Skip Navigation
Skip to contents

ACC : Acute and Critical Care

OPEN ACCESS
SEARCH
Search
Advanced Search
mobile menu button

Articles

Page Path
HOME > Acute Crit Care > Volume 40(2); 2025 > Article
Original Article
Infection Neutrophil-to-lymphocyte-to-albumin ratio as a prognostic marker for mortality in sepsis and septic shock in Vietnam
Acute and Critical Care 2025;40(2):244-251.
DOI: https://doi.org/10.4266/acc.003576
Published online: May 28, 2025

1College of Health Sciences, VinUniversity, Hanoi, Vietnam

2Medical Intensive Care Unit, 108 Military Central Hospital, Hanoi, Vietnam

Corresponding Author: Pham Dang Hai Medical Intensive Care Unit, 108 Military Central Hospital, No. 1 Tran Hung Dao St, Ha Noi 100000, Vietnam Tel: +84-98-789-8960 Email: bsphamdanghai@gmail.com
• Received: August 29, 2024   • Revised: March 26, 2025   • Accepted: March 27, 2025

© 2025 The Korean Society of Critical Care Medicine

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

  • 6,339 Views
  • 111 Download
  • 6 Web of Science
  • 5 Crossref
prev next
Full Article

Download PDF Download PDF

  • Background
    Sepsis and septic shock are life-threatening global health challenges associated with high mortality rates. Early identification of high-risk patients is critical for improving outcomes. In the present study, the association between the neutrophil-to-lymphocyte-to-albumin ratio (NLAR) and mortality in septic patients was evaluated.
  • Methods
    A retrospective study was performed at a tertiary hospital in Vietnam. Patients ≥18 years of age diagnosed with sepsis or septic shock based on the Sepsis-3 criteria were included. Exclusion criteria included recent corticosteroid use within 7 days, autoimmune diseases, hematological disorders, and active cancer within 5 years. NLAR was calculated from complete blood counts and albumin levels within the first 24 hours of intensive care unit admission. Receiver operating characteristic (ROC) curves were used to determine the predictive ability of NLAR for in-hospital mortality.
  • Results
    The present study included 141 patients with a mean age of 72 years. Non-survivors were significantly older with higher rates of mechanical ventilation. NLAR was significantly elevated in non-survivors compared with survivors (median [interquartile range]: 0.88 [0.57–1.24] vs. 0.44 [0.28–0.77], P<0.001). In ROC analysis, the area under the curve for NLAR was 0.70 (P<0.001). Using a cutoff value of 0.56, NLAR showed a sensitivity of 77.8% and a specificity of 61.5% for predicting in-hospital mortality.
  • Conclusions
    Elevated NLAR on admission was associated with a higher mortality rate in sepsis patients. NLAR could be used as an early prognostic marker for sepsis mortality.
  • Key Words: mortality; neutrophil-to-lymphocyte-to-albumin ratio; sepsis; septic shock
Sepsis is a life-threatening condition and a public health challenge globally. The prevalence of sepsis and septic shock has been steadily increasing, reaching around 49 million cases of sepsis and 11 million sepsis-related deaths worldwide in 2017 [1]. Although significantly developed for the management of patients, sepsis remains a leading cause of death across the world, with a mortality rate of 34.7% in a meta-analysis in 2020 [2]. One critical principle for the management of sepsis is early and accurate detection of patients at high risk of death [3]. Although many biomarkers, such as interleukin 6, procalcitonin, lactate, presepsin, and neutrophil-to-white blood cell ratio (NWR), have been investigated to predict 28-day mortality in patients with sepsis, future research is needed to discover useful markers for sepsis prognosis [4].
The complete blood count has been an indispensable laboratory test for the initial evaluation of sepsis and sepsis shock patients. Based on the complete blood count, the neutrophil-to-lymphocyte ratio (NLR) can be easily calculated. Although the mechanism of NLR elevation is unclear, the explanation may be based on the pathophysiology of neutrophilia and lymphopenia with systemic inflammation and stress [5]. In several studies, neutrophils were elevated in response to the increase in proinflammatory mediators and lymphocytes decreased due to sepsis-induced apoptosis in systemic inflammatory conditions similar to sepsis [6-8]. Some authors have validated the predictive value of NLR in the prognosis of sepsis severity and outcomes [9,10]. Albumin, a key protein in the human body, plays a critical role in modulating inflammation, maintaining oncotic pressure, and neutralizing oxidative stress [11]. Hypoalbuminemia was associated with short- and long-term outcomes in septic patients, including increased mortality [12,13]. Serum albumin was shown to have a predictive value in 30-day mortality in septic patients, especially in patients with low-to-medium Sequential Organ Failure Assessment (SOFA) scores [14]. In addition, biomarkers incorporating albumin, such as the lactate-to-albumin ratio, have demonstrated prognostic value in sepsis [15]. Based on the heavy burden of sepsis, septic shock, and the prognostic value of the NLR and albumin, the neutrophil-to-lymphocyte-to-albumin ratio (NLAR) was evaluated in the present study as a novel biomarker for predicting in-hospital mortality in patients with sepsis and septic shock.
The Ethics Committee of the 108 Military Central Hospital approved this study (No. 488/GCN- BV) and waived the need for informed consent due to the retrospective study design.
Study Population
This was a retrospective observational study conducted at the intensive care unit (ICU) of a tertiary hospital in Vietnam, focusing on patients admitted for sepsis or septic shock between January 2021 and December 2022. Inclusion criteria included all patients >18 years of age diagnosed with sepsis or septic shock according to the Sepsis-3 criteria. Patients were excluded if they had used corticosteroids within the past 7 days, had a history of autoimmune diseases or hematological disorders, or had active cancer within the past 5 years (Figure 1).
Data Collection
Data were collected from patient medical records. Information included demographic details (age, sex), medical history (comorbidities), vital signs, source of infection, mechanical ventilator requirement, continuous renal replacement therapy, and in-hospital mortality. Laboratory test results including complete blood count (white blood cell [WBC] count, neutrophil count, lymphocyte count, red blood cell count, hemoglobin, hematocrit, platelet), biochemistry panel (urea, creatinine, aspartate aminotransferase, alanine aminotransferase, total bilirubin, albumin, procalcitonin, electrolytes), lactate, and blood culture within the first 24 hours of ICU admission were collected. The NLR was calculated as the absolute neutrophil count divided by the absolute lymphocyte count. The NLAR was defined as the ratio of the NLR to the albumin level. SOFA, Acute Physiology and Chronic Health Evaluation (APACHE) II, Simplified Acute Physiology Score (SAPS) II, and modified Nutrition Risk in the Critically Ill (mNUTRIC) scores were calculated within 24 hours of ICU admission.
Statistical Analysis
Epi Info version 7.6.0.2, SPSS Statistics 29 (IBM Corp.) was used for data analysis. Categorical variables were described as frequencies (percentages). Continuous variables were introduced as mean±standard deviation for parametric variables or median (interquartile range) for nonparametric variables. Categorical variables were analyzed using the appropriate chi-square test or Fisher's exact test. Normally distributed data were analyzed using the Student t-test and non-normally distributed data analyzed using the Mann-Whitney U-test. The receiver operating characteristic (ROC) curve was performed to calculate the area under the curve (AUC) for NLR and NLAR to predict in-hospital mortality. The best cutoff value was chosen as the maximum value of the sum of sensitivity and specificity. Univariable and multivariable logistic regression analyses were used to confirm independent predictors of in-hospital mortality. Results were considered statistically significant when the P-value was <0.05.
A total of 141 patients were included in the study after screening for exclusion criteria. The study population had a mean age of 72 years, with non-survivors being significantly older (mean age, 76.8 vs. 69.8 years; P<0.01). Males represented 70.2% of the population with no significant sex difference between survivors and non-survivors. Hypertension (53.2%) and diabetes mellitus (35.5%) were common comorbidities, showing similar prevalence among survivors and non-survivors. The proportion of septic shock was 80.1%. Non-survivors had higher rates of mechanical ventilation (80.0% vs. 43.8%) and continuous renal replacement therapy (64.4% vs. 31.3%) compared with survivors. Respiratory tract infections accounted for the majority of cases at 44.7%. Pneumonia was significantly more prevalent among non-survivors than survivors (68.9% vs. 33.3%, P<0.001) and urinary tract infections were more common among survivors than non-survivors (26% vs. 2.2%). Non-survivors had significantly higher median SOFA, APACHE II, SAPS II, and mNUTRIC scores than survivors (P<0.01) (Table 1).
The median WBC and neutrophil counts in the study population were 14.7 G/L and 13.4 G/L, respectively, with similar values observed between survivors and non-survivors. However, non-survivors exhibited lower absolute lymphocyte counts than survivors (0.55 G/L vs. 0.91 G/L; P<0.001). The NLR and NLAR were notably elevated in non-survivors compared with survivors: NLR (median [interquartile range]: 23.0 [13.0–35.9] vs. 12.1 [8.4–20.4], P<0.001) and NLAR (0.88 [0.57–1.24] vs. 0.44 [0.28–0.77], P<0.001). Albumin level was lower in non-survivors than in survivors (28.3 [24.3–31.0] vs. 29.6 [26.9–32.7], P=0.01) (Table 2).
The NLR and NLAR demonstrated statistically significant predictive ability for mortality with AUCs of 0.68 and 0.70, respectively (Figure 2). The optimal cutoff value for NLR was 22.9, showing 51.1% sensitivity and 81.3% specificity. Similarly, the optimal cutoff for NLAR was 0.56 with 77.8% sensitivity and 61.5% specificity (Table 3). In multivariable logistic regression, factors significantly associated with increased mortality included the requirement for mechanical ventilation, higher SOFA score, and elevated NLAR. Mechanical ventilation was associated with a 4.23-fold increase in mortality risk. In addition, each point increase in SOFA score and NLAR was associated with substantial increases in mortality risk (1.16-fold and 3.17-fold, respectively) (Table 4).
Sepsis is a complex infectious condition with high prevalence and mortality [1]. In the present study, non-survivors had significantly higher NLR and NLAR compared with survivors of sepsis. After adjusting for potential covariates, NLAR maintained its correlation with in-hospital mortality (odds ratio [OR], 3.17; 95% CI, 1.58–6.36). The AUCs in ROC curve analysis for NLR and NLAR were 0.68 (95% CI, 0.60–0.76) and 0.70 (95% CI, 0.62–0.78), respectively. With a cutoff of 0.56, NLAR had a sensitivity of 77.8% and specificity of 61.5% for in-hospital mortality. To the best of our knowledge, this was the first study in which NLAR was investigated as a novel predictor of mortality in patients with sepsis.
Patients who suffer from sepsis have to take into account the short-term high mortality rate and long-term sequelae. In a nationwide population-based study from Taiwan, an increased all-cause mortality in sepsis survivors was observed compared with the overall population, which persisted for up to 5 years [16]. In developing countries, a good prognostication tool can help healthcare providers allocate resources more quickly to sicker patients, leading to better patient outcomes and reducing post-sepsis complications. The SOFA score has been used both as a diagnostic tool and a prognostic tool for sepsis. The SOFA score was validated in many studies with different populations, including the Vietnamese population [17,18]. However, calculation of the score includes six complicated parameters that require results from arterial blood gas. Thus, NLR and NLAR could be simpler alternatives for predicting sepsis prognosis, particularly in resource-limited settings.
NLR has been suggested a novel marker that reflects two key immune systems including innate immunity and adaptive immunity [19]. NLR increases in various situations where physiological stress rises, including sepsis [20]. In the hyperinflammatory phase, a surge in neutrophils occurs, driven by pro-inflammatory mediators as a process of the innate immunity, leading to an elevated NLR [21]. Dysfunction of the adaptive immunity, represented by significant lymphopenia, is a hallmark of sepsis [7]. A marked increase in lymphocyte apoptosis was observed in septic shock patients when compared with healthy controls [8]. As sepsis progresses and the immune system becomes exhausted, lymphopenia may worsen, further contributing to a high NLR. However, in the later stages of immunoparalysis, both neutrophil production and function may be impaired, potentially leading to a decrease in NLR. This highlights the complex relationship between NLR and the different immune phases of sepsis. Although in the present study NLR was measured at a single time point after admission and cannot fully capture these dynamic changes, it provides valuable insights into the prognostic value of NLR at the initial presentation of sepsis.
NLR was significantly higher in non-survivors compared with survivors of sepsis in a 2019 meta-analysis [9]. However, a significant heterogeneity existed between studies. We hypothesized that incorporating albumin into NLR could enhance its prognostic value. Albumin, which accounts for more than half of human plasma proteins, plays a vital role in the body. Albumin is essential during the inflammatory process for expanding volume, transporting important substances, and protecting from oxidative stress [11]. Hypoalbuminemia in sepsis can reflect the severity of inflammation, nutritional status, and the interplay between liver function and gut microbiota, all of which are associated with worse outcomes [12,22,23]. By combining NLR with albumin, NLAR may offer a more comprehensive assessment of the patient's physiological state and immune response. Although both NLR and NLAR can be elevated in various inflammatory conditions, the potential to reflect both immune dysregulation and nutritional status renders NLAR a promising prognostic marker in sepsis. Compared with other similar indices, such as the delta neutrophil index, which focuses solely on neutrophil changes, and the neutrophil percentage-to-albumin ratio (NPAR), which does not include lymphocyte counts, NLAR may offer a broader perspective on sepsis pathophysiology [24,25].
In a study in China, an association was found between elevated NPAR and mortality in sepsis patients [25]. Although both NLAR and NPAR incorporate neutrophils and albumin, NLAR also includes lymphocyte count which reflects the adaptive immunity and is significantly affected in sepsis. Thus, the inclusion of lymphocytes in NLAR could provide a more comprehensive overview of the host's immune response to infection.
In infection, neutrophils are the first line of defense because they are rapidly mobilized from the bone marrow and migrate to the infection site, leading to neutrophilia. However, in sepsis, spontaneous apoptosis of neutrophils was found inhibited and the lifespan of neutrophils was extended. In addition, all four stages of neutrophil margination were found affected during sepsis [21]. In the present study, a difference was not observed in neutrophil count between survivors and non-survivors (13.3 G/L vs. 14.4 G/L, P=0.957). Conversely, extensive lymphocyte apoptosis and T-cell anergy were described in sepsis [8]. These processes lead to lymphopenia and sepsis-induced immunosuppression. In the present study, a significantly lower lymphocyte count was observed in non-survivors (0.55 G/L vs. 0.91 G/L, P<0.001). In addition, the albumin level in non-survivors was lower than in survivors (28.3 g/L vs. 29.6 g/L, P=0.010). NLAR incorporates three variables, neutrophils, lymphocytes, and albumin, representing different aspects of sepsis pathophysiology. Despite the similar AUC for NLAR compared with NLR, NLAR could more adequately capture the complexity of sepsis pathogenesis.
The present study had several limitations. First, this was a single-center, retrospective study inherently prone to biases. Second, the study population was small and the baseline characteristics do not represent the overall population of Vietnam. Third, although many variables were included in the analyses, possible confounders may still exist that can alter the relationship between independent and dependent variables, possibly leading to bias. Finally, the NLAR was recorded only on admission and changes in NLAR could not be monitored during hospitalization. The results of the present study should be validated in future studies including larger, multicenter cohorts and the dynamic changes in NLAR explored during the course of sepsis treatment.
In conclusion, elevated NLAR level on admission was associated with poor outcomes in patients with sepsis. Due to the simplicity of NLAR and ability to reflect complex pathogenesis, NLAR can be considered a rapid and effective tool for sepsis prognostication. However, further research is needed to confirm the robustness of NLAR in predicting sepsis severity.
▪ Elevated neutrophil-to-lymphocyte-to-albumin ratio (NLAR) was associated with significantly higher mortality rates in septic patients.
▪ NLAR demonstrated moderate predictive ability for in-hospital mortality, with area under the curve of 0.70 in receiver operating characteristic analysis.
▪ Elevated NLAR could potentially serve as an early prognostic marker for identifying high-risk septic patients.

CONFLICT OF INTEREST

No potential conflict of interest relevant to this article was reported.

FUNDING

None.

ACKNOWLEDGMENTS

None.

AUTHOR CONTRIBUTIONS

Conceptualization: NVVT, PDH. Methodology: NVVT, PDH. Formal analysis: NVVT. Data curation: NVVT. Visualization: NVVT. Project administration: PDH. Writing - original draft: NVVT, LTL, NTTV. Writing - review & editing: PDH. All authors read and agreed to the published version of the manuscript.

Figure 1.
Flowchart of patient selection process.
acc-003576f1.jpg
Figure 2.
Receiver operating characteristic curves of the neutrophil-to-lymphocyte ratio (NLR), neutrophil-to-lymphocyte-to-albumin ratio (NLAR), and severity scores as predictors for in-hospital mortality. SOFA: Sequential Organ Failure Assessment; APACHE: Acute Physiology and Chronic Health Evaluation.
acc-003576f2.jpg
Table 1.
Baseline characteristics of the study population
Variable Total (n=141) Survivor (n=96) Non-survivor (n=45) P-value
Age (yr) 72±14 70±14 77±13 0.006
Male 99 (70.2) 62 (64.6) 34 (82.2) 0.033
Comorbidity
 Hypertension 75 (53.2) 48 (50.0) 27 (60.0) 0.267
 Diabetes mellitus 50 (35.5) 32 (33.3) 18 (40.0) 0.440
 Stroke 28 (19.9) 17 (17.7) 11 (24.4) 0.350
 Chronic coronary disease 8 (5.7) 5 (5.2) 3 (6.7) 0.727
 Heart failure 12 (8.5) 5 (5.2) 7 (15.6) 0.040
 COPD 6 (4.3) 2 (2.1) 4 (8.9) 0.062
 Liver cirrhosis 3 (2.1) 1 (1.0) 2 (4.4) 0.192
 Chronic kidney disease 19 (13.5) 8 (8.3) 11 (24.4) 0.009
Clinical features of severity
Septic shock 113 (80.1) 73 (76.0) 23 (88.9) 0.075
 Positive blood culture 48 (34.0) 33 (34.4) 15 (34.1) 0.974
 Mechanical ventilation 78 (55.3) 42 (43.8) 36 (80.0) <0.001
 CRRT 59 (41.8) 30 (31.3) 29 (64.4) <0.001
Site of infection
 Pulmonary 63 (44.7) 32 (33.3) 31 (68.9) <0.001
 Gastrointestinal 28 (19.9) 22 (22.9) 6 (13.3) 0.184
 Urinary 26 (18.4) 25 (26.0) 1 (2.2) 0.001
 Skin and soft tissue 7 (5.0) 4 (4.2) 3 (6.7) 0.524
Hemodynamics
 SBP (mm Hg) 107 (94–120) 110 (95–120) 100 (93–120) 0.875
 DBP (mm Hg) 60 (50–70) 60 (50–70) 60 (50–70) 0.632
 MAP (mm Hg) 77 (70–86) 77 (69–87) 73 (70–83) 0.832
 HR (bpm) 110 (95–129) 110 (90–125) 118 (100–130) 0.296
Severity score
 SOFA 10 (8–13) 9 (7–12) 12 (10–14) <0.001
 APACHE II 20 (16–24) 19 (15–23) 22 (20–24) 0.003
 SAPS II 45 (37–57) 42 (33–52) 52 (43–64) <0.001
 mNUTRIC 5 (4–6) 5 (3–6) 6 (6–7) <0.001

Values are presented as mean±standard deviation, number (%), or median (interquartile range).

COPD: chronic obstructive pulmonary disease; CRRT: continuous renal replacement therapy; SBP: systolic blood pressure; DBP: diastolic blood pressure; MAP: mean arterial pressure; HR: heart rate; SOFA: Sequential Organ Failure Assessment; APACHE: Acute Physiology and Chronic Health Evaluation; SAPS: Simplified Acute Physiology Score; mNUTRIC: modified Nutrition Risk in the Critically Ill.

Table 2.
Laboratory features of the study population
Variable Total (n=141) Survivor (n=96) Non-survivor (n=45) P-value
WBC count (G/L) 14.7 (9.1–20.8) 14.6 (8.6–20.8) 15.2 (11.0–20.5) 0.739
Neutrophil (G/L) 13.4 (8.0–18.9) 13.3 (7.3–18.9) 14.4 (9.3–18.6) 0.957
Lymphocyte (G/L) 0.78 (0.45–1.26) 0.91 (0.53–1.33) 0.55 (0.30–0.79) <0.001
NLR 15.2 (9.0–25.5) 12.1 (8.4–20.4) 23.0 (13.0–35.9) <0.001
NLAR 0.57 (0.31–0.93) 0.44 (0.28–0.77) 0.88 (0.57–1.24) <0.001
RBC count (T/L) 4.0 (3.3–4.5) 4.3 (3.5–4.7) 3.6 (3.1–4.0) <0.001
Hemoglobin (g/L) 118 (96–132) 124 (106–136) 101 (93–116) <0.001
HCT (%) 36.5 (30.2–40.7) 38.2 (32.6–41.8) 31.9 (27.2–37.0) <0.001
Platelet count (G/L) 199 (113–270) 198 (123–260) 212 (86–303) 0.915
Urea (mmol/L) 13.1 (9.5–19.9) 12.6 (9.0–17.9) 15.0 (11.7–23.1) 0.194
Creatinine (µmol/L) 173 (113–270) 168 (109–255) 187 (137–279) 0.619
AST (U/L) 49 (30–173) 49 (30–160) 56 (37–250) 0.361
ALT (U/L) 41 (20–121) 41 (20–115) 47 (22–168) 0.452
Total bilirubin (µmol/L) 19.4 (12.1–30.6) 18.4 (12.1–30.3) 22.0 (12.1–31.7) 0.569
Albumin (g/L) 28.9 (26.0–32.0) 29.6 (26.9–32.7) 28.3 (24.3–31.0) 0.010
Procalcitonin (ng/mL) 20.7 (4.8–98.9) 36.9 (5.7–114.6) 11.8 (4.4–38.3) 0.022
Sodium (mmol/L) 136 (132–140) 136 (132–140) 136 (132–140) 0.614
Potassium (mmol/L) 3.8 (3.3–4.5) 3.7 (3.3–4.2) 4.2 (3.6–4.7) 0.115
Bicarbonate (mmol/L) 18.9 (15.2–22.5) 19.2 (15.6–22.4) 17.8 (15.0–22.6) 0.598
Lactate (mmol/L) 3.5 (2.1–6.1) 3.1 (1.9–5.4) 4.0 (2.8–7.1) 0.020

Values are presented as median (interquartile range).

WBC: white blood cell; NLR: neutrophil-lymphocyte ratio; NLAR: neutrophil-to-lymphocyte-to-albumin ratio; RBC: red blood cell; HCT: hematocrit; AST: aspartate aminotransferase; ALT: alanine aminotransferase.

Table 3.
ROC analysis of NLR, NLAR, SOFA score, and APACHE II score as predictors for in-hospital mortality
Variable Cutoff Sensitivity (%) Specificity (%) AUC 95% CI P-value
NLR 22.9 51.1 81.3 0.68 0.60–0.76 <0.001
NLAR 0.56 77.8 61.5 0.70 0.62–0.78 <0.001
SOFA score 10 65.6 66.7 0.70 0.62–0.78 <0.001
APACHE II score 18 50.0 82.2 0.65 0.57–0.73 0.001

ROC: receiver operating characteristic; NLR: neutrophil-lymphocyte ratio; NLAR: neutrophil-to-lymphocyte-to-albumin ratio; SOFA: Sequential Organ Failure Assessment; APACHE: Acute Physiology and Chronic Health Evaluation; AUC: area under the curve.

Table 4.
Multivariable logistic regression of NLAR and in-hospital mortality
Variable In-hospital mortality
OR 95% CI P-value
Age 1.03 0.99–1.06 0.134
History of heart failure 1.76 0.44–7.01 0.422
Mechanical ventilation 4.23 1.44–12.44 0.009
SOFA score 1.16 1.01–1.33 0.039
NLAR 3.17 1.59–6.36 0.001

NLAR: neutrophil-to-lymphocyte-to-albumin ratio; OR: odds ratio; SOFA: Sequential Organ Failure Assessment.

  • 1. Rudd KE, Johnson SC, Agesa KM, Shackelford KA, Tsoi D, Kievlan DR, et al. Global, regional, and national sepsis incidence and mortality, 1990-2017: analysis for the Global Burden of Disease Study. Lancet 2020;395:200-11.ArticlePubMedPMC
  • 2. Bauer M, Gerlach H, Vogelmann T, Preissing F, Stiefel J, Adam D. Mortality in sepsis and septic shock in Europe, North America and Australia between 2009 and 2019: results from a systematic review and meta-analysis. Crit Care 2020;24:239.ArticlePubMedPMCPDF
  • 3. Evans L, Rhodes A, Alhazzani W, Antonelli M, Coopersmith CM, French C, et al. Surviving sepsis campaign: international guidelines for management of sepsis and septic shock 2021. Intensive Care Med 2021;47:1181-247.ArticlePubMedPMC
  • 4. Molano-Franco D, Arevalo-Rodriguez I, Muriel A, Del Campo-Albendea L, Fernández-García S, Alvarez-Méndez A, et al. Basal procalcitonin, C-reactive protein, interleukin-6, and presepsin for prediction of mortality in critically ill septic patients: a systematic review and meta-analysis. Diagn Progn Res 2023;7:15.ArticlePubMedPMCPDF
  • 5. van der Poll T, Shankar-Hari M, Wiersinga WJ. The immunology of sepsis. Immunity 2021;54:2450-64.ArticlePubMed
  • 6. Shen XF, Cao K, Jiang JP, Guan WX, Du JF. Neutrophil dysregulation during sepsis: an overview and update. J Cell Mol Med 2017;21:1687-97.ArticlePubMedPMCPDF
  • 7. de Pablo R, Monserrat J, Prieto A, Alvarez-Mon M. Role of circulating lymphocytes in patients with sepsis. Biomed Res Int 2014;2014:671087.ArticlePubMedPMC
  • 8. Zhang Y, Li J, Lou J, Zhou Y, Bo L, Zhu J, et al. Upregulation of programmed death-1 on T cells and programmed death ligand-1 on monocytes in septic shock patients. Crit Care 2011;15:R70.ArticlePubMedPMCPDF
  • 9. Huang Z, Fu Z, Huang W, Huang K. Prognostic value of neutrophil-to-lymphocyte ratio in sepsis: a meta-analysis. Am J Emerg Med 2020;38:641-7.ArticlePubMed
  • 10. Liu X, Shen Y, Wang H, Ge Q, Fei A, Pan S. Prognostic significance of neutrophil-to-lymphocyte ratio in patients with sepsis: a prospective observational study. Mediators Inflamm 2016;2016:8191254.ArticlePubMedPMCPDF
  • 11. Arroyo V, García-Martinez R, Salvatella X. Human serum albumin, systemic inflammation, and cirrhosis. J Hepatol 2014;61:396-407.ArticlePubMed
  • 12. Cao Y, Su Y, Guo C, He L, Ding N. Albumin level is associated with short-term and long-term outcomes in sepsis patients admitted in the ICU: a large public database retrospective research. Clin Epidemiol 2023;15:263-73.ArticlePubMedPMCPDF
  • 13. Furukawa M, Kinoshita K, Yamaguchi J, Hori S, Sakurai A. Sepsis patients with complication of hypoglycemia and hypoalbuminemia are an early and easy identification of high mortality risk. Intern Emerg Med 2019;14:539-48.ArticlePubMedPMCPDF
  • 14. Turcato G, Zaboli A, Sibilio S, Fanni Canelles M, Rella E, Giudiceandrea A, et al. Prognostic role of serum albumin in predicting 30-day mortality in patients with infections in emergency department: a prospective study. J Clin Med 2023;12:3447.ArticlePubMedPMC
  • 15. Bou Chebl R, Geha M, Assaf M, Kattouf N, Haidar S, Abdeldaem K, et al. The prognostic value of the lactate/albumin ratio for predicting mortality in septic patients presenting to the emergency department: a prospective study. Ann Med 2021;53:2268-77.ArticlePubMedPMC
  • 16. Ou SM, Chu H, Chao PW, Lee YJ, Kuo SC, Chen TJ, et al. Long-term mortality and major adverse cardiovascular events in sepsis survivors: a nationwide population-based study. Am J Respir Crit Care Med 2016;194:209-17.ArticlePubMed
  • 17. Phu TN, Thao DT, Thu VP, Truyen NV. Septic shock outcome and factors associated with mortality in the intensive care unit in Vietnam. J Med Assoc Thai 2021;104:1249-54.Article
  • 18. Do SN, Dao CX, Nguyen TA, Nguyen MH, Pham DT, Nguyen NT, et al. Sequential Organ Failure Assessment (SOFA) Score for predicting mortality in patients with sepsis in Vietnamese intensive care units: a multicentre, cross-sectional study. BMJ Open 2023;13:e064870. ArticlePubMedPMC
  • 19. Buonacera A, Stancanelli B, Colaci M, Malatino L. Neutrophil to lymphocyte ratio: an emerging marker of the relationships between the immune system and diseases. Int J Mol Sci 2022;23:3636.ArticlePubMedPMC
  • 20. Zahorec R. Neutrophil-to-lymphocyte ratio, past, present and future perspectives. Bratisl Lek Listy 2021;122:474-88.ArticlePubMed
  • 21. Zhang F, Liu AL, Gao S, Ma S, Guo SB. Neutrophil dysfunction in sepsis. Chin Med J (Engl) 2016;129:2741-4.ArticlePubMedPMC
  • 22. Artigas A, Wernerman J, Arroyo V, Vincent JL, Levy M. Role of albumin in diseases associated with severe systemic inflammation: pathophysiologic and clinical evidence in sepsis and in decompensated cirrhosis. J Crit Care 2016;33:62-70.ArticlePubMed
  • 23. Riviati N, Indrajaya T, Saleh I, Ali Z, et al. Serum albumin as prognostic marker for older adults in hospital and community settings. Gerontol Geriatr Med 2024;10:23337214241249914.ArticlePubMedPMCPDF
  • 24. Ahn C, Kim W, Lim TH, Cho Y, Choi KS, Jang BH. The delta neutrophil index (DNI) as a prognostic marker for mortality in adults with sepsis: a systematic review and meta-analysis. Sci Rep 2018;8:6621.ArticlePubMedPMCPDF
  • 25. Hu C, He Y, Li J, Zhang C, Hu Q, Li W, et al. Association between neutrophil percentage-to-albumin ratio and 28-day mortality in Chinese patients with sepsis. J Int Med Res 2023;51:3000605231178512.ArticlePubMedPDF

Figure & Data

References

    Citations

    Citations to this article as recorded by  
    • Vitamin B1 and sepsis: a prospective single-center study
      Wenbo Yan, Yushu Ma, Jingping Yang, Hongyan Wang, Tiewei Li
      Frontiers in Nutrition.2026;[Epub]     CrossRef
    • Altered albumin/neutrophil to lymphocyte ratio are associated with all-cause and cardiovascular mortality for advanced cardiovascular-kidney-metabolic syndrome
      Xiaoshuang Yin, Jinmei Zou, Jing Yang
      Frontiers in Nutrition.2025;[Epub]     CrossRef
    • The Neutrophil-to-Albumin Ratio (NAR) Reflects the Severity of the Post-CABG Inflammatory Response and Is Associated with a Pre-Existing Pro-Inflammatory Monocyte Profile
      Mikhail A. Popov, Siarhei A. Dabravolski, Vladislav V. Dontsov, Sergei A. Vzvarov, Evgeniy G. Agafonov, Dmitriy I. Zybin, Alexandra K. Kharabet, Olga V. Radchenkova, Dmitriy R. Saveliev, Victoria P. Pronina, Svetlana S. Verkhova, Nikita G. Nikiforov, Yego
      Life.2025; 15(12): 1790.     CrossRef
    • Neutrophil Extracellular Traps in Sepsis and Sepsis-Related Organ Dysfunction
      Wenbo Yan, Xiyuan Xu, Xiaojuan Li, Yushu Ma, Lining Guo, Jingping Yang, Zhipeng Jin, Jie Zhang, Tiewei Li
      ImmunoTargets and Therapy.2025; Volume 14: 1373.     CrossRef
    • Diagnostic utility of serum prostate-specific antigen and circulating inflammatory markers for differentiating prostate cancer from benign prostatic hyperplasia
      Dawei Luo
      American Journal of Cancer Research.2025; 15(11): 4765.     CrossRef

    • PubReader PubReader
    • ePub LinkePub Link
    • Cite
      CITE
      export Copy
      Close
      Download Citation
      Download a citation file in RIS format that can be imported by all major citation management software, including EndNote, ProCite, RefWorks, and Reference Manager.
      Format:
      • RIS — For EndNote, ProCite, RefWorks, and most other reference management software
      • BibTeX — For JabRef, BibDesk, and other BibTeX-specific software
      Include:
      • Citation for the content below
      Neutrophil-to-lymphocyte-to-albumin ratio as a prognostic marker for mortality in sepsis and septic shock in Vietnam
      Acute Crit Care. 2025;40(2):244-251.   Published online May 28, 2025
      DOI: https://doi.org/10.4266/acc.003576
      Close
    • XML DownloadXML Download
    Figure
    • 0
    • 1
    Neutrophil-to-lymphocyte-to-albumin ratio as a prognostic marker for mortality in sepsis and septic shock in Vietnam
    Image Image
    Figure 1. Flowchart of patient selection process.
    Figure 2. Receiver operating characteristic curves of the neutrophil-to-lymphocyte ratio (NLR), neutrophil-to-lymphocyte-to-albumin ratio (NLAR), and severity scores as predictors for in-hospital mortality. SOFA: Sequential Organ Failure Assessment; APACHE: Acute Physiology and Chronic Health Evaluation.

    Figure 1.

    Figure 2.

    Neutrophil-to-lymphocyte-to-albumin ratio as a prognostic marker for mortality in sepsis and septic shock in Vietnam
    Variable Total (n=141) Survivor (n=96) Non-survivor (n=45) P-value
    Age (yr) 72±14 70±14 77±13 0.006
    Male 99 (70.2) 62 (64.6) 34 (82.2) 0.033
    Comorbidity
     Hypertension 75 (53.2) 48 (50.0) 27 (60.0) 0.267
     Diabetes mellitus 50 (35.5) 32 (33.3) 18 (40.0) 0.440
     Stroke 28 (19.9) 17 (17.7) 11 (24.4) 0.350
     Chronic coronary disease 8 (5.7) 5 (5.2) 3 (6.7) 0.727
     Heart failure 12 (8.5) 5 (5.2) 7 (15.6) 0.040
     COPD 6 (4.3) 2 (2.1) 4 (8.9) 0.062
     Liver cirrhosis 3 (2.1) 1 (1.0) 2 (4.4) 0.192
     Chronic kidney disease 19 (13.5) 8 (8.3) 11 (24.4) 0.009
    Clinical features of severity
    Septic shock 113 (80.1) 73 (76.0) 23 (88.9) 0.075
     Positive blood culture 48 (34.0) 33 (34.4) 15 (34.1) 0.974
     Mechanical ventilation 78 (55.3) 42 (43.8) 36 (80.0) <0.001
     CRRT 59 (41.8) 30 (31.3) 29 (64.4) <0.001
    Site of infection
     Pulmonary 63 (44.7) 32 (33.3) 31 (68.9) <0.001
     Gastrointestinal 28 (19.9) 22 (22.9) 6 (13.3) 0.184
     Urinary 26 (18.4) 25 (26.0) 1 (2.2) 0.001
     Skin and soft tissue 7 (5.0) 4 (4.2) 3 (6.7) 0.524
    Hemodynamics
     SBP (mm Hg) 107 (94–120) 110 (95–120) 100 (93–120) 0.875
     DBP (mm Hg) 60 (50–70) 60 (50–70) 60 (50–70) 0.632
     MAP (mm Hg) 77 (70–86) 77 (69–87) 73 (70–83) 0.832
     HR (bpm) 110 (95–129) 110 (90–125) 118 (100–130) 0.296
    Severity score
     SOFA 10 (8–13) 9 (7–12) 12 (10–14) <0.001
     APACHE II 20 (16–24) 19 (15–23) 22 (20–24) 0.003
     SAPS II 45 (37–57) 42 (33–52) 52 (43–64) <0.001
     mNUTRIC 5 (4–6) 5 (3–6) 6 (6–7) <0.001
    Variable Total (n=141) Survivor (n=96) Non-survivor (n=45) P-value
    WBC count (G/L) 14.7 (9.1–20.8) 14.6 (8.6–20.8) 15.2 (11.0–20.5) 0.739
    Neutrophil (G/L) 13.4 (8.0–18.9) 13.3 (7.3–18.9) 14.4 (9.3–18.6) 0.957
    Lymphocyte (G/L) 0.78 (0.45–1.26) 0.91 (0.53–1.33) 0.55 (0.30–0.79) <0.001
    NLR 15.2 (9.0–25.5) 12.1 (8.4–20.4) 23.0 (13.0–35.9) <0.001
    NLAR 0.57 (0.31–0.93) 0.44 (0.28–0.77) 0.88 (0.57–1.24) <0.001
    RBC count (T/L) 4.0 (3.3–4.5) 4.3 (3.5–4.7) 3.6 (3.1–4.0) <0.001
    Hemoglobin (g/L) 118 (96–132) 124 (106–136) 101 (93–116) <0.001
    HCT (%) 36.5 (30.2–40.7) 38.2 (32.6–41.8) 31.9 (27.2–37.0) <0.001
    Platelet count (G/L) 199 (113–270) 198 (123–260) 212 (86–303) 0.915
    Urea (mmol/L) 13.1 (9.5–19.9) 12.6 (9.0–17.9) 15.0 (11.7–23.1) 0.194
    Creatinine (µmol/L) 173 (113–270) 168 (109–255) 187 (137–279) 0.619
    AST (U/L) 49 (30–173) 49 (30–160) 56 (37–250) 0.361
    ALT (U/L) 41 (20–121) 41 (20–115) 47 (22–168) 0.452
    Total bilirubin (µmol/L) 19.4 (12.1–30.6) 18.4 (12.1–30.3) 22.0 (12.1–31.7) 0.569
    Albumin (g/L) 28.9 (26.0–32.0) 29.6 (26.9–32.7) 28.3 (24.3–31.0) 0.010
    Procalcitonin (ng/mL) 20.7 (4.8–98.9) 36.9 (5.7–114.6) 11.8 (4.4–38.3) 0.022
    Sodium (mmol/L) 136 (132–140) 136 (132–140) 136 (132–140) 0.614
    Potassium (mmol/L) 3.8 (3.3–4.5) 3.7 (3.3–4.2) 4.2 (3.6–4.7) 0.115
    Bicarbonate (mmol/L) 18.9 (15.2–22.5) 19.2 (15.6–22.4) 17.8 (15.0–22.6) 0.598
    Lactate (mmol/L) 3.5 (2.1–6.1) 3.1 (1.9–5.4) 4.0 (2.8–7.1) 0.020
    Variable Cutoff Sensitivity (%) Specificity (%) AUC 95% CI P-value
    NLR 22.9 51.1 81.3 0.68 0.60–0.76 <0.001
    NLAR 0.56 77.8 61.5 0.70 0.62–0.78 <0.001
    SOFA score 10 65.6 66.7 0.70 0.62–0.78 <0.001
    APACHE II score 18 50.0 82.2 0.65 0.57–0.73 0.001
    Variable In-hospital mortality
    OR 95% CI P-value
    Age 1.03 0.99–1.06 0.134
    History of heart failure 1.76 0.44–7.01 0.422
    Mechanical ventilation 4.23 1.44–12.44 0.009
    SOFA score 1.16 1.01–1.33 0.039
    NLAR 3.17 1.59–6.36 0.001
    Table 1. Baseline characteristics of the study population

    Values are presented as mean±standard deviation, number (%), or median (interquartile range).

    COPD: chronic obstructive pulmonary disease; CRRT: continuous renal replacement therapy; SBP: systolic blood pressure; DBP: diastolic blood pressure; MAP: mean arterial pressure; HR: heart rate; SOFA: Sequential Organ Failure Assessment; APACHE: Acute Physiology and Chronic Health Evaluation; SAPS: Simplified Acute Physiology Score; mNUTRIC: modified Nutrition Risk in the Critically Ill.

    Table 2. Laboratory features of the study population

    Values are presented as median (interquartile range).

    WBC: white blood cell; NLR: neutrophil-lymphocyte ratio; NLAR: neutrophil-to-lymphocyte-to-albumin ratio; RBC: red blood cell; HCT: hematocrit; AST: aspartate aminotransferase; ALT: alanine aminotransferase.

    Table 3. ROC analysis of NLR, NLAR, SOFA score, and APACHE II score as predictors for in-hospital mortality

    ROC: receiver operating characteristic; NLR: neutrophil-lymphocyte ratio; NLAR: neutrophil-to-lymphocyte-to-albumin ratio; SOFA: Sequential Organ Failure Assessment; APACHE: Acute Physiology and Chronic Health Evaluation; AUC: area under the curve.

    Table 4. Multivariable logistic regression of NLAR and in-hospital mortality

    NLAR: neutrophil-to-lymphocyte-to-albumin ratio; OR: odds ratio; SOFA: Sequential Organ Failure Assessment.

    Table 1.

    Table 2.

    Table 3.

    Table 4.

    ACC : Acute and Critical Care
    © The Korean Society of Critical Care Medicine.
    TOP