Hemothorax and Occult Pneumothorax, Management of

Authors

Nathan T. Mowery, MD
Oliver L. Gunter, MD
Bryan R. Collier, DO
Jose’ J. Diaz, Jr., MD
Elliott Haut, MD
Amy Hildreth, MD
Michelle Holevar, MD
John Mayberry, MD
Erik Streib, MD

I. Statement of the Problem

Thoracic trauma is a notable cause of morbidity and mortality in American trauma centers, where 25% of trau­matic deaths are related to injuries sustained within the thoracic cage.^[1] Chest injuries occur in ~60% of polytrauma cases; therefore, a rough estimate of the occurrence of hemo­thorax related to trauma in the United States approaches 300,000 cases per year.^[2] The management of hemothorax and pneumothorax has been a complex problem since it was ?rst described over 200 years ago. Although the majority of chest trauma can be managed nonoperatively, there are several questions surrounding the management of hemothorax and occult pneumothorax that are not as easily answered.

The technologic advances have raised the question of what to do with incidentally found hemothorax and pneumotho­rax discovered during the trauma evaluation. Previously, we were limited by our ability to visualize quantities <500 mL of blood on chest radiograph. Now that smaller volumes of blood can be visualized via chest computed tomography (CT), the manage­ment of these ?ndings presents interesting clinical questions.

In addition to early identi?cation of these processes, these patients often ?nd themselves with late complications such as retained hemothorax and empyema. The approach to these complex problems continues to evolve.

Finally, as minimally invasive surgery grows and ?nds new applications, there are reproducible bene?ts to the patients in pursuing these interventions as both a diagnostic and therapeutic interventions. Video-assisted thoracoscopic surgery (VATS) has a growing role in the management of trauma patients. 

II. Process

A computerized search of the National Library of Medi­cine MEDLINE database was undertaken using the PubMed Entrez interface. English language citations during the period of 1965 through 2008 using the primary search strategy: 

hemothorax[mh] pneumothorax[mh] AND humans[mh] NOT (case reports[pt] OR letter[pt] OR comment[pt] OR news[pt])

Review articles were also excluded. The PubMed Related Articles algorithm was also used to identify additional articles similar to the items retrieved by the primary strategy. Of ~127 articles identi?ed by these two techniques, those dealing with either prospective or retrospective studies examining hemotho­rax and pneumothorax were selected, comprising 43 institutional studies evaluating diagnosis and management of adult patients with hemothorax or pneumothorax (Table 1). The articles were reviewed by a group of nine surgeons who collaborated to produce this practice management guideline.

The correlation between the evidence and the recom­mendations is as follows:

Level I

This recommendation is convincingly justi?able based on the available scienti?c information alone. It is usually based on Class I data; however, strong Class II evidence may form the basis for a Level 1 recommendation, especially if the issue does not lend itself to testing in a randomized format. Conversely, weak or contradictory Class I data may not be able to support a Level 1 recommendation.

Level II

This recommendation is reasonably justi?able by avail­able scienti?c evidence and strongly supported by expert critical care opinion. It is usually supported by Class II data or a preponderance of Class III evidence.

Level III

This recommendation is supported by available data, but adequate scienti?c evidence is lacking. It is generally supported by Class III data. This type of recommendation is useful for educational purposes and in guiding future research.

III. Recommendations

Diagnosis

1. Ultrasound can reliably be used to identify pneumothorax and pleural effusion (Level 2).
2. CT of the chest is indicated in patients with persistent opacity on chest radiograph after tube thoracostomy to determine whether signi?cant undrained ?uid exists (Level 2).
3. Primary VATS of stable penetrating thoracoabdominal wounds is safe and effective for the diagnosis and man­agement of selected diaphragm and pulmonary injuries (Level 2).

Management of Massive Hemothorax

1. Patient physiology should be the primary indications for surgical intervention rather than absolute numbers of ini­tial or persistent output (Level 2).
2. 1500 mL via a chest tube in any 24-hour period regardless of mechanism should prompt consideration for surgical exploration (Level II). 

Management of Hemothorax

1. All hemothoraces, regardless of size, should be considered for drainage (Level 3).
2. Attempt of initial drainage of hemothorax should be with a tube thoracostomy (Level 3).
3. Persistent retained hemothorax, seen on plain ?lms, after placement of a thoracostomy tube should be treated with early VATS, not a second chest tube (Level 1).
4. VATS should be done in the ?rst 3 days to 7 days of hospitalization to decrease the risk of infection and con­version to thoracotomy (Level 2).
5. Intrapleural thrombolytic may be used to improve drain­age of subacute (6-day to 13-day duration) loculated or exudative collections, particularly patients where risks of thoracotomy are signi?cant (Level 3). 

Management of Occult Pneumothorax

1. Occult pneumothorax, those not seen on chest radiograph, may be observed in a stable patient regardless of positive pressure ventilation (Level 3).
2. Scoring systems are not accurate in predicting which patients will need a tube thoracostomy for occult pneu­mothorax (Level 3).
3. A persistent air leak on postinjury day 3 should prompt a VATS evaluation (Level 2).

IV. Scientific Foundation

Historical Background

Hemorrhage from or within the chest has been de­tailed in numerous medical writings dating back to ancient times. Although lesser forms of trauma were commonly treated in the ancient physician’s daily practice, major injuries, especially those to the chest, were dif?cult to treat and often lethal.

By the 18th century, treatment for hemothorax was advocated; however, surgeons disagreed as to its form. A number of surgeons, including John Hunter in 1794, advo­cated the creation of an intercostal incision and drainage of the hemothorax. Those of the opposing view recommended closure of chest wounds without drainage. Although Hunter’s method was effective in evacuating the hemothorax, the morbidity associated with the creation of an iatrogenic pneu­mothorax as a result of the procedure was signi?cant. The risks associated with wound closure or conservative manage­ment included the possibility that empyema with sepsis would develop or that persistent trapped lung with permanent reduction of pulmonary function would result.

Observing the advantages and dangers of both forms of therapy, Guthrie, in the early 1800s, proposed early evacua­tion of blood through an existing chest wound. He asserted that if bleeding from the chest persisted, the wound should be closed in the hope that existing intrathoracic pressure would halt the bleeding. If the desired effect was accomplished, he advised that the wound be reopened several days later for the evacuation of retained clotted blood or serous ?uid.

By the 1870s, early hemothorax evacuation by trocar and cannula or by intercostal incision was considered stan­dard practice. Not long after this, underwater seal drainage was described by a number of different physicians. This basic technique has remained the most common form of treatment for hemothorax and other pleural ?uid collections to this day.^[3]

V. Diagnostic Evaluation of Hemothorax

Plain Films

The upright chest radiograph remains the primary di­agnostic study in the acute evaluation of hemothorax. In the normal unscarred pleural space, a hemothorax is noted as a meniscus of ?uid blunting the costophrenic angle or dia­phragmatic surface and tracking up the pleural margins of the chest wall when viewed on the upright chest X-ray (CXR) ?lm. As much as 400 mL to 500 mL of blood is required to obliterate the costophrenic angle as seen on an upright chest radiograph. In the acute trauma setting, the portable supine chest radiograph may be the ?rst and only view available from which to make de?nitive decisions regarding therapy. The presence and size of a hemothorax is much more dif?cult to evaluate on supine ?lms. As much as 1,000 mL of blood may be missed when viewing a portable supine CXR ?lm. CXR has been found to be a poor predictor of patients requiring a VATS.^[4]

Ultrasound

Trauma ultrasonography is used at some trauma centers in the initial evaluation of patients for hemothorax. One drawback of ultrasonography for the identi?cation of trau­matic hemothorax is that associated injuries readily seen on chest radiographs in the trauma patient, such as bony injuries, widened mediastinum, and pneumothorax, are not readily identi?able on chest ultrasonography. One advantage is the ability to detect pneumothorax more quickly in circumstances than plain ?lms or CT would allow.^[5] There continues to be a push to move ultrasound application to the intensive care unit (ICU) bedside to allow the intensivist to gain information without the burden of transporting patients. Ultrasound has reliably been shown to document the presence and volume of a pleural effusion. Intensivists have also attempted to use it to document pulmonary contusions with less success.^[6] [7] The current role of ultrasound in the ICU would appear to be when CT is unavailable or if the patient’s physiology would not permit transport. The sensitivity and speci?city are not superior to CT, and ultrasound does not offer a global picture of the thoracic anatomy.

Computed Tomography

Computed tomographic scan is a highly accurate diag­nostic study for pleural ?uid or blood. In the initial trauma setting, it does not necessarily have a primary role in the diagnosis of hemothorax and pulmonary contusion but is complementary to chest radiography. CT may actually be too sensitive in identifying clinically nonsigni?cant injuries.^[8] This is an area of controversy not addressed in this Practice Management Guidelines. Because many victims of blunt trauma do undergo a chest and/or abdominal computed to­mographic scan evaluation, hemothorax not seen on initial chest radiographs might be identi?ed and treated.

Computed tomographic scan may also be value later in the course of the chest trauma for localization and quanti?­cation of any retained collections of clot and potential em­pyema within the pleural space. Numerous authors have suggested the need for further evaluation of persistent abnor­mal plain ?lm ?ndings or patients who fail to progress on the ventilator with CT.^[9] [10] Early, aggressive investigation of potential hemothorax can lead to the discovery of patho­logic processes that can have an effect on patient’s short and long-term recovery. Conversely, delaying further im­aging may severely limit the physicians options for oper­ative approaches.^[9]

Primary Video-Assisted Thoracoscopy

Surgeons continue to explore the utility of VATS pro­cedures for both primary diagnosis and therapy. In stable trauma patients with thoracic injuries, proceeding directly to VATS to identify injuries even before placement of a chest tube has been shown to be safe.^[11] [12] It is unknown based on the current literature if such a course of actions leads to shorter hospitalizations or fewer complications than tube thoracostomy alone. In the case of thoracoabdominal wounds, VATS can identify injuries missed on CT.^[11] [13]

Evaluation of the Evidence Supporting Early Operative Management for Massive Hemothorax

Thoracotomy is the procedure of choice for surgical exploration of the chest when massive hemothorax or persis­tent bleeding is present. Traditional criteria indicating the necessity to proceed with urgent thoracotomy are as follows:

Y More than 1,500 mL of blood immediately evacuated by tube thoracostomy. Y Persistent bleeding from the chest, de?ned as 150 mL/h to 200 mL/h for 2 hours to 4 hours. Y Persistent blood transfusion is required to maintain he­modynamic stability.

These criteria were developed from expert opinion and not from prospective trials. In fact, submitting these criteria to prospective study would be dif?cult and unethical. Instead, the evidence to supporting indications for urgent thoracotomy based on tube thoracostomy output is derived from a variety of descriptive retrospective studies over the past 30 years. In these case series of mostly penetrating chest injuries, sur­geons merely contrasted patients who “required” urgent tho­racotomy with those patients who did not.^[14–19] The military experience in World War II and Vietnam also helped to establish many of the indications for penetrating trauma to the chest.^[19] Indications for urgent thoracotomy were based on physiology, a premise is still recommended, and minimum chest tube output amounts (i.e., 800 mL) which has in?ated over time. The numbers for both initial output and persistent output have continued to increase as surgeons have taken more liberties over time. These early studies suffered from a lack of statistical power or ability to differentiate from a control group. Mansour et al.^[20] attempted to establish a difference between penetrating and blunt injury observing that patients with blunt trauma rarely required urgent inter­vention based on chest tube output. They suggested that physiology and refractory shock rather than absolute volumes of output should be the indication for urgent thoracotomy. Karmy-Jones et al.^[21] attempted to de?ne the indications for urgent thoracotomy more clearly in a multicenter retrospec­tive trial. They advocated thoracotomy when total chest tube output exceeded 1,500 mL in a 24-hour period regardless of the mechanism of injury. In this series, mortality increased linearly with chest tube output and the mortality at 1,500 mL was three times greater than at 500 mL. This ?nding lends validity to the proposed volume of 1,500 mL as an indicator for thoracotomy, but this report did not elaborate on the coexisting physiologic parameters that were present at differ­ent chest tube outputs.

Evaluation of the Evidence Supporting Early Operative Management for Retained Hemothorax

Tube thoracostomy drainage is the primary mode of treatment for hemothorax. In adult patients, large-bore chest tubes, usually 36 F to 42 F, is the traditional means used to achieve adequate drainage in adults.

Surgeons debate how large a hemothorax can be safely observed. Billelo et al.^[22] contended that collections <1.5 cm on CT can be observed, but their report is severely limited by a lack of long-term follow-up to determine the true risk of ?brothorax or empyema. Others contend that empyema can be prevented entirely by evacuation of hemothorax in the ?rst 7 days.^[23] [24] Conversely, radiographically apparent hemotho­rax after chest tube placement leads to a 33% rate of empy­ema.^[25] Most authors have used the estimated volume of 500 mL, the amount needed to be seen on plain X-ray, as the entry point into studies looking at evacuation of retained hemotho­rax.^{[4] [23] [26]}

It is unknown whether complications of retained hemothorax including empyema and ?brothorax could be decreased by a more aggressive approach.

After tube thoracostomy is performed, a repeat chest radiograph should always be obtained. This helps identify chest tube position, helps determine completeness of the hemothorax evacuation, and may reveal other intrathoracic pathology previously obscured by the hemothorax. The pres­ence of retained hemothorax on postplacement CXR has been shown to be an independent predictor of the development of an empyema in 33% of patients.^[25] If drainage is incomplete as visualized on the postthoracostomy chest radiograph, place­ment of a second drainage tube should be discouraged. In a prospective randomized trial, Meyer et al.^[27] showed that patients who had retained hemothorax on plain ?lms 72 hours after initial chest tube output bene?ted from early VATS instead of a second chest tube. Patients undergoing VATS had signi?cantly shorter duration of chest tube drainage, fewer days in the hospital after the procedure, and lower hospital costs than putting in a second chest tube. In addition, 10 of the 24 patients who underwent a second chest tube required surgical intervention later in their hospital stay.

Evaluation of the Evidence for the Timing of Surgical Intervention

The timing of surgical intervention for retained hemo­thorax continues to be controversial. VATS performed early in the patient’s hospital course may be associated with less morbidity.^{[12] [23] [27] [28]}

Early VATS (before day 3) results in statistically signi?cant reduction in operative dif?culty, con­tamination/infection of clot, and hospital length of stay com­pared with those performed later.^[26] There seems to be no absolute contraindication to attempting VATS in a delayed fashion as successful procedures have been performed as far out as 14 days.^[29] The surgeon should be prepared and counsel the patient that conversion to thoracotomy becomes more likely after 5 days.^[26] [28]

Operative Approach

Successful thoracoscopic surgery for retained hemothorax is being reported with greater frequency. Several surgeons have made the claim that VATS has distinct advantages over open thoracotomy for the evacuation of retained hemothorax and empyema.^[28] [30] Bene?ts named include fewer pulmonary com­plications, shorter time to recovery, and less long-term dis­ability.^[31] Infectious complications have been shown to be higher in thoracotomy.^[23]

Fibrinolytics

In an effort to move to a nonoperative method of evacuating retained hemothorax, authors have proposed using various ?brinolytics. Some authors have been able to docu­ment clot evacuation using intrapleural ?brolytics.^[32] [33] Al­though these studies have demonstrated safety, it is dif?cult to gauge the contribution of the ?brolytic agent made in the success of the evacuation rather than well-placed drains. Oguzkaya et al.^[34] showed that VATS is a more effective procedure than intrapleural streptokinase for the management of posttraumatic retained hemothorax with VATS patients having a statistically signi?cant shorter hospital stay and decreased need for additional therapy. Currently, ?brinolytic agents would have to be seen as a second-line agent behind surgical intervention when the risks of surgery are too great to the patient’s overall outcome.

Evaluation of the Evidence Supporting Management for Occult Pneumothorax

As computed tomographic scan is being performed more commonly in the evaluation of trauma patients, many injuries are now identi?ed, which had previously not been detected. Occult pneumothorax, usually de?ned as a pneu­mothorax that is seen on chest CT but not on plain ?lms, is being diagnosed more frequently.^[35] [36] Some authors have argued that some of these occult pneumothoraces are missed^[37] rather than invisible injuries. Retrospective data would support that placing a chest tube will lead to longer hospital stays and longer ICU stay.^[38] The issue is trying to determine the lesions that will progress and that can safely be observed. Wolfman et al.^[39] used the location of the pneumo­thorax to predict which would fail observation and found only very small anterior pneumothorax could be observed with a high rate of success (81%). De Moya et al.^[40] attempted to categorize pneumothoraces using a scoring system based on size and location in a retrospective analysis.

Another key question has been the factor of positive pressure ventilation. Many authors have excluded all patients who were to undergo positive pressure ventilation^[35] [41] while others included them in the analysis.^[38] Enderson et al.^[42] attempted to answer the question in a prospective fashion. They found that patients with pneumothoraces treated with observation who underwent positive pressure ventilation de­veloped an unacceptable rate of complications with 3 of the 15 patients on positive pressure developing a tension pneu­mothorax. Conversely, Brasel et al.^[43] found the opposite to be true in a prospective randomized study. They found no increase in complications regardless of whether chest tube or observation was chosen. Notably, two of the three patients in the observation arm who required a chest tube for progression of the pneumothorax did so after being placed on positive pressure ventilation. Both studies suffered from low numbers but would support the notion that the majority of patients with occult pneumothoraces will not have progression regardless of the presence of positive pressure ventilation.

Evaluation of the Evidence Supporting Management of Posttraumatic Empyema

Approximately 3% of patients with chest trauma will develop a posttraumatic empyema. This number is slightly higher in penetrating trauma.^[44] [45] Many authors have at­tempted to de?ne the risk factors for posttraumatic empyema. There are consistent risk factors that appear in multiple studies including persistent pleural effusion/hemothorax and the duration of a tube thoracostomy.^[44] In addition, the place­ment of multiple tubes has been associated in a prospective^[27] and retrospective^[46] fashion to lead to empyema. These ?ndings have lead authors to recommend complete evacuation of the chest following trauma to avoid the morbidity of empyema.^[47]

Other Indications for VATS in the Trauma Field

There is also data to support the use of VATS for other indications. In addition to its value in diagnostic evaluation and evacuation of retained hemothorax, authors have de­scribed its value in treating persistent pneumothorax/air leak. The safety and high success rate in identifying the causative lesion has been documented for this indication.^[48] Schermer et al.^[49] found that in patients with a persistent air leak, under­going a VATS at day 3 had shorter hospital stays and less days with a chest tube. Given the data concerning increased chest tube days and empyema risk, one could hypothesize that this might also decrease late complications.

VI. Summary

To summarize, plain ?lms are used a screening tool, but additional imaging in the form of CT is needed in any patient that has persistent radiographic abnormalities after placement of simple tube thoracostomy. The physician should attempt to clear the chest cavity of all retained hemothorax as early in the hospital course as the patient’s physiology will allow. The preferred methods of this would be a VATS over a second chest tube. VATS can be attempted in the ?rst 5 days with a low conversion rate to thoracotomy, but there is a decreasing success rate after this time period. Surgery outside of this initial window does not preclude attempting a thoracoscopic approach for retained hemothorax or for empyema but should be undertaken with both the surgeons and patient’s expecta­tions for an increased possibility of open thoracotomy. The decision to perform early evacuation of retained hemothorax with VATS technology is likely to greatly diminish the number of patients who develop the sequelae of empyema and ?brothorax. Although it adds an operative procedure to the patient’s management, this approach provides de?nitive treatment, while avoiding the morbidity of a formal thoracot­omy, and decreases total hospital stay when compared with more conservative management methods.

VII. References

1. Manlulu AV, Lee TW, Thung KH, Wong R, Yim AP. Current indica­tions and results of VATS in the evaluation and management of hemo­dynamically stable thoracic injuries. Eur J Cardiothorac Surg. 2004;25: 1048–1053.
2. Richardson JD, Miller FB, Carrillo EH, Spain DA. Complex thoracic injuries. Surg Clin North Am. 1996;76:725–748. 
3. Rusch VW, Ginsberg RJ. Chest wall, pleura, lung and mediastinum. Schwartz SI, ed. Principles of Surgery. New York, NY: McGraw-Hill; 1999;667–790.
4. Velmahos GC, Demetriades D. Early thoracoscopy for the evacuation of undrained haemothorax. Eur J Surg. 1999;165:924–929.
5. Soldati G, Testa A, Pignataro G, et al. The ultrasonographic deep sulcus sign in traumatic pneumothorax. Ultrasound Med Biol. 2006;32:1157– 1163.
6. Rocco M, Carbone I, Morelli A, et al. Diagnostic accuracy of bedside ultrasonography in the ICU: feasibility of detecting pulmonary effusion and lung contusion in patients on respiratory support after severe blunt thoracic trauma. Acta Anaesthesiol Scand. 2008;52:776–784.
7. Soldati G, Testa A, Silva FR, Carbone L, Portale G, Silveri NG. Chest ultrasonography in lung contusion. Chest. 2006;130:533–538.
8. Kwon A, Sorrells DL Jr, Kurkchubasche AG, Cassese JA, Tracy TF Jr, Luks FI. Isolated computed tomography diagnosis of pulmonary contu­sion does not correlate with increased morbidity. J Pediatr Surg. 2006; 41:78–82.
9. Watkins JA, Spain DA, Richardson JD, Polk HC Jr. Empyema and restrictive pleural processes after blunt trauma: an under-recognized cause of respiratory failure. Am Surg. 2000;66:210–214.
10. Velmahos GC, Demetriades D, Chan L, et al. Predicting the need for thoracoscopic evacuation of residual traumatic hemothorax: chest radio­graph is insuf?cient. J Trauma. 1999;46:65–70.
11. Divisi D, Battaglia C, De BB, et al. Video-assisted thoracoscopy in thoracic injury: early or delayed indication? Acta Biomed. 2004;75:158–163.
12. Liu DW, Liu HP, Lin PJ, Chang CH. Video-assisted thoracic surgery in treatment of chest trauma. J Trauma. 1997;42:670–674.
13. Paci M, Ferrari G, Annessi V, de FS, Guasti G, Sgarbi G. The role of diagnostic VATS in penetrating thoracic injuries. World J Emerg Surg. 2006;1:30.
14. Kish G, Kozloff L, Joseph WL, Adkins PC. Indications for early thoracotomy in the management of chest trauma. Ann Thorac Surg. 1976;22:23–28.
15. Siemens R, Polk HC Jr, Gray LA Jr, Fulton RL. Indications for thoracotomy following penetrating thoracic injury. J Trauma. 1977;17: 493–500.
16. Mattox KL. Thoracic injury requiring surgery. World J Surg. 1983;7: 49–55.
17. Reul GJ Jr, Beall AC Jr, Jordan GL Jr, Mattox KL. The early operative management of injuries to great vessels. Surgery. 1973;74:862–873.
18. Oparah SS, Mandal AK. Operative management of penetrating wounds of the chest in civilian practice. Review of indications in 125 consecutive patients. J Thorac Cardiovasc Surg. 1979;77:162–168.
19. McNamara JJ, Messersmith JK, Dunn RA, Molot MD, Stremple JF. Thoracic injuries in combat casualties in Vietnam. Ann Thorac Surg. 1970;10:389–401.
20. Mansour MA, Moore EE, Moore FA, Read RR. Exigent postinjury thoracotomy analysis of blunt versus penetrating trauma. Surg Gynecol Obstet. 1992;175:97–101.
21. Karmy-Jones R, Jurkovich GJ, Nathens AB, et al. Timing of urgent thoracotomy for hemorrhage after trauma: a multicenter study. Arch Surg. 2001;136:513–518.
22. Bilello JF, Davis JW, Lemaster DM. Occult traumatic hemothorax: when can sleeping dogs lie? Am J Surg. 2005;190:841–844.
23. Heniford BT, Carrillo EH, Spain DA, Sosa JL, Fulton RL, Richardson JD. The role of thoracoscopy in the management of retained thoracic collections after trauma. Ann Thorac Surg. 1997;63:940–943.
24. Fabbrucci P, Nocentini L, Secci S, et al. Video-assisted thoracoscopy in the early diagnosis and management of post-traumatic pneumothorax and hemothorax. Surg Endosc. 2008;22:1227–1231.
25. Karmy-Jones R, Holevar M, Sullivan RJ, Fleisig A, Jurkovich GJ. Residual hemothorax after chest tube placement correlates with in­creased risk of empyema following traumatic injury. Can Respir J. 2008;15:255–258.
26. Vassiliu P, Velmahos GC, Toutouzas KG. Timing, safety, and ef?cacy of thoracoscopic evacuation of undrained post-traumatic hemothorax. Am Surg. 2001;67:1165–1169.
27. Meyer DM, Jessen ME, Wait MA, Estrera AS. Early evacuation of traumatic retained hemothoraces using thoracoscopy: a prospective, randomized trial. Ann Thorac Surg. 1997;64:1396–1400.
28. Morales Uribe CH, Villegas Lanau MI, Petro Sanchez RD. Best timing for thoracoscopic evacuation of retained post-traumatic hemothorax. Surg Endosc. 2008;22:91–95.
29. Navsaria PH, Vogel RJ, Nicol AJ. Thoracoscopic evacuation of retained posttraumatic hemothorax. Ann Thorac Surg. 2004;78:282–285.
30. Scherer LA, Battistella FD, Owings JT, Aguilar MM. Video-assisted thoracic surgery in the treatment of posttraumatic empyema. Arch Surg. 1998;133:637–641.
31. Ben-Nun A, Orlovsky M, Best LA. Video-assisted thoracoscopic sur­gery in the treatment of chest trauma: long-term bene?t. Ann Thorac Surg. 2007;83:383–387.
32. Kimbrell BJ, Yamzon J, Petrone P, Asensio JA, Velmahos GC. In­trapleural thrombolysis for the management of undrained traumatic hemothorax: a prospective observational study. J Trauma. 2007;62: 1175–1178.
33. Pollak JS, Passik CS. Intrapleural urokinase in the treatment of loculated pleural effusions. Chest. 1994;105:868–873.
34. Oguzkaya F, Akcali Y, Bilgin M. Videothoracoscopy versus intrapleural streptokinase for management of post traumatic retained haemothorax: a retrospective study of 65 cases. Injury. 2005;36:526–529.
35. Hill SL, Edmisten T, Holtzman G, Wright A. The occult pneumothorax: an increasing diagnostic entity in trauma. Am Surg. 1999;65:254–258.
36. Ball CG. 2005 Incidence, risk factors, and outcomes for occult pneu­mothoraces in victims of major trauma. J Trauma. 2005;59:917–924; discussion 924–925.
37. Ball CG, Kirkpatrick AW, Fox DL, et al. Are occult pneumothoraces truly occult or simply missed? J Trauma. 2006;60:294–298.
38. Collins JC, Levine G, Waxman K. Occult traumatic pneumothorax: immediate tube thoracostomy versus expectant management. Am Surg. 1992;58:743–746.
39. Wolfman NT, Myers WS, Glauser SJ, Meredith JW, Chen MY. Validity of CT classi?cation on management of occult pneumothorax: a prospec­tive study. AJR Am J Roentgenol. 1998;171:1317–1320.
40. de Moya MA, Seaver C, Spaniolas K, et al. Occult pneumothorax in trauma patients: development of an objective scoring system. J Trauma. 2007;63:13–17.
41. Garramone RR Jr, Jacobs LM, Sahdev P. An objective method to measure and manage occult pneumothorax. Surg Gynecol Obstet. 1991; 173:257–261.
42. Enderson BL, Abdalla R, Frame SB, Casey MT, Gould H, Maull KI. Tube thoracostomy for occult pneumothorax: a prospective randomized study of its use. J Trauma. 1993;35:726–729.
43. Brasel KJ, Stafford RE, Weigelt JA, Tenquist JE, Borgstrom DC. Treatment of occult pneumothoraces from blunt trauma. J Trauma. 1999;46:987–990.
44. Eren S, Esme H, Sehitogullari A, Durkan A. The risk factors and management of posttraumatic empyema in trauma patients. Injury. 2008;39:44–49.
45. Helling TS, Gyles NR III, Eisenstein CL, Soracco CA. Complications following blunt and penetrating injuries in 216 victims of chest trauma requiring tube thoracostomy. J Trauma. 1989;29:1367–1370.
46. Aguilar MM, Battistella FD, Owings JT, Su T. Posttraumatic empyema. Risk factor analysis. Arch Surg. 1997;132:647–650.
47. Eddy AC, Luna GK, Copass M. Empyema thoracis in patients under­going emergent closed tube thoracostomy for thoracic trauma. Am J Surg. 1989;157:494–497.
48. Carrillo EH, Schmacht DC, Gable DR, Spain DA, Richardson JD. Thoracoscopy in the management of posttraumatic persistent pneumo­thorax. J Am Coll Surg. 1998;186:636–639.
49. Schermer CR, Matteson BD, Demarest GB III, Albrecht RM, Davis VH. A prospective evaluation of video-assisted thoracic surgery for persistent air leak due to trauma. Am J Surg. 1999;177:480–484.

Table