AJR 2004; 183:307-314
© American Roentgen Ray Society
Imaging of Hereditary Hemorrhagic Telangiectasia
Jeff Jaskolka1,
Louis Wu1,
Raymond P. Chan1 and
Marie E. Faughnan2
1 Department of Medical Imaging, Toronto HHT Centre, St. Michael's Hospital,
University of Toronto, 30 Bond St.,Toronto, ON M5B 1W8, Canada.
2 Department of Medicine, Toronto HHT Centre, St. Michael's Hospital, University
of Toronto, ON M5B 1W8, Canada.
Received September 22, 2003;
accepted after revision January 29, 2004.
Address correspondence to L. Wu.
Introduction
Hereditary hemorrhagic telangiectasia, or Osler-Weber-Rendu disease, was
first recognized in 1896. It is an autosomal dominant disorder with variable
penetrance characterized by epistaxis, mucocutaneous telangiectases, and
visceral arteriovenous malformations. The prevalence is estimated to be
approximately 1:10,000 [1],
with considerable regional variability. A definitive clinical diagnosis
requires the presence of at least three of the following symptoms: recurrent
spontaneous epistaxis, mucocutaneous telangiectases, visceral arteriovenous
malformations, or evidence of autosomal dominant inheritance
[2]. Hereditary hemorrhagic
telangiectasia is a multisystem disease with a variety of imaging
manifestations. Although epistaxis and mucocutaneous telangiectases are the
most common clinical manifestations of the disease, visceral arteriovenous
malformations lead to the most serious complications. The extent and
distribution of visceral arteriovenous malformations vary among and within
affected families, with the most commonly affected organs being the lung,
brain, liver, and gastrointestinal tract. The purpose of this article is to
provide a brief review of the organ systems that can be affected and the
relevant findings on diagnostic imaging.
Lung
The primary manifestations of hereditary hemorrhagic telangiectasia in the
lung are pulmonary arteriovenous malformations, although patients may also
have telangiectases [1,
3]. The prevalence is
20–50% of the population with hereditary hemorrhagic telangiectasia,
with 60% of patients having multiple lesions. Many patients are asymptomatic,
and, in fact, neurologic complications including stroke, transient ischemic
attack, and brain abscess are often the initial presentation of patients with
pulmonary arteriovenous malformations
[1]. When symptomatic, patients
most commonly present with dyspnea on exertion, but they may also develop
cyanosis, polycythemia, massive hemoptysis, or spontaneous hemothorax.
On chest radiographs, the classic appearance of a pulmonary arteriovenous
malformation consists of a well-defined nodule, representing the aneurysm,
associated with one or more tubular opacities contiguous with the pulmonary
hilum, representing the enlarged draining veins. Pulmonary arteriovenous
malformations are often multiple and have a predilection for affecting the
lower lobes. Chest radiographs are neither sensitive nor specific. Lesions may
be difficult to identify because they are commonly situated at the posterior
of the base of the lungs, where they may be obscured by overlying structures
(Figs. 1A,
1B and
1C).
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Fig. 1A. —46-year-old woman with hereditary hemorrhagic telangiectasia
and multiple pulmonary arteriovenous malformations. Posteroanterior chest
radiograph shows well-defined lingular nodule with adjacent tubular opacity
(arrowhead) representing aneurysm and draining vein of pulmonary
arteriovenous malformation.
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Fig. 1B. —46-year-old woman with hereditary hemorrhagic telangiectasia
and multiple pulmonary arteriovenous malformations. Lateral chest radiograph
shows well-defined lingular nodule with adjacent tubular opacity
(arrowhead) representing aneurysm and draining vein of pulmonary
arteriovenous malformation. Second pulmonary arteriovenous malformation
(arrow) is faintly seen at base of right lung.
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Fig. 1C. —46-year-old woman with hereditary hemorrhagic telangiectasia
and multiple pulmonary arteriovenous malformations. Right pulmonary angiogram
shows complex basal pulmonary arteriovenous malformations (arrows).
Note presence of three separate segmental feeding arteries.
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Findings on helical CT include a single or multiple pulmonary nodules with
enlarged feeding vessels, draining vessels, or both
[3] (Figs.
2A and
2B). Alternatively, the
appearance may be that of a serpiginous mass with vascular connections. Thin
collimation allows multiplanar reformations that may be helpful in
characterization of lesions. The diagnosis of hereditary hemorrhagic
telangiectasia does not require the administration of IV contrast material,
which theoretically poses a risk of paradoxical air embolism if air is
inadvertently injected through the IV line.
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Fig. 2A. —58-year-old woman with hereditary hemorrhagic telangiectasia
that caused decreased exercise tolerance and cyanosis. Unenhanced thoracic CT
scan shows pulmonary arteriovenous malformation (arrow) in right
lower lobe.
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Fig. 2B. —58-year-old woman with hereditary hemorrhagic telangiectasia
that caused decreased exercise tolerance and cyanosis. Unenhanced thoracic CT
scan obtained at lower level than A shows multiple bilateral pulmonary
arteriovenous malformations (arrows).
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The reference standard for imaging pulmonary arteriovenous malformations is
pulmonary angiography. The angioarchitecture may be described as simple
(Fig. 2C) or complex
(Fig. 1C). Simple pulmonary
arteriovenous malformations are fed by one or more branches of the same
segmental artery, whereas complex lesions are supplied by branches of at least
two different segmental arteries. It is estimated that 90% of pulmonary
arteriovenous malformations in the population with hereditary hemorrhagic
telangiectasia are simple, with the remaining 10% being complex
[2]. In rare cases, a pulmonary
arteriovenous malformation may have a systemic arterial supply and drainage
[2,
3]. Embolotherapy, the primary
treatment for pulmonary arteriovenous malformations, is generally indicated
for lesions with feeding arteries 3 mm in diameter or larger (Figs.
3A and
3B). Approximately 10% of
embolized pulmonary arteriovenous malformations reperfuse, and most of these
are easily treated with a repeated session of embolotherapy
[2] (Figs.
4A,
4B,
4C, and
4D).
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Fig. 2C. —58-year-old woman with hereditary hemorrhagic telangiectasia
that caused decreased exercise tolerance and cyanosis. Superselective right
pulmonary angiogram obtained using 5-French catheter shows pulmonary
arteriovenous malformation with simple angioarchitecture in right lower lobe.
Note presence of embolization coils (arrow) from prior treatment of
different arteriovenous malformation.
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Fig. 3A. —44-year-old woman with hereditary hemorrhagic telangiectasia
and lingular pulmonary arteriovenous malformation. Left pulmonary angiogram
shows large solitary lingular pulmonary arteriovenous malformation. Note
feeding artery (white arrowhead), aneurysm sac (arrow), and
draining vein (black arrowhead).
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Fig. 3B. —44-year-old woman with hereditary hemorrhagic telangiectasia
and lingular pulmonary arteriovenous malformation. Angiogram obtained after
coil embolization (arrowhead) shows absence of flow through pulmonary
arteriovenous malformation.
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Fig. 4A. —45-year-old man with hereditary hemorrhagic telangiectasia
and reperfused pulmonary arteriovenous malformation. Initial left pulmonary
angiogram shows large pulmonary arteriovenous malformation in lower lobe.
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Fig. 4B. —45-year-old man with hereditary hemorrhagic telangiectasia
and reperfused pulmonary arteriovenous malformation. Angiogram obtained
immediately after embolization shows coils occluding feeding vessel and no
further opacification of pulmonary arteriovenous malformation.
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Fig. 4C. —45-year-old man with hereditary hemorrhagic telangiectasia
and reperfused pulmonary arteriovenous malformation. Pulmonary angiogram
obtained 2 years after B shows subtle contrast opacification
(arrow) of aneurysm in previously treated pulmonary arteriovenous
malformation.
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Fig. 4D. —45-year-old man with hereditary hemorrhagic telangiectasia
and reperfused pulmonary arteriovenous malformation. Superselective angiogram
more clearly shows aneurysm and draining vein perfusion beyond previously
placed coils.
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A sensitive, noninvasive test—such as contrast-enhanced transthoracic
echocardiography— is recommended as a screening technique for pulmonary
arteriovenous malformations in patients with hereditary hemorrhagic
telangiectasia [4]. The delayed
appearance of microbubbles in the chambers of the left heart after IV
injection of agitated saline is suggestive of an intrapulmonary shunt (Figs.
5A and
5B). This technique does not
show the precise location or morphology of the pulmonary arteriovenous
malformations and therefore has limited use as a screening test. Helical CT is
probably also a sensitive method for detection of pulmonary arteriovenous
malformations [3], although its
operating characteristics have been less well studied than those of
echocardiography in this population.
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Fig. 5A. —58-year-old man with hereditary hemorrhagic telangiectasia
and remote history of stroke, spontaneous hemothorax, and positive findings on
contrast-enhanced echocardiogram for large pulmonary arteriovenous
malformation. Initial four-chamber echocardiogram obtained after contrast
injection of agitated saline shows normal finding of hyperechoic bubbles
(asterisk) in right atrium and ventricle.
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Fig. 5B. —58-year-old man with hereditary hemorrhagic telangiectasia
and remote history of stroke, spontaneous hemothorax, and positive findings on
contrast-enhanced echocardiogram for large pulmonary arteriovenous
malformation. Corresponding delayed echocardiogram shows bubbles resulting
from intrapulmonary shunt in left atrium and ventricle (LV).
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Brain
Various neurologic symptoms are common in patients with hereditary
hemorrhagic telangiectasia, including migraine, ischemia, intracranial
hemorrhage, and seizures. Approximately two thirds of these symptoms represent
complications of pulmonary arteriovenous malformations caused by bland or
septic emboli passing through the abnormal fistulous communications in the
lungs, resulting in stroke (Fig.
6), transient ischemic attack, and brain abscess
[5]
(Fig. 7).
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Fig. 6. —36-year-old previously healthy man with right cerebellar
infarct. Subsequent investigation confirmed presence of pulmonary
arteriovenous malformation. Unenhanced axial CT scan obtained 2 days after
onset of symptoms shows diffuse hypoattenuation of right cerebellar hemisphere
due to infarction. Note hydrocephalus due to compression of fourth
ventricle.
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Fig. 7. —30-year-old man with hereditary hemorrhagic telangiectasia
and pulmonary arteriovenous malformation complicated by cerebral abscess.
Enhanced axial CT scan shows ring-enhancing abscess in left frontal lobe with
vasogenic edema and mild subfalcine herniation.
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Approximately one third of neurologic symptoms, including seizure and
intracranial hemorrhage, are directly related to brain or spinal vascular
malformations. Because cerebral arteriovenous malformations are present in
5–23% of patients, routine screening and treatment of these lesions is
recommended [6]. On MRI,
cerebral arteriovenous malformations appear as areas of serpiginous flow voids
insinuating into the brain parenchyma
(Fig. 8A). Patients often have
multiple malformations of varying types, many of which have an atypical or
indeterminate MRI appearance. Cerebral angiography may be required for
diagnosis of equivocal lesions and for treatment planning
(Fig. 8B). Therapy for
symptomatic cerebral arteriovenous malformations is surgical resection,
stereotactic radiosurgery, embolization, or a combination of these
treatments.
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Fig. 8A. —25-year-old man with hereditary hemorrhagic telangiectasia
and large cerebral arteriovenous malformation. Axial fast spin-echo
T2-weighted image shows cerebral arteriovenous malformation (arrow)
with heterogeneous signal intensity in left frontoparietal region. Note
prominent tubular flow void (arrowhead) anterior to malformation
corresponding to draining vein.
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Fig. 8B. —25-year-old man with hereditary hemorrhagic telangiectasia
and large cerebral arteriovenous malformation. Lateral projection of left
internal carotid angiogram shows large aneurysm sac (white arrow)
with enlarged, tortuous feeding arteries (white arrowheads) and
shunting into dilated cortical veins (black arrowheads) and superior
sagittal sinus (black arrow).
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Spinal arteriovenous malformations are much rarer than cerebral
arteriovenous malformations and may appear as serpiginous flow voids on
spin-echo MRI (Fig. 9A).
Angiography shows enlarged feeding vessels with early shunting into a dilated
venous system (Fig. 9B).
Treatment consists of surgery, embolization, or a combination of the two.
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Fig. 9A. —9-year-old boy presenting with subarachnoid hemorrhage
secondary to spinal arteriovenous malformation. Hereditary hemorrhagic
telangiectasia was subsequently diagnosed. Sagittal spin-echo T1-weighted
image shows numerous serpiginous flow voids (arrow) posterior to
spinal cord.
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Fig. 9B. —9-year-old boy presenting with subarachnoid hemorrhage
secondary to spinal arteriovenous malformation. Hereditary hemorrhagic
telangiectasia was subsequently diagnosed. Anterior intercostal angiogram
obtained at level of T10 vertebra confirms presence of spinal arteriovenous
malformation (arrow) draining into dilated, tortuous medullary veins
seen on MR image (A).
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Liver
The prevalence of liver involvement in hereditary hemorrhagic
telangiectasia ranges from 8–30%, with more than half the patients being
asymptomatic. Three clinical presentations of hepatic involvement have been
described: high-output heart failure, portal hypertension, and biliary cystic
disease. Symptoms primarily arise from shunts from the hepatic artery to the
hepatic veins, portal veins, or both. Abnormal blood supply and focal areas of
ischemia may cause irregularities of the bile ducts in addition to atypical
cirrhosis [7]. Resulting signs
of portal hypertension can be seen on sonography, CT, and MRI.
Cross-sectional imaging with contrast-enhanced CT or MRI commonly reveals a
dilated and tortuous hepatic artery with diffuse parenchymal telangiectases.
Dynamic studies may also show early enhancement of enlarged portal or hepatic
veins. Discrete hepatic arteriovenous malformations are rare.
Doppler sonographic findings include abnormal echogenicity of the liver
parenchyma with dilation of the hepatic arteries (> 6 mm), celiac axis,
portal veins, or hepatic veins. Elevated and turbulent celiac and hepatic
arterial flows are common. Rarely, abnormal arteriovenous anastomoses may be
shown (Figs. 10A,
10B, and
10C). Findings on Doppler
sonography can be abnormal before frank hepatic vascular malformations are
visualized [8].
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Fig. 10A. —61-year-old man with hereditary hemorrhagic
telangiectasia–related liver disease. Sonogram obtained through right
lobe of liver shows markedly enlarged and tortuous hepatic artery
(arrow).
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Fig. 10B. —61-year-old man with hereditary hemorrhagic
telangiectasia–related liver disease. Pulsed Doppler sonogram shows
increased velocity and flow volume in hepatic artery. Spectral analysis shows
aberrant waveform consistent with decreased peripheral resistance.
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On hepatic angiography, diffuse telangiectases are the most common finding
along with arteriovenous or arterioportal shunting. Dilated and tortuous
hepatic and celiac arteries are commonly seen. Rarely, discrete hepatic
arteriovenous malformations may be visualized.
Gastrointestinal Tract
Recurrent upper or lower gastrointestinal bleeding occurs in approximately
20% of patients with hereditary hemorrhagic telangiectasia, predominantly
after age 50, and can be difficult to manage. Patients typically have
telangiectases but may also have small arteriovenous malformations or
angiodysplasias of the stomach, duodenum, small bowel, or colon. Small
malformations can be impossible to visualize using any imaging technique.
Large arteriovenous malformations, however, may be diagnosed on conventional
CT [1] or CT angiography (Figs.
11A,
11B and
12A,
12B,
12C,
12D,).
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Fig. 11A. —68-year-old man with hereditary hemorrhagic telangiectasia
and duodenal arteriovenous malformation. Early image from superior mesenteric
angiography shows dilated, tortuous pancreaticoduodenal arteries
(arrow) supplying duodenal arteriovenous malformation.
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Fig. 11B. —68-year-old man with hereditary hemorrhagic telangiectasia
and duodenal arteriovenous malformation. Later image from same examination as
A shows dilated, tortuous pancreaticoduodenal arteries (arrow)
supplying duodenal arteriovenous malformation. Note early filling of vein
(arrowhead) resulting from arteriovenous shunting.
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Fig. 12A. —68-year-old woman with hereditary hemorrhagic telangiectasia
and anemia related to gastrointestinal involvement. Contrast-enhanced CT scan
obtained at level of pancreas shows multiple ill-defined, hyperattenuating
foci (arrows) within pancreatic parenchyma.
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Fig. 12B. —68-year-old woman with hereditary hemorrhagic telangiectasia
and anemia related to gastrointestinal involvement. Splenic angiogram confirms
presence of multiple pancreatic arteriovenous malformations
(arrows).
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Fig. 12C. —68-year-old woman with hereditary hemorrhagic telangiectasia
and anemia related to gastrointestinal involvement. Inferior mesenteric
angiogram shows colonic arteriovenous malformation (arrow) arising
from branch of sigmoid artery.
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Fig. 12D. —68-year-old woman with hereditary hemorrhagic telangiectasia
and anemia related to gastrointestinal involvement. Superior mesenteric
angiogram shows arteriovenous malformations at hepatic flexure supplied by
branch of right colic artery.
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Conclusion
Hereditary hemorrhagic telangiectasia is a multiorgan vascular dysplasia
that primarily affects the dermatologic, respiratory, central nervous, and
gastrointestinal systems, although virtually every body system can be
affected. Although rare, the disease is being recognized with increasing
frequency, and therefore radiologists should be familiar with the wide
spectrum of associated imaging findings.
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Introduction
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