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Division of Cardiothoracic Surgery, University of Alabama, Birmingham, Alabama
Accepted for publication December 31, 2007.
* Address correspondence to Dr Cerfolio, Department of Surgery, Division of Cardiothoracic Surgery, University of Alabama at Birmingham, 703 19th St S, ZRB 739, Birmingham, AL 35294 (Email: rcerfolio{at}uab.edu).
Presented at the Fifty-fourth Annual Meeting of the Southern Thoracic Surgical Association, Bonita Springs, FL, Nov 7–10, 2007.
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Methods: A retrospective review was made of a prospective database. Patients who underwent pulmonary resection and in whom clinically detected SE were studied.
Results: Of 4,023 patients between January 1999 and June 2006, 255 patients (6.3%) had clinically apparent SE. Predictors of developing SE by multivariate analysis were preoperative forced expiratory volume of air in 1 second (FEV1%) less than 50%, having an air leak, and having had a previous thoracotomy. Despite maximizing chest tube suction, 85 patients (33%) had recalcitrant SE. These patients with recalcitrant SE were more likely to have a lower median FEV1% (p = 0.037), a previous ipsilateral thoracotomy, and have undergone a lobectomy (p < 0.001). Recently, 64 of the 85 patients underwent single-incision, video-assisted thorascopic surgery with pneumolysis and chest tube placement, which successfully resolved the SE within 24 hours in all patients except 1. These 64 patients had a significantly shorter hospital stay (6 versus 9 days, p = 0.02) and less time with recalcitrant SE than the other 21 patients.
Conclusions: Subcutaneous emphysema is more likely in patients who have an FEV1% less than 50% and who undergo a redo thoracotomy. Recalcitrant SE emphysema (SE that persists despite increasing chest tube suction) is more likely in patients who undergo lobectomy and is best treated by video-assisted thorascopic surgery with pneumolysis between the leaking lung, which is usually partially adhered to the previously opened intercostal space. This directs the air leak back into the pleural space and out of the subcutaneous space. This procedure shortens the duration of SE and hospital stay.
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Definitions
Clinically symptomatic SE was defined as air under the skin that was perceptible by the clinician, patient, or family member, or a change in voice. Patients who had SE that was only radiologically apparent were not included in this study. Persistent or recalcitrant SE was defined as SE that did not resolve despite the presence of a patent, functional chest tube on high suction in the pleural space.
Surgical Technique of VATS Pneumolysis for Recalcitrant SE
Patients with recalcitrant SE who were taken back to the operating room underwent the following procedure. A bronchoscopy was performed to ensure there was no bronchopleural fistula, and usually the procedure was done with a single-lumen endotracheal tube only. One single 2- to 3-cm incision was made between the previous thoracotomy incision and the previous chest tube incision (thus inferior to the initial thoracotomy incision but superior to the previous chest tube incisions). Video-assisted thorascopic surgery was carried out through this sole incision, and the lung, which was commonly found to be adhered to the part of the chest that had been previously opened, was taken down using a sucker, as these adhesions were usually only a few days old. That caused the pulmonary alveolar leak (which was a pulmonary alveolar-subcutaneous fistula) to now drain into the pleural space instead of the subcutaneous space (making it an alveolar-pleural fistula). A new 28F soft chest tube (Deknatel) was placed through the incision, and it was placed on –40 cm of wall suction. Once the subcutaneous emphysema resolved or diminished, patients were placed on an Atrium Express (Atrium Medical Corporation, Hudson, New Hampshire) and discharged home after 1 day of observations to ensure the SE did not return on this compact home portable device.
Statistics
A 
2 analysis or Fisher exact test was used to evaluate discrete dichotomous variables. Analysis of variance (ANOVA) was used for discreet nondichotomous variables. For continuous variables, Student's t test or the Mann-Whitney U test was used to compare means. All comparisons were two-sided with a p value of less than 0.05 used to indicate statistical significance. Univariate analyses were performed with a two-sided log-rank test [6]. Variables with a significant difference between groups based on results of the univariate analyses were entered as candidate variables in a multivariate analysis with both forward and backward stepwise inclusion of factors, with an inclusion criterion of p 0.05. All statistical analysis was performed using SAS v. 9.0 (SAS Institute, Cary, North Carolina).
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One important possible variable for this increase may be that we are operating on more patients with low FEV1% and DLCO%. As shown in this paper, both the FEV1% and DLCO% were predictors of developing SE, and they were also predictors of having recalcitrant SE on univariate analysis. Another cause may be that we, like others, have changed to placing only one chest tube after lobectomy instead of two. In addition, we now use a softer tube (a 28F chest tube), which, although it may be less painful, it is also more susceptible to kinking with patient movement. We now prefer two tubes for patients who have "nonsewable" air leaks and those with a large pleural space deficit noted after reexpanding the lung at the time of chest closure. If there is a significant pleural space deficit and concomitant nonsewable air leaks, a pleural tent for upper space problems [7] should be performed and a pneumoperitoneum for lower space problems.
We have shown in a prospective study that pneumoperitoneum created at the time of the thoracotomy is safe and effective after concomitant lower and middle right lobectomies [8] and reduces air leak duration and hospital stay. In addition, Brunelli and colleagues [7] have shown that the use of pleural tents after upper lobectomy may reduce the incidence of air leaks as well. Recall that patients who underwent pleural tents or pneumoperitoneum were eliminated from this study. We now also advocate the placement of a subcutaneous drain over the intercostal space and position it extrathoracically in selected patients to further help prevent SE. Yet despite all of these intraoperative techniques, patients still have air leaks and SE. The final, and perhaps most important cause of the rising incidence of SE and recalcitrant SE, is the almost exclusive use of water seal in patients with air leaks after postoperative day 1.
Chest Tube Management
Many use water seal for patients with air leaks because of our previous prospective randomized studies as well as those of Marshal and coworkers [9–12]. These studies suggest that water seal is the optimal chest tube setting in patients with air leaks after lung resection. The presence of a pneumothorax and an air leak is not an indication for suction, as we have shown in 2005 [13]. However, in some patients, such as those with a large leak (greater than an E3 on the RDC classification system) some suction is needed. When SE or voice changes develop secondary to SE, we believe this is an absolute indication to add suction to the chest tube. We use the least amount of suction required (as we believe the more the suction, the larger the leak gets) to eliminate the SE. We prefer to start with –10 cm of suction and observe the patient for 4 to 6 hours. Brunneli and colleagues [14] have also presented strong, provocative randomized data that suggest that use of intermittent suction (they prefer it at night when patients are not walking) may be best for pulmonary air leaks. If the SE continues despite adding as much as –40 cm of suction, then another chest tube is indicated. The placement of a new chest tube at the bedside can be successful in most patients, but it is painful and can be difficult to position ideally because of the SE and the previous surgery. It also does not work in some patients, and it was those patients who we took to the operating room and discovered the reason.
As shown in this paper, we have found that a common etiology of SE is that the part of the lung that is leaking air is often adhered to the intercostal space that had been previously opened. This is true for patients that had a thoracotomy or a VATS. The air leak from the lung goes into the SE tissue and not into the pleural space, and thus another chest tube is not effective at reducing the SE. Once in the extrathoracic space at the intercostal opening, the air follows the path of least resistance, and it easily dissects through the recently surgically disrupted tissue planes into the subcutaneous fascia. It can then traverses into the face, eyelids, or larynx or even downward into the groin. As seen in this series, once we made this discovery (after the first 21 patients with recalcitrant SE), we started to offer VATS more quickly in these patients if increasing the suction on the existing chest tube did not improve the SE within 24 hours instead of placing another chest tube at the bedside.
In this study, we have shown that a single-incision VATS, using a single-lumen tube only, is safe, easy, quick, and effective. It is not difficult to lyse or take down these 3- to 5-day-old adhesions using only one incision and by placing a sucker alongside the VATS camera. This maneuver drives the leak back into the pleural space where it can be controlled with the new chest tube. We have not used glues or sealants over the part of the lung or tried to restaple that area because the tissue is usually very inflamed. A new chest tube is then placed through this incision and placed on suction overnight. That eradicated the SE in all but 1 of the 64 patients in this series. We then send the patient home a few days later with the chest tube still in the chest and attached to a closed portable outpatient device, as previously described [9]. When VATS was performed immediately in these 64 patients, instead of trying a bedside chest tube first, the length of stay was significantly shorter (6 days compared with 9, p = 0.02), and they had less time with recalcitrant SE than the other 21 patients. All 85 patients went home with chest tubes attached to a home portable compact device but discharge was not permitted for patients until the SE was resolved.
The strengths of this study include the reduction of confounding factors by the use of one surgeon and the near 100% follow-up of patients. However, the limitations are significant. First, the data are retrospective and nonrandomized. Second, the majority of our data are related to "our experience." Additionally, the technique of VATS pneumolysis was employed in only the latter half of this study. Ideally, from a scientific standpoint, we should have randomly allocated the patients to a bedside chest tube or to a VATS procedure, but our experience and intraoperative observations now strongly biase us toward preferring VATS. We would no longer condone a trial that randomly assigned patients to an additional bedside chest tube over a VATS reexploration and chest tube placement.
In conclusion, the management of SE, like air leaks, should be based on scientific objective data. Our algorithm for this problem is to first ensure the existing chest tube is in the pleural space, is patent, is correctly attached to the drainage system, and is not clogged, twisted, or clamped. If the tube is patent and the addition of high wall suction does not resolve the SE, then an additional bedside chest tube is a reasonable option. However, it is no longer our next procedure of choice. As shown from the data above, we have found that most common cause of SE is from a leaking portion of the lung, which is often adhered to the part of the chest that was previously opened. This causes the air that is leaking from the lung to dissect into the subcutaneous space instead of the pleural space. Once in the subcutaneous space, it can easily travel through the already surgically dissected tissue planes and lead to SE in the face, eyelids, larynx, or groin area. Single-incision VATS using a single-lumen tube is safe, quick, and effective. It almost always will successfully eradicate the problem within 6 to 12 hours. That avoids the delays and morbidity associated with a bedside chest tube or computed tomography–guided catheters, which although at times is effective, takes longer to eliminate the SE. Video-assisted thorascopic surgery allows the patients with air in the eyelids to see sooner, and that helps restore the confidence of the patient and family in the physician's care. The use of small supraclavicular incisions to help evacuate the air is rarely needed and should be reserved for the very rare patient who has failed a VATS procedure and all other measures.
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Again, we commend your group for always looking at common problems that we don't really have any evidence-based medicine data for, and always trying to improve our daily practice in such a thoughtful and organized fashion. My first point addresses your statement in the abstract, the incidence of the subcutaneous emphysema is increasing. In your paper on the treatment of persistent air leaks that you actually presented here 6 years ago, in that paper of nearly 700 patients, your incidence of subcutaneous emphysema was actually 0.9%. You state the risk factors that are indeed the real causes for this. It is inferred that with a lower FEV1 that these patients may be more emphysematous, yet in your manuscript that you kindly provided to me, these patients who had to go to surgery were actually almost 10 years younger than those ones who actually had no problems with subcutaneous emphysema. So what is the explanation? Is it because they will tolerate a second operation better? Is there a change in your surgical technique such as going to video-assisted thorascopic surgery (VATS)? For instance, I don't really find this problem that often in my practice. I actually still use these blowholes that my teacher, Jamie Olak, taught me. I find that these blowholes actually take care of things. They do decompress the air leak, and then obviously we try to avoid the second operation.
DR CERFOLIO: Thank you for your kind comments and since I am a hockey player I enjoy scoring a hat trick in any game or having three papers or more on at one meeting. It is my team that gets the credit for that, not I.
We have had an increased incidence of subcutaneous emphysema. I took out the possible reasons for this in my slides, for time's sake, but it is in the manuscript, and we enumerate some reasons. One, I have gone to one chest tube after a lobe instead of two; two, I use a 28F chest tube that is soft; I use a little softer tube than I did 5 or 6 years ago. I don't have data that it decreases pain, I suspect it does, but I also think it is more susceptible to kinking, especially as we have increased the physical therapy of our patients and they move around a lot in bed and in chairs postoperatively. So they now move more, walk more, do more activities. I think you are more likely to get problems there. So I think those are two potential factors for the increased incidence.
DR YANG: My second point addresses the operative procedure itself. Perhaps you can elaborate more on who you would not offer the procedure to and would want to treat conservatively, which you may not want to after hearing the talk. In the occasional patient in whom we see subcutaneous emphysema after lung reduction surgery, as I said, we still use these blowholes, and I say anecdotally, we don't have to do another operation.
In the manuscript you state that you use a single-lumen tube to intubate these patients, first, to make sure that there is no bronchial stump leak. But wouldn't that, based on your mechanism that you propose, increase the subcutaneous air during the induction of the anesthesia? And why create another incision? You state you are making another incision between the thoracotomy site and the chest tubes. You have got two chest tube sites already from your second—
DR CERFOLIO: One chest tube.
DR YANG: I thought these patients had a second chest tube.
DR CERFOLIO: There may be a second bedside chest tube placed, but I almost never use that or the old chest tube site to do the VATS. I make a new clean incision.
DR YANG: Again, so sometimes you could use those holes for your camera site. So why do another chest tube?
DR CERFOLIO: I will answer the second question first. I guess you probably could. I am very much into cosmetics so I don't like to make lots of incisions, but I consider that incision dirty; it has had a tube in it for 3 days. But you are right, I probably could put a camera through there and just another tube through. We haven't done that.
One of the reasons is the diaphragm comes up a little bit after a resection, and I always tell the resident, you know, when a lobe has been removed you have a little diaphragmatic elevation, and I make my chest tube incision very, very low at the time of the first operation and very anterior to decrease pain—the space between the ribs is greatest here and, really, if I put in a camera, I would have to come over the diaphragm. That is the reason I make this new incision higher.
The second reason that I do a single-lumen tube is because I want to do this quick and efficiently. I mean, there are a couple of patients who have massive subcutaneous emphysema and I think you do need to place a double lumen, but if they are not blown up with subcutaneous air, it is easy to intubate them. Then we use a short period of apnea. And I have been impressed with how much VATS you can do with a single-lumen tube. For instance, the patient with interstitial lung disease in the intensive care unit on 100% oxygen, I do VATS lung biopsies all the time on them with a single-lumen tube and just a short period of apnea. So I have gotten very, very comfortable doing VATS with single lumens. Many of my hyperhydrosis patients get a single lumen. It just goes on and on and on. I think that is the reason. I have no problem with using the double lumen.
DR YANG: Okay. So great talk, and again, I thank the Program Committee for the invitation to discuss this.
DR JOSEPH B. ZWISCHENBERGER (Lexington, KY): Cerf, as always, there is a lot to be learned from your presentations, but it appears what you have taught us today is to routinely use two chest tubes after pulmonary resection.
DR CERFOLIO: Zwisch, thanks, your point is a good point. I would say I believe in science, and there is not one but two and maybe three prospective studies done by authors I believe who have shown a single chest tube works as well in their hands as two tubes. So when I come to a meeting like this and I see a study like that, I go back and I change my practice. I really do, and those presentations changed my practice. And as I mentioned yesterday in my lecture in the postgraduate course, honestly, I have been burned a little bit with this increasing subcutaneous emphysema since going to one tube. Maybe I am putting the one tube in the wrong spot, maybe I am doing something else wrong, I don't know. But maybe you are right. And so as I mentioned yesterday in the postgraduate, what I do now, I fill the chest with water, bring the lung up. If I see a big residual space—and I can't do a pleural tent because I have already gone extrapleurally or it is not a lower lobe thing—where I am not going to do a pneumoperitoneum and they got air leaks I can't control, the patient gets two tubes. But this is very rare. I hardly ever use a pleural tent and almost only perform a pneumoperitoneum after a bilobectomy with removal of the right middle and lower lobes. But I use it selectively. If I don't see an air leak in the operating room, the lung is normal, its compliance is good, the DLCO is good, I give them one tube. So I am a selective one-tuber now after a lobectomy. I am not dogmatic about anything, and each patient is different, and we change our protocol based on each patient's characteristics.
DR SHANDA HALEY BLACKMON (Houston, TX): Dr Cerfolio, I was wondering if your VATS pneumolysis patients were also included in your muscle dangle trial, and if so, were they equally distributed among the two groups?
DR CERFOLIO: That is a great question. I don't know the answer to that. I would have to go back and look, to be honest. I don't know. But that is a very interesting question because I wondered if the muscle flap led to more space between the ribs and thus increased the incidence of subcutaneous emphysema. It does not if you close correctly, and if I do not transpose it into the chest to buttress the bronchus or some other structure. If it dangles, it just goes back to its normal place when we close, and you cannot even tell we harvest it. If I cut it and do not transpose it in the chest, I place it back in its normal position in between the ribs. However, when I cut it and put it on a bronchus—as I showed you yesterday with those intraoperative pictures, I don't put the ribs together—those patients may have a much higher incidence of subcutaneous emphysema. I can tell you now that over the last 6 to 9 months, I have been placing a small flat drain over the rib opening and under the serratus that I preserve and leave it in for about 1 or 2 days after surgery to help prevent subcutaneous air. So that is a very good point.
DR JOHN A. HOWINGTON (Cincinnati, IL): So, Cerf, my question would be, you have seen this increased incidence of subcutaneous emphysema and to avoid it you say you put the JP drain. Is that helping you? Are you having a higher incidence of subcutaneous emphysema because you are dangling or cutting the intercostal muscle, or both, and is that the source and not a single chest tube? I am a single chest tube user, and I have not seen that high an incidence of subcutaneous emphysema.
DR CERFOLIO: But maybe you do a better job with your stapler and air leaks than I do or perhaps there are other reasons for your better results.
When we talk about the intercostal muscle, I think one of the risks is subcutaneous emphysema if you transpose the muscle into the chest and close leaving a space between the ribs. A lot people would say no, because when they close, they put the ribs right against one another, and I don't like to do that. I believe they rub and that hurts. I put them back the way God had them initially, just minus the muscle in between them. We have written an abstract for, I think the AATS—wasn't it, Ayesha?—about this exact issue after pneumonectomy, where I always use an intercostal muscle to buttress the bronchus. In that case, I worry about not only air but also fluid coming out of the pneumonectomized space and show that we do a better job with subcutaneous emphysema since using this subcutaneous drain.
DR DANIEL L. MILLER (Atlanta, GA): I think one of the most important aspects about subcutaneous emphysema is that you need to educate the patient and the family, because usually it gets worse before it gets better. Also, I know you do a lot of cases at UAB, but now we know why: you are operating on your patients twice.
DR CERFOLIO: Actually three times, because I do often do a mediastinoscopy under a separate anesthetic as well—that is why my numbers are so artificially inflated and why I will do more than 1,200 operations this year and did more than 1,150 last year.
DR MILLER: I think it all goes back to technique, and the lung is stuck to your intrathoracic incision. So if you do a VATS lobectomy you wouldn't have that problem.
DR CERFOLIO: I disagree, because we get subcutaneous emphysema after VATS procedures as well.
DR MILLER: The big question is, was there a difference in regard to which lobe was operated on, because a lot of times I will use a single tube for a lower lobe with just a right angle, whereas for an upper lobe, the majority of the time I still use two tubes because of superior space issues, and I think it is something to look at in your patients.
Also, in regard to your dangle flap, as we learned about yesterday, at any time has the lung been trapped, in that it did not allow the lung to expand completely. That dangle actually might be a problem.
DR CERFOLIO: No, no. The dangle just hangs down as we do the case. When we finish it, we put it right back to where it was when we started, we just do not crush it with the retractor during spreading. The muscle goes right back to its normal positions, where God had it. Because, remember, we're putting intercostal sutures in, thus the sutures go through the sixth rib, under the intercostal muscle, and then over the top of the fifth rib, and when we close, we bring the muscle right back to where it was. So we are very, very teleologic in terms of the closure. I want to put everything back the way I found it.
DR MILLER: Teleologic?
DR CERFOLIO: Yes, teleologic. You can look it up. It is the right word.
DR MILLER: Is that above or below the dangle?
DR CERFOLIO: Your second question is a great question. I had the same impression, but our analysis did not show a higher problem after upper lobectomy. But that surprised me, because I assumed that they would have. But as usual, the data proved my assumption wrong.
DR RUSSELL R. KRAEGER (St. Louis, MO): I have just two questions for you. In your initial procedure, are you using any sealants at all, because we are and we don't see this incidence that you see. And my second question, on your redo, would you use a sealant or a talc?
DR CERFOLIO: Two good questions. First question, I don't use a sealant, have not in probably 6 or 7 years. There is no FDA-approved sealant for the lung. But some use Tissela—a glue. So I would say to you, what does it cost? How many patients really needed it? Are you sure they are not going to have other problems from this material 20 years down the road? Have you looked at the molecules in Tissela, and so forth? And do you really need it in everybody, is the big question. I mean, that is fine and maybe you are doing a good job, but those are questions to consider. Your second question was?
DR KRAEGER: The use of sealant or talc.
DR CERFOLIO: Well, as I mentioned, I haven't done that, because I still think that this is a problem that we can take care of just by driving the air leak back into the pleural space and managing them with a tube, and I leave that tube in. They go home on an Atrium, one of these little portable devices that fits on your belt. I like that little compact Atrium, and they go home with that. But they buy a tube for a week or two even if they have no air leak, because a lot of them never had an air leak initially because the leaks were not intrapleural, they were leaking into the subcutaneous. They go home on that, on Keflex twice a day for 2 weeks, and then we pull them out in the clinic.
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This article has been cited by other articles:
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  R. J. Cerfolio, D. J. Minnich, and A. S. Bryant The Removal of Chest Tubes Despite an Air Leak or a Pneumothorax. Ann. Thorac. Surg., June 1, 2009; 87(6): 1690 - 1696. [Abstract] [Full Text] [PDF]
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