The Nutritional Risk in the Critically Ill (NUTRIC) score was proposed by Heyland
et al. to identify critically ill patients who require aggressive nutritional therapy.[ ] It incorporated factors that could affect immune dysfunction and acute as well as chronic inflammation, such as age, Acute Physiology and Chronic Health Evaluation II (APACHE II) score, Sequential Organ Failure Assessment (SOFA) score, comorbidities, the number of days from hospital to intensive care unit (ICU) admission, and serum interleukin 6 (IL-6) levels.[ 1 ] In a recent systematic review, the NUTRIC score has been shown to predict adverse outcomes in critically ill patients and its utility in this specific population was proposed as an important research area.[ 1 ] The modified NUTRIC (mNUTRIC) without IL-6 has been shown to be as valuable as the NUTRIC score in implementing individualized nutritional support in patients at higher risk.[ 2 ] Acute febrile illness (AFI) patients with acute respiratory distress syndrome (ARDS), along with hepatic or renal involvement, have higher 3 mortality than a non-ARDS subset of AFI patients.[ ] However, among the all-cause ARDS patients, those with AFI-related ARDS have lesser 4 mortality than non-AFI ARDS.[ ] AFI is a fever that is acute in onset, undifferentiated, and lasts <2 weeks.[ 5 ] There are various studies on 6 mortality predictors of AFI such as advanced age, hyperbilirubinemia, acute kidney injury (AKI), ARDS, and platelets <20,000/mL.[ 5 7 8 ] However, literature is scarce regarding predictors of 9 mortality in AFI-ARDS patients specifically.
APACHE II score and SOFA score are predictors of
mortality in the critically ill, whereas the NUTRIC score was originally developed to identify patients who will reap maximum advantage from active nutritional therapy.[ 1 10 ] Rather than separate tools for 11 mortality prediction and the need for aggressive nutrition, if a single tool (like mNUTRIC) can predict both the outcome and need for aggressive nutrition in ARDS patients, its utility will be immense for clinicians.
The NUTRIC score originally developed by Heyland et al aimed to identify critically ill patients who are at higher nutritional risk and at a risk of adverse outcome and may be ameliorated by early aggressive nutritional therapy.[
] The variables in this score were based on a conceptual model that incorporated acute and chronic inflammation, acute and chronic nutritional status, and adverse clinical outcomes.[ 1 ] The score included five variables – age, APACHE II score, SOFA score, number of comorbidities, days from hospital to ICU admission, and inflammatory biomarker IL-6.[ 1 ] The authors had written that “We expected this model to explain additional 1 mortality risk, above and beyond what would be derived from the use of traditional measures of severity of illness (APACHE II score and baseline SOFA).”[ ] However, IL-6 may be unavailable across all settings, and without it, the mNUTRIC (designated as mNUTRIC) has been shown to predict adverse outcomes in critically ill patients, comparable to the original NUTRIC score.[ 1 ] Thus, we used the mNUTRIC score in ARDS patients to predict 3 mortality on admission to the ICU. Evaluation of the mNUTRIC score will serve two purposes at the same time: (a) it will identify patients who require early aggressive nutrition, and (b) it will identify patients who are at a higher risk of adverse outcomes in critically ill patients like ARDS. Aim
We aimed to study the utility of the mNUTRIC score at ICU admission as a predictor of
mortality in all-cause ARDS and AFI-ARDS. Objectives
The primary objective was to determine the utility of the mNUTRIC score at ICU admission as an independent predictor of
mortality in all-cause ARDS and AFI-ARDS patients, along with the cutoff mNUTRIC score to predict mortality.
The secondary objective was to compare the
mortality rates of ARDS between AFI-ARDS and non-AFI-ARDS. METHODS
We recruited 216 ARDS patients from two observational studies conducted at our tertiary care medical college hospital. Both the studies were permitted by the institutional ethics committee (IEC). The IEC permission for the first study was IEC 591/2019 with Clinical Trials Registry of India (CTRI) registration number CTRI/2019/11/021857, whereas the IEC permission for the second study was IEC 765/2019, with CTRI registration CTRI/2020/04/024940. The first study aimed to study the correlation of serum albumin and lung aeration as evidenced by lung ultrasound scores in ARDS patients with inclusion criteria being adult patients with ARDS definition as per Berlin’s criteria with age 18–70 years who were non-COVID-19 positive. The second study aimed to study the profile of driving pressure in ARDS with inclusion criteria being adult patients with ARDS definition as per Berlin’s criteria with age 18–80 years who were non-COVID-19 positive. No duplication of any patient data was there among the 216 patients. The study was conducted from November 2019 to April 2022 in ARDS patients admitted to ICU. Criteria for admission to ICU in our setup are if the patient fulfills any of the following – an increase in SOFA score ≥2 in 48 h of hospital admission, respiratory rate ≥40 or <9 breaths/min, oxygen saturation <90% on ≥50% oxygen, threatened airway, pulse rate <40 or >140/min, systolic blood pressure <90 mmHg, sudden drop in Glasgow Coma Score (GCS) >2 points, GCS <8, repeated seizures, and respiratory acidosis.[
For the present study, we retrieved data of age, gender, APACHE II score, SOFA score, primary diagnosis, diagnosis of AFI, comorbidities, the ratio of partial pressure of arterial blood to the fraction of inspired oxygen (PaO
2/FiO 2), days from hospital to ICU admission, mNUTRIC score on the day of admission to ICU, length of ICU stay (days), and mortality outcome. The mNUTRIC score was assessed for each patient on the day of admission to ICU (minimum of 0 to a maximum of 9 points).[ ] The detailed scoring was – (a) age: <50, 50–<75, and ≥75 years were scored 0, 1, and 2 points, respectively; (b) APACHE II score: <15, 15–20, 20–28, and ≥28 were scored 0, 1, 2, and 3 points, respectively; (c) SOFA score: <6, 6–≤10, and ≥10 were scored 0, 1, and 2 points, respectively; (d) number of comorbidities: 0–1 and ≥2 were scored 0 and 1 point, respectively; and (e) days of hospital to ICU admission: 0–<1 and >1 day were scored 0 and 1 point, respectively.[ 1 ] This score was calculated excluding the IL-6. The total mNUTRIC score was calculated by adding all the components. The minimum and maximum mNUTRIC score is 0 to 10. 1
As per the guidelines of the American Society for Parenteral and Enteral Nutrition 2016, we provide enteral nutrition to all patients of ARDS in the ICU. The total energy (calories) provided is 20–25 kcal/kg/day, with a protein intake of about 1.2–1.5 g/kg/day.[
] We begin enteral nutrition within 24 h following ICU admission in patients with ARDS as per the 2016 guidelines. These were followed when the study was being conducted. 13
The number of AFI-ARDS cases was noted from the records. The AFI-related etiology caused AFI ARDS. All-cause ARDS in our study refers to the ARDS caused by all etiologies of ARDS (pulmonary or extrapulmonary, AFI related, or non-AFI related). In the AFI-ARDS patients, serum creatinine, bilirubin, and platelet count on the day of ICU admission were noted. PaO
2/FiO 2 < 100 was considered severe ARDS as per the Berlin definition.[ ] 14 Statistical analysis
Statistical analysis was done using software IBM Statistical Package for the Social Sciences (SPSS) Statistics Software version 188.8.131.52 (15) (IBM Corp. Armonk, NY, USA: IBM). Descriptive statistics of the continuous variables following parametric distribution were expressed as mean and standard deviation, and those following nonparametric distribution were expressed as the median and interquartile range. For the comparison of means of continuous variables in two groups with parametric distribution, the independent Student’s
t-test was used. Mann–Whitney U-test was used in the comparison of medians of the two groups. Pearson’s Chi-square test was used for the comparison of categorical variables between two groups. Univariate Cox regression analysis of the variables was done to predict mortality in the all-cause ARDS patients ( n = 216) and AFI-ARDS patients ( n = 73). 95% confidence interval (CI) was calculated, and P < 0.05 was taken as significant. P ≤ 0.05 was taken to limit the Type I error at 5%, above which the null hypothesis was accepted. For the multivariable Cox regression analysis for mortality prediction in all-cause ARDS patients ( n = 216), the variables with a significant P value in univariate analysis were taken. However, the variables such as age, APACHE II score, and SOFA score, which are included in the mNUTRIC score, were not taken as separate variables in the multivariable regression to avoid the concept of collinearity. For the multivariable Cox regression analysis of factors predicting mortality in the AFI-ARDS group, predefined variables such as severe thrombocytopenia (platelet count <50,000/mL), raised serum bilirubin ≥2 mg/dL, and AKI with serum creatinine level ≥2 mg/dL were taken irrespective of their P values in the univariate Cox regression analysis to predict mortality. This was because it was shown in the literature that severe thrombocytopenia (platelet count <50,000/mL), serum bilirubin ≥2 mg/dL, and AKI with serum creatinine level ≥2 mg/dL were significant predictors of mortality in AFI patients.[ 9 15 ] The mNUTRIC score was taken in the multivariable Cox regression analysis, as it was found to be a significant factor in predicting 16 mortality in the univariate analysis. Bootstrap analysis of the variables which were included in the multivariable Cox regression analysis in all-cause ARDS patients ( n = 216) to predict mortality was done. Bootstrap analysis was done using simple sampling with the enter method, using the biased corrected accelerated method. The receiver operating characteristic (ROC) curve was plotted to determine the area under the curve (AUC) of the continuous variables found significant in univariate analysis to predict mortality in all-cause ARDS and AFI-ARDS groups, and sensitivity, specificity, P value, optimal cutoff value as per our ROC, and 95% CI were calculated. Kaplan–Meier survival plot and log-rank P value were calculated for mNUTRIC score above and below the cutoff value ≥4 for the survival analysis in the AFI-ARDS patients ( n = 73). RESULTS
A total of 216 ARDS patients were included in the study. The AFI-ARDS patients were 73 (33.8%), and the non-AFI ARDS patients were 143 (66.2%). The etiology of AFI were due to leptospirosis 35, dengue 10, scrub typhus 14, rickettsial fever 4, and no specifical cause was identified in 10 cases. The demographic and characteristics of the 216 patients are depicted [
Table 1]. There was a significant difference in mortality between the AFI-ARDS (16/73) and non-AFI-ARDS (62/143) groups (21.9% vs. 43.34%, P = 0.002, Pearson’s Chi-square test). The number of severe ARDS in the AFI-ARDS (13/73) and non-AFI ARDS patients (31/143) was comparable (17.8% vs. 21.7%, P = 0.504, Pearson’s Chi-square test). Among the 216 all-cause ARDS patients, there was a significant difference between the APACHE II score, SOFA score, mNUTRIC score, and length of ICU stay between the survival and mortality groups [ Table 2]. Univariate Cox regression analysis of all-cause ARDS patients to predict mortality showed that APACHE II score, SOFA score, mNUTRIC score, AFI-ARDS, and severe ARDS were predictors of mortality [ Table 3]. Multivariable Cox regression analysis of all-cause ARDS patients to predict mortality showed that only the mNUTRIC score was an independent predictor of mortality ( P < 0.001, hazard ratio [HR]: 1.485, 95% CI [1.290–1.711]) [ Table 4]. Among the continuous variables to predict mortality, mNUTRIC had the highest AUC in the ROC curve (AUC: 0.778, 95% CI [0.714–0.842], P < 0.001, cutoff score ≥4, sensitivity 82.1%, specificity 65.9%) [ Figure 1]. The AUC of the APACHE II score and SOFA score was lesser than the AUC of the mNUTRIC score to predict mortality (0.774 and 0.730, respectively). Table 1:
Demographic and other characteristics of all-cause acute respiratory distress syndrome patients (
n=216) Table 2:
Difference in characteristics between the
mortality and survival groups in all-cause acute respiratory distress syndrome patients ( n=216) Table 3:
Univariate Cox regression analysis for predicting
mortality in all-cause acute respiratory distress syndrome ( n=216) Table 4:
Multivariable Cox regression analysis for predicting
mortality in all-cause acute respiratory distress syndrome ( n=216) Figure 1:
The AUC of mNUTRIC score is the highest as compared to the APACHE II score and SOFA score to predict
mortality in all-cause ARDS patients ( n = 216). ROC: Receiver operating characteristic curve, APACHE II: Acute Physiology and Chronic Health Evaluation II, SOFA: Sequential Organ Failure Assessment, mNUTRIC: Modified Nutritional Risk in the Critically ill
A separate analysis of the AFI-ARDS patients (
n = 73) was done. The characteristics and demographics of the AFI-ARDS patients are depicted [ Table 5]. Among AFI-ARDS patients, the APACHE II score, SOFA score, mNUTRIC score, and serum creatinine were significantly different between the survival and mortality groups, whereas the age, platelet count, bilirubin level, and severity of ARDS were not statistically different between the survival and mortality groups [ Table 6]. Univariate Cox regression analysis of AFI-ARDS patients ( n = 73) to predict mortality showed that the APACHE II score, SOFA score, and mNUTRIC score were significant [ Table 7]. Multivariable Cox regression analysis to predict mortality in AFI-ARDS patients showed that the mNUTRIC was an independent predictor of mortality ( P = 0.01, HR: 1.529, 95% CI [1.109–2.107]) [ Table 8]. With each point increase in mNUTRIC score, the odds of mortality rose by 1.529 times in the AFI-ARDS patients [ Table 8]. The ROC curve was plotted to predict mortality in the AFI-ARDS group, and the AUC of the mNUTRIC score was the highest (0.769, cutoff score: 4, P = 0.001, 95% CI: 0.630–0.908, 81.3% sensitivity, 66.67% specificity) as compared to APACHE II and SOFA scores (0.760 for both) [ Figure 2]. Bootstrap analysis of the variables which were included in the multivariable Cox regression analysis to predict mortality in all-cause ARDS patients ( n = 216) showed that only the mNUTRIC score was significant in predicting mortality ( P < 0.001, 95% CI [0.265–0.536]) [ Table 9]. The Kaplan–Meier survival curves of AFI-ARDS patients with mNUTRIC cutoff score 4, which we obtained from the AUC of our study, showed a significant difference (log-rank test P < 0.001) [ Figure 3]. The Cox proportional regression showed that HR of mortality in AFI-ARDS patients with mNUTRIC ≥4 is 6.193, P = 0.004, 95% CI (1.763–21.757). Table 5:
Characteristics and demographics of patients with acute febrile illness-acute respiratory distress syndrome (
n=73) Table 6:
Analysis of the factors in
mortality and survival groups in acute febrile illness-acute respiratory distress syndrome patients ( n=73) Table 7:
Univariate Cox regression analysis for predicting
mortality in acute febrile illness-acute respiratory distress syndrome category Table 8:
Multivariable Cox regression analysis for predicting
mortality in acute febrile illness-acute respiratory distress syndrome category Table 9:
Bootstrap analysis of the variables which were included in the multivariable Cox regression analysis in all-cause acute respiratory distress syndrome patients (
n=216) to predict mortality Figure 2:
The ROC curve showing the highest AUC of mNUTRIC score 0.769 to predict
mortality in AFI-ARDS patients, cutoff ≥4. ROC: Receiver operating characteristic curve, AUC: Area under the curve, mNUTRIC: Modified Nutritional Risk in the Critically Ill, AFI-ARDS: Acute febrile illness-Acute respiratory distress syndrome Figure 3:
The Kaplan–Meier survival curves of AFI-ARDS patients with mNUTRIC cutoff score <4 and mNUTRIC score ≥4 were different, with Log-rank (Mantel-Cox)
P < 0.001. AFI-ARDS: Acute febrile illness-Acute respiratory distress syndrome, mNUTRIC: Modified Nutritional Risk in the Critically ill DISCUSSION
AFI is an important cause of ICU admission and ARDS in India.[
] AFI is a fever that is acute in onset, undifferentiated, and <2 weeks in duration.[ 6 ] Literature reveals 6 mortality of about 23%–25% for AFI-ARDS patients, as against a mortality rate of about 44% for all-cause ARDS.[ 5 ] We also found a significantly lower 6 mortality rate of about 22% in AFI-ARDS compared to 43.34% in non-AFI ARDS, even though the proportion of patients with severe ARDS was comparable between the AFI-ARDS and non-AFI ARDS groups.
ARDS has two subphenotypes, each having different clinical and biological features and different responses to treatment.[
] Type 1 phenotype has lesser inflammation, shock, and 17 mortality, whereas Type 2 is hyperinflammatory with higher mortality, even though no particular clinical factor or biological variable can identify the phenotypes of ARDS.[ ] It has been postulated that leptospirosis/AFI-induced ARDS may be associated with phenotype 2 as it has lesser IL-8 levels.[ 17 ] The severity of ARDS and renal or liver dysfunction cannot differentiate the phenotypes of ARDS.[ 17 ] 17
With this background, we evaluated the utility of the mNUTRIC score in predicting
mortality in all-cause ARDS and AFI-ARDS, which are associated with lesser mortality rates. Since the NUTRIC score was based on an analysis model of acute and chronic inflammation, acute and chronic starvation, nutritional status, and clinical outcomes in terms of mortality, the authors expected that the NUTRIC model would predict mortality risk better than APACHE II and SOFA.[ ] 1
In our study, the mNUTRIC was a better tool to predict
mortality in both all-cause ARDS and AFI-ARDS groups, as compared to the APACHE II score and SOFA score, as evidenced by the higher AUC of the ROC plots to predict mortality. Since the mNUTRIC has been shown to be as useful as NUTRIC (IL-6 being unavailable in many resource-limited settings), we used the mNUTRIC to predict mortality in both all-cause and AFI-ARDS.[ ] However, in the study done on mNUTRIC in sepsis patients by Jeong 3 et al., the authors proposed a cutoff score of ≥6 to predict poor outcomes.[ ] We found a lesser cutoff of mNUTRIC of ≥4 in both all-cause ARDS and AFI-ARDS patients to predict 3 mortality. Our cutoff value of mNUTRIC was also lesser than that found by Mukhopadhyay et al. (cutoff score ≥5) in their study on critically ill to predict mortality.[ ] This could be because all our patients were not just with sepsis but also had ARDS, and thus, even a lesser cutoff value of mNUTRIC ≥4 as compared to the abovementioned studies increased their risk of 18 mortality.
In a study on scrub typhus, age and creatinine were found to be predictors of
mortality.[ ] We found that serum creatinine was significantly different in survival and 9 mortality groups in the AFI-ARDS patients. However, after the regression analysis, only the mNUTRIC score was found to predict mortality independently. Regression analysis in our study found that serum creatinine, severe thrombocytopenia (platelet count <50,000/μL, hyperbilirubinemia could not predict mortality. Our results differed from those of Zhai et al. and Adhikari et al where serum bilirubin level ≥2 mg/dL and creatinine >1.4 mg/dL on ICU admission was associated with mortality in AFI-ARDS.[ 9 ] 19
However, the reduced
mortality rate in AFI-ARDS, as we found in our study, was similar to that of previous studies in AFI-ARDS.[ 5 ] The reduced 6 mortality in AFI-ARDS could be because of efficacious treatment like doxycycline or azithromycin in AFI; it could have led to the resolution of ARDS in the AFI cases of leptospirosis and scrub typhus.[ ] 20
The odds of
mortality increased by 1.4 times with each point increase in the mNUTRIC score in critically ill patients in the study by Rahman et al.[ ] Our results were similar, and we found that each point increase in mNUTRIC score in AFI-ARDS patients increased the odds of 21 mortality by 1.53 times. Various other utilities of NUTRIC score have been performed in literature, and NUTRIC score helps predict not only high nutritional risk and mortality but also the length of mechanical ventilation, pulmonary complications, and the length of hospital stay. However, to our knowledge, this is the first study on the utility of the mNUTRIC score to predict adverse outcomes in AFI-ARDS patients.
mortality predictors in the all-cause ARDS patients, studies have found different factors or indices, such as oxygenation index on day 3 of ICU by Balzer et al., the plateau airway pressure score by Villar et al., and driving pressure by Amato et al.[ 22 23 ] For 24 mortality prediction, the concern with the utility of these scores/indices is that in ARDS patients, clinicians have to deeply sedate the patients and then perform ventilator maneuvers to calculate all these scores. Thus, if a single score like mNUTRIC, which is commonly calculated, could predict multiple outcomes such as the need for aggressive nutrition and mortality in AFI-ARDS patients, it would be less labor intensive and more clinically feasible.
The significant finding in our study is that the mNUTRIC score with a cutoff of ≥4 has a higher HR for
mortality in AFI-ARDS than all-cause ARDS. The same mNUTRIC score may have a different cutoff for various clinical conditions to predict outcomes, like ≥5 for nutritional risk in mechanically ventilated patients or ≥4, as we found to predict mortality in AFI-ARDS and all-cause ARDS.[ ] 25
Our study had specific strengths. With 216 ARDS patients, we analyzed factors predicting
mortality in AFI-ARDS and all-cause ARDS separately, along with univariate Cox regression and multivariable Cox regression analysis to ascertain independent predictors of mortality. Thus, by performing the univariate and multivariable Cox regression analysis for mortality, the significance of “time” in the time to event ( mortality) was also considered. We have analyzed the mortality predictors of AFI-ARDS patients, which are unique in our tropical regions. We used a helpful score like the mNUTRIC score to predict mortality, which is also a part of the standard of care to predict patients who may require early vigorous nutritional therapy. We have used the cutoff mNUTRIC score to plot Kaplan–Meier survival analysis and could show that the survival outcomes were significantly different in those with mNUTRIC scores, <4 and ≥4. However, the limitation was that it was a single-center study. Factors such as days of antibiotic therapy, liver enzyme levels, and the presence of multi-drug resistant infection were not incorporated. CONCLUSION
The mNUTRIC score is an independent predictor of
mortality in all-cause ARDS and AFI-ARDS patients. In AFI-ARDS patients, with each point increase in the mNUTRIC score, the odds of mortality rose by 1.53 times. In both the groups, all-cause ARDS patients and AFI-ARDS patients, the mNUTRIC score (cutoff ≥ 4) at ICU admission is a better tool than the APACHE II score and SOFA score to predict mortality. Research quality and ethics statement
The data were recorded from two prospective observational ARDS studies conducted at a single-center tertiary care hospital. The IEC permission for the first study was IEC 591/2019 with CTRI registration number CTRI/2019/11/021857, whereas the IEC permission for the second study was IEC 765/2019, with CTRI registration CTRI/2020/04/024940. The investigators of both studies are authors of this study. The authors followed applicable EQUATOR Network (
) guidelines during this research project. http://www.equator-network.org/ Declaration
We also certify that none of the authors is a member of the Editorial Board of the
Journal of Emergencies, Trauma, and Shock. Financial support and sponsorship
The authors Ms. Pratibha Todur (Principal Investigator), Dr. N. Anitha (Co-Principal investigator), and Dr. Souvik Chaudhuri (Co-Investigator) thank the Indian Council for Medical Research (ICMR), Ministry of Health and Family Welfare, Government of India, for the extramural
ad hoc grant. (IRIS/Proposal No. 2020 1322, No. 5/8-4/13/Env/2020-NCD-II) for the financial support. Conflicts of interest
There are no conflicts of interest.
The authors thank the dedicated health-care professionals and staff who provide care for critically ill patients in the unit where the study was conducted.
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