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The role of omental transfer in Buerger's disease: New


Delhi's experience.
Aust N Z J Surg. 1996; 66(6):372-6 (ISSN: 0004-8682)

Singh I ; Ramteke VK
Department of Surgery, Maulana Azad Medical College, New Delhi, India.
BACKGROUND: Buerger's disease is a specific, idiopathic, recurrent, segmental, inflammatory,
obliterative vascular disease involving medium-sized arteries and veins of the limbs. We
performed omental transfer on a group of patients with Buerger's disease that had previously
undergone lumbar sympathectomy and the results are described. METHODS: Between January
1988 and December 1993, 100 cases of peripheral vascular disease (PVD) diagnosed as
Buerger's Disease were subjected to femoral angiography. Fifty cases of angiographic
intermediate/distal type blocks underwent omental transposition. RESULTS: Of 50 patients
subjected to omental transfer all had intermittent claudication, 40 had rest pain of whom 36 had
non-healing ulcers, 8 had gangrene and 32 had bilateral lower limb involvement. Fifteen patients
underwent bilateral omental transfer and posterior tibial artery biopsy was performed in 40. All
patients showed improved skin temperature, rest pain decreased in 36 and claudication distance
increased in 48. Ulcers healed in 32 of 36 patients and the line of demarcation receded in six of
eight patients with gangrene. CONCLUSIONS: Omental transfer improved skin and muscle
microcirculation and forestalled the need for amputation by providing symptomatic relief and
clinically arresting the progress of Buerger's disease. Omental transfer should be considered
seriously as an alternative to other modalities of therapy to delay the ischaemic complications of
Buerger's disease.

PreMedline Identifier: 8678856

REVIEW ARTICLE
Year : 2001 | Volume : 47 | Issue : 2 | Page : 137-42
Omentopexy for limb salvage in Buerger's disease: indications, technique and results.
Talwar S, Choudhary SK
Department of Cardiothoracic and Vascular Surgery, All India Institute of Medical
Sciences, New Delhi, India. , India
Correspondence Address:
Talwar S
Department of Cardiothoracic and Vascular Surgery, All India Institute of Medical
Sciences, New Delhi, India.
India
Source of Support: None, Conflict of Interest: None
:: Abstract
Buerger's disease is a limb-threatening condition occurring in the young and productive
age group and its management has always been a challenging problem. A large number of
medical and surgical options have been suggested, but the quest for an ideal solution to
this problem continues. Omentopexy for Buerger's disease is an attractive option, which
is rapidly gaining popularity. We discuss the historical aspects, technical considerations
and results of omental transfer for this limb-threatening condition. In doing so, the
relevant literature on the subject has been extensively reviewed. In all published series,
there has been marked improvement in intermittent claudication and rest pain. Ischaemic
ulcers have healed and the progression of gangrene has stopped. If carried out with the
complete understanding of the anatomy of the omental vascular arcade, the results of
omentopexy are gratifying, thus avoiding amputation and conserving the limb.

Keywords: Arm, blood supply,Human, Intermittent Claudication, surgery,Ischemia,


surgery,Leg, blood supply,Omentum, blood supply,surgery,Thromboangiitis Obliterans,
surgery,Vascular Surgical Procedures, methods,
How to cite this article:
Talwar S, Choudhary SK. Omentopexy for limb salvage in Buerger's disease: indications,
technique and results. J Postgrad Med 2001;47:137
How to cite this URL:

Talwar S, Choudhary SK. Omentopexy for limb salvage in Buerger's disease: indications,
technique and results. J Postgrad Med [serial online] 2001 [cited 2008 May 6];47:137.
Available from: http://www.jpgmonline.com/text.asp?2001/47/2/137/209
Buergers disease (Thromboangitis Obliterans) is a condition characterised by segmental
occlusion of small and medium sized arteries of the lower and sometimes of upper
extremities in young male smokers, often associated with migratory thrombophlebitis.[1],
[2] Its treatment has remained an enigma and multiple strategies have been employed.
Drug therapy is of little benefit.[2],[3],[4] Surgical treatment options have consisted of
sympathectomy,[5] direct arterial surgery,[6] adrenalectomy,[7] and amputation as a last
resort.[3] With the exception of cessation of smoking, none of these measures is curative
and conflicting results have been obtained.[2],[3],[4],[7],[8]
However, in patients with critical limb ischaemia, surgery is required to salvage the limb.
Traditionally, patients who have ischaemic signs and symptoms have been offered
sympathectomy[5] despite the fact that relapses are frequent due to normalisation of
vasomotor tone within two weeks to six months after operation.[7],[9] Results of
adrenalectomy also continue to be disappointing.[10]
Arterial reconstruction is usually impossible due to distal nature of the disease and carries
a high failure rate.[12] These considerations have always prompted surgeons to look for
an alternative solution in the form of omental transfer. In this review, we discuss the
historical aspects, technical considerations and results of omental transfer for this limbthreatening condition.
:: Historical aspects
The vascularising properties of omentum have been known since a long time and have
included use for absorption of ascites,[12] Myocardial, cerebral and spinal cord
revascularisation,[13],[14],[15] and protection of oesophagogastric anastomosis.[16]
Based on these, pedicled omental transfer was first used by Goldsmith and his colleagues
for surgical relief of chronic lymphoedema of lower limbs in 1967.[17] Casten and Alday
first used this for 24 cases of atherosclerosis[18] and reported excellent clinical results in
terms of relief of symptoms and complete healing of ulceration and gangrenous areas of
toes and feet.
:: Surgical anatomy
An understanding of the vascular anatomy of the omental vascular arcade [Figure - 1] is
crucial to the concept of omental lengthening. The right and the left gastroepiploic
arteries and their branches along the greater curative of the stomach form the omental

vascular arcade. The branches consist of the right and left omental artery the middle
omental artery the accessory omental artery and shot omental arteries. The middle
omental artery, which is the major branch further, divides into right and left branch which
join the right and left omental arteries. The presence of this omental arcade allows the
omentum to be lengthened as far as down the ankle by division of the side branches
basing the pedicle on the right or the left gastroepiploic artery.
Alday and Goldsmith[19] performed autopsy studies on 136 adult cadavers and described
five types of omental vascular arcades depending upon the level of bifurcation or the
absence of the middle omental artery [Figure - 2]. Type 1 is most common and involves
bifurcation of the middle omental artery near the lower end of the omentum. In type 2 the
middle omental artery bifurcates midway between the gastroepiploic arcade and the
lower end of the omentum. In type 3, it bifurcates 2-3 centimetres from the gastroepiploic
arcade. In type 4 the middle omental artery is absent and the right and left omental
arteries form the omental vascular arcade. In type 5, the terminal branch of the splenic
artery develops into the left omental artery and the right gastroepiploic artery gives rise to
the middle omental artery. The knowledge of these types of variations is important as the
line of division of the vessels depends on this.
:: Procedure for omental lengthening
This was just described by Goldsmith and de Los Santos[17] for relief of chronic
lymphoedema of the extremities in 1967 and later by us and others.[18],[19],[20],[21],
[22],[23],[24],[25],[26],[27],[28],[29],[30] Usually a midline incision is used; however in
recent times it has been combined with single stage sympathectomy in which case a
transverse incision is preferred.[32] The omentum is freed from the transverse colon
along the vascular plane and then from the greater curvature of the stomach taking care to
preserve the gastroepiploic arcades and the blood vessel between the arcades. In doing so
the pedicle is based on either the right or the left gastroepiploic artery based on the
dominance.
This pedicled graft is then lengthened depending upon the vascular anatomy and the
branches along the greater curvature of the stomach are tied with silk sutures. As shown
in [Figure - 3], a subfascial tunnel is then prepared on the anteromedial aspect of the
thigh and leg up to the ankle of the affected limbs after making multiple skin incision.
The lengthened omentum is passed down through this tunnel from the abdomen and
pelvis up to the ankle where it is anchored to the underlying muscle using interrupted silk
sutures. The average operating time for the procedure is usually 140-180 minutes.
:: Indications
The traditional indications for omentopexy on patients are[20] failure of lumbar
sympathectomy to heal the ulceration or poor demarcation despite lumbar

sympathectomy, ulceration not responding to conservative treatment and incapacitating


rest pain and claudication after lumbar sympathectomy. However, with the realisation of
the short-term benefits of lumbar sympathectomy, single stage lumbar sympathectomy
and omentopexy has also been proposed to be equally successful with the advantages of a
single stage operation and low cost.[31]
:: Mechanism of action
When the procedure was introduced for patients with atherosclerosis, it was thought that
omental transposition works by supplying extra blood to the ischaemic limb. However,
this is difficult to believe, as the diameter of omental vessels is roughly one-tenth of the
popliteal artery.[32] Later studies have demonstrated that the possible mechanism of
action of omental transfer is an increase in local collateral circulation rather than any
significant increase in blood flow.[20],[23],[25] It has also been demonstrated that the
omentum contains a lipid fraction which promotes neovascularisation.[33],[34] Thus a
local action on limb musculature with increased local collateral circulation may be a
possible mode of action.
:: Results technical success during surgery
[Table - 1], [Table - 2]

The operation is easy if performed with the complete understanding of the anatomy of the
omental vascular arcade. It is usually possible to lengthen the omentum up to the ankle in
nearly all patients. In only three out of 62 cases of pedicled omental transfer performed
by us[30] this was not possible and we could bring the omentum down only up to the
mid-thigh level. Satisfactory results have been obtained even if the omentum has been
brought down up to the mid-thigh level.[27],[29] The technical success of the procedure
is reflected by the immediate and late post-operative results (detailed below).
:: Clinical improvement during immediate post-operative period
The immediate post-operative results are an indication of the efficacy of omentopexy.
These consist of postoperative relief of rest-pain, increase in claudication distance, failure
of progression of gangrene and healing of ulcers. Relief of symptoms has been almost
immediate in most series.[20],[21],[22],[23],[24],[25],[26],[27],[28],[29],[30] Patients
have reported relief of pain in the ischaemic limb even while they had pain at the
abdominal incision site.[30] This has been partly explained by psychological factors and
cessation of smoking following surgery; however increase in tissue oxygen saturation
points to increased blood flow as the possible mechanism of action.[30] Another
important feature of clinical improvement in the post-operative period is an increase in

the claudication distance, improvement in skin temperature, and improvement in tissue


oxygen saturation as measured by pulse oximetry.[27],[28],[30]
:: Long-term follow-up
At a mean follow-up ranging from 1-5 years in most series,[21],[22],[23],[24],[25],[26],
[27],[28],[29],[30],[31],[32],[33],[34],[35],[36],[37] the improvement has been sustained
with progressive improvement in claudication distance, healing of ulcers and avoidance
of major amputations as evident from [Table - 1]. Thus, it has been possible to save the
limb in many patients who would otherwise have required below knee or even mid-thigh
amputation for relief of pain or gangrene.
:: Objective assessment of results of omentopexy
Objective assessment of the results of omentopexy has been carried out using
angiography,[23],[25],[28] measurement of tissue oxygen saturation,[27],[28],[30] digital
plethysmography and tread- mill exercise testing.[27]
The measurement of tissue oxygen saturation has been particularly useful as this has
improved within hours of surgery and has shown sustained improvement on early and
late follow-up [Table - 2]. Nishimura et al[35] have shown an increase in muscle blood
flow during exercise and reactive hyperaemia by using Xenon (X 133) clearance studies.
Agarwal et al[23] performed postoperative angiography in 50 patients who underwent
omental grafting and observed increased number of collaterals at graft site with filling of
vessels distal to the block in the limbs. In an extension of the same study,[36] 20 dogs
underwent allograft omental transfer in hind limbs after ligation of the femoral artery in
10 of these. At the end of three weeks, exploration of the graft site revealed increased
number of collaterals at the graft site with filling of vessels distal to the site of the block.
The authors concluded that even a blood group and human leukocyte antigen mismatched
omental graft is taken up and revascularises the ischaemic limb.
Bhargava et al[27] performed treadmill exercise testing of the patients before and after
omentopexy. In the preoperative period, the claudication free period on treadmill was 2-3
minutes, which increased to 6-9 minutes following omentopexy (p<0.05). Also mean
tolerated workload increased significantly. Subodh et al[25] performed post-operative
Doppler studies and selective coeliac- axis angiography to study the circulation in the
omental graft. In 18 of their 20 cases, the arterial pulsations were heard till the knee on
Doppler study. In 2 cases in which they were not heard, there was no improvement in
symptoms. However on coeliac-axis angiography, the omental vessels were visualised till
mid-thigh in only six and up to the knee in only four patients. The authors concluded that
omental transposition probably works by promoting local collateralisation. Similar
conclusions were drawn in another study comparing free versus pedicled omental grafts.

[20] Khazanchi et al[37] have also reported improved vascularity in the limb on serial
Doppler studies after omentopexy.
:: Complications and technical failures
In general, the operation is very safe. Even when the omental graft has autolysed, major
complications are unusual. The most frequently encountered complications include
prolonged ileus and minor wound infection at the incision sites. Incisional hernia has
been reported to occur from the abdominal incision site.[26],[27],[30]
Failures have been shown to result in patients in whom the mobilisation of the omentum
has been improper.[30] Majority of these occur if the surgeon is unfamiliar with the
anatomy of the omental vascular arcade. Handling of the omentum should be gentle to
prevent thrombosis of omental vessels and care should be taken to prevent omental
torsion while tunnelling.
Presently, there is no experience with omentopexy in patients who have undergone
previous abdominal surgery. In these patients the surgery may be nearly impossible due to
extensive adhesions between the omentum and gut.
:: Future directions
As described by us recently, single stage lumbar sympathectomy and omentopexy is
rapidly emerging as the procedure of choice in these patients with the advantages of a
single stage operation and low cost.[31] However, much work needs to be done in this
field. The question regarding the mechanism of action of omentum needs to be answered.
Long term prospective randomised and controlled clinical trials with longer follow-up are
required to establish this procedure as the first line of management of patients with
Buergers disease. Till then, the quest for an ideal treatment for this grave limbthreatening condition must continue.
:: References
1.
2.
3.
4.

Buerger L. Thromboangitis Obliterans: a study of the vascular lesions leading to


presenile spontaneous gangrene. Am J Med Sci 1908; 136:567-580.
Olin JW. Thromboangitis Obliterans (Buergers Disease). New Engl J Med 2000;
343:864-869.
Fiessinger JN, Schafer M. Trial of iloprost versus aspirin treatment for critical limb
ischaemia of thromboangitis obliterans. The TAO study. Lancet 1990; 335:555557.
Talwar S, Choudhary SK, Bhan A. Buergers disease. Indian Journal of Cardiology
1998; 1:31-34.

5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.

Lau H, Cheng SK. Buergers disease in Hong Kong: a review of 89 cases. Aust NZ J
Surg 1997; 67:264-269.
Sasajima T, Kubo Y, Inaba M, Goh K. Plantar or dorsalis pedis artery bypass in
Buergers disease. Ann Vasc Surg 1994; 8:248-257.
Stricht VJ, Goldstein M, Flamand JP, Belenger J. Evolution and prognosis of
thromboangitis obliterans. J Cardiovasc Surg (Torino)1973; 14:9-16..
Kunlin J, Lengua F, Testart J, Pajot A. F. Thromboangiosis or thromboangitis treated
by adrenalectomy and sympathectomy from 1942 to 1962. J Cardiovasc Surg
(Torino) 1973 ;14:21-27.
Komori K, Kawasaki K, Okazaki J, Eguchi D, Mawatari K, Okadome K, et al.
Thoracoscopic sympathectomy for Buergers disease of the upper extremities. J Vasc
Surg 1995; 22:344-346.
Nakajima N. The change in concept and surgical treatment on Buergers diseasepersonal experience and review. Int J Cardiol 1998; 66(Suppl.1):S273-S280.
Nishikimi N. Fate of limbs with failed vascular reconstruction in Buergers disease.
Int J Cardiol 2000; 75(Suppl1):S183-185.
Drummond D, Morison R. A case of ascites due to cirrhosis of liver cured by
operation. Br Med J 1896; 2:728.
Vineberg A, Lwin MM. Fostering a natural artery bypass for disseminated coronary
artery disease by pericoronary omental strips. Surg Gynecol Obstet 1973; 137:565578.
Goldsmith HS, Saunders RL, Reeves AG, Allen CD, Milne J. Omental transposition
to brain of stroke patients. Stroke 1979; 10:471-472.
Goldsmith HS, Neil-Dwyer G, Barsoum L. Omental transposition to the chronically
injured human spine. Paraplegia 1986; 24:173-74.
Zhang K, Yang YH. Use of pedicled omentum in oesophagogastric anastomosis:
analysis of 100 cases. Ann R Coll Surg Engl 1987; 69:209-211.
Goldsmith HS, de Los Santos R. Omental transposition for primary lymphoedema.
Surg Gynecol Obstet 1967; 125:607-610.
Casten DF, Alday ES. Omental transfer for revascularization of the extremities. Surg
Gynecol Obstet 1971; 123:301-304.
Alday ES, Goldsmith HS. Surgical technique for omental lengthening based on
arterial anatomy. Surg Gynecol Obstet 1972; 135:103-107.
Talwar S, Jain S, Porwal R, Laddha BL, Prasad P. Free versus pedicled omental
grafts for limb salvage in Buergers disease. Aust N Z J Surg 1998; 68:38-40.
Hoshino S, Nakayama K, Igari T, Honda K. Long term results of omental
transplantation for chronic occlusive arterial diseases. Int Surg 1983; 68:47-50.
Maurya SD, Singhal S, Gupta HC, Elhence IP, Sharma BD. Pedicled omental grafts
in the revascularization of ischaemic lower limbs in Buergers disease. Int Surg
1985; 70:253-255.
Agarwal VK, Bajaj S. Salvage of end stage extremity by omentopexy in Buergers
disease. Indian Journal of Thoracic and Cardiovascular Surgery 1987; 5:12-17.
Babu RD, Menon NG, Vaidyanathan S. Pedicled omental transplantation for end
stage Buergers disease as a limb salvage procedure. Indian Journal of Surgery 1990;
52:463-71.
Subodh S, Mohan JC, Malik VK. Omentopexy in limbs revascularization in

26.
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.

37.

Buergers disease. Indian Heart J 1994; 46:355-357.


Singh I, Ramteke VK. The role of omental transfer in Buergers disease: New Delhi
experience. Aust. N.Z. J. Surg 1996; 66:372-376.
Bhargava JS, Makker A, Bhargava K, Shaunik AV, Sharda A, Kumar PS. Pedicled
omental transfer for ischaemic limbs- a 5- year experience. J Indian Med Assoc
1997; 95:100-102.
Supe A, Pandya S, Kamble M, Shikare S. Omental transfer for revascularization of
lower extremity in peripheral vascular disease. Indian Journal of Surgery 1998;
60:115-118.
Ranwaka R, Sharma RK, Mathur SN, Sachdeva G. Revascularization of limbs by
omental transfer. Indian Journal of Surgery 1999; 61:364-66.
Talwar S, Jain S, Porwal R, Laddha BL, Prasad P. Pedicled omental transfer for limb
salvage in Buergers disease. Int J Cardiol 2000; 72:127-132.
Talwar S, Prasad P. Single stage lumbar sympathectomy and omentopexy a new
surgical approach towards patients With Buergers disease. Trop Doct 2001. (In
press)
Lieberman MD, White H. The greater omentum. Heidelberg: Springer Verlag;
1983.
Goldsmith HS, Griffith AL, Catsimpoolas N. Increased vascular perfusion after
administration of an omental lipid fraction. Surg Gynecol Obstet 1986; 162:579583.
Goldsmith HS, Griffith AL, Kupferman A, Catsimpoolas N. Lipid Angiogenic factor
from Omentum. JAMA 1984; 252:2034-2036.
Nishimura A, Sano F, Nakanishi Y, Koshino I, Kasai Y. Omental transplantation for
relief of limb ischaemia. Surg Forum 1977; 28:213-215.
Agarwal VK, Agarwal S. Omental allograft: its role in revascularization of ischaemic
limbs with special reference to the Buergers disease- a clinical and experimental
study. In: Matsumoto A, DeBakey ME, Kondo J, editors. Advances in
Cardiovascular Surgery. New York; Elsevier Science: 1991. pp 89-96.
Khazanchi RK, Nanda V, Kumar R, Garg P, Guleria S, Bal S. Omentum
autotransplantation in thromboangitis obliterans: report of three cases. Surg Today
1999; 29:86-90.

Omentopexy for Limb Salvage in Buergers Disease: Indications,


Technique and Results
Talwar S, Choudhary SK

Department of Cardiothoracic and Vascular Surgery, All India Institute of Medical


Sciences, New Delhi, India.
Code Number: jp01041
Abstract

Buergers disease is a limb-threatening condition occurring in the young and


productive age group and its management has always been a challenging
problem. A large number of medical and surgical options have been suggested,
but the quest for an ideal solution to this problem continues. Omentopexy for
Buergers disease is an attractive option, which is rapidly gaining popularity. We
discuss the historical aspects, technical considerations and results of omental
transfer for this limb-threatening condition. In doing so, the relevant literature on
the subject has been extensively reviewed. In all published series, there has
been marked improvement in intermittent claudication and rest pain. Ischaemic
ulcers have healed and the progression of gangrene has stopped. If carried out
with the complete understanding of the anatomy of the omental vascular arcade,
the results of omentopexy are gratifying, thus avoiding amputation and
conserving the limb.
Key Words: Buergers disease, thromboangitis obliterans, peripheral vascular
disease, omental transfer.
uergers disease (Thromboangitis Obliterans) is a condition characterised by
segmental occlusion of small and medium sized arteries of the lower and
sometimes of upper extremities in young male smokers, often associated with
migratory thrombophlebitis.(1,2) Its treatment has remained an enigma and
multiple strategies have been employed. Drug therapy is of little benefit.(2-4)
Surgical treatment options have consisted of sympathectomy,(5) direct arterial
surgery,(6) adrenalectomy,(7) and amputation as a last resort.(3) With the
exception of cessation of smoking, none of these measures is curative and
conflicting results have been obtained.(2-4,7,8)
However, in patients with critical limb ischaemia, surgery is required to salvage
the limb. Traditionally, patients who have ischaemic signs and symptoms have
been offered sympathectomy(5) despite the fact that relapses are frequent due to
normalisation of vasomotor tone within two weeks to six months after operation.
(7,9) Results of adrenalectomy also continue to be disappointing.(10)
Arterial reconstruction is usually impossible due to distal nature of the disease
and carries a high failure rate.(12) These considerations have always prompted
surgeons to look for an alternative solution in the form of omental transfer. In this

review, we discuss the historical aspects, technical considerations and results of


omental transfer for this limb-threatening condition.
Historical Aspects

The vascularising properties of omentum have been known since a long time and
have included use for absorption of ascites,(12) Myocardial, cerepal and spinal
cord revascularisation,(13-15) and protection of oesophagogastric anastomosis.
(16)
Based on these, pedicled omental transfer was first used by Goldsmith and his
colleagues for surgical relief of chronic lymphoedema of lower limbs in 1967.(17)
Casten and Alday first used this for 24 cases of atherosclerosis(18) and reported
excellent clinical results in terms of relief of symptoms and complete healing of
ulceration and gangrenous areas of toes and feet.
Surgical Anatomy
n understanding of the vascular anatomy of the omental vascular arcade ( Figure 1) is crucial to
the concept of omental lengthening. The right and the left gastroepiploic arteries and their
panches along the greater curative of the stomach form the omental vascular arcade. The
panches consist of the right and left omental artery the middle omental artery the accessory
omental artery and shot omental arteries. The middle omental artery, which is the major panch
further, divides into right and left panch which join the right and left omental arteries. The
presence of this omental arcade allows the omentum to be lengthened as far as down the ankle
by division of the side panches basing the pedicle on the right or the left gastroepiploic artery.
Alday and Goldsmith(19) performed autopsy studies on 136 adult cadavers and described five
types of omental vascular arcades depending upon the level of bifurcation or the absence of the
middle omental artery (Figure 2). Type 1 is most common and involves bifurcation of the middle
omental artery near the lower end of the omentum. In type 2 the middle omental artery bifurcates
midway between the gastroepiploic arcade and the lower end of the omentum. In type 3, it
bifurcates 2-3 centimetres from the gastroepiploic arcade. In type 4 the middle omental artery is
absent and the right and left omental arteries form the omental vascular arcade. In type 5, the
terminal panch of the splenic artery develops into the left omental artery and the right
gastroepiploic artery gives rise to the middle omental artery. The knowledge of these types of
variations is important as the line of division of the vessels depends on this.
Procedure for Omental Lengthening
This was just described by Goldsmith and de Los Santos(17) for relief of chronic lymphoedema of
the extremities in 1967 and later by us and others.(18,19-30) Usually a midline incision is used;
however in recent times it has been combined with single stage sympathectomy in which case a
transverse incision is preferred.(32) The omentum is freed from the transverse colon along the
vascular plane and then from the greater curvature of the stomach taking care to preserve the
gastroepiploic arcades and the blood vessel between the arcades. In doing so the pedicle is
based on either the right or the left gastroepiploic artery based on the dominance.
This pedicled graft is then lengthened depending upon the vascular anatomy and the panches
along the greater curvature of the stomach are tied with silk sutures. As shown in Figure 3, a
subfascial tunnel is then prepared on the anteromedial aspect of the thigh and leg up to the ankle
of the affected limbs after making multiple skin incision. The lengthened omentum is passed down
through this tunnel from the abdomen and pelvis up to the ankle where it is anchored to the

underlying muscle using interrupted silk sutures. The average operating time for the procedure is
usually 140-180 minutes.
Indications
The traditional indications for omentopexy on patients are(20) failure of lumbar sympathectomy to
heal the ulceration or poor demarcation despite lumbar sympathectomy, ulceration not
responding to conservative treatment and incapacitating rest pain and claudication after lumbar
sympathectomy. However, with the realisation of the short-term benefits of lumbar
sympathectomy, single stage lumbar sympathectomy and omentopexy has also been proposed to
be equally successful with the advantages of a single stage operation and low cost.(31)
Mechanism of action
When the procedure was introduced for patients with atherosclerosis, it was thought that omental
transposition works by supplying extra blood to the ischaemic limb. However, this is difficult to
believe, as the diameter of omental vessels is roughly one-tenth of the popliteal artery.(32) Later
studies have demonstrated that the possible mechanism of action of omental transfer is an
increase in local collateral circulation rather than any significant increase in blood flow.(20,23,25)
It has also been demonstrated that the omentum contains a lipid fraction which promotes
neovascularisation.(33,34) Thus a local action on limb musculature with increased local collateral
circulation may be a possible mode of action.
Technical Success during Surgery

he operation is easy if performed with the complete understanding of the


anatomy of the omental vascular arcade. It is usually possible to lengthen the
omentum up to the ankle in nearly all patients. In only three out of 62 cases of
pedicled omental transfer performed by us(30) this was not possible and we
could ping the omentum down only up to the mid-thigh level. Satisfactory results
have been obtained even if the omentum has been pought down up to the midthigh level.(27,29) The technical success of the procedure is reflected by the
immediate and late post-operative results (detailed below).
Clinical improvement during immediate post-operative period

he immediate post-operative results are an indication of the efficacy of


omentopexy. These consist of postoperative relief of rest-pain, increase in
claudication distance, failure of progression of gangrene and healing of ulcers.
Relief of symptoms has been almost immediate in most series.(20-30) Patients
have reported relief of pain in the ischaemic limb even while they had pain at the
abdominal incision site.(30) This has been partly explained by psychological
factors and cessation of smoking following surgery; however increase in tissue
oxygen saturation points to increased blood flow as the possible mechanism of
action.(30) Another important feature of clinical improvement in the postoperative period is an increase in the claudication distance, improvement in skin
temperature, and improvement in tissue oxygen saturation as measured by pulse
oximetry.(27,28,30)
Long-term follow up

At a mean follow-up ranging from 1-5 years in most series,(21-37) the improvement has been
sustained with progressive improvement in claudication distance, healing of ulcers and avoidance
of major amputations as evident from Table 1. Thus, it has been possible to save the limb in
many patients who would otherwise have required below knee or even mid-thigh amputation for
relief of pain or gangrene.
Objective assessment of results of omentopexy
Objective assessment of the results of omentopexy has been carried out using angiography,
(23,25,28) measurement of tissue oxygen saturation,(27,28,30) digital plethysmography and
tread- mill exercise testing.(27)
The measurement of tissue oxygen saturation has been particularly useful as this has improved
within hours of surgery and has shown sustained improvement on early and late follow-up ( Table
2). Nishimura et al(35) have shown an increase in muscle blood flow during exercise and reactive
hyperaemia by using Xenon (X 133) clearance studies.
Agarwal et al(23) performed postoperative angiography in 50 patients who underwent omental
grafting and observed increased number of collaterals at graft site with filling of vessels distal to
the block in the limbs. In an extension of the same study,(36) 20 dogs underwent allograft
omental transfer in hind limbs after ligation of the femoral artery in 10 of these. At the end of three
weeks, exploration of the graft site revealed increased number of collaterals at the graft site with
filling of vessels distal to the site of the block. The authors concluded that even a blood group and
human leukocyte antigen mismatched omental graft is taken up and revascularises the ischaemic
limb.
Bhargava et al(27) performed treadmill exercise testing of the patients before and after
omentopexy. In the preoperative period, the claudication free period on treadmill was 2-3 minutes,
which increased to 6-9 minutes following omentopexy (p<0.05). Also mean tolerated workload
increased significantly. Subodh et al25 performed post-operative Doppler studies and selective
coeliac- axis angiography to study the circulation in the omental graft. In 18 of their 20 cases, the
arterial pulsations were heard till the knee on Doppler study. In 2 cases in which they were not
heard, there was no improvement in symptoms. However on coeliac-axis angiography, the
omental vessels were visualised till mid-thigh in only six and up to the knee in only four patients.
The authors concluded that omental transposition probably works by promoting local
collateralisation. Similar conclusions were drawn in another study comparing free versus pedicled
omental grafts.20 Khazanchi et al37 have also reported improved vascularity in the limb on serial
Doppler studies after omentopexy.
Complications and technical failures
In general, the operation is very safe. Even when the omental graft has autolysed, major
complications are unusual. The most frequently encountered complications include prolonged
ileus and minor wound infection at the incision sites. Incisional hernia has been reported to occur
from the abdominal incision site.(26,27,30)
Failures have been shown to result in patients in whom the mobilisation of the omentum has been
improper.(30) Majority of these occur if the surgeon is unfamiliar with the anatomy of the omental
vascular arcade. Handling of the omentum should be gentle to prevent thrombosis of omental
vessels and care should be taken to prevent omental torsion while tunnelling.
Presently, there is no experience with omentopexy in patients who have undergone previous
abdominal surgery. In these patients the surgery may be nearly impossible due to extensive
adhesions between the omentum and gut.

Future Directions
As described by us recently, single stage lumbar sympathectomy and omentopexy is rapidly
emerging as the procedure of choice in these patients with the advantages of a single stage
operation and low cost.(31) However, much work needs to be done in this field. The question
regarding the mechanism of action of omentum needs to be answered. Long term prospective
randomised and controlled clinical trials with longer follow-up are required to establish this
procedure as the first line of management of patients with Buergers disease. Till then, the quest
for an ideal treatment for this grave limb-threatening condition must continue.
References
1. Buerger L. Thromboangitis Obliterans: a study of the vascular lesions leading to presenile
spontaneous gangrene. Am J Med Sci 1908; 136:567-580.
2. Olin JW. Thromboangitis Obliterans (Buergers Disease). New Engl J Med 2000;
343:864-869. MEDLINE
3. Fiessinger JN, Schafer M. Trial of iloprost versus aspirin treatment for critical limb
ischaemia of thromboangitis obliterans. The TAO study. Lancet 1990; 335:555-557.

MEDLINE
4. Talwar S, Choudhary SK, Bhan A. Buergers disease. Indian Journal of Cardiology 1998;
1:31-34.
5. Lau H, Cheng SK. Buergers disease in Hong Kong: a review of 89 cases. Aust NZ J
Surg 1997; 67:264-269.
6. Sasajima T, Kubo Y, Inaba M, Goh K. Plantar or dorsalis pedis artery bypass in Buergers
disease. Ann Vasc Surg 1994; 8:248-257. MEDLINE
7. Stricht VJ, Goldstein M, Flamand JP, Belenger J. Evolution and prognosis of
thromboangitis obliterans. J Cardiovasc Surg (Torino)1973; 14:9-16..
8. Kunlin J, Lengua F, Testart J, Pajot A. F. Thromboangiosis or thromboangitis treated by
adrenalectomy and sympathectomy from 1942 to 1962. J Cardiovasc Surg (Torino)
1973 ;14:21-27. MEDLINE
9. Komori K, Kawasaki K, Okazaki J, Eguchi D, Mawatari K, Okadome K, et al.
Thoracoscopic sympathectomy for Buergers disease of the upper extremities. J Vasc
Surg 1995; 22:344-346. MEDLINE
10. Nakajima N. The change in concept and surgical treatment on Buergers diseasepersonal experience and review. Int J Cardiol 1998; 66(Suppl.1):S273-S280. MEDLINE
11. Nishikimi N. Fate of limbs with failed vascular reconstruction in Buergers disease. Int J
Cardiol 2000; 75(Suppl1):S183-185. MEDLINE
12. Drummond D, Morison R. A case of ascites due to cirrhosis of liver cured by operation. p
Med J 1896; 2:728.
13. Vineberg A, Lwin MM. Fostering a natural artery bypass for disseminated coronary artery
disease by pericoronary omental strips. Surg Gynecol Obstet 1973; 137:565-578.

MEDLINE
14. Goldsmith HS, Saunders RL, Reeves AG, Allen CD, Milne J. Omental transposition to
pain of stroke patients. Stroke 1979; 10:471-472. MEDLINE
15. Goldsmith HS, Neil-Dwyer G, Barsoum L. Omental transposition to the chronically injured
human spine. Paraplegia 1986; 24:173-74. MEDLINE
16. Zhang K, Yang YH. Use of pedicled omentum in oesophagogastric anastomosis: analysis
of 100 cases. Ann R Coll Surg Engl 1987; 69:209-211. MEDLINE
17. Goldsmith HS, de Los Santos R. Omental transposition for primary lymphoedema. Surg
Gynecol Obstet 1967; 125:607-610. MEDLINE
18. Casten DF, Alday ES. Omental transfer for revascularization of the extremities. Surg
Gynecol Obstet 1971; 123:301-304.

19. Alday ES, Goldsmith HS. Surgical technique for omental lengthening based on arterial
anatomy. Surg Gynecol Obstet 1972; 135:103-107. MEDLINE
20. Talwar S, Jain S, Porwal R, Laddha BL, Prasad P. Free versus pedicled omental grafts for
limb salvage in Buergers disease. Aust N Z J Surg 1998; 68:38-40. MEDLINE
21. Hoshino S, Nakayama K, Igari T, Honda K. Long term results of omental transplantation
for chronic occlusive arterial diseases. Int Surg 1983; 68:47-50. MEDLINE
22. Maurya SD, Singhal S, Gupta HC, Elhence IP, Sharma BD. Pedicled omental grafts in the
revascularization of ischaemic lower limbs in Buergers disease. Int Surg 1985; 70:253255. MEDLINE
23. Agarwal VK, Bajaj S. Salvage of end stage extremity by omentopexy in Buergers
disease. Indian Journal of Thoracic and Cardiovascular Surgery 1987; 5:12-17.
24. Babu RD, Menon NG, Vaidyanathan S. Pedicled omental transplantation for end stage
Buergers disease as a limb salvage procedure. Indian Journal of Surgery 1990; 52:46371.
25. Subodh S, Mohan JC, Malik VK. Omentopexy in limbs revascularization in Buergers
disease. Indian Heart J 1994; 46:355-357. MEDLINE
26. Singh I, Ramteke VK. The role of omental transfer in Buergers disease: New Delhi
experience. Aust. N.Z. J. Surg 1996; 66:372-376. MEDLINE
27. Bhargava JS, Makker A, Bhargava K, Shaunik AV, Sharda A, Kumar PS. Pedicled
omental transfer for ischaemic limbs- a 5- year experience. J Indian Med Assoc 1997;
95:100-102. MEDLINE
28. Supe A, Pandya S, Kamble M, Shikare S. Omental transfer for revascularization of lower
extremity in peripheral vascular disease. Indian Journal of Surgery 1998; 60:115-118.
29. Ranwaka R, Sharma RK, Mathur SN, Sachdeva G. Revascularization of limbs by
omental transfer. Indian Journal of Surgery 1999; 61:364-66.
30. Talwar S, Jain S, Porwal R, Laddha BL, Prasad P. Pedicled omental transfer for limb
salvage in Buergers disease. Int J Cardiol 2000; 72:127-132. MEDLINE
31. Talwar S, Prasad P. Single stage lumbar sympathectomy and omentopexy a new
surgical approach towards patients With Buergers disease. Trop Doct 2001. (In press)
32. Lieberman MD, White H. The greater omentum. Heidelberg: Springer Verlag; 1983.
33. Goldsmith HS, Griffith AL, Catsimpoolas N. Increased vascular perfusion after
administration of an omental lipid fraction. Surg Gynecol Obstet 1986; 162:579-583.

MEDLINE
34. Goldsmith HS, Griffith AL, Kupferman A, Catsimpoolas N. Lipid Angiogenic factor from
Omentum. JAMA 1984; 252:2034-2036. MEDLINE
35. Nishimura A, Sano F, Nakanishi Y, Koshino I, Kasai Y. Omental transplantation for relief of
limb ischaemia. Surg Forum 1977; 28:213-215. MEDLINE
36. Agarwal VK, Agarwal S. Omental allograft: its role in revascularization of ischaemic limbs
with special reference to the Buergers disease- a clinical and experimental study. In:
Matsumoto A, DeBakey ME, Kondo J, editors. Advances in Cardiovascular Surgery. New
York; Elsevier Science: 1991. pp 89-96.
37. Khazanchi RK, Nanda V, Kumar R, Garg P, Guleria S, Bal S. Omentum
autotransplantation in thromboangitis obliterans: report of three cases. Surg Today 1999;
29:86-90. MEDLINE

THORACOSCOPIC SYMPATHECTOMY FOR BUERGERS DISEASE: A


CASE REPORT
Hrvoje Hochstdter, Miroslav Bekavac Belin, Drago DeSyo, August Miji and
Dubravka ali
Department of Surgery, Sestre milosrdnice University Hospital, Zagreb, Croatia
SUMMARY A case is presented of thoracoscopic sympathectomy in a 40-year-old male patient with a diagnosis of Buergers disease, who
presented with vasospastic symptoms of coldness and pain at rest in his upper extremities, and a syndrome of analgesic overdosage. The patient
was scheduled for operation. The operation was assisted by an experienced vascular surgeon. No major complications were observed during the
operation. Postoperative recovery of the patient was fast, and he was discharged from the hospital on the second postoperative day, free from
vasospastic symptoms and with no analgesia required.

Key words: Thromboangiitis obliterans, surgery; Sympathectomy; methods; Thoracoscopy;

Introduction
Buergers disease is a specific, idiopathic, recurrent, segmental, inflammatory obliterative vascular disease
involving medium-sized arteries and veins of the limbs1. Upper thoracic sympathectomy has an established
role in the treatment of selected patients with hyperhidrosis, causalgia, Raynauds disease, long QT
syndrome, and Buergers disease2. Sympathectomy with the removal of the second thoracic ganglion of the
ipsilateral side effectively reduces the sympathetic drive to the hand by removing the preganglionic fibers
to the upper extremities and results in relief of vasospastic symptoms, in dryness of the palm and relief of
pain and trophic ulcera1-3.
Several open surgery approaches are available. Although the supraclavicular route is commonly used, the
abundance of important structures in the root of the neck makes the approach difficult. The posterior
approach, although direct, necessitates partial rib resection and is consequently painful4. The transthoracic
approach is convenient as it is direct and the access is good, but it requires a thoracotomy. Presently, as
open thoracoscopy is being replaced by minimal access video-thoracoscopy techniques, the transthoracic
route has attracted even greater popularity than before 4,5.
Operative Method
The patient requires general anesthesia with double-lumen endotracheal intubation for single lung
ventilation. Positioning of the patient is similar to other types of thoracoscopic procedures, i.e. the full
lateral position with the affected side upward.
The video-endoscope port is 10 mm in size and is introduced in the 4th intercostal space in the midaxillary
line after prior deflation of the lung. Two 5-mm operating ports are also placed along the anterior axillary
line at the 4th and 6th intercostal spaces.
The thoracic view of the inlet of the chest shows the ribs in concentric alignment. The sympathetic chain is
identified as a white beaded cord beneath the parietal pleura and lying over the neck of the ribs.

Each ganglion is represented by a slight dilatation at intervals along the nerve chain. The first thoracic
ganglion is usually fused with the lower cervical ganglion to form the stellate ganglion. The second and
third thoracic ganglia are fusiform and lie in relation to the neck of the third and fourth ribs, respectively.
The sympathetic chain lies underneath the parietal pleura and may not be distinct video-endoscopically
until the pleura has been incised and dissected off to expose the nerve trunk. The individual ganglia should
be clearly identified to avoid injury to the lower cervical/first thoracic (stellate) ganglion, which will result
in an ipsilateral Horners syndrome. The upper resection margin of the second thoracic ganglion should not
extend above the lower border of the second rib if injury to the stellate ganglion is to be avoided. Division
of the overlying pleura in the line of the sympathetic trunk allows the ganglion to be easily approached. The
second thoracic ganglion is freed by dissection, and ablative surgery can be completed by either
electrocautery or complete excision of the whole ganglion. The sympathetic chain is divided twice, once
below the first thoracic ganglion, just above the upper border of the third rib, with laparoscopic hook
scissors or microscissors. The second thoracic ganglion is then completely removed for histologic
examination.
Postdivision of the ganglion results in a rise of blood flow to the hand. A cutaneous temperature probe can
be used to show changes in skin temperature following sympathectomy.
A chest drain is inserted through the 10-mm port at the end of the lung reinflation.
Results
The patient, a 40-year-old man with a diagnosis of Buergers disease, presented with vasospastic symptoms
of coldness and pain at rest in both of his arms. The patient had been operated on by lumbar
sympathectomy using an open method at another hospital.
Now, the patient suffered from heavy analgesic overdosing and trophic ulcers of the fingers, resistant to
conservative therapy. He was scheduled for thoracoscopic sympathectomy, in consultation with an
experienced vascular surgeon. Bilateral thoracoscopic sympathectomy was performed as described above.
During the operation, no major complications occurred. Postoperative recovery of the patient was quite
fast. A minor subcutaneous emphysema resorbed on the second day postoperatively, when the patient was
discharged from the hospital. Vasospastic symptoms disappeared, and the patient required no analgesic
therapy anymore. Outpatient follow-up showed rapid disappearance of the trophic ulcers and restoration of
the skin continuity.
Discussion
Thoracoscopic sympathectomy is an easy to perform and safe method in comparison with open surgery
thoracotomy. It enables fast recovery and short hospitalization of the patient. Thoracoscopic
sympathectomy points to a potential of further improvement in the surgical treatment for Buergers disease.

Correspondence to: Hrvoje Hochstdter, M.D., Department of Surgery, Sestre milosrdnice University Hospital, Vinogradska c. 29, HR-10000
Zagreb, Croatia

Received November 11, 1999, accepted March 2, 2000

References

1. HARDY JD. Hardys textbook of surgery. Philadelphia: JB Lippincott Company, 1983:845-8.


2. ISHIBASHI H, HAYAKAWA N. Thoracoscopic sympathectomy for Buergers disease: a report on the successful treatment of four patients.
Surg Today 1995;25:180-3.
3. KOMORI K, KAWASAKI K, OKAZAKI J. Thoracoscopic sympathectomy for Buergers disease of the upper extremities. J Vasc Surg
1995;22:344-6.
4. MACK P. Manual of basic operative laparoscopic and thoracoscopic surgery. Singapore Forces Publications, 1993.
5. WATFANASIRICHAIGOON S, KATKHOUDA N, NGAORUNSGARI U. Totally extraperitoneal laparoscopic lumbar sympathectomy. End
Surgery 1994;12:122-5.

Saetak
TORAKOSKOPSKA SIMPATEKTOMIJA KOD BUERGEROVE BOLESTI: PRIKAZ
BOLESNIKA
H. Hochstdter, M. Bekavac Belin, D. DeSyo, A. Miji i D. ali
Prikazan je sluaj torakoskopske simpatektomije u 40-godinjeg bolesnika s dijagnozom Buergerove
bolesti sa simptomima hladnoe ruku i bolova u mirovanju, kao i predoziranosti analgeticima. Bolesnik je
odreen za operacijsko lijeenje, koje je izvedeno uz asistenciju iskusnog vaskularnog kirurga. Za vrijeme
operacije nije bilo veih komplikacija. Poslijeoperacijski oporavak bio je brz i bolesnik je otputen iz
bolnice drugoga dana nakon operacije, uz nestanak vazospastinih simptoma i bez potrebe za analgeticima.

Kljune rijei: Tromboangiitis obliterans, operacija; Simpatektomija, metode; Torakoskopija


Orphanet J Rare Dis. 2006; 1: 14.
Published online 2006 April 27. doi: 10.1186/1750PMCID: PMC1523324
1172-1-14.
Copyright 2006 Arkkila; licensee BioMed Central Ltd.

Thromboangiitis obliterans (Buerger's


disease)
Perttu ET Arkkila

Department of Gastroenterology, Helsinki University, Centrala Hospital, 00029


Hus, Finland
Corresponding author.
Perttu ET Arkkila: perttu.arkkila@hus.fi
Received April 5, 2006; Accepted April 27, 2006.
This is an Open Access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/2.0),
which permits unrestricted use, distribution, and reproduction in any medium,
provided the original work is properly cited.
Top
Abstract
Disease name and synonyms
Definition
Epidemiology
Clinical description
Diagnostic criteria
Diagnostic methods
Differential diagnosis

Abstract
Thromboangiitis
obliterans or Buerger's
disease is a segmental
occlusive inflammatory
condition of arteries

Etiology
Histopathology
Management including treatment
References

and veins,
characterized by
thrombosis and
recanalization of the
affected vessels. It is a
non-atherosclerotic
inflammatory disease
affecting small and
medium sized arteries
and veins of upper and
lower extremities. The
clinical criteria include:
age under 45 years;
current or recent
history of tobacco use;
presence of distalextremity ischemia
indicated by
claudication, pain at
rest, ischemic ulcers or
gangrenes and
documented by noninvasive vascular
testing; exclusion of
autoimmune diseases,
hypercoagulable states
and diabetes mellitus;
exclusion of a proximal
source of emboli by
echocardiography or
arteriography;
consistent
arteriographic findings
in the clinically
involved and noninvolved limbs. The
disease is found
worldwide, the
prevalence among all
patients with peripheral
arterial disease ranges

Top

from values as low as


0.5 to 5.6% in Western
Europe to values as
high as 45 to 63% in
India, 16 to 66% in
Korea and Japan, and
80% among Ashkenazi
Jews. The etiology of
thromboangiitis
obliterans is unknown,
but use or exposure to
tobacco is central to the
initiation and
progression of the
disease. If the patient
smokes, stopping
completely is an
essential first step of
treatment. The
effectiveness of other
treatments including
vasodilating or anticlotting drugs, surgical
revascularization or
sympathectomy in
preventing amputation
or treating pain,
remains to be
determined.
Disease name and
synonyms
Thromboangiitis
obliterans
Buerger's disease

Top

Definition
Thromboangiitis
obliterans (TAO) is a
segmental occlusive
inflammatory condition

of arteries and veins,


characterized by
thrombosis and
recanalization of the
affected vessels [1,2]. It
is a non-atherosclerotic
inflammatory disease
affecting small and
medium sized arteries
and veins of the upper
and lower extremities
[3].
Top

Epidemiology
The disease is found
worldwide, but the
highest incidence of
thromboangiitis
obliterans occurs in the
Middle and Far East
[4,5]. The prevalence
of the disease in the
general population in
Japan was estimated at
5/100,000 persons in
1985 [6]. The
prevalence of the
disease among all
patients with peripheral
arterial disease ranges
from values as low as
0.5 to 5.6% in Western
Europe to values as
high as 45 to 63% in
India, 16 to 66% in
Korea and Japan, and
80% among Jews of
Ashkenazi ancestry
living in Israel. Part of
this variation in disease
prevalence may be due

to variability in
diagnostic criteria [7,8].
Top
Abstract
Disease name and synonyms
Definition
Epidemiology
Clinical description
Diagnostic criteria
Diagnostic methods
Differential diagnosis
Etiology
Histopathology
Management including treatment
References

Clinical description
The onset of Buerger's
disease occurs between
40 and 45 years of age,
and men are most
commonly affected. It
begins with ischemia of
the distal small vessels
of the arms, legs, hands
and feet. Involvement
of the large arteries is
unusual and rarely
occurs in the absence of
occlusive disease of the
small vessels [9].
Patients may present
with claudication of the
feet, legs, hands and
arms. The pain
typically begins in the
extremities, but may
radiate to more central
parts of the body. As
the disease progresses,
typical calf claudication
and eventually
ischemic pain at rest
and ischemic
ulcerations on the toes,
feet or fingers may
develop [10]. Due to
the likehood of
involvement of more
than one limb [11], it is
advisable to obtain an
arteriogram of both
arms or legs, or all four
limbs in patients who

present with clinical


involvement of only
one limb. Limbs that
are clinically not
affected could present
arteriographic
abnormalities. Other
signs and symptoms of
the disease may include
numbness and/or
tingling in the limbs,
skin ulcerations and
gangrene of the digits.
Superficial
thrombophlebitis and
Raynaud's phenomenon
occur in approximately
40% of patients with
thromboangiitis
obliterans [3].
Although Buerger's
disease most commonly
affects the small and
medium-sized arteries
and veins in the arms,
hands, legs and feet, it
has been reported in
many other vascular
beds. There are case
reports of involvement
of the cerebral and
coronary arteries, aorta,
intestinal vessels, and
even multiple-organ
involvement [12-15].
When TAO occurs in
unusual locations, the
diagnosis should be
made only when

histopathological
examination identifies
the acute-phase lesions
[3].
Gastrointestinal
involvement of TAO
remains rare, however,
intestinal
manifestations like
stricture or perforation
of the colon may
become apparent long
before symptoms of
severe peripheral
arterial disease in
patients with TAO [14].
Top
Abstract
Disease name and synonyms
Definition
Epidemiology
Clinical description
Diagnostic criteria
Diagnostic methods
Differential diagnosis
Etiology
Histopathology
Management including treatment
References

Diagnostic criteria
Since the specificity of
Buerger's disease is
characterized by
peripheral ischemia of
inflammatory nature
with a self-limiting
course, diagnostic
criteria should be
discussed from clinical
point of view.
Several different
criteria have been
proposed for the
diagnosis of
thromboangiitis
obliterans.
Diagnostic criteria of
Shionoya (1998) [16]
smoking history;
onset before the age

of 50 years;
infrapopliteal arterial
occlusions;
either arm
involvement or
phlebitis migrans;
absence of
atherosclerotic risk
factors other than
smoking.
Diagnostic criteria of
Olin (2000) [10]
age under 45 years;
current or recent
history of tobacco use;
the presence of distalextremity ischemia
indicated by
claudication, pain at
rest, ischemic ulcers or
gangrenes and
documented by noninvasive vascular
testing;
exclusion of
autoimmune diseases,
hypercoagulable states
and diabetes mellitus;
exclusion of a
proximal source of
emboli by
echocardiography or
arteriography;
consistent

arteriographic findings
in the clinically
involved and noninvolved limbs.
Top
Abstract
Disease name and synonyms
Definition
Epidemiology
Clinical description
Diagnostic criteria
Diagnostic methods
Differential diagnosis
Etiology
Histopathology
Management including treatment
References

Diagnostic methods
No specific laboratory
test for diagnosing
Buerger's disease is
available. Unlike other
types of vasculitis, in
patients with Buerger's
disease the acute-phase
reactions (such as the
erythrocyte
sedimentation rate and
C-reactive protein
level) are normal [3].
Recommended tests to
rule out other causes of
vasculitis include a
complete blood cell
count; liver function
tests; determination of
serum creatinine
concentrations, fasting
blood sugar levels and
sedimentation rate;
tests for antinuclear
antibody, rheumatoid
factor, serologic
markers for CREST
(calcinosis cutis,
Raynaud phenomenon,
sclerodactyly and
telangiectasia)
syndrome and
scleroderma, and
screening for
hypercoagulability.

Screening for
hypercoagulopathy,
including
antiphosolipid
antibodies and
homocystein in patients
with Buerger's disease,
is recommended.
If a proximal source of
embolization is
suspected, transthoracic
or transesophageal
echocardiography and
arteriography should be
performed.
Angiographic findings
include severe distal
segmental occlusive
lesions. The more
proximal arteries are
normal. The role of
modern imaging
methods, such as
computerised
tomography (CT) and
magnetic resonance
imaging (MRI) in
diagnosis and
differential diagnosis of
Buerger's disease still
remains unsettled. In
patients with leg
ulceration suspected of
having TAO, the Allen
test should be
performed to assess the
circulation in the hands
and fingers [17].
Top
Abstract

Differential diagnosis

Disease name and synonyms


Definition
Epidemiology
Clinical description
Diagnostic criteria
Diagnostic methods
Differential diagnosis
Etiology
Histopathology
Management including treatment
References

The distal nature of


TAO and the
involvement of the legs
and arms help to
differentiate this
disease from
atherosclerosis. In
TAO, the internal
elastic lamina and the
media are preserved in
contrast to systemic
vasculitis, in which
disruption of these
lamina is usually
striking [18].
An abnormal Allen test
[7,19] in a young
smoker presenting with
leg ulcerations is highly
suggestive of TAO.
This test demonstrates
small vessel
involvement in both the
arms and the legs.
However, an abnormal
result can also be
present in other types
of small vessel
occlusive diseases of
the hand such as
scleroderma, CREST
syndrome, repetitive
trauma, emboli,
hypercoagulable states
and vasculitis.

Top
Abstract
Disease name and synonyms
Definition
Epidemiology
Clinical description

Etiology
Although the cause of
Buerger's disease
remains unknown, a

Diagnostic criteria
Diagnostic methods
Differential diagnosis
Etiology
Histopathology
Management including treatment
References

strong association with


tobacco use has been
established [3]. Use or
exposure to tobacco
plays central role in the
initiation and
progression of the
disease. By using an
antigen-sensitive
thymidineincorporation assay,
Adar et al. [20] showed
that patients with TAO
have an increased
cellular sensitivity to
type I and III collagen,
compared to that in
patients with
arteriosclerosis
obliterans or healthy
males. De Moerloose et
al. [21] found a marked
decrease in frequency
of the HLA-B12
antigen in patients with
Buerger's disease (2.2%
vs. 28% in controls).
Similarly to other
autoimmune diseases,
TAO may have a
genetic predisposition
without a direct
"causative" gene
mutation. Most
investigators feel that
Buerger's disease is an
immune-mediated
endarteritis. Recent
immunocytochemical
studies have

demonstrated a linear
deposition of
immunoglobulins and
complement factors
along the elastic lamina
[22]. The inciting
antigen has not been
discovered. The role of
hyperhomocysteinemia
in the pathogenesis of
Buerger's disease is
controversial [23]. An
association between
thrombophilic
conditions such as
antiphospholipid
syndrome and
Buerger's disease has
also been suggested
[24].
Peripheral
endothelium-dependent
vasodilation is impaired
in patients with
Buerger's disease,
while non-endothelial
mechanisms of
vasodilation seem to be
intact [25].
Top
Abstract
Disease name and synonyms
Definition
Epidemiology
Clinical description
Diagnostic criteria
Diagnostic methods
Differential diagnosis
Etiology
Histopathology
Management including treatment
References

Histopathology
While the clinical
criteria of TAO are
relatively well defined,
there is no consensus
on the histopathological
findings [26]. It is
particularly difficult to
distinguish
morphologically TAO

from ateriosclerosis
obliterans (ASO).
Histopatological
findings are also known
to vary according to the
duration of the disease
[3]. The findings are
most likely to be
diagnostic in the acute
phase of the disease,
most commonly at
biopsy of a segment of
a vessel with
superficial
thrombophlebitis [10].
Other histopathological
phases, such as
intermediate (subacute)
and end-state (chronic)
phases, have been
described.
The acute-phase
lesions include an
occlusive, highly
cellular, inflammatory
thrombus with less
inflammation in the
walls of the blood
vessels.
Polymorphonuclear
leukocytes,
microabscesses and
multinucleated giant
cells may exist. When
TAO occurs in unusual
locations, the diagnosis
should be made only
when histopathological
examination identifies

the acute-phase lesion.


In the intermediate
phase of disease there
is progressive
organization of the
thrombus in the arteries
and veins.
When only organized
thrombus and fibrosis
are found in the blood
vessels, the phase is
considered to be endstage [27-29].

Thromboangiitis obliterans (Buerger's disease)


Perttu ET Arkkila
Department of Gastroenterology, Helsinki University, Centrala Hospital, 00029 Hus, Finland
author email
corresponding author email
Orphanet Journal of Rare Diseases 2006, 1:14doi:10.1186/1750-1172-1-14
The electronic version of this article is the complete one and can be found online at:
http://www.OJRD.com/content/1/1/14
Received:

5 April 2006

Accepted:

27 April 2006

Published: 27 April 2006


2006 Arkkila; licensee BioMed Central Ltd.
This is an Open Access article distributed under the terms of the Creative Commons Attribution
License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution,
and reproduction in any medium, provided the original work is properly cited.

Abstract
Thromboangiitis obliterans or Buerger's disease is a segmental occlusive inflammatory
condition of arteries and veins, characterized by thrombosis and recanalization of the affected
vessels. It is a non-atherosclerotic inflammatory disease affecting small and medium sized
arteries and veins of upper and lower extremities. The clinical criteria include: age under 45
years; current or recent history of tobacco use; presence of distal-extremity ischemia
indicated by claudication, pain at rest, ischemic ulcers or gangrenes and documented by noninvasive vascular testing; exclusion of autoimmune diseases, hypercoagulable states and
diabetes mellitus; exclusion of a proximal source of emboli by echocardiography or
arteriography; consistent arteriographic findings in the clinically involved and non-involved

limbs. The disease is found worldwide, the prevalence among all patients with peripheral
arterial disease ranges from values as low as 0.5 to 5.6% in Western Europe to values as high
as 45 to 63% in India, 16 to 66% in Korea and Japan, and 80% among Ashkenazi Jews. The
etiology of thromboangiitis obliterans is unknown, but use or exposure to tobacco is central to
the initiation and progression of the disease. If the patient smokes, stopping completely is an
essential first step of treatment. The effectiveness of other treatments including vasodilating
or anti-clotting drugs, surgical revascularization or sympathectomy in preventing amputation
or treating pain, remains to be determined.

Disease name and synonyms


Thromboangiitis obliterans
Buerger's disease

Definition
Thromboangiitis obliterans (TAO) is a segmental occlusive inflammatory condition of arteries
and veins, characterized by thrombosis and recanalization of the affected vessels [1,2]. It is a
non-atherosclerotic inflammatory disease affecting small and medium sized arteries and veins
of the upper and lower extremities [3].

Epidemiology
The disease is found worldwide, but the highest incidence of thromboangiitis obliterans occurs
in the Middle and Far East [4,5]. The prevalence of the disease in the general population in
Japan was estimated at 5/100,000 persons in 1985 [6]. The prevalence of the disease among
all patients with peripheral arterial disease ranges from values as low as 0.5 to 5.6% in
Western Europe to values as high as 45 to 63% in India, 16 to 66% in Korea and Japan, and
80% among Jews of Ashkenazi ancestry living in Israel. Part of this variation in disease
prevalence may be due to variability in diagnostic criteria [7,8].

Clinical description
The onset of Buerger's disease occurs between 40 and 45 years of age, and men are most
commonly affected. It begins with ischemia of the distal small vessels of the arms, legs, hands
and feet. Involvement of the large arteries is unusual and rarely occurs in the absence of
occlusive disease of the small vessels [9]. Patients may present with claudication of the feet,
legs, hands and arms. The pain typically begins in the extremities, but may radiate to more
central parts of the body. As the disease progresses, typical calf claudication and eventually
ischemic pain at rest and ischemic ulcerations on the toes, feet or fingers may develop [10].
Due to the likehood of involvement of more than one limb [11], it is advisable to obtain an
arteriogram of both arms or legs, or all four limbs in patients who present with clinical
involvement of only one limb. Limbs that are clinically not affected could present
arteriographic abnormalities. Other signs and symptoms of the disease may include numbness
and/or tingling in the limbs, skin ulcerations and gangrene of the digits. Superficial
thrombophlebitis and Raynaud's phenomenon occur in approximately 40% of patients with
thromboangiitis obliterans [3].

Although Buerger's disease most commonly affects the small and medium-sized arteries and
veins in the arms, hands, legs and feet, it has been reported in many other vascular beds.
There are case reports of involvement of the cerebral and coronary arteries, aorta, intestinal
vessels, and even multiple-organ involvement [12-15].
When TAO occurs in unusual locations, the diagnosis should be made only when
histopathological examination identifies the acute-phase lesions [3].
Gastrointestinal involvement of TAO remains rare, however, intestinal manifestations like
stricture or perforation of the colon may become apparent long before symptoms of severe
peripheral arterial disease in patients with TAO [14].

Diagnostic criteria
Since the specificity of Buerger's disease is characterized by peripheral ischemia of
inflammatory nature with a self-limiting course, diagnostic criteria should be discussed from
clinical point of view.
Several different criteria have been proposed for the diagnosis of thromboangiitis obliterans.

Diagnostic criteria of Shionoya (1998) [16]


smoking history;
onset before the age of 50 years;
infrapopliteal arterial occlusions;
either arm involvement or phlebitis migrans;
absence of atherosclerotic risk factors other than smoking.

Diagnostic criteria of Olin (2000) [10]


age under 45 years;
current or recent history of tobacco use;
the presence of distal-extremity ischemia indicated by claudication, pain at rest, ischemic
ulcers or gangrenes and documented by non-invasive vascular testing;
exclusion of autoimmune diseases, hypercoagulable states and diabetes mellitus;
exclusion of a proximal source of emboli by echocardiography or arteriography;
consistent arteriographic findings in the clinically involved and non-involved limbs.

Diagnostic methods
No specific laboratory test for diagnosing Buerger's disease is available. Unlike other types of
vasculitis, in patients with Buerger's disease the acute-phase reactions (such as the
erythrocyte sedimentation rate and C-reactive protein level) are normal [3].

Recommended tests to rule out other causes of vasculitis include a complete blood cell count;
liver function tests; determination of serum creatinine concentrations, fasting blood sugar
levels and sedimentation rate; tests for antinuclear antibody, rheumatoid factor, serologic
markers for CREST (calcinosis cutis, Raynaud phenomenon, sclerodactyly and telangiectasia)
syndrome and scleroderma, and screening for hypercoagulability. Screening for
hypercoagulopathy, including antiphosolipid antibodies and homocystein in patients with
Buerger's disease, is recommended.
If a proximal source of embolization is suspected, transthoracic or transesophageal
echocardiography and arteriography should be performed. Angiographic findings include
severe distal segmental occlusive lesions. The more proximal arteries are normal. The role of
modern imaging methods, such as computerised tomography (CT) and magnetic resonance
imaging (MRI) in diagnosis and differential diagnosis of Buerger's disease still remains
unsettled. In patients with leg ulceration suspected of having TAO, the Allen test should be
performed to assess the circulation in the hands and fingers [17].

Differential diagnosis
The distal nature of TAO and the involvement of the legs and arms help to differentiate this
disease from atherosclerosis. In TAO, the internal elastic lamina and the media are preserved
in contrast to systemic vasculitis, in which disruption of these lamina is usually striking [18].
An abnormal Allen test [7,19] in a young smoker presenting with leg ulcerations is highly
suggestive of TAO. This test demonstrates small vessel involvement in both the arms and the
legs. However, an abnormal result can also be present in other types of small vessel occlusive
diseases of the hand such as scleroderma, CREST syndrome, repetitive trauma, emboli,
hypercoagulable states and vasculitis.

Etiology
Although the cause of Buerger's disease remains unknown, a strong association with tobacco
use has been established [3]. Use or exposure to tobacco plays central role in the initiation
and progression of the disease. By using an antigen-sensitive thymidine-incorporation assay,
Adar et al. [20] showed that patients with TAO have an increased cellular sensitivity to type I
and III collagen, compared to that in patients with arteriosclerosis obliterans or healthy males.
De Moerloose et al. [21] found a marked decrease in frequency of the HLA-B12 antigen in
patients with Buerger's disease (2.2% vs. 28% in controls). Similarly to other autoimmune
diseases, TAO may have a genetic predisposition without a direct "causative" gene mutation.
Most investigators feel that Buerger's disease is an immune-mediated endarteritis. Recent
immunocytochemical studies have demonstrated a linear deposition of immunoglobulins and
complement factors along the elastic lamina [22]. The inciting antigen has not been
discovered. The role of hyperhomocysteinemia in the pathogenesis of Buerger's disease is
controversial [23]. An association between thrombophilic conditions such as antiphospholipid
syndrome and Buerger's disease has also been suggested [24].
Peripheral endothelium-dependent vasodilation is impaired in patients with Buerger's disease,
while non-endothelial mechanisms of vasodilation seem to be intact [25].

Histopathology
While the clinical criteria of TAO are relatively well defined, there is no consensus on the
histopathological findings [26]. It is particularly difficult to distinguish morphologically TAO
from ateriosclerosis obliterans (ASO). Histopatological findings are also known to vary
according to the duration of the disease [3]. The findings are most likely to be diagnostic in
the acute phase of the disease, most commonly at biopsy of a segment of a vessel with
superficial thrombophlebitis [10]. Other histopathological phases, such as intermediate
(subacute) and end-state (chronic) phases, have been described.
The acute-phase lesions include an occlusive, highly cellular, inflammatory thrombus with
less inflammation in the walls of the blood vessels. Polymorphonuclear leukocytes,
microabscesses and multinucleated giant cells may exist. When TAO occurs in unusual
locations, the diagnosis should be made only when histopathological examination identifies the
acute-phase lesion.
In the intermediate phase of disease there is progressive organization of the thrombus in
the arteries and veins.
When only organized thrombus and fibrosis are found in the blood vessels, the phase is
considered to be end-stage [27-29].

Management including treatment


The most effective treatment for Buerger's disease is smoking cessation. It is therefore
essential that patients diagnosed with Buerger's disease stop smoking immediately and
completely in order to prevent progression of the disease and avoid amputation [3,30]. Early
treatment is also important, because Buerger's disease may provoke social problems that
influence quality of life [31]. Even smoking one or two cigarettes per day or using smokeless
tobacco (chewing tobacco or using nicotine-containing patches) may keep the disease active
[32,33]. If there is no gangrene when the patient discontinues smoking, amputation is
avoided. Patients who continue smoking are at risk of amputation of fingers and toes.
Physicians must educate and counsel their patients repeatedly about the importance of
discontinuing the use of all tobacco products.
Despite the very strong correlation between smoking cessation and the decline of clinical
manifestations of TAO, patients may continue to have claudication or Raynaud's phenomenon
after complete cessation of tobacco usage [3].
Supportive care should be directed towards maximizing blood supply to the affected limbs.
Care should be taken to avoid thermal, chemical or mechanical injury, especially from poorly
fitting footwear or minor surgery of digits, as well as fungal infection. Vasoconstriction
provoked by cold-exposure or drugs should be avoided.
Despite the clear role of inflammation in the pathogenesis of TAO, anti-inflammatory agents,
such as steroids, have not been shown to be of real benefit. The results of intravenous therapy
with Iloprost (a prostaglandin analogue) show that this drug is superior to aspirin in providing
total pain relief at rest and complete healing of all trophic changes. It diminishes the risk of
amputation [34]. Although acetylsalicylic acid (aspirin) is often prescribed to patients with

Buerger's disease, the benefit of this or other orally administered anti-clotting agents has not
been confirmed by controlled studies. Intra-arterial thrombolytic therapy with streptokinase
has been tested in some patients with gangrene or pregangrenous lesions of the toes or feet,
with some success in avoiding amputation [35].
For patients with TAO, arterial revascularization is usually not possible due to the diffuse
segmental involvement and distal nature of the disease [3]. The benefit of bypass surgery to
distal arteries also remains controversial because of the high incidence of graft failure [36].
However, if the patient has severe ischemia and there is a distal target vessel, bypass surgery
with the use of an autologous vein should be considered [37-39].
Sympathectomy may be performed to decrease arterial spasm in patients with Buerger's
disease. A lapraroscopic method for sympathectomy has also been used [40,41].
Sympathectomy has been shown to provide short-term pain relief and to promote ulcer
healing in some patients with Buerger's disease, but no long-term benefit has been confirmed
[40]. Spinal cord stimulator and vascular endothelial growth factor gene therapy have been
used experimentally in patients with Buerger's disease with promising results [42,43].

References
1. Buerger L: Thromboangiitis obliterans: a study of the vascular lesions leading
to presenile gangrene.
Am J Med Sci 1908, 136:567-580.
Return to text
2. Buerger L: The circulatory disturbance of the extremities: including gangrene,
vasomotor and trophic disorders. Philadelphia, Saunders; 1924.
Return to text
3. Olin JW, Young JR, Graor RA, Ruschhaupt WF, Bartholomew JR: The changing clinical
spectrum of thromboangiitis obliterans (Buerger's disease).
Circulation 1990, 82:IV3-8. PubMed Abstract
Return to text
4. Lie JT: Thromboangiitis obliterans (Buerger's disease) revisited.
Pathol Annu 1988, 23:257-291. PubMed Abstract
Return to text
5. Lie JT: The rise and fall and resurgence of thromboangiitis obliterans
(Buerger's disease).
Acta Pathol Jpn 1989, 39:153-158. PubMed Abstract
Return to text
6. Shionoya S: Buerger's disease (thromboangiitis obliterans). In Vascular Surgery.
4th edition. Edited by: Rutherford RB. Philadelphia: WB Saunders; 1994:235-245.
Return to text
7. Cachovan M: Epidemiologic und geographisches Verteilungsmuster der
Thromboangiitis obliterans. In Thromboangiitis obliterans Morbus WiniwarterBuerger. Edited by: Heidrich H. Stuttgart, Germany Georg Thieme; 1988:31-36.
Return to text
8. Matsushita M, Nishikimi N, Sakurai T, Nimura Y: Decrease in prevalence of
Buerger's disease in Japan.
Surgery 1998, 124:498-502. PubMed Abstract | Publisher Full Text

Return to text
9. Shionoya S, Ban I, Nakata Y, Matsubara J, Hirai M, Kawai S: Involvement of the iliac
artery in Buerger's disease (pathogenesis and arterial reconstruction).
J Cardiovasc Surg (Torino) 1978, 19:69-76. PubMed Abstract
Return to text
10. Olin JW: Thromboangiitis obliterans (Buerger's disease).
N Engl J Med 2000, 343:864-869. PubMed Abstract | Publisher Full Text
Return to text
11. Shionoya S: Buerger's disease (thromboangiitis obliterans). In Vascular
surgery. 3rd edition. Edited by: Rutherford RB. Philadelphia: W.B Saunders;
1989:207-217.
Return to text
12. Harten P, Muller-Huelsbeck S, Regensburger D, Loeffler H: Multiple organ
manifestations in thromboangiitis obliterans (Buerger's disease). A case
report.
Angiology 1996, 47:419-425. PubMed Abstract
Return to text
13. Donatelli F, Triggiani M, Nascimbene S, Basso C, Benussi S, Chierchia SL, Thiene G,
Grossi A: Thromboangiitis obliterans of coronary and internal thoracic
arteries in a young woman.
J Thorac Cardiovasc Surg 1997, 113:800-802. PubMed Abstract | Publisher Full Text
Return to text
14. Arkkila PE, Kahri A, Farkkila M: Intestinal type of thromboangiitis obliterans
(Buerger disease) preceding symptoms of severe peripheral arterial disease.
Scand J Gastroenterol 2001, 36:669-672. PubMed Abstract | Publisher Full Text
Return to text
15. Kurata A, Nonaka T, Arimura Y, Nunokawa M, Terado Y, Sudo K, Fujioka Y: Multiple
ulcers with perforation of the small intestine in Buerger's disease: a case
report.
Gastroenterology 2003, 125:911-916. PubMed Abstract | Publisher Full Text
Return to text
16. Shionoya S: Diagnostic criteria of Buerger's disease.
Int J Cardiol 1998, 1:243-245. Publisher Full Text
Return to text
17. Allen EV: Thromboangiitis obliterans: methds of diagnosis of chronic
occlusive arterial lesions distal to the wrist with illustrative cases.
Am J Med Sci 1929, 178:237-244.
Return to text
18. Olin JW, Lie JT: Thromboangiitis obliterans (Buerger's disease). In Vascular
medicine. 2nd edition. Edited by: Loscalzo J, Creager MA, Dzau VJ. Boston: Little
Brown; 1996:1033-1049.
Return to text
19. Olin JM, Lie JT: Thromboangiitis obliterans (Buerger's disease). In Current
management of hypertensive and vascular diseases. Edited by: Cooke JP, Frohlich ED.
St Louis: Mosby-Year Book; 1992:265-271.
Return to text
20. Adar R, Papa MZ, Halpern Z, Mozes M, Shoshan S, Sofer B, Zinger H, Dayan M,
Mozes E: Cellular sensitivity to collagen in thromboangiitis obliterans.

N Engl J Med 1983, 308:1113-1116. PubMed Abstract


Return to text
21. de Moerloose P, Jeannet M, Mirimanoff P, Bouvier CA: Evidence for an HLA-linked
resistance gene in Buerger's disease.
Tissue Antigens 1979, 14:169-173. PubMed Abstract
Return to text
22. Kobayashi M, Ito M, Nakagawa A, Nishikimi N, Nimura Y: Immunohistochemical
analysis of arterial wall cellular infiltration in Buerger's disease (endarteritis
obliterans).
J Vasc Surg 1999, 29:451-458. PubMed Abstract | Publisher Full Text
Return to text
23. Diehm C, Stammler F: Thromboangiitis obliterans (Buerger's disease).
N Engl J Med 2001, 344:230-231. PubMed Abstract | Publisher Full Text
Return to text
24. Adar R, Papa MZ, Schneiderman J: Thromboangiitis obliterans: an old disease in
need of a new look.
Int J Cardiol 2000, 75:167-170. PubMed Abstract | Publisher Full Text
Return to text
25. Makita S, Nakamura M, Murakami H, Komoda K, Kawazoe K, Hiramori K: Impaired
endothelium-dependent vasorelaxation in peripheral vasculature of patients
with thromboangiitis obliterans (Buerger's disease).
Circulation 1996, 94:211-215.
Return to text
26. Kurata A, Franke FE, Machinami R, Schulz A: Thromboangiitis obliterans: classic
and new morphological features.
Virchows Arch 2000, 436:59-67. PubMed Abstract | Publisher Full Text
Return to text
27. Leu HJ: Early inflammatory changes in thromboangiitis obliterans.
Pathol Microbiol (Basel) 1975, 43:151-156. PubMed Abstract
Return to text
28. Lie JT: Diagnostic histopathology of major systemic and pulmonary vasculitic
syndromes.
Rheum Dis Clin North Am 1990, 16:269-292. PubMed Abstract
Return to text
29. Shionoya S, Leu HJ, Lie JT: Buerger's disease (Thromboangiitis obliterans). In
Vascular pathology. Edited by: Stehbens WE, Lie JT. London: Chapman & Hall
Medical; 1995:657-678.
Return to text
30. Shionoya S: What is the Buerger's disease?
World J Surg 1983, 7:544-551. PubMed Abstract | Publisher Full Text
Return to text
31. Ohta T, Ishioashi H, Hosaka M, Sugimoto I: Clinical and social consequences of
Buerger disease.
J Vasc Surg 2004, 39:176-180. PubMed Abstract | Publisher Full Text
Return to text
32. Joyce JW: Buerger's disease (Thromboangiitis obliterans).
Rheum Dis Clin North Am 1990, 16:463-470. PubMed Abstract
Return to text

33. Lie JT: Thromboangiitis obliterans (Buerger's disease) and smokeless


tobacco.
Arthritis Rheum 1988, 31:812-813. PubMed Abstract
Return to text
34. Fiessinger JN, Shafer M: Trial of Iloprost versus Aspirin treatment for critical
limb ischaemia of thromboangiitis obliterans. The TAO Study.
Lancet 1990, 335:555-557. PubMed Abstract | Publisher Full Text
Return to text
35. Hussein EA, el Dorri A: Intra-arterial streptokinase as adjuvant therapy for
complicated Buerger's disease: early trials.
Int Surg 1993, 78:54-58. PubMed Abstract
Return to text
36. Sasajima T, Kubo Y, Inaba M, Goh K, Azuma N: Role of infrainguinal bypass in
Buerger's disease: an eighteen-year experience.
Eur J Vasc Endovasc Surg 1997, 13:186-192. PubMed Abstract | Publisher Full Text
Return to text
37. Inada K, Iwashima Y, Okada A, Matsumoto K: Nonatherosclerotic segmental
arterial occlusion of the extremity.
Arch Surg 1974, 108:663-667. PubMed Abstract
Return to text
38. Sayin A, Bozkurt AK, Tuzun H, Vural FS, Erdog G, Ozer M: Surgical treatment of
Buerger's disease: experience with 216 patients.
Cardiovasc Surg 1993, 1:377-380. PubMed Abstract
Return to text
39. Watarida S, Shiraishi S, Fujimura M, Hirano M, Nishi T, Imura M, Yamamoto I:
Laparoscopic lumbar sympathectomy for lower-limb disease.
Surg Endosc 2002, 16:500-503. PubMed Abstract | Publisher Full Text
Return to text
40. Chander J, Singh L, Lal P, Jain A, Lal P, Ramteke VK: Retroperitoneoscopic lumbar
sympathectomy for buerger's disease: a novel technique.
JSLS 2004, 8:291-296. PubMed Abstract
Return to text
41. Lau H, Cheng SW: Buerger's disease in Hong Kong: a review of 89 cases.
Aust N Z J Surg 1997, 67:264-269. PubMed Abstract
Return to text
42. Swigris JJ, Olin JW, Mekhail NA: Implantable spinal cord stimulator to treat the
ischemic manifestations of thromboangiitis obliterans (Buerger's disease).
J Vasc Surg 1999, 29:928-935. PubMed Abstract | Publisher Full Text
Return to text
43. Isner JM, Baumgartner I, Rauh G, Schainfeld R, Blair R, Manor O, Razvi S, Symes JF:
Treatment of thromboangiitis obliterans (Buerger's disease) by
intramuscular gene transfer of vascular endothelial growth factor:
preliminary clinical results.
J Vasc Surg 1998, 28:964-973. PubMed Abstract | Publisher Full Text