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Anatomical and functional evaluation of the cardiovascular system in Marfan syndrome

Nollen, G.J.

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Citation for published version (APA):Nollen, G. J. (2004). Anatomical and functional evaluation of the cardiovascular system in Marfan syndrome.

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Download date: 15 Jun 2020

CHAPTER R

Magneti cc resonanc e imagin g of the main pulmonar yy artery : reliabl e assessmen t of

dimension ss in Marfan patient s on a simpl ee axial spin echo image

Gijss J. Nollen1, Klaartje E. van Schijndel1, Janneke Timmermans3, Maartenn Groenink1, Jelle O. Barentsz4, Ernst E. van der Wall5,

Jaapp Stoker2, Barbara J.M. Mulder1

Fromm the Departments of Cardiology1 and Radiology2 of the Academic Medical Center,, Amsterdam, the Departments of Cardiology3 and Radiology4 of the

Universityy Medical Center St Radboud, Nijmegen and the Department of Cardiology55 Leiden University Medical Center, The Netherlands

Thee International Journal of Cardiovascular Imaging 2003:19:141-147

Abstrac t t Objective : :

Too investigate if a simple axial spin echo (SE) image can be used for reliable assessment

off pulmonary artery dimensions in patients with Marfan syndrome.

Methods : :

Fiftyy Marfan patients (mean age 33 (10 years; 34 men, 16 women) and 15 normal

subjectss (mean age 28 4 years; 9 men, 6 women) underwent cardiac magnetic resonance

imagingg (MRI). Pulmonary artery dimensions were obtained on axial spin echo images at

twoo different levels: 1) the level of the pulmonary artery root, and 2) the level of the

pulmonaryy artery bifurcation. To evaluate the accuracy of axial plane measurements 10

Marfann patients also underwent contrast enhanced MR angiography (CE-MRA).

Results: :

Inn the 10 Marfan patients who also underwent CE-MRA, the mean diameter at the

pulmonaryy bifurcation assessed with CE-MRA (31.5 3.6 mm) was almost equal to mean

diameterr assessed with axial SE (30.7 6 mm). Agreement of methodology according

too Bland and Altman analysis showed a 95% confidence interval ranging from -2.6 to +

4.44 mm for all distances of the pulmonary artery root. In Marfan patients the mean right-

leftt diameter measured on both axial SE images and CE-MRA was approximately 2.5 mm

largerr than the anterior-right and anterior-left diameters (p<0.001).

Conclusions: :

Axiall SE MR imaging is a reliable and easy acquisition to measure pulmonary artery

dimensionss in patients with Marfan syndrome, and could be used for follow-up, especially

inn patients with severe involvement of the cardiovascular system. Not only the pulmonary

arteryy trunk but also the asymmetric pulmonary root should be measured, although the

clinicall relevance of the asymmetric root is not yet known.

Introductio n n Thee Marfan syndrome is an autosomal dominant inherited disorder of connective tissue

withh variable manifestations in primarily skeletal, ocular and cardiovascular organ

systems1.. Diagnosis is based on a combination of major and minor clinical features

classifiedd in 1986 (Berlin nosology) and revised by an experts'consensus (Ghent nosology

1996)2'3.. Although dilatation of the main pulmonary artery is a criterion for establishing

diagnosis,, until recently little was known about the pulmonary artery in Marfan syndrome.

Sincee normal values for the pulmonary artery diameter were not available at that time, it

wass advised in the Ghent criteria to detect dilatation provisionally by echocardiography,

computedd tomography (CT) or magnetic resonance imaging (MRI) using nomograms for

thee aorta3-4.

Normall values for pulmonary artery bifurcation have been assessed from axial scans in a

smalll number of patients510. In a very recent study, it was shown that in normal subjects,

ass well as in Marfan patients, dimensions measured at the pulmonary artery root were

significantlyy larger than dimensions measured at the pulmonary artery bifurcation on

axiall SE MR images11. In that study, it was also shown that Marfan patients had significantly

largerr pulmonary artery dimensions than normal subjects.

Simplee assessment of pulmonary artery diameters is useful in individuals who are referred

forr screening on the Marfan syndrome and for follow-up of Marfan patients. With the

increasedd survival of patients with aortic complications, pulmonary artery dilatation might

becomee of clinical relevance in the future11.

Thee aim of the present study was to investigate if a simple axial spin echo (SE) image can

bee used for reliable assessment of pulmonary artery dimensions in patients with Marfan

syndrome. .

Method s s Studyy population

Fiftyy consecutive Marfan patients (mean age 33 10 years; 34 men, 16 women) underwent

routinee cardiac MR imaging in the Academic Medical Center, Amsterdam and the

Universityy Medical Center St Radboud, Nijmegen. Diagnosis of Marfan syndrome had

beenn established according to the Ghent Criteria3. Thirty-five patients had undergone an

aorticc root replacement. Pulmonary artery dilatation had not been previously diagnosed

inn any of the patients with Marfan syndrome, nor did they have a history of left-right

shunt,, pulmonary arterial hypertension, or pulmonary or tricuspid valvular regurgitation.

Thee normal group consisted of 15 age-and-sex matched healthy subjects (mean age 28

44 years; 9 men, 6 women). The study was approved by the local ethical committee and

individuall oral and written informed consent was obtained in each patient.

Magneticc resonance imaging and analysis Imagingg was performed on a Siemens Magnetom Vision 1.5 Tesla MR system (Siemens

Medicall Systems, Erlangen, Germany). The aorta was imaged in axial and oblique sagittal

planess using a standard ECG-gated Tl -weighted spin echo (SE) sequence. Repetition

timee equalled the R-R interval, echo time was 12 ms, imaging matrix was 256 x 256,

fieldd of view 350 mm, slice thickness was 6-8 mm and there was a slice gap depending

onn patient size with a maximum of 0.5 mm. Typical acquisition time was 4-5 minutes

dependingg on the R-R interval. Additional conventional breath-hold contrast-enhanced-

3DD gradient-echo MR angiography (CE-MRA) was performed in 10 patients. Repetition

timee was 4.60 ms, echo time 1.80 ms, flip angle , imaging matrix was 512 x 512, field

off view 500 mm and there was no slice gap.

Forr analysis the MR imaging software tool MASS® (Medis, Leiden, The Netherlands) was

used.. Two trained observers who reached a consensus on each measurement performed

alll measurements.

Measurementt of main pulmonary artery and accuracy of measurements

Mainn pulmonary artery dimensions were assessed on axial SE images at two levels: 1) the

levell of the pulmonary artery root, and 2) the level of the pulmonary artery bifurcation.

Thee region of the ascending aorta and pulmonary artery was magnified to full screen

size.. Pulmonary sinuses were named by their relationship to the aortic valve: right, left

andd anterior (nonseptal)12. Three distances were obtained from the inner contours of the

pulmonaryy artery root according to the aortic root measurements by Meijboom et al.13:1)

fromm the anterior to the right sinus, 2) from the anterior to the left sinus, and 3) from the

rightt to the left sinus. Figure 1 shows a representative image demonstrating the two levels

att which the main pulmonary artery was measured.

Too evaluate the accuracy of axial plane measurements, in 10 patients who also underwent

CE-MRA,, the pulmonary artery was reconstructed double oblique using multi planar

reconstructionn (Figure 2). The pulmonary root was measured in the three defined directions.

Thee pulmonary artery bifurcation diameter was assessed perpendicular to the pulmonary

trunkk just proximal to the bifurcation. To assess partial volume effects on axial SE images,

correlationn between angle of the pulmonary root in the coronal and sagittal plane and

thee distances measured on axial planes were investigated.

Figur ee 1 Levels of measurement on axial SE planes in a Marfan patient: (A - D) is from cranial to caudal:: (B) main pulmonary artery diameter measurement at the level of pulmonary artery bifurcation, (D)) pulmonary artery root measurements: anterior-right diameter, anterior-left diameter and right-left diameter. .

a a 10 0

39 9

Figur ee 2 CE-MRA of the pulmonary artery. (A): Level of the main pulmonary artery diameter measurementt at the level of pulmonary artery bifurcation. (B): image used for multiplanar reconstruction. C:: image perpendicular to the pulmonary artery root. Ant.= anterior.

3 3 a. a.

en n c c

c c ro ro c c O O

Statistics s

Dataa are given as mean SD. Differences between the groups were assessed by the

unpairedd Student's f test. The statistical analysis was performed wi th the SPSS statistical

packagee (SPSS Inc, Chicago, Illinois, USA). The level of significance was set at p < 0.05.

Results s Alll main pulmonary artery dimensions measured on axial SE planes in normal subjects

andd Marfan patients are shown in Figure 3.

Inn the 10 Marfan patients who also underwent CE-MRA, the mean diameter at the

pulmonaryy bifurcation assessed with CE-MRA (31.5 3.6 mm) was almost equal to mean

diameterr assessed with axial SE (30.7 3.6 mm). Agreement of methodology according

too Bland and Altman analysis showed a 9 5 % confidence interval ranging from -2 .6 to +

4.44 mm for all distances of the pulmonary artery root (Figure 4).

40 0

54 4 52 2 50 0 48 8 46 6 44 4 42 2 400 -38 8 36 6 344 -322300 -28 8 26 6 24 4 22 2 20 0 18 8

P<0.0011 P<0.001 P<0.001 P<0.001

> >

'i 'i

control l Marfan n

Figur ee 3 Meann diameters of the main pulmonary arteryy in normal subjects and in Marfan patientss measured on axial SE images

A - R R L - A A

< < 5 5

10 0

2 2 0 0

-2 2 -4 4 -6 6 -8 8

-10 0

oo 99

u oo p oo oo o o

—nz—nz O O ^ o o o o

255 30 35 40 45 averagee diameter (mm)

50 0

Figuree 4 Blandd Altman analysis. Differences betweenn measurements of distances of thee pulmonary artery root on CE-MRA andd on axial SE planes against their means,, dotted lines indicate 95% confidencee interval.

Thee mean angle of the pulmonary artery root measured on oblique sagittal planes was 33

degreess (range 20 - 42) and was not different in normal subjects and Marfan patients. No

correlationn between this angle and the difference between anterior-right and right-left

diameterr was found. The angle measured on coronal planes was minimal and never

exceededd six degrees.

Inn contrast to normal subjects in whom the three diameters of the pulmonary artery root

weree not different, in Marfan patients the mean right-left diameter measured on both

axiall SE images and CE-MRA was approximately 2.5 mm larger than the anterior-right

andd anterior-left diameters (p<0.001) (Figure 3). The anterior-right diameter appeared to

bee the direction that, measured on both axial SE images and CE-MRA, showed the smallest

differencee and the smallest variability between the two MR sequences compared to the

anterior-leftt and right-left diameters (Figure 5).

AA good correlation was found between pulmonary artery and aortic root diameter in

non-operatedd Marfan patients (Figure 6).

QJJ < i tt o£

UJ J

U U

5.0 0

2.5--

0.0--

-2.5 5

-5.0 0

T T '' T

P = ^ ^

"l — —

A-RR diameter L-A diameter R-Ldiameter

Figuree 5 Differencee between pulmonary artery roott measurements on MRA and on axiall SE plane for the three directions. Boxess extend from the 25th to the 75th percentile,, with a horizontal line at the medianmedian (50th percentile). Whiskers extendd down to the smallest value and upp to the largest.

Q. .

41 1

600 -I

555

500

45 5

40 0

35 5

30 0

25 5

20 0 20 0 255 30 35 40 45

pulmonaryy root diameter (mm)

Figur ee 6 Correlationn between pulmonary artery roott diameter and aortic root diameter in 155 non-operated Marfan patients.

c c o o _E E 3 3 Q--

C C

O O Dl l C C O) )

Discussion n Inn the present study it was shown that diameters measured on axial SE images were not

significantlyy different from diameters measured after double-oblique reconstruction on

CE-MRAA at both the pulmonary artery root and bifurcation. It was also shown that in

Marfann patients the mean right-left diameter of the pulmonary artery root measured on

bothh axial SE images and CE-MRA was approximately 2.5 mm larger than the anterior-

rightt and anterior-left diameters.

Comparingg imaging methods

Thee available methods to image the pulmonary arteries include color-Doppler-

echocardiography,, pulmonary angiography, CT and MR imaging. In this study we

comparedd SE with CE-MRA for several reasons. Color-Doppler-echocardiography is limited

byy only being able to depict the intramediastinal course of the vessels14. Pulmonary

angiographyy was thought to be the "gold standard" for the measurement of pulmonary

artery.. However its invasive nature carries a small risk of morbidity and mortality15-16.

Comparedd with both CT and pulmonary angiography, CE-MRA is a noninvasive imaging

techniquee for assessing great vessels and pulmonary vessels without the need for ionizing

radiationn or iodinated contrast material1718.

Accuracyy of measurements

Diameterss of the pulmonary artery measured at both levels corresponded very well between

thee two methods (SE and CE-MRA). Although the axial SE images were not perpendicular

too the pulmonary root and partial volume effects could be expected, these effects did not

influencee the accuracy of measurement, since no significant correlation between angles

off the pulmonary root measured in the oblique sagittal plane and difference between

diameterss was found. 42 2

Measurementt of main pulmonary artery

Inn Marfan patients the mean right-left diameter measured on both axial SE images and

CE-MRAA images was approximately 2.5 mm larger than the anterior-right and anterior-

leftt diameters (p<0.001). Asymmetry of the main pulmonary artery, observed in this study,

hass also been described by Sloth et al., as it has been shown for the aortic root by various

authors13-19-20.. Further follow-up studies are needed to examine the clinical significance

off the asymmetric pulmonary root.

Pulmonaryy artery dilatation and aneurysms are rare pathologic conditions that may be

causedd by congenital heart disease, infection, pulmonary hypertension and are

occasionallyy idiopathic2126. In 1947 Deterling et al. reviewed 109.571 autopsy studies

andd concluded that only eight cases of pulmonary artery aneurysms had been

documented27.. Until now, only two cases of pulmonary artery dissection in Marfan

syndromee have been reported28,29. One case report of pulmonary artery dissection in

bovinee Marfan syndrome has been described30.

AA uniform approach for pulmonary aneurysm is not yet available, because little is known

aboutt natural history and long-term outcome following medical or surgical treatment.

Somee investigators argue that surgical repair is recommended when an aneurysm is

discovered3132.. Others believe that surgery should only be considered for large aneurysms

iff the patient has an acceptably low operative risk22.

Inn a recent study it was suggested that dilatation of the pulmonary root increased with

progressivee involvement of the cardiovascular system in Marfan patients. Although main

pulmonaryy artery aneurysm and dissection have been reported only rarely in the past,

theyy could become of more clinical relevance in the near future because of increased

longevityy in Marfan patients11.

Conclusion s s Axiall SE MR imaging is a simple and reliable acquisition method to measure pulmonary

arteryy dimensions in patients with Marfan syndrome, and could be used for follow-up,

especiallyy in patients with severe involvement of the cardiovascular system. Not only the

pulmonaryy artery trunk, but also the asymmetric pulmonary root should be measured,

althoughh the clinical relevance of the asymmetric root is not yet known.

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