ATS
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to Personal Folders
Right arrow Download to citation manager
Right arrow Author home page(s):
Richard K. Freeman
Thomas C. Wozniak
Edward B. Fitzgerald
Right arrow Permission Requests
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Freeman, R. K.
Right arrow Articles by Fitzgerald, E. B.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Freeman, R. K.
Right arrow Articles by Fitzgerald, E. B.
Related Collections
Right arrow Diaphragm

Ann Thorac Surg 2006;81:1853-1857
© 2006 The Society of Thoracic Surgeons

Original article: General thoracic

Functional and Physiologic Results of Video-Assisted Thoracoscopic Diaphragm Plication in Adult Patients With Unilateral Diaphragm Paralysis

Richard K. Freeman, MD a , * , Thomas C. Wozniak, MD b , Edward B. Fitzgerald, MD a

a Department of Thoracic and Cardiovascular Surgery, St. Vincent Hospital, Indianapolis, Indiana
b Department of Thoracic and Cardiovascular Surgery, Methodist Hospital, Indianapolis, Indiana

Accepted for publication November 22, 2005.

* Address correspondence to Dr Freeman, 8433 Harcourt Rd, Suite 100, Indianapolis, IN 46260 (Email: rfreeman{at}corvascmds.com).

Presented at the Fifty-first Annual Meeting of the Southern Thoracic Surgical Association, Cancun, Mexico, Nov 2–4, 2004.


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 Discussion
 References
 
BACKGROUND: Plication of the hemidiaphragm for unilateral diaphragm paralysis is infrequently performed in adults. Barriers to diaphragm plication have included the perceived need for thoracotomy and uncertainty of the potential benefits. The purpose of this investigation was to assess the effects of video-assisted thoracoscopic diaphragm plication in symptomatic adult patients with unilateral diaphragm paralysis.

METHODS: Patients with unilateral diaphragm paralysis underwent an evaluation that included a chest radiograph, fluoroscopic sniff test, pulmonary spirometry, and the Medical Research Council (MRC) dyspnea score. Patients with symptomatic unilateral diaphragm paralysis present for at least 6 months were offered video-assisted thoracoscopic diaphragm plication. Patients who underwent diaphragm plication as well as those who declined surgery were reassessed at 6 months with a chest radiograph, spirometry, and the MRC dyspnea score.

RESULTS: Twenty-five patients underwent left (19) or right (6) diaphragm plication through video-assisted thoracoscopic diaphragm plication (22) or thoracotomy (3). There were no operative deaths. Mean hospital length of stay for diaphragm plication was 3.7 days for video-assisted thoracoscopic diaphragm plication and 5.4 days for thoracotomy. After diaphragm plication, mean forced vital capacity, forced expiratory volume at 1 second, functional residual capacity, and total lung capacity improved by 17%, 21.4%, 20.3%, and 16.1%, respectively (p < 005) at 6 months. Mean MRC dyspnea scores also significantly improved in the operative cohort (p < 0001). Seventeen patients in the surgical cohort had returned to work at 6 months. Seven patients treated without surgery displayed a trend toward more frequent hospitalizations and deteriorating pulmonary spirometry and MRC dyspnea scores during the follow-up period.

CONCLUSIONS: Plication of the hemidiaphragm using minimally invasive techniques produced significant improvements in patients' functional status, pulmonary spirometry, and MRC dyspnea scores. Video-assisted thoracoscopic diaphragm plication should be considered appropriate therapy in symptomatic adult patients with unilateral diaphragm paralysis.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 Discussion
 References
 
Plication of the hemidiaphragm is infrequently performed for unilateral diaphragm paralysis in adults despite its successful use in children. Barriers to diaphragm plication have included the lack of attribution of symptoms to unilateral diaphragm paralysis, uncertainty of the potential benefits of plication, the perceived need for thoracotomy, and the paucity of literature pertaining to diaphragm plication in adults. The purpose of this investigation was to assess the subjective and objective effects of video-assisted thoracoscopic diaphragm plication in symptomatic adult patients with unilateral diaphragm paralysis.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 Discussion
 References
 
Patients at least 21 years of age referred to two tertiary care centers for thoracic surgery over a 3-year period for the evaluation of unilateral diaphragm paralysis received informed consent for this investigation (Institutional Review Board approval September 2001). If they agreed to participate, they received a standardized evaluation that included a history and physical examination, a chest radiograph, a fluoroscopic "sniff" test, pulmonary spirometry, and administration of a subjective dyspnea scale, the Medical Research Council (MRC) dyspnea score (Table 1) [1, 2]. Patients without a clear etiology for their unilateral diaphragm paralysis also underwent a neurologic consultation and a computed tomography imaging or magnetic residence imaging study of the brain. All patients referred for unilateral diaphragm paralysis were enrolled in a pulmonary rehabilitation program under the supervision of a pulmonary physician whether they participated in this investigation or not. Excluded from participation in this investigation were patients with an upper motor neuron or malignant etiology for their diaphragm plication, patients with bilateral diaphragm plication, patients with acute respiratory failure or mechanically ventilated patients, and patients with significant comorbid disease who would not likely be candidates for diaphragm plication.


View this table:
[in this window]
[in a new window]
  		Table 1. The Medical Research Council Dyspnea Scale
 
Patients with lifestyle-limiting dyspnea (MRC dyspnea score ≥ 3) from unilateral diaphragm paralysis present for at least 6 months were offered diaphragm plication. When possible, this was performed utilizing video-assisted thoracoscopic techniques, as previously described [3]. When using thoracoscopy, three 10-mm ports were utilized in the midclavicular and midaxillary lines of the eighth intercostals space as well as midway between the spine and the medial border of the scapula in the sixth intercostals space. Whether performing thoracoscopy or a thoracotomy, the uncut hemidiaphragm was plicated with a series of six to eight parallel U stitches using contralateral single lung ventilation. After transecting the inferior pulmonary ligament, sutures were placed beginning medially on the diaphragm and progressing laterally until the hemidiaphragm was nearly flat and taut (Fig 1). If performing the procedure thoracoscopically, the Endostitch (Ethicon Endo-Surgery, Cincinnati, Ohio) was used for intracorporeal suture placement. After surgery, patients' pleural spaces were drained using standard chest tubes. Patients were discharged home at least 24 hours after their chest tubes were removed, when adequate analgesic could be maintained with oral medications and a diet tolerated.


Figure 1
View larger version (28K):
[in this window]
[in a new window]
  		Fig 1. Method of diaphragm plication (video-assisted or thoracotomy).

 
An attempt was made to reassess all patients 6 months after diaphragm plication or their initial assessment in the nonsurgical cohort. Evaluation included a chest radiograph, pulmonary spirometry, administration of the MRC dyspnea score, review of any interim hospitalizations, and assessment of their ability to work.

Statistical Analysis
Continuous data are expressed as the mean plus or minus the standard deviation of the mean except where otherwise indicated. Differences between categorical variables were evaluated by Fisher's exact test. Differences between continuous variables were measured by the two-tailed Student t test. Statistical significance was accepted as p less than 0.05. This investigation was prospectively approved and monitored by our Institutional Review Board.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 Discussion
 References
 
Of the patients referred during the first 4 years of the study period for evaluation of unilateral diaphragm paralysis, 32 met the investigation's entrance criteria and gave consent to participate. All patients were offered diaphragm plication. Seven patients refused surgery but were willing to continue in the follow-up portion of the investigation. Reasons for declining surgery included the desire to avoid surgery (3), the need to care for a disabled family member (2), and the need to geographically relocate (2). Patient demographics as well as the etiologies of diaphragm plication are displayed in Table 2.


View this table:
[in this window]
[in a new window]
  		Table 2. Demographics for Patients Treated With and Without Diaphragm Plication for Unilateral Diaphragm Paralysis
 
Twenty-two patients had diaphragm plication accomplished using video-assisted thoracoscopic techniques, and 3 required conversion to thoracotomy. All 3 of these patients had a body mass index of 30 kg/m2 or greater. Mean length of stay for video-assisted thoracoscopic diaphragm plication and thoracotomy patients was 3.7 and 5.4 days, respectively. One patient in the video-assisted thoracoscopic diaphragm plication group (4%) experienced a superficial wound infection of a port incision. One patient in the thoracotomy group (33%) was found to have a lower extremity deep vein thrombosis after discharge from the hospital. There were no deaths of any patients undergoing diaphragm plication during the follow-up period.

Follow-up was complete in the nonsurgical group. Twenty-four of the 25 patients who underwent diaphragm plication also completed their 6-month assessment. Changes in MRC dyspnea scores, pulmonary spirometry expressed as mean percentages, work status, and pulmonary-related hospitalizations at 3 months are displayed in Table 3 for patients undergoing diaphragm plication. Significant improvements for all values measured except residual volume were seen in patients undergoing diaphragm plication. No patients treated with diaphragm plication required subsequent hospital admission, with 17 of these patients having returned to work at their 6-month assessment.


View this table:
[in this window]
[in a new window]
  		Table 3. Functional Status at Six-Month Follow-Up for Patients Treated With Diaphragm Plication for Unilateral Diaphragm Paralysis
 
Despite continued pulmonary rehabilitation, patients who declined diaphragm plication experienced no significant change in their mean pulmonary spirometry or MRC scores at their 6-month follow-up visit. There was a trend, however, toward worsening of these values. Patients who did not undergo diaphragm plication had an average of 1.3 pulmonary-related hospital admissions at 6-month follow-up. Of the patients who refused surgery, 3 had either not returned to work or had left their job because of dyspnea at their 6-month evaluation.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
Discussion
 References
 
Paralysis of the hemidiaphragm can produce significant alterations in respiratory physiology. These include atalectasis and ventilation/perfusion mismatch, shift of the mobile mediastinum to the contralateral side, worsening of pulmonary spirometry, paradoxical movement of the affected hemidiaphragm, and the preferential redistribution of pulmonary blood flow to the contralateral lungs [4, 5]. The results of these physiologic changes can result in acute respiratory failure requiring mechanical ventilation, more common in the pediatric population, or symptoms of chronic dyspnea, seen more often in adults.

Plication of the hemidiaphragm has become the accepted treatment for pediatric patients with significant respiratory impairment because of unilateral diaphragmatic paralysis [6, 7]. Modern series have found significant improvement in patients' respiratory status after diaphragmatic plication with little associated morbidity. In fact, de Vries and coworkers [8], based on their series of 23 patients, called for the use of diaphragm plication earlier in the course patients with unilateral diaphragm paralysis in an attempt to prevent the long-term effects of diaphragmatic paralysis.

The use of diaphragm plication in the treatment of adult patients with unilateral diaphragm paralysis, however, has remained unusual. This lack of use is likely multifactorial and includes its relative rarity as clinical condition, a failure to recognize the association between patients' symptoms and unilateral diaphragm paralysis, and uncertainty of the potential benefits of diaphragm plication in adults. Other factors contributing to the rare use of diaphragm plication in adult patients likely include the perceived need for thoracotomy, a lack of familiarity with the procedure in adults among surgeons, and the quality of literature discussing diaphragm plication in adults.

Several case reports can be found in which diaphragm plication has been successful in adult patients with unilateral diaphragm paralysis [9–11]. Two published series also exist in which adults were included. The first, by Rebet and associates [12], summarized their results with 13 pediatric and 11 adult patients. Although follow-up was not uniform, they found resolution of dyspnea in 9 of their 10 adult patients operated on for dyspnea with significant improvements in pulmonary spirometry values in some patients [12].

Somanski and colleagues [13] sought to more precisely compare diaphragm plication in an adult and pediatric population. They retrospectively reviewed their experience with 10 pediatric patients and 12 adult patients. They found that diaphragm plication performed in pediatric patients with unilateral diaphragm paralysis for acute respiratory failure resulted in a 70% rate of being separated from mechanical ventilation at median of 4 days. However, only 1 of 4 adult patients with unilateral diaphragm paralysis who underwent diaphragm plication secondary to acute respiratory failure was able to be successfully weaned from the ventilator. In contradistinction, all 7 of the adult patients with unilateral diaphragm paralysis undergoing diaphragm plication for chronic symptoms of dyspnea realized a marked subjective improvement in their dyspnea scale and pulmonary spirometry.

The purpose of this investigation was to assess the subjective and objective outcomes of adult patients undergoing diaphragm plication for chronic dyspnea attributable to unilateral diaphragm paralysis. Primarily of interest was whether diaphragm plication was an appropriate treatment for selected adult patients with dyspnea and unilateral diaphragm paralysis. Subjectively, patients who underwent diaphragm plication realized a mean improvement in their MRC dyspnea score of 1.9. Furthermore, of the 19 patients who had left their jobs because of dyspnea, 17 had returned to work at their 6-month reassessment. Pulmonary spirometry also found significant improvements in mean percent changes in all variables measured except residual volume in these patients.

In comparison, patients who declined diaphragm plication realized no objective or subjective improvement in their dyspnea during the follow-up period. Three patients in the nonsurgical group also accepted disability during the follow-up period and left their jobs. Furthermore, these patients required a mean of 1.3 hospital admissions during the 6-month follow-up period for respiratory illnesses. This finding is in contrast to patients undergoing diaphragm plication, none of whom required admission to the hospital for any reason after surgery.

Also of specific interest in this investigation was whether the potential benefits of decreased hospital length of stay and recovery time found in other minimally invasive thoracic surgical procedures would be realized in patients undergoing diaphragm plication using minimally invasive techniques. Previous reports of video-assisted thoracoscopic diaphragm plication by Van Smith and associates [14], Hwang and associates [15], and Huttl and colleagues [16] found success with a minimally invasive technique in isolated patients. Further encouragement was seen in the report of video-assisted thoracoscopic diaphragm plication performed in 5 children by Hines [17]. This study does not allow comparison of patients undergoing a minimally invasive approach to diaphragm plication to those having a standard plication through thoracotomy. However, the results of objective measures as well as return to work compare favorably with published results of patients undergoing diaphragm plication through thoracotomy [18].

Methods employed in this study not found in other published reports of diaphragm plication in adults include its prospective method, a uniform preoperative evaluation strategy, preferential use of video-assisted thoracoscopic diaphragm plication, the combined use of pulmonary spirometry and an objective dyspnea scale, and the continued assessment of surgical and nonsurgical patients. The use of these techniques was intended to strengthen any conclusions that might be realized from this review. However, two areas of weakness exist in this investigation as currently reported. First, the numbers of patients overall and in two of the treatment subsets are small. This investigation, however, represents both the largest published series of adult patients undergoing diaphragm plication and the largest number of adult patients undergoing video-assisted thoracoscopic diaphragm plication in the medical literature. Secondly, although our investigation continues, the results presented represent follow-up only to the 6-month mark.

In conclusion, this investigation demonstrates that adult patients with chronic dyspnea attributable to unilateral diaphragm paralysis received significant benefits from diaphragm plication. Such benefits include decreased dyspnea as measured by the MRC dyspnea score, improved pulmonary spirometry, a trend toward less frequent respiratory associated hospitalizations, and frequent return to work. Furthermore, video-assisted thoracoscopic diaphragm plication appears to be an effective method of diaphragm plication and is associated with a relatively short hospital length of stay when compared with patients undergoing diaphragm plication through thoracotomy [18]. Based on the results of this investigation, it is recommended that adult patients with unilateral diaphragm paralysis who have symptoms of chronic dyspnea that are lifestyle limiting be evaluated for video-assisted thoracoscopic diaphragm plication.


   Discussion
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Discussion
References
 
DR D. GLENN PENNINGTON (Johnson City, TN): You didn't mention what size ports were used.

DR FREEMAN: We in general for these patients used 10 mm ports, because one of the things that we use is an Endostitch device, which requires a 10 mm port. So in general we would use three 10-mm ports.

DR DANIEL L. MILLER (Atlanta, GA): I enjoyed your presentation. I think it is a very interesting topic that we don't discuss a lot at these meetings. One thing that I think you brought up, a very good point, was in regards to the BMI, and when we do have the larger patients it is almost impossible to do that thorascopically.

One question I have is what is your timing on doing these patients, especially after coronary artery bypass surgery or open heart surgery, because, as you know, recovery may occur at 3 months, 4 months, 6 months, and what is your time period for that?

Secondly, in your technique using the Endostitch, which is not a very deep stitch into the diaphragm, so I think it does cut down your risk of injury to a viscous down below, but I am very concerned that you are only putting two stitches on either side. We usually run the suture continuously back and forth to do that. So I wish you would comment on that. And also too on some of those larger patients you could use CO2. Did you use CO2 on any of your patients?

DR FREEMAN: Thank you, Dr Miller. We in general like to wait at least 6 months before we would pursue plication, and in general I think the medical literature would support that if you are going to get function back, it would usually occur within 6 months. The cartoon may have been a little deceiving. We generally use 6 to 8 U sutures of material, and the Endostitch in these patients I think works out; if you can grasp the diaphragm and pull it up, it is usually fairly loose and you can get full thickness bites, but you do have to elevate it, especially on the left side, to prevent injury to interabdominal viscous. We do not use CO2 routinely.

DR STEPHEN D. CASSIVI (Rochester, MN): I would echo what Dr Miller said. This is a topic that is rarely discussed, but I think it is important. I have two questions. The first is: did you look for paradoxical motion in the diaphragm in order to choose the patients for your surgery? That is the key factor. Whether these patients have diaphragmatic paralysis is what gets them to the door, but what gets them into the operating room should be whether they have true paradoxical breathing. I think that is at least borne out in your abstract where you have observed more left-sided cases than right-sided ones. I think that is one indication that paradoxical breathing is the problem.

My second question is whether you measured inspiratory and expiratory pressures, the so-called bugle pressures. I think these are much more sensitive and actually more specific in terms of getting objective data on whether your operation has done the patient any good or not?

DR FREEMAN: Thank you. Part of our fluoroscopic evaluation preoperatively was certainly to look for paradoxical motion, and that was a strong indication for us. And we did not measure pressures.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 Discussion
 References
 

  1. Bestal JC, Paul EA, Garrod R, Jones PW, Wedzicha JA. Usefulness of the Medical Research Council Dyspnea Scale as a measure of disability in patients with chronic obstructive pulmonary disease Thorax 1999;54:581-586.[Abstract/Free Full Text]
  2. Baddini-Martinez JA, Yamamoto-Martinez T, Lovetro-Galhardo FP, de Castro-Pereira CA. Dyspnea scales as a measure of health-related quality of life in patients with idiopathic pulmonary fibrosis Med Sci Monit 2002;8:405-410.
  3. Gharagozloo F, McReynolds SD, Snyder L. Thoracoscopic plication of the diaphragm Surg Endosc 1995;9:1204-1206.[Medline]
  4. Stevenson JG. Effects of unilateral diaphragm paralysis on branch pulmonary artery flow J Am Soc Echocardiogr 2002;15:1132-1139.[Medline]
  5. Schwartz MZ, Filler RM. Plication of the diaphragm for symptomatic phrenic nerve paralysis J Pediatr Surg 1978;13:259-263.[Medline]
  6. Langer JC, Filler RM, Coles J, Edmonds JF. Plication of the diaphragm for infants and young children with chronic nerve palsy J Pediatr Surg 1988;23:749-751.[Medline]
  7. Kizilcan F, Tanyel FC, Hicsonmez A, Buyukpamukcu N. The long term results of diaphragmatic plication J Pediatr Surg 1993;28:42-44.[Medline]
  8. DeVries TS, Koens BL, Vos A. Surgical eventration caused by phrenic nerve injury in the newborn J Pediatr Surg 1998;33:602-605.[Medline]
  9. Ciccolella DE, Daly BD, Celli BR. Improved diaphragmatic function after surgical plication for unilateral diaphragmatic paralysis Am Rev Respir Dis 1992;146:797-799.[Medline]
  10. Shiraish Y, Miyamoto T, Shimado I, Pak C, Shinkura N, Ohno N. Bilateral diaphragmatic plication for an adult patient J Jpn Assoc Thorac Surg 1991;39:1927-1931.
  11. Stolk J, Versteegh Mim. Long term effects of bilateral plication of the diaphragm?? Chest 2000;117:786-789.[Abstract/Free Full Text]
  12. Ribet M, Linder JL. Plication of the diaphragm for unilateral eventration of paralysis Eur J Cardiothorac Surg 1992;6:1992.
  13. Simansky D, Paley M, Refaely Y, Yellin A. Diaphragm plication following chronic nerve injurya comparison of pediatric and adult patients. Thorax 2002;57:613-616.[Abstract/Free Full Text]
  14. Van Smith C, Jacobs JP, Burke RP. Minimally invasive diaphragmatic plication in an Infant Thorac Surg 1998;65:842-844.[Abstract/Free Full Text]
  15. Hwang Z, Shin JS, Cho YH, Sun K, Lee IS. A simple technique for the thoracoscopic plication of the diaphragm Chest 2003;124:376-378.[Abstract/Free Full Text]
  16. Huttl TP, Meyer G, Geiger TK, Schildberg FW. Indications, techniques and results of laparoscopic surgery for diaphragmatic diseases Zen Chir 2002;127:598-603.
  17. Hines MH. Video-assisted diaphragm plication in children Ann Thorac Surg 2003;76:234-236.[Abstract/Free Full Text]
  18. Wright CD, Williams JG, Oglivie CM, Donnelly RJ. Results of diaphragmatic plication for unilateral diaphragmatic paralysis J Thorac Cardiovasc Surg 1985;90:195-198.[Abstract]



This article has been cited by other articles:


Home page
 Eur. J. Cardiothorac. Surg.Home page
P. Calvinho, C. Bastos, J. E. Bernardo, L. Eugenio, and M. J. Antunes
Diaphragmmatic eventration: long-term follow-up and results of open-chest plicature
Eur. J. Cardiothorac. Surg., November 1, 2009; 36(5): 883 - 887.
[Abstract] [Full Text] [PDF]

Home page
 Ann. Thorac. Surg.Home page
R. K. Freeman, J. Van Woerkom, A. Vyverberg, and A. J. Ascioti
Long-term follow-up of the functional and physiologic results of diaphragm plication in adults with unilateral diaphragm paralysis.
Ann. Thorac. Surg., October 1, 2009; 88(4): 1112 - 1117.
[Abstract] [Full Text] [PDF]

Home page
 MMCTSHome page
M. I. M. Versteegh and A. T. Jouk Tjien
Diaphragm plication in adult patients with diaphragm paralysis
MMCTS, December 17, 2007; 2007(1217): 2568.
[Abstract] [Full Text] [PDF]

Home page
 Eur. J. Cardiothorac. Surg.Home page
M. I.M. Versteegh, J. Braun, P. G. Voigt, D. B. Bosman, J. Stolk, K. F. Rabe, and R. A.E. Dion
Diaphragm plication in adult patients with diaphragm paralysis leads to long-term improvement of pulmonary function and level of dyspnea
Eur. J. Cardiothorac. Surg., September 1, 2007; 32(3): 449 - 456.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to Personal Folders
Right arrow Download to citation manager
Right arrow Author home page(s):
Richard K. Freeman
Thomas C. Wozniak
Edward B. Fitzgerald
Right arrow Permission Requests
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Freeman, R. K.
Right arrow Articles by Fitzgerald, E. B.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Freeman, R. K.
Right arrow Articles by Fitzgerald, E. B.
Related Collections
Right arrow Diaphragm

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
ANN THORAC SURG ASIAN CARDIOVASC THORAC ANN EUR J CARDIOTHORAC SURG
J THORAC CARDIOVASC SURG ICVTS ALL CTSNet JOURNALS