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The Prognostic Role of Neutrophil-to-Lymphocyte Ratio, Monocyte-to-Lymphocyte Ratio, and Platelet-to-Lymphocyte Ratio in the Risk of Major Adverse Cardiovascular Events and Mortality in Patients with COVID-19: a State-of-the-Art Review

Eliza Mihaela Arbănași
Eliza Mihaela Arbănași
 y 
Eliza Russu
Eliza Russu
   | 27 jun 2024
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Article Category: Review
Publicado en línea: 27 jun 2024
Páginas: 61 - 70
Recibido: 17 dic 2023
Aceptado: 09 ene 2024
DOI: https://doi.org/10.2478/jce-2024-0010
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© 2024 Eliza Mihaela Arbănași et al., published by Sciendo
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.

FIGURE 1.

A, ROC analysis and AUC for NLR regarding mortality. Values are expressed per 1 s.d. increase regarding the median value. B, Distribution of the optimal cut-off values for NLR regarding mortality. Values are expressed per 1 s.d. increase regarding the median value. C, The position of the optimal cut-off value depending on the sensitivity and specificity of each value, regarding mortality.
A, ROC analysis and AUC for NLR regarding mortality. Values are expressed per 1 s.d. increase regarding the median value. B, Distribution of the optimal cut-off values for NLR regarding mortality. Values are expressed per 1 s.d. increase regarding the median value. C, The position of the optimal cut-off value depending on the sensitivity and specificity of each value, regarding mortality.

FIGURE 2.

A, ROC analysis and AUC for MLR regarding mortality. Values are expressed per 1 s.d. increase regarding the median value. B, Distribution of the optimal cut-off values for MLR regarding mortality. Values are expressed per 1 s.d. increase regarding the median value. C, The position of the optimal cut-off value depending on the sensitivity and specificity of each value, regarding mortality.
A, ROC analysis and AUC for MLR regarding mortality. Values are expressed per 1 s.d. increase regarding the median value. B, Distribution of the optimal cut-off values for MLR regarding mortality. Values are expressed per 1 s.d. increase regarding the median value. C, The position of the optimal cut-off value depending on the sensitivity and specificity of each value, regarding mortality.

The association between NLR and clinical outcomes: ORs, HRs, and survival analyses

Study Biomarker OR/HR 95% CI p value Outcome Kaplan–Meier survival analysis log rank p value
Lower Upper
Fois et al.34 NLR 1.02 0.99 1.06 0.10 Mortality In-hospital mortality based on cut-off value <0.001
Abrishami et al.20 NLR 1.124 1.01 1.25 0.036 Mortality – –
Pakos et al.21 NLR 1.038 1.003 1.074 0.031 Mortality – –
Allahverdiyev et al.22 NLR 1.261 1.054 1.509 0.011 Mortality – –
Zeng et al.23 NLR 5.4 2.6 11.1 <0.001 Mortality Disease deterioration based on cut-off value <0.001
21.2 2.8 161.3
19.8 2.6 151.4
Moradi et al.36 NLR 1.03 1.003 1.07 0.03 Mortality One-month mortality based on cut-off value 0.16
Rose et al.24 NLR 1.82 1.14 2.95 0.013 Mortality – –
Halmaciu et al.25 NLR 24.13 12.2 47.73 <0.001 Mortality – –
Arbănași et al.26 NLR 16.32 9.09 29.3 <0.001 Mortality – –
Mureșan et al.27 NLR 13.07 8.29 20.62 <0.001 Mortality – –
Citu et al.28 NLR 3.85 1.35 10.95 0.01 Mortality In-hospital mortality based on cut-off value <0.001
Ghobadi et al.29 NLR 3.57 2.859 4.458 <0.0001 Mortality In-hospital mortality based on cut-off value for non-elderly and elderly <0.001 / <0.001
Regolo et al.30 NLR 1.62 – – <0.0001 Mortality In-hospital mortality based on tertiles <0.0001
Seyfi et al.31 NLR 1.121 1.072 1.179 <0.0001 Mortality – –
Zhan et al.32 NLR 2.24 1.49 4.47 <0.001 MACE 6-month MACE based on cut-off value 0.010
Arbănași et al.26 NLR 30.28 13.97 65.6 <0.001 Acute limb ischemia – –
Mureșan et al.27 NLR 11.7 7.99 17.13 <0.001 Deep vein thrombosis – –
Mureșan et al.27 NLR 10.5 5.86 18.8 <0.001 Acute pulmonary embolism – –
Predenciuc et al.33 NLR 2.46 1.0 6.03 0.04 Major amputation or mortality – –

NLR studies and predictive values for clinical outcomes

Study Year Country Biomarker Study group value Control group value Cut-off value AUC ROC analysis Sensitivity (%) Specificity (%) Outcome
Fois et al.34 2020 Italy NLR 9.17 5 15.2 0.697 38% 97% Mortality
Abrishami et al.20 2020 Iran NLR 5.02 3.02 3.65 0.678 62.5% 60% Mortality
Pakos et al.21 2020 USA NLR 6.4 4.5 – – – – Mortality
Allahverdiyev et al.22 2020 Turkey NLR 12.1 3.2 3 0.842 92% 53% Mortality
Zeng et al.23 2021 China NLR 5.33 2.14 2.6937 0.828 92.9% 63.9% Mortality
Moradi et al.36 2021 Iran NLR 5 4.1 3.3 – – – Mortality
Yildiz et al.37 2021 Belgium NLR – – 5.94 0.665 62% 64% Mortality
Karaaslan et al.38 2022 Turkey NLR 9.27 2.73 4.21 0.810 77.1% 73.7% Mortality
Kudlinski et al.39 2022 Poland NLR 17.7 12.29 11.57 0.629 63% 60.5% Mortality
Rose et al.24 2022 Switzerland NLR 8.2 5.0 – – – – Mortality
Halmaciu et al.25 2022 Romania NLR 11.04 3.73 6.97 0.869 80.5% 85.4% Mortality
Arbănași et al.26 2022 Romania NLR 8.45 3.01 4.57 0.845 86.6% 72% Mortality
Mureșan et al.27 2022 Romania NLR 9.74 5.38 9.4 0.868 81.8% 74.4% Mortality
Citu et al.28 2022 Romania NLR 13.83 8.31 9.1 0.689 70% 67% Mortality
Ghobadi et al.29 2022 Iran NLR 6.07 4.7 9.38 0.817 73.3% 86.5% Mortality
Regolo et al.30 2022 Italy NLR – – 11.38 0.772 72.9% 71.9% Mortality
Seyfi et al.31 2023 Iran NLR 11.3 5.8 7.02 0.760 63% 83% Mortality
MACE
Strazzulla et al.35 2021 France NLR 7.5 3.2 – – – – Acute pulmonary embolism
Zhan et al.32 2021 China NLR 16.28 4.75 10.14 0.803 81.2 82.6 MACE
Arbănași et al.26 2022 Romania NLR – – 8.34 0.882 81.6% 87.4% Acute limb ischemia
Mureșan et al.27 2022 Romania NLR – – 9.63 0.836 77% 77.8% Deep vein thrombosis
Mureșan et al.27 2022 Romania NLR – – 13.67 0.801 67.7% 81% Acute pulmonary embolism
Predenciuc et al.33 2022 Republic of Moldova NLR 11.1 6.3 5.4 – – – Major amputation or mortality
Khorvash et al.40 2022 Iran NLR 13.9 8.03 – – – – Acute ischemic stroke

The association between MLR and clinical outcomes: ORs, HRs, and survival analyses

Study Biomarker OR/HR 95% CI p value Outcome Kaplan–Meier survival analysis log rank p value
Lower Upper
Fois et al.34 MLR 1.60 0.62 4.09 0.32 Mortality In-hospital mortality based on cut-off value 0.006
Halmaciu et al.25 MLR 6.49 2.51 22.24 <0.001 Mortality – –
Arbănași et al.26 MLR 5.51 3.50 8.67 <0.001 Mortality – –
Mureșan et al.27 MLR 6.89 4.64 10.23 <0.001 Mortality – –
Citu et al.28 MLR 3.05 1.16 8.05 0.02 Mortality In-hospital mortality based on cut-off value <0.001
Ghobadi et al.29 MLR 1.502 1.212 1.86 <0.0001 Mortality In-hospital mortality based on cut-off value for non-elderly and elderly <0.001
Arbănași et al.26 MLR 6.82 3.51 13.28 <0.001 Acute limb ischemia – –
Mureșan et al.27 MLR 11.19 7.68 16.29 <0.001 Deep vein thrombosis – –
Mureșan et al.27 MLR 8.96 5.11 15.69 <0.001 Acute pulmonary embolism – –

General characteristics of the studies included in the analysis

Study Patients, n Mean age, years Male sex, n (%) Hypertension, n (%) Ischemic heart disease, n (%) Diabetes, n (%) Obesity, n (%) Active smoking, n (%) Observation
Fois et al.34 119 72 77 (64.7%) – – 25 (21%) 27 (22.69%) 36 (30.25%) NLR, MLR, and PLR
Abrishami et al.20 100 55.5 68 (68%) 33 (33%) 21 (21%) 21 (21%) 25 (25%) – NLR and PLR
Pakos et al.21 242 66.03 208 (85.95%) 180 (74%) – 118 (49%) – – NLR
Allahverdiyev et al.22 455 56 217 (47.7%) 170 (37.4%) 88 (19.3%) 128 (28.1%) – – NLR
Zeng et al.23 352 >60 years 133 (37.78%) 190 (53.97%) – – – – 57 (16.19%) NLR
<60 years 219 (62.22%)
Moradi et al.36 219 – 137 (62.6%) 85 (38.8%) 46 (21%) 83 (38%) – 23 (10.5%) NLR
Yildiz et al.37 198 Derivation group 64.4 110 (55%) 101 (51%) 107 (54%) 49 (25%) – 8 (4%) NLR
Validation group 65 65 (64%) 52 (51.5%) 45 (44.6%) 22 (21.8%) – 2 (2%)
Karaaslan et al.38 191 54.32 94 (49.2%) 72 (37.7%) – 44 (23%) – – NLR and PLR
Kudlinski et al.39 285 62 189 (66.3%) 153 (55.2%) 26 (9.4%) 57 (20.7%) 134 (47.7%) 20 (7%) NLR
Rose et al.24 454 – 291 (64.1%) 225 (49.6%) 137 (30.2%) 119 (26.2%) 103 (22.7%) – NLR and PLR
Halmaciu et al.25 267 71.19 159 (59.55%) 167 (62.55%) 145 (54.31%) 116 (43.45%) 69 (25.84%) 99 (37.08%) NLR and MLR
Arbănași et al.26 510 69.6 247 (62.37%) 228 (57.78%) 138 (34.85%) 150 (37.88%) 114 (28.79%) 134 (33.84%) NLR, MLR, and PLR
Mureșan et al.27 889 70.5 474 (53.32%) 735 (82.67%) 513 (57.70%) 268 (30.14%) 146 (16.42%) 256 (28.79%) NLR, MLR, and PLR
Citu et al.28 108 63.31 56 (51.9%) 76 (70.4%) 51 (47.2%) 50 (46.3%) – – NLR, MLR, and PLR
Ghobadi et al.29 1,792 Elderly 76.29 988 (55.13%) – – 522 (29.12%) – – NLR, MLR, and PLR
Non-elderly 48.35
Regolo et al.30 411 72 237 (57.7%) 244 (59.4%) 70 (17.1%) 111 (27%) – – NLR
Seyfi et al.31 312 – – – – – – – NLR
Strazzulla et al.35 184 – 103 (55.97%) – – – – – NLR and PLR
Zhan et al.32 159 – 73 (45.91%) 72 (45.28%) 15 (9.43%) 33 (20.75%) – 53 (33.33%) NLR
Predenciuc et al.33 130 71 86 (66.2%) 117 (90%) 106 (81.5) 39 (30%) – – NLR
Khorvash et al.40 211 66.28 110 (52.13%) 126 (59.7%) 53 (25.1%) 103 (48.8%) – – NLR

MLR studies and predictive values for clinical outcomes

Study Year Country Patients, n Biomarker Study group value Control group value Cut-off value AUC ROC analysis Sensitivity (%) Specificity (%) Outcome
Fois et al.34 2020 Italy 119 MLR 0.429 0.333 0.364 0.617 69% 57% Mortality
Halmaciu et al.25 2022 Romania 267 MLR 0.75 0.33 0.54 0.826 74.4% 81.6% Mortality
Arbănași et al.26 2022 Romania 510 MLR 0.62 0.32 0.45 0.758 68.4% 74% Mortality
Mureșan et al.27 2022 Romania 889 MLR 1.14 0.47 0.78 0.794 71.3% 74% Mortality
Citu et al.28 2022 Romania 108 MLR 0.83 0.53 0.69 0.661 58% 74% Mortality
Ghobadi et al.29 2022 Iran 1,792 MLR 0.20 0.16 0.26 0.628 59.4% 62.4% Mortality
MACE
Arbănași et al.26 2022 Romania 510 MLR – – 0.49 0.787 71.4% 71.6% Acute limb ischemia
Mureșan et al.27 2022 Romania 889 MLR – – 0.78 0.824 77% 76.2% Deep vein thrombosis
Mureșan et al.27 2022 Romania 889 MLR – – 0.81 0.766 71% 72.1% Acute pulmonary embolism

PLR studies and predictive values for clinical outcomes

Study Year Country Patients, n Biomarker Study group value Control group value Cut-off value AUC ROC analysis Sensitivity (%) Specificity (%) Outcome
Fois et al.34 2020 Italy 119 PLR 265 214 240 0.572 59% 58% Mortality
Abrishami et al.20 2020 Iran 100 PLR 202 160.8 – 0.559 – – Mortality
Karaaslan et al.38 2022 Turkey 191 PLR 287.5 139.94 189.5 – – – Mortality
Rose et al.24 2022 Switzerland 454 PLR 268.3 215.5 – – – – Mortality
Arbănași et al.26 2022 Romania 510 PLR 229.83 128.22 177.51 0.775 68.4% 77.5% Mortality
Mureșan et al.27 2022 Romania 889 PLR 363.16 156.22 266.9 0.819 72% 81.1% Mortality
Citu et al.28 2022 Romania 108 PLR 345 324 – – – – Mortality
Ghobadi et al.29 2022 Iran 1,792 PLR 168 154 230 0.585 52.6% 63.1% Mortality
MACE
Strazzulla et al.35 2021 France 184 PLR 259 204 – – – – Acute pulmonary embolism
Arbănași et al.26 2022 Romania 510 PLR – – 178.99 0.858 81.6% 73.1% Acute limb ischemia
Mureșan et al.27 2022 Romania 889 PLR – – 230.67 0.802 72.8% 76.8% Deep vein thrombosis
Mureșan et al.27 2022 Romania 889 PLR – – 207.06 0.734 74.2% 61.3% Acute pulmonary embolism

The association between PLR and clinical outcomes: ORs, HRs, and survival analyses

Study Biomarker OR/HR 95% CI p value Outcome Kaplan–Meier survival analysis log rank p value
Lower Upper
Fois et al.34 PLR 1.0006 1.00 1.0013 0.058 Mortality In-hospital mortality based on cut-off value 0.13
Rose et al.24 PLR 1.37 0.79 2.46 0.27 Mortality – –
Arbănași et al.26 PLR 7.47 4.71 11.83 <0.001 Mortality
Mureșan et al.27 PLR 11.04 7.34 16.62 <0.001 Mortality
Ghobadi et al.29 PLR 1.451 1.17 1.799 <0.0001 Mortality In-hospital mortality based on cut-off value for non-elderly and elderly <0.001 / 0.10
Arbănași et al.26 PLR 12.07 7.71 21.77 <0.001 Acute limb ischemia – –
Mureșan et al.27 PLR 8.36 5.82 12.02 <0.001 Deep vein thrombosis – –
Mureșan et al.27 PLR 6.26 3.54 11.07 <0.001 Acute pulmonary embolism – –
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