Download Individual pulmonary vein imaging by transthoracic

European Journal of Echocardiography (2008) 9, 655–660
doi:10.1093/ejechocard/jen032
Individual pulmonary vein imaging by transthoracic
echocardiography: an inadequate traditional
interpretation
Xinsheng Huang*, Yigao Huang, Tao Huang, Wenhui Huang, and Zhendong Huang
Received 24 August 2007; accepted after revision 9 January 2008; online publish-ahead-of-print 19 February 2008
KEYWORDS
Echocardiography;
Pulmonary vein;
Angiography
Aims There existed an ambiguity in the current echo literature about the identification of the pulmonary veins imaged by echocardiography. This study was designed to identify the site and blood flow of
individual pulmonary veins by transthoracic echocardiography.
Methods and results Transthoracic echocardiography was used to display individual pulmonary veins in
the apical and parasternal short-axis views in 20 adult patients with atrial septal defect. Cardiac catheterization, selective angiography, and contrast echocardiography were used to identify and validate the
exact site of individual pulmonary veins. The right lower and upper veins were best seen in the apical
four-chamber and the near apical five-chamber views, respectively. Both left pulmonary veins were best
displayed in the parasternal short-axis view. When all the individual pulmonary veins were seen simultaneously in the apical views, from left to right of the sector, they were the right upper, right lower, left
lower, and left upper pulmonary veins, respectively.
Conclusion This prospective study provides a feasible method to prove that transthoracic echocardiography can visualize clearly and identify accurately the exact site of each pulmonary vein. The information should be helpful to study various pulmonary venous diseases.
Introduction
Methods
There has been potential difficulty in visualizing the four
pulmonary veins by transthoracic echocardiography. The
important factors against their imaging are the veins being
located in the far field and outside cardiac structures. Up
to now, no controlled study has been carried out to identify
the individual pulmonary veins. Previous viewpoint in textbooks1,2 or literatures3–8 may be a subjective judgement
and is not validated by other imaging techniques. Therefore,
we have reason to suspect and search for an appropriate
method to validate the exact site of individual pulmonary
veins so as to prevent echocardiographic misinterpretation.
Using cardiac catheterization, selective pulmonary vein
angiography, and contrast echocardiography as control,
this prospective study was designed to prove our hypothesis
and to identify the site and blood flow of individual pulmonary veins by transthoracic echocardiography in adult
patients with atrial septal defect (ASD).
Study patients
* Corresponding author. Tel: þ8620 83827812 10260; fax: þ8620 83875453.
E-mail address: [email protected]
In this study, 20 consecutive adult patients (4 men and 16 women,
aged 20–57 years, mean 37) with ostium secundum ASD and significant left-to-right shunt were referred to our institute from September 2006 to February 2007. During their hospitalization, they
underwent cardiac catheterization, pulmonary vein angiography,
contrast echocardiography, and/or transcatheter closure. Patients
were stratified by New York Heart Association functional classification (class I–IV). Written informed consent was obtained from
all patients.
Echocardiography
Clinical echocardiograms were obtained in all subjects in the left
lateral decubitus position by an experienced sonographer using an
Acuson Sequoia C256 (Acuson, Mountain View, CA, USA) echocardiographic imaging system equipped with a 2.0–3.5 MHz transducer. An
ECG was recorded and displayed simultaneously on the image. With
the use of Doppler colour flow as a guide, right lower pulmonary
vein (RLPV) and right upper pulmonary vein (RUPV) were shown in
the apical views and left upper and lower ones in the parasternal
short axis and/or the apical four-chamber views. The right
Published on behalf of the European Society of Cardiography. All rights reserved. & The Author 2008.
For permissions please email: [email protected].
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Department of Cardiovascular Medicine, Guangdong Provincial People’s Hospital, No. 106 Zhongshan 2 Road,
Guangzhou 510080, China
656
pulmonary venous blood flow velocity was measured by placing the
sample volume 1 cm upstream in the RUPV and RLPV.
All echocardiographic data were stored digitally on magneto-optical
disk for subsequent off-line analysis.
X. Huang et al.
Table 1 Data of the study of echocardiography and
catheterization in all patients
Sex
Age
RLPV
Vmax
(m/s)
RUPV
Vmax
(m/s)
PAP (mmHg)
S(D/M)
Qp/Qs
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
F
F
F
F
F
F
M
F
F
M
F
M
F
F
F
F
M
F
F
F
40
20
26
51
20
38
37
36
26
57
22
50
42
56
54
49
53
29
22
28
0.61
0.61
0.65
0.72
0.79
0.79
0.48
0.74
0.62
0.65
0.79
0.60
0.74
0.78
0.89
0.62
0.78
0.83
0.76
0.58
0.65
0.73
0.71
0.93
1.13
0.76
0.57
1.08
0.61
0.58
0.74
0.67
0.88
0.64
0.83
0.72
0.91
0.72
0.86
0.88
32 (9/23)
40 (13/21)
32 (11/19)
38 (14/22)
26 (8/17)
40 (13/26)
32 (9/19)
32 (10/22)
36 (11/22)
39 (9/21)
49 (16/32)
50 (13/33)
59 (20/38)
41 (11/22)
75 (37/51)
76 (31/48)
53 (16/31)
28 (8/18)
31 (11/19)
34 (11/18)
1.4
2.1
3.2
3.0
1.8
1.5
1.7
2.3
2.8
2.5
2.7
2.1
2.2
1.8
1.6
1.9
2.2
2.1
2.0
1.9
Catheterization evaluation and pulmonary
vein angiography
All patients were in the supine position in catheterization laboratory. Each procedure was performed with patients staying awake
under local anaesthesia. Access was obtained through the right
femoral vein and artery. Each patient was given intravenous injection of 3000 U of heparin, whose pressures and oxygen saturations
of right and left heart chambers were obtained through cardiac
catheterization. Pulmonary (Qp) and systemic (Qs) blood volume
flow and shunt fraction (Qp/Qs) were calculated. The left atrium
(LA) was entered through the ASD. Contrast angiogram was done
by hand injection of a contrast agent through the catheter to identify the site of each pulmonary vein in the postero-anterior view of a
chest radiograph.
Contrast echocardiography
After identification of the site of each pulmonary vein with the
angiogram, the catheter was kept in the same position and agitated
saline of 8 mL was injected by hand into each vein to visualize
its site and running by contrast echocardiography. Contrast
echocardiogram was obtained in the supine position by an experienced sonographer using a GE Vingmed Vivid Seven machine with
a 1.7–3.4 MHz multifrequency transducer. An ECG was recorded
and displayed simultaneously on the image. With the use of
Doppler colour flow as a guide, contrast echocardiogram of RUPV
and RLPV was shown in the apical views, whereas that of left
upper and lower ones was shown in the parasternal short-axis
view. All echo data were dealt with as mentioned earlier.
D, diastolic; M, mean; PAP, pulmonary artery pressure; Qp/Qs,
pulmonary-to-systemic blood flow ratio; RLPV, right lower pulmonary
vein; RUPV, right upper pulmonary vein; S, systolic; Vmax, maximal
blood flow velocity.
Statistical analysis
All data were presented as mean+SD. Statistical differences of two
groups were calculated and analysed using the paired Student’s
t-test. Statistical significance is set at P-value ,0.05.
Results
Echocardiography
The data of the study of echocardiography and catheterization in all patients were summarized in Table 1. The proximal portion of the RLPV in the apical four-chamber view
was seen draining into the LA almost perpendicular to its
posterior aspect, and the blood flow of the vein was virtually
parallel to ultrasound beam and atrial septum (Figure 1,
left). Visualization of the RUPV made it necessary to tilt
the transducer slightly anteriorly in the apical four-chamber
view, when a portion of the left ventricular outflow tract
could also be seen. Namely, lying between the apical fourand five-chamber views or near apical five-chamber view
was used, which entered, in a tilting position, the right
postero-medial aspect of the LA (Figure 1, right). Eight
cases (40%) could be shown simultaneously to have two
right pulmonary veins entering the LA in the same view,
each of which was seen to have a separate ostium into the
LA. Separate right or left pulmonary veins more than two
draining into the LA were not found in the study.
The parasternal short-axis view at the level of the aorta and
LA was the most ideal window to display the left upper pulmonary vein (LUPV). A length of the longitudinal section of
Figure 1 Doppler colour flow images of both right pulmonary
veins. Left, the image of right lower pulmonary vein in the apical
four-chamber view with colour flow mapping showing the vein draining into the LA almost perpendicular to its posterior aspect and virtually parallel to ultrasound beam and atrial septum. Right, the
Doppler colour flow image of the right upper pulmonary vein in
near apical five-chamber view indicates the vein in the right
postero-medial aspect of the LA in a tilting position. DAO, descending aorta; LA, left atrium; LV, left ventricle; RA, right atrium; RL,
right lower pulmonary vein; RU, right upper pulmonary vein; RV,
right ventricle.
the vein could be shown in all patients, which entered the
LA through its lateral aspect in a slightly left anterior to
right posterior direction (Figure 2). It might be comparatively
difficult to visualize the left lower pulmonary vein (LLPV)
opening into the LA. A short proximal segment of the longitudinal section of the LLPV could be visualized only in 12
patients (60%), which opened into the lateral aspect of the
LA with a slightly left posterior to right anterior direction
(Figure 2). Either a transverse section or being unrevealing
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No.
Transthoracic echo and individual pulmonary veins
657
42 + 14 mmHg. Five patients had moderate-to-severe
pulmonary hypertension (pulmonary artery systolic pressure
50 mmHg). Pulmonary-to-systemic blood flow ratio
(Qp/Qs) was 2.1 + 0.5.
Pulmonary vein angiography and contrast
echocardiography
Figure 3 Two-dimensional and Doppler colour flow images of four
pulmonary veins in the apical four-chamber view. Left, the twodimensional image showing the four pulmonary veins in a view.
Middle, the Doppler colour flow image of the two right pulmonary
veins; left, the Doppler colour flow image of the two left pulmonary
veins in the view. Abbreviations as in Figures 1 and 2.
was found by two-dimensional echocardiography in the
remaining patients. However, colour Doppler flow of the
vein draining into the LA could be found in all patients.
In the study, only one patient was seen simultaneously to
have all four pulmonary veins draining into the LA in the
apical four-chamber view in the left lateral decubitus position
(Figure 3). The orientation of the four pulmonary veins, from
left to right of the sector, were: right upper, right lower, left
lower, and left upper pulmonary veins, respectively.
Echocardiograms of good quality for all patients were
obtained in the left lateral decubitus position in the study.
As the angle between the ultrasound beam and the blood
flow direction of the left pulmonary veins was too large in
both apical four-chamber and parasternal short-axis views,
we did not measure the blood flow velocity of these veins.
No angle correction was made for measuring the blood
flow velocity of both right pulmonary veins.
The blood flow velocity of the RUPV and LUPV was
0.78 + 0.15 and 0.70 + 0.10 m/s, respectively. Their
difference was of no significance in statistics (P . 0.50).
Discussion
Using selective angiography and contrast echocardiography
as control, this prospective study has proven that transthoracic echocardiography can be most helpful in the orientation
of the pulmonary veins that were previously ambiguous. This
provides information ensuring that each vein can be visualized accurately in both location and blood flow by transthoracic echocardiography.
Pulmonary vein angiography,9–11 intracardiac echocardiography,12 transoesophageal echocardiography,13 computed
tomography,14,15 or magnetic resonance angiography16,17
are often used to assess pulmonary vein anatomy and
blood flow. All four pulmonary veins can be occasionally
seen draining into the LA from suprasternal view, particularly in children but rarely in the adult. Visualizing all four
pulmonary veins may be very difficult from the apical and
parasternal views. The traditional textbook was of the
opinion that the pulmonary veins seen in the apical fourchamber view, from left to right of the sector, were the
right upper, left upper, and the LLPVs, respectively,
whereas the right lower one was usually not visualized in
the apical four-chamber view.1,2 Investigators, on evaluating
pulmonary venous flow, were in general agreement that
what was displayed in the apical four-chamber view was
the blood flow of an RUPV,3–8 which was considered almost
parallel to the ultrasound beam.
However, in the study, it was found that both apical and
parasternal short-axis views were the ideal ultrasound
windows for evaluation of both the right pulmonary veins
and the left ones, respectively. When the site of four pulmonary veins is seen simultaneously in an apical fourchamber view, displayed from left to right of the sector,
they should be right upper, right lower, left lower, and left
upper pulmonary veins, respectively. The blood flow of the
pulmonary vein that Doppler ultrasound explores in the
apical four-chamber view in the literatures3–8 should be
that of the RLPV. For the majority of patients, the transducer must be tilted slightly anteriorly in order to explore the
blood flow of RUPV, namely, the blood flow of RUPV should
be measured in the near apical five-chamber view.
Anatomy of the pulmonary veins
Cardiac catheterization
All patients underwent cardiac catheterization without
any complications. Pulmonary artery systolic pressure was
The pulmonary vein orifices lie on the posterolateral (left
pulmonary veins) and posteromedial (right pulmonary
veins) aspects of the left atrial cavity. The LUPV and RUPV
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Figure 2 Two-dimensional and Doppler colour flow images of the
left upper and lower pulmonary veins separated into the LA in the
parasternal short-axis view in a patient with a mildly enlarged LA.
Left, the left upper and lower pulmonary veins in the parasternal
short-axis view showing separate opening into LA. Right, the
Doppler colour flow image of both left pulmonary veins in this
view. ASD, atrial septal defect; AO, aorta; IVC, inferior vena cava;
LAA, left atrial appendage; other abbreviations as in Figure 1.
Angiograms of four pulmonary veins were obtained successfully in all patients. Contrast images of these veins were
adequately visualized and suitable for evaluation in all
patients. The angiography and contrast echocardiography
of each of the individual pulmonary veins were summarized
in Table 2 and also shown in Figure 4–7. The catheter could
be clearly visualized in the LUPV, but was difficult to be seen
in other veins.
658
X. Huang et al.
Table 2 The angiography and contrast echocardiography of the individual pulmonary veins
Angiography
View
Course of entering the LA
View
Course of entering the LA
RLPV
Apical fourchamber
Opening into the LA from its rear and
almost parallel to the ultrasound
beam
P-A
RUPV
Near apical
five-chamber
Parasternal short
axis
Draining obliquely into the LA through its
right posterior aspect
The vein entering LA through its lateral
aspect with a slightly left posterior to
right anterior direction
P-A
The distal cardiac segment of the vein running along the
right inferior to left superior direction, with the
proximal portion entering almost perpendicularly the
LA from left to right direction
Coursing along the right superior to left inferior direction
Parasternal short
axis
Draining into the LA in a slightly left
anterior to right posterior direction
P-A
LLPV
LUPV
P-A
The distal cardiac segment of the vein running along the
left inferior to right superior direction and the
proximal portion entering the LA from left to right,
and perpendicular to the its wall
The vein running from the left superior to right inferior
direction
LA, left atrium; LLPV, left lower pulmonary vein; LUPV, left upper pulmonary vein; P-A, postero-anterior; RLPV, right lower pulmonary vein; RUPV, right
upper pulmonary vein.
Figure 4 Angiogram and contrast echocardiogram of the right
upper pulmonary vein. Left, the angiogram showing the coursing
of the vein draining into the LA in right superior to left inferior
direction. Middle, the echocardiogram of the vein in the near
apical five-chamber view, displaying the coursing of the vein draining obliquely into the LA through its right posterior aspect. Right,
the contrast echocardiogram of the vein in the same view showing
the vein opacified by the contrast agent. Abbreviations as in
Figure 1.
enter the LA in an anterosuperior direction, whereas the
lower ones open into the LA perpendicular to its posterior
wall.18 The upper and lower orientation of the sector in
the apical four-chamber view is always described as anatomic superior and inferior relationship.1 The plane that
transects the heart approximately parallel to the dorsal
and ventral surfaces of the body will be referred to as the
four-chamber plane.19 Such descriptions of the orientation
about the apical four-chamber view may make one consider
subjectively that the view was similar to a frontal plane
rather than a transverse plane, which may be an important
cause to misread the location of individual veins in the
apical four-chamber view. The three primary planes of the
heart of the short axis, four-chamber, and long-axis views
do not correspond with the standard transverse, frontal,
and sagittal anatomic planes of the body.20 The frontal
and transverse planes may be more useful for describing
the spatial orientation of pulmonary vein ostia.17 Although
the spatial relationships can be provided by two-dimensional
Figure 5 The angiogram and contrast echocardiogram of the right
lower pulmonary vein. Left, the angiogram of the vein showing its
distal cardiac segment running along the right inferior to left
superior direction, with its proximal portion entering almost perpendicular to the LA from the left to the right direction. Middle,
the echocardiogram of the vein in the apical four-chamber view.
Right, the contrast echocardiogram of the vein in the same view,
the proximal segment of the vein opacified and draining almost perpendicularly into the LA from its rear, and virtually parallel to the
ultrasound beam. C, catheter; other abbreviations as in Figures 1
and 2.
echocardiography,they should never be used as the sole
diagnostic criterion.
Both right pulmonary veins are easily visualized in the
apical four-chamber view and so is the left upper one in
the parasternal short-axis view. However, it might be difficult for two-dimensional echocardiography to display the
left lower one. Several reasons may be used to explain
this to occur. First, the LLPV is covered by surrounding structures such as the descending aorta and the lung. Secondly,
the ostia of both left pulmonary veins may be too close to
be differentiated by the transthoracic echocardiography.
Thirdly, the anatomic variant of the spatial orientation of
pulmonary vein ostia may also be a cause, because the incidence of pulmonary venous anatomic variants was reported
to be as high as 38%.21 However, the pathological analysis
did not refer to these anatomic variants.22
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Contrast echocardiography
Transthoracic echo and individual pulmonary veins
dilated pulmonary veins, which made them easy to be visualized by Doppler colour flow mapping and two-dimensional
echocardiography, and this, in turn, led to the dilation of the
right heart, causing a change in the cardiac position that
may be somewhat different from that of the patients with
normal-sized heart. These may give rise to some error in
the result. However, in our clinical practice, we have also
observed different patient groups including those with
normal-sized heart, which had similar results as stated
earlier with exception that visualizing the RUPV was even
more difficult than the right lower one. This confirms that
the studied result can be applied without limitation.
In our practice, it may be difficult to visualize the LLPV.
Fortunately, anomalous left lower pulmonary venous connection alone may be very rare.26,27 Another possible limitation is that transthoracic echocardiography may be difficult
to obtain images of good quality, as it happens that the pulmonary veins are located in the far field. However, an
experienced sonographer can adjust acoustic window to
optimize the image. Transoesophageal echocardiography
may be helpful to patients with suboptimal transthoracic
images.
Conclusions
Figure 7 The angiogram and contrast echocardiogram of the left
lower pulmonary vein. Left, the angiogram showing that the distal
cardiac segment of the vein running along the left inferior to the
right superior direction with the proximal portion entering the LA
from left to right and perpendicular to its wall. Middle, a suboptimal
echocardiogram of the vein in the parasternal short-axis view. Right,
the contrast echocardiogram of the vein in the same view, the vein
was identified by its opcaification entering the LA through its lateral
aspect with a slightly left posterior to right anterior direction. C,
catheter; PA, pulmonary artery; other abbreviations as in
Figures 1 and 2.
Pulmonary vein imaging by transoesophageal
echocardiography
The pulmonary veins are relatively difficult to be examined
by transthoracic echocardiography in adults, but can be well
seen by transoesophageal echocardiography. The LUPV is
identifiable running above and parallel to the left atrial
appendage,23 which is similar to that shown in the parasternal short-axis view. Transoesophageal echocardiography is
allowed to identify 100% of RUPV and LUPV.24 However,
both lower ones were the most difficult to be imaged and
visualized in only 74% of the left lower24 and 75% of the
right lower ones,25 respectively. Given this condition, the
blood flow velocity pattern was usually recorded in both
upper ones by transoesophageal echocardiography.3
Study limitations
All the study patients suffered from ASD with significant
left-to-right shunt and abundant blood flow of the mildly
Individual pulmonary vein imaging by transthoracic echocardiography seems to be feasible. There may exist some ambiguity about the traditional point of view accepted generally.
Using angiography and contrast echocardiography as control
in this study, the accurate position of each pulmonary vein
can be documented in the parasternal short-axis and
apical views. The right lower and upper veins were best
seen in the apical four-chamber and the near apical fivechamber views, respectively. Both left pulmonary veins
were best displayed in the parasternal short-axis view.
This expertise should be helpful to evaluate various proximal
pulmonary venous diseases in their further studies.
Conflict of interest: none declared.
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