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DOI:10.2214/AJR.07.2966
AJR 2008; 190:892-901
© American Roentgen Ray Society

Original Research

MR Angiography for Detection of Pulmonary Arteriovenous Malformations in Patients with Hereditary Hemorrhagic Telangiectasia

Guenther Schneider1, Michael Uder2, Michael Koehler3, Miles A. Kirchin4, Alexander Massmann1, Arno Buecker1 and Urban Geisthoff5

1 Department of Diagnostic and Interventional Radiology, University Hospital of Saarland, 66421 Homburg/Saar, Germany.
2 Department for Radiology, Friedrich-Alexander-University, Erlangen-Nuremberg, Germany.
3 Department for Clinical Radiology, Westfaelische Wilhelms-University, Muenster, Germany.
4 Worldwide Medical & Regulatory Affairs, Bracco Imaging SpA, Milan, Italy.
5 Department of Otorhinolaryngology, University Hospital of Saarland, Homburg/Saar, Germany.

Received August 1, 2007; accepted after revision October 21, 2007.

 
M. A. Kirchin is an employee of Bracco Imaging.

Address correspondence to G. Schneider (guentherschneider{at}googlemail.com).


Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
OBJECTIVE. The purpose of our study was to evaluate contrast-enhanced MR angiography (CE-MRA) as a screening procedure for the detection of pulmonary arteriovenous malformations (AVMs) in patients with hereditary hemorrhagic telangiectasia (HTT).

MATERIALS AND METHODS. Two hundred three consecutive subjects (patients with diagnosed HHT or first-degree relatives; 87 males, 116 females; 6–83 years old) underwent pulmonary CE-MRA with 0.1 mmol/kg of gadobenate dimeglumine. The presence of pulmonary AVM was scored as 0 (none present), 1 (definitely present), or 2 (uncertain) and was evaluated by patient sex and pulmonary AVM size (< 5, 5–10, 11–15, 16–20, > 20 mm). Patients scored as 1 or 2 with at least one pulmonary AVM of ≥ 5 mm underwent conventional pulmonary angiography for possible embolization. Pulmonary AVM detection on CE-MRA and pulmonary angiography was compared using paired Student's t tests.

RESULTS. The presence of pulmonary AVM was considered definite in 56 of 203 (27.6%) patients and uncertain in one of 203 patients on CE-MRA. Of 156 pulmonary AVMs detected on CE-MRA, 124 (49 in 27 males, 75 in 30 females) were detected on first screening CE-MRA and 32 on follow-up CE-MRA. Pulmonary AVMs on CE-MRA were solitary in 25 patients, multiple in 31 patients, and predominantly small (< 5 mm, n = 32; 5–10 mm, n = 45). Significantly (p < 0.0001) fewer pulmonary AVMs were detected on pulmonary angiography (76/96 [79.2%] evaluable pulmonary AVMs in 40 patients before first pulmonary angiography; 92/119 [77.3%] pulmonary AVMs overall). Three-dimensional maximum-intensity-projection reconstructions permitted improved pulmonary AVM visualization and embolization planning of complex pulmonary AVMs.

CONCLUSION. CE-MRA is suitable for screening patients with HHT. It permits accurate detection and staging of pulmonary AVMs, appropriate differentiation of lesions requiring embolization and accurate orientation, and visualization and planning of embolization therapy.

Keywords: contrast-enhanced MR angiography • embolization therapy • hereditary hemorrhagic telangiectasia • lung • pulmonary angiography • pulmonary arteriovenous malformations • screening


Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Hereditary hemorrhagic telangiectasia (HHT), also known as Osler-Weber-Rendu disease, is an autosomal dominant vascular disease affecting approximately one in 5,000–8,000 people [1–4]. It is characterized by recurrent epistaxis; by mucocutaneous telangiectases of the nose, mouth, lips, and fingertips; and by arteriovenous malformations (AVMs) that affect the arteries of the brain, lung, nose, and gastrointestinal system, causing serious morbidity and a high rate of mortality in affected patients [1, 2, 5–9]. The first symptoms arise in childhood (typically < 10 years), with recurrent and increasing nose bleeding due to mucocutaneous telangiectases [5, 6]. By the age of 16 years, more than 70% of genetically affected individuals will have developed signs of HHT, rising to about 90% by the age of 40 years [1, 8, 10, 11].

Pulmonary AVMs are present in up to 30% of patients with HHT [1, 11–15] and represent direct communications between the pulmonary arteries and pulmonary veins that arise due to degeneration of the capillary network and reciprocal development of direct shunts between arteriola and venula. Pulmonary AVMs may be single or multiple and usually manifest as fragile thin-walled aneurysms that may increase in size [13, 14, 16, 17] and that are potentially at risk for hemorrhage into a bronchus or the pleural cavity [9, 16, 18]. The risk of hemorrhage or serious neurologic consequences—ranging from migraine [19] to transient ischemic attacks, stroke, cerebral abscess, and seizure [1, 12, 15, 16, 20–23]—is high, even in patients with clinically silent pulmonary AVMs [1, 16]. Accurate screening of patients with, or at risk for, HHT and effective treatment of detected pulmonary AVMs are therefore essential to avoid potential complications and to reduce associated morbidity and mortality [1–4, 8, 11, 12, 15, 16, 23, 24].

Of the screening methods available, contrast echocardiography [25–27], radionuclide perfusion [28, 29], and gas exchange or pulse oximetry methods [12, 30, 31] are effective to a greater or lesser extent in detecting right-to-left shunts associated with pulmonary AVM presence, but do not provide detailed information concerning anatomic detail or pulmonary AVM location. CT is another noninvasive technique that permits diagnosis and improved definition of pulmonary AVM vascular anatomy [32–34] and that may prove beneficial with the advent of MDCT technology [35, 36]. However, ionizing radiation is a potential drawback to the routine use of CT for pulmonary AVM screening and follow-up, particularly in young subjects or women of child-bearing age, and particularly if patients require regular follow-up over an extended period. For the same reasons, and because of the high cost, time requirements, and inherent complications, conventional pulmonary angiography is inappropriate as a screening tool and is today usually used solely for preinterventional localization during embolization therapy [37].

Of the noninvasive methods available, contrast-enhanced MR angiography (CE-MRA) fulfills many of the requisites of a suitable screening technique for patients with HHT in that it does not require ionizing radiation; it is increasingly widely available; and it is potentially able to provide precise information on the number, location, and complexity of pulmonary AVMs, if present. However, whereas a number of small-scale studies and case reports have shown the feasibility of CE-MRA for the diagnosis and identification of pulmonary AVMs, particularly of lesions > 3 mm [38–44], there are as yet no reports on the potential value of CE-MRA for pulmonary AVM screening and follow-up in a large cohort of patients with HHT. Thus, the present study was performed to evaluate the usefulness of CE-MRA compared with conventional pulmonary angiography for the detection and follow-up of pulmonary AVMs in patients with diagnosed HHT. Moreover, because of the 3D reconstruction capabilities of CE-MRA and the possibility of precisely displaying pulmonary AVM feeding vessels [40], the value of CE-MRA as a preoperative aid to embolization therapy was also assessed.


Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Subject Population
The evaluation of patients undergoing routine clinical workup for the presence of pulmonary AVMs received institutional review board and ethics committee approval. Written informed consent was not required of patients in this study because the diagnostic tests were performed in conjunction with other routine screening procedures for AVMs in the brain and liver.

A total of 203 consecutive adult and pediatric patients (87 males: mean age, 47.4 ± 17.6 years; range, 6–83 years; and 116 females: 46.1 ± 15 years; range, 11–74 years) who fulfilled the diagnostic criteria for definite HHT as described by Shovlin et al. [45], or who were first-degree relatives of a patient with HHT, were evaluated as part of clinical routine between January 2000 and September 2006. Of these 203 patients, 27 (13.3%) had a confirmed genetic defect causing HHT. All patients were referred for pulmonary CE-MRA because of the positive diagnosis of HHT or because they were a first-degree relative of a patient with HHT. Follow-up CE-MRA examinations were performed at regular intervals according to the findings of screening studies and the first CE-MRA examination. Follow-up of patients with no evidence of pulmonary AVMs on the basis of screening and initial CE-MRA was performed after 2 years in patients with confirmed HHT and after 5 years in first-degree relatives of patients with HHT who themselves had no confirmed diagnosis of HHT. A first follow-up CE-MRA examination of patients confirmed to have small (< 5 mm) pulmonary AVMs for which no embolization therapy was planned was typically performed after approx imately 1 year. For patients with embolized pul monary AVMs, follow-up CE-MRA was performed initially at 3 months after therapy and again at 1 year in patients with additional small (< 5 mm) pulmonary AVMs or at 2 years in patients with no residual lesions (Fig. 1). In one patient, follow-up CE-MRA was performed at 6 years after initial screening CE-MRA because of poor patient com pliance resulting in intervening unavailability of the patient for scheduled follow-up.


Figure 1
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  		Fig. 1 —Flowchart shows management of patients with proven hereditary hemorrhagic telangiectasia (HTT) (criteria described by Shovlin et al. [45]). CE-MRA = contrast-enhanced MR angiography, PAVM = pulmonary arteriovenous malformation, and first-degree relatives. PA = pulmonary angiography.

 
Pulmonary Contrast-Enhanced MR Angiography
Pulmonary MR angiography was performed at 1.5 T (Magnetom Vision [gradient-switching capability = 25 mT · m–1; slew rate = 40 · T · m–1 · s–1] or Magnetom Sonata [gradient-switching capa bility = 40 mT · m–1; slew rate = 200 T · m–1 · s–1], Siemens Medical Solutions) using a phased-array body coil with the patient lying supine head first in the bore of the magnet with arms extended above the head.

Accurate positioning of the imaging slab was achieved after preliminary acquisition in three orthogonal plains of T1-weighted FLASH scout images (TR/TE, 15/6; flip angle, 30°; matrix, 128 x 256; field of view, 500 mm; section thickness, 10 mm; 5 sections) and localizer T2-weighted half-Fourier rapid acquisition with relaxation enhancement (RARE) images (infinite/90; flip angle, 150°; interecho spacing, 4.4 milliseconds; 1 signal average; matrix, 160 x 256 [half-Fourier reconstruction]; acquisition time, 14 seconds) obtained during inspiration breath-hold. A rectangular field of view, typically 300 x 400 mm, was used for axial and sagittal acquisitions, whereas a field of view of 400 x 400 mm was used for coronal imaging. If necessary, the field of view was modified for each patient.

CE-MRA of the thorax was performed using one of two approaches, depending on patient body size. A single coronal 3D volume over the entire thorax was used for simultaneous imaging of both lungs in patients whose entire lung measured < 160 mm in the anteroposterior direction, whereas separate sagittal acquisitions of each lung were obtained in patients with an anteroposterior lung dimension larger than 160 mm.

All patients underwent unenhanced and dual-phase CE-MRA examinations under breath-hold (breath-hold duration, 16–19 seconds depending on the slab thickness). Initiation of the first CE-MRA acquisition began approximately 2 minutes after completion of the unenhanced acquisition, and 8 seconds separated the two CE-MRA acquisitions. CE-MRA was performed using a 3D gradient-echo sequence (4.6/1.8; flip angle, 30°; matrix, 160–180 x 512; field of view, 320 x 450–500 mm [coronal] or 250 x 380–400 mm [sagittal]; slab thickness, 120–160 mm; reconstructed slice thickness, 1.82–2.2 mm) with asymmetric k-space acquisition in which the center of k-space was acquired during the first third of the sequence. The contrast agent used was gadobenate dimeglumine (MultiHance, Bracco Imaging), which was administered at a single dose of 0.1 mmol/kg of body weight to patients for whom a single CE-MRA acquisition of both lungs was obtained and as two injections of 0.05 mmol/kg of body weight to larger patients requiring separate acquisitions of each lung.

Timing of the CE-MRA acquisition relative to the contrast injection was determined using a test bolus approach based on the arrival of 2 mL of gadobenate dimeglumine at the level of the pulmonary arteries. For determination of the contrast transit time, axial 2D T1-weighted turbo FLASH images (5.8/2.4; flip angle, 10°; matrix, 128 x 256; field of view, 400 mm; section thickness, 8 mm) were acquired at a rate of one image per second over 30 seconds beginning simultaneously with the start of the test bolus injection. The time between the start of the test bolus injection and the peak of signal intensity enhancement in the pulmonary trunk minus one fourth of the acquisition time of the MR angiography sequence was taken as the required delay before CE-MRA image acquisition.

All injections of gadobenate dimeglumine were made using a power injector (Injektron MRT, Medtron) via an antecubital vein of the right arm at a rate of 2.5 mL/s and were followed by a 20-mL saline flush at the same rate. The entire examination required approximately 20 minutes for each patient.

Data Postprocessing
All acquired MR angiograms were reconstructed on a separate satellite console using a standardized protocol. After subtraction of the unenhanced data sets, image postprocessing was performed to obtain targeted rectangular maximum-intensity-projection (MIP) reconstructions that encompassed the entire thoracic vasculature. Each MIP reconstruction was rotated in the coronal plain with an increment of 5° between each image. For patients in whom one single volume was acquired, additional separate reconstructions were obtained of the left and right pulmonary vasculature. Additional interactive sub volume MIP reconstructions were obtained to better define the vascular morphology and feeding vessels of detected pulmonary AVMs indicated for embolization.

Image Evaluation
Images were evaluated in consensus by two radiologists who had 8 and 12 years of experience in MRI in general and CE-MRA in particular. Assessment was performed of both CE-MRA raw data images (coronal source images and axial slices reformatted to a slice thickness of 2–4 mm) and MIP reconstructions. Images were evaluated for pulmonary AVM presence according to a 3-point scale in which 0 = no pulmonary AVM present, 1 = pulmonary AVM definitely present, and 2 = uncertain for pulmonary AVM presence. The size and location (right upper, right middle, or right lower lobe [RUL, RML, RLL, respectively] and left upper or left lower lobe [LUL, LLL, respectively]) of detected pulmonary AVMs were recorded for all patients scored as 1 or 2 for pulmonary AVM presence.

Detected pulmonary AVMs were considered simple if they were determined to have only one feeder artery and one draining vessel. Conversely, pulmonary AVMs with more than one feeder or draining vessel were considered complex.

Pulmonary Angiography and Embolization Therapy
Pulmonary angiography before possible emboliz ation therapy was performed in all patients whose positive CE-MRA findings indicated one or more pulmonary AVMs of ≥ 5 mm across the largest dimension of the aneurismal structure who would potentially benefit from embolization therapy. Five millimeters was chosen as the minimum size for possible embolization therapy because small pulmonary AVMs are less likely to hemorrhage and thus less of a short-term risk and because feeder vessel access is typically smaller than 3 mm in pulmonary AVMs < 5 mm and thus less amen able to treatment. No patients with positive findings on CE-MRA were found to have contraindications for catheter angiography with iodinated contrast media. For ethical reasons, patients with negative findings on other screening procedures (chest radiography, measurement of peripheral oxygen saturation, echo-bubble enhanced Doppler sonography) and no pulmonary AVMs on CE-MRA were not referred for pulmonary angiography. Likewise, pulmonary angiography was not performed in patients for whom pulmonary angiography and subsequent pulmonary AVM embolization were considered inappropriate or of little value (i.e., in patients with small [< 5 mm] pulmonary AVMs on CE-MRA). Patients scored as 1 or 2 for pulmonary AVM presence on CE-MRA but with pulmonary AVMs of < 5 mm were referred for follow-up CE-MRA before possible pulmonary angiography and embolization later.

Pulmonary angiography and embolization procedures were performed by different experienced (5–10 years) interventional radio logists who were aware of the positive CE-MRA findings and who intended using the CE-MRA images as a road map for the pulmonary angio graphy procedure. For pulmonary angiography a 7-French introducer sheath was introduced over a guidewire in the right femoral vein under local anesthesia, and a 4-French pigtail catheter was passed via the inferior vena cava into the right and left pulmonary arteries. For selective catheter ization of pulmonary AVM feeding arteries and embolization therapy, we used a 7-French guiding catheter with hydrophilic coating and a matched inner coaxial catheter (white Lumax, Cook).

Patients undergoing initial global pulmonary angiography to achieve a general overview of the anatomy and presence of pulmonary AVMs received injections of iodinated contrast medium (Iomeron-300 [iomeprol-300], Bracco) by means of a power injector (25 mL at 10 mL/s via a 5-French pigtail catheter) into the main left or right pulmonary artery, whereas patients undergoing selective pulmonary angiography received manual contrast material injections into the segmental arteries as necessary. In all cases, an Axiom Artis (Siemens Medical Solutions) angiography system was used. Embolizations were performed with U.S. Food and Drug Administration–approved Nester Em bo lization Coils, Platinum (Cook Medical) of different sizes using either scaffold or anchor technique as described elsewhere [46–48].

Statistical Analysis
Detected pulmonary AVMs on CE-MRA were evaluated in terms of size (< 5, 5–10, 11–15, 16–20, and > 20 mm) and distribution for all subjects together and for male and female subjects separately. Additional evaluation was performed for pulmonary AVM presence among women of child-bearing age (< 50 years old). To assess the value of CE-MRA as a pulmonary AVM screening technique for patients with HHT, the number and distribution of pulmonary AVMs detected on CE-MRA before the first pulmonary angiography procedure were compared with the number and distribution detected during the first pulmonary angiography procedure. The two techniques were compared for pulmonary AVM detection using paired Student's t tests at a significance level of p < 0.05. Subsequent evaluations were performed to compare pulmonary AVM detection on first screening CE-MRA with pulmonary AVM detection on follow-up CE-MRA and to compare overall pulmonary AVM detection across all CE-MRA examinations with overall pulmonary AVM detection across all pulmonary angiography procedures.


Figure 2
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  		Fig. 2A —56-year-old man with proven hemorrhagic telangiectasia (HTT) according to criteria described by Shovlin et al [45]. Maximum-intensity-projection reconstruction shows two pulmonary arteriovenous malformations (AVMs) (arrows) in right lung. Larger AVM shows one feeding artery, one draining vein, and septate aneurysm sac. Smaller AVM similarly has one feeding artery and one draining vein (no septations).

 


Figure 3
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  		Fig. 2B —56-year-old man with proven hemorrhagic telangiectasia (HTT) according to criteria described by Shovlin et al [45]. Volume rendering of same data set accurately depicts 3D orientation of feeding arteries to both pulmonary AVMs.

 


Figure 4
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  		Fig. 2C —56-year-old man with proven hemorrhagic telangiectasia (HTT) according to criteria described by Shovlin et al [45]. Selective pulmonary angiography of right lung (C) reveals both pulmonary AVMs (arrows, C), although detailed anatomy is seen only on superselective pulmonary angiography of feeding arteries (D and E). Note that in E larger pulmonary AVM (arrow) is already embolized.

 


Figure 5
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  		Fig. 2D —56-year-old man with proven hemorrhagic telangiectasia (HTT) according to criteria described by Shovlin et al [45]. Selective pulmonary angiography of right lung (C) reveals both pulmonary AVMs (arrows, C), although detailed anatomy is seen only on superselective pulmonary angiography of feeding arteries (D and E). Note that in E larger pulmonary AVM (arrow) is already embolized.

 


Figure 6
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  		Fig. 2E —56-year-old man with proven hemorrhagic telangiectasia (HTT) according to criteria described by Shovlin et al [45]. Selective pulmonary angiography of right lung (C) reveals both pulmonary AVMs (arrows, C), although detailed anatomy is seen only on superselective pulmonary angiography of feeding arteries (D and E). Note that in E larger pulmonary AVM (arrow) is already embolized.

 
Finally, the value of CE-MRA for the identification and preoperative assessment of complex pulmonary AVMs (i.e., a pulmonary AVM with more than one feeding or draining vessel) was determined in terms of the quality and extent of visualization of feeding and draining vessels compared with the quality of visualization achievable on pulmonary angiography alone.


Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Detection of Pulmonary AVMs on Pulmonary CE-MRA
First screening CE-MRA—CE-MRA was performed successfully in all patients and all CE-MRA image sets were interpretable, with no major imaging- or patient-related artifacts.

Of the 203 patients evaluated, 56 (27.6%) were considered to definitely have one or more pulmonary AVMs (pulmonary AVM presence score = 1) on first screening pulmonary CE-MRA, and one (0.5%) additional patient was considered uncertain for pulmonary AVM presence (score = 2). Because all patients were evaluated as part of clinical routine, this latter patient was considered positive for pulmonary AVM presence for subsequent clinical workup. No pulmonary AVMs were detected on CE-MRA in any patient fulfilling the diagnostic criteria for HHT whose preliminary screening examinations were negative. No pulmonary AVMs were detected on CE-MRA in one patient considered positive on the basis of findings from prior echo-bubble-enhanced Doppler sonography. Because all other screening examinations in this patient were negative, and the patient was considered at increased risk for catheter angiography, no follow-up pulmonary angiography was performed in this patient.


Figure 7
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  		Fig. 3A —30-year-old woman with three pulmonary arteriovenous malformations (AVMs). Pulmonary AVMs are detected on maximum-intensity-projection reconstruction.

 


Figure 8
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  		Fig. 3B —30-year-old woman with three pulmonary arteriovenous malformations (AVMs). Multiplanar reconstructions reveal three feeding arteries (arrows). This additional information was considered of value for improved embolization planning.

 


Figure 9
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  		Fig. 3C —30-year-old woman with three pulmonary arteriovenous malformations (AVMs). Multiplanar reconstructions reveal three feeding arteries (arrows). This additional information was considered of value for improved embolization planning.

 
Initial screening CE-MRA revealed 124 pulmonary AVMs, of which 49 were found in 27 men (mean age, 44.7 ± 16.2 years) and 75 were found in 30 women (46.0 ± 12.7 years). The detected pulmonary AVMs were solitary in 25 patients and multiple (n = 2–8) in 31 patients (Figs. 2A, 2B, 2C, 2D, 2E, 3A, 3B, and 3C). A total of 46 pulmonary AVMs were detected on first screening CE-MRA among 17 women of child-bearing age (< 50 years; mean age, 37.4 ± 10 years).

Most of the 124 pulmonary AVMs detected on first screening CE-MRA were small (< 5 mm, n = 32; 5–10 mm, n = 45), although 19 lesions exceeded 20 mm, of which the largest measured up to 60 mm in the longest dimension (Table 1). The smallest pulmonary AVM detected on first screening CE-MRA was 2 mm.


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  		TABLE 1: Distribution by Size of Pulmonary Arteriovenous Malformations (AVMs) Detected on First Screening Contrast-Enhanced MR Angiography

 

Follow-up CE-MRA—Of the 57 patients considered to have one or more pulmonary AVMs on first screening CE-MRA, 26 subjects underwent one or more follow-up CE-MRA examinations up to and including May 2006. Sixteen of these 26 patients also underwent pulmonary angiography with or without embolization before follow-up CE-MRA. Among these 26 patients, follow-up CE-MRA detected 32 additional pulmonary AVMs in six patients that were not present on first screening CE-MRA or intervening pulmonary angiography. The 32 new pulmonary AVMs comprised 16 that were detected in five women who were between 40 and 49 years old and 16 that were detected in one man who was 56 years old at first screening CE-MRA (Figs. 4A and 4B). The mean interval between the first CE-MRA examination and a first follow-up CE-MRA examination was 13.9 ± 7.2 months for the five female patients, during which 14 of the 16 new pulmonary AVMs developed. The remaining two additional pulmonary AVMs were present in two of three female patients who underwent a second follow-up CE-MRA examination at 21.2 ± 18.6 months after the first follow-up examination. The interval between initial screening CE-MRA and follow-up CE-MRA in the one male patient was 6 years. The 16 additional pulmonary AVMs seen on follow-up CE-MRA in this patient were distributed unevenly between the two lungs (six pulmonary AVMs in the right lung, 10 in the left). The 32 new pulmonary AVMs were predominantly small (< 5 mm, n = 16; 5–10 mm, n = 15; 11–15 mm, n = 1). Follow-up pulmonary angiography in these six patients revealed only 25 new pulmonary AVMs.


Figure 10
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  		Fig. 4A —56-year-old man with multiple pulmonary arteriovenous malformations (AVMs). Initial screening contrast-enhanced MR angiography (CE-MRA) reveals several small pulmonary AVMs in both lungs.

 

Figure 11
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  		Fig. 4B —56-year-old man with multiple pulmonary arteriovenous malformations (AVMs). Follow-up CE-MRA 6 years later reveals several new pulmonary AVMs (arrows) not seen on first screening CE-MRA and increased lesion size for several preexisting pulmonary AVMs (arrowheads).

 
Comparison of CE-MRA with Conventional Pulmonary Angiography
A comparison of CE-MRA and conventional pulmonary angiography for pulmonary AVM detection is shown in Table 2 for both initial screening CE-MRA compared with first pulmonary angiography and for follow-up CE-MRA compared with all pulmonary angiography examinations. Overall, 40 (17 men, 23 women) of the 57 patients with 103 pulmonary AVMs definitely (n = 102) or possibly (n = 1) detected on initial screening CE-MRA were subsequently referred for global (n = 36) or selective (n = 4) pulmonary angiography before possible embolization, depending on the size and location of the pulmo nary AVMs on CE-MRA. The four patients undergoing selective pulmonary angiography comprised one man who was 41 years old and had one large (60 x 30 mm) pulmonary AVM in the left lung and one small (5 mm) pulmonary AVM in the right lung, and three women with eight pulmonary AVMs overall in the left lung and five pulmonary AVMs in the right lung. Selective pulmonary angiography in these patients resulted in a lack of angiographic correlation for seven pulmonary AVMs detected on CE-MRA in the contralateral lung. Consequently, direct comparison of CE-MRA and pulmonary angiography was possible for 96 pulmonary AVMs detected on screening CE-MRA. Of these 96 pulmonary AVMs, initial pulmonary angiography detected only 76 (79.2%) lesions (p < 0.0001) (Table 2). The 20 pulmonary AVMs not seen on pulmonary angiography were in all cases small (14 were ≤ 5 mm, three were 7 mm, two were 10 mm, one was 12 mm) and distributed throughout the lung (three, zero, and seven in the RUL, RML, and RLL, respectively; seven and three in the LUL and LLL, respectively). The one patient with a score of 2 (uncertain) for pulmonary AVM presence on CE-MRA (for a suspected lesion of 7 mm in the RLL) was determined not to have a pulmonary AVM after pulmonary angiography and follow-up CE-MRA. Global pulmonary angiography was performed in 15 of the 17 women of child-bearing age who had pulmonary AVMs detected on first screening CE-MRA. Of the 43 pulmonary AVMs with angiographic correlation in these women, pulmonary angio graphy detected only 32 (74.4%) lesions.


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  		TABLE 2: Comparison of Contrast-Enhanced MR Angiography (CE-MRA) and Global or Selective Pulmonary Angiography (PA) for Detection of Pulmonary Arteriovenous Malformations

 

Similar results were obtained when comparing the overall detection of pulmonary AVMs after follow-up CE-MRA with the detection after all pulmonary angiography procedures. In all, only 92 (77.3%) of 119 pulmonary AVMs detected on CE-MRA were seen on pulmonary angiography (p = 0.0003) (Table 2).

Embolization
Of the 92 pulmonary AVMs detected overall on pulmonary angiography, 83 (90.2%) were successfully embolized. Those that were not embolized were considered either too small to be clinically relevant (six pulmonary AVMs each ≤ 3 mm in size) or were highly complex with either undetectable feeding arteries (a single 10-mm pulmonary AVM with a large septate aneurysmal sac and low flow) or multiple small feeding arteries from different segmental arteries (a single large 60 x 30 mm pulmonary AVM). In both these latter cases, embolization was attempted without success. The remaining pulmonary AVM that was not embolized was scheduled for embolization later. No complications occurred in any patient referred for pulmonary angiography, and no case of reperfusion of embolized pulmonary AVMs was reported.

Complex Pulmonary AVMs
A total of 51 complex pulmonary AVMs were detected on CE-MRA in 26 of the 56 patients determined to definitely have one or more pulmonary AVMs (28 pulmonary AVMs in 10 men, 23 pulmonary AVMs in 16 women). Most patients with complex pulmonary AVMs had only one (n = 17; five men, 12 women) (Figs. 5A, 5B, 5C, and 5D) or two (n = 5; two men, three women) lesions, although four patients were determined to have three or more complex pulmonary AVMs (one man and one woman with three complex pulmonary AVMs each, one man with four complex pulmonary AVMs, and one man with eight complex pulmonary AVMs). The smallest complex pulmonary AVM detected on CE-MRA was 3 mm; all others were ≥ 5 mm (17 were 5–10 mm, eight were 11–15 mm, five were 16–20 mm, and 14 were > 20 mm in the longest direction), with the largest measuring 40 x 50 x 60 mm in a 67-year-old woman. Of the 51 complex pulmonary AVMs detected, 45 were referred for pulmonary angiography, of which 43 were successfully embolized. Only the two above-mentioned lesions with undetectable or multiple feeding arteries were not successfully embolized. The ability to interactively scroll CE-MRA raw data images and to acquire MIP reconstructions of complex pulmonary AVMs that accurately displayed the angioarchitecture of the lesion in 3D were considered invaluable for subsequent selective and superselective catheterization of the feeding vessels because precise orientation before intervention could be gained (Figs. 3A, 3B, and 3C).


Figure 12
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  		Fig. 5A —26-year-old woman (daughter of patient in Figs. 2A, 2B, 2C, 2D, and 2E). Maximum-intensity-projection contrast-enhanced MR angiography (CE-MRA) image shows a complex pulmonary arteriovenous malformation (AVM) in the right lung.

 

Figure 13
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  		Fig. 5B —26-year-old woman (daughter of patient in Figs. 2A, 2B, 2C, 2D, and 2E). Anatomy is much better depicted on volume-rendered CE-MRA image, which reveals two peripheral feeding arteries (arrows) and one central feeding artery that divides into two further feeding arteries (arrowheads) just before pulmonary AVM. In addition, two draining veins (asterisks) are nicely depicted.

 

Figure 14
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  		Fig. 5C —26-year-old woman (daughter of patient in Figs. 2A, 2B, 2C, 2D, and 2E). Superselective pulmonary angiography of central feeding artery confirms findings in B.

 

Figure 15
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  		Fig. 5D —26-year-old woman (daughter of patient in Figs. 2A, 2B, 2C, 2D, and 2E). Embolization of central feeding arteries leads to reflux of contrast medium into two peripheral feeding arteries.

 

Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Pulmonary angiography has traditionally been the gold standard approach for diagnosis of pulmonary AVMs and is considered mandatory to determine the position and structure of all abnormal vascular lesions in the lungs before surgical or interventional treatment. Unfortunately, pulmonary angiography is labor-, cost-, time-, and radiation-intensive and thus is impractical as a pulmonary AVM screening tool for patients with HHT. Radiation exposure in itself is sufficient to preclude its use in pediatric patients and in women of child-bearing age who are likely to require regular follow-up examinations for the presence of pulmonary AVM, regardless of whether intervening embolization therapy is performed. The results of our study show not only that CE-MRA is an effective screening tool for the detection of pulmonary AVMs but also that it is a superior technique to global or selective pulmonary angiography, permitting the detection of significantly more pulmonary AVMs both overall (p = 0.0003) and when compared solely with initial global or selective pulmonary angiography (p < 0.0001). Although the pulmonary AVMs missed on pulmonary angiography were predominantly small and possibly of limited immediate clinical relevance, a reported tendency to increase in size over time [13, 14, 16, 17] highlights the need for careful monitoring for the presence of pulmonary AVMs. Interestingly, the greatest benefit for CE-MRA over pulmonary angiography for pulmonary AVM detection was noted for women. Although this was possibly a result of there being more pulmonary AVMs and more multiple pulmonary AVMs in women, this finding may nevertheless be of considerable interest given that pregnancy is associated with an increased rate of pulmonary AVM growth [9, 15, 49] and a concomitantly greater risk of complications such as pulmonary AVM hemorrhage [9, 16, 18, 46]. Notably, pulmonary angiography detected only 32 (74.4%) of 43 pulmonary AVMs that were detected on CE-MRA in 15 women of child-bearing age.

Of particular interest in this study was the detection of 32 additional pulmonary AVMs in six patients on follow-up CE-MRA that were not present on first screening CE-MRA or intervening pulmonary angiography. Although most pulmonary AVMs in patients with HHT are congenital, secondary or acquired pulmonary AVMs are not rare [15, 50–52]. In this study, 16 additional pulmonary AVMs were detected in five women between 40 and 49 years old, and the remaining 16 additional lesions were detected in one man who was 54 years old. Because none of the patients was known to have a specific medical history that might account for secondary pulmonary AVM development and because the CE-MRA examination protocol and image postprocessing were identical for all examinations in all patients, it is possible either that entirely new pulmonary AVMs arose in these patients over time or, more likely, that the size of the pulmonary AVMs was below the limits of detection on first screening CE-MRA and pulmonary angiography but increased in size before follow-up CE-MRA. In this study, most of the additional pulmonary AVMs detected on follow-up CE-MRA were comparatively small; just one additional pulmonary AVM was determined to be greater than 10 mm, and half were determined to be smaller than 5 mm. Notably, the smallest pulmonary AVM detected on CE-MRA in this study was 2 mm, so it seems feasible that very small pulmonary AVMs in these patients may not have been detected on first screening CE-MRA. Possibly the routine detection of even very small (< 2 mm) pulmonary AVMs will be achievable with the improved spatial resolution of 3-T MRI systems [44]. Likewise, developments in contrast agent design may also improve detection of very small pulmonary AVMs. In our study, gadobenate dimeglumine was used because the increased R1 relaxivity of this agent in blood [53] has proven to be advantageous in various MRI applications for the improved visualization of small vessels and poorly enhancing lesions [54–57]. A final consideration concerning the additional 32 pulmonary AVMs on follow-up CE-MRA is that they were all present in patients with multiple pulmonary AVMs. Previous reports suggest that increases in pulmonary AVM size are more likely when they are multiple [13, 16].

Of the various approaches to the treatment of pulmonary AVMs, coil embolization is widely considered the safest and most effective technique (37, 46–48, 58–61). However, successful embolization depends on satisfactory visualization of the feeding vessels of the pulmonary AVM to adequately position the embolization catheter. Although visualization of the feeding vessels on pulmonary angiography is not usually problematic in simple pulmonary AVMs that comprise just one arterial feeding vessel and one draining vein [62], it may be more difficult in complex pulmonary AVMs that have multiple feeding vessels because of the limited projections available on conventional pulmonary angio graphy. Beyond merely detecting more pulmonary AVMs than were detected on pulmonary angiography, our study also shows the additional value of CE-MRA for preoperative planning of the embolization procedure. Specifically, this study shows that the possibility of acquiring MIP reconstructions of complex pulmonary AVMs in multiple planes and of visualizing the feeding vessels in a manner not necessarily achievable on conventional pulmonary angiography can aid con siderably in the embolization procedure. Although state-of-the-art rotational angiography systems also permit visualization in multiple planes, that technique is necessarily limited by the need to expose patients to ionizing radiation, which may be problematic for patients who require repeated interventions.

The principal limitation of our study is that although patients with confirmed HHT were prospectively and consecutively evaluated with CE-MRA, pulmonary angiography was performed only in those patients who had positive pulmonary AVM findings on CE-MRA for whom embolization therapy was considered a realistic possibility. Thus, pulmonary angiography was not performed in patients with negative findings on CE-MRA or in patients with small (< 5 mm) pulmonary AVMs on CE-MRA for whom embolization was considered unnecessary. Similarly, selective rather than global pulmonary angiography or pulmonary angiography of only one lobe was performed if a patient was shown on CE-MRA to have pulmonary AVMs limited to a specific lobe of the lungs. The restricted use of pulmonary angiography was solely for ethical reasons, to limit the exposure to ionizing radiation and potentially nephrotoxic iodinated contrast media of patients who may require numerous additional follow-up screen ing examinations over a long time. For similar reasons, in those patients in whom pulmonary angiography was performed, care was taken to limit the radiation and contrast medium exposure as much as possible. However, it should be emphasized that in all cases the conventional angiograms provided sufficient coverage of the pulmonary arterial vasculature not only to reliably compare pulmonary angiography with CE-MRA in terms of the visualization of potentially treatable pulmonary AVMs, but also to potentially detect small pulmonary AVMs only incidentally seen on CE-MRA; only four of 40 patients underwent selective rather than global pulmonary angiography because CE-MRA revealed only small pulmonary AVMs that were considered of insufficient immediate concern.

A second limitation is that comparison with other possible noninvasive screening procedures such as unenhanced or contrast-enhanced CT was not performed. Again, the absence of CT as a comparative examination was solely for ethical reasons: Procedures that use ionizing radiation are considered inappropriate at our institution for applications that may require regular follow-up over several years, particularly if they involve pediatric patients or women of child-bearing age. On the other hand, it is clear that CT with or without iodinated contrast medium is another sensitive noninvasive technique for the detection and evaluation of pulmonary AVMs [33, 34, 36], and further work should be performed to compare CE-MRA and MDCT intraindividually for diagnostic performance.

In conclusion, our study shows that CE-MRA is applicable both as a sensitive screening tool for the detection of pulmonary AVMs in patients with HHT and as a valuable adjunct to the preinterventional planning of embolization therapy. Moreover, CE-MRA may also prove invaluable for follow-up of embo lization procedures to determine the suc cess of the procedure or the need for re peat embolization. The possibility of detecting small pulmonary AVMs and following their clinical progression over time without concern about radiation exposure, and the avoidance of potentially nephrotoxic iodinated con trast media and the inherent complications of catheter angiography, are specific advantages of CE-MRA over pulmonary angiography. The possibility to detect small pulmonary AVMs and to follow their clinical progression over time without concern to radiation exposure, the need for potentially nephrotoxic iodinated contrast media, or the inherent complications of catheter angiography, represent a specific advantage over pulmonary angiography, and in the case of radiation exposure and iodinated contrast media, also other potential screening tools such as MDCT angiography. This may be particularly important for routine screening of pediatric subjects and women of child-bearing potential.


References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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