Long-Term Clinical Outcomes and Prognostic Factors After Pericardiectomy for Constrictive Pericarditis in a Japanese Population

Abstract

Background: Constrictive pericarditis (CP) is characterized by impaired diastolic cardiac function leading to heart failure. Pericardiectomy is considered effective treatment for CP, but data on long-term clinical outcomes after pericardiectomy are limited.

Methods and Results: We retrospectively investigated 45 consecutive patients (mean age, 59±14 years) who underwent pericardiectomy for CP. Preoperative clinical factors, parameters of cardiac catheterization, and cardiac events were examined. Cardiac events were defined as hospitalization owing to heart failure or cardiac death. Median follow-up was 5.7 years. CP etiology was idiopathic in 16 patients, post-cardiac surgery (CS) in 21, tuberculosis-related in 4, non-tuberculosis infection-related in 2, infarction-related in 1, and post-radiation in 1. The 5-year event-free survival was 65%. Patients with idiopathic CP and tuberculosis-related CP had favorable outcomes compared with post-CS CP (5-year event-free survival: idiopathic, 80%; tuberculosis, 100%; post-CS, 52%). Higher age (hazard ratio: 2.51), preoperative atrial fibrillation (3.25), advanced New York Heart Association class (3.92), and increased pulmonary artery pressure (1.06) were predictors of cardiac events. Patients with postoperative right-atrial pressure ≥9 mmHg had lower event-free survival than those with right-atrial pressure <9 mmHg (39% vs. 75% at 5 years, P=0.013).

Conclusions: Long-term clinical outcomes after pericardiectomy among a Japanese population were related to the underlying etiology and the patient’s preoperative clinical condition. Postoperative cardiac catheterization may be helpful in the prediction of prognosis after pericardiectomy.

Constrictive pericarditis (CP) is characterized by impaired diastolic filling of the ventricles as a result of scarring and consequent loss of the normal elasticity of the pericardial sac, which leads to heart failure.^1,2

Pericardiectomy is considered to be the mainstay of CP treatment. However, medical therapy may be used to optimize hemodynamics preoperatively and for palliative control of symptoms in patients who are not candidates for surgery.³

Long-term clinical outcomes after pericardiectomy for CP vary according to the etiology.^4–7 In “developed” countries, the most common causes of CP are idiopathic, post-cardiac surgery (CS), and post-radiation. Tuberculosis (TB) is a rare cause of CP in developed countries, whereas it is a major cause of CP in “developing” countries.^8,9 Therefore, there may be ethnic differences in the etiology and prognosis of CP.¹⁰

Several reports on clinical outcomes after pericardiectomy have been published, mainly from Europe and the USA.^4–6,11 With respect to Japanese populations, Tokuda et al have reported on the short-term surgical outcome of pericardiectomy,¹² but there are few reports about long-term clinical outcomes after pericardiectomy.

The purpose of the present study was to clarify the long-term clinical outcomes and prognostic factors after pericardiectomy for CP among a Japanese population.

Methods

Study Population

We retrospectively investigated 48 consecutive patients who underwent pericardiectomy for CP between 1985 and 2014 at Tenri Hospital.

Among these 48 patients, 3 who had significant valvular disease (2 with mitral regurgitation; 1 with mitral stenosis) and underwent concomitant replacement of the mitral valve at pericardiectomy were excluded. Hence, 45 patients were enrolled.

The diagnosis of CP was based on clinical features, characteristics of transthoracic echocardiography, parameters of right-heart catheterization, and other imaging modalities (chest radiography, computed tomography, magnetic resonance imaging). Clinical outcomes and their predictors were evaluated. The study protocol was approved by the Institutional Ethics Committee at Tenri Hospital (Nara, Japan).

Etiologies of CP and Pericardiectomy

In accordance with previous reports, the etiology of CP was determined from the medical history of the patient.^5,6 “Postoperative constriction” was defined as post-CS CP, and prior CS was classified as follows: coronary artery bypass grafting (CABG); valve operation; and valve operation with CABG. “Constriction with a previous history of chest radiation” was defined as post-radiation CP. Additional possible etiologies of CP were infectious (bacterial and fungal) or infarction-related CP. Furthermore, infectious CP was divided into TB-related CP or non-TB-related CP. “Idiopathic CP” was defined as constriction after previous viral infection. Patients who could not be classified into any of the groups described were also considered to have idiopathic CP.

“Total pericardiectomy” was defined as resection of the anterior pericardium between the 2 phrenic nerves, the basal aspect of the pericardium over the diaphragm, the posterior part of the pericardium over the diaphragm lying on the left and right ventricles, and the pericardium over the great arteries and both atria. “Partial pericardiectomy” was defined as any pericardial excision that did not meet the criteria for total pericardiectomy.

Cardiac Events After Pericardiectomy and Predictors

“Cardiac events” were defined as either hospitalization owing to heart failure or cardiac death. “Cardiac death” was defined as sudden death or death from congestive heart failure. “Perioperative mortality” was defined as death during hospitalization for pericardiectomy.

To analyze the predictors of cardiac events, we examined the clinical factors, preoperative clinical condition, and preoperative parameters of cardiac catheterization. Clinical factors were age, sex, and underlying disease. Underlying disease included hypertension, diabetes mellitus, dyslipidemia, coronary artery disease, and atrial fibrillation (AF). Hypertension was defined by a systolic blood pressure (BP) ≥140 mmHg and/or a diastolic BP ≥90 mmHg, or use of antihypertensive medications. Dyslipidemia was defined as a serum cholesterol level ≥220 mg/dL or use of cholesterol-lowering medications. Diabetes mellitus was defined as hyperglycemia that necessitated use of medications. Coronary artery disease was defined by previous history of angina, myocardial infarction, or percutaneous coronary intervention, or a significant stenosis in a coronary artery revealed by coronary angiography. Preoperative clinical condition was evaluated by New York Heart Association (NYHA) class based on reporting of symptoms by the patients. Data on cardiac catheterization included systolic BP, systolic pulmonary artery pressure, mean right-atrial pressure (RAP), mean pulmonary capillary wedge pressure, cardiac output, and the cardiac index (CI).

Effectiveness of Pericardiectomy

To evaluate the effectiveness of pericardiectomy, we also analyzed preoperative and postoperative changes in clinical status (NYHA class) and hemodynamics (RAP and CI). Postoperative cardiac catheterization was undertaken before hospital discharge.

Furthermore, we divided the patients into 2 groups based on their postoperative RAP or CI and compared cardiac event-free survival. The cutoff value of postoperative RAP was determined by the median value. Postoperative CI was dichotomized using a clinically meaningful reference value.

Statistical Analysis

Statistical analyses were carried out using JMP v8 (SAS Institute Inc., Cary, NC, USA). Continuous variables are presented as the mean±SD or median and interquartile range. Event-free survival is shown by Kaplan-Meier curves, and comparisons between several groups were done using a log-rank test. Relative risk and 95% confidence intervals were calculated using Cox proportional hazard analysis. P<0.05 was considered significant.

Results

Baseline Characteristics of Patients (Table 1)

The study population comprised 34 men and 11 women with a mean age of 59±14 years at the time of pericardiectomy. Etiology of CP was idiopathic in 16 patients (36%), post-CS in 21 patients (47%), TB-related in 4 patients (9%), non-TB-related in 2 patients (4%), infarction-related in 1 patient (2%), and post-radiation in 1 patient (2%). Among the 21 patients with post-CS CP, prior CS was CABG in 11 patients, valve operation in 9 patients (mitral valve, 4; aortic valve, 2; mitral and aortic valves, 3), and valve operation with CABG in 1 patient.

Table 1. Baseline Characteristics of the CP Patients at Pericardiectomy

	Idiopathic (n=16)	Post-CS (n=21)	TB (n=4)	Non-TB (n=2)	Infarction-related (n=1)	Post-radiation (n=1)
Age (years)	57±17	61±13	59±9.0	55±4.5	75	53
Sex (male)	12 (75)	16 (76)	3 (75)	2 (100)	1 (100)	0 (0)
NYHA class (III or IV)	9 (56)	17 (81)	3 (75)	2 (100)	0 (0)	1 (100)
Comorbidities (%)
Hypertension	2 (13)	9 (43)	1 (25)	0 (0)	1 (100)	0 (0)
Dyslipidemia	1 (6.3)	5 (24)	0 (0)	0 (0)	1 (100)	0 (0)
Diabetes mellitus	2 (13)	3 (14)	0 (0)	1 (50)	0 (0)	0 (0)
Atrial fibrillation	5 (31)	11 (52)	1 (25)	0 (0)	1 (100)	1 (100)
Coronary artery disease	0 (0)	12 (57)	0 (0)	0 (0)	1 (100)	0 (0)
Pericardial calcification	6 (38)	5 (24)	1 (25)	0 (0)	1 (100)	1 (100)
Data for preoperative catheterization
Systolic BP (mmHg)	102±14	112±16	113±17	84±3.0	84	84
Systolic PAP (mmHg)	33±7.2	36±8.8	33±3.0	27±1.0	35	34
Mean PCWP (mmHg)	18±4.6	18±3.5	17±2.2	16±0.5	14	18
RAP (mmHg)	17±4.3	16±4.7	17±2.5	15±3.0	14	15
CO (L/min)	3.8±0.8	3.6±1.3	3.2±0.7	3.5±0.6	2.78	2
CI (L/min/m2)	2.4±0.5	2.2±0.8	2.0±0.4	2.1±0.4	1.67	1.5
Laboratory data
Hemoglobin (g/dL)	12±1.9	12±1.5	12±1.3	12±1.5	14	14
Albumin (g/dL)	3.6±0.5	3.7±0.4	3.7±0.6	3.6±0.5	3.1	4.7
Creatinine (mg/dL)	1.0±0.3	1.2±0.4	0.9±0.04	0.8±0.0	1.3	0.9
Bilirubin (mg/dL)	1.4±0.4	1.4±0.7	1.0±0.4	1.2±0.5	3.3	1.7
Na (mEq/L)	139±2.4	138±3.7	140±2.2	135±5.5	129	134
TTE data (n=34)	(n=12)	(n=15)	(n=3)	(n=2)	(n=1)	(n=1)
LVEF (%)	62±13	60±14	50±13	68±2.5	36	64
LVDd (mm)	43±6.7	46±6.7	44±5.6	47±1.5	45	35
LAD (mm)	42±8.9	52±17	32±2.5	36±3.0	66	38
Surgical procedure (%)
Total pericardiectomy	15 (94)	14 (67)	4 (100)	1 (50)	1 (100)	1 (100)
On pump	6 (38)	6 (29)	0 (0)	0 (0)	0 (0)	1 (100)
Prior CS	–		–	–	–	–
CABG		11 (52)
Valve operation		9 (43)
CABG+valve operation		1 (4.8)

BP, blood pressure; CABG, coronary artery bypass grafting; CI, cardiac index; CO, cardiac output; CS, cardiac surgery; LAD, left atrial dimension; LVDd, left ventricular end-diastolic dimension; LVEF, left ventricular ejection fraction; NYHA, New York Heart Association; PAP, pulmonary artery pressure; PCWP, pulmonary capillary wedge pressure; RAP, right-atrial pressure; TB, tuberculosis; TTE, transthoracic echocardiography.

Cardiac Events

The median follow-up period was 5.7 (range, 0.8–10.3) years. Overall cardiac event-free curves and survival curves from cardiac death are shown in Figure 1A and 1B, respectively. Perioperative mortality rate was 6.7%, and the cause of perioperative death was progressive heart failure in all patients. Respective cardiac event-free survival and survival from cardiac death were 65% and 84% at 5 years, and 55% and 80% at 7 years.

Figure 1.

Overall cardiac event-free survival (A) and freedom from cardiac death (B). Comparison of cardiac event-free survival (C) and freedom from cardiac death (D) among patients with idiopathic CP, post-CS CP, TB-related CP, non-TB-related CP, infarction-related CP, and post-radiation CP. CP, constrictive pericarditis; CS, cardiac surgery.

Figure 1C and 1D show the cardiac event-free survival and survival from cardiac death based on the underlying etiology, respectively. Idiopathic CP and TB-related CP showed favorable outcomes compared with post-CS CP (5-year cardiac event-free survival: idiopathic, 80%; TB-related, 100%; post-CS, 52%). The number of patients with non-TB-related and infarction-related CP was very small, but none experienced a cardiac event, whereas 1 patient with post-radiation CP died from congestive heart failure <1 year after pericardiectomy. Survival from cardiac death elicited similar results (5-year survival: idiopathic, 92%; TB-related, 100%; non-TB-related, 100%; infarction-related, 100%; post-CS, 73%; post-radiation, 0%).

Predictors of Cardiac Events

Table 2 details the results of the univariate analysis to identify predictors of cardiac events. Univariate analysis showed higher age (≥65 years, P=0.033), preoperative AF (P=0.006), preoperative advanced NYHA class (P=0.013), and increased systolic pulmonary artery pressure (P=0.047) to be significant predictors of cardiac events.

Table 2. Univariate Analysis for Predictors of Cardiac Events After Pericardiectomy

	HR (95% confidence interval)	P value
Age (>65 years)	2.51 (1.08–6.30)	0.033
Sex (male)	1.58 (0.60–3.82)	0.34
NYHA class (III or IV)	3.92 (1.30–17.1)	0.013
Comorbidities
Hypertension	1.40 (0.59–3.19)	0.44
Dyslipidemia	0.95 (0.31–2.42)	0.92
Diabetes mellitus	1.85 (0.42–5.95)	0.38
Atrial fibrillation	3.26 (1.41–8.15)	0.006
Coronary artery disease	1.30 (0.55–2.98)	0.54
Pericardial calcification	0.45 (0.16–1.13)	0.09
Data for preoperative catheterization
Systolic BP (per 1 mmHg)	1.00 (0.98–1.03)	0.71
Systolic PAP (per 1 mmHg)	1.06 (1.00–1.12)	0.047
Mean PCWP (per 1 mmHg)	1.04 (0.91–1.18)	0.55
RAP (per 1 mmHg)	0.94 (0.83–1.04)	0.27
CO (per 1 L/min)	0.79 (0.52–1.15)	0.22
CI (per 1 L/min/m2)	0.76 (0.38–1.45)	0.42
Laboratory data
Hemoglobin (per 1 g/dL)	0.85 (0.64–1.12)	0.24
Albumin(per 1 g/dL)	0.93 (0.38–2.20)	0.88
Creatinine (per 1 mg/dL)	2.54 (0.94–5.94)	0.064
Bilirubin (per 1 mg/dL)	0.95 (0.51–1.64)	0.85
Na (per 1 mEq/L)	0.94 (0.86–1.03)	0.22
Surgical procedure
Total pericardiectomy	1.90 (0.69–6.67)	0.23
On pump	1.83 (0.77–4.20)	0.17

HR, hazard ratio. Other abbreviations as in Table 1.

Freedom from cardiac events was lower in patients with preoperative AF (n=19) than in those without AF (n=26) (41% vs. 86% at 5 years; P=0.005) (Figure 2A). Freedom from cardiac events was also lower in patients with preoperative advanced NYHA class (III–IV) (n=32) than in those with NYHA class I–II (n=13) (58% vs. 88% at 5 years; P=0.021) (Figure 2B).

Figure 2.

Comparison of cardiac event-free survival between patients with and without preoperative atrial fibrillation (AF) (A). Comparison of cardiac event-free survival between patients in preoperative New York Heart Association (NYHA) class I–II and those in NYHA class III–IV (B).

Postoperative Changes in Clinical Status and Hemodynamics

Preoperative and postoperative NHYA classes are shown in Figure 3. A total of 32 patients (71%) were in NYHA class III–IV preoperatively, which improved to NYHA class I–II (n=38, 84%) after pericardiectomy. However, 16% remained in NYHA class III even after pericardiectomy.

Figure 3.

Comparison of preoperative and postoperative New York Heart Association (NYHA) class, right-atrial pressure (RAP), and cardiac index (CI) in patients with constrictive pericarditis.

For 26 patients who underwent postoperative cardiac catheterization, we compared preoperative and postoperative RAP and CI. Postoperative RAP decreased significantly (P<0.01). CI also increased postoperatively, but the change was not significant (P=0.12) (Figure 3). Cardiac event-free survival was significantly lower in patients with postoperative RAP ≥9 mmHg (n=13) than in those with RAP <9 mmHg (n=13) (39% vs. 75% at 5 years; P=0.013) (Figure 4A). A subgroup of patients with postoperative CI <2.2 L/min/m² (n=9) also had lower cardiac event-free survival compared with those with CI ≥2.2 L/min/m² (n=17), but the difference was not significant (56% vs. 59% at 5 years; P=0.051) (Figure 4B). Furthermore, there was no significant difference in surgical strategy (partial or total pericardiectomy) among these subgroups. Surgical strategy was not directly related to improvement in hemodynamics, such as postoperative RAP and CI. These cutoff values were determined by median values or clinically meaningful reference values, as described in the Methods.

Figure 4.

Comparison of cardiac event-free survival between CP patients with postoperative right-atrial pressure (RAP) ≥9 mmHg and those with postoperative RAP <9 mmHg (A). Comparison of cardiac event-free survival between the patients with postoperative cardiac index (CI) ≥2.2 L/min/m² and those with postoperative CI <2.2 L/min/m² (B). CP, constrictive pericarditis.

Discussion

In the present study, we examined the etiology of CP, long-term clinical outcomes, and prognostic factors after pericardiectomy among a Japanese population. Long-term clinical outcomes were affected by etiology, and post-CS CP had a higher event rate than idiopathic CP or TB-related CP. Higher age, preoperative AF, advanced NYHA class, and pulmonary hypertension were related to poor clinical outcomes.

Surgical Mortality

Surgical removal of the pericardium is associated with a considerable (6–12%) mortality rate.^13–15 In our study, the perioperative mortality rate was 6.7%, which was in accordance with previous studies. The most common cause of operative death is low-output heart failure.^5,10 In agreement with previous studies, the cause of death was progressive heart failure in all 3 patients who died perioperatively in the present study.

Long-Term Clinical Outcomes and Predictive Factors

Long-term clinical outcomes after pericardiectomy for CP are related to the underlying etiology.^4–7,16 Bertog et al⁵ reported that survival at a median follow-up of 6.9 years was 63% among 163 patients undergoing pericardiectomy. Idiopathic CP was related to the best survival (88%), followed by post-CS CP (66%) and post-radiation CP (27%). Szabó et al found that idiopathic CP and TB-related CP had a good prognosis (81% and 80%, respectively) followed by post-CS (50%), and post-radiation (0%), at 5 years after pericardiectomy.⁶ In the present study, overall event-free survival and survival from cardiac death at a median follow-up of 5.7 years were 62% and 84%, respectively. Post-CS CP showed a poor prognosis compared with idiopathic CP and TB-related CP. Our study population included only 1 patient with post-radiation CP, but this patient died <1 year after pericardiectomy, our result was substantially similar to the reports mentioned above.

Preoperative clinical status, not only the etiology of CP, might affect the prognosis after pericardiectomy. Studies have reported higher age and pulmonary hypertension to be related to poor clinical outcomes,^4,5 which is consistent with our study. Pulmonary hypertension is considered to reflect the severity of constriction and concomitant myocardial dysfunction.⁵

A correlation between preoperative NYHA class and the prognosis after pericardiectomy is well known, as shown in the present study.^4,6 Multi-organ dysfunction may progress, alongside a longer period of time with pericardial constriction and low output. Furthermore, atrophy of myocardial cells may develop during long-term compression by the pericardium. NYHA class is thought to reflect the clinical condition. Therefore, pericardiectomy should be undertaken as early as possible after the diagnosis of CP is made before multi-organ dysfunction and/or myocardial atrophy occurs beyond the point of reversibility.

Furthermore, preoperative AF was related to a high prevalence of cardiac events. The present study is the first to demonstrate the relationship between AF and the prognosis of CP. In early diastole, blood stored in the left atrium is driven into the left ventricle by the high early diastolic atrial-ventricular pressure gradient. At end-diastole, atrial contraction occurs, forcing blood to fill the left ventricle.¹⁷ The left atrium contributes considerably to cardiac function. Among CP patients with AF, the loss of atrial contraction at end-diastole, in addition to the impaired diastolic filling of the left ventricle caused by a constricted pericardial sac, might have a further influence on cardiac filling and output, which may be related to poor clinical outcomes.

Regarding the transthoracic echocardiographic characteristics, previous studies report preoperative high early (E) diastolic mitral inflow velocity and postoperative persistent abnormal diastolic filling pattern on Doppler echocardiography are related to poor prognosis.^18,19 However, our study included old data and several CP patients after mitral valve replacement, so the E velocity and diastolic filling pattern could not be assessed. Furthermore, because of the study’s retrospective nature, serial transthoracic echocardiography had not been performed in all the patients. Therefore, the chronological change in the diastolic filling pattern also could not be evaluated.

Effectiveness of Pericardiectomy

It has been reported that pericardiectomy can provide symptom relief and hemodynamic improvement in most patients, but a certain proportion of patients do not show any postoperative improvement.⁶

In our study, the number of patients in NYHA class III–IV decreased from 32 (71%) to 7 (16%) postoperatively, and RAP and CI also improved. However, 16% of the study patients remained in NYHA class III even after pericardiectomy. This finding may be related to incomplete removal of the pericardial sac, involvement of visceral epicardium, or myocardial atrophy.⁴

As for surgical strategy (partial or total pericardiectomy), its effect on long-term outcomes remains controversial.^12,14,16,20 In the present study, Cox proportional hazard analysis did not identify surgical strategy as a predictor of cardiac events. However, the patients with post-CS CP showed poorer prognosis and higher rate of partial pericardiectomy than the other groups of CP patients. Therefore, it is possible that partial pericardiectomy is related to the poor prognosis of post-CS CP.

Clinical Implications of Postoperative Cardiac Catheterization

In the present study, the subgroup of patients with postoperative RAP ≥9 mmHg had low cardiac event-free survival in comparison with those with RAP <9 mmHg. The subgroup of patients with CI ≥2.2 L/min/m² also had low cardiac event-free survival compared with those with CI <2.2 L/min/m². Our study suggests that patients who achieve release of constriction by pericardiectomy and experience marked improvement in hemodynamics have a good prognosis, whereas those who do not have a release of constriction have a poor prognosis. Therefore, postoperative cardiac catheterization may be helpful in the prediction of long-term clinical outcome after pericardiectomy.

Study Limitations

This is the first study to summarize the long-term clinical outcomes after pericardiectomy for CP among a Japanese population. However, the present study has 3 main limitations.

First, the prevalence of CP was low, therefore, the total number of patients was relatively small. Second, our study population consisted mainly of those with idiopathic CP or post-CS CP, and the number of patient with post-radiation or TB-related CP was limited. This was a single-center retrospective cohort study, and this deviation in etiology was inevitable, and might have affected our results. Third, there was a limited number of patients, so we could not undertake a multivariate analysis to identify prognostic factors after pericardiectomy.

Conclusions

Long-term clinical outcomes after pericardiectomy for CP among a Japanese population were related to the underlying etiology and preoperative clinical condition. Postoperative cardiac catheterization may be helpful in predicting prognosis after pericardiectomy.

Conflicts of Interest / Name of Grant

None.

References

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