Skip to main content
Top
Published in: BMC Oral Health 1/2023

Open Access 01-12-2023 | COVID-19 | Research

Association between the severity of periodontitis, COVID-19, C-reactive protein and interleukin-6 levels in hospitalized patients: a case‒control study

Authors: Janet Moradi Haghgoo, Parviz Torkzaban, Maryam Farhadian, Sayed Ali Moosavi Sedeh

Published in: BMC Oral Health | Issue 1/2023

Login to get access

Abstract

Background

The COVID-19 pandemic is perhaps one of the most important events of the 21st century. Periodontitis is one of the most prevalent diseases of the oral cavity. Due to possible pathways of interaction between these two diseases, we investigated their association.

Methods

The study population consisted of hospitalized patients with established COVID-19 diagnoses. Patients with mild to moderate COVID-19 were considered controls, while cases had severe to critical COVID-19. Periodontal examination and serum and saliva sampling were performed for each patient. Relevant medical data were extracted from patients’ hospital files.

Results

Of the enrolled patients, 122 were included in the statistical analyses. The severity of periodontitis was directly and significantly correlated with the severity of COVID-19 (P < 0.001). Patients with generalized stage III or IV periodontitis displayed an adjusted odds ratio of 4.24 for severe to critical COVID-19. Salivary and serum interleukin-6 levels were significantly associated with COVID-19 severity (P values: 0.002 and 0.004, respectively). Hospitalization length was significantly associated with the severity of periodontitis (P = 0.004). Clinical attachment level and gingival index were associated with increased odds for adverse events (P values: 0.004 and 0.035, respectively), while number of remaining teeth was associated with decreased odds for adverse events (P = 0.023).

Conclusions

This study showed that the severity of periodontitis is associated with the severity of COVID-19. This association might manifest as increased odds of adverse events. COVID-19 severity was associated with higher levels of salivary and serum interleukin-6 levels.
Literature
1.
go back to reference Corman VM, Lienau J, Witzenrath M. Coronaviruses as the cause of respiratory infections. Internist (Berl). 2019;60(11):1136–45.PubMed Corman VM, Lienau J, Witzenrath M. Coronaviruses as the cause of respiratory infections. Internist (Berl). 2019;60(11):1136–45.PubMed
2.
go back to reference Fehr AR, Channappanavar R, Perlman S. Middle East Respiratory Syndrome: Emergence of a Pathogenic Human Coronavirus. Annu Rev Med. 2017;68(1):387–99.PubMed Fehr AR, Channappanavar R, Perlman S. Middle East Respiratory Syndrome: Emergence of a Pathogenic Human Coronavirus. Annu Rev Med. 2017;68(1):387–99.PubMed
3.
go back to reference Chan JFW, Yuan S, Kok KH, To KKW, Chu H, Yang J, Xing F, Liu J, Yip CCY, Poon RWS, et al. A familial cluster of pneumonia associated with the 2019 novel coronavirus indicating person-to-person transmission: a study of a family cluster. Lancet. 2020;395(10223):514–23.PubMedPubMedCentral Chan JFW, Yuan S, Kok KH, To KKW, Chu H, Yang J, Xing F, Liu J, Yip CCY, Poon RWS, et al. A familial cluster of pneumonia associated with the 2019 novel coronavirus indicating person-to-person transmission: a study of a family cluster. Lancet. 2020;395(10223):514–23.PubMedPubMedCentral
6.
go back to reference Hoffmann M, Kleine-Weber H, Schroeder S, Krüger N, Herrler T, Erichsen S, Schiergens TS, Herrler G, Wu NH, Nitsche A. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell. 2020;181(2):271–80.PubMedPubMedCentral Hoffmann M, Kleine-Weber H, Schroeder S, Krüger N, Herrler T, Erichsen S, Schiergens TS, Herrler G, Wu NH, Nitsche A. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell. 2020;181(2):271–80.PubMedPubMedCentral
7.
go back to reference Wang K, Chen W, Zhou YS, Lian JQ, Zhang Z, Du P, Gong L, Zhang Y, Cui HY, Geng JJ, et al. SARS-CoV-2 invades host cells via a novel route: CD147-spike protein. Signal Transduct Target Ther. 2020;5:283.PubMedPubMedCentral Wang K, Chen W, Zhou YS, Lian JQ, Zhang Z, Du P, Gong L, Zhang Y, Cui HY, Geng JJ, et al. SARS-CoV-2 invades host cells via a novel route: CD147-spike protein. Signal Transduct Target Ther. 2020;5:283.PubMedPubMedCentral
8.
go back to reference Bordallo B, Bellas M, Cortez AF, Vieira M, Pinheiro M. Severe COVID-19: what have we learned with the immunopathogenesis? Adv Rheumatol. 2020;60(1):50.PubMedPubMedCentral Bordallo B, Bellas M, Cortez AF, Vieira M, Pinheiro M. Severe COVID-19: what have we learned with the immunopathogenesis? Adv Rheumatol. 2020;60(1):50.PubMedPubMedCentral
9.
go back to reference Wu Z, McGoogan JM. Characteristics of and Important Lessons From the Coronavirus Disease 2019 (COVID-19) Outbreak in China: Summary of a Report of 72 314 Cases From the Chinese Center for Disease Control and Prevention. JAMA. 2020;323(13):1239–42.PubMed Wu Z, McGoogan JM. Characteristics of and Important Lessons From the Coronavirus Disease 2019 (COVID-19) Outbreak in China: Summary of a Report of 72 314 Cases From the Chinese Center for Disease Control and Prevention. JAMA. 2020;323(13):1239–42.PubMed
10.
go back to reference Chen I-Y, Moriyama M, Chang M-F, Ichinohe T. Severe acute respiratory syndrome coronavirus viroporin 3a activates the NLRP3 inflammasome. Front Microbiol. 2019;10:50.PubMedCentral Chen I-Y, Moriyama M, Chang M-F, Ichinohe T. Severe acute respiratory syndrome coronavirus viroporin 3a activates the NLRP3 inflammasome. Front Microbiol. 2019;10:50.PubMedCentral
11.
go back to reference Iwasaki A, Yang Y. The potential danger of suboptimal antibody responses in COVID-19. Nat Rev Immunol. 2020;20(6):339–41.PubMedCentral Iwasaki A, Yang Y. The potential danger of suboptimal antibody responses in COVID-19. Nat Rev Immunol. 2020;20(6):339–41.PubMedCentral
12.
go back to reference Henderson LA, Canna SW, Schulert GS, Volpi S, Lee PY, Kernan KF, Caricchio R, Mahmud S, Hazen MM, Halyabar O, et al. On the Alert for Cytokine Storm: Immunopathology in COVID-19. Arthritis Rheumatol. 2020;72(7):1059–63.PubMedPubMedCentral Henderson LA, Canna SW, Schulert GS, Volpi S, Lee PY, Kernan KF, Caricchio R, Mahmud S, Hazen MM, Halyabar O, et al. On the Alert for Cytokine Storm: Immunopathology in COVID-19. Arthritis Rheumatol. 2020;72(7):1059–63.PubMedPubMedCentral
13.
go back to reference Richardson S, Hirsch JS, Narasimhan M, Crawford JM, McGinn T, Davidson KW, the Northwell C-RC. Presenting Characteristics, Comorbidities, and Outcomes Among 5700 Patients Hospitalized With COVID-19 in the New York City Area. JAMA. 2020;323(20):2052–9.PubMedPubMedCentral Richardson S, Hirsch JS, Narasimhan M, Crawford JM, McGinn T, Davidson KW, the Northwell C-RC. Presenting Characteristics, Comorbidities, and Outcomes Among 5700 Patients Hospitalized With COVID-19 in the New York City Area. JAMA. 2020;323(20):2052–9.PubMedPubMedCentral
14.
go back to reference Petersen PE, Ogawa H. The global burden of periodontal disease: towards integration with chronic disease prevention and control. Periodontology 2000. 2012;60(1):15–39. Petersen PE, Ogawa H. The global burden of periodontal disease: towards integration with chronic disease prevention and control. Periodontology 2000. 2012;60(1):15–39.
15.
go back to reference James SL, Abate D, Abate KH, Abay SM, Abbafati C, Abbasi N, Abbastabar H, Abd-Allah F, Abdela J, Abdelalim A, et al. Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. The Lancet. 2018;392(10159):1789–858. James SL, Abate D, Abate KH, Abay SM, Abbafati C, Abbasi N, Abbastabar H, Abd-Allah F, Abdela J, Abdelalim A, et al. Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. The Lancet. 2018;392(10159):1789–858.
16.
go back to reference Curtis MA, Diaz PI, Van Dyke TE. The role of the microbiota in periodontal disease. Periodontology 2000. 2020;83(1):14–25. Curtis MA, Diaz PI, Van Dyke TE. The role of the microbiota in periodontal disease. Periodontology 2000. 2020;83(1):14–25.
17.
go back to reference Page RC, Kornman KS. The pathogenesis of human periodontitis: an introduction. Periodontology 2000. 1997;14(1):9–11.PubMed Page RC, Kornman KS. The pathogenesis of human periodontitis: an introduction. Periodontology 2000. 1997;14(1):9–11.PubMed
18.
go back to reference Campisi G, Bizzoca ME, Lo Muzio L. COVID-19 and periodontitis: reflecting on a possible association. Head Face Med. 2021;17(1):16.PubMedCentral Campisi G, Bizzoca ME, Lo Muzio L. COVID-19 and periodontitis: reflecting on a possible association. Head Face Med. 2021;17(1):16.PubMedCentral
19.
go back to reference Gupta S, Mohindra R, Chauhan PK, Singla V, Goyal K, Sahni V, Gaur R, Verma DK, Ghosh A, Soni RK, et al. SARS-CoV-2 Detection in Gingival Crevicular Fluid. J Dent Res. 2021;100(2):187–93. Gupta S, Mohindra R, Chauhan PK, Singla V, Goyal K, Sahni V, Gaur R, Verma DK, Ghosh A, Soni RK, et al. SARS-CoV-2 Detection in Gingival Crevicular Fluid. J Dent Res. 2021;100(2):187–93.
20.
go back to reference Górska R, Gregorek H, Kowalski J, Laskus-Perendyk A, Syczewska M, Madaliński K. Relationship between clinical parameters and cytokine profiles in inflamed gingival tissue and serum samples from patients with chronic periodontitis. J Clin Periodontol. 2003;30(12):1046–52. Górska R, Gregorek H, Kowalski J, Laskus-Perendyk A, Syczewska M, Madaliński K. Relationship between clinical parameters and cytokine profiles in inflamed gingival tissue and serum samples from patients with chronic periodontitis. J Clin Periodontol. 2003;30(12):1046–52.
21.
go back to reference Sanz M, Ceriello A, Buysschaert M, Chapple I, Demmer RT, Graziani F, Herrera D, Jepsen S, Lione L, Madianos P. Scientific evidence on the links between periodontal diseases and diabetes: Consensus report and guidelines of the joint workshop on periodontal diseases and diabetes by the International Diabetes Federation and the European Federation of Periodontology. Diabetes Res Clin Pract. 2018;137:231–41. Sanz M, Ceriello A, Buysschaert M, Chapple I, Demmer RT, Graziani F, Herrera D, Jepsen S, Lione L, Madianos P. Scientific evidence on the links between periodontal diseases and diabetes: Consensus report and guidelines of the joint workshop on periodontal diseases and diabetes by the International Diabetes Federation and the European Federation of Periodontology. Diabetes Res Clin Pract. 2018;137:231–41.
22.
go back to reference Shimada Y, Komatsu Y, Ikezawa-Suzuki I, Tai H, Sugita N, Yoshie H. The Effect of Periodontal Treatment on Serum Leptin, Interleukin-6, and C-Reactive Protein. J Periodontol. 2010;81(8):1118–23. Shimada Y, Komatsu Y, Ikezawa-Suzuki I, Tai H, Sugita N, Yoshie H. The Effect of Periodontal Treatment on Serum Leptin, Interleukin-6, and C-Reactive Protein. J Periodontol. 2010;81(8):1118–23.
23.
go back to reference Kaczyński T, Wroński J, Głuszko P, Kryczka T, Miskiewicz A, Górski B, Radkowski M, Strzemecki D, Grieb P, Górska R. Salivary interleukin 6, interleukin 8, interleukin 17A, and tumour necrosis factor α levels in patients with periodontitis and rheumatoid arthritis. Cent Eur J Immunol. 2019;44(3):269.PubMedCentral Kaczyński T, Wroński J, Głuszko P, Kryczka T, Miskiewicz A, Górski B, Radkowski M, Strzemecki D, Grieb P, Górska R. Salivary interleukin 6, interleukin 8, interleukin 17A, and tumour necrosis factor α levels in patients with periodontitis and rheumatoid arthritis. Cent Eur J Immunol. 2019;44(3):269.PubMedCentral
24.
go back to reference Loos BG, Craandijk J, Hoek FJ, Dillen PMEW-v, Van Der Velden U. Elevation of systemic markers related to cardiovascular diseases in the peripheral blood of periodontitis patients. J Periodontol. 2000;71(10):1528–34. Loos BG, Craandijk J, Hoek FJ, Dillen PMEW-v, Van Der Velden U. Elevation of systemic markers related to cardiovascular diseases in the peripheral blood of periodontitis patients. J Periodontol. 2000;71(10):1528–34.
25.
go back to reference Han H, Ma Q, Li C, Liu R, Zhao L, Wang W, Zhang P, Liu X, Gao G, Liu F, et al. Profiling serum cytokines in COVID-19 patients reveals IL-6 and IL-10 are disease severity predictors. Emerg Microbes Infect. 2020;9(1):1123–30.PubMedCentral Han H, Ma Q, Li C, Liu R, Zhao L, Wang W, Zhang P, Liu X, Gao G, Liu F, et al. Profiling serum cytokines in COVID-19 patients reveals IL-6 and IL-10 are disease severity predictors. Emerg Microbes Infect. 2020;9(1):1123–30.PubMedCentral
26.
go back to reference Herold T, Jurinovic V, Arnreich C, Lipworth BJ, Hellmuth JC, von Bergwelt-Baildon M, Klein M, Weinberger T. Elevated levels of IL-6 and CRP predict the need for mechanical ventilation in COVID-19. J Allergy Clin Immunol. 2020;146(1):128-136.e124.PubMedCentral Herold T, Jurinovic V, Arnreich C, Lipworth BJ, Hellmuth JC, von Bergwelt-Baildon M, Klein M, Weinberger T. Elevated levels of IL-6 and CRP predict the need for mechanical ventilation in COVID-19. J Allergy Clin Immunol. 2020;146(1):128-136.e124.PubMedCentral
27.
go back to reference Chi Y, Ge Y, Wu B, Zhang W, Wu T, Wen T, Liu J, Guo X, Huang C, Jiao Y, et al. Serum Cytokine and Chemokine Profile in Relation to the Severity of Coronavirus Disease 2019 in China. J Infect Dis. 2020;222(5):746–54. Chi Y, Ge Y, Wu B, Zhang W, Wu T, Wen T, Liu J, Guo X, Huang C, Jiao Y, et al. Serum Cytokine and Chemokine Profile in Relation to the Severity of Coronavirus Disease 2019 in China. J Infect Dis. 2020;222(5):746–54.
28.
go back to reference Moradi Haghgoo J, Torkzaban P, Farhadian M, Rabienejad N, Moosavi Sedeh SA. Hematologic tests and their association with the severity of COVID-19 and periodontitis in hospitalized patients: a case–control study. BMC Oral Health. 2023;23(1):473.PubMedCentral Moradi Haghgoo J, Torkzaban P, Farhadian M, Rabienejad N, Moosavi Sedeh SA. Hematologic tests and their association with the severity of COVID-19 and periodontitis in hospitalized patients: a case–control study. BMC Oral Health. 2023;23(1):473.PubMedCentral
29.
go back to reference Löe H, Silness J. Periodontal Disease in Pregnancy I. Prevalence and Severity. Acta Odontologica Scandinavica. 1963;21(6):533–51. Löe H, Silness J. Periodontal Disease in Pregnancy I. Prevalence and Severity. Acta Odontologica Scandinavica. 1963;21(6):533–51.
30.
go back to reference Mombelli A, van Oosten MAC, Schürch E Jr, Lang NP. The microbiota associated with successful or failing osseointegrated titanium implants. Oral Microbiol Immunol. 1987;2(4):145–51. Mombelli A, van Oosten MAC, Schürch E Jr, Lang NP. The microbiota associated with successful or failing osseointegrated titanium implants. Oral Microbiol Immunol. 1987;2(4):145–51.
31.
go back to reference Papapanou PN, Sanz M, Buduneli N, Dietrich T, Feres M, Fine DH, Flemmig TF, Garcia R, Giannobile WV, Graziani F, et al. Periodontitis: Consensus report of workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Periodontol. 2018;89(S1):S173–82.PubMed Papapanou PN, Sanz M, Buduneli N, Dietrich T, Feres M, Fine DH, Flemmig TF, Garcia R, Giannobile WV, Graziani F, et al. Periodontitis: Consensus report of workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Periodontol. 2018;89(S1):S173–82.PubMed
32.
go back to reference Tonetti MS, Greenwell H, Kornman KS. Staging and grading of periodontitis: Framework and proposal of a new classification and case definition. J Periodontol. 2018;89(S1):S159–72.PubMed Tonetti MS, Greenwell H, Kornman KS. Staging and grading of periodontitis: Framework and proposal of a new classification and case definition. J Periodontol. 2018;89(S1):S159–72.PubMed
33.
go back to reference Li G, Yang Y, Gao D, Xu Y, Gu J, Liu P. Is liver involvement overestimated in COVID-19 patients? A meta-analysis. Int J Med Sci. 2021;18(5):1285–96.PubMedCentral Li G, Yang Y, Gao D, Xu Y, Gu J, Liu P. Is liver involvement overestimated in COVID-19 patients? A meta-analysis. Int J Med Sci. 2021;18(5):1285–96.PubMedCentral
34.
go back to reference Migliaccio MG, Di Mauro M, Ricciolino R, Spiniello G, Carfora V, Verde N, Mottola FF, Coppola N. Renal involvement in COVID-19: a review of the literature. Infect Drug Resist. 2021;14:895–903.PubMedPubMedCentral Migliaccio MG, Di Mauro M, Ricciolino R, Spiniello G, Carfora V, Verde N, Mottola FF, Coppola N. Renal involvement in COVID-19: a review of the literature. Infect Drug Resist. 2021;14:895–903.PubMedPubMedCentral
35.
go back to reference Siddiqi HK, Libby P, Ridker PM. COVID-19 - A vascular disease. Trends Cardiovasc Med. 2021;31(1):1–5.PubMed Siddiqi HK, Libby P, Ridker PM. COVID-19 - A vascular disease. Trends Cardiovasc Med. 2021;31(1):1–5.PubMed
36.
go back to reference Terpos E, Ntanasis-Stathopoulos I, Elalamy I, Kastritis E, Sergentanis TN, Politou M, Psaltopoulou T, Gerotziafas G, Dimopoulos MA. Hematological findings and complications of COVID-19. Am J Hematol. 2020;95(7):834–47.PubMedPubMedCentral Terpos E, Ntanasis-Stathopoulos I, Elalamy I, Kastritis E, Sergentanis TN, Politou M, Psaltopoulou T, Gerotziafas G, Dimopoulos MA. Hematological findings and complications of COVID-19. Am J Hematol. 2020;95(7):834–47.PubMedPubMedCentral
37.
go back to reference WHO: WHO severity definitions. Living guidance for clinical management of COVID-19: living guidance, 23 November 2021. Geneva: World Health Organization; 2021. p. 15. WHO: WHO severity definitions. Living guidance for clinical management of COVID-19: living guidance, 23 November 2021. Geneva: World Health Organization; 2021. p. 15.
38.
go back to reference Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z, Xiang J, Wang Y, Song B, Gu X. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet. 2020;395(10229):1054–62.PubMedPubMedCentral Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z, Xiang J, Wang Y, Song B, Gu X. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet. 2020;395(10229):1054–62.PubMedPubMedCentral
39.
go back to reference Guan WJ, Ni ZY, Hu Y, Liang WH, Ou CQ, He JX, Liu L, Shan H, Lei Cl, Hui DSC. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med 2020;382(18):1708-1720. Guan WJ, Ni ZY, Hu Y, Liang WH, Ou CQ, He JX, Liu L, Shan H, Lei Cl, Hui DSC. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med 2020;382(18):1708-1720.
40.
go back to reference Aiello A, Farzaneh F, Candore G, Caruso C, Davinelli S, Gambino CM, Ligotti ME, Zareian N, Accardi G. Immunosenescence and Its Hallmarks: How to Oppose Aging Strategically? A Review of Potential Options for Therapeutic Intervention. Front Immunol. 2019;10:2247.PubMedCentral Aiello A, Farzaneh F, Candore G, Caruso C, Davinelli S, Gambino CM, Ligotti ME, Zareian N, Accardi G. Immunosenescence and Its Hallmarks: How to Oppose Aging Strategically? A Review of Potential Options for Therapeutic Intervention. Front Immunol. 2019;10:2247.PubMedCentral
41.
go back to reference Noack B, Genco RJ, Trevisan M, Grossi S, Zambon JJ, De Nardin E. Periodontal Infections Contribute to Elevated Systemic C-Reactive Protein Level. J Periodontol. 2001;72(9):1221–7. Noack B, Genco RJ, Trevisan M, Grossi S, Zambon JJ, De Nardin E. Periodontal Infections Contribute to Elevated Systemic C-Reactive Protein Level. J Periodontol. 2001;72(9):1221–7.
42.
go back to reference Gümüş P, Nizam N, Lappin DF, Buduneli N. Saliva and Serum Levels of B-Cell Activating Factors and Tumor Necrosis Factor-α in Patients With Periodontitis. J Periodontol. 2014;85(2):270–80. Gümüş P, Nizam N, Lappin DF, Buduneli N. Saliva and Serum Levels of B-Cell Activating Factors and Tumor Necrosis Factor-α in Patients With Periodontitis. J Periodontol. 2014;85(2):270–80.
43.
go back to reference Prakasam S, Srinivasan M. Evaluation of salivary biomarker profiles following non-surgical management of chronic periodontitis. Oral Dis. 2014;20(2):171–7. Prakasam S, Srinivasan M. Evaluation of salivary biomarker profiles following non-surgical management of chronic periodontitis. Oral Dis. 2014;20(2):171–7.
44.
go back to reference Hajishengallis G. Aging and its impact on innate immunity and inflammation: Implications for periodontitis. J Oral Biosci. 2014;56(1):30–7.PubMedCentral Hajishengallis G. Aging and its impact on innate immunity and inflammation: Implications for periodontitis. J Oral Biosci. 2014;56(1):30–7.PubMedCentral
45.
go back to reference Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, Zhang L, Fan G, Xu J, Gu X, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395(10223):497–506.PubMedPubMedCentral Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y, Zhang L, Fan G, Xu J, Gu X, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395(10223):497–506.PubMedPubMedCentral
46.
go back to reference Karagiannidis C, Mostert C, Hentschker C, Voshaar T, Malzahn J, Schillinger G, Klauber J, Janssens U, Marx G, Weber-Carstens S, et al. Case characteristics, resource use, and outcomes of 10 021 patients with COVID-19 admitted to 920 German hospitals: an observational study. Lancet Respir Med. 2020;8(9):853–62.PubMedCentral Karagiannidis C, Mostert C, Hentschker C, Voshaar T, Malzahn J, Schillinger G, Klauber J, Janssens U, Marx G, Weber-Carstens S, et al. Case characteristics, resource use, and outcomes of 10 021 patients with COVID-19 admitted to 920 German hospitals: an observational study. Lancet Respir Med. 2020;8(9):853–62.PubMedCentral
47.
go back to reference da Silva JS, Gabriel-Costa D, Wang H, Ahmad S, Sun X, Varagic J, Sudo RT, Ferrario CM, Dell Italia LJ, Zapata-Sudo G. Blunting of cardioprotective actions of estrogen in female rodent heart linked to altered expression of cardiac tissue chymase and ACE2. J Renin Angiotensin Aldosterone Sys. 2017;18(3):1470320317722270. da Silva JS, Gabriel-Costa D, Wang H, Ahmad S, Sun X, Varagic J, Sudo RT, Ferrario CM, Dell Italia LJ, Zapata-Sudo G. Blunting of cardioprotective actions of estrogen in female rodent heart linked to altered expression of cardiac tissue chymase and ACE2. J Renin Angiotensin Aldosterone Sys. 2017;18(3):1470320317722270.
48.
go back to reference Ciaglia E, Vecchione C, Puca AA. COVID-19 infection and circulating ACE2 levels: protective role in women and children. Front Pediatr. 2020;8:206.PubMedCentral Ciaglia E, Vecchione C, Puca AA. COVID-19 infection and circulating ACE2 levels: protective role in women and children. Front Pediatr. 2020;8:206.PubMedCentral
49.
go back to reference Shiau HJ, Reynolds MA. Sex differences in destructive periodontal disease: a systematic review. J Periodontol. 2010;81(10):1379–89. Shiau HJ, Reynolds MA. Sex differences in destructive periodontal disease: a systematic review. J Periodontol. 2010;81(10):1379–89.
50.
go back to reference Ioannidou E. The Sex and Gender Intersection in Chronic Periodontitis. Front Public Health. 2017;5:189.PubMedCentral Ioannidou E. The Sex and Gender Intersection in Chronic Periodontitis. Front Public Health. 2017;5:189.PubMedCentral
51.
go back to reference Anand PS, Jadhav P, Kamath KP, Kumar SR, Vijayalaxmi S, Anil S. A case-control study on the association between periodontitis and coronavirus disease (COVID-19). J Periodontol. 2022;93(4):584–90. Anand PS, Jadhav P, Kamath KP, Kumar SR, Vijayalaxmi S, Anil S. A case-control study on the association between periodontitis and coronavirus disease (COVID-19). J Periodontol. 2022;93(4):584–90.
52.
go back to reference Marouf N, Cai W, Said KN, Daas H, Diab H, Chinta VR, Hssain AA, Nicolau B, Sanz M, Tamimi F. Association between periodontitis and severity of COVID-19 infection: a case–control study. J Clin Periodontol. 2021;48(4):483–91.PubMedCentral Marouf N, Cai W, Said KN, Daas H, Diab H, Chinta VR, Hssain AA, Nicolau B, Sanz M, Tamimi F. Association between periodontitis and severity of COVID-19 infection: a case–control study. J Clin Periodontol. 2021;48(4):483–91.PubMedCentral
53.
go back to reference Gupta S, Mohindra R, Singla M, Khera S, Sahni V, Kanta P, Soni RK, Kumar A, Gauba K, Goyal K, et al. The clinical association between Periodontitis and COVID-19. Clin Oral Invest. 2022;26(2):1361–74. Gupta S, Mohindra R, Singla M, Khera S, Sahni V, Kanta P, Soni RK, Kumar A, Gauba K, Goyal K, et al. The clinical association between Periodontitis and COVID-19. Clin Oral Invest. 2022;26(2):1361–74.
54.
go back to reference Fredriksson MI, Figueredo CMS, Gustafsson A, Bergström KG, Åsman BE. Effect of periodontitis and smoking on blood leukocytes and acute-phase proteins. J Periodontol. 1999;70(11):1355–60. Fredriksson MI, Figueredo CMS, Gustafsson A, Bergström KG, Åsman BE. Effect of periodontitis and smoking on blood leukocytes and acute-phase proteins. J Periodontol. 1999;70(11):1355–60.
55.
go back to reference Gong J, Dong H, Xia QS, Huang ZY, Wang DK, Zhao Y, Liu WH, Tu SH, Zhang MM, Wang Q. Correlation analysis between disease severity and inflammation-related parameters in patients with COVID-19: a retrospective study. BMC Infect Dis. 2020;20(1):1–7. Gong J, Dong H, Xia QS, Huang ZY, Wang DK, Zhao Y, Liu WH, Tu SH, Zhang MM, Wang Q. Correlation analysis between disease severity and inflammation-related parameters in patients with COVID-19: a retrospective study. BMC Infect Dis. 2020;20(1):1–7.
56.
go back to reference Kermali M, Khalsa RK, Pillai K, Ismail Z, Harky A. The role of biomarkers in diagnosis of COVID-19 – A systematic review. Life Sci. 2020;254:117788.PubMedCentral Kermali M, Khalsa RK, Pillai K, Ismail Z, Harky A. The role of biomarkers in diagnosis of COVID-19 – A systematic review. Life Sci. 2020;254:117788.PubMedCentral
57.
go back to reference Polepalle T, Moogala S, Boggarapu S, Pesala DS, Palagi FB. Acute phase proteins and their role in periodontitis: a review. J Clin Diagn Res. 2015;9(11):Ze01-05.PubMedCentral Polepalle T, Moogala S, Boggarapu S, Pesala DS, Palagi FB. Acute phase proteins and their role in periodontitis: a review. J Clin Diagn Res. 2015;9(11):Ze01-05.PubMedCentral
58.
go back to reference Bastug A, Bodur H, Erdogan S, Gokcinar D, Kazancioglu S, Kosovali BD, Ozbay BO, Gok G, Turan IO, Yilmaz G, et al. Clinical and laboratory features of COVID-19: predictors of severe prognosis. Int Immunopharmacol. 2020;88:106950.PubMedCentral Bastug A, Bodur H, Erdogan S, Gokcinar D, Kazancioglu S, Kosovali BD, Ozbay BO, Gok G, Turan IO, Yilmaz G, et al. Clinical and laboratory features of COVID-19: predictors of severe prognosis. Int Immunopharmacol. 2020;88:106950.PubMedCentral
59.
go back to reference Del Valle DM, Kim-Schulze S, Huang HH, Beckmann ND, Nirenberg S, Wang B, Lavin Y, Swartz TH, Madduri D, Stock A, et al. An inflammatory cytokine signature predicts COVID-19 severity and survival. Nat Med. 2020;26(10):1636–43.PubMedCentral Del Valle DM, Kim-Schulze S, Huang HH, Beckmann ND, Nirenberg S, Wang B, Lavin Y, Swartz TH, Madduri D, Stock A, et al. An inflammatory cytokine signature predicts COVID-19 severity and survival. Nat Med. 2020;26(10):1636–43.PubMedCentral
60.
go back to reference da Silva FRP, Pessoa LdS, Shin JI, Alves EHP, Koga RS, Smith CV, Vasconcelos DFP, Pereira ACTdC. Polymorphisms in the interleukin genes and chronic periodontitis: A field synopsis and revaluation by Bayesian approaches. Cytokine. 2021;138:155361. da Silva FRP, Pessoa LdS, Shin JI, Alves EHP, Koga RS, Smith CV, Vasconcelos DFP, Pereira ACTdC. Polymorphisms in the interleukin genes and chronic periodontitis: A field synopsis and revaluation by Bayesian approaches. Cytokine. 2021;138:155361.
61.
go back to reference Vakil MK, Mansoori Y, Al-Awsi GRL, Hosseinipour A, Ahsant S, Ahmadi S, Ekrahi M, Montaseri Z, Pezeshki B, Mohaghegh P, et al. Individual genetic variability mainly of Proinflammatory cytokines, cytokine receptors, and toll-like receptors dictates pathophysiology of COVID-19 disease. J Med Virol. 2022;94(9):4088–96.PubMedCentral Vakil MK, Mansoori Y, Al-Awsi GRL, Hosseinipour A, Ahsant S, Ahmadi S, Ekrahi M, Montaseri Z, Pezeshki B, Mohaghegh P, et al. Individual genetic variability mainly of Proinflammatory cytokines, cytokine receptors, and toll-like receptors dictates pathophysiology of COVID-19 disease. J Med Virol. 2022;94(9):4088–96.PubMedCentral
62.
go back to reference Wang Z, Li Y, Zhou Y, Qiao Y. Association between the IL-10 rs1800872 polymorphisms and periodontitis susceptibility: a meta-analysis. Medicine (Baltimore). 2019;98(40):e17113. Wang Z, Li Y, Zhou Y, Qiao Y. Association between the IL-10 rs1800872 polymorphisms and periodontitis susceptibility: a meta-analysis. Medicine (Baltimore). 2019;98(40):e17113.
63.
go back to reference Rizvi S, Rizvi SMS, Raza ST, Abbas M, Fatima K, Zaidi ZH, Mahdi F. Implication of single nucleotide polymorphisms in Interleukin-10 gene (rs1800896 and rs1800872) with severity of COVID-19. Egypt J Med Hum Genet. 2022;23(1):145.PubMedCentral Rizvi S, Rizvi SMS, Raza ST, Abbas M, Fatima K, Zaidi ZH, Mahdi F. Implication of single nucleotide polymorphisms in Interleukin-10 gene (rs1800896 and rs1800872) with severity of COVID-19. Egypt J Med Hum Genet. 2022;23(1):145.PubMedCentral
64.
go back to reference Wang Z, Ji JS, Liu Y, Liu R, Zha Y, Chang X, Zhang L, Liu Q, Zhang Y, Zeng J, et al. Survival analysis of hospital length of stay of novel coronavirus (COVID-19) pneumonia patients in Sichuan, China. PLoS One. 2020;17(1):e0261216. Wang Z, Ji JS, Liu Y, Liu R, Zha Y, Chang X, Zhang L, Liu Q, Zhang Y, Zeng J, et al. Survival analysis of hospital length of stay of novel coronavirus (COVID-19) pneumonia patients in Sichuan, China. PLoS One. 2020;17(1):e0261216.
65.
go back to reference Xu H, Zhong L, Deng J, Peng J, Dan H, Zeng X, Li T, Chen Q. High expression of ACE2 receptor of 2019-nCoV on the epithelial cells of oral mucosa. Int J Oral Sci. 2020;12(1):8.PubMedPubMedCentral Xu H, Zhong L, Deng J, Peng J, Dan H, Zeng X, Li T, Chen Q. High expression of ACE2 receptor of 2019-nCoV on the epithelial cells of oral mucosa. Int J Oral Sci. 2020;12(1):8.PubMedPubMedCentral
66.
go back to reference Gao Y, Kok WL, Sharma V, Illsley CS, Hanks S, Tredwin C, Hu B. SARS-CoV-2 infection causes periodontal fibrotic pathogenesis through deregulating mitochondrial beta-oxidation. Cell Death Discov. 2023;9(1):175.PubMedCentral Gao Y, Kok WL, Sharma V, Illsley CS, Hanks S, Tredwin C, Hu B. SARS-CoV-2 infection causes periodontal fibrotic pathogenesis through deregulating mitochondrial beta-oxidation. Cell Death Discov. 2023;9(1):175.PubMedCentral
67.
go back to reference Duarte PM, da Rocha M, Sampaio E, Mestnik MJ, Feres M, Figueiredo LC, Bastos MF, Faveri M. Serum levels of cytokines in subjects with generalized chronic and aggressive periodontitis before and after non-surgical periodontal therapy: a pilot study. J Periodontol. 2010;81(7):1056–63. Duarte PM, da Rocha M, Sampaio E, Mestnik MJ, Feres M, Figueiredo LC, Bastos MF, Faveri M. Serum levels of cytokines in subjects with generalized chronic and aggressive periodontitis before and after non-surgical periodontal therapy: a pilot study. J Periodontol. 2010;81(7):1056–63.
68.
go back to reference Akbari H, Tabrizi R, Lankarani KB, Aria H, Vakili S, Asadian F, Noroozi S, Keshavarz P, Faramarz S. The role of cytokine profile and lymphocyte subsets in the severity of coronavirus disease 2019 (COVID-19): a systematic review and meta-analysis. Life Sci. 2020;258:118167.PubMedCentral Akbari H, Tabrizi R, Lankarani KB, Aria H, Vakili S, Asadian F, Noroozi S, Keshavarz P, Faramarz S. The role of cytokine profile and lymphocyte subsets in the severity of coronavirus disease 2019 (COVID-19): a systematic review and meta-analysis. Life Sci. 2020;258:118167.PubMedCentral
69.
go back to reference Mulchandani R, Lyngdoh T, Kakkar AK. Deciphering the COVID-19 cytokine storm: Systematic review and meta-analysis. Eur J Clin Invest. 2021;51(1):e13429. Mulchandani R, Lyngdoh T, Kakkar AK. Deciphering the COVID-19 cytokine storm: Systematic review and meta-analysis. Eur J Clin Invest. 2021;51(1):e13429.
70.
go back to reference Hajishengallis G. Interconnection of periodontal disease and comorbidities: Evidence, mechanisms, and implications. Periodontology 2000. 2022;89(1):9–18.PubMedCentral Hajishengallis G. Interconnection of periodontal disease and comorbidities: Evidence, mechanisms, and implications. Periodontology 2000. 2022;89(1):9–18.PubMedCentral
71.
go back to reference Brock M, Bahammam S, Sima C. The relationships among periodontitis, pneumonia and COVID-19. Front Oral Health. 2022;2:801815.PubMedCentral Brock M, Bahammam S, Sima C. The relationships among periodontitis, pneumonia and COVID-19. Front Oral Health. 2022;2:801815.PubMedCentral
Metadata
Title
Association between the severity of periodontitis, COVID-19, C-reactive protein and interleukin-6 levels in hospitalized patients: a case‒control study
Authors
Janet Moradi Haghgoo
Parviz Torkzaban
Maryam Farhadian
Sayed Ali Moosavi Sedeh
Publication date
01-12-2023
Publisher
BioMed Central
Keyword
COVID-19
Published in
BMC Oral Health / Issue 1/2023
Electronic ISSN: 1472-6831
DOI
https://doi.org/10.1186/s12903-023-03270-x

Other articles of this Issue 1/2023

BMC Oral Health 1/2023 Go to the issue