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Original Article

Coronary artery bypass graft failure and itsrelationship to target artery percentage stenosisand competitive flow. A CT angiographic analysis

Rochita Venkata Ramanan*, Anandkumar Ramalingam

Department of Radiology, Apollo Hospitals, Chennai, India

a r t i c l e i n f o

Article history:

Received 31 July 2014

Accepted 17 September 2014

Available online xxx

Keywords:

CABG failure

CT angiography

Competitive flow

* Corresponding author. No. 34 Srinivasa Mu(home), þ91 9840024528 (mobile).

E-mail address: [email protected] (R.V

Please cite this article in press as: Ramatarget artery percentage stenosis and com10.1016/j.apme.2014.09.001

http://dx.doi.org/10.1016/j.apme.2014.09.0010976-0016/Copyright © 2014, Indraprastha M

a b s t r a c t

Objectives: The Coronary Artery Bypass Graft (CABG) failure is a cause ofmajor cardiac events.

CABG to coronary arteries with low-grade stenosis resulting in competitive flow and graft

failures is a controversial issue. Some studies refute this. All of these studies have been per-

formed with Invasive Catheter Angiogram. This study is the first one to investigate the rela-

tionship between CABG failure and chronic competitive flowwith Coronary CT Angiogram.

Materials and methods: 1445 grafts in 438 patients were studied. The degree of stenosis of the

grafted coronary artery was obtained from the preoperative ICA. The post-CABG CTA was

performed on the Aquilion 64 and Aquilion One 320 slice scanners. The study group was

divided according to graft types into LIMA þ Right internal mammary artery, SVG and left

radial artery. Each type was further divided into “Patent” and “Failed” groups. The two

groups were compared for target artery percentage stenosis below and above 75%. Each

graft type was further divided into subgroups according to years after CABG and compared

similarly.

Results: 72% of total grafts including LIMA, RIMA, SVG and LRA when placed on coronary

arteries with less than 75% stenosis failed as compared to 22.8% grafts failing when placed

on coronary arteries with more than 75% stenosis (p < 0.0001) irrespective of number of

years post CABG.

Conclusion: When faced with competitive flow all graft types fail equally irrespective of

number of years post CABG.

Copyright © 2014, Indraprastha Medical Corporation Ltd. All rights reserved.

1. Introduction

The Coronary Artery Bypass Graft (CABG) procedure is

considered a “medical marvel”, a popular operation that has

stood the test of time. As demonstrated in several clinical

rthy Avenue, Off L B road,

. Ramanan).

nan RV, Ramalingam Apetitive flow. A CT ang

edical Corporation Ltd. A

trials, it gives better survival and fewer repeat re-

vascularizations as compared to Percutaneous Coronary

Intervention (PCI) in diabetics and patients with multivessel

ischemic heart disease. However, graft failure is a cause of

major cardiac events.

Adayar, Chennai 600020, Tamil Nadu, India. Tel.: þ91 44 24417055

, Coronary artery bypass graft failure and its relationship toiographic analysis, Apollo Medicine (2014), http://dx.doi.org/

ll rights reserved.

mailto:[email protected]

www.sciencedirect.com/science/journal/09760016

www.elsevier.com/locate/apme

http://dx.doi.org/10.1016/j.apme.2014.09.001




Studies reveal that 1 in 10 patients undergoing CABG have

at least 1 occluded graft at 30 days and one in 20 of all grafts

are blocked.1 The 10-year patency rates of the Left Internal

Mammary (LIMA) graft are reported to be above 90%. However,

if and when the LIMA graft, which is the most robust conduit,

fails, the options of future revascularisation are significantly

handicapped. Early Saphenous Vein Graft (SVG) failure is

known to be associated with worse long term outcomes after

CABG.2 Despite good overall outcomes with CABG, 30% of

SVGs have been known to fail within 12e18 months. SVG

failure is also associated with a higher rate of perioperative MI

and a higher incidence of MI and revascularization at 1 year.3

Several causes of graft failure are known. Among these,

CABG to coronary arteries with low-grade proximal stenosis

continues to be a controversial issue. Some studies state that

anastomosis of grafts to coronary arteries with low grade

stenosis leads to reduced ante grade flow through the graft, a

condition known as chronic competitive flow, whichmay lead

to early graft failure. Other studies have refuted this fact and

recommend grafting to moderately stenosed coronary ar-

teries. Some canine experiments have demonstrated that

arterial grafts on arteries with no stenosis remained patent at

the end of a two-month follow up advocating CABG to

moderately stenosed coronary arteries.

SVGs are more prone to failure than arterial conduits.

Surgical factors, intimal hyperplasia and atherosclerosis are

thought to be the main reasons for SVG failure. No clear un-

derstanding is present on the effect of chronic flow competi-

tion on SVG.

64-slice CT technology has been proved to have a high

diagnostic accuracy in assessing CABGs as well as native

coronary artery stenosis.

Recent studies show that the 320 slice CT scanners are

more accurate than the 64 slice scanners. Percent diameter

stenosis determined with the use of 320-slice CT Angiography

(CTA) shows good correlation with Invasive Catheter Angio-

gram (ICA) (p < 0.0001).4 While competitive flow has been

addressed with ICA, it has not been evaluated before to our

knowledge with CTA. CTA gives the unique advantages of

simultaneously visualizing all the bypass grafts as well as

evaluating the target arteries for their luminal stenosis. Ma-

jority of the earlier studies have also addressed graft types

separately and near, intermediate and long term CABG failure

separately. This study, for the first time investigates the rela-

tionship between CABG failure and chronic competitive flow

across all terms and all graft types in a comprehensive and

panoramic manner with the help of CTA. The objective of the

study is to determine whether flow competition from border-

line stenotic coronary arteries can cause failure of the bypass

graft placed on such an artery. The study also highlights the

sign of competitive flow from target coronary artery on CTA.

2. Materials and methods

2.1. Study population

1445 grafts in 438 patients referred between 2007 and 2012 to

our department for Coronary CTA 4 months to 23 years after

CABG, were included in this retrospective study. These

Please cite this article in press as: Ramanan RV, Ramalingam Atarget artery percentage stenosis and competitive flow. A CT ang10.1016/j.apme.2014.09.001

patients had no other additional procedures like valve

replacement at the time of CABG. Average number of grafts

per patient was 3.2. Patients ranged in age from 37 to 84 and

had amean age of 60.1 years with 401men and 37 women. 236

patients were symptomatic. The remaining 202 were asymp-

tomatic and referred for checking graft patency. The average

left ventricular ejection fractionwas 58%. 50% of patientswere

diabetics, 57% hypertensives, 56% dyslipidemics, and 31%

were smokers. 41% had a family history of coronary artery

disease and 43% had no risk factors at all. 42% had an MI prior

to the CABG. In cases with sequential grafts, each segment

was counted as a separate graft.

2.2. Angiographic data

The degree of preoperative stenosis of the grafted coronary

artery was obtained from the preoperative ICA. The post-

CABG CTA was performed on the Aquilion 64 and Aquilion

One 320, Toshiba Japan, scanners. 46% of the patients under-

went the study on the 64 slice CT and the remaining under-

went a 320 slice CT. IV contrast used was Optiray 350 mg,

Mallinckrodt USA. ECG gated scans were performed through

the heart after 65 ml of intravenous contrast injection at the

rate of 4.5 ml/s with a pressure injector chased by a bolus of

30 ml of normal saline at the same rate. The images were

interpreted on curved reconstructions through the vessel

lumen as well as the cross sections on a dedicated worksta-

tion. A senior and a junior radiologist interpreted the scans

separately. Consensus was arrived at by discussion prior to

final report generation. The percentage of stenosis on the CT

Angiograms was calculated with calipers on cross sections of

the minimum luminal diameter of the stenotic segment and

the reference vessel diameter of the adjacent normal

segment.

The study group was divided according to graft types into

LIMA þ Right internal mammary artery (RIMA), SVG and left

radial artery (LRA). Each typewas further divided into “Patent”

and “Failed” groups. The failed group consisted of occluded,

diffusely narrowed, and grafts with more than 70% stenosis.

The two groups were compared for target artery percentage

stenosis below and above 75%.

Each graft type was further divided into subgroups ac-

cording to years after CABG as follows: less than 2, 2e5, 5e7,

7e10, 10e15 and more than 15 years post CABG. These sub-

groups were again compared for the percent stenosis of the

target artery.

2.3. Statistical analysis

The statistical analysiswas performed per conduit and not per

patient. Chi Square Test, pValues, Odds ratio, CI and z statistic

were calculated. In all tests, differences were considered not

significant when p > 0.05.

3. Results

In our study, of the total 1445 grafts 8.6% failed within 2 years,

13.8% failed within 5 years and 23.5% failed within 10 years.

72% of total grafts including LIMA, RIMA, SVG and LRA when




Fig. 1 e The left panel of the bar chart shows patency of total grafts (IMA, LRA and SVG together) when placed on target

arteries with less than or more than 75% stenosis. Majority of grafts fail when placed on arteries with less than 75%

stenosis. The right panel shows a breakup of specific graft types. IMA, SVG and LRA all respond to competitive flow similarly

with majority failing below 75% target artery stenosis.

a p o l l o m e d i c i n e x x x ( 2 0 1 4 ) 1e1 0 3

placed on coronary arteries with less than 75% stenosis failed

as compared to 22.8% grafts failing when placed on coronary

arteries with more than 75% stenosis with a p < 0.0001, Odds

ratio of 1.14, 95% CI of 0.60e2.15 and z statistic of 0.398 (Fig. 1

left panel).

When placed on target arteries with less than 75% stenosis,

67% of the internal mammary arteries (IMAs), 73.3% of the

SVGs and 75% of the LRA failed revealing no statistical dif-

ference in failure rates (p ¼ 0.4) (Fig. 1 right panel upper half).

This suggests that when faced with competitive flow all graft

types fail equally. In grafts placed on target vessels with more

than 75% stenosis, 86.8% of IMA and 83.5% of LRA were patent

as compared to70.7% of the SVGs. This suggests that the

arterial grafts are better conduits as compared to the SVG,

with IMAs being the champion (Fig. 1 right panel lower half).

In the subgroups broken down as years after CABG (<2,2e5, 5e7, 7e10, 10e15 and >15 years) significant number of

grafts regardless of graft type (IMA, SVG or LRA) failed when


placed on target arteries with less than 75% stenosis and

majority survived when placed on arteries with more than

75% stenosis. (Figs. 2e4) SVG showed higher failure rates as

graft age progressed.

4. Discussion

4.1. Competitive flow from moderately stenosed targetcoronary arteries causing graft failure

The issue of whether to graft coronary arteries with moderate

stenosis and what effect this has on the graft as well as native

coronary arteries has been discussed over the past two de-

cades. Barner and others found as early as the 1970s, a diffuse

reduction in the caliber of the Internal mammary artery (IMA)

graft which was called “disuse atrophy” because the native

coronary arteries to which the IMAs were anastomosed




Fig. 2 e The bar chart with breakup of the IMA grafts according to years after the CABG shows that significant numbers fail

when placed on target arteries with less than 75% stenosis irrespective of the time interval after CABG. The 7e10 and

10e15 years bars showing grafts patent on less than 75% target artery stenosis can be explained by factors such as

erroneous %stenosis on the ICA or graft supplying adjacent arteries with critical stenosis.


appeared to be patent and to have good flow thereby

rendering the graft useless.5,6 This phenomenon is now

commonly known as the “String Phenomenon” (Fig. 5).

Though other studies have shown that competitive flow

causes graft failure7,8 and does not increase the blood supply

to the myocardium in the region of the grafted coronary ar-

tery,9 there have been opponents of the competitive flow

theory who recommended grafting to moderately stenosed

coronary arteries. Canine experiments have shown that

arterial conduits grafted on fully patent native arteries

remained patent. However, patency was assessed at a

maximum of 2 months, which is not enough to predict the

long-term effect of competitive flow.10,11


In some of the earlier studies on potential predictive fac-

tors of IMA occlusion, control angiograms were obtained

relatively soon after CABG. Grafts on moderate stenosis were

found to be patent and recommended. However these studies

too did not address the long-term effect of flow

competition.12,13

In a large long term study between 1982 and 2002 Shah

et al. showed that target artery stenosis did not affect IMA

graft patency.14 This could be because only two broad cate-

gories of 60e79% and 80e99% stenosis of target arteries were

considered. If majority of grafts in the 60e79% group were on

79% stenosis it would not reflect the effect of a 60% target

artery stenosis on the grafts. In our studymajority of grafts on




Fig. 3 e Bar chart with breakup of the LRA grafts according to years after the CABG shows that significant numbers fail when

placed on target arteries with less than 75% stenosis irrespective of the time interval after CABG.


a target artery stenosis of 79% survived whereas on 60% ste-

nosis did not.

Glineur et al. have also divided patients into very broad

groups of native vessel percent stenosis, clubbing 65%e99%

stenosis together. It is not clear whether the grafts, which

survived, were closer to 65% or 99%.15

Sabik et al. found that internal thoracic artery graft patency

does decrease as coronary artery competitive flow increases.

However, they included diffusely narrowed grafts into the

patent category instead of the failed and therefore found that

the effect of competitive flow on ITA graft patency ismild, and

at no degree of proximal coronary stenosis is there a severe

decline in ITA patency. They therefore recommended

bypassing coronary arteries with moderate degrees of

stenoses.16

Manninen et al. found in their study that vein grafts were

more likely to fail on moderately stenosed target arteries


rather than arterial grafts. Contrary to this, we found that both

arterial and venous grafts shut down equally if placed on

insignificant stenosis. The string sign was not included in

graft failure by above workers. However, in the conclusion

they agree that if it were included then arterial and venous

grafts would appear to fail equally on insignificant percent

stenosis.17

4.2. Competitive flow from a graft placed on an adjacentartery or an adjacent ungrafted native artery causing graftfailure

We found that 0.01% of the LIMA, 0.02% of the SVG and 0.01%

of the LRA grafts failed because of competitive flow from

patent grafts to adjacent vessels or an ungrafted largely open

native coronary artery. In one of our cases with significant

proximal LAD stenosis, a LIMA placed on the LAD downstream




Fig. 4 e Bar chart with breakup of the SVG grafts according to years after the CABG shows that significant numbers fail when

placed on target arteries with less than 75% stenosis irrespective of the time interval after CABG. The 2 grafts, which appear

to survive on target arteries with less than 75% stenosis in the 2e5 year group, can be explained by factors such as

erroneous %stenosis on the ICA.


(at a level more distal) to a grafted diagonal branch failed, due

to flow competition when the diagonal ostium was not

significantly stenosed. Due to a relatively more proximal

positioning of the diagonal graft, there occurred a free

competitive flow through the diagonal graft into the diagonal

and thence to the LAD (Fig. 6).

A similar phenomenonwas observed in one of our patients

with critical Left main stenosis, where a LIMA to distal LAD

failed due to free flow from a graft on the early OM branch

located upstream, through the widely patent LCx ostium into

the LAD.

This is consistent with observations of Achouh et al.18


4.3. Graft failure when placed on occluded or criticallystenosed arteries

0.02% of LIMA and 0.1% [32/339] of SVGs in our study failed

despite landing on target arteries, which were occluded, or

more than 90% stenosed. Here the distal target segments

beyond occlusions or very tight stenosis were poorly opacified

on ICA and graft worthiness could not be assessed. Grafts

probably landed on diffusely diseased segments and occluded.

We found this phenomenon more commonly with the RCA

territory grafts. Myers et al. found, similarly that though pre-

operative ICA showed otherwise, coronary arteries could not




Fig. 5 e 3D volume rendered CTA shows a composite graft arrangement with the LIMA anastomosed to the Diagonal and

then to distal Left anterior descending (LAD). The LRA to Obtuse marginal branch of the left circumflex is anastomosed

proximally to the LIMA. The proximal LIMA segment connecting to the LRA is large calibered as it supplies a critical stenosis

in the circumflex. However the mid LIMA segment to the Diagonal is diffusely small calibered due to competitive flow from

the insignificant stenosis in the proximal LAD and the diagonal branch. The distal segment of the LIMA to LAD is once again

large caliber being supplied by the patent diagonal branch.

Fig. 6 e 3D volume rendered CTA. The LIMA to LAD is

occluded due to competitive flow from the SVG to the

diagonal branch located upstream from the point of LIMA

anastomosis to the LAD giving it a hemodynamic

advantage over the LIMA graft. The Distal LAD is now

supplied from free flow through the SVG to the diagonal via

a patent diagonal osmium (arrows).



be revascularized often with a plain CABG procedure after

making an arteriotomy due to extensive plaques.19

4.4. Graft survival on less than 75% target arterystenosis due to adjacent territory supply

0.1% of LIMA, 0.05% of SVG and 0.04% of LRA grafts in our

study survived on less than 75% target artery stenosis as they

were supplying the adjacent un-grafted but critically stenosed

artery. For example grafts on distal LAD that supplied the

critically stenosed but un-grafted Posterior descending artery

via collaterals around the cardiac apex survived even when

they were grafted on less than 75% LAD stenosis. A similar

phenomenon could be seen when Obtuse marginal grafts

supplied the Posterolateral branches of the Right coronary

artery or vice versa.

4.5. Graft survival on less than 75% target arterystenosis in chronic heavy smokers

In two of our patients who were chronic heavy smokers grafts

survived on less than 75% stenosis. This could be attributed to

severe micro-vascular disease in the myocardium upgrading

the need for revascularization.

4.6. Competitive flow due to inaccurate percentagestenosis on ICA causing graft failure

In our study, 21% (22/101) of the occluded IMA grafts, 11% (36/

339) of the occluded SVGs and 29% (15/51) of the occluded LRA

grafts that failed on target arteries with more than 75% ste-

nosis as seen on the preoperative ICA, revealed that on the




Fig. 7 e The left panel shows a volume rendered 3D CTA where the LIMA is anastomosed to the LAD. A composite LRA graft

is anastomosed proximally to the LIMA and distally sequentially to the two OM branches. The LIMA segment connecting to

the LRA is largely patent as it supplies the critical stenosis in mid circumflex. However the LIMA segment to the LAD

becomes string like and occludes distally due to the flow competition from the LAD. The right panel shows a curved

reconstruction through the LAD. The two calcified plaques cause only 40% stenosis of the LAD. On review of the ICA this

segment appeared 70% stenosed due to foreshortening of the artery.


post-CABG CTA the percentage stenosis of the target coronary

artery was in fact less than 75%. This inaccurate percent ste-

nosis on ICA caused competitive flow and subsequent graft

failure.

Several authors have questioned the accuracy and repro-

ducibility of ICA. Visual interpretation of the ICA exhibited

clinically significant intra-observer and inter-observer vari-

ability, with differences in the estimation of stenosis severity

approaching 50%.

Studies also reported major discrepancies between the

apparent angiographic severity of lesions and postmortem

histology.20

Due to tortuosity and foreshortening of arteries, moderate

coronary artery stenosis can sometimes appear severe on ICA

and grafts placed on such stenosis appear to fail due to “no

apparent reason” (Fig. 7). Similarly very significant stenosis

may appear moderate on ICA because of the morphology of

the lesion within the coronary arterial lumen. When such

arteries are grafted, the graft appears to survive on a moder-

ately stenosed artery whereas in fact it has survived on a

critically stenosed one.20

4.7. Accelerated atherosclerosis after CABG

When grafts occlude the native coronary arteries do not

remain as they were prior to grafting. CABG is associated with

accelerated atherosclerosis in the target artery segments

proximal to graft anastomosis with several proceeding to oc-

clusion.21,22 In fact, the site of PCI in post CABG patients is

significantlymore in the native coronary artery proximal to an


occluded graft as compared to a stenosed graft, coronary

stenosis distal to a patent graft or on a non-grafted vessel.18

Because of the diffuse nature of this accelerated disease, PCI

becomes challenging and even impossible in some cases.23 It

would therefore be judicious to not graft borderline stenotic

coronary arteries where a competitive flow would result in

graft occlusion and the native artery borderline stenosis

would progress to diffuse critical stenosis defeating the very

purpose of revascularisation.

4.8. Sign of competitive flow on CT

Competitive flow on ICA has been defined as a phenomenon

where the target coronary branch and anastomotic site are

clearly opacified in the native coronary injection, but not on

injection of the in situ graft.24 An adaptation of the same sign

can be seen on CTA. Grafts that are occluded from the prox-

imal anastomotic site upto the distal segment with only the

distal anastomotic site patent and opacified through the flow

in the borderline stenotic native coronary artery backing up

retrograde into the graft are a clear indicator of competitive

flow (Fig. 8).

4.9. Advantage of studying CABG failure by CTA vs. ICA

In ICA each graft and the native coronary arteries are injected

individually giving separate images, which then have to be

collated in the mind of the investigator to form the total pic-

ture. On the other hand CTA simultaneously demonstrates all

grafts and native arteries in a 3D format, which gives a




Fig. 8 e A, B, C: Panel A demonstrates competitive flow to the LIMA. In this 3D volume rendered image the heart and several

grafts have been faded into the background in order to bring attention to the Left main artery, LAD and the diagonal branch

together with its LIMA graft. The LIMA placed on the diagonal branch is occluded proximally. The distal segment of the

LIMA is opacified through flow from the insignificantly stenosed LAD and diagonal backing up retrogradely into the graft.

This may be considered a sign of competitive flow on CTA. Panel B and C demonstrate competitive flow to a vein graft. Panel

B shows a curved reconstruction through the thrombosed SVG graft and demonstrates the distal anastomotic site that

remains patent due to retrograde competitive flow from the OM branch (arrow). Panel C shows a 3D volume rendered image

with patent LIMA graft to LAD, patent SVG to Diagonal and an occluded SVG to OM. The distal anastomosis and the distal

most bit of the SVG graft to OM is opacified by the retrograde flow through the insignificantly stenosed OM branch.


panoramic and global view of the heart and its conduits. The

diffuse critical narrowing of one graft in comparison with a

largely patent adjacent graft clearly demonstrates graft fail-

ure. A widely patent native artery with its failed graft seen

simultaneously leaves no doubt as to the cause of the graft

failure.

4.10. Recommendations for future research

Large prospective trials may be conducted with CABG based

on percentage stenosis measured by cross sectional preoper-

ative CTA image with the help of calipers and usingminimum

luminal diameter and adjacent normal reference vessel

diameter. Graft failure can then be assessed on follow up CTA

to ascertain the cutoff value of percent stenosis or minimum

luminal diameter below which competitive flow would occur

causing graft failure. CABG recommendations should ideally

be based on cross sectional imaging like CTA.

In conclusion, ours is the first study that assesses CABG

failure due to competitive flow by CTA. It proves that CABG to

coronary arteries that have less than 75% stenosis causes

chronic competitive flow to the graft from the target coronary

artery resulting in reduced flow through the graft. This slow

flow causes reduction in graft caliber and eventual graft oc-

clusion. Arterial as well as venous grafts succumb to

competitive flow equally and fail. To add to this dilemma,

inaccurate percentage stenosis on ICA caused by myriad fac-

tors may cause arteries with insignificant stenosis seem sig-

nificant enough to be grafted resulting in graft failure. Hence

pre CABG assessment of coronary arteries with CTA and true

stenosis measured with calipers on cross section images


would be worthwhile to decide which arteries need grafting.

Arteries with moderate stenosis may be left ungrafted and

medically managed till they do need intervention in the form

of stenting.

Funding received

We received no support from any organization for the sub-

mitted work, have no financial relationships with any orga-

nizations that might have an interest in the submitted work

and no other relationships or activities that could appear to

have influenced the submitted work.

Conflicts of interest

All authors have none to declare (Ref.JSS).

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coronary artery bypass graft failure and its relationship to target artery percentage stenosis and...

Health & Medicine

causes of graft failure

graft types

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