Thymoma in patients with MG
Characteristics and long-term outcome
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Abstract
Objective: To examine the characteristics of thymoma when associated with MG and to evaluate those conditions that can complicate management and affect survival.
Methods: The study includes 207 myasthenic patients who were operated on for thymoma, with at least 1-year follow-up from surgery. MG severity and response to treatment, the occurrence of paraneoplastic diseases and extrathymic malignancies, thymoma histologic types and stages, adjuvant therapy, tumor recurrences, and causes of death were recorded.
Results: MG-associated thymoma was predominantly of B type and was invasive in the majority of patients. MG was generally severe, and most patients remained dependent on immunosuppressive therapy. Other paraneoplastic disorders and extrathymic malignancies were found in 9.66 and 11.11% of patients. Thymoma recurrences occurred in 18 of 115 patients with invasive tumors (15.65%) and were often associated with the onset/aggravation of autoimmune diseases. On completion of the study, MG and thymoma accounted for a similar mortality rate.
Conclusions: Thymoma should be considered as a potentially malignant tumor requiring prolonged follow-up. The presence of myasthenic weakness can still complicate its management. Thymoma-related deaths are bound to outnumber those due to MG in the future.
Thymomas are thymic epithelial tumors, generally characterized by an indolent growth with local invasiveness; distant metastases are distinctly uncommon.1 Tumor stage, extent of surgical resection, and histology are the accepted criteria in predicting survival.2,3⇓
It is well known that thymoma patients can develop different paraneoplastic disorders, of which MG is by far the most common.4 Some of these diseases improve after thymoma removal.5 Others are not significantly affected and may even present after surgery6,7⇓; they often require treatment of their own and may carry a poor prognosis. An increased risk for malignancy has also been reported in association with thymoma.8
The presence of myasthenic weakness was previously considered an aggravating factor, as it represented an increased risk for surgery and an independent cause of mortality.9 Nowadays, thanks to improved management, MG no longer represents an adverse prognostic factor; instead, it appears to confer a survival advantage due to earlier diagnosis of the tumor, closer follow-up, and possible beneficial effect of steroids, which are widely used for the treatment of the disease.10 Conversely, the presence of thymoma is thought to worsen the prognosis of MG, as symptoms are usually severe in these patients and are not significantly improved by thymectomy.11,12⇓
We reviewed a large cohort of subjects with MG who underwent thymectomy for thymoma. Our purpose was to examine the characteristics of this tumor when associated with MG and evaluate those factors that can complicate management and affect outcome.
Methods.
This is a retrospective study spanning from 1972 to 2001. It includes subjects with MG who were operated on for thymoma with at least 1-year follow-up from surgery. All but 10 patients were operated on in our institution; all were treated for MG in our department.
MG and associated diseases.
The diagnosis of MG was based on the association of clinical data with at least two of these features: positive response to anticholinesterase injection, electrophysiologic signs of neuromuscular transmission defect, detectable antiacetylcholine receptor antibodies. Disease severity was graded according to the Myasthenia Gravis Foundation of America (MGFA) clinical classification.13
Treatment was administered according to the accepted guidelines14,15⇓: anticholinesterases constituted the sole pharmacologic therapy in mildly affected subjects; immunosuppressive therapy was performed in patients with disabling disease, using oral corticosteroids (prednisone) generally associated with azathioprine. Prednisone was usually started at a high daily dosage (0.8 to 1 mg/kg), gradually shifting to an alternate-day schedule, followed by progressive reduction to the minimum maintenance dose or withdrawal. Azathioprine was used at a starting dose of 2.5 to 3 mg/kg/d and was gradually reduced to the maintenance dose of ≤1 mg/kg/d. Cyclosporine A at a dosage of 3 to 4 mg/kg/d was used in patients with contraindications or unsatisfactory response to azathioprine. Recently, mycophenolate mofetil in association with prednisone was employed in selected patients unresponsive to other immunosuppressants.16 Plasma exchange (PE) and IV immunoglobulin (IVIG) were used in association with immunosuppressive therapy in treating severely ill patients, in preparation for surgery and, more rarely, as periodic treatment.
During the follow-up period, changes in disease severity, therapeutic regimens, and side effects of treatment were monitored. In the presence of symptoms/signs or laboratory findings of associated diseases, patients underwent specific diagnostic tests. The occurrence of paraneoplastic diseases and their treatment, extrathymic malignancies, and causes of death were recorded.
Thymoma staging system and treatment.
Tumor extent at surgery was evaluated on the basis of written surgical records and pathologic findings and was graded according to the Masaoka system (Stage I: macroscopically encapsulated and no microscopic capsular invasion; Stage II: macroscopic invasion into adjacent tissue—fatty or mediastinal pleura—or microscopic capsular invasion; Stage III: macroscopic invasion into adjacent organs; Stage IVa: pleural/pericardial dissemination; Stage IVb: lymphogenous/hematogenous metastases).17
Histologic diagnoses were reviewed using hematoxylin/eosin-stained sections and were reclassified according to the World Health Organization classification.18 Table 1 summarizes the definitions of World Health Organization classification together with its prognostic and functional implications.4,19⇓ The morphology of the residual thymus was also noted. Nineteen cases remained unclassified as pathologic slides were not available (17 patients) or because of extensive tumor necrosis (2 patients).
Table 1 Definitions of World Health Organization classification of thymic epithelial tumors
The surgical approach was by posterolateral thoracotomy in five cases; median sternotomy followed by extended thymectomy was performed in all the remaining patients. Extended thymectomy included complete resection of the thymoma along with the thymic gland and perithymic fat tissue; when necessary, it was associated with resection of the pleura, pericardium, lung, phrenic nerve, and pleural implants.
Mediastinal irradiation at a dose ranging from 45 to 55 Gy was performed postoperatively in patients with invasive thymoma, except in eight patients, three of whom did not receive radiotherapy because of a too disseminated tumor. Chemotherapy was carried out according to standard cisplatin-based protocols consisting of doxorubicin (50 mg/m2 IV day 1)/cyclophosphamide (500 mg/m2 IV day 1)/cisplatin (50 mg/m2 IV day 1) or etoposide (100 mg/m2 IV days 1 to 3)/cisplatin (80 mg/m2 IV day 1); cycles were repeated every 3 weeks. Chemotherapy was used preoperatively in three and postoperatively in six patients with Stage III and IVa thymoma.
Tumor surveillance was performed with chest CT/MRI every 1 to 2 years.
Thymoma recurrence: diagnosis and treatment.
Recurrences were radiologically diagnosed; in patients who did not undergo further surgery, histologic diagnosis was made by needle or open biopsy.
Treatment was based on tumor extension. Surgical resection was performed whenever feasible, followed by radiotherapy when it had not been done at the time of the first operation. Chemotherapy was administered in patients with Stage III to IV disease. In patients who had received cisplatin-based chemotherapy, other regimens were used: single-agent ifosfamide (1.5 g/m2 IV days 1 to 5), every 3 to 4 weeks, in two cases and the combination of cyclophosphamide (600 mg/m2 IV day 1)/procarbazine (100 mg/m2 PO days 1 to 14)/vincristine (1.4 mg/m2 IV day 1), every 4 weeks, in two other patients.
Results.
Our cohort comprised 207 patients: 105 males and 102 females with age at thymectomy ranging 11 to 75 years (mean 47.66 years). Except for six patients who died within 30 days of surgery, follow-up at completion of the study (December 2001) ranged from 1 month to 29 years (mean 10.1 years, median 8.25 years). At the end of the observation period, 141 patients were alive, 50 had died, and 16 had been lost to follow-up.
Thymoma histologic types and stages.
Of 207 patients, 92 (44.44%) had a noninvasive (Stage I) thymoma and 115 (55.56%) an invasive tumor: it was in Stage II in 64 cases (30.92%), in Stage III in 45 (21.74%), and Stage IVa in 6 (2.90%).
The onset of MG preceded the detection of thymoma in 194 patients; in this group, the rate of invasive tumors was 53.61% (104/194). Thirteen subjects developed MG 0.5 to 10 years after thymectomy; an invasive tumor was found in 11 of these cases (84.61%).
Thymoma was correctly diagnosed on CT scan, except in four MG patients. In two of these, the tumor was found intraoperatively as a small nodule within a hyperplastic thymus; in the other two patients, who, being older than 60, had not been considered as candidates for therapeutic thymectomy, thymoma was diagnosed by a second CT scan 1 year after the first examination.
Histology was evaluated in 188 patients, of whom 112 were taking immunosuppressive drugs at the time of thymectomy. Tumor subtypes were the following: type A in 4 patients (2.13%), type AB in 19 (10.11%), type B1 in 42 (22.34%), type B2 in 104 (55.32%), type B3 in 6 (3.19%), and combined B2/B3 in 12 (6.38%); 1 patient (0.53%) was found to have a combined tumor consisting of a mixed B2/B3 thymoma and a nonorganotypic high-grade carcinoma. Histologic types and tumor stages are shown in table 2. Thymoma was, in most cases, constituted by a single nodule, with maximum diameter up to 11 cm; in five cases, multiple macroscopic nodules were found. Thymic remnants showed changes of lymphofollicular hyperplasia in 69 cases (36.70%).
Table 2 Tumor histology and stage at thymomectomy
MG course and treatment.
The maximum MG severity was the following: purely ocular myasthenia (MGFA Grade I) in 4 cases (1.93%), mild generalized disease (Grade II) in 56 (27.06%), moderate disease (Grade III) in 78 (37.68%), and severe disease (Grade IV) in 22 (10.63%); 47 (22.70%) patients experienced, during the course of the disease, one or more respiratory crises requiring assisted ventilation (Grade V).
Of the194 patients who were affected with MG before thymectomy, 40 (20.62%) experienced a deterioration in the disease in the first year after surgery, requiring the start of immunosuppressive treatment or an increase in drug dosage.
A total of 169 patients of 207 (81.64%) received immunosuppressive treatment during the observation period.
The course of MG reflected the changes in the disease management between the 1970s and later decades. In the earlier period, MG-related mortality was higher and the disease course was generally brittle with frequent phases of deterioration occurring mainly in the first years from onset. In recent decades, more patients have achieved good control of their disease, although they generally remain dependent on immunosuppressive therapy.
Outcome was evaluated in 185 cases who had completed follow-up or had survived for at least 1 month after surgery. At the end of follow-up (or at the time of death), 143 patients were still on immunosuppression: 49 were treated with prednisone, 73 with prednisone and azathioprine, 12 with azathioprine alone, 5 with prednisone and cyclosporine, and 3 with prednisone and mycophenolate mofetil. Forty patients were asymptomatic, but only 17 of them had achieved drug-free remission; 12 still had disabling weakness, despite high-dose immunosuppression and periodic treatment with PE and IVIG; 8 had died of MG; those remaining were still symptomatic with mild to moderate symptoms.
Thymoma recurrences.
Neither patients with Stage I thymoma nor patients with type A or AB thymoma, irrespective of stage, experienced tumor relapses. One or more recurrences occurred in 18 of 115 cases (15.65%) with invasive tumors: in particular, in 4 of 64 (6.25%) patients in Stage II, in 10 of 45 (22.22%) in Stage III, and in 4 of 6 (66.66%) in Stage IVa.
The clinical characteristics and outcome in patients with recurrences are shown in table 3.
Table 3 Clinical characteristics of patients with thymoma recurrences
In patients with thymomas (from Patients 1 through 17), the interval between thymectomy and detection of recurrences ranged from 2 to 16 years, being generally shorter in the case of more advanced tumors (the mean time interval was 8.50 years for Stage II, 5.77 years for Stage III, and 3.25 years for Stage IVa thymomas). Five patients had tumor relapse two or even three times. Recurrences arose intrathoracically, although in two patients (Patients 6 and 9), they spread contiguously into the abdomen and the epidural space. Histology was the same as the first tumor, but recurrences often showed a higher grade of cellular atypia and fewer lymphocytes.
Four patients with one to two mediastinal masses underwent complete surgical resection: three of them were tumor-free at the last control, and one developed disseminated intrathoracic disease. Eleven patients with multiple nodules were treated with subtotal surgery and chemotherapy or with chemotherapy alone; three of them were tumor-free at the last control. Two patients refused any treatment (Patients 16 and 17): one survived 7 years, and the other died of unrelated causes.
In the patient whose first tumor showed combined features of B2/B3 thymoma and carcinoma (Patient 18), hematogenous metastases (in bone and liver) were diagnosed 6 months after surgery. This patient died shortly afterward. Histologic examination of the autopsy material revealed that recurrences had originated from the carcinomatous component of the first tumor.
Relapse of thymoma affected the course of MG differently. In three patients, the onset of myasthenic symptoms occurred together with the first or even the second tumor recurrence. Seven patients—all receiving immunosuppressive treatment—had deterioration in MG that was severe in two cases (Patients 7 and 11). The other patients remained in good control of their disease, including three subjects who had achieved drug-free remission (Patients 9, 13, and 15).
The onset of pure red cell aplasia (PRCA) was associated with a second thymoma recurrence (Patient 6); 10 months later, this patient also developed neuromyotonia (NMT).
Thymoma-related deaths were observed in seven of these patients.
Associated diseases.
Other autoimmune diseases were diagnosed in 20 of 207 patients (9.66%). Five subjects had a combination of two or more disorders listed in table 4.
Table 4 Associated autoimmune diseases
NMT was diagnosed on the basis of muscle cramps and myokymia associated with electromyographic finding of spontaneous firing of single motor units as double, triple, and multiple discharges; serum anti-voltage-gated potassium channel (anti-VGKC) antibodies were positive in one of the four affected patients. In these subjects, NMT was a transient disease, with a florid phase of 2 to 3 months, after which symptoms slowly subsided. Two patients with painful muscle cramps were treated with PE and oral phenytoin; both were able to discontinue treatment.
Limbic encephalitis (LE) was characterized by severe impairment of recent memory and tonic-clonic seizures, associated with brain MRI changes consisting of increased signal of both hippocampal areas on T2-weighted images; serum anti-Hu and anti-VGKC antibody levels were both negative. This patient, after treatment for thymoma, while recovering from LE, developed NMT and subsequently MG.
The two cases of vitiligo and one case of glomerulonephritis preceded MG and thymoma by several years; LE and pemphigus were diagnosed together with thymoma and improved with its treatment; PRCA occurred at the time of tumor recurrence; the onset of the other diseases was after thymectomy, with a time interval ranging from 2 months to 17 years. Most of these diseases occurred in patients on immunosuppression and required further increase in drug dosage. In some cases, they represented a serious aggravation of clinical status: the patient with PRCA is still dependent on transfusions despite treatment with steroids and cyclosporine; autoimmune thrombocytopenia was followed by B-cell lymphoma. One patient died of septicemia during cyclophosphamide treatment for membranous glomerulonephritis.
Twenty-three of 207 patients (11.11%) developed 25 extrathymic malignancies. Five tumors were diagnosed at the same time as the thymoma, and the others occurred after thymectomy (table 5). Twenty-one tumors occurred in patients under immunosuppression, 13 in subjects who had received radiotherapy. Four patients died of extrathymic malignancy.
Table 5 Extrathymic malignancies
On completion of the study, 50 patients had died. Table 6 shows the causes of death. Most MG-related deaths were observed within 3 years of surgery, whereas thymoma-related mortality, being linked to tumor recurrences, occurred later, except in the patient with metastatic thymic carcinoma. Iatrogenic deaths that occurred in the first months after surgery were observed in the 1970s and were due mainly to side effects of steroids or prolonged assisted ventilation; later iatrogenic deaths were related to infectious complications of immunosuppressive treatment. Seven patients died of sudden death, having shown no previous signs of cardiac disease.
Table 6 Causes of death
Discussion.
The association of thymoma with autoimmune diseases has been related to the intratumorous generation of mature T cells, although the pathogenic mechanisms leading to the various paraneoplastic disorders are probably different.20 In agreement with other authors,3,4,19⇓⇓ we found MG to be most commonly associated with B thymomas and to a lesser extent, with the AB subtype, that is, with functional tumors in terms of inducing T-cell maturation. The high proportion of B2/B1 tumors in our series could in part be related to histopathologic changes induced by preoperative steroid treatment.21
It has been reported that subjects with MG have less advanced thymomas than thymoma patients without MG, as the presence of neuromuscular symptoms favors an earlier detection of the tumor.2,10⇓ Our data confirm this view. First, we found a striking difference in the tumor stage between patients who had been diagnosed as myasthenic before and those who developed MG after thymectomy. Second, when compared with other studies including patients with and without MG, our series was characterized by a reduced rate of invasive tumors10,22⇓ or at least by a lower proportion of advanced (Stage III and IV) disease.2,23⇓ Nevertheless, an invasive thymoma was still present in the majority of our patients.
The risk that small thymomas escape radiologic diagnosis is particularly relevant when thymectomy is not indicated for the treatment of MG (i.e., elderly patients, ocular myasthenia); in these cases, we think it worthwhile to perform a control CT scan at a later date and look for tumor serologic markers. Serum antibodies against muscle antigens such as titin have been reported to be predictive of the presence of thymoma,24 especially in patients under 60.25
The treatment of completely capsulated thymoma is limited to surgery, given the very low recurrence rate at this stage, whereas postoperative radiotherapy is generally recommended for more advanced disease, even for completely resected Stage II tumors.26 Our experience confirms this indication, as three of four relapsing Stage II tumors had not been irradiated at the time of the first operation. For patients with Stage III and IV thymoma, chemotherapy, generally performed via platinum-based regimens, has been used with encouraging results.27,28⇓
Our data confirm the importance of invasiveness and histology in determining tumor relapses (both the recurrence rate and the interval to recurrence were related to the Masaoka stage; only B subtypes relapsed). As thymoma can recur after a long interval, oncologic surveillance must be prolonged and even lifelong. In the absence of definite guidelines, follow-up consists of periodic radiologic examinations; a serologic marker for thymoma recurrence can be provided by serum antibodies against interferon-α and interleukin-12, as recently reported.25 The finding that secondary thymomas can support T-cell maturation29 is in accordance with their possible association with the onset/aggravation of autoimmune disorders.
Treatment of recurrences is not yet codified and includes surgery and adjuvant therapies. In our and others’ experience,30,31⇓ reoperation, even for repeatedly recurrent thymomas, has proven effective in prolonging survival. Although patients with disseminated disease showed an overall poor prognosis, survival was prolonged even in untreated cases. A much more malignant course was observed in the only patient with combined B2/B3/C tumor, in whom the carcinomatous component of the first tumor gave rise to early hematogenous metastases.
Although the oncologic prognosis of thymoma is more favorable in MG than in non-MG patients, the coexistence of myasthenic weakness should be regarded as a risk factor as both the disease and its treatment still contribute to mortality. In our and others’ experience,11,32⇓ thymoma-associated MG is generally a severe disease whose current good prognosis depends mainly on immunosuppressive therapy. In agreement with previous reports,12,33⇓ thymectomy did not significantly improve the course of the disease, which in a proportion of patients reached its maximum severity after surgery; moreover, aggressive thoracic surgery for recurrent thymoma represents a serious risk in these patients, requiring adequate preparation and careful postoperative monitoring.
In our series, NMT was the most frequent neurologic disorder apart from MG; it was altogether a benign disease, which responded well to symptomatic therapy. Anti-VGKC antibodies are considered to be pathogenic in both NMT34 and thymoma-associated LE.5 These antibodies tested negative in the subject affected with both NMT and LE, although in this patient, CNS dysfunction was reversed by thymoma treatment,35 suggesting that thymoma can elicit antibodies directed against CNS antigens other than VGKC.
The association with non-neurologic paraneoplastic diseases is of prognostic significance. In particular, disorders of hematopoiesis represent severe complications, as they are often refractory to treatment.36 It is also worth noting that a number of patients in our series died of sudden death; although autopsy studies were not performed, it is possible that some of these cases were affected by myocarditis, which could have been responsible for fatal arrythmia.37
The reported association of thymoma with a higher incidence of second malignancy8 represents an additional reason for accurate follow-up of these cases. The percentage of subjects with extrathymic cancers in our series (11.11%) was within the values observed by others, ranging from 8 to 33%.8,10,38⇓⇓ The thymoma-associated oncologic risk appears to be intrinsic, rather than related to other factors such as MG, thymectomy, and radiotherapy10,38⇓; however, we cannot exclude that, in our population, some extrathymic malignancies were related to long-term immunosuppression.
In our series, MG and thymoma account for a similar death rate; however, it should be considered that the current MG-related mortality is lower, our results being flawed by the inclusion of patients treated in the 1970s; conversely, deaths due to thymoma are likely to increase in future studies. From our experience, MG-associated thymoma is, in most cases, a potentially malignant tumor that requires prolonged follow-up and can affect survival both directly and indirectly.
Acknowledgments
Acknowledgment
The authors thank Prof. Angela Vincent of the Institute of Molecular Medicine, John Radcliffe Hospital, Oxford, UK, for having dosed anti-VGKC antibodies.
- Received April 12, 2002.
- Accepted July 23, 2002.
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