DOI:10.2214/AJR.05.1622
AJR 2006; 186:S219-S223
© American Roentgen Ray Society
Radiological Reasoning: Pulmonary Embolism—Thinking Beyond the Clots
Pierre D. Maldjian1,
Ather Anis2 and
Muhamed Saric2
1 Department of Radiology, University Hospital, UMDNJ-NJ Medical School, 150
Bergen St., UH C-320, Newark, NJ 07103-2406.
2 Department of Medicine, Division of Cardiology, University Hospital, UMDNJ-NJ
Medical School, Newark, NJ.
Received September 12, 2005;
accepted after revision December 5, 2005.
This Radiological Reasoning article is available for SAM credit and
CME credits when completed with the additional educational material provided
in "Imaging of Pulmonary Embolism: Self-Assessment Module." See
page S215 for
details.
Address correspondence to P. D. Maldjian
(maldjipd{at}umdnj.edu).
Abstract
Objective
We discuss the CT findings in a case of pulmonary embolism complicated by
paradoxical embolism in a patient with a patent foramen ovale and atrial
septal aneurysm.
Conclusion
When confronted with a case of pulmonary embolism on CT, besides evaluating
the extent of pulmonary artery occlusion, the radiologist should examine the
cardiovascular system to identify any unsuspected underlying or associated
conditions.
Keywords: cardiopulmonary imaging • embolism • heart
Case History
A 60-year-old woman with no significant medical history had resection of a
5-cm non–small cell lung carcinoma of the left lower lobe. This required
a pneumonectomy because the tumor encased the left pulmonary artery. Two days
after surgery, while attempting to ambulate, the patient became acutely short
of breath and hypoxic. Due to the clinical suspicion for pulmonary embolism,
CT pulmonary angiography was performed (Figs.
1A,
1B,
1C, and
1D). (At this point, if the
abstract has not been reviewed, we encourage the reader to examine the CT
images to formulate a diagnosis before proceeding further.)
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Fig. 1A —60-year-old woman who developed acute dyspnea and hypoxia 2 days
after left pneumonectomy. Images are from CT pulmonary angiography. CT images
at level of right interlobar artery (A), at level of cardiac chambers
(B), through upper abdomen (C), and at level of superior pole of
left kidney (D).
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Fig. 1B —60-year-old woman who developed acute dyspnea and hypoxia 2 days
after left pneumonectomy. Images are from CT pulmonary angiography. CT images
at level of right interlobar artery (A), at level of cardiac chambers
(B), through upper abdomen (C), and at level of superior pole of
left kidney (D).
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Fig. 1C —60-year-old woman who developed acute dyspnea and hypoxia 2 days
after left pneumonectomy. Images are from CT pulmonary angiography. CT images
at level of right interlobar artery (A), at level of cardiac chambers
(B), through upper abdomen (C), and at level of superior pole of
left kidney (D).
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Fig. 1D —60-year-old woman who developed acute dyspnea and hypoxia 2 days
after left pneumonectomy. Images are from CT pulmonary angiography. CT images
at level of right interlobar artery (A), at level of cardiac chambers
(B), through upper abdomen (C), and at level of superior pole of
left kidney (D).
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CT
The CT scan shows subcutaneous emphysema with air and fluid in the left
pneumonectomy space. There is a central area of hypoattenuation in the
interlobar branch of the right pulmonary artery and in the pulmonary artery to
the right middle lobe. Multiple segmental pulmonary arterial filling defects
are also present in the right lower lobe. The atrial septum appears deformed
with curvature convex toward the left atrium. In the upper abdomen, there is a
large wedge-shaped area of hypoattenuation in the spleen and a small subtle
area of decreased enhancement in the medial aspect of the superior pole of the
left kidney.
Expert Discussion (Dr. Maldjian)
The left-sided subcutaneous emphysema and air and fluid in the left
pneumonectomy space are expected postoperative findings and do not require
further discussion. The filling defects in the pulmonary vessels represent
pulmonary emboli. Normally, the short-axis diameter of the right ventricle is
about equal to that of the left ventricle. In this case, the right ventricle
is dilated compared with the left ventricle. This finding on CT in association
with pulmonary embolism may indicate right ventricular dysfunction secondary
to the acute elevation of pulmonary artery pressure
[1]. The right atrium is also
dilated, which is probably due to the elevated right-sided cardiac
pressures.
The large wedge-shaped defect in the spleen and the small low-attenuation
area in the superior pole of the left kidney represent infarcts. These
findings in a patient with pulmonary embolism indicate paradoxical embolism.
Paradoxical emboli are most commonly caused by an intracardiac communication
between the systemic and pulmonary circulations. Patent foramen ovale and
atrial septal defect are the two most common cardiac abnormalities associated
with paradoxical emboli [2].
Therefore, we should now scrutinize the image through the cardiac chambers.
The atrial septum is bulging abnormally toward the left atrium. This finding
is consistent with an atrial septal aneurysm (ASA). Bowing of the ASA toward
the left atrium indicates that at the instant the image was obtained the
pressure in the right atrium exceeded that in the left atrium. This difference
in pressure can be transient, related to the phase of the cardiac cycle, but
in this case likely reflects acute elevation of the right-sided cardiac
pressures.
The significance of an ASA is its association with patent foramen ovale
(PFO). Approximately 70% of patients with an ASA also have a PFO
[3]. Thus, we can now postulate
a diagnosis that explains all of the CT findings. The pulmonary embolism
caused elevation of the right-sided intracardiac pressures that resulted in
increased right-to-left shunting through a PFO, thereby predisposing the
patient to paradoxical emboli.
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Fig. 2A —Images from transesophageal echocardiography performed 6 days after
CT study show atrial septal aneurysm oscillating throughout cardiac cycle and
right-to-left shunt at atrial level after administration of agitated saline.
RA = right atrium, LA = left atrium, AV = aortic valve, arrow = atrial septum.
Image in diastole shows bulging of atrial septum toward right atrium.
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Fig. 2B —Images from transesophageal echocardiography performed 6 days after
CT study show atrial septal aneurysm oscillating throughout cardiac cycle and
right-to-left shunt at atrial level after administration of agitated saline.
RA = right atrium, LA = left atrium, AV = aortic valve, arrow = atrial septum.
Image in systole shows atrial septum bulging into left atrium.
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Fig. 2C —Images from transesophageal echocardiography performed 6 days after
CT study show atrial septal aneurysm oscillating throughout cardiac cycle and
right-to-left shunt at atrial level after administration of agitated saline.
RA = right atrium, LA = left atrium, AV = aortic valve, arrow = atrial septum.
Image after administration of saline containing microbubbles shows increased
echogenicity in right atrium representing bolus and speckled echoes in left
atrium from passage of microbubbles through patent foramen ovale.
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Clinical Management
After the CT examination, the patient received IV infusion of heparin for
systemic anticoagulation. Vascular sonography of the lower extremities
performed 2 days later was negative for deep venous thrombosis. Because
swelling and erythema of the patient's left arm were noted by the clinical
service, vascular sonography of the left upper extremity was also performed,
which revealed thrombosis of the cephalic vein extending into the left
subclavian vein. The thrombophlebitis was likely a complication from IV
cannulation and was deemed the source of the pulmonary emboli.
Transthoracic and transesophageal echocardiography was performed 6 days
after CT. An ASA was seen on the transesophageal study (Figs.
2A and
2B), although it was not
visible on the transthoracic study. The transesophageal study obtained with
saline used as contrast material also confirmed the presence of a PFO
(Fig. 2C). No intracardiac
thrombi were present. Right ventricular function was normal. The patient
recovered uneventfully and was discharged from the hospital after converting
to oral warfarin to continue anticoagulation. The final diagnosis was
pulmonary embolism and paradoxical embolism with PFO and ASA.
Expert Discussion (Dr. Maldjian)
In most cases, thrombi from the lower extremities are the source for
pulmonary emboli, and it is rare to encounter a patient with pulmonary
embolism from clots in the upper extremity. Although a negative sonography
examination of the lower extremities does not completely exclude lower
extremity veins as a source of emboli, the known thrombus in the upper
extremity was the most likely source in this patient. Because the patient had
only one lung, it would not require a large amount of embolized clot from the
thrombus in the subclavian vein to result in significant compromise of the
pulmonary circulation. The patient may also have been at increased risk for
thrombophlebitis because a hypercoagulable state is associated with malignancy
[4].
The fact that the ASA was visible on only the transesophageal
echocardiogram is not surprising because ASAs are commonly missed on a
transthoracic study alone [3].
Normal right ventricular function at the time of echocardiography given the
appearance on CT likely reflects a good therapeutic response. On
echocardiography, the diagnosis of PFO is made using agitated saline (saline
containing microbubbles of air) as a sonography contrast agent. The saline is
injected IV, and the sonographer looks for passage of microbubbles from the
right atrium to the left atrium through the atrial septum. The patient can be
asked to cough or bear down (Valsalva maneuver) during the injection; these
actions transiently elevate right atrial pressure and increase the amount of
shunting through a PFO [5].
Commentary
A definitive diagnosis of paradoxical embolism requires detection of
thrombus lodged in the intracardiac defect, most commonly right atrial
thrombus crossing a PFO. Such direct observation is rare and is usually
limited to sporadic echocardiographic reports
[6]. In clinical practice the
diagnosis of paradoxical embolism is usually presumptive and requires
detection of the following three elements: first, systemic embolism without an
apparent source in the left heart or proximal arterial tree (no evidence of
atrial fibrillation or severe atherosclerosis of the thoracic aorta); second,
venous thrombus or pulmonary embolus as an embolic source; and, third,
right-to-left shunting through an abnormal communication between the right and
left circulations, such as a PFO, atrial septal defect, or pulmonary
arteriovenous malformation [2,
6].
A PFO is the most common abnormal communication between the right and left
circulations associated with paradoxical embolism. Both echocardiography and
autopsy studies have shown that the prevalence of PFO is approximately 25%
[7,
8]. A PFO usually remains
physiologically closed as long as the pressure in the left atrium is higher
than the pressure in the right atrium. However, common maneuvers, such as
inspiration, cough, or Valsalva, can result in transient elevation of right
atrial pressure sufficient to allow paradoxical emboli to pass from the right
atrium to the left via the PFO
[9]. The eustachian valve
(valve of the inferior vena cava) may also direct blood return from the
inferior vena cava directly onto the PFO, promoting passage of thrombi from
the lower extremity veins to the systemic circulation
[10]. Echocardiographers can
take advantage of this phenomenon as the sensitivity for the detection of a
PFO is increased when agitated saline contrast material is injected through a
femoral vein rather than an antecubital vein
[11].
An ASA is a congenital cardiac abnormality characterized by saccular
formation of the interatrial septum. Redundant atrial septal tissue results in
bulging of the septum into either or both atria during the cardiac cycle. ASA
has a high association with PFO: 70% of patients with an ASA also have a PFO.
The combination of ASA and PFO also puts the patient at increased risk for
cryptogenic stroke likely from paradoxical emboli
[3]. It has been theorized that
the motion of the ASA promotes paradoxical shunting by enhancing the already
preferential orientation of blood flow from the inferior vena cava toward the
PFO [12]. Transesophageal
echocardiography is considered the best imaging test for the diagnosis of PFO
and ASA [5]. Recently,
contrast-enhanced dynamic MRI with the Valsalva maneuver has also been shown
to be useful in the diagnosis of ASA and PFO
[13].
Pulmonary embolism in the setting of a coexistent PFO increases the risk of
paradoxical embolism due to elevated right-sided cardiac pressure increasing
right-to-left shunting through the PFO
[14]. It has been shown that
right-to-left shunting through a PFO is increased in acute pulmonary embolism
even in hemodynamically stable patients without preexisting cardiopulmonary
disease [15]. In their a study
of patients with acute major pulmonary embolism, Konstantinides et al.
[6] found right-to-left
shunting through a PFO to be an independent predictor of adverse outcome. In
that study, those patients with a PFO had a significantly higher incidence of
death (33% vs 14%) and ischemic stroke (13% vs 2.2%) than those without a PFO
[6].
Therapeutic options for paradoxical embolism associated with PFO include
anticoagulation, thrombectomy, placement of an inferior vena cava filter (if
the source for emboli is from the lower extremity), and closure of the PFO
[16]. Recurrent paradoxical
embolism in the presence of a PFO and ASA is considered an unequivocal
indication for PFO closure
[10]. Closure of a PFO can now
be accomplished with devices implanted percutaneously
[17].
When confronted with a case of pulmonary embolism on CT, besides
identifying the extent of pulmonary artery occlusion, the radiologist should
examine the cardiovascular system for any associated abnormalities. Dilatation
of the right ventricle and interventricular septal shift toward the left
ventricle are associated with right ventricular dysfunction secondary to
pressure overload. Other signs of pressure overload of the right heart include
enlargement of the right atrium and the inferior vena cava
[18]. Patients with right
ventricular dysfunction after pulmonary embolism have a higher mortality rate
than those with normal right ventricular function even if hemodynamically
stable at presentation [19,
20]. Therefore, right
ventricular dysfunction in patients with pulmonary embolism places them at
increased risk and may be an indication for aggressive intervention, such as
thrombolytic therapy, as opposed to anticoagulation alone
[21].
A PFO on CT pulmonary angiography can manifest as decreased enhancement of
the pulmonary artery with early enhancement of the thoracic aorta from
augmentation of right-to-left shunting through the defect caused by deep
inspiration [22] (although
this was not present in our patient). Significant deviation of the atrial
septum might indicate an ASA, and as we have seen, this finding should also
raise suspicion for a possible coexisting PFO. The cardiac chambers and
systemic arteries should also be scrutinized because paradoxical embolism can
have characteristic findings on CT
[23–25].
In conclusion, we have presented a case of pulmonary embolism complicated
by paradoxical embolism in a patient with an ASA and PFO. Although the
diagnosis of pulmonary embolism on CT may be straightforward, it is essential
that the radiologist examine the remainder of the cardiovascular system for
ancillary findings to diagnose unsuspected underlying conditions. The
radiologist should look and think beyond the pulmonary clots.
References
- Contractor S, Maldjian PD, Sharma VK, Gor DM. Role of helical CT in
detecting right ventricular dysfunction secondary to acute pulmonary embolism.
J Comput Assist Tomogr 2002;26
: 587-591[CrossRef][Medline]
- Ward R, Jones D, Haponik EF. Paradoxical embolism: an
underrecognized problem. Chest 1995;108
: 549-558[Abstract/Free Full Text]
- Cabanes L, Mas JL, Cohen A, Amarenco P, et al. Atrial septal
aneurysm and patent foramen ovale as risk factors for cryptogenic stroke in
patients less than 55 years of age: a study using transesophageal
echocardiography. Stroke 1993;24
: 1865-1873[Abstract/Free Full Text]
- Falanga A. Thrombophilia in cancer. Semin Thromb
Haemost 2005; 31:104
-110[CrossRef][Medline]
- Gill EA, Quaife RA. The echocardiographer and the diagnosis of
patent foramen ovale. Cardiol Clin 2005;23
: 47-52[CrossRef][Medline]
- Konstantinides S, Geibel A, Kasper W, Olschewski M, Blumel L, Just
H. Patent foramen ovale is an important predictor of adverse outcome in
patients with major pulmonary embolism. Circulation1998; 97:1946
-1951[Abstract/Free Full Text]
- Gill EA. Definitions and pathophysiology of the patent foramen
ovale: broad overview. Cardiol Clin 2005;23
: 1-6[CrossRef][Medline]
- Meissner I, Whisnant JP, Khandheria BK, et al. Prevalence of
potential risk factors for stroke assessed by transesophageal echocardiography
and carotid ultrasonography: the SPARC study. Mayo Clin
Proc 1999; 74:862
-869[Medline]
- Wu LA, Malouf JF, Dearani JA, et al. Patent foramen ovale in
cryptogenic stroke: current understanding and management options.
Arch Intern Med 2004;164
: 950-956[Abstract/Free Full Text]
- Meier B, Lock JE. Contemporary management of patent foramen ovale.
Circulation 2003;107
: 5-9[Free Full Text]
- Cramer SC. Patent foramen ovale and its relationship to stroke.
Cardiol Clin 2005;23
: 7-11[Medline]
- Mas JL, Arquizan C, Lamy C, et al. Recurrent cerebrovascular events
associated with patent foramen ovale, atrial septal aneurysm, or both.
N Engl J Med 2001;345
: 1740-1746[Abstract/Free Full Text]
- Mohrs OK, Petersen SE, Erkapic D, et al. Diagnosis of patent
foramen ovale using contrast-enhanced dynamic MRI: a pilot study.
AJR 2005; 184:234
-240[Abstract/Free Full Text]
- Kasper W, Geibel A, Tiede N, Just H. Patent foramen ovale in
patients with haemodynamically significant pulmonary embolism.
Lancet 1992; 340:561
-564[CrossRef][Medline]
- Miller RL, Das S, Anandarangam T, et al. Relation between patent
foramen ovale and perfusion abnormalities in acute pulmonary embolism.
Am J Cardiol 1997;80
: 377-378[CrossRef][Medline]
- Inoue T, Tadehara F, Hinoi T, et al. Paradoxical peripheral
embolism coincident with acute pulmonary thromboembolism. Intern
Med 2005; 44:243
-245[Medline]
- Carroll JD, Dodge S, Groves BM. Percutaneous patent foramen ovale
closure. Cardiol Clin 2005;23
: 13-33[Medline]
- Cheriex EC, Sreeram N, Eussen YF, Pieters FA, Wellens HJ. Cross
sectional Doppler echocardiography as the initial technique for the diagnosis
of acute pulmonary embolism. Br Heart J1994; 72:52
-57[Abstract/Free Full Text]
- Grifoni S, Olivotto I, Cecchini P, et al. Short-term clinical
outcome of patients with acute pulmonary embolism, normal blood pressure, and
echocardiographic right ventricular dysfunction.
Circulation 2000;101
: 2817-2822[Abstract/Free Full Text]
- Van der Meer RW, Pattynama PM, Van Strijen MJ, et al. Right
ventricular dysfunction and pulmonary obstruction index at helical CT:
prediction of clinical outcome during 3-month follow-up in patients with acute
pulmonary embolism. Radiology 2005;235
: 798-803[Abstract/Free Full Text]
- Lualdi JC, Goldhaber SZ. Right ventricular dysfunction after acute
pulmonary embolism: pathophysiologic factors, detection, and therapeutic
implications. Am Heart J 1995;130
: 1276-1282[CrossRef][Medline]
- Henk CB, Grampp S, Linnau KF, et al. Suspected pulmonary embolism:
enhancement of pulmonary arteries at deep-inspiration CT
angiography—influence of patent foramen ovale and atrial septal defect.
Radiology 2003;226
: 749-755[Abstract/Free Full Text]
- Kim JH, Seo JB, Do KH, et al. Paradoxical embolism detected on CT
angiography and treated with temporary inferior vena cava filtration and
anticoagulation. AJR 2004;183
: 1244-1246[Free Full Text]
- Delalu P, Ferretti GR, Bricault I, Ayanian D, Coulomb M.
Paradoxical emboli: demonstration using helical computed tomography of the
pulmonary artery associated with abdominal computed tomography. Eur
Radiol 2000; 10:384
-386[CrossRef][Medline]
- Oliver TB, Reid JH. Thoracic aortic dissection that wasn't: CT
demonstration of probable paradoxical embolus secondary to unsuspected
pulmonary embolus. Br J Radiol 1997;70
: 840-842[Abstract]
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AJR 2006 186: S215-S218.
[Abstract]
[Full Text]
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P. D. Maldjian and F. S. Chew
Imaging of pulmonary embolism: self-assessment module.
Am. J. Roentgenol.,
March 1, 2006;
186(3 Suppl):
S215 - S218.
[Abstract]
[Full Text]
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Abstract
Case History
