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Study on the concentration of urine neutrophil gelatinase-associated lipocalin in acute renal failure patients

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Objectives: To evaluate urine neutrophil gelatinase-associated lipocalin (uNGAL) concentration and its relation with causes, categories, stages and biochemical indexes of acute kidney injury (AKI) patients.

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STUDY ON THE CONCENTRATION OF URINE NEUTROPHIL GELATINASE-ASSOCIATED LIPOCALIN IN ACUTE RENAL

FAILURE PATIENTS

Pham Ngoc Huy Tuan*; Le Viet Thang**

SUMMARY

Objectives: To evaluate urine neutrophil gelatinase-associated lipocalin (uNGAL) concentration and its relation with causes, categories, stages and biochemical indexes of acute kidney injury (AKI) patients Subjects and methods: A prospective, cross-sectional study in 96 patients with AKI who admitted to General ICU, Trungvuong Hospital, Hochiminh city from 12 - 2013 to

01 - 2017 and a control group of 51 healthy people uNGAL had been done in all 96 patients and healthy people Results: All of the AKI patients (100%) had uNGAL elevation The average concentration of uNGAL in study group (412.26 ng/mL) was significantly higher than in control group (10.74 ng/mL) with p < 0.001 There was no relationship between AKI causes and uNGAL concentration with p > 0.05 The concentration of uNGAL was significantly higher in oliguria group in comparison with non-oliguria group (558.32 ng/mL vs 342.6 ng/mL) with p < 0.005 Patients’ uNGAL concentrations at the time of ICU admission were significantly related to their KDIGO stage (p < 0.001) Urinary NGAL had a moderate positive relationship with serum urea concentration (r = 0.529, p < 0.001) and a strong positive linear relationship with serum creatinine concentration (r = 0.852, p < 0.001) Conclusion: Urinary NGAL elevation was common in AKI patients The concentration of uNGAL depended on category and stage of AKI It had a moderate positive relationship with serum urea and strong positive relationship with creatinine concentration

* Keywords: Acute kidney injury; Urine neutrophil gelatinase-associated lipocalin

INTRODUCTION

Acute kidney injury is a common and

devastating problem with in-hospital mortality

of 40% to 80% in the intensive care setting

[10] The traditional blood (creatinine,

blood urea nitrogen) and urine markers of

kidney injury (casts, fractional excretion of

sodium, urinary concentrating ability) that

have been used for decades in clinical

studies for diagnosis and prognosis of AKI

are insensitive and nonspecific and do not

directly reflect injury to kidney cells Therefore, early recognition of renal injury

is important and may help prevent further renal damage and functional impairment Neutrophil gelatinase-associated lipocalin

is a small, 23 kDa protein that is an early biomarker for ischemic, septic or nephrotoxic kidney injury It is normally produced at low levels by the epithelial cells of the kidney, but it is quickly upregulated in the thick ascending limb (TAL) of the loop of Henle and the collecting ducts within three

* Trungvuong Hospital

** 103 Military Hospital

Corresponding author: Pham Ngoc Huy Tuan (bshuytuantv@yahoo.com.vn)

Date received: 12/09/2017

Date accepted: 22/11/2017

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hours of tubular epithelial injury Urinary

NGAL (uNGAL) has been evaluated as an

early biomarker of renal tubular damage

in a acute clinical settings such as the

operating room, ICU and emergency

department, and in high-risk procedures

such as cardiac surgery, radio-contrast

injection and after adult and pediatric

kidney and liver transplantation[1, 6, 7, 8, 9]

There is considerable evidence that

compared to increases in serum creatinine,

NGAL detects early or subclinical kidney

injury earlier, and predicts dialysis

requirement and mortality better[1]

In Vietnam, there are lack of studies on

the role of uNGAL in AKI diagnosis and

prognogsis in patients admitted to General

ICU Therefore, we have conducted this

research with the aim: Evaluation of the

uNGAL concentration and its relation with

causes, categories, stages and some

biochemical indexes of AKI patients

SUBJECTS AND METHODS

1 Subject

The study was conducted with a study

group of 96 AKI patients who admitted

to General ICU, Trung Vuong Hospital,

Hochiminh city from 12 - 2013 to 01 - 2017

and a control group of 51 healthy people

* Excluding criteria: Patients with chronic

kidney failure, did not fit with diagnostic

criteria, did not enough test results, anuria

patients or did not agree to participate in

the study

2 Methods

* Study design: A cross-sectional

descriptive study

* uNGAL measurement: 24-hour urine

was collected After that, the volume of urine

was measured before collecting 1 mL sample for testing purpose uNGAL was measured by the sandwich ELISA method using NGAL monoclonal antibody in the NGAL kit After that, the sample will be analyzed by Achitech System of Abbott, America to measure uNGAL concentration

* Diagnostic criteria: KDIGO definition

and classification of AKI [5]

- Diagnostic criteria for AKI: Serum creatinine increases ≥ 0.3 mg/dL (26.4 μmol/L compared to basic creatinine within

48 h or urine volum < 0.6 mL/kg BW/hour

at least 6 hours

- AKI degree:

+ AKI degree 1: serum creatinine from

< 220 μmol/L

+ AKI degree 2: serum creatinine from

220 - 353.6 μmol/L

+ AKI degree 3: ≥ 353.6 μmol/L

* Statistical analysis:

Statistical analyses were conducted using SPSS 20.0

RESULTS AND DISCUSSIONS

Table 1: uNGAL concentration in study

group

Index

Control group (n = 51)

Study group (n = 96)

p

uNGAL (ng/mL)

10.74 ± 5.18

412.26 ±

The average concentration of uNGAL in study group was 412.26 ng/mL which was significantly higher than in control group (10.74 ng/mL) with p < 0.001 The maximum

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and minimum concentration of uNGAL was

1292.38 and 69.63 ng/mL, respectively

With the range of urinary NGAL from 43.62

to 114.66 ng/mL, all of the AKI patients

(100%) had uNGAL elevation Study by Au

V also showed that the mean immediate

postoperative uNGAL levels in patients who

developed sustained AKI were 204.8

ng/mL, and significantly higher than those

who had normal renal function (31.9 ±

113 ng/mL) with p < 0.001 [1] This result

was similar to other studies by Geus H.R,

Makris K, Zappitelli M: there was a

significant higher of uNGAL concentration

in patients who diagnosed AKI compared

with non-AKI patients with p < 0.05 [6, 7, 8]

These differences in uNGAL concentration

were expected because kidney injury

associated with primary renal insults may

be more severe than that in most patients

included in our study, but our patients

were probably more severely ill

In current clinical practice, the gold

standard for identification and classification

of AKI is dependent on serial serum

creatinine measurements, which are

especially unreliable during acute

changes in kidney function We identified

uNGAL as one of the most upregulated

genes in the kidney soon after ischemic

injury NGAL protein was also markedly

induced in kidney tubule cells and easily

detected in the plasma and urine in animal

models of ischemic and nephrotoxic AKI

The expression of uNGAL protein was

also dramatically increased in kidney

tubules of humans with ischemic, septic,

and post-transplant AKI Importantly,

NGAL in the urine was found to be an

early predictive biomarker of AKI in a variety of acute clinical settings Emerging experimental and clinical evidence indicated that in the early phases of AKI from diverse etiologies, NGAL accumulates within two distinct pools, namely, a renal and a systemic pool Gene expression studies in AKI have clearly demonstrated rapid and massive upregulation of NGAL mRNA in the thick ascending limb of Henle's loop and the collecting ducts, with resultant synthesis of NGAL protein in the distal nephron (the renal pool) and secretion into the urine where it comprises the major fraction of uNGAL

This finding also confirms the need for future research to evaluate uNGAL in different renal disease subgroups in order

to understand fully how best to use uNGAL

to diagnose AKI

Table 2: Relation between urine NGAL

concentration and the causes of AKI (n = 96)

Causes n Urine NGAL (ng/mL)

(5) and others < 0.01

In our study, sepsis was the most common cause with the proportion of 60.4% There was no significant difference between these causes with p > 0.05 Our result was similar to study by Vaidya D.S: there was no significant difference between uNGAL concentration and several causes

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of AKI in these studies (p > 0.05) [10], but

was different with studies by Di Nardo M

and Geus H.R (there was a significant

higher concentration of uNGAL in septic

AKI patients than non-septic AKI patients

with p < 0.001 [4, 6] Lipoproteins also

have strong affinity that trigger an innate

immune response Therefore, it could be

postulated that these circulating ligands

that are linked to tubular epithelial TLR

activation are responsible for the increased

uNGAL concentrations, which we observed

in patients with sepsis However, there

were no increases in their SCr levels

However, recent studies in patients with

sepsis, septic shock, and systemic

inflammatory response syndrome has

reported contradictory findings A possible

explanation for this difference is the

variability of the subject inclusion time

(up to 48 h after ICU admission) Intensive

resuscitation and the administration of

antibiotics may have already occurred

before study inclusion, therefore most likely

inducing rapid changes of uNGAL values

Table 3: Relation between urine NGAL

concentration and AKI category (n = 96)

(ng/mL)

In our study, category of anuria occupied

32.3% all of AKI patients The concentration

of uNGAL was significantly higher in anuria

group compared with non-anuria group

(558.32 ng/mL compared with 342.6 ng/mL)

with p < 0.01 Our findings highlight the

mechanistic insights of NGAL levels

based on the specimens being measured Urine NGAL is proposed to derive predominantly from local renal synthesis

of NGAL in the thick ascending limb of the loop of Henle and the collecting ducts when under inflammatory and oxidative stress Therefore, the concentration of uNGAL was directly related to the renal tubule injury in AKI patients as well as urine excretion ability

Table 4: Relation between uNGAL

concentration and stage of AKI (n = 96)

AKI stages

Urine NGAL (ng/mL)

pAnova

< 0.001

p 1-2 , p 1-3 < 0.001,

p 2-3 = 0.002

According to the KDIGO classification, the stage 1 AKI in our study made up the highest proportion (70.8%) Stage 2 and 3 occupied smaller proportion (21.9% and 7.3%, respectively) Our results also pointed that patients’ uNGAL concentrations at the time of ICU admission were significantly related to their KDIGO stage (p < 0.001) This result was similar to the study by Geus H.R (p < 0.0001) and Zapittelli M (p < 0.0002) when research on the relation between uNGAL and RIFFLE stage [6, 8] NGAL fulfills a central role in regulating epithelial neogenesis, and in iron chelation and delivery after ischemic or toxic insults

to the renal tubular epithelium After kidney injury, NGAL is rapidly expressed on the apical epithelial membranes of the distal nephron NGAL is excreted in the urine

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through exocytosis and has local

bacteriostatic and proapoptotic effects

Therefore, uNGAL concentration had a

positive relation with the level of renal

damage which exhibited throughout the

high stage of KDIGO classification

Table 5: Correlation between uNGAL and

serum urea, creatinine concentration (n = 96)

Indexes

uNGAL

Correlation equation

169.141

- 150.730

In our study, uNGAL had a moderate

positive relationship with serum urea

concentration (r = 0.529, p < 0.001) and a

strong positive linear relationship with

serum creatinine concentration (r = 0.852,

p < 0.001) Boglignano D also pointed

that a significant correlation was also found between serum creatinine and uNGAL (r = 0.399, p < 0.001) [2] NGAL has mainly been studied in the setting

of acute renal failure Patients who experienced acute renal dysfunction showed

a marked increase in uNGAL levels, which preceded the increase in serum creatinine by a day In a single case of acute tubular necrosis due to heart failure induced hypotension, NGAL tubular expression was reported to be strongly increased [3] Hence, measurements of NGAL may serve as a very early marker of worsening renal function Urinary (or plasma) NGAL levels could therefore be used to adjust therapy, to anticipate and possibly prevent expected renal injury, even before a peak in serum creatinine occurs This potential of NGAL needs to be explored further in future studies

uNGAL = 17.304 x ure + 169.141

0

200

400

600

800

1000

1200

1400

1600

1800

Ure

Chart 1: Correlation between urine NGAL and urea concentration

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uNGAL = 2.616 x creatinin - 150.730

0

500

1000

1500

2000

2500

Serum creatinin

Chart 2: Correlation between urine NGAL and creatinine concentration

CONCLUSIONS

In our study, all of the AKI patients

(100%) had urine NGAL elevation The

average concentration of uNGAL in our

study group (412.26 ng/mL) was significantly

higher than in control group (10.74 ng/mL)

with p < 0.001 There was no significant

difference between AKI causes and

uNGAL concentration with p > 0.05 The

concentration of uNGAL was significantly

higher in oliguria group compared with

non-oliguria group (558.32 ng/mL compared

with 342.6 ng/mL) with p < 0.005 Patients’

uNGAL concentrations at the time of ICU

admission were significantly related to

their KDIGO stage (p < 0.001) Urinary NGAL

had a moderate positive relationship with

serum urea concentration (r = 0.529,

p < 0.001) and a strong positive linear relationship with serum creatinine concentration (r = 0.852, p < 0.001)

REFFERENCES

1 Au V et al Urinary neutrophil

gelatinase-associated lipocalin (NGAL) distinguishes sustained from transient acute kidney injury after general surgery KI reports 2016, 1 (1), pp.3-9

2 Bolignano D et al Neutrophil

gelatinase-associated lipocalin (NGAL) as a marker of

kidney damage American Journal of Kidney

Diseases 2008, 52 (3), pp.595-605

3 Damman K et al Urinary neutrophil

gelatinase associated lipocalin (NGAL),

a marker of tubular damage, is increased in patients with chronic heart failure European Journal of Heart Failure 2008, 10 (10), pp.997-1000

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4 Di Nardo M et al Impact of severe

sepsis on serum and urinary biomarkers of

acute kidney injury in critically Ill children: An

observational study Blood purification 2013,

35 (1-3), pp.172-176

5 Disease K Improving global outcomes

(KDIGO) acute kidney injury work group: KDIGO

clinical practice guideline for acute kidney

injury Kidney Int Suppl 2012, 2, pp.1-138

6 Geus H.R.H.D et al Neutrophil gelatinase-

associated lipocalin at ICU admission predicts

for acute kidney injury in adult patients

American Journal of Respiratory and Critical

Care Medicine 2011, 183 (7), pp.907-914

7 Makris K et al Urinary neutrophil

gelatinase-associated lipocalin (NGAL) as an

early marker of acute kidney injury in critically ill multiple trauma patients, in Clinical Chemistry and Laboratory Medicine 2009, p.79

8 Zappitelli M et al Urine neutrophil

gelatinase-associated lipocalin is an early marker of acute kidney injury in critically ill children: a prospective cohort study Critical Care 2007, 11 (4), p.R84

9 Chertow G.M et al Acute kidney injury,

mortality, length of stay, and costs in hospitalized patients J Am Soc Nephrol 2005, 16 (11), pp.3365-3370

10 Vaidya V.S et al Urinary biomarkers

for sensitive and specific detection of acute kidney injury in humans Clin Transl Sci 2008,

1 (3), pp.200-208

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