Endovascular management of pulmonary arteriovenous malformations presenting as multiple brain abscesses

Abstract

Pulmonary arteriovenous malformations (PAVMs) are rare vascular lesions characterised by abnormal connections between the pulmonary artery and vein bypassing the pulmonary capillary bed and causing right-to-left shunt. Paradoxical embolism is known to occur in these cases, leading to inoculation of septic focus in the systemic circulation. We report a case of multiple PAVMs who presented clinically with seizures and altered sensorium. On radiological work-up, multiple brain abscesses and large PAVMs were evident. The patient was successfully treated by endovascular embolisation of the PAVMs using a vascular plug and multiple coils. The patient showed complete clinical recovery and resolution of brain abscesses on follow-up.

Background

Pulmonary arteriovenous malformations (PAVMs) are rare lesions with significant clinical complications. Although most of the patients are asymptomatic, the right-to-left shunt produced by PAVM may result in easy access of septic or non-septic emboli to systemic circulation causing serious central nervous system (CNS) complications.^1–3 The CNS complications associated with PAVMs are neurological events, including transient ischaemic attacks, recurrent strokes, brain abscesses and seizures.^{1 4 5} It is recommended searching for PAVM in patients with cryptogenic brain abscesses. More than 90% of PAVMs are associated with hereditary haemorrhagic telangiectasia (HHT), also known as Osler-Weber-Rendu syndrome. The clinical interventional radiologist is well suited to assume an increasing role in identifying, evaluating and managing patients with PAVMs and HHT.^{2 4} Here, we present a case of multiple PAVMs, who presented with multiple brain abscesses. We also report the experience of using Amplatzer vascular plugs and coils in the management of the PAVMs.

Case presentation

A man in his 30s presented with headache, diplopia and three episodes of generalised tonic–clonic seizure in the previous month. He had altered sensorium for the last 10 days. He had a history of occasional episodes of syncope, episodic headache and breathing difficulty, mainly in an upright position. There was a history of left-sided hemiparesis and drooping of the right eyelid 12 years ago. Then he was diagnosed with polycythaemia at a peripheral health centre and underwent phlebotomy multiple times. No further work-up could be done at that time as the patient did not return for further evaluation after recovery and was loss to follow-up. The patient was a non-smoker; however, he consumed alcohol occasionally.

On general examination, there was the presence of cyanosis and finger clubbing. The patient was normotensive, chest sounds were vesicular and there was no evidence of murmurs on cardiac auscultation. The patient was disoriented and his Glasgow Coma Scale score was 13/15 (E4M5V4). Neck rigidity and Kernig’s sign were absent. He had mild ptosis with slightly decreased visual acuity on the right side (right eye=6/18, left eye=6/12) and mild papilloedema bilaterally on fundus examination. The deep tendon reflexes were exaggerated (++) with extensor plantar reflexes bilaterally.

Investigations

The blood work-up showed raised haemoglobin (Hb) and haematocrit (HCT) (Hb=19.3, HCT=62.4) and decreased oxygen saturation (SpO₂) on room air (SpO₂=88%). The patient was sent for a radiological work-up. MRI of the brain showed multiple hyperintense lesions in bilateral cerebral hemispheres with significant perilesional oedema on T2-weighted images. The peripheral wall of the lesions was T2 hypointense. Diffusion-weighted images showed a significant restriction in the central part of the lesions. On post-contrast T1-weighted images, the lesions were showing peripheral rim enhancement (figure 1). These findings were suggestive of multiple brain abscesses. Chest roentgenogram (X-ray) showed a well-defined smooth outlined radio-opacity in the left mid-zone. Further work-up with CT angiography was done to characterise the lung lesion. CT angiography showed a large PAVM on the left side supplied by the upper lobar segmental branch of the left pulmonary artery and draining into the left upper pulmonary vein. The nidus of the PAVM was aneurysmally dilated. Another small-sized PAVM with an aneurysmally dilated nidus was seen in the right lower lobe supplied by a subsegmental branch of the right lower lobe pulmonary artery and draining into the respective pulmonary vein (figure 2). Ultrasonography of the abdomen was normal and no evidence of altered echotexture/AVMs was noted in abdominal visceral organs. The blood culture did not show any microbial growth. Transthoracic echocardiography did not reveal any cardiac vegetation. Based on the clinical features, blood investigations and radiological work-up, a diagnosis of PAVMs with secondary polycythaemia and multiple brain abscesses was made.

Figure 1.

Axial sections MRI: T2WI (A) shows multiple hyperintense lesions with hypointense rim and significant perilesional oedema; DWI (B) shows significant central diffusion restriction within the lesions; T1WI (C) non-contrast and (D) post-contrast images show peripheral rim enhancement of the lesions. DWI, diffusion-weighted image; T1WI, T1-weighted image; T2WI, T2-weighted image.

Figure 2.

(A) Chest X-ray posteroanterior view shows a well-defined radio-opacity with a smooth lobulated margin in the left mid-zone (arrow). CT angiography (CTA) maximum intensity projection (MIP) image in (B) coronal oblique plane shows a large pulmonary arteriovenous malformation (PAVM) on the left side supplied by a segmental branch of the left pulmonary artery. CTA MIP image in (C) coronal oblique plane shows another PAVM in right lower lobe supplied by a subsegmental branch of the pulmonary artery and draining into the right lower pulmonary vein. Volume-rendered CTA image (D) shows the PAVMs fed by the pulmonary artery and draining into the pulmonary vein.

Treatment

The patient was started on broad-spectrum intravenous antibiotics (ceftriaxone, metronidazole and vancomycin), antiepileptic drugs and a short course of steroids. Since there was evidence of perilesional oedema and mass effect on MRI scans, surgical exploration was also kept as a standby option should the conservative measures fail. On medical therapy, the patient showed significant clinical improvement and then he was referred to the interventional radiology department for endovascular embolisation of PAVMs.

Procedure: under general anaesthesia, right femoral vein access was obtained with an 8 F vascular sheath. Then a 6 F guide catheter was advanced over 0.035” hydrophilic guidewire to the left main pulmonary artery. Digital subtraction angiography (DSA) showed a large aneurysmally dilated PAVM in the left lung supplied by a dilated upper lobar segmental branch of the left pulmonary artery with rapid shunting of contrast into the superior pulmonary vein. Then the guide catheter was further advanced into the feeding pulmonary artery close to the aneurysmally dilated nidus. Then, an Amplatzer vascular plug (Abbott cardiovascular, USA) was deployed into the supplying artery. Post-vascular plug deployment DSA showed occlusion of the major feeding artery; however, the PAVM was still filling by another small calibre branch of the pulmonary artery. This feeder was then super-selectively cannulated using a microcatheter and embolised with multiple coils. The following DSA showed complete embolisation of the large PAVM. Then, the guide catheter was replaced into the right pulmonary artery, and using a 5 F diagnostic catheter, the lower lobe segmental branch of the right pulmonary artery was selectively cannulated. Then, the subsegmental branch, supplying the lower lobe PAVM, was super-selectively cannulated with a microcatheter and multiple coils were placed into the aneurysmally dilated nidus and the supplying feeder close to the nidus. Post-procedure DSA showed complete embolisation of the PAVMs (figure 3).

Figure 3.

Anteroposterior projection DSA images: (A) angiogram taken through 6 F guide catheter placed in left upper lobar pulmonary artery shows aneurysmally dilated large PAVM; (B) angiogram after vascular plug deployment and occlusion of the major feeder shows another small branch supplying the PAVM; (C) selective cannulation of the smaller feeder with a microcatheter for coil embolisation; (D) post-embolisation angiogram of the left upper lobar pulmonary artery shows non-filling of the left lung PAVM; (E) selective cannulation of the right lower lobe segmental pulmonary artery with a 5 F diagnostic catheter; (F) super-selective cannulation of the subsegmental branch of the right lower lobe pulmonary artery with microcatheter and tip of microcatheter in the aneurysmally dilated PAVM for coil embolisation; (G) post-coiling angiogram of the right pulmonary artery shows non-filling of the right lower lobe PAVM; (H) angiogram taken from the main pulmonary artery trunk shows complete embolisation of all the feeders to the PAVMs. DSA, digital subtraction angiography; PAVM, pulmonary arteriovenous malformation.

Outcome and follow-up

The patient was extubated and post-procedure recovery was uneventful. The clinical condition improved further with medical therapy. The fever and headache subsided and there was no subsequent seizure episode. The patient was discharged after 10 days on oral antibiotics, antiepileptics and antiplatelets, and asked to come for a follow-up in the outpatient department. At the 6-month follow-up, chest X-ray showed the vascular plug and coils in place with a significant reduction in the left mid-zone radio-opacity size. Contrast MRI showed complete resolution of all the brain abscesses except one in the right frontal lobe, which also showed a significant decrease in size and perilesional oedema (figure 4).

Figure 4.

Follow-up imaging after 6 months: (A) chest X-ray PA view shows vascular plug and coils in left mid-zone and right lower zone. Left mid-zone radio-opacity has significantly decreased in size. Axial MRI: (B) T2WI, (C) DWI, (D) pre-contrast T1WI and (E) post-contrast T1WI show resolution of all except right frontal lobe brain abscess, which also has reduced significantly in size with decreased perilesional oedema. DWI, diffusion-weighted image; PA, posteroanterior; T1WI, T1-weighted image; T2WI, T2-weighted image.

Discussion

PAVMs are abnormal fistulous connections between pulmonary arteries and veins and represent an intrapulmonary right-to-left shunt. If left untreated, they may manifest as stroke or brain abscess due to paradoxical embolism of septic foci, as was the case in our patient. The pulmonary capillary bed, which normally functions as a filter of septic emboli, is bypassed in cases of PAVM leading to distal inoculation of the infection.1 2 4 5 Other symptoms and signs of PAVMs include dyspnoea on exertion, polycythaemia, increased HCT, cyanosis and finger clubbing. These symptoms are the result of significant right-to-left shunting leading to chronically reduced blood oxygenation and persistent hypoxaemia.^{4 6} Though the patients may remain asymptomatic for long duration, severe neurological events such as transient cerebral ischaemia, stroke and brain abscesses occur in approximately 6%–10% of untreated cases of PAVM.2 3 6–8 The risk of CNS complications becomes significant when the feeding pulmonary artery is >3 mm in diameter.2–4 7 9

PAVMs are commonly associated with HHT in up to 90% of cases.1 2 4 8–10 Most patients are diagnosed by the screening of patients and their close relatives with HHT. Occasionally, some patients without HHT are found based on evaluation of their clinical symptoms or radiological work-up of rounded radio-opacity on chest X-rays.^{4 5 11}

The diagnosis of HHT is based on ‘Curacao clinical diagnostic criteria’, which include recurrent epistaxis, multiple site telangiectasias, pulmonary and visceral AVMs and a family history of HHT. At least three of these criteria should be present in a patient to be diagnosed as definite HHT.¹² Our patient had isolated PAVMs and did not fulfil other criteria, thus HHT was excluded in our case. Uniform guideline for screening of PAVMs is not present. Contrast echocardiography is considered to be the most sensitive investigation and no further evaluation is required if it is negative.¹¹ If positive or equivocal, CT angiography is performed, which provides the definitive diagnosis and demonstrates the PAVM along with the arterial feeders and the draining veins in great detail.^{4 5 9} PAVMs are classified as simple and complex types.² The simple type is more common (~80%) and has a single arterial feeder to the malformation. Complex malformations (~20%) have more than one arterial feeder and draining veins.^{2 7–9}

Historically, the PAVMs were treated with surgical resection. Percutaneous transluminal embolisation of PAVM was first introduced as a treatment option in 1977.⁴ Endovascular therapy is a minimally invasive treatment where the feeding artery to the PAVM is occluded with coils or vascular plugs or a combination of both and it is associated with minimal morbidity and no mortality. It is a lung-preserving treatment with a very high technical success rate.^{4 8 9} For endovascular embolisation, an appropriately sized mechanical agent (coils or vascular plug) is used to occlude the feeding artery. Embolisation of the aneurysmal sac is not required after complete occlusion of the feeding artery because it gradually decreases in size on follow-up imaging, as seen in our case.² The embolisation agent should be properly sized to prevent the risk of its migration into systemic circulation through the right-to-left shunt. Embolisation coils can be used for any PAVM. Forming a dense cross-sectional network of metal is important for achieving long-term occlusion.⁴ The first coil should be either 20% or 1–2 mm larger than the feeding pulmonary artery diameter.⁹ The detachable coils are expensive; however, they have the advantage of retrievability and can be relocated in case the deployment is unsatisfactory. There are two main disadvantages to using non-detachable coils. First, the non-detachable/push coils cannot be relocated in case of their suboptimal/unsatisfactory deployment in the vessel. The second limitation is that normal pulmonary vessels arising adjacent to the PAVM may need to be sacrificed to anchor the coils.^{7 8 10} Amplatzer vascular plugs address these limitations. Before detachment and final deployment in the candidate vessels, these can be repositioned. Also, as here they are anchored in the target vessel itself, there is no need to sacrifice the normal adjacent vessels.2 3 6 9 10 The vascular plug is a mesh of interwoven metallic wires mounted on a long delivery wire and loaded within plastic tubing in a constrained fashion.⁴ They are particularly suitable for the embolisation of medium-to-large-sized vessels. Typically, the vascular plug should be 30%–50% oversized for the diameter of the target vessel.^{6 9} It is loaded in the guide catheter already placed within the target vessel lumen. Then, it is deployed by unsheathing and detached by unscrewing the delivery wire and when released, it occludes the target vessel lumen.

The potential drawbacks are the need to have the guiding catheter within the target vessel lumen at the site of embolisation and the higher unit cost of the plug compared with the coils. However, the cost factor is nullified by the fact that one needs to use fewer plugs compared with coils for embolisation of similarly sized PAVM.^{4 6 10} Thus, overall expenses may be the same or at times even less when the vascular plugs are used for embolisation. Vessel recanalisation had been described with the first version of the plug; however, it is rare with newer generation devices.^{8 10}

Learning points.

• Pulmonary arteriovenous malformations (PAVMs) are rare vascular lesions producing intrapulmonary right-to-left shunt and can lead to paradoxical embolism of septic foci into the systemic circulation.

• All patients with cryptogenic brain abscesses should be evaluated and screened for PAVMs.

• Endovascular embolisation with coils/vascular plugs is the preferred treatment of PAVMs with minimal morbidity and excellent prognosis.

• The embolisation of PAVMs leads to the resolution of clinical symptoms and infective complications including brain abscesses.

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