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Ann Thorac Surg 2006;82:1519-1521
© 2006 The Society of Thoracic Surgeons

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Case Reports

Tuberculous Pericardial Effusion After Coronary Artery Bypass Graft

^a Department of Cardiac Surgery, Hammersmith Hospital, London, United Kingdtom
^b Department of Infectious Disease, Hammersmith Hospital, London, United Kingdom
^c Department of Histopathology, Hammersmith Hospital, London, United Kingdom
^d Department of Immunology & Molecular Pathology, University College London, Windeyer Building, London, United Kingdom

Accepted for publication February 7, 2006.

^_* Address correspondence to Dr Hornick, Department of Cardiac Surgery, National Heart and Lung Institute, Imperial College, 2nd Floor, B Block, Hammersmith Campus, Du Cane Rd, London, W12 0NN, UK (Email: p.hornick{at}imperial.ac.uk).

	Abstract

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We describe a case of a recurrent pericardial effusion after coronary artery bypass grafting. This was initially considered to be due to post-pericardiotomy syndrome, but was later treated empirically as tuberculosis. After definitive surgery for this condition, pericardial histology and immunohistochemistry confirmed the diagnosis of tubercular pericarditis. At 4-months follow-up, while continuing anti-tuberculous therapy and corticosteroids, the patient showed consistent improvement without further recurrence of his pericardial effusion. Local reactivation of tuberculosis after pericardiotomy has not been previously reported and merits careful consideration in population groups in which tuberculosis is highly endemic.

	Introduction

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Tuberculosis (TB) constitutes a significant world health burden. Although less common in the developed world, its rising incidence has been of increasing concern. It is well known that TB represents a common cause of pericardial effusion in population subgroups at risk. This report outlines a unique case whereby a patient undergoing coronary artery bypass grafting developed a recurrent post-pericardiotomy effusion due to reactivation of dormant TB.

A 47-year-old Indian man, who has resided in the United Kingdom for more than 30 years, underwent elective coronary artery bypass grafting (CABG) for ischemic heart disease. He had no past history of TB. At the time of surgery, he had been well with no antecedent symptoms. He had a normal preoperative assessment including chest roentgenogram, full blood count, and renal and liver biochemistry. At operation, no pericardial abnormalities were noted and there was no effusion. He was discharged fit and well on postoperative day 10. During the ensuing 3-month period he presented twice with exertional breathlessness. At these times he was afebrile with no leukocytosis or rise in his C-reactive protein. However, on each occasion, a computed tomographic scan and transthoracic echocardiography revealed a significant pericardial collection that was completely drained using minimally invasive methods providing full symptomatic improvement. Six weeks after discharge, he again presented with a large compromising pericardial effusion. On this occasion, a large pericardial window was fashioned together with insertion of a pericardial drain. Tissue and pericardial fluid specimens were collected for histology, immunohistochemistry, and microbiology.

Despite the absence of any constitutional symptoms, and an anergic 10-unit Mantoux skin test, in view of the recurrent effusions and his ethnicity, the risk of TB was considered to be sufficiently high to warrant empirical anti-TB treatment. Therefore he was started on combination therapy with Rifater (Aventis Pharma, Kent, UK), comprising a daily dose of 720 mg of rifampin, 300 mg of isonaizid and 1.8 g of pyrazinamide, together with 400 mg/day of moxifloxacin (ethambutol not used due to color blindness) and corticosteroids (80 mg prednisolone). This presumptive diagnosis of TB was supported by histologic examination of the resected pericardial tissue, which showed epithelioid cell granuloma with Langhans-type giant cells. The epithelioid granulomas were immunohistochemically positive with a polyclonal antibody specific to mycobacterium TB (anti-MTB polyclonal, Novocastra plc, Newcastle, UK) (Fig 1).

View larger version (126K): [in this window] [in a new window]   Fig 1. (A) Hematoxylin and eosin, pericardium, with macrophage and epithelioid cell granuloma containing giant cells. (B) High power view of granuloma containing Langhans-type giant cell (nuclei at one end, open arrowhead). (C) Immunohistochemistry for tuberculosis (TB)-specific antigens. Sections were rabbit affinity-adsorbed antibodies specific to Mycobacterium TB (anti-MTB polyclonal, Novocastra plc, Newcastle, UK) were incubated according to the manufacturer's instructions and were developed with immunoperoxidase and di-amino-benzidine (brown). This procedure will detect not only intact bacilli but TB-specific epitopes derived from proteolytic degradation (eg, in lysosomes or in antigen-presentation pathways). (D) Immunohistochemistry controls. (Main image = negative control [pre-immune rabbit serum] corresponding to C). Inset: TB-IHC (immunohistochemistry) on positive control tissue containing known AAFBs (acid-alcohol-fast bacilli), showing immunopositive TB bacillus (arrow) and macrophages immunopositive for TB-antigen (red arrowhead) (scalebars = distance indicated).

	Comment

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The development of a late pericardial effusion with variable clinical symptoms such as fever, chest pain, and malaise after coronary artery bypass surgery is commonly ascribed to postcardiac injury syndrome, a term that includes post-pericardiotomy syndrome and Dressler syndrome [1]. Indeed, Tsang and colleagues [2] noted that of 209 hemodynamically significant late pericardial effusions, just more than one third were considered to be due to postcardiac injury syndrome, with anticoagulation causing a hemopericardium in the remaining cases. Although postcardiac injury syndrome can still be of a recurrent nature, such recurrences need to be considered with utmost concern and also warrant a thorough investigation, particularly in the context of TB.

In general, TB pericardial effusions are relatively uncommon in developed countries, and there are no reports after pericardiotomy. Sagrista-Sauleda and colleagues [3] studied 322 patients with pericardial effusions for a 6-year period and found TB as a cause in only 2%. Nevertheless, increasing international migration has increased the risks. The incidence of TB has been rising by 25% in England for the last 10 years with 2 in 5 cases found in London and 7 in 10 being from an ethnic minority background [4]. Tuberculous pericarditis usually spreads from the lungs, mediastinal nodes, or bony structures, but can also spread through the hematogenous route. It may sometimes be associated with an effusion. Progression commonly leads to a constrictive pericarditis. The mortality rate in untreated acute effusive tuberculous pericarditis approaches 85% [5].

Identification of Mycobacterium TB in pericardial fluid or tissue, or the presence of caseous granulomas in histologic examination of pericardial tissue establishes the diagnosis [5]. Finding acid-alcohol-fast bacilli (AAFB) within the granuloma is conclusive, but insensitive. In contrast, TB immunohistochemistry is both sensitive and specific [6]. This is probably because antibodies detect not just intact bacilli, but also epitopes that are generated from the processing of killed bacteria. In addition, even in isolated broth suspensions of mycobacteria, immunohistochemistry is several fold more sensitive than AAFB [6]. Thus, TB immunohistochemistry may differentiate between TB and other causes of epitheloid cell granulomas (eg, sarcoidosis). Our TB immunohistochemistry was confirmed by positive control tissue that confirmed the antibodies were positively stained identifiable bacilli in addition to more diffuse staining of the granuloma macrophages.

Once diagnosed with TB, patients are treated with anti-TB therapy for a period of 6 months. Controversy remains regarding the use of steroids in TB pericarditis. Nevertheless, systematic review of the literature, especially trial data from South Africa, indicates that they may have a role in nonresolving effusions [7].

Cardiopulmonary bypass [8] and surgery are known to be immunosuppressive. We postulate that this immunosuppression led to reactivation of tubercular pericarditis causing large recurrent pericardial effusions until appropriate anti-TB treatment was initiated.

A high index of suspicion and early investigation is required in recurrent pericardial effusions after cardiac surgery, especially in immigrant populations. Although immunohistochemistry is a very sensitive and novel mode of diagnosis, treatment with anti-TB drugs and steroids may need to be started empirically and will help to prevent long-term complications.

	References

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1. Khan AH. The post cardiac injury syndromes Clin Cardiol 1992;15:67-72.[Medline]
2. Tsang TS, Barnes ME, Hayes SN, et al. Clinical and echocardiographic characteristics of significant pericardial effusions following cardiothoracic surgery and outcomes of echo-guided pericardiocentesis for management: Mayo Clinic experience, 1979-1998 Chest 1999;116:322-331.[Abstract/Free Full Text]
3. Sagrista-Sauleda J, Merce J, Permanyer-Miralda G, Soler-Soler J. Clinical clues to the causes of large pericardial effusion Am J Med 2000;109:95-101.[Medline]
4. Stopping tuberculosis in England: an action plan from the Chief Medical Officer. Department of Health, Oct 2004. Available at: http://www.dh.gov.uk/PublicationsAndStatistics/Publications/PublicationsPolicyAndGuidance/PublicationsPolicyAndGuidanceArticle.html. Accessed December 30, 2005..
5. Maisch B, Seferovic PM, Ristic AD, et al. Guidelines on the diagnosis and management of pericardial diseases executive summary; the Task force on the diagnosis and management of pericardial diseases of the European Society Of Cardiology Eur Heart J 2004;25:587-610.[Free Full Text]
6. Ulrichs T, Lefmann M, Reich M, et al. Modified immunohistological staining allows detection of Ziehl-Neelsen-negative Mycobacterium tuberculosis organisms and their precise localization in human tissue J Pathol 2005;205:633-640.[Medline]
7. Ntsekhe M, Wiysonge C, Volmink JA, Commerford PJ, Mayosi BM. Adjuvant corticosteroids for tuberculous pericarditis: promising, but not proven Q J Med 2003;96:593-599.
8. Markewitz A, Faist E, Lang S, Endres S, Fuchs D, Reichart B. Successful restoration of cell-mediated immune response after cardiopulmonary bypass by immunomodulation J Thorac Cardiovasc Surg 1993;105:15-24.[Abstract]

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Sampurna M. Tuladhar Philip Hornick Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Tuladhar, S. M. Articles by Hornick, P. Search for Related Content PubMed PubMed Citation Articles by Tuladhar, S. M. Articles by Hornick, P. Related Collections Pericardium