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Ann Thorac Surg 2009;87:1690-1696. doi:10.1016/j.athoracsur.2009.01.077
© 2009 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

The Removal of Chest Tubes Despite an Air Leak or a Pneumothorax

Robert J. Cerfolio, MDa,*, Douglas J. Minnich, MDb, Ayesha S. Bryant, MSPH, MDb

a Department of Surgery, Division of Cardiothoracic Surgery, University of Alabama at Birmingham, Birmingham, Alabama
b Department of Cardiothoracic Surgery, University of Alabama at Birmingham, Birmingham, Alabama

Accepted for publication January 7, 2009.

* Address correspondence to Dr Cerfolio, Division of Cardiothoracic Surgery, University of Alabama at Birmingham, 703 19th St S, ZRB 739, Birmingham, AL 35294 (Email: robert.cerfolio{at}ccc.uab.edu).

Presented at the Fifty-fifth Annual Meeting of the Southern Thoracic Surgical Association, Austin, TX, Nov 5–8, 2008.


    Abstract
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 References
 
Background: The presence of an air leak is currently a contraindication for removal of a chest tube. The objective of this series was to evaluate the safety of chest tube removal in patients with an air leak.

Methods: This study was a retrospective cohort study of a prospective database. Patients who underwent elective pulmonary resection and were discharged home with a chest tube were eligible.

Results: Between July 2000 and July 2007, 6,038 patients underwent elective pulmonary resection by one general thoracic surgeon. One hundred and ninety-nine patients (3.8%) with a persistent air leak had their chest tubes placed to a suctionless portable drainage device and were discharged home. One hundred ninety-four patients (97%) returned to our clinic (median, postdischarge day 16). One hundred thirty-seven patients had no air leak, and 57 patients still had an air leak. All 137 patients (including 26 with a nonexpanding pneumothorax) had their chest tubes removed. In addition, all 57 patients (including 19 who had pneumothorax as well) had their chest tubes removed without sequela (9 after provocative clamping). At 3 months' follow-up, all patients were asymptomatic without evidence of pleural space problems, except 3 (all in the persistent air leak group) in whom an empyema developed.

Conclusions: Patients with air leaks can be safely discharged home with their chest tubes. These tubes can be safely removed even if the patients have a pneumothorax, if the following criteria are met: the patients have been asymptomatic, have no subcutaneous emphysema after 14 days on a portable device at home, and the pleural space deficit has not increased in size.


    Introduction
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 References
 
Over the past decade, surgeons have made great advances in the management of chest tubes through the use of prospective randomized studies [1–3]. Before the objective data gleaned from several studies, most decisions were based on subjective opinion based on where and with whom one trained, as opposed to results from peer-reviewed, evidence-based medicine.

We have studied the problem of air leaks and chest tube management and, like Brunelli and colleagues [4], have attempted to apply science to this concept [5–7]. A simplified set of conclusions from all of these studies include the following: one can predict preoperatively with some degree of certainty which patients are likely to have a persistent air leak; that water seal, and not suction, is the best setting for chest tubes in most patients with air leaks (as long as the leak is not large); and that some suction may help promote sealing in some patients with large air leaks if the chest roentgenogram shows a lack of pleural-pleural apposition. Moreover, we have shown that it is safe to remove chest tubes when the drainage is as high as, but not greater than, 450 cc/day [8], and we recently evaluated the use of digital air leak meters and drainage devices [9].

Importantly, it has been shown that patients can be discharged home safely on outpatient drainage devices if they have an air leak after postoperative day 4 [8, 10]. However, when we first reported that chest tubes could be removed from patients with air leaks, many were skeptical of this concept, and many still have a difficult time adopting this concept in their practice. The primary objective of this study was to report our experience with sending patients home with a chest tube attached to an outpatient device and removing the chest tube 2 weeks postoperatively, even if the patient had an air leak and even if some patients had a concomitant pneumothorax as well.


    Material and Methods
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 References
 
Patients who underwent elective nonpneumonectomy pulmonary resection between July 2000 and July 2007 were eligible for this study. Patients were excluded if they were less than 19 years of age, and underwent decortication, empyectomy, pneumonectomy, or esophagogastrectomy. Patients with nonsmall-cell lung cancer who underwent pulmonary resection had complete thoracic lymphadenectomy, as previously described [11]. Patients had one chest tube placed after lobectomy, starting January 2005; before this time, we routinely used two tubes. Tubes were managed as outlined below and were assessed twice per day (on morning and afternoon rounds) for an air leak. A chest radiograph was performed once a day (early morning). It was repeated only if the patient had worsening oxygen saturation, subcutaneous air, or complications. If patients had a persistent air leak (as defined below), their tube was attached to outpatient suctionless device. The devices most commonly used in this study were the Heimlich valve, early in our experience, the Atrium Express (Atrium Medical, Hudson, NH), used throughout much of this series, and most recently, the mini Sahara (Teleflex, Mansfield, MA). In general, when patients had a persistent air leak on postoperative day 3, their tubes were attached to one of these outpatient devices. The patients were observed for 6 hours, and a repeat chest radiograph was performed. If there was no expanding subcutaneous emphysema or an enlarging pneumothorax, then the patient was discharged home on the outpatient device. Patients did not receive antibiotics while in the hospital; however, those who were discharged home with a chest tube in place were prescribed cephalexin, 500 mg daily, for the duration they had the tube.

When patients returned to the clinic, a chest roentgenogram was performed before they saw us. The presence or absence of an air leak was then determined, and this film was compared with the discharge film. After chest tube removal, a repeat chest radiograph was performed within 4 hours. The chest tube site was covered loosely (unlike the manner in which we cover a chest tube site that is only 3 to 4 days old). Follow-up surveillance was performed using hospital and clinic databases, along with our office prospective database, in which any postdischarge patient-related call was logged by our clinical team. Patients often called to update us on their status.

The Institutional Review Board of the University of Alabama at Birmingham approved this study and the electronic prospective database. Patient consent was obtained for entry into the prospective database, and patients were aware that these data would be used for research purposes, but patient consent was waived for participation in this particular study.

Chest Tube Management
From July 2000 until December 2004, most patients had two chest tubes placed after lobectomy. One was positioned apical-posteriorly and the other apical-anteriorly. After January 2005, only one apical-posteriorly placed chest tube was used after lobectomy. One tube was used for wedge resection or segmentectomy throughout the study time frame. However, if the patient had an air leak that could not be sewn closed before chest closure, and there appeared to be a significant pleural space problem after lung expansion, a second chest tube was placed apically and anteriorly. All chest tubes were 28F soft Deknatel (Teleflex, Mansfield, MA) tubes. These tubes were connected to a Sahara S-1100a Pleur-evac Chest Drainage System (Genzyme Biosurgery, Cambridge, MA). However, from 2006 to 2007, some patients had their chest tube placed to a Digivent (Millicore, Danderyd, Sweden) and some to a Medela (Medela, Huvudkontor, Switzerland) digital air leaks system as parts of other studies. Chest tubes were placed to –20 cm of wall suction on the day of surgery, and then were changed to water seal on the morning of postoperative day 1. The chest tubes remained on water seal unless a patient had a symptomatic pneumothorax or clinically significant subcutaneous emphysema [12].

Definitions
A nonexpanding pneumothorax was defined as a pneumothorax that was not any larger, based on comparison with the most recent chest roentgenogram, compared with a previous one. The readmission rate was defined as any overnight hospital admission within 3 months of discharge date. For patients who were readmitted to other services at the University of Alabama or to other hospitals, the cause for readmission and the treatment rendered were determined by review of our notes, letters and notes from the admitting physician, and by the discharge summary. A readmission that was due or partially due to a pleural effusion was defined as any patient who was readmitted within 90 days of discharge, whose pleural effusion was determined to be the cause of the readmission, whose symptoms that led to the readmission were possibly secondary to the pleural effusion, or whose pleural effusion was greater on readmission than on discharge and required any type of intervention to drain an effusion that was ipsilateral to the previous thoracotomy performed within the last 60 days. Limited pulmonary function was defined as forced expiratory volume of air in 1 second (FEV1%) of less than 50 or lung diffusion capacity for carbon monoxide (DLCO%) of less than 80 in our patient population. A persistent air leak was defined as an air leak that was present on postoperative day 4.

Statistics
Data were analyzed by using the Student t test and the Wilcoxon and {chi}2 tests as appropriate. A stepwise multivariate logistic regression model was used to correct for the effect of multiple variables and their interactions for persistent air leak. Variables that were associated with persistent air leak with a p value of less than 0.1 in the univariate analysis were entered into the multivariate model. The software used was SAS version 9.1 (SAS Institute, Cary, NC). A two-sided p value of less than 0.05 was considered statistically significant and unlikely due to chance.


    Results
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 References
 
From July 2000 to July 2007, 6,038 patients underwent elective pulmonary resection by one general thoracic surgeon. There were 199 patients who had a persistent air leak who tolerated their chest tubes attached to an outpatient device without suction for 24 hours. (The number of patients who initially failed this maneuver and had to be returned to suction is unknown). These patients were sent home with a chest tube connected to the outpatient device. Of these 199 patients, 194 (97%) returned to our clinic, and their characteristics are shown in Table 1. Five patients were seen at the clinic of their primary care provider only because of transportation issues, and none had an air leak. All of their chest tubes were removed, and by report, none had complications but, because of the lack of chest roentgenogram information, they were removed from further analysis in this study. The remaining 194 patients returned to our clinic a median of 16.5 days after discharge. Their characteristics are shown in Table 2, stratified by their air leak status upon return to the clinic (after being home on the outpatient device for about 2 weeks). Univariate analysis showed that diabetes mellitus, smoking within 4 weeks before surgery, limited pulmonary function (as defined by FEV1% less than 50 or DLCO% less than 80%, or both), previous ipsilateral thoracotomy, and chronic steroid use were statistically significantly different between patients who did and did not have an air leak during the postoperative visit. On multivariate analysis, poor pulmonary function tests (p = 0.004, odds ration = 2.36, confidence interval: 1.82 to 2.96) and a history of neoadjuvant therapy (p = 0.001, odds ratio = 1.89, confidence interval: 1.31 to 2.75) remained significant predictors for air leak at the time of the clinic visit.


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Table 1 Patient Characteristics
 

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Table 2 Univariate Comparisons of Patients Who Did and Did Not Have Air Leak During Postoperative Clinic Visit, n = 194
 
Figure 1 depicts the follow-up results for the 194 patients. Upon return to clinic, 137 patients had no air leak present, and 57 had a persistent air leak. Of the 137 with no leak, 26 had a pneumothorax. However, only 5 patients had a pneumothorax that was slightly larger than at discharge. These 5 patients underwent readmission and in-hospital chest tube clamping and observation overnight. All did well and had their chest tubes removed the next morning. Therefore, 132 patients of the 137 had their tubes removed in the clinic, even though 21 had a pneumothorax.


Figure 1
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Fig 1. Outcomes of chest tube (CT) study. The numbers in parentheses indicate the number of patients. Dashed line indicates management based on our previous protocol.

 
There were 57 patients who returned to the clinic with a persistent air leak, also as shown in Figure 1. Of these 57 patients, 38 had no pneumothorax and 19 did. Thirty-three of the 38 patients without a pneumothorax had their chest tubes removed in the clinic. The first 5 patients were readmitted because they represented our initial experience, and they underwent in-hospital chest tube clamping and observation before tube removal. Of the 19 patients with both a persistent air leak and a pneumothorax, 4 patients were readmitted for overnight surveillance with chest tube clamping because their air leak was larger. All 9 of these patients had their chest tube removed the next day without sequela.

Five patients were readmitted to our hospital or other hospitals before their scheduled 3-week postoperative clinic visit. The causes for readmission were the following: nausea, vomiting, and dehydration in 2 patients, and pain control, pneumonia, and a transient ischemic attack in 1 patient each. At 3-month follow-up, all patients were asymptomatic without evidence of pleural space problems. Patients who had a fixed pleural space deficit had filling of the space with fluid. One patient had progressive dyspnea, and he underwent thoracentesis at an outside hospital; however, his fluid later returned and his dyspnea improved with medical management. Importantly, an empyema developed in 3 patients (3 of 194 = 1.5%, or 3 of 57 with a persistent leak = 5.3%). All of these patients had an air leak when they returned to our clinic for their postoperative week 3 visit. All 3 patients were immunocompromised, 2 had a previous solid organ transplant, all 3 were on steroid therapy, and all 3 had a lobectomy. These 3 patients underwent reoperation with empyectomy and were subsequently discharged home (hospital lengths of stay were 3, 4, and 7 days).


    Comment
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 References
 
We and others have shown that chest tubes can be removed early on postoperative day 2 after pulmonary lobectomy, and even on postoperative day 1 after a wedge resection if the drainage is less than 450 cc per day [8]. We have shown that if patients have an air leak, the chest tube is best managed when placed to water seal and suction avoided. This concept has been confirmed by Marshall and coworkers [3] and partially confirmed by Brunelli and associates [13]. That is even true if the patient has a pneumothorax and an air leak, as long as there is not an expanding pneumothorax on water seal or the development of subcutaneous emphysema [14].

In this study, we have shown that patients can be sent home with a chest tube with an air leak, and the tube can be removed in the clinic approximately 2 to 3 weeks postoperatively, even if the air leak or pneumothorax are still present, with few or no sequelae. Patients do not need to be admitted for provocative chest tube clamping. The tube can simply be removed in the outpatient clinic if the chest radiograph shows no expansion of the fixed pleural space deficit that was present when the tube was on suction and if the patient is breathing well without worsening dyspnea or development of subcutaneous emphysema while home for 2 weeks.

The mechanism of action that prevents the lung from collapsing when a chest tube is removed in a patient who still has an air leak is not fully understood. These patients are at least 21 days after surgery, and the tube has been on water seal for at least 14 days while the patients were at home. This observation suggests the pleural space is stable. Even if there is a pneumothorax or fixed pleural space deficit, the lung likely has formed enough adhesions to surrounding structures to prevent collapse and prevent tension pneumothorax. Therefore, even though the lung may still be leaking, that does not lead to an expanding or a tension pneumothorax. The key is to remove the tube as soon as possible from these patients because further delay probably only increases the risk of empyema.

The manner in which the chest tube is removed from these patients deserves special consideration. Because these patients have a continued air leak, the dressing is intentionally placed loosely around the chest tube site for some air to escape the pleural space, instead of placing an airtight dressing as is normally done. The concern for air entering the pleural space after chest tube removal, which is important for the more typical patient, is not a concern with these patients. Moreover, the chest tube site is often red and tender since a tube has been in it for 3 weeks. No matter how the chest tube is sutured to the skin, there will be inflammation around the chest tube track, and it will be epithelialized after 3 weeks. We use a large no. 5 Ethicon (Johnson & Johnson, Somerset, NJ) suture in the operating room and take a large deep bite of the subcutaneous tissue when we secure the chest tube to the skin. We make the stitch loose on the skin so it does not become ischemic, yet it is deep in the subcutaneous tissue and tight around the chest tube.

We are often sent patients who have had tubes in for 2 to 3 months or even longer because "the patient still has an air leak," and in many, an iatrogenic empyema has developed. Air leaks probably introduce infected or dirty air into the pleural space, and that, coupled with an indwelling chest tube, likely serve as a nidus of infection that leads to empyema. As seen in this study, 3 patients had an empyema after just 3 weeks with a chest tube. Thus, the risk exists in all patients. All 3 had to be taken back to the operating room for decortication and empyectomy; muscle transfer may be required if there is a fixed pleural space deficit that is infected that the lung cannot fill. All of these patients were immunocompromised, all had a persistent air leak at 3-week follow-up, and all had a relatively large fixed pleural space deficit.

The strengths of this study include the large number of patients, the high rate of follow-up, and the performing of all procedures by one surgeon. The primary limitation of this study is that our chest tube management algorithm changed during the study period and that the study was retrospective.

In conclusion, we have shown that air leaks and fixed pleural space deficits are common after pulmonary resection, especially after lobectomy. These fixed pleural space deficits do not require intervention, and chest tubes can be safely removed from the vast majority of patients, even if there is an air leak or if a chest radiograph shows a pneumothorax, if the patient can tolerate an outpatient suctionless device for 2 weeks and remain asymptomatic.


    Discussion
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 References
 
DR JOSEPH I. MILLER (Atlanta, GA): First, I would like to thank the Association for the privilege of discussing the paper. I thank Cerf for sending me a copy of it, and as our esteemed president, John Hammon, has said, this is the third in a series. So with this, I would like to present these remarks both on the basis of what has been presented today and also what is in the body of the manuscript, because I think some of the interesting things are in the body of the manuscript, not included in the presentation.

First, I want to say I am very proud of Cerf and what he has accomplished at the University of Alabama. He is certainly one of the truly rising young stars in general thoracic surgery. In the spirit of the Southern Thoracic, though, discussion should be both humorous and informative, and with that, I would like to make these remarks.

Now, let us look at the facts of the paper. It is a large study by one surgeon, 5,198 operated patients in a large sample size, of whom 193 in the paper sent to me, or 3.8%, had a persistent air leak and were discharged home with an underwater seal device. Note in the paper he used four different underwater seal devices to go home with. At Emory it takes an act of Congress to change one of them. So, Cerf, I congratulate you on that.

But the fact that they could go home on an underwater seal device is not anything new. Many people have done that since the 1980s and 1990s in the lung volume, the AIDS era, with pneumocystis and pentamidine. So the fact that they were discharged home is not necessarily new.

Now, let us focus on the real heart of the paper, the 57 patients with a persistent air leak upon whom Cerf had the fortitude to go ahead and remove the tube despite the persistent air leak. Of the 57, there were no complications, no mortality except three empyemas. This is like "The Perfect Paper." It reminds me a little of "The Perfect Storm."

He states in the paper, but it was not presented, "We have studied the problems of air leaks and management and have attempted to apply science to their concept." He then makes a number of points, all of which are known by experienced thoracic surgeons. He makes it a point of when to use one or two chest tubes, but this is really not anything new. He supports all of his previously stated and reported data as if this is the gospel according to Cerf.

He then states that it requires—this is in the paper—a PGY-10 to remove the chest tube at a late time. He further states that a new and randomized trial is under way at our institution to determine the best way to remove a chest tube either on inspiration or expiration.

Now, the true facts and worth of this paper are as follows. A well-known, rising national surgeon who has been well advanced and is one of the truly rising stars in general thoracic surgery has broken the myth that a chest tube cannot be removed with a persistent air leak. Cerf has shown that a chest tube can be removed without significant complications. The fact that these patients can be sent home is not new, but the fact that after 21 days, with certain stipulations met, the tube can be removed without sequelae or complications, this is the first time that I have ever heard this presented at a national meeting, and I think this is the value of your paper, and I truly congratulate you. It is well documented, it is well substantiated.

Cerf, I think this probably is the best paper that you have yet to present, and I am pleased to discuss it. Keep Ayesha [Bryant] by your side. Doug [Minnich], you did a great job. These comments are offered by a senior thoracic surgeon in the spirit of discussion at the Southern Thoracic Surgical Association. Thank you.

DR CERFOLIO: I want to hear Dr Minnich respond to that.

DR MINNICH: Thank you.

DR CERFOLIO: Doug, I don't think there was a question there to respond to—I do not have too much to say after that except I appreciate Dr Miller's candidness and his humor. We do want to make the meeting fun, and as usual, Dr Miller was both informative and entertaining. I do appreciate his kind comments at the end.

DR WILLIAM A. COOK (North Andover, MA): I am rising for two reasons. I want to prevent the group from Atlanta from piling on, but it stuns me, it stuns me to realize that a man with your perception has missed the one real thing that you had in your own hand. Your last presentation on shingling ribs, if you had only extended it a bit, you would have accomplished what we call a thoracoplasty and you probably wouldn't have had all those air leaks to begin with.

DR CERFOLIO: Thank you, Dr Cook.

DR KAMAL A. MANSOUR (Atlanta, GA): On a serious note, I think your point is well taken. All thoracic surgeons deal with chest tubes, and they really do not know what to do when the tubes keep on leaking air for more than 10 days. I have two points. The first is you put in a Heimlich valve and send the patient home, which is a great idea. My warning is that if there is chest tube drainage, fluid, not only air, and you put in a Heimlich valve, then the incidence of infection is going to be very high. I suggest that you should not send patients home with a Heimlich valve that is draining.

The second point—which is very important—is, is there any instance where you have to go in and close that miserable hole and finish with it? I noticed that you insist on not bringing the patient back to the operating room by any means, even on account of having infection. My point is, as we teach, if the tube stays more than 10 to 14 days and the air leak is continuous and not slowing down, you should take them to surgery and close the hole. Thank you very much.

DR MINNICH: Thank you, Dr Mansour. Your comment regarding Heimlich valves and persistent drainage is an important one. Among the devices that are listed, there was a progression in the device that was used throughout the study period. Most recently, the primary device being used is a mini-Sahara device, which does provide a receptacle to drain any effluent that may be present. I would agree that the issues with persistent fluid drainage through a Heimlich valve can become a very messy problem for the patient to deal with at home.

With regard to reoperation for a persistent air leak, there were no patients in this series who required an additional procedure specifically for the air leak. All of them tolerated their chest tubes being removed with no sequelae.

DR RODNEY LANDRENEAU (Pittsburgh, PA): I am just concerned, and I think really we ought to have, if we are going to do this or try to promote this, a study beyond just a single institution. Certainly, all of the things that I have read and reviewed of your work and the work of the University Alabama have been eye opening and thought provoking, and even with the last paper you had with regard to early removal of the tube with high volumes. I believe your data. It is just that in Pittsburgh, I must be unlucky, because every time I remove a tube that has still got an air leak I get an empyema 2 or 3 weeks later. So that is my concern about this. My own personal experience with this, or at least my subjective experience, doesn't match what you are seeing, and we ought to do a study.

DR CERFOLIO: Can I take a swing at that, Dr Minnich?

DR MINNICH: Sure.

DR CERFOLIO: So what I would say is, you are right, we would like to see this corroborated in other centers and published. I can tell you that I have gotten e-mails and telephone calls from lots of people in this room who have done this after they have e-mailed me about a patient, and it has worked for them from what they have told me.

But you have to be very careful and apply this to the properly selected patients. You cannot just "take a chest tube out in a patient with an air leak"—that is not what I am saying or our data are saying. Our data apply to a specific set of patients. It applies to patients who have an air leak at 3 or 4 days and they are otherwise ready for discharge home. You put them on a suctionless device, an Atrium Express or a mini-Sahara. If their lung falls and they get subcutaneous air or they become symptomatic, you can't pull the tube out and you cannot send them home. You have got to wait, put them back on a little bit of suction, and try it again. When they finally can tolerate water seal and there is no pneumothorax, or a small one, that is stable and the patient is asymptomatic and there is no new subcutaneous air, no increasing pneumothorax, no problems after 24 hours on the Atrium Express or the mini-Sahara, then you have won. Then you can send them home on the Atrium Express for 2 weeks, and we give them 500 mg of Keflex a day, a low prophylactic dose.

And I promise you, I promise you if they come back in your clinic postoperatively, 3 weeks (which is usually 2 weeks at home on that Atrium Express), you can pull that tube out every time, whether they are leaking or not, whether they still have the pneumothorax or not, whether there is still subcutaneous air or not—as long as they are asymptomatic, their pneumothorax is not bigger, and they don't have more or new subcutaneous air. The sooner you get the tube out now, the better, and the less likely they are going to get an empyema. The ones who get empyema are the ones who are still leaking at 3 weeks postoperatively and who had a concomitant pneumothorax. I think this is because the air that leaks is "dirty" or infected, and the pleural space is not filled by the lung because of the fixed pleural space deficit.

DR LANDRENEAU: That is my concern. It is not the fact the lung is going to drop. It is really the late sequelae.

DR CERFOLIO: Yes, and as we have shown in this study, we had three empyemas—we have had that experience as well. But it is uncommon if you do not wait too long and you get the tube out after 3 weeks—2 weeks after they are home on the Atrium Express or the mini-Sahara.


    References
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 References
 

  1. Cerfolio RJ, Bass CS, Katholi CR. Prospective randomized trial compares suction versus water seal for air leaks Ann Thorac Surg 2001;71:1613-1617.[Abstract/Free Full Text]
  2. Cerfolio RJ, Tummala RP, Holman WL, et al. A prospective algorithm for the management of air leaks after pulmonary resection Ann Thorac Surg 1998;66:1726-1731.[Abstract/Free Full Text]
  3. Marshall MB, Deeb ME, Bleier JI, et al. Suction vs water seal after pulmonary resection: a randomized prospective study Chest 2002;121:831-835.[Abstract/Free Full Text]
  4. Cerfolio RJ, Bass CS, Pask MH, Katholi CR. Predictors and treatment of persistent air leaks Ann Thorac Surg 2002;73:1727-1730.[Abstract/Free Full Text]
  5. Brunelli A, Ximue F, Refai M, Salati M, Marasco R, Sabbatini A. Air leaks after lobectomy increase the risk of empyema but not of cardiopulmonary complications: a case-matched analysis Chest 2006;130:1150-1156.[Abstract/Free Full Text]
  6. Brunelli A, Sabbatini A, Ximue F, Refai MA, Salati M, Marasco R. Alternate suction reduces prolonged air leak after pulmonary lobectomy: a randomized comparison versus water seal Ann Thorac Surg 2005;80:1052-1055.[Abstract/Free Full Text]
  7. Brunelli A, Monteverde M, Borri A, Salati M, Marasco RD, Fianchini A. Predictors of prolonged air leak after pulmonary lobectomy Ann Thorac Surg 2004;77:1205-1210.[Abstract/Free Full Text]
  8. Cerfolio RJ, Bryant AS. Results of a prospective algorithm to remove chest tubes after pulmonary resection with high output J Thorac Cardiovasc Surg 2008;135:269-273.[Abstract/Free Full Text]
  9. Cerfolio RJ, Bryant AS. The benefits of continuous and digital air leak assessment after elective pulmonary resection: a prospective study Ann Thorac Surg 2008;86:396-401.[Abstract/Free Full Text]
  10. McKenna RJ, Mahtabifard A, Pickens A. Fast-tracking after video-assisted thoracoscopic surgery lobectomy, segmentectomy, and pneumonectomy Ann Thorac Surg 2007;84:1663-1667.[Abstract/Free Full Text]
  11. Cerfolio RJ, Bryant AS. The distribution and likelihood of lymph node metastasis based on the lobar location of nonsmall-cell lung cancer Ann Thorac Surg 2006;81:1969-1973.[Abstract/Free Full Text]
  12. Cerfolio RJ. Recent advances in the treatment of air leaks Curr Opin Pulm Med 2005;11:319-323.[Medline]
  13. Brunelli A, Sabbatini A, Xiume' F, Refai MA, Salati M, Marasco R. Alternate suction reduces prolonged air leak after pulmonary lobectomy: a randomized comparison versus water seal Ann Thorac Surg 2005;80:1052-1055.[Abstract/Free Full Text]
  14. Cerfolio RJ, Bryant AS, Maniscalco LM. Management of subcutaneous emphysema after pulmonary resection Ann Thorac Surg 2008;85:1759-1763.[Abstract/Free Full Text]



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M. Liberman, A. Muzikansky, C. D. Wright, J. C. Wain, D. M. Donahue, J. S. Allan, H. A. Gaissert, C. R. Morse, D. J. Mathisen, and M. Lanuti
Incidence and Risk Factors of Persistent Air Leak After Major Pulmonary Resection and Use of Chemical Pleurodesis
Ann. Thorac. Surg., March 1, 2010; 89(3): 891 - 898.
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C. F. Chong
Management of Patients With Persistent Air Leak After Elective Pulmonary Resection
Ann. Thorac. Surg., February 1, 2010; 89(2): 671 - 671.
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R. J. Cerfolio
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Ann. Thorac. Surg., February 1, 2010; 89(2): 671 - 672.
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