Restenosis and occlusion after carotid surgery assessed by duplex scanning and digital

subtraction angiography.
V Zbornikova, J Elfstrom, C Lassvik, I Johansson, J E Olsson and U Bjornlert

Stroke. 1986;17:1137-1142
doi: 10.1161/01.STR.17.6.1137
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 CELL DENSITY AROUND SMALL BRAIN INFARCTS/Nedergaard et al 1137

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of brain infarcts? The penumbra zone. Acta Neurol Scand, in press
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Neurosurg 56: pp 482-497, 1982

Restenosis and Occlusion After Carotid Surgery Assessed by

Duplex Scanning and Digital Subtraction Angiography
VERA ZBORNIKOVA, M . D . , P H . D . , * JOHAN ELFSTROM, M . D . , P H . D . , ! CLAES LASSVIK, M . D . , P H . D . , $

INGEGERD JOHANSSON, M . D . , § JAN-EDVIN OLSSON, M . D . , P H . D . , * AND U L F BJORNLERT, M.D.H

SUMMARY In a study of 140 patients operated upon with 143 carotid endarterectomies (mean follow-up
time 5.2 ± 2.3 years, range 1 month — 9.3 years), vessel morphology was examined with duplex scanning in
113 patients and with digital subtraction angiography (DSA) in 82 patients. The operative mortality was
1.4%; persisting stroke morbidity 3.6% and the combined operative mortality/morbidity 5%. During the
follow-up time a further 20 patients (14.5%) died, 13 had new strokes and 14 new TIAs. By life table
analysis, the annual rate of stroke including the operative period was 2.7% (1.7% on the operated side and
1.0% on the non-operated side). Fourteen new occlusions (12%) of the operated carotid artery was found
and restenosis (>50%) in 13 patients (11.2%). Progression of the atherosclerotic disease in the contralaterai
non-operated carotid artery was found in 41 patients (37%) including 3 new occlusions. Agreement DSA/
duplex was 88% on the operated side and 92% on the non-operated side. New strokes or TIAs on the
operated side were more common in patients with occlusions or restenosis (p < 0.05), whereas no symptoms
were referable to occlusions on the non-operated side. Risk factor analysis revealed an increased risk of
atherosclerotic progression on the non-operated side in smokers and those with two or more risk factors.
The risk of restenosis in the operated carotid artery was higher in females (p < 0.025).
Stroke Vol 17, No 6, 1986

MORPHOLOGICAL AND HAEMODYNAMIC
CHANGES in extracranial arteries following endarter-
ectomy have not been extensively investigated, since
serial angiography examinations involve a certain
risk.' • 2 The rate of restenosis > 50% of diameter reduc-
tion/occlusion has previously been investigated pre-
dominantly in patients with recurrent neurological
symptoms and is reported to amount to 1-5%. w Using
continuous wave Doppler, the incidence of restenosis
> 5 0 % and occlusion has been reported to be 36% after
a mean observation time of 6 years. 6 A combination of
From the Departments of Neurology,* Surgery,t Clinical Physiol-
ogy, t Diagnostic Radiology,§ University Hospital, Linkoping, and the
Department of Diagnostic Radiology,11 Motala Hospital, Motala,
Sweden.
This study was supported by grants from County Council of Ostergot-
Iand, Mutual Group Life Insurance Company, Stockholm, Tore Nils-
son's Foundation, and Lion's Foundation.
Address correspondence to: VeraZbomikova, M.D., Ph.D., Depart-
ment of Neurology, University Hospital, S-581 85 Linkoping, Sweden.
Received January 28, 1986, revision # 1 accepted July 7, 1986.
2-D image and pulsed Doppler, so-called duplex, of-
fers the advantage of providing both anatomical and
haemodynamic information ahd makes possible the
detection of stenosis less than 50%.7> 8 The validity of
this method has also been demonstrated in patients
after endarterectomy in comparison with postoperative
angiogram.9 With this technique, the incidence of re-
stenosis >50%/occlusion has been reported to be
19%10 after a mean observation time of 16 months.
A new semi-invasive method, digital subtraction an-
giography (DSA), has gained wide use during recent
years and is still under evaluation although hitherto the
reported results are less accurate compared to conven-
tional angiography."" 13
The aim of the present study was to evaluate the
frequency of restenosis or occlusion after carotid end-
arterectomy (CE), the possible correlation between
morphological changes and recurrent symptoms and
the possible influence of vascular risk factors on these
events.
There are few published investigations on the natu-
ral course of asymptomatic carotid artery lesions.14

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1138 STROKE
The contralateral non-operated artery was therefore
studied as well in order to elucidate this problem.
Materials and Methods
Patients
At the University Hospital, Linkoping, Sweden,
143 carotid endarterectomies were performed in 140
patients during the period 1974-82. One hundred and
thirty-seven patients had unilateral operation and three
bilateral. There were 111 males and 29 females with a
mean age 61 ± 7.7 years. Neurological investigation
including angiography and selection of candidates for
surgery was done at the Department of Neurology.
Fifty-nine patients (42%) had transient ischemic at-
tacks (TIA) and 74 (53%) minor stroke; all selected to
carotid lesions on the operated side. Seven patients had
asymptomatic stenosis with a high degree lesion on the
contralateral side. In the latter category, the operation
was done in order to improve intracranial haemody-
namics. The ratio left/right CE was 76/67.
All patients had angiogTaphy, the majority both se-
lective common carotid angiography and arcus arch
angiography. Plaques with stenosis <15% diameter
reduction were found in 18 patients, stenosis 16—49%
in 30 patients, stenosis 50-75% in 28 patients, and
stenosis 76-99% in 64 patients. On the contralateral
side, high grade lesions were noted in 16 vessels; ste-
nosis 50-75% in 9 vessels, stenosis 76-99% in 5 ves-
sels and in 2 vessels occlusion was found.
Established vascular risk factors were the following:
treated arterial hypertension in 81 patients (58%), dia-
betes mellitus in 11 (8%) and smoking in 84 patients
(60%), angina pectoris in 26 patients (19%) and pre-
vious myocardial infarction in 8 patients (6%). Periph-
eral vascular disease was present in 11 (8%) and hyper-
lipidemia in 29 patients (21%). One hundred and
thirteen patients were treated with anticoagulant drugs
(AC) before, and approximately 2-3 months after op-
eration. Fifteen received antiplatelet drugs and the re-
maining patients were without antithrombotic therapy.
The operations, performed by three vascular sur-
geons, were conventional endarterectomies. Intralu-
minal shunt was used in 106 patients.
After thrombendarterectomy all patients were reex-
amined by a neurologist within one week, after three
months and thereafter yearly. At follow-up investiga-
tion in 1983-84, 118 patients, representing 121 CE,
were available. The examination included neurologi-
cal status, filling in of a special questionnaire, duplex
scanning of the carotid vessels and periorbital Doppler
examination. All medical records from the Depart-
ments of Surgery and Neurology were available in-
cluding those of patients who died. When a patient
died at another hospital, the death certificate and a
copy of the medical record was requested. The mean
observation time between operation and examination
was 5.2 ± 2.3 (SD) years, (range 1 month-9.3 years).
Only 8 patients, of whom 4 had died, were observed
less than 2 years. All patients were advised to perform
DSA, but 20 refused.
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VOL 17, No 6, NOVEMBER-DECEMBER 1986
Duplex Scanning
Duplex scanning was performed in 113 patients.
The duplex scanner (ATL Mark 500) was equipped
with a combined 7.5 MHz short focus transducer used
for two-dimensional echo image and a 5 MHz short
focus variable single-gate pulsed Doppler with Fast
Fourier spectral analysis in the same scan head, as
described earlier.8
The duplex findings were classified as follows: (1)
normal: a narrow spectral flow curve throughout systo-
le and no visible plaques; (2) stenosis <15%: slight
spectral broadening in the decelerating phase of systole
and/or small wall irregularities; (3) stenosis 16-49%:
spectral broadening throughout systole, velocity up to
1.2 m/sec; (4) stenosis 50-75%: velocity exceeding
1.2 m/s; (5) stenosis 76-99%. Subgrouping into these
two last categories was done using the following equa-
tion: y = 45.8 ± 7.19 peak systolic velocity (m/sec)
+ 4.8 late diastolic velocity (m/sec) + 7.2 the result
of periorbital Doppler (coded as normal = 0 and ab-
normal = 1); (6) occlusion: no signal detected in the
imaged vessel and usually low diastolic flow close to
zero in common carotid artery.8
Digital Subtraction Angiography
DSA was performed in 82 patients with a Techni-
care DR 960. For each imaging sequence, 40 ml bolus
of iodinated contrast media was injected into the cen-
tral venous system. A routine DSA study included two
oblique views of die carotid arteries and, in case of
vessel superimposition, additional projections were
performed. The stenosis was measured as the greatest
percentage reduction of the lumen diameter seen in any
projection. DSA could not be carried out because of
contrast allergy in 5 patients, increased creatinine level
in two patients and technical problems in a further two
patients. In two patients, the images were uninterpreta-
ble due to motion artifacts. Twenty patients did not
accept the investigation, and in two symptomatic pa-
tients, conventional multiplane arteriography was per-
formed instead of DSA.
DSA results were classified into the following cate-
gories: (1) normal, (2) stenosis 1-49%, (3) stenosis
50-75%, (4) stenosis 76-99% and (5) occlusion.
Statistical Methods
The Chi-square test and life table analyses were used
for statistical evaluation.
Results
Clinical Events
The longitudinal course of clinical events is present-
ed in table 1.
Early Perioperative Period
During the operation and in the week following the
operation, 6 patients had TIA/RIND and 7 patients had
a stroke; in the latter group two patients died within 5
weeks after the operation. Thus the peri-operative
mortality was 1.4%, persisting morbidity 3.6% and
combined mortality-morbidity 5%.
 DUPLEX AND DSA AFTER CAROTID SURGERYIZbornikova et al 1139

TABLE 1 The Longitudinal Course of Clinical Events

Operated side Non-operated side
Penoperatively
n = 140 6TIA 0
7 stroke
(2 deaths)
Late follow-up
dead 1 stroke 2 stroke (1 VB)
n = 20
(+ 2periop)
Not examined 1 TIA 1 TIA
n = 5
Follow-up examinations 10TIA 4T1A(1 VB)
n = 113 5 stroke 5 stroke (1 VB)
n = 140 (143 CE). VB = vertebrobasilar.
Recurrent Symptoms
During the follow-up period (mean 5.2 ± 2.3 years,
range 1 month — 9.3 years) of the remaining 138
patients, a further 20 patients died (14.5%), three of
whom had experienced stroke; one on the operated
side, one from the contralateral side and one from the
vertebral-basilar territory. The latter patient died due
to brainstem infarction, but the other patients died
from causes other than neurological — myocardial
infarction (13), neoplasm (1) and from other causes
(5). Of the 118 surviving patients, 5 could not partici-
pate in the study, one of whom suffered from sequele
after subarachnoid haemorrhage and another patient
had had TIA from the operated side and from the
vertebral-basilar system. The remaining three patients
were asymptomatic.
Thus 113 patients were able to attend the complete
follow-up examination. Among these patients, 10
(8.9%) had experienced stroke and 14 (13.2%) TIA. In
5 patients with stroke (4.3%) and 10 patients with TIA
(8.9%), the lesion was referable to the operated side.
Pour strokes (3.6%) and 3 TIA (2.7%) were referable
to the contralateral non-operated side. One patient had
stroke (0.9%) and one TIA (0.9%) related to the verte-
bral-basilar territory. Eighty nine patients remained
asymptomatic.
Total Peri- and Postoperative Period
Using the life table (fig. 1), at 9 years 23.2% of the
patients had experienced new strokes, 11.1% being
referable to operated vessels. The annual stroke rate
was 1.7% on the operated side and 1.0% on the non-
operated side, a total of 2.7% on all sides. If periopera-
tive strokes were excluded, the annual incidence of
stroke was 0.7% on the operated side and unchanged
on the non-operated side.
Morphological Findings
Operated Side
Twenty seven (24%) were found to have either a
high grade stenosis (>50%) or an occlusion diagnosed
by at least one method. In 13 patients (11.5%), a
12 24 36 48 6O 72 96 108
Month* pott operative
FIGURE 1. Probability of survival free of stroke after CE on
operated vessels, non-operated vessels and on all patients using
the life table analysis.
restenosis >50% was detected and in 14 patients
(12.5%) there was an occlusion. The risk of restenosis
was higher in females (p < 0.025, chi square 5.24).
The presence of restenosis/occlusion was significantly
commoner in the vessels with high grade (>50%) pre-
operative stenosis (p < 0.025, chi square 5.47). Twen-
ty two of 70 vessels with preoperative high grade ste-
nosis developed late restenosis/occlusion compared to
5 of 46 vessels with preoperative low-grade (<50%)
stenosis. Investigation by duplex scanning was per-
formed in 113 patients. The results are given in figure
2. The results of the DSA performed on 82 patients are
given in figure 3. DSA showed a smaller number of
restenoses, only 3 stenoses >50% of which one
>75%. The difference between duplex and DSA,
however, was often only 10-20% (table 2). The du-
plex results agreed with DSA in 72 of 82 vessels
(88%).
The Correlation Between Clinical and Morphological
Findings (Fig 2 & 3)
In the group with restenosis >50%, 3 patients had
new neurological symptoms, one of them TIA + mi-
nor stroke and another patient TIA alone, 6 and 3 years
Patients
50-
45
40
35
TIA
30
I Stroke
25
20
15
10-
LQ-
0 1-15 16-49 50-75 76-99 100 % stenosis
FIGURE 2. Result of Duplex scanning showing vessel mor-
phology vs neurological events on 113 patients on the operated
side.

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1140 STROKE VOL 17, No 6, NOVEMBER-DECEMBER 1986

Patients Patients
7O
50
60 45
40
50
35
30 | TIA
4f> T1A
Stroke
Stroke 25
30
20
20 15
10
5

0 1-49 50-75 76-99 100 %stenosls 0 1-15 16-49 50-75 76-99 100 Sstenosis
FIGURE 3. Result of DSA showing vessel morphology vs neu- FIGURE 4. Result of duplex scanning showing vessel mor-
rological events on 82 patients on the operated side. phology vs neurological symptoms on the contralateral non-
operated side.
respectively, after the operation. The third patient with
progress in all stenosis > 1 5 % lumen diameter reduc-
stenosis > 7 5 % had stroke 7 years postoperatively.
tion (table 3). With DSA, 79 non-operated vessels
Fourteen of the examined patients had an occlusion
were examined. Two symptomatic vessels were exam-
of the operated artery. Of these, 4 had late symptoms
ined by aortocervical angiography. DSA classified 9
(3 TIA, one stroke) (fig 2).
vessels as stenosis 50-75%, 5 as stenosis 76-99% and
In 86 patients in whom the vessels operated on were
5 as an occlusion. Agreement DSA-duplex on the non-
patent and without restenosis at the follow-up, late
operated side was 73/79 (92%), which is slightly better
recurrent symptoms had appeared in only 8 patients
than on the operated side. Using both methods, a total
(7%). Late recurrent symptoms were thus commoner
of 41 vessels progressed from a category of lesser
in patients with stenosed or occluded arteries (p <
degree of lumen diameter reduction to a category of
0.05, chi square 3.88) (fig 2).
greater diameter reduction, compared to preoperative
Non-operated Side angiography.
One hundred and ten vessels were examined by du- Risk Factors
plex scanning. The results are presented in figure 4.
We found no correlation between risk factors, the
Compared with angiographic findings before oper-
number of neurological events and postoperative ves-
ation, a clear progression of atherosclerotic disease
sel morphology on the operated side. There was, how-
was noted in 38 patients (34.5%) when estimating ever, a relationship between the number of risk factors
TABLE 2 Disagreement Duplex/DSA in Classification of Stenosis and progression of atherosclerotic disease on the non-
2:50% operated side, where 27 of 41 patients had at least two
Sex Age Duplex PSA or more risk factors, a significant difference (p < 0.05,
a) Operated side M 67 50% 40%
M 63 75% 15% TABLE 3 Atherosclerotic Disease Progression on the Non-oper-
ated Side Assessed1 by Angiography before Operation vs Duplex
M 52 50% 15% Scanning after Operation
M 76 60% 40% Duplex after
M 73 50% 25% Angio Nor- 1- 16- 50- 76-
F 54 50% 40% before mal 15% 49% 75% 99% 100% Total
M 46 60% 25% Normal 6s 10
1-15% 5 24-r 8 5ss 1 43
b) Non-operated side F 74 50% 30% 16-49% 2 14 9 13S 3 40
M 60 16-49% 50% 50-75% 1 4 4T 9
M 63 16-49% 50% 76-99% 1 4 5
M 60 50% 40% 100% 2 2
M 60 15% 50% Total 7 45 22 22 9 5 110
F 69 50% 25% T - TIA; S - Stroke.

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 DUPLEX AND DSA AFTER CAROTID SURGERYIZbornikova et al
chi square 4.29) from the group which did not pro-
gress. In the latter group, 30 of 69 patients had a
combination of two or more risk factors. As a single
risk factor, smoking was related (p < 0.05, chi square
3.8, one-tailed test) to atherosclerotic disease progres-
sion: 31 of 41 patients with progression were smokers
as opposed to 38 of 69 patients in whom the atheroscle-
rotic lesions were stable. Furthermore, 10 of 41 pa-
tients with progression had a history of myocardial
infarction either prior to operation or during the fol-
low-up, compared to only 6 of the 69 patients without
progression (p < 0.05, chi square 3.91). Hyperlipide-
mia was insignificant.
Discussion
The clinical results are in accordance with several
other studies and show a concentration of mortality and
morbidity during the operative period.13 If the strokes
during the operation and the following month are ex-
cluded, new strokes on all sides occurred at a rate of
1.7% per year, which is'about the same rate as has been
reported during long-term follow-up after CE in other
studies.16
Approximately a half of the new strokes appeared in
the territory of the operated carotid artery during the
perioperative period, and at that time no strokes oc-
curred on the side not operated on. Thereafter no dif-
ference in stroke frequency between the operated and
non-operated side was observed. For this reason it is
probable that these late strokes were related to the
natural progression of the atherosclerotic process. On
the operated side, there was a stronger relation be-
tween the grade of restenosis or occlusion and the
appearance of a new stroke. Most previous studies of
the postoperative pathology have been evaluated only
in patients with recurrent symptoms. However, Zierler
1982, using ultrasonic duplex examination, found in
76 patients (89 CE) that 19% of the operated vessels
had a severe restenosis within 16 months.10 Only one
occlusion was found. That result can be compared with
the present rate of 23% restenosis or occlusion during a
long follow-up time after the operation of mean 62
months.
Totally, 14 occlusions (12%) were found in 116
operated and examined vessels. About the same
amount was found by Norrving et al 1981, who per-
formed angiography in the common carotid artery
within 2 weeks after the operation in 81 CE patients
and found 7 early occlusions. With ultrasound tech-
nique, 10 occlusions (16%) were found in the same
investigation at follow-up after 72 months in 64 exam-
ined operated vessels.6 Comparable results are report-
ed by Schutz, 1970, who with angiography found 6
occlusions (12%) in 50 patients.17 Recently, also Pa-
dayachee, 1983, using continuous wave Doppler,
found occlusion of the operated internal carotid artery
in 7 of 54 CE patients (13%), all associated with a
stroke within the first postoperative week.18
In our study, no risk factor could be found to predict
the rate of restenosis or occlusion on the operated side,
except that high-grade restenosis/occlusion were sig-
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1141
nificantly commoner in vessels with high-grade preop-
erative stenosis and that proportionately more females
developed recurrent stenosis. Possible explanations
are that females have smaller arteries3 or differing
platelet function19 than males.
In order to detect early restenosis or occlusion, a
perioperative Doppler investigation may be performed
after closure of the arteriotomy but before skin clo-
sure.20 The finding of a lack of improvement or a
deterioration in the Doppler spectrum may be useful in
selecting patients for operative angiography. An early
detected severe restenosis or occlusion in an operated
patient is an indication for immediate revision.
The results presented in this study do not allow
unequivocal conclusions to be drawn. As shown in
figures 2 and 4, late neurological symptoms were seen
both in low and high grade stenotic vessels, whereas
normal vessels were asymptomatic.
If the results of two methods used in the study (the
duplex ultrasound and the DSA technique) are com-
pared, good agreement is seen in the detection of oc-
clusions on both sides and restenosis in the non-operat-
ed carotid vessels. On the operated side, the duplex
technique more often showed stenosis 50-75% than
did DSA. Two alternative explanations alone or in
combination are possible; duplex tended to slightly
overestimate the degree of stenosis because of post-
operative remodelling of bulb geometry; DSA tended
to underestimate the severity of lesions. This has
been shown in several studies in comparison with
angiography.13'21
To date, there is no way of fortelling which vessels
might develop late symptoms and morphological le-
sions after carotid endarterectomy in patients with
atherosclerotic vessel disease. The duplex ultrasound
technique would seem to be the most appropriate meth-
od for the serial follow-up of the postoperative course
in these "at risk" patients.
Acknowledgments
We thank Mr. Erik Leander, lecturer in statistics, and Mrs. Monica
Rosander, Department of Mathematics, University of Linkoping for
help with statistical evaluation.
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Arch Surg 119: 664-669, 1984

Familial Hyperlipidemia in Stroke in the Young

B.C. BANSAL, M.D., M.A.M.S., F.I.A.M.S.,* A.K. SOOD, M.D., t C.B. BANSAL, M.D.t

SUMMARY Serum cholesterol, low density lipoproteins (LDL), very low density lipoproteins (VLDL)
and chylomicron levels were studied in 25 young patients (age 40 years or less) of non-embolic ischemic
stroke of unknown aetiology. Fifteen patients were males and 10 were females. The prevalence of hyperlip-
idemia was found to be 60%. Fredrickson's type lib hyperlipoproteinemia was the commonest (32%)
abnormal pattern observed, followed by type Ila (12%), type IV (12%) and type V (4%). Family studies
were carried out in all the 25 index patients (15 hyperlipidemic and 10 normolipidemic). Familial hyperlip-
idemia (i.e. 2 or more hyperlipidemic members in the same family) was found in 9 of the 15 hyperlipidemic
index patients and in none of the normolipidemic index patients. The common pattern was found to be that
of familial combined hyperlipidemia. The study indicates that screening the family members of hyperlipid-
emic young patients of non-embolic ischemic stroke may delineate a group of high risk individuals for
possible primary prevention before they develop the disease.
Stroke Vol 17, No 6, 1986

SINCE CEREBRAL STROKE is often crippling, and
the impact of treatment on the prognosis is limited, the
potential to control the disease lies in its primary pre-
vention.'"3 This implies reliable and comprehensive
information on the factors related to the risk of stroke.
Hyperlipidemia has been considered as one of the im-
portant risk factors in the causation of atherothrombot-
ic stroke.4"9 The task of identifying the individuals with
high lipid levels in the general population sounds cum-
bersome. A desirable and feasible alternative ap-
proach, however, could be to screen the first degree
From the Medical College and Hospital, Rohtak — 124001 Haryana,
India.
Dr. Bhupendra Chandra Bansal, M.D., M.A.M.S., F.I.A M.S.,
Professor of Medicine and Head Department of Neurology.*
Dr. Arun Kumar Sood, M.D., Reader, Medicine.t
Dr. Chander Bhan Bansal, M.D., Registrar in Medicine.t
Address correspondence to: Dr. B.C. Bansal, 15/8 FM, Medical
Enclave, Medical College, Rohtak, Haryana, India.
Received February 19, 1986; revision # 1 accepted July 7, 1986.
relatives of hyperlipidemic young patients of athero-
thrombotic stroke for familial hyperlipidemia, thus de-
lineating a group of high risk individuals for possible
primary prevention before they develop the stroke.
Since the relative contribution of genetic factors in the
causation of any trait may vary among different popu-
lations, a pilot study has been carried out to identify the
importance of familial hyperlipidemia in patients of
ischemic stroke in Haryana (North India).
Material and Methods
Selection of the Index Patients
This study was conducted in the Department of Neu-
rology at Medical College and Hospital, Rohtak (Har-
yana). Twenty-five patients (15 males and 10 fe-
males), of the age of 40 years or less, suffering from
cerebral infarction (nonembolic ischemic stroke) of
unknown aetiology (based on the criteria of Walker et
al, 198110) were taken for the study as index patients.
Diagnosis was made on the basis of history, physical

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