Revista Mexicana de Cardiología C C B R Vol. 27 No. 2 April-June 2016 Biventricular secondary to calcified tuberculous constrictive : a case report and review

Falla cardiaca biventricular secundaria a pericarditis constrictiva calcificada de origen tuberculoso: reporte de un caso y revisión

Víctor Hugo Contreras-Gutiérrez*

Key words: Pulmonary ABSTRACT RESUMEN , heart failure, calcifi ed A 41-year-old man with a medical history of pulmonary Un hombre de 41 años con antecedente de tuberculosis . tuberculosis presented to the emergency department com- pulmonar se presentó en el servicio de urgencias refi rien- plaining of progressive dyspnea, lower limbs edema and do un cuadro de disnea progresiva, edema de miembros Palabras clave: increased abdominal volume of three months of evolution. inferiores e incremento del volumen abdominal de tres Tuberculosis He was diagnosed of heart failure by clinical fi ndings. meses de evolución. El paciente fue diagnosticado de pulmonar, However imaging tests showed a heavily thickened cal- insufi ciencia cardiaca por los hallazgos clínicos. Sin insufi ciencia cifi ed pericardium and bilateral pleural eff usion. A skin embargo estudios de imagen mostraron un pericardio cardiaca, pericardio tuberculin test was performed, giving a positive result. importantemente calcifi cado y derrame pleural bilateral. calcifi cado. The diagnosis of biventricular heart failure secondary to Se realizó la prueba de tuberculina, siendo positiva. Se lle- calcifi ed tuberculous pericarditis was reached. The patient gó al diagnóstico de insufi ciencia cardiaca biventricular rejected surgical intervention and conservative treatment secundaria a pericarditis constrictiva de origen tubercu- for heart failure as per guidelines was implemented. loso. El paciente rechazó la intervención quirúrgica y se implementó tratamiento conservador para falla cardiaca sustentado en guías.

INTRODUCTION pericarditis and neoplastic pericardial diseases and high (20-30%) in bacterial pericarditis, onstrictive pericarditis is the result of a especially purulent pericarditis.3 Cchronic inflammatory process that leads to In constrictive pericarditis the diastolic fill- scarring, thickening, fibrosis and calcification ing of the ventricles is impaired and clinical of the pericardium which leads to impaired manifestations are generally those of right heart diastolic filling of the heart. The most common failure with preserved left ventricular func- causes are mediastinal radiation, chronic idio- tion, at least in the first stages of the disease. pathic pericarditis, and after cardiac surgery in Symptoms include fatigue, peripheral edema, developedwww.medigraphic.org.mx countries. However, tuberculosis is breathlessness, passive hepatic congestion, * Medical Resident at still the most frequent cause in the developing nonspecific abdominal complaints; and as the the General Hospital of and underdeveloped world, as well as, in im- disease progresses, abdominal swelling second- Mexico. munocompromised patients.1,2 It can occur af- ary to ascites, jaundice, generalized edema and ter virtually any pericardial disease process but cardiac cirrhosis. Other important signs are the Received: 09/05/2016 the risk of progression is related to the etiology; recurrent pleural effusions and syncope, due Accepted: being low (1%) in viral and idiopathic pericar- to low output status secondary to reduced 11/07/2016 ditis, intermediate (2-5%) in immune-mediated preload.3-7

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The jugular veins are distended. The normal bpm and right with a QRS inspiratory drop in jugular venous distention axis to 90o without any other alteration. Chest may be replaced by a rise in venous pressure X-ray showed right pleural effusion and signs (Kussmaul’s sign) due to a right ventricle unable of congestive heart failure with an enlarged to accommodate the blood proceeding from cardiac silhouette, redistribution and interstitial the venous return, being into a fixed space, edema. It was observed an area of increased delimited by the stiff pericardium. Kussmaul’s density suggestive of a calcified pericardium sign is also present in cases of severe right heart (Figure 1). failure, especially in association with tricuspid Echo imaging reported dilated right heart regurgitation. Pulsus paradoxus is present cavities with paradoxical septum motion, re- when systolic pressure decreases more than duced right ventricular systolic function with 10 mmHg during inspiration, and it is second- a tricuspid annulus plane systolic excursion ary to the shift of the interventricular septum (TAPSE) of 13 mm (normal > 17), elevated to the left, impeding an adequate filling of the systolic pulmonary artery pressure (SPAP) of left ventricle. The classic auscultatory finding of 65 mmHg, mild tricuspid regurgitation and pericardial constriction is a pericardial knock a restrictive diastolic filling pattern, with an that occurs as a high-pitched sound early in E/A index of 2.4. The pericardium layers were diastole when there is the sudden cessation hyperechoic. of rapid ventricular diastolic filling. When ac- A computed tomography (CT) scan was curately recognized, a pericardial knock is a performed to obtain a better visualization of specific but insensitive indicator of pericardial the pericardium. It showed a thick and heavily constriction.1-7 calcified pericardium affecting the most part of In many cases of chronic pericardial con- the cardiac circumference. A moderate right striction, definitive treatment is surgical and pleural effusion, as documented previously consists in wide resection of both pericardial on chest X-ray, was still present (Figure 2 A-C). layers, however it has a high mortality risk that Extension of the CT scanning to the abdomen, goes from 6 to 12% according to different case showed hepatic and splenic enlargement, ac- series.1,3-9 companied by moderate ascites (Figure 3). On his medical history, he referred having CLINICAL CASE been diagnosed of pulmonary tuberculosis

A 41-year-old man with a medical history of pulmonary tuberculosis presented to the emer- gency department complaining of dyspnea, lower limbs edema and increased abdominal volume of 3 months of evolution. This occasion with exacerbation of symptoms. On first examination, elevated jugular ve- nous pressure was evident, with an estimated

pressure of 11 cmH2O; rales at the base of both lungs were auscultated, with decreased respira- tory sounds at the base of the right lung; gen- eralized edema was present, mainly affecting the lowerwww.medigraphic.org.mx limbs; first and second heart sounds were diminished in intensity, and a prominent third heart sound (a pericardial knock) in early diastole was present. The patient was admitted to hospitalization for hemodynamic stabiliza- Figure 1. Chest X-ray showing signs of congestive heart tion and further research. failure with right pleural eff usion, an enlarged cardiac It was documented on electrocardiogram silhouette, and an image of increased density (arrows) (ECG) the presence of sinus of 130 suggestive of pericardial calcium.

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Figure 2 A-C. Thoracic CT imaging at diff erent axial segments showing a thickened calcifi ed pericardium and moderate right pleural eff usion.

of cases in human immu- nodeficiency virus (HIV) infected people, and for 50-70% in developing countries where tu- berculosis is endemic. Congestive heart failure secondary to chronic compression is the most common clinical presentation. Mortality in these patients is high, ranging from 17-40% at six months after diagnosis.3 In the world extra-pulmonary tuberculosis represents 10% of cases. Tuberculous pericar- ditis, caused by tuberculosis, is found in approximately 1% of all autopsied cases of tuberculosis and in 1% to 2% of in- Figure 3. Abdominal CT showing hepatic and splenic stances of the pulmonary form of the disease. enlargement accompanied by ascites. The incidence of the disease is highly variable depending on regional aspects, in Latin America it goes from 0.5% to 1.5% and till 2007 showing three years ago and that he interrupted treat- an annual decrease of approximately 5%.10 In ment voluntarily at the third month of initia- 2009 in Mexico 17.5% of tuberculosis cases tion with no subsequent following up. A skin were extra-pulmonary.11 tuberculin test was performed, being positive. In México it has been observed an as- Calcified tuberculous constrictive pericardi- sociation between tuberculosis and diabetes tis was diagnosed and first-line antitubercular mellitus, malnutrition, and alcohol and drugs agents were initiated. Surgical treatment (peri- consumption. Overcrowding and a low cultural cardiectomy) was proposed to the patient, level are also risk factors to have the disease.12 explaining the benefits and risks of the pro- Pericardial involvement usually develops by cedure. He refused surgical intervention, and retrograde lymphatic spread of M. tuberculosis pharmacological therapy for heart failure as per from peritracheal, peribronchial, or mediastinal guidelines was implemented. lymph nodes or by hematogenous spread from www.medigraphic.org.mxprimary tuberculous infection. The lymphatic DISCUSSION drainage of the pericardium is primarily to the anterior and posterior mediastinal and tracheo- Tuberculous pericarditis is not a frequent cause bronchial lymph nodes as suggested by the pat- of heart failure in the developed world, ac- tern of lymphadenopathy seen in tuberculous counting for less than 4% of pericardial disease pericarditis.13,14 in these countries; however in underdeveloped The immune response of the pericardium to countries it does account for more than 90% the protein antigens of the bacillus induce a de-

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layed hypersensitivity response, stimulating the volume. For this reason the expansion of the releasing of cytokines by lymphocytes, which heart chambers during diastole is limited by activate macrophages and lead to granuloma the rigid pericardial sac with an impeded atrial formation. This hypersensitivity reaction is or- contribution to mid- and late diastolic filling, chestrated by TH-1 lymphocytes. The histologi- while the early diastolic filling is unimpeded. cal pattern seems to be affected by the immune The predominant ventricular filling will fall in status of the patient, with fewer granuloma the first third of diastole. This produces the formation in HIV-infected patients.13 hemodynamic dip-plateu pattern or square Four pathological stages of tuberculous root sign of ventricular filing pressures during pericarditis are recognized: (1) fibrinous exu- cardiac catheterization the rapid «Y» descent in dation with initial inflammatory infiltration; (2) the jugular venous pressure and plateau during serosanguinous effusion with a predominantly right heart catheterization.4,5,7,16 lymphocytic exudate with monocytes and foam Doppler echocardiography is useful for the cells; (3) absorption of effusion with granulo- diagnosis of constrictive pericarditis and help matous caseation and pericardial thickening distinguish it from restrictive cardiomyopa- caused by fibrin and collagen leading to fibrosis; thy.5,7,9 In constrictive pericarditis because of and (4) constrictive scarring.13,14 the reciprocal filling changes with respiration, Nowadays is not common to observe a the tricuspid velocity increases in inspirations severe calcification of the pericardium, be- while the mitral velocity decreases. This phe- cause it occurs much less commonly in those nomenon represents the enhanced ventricular patients with constrictive pericarditis secondary interaction, which characterizes constrictive to radiation or a previous surgery; in which pericarditis but it is absent in both normal sub- the pericardial thickness may even be normal. jects and cases of restrictive .5 However in tuberculous constrictive pericarditis Although pulmonary embolism, right it is not so infrequent to observe calcification ventricular infarction, and chronic obstruc- of the pericardium.4 tive lung diseases, must be also considered. The main differential diagnosis is made Several echocardiographic parameters can between pericardial constriction and restric- be used to differentiate among them. Cardiac tive cardiomyopathy.1-9,15 In both conditions magnetic resonance (CMR) and computed to- ventricular filling is restricted and a high driv- mography (CT) are best suited to visualize the ing pressure across the valves at the time of pericardium.1,3,6-8 In CT and CMR, the healthy atrioventricular valve opening results in early pericardium is normally visualized as a fibrous rapid diastolic filling and an abrupt increase lining surrounding the heart with a minimal in ventricular pressure.4,7 In a healthy person fluid layer. Minimal pericardial calcifications during inspiration there is an increase in fill- are early detectable in thoracic CT.5 ing of the right ventricle because of enhanced According to the recent European guide- venous return but filling of the left ventricle is lines transthoracic echocardiography and chest unaffected during the whole cardiac cycle. In X-ray are recommended in all patients with a patient with constrictive pericarditis, during suspected constrictive pericarditis, though the inspiration the left ventricle is underfilled and latter is not useful to visualize calcifications in there is a reciprocal increase in filling of the the pericardium, they can be seen sometimes right ventricle, while during expiration occurs in lateral views in the posterior border.3 CT and/ the opposite.4 or CMR are indicated as second-level imaging Constrictivewww.medigraphic.org.mx pericarditis is characterized techniques to assess calcifications, pericardial by an early rapid filling and equalization of thickness, and degree and extension of peri- end diastolic pressures in all four cardiac cardial involvement. However cardiac cath- chambers. Because of increased ventricular eterization is indicated only when non-invasive interdependence in constrictive pericarditis, diagnostic methods do not provide a definite the right ventricle expands during inspiration diagnosis of constriction.1-8 producing a ventricular septal shift towards the The benefits of pericardiectomy are well es- left ventricle, without a change in total cardiac tablished for permanent constrictive pericardi-

Rev Mex Cardiol 2016; 27 (2): 95-100 www.medigraphic.com/revmexcardiol Contreras-Gutiérrez VH. Biventricular heart failure secondary to calcifi ed tuberculous constrictive pericarditis 99

tis. Surgical intervention can provide complete have a good response to antitubercular drugs, at relief of symptoms,4 however, a wide resection least in the first stages of the disease. However of both pericardial layers has to be made, and severe calcification of the most part of the peri- though it can be of great benefit for the af- cardium, the last stage of progression of tisular fected patients, the mortality risk during the affection, is not frequently observed and has a procedure is high, reaching 6-12% according to poor prognosis if not surgically treated. different reports. Major complications include The case of our patient showed a non- acute perioperative cardiac insufficiency and common pattern of severe pericardial affection ventricular wall rupture.3,4,6 that played a major role in the therapeutic deci- In a case series reported in Mexico 30 years sions. As mentioned above the degree of the ago, 48% of patients presented complications calcifications and the pericardial adherences to Esteafter documento pericardiectomy, es elaborado being por Medigraphic low-output heart the myocardium posed the patient into a higher failure, right atrium lesion, bleeding, left ven- risk of mortality during and/or after the surgical tricle lesion, pulmonary thromboembolism and intervention, however it is the only intervention pneumothorax in that order the most frequent.16 that would allow to improve the prognosis in In a more recent report from the US in 2004 the this stage of the disease. most frequent cause of death in the periopera- Although there are several risk factors that tive period was still low-output heart failure.17 allow the progression of the disease, our patient Some patients may not benefit from peri- lack the majority of them; he had no immuno- cardiectomy and this may be due to myocar- logic compromise, no chronic or degenerative dial compliance abnormalities, myocardial disorders, and referred a low level of alcohol atrophy after prolonged constriction, residual consumption. However his social conditions, constriction or other myocardial processes.1,5 a poor understanding of the disease and the Techniques have been described in which importance of treatment adherence, played a utilization of laser or ultrasound are effective major role in leading him to this chronic fatal for the debridement of the adherences of an complication. extensively calcified pericardium to the epicar- dium, which have an increased bleeding risk. ETHICAL DISCLOSURES Areas of strong calcification or dense scaring may be left as islands to avoid major bleeding. • Animal and human protection. The authors Occasionally, some patients are candidates to declare that in this research no animal or video-assisted thoracoscopic pericardiectomy human experiments have been performed. in experienced centers.1,3,6,7 • Data confidentiality. The authors declare Long-term survival after pericardiectomy that in this manuscript there are no data for constrictive pericarditis have been found that identifies any patient. to be related to underlying etiology. Idiopathic • Right to privacy and informed content. The cases have shown the best survival rate than authors declare that in this manuscript there miscellaneous groups, including tuberculous are no data that identifies any patient. pericarditis. The impact of pericardial calci- fication on perioperative mortality is still not clear, although some studies have reported an REFERENCES increased mortality in these patients.17 Medical therapy is supportive, and aimed 1. Little WC, Freeman GL et al. Pericardial disease. Cir- at controllingwww.medigraphic.org.mx symptoms of congestion with culation. 2006; 113 (12): 1622-1632. diuretics in advanced cases, and when surgery 2. Permanyer-Miralda G. Acute pericardial disease: ap- 5,8 proach to the etiologic diagnosis. Heart. 2004; 90: is contraindicated or at high risk. 252-254. 3. Yehuda Adler, Philippe Charron, Massimo Imazio et al. CONCLUSIONS 2015 ESC Guidelines for the diagnosis and manage- ment of pericardial diseases. European Heart Journal. 2015; 36: 2921-2964. Pericardial disease is not a rare form of mani- 4. Nishimura R. Constrictive pericarditis in the modern festation of tuberculosis infection, and it usually era: a diagnostic dilemma. Heart. 2001; 86: 619-623.

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