
Influence
of the greater saphenous vein graft quality in the early patency of
infrainguinal revascularizations
(
PDF version)
Jorge
R. R. Timi1, Julio C. U. Coelho2,
Luiz F. Bleggi-Torres3, Fabiola Medeiros4
1
Vascular surgeon, Division of Vascular Surgery, Hospital de Clínicas,
Universidade Federal do Paraná (HC-UFPR) and Hospital Nossa Senhora
das Graças - Curitiba - Brazil.
2 Chairman, Division of Gastrointestinal Surgery, HC-UFPR.
3 Chairman, Division of Pathology, HC-UFPR.
4 Student Research Fellow, Division of Pathology, HC-UFPR.
Correspondence:
Jorge R. R. Timi
Rua Padre Agostinho, 1923/2601
CEP 80710-000 - Curitiba - PR
Tel.: + 55 41 244.8787
E-mail: jorgetimi@terra.com.br
ABSTRACT
Objectives:
The authors evaluate the quality of the greater saphenous veins
used in lower limb revascularizations at the moment of their implantation,
using a semiquantitative histopathological method, relating the
vein quality with patient's sex and age, as well as the influence
on early patency rates.
Method: A total of 144 veins of 144 patients were studied,
88 male and 56 female, with a mean age of 65.7 years. The vein was
stained with hematoxylin-eosin. The degree of intimal hyperplasia
and hypertrophy of the longitudinal and circular muscular layers
of the media were analyzed. The quality of the vein was classified,
by adding the grades of each layer, into good, regular and questionable
quality.
Results: As to quality, 82 veins (57%) were classified as
good, 49 (34%) as regular and 13 (9%) as questionable. In six months,
the primary patency of good quality veins was 80.5%, that of regular
quality veins was 79.6% and the patency of questionable quality
veins was 84.6%.
Conclusion: No differences were seen in vein quality, either
in the individual evaluation of each layer or in the global evaluation
of the three layers, regarding the patient's sex and age. No difference
was observed regarding the patency of the grafts.
Key-words:
saphenous vein, lower extremity, grafts.
Palavras-chave: veia safena, membros inferiores, enxertos.
J
Vasc Br 2003;2(2):91-8
Over the
past fifty years, the greater saphenous veins have been used as arterial
graft. It is an easily obtained and inexpensive graft. The diameter,
length and wall of greater saphenous veins are satisfactory, and also
resistant to infections. However, in some circumstances, the surgeon
cannot find adequate grafting conditions due to diameter alterations,
total or segmental occlusion or varicose dilatation. The decision on
which vein to use as a graft is a personal choice, and this is done
by visually evaluating the vein, during the procedure, and determining
its quality and possibility of use, without any scientific criteria.
At other times, depending on the recipient arteries, the greater saphenous
vein is the only available graft option, despite its quality. An inadequate
greater saphenous vein is considered a significant contributing factor
for early graft failure, possibly associated with limb loss. The histopathological
analysis of the greater saphenous veins used as arterial grafts aims
at providing a reliable criterion to the surgeon about the quality of
the graft, mainly regarding the follow-up and prognosis of revascularization.
The aims of this study are to1) analyze the quality of the greater saphenous
veins used as arterial grafts by a semiquantitative histopathological
method; 2) evaluate the influence of the greater saphenous vein quality
in the early patency of arterial grafts; 3) compare the patient's sex
and age with the quality of the greater saphenous veins.
METHOD
A total
of 144 greater saphenous veins used as arterial grafts in the lower
limb revascularizations of 144 patients were analyzed. There were 88
males (61.1%) and 56 females (38.1%), with a mean age of 65.7 years.
The mean age for males was 65.4 years, lower than the mean age for females
of 67.1 years.
The inclusion criteria were the following:
- The patients were submitted to infrainguinal lower limb revascularization.
- All patients agreed to the study design.
- The surgical indications were atherosclerosis, popliteal artery aneurysm,
or femoropopliteal prosthesis infection.
- The revascularization was performed with venous grafts.
- The venous graft was the greater saphenous vein.
- At least one centimeter of the distal portion of the greater saphenous
vein was submitted to histopathological evaluation.
- The patients were followed for at least six months postoperatively.
At the end of a lower limb revascularization with the use of a greater
saphenous vein graft, a circular segment of at least one centimeter
in length, taken from the distal portion of the graft, was sent to histopathological
study. The vein was stained with hematoxylin-eosin. The evaluation was
based on the venous layers, according to the criteria proposed by Milroy
et al.1 The degree of intimal hyperplasia
and hypertrophy of the longitudinal and circular muscular layers of
the media was analyzed. Each of the three layers was classified into
three degrees, according to its alterations: I - minimal, II - moderate,
III - severe. The inclusion criteria for each layer are given in Table
1. A grade was given to each degree: Grade I - one point; Grade II -
two points; Grade III - three points. The score of each greater saphenous
vein varied from three to nine. The quality of the vein was classified
by adding the grades of each layer: good quality - up to three points,
regular quality - four or five points, questionable quality - six points
or higher.
Table
1 - Histopathological
grading and scoring of the greater saphenous vein layers
 |
|
Grade |
Evaluation |
% |
Score |
 |
|
I |
Mild |
1-24
|
1 |
|
II |
Moderate |
25-50 |
2 |
|
III |
Severe |
51-100 |
3 |
 |
The patients
were distributed into three groups according to their age: 46 to 59
years, 60 to 69 years and 70 to 88 years, as shown in Table 2.
Table
2 - Patient
distribution according to sex and age
|
|
|
Age (years) |
Male |
Female |
Total |
% |
 |
|
46-59 |
29 |
13 |
42 |
29.2 |
|
60-69 |
33 |
13 |
46 |
31.9 |
|
70-88 |
26 |
30 |
56 |
38.5 |
 |
The grades
were compared with the patient's sex and age, as well as with the early
patency of the grafts, which was defined as six months postoperatively.
The statistical analysis was performed by the chi-squared test. The
analysis of variance was used for comparison of the means. The alpha
error was established at 5% to reject the null hypothesis.
RESULTS
The length of the distal portion of the greater saphenous vein sent to
histopathological study varied from 1 to 6 cm (mean of 2.4 cm). The veins
had a mean diameter of 3.81 mm varying from 2 to 7 mm.
Most of the greater saphenous veins evaluated (57%) were classified as
good quality (up to three points), 34% as regular quality (four or five
points) and 9% as questionable quality (six points or higher). This distribution
is shown in Table 3.
Table
3 - Quality
of greater saphenous vein in 144 analyses
 |
|
Quality |
n. of veins |
% |
 |
|
Good |
82 |
57 |
|
Regular |
49 |
34 |
|
Questionable |
13 |
9 |
 |
Examples
of the histopathology of the greater saphenous veins are shown in Figures
1 to 3.
Figure
1 - Greater saphenous vein with intimal and circular muscular layers
degree I and longitudinal muscular layer degree II (hematoxylin-eosin
x 40).

Figure
2 - Greater saphenous vein with intimal and longitudinal muscular layers
degree III and circular muscular layer degree II (hematoxylin-eosin
x 40).

Figure
3 - Greater saphenous vein with intimal layer degree III (hematoxylin-eosin
x 40).

There
were no differences among the three groups as far as the quality of
the greater saphenous veins and associated diseases, surgical indication,
drainage, surgical method, and donor and recipient arteries were concerned.
The most frequently associated disease was systemic arterial hypertension,
followed by diabetes mellitus and heart diseases (Table 4).
Table
4 - Associated
diseases*
 |
|
Disease
|
n. of patients |
|
|
|
Hypertension
|
92 |
|
Diabetes mellitus
|
70 |
|
Heart disease
|
54 |
|
Cerebrovascular disease
|
27 |
|
Chronic obstructive pulmonary disease
|
14 |
|
Peptic ulcer
|
10
|
|
Chronic renal failure
|
4 |
|
Abdominal aortic aneurysm
|
4 |
|
Diverticulitis
|
1 |
|
Paget’s disease
|
1 |
|
Multiple sclerosis
|
1 |
|
Parkinson’s disease
|
1 |
 |
*70
patients had more than one associated disease
The indication
for surgical treatment according to the clinical categories of SVS/ISCVS2
is given in Table 5. Most of the patients were operated on due to limb
loss risk (categories 4 and 5). In only three patients the surgical
indication resulted from disabling intermittent claudication.
Table
5 -
Indication of surgical treatment according to the clinical categories
of SVS/ISCVS
 |
|
Indication |
Categories |
n |
% |
 |
|
Tissue loss |
5 |
110 |
76.4 |
|
Rest pain |
4 |
25 |
17.3 |
|
Popliteal artery aneurysm |
- |
5 |
3.5 |
|
Intermittent claudication |
3 |
3 |
2.1 |
|
Prosthesis infection |
- |
1 |
0.7 |
 |
A variety
of surgical methods were performed depending on the combinations between
the graft and donor and recipient arteries (Table 6). The femoral artery
was the donor artery in 135 cases, corresponding to 58 common femoral,
35 superficial femoral and 42 deep femoral. The popliteal artery was
the donor at the remaining grafts with four proximal anastomoses above
and five below the knee. The popliteal artery was the graft recipient
site in 80 cases, with 21 anastomoses above and 49 below the knee. The
other recipient arteries in order of frequency were: 27 peroneal, 15
anterior tibial, 14 posterior tibial, seven tibioperoneal trunk and
one superficial femoral. In the 80 cases in which the popliteal artery
was the recipient, three were in isolated segment. In two distal bypasses
an arteriovenous fistula was associated.
Table
6 - Surgeries
performed in 144 patients
 |
|
Bypass |
n. of patients |
 |
|
Femoropopliteal |
79 |
|
Femoroperoneal |
24 |
|
Femoro-posterior tibial |
13 |
|
Femoro-anterior tibial |
12 |
|
Femoro-tibioperoneal trunk |
6 |
| Popliteal-peroneal
|
3 |
|
Popliteal-anterior tibial |
3 |
|
Femoro-superficial femoral |
1 |
|
Popliteal-tibioperoneal trunk |
1 |
| Popliteal-posterior
tibial |
1 |
| Popliteal-popliteal
|
1 |
 |
Table
7 shows the runoff in each case, that is, the number of patent arteries
in each limb to be revascularized. Three limbs did not have any patent
artery in the leg being revascularized in an isolated segment of the
popliteal artery.
Table
7 - Number
of patent distal arteries in 144 limbs
 |
|
Patent arteries |
Limbs |
% |
 |
|
0 |
3 |
2.1 |
|
1 |
55 |
38.1 |
|
2 |
43 |
29.9 |
|
3 |
43 |
29.9 |
 |
Table
8 exhibits the percentages of patent distal artery. The peroneal artery
presented the highest patency rate: 78.5%, representing 113 patent arteries
in 144 limbs analyzed, statistically significant compared to the posterior
and anterior tibial patency.
Table
8 - Patency
of leg arteries in 144 limbs
 |
|
Artery |
Patent |
% |
 |
|
Peroneal |
113 |
78.5 |
|
Posterior tibial |
80 |
55.6 |
|
Anterior tibial |
77 |
53.5 |
 |
P < 0.01
Table 9
shows the method of greater saphenous vein utilization in each lower
limb revascularization. There was equal utilization of reversed and
in situ methods despite the author's preference for the in
situ utilization.
Table
9 - Utilization
of the greater saphenous vein in 144 infrainguinal revascularizations
 |
|
Method |
Grafts |
% |
 |
| In
situ |
68 |
47.2 |
| Reversed
|
68 |
47.2 |
| Ex
situ |
6 |
4.2 |
| Combined
|
2 |
1.4 |
 |
Table
10 exhibits the frequency of smoking according to sex, showing a predominance
in males.
Table
10 - Frequency
of smoking according to patient's sex
 |
|
Sex |
Patients |
Smoking |
% |
 |
|
Male |
88 |
83 |
94.3 |
|
Female |
56 |
32 |
57.1 |
|
Total |
144 |
115 |
79.9 |
 |
P
< 0.01
The relation
between vein quality and sex is shown in Table 11, with no statistically
significant difference being observed.
Table
11 - Quality
of greater saphenous vein according to patient's sex
|
|
|
|
Good |
Regular
|
Questionable
|
 |
|
|
Veins |
% |
Veins |
% |
Veins |
% |
| Male
|
48 |
54.6 |
32 |
36.4 |
8 |
9.0 |
| Female
|
34 |
60.7 |
17 |
30.4 |
5 |
8.9 |
 |
P
> 0.05
No statistically
significant difference was seen regarding vein quality and patient's
age, which shows that the deterioration of the histological quality
of the veins is not related to the advance of age (Table 12).
Table
12 - Quality
of greater saphenous vein according to patient's age (years).
|
|
|
|
Good |
Regular
|
Questionable |
|
|
|
|
Veins |
% |
Veins |
% |
Veins |
% |
|
46-59 |
27 |
64.3 |
11 |
26.2 |
4 |
9.6 |
|
60-69 |
25 |
54.3 |
20 |
43.5 |
1 |
2.2
|
|
70-88 |
30 |
53.7 |
18 |
32.1 |
8 |
14.2 |
|
Total |
82 |
57.0 |
49 |
34.0 |
13 |
9.0 |
|
|
P
> 0.05
Table
13 analyzes the primary patency of arterial grafts according to vein
quality. In this study, we did not find any difference between the early
patency of the graft and the histopathological quality of the greater
saphenous vein, considering that the veins of questionable quality have
had similar early patency rates compared with the veins of good and
regular quality.
Table
13- Relation
between early patency of the graft and quality of the greater saphenous
vein
 |
|
|
Patent |
Occluded
|
|
|
Grafts |
% |
Grafts |
% |
 |
|
Good |
66 |
80.5 |
16 |
19.5 |
|
Regular |
39 |
79.6 |
10 |
20.4 |
|
Questionable |
11 |
84.6 |
2 |
15.4 |
 |
P
> 0.05
DISCUSSION
The indications
for lower limb revascularization can be divided into two groups: absolute
and relative. There is a consensus in the literature about absolute
indications; they are performed in cases of limb salvage, corresponding
to tissue loss and rest pain. Concerning relative indications, divergent
opinions and procedures are seen in literature, this group comprises
patients with intermittent claudication and progressive claudication.
In the former one, the patient has limitations only in his home environment
and, in the latter, the patient presents with gradual reduction of walking
distance despite clinical intervention. Both are accepted as surgical
indication in the vascular surgery literature, in contrast to intermittent
claudication, which limits professional activity or brings about change
in lifestyle, and has some restrictions on surgical indications.2
In this study, the surgical indication for intermittent claudication
was limited to those patients with gradual deterioration of walking
distance despite clinical treatment, corresponding to 2.1%. Surgical
indication was not restricted by the literature in 97.9% of the cases:
tissue loss, rest pain, popliteal artery aneurysm and prosthesis infection.
The associated diseases were evenly distributed as far as the patient's
sex and age were concerned, especially in diabetics who have a higher
risk for graft failure due to the increase of peripheral vascular resistance.3
However, the revascularization outcome in diabetic patients can be the
same as in non-diabetic patients, even in grade 5 of SVS/ISCVS classification
and in distal grafts.4 The outcome of paramalleolar
grafts can be even higher in diabetics,5
considering that the peripheral vascular resistance is not an isolated
factor in the outcome of distal revascularizations.6
The frequency of smoking presented itself as the only difference between
groups, and was higher among males. Smoking is an important risk factor
for obliterative atherosclerosis,7 and is
also related to the increased development of intimal hyperplasia after
vascular injury.8 Smoking cessation improves
arterial insufficiency in claudicant patients, increasing the walking
distance and decreasing the progression of atherosclerotic disease after
lower limb revascularization.9
Besides the quality of distal arteries, another important factor concerns
the graft material and its availability relative to autogenous graft.
In this study, the number and types of patent arteries were equally
distributed among all groups. The peroneal artery was the least involved
by atherosclerotic disease.
Autogenous grafts are known as the best material for lower limb revascularizations.
They have been used for 50 years,10 most
of which correspond to greater saphenous vein used in situ, reversed
or ex situ.
With regard to the quality of the greater saphenous vein, the veins
with long or segmental occlusions are initially discarded. Those partially
occluded veins are used in composite grafts. The vein diameter is also
considered an exclusion criterion. Before the popularization among vascular
surgeons of the in situ utilization of the greater saphenous vein,11
veins with a diameter lower than 4 mm were discarded. However, with
the in situ utilization, veins with a diameter of 2 mm or more can be
used. In this study, the average diameter of the distal portion of the
vein was 3.81 mm, varying from 2 to 7 mm. Dilatations are also an exclusion
criterion for the use of greater saphenous vein, especially when they
involve multiple segments. An isolated dilatation can be removed and
the remaining segments can be anastomosed and used on the revascularization.
Dilated veins can also be covered in bovine pericardium, which works
as an external support.12
The greater saphenous vein can be classified according to a semiquantitative
histopathological method.1 The degree of
intimal hyperplasia and hypertrophy of the longitudinal and circular
muscular layers of the media are classified into: I - minimal, II -
moderate, III - severe. A grade is given to each degree: Grade I - one
point, Grade II - two points, Grade III - three points. By adding the
grades given to each layer, the vein quality is classified into: good
- up to three points, regular - four or five points, questionable -
six points or higher. Most of the greater saphenous veins evaluated
(57%) were classified as good quality, 34% as regular quality and 9%
as questionable quality.
Concerning the relation between vein quality and patient's sex, no significant
difference was observed probably because the clear presence of varicose
veins, which are more frequently found in women. These veins have not
been used (in case of focal dilatation, the greater saphenous vein has
been covered with bovine pericardium), showing that women who develop
arterial disease with no varicose saphenous vein due to multiple pregnancies
or hormonal alterations,13 have greater
saphenous vein of similar quality to men's.
It is classically admitted that the quality of the greater saphenous
vein decreases with age, however, in this study no significant difference
was observed among age groups, from 46 to 88 years, which suggests further
similar evaluations in younger groups in order to determine the period
of life in which this decrease occurs.
In this study, the authors did not find difference between the early
patency of the graft and the histopathological quality of the greater
saphenous vein. The veins of questionable quality have shown similar
early patency rates compared with the veins of good and regular quality,
showing that the quality of the greater saphenous vein is not an isolated
factor in early patency rates of arterial grafts. These results have
led the authors to continue the follow-up of the patients submitted
to lower limb revascularizations with veins of questionable quality
in a specific protocol.
Early graft failure results from an association of multiple factors
including surgical indication; (in this study 67% of the patients have
already had trophic lesions, and the failure rate is higher in limb
salvage patients); the quality of proximal and distal bed; and the patient's
clinical status, mainly in the immediate postoperative period.
All revascularizations were performed in this series with different
combinations between donor and recipient arteries. In three cases, revascularization
was done in an isolated segment of the popliteal artery and, in two
cases, an arteriovenous fistula with common "ostia" was associated.
An equal number of in situ and reversed greater saphenous vein
revascularizations were performed, despite the author's preference for
the in situ technique. However, when the reversed vein was used,
the results were similar. With the introduction of angioscopic valvulotomy,
the in situ technique will be performed in a larger number of
patients. In a few cases, nonreversed greater saphenous vein was used
ex situ due to the diameter discrepancy of the recipient artery.
In this study, only two cases required the use of contralateral greater
saphenous vein segment as a complementary conduit. Composite grafts
with another vein, except the greater saphenous vein, were excluded.
The conclusions of this study were that most of the greater saphenous
veins used as arterial grafts have acceptable quality (good or regular);
there is no relation between the greater saphenous vein quality and
patient's sex; the quality of the greater saphenous vein does not change
with age; the histopathological quality of the greater saphenous vein
is not an isolated factor for the early patency of arterial grafts.
REFERENCES
1.
Milroy CM, Scott DJ, Beard JD, Horrocks M, Brafield JWB. Histological
appearances of the long saphenous vein. J Pathol 1989;159:331-6.
2.
Rutherford RB, Flanigan DP, Gupka SK, et al. Suggested standards for
reports dealing with lower extremity ischemia. J Vasc Surg 1986;4:80-94.
3.
Moore WS, Malone JM. Vascular reconstruction in the diabetic patient.
Angiology 1978;29:741-8.
4.
Rosenblatt MS, Quist WC, Sidawy AN, et al. Results of vein graft reconstruction
of the lower extremity in diabetic and nondiabetic patients. Surg Gynaecol
Obstet 1990;171:331-5.
5.
Plecha EJ, Lee C, Hye RJ. Factors influencing the outcome of paramalleolar
bypass grafts. Ann Vasc Surg 1996;10:356-60.
6.
Wahlberg E, Jorneskog G. Patients with diabetes and critical limb ischemia
have a high peripheral vascular resistance. Ann Vasc Surg 1997;11:224-9.
7.
Fowkes FG. Epidemiology of atherosclerotic arterial disease in the lower
limbs. Eur J Vasc Surg 1988;2:283-91.
8.
Law MM, Gelabert HA, Moore WS, et al. Cigarette smoking increases the
development of initial hyperplasia after vascular injury. J Vasc Surg
1996;23:401-9.
9.
Smith I, Franks PS, Greenhalgh RM, et al. The influence of smoking cessation
and hypertriglyceridaemia on the progression of peripheral arterial
disease and the onset of critical ischaemia. Eur J Vasc Endovasc Surg
1996;11:402-8.
10.
Kunlin J. Le traitement de l'artérite oblitérative par
la greffe veineuse. Arch Mal Coeur 1949;42:371-3.
11.
Leather RP, Powers SR, Karmody AM. A reappraisal of the in situ saphenous
vein arterial bypass: its use in limb salvage. Surgery 1979;86:453-61.
12.
Timi JRR. Restauração femoro-poplítea. Anais do
30º Congresso Brasileiro de Angiologia e Cirurgia Vascular; 1993.
p. 99-100.
13.
Sadick NS. Predisposing factors of varicose and telangiectatic leg veins.
J Dermatol Surg Oncol 1992;18:883-6.
|