Computed Tomography Angiography in Chronic Pulmonary

Thromboembolism

Review Article

INTRODUCTION

Clinical symptoms in patients with chronic pulmonarythromboembolism are nonspecific and are related to thedevelopment of pulmonary hypertension. Symptomsworsen as the right ventricular functional capacitydeteriorates. Chronic thromboembolic pulmonaryhypertension often is identified during the diagnosticwork-up in patients with unexplained pulmonaryhypertension, and radiologists must be aware of itsradiologic manifestations because it is a treatable cause ofpulmonary hypertension in some patients.

Clinical Manifestations

Symptoms are nonspecific and are related to thedevelopment of pulmonary hypertension. The extent ofvascular obstruction is a major determinant of the severityof pulmonary hypertension. In the majority of symptomaticpatients, more than 40% of the pulmonary vascular bed isobstructed [1,2]. Patients with chronic thromboembolicpulmonary hypertension may be asymptomatic for severalyears before their presentation with symptoms such asrecurrent acute or progressive exertional dyspnoea,chronic non-productive cough, atypical chest pain,tachycardia, syncope, and cor pulmonale [1-4]. Theclinical deterioration parallels the loss of right ventricularfunctional capacity. In these patients, pulmonary arterial

COMPUTED TOMOGRAPHY ANGIOGRAPHY IN CHRONIC PULMONARYTHROMBOEMBOLISM

Neha Shah, Dipal Shah, Sandip Shah, Yogesh Gohil, Bhavesh Vasani and Awani Patel*Consultant Radiologist, Department of Radiodiagnosis, Apollo Hospitals International Limited, 1A, GIDC Bhat,

Gandhinagar, Ahemdabad 382 428, India.Correspondence to: Dr Neha Shah, Department of Radiodiagnosis, Apollo Hospitals International Limited,

1A, GIDC Bhat, Gandhinagar, Ahmedabad, Ahemdabad 382 428, India.e-mail:nehashah_29@yahoo.com

Chronic thromboembolic pulmonary hypertension is clearly more common than previously was thought, andmisdiagnosis is common because patients often present with nonspecific symptoms related to pulmonaryhypertension. Computed tomography (CT) is a useful alternative to conventional angiography not only fordiagnosing chronic pulmonary thromboembolism but also for determining which cases are treatable withsurgery and confirming technical success postoperatively. Early recognition of chronic pulmonarythromboembolism may help improve the outcome, since the condition is potentially curable with pulmonarythromboendarterectomy.

Key words: CT Angiography, Chronic pulmonary thromboembolism.

Abbreviations: CT – Computed Tomography, PE – Pulmonary Embolism.

pressure is elevated, right atrial pressures are high,cardiac output is reduced, and pulmonary capillary wedgepressures are normal [2,5].

Pathophysiology

Among the various causes of pulmonaryhypertension, chronic thromboembolic obstruction of thepulmonary arteries is important because this condition ispotentially curable by means of pulmonaryendarterectomy. Several mechanisms are postulated to beresponsible for the development of chronic pulmonaryhypertension, including the recurrence of acute embolicevents; the incomplete resolution of treated thrombi,leading to variable degrees of residual vascularobstruction; and the propagation of an in situ thrombusinto pulmonary branch vessels. The hemodynamic basisof pulmonary hypertension in patients with chronicpulmonary hypertension includes the occlusion of centraland/or peripheral pulmonary arteries by chronicthrombotic lesions, as well as the development of distalarteriolar vasculopathy in the nonobstructed areas, acondition that is caused by pulmonary hypertension itself.Clinically, the disease manifestation of chronicpulmonary hypertension is similar to that of primaryidiopathic pulmonary hypertension, a condition that isassociated with disappointing management despiteadvances in pharmacotherapy and transplantation [6].

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Pathogenesis or natural history of pulmonaryemboli

Haemodynamic failure and death occurs in 20–40% ofpatients within 1 hour of acute pulmonary emboli [7].Among survivors, the natural evolution, in most cases, isresorption of blood clots by local fibrinolysis withcomplete restoration of the pulmonary arterial bed. In 0.1–0.4% of cases, for reasons which are unknown, resorptiondoes not occur and the emboli evolve to an organised clotinside the pulmonary artery. Abnormalities in haemostasisor fibrinolysis, and recurrent emboli are possiblecontributors. The pulmonary arterial bed becomesoccluded resulting in right heart remodelling. Theoccurrence of dyspnoea after a symptom-free interval ofseveral years is not due to recurrent emboli, but to thedevelopment of local thrombosis. This phenomenon issecondary to the low blood flow upstream from theobstructed pulmonary artery or, more likely, to thedevelopment of an arteritis in the non-obstructedterritories, similar to those seen in primary pulmonaryhypertension. These pathophysiological events explainthe inevitable worsening of pulmonary hypertension withtime and the occasionally delayed or incompleteregression of pulmonary hypertension after pulmonaryendarterectomy [8].

Relationship between obstruction andpulmonary vascular resistance

The extent of vascular obstruction is a majordeterminant of the severity of pulmonary hypertension inpatients with chronic pulmonary thromboembolism. Inmost cases 40% of the pulmonary vascular bed isobstructed. Worsening of pulmonary hypertension mayinvolve recurrent thromboembolism or in situ thrombosis,and remodelling of small distal pulmonary arteries in thenon-occluded areas, similar to that encountered in primarypulmonary hypertension [8].

CT technique

Chronic pulmonary thromboembolism is oftenidentified during the diagnostic work-up in patients withunexplained pulmonary hypertension. Patients receive 70to 100 mL of contrast material at an injection rate of 4 mL/sec. The desired opacification of the pulmonary andsystemic circulation can be achieved by using a longerdelay from contrast material injection to imageacquisition; we use a trigger threshold, 120 HU with acircular region of interest centered on the main pulmonaryartery.

The scanning is performed in the caudal-cranialdirection because most pulmonary emboli are found in the

lower lung lobes and, if the patient is unable to sustainbreath holding throughout image acquisition, the lowerlobes are imaged in the initial seconds of the breath hold.Because some signs of chronic thromboembolism (e.g.,bands) may be overlooked with the high contrastmediastinal window settings, we view the images by usingdifferent gray scales for interpretation.

Multiplanar reformatted images and maximumintensity projection images that provide longitudinalviews of vessels may help clarify confusing orquestionable findings and may better depict obstructions,stenosis, and flattened peripheral thrombotic material thatotherwise might be overlooked.

CT features of chronic pulmonarythromboembolism

CT features of chronic pulmonary thromboembolismare classified as vascular signs or parenchymal signs. Thevascular signs include direct pulmonary artery signs(results of thrombus organization), signs due to pulmonaryhypertension (results of the sustained increase inpulmonary vascular resistance) and signs due to systemiccollateral supply (results of decreased pulmonary arteryflow). The parenchymal signs include scars, a mosaicperfusion pattern, focal ground glass opacities andbronchial dilatation [5].

Vascular Signs

Pulmonary Arterial Signs

Complete obstruction

On angiography, complete vessel cut-off due to

Fig 1. Axial contrast enhanced CT shows complete occlusionof left lower lobe of pulmonary artery in comparisonwith right lower lobe pulmonary artery which containsperipheral thrombosis.

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chronic embolism has a convex margin with respect to thecontrast material and has been described as a “pouch”defect [9]. This differs from the appearance of a completeobstruction caused by acute pulmonary embolism in that aconcavity can be seen within the contrast material due tothe trailing edge of thrombus. On CT, an additional findingis a decrease in the diameter of the vessel distal to thecomplete obstruction. This permanent reduction in vesseldiameter is due to contraction of thrombus in chronic PE[10]. The additional findings of an abrupt decrease in

vessel diameter and absence of contrast material in thevessel segment distal to the total obstruction are easier toidentify [11].

Non-obstructive filling defects

The organized thrombus of chronic PE can causeintimal irregularities, bands and webs, and abrupt vesselnarrowing; any of these can lead to a pulmonary arterystenosis.

(a)

(b) (c)Fig 2. (a) sagital contrast enhanaced CT shows eccentric chronic thrombus along anteriosuperior wall of main pulmonary trunk.

(b) coronal contrast enhanced CT shows eccentrically located thrombus with broad base forming obtuse angle withvessel wall in right lower lobe pulmonary artery. (c) axial contrast enhanced CT shows bilateral eccentric chronic thrombiproducing irregular contour of the intimal surface of the lower lobe pulmonary arteries on both sides.

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(a) (b)

(c) (d)

Fig 3 Contrast enhanced CT scan in axial, coronal and sagital images in different patient show a liner structure anchored tothe vessel wall in multiple segmental and subsegmental vessels suggestive of band.

Intimal irregularities

Intimal irregularities are broad-based, smoothmargined abnormalities that create obtuse angles with thevessel wall (Fig. 2). They may be unilateral or bilateral.Pulmonary artery intimal irregularities can also be due toplaques secondary to pulmonary hypertension [12].

Bands and Webs

A band is defined as a delicate ribbon like structureanchored to the vessel wall at two ends with a freeunattached mid portion. A band generally ranges from 0.3to 2 cm in length and from less than 0.1 to 0.3 cm in width.It is often orientated in the direction of blood flow alongthe long axis of the vessel. A web is a descriptive term forbands that have branches and form networks of varying

complexity. Bands and webs are seen as thin linessurrounded by contrast material on CT angiography [5](Fig 3).

Abrupt vessel narrowing

Abrupt vessel narrowing, often the result ofrecanalization, manifests angiographically as an abruptconvergence of contrast material that leads to a thincolumn of intravascular contrast material distally. Thisnonreversible finding can also be detected on CT images,which can be used to identify the cause of the stenosis[12].

Calcifications within chronic thrombi are seen in asmall number of patients (Fig 4). On contrast enhancedCT images with the usual mediastinal window settings,

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Fig 4. Coronal contrast enhanced CT scan shows partiallycalcified thrombus in left main pulmonary artery.

calcified thrombi may be obscured by surroundingcontrast material [5].

Signs of pulmonary hypertension

Enlargement of the main pulmonary artery

Increased vascular resistance due to the obstructedvascular bed leads to dilatation of the central pulmonaryarteries. Enlargement of the main pulmonary artery to adiameter of more than 29 mm may occur in the presence ofpulmonary hypertension, When the ratio of the diameter ofthe main pulmonary artery to the diameter of the aortameasured on CT scans is greater than 1:1, there is a strongcorrelation with elevated pulmonary artery pressure (Fig 5).

Fig 5. Axial contrast enhanced CT scan shows an enlargedpulmonary trunk with a maximum diameter of 37 mmnear its bifurcation and chronic peripherally situatedthrombus in right and left main pulmonary artery.

Right heart disease is a common. The increasedworkload borne by the right heart results in rightventricular enlargement and hypertrophy (right ventri-cular myocardial thickness greater than 4 mm). Over time,right ventricular function deteriorates, even in the absenceof recurrent embolism, presumably because of thedevelopment of hypertensive vascular lesions in thenonobstructed pulmonary artery bed and of vasculopathyin vessels distal to obstructed arteries. Dilatation of theright ventricle is considered present when the ratio of thediameter of the right ventricle to that of the left ventricle isgreater than 1:1 and there is bowing of the interventricularseptum toward the left ventricle ( Fig. 6a). At CT, thesesigns can be evaluated even without electrocardiographicgating. The minor axis of the right and left ventricularchambers can be measured in the axial plane at theirwidest points, in diastole, between the inner surface of thefree wall and the surface of the interventricular septum.The diastolic maxima of the right and left ventricles maybe reached at slightly different levels. Right ventricularenlargement may be accompanied by dilatation of thetricuspid valve annulus and resultant tricuspid valveregurgitation (Fig 6b). Patients with severe pulmonaryhypertension may present with mild pericardial thickeningor a small pericardial effusion. The presence of pericardialeffusion implies a worse prognosis. Patients with chronicthromboembolic pulmonary hypertension may haveenlarged lymph nodes.

Poststenotic dilatation

Poststenotic dilatation or aneurysm commonly occursas a manifestation of chronic thromboembolic disease.The differential diagnosis includes congenital causes—forexample, Marfan syndrome—or acquired causes.Acquired causes include mycotic aneurysms secondary toseptic emboli or adjacent pulmonary infection,pseudoaneurysms resulting from extra- or endovasculartrauma (e.g., pulmonary artery catheterization), Behçetdisease and Takayasu’s arteritis [12].

Tortuous vessels

Tortuous pulmonary vessels have been well describedin patients with pulmonary artery hypertension. Thisradiologic sign is also seen in patients with pulmonaryartery hypertension secondary to chronic thromboembolicdisease [12].

Enlargement of bronchial arteries

The lung is unusual because it is supplied by twodistinct vascular systems—the pulmonary and bronchialarteries. The main function of the pulmonary artery is gasexchange, whereas the bronchial artery provides nutrition

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1%–2% of the cardiac output. In patients with chronicthromboembolic pulmonary hypertension, bronchial flowmay represent almost 30% of the systemic blood flow.Systemic-to-pulmonary arterial anastomosis developsbeyond the level of obstruction to fill pulmonary arteriesdownstream. The bronchial arteries usually arise from thedescending aorta at the level of the carina. Abnormaldilatation of the proximal portion of the bronchial arteries(diameter of more than 2 mm) and arterial tortuosity areCT findings indicative of bronchial arteryhypervascularization (Fig 8). Abnormally enlargedbronchial and nonbronchial systemic arteries are foundmore frequently in patients with chronic thromboembolicpulmonary hypertension (73%) than in patients withidiopathic pulmonary hypertension (14%); these findingscould help distinguish between these two entities. Themost frequently depicted abnormal nonbronchial systemicarteries were the inferior phrenic (Fig 8), intercostal andinternal mammary arteries. Another important finding isthat dilated bronchial arteries are positively correlatedwith a lower mortality rate after pulmonarythromboendarterectomy. Development of systemichypervascularization may also be responsible forhemoptysis in these patients.

Nonuniform arterial perfusion

Chronic PE can cause a nonuniform arterial perfusionpattern identifiable on angiography and can manifest as amosaic pattern of lung attenuation on CT [13]. Thispattern appears as sharply demarcated regions ofdecreased and increased attenuation because of irregular

to the bronchial structures, pulmonary vessels,parenchyma, lymph nodes and pleura. Imaging of thepulmonary artery has been studied extensively; however,the bronchial artery has become the focus of recentrenewed interest. The bronchial arteries usually arise fromthe aorta and intercostal arteries and drain into the leftatrium via pulmonary veins and partly into the right atriumvia the azygos vein. These arteries have a maximumdiameter of 1.5 mm and are rarely seen on helical CT [13].

Bronchial arterial flow increases in response tochronic obstruction of the pulmonary arteries in patientswith chronic thromboembolic pulmonary hypertension.The normal bronchial arterial blood flow is of the order of

(a) (b)

Fig 6. (a) Axial contrast enhanced CT shows dilatation of right ventricle with a ratio of more than 1:1 between right and leftventricle diameters and leftward septal bowing. (b) Axial contrast enhanced CT scan at a lower level shows opacificationof the IVC and hepatic veins because of the retrograde flow of contrast material which is often seen in patient withelevated right atrial and right ventricular pressure.

Fig 7. Sagital reformatted CT shows organized thrombus as acause of intimal irregularity and tortuous vessels.

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(a) (b)

Fig 9. Axial and coronal lung window images show mosaic perfusion pattern with marked regional variation in attenuation oflung parenchyma and disparity in the size of the segmental vessels with larger diameter vessels in the region of increasedattenuation.

perfusion (Fig 9). Low attenuation is due either tohypoperfusion in areas distal to occluded vessels or todistal vasculopathy in nonoccluded areas, and increasedattenuation has been related to the redistribution of bloodflow to the patent arterial bed [5]. Mosaic perfusion isseen much more commonly in patients with chronicthromboembolic pulmonary hypertension than in patientswith idiopathic pulmonary hypertension and is alsocommonly seen in pulmonary hypertention due to vasculardisease than in those with pulmonary hypertension due tocardiac or lung disease.

In addition, on CT one can see that the affectedpulmonary arteries are permanently small relative to theaccompanying bronchi and that unaffected arteries areoften larger than their accompanying bronchi [13].

Parenchymal scar

Scars from prior pulmonary infarctions are commonlydepicted in areas of decreased lung attenuation on CTscans obtained in patients with chronic thromboembolicpulmonary hypertension. These scars may appear asparenchymal bands, wedge-shaped opacities, peripheral

Fig 8. Coronal thick MIP CT image show enlargement of bronchial and branch of right inferior phrenic artery.

(a) (b)

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nodules, cavities or irregular peripheral linear opacities(Fig 10). The appearance most suggestive of scar tissuefrom infarction is a wedge-shaped pleural based opacity;however, an infarct may constrict with age and take on themore linear shape of a parenchymal band. Parenchymalscars often occur in multiples, generally are found in thelower lobes and often are accompanied by pleuralthickening.

DIFFERENTIATION OF ACUTE AND CHRONICTHROMBOEMBOLISM

Chronic pulmonary thromboembolism often isdiscovered during CT pulmonary angiography performedto rule out acute pulmonary thromboembolism in a patientwho presents with dyspnea. Acute and chronic thrombo-embolism commonly coexist. In cases of acute completeobstruction, the diameter of the pulmonary artery may beincreased because of impaction of the thrombus bypulsatile flow. Conversely, in chronic thromboembolicdisease, the diameter of the vessel distal to a completeobstruction is markedly decreased. An acutenonobstructive filling defect may be central or eccentric inlocation. In acute thromboembolism, a nonobstructiveeccentric filling defect forms acute angles with the vesselwall. Conversely, partially obstructive chronicthromboembolism appears as a peripheral crescent-shaped defect that forms obtuse angles with the vesselwall. An acute nonobstructive central defect appearssurrounded by contrast-enhanced blood. If the distinctionbetween acute and chronic or recurrent pulmonarythromboembolism is unclear, the presence of dilatedbronchial arteries supports a diagnosis of recurrent orchronic pulmonary thromboembolism. The mean

attenuation in the presence of chronic thromboembolismis significantly higher than that in acutethromboembolism. The higher mean attenuation in thepresence of chronic pulmonary thromboembolism is likelyrelated to enhancement of the organizing thrombus,retraction of the thrombus with its concentrations ofhaemoglobin and iron, and, possibly, calcium deposition.Acute embolic obstruction of a significant amount of thepulmonary circulation (usually estimated as more than30%) increases pulmonary vascular resistance and leads toacute pulmonary hypertension and, in some cases, rightventricular dysfunction and dilatation. However, sincepulmonary hypertension is not firmly established in casesof acute obstruction, right ventricular hypertrophy has notyet developed.

CONCLUSION

Chronic thromboembolic pulmonary hypertension isclearly more common than previously was thought. Itoften has been misdiagnosed because patients presentwith nonspecific symptoms. Knowledge of the radiologicimaging signs is required to detect and accuratelydiagnose the condition. Because chronicthromboembolism is potentially curable with pulmonarythromboendarterec-tomy, early recognition may improvethe outcome in cases that are technically operable. Themain objective of cross-sectional imaging in patients withchronic thromboembolic pulmonary hypertension (afterconfirming the diagnosis and differentiating the diseasefrom other causes of pulmonary hypertension) is tocorrectly assess the technical feasibility of surgery. In thisregard, CT angiography represents the future for diagnosisand management of chronic thromboembolic pulmonary

(a) (b)Fig 10. Coronal MIP and axial images show peripheral linear opacity in left lower lobe, a feature that represents old infarct.

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hypertension. MDCT is a useful technique for predictionof surgical operability in cases of chronic thromboembolicpulmonary hypertension because it accurately depicts anendarterectomy plane. MDCT is used as an additional toolfor selection of patients who would most benefit fromthromboendarterectomy.

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