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Jurnal Kardio - Cardiac MRI Pericarditis
Jurnal Kardio - Cardiac MRI Pericarditis
A R T I C LE I N FO A B S T R A C T
Keywords: Background: Evaluation of pediatric pericarditis depends on the physical examination, electrocardiography and
Pericarditis echocardiography. However, a multimodality imaging approach which includes cardiac magnetic resonance
Pediatrics imaging (MRI) has been adopted in the adult population. The use of such an approach in the pediatric population
Magnetic resonance imaging has not been studied well.
Cardiac imaging
Objective: The present study was intended to describe a single institution's experience with the use of cardiac
Constrictive pericarditis
MRI in the evaluation of pericarditis in the pediatric population.
Study Design: A retrospective review of patients who had a cardiac MRI before the age of 21 years, between 2005
and 2014, to evaluate for pericardial pathology including pericarditis, constrictive pericarditis, recurrent peri-
carditis and pericardial effusion was performed. Patients were excluded if the cardiac MRI was done for eva-
luation of pathologies other than those related to the pericardium. Patients with predominant myocarditis were
also excluded. The cardiac MRI and the echocardiograms were reviewed by a single blinded investigator.
Results: Twenty-one patients satisfied the inclusion criteria. The study population were predominantly male
(81%) older adolescents (mean age: 17 ± 3 years). The major indications for cardiac MRI included evaluation of
myocardial involvement in acute pericarditis, modulation of therapy in recurrent pericarditis and confirmation
of constriction. Cardiac MRI was comparable to echocardiogram in detecting constrictive physiology and was
useful in determining the presence of active pericardial inflammation. Systemic inflammatory diseases de-
monstrated higher values on quantification of late gadolinium enhancement.
Conclusion: We have reported on a relatively large series of pediatric patients with pericarditis evaluated by
cardiac MRI. Cardiac MRI may be a useful adjunct to conventional imaging in selected pediatric patients with
pericarditis.
1. Introduction magnetic resonance imaging (MRI) has been adopted in the adult po-
pulation [1,3,7]. Reports on the use of cardiac MRI for the evaluation of
Pericarditis is characterized by inflammation of the pericardium. It pediatric pericarditis have been limited to case reports. The present
can be acute, incessant, recurrent or chronic and can be complicated by study was intended to describe our single institution's experience with
pericardial effusion leading to cardiac tamponade or constrictive peri- the use of cardiac MRI in the evaluation of pericarditis in the pediatric
carditis [1–3]. Similar to adults, pericarditis in childhood can be sec- population.
ondary to infectious or non-infectious causes (rheumatologic, meta-
bolic, neoplastic or post-surgical) or can be idiopathic and can lead to 2. Patients and methods
complications [3–6]. Evaluation of pediatric pericarditis depends on the
physical examination, electrocardiography and echocardiography. This was a retrospective, single institutional study. Patients with
However, a multi-modality imaging approach, which includes cardiac ICD-9 codes for pericarditis, constrictive pericarditis, recurrent/chronic
Abbreviations: ASE, American Society of Echocardiography; MRI, magnetic resonance imaging; EACVI, European Association of Cardio Vascular Imaging
⁎
Corresponding author at: Pediatric Cardiology Fellow, The Heart Institute, Cincinnati Children's Hospital Medical Center, 3333 Burnet Avenue, MLC 2003, Cincinnati, OH 45229,
United States.
E-mail address: shankarbaskar@gmail.com (S. Baskar).
https://doi.org/10.1016/j.ppedcard.2018.05.003
Received 17 January 2018; Received in revised form 20 April 2018; Accepted 2 May 2018
1058-9813/ © 2018 Elsevier B.V. All rights reserved.
S. Baskar et al. Progress in Pediatric Cardiology 50 (2018) 39–45
pericarditis and pericardial effusion, who had cardiac MRI at the 2.3. Statistical data analysis
Cleveland Clinic before the age of 21 years, between 2005 and 2014,
were included in the study. Patients were excluded if the cardiac MRI After quantification, late gadolinium enhancement was compared
was done for evaluation of pathologies other than those related to the after grouping patients by diagnosis (acute pericarditis/myoper-
pericardium. Patients were also excluded if there was evidence of icarditis, effusive-constrictive pericarditis and recurrent pericarditis),
predominant myocarditis, which was defined as the presence of ven- etiology (viral/idiopathic and systemic) and course (resolved and re-
tricular dysfunction demonstrated by echocardiogram or cardiac MRI. current). Statistics was performed using SPSS 22 (IBM Corp. Released
Patients with ventricular dysfunction were excluded since the man- 2013. Armonk, NY: IBM Corp).
agement and evaluation of such patients with predominant myocarditis
differs from those with pericarditis [8]. This study was approved by the 3. Results
Cleveland Clinic institutional review board and need for informed
consent was waived. The study protocol conforms to the ethical A total of 66 patients were initially identified based on the inclusion
guidelines of the 1975 Declaration of Helsinki as reflected in a priori criteria. After exclusion of patients who had cardiac MRI done for
approval by the institution's human research committee. pathologies other than those involving the pericardium and those with
predominant myocarditis, 21 patients were included in the study. The
majority of patients were male (80%) who were predominantly diag-
2.1. Definitions nosed in adolescence (mean age: 16.8 ± 2.8 years) with a mean age at
cardiac MRI of 17.5 years (SD: 3 years). Four patients were diagnosed
Acute pericarditis was diagnosed if 2 or more of the following were with acute pericarditis/myopericarditis, 11 with recurrent pericarditis
present for < 3 months, 1. typical chest pain, 2. pericardial rub, 3. ty- and 6 with constrictive pericarditis/effusive-constrictive pericarditis.
pical ECG changes, and 4. new or worsening pericardial effusion [1]. (Table 1). Patients were subdivided into groups based on the pericardial
Myopericarditis was diagnosed in the presence of elevated troponin pathologic process at the time of first cardiac MRI and their char-
along with evidence of pericarditis and in the absence of ventricular acteristics with course are described below.
dysfunction by echocardiogram or cardiac MRI. Recurrent pericarditis
was defined as recurrence of pericarditis after an asymptomatic period
of ≥6 weeks. Constrictive pericardial physiology was suspected in the 3.1. Blinded review of cardiac MRI and echocardiogram
presence of respirophasic echocardiographic changes that included in-
spiratory ventricular septal motion towards the right ventricle (septal Cardiac MRI was useful in detecting pericardial inflammation evi-
bounce) on 2D and/or an abnormal filling pattern of the left ventricular dent by the presence of late gadolinium enhancement, when there was
and right ventricular in diastole (> 25% fall in mitral inflow velocity no evidence of pericarditis on the echocardiogram. Of the 21 patients in
and > 40% increase in tricuspid velocity in the first beat after in-
spiration) on Doppler echocardiography. The presence of diastolic
septal bounce with flattening of the interventricular septum during
inspiration and diastolic restraint were considered supportive of a Table 1
constrictive physiology on cardiac MRI [1]. Effusive-constrictive peri- Patient characteristics (n = 21).
carditis was diagnosed based on the presence of pericardial effusion and
Demographics No./percent
constrictive physiology.
Male 17 (81%)
Age at diagnosis (mean ± SD, years) 17 ±3
Age at index CMR (mean ± SD, years) 17 ±3
2.2. Imaging and data collection
Referred patients 12 (62%)
Presenting complaints
All patients had comprehensive echocardiograms with re- Chest pain 9 (43%)
spirometers based on guidelines for patients with pericardial diseases Evaluation of recurrent pericarditis 9 (43%)
[1]. Cardiac MRI was performed on a 1.5 T MRI scanner (Achieva XR, Other1 4 (19%)
Examination
Philips Medical Systems, Best, Netherlands), using commercially Normal 13 (62%)
available software, electrocardiographic triggering and dedicated Pericardial rub 4 (19%)
phased-array receiver coils as previously described [9]. Late gadolinium Elevated JVP 2 (10%)
enhancement images were obtained in long- and short-axis orienta- Other 2 2 (10%)
Laboratory evaluation
tions, 10 min after the intravenous injection of gadolinium
Elevated CRP 11/20 (55%)
(0.1–0.2 mmol/kg body weight) while using a phase-sensitive inversion Elevated WSR 8/20 (40%)
recovery technique, along with selection of inversion time for optimal Elevated troponins 2/14 (14%)
nulling of the myocardium. We used an 8 mm thickness slice with 2 mm ECG
gap. Electronic patient records were reviewed for presenting com- Normal 10 (48%)
ST-segment changes 4 (19%)
plaints, past history, clinical examination, laboratory tests for in- T-wave changes 4 (19%)
flammatory markers and myocardial injury (troponin) and electro- ST-segment and T-wave changes 1 (5%)
cardiogram (ECG). The echocardiogram and the cardiac MRI were Diagnosis after index CMR
independently reviewed by one of the investigator (K.P) who was Acute pericarditis 2 (10%)
Acute myopericarditis 2 (10%)
blinded to the final reported results and the patient's clinical informa-
Recurrent pericarditis 11 (52%)
tion. Late gadolinium enhancement was quantified using CMR42 soft- Constrictive pericarditis 3 (14%)
ware (Circle Cardiovascular Imaging Inc., Calgary, Canada) by a single Effusive-constrictive pericarditis 3 (14%)
validated observer (P.C.C) for patients with quantifiable evidence of Etiology
pericardial Late gadolinium enhancement as previously explained [10]. Idiopathic/viral 16 (76%)
Rheumatologic 3 (14%)
In brief, manual contouring of the pericardium was performed on short- Others3 2 (10%)
axis late gadolinium enhancement images, and signals > 6 SD from the
normal myocardium was quantified. 1. Shortness of breath, ascites, syncope and evaluation of constrictive peri-
carditis; 2. Tachycardia, hepatomegaly; 3. Others - trauma, histoplasmosis.
40
S. Baskar et al. Progress in Pediatric Cardiology 50 (2018) 39–45
Table 2
Characteristics of patients with acute pericarditis.
Diagnosis after index Age at CMR Time since onset of Troponin Echocardiography Index CMR LGE quantification Indication of Course
CMR (years) pericarditis (cm3) index MRI
1 Acute myopericarditis 19 3 days Elevated Small PEff Small PEff, pericardial 108 A Resolved
and myocardial LGE
2 Acute myopericarditis 20 1 month Elevated Small PEff Moderate PEff, 17 A Resolved
pericardial LGE
3 Acute pericarditis 17 2 years Normal Normal Pericardial LGE 65 B, C Resolved
4 Acute pericarditis 17 2 days Normal Normal Pericardial LGE 74 D Resolved
Abbreviations: LGE, Late gadolinium enhancement; PE, Pericardial effusion; A, Clinical evidence of myocarditis; B, Failure to respond to anti-inflammatory therapy;
C, Atypical clinical presentation; D, Suspicion of constrictive pericarditis.
Fig. 1. Serial cardiac MRI in a 17-year-old patient who had initially presented for evaluation of persistent symptoms due to acute pericarditis. A: Index cardiac MRI
using late gadolinium enhancement technique demonstrating active inflammation involving most of the pericardium (red arrow). B: Cardiac MRI of the same patient
after 3 months of therapy with colchicine and steroids demonstrating resolution of inflammation (red arrow).(For interpretation of the references to color in this
figure legend, the reader is referred to the web version of this article.)
the study, 9 patients (43%) had a normal echocardiogram with the 3.3. Recurrent pericarditis
cardiac MRI demonstrating evidence of pericardial inflammation by
late gadolinium enhancement. Seven of these patients had recurrent There were 11 patients with recurrent pericarditis at the time of
pericarditis and 2 patients with acute pericarditis and the etiology was their first cardiac MRI (Table 3), which was done at an average of 1 year
viral/idiopathic in all patients. Cardiac MRI was comparable to echo- from the time of initial diagnosis of pericarditis (Fig. 2). No specific
cardiogram in detecting constrictive physiology. etiology had been found in the majority of recurrent pericarditis pa-
tients (9 patients, 82%), and they were deemed to have idiopathic or
viral pericarditis. The etiology in the other 2 patients were histo-
3.2. Acute pericarditis
plasmosis and anti-phospholipid syndrome. Monitoring for the presence
and severity of pericardial inflammation in order to modulate man-
There were 4 patients with acute pericarditis, of whom 2 had
agement was the main indication for the index cardiac MRI. Based on
myocardial involvement in the form of myopericarditis (Table 2). No
the cardiac MRI results along with the clinical presentation, 8 of these
specific etiology was found in any of the patients, and pericarditis was
patients (73%) had their anti-inflammatory medications modified. Ad-
considered to be idiopathic in nature. Patient 3 had a cardiac MRI due
dition of prednisone to the treatment regimen or changes in the dosing
to atypical presentation with exercise limitation and persistent chest
of the prednisone were the most frequent therapeutic change.
pain 2 weeks after an episode of clinically diagnosed acute pericarditis.
He had an otherwise normal cardiac evaluation including echocardio-
gram. Cardiac MRI revealed minimal enhancement of the pericardium 3.4. Constrictive pericarditis/effusive-constrictive pericarditis
at the base of the ventricles consistent with pericardial inflammation
episode. Cardiac MRI was obtained in patient 4 due to concerns for A total of 6 patients demonstrated constrictive physiology on car-
constrictive physiology, which demonstrated late gadolinium en- diac MRI, and 3 of these had effusive-constrictive pericarditis (Table 4).
hancement of the pericardium without any constrictive physiology All the three patients with isolated constrictive pericarditis underwent
(Fig. 1). Our independent review of the echocardiogram did not reveal pericardial resection. Two patients with effusive-constrictive peri-
any evidence of constrictive physiology. carditis were found to have connective tissue disease and had evidence
41
S. Baskar et al. Progress in Pediatric Cardiology 50 (2018) 39–45
APLAS, Anti-phospholipid antibody syndrome; LGE, Later gadolinium enhancement; PEff, Pericardial effusion; D, Suspicion of constrictive pericarditis; E, Monitor the presence or severity of inflammation to modulate
of complex pericardial effusions with constrictive physiology on the
Indication for CMR
cardiac MRI. Following the cardiac MRI, additional anti-inflammatory
agents were recommended (steroids or azathioprine) for all 3 of the
E,D patients with effusive-constrictive pericarditis.
E
E
E
E
E
E
E
E
E
LGE quantification (cm3)
123
NA
NA
29
14
47
26
65
10
68
4. Discussion
Pericardial LGE
Pericardial LGE
Pericardial LGE
Pericardial LGE
Pericardial LGE
pericardial LGE
Moderate PEff
carditis.
Trivial PEff
The patients included in our study were older at the time of initial
Normal
Normal
Normal
Normal
Normal
Normal
Normal
Viral/Idiopathic
Viral/Idiopathic
Viral/Idiopathic
Viral/Idiopathic
Viral/Idiopathic
Viral/Idiopathic
Viral/Idiopathic
Viral/Idiopathic
Histoplasmosis
APLAS
0.5
0.5
1
2
1
1
1
1
1
2
1
vated troponins in pediatric patients with chest pain that can be seen in
Diagnosis after index CMR
42
S. Baskar et al. Progress in Pediatric Cardiology 50 (2018) 39–45
Fig. 2. Index cardiac MRI of patient with recurrent pericarditis demonstrating A: circumferential active inflammation by late gadolinium enhancement technique
(red arrow) B: T2-weighted short-tau inversion recovery imaging demonstrating active inflammation (red arrow).(For interpretation of the references to color in this
figure legend, the reader is referred to the web version of this article.)
evidence of peri-myocarditis. If the LV systolic function is reduced a secondary to the limited numbers, since previous work has shown
heart failure regimen may be initiated. For those patients with normal modest correlation [17]. Recent studies have also demonstrated that
LV systolic function, treatment is done with standard anti-inflammatory pericardial late gadolinium enhancement might predict reversibility of
therapy [3]. constriction by anti-inflammatory medications, however further studies
Recurrent pericarditis is rare in children and can have an un- are warranted [18].
predictable course [6,11]. The present report included patients pre- Although studies directly comparing cardiac MRI and echocardio-
dominantly with idiopathic recurrent pericarditis with a minority gram in the diagnosis of pericardial pathology are lacking, there is
having associated systemic diseases. Pericardial enhancement in car- strong evidence for the role of cardiac MRI in the detecting pericardial
diac MRI can provide supportive evidence and may be useful in ruling pathology. Similar to the ASE and EACVI guidelines on the multi-
out pericardial inflammation in patients with recurrent pericarditis modality imaging of pericarditis in adults, we found that cardiac MRI
presenting with atypical chest pain [1]. Cardiac MRI guided therapy for was used in cases with suspected myocarditis, modulating therapy in
recurrent pericarditis has been shown to decrease recurrences and ex- recurrent pericarditis and confirming constrictive pericarditis. Our in-
posure to steroids [13,16]. dependent review of the prior studies, demonstrate that half of the
In constrictive pericarditis, the pericardium becomes thickened and patients with active inflammation of the pericardium might have a
inelastic, limiting the diastolic filling of the ventricles. Cardiac MRI normal echocardiogram and would be detected by late gadolinium
demonstrates thickening of the pericardium, enhancement of peri- enhancement on cardiac MRI. As expected, cardiac MRI and echo-
cardium in some patients, hemodynamic and respirophasic alterations, cardiogram were comparable in detecting constrictive physiology.
and pericardial-myocardial adherence on myocardial tagging. Based on
the increased thickness and presence of inflammation of pericardium, 5. Study limitations
Cardiac MRI can be useful in differentiating restrictive cardiomyopathy
from constrictive pericarditis [1,7]. Both the ASE and EACVI consider This study has some notable limitations, which includes a relatively
cardiac MRI to be useful in the evaluation of patients with an echo- small and heterogeneous group of patients, biases associated with a
cardiogram suspicious for constrictive pericarditis and for follow-up of retrospectively collected data on clinical characteristics and treatment.
these patients and prior to undergoing surgical pericardial intervention. There might also be a selection bias due to the most severely affected
Similar to constrictive pericarditis, in effusive-constrictive pericarditis patient being referred for cardiac MRI and the absence of specific in-
cardiac MRI is considered helpful in confirming diagnosis when sus- dications in the pediatric population resulting in referral for cardiac
pected by echocardiogram and for follow-up. Cardiac MRI may be MRI based on the physician preference. A small sample size, sig-
useful in better delineating pericardial thickness in the face of peri- nificantly decreases the accuracy of the statistical analysis associated
cardial effusion. Since the management of constrictive pericarditis may with late gadolinium enhancement quantification. Finally, we did not
include surgical intervention, prompt identification of constrictive report on the T2 weighted STIR images on pericardial edema, since the
pericarditis is important in patients with an inconclusive echocardio- brightness of images could be influenced by concomitant pericardial
gram. effusion. However, future prospective studies should assess the value of
Late gadolinium enhancement quantification is a novel method of both edema (T2 STIR), inflammation (LGE) and its quantification as an
objectively defining the degree of inflammation [10,13]. Although we incremental value in the prognosis of these patients.
have very limited number of patients, we identified a trend to have
higher late gadolinium enhancement among patients with systemic 6. Conclusion
diseases such as SLE. However, there was no significant correlation
between inflammatory markers and LGE quantification. This is likely We have reported on a relatively large case series of pediatric
43
S. Baskar et al. Progress in Pediatric Cardiology 50 (2018) 39–45
B, Failure to respond to anti-inflammatory therapy; D, Suspicion of constrictive pericarditis; F, to distinguish constriction from restriction; G, Evaluation of presence of inflammation in effusive-constrictive pericarditis;
Indication of index
D, G
D, G
B, G
MRI
D, F
D
Viral/Idiopathic
Viral/Idiopathic
Viral/Idiopathic
MCTD/SLE
Etiology
Trauma
overlap
SLE
Follow-up
Recurrent
Improved
Improved
Improved
Improved
Improved
Pericardial
Pericardial
Pericardial
resection
resection
resection
NA
NA
NA
274
NA
NA
NA
23
Funding source
Complex PEff, pericardial thickening, constrictive
None.
Complex PEff, pericardial LGE, constrictive
Pericardial thickening, Pericardial LGE,
Conflict of interest
physiology, LGE - not performed
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