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(Radiology. 2001;219:243-246.)
© RSNA, 2001


Thoracic Imaging

Pulmonary Arteriovenous Malformations: Three-dimensional Gadolinium-enhanced MR Angiography—Initial Experience1

Daniel D. Maki, MD, Evan S. Siegelman, MD, David A. Roberts, MD, PhD, Richard A. Baum, MD and Warren B. Gefter, MD

1 From the Department of Radiology, University of Pennsylvania Medical Center, Philadelphia. Received August 9, 1999; revision requested September 27; final revision received September 12, 2000; accepted September 19. Address correspondence to D.D.M., Scottsdale Medical Imaging, 3501 N Scottsdale Rd, Ste 130, Scottsdale, AZ 85251 (e-mail: cactusrad@hotmail.com).


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To determine whether three-dimensional gadolinium-enhanced magnetic resonance (MR) angiography could be used to identify pulmonary arteriovenous malformations (PAVMs) and to accurately identify the size and number of feeding arteries.

MATERIALS AND METHODS: Eight patients suspected of having PAVM were examined with three-dimensional MR angiography at 1.5 T. Images were reviewed by a single radiologist blinded to conventional angiographic findings who evaluated each image for the size, number, and location of PAVMs, as well as for the size and number of feeding arteries. Five patients underwent conventional angiography with embolization therapy, and one patient underwent lobectomy. Two patients did not undergo either surgery or angiography.

RESULTS: Three-dimensional MR angiography revealed nine (90%) of 10 PAVMs that were confirmed at conventional angiography (n = 9) or examination of a surgical specimen (n = 1). The single PAVM that was not identified prospectively at MR angiography was small (3–4 mm) and peripheral. Two additional PAVMs were identified in the two patients who did not undergo surgery or angiography.

CONCLUSION: Three-dimensional MR angiography is a promising technique for use in the diagnosis of PAVM, although small (<5-mm) PAVMs may be more difficult to identify with the technique. The technique is a particularly useful means of noninvasively demonstrating the size and number of feeding arteries prior to treatment.

Index terms: Angiography, 60.1241 • Arteriovenous malformations, pulmonary, 60.1494 • Lung, MR, 60.121411, 60.121412 • Magnetic resonance (MR), vascular studies, 60.121412, 60.12142, 60.12143


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Pulmonary arteriovenous malformations (PAVMs) are the result of abnormal communication between pulmonary arteries and pulmonary veins. Although PAVMs can result from trauma, they are most often congenital. Approximately 70% of PAVMs are associated with hereditary hemorrhagic telangiectasia, also known as Rendu-Osler-Weber syndrome (1). Hereditary hemorrhagic telangiectasia has an autosomal dominant transmission pattern, with an estimated prevalence of approximately one in 40,000 to one in 2,000 (1).

Large PAVMs may manifest early in life with cyanosis or congestive heart failure. More often, however, patients develop symptoms between the 4th and 6th decades (2). The presence and severity of symptoms are correlated with size of the PAVM (2). Typically, a solitary PAVM less than 2 cm is asymptomatic; multiple lesions are more frequently symptomatic (2). The most common symptoms include dyspnea and hemoptysis.

Although pulmonary angiography remains the standard for the evaluation of PAVM (2,3), it remains an invasive procedure with associated, albeit small, rates of morbidity and mortality. The purpose of our study was to determine whether three-dimensional (3D) gadolinium-enhanced magnetic resonance (MR) angiography could be used to identify PAVMs and to accurately identify the size and number of feeding arteries.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Patient Population
By using a computerized search of radiology reports, all patients being evaluated with MR imaging of the chest for PAVMs between January 1995 and December 1998 were identified. Eight patients (five male, three female; mean age, 38.9 years; age range, 17–73 years) were referred because findings at chest radiography or at chest CT were suggestive of PAVMs. (These findings were later shown to indeed represent PAVMs.)

All patients underwent MR examination of the chest, as described later. Five patients subsequently underwent conventional pulmonary angiography to confirm the presence of PAVM, as well as to provide embolization therapy (mean, 29 weeks; range, 1–130 weeks following MR imaging). Of the three patients who did not undergo angiography, one subsequently underwent lobectomy 3 weeks following MR examination for confirmation and treatment of the PAVM. The remaining two patients did not undergo further evaluation or treatment. A family history of hereditary hemorrhagic telangiectasia was known in two patients.

Imaging Techniques
All MR images were obtained with a 1.5-T magnet (Signa; GE Medical Systems, Milwaukee, Wis). Imaging was performed with patients in the supine position by using a surface coil and both cardiac and respiratory gating. All patients underwent multiplanar imaging with T1-weighted gradient-echo sequences, as well as conventional fast spin-echo or single-shot T2-weighted sequences.

Seven of the eight patients also underwent 3D volumetric gadolinium-enhanced MR angiography; one patient underwent imaging in 1995, prior to adoption of this technique into our standard protocol. While our 3D contrast-enhanced MR angiographic sequence was modified slightly during the study period, the following represents the sequence used in the majority of our patients. The contrast material–enhanced studies were performed by using a 3D dynamic fast spoiled gradient-echo sequence performed in the coronal plane (<7.4/<2.5 [repetition time msec/echo time msec], 10°–40° flip angle, 26–44 partitions, 4.0–4.4-mm section thickness reconstructed to 2.0–2.2 mm [x2 zero fill interpolation]). The matrix used was 256–512 in the frequency-encoding direction and 128–160 in the phase-encoding direction. A bandwidth of 64 kHz was used, and one-half to one signal was acquired. Contrast material (gadopentetate dimeglumine [Magnevist]; Berlex Laboratories, Wayne, NJ, or gadodiamide [Omniscan]; Sanofi Winthrop Pharmaceuticals, New York, NY; 0.1–0.2 mmol per kilogram of body weight) was injected rapidly by hand, followed by a saline flush. A timing bolus was not administered. Rather, MR angiography was initiated by the physician immediately following rapid bolus injection into an 18-gauge antecubital intravenous angiographic catheter. Fat saturation was performed by using a spectrally fat-selective inversion pulse (inversion time, 27 msec).

All images and angiograms were interpreted prospectively by radiologists who had knowledge of the clinical history and who suspected the presence of PAVMs. Prospectively, only the size of the PAVM and the number of feeding vessels were typically reported. For our retrospective analysis, images were reinterpreted by a single radiologist (E.S.S.) who was blinded to the patients’ conventional angiographic findings (Fig 1). The raw coronal data set for each MR angiogram was reviewed, as were maximum intensity projection images. No patients underwent conventional angiography prior to MR imaging. Images were evaluated for the size and number of PAVMs, as well as for the number of feeding arteries.



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Figure 1a. (a) Coronal 3D gadolinium-enhanced maximum intensity projection gradient-echo MR arteriogram (6.0/1.0) demonstrates a small PAVM (solid arrow) in the superior segment of the left lower lobe, with a feeding artery (large open arrow) and a draining vein (small open arrow). Note that differentiation between arteries and veins is difficult on this maximum intensity projection image, but it is easily performed on images of the raw data. (b) Conventional selective pulmonary MR angiogram findings confirm the presence of a feeding artery (large arrow) and a draining vein (small arrow).

 


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Figure 1b. (a) Coronal 3D gadolinium-enhanced maximum intensity projection gradient-echo MR arteriogram (6.0/1.0) demonstrates a small PAVM (solid arrow) in the superior segment of the left lower lobe, with a feeding artery (large open arrow) and a draining vein (small open arrow). Note that differentiation between arteries and veins is difficult on this maximum intensity projection image, but it is easily performed on images of the raw data. (b) Conventional selective pulmonary MR angiogram findings confirm the presence of a feeding artery (large arrow) and a draining vein (small arrow).

 
In patients who underwent thoracic computed tomography (CT), a routine volumetric 7-mm helical image (pitch of 1.5) was obtained from the thoracic inlet to the adrenal glands during the arterial phase of enhancement (Fig 2). A contrast agent (diatrizoate meglumine [Hypaque 60%]; Nycomed, Princeton, NJ; 100 mL), administered with an injection rate of 2 mL/sec, was used.



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Figure 2a. (a) Coronal 3D gadolinium-enhanced maximum intensity projection gradient-echo MR arteriogram (6.0/1.0) shows a 5-cm PAVM (*) in the right lower lobe, with a solitary feeding artery (small solid arrow) and a draining vein (large solid arrow). A small 3-4-mm PAVM in the posterior peripheral right lower lobe (open arrow), which was not identified prospectively, is also present. (b) Conventional selective pulmonary angiogram obtained after coil embolization of the 5-cm PAVM (open arrow) reveals a 3-4-mm PAVM (solid arrow). (c) Transverse contrast-enhanced CT image shows the peripheral location of this small PAVM (arrow), which was not identified prospectively, that resides deep within the posterior sulcus.

 


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Figure 2b. (a) Coronal 3D gadolinium-enhanced maximum intensity projection gradient-echo MR arteriogram (6.0/1.0) shows a 5-cm PAVM (*) in the right lower lobe, with a solitary feeding artery (small solid arrow) and a draining vein (large solid arrow). A small 3-4-mm PAVM in the posterior peripheral right lower lobe (open arrow), which was not identified prospectively, is also present. (b) Conventional selective pulmonary angiogram obtained after coil embolization of the 5-cm PAVM (open arrow) reveals a 3-4-mm PAVM (solid arrow). (c) Transverse contrast-enhanced CT image shows the peripheral location of this small PAVM (arrow), which was not identified prospectively, that resides deep within the posterior sulcus.

 


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Figure 2c. (a) Coronal 3D gadolinium-enhanced maximum intensity projection gradient-echo MR arteriogram (6.0/1.0) shows a 5-cm PAVM (*) in the right lower lobe, with a solitary feeding artery (small solid arrow) and a draining vein (large solid arrow). A small 3-4-mm PAVM in the posterior peripheral right lower lobe (open arrow), which was not identified prospectively, is also present. (b) Conventional selective pulmonary angiogram obtained after coil embolization of the 5-cm PAVM (open arrow) reveals a 3-4-mm PAVM (solid arrow). (c) Transverse contrast-enhanced CT image shows the peripheral location of this small PAVM (arrow), which was not identified prospectively, that resides deep within the posterior sulcus.

 
Selective screen-film pulmonary angiography was performed by full-time interventional radiologists (including R.A.B.). Anteroposterior and oblique views were obtained in each lung by using injection rates ranging from 20 to 40 mL/sec. For each PAVM identified, size measurements of all feeding arteries, as well as measurements of the malformation itself, were reported prospectively. All measurements were adjusted by 20% to account for estimated magnification.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Of eight patients who underwent 3D MR angiography, five subsequently underwent conventional pulmonary angiography (Table). Nine PAVMs were prospectively identified at conventional angiography in these five patients, eight of which were identified at MR imaging (both prospectively and retrospectively). The single lesion that was missed at MR imaging by both the prospective and blinded retrospective readers was 3–4 mm and subpleural. This lesion was also missed prospectively at contrast-enhanced CT because of its small size and of its location deep within the posterior sulcus. Retrospectively, the lesion was present at CT and was apparent, but subtly, at MR imaging, when its location was revealed at angiography. There were no false-positive lesions identified at MR imaging. All five patients who underwent pulmonary angiography also underwent coil embolization as definitive treatment of eight PAVMs.


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Size, Location, Feeding Arteries to, and Treatment of PAVM
 
One patient was treated with lobectomy, the findings of which confirmed the presence of a single PAVM as identified at MR imaging. No other PAVMs were identified in the resected lobe, which was otherwise reported to represent normal lung. The remaining two patients did not undergo angiography or surgery for confirmation or treatment of the two additional PAVMs (one each) identified at MR imaging.

MR angiography revealed supplying arteries to all nine angiographically confirmed PAVMs. The mean number of feeding arteries was 1.8 (range, 1–3 feeding arteries) per PAVM. The size of the feeding arteries ranged from 2 to 22 mm in diameter, with a mean of 13 mm. Three-dimensional MR angiography reliably demonstrated feeding arteries that were larger than 3 mm, but two vessels were missed that were 2 and 3 mm in diameter, as estimated at conventional angiography.


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Because PAVMs are found in up to 30% of patients carrying the hereditary hemorrhagic telangiectasia gene and because these lesions can lead to high-output congestive failure and paradoxical emboli, an accurate noninvasive method of screening for these lesions is needed (4). Although some patients will present after paradoxical emboli, many patients remain asymptomatic. Screening is typically and initially performed with posteroanterior and lateral chest radiography, followed by helical CT of the chest to better characterize any lesions (3,5). Detection and localization of PAVMs facilitates planning of further interventions. Specifically, knowledge of the size and number of feeding arteries is helpful in preembolization planning. If the feeding artery is greater than 3 mm in diameter, patients may undergo diagnostic pulmonary angiography and embolization (4).

Early studies (68) in which the role of thoracic MR imaging was evaluated revealed low signal intensity, or so-called flow voids, in PAVMs when they were studied with a conventional spin-echo technique. However, larger lesions, particularly those with peripheral thrombus or slow flow, may demonstrate low to intermediate signal intensity on images obtained with such sequences. Furthermore, a variety of lesions, including air cysts, calcified lesions, or chronic hematomas, can cause low signal intensity on spin-echo images (9).

Several techniques were subsequently developed that improved MR imaging sensitivity to flow states. One such technique involved use of a gated MR technique with reconstructed phase images, which helped in the discrimination of flowing blood, such as that in a PAVM, from stationary tissues, such as in a hematoma or solid nodule (9). Subsequent investigators (10) introduced the gradient-recalled-echo technique, which showed dramatically higher sensitivity to blood flow, even with slow-flow states. Unfortunately, the gradient-recalled-echo technique was also limited by potential false-positive results, as was the conventional spin-echo technique. Specifically, mucus, atelectasis, and various stages of thrombus may appear hyperintense on gradient-recalled-echo images, incorrectly suggesting PAVM (11).

Three-dimensional contrast–enhanced MR angiography has become the MR technique of choice for imaging vascular structures in the thorax (1215). The application of 3D MR angiography to the depiction of PAVMs has received little attention in the literature (16). We have described the evaluation of eight patients with this technique for the identification and characterization of 12 separate PAVMs.

One angiographically proved PAVM was prospectively missed at MR imaging. However, this lesion was 3–4 mm in size and deep within the posterior sulcus. PAVMs smaller than 5 mm may be difficult to resolve with MR imaging, particularly if they are peripherally located, given the difficulties of cardiac and respiratory motion and the susceptibility artifacts related to aerated lung parenchyma. Furthermore, the feeding artery to this PAVM was only 1–2 mm in diameter and was smaller than arteries typically treated with embolization. It was not possible to selectively catheterize the feeding vessel in this case, and, hence, the lesion was left untreated. Although this small lesion was not identified prospectively, in retrospect the lesion was present at both CT and MR examinations. MR angiography consistently revealed feeding arteries that were 4 mm or greater in diameter. There were no false-positive diagnoses of PAVM in those patients who subsequently underwent conventional angiography for definitive diagnosis.

In conclusion, MR angiography is a promising technique for the evaluation of PAVM. Three-dimensional MR angiography allows for the identification of not only the PAVM but also the size and number of supplying arteries.


    FOOTNOTES
 
Abbreviations: PAVM = pulmonary arteriovenous malformation, 3D = three-dimensional

Author contributions: Guarantor of integrity of entire study, D.D.M.; study concepts and design, D.D.M., E.S.S.; definition of intellectual content, D.D.M., E.S.S.; literature research, all authors; clinical studies, all authors; data acquisition and analysis, D.D.M., E.S.S.; statistical analysis, D.D.M.; manuscript preparation, D.D.M., E.S.S.; manuscript editing and review, all authors; manuscript final version approval, E.S.S.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Guttmacher AE, Marchuk DA, White RI, Jr. Hereditary hemorrhagic telangiectasia. N Engl J Med 1995; 333:918-924.[Free Full Text]
  2. Dines DE, Arms RA, Bernatz PE, Gomes MR. Pulmonary arteriovenous fistulas. Mayo Clin Proc 1974; 49:460-465.[Medline]
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  5. Remy J, Remy-Jardin M, Wattinne L, Deffontaines C. Pulmonary arteriovenous malformations: evaluation with CT of the chest before and after treatment. Radiology 1992; 182:809-816.[Abstract/Free Full Text]
  6. Webb WR, Gamsu G, Golden JA, Crooks LE. Nuclear magnetic resonance of pulmonary arteriovenous fistula: effects of flow. J Comput Assist Tomogr 1984; 8:155-157.[Medline]
  7. Gutierrez FR, Glazer HS, Levitt RG, Moran JF. NMR imaging of pulmonary arteriovenous fistulae. J Comput Assist Tomogr 1984; 8:750-752.[Medline]
  8. Gefter WB. Chest applications of magnetic resonance imaging: an update. Radiol Clin North Am 1988; 26:573-588.[Medline]
  9. Brown JJ, Gilbert T, Gamsu G, Golden JA, Higgins CB. MR imaging of low signal intensity pulmonary lesions using flow-sensitive techniques. J Comput Assist Tomogr 1988; 12:560-564.[Medline]
  10. Dinsmore BJ, Gefter WB, Hatabu H, Kressel HY. Pulmonary arteriovenous malformations: diagnosis by gradient-refocused MR imaging. J Comput Assist Tomogr 1990; 14:918-923.[Medline]
  11. Silverman JM, Julien PJ, Herfkens RJ, Pelc NJ. Magnetic resonance imaging evaluation of pulmonary vascular malformations. Chest 1994; 106:1333-1338.[Abstract/Free Full Text]
  12. Krinsky GA, Rofsky NM, DeCorato DR, et al. Thoracic aorta: comparison of gadolinium-enhanced three-dimensional MR angiography with conventional MR imaging. Radiology 1997; 202:183-193.[Abstract/Free Full Text]
  13. Ho VB, Prince MR. Thoracic MR aortography: imaging techniques and strategies. RadioGraphics 1998; 18:287-309.[Abstract]
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  16. Vrachliotis TG, Bis KG, Kirsch MJ, Shetty AN. Clinical note: contrast-enhanced MRA in pre-embolization assessment of a pulmonary arteriovenous malformation. J Magn Reson Imaging 1997; 7:434-436.[Medline]



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