RES E AR C H A R T I C L E Open Access
The effect of the time interval between coronary
angiography and on-pump cardiac surgery on
risk of postoperative acute kidney injury:
Yijie Hu, Zhiping Li, Jianming Chen, Cheng Shen, Yi Song and Qianjin Zhong
Background: Reports of the association between the time interval from coronary angiography (CAG) to cardiac
surgery and risk of postoperative acute kidney injury (AKI) are controversial. We attempted to examine this
association by conducting a meta-analysis.
Methods: We searched the Pubmed, MEDLINE, EMBASE, Web of Science databases, and the Cochrane Library from
January 1966 to March 2013. A meta-analysis of studies reporting data for 1-day and 3-day time intervals between
CAG and cardiac surgery was conducted after evaluation of heterogeneity and publication bias. Study-specific
estimates were combined with inverse variance-weighted averages of logarithmic odds ratios (ORs) in fixed-effects
Results: From 8 studies involving 11542 persons, the pooled OR of AKI associated with an interval of 1 day or less
between CAG and surgery was 1.21 (95% confidence interval (CI), 1.04 to 1.39) relative to an interval of more than
1 day. From 4 studies involving 5420 persons in the cardiopulmonary-bypass subgroup, the pooled OR of AKI
associated with an interval of 3 days or less between CAG and surgery was 1.25 (95% CI, 1.07 to 1.43) relative to an
interval of more than 3 days. The adjusted OR of the study in the cardiopulmonary bypass/ deep hypothermic
circulatory arrest subgroup was 0.35 (95% CI, 0.17 to 0.73).
Conclusions: A time interval of 1 day or less between CAG and on-pump cardiac surgery was significantly
associated with increased risk of AKI. A delay of on-pump cardiac surgery until 24 hours after CAG can potentially
decrease postoperative AKI.
Keywords: Acute kidney injury, Coronary angiography, Cardiac surgery
Postoperative acute kidney injury (AKI) is one of the
most serious and frequent complications of cardiac
surger y. Previous studies have demonstrated that even
small increases in serum cre atinine following cardiac
surgery are independently a ssociated with increased
mortality and longer hospitalization [1-3]. As no
causal therapy f or AKI is currently available, every
Lately it has become common practice to provide
same admission  or even one-stage diagnostic coron-
ary angiography (CAG) and surgical services for patients
undergoing cardiovascular surgery. The types of surgeries
mainly include coronary artery bypass grafting (CABG),
aortic surgery, and valve surgery. AKI is reported to occur
in up to 30% of patients after on-pump cardiac surgery
[6,7], while contrast-induced nephropathy after CAG
occurs in up to 10% of patients with normal renal func-
tion and up to 25% of patients with pre-existing renal
impairment . Hence, many studies have dealt with
the question of whether the closely spaced “double hit”
on renal function increases the risk of postoperative
* Correspondence: firstname.lastname@example.org
Department of Cardiovascular Surgery, Institute of Surgery Research, Daping
Hospital, Third Military Medical University, No. 10 Changjiang Zhi Road,
Yuzhong District, Chongqing 400042, China
© 2013 Hu et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly cited.
Hu et al. Journal of Cardiothoracic Surgery 2013, 8:178
AKI. Conflicting data have been reported. Some authors
claimed that the risk of AKI after cardiac surgery is not
influenced by the time interval between angiography and
cardiac surgery [9-13]. Conversely, other authors empha-
sized the deleterious effect of performing both procedures
in close succession [14-17].
In view of the limited clarity of the available data, we
conducted a systematic review of the literature and a
meta-analysis of selected studies to evaluate the effect of
the time interval between CAG and cardiac surgery on
risk of postoperative AKI.
The keywords used to search included the following:
“cardiac surgery or CABG or valve surgery or aortic sur-
gery” and “catheterization or angiography or percutan-
eous coronary intervention” and "acute kidney injury or
AKI or renal failure." A computerized search of the
Pubmed, MEDLINE, EMBASE, Web of Science data-
bases, and the Cochrane Library from January 1966 to
March 20 13 was undertaken to identify potentially eli-
gible studies on the basis of the title, abstract, and key-
words; no language limitation was applied. Then, the full
content of each article was examined to decide which
studies met the inclusion and exclusion criteria men-
tioned in the next section. The reference lists from all
studies, narrative reviews, and systematic reviews identi-
fied by electronic searches were manually searched to
identify additional eligible studies. Two authors (Yijie
Hu and Zhiping Li) independently performed the eligi-
bility assessments; if opinion s differed, the differences
were resolved by consensus.
Inclusion and exclusion criteria
Included studies met the following criteria: (1) the study
focused on the risk of AKI and the time interval between
angiography and cardiac surgery; (2) the study was a
randomized controlled trial, case-control, or cohort
study; (3) the study either provided risk estimates with
the odds ratio (OR), and 95% confidence interval (95%
CI), or suffic ient information was available to calculate
the OR and 95% CI.
A study was excluded from the meta-analysis if (1) it
only provided an effect estimate but no means to calcu-
late a 95% CI; (2) it did not provide an accurate defin-
ition of AKI; (3) it did not provide an accurate time
interval; (4) off-pump heart surgery was performed, but
the combined AKI risk due to contrast media and car-
diopulmonary bypass (CPB) could not be evaluated; or
(5) it was a low-quality study. In the case of multiple
studies with the same or overlapping data published by
the same researchers, we selected the most recent study
with the largest number of participants.
For each study, two authors (Yijie Hu and Yi Song)
extracted the following data: the first author’s surname,
country the study was conducted in, year reported, study
design, sample size, primary operation, definition of
AKI, effect estimate (95% CI), and adjusted covariates.
If the effect estimate could be acquired from the
searched results of the tabulated literature, they were
extracted carefully from all eligible publications, which
met the inclusion criteria. If data were not directly avail-
able, they were calculated from the published positive
predictive values and/or the negative predictive values
when appropriate. If a study contained unclear or in-
complete information, the reviewers contacted the ori-
ginal authors for verification. Differences in data
extraction were resolved by a third reviewer, referring
back to the original article.
We applied the Newcastle-Ottawa scale (NOS)  to
evaluate the qualities of the included studies. A “star sys-
tem” was used to judge the data quality of these studies
on the basis of three broad categories: the selection, the
comparability, and the outcome or exposure of interest.
The stars were summed to compare the quality of a
study in a quantitative fashion. The scores ranged from
0 to 9 stars. Studies with scores of 6 stars or greater
were considered to be of high quality studies. Two re-
viewers (Yijie Hu and Yi Song) independently evaluated
and cross-checked the qualities of the included studies,
and assessed the bias of the studies. An open discussion
was held to confirm the scores of those studies that re-
ceived a different score from each reviewer.
For each study, data regarding the incidence of AKI were
used to generate ORs and 95% CI; or the adjusted ORs
and 95% CI were extracted directly. According to time
intervals reported in the literature, two meta-analyses
were conducted: one analysis for interval of 1 day or
less (the <1-day group), and one analysis for interval of
3 days or less ( the <3-day group). Among the studies of
each group, AKI was mainly induced by contrast and
ischemia-reperfusion injury after cardiopulmonary by-
pass, with the exception of the only study that used deep
hypothermic circulatory arrest (DHCA), which we
reported separately. All studies included in the subgroup
analysis are functionally identical, and the effect size in
our meta-analysis differ mainly because of sampling
error. Accordingly the pooled OR estimates were com-
bined by using inverse variance-weighted averages of
logarithmic ORs in a fixed-effe cts model (the Mantel–
Haenszel method). Heterogeneity among studies was de-
termined by the chi-square-based Q test and the I
Hu et al. Journal of Cardiothoracic Surgery 2013, 8:178 Page 2 of 7
statistics. A P value of less than .05 for the Q test and
value of greater than 50% were considered as a
measure of severe heterogeneity. A funnel plot was
constructed to determine if publication bias existed and
to examine differences between the effects in large and
small studies; the studies were also assessed by applying
Egger’s weighted regression test. The Egger’s test was
also applied to assess less than 6 studies, with a P value
of < 0.05 indicating significant publication bia s among
the included studies. The effects sizes, given as the OR
on a logarithmic scale, were plotted against a measure of
precision expressed as the inverse standard error. All
statistical analyses were performed by using Stata Statis-
tical Software (Version 11.0; StataCorp LP, Texas, USA).
Description of the studies
As outlined in Figure 1, we identified 9 studies for the
meta-analysis, including 5 cohort studies and 4 case-
control studies. Detailed characteristics of the studies
are listed in Table 1. Among the 9 stud ies, 5 studies used
the AKI Network definition of AKI , an absolute in-
crease in serum creatinine to ≥0.3 mg/dL, or a relative
increase of ≥50% from the baseline value within 48 h
after surgery, or a requirement for postoperative dialysis;
3 studies defined AKI on the basis of the RIFLE (Risk,
Injury, Failure, Loss , End-stage renal disease) criteria
 (“R” stage: plasma creatinine levels ≥1.5 × baseline;
“I” stage: plasma creatinine levels ≥2.0 × baseline); and 1
study defined AKI as a greater tha n 25% rise in serum
creatinine by the third postoperative day or as renal dys-
function that required the initiation of dialysis. Quality
assessment of all studies was performed by using the
NOS method (Table 2). The assessments ranged from a
star rating of 6 to 8 (mean star rating, 7) with a higher
value indicating better methodology.
There were 8 studies of a 1-day time interval between
CAG and cardiac surgery, and 5 studies of a 3-day time
Meta-analysis of studies reporting data for a 1-day time
interval between CAG and cardiac surgery
Four of the 8 individual studies demonstrated a statisti-
cally significant effect of a ≤ 1-day time interval on the
incidence of AKI. Pooled analysis of the 8 studies re-
vealed a significant increase in AKI risk by a factor of
1.21 with a ≤1-day time interval relative to >1 day
in fixed-effect s models (Figure 2). There was minimal
trial heterogeneity (I
= 24.0%, P = 0.238). Assessment
of publication bias by visual examination of the funnel
plot (Figure 3) and by application of Egger’s weighted
regression test (P = 0.102) indicated no significant publi-
Meta-analysis of studies reporting data for a 3-day time
interval between CAG and cardiac surgery
The 5 studies of a 3-day time interval exhibite d severe
= 86.7%, P < 0.01). After comparing the
basic and clinical characteristics of the 5 studies, we di-
vided them into two subgroups: one (the CPB subgroup)
included 4 studies that did not use deep hypothermic
circulatory arrest (DHCA), which is a significant risk fac-
tor of AKI [23,24]; and the other (the CPB/DHCA sub-
group) included only one study that did use DHCA.
Meta-regression was not further performed due to the
limited number of available studies.
In the CPB subgroup, only 1 of the 4 studies demon-
strated a statistically significant effect of a ≤ 3-day time
interval between CAG and cardiac surgery on the inc i-
dence of AKI. Pooled analysis of the 4 studies revealed a
significant increase in AKI risk, by a factor of 1.25, with
a ≤ 3-day time interval relative to > 3 days in fixed-effects
models (Figure 4). The 4 studies of this subgroup
exhibited no heterogeneity (I
= 0%, P = 0.682). In
addition, Egger’s test revealed no e vidence of significant
publication bias (P = 0.295).
The study in the CPB/DHCA subgroup showed no
significant difference in AKI risk between a 3-day time
interval and an interval of more than 3 days, with an ad-
justed OR of 0.35 (95% CI, 0.17-0.73; P = 0.005).
This meta-analysis is the first to evaluate the impact of
the time interval between CAG and cardiac surgery on
postoperative AKI incidence. Our results suggest that a
≤1-day time interval significantly increases postoperative
AKI. This review provides important evidence that may
resolve the ongoing controversy arising from previous
Figure 1 Flow diagram of study selection for the meta-analysis.
AKI = acute kidney injury; CAG = coronary angiography.
Hu et al. Journal of Cardiothoracic Surgery 2013, 8:178 Page 3 of 7
studies. For instance, Ko et al published a series of 2133
consecutive patients who underwent cardiac surgery but
found no association between the time interval from
angiography to surgery and the incidence of postopera-
tive AKI . Conversely, Ranucci et al recently reported
that surgery on the same day as angiography signifi-
cantly increases the risk of AKI, after risk-adjustment in
a total of 4440 consecutive patients ; these results
closely resemble those of the present meta-analysis. The
validity of these results supports the idea that the
Table 1 Main characteristics of 9 included studies
Study Year Country Type of study Sample size Main operation Definition
Ranucci  2013 USA Cohort 4440 CABG A 21.7% Age, EF, MI, congestive heart failure,
previous operation, urgent operation,
creatinine, CPB duration, nadir HCT
Ko  2012 USA Cohort 2133 CABG A 32.0% None
Mcllroy  2012 USA Cohort 644 CABG A 21.9% Age, BMI, CPB duration, procedure
type, N-acetylcysteine administration,
Greason  2012 USA Cohort 642 AVR A 22.7% None
Andersen  2012 USA Case-control 285 Aorta replacement B (R) 31.0% Age, sex, BMI, eGFR, hypertension,
CHF, diabetes, CPB duration, EF,
hemoglobin, aprotinin exposure
Mehta  2011 USA Case-control 2441 CABG A 17.1% Age, sex, race, BMI, diabetes, CHF, MI,
EF, hypertension, contrast volume and
type, cardiogenic shock, cross-clamp
time, creatinine, hemoglobin
Medalion  2010 Israel Case-control 395 CABG B (R) 13.6% None
Hennessy  2010 USA Cohort 197 Valve Surgery B (I) 6.6% None
Del Duca  2007 Canada Case-control 649 CABG C 24.0% Age, CPB duration, baseline GFR
A: defined by the AKI network: absolute increase of ≥ 0.3 mg/dL or a relative increase of ≥ 50% in serum creatinine from baseline value within 48 h after surgery,
or a requirement for postoperative dialysis.
B: defined by the Risk, Injury, Failure, Loss, End-stage renal disease (RIFLE) criteria for acute renal failure, which are based on differences betwe en the baseline and
peak postoperative serum creatinine levels (“R” stage: plasma creatinine level ≥ 1.5 × baseline; “I” stage: plasma creatinine level ≥ 2.0 × baseline).
C: defined as a rise in serum creatinine of greater than 25% by the third postoperative day or renal dysfunction that requ ires the initiation of dialysis.
Abbreviations, AKI acute kidney injury, AVR aortic valve replacement, BMI body mass index; CABG coronary artery bypass grafting, CHF congestive heart failure, CPB
cardiopulmonary bypass, DHCA deep hypothermic circulatory arrest, EF ejection fraction, eGFR estimated glomerular filtration rate, GFR glomerular filtration rate,
HCT hematocrit, IMA internal mammary artery, MI myocardial infarction.
Table 2 Assessment of study quality
Study Quality indicators from the Newcastle-Ottawa scale Score
Selection Comparability Exposure/Outcome
1234 5a 5b 6 7 8
Ranucci  Yes Yes No Yes No No Yes Yes Yes 6
Ko  Yes Yes No Yes No No Yes Yes Yes 6
Mcllroy  Yes Yes No Yes Yes Yes Yes Yes Yes 8
Greason  Yes No No Yes Yes Yes Yes Yes Yes 7
Andersen  Yes Yes No Yes No Yes Yes Yes Yes 7
Mehta  Yes Yes No Yes Yes Yes Yes Yes Yes 8
Medalion  Yes Yes No Yes Yes No Yes Yes Yes 7
Hennessy  Yes No No Yes Yes Yes Yes Yes Yes 7
Del Duca  No Yes No No Yes Yes Yes Yes Yes 6
Hu et al. Journal of Cardiothoracic Surgery 2013, 8:178 Page 4 of 7
incidence of postoperative AKI can be contained by lim-
iting the practice of performing cardiac surgery on the
same day as angiography .
The 5 studies of a 3-day time interval that were in-
cluded in this meta-analysis exhibited severe heterogen-
eity. After considering the obvious difference of the use
of DHCA, a risk factor of AKI [23,24], we divided the
studies into to two subgroups: the CPB subgroup, in-
cluded 4 studies; and the CPB/DHCA subgroup, only 1.
Once we removed the study that used DHCA, the het-
erogeneity of the CPB subgroup disappeared.
Analysis of the CPB subgroup determined that a time
interval of 3 days or less between CAG and cardiac sur-
gery significantly increases postoperative AKI. This time
interval includes surgeries performed 1, 2, and 3 days
after CAG. Without consideration of the effect of a time
interval of 1 day or less , it is difficult to evaluate the ef-
fect of 2-day and 3-day time intervals on the incidence
of postope rative AKI. In fact, the pooled effect is largely
based on data on the incidence of AKI from 2 studies,
which contributed to more than 90% of the total weight.
In the cohort study by Ko et al, the number of days
Figure 2 Forest plot for time interval, ≤1-day vs >1 day. The estimated odds ratio (OR) of each individual article corresponds to the middle
of the squares, and the horizontal line gives the 95% confidence interval (CI). The sum of the statistics along with the summary
OR is represented by the middle of the solid diamonds. The heterogeneity test statistic (I statistic) between articles is given below the
Figure 3 Funnel plot for studies of a 1-day time interval.
Hu et al. Journal of Cardiothoracic Surgery 2013, 8:178 Page 5 of 7
between CAG and cardiac surgery was not a predictor
of postoperative AKI after the data were adjusted for
confounding factors (OR, 0.99; 95% CI, 0.99 - 1.00; P =
0.41) . In the study by Mehta et al, cardiac surgeries
performed 2 days and 3 days after CAG were not associ-
ated with an increased risk of AKI when compa red with
those performed later (OR, 1.26; 95% CI, 0.94 – 1.74;
and OR, 1.11; 95% CI, 0.77 – 1.59) . Accordingly, the
significant association between a time interval of 3 days
or less and increased risk of AKI may have resulted from
inclusion of data from a time interval of 1 day or less,
not from inclusion of data from 2-day or 3-day time
The lack of associat ion between CAG on preoperative
days 1 through 3 and increased risk of AKI in the one
study of the CPB/DHCA subgroup seems controversial,
given that the pooled effect of the CPB subgroup did
show a significant association (adjusted OR, 0.35; 95%
CI, 0.17-0.73; P = 0.005) . However, the CPB/DHCA
subgroup had a much more higher incidence of AKI,
about 31% if defined by the RIFLE criteria, while, the
highest incidence of the other studies was only 18% if
defined by the RIFLE criteria, or 32% if defined by the
AKI network criteria . W e interpret this to mean that
DHCA plays an important role in postoperative AKI.
Moreover, the inc reased risk of AKI due to DHCA
would probably “dilute” the difference between any
CPB/DHCA subgroups containing stud ies that report
data from different time intervals.
Our review has several limitations that must be con-
sidered for accurate interpretation of the reported ef-
fect s. First, this observational meta-analysis was based
on a limited number of cohort and case-control studies
and was short of randomized trials and a large scale of
comprehensive clinical trials. Accordingly, the potential
confounding factors such as age, mellitus diabetes, type
of disease, type or complexity of the operation, bypass
time and the use of DHCA were unequally distributed .
The impact of this bias on the estimated effects
presented in this review is unknown, even after adjust-
ment. To address this issue, the methods we used to se-
lect studies and analyze pooled data were in accordance
with the MOOSE guideline  and current recommen-
dations for meta-analysis of observational trials. Add-
itionally, we used a funnel plot analysis and Eggers'
test to exclude publication bias. Secondly, this review
was limited by the use of different definitions of AKI,
although Haase et al reported tha t the incidence of post-
operative AKI in patients with cardiac surgery was simi-
lar when AKI was defined according to either the RIFLE
or the AKI Network classification . We attempted to
mitigate this bias to some extent by adopting OR as the
summary statistic. Lastly, our review did not account for
differences in study quality, since the rating of methodo-
logical qua lity was “goo d ” for all included studies.
The results of this meta-analysis strongly support an as-
sociation between a ≤ 1-day time interval from CAG to
cardiac surgery and increased risk of AKI. The similar
association between a day time interval of 3 days or less
and risk of AKI probably resulted from inclusion of data
from an interval of a day or less. We propose that the
delay of cardiac surgery until 24 hours after C AG can
potentially decrease postoperative AKI. In the future it
will be necessary to evaluate the risk of a short time
interval between CAG and cardiac surgery in a random-
ized trial, and clarify the other AKI risk factors in the
setting of a short interval between CAG and cardiac
surgery. This would help to adjust the estimation of
Figure 4 Forest plot for time interval, ≤3-day vs >3 days, in CPB subgroup. The estimated odds ratio (OR) of each individual article
corresponds to the middle of the squares, and the horizontal line gives the 95% confidence interval (CI).The sum of the statistics along with the
summary OR is represented by the middle of the solid diamonds. The heterogeneity test statistic (I statistic) between articles is given below the
Hu et al. Journal of Cardiothoracic Surgery 2013, 8:178 Page 6 of 7
appropriate individual risk and to optimize the flow of
treatment in patients who require diagnostic preopera-
tive coronary angiography.
CAG: Coronary angiography; AKI: Acute kidney injury; ORs: Odds ratios;
CI: Confidence interval; CABG: Coronary artery bypass grafting;
CPB: Cardiopulmonary bypass; DHCA: Deep hypothermic circulatory arrest.
The authors declare that they have no competing interests.
ZQ and HY designed the study. HY and LZ carried out studies searching and
performed the eligibility assessments. HY and SY evaluated the qualities of
the included studies and carried out data extracting. ZQ, CJ, LZ and SC
analyzed and interpreted the data. HY drafted the manuscript. ZQ, LZ, CJ and
SC made critical revision of the manuscript for important intellectual content.
All authors read and approved the final manuscript.
We thank Yao Zhang, associated professor of Department of Epidemiology,
Clinic Epidemiology Center, Third Military Medical University, for help on
Received: 18 June 2013 Accepted: 1 August 2013
Published: 3 August 2013
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Cite this article as: Hu et al.: The effect of the time interval between
coronary angiography and on-pump cardiac surgery on risk of
postoperative acute kidney injury: a meta-analysis. Journal of
Cardiothoracic Surgery 2013 8:178.
Hu et al. Journal of Cardiothoracic Surgery 2013, 8:178 Page 7 of 7