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Original Articles: General Thoracic

Ipsilateral Diaphragmatic Motion and Lung Function in Long-Term Pneumonectomy Patients

^a Department of Thoracic Surgery, Université Laval, Québec, Canada
^b Department of Radiology, Université Laval, Québec, Canada
^c Department of Pneumology, Université Laval, Québec, Canada
^d Institut Universitaire de Cardiologie et de Pneumologie, Université Laval, Québec, Canada

Accepted for publication May 15, 2008.

^_* Address correspondence to Dr Deslauriers, Institut de Cardiologie et de Pneumologie de l'Université Laval, Hôpital Laval, 2725 chemin Ste-Foy, Québec, P Québec, G1V 4G5, Canada (Email: jean.deslauriers{at}chg.ulaval.ca).

Presented at the Forty-fourth Annual Meeting of The Society of Thoracic Surgeons, Fort Lauderdale, FL, Jan 28–30, 2008.

	Abstract

Top Abstract Introduction Patients and Methods Results Comment Discussion Acknowledgments References

 
Background: The physiologic advantages of preserving phrenic nerve integrity and normal diaphragmatic motion (DM) during the course of pnemonectomy are incompletely understood. This study was conducted to investigate potential benefits of this strategy on postoperative lung function.

Methods: Among 523 consecutive patients who underwent pneumonectomy for lung cancer between January 1992 and September 2001, 117 were alive at the time of study (March to December 2006) and thus had 5 years' minimum follow-up. Of those, 17 were excluded and 12 could not have magnetic resonance imaging (MRI), leaving 88 patients available for study. Diaphragmatic motion was assessed by MRI during deep breathing, and patients were classified as having normal and synchronous diaphragmatic motion (n = 44) or abnormal diaphragmatic motion (immobile or paradoxical, n = 44). These findings were correlated with expiratory volume measurements, gas exchange (arterial blood gases), and exercise tolerance (6-minute walk test).

Results: The mean follow-up time was 9.3 years. Patients with abnormal DM were younger than patients with normal DM and were more likely to have had a right or an extended pneumonectomy (p < 0.01). Despite comparable preoperative lung function, patients with abnormal DM had significantly worse postoperative lung volumes (forced expiratory voume in 1 second, forced vital capacity, lung diffusion capacity for carbon monoxide; p < 0.01) and exercise capacity (6-minute walk test, percent predicted, p < 0.05) than patients with normal DM.

Conclusions: Because the long-term effects of a paralyzed hemidiaphragm in pneumonectomy patients are characterized by significant alterations in lung function, all surgeons doing this type of work should take every precaution to avoid technical errors that could lead to phrenic nerve injury or interruption.

	Introduction

Top Abstract Introduction Patients and Methods Results Comment Discussion Acknowledgments References

 
Despite the increasing role of limited resections such as standard or bronchoplastic lobectomies, pneumonectomy is required in approximately 15% to 20% of patients undergoing surgical resection of primary lung cancer [1]. This procedure is, however, associated with higher risks of 30-day operative mortality [2] and significantly worse alterations in residual lung function. Indeed, several studies [3–6] have shown decreased expiratory lung volumes ranging from 25% to 40% of predicted values depending on preoperative function, age at the time of pneumonectomy, and which lung had been removed. It is also likely that anatomic factors such as compensatory hyperinflation of the residual lung [6], and function of the ipsilateral hemidiaphragm have an effect on postpneumonectomy lung function.

The long-term pneumonectomy space is characterized by ipsilateral mediastinal shift, contraction of the intercostal spaces, and elevation of the hemidiaphragm [7]. Whether this hemidiaphragm is mobile and functional and whether diaphragmatic motion correlates with objective determinants of lung function is incompletely understood and has never been studied, even if some authors [8] have suggested that in total space obliteration, the hemidiaphragm remains fixed above the fourth rib.

This study was designed to test the hypothesis that intraoperative phrenic nerve injury during the course of pneumonectomy with secondary loss of diaphragmatic motion as assessed by dynamic magnetic resonance imaging (MRI) may be associated with more significant long-term alterations of pulmonary function than if the phrenic nerve had been preserved.

	Patients and Methods

Top Abstract Introduction Patients and Methods Results Comment Discussion Acknowledgments References

 
Study Population and Patient Selection
Among 523 consecutive patients who underwent pneumonectomy for lung cancer between January 1992 and September 2001, 117 were still alive at the time of the study (March to December 2006) and thus had 5-year minimum follow-up. Twenty-nine patients were excluded because of a contraindication to MRI (n = 12), cognitive deficit (n = 5), cancer recurrence (n = 5), or for other reasons (n = 7), leaving 88 patients available for study. The protocol received approval from the Hospital Institutional Review Board, and written consent was obtained from all patients.

Patient Evaluation
Over a 1-day period, each patient underwent complete medical history and physical examination, standard posteroanterior and lateral chest radiographs, thoracic MRI, pulmonary function tests, arterial blood gas analysis, and 6-minute walk test.

Magnetic Resonance Imaging and Assessment of Diaphragmatic Motion
The studies were performed in a 1.5T MR system (Intera 1.5T; Philips Medical Systems, Best, Netherlands), using a cardiac 5-channel coil for certain sequences and with the body coil for the dynamic sequences. The study comprised T1 TSE black blood axial and coronal cardiac-gated images (field of view approximately 35 cm, 5-mm gap; 256 acquired matrix, 512 3-D reconstruction matrix; TR approximately 700 ms; TE approximately 9 ms; TSE factor 20; SENSE (sensitivity encoding) parallel imaging factor 1,7; 2 NSA (number of signal averages), 13-s breath hold). Dynamic evaluation of the diaphragms was performed in a coronal or coronal-oblique plane through top of the diaphragms, also with a balanced-FFE (fast filed echo) single-shot sequence. A 40- to 60-s acquisition was obtained, to obtain between 5 and 8 full respiratory cycles (field of view approximately 35 cm; 10-mm thickness; 96 acquired matrix, 128 3-D reconstruction matrix; TR/T = shortest, typically 1.98/0.99 ms; flip 50 degrees; 0.105-s image acquisition time). The level of acquisition was determined by interactive real-time positioning. Before starting the acquisition, the patient was instructed and coached to inhale as rapidly as possible, then to exhale after a 2- to 3-s wait before repeating the cycle until acquisition stopped. Because of the advances of MR equipment used, this method differs significantly from that proposed by Gierada and colleagues in 1995 [9], and as used by Takazukura and associates [10] more recently.

The images were processed on a dedicated analysis workstation (ViewForum; Philips, Best, Netherlands). Cine loops of the acquired sequence were evaluated. Diaphragmatic excursion was evaluated by visual inspection of the line loops and by calculating the difference in distance from a fixed point at the apex to the highest points of both hemidiphragms, at the maximum inspiration and functional residual capacity, using the same temporal frame for both sides.

Diaphragmatic motion of the postpneumonectomy side was characterized as normal or paralyzed. Motion of this diaphragm was defined as normal when the distance from the fixed point at the apex increased between the frame at functional residual capacity and the one at end inspiration. Conversely, immobile diaphragms or diaphragms with paradoxic movement were defined as paralyzed diaphragms. Paradoxic motion implied elevation of the affected diaphragm, without concurrent equivalent elevation of the ribs adjacent to the diaphragm. Using the same criteria, four independent evaluations were performed by three radiologists (S.M., M.Q., L.C.) and one thoracic surgeon (P.U.). Differences were discussed by the entire group to reach a consensus. Arbitration by the senior radiologist was required in the 2 cases where a consensus could not be reached.

Assessment of Hyperinflation of the Residual Lung
Posteroanterior chest radiography was performed to objectively assess controlateral lung hyperinflation. A horizontal straight line was drawn from the middle of the spine toward the chest wall at the level of maximal controlateral lung hyperinflation. The importance of hyperinflation was defined as the ratio of the maximal distance from the middle of the spine to the extremity of the lung hyperinflation over the maximal distance from the middle of the spine to the chest wall. These evaluations were performed independently by one radiologist (S.F.) and one thoracic surgeon (P.U.), and obtained values were averaged out. In case of discordant values of more than 5%, a second radiologist (S.M.) arbitrated to reach an agreement.

Pulmonary Function Studies, Blood Gas Analysis, and 6-Minute Walk Test
Lung volumes were measured by phlethysmography using a constant-volume chamber, and carbon monoxide diffusing capacity was measured by single-breath method (Vmax Spectra 22D; SensorMedics, Yorba Linda, California). All measurements were performed according to European Respiratory Society recommendations [11, 12]. Individual results were compared to the predicted values [13, 14]. Preoperative pulmonary function tests data were recorded from patients'medical records. Arterial blood gases from the radial artery were obtained at rest with the subject in the seated position after 10 minutes of rest and with no oxygen and were immediately analyzed. A nonencouraged 6-minute walk test was performed according to the American Thoracic Society recommendations [15]. Individual 6-minute walked distances were compared to the predicted values [16].

Statistical Analysis
Qualitative data are presented as percentages, and quantitative data as mean ± SD. Differences in proportions were tested with the ² test, and continuous variables were compared with the one-way analysis of variance. The univariate normality assumptions were verified with the Shapiro-Wilk test, and the Brown and Forsythe variation of Levene's test statistics was used to verify the homogeneity of variances. Univariate regression approach was performed to find predictors of residual long-term lung function after pneumonectomy for lung cancer. The first stage was to perform generalized additive models separately for each of the predictor variables, as there was no a priori reason for using a particular model, and this approach may suggest the appropriate functional form between the dependent variable (forced expiratory volume in 1 second [FEV₁], %) and the independent variables. After investigation, for all variables, the linear models were retained to relate the response variable to the explanatory variables. The next stage was to use a stepwise selection strategy with different combinations of predictors in the model to see if there was significant difference in the goodness of fit. The variables with an univariate association with lung function (p < 0.20) were candidates in the multivariate model building. The same approach was used to add interaction terms into the statistical model. The results were considered significant with p values of 0.05 or less. The data were analyzed using the statistical package program SAS version 9.1.3. (SAS Institute, Cary, North Carolina).

	Results

Top Abstract Introduction Patients and Methods Results Comment Discussion Acknowledgments References

 
Baseline characteristics of the study population are shown in Table 1. The mean age of the 88 patients at the time of study was 68 ± 10 years (range, 35 to 89), and there were 66 female and 22 male patients. Mean preoperative values for FEV₁, forced vital capacity (FVC), and carbon monoxide diffusing capacity (DLCO) were all within 80% to 85% of predicted values for age and sex. Right pneumonectomy was performed in 41 patients (47%), and left pneumonectomy was performed in 47 patients (53%). Extended pneumonectomy, defined as a pneumonectomy with intrapericardial ligation of pulmonary blood vessels, an extrapleural or a completion pneumonectomy, or a pneumonectomy with carinal, superior vena cava, or chest wall resection, was performed in 60 patients (68%); a simple pneumonectomy was performed in the remaining 28 patients (32%). Resected tumors were mostly of squamous histology (63%); and according to the pTNM terminology [17], there were 16 patients (18%) with stage I disease, 33 patients (38%) with stage II disease, and 35 patients (40%) with stage III disease. Four patients were not staged because the pneumonectomy had been done for recurrent disease (n = 3) and for metastatic disease (n = 1).

Clinical Characteristics of Patients With Abnormal Postoperative Diaphragmatic Motion
Patients with abnormal diaphragmatic motion were younger than patients with normal diaphragmatic motion, and they were more likely to have undergone right pneumonectomy (p < 0.01; Table 1). They were also more likely to have had higher cancer stage and to have undergone an extended pneumonectomy (p < 0.01).

Despite comparable preoperative lung function, patients with abnormal diaphragms had significantly worse postoperative expiratory lung volumes and exercise capacity (% predicted) than patients with normal diaphragms (Table 2). Interestingly, among the 44 patients with abnormal diaphragms, there was no difference in FEV₁ between those with an immobile diaphragm (n = 22) and those whose diaphragm had a paradoxical motion (n = 22; Fig 1).

View larger version (13K): [in this window] [in a new window]   Fig 1. Postoperative lung function according to postoperative ipsilateral diaphragmatic motion. Patients with preserved diaphragmatic function had less alteration in postoperative forced expiratory volume in 1 second (FEV1) than patients with abnormal diaphragm motion. There was, however, no difference in FEV1 between patients with immobile diaphragm and patients whose diaphragm had a paradoxical motion. Comparisons among means were performed using analysis of variance followed by Fisher's PLSD test. (PLSD = procedure of least significant difference.)

In univariate linear regression analysis, postoperative FEV₁ correlated with age of the patient (better FEV₁ in younger patients), preoperative lung function (better FEV₁ in patients with better preoperative lung function), lung hyperinflation (better FEV₁ in patients with more important hyperinflation), and the presence or absence of abnormal diaphragmatic motion (Table 3).

	Comment

Top Abstract Introduction Patients and Methods Results Comment Discussion Acknowledgments References

View larger version (120K): [in this window] [in a new window]   Fig 2. The anatomy of the diaphragm, which should be viewed as a single muscular unit with two halves. Modified from Graeber and Nazim [30], with permission from Elsevier Inc.

View larger version (84K): [in this window] [in a new window]   Fig 3. Diagram showing (A) the right hilum and phrenic nerve (arrow), and (B) the left hilum and phrenic nerve (arrow). Modified from Warren and Milloy [31], with permission from Elsevier.

This surgical myth goes back to the early days of pneumonectomy where it was thought that the phrenic nerve should be crushed (phrenic crush) or even resected (phrenicectomy) during the course of pneumonectomy to raise the hemidiaphragm and infradiaphragmatic abdominal organs. It was presumed that diaphragmatic elevation would serve two purposes, the first one being to reduce the size of the pneumonectomy space, making it easier to obliterate; and the second, and likely more important, one was that an elevated diaphragm would, to some extent, prevent hyperinflation of the residual lung thought to be associated with worse functional results. Since then, surgeons have had diverging opinions about the value of preserving the phrenic nerve during the course of pneumonectomy, even if one study [26] showed that when the phrenic nerve had not been transected at operation, its motor function, as assessed by phrenic nerve conduction time (interval between stimulation of the nerve in the neck and onset of diaphragmatic muscle action potential), had remained within the normal control range in 10 patients who had undergone pneumonectomy years before (mean, 8 years; range, 2 to 11).

In normal persons, diagnostic imaging of the diaphragm is challenging owing to its thin structure and complex shape [27]. In the context of a pneumonectomy space, which is contracted and often obliterated by fibrotic tissue, imaging of the diaphragm is even more difficult; and this is probably the main reason why no previous studies have attempted to correlate diaphragmatic motion with lung function in those patients. The multiplanar imaging capability of MRI has, however, improved considerably the depiction of the diaphragm, and dynamic MRI enables real-time imaging of diaphragmatic motion [28, 29] with both quantitative and qualitative assessment of diaphragmatic function.

In the present study, changes in expiratory lung volumes, gas exchange, and exercise capacity were correlated with diaphragmatic motion in 88 patients who had undergone pneumonectomy for lung cancer 5 or more years before. The results indicate that although the underlying lung had been removed, patients with abnormal diaphragmatic motion presumably secondary to the loss of phrenic nerve motor function have significantly worse respiratory mechanics and lung function as assessed by FEV₁ (p < 0.001), FVC (p < 0.001), FEV₁/FVC, total lung capacity (p = 0.022), and DLCO (p = 0.003) than patients with normal diaphragmatic motion. Indeed, postoperative diaphragmatic motion was the most important factor influencing postoperative lung function. The fact that abnormal diaphragmatic motion has less effect on exercise tolerance as determined by the 6-minute walk test indicates that this test reflects the overall general condition and cardiopulmonary status of the patient rather than their pulmonary function alone.

The important question to ask is, why is there such a difference between patients who still have a mobile diaphragm and patients who have a paralyzed diaphragm? To answer this question, one has to look at the diaphragm as a single muscle (Fig 2) with two separate but interconnected halves. In such a muscular arrangement, it is more than likely that denervating one half of the unit will affect the entire unit in terms of synchronicity and, most importantly, in terms of efficiency. As the entire diaphragm acts as a pistonlike pressure generator during inspiration, a functioning diaphragm likely contributes to the generation of overall negative intrathoracic pressure, even if there is no underlying lung. Similarly, a paralyzed diaphragm is bound to adversely affect the generation of this negative intrathoracic presence, and thus to impair the efficiency of the residual respiratory system.

The aims of surgical therapy in resectable lung cancer are to cure the disease, improve life expectancy, and preserve as much quality of life and lung function as possible. Because our results indicate that the long-term effects of a paralyzed hemidiaphragm in pneumonectomy patients are characterized by significant alterations in expiratory lung volumes and exercise tolerance, the clear message to all surgeons doing pneumonectomies is that they should take every precaution to avoid technical errors that could lead to phrenic nerve injuries during the course of the operation.

	Discussion

Top Abstract Introduction Patients and Methods Results Comment Discussion Acknowledgments References

 
DR RAYMOND P. ONDERS (Cleveland, OH): Excellent talk. I have two questions. I know the Canadian health system, so why did you use an MRI as opposed to an ultrasound to look at—it's beautiful pictures—but why did you use an MRI and not an ultrasound? That's my first question.

The second question is, why did you not do a phrenic nerve study on these patients? And kind of the third point is that everybody talks about the phrenic nerve being cut, and it's usually not cut. It's a demyelinization. And interestingly, we've now done 3 compassionate-use patients who actually had alleged phrenic nerve injuries, negative phrenic nerve studies. The diaphragm's not moving, but we're actually able to pace their diaphragm and get that back.

And more important is the problem with the demyelinization, it's the nodes of Raynaud that can't have the signal go down. And actually if you're not utilizing that muscle, it will not repair itself. So not only were we able to pace the diaphragm on these 3 patients, actually, the patients recovered volitional control of their diaphragm again.

And so there's the trophic effect for early electrical stimulation. And obviously we're going to be starting a trial for such cases hopefully in the United States this year, FDA and God willing, that will look at that more closely, but we've done it on compassionate use.

So really the question is why not use ultrasound, why didn't you do a phrenic nerve study, and really what's your future? Now that you've seen this, do you think you're going to do anything different in your operations?

DR UGALDE: Thank you for your very interesting questions. First of all, I must say that this study is part of a major research project that we performed in Quebec to study a large series of long-term pneumonectomy patients. Today's paper is the result of a working hypothesis that diaphragmatic paralyses secondary to phrenic nerve injury may be associated with more significant loss of pulmonary function than if the phrenic nerve had been preserved.

The MRI was the examination chosen for the major project; however, the MRI is an excellent qualitative and quantitative method to evaluate diaphragmatic function and motion. I believe that your comment is probably related to the fact that Canada has a public health system and, obviously, the MRI is implied in higher costs.

DR ONDERS: A phrenic nerve study to see if the nerve is intact?

DR UGALDE: Since the complete research project wasn't designed to evaluate the functionality of the phrenic nerve, we did not perform phrenic nerve studies. Because we were present during the 88 MRIs, we could observe major anatomical and respiratory differences between patients with normal and paralyzed diaphragms. So the question just popped! Does diaphragmatic motion correlates with objective parameters of lung function?

DR ONDERS: They are beautiful pictures.

DR GEORGE B. HAASLER (Milwaukee, WI): Thank you for a beautiful talk. The only thing I wasn't sure of is, which of the phrenic nerves in these patients were actually deliberately sectioned? Do you know the answer to that? You know what we've done in Milwaukee is at the time of operation, if we do section the nerve, we just go ahead and plicate the diaphragm at the same time, both to avoid it becoming fixed in a very elevated position, and perhaps to help with function of that remaining lung if we've chosen to leave a piece of lung. Obviously that doesn't quite apply to your paper, but it may apply depending on where the diaphragm may get fixed. Thank you.

DR UGALDE: I think that this study puts down a surgical myth that goes back to the early days of pneumonectomy where it was thought that the phrenic nerve should be crushed or resected during a pneumonectomy to raise the hemidiaphragm. On the contrary, nobody has ever shown that the phrenic nerve should be preserved by all means. With these data, we have at least considered if diaphragmatic plication could benefit this group of patients.

Of the 44 patients with immobile diaphragm, 24 patients had the phrenic nerve deliberately cut owing to the type of pneumonectomy (intrapericardial). In 14 cases it was for oncological reasons (direct invasion of cancer). Only in 6 patients, we could not identify the reason why the nerve was interrupted.

DR HAASLER: Did you know the ones who were cut, which were in the paradoxic group as opposed to just the immobile group?

DR UGALDE: No. We didn't go that far in the analyses.

DR HAASLER: Thank you.

DR UGALDE: However, since there wasn't any difference in terms of FEV₁ between the paradoxic and the immobile, I don't think it really matters.

DR DONINGTON: Thank you very much. Really, a very nice paper.

	Acknowledgments

Top Abstract Introduction Patients and Methods Results Comment Discussion Acknowledgments References

 
This work has been supported by a research grant from the "Chaire de recherche JD Begin," an unrestricted grant from Sanofi-Aventis Canada, Inc, and a gracious donation of 50% of the gadolinium chelate Omniscan used in this study.

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Top Abstract Introduction Patients and Methods Results Comment Discussion Acknowledgments References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Paula Ugalde Yves Lacasse Jean Deslauriers Permission Requests Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Ugalde, P. Articles by Deslauriers, J. Search for Related Content PubMed PubMed Citation Articles by Ugalde, P. Articles by Deslauriers, J. Related Collections Lung - cancer Diaphragm