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Eur J Cardiothorac Surg 2001;20:705-711
© 2001 Elsevier Science NL

Vocal cord dysfunction after left lung resection for cancer

^a Department of General and Thoracic Surgery, Clermont-Ferrand University Hospital, Clermont-Ferrand, France
^b Department of Otolaryngology, Head and Neck Surgery, Clermont-Ferrand University Hospital, Clermont-Ferrand, France
^c Department of Anesthesia, Clermont-Ferrand University Hospital, Clermont-Ferrand, France
^d Department of Biostatistics, University of Auvergne, Clermont-Ferrand, France

Received 12 February 2001; received in revised form 10 May 2001; accepted 23 May 2001.

Corresponding author. Tel.: +33-4-7375-1567; fax: +33-4-7375-1566
e-mail: mfilaire{at}chu-clermontferrand.fr

	Abstract

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion References

 
Objectives: To evaluate the prevalence, the impact-related postoperative complications and the risk factors of vocal cord dysfunction (VCD) after left lung resection for cancer. Methods: From February 1996 to April 1999, a review of prospectively gathered data was performed on 99 consecutive patients who underwent a pneumonectomy (n=50) or a lobectomy (n=49) with a mediastinal lymph node dissection. A fiber optic laryngeal examination was performed preoperatively for all patients and within the first week postoperatively in patients with symptom(s) or sign(s) of VCD or respiratory complications. Results: Thirty-one patients (31%) had a postoperative VCD (group VCD) and 68 (68%) did not (group non-VCD). Mortality rate was 19% in group VCD and 9% in group non-VCD (P=0.13). Group VCD patients developed more pulmonary complications (P=0.014) and cardiac complications (P<0.001) compared to group non-VCD patients. A higher rate of reintubation (P=0.005), pneumonia (P=0.06), arrhythmia (P=0.002), cardiac failure (P<0.001) was noticeable in group VCD and may account for the higher rate of complications in this group. Using multivariate analysis, preoperative radiotherapy (P=0.001) and pneumonectomy (P=0.008) were predictive of postoperative VCD. Hospital stay was 22±16 days in group VCD and 13±9 days in group non-VCD (P<0.002). Conclusion: VCD is a frequent event that can lead to dramatic pulmonary complications. We would recommend to track it and to treat it as early as possible.

Key Words: Vocal cord dysfunction • Lung cancer • Postoperative complications

	1. Introduction

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion References

 
Because of their anatomic location around the aortic arch, left vagus nerve (VN) and recurrent laryngeal nerve (RLN) can be invaded by intrathoracic malignant neoplasms. For the same reason, these nerves can be severed during hilar lung tumor resection or mediastinal lymph nodes dissection. Lesion of these nerves results in left vocal cord dysfunction (VCD), that in turn is responsible for variable degree of glottic incompetence and swallowing disorders [1,2]. Respiratory consequences of these nerve dysfunctions can be life-threatening in patients undergoing pulmonary resection who have consequently limited pulmonary reserve. The incidence of postsurgical VCD has been unequally investigated. In thoracic surgery, where VCD is particularly deleterious, due to life-threatening complications, a few studies are currently available. Among these, the studies reported by Yellin et al. [3] as well as those later reported by Massard et al. [4] brought evidence that previous history of head and neck surgery for cancer with total or partial laryngeal conservation, so-called conservative surgery, increased the risk of postoperative respiratory complications following lung resection. In particular, aspiration enhanced difficulties to clear secretions can induce pneumonia and finally respiratory distress. Our purpose was to evaluate the prevalence of the unilateral VCD after left lung resection for cancer and to focus more particularly on the incidence and impact-related postoperative complications. Our second goal was to identify risk factors of VCD and relations between vocal cord position, type of nervous lesion, and postoperative complications.

	2. Patients and methods

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion References

 
2.1. Patient populations
From February 1996 to April 1999, 100 patients underwent left lobectomies or pneumonectomies for non-small cell lung cancer in our institution. All the patients were considered operable according to the existing guidelines for pulmonary resections [5] and diagnosis of cancer was obtained preoperatively or intraoperatively before resection. Intraoperative findings in a patient with a functional contra-indication for pneumonectomy have shown a microscopic involvement of the end of the main bronchus. This patient was excluded of the study because we performed a lobectomy with lymph nodes sampling but not a real lymphadenectomy as described below. The remaining 99 patients composed our study group and were entered prospectively in the clinical database. Twenty-seven patients received a preoperative treatment with chemotherapy (n=21), radiotherapy (n=2), or both chemotherapy and radiotherapy (n=4). Among the six patients with preoperative radiotherapy, three received a dose of 54 Gy after a previous left lobectomy for cancer and three received a dose of 40 Gy with a concomitant chemotherapy for stage IIIB disease.

2.2. Preoperative assessment
Complete history, physical examination, complete blood cell count, biochemical profile, chest roentgenogram, computed tomographic scan of chest, brain and upper abdomen, electrocardiography (ECG), routine pulmonary function tests, arterial blood gases, and fiber optic laryngeal examination by an otoloryngologist composed the preoperative assessment for all patients. Differential lung perfusion scans were performed in pneumonectomy patients and in lobectomy patients with marginal pulmonary function test.

2.3. Surgical procedure
Endotracheal intubation was performed with double lumen tube with carinal spur for lobectomy, without carinal spur for pneumonectomy (Rush-Pilling SA, 31460 Le Faget, France). The size of the endotracheal tube was N°35 to N°37 for women and N°39 to N°41 for men. The surgical approach was a lateral or a postero-lateral thoracotomy by the fith intercostal space. For pneumonectomy, we usually performed mediastinal lymph nodes dissection before the lung resection in order to have a correct exposure of the main bronchus. The inferior pulmonary, the para-esophageal and the sub-carinal lymph nodes were excised after division of the inferior pulmonary ligament and the posterior mediastinal pleura. The sub-aortic lymph node compartment was exposed by incising the mediastinal pleura behind the phrenic nerve and laterally to the inferior aspect of the horizontal arch of the aorta. The pleura was reflected and mediastinal fat and nodes were gently dissected. Hemostasis in the sub-aortic area was performed with surgical clips and we never used electric coagulation. The VN or RLN were deliberately resected if they could not be dissected free from the tumor or because there were in too close contact with macroscopically invaded nodes. Adequate en bloc resection of this node-bearing area provides us with a direct visualization of the pericardium, the horizontal arch of the aorta, the pulmonary artery, the carina, and the esophagus.

2.4. Assessment of vocal cord dysfunction and postoperative course
After tracheal extubation, monitoring of laryngeal function was made with a particular attention. A fiber optic laryngeal examination was performed in case of hoarseness, aspiration, ineffective cough, dysphagia, or pneumonia. VCD was considered if the left vocal cord was paralyzed. It could be abducted (extremely lateralized), intermediate (3–4 mm from midline) or paramediane (1–2 mm from midline). Patients with VCD compose the group VCD and patients without VCD the group non-VCD.

Mortality was defined as death occurring within 30 days of surgery or beyond that period if the patient had not left the hospital. Postoperative complications (Cpo) were classified into pulmonary complications (PCpo), cardiac complications (CCpo) and other complications (OCpo). Pulmonary complications were defined as pneumonia (temperature >38°C for 48 h, purulent sputum production and infiltrate on chest roentgenogram), lobar atelectasis, postoperative bronchoscopy for atelectasis or major sputum production, pulmonary embolus, non-cardiac pulmonary edema, mechanical ventilation >48 h, reintubation, and tracheostomy. Cardiac complications were defined as myocardial ischemia, arrhythmia and cardiac failure (need of inotrop drug infusion). Other complications were defined as empyema, bronchopleural fistula, bleeding, and general complications. Hospital stay was defined as the number of days in the hospital after surgery.

2.5. Statistical analysis
The comparison between preoperative data, surgical resection, pathologic finding and postoperative course of group VCD and group non-VCD was carried out by means of the Mann–Whitney test for continuous variables and a Chi-square test for categoric variables. When the expected value was <5, the Fisher's exact test was used. Multivariate analysis by partition of Chi-square using PCSM statistical package (Delta Consultants, Meylan, France) was applied to determine whether qualitative variables were predictive of VCD. Parameters with a P<0.1 at the Chi-square test were selected to be entered into the partition model. Briefly, with the partition of the Chi-square, the selected and supposed explanatory variables are graded. Finally, the eligible variables are independently associated with the occurrence of VCD. A probability below 0.05 was accepted as statistically significant.

	3. Results

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion References

 
3.1. Study population
Pneumonectomy was performed in 50 patients and lobectomy in 49. VCD occurred in 31 patients (31%) whom composed the group VCD. Preoperative VCD was observed in three patients because of VN invasion by the tumor in two cases and RLN injury during mediastinoscopy in the latter case. In 15 patients, VCD was due to deliberate resection of the intrathoracic segment of the nerve that was invaded or too close to the tumor to be preserved. Thirteen patients had an unexpected VCD despite surgical nerve preservation. The remaining 68 patients with normal laryngeal motility composed the group non-VCD. The characteristics of the VCD and non-VCD groups are given in Table 1 with a comparison between the two.

3.3. Symptoms
Hoarseness occurred in all patients with VCD, aspiration in 11 (35%), poor cough in eight (25%) (need of a bronchoscopy for major sputum production), and dysphagia in two (6.5%). A bronchoscopy for inefficient cough was necessary in 54% of the patients who had aspiration compared to 15% of the patients who did not (P=0.025). Thirty-six percent of the patients who had aspiration developed pneumonia compared to 10% of the patients who did not (P=0.088).

3.4. Mortality and morbidity
Mortality was 12% in our study, but it was not statistically different between groups VCD and non-VCD (P=0.13). Table 2 shows the prevalence of mortality in each group and the cause of death.

We also compared mortality and morbidity between pneumonectomy patients of the two groups. Pneumonectomy patients of the group VCD (n=21) needed more reintubations (P=0.044), and developed more aspirations (P=0.0003) and cardiac failure (P=0.027) compared to the pneumonectomy patients of the non-VCD group (n=27). The higher prevalence of postoperative bronchoscopies (P=0.065), PCpo (P=0.064), CCpo (P=0.064) and mortality (P=0.42) among pneumonectomy patients of the VCD group were not statistically significant.

3.5. Relations between nerve injury, vocal cord position, and morbidity
This analysis only concerned 28 patients of group VCD, i.e. patients who had no preoperative VCD in order to consider only patients with acute postoperative VCD. The relationship between vocal cord position and nerve injury are shown in Table 4. Note that an abducted position of the vocal cord was found in the vast majority of cases (87%) of RLN or VN section. Forty-seven percent of the patients with an abducted vocal cord needed a postoperative bronchoscopy compared to 9% of patients with intermediate or paramediane vocal cord position (P=0.032). In contrast, patients with an abducted vocal cord did not have significantly more aspiration (P=0.89), pneumonia (P=0.61), reintubation (P=0.25), lobar atelectasis (P=0.85) or PCpo (P=0.25) than the rest of the 29 patients.

	4. Discussion

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion References

• occurs in one-third of the patients after left lung resection and mediastinal lymph nodes dissection for cancer,
  
• is associated with a higher rate of morbidity with a higher rate of reintubation and arrhythmia,
  
• occurs more frequently in patients who received preoperative radiotherapy or who underwent pneumonectomy.
  

It is clear that lung surgery for cancer is not a rare cause of VCD. In a retrospective study based on 280 patients with unilateral vocal fold immobility, Benninger et al. [7] found that 24% of the patients were secondary to extra laryngeal malignancies, 80% of which were due to pulmonary or mediastinal disease. In 1029 patients reviewed from the literature, Terris et al. [8] found that 20% of cases of VCD were associated with lung cancer. Undoubtedly, one of the most frequent extra laryngeal causes of VCD is represented by intrathoracic malignancies and in particular, lung cancer. However, to date, the prevalence of postoperative VCD has been unequally investigated. For example, after patent ductus arteriosus ligation, Zbar et al. [9] have reported a prevalence of only 7.4% of vocal cord paralysis with no improvement after an average follow-up of 6 months. After carotid endarteriectomy, Curran et al. [10] found a 20% prevalence of VCD, which was transient in 90% of the cases. In a retrospective study of 1026 patients undergoing thyroid gland surgery, Wagner et al. [11] found that VCD occurred in 5.9% of the cases. Surprisingly, our results show that left lung resection for cancer is associated with a higher prevalence of VCD compared with other cervical or thoracic surgical procedure for benign pathologies.

VCD was the result of the surgical section of VN or RLN in 58% of our patients with VCD. In these cases, the nerves could not be dissected free from the tumor because of a direct tumor or lymphatic invasion of the sub-aortic region. In the remaining 42% of the cases, VCD was unexpected because the nerve was thought to be preserved. It is important to note that we never used electric coagulation but surgical clips for hemostasis during lymph nodes dissection. Therefore, one can exclude various degrees of heat-related nerve injury. Firstly, VN and RLN may have been stretched during hilar tumor dissection of the aortic window resulting in neuropraxia. Secondly, injury to these nerves could be due to the damage of the perineural vasculature. Indeed, perineural vascular injury is considered by some authors as a cause of RLN paralysis after thyroidectomy [12]. In a recent anatomic study, we showed that branches arising from the anterior broncho-esophageal artery were a constant blood supply to the sub-aortic segment of VN and the origin of RLN. Therefore, nervous ischemia during sub-aortic lymph node excision is likely to occur and could explain postoperative VCD [13]. Thirdly, anatomic studies have shown that the anterior terminal branch, designated as the motor branch, is located laterally, whose position makes it particularly exposed to surgical wound or trauma [14]. From our point of view, there is no doubt that this lateral position of the motor fibers within the nerve can give account of the postoperative VCD, even though the nerve was anatomically preserved.

In our study, it is more interesting that in case of nervous section, 83% of patients had an abducted vocal cord. In contrast, when the nerves were thought to be preserved, we only noted an abducted vocal cord in 50% of cases. For us, these results suggest that the respiratory function of the RLN, mediated by the fibers directed to the cricoarythenoid muscle (the only muscle dilatator of the glottis) is more sensitive to surgical injury than the phonatory fibers directed to the glottal constrictors. Because anastomotic networks are often found between the superior laryngeal nerve (SLN) and RLN, within the interarythenoid muscle, or within the thyroarythenoid muscle [15], the position of the impaired vocal cord could depends upon the development of these networks. Thus, even though these constrictor muscles are deprived of RLN fibers, they can still be connected with other motor fibers arising from SLN, allowing for persistent capacity of adduction motility.

Whereas an abducted vocal cord was associated with less efficient cough, we did not observe a significant increase of pneumonia in these cases. It is likely that pneumonia could be avoided by postoperative bronchoscopy. Further, it is not surprising that the vocal cord position was not correlated with aspiration. Indeed, it is clear that aspiration depends upon multiple causes such as a glottal protection by the epiglottis or the performance of the sensitive innervation of the larynx, for instance. Because swallowing depends on the integrity of both motor and sensitive innervation, it is likely that swallowing disorders are more frequently mentioned after both lesions of RLN and SLN than after unilateral RLN paralysis alone [16].

Hoarseness is reported to occur in 86–100% of patients after surgical RLN paralysis [1,17,18]. In our study, all patients with VCD had hoarseness likely because the contralateral vocal cord was unable to immediately compensate the laryngeal paralysis. In 45% of the patients, hoarseness was the only one symptom of VCD. Thus, in cases of hoarseness, a laryngeal examination should be rapidly realized to confirm the diagnosis of VCD and to prevent its consequences. Aspiration must be tracked, inasmuch as it can be asymptomatic [17] because it can result in sudden choking, gradual bronchial obstruction, and pneumonia, which are dramatic complications, more likely to occur in patients with less efficient cough and impaired pulmonary function. This was particularly well shown by Henderson et al. [2]. In 15 patients with VCD caused by bronchogenic carcinoma, these authors found that 73% had aspiration. Similarly in 111 patients with VCD and after esophageal cancer surgery, Hirano et al. [18] found that 53% had aspiration, most often associated with a weak cough. Eighty four percent of these patients developed pneumonia and 47% needed a tracheostomy. In our study, the 35% prevalence of aspiration in patients with VCD is low and probably underestimated because we only recorded symptomatic aspiration.

In our study, VCD did not have a significant influence on mortality. As a matter of fact, in both groups, the most frequent cause of death was not the consequence of VCD. Yet, let us remark that two of the three patients who died of pneumonia had VCD.

The lack of airway protection resulting from laryngeal dysfunction can be associated with respiratory complications. This was evident in our studies where postoperative pulmonary complications occurred in 51% of the patients with VCD but in only 26% of the others. Others authors have also reported that laryngeal dysfunction increases morbidity after thoracic surgery. Massard et al. [4] have undoubtedly pointed out an increased risk of respiratory complications due to aspiration, following lung surgery in patients with previous history of voice sparing surgery for pharyngo-laryngeal malignancy (23%) compared to patients with total laryngectomy. Hirano et al. [18] have reported a rate of 45% of aspiration pneumonia in patients with VCD caused by esophageal cancer surgery. By contrast, respiratory complications caused by VCD are very uncommon after surgery of the carotid artery, thyroid gland, and ductus arteriosus in young patients [9–11]. These results show that patients undergoing lung or esophageal surgery for cancer are at high risk of postoperative complications in case of VCD. Undoubtedly, one of the main reasons of increased risk of VCD-related pulmonary complication, is due to the reduction of air flow and vital capacity after lung resection [19]. This characteristic, which is specific to thoracic surgery, jeopardizes the ability to generate an efficient cough and to clear secretions and aspirations. Impaired ventilation, dyspnea, and increased respiratory work may generate fatigue of respiratory muscles in patients with lowest ventilatory reserve. This problem may be crucial after pneumonectomy. Thus, it was not surprising, in our study, that patients with VCD differed significantly from patients without VCD by a higher rate of reintubation. Among patients with VCD, those who needed reintubation had a restrictive pattern at the preoperative pulmonary function tests. Finally,the major cause of reintubation was respiratory muscle fatigue resulting from bronchial obstruction by sputum and weak cough in four patients (57%).

Little is known about the responsibility of VN or LRN section in the occurrence of arrhythmia after thoracic operations. Numerous risk factors of arrhythmia including atrial inflammation, pericarditis, pulmonary hypertension, hypoxemia, cardiac failure, deranged hemodynamics caused by valvular diseases, and increased vagal or sympathetic tone can exist [20]. Because the heart is innervated by both sympathetic and parasympathetic nerves that form the cardiac plexus located under the aortic arch, one can hypothesize that injury to the VN and RLN predispose to arrhythmia.

In a large retrospective study, Asamura et al. [21] found that RLN or VN section was not predictive of arrhythmia. In our study, univariate analysis showed that the occurrence of VCD was a risk factor of arrhythmia as well as pericardiotomy and cardiac failure but that the extent of the resection was not. A multivariable analysis of these four variables revealed that the occurrence of a cardiac failure (need of inotrop drug) was the only one significant risk factor. Also, we observed that preoperative cardiac events were present in 66% of our patients with arrhythmia compared to 40% in patient without arrhythmia (P<0.045). If injury to VN and RLN results in an imbalance between sympathetic and parasympathetic tones, it may influence arrhythmia like other risk factors mentioned previously. Therefore, for us, the preoperative cardiac status is the more important factor to consider in order to predict arrhythmia.

The VN or RLN are at high risk of injury during dissection of the sub-aortic region. Our report shows that the risk was considerably increased in case of preoperative radiotherapy or pneumonectomy. In both situations, the identification and the respect of the nerve were more difficult and sometimes impossible because of tissue fibrosis after radiotherapy or because of their close proximity to the tumors in case of pneumonectomy. In contrast, the size and the invasion of the sub-aortic lymph nodes were not associated with a higher rate of VN or RLN injury.

In conclusion, our study brings additional evidence that VCD after left lung resection for cancer is a frequent event that can lead to dramatic pulmonary complications. Right RLN injury may also occur following right lung cancer resection with extensive lymph node dissection up to the sub-clavian artery. It would be ideal to avoid RLN and VN injury, and in this aim, intraoperative evoked laryngeal monitoring is promising [22]. Lastly, since VCD can be a highly deleterious event, we would recommend to track it and to treat it as early as possible in such patients just operated for lung cancer.

	Acknowledgments

 
We thank Mrs Martine Collomb for her help in the preparation of the manuscript.

	References

Top Abstract 1. Introduction 2. Patients and methods 3. Results 4. Discussion 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): Adel Naamee Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Filaire, M. Articles by Escande, G. Search for Related Content PubMed PubMed Citation Articles by Filaire, M. Articles by Escande, G. Related Collections Lung - cancer