(Circulation. 1996;94:1635-1641.)
© 1996 American Heart Association, Inc.
Articles |
Pericardioscopy in the Etiologic Diagnosis of Pericardial Effusion in 141 Consecutive Patients
the C Division of Cardiology (O.N., A.M., P. de G., P.G., G.D.), Heart Hospital, and the Division of Thoracic Surgery (H.P., A.W.), Calmette Hospital, University of Lille, France.
Correspondence to Alain Millaire, MD, PhD, Service de Cardiologie C Hopital Cardiologique, Centre Hospitalier Regional Universitaire, Bld du Pr Leclercq, 59037 Lille Cedex, France.
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Abstract |
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Background Although previous small series have documented the utility of pericardioscopy for accurate etiologic diagnosis of pericardial effusion, this technique remains underused. The aim of our study was to assess the benefits and risks of surgical pericardioscopy in a large prospective series.
Methods and Results One hundred forty-one consecutive patients with unexplained pericardial effusion underwent 142 pericardioscopies with a rigid mediastinoscope. For each patient, the etiologic data obtained by pericardioscopy (visualization of pericardium, guided biopsies, subxiphoid window biopsy, and fluid analysis) were compared with the results that would have been obtained with only conventional surgical drainage and biopsy (subxiphoid window biopsy and fluid analysis). After complete workup, a specific cause was found in 69 cases (48.6%); the other 73 cases were considered idiopathic effusions (51.4%). Procedural and in-hospital mortality was 8 of 141 patients (5.6%). No death was directly attributable to pericardioscopy. During long-term follow-up (median duration, 24 months; range, 6 to 96), a previously unrecognized cause was discovered in 6 patients (4%). By comparing the areas under the receiver-operating characteristic curves, the diagnostic advantage of pericardioscopy was significant for the whole series (pericardioscopy, 0.98±0.011; conventional surgical drainage, 0.89±0.029; P<.001). The increase in sensitivity was more marked for some types such as neoplastic (21%), radiation-induced (100%), or purulent (83%) effusions.
Conclusions Our data demonstrate that pericardioscopy increases the diagnostic sensitivity of surgical pericardial drainage and biopsy without specific risk.
Key Words: pericarditis • pericardium • diagnosis • surgery • biopsy
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Introduction |
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Pericardial effusions may be caused by a variety of disorders.1 Some of these diseases have very poor prognoses, whereas others require specific therapy; an accurate etiologic diagnosis is therefore particularly important. We have previously reported on patients in whom a specific and sometimes severe etiology has been found after completion of a careful workup: aortic dissection,2 malignancies,3 postradiation,4 Still's disease,5 mycoplasma pneumoniae,6 and Q fever.7
Since the first description by Santos and Frater,8 we and others have documented the utility of PCS.9 10 11 12 13 14 15 Despite these studies, all of which demonstrate the advantages of the technique and the absence of significant side effects, recent papers still rely on the classic pericardiocentesis and/or subxiphoid window biopsy for diagnosis, without discussion of alternative techniques.16 17 18 The most probable reason for this is that clinicians consider the arguments for the use of PCS too weak or based on small series.
A prospective study in patients with PEs was started in our hospital in 1985 with the following objectives: (1) to assess the etiologic diagnostic yield of PCS compared with pericardiocentesis and subxiphoid window biopsy, (2) to assess the risk of PCS, and (3) to follow up our patients to confirm the accuracy of our diagnosis after PCS.
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Methods |
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Patient Selection
All patients referred with pericarditis to the University of Lille (France) tertiary referral center between July 1985 and September 1993 were considered for inclusion. Among these patients, those who had a PE that required drainage for diagnostic or therapeutic purposes were included in the study. Patients referred after September 1993 were excluded from this report to allow adequate follow-up. Patients with recent myocardial infarction or recent cardiac surgery were excluded, as were patients with hypothyroidism (because the diagnosis of thyroid disorders is generally made rapidly and such patients generally do not require drainage since the PE decreases with thyroid supplementation). The initial patients included in this study were included in previous reports.3 12
PCS Technique
All procedures were performed with patients under general anesthesia except for some patients with tamponade in whom local anesthesia was used. An incision was made over the distal sternum, xiphoid, and upper abdomen. The anterior rectus fascia was opened, and the xiphoid process was removed. A plane was dissected beneath the sternum by use of blunt dissection, and the pericardium was then identified. Needle aspiration of the fluid was performed for cytological, biochemical, bacterial, and immunologic studies. Excision of a small portion of the subxiphoid pericardium was then performed for histological examination (called subxiphoid window biopsy). A rigid mediastinoscope developed by Maassen (length, 17 cm) or a pericardioscope developed by Wurtz (length, 23 cm) was subsequently inserted into the pericardial sac. The pericardial surfaces were directly visualized through the mediastinoscope. PCS-guided biopsies were performed under direct visualization on abnormal-appearing areas of the pericardium (subsequently referred to as guided biopsy). Complete fluid aspiration was performed, and if necessary, deposits were removed from the pericardial cavity. The mediastinoscope was then removed, and a chest tube was left in place for further drainage. After drainage, the tube was removed, and the incision was closed.
All patients had cytological, biochemical, bacterial, and immunologic studies of the pericardial fluid, as is usual in pericardiocentesis. Histopathological examination of the subxiphoid window biopsy was also performed, as is usual in classic subxiphoid surgical drainage. Finally, PCS specifically enabled us to perform two diagnostic tests: direct visualization of the pericardial surfaces and guided biopsies of suspicious areas. The various appearances of the pericardium that are considered diagnostic criteria were described previously.12
Study Protocol
Besides PCS, all patients had a careful clinical history and physical examination, a chest x-ray, an ECG, red and white blood cell counts, erythrocyte sedimentation rate count, serum urea and creatinine tests, a tuberculin skin test, a sputum analysis for tuberculous bacilli, a test for antinuclear antibodies, antistreptolysin titer, rheumatoid factor determination, viral titers (including human immunodeficiency virus), thyroid function tests, a serum amylase test, and tumor markers.
The diagnosis of PE was established in all patients by 2D echocardiography. In some patients, other imaging techniques (CT scan or MRI) were performed either because of poor echogenicity or because the clinical or echocardiographic data required confirmation or more accurate data.
A PE was classified as acute if the symptoms lasted <1.5 months, subacute if >1.5 months and <3 months, and chronic if >3 months or discovered incidentally. Hemodynamic tolerance of PE was assessed with clinical (presence of pulsus paradoxus) and echocardiographic (diastolic collapse of the right ventricle and/or right atrium) criteria.
Follow-up
Short-term follow-up was performed by a review of hospital records. Events recorded included mortality possibly related to PCS (ie, occurring during PCS) and in-hospital mortality (during the 10 days after PCS). Data concerning potential complications of PCS also were collected. After discharge, patients were treated with colchicine to prevent recurrent PE.19
For long-term follow-up, the referring general practitioners or cardiologists and the patients were contacted by telephone to ascertain whether PE had recurred, whether a previously unrecognized possible cause for the PE (eg, neoplasm) had been established, and whether the patient was alive. In some cases, the etiologic diagnosis was obtained only after open-chest cardiac surgery or at autopsy.
Diagnostic Yield of PCS
Because PCS is an investigation that cumulates several diagnostic tests (some of which can also be obtained by pericardiocentesis or classic subxiphoid surgical drainage), each test was considered separately. If the biochemical, bacterial, cytological, or immunologic analysis of the fluid provided a definitive diagnosis, this diagnosis was considered as having been established by pericardiocentesis. If pericardial biopsy through the subxiphoid window established a definite diagnosis, this diagnosis was considered as having been obtained by classic subxiphoid surgical biopsy. If direct visualization of the pericardial surfaces and/or guided biopsies of suspicious areas visualized by PCS established the definite diagnosis, this diagnosis was considered as having been obtained by PCS. False-negative diagnoses on PCS were assessed if a potential cause was revealed during the follow-up period.
A PE was considered idiopathic if the complete workup (including PCS) did not reveal any specific cause and if direct visualization showed either normal pericardial surfaces or slightly inflamed surfaces with negative guided biopsies. A PE was considered as paraneoplastic if the complete workup was negative but the patient had a recent history of extracardiac neoplasm. In such situations, to enable a comparison with previously published work,18 20 we considered PCS unproductive if the diagnosis was made during follow-up. In patients with suspected tuberculous PE (in whom definite diagnosis by culture for tuberculous bacilli generally requires 2 months), the diagnosis was considered as having been obtained by PCS if direct visualization of the pericardium showed typical or suggestive appearances (without direct visualization of tuberculous bacilli in pericardial fluid) with or without typical histological findings or as having been obtained by subxiphoid window biopsy if histological examination showed typical appearances. In cases of postradiation PE, the diagnosis was considered as having been obtained by PCS if the fluid tests and the subxiphoid window biopsy were negative and direct visualization was typical or suggestive. The diagnosis of purulent PE was considered as having been established by pericardiocentesis if altered white blood cells were present (cultures were consistently negative in our cases because of previous empirical antibiotic treatment) or if the fluid had a purulent appearance and by PCS if the diagnosis was established on the basis of visual inspection of the pericardium without conclusive findings after analysis of pericardial fluid.
PCS Safety
The PCS technique did not change throughout the study period. However, because some of the initial patients studied died during induction of anesthesia, subsequent patients who had clinical or echocardiographic signs of tamponade had an initial transcutaneous pericardial drainage before PCS. This approach was begun September 1989. Mortality was compared for the two approaches.
Statistical Analysis
Continuous data are reported as means and ranges; categorical data are given as percentages. Comparison of categorical percentages was performed with the 
2 test, with the Yates correction used when appropriate. Differences were considered significant for values of P<.05. To calculate the diagnostic sensitivity of PCS, subxiphoid window biopsy, and pericardiocentesis, we considered the final diagnosis at the end of the follow-up as the reference standard. To calculate specificity, we considered as false positives the patients in whom the diagnosis obtained with PCS was altered during the follow-up. If PCS was initially nondiagnostic (eg, giving a diagnosis of idiopathic PE) but a definite diagnosis was obtained during follow-up, such cases were considered false negatives.
The ability of each technique (pericardiocentesis, subxiphoid window biopsy, or PCS) to discriminate between patients with and without specific causes (idiopathic and paraneoplastic effusions) was determined by means of ROC curves. The area under each ROC curve was derived from the Wilcoxon statistic.21 A five-category scale was used to produce the ROC curve (definitely nonspecific, possibly nonspecific, questionable, probably specific, and definitely specific with respect to the final etiology [ie, after follow-up]). Correlation between areas was determined with the Kendall 
test. Comparison of areas under the ROC curves was performed by the method of Hanley and McNeil22 with a two-tailed z statistic.
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Results |
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Study Population
Four hundred and sixteen patients with acute or chronic pericarditis were admitted to our unit during the inclusion period. Among these patients, 275 were excluded because they had pericarditis without a significant PE, an obvious cause (eg, hypothyroidism), or a PE that rapidly resolved under medical treatment. The remaining 141 patients (97 men, 44 women) are the subject of this report. They had 142 PCSs (1 patient with a non-Hodgkin's lymphoma had 2 PCSs in 9 months; the second episode of pericardial effusion occurred after radiation therapy). Mean age was 54.2 years (range, 18 to 82 years). PE was acute in 47 patients (33%), subacute in 39 (27.5%), and chronic in 56 (39.5%). In 2 chronic PEs, the pericarditis was effusive-constrictive. Pericardial tamponade was the presenting feature in 20 patients (14%).
Two-dimensional echocardiography was performed in all patients. In 101 patients (72%), a thoracic CT scan also was performed.
PCS was performed in all but 3 patients under general anesthesia. The approach was subxiphoid in all but 4 patients who had a thoracic approach because of a history of surgery for esophageal neoplasm (2 patients) or an anterior mediastinal tumor that hindered a subxiphoid approach (1 patient) or because PCS had been performed a few months earlier (1 patient). The mean volume of fluid withdrawn was 350 mL (range, 50 [in a patient with previous transcutaneous drainage] to 1200 mL).
PCS Safety
Mortality during surgical PCS was 2.1% (3 patients). Death occurred during induction of anesthesia (ie, before PCS) despite immediate percutaneous drainage. In-hospital mortality was 3.5% (5 patients). The causes of death were pulmonary embolism (2 patients), acute respiratory distress caused by severe bronchospasm (1 patient), septicemia (1 patient), and ventricular fibrillation (1 patient). All deaths occurred in patients with very severe illnesses or very poor general conditions: pericardial metastases (n=4), fungal PE and AIDS (n=1), pulmonary neoplasm with metastases (n=1), rheumatoid polyarthritis with acinetobacter septicemia (n=1), and purulent PE after staphylococcus septicemia (n=1).
Morbidity was represented by premature ventricular beats occurring during PCS and ending after withdrawal of the pericardioscope.
Etiologic Diagnosis After PCS
A specific cause was found after complete workup, including PCS in 69 patients (48.6%). The different causes are reported in Table 1
. In the other 73 patients (51.4%), no specific cause was found to explain the PEs. Table 2 gives the decisive diagnostic tests for some specific causes.
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Follow-up
Long-term follow-up (mean duration, 24 months; range, 6 to 96 months) was available in 93% of patients. Overall mortality was 46%. The main causes of mortality (35%) were progression of a neoplasm in patients with a neoplastic, paraneoplastic, or radiation-induced PE or overwhelming infection in patients with purulent PE. In the other patients who died (11%), the cause of death was not related to their pericardial diseases.
There was no false-positive diagnosis in our series; thus, the specificity of our workup with PCS was considered 100%. However, in 1 patient, a potential false positive was initially suspected. Indeed, a discrepancy was initially found between direct visualization of pericardium (considered normal) and the results of pericardial biopsies (considered carcinomatous lymphangitis). Because a second analysis of the biopsies was reported as compatible with nonspecific inflammation, this patient was considered to have an idiopathic PE. The follow-up confirmed this diagnosis (the patient was still alive after 52 months).
During this follow-up, a previously unrecognized cause of PE was discovered in 6 of the 141 patients. The overall sensitivity of our workup with PCS was thus considered 96%. The 6 false negatives included 2 patient with malignant effusions, 1 with chronic aortic dissection, and 3 with an extracardiac cancer without pericardial involvement. In the first patient with malignant PE, PCS was performed under local anesthesia, so PCS was difficult and incomplete. Early death occurred as a result of acute respiratory distress (history of severe silicosis). Autopsy revealed local invasion of the pericardium and myocardium from a bronchial carcinoma. In the second patient, a rhabdomyosarcoma was undetected after a complete workup for PE (2D echocardiography, CT scan, MRI, and PCS). One month later, failure of the right side of the heart occurred and led to the diagnosis of rhabdomyosarcoma by 2D echocardiography. The diagnosis was confirmed by CT scan and MRI. In the patient with an aortic dissection (the dissection was considered chronic because the chest pain had occurred 2 months before), a workup with echocardiography and PCS did not detect the true cause of the PE. A CT scan performed during follow-up aided in the correct diagnosis and showed thrombus formation in the false channel of the dissection.2 In the last 3 patients, a neoplasm was discovered during the first year of follow-up (2 to 10 months). In these 3 patients, PCS initially showed a normal pericardium and no recurrence of PE occurred during follow-up.
Relapses of PE occurred in 13 patients (9.2%) during the first 9 months of follow-up. Of the 13 patients, 2 required corticosteroid therapy, and 1 had further multiple recurrences and became corticodependent.
ROC Analysis
The areas under the ROC curves (see the Figure) were 0.78 for pericardiocentesis (SE=0.039), 0.89 for subxiphoid window biopsy (SE=0.029), and 0.98 for PCS (SE=0.011). The comparison of the areas under the curves for PCS compared with pericardiocentesis showed a statistically significant difference (z=5.34, P<.001), as did the comparison between the areas under the curves for PCS and subxiphoid window biopsy (z=3.57, P<.001).
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Comparison of Early and Late Experiences
Comparison of the safety of PCS during the initial (July 1985 through September 1989) and the subsequent (September 1989 through September 1993) periods shows that no perioperative deaths occurred during the late period, although 3 deaths occurred during the early period. In-hospital mortality was also lower (2 of 80 patients, 2.5%) during the late period than the early period (5 of 62 patients, 10%). The differences, however, were not statistically significant.
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Discussion |
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Diagnostic Yield of PCS
With respect to the specificities of PCS (direct visualization of pericardial surfaces and guided biopsies), our study clearly demonstrates the usefulness of PCS. In our 141 patients, the diagnostic yield of PCS was superior to that of pericardiocentesis or subxiphoid surgical drainage (Table 2
and the Figure). This result is based on the largest series of patients published to date (Table 3).8 9 10 11 12 13 14 15 23 24 25 26 27 The superiority of PCS was particularly noticeable for neoplastic PE because this diagnosis would otherwise have been missed in 5 patients (5 of 24 neoplastic pericarditis, 21%) if PCS and guided biopsies had not been performed (Table 2). This increase in sensitivity (21%) for PCS compared with subxiphoid window biopsy is similar to that previously reported in a smaller series of patients.3 This superiority was also evident for radiation-induced pericarditis and tuberculous pericarditis. In radiation-induced pericarditis, PCS enabled a positive diagnosis to be reached by visualizing a diagnostic appearance of the pericardium, not just by excluding other possible diagnoses (such as metastases). The increase in sensitivity was thus considered 100% (see Table 2). In tuberculous PE, PCS enabled a rapid positive diagnosis (because diagnostic features were immediately visualized), and it was not necessary to await the results of cultures (obtained in 2 months) to initiate antituberculous therapy. The increase of sensitivity can be considered to be 66% (Table 2). Conversely, for normal-appearing pericardium, antituberculous therapy was not initiated. Follow-up confirmed the accuracy of the initial diagnosis. This superiority of PCS was more evident because the diagnostic yield of pericardiocentesis was low in our study (18.3%). Such low yields were previously described by other authors who reported values ranging from 6% to 26%.18 20 The diagnostic value of subxiphoid window biopsy also was low in our study (23.2%; ie, an increase of 4.9% compared with pericardiocentesis) as in other studies (0% to 5%).18 20 This increase in sensitivity of PCS would have been even higher if we had considered normal findings on PCS diagnostic of idiopathic PE. Indeed, in such patients, the diagnosis was stated with a greater security by the completeness of PCS (compared with classic surgical drainage), although a definite diagnosis can be confirmed only by a favorable long-term outcome.
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These diagnostic advantages of PCS could explain why our proportion of patients with idiopathic PE was low (35.9%) compared with series that did not use PCS (78% to 86%).18 20 However, comparison of our results with other studies dealing with the etiologic diagnosis of pericarditis is difficult because the inclusion criteria are quite different. Although all patients in our series had PE, 46% of the patients reported by Permanyer-Miralda et al20 and 40% of the patients reported by Zayas et al18 did not have PE. Whereas all types of PE were included in our study, Permanyer-Miralda et al and Zayas et al excluded chronic PE; Permanyer-Miralda et al also excluded patients with known neoplastic disease or radiation. Finally, we excluded from the subgroup of idiopathic PE those patients who had documented extracardiac neoplasms and classified such effusions as paraneoplastic PE. Indeed, we previously demonstrated that such patients had poor prognoses, most of them dying within 1 year.3 Even when these patients with paraneoplastic PE (19 patients) are added to those with true idiopathic PE (51 patients), the total remains lower (49.3%) than the usual proportion of idiopathic PE.
False negatives could nevertheless have occurred in our series (in particular in the subgroup of paraneoplastic PE) as reported previously.3 In the present series, two false negatives were discovered; one probably was caused by the difficulty of adequate inspection of the pericardium under local anesthesia. However, our follow-up was careful (93% of the patients) and relatively long (mean duration, 24 months). This follow-up was long enough to ensure that all previously unrecognized causes of PE would be diagnosed. Indeed, the longest time to discovery of a previously unrecognized cause for PE was <1 year in our study. Other studies did not demonstrate that longer follow-up would enable diagnosis of other unrecognized causes: no new diagnosis was found in the report of Permanyer-Miralda et al20 after 31 months and two cancers were diagnosed after 1 year in the report of Zayas et al.18
PCS Safety
In our series, as in the previously published series (Table 3), PCS did not increase the mortality or morbidity of surgical drainage. No death was directly related to PCS. During the second period of the present study, after the hemodynamic state of patients with poor hemodynamic intolerance (transcutaneous pericardial drainage before PCS, as described by other authors24 ) was improved, no death was related to the hemodynamic tolerance of the PE. Performing PCS under local anesthesia is another possibility in cases of tamponade. However, local anesthesia was responsible for one of our two false negatives (Table 1). Other authors consider that the induction of anesthesia should begin only if the subxiphoid approach can be performed immediately.15
Study Limitations
Our study did not allow us to compare the results of surgical PCS with those of medical pericardiocentesis with or without 2D echocardiographic guidance, which is considered to have a low risk (no mortality for guidance with 2D echo28 ). Whatever the risk of pericardiocentesis, this technique has a low sensitivity (18.3% in our series) and does not permit pericardial biopsies, which are very often required for etiologic diagnosis.
Our study did not allow us to compare PCS with other techniques: flexible pericardioscope,9 11 percutaneous PCS,14 or PCS through a thoracic approach with video.24 25 26 27 All these techniques are more or less variants of the standard technique with some refinements (eg, a minimally invasive approach) rather than truly different techniques. Among these different techniques, video-assisted thoracoscopy has become popular because of its minimal invasiveness. Despite excellent visualization of the pericardium, the diagnostic superiority of this new technique has not yet been clearly proved by recent work based on limited series.24 25 26 27 The most attractive advantage of this technique could be a therapeutic advantage because a larger window of pericardium can be excised through thoracoscopic approach than through the subxiphoid route, which might lead to a lower incidence of recurrence.8 26 29 However, despite generally small windows (4x4 cm) in our series, our recurrence rate was similar to that reported by Piehler et al,29 who performed partial or complete pericardiectomies (9.2% versus 10%). Our recurrence rate could possibly be related to the favorable effect of colchicine.19 On the other hand, video-assisted thoracoscopy had some significant limitations: (1) a stable hemodynamic state is required because this technique is performed with the patient under general anesthesia in a lateral position and with an ipsilateral pulmonary collapse and (2) only the ipsilateral side can be correctly visualized.
The limitations of rigid PCS were described previously.3 In particular, some parts of the pericardial cavity, ie, the lateral wall of the left ventricle, cannot be correctly investigated. This is one reason for long-term follow-up. Another possibility would be to combine the PCS with a thoracoscopic approach in case of negative PCS or a suggestive CT scan or MRI.
Study Implications
For further studies dealing with etiologic diagnosis of PEs, PCS should be systematically recommended (or at least discussed) in PEs that require diagnostic investigations or interventional treatment.
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Selected Abbreviations and Acronyms |
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Footnotes |
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Presented in part at the XVIIth Congress of the European Society of Cardiology, Amsterdam, August 20-24, 1995.
Received February 1, 1996; revision received April 8, 1996; accepted April 14, 1996.
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References |
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