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 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 35  |  Issue : 3  |  Page : 1280-1287

Study of serum albumin level in critically ill children admitted to ICUs


1 Department of Pediatrics, Faculty of Medicine, Menoufia University, Menoufia, Egypt
2 Department of Pediatrics, Faculty of Medicine, Alexandria University, Alexandria, Egypt
3 Department of Clinical Pathology, Faculty of Medicine, Menoufia University, Menoufia, Egypt

Date of Submission26-Mar-2022
Date of Decision04-Jun-2022
Date of Acceptance05-Jun-2022
Date of Web Publication29-Oct-2022

Correspondence Address:
Dina M M. Ali
Alexandria government, El Soyof
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/mmj.mmj_100_22

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  Abstract 


Objectives
The aim of the current study was to study serum albumin level in critically ill children admitted to the pediatric ICU in Menoufia University hospital and its relation to the outcome.
Background
Hypoalbuminemia is a common feature in critically ill children in pediatric ICUs and is associated with a poor outcome.
Patients and methods
A cross-sectional study was conducted on 118 critically ill children from January 2021 to December 2021. All patients in the present study were subjected to detailed history, physical examination, and laboratory investigations. Pediatric Sequential Organ Failure Assessment (PSOFA), Pediatric Risk of Mortality III (PRISM III), and neutrophil percentage-to-albumin ratio (NPAR) scores were measured in the first 24 h of admission.
Results
Within the first 24 h of admission, 72 (61%) cases had hypoalbuminemia while during pediatric ICU admission, 84 (71.2%) cases had hypoalbuminemia. Hypoalbuminemia at admission was associated with significant higher PSOFA and NPAR scores, lower Glasgow coma scale, lower platelets count, lower Na level, and higher C-reactive protein levels while during pediatric ICU admission it was associated with significant worse final outcome, lower platelets count, lower Na level, higher PSOFA, NPAR, and PRISM III scores in comparison to the non-hypoalbuminemia group. According to the receiver operating characteristic curve study of scoring systems to predict mortality, PSOFA and NPAR scores were significantly high in the studied groups at admission while PSOFA, PRISM III, and NPAR scores were significantly high in the studied groups during pediatric ICU admission.
Conclusion
Hypoalbuminemia is an independent predictor of pediatric ICU mortality.

Keywords: critical illness, hypoalbuminemia, ICUs, poor outcome


How to cite this article:
Tawfik MA, Ali DM, Aboelkhair NT, Zouna ZS. Study of serum albumin level in critically ill children admitted to ICUs. Menoufia Med J 2022;35:1280-7

How to cite this URL:
Tawfik MA, Ali DM, Aboelkhair NT, Zouna ZS. Study of serum albumin level in critically ill children admitted to ICUs. Menoufia Med J [serial online] 2022 [cited 2024 Mar 29];35:1280-7. Available from: http://www.mmj.eg.net/text.asp?2022/35/3/1280/359642




  Introduction Top


According to the WHO definition critical illnesses are any severe problem with the airway, breathing or circulation, or acute deterioration of conscious state, which includes apnea, upper airway obstruction, hypoxemia, central cyanosis, severe respiratory distress, total inability to feed, shock, severe dehydration, active bleeding requiring transfusion, and unconsciousness or seizure[1].

Albumin, the major serum protein, has multiple important physiological functions including maintenance of colloidal osmotic pressure, binding of a wide variety of compounds, and provision of the bulk of plasma antioxidant activity[2].

The etiology of hypoalbuminemia is complex. In general, it is ascribed to diminished synthesis in malnutrition, malabsorption, and hepatic dysfunction or increased losses in nephropathy or protein-losing enteropathy[3].

In critically ill children the inflammatory process decreases the synthesis of albumin and increases its breakdown. Diversion of synthetic capacity to other acute-phase reactant proteins is another cause of hypoalbuminemia in critical illnesses; also, capillary permeability increases dramatically and alters albumin exchange between intravascular and extravascular spaces[4].

Hypoalbuminemia defined as an albumin level of less than 3.5 g/dl for patients 7 months or older and less than 2.5 g/dl for patients younger than 7 months[5].

The aim of the present study was to assess the serum albumin level in critically ill children admitted to the ICU and its relation to outcome.


  Patients and methods Top


The present study was a cross-sectional study conducted on 118 cases; their ages ranged from 1 to 12 years with a mean age of 2.40 ± 2.17 years, 63 (53.4%) males and 55 (46.4%) females, diagnosed as critically ill according to the WHO guidelines whatever the initial diagnosis at the time of admission to the pediatric ICU in Menoufia University hospital from January 2021 to December 2021. The study protocol was approved by the Menoufia Faculty of Medicine Committee for Medical Research Ethics; also informative consents were taken from all guardians of patients.

Patients in the present study were divided regarding serum albumin level measured by the dye-binding method within the first 24 h and the mean values of the measured serum albumin level every 3 days during admission to pediatric ICU into two groups: non-hypoalbuminemia group in which serum albumin level more than or equal to 3.5 g/dl and hypoalbuminemia group in which serum albumin level less than 3.5 g/dl. Patients of both sexes, aged from 1 to 12 years and diagnosed critically ill according to WHO guidelines whatever the initial diagnosis at the time of admission were included in the present study. While patients who had severe protein-energy malnutrition (weight-for-height-3 SD), chronic liver disease, chronic kidney disease, chronic gastrointestinal disease, second or third-degree burns, patients who received blood products or albumin before measuring the albumin level or parenteral nutrition before pediatric ICU admission, and patients die in the first 24 h of admission to pediatric ICU were excluded from our study. All patients in the present study were subjected to detailed history and clinical examination.

All laboratory investigations had been measured within the first 24 h of admission and remeasured during the period of admission to the pediatric ICU, includes complete blood count, C-reactive protein (CRP) test (mg/l), serum electrolytes (serum sodium level in mmol/l – serum potassium level in mmol/l – total serum calcium level in mg/dl), kidney functions (mg/dl), blood gas analysis and random blood glucose level (mg/dl) at the time of admission to the pediatric ICU. Radiologic investigation when needed according to the initial presenting diagnosis to the pediatric ICU.

The used scoring systems in this study were the Pediatric Sequential Organ Failure Assessment (PSOFA score), Pediatric Risk of Mortality Score (PRISM III), and neutrophil percentage-to-albumin ratio (NPAR), and all of them were measured during the first 24 h of admission to pediatric ICU.

Statistical analysis of the data

Data were fed to the computer and analyzed using IBM SPSS software package, version 20.0. (IBM Corp., Armonk, New York, USA). Qualitative data were described using number and percent. Quantitative data were described using range (minimum and maximum), mean, and SD. Significance of the obtained results was judged at the 5% level.

The used tests were χ2 test, Monte Carlo correction, Student's t test, Mann–Whitney test, receiver-operating characteristic (ROC) curve, sensitivity, specificity, positive predictive value, and negative predictive value.


  Results Top


Most cases were male (53.4%) with a mean age of 2.40 ± 2.17 years. According to provisional diagnosis at the time of admission the most common cause was respiratory diseases (60 cases, 50.8%). The mean duration of admission was 8.25 ± 4.16 days. According to the final outcome most cases were improved and discharged (99 cases, 83.8%). Hypoalbuminemia was observed in 72 (61%) cases within 24 h of admission with a mean serum albumin of 3.33 ± 0.56 g/dl, while the mean of serum albumin level during pediatric ICU admission was 3.29 ± 0.58 g/dl. As regards the Glasgow coma scale (GCS) measured at the time of admission to the pediatric ICU the mean was 12.99 ± 2.13 ranging from 7.0 to 15.0 and it was of statistical significance in this study as P value of 0.034. As regards scoring systems, the mean PSOFA was 4.27 ± 3.13, PRISM III 15.82 ± 3.75, and NPAR 19.36 ± 9.43 [Table 1].
Table 1: Demographic and clinical data of all studied cases

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As regards correlation between serum albumin level within 24 h of admission and other collected data GCS, platelets, serum Na, and CRP showed significant difference in the hypoalbuminemia group when compared with the non-hypoalbuminemia group (P = 0.034, 0.017, 0.003, and 0.019, respectively). However, PSOFA and NPAR scores showed significant increase in the hypoalbuminemia group when compared with the non-hypoalbuminemia group (P = 0.011 and 0.003, respectively). Sex, age, provisional diagnosis at admission, duration of admission, final outcome, and PRISM III score did not show significant difference between hypoalbuminemia and non-hypoalbuminemia groups (P > 0.05) [Table 2].
Table 2: Correlation between serum albumin level within 24 h of admission and other collected data

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As regards correlation between mean values of serum albumin level during pediatric ICU admission and other collected data, final outcome, platelets, serum Na, PSOFA, PRISM III, and NPAR showed significant difference in the hypoalbuminemia group when compared with the non-hypoalbuminemia group (P = 0.001, P = 0.038, P < 0.001, P = 0.001, P < 0.001, P = 0.003, respectively). Sex, age, and duration of admission did not show significant difference between hypoalbuminemia and non-hypoalbuminemia groups (P > 0.05) [Table 3].
Table 3: Correlation between mean values of serum albumin during pediatric ICU admission and other collected data

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As regards scoring systems' validity to predict mortality in the studied groups at 24 h of pediatric ICU admission, the PSOFA score best detected cutoff point is more than or equal to 3 with a sensitivity of 61.11%, specificity of 60.78%, and area under the ROC curve (AUC) of 0.638 [95% confidence intervals (CI): 0.537–0.739] (P ≤ 0.012). The NPAR score best detected cutoff point is more than or equal to 18.2 with a sensitivity of 65.50%, specificity of 65.22%, and an AUC of 0.665 (95% CI: 0.567–0.762) (P ≤ 0.003) [Figure 1].
Figure 1: ROC curve study of scoring systems of the studied groups at 24 h of pediatric ICU admission. ROC, receiver-operating characteristic.

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As regards scoring systems' validity to predict mortality in the studied groups during the pediatric ICU admission, the PSOFA score best detected cutoff point is more than or equal to 3 with a sensitivity of 60.71%, specificity of 67.65%, and an AUC of 0.687 (95% CI: 0.589–0.784) (P ≤ 0.002). The PRISM III score best detected cutoff point is more than or equal to 15 with a sensitivity of 69.05%, specificity of 61.76%, and an AUC of 0.705 (95% CI: 0.605–0.805) (P ≤ 0.001). The NPAR score best detected cutoff point is more than or equal to 16.8 with a sensitivity of 70.24%, specificity of 61.76%, and an AUC of 0.676 (95% CI: 0.576–0.776) (P ≤ 0.003) [Figure 2].
Figure 2: ROC curve of scoring systems of the studied groups during pediatric ICU admission. ROC, receiver-operating characteristic.

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  Discussion Top


There is a close relation between critical illness and hypoalbuminemia as critical illness alters the distribution of albumin between intravascular and extravascular compartments, affects the rate of albumin synthesis, and increases albumin clearance and degradation; also it increases capillary leakage and these occur as a result of various factors including the effects of cytokines, prostaglandins, and endotoxins from Gram-negative bacteria[2].

Hypoalbuminemia in adult patients is a marker of disease severity and has been associated with prolonged ventilatory dependence and length of intensive care stay. It is also an independent predictor of mortality, and it is associated with poor outcome in critically ill adults[4].

There is a paucity of data evaluating serum albumin levels and outcome of critically ill children admitted to the ICU. Therefore, the aim of the present study was to study serum albumin level in critically ill children admitted to the ICU and its relation to the outcome.

The present study was conducted on 118 cases diagnosed to have critical illness according to WHO guidelines. The studied groups were matched in demographic data. There was no statistically significant difference in vital signs, blood gases, and kidney function among the studied groups. Therefore, there was no systemic illness affecting the scope of the study in the studied cases. As regards the distribution of the studied cases according to serum albumin within 24 h of admission hypoalbuminemia was observed in 72 (61%) cases, while 46 (39%) cases were non-hypoalbuminemic.

This incidence was nearly similar to Durward et al.[6] who found that the incidence of hypoalbuminemia at the time of admission was 57%, increasing to 76% at 24 h, and Leite et al.[7] found that admission hypoalbuminemia was present in 64.2% of patients. Also, Moustafa et al.[8] found that hypoalbuminemia was present at admission in 40.66% patients. Horowitz and Tai[9] found the incidence of hypoalbuminemia to be 33% at admission to the pediatric ICU.

Difference in the incidence of hypoalbuminemia between our study and previous studies may be explained by the difference in the definition of hypoalbuminemia. Tiwari and colleagues defined hypoalbuminemia as a serum albumin level lower than 2.5 g/dl while Durward and colleagues defined it as lower than 3.3 g/dl.

In our study, hypoalbuminemia was defined as a serum albumin level lower than 3.5 g/dl. Thus, a clear definition of hypoalbuminemia in pediatric patients should be made in order to give greater weightage to all these studies.

In the present study, the mean albumin level was 3.33 ± 0.56 g/dl ranging from 1.90 to 5.90 g/dl at admission. This was comparable to Bhandarkar et al.[10] who found that the median levels of serum albumin at pediatric ICU admission was 3.30 g/dl.

Distribution of the studied cases according to mean values of serum albumin during pediatric ICU admission (n = 118): hypoalbuminemia was observed in 84 (71.2%) cases while 34 (28.8%) cases were non-hypoalbuminemiac. There was a higher percentage of hypoalbuminemia group during pediatric ICU admission than at admission. This was comparable to a study by Tiwari et al.[11], who found that hypoalbuminemia was present on admission in 21% patients that increased to 34% at the end of first week and to 37% during rest of the stay in the pediatric ICU.

Mean albumin level was 3.29 ± 0.58 g/dl ranging from 1.50 to 5.50 g/dl during pediatric ICU admission. This was comparable to a study by Kumar et al.[12], who found that the mean serum albumin level was 3.38 ± 0.89 g/dl.

The present study showed that no significant difference was found between the studied groups and provisional diagnosis at admission as regards respiratory, neurology, gastrointestinal, and sepsis. In agreement with our results, Golhar et al.[13] found that there was no significant difference in systems affected between the two studied groups. Contrary to our results, Kumar et al.[12] found that the incidence of hypoalbuminemia was more common in children with infectious disease and sepsis.

The present study showed that no significant difference was found between the two studied groups according to anthropometric measures and duration of admission. In agreement with our results, Yanni et al.[14] studied critically ill children admitted to the pediatric ICU and found that mean age, weight, nutritional status, and type of cases (surgical or nonsurgical) did not show significant differences between the two groups. Also, albumin levels do not affect the length of stay. Also, Kim et al.[15] found no statistically significant difference in ge, sex, nutritional status, length of ICU stay, and the main reason for ICU admission between the two groups. Contrary to our results, Tiwari et al.[11] found that hypoalbuminemic patients had prolonged pediatric ICU stay. Also, Golhar et al.[13] found that the mean length of pediatric ICU stay in the hypoalbuminemia group was statistically longer than in the control (normal albumin) group.

Moreover, we found a significant difference between the two studied groups during pediatric ICU admission according to the final outcome. In agreement with our results, Golhar et al.[13] found that there was a significant difference in outcome between the hypoalbuminemia and normal albumin groups.

As regards complete blood count, only platelet count showed a significant decrease in the hypoalbuminemia group when compared with the non-hypoalbuminemia group. In agreement with our results, Kim et al.[16] found that children with hypoalbuminemia had lower platelet levels compared with children with normal albumin levels.

In the current study, serum Na showed a significant decrease in the hypoalbuminemia group when compared with the non-hypoalbuminemia group while serum potassium and serum calcium did not show significant difference between the two groups.

Contrary to our results, Gaafar and Sakar[17] comparing normoalbuminuric to hypoalbuminemic patients showed significant difference in total calcium.

As regards CRP (mg/dl), its mean in hypoalbuminemia group was 47.86 ± 41.54 ranging from 6.0 to 229.0 while in the non-hypoalbuminemia group was 47.21 ± 44.66 ranging from 6.0 to 219.0. There is significant difference between the two groups regarding CRP. Similarly Kim et al.[16] found that patients with hypoalbuminemia had a statistically significant higher CRP and PRISM III score.

In the current study, GCS at admission showed significant decrease in the hypoalbuminemia group (GCS was 12.71 ± 2.18 ranging from 7.0 to 15.0) when compared with the non-hypoalbuminemia group (GCS was 13.43 ± 2.0 ranging from 8.0 to 15.0).

In agreement with our results, Kumar et al.[12] found that hypoalbuminemia at admission was independently associated with mortality and these factors include age less than 1 year at admission, shock at admission, and GCS less than 8 at admission.

In agreement with our results, Chen et al.[18] reported that serum albumin was positively correlated with GCS in patients with traumatic brain injury.

As regards scoring systems, validity to predict mortality in the studied groups at 24 h of pediatric ICU admission, the PSOFA score best detected cutoff point is more than or equal to 3 with a sensitivity of 61.11%, specificity of 60.78%, and an AUC of 0.638 (95% CI: 0.537–0.739) (P ≤ 0.012). In agreement with our results, El-Nawawy[19] found that the SOFA score at admission was a good predictor of mortality in the overall pediatric ICU population. Moreover, the SOFA score had a good AUC of 0.886 for prediction of 30-day mortality.

As regards scoring systems' validity to predict mortality in the studied groups during pediatric ICU admission, the PSOFA score best detected cut-off point is more than or equal to 3, sensitivity of 60.71%, specificity of 67.65%, and an AUC of 0.687 (95% CI: 0.589–0.784) (P ≤ 0.002). Sayed et al.[20] conducted a study at the pediatric ICU, Pediatric Hospital, Benha University and Benha Children hospital and found that the value of PSOFA score was significantly higher among nonsurvived than survived cases. Total PSOFA more than or equal to 9.0 had the highest diagnostic characteristics in the prediction of death. Matics and Sanchez-Pinto[21] found that the maximum PSOFA score had excellent discrimination for in-hospital mortality, with an AUC of 0.94 (95% CI: 0.92–0.95).

The best cut-off score for SOFA in the Castelli et al.[22] study was also 4.5, with an AUC of 0.731, sensitivity of 73%, specificity of 68%, and negative predictive value of 86%, and positive predictive value of 47%.

As regards PRISM III best detected cutoff point is more than or equal to 15 with a sensitivity of 69.05%, specificity of 61.76%, and an AUC of 0.705 (95% CI: 0.605–0.805) (P ≤ 0.001). Similarly Bellad et al.[23] reported an overall mortality of 16.7 with 89.2% accuracy at a cutoff score of 15. Also, Dey et al.[24] in their study of PRISM III score in first 24 h observed PRISM as a sensitive predictor of outcome at a cutoff point of 13.5. Nasser et al.[25] showed that the AUC was 0.987 (95% CI: 0.968–1.000) for PRISM III scores. Findings were shown to have a good discriminatory performance between survivors and nonsurvivors.

An Indian study conducted by Varma et al.[26] showed that the overall performance of the PRISM III score was good with an AUC of 0.86 (good discrimination) with reasonable agreement between the observed and expected mortality.

Recently, the NPAR, in which neutrophil percentages are divided by serum albumin concentration, is used as a systemic inflammation-based predictor in patients with palliative pancreatic cancer[27], acute kidney injury[28], and septic shock[29]. Nevertheless, the predictive value of NPAR on mortality in pediatric ICU patients is not known. To the best of our knowledge, this is the first study to assess NPAR score in the prediction of final outcome and mortality in pediatric ICU. As regards NPAR the best detected cutoff point is more than or equal to 16.8 with a sensitivity of 70.24%, specificity of 61.76%, and an AUC of 0.676 (95% CI: 0.576–0.776) (P ≤ 0.003) to predict mortality in the studied groups during the pediatric ICU admission. Also, it is excellent with a best detected cutoff point of more than or equal to 18.2, sensitivity of 62.50%, specificity of 65.22%, and an AUC of 0.665 (95% CI: 0.567–0.762) (P ≤ 0.003) to predict mortality in the studied groups at admission.


  Conclusion Top


  1. Hypoalbuminemia is a common feature in critically ill children in the pediatric ICU.
  2. Hypoalbuminemia is an independent predictor of pediatric ICU mortality and of final outcome in critically ill children.


Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
World Health Organization. Updated guideline: paediatric emergency triage, assessment and treatment: care of critically-ill children. World Health Organization; 2016. Available from: https://apps.who.int/iris/handle/10665/204463.  Back to cited text no. 1
    
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Levitt DG, Levitt MD. Quantitative assessment of the multiple processes responsible for bilirubin homeostasis in health and disease. Clin Exp Gastroenterol 2014; 7:307.  Back to cited text no. 2
    
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Lee JY, Lee SH, Jung MJ, Lee JG. Perioperative risk factors for in-hospital mortality after emergency gastrointestinal surgery. Medicine 2016; 95:35.  Back to cited text no. 3
    
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Kittisakmontri K, Reungrongrat S, Lao-Araya M. Hypoalbuminaemia at admission predicts the poor outcomes in critically ill children. Anaesthesiol Intensive Ther 2016; 48:158–161.  Back to cited text no. 4
    
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Durward A, Mayer A, Skellett S, Taylor D, Hanna S, Tibby SM, Murdoch IA. Hypoalbuminaemia in critically ill children: incidence, prognosis, and influence on the anion gap. Arch Dis Child 2003; 88:419–422.  Back to cited text no. 6
    
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Leite HP, da Silva AV, de Oliveira Iglesias SB, Nogueira PC. Serum albumin is an independent predictor of clinical outcomes in critically ill children. Pediatr Crit Care Med 2016; 17:e50–e57.  Back to cited text no. 7
    
8.
Moustafa AA, Al Halawany AS, Rafa MF. Evaluation of hypoalbuminemia as a predictor of clinical outcome in critically ill children in Alexandria University Children's Hospital. J Med Sci Clin Res 2018; 6:32299–32306.  Back to cited text no. 8
    
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Horowitz IN, Tai K. Hypoalbuminemia in critically ill children. Arch Pediatr Adolesc Med 2007; 161:1048–1052.  Back to cited text no. 9
    
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Bhandarkar N, Save S, Bavdekar SB, Sisodia P, Desai S. Serum albumin and C-reactive protein as predictors of adverse outcomes in critically ill children: a prospective observational pilot study. Indian J Pediatr 2019; 86:758–759.  Back to cited text no. 10
    
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Tiwari LK, Singhi S, Jayashree M, Baranwal AK, Bansal A. Hypoalbuminemia in critically sick children. Indian journal of critical care medicine. Indian Soc Crit Care Med 2014; 18:565.  Back to cited text no. 11
    
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Kumar S, Aroor S, Kini PG, Mundkur S, Moideen A. Hypoalbuminemia as a marker of adverse outcome in children admitted to pediatric intensive care unit. Indian J Child Health 2018; 5:55029644.  Back to cited text no. 12
    
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Golhar ST, Agrawal H, Chauhan UM, Madhura A. Hypoalbuminemia in critically sick children. Int J Contemp Pediatr 2019; 6:922–926.  Back to cited text no. 13
    
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Yanni GN, Munar Lubis MA. The influence of albumin level in critically ill children to length of stay and mortality in paediatric intensive care unit. J Med Sci 2019; 7:3455.  Back to cited text no. 14
    
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Kim Y, Massie L, Murata GH, Tzamaloukas AH. Discrepancy between measured serum total carbon dioxide content and bicarbonate concentration calculated from arterial blood gases. Cureus 2015; 7:12.  Back to cited text no. 15
    
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Kim YS, Sol IS, Kim MJ, Kim SY, Kim JD, Kim YH, et al. Serum albumin as a biomarker of poor prognosis in the pediatric patients in intensive care unit. Korean J Crit Care Med 2017; 32:347.  Back to cited text no. 16
    
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Gaafar H, Sakar M. Hypocalcemia in the critically ill child. Med J Cairo Univ 1994; 62:67–73.  Back to cited text no. 17
    
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Chen D, Bao L, Lu SQ, Xu F. Serum albumin and prealbumin predict the poor outcome of traumatic brain injury. PLoS ONE 2014; 9:e93167.  Back to cited text no. 18
    
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El-Nawawy A. Evaluation of the outcome of patients admitted to the pediatric intensive care unit in Alexandria using the pediatric risk of mortality (PRISM) score. J Trop Pediatr 2003; 49:109–114.  Back to cited text no. 19
    
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Bellad R, Rao S, Patil VD, Mahantshetti NS. Outcome of intensive care unit patients using pediatric risk of mortality (PRISM) score. Indian Pediatr 2009; 46:1091–1092.  Back to cited text no. 23
    
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Dey PK, Prusty JB, Ghosh T, Kumar S, Choudhury J. Prediction of mortality risk by application of Pediatric Risk of Mortality (PRISM) score in tertiary care pediatric intensive care unit-a prospective observational study. JMSCR 2019; 7:54–61.  Back to cited text no. 24
    
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Nasser M, Y Al-Sawah A, R Hablas W, M Mansour A. Reliability Of Pediatric Risk Of Mortality III (Prism III) and Pediatric Index Of Mortality 3 (Pim3) scores in the pediatric intensive care unit of El-Hussein University Hospital. Al-Azhar J Pediatr 2020; 23:1048–1071.  Back to cited text no. 25
    
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