Constrictive Pericarditis with Biventricular Systolic Dysfunction in a Pediatric Patient

Plicy Perez-Kersey MD^{1, 2}, Christina L. Greene MD^3,4, Nicholas K. Brown MD<sup>1, 2

1</sup>Seattle Children’s Hospital Heart Center; Seattle, WA
²University of Washington School of Medicine, Department of Pediatrics, Division of Cardiology; Seattle, WA
³Children’s Hospital of Orange County Heart Institute; Orange, CA
⁴University of California, Los Angeles; Los Angeles, CA

 

Clinical History

A 17-year-old male presented with a six-month history of fatigue, unintentional weight loss, cough, and dyspnea on exertion following a two-month trip to West Africa. Upon return from his trip, he was diagnosed with a severe malaria infection and required hospitalization for IV antimicrobials. After that hospitalization, he developed the aforementioned symptoms which progressed over time. The cardiac exam was notable for tachycardia, narrow pulse pressure, and prominent pulsus paradoxus. Labs included a negative troponin and a mildly elevated brain natriuretic peptide (BNP) of 140 pg/mL (0-41 pg/mL). Transthoracic echocardiogram (TTE) showed a hyperechoic and severely thickened pericardium (9-10 mm), mild to moderate biventricular systolic dysfunction with a diastolic septal bounce, and moderate mitral and tricuspid valve regurgitation (Movie 1). A computed tomography (CT) scan of the chest confirmed a severely thickened pericardium without pericardial calcifications or a pericardial effusion, as well as multifocal consolidations, lymphadenopathy, and bilateral large pleural effusions (Movie 2). Bilateral chest tubes were placed, but the effusions were loculated and persisted over time. Although his QuantiFERON-TB Gold test was positive, all other testing, including a pleural biopsy performed during chest tube placement, was negative for active tuberculosis. Based on a high index of clinical suspicion, he was initiated on standard four-drug therapy with rifampin, isoniazid, pyrazinamide, and ethambutol (RIPE) for presumed disseminated tuberculosis, as well as a ten-week course of high-dose steroids for suspected tuberculosis-related constrictive pericarditis. 

Movie 1. TTE images. Parasternal short-axis view (A) showing hyperechoic and severely thickened pericardium, and mild to moderate biventricular systolic dysfunction with a diastolic septal bounce. Apical 4-chamber view (B) showing moderate mitral and tricuspid valve regurgitation.

Movie 2. CT scan of the chest in the coronal plane from posterior to anterior demonstrating severely thickened pericardium without pericardial calcifications or a pericardial effusion, as well as multifocal consolidations, lymphadenopathy, and bilateral large pleural effusions.

 

CMR Findings

Cardiac magnetic resonance imaging (CMR) was performed on a 1.5T Avanto Fit (Siemens Healthineers, Erlangen, Germany) after four weeks of therapy, and demonstrated circumferential adherence of thickened pericardium to the underlying myocardium without a pericardial effusion, as well as mild to moderate biventricular systolic dysfunction (left ventricular ejection fraction (LVEF) 42%, right ventricular ejection fraction (RVEF) 35%) by cine balanced steady state free precession (bSSFP) imaging. Additionally, real-time cine bSSFP imaging verified evidence of ventricular interdependence with a prominent septal bounce and significant flattening with inspiration (Figure 1, Movie 3). By 2D phase sensitive inversion recovery (PSIR) imaging, there was diffuse pericardial late gadolinium enhancement (LGE) without myocardial involvement (Figure 2). There was no obvious myocardial or pericardial edema based on T2 dark blood short tau inversion recovery (STIR) imaging. Strain analysis using tissue tracking (cvi42, Circle Cardiovascular Imaging, Calgary, Alberta, Canada) showed decreased global longitudinal strain (GLS -4.2%; normal <-18 to -20%) with regionally decreased global circumferential strain (GCS -9.9%; normal <-20%) and global radial strain (GRS 13.4%; normal 35-59%) values in the regions with thickest pericardium along the mid to apical lateral wall segments (Figure 3, Movie 4).[1,2]

Movie 3. Four-chamber (A) and short-axis (B) real-time cine bSSFP imaging shows bilateral pleural effusions, thickened pericardium, mild to moderate biventricular systolic dysfunction, and a prominent septal bounce.

Figure 1. Short-axis real-time still frames during inspiration (A) and expiration (B) demonstrate significant septal flattening with inspiration, consistent with interventricular dependence.

Figure 2. T2 dark blood STIR imaging short axis (A) did not show evidence of myocardial or pericardial edema. Four-chamber (B) and short axis (C) PSIR imaging showed circumferential pericardial LGE without myocardial involvement.

Figure 3. Decreased global longitudinal strain (C, -4.2%) with decreased regional circumferential (B) and radial (A) strain along the anterolateral wall in regions with thickest pericardium.

Movie 4. Strain analysis was performed by feature tracking (A) and was then translated to a 3D map of radial strain (B), demonstrating decreased radial motion of both ventricles. The septum and right ventricular base were relatively preserved compared to the lateral walls which were tethered to the pericardium.

 

Conclusion

In this case, CMR served an important complimentary role in highlighting the pericardial thickening/fibrosis and constrictive physiology via non-invasive means, consistent with the patient’s clinical presentation and findings by other imaging modalities. CMR allowed us to distinguish pericardial thickening from a pericardial effusion as the cine bSSFP imaging showed a fixed thickened pericardium rather than shifting fluid, T2 mapping did not show pericardial edema, and PSIR imaging showed a bright pericardium. Through various sequences, CMR also emphasized the severity and extent of the patient’s pericardial disease, which was associated with both diastolic and systolic biventricular dysfunction. Notably, CMR confirmed the absence of myocardial inflammation and fibrosis, thereby ruling out other processes such as myocarditis or infiltrative diseases.

Due to evidence of persistent constrictive physiology following one month of therapy, complete pericardiectomy and right pleural decortication were performed under mild hypothermic cardiopulmonary bypass (122 min). Intra-operatively, a severely thickened pericardium (>15 mm) encased the heart and was found to be adherent to the underlying myocardium of both ventricles, as suspected from regional strain imaging by CMR (Figure 4). Following pericardiectomy, there was immediate auto-diuresis with normalization of biventricular systolic function by post-operative transesophageal echocardiography. Pathology of the pericardial tissue confirmed the presence of Mycobacterium tuberculosis complex DNA as well as necrotizing granulomatous lymphadenitis. After consultation with the local public health department, the planned treatment duration was six months, including at least two months of RIPE therapy followed by rifampin and isoniazid for the remainder of the treatment course. At a one-month follow-up visit, the patient reported feeling well without any residual symptoms. 

Figure 4. Gross intra-operative specimen. A severely thickened pericardium (>15 mm) encased the heart and was adherent to the underlying myocardium of both ventricles.

 

Perspective

Constrictive pericarditis is caused by thickening and fibrosis of the pericardium leading to a non-compliant encasement of the intracardiac structures with pressure dissociation from the remainder of the intrathoracic compartment.[3] While tuberculosis is the leading cause of constrictive pericarditis in adults living in developing nations, the diagnosis is rare in children and adolescents worldwide.[4,5] Constrictive pericarditis typically presents with signs and symptoms of diastolic dysfunction with preserved systolic function.[6] As the disease progresses from an acute/subacute to a more chronic phase, the pericardium can become calcified with myocardial extension of fibrosis or thinning/atrophy.[3,7] As our patient did not have significant enhancement on T2-weighted STIR imaging, this was likely a more chronic process, which fits with the presentation timeline and negative findings on some of the initial testing for active tuberculosis. However, the significant biventricular systolic dysfunction by CMR seen in our patient is unusual in the absence of obvious myocardial involvement, as evidenced by a negative troponin, normal wall thickness, and lack of myocardial LGE. We identified one prior case report in an adult patient with effusive-constrictive pericarditis and biventricular systolic dysfunction, but to our knowledge, pediatric tuberculous constrictive pericarditis associated with significant biventricular systolic dysfunction is rare.[8] The etiology of systolic dysfunction in our patient was likely related to regional adhesions of the thickened pericardium to the underlying myocardium as systolic dysfunction completely resolved immediately following pericardiectomy.

CMR can also be particularly useful in differentiating constrictive pericarditis from restrictive cardiomyopathy, as both conditions may present with similar clinical symptoms and echocardiographic findings. In restrictive cardiomyopathy, real-time cine imaging typically does not demonstrate marked respiratory septal shift or enhanced ventricular interdependence because the pericardium remains compliant. Myocardial tissue characterization findings of diffuse myocardial fibrosis, infiltrative patterns of late gadolinium enhancement, increased native T1 values, or elevated extracellular volume may favor restrictive cardiomyopathy. In contrast, constrictive pericarditis is more commonly associated with pericardial thickening, enhancement, calcification (better demonstrated by CT), and preserved myocardial tissue characteristics.  Lastly, regional strain abnormalities like the ones seen in our case have been described in adult patients as a helpful discriminator between constrictive pericarditis and restrictive cardiomyopathy, with a significant improvement in circumferential strain following pericardiectomy.[9] In summary, CMR played an important role in this case by characterizing the disease process/timeline, solidifying the diagnosis, and informing the treatment plan.

Click here to view the entire CMR on CloudCMR.

 

References

1. Yang W, Xu J, Zhu L, Zhang Q, Wang Y, Zhao S, Lu M. Myocardial Strain Measurements Derived From MR Feature-Tracking: Influence of Sex, Age, Field Strength, and Vendor. JACC Cardiovasc Imaging. 2024 Apr;17(4):364-379.
2. Voges I, Negwer I, Caliebe A, Boroni Grazioli S, Daubeney PEF, Uebing A, Pennell DJ, Krupickova S. Myocardial Deformation in the Pediatric Age Group: Normal Values for Strain and Strain Rate Using 2D Magnetic Resonance Feature Tracking. J Magn Reson Imaging. 2022 Nov;56(5):1382-1392.
3. Al-Kazaz M, Klein AL, Oh JK, Crestanello JA, Cremer PC, Tong MZ, Koprivanac M, Fuster V, El-Hamamsy I, Adams DH, Johnston DR. Pericardial Diseases and Best Practices for Pericardiectomy: JACC State-of-the-Art Review. J Am Coll Cardiol. 2024 Aug 6;84(6):561-580.
4. Venuti L, Condemi A, Albano C, Boncori G, Garbo V, Bagarello S, Cascio A, Colomba C. Tuberculous Pericarditis in Childhood: A Case Report and a Systematic Literature Review. Pathogens. 2024 Jan 26;13(2):110.
5. Giliomee LJ, Doubell AF, Robbertse PS, John TJ, Herbst PG. Novel role of cardiovascular MRI to contextualise tuberculous pericardial inflammation and oedema as predictors of constrictive pericarditis. Front Cardiovasc Med. 2024 Mar 18;11:1329767. 
6. Geske JB, Anavekar NS, Nishimura RA, Oh JK, Gersh BJ. Differentiation of Constriction and Restriction: Complex Cardiovascular Hemodynamics. J Am Coll Cardiol. 2016 Nov 29;68(21):2329-2347.
7. Conte E, Agalbato C, Melotti E, Marchetti D, Schillaci M, Ratti A, Ippolito S, Pancrazi M, Perone F, Dalla Cia A, Pepi M, Pontone G, Imazio M, Brucato A, Chetrit M, Klein A, Andreini D. The Contemporary Role of Cardiac Computed Tomography and Cardiac Magnetic Resonance Imaging in the Diagnosis and Management of Pericardial Diseases. Can J Cardiol. 2023 Aug;39(8):1111-1120.
8. Haq IU, Davies DR, Yao R, Bratt A, Sinak LJ, Singh M. Effusive-Constrictive Tuberculosis Pericarditis with Biventricular Systolic Dysfunction. CASE (Phila). 2022 May 13;6(5):212-217.
9. Kusunose K, Dahiya A, Popović ZB, Motoki H, Alraies MC, Zurick AO, Bolen MA, Kwon DH, Flamm SD, Klein AL. Biventricular mechanics in constrictive pericarditis comparison with restrictive cardiomyopathy and impact of pericardiectomy. Circ Cardiovasc Imaging. 2013 May 1;6(3):399-406.

Case prepared by:
Jason N. Johnson, MD MHS
Editor-in-Chief, Cases of SCMR
Le Bonheur Children’s Hospital, The University of Tennessee Health Science Center, St. Jude Children’s Research Hospital