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European Journal of Echocardiography Advance Access published online on October 24, 2008
European Journal of Echocardiography, doi:10.1093/ejechocard/jen258
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Published on behalf of the European Society of Cardiology. All rights reserved. © The Author 2008. For permissions please email: journals.permissions@oxfordjournals.org

Using mitral ‘annulus reversus’ to diagnose constrictive pericarditis

Christina S. Reuss1, Susan M. Wilansky1, Steven J. Lester1, Joan L. Lusk1, Diane E. Grill2, Jae K. Oh3 and A. Jamil Tajik1,*

1 Division of Cardiovascular Diseases, Mayo Clinic, 13400 East Shea Boulevard, Scottsdale, AZ 85259, USA
2 Division of Biostatistics, Mayo Clinic, Rochester, MN, USA
3 Division of Cardiovascular Diseases, Mayo Clinic, Rochester, MN, USA

Received 27 June 2008; accepted after revision 12 September 2008.

* Corresponding author. E-mail address: jtajik{at}mayo.edu


   Abstract
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 Abstract
Introduction
 Methods
 Results
 Discussion
 Conclusion
 Funding
 References
 
Aims: To characterize mitral medial and lateral annular velocities in constrictive pericarditis or restrictive cardiomyopathy compared with normal subjects.

Methods and results: Tissue Doppler imaging peak systolic velocity (S'), peak early diastolic annular velocity (e'), and timing difference between mitral early flow and early annular movement were measured in 14 patients with constrictive pericarditis, 10 with restrictive cardiomyopathy, and 17 normal subjects using the apical four-chamber view lateral and medial mitral annulus. In controls, mitral lateral e' velocity was 25% higher than medial e' velocity (13.0 ± 3.1 vs. 10.7 ± 2.8 cm/s; P = 0.02), whereas with constrictive pericarditis, averaged lateral e' velocity was 2% lower than medial e' velocity (10.7 ± 2.5 vs. 11.2 ± 3.1 cm/s; P > 0.05). This relationship represented a reversal of lateral and medial e' velocities compared with normal subjects (P = 0.004). Differences in S', E/e', and timing intervals between normal subjects and patients with constrictive pericarditis were not statistically significant; however, restrictive cardiomyopathy could be distinguished from constrictive pericarditis and controls with all other parameters (S', E/e', medial and lateral e' velocities, and timing interval differences; all P < 0.05).

Conclusion: Practical applications of tissue Doppler imaging for evaluation of possible constrictive pericarditis include reversal of the relationship between lateral and medial e' velocities (i.e. ‘annulus reversus’).

Keywords: Cardiomyopathy; Doppler ultrasound; Echocardiography, adult; Pericardial heart disease


   Introduction
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 Conclusion
 Funding
 References
 
Constrictive pericarditis and restrictive cardiomyopathy are challenging entities for echocardiographers to differentiate; however, advances in tissue Doppler imaging technology have led to more sophisticated methods to distinguish these cardiac conditions.1,2 Specifically, tissue Doppler imaging has allowed the determination of discrete amplitude cut points at the lateral mitral annulus to distinguish constrictive pericarditis from restrictive cardiomyopathy without overlap.3 Tissue Doppler imaging of the interventricular septum can also be used to distinguish constrictive pericarditis from abnormal septal motion due to other causes.4 We have reported the observation of annulus paradoxus in patients with constrictive pericarditis when there is an inverse relationship between the pulmonary capillary occlusion pressure and the ratio of transmitral velocity to mitral lateral annulus early diastolic velocity (E/e') compared with high left ventricular filling pressure in patients without pericardial disease.5 Our continued research into this entity has led to another observation unique to patients with constrictive pericarditis and is added to the echocardiographic armamentarium to identify this condition.

We hypothesized that the relationship of amplitude differences in the mitral lateral (lat) and medial (med) annulus may be useful in differentiating those patients with constrictive pericarditis from normal subjects as well as from those patients with restrictive cardiomyopathy. Thus, we sought to characterize and compare mitral annular velocities and timing intervals among these three groups.


   Methods
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 Abstract
 Introduction
 Methods
Results
 Discussion
 Conclusion
 Funding
 References
 
Study group
We searched the Echocardiography Information Management Systems database of Mayo Clinic, Scottsdale, Arizona, for records that listed any of the following search terms as a final diagnosis: normal echocardiogram, constriction, constrictive pericarditis, cardiac amyloidosis, amyloid, amyloidosis, and restrictive cardiomyopathy. All patients (age range, 27–88 years) who underwent transthoracic echocardiography between 2004 and 2006 at Mayo Clinic, Scottsdale, Arizona, were included in this study. Patients were excluded if atrial fibrillation was noted at the time of the study or if inadequate Doppler signals precluded offline analysis. After exclusion criteria were applied, 41 patients remained for analysis (17 normal controls, 14 with constrictive pericarditis, and 10 with cardiac amyloidosis).

Echocardiographic examination
From stored digital transthoracic echocardiographic still frames, we independently remeasured all parameters using electronic calipers on the ProSolv CV Analyzer 3.0 viewing program (ProSolv CardioVascular, Indianapolis, Indiana). Peak mitral inflow velocity was measured in early (E) and late (A) diastole in cm/s using pulsed-wave Doppler. Peak annular velocities were measured from the apical four-chamber view at peak annular systole (S'), early (e'), and late (a') diastole in cm/s from the mitral lateral and medial annulus. Timings of annular movement and mitral flow were determined by measuring the duration (ms) from the onset of the QRS to the onset of annular motion and the onset of the E-wave, respectively. Pulsed-wave Doppler was performed in patients with constrictive pericarditis using simultaneous nasal respirometer recordings.2 Varying sweep speeds of 25–100 mm/s were used. Analysis of Doppler velocities was performed on the first beat immediately after the onset of inspiration and expiration. Additionally, in patients with constrictive pericarditis, we averaged data over 5 to 10 beats throughout the respiratory cycle and reported it as the averaged parameter. The averaged e' velocity throughout the respiratory cycle was used to minimize the potential respirophasic impact of load on e' velocity in patients with constriction.

Statistical analysis
Data are presented as mean ± SD. One-way analysis of variance was used to test for statistically significant differences in the echocardiographic variables among the normal controls, the constrictive pericarditis patients (on inspiration), and the restrictive cardiomyopathy patients. If the overall F-test was significant (P < 0.05), then pairwise comparisons among the three groups were conducted.


   Results
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 Abstract
 Introduction
 Methods
 Results
Discussion
 Conclusion
 Funding
 References
 
Patient characteristics
Of the 41 patients, 17 were normal subjects (mean age 44 years; range 27–66 years). Fourteen patients had constrictive pericarditis (71% idiopathic and 29% with a history of coronary artery bypass grafting). The mean age of this group was 63 years (range 25–75 years), and 85% of them were men. Of the 10 patients with restrictive cardiomyopathy, all had cardiac amyloidosis (60% with positive endomyocardial biopsy, 40% with a positive fat pad aspirate). Their mean age was 69 years (range 47–88 years).

Amplitude variables
Doppler echo findings among the three groups showed no statistically significant difference in mitral E velocity (P > 0.05; Table 1). The E/A ratio was higher in normal controls and in patients with constrictive pericarditis compared with patients with restrictive cardiomyopathy (1.54 ± 0.41 and 1.48 ± 0.45 vs. 2.63 ± 1.45; P = 0.003). The e' velocities were significantly higher in patients with constrictive pericarditis compared with patients with restrictive cardiomyopathy [averaged e'lat 10.7 ± 2.5 vs. 3.7 ± 1.7 cm/s (P < 0.001) and averaged e'med 11.2 ± 3.1 vs. 3.8 ± 2.4 cm/s (P < 0.001)]. These values were not statistically significantly different from the normal controls. The E/e' ratio was significantly lower in patients with constrictive pericarditis compared with patients with restrictive cardiomyopathy [E/e'lat 6 ± 4 vs. 22 ± 8 (P = 0.001) and E/e'med 6 ± 3 vs. 28 ± 17 (P = 0.001)]. The S' velocity was significantly higher in patients with constrictive pericarditis compared with patients with restrictive cardiomyopathy [S'lat 8.2 ± 1.7 vs. 3.3 ± 1.3 cm/s (P < 0.001); S'med 8.1 ± 0.7 vs. 3.8 ± 1.9 cm/s (P < 0.001)].


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  		Table 1 Echocardiographic data in patients with constrictive pericarditis, restrictive cardiomyopathy, and normal controls*

 
Annulus reversus
In normal subjects, mitral lateral e' velocity was higher than the medial e' velocity by 25% (13.0 ± 3.1 vs. 10.7 ± 2.8 cm/s; P = 0.02), whereas in patients with constrictive pericarditis the averaged lateral e' velocity was lower than the medial e' velocity by 2% (10.7 ± 2.5 vs. 11.2 ± 3.1 cm/s; P > 0.05). The absolute difference of the averaged lateral and medial e' velocities for constrictive pericarditis was –0.55 ± 2.57 and 2.27 ± 2.79 cm/s in controls. This relationship represents a reversal of the typical lateral and medial e' velocities observed in controls, hence termed ‘annulus reversus’ (P = 0.004; Figure 1).


Figure 1
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  		Figure 1 Doppler representation of annulus reversus. The normal relationship (top panel) between lateral mitral e' and medial mitral e' is reversed in constrictive pericarditis (middle panel) but not in restrictive cardiomyopathy (bottom panel).

 
Timing intervals
The time difference between the onset of mitral flow and the onset of e' ({Delta}TE–e') in normal subjects at the lateral and medial annuli was –43 ± 12 and –35 ± 26 ms, respectively. This finding remains in those patients with constrictive pericarditis, in whom the {Delta}TE–e' at the lateral and medial sites is –44 ± 31 and –27 ± 41 ms, respectively (P > 0.05 compared with patients with normal function). In contrast, restrictive cardiomyopathy showed a prolonged time difference with the e' motion occurring after E flow ({Delta}TE–e' lat +36 ± 38 ms; {Delta}TE–e' med +37 ± 40 ms; P < 0.001) compared with patients with constrictive pericarditis or with controls.


   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
Conclusion
 Funding
 References
 
The principal finding of this study is the identification of the reversal of the normal relationship of mitral lateral e' and medial e' velocities. In constrictive pericarditis, the lateral e' velocity is lower than the medial e' velocity, resulting in annulus reversus. This novel finding has not been reported previously. We noted annulus reversus in patients with constrictive pericarditis despite normal e' velocities (>8 cm/s). Because of respirophasic differences in e' velocities at both annuli in patients with constrictive pericarditis, we recommend taking an average of all absolute values throughout one respiratory cycle. Doing so obviates the need to define discrete dichotomous values for the inspiration and expiration. We hypothesize that the finding of annulus reversus is likely due to the tethering of the adjacent fibrotic and scarred pericardium, which influences the lateral mitral annulus of patients with constrictive pericarditis. Therefore, in a patient with preserved mitral e' velocities (>8 cm/s) and a low E/e' ratio (<8; annulus paradoxus), the recognition of annulus reversus should alert the interpreting echocardiographer to the diagnosis of constrictive pericarditis.

Patients with restrictive cardiomyopathy did not exhibit annulus reversus; however, we found that absolute cut points of lateral e' velocity >6.5 cm/s and a medial e' velocity of >8 cm/s exhibited high sensitivity and specificity for distinguishing this group of patients from those with constrictive pericarditis (lateral sensitivity and specificity 100%; medial sensitivity 100%; specificity 90%), which is consistent with prior reports.3,6 Additionally, restrictive cardiomyopathy can be distinguished from constrictive pericarditis using absolute velocity values of the medial and lateral S' and e' (P < 0.001).

Another finding of this study emphasizes the importance of maximizing the high temporal resolution that echocardiography provides to quantify timing variables that are less likely to be influenced by angle dependency.7 The comparison of patients with constrictive pericarditis to those with restrictive cardiomyopathy showed that annular motion occurs before E flow at both sites (P < 0.05). In restrictive cardiomyopathy, annular motion occurs after E flow. This timing delay has been previously noted during acute myocardial ischaemia and has been shown to correlate well with impaired left ventricular relaxation (tau) in dogs (r = 0.85; P < 0.05).8 Recently published data show that incrementally adding the timing difference to septal mitral e' and S' velocities facilitates the differentiation of constrictive pericarditis from restrictive cardiomyopathy with 94% sensitivity.9


   Conclusion
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
Funding
 References
 
A comprehensive echocardiographic evaluation should include the detailed tissue Doppler imaging analysis of both medial and lateral mitral annular velocities and their relationship. Constrictive pericarditis is characterized by preserved tissue Doppler imaging (both e' and S') and by the presence of annulus paradoxus, to which we now add the observation of annulus reversus.


   Funding
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
 Funding
References
 
Funding for C.S.R. was provided through the Peter J. Grant Post-Doctoral Fellowship in Advanced Echocardiography 2006–2007 by the Graduate School of Medical Education, College of Medicine, Mayo Clinic.


   Acknowledgements
 
We wish to thank Ms Bonnie L. Schimek for medical graphics assistance.


   References
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 Abstract
 Introduction
 Methods
 Results
 Discussion
 Conclusion
 Funding
 References
 

  1. Hatle LK, Appleton CP, Popp RL. Differentiation of constrictive pericarditis and restrictive cardiomyopathy by Doppler echocardiography. Circulation (1989) 79:357–70.[Abstract/Free Full Text]
  2. Oh JK, Hatle LK, Seward JB, Danielson GK, Schaff HV, Reeder GS, et al. Diagnostic role of Doppler echocardiography in constrictive pericarditis. J Am Coll Cardiol (1994) 23:154–62.[Abstract]
  3. Garcia MJ, Rodriguez L, Ares M, Griffin BP, Thomas JD, Klein AL. Differentiation of constrictive pericarditis from restrictive cardiomyopathy: assessment of left ventricular diastolic velocities in longitudinal axis by Doppler tissue imaging. J Am Coll Cardiol (1996) 27:108–14.[Abstract]
  4. Sengupta PP, Mohan JC, Mehta V, Arora R, Khandheria BK, Pandian NG. Doppler tissue imaging improves assessment of abnormal interventricular septal and posterior wall motion in constrictive pericarditis. J Am Soc Echocardiogr (2005) 18:226–30.[CrossRef][Web of Science][Medline]
  5. Ha JW, Oh JK, Ling LH, Nishimura RA, Seward JB, Tajik AJ. Annulus paradoxus: transmitral flow velocity to mitral annular velocity ratio is inversely proportional to pulmonary capillary wedge pressure in patients with constrictive pericarditis. Circulation (2001) 104:976–8.[Abstract/Free Full Text]
  6. Rajagopalan N, Garcia MJ, Rodriguez L, Murray RD, Apperson-Hansen C, Stugaard M, et al. Comparison of new Doppler echocardiographic methods to differentiate constrictive pericardial heart disease and restrictive cardiomyopathy. Am J Cardiol (2001) 87:86–94.[CrossRef][Web of Science][Medline]
  7. Oh JK, Tajik J. The return of cardiac time intervals: the phoenix is rising. J Am Coll Cardiol (2003) 42:1471–4.[Free Full Text]
  8. Rivas-Gotz C, Khoury DS, Manolios M, Rao L, Kopelen HA, Nagueh SF. Time interval between onset of mitral inflow and onset of early diastolic velocity by tissue Doppler: a novel index of left ventricular relaxation: experimental studies and clinical application. J Am Coll Cardiol (2003) 42:1463–70.[Abstract/Free Full Text]
  9. Choi EY, Ha JW, Kim JM, Ahn JA, Seo HS, Lee JH, et al. Incremental value of combining systolic mitral annular velocity and time difference between mitral inflow and diastolic mitral annular velocity to early diastolic annular velocity for differentiating constrictive pericarditis from restrictive cardiomyopathy. J Am Soc Echocardiogr (2007) 20:738–43.[CrossRef][Web of Science][Medline]

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