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(Circulation. 2003;108:1852.)
© 2003 American Heart Association, Inc.

Clinical Investigation and Reports

Constrictive Pericarditis in 26 Patients With Histologically Normal Pericardial Thickness

Deepak R. Talreja, MD; William D. Edwards, MD; Gordon K. Danielson, MD; Hartzell V. Schaff, MD; A. Jamil Tajik, MD; Henry D. Tazelaar, MD; Jerome F. Breen, MD; Jae K. Oh, MD

From the Division of Cardiovascular Diseases and Internal Medicine (D.R.T., A.J.T., J.K.O.), the Division of Anatomic Pathology (W.D.E., H.D.T.), the Division of Cardiovascular Surgery (G.K.D., H.V.S.), and the Department of Radiology (J.F.B.), Mayo Clinic, Rochester, Minn.

Reprint requests to Jae K. Oh, MD, Division of Cardiovascular Diseases and Internal Medicine, Mayo Clinic, 200 First St SW, Rochester, MN 55905.

Received April 15, 2003; revision received July 7, 2003; accepted July 8, 2003.

	Abstract

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Background— Traditionally, increased pericardial thickness has been considered an essential diagnostic feature of constrictive pericarditis. Although constriction with a normal-thickness pericardium has been demonstrated clinically by noninvasive imaging, the details of clinicopathological correlates have not been described.

Methods and Results— A total of 143 patients with proven constriction underwent pericardiectomy at Mayo Clinic between 1993 and 1999. Their baseline characteristics, operative data, and pathological specimens were reviewed retrospectively. The pericardium was of normal thickness (2 mm) in 26 patients (18%; group 1) and was thickened (>2 mm) in 117 (82%; group 2). The most common causes of constriction in group 1 included previous cardiac surgery, chest irradiation, previous infarction, and idiopathic disease. There was little difference in symptoms and findings on physical examination between the 2 groups. Microscopically, no patient had an entirely normal pericardium. Histopathological abnormalities in group 1 were mild and focal, including fibrosis, inflammation, calcification, fibrin deposition, and focal noncaseating granulomas. Pericardiectomy was equally effective in relieving symptoms regardless of the presence or absence of increased thickness.

Conclusions— Pericardial thickness was not increased in 18% of patients with surgically proven constrictive pericarditis, although the histopathological appearance was focally abnormal in all cases. When clinical, echocardiographic, or invasive hemodynamic features indicate constriction in patients with heart failure, pericardiectomy should not be denied on the basis of normal thickness as demonstrated by noninvasive imaging.

Key Words: pathology • pericarditis • pericardium

	Introduction

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The clinical and diagnostic distinction between constrictive pericarditis and myocardial diseases, especially the restrictive cardiomyopathies, has often been difficult because hemodynamic behaviors of the 2 processes are similar.¹ Pericardial thickness may help distinguish between these processes.² Normal pericardial thickness is 2 mm or less, a thickness greater than 4 mm suggests pericardial constriction, and one greater than 6 mm has a high specificity for constriction.³ The erroneous conclusion has been drawn that the presence of increased pericardial thickness is an essential diagnostic feature of constrictive pericarditis. This dogma has created a clinical dilemma in patients with hemodynamic findings suggestive of constriction present without increased pericardial thickness.

Seifert et al⁴ demonstrated that 12% of patients undergoing pericardial resection had a "normal" pericardium. Despite limited data on the subject, some constricted pericardia may be thin enough to be unrecognized as abnormal by any current preoperative imaging technique.³ The present study was undertaken to examine the clinical and pathological features of patients with a normal-thickness pericardium who have undergone pericardial resection for constriction.

	Methods

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Study Group
From January 1, 1993, through December 31, 1999, all parietal and fused pericardial specimens surgically excised at Mayo Clinic were reviewed under a protocol approved by the Mayo Foundation Institutional Review Board. All patients provided informed consent for review of their medical records and operative specimens and for subsequent follow-up. Among 344 pericardial specimens,⁵ 143 were from patients with pericardial constriction and became the study group for this investigation.

The diagnosis of constrictive pericarditis was made on the basis of clinical, diagnostic, surgical, and pathological criteria. Initially, the clinician integrated information from clinical and diagnostic modalities (computed tomography [CT], MRI, echocardiography, and high-fidelity pressure catheterization) to select patients for pericardiectomy. In cases in which the clinician was uncertain of the diagnosis on the basis of noninvasive and invasive testing, myocardial biopsy was performed. Surgical and pathological findings were subsequently reviewed to confirm the preoperative diagnosis.

Clinical Features
Medical records were reviewed independently by a reviewer blinded to the specific pathological findings. Demographic information recorded included age and gender; historical information relating to the cause of pericardial disease; and relevant symptoms, physical examination findings, and preoperative studies, including echocardiography, cardiac catheterization, and radiographic imaging.

Surgical Procedure
The majority of patients in both groups underwent radical pericardiectomy (19/26 [73%] in group 1 and 100/117 [85%] in group 2), with operative findings recorded at the time of the procedure. Radical pericardiectomy included removal of the anterior (between the phrenic nerves on the right and left, from the level of the great arteries to the diaphragmatic surface), lateral (posterior to the left phrenic nerve), inferior (along the diaphragmatic surface), and posterior (to the atrioventricular junction) sections of the pericardium. Among those patients with less than a complete radical pericardiectomy, all but 3 had complete resection of the pericardium except for small islands of pericardial tissue around the atria. The remaining 3 patients (1 in group 1 and 2 in group 2) had all undergone previous cardiac surgery that resulted in dense diaphragmatic scar tissue that prevented complete resection of this portion of the pericardium. Instead, the pericardial tissue between the 2 phrenic nerves was resected, and a portion of the diaphragmatic pericardium was left behind. Operative reports, hospital discharge notes, and subsequent outpatient and inpatient notes were evaluated for details of the follow-up period.

Pathological Features
Surgical pathology specimens and reports were reviewed for measurements of maximal pericardial thickness grossly (Fig. 1), and the corresponding microscopic slides were examined for the presence of inflammation (acute or chronic), calcification (gross or microscopic), fibrosis, granulation tissue, fibrin deposition, granulomas (caseating or noncaseating, along with results of special stains for specific organisms), hemosiderin deposition, and mesothelial hyperplasia.

View larger version (150K): [in this window] [in a new window]   Figure 1. A, Pericardial specimen from patient with normal pericardial thickness. Pericardial dimension is 1.5 mm in depth with 3 mm of fat on exterior surface of pericardium. B, Pericardial specimen from patient with increased pericardial thickness. Pericardial dimension is 7 mm in depth with fat on exterior surface of pericardium (both specimens, hematoxylin and eosin, original magnification x10).

Statistical Analysis
Detailed demographic, clinical, and pathological characteristics were recorded from all patients and used to create a database retrospectively. All statistical analysis was performed with use of JMP software (SAS Institute, Inc). Univariate analysis with standard t tests was used to compare all continuous variables; when both preoperative and postoperative measurements were available, they were compared with match-pair t testing. All nominal variables were compared with use of the Fisher exact test. All statistical tests were 2 tailed, and a probability value of less than 0.05 was considered to indicate statistical significance.

	Results

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Study Groups
Patients were divided into 2 study groups: those with normal pericardial thickness of 2 mm or less (group 1) and those with pericardial thickness of more than 2 mm (group 2). There were 26 patients in group 1 and 117 patients in group 2.

Clinical Findings
Demographics
Among the 26 patients in group 1 (normal pericardial thickness), the mean age was 60 years (range, 42 to 81 years); 20 patients (77%) were male. A similar distribution was found among the 117 patients in group 2 (increased pericardial thickness), with a mean age of 57 years (range, 12 to 82 years); 88 (75%) were male. Thus, the age and gender distribution were similar for the 2 groups. Comorbid medical conditions (including diabetes mellitus, hypertension, and hyperlipidemia) were more common in group 1, but no association was statistically significant.

Causes of Constriction
Review of the medical records revealed that some patients had more than 1 underlying cause of constriction (Table 1). For group 1, the most common causes were previous cardiac surgery (42%), thoracic irradiation (19%), previous myocardial infarction (12%), and idiopathic disease (12%). For group 2, the most common causes were idiopathic disease (31%), cardiac surgery (25%), infection (20%), and thoracic irradiation (14%). Thus, iatrogenic causes accounted for 61% of group 1 patients and 39% of group 2. Among the causes that were more common in group 1, previous coronary artery bypass grafting (P0.03) and valvular surgery (P0.04) were statistically significant. The only cause more common among group 2 patients by a statistically significant margin was idiopathic disease (P0.001).

View this table: [in this window] [in a new window]   TABLE 1. Causes of Constrictive Pericarditis

Symptoms
The presence of symptoms was similar between the 2 groups. Symptoms suggestive of right heart failure (such as anasarca, abdominal distention, and lower-extremity edema) were slightly more common in group 1 patients. Nonspecific symptoms, including fatigue, anorexia, nausea, dyspepsia, and weight loss, were significantly more common in group 2 patients.

Physical Findings
There was little difference in the physical examination findings between the 2 groups. The single exception was a greater incidence of pericardial rub in patients from group 2 (17% versus 0%; P0.01). Pericardial knock was auscultated in 38% of the patients in group 1 and 44% in group 2 (P0.84). No statistically significant difference was noted in the incidence of elevated jugular venous pressure or the presence of rapid X or Y descents in the jugular venous waveform or the incidence of Kussmaul sign, pulsus paradoxus, muffled heart sounds, ascites, hepatomegaly, splenomegaly, or pleural effusion.

Chest Radiography
Pulmonary vascular congestion was seen more frequently in group 1 than in group 2 (54% versus 27%; P0.02). There was no statistically significant difference between the mean±SD ejection fraction among those with pulmonary vascular congestion, 58%±9.7%, compared with those without pulmonary vascular congestion, 56%±9.6% (P0.30). Pericardial calcification was grossly visible on chest radiography in 10 of 27 patients (37%) from group 1 and 30 of 117 patients (26%) from group 2 (P<0.23). Otherwise, findings on chest radiography did not differ significantly between the 2 groups (Table 2).

View this table: [in this window] [in a new window]   TABLE 2. Findings on Initial Diagnostic Workup

Computed Tomography
CT findings were less often diagnostic of constriction in group 1 than group 2 (Table 2). Abnormal ventricular morphology was seen in patients from both groups but was more common in patients from group 1 (56% versus 25%; P0.02). The finding of calcium in the pericardium was not significantly different between the groups.

Cardiac Catheterization
Respiratory variation was seen more commonly in group 1 patients than in those from group 2 (Table 2). Otherwise, overall results at cardiac catheterization were similar between the 2 groups.

Echocardiography
Echocardiography was more often diagnostic in both groups than any other test performed (Table 2). As with CT, the pericardium appeared thickened in some patients later shown at surgery to have normal pericardial thickness. Although atrial enlargement was more prevalent in group 1 than in group 2, the difference was not statistically significant.

Myocardial Biopsy
Myocardial biopsy was performed only when the treating clinician lacked enough confidence about the diagnosis to proceed to operative pericardiectomy. Ultimately, myocardial biopsy was performed in 2 (8%) of 26 patients from group 1 and 5 (19%) of 26 patients from group 2. In these patients, the biopsy specimens showed nonspecific findings and no evidence of restrictive myocardial diseases.

Surgical Findings
At the time of surgery, measurements of right atrial pressure, pulmonary artery systolic pressure, pulmonary artery diastolic pressure, cardiac output, and cardiac index were performed before and immediately after pericardiectomy. There were no statistically significant differences in these measurements between the 2 groups (Table 3).

View this table: [in this window] [in a new window]   TABLE 3. Hemodynamic Changes at Surgery

Patients in both groups showed significant hemodynamic improvement after resection of their pericardia. The mean right atrial pressure decreased in group 1 patients from a mean of 21 to 12 mm Hg (P<0.001) and in group 2 patients from a mean of 22 to 11 mm Hg (P<0.001). The pulmonary artery systolic pressure decreased in group 1 patients from a mean of 39 to 35 mm Hg (P0.008) and in group 2 patients from a mean of 38 to 32 mm Hg (P<0.001). The pulmonary artery diastolic pressure decreased in group 1 patients from a mean of 20 to 16 mm Hg (P0.008) and in group 2 patients from a mean of 22 to 15 mm Hg (P<0.001). The cardiac index increased in group 1 patients from a mean of 1.9 to 3.0 L · min^-1 · m^-2 (P<0.001) and in group 2 patients from a mean of 2.4 to 3.6 L · min^-1 · m^-2 (P<0.001).

Pathological Findings
No patient in group 1 had an entirely normal pericardium by microscopy; all had either focal fibrosis or focal calcification (Table 4). Of note, inflammation, especially chronic inflammation, was significantly less common in group 1 than group 2 (54% versus 90%; P<0.001). There was no hemosiderin deposition, granulation tissue, or mesothelial hyperplasia among group 1 patients.

View this table: [in this window] [in a new window]   TABLE 4. Pathological Findings

Follow-Up Results
The mean duration of hospitalization as recorded in hospital discharge notes was similar between the groups (14 days for group 1 versus 12 days for group 2; P0.64). The number of deaths during the perioperative and postoperative period (including 30 days after surgery) was also similar (7.6% in group 1 and 3.4% in group 2; P0.61).

Follow-up after hospital discharge was available at a mean of 2.6 years. After exclusion of perioperative deaths, patients in both groups showed improvement in functional class (Fig. 2). In the group 1 patients, the mean New York Heart Association functional class decreased from 3.1 to 1.9 (P<0.001). In group 2 patients, the mean functional class decreased from 2.9 to 1.6 (P<0.001). During subsequent long-term follow-up, patients from both groups had similar responses to surgery. The mortality rate remained similar over the total available period of follow-up; there were 7 deaths (29%) in group 1 and 27 (23%) in group 2.

View larger version (19K): [in this window] [in a new window]   Figure 2. New York Heart Association heart failure class for patients before and after pericardiectomy. Postoperative assessment was done at first follow-up contact. Patients who died in perioperative period were excluded. Numbers in parentheses indicate numbers of patients.

	Discussion

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Numerous investigators have attempted to correlate the noninvasive diagnosis of increased pericardial thickness with pathological findings.^1,6,7 CT, especially ultrafast and cine-gated CT, and MRI are most often used to assess pericardial thickness noninvasively. Moncada et al² used CT to examine the pericardia of 15 patients with symptoms suggestive of pericardial disease and found pericardial thickening by CT in 9 of 10 patients whose biopsy specimens showed thickened pericardium. Isner et al⁷ reviewed 7 patients with constrictive or restrictive physiology and verified that the 4 who had thickened pericardium on CT (4 mm) were the only patients with pericardial thickening on pathological examination. Isner et al⁸ studied another 34 patients with suspected pericardial disease; 9 had pericardial thickening on CT scan, which was verified by tissue analysis in 4 (the remainder had no pathological evaluation).

Few studies have shown a correlation between normal pericardial thickness on radiographic imaging and normal thickness on pathological examination. Oren et al⁹ reported that in a group of 12 patients with hemodynamic findings suggestive of constrictive pericarditis on noninvasive and invasive workups, 5 had pericardial thickening by both CT and tissue analysis, and 7 had normal pericardial thickness by both examinations. In addition to CT and MRI, echocardiography has been used to assess pericardial thickness. Although echocardiographic results depend more on operator technique and gain settings, increased thickness can often be noted as well, with reasonable correlation to findings at pathology.¹⁰ Clearly, the data suggest the utility of these techniques as surrogates for assessing increased pericardial thickness.

Our findings confirm the concept that constrictive pericarditis can occur in patients with normal pericardial thickness. In fact, in the present study, pericardial thickness was normal in 18% of patients with surgically proven constrictive pericarditis. The histopathological appearance was abnormal in all patients with normal-thickness pericardial constriction, although the abnormalities were mild or focal in nature.

Traditionally, pericardial constriction has been associated with a normal-sized heart with restricted diastolic filling secondary to a rigid calcific pericardial shell. We believe that a thin pericardium may underlie a similar pathophysiological process in some patients. Rather than being like a suit of armor encasing the heart, the constriction is analogous to the thin wet suit worn by a diver. Even in patients with prominent pericardial thickening and calcification, progressive constriction may be the result of not only fibrocalcific thickening but also shrinkage in pericardial volume. Although the pericardium consists primarily of extracellular collagen (with very little elastic tissue), it is still living tissue with fibroblasts to replenish collagen that degenerates over time. If the rate of collagen production is less than the rate of its degradation, then pericardial volume progressively decreases. In this manner, constriction could result even with a pericardium of normal thickness. Given the retrospective nature of the present study, patients entered the study as the diagnosis of constrictive pericarditis was made by the treating clinician. Therefore, a limitation of the study is the inability to include patients with constrictive pericarditis in whom the diagnosis was not made on the basis of clinical and diagnostic evaluation. Further studies, especially prospective investigations, are needed to test this concept.

The present study reiterates the importance of assessing hemodynamic data in making the diagnosis of constrictive physiology. Although radiographic determination of pericardial thickness is often taken into account during the assessment, increased pericardial thickness does not necessarily imply constriction. Conversely, normal pericardial thickness does not necessarily exclude a diagnosis of constrictive pericarditis. Radical pericardiectomy is the definitive treatment for constriction and generally improves cardiac hemodynamics by reestablishing normal physiological filling of cardiac chambers. It should not be denied because of normal pericardial thickness demonstrated by noninvasive imaging when clinical, echocardiographic, or invasive hemodynamic features indicate constriction.

	References

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This Article Abstract Full Text (PDF) All Versions of this Article: 108/15/1852    most recent 01.CIR.0000087606.18453.FDv1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Talreja, D. R. Articles by Oh, J. K. Search for Related Content PubMed PubMed Citation Articles by Talreja, D. R. Articles by Oh, J. K. Related Collections Pericardial disease