metricas
covid
Buscar en
Clinics
Toda la web
Inicio Clinics Time-to-event assessment for the discovery of the proper prognostic value of cli...
Journal Information
Vol. 77.
(January - December 2022)
Share
Share
Download PDF
More article options
Vol. 77.
(January - December 2022)
Comments
Full text access
Time-to-event assessment for the discovery of the proper prognostic value of clinical biomarkers optimized for COVID-19
Visits
1093
José Raniery Ferreira Junior
Hospital das Clínicas HCFMUSP, Faculdade de Medicina, Universidade de São Paulo, São Paulo, SP, Brazil
This item has received
Article information
Full Text
Bibliography
Download PDF
Statistics
Figures (1)
Tables (1)
Table 1. Discovered biomarkers according to the patient age and hospitalization time.
Full Text

In the early days of the pandemic, clinical COVID-19 biomarkers were investigated to predict mortality.1 Yan et al., for instance, proposed a straightforward decision tree with three variables: Lactic Dehydrogenase (LDH), high-sensitivity C-Reactive Protein (hs-CRP), and lymphocyte percentage. They claimed to obtain more than 90% accuracy on a test set. Although it is an interesting approach, Yan et al. considered the problem a classification task (dead vs. alive), which may not be the proper way to deal with continuous time-to-event data.2–4 Moreover, machine-learning-based assessment is pruned to over-optimistic results using small sampling for training. In addition, it has been shown that their model has limited performance on external datasets.5–7 These two limitations are possibly due to data overfitting.

Therefore, the authors performed time-to-event analyses using the original dataset to find a proper predictive potential for the investigated biomarkers. The authors’ evaluation aimed to optimize the clinical variables previously modeled and discover other biomarkers with prognostic value. By opposing the original strategy, the authors also focused on identifying biomarkers for different sub-populations, according to patient aging and hospitalization time.

Original data is publicly available.1 The dataset comprised demographics data of age (varying 18–95, averaging 58.8 ± 16.5 years old) and sex (224 men, 151 women), along with the results of 74 blood tests in different hospitalization times. The variables obtained for each patient is listed as follows: 2019-ncov nucleic acid detection, activation of partial thromboplastin time, albumin, alkaline phosphatase, amino-terminal brain natriuretic peptide precursor, antithrombin, aspartate aminotransferase, basophil count, basophil percentage, calcium, corrected calcium, creatinine, d-d dimer, direct bilirubin, egfr, eosinophil count, eosinophils percentage, esr, ferritin, fibrin degradation products, fibrinogen, globulin, glucose, glutamic-pyruvic transaminase, hbsag, hco3-, hcv antibody quantification, hematocrit, hemoglobin, hiv antibody quantification, hypersensitive cardiac troponini, hypersensitive c-reactive protein, indirect bilirubin, interleukin 10, interleukin 1β, interleukin 2 receptor, interleukin 6, interleukin 8, international standard ratio, lactate dehydrogenase, lymphocyte count, lymphocyte percentage, mean corpuscular hemoglobin, mean corpuscular hemoglobin concentration, mean corpuscular volume, mean platelet volume, monocytes count, monocytes percentage, neutrophils count, neutrophils percentage, ph value, platelet count, platelet large cell ratio, plt distribution width, procalcitonin, prothrombin activity, prothrombin time, quantification of treponema pallidum antibodies, rbc distribution width sd, red blood cell count, red blood cell distribution width, serum chloride, serum potassium, serum sodium, thrombin time, thrombocytocrit, total bilirubin, total cholesterol, total protein, tumor necrosis factorα, urea, uric acid, white blood cell count, and γ-glutamyl transpeptidase.

The authors split the dataset into discovery and validation subsets to perform a robust assessment and validate the results. The thresholds identified in the discovery set were then applied in the validation set to confirm further performance. Patient risk groups were stratified according to the variables’ median.3,4 The log-rank test assessed the difference between Kaplan-Meier curves and Cox proportional hazards regression models. R v4.1.0 packages of survival v3.2.3 and survminer v0.4.7 performed statistical analyses, with p < 0.05 considered significant.

As expected, the older the patient is, the worst is the prognosis;8,9 the threshold of 62 years obtained significant difference on survival curves (Fig. 1a). The overall assessment disregarding patient age and hospitalization timing found predictive value in 53 variables, including LDH and hs-CRP (Fig. 1b–c). Moreover, other biomarkers yielded relevant information on COVID-19 prognostication (Table 1). For instance, high-risk groups stratified by fibrin degradation products presented a 97% likelihood of death and a Hazard Ratio (HR) of 4.26 (95% Confidence Interval [95% CI]: 1.88–9.64); and elevated Interleukin-6 (IL-6) associated with 65% likelihood of death and HR of 18.20 (95% CI: 2.42-136.54).

Fig. 1.

Kaplan-Meier curves of the clinical biomarkers of (a) age, (b) Lactic Dehydrogenase (LDH), (c) high-sensitivity C-Reactive Protein (hs-CRP), (d) LDH combined with hs-CRP.

(0.13MB).
Table 1.

Discovered biomarkers according to the patient age and hospitalization time.

      High-risk groupLow-risk group 
  Relevant biomarkers  Threshold discovered  Proportion of deaths  Mean survival days  Proportion of deaths  Mean survival days  Log-rank p-value 
Demographics: 1 significant variableAge  62  0.824  7.9  0.146  11.2  < 0.001 
Sex  Male / Female  0.542  9.5  0.296  10.1  0.120 
Overall (disregarding patient age and hospitalization timing): 53 significant variablesLactate dehydrogenase  334  0.835  10.1  0.041  12.8  < 0.001 
Hypersensitive c-reactive protein  47.2  0.785  9.6  0.089  13.1  < 0.001 
Lymphocyte (%)  11.6  0.793  10.8  0.134  13.2  < 0.001 
Fibrin degradation products  16.9  0.974  10.4  0.226  10.8  < 0.001 
Interleukin-6  18.3  0.655  10.7  0.045  12.8  < 0.001 
Hypersensitive cardiac troponinI  22.8  0.902  6.8  0.273  12.3  < 0.001 
First sample after admission (disregarding patient age): 40 significant variablesLactate dehydrogenase  328  0.732  8.8  0.094  11.2  < 0.001 
Hypersensitive c-reactive protein  51.9  0.732  8.6  0.065  11.6  < 0.001 
Lymphocyte (%)  14.9  0.700  8.8  0.125  11.3  < 0.001 
Fibrin degradation products  4.9  0.875  9.0  0.095  9.6  <0.001 
Interleukin-6  19.53  0.667  10.2  0.071  12.0  < 0.01 
Procalcitonin  0.09  0.853  8.2  0.071  13.6  < 0.001 
Last sample before discharge or death (disregarding patient age): 46 significant variablesLactate dehydrogenase  261  0.733  8.6  0.000  11.8  < 0.001 
Hypersensitive c-reactive protein  23.9  0.780  8.0  0.000  12.4  < 0.001 
Lymphocyte (%)  14.35  0.806  8.3  0.083  11.5  < 0.001 
Fibrin degradation products  5.9  0.952  8.7  0.125  9.7  < 0.001 
Procalcitonin  0.09  0.882  8.0  0.036  13.8  < 0.001 
HCO3-  24.1  0.638  7.6  0.115  13.9  < 0.001 
Patients with age <62 years (disregarding hospitalization timing): 31 significant variablesLactate dehydrogenase  232.5  0.360  14.1  0.000  18.3  < 0.001 
Hypersensitive c-reactive protein  11.6  0.417  14.1  0.000  18.6  < 0.001 
Lymphocyte (%)  22.15  0.362  15.6  0.089  16.0  < 0.01 
Fibrin degradation products  0.769  9.1  0.000  14.4  < 0.001 
International standard ratio  1.05  0.531  11.4  0.000  18.0  < 0.001 
Calcium  2.15  0.463  14.8  0.042  16.2  < 0.001 
Patients with age ≥62 years (disregarding hospitalization timing): 29 significant variablesLactate dehydrogenase  470  0.986  11.6  0.603  16.4  < 0.001 
Hypersensitive c-reactive protein  88.3  0.922  12.4  0.596  16.2  < 0.001 
Lymphocyte (%)  5.3  0.967  13.3  0.627  14.2  < 0.01 
Hypersensitive cardiac troponin I  51.4  1.000  11.9  0.800  14.2  < 0.01 
Monocytes (%)  4.1  0.986  13.5  0.552  14.1  < 0.001 
Alkaline phosphatase  77  0.952  11.1  0.687  16.2  < 0.001 

Furthermore, LDH and hs-CRP combined presented complementary predictive potential in multivariate assessment (Fig. 1d). With both biomarkers’ values elevated, patients showed a likelihood of death of 87%, the mean survival time of 9.5 days, and HRs of 8.19 (95% CI: 2.27–29.52) and 3.90 (95% CI: 1.41–10.72). Conversely, when either LDH or hs-CRP yielded low value, potentially indicating lower risk, the age determined the worse prognosis in the multivariate signature (p<0.001), resulting in a likelihood of death of 72% and HR of 7.01 (95% CI: 3.10–15.84) for the elderly patients.

Results confirmed poor short-term prognosis to abnormal levels of some indicators, such as LDH,1,9-11 CRP,1,8-11 lymphocytes,1,8-10 IL-6,12 and procalcitonin.11 These findings could provide insights into COVID-19 research, such as key levels of fibrin degradation products, which are directly associated with the Dimerized plasmin fragment D and could indicate active coagulation and thrombosis.9-11

Yan et al. had already mentioned that lymphocytes might serve as a potential therapeutic target.1 Still, the authors highlight the role of IL-6, a cytokine that induces inflammatory response and has prognostic value. Although IL-6 blockade is not the standard strategy for COVID-19 treatment, interleukin-6 remains the best available biomarker for severity assessment and still holds great potential for targeted therapy.12

In this work, the authors have identified relevant biomarkers that are fully available in medical practice and be a mainstay for the clinical evaluation of COVID-19. These biomarkers correlated with short-term outcomes and could support the management of the disease with early interventions, ultimately leading to better endpoints such as decreased deterioration and mortality. Future works include a prospective evaluation to increase robustness and the assessment across different geographic populations, as each region has its genomic specificity.

References
[1]
L Yan, HT Zhang, J Goncalves, Y Xiao, M Wang, Y Guo, et al.
An interpretable mortality prediction model for COVID-19 patients.
Nat Mach Intell, 2 (2020), pp. 283-288
[2]
S Leger, A Zwanenburg, K Pilz, F Lohaus, A Linge, K Zöphel, et al.
A comparative study of machine learning methods for time-to-event survival data for radiomics risk modelling.
[3]
JR Ferreira Junior, DA Cardona Cardenas, RA Moreno, MF de Sá Rebelo, JE Krieger, MA Gutierrez.
Novel chest radiographic biomarkers for COVID-19 using radiomic features associated with diagnostics and outcomes.
J Digit Imaging, 34 (2021), pp. 297-307
[4]
HJ Aerts, ER Velazquez, RR Leijenaar, C Parmar, P Grossamnn, S Carvalho, et al.
Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach.
Nat Commun, 5 (2014), pp. 4006
[5]
C Dupuis, E Montmollin, M Neuville, B Mourvillier, S Ruckly, JF. Timsit.
Limited applicability of a COVID-19 specific mortality prediction rule to the intensive care setting.
Nat Mach Intell, 3 (2021), pp. 20-22
[6]
MJR Quanjel, TC van Holten, PC Gunst-van der Vliet, J Wielaard, B Karakaya, M Söhne, et al.
Replication of a mortality prediction model in Dutch patients with COVID-19.
Nat Mach Intell, 3 (2021), pp. 23-24
[7]
M Barish, S Bolourani, LF Lau, S Shah, TP. Zanos.
External validation demonstrates limited clinical utility of the interpretable mortality prediction model for patients with COVID-19.
Nat Mach Intell, 3 (2021), pp. 25-27
[8]
Y Allenbach, D Saadoun, G Maalouf, M Vieira, A Helio, J Boddaert, et al.
Development of a multivariate prediction model of intensive care unit transfer or death: a French prospective cohort study of hospitalized COVID-19 patients.
[9]
A Sisó-Almirall, B Kostov, M Mas-Heredia, S Vilanova-Rotllan, E Sequeira-Aymar, M Sans-Corrales, et al.
Prognostic factors in Spanish COVID-19 patients: a case series from Barcelona.
[10]
JS Zhu, P Ge, C Jiang, Y Zhang, X Li, Z Zhao, et al.
Deep-learning artificial intelligence analysis of clinical variables predicts mortality in COVID-19 patients.
J Am Coll Emerg Physicians Open, 1 (2020), pp. 1364-1373
[11]
Y Huang, X Lyu, D Li, L Wang, Y Wang, W Zou, et al.
A cohort study of 676 patients indicates D-dimer is a critical risk factor for the mortality of COVID-19.
[12]
LYC Chen, RL Hoiland, S Stukas, CL Wellington, MS. Sekhon.
Assessing the importance of interleukin-6 in COVID-19.
Lancet Respir Med, 9 (2021), pp. e13
Copyright © 2022. HCFMUSP
Download PDF
Article options
es en pt

¿Es usted profesional sanitario apto para prescribir o dispensar medicamentos?

Are you a health professional able to prescribe or dispense drugs?

Você é um profissional de saúde habilitado a prescrever ou dispensar medicamentos