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 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 35  |  Issue : 4  |  Page : 1802-1809

Urinary neutrophil gelatinase-associated lipocalin in acute tubular injury among children with severe gastroenteritis


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

Date of Submission22-Jul-2022
Date of Decision16-Aug-2022
Date of Acceptance22-Aug-2022
Date of Web Publication04-Mar-2023

Correspondence Address:
Mostafa A. B. Etman
Tala, Menoufia
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/mmj.mmj_243_22

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  Abstract 


Background
Acute kidney injury (AKI) is a serious complication in critically ill children. It is a risk factor for mortality, prolonged stays in the ICU, and prolonged mechanical ventilation.
Objectives
To investigate urinary neutrophil gelatinase-associated lipocalin (NGAL) concentrations as an early biomarker of prerenal AKI in severe dehydrated pediatric patients with acute gastroenteritis.
Patients and methods
A cross-sectional study was conducted during the period study from August 2020 till March 2021, on 69 children, aged from 1 to 108 months, at the pediatric ICU) of Faculty of Medicine, Menoufia University, after obtaining consent from their parents and caregivers.
Results
NGAL level was highly significantly increased in the death group (1550.00 ± 57.74) than in the failure group (1425.00 ± 27.39), the injury group (929.76 ± 31.18), the risk group (866.36 ± 15.89), and the normal group (810.12 ± 37.42) (P < 0.001).
Conclusion
Urinary NGAL is a promising biomarker of AKI before a rise in serum creatinine) occurs. Severe dehydrated children have higher urinary NGAL concentrations compared with controls even in early stage with normal creatinine levels. So, urinary NGAL levels can be used for the early prediction of tubular renal impairment in children with severe dehydration better than creatinine.

Keywords: acute gastroenteritis, acute kidney injury, acute tubular injury, dehydration, early biomarker, lipocalin


How to cite this article:
Abd Elnaby SA, Mohamed Soliman MA, Etman MA, Abdelaziz AA. Urinary neutrophil gelatinase-associated lipocalin in acute tubular injury among children with severe gastroenteritis. Menoufia Med J 2022;35:1802-9

How to cite this URL:
Abd Elnaby SA, Mohamed Soliman MA, Etman MA, Abdelaziz AA. Urinary neutrophil gelatinase-associated lipocalin in acute tubular injury among children with severe gastroenteritis. Menoufia Med J [serial online] 2022 [cited 2024 Mar 28];35:1802-9. Available from: http://www.mmj.eg.net/text.asp?2022/35/4/1802/370992




  Introduction Top


Acute kidney injury (AKI) is a frequent and serious complication in critically ill children [1]. Moreover, it has been shown to be an independent risk factor for mortality, prolonged length of ICU stays, and prolonged mechanical ventilation [2]. Current consensus criteria for diagnosing AKI are based on changes in serum creatinine and urine output [3]. One must realize, however, serum creatinine is an indicator of glomerular function rather than renal tubular cell damage, which typically occurs during the initial phase of AKI in ICU patients [4].

Dehydration associated with gastroenteritis represents one of the leading causes of admission and morbidity in the pediatric emergency department [5]. It is also the most common cause of electrolyte abnormalities in children presenting at the emergency department; globally, diarrheal disease is responsible for ~10% of deaths in children under 5 years of age [6]. Considering its extensive global effect, it is not surprising that there are several serious complications associated with severe dehydration including hypovolemic shock, prerenal AKI, and acute tubular necrosis. Clinicians must determine whether patients only need to be rehydrated or whether they face more substantial morbidity. Consequently, there has been considerable interest in developing a simple noninvasive tool for measuring the severity of dehydration in children [6].

Acute dehydration caused by rotavirus gastroenteritis is seen frequently in pediatric age group. The most important treatment modality in these patients is recognizing and treating dehydration, electrolyte imbalance, and AKI. Rotavirus, norovirus, adenovirus, and astrovirus are known to cause viral gastroenteritis. Rotavirus is the most common cause of gastroenteritis in children and is prevalent in similar rates in both the developed and developing world [7]. Rotavirus gastroenteritis in infants and young children may last 5–7 days. Vomiting occurs in 90% of patients with low-grade fever or hyperpyrexia. Diarrhea occurs in about 30% and is characterized by odorless watery stool and is common in winter [8].

In the developed world, Campylobacter jejuni is the primary cause of bacterial gastroenteritis [8]. In children, bacteria are the cause in about 15% of cases, with the most common types being Escherichia coli, Salmonella, Shigella, and Campylobacter species [9]. The most common history findings for a patient with gastroenteritis are nausea, diarrhea (watery or bloody in dysentery), vomiting, abdominal pain, and high-grade fever (suggests an invasive organism as the cause) [10].

A number of protozoa can cause gastroenteritis [9]. Giardia lamblia is most common, but Entamoeba histolytica, Cryptosporidium spp, and other species have also been implicated. As a group, these agents comprise about 10% of cases in children. Protozoal gastroenteritis is manifested by abdominal pain, tenesmus, and offensive stool [11].

Neutrophil gelatinase-associated lipocalin (NGAL) is a small, 25-kDa protein initially discovered in activated human neutrophils. NGAL is expressed in limited quantities in other human tissues, including lungs, spleen, and kidneys. It is thought to inhibit bacterial growth, scavenge iron, and induce epithelial growth [2]. Plasma NGAL is freely filtered by the glomerulus and then largely reabsorbed by proximal tubular cells [12]. Upon renal tubular injury, NGAL reabsorption may be decreased, whereas NGAL de novo synthesis in epithelial cells of the loop of Henle and of distal tubule segments is strongly upregulated after which it is found in high concentrations in the urine [13].

There is only one adult study in the literature investigating serum NGAL levels in patients with acute gastroenteritis [14]. In this study, serum NGAL levels were shown to be higher in dehydrated patients compared with healthy controls. To the best of our knowledge, there is no pediatric age group study investigating urine NGAL levels in dehydrated patients [15].

Thus, the aim of this study was to investigate urinary NGAL concentrations as an early biomarker of prerenal AKI in severe dehydrated pediatric patients with acute gastroenteritis.


  Patients and methods Top


A cross-sectional study was conducted on 69 children, with ages ranging from 1 to 108 months at the pediatric intensive care unit (PICU), Faculty of Medicine, Menoufia University, after obtaining consent from their parents and caregivers during the period study from August 2020 till March 2021. The studied patients were classified into two groups: group I included 24 children with gastroenteritis with non-AKI, and group II included 45 children with gastroenteritis with AKI. Inclusion criteria were all sick patients ranging from 1 to 108 months of age, admitted to the PICU unit during the study period, both sexes, and children with severe gastroenteritis and severe dehydration. Exclusion criteria were children without parental consent or those who were admitted electively to PICU, patients under renal replacement therapy, children with chronic kidney disease as well as neonates (age <1 month old). Moreover, chronic hepatic, intestinal, renal, neurologic, metabolic, and immunologic diseases and drug usage for any disease were considered as criteria for exclusion. In addition, mild and moderate GE, clinically diagnosed bacterial GE consisting of high-grade fever with ill and toxic child with persistent vomiting and diarrhea (offensive with ± blood) with bad food intake, viral GE consisted of low-grade fever persistent vomiting and diarrhea (watery and odorless in winter), and mixed GE (mixed symptoms of bacterial and viral infection) were excluded. Ethical consideration: all participants were volunteers. Written or informed consent was obtained from their parents and caregivers after explaining the aim of the study. Approval of the study protocol was obtained by the ethical scientific committee of Menoufia faculty of medicine.

All patients and controls included in the study were subjected to the following: full history taking included family history of underlying kidney disease; full clinical examination, focusing on general examination, with measurement of blood pressure, temperature, respiratory rate, and heart rate; and local examination, such as chest, abdominal, cardiac, and neurological examination. The clinical dehydration score consists of four clinical characteristics: general appearance, eyes, mucous membranes, and tears. Each was scored as 0, 1, or 2 for a total score of 0–8, with 0 representing no dehydration; 1–4, some dehydration; and 5–8, moderate/severe dehydration, according to Bailey et al. [16]. Routine investigations included urine analysis, serum creatinine (mg/dl), creatinine clearance, serum urea (mg/dl), serum sodium, serum potassium, urine output in 24 h, stool microscopic examination and culture for bacterial gastroenteritis, and abdominopelvic ultrasound and radiography. Special investigations included concentrations of NGAL in urine samples determined by a quantitative kit at admission. The Human NGAL ELISA Kit (Thermo Fisher Scientific Inc.; NYSE: TMO, Waltham, Massachusetts, USA) was used. Principle of human NGAL test: The kit uses antibody sandwich enzyme-linked immunosorbent assay to assay the level of human NGAL in samples. Urine sample is centrifuged and then a deposit was obtained, which contains NGAL. This was added to a monoclonal antibody enzyme assay to form an immune complex, then the plate was washed five times to remove the uncombined enzyme, followed by addition of a chromogen solution and then addition of a stop solution. Sensitivity was 10.511 ng/ml, and the assay range was 12–3000 ng/ml. This assay has high sensitivity and excellent specificity for detection of NGAL. No significant cross-reactivity or interference between NGAL and analogs was observed.

Statistical analysis

Results were tabulated and statistically analyzed using a standard computer program using Microsoft Excel 2019 and SPSS V.25 program (SPSS 25.0 for Mac; SPSS Inc., Chicago, Illinois, USA). Two types of statistics were done: descriptive statistics, where description of data was in the form of mean ± SD for quantitative data and frequency and proportion for qualitative data. The mean is the sum of all observations by the number of observations, whereas the standard deviation is a measure of the degree of scatter of individual varieties around their mean. Analytical statistics comprised χ2, Fisher's exact test, Mann–Whitney test, correlation coefficient test (Person test), and the receiver operating characteristic (ROC) curve. P value less than 0.05 was considered a significant level.


  Results Top


A total of 69 patients were included in the study. Weight, age, and sex distribution showed no significant difference between the studied groups (P > 0.05). However, length, BMI, and systolic and diastolic blood pressures were significantly increased in the viral GE group than in the other group (P < 0.05). However, respiration, temperature, and pulse were significantly increased in the bacterial GE group than in the other group (P < 0.05). NGAL levels were significantly increased among bacterial infection (1111.47 ± 299.16 ng/ml) compared with mixed infection (900 ± 164.14 ng/ml) and viral infection (861.28 ± 79.53 ng/ml) [Table 1].
Table 1: Comparison between viral, bacterial, and mixed gastroenteritis groups regarding demographic, clinical data, vital signs, and neutrophil gelatinase-associated lipocalin levels in relation to cause of gastroenteritis

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Moreover, total leukocyte count, neutrophil, urea, blood urea nitrogen (BUN), creatinine, creatinine clearance, potassium, hemoglobin (Hb), serum osmolarity, general condition, eye status, skin and mucus membrane, tears, and score were significantly increased in the AKI group than in the non-AKI group. However, sodium showed a different variation with the studied group. On the contrary, there were no significant differences between the studied groups regarding, pH, HCO3, PCO2, and random blood sugar (P > 0.05). Moreover, NGAL level was significantly increased in the AKI group (1031.20 ± 244.95 ng/ml) than in the non-AKI group (810.13 ± 37.43 ng/ml) (P < 0.05) [Table 2].
Table 2: Clinical dehydration score, laboratory investigation, and neutrophil gelatinase-associated lipocalin level in the studied groups

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Additionally, the ROC curve analysis indicated that NGAL had a sensitivity of 92.5% and a specificity of 65% at area under the curve (AUC) of 0.819 with a cutoff value more than or equal to 802 ng/ml, indicating acute tubular injury in children with severe gastroenteritis and severe dehydration in PICU [Table 3], [Figure 1].
Table 3: Receiver operating characteristic curve analysis of neutrophil gelatinase-associated lipocalin as an early indicator of acute tubular injury in children with severe gastroenteritis and severe dehydration in pediatric intensive care unit

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Figure 1: ROC curve analysis of NGAL as an early indicator of acute tubular injury in children with severe gastroenteritis and severe dehydration in PICU. NGAL, neutrophil gelatinase-associated lipocalin; PICU, pediatric intensive care unit; ROC, receiver operating characteristic.

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Furthermore, NGAL level was highly significantly increased in the death group (1550.00 ± 57.74) than in the failure group (1425.00 ± 27.39), the injury group (929.76 ± 31.18), the risk group (866.36 ± 15.89), and the normal group (810.12 ± 37.42), with P value less than 0.001 [Table 4].
Table 4: Neutrophil gelatinase-associated lipocalin level of the studied patients

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Moreover, NGAL level was significantly increased in the high level of Hb group (1475.00 ± 75.46) than in the low level of Hb group (904.40 ± 40.76) and the normal group (810.12 ± 37.42), with P value less than 0.001. Moreover, NGAL level was significantly increased among prerenal and intrinsic renal failure group (1475.00 ± 75.46) than prerenal failure group (904.40 ± 40.76), with P value less than 0.001. In addition, NGAL level was significantly increased in the death group (1550.00 ± 57.74) than in the survivor group (980.59 ± 190.29), with P value less than 0.001 [Table 5].
Table 5: Comparison between hemoglobin level, stages of renal failure, death, and survivor regarding neutrophil gelatinase-associated lipocalin level of the studied groups

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  Discussion Top


Acute gastroenteritis is a major cause of morbidity and mortality, with three to five billion cases and nearly two million deaths occurring each year in children under 5 years of age, mostly in the developing world. The most important and dangerous complications related to AGE are dehydration, metabolic acidosis, and electrolyte disturbances [17] One of the most common causes of pediatric AKI is kidney hypoperfusion (prerenal AKI). By this mechanism, AGE could underlie about 12% of the AKI in children. Hospitalized children who develop AKI could experience longer hospital stays and higher mortality in the short term and increased risk of chronic kidney disease, hypertension, and proteinuria in the long term [18]. So, the aim of this study was to investigate urine NGAL concentrations as an early biomarker of prerenal AKI in severe dehydrated pediatric patients with acute gastroenteritis.

This study showed that systolic and diastolic blood pressures were significantly increased in the viral GE group than in the other groups (P < 0.05). However, respiration, temperature, and pulse were significantly increased in the bacterial GE group than in the other groups (P < 0.05). This is in agreement with a study by Mohamed et al. [19], who found a statistically significant difference between the studied groups regarding systolic blood pressure and BMI. Results of Koch et al.[20] were consistent with ours, where a significant difference was found regarding systolic blood pressure and diastolic blood pressure. On the contrary, this result was in contrast with the findings of Tam et al. [6], who conducted a study to compare clinical and biochemical markers of dehydration with the clinical dehydration score in children and clarified that following treatment, systolic and diastolic blood pressures declined in the dehydrated group in response to fluid treatment (two-tailed paired t test P=0.04, and P < 0.0001, respectively).

The current study showed that there were highly significant differences in the AKI group than in the non-AKI group regarding general condition, eye status, skin and mucus membrane, tears, and score (P < 0.05). Marzuillo et al.[17] found that duration of symptoms before hospitalization as anamnestic, dehydration more than 5% as clinical, and serum bicarbonate levels as biochemical parameters were significant and independent predictors for AKI in children hospitalized for AGE. The infectious agents were not able to influence the prevalence of AKI. This implies that the effect of vomiting, diarrhea, and subsequent dehydration is the main mechanism underlying AKI, with no effect of the AGE etiology.

The present study showed that total leukocyte count, neutrophil, urea, BUN, creatinine, creatinine clearance, potassium, Hb, and serum osmolarity were significantly increased in the AKI group than in the non-AKI group. However, sodium showed a different variation with the studied group. On the contrary, there were no significant differences between the studied groups regarding pH, HCO3, PCO2, and random blood sugar (P > 0.05). This finding matched with Marzuillo et al. [17], who did a study to evaluate prevalence of AKI and its risk factors in children hospitalized for AGE to identify early predictors of AKI and showed that there were significant differences between patients with AKI compared with patients without AKI regarding serum sodium level, serum phosphate level (mg/dl), and urea serum level. Moreover, Youssef et al.[21] reported that there was a significant increase between the two groups with and without AKI regarding urea and creatinine at admission and at third day (P<0.05). Vega and Avva [22] have demonstrated that serum urea increased and serum bicarbonate decreased with increasing percentage of lost body weight. The study by Tam et al.[6] also confirmed more urea in patients, although the degree of change was modest and not clinically significant. This is in agreement with Bagshaw et al. [23], who reported that urea is not produced at a constant rate, and the rate can be influenced by extrarenal factors. Urea production can be increased by diet, critical illness, burns, trauma, gastrointestinal bleeding, and sepsis. Moreover, in patients with decreased circulating blood volume owing to volume depletion or low cardiac output, resorption of urea increases because of the relationship between urea levels and water conservation mechanisms. Therefore, urea can be influenced by multiple factors and does not represent real-time changes in GFR.

On the contrary, Marzuillo et al.[17] reported that there were no significant differences between patients with AKI compared with patients without AKI regarding serum bicarbonates levels and serum potassium level (mEq/l). Çelik et al.[15] showed that the mean Hb levels, platelet count, and creatinine levels were not different in the two groups (dehydrated patients and healthy controls). On the contrary, the mean white blood cell count, BUN, and C-reactive protein levels were significantly higher in patients when compared with healthy controls (P = 0.001, 0.047, and 0.012, respectively).

This study showed that NGAL level was significantly increased in the AKI group than in the non-AKI group. This result was in congruence with Rabeea et al. [24], who conducted a study to investigate the value of NGAL and high-sensitivity C-reactive protein as markers for early detection of AKI in neonatal sepsis and found that levels of serum NGAL were significantly higher (P < 0.001) in the AKI subgroup as compared with no-AKI subgroup. Moreover, Youssef et al.[21] reported a significant increase between two groups with and without AKI regarding NGAL at admission and at third day (P<0.05). In addition, Bailey et al.[25] reported that there was a significant difference in serum NGAL between healthy children and critically ill children.

The current study showed that NGAL had a sensitivity of 92.5% and a specificity of 65% at AUC of 0.819 and cutoff value more than 802 ng/ml in indicating acute tubular injury in children with severe gastroenteritis and severe dehydration in PICU. Several studies have showed a lower cutoff value than our results, such as Akcan-Arikan et al. [26], who showed that at a cutoff of 139 ng/ml, the receiver operating characteristic curve of NGAL revealed an AUC of 0.677 with 95% [confidence interval (CI) of 0.557–0.786]. The sensitivity of NGAL was 86%, specificity was 39%, positive predictive value was 39%, and negative predictive value was 94%. Moreover, Youssef et al.[21] presented the receiver operating characteristic curve of NGAL for early detection of AKI and revealed an AUC of 0.63 with 95% (CI of 0.50–0.77). At cutoff value of 89.5 ng/ml, the sensitivity of NGAL was 84.6%, the specificity was 59.6%, positive predictive value was 36.7%, and negative predictive value was 68.4%. Singer et al.[27] reported that the AUC of NGAL (0.87, CI 0.81–0.94) was significantly higher than that of any other marker tested (P < 0.05).

However, Rabeea et al.[24] showed that ROC curves analysis suggested that a serum NGAL cutoff value of 144 ng/ml in neonatal sepsis can predict the development of AKI with a sensitivity of 100%, specificity of 95.6%, positive predictive value of 96.4%, and negative predictive value of 100%. Moreover, Cruz et al.[28] showed that serum NGAL at a cut-off value more than 89.6 ng/ml had 100% sensitivity and 92.3% specificity to detect AKI. The difference in NGAL sensitivity between studies may be due to the difference in value when calculating the cutoff.

The present study showed that NGAL level was highly significantly increased in the death group (1550.00 ± 57.74) than in the failure group (1425.00 ± 27.39), the injury group (929.76 ± 31.18), the risk group (866.36 ± 15.89), and the normal group (810.12 ± 37.42) (P < 0.001). We are the first to study a comparison of NGAL level according to the RIFLE criteria. However, Mohkam et al.[29] found that 77.5% developed AKI by RIFLE criteria, and among them, 43% met the risk (R), 51% the injury (I), and about 6% the failure (F) criteria.

This study showed that NGAL level was significantly increased among prerenal and intrinsic renal failure group (1475.00 ± 75.46) than prerenal failure group (904.40 ± 40.76), with P value less than 0.001. Singer et al.[27] showed that NGAL levels were significantly higher in patients with a clinical diagnosis of intrinsic AKI when compared with prerenal AKI (P = 0.007).


  Conclusion Top


Urinary NGAL is a promising biomarker of AKI before a rise in serum creatinine occurs. Severe dehydrated children have higher urinary NGAL concentrations compared with controls even in early stage with normal creatinine levels. Therefore, urinary NGAL levels can be used for the early prediction of tubular renal impairment in children with severe dehydration better than creatinine.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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