Eur J Cardiothorac Surg 2007;32:449-456. doi:10.1016/j.ejcts.2007.05.031
Copyright © 2007, European Association for Cardio-Thoracic Surgery. Published by Elsevier B.V. All rights reserved
Diaphragm plication in adult patients with diaphragm paralysis leads to long-term improvement of pulmonary function and level of dyspnea
Michel I.M. Versteegha,*,
Jerry Brauna,
Pieter G. Voigta,
Daniël B. Bosmana,
Jan Stolkb,
Klaus F. Rabeb,
Robert A.E. Diona
a Department of Cardio-thoracic Surgery, Leiden University Medical Center, Leiden, The Netherlands
b Department of Pulmonology, Leiden University Medical Center, Leiden, The Netherlands
Received 2 February 2007;
received in revised form 8 May 2007;
accepted 23 May 2007.
* Corresponding author. Address: Leiden University Medical Center, Department of Cardio-thoracic Surgery, K6-S, P.O. Box 9600, 2300 RC Leiden, The Netherlands. Tel.: +31 71 5262355; fax: +31 71 5266359. (Email: m.i.m.versteegh{at}lumc.nl).
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Abstract
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Objective: There is still controversy about the feasibility and long-term outcome of surgical treatment of acquired diaphragm paralysis. We analyzed the long-term effects on pulmonary function and level of dyspnea after unilateral or bilateral diaphragm plication. Methods: Between December 1996 and January 2006, 22 consecutive patients underwent diaphragm plication. Before surgery, spirometry in both seated and supine positions and a Baseline Dyspnea Index were assessed. The uncut diaphragm was plicated as tight as possible through a limited lateral thoracotomy. Patients with a follow-up exceeding 1 year (n
= 17) were invited for repeat spirometry and assessment of changes in dyspnea level using the Transition Dyspnea Index (TDI). Results: Mean follow-up was 4.9 years (range 1.2–8.7). All spirometry variables showed significant improvement. Mean vital capacity (VC) in seated position improved from 70% (of predicted value) to 79% (p
< 00.03), and in supine position from 54% to 73% (p
= 0.03). Forced expiratory volume in 1 s (FEV1) in supine position improved from 45% to 63% (p
= 0.02). Before surgery the mean decline in VC changing from seated to supine position was 32%. At follow-up this had improved to 9% (p
= 0.004). For FEV1 these values were 35% and 17%, respectively (p
< 0.02). TDI showed remarkable improvement of dyspnea (mean + 5.69 points on a scale of –9 to +9). Conclusion: Diaphragm plication for single- or double-sided diaphragm paralysis provides excellent long-term results. Most patients were severely disabled before surgery but could return to a more or less normal way of life afterwards.
Key Words: Diaphragm plication • Diaphragm paralysis • Phrenic nerve dysfunction • Surgical treatment of dyspnea
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1. Introduction
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Diaphragm paralysis results from an acquired dysfunction of the phrenic nerve and is rather uncommon in adults. It should not be confused with eventration of the diaphragm, a congenital disorder with permanently raised parts of the abnormally thin hemi-diaphragm. The exact incidence of diaphragm paralysis is not known since generally it is not recognized. Patients usually present with dyspnea on exertion; however, the severe and progressive dyspnea when bending over or changing to supine position is often even more disabling and almost pathognomonic for this disease. Patients eventually have to sleep in an upright position and have to stop working. The progression of dyspnea is caused by a decline in lung volumes, i.e. vital capacity (VC) and forced expiratory volume in 1 s (FEV1). The degree of decline is variable [1]. Also, immersion in water (taking a bath or swimming) causes deterioration of dyspnea by the increased pressure on the abdomen. Although it might be conceivable that long-lasting diaphragm paralysis leads to a cor pulmonale, there is no evidence for this statement.
Phrenic nerve dysfunction can be caused by any disorder affecting nerve tissues, e.g. vasculitis, neuromuscular diseases like amyotrophic lateral sclerosis [2], and trauma. Thermal trauma or direct laceration during dissection of the internal mammary artery in coronary artery revascularization [3,4] and surgery for tumors involving the phrenic nerve should be mentioned especially. Diaphragm paralysis can also be part of a neuropathological entity called neuralgic amyotrophy [5–7]. These patients have a history of a viral infection like a common cold or influenza and sudden pain in the shoulder or neck region before the onset of progressive dyspnea [5,6]. They typically suffer from a weakness of the arm, which eventually recovers. Although some recovery of diaphragmatic strength has been described in neuralgic amyotrophy, both the extent and duration of recovery are highly variable [8]. If there is no sign of recovery at all after 1 year, chances of complete recovery of muscle strength are small [5]. Development of unilateral or bilateral (mono-) neuritis of the phrenic nerve (without any known cause) is sometimes considered a variety of neuralgic amyotrophy without the typical limb-muscle weakness [5–7,9,10].
Diaphragm paralysis can be suspected on a chest X-ray. Pulmonary function tests in upright and supine positions and a paradoxical diaphragm movement in a sniff-test using fluoroscopy or ultrasound confirm the diagnosis. Other suggested investigations [1,5,6,11] are not necessary and only add costs to the diagnostic route [1,12].
Surgical treatment by diaphragm plication has been described since 1985 in small series for unilateral paralysis [13–17] and in three patients with bilateral paralysis [18]. There is still controversy around this treatment, especially regarding its long-term outcome. We describe our experience in 22 patients of whom 5 had bilateral and 17 unilateral paralysis. We focus on both pulmonary function tests and dyspnea scores before surgery and at long-term follow-up.
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2. Material and methods
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2.1 Patient population
Between December 1996 and January 2006, 22 consecutive patients underwent surgical treatment for diaphragm paralysis. Since most patients had their paralysis for at least 1 year, the chance of recovery was small, which in combination with the symptoms, was the indication to consider surgical treatment. Mean age was 62 years (range 37–89 years) and half of them were male. Mean body mass index (BMI) in our patient group was 28.2 (range 22.0–34.4). Five patients had a bilateral paralysis. The initial findings from three patients have been reported previously [18]. The longest period of documented unilateral paralysis was 23 years and was present on the left side in a patient with a recent onset of right-sided paralysis. In three patients the cause of diaphragm paralysis was obviously iatrogenic (two after CABG, one after resection of a malignant thymoma), in one patient it was associated with a brachial plexus trauma, and six had neuralgic amyotrophy. Etiology was unknown in 12 patients. All patients suffered from dyspnea, aggravating when adopting a recumbent position. They all slept in upright position and three patients needed support with continuous positive airway pressure (CPAP). Patient data are presented in Table 1
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2.1.1 Diagnostic tests
Diaphragm paralysis was suspected when finding an elevated (hemi-) diaphragm on chest X-ray (Fig. 1A) and confirmed by a sniff-test during fluoroscopy or ultrasound examination. Preoperatively, pulmonary function tests and dyspnea level assessment were performed (see below). In patients with long-lasting paralysis, a right-sided heart catheterization (n
= 2) or an echocardiography (n
= 5) was also performed to check for pulmonary hypertension. Two patients did have pulmonary hypertension, one of whom received sildenafil citrate (Viagra®).
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Fig. 1. Patient with a left-sided diaphragm paralysis. (A) Typical preoperative chest X-ray of a patient with a left-sided diaphragm paralysis. (B) Postoperative chest X-ray of the same patient.
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2.1.2 Pulmonary function tests
VC and FEV1 were both measured in upright and supine positions according to the guidelines of the European Respiratory Society (ERS) and expressed as a percentage of the predicted values. When patients were not able to lie completely flat, they were positioned individually as flat as possible. Baseline pulmonary function was compromised (Table 2
). The typical deterioration when changing from upright to supine position was obvious, and is expressed both as an absolute value (Fig. 2
) and as a relative decline (Table 2) compared to the volumes in the upright position.
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Fig. 2. Preoperative decline in FEV1 changing from seated to supine position expressed as percentage of predicted values.
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2.1.3 Dyspnea score
The level of dyspnea was assessed using the Baseline Dyspnea Index (BDI) and Transition Dyspnea Index (TDI) as proposed by Mahler et al. [19] (see Appendix A). The BDI rates the patient's functional impairment, the magnitude of task needed to evoke dyspnea, and the magnitude of effort associated with this task before treatment. In each of these three categories the patient's condition is rated from 0 (severely impaired) to 4 (unimpaired). Ratings of the three categories are added, yielding the BDI score. The lower the total score, the worse the severity of dyspnea. To evaluate the result of treatment the TDI was used. Changes for all three categories are rated by the physician from –3 for major deterioration to +3 for major improvement. Adding these scores produces the total TDI score, which can thus range from –9 to +9.
2.2 Surgical procedure
A limited lateral thoracotomy is performed through the 8th intercostal space. The uncut diaphragm is shortened first in anteroposterior direction with a number of U-stitches (Mersilene® 2; Ethicon®, Norderstedt, Germany), usually starting on the mediastinal side (Figs. 3 and 4
). No material to reinforce the sutures is used. It is very important to pass the needles with extreme care to avoid damaging the abdominal organs since the diaphragm is usually very thin (Fig. 3). These sutures are tied as tight as possible. A second layer below the first can be placed in case of insufficient tightness (at the discretion of the surgeon). Then, another radial U-stitch is used to complete the shortening in lateral direction. Redundant tissue is flattened both anteriorly and posteriorly to the plicature with running sutures (Ethibond® 2-0, Ethicon®) (Figs. 4 and 5
). The result is a tense and firm diaphragm (Figs. 4G, 5, and 1B). Whenever feasible, patients are extubated in the operating theatre.
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Fig. 3. Intra-operative photograph showing the extreme thinness of the diaphragm. The first layer of U-stitches is depicted here.
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Fig. 4. Diaphragm plication. Drawing (A) illustrates the paralytic diaphragm. Drawing (B) shows the first row of U-stitches, starting on the mediastinal side. Drawing (C) shows the optional second layer, if the surgeon is not yet satisfied with the tightness. Drawings (D) and (E) are showing the radial U-stitch to complete the shortening, leaving redundant tissue in the middle of the operating field. Drawing (F) shows the running sutures to flatten the redundant tissue anteriorly and posteriorly to the plicature. Drawing (G) shows the final result.
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Fig. 5. Final result. Intra-operative photograph showing the final result of the operative procedure: a tight and firm diaphragm.
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Three patients with bilateral paralysis underwent plication of both hemi-diaphragms in a single procedure. The other two patients had two separate procedures with an interval of 2 months.
2.3 Follow-up
All patients with a postoperative interval exceeding 1 year (n
= 17) were invited for repeat spirometry and assessment of their actual dyspnea by TDI in our hospital. A chest X-ray was also performed.
2.4 Statistical analysis
Continuous data are expressed as mean values. Values of VC and FEV1 are expressed as percentage of that predicted. The rate of decline of both parameters changing from upright to supine position is expressed as percentage of the volume in upright position. Follow-up data are compared with preoperative values using Student's t-test for paired and unpaired data when appropriate. The Pearson correlation coefficient (r) was calculated for pre- and postoperative function test data and for dyspnea indices. For all tests a p-value < 0.05 (two-sided) was considered significant.
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3. Results
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Diaphragm plication could be achieved in all patients. There were no intra-operative complications.
3.1 In hospital
Three patients died in hospital. The first patient (patient #7, Table 1) had an uneventful procedure and postoperative course. The night before discharge she was found dead. Postmortem examination revealed acute myocardial infarction with two-vessel coronary artery disease. The second patient (patient #16) had long-lasting bilateral diaphragm paralysis associated with severe hypercapnia (pCO2 on room air: 6.8–11.8 kPa) and pulmonary hypertension. Postoperatively she developed renal insufficiency and died of right heart failure. The third patient (patient #19) had a family history of thrombosis. Although all routine tests for coagulopathies were normal, she received high-dose nadroparin prophylaxis starting the day before surgery. During the second postoperative night she sustained an electromechanical dissociation on the ward. Postmortem examination revealed massive pulmonary embolism in both lungs.
Mean postoperative hospital stay was 5.5 days (range 3–10). Starting this new program there was an intensive care unit (ICU) bed available for all patients, which was not used in seven cases. One patient (patient #16) stayed in the ICU for 5 days because of the above-mentioned complications. The other 14 stayed there just one night. Five patients who developed a paralytic ileus for 2 or 3 days recovered spontaneously. Almost all patients experienced a feeling of tightness in the lower chest/upper abdominal area after the procedure.
3.2 Long-term follow-up
There were no late deaths. At the time of follow-up 17 patients had a postoperative interval exceeding 1 year. Sixteen participated in our restudy including spirometry and assessment of TDI. Thirteen patients were assessed in our hospital; three underwent pulmonary function tests at their referring hospitals while TDI assessment was performed by telephone. The only patient who denied participation claimed that he was much improved. Mean follow-up was 4.9 years (range 1.2–8.7 years). There were no signs of recurrent elevation, ruptures, or tears of the plicated diaphragms as determined by chest X-ray. In one patient the diaphragm appeared to be slightly elevated 8 years after the operation compared to the immediate postoperative chest X-ray. All patients felt better after surgery but nine still experienced a feeling of tightness. Four complained of post-thoracotomy pain. All but one patient in the working age group resumed their work. All could sleep in supine position again. Three patients who needed CPAP support before the operation did no longer need it at follow-up.
3.3 Spirometry at follow-up
All spirometry variables showed significant improvement at follow-up compared to baseline (Table 2); mean VC in upright and supine and mean FEV1 in upright and supine position. The improvement becomes even more obvious calculating the decline in loss of VC and FEV1 changing positions (expressed as percentage loss compared to upright position) (p
= 0.004) and TDI. A correlation was found between the preoperative VC in supine position and improvement of the same variable postoperatively (r
= 0.73), and also with the improvement of the postoperative FEV1 in supine position (r
= 0.71). The decline in preoperative VC changing from upright to supine position proved to be strongly correlated with the amount of decrease of these values at follow-up (r
= 0.78) and the decline in FEV1 preoperatively with the amount of decrease of both the postoperative decline in FEV1 (r
= 0.80) and VC (r
= 0.78). To summarize, a worse pulmonary function test before surgery was correlated with a better test at follow-up.
3.4 Dyspnea level assessment
Mean (preoperative) BDI score in the study patients was 4.6 (range 0–11). Mean (postoperative) TDI score was +5.69 (range 0 to +9) on a scale from –9 to +9, indicating that no patient deteriorated and almost all improved remarkably. BDI was correlated with the extent of improvement at follow-up (r
= 0.63). There was no correlation between TDI and improvement of pulmonary function at follow-up, and we could not determine a threshold of preoperative pulmonary function tests to predict the outcome in TDI.
In seven patients with both short-term and long-term follow-up data available, long-term and short-term results were similar, indicating that functional improvement after diaphragm plication occurs early and is sustained over time.
3.5 Unilateral or bilateral diaphragm paralysis and plication
Although there was a tendency of worse baseline spirometry values for patients with double-sided diaphragm paralysis, differences were not statistically significant with the exception of the loss of volumes when changing from upright to supine position (Table 3
). BDI was not different in patients with unilateral or bilateral paralysis.
The fact that the extent of improvement of some spirometry values does not reach statistical significance comparing both groups is possibly due to the small number of patients with bilateral surgery. Although mean TDI score for patients after bilateral plication has a tendency to be less than after unilateral plication, this study proves there is still a major improvement.
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4. Discussion
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Surgical treatment of diaphragm paralysis by plication has been described since 1985 in small series for unilateral paralysis [13–17,20,21] and in three patients with bilateral paralysis [18]. Some studies only or mainly concern patients after cardiac surgery with problems at weaning from ventilation [16,22]. Follow-up in most studies is limited both in patient numbers and in time; Higgs et al. described a group of 19 patients with long-term follow-up in 15 [15]. In contrast to our results, they found only a limited effect of positional changes on pulmonary function, both before and after surgery. In fact, FEV1 changing to supine position even worsened after the procedure, both immediately and at long-term follow-up. In our study, the beneficial effect of the surgical procedure was obvious and significant, both for the loss of VC and for loss of FEV1. Freeman et al. described a series of unilateral diaphragm plications in 25 patients with improved spirometry values at follow-up [17]; however, this concerns only 6 months follow-up. The only article to date describing bilateral diaphragm plication comes from our own group [18]. The number of patients was small (three surgically treated patients and three controls), but follow-up (2 years) was complete.
Higgs was the first to use a dyspnea score to evaluate his patients. He used the score of the American Thoracic Society (ATS) and Medical Research Council (MRC), which was also used by Freeman. Mahler et al. showed the limitations of this score in 1984 by indicating that the MRC/ATS score primarily focuses on the magnitude of task that provokes dyspnea [19]. The magnitude of effort associated with this task is not considered. This is important because there is a large difference between climbing two flights of stairs at high speed or very slowly. Also the functional impairment resulting from the dyspnea is not considered in the MRC/ATS score. The impact of functional impairment is amongst others related to patient age and is strongly associated with quality of life. Mahler introduced a new score with assessment of functional impairment, magnitude of task provoking dyspnea, and the magnitude of effort associated with that task. All three categories are rated before (BDI) and after (TDI) treatment. This score has been validated in the United States [22] and in a number of other countries including The Netherlands [23]. Patterns of response to an effective pharmacological treatment in patients with COPD usually show a total TDI score of +1 or +2 points [22,24]. We believe that the huge TDI scores in our patients indicate the major functional impairment posed on these patients by their diaphragm paralysis.
Non-invasive ventilation techniques are described to relieve symptoms in patients with diaphragm paralysis and to prevent ventilatory failure [1] and can in selected cases be applied while waiting for the diaphragm to recover after iatrogenic trauma [12]. Several patients in our study used CPAP masks before surgery. Despite their benefits their negative impact on daily life is not to be underestimated. The fact that patients could stop CPAP treatment after surgery is a major clinical benefit.
Until 2006 only a few reports with very limited numbers of patients have been published using a laparoscopic or thoracoscopic technique for surgical plication [21]. Freeman et al. were the first to describe a patient group of substantial size treated with this technique [17]. One could wonder if these video-assisted techniques are the optimal choice. First, the advantages of a thoracoscopic technique are not obvious. Although the incisions are smaller, the incidence and intensity of post-thoracotomy pain does not seem to be very different [25]. Secondly, a paralyzed diaphragm can be very thin and extreme care has to be taken not to puncture the abdominal organs. Can this be performed safely for the patients with bilateral surgery using thoracoscopy? Furthermore it can be difficult to fully inspect the highly elevated dome of a paralyzed diaphragm. The third argument considers the tightness of the plication. We strongly believe that the diaphragm should be rendered as tense as possible (Figs. 1B and 4) and that this explains why the beneficial effects of the plication in our patients are sustained over time. We do not believe that such a tense diaphragm can be achieved with a video-assisted technique lacking full tactile feedback. Obviously, there are no head-to-head comparisons to date.
A limitation of this study is the lack of a control group. In our previous publication, however, we showed that all patients in the control group deteriorated during the study period in contrast to the treated patients [18]. The same was described by Freeman et al., despite all other treatment options offered to the patients who refused surgical treatment [17]. Although three patients in this study died in hospital, death was directly related to the surgical procedure in only one case. The improvement of the patients was found to be sustained at follow-up and there is no alternative treatment: in our opinion this justifies the use of surgical plication as soon as spontaneous recovery has become unlikely.
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5. Conclusions
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Diaphragm paralysis can be severely disabling. Surgical treatment by plication of the diaphragm can be done with excellent long-term results both in patients with unilateral or bilateral diaphragm paralysis, regardless of the etiology of phrenic nerve dysfunction. Follow-up examinations reveal not only significant improvement of pulmonary function test parameters but also a remarkable improvement of the level of dyspnea, resulting in the possibility for these patients to return to a more or less normal way of life. Although the magnitude of benefit of surgical treatment for patients with bilateral paralysis is less compared to that in patients with unilateral paralysis, results at long-term follow-up still suggest an important clinical benefit even in this difficult group of patients.
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Appendix A
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Baseline Dyspnea Index
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Appendix B
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Transition Dyspnea Index
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Footnotes
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\#9734; Presented at the joint 20th Annual Meeting of the European Association for Cardio-thoracic Surgery and the 14th Annual Meeting of the European Society of Thoracic Surgeons, Stockholm, Sweden, September 10–13, 2006.
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Top
Abstract
1. Introduction
