ARDS severity in COVID-19: a case–control study of laboratory biomarkers and IL-10 SNP analysis
Keywords:
Acute respiratory distress syndrome, COVID-19, cytokines, hematological parameters, polymorphism
Abstract
Background: Acute respiratory distress syndrome (ARDS), which is often observed in severe cases of coronavirus disease 2019 (COVID-19), is known to be a major contributor to higher mortality rates. This study assesses how hematological parameters, inflammatory biomarkers, cytokines, and the –1,082 A/G polymorphism are associated with ARDS severity in COVID-19 patients.
Methods: Following exclusions, a 6-month prospective case–control study included 82 healthy controls (HCs) and 158 COVID-19 patients with varying severities of ARDS (mild: 73, moderate: 53, and severe: 32). Blood samples were collected at admission, and laboratory biomarkers were assessed using various methods. Statistical analyses included one-way analysis of variance with Tukey’s test for group comparisons, Pearson correlation, and receiver operating characteristic curve for analyzing independent associations with COVID-19 severity. Multiple linear regression and chi-square tests were used to evaluate quantitative outcomes and categorical associations, respectively.
Results: Severe ARDS patients exhibited higher C-reactive protein (CRP) levels compared to HCs. Compared to HCs, patients with moderate and severe ARDS had higher neutrophil to lymphocyte ratio (NLR), neutrophil counts, tumor necrosis factor-alpha, and interleukin-10 (IL-10), as well as lower lymphocyte counts and reduced partial pressure of oxygen/fraction of inspired oxygen (PaO2/FiO2) ratio. IL-10, body mass index, CRP, and NLR were associated with reduced PaO2/FiO2 ratio. IL-10 and CRP had the highest area under curve values toward ARDS severity. COVID-19 patients possessing the –1,082 A/G single nucleotide IL-10 GG and GA genotypes and the G allele presented with less severe ARDS.
Conclusion: Hematological indices (neutrophil count and NLR), CRP, and serum IL-10 hold promise in monitoring ARDS severity in COVID-19 patients. In addition, COVID-19 patients with GG and AG genotypes and the G allele of the IL-10 gene’s–1,082 A/G polymorphism experience less severe ARDS. This highlights the potential protective role of IL-10 genetic variation in modulating the severity of inflammatory responses during severe acute respiratory syndrome-coronavirus-2 infection and may serve as a useful genetic marker for risk stratification in clinical settings.
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References
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28. Field AP. Discovering statistics using IBM SPSS statistics. 4th ed. Thousand Oaks, CA: SAGE Publications; 2013.
29. Cohen J, Cohen P, West SG, Aiken LS. Applied multiple regression/correlation analysis for the behavioral sciences. New York, NY: Routledge; 2015.
30. Hosmer DW Jr, Lemeshow S, Sturdivant RX. Applied Logistic Regression. Hoboken, NJ: John Wiley & Sons; 2013.
31. Batah SS, Fabro AT. Pulmonary pathology of ARDS in COVID-19: a pathological review for clinicians. Respir Med. 2021;176:106239. doi: 10.1016/j.rmed.2020.106239
32. Bellani G, Laffey JG, Pham T, Fan E, Brochard L, Esteban A, et al. Epidemiology, patterns of care, and mortality for patients with acute respiratory distress syndrome in intensive care units in 50 countries. JAMA. 2016;315(8):788–800. doi: 10.1001/jama.2016.0291
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40. Kong M, Zhang H, Cao X, Mao X, Lu Z. Higher level of neutrophil-to-lymphocyte is associated with severe COVID-19. Epidemiol Infect. 2020;148:e139. doi: 10.1017/S0950268820001557
41. Smail SW, Babaei E, Amin K, Abdulahad WH. Serum IL-23, IL-10, and TNF-α predict in-hospital mortality in COVID-19 patients. Front Immunol. 2022;14:1145840. doi: 10.3389/fimmu.2023.1145840
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43. Herfarth H, Schölmerich J. IL-10 therapy in Crohn’s disease: at the crossroads. Treatment of Crohn’s disease with the anti-inflammatory cytokine interleukin 10. Gut. 2002;50(2):146–7. doi: 10.1136/gut.50.2.146
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45. Shahbazi M, Abadi JSA, Roshandel D, Koochaki M, Amiri H, Kohansal R, et al. Combination of interleukin-10 gene promoter polymorphisms with HLA-DRB1* 15 allele is associated with multiple sclerosis. Indian J Med Res. 2017;145(6):746–52. doi: 10.4103/ijmr.IJMR_1225_15
46. Abbood SJA, Anvari E, Fateh A. Association between interleukin-10 gene polymorphisms (rs1800871, rs1800872, and rs1800896) and severity of infection in different SARS-CoV-2 variants. Hum Genomics. 2023;17(1):19. doi: 10.1186/s40246-023-00468-6
47. Rizvi S, Rizvi SMS, Raza ST, Abbas M, Fatima K, Zaidi ZH, et al. 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. doi: 10.1186/s43042-022-00344-3
48. Gong MN, Taylor B, Williams PL, Zhou W, Wang MZ, Pothier L, et al. Interleukin-10 polymorphism in position -1082 and acute respiratory distress syndrome. Eur Respir J. 2006;27:674–81. doi: 10.1183/09031936.06.00046405
2. Worldometer. Coronavirus death toll 2024 [updated 13 April 2024]. Available from: https://www.worldometers.info/coronavirus/coronavirus-death-toll/ [cited 13 April 2024].
3. Shih L-J, Yang C-C, Liao M-T, Lu K-C, Hu W-C, Lin C-P. An important call: suggestion of using IL-10 as therapeutic agent for COVID-19 with ARDS and other complications. Virulence. 2023;14(1):2190650. doi: 10.1080/21505594.2023.2190650
4. Huang SR, Ma AY, Liu Y, Qu Y. Effects of inflammatory factors including plasma tumor necrosis factor-α in the clinical treatment of acute respiratory distress syndrome. Oncol Lett. 2017;13(6):5016–20. doi: 10.3892/ol.2017.6090
5. Chen Z, Hu Y, Xiong T, Chen C, Su XX, Huang Y, et al. IL-10 promotes development of acute respiratory distress syndrome via inhibiting differentiation of bone marrow stem cells to alveolar type 2 epithelial cells. Eur Rev Med Pharmacol Sci. 2018;22(18):6085–92.
6. Bano Mehdi K, Jehan S, Akhter M, Angez M, Nasir N. Utility of neutrophil to lymphocyte ratio to predict acute respiratory distress syndrome in COVID-19: short communication. Ann Med Surg (Lond). 2023;85(6):3232–6. doi: 10.1097/MS9.0000000000000758
7. Song M, Liu Y, Lu Z, Luo H, Peng H, Chen P. Prognostic factors for ARDS: clinical, physiological and atypical immunodeficiency. BMC Pulm Med. 2020;20(1):102. doi: 10.1186/s12890-020-1131-0
8. Meyer NJ, Calfee CS. Novel translational approaches to the search for precision therapies for acute respiratory distress syndrome. Lancet Respir Med. 2017;5(6):512–23. doi: 10.1016/S2213-2600(17)30187-X
9. Liu H, Zhang H, Wan G, Sang Y, Chang Y, Wang X, et al. Neutrophil-lymphocyte ratio: a novel predictor for short-term prognosis in acute-on-chronic hepatitis B liver failure. J Viral Hepat. 2014;21(7):499–507. doi: 10.1111/jvh.12160
10. Smilowitz NR, Kunichoff D, Garshick M, Shah B, Pillinger M, Hochman JS, et al. C-reactive protein and clinical outcomes in patients with COVID-19. Eur Heart J. 2021;42(23):2270–9. doi: 10.1093/eurheartj/ehaa1103
11. Mohd Zawawi Z, Kalyanasundram J, Mohd Zain R, Thayan R, Basri DF, Yap WB. Prospective roles of tumor necrosis factor-alpha (TNF-α) in COVID-19: prognosis, therapeutic and management. Int J Mol Sci. 2023;24(7):6142. doi: 10.3390/ijms24076142
12. Yang G, Hamacher J, Gorshkov B, White R, Sridhar S, Verin A, et al. The dual role of TNF in pulmonary edema. J Cardiovasc Dis Res. 2010;1(1):29–36. doi: 10.4103/0975-3583.59983
13. Lucas R, Hadizamani Y, Enkhbaatar P, Csanyi G, Caldwell RW, Hundsberger H, et al. Dichotomous role of tumor necrosis factor in pulmonary barrier function and alveolar fluid clearance. Front Physiol. 2021;12:793251. doi: 10.3389/fphys.2021.793251
14. Aisiku IP, Yamal JM, Doshi P, Benoit JS, Gopinath S, Goodman JC, et al. Plasma cytokines IL-6, IL-8, and IL-10 are associated with the development of acute respiratory distress syndrome in patients with severe traumatic brain injury. Crit Care. 2016;20:288. doi: 10.1186/s13054-016-1470-7
15. Liu CH, Kuo SW, Ko WJ, Tsai PR, Wu SW, Lai CH, et al. Early measurement of IL-10 predicts the outcomes of patients with acute respiratory distress syndrome receiving extracorporeal membrane oxygenation. Sci Rep. 2017;7(1):1021. doi: 10.1038/s41598-017-01225-1
16. Suárez A, Castro P, Alonso R, Mozo L, Gutiérrez C. Interindividual variations in constitutive interleukin-10 messenger RNA and protein levels and their association with genetic polymorphisms. Transplantation. 2003;75(5):711–17. doi: 10.1097/01.TP.0000055216.19866.9A
17. Galley HF, Lowe PR, Carmichael RL, Webster NR. Genotype and interleukin-10 responses after cardiopulmonary bypass. Br J Anaesth. 2003;91(3):424–6. doi: 10.1093/bja/aeg174
18. Gong MN, Thompson BT, Williams PL, Zhou W, Wang MZ, Pothier L, et al. Interleukin-10 polymorphism in position -1082 and acute respiratory distress syndrome. Eur Respir J. 2006;27(4):674–81. doi: 10.1183/09031936.06.00046405
19. Mohamedsalih P, Salih K, Kareem B, Sabir D. Tracking SARS-CoV-2 variants in Kurdistan Region of Iraq. ZANCO J Pure Appl Sci. 2023;35:128–36. doi: 10.21271/ZJPAS.35.5.12
20. WHO. Clinical management of severe acute respiratory infection when Middle East respiratory syndrome coronavirus (MERS-CoV) infection is suspected: interim guidance. Geneva: World Health Organization; 2019.
21. Ranieri VM, Rubenfeld GD, Thompson BT, Ferguson ND, Caldwell E, Fan E, et al. Acute respiratory distress syndrome: the Berlin definition. JAMA. 2012;307(23):2526–33. doi: 10.1001/jama.2012.5669
22. Matthay MA, Arabi Y, Arroliga AC, Bernard G, Bersten AD, Brochard LJ, et al. A new global definition of acute respiratory distress syndrome. Am J Respir Crit Care Med. 2024;209(1):37–47. doi: 10.1164/rccm.202303-0558WS
23. Murad K, Goff DC, Jr., Morgan TM, Burke GL, Bartz TM, Kizer JR, et al. Burden of comorbidities and functional and cognitive impairments in elderly patients at the initial diagnosis of heart failure and their impact on total mortality: the cardiovascular health study. JACC Heart Fail. 2015;3(7):542–50. doi: 10.1016/j.jchf.2015.03.004
24. Borque L, Bellod L, Rus A, Seco ML, Galisteo-Gonzalez F. Development and validation of an automated and ultrasensitive immunoturbidimetric assay for C-reactive protein. Clin Chem. 2000;46(11):1839–42. doi: 10.1093/clinchem/46.11.1839
25. Aboab J, Louis B, Jonson B, Brochard L. Relation between PaO2/FIO2 ratio and FIO2: a mathematical description. In: Pinsky MR, Brochard L, Hedenstierna G, Antonelli M, eds. Applied physiology in intensive care medicine 1: physiological notes – technical notes – seminal studies in intensive care. BerlIn: Springer Berlin Heidelberg; 2012, pp. 63–6.
26. Perrey C, Turner SJ, Pravica V, Howell WM, Hutchinson IV. ARMS-PCR methodologies to determine IL-10, TNF-α, TNF-β and TGF-β1 gene polymorphisms. Transpl Immunol. 1999;7(2):127–8. doi: 10.1016/S0966-3274(99)80030-6
27. Qadir FA, Pirdawid AO, Aali MH, Smail SW, Khudhur ZO, Shareef AA, et al. Association study of interleukin 10 gene polymorphisms in Iraqi patients with multiple sclerosis. Gene Rep. 2020;21:100948. doi: 10.1016/j.genrep.2020.100948
28. Field AP. Discovering statistics using IBM SPSS statistics. 4th ed. Thousand Oaks, CA: SAGE Publications; 2013.
29. Cohen J, Cohen P, West SG, Aiken LS. Applied multiple regression/correlation analysis for the behavioral sciences. New York, NY: Routledge; 2015.
30. Hosmer DW Jr, Lemeshow S, Sturdivant RX. Applied Logistic Regression. Hoboken, NJ: John Wiley & Sons; 2013.
31. Batah SS, Fabro AT. Pulmonary pathology of ARDS in COVID-19: a pathological review for clinicians. Respir Med. 2021;176:106239. doi: 10.1016/j.rmed.2020.106239
32. Bellani G, Laffey JG, Pham T, Fan E, Brochard L, Esteban A, et al. Epidemiology, patterns of care, and mortality for patients with acute respiratory distress syndrome in intensive care units in 50 countries. JAMA. 2016;315(8):788–800. doi: 10.1001/jama.2016.0291
33. Thapa K, Verma N, Singh TG, Kaur Grewal A, Kanojia N, Rani L. COVID-19-associated acute respiratory distress syndrome (CARDS): mechanistic insights on therapeutic intervention and emerging trends. Int Immunopharmacol. 2021;101(Pt A):108328. doi: 10.1016/j.intimp.2021.108328
34. Diamond M, Peniston HL, Sanghavi DK, Mahapatra S. Acute respiratory distress syndrome. StatPearls. Treasure Island, FL: StatPearls Publishing LLC; 2024.
35. Ding L, Chen Y, Su N, Xu X, Yin J, Qiu J, et al. Comparison of acute respiratory distress syndrome in patients with COVID-19 and influenza A (H7N9) virus infection. Int J Infect Dis. 2022;122:593–8. doi: 10.1016/j.ijid.2022.06.053
36. Perschinka F, Mayerhöfer T, Lehner GF, Hasslacher J, Klein SJ, Joannidis M. Immunologic response in bacterial sepsis is different from that in COVID-19 sepsis. Infection. 2022;50(4):1035–7. doi: 10.1007/s15010-022-01803-0
37. Batra R, Whalen W, Alvarez-Mulett S, Gomez-Escobar LG, Hoffman KL, Simmons W, et al. Multi-omic comparative analysis of COVID-19 and bacterial sepsis-induced ARDS. PLOS Pathog. 2022;18(9):e1010819. doi: 10.1371/journal.ppat.1010819
38. Yu J, Wang Y, Lin S, Jiang L, Sang L, Zheng X, et al. Severe COVID-19 has a distinct phenotype from bacterial sepsis: a retrospective cohort study in deceased patients. Ann Transl Med. 2021;9(13):1054. doi: 10.21037/atm-21-1291
39. Wong JJM, Leong JY, Lee JH, Albani S, Yeo JG. Insights into the immuno-pathogenesis of acute respiratory distress syndrome. Ann Transl Med. 2019;7(19):504. doi: 10.21037/atm.2019.09.28
40. Kong M, Zhang H, Cao X, Mao X, Lu Z. Higher level of neutrophil-to-lymphocyte is associated with severe COVID-19. Epidemiol Infect. 2020;148:e139. doi: 10.1017/S0950268820001557
41. Smail SW, Babaei E, Amin K, Abdulahad WH. Serum IL-23, IL-10, and TNF-α predict in-hospital mortality in COVID-19 patients. Front Immunol. 2022;14:1145840. doi: 10.3389/fimmu.2023.1145840
42. Tilg H, van Montfrans C, van den Ende A, Kaser A, van Deventer SJ, Schreiber S, et al. Treatment of Crohn’s disease with recombinant human interleukin 10 induces the proinflammatory cytokine interferon gamma. Gut. 2002;50(2):191–5. doi: 10.1136/gut.50.2.191
43. Herfarth H, Schölmerich J. IL-10 therapy in Crohn’s disease: at the crossroads. Treatment of Crohn’s disease with the anti-inflammatory cytokine interleukin 10. Gut. 2002;50(2):146–7. doi: 10.1136/gut.50.2.146
44. Teixeira PC, Dorneles GP, Santana Filho PC, da Silva IM, Schipper LL, Postiga IAL, et al. Increased LPS levels coexist with systemic inflammation and result in monocyte activation in severe COVID-19 patients. Int Immunopharmacol. 2021;100:108125. doi: 10.1016/j.intimp.2021.108125
45. Shahbazi M, Abadi JSA, Roshandel D, Koochaki M, Amiri H, Kohansal R, et al. Combination of interleukin-10 gene promoter polymorphisms with HLA-DRB1* 15 allele is associated with multiple sclerosis. Indian J Med Res. 2017;145(6):746–52. doi: 10.4103/ijmr.IJMR_1225_15
46. Abbood SJA, Anvari E, Fateh A. Association between interleukin-10 gene polymorphisms (rs1800871, rs1800872, and rs1800896) and severity of infection in different SARS-CoV-2 variants. Hum Genomics. 2023;17(1):19. doi: 10.1186/s40246-023-00468-6
47. Rizvi S, Rizvi SMS, Raza ST, Abbas M, Fatima K, Zaidi ZH, et al. 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. doi: 10.1186/s43042-022-00344-3
48. Gong MN, Taylor B, Williams PL, Zhou W, Wang MZ, Pothier L, et al. Interleukin-10 polymorphism in position -1082 and acute respiratory distress syndrome. Eur Respir J. 2006;27:674–81. doi: 10.1183/09031936.06.00046405
Published
2025-07-07
How to Cite
Smail , S. W., Albarzinji , N., Karim , K. J., Salih , R. H., & Janson , C. (2025). ARDS severity in COVID-19: a case–control study of laboratory biomarkers and IL-10 SNP analysis. Upsala Journal of Medical Sciences, 130, e11515. https://doi.org/10.48101/ujms.v130.11515
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