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Constrictive Pericarditis Treated by Surgery

Article in Texas Heart Institute journal / from the Texas Heart Institute of St. Luke's Episcopal Hospital, Texas Children's Hospital · April 2012
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Clinical
Investigation Constrictive Pericarditis
Treated by Surgery
Alireza A. Ghavidel, MD We reviewed the records of 45 patients (mean age, 46.6 ± 14.9 yr; range, 21–84 yr) with
Maziar Gholampour, MD a diagnosis of constrictive pericarditis who had undergone pericardiectomy from 1994
Majid Kyavar, MD, FACC
Yalda Mirmesdagh, MD
through 2006. Preoperatively, 2 of the patients (4.4%) were in New York Heart Association
Mohammad-Bagher (NYHA) functional class I, 20 (44.4%) in class II, 22 (48.9%) in class III, and 1 (2.2%) in class
Tabatabaie, MD IV. Pericardial calcification was detected in 20% of plain chest radiographs. Constrictive
pericarditis was caused by tuberculosis in 22.2%, chronic renal failure in 8.9%, a history
of sternotomy in 4.4%, and malignancy in 4.4%. The cause was idiopathic in 60% of the
patients. Low-output state was the most common postoperative problem (22.2%).
The mean follow-up period was 40 ± 18 months (range, 3–144 mo). Three months post-
operatively, only 1 of 43 available patients (2.3%) was in NYHA class III, while the rest were
in class I (36 patients; 83.7%) or II (6 patients; 14%). The overall mortality rate was 4.4%: 1
patient with tuberculosis died of respiratory insufficiency while hospitalized, and 1 died of
metastatic adenocarcinoma during follow-up.
Our results show that pericardiectomy remains an effective procedure in the treatment
of constrictive pericarditis. Tuberculosis is still an important cause of constrictive pericar-
ditis in Iran, despite intensive vaccination and use of antitubercular drugs. (Tex Heart Inst
J 2012;39(2):199-205)

C
Key words: Calcinosis;
onstrictive pericarditis is an uncommon cause of heart failure. Approximately
heart failure; low-output syn- 15% of patients with acute pericarditis experience cardiac tamponade. Ef-
drome; pericardial effusion; fusive pericarditis is found in 5% of cases of acute tamponade, but only
pericardiectomy; pericardi-
tis, constrictive/complica-
1.2% of these patients develop chronic constrictive pericarditis. Tuberculosis (TB)
tions/surgery; pericarditis, is the cause of nearly 4% of acute pericarditis cases and 7% of cardiac tamponade
tubercular/surgery; recovery cases. According to reports during the past decade, the incidence of purulent and TB
of function; retrospective
studies; treatment outcome
pericarditis was 55/1,184 patients (4.6%).1
In the past, idiopathic inflammation and TB constituted the most common causes
of constrictive pericarditis. However, during the last 20 years there has been a shift in
From: Departments of
Cardiovascular Surgery
the causes of constrictive pericarditis: radiation and previous cardiac surgery currently
(Drs. Ghavidel, Gholam- are the prime suspects in constrictive pericarditis cases in the Western world.2
pour, and Tabatabaie), This retrospective study was conducted to determine the causes of constrictive peri-
Intervention­al Cardiology
(Dr. Kyavar), and Heart
carditis in our institution’s patient population over the past 12 years, with a view in
Valve Research Center particular toward ascertaining whether TB would emerge as a significant cause.
(Dr. Mirmesdagh), Rajaee
Cardiovascular Medical
Research Center, Tehran Patients and Methods
University of Medical
Science, 1996911151 All patients who had undergone pericardiectomy at Rajaee Heart Center from 1994
Tehran, Iran
through 2006 were identified in our surgical database. Clinical and operative details
were retrieved from the hospital notes. Patient follow-up was performed by the cardiac
Address for reprints: surgeons and cardiologists in the hospital clinic. Perioperative death was defined as
Alireza Alizadeh Ghavidel,
MD, Cardiovascular
death within 30 days of the operation or during the same hospital admission.
Surgery Department, There were 45 patients, including 28 men (62.2%), with a mean age of 46.6 ±
Rajaee Cardiovascular 14.9 years (range, 21–84 yr). The diagnosis of constrictive pericarditis was confirmed
Medical Research Center,
Tehran University of Medi-
by clinical presentation, echocardiographic study, cardiac catheterization, and chest
cal Science, Vali-Asr Ave., computed tomographic (CT) scan, as needed. During the procedure, tissue and fluid
1996911151 Tehran, Iran sampling—for aerobic and anaerobic cultures and histopathologic studies—was done
for an evaluation of the causal factors. The diagnosis of TB was confirmed on the
E-mail: basis of clinical findings in combination with histopathologic features, including the
[email protected] presence of acid-fast bacilli in Ziel-Nelson tissue staining, typical granuloma and ca-
seous necrosis, and bacteriologic studies using the polymerase chain reaction (PCR)
© 2012 by the Texas Heart ® test on the pericardial fluid or tissue for evidence of mycobacterium tuberculosis. Six
Institute, Houston patients were admitted with a diagnosis of TB, 4 had chronic renal failure, 2 had a

Texas Heart Institute Journal Constrictive Pericarditis Treated by Surgery 199

history of open cardiac surgery, and 1 had a history of presence of various degrees of pericardial calcification
exposure to chemical weapons. The preoperative char- was patently high (19/26 patients; 73%). Pericardial
acteristics of the patients are shown in Table I. thickening was reported in almost all of the patients,
Dyspnea with or without peripheral edema or asci- and 3 patients had more than 10 mm of thickness upon
tes was the most common symptom. The rates of peri- chest CT scanning.
cardial rub, high jugular venous pressure, and pulsus The surviving patients were monitored from 3 to 144
paradoxus in physical examination were statistically months (median, 41 mo), and 3- and 6-month follow-
insignificant. Eight patients had normal physical find- up periods were completed for 43/44 (97.7%) and
ings. Nineteen patients had atrial fibrillation at the time 38/44 (86.4%) of the patients, respectively. The pre-
of surgery. Pericardial calcification on plain chest radi- operative hemodynamic and echocardiographic char-
ography was seen in 9 patients, and 8 had no unusual acteristics of the patients are presented in Tables II and
changes. The diaphragmatic, apical, and left borders of III, respectively.
the cardiac shadow on the chest radiograph were the
most common sites of calcification. Most of the radio- Surgical Technique
graphs showed areas spared from calcification; however, The primary surgical goal was total pericardiectomy,
in 2 of the 9 patients, global pericardial calcification including the resection of the anterior pericardium be-
was seen on the radiograph. Chest CT scanning was tween the 2 phrenic nerves, the basal aspect of the peri-
performed in only 26 (57.8%) of the patients, but the cardium over the diaphragm, the posterior part of the
pericardium lying on the left and right ventricles, and
the pericardium over the great arteries and both atria.
TABLE I. Preoperative Characteristics of the 45 Patients In the patients who had thick, dense, and constrictive
pericardium over the pulmonary veins, pericardial re-
Variable No. (%) section was also performed beyond the phrenic nerves.
In these patients, an effort was made to save the phrenic
Mean age (yr) 46.6 ± 14.9
Age range (yr) 21–84 nerves as pediculated tissue. The left phrenic nerve was
Male/female sex 28/17 sacrificed in 2 patients because of severe calcification
Clinical Presentation (main symptom) and adhesion of the nerve to the pericardium. More-
Dyspnea on exertion 26 (57.8) over, attempts were made to decorticate the constrictive
Dyspnea on exertion and leg edema 2 (4.4) white, fibrotic, and thickened layer of the epicardium
Dyspnea on exertion and ascites 5 (11.1)
Dyspnea on exertion, ascites, and edema 6 (13.3) over the ventricles. Some patients could undergo only
Dyspnea on exertion and generalized edema 2 (4.4) partial pericardiectomy as a consequence of inadequate
Dyspnea on exertion and chronic cough 1 (2.2) exposure (in 2 patients approached via thoracotomy),
Atypical chest pain 2 (4.4)
Syncope 1 (2.2) high risk of coronary artery or myocardial damage, or
severe bleeding. In such cases, the pericardium over the
Medical History
Pulmonary tuberculosis 6 (13.3)
right atrium or superior and inferior venae cavae was left
Chronic renal failure 4 (8.9) intact. In 2 patients, the pericardium could be resected
Chronic obstructive pulmonary disease 1 (2.2)
Aortic valve replacement 1 (2.2)
Mitral valve replacement 1 (2.2) TABLE II. Preoperative Hemodynamic Characteristics in
Exposure to chemical weapons 1 (2.2) the 45 Patients
Clinical Findings
Ascites 4 (8.9) Pressure (Range)
Peripheral edema 4 (8.9) Variable mmHg
Ascites and peripheral edema 7 (15.6)
Ascites and hepatomegaly 12 (26.7) LVED 18.7 ± 7.1 (11–26)
Pulsus paradoxus 2 (4.4)
Pericardial rub 4 (8.9) RVED 17.2 ± 4.4 (5–23)
High jugular venous pressure 4 (8.9)
Normal clinical findings 8 (17.8) Right atrium 19.8 ± 5.3 (18–28)

Chest Radiographic Findings Right ventricle 41.2 ± 10 (25–70)

Cardiomegaly 24 (53.3) Left ventricle 122 ± 21 (80–190)
Pericardial calcification 9 (20.0)
Pleural effusion 4 (8.9) Aorta 126 ± 20 (90–180)
Normal 8 (17.8)
Pulmonary artery 38 ± 9.3 (14–50)
Cardiac Rhythm
Sinus 21 (46.7) LVED = left ventricular end-diastolic; RVED = right ventricular
Atrial fibrillation 19 (42.2) end-diastolic
Left bundle branch block 3 (6.7)
Left anterior hemiblock 2 (4.4) Data are presented as mean ± SD and range.

200 Constrictive Pericarditis Treated by Surgery Volume 39, Number 2, 2012

TABLE III. Preoperative Findings of the Echocardiographic complete destruction of his lungs due to pulmonary TB;
Studies in the 45 Patients he died on the 24th postoperative day because of pul-
Variable No. Cases (%)
monary insufficiency, despite the fact that his phrenic
nerves had been saved during the surgical procedure.
Mild pericardial effusion 17 (37.8) The late mortality rate was 2.3% (1/44) in our study.
Moderate-to-severe 4 (8.9)
The man who died had presented in NYHA class II,
pericardial effusion and histopathology showed that the pericardium was
involved with a metastatic adenocarcinoma; he died 7
Massive pericardial 1 (2.2)
effusion (tamponade) months after surgery as a result of hepatic insufficiency
due to metastatic adenocarcinoma of the colon.
Thickened pericardium 43 (95.6)
The surgical approach included sternotomy in 43
Severe mitral regurgitation 1 (2.2) patients (95.6%) and thoracotomy in the remaining
and mild TR 2 (4.4%). Cardiopulmonary bypass was performed in
Severe TR 1 (2.2) only 9 patients (20%). Severe hemodynamic instability
Mild-to-moderate TR 3 (6.7)
in 4 patients (8.9%), concomitant valve replacement in
3 (6.7%), and severe iatrogenic intraoperative bleeding
Severe mitral stenosis 1 (2.2) in 2 (4.4%) were the primary reasons for CPB use. In
Severe AS and moderate AI 1 (2.2) addition to pericardiectomy, 1 patient underwent aor-
Mean preoperative LVEF (range) 0.47 ± 0.7 (0.30–0.60)
tic valve replacement; 1, mitral valve replacement; and
1, tricuspid valve replacement. Twenty-eight patients
Mean PAP, mmHg (range) 38 ± 9.2 (14–50) (62.2%) required resection of the fibrotic dense epicar-
AI = aortic insufficiency; AS = aortic stenosis; LVEF = left dium. The use of inotropic agents is shown in Figure 1.
ventricular ejection fraction; PAP = pulmonary artery pressure; It is of interest that 22 patients (48.9%) had constric-
TR = tricuspid regurgitation tive pericarditis associated with pericardial effusion.
The most common early postoperative complication
was low-output syndrome (10 patients). The mean vol-
only in patches; therefore, some islands of epicardium ume of postoperative mediastinal bleeding was 433 ±
and pericardium were left intact. 215 mL (range, 100–1,300 mL). One patient was re-
Three patients required concomitant valve replace- explored due to excessive mediastinal hemorrhaging.
ment. In these patients, the anterior wall of the pericar- The mean number of postoperative blood transfusions
dium was resected before the remaining pericardium was 1.8 ± 0.7 units (range, 0–6 units). Table IV shows
and epicardium were resected under cardiopulmonary the early post-pericardiectomy complications.
bypass (CPB). Except for the 2 patients who under- The functional status of the patients improved after
went partial pericardiectomy via left thoracotomy at the pericardiectomy. Forty-two of the 45 patients (93.3%)
surgeon’s discretion, all the others were approached via had been in NYHA class II or III before the operation,
median sternotomy. The primary intention was pericar- but 3 months postoperatively only 1 of 43 available pa-
diectomy without CPB; nonetheless, the concomitant tients (2.3%) was in NYHA class III, and the rest were
cardiac procedure (3 patients), hemodynamic instabil- in class I (83.7%) or II (14%) (Fig. 2).
ity during manipulation, severe surgical bleeding, and
the need for sufficient exposure necessitated the institu-
tion of CPB.

Statistical Analysis
All of the continuous variables are expressed as mean
± SD and the categorical variables as percentages. The
c2 and Student t tests were performed as appropriate.
The Wilcoxon signed rank test was used to compare
the New York Heart Association (NYHA) functional
classes of patients preoperatively and postoperatively. A
P value <0.05 was considered statistically significant.

Results
The overall mortality rate in this series was 4.4% (2/45). Fig. 1 Comparison of the use of inotropic agents during the peri-
The only early death (2.2%) was that of a 38-year-old operative and late postoperative periods.
man, who had presented in NYHA class III and had

Texas Heart Institute Journal Constrictive Pericarditis Treated by Surgery 201

 Chronic nonspecific inflammatory changes were the Table V lists the final diagnoses in our patients, and
most common histopathologic findings (33/45; 7.3%). it shows that TB was the most common known cause
Eight patients (17.8%) had the characteristic histopath- of constrictive pericarditis in this patient population.
ologic features of TB, 1 had pericardial involvement
with non-Hodgkin’s lymphoma, and 1 had pericardial Discussion
metastatic adenocarcinoma. Of note, 2 patients had
normal histologic findings. Microbiologic examina- Constrictive pericarditis is an infrequent cause of a very
tions, including PCR testing in 2 other patients, indi- common condition, heart failure. It is defined as the
cated the presence of TB; the overall TB pericarditis chronic fibrous thickening of the wall of the pericar-
rate, therefore, reached 22.2% in this series (10/45). dial sac, which leads to abnormal diastolic filling.1,2 The
course of the disease is usually slow and the symptoms
TABLE IV. Early Postoperative Complications are nonspecific; consequently, in many cases the symp-
toms may be present for 12 months or longer before a
Complication No. (%) diagnosis is made.2
Low-output syndrome 10 (22.2)
The diagnosis of constrictive pericarditis can be a
challenging process, but it seems advisable that patients
Surgical bleeding 1 (2.2) with heart failure but preserved left ventricular function
Pleural effusion 4 (8.9) be considered for this diagnosis. Although the right and
left ventricular diastolic pressures are equalized in this
Acute renal failure 1 (2.2)
disease, symptoms of right-sided heart failure are likely
Respiratory failure 1 (2.2) to dominate. While it is not definitive, the conventional
Long-term intubation 2 (4.4) hallmark of constrictive pericarditis has been the pres-
ence of pericardial thickening of more than 3 mm.2,3
Hepatic failure 0
Pericardiectomy is the accepted treatment for con-
Wound problems 0 strictive pericarditis; be that as it may, hemodynamic
Repeat pericardiectomy 0 results after surgery range from complete recovery to
no benefit.3-8 These variable results might arise from
different approaches to the surgical procedure or from
incomplete pericardial resection. The study by Senni
and colleagues,3 which had a long follow-up period, re-
ported the persistence of some degree of left ventricu-
lar diastolic dysfunction in approximately 40% of the
patients, even after total pericardiectomy. The authors
posited that this abnormal ventricular compliance
might be due to myocardial changes in tandem with
incomplete pericardiectomy. DeValeria and colleagues 6
reported that the myocardial atrophy and fibrosis found
at autopsy in constrictive pericarditis patients might
indicate some degree of restrictive abnormality of the
Fig. 2 Postoperative improvement in functional status on the ventricle after pericardiectomy.
basis of New York Heart Association (NYHA) functional class at Low-output syndrome was the most common prob-
3 months. lem during the early postoperative phase in the present
study. This low-output state after pericardiectomy might
have been due to incomplete pericardiectomy. Nonethe-
TABLE V. Final Diagnosis in Patients with Constrictive less, the above-mentioned changes, together with post-
Pericarditis
operative transient interstitial edema, could have had
Final Diagnosis No. Patients (%) an effect. Entrapment of the heart chambers by insuf-
ficiently resected fibrotic epicardium might have caused
Idiopathic disease 27 (60) persistent diastolic dysfunction and a postoperative low-
Tuberculosis 10 (22.2) output state. Figure 1 shows that 10 patients needed
Chronic renal failure 4 (8.9)
moderate doses of inotropic agents postoperatively and
3 required high doses; whereas, in the preoperative
Postpericardiectomy 2 (4.4)
period, only 7 patients had needed inotropic support.
Metastatic adenocarcinoma of the colon 1 (2.2) Furthermore, none of the survivors required inotropic
Non-Hodgkin’s lymphoma 1 (2.2) agents during the late phase of hospitalization. These
changes may appear to be important, but they were not

202 Constrictive Pericarditis Treated by Surgery Volume 39, Number 2, 2012

statistically significant (P=0.068). No correlation was In 2 different studies,15,16 the overall incidence of
found between the use of inotropic agents and the use of pericardial calcification detected on chest radiographs
CPB (P=0.08). Bozbuga and associates9 suggested that ranged between 5% and 27%. Bozbuga and colleagues9
low-output syndrome could also be caused by changes found pericardial calcification in 44% of patients with
in cardiac architecture. In other words, long periods of TB pericarditis. In our series, this radiographic find-
myocardial compression are likely to contribute to the ing occurred in 20% of all patients and 30% of patients
remodeling of the ventricles and to the weakening of the with TB pericarditis. Statistically, there was no correla-
myocardium in patients who have undergone long peri- tion between pericardial calcification and TB (P=0.07).
ods of symptomatic pericardial constriction. Omoto and Surprisingly, in the data available to us for review, only
colleagues10 reported that the postoperative low-output a small proportion of our patients had elevated jugular
state gradually improved in most of their patients. venous pressure (Table I). We would like to emphasize
Most of our patients were operated on through a that we were obliged to use medical history sheets. Also,
median sternotomy, which allows excellent access and unfortunately, the importance of physical findings in
a better possibility of complete resection. Cardiopul- clinical judgment, especially in cardiology, seems to
monary bypass was used in 9 patients; the primary have declined and physical examination has been re-
reasons for the use of CPB were severe hemodynamic placed by routine echocardiographic studies.17
instability during heart manipulation in 4 patients, con- The overall and in-hospital mortality rates in the
comitant valve replacement in 3, and severe iatrogenic present study were 4.4% and 2.2%, respectively. Previ-
mediastinal bleeding in 2 other patients. Our prefer- ously reported data showed in-hospital mortality rates
ence was pericardiectomy without CPB; however, we ranging from 4.9% to 16%.6,12,13,18-20 The mortality rate
believe that total pericardiectomy (if possible) using after pericardiectomy in patients with TB pericarditis
CPB is more advantageous than partial decortication ranges from 3% to 16%.21 The known predictors for
of the pericardium without CPB. Thoracotomy may post-pericardiectomy death include advanced age, atrial
be preferable in patients who have purulent pericarditis, fibrillation, concomitant severe TR, postoperative ino-
in which case sternotomy increases the risk of wound tropic support, high pulmonary artery pressure, radia-
infection and sternal dehiscence.11 In our study, the tion history, renal failure, low left ventricular ejection
thoracotomy approach was applied in only 2 patients: fraction, and incomplete pericardiectomy; in the pres-
sternotomy was avoided in 1 patient due to a history of ent study, however, neither univariate nor multivariate
mitral valve replacement and in the other due to cos- analysis found a risk factor for early death. This may be
metic considerations. due to the small size of our patient population.9,12,13,18
Our patients’ NYHA functional status improved Constrictive pericarditis exhibits a heterogeneous pat-
considerably after pericardiectomy. Indeed, most of our tern and arises from different causes, depending on the
patients were in NYHA class I or II postoperatively (P geographic area from which it is reported. In 1999, re-
<0.001). Except for 3 patients, 1 of whom died in the ports from developed countries indicated that 50% of
early postoperative period due to respiratory failure, all cases were due to prior pericarditis, cardiac surgery,
patients had better functional status postoperatively. and radiation therapy, and nearly 30% of cases were
One patient, who had presented in NYHA class III, idiopathic.2
remained in the same functional class after partial Tubercular pericarditis is found in approximately
pericardiectomy. Another patient, who was in NYHA 1% of all autopsied cases of TB and in 1% to 2% of
class III shortly after pericardiectomy, had shown no patients with pulmonary TB.9,21 Tuberculosis has been
evidence of tricuspid regurgitation (TR) in preoperative reported to be the cause of nearly 4% of the cases of
echocardiographic studies but exhibited moderate-to- acute pericarditis, 7% of cardiac tamponade, and 6%
severe TR in postoperative studies. By midterm follow- of constrictive pericarditis.22 McCaughan and associ-
up, this patient had improved with medication and ates 23 reported that active TB was present in 6.1% of
did not need further intervention. Most likely, the TR their cases of constrictive pericarditis, and Ling and
had been underestimated in preoperative transthoracic colleagues 2 reported even a smaller percentage (0.7%).
echocardiography. Johnson and colleagues 12 reported In stark contrast, 38% to 83% of the cases of constric-
that post-pericardiectomy TR can be caused by right tive pericarditis are still caused by TB in developing
ventricular dilation. Gongora and coworkers 13 stated countries.9,12,24
that tricuspid regurgitation may worsen after pericardi- Pericardial involvement in TB patients usually oc-
ectomy. curs as a result of the lymphatic extension of mycobac-
Buckingham and co-investigators,14 using transesoph- terium tuberculosis or of the hematogenous spreading
ageal echocardiography, reported that mitral insuffi- of primary TB infection.21 Tubercular pericarditis has 3
ciency might be seen after pericardiectomy as a result of clinical presentations: pericardial effusion, constrictive
papillary muscle elongation. In our series, no significant pericarditis, and a combination of the two. The clinical
postoperative mitral regurgitation was observed. features of TB pericarditis are highly variable, ranging

Texas Heart Institute Journal Constrictive Pericarditis Treated by Surgery 203

from an absence of symptoms to severe constriction, diotomy constrictive pericarditis or the perceived high
and the diagnosis is frequently missed on cursory clini- surgical risk of reoperation.
cal examination.21 The diagnosis of TB was made in One of our patients had been exposed to chemical
22.2% of our patients, which means that despite all the weapons during the Iran–Iraq war. His histopathologic
vaccination programs and anti-TB medications in Iran, study revealed only nonspecific chronic inflammatory
this disease remains an important cause of constrictive findings. Moreover, our review of the medical literature
pericarditis. Of note, one third of our TB patients were did not show any distinct relationship between chemi-
Afghan immigrants; nonetheless, the incidence of 17% cal bomb exposure and constrictive pericarditis.
(7 patients) for TB pericarditis in the native Iranian Limitations. Limitations of the present study include
portion of our study group (41 patients) indicates that its retrospective design, its small number of patients,
TB continues to be a frequent source of constrictive and its relatively short follow-up period. Therefore, our
pericarditis in our country. We believe that the preva- findings may have shortcomings and may not be con-
lence of TB pericarditis might be higher than the per- clusive.
centage presented here because of the underdiagnosis Conclusion. Our results show that pericardiectomy
of TB infection and the overlap of symptoms between remains an effective procedure in the treatment of con-
constrictive pericarditis and pulmonary TB. Even in strictive pericarditis in that it yields low mortality rates
developed countries, it seems that TB pericarditis will and excellent functional outcomes. Another finding of
not remain a rare disease during the next decade, due significance is that, despite intensive vaccination and
to the association between TB and human immuno- use of anti-TB drugs in our country, TB is still an im-
deficiency viral infection.21,22 portant cause of constrictive pericarditis.
The prevalence of constrictive pericarditis with id-
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204 Constrictive Pericarditis Treated by Surgery Volume 39, Number 2, 2012

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