Clinical Radiology 67 (2012) 1207e1211

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Clinical Radiology
journal homepage: www.clinicalradiologyonline.net

Pictorial Review

Imaging appearances of Buerger’s disease complications

in the upper and lower limbs
S.J. Dimmick a, b, *, A.C. Goh a, E. Cauzza c, L.S. Steinbach d, I. Baumgartner e,
E. Stauffer f, E. Voegelin g, S.E. Anderson b, h
a
Department of Radiology, Royal North Shore Hospital, St Leonards New South Wales, Australia
b
Medical Imaging, The University of Notre Dame Australia, Sydney School of Medicine, Sydney, Australia
c
Department of Radiology, Ospedale San Giovanni, Bellinzona, Switzerland
d
Department of Radiology, University of California San Francisco, San Francisco, USA
e
Department of Angiology, Subsection Hand Surgery, University Hospital of Bern, Inselspital, Bern, Switzerland
f
Institute of Pathology, Frieburg, Switzerland
g
Department of Orthopedics, Subsection Hand Surgery, University Hospital of Bern, Inselspital, Bern, Switzerland
h
Department of Radiology, Subsection Hand Surgery, University Hospital of Bern, Inselspital, Bern, Switzerland

art icl e i nformat ion

Thromboangiitis obliterans (Buerger’s disease) is a rare, non-atherosclerotic, segmental,
Article history: inflammatory vasculitis that most commonly involves small and medium-sized arteries, veins
Received 21 December 2011 and nerves of the extremities and affects tobacco smokers between the ages of 25 and 45 years.
Received in revised form The manifestations of Buerger’s disease can be extremely variable and, therefore, awareness of
1 April 2012 the condition is important for both general and musculoskeletal radiologists. This paper
Accepted 11 April 2012 presents the radiological appearance of the sequelae of Buerger’s disease involving the upper
and lower limbs.
Ó 2012 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.

Introduction wall. It is postulated that the inflammatory process is driven

by abnormalities in imunoreactivity.2
Thromboangiitis obliterans or Buerger’s disease is a non-
Incidence
atherosclerotic, segmental, inflammatory vasculitis, which
was first described in 1879. Small and medium-sized
The prevalence of Buerger’s disease is higher in the
arteries, veins, and nerves of the extremities are most
Middle East, Mediterranean, and in Asia than in Western
commonly affected. Cerebral, coronary, renal, mesenteric,
Europe and North America. The reported incidence is 12.6
and pulmonary arteries are less frequently involved.1 The
per 100,000 patients in North America.2e4 Although the
disease process is characterized by a highly cellular
overall incidence has decreased in North America over
inflammatory thrombus with relative sparing of the vessel
the last 30 years, there has been an increase in women. This
been attributed to a decline in cigarette smoking in men and
an increase in the number of women who smoke.5
* Guarantor and correspondent: S.J. Dimmick, Department of Radiology, Aetiology/pathophysiology
Royal North Shore Hospital, St Leonards New South Wales 2076, Australia.
Tel.: þ61 2 99268505; fax: þ61 2 99266204.
E-mail addresses: sdimmick@nsccahs.health.nsw.gov.au, sdimmick@med. The pathophysiology of Buerger’s disease is not
usyd.edu.au (S.J. Dimmick). completely understood but is likely multifactorial involving

0009-9260/$ e see front matter Ó 2012 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.crad.2012.04.005
1208 S.J. Dimmick et al. / Clinical Radiology 67 (2012) 1207e1211
a combination of hereditary susceptibility, tobacco exposure,
immune, and coagulable responses.6 Exposure to tobacco is
central to the initiation, maintenance, and progression of the
disease.4 Although smoking tobacco is by far the most
common risk factor, thromboangiitis obliterans may also
develop as a result of chewing tobacco or marijuana use.7
Previous studies have demonstrated an elevation in the
amount of anti-endothelial antibodies and impairment in
endothelial-dependent vasodilatation in patients with
Buerger’s disease. Peripheral endothelium-dependent vaso-
dilation is impaired in both diseased and non-diseased
limbs. This supports the hypothesis that Buerger’s disease
may be an autoimmune disorder that is initiated by an
unknown antigen within the intima of the vessel wall.8,9
Nearly two-thirds of patients with Buerger’s disease have
severe periodontal disease, and chronic anaerobic peri-
odontal infection may represent an additional risk factor for
the development of the disease.4
Histopathology
Buerger’s disease involves three phases: acute, subacute,
and chronic. In the acute phase, occlusive thrombi are
deposited within the lumen of vessels, which are highly
cellular, containing polymorphonuclear neutrophils,
microabscesses, and multinucleated giant cells. Although
inflammation involves all layers of the vessel wall, the
normal architecture of the vessel wall is preserved.4 These
findings distinguish Buerger’s disease from atherosclerosis
and other systemic vasculitides.6
Occlusive thrombi undergo progressive organization
during the subacute phase.10
In the chronic phase, there is extensive recanalization of
vessels, increased vascularization of the media and adven-
titial and perivascular fibrosis. This chronic phase is indis-
tinguishable histologically from any other chronic vascular
disease.10
Clinical presentation
Patients usually present before the age of 45 years. The
most common presenting symptoms include intermittent
claudication, superficial thrombophlebitis, paraesthesias,
rest pain, necrosis, ulceration or Raynaud phenomenon.4
The lower extremities are involved in 100% of cases and
the upper extremities in 44%.6 The disease rarely affects the
vessels proximal to the popliteal and brachial arteries but
involves multiple vessels more distally. Involvement of both
the upper and lower extremities and the size and location of
affected vessels help distinguish Buerger’s disease from
atherosclerosis.4
Superficial thrombophlebitis may predate the onset of
ischaemic symptoms caused by arterial occlusive disease
and frequently parallels disease activity. Patients may
describe a migratory pattern of tender nodules that follow
a venous distribution in both the arms and legs.4 Migrating
phlebitis (phlebitis saltans) in young patients is, therefore,
highly suggestive of Buerger’s disease. Deep venous
thrombosis is unusual.
Periods of exacerbation and remission is a characteristic
feature. The disease intensifies usually at the age of 30e40
years and then symptoms diminish. In persons at the age of
60 years or more recurrence is almost never observed.11
Recurrent episodes of large joint arthritis and transient,
migratory single joint episodes accompanied by local signs
of inflammation have also been described.12 When present,
joint symptoms usually precede the onset of digital
ischaemia. In this way, Buerger’s disease may resemble
other forms of vasculitis, which are often heralded by
musculoskeletal complaints. The arthritis disappears
definitively with the appearance of ischaemic signs.13
Diagnostic criteria
There are currently no accepted clinical criteria for the
diagnosis of Buerger’s disease, however, multiple have been
published 1,14e16; the most commonly accepted is by Shio-
noya.15 All five criteria must be fulfilled to diagnose
Buerger’s disease. These include: (1) smoking history; (2)
onset before the age of 50 years; (3) infrapopliteal arterial
occlusive disease; (4) either upper limb involvement or
phlebitis migrans; and (5) absence of atherosclerotic risk
factors other than smoking. Although not a definitive
criteria, two or more limbs should be involved.
Laboratory studies
There are no specific laboratory tests to aid in the diag-
nosis of Buerger’s disease; however, a complete serological
profile should be undertaken to exclude other vasculitides
that may mimic this disease.7,10 Serum acute phase reac-
tants (e.g., C-reactive protein) are elevated in other forms of
vasculitis, but are not elevated in Buerger’s disease. A drug
screen to exclude the ingestion of illicit drugs, such as
cocaine, amphetamines, and cannabis, may also be neces-
sary. These drugs may cause a vasculitis, which may mimic
Buerger’s disease angiographically.17,18
Imaging findings
Angiography
The gold standard for diagnosis is digital subtraction
angiography, although there are no pathognomonic angio-
graphic findings. The disease is confined most often to the
distal circulation and is almost always infrapopliteal in
the lower extremities and distal to the brachial artery in the
upper extremities. The more proximal arteries should be
normal in appearance (Fig 1).
Angiography demonstrates segmental areas of diseased
vessels interspersed with normal blood vessel segments.8
Multiple vascular occlusions, skip and segmental lesions
may be visualized with collateralization around the
obstructions (corkscrew, “tree root” or “spider’s leg” collat-
erals: Martonell’s sign). These vessels represent pathologi-
cally widened vasa vasorum.6
 S.J. Dimmick et al. / Clinical Radiology 67 (2012) 1207e1211 1209

Figure 1 (a) A 27-year-old man presented for angiographic investigation of progressive changes within the hands, greatest on the right, to assess
for a vascular cause. Observation of the right hand shows protrusion of the distal phalanges though the nail bed of the second to fourth digits.
The fingers are oedematous and erythematous due to ischaemia. There is necrosis of the nail bed of the third digit. (b) Digital subtraction
angiography image (anteroposterior projection) of the right forearm shows normal proximal arteries. Within the mid forearm, the radial (thick
arrow) and ulnar (thin arrow) arteries terminate, with multiple “corkscrew” collaterals visualized in the distal forearm and hand. These findings
are evident in Buerger’s disease. (c) Angiographic image (anteroposterior projection) of the distal forearm, wrist, and hand, which demonstrates
“corkscrew” collaterals with minimal filling of the digital arteries.

Unfortunately, corkscrew collaterals are not pathogno- Osteomyelitis

monic of Buerger’s disease as they may be seen in diseases
such as systemic lupus erythromatosis, mixed connective Osteomyelitis and/or septic arthritis are a potentially
tissue disease, scleroderma, CREST (calcinosis, Raynaud’s devastating complication of Buerger’s disease (Fig 3).
syndrome, oesophageal dysmotility, sclerodactyly and Although osteomyelitis may be found in a multitude of
telangiectasia) syndrome or any other small vessel occlusive other disease processes, Buerger’s disease may cause a dry
disease or in patients with cocaine, amphetamine, or gangrene, which should be considered as a differential
cannabis ingestion.8 diagnosis in middle-aged smokers.
Computed tomography (CT) and magnetic resonance MRI features of infection may be subtle in Buerger’s
angiography (MRA) currently do not play a direct role in the disease with dry gangrene, given poor perfusion and hence
diagnosis of Buerger’s disease.19 Some authors believe that
both modalities lack the spatial resolution necessary to
detect small-artery pathology.2 Limited coverage of
40e50 cm is also currently a shortfall of MRA.20 A number
of recently published studies, however, demonstrate the
potential diagnostic value of both unenhanced and
contrast-enhanced MRA in peripheral vasculitides.20e23
When utilized, CT and MRA may identify segmental
stenoses/occlusions, collateral vessels adjacent to sites of
occlusion, a proximal source of embolic disease or may
assist in excluding other vasculitides.19,20

Acro-osteolysis

Acro-osteolysis and cortical bone resorption is

a common finding on plain film studies in Buerger’s
disease (Fig 2) and is secondary to ischaemia/occlusion of
supplying arteries. MRI may be undertaken to exclude
osteomyelitis as a cause of cortical bone resorption. The
findings of acro-osteolysis on MRI include bone resorption
Figure 2 A 33-year-old man underwent radiographs of the toes to
and underlying bone oedema on proton density or T2- exclude osteomyelitis on a background a non-healing ulcer on the
weighted sequences with fat saturation. Lack of enhance- plantar aspect of the second digit. The radiograph demonstrates acro-
ment on contrast-enhanced sequences and lack of soft osteolysis of the terminal tuft of the second toe. Osteomyelitis could
tissue or bony abscess or phlegmon excludes a diagnosis of not be excluded on this plain film. Unfortunately, the patient did not
osteomyelitis. have CT or MRI imaging.
1210 S.J. Dimmick et al. / Clinical Radiology 67 (2012) 1207e1211

Figure 3 (a) 41 year old male, status post debridement/resection of soft tissue of the distal aspect of the first digit. MR sagittal T1-weighted
image of the first digit demonstrates bone erosion of the tuft of the distal phalanx and subtle altered marrow signal intensity. (b) Sagittal
T2-weighted fat saturated image demonstrates loss of cortical bone of the tuft of the distal phalanx and altered marrow signal within the
adjacent medullary bone. High signal intensity was also noted within the adjacent soft tissues without evidence of abscess formation. (c) Sagittal
T1-weighted fat saturated post contrast image demonstrates enhancement within the distal phalanx consistent with osteomyelitis. Histology
confirmed the imaging findings. The minimal signal change and enhancement within the bone and soft tissues is due to the relative lack of
inflammatory response as a consequence of poor vascular perfusion.

Figure 4 MRI of a 45 year old female who had a five pack a day smoking history for investigation of a forearm mass. T1-weighted, fat-suppressed,
post-gadolinium contrast-enhanced images, (a) coronal, (b) sagittal, and (c) transverse images do not demonstrate a discrete mass; however,
revealed an area of enhancement within the soft tissues of the ulnar aspect of the volar forearm within and adjacent to the thrombosed ulnar artery
(best seen on image c). Image c also shows central intra-arterial and adjacent soft-tissue enhancement associated with ulnar artery thrombosis. The
histopathology demonstrated the characteristic features of Buerger’s disease on histopathology performed after the MRI.

decreased inflammatory response compared to what is
usually associated with osteomyelitis.
Pseudotumour
In a single case identified by the authors, a patient who was
subsequently diagnosed with Buerger’s disease presented
with a palpable mass involving the forearm. At imaging, the
site of the palpable lump corresponded to a “pseudotumour”
secondary to an occlusion of the ulnar artery (Fig 4). The
pseudotumour presumably represents inflammatory change
adjacent to the site of vascular occlusion. This presumably has
the potential to occur with any disease capable of causing
a vascular occlusion and, therefore, may not be pathognomonic
to Buerger’s disease. On review of the literature, the radiolog-
ical findings of this entity have not been previously described.
When an inflammatory mass or “pseudotumour” is
identified, it is important to assess flow voids within the
adjacent vessels to assess for occlusion or slow flow. When
a vascular occlusion is identified on imaging, Buerger’s
disease should be a differential diagnosis.
Conclusion
Buerger’s disease is a rare, but important cause of
vasculitis in middle-aged smokers. Radiologists should be
aware of the imaging findings of this disease and its
complications in the peripheries to ensure prompt diag-
nosis and treatment.
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