A New Classification for Pleural Effusions After CABG Surgery
By Jay T. Heidecker, MD
To print for Mac press 'Cmd+p' on your keyboard. To print for Windows press 'Ctrl+p' on your keyboard.
Objectives
To understand the causes of pleural effusions during different time intervals following coronary artery bypass graft (CABG) surgery.
To understand the pathophysiology and clinical presentation of the postcardiac injury syndrome.
To provide the differential diagnosis and varied clinical presentation of late post-CABG pleural effusion.
To understand the pathophysiology and management of trapped lung and its resultant pleural effusion.
Key words: coronary artery bypass graft; pleural effusion; postcardiac injury syndrome; trapped lung
Abbreviations: CABG = coronary artery bypass graft; IMA = internal mammary artery; LDH = lactate dehydrogenase; PCIS = postcardiac injury syndrome
Coronary artery bypass graft (CABG) surgery is performed on more than 600,000 patients per year in the United States.1 Patients commonly develop pleural effusions directly related to this surgery, making this procedure one of the most common causes of a pleural effusion. The cause and management differs because of the varied pathogenesis and time course of these pleural effusions. These effusions can be most appropriately categorized by time intervals: (1) perioperative (within the first week); (2) early (within the first month); (3) late (2 to 12 months); and (4) persistent (after 6 months).
Although the pathophysiology of pleural effusions in the perioperative period following CABG can differ, these effusions usually will resolve without intervention. The effusions that occur later than 1 week and within 1 month typically are associated with acute chest pain and fever and usually require antiinflammatory medication. The persistent effusions are the consequence of dysfunctional healing of the pleural space resulting in a visceral pleural peel or fibrosis, which may lead to a trapped lung that may require decortication.
Perioperative CABG Pleural Effusions
Pleural effusions have been reported to occur in the immediate postoperative period in 41 to 87% of patients.2-5 These effusions are typically small and left-sided but can be bilateral. There are two distinct pleural effusions directly related to CABG in the perioperative period: (1) effusions resulting from atelectasis from diaphragm dysfunction; and (2) hemorrhagic effusions from internal mammary artery (IMA) harvesting. In addition, pleural effusions from congestive heart failure may occur following CABG.
Pleural Effusions From Diaphragm DysfunctionClinical CharacteristicsAtelectasis is extremely common after CABG and may be related to diaphragm paresis/paralysis. Fedullo and colleagues6 observed left diaphragm dysfunction (detected by comparing right and left diaphragm excursion by ultrasonography) in 8 of 48 post-CABG patients (16%). Direct cold cardioplegia, associated with an increased incidence of left lower lobe atelectasis7 and effusion,8 induced phrenic nerve paresis,8 which lasted from 6 to 28 days.7 In a study of 30 patients, Vargas and colleagues5 found an 87% incidence of atelectasis by CT scan 2 days post-CABG; this atelectasis was associated with small and often bilateral effusions. They also found a significant correlation between the degree of atelectasis and presence of pleural effusion between postoperative day 2 and 7 (r=0.53; p=0.0025).5 Therefore, most immediate post-CABG effusions are caused by atelectasis.
Diagnosis, Management, and SequelaeThe pleural effusions that result from diaphragm dysfunction are often diagnosed by their radiographic appearance. The effusions are small, with associated ipsilateral atelectasis on the left; thoracentesis is rarely performed. Management of these effusions is conservative. Avoidance of direct topical cold cardioplegia may lessen the risk of phrenic nerve paresis/paralysis and atelectasis. Early mobilization, incentive spirometry, and effective pain control will also minimize atelectasis. An improvement in postoperative pain and FVC has been documented with the use of subxiphoid chest tubes.9 These pleural effusions usually resolve spontaneously within 2 weeks without clinical sequelae.
Pleural Effusions From IMA HarvestingClinical CharacteristicsThe surgical technique employed can affect the development of pleural effusions following CABG in the immediate postoperative period. The use of an IMA graft tends to result in an ipsilateral pleural effusion more frequently than a saphenous vein graft (87% vs 47% at postoperative day 6; p<0.05; n=200).4 The presumed cause of pleural effusions related to IMA harvesting is parietal pleural injury. When the IMA is harvested with the pleural and thoracic fascia intact, the reported incidence of postoperative pleural effusion is 5 to 11%,10,11 but increases to 2010 to 50%11 when the pleura and thoracic fascia are incised. Large pleural effusions in the immediate postoperative period occur with an incidence of 0.5 to 8.5%.4,12,13
Diagnosis, Management, and SequelaeThe larger pleural effusions are typically hemorrhagic and inflammatory, with elevated protein and lactate dehydrogenase (LDH) levels.14 In a study of therapeutic thoracentesis for symptomatic patients following CABG, the early large effusions had a mean RBC count of 706,000/mL, mean WBC count of 30,000/mL with 39% eosinophils, and a mean LDH of 1,368 U/dL.15 Usually, only one or two thoracenteses were required for resolution.14 Diclofenac may decrease pleural effusions following CABG and could be considered for treatment of large effusions.16 As some patients with a persistent pleural effusion following CABG can develop a trapped lung17 (vide infra), patients with a symptomatic effusion should be followed after therapeutic thoracentesis to ensure resolution.
Other Perioperative Pleural Effusions Not Directly Related to CABG
Following cardiac surgery, some patients develop a stunned myocardium. Intraoperatively, patients often require substantial volume loading because of redistribution of fluids secondary to increased vascular permeability. An increase in myocardial water by 3.5% has been shown to decrease cardiac output by 40%.18 Thus, as fluid redistributes into the vascular space in patients with a transient stunned myocardium, pulmonary edema with bilateral pleural effusions can develop. Noncardiogenic pulmonary edema from a systemic inflammatory response may rarely be causative. Other causes of pleural effusions in the immediate postoperative period to be considered include pleural infection, pulmonary embolus, and chylothorax. These pleural effusions can usually be distinguished by their clinical presentation and pleural fluid analysis. The causes of immediate post-CABG pleural effusions and their characteristics based on pleural fluid analysis are listed in Table 1.
Table 1. Perioperative Post-CABG Pleural Effusions (Within 1 Week of Surgery)*
Clinical Characteristics
Radiograph Findings
Pleural Fluid Analysis
Proposed Mechanism
Management
Sequelae
Atelectasis
Immediate postoperative period; often associated with splinting
Ipsilateral volume loss; small, left- sided effusion
Transudate
Phrenic nerve dysfunction; splinting
Spontaneous resolution
Resolution of diaphragm dysfunction can be slow (over weeks)
Bloody effusion
Small to large effusion; within days of CABG
Left -sided, small to large effusion
Bloody, neutrophilic, exudative
Pleural injury from IMA harvesting
Thoracentesis if symptomatic, large effusion; usually resolves spontaneously
Can progress to chronic lymphocytic effusion of unknown etiology
CHF
Dyspnea, lower-extremity edema, PND, orthopnea
Bilateral effusions; right > left; pulmonary edema
Mononuclear- predominant transudate
Myocardial edema from SIRS; underlying ischemia
CHF management
None
Rare effusions
Pulmonary embolus
Ipsilateral chest pain, acute dyspnea
Small effusion; may have peripheral consolidation
Bloody, PMN-predominant exudate; transudate (20%)
Ischemia/infarct; transudate from atelectasis
Anticoagulation
Usually no sequelae
Empyema
Fever, chest pain, purulent drainage from chest tube
Moderate to large effusion; loculation; may have ipsilateral infiltrate
Pus, neutrophil-predominant exudates, pH < 7.20; Gram stain may reveal organism
Contamination from chest tube; sequela of hospital-acquired pneumonia
Antibiotics, drainage
Can progress to pleural sepsis and later trapped lung if untreated
Chylothorax
Dyspnea; immediate postoperative period
Usually left-sided; can be right-sided and massive
Exudative; milky, high triglycerides; chylomicrons present
Thoracic duct or collateral injury during surgery
Low-fat diet; parenteral nutrition; thoracic duct ligation or pleurodesis for severe cases
Malnutrition and infection with prolonged chest tube drainage
*CHF = congestive heart failure; PND = paroxysmal nocturnal dyspnea; SIRS = systemic inflammatory response syndrome; PMN = polymorphonuclear leukocyte.
Early Post-CABG Pleural EffusionsPostcardiac Injury SyndromeHistory: Dressler,19 in 1958, described a syndrome characterized by fever, chest pain, ECG evidence of pericarditis, pleurisy, and pneumonitis in 44 patients following myocardial infarction. The syndrome occurred within days of the myocardial infarction and was associated with frequent relapses. The term postcardiac injury syndrome (PCIS) was introduced by Stelzner and colleagues20 in 1983 to include the characteristic syndrome following myocardial infarction, cardiac surgery, penetrating chest trauma, pericardial injury, or pacemaker placement. PCIS following cardiac surgery is relatively common. In a prospective study of 86 patients, the incidence was 30%.21 Pleural effusions as a result of the PCIS have a similar pathogenesis, clinical presentation, pleural fluid analysis, natural history, and treatment.
Clinical Presentation: The true incidence of PCIS is unknown. In a series of 400 pediatric patients surviving intrapericardial surgery, the incidence of PCIS, clinically associated with increased serum antimyocardial antibodies, was 27%.22 Following CABG, the incidence of complete PCIS with symptoms and antimyocardial antibodies has been reported to be 13%, with 26% described as having the clinical syndrome only.23 When the syndrome is mild, symptoms can be mistaken for postoperative surgical pain and fever that can readily be treated with antiinflammatory medications. PCIS effusions can occur within a few days or up to 1 year after CABG, with the most common appearance at 3 weeks. Thus, PCIS can overlap with perioperative and late post-CABG effusions. However, unlike perioperative post-CABG effusions, patients with PCIS manifest characteristic clinical features. The typical syndrome includes pleuritic chest pain (91%), fever (66%), pericardial rub (63%), and dyspnea (57%) with an elevated erythrocyte sedimentation rate (~62 mm/h) (96%),20 pleural effusions (83%), and parenchymal infiltrates (74%) occurring within 3 weeks of CABG.20 Crackles (51%), an enlarged cardiac silhouette (49%), leukocytosis (49%), and a pleural rub (41%) commonly occur. Figure 1 illustrates a characteristic radiograph of PCIS. An ECG may demonstrate diffuse ST-segment elevation consistent with pericarditis.
Figure 1. Radiographic appearance of patient with PCIS. Note the presence of pleural effusion with alveolar infiltrates.
Pathogenesis: PCIS is likely caused by an exaggerated immune response. After myocardial injury, myocardial antigens appear to be released into the circulation. Antibodies against heart sarcolemma, skeletal muscle sarcolemma, and endothelium have been found in 16 (84%), 17 (90%), and 18 (95%) of 19 patients, respectively, who had PCIS following cardiac surgery.24 In contrast, 28 patients who underwent cardiac surgery but had no PCIS symptoms manifested these antibodies less commonly: 5 (18%), 7 (25%), and 8 (29%), respectively.24 The natural history of serum antimyocardial antibody titers is elevation by postoperative day 14 with a gradual decline over 30 days. The rise and fall in antibody titers appears to mimic the clinical course of the patient.21 In our opinion, the uncommon reporting of PCIS in current literature may be attributed to masking by antiinflammatory and pain medications.
Diagnosis, Treatment, and Sequelae: Pleural fluid analysis can be useful in confirming the diagnosis of post-CABG PCIS effusion.20 The pleural fluid from PCIS is characteristically a hemorrhagic exudate. The protein level is >3.0 g/dL, the pH is usually >7.40, and the LDH level is clearly in the exudative range.20 If pleural fluid analysis is performed within 10 days of the initial clinical symptoms, the predominant cell will be the neutrophil; after 10 days, macrophages and lymphocytes predominate.20 Pleural fluid characteristics of the effusions that occur in the early post-CABG period are listed in Table 2.
Patients with PCIS usually require antiinflammatory therapy for relief of symptoms,20,25,26 including prednisone in some cases. Approximately 50% of patients will relapse and need additional antiinflammatory therapy. With the recent data of an increased risk of myocardial infarction from rofecoxib,27 cyclooxygenase-2 inhibitors should be avoided in these patients. In addition, indomethacin has been shown to impair ventricular healing following myocardial infarction.28 Therefore, in the setting of recent myocardial ischemia, we recommend aspirin for antiinflammatory treatment. Corticosteroids typically result in rapid resolution of symptoms20,25,29; however, early withdrawal often results in recurrence.29 Given the deleterious effect of corticosteroids on wound healing and recurrence of PCIS effusions following withdrawal, we reserve corticosteroids for patients with moderate to severe persistent symptoms. Narcotics should be considered for patients with severe chest pain. Therapeutic thoracentesis should be performed if clinically significant dyspnea is present; however, it will not alter the natural course of PCIS.
Most patients will have resolution of PCIS without clinically important sequelae. However, there have been cases of delayed pericardial tamponade following cardiac surgery from PCIS.30 More importantly, PCIS has been implicated in cases of late constrictive pericarditis after CABG.31 Whether PCIS plays a role in the development of trapped lung following CABG or graft failure is uncertain. Although tamponade, constrictive pericarditis, and graft failure are uncommon, they can result in morbidity and be life-threatening. Therefore, patients with PCIS effusions should be followed closely during the course of the illness and periodically after resolution.
Late Post-CABG Pleural Effusions
There are four distinct effusions that occur 2 to 12 months following CABG, the so-called late effusions. They include the following: (1) PCIS-related effusions; (2) lymphocytic effusions of uncertain cause; (3) effusions due to constrictive pericarditis; and (4) effusions from lung entrapment. The distinguishing characteristics of these effusions are shown in Table 3. PCIS effusions have previously been discussed (vide supra). A 20% incidence of pleural effusions 3 months following CABG was reported in a series of 200 patients; however, a thoracentesis was required in only a few patients (1.5%).12 In patients with large pleural effusions not from congestive heart failure, management options include observation, serial thoracenteses, chest tube drainage, fibrinolytics, pleurodesis, pericardial stripping, or decortication depending upon the cause of the effusion, morbidity to the patient, and complexity of the affected pleural space.
Lymphocytic Exudative Effusions of Uncertain CauseLymphocytic exudative effusions of uncertain cause can either persist following CABG or appear months later. Possible causes of these effusions include persistent lymphatic injury related to surgery13 and immune mechanisms, such as PCIS.13,32 Unlike typical PCIS effusions and the perioperative pleural effusions that likely occur from pleural injury with IMA harvesting, these effusions are not hemorrhagic. The resolution of these effusions is slower than in those arising from direct pleural injury13; persistence may require definitive therapy. Pleural histology reveals active lymphocytic inflammation without fibrosis.17 It is our opinion that the majority of these post-CABG lymphocytic effusions of uncertain cause represent a chronic form of PCIS with minimal symptomatology. In general, management should be conservative, with therapeutic thoracentesis for symptom relief or a trial of steroids; thoracoscopic pleurodesis should be reserved for those with persistent symptoms that affect quality of life.
Constrictive Pericarditis Effusions Constrictive pericarditis is an uncommon cause of late pleural effusions following CABG. Presenting symptoms include dyspnea with exertion, abdominal swelling, and peripheral edema. The physical examination typically reveals jugular venous distension, deep X and Y descents, hepatomegaly, and a Kussmaul sign. Bilateral pleural effusions are common. Thoracentesis reveals a transudate, unless there is early effusive-constrictive pericarditis from PCIS, in which case a bloody exudate may be present. The diagnosis of constrictive pericarditis is established at left and right heart catheterization with decreased cardiac output, equalization of pressures across the cardiac chambers during diastole, and a characteristic “dip and plateau” of right and left ventricular diastolic pressures indicative of early rapid ventricular filling followed by a rapidly elevated pressure from the noncompliant pericardium. In one series,31 23 of 37 patients (62%) with constrictive pericarditis following CABG had antecedent PCIS. The pleural effusions from constrictive pericarditis resolve following pericardiectomy.
Effusions from Lung EntrapmentThe incidence of pleural effusions from lung entrapment following CABG is unknown. Lung entrapment is defined as a process in which the lung is prevented from expanding to the chest wall with a concomitant inflammatory pleural process. For a pleural effusion to form from lung entrapment, the shape of the unexpandable lung must be significantly different from the chest wall so that chest wall conformation cannot occur.33 This creates a persistent negative intrapleural pressure that generates a chronic pleural effusion. However, in contrast to a trapped lung from remote inflammation/infection, there is a persistent inflammatory or malignant process with lung entrapment. Pleural effusion from lung entrapment likely represents a transition between the persistent lymphocytic, exudative pleural effusion after CABG and a trapped lung. Thoracentesis typically reveals a lymphocycte-predominant exudate. Management of the patient with lung entrapment from a persistent post-CABG effusion depends on the degree of symptoms. We routinely perform pleural manometry to evaluate these patients so that they can be appropriately referred for video-assisted thoracoscopic surgery if they have significant dyspnea related to their effusion.33
Table 3. Late Post-CABG Pleural Effusions (Occurring 2 to 12 Months Following CABG)*
Clinical Characteristics
Radiograph Findings
Pleural Fluid Analysis
Proposed Mechanism
Management
Sequelae
Lymphocytic effusion of uncertain etiology
Small to large effusion; usually apparent within days of CABG
Usually left-sided, small to large effusion
Exudative;nonhemorrhagic; lymphocytepredominant
May represent a chronic form of PCIS or persistent pleural injury from CABG
Usually resolves with conservative management
Can progress to trapped lung requiring decortication
Constrictive pericarditis
Occurs months after CABG; dyspnea, edema, jugular venous distention, Kussmaul sign
Bilateral effusions; may have calcified pericardium
Lymphocyte-predominant transudate
Persistent PCIS results in pericardial thickening with cardiac restriction and venous hypertension
Careful diuretic use if mild; if severe, pericardiectomy
Lung entrapment
Small to large effusion; possible dyspnea
Usually left-sided, small to large effusion; may have ipsilateral volume loss
Exudative; nonbloody; lymphocyte predominant; pleural manometry shows biphasic elastance curve
Persistent inflammation results in exudative effusion with pleural restriction
May resolve with conservative management
Can progress to trapped lung requiring decortication
*For PCIS, see Table 2.
Persistent Post-CABG Pleural EffusionTrapped LungClinical Features: Trapped lung is one of the few causes of a persistent, benign effusion that develops following the resolution of an inflammatory process (Table 4). It is an uncommon complication of poorly treated empyema, tuberculous empyema, uremic pleuritis, and rheumatoid pleurisy, and following cardiac surgery.33 A trapped lung should be suspected in a patient with a persistent effusion that reaccumulates rapidly to the same prethoracentesis volume. Radiographic characteristics include a small to moderate pleural effusion without contralateral and sometimes ipsilateral mediastinal shift indicative of a restrictive pleural space.
The incidence of trapped lung after CABG is unknown; however, in the study by Lee and colleagues,17 an analysis of 2 years of follow-up of patients who had undergone CABG revealed eight patients with a persistent pleural effusion who required surgical intervention. Because trapped lung represents an end-stage fibrotic process,33 it usually manifests several months to years after the pleural injury. Thus, trapped lung should be considered when a patient presents with a persistent left-sided pleural effusion in the months to years following CABG.
Pathophysiology: The pathophysiology of trapped lung explains why effusions occur and why the patient may not experience dyspnea. Trapped lung represents the end-stage of dysfunctional healing of the pleura during a severe inflammatory process. In some pathologic states, the mesothelium is incapable of complete self-repair and removal of inflammatory debris. An extracellular neo-matrix develops that serves as a scaffolding for persistent inflammation, fibroblast migration, and dysfunctional pleural repair.34
Assuming that an inflammatory process like PCIS persists without the normal reparative mechanisms, a thick visceral pleural peel can develop over months to years, resulting in restriction of lung expansion. The chest wall is unable to conform to this local geometry, resulting in a persistently negative pressure pleural space. This space fills with fluid in an attempt to normalize the intrapleural pressure. Pleural fluid analysis from the trapped lung effusions will usually be transudative. It is important to note that with a trapped lung, any dyspnea that is present is caused by lung restriction and not the pleural effusion per se. Therefore, thoracentesis is ineffective in alleviating the patient’s dyspnea.33
Diagnosis, Treatment, and Sequelae: The diagnosis of a trapped lung can be confirmed physiologically and with imaging. We routinely perform pleural manometry during therapeutic thoracentesis of any patient with suspected trapped lung. During manometry, intrapleural pressures are monitored as fluid is drained in sequential aliquots.35 The manometric characteristics of a trapped lung are an initial negative intrapleural pressure and a pleural elastance >14.5 cm H20/L (a change in intrapleural pressure of >14.5 cm H20 after removal of 1 L of fluid).36 These patients will have a characteristic elastance curve diagnostic of trapped lung.37,38 When pleural manometry is compatible with trapped lung, we routinely allow air to enter the pleural space to relieve the chest pain induced by fluid removal and perform a CT scan to document pleural thickening as shown in Figure 2 (top). Furthermore, a chest tube placed into the pleural space will not result in complete lung expansion (Fig 2, bottom). An additional characteristic of a trapped lung is rapid recurrence of the effusion after thoracentesis, usually over 48 to 72 h. At thoracoscopy or thoracotomy, the trapped lung will expand completely with decortication if the underlying lung is relatively normal, at least up to 20 years following the initial pleural insult.
Figure 2. Top, CT scan of patient with trapped lung and pneumothorax following thoracentesis. Lines draw attention to the following: (1) On the left side of the image, marked visceral pleural thickening limiting lung expansion to the chest wall, resulting in trapped lung; and (2) on the right side of the image, marked ipsilateral mediastinal shift in the presence of pneumothorax, suggestive of negative intrapleural pressure. Bottom, Chest radiograph of same patient showing trapped lung with characteristic basilar pneumothorax and ipsilateral mediastinal shift. Note absence of lung expansion despite chest tube placement. Lines draw attention to the basilar pneumothorax (top line), the small-bore chest tube (middle), and the absence of ipsilateral mediastinal shift (bottom).
Conclusion
Pleural effusions are common following CABG surgery. The timing of the effusion following CABG suggests the cause and clinical course. Perioperative pleural effusions occurring in the immediate postoperative period (within the first week) are usually caused by diaphragm dysfunction and atelectasis or by IMA harvesting. Management is conservative as these effusions are usually self-limited. Only large, symptomatic effusions require thoracentesis. The early post-CABG pleural effusions that occur within the first month following CABG likely usually arise from PCIS; patients present with chest pain, fever, a left lower lobe infiltrate, and lymphocytic exudates on pleural fluid analysis. If symptoms are severe, corticosteroids are usually effective. When pleural effusions are present within 12 months of CABG (late effusions), they likely represent a variant of PCIS, constrictive pericarditis, or lung entrapment. Persistent, stable pleural effusions in the months to years following CABG surgery are usually caused by trapped lung. If significant pleural restriction is present, dyspnea can be severe, which can only be relieved with decortication. Diagnostic thoracentesis should be performed for patients with large, symptomatic pleural effusions or fever following CABG surgery. Proper diagnosis is critical to the management of these effusions, as management options vary depending on the cause and course of the effusion and may include observation, therapeutic thoracentesis, corticosteroids, or decortication.
References
Light RW. Pleural effusions after coronary artery bypass graft surgery. Curr Opin Pulm Med 2002; 8:308–311
Peng MJ, Vargas FS, Cukier A, et al. Postoperative pleural changes after coronary revascularization: comparison between saphenous vein and internal mammary artery grafting. Chest 1992; 101:327–330
Daganou M, Dimopoulou I, Michalopoulos N, et al. Respiratory complications after coronary artery bypass surgery with unilateral or bilateral internal mammary artery grafting. Chest 1998; 113:1285–1289
Hurlbut D, Myers ML, Lefcoe M, et al. Pleuropulmonary morbidity: internal thoracic artery versus saphenous vein graft. Ann Thorac Surg 1990; 50:959–964
Vargas FS, Uezumi KK, Janete FB, et al. Acute pleuropulmonary complications detected by computed tomography following myocardial revascularization. Rev Hosp Clin Fac Med Sao Paulo 2002; 57:135–142
Fedullo AJ, Lerner RM, Gibson J, et al. Sonographic measurement of diaphragmatic motion after coronary artery bypass surgery. Chest 1992; 102:1683–1686
Benjamin JJ, Cascade PN, Rubenfire M, et al. Left lower lobe atelectasis and consolidation following cardiac surgery: the effect of topical cooling on the phrenic nerve. Radiology 1982; 142:11–14
Nikas DJ, Ramadan FM, Elefteriades JA. Topical hypothermia: ineffective and deleterious as adjunct to cardioplegia for myocardial protection. Ann Thorac Surg 1998; 65:28–31
Hagl C, Harringer W, Gohrbandt B, et al. Site of pleural drain insertion and early postoperative pulmonary function following coronary artery bypass grafting with internal mammary artery. Chest 1999; 115:757–761
Ali IM, Lau P, Kinley CE, et al. Opening the pleura during internal mammary artery harvesting: advantages and disadvantages. Can J Surg 1996; 39:42–45
Bonacchi M, Prifti E, Giunti G, et al. Respiratory dysfunction after coronary artery bypass grafting employing bilateral internal mammary arteries: the influence of intact pleura. Eur J Cardiothorac Surg 2001; 19:827–833
Aarnio P, Kettunen S, Harjula A. Pleural and pulmonary complications after bilateral internal mammary artery grafting. Scand J Thorac Cardiovasc Surg 1991; 25:175–178
Light RW, Rogers JT, Cheng D, et al. Large pleural effusions occurring after coronary artery bypass grafting. Ann Intern Med 1999; 130:891–896
Light RW, Rogers JT, Moyers JP, et al. Prevalence and clinical course of pleural effusions at 30 days after coronary artery and cardiac surgery. Am J Respir Crit Care Med 2002; 166:1567–1571
Sadikot RT, Rogers JT, Cheng DS, et al. Pleural fluid characteristics of patients with symptomatic pleural effusion after coronary artery bypass graft surgery. Arch Intern Med 2000; 160:2665–2668
Niva M, Biancari F, Valkama J, et al. Effects of diclofenac in the prevention of pericardial effusion after coronary artery bypass surgery: a prospective, randomized study. J Cardiovasc Surg (Torino) 2002; 43:449–453
Lee YC, Vaz MA, Ely KA, et al. Symptomatic persistent post-coronary artery bypass graft pleural effusions requiring operative treatment: clinical and histologic features. Chest 2001; 119:795–800
Laine GA, Allen SJ. Left ventricular myocardial edema. Lymph flow, interstitial fibrosis, and cardiac function. Circ Res 1991; 68:1713–1721
Dressler W. The post-myocardial-infarction syndrome: a report on forty-four cases. AMA Arch Intern Med 1959; 103:28–42
Stelzner TJ, King TE Jr, Antony VB, et al. The pleuropulmonary manifestations of the postcardiac injury syndrome. Chest 1983; 84:383–387
Engle MA, McCabe JC, Ebert PA, et al. The postpericardiotomy syndrome and antiheart antibodies. Circulation 1974; 49:401–406
Engle MA. Pericardiotomy and allied syndromes. In: Reddy PS, ed. Pericardial disease. New York, NY: Raven Press, 1982; 313
De Scheerder I, De Buyzere M, Robbrecht J, et al. Postoperative immunological response against contractile proteins after coronary bypass surgery. Br Heart J 1986; 56:440–444
Maisch B, Schuff-Werner P, Berg PA, et al. Clinical significance of immunopathological findings in patients with post-pericardiotomy syndrome. II. The significance of serum inhibition and rosette inhibitory factors. Clin Exp Immunol 1979; 38:198–203
Kaminsky ME, Rodan BA, Osborne DR, et al. Postpericardiotomy syndrome. AJR Am J Roentgenol 1982; 138:503–508
Khan AH. The postcardiac injury syndromes. Clin Cardiol 1992; 15:67–72
Mukherjee D, Nissen SE, Topol EJ. Risk of cardiovascular events associated with selective COX-2 inhibitors. Jama 2001; 286:954–959
Jugdutt B, Basualdo C. Myocardial infarct expansion during indomethacin or ibuprofen for symptomatic post-infarction pericarditis: influence of other pharmacologic agents during early remodeling. Can J Cardiol 1989; 5:211–221
Engle MA, Gay WA Jr, Kaminsky ME, et al. The postpericardiotomy syndrome then and now. Curr Probl Cardiol 1978; 3:1–40
Ofori-Krakye S, Tyberg T, Geha A, et al. Late cardiac tamponade after open heart surgery: incidence, role of anticoagulants in its pathogenesis and its relationship to the postpericardiotomy syndrome. Circulation 1981; 63:1323–1328
Killian DM, Furiasse JG, Scanlon PJ, et al. Constrictive pericarditis after cardiac surgery. Am Heart J 1989; 118:563–568
Kim YK, Mohsenifar Z, Koerner SK. Lymphocytic pleural effusion in postpericardiotomy syndrome. Am Heart J 1988; 115:1077–1079
Doelken P, Sahn SA. Trapped lung. Semin Respir Crit Care Med 2001; 22:631–636
Huggins JT, Sahn SA. Causes and management of pleural fibrosis. Respirology 2004; 9:441–447
Doelken P, Huggins JT, Pastis NJ, et al. Pleural manometry: technique and clinical implications. Chest 2004; 126:1764–1769
Heidecker J, Huggins JT, Sahn SA, et al. Pathophysiology of pneumothorax following ultrasound-guided thoracentesis. Chest 2006; 130:1173–1184
Doelken P, Huggins JT, Pastis NJ, et al. Pleural manometry: technique and clinical implications. Chest 2004; 126:1764–1769
Huggins JT, Sahn SA, Heidecker J, et al. Characteristics of trapped lung: pleural fluid analysis, manometry, and air-contrast chest CT. Chest 2007; 131:206–213 Copyright ©2007 American College of Chest Physicians
