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Transcript
Constrictive Pericarditis in the Modern Era
Evolving Clinical Spectrum and Impact on Outcome
After Pericardiectomy
Lieng H. Ling, MBBS, MRCP; Jae K. Oh, MD; Hartzell V. Schaff, MD; Gordon K. Danielson, MD;
Douglas W. Mahoney, MSc; James B. Seward, MD; A. Jamil Tajik, MD
Downloaded from http://circ.ahajournals.org/ by guest on June 14, 2017
Background—The clinical spectrum of constrictive pericarditis (CP) has been affected by a change in incidence of
etiological factors. We sought to determine the impact of these changes on the outcome of pericardiectomy.
Methods and Results—The contemporary spectrum of CP in 135 patients (76% male) evaluated at the Mayo Clinic from
1985 to 1995 was compared with that of a historic cohort. Notable trends were an increasing frequency of CP due to
cardiac surgery and mediastinal radiation and presentation in older patients (median age, 61 versus 45 years).
Perioperative mortality decreased (6% versus 14%, P50.011), but late survival was inferior to that of an age- and
sex-matched US population (5768% at 10 years). The long-term outcome was predicted independently by 3 variables
in stepwise logistic regression analyses: (1) age, (2) NYHA class, and most powerfully, (3) a postradiation cause. Of
90 late survivors in whom functional class could be determined, functional status had improved markedly (2.660.7 at
baseline versus 1.560.8 at latest follow-up [P,0.0001]), with 83% being free of clinical symptoms.
Conclusions—The evolving profile of CP, with increasingly older patients and those with radiation-induced disease in the
past decade, significantly affects postoperative prognosis. Long-term results of pericardiectomy are disappointing for
some patient groups, especially those with radiation-induced CP. By contrast, surgery alleviates or improves symptoms
in the majority of late survivors. (Circulation. 1999;100:1380-1386.)
Key Words: pericarditis n prognosis n surgery
C
onstrictive pericarditis (CP), although uncommon, commands substantial clinical interest because of the perceived potential for surgical cure. In the past 15 years, several
reports have highlighted changes in the spectrum of CP in the
United States, characterized chiefly by a declining incidence
of tuberculous pericarditis and an increase in the frequency of
cases resulting from therapeutic mediastinal radiation and
cardiac surgery.1–3 Few data, however, exist on the impact of
these changes on outcome after pericardiectomy. In addition,
outcome analysis has focused predominantly on a mortality
end point; markers for recurrent congestive heart failure
(CHF) symptoms, for example, are unknown.
We hypothesized that the observed changes in the clinical
spectrum of CP influence postoperative prognosis in the
current era. Because the epidemiology of CP is strongly
influenced by geography and referral bias, changes in disease
patterns are most appropriately defined vis-à-vis a historic
cohort from the same institution. Accordingly, we reviewed
the cases of patients with proven CP evaluated at the Mayo
Clinic in the past decade and identified contemporary trends
in relation to 231 patients examined at our institution from
1936 through 1982.4
Methods
All patients with the diagnosis of CP in the medical and surgical
indexes of the Mayo Clinic from January 1985 through June 1995
were screened. Only patients with CP confirmed at surgery or
autopsy were included.
During this period, 135 patients were identified: 133 at surgery
and 2 at autopsy. Case histories were reviewed, and clinical findings
by a staff cardiologist were recorded. Follow-up of patients was done
with a mailed questionnaire, hospital records, and telephone calls to
the patients, their relatives, and their physicians. The circumstances
and causes of death recorded in death certificates were verified
whenever possible with the patient’s physician or the coroner who
certified the death. Concomitant medical illnesses were assigned
weights and summed as a comorbidity index for survival analyses.
Definitions
Radical pericardiectomy was defined as wide excision of the pericardium anteriorly between the 2 phrenic nerves and from the great arteries
superiorly to the diaphragm inferiorly, posterior to the left phrenic nerve
(which is left on a pedicle) to the left pulmonary veins, and including the
pericardium on the diaphragmatic and posterior surfaces of the ventricles.4 Constricting layers of epicardium were also removed. The atria
and venae cavae were decorticated only if the dissection could be
accomplished easily, without risk of hemorrhage.4,5 Pericardiectomy
was considered partial if both ventricles could not be decorticated
completely because of dense myopericardial adhesions or calcification.
Received December 8, 1998; revision received June 28, 1999; accepted July 7, 1999.
From the Division of Cardiovascular Diseases and Internal Medicine (L.H.L., J.K.O., J.B.S., A.J.T.), the Division of Thoracic and Cardiovascular
Surgery (H.V.S., G.K.D.), and the Section of Biostatistics (D.W.M.), Mayo Clinic and Mayo Foundation, Rochester, Minn. Dr Ling is now at the Cardiac
Department, National University Hospital, 5 Lower Kent Ridge Rd, Singapore 119074.
Reprint requests to Dr Jae K. Oh, Mayo Clinic, 200 First St SW, Rochester, MN 55905.
© 1999 American Heart Association, Inc.
Circulation is available at http://www.circulationaha.org
1380
Ling et al
Constrictive Pericarditis
1381
TABLE 1. Candidate Predictors of Outcome Used in Univariate
Proportional Hazards Analyses
Clinical
Laboratory
Intraoperative
Age
Serum creatinine
Completeness of
Sex
Serum sodium
pericardiectomy*
NYHA class
Serum bilirubin
Concomitant CABG or
Symptom duration
Serum transaminases
valve surgery
Peripheral edema
Serum albumin
Requirement for
Ascites
Atrial fibrillation or atrial flutter cardiopulmonary bypass*
Pericardial knock
Low ECG voltage
Radiation cause
Cardiothoracic ratio
Known CAD†
Calcification on CXR
Smoking history
Comorbidity index
Diuretic dose‡
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CABG indicates coronary artery bypass graft surgery; CAD, coronary artery
disease; and CXR, chest radiograph.
*Variables not used as baseline predictors in multivariate analyses as
generally unpredictable before pericardiectomy.
†Includes patients with previous documented myocardial infarction and coronary
bypass surgery or coronary artery narrowing (diameter stenosis .70%) demonstrated by “screening” coronary angiography before pericardiectomy.
‡Defined as dose in milligrams of furosemide or bumetanide, multiplied by a
conversion factor of 40, and stratified as no diuretic use, #80 mg, or .80 mg.
For uniformity with other studies, perioperative death was defined
as that occurring within 30 days after surgery. However, all deaths
within the same hospitalization as for surgery were included in
analysis of predictors of perioperative death. Cardiac-related death
was defined as death due to cardiac causes, such as progressive CHF
or sudden death. Sudden unexpected death was defined according to
the criteria of Hinkle and Thaler,6 whereas sudden expected death
was abrupt death occurring in the setting of progressive CHF or an
episode of CHF in the preceding 12 months. A poor cardiovascular
outcome was defined as any combination of the end points of
perioperative death, late cardiovascular death, and new-onset or
recurrent New York Heart Association (NYHA) class III to IV CHF.
Statistical Analysis
Categorical data, expressed as percentages, were compared by the t
test or x2 test, as appropriate. Continuous variables, expressed as
mean6SD or median values, were compared by the 2-sample
Wilcoxon rank sum test. The rates of all-cause mortality, perioperative death, late survival, late cardiac-related death, recurrent NYHA
class III to IV CHF, and a poor late cardiovascular outcome were
estimated by the Kaplan-Meier method. Late survival curves were
compared with those of a normal 1990 US population matched for
age and sex by the log-rank test. Baseline predictors of subsequent
sudden death were identified by univariate Cox proportional hazards
analysis initially performed on candidate variables (Table 1). Variables univariately significant on the basis of a threshold value of
P#0.15 were entered stepwise into a multivariable logistic regression model to confirm independent predictive value. A value of
P,0.05 was considered statistically significant.
Results
Incidence and Causes
The causes of CP in the 135 study patients and the 231
patients of the historic series are depicted in Figure 1. An
indeterminate cause of CP was significantly less common in
the contemporary cohort (33% versus 73%, P,0.0001). The
3 most common identifiable causes were cardiac surgery
(18%), pericarditis (16%), and mediastinal irradiation (13%).
Patients who had received radiotherapy most commonly
had Hodgkin’s lymphoma (8 patients) or breast cancer (7
Figure 1. Causes of 366 cases of CP confirmed at surgery (or
autopsy) at the Mayo Clinic in the 2 periods surveyed: 1936
through 1982 (n5231) and 1985 to June 1995 (n5135).
patients), a median of 13.1 years (range, 1.0 to 40.6 years)
before pericardiectomy. Of the patients with connective tissue
disease or arthritides, 6 had rheumatoid arthritis and 1 each
had rheumatic fever (with myopericarditis), polymyalgia
rheumatica, psoriatic arthropathy, and Still’s disease. Infectious causes identified were fungal pericarditis (histoplasmosis and candidiasis) in 2 patients and tuberculosis and
Whipple’s disease in 1 patient each. Miscellaneous causes
included myeloproliferative disorders, malignancy, trauma,
asbestosis, drug-induced causes, and complicated pacemaker
lead replacement. CP was diagnosed in 2 patients at autopsy:
1 had had cardiac surgery and the other had tumor encasement by non-Hodgkin’s lymphoma.
Clinical Characteristics
Clinical characteristics of the study population are shown in
Table 2. The presentation was CHF in 90 patients (67%),
chest pain in 11 (8%), abdominal symptoms in 8 (6%),
cardiac tamponade in 7 (5%), atrial arrhythmia in 6 (4%), and
frank liver disease in 5 (4%). In the other 8 patients, the initial
presentation included postoperative low cardiac output state,
recurrent pleural effusion, transient ischemic attack, and
syncope. The median symptomatic duration before pericardiectomy was 11.7 months (range, 3 days to 29.1 years).
Chronicity of symptoms characterized patients with an indeterminate cause of CP (mean, 17.4 months).
Surgery
Pericardiectomy was performed in 132 of the 135 patients.
One patient who had previously had radiotherapy underwent
triple coronary artery bypass graft surgery and a tricuspid
annuloplasty, but the patient’s condition deteriorated intraoperatively and pericardiectomy was not performed. Radical
pericardiectomy was performed in 117 patients (89%). Pericardial resection was deemed incomplete in the other 15
patients (11%). Ultrasonic debridement of calcified pericardium was performed in 12 patients (9%), coronary artery
bypass grafting was performed in 10 patients (8%), valve
replacement or repair in 5 (4%), and a combined coronary
artery-valve procedure, atrial septal defect closure, resection
of subaortic stenosis, and right ventricular outflow tract
enlargement in 1 patient (0.8%) each. Cardiopulmonary
bypass was used in 45 patients; the mean extracorporeal
circulation time was 88658 minutes.
1382
Circulation
September 28, 1999
TABLE 2. Preoperative Characteristics of 135 Patients With CP Diagnosed From
January 1985 Through June 1995 Compared (Where Data Available) With a
Historic Mayo Cohort From 1936 Through 1982
1985–1995 Cohort (n5135)
Characteristic
No. or Value
%
1936 –1982 Cohort (n5231)
No. or Value
%
P
Age, y
56616
NA
zzz
Median
Mean
61
45
zzz
Range
11–78
0.8–83
Male
103
76
171
74
0.63
Symptom duration, mo
Median
11.7
14.0
Range
0.1–349
1.0–348
NYHA class
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I–II
40
30
72
31
III–IV
93
69
159
69
2
1
0
0
Indeterminate
0.83
Elevated JVP
119*
93*
229
99
0.001
Peripheral edema
103
76
162
70
0.20
Hepatomegaly
71
53
169
73
,0.0001
Pericardial knock or S3
63
47
106
46
0.89
Ascites
50
37
139
60
,0.0001
Pleural effusion
47
35
NA
zzz
zzz
Kussmaul’s sign
28
21
NA
zzz
zzz
Pulsus paradoxus
25
19
NA
zzz
zzz
Pericardial rub
22
16
NA
zzz
zzz
Known CAD
26
20
NA
zzz
zzz
Diuretic use
68
50
NA
Atrial arrhythmia
22
16
68
zzz
29
zzz
,0.0001
Low QRS voltage
37
27
92
40
0.083
Pericardial calcification
34
25
92
40
0.007
JVP indicates jugular venous pressure; CAD, coronary artery disease; and NA, not available.
*Indeterminate in 7 of 135 patients.
Overall Survival
Late Survival
Information about death was available for all except 1 patient
(99%) and for other end points in 129 patients (98%). In
patients dismissed from the hospital, the mean follow-up
period was 3.963.0 years (maximum, 12.2 years). There
were 39 deaths (30%), of which 26 occurred after hospital
dismissal. At 5 and 10 years, overall survival was 7165%
and 5268%, respectively. Independent determinants of overall survival were age, previous radiotherapy, NYHA class,
and serum concentration of sodium (Table 3).
At last follow-up, 93 of the 119 operative survivors (78.2%)
were alive. Survival at 5 and 10 years was 7865% and
5768%, respectively, and was inferior to that of an age- and
sex-matched US population (log-rank P,0.001) (Figure 2).
This difference was not observed for the historic cohort,
which had an identical proportion of patients with advanced
NYHA symptoms.4 In stepwise multivariate analysis, independent predictors of late survival were age, NYHA class,
and previous radiation (Table 3 and Figure 3). The difference
from expected survival was still statistically significant even
when patients with radiation disease were excluded (log-rank
P50.016) (Figure 2).
Perioperative Deaths
The 30-day perioperative mortality was 6% (8 of 132). This
compares favorably with the 14% perioperative mortality in
the historic cohort (x256.40, P50.011). A total of 13 patients
died in hospital. The principal causes of death were low
output state in 6 patients, sepsis in 3, uncontrolled hemorrhage in 2, and renal failure and respiratory insufficiency in 1
each. Of these 13 patients, pericardiectomy was incomplete in
6 (univariate P,0.0001 for prediction of perioperative
death), and cardiopulmonary bypass was required in 9.
Late Cardiovascular Deaths
The late deaths in 26 patients resulted from cardiac-related
causes in 17, pleuropulmonary disease in 2, noncardiac
illness in 6, and an unknown cause in 1. None of the patients
who had radiation therapy died of recrudescent neoplastic
disease.
Ling et al
TABLE 3. Multivariate Predictors of Outcome After
Pericardiectomy in 132 Patients With CP
Adjusted
Hazard Ratio
95% CI
P
Age
1.07
1.04–1.10
,0.0001
NYHA class
2.43
1.22–4.86
0.012
Previous radiation
5.13
2.49–10.56
,0.0001
1.11
1.04–1.18
0.001
Age
1.08
1.04–1.12
,0.0001
NYHA class
3.99
1.76–9.08
0.0009
11.80
4.57–30.44
Age
1.07
1.03–1.12
NYHA class
3.38
1.25–9.19
0.017
20.74
6.77–63.52
,0.0001
Age
1.04
1.01–1.07
0.010
Previous radiation
9.47
4.19–21.39
,0.0001
Ascites
2.19
1.03–4.67
0.042
Outcome
Overall survival
No. of
Events
39
Serum sodium
Late survival
26
Previous radiation
Late CV death
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Previous radiation
Late NYHA class III–IV CHF
,0.0001
17
0.0009
30
CV indicates cardiovascular; CHF, congestive heart failure.
Cardiac-related deaths were due to progressive CHF in 14
patients (4 terminated in sudden expected death) and were
sudden and unexpected in 3. The cumulative incidence of
cardiovascular deaths was 1464% and 3569% at 5 and 10
years, respectively. Independent predictors of late cardiacrelated deaths were previous radiotherapy, NYHA class III to
IV symptoms, and age (Table 3).
Late NYHA Class III to IV CHF Symptoms
Recurrent or new NYHA class III to IV symptoms supervened in 37 of 119 patients (31%) at some stage of late
follow-up. The median time to onset of new or recurrent CHF
symptoms was 7.1 months (range, 0.4 to 137.1 months).
Three patients were reoperated on for recurrent CP. The
5- and 10-year incidence of late NYHA class III to IV CHF,
2565% and 4169%, respectively, parallels that of late
Constrictive Pericarditis
1383
cardiovascular deaths, consistent with the observation that
most severely symptomatic patients died eventually of a
cardiac-related cause. Multivariate predictors of late CHF
were age, radiation, and the presence of ascites (Table 3).
Of the 89 patients alive at latest follow-up with complete
follow-up information, 74 (83%) were either asymptomatic or
mildly symptomatic (Figure 4). Mean functional class was
2.660.7 at baseline, compared with 1.560.8 after pericardiectomy (mean change, 1.160.9, P,0.0001).
Freedom From Poor Cardiovascular Outcome
Of 129 patients with complete follow-up information, 75
(58%) were alive and free of CHF at latest follow-up. At 5
and 10 years, 7065% and 4368% of patients, respectively,
were free of a poor cardiovascular outcome. This end point
occurred in 15 of 17 patients (88%) who had received
radiation, including 13 deaths, and in 31 of 112 patients
(28%) without a radiation basis for CP (P,0.0001). The
dismal outcome for patients with radiation disease was
reflected in a 1266% freedom from any cardiovascular event
by 5 years.
Discussion
In comparing our contemporary patients with a historical
cohort that had pericardiectomy at the Mayo Clinic4 —a total
experience spanning nearly 6 decades—several trends were
observed: (1) patients in the last decade were older (median
age, 61 years versus 45 years), (2) previous open heart
surgery and mediastinal irradiation emerged as important
causes of CP, (3) operative mortality was significantly lower,
but (4) late survival was not as good as expected.
The increasing importance of iatrogenic causes of CP2,3,7–9
is reflected in the marked decline in the proportion of
indeterminate causes in the present series. Postoperative CP
may not be as uncommon as previously believed.2,7,9,10 At the
current level of 725 000 such procedures performed annually
in the United States, a conservative 0.3% incidence could
yield up to 2200 new cases annually. Therapeutic radiation
could also remain a significant cause of pericardial disease.
Cardiac structures are exquisitely sensitive to the effects of
radiation, which often become manifest decades later.11,12 In
addition, improved cancer cure rates have resulted in greater
longevity and thus the likelihood of developing cardiovascular sequelae.13 Active tuberculous CP, present in 6.1% of
patients in the series of McCaughan et al,4 was rare in our
patients (0.7%). This declining trend is in contradistinction to
recent reports from other geographic regions,14 –16 emphasizing again the heterogeneity of disease patterns.
Operative Mortality
Figure 2. Late survival (perioperative deaths excluded) after
pericardiectomy for CP compared with that of an age- and sexmatched US population (left) and after patients with radiationinduced disease were excluded (right). Numbers at bottom represent percentage of expected survival for specified intervals.
The decline in operative mortality at our institution from 25%
in the earlier half of this century5 to 6% at present probably
is related to improvements in surgical technique, anesthesia,
and postoperative care. Despite the inclusion of older patients
and those with radiation-induced CP, our results compare
favorably with the 6% to 19% rate of larger series published
after 1985.1–3,14,15,17
1384
Circulation
September 28, 1999
Figure 3. Late survival stratified by age #55
years versus .55 years (left), NYHA class I to III
versus class IV (middle), and nonradiation versus radiation causes (right). Baseline NYHA
class was indeterminate in 2 patients.
Late Survival
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Unlike our earlier experience, late survival was inferior to
that of an age- and sex-matched control population. The
difference in survival was not entirely explained by the
increased prevalence of radiation-induced CP. Two reasons
may account for this observation. First, patients with CP often
have systemic or pleuropulmonary disease that increases the
risk of non– cardiac-related deaths. However, comorbidity
was not a significant predictor of late survival in our study.
Second, improved perioperative management and medical
therapy could have deferred attrition in patients with associated myocardial disease. This latter possibility is supported
by 2 observations: (1) preoperative NYHA class independently predicted late cardiac-related deaths and (2) the survival
curves diverged early, after only 18 months.
Late death occurred suddenly in 6 patients. Sudden death
has been reported in the setting of CP18 and after pericardiectomy.1,5,19 Occult atherosclerotic coronary artery disease
may be suspected, but the pericardial process can also
obliterate epicardial vessels and cause myocardial ischemia.20,21 This is unlikely after pericardiectomy unless it was
incomplete. In 2 of our patients with radiation disease, sudden
death could have resulted from accelerated coronary
atherosclerosis.8,22
Predictors of Late Events
All long-term outcomes were predicted consistently by 3
baseline variables: age, NYHA class, and a radiation cause
for CP.
A correlation between NYHA class and overall or late
survival has been observed by us and others and is the basis
for advocating early pericardiectomy.1,4,17 However, the effect of age on survival after pericardiectomy has not previously been apparent because of the uniformly young populations studied, especially from regions in which tuberculosis is
endemic.1,4,14,23,24 The median age of our patients is at least a
decade older than that in other series.1,4,14,19,20,25–30 Greater
physician awareness and a comprehensive Doppler echocardiographic examination could have been instrumental in
diagnosing CP in these older patients.31
Previous radiotherapy was the most powerful predictor of
all outcome measures. The deleterious late effects of radiation
on cardiac structures other than the pericardium have been
well described.8,12,32,33 Pericardiectomy is more challenging
because of mediastinal fibrosis, which limits complete resection,34,35 and postoperative recovery may be prolonged because of chest wall fibrosis. Long-term survival is also
compromised by pulmonary interstitial disease, impaired
immunological responses, and recurrent primary tumor or
secondary neoplasms from chemotherapy. However, all
deaths in our patients with radiation pericarditis were cardiacrelated. Our study confirms the guarded long-term outcome
of these patients, even if some derived initial symptomatic
relief after pericardiectomy. The recognition of such poorrisk subgroups also facilitates objective comparisons of survival data. For instance, although Tirilomis et al17 reported a
5-year overall survival of 85% after pericardiectomy, the
mean age of their patients was 44 years, and only 1 patient
had radiation-induced CP.
Late Functional Status
Figure 4. Change in NYHA functional class in 93 late survivors,
showing marked symptomatic improvement in most patients
after pericardiectomy. NYHA class was indeterminate in 1
patient before surgery and unknown in 3 patients at latest
follow-up.
Pericardiectomy provided excellent relief of symptoms in
most late survivors in our study. However, nearly one third of
these patients experienced either new or recurrent NYHA
class III to IV symptoms at some time during follow-up. This
could be due to incomplete surgical resection.36 –38 In our
study, incomplete pericardiectomy was significantly associated with recurrence of late CHF in univariate analysis.
However, the majority of patients in whom recurrent symptoms developed had had radical surgery. The culprit pathophysiological mechanisms in these instances are not well
characterized but include immobilization atrophy, myoperi-
Ling et al
cardial involvement by the same pathological process (exemplified by radiation disease), or physical extension of pericardial calcification into the myocardium.20,39 – 41 Residual
myocardial fibrosis was likely in our patients who had
recurrent CHF symptoms, because (1) many had radiationinduced disease and (2) restrictive left ventricular filling
could be documented by serial Doppler echocardiography in
some patients.31,42
Involvement of adjacent pleuropulmonary structures by the
constrictive disease process39 and concomitant chronic obstructive lung disease limited functional recovery in nearly a
fifth of patients. Clearly, these mechanisms are not mutually
exclusive in individual cases.
Limitations
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Selecting cases of CP on the basis of thoracotomy findings to
reflect incidence represents a bias of all surgical studies. It is
likely that more cases remain unoperated on, because of underdiagnosis, minimal symptoms, or high operative risk. However,
inspection of the pericardium remains the gold standard for the
diagnosis of CP and may be the only way to prove the diagnosis
in relation to restrictive cardiomyopathy.31,43
Incomplete functional recovery in some patients may be
the result of gradual adaptation of the released ventricles to
loading conditions and may not represent the permanent
functional state. However, nearly all our patients had
follow-up of at least 1 year, and myocardial recovery should
have occurred by that time.44,45
Unlike other investigators,1 we did not include cardiac
catheterization variables for prediction of outcome. This test,
which was done in 65 of the 132 patients, is currently not
performed routinely in the workup of CP at our institution
unless echocardiographic findings are nondiagnostic.
Because patients who had concomitant surgical procedures
were excluded from our historic cohort, a direct comparison
of outcome between the historic and contemporary patient
groups may preferentially favor the former. However, the
occasional need for concomitant coronary artery bypass graft
surgery and valvular procedures did not have significant
impact on early and late mortality in univariate analyses,
consistent with the findings of other studies.29,36
Conclusions
CP is a heterogeneous disease. Increasingly important causes
in the current era include previous mediastinal irradiation and
cardiac surgery. Although pericardiectomy is often performed, it may not offer a cure or good long-term result for
patients with CP that is advanced or due to radiation disease.
Cardiac transplantation could be considered in selected patients without recurrent tumor and with good pulmonary
reserve, particularly if severe valvular disease coexists. However, postoperative prognosis and functional outcomes remain good for most other patients with CP and excellent for
younger patients without radiation pericarditis.
Acknowledgment
Dr Ling was supported by a Faculty Development Program Scholarship from the National University Hospital, Singapore, and by the
Mayo Clinic. We thank Jami A. Spitzer for help with preparation of
the manuscript.
Constrictive Pericarditis
1385
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Constrictive Pericarditis in the Modern Era: Evolving Clinical Spectrum and Impact on
Outcome After Pericardiectomy
Lieng H. Ling, Jae K. Oh, Hartzell V. Schaff, Gordon K. Danielson, Douglas W. Mahoney,
James B. Seward and A. Jamil Tajik
Downloaded from http://circ.ahajournals.org/ by guest on June 14, 2017
Circulation. 1999;100:1380-1386
doi: 10.1161/01.CIR.100.13.1380
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