European Journal of Heart Failure (2010) 12, 3237

doi:10.1093/eurjhf/hfp169

Acute kidney injury and outcomes in acute

decompensated heart failure: evaluation
of the RIFLE criteria in an acutely
ill heart failure population
Noritake Hata*, Shinya Yokoyama, Takuro Shinada, Nobuaki Kobayashi,
Akihiro Shirakabe, Kazunori Tomita, Mitsunobu Kitamura, Osamu Kurihara,
and Yasuhiro Takahashi
Division of Intensive Care Unit, Chiba Hokusoh Hospital, Nippon Medical School, 1715 Kamagari, Inbamura, Inbagun, Chiba 270-1694, Japan
Received 11 June 2009; revised 16 September 2009; accepted 9 October 2009

Aims

The clinical course including the outcome of acute decompensated heart failure (ADHF) correlates with renal dysfunction, but the evaluation of renal function has not yet been standardized. We therefore investigated the relationship between the prognosis of ADHF and acute kidney injury (AKI) evaluated using the risk, injury, failure, loss, end
stage (RIFLE) criteria.
.....................................................................................................................................................................................
Methods
This study assessed 376 consecutive patients with ADHF admitted to the intensive care unit (ICU) (mean age 71.6
and results
years; 238 male). The underlying aetiology was ischaemic heart disease, hypertensive heart disease, cardiomyopathy,
valvular diseases, and other in 124, 70, 60, 107, and 15 patients, respectively. We defined AKI according to the RIFLE
criteria, and the most severe RIFLE classifications during hospitalization were adopted to assess patient outcomes.
The in-hospital mortality was significantly higher among patients with AKI (29 of 275; 10.5%) than in those
without AKI (1 of 101; 1.0%, P 0.0010). Both ICU and hospital stays were longer for patients with AKI
(8.8 + 15.4 vs. 48.6 + 47.6 days), than for patients without (5.0 + 2.8 vs. 25.7 + 16.8 days, P , 0.05 and P , 0.001).
.....................................................................................................................................................................................
Conclusion
Acute kidney injury evaluated by the RIFLE criteria was associated with a poorer outcome for patients with ADHF.

----------------------------------------------------------------------------------------------------------------------------------------------------------Keywords

Cardiovascular disease Renal damage Prognosis

Introduction
Acute kidney injury (AKI) affects the outcome of patients admitted
to intensive care unit (ICU).1 3 In addition, the outcomes of
acute decompensated heart failure (ADHF) correlate with renal
dysfunction,4,5 however, to date a consensus regarding the most
appropriate methods for evaluating renal function and AKI has
not been reached. The RIFLE criteria have recently been established as the standard method for evaluating AKI in critically ill
patients including those with neurological, cardiovascular, pulmonary, malignant, and gastrointestinal diseases,6,7 but the clinical significance of such evaluations has not been determined in patients
with heart failure. In this study, we therefore investigated the

association between ADHF outcomes and AKI evaluated by this

method.

Methods
Study population
We investigated the clinical course of 376 consecutive patients with
ADHF who were admitted to the ICU in Chiba Hokusoh Hospital,
Nippon Medical School, Japan, between April 2000 and June 2008.
Heart failure was diagnosed based on the Framingham criteria.8
Patients with acute cardiovascular disease such as acute myocardial
infarction (AMI), myocarditis, pericarditis, and Takotsubo cardiomyopathy were excluded from the study. In addition, only the first

* Corresponding author. Tel: 81 476 99 1111, Fax: 81 476 99 1911, Email: hata-n@nms.ac.jp
Published on behalf of the European Society of Cardiology. All rights reserved. & The Author 2010. For permissions please email: journals.permissions@oxfordjournals.org.

33

AKI and outcomes in ADHF

admission was considered for patients who were readmitted to the

ICU during the study period (n 80). Patients who had undergone
renal replacement therapy before admission were also excluded
(n 15).

Data collection
Data were retrospectively retrieved from hospital medical records.
Laboratory data included serum creatinine, daily urine output, and
brain-type natriuretic peptide (BNP) levels during hospitalization.
Age, sex, history of chronic renal insufficiency, and haemodialysis,
aetiology of heart failure, Killip classification of heart failure severity,
and left ventricular ejection fraction measured by cardiac ultrasonography (Teichholz method) were recorded. Furthermore, medications
administered in the ICU, use of acute blood purification therapy, any
heart surgery, duration of ICU and hospital stays, and in-hospital mortality were also evaluated.

Evaluation of acute kidney injury

In view of the fact that the majority of patients with ADHF receive
treatment with diuretics which influence urine output, and since
urine output could not be precisely measured in the general wards;
AKI was investigated based only on the creatinine criteria of the
RIFLE classification.9,10 Patients were classified as having: no AKI,
Class R (risk), Class I (injury), and Class F (failure). Patients were classified twice according to the RIFLE criteria: upon admission (RIFLEadm)
and the most severe classification recorded while in hospital
(RIFLEmax). The RIFLEmax in patients who received renal replacement
therapy was Class F.11 Furthermore, RIFLEmax was evaluated before
heart surgery in surgical patients. Serum creatinine levels in patients
without chronic renal insufficiency according to their medical history
were calculated using the Modification of Diet in Renal Disease
(MDRD) equation as recommended by the Acute Dialysis Quality
Initiative, by solving the MDRD equation for serum creatinine
(CrMDRD) assuming a glomerular filtration rate of 75 mL/min/
1.73 m2.12,13 The baseline level of creatinine was the lowest value
recorded during admission for patients with chronic renal insufficiency.
The lower of the lowest creatinine value during hospitalization or
CrMDRD creatinine served as the baseline value for patients
without chronic renal insufficiency. The RIFLE classification was
based on the ratio of the maximum serum creatinine value to the baseline creatinine value (Table 1). Patients were separated into two groups
based on the presence of AKI (RIFLEmax Class R, I, and F) during hospitalization. The duration of ICU and hospital stays, and death while in
hospital were considered as outcomes. The relationship between
RIFLEmax and outcomes was evaluated. The Institutional Ethics
Review Board approved the study protocol.

Statistical analysis
All continuous data are expressed as means + standard deviation and
the mean differences between groups were analysed using Students
t-test or analysis of variance (ANOVA). Proportional differences
were analysed using the Fisher exact analysis. Categorical variables
were analysed using the x2 test. A P-value of less than 0.05 was considered statistically significant. All data were analysed using StatView
5 software for Windows (SAS Institute, Cary, NC, USA), and SPSS
14.0 J for Windows (SPSS Japan Institute, Tokyo, Japan).

Results
Presence of acute kidney injury during
admission
In the 227 patients without chronic renal insufficiency, baseline
creatinine levels were based on the lowest creatinine values in
75 patients and on CrMDRD in 152 patients. We identified AKI
in 125 patients (33%) with ADHF upon admission, but this
increased to 275 patients (73%) during the hospital stay. Acute
kidney injury developed while hospitalized in 150 of the 251
patients (60%) who were free of AKI upon admission (Figure 1).
The RIFLEadm values of the 151 patients with RIFLEmax Class R
were no AKI and RIFLEmax Class R in 104 and 47 patients, respectively. The 70 patients with RIFLEmax Class I were classified upon
admission as having no AKI (n 23), Class R (n 29), and Class
I (n 18). Moreover, of the 54 patients with RIFLEmax Class F,
23, 14, 7, and 10 were evaluated upon admission as having no
AKI, Class R, Class I, and Class F, respectively. Thirty patients
received renal replacement therapy and were evaluated as having
AKI (Class F). Patients were assigned to the AKI (n 275) and
non-AKI (n 101) groups based on their RIFLEmax values.

Characteristics of patients and acute

kidney injury
The relationship between baseline characteristics upon admission
and the presence of AKI during hospitalization is shown in
Table 2. Patients in the AKI group were older (72.5 + 11.5 years;
P 0.0087), more likely to be female (43%; P , 0.0001), and
less likely to have a history of chronic renal insufficiency (18%;
P , 0.0001) than those in the non-AKI group (69.0 + 12.3 years,
female 19%; 57% chronic renal insufficiency). However, the aetiology of heart failure was similar in both groups (Table 2). Clinical

Table 1 Definition of RIFLE classification

Category

Serum creatinine criteria

Urine output criteria

Non-AKI

Maximal increase in serum creatinine ,1.5 baseline

Risk (Class R)
Injury (Class I)

Maximal increase in serum creatinine 1.5 baseline

Maximal increase in serum creatinine 2.0 baseline

,0.5 mL/kg/h for 6 h

,0.5 mL/kg/h for 12 h

Failure (Class F)

Maximal increase in serum creatinine 3.0 baseline or 4 mg/dL with an

acute rise .0.5 mg/dL

,0.3 mL/kg/h for 24 h or anuria for 12 h

...............................................................................................................................................................................
AKI

AKI, acute kidney injury.

34

N. Hata et al.

Figure 1 Acute kidney injury (AKI) was evident in 125 of the 376 patients (33%) with acute exacerbation of heart failure upon admission
(RIFLEadm, upper bar). Acute kidney injury developed during hospitalization in 150 of the 251 patients (60%) without acute kidney injury on
admission. (RIFLEmax, bottom bar).

Table 2 Characteristics of patients according to the presence of acute kidney injury

Non-AKI (n 5 101)

AKI (n 5 275)

P-value

Age (years)
Gender (male/female)

69.0 + 12.3
82/19

72.5 + 11.5
156/119

0.0087
,0.0001
,0.0001

...............................................................................................................................................................................

Chronic renal insufficiency (no/yes)

44/57

183/92

Aetiology
Ischaemic heart disease

35

89

Valvular heart disease

24

89

0.1278

Hypertensive heart disease

Cardiomyopathy

16
23

48
37

0.7593
0.0382

Other

12

0.7677

0.7110

AKI, acute kidney injury.

characteristics upon admission are shown in Table 3; serum creatinine levels, haemodynamics, cardiac rhythm, severity of heart
failure (NYHA and Killip classification), left ventricular ejection
fraction, and serum BNP levels were not significantly different
between the groups.

Acute kidney injury and treatment

The medications and surgical treatments used during hospitalization are shown in Table 4. The administration of inotropic
agents and heart surgery were more frequent in the AKI, than in

the non-AKI group, but no other differences in treatment

methods were evident.

Acute kidney injury and outcomes

The duration of ICU and hospital stays, and the in-hospital mortality of both groups are shown in Table 5. The ICU and hospital
stays were significantly longer for the AKI than for the non-AKI
group (8.8 + 15.4 vs. 5.0 + 2.8 days, P , 0.05 and 48.6 + 47.6
vs. 25.7 + 16.8 days, P , 0.0001, respectively). Twenty-nine of
the 275 patients with AKI died in hospital, whereas only one

35

AKI and outcomes in ADHF

Table 3 Clinical findings on admission

non-AKI (n 5 101)

AKI (n 5 275)

P-value

...............................................................................................................................................................................
Serum creatinine (mg/dL)

1.29 + 0.54

1.33 + 0.79

0.6082

Systolic blood pressure (mmHg)

Diastolic blood pressure (mmHg)

163.1 + 40.0
88.8 + 22.0

155.7 + 44.9
84.7 + 24.8

0.1472
0.1542

Heart rate (b.p.m.)

116.7 + 29.4

113.7 + 32.3

0.4086

Cardiac rhythm
Sinus rhythm

0.7104

67

188

Atrial fibrillation

30

71

0.5117

Ventricular fibrillation
Other

0
4

3
13

0.5671
.0.9999

II
III

17
66

29
172

0.1109
0.6317

IV

18

74

0.0788

NYHA classification

Killip classification
I

13

32

II

41

111

.0.9999

III
IV

40
0

106
9

0.9051
0.1203

No record
LVEF upon admission (%)
BNP upon admission (ng/mL)

0.7230

0.8132

34.3 + 15.3
1001 + 837

36.2 + 16.4
1110 + 1203

0.3343
0.4895

AKI, acute kidney injury; NYHA, New York Heart Association; LVEF, left ventricular ejection fraction; BNP, brain-type natriuretic peptide.

Table 4 Medication and other treatment methods in

acute kidney injury and non-acute kidney injury groups
Total
(n 5 376)

non-AKI
(n 5 101)

AKI
(n 5 275)

P-value

Diureticsa

360 (95.7)

97 (96.0)

263 (95.6)

.0.9999

Vasodilatorsb
Inotropic
agentsc
Temporary
pacing
Ventilator

350 (93.1)
271 (72.1)

91 (90.1)
55 (54.5)

259 (94.2)
178 (64.7)

0.1736
0.0733

12 (3.2)

2 (2.0)

10 (3.6)

0.5267

125 (33.2)

22 (21.8)

103 (37.5)

0.0044

................................................................................

IABP

10 (2.7)

10 (3.6)

0.0682

PCPS

1 (0.2)

1 (0.4)

.0.9999

21 (7.6)

0.0120

Heart surgery

22 (5.9)

1 (1.0)

Number of patients with % in parentheses. AKI, acute kidney injury; IABP,

intra-aortic balloon pump; PCPS, percutaneous cardio-pulmonary support.
a
Included furosemide, canrenoate, and carperitide (recombinant form of human
atrial natriuretic peptide).
b
Included nitrates, nicorandil, and phosphodiesterase inhibitors.
c
Included catecholamines, digitalis, and phosphodiesterase inhibitors.

patient without AKI died. The in-hospital mortality rate was significantly higher in the AKI than in the non-AKI group (10.5 vs.
1.0%. P 0.0010). These outcomes correlated with the RIFLE
criteria and were most significant among Class F of the AKI
group.

Discussion
Definition of acute kidney injury
Several epidemiological studies and clinical trials have used either
simple absolute or relative changes in serum creatinine level as surrogates for changes in kidney function to define acute renal failure.
However, the applicability of serum creatinine levels or other biochemical markers alone is limited.1,14,15 The RIFLE criteria are now
considered the standard method for evaluating AKI in critically ill
patients including those with neurological, cardiovascular, pulmonary, malignant, and gastrointestinal diseases.6,7 In this study, we
evaluated the methodology of the RIFLE criteria in an acutely ill
heart failure population. However, only the creatinine criteria of
the RIFLE classification were evaluated in the present study,
because urine output was influenced by the diuretic therapy administered to the majority of our ADHF patients, and also because
urine output could not be measured in the general wards. Lopes
et al.16 reported that serum creatinine seemed to be a better predictor of mortality than urine output because the former led to a
worse RIFLE class. Patients who had undergone renal replacement
therapy were regarded as RIFLEmax Class F, as described by
Mehta et al.11

Acute kidney injury and critically

ill patients
Acute kidney injury in critically ill patients has been investigated
over the past decade. Donnahoo reported that AKI itself could

36

N. Hata et al.

Table 5 Acute kidney injury and outcome

Cases

ICU stay (days)

Hospital stay (days)

In-hospital death (cases)

Mortality (%)

...............................................................................................................................................................................
Non-AKI group

101

5.0 + 2.8

25.7 + 16.8

1.0

AKI group
RIFLEmax Class R

275
151

8.8 + 15.4*
6.3 + 4.2

48.6 + 47.6
37.5 + 20.4

29
0

10.5
0.0

RIFLEmax class I

70

6.4 + 3.4

49.1 + 33.1

4.3

RIFLEmax Class F

54

19.1 + 32.5

79.7 + 88.9

26

49.1

ICU, intensive care unit; AKI, acute kidney injury; R, risk; I, injury; F, failure.
*P , 0.05.

P , 0.0001.

P 0.0010 or P , 0.01.

lead to a non-infectious, proinflammatory response with leucocyte

activation, proinflammatory cytokine secretion and the recruitment of neutrophils and macrophages with resultant lung injury,
as has been demonstrated in animal models of ischaemia
reperfusion-induced acute renal failure.17 Acute kidney injury is
frequently encountered in critically ill patients and characteristically
leads to an increase in morbidity and mortality. Acute renal failure
severe enough to require renal replacement therapy develops in
5% of general ICU patients.2 Although Hoste et al.3 reported
that AKI evaluated by the RIFLE criteria is associated with outcomes in critically ill patients, the relationship between AKI
defined according to the RIFLE criteria and outcomes of patients
with heart failure have not previously been evaluated in detail.
Bagshaw et al.18 investigated the clinical applicability of the RIFLE
criteria in a large heterogeneous cohort of critically ill patients
admitted to the ICU and found that these criteria represent a
simple tool for the detection and classification of AKI and for correlation with clinical outcomes. They considered that 72% of
patients with acute exacerbation of heart failure had AKI during
hospitalization and concluded that the RIFLE classification is significantly related to outcomes including ICU stay, hospital stay, and
in-hospital mortality. Other investigators have reported a relationship between AKI and outcome following sepsis,19 stroke,20 and
cardiothoracic surgery.21 Uchino et al.22 reported that the RIFLE
criteria for acute renal failure classified 20% of study patients
admitted to general wards and the ICU as having some degree
of acute impaired renal function and that such classification was
useful in predicting hospital mortality.

Acute kidney injury and cardiovascular

diseases
Lee et al.23 found that a higher BUN and lower SBP were significant
and independent predictors of both 30-day and 1-year mortality
rates in the Enhanced Feedback for Effective Cardiac Treatment
(EFFECT) study. De Luca et al.24 found that the assessment of
blood pressure and renal function are essential for stratifying
patients presenting with acute heart failure. Fonarow et al.4
reported that BUN, SBP, and creatinine levels were the three variables most predictive of in-hospital mortality in the Acute Decompensated Heart Failure National Registry (ADHERE) and
Gheorghiade et al.5 found that multiple evaluations demonstrated
the prognostic value of SBP and indices of renal function in acute

heart failure syndromes. Silverberg reported that about half of all

patients with congestive heart failure have chronic kidney
disease, whereas congestive heart failure is 15 times more frequent in patients with chronic kidney disease than in those with
normal renal function.25 He also stated that congestive heart
failure exacerbates nephropathy, whereas chronic kidney disease
is associated with accelerated atherosclerosis, microvessel
disease, endothelial dysfunction, increased sympathetic activity,
and cardiac pathology.25 Lassnigg et al.21 reported that small
changes in serum creatinine are associated with a worse
outcome for patients after cardiothoracic surgery. However, the
definition of AKI was not standardized in these studies, and therefore the present study investigated the clinical applicability of the
RIFLE criteria to the evaluation of AKI in patients with ADHF.
Acute kidney injury evaluated by the RIFLE criteria correlated
with poor ADHF outcomes. This is the first report to describe
the clinical value of the RIFLE criteria, in terms of the relationship
between AKI evaluated by the RIFLE criteria and outcomes in
patients with ADHF.
The incidence of mortality and adverse events after AMI is high
in patients with severe and end-stage renal disease.26,27 We therefore excluded patients with heart failure after acute cardiac diseases such as AMI and acute myocarditis from this study,
because contrast-induced nephropathy frequently arises in such
patients and it is also associated with prolonged hospitalization
and adverse clinical outcomes after coronary angiography and/or
percutaneous coronary intervention.28,29

Study limitations
The ratio of the maximum serum creatinine to baseline creatinine
was underestimated in patients with chronic renal insufficiency due
to high baseline creatinine values. The time course of changes in
the occurrence of AKI was not precisely evaluated. A multi-centre
study should be performed to evaluate the influence of medications administered during the hospital admission. The RIFLE
classification could not be evaluated quickly in our study, therefore
further studies should investigate its ability to predict AKI occurrence at an earlier stage of hospitalization. Although, the RIFLE criteria are clear and easy to understand, they are nevertheless
complex and labour-intensive to calculate and are therefore
mostly used in retrospective evaluations. Colpaert et al.30 stated
that using an electronic alert based on the RIFLE criteria, which

AKI and outcomes in ADHF

warned the physician in real-time when kidney function is deteriorating, could help to implement these criteria in routine clinical
practice. These authors are currently investigating whether the
implementation of real-time electronic RIFLE alerts can induce
faster therapeutic intervention and are also evaluating the impact
of more timely interventions on the preservation of kidney function and patient outcome. Although no precise resolution of
poor outcomes in ADHF patients with AKI was identified from
this study, use of cardio-renal protective medicines and early
initiation of renal replacement therapy should be recommended
for these patients.
In conclusion, a third of patients with ADHF had AKI upon
admission, but AKI also occurred in 60% of ADHF patients
during hospitalization who did not have AKI at the time of admission. The presence of AKI during hospitalization was associated
with poor outcomes in patients with ADHF, as has been reported
in patients with other critical illnesses. The RIFLE criteria should be
developed into a clinically available and standardized method for
evaluating AKI.

Acknowledgements
We are grateful to the staff of the intensive care unit and the
medical records office in Chiba Hokusoh Hospital, Nippon
Medical School, for collecting the medical data.
Conflict of interest: none declared.

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