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14 Use ofFluorescence Guidance inCardiothoracic Surgery
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with the IMA not occluded are used to generate pixel intensity
grafts. The difference represents the ow to the anterior wall of
the heart provided by the IMA graft (Fig.14.2). The additional
ow to the anterior wall from the IMA blood supply can be quantitated by subtracting these two values. Obviously, separate
images are recorded for each injection and compared. The lack of
increased ow may be a sign of competitive ow due to a nonphysiologic proximal coronary artery stenosis. The importance to
competitive blood ow is unknown. The next areas of research
will include attempting to quantitate blood ow to the myocardium.
It is important to realize that the intensity of the surface pixels
may not reect the heterogenous blood ow which occurs deeper
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ost Graft Image
Fig. 14.2 Pixel intensity measurements approximate myocardial blood ow
using the SPY Q analysis program. Measurements are made with the crossclamp off. In the left panel, the blue represents anterior wall pixel intensity
(blood ow), to the native myocardium (pre-grafting; IMA occluded). The
red line represents the average pixel intensity after grafting with the IMA
(post-grafting; IMA graft open). If the native ow is normalized to a value of
1 (middle panel), then the increased ow with the new IMA graft is quantitated to 6.45 times the blood ow. The right panel shows myocardial perfusion of the native vessel (blue), the improved ow with a new IMA graft (red),
and the ow added to the anterior wall (green) [30]. Reproduced with rights:
Mitsuo Kusano. IICG Fluorescent Imaging and navigation Surgery. Springer.
Chap. 6 Takahashi, M, Masuda M, Miyajima K, etal. Innovative SPY Intraoperative Imaging and Validation Technologies for Coronary Artery Bypass
Grafting Surgery. Figure14.3, 2016
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in the myocardium and endocardial surfaces. This will always be
a limitation to blood ow analysis using this technique. Not to
mention the very un-physiologic state being studied with an
arrested heart in diastole. To truly asses changes in myocardial
blood ow before and after bypass grafting, the heart must be
assessed not only under similar work conditions, but all layers of
the myocardium need to be assessed, which is not feasible during
bypass grafting surgery.
D. Muehrcke
Validation Studies
Takahashi and associates [23] were one of the rst authors to
compare IFI with TTFM in off-pump cases in Japan. Each patient
served as their own control. They demonstrated high-quality IFI
images in 290 grafts of 72 off-pump CABG cases (mean of 4.0
grafts per patient). Four anastomoses (1.4%), including 2 proximal and 2 distal, were revised because of defects detected by SPY
images. In one case (Fig.14.3), the SPY system revealed no blood
ow in a radial sequential graft, although transit-time ow meter
measurements taken on the sequential portion of the bypass graft
showed a diastolic dominant pattern with intermediate ow of
24 mL/min. SPY images revealed the proximal portion of the
radial artery graft, between the aorta and the obtuse marginal
artery, to be non-patent, allowing them to revise the graft while
the patient was still on the operating table. After revision, slide B
on the right demonstrates IFI imaging showing both the aorta to
obtuse marginal 1 graft and the sequential obtuse marginal 1 to
obtuse marginal 2 graft the be patent. The TTFM ow increased
from 22mL/min top 55 mL/min in the sequential portion of the
graft. The authors concluded that using the SPY system, technical
failures could be completely resolved during surgery. They stated
that the use of the SPY system for intraoperative graft validation
during off-pump CABG may become the gold standard for surgical management in the near future. Importantly, Takahashi was
able to demonstrate a signicant aw in TTFM analysis, that is,
the inability to visually assess the bypass grafts. He demonstrated
a
b
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55 ml/min
Fig. 14.3 Slide A represents the IFI images of a radial sequential graft from
the circumex obtuse marginal 1 to the circumex obtuse marginal 2. By IFI
the free radial graft from the aorta to the obtuse marginal 1 is occluded; however, the ow measured on the sequential obtuse marginal 1 to obtuse marginal 2 reveals a ow of 24mL/min. After revision, slide B on IFI imaging
shows both the aorta to obtuse marginal 1 graft and the sequential obtuse
marginal 1 to obtuse marginal 2 graft the be patent. The TTFM ow increased
from 22 mL/min to 55 mL/min [31]. (Reproduced with permission: Takahashi, Msao, Ishikawa, Toshihiro. SPY: an innovative intra-operative imaging
system to evaluate graft patency during off-pump coronary artery bypass
grafting. Interactive CardioVascular and Thoracic Surgery 3 (2004) 479–483)
two cases where sequential grafts were used wherein TTFM was
unable to identify graft closure correctly.
In another patient depicted in Fig. 14.4, an in situ internal
mammary artery has been used as a sequential graft between the
diagonal and the left anterior descending (LAD) artery.
Intraoperative uorescence imaging reveals that the sequential
portion between the diagonal and the LAD artery is occluded
despite the TTFM ow measuring a ow of 22 mL/min, when
measured in the IMA to diagonal graft. The images on the right
were taken after the graft was revised in the operating room. It
demonstrates excellent ow through both anastomoses of the
sequential diagonal to LAD graft. The TTFM ow was unchanged
(22mL/min) after revision. In both cases presented, the TTFM
was not helpful in detecting a signicant intraoperative graft
occlusion because of a lack of visual assessment of the graft.
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LITA - 1st diagonal - LAD grafting.
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22
40
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Probe size 3.0 mm
LITA
Diagonal Diagonal
LAD
LITA
PI PI2.3
LIMA Sequential LA
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D. Muehrcke
LAD
2.4
IMA Sequential LAD
Fig. 14.4 Sequential IMA to diagonal and LAD graft. On the left the diagonal to LAD sequential graft is occluded by IFI; however, TTFM measured a
ow of 22mL/min. After revision IFI shows the entire sequential graft to be
patent; however, there was no change in the TTFM ow of 22mL/min [31].
(Reproduced with permission: Takahashi, Msao, Ishikawa, Toshihiro. SPY:
an innovative intra-operative imaging system to evaluate graft patency during
off-pump coronary artery bypass grafting. Interactive CardioVascular and
Thoracic Surgery 3 (2004) 479–483)
Desai and colleagues [24] also noted that early CABG failures
may be corrected if identied intraoperatively. These researchers
like Takahashi compared the diagnostic accuracy of transit-time
ultrasound ow measurement and ICG uorescent-dye graft angiography. Both imaging studies were performed in each patient, as
they acted as their own control. Virtually all cases were performed
with cardioplegic arrest on the cardiopulmonary bypass machine.
Patients undergoing isolated CABG with no contraindications for
postoperative angiography were enrolled in the study. Patients
were randomly assigned to be evaluated with either ICG angiography (ICG) and then transit-time ultrasonic ow measurement or
transit-time ow then ICG angiography. Interestingly, all patients
underwent X-ray angiography on postoperative day 4. The primary end-point of the trial was to determine the sensitivity and
specicity of the two techniques versus standard X-ray angiography to detect graft occlusion or greater than 50% stenosis in the
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graft or peri-anastomotic area. A total of 106 patients were
enrolled, and X-ray angiography was performed in 46 patients. In
total, 139 grafts were reviewed with all 3 techniques and 12 grafts
(8.2%) were demonstrated to have greater than 50% stenosis or
occlusion by the reference standard. The sensitivity and specicity of ICG to detect greater than 50% stenosis or occlusion was
83.3% and 100%, respectively. The sensitivity and specicity of
transit-time ultrasonic ow measurement to detect greater than
50% stenosis or occlusion was 25% and 98.4%, respectively. The
p value for the overall comparison of sensitivity and specicity
between ICG and transit-time ow ultrasonography was 0.011.
The difference between sensitivity for ICG and transit-time ow
measurement was 58% with a 95% condence interval (CI) of
30% to 86%, p=0.023. The authors concluded that ICG provided
a better diagnostic method of detecting clinically signicant graft
errors than did transit-time ultrasound ow measurement. They
also had patients who had marginal TTFM graft ows (5–40mL/
min) but had occluded grafts when visualized using ICG.
In a separate study, Wasada and associates [25] evaluated the
intraoperative uorescence imaging (IFI) system in the real-time
assessment of graft patency during off-pump CABG. Patients
undergoing off-pump CABG received IFI analysis, intraoperative
transit time owmetry, and postoperative X-ray angiography. A
total of 507 grafts in 137 patients underwent analysis. Of all the
IFI analyses, 379 (75%) grafts were visualized clearly up to the
distal anastomosis. With regard to anastomosis location, anterior
location was associated with a higher percentage of fully analyzable images (90%). More than 80% of images were analyzable,
irrespective of graft type; six grafts with acceptable transit-time
owmetry results were diagnosed with graft failure by IFI, which
required on-site graft revision. All revised grafts’ patency was
conrmed by postoperative X-ray angiography. Conversely, 21
grafts with unsatisfactory transit-time owmetry results
demonstrated acceptable patency with IFI. Graft revision was
considered unnecessary in these grafts, and 20 grafts (95%) were
patent by postoperative X-ray angiography. Compared with slow
washout, fast washout was associated with a higher preoperative
ejection fraction, use of internal mammary artery grafts, and ante-
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rior anastomosis location. The authors concluded that the IFI system enabled on-site assessment of graft patency, providing both
morphologic and functional information. They concluded that this
technique may help reduce procedure-related, early graft failures
in off-pump bypass patients.
D. Muehrcke
Interpretation
Several researchers have attempted to quantitate myocardial perfusion or graft ow using IFI.None have been able to quantitate
myocardial blood ow reliably using the pixel intensity measurements which are used in assessing graft patency. It is important to
understand that as a result of the low energy used in the laser to
obtain images using IFI, only 2mm of the myocardial surface can
be imaged. Therefore, any quantitative analysis presumes that
myocardial blood ow is universal through the entire thickness of
the ventricular wall. This obviously may be not true and represents a potential inaccuracy of this methodology. Nonetheless,
Detter et al. [26] have shown that myocardial blood ow is
reduced in a step-like fashion with greater degrees of coronary
stenosis. Moreover, Yamamato [27] has shown a similar association looking at the ow in the vessel itself, not the myocardium.
Both attempted to assess myocardial ow by measuring peak
pixel intensity and time to peak pixel intensity.
Detter etal. [26] attempted to quantify the blood supply to the
heart by measuring the maximum pixel intensity of the myocardium and time to maximum intensity during the myocardial phase
of IFI imaging. They evaluated the ability of IFI to quantitatively
assess the effect of coronary stenosis of variable severity on myocardial perfusion using two separate methods. They compared the
effect of variable coronary artery stenosis invivo (coronary stenosis of 25%, 50%, 75%, and 100% ow restriction) using IFI
compared to the gold standard assessment using the uorescent
microsphere method. Using open-chest pigs, graded stenosis and
total occlusion of the left anterior descending coronary artery
were created. They showed that increasing graded stenosis and
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total vessel occlusion reduced normalized background-subtracted
peak uorescence intensity and the slope of uorescence intensity
signicantly. Moreover, background-subtracted peak uorescence
intensity and slope of uorescence intensity (analyzed by ICG)
demonstrated good linear correlation with uorescent
microsphere- derived myocardial blood ow. These quantitative
assessments of myocardial blood ow using IFI are mostly used
to show an increase or no change in myocardial blood ow following bypass grafting (Figs.14.5 and 14.6). They concluded that
the impairment of myocardial perfusion in response to increased
coronary stenosis severity and total vessel occlusion can be quantitatively assessed by ICG and correlates well with results obtained
by uorescent microsphere assessment.
Ferguson etal. have also reported that the change in uorescence intensity is a direct indicator of the change in the myocardial perfusion using perfusion pixel analysis [28]. Using this
methodology his group has used IFI to assess competitive ow
after bypass grafting. He has shown that when there is no increase
in myocardial perfusion after grafting, the native vessel stenosis is
likely not physiologically signicant despite how tight the native
vessel stenosis appeared visually. This may help reduce the
incidence of early graft closure by better understanding which
types grafts are more prone to competitive ow after they are constructed. Looking at 167 bypass patients with 359 grafts (53%
arterial), all grafts were widely patent by IFI, and 24% of the arterial and 22% of the saphenous vein grafts showed no regional
myocardial perfusion change in response to bypass grafting, consistent with competitive ow. In 165 in situ internal mammary
grafts to the left anterior descending artery (>70% visual stenosis
on preoperative angiogram), 40 had no change in regional myocardial perfusion, and 32 of the 40 had competitive ow imaged.
They concluded that an important number of angiographic patient
bypass grafts demonstrated no change in regional myocardial perfusion suggesting anatomical, but nonfunctional stenosis in the
target vessel epicardial coronary arteries. In in situ arterial grafts
imaged, competitive ow was associated with nonfunctional stenosis in the target vessel epicardial coronary artery. During the
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D. Muehrcke
Fig. 14.5 Time-intensity curves of the left ventricular anterior wall analyzed
by slope of uorescence intensity (SFI) in a representative experiment at
baseline and four graded coronary stenosis (25%, 50%, 75%, and 100% ow
restriction). a.u. equals arbitrary units. One can see the diminished intensity
of the uorescence with increasing degrees of vessel stenosis. (Reproduced
with permission: Detter C, Wipper S, Russ D, If and A, Burdorf L, Thein E,
etal. Fluorescent cardiac imaging: a novel intraoperative method for quantitative assessment of myocardial perfusion during graded coronary artery stenosis. Circulation. 2007;116 (9):1007–14)
discussion of this paper [29], it was pointed out that the surgeon
only nds out that graft has competitive ow after the graft has
been performed, thereby limiting the usefulness of the technique.
40
BSFI
0% 25% 50% 75% 100%
Rest flow
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Flow reductio
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Fig. 14.6 Background-subtracted peak uorescence intensity (BSFI) (left)
and slope of uorescence intensity (SFI) (right) obtained at baseline and four
graded coronary stenosis (25%, 50%, 75%, and 100% ow restriction) in 11
animals (Reproduced with permission: Detter C, Wipper S, Russ D, If and A,
Burdorf L, Thein E, etal. Fluorescent cardiac imaging: a novel intraoperative
method for quantitative assessment of myocardial perfusion during graded
coronary artery stenosis. Circulation. 2007;116 (9):1007–14)
Moreover, as the IFI in this study was not performed under stress,
the physiologic importance of the epicardial stenosis may have
been underestimated. Moreover, Sabik [29] pointed out that there
is likely a benet to bypassing coronary arteries without signicant fraction ow reserve numbers as 80% of the grafts remain
patient at a year, and the long-term effect is likely benecial to the
patient as their disease is likely to progress.
While some authors have found IFI helpful in evaluating stenosis at the anastomosis [24, 30], direct assessment of the severity of
vessel stenosis by IFI can be limited. While the previously mentioned studies have illustrated that the extent of changes in ICG
uorescence intensity of the myocardial wall is useful, the human
myocardium is often covered with an epicardial fat pad that limits
ICG uorescence imaging and therefore making analysis often
times inaccurate.
Therefore, Yamamoto etal. [31], using an exvivo model, studied the effect of vessel stenosis on the maximum intensity and
time to maximum intensity in the vessels only, not the myocardium. During near-infrared (NIR) angiography, the uorescence
intensity was calculated during pre- and post-stenosis in an articial exvivo circuit, using NIR angiography. They measured the
time to maximum uorescence intensity and the absolute maxi-
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mum intensity. They found that severe stenosis (greater than 75%)
attenuated the increase in ICG uorescence intensity in the vessel
but not the time to maximum uorescence. The conventional
visual qualitative NIR angiographic assessment may produce a
false result, due to the human eye not being able to perceive a difference in the intensity of the uorescence. The anastomoses may
appear normal as the ow rate (time to peak intensity) is not
affected by greater degrees of stenosis. The surgeon is likely to
see ow through the anastomosis but not perceive a diminished
intensity of the uorescent dye. The estimation is made worse by
the fact that the time to maximal intensity if one looks at the ow
through the vessel only is the same whether there is a tight stenosis at the anastomosis or not. This technique cannot detect small
differences over time [32]. Since arterial stenosis attenuates
increases in ICG uorescence intensity through vessels, quantitative analysis using NIR angiography could predict vessel stenosis.
This quantitative assessment may provide a more precise evaluation of vessel stenosis or graft complications, as this ex vivo study
was able to detect vessel stenosis exceeding 75%.
D. Muehrcke
Clinical Results
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].
SPY imaging has been the topic of a substantial body of evidence supporting its use in CABG surgery. In 2009, cardiac surgeon researchers presented results from 350 patients undergoing
CABG including SPY imaging enrolled in the VICTORIA
Multicenter Registry. VICTORIA data showed that the complication rates, including reoperation and long length of stay, were
50% lower than expected compared to similar patients enrolled in
the Society of Thoracic Surgeon’s (STS) national cardiac database. The STS database is one of the longest-standing and largest
existing medical datasets that exist today [4].
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