Abstract
-
Purpose
We evaluated the efficacy of the modified Nutrition Risk in Critically Ill (mNUTRIC) score for malnutrition screening and its association with mortality in intensive care unit (ICU) patients with COVID-19.
-
Methods
The nutritional status of 129 COVID-19 ICU patients admitted between February 2021 and May 2022 was assessed using American Society for Parenteral and Enteral Nutrition/Academy of Nutrition and Dietetics (ASPEN/AND) criteria. The sensitivity, specificity, and clinical correlations of the mNUTRIC score were analyzed.
-
Results
Of the 129 patients, 35 (27.1%) met the ASPEN/AND malnutrition criteria. Multivariable analysis identified the mNUTRIC score, underlying malignancy, and mechanical ventilation as significant factors associated with malnutrition. The mNUTRIC score had a sensitivity of 77.1% and specificity of 63.8% (area under the curve [AUC], 0.71; 95% confidence interval [CI], 0.62–0.79) for diagnosing malnutrition, improving to 88.6% and 80.9%, respectively, after adjusting for malignancy and ventilation (AUC, 0.89; 95% CI, 0.82–0.95). Patients with a low mNUTRIC score had a mortality rate of 2.9% and a median ICU stay of 7.7 days (range, 0–84.2 days), whereas those with a high score (≥5) had a mortality rate of 13.1% and a median ICU stay of 10.2 days (range, 1.4–88.5 days) (P=0.046 and P=0.011, respectively).
-
Conclusion
The mNUTRIC score is an effective screening tool for malnutrition in ICU patients with COVID-19, especially those with malignancy or requiring mechanical ventilation, and is strongly associated with mortality and length of ICU stay.
-
Keywords: COVID-19; Intensive care units; Malnutrition; Nutrition assessment
Introduction
Patients admitted to the intensive care unit (ICU) frequently experience a prolonged systemic inflammatory response due to various infections, often accompanied by sepsis or multiple organ failure. These patients require a range of treatments, including mechanical ventilation, sedatives, and neuromuscular blocking agents. Both their underlying condition and the extended duration of ICU treatment are recognized risk factors for developing malnutrition and sarcopenia [
1,
2]. Furthermore, the emergence of severe COVID-19 pneumonia has underscored the significance of nutritional support as a prognostic factor during the management of severe cases of COVID-19 [
3,
4].
Several studies have explored screening tools for adequate nutrition support [
5-
7]. However, many of these tools depend on information obtained from patient interviews, such as recent dietary changes and weight loss or gain. In actual clinical practice, particularly when admitting patients to the ICU with severe COVID-19 pneumonia, it is often challenging to gather this information reliably [
8]. Therefore, there is a pressing need for a faster and more practical tool to assess nutritional status.
The Nutrition Risk in Critically Ill (NUTRIC) score offers a rapid and straightforward method for screening malnutrition by evaluating patients at ICU admission. It incorporates variables such as age, Acute Physiology and Chronic Health Evaluation (APACHE) II score, Sequential Organ Failure Assessment (SOFA) score, and the presence of comorbidities. Although the original NUTRIC score requires measurement of interleukin-6 (IL-6), this is often impractical in routine ICU settings. As a result, the modified NUTRIC (mNUTRIC) score, which excludes IL-6, is now widely utilized [
9-
11].
This study aimed to investigate the clinical utility of the mNUTRIC score as a nutrition screening tool in critically ill patients with COVID-19 pneumonia, as well as its association with clinical outcomes.
Methods
Study design and participants
Between February 2021 and May 2022, all patients admitted to the ICU with COVID-19 pneumonia were included in the study. Patients who were discharged from the ICU within 48 hours, or who were admitted solely for isolation or close observation, were excluded.
Patients were managed in a negative-pressure ICU in accordance with institutional COVID-19 protocols. Treatment protocols included the use of remdesivir, corticosteroids, and prone positioning when indicated. Standard ICU equipment and care pathways were followed, encompassing sedation, mechanical ventilation, continuous renal replacement therapy, and extracorporeal membrane oxygenation (ECMO) as appropriate.
After ICU admission, the attending physician assessed each patient. If the patient was at high risk for malnutrition, such as those with difficulty maintaining an oral diet or with a prior history of hospitalization, they were referred to the nutrition support team (NST). The NST evaluated nutritional status according to the American Society for Parenteral and Enteral Nutrition/Academy of Nutrition and Dietetics (ASPEN/AND) criteria (
Supplement 1) [
2].
The mNUTRIC score was calculated based on the patient's age, the SOFA score within 24 hours of ICU admission, and the APACHE II score. The sensitivity and specificity of the mNUTRIC score were evaluated with respect to malnutrition status as determined by the ASPEN/AND criteria. Additionally, to analyze clinical outcomes in relation to the mNUTRIC score, patients were divided into two groups: a low mNUTRIC score group (score <5) and a high mNUTRIC score group (score ≥5). We then compared ICU mortality and length of ICU stay between these groups.
This study was approved by the Institutional Review Board of National Cancer Center (approval no. NCC 2022-0307). Due to its retrospective design, the requirement for informed consent was waived by the IRB.
Statistical analysis
Continuous variables are presented as mean±standard deviation for normally distributed data, and as median with interquartile range (IQR) for data not following a normal distribution. Categorical variables were compared using the chi-square test or the Fisher exact test, as appropriate. Continuous variables between two groups were analyzed using either the Student t test or the Mann-Whitney U test, depending on data normality.
To evaluate the diagnostic performance of the mNUTRIC score, receiver operating characteristic curve analysis was performed, and the area under the curve (AUC) was calculated. To assess whether the classification performance of the mNUTRIC score improved with adjustment, a logistic regression model including malignancy and mechanical ventilation (each as dichotomous variables) was constructed, and the AUC was recalculated based on the multivariable model.
Variables with a P-value <0.1 in univariable analysis or of recognized clinical relevance were included as candidates for multivariable logistic regression. Backward stepwise logistic regression was used for variable selection. Multicollinearity among the retained variables was assessed using variance inflation factors (VIFs), with variables showing a VIF >5 excluded from the final model. The Youden index was used to determine the optimal cutoff point for the mNUTRIC score in identifying malnutrition.
All statistical analyses were performed using R version 4.2.2 (R Foundation for Statistical Computing).
Results
Patient characteristics
Among the 129 patients included in the study, 35 (27.1%) were identified as malnourished according to the ASPEN/AND criteria. Comparison between groups revealed that the no-malnutrition group had a significantly higher body mass index (BMI; 25.0±4.2 kg/m
2 vs. 22.8±3.9 kg/m
2, P=0.006), while the malnutrition group showed a greater proportion of patients with underlying malignancy (51.4% vs. 24.5%, P=0.003). Additionally, at ICU admission, the malnutrition group had significantly higher APACHE II, SOFA, and mNUTRIC scores compared to the no-malnutrition group. Regarding ICU outcomes, the malnutrition group experienced a significantly longer ICU stay (13.0 days [IQR, 2.4–88.5] vs. 7.5 days [IQR 2.4–84.2], P<0.001) and a higher mortality rate (20.0% vs. 3.2%, P=0.004) (
Table 1).
Multivariable analysis of factors associated with malnutrition
Backward stepwise logistic regression removed age, BMI, albumin, and C-reactive protein from the model due to lack of statistical significance. VIF analysis of the remaining variables showed that APACHE II and SOFA scores had high multicollinearity with the mNUTRIC score and were therefore excluded. As a result, the final model included mNUTRIC score, underlying malignancy, and mechanical ventilation as independent predictors of malnutrition. Multivariable analysis identified the mNUTRIC score (odds ratio [OR], 3.88; 95% confidence interval [CI], 1.39–10.82; P=0.01), underlying malignancy (OR, 7.55; 95% CI, 2.21–25.77; P=0.001), and mechanical ventilation (OR, 16.43; 95% CI, 4.93–54.72; P<0.001) as statistically significant predictors (
Table 2).
Validation of the mNUTRIC score
The mNUTRIC score showed a sensitivity of 77.1% and a specificity of 63.8% for diagnosing malnutrition (AUC, 0.71) (
Fig. 1,
Supplement 2). When adjusted for the presence of malignancy and mechanical ventilation, sensitivity and specificity improved to 88.6% and 80.9%, respectively (AUC, 0.89; 95% CI, 0.82–0.95) (
Fig. 2).
Clinical outcomes associated with high and low mNUTRIC scores
Assessment of the association between mNUTRIC score and ICU outcomes demonstrated that patients with a low mNUTRIC score had a mortality rate of 2.9% and a median ICU stay of 7.7 days (range, 0–84.2 days). In contrast, those with a high mNUTRIC score (≥5) had a mortality rate of 13.1% and a median ICU stay of 10.2 days (range, 1.4–88.5 days); both differences were statistically significant (P=0.046 and P=0.011, respectively) (
Table 3). Youden index analysis confirmed that a score of 5 was the optimal cutoff value for predicting malnutrition using the mNUTRIC score.
Discussion
This study demonstrated the utility of the mNUTRIC score as a screening tool for malnutrition in ICU patients diagnosed with COVID-19, showing a significant association with clinical outcomes, including ICU length of stay and mortality. Notably, the diagnostic performance of the score was further improved when adjusting for malignancy and ventilator care variables. Previous studies evaluating the mNUTRIC score in ICU populations have reported comparable performance in nutritional assessment, and this study similarly affirms the value of the mNUTRIC score in this context [
11,
12].
Various nutritional assessment tools have been investigated for diagnosing malnutrition in critically ill patients. However, most widely used nutrition assessment tools in current practice require patient or caregiver interviews and depend on variables such as reduced food intake and weight loss [
4-
6]. Additionally, assessment methods such as the ASPEN/AND criteria and the Patient-Generated Subjective Global Assessment necessitate a physical examination to evaluate parameters including fat mass and muscle function [
2,
13]. In severe COVID-19 patients, conducting interviews or performing physical examinations is particularly challenging due to the need for infection control and the frequent use of sedatives during ventilator care or ECMO for acute respiratory distress syndrome caused by COVID-19 [
14,
15]. The mNUTRIC score provides a simple screening method for assessing nutritional status using fundamental patient data (such as age, pre-ICU admission duration, and comorbidities) along with measurements collected at admission, including the APACHE and SOFA scores. Thus, the use of mNUTRIC may help overcome limitations related to traditional patient assessments in the unique context of COVID-19, serving as a practical alternative for nutritional screening.
In this study, we observed improved diagnostic performance of the mNUTRIC score after adjusting for underlying cancer and variables related to ventilator therapy, indicating that both factors are closely associated with malnutrition. Prior studies have reported that malnutrition is common among critically ill cancer patients and is linked to prolonged mechanical ventilation and increased ICU mortality [
16,
17]. Nutritional risk has also been shown to correlate with the duration of mechanical ventilation and adverse outcomes in patients with hematological malignancies. It is well established that malignancy can lead to functional decline and cachexia, both of which are strongly associated with malnutrition [
18,
19]. Additionally, cancer-related treatments, including surgical interventions and anticancer therapies, are known contributors to malnutrition [
20]. Second, mechanical ventilator care not only leads to respiratory muscle weakness but also induces a bedridden state, contributing to sarcopenia [
21]. Furthermore, the administration of sedatives and neuromuscular blocking agents during ventilator care in COVID-19 patients is recognized as an additional risk factor for sarcopenia [
22].
This study has several limitations. It was conducted at a single institution with a relatively small cohort and was retrospective in design. Moreover, the mNUTRIC score does not include direct indicators of nutritional status, such as weight, muscle mass, or muscle function. Therefore, further research is warranted to explore the relationship between the mNUTRIC score and comprehensive measures of nutritional status.
In conclusion, among ICU patients with COVID-19 and underlying malignancy and/or requiring mechanical ventilation, the mNUTRIC score demonstrated clear utility as a malnutrition screening tool. The mNUTRIC score showed strong correlations with clinical outcomes, including ICU mortality and length of stay.
Authors’ contribution
Conceptualization: SSH. Data curation: WHH. Formal analysis: JHL. Investigation: JML, SSH. Supervision: SSH. Writing–original draft: WHH, JHL, SSH. Writing–review & editing: HML, JYK, MYJ, JML. All authors read and approved the final manuscript.
Conflict of interest
The authors of this manuscript have no conflicts of interest to disclose.
Funding
This work was supported by a grant (NCC 2310350-3) from the National Cancer Center, Republic of Korea.
Data availability
Contact the corresponding author for research data availability.
Acknowledgments
None.
Supplementary materials
Fig. 1.ROC curve for the mNUTRIC score. ROC, receiver operating characteristic; AUC, area under the ROC curve; mNUTRIC score, modified Nutrition Risk in Critically Ill score; CI, confidence interval; PPV, positive predictive value; NPV, negative predictive value.
Fig. 2.ROC curve for the mNUTRIC score when adjusted for malignancy and mechanical ventilation. ROC, receiver operating characteristic; AUC, area under the ROC curve; mNUTRIC score; modified Nutrition Risk in Critically Ill score; CI, confidence interval; PPV, positive predictive value; NPV, negative predictive value.
Table 1.
Variables |
No malnutrition (n=94) |
Malnutrition (n=35) |
P-value |
Sex |
|
|
|
Male |
52 (55.3) |
17 (48.6) |
0.494a
|
Female |
42 (44.7) |
18 (51.4) |
|
Age (yr) |
63.0±13.0 |
67.7±11.8 |
0.066b
|
BMI (kg/m2) |
25.0±4.2 |
22.8±3.9 |
0.006b
|
Underlying disease |
|
|
|
DM |
23 (24.5) |
14 (40.0) |
0.082a
|
HTN |
46 (48.9) |
20 (57.1) |
0.407a
|
COPD |
5 (5.3) |
1 (2.9) |
>0.999c
|
CVA |
12 (12.8) |
6 (17.1) |
0.571c
|
Malignancy |
23 (24.5) |
18 (51.4) |
0.003a
|
Nutrition route |
|
|
<0.001a
|
No nutritional support |
62 (66.0) |
2 (5.7) |
|
Enteral feeding |
12 (12.8) |
24 (68.6) |
|
Parenteral |
20 (21.3) |
9 (25.7) |
|
APACHE II |
25 (12–34) |
27 (13–50) |
0.006d
|
SOFA |
1 (0–7) |
2 (0–10) |
0.002d
|
mNUTRIC score |
4 (1–7) |
6 (3–8) |
<0.001d
|
Initial laboratory tests |
|
|
|
Albumin (g/dL) |
3.3±0.6 |
3.0±0.4 |
0.005b
|
CRP (mg/dL) |
8.2±6.0 |
11.8±7.7 |
0.008b
|
Ventilator care |
15 (16.0) |
24 (68.6) |
<0.001a
|
CRRT |
2 (2.1) |
8 (22.9) |
<0.001c
|
ECMO |
4 (4.3) |
4 (11.4) |
0.211c
|
ICU length of stay (day) |
7.5 (2.0–84.2) |
13.0 (2.4–88.5) |
<0.001d
|
Outcome |
|
|
0.004c
|
Survival |
91 (96.8) |
28 (80.0) |
|
Mortality |
3 (3.2) |
7 (20.0) |
|
Table 2.Multivariable analysis of factors associated with malnutrition
Variable |
Univariable analysis |
Multivariable analysis |
OR (95% CI) |
P-value |
OR (95% CI) |
P-value |
Sex |
Male |
Ref |
|
|
|
|
Female |
1.31 (0.60–2.85) |
0.495 |
|
|
Age |
|
1.03 (0.99–1.06) |
0.069 |
|
|
BMI |
|
0.87 (0.79–0.96) |
0.009 |
|
|
Underlying disease |
|
|
|
|
|
DM |
No |
Ref |
|
|
|
|
Yes |
2.05 (0.90–4.69) |
0.086 |
|
|
HTN |
No |
Ref |
|
|
|
|
Yes |
1.39 (0.63–3.04) |
0.408 |
|
|
COPD |
No |
Ref |
|
|
|
|
Yes |
0.52 (0.05–4.64) |
0.561 |
|
|
CVA |
No |
Ref |
|
|
|
|
Yes |
1.41 (0.48–4.11) |
0.525 |
|
|
Malignancy |
No |
Ref |
|
Ref |
|
|
Yes |
3.26 (1.45–7.36) |
0.004 |
7.55 (2.21–25.77) |
0.001 |
APACHE II |
|
1.13 (1.04–1.23) |
0.003 |
|
|
SOFA |
|
1.52 (1.19–1.94) |
0.001 |
|
|
mNUTRIC score |
Low |
Ref |
|
Ref |
|
|
High |
5.95 (2.43–14.56) |
<0.001 |
3.88 (1.39–10.82) |
0.010 |
Initial laboratory tests |
|
|
|
|
|
Albumin |
|
0.34 (0.14–0.86) |
0.023 |
|
|
CRP |
|
1.08 (1.01–1.14) |
0.010 |
|
|
Ventilator care |
No |
Ref |
|
Ref |
|
|
Yes |
11.48 (4.66–28.32) |
<0.001 |
16.43 (4.93–54.72) |
<0.001 |
CRRT |
No |
Ref |
|
|
|
|
Yes |
13.62 (2.73–68.00) |
0.002 |
|
|
ECMO |
No |
Ref |
|
|
|
|
Yes |
2.90 (0.68–12.31) |
0.148 |
|
|
ICU length of stay |
|
1.04 (1.01–1.07) |
0.004 |
Table 3.Clinical outcomes according to mNUTRIC scores
Variable |
Low mNUTRIC score (<5) |
High mNUTRIC score (≥5) |
P-value |
Mortality |
2 (2.9) |
8 (13.1) |
0.046a
|
ICU length of stay |
7.7 (0–84.2) |
10.2 (1.4–88.5) |
0.011b
|
Ventilator care |
12 (17.6) |
27 (44.3) |
0.001a
|
ECMO |
3 (4.4) |
5 (8.2) |
0.475c
|
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