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Ann Thorac Surg 2008;85:1901-1907. doi:10.1016/j.athoracsur.2008.01.041
© 2008 The Society of Thoracic Surgeons

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Original Articles: General Thoracic

A Nondivided Intercostal Muscle Flap Further Reduces Pain of Thoracotomy: A Prospective Randomized Trial

Robert James Cerfolio, MDa,*, Ayesha S. Bryant, MSPH, MDb, Lee M. Maniscalco, BSc

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

Accepted for publication January 11, 2008.

* 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-fourth Annual Meeting of the Southern Thoracic Surgical Association, Bonita Springs, FL, Nov 7–10, 2007.


    Abstract
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 
Background: The pain of thoracotomy may be related to trauma to the intercostal nerves.

Methods: This was a prospective randomized study of 160 patients. All patients had a functioning epidural, similar type and size thoracotomy, an intercostal muscle flap (ICM) harvested before rib spreading, inferior rib drilling, and postoperative pain management. In one group, the ICM was left intact distally and it dangled (D group); the ICM in the other was cut distally (C group). Pain was assessed using multiple pain scores. Outcomes assessed were qualitative and quantitative pain scores, number of ribs broken, spirometric values, analgesic use, and return to baseline activity for postoperative days 1 to 5 and weeks 2, 3, 4, 8, and 12.

Results: The D group had 85 patients and the C group, 75. The groups had similar demographics, types of procedures, and histology. Intrahospital pain scores were similar; however, at postoperative weeks 3, 4, 8, and 12, the D group had significantly lower mean numeric pain scores and was using fewer analgesics (p < 0.05 for all). At 12 weeks, patients in the D group were more likely to have returned to baseline activity (p = 0.002).

Conclusions: An ICM flap reduces pain. Harvesting and then leaving the ICM flap intact instead of cutting it before rib spreading further reduced thoracotomy pain. This technique, when added to rib drilling, leads to reduced pain on postoperative weeks 3 to 12, to quicker return to baseline activity, and lessens the need for analgesics.


    Introduction
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 
Posterior lateral thoracotomy is frequently performed and remains quite painful. Studies have shown that chronic pain, defined as pain after 6 months, is common and can occur in up to 67% of patients who have had a thoracotomy [1–4]. During the past 4 years, we have studied the problem of pain from thoracotomy in several prospective trials, and although some techniques have failed to reduce pain [5], some have been successful. We postulated that most of the pain was from trauma to the intercostal nerves [6, 7].

In 2003 we reported a prospective study that showed that sutures placed through the ribs (intracostal sutures) decreased the pain compared with sutures that go around the ribs (paracostal sutures) during thoracotomy closure [8]. D'Andrilli and colleagues [9] in 2006 showed in a prospective study that the preemptive injection of a local anesthetic before rib spreading, but after incision to ensure proper injection in the intercostal muscle (ICM), also reduces pain.

In 2005 we reported [10] another prospective randomized study that showed that the harvesting of an ICM flap before rib spreading to avoid the ICM and the intercostal nerve that runs in it from being crushed by the retractor also reduced pain. In that study, the ICM was harvested, as shown in Figure 1, and was cut distally and reflected posteriorly so as not to obstruct the surgeon's view during the operation.


Figure 1
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Fig 1. Drawings show the technique of creating an intracostal muscle (ICM) flap. The middle panel shows the group with the ICM cut ("C group"), and the right panel shows the ICM dangling ("D group").

 
All patients in our current study underwent ICM harvest before rib spreading. In half of the patients, however, the ICM and the intercostal nerve that runs in it were left intact distally and in the other half, the muscle was cut and reflected posteriorly, as we had been doing previously. The two different techniques are shown in Figure 1, and the results of this randomized study are presented.


    Material and Methods
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 
Between June 2005 and May 2006, all asymptomatic patients who were to undergo a posterior lateral thoracotomy for an indeterminate pulmonary nodule or for a biopsy-proven non-small cell lung cancer performed by one general thoracic surgeon (R.J.C.) at the University of Alabama in Birmingham (UAB) were eligible for this trial.

Patients were excluded if they presented with any type of pain, had a history of chronic pain syndrome, methadone or other narcotic use, psychiatric illness, had radiologic evidence of parietal pleural or rib invasion, or a history of opiate or steroid use 6 months before the operation. All of these patients were excluded because they had pain before the operation. Also excluded were patients who had had a previous thoracotomy, had received neoadjuvant therapy, or refused entry into the trial. If sleeve lobectomy or pneumonectomy was performed, or previous radiation given, patients were excluded because the intercostal flap muscle had been divided and used to cover the bronchi and thus these patients could not be randomized. Finally, patients aged younger than 19 years were also excluded.

Careful preoperative assessment, including pulmonary function tests, computed tomography (CT), and positron emission tomography (PET) were performed in all patients along with the selective use of cardiac stress tests as previously described at length [11]. Patients who met the enrollment criteria were randomly assigned the day of surgery to either the dangling (D group) muscle flap technique or the cut (C group) intercostal muscle technique. Only the surgeon and some of the surgical team were aware of the patients' assignment. Office staff that was responsible for surveying patients, performing data entry, and performing phone surveys was blinded, as were the patients. The Institutional Review Board of the UAB approved this study, along with the prospective database used concomitantly. Patient consent was obtained for entry into the study and into the database.

Intraoperative Technique
An epidural was placed in all patients preoperatively. If the epidural was deemed to be nonfunctional at any time postoperatively by the pain service, the patient was eliminated from the study. Patients were also eliminated if they had significant complications such as confusion, transfer to the intensive care unit, or required intubation that precluded them from participating in the study. Patients who had prolonged air leaks and were sent home with a chest tube in place connected to a Heimlich valve or connected to a water seal device were also excluded.

All openings and closings were performed by one surgeon, with assistance from various cardiothoracic fellows and general surgical residents. All skin incisions were the length of the posterior half of the latissimus dorsi muscle. The posterior half of the latissimus dorsi was cut, and the entire serratus anterior muscle was preserved. Once the sixth rib was identified, the intercostal muscle above it as well as two intercostal muscle bundles above and two below were all injected with 0.25% Marcaine (Abbott Labs, North Chicago IL) with epinephrine. The maximum dose of Marcaine was calculated by body weight (3.0 mg/kg), and 50% of this dose was drawn into a syringe. It was then injected evenly into the 5 intercostal muscles using an 18-guage needle. The chest was entered over the top of the sixth rib in all patients. The rib was not cut or shingled intentionally. At this point, the surgeon was made aware of which group the patient had been randomized into and the appropriate procedure was performed.

The fifth ICM was harvested off of the inferior edge of the fifth rib by use of a cautery. The cautery setting was 70 for the entire case. The muscle was deflected downward with a forceps and the cautery was quickly moved under the inferior surface of the rib to avoid thermal injury to the ICM neurovascular bundle and to maintain the viability of the flap so it could be used later to cover or buttress the bronchi after lobectomy, as shown in Figure 1. The ICM was taken down off most of the rib. In the C group, it was then cut distally just under just under the serratus anterior muscle and reflected posteriorly. In the D group, it was kept intact and dangled under the retractor after it was placed. It was later suspended in a small soft drain during the operation so it did obstruct the surgeon's view of the upper chest.

We attempted to avoid rib fracture by slowly opening the chest retractor. If rib fracture did occur, we resected a small 1- to 2-cm piece of rib to prevent the two ends from rubbing against one another.

After completion of the appropriate pulmonary resection and thoracic lymphadenectomy, the suspending drain was removed from the ICM and it was placed back in its normal anatomic position. One 28F soft chest tube was placed. Intracostal sutures were used for all closures.

Patients in this series received identical postoperative pain regimens. Ketorolac tromethamine (Toradol, Nutley, NJ) was given to all patients in the recovery room and daily until postoperative day 2. Intravenous morphine was used for breakthrough pain. Epidurals were removed on the morning of postoperative day 2 in almost all patients, and patients were started on oxycodone and acetaminophen (Tylox, McNeil Pharmaceuticals, Springhouse, PA). Members of the pain service who managed the epidural and the nurses on our team, nurses on the floor, and the data collectors were all blinded to patient randomization assignment.

Pain Score Assessment
The numeric rating scale (NRS) [12] and visual pain score (VPS) [13] were used for patients while hospitalized. Patients were interviewed daily between 4 PM and 9 PM by one blinded data collector who used the same script each day. Patients usually received oral analgesics between 2 PM and 6 PM. The amount of pain medicine used was also recorded. In-hospital complications were noted, and chest roentgenograms were performed daily.

Once discharged, the VPS score was not used; however, the NRS with other quality-of-life questions were used. One of 2 interviewers called patients at home and used a standard outpatient script to assess their pain. The calls were made between 1 PM and 5 PM at postoperative weeks 2, 4, 8, and 12. If patients returned for a 3-week postoperative check in the clinic, a numeric pain score was recorded using the same script as in the hospital.

During postoperative weeks 4, 8, and 12, patients were asked if they had returned to their baseline activities. Baseline activities were defined as those activities of daily living in which the patient routinely participated preoperatively, such as cooking, cleaning, showering, and gardening.

Statistical Analysis
A power analysis performed before the study commenced indicated that 150 patients (75 patients in each group) were needed. The power analysis was based on previous studies and indicated a sample sizes of 75 in each group would provide 90% power ({alpha} = 0.05, β = 0.1). An interim analysis was planned after approximately 50 patients were enrolled in each group. Data for all patients who were randomly assigned to a group were analyzed on an intention-to-treat basis. Given the need to randomize patients before operation in this study, patients who were unable to answer the pain survey each day because of confusion or intubation (or other reasons) were excluded from the study and any analysis.

For the analysis of differences between groups, we used two-tailed t tests or nonparametric tests if the results were not normally distributed. The Fisher exact test or {chi}2 test was used to compare proportions. An analysis of variance for repeated measurements was performed to compare the pain scores for the two groups. Time to the resumption of normal activity (ie, percentages for categoric variables) was analyzed with Kaplan-Meier survival curves, and differences between the two treatment groups were compared by the log-rank test. A two-sided value of p < 0.05 was considered to represent a statistically significant difference between two groups unlikely due to chance.


    Results
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 
Between June 2005 and May 2006, 753 patients underwent a surgical procedure by one general thoracic surgeon. A thoracotomy for pulmonary resection was done in 263 patients. The study randomized 167 of these patients and 160 completed the study. Reasons for dropout were immediate postoperative transfer to the ICU in 3 patients, malfunctioning epidural in 2, need to perform chest wall reconstruction in 1, and a history of narcotic abuse that was not initially disclosed at time of screening in 1 patient. No statistically significant differences were found between randomization groups for the previously identified demographic characteristics that have been shown to affect pain perception or reporting, or both (Table 1).


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Table 1 Patient Characteristics and Pathology Stratified by Randomization Group a
 
The mean time to perform the ICM flap was 45 seconds, which was significantly shorter than the 3.7 minutes in our previously reported experience in 2003. Although 10 patients in the C group had broken ribs compared with 6 patients in the D group, this increased incidence was not statistically significant. The median length of stay was 4.0 days in the D group compared with 4.4 days the C group, but this difference did not reach statistical significance (p = 0.081).

Table 2 reports the outcomes for postoperative days (PODs) 1 through 5. Patients in the D group had significantly lower numeric (2.14 vs 2.69, p = 0.035) and visual pain scores (1.30 vs 2.15, p = 0.014) on POD 2; however, no other significant differences between the two groups were noted. Almost all patients in both groups were ambulatory and all had their epidural removed by POD 2. The two groups used a similar amount of pain medicine while in the hospital.


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Table 2 In-Hospital Pain Assessment for the Randomized Groups During the Hospitalization
 
Hospital complications are summarized in Table 3. The C group patients had increased morbidity (37%) compared with the D group (24%); however, this difference did not achieve statistical significance (p = 0.084). A similar trend were seen for operative death, at 6 patients in the C group vs 3 patients in the D group (p = 0.377).


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Table 3 In-Hospital Morbidity Stratified by Randomized Group
 
Patients randomized to the D group had a lower numeric pain score at postoperative weeks 3, 4, 8, and 12 compared with the C group (Table 4). Fewer patients in the D group used prescription pain medications compared with the C group at 4, 8, and 12 weeks postoperatively.


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Table 4 Outpatient Postoperative Assessment Stratified by Randomization Group
 
No significant difference was observed in the number of patients readmitted within 30 days after operation or the number of patients who received adjuvant therapy. At 12 weeks postoperatively, the D group patients were more likely to have returned to their baseline activity (89%) compared with the C group patients (74%, p = 0.002).


    Comment
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 
Acute and chronic pain remains one of the most common problems after thoracotomy, and thus we have performed several prospective studies to identify ways to reduce it. Video-assisted thoracoscopic surgery (VATS) is an increasingly used technique that may also reduce pain, but still few pulmonary resections in the United States are performed in this manner. Although we believe more and more operations will be performed using VATS techniques, a certain percentage may not be able to be performed in this manner and some data suggest that lung palpation may be preferred for patients with cancer [14]. Thoracotomy will thus probably remain a common procedure for general thoracic surgeons even in the foreseeable future.

In this prospective randomized trial, we have shown that the addition of third technique to the other two techniques we have previously described [8, 10] further reduces the pain of thoracotomy. We found that the harvesting of an ICM flap and then leaving the flap intact distally and not cutting it—and thus the intercostal nerve that runs in it—may further reduce postoperative thoracotomy pain. The strengths of this study include not only some of the techniques that we have featured in our previous studies (including one surgeon, the use a pain script, the timing of the pain assessment, and objective pain scores) but also some improvements. For example, in this series we excluded patients who had received neoadjuvant therapy to exclude interaction and confounding factors, we clarified the language in our pain survey script to avoid ambiguity, such as in place of "narcotic" we used "prescription," we more definitively described "return to baseline activities," and we obtained data on POD 5. The limitations of this study however remain the same as our other studies and revolve around the inherently subjective nature of pain.

In 2005 we showed that harvesting an ICM resulted in more broken ribs. This may be due to the upper rib being less protected after the muscle has been removed from it. However, this was not associated with increased pain, and this is probably because when we close the chest in a patient who has sustained a broken rib, we ensure the two edges do not rub against one another by removing a small piece. In this study, we found more ribs were broken in the divided group than the dangle group.

The dangle technique obviously does not allow for the ICM to be transposed into the chest, and thus we do not recommend it for patients who have an indication for bronchial or esophageal buttressing. This includes patients who have had preoperative radiation, chemotherapy, and those who are immunocompromised; therefore, its only advantage is for the reduction of pain.

We used very strict entry criteria to ensure that other factors did not affect our results and thus eliminated a large number of patients, but this was only done to ensure the study's accuracy. In our practice, however, we do use a dangling ICM for most all patients, including those who undergo redo thoracotomy or for patients who are on methadone therapy preoperatively. It is part of our routine regimen for any posterior lateral thoracotomy unless the ICM is needed inside the chest. We usually only harvest the muscle the length of the retractor's blades to ensure the ICM nerve is not crushed by the chest retractor. We prefer to keep the cautery setting on 70 throughout the case and during ICM harvesting because we believe the operation is more efficient this way. If the cautery is swiftly passed under the rib, there does not seem to be thermal injury to the underlying muscle and nerve. The harvesting of the ICM only takes 30 to 45 seconds. However, setting the cautery level lower may be needed if harvesting is not done with alacrity.

If an osteal elevator is used to harvest the ICM, osteoclasts will remain on the muscle and the flap may calcify. Although some believe this is a problem with the ICM, if the flap is used to buttress a closed bronchus such as after lobectomy or pneumonectomy, calcification may be a desired characteristic. However, if the ICM is used to wrap part of (we never recommend 360° wrapping of anything with any flap) a sleeve resection of the pulmonary artery or the bronchus, then calcification over time may represent a problem. For this reason, we prefer the use of cautery to harvest the ICM and with this technique the flap does not calcify over time [15].

In conclusion, we have shown that the harvesting of an ICM flap and leaving the muscle intact so it dangles under the chest retractor leads to the further reduction of the pain of thoracotomy. When the ICM is needed to cover an irradiated bronchus or to repair a perforated esophagus, we still recommend its use and that, of course, requires distal division for transposition to the area in the chest that requires buttressing. In a standard thoracotomy, however, we recommend harvesting the muscle before rib spreading, leaving the muscle intact distally, and allowing it to dangle. Patients who undergo this technique have less pain, and when added to rib drilling, these techniques together lead to reduced pain during postoperative weeks 3 to 12, reduce the need for prescription analgesics, and lead to a quicker return to baseline activity.

Pain, like any other postoperative complication, is best treated by prevention. Acute pain control helps prevent chronic pain syndrome [4]. Thus, future studies should examine other, easily reproducible and inexpensive ways to reduce the pain of thoracotomy or VATS, such as drilling holes in the bottom rib, injecting local anesthetic in the nerves before chest retraction, and the harvesting and not cutting of an ICM flap.


    Discussion
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 
DR DANIEL L. MILLER (Atlanta, GA): Well, Cerf, again, I applaud you on your prospective studies. This is the fourth in the pain series. You had four in the air leak series. I know your IRB office is probably right next door to yours at UAB, and they are painful when you get another study.

But the big thing here, I think you have shown that it is very important that the surgeon gets involved in the operating room to look at the issue of pain, because the majority of the time, 75% of the calls that we get in the office, and I am sure the majority of the rest of the surgeons in the room, it is in regards to pain, and that is a major, major issue, and it takes up a lot of time, and a lot of nursing help to do that.

I think one of the things that I am concerned with here is, first of all, you are doing all these preemptive things, but the one thing that you are not doing, you put a rib spreader in and you spread at will. You do not shingle a rib. In this study, 10% of your patients had broken ribs just from the rib spreader. So I think with all these special maneuvers that you are doing, you are still just cranking away. I am a shingle man. You were taught how to shingle at the beginning. You have gotten away from that.

DR CERFOLIO: I got away from it because it was worse, but go ahead.

DR MILLER: I think that is an issue that you need to look at. I think the big thing, too, in all this is in regards to late postthoracotomy pain syndrome at a year, because a lot of times we had a lot of patients who had neuroma formations and so forth. Because when you take your "dangle" down, or whatever it is called, if you do a Google search and pull up "dangle," there is no association with a muscle at all, number two is with fishing, which Bill Cook would appreciate that, and number one is with Viagra, but we won't go into that.

DR CERFOLIO: That is another problem.

DR MILLER: Yes, that is another problem. But the big thing is what happens at a year. And also, too, when you take the muscle down, you are using electrocautery, and if you are preserving that nerve you may be causing damage to that nerve to have neuroma formation. As our older colleagues would teach us, a takedown from a periosteal elevator or so forth is another way to do that. Loved the study, but the big thing is in regards to late pain and your technique and rib spreading.

DR CERFOLIO: Dan, thanks and it is always an honor for me to have you discuss my stuff. First, we do not crank the retractor at will; in fact, we do quite the opposite. I slowly open the retractor, and if you do that you usually do not break a rib. If you look at all of the data on all of my series combined, you will see that about 10% to 15% of patients get a broken rib. When we break, a rib they are usually in elderly women or thin men. When a fractures occur, it usually is anterior, much more anteriorly positioned than when you shingle, which is in the back. Here, anteriorly where the ribs are further apart when you remove the small piece of rib to prevent rubbing, you are less likely to injure the artery. If you injure the artery, you have to Bovie (Bovie Medical Corp, St Petersburg, FL) it and that can hurt the nerve. So I got smart and stopped shingle in 1998.

Second, you question the Bovie setting on 70. I do the whole case on 70. As you know, I go very quickly and when I harvest the intercostal muscle, if I was injuring the nerve, the pain scores would be higher not lower. Some people want to turn the Bovie down to 40. You could do that; you could turn the Bovie down. I feel comfortable leaving it on 70, and it takes literally 30 to 35 seconds to take the whole thing down. It is a piece of cake. For some surgeons, I think you are right: they will be less likely to injure the nerve with it set on 30.

Number 3, you asked about have we eliminated pain completely. No we have not. In the second study we wrote, I have a sentence in that paper that we had eliminated postthoracotomy pain syndrome, which means no pain at 6 months. That was true at that time, but it is not true now. I now know of at least 7 or 8 patients in my practice who have complained on follow-up appointments or appointments for other reasons about some mild pain, who got the muscle flap, who got the drilling. I still have a few patients that have some pain after 6 months. But it is very, very few, less than 1%. We tell our patients at 3 weeks post-op that they can go back to golf, tennis, sexual activity, anything they want to do; God bless them, 3 weeks after thoracotomy.

DR MILLER: But your technique of the dangle, you could actually shingle up instead of shingling down.

DR CERFOLIO: No. The rib is not shingled. I just take the intercostal muscle off the rib. The rib is left alone. It is a rib-sparing procedure. And I market it. The way you market your VATS lobectomy, I market a rib-sparing, nerve-sparing procedure, and part of this is marketing.

DR MILLER: Well, the bottom line is think VATS lobectomy.

DR CERFOLIO: When I can palpate the other lobes with the VATS, I am happy to do consider it. For benign disease, I think VATS lobectomy is fine and it may be fine for cancer as well. I prefer to be able to palpate the rest of the lung.


    Acknowledgments
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 
The authors thank Steven Goldberg for the illustrations.


    References
 Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Discussion
 Acknowledgments
 References
 

  1. Kalso E, Perttunen K, Kassinen S. Pain after thoracic surgery Acta Anaesthesiol Scand 1992;36:96-100.[Medline]
  2. Matsunaga M, Dan K, Manable FY, et al. Residual pain of 90 thoracotomy patients with malignancy and non-malignancy Pain 1990(Suppl 5):S148.
  3. Kanner RM, Martini N, Foley KM. Nature and incidence of post-thoracotomy pain Proc Am Soc Clin Oncol 1982;1:152.
  4. Katz J, Jackson M, Kavanagh BP, Sandler AN. Acute pain after thoracic surgery predicts long-term post-thoracotomy pain Clin J Pain 1996;12:50-55.[Medline]
  5. Cerfolio RJ, Bryant AS, Bass CS, Bartolucci AA. A prospective, double-blinded, randomized trial evaluating the use of preemptive analgesia of the skin before thoracotomy Ann Thorac Surg 2003;76:1055-1058.[Abstract/Free Full Text]
  6. Toledo-Pereyra LH, Demeester TR. Prospective randomized evaluation of intrathoracic intercostals nerve block with bupivacaine on postoperative ventilatory function Ann Thorac Surg 1979;27:203-205.[Abstract]
  7. Hazelrigg SR, Landreneau RJ, Boley TM, et al. The effect of muscle sparing versus posterolateral thoracotomy on pulmonary function, muscle strength, and postoperative pain J Thorac Cardiovasc Surg 1991;101:394-401.[Abstract]
  8. Cerfolio RJ, Price TN, Bryant AS, Sale Bass C, Bartolucci AA. Intracostal sutures decrease the pain of thoracotomy Ann Thorac Surg 2003;76:407-411.[Abstract/Free Full Text]
  9. D'Andrilli A, Ibrahim M, Ciccone AM, et al. Intrapleural intercostal nerve block associated with mini-thoracotomy improves pain control after major lung resection Eur J Cardiothor Surg 2006;29:790-794.[Abstract/Free Full Text]
  10. Cerfolio RJ, Bryant AS, Patel B, Bartolucci AA. Intercostal muscle flap reduces the pain of thoracotomy. A prospective randomized trial. J Thorac Cardiovasc Surg 2005;130:987-993.[Abstract/Free Full Text]
  11. Cerfolio RJ, Bryant AS, Ojha B, Eloubeidi M. Improving the inaccuracies of clinical staging of patients with NSCLC: a prospective trial Ann Thorac Surg 2005;80:1207-1213.[Abstract/Free Full Text]
  12. Downie WW, Leatham PA, Rhind VM, Wright V, Branco JA, Anderson JA. Studies with pain rating scales Ann Rheum Dis 1978;37:378-381.[Abstract/Free Full Text]
  13. Wong D. Whaley & Wong's essentials of pediatric nursing5th ed.. New York, NY: Mosby-Year Book Inc; 1997. pp. 1215.
  14. Cerfolio RJ, Bryant AS. Is palpation of the non-resected pulmonary lobe(s) required for patients with non-small cell lung cancer?. A prospective study. J Thorac Cardiovasc Surg 2008;135:261-268.[Abstract/Free Full Text]
  15. Cerfolio RJ, Bryant AS, Yamamuro M. Intercostal muscle flap to buttress the bronchus at risk and the thoracic esophageal–gastric anastomosis Ann Thorac Surg 2005;80:1017-1020.[Abstract/Free Full Text]



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