Carátula del artículo
The Effect of Female Sex on Short-Term Outcomes of Patients
Undergoing Off-Pump Versus On-Pump Coronary Artery Bypass
Grafting
South China University of
Technology, People’s Republic of China
South China University of
Technology, People’s Republic of China
South China University of
Technology, People’s Republic of China
Tian-yuan Wu
South China University of
Technology, People’s Republic of China
Yu Chen
South China University of
Technology, People’s Republic of China
Wei-jie Li eylwj@scut.edu.cn
South China University of
Technology, People’s Republic of China
Brazilian Journal of Cardiovascular Surgery, vol. 38, no. 1, pp. 110-123, 2023
Sociedade Brasileira de Cirurgia Cardiovascular
Received: 13 May 2021
Accepted: 07 January 2022
INTRODUCTION
Coronary artery disease (CAD) is the leading cause of death in both developed and
developing countries[1]. The
mortality and quality of life of CAD patients have been significantly improved by
the effective application of primary[2] and secondary prevention[3]. Clinical trials have shown that improving the management
of hypertension[4], diabetes
mellitus[5], and
hyperlipidemia[6] promoted
better clinical outcomes in CAD patients. However, several risks factors affecting
the outcomes of CAD patients remain unclear[7].
Coronary artery bypass grafting (CABG) is a treatment strategy for coronary artery
revascularization. According to the American Heart Association CABG guideline, the
female sex is a risk factor for adverse outcomes[8]. In Kim et al.[9] meta-analysis involving 23 studies, early mortality and
complications were higher among females after CABG than among males. However, this
conclusion was based on the studies of on-pump CABG (ONCAB) or studies not
stratified based on the cardiopulmonary bypass technique used.
In the CABG Off or On Pump Revascularization Study[10] (CORONARY) and the Randomized On/Off Bypass
trial[11] (ROOBY), there
was no significant difference between off-pump CABG (OPCAB) and ONCAB in the 30-day
mortality rate. In addition, there was no significant difference in the occurrence
of myocardial infarction (MI), stroke, or renal failure requiring dialysis between
OPCAB and ONCAB groups in the CORONARY study[10]. However, to this date, there are no reports concerning
the influence of sex difference on the outcomes of OPCAB vs. ONCAB
clinically.
The study by Attaran et al.[12] was
the first meta-analysis that compared the short-term outcomes between off-pump
vs. on-pump revascularization among female patients. In this
study, no statistically significant difference was observed in the 30-day mortality
rate and other morbidity outcomes between the OPCAB and ONCAB groups, except for
perioperative MI. Recently, several new studies in this field, including the
propensity score matching (PSM) study[13] and studies that were adjusted for cardiovascular risk
factors[13,14], have been published. This study aims to
investigate the latest research to study the effect of the female sex on short-term
outcomes in OPCAB vs. ONCAB patients.
METHODS
Since this study is a systematic review and meta-analysis based on previous articles,
ethics committee approval was not required; it was conducted in accordance with the
Helsinki Declaration of 1975 (revised in the year 2000). This is an observational
meta-analysis that followed the guidelines for the Meta-analysis of Observational
Studies in Epidemiology. This study has been registered on PROSPERO
(CRD42021250888). We searched literature databases including PubMed®, Web of
Science™, Embase®, Scopus™, Ovid, the China National Knowledge Infrastructure (or
CNKI), the Chinese Biomedical Literature service system (or SinoMed), and the
Wanfang Data Knowledge Service Platform with the keywords “coronary artery bypass”,
“female”, “women”, “woman”, “gender”, and “sex”. We did not limit the start time of
the studies, but we limited their end time to 2021-8-1, when retrieving the
literature. After this strategy, 4,358 pieces of literature were retrieved. LSL and
PYC carefully read and analyzed all the retrieved studies, and the publications were
further screened according to the flow chart shown in Figure 1. Finally, 12 retrospective observational studies were included
in our meta-analysis. Of the 12 studies, two were PSM studies.
Fig. 1
Flow diagram describing study selection in our meta-analysis.
CABG=coronary artery bypass grafting; CNKI=China National Knowledge
Infrastructure; SinoMed=Chinese biomedical literature service
system
We included two main types of studies in our meta-analysis: 1) studies which only
included female patients grouped by OPCAB and ONCAB and 2) studies which included
male and female patients undergoing CABG (OPCAB and ONCAB), but containing a clear
delineation between OPCAB and ONCAB subgroups. Both types of studies must also
possess documented primary and secondary endpoints.
Primary endpoints included in-hospital death, 30-day death rate after surgery,
postoperative MI, and stroke. Secondary endpoints included postoperative acute renal
failure (ARF), renal replacement therapy, blood transfusion, reoperation for
bleeding, sternal wound infection, atrial fibrillation, and postoperative lower
cardiac output.
The selected literature was not restricted by language. Abstracts, conference
abstracts, and supplementary issues were also included. Patients who underwent
concomitant surgical procedures such as valvular repair or replacement, correction
of congenital malformation, and ascending aortic aneurysm repair, to name a few,
were excluded from this study. FJ and PYC analyzed the data extracted from these
studies. A consensus was reached through discussion in cases of disagreements.
Extraction of Data
LWJ and FJ extracted data from the selected literature, including the first
author’s name, the year when the study was published, the type of research, and
the country where the study was conducted. General characteristics such as age,
race, body mass index, and smoking status were recorded. Preoperative diseases
including hypertension, diabetes, hyperlipidemia, heart failure, stroke, and
peripheral vascular disease were included. Patients’ echocardiographic
measurement parameters, such as left ventricular ejection fraction, were also
collected. Primary and secondary endpoints were collected for investigation. The
quality of the studies was evaluated according to the Newcastle-Ottawa Scale (or
NOS).
Statistical Analysis
RevMan 5.4 (Nordic Cochrane Center) statistical software was employed for
meta-analysis. A P-value of < 0.05 was considered
statistically significant. Publication bias was assessed using visual inspection
of funnel plots. All included studies were retrospective in nature. A
random-effects model was adopted in this study to avoid the impact of
inter-study heterogeneity on the results.
RESULTS
Literature Retrieval
We searched the literature database as abovementioned; 4,358 scientific works
were retrieved after preliminary screening. We then further screened the
literature according to the strategy in Figure
1. Ultimately, 12 studies were included in our meta-analysis. All
studies were retrospective observational studies. Primary and secondary
endpoints were extracted for analysis.
Characteristics of the Included Studies
The 12 studies included were observational, three reports were from the United
States of America[13,15-18], and the remaining were clinical studies from
Germany[19-21], Netherlands[14,22], Portugal[23], Poland[24-27], and
Canada[28,29]. The detailed characteristics
of the included patients and quality assessment are shown in Table 1. We investigated in-hospital
mortality rate (Figure 2), 30-day hospital
mortality rate (Figure 3), myocardial
infarction incidence (Figure 4), stroke
incidence (Figure 5), incidence of red
blood cell transfusion and re-exploration for bleeding (Supplementary Figure 1), acute renal failure and renal
replacement therapy (Supplementary Figure
2), deep wound infection (Supplementary
Figure 3A), atrial fibrillation (Supplementary Figure 3B), and postoperative lower cardiac output
(Supplementary Figure 3C) among female
patients received ONCAB or OPCAB. A funnel plot is shown in Supplementary Figures 4-8.
Table 1
Characteristics of the included studies.
* Newcastle-Ottawa quality assessment scale for cohort studies
Fig. 2
Forest plots demonstrating in-hospital mortality of off-pump
coronary artery bypass grafting (OPCAB) vs. on-pump coronary
artery bypass grafting (ONCAB) for (a) original data without
adjustment, (b) in-hospital mortality with cardiovascular risk
factor adjustment, (c) in-hospital mortality of propensity score
matching studies. Chi=Chi-squared; CI=confidence interval;
df=degree of freedom; IV=inverse variance; M-H=Mantel-Haenszel;
SE=standard error; Tau=Tau-squared
Fig. 3
Forest plot demonstrating the 30-day hospital mortality rate
of off-pump coronary artery bypass grafting (OPCAB) vs. on-pump
coronary artery bypass grafting (ONCAB). Chi=Chi-squared;
CI=confidence interval; df=degree of freedom;
M-H=Mantel-Haenszel; Tau=Tau-squared
Fig. 4
Forest plot demonstrating postoperative myocardial
infarction incidence of off-pump coronary artery bypass grafting
(OPCAB) vs. on-pump coronary artery bypass grafting (ONCAB).
Chi=Chi-squared; CI=confidence interval; df=degree of freedom;
M-H=Mantel-Haenszel; Tau=Tau-squared
Fig. 5
Forest plots demonstrating postoperative stroke incidence of
off-pump coronary artery bypass grafting (OPCAB) vs. on-pump
coronary artery bypass grafting (ONCAB) for (a) original data
without adjustment, (b) stroke with cardiovascular risk factor
adjustment, (c) stroke of propensity score matching studies.
Chi=Chi-squared; CI=confidence interval; df=degree of freedom;
IV=inverse variance; M-H=Maentel-Haenszel; SE=standard error;
Tau=Tau-squared
Supplementary Fig. 1
Forest plots demonstrating off-pump coronary artery bypass
grafting (OPCAB) vs. on-pump coronary artery bypass grafting
(ONCAB) incidence of (a) blood cell transfusion, (b)
re-exploration for bleeding, (c) re-exploration for bleeding of
propensity score matching (PSM) studies. Chi=Chi-squared;
CI=confidence interval; df=degree of freedom;
M-H=Mantel-Haenszel; Tau=Tau-squared
Supplementary Fig. 2
Forest plots demonstrating off-pump coronary artery bypass
grafting (OPCAB) vs. on-pump coronary artery bypass grafting
(ONCAB) incidence of (a) acute renal failure, (b) acute renal
failure with cardiovascular risk factor adjustment, (c) renal
replacement therapy. aOR=adjusted odds ratio; Chi=Chi-squared;
CI=confidence interval; IV=inverse variance; df=degree of
freedom; M-H=Mantel-Haenszel; SE=standard error;
Tau=Tau-squared
Supplementary Fig. 3
Forest plots demonstrating off-pump coronary artery bypass
grafting (OPCAB) vs. on-pump coronary artery bypass grafting
(ONCAB) incidence of (a) deep sternal wound infection, (b)
atrial fibrillation (AF), (c) postoperative lower cardiac
output. Chi=Chi-squared; CI=confidence interval; df=degree of
freedom; M-H=Mantel-Haenszel; Tau=Tau-squared
Supplementary Fig. 4
Funnel plot of off-pump coronary artery bypass grafting vs.
on-pump coronary artery bypass grafting for (a) in-hospital
mortality, (b) in-hospital mortality with cardiovascular risk
factor adjustment, (c) in-hospital mortality of propensity score
matching (PSM) studies, (d) 30-day mortality. aOR=adjusted odds
ratio; OR=odds ratio; SE=standard error
Supplementary Fig. 5
Funnel plot of off-pump coronary artery bypass grafting vs.
on-pump coronary artery bypass grafting for (a) postoperative
stroke incidence, (b) postoperative stroke incidence with
cardiovascular risk factor adjustment, (c) postoperative stroke
incidence of propensity score matching (PSM) studies, (d)
postoperative myocardial infarction (MI) incidence. aOR=adjusted
odds ratio; OR=odds ratio; SE=standard error
Supplementary Fig. 6
Funnel plot of off-pump coronary artery bypass grafting vs.
on-pump coronary artery bypass grafting for (a) blood cell
transfusion, (b) re-exploration for bleeding, (c) re-exploration
for bleeding of propensity score matching (PSM) studies. OR=odds
ratio; SE=standard error
Supplementary Fig. 7
Funnel plot of off-pump coronary artery bypass grafting vs.
on-pump coronary artery bypass grafting for (a) acute renal
failure, (b) acute renal failure with cardiovascular risk factor
adjustment, (c) renal replacement therapy. aOR=adjusted odds
ratio; OR=odds ratio; SE=standard error
Supplementary Fig. 8
Funnel plot of off-pump coronary artery bypass grafting vs.
on-pump coronary artery bypass grafting for (a) atrial
fibrillation (AF), (b) deep sternal wound infection, (c)
postoperative lower cardiac output. OR=odds ratio; SE=standard
error
Clinical Characteristics of the Included Patients
A total of 31,115 patients were enrolled in the 12 studies, including 20,245
women who underwent ONCAB and 10,910 women who underwent OPCAB. The clinical
characteristics and differences between female patients who underwent OPCAB or
ONCAB, including age, hypertension, diabetes, smoking status, ejection fraction,
chronic obstructive pulmonary disease, peripheral vascular disease, and previous
MI, are shown in Table 2.
Table 2
Characteristics of study participants from the included
studies.
a Indicates a statistically significant association
Effect of OPCAB on In-Hospital Mortality Rate Among Female Patients
We included eight studies to investigate the effect of OPCAB on in-hospital
mortality in women. Female coronary heart disease patients undergoing ONCAB were
the control group. A total of 23,896 women were enrolled in these eight studies,
including 9,833 women who underwent OPCAB and 14,063 women who underwent ONCAB.
The number of deaths in OPCAB and ONCAB patients was 264 and 483, respectively.
The in-hospital mortality rate in female patients who underwent OPCAB was
significantly lower than in those in the ONCAB group (2.7% vs.
3.4%; odds ratio [OR] 0.76; 95% confidence interval [CI] 0.65-0.89) (Figure 2A).
In two of the eight studies, OR values were corrected for cardiovascular risk
factors. Consistently with the meta-analysis results of these eight studies, the
mortality rate of female patients who underwent OPCAB was lower than of those in
the ONCAB group (OR 0.68; 95% CI 0.52-0.89) (Figure 2B).
Among these eight studies, a PSM method was employed in two of them. A total of
3,836 female patients who underwent OPCAB and 3,836 female patients who
underwent ONCAB were enrolled in these two studies. The number of deaths in
OPCAB and ONCAB patients was 118 and 146, respectively. In contrast to the
abovementioned results, there was no significant difference in in-hospital
mortality rate between female patients who underwent OPCAB or ONCAB (3.1%
vs. 3.8%; OR 0.80; 95% CI 0.63-1.03) (Figure 2C).
Effect of OPCAB on 30-Day Hospital Mortality Rate Among Female
Patients
We selected four studies to investigate the effect of OPCAB on the 30-day
postoperative mortality rate in female patients. Female patients who underwent
ONCAB were employed as the control group. A total of 7,529 women were enrolled
in these four studies, including 1,077 OPCAB patients and 6,182 ONCAB patients.
The female 30-day death rate of OPCAB and ONCAB were nine and 222, respectively.
Patients who underwent OPCAB had a lower 30-day mortality rate than those in the
ONCAB group (0.8% vs. 3.6%; OR 0.28; 95% CI 0.15-0.55) (Figure 3).
Effect of OPCAB on Myocardial Infarction Incidence Among Female
Patients
We included six studies to investigate the effect of OPCAB on postoperative MI in
female patients. There was no significant difference in the incidence of
postoperative MI in women who underwent OPCAB compared with those that underwent
ONCAB (1.3% vs. 2.3%; OR 0.88; 95% CI 0.54-1.43). Of the 12
studies included in this study, the PSM method was employed in one, and the
result of this study was consistent with previous results (Figure 4).
Effect of OPCAB on Stroke Incidence Among Female Patients
We included eight studies to investigate the effect of OPCAB on stroke in female
patients. Female patients who underwent ONCAB were used as the control group. A
total of 27,657 women were enrolled in these eight studies, including 10,269
women who underwent OPCAB and 17,388 women who underwent ONCAB. The number of
postoperative strokes in OPCAB and ONCAB female patients was 123 and 359,
respectively. The incidence of postoperative stroke in OPCAB female patients was
lower than in those in the ONCAB group (1.2% vs. 2.1%; OR 0.59;
95% CI 0.48 - 0.73) (Figure 5A).
Among these eight studies, two used the PSM method. Consistently with previous
results, the incidence of stroke in the OPCAB group was lower than in the ONCAB
group (1.0% vs. 1.8%; OR 0.56; 95% CI 0.37-0.83) (Figure 5B). In two of the eight studies,
postoperative stroke OR values were adjusted for cardiovascular risk factors. In
contrast to previous results, there was no significant difference in the
incidence of postoperative stroke between the OPCAB and ONCAB groups (OR 0.87;
95% CI 0.66-1.16) (Figure 5C).
Effect of OPCAB on the Incidence of Red Blood Cell Transfusion and
Re-exploration for Bleeding
We included three studies to investigate the effect of OPCAB on blood transfusion
occurrence in female patients. The incidence of blood transfusion in female
patients who received OPCAB was lower than in those in the ONCAB group (31.1%
vs. 61.4%; OR 0.27; 95% CI 0.16-0.46) (Supplementary Figure 1A).
Seven studies were included to investigate the effect of OPCAB on re-exploration
for bleeding among female patients. Postoperative re-exploration bleeding was
lower in female OPCAB patients than in those in the ONCAB group (4.2%
vs. 4.8%; OR 0.70; 95% CI 0.50-0.97) (Supplementary Figure 1B). However, in the meta-analysis of
PSM studies, there was no significant difference in re-exploration for bleeding
incidence in female ONCAB patients compared with the control group
(Supplementary Figure 1C).
Effect of OPCAB on Acute Renal Failure and Renal Replacement Therapy in
Female Patients
We included seven studies to investigate the effect of OPCAB on postoperative ARF
among female patients. A total of 25,508 women were enrolled, including 10,011
women who underwent OPCAB and 15,497 women who underwent ONCAB. The incidence of
ARF in OPCAB female patients was lower than in those in the ONCAB group (1.9%
vs. 3.6%; OR 0.62; 95% CI 0.42-0.91) (Supplementary Figure 2A). Two studies that investigated OR
adjusted by cardiovascular risk factors also showed a lower risk of
postoperative ARF in women who underwent OPCAB (OR 0.69; 95% CI 0.56-0.84)
(Supplementary Figure 2B). We also found
that the incidence of female patients receiving renal replacement therapy after
surgery was lower in the OPCAB than in the ONCAB group (1.02%
vs. 2.57%; OR 0.51; 95% CI 0.28-0.91) (Supplementary Figure 2C).
Effect of OPCAB on Deep Wound Infection in Female Patients
Six studies were included to investigate the impact of OPCAB on deep wound
infection among female patients. A total of 9,707 OPCAB female patients and
13,970 ONCAB female patients were included in these studies. We found that the
incidence of deep wound infection in OPCAB patients was lower than in ONCAB
patients (0.3% vs. 0.7%; OR 0.58; 95% CI 0.37-0.90)
(Supplementary Figure 3A).
Effect of OPCAB on Atrial Fibrillation and Postoperative Lower Cardiac
Output
We included six studies to investigate the effect of OPCAB on postoperative
atrial fibrillation in women. A total of 6,319 female patients who underwent
OPCAB and 9,927 female patients who underwent ONCAB were included in these
studies. The incidence of postoperative atrial fibrillation showed no
statistical difference in OPCAB patients compared with ONCAB patients (20.2%
vs. 23.4%; OR 0.85; 95% CI 0.68-1.06) (Supplementary Figure 3B). Three studies were included to
investigate the effect of OPCAB on postoperative lower cardiac output in women.
The results showed no significant difference in postoperative lower cardiac
output incidence in OPCAB patients compared with ONCAB patients (5.3%
vs. 6.5%; OR 0.88; 95% CI 0.52-1.51) (Supplementary Figure 3C).
DISCUSSION
In this study, we included 12 retrospective observational studies regarding the
influence of the female sex on the short-term clinical outcomes following OPCAB and
ONCAB. A total of 31,115 patients were included, which consisted of 20,245 males and
10,910 females. We observed that the incidence of adverse events in female patients
who underwent OPCAB was lower or not significant, but not higher, than in those in
the ONCAB group.
According to the American Heart Association guidelines for CABG, women are at a
higher risk for adverse clinical outcomes, including postoperative mortality and
stroke[8]. However, most of
these studies are based on ONCAB. Previous research from Risum et al.[29] confirmed that the risk of early
mortality and low-output syndrome needing intra-aortic balloon support was higher in
women than in men. In addition, a meta-analysis from Wognsen et al.[30] found that females run an
increased risk of early death and the development of postoperative complications
after CABG compared with males. These results were mainly caused by the increased
complexity of the procedure due to women’s smaller body surface area[30].
OPCAB is performed on a beating heart without extracorporeal bypass compared with
traditional extracorporeal bypass surgery. OPCAB has many advantages, such as
shorter operation time, reduced hospitalization and intensive care unit length of
stay, lower medical costs, and fewer surgery-related complications[31].
Large randomized controlled clinical trials, including CORONARY[10] and ROOBY[11], found no significant difference
between OPCAB and ONCAB regarding the 30-day death rate, MI, stroke, or renal
failure requiring dialysis. However, these clinical studies did not investigate
whether female patients who underwent OPCAB had a better short-term outcome compared
to female patients who underwent ONCAB.
A meta-analysis from Attaran et al.[12] investigated short-term outcomes among OPCAB
vs. ONCAB female patients. In this study, no statistically
significant difference was observed in the 30-day mortality rate and other morbidity
outcomes between the OPCAB and ONCAB groups, except for perioperative MI. This
study’s results are limited because both 30-day mortality and not in-hospital
mortality rates were considered primary endpoints after CABG, but most of the
included research investigated in-hospital mortality rates. Although 30-day
mortality and in-hospital mortality rates are both short-term effects, failure to
delineate them may give incorrect conclusions. Furthermore, Attaran et al.’s study
did not investigate the OR adjusted by cardiovascular risk factors, leading to
confounding factors affecting the results[12].
In contrast to Attaran’s study, we found that the in-hospital and 30-day mortality
rates in female patients who underwent OPCAB were significantly lower than in those
in the ONCAB group in studies with and without cardiovascular risk factor
adjustment. The in-hospital mortality rate of OPCAB female patients was not
significantly different from ONCAB female patients in PSM studies. In the primary
meta-analysis, the incidence of postoperative stroke in female patients who
underwent OPCAB was lower than in those in the ONCAB group, while the difference in
postoperative stroke between OPCAB and ONCAB in PSM studies and post-MI was
insignificant. The incidence of unfavorable outcomes in female patients who
underwent OPCAB was not higher than in those in the ONCAB group. In summary, the
short-term clinical outcomes of women who underwent OPCAB were not worse than of
those in the ONCAB group. Notably, the in-hospital mortality and postoperative
30-day mortality rates of OPCAB patients were lower than of ONCAB patients. We
surmise that this may be related to the fact that OPCAB causes less trauma and
minimally affects patients’ circulation compared to ONCAB.
Limitations
Our study has the following shortcomings: 1) we had not retrieved random control
studies, so the studies we included were all retrospective case-control
observational studies that might attenuate our research’s strength; 2) our study
did not further explore the effect of sex difference on long-term prognosis
after CABG due to the lack of relevant literature.
CONCLUSION
Compared to the American Heart Association CABG guideline, the incidence of adverse
events in female patients who underwent OPCAB was lower or not significant, but not
higher, than in those in the ONCAB group. Our findings should nevertheless be
treated with caution due to the limitations attributed to observational studies.
Randomized controlled trials are warranted to further substantiate our conclusion in
the future.
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Notes
Notes
Financial support: This work was supported by Guangzhou City Science and
Technology Program (No. 202102021100) and Guangzhou Traditional Chinese medicine
and Integrated Traditional Chinese and Western Medicine science and and
technology project (20222A010003) to Dr. Jun Fan.
Conflict of interest declaration
No conflict of interest.
Author notes
# Contributed equally.
This study was carried out at the Department of Cardiology, Guangzhou First
People’s Hospital, School of Medicine, South China University of Technology,
Guangzhou, People’s Republic of China.
Correspondence Address: Wei-jie Li, https://orcid.org/0000-0002-7103-7543, Department of Cardiology,
Guangzhou First People’s Hospital, School of Medicine, South China University of
Technology, No. 1 Panfu Road, Guangzhou, People’s Republic of China, Zip Code:
510180, E-mail: eylwj@scut.edu.cn
