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\begin{document}

\title{Graft patency and completeness of revascularization in minimally
invasive multivessel coronary artery bypass surgery}



\author[1]{Lufeng Zhang}%
\author[1]{Yuanhao Fu}%
\author[1]{Yicheng Gong}%
\author[1]{Hong  Zhao}%
\author[1]{Song WU}%
\author[1]{Hang Yang}%
\author[1]{Zhe Zhang}%
\author[1]{Yunpeng Ling}%
\affil[1]{Peking University Third Hospital}%


\vspace{-1em}



  
  \date{May 25, 2024}


\begingroup
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\selectlanguage{english}
\begin{abstract}
Objectives: Graft patency and completeness of revascularization were
analyzed in patients who underwent off-pump minimally invasive coronary
artery bypass grafting via left small thoracotomy. Methods: We
retrospectively reviewed the invasive angiography findings and clinical
data of 186 consecutive patients who underwent off-pump minimally
invasive coronary artery bypass grafting via left small thoracotomy. The
left internal thoracic artery and saphenous vein were used to bypass two
or more of three coronary artery systems: the left anterior descending
artery, left circumflex artery, or right coronary artery. Before
hospital discharge, invasive angiography was performed to assess graft
patency and completeness of revascularization. Clinical variables during
hospitalization and follow-up were collected and analyzed. Results: All
186 patients successfully underwent off-pump minimally invasive coronary
artery bypass grafting without conversion to sternotomy or assistance of
cardiopulmonary bypass. The mean graft number was 2.81 per patient
(range, 2--5), and the total number of grafts was 522. The in-hospital
mortality rate was 1.6\% (3/186). A total of 181 of 186 (97.3\%)
patients underwent postoperative invasive angiography. Among the 510
grafts assessed by angiography, the total graft patency rate was 96.3\%
(491/510) {[}98.3\% (171/174) for left internal thoracic artery grafts
and 95.2\% (318/334) for saphenous vein grafts{]}. The rate of complete
revascularization was 98.8\% (510/516) of the total grafts in 180 of 186
(96.8\%) patients. Conclusions: Minimally invasive coronary artery
bypass grafting using left internal thoracic artery and saphenous vein
grafts provides acceptable graft patency and completeness of
revascularization for patients with multivessel disease.%
\end{abstract}%



\sloppy


\textbf{Abbreviations:}

A.o Ascending aorta

BMI Body mass index

CABG Coronary artery bypass grafting

COPD Chronic obstructive pulmonary disease

CR Completeness of revascularization

CT Computed tomography

DES Drug eluting stent

EF Ejection fraction

IABP Intra-aortic balloon pump

ICR Incomplete revascularization

ICU Intensive care unit

LAD Left anterior descending artery

LITA Left internal thoracic artery

LCX Left circumflex artery

LM Left main artery

LVEDD Left ventricular end-diastolic dimension

MACCE Major adverse cardiovascular and cerebral events

MI Myocardium infarction

MICS CABG Minimally invasive coronary surgery-coronary artery bypass
grafting

OPCAB Off pump coronary artery bypass

PCI Percutaneous coronary intervention

RA Radial artery

RBC Red blood cell

RCA Right coronary artery

SV Saphenous vein

\textbf{Introduction}

For several decades, coronary artery bypass grafting (CABG) has been
considered the gold standard treatment for coronary
disease\textsuperscript{1,2}. CABG has good outcomes
\textsuperscript{3}because of complete revascularization (CR) and good
graft patency. Off-pump CABG (OPCAB) was shown in a randomized
trial\textsuperscript{4} and retrospective analysis \textsuperscript{5}
to have the same advantages as on-pump CABG while avoiding the
morbidities associated with blood--machine interactions. However, these
approaches are potentially associated with surgical invasiveness
involving the sternum and wound complications. In the era of minimally
invasive surgery, patients prefer durable outcomes and less
invasiveness, which help them to recover their normal activity.
Minimally invasive coronary surgery--CABG (MICS CABG) via left anterior
thoracotomy is reportedly a less invasive and sternum-sparing approach
for multivessel or left main artery disease \textsuperscript{6-9}.
Unlike CABG via sternotomy, which has been studied for many years with
convincing data showing its effectiveness and reproducibility, fewer
objective data are available for MICS CABG, especially angiographic data
regarding the graft patency and CR rates \textsuperscript{10-12}.

In MICS CABG, limited space for visualization and heart manipulation
adds technical difficulty when constructing anastomoses to the lateral
or post-inferior epicardial vessels \textsuperscript{13}. This might be
associated with impaired graft patency and incomplete revascularization
(ICR). After adopting OPCAB and minimally invasive direct CABG as
routine practice for surgical revascularization, we transformed our
practice to MICS CABG for multivessel and left main artery disease. Our
preliminary experience made it possible to revascularize target vessels
with a left internal thoracic artery (LITA) and sequential saphenous
vein (SV) graft via minimal thoracotomy. In the present study, we
analyzed a series of 186 consecutive patients who underwent MICS CABG
with a focus on the postoperative graft patency and CR rates.

\textbf{Patients and Methods}

From 24 November 2016 to 23 December 2019, 186 patients who had been
diagnosed with multivessel or left main coronary artery disease by
coronary angiography were referred for surgical revascularization. After
preoperative examination and exclusion of other cardiovascular
abnormalities, elective MICS CABG via small left thoracotomy was
performed by surgeons who had passed the steep learning curve of this
procedure. This study was approved by the ethics committee of Peking
University Third Hospital.

Contraindications for this procedure included an unstable preoperative
hemodynamic status, severe pulmonary dysfunction, severe obesity,
thoracic cavity deformity, and porcelain ascending aorta (A.o)
calcification as indicated by computed tomography (CT). The patients'
preoperative characteristics are listed in Table 1.

The preoperative antiplatelet regimen was administration of 100 mg of
oral aspirin per day from admission to the day before the operation. In
patients who had undergone percutaneous coronary intervention (PCI)
\textless{}1 year preoperatively while the stent remained patent, a dual
antiplatelet regimen of 100 mg of aspirin and 75 mg of clopidogrel per
day was adopted until the day before the operation.

An individualized surgical plan for revascularization was established
preoperatively according to each patient's variables and coronary
anatomy. All 186 patients were intent to achieve complete myocardial
revascularization with the use of two grafts to bypass two or more of
three coronary systems: the left anterior descending artery (LAD), left
circumflex artery (LCX), and right coronary artery (RCA).

The patient was placed in the supine position with a soft pad under the
left scapula, which elevated the left chest by 10 cm. The patient was
then intubated with a double-lumen endotracheal tube. An external
defibrillator pad was placed for emergency defibrillation. A Swan-Ganz
catheter was placed via the right internal jugular vein into the
pulmonary artery for intraoperative hemodynamic monitoring. After
draping, a 7- to 8-cm-long incision, two-thirds lateral to the left
middle clavicle line, was made via the fifth intercostal space after
establishing single-lung ventilation. The chest wall was lifted with a
retraction system, and the LITA was carefully identified and harvested
in a pedicled manner under direct vision from the innominate vein
superiorly to its bifurcation or trifurcation inferiorly. The thymus and
pericardial fat tissue were dissected and removed with cautery for
exposure of the A.o before pericardiotomy. Heparin (1 mg/kg) was
administered to achieve an activated clotting time of \textgreater{}250
seconds. Heparin was supplemented at 30-minute intervals to keep the
activated clotting time at \textgreater{}250 seconds. After
pericardiotomy, the target vessel was identified and exposed. At the
same time, an endoscopic or open procedure to harvest the SV was
performed by the surgical staff. The SV was prepared in heparinized
solution after ligation of its branches.

An apical suction device was used to position the heart, and the target
vessel was then stabilized with a vacuum-assisted Octopus Nuvo
epicardial stabilizer (Medtronic, Minneapolis, MN, USA). After
arteriotomy, an intracoronary shunt was routinely inserted into the
vessel to minimize acute ischemia. Handsewn distal anastomosis was
accomplished with a running 7-0 or 8-0 Prolene suture (Ethicon, Inc.,
Somerville, NJ, USA). The routine revascularization strategy was the
LITA to LAD first, then proximal anastomosis to the A.o with the SV or
radial artery (RA), followed by sequential grafting with a single SV or
RA graft \textsuperscript{14} to bypass the trunk or branch of the LAD,
LCX, or RCA.

Placement of traction sutures on the right pericardium lateral to the
A.o, together with insertion of a moist sponge between the right
pericardium and A.o, pushed the A.o leftward and facilitated exposure of
the proximal A.o. The proximal anastomosis was performed using 6-0
running propylene suture (Ethicon, Inc.) with the aid of a long-shaft
side clamp to connect the SV with the A.o. The presence of an eggshell
A.o that had not been visible in the preoperative CT scan excluded the
possibility of proximal A.o anastomosis. In such cases, the SV graft was
anastomosed to the left axillary artery via a horizontal incision placed
1 cm under the clavicle, then passed through the first intercostal space
as a sequential graft to bypass the target vessels. Epicardial coronary
arteries with a caliber of \textgreater{}1.5 mm and proximal stenosis of
\textgreater{}70\% were grafted intraoperatively. In two patients, the
left RA was used because of shortage of the SV. The distribution of the
grafts and target vessels are listed in Table 2.

After neutralization of heparin with protamine, the pericardium was
closed. An indwelling catheter was inserted percutaneously and passed
underneath the pleura under direct visualization to block the
intercostal nerves and thus allow for continuous injection of analgesics
postoperatively. A \#28 left chest drainage tube was inserted via the
sixth intercostal space lateral to the incision. The patients were
extubated in the intensive care unit and received an oral dual
antiplatelet regimen of daily aspirin (100 mg) and clopidogrel (75 mg).
The standard regimen after hospital discharge was lifelong continuation
of the aspirin and [?]1-year continuation of the clopidogrel.

The patients underwent invasive coronary artery and graft angiography
via the left RA or femoral artery before hospital discharge. The
postoperative angiograms were reviewed by three coronary surgeons. Each
graft was viewed in at least two orthogonal planes and scored on the
worst appearance of the graft. Graft assessment was standardized by the
FitzGibbon gradation as the presence of stenosis at either the
proximal/distal anastomosis or trunk of the graft: grade A, perfectly
patent; grade B, patent with stenosis reducing the caliber to
\textless{}50\% of the target coronary artery; and grade O, occluded
graft. Grade A and B grafts were deemed patent. The CR rate was the
ratio of the number of grafts constructed intraoperatively to the number
of grafts intended to be constructed. Complementary PCI was performed
with a drug-eluting stent if indicated.

The patients were followed up via the WeChat app by a single physician
assistant after discharge. Major adverse cardiovascular and cerebral
events (MACCE) and all causes of death were recorded.

\textbf{Statistical analyses}

Descriptive, continuous variables are presented as mean and standard
deviation, median and range; categorical variables are presented as
frequencies and percentages.

\textbf{Results}

In total, 186 patients successfully underwent elective MICS CABG. The
mean number of grafts per patient was 2.81 (range, 2--5). Overall, 522
grafts were constructed. No patient required conversion to sternotomy or
extracorporeal circulation support intraoperatively. Three of 186
(1.6\%) patients required intraoperative support by an intra-aortic
balloon pump (IABP) because of ischemia, arrhythmia, or hemodynamic
instability. Postoperatively, eight (4.3\%) patients underwent
re-exploration. Additionally, three (1.6) patients underwent insertion
of an IABP for postoperative hemodynamic support. The postoperative
mortality rate was 1.6\% (3/186). The cause of death was postoperative
myocardial infarction in two patients and stroke in one patient. The
postoperative variables are listed in Table 3.

A total of 181 patients underwent postoperative angiography before
discharge. The reasons why the remaining five patients did not undergo
angiography are listed in Table 4. The postoperative graft angiography
showed that the overall patency rate was 96.3\% (491/510). Further
analysis of graft patency showed that the patency rate of the LITA was
98.3\% (171/174), that of the SV was 95.2\% (318/334), and that of the
RA was 100\% (2/2). The subgroup analysis results of the graft patency
rate in the three different systems of the coronary artery and/or its
branches are shown in Table 5.

A total of 96.8\% (180/186) of patients achieved complete coronary
revascularization. One of the six patients with ICR developed
postoperative bradycardia and hypotension. This patient underwent
emergency invasive angiography with the support of an IABP and recovered
after treatment of a tight stenosis at the orifice of the RCA with a
drug-eluting stent. The CR rate was 97.3\% (181/186) after complementary
PCI. The main cause of ICR was underestimation of stenosis on the
preoperative angiogram.

Calculated by graft, the revascularization rate was 98.9\% (522/528)
before and 99.1\% (523/528) after complementary PCI.

In total, 179 of 183 (97.8\%) patients were closely followed up for a
mean of 18 \selectlanguage{ngerman}± 10.2 months (range, 4--41 months). During follow-up, one
patient experienced sudden death and another died of stomach cancer at 1
and 36 months after discharge, respectively. Five of 183 (2.7\%)
patients developed postoperative major adverse cardiovascular and
cerebral events (4 strokes and 1 repeat PCI for native coronary artery
restenosis). Finally, 182 of 183 (99.5\%) patients survived without
symptoms of myocardial ischemia.

\textbf{Discussion}

MICS CABG has been proven to be a reliable and reproducible alternative
to conventional CABG \textsuperscript{6}. Convincing data show that MICS
CABG provides the benefits of a low transfusion rate, short length of
hospital stay, and rapid recovery to normal
activity\textsuperscript{7,12}. Graft patency and CR are predictive of
the short- and long-term outcomes of patients who undergo coronary
revascularization. Most previous studies used 64- or 256-slice CT
angiography as a noninvasive approach, which showed reliable and
convincing results \textsuperscript{12,15}. In our preliminary study
using CT evaluation (data not shown), the trunk of the graft was well
constructed while the distal anastomosis was less precise for assessment
than transcatheter angiography, especially when the FitzGibbon grade was
B (impaired anastomosis but patent graft). Despite its high
invasiveness, selective coronary and graft angiography via insertion of
a catheter into the orifice of the target vessel was a precise approach
for assessment of the coronary artery or graft.

Invasive postoperative angiography has proven the effectiveness and
superior long-term outcome of CABG versus PCI, which is attributed to
the high CR rate and good graft patency. Some studies did not involve
invasive angiography, mostly because the patients were reluctant to
undergo an invasive intervention. Patients who were not evaluated were
usually asymptomatic; thus, the graft patency rate might have been
underestimated. Furthermore, early postoperative silent occlusion of the
graft makes the real graft patency rate more
unpredictable\textsuperscript{16}.

In our institution, postoperative invasive angiography is routinely
performed for every patient who undergoes surgical revascularization
without a contraindication for quality control. Complementary PCI is
performed to revise either a problematic graft or native coronary
vessel.

Notably, although interventionists are trained to be skillful in native
coronary angiography, not all of them are familiar with LITA and SV/RA
graft angiography. It is sometimes necessary to switch to a femoral
approach for selective angiography of the proximal anastomosis in the
anterior wall of the A.o. The exact location of the proximal anastomosis
might be anywhere in the anterior wall of the A.o. An excessive exposure
time and contrast use makes this challenging. The most likely location
of the proximal anastomosis performed with a side-biter during MICS CABG
is the anterior wall of the A.o just at the level of the tracheal
carina, which can be easily identified by X-ray fluoroscopy in the
catheter laboratory. Selective angiography of the LITA can be performed
via the left RA or femoral artery. The patients in the present study
underwent successful coronary and graft inspection with the
above-described method.

ICR induces postoperative angina, may jeopardize the late outcome, and
usually necessitates repeat revascularization. The technical difficulty
of off-pump heart manipulation and the limited exposure for target
vessel anastomosis in MICS CABG add to the difficulty of accomplishing
CR. The clinical volume of surgical coronary revascularization was 500
to 600 cases (half OPCAB and half sternum-sparing cases) per year in our
center. Before we adopted MICS CABG in our clinical practice, we had
performed more than 800 minimally invasive direct CABG procedures for
treatment of isolated LAD lesions or in combination with PCI procedures
for treatment of multivessel disease. We adopted the ``Nambiar
technique'' \textsuperscript{10} when starting MICS CABG with the
bilateral internal thoracic arteries and performed this procedure in
about 50 cases. Once we had become comfortable with handsewn proximal
anastomosis using a side clamp, we routinely performed the ``proximal
first'' sequential graft \textsuperscript{17} after LITA-to-LAD
anastomosis. This strategy provides the greatest possible blood supply
to the myocardium during manipulation of the heart, minimizing the
possibility of intraoperative hemodynamic instability.

Total arterial revascularization provides good short- and long-term
graft patency and is superior to venous grafting. We have widely
performed MICS CABG with deployment of the bilateral internal thoracic
arteries and RA, and we plan to provide our data in the near future.

The causes of ICR include an invisible target vessel, hemodynamic
instability precluding positioning of the heart, and underestimation of
the target vessel caliber. One patient underwent complementary PCI for
CR of the myocardium. The CR rate in this group of patients undergoing
MICS CABG was not inferior to that of patients undergoing OPCAB or
on-pump CABG in other studies \textsuperscript{18,19}. This finding
proves that MICS CABG can attain a good CR rate similiar to that
attained by conventional procedures.

\textbf{Conclusion}

MICS CABG using LITA and SV grafts provides good graft patency and CR
rates for patients with multivessel disease.

\textbf{Limitations:}

First, this study only showed short term in-hospital angiographic
result, which is more related to surgical technique during operation.
Data regarding mid- and long-term angiographic result will provide more
information. Second, this is a retrospective study of clinical outcome,
graft patency and CR in patients underwent MICS CABG. Prospective,
randomized analysis of MICS CABG comparing with conventional CABG would
be more convincing.

\textbf{Acknowledgement:} The authors sincerely thank Hui Zheng for
doing follow up work for this group patients, Angela Morben, DVM, ELS,
from Liwen Bianji, Edanz Editing China, for editing the English text of
a draft of this manuscript.

\textbf{Funding statement:} None

\textbf{Conflict of interest statement:} None

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