introduction
2. Methods
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Stein, R.A.; Ometa, O.; Broker, T.R. COVID-19: The Pseudo-Environment and the Need for a Paradigm Change. Germs 2021, 11, 468–477. [Google Scholar] [CrossRef] [PubMed]
- Ayenigbara, I.O.; Adeleke, O.R.; Ayenigbara, G.O.; Adegboro, J.S.; Olofintuyi, O.O. COVID-19 (SARS-CoV-2) pandemic: Fears, facts and preventive measures. Germs 2020, 10, 218–228. [Google Scholar] [CrossRef] [PubMed]
- Preda, M.; Dinu, R.S.; Prasacu, I.; Manolescu, L.S.C. SARS-CoV-2 Infection Anxiety, Knowledge and Attitudes in University Degree Pregnant Women from Romania-A Cross-Sectional Observational Survey in the First Two Pandemic Years. Vaccines 2022, 11, 35. [Google Scholar] [CrossRef] [PubMed]
- Long, B.; Carius, B.M.; Chavez, S.; Liang, S.Y.; Brady, W.J.; Koyfman, A.; Gottlieb, M. Clinical update on COVID-19 for the emergency clinician: Presentation and evaluation. Am. J. Emerg. Med. 2022, 54, 46–57. [Google Scholar] [CrossRef]
- Hassine, I.H. COVID-19 vaccines and variants of concern: A review. Rev. Med. Virol. 2022, 32, e2313. [Google Scholar] [CrossRef]
- Dumea, E.; Barbu, E.C.; Chitu, C.E.; Lazar, M.; Ion, D.A. Clinical, biochemical and pulmonary CT imaging features for hepatobiliary involvement in COVID-19. Germs 2023, 13, 121–129. [Google Scholar] [CrossRef]
- Novelli, G.; Moretti, M.; Meazzini, M.C.; Bernasconi, D.P.; Malandrin, S.M.I.; Raggi, M.; Cassé, C.M.A.; Pavesi, L.A.; Sozzi, D. The analysis of saliva as screening in patients with COVID-like symptoms. Germs 2023, 13, 388–391. [Google Scholar] [CrossRef]
- Somero, M.; Akagi, E.; Bhargava, A. Facial nerve palsy: An early sign of COVID-19. Germs 2023, 13, 60–64. [Google Scholar] [CrossRef]
- Glavina, A.; Badrov, J.; Lukenda, M.; Dzaja, K.; Biocina-Lukenda, D.; Lugovic-Mihic, L. COVID-19 and oral lesions: 2020–2024 outpatient case series and literature review. Acta Dermatovenerol. Alp. Pannonica Adriat. 2024, 33, 41–48. [Google Scholar] [CrossRef]
- Sandulescu, O.; Sandulescu, M. The 5Ds of optimized antimicrobial prescription in dental medicine. Germs 2023, 13, 207–209. [Google Scholar] [CrossRef]
- Prakash, K.; Bindu, R.; Sanoj, N.M. Prevalence of Oral Manifestations in COVID-19-Diagnosed Patients at a Tertiary Care Hospital in Kerala. J. Maxillofac. Oral Surg. 2023, 23, 296–300. [Google Scholar] [CrossRef] [PubMed]
- Vila, T.; Sultan, A.S.; Montelongo-Jauregui, D.; Jabra-Rizk, M.A. Oral Candidiasis: A Disease of Opportunity. J. Fungi 2020, 6, 15. [Google Scholar] [CrossRef] [PubMed]
- Nicolescu, M.I.; Balanici, A.M. Competition for tooth surface—Microbial Olympics. Germs 2024, 14, 9–10. [Google Scholar] [CrossRef] [PubMed]
- Iosif, L.; Tancu, A.M.C.; Amza, O.E.; Dimitriu, B.; Ispas, A.; Pantea, M.; Imre, M. Qualitative assessment of the removable denture microbiome. Germs 2024, 14, 28–37. [Google Scholar] [CrossRef]
- Iranmanesh, B.; Khalili, M.; Amiri, R.; Zartab, H.; Aflatoonian, M. Oral manifestations of COVID-19 disease: A review article. Dermatol. Ther. 2021, 34, e14578. [Google Scholar] [CrossRef]
- Salehi, M.; Ahmadikia, K.; Badali, H.; Khodavaisy, S. Opportunistic Fungal Infections in the Epidemic Area of COVID-19: A Clinical and Diagnostic Perspective from Iran. Mycopathologia 2020, 185, 607–611. [Google Scholar] [CrossRef]
- Alfaifi, A.A.; Wang, T.W.; Perez, P.; Sultan, A.S.; Meiller, T.F.; Rock, P.; Kleiner, D.E.; Chertow, D.S.; Hewitt, S.M.; Gasmi, B.; et al. SARS-CoV-2 Infection of Salivary Glands Compromises Oral Antifungal Innate Immunity and Predisposes to Oral Candidiasis. bioRxiv 2024. [Google Scholar] [CrossRef]
- Ahmed, N.; Mahmood, M.S.; Ullah, A.; Araf, Y.; Rahaman, T.I.; Moin, A.T.; Hosen, M.J. COVID-19-Associated Candidiasis: Possible Patho-Mechanism, Predisposing Factors, and Prevention Strategies. Curr. Microbiol. 2022, 79, 127. [Google Scholar] [CrossRef]
- Chen, X.; Liao, B.; Cheng, L.; Peng, X.; Xu, X.; Li, Y.; Hu, T.; Li, J.; Zhou, X.; Ren, B. The microbial coinfection in COVID-19. Appl. Microbiol. Biotechnol. 2020, 104, 7777–7785. [Google Scholar] [CrossRef]
- Ministry of Health. Ordin nr. 260 din 4 Februarie 2022–Privind Modificarea Anexei la Ordinul Ministrului Sănătății nr. 487/2020 Pentru Aprobarea Protocolului de Tratament al Infecției cu Virusul SARS-CoV-2; Ministry of Health: Bucharest, Romania, 2022.
- Streinu-Cercel, A.; Miron, V.D.; Oană, A.A.; Irimia, M.; Popescu, R.Ș.; Dărămuș, I.A.; Moțoi, M.M.; Ceapraga, G.J.; Săndulescu, O. Real-World Use of Molnupiravir in the Treatment of Outpatients with SARS-CoV-2 Infection-A Patient Profile Based on the Experience of a Tertiary Infectious Disease Center. Pharmaceuticals 2022, 15, 1065. [Google Scholar] [CrossRef]
- Di Spirito, F.; Iandolo, A.; Amato, A.; Caggiano, M.; Raimondo, A.; Lembo, S.; Martina, S. Prevalence, Features and Degree of Association of Oral Lesions in COVID-19: A Systematic Review of Systematic Reviews. Int. J. Environ. Res. Public Health 2022, 19, 7486. [Google Scholar] [CrossRef] [PubMed]
- Babamahmoodi, F.; Rezai, M.S.; Ahangarkani, F.; Kali, A.M.; Alizadeh-Navaei, R.; Alishahi, A.; Najafi, N.; Haddadi, A.; Davoudi, A.; Azargon, L.; et al. Multiple Candida strains causing oral infection in COVID-19 patients under corticosteroids and antibiotic therapy: An observational study. Front. Cell. Infect. Microbiol. 2022, 12, 1103226. [Google Scholar] [CrossRef] [PubMed]
- Salehi, M.; Ahmadikia, K.; Mahmoudi, S.; Kalantari, S.; Jamalimoghadamsiahkali, S.; Izadi, A.; Kord, M.; Manshadi, S.A.D.; Seifi, A.; Ghiasvand, F.; et al. Oropharyngeal candidiasis in hospitalised COVID-19 patients from Iran: Species identification and antifungal susceptibility pattern. Mycoses 2020, 63, 771–778. [Google Scholar] [CrossRef] [PubMed]
- Riad, A.; Gomaa, E.; Hockova, B.; Klugar, M. Oral candidiasis of COVID-19 patients: Case report and review of evidence. J. Cosmet. Dermatol. 2021, 20, 1580–1584. [Google Scholar] [CrossRef]
- Pisano, M.; Romano, A.; Di Palo, M.P.; Baroni, A.; Serpico, R.; Contaldo, M. Oral Candidiasis in Adult and Pediatric Patients with COVID-19. Biomedicines 2023, 11, 846. [Google Scholar] [CrossRef]
- Salehi, M.; Khajavirad, N.; Darazam, I.A.; Hashemi, S.J.; Ansari, S.; Ghiasvand, F.; Jamalimoghadamsiahkali, S.; Izadi, A.; Kiyaei, R.S.; Seifi, A.; et al. Risk Factors of Oropharyngeal Candidiasis in COVID-19 Patients: A Case-control Study. Arch. Clin. Infect. Dis. 2021, 16, e114631. [Google Scholar] [CrossRef]
- Negm, E.M.; Mohamed, M.S.; Rabie, R.A.; Fouad, W.S.; Beniamen, A.; Mosallem, A.; Tawfik, A.E.; Salama, H.M. Fungal infection profile in critically ill COVID-19 patients: A prospective study at a large teaching hospital in a middle-income country. BMC Infect. Dis. 2023, 23, 246. [Google Scholar] [CrossRef]
- Winning, L.; Lundy, F.T.; Blackwood, B.; McAuley, D.F.; El Karim, I. Oral health care for the critically ill: A narrative review. Crit. Care 2021, 25, 353. [Google Scholar] [CrossRef]
- Jeronimo, L.S.; Esteves Lima, R.P.; Suzuki, T.Y.U.; Discacciati, J.A.C.; Bhering, C.L.B. Oral Candidiasis and COVID-19 in Users of Removable Dentures: Is Special Oral Care Needed? Gerontology 2022, 68, 80–85. [Google Scholar] [CrossRef]
- Preda, M.; Chivu, R.D.; Ditu, L.M.; Popescu, O.; Manolescu, L.S.C. Pathogenesis, Prophylaxis, and Treatment of Candida auris. Biomedicines 2024, 12, 561. [Google Scholar] [CrossRef]
- Mba, I.E.; Nweze, E.I. Mechanism of Candida pathogenesis: Revisiting the vital drivers. Eur. J. Clin. Microbiol. Infect. Dis. 2020, 39, 1797–1819. [Google Scholar] [CrossRef] [PubMed]
- Sandulescu, O.; Sandulescu, M. Oral biofilms—Pivotal role in understanding microbes and their relevance to the human host. Germs 2023, 13, 7–9. [Google Scholar] [CrossRef] [PubMed]
- Segrelles-Calvo, G.; Araújo, G.R.d.S.; Frases, S. Systemic mycoses: A potential alert for complications in COVID-19 patients. Future Microbiol. 2020, 15, 1405–1413. [Google Scholar] [CrossRef] [PubMed]
- Farhan, M.A.; Moharram, A.M.; Salah, T.; Shaaban, O.M. Types of yeasts that cause vulvovaginal candidiasis in chronic users of corticosteroids. Med. Mycol. 2019, 57, 681–687. [Google Scholar] [CrossRef]
- Drăgănescu, A.C.; Miron, V.D.; Săndulescu, O.; Bilaşco, A.; Streinu-Cercel, A.; Sandu, R.G.; Marinescu, A.; Gunșahin, D.; Hoffmann, K.I.; Horobeț, D.Ș.; et al. Omicron in Infants—Respiratory or Digestive Disease? Diagnostics 2023, 13, 421. [Google Scholar] [CrossRef]
- Rocha, F.A.C.; Alves, A.M.C.V.; Rocha, M.F.G.; Cordeiro, R.d.A.; Brilhante, R.S.N.; Pinto, A.C.M.D.; Nunes, R.d.M.; Girão, V.C.C.; Sidrim, J.J.C. Tumor necrosis factor prevents Candida albicans biofilm formation. Sci. Rep. 2017, 7, 1206. [Google Scholar] [CrossRef]
- Kazancioglu, S.; Bodur, H.; Mumcuoglu, I.; Bastug, A.; Ozbay, B.O.; Aydos, O.; Dinc, B. Candidemia in critically ill COVID-19 patients: Risk factors and impact on mortality. Heliyon 2024, 10, e28033. [Google Scholar] [CrossRef]
- Ortega-Loubon, C.; Cano-Hernández, B.; Poves-Alvarez, R.; Muñoz-Moreno, M.F.; Román-García, P.; Balbás-Alvarez, S.; de la Varga-Martínez, O.; Gómez-Sánchez, E.; Gómez-Pesquera, E.; Lorenzo-López, M.; et al. The Overlooked Immune State in Candidemia: A Risk Factor for Mortality. J. Clin. Med. 2019, 8, 1512. [Google Scholar] [CrossRef]
- Xiao, J.L.; Xu, G.C.; de Hoog, S.; Qiao, J.J.; Fang, H.; Li, Y.L. Oral Prevalence of Candida Species in Patients Undergoing Systemic Glucocorticoid Therapy and the Antifungal Sensitivity of the Isolates. Infect. Drug Resist. 2020, 13, 2601–2607. [Google Scholar] [CrossRef]
- Garcia-Cuesta, C.; Sarrion-Perez, M.G.; Bagan, J.V. Current treatment of oral candidiasis: A literature review. J. Clin. Exp. Dent. 2014, 6, e576–e582. [Google Scholar] [CrossRef]
Characteristics | All Patients | Group with Oral Candidiasis | Group without Oral Candidiasis | p-Value |
---|---|---|---|---|
N = 294 | N = 50 | N = 244 | ||
Demographic data | ||||
Female | 147 (50.0%) | 31 (62.0%) | 116 (47.5%) | 0.062 |
Age, years, median (IQR) | 52 (43, 64) | 55.5 (47, 69) | 51.5 (42, 63) | 0.052 |
SARS-CoV-2 variant | ||||
Alpha | 52 (17.7%) | 4 (8.0%) | 48 (19.7%) | 0.143 |
Beta | 157 (53.4%) | 30 (60.0%) | 127 (52.0%) | |
Delta | 85 (28.9%) | 16 (32.0%) | 69 (28.3%) | |
Disease form | ||||
Moderate | 106 (36.1%) | 7 (14.0%) | 99 (40.6%) | <0.001 |
Severe | 188 (63.9%) | 43 (86.0%) | 145 (59.4%) | |
Chronic condition | ||||
At least one chronic condition | 218 (74.1%) | 40 (80.0%) | 178 (73.0%) | 0.300 |
Obesity | 158 (53.7%) | 30 (60.0%) | 128 (52.5%) | 0.330 |
High blood pressure | 146 (49.7%) | 30 (60.0%) | 116 (47.5%) | 0.108 |
Diabetes mellitus | 57 (19.4%) | 12 (24.0%) | 45 (18.4%) | 0.365 |
Cardiovascular disease | 108 (36.7%) | 19 (38.0%) | 89 (36.5%) | 0.839 |
Chronic lung disease | 17 (5.8%) | 4 (8.0%) | 13 (5.3%) | 0.461 |
Chronic kidney disease | 14 (4.8%) | 3 (6.0%) | 11 (4.5%) | 0.652 |
Neurological diseases | 15 (5.1%) | 3 (6.0%) | 12 (4.9%) | 0.751 |
Feature | All Patients | Group with Oral Candidiasis | Group without Oral Candidiasis | p-Value |
---|---|---|---|---|
N = 294 | N = 50 | N = 244 | ||
Neutrophil count, cells/µL, median (IQR) | 4100 (2800, 6425) | 4950 (3125, 7470) | 3970 (2705, 6375) | 0.069 |
Increased neutrophil count, n (%) | 67 (22.8%) | 16 (32.0%) | 51 (20.9%) | 0.088 |
Decreased neutrophil count, n (%) | 13 (4.4%) | 0 (0.0%) | 13 (5.3%) | NA |
Lymphocyte count, cells/µL, median (IQR) | 900 (615, 1200) | 720 (600, 1100) | 900 (640, 1200) | 0.168 |
Increased lymphocyte count, n (%) | 5 (1.7%) | 2 (4.0%) | 3 (1.2%) | 0.167 |
Decreased lymphocyte count, n (%) | 228 (77.6%) | 41 (82.0%) | 187 (76.6%) | 0.408 |
Fibrinogen, mg/dL, median (IQR) | 485 (387, 577.3) | 519.5 (447.5, 607.5) | 474.5 (370, 560.8) | 0.048 |
Increased fibrinogen, n (%) | 218 (74.1%) | 42 (84.0%) | 176 (72.1%) | 0.081 |
C-reactive protein, mg/L, median (IQR) | 71 (30.8, 110) | 81.5 (44.5, 143.3) | 70 (28, 107.5) | 0.026 |
Increased C-reactive protein, n (%) | 284 (96.6%) | 50 (100%) | 234 (95.9%) | 0.145 |
IL-1, pg/L, median (IQR) | 2.4 (0.2, 7.0) | 2.8 (0.5, 10.3) | 2.4 (0.2, 6.3) | 0.460 |
Increased IL-1, n (%) | 91 (31.0%) | 17 (34.0%) | 74 (30.3%) | 0.609 |
IL-6, pg/L, median (IQR) | 59.5 (15.8, 220) | 77.5 (10.9, 709.1) | 53.5 (16, 182) | 0.189 |
Increased IL-6, n (%) | 216 (73.5%) | 37 (74.0%) | 179 (73.4%) | 0.926 |
LDH, U/L, median (IQR) | 315 (250.8, 400.5) | 375 (311.8, 486.8) | 306 (245.3, 381.5) | <0.001 |
Increased LDH, n (%) | 226 (76.9%) | 44 (88.0%) | 182 (74.6%) | 0.040 |
Ferritin, ng/mL, median (IQR) | 563 (263.3, 1267) | 841 (463.3, 1650) | 540.5 (240.3, 1212.8) | 0.007 |
Increased ferritin, n (%) | 205 (69.7%) | 43 (86.0%) | 162 (66.4%) | 0.006 |
AST, U/L, median (IQR) | 54 (35, 79) | 60.5 (39.8, 83) | 53.5 (34, 76) | 0.130 |
Increased AST, n (%) | 137 (46.6%) | 27 (54.0%) | 110 (45.1%) | 0.249 |
ALT, U/L, median (IQR) | 76 (40.8, 124.5) | 80 (58.8, 140.3) | 76 (38, 120) | 0.224 |
Increased ALT, n (%) | 178 (60.5%) | 36 (73.5%) | 142 (58.7%) | 0.053 |
Amylase, U/L, median (IQR) | 67.5 (48.8, 99) | 72.5 (51.8, 99) | 66 (48, 99) | 0.839 |
Increased amylase, n (%) | 65 (22.1%) | 10 (20.0%) | 55 (22.5%) | 0.693 |
Lipase, U/L, median (IQR) | 167.5 (106.8, 298.5) | 175.5 (100.8, 319) | 166.5 (109.3, 290.5) | 0.626 |
Increased lipase, n (%) | 74 (25.2%) | 15 (30.0%) | 59 (24.2%) | 0.388 |
Feature | All Patients | Group with Oral Candidiasis | Group without Oral Candidiasis | p-Value |
---|---|---|---|---|
N = 294 | N = 50 | N = 244 | ||
Treatment | ||||
Antibiotics | 259 (88.1%) | 49 (98.0%) | 210 (86.1%) | 0.017 |
Biological therapy | 139 (47.3%) | 27 (54.0%) | 112 (45.9%) | 0.239 |
Corticosteroids | 254 (86.4%) | 50 (100%) | 204 (83.6%) | 0.003 |
Anticoagulants | 292 (99.3%) | 50 (100%) | 242 (99.2%) | 0.521 |
Antifungal therapy | 70 (23.8%) | 45 (90.0%) | 25 (10.2%) | <0.001 |
Evolution | ||||
Days since onset, median (IQR) | 7 (5, 10) | 7 (6, 10) | 7 (5, 9) | 0.219 |
Duration of hospitalization, days, median (IQR) | 10 (7, 14) | 12.5 (9, 18.25) | 9.5 (7, 13.75) | 0.001 |
Respiratory failure, n (%) | 193 (65.6%) | 44 (88.0%) | 149 (61.1%) | <0.001 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Kouris, E.C.; Mirea, S.I.; Luminos, M.L.; Miron, V.D. The Incidence and Characteristics of Oral Candidiasis in Patients Hospitalized for SARS-CoV-2 Infection During the Circulation of Alpha, Beta, and Delta Variants. Microorganisms 2024, 12, 2090. https://doi.org/10.3390/microorganisms12102090
Kouris EC, Mirea SI, Luminos ML, Miron VD. The Incidence and Characteristics of Oral Candidiasis in Patients Hospitalized for SARS-CoV-2 Infection During the Circulation of Alpha, Beta, and Delta Variants. Microorganisms. 2024; 12(10):2090. https://doi.org/10.3390/microorganisms12102090
Chicago/Turabian StyleKouris, Elena Camelia, Sînziana Irina Mirea, Monica Luminița Luminos, and Victor Daniel Miron. 2024. "The Incidence and Characteristics of Oral Candidiasis in Patients Hospitalized for SARS-CoV-2 Infection During the Circulation of Alpha, Beta, and Delta Variants" Microorganisms 12, no. 10: 2090. https://doi.org/10.3390/microorganisms12102090
APA StyleKouris, E. C., Mirea, S. I., Luminos, M. L., & Miron, V. D. (2024). The Incidence and Characteristics of Oral Candidiasis in Patients Hospitalized for SARS-CoV-2 Infection During the Circulation of Alpha, Beta, and Delta Variants. Microorganisms, 12(10), 2090. https://doi.org/10.3390/microorganisms12102090