Download PDF
Semin Respir Crit Care Med 2019; 40(03): 361-374
DOI: 10.1055/s-0039-1694699
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Medical and Surgical Management of Empyema

Mark S. Godfrey
1   Pulmonary, Critical Care and Sleep Medicine, Yale New Haven Hospital, New Haven, Connecticut
,
Kyle T. Bramley
1   Pulmonary, Critical Care and Sleep Medicine, Yale New Haven Hospital, New Haven, Connecticut
,
Frank Detterbeck
2   Section of Thoracic Surgery, Yale University School of Medicine, New Haven, Connecticut
› Author Affiliations
Further Information

Publication History

Publication Date:
16 September 2019 (online)

   Permissions and Reprints

Abstract

Infection of the pleural space is an ancient and common clinical problem, the incidence which is on the rise. Advances in therapy now present clinicians of varying disciplines with an array of therapeutic options ranging from thoracentesis and chest tube drainage (with or without intrapleural fibrinolytic therapies) to video-assisted thoracic surgery (VATS) or thoracotomy. A framework is provided to guide decision making, which involves weighing multiple factors (clinical history and presentation, imaging characteristics, comorbidities); multidisciplinary collaboration and active management are needed as the clinical course over a few days determines subsequent refinement. The initial choice of antibiotics depends on whether the empyema is community-acquired or nosocomial, and clinicians must recognize that culture results often do not reflect the full disease process. Antibiotics alone are rarely successful and can be justified only in specific circumstances. Early drainage with or without intrapleural fibrinolytics is usually required. This is successful in most patients; however, when surgical decortication is needed, clear benefit and low physiologic impact are more likely with early intervention, expeditious escalation of interventions, and care at a center experienced with VATS.

Keywords

empyema - pleural infection - tissue plasminogen activator - deoxyribonuclease - thoracoscopy - video-assisted thoracic surgery

Disclosure Statement

The authors have no relationship with a commercial company that has a direct financial interest in subject matter or materials discussed in the article or with a company making a competing product.


 

  • References

  • 1 Tung J, Carter D, Rappold J. Empyema commission of 1918-Impact on acute care surgery 100 years later. J Trauma Acute Care Surg 2019; 86 (02) 321-325
    CrossrefPubMedGoogle Scholar
  • 2 The Empyema Commission. Cases of empyema at Camp Lee, VA: preliminary report. JAMA 1918; 71 (05) 366-373
    CrossrefPubMedGoogle Scholar
  • 3 Light RW. Pleural Diseases. 6th ed. Philadelphia, PA: Wolters Kluwer; 2013
    Google Scholar
  • 4 Scarci M, Abah U, Solli P. , et al. EACTS expert consensus statement for surgical management of pleural empyema. Eur J Cardiothorac Surg 2015; 48 (05) 642-653
    CrossrefPubMedGoogle Scholar
  • 5 Zahid I, Routledge T, Billè A, Scarci M. What is the best treatment of postpneumonectomy empyema?. Interact Cardiovasc Thorac Surg 2011; 12 (02) 260-264
    CrossrefPubMedGoogle Scholar
  • 6 Balfour-Lynn IM, Abrahamson E, Cohen G. , et al. BTS guidelines for the management of pleural infection in children. Thorax 2005; 60 (Suppl. 01) i1-21
    CrossrefPubMedGoogle Scholar
  • 7 Falguera M, Carratalà J, Bielsa S. , et al. Predictive factors, microbiology and outcome of patients with parapneumonic effusion. Eur Respir J 2011; 38 (05) 1173-1179
    CrossrefPubMedGoogle Scholar
  • 8 Chalmers JD, Singanayagam A, Murray MP, Scally C, Fawzi A, Hill AT. Risk factors for complicated parapneumonic effusion and empyema on presentation to hospital with community-acquired pneumonia. Thorax 2009; 64 (07) 592-597
    CrossrefPubMedGoogle Scholar
  • 9 Brims F, Popowicz N, Rosenstengel A. , et al. Bacteriology and clinical outcomes of patients with culture-positive pleural infection in Western Australia: a 6-year analysis. Respirology 2019; 24 (02) 171-178
    PubMedGoogle Scholar
  • 10 Nayak R, Lougheed MD, Brogly S, Lajkosz K, Petsikas D. Thoracic empyema - 20 year trends in management and outcomes in Ontario, Canada. Am J Respir Crit Care Med 2018; 197: A4215
    PubMedGoogle Scholar
  • 11 Finley C, Clifton J, Fitzgerald JM, Yee J. Empyema: an increasing concern in Canada. Can Respir J 2008; 15 (02) 85-89
    CrossrefPubMedGoogle Scholar
  • 12 Søgaard M, Nielsen RB, Nørgaard M, Kornum JB, Schønheyder HC, Thomsen RW. Incidence, length of stay, and prognosis of hospitalized patients with pleural empyema: a 15-year Danish nationwide cohort study. Chest 2014; 145 (01) 189-192
    CrossrefPubMedGoogle Scholar
  • 13 Lehtomäki A, Nevalainen R, Ukkonen M, Nieminen J, Laurikka J, Khan J. Trends in the incidence, etiology, treatment, and outcomes of pleural infections in adults over a decade in a Finnish University hospital. Scand J Surg 2019 (e-pub ahead of print): Doi: 10.1177/1457496919832146
    PubMedGoogle Scholar
  • 14 Farjah F, Symons RG, Krishnadasan B, Wood DE, Flum DR. Management of pleural space infections: a population-based analysis. J Thorac Cardiovasc Surg 2007; 133 (02) 346-351
    CrossrefPubMedGoogle Scholar
  • 15 Grijalva CG, Zhu Y, Nuorti JP, Griffin MR. Emergence of parapneumonic empyema in the USA. Thorax 2011; 66 (08) 663-668
    CrossrefPubMedGoogle Scholar
  • 16 Bender JM, Ampofo K, Sheng X, Pavia AT, Cannon-Albright L, Byington CL. Parapneumonic empyema deaths during past century, Utah. Emerg Infect Dis 2009; 15 (01) 44-48
    CrossrefPubMedGoogle Scholar
  • 17 Semenkovich TR, Olsen MA, Puri V, Meyers BF, Kozower BD. Current state of empyema management. Ann Thorac Surg 2018; 105 (06) 1589-1596
    CrossrefPubMedGoogle Scholar
  • 18 Khan JA, Lehtomäki AI, Toikkanen VJ, Ukkonen MT, Nevalainen RM, Laurikka JO. Long-term prognosis and causes of death after pleural infections. Scand J Surg 2018; 107 (02) 145-151
    CrossrefPubMedGoogle Scholar
  • 19 Rahman NM, Kahan BC, Miller RF, Gleeson FV, Nunn AJ, Maskell NA. A clinical score (RAPID) to identify those at risk for poor outcome at presentation in patients with pleural infection. Chest 2014; 145 (04) 848-855
    CrossrefPubMedGoogle Scholar
  • 20 Mikkola R, Kelahaara J, Heikkinen J, Lahtinen J, Biancari F. Poor late survival after surgical treatment of pleural empyema. World J Surg 2010; 34 (02) 266-271
    CrossrefPubMedGoogle Scholar
  • 21 Schweigert M, Solymosi N, Dubecz A. , et al. Surgery for parapneumonic pleural empyema--what influence does the rising prevalence of multimorbidity and advanced age has on the current outcome?. Surgeon 2016; 14 (02) 69-75
    CrossrefPubMedGoogle Scholar
  • 22 Ahmed RA, Marrie TJ, Huang JQ. Thoracic empyema in patients with community-acquired pneumonia. Am J Med 2006; 119 (10) 877-883
    CrossrefPubMedGoogle Scholar
  • 23 Maskell NA, Davies CWH, Nunn AJ. , et al; First Multicenter Intrapleural Sepsis Trial (MIST1) Group. U.K. controlled trial of intrapleural streptokinase for pleural infection. N Engl J Med 2005; 352 (09) 865-874
    CrossrefPubMedGoogle Scholar
  • 24 Rahman NM, Maskell NA, West A. , et al. Intrapleural use of tissue plasminogen activator and DNase in pleural infection. N Engl J Med 2011; 365 (06) 518-526
    CrossrefPubMedGoogle Scholar
  • 25 Marks DJB, Fisk MD, Koo CY. , et al. Thoracic empyema: a 12-year study from a UK tertiary cardiothoracic referral centre. PLoS One 2012; 7 (01) e30074
    CrossrefPubMedGoogle Scholar
  • 26 Birkenkamp K, O'Horo JC, Kashyap R. , et al. Empyema management: a cohort study evaluating antimicrobial therapy. J Infect 2016; 72 (05) 537-543
    CrossrefPubMedGoogle Scholar
  • 27 Misthos P, Sepsas E, Konstantinou M, Athanassiadi K, Skottis I, Lioulias A. Early use of intrapleural fibrinolytics in the management of postpneumonic empyema. A prospective study. Eur J Cardiothorac Surg 2005; 28 (04) 599-603
    CrossrefPubMedGoogle Scholar
  • 28 Tong BC, Hanna J, Toloza EM. , et al. Outcomes of video-assisted thoracoscopic decortication. Ann Thorac Surg 2010; 89 (01) 220-225
    CrossrefPubMedGoogle Scholar
  • 29 Sullivan KM, O'Toole RD, Fisher RH, Sullivan KN. Anaerobic empyema thoracis. The role of anaerobes in 226 cases of culture-proven empyemas. Arch Intern Med 1973; 131 (04) 521-527
    CrossrefPubMedGoogle Scholar
  • 30 Majid A, Kheir F, Folch A. , et al. Concurrent intrapleural instillation of tissue plasminogen activator and DNase for pleural infection. A single-center experience. Ann Am Thorac Soc 2016; 13 (09) 1512-1518
    CrossrefPubMedGoogle Scholar
  • 31 Park C-K, Oh H-J, Choi H-Y. , et al. Microbiological characteristics and predictive factors for mortality in pleural infection: a single-center cohort study in Korea. PLoS One 2016; 11 (08) e0161280
    CrossrefPubMedGoogle Scholar
  • 32 Alfageme I, Muñoz F, Peña N, Umbría S. Empyema of the thorax in adults. Etiology, microbiologic findings, and management. Chest 1993; 103 (03) 839-843
    CrossrefPubMedGoogle Scholar
  • 33 LeMense GP, Strange C, Sahn SA. Empyema thoracis. Therapeutic management and outcome. Chest 1995; 107 (06) 1532-1537
    CrossrefPubMedGoogle Scholar
  • 34 Burgos J, Lujan M, Falcó V. , et al. The spectrum of pneumococcal empyema in adults in the early 21st century. Clin Infect Dis 2011; 53 (03) 254-261
    CrossrefPubMedGoogle Scholar
  • 35 Davies HE, Davies RJO, Davies CWH. , BTS Pleural Disease Guideline Group. Management of pleural infection in adults: British Thoracic Society Pleural Disease Guideline 2010. Thorax 2010; 65 (Suppl. 02) ii41-ii53
    PubMedGoogle Scholar
  • 36 Shen KR, Bribriesco A, Crabtree T. , et al. The American Association for Thoracic Surgery consensus guidelines for the management of empyema. J Thorac Cardiovasc Surg 2017; 153 (06) e129-e146
    CrossrefPubMedGoogle Scholar
  • 37 El Solh AA, Alhajjhasan A, Ramadan FH, Pineda LA. A comparative study of community- and nursing home-acquired empyema thoracis. J Am Geriatr Soc 2007; 55 (11) 1847-1852
    CrossrefPubMedGoogle Scholar
  • 38 Light RW. Parapneumonic effusions and empyema. Proc Am Thorac Soc 2006; 3 (01) 75-80
    CrossrefPubMedGoogle Scholar
  • 39 Colice GL, Curtis A, Deslauriers J. , et al. Medical and surgical treatment of parapneumonic effusions : an evidence-based guideline. Chest 2000; 118 (04) 1158-1171
    CrossrefPubMedGoogle Scholar
  • 40 Light RW. A new classification of parapneumonic effusions and empyema. Chest 1995; 108 (02) 299-301
    CrossrefPubMedGoogle Scholar
  • 41 Rahman NM, Mishra EK, Davies HE, Davies RJO, Lee YCG. Clinically important factors influencing the diagnostic measurement of pleural fluid pH and glucose. Am J Respir Crit Care Med 2008; 178 (05) 483-490
    CrossrefPubMedGoogle Scholar
  • 42 Maskell NA, Gleeson FV, Darby M, Davies RJO. Diagnostically significant variations in pleural fluid pH in loculated parapneumonic effusions. Chest 2004; 126 (06) 2022-2024
    CrossrefPubMedGoogle Scholar
  • 43 Pine JR, Hollman JL. Elevated pleural fluid pH in Proteus mirabilis empyema. Chest 1983; 84 (01) 109-111
    CrossrefPubMedGoogle Scholar
  • 44 Andrews N, Parker E, Shaw R, Wilson N, Webb W. Management of nontuberculous empyema: a statement of the subcommittee on surgery. Am Rev Respir Dis 1962; 85: 935-936
    PubMedGoogle Scholar
  • 45 Heffner JE, McDonald J, Barbieri C, Klein J. Management of parapneumonic effusions. An analysis of physician practice patterns. Arch Surg 1995; 130 (04) 433-438
    CrossrefPubMedGoogle Scholar
  • 46 Ashbaugh DG. Empyema thoracis. Factors influencing morbidity and mortality. Chest 1991; 99 (05) 1162-1165
    CrossrefPubMedGoogle Scholar
  • 47 Sasse S, Nguyen TK, Mulligan M, Wang NS, Mahutte CK, Light RW. The effects of early chest tube placement on empyema resolution. Chest 1997; 111 (06) 1679-1683
    CrossrefPubMedGoogle Scholar
  • 48 Sasse SA, Causing LA, Mulligan ME, Light RW. Serial pleural fluid analysis in a new experimental model of empyema. Chest 1996; 109 (04) 1043-1048
    CrossrefPubMedGoogle Scholar
  • 49 Luh S-P, Chou M-C, Wang L-S, Chen J-Y, Tsai T-P. Video-assisted thoracoscopic surgery in the treatment of complicated parapneumonic effusions or empyemas: outcome of 234 patients. Chest 2005; 127 (04) 1427-1432
    PubMedGoogle Scholar
  • 50 Waller DA, Rengarajan A, Nicholson FHG, Rajesh PB. Delayed referral reduces the success of video-assisted thoracoscopic debridement for post-pneumonic empyema. Respir Med 2001; 95 (10) 836-840
    CrossrefPubMedGoogle Scholar
  • 51 Lardinois D, Gock M, Pezzetta E. , et al. Delayed referral and gram-negative organisms increase the conversion thoracotomy rate in patients undergoing video-assisted thoracoscopic surgery for empyema. Ann Thorac Surg 2005; 79 (06) 1851-1856
    CrossrefPubMedGoogle Scholar
  • 52 Stefani A, Aramini B, della Casa G. , et al. Preoperative predictors of successful surgical treatment in the management of parapneumonic empyema. Ann Thorac Surg 2013; 96 (05) 1812-1819
    CrossrefPubMedGoogle Scholar
  • 53 Jagelavicius Z, Jovaisas V, Mataciunas M, Samalavicius NE, Janilionis R. Preoperative predictors of conversion in thoracoscopic surgery for pleural empyema. Eur J Cardiothorac Surg 2017; 52 (01) 70-75
    CrossrefPubMedGoogle Scholar
  • 54 Kim B-Y, Oh B-S, Jang W-C, Min Y-I, Park Y-K, Park J-C. Video-assisted thoracoscopic decortication for management of postpneumonic pleural empyema. Am J Surg 2004; 188 (03) 321-324
    CrossrefPubMedGoogle Scholar
  • 55 Waller DA, Rengarajan A. Thoracoscopic decortication: a role for video-assisted surgery in chronic postpneumonic pleural empyema. Ann Thorac Surg 2001; 71 (06) 1813-1816
    CrossrefPubMedGoogle Scholar
  • 56 Lawrence DR, Ohri SK, Moxon RE, Townsend ER, Fountain SW. Thoracoscopic debridement of empyema thoracis. Ann Thorac Surg 1997; 64 (05) 1448-1450
    CrossrefPubMedGoogle Scholar
  • 57 Chung JH, Lee SH, Kim KT, Jung JS, Son HS, Sun K. Optimal timing of thoracoscopic drainage and decortication for empyema. Ann Thorac Surg 2014; 97 (01) 224-229
    CrossrefPubMedGoogle Scholar
  • 58 Moulton JS, Benkert RE, Weisiger KH, Chambers JA. Treatment of complicated pleural fluid collections with image-guided drainage and intracavitary urokinase. Chest 1995; 108 (05) 1252-1259
    CrossrefPubMedGoogle Scholar
  • 59 Levinson GM, Pennington DW. Intrapleural fibrinolytics combined with image-guided chest tube drainage for pleural infection. Mayo Clin Proc 2007; 82 (04) 407-413
    CrossrefPubMedGoogle Scholar
  • 60 Davies CW, Kearney SE, Gleeson FV, Davies RJ. Predictors of outcome and long-term survival in patients with pleural infection. Am J Respir Crit Care Med 1999; 160 (5, Pt 1): 1682-1687
    CrossrefPubMedGoogle Scholar
  • 61 Maskell NA, Batt S, Hedley EL, Davies CWH, Gillespie SH, Davies RJO. The bacteriology of pleural infection by genetic and standard methods and its mortality significance. Am J Respir Crit Care Med 2006; 174 (07) 817-823
    CrossrefPubMedGoogle Scholar
  • 62 Mandal AK, Thadepalli H, Mandal AK, Chettipally U. Outcome of primary empyema thoracis: therapeutic and microbiologic aspects. Ann Thorac Surg 1998; 66 (05) 1782-1786
    CrossrefPubMedGoogle Scholar
  • 63 Ferrer A, Osset J, Alegre J. , et al. Prospective clinical and microbiological study of pleural effusions. Eur J Clin Microbiol Infect Dis 1999; 18 (04) 237-241
    CrossrefPubMedGoogle Scholar
  • 64 Koma Y, Inoue S, Oda N. , et al. Clinical characteristics and outcomes of patients with community-acquired, health-care-associated and hospital-acquired empyema. Clin Respir J 2017; 11 (06) 781-788
    CrossrefPubMedGoogle Scholar
  • 65 Lin YC, Chen HJ, Liu YH, Shih C-M, Hsu W-H, Tu C-Y. A 30-month experience of thoracic empyema in a tertiary hospital: emphasis on differing bacteriology and outcome between the medical intensive care unit (MICU) and medical ward. South Med J 2008; 101 (05) 484-489
    CrossrefPubMedGoogle Scholar
  • 66 Tu C-Y, Hsu W-H, Hsia T-C. , et al. The changing pathogens of complicated parapneumonic effusions or empyemas in a medical intensive care unit. Intensive Care Med 2006; 32 (04) 570-576
    CrossrefPubMedGoogle Scholar
  • 67 Menzies SM, Rahman NM, Wrightson JM. , et al. Blood culture bottle culture of pleural fluid in pleural infection. Thorax 2011; 66 (08) 658-662
    CrossrefPubMedGoogle Scholar
  • 68 Insa R, Marín M, Martín A. , et al. Systematic use of universal 16S rRNA gene polymerase chain reaction (PCR) and sequencing for processing pleural effusions improves conventional culture techniques. Medicine (Baltimore) 2012; 91 (02) 103-110
    PubMedGoogle Scholar
  • 69 Kawanami T, Fukuda K, Yatera K, Kido M, Mukae H, Taniguchi H. A higher significance of anaerobes: the clone library analysis of bacterial pleurisy. Chest 2011; 139 (03) 600-608
    CrossrefPubMedGoogle Scholar
  • 70 Psallidas I, Kanellakis NI, Bhatnagar R. , et al. A pilot feasibility study in establishing the role of ultrasound-guided pleural biopsies in pleural infection (the AUDIO study). Chest 2018; 154 (04) 766-772
    CrossrefPubMedGoogle Scholar
  • 71 Meyer CN, Rosenlund S, Nielsen J, Friis-Møller A. Bacteriological aetiology and antimicrobial treatment of pleural empyema. Scand J Infect Dis 2011; 43 (03) 165-169
    CrossrefPubMedGoogle Scholar
  • 72 Lindstrom ST, Kolbe J. Community acquired parapneumonic thoracic empyema: predictors of outcome. Respirology 1999; 4 (02) 173-179
    CrossrefPubMedGoogle Scholar
  • 73 Micek ST, Dunne M, Kollef MH. Pleuropulmonary complications of Panton-Valentine leukocidin-positive community-acquired methicillin-resistant Staphylococcus aureus: importance of treatment with antimicrobials inhibiting exotoxin production. Chest 2005; 128 (04) 2732-2738
    CrossrefPubMedGoogle Scholar
  • 74 Bartlett JG, Gorbach SL, Thadepalli H, Finegold SM. Bacteriology of empyema. Lancet 1974; 1 (7853): 338-340
    PubMedGoogle Scholar
  • 75 Boyanova L, Djambazov V, Gergova G. , et al. Anaerobic microbiology in 198 cases of pleural empyema: a Bulgarian study. Anaerobe 2004; 10 (05) 261-267
    CrossrefPubMedGoogle Scholar
  • 76 Brook I, Frazier EH. Aerobic and anaerobic microbiology of empyema. A retrospective review in two military hospitals. Chest 1993; 103 (05) 1502-1507
    CrossrefPubMedGoogle Scholar
  • 77 Civen R, Jousimies-Somer H, Marina M, Borenstein L, Shah H, Finegold SM. A retrospective review of cases of anaerobic empyema and update of bacteriology. Clin Infect Dis 1995; 20 (Suppl. 02) S224-S229
    CrossrefPubMedGoogle Scholar
  • 78 Shinzato T, Saito A. A mechanism of pathogenicity of “Streptococcus milleri group” in pulmonary infection: synergy with an anaerobe. J Med Microbiol 1994; 40 (02) 118-123
    CrossrefPubMedGoogle Scholar
  • 79 Dyrhovden R, Nygaard RM, Patel R, Ulvestad E, Kommedal Ø. The bacterial aetiology of pleural empyema. A descriptive and comparative metagenomic study. Clin Microbiol Infect 2019; 25 (08) 981-986
    CrossrefPubMedGoogle Scholar
  • 80 Chen KY, Hsueh PR, Liaw YS, Yang PC, Luh KT. A 10-year experience with bacteriology of acute thoracic empyema: emphasis on Klebsiella pneumoniae in patients with diabetes mellitus. Chest 2000; 117 (06) 1685-1689
    CrossrefPubMedGoogle Scholar
  • 81 Bartlett JG, Finegold SM. Anaerobic infections of the lung and pleural space. Am Rev Respir Dis 1974; 110 (01) 56-77
    PubMedGoogle Scholar
  • 82 Landay MJ, Christensen EE, Bynum LJ, Goodman C. Anaerobic pleural and pulmonary infections. AJR Am J Roentgenol 1980; 134 (02) 233-240
    CrossrefPubMedGoogle Scholar
  • 83 Popowicz ND, Lansley SM, Cheah HM. , et al. Human pleural fluid is a potent growth medium for Streptococcus pneumoniae. PLoS One 2017; 12 (11) e0188833
    CrossrefPubMedGoogle Scholar
  • 84 Okiror L, Coltart C, Bille A. , et al. Thoracotomy and decortication: impact of culture-positive empyema on the outcome of surgery. Eur J Cardiothorac Surg 2014; 46 (05) 901-906
    CrossrefPubMedGoogle Scholar
  • 85 Brutsche MH, Tassi G-F, Györik S. , et al. Treatment of sonographically stratified multiloculated thoracic empyema by medical thoracoscopy. Chest 2005; 128 (05) 3303-3309
    CrossrefPubMedGoogle Scholar
  • 86 Nielsen J, Meyer CN, Rosenlund S. Outcome and clinical characteristics in pleural empyema: a retrospective study. Scand J Infect Dis 2011; 43 (6–7): 430-435
    CrossrefPubMedGoogle Scholar
  • 87 White HD, Henry C, Stock EM, Arroliga AC, Ghamande S. Predicting long-term outcomes in pleural infections. RAPID score for risk stratification. Ann Am Thorac Soc 2015; 12 (09) 1310-1316
    CrossrefPubMedGoogle Scholar
  • 88 Meyer CN, Armbruster K, Kemp M, Thomsen TR, Dessau RB. ; Danish Pleural Empyema group. Pleural infection: a retrospective study of clinical outcome and the correlation to known etiology, co-morbidity and treatment factors. BMC Pulm Med 2018; 18 (01) 160
    CrossrefPubMedGoogle Scholar
  • 89 Khemasuwan D, Sorensen J, Griffin DC. Predictive variables for failure in administration of intrapleural tissue plasminogen activator/deoxyribonuclease in patients with complicated parapneumonic effusions/empyema. Chest 2018; 154 (03) 550-556
    CrossrefPubMedGoogle Scholar
  • 90 Rashwan R, Varano Della Vergiliana JF, Lansley SM. , et al. Streptococcus pneumoniae potently induces cell death in mesothelial cells. PLoS One 2018; 13 (07) e0201530
    CrossrefPubMedGoogle Scholar
  • 91 Lee K-L, Chen W-L, Chen R-J, Lai KS, Chung C-L. Lipoteichoic acid upregulates plasminogen activator inhibitor-1 expression in parapneumonic effusions. Respirology 2018; 23 (01) 89-95
    PubMedGoogle Scholar
  • 92 Keeling AN, Leong S, Logan PM, Lee MJ. Empyema and effusion: outcome of image-guided small-bore catheter drainage. Cardiovasc Intervent Radiol 2008; 31 (01) 135-141
    PubMedGoogle Scholar
  • 93 Shankar S, Gulati M, Kang M, Gupta S, Suri S. Image-guided percutaneous drainage of thoracic empyema: can sonography predict the outcome?. Eur Radiol 2000; 10 (03) 495-499
    CrossrefPubMedGoogle Scholar
  • 94 Rahman NM, Maskell NA, Davies CWH. , et al. The relationship between chest tube size and clinical outcome in pleural infection. Chest 2010; 137 (03) 536-543
    CrossrefPubMedGoogle Scholar
  • 95 Cafarotti S, Dall'Armi V, Cusumano G. , et al. Small-bore wire-guided chest drains: safety, tolerability, and effectiveness in pneumothorax, malignant effusions, and pleural empyema. J Thorac Cardiovasc Surg 2011; 141 (03) 683-687
    CrossrefPubMedGoogle Scholar
  • 96 Janda S, Swiston J. Intrapleural fibrinolytic therapy for treatment of adult parapneumonic effusions and empyemas: a systematic review and meta-analysis. Chest 2012; 142 (02) 401-411
    CrossrefPubMedGoogle Scholar
  • 97 Nie W, Liu Y, Ye J. , et al. Efficacy of intrapleural instillation of fibrinolytics for treating pleural empyema and parapneumonic effusion: a meta-analysis of randomized control trials. Clin Respir J 2014; 8 (03) 281-291
    CrossrefPubMedGoogle Scholar
  • 98 Komissarov AA, Florova G, Azghani AO. , et al. Dose dependency of outcomes of intrapleural fibrinolytic therapy in new rabbit empyema models. Am J Physiol Lung Cell Mol Physiol 2016; 311 (02) L389-L399
    CrossrefPubMedGoogle Scholar
  • 99 Light RW, Nguyen T, Mulligan ME, Sasse SA. The in vitro efficacy of varidase versus streptokinase or urokinase for liquefying thick purulent exudative material from loculated empyema. Hai 2000; 178 (01) 13-18
    PubMedGoogle Scholar
  • 100 Zhu Z, Hawthorne ML, Guo Y. , et al. Tissue plasminogen activator combined with human recombinant deoxyribonuclease is effective therapy for empyema in a rabbit model. Chest 2006; 129 (06) 1577-1583
    CrossrefPubMedGoogle Scholar
  • 101 Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS. Extracellular DNA required for bacterial biofilm formation. Science 2002; 295 (5559): 1487
    CrossrefPubMedGoogle Scholar
  • 102 Komissarov AA, Florova G, Idell S. Effects of extracellular DNA on plasminogen activation and fibrinolysis. J Biol Chem 2011; 286 (49) 41949-41962
    CrossrefPubMedGoogle Scholar
  • 103 Skeete DA, Rutherford EJ, Schlidt SA, Abrams JE, Parker LA, Rich PB. Intrapleural tissue plasminogen activator for complicated pleural effusions. J Trauma 2004; 57 (06) 1178-1183
    CrossrefPubMedGoogle Scholar
  • 104 Thommi G, Nair CK, Aronow WS, Shehan C, Meyers P, McLeay M. Efficacy and safety of intrapleural instillation of alteplase in the management of complicated pleural effusion or empyema. Am J Ther 2007; 14 (04) 341-345
    CrossrefPubMedGoogle Scholar
  • 105 Gervais DA, Levis DA, Hahn PF, Uppot RN, Arellano RS, Mueller PR. Adjunctive intrapleural tissue plasminogen activator administered via chest tubes placed with imaging guidance: effectiveness and risk for hemorrhage. Radiology 2008; 246 (03) 956-963
    CrossrefPubMedGoogle Scholar
  • 106 Froudarakis ME, Kouliatsis G, Steiropoulos P. , et al. Recombinant tissue plasminogen activator in the treatment of pleural infections in adults. Respir Med 2008; 102 (12) 1694-1700
    CrossrefPubMedGoogle Scholar
  • 107 Thommi G, Shehan JC, Robison KL, Christensen M, Backemeyer LA, McLeay MT. A double blind randomized cross over trial comparing rate of decortication and efficacy of intrapleural instillation of alteplase vs placebo in patients with empyemas and complicated parapneumonic effusions. Respir Med 2012; 106 (05) 716-723
    CrossrefPubMedGoogle Scholar
  • 108 Luengo-Fernandez R, Penz E, Dobson M. , et al. Cost-effectiveness of intrapleural use of tissue plasminogen activator and DNase in pleural infection: evidence from the MIST2 randomised controlled trial. Eur Respir J 2019 (e-pub ahead of print). Doi: 10.1183/13993003.01550-2018
    PubMedGoogle Scholar
  • 109 Hooper CE, Edey AJ, Wallis A. , et al. Pleural irrigation trial (PIT): a randomised controlled trial of pleural irrigation with normal saline versus standard care in patients with pleural infection. Eur Respir J 2015; 46 (02) 456-463
    CrossrefPubMedGoogle Scholar
  • 110 Heimes J, Copeland H, Lulla A. , et al. The use of thrombolytics in the management of complex pleural fluid collections. J Thorac Dis 2017; 9 (05) 1310-1316
    CrossrefPubMedGoogle Scholar
  • 111 Popowicz N, Bintcliffe O, De Fonseka D. , et al. Dose de-escalation of intrapleural tissue plasminogen activator therapy for pleural infection. The alteplase dose assessment for pleural infection therapy project. Ann Am Thorac Soc 2017; 14 (06) 929-936
    CrossrefPubMedGoogle Scholar
  • 112 Fysh ETH, Tremblay A, Feller-Kopman D. , et al. Clinical outcomes of indwelling pleural catheter-related pleural infections: an international multicenter study. Chest 2013; 144 (05) 1597-1602
    CrossrefPubMedGoogle Scholar
  • 113 Komissarov AA, Rahman N, Lee YCG. , et al. Fibrin turnover and pleural organization: bench to bedside. Am J Physiol Lung Cell Mol Physiol 2018; 314 (05) L757-L768
    CrossrefPubMedGoogle Scholar
  • 114 Florova G, Azghani A, Karandashova S. , et al. Targeting of plasminogen activator inhibitor 1 improves fibrinolytic therapy for tetracycline-induced pleural injury in rabbits. Am J Respir Cell Mol Biol 2015; 52 (04) 429-437
    CrossrefPubMedGoogle Scholar
  • 115 Philip-Joët F, Alessi MC, Philip-Joët C. , et al. Fibrinolytic and inflammatory processes in pleural effusions. Eur Respir J 1995; 8 (08) 1352-1356
    CrossrefPubMedGoogle Scholar
  • 116 Lin F-C, Chen Y-C, Chen F-J, Chang S-C. Cytokines and fibrinolytic enzymes in tuberculous and parapneumonic effusions. Clin Immunol 2005; 116 (02) 166-173
    CrossrefPubMedGoogle Scholar
  • 117 Idell S, Florova G, Shetty S. , et al. Precision-guided, personalized intrapleural fibrinolytic therapy for empyema and complicated parapneumonic pleural effusions: the case for the fibrinolytic potential. Clin Pulm Med 2017; 24 (04) 163-169
    CrossrefPubMedGoogle Scholar
  • 118 Beckert L, Brockway B, Simpson G. , et al. Phase 1 trial of intrapleural LTI-01; single chain urokinase in complicated parapneumonic effusions or empyema. JCI Insight 2019; 5: 127470
    PubMedGoogle Scholar
  • 119 McClune JR, Wilshire CL, Gorden JA. , et al. Safety and efficacy of intrapleural tissue plasminogen activator and DNase during extended use in complicated pleural space infections. Can Respir J 2016; 2016: 9796768
    CrossrefPubMedGoogle Scholar
  • 120 Kheir F, Cheng G, Rivera E. , et al. Concurrent versus sequential intrapleural instillation of tissue plasminogen activator and deoxyribonuclease for pleural infection. J Bronchology Interv Pulmonol 2018; 25 (02) 125-131
    CrossrefPubMedGoogle Scholar
  • 121 Bishwakarma R, Shah S, Frank L, Zhang W, Sharma G, Nishi SPE. Mixing it up: coadministration of tPA/DNase in complicated parapneumonic pleural effusions and empyema. J Bronchology Interv Pulmonol 2017; 24 (01) 40-47
    CrossrefPubMedGoogle Scholar
  • 122 Komissarov AA, Florova G, Azghani AO. , et al. The time course of resolution of adhesions during fibrinolytic therapy in tetracycline-induced pleural injury in rabbits. Am J Physiol Lung Cell Mol Physiol 2015; 309 (06) L562-L572
    CrossrefPubMedGoogle Scholar
  • 123 Piccolo F, Popowicz N, Wong D, Lee YCG. Intrapleural tissue plasminogen activator and deoxyribonuclease therapy for pleural infection. J Thorac Dis 2015; 7 (06) 999-1008
    PubMedGoogle Scholar
  • 124 Davies CW, Lok S, Davies RJO. The systemic fibrinolytic activity of intrapleural streptokinase. Am J Respir Crit Care Med 1998; 157 (01) 328-330
    CrossrefPubMedGoogle Scholar
  • 125 Berglin E, Ekroth R, Teger-Nilsson AC, William-Olsson G. Intrapleural instillation of streptokinase. Effects on systemic fibrinolysis. Thorac Cardiovasc Surg 1981; 29 (02) 124-126
    Article in Thieme ConnectPubMedGoogle Scholar
  • 126 Mehta HJ, Biswas A, Penley AM, Cope J, Barnes M, Jantz MA. Management of intrapleural sepsis with once daily use of tissue plasminogen activator and deoxyribonuclease. Respiration 2016; 91 (02) 101-106
    CrossrefPubMedGoogle Scholar
  • 127 Piccolo F, Pitman N, Bhatnagar R. , et al. Intrapleural tissue plasminogen activator and deoxyribonuclease for pleural infection. An effective and safe alternative to surgery. Ann Am Thorac Soc 2014; 11 (09) 1419-1425
    CrossrefPubMedGoogle Scholar
  • 128 Alemán C, Porcel JM, Alegre J. , et al. Intrapleural fibrinolysis with urokinase versus alteplase in complicated parapneumonic pleural effusions and empyemas: a prospective randomized study. Hai 2015; 193 (06) 993-1000
    PubMedGoogle Scholar
  • 129 Godfrey MS, Puchalski J. Nondraining indwelling pleural catheters in malignant pleural effusion: how safe is fibrinolysis in patients at high risk of bleeding?. Am J Respir Crit Care Med 2019; 199: A1256
    PubMedGoogle Scholar
  • 130 Ravaglia C, Gurioli C, Tomassetti S. , et al. Is medical thoracoscopy efficient in the management of multiloculated and organized thoracic empyema?. Respiration 2012; 84 (03) 219-224
    CrossrefPubMedGoogle Scholar
  • 131 Solèr M, Wyser C, Bolliger CT, Perruchoud AP. Treatment of early parapneumonic empyema by “medical” thoracoscopy. Schweiz Med Wochenschr 1997; 127 (42) 1748-1753
    PubMedGoogle Scholar
  • 132 Wait MA, Sharma S, Hohn J, Dal Nogare A. A randomized trial of empyema therapy. Chest 1997; 111 (06) 1548-1551
    CrossrefPubMedGoogle Scholar
  • 133 Bilgin M, Akcali Y, Oguzkaya F. Benefits of early aggressive management of empyema thoracis. ANZ J Surg 2006; 76 (03) 120-122
    CrossrefPubMedGoogle Scholar
  • 134 Feller-Kopman D, Light R. Pleural disease. N Engl J Med 2018; 378 (08) 740-751
    CrossrefPubMedGoogle Scholar
  • 135 Corcoran JP, Wrightson JM, Belcher E, DeCamp MM, Feller-Kopman D, Rahman NM. Pleural infection: past, present, and future directions. Lancet Respir Med 2015; 3 (07) 563-577
    CrossrefPubMedGoogle Scholar
  • 136 Corcoran JP, Rahman NM. Effusions from infections: parapneumonic pleural effusion and empyema. In: Light RW, Lee YCG. , eds. Textbook of Pleural Diseases. 3rd ed. Boca Raton, FL: CRC Press; 2016: 295-330
    Google Scholar
  • 137 Reichert M, Hecker M, Witte B. , et al. Stage-directed therapy of pleural empyema. Langenbecks Arch Surg 2017; 402 (01) 15-26
    CrossrefPubMedGoogle Scholar
  • 138 Ferrufino E, Mejía C, Ortiz de la Tabla V, Chiner E. Empyema caused by Legionella pneumophila. Arch Bronconeumol 2012; 48 (03) 102-103
    PubMedGoogle Scholar
  • 139 Winn Jr WC, Myerowitz RL. The pathology of the Legionella pneumonias. A review of 74 cases and the literature. Hum Pathol 1981; 12 (05) 401-422
    CrossrefPubMedGoogle Scholar
  • 140 Sahn SA, Light RW. The sun should never set on a parapneumonic effusion. Chest 1989; 95 (05) 945-947
    CrossrefPubMedGoogle Scholar
  • 141 Akhan O, Ozkan O, Akinci D, Hassan A, Ozmen M. Image-guided catheter drainage of infected pleural effusions. Diagn Interv Radiol 2007; 13 (04) 204-209
    PubMedGoogle Scholar
  • 142 Kearney SE, Davies CW, Davies RJO, Gleeson FV. Computed tomography and ultrasound in parapneumonic effusions and empyema. Clin Radiol 2000; 55 (07) 542-547
    CrossrefPubMedGoogle Scholar
  • 143 Schweigert M, Solymosi N, Dubecz A. , et al. Surgical management of pleural empyema in the very elderly. Ann R Coll Surg Engl 2012; 94 (05) 331-335
    PubMedGoogle Scholar
  • 144 Neff CC, vanSonnenberg E, Lawson DW, Patton AS. CT follow-up of empyemas: pleural peels resolve after percutaneous catheter drainage. Radiology 1990; 176 (01) 195-197
    CrossrefPubMedGoogle Scholar
  • 145 Kho P, Karunanantham J, Leung M, Lim E. Debridement alone without decortication can achieve lung re-expansion in patients with empyema: an observational study. Interact Cardiovasc Thorac Surg 2011; 12 (05) 724-727
    CrossrefPubMedGoogle Scholar
  • 146 Striffeler H, Gugger M, Im Hof V, Cerny A, Furrer M, Ris HB. Video-assisted thoracoscopic surgery for fibrinopurulent pleural empyema in 67 patients. Ann Thorac Surg 1998; 65 (02) 319-323
    CrossrefPubMedGoogle Scholar
  • 147 Angelillo-Mackinlay T, Lyons GA, Piedras MB, Angelillo-Mackinlay D. Surgical treatment of postpneumonic empyema. World J Surg 1999; 23 (11) 1110-1113
    CrossrefPubMedGoogle Scholar
  • 148 Cassina PC, Hauser M, Hillejan L, Greschuchna D, Stamatis G. Video-assisted thoracoscopy in the treatment of pleural empyema: stage-based management and outcome. J Thorac Cardiovasc Surg 1999; 117 (02) 234-238
    CrossrefPubMedGoogle Scholar
  • 149 Roberts JR. Minimally invasive surgery in the treatment of empyema: intraoperative decision making. Ann Thorac Surg 2003; 76 (01) 225-230 , discussion 229–230
    CrossrefPubMedGoogle Scholar
  • 150 Solaini L, Prusciano F, Bagioni P. Video-assisted thoracic surgery in the treatment of pleural empyema. Surg Endosc 2007; 21 (02) 280-284
    CrossrefPubMedGoogle Scholar
  • 151 Cardillo G, Carleo F, Carbone L. , et al. Chronic postpneumonic pleural empyema: comparative merits of thoracoscopic versus open decortication. Eur J Cardiothorac Surg 2009; 36 (05) 914-918
    CrossrefPubMedGoogle Scholar
  • 152 Reichert M, Pösentrup B, Hecker A. , et al. Thoracotomy versus video-assisted thoracoscopic surgery (VATS) in stage III empyema-an analysis of 217 consecutive patients. Surg Endosc 2018; 32 (06) 2664-2675
    CrossrefPubMedGoogle Scholar