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Ann Thorac Surg 2001;72:1691-1697
© 2001 The Society of Thoracic Surgeons

Original article: general thoracic

Decade-long experience with surgical therapy of myasthenia gravis: early complications of 324 transsternal thymectomies

József Kas, MD*a, Dorottya Kiss, MDb, Veronika Simon, MDb, Egon Svastics, PhDa, László Major, MDa, Albert Szobor, DSCc

a Department of Surgery, Budapest, Hungary
b Anesthesiology and Intensive Care Unit, Buda MÁV Hospital, Budapest, Hungary
c Department of Neurology, South-Pest County and Teaching Hospital, Budapest, Hungary

Accepted for publication June 23, 2001.

* Address reprint requests to Dr Kas, Buda MÁV Hospital, Szanatórium u 2/a, H-1528 Budapest, Hungary
e-mail: kasaczel{at}matavnet.hu


   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Comment
 References
 
Background. We studied the incidences and evaluated the management of early postoperative complications after thymectomy for myasthenia gravis.

Methods. During the period between 1987 and 1996, 324 thymectomies were performed through median sternotomy access under general anesthesia. Postoperative management was administered according to a standardized protocol of anticholinesterase medication, which was withdrawn for the 48 hours of obligatory postoperative mechanical ventilation. The mean age of patients was 34 years (range, 8 to 71 years).

Results. One hundred forty-nine patients made an uneventful recovery; 104 patients had only minor complications, whereas 71 patients had major complications. The mortality rate was 0.6% (2 patients). The major surgical complications were recorded as sternal bleeding (1 patient) and sternal disruption (1 patient). The major general complications were recorded as tracheal stenosis (1 patient), pneumonia (3 patients), heart failure (1 patient), gastric hemorrhage (1 patient), and respiratory insufficiency (71 patients). Forty-six reintubations were performed on 40 patients and 19 tracheostomies (6%) were performed postoperatively.

Conclusions. The excessive incidence of respiratory insufficiency and airway-associated morbidity was potentially related, at least partially, to prolonged mechanical ventilation and withdrawal of anticholinesterase medication. Earlier weaning of patients with revision of 48-hour withdrawal of anticholinesterase medication is necessary.


   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Comment
 References
 
Surgical removal of the thymus has become an accepted and practiced therapeutic option worldwide for myasthenia gravis since Blalock and colleagues [1] first performed this intervention in 1936 and described its technique in 1939. Although the usefulness of this operation has never been tested in prospective randomized trials, large series published in the literature unequivocally established the value of thymectomy. In particular, the superiority of surgical treatment over conventional management is demonstrated by the higher proportion of definitively cured patients, the percentage and magnitude of clinical remissions, the lower dose-requirements of anticholinesterase medications, and prolonged survival. The international literature on myasthenia gravis has always emphasized the long-term impact of thymectomy on the natural course of the disease. Less attention has been paid to perioperative complications. It soon became evident that the mortality and morbidity of transcervical thymectomy was substantially lower than operations performed through the transsternal route. However, the latter approach offers full access to the mediastinum and makes extended excision of the gland possible. Considering that these advantages lead to better long-term results and thereby exceed the drawbacks of greater surgical stress imposed on patients, many experts prefer transsternal thymectomy [2–8]. In the Hungarian clinical practice, partial [9] or total [10–12] transsternal access has always been and still is the method of choice to perform thymectomy.

The present study describes our experiences of managing early postoperative complications after simple or extended thymectomies performed through median sternotomy. Relevant literature has been researched to supplement our data, as well as obtain valid conclusions to improve our own practice.


   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Comment
 References
 
During the period from January 1, 1987, to May 31, 1996, primary operations for myasthenia gravis were performed on 324 patients. One patient underwent re-thymectomy and was not included in this study. Operative and perioperative management was conducted according to the treatment protocol developed through the analysis of our experience obtained with 404 thymectomies performed between 1972 and 1986. Importantly, surgical strategy was updated during the study period when extended thymectomy with removal of perithymic fat was adopted instead of simple excision of the gland. This change was justified by international experience and proprietary data on the prevalence of ectopic thymus tissue. The principal features of the treatment protocol are summarized as follows.

In determining the indications for operations, it is our belief that all patients with myasthenia should have the operation unless the necessary preconditions (ie, informed consent from the patient, appropriate cardiorespiratory and hematological status, crisis-free condition, younger than 60 years of age, resectable thymoma) cannot be established or surgery is contraindicated. Nevertheless, surgical treatment is declined in purely ocular or congenital nonprogressive myasthenia. By contrast, the simultaneous occurrence of myasthenia with thymoma is considered a double indication. Although enhanced caution is undoubtedly necessary in elderly patients older than 60 years of age, it is not regarded a contraindication by itself. Approximately half of the patients (47%) with newly diagnosed myasthenia had operations for it during the 10-year period analyzed. Most of the remaining patients who had ocular myasthenia, were in remission or in the inactive stage of the disease, or had a serious accompanying disorder (usually recent myocardial infarction or chronic respiratory disease) were managed by other treatment modalities. The majority of patients older than 60 years of age were managed conservatively. Several patients declined operations.

All surgical patients underwent cholinesterase inhibition, which was suspended for 48 hours after the operation while mechanical ventilation was applied to ensure adequate respiration. This practice is based on the "resting process" principle [13]. It has been observed that a brief withdrawal and then reinstitution of cholinergic medication after a respiratory crisis results in an enhanced therapeutic efficacy explained by the augmentation of the sensitivity of motor endplates during drug withdrawal and mechanical ventilation. An operation is a known precipitating factor of respiratory crisis. Therefore, mechanical ventilation in combination with the withdrawal of the cholinesterase inhibitor for 48 hours was included in the protocol as a preventive measure intended to reduce the incidence of respiratory crises and postoperative mortality. When the duration of respiratory insufficiency exceeds 72 hours, mechanical ventilation is continued through a tracheostomy tube.

Originally the standard practice of our institute was to perform simple thymectomy through total median sternotomy. However, in 1991 this was changed to extended thymectomies (with excision of perithymic fat and the adjacent mediastinal pleura) according to the method of Jaretzki and Wolff [14].

A thymectomy is performed under general anesthesia, and stabilization of the patients is done in the intensive care unit, which usually takes an average of 4 to 5 days.

Preventive antibiotic therapy is administered during ventilatory support. Antimicrobial prophylaxis was initiated in agreement with established professional guidelines to mitigate the risk of nosocomial respiratory infections (eg, pneumonia) and postoperative wound sepsis. During the study period, nosocomial infections have been caused in our institution by streptococcus and staphylococcus strains. Consequently, prophylactic antibiotic treatment was given (ie, usually penicillin and an aminoglycoside are administered in combination).

Adherence to standardized diagnostic and therapeutic principles was guaranteed by the fact that 96% of our patients had follow-ups by the same team of neurologists. Similarly, perioperative care was the responsibility of surgeons and anesthetists of the same institution.

Essential features of the patient population
The mean age of the study population was 34 years (range, 8 to 71 years). Male to female ratio was 3:1 on average; however, substantial differences were observed between individual age groups. Twenty pediatric patients were operated on; the ratio of boys to girls was 1:3. The male to female ratio was 1:5 in the subgroup of patients aged 15 to 40 years and nearly 1:1 in older age groups.

The majority of patients underwent operations within 3 years of the first occurrence of symptoms (Table 1). The subjects were stratified into clinical status categories (Table 2) according to the classification developed by the Myasthenia Gravis Foundation of America (MGFA) [15].


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  		Table 1. Duration of Myasthenic Symptoms (From Onset to Surgery)

 

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  		Table 2. The Patients’ Clinical Condition as Reflected by Myasthenia Gravis Foundation of America Clinical Classification (n = 324)

 
All patients were maintained on anticholinesterase medication until their operations. In the preoperative period, 31 patients received immunosuppressive therapy (azathioprine or steroids, or both), 13 patients were treated with irradiation, and 35 patients by plasmapheresis. Twenty-four patients survived a myasthenic crisis earlier; 18 of these required ventilatory support through tracheostomy in 6 patients. At the time of surgery, 83 patients suffered from at least one accompanying disorder (Table 3). The histologic findings are summarized in Table 4. The prevalence of thymoma was 9.3% in this population; the tumor was accompanied by thymic hyperplasia in 4 patients, and persisting thymic tissue in 5 patients. Thymic tissue could not be identified in the removed thymus glands of 4 patients.


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  		Table 3. Concomitant Diseases at the Time of the Operation

 

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  		Table 4. Histologic Findings

 
The postoperative follow-up of patients was documented until 1998. According to these records, complete remission (absence of symptoms and signs during follow-up despite interrupted treatment) was achieved in 66 patients (20.5%). Forty-four of these patients underwent simple thymectomy, whereas 22 of these patients underwent extended resections; this group did not include any patients with a thymoma or stage IVa or IVb myasthenia. Surgical treatment resulted in obvious improvement in 236 patients (73.3%). In this group, simple thymectomy was performed on 125 patients and extended resection on 84 patients. These subjects included a patient with stage IVa and 16 patients with stage IVb disease, and 27 patients had thymoma. Six of these patients died during the follow-up period from acute exacerbation of myasthenia (respiratory crisis). The condition of 14 patients (4.4%) remained unchanged; 8 of 14 patients underwent simple thymectomies, 5 of 14 patients underwent extended thymectomies, and 1 of 14 patients had thymoma. In addition, 5 of these 14 patients died; 1 patient died from cardiac disease. Myasthenia deteriorated in 6 patients (1.8%); 1 of 6 patients underwent simple thymectomies, 2 of 6 patients underwent extended thymectomies, and 3 of 6 patients had thymomas; in this group, 4 of these patients died.


   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Comment
 References
 
Postoperative adverse events were categorized as either surgical (Table 5) or systemic (Table 6) complications. Recovery was uneventful in 149 patients (46%); complications were mild in 104 patients (32%). Seventy-one patients (22%) suffered serious complications. Two patients (0.6%) died; 1 patient died on postoperative day 6 from unexpected cardiac arrest, and the other patient died on postoperative day 9 from respiratory insufficiency caused by pneumonia.


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  		Table 5. The Prevalence of Surgical Complications in Subgroups Undergoing Simple or Extended Thymectomy, or Removal of Thymoma

 

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  		Table 6. The Prevalence of Systemic Complications in Subgroups Undergoing Simple or Extended Thymectomy, or Removal of Thymoma

 
Surgical complications were ameliorated as follows. Brisk hemorrhage from the sternotomy wound required reoperation in 1 patient. Superficial wound healing problems (seven wound infections, three seromas, and one hematoma) responded to simple incision. Deep soft tissue infections (involving the sternum or mediastinum) did not occur. Intrathoracic complications (hemothorax, pneumothorax, chylothorax, or hydrothorax) were eliminated by tube-thoracostomy or percutaneous needle aspiration. Disruption of the sternotomy wound was observed in a patient afflicted by chylopneumothorax that was managed with drainage. This patient rejected reoperation and spontaneous consolidation of the sternotomy wound took several weeks.

Only tachyarrhythmias associated with supraventricular or ventricular extrasystole were considered cardiac complications. Atrial or ventricular fibrillation did not occur. Sinus tachycardias with heart rates of more than 120 per minute were recorded during mechanical ventilation in 132 patients. Retention of respiratory secretions was diagnosed by auscultation, radiography, bronchological examination, or suctioning in the case of intubated patients. In 7 patients this complication was associated with definite atelectasis of the lower lung lobes. Treatment comprised expectoration assisted by respiratory physical therapy or direct suctioning through a bronchoscope or a catheter inserted through the intratracheal tube. Purulent tracheobronchitis developed primarily in patients (26 of 31) ventilated longer than 24 hours; this was managed by sequential antibiotic therapy. Twenty-two patients had laryngeal damage after translaryngeal intubation for 2 or more days, and 2 patients had laryngeal damage for just 24 hours; this was accompanied by respiratory stridor in 17 of these patients. Laryngeal events were mild in 10 patients, whereas 14 patients had laryngeal events occur either alone or in combination with other complications and required bronchologic intervention, reintubation, or tracheostomy. Three patients developed pneumonia during mechanical ventilation for at least 2 days; 2 of these patients were preceded by the retention of secretions and atelectasis. The duration of postoperative mechanical ventilation is detailed in Figure 1. Seventeen patients were extubated on the operating day. Ninety-six patients were extubated after 24 hours of mechanical ventilation. Except for 1 patient who removed the endotracheal tube inadvertently, the deviation from the treatment protocol was justified by mild myasthenic symptoms and a low dose requirement of the cholinesterase inhibitor. The consequences of the treatment protocol changes were controversial because the endotracheal tube had to be reinserted on the day of extubation in 15 of 113 patients. Among other factors, this might be related to the fact that transient withdrawal of cholinesterase inhibitors was maintained for 48 hours despite early extubation.



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  		Fig 1. Duration of postoperative mechanical ventilation.

 
Respiratory failure was diagnosed when extubation was not feasible after 48 hours of mechanical ventilation because of pronounced myasthenic muscle weakness, abundant respiratory secretions, radiologic changes, abnormalities of arterial blood gases, or dysrhythmia. According to this criterion, 31 patients required prolonged ventilation, whereas 40 patients developed respiratory failure after extubation. Thus reintubation was performed on 46 patients; tracheostomy and reinstitution of ventilatory support was necessary for 19 patients. The principal causes leading to reintubation were increasing myasthenic weakness during the withdrawal of anticholinesterase medication, laryngeal injury resulting from translaryngeal intubation, and cholinergic crisis that occurred in 4 patients after treatment with cholinesterase inhibitors was restarted. In addition, 5 patients had retention of respiratory secretions and extreme muscle weakness that caused respiratory crisis; this was successfully corrected by bronchoscope suctioning without reintubation or ventilatory support. In total, 40 bronchoscopic interventions were performed on 28 patients for diagnostic or therapeutic purposes, or both. Anemia (a hematocrit value of 0.30 or less) was diagnosed in 112 patients; 60 of these patients received packed red blood cells (1 to 3 U). Also, according to clinical indications, blood transfusions were administered to 49 patients with hematocrit values of more than 0.30. The source of serious blood loss was postoperative bleeding from the sternotomy wound in 1 patient, and another patient developed gastric hemorrhage.


   Comment
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
References
 
Postoperative complication rate was always an essential argument in the controversy between the advocates of transcervical versus transsternal access for thymectomy. This is no surprise because initial series of partial or total sternotomy were associated with an early mortality rate of 5% to 30% [6, 9, 11, 12, 16–19], which is rather high by current standards. However, by the 1970s there was a better understanding of the pathophysiology of myasthenia gravis, improved selection and preparation of surgical candidates by experienced teams of neurologists, and an impressive progress of surgical technique, anesthesiology, and intensive therapy that reduced mortality (range, 0% to 2%) [2–5, 7, 10, 11, 20–24]. Notwithstanding this fact, the majority of authors neglect the explication of their morbidity statistics. Only five reviews discuss nonfatal complications in detail [2, 3, 7, 22, 24]. The shortage of valid reference information makes it difficult to interpret our results and compare data. The lack of standardized criteria causes additional confusion in the calculation of complication rates. In our series, 112 patients had hematocrit values at 0.30 or less. Therefore, if the arbitrary threshold for diagnosing anemia is set at 0.25, only 14 of these patients were afflicted by this complication. Furthermore, several complications cannot be quantified objectively and this makes the comparison of published data almost unreasonable. Examples of this category include retention of respiratory secretions, laryngeal injury, and upper airway infection. Monitoring and meticulous registration of these complications is nevertheless considered important to enhance in-house quality assurance.

It is unclear whether respiratory insufficiency should be deemed a complication or not. This phenomenon is an inherent component of the myasthenic crisis; it is a typical feature that can occur even if myasthenia gravis is treated noninvasively. In the early days of thymectomy, myasthenic crisis was a dreaded complication that made ventilatory support compulsory, almost invariably through tracheostomy, and this made the substantial reduction of operative mortality possible [6, 18]. Considering the diverse outcomes of various surgical methods and perioperative management protocols, the relationship between individual treatment options and the risk of respiratory insufficiency, which is thus regarded as a complication, must be elucidated.

The following incidences of surgical complications are quoted in the literature: bleeding, 0.5% [2]; wound infection, 1% to 7% [2, 3, 7, 20–22, 24]; chylothorax, 0.5% [2] to 1% [22]; sternal disruption, 1% to 4% [22, 24, 25]; thoracic empyema, 1% [22]; mediastinitis, 1.6% [3]; hydrothorax, 4% [7] to 4.5% [2]; pneumothorax, 2% [7]; injury to the phrenic nerve, 0% to 4.5% [2, 10, 20–22, 24, 26]; and damage to the recurrent nerve, 0% to 4.5% [2, 22, 24, 26].

None of the other publications mention laryngeal injury among systemic complications. In addition, occasional quoted complications include anemia requiring transfusion, 1% [2]; tracheal injury, 3.5% [6]; retention of respiratory secretions, 10% [27, 28]; atelectasis, 7% [27, 28]; pulmonary embolism, 1% [2, 22]; deep venous thrombosis, 1% [7]; and subclavian vein thrombosis, 1% [7]. According to the literature pneumonia develops in 1% to 4% of patients [2, 7, 21, 24, 29] or even as much as 14.4% of patients [3]; whereas upper airway infections afflict 1.5% [2] to 35% [24] of surgical patients. Cardiac arrhythmia is mentioned in the 1% to 2% rate [3, 7, 27].

Operative morbidity varies in range between 4% and 33% [2, 21, 22, 25, 29–31].

Several authors place special emphasis on the relationship between respiratory insufficiency and ventilatory support; some specify the incidence of this complication accurately: 6% [2], 10% [21, 27], and 33% [32], whereas others only can be estimated rather inaccurately from the duration of ventilatory support [7, 8, 10, 26, 29, 31, 33–35] and the rate of reintubations [7, 24, 25, 29]. The comparisons of meager data are very difficult because the criteria applied for the calculation of the incidence rates of respiratory insufficiency are not described in any of the cited articles. The rate of tracheostomy varies between the extremes of 0% and 100% [6–8, 10–12, 18, 19, 24, 31, 36]. However, this tells nothing about the incidence of respiratory complications because many authors performed preventive tracheostomy to eliminate the risk of respiratory insufficiency. High tracheostomy rates were typical of surgical series published before the 1980s. The 6% incidence found in our patient population seems acceptable; however, in 8 patients the indication for tracheostomy was laryngeal injury from prolonged translaryngeal intubation that had occurred alone or in combination with other airway complications. As demonstrated in prospective endoscopic studies, long-term translaryngeal intubation is associated with a high complication rate [37]. Edematous swelling of the mucosa, granuloma formation, or thick secretions usually does not cause significant difficulties in the breathing of patients with an intact musculature. However, these laryngeal complications can precipitate a respiratory crisis in myasthenia and especially in patients with predominant weakness of oropharyngeal or respiratory muscles. Tracheostomy may become necessary to preclude further traumatization of the larynx [38].

Although many efforts have been made to identify patients at high risk of postoperative respiratory insufficiency, none of the selected predisposing factors was of sufficient predictive value [39]. Owing to the largely unknown and unpredictable nature of myasthenia and as suggested by early surgical experience, there are two theoretical alternatives available for postoperative ventilation: (1) All, or the majority, of patients should receive mechanical ventilation for shorter or longer periods [6, 8, 18, 23, 28, 31, 33]; and (2) The vast majority of patients can be safely extubated shortly after an operation, and permanent ventilatory support is necessary only when respiratory crisis develops [7, 10, 25, 27, 32, 35, 36, 39, 40]. The management protocol adopted by our institute in 1972 is based on the former alternative, and in regard to perioperative mortality rates it has been applied with satisfactory results. However, morbidity rates associated with respiratory insufficiency and other airway complications are higher in our series than the corresponding data from other authors.

Thus, the analysis of our mortality and morbidity statistics and their comparison to relevant information published in the literature leads to the following conclusions. Simple or extended thymectomies are both associated with essentially identical complication rates. The lower than 1% mortality rate found in this series is similar to data from operative statistics obtained on large patient populations undergoing transsternal thymectomies. The incidence of surgical complications in our series stands comparison with data from the literature. However, some of the systemic complications (ie, respiratory insufficiency, airway-associated morbidity, and anemia) occurred more frequently or deficient information precluded comparison to data from other sources. The 48-hour ventilatory support and simultaneous withdrawal of anticholinesterase medication are important elements of our postoperative management protocol. Nevertheless, an etiologic (at least partial) relationship between these interventions and the high frequency of respiratory insufficiency and airway-associated morbidity can be postulated. The lack of sufficient reference data precludes comparing the incidence of reintubation and blood transfusions in our series and in other patient populations. Nevertheless, the proportion of patients requiring transfusion seems extraordinarily high in our series. Bronchoscopy was an invaluable tool for the diagnosis and management of airway-associated morbidity. In view of the previous information, the following amendments to our postoperative management protocol seem reasonable. The duration of postoperative ventilatory support (currently 48 hours) and withdrawal of anticholinesterase medication should be reduced substantially along with the number of blood transfusions. The ultimate goal is to decrease operative morbidity significantly while maintaining perioperative mortality at the current low level.


   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Comment
 References
 

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Thymectomy for Myasthenia Gravis: 12-Year Experience
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