Expert Review on Nonsurgical Management of Parapneumonic Effusion: Advances, Controversies, and New Directions

 

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Abstract

Parapneumonic effusion and empyema are rising in incidence worldwide, particularly in association with comorbidities in an aging population. Also driving this change is the widespread uptake of pneumococcal vaccines, leading to the emergence of nonvaccine-type pneumococci and other bacteria. Early treatment with systemic antibiotics is essential but should be guided by local microbial guidelines and antimicrobial resistance patterns due to significant geographical variation. Thoracic ultrasound has emerged as a leading imaging technique in parapneumonic effusion, enabling physicians to characterize effusions, assess the underlying parenchyma, and safely guide pleural procedures. Drainage decisions remain based on longstanding criteria including the size of the effusion and fluid gram stain and biochemistry results. Small-bore chest drains appear to be as effective as large bore and are adequate for the delivery of intrapleural enzyme therapy (IET), which is now supported by a large body of evidence. The IET dosing regimen used in the UK Multicenter Sepsis Trial -2 has the most evidence available but data surrounding alternative dosing, concurrent and once-daily instillations, and novel fibrinolytic agents are promising. Prognostic scores used in pneumonia (e.g., CURB-65) tend to underestimate mortality in parapneumonic effusion/empyema. Scores specifically based on pleural infection have been developed but require validation in prospective cohorts.

Publication History

Article published online:
10 July 2023

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• References

• 1 Grijalva CG, Zhu Y, Nuorti JP, Griffin MR. Emergence of parapneumonic empyema in the USA. Thorax 2011; 66 (08) 663-668
  CrossrefPubMedGoogle Scholar
• 2 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
• 3 Corcoran JP, Psallidas I, Gerry S. et al. Prospective validation of the RAPID clinical risk prediction score in adult patients with pleural infection: the PILOT study. Eur Respir J 2020; 56 (05) 2000130
  CrossrefPubMedGoogle Scholar
• 4 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
  CrossrefPubMedGoogle Scholar
• 5 Cargill TN, Hassan M, Corcoran JP. et al. A systematic review of comorbidities and outcomes of adult patients with pleural infection. Eur Respir J 2019; 54 (03) 54
  CrossrefPubMedGoogle Scholar
• 6 Shipe ME, Maiga AW, Deppen SA. et al. Cost-effectiveness analysis of fibrinolysis vs thoracoscopic decortication for early empyema. Ann Thorac Surg 2021; 112 (05) 1632-1638
  CrossrefPubMedGoogle Scholar
• 7 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
• 8 Li ST, Tancredi DJ. Empyema hospitalizations increased in US children despite pneumococcal conjugate vaccine. Pediatrics 2010; 125 (01) 26-33
  CrossrefPubMedGoogle Scholar
• 9 Goldbart AD, Leibovitz E, Porat N. et al. Complicated community acquired pneumonia in children prior to the introduction of the pneumococcal conjugated vaccine. Scand J Infect Dis 2009; 41 (03) 182-187
  CrossrefPubMedGoogle Scholar
• 10 Wu PS, Huang LM, Chang IS. et al. The epidemiology of hospitalized children with pneumococcal/lobar pneumonia and empyema from 1997 to 2004 in Taiwan. Eur J Pediatr 2010; 169 (07) 861-866
  CrossrefPubMedGoogle Scholar
• 11 Mahon C, Walker W, Drage A, Best E. Incidence, aetiology and outcome of pleural empyema and parapneumonic effusion from 1998 to 2012 in a population of New Zealand children. J Paediatr Child Health 2016; 52 (06) 662-668
  CrossrefPubMedGoogle Scholar
• 12 Finley C, Clifton J, Fitzgerald JM, Yee J. Empyema: an increasing concern in Canada. Can Respir J 2008; 15 (02) 85-89
  CrossrefPubMedGoogle Scholar
• 13 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
• 14 Bobbio A, Bouam S, Frenkiel J. et al. Epidemiology and prognostic factors of pleural empyema. Thorax 2021; 76 (11) 1117-1123
  CrossrefPubMedGoogle Scholar
• 15 Arnold DT, Hamilton FW, Morris TT. et al. Epidemiology of pleural empyema in English hospitals and the impact of influenza. Eur Respir J 2021; 57 (06) 57
  CrossrefPubMedGoogle Scholar
• 16 Mummadi SR, Stoller JK, Lopez R, Kailasam K, Gillespie CT, Hahn PY. Epidemiology of adult pleural disease in the United States. Chest 2021; 160 (04) 1534-1551
  CrossrefPubMedGoogle Scholar
• 17 Lu HY, Liao KM. Risk of empyema in patients with COPD. Int J Chron Obstruct Pulmon Dis 2018; 13: 317-324
  CrossrefPubMedGoogle Scholar
• 18 Shen TC, Chen CH, Wang IK. et al. Risk of empyema in patients with end-stage renal disease: a nationwide propensity-matched cohort study. QJM 2017; 110 (07) 425-430
  PubMedGoogle Scholar
• 19 Shen TC, Chen CH, Lai HC. et al. Risk of empyema in patients with chronic liver disease and cirrhosis: a nationwide, population-based cohort study. Liver Int 2017; 37 (06) 862-870
  CrossrefPubMedGoogle Scholar
• 20 Feikin DR, Kagucia EW, Loo JD. et al; Serotype Replacement Study Group. Serotype-specific changes in invasive pneumococcal disease after pneumococcal conjugate vaccine introduction: a pooled analysis of multiple surveillance sites. PLoS Med 2013; 10 (09) e1001517
  CrossrefPubMedGoogle Scholar
• 21 Byington CL, Hulten KG, Ampofo K. et al. Molecular epidemiology of pediatric pneumococcal empyema from 2001 to 2007 in Utah. J Clin Microbiol 2010; 48 (02) 520-525
  CrossrefPubMedGoogle Scholar
• 22 Obando I, Muñoz-Almagro C, Arroyo LA. et al. Pediatric parapneumonic empyema, Spain. Emerg Infect Dis 2008; 14 (09) 1390-1397
  CrossrefPubMedGoogle Scholar
• 23 Wiese AD, Griffin MR, Zhu Y, Mitchel Jr. EF, Grijalva CG. Changes in empyema among U.S. children in the pneumococcal conjugate vaccine era. Vaccine 2016; 34 (50) 6243-6249
  CrossrefPubMedGoogle Scholar
• 24 Nath S, Thomas M, Spencer D, Turner S. Has the incidence of empyema in Scottish children continued to increase beyond 2005?. Arch Dis Child 2015; 100 (03) 255-258
  CrossrefPubMedGoogle Scholar
• 25 Díaz-Conradi A, Hernández S, García-García JJ. et al. Complicated pneumococcal pneumonia with pleural effusion or empyema in the 13-valent pneumococcal conjugate vaccine era. Pediatr Pulmonol 2019; 54 (05) 517-524
  CrossrefPubMedGoogle Scholar
• 26 Strachan R, Homaira N, Beggs S. et al. Assessing the impact of the 13 valent pneumococcal vaccine on childhood empyema in Australia. Thorax 2021; 76 (05) 487-493
  CrossrefPubMedGoogle Scholar
• 27 Karandashova S, Florova G, Azghani AO. et al. Intrapleural adenoviral delivery of human plasminogen activator inhibitor-1 exacerbates tetracycline-induced pleural injury in rabbits. Am J Respir Cell Mol Biol 2013; 48 (01) 44-52
  CrossrefPubMedGoogle Scholar
• 28 Tucker TA, Jeffers A, Alvarez A. et al. Plasminogen activator inhibitor-1 deficiency augments visceral mesothelial organization, intrapleural coagulation, and lung restriction in mice with carbon black/bleomycin-induced pleural injury. Am J Respir Cell Mol Biol 2014; 50 (02) 316-327
  CrossrefPubMedGoogle Scholar
• 29 Maskell NA, Batt S, Hedley EL, Davies CW, Gillespie SH, Davies RJ. 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
• 30 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
• 31 Hassan M, Cargill T, Harriss E. et al. The microbiology of pleural infection in adults: a systematic review. Eur Respir J 2019; 54 (03) 54
  CrossrefPubMedGoogle Scholar
• 32 Maskell NA, Davies CW, 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
• 33 Byington CL, Spencer LY, Johnson TA. et al. An epidemiological investigation of a sustained high rate of pediatric parapneumonic empyema: risk factors and microbiological associations. Clin Infect Dis 2002; 34 (04) 434-440
  CrossrefPubMedGoogle Scholar
• 34 Lin YT, Chen TL, Siu LK, Hsu SF, Fung CP. Clinical and microbiological characteristics of community-acquired thoracic empyema or complicated parapneumonic effusion caused by Klebsiella pneumoniae in Taiwan. Eur J Clin Microbiol Infect Dis 2010; 29 (08) 1003-1010
  CrossrefPubMedGoogle Scholar
• 35 Bai KJ, Wu IH, Yu MC. et al. Tuberculous empyema. Respirology 1998; 3 (04) 261-266
  CrossrefPubMedGoogle Scholar
• 36 Strachan R, Jaffé A. Australian Research Network in Empyema. Assessment of the burden of paediatric empyema in Australia. J Paediatr Child Health 2009; 45 (7-8): 431-436
  CrossrefPubMedGoogle Scholar
• 37 Nigo M, Vial MR, Munita JM. et al. Fungal empyema thoracis in cancer patients. J Infect 2016; 72 (05) 615-621
  CrossrefPubMedGoogle Scholar
• 38 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
• 39 Charoentunyarak S, Kananuraks S, Chindaprasirt J, Limpawattana P, Sawanyawisuth K. Blood culture bottle and standard culture bottle methods for detection of bacterial pathogens in parapneumonic pleural effusion. Jundishapur J Microbiol 2015; 8 (10) e24893
  CrossrefPubMedGoogle Scholar
• 40 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
• 41 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
• 42 Blackmore CC, Black WC, Dallas RV, Crow HC. Pleural fluid volume estimation: a chest radiograph prediction rule. Acad Radiol 1996; 3 (02) 103-109
  CrossrefPubMedGoogle Scholar
• 43 Brixey AG, Luo Y, Skouras V, Awdankiewicz A, Light RW. The efficacy of chest radiographs in detecting parapneumonic effusions. Respirology 2011; 16 (06) 1000-1004
  CrossrefPubMedGoogle Scholar
• 44 Porcel JM, Pardina M, Alemán C, Pallisa E, Light RW, Bielsa S. Computed tomography scoring system for discriminating between parapneumonic effusions eventually drained and those cured only with antibiotics. Respirology 2017; 22 (06) 1199-1204
  CrossrefPubMedGoogle Scholar
• 45 Xirouchaki N, Magkanas E, Vaporidi K. et al. Lung ultrasound in critically ill patients: comparison with bedside chest radiography. Intensive Care Med 2011; 37 (09) 1488-1493
  CrossrefPubMedGoogle Scholar
• 46 Lichtenstein D, Goldstein I, Mourgeon E, Cluzel P, Grenier P, Rouby JJ. Comparative diagnostic performances of auscultation, chest radiography, and lung ultrasonography in acute respiratory distress syndrome. Anesthesiology 2004; 100 (01) 9-15
  CrossrefPubMedGoogle Scholar
• 47 Yang PC, Luh KT, Chang DB, Wu HD, Yu CJ, Kuo SH. Value of sonography in determining the nature of pleural effusion: analysis of 320 cases. AJR Am J Roentgenol 1992; 159 (01) 29-33
  CrossrefPubMedGoogle Scholar
• 48 Asciak R, Hassan M, Mercer RM. et al. Prospective analysis of the predictive value of sonographic pleural fluid echogenicity for the diagnosis of exudative effusion. Respiration 2019; 97 (05) 451-456
  CrossrefPubMedGoogle Scholar
• 49 Kearney SE, Davies CW, Davies RJ, Gleeson FV. Computed tomography and ultrasound in parapneumonic effusions and empyema. Clin Radiol 2000; 55 (07) 542-547
  CrossrefPubMedGoogle Scholar
• 50 Chen CH, Chen W, Chen HJ. et al. Transthoracic ultrasonography in predicting the outcome of small-bore catheter drainage in empyemas or complicated parapneumonic effusions. Ultrasound Med Biol 2009; 35 (09) 1468-1474
  CrossrefPubMedGoogle Scholar
• 51 Peris A, Tutino L, Zagli G. et al. The use of point-of-care bedside lung ultrasound significantly reduces the number of radiographs and computed tomography scans in critically ill patients. Anesth Analg 2010; 111 (03) 687-692
  CrossrefPubMedGoogle Scholar
• 52 Davies HE, Davies RJ, Davies CW. 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
• 53 Sodhi KS, Bhatia A, Nichat V. et al. Chest MRI as an emerging modality in the evaluation of empyema in children with specific indications: pilot study. Pediatr Pulmonol 2021; 56 (08) 2668-2675
  CrossrefPubMedGoogle Scholar
• 54 Konietzke P, Mueller J, Wuennemann F. et al. The value of chest magnetic resonance imaging compared to chest radiographs with and without additional lung ultrasound in children with complicated pneumonia. PLoS One 2020; 15 (03) e0230252
  CrossrefPubMedGoogle Scholar
• 55 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
• 56 Towe CW, Srinivasan S, Ho VP. et al. Antibiotic resistance is associated with morbidity and mortality after decortication for empyema. Ann Thorac Surg 2021; 111 (01) 206-213
  CrossrefPubMedGoogle Scholar
• 57 Iliopoulou M, Skouras V, Psaroudaki Z. et al. Bacteriology, antibiotic resistance and risk stratification of patients with culture-positive, community-acquired pleural infection. J Thorac Dis 2021; 13 (02) 521-532
  CrossrefPubMedGoogle Scholar
• 58 Horowitz ML, Schiff M, Samuels J, Russo R, Schnader J. Pneumocystis carinii pleural effusion. Pathogenesis and pleural fluid analysis. Am Rev Respir Dis 1993; 148 (01) 232-234
  CrossrefPubMedGoogle Scholar
• 59 Uttamchandani RB, Daikos GL, Reyes RR. et al. Nocardiosis in 30 patients with advanced human immunodeficiency virus infection: clinical features and outcome. Clin Infect Dis 1994; 18 (03) 348-353
  CrossrefPubMedGoogle Scholar
• 60 Schnapp LM, Geaghan SM, Campagna A. et al. Toxoplasma gondii pneumonitis in patients infected with the human immunodeficiency virus. Arch Intern Med 1992; 152 (05) 1073-1077
  CrossrefPubMedGoogle Scholar
• 61 Kanellakis NI, Wrightson JM, Gerry S. et al. The bacteriology of pleural infection (TORPIDS): an exploratory metagenomics analysis through next generation sequencing. Lancet Microbe 2022; 3 (04) e294-e302
  CrossrefPubMedGoogle Scholar
• 62 Ko SC, Chen KY, Hsueh PR, Luh KT, Yang PC. Fungal empyema thoracis: an emerging clinical entity. Chest 2000; 117 (06) 1672-1678
  CrossrefPubMedGoogle Scholar
• 63 Bedawi EO, Ricciardi S, Hassan M. et al. ERS/ESTS statement on the management of pleural infection in adults. Eur Respir J 2023; 61 (02) 2201062
  CrossrefPubMedGoogle Scholar
• 64 Botana Rial M, Pérez Pallarés J, Cases Viedma E. et al. Diagnosis and treatment of pleural effusion. Recommendations of the Spanish Society of Pulmonology and Thoracic Surgery. Update 2022. Arch Bronconeumol 2023; 59 (01) 27-35
  CrossrefPubMedGoogle Scholar
• 65 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
• 66 Porcel JM, Ferreiro L, Rumi L. et al. Two vs. three weeks of treatment with amoxicillin-clavulanate for stabilized community-acquired complicated parapneumonic effusions. A preliminary non-inferiority, double-blind, randomized, controlled trial. Pleura Peritoneum 2020; 5 (01) 20190027
  CrossrefPubMedGoogle Scholar
• 67 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
• 68 Stern JB, Fournel L, Wyplosz B. et al. Early and delayed post-pneumonectomy empyemas: microbiology, management and prognosis. Clin Respir J 2018; 12 (04) 1753-1761
  CrossrefPubMedGoogle Scholar
• 69 Tagarro A, Otheo E, Baquero-Artigao F. et al; CORTEEC Study Group. Dexamethasone for parapneumonic pleural effusion: a randomized, double-blind, clinical trial. J Pediatr 2017; 185: 117-123.e6
  CrossrefPubMedGoogle Scholar
• 70 Fitzgerald DB, Waterer GW, Budgeon C. et al. Steroid Therapy and Outcome of Parapneumonic Pleural Effusions (STOPPE): a pilot randomized clinical trial. Am J Respir Crit Care Med 2022; 205 (09) 1093-1101
  CrossrefPubMedGoogle Scholar
• 71 Ashbaugh DG. Empyema thoracis. Factors influencing morbidity and mortality. Chest 1991; 99 (05) 1162-1165
  PubMedGoogle Scholar
• 72 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
• 73 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
• 74 Potts DE, Levin DC, Sahn SA. Pleural fluid pH in parapneumonic effusions. Chest 1976; 70 (03) 328-331
  CrossrefPubMedGoogle Scholar
• 75 Himelman RB, Callen PW. The prognostic value of loculations in parapneumonic pleural effusions. Chest 1986; 90 (06) 852-856
  CrossrefPubMedGoogle Scholar
• 76 Huang HC, Chang HY, Chen CW, Lee CH, Hsiue TR. Predicting factors for outcome of tube thoracostomy in complicated parapneumonic effusion for empyema. Chest 1999; 115 (03) 751-756
  CrossrefPubMedGoogle Scholar
• 77 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
• 78 Heffner JE, Brown LK, Barbieri C, DeLeo JM. Pleural fluid chemical analysis in parapneumonic effusions. A meta-analysis. Am J Respir Crit Care Med 1995; 151 (06) 1700-1708
  CrossrefPubMedGoogle Scholar
• 79 Rahman NM, Mishra EK, Davies HE, Davies RJ, Lee YC. 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
• 80 Cheng DS, Rodriguez RM, Rogers J, Wagster M, Starnes DL, Light RW. Comparison of pleural fluid pH values obtained using blood gas machine, pH meter, and pH indicator strip. Chest 1998; 114 (05) 1368-1372
  CrossrefPubMedGoogle Scholar
• 81 Fitzgerald DB, Leong SL, Budgeon CA. et al. Relationship of pleural fluid pH and glucose: a multi-centre study of 2,971 cases. J Thorac Dis 2019; 11 (01) 123-130
  CrossrefPubMedGoogle Scholar
• 82 Arnold DT, Hamilton FW, Elvers KT. et al. Pleural fluid suPAR levels predict the need for invasive management in parapneumonic effusions. Am J Respir Crit Care Med 2020; 201 (12) 1545-1553
  CrossrefPubMedGoogle Scholar
• 83 Bedawi EO, Kanellakis NI, Corcoran JP. et al. The biological role of pleural fluid PAI-1 and sonographic septations in pleural infection: analysis of a prospectively collected clinical outcome study. Am J Respir Crit Care Med 2023; 207 (06) 731-739
  CrossrefPubMedGoogle Scholar
• 84 Komissarov AA, Idell S. PAI-1 drives septation and clinical outcomes in pleural infection. Am J Respir Crit Care Med 2023; 207 (06) 653-655
  CrossrefPubMedGoogle Scholar
• 85 Fitzgerald DB, Lee YCG. Pleural infection: to drain or not to drain?. Respirology 2017; 22 (06) 1055-1056
  CrossrefPubMedGoogle Scholar
• 86 Letheulle J, Tattevin P, Saunders L. et al. Iterative thoracentesis as first-line treatment of complicated parapneumonic effusion. PLoS One 2014; 9 (01) e84788
  CrossrefPubMedGoogle Scholar
• 87 Arnold DT, Tucker E, Morley A. et al. A feasibility randomised trial comparing therapeutic thoracentesis to chest tube insertion for the management of pleural infection: results from the ACTion trial. BMC Pulm Med 2022; 22 (01) 330
  CrossrefPubMedGoogle Scholar
• 88 Horsley A, Jones L, White J, Henry M. Efficacy and complications of small-bore, wire-guided chest drains. Chest 2006; 130 (06) 1857-1863
  CrossrefPubMedGoogle Scholar
• 89 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
• 90 Rahman NM, Maskell NA, Davies CW. et al. The relationship between chest tube size and clinical outcome in pleural infection. Chest 2010; 137 (03) 536-543
  CrossrefPubMedGoogle Scholar
• 91 Taniguchi J, Nakashima K, Matsui H. et al. The relationship between chest tube position in the thoracic cavity and treatment failure in patients with pleural infection: a retrospective cohort study. BMC Pulm Med 2022; 22 (01) 358
  CrossrefPubMedGoogle Scholar
• 92 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
• 93 Davies HE, Rahman NM, Parker RJ, Davies RJ. Use of indwelling pleural catheters for chronic pleural infection. Chest 2008; 133 (02) 546-549
  CrossrefPubMedGoogle Scholar
• 94 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
• 95 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
• 96 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
• 97 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
• 98 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
• 99 Popowicz ND, Piccolo F, Yap E. et al. Long-term follow-up after intrapleural tPA/DNase therapy for pleural infection. Respirology 2021; 26 (04) 388-391
  CrossrefPubMedGoogle Scholar
• 100 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 (10) 5
  PubMedGoogle Scholar
• 101 Akulian J, Bedawi EO, Abbas H. et al; Interventional Pulmonary Outcomes Group. Bleeding risk with combination intrapleural fibrinolytic and enzyme therapy in pleural infection—an international, multicenter, retrospective cohort study. Chest 2022; 162 (06) 1384-1392
  CrossrefPubMedGoogle Scholar
• 102 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
• 103 Hart JA, Badiei A, Lee YCG. Successful management of pleural infection with very low dose intrapleural tissue plasminogen activator/deoxyribonuclease regime. Respirol Case Rep 2019; 7 (03) e00408
  CrossrefPubMedGoogle Scholar
• 104 Lansley SM, Cheah HM, Varano Della Vergiliana JF, Chakera A, Lee YC. Tissue plasminogen activator potently stimulates pleural effusion via a monocyte chemotactic protein-1-dependent mechanism. Am J Respir Cell Mol Biol 2015; 53 (01) 105-112
  CrossrefPubMedGoogle Scholar
• 105 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
• 106 Tremblay A, Stather DR, Maceachern P. How should we manage empyema complicating tunneled pleural catheter placement?. J Bronchology Interv Pulmonol 2010; 17 (02) 106-108
  CrossrefPubMedGoogle Scholar
• 107 Fitzgerald DB, Muruganandan S, Tsim S. et al. Intrapleural fibrinolytics and deoxyribonuclease for treatment of indwelling pleural catheter-related pleural infection: a multi-center observational study. Respiration 2021; 100 (05) 452-460
  CrossrefPubMedGoogle Scholar
• 108 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
• 109 Wu J, Liu C, Lee S, Kuo Y, Hsieh T. Assessment of the Charlson comorbidity index score, CHADS2 and CHA2DS2-VASc scores in predicting death in patients with thoracic empyema. Heart Lung 2018; 47 (02) 157-161
  CrossrefPubMedGoogle Scholar
• 110 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
• 111 Touray S, Sood RN, Lindstrom D. et al. Risk stratification in patients with complicated parapneumonic effusions and empyema using the RAPID score. Lung 2018; 196 (05) 623-629
  CrossrefPubMedGoogle Scholar
• 112 Vincent JL, de Mendonça A, Cantraine F. et al. Use of the SOFA score to assess the incidence of organ dysfunction/failure in intensive care units: results of a multicenter, prospective study. Working group on “sepsis-related problems” of the European Society of Intensive Care Medicine. Crit Care Med 1998; 26 (11) 1793-1800
  CrossrefPubMedGoogle Scholar
• 113 Vincent JL, Moreno R, Takala J. et al. The SOFA (Sepsis-related Organ Failure Assessment) score to describe organ dysfunction/failure. On behalf of the working group on sepsis-related problems of the European Society of Intensive Care Medicine. Intensive Care Med 1996; 22 (07) 707-710
  CrossrefPubMedGoogle Scholar
• 114 Seymour CW, Liu VX, Iwashyna TJ. et al. Assessment of clinical criteria for sepsis: for the third international consensus definitions for sepsis and septic shock (Sepsis-3). JAMA 2016; 315 (08) 762-774
  CrossrefPubMedGoogle Scholar
• 115 Asai N, Shibata Y, Hirai J. et al. Could quick SOFA and SOFA score be a predictive tool for 30-day and in-hospital mortality in acute empyema?. J Infect Chemother 2022; 28 (12) 1687-1692
  CrossrefPubMedGoogle Scholar
• 116 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
• 117 Dean NC, Griffith PP, Sorensen JS, McCauley L, Jones BE, Lee YC. Pleural effusions at first ED encounter predict worse clinical outcomes in patients with pneumonia. Chest 2016; 149 (06) 1509-1515
  CrossrefPubMedGoogle Scholar