(Circulation. 2000;101:2355.)
© 2000 American Heart Association, Inc.
Clinical Investigation and Reports |
Intracoronary ß-Irradiation With a Liquid 188Re-Filled Balloon
Six-Month Results From a Clinical Safety and Feasibility Study
From the University of Ulm, Department of Cardiology (M.H., J.W., M.W., H.H., R.V., H.H.O., M.K., V.H.) and Department of Nuclear Medicine (S.N.R., J.K.), Ulm, Germany.
Correspondence to Martin Höher, MD, University of Ulm, Department of Cardiology, Robert-Koch-Straße 8, 89081 Ulm, Germany. E-mail martin.hoeher{at}medizin.uni-ulm.de
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Abstract |
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Background—Coronary irradiation is a new concept to reduce restenosis. We evaluated the feasibility and safety of intracoronary irradiation with a balloon catheter filled with 188Re, a liquid, high-energy ß-emitter.
Methods and Results—Irradiation with 15 Gy at 0.5-mm tissue depth was performed in 28 lesions after balloon dilation (n=9) or stenting (n=19). Lesions included 19 de novo stenoses, 4 occlusions, and 5 restenoses. Irradiation time was 515±199 seconds in 1 to 4 fractions. There were no procedural complications. One patient died of noncardiac causes at day 23. One asymptomatic patient refused 6-month angiography. Quantitative angiography after intervention showed a reference diameter of 2.77±0.35 mm and a minimal lumen diameter of 2.36±0.43 mm. At 6-month follow-up, minimal lumen diameter was 1.45±0.88 mm (late loss index 0.57). Target lesion restenosis rate (>50% in diameter) was low (12%; 3 of 26). In addition, we observed 9 stenoses at the proximal or distal end of the irradiation zone, potentially caused by the short irradiation segment and the decreasing irradiation dose at its borders ("edge" stenoses). The total restenosis rate was 46% and was significantly lower (29% vs 70%, P=0.042) when the length of the irradiated segment was more than twice the lesion length.
Conclusions—Coronary irradiation with a 188Re-filled balloon is technically feasible and safe, requiring only standard percutaneous transluminal coronary angioplasty techniques. The target lesion restenosis rate was low. The observed edge stenoses appear to be avoidable by increasing the length of the irradiated segment.
Key Words: angioplasty • coronary disease • radioisotopes • restenosis
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Introduction |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Restenosis is a major limitation of coronary angioplasty. Its biology includes inflammation, proliferation, and migration of smooth muscle cells and remodeling of the vascular wall.1 Local irradiation has been shown to inhibit neointima formation in animal experiments.2 3 4 Initial trials using
-sources
indicated the clinical effectiveness of coronary
brachytherapy.5 6 In a first randomized trial, Teirstein
et al6 showed a significant reduction of the
restenosis rate after intracoronary -irradiation of
dilated restenotic lesions. Recently, they demonstrated the
persistence of the initial effect and a significantly lower event rate
after 2 years.7 Promising angiographic results have also
been reported with 90Sr/90Y
ß-irradiation.8 9 A procedural advantage of
ß-radiation is its low penetration depth, minimizing the ionizing
exposure of both the patient and the operator. However, the fast
decrease of ß-radiation energy within 2 to 5 mm has raised the
question of an inhomogeneous dose delivery to the vascular
tissue and the need for centering the radiation device. 188Re is a high-energy ß-emitter available in liquid form. The purpose of this study was to evaluate the feasibility and safety of intracoronary ß-irradiation with a liquid 188Re-filled balloon.
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Methods |
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This study was approved by the local ethics committee and the German radiation authorities. Inclusion criteria were written informed consent; age 18 to 80 years; ischemia by symptoms or exercise testing; intended angioplasty of a native coronary artery or a bypass graft; and a reference vessel diameter suitable for a 3.0-mm irradiation balloon. Exclusion criteria were acute myocardial infarction, unprotected main stem disease, strong vessel tortuosity, pregnancy, contraindication to aspirin, ticlopidine or heparin, and illness limiting the survival within 6 months.
Radiation Source and Dosimetry
Liquid 188Re is a high-energy ß-emitter
that is available daily from the
188W/188Re generator (Oak
Ridge National Laboratory, Oak Ridge, Tenn) and has a half-life of 17
hours. The ß-particles have a maximal energy of 2.12 MeV and a mean
energy of 764 keV. A principle -ray component of 155 keV accounts
for 15% of the radiation intensity and allows excellent control of
contamination.
Before this clinical trial, we performed detailed in vitro studies to evaluate the dosimetry of a liquid 188Re-filled angioplasty balloon catheter.10 The dose decrease with increasing distance from the balloon surface was measured and compared with expected values derived from the point kernel function of 188Re in water.11 Very good correlation was demonstrated for the energy dose deposited and the fast dose decrease to 50% at 0.5 mm distance and to 10% at 2.5 mm distance from the balloon surface. From these data, the irradiation times required for a targeted dose can be calculated, dependent on the size of the irradiation balloon and the actual specific volume of 188Re.
Irradiation times were calculated to deliver 15 Gy in a tissue depth of 0.5 mm. This corresponds to a dose of 30 Gy at the surface of the balloon. Potential variations in dose delivery caused by minor differences between the actual and the nominal diameter of the irradiation balloon are <10%.10 12
Carrier-free 188Re (perrhenate) was obtained from
a 188W/188Re generator by
elution with saline and was concentrated by anion exchange columns to a
specific volume of 1.7±0.6 GBq/mL (46.5±16.6 mCi/mL).13
A volume of 1.3 mL was filled into a 3.0-mL syringe shielded with 5-mm
plastic. Because of the -radiation component, a lead container was
used for transportation.
Previously, we have demonstrated that in the exceptional event of balloon rupture, perchlorate can be administered orally to block the thyroid and gastric mucosa and to reduce the radiation burden to an effective dose of 0.16 mSv/MBq 188Re.14 Perchlorate was not used prophylactically.
Irradiation Procedure
All patients were pretreated with 100 mg/d aspirin for 
5 days.
They received a 10 000-U bolus of heparin before angioplasty, adjusted
to the activated clotting time (>280 seconds). Aspirin (100
mg/d) was continued throughout the study. Patients with stents
additionally received 250 mg ticlopidine BID for 6 weeks. Irradiation
was carried out after successful angioplasty with or without stenting.
Patient inclusion was based on on-line quantitative coronary
angiography. Only patients with a vessel size suitable for a 3.0-mm
balloon and an ischemic tolerance of 1 minute during the
preceding angioplasty received irradiation.
For irradiation, the angioplasty balloon was replaced by a noncompliant
balloon of the same diameter and the same length equipped with a
proximal and distal radio-opaque marker (Tacker, Cordis
Europe). During intermittent contrast injections from the guiding
catheter, indicating the position of the lesion and of landmark side
branches, the deflated balloon was positioned, covering the target
lesion and matching the position of the previous angioplasty balloon.
The 188Re-filled syringe and an empty 50-mL
syringe were connected to the balloon by a 3-way valve (Figure 1
). With the empty syringe, a negative
pressure was applied to the balloon. Afterward, the valve was closed
and the empty syringe was replaced by a stopper. The 3-way valve was
operated with a 10-cm plastic stick. For irradiation, the balloon was
manually inflated with an approximate inflation pressure of 3 to 4 atm.
Because of the low viscosity of the liquid 188Re,
this procedure is sufficient for complete filling of the balloon
without bubbles, as we know from our in vitro trials. During inflation,
the ECG and anginal symptoms were attentively observed. Inflation was
stopped and dose delivery was fractionated in the case of severe
anginal pain, marked ST-segment changes, decrease of blood pressure, or
frequent ventricular arrhythmias. When the
irradiation had to be fractionated, the balloon was deflated for 3 to 5
minutes but left in place across the target stenosis to avoid
shifts of the balloon and to minimize radiation exposure to other
areas. After irradiation, the balloon was removed with forceps, and the
whole system including the shielded syringe was brought back to the
department of nuclear medicine for decay. Finally, the
catheterization laboratory was checked for radiation
contamination.
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Study Design
Patients scheduled for coronary angioplasty were
informed and gave their written consent for intracoronary
irradiation and angiographic follow-up examination. In this safety and
feasibility trial, no restrictions were made according to
restenosis, bypass grafts, or total occlusions. The inclusion
of patients into the study was done after successful angioplasty.
Clinical follow-up was performed after 3 months and angiographic
follow-up after 6 months.
Quantitative Coronary Angiography
Coronary angiography before and after angioplasty and at
follow-up was performed in the same projections of the treated
lesion after intracoronary glycerol-trinitrate. Angiographic
measurements were done with the Pie Medical software 2.1 (Pie Medical
Imaging). Each projection calibration was done from the unfilled
guiding catheter.
Statistical Analysis
Continuous variables are presented as mean±SD and
compared with the unpaired Mann-Whitney U test or the paired
Wilcoxon test. Discrete variables were expressed as counts
and percentages and compared by means of 
2
analysis. Statistical significance was set at the 5% 
-error
level (P<0.05).
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Results |
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Between December 1997 and August 1998, 28 patients received irradiation after successful coronary angioplasty. Lesions were located in the left anterior descending coronary artery (n=9), the circumflex artery (Cx, n=8), the right coronary artery (n=10), and a bypass graft (n=1). In 17 patients, stenting was done before irradiation and in another 2 patients, stenting was performed afterward. Abciximab was given in 7 of 28 patients.
Irradiation was done with 3.0-mm (n=16) and 3.5-mm (n=12) balloons, with a length of 20 mm (n=24), 30 mm (n=3), and 40 mm (n=1), sufficient to cover the whole lesion. The irradiation balloon was selected with the same diameter and length as the angioplasty balloon. In all patients, the prescribed dose of 15 Gy was delivered. The mean irradiation time was 515±199 seconds (range 220 to 990). Irradiation was performed in 1 fraction (n=12), 2 fractions (n=7), 3 fractions (n=7), and 4 fractions (n=2) to limit ischemia. There were no adverse effects of the irradiation procedure except anginal pain and ST-segment changes. There was no radiation leakage within a patient. One minimal leak of the 3-way valve contaminated only the underlying water-resistant drape.
Clinical and Procedural Data
The study collective consisted of 18 men and 10 women with a mean
age of 63.4±12.7 years. Four patients had diabetes mellitus, 16 had
hyperlipidemia, 18 had hypertension, and 14 had a
history of smoking. Single-vessel disease was present in 9
patients, 2-vessel disease in 14 patients, and 3-vessel disease in 5
patients. Left ventricular ejection fraction was 68±15%.
Ten patients had a recent myocardial infarction; 11 patients had
unstable angina. There were 19 de novo stenoses, 4 occlusions,
3 restenoses, and 2 in-stent restenoses. Lesion
morphology included 13 type A/B1 and 15 type B2 lesions. Nonoccluded
lesions were predominantly eccentric (n=19). Angioplasty before
irradiation was performed with 1 balloon inflation in 4 lesions, with 2
inflations in 8 lesions, and with 3 inflations in 16 lesions (mean
3.0±1.8 inflations).
The mean lesion length was 11.8±4.3 mm (range 6.0 to 25.0). Six patients had minor vessel calcifications; no vessel was heavily calcified. Angioplasty resulted in an acute gain of 1.74±0.59 mm. The mean ratio of the irradiation balloon diameter to the reference diameter after angioplasty was 1.17±0.13 mm (range 0.93 to 1.49) and to the largest angioplasty balloon used was 1.07±0.09 mm (range 1.0 to 1.2). The mean difference of the length of the irradiation balloon and the length of initial lesion was 11.1±3.6 mm (range 3.7 to 18.6). The mean ratio of the length of the irradiation balloon to the lesion length was 2.21±0.63 (range 1.23 to 3.36).
Follow-Up Data
There were no in-hospital complications related to the
coronary intervention. One 76-year-old male patient died 23
days after stenting and irradiation of the right coronary
artery as the result of kidney failure after unsuccessful
percutaneous transluminal angioplasty of a renal
artery. Autopsy was declined by his relatives. The remaining 27
patients were followed up for 6 months. Clinical follow-up after 3
months revealed no further death, no myocardial infarctions, and no
revascularizations. After 6 months, there were
still no further deaths but 1 myocardial infarction caused by a late
stent thrombosis 109 days after stenting and irradiation. This patient
also had received ticlopidine for the protocol specified for 6 weeks,
as specified by the protocol. At 6 months, 13 patients were
asymptomatic and 13 had stable angina. One
asymptomatic female patient with a negative stress test
declined follow-up angiography 6 months after angioplasty and
irradiation of the Cx.
Follow-up angiography was performed in 26 patients after 177±27 days.
Figure 2 shows an example of a good
6-month result after angioplasty and irradiation of the Cx. The
dichotomous restenosis rate (>50%) restricted to the target
lesion was only 12% (3 of 26). In terms of the lesion type, target
lesion restenosis occurred in 1 de novo lesion, in 1 occlusion,
and in 1 restenosis.
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Additionally, we observed 9 newly developed stenoses (average
78±16%) outside of the target lesion located at the proximal or
distal end of the irradiation zone (Figure 3). Thus, the overall stenosis
rate at follow-up was 46% (12 of 26). There was no significant change
of the reference diameter. Including both target lesion
restenoses and newly developed "edge" stenoses at
the end of the irradiation zone, the mean late lumen loss was
0.91±0.81 mm and mean late loss index was 0.57±0.57
(Table). Repeat PTCA was performed in a total of
6 (23%) patients: 1 patient with target lesion restenosis and
in 5 patients with edge stenoses.
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A low restenosis rate was observed in proximal lesions (11%, 1 of 9) and in stented de novo stenoses (21%, 3 of 14). High restenosis rates were seen in the small groups of previously occluded (75%, 3 of 4) or restenosed (50%, 2 of 4) vessels.
To gain further insights into the mechanisms of edge stenoses,
we analyzed the ratio of the length of the irradiation balloon
to the length of the lesion, that is, the extent to which the
irradiation balloon exceeded the stenosed area. The restenosis
rate was significantly lower in patients in whom this ratio exceeded 2
compared with those with a ratio below 2 (Figure 4).
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Discussion |
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Local irradiation from different sources has been shown to inhibit neointima formation in animal experiments.2 3 4 Thus far, 4 human studies of intracoronary brachytherapy have been reported.5 6 7 8 15 Condado et al5 and Teirstein et al6 7 showed a reduction of late lumen loss and a lower restenosis rate at 6 months and during 2 to 3 years of follow-up with
-irradiation from a 192Ir
source. Verin et al15 demonstrated the technical
feasibility of intracoronary ß-irradiation with an 18-Gy
inner arterial surface dose applied from a centered
90Y wire but did not find an obviously reduced
restenosis rate at the treated site (6 of 15, 40%). Recently,
King et al8 showed a low restenosis rate of 15%
(3 of 20) of the target lesion after intracoronary
ß-irradiation with 12 to 16 Gy at 2-mm distance from the center of a
90Y source. In addition, they found some positive
remodeling of the treated segments in 9 of the 20 patients but no
aneurysms.
This study is the first report the use of a liquid
188Re-filled balloon catheter for
intracoronary irradiation in humans. We demonstrated the
technical feasibility (100%) and the safety of this new technique.
With the use of standard PTCA technology, coronary
188Re brachytherapy could be performed with low
additional technical efforts. Like other high-energy ß-emitters,
188Re allows us to apply a high focal radiation
dose over a short period of time. Because of its low penetration depth,
the use of ß-radiation reduces the ionizing exposure of the patient
and the operator and requires less effort for radioprotection in the
catheterization laboratory compared with -sources.
Features of 188Re, facilitating
intracoronary application, are the high ß-energy, its liquid
form, and the short half-life of 17 hours with daily availability from
the 188W/188Re generator.
Filling a conventional balloon catheter with liquid
188Re results in a self-centering irradiation
source independent from bending of the artery, cardiac motion, and
stenosis morphology. When the size of the radiation balloon is
matched to the diameter of the artery, there is direct contact between
the radiation source and the inner vessel wall. This results in equal
and predefined radiation doses at equidistant points from the luminal
surface of the vessel independent from the vessel size. The
188Re-filled balloon therefore avoids the problem
of centering a thin radioactive wire within the vessel. However, it
does not affect the characteristic fast radial dose decrease of
ß-radiation in contrast with -radiation, resulting in a
significantly lower dose at the deeper adventitial layers compared with
the luminal surface.
The dose prescribed in this initial feasibility trial of liquid
188Re was chosen from the following
considerations: Teirstein et al6 showed a significant
effect with 26.5±3.5 Gy at a distance of 1.02±0.16 mm from the
ribbon source to the target lesion. This corresponds to our dose of 30
Gy at the balloon surface in contact with the luminal vessel side.
Compared with the pilot study of Verin et al15 that found
no impressive effect with 18 Gy at the inner vessel side, our dose was
chosen 50% higher. In this first feasibility trial with
188Re, we took care to avoid radiation induced
pseudoaneurysms that previously had been described by Condado
et al5 with a recalculated dose of 38.5 Gy delivered at a
distance of 1.5 mm from the radioactive wire. Although the risk
for developing pseudoaneurysms might be much less with
low-penetrating ß-radiation and the fact that Condado et al
considered it likely that the treated site received up to 92 Gy, we
decided to stay below the limit of 38 Gy at the balloon surface. With
regard to the fast dose decrease of ß-radiation, we accepted a low,
potentially inadequate dose in the deeper, adventitial layers. Prior
animal studies from Waksman et al16 showed that with a
dosage of 14 Gy at 2 mm from the radiation source, the effect of
ß- and -radiation on the suppression of neointima
formation was comparable. However, when delivering radiation from a
centered wire source, the artery is not expanded to 3.0 mm and
therefore the tissue dose at a 2-mm radius from the source center is
probably higher at least in some portions of the arterial
wall compared with the 15 Gy dose in 0.5-mm tissue depth of this
study.
Our 6-month angiographic results after 188Re
irradiation were characterized by 2 aspects: The target lesion
restenosis rate was only 12%, which is comparable to the
results from the BERT feasibility trial,8 showing a 15%
restenosis rate at the target lesion. However, a disappointing
finding of this feasibility study was the high incidence (35%) of new
edge stenoses, increasing the overall restenosis rate
to 46%. Including these edge stenoses, late lumen loss was
0.57 in this trial and comparable to the results from Verin et
al15 (
0.50). Such edge stenoses could be due to
a low irradiation dose within a traumatized vessel segment. A
proliferative tissue response has been described with low dose
192Ir irradiation of 10 Gy applied before balloon
overdilation in a pig model4 and after external x-ray
application.17 However, edge stenoses have not
been described from the BERT trial,8 9 18 although the
authors applied very similar ß-irradiation doses. Recently
Sabaté et al19 analyzed the volumetric
changes after irradiation according to the BERT trial with the use of
3D ultrasound. They also found a reduced effect at the edges with a
decrease in luminal volume due to an increase in plaque volume and no
net change in external elastic membrane volume, but only 1 of 21
lesions showed an angiographic edge stenosis.
Our data indicate that the occurrence of edge stenoses is significantly influenced by the extent to which the irradiated segment is longer than the dilated lesion. In this study, the 188Re balloon had the same length as the dilation balloon. With a mean balloon length of 21.8±4.8 mm (range 20 to 40 mm), the irradiated segment was shorter than in the BERT trial, in which a 30-mm delivery system was used. Mean lesion length was slightly longer (11 mm) in this study compared with BERT (9 mm). Possibly, a decreasing dose at the ends of the balloon applied in an already traumatized tissue segment triggers a proliferative response. In this study, a mean of 3.0±1.9 balloon inflations were performed during angioplasty before irradiation. Because of slight shifts of the angioplasty balloon, the traumatized segment can be expected to be even longer than the simple length of the dilation balloon.
There are some other factors that potentially reduce the effective tissue dose. Two thirds of the patients received coronary stents before irradiation. Experimental studies indicate that stents reduce the radiation dose by 4% to 14%, depending on the stent type.20 We did not correct the irradiation dose with and without stenting. However, assuming a maximum dose reduction of 14%, the remaining dose of 12.9 Gy would still have been in the dose range applied in the BERT trial. Furthermore, ß-radiation is shielded by calcium. Although there were no heavily calcified lesions in this study, it should be mentioned that angiography has a limited sensitivity for inhomogeneous, focal calcific deposits.21 As a safety and a feasibility study, this trial was not restricted to certain lesion types. Although the case numbers were small, restenoses were frequent (5 of 8) in previously restenosed and occluded lesions. Because of the fast dose decrease of ß-radiation within the vessel wall, it cannot be excluded that in lesions with a high plaque burden the effective dose to the proliferating tissue elements might have been too low.
Study Limitations
The number of patients in this feasibility trial was limited. The
study did not include a control group and thus was not randomized.
Because of the lack of the control group, we could not prove the
efficacy of 188Re irradiation, and it remains
open whether the low target lesion restenosis rate is indeed
due to the irradiation procedure. Concerning the safety of this new
method, our study is limited to the procedural results and 6-month
follow-up. Because of the geometry of the
188Re-filled balloon, the dose was homogenous at
the inner vessel surface. However, we did not use intravascular
ultrasound to evaluate plaque burden and did not adapt the prescribed
ß-irradiation dose to vessel wall thickness.
Hypoxia reduces the biological effect of radiation in malignant tissue.22 This raises the question whether radiation delivered from an inflated balloon is less effective than irradiation from a nonoccluding device caused by compression of the vessel wall and compromise of the vasa vasorum. However, our previous animal studies with the 188Re-filled balloon showed a significant reduction of neointimal hyperplasia with 7.5 Gy in 0.5-mm tissue depths, which is comparable to the data from nonoccluding ß-emitting catheters.2 Furthermore, it is unclear which degree of hypoxia is reached in the vessel wall and whether oxygen concentration in the target cells is low enough (0.02%) to diminish radiation-induced formation of DNA strand breaks,22 taking into account the short duration of balloon inflations (mean 262±140 seconds), the low inflation pressure (3 to 4 atm), and the anatomy of vasa vasorum in the adventitia.23
With the use of a liquid- filled, radioactive balloon, there is always a decreasing irradiation dose at the edges of the balloon. From our data, delivery of such a decreasing dose in a diseased segment traumatized by angioplasty predisposes for the development of edge stenosis. Usage of longer radioactive balloons exceeding the traumatized segment should limit the occurrence of edges stenosis, shifting the dose decrease at the edge of the balloon into nontraumatized segments. Low-pressure inflation of the radioactive balloon alone will not cause new vessel trauma, as we know from vessel occlusion during angioscopy.24
Conclusions
Coronary irradiation with a
188Re-filled balloon is technically feasible and
safe. The target lesion restenosis rate was low. The observed
edge stenoses appear to be avoidable by increasing the length
of the irradiated segment. A randomized trial is warranted to evaluate
the efficacy of 188Re brachytherapy.
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Acknowledgments |
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This study was supported by the Deutsche Forschungsgemeinschaft (SFB 451-B6).
Received September 29, 1999; revision received December 1, 1999; accepted December 22, 1999.
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