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Urine is also more likely to contain biomarkers arising from the kidney. On the other hand, urine samples are likely to undergo protein degradation, also urine biomarker concentrations can be affected by urine flow rate changes. Serum samples can be obtained also in anuric patients and serum biomarkers tend to be more stable.
The disadvantage of serum biomarkers is that they can reflect systemic response to certain diseases and CPB bypass, rather than specific kidney dysfunction. Despite the promising findings at the level of basic research, this knowledge has not been yet transferred to clinical practice as agreement regarding the appropriate thresholds for diagnosis of AKI is yet to be confirmed. Clinical use of novel biomarkers will most likely remain limited until prospective multicentre studies demonstrate their utility [ 9 ].
Neutrophil gelatinase-associated lipocalin NGAL concentration in renal proximal tubules increases rapidly after renal ischemia-reperfusion injury and, as such, it has been extensively investigated as a novel biomarker for AKI [ 7 ]. Few studies in animal models concluded that NGAL is one of the most upregulated genes and proteins in the kidney very early after the kidney injury [ 3 ]. Tubule epithelial cells that were undergoing proliferation and regeneration were identified as the site of the highest NGAL protein expression [ 3 ]. This may suggest the NGAL role in the repair process.
Urine NGAL is mostly derived from the distal nephron epithelial cells while plasma NGAL originates from damaged tubules via back leak and also from extrarenal organs [ 14 ]. It remains unclear to what extent non-renal NGAL sources might adversely affect the diagnostic accuracy. The lack of a standard AKI definition, the lack of precisely identified cut-off values and differences in clinical assay characteristics are additional limitations preventing widespread use of NGAL in clinical practice [ 3 ]. Another important point to bear in mind is the fact that the success of NGAL as also some other biomarkers mentioned in the article is based on the studies conducted in carefully selected homogenous populations.
Regarding that many other conditions such as age, anaemia, cancer and inflammatory conditions NGAL is acute phase reactant can affect NGAL concentration makes NGAL performance as a reliable predictive biomarker of AKI poorer in real-life patients with comorbidities or in critically-ill patients [ 15 , 16 ] and these patients are common in the field of the cardiovascular surgery. This has been the largest study of its kind so far. In both populations NGAL urine and plasma concentrations were the highest within 6 hours after surgery and showed improved risk prediction [ 3 ].
Author Beckhardt to speak about his Roy Neely novels
Moreover, urinary NGAL seems to be increased also in acute urinary tract infections [ 22 ]. Urinary kidney injury molecule 1 KIM-1 , another biomarker described in our paper was not shown to be a helpful biomarker in the setting of the urinary tract infection. Recent research has provided valuable data about cut-off values. In the prospective, large, multicentric observational cohort study, plasma NGAL had the strongest ability to predict the progression of AKI.
However, one of the problems of published studies is lack of following standard guidelines for reporting studies of diagnostic accuracy. Such guidelines should be considered to minimize study errors and heterogeneity in the reported predictive NGAL value, the time point of measurement, assay used and conditions of sample storage [ 3 ]. Kidney injury molecule-1 KIM-1 is an immunoglobulin Ig superfamily transmembrane receptor that is expressed in the tubules in the setting of kidney injury to aid the removal of necrotic and apoptotic debris.
KIM-1 is expressed at a low level in normal kidneys, but after ischemic injury, upregulation of the protein is increased in proximal tubules [ 24 ]. Animal studies have shown that the levels of urinary KIM-1 increase in models of ischemic AKI, sometimes without adjuvant creatinine elevation [ 25 ]. KIM-1 was markedly elevated in dedifferentiated proximal tubular cells of ischemic rat kidney. Unfortunately, these excellent results could not be reiterated in human studies so far. In one study KIM-1 [ 26 ] did not perform better than sCr or urine output in the prediction of renal replacement therapy or death, with an AuROC of only 0.
Another finding of this study was that combining multiple AKI biomarkers improved the overall predictive value [ 11 ]. A recent study of adults who underwent cardiac surgery illustrated that preoperative urinary KIM-1 levels were able to predict the development of AKI with AUC of 0. A systemic review revealed that KIM-1 is an efficient urinary biomarker of AKI within 24 hours after kidney injury when aetiology was ischemic acute tubular necrosis.
A meta-analysis of 11 studies revealed that urinary KIM-1 showed the best performance characteristics in patients after cardiac surgery hours after CPB, however, the diagnostic accuracy was better in infants and children than in adults. This is probably due to significant comorbid conditions, such as atherosclerosis, hypertension and diabetes mellitus being prevalent in adults [ 24 ]. Despite numerous analyses being carried out, the small study populations and heterogeneous patient type, the clinical applicability of KIM-1 as an biomarker for early AKI detection needs to be validated in larger studies with more homogenous study population [ 24 ].
The concentration of KIM-1 is also affected by other conditions such as sepsis and use of contrast media. Age is another factor that affects expression of KIM In addition, the urinary concentration may be influenced by common diseases such as diabetes mellitus, hypertension and atherosclerosis [ 24 ]. Interleukin IL is a proinflammatory cytokine with a molecular weight of 18 kDa. The major source of production is renal tubular cells and macrophages.
Its preoperative levels are low and increase in patients who develop AKI [ 20 ]. IL is up-regulated in response to ischemic reperfusion injury. It is specific to the renal tubules [ 28 ]. It has been shown in animal studies that inhibiting IL in mice decrease the severity of ischemic AKI [ 11 ]. Another animal model demonstrated significant increases in IL in whole kidneys after experimentally induced AKI.
IL levels may represent a non-specific marker of bypass-associated systemic inflammation rather than tubular damage, because urinary IL correlated with the duration of CPB [ 29 ]. In a small study with patients urine IL appeared to be superior to creatinine in early detection of AKI. It also performed better at differentiating pre-renal from intrinsic tubular AKI. In a study that compared 32 urinary biomarkers IL was the best predictor of the primary outcome of worsening AKI or death as well as the secondary outcome of AKIN stage 3 or death [ 10 ].
Results of a multicentre, prospective observational cohort study showed that urinary IL is a promising biomarker in its ability to predict the worsening of AKI at the time of creatinine-based diagnosis of AKI [ 23 ]. IL levels have been observed to correlate with mortality in patients not only with AKI but also infections, hepatitis, malignancies and SLE. Serum IL elevation correlates with cardiovascular, cerebrovascular and peripheral vascular events in patients on haemodialysis [ 30 ].
Cystatin C CysC is a 13 kDa proteinase inhibitor, formed in all cells with a cell nucleus that enters the proximal tubules by glomerular filtration. The protein is reabsorbed by the healthy proximal tubular cells and in disease free individuals only minimal concentrations are found in urine [ 8 ]. A recent study published by Ghonemy et al. So the conclusion was that CysC values measured immediately at the end of the operation provide an early indication of the possible onset of AKI but the predictive values depend on the AKI definition.
CysC was a poor biomarker of AKI in the first 24 hours after cardiac surgery [ 32 ]. Another study, a prospective, single centre study with 70 patients, found that early post-op serum CysC increase appears to be a moderate biomarker in the prediction of AKI. A preoperative and intraoperative CysC increase has only a limited diagnostic and predictive value [ 31 ]. The conclusion of this large, multicentre study was that CysC was less sensitive for AKI detection compared with creatinine but the presurgical CysC level was a stronger predictor of AKI than the presurgical creatinine of eGFRCr glomerular filtration rate estimated from creatinine [ 17 ].
Two prior studies did not demonstrate a clear advantage for serum CysC in predicting AKI following adult cardiac surgery [ 33 ]. In the study by Wald et al. Another finding of this study was that CysC rose later than creatinine in patients who developed AKI [ 31 ]. The role of urinary CysC as a biomarker of cardiac surgery-associated AKI is controversial with small studies demonstrating mixed results its role remains questionable. It can be recognized as an additional biomarker in the panel of novel biomarkers for AKI diagnosis.
There are still data that support the utility of urinary CysC in other clinical settings. Critical illness and nephrotoxin-associated AKI are such examples [ 35 ]. In one study [ 36 ], plasma CysC was shown to be a good predictor for AKI in patients after acute myocardial infarction. Another published paper demonstrated a correlation between serum CysC and AKI in patients with major burns [ 37 ]. In an article with only abstract being available in English, researchers found an association between serum CysC and the metabolic syndrome [ 38 ]. Both, tissue inhibitor of metalloproteinase-2 TIMP-2 and insulin like growth factor binding protein 7 IGFBP7 are involved in G1 cell cycle arrest of renal tubular cells during the early period of cell injury caused by ischaemic or inflammatory processes [ 39 ].
Authors concluded that this difference in results could be due to different risk groups of patients. In the study by Wetz et al. In the paper published by Meersh et al. Fatty acid binding proteins are small 15 kDa cytoplasmic proteins expressed in tissues with active fatty acid metabolism. Their function is facilitation of long-chain fatty acid transport, regulation of gene expression and reduction of oxidative stress.
In the human kidney, liver fatty acid-binding protein L-FABP is expressed in the proximal tubules as the major source of energy metabolism. It binds free fatty acids and has a renoprotective role [ 12 ]. L-FABP is undetectable in healthy urine. The AUC was 0.
With AUC of 0. L-FABP is a promising candidate to become a biomarker for AKI detection, but this prediction is based on studies that included patients with contrast nephropathy, patients with chronic kidney disease and pharmacologically induced AKI. Further studies are needed with patients after CPB cardiac surgery [ 44 ].
Originally, Klotho was identified as the product of an antiaging gene in and has become a major focus in the renal field for the past 5 years. In the mammalian kidney, Klotho is expressed at two sites; distal convoluted tubules and proximal convoluted tubule. Two Klotho proteins were identified: It has been proposed that downregulation of renal Klotho in AKI is a general phenomenon following acute kidney insults such as ischemia, oxidative stress and exposure to nephrotoxins.
Thus, Klotho is considered as an early biomarker of AKI and it has potential of becoming a therapeutic agent. In a rodent model, Klotho levels were sustainably decreased 3 hours after the induced AKI by ischemia-reperfusion injury, advocating that renal Klotho is one of the earliest biomarkers of kidney injury. Another animal study has shown downregulation of Klotho in AKI regardless of aetiology [ 45 ].
At the moment we do not have data regarding the role of Klotho as a biomarker for AKI from human studies [ 45 ]. Roundabout protein 4 Robo4 is an endothelial-expressed transmembrane receptor and regulator of cell activation. Roundabout proteins are a family of transmembrane receptors originally identified for their role in axon guidance during development of the nervous system.
So far, four receptors have been identified.
Robo4 was described as an endothelial expressed gene. Plasma levels of Robo4 were significantly higher in patients 2 hours post-operatively compared with levels prior to surgery. In the same study, they found a positive association between urine NGAL levels and plasma Robo4 levels 2 hours after the surgery. Elevated post-operative plasma Robo4 levels correlated significantly and positively with plasma and urine NGAL levels. The association maintained when patients were divided into those with and without AKI.
There were no association between creatinine and Robo4 [ 46 ]. Semaphorin 3A is another promising biomarker for early AKI detection. It is highly expressed after AKI in mice and humans, but its pathophysiological role is unknown. So far, conducted research revealed that semaphorin 3A mediates tubular epithelial cell apoptosis and inflammation and that in non-diseased kidneys this molecule is expressed in renal collecting ducts and podocytes [ 47 ]. In one study, urine semaphorin 3A increased 2 hours after CPB and peaked at 6 hours, its concentration decreased to a non-significant level at 12 hours after CPB.
Netrin-1 has been recently identified as a novel tubular injury biomarker with a potential to diagnose AKI much earlier than existing biomarkers of kidney injury. It is a laminin-related secreted protein highly induced after acute and chronic kidney injury [ 50 ]. In the same study [ 51 ], urinary KIM-1 was associated with poor prognosis. To date only one study [ 52 ] with netrin-1 investigation for AKI detection after cardiac surgery has been published.
In addition, in the same study netrin-1 correlated with duration, severity of AKI and with duration of the hospitalisation. Cysteine-rich protein 61 CYR61 is an extracellular matrix molecule. Preclinical studies showed that the CYR61 concentration is increased at sites of inflammation, wound healing accompanied with chronic inflammation and tissue injury [ 53 ].
One study performed on mice in which unilateral kidney ischemia reperfusion injury was induced, proposed that stoppage of CYR61 stops inflammatory damage associated with ischemic AKI. Another study on mice revealed rapid up-regulation of the CYR61 gene in kidney after induced renal ischemia. Induction of the protein was detected within one hour following ischemia. Currently we lack data about CYR61 values in humans or its changes in kidney injury [ 54 ]. The non-existence of a sensitive, specific and early marker of AKI has been a limiting factor in fast diagnosis of AKI and its treatment.
Although serum creatinine is the standard marker, it has numerous limitations, with its dependence on age, sex and muscle mass being most impactful. Existence of chronic renal failure also affects creatinine levels. These are main reasons for inability of creatine level changes to detect time and type of renal injury [ 24 ].
There are many biomarkers for detection of early kidney injury undergoing scientific and clinical research with NGAL being the most promising. However, NGAL is still not routinely used in clinical practice because overall results are inconsistent, with variations in sample collection protocols, procedure type and patient population. Definition of AKI is still not standardised [ 7 ]. Regarding diagnostic usefulness of NGAL and other novel biomarkers, authors vary in their opinions from very optimistic to negative [ 2 ]. There are few explanations why the results are so broad.
Biomarkers are investigated in different clinical settings, paediatric post-cardiac bypass, to patients with septic shock, adults after cardiac surgery with CPB. Timing of renal injury is not well known in all settings. Furthermore, AKI is not the only cause of raise of biomarker levels. Some of these are also associated with sepsis, diabetic nephropathy, systemic lupus erythematosus, haemolytic uremic syndrome and inflammation [ 2 ].