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��B	f:�������������A systematic review on prognostic indicators of acute liver failure and their predictive value for poor outcome
Running title: Review on prognostic indicators of ALF

Kama A. Wlodzimirow MEng.1, Saeid Eslami Pharma PhD1,2, Ameen Abu-Hanna PhD1, Martin Nieuwoudt PhD3, Robert A.F.M. Chamuleau PhD MD4

1Department of Medical Informatics, Academic Medical Center, University of
Amsterdam, Amsterdam, The Netherlands
2Pharmaceutical research center, School of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran
3 South African DST/NRF Centre of Excellence in Epidemiological Modelling and Analysis, Stellenbosch, South Africa.
4Tytgat Institute for Liver and Intestinal Research, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands



Grant support: K.W. is financial supported by a grant from insurance company Fonds NutsOhra, Zorgsubsidies, The Netherlands.
 
All authors made substantial contributions to the study design and methods. KW, SE and RC performed the literature search, evaluated studies, extracted data, analyzed data and drafted the manuscript. All authors interpreted the results and were involved in revising the final manuscript.


Correspondence to:
Robert Chamuleau
Tytgat Institute for Liver and Intestinal Research, 
Academic Medical Centre, University of Amsterdam
PO box 22700, 1100 DE Amsterdam, the Netherlands
Tel. 0031 20 5665405
Fax 0031 20 5669190e-mail: r.a.chamuleau@amc.uva.nl
Abstract
Context: Knowledge of the wide spectrum of indicators used worldwide to predict outcome in patients with acute liver failue (ALF) can be a useful starting point to find a better prognostic index for ALF.
Objective: To systematically identify and summarize prognostic indicators in patients with ALF and to evaluate their predictive value. 
Data Sources: Online databases MEDLINE� (1950-2012) and EMBASE� (1980-2012) were searched and considered studies published up to 01 January 2012.
Study selection: Articles were included if they reported original data from a clinical trial or observational study on adult patients with ALF and if one of their main objectives was evaluating prognostic indicators of ALF outcome. Of 1233 studies identified 103 were included for detailed analysis.
Results: 234 indicators and their effect on patient outcome were extracted and categorized into 8 categories: general markers (n=24), bio-markers (n=111), hemodynamics (n=11), liver function tests (n=5), imaging/morphology (n=11), scoring systems (n=38), time intervals (n=16), and treatments (n=18). The most frequently reported indicators were: coagulopathy, bilirubin, age and hepatic encephalopathy. 
Conclusion: There is large heterogeneity in prognostic indicators of ALF, methods of measurement, complexity of calculation and threshold values. This review provides large amount of information, including the extensive list of worldwide used indicators to predict outcome in patients with ALF, what can be useful for the future studies on ALF. 



Keywords: 
acute liver failure, fulminant hepatic failure, prognosis, predictive indicators, acute liver injury
Background 
Acute liver failure (ALF) is a syndrome with a high mortality up to 80% depending on the etiology and the clinical experience of the reference center (1). An early and exact assessment of the severity of ALF together with a prediction of its further development is critical in order to determine the further management of the patient. 
Spontaneous recovery occurs in a minority of patients with ALF. In most cases the only life saving treatment for ALF is liver transplantation (LT) with a 1 year survival of > 70%. The timely identification of patients with spontaneous recovery helps prevent LT and also the need for lifelong immunosuppressive therapy. Distinguishing patients requiring LT from those who will survive receiving only intensive medical care remains challenging. This distinction is also important in light of the worldwide shortage of liver donors. 
The critical decision for LT should be informed by the likelihood of spontaneous recovery, and many criteria for predicting this likelihood have been suggested. However, these criteria are not universally accepted. Most commonly used prognostic models like KCC (the King's College Criteria), Clichy criteria and MELD (Model of End-Stage Liver Disease) have shown inconsistent sensitivity and specificity. Prior reviews on paracetamol-induced ALF reported for KCC a pooled sensitivity of 58.2% and specificity of 94.6% (2) and a sensitivity range of 67% - 100% and specificity range of 52%-98% (3). Meta-analysis (4) of KCC for non-paracetamol-induced ALF reported pooled sensitivity of 68% (ranging from 13% to 96%) and specitificity of 82% (ranging from 36% to 100%). Sensitivity and specificity of Clichy Criteria ranged between 58 and 86% and 56 to 100% respectively (5-8). MELD, primarily designed to estimate mortality of cirrhotic patients undergoing transjugular intrahepatic portosystemic shunt (9), was later applied to patients with end-stage chronic liver disease (10) and used for organ allocation in patients awaiting LT (11). Since 2003 (3) MELD is used to predict prognosis in ALF patients and some studies report its superiority to KCC (12). Reported sensitivity and specificity of MELD ranges, respectively, from 54 to 96.5% and 54 to 88% (13-22).
There is consequently a need for a better prognostic index. At present no specific biomarker or set of biomarkers have been shown with sufficient sensitivity and specificity. In order to create a better prognostic index one needs to have a better understanding of the used prognostic indicators such as commonly used scoring systems as well as single predictor variables.  

Objectives
To identify and summarize previously employed prognostic indicators in terms of mortality and morbidity in patients with ALF and to assess the possibility of performing meta-analysis of the clinical studies on prognostic indicators for ALF. 

Materials and Methods
The following databases were searched: Ovid Embase(R) (1980 to 2012), Ovid MEDLINE(R) and Ovid MEDLINE(R) In-Process & Other Non-Indexed Citations (1950 to 2012) for journal articles based on keywords in title, abstract and MeSH terms, using the following query: (prognosis OR prognostic OR predict*) AND (acute liver failure OR fulminant hepatic failure OR acute liver injury OR acute hepatic failure OR (acute on chronic AND liver failure)). The asterisk �*� indicates the wildcard that may stand for any combination of characters (including nothing), so predict* stands also for �prediction� etc. �Liver failure� and �prognosis� were MeSh terms. All duplicate articles were removed and only English-language articles were included. The final search considered studies published up to 01 January 2012. Articles were included if they reported original data from a clinical trial or observational study on adult patients with ALF and if one of their main objectives was evaluating prognostic indicators of ALF outcome. Two reviewers independently screened the titles and abstracts. In the first step conference abstracts and papers, reviews, comments and case studies were excluded. Then, based on titles and abstracts studies were excluded that focused on animal models, pediatric population, hepatitis and other diseases, or studies that only evaluated therapeutic options (e.g. LT, supportive devices etc). Discrepancies between the 2 reviewers were resolved by consensus involving a third reviewer. Figure 1 shows the search flowchart. 
The initial two reviewers then extracted prognostic indicators of ALF. Discrepancies between them were again resolved by consensus involving the third reviewer.

A study�s statistical approach was classified as �univariate analysis�, when association was investigated between indicators and outcomes without adjusting for other possible confounders. Alternately, when association between an indicator and outcome was adjusted for other possible confounders, the approach was classified as �multivariate analysis�. Association was presented when the study reported the statistical significance level. 
Where possible, the association with mortality at admission was reported. An indicator could have positive (+) or negative (-) association when it was significantly associated with mortality. �Positive association� was used when the indicator was higher in non-survivors or tended to increase together with mortality. �Negative association� was used when the indicator was lower in non-survivors or tended to increase when mortality decreased (protective indicator). �No association� was used when the indicator was not significantly associated with mortality. 
If no other time point was reported, the admission values of indicators were analyzed in the studies. Indicators were either continuous or categorical. 

The indicators were divided into 8 categories: general markers, bio-markers, hemodynamics, liver function tests, imaging/morphology, scoring systems, time intervals, and treatment. �General markers� were indicators falling outside the 7 specific categories. �Bio-marker� was defined as a measurable compound or molecule used as an indicator of biological state. �Hemodynamics� was defined as flow, pressure or vascular resistance for systemic or portal circulation. �Liver function test� (LFT) was defined as any clinical assay designed to give information about the quantitative functional capacity of the patient's liver. �Imaging/morphology� was defined as features of liver biopsy, ultrasound or CT-scan. �Scoring system� was defined as any composite mathematical algorithm used for assessment and prediction of development of disease. �Treatment� was defined as any therapeutic plan. 

Results
Searching the online databases resulted in 1233 articles. Initial screening of titles and abstracts resulted in 125 articles for full text review, of which 103 articles were retained. 

Table 1 in appendix shows the characteristic of the final studies: a total of 10254 patients were included, with the largest study including 588 patients. Among the studies where gender was reported 54% of patients were female. In 13 studies (1390 patients) gender was not reported.
The most common etiology was viral, particularly hepatitis A and B virus, followed by paracetamol and other drug overdoses, and then acute autoimmune hepatitis.
64 studies performed univariate and 39 multivariate analysis. 28% of all studies were prospective, 27% retrospective, and 45% did not provide an indication of the design. 

234 different indicators and their effect on patient outcome were extracted from the studies and divided into 8 categories: 24 general markers, 111 bio-markers, 11 hemodynamics, 5 liver function tests, 11 imaging/morphology, 38 scoring systems, 16 time intervals, and 18 treatments. 142 indicators were encountered only once in the studies. 

Table 2 in appendix presents the indicators together with their association with mortality and morbidity, associations that are the results of either univariate or multivariate statistical analysis and if reported, their intervals or cut-off values. A short summary of this table presenting the �top3� of the most often studied indicators within each category is shown in table 1. Single studies are excluded from this table. Summary of the most often studied indicators is given below.  

Some studies performed separate analysis for specific subgroups of patients, e.g. patients with paracetamol (POD) and non paracetamol (nPOD) etiology or different outcomes such as survival versus death with or without LT, e.g. (1). 
The most commonly studied indicators in each category are:  

General Markers (n=24)
The most often studied general marker was age (47 studies) and 14 studies found it to be positively associated with mortality in univariate analysis. One of these studies (23) found a positive association with mortality in nPOD patients, while for POD patients no association with mortality was found. 25 out of 46 studies did not find an association between age and mortality in univariate analysis. 10 studies found a positive association with mortality on multivariate analysis and 8 did not. 3 studies did not report whether the association with mortality was significant or not. Studies considered age as continuous or categorical variable. 14 studies considered age as categorical variable with 7 different cut-off points, where cut-off point of 40 years was reported most often (4 times). 

The second most often studied general marker of ALF was hepatic encephalopathy (HE) (42 studies). 18 studies found HE positively associated with mortality in univariate analysis. One of these (24) found this association only at 10-20 days following the onset of HE, while at onset of HE this association was not found. 15 out of 41 studies did not find an association between HE and mortality in univariate analysis. One study (25) reported significant associations with mortality both in univariate and multivariate analysis without reporting the direction of the association. 12 studies showed positive associations with mortality in multivariate analyses in at least one time point in the course of the disease or in one subgroup of patients (e.g. POD on nPOD). 2 studies (24), (26) out of the above 11 demonstrated positive associations with mortality in some time points but not in other time points in multivariate analysis. One study (27) found a positive association with mortality in POD subgroup and not in the nPOD subgroup of patients using multivariate analysis. 
10 studies did not show a significant association between HE and mortality in multivariate analysis. 4 studies did not report whether the association with mortality was significant or not. 

Bio-markers (n=111) 
The most commonly studied bio-marker was total bilirubin (55 studies). 25 studies found bilirubin positively associated with mortality in univariate analysis. 6 studies (23), (20), (28), (29), (30), (31) considered either different time points during the course of disease or different subgroups of patients and showed mixed-results (positive or negative or no association with mortality). One study (31) found negative association with mortality in univariate analysis considering subgroup of POD patients. 27 studies did not find an association between bilirubin and mortality in univariate analysis. 13 studies found a positive association with mortality in multivariate analysis in at least one time point during the course of the disease or in one patient subgroup. One of these (26) showed a significant positive association with mortality for a value at day 4 of HE but not at admission nor on days 8 and 15 of HE in multivariate analysis. One study (27) found a positive association in the nPOD subgroup and not in the POD subgroup of patients in multivariate analysis. One study (31) found a positive association with mortality for a peak value during the stay in hospital only in nPOD subgroup of patients, while in the POD subgroup a negative association was found.
8 studies did not show any significant association between bilirubin and mortality in multivariate analysis. 4 studies did not report whether the association with mortality was significant or not. Studies considered bilirubin as continuous or categorical variable. 20 studies considered bilirubin as categorical variable with different cut-off points, most often 15mg/dL (4 times). 

The second most commonly studied bio-marker was coagulation measured by prothrombin time (PT) and/or INR (36 studies expressed as PT, 21 studies as INR and 6 studies as both PT and INR). 30 studies found positive associations between coagulopathy and mortality in univariate analysis. One study (20)  showed this association only at 1 to 6 days after the onset of HE. 2 other studies (1), (28) found this association in one subgroup of patients without finding it in another. In one study (30)  this association was found when PT was considered a categorical variable with a cut-off point of 50 seconds and could not repeat it for a cut-off point of 100s. One study (13) demonstrated positive association with mortality at the date of admission as well as at the date of the highest levels of M65 (epitope of cytokeratin 18 released from destroyed cells). 7 studies found negative associations between coagulopathy and mortality in univariate analysis in at least one time point during the course of the disease. 4 studies (24), (6), (32), (33) showed significant positive associations with mortality in some time points, without repeating it in other time points. 27 studies did not find associations between coagulopathy and mortality in univariate analysis. 
One study (25) reported significant association with mortality both in univariate and multivariate analysis without reporting the direction of association. 14 studies reported positive associations with mortality in multivariate analysis and 9 other studies did not. 3 studies showed negative associations with mortality on multivariate analysis. One (24) of these studies found this association only at 10-20 days after onset of HE. 8 studies did not report whether the association with mortality was significant or not. 

20 studies described alternate clotting related bio-markers, such as: ATIII, factor II, V, VII, VIII, fibrinogen degradation products, fibrinogen, hepaplastin, platelets, and thromboplastin time.  

Hemodynamics (n=11)
The most common studied was cerebral edema (CE), a consequence of increased intracranial pressure (8 studies). 6 studies found CE positively associated with mortality in univariate analysis. 3 studies showed positive associations with mortality on multivariate analysis and 2 other studies did not. One study did not report whether the association with mortality was significant or not.

The second most common studied indicator was heart rate (HR) (3 studies). 3 studies found HR positively associated with mortality in univariate analysis. One study (34) found this association only at the onset of HE, but did not find the association for the value at hospital admission. One study found no association with mortality on multivariate analysis. 

Besides intracranial pressure, which was studied twice, the rest of indicators in this category were studied only once.

Liver function tests (n=5)
The most common test was galactose elimination capacity (GEC) (4 studies). 2 studies found a negative association with mortality in univariate analysis, of which 1 study also did so in multivariate analysis. 2 studies did not find an association with mortality in univariate analysis. 
One study (35) conducted separate analyses for GEC measured within the first 72 hours and after 72 hours after acetaminophen ingestion but did not report whether the association with mortality was significant or not.
The following 4 tests were studied once. The plasma disappearance rate of indocyanine green (ICG-PDR) was found to have a negative association with mortality, while the other tests, such as: antipyrin clearance, caffeine clearance and plasma phenazone clearance were not associated with mortality.

Imaging/histology (n=11)
The most commonly studied indicator was liver volume expressed as standard liver volume (SLV) or ratio of estimated liver volume (ELV/SLV) (4 studies). 3 studies found a negative association with mortality in univariate analysis, and 2 of these also in multivariate analysis. One of these found this association only for the ELV/SLV ratio, but for not for SLV alone. 
2 studies did not find an association between liver volume and mortality in univariate analysis. 4 studies considered it as categorical variable with different cut-off points. 

The second most often studied was caspase activity = apoptose activity (M30) (3 studies). 2 studies found it positively associated with mortality on univariate analysis, of which 1 study found this association only at the date of the highest levels of M65 (epitope of cytokeratin 18 released from destroyed cells). One study and 1 other study found negative association and no association with mortality in univariate analysis, respectively. 
The rest of the indicators in this category were studied only once.

Scoring systems (n=38)
The KCC (26 studies) was the most commonly studied scoring system. 3 studies found positive associations between KCC and mortality in univariate analysis and 3 did not. 2 studies showed positive associations with mortality on multivariate analysis. One study (8) found this association only when comparing survivors with deceased patients but this association was not found when the deceased group was extended with transplanted patients. 19 studies did not report whether the association with mortality was significant or not. 

The MELD (18 studies) was the second most commonly studied score. 12 studies found MELD positively associated with mortality in univariate analysis. One study (20) found a positive association with mortality only at 1 to 6 days after the onset of HE and not at the onset of HE. 5 studies did not find an association between MELD and mortality in univariate analysis. 5 studies showed positive associations with mortality in multivariate analysis and 1 other did not. 3 studies did not report whether the association with mortality was significant or not. The MELD score was considered as either a continuous or categorical variable. 11 studies considered it a categorical variable with different cut-off points, where a cut-off point of 30 was reported most often (5 times).

Other scoring systems such as the APACHE II, Clichy criteria or SOFA scores were studied less often. Modifications of the KCC and MELD were found in only single studies.

Time intervals (n=16)
The most often studied was the interval from the onset of jaundice to onset of HE (14 studies). 8 studies found it positively associated with mortality in univariate analysis and 5 did not. 3 studies also found this association in multivariate analysis. 2 studies did not find an association with mortality in multivariate analysis. 13 studies considered it as a categorical variable with different range of cut-off points (below 1 week, 1-2 weeks, 2-3 weeks, 3-4 weeks and above 4 weeks, of which 1 week was most often considered  (9 studies).

The second most often studied was interval from onset of symptoms to diagnosis (3 studies). All studies did not find an association with mortality, 1 study in a univariate analysis, 1 study in multivariate analysis, and 1 study in both. All studies considered it as a categorical variable with a cut-off point of 7 days.
The other time intervals from this category were studied only once or twice.

Treatments (18)
Most reported was steroid therapy (4 studies). None of the studies found associations with mortality in univariate analysis.

The second most often studied treatments were: fresh frozen plasma infusion, hemodiafiltration, hemodialysis, plasma exchange, and artificial ventilation (each 3 studies). All studies did not find an association with mortality in univariate analysis for all these treatments, except for artificial ventilation, for which all studies found a positive association with mortality. 

Discussion
In our former review (36) we reported that there is a wide diversity in ALF definitions used in the literature. In our other review (37) we identified, characterized and assessed the quality of newly developed prognostic models of mortality for ALF patients and provided recommendations for future research on prediction models for ALF. This review is another part of the research on ALF. 
To our knowledge this is first systematic review exclusively dedicated to prognostic indicators for patients with ALF. In this review we identified, categorized and listed prognostic indicators used for prediction of outcome in patients with ALF as used in 103 studies. One of our goals at the start of the review was to present the results in a synthetic and quantitive way. However, due to the large heterogeneity of the findings we were forced to turn to the descriptive way. The differences in methods of indicators� measurement and the complexity of calculation of indicators (e.g. calculation mean, median, peak, threshold values) hamper the comparability among the studies and hinder performing such quantitative analysis. Although meta-analysis is theoretically possible, the results will not be meaningful.
Prior reviews on ALF are much more limited in the number of included studies (14 studies (2)), inclusion criteria and in the search terms (only �acute liver failure� and �prognosis� (3)) compared to our study . 
We allowed search to any synonym of ALF without limiting search a priori. The strength of our study is its extensiveness. We summarized a large number of indicators used worldwide to predict outcome in patients with ALF. This study provides a good overview of both the commonly used indicators (like bilirubin, age, HE, PT, INR) as well as less frequent, (hopefully promising) indicators. In addition our analysis covered a great heterogeneity of patients with ALF (or FHF) due to many different etiologies such as viral, acetaminophen overdose, Wilson disease and others. A limitation of our search is that we only addressed studies in which the prognostic effect of indicators formed a main objective; we may consequently have missed studies with a more limited focus on prediction. Our study may be limited by publication bias of studies on ALF outcome evaluation. 
The categories of indicators are more or less subjective, but are helpful to find a way in the large variety. 
On the whole, many studies did not motivate their choice for a specific subset of indicators. The majority of the studies was retrospective, and if the kind of the study was not reported one can assume it was retrospective, making the study limited in validity due to a lack of control in the quality of the available data.
In some studies it was not clear why the indicators which where not associated with mortality on univariate analysis were taken to the further analysis, such as multivariate analysis using e.g. logistic regression. In addition it was often unclear which indicators were considered as continuous and which as categorical. Also the reason to convert the continuous indicators to categorical was often not given. Furthermore the reasoning behind a certain threshold value of an indicator was not always clearly explained.
Studies reported association with mortality by analyzing the group of survivors and the group of non-survivors. In the studies where some patients received LT these patients were often added to the group of deaths. Associations found in such studies are questionable. Adding LT patients to �non-survivors� caused that the association with mortality reached significance. For example, one study (29) reported no association with mortality for bilirubin when comparing survivors with �non-survivors�, but extending this group with LT patients made bilirubin positively associated with mortality. To avoid such inaccuracy we advise to perform a separate analysis to compare the transplantation patients� characteristics to the death group. When the groups are similar one can consider forming the group with the combined outcome of �non-survivors�.  
In some cases mixed results were found when comparing the results, i.e. either positive or negative or no association with mortality. It remains intriguing why the direction of the association in various studies was incompatible, e.g. 2 studies (21), (38) reported positive association with mortality for male sex but 1 study (6) negative association. One explanation might be differences in the etiology: viral in (21), (38) and non-viral in (6). 

Indicators designed to measure the same underlying concept differed among the studies. For example coagulopathy which plays a crucial role in assessing of liver�s damage has been expressed by PT or INR. Of note, there are different thresholds for PT and INR values. A comparison of studies becomes then difficult, and even more difficult when in some studies PT is expressed as percentage of normal and in other as prolongation (in seconds). PT values depend on baseline values and measurement methods. However, there is large variation in laboratory assays, mainly due to the source of the used thromboplastin. For this reason INR seems to be more appropriate. Hovewer, there is no uniform standardisation of measuring coagulopathy in ALF patients.
In our systematic review we extracted a very large number of variables used for prediction in ALF. We suggest that next to the most often used indicators like age, HE, bilirubin and coagulopathy, which are already part of the most commonly accepted scoring systems such as KCC, MELD and Clichy criteria, the variables involved in the pathophysiology of ALF should be used for prediction of ALF like e.g. plasma ammonia, a contributing factor to hepatic encephalopathy, plasma lactate, representing disturbance of metabolic homeostasis and IL6/IL10 as biomarkers of the inflammatory response. 
When comparing results of various studies one must consider differences in case-mix, in etiology, therapies, power of the analysis, and outcome measures. The variability in the prognostic indicators of ALF and their threshold values hamper the comparability among the studies. In general none indicator appears to be conclusive in multivariate analysis. There is still a clear need to define the best combination of prognostic indicators for ALF, which should be tested in a large prospective study of ALF patients with different etiologies. Our unique inventarisation will be a good starting point for developing a prognostic index for ALF of clinical importance.
Figure Legends 
Figure1. Search flowchartTable1. Top 3 of the most often studied indicators within each category
IndicatorUnivariate analysisMultivariate analysisNRCat: General markersAge 
47 studies14 studies +ass (1)*
25 studies no ass.(1)*10 studies +ass. 
8 studies no ass.3 studies  Hepatic encephalopathy (HE) 
42 studies 18 studies +ass. (1)*
15 studies no ass (1)*
1 study ass. but direction NR12 studies +ass. (3)*
10 studies no ass. (3)*
1 study ass. but direction NR4 studies  Sex/gender
36 studies2 studies +ass.
1 study �ass.
28 studies no ass.1 study +ass.
1 study �ass. 
5 studies no ass.3 studies  Cat: Bio-markersBilirubin total 
55 studies 25 studies +ass (6)*
1 study �ass. (1)*
28 studies no ass. (5)*13 studies +ass. (3)*
1 study �ass. (1)*
8 studies no ass. (2)* 4 studies  Coagulopathy 
PT 42 studies 
INR 27 studies 
30 studies +ass (5)*
7 studies �ass. (4)*
1 study ass. but direction NR (1)*
27 studies no ass. (10)*14 studies +ass. 
3 studies �ass. 
1 study ass. but direction NR (1)*
9 studies no ass. (1)*8 studies  Creatinine
40 studies16 studies +ass. (6)*
1 study �ass. (1)*
1 study ass. but direction NR (1)*
25 studies no ass. (6)*4 studies +ass. 
1 study ass. but direction NR (1)*
7 studies no ass. (1)*2 studiesCat: HemodynamicsCerebral edema 
8 studies6 studies +ass. 3 studies +ass. 
2 studies no ass. 1 study  Heart rate 
3 studies3 studies +ass. (1)*
1 study no ass. (1)*1 study no ass. ICP (Intracranial pressure) 
2 studies2 studies +ass.1 study no ass.Cat: Liver function testsGalactose elimination capacity (GEC) 4 studies2 studies �ass. 
2 studies no ass. 1 study �ass. 
1 study  Cat: Morphology / HistologyLiver volume 
4 studies3 study �ass. (1)*
2 studies no ass. (1)*2 study �ass. 
Caspase activity / apoptose activity (M-30) 3 studies1 study �ass. 
2 studies +ass. (1)* 
1 study no ass. (1)*Cat: Scoring systemsKCC 
26 studies3 studies +ass. 
3 studies no ass. 2 studies +ass. 
1 study no ass. 19 studies  MELD 
18 studies11 studies +ass. (1)*
5 studies no ass. (1)*5 studies +ass. 
1 study no ass.4 studies APACHE II 
7 studies3 studies +ass. 
1 study no ass. 2 studies +ass.2 studiesCat: IntervalsInterval jaundice (icterus) to HE 14 studies8 studies +ass. 
5 studies no ass. 3 studies +ass. 
2 studies no ass. Interval onset of symptoms to diagnosis 3 studies2 studies no ass. 
2 studies no ass. Cat: TreatmentsSteroids / corticosteroids  4studies4 studies no ass. Fresh frozen plasma infusion 
3 studies3 studies no ass. Hemodiafiltration 3 studies3 studies no ass. Hemodialysis 3 studies3 studies no ass. Plasma exchange 3 studies3 studies no ass. Ventilation / intubation 
3 studies3 studies +ass. 
+ass. = significant positive association with mortality (lower/less in survivors, higher/more in non-survivors); �ass. = significant negative association with mortality (higher/more in survivors, lower/less in non-survivors); no ass. = no significant association with mortality
NR = significant association with mortality not reported
()*= number of studies with mixed results (positive or negative or any), so double counted 
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