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Use ofFluorescence
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Guidance inCardiothoracic
14
Surgery
DerekMuehrcke
Indications
The ability to accurately identify coronary artery anatomy and
ensure patent bypass grafts is critical to surgical outcome during
open heart surgery. Coronary artery bypass graft patency is the
major predictor of long-term survival after coronary artery bypass
grafting surgery [1]. Technical anastomotic problems are a major
source of early graft closure [2, 3]. The ability to reliably assess
the patency of coronary artery bypass grafts using intraoperative
uorescence imaging has been shown to improve short-term
patient outcomes after coronary artery bypass grafting [4] and to
reduce hospital cost of CABG [5, 6]. Several techniques have
been used to assess intraoperative graft ow and patency. Most
have had drawbacks limiting their use. These have been reviewed
previously by Balacumaraswami and Taggert [7]. Electromagnetic
Supplementary Information The online version contains supplementary
material available at
D. Muehrcke (*)
Cardiovascular and Thoracic Surgery at Flagler Hospital,
Saint Augustine, FL, USA
© The Author(s), under exclusive license to Springer Nature
Switzerland AG 2023
N. Szoka et al. (eds.), The SAGES Manual of Fluorescence-Guided
Surgery, https://doi.org/10.1007/978-3-031-40685-0_14
https://doi.org/10.1007/978- 3- 031- 40685- 0_14.
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owmetry, based on principles of electromagnetic induction, can
quantitate blood ow accurately under experimental conditions
where it assumes laminar ow. However, in the clinical setting,
ow values uctuate with movement and changing hematocrit,
and consequently, its use has been short lived [8–10]. Continuous
wave (CW) and pulsed wave (PW) Doppler velocity measurements have been used to assess intraoperative graft patency.
Although, easy to use, continuous wave (CW) and pulsed wave
(PW) Doppler velocity measurements are based on the principle
of a change in Doppler velocity, detectors have no range resolution and PW Doppler systems were affected by the angle of
insonation [10]. Epicardial ultrasound scanning [11] uses an epicardial probe, which provides satisfactory images of coronary stenosis and graft anastomoses but does not provide real-time
angiographic images. Thermal coronary angiography, based on
the creation of thermal images with an infrared camera, depends
on the temperature difference between the myocardium and the
coronary arteries generated with the use of cold or warm saline or
cardioplegic injections. Although this provides images of graft
function, resolution varies depending on temperature differences
[12]. None of these techniques produce reliable or consistent
results.
D. Muehrcke
Intraoperative Techniques ofGraft Patency
Assessment
There are three currently used popular methods of measuring
graft patency in CABG surgery. The best but most expensive
method is coronary angiography. It does represent the gold standard to determine graft patency. Coronary angiography provides a
clear multiplane visual assessment of all proximal and distal anastomoses. It is however invasive, expensive, and difcult to perform after heart surgery without having a cardiologist and cardiac
catheterization lab available.
Transient time owmetry (TTFM) and intraoperative uorescence imaging (IFI) are currently the two most popular methods
of assessing intraoperative coronary artery bypass graft patency.
14 Use ofFluorescence Guidance inCardiothoracic Surgery
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Both are relatively inexpensive and easy to perform and can provide real-time intraoperative assessment of graft patency. Below
we will discuss both of these techniques: their methodology, current experience, results, and limitations.
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Transit-Time Flowmetry (TTFM)
Transit-time owmetry (Medistim AS, Norway) is a technique
based on the principle of transit-time ultrasound technology. It
uses a perivascular ow probe, which consists of two ultrasonic
transducers and a xed acoustic reector, which holds the graft
perpendicular to the position of the transducers and the reector.
The transit time taken from the wave of ultrasound to travel from
one transducer to another is derived by the ow meter and provides an accurate measure of ow volume [13].
Technique
The ow probes require the use of an ultrasound gel applied to the
lumen of the ow probe. It is important to ensure the graft occupies at least 75% of the area within the probe to get an accurate
reading (Fig.14.1). The coupling agent (gel) improves ultrasound
imaging. Results are quantitatively reported as mean graft ow
and a ow waveform is generated. In addition to the ow waveform, the systems provide various calculated derivatives such as
mean graft ow (MGF), pulsatile index (PI), and diastolic ow
index (DFI).
Mean graft ow is expressed as mL/min which indicates the
quantity of graft ow at the time of the measurement. Mean graft
ow values above 40mL/min indicate satisfactory ow, and values less than 5mL/min are considered unsatisfactory, prompting
revision [13]. When mean graft ow value between 5mL/min and
40 mL are obtained, interpretation depends on certain derived
values such as PI and DFI.PI is expressed as an absolute number
of the value obtained by the dips between the maximum ow and
the minimum ow divided by the mean ow. It gives an estimate
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Fig. 14.1 TTFM ow probe with bypass graft inserted for reading of ow
expressed as mL/min. The ultrasound ow meter measures the velocity of a uid
with ultrasound to calculate volume ow. Using ultrasound transducers, the ow
meter can measure the average velocity along the path of an emitted beam of
ultrasound, by averaging the difference in measured transit time between the
pulses of ultrasound propagating into and against the direction of ow
D. Muehrcke
of the resistance to graft ow. Generally, a PI value of more than
5 is considered to indicate unsatisfactory graft ow [14] and revision should be considered; however, PI alone cannot be used to
determine graft revision. DFI is expressed with the percentage of
total graft ow which occurs during diastole. A predominant diastolic ow in the graft with a DFI that is more than 50 is considered normal, similar to the native coronary blood ow [15]. A DFI
less than 50 is cause for concern. Unfortunately, there are no
images of graft ow produced using this technique to help validate visually marginal or concerning derived values.
Current Experience andResults
Several groups have reported the clinical usefulness of TTFM to
assess graft patency.
D’Ancona etal. reported the need to revise 37 of 1147 graft
(3%) in 33 of 409 off-pump coronary artery bypass grafts (8%).
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407
They emphasize the reliance on correct analysis of TTFM ow
patterns to correct the abnormalities, since interpretation of the
derived values is variable and may be inconclusive [16].
Likewise, Taggert’s group [17] has used TTFM in over 100
patients, and it was found to be useful in conrming graft patency
in the majority of patients with good mean graft ow values.
Using both TTFM and intraoperative uorescence imaging (IFI)
modalities in the same patient, they found that in the majority of
grafts, both TTFM and IFI reliably conrmed graft patency.
However, in 3.8% of grafts (10% of patients) with low mean graft
ow situations, where TTFM indicated the need to revise the
grafts, IFI conrmed satisfactory visual antegrade ow. Because
the ow through the grafts could be visualized, no revisions were
performed. Taggert expressed concerns that TTFM may overestimate the need for graft revision.
TTFM has been used in the assessment of graft patency with a
greater degree of accuracy compared with other ow measurement modalities, such as electromagnetic owmetry, which varies
with movement and hematocrit and Doppler owmeters, which
vary with the angle of insonation [18, 19]. It has correctly identied occluded grafts when other tests suggested a patent graft.
This includes situations where a pulse was felt in an occluded
graft (as a tactile pulse can be felt in occluded grafts which can be
misinterpreted as “ow”). TTFM can detect graft occlusion even
when the ECG remains normal and echocardiography identies
normal wall motion. Jakobsen noted that only one of the ve cases
with TTFM documented graft occlusion was the graft impairment
reected in abnormal ECG ndings [20]. Walpoth and colleagues
describe two cases in which TTFM detected graft occlusion
despite adequate perfusion of the graft assessed by the surgeon’s
ngers, which was corrected on the operating room table [21].
TTFM unfortunately does not always reliably predict graft or
anastomotic stenosis as reported by several groups. Hirotani and
colleagues evaluated TTFM measurements in a series of 291 in
situ internal mammary artery grafts and 190 saphenous vein grafts
in 171 patients. They compared the intraoperative measurements
with postoperative coronary angiogram performed before hospital
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discharge [19]. They found that mean graft ow, as measured by
TTFM failed to predict stenosis or partially occluded grafts on
postoperative angiograms. Jakobsen and Kjaergard reported 1.8%
graft revision rate in a series of 280 CABG patients [20].
D. Muehrcke
Limitations
In the majority of patients with good MGF (>40mL/min), TTFM
reliably indicates graft patency. However, in low mean graft ow
situations, interpretation of PI and DFI values is arbitrary, and
there is considerable uncertainty regarding adequacy of graft
patency. Transit-time ow measurement is a very easy device to
use; however, it does not show a visual image of the graft. When
the graft is subjected to spasm, or the stenosis of the native coronary artery is not very severe, ow measurement data may not be
diagnostic.
Intraoperative Fluorescent Imaging (IFI) System
Principle
SPY intraoperative uorescence imaging received FDA 510(K)
clearance in 2005 as a system to assess graft patency after CABG
surgery. The IFI system SPY™ (STRYKER corporation,
Kalamazoo MI) depends on the uorescent properties of indocyanine green (ICG) dye. ICG rapidly binds to the plasma proteins
when injected intravenously and is therefore conned to the intravascular compartment. Indocyanine green is excreted unchanged
by the liver with a half-life of 3–5min; thus, there is no potential
for nephrotoxic effects for those patients with compromised renal
function. The dye also has an excellent safety prole. The incident
of allergic reactions to ICG is approximately 1in 40,000, and it
has been reported mainly in patients with an allergy to iodine
[22]. The risk of allergic reactions is strongly dose dependent,
being greatest with a dose in excess of 0.5mg/kg weight. A lower
density laser with a total output of 2.7 w spread over an area of
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7.5cm×7.5cm at a distance of 30cm has a depth of penetration
of about 1–2mm to avoid thermal damage. ICG uoresces when
illuminated with a laser light of 806 nm and emits light at the
longer wavelength at 830 nm. The imaging camera head is a
charged couple device video camera and is positioned over the
exposed heart, and the laser is activated before the rst pass of a
bolus of ICG through the eld of view. Images of the coronary
arteries and bypass grafts are acquired at a rate of 30 frames/s and
may be viewed in real time. The near-infrared light can maximally
penetrate 1–2 mm of soft tissue. The uorescence sequentially
shows illumination of the graft or coronary artery lumen, a blush
of the epicardium occurs as the dye passes through the microcirculation, and, nally, washout occurs as the dye enters the coronary veins.
The ICG dye transmission time is dependent on various factors
including the systemic arterial pressure, competitive native coronary blood ow on the severity of native proximal coronary stenosis, distal coronary vascular resistance, and conduit diameter. The
proximal target coronary artery snaring with a silastic sling facilitates anastomotic visualization and largely eliminates competitive
ow [16]. Skeletonized internal thoracic artery (ITA) and radial
artery (RA) conduit provider better visualization than pedicle
ones. The appearance of uorescent images, as the dye passes
through the bypass graft, conrms graft patency.
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Technique
There are three different techniques we use to visualize CABG
grafts and one technique we use to identify epicardial coronary
arteries during redo bypass surgery or for intramyocardial vessel
identication. We typically perform coronary artery bypass grafting using the cardiopulmonary bypass machine with the heart
arrested. We feel this technique allows us to bypass more vessels,
improves long-term graft patency, and improves long-term
survival than off-pump bypass techniques. However, the techniques can easily be used with off-pump bypass grafting, with
special attention to not allowing air down the grafts being assessed.
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D. Muehrcke
A direct handheld injection of ICG down individual vein grafts is
used to assess each vein graft distal anastomosis and to assess
perfusion of the heart (Video 14.1). The important internal thoracic artery to left anterior descending artery bypass graft is
assessed by injection ICG dye into the heart-lung machine.
Imaging of each graft takes only 2–3min (Video 14.2). Typically,
we perform our vein graft anastomoses rst followed by the IMA
to LAD anastomosis. Each distal vein graft anastomosis can be
tested by injecting 10ccs of contrast down the vein graft (or free
arterial graft) through a syringe. The concentration of the ICG
used has decreased with the newer SPY-PHI handheld cameras as
they have improved penetration. The concentration we use is
made up by placing 0.3 ccs (0.375 mg) of ICG (concentration
2.5 mg/mL) into 500 ccs of normal saline (nal concentration
0.00075mg/mL). Thirty-ve ccs of this solution is mixed with
10ccs of heparinized blood mixed with nitroglycerine (0.38mg)
for direct injection down the vein grafts or free internal thoracic
artery grafts. Ten ccs of the nal mixture is injected down the vein
graft as images are acquired, and then the graft is ushed with
heparinized blood as a washout. Care must be taken not inject air
down the grafts, especially when performing off-pump bypass
grafting. The images develop instantaneously in real time. We
specically look for tactile ow resistance through the vein graft,
and the ICG contrast image through the anastomosis, and the epicardial artery. The tactile response of how hard or easy it is to
inject the solution gives feedback as to the ow in the bypassed
vessel. The rate of hand-injected ow is determined by several
factors including the diameter of the vein, the size of the anastomosis, the size of the epicardial artery grafted, and the resistance
in the vascular bed distal to the anastomosis. Moreover, we look
for the three phases of uorescence. The rst is the arterial phase,
where the vein graft, anastomosis, and artery are illuminated. The
second phase is where the myocardium is illuminated, and the
third phase is the venous phase when the veins on the heart are
imaged.
An injection of the ICG into the heart-lung machine is used to
assess IMA to coronary artery ow when the cross clamp is on, as
the in situ graft is the only source of blood ow to the heart with
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the cross clamp on (Video 14.2). Flow through the in situ IMA
graft is evaluated by injecting 0.8 cc of undiluted ICG dye
(1.0mg) into the heart-lung machine. Imaging will take 10–15s
to occur. There should be a brisk transition from the IMA graft
into the left anterior descending coronary artery.
At the end of the procedure after performing the proximal
anastomoses, all proximal anastomoses are assessed simultaneously by injecting 0.3ccs of undiluted ICG (0.375mg) into the
central line (Video 14.3). This is followed by a 10-cc ush of normal saline. Visualization of the proximal anastomoses will take
10–15s to appear as the dye works its way through the heart to the
aorta. Revisions are based on the ndings of the gross blood ow
images. The images are then recorded on computer hard drive as
well as a copy of selected screenshots which are placed into the
patient’s chart. Repeat ICG injections can be administered at short
intervals (after 2 or 3min after the dye washes out) and still generate excellent image quality. Any extravasated dye from a leak at
the anastomosis may obscure images.
The determination of a left anterior descending toe left anterior
descending artery occlusion can be identied easily intraoperatively (Video 14.4). If there is no ow, then the graft can be revised
immediately to insure a patent graft (Video 14.5). In a similar
fashion, an occluded proximal bypass vein graft can de identied
(Video 14.6). These grafts can also be revised immediately to
ensure open grafts at the end of the procedure (Video 14.7).
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Peals andPitfalls ofBypass Graft Imaging
The most important concern with intraoperative imagine using
ICG is the concentration of the dye. We have signicantly
decreased the concentration of the dye solution with the more
powerful handheld SPY-PHI camera. Using a too concentrated
dye solution washes out the images and details such as kinks and
narrowing and even twists in an anastomosis can be obscured. A
too dilute solution will fail to identify epicardial vessels under
scar tissue in redo bypass surgery and may not allow an intramyo-
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D. Muehrcke
cardial epicardial vessel to be seen. Moreover, too dilute of a dye
solution not show graft narrowing.
When performing a root injection of 30–60-cc ICG dye directly
into the root through the anti-grade cardioplegia needle to evaluate for epicardial vessels obscured by overlying scan tissue in
redo procedures (Video 14.8), care must be taken not to introduce
are into the root when doing this. When the heart is arrested, the
dye will not be washed out, as no ush out is used, so the operator
has much more time to nd the images. The difculty occurs
when one has to mark the location of the illuminated vessel while
visualizing on a camera screen, not looking at the heart. One technique we have found helpful is to use a sterile felt marking pen
and touch dots along the illuminated vessel which can easily be
seen on the camera screen. The surgeon then has to just connect
the dots with a scalpel to nd the subtended epicardial vessel. We
have found attempting to draw a straight line over the obscured
epicardial vessel while looking at the camera screen is very difcult and leads to errors in nding the surface vessels. Similar to
operating using a video-assisted thoracoscope (VATS) screen,
one’s movements are opposite to the images viewed. As such
there is learning curve. When looking for buried intramyocardial
vessels, the new SPYPHI scope appears to have deeper tissue penetration and allow nding obscured vessel easier. We have no
experience using a more concentrated solution to see if even
deeper penetration of the images occurs facilitating identication
of intramyocardial vessels.
Another pitfall of the intraoperative assessment of bypass
grafts is when extravasation occurs out of a leaky distal anastomosis, as the contrast is not washed away. The dye can stain the epicardial surface and obscure some images as the uorescent dye
remains. Usually this is not a problem as the ow through the
anastomosis is easily seen on subsequent injections.
One interesting area of ongoing study is the possibility to
assess the presence of competitive ow through the important
IMA to LAD anastomosis if one calculates the pixel intensity to
the anterior wall using qualication hardware. With the cross
clamp off, serial central line injections of ICG with the IMA
occluded using a soft vascular clap rst and then subsequently
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