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Eur J Cardiothorac Surg 2007;31:731-736. doi:10.1016/j.ejcts.2007.01.024
Copyright © 2007, European Association for Cardio-Thoracic Surgery. Published by Elsevier B.V. All rights reserved

Role of flourine-18 fluorodeoxyglucose positron emission tomography in thymic pathology

Hatem El-Bawaba,*, Abdul Aziz Al-Sugaira, Mohammed Rafaya, Wassem Hajjarb, Mohammed Mahdya, Khaled Al-Kattana,b

a King Faisal Specialist Hospital & Research Centre, Riyadh, Saudi Arabia
b King Khaled University Hospital, Riyadh, Saudi Arabia

Received 30 August 2006; received in revised form 21 December 2006; accepted 15 January 2007.

* Corresponding author. Address: King Faisal Specialist Hospital & Research Centre, Department of Surgery (MBC 40), P.O. Box 3354, Riyadh 11211, Kingdom of Saudi Arabia. Tel.: +966 1 442 7776; fax: +966 1 442 7772. (Email: hysahmed{at}gmail.com).


   Abstract
Top
 Abstract
1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 5. Conclusion
 Appendix A
 References
 
Objective: To evaluate the utilization of positron emission tomography (PET) scan with fluorine-18 fluorodeoxyglucose (FDG) in thymic pathology. Methods: Twenty-five consecutive patients with thymic pathology underwent FDG–PET after being evaluated by computed tomography (CT). The indication for CT was myasthenia gravis in 10, anterior mediastinal mass in 7, and recurrent thymic tumor after surgical excision in 8 patients. The results of PET were compared with results obtained by CT, and histopathologic examination of the surgical specimens. Results: All mediastinal abnormal thymic tissue showed FDG uptakes. FDG–PET managed to differentiate between thymic hyperplasia and thymoma in myasthenia gravis group (n = 10) in which CT images were questionable in two patients. There was one case of ectopic thymic tissue which was not diagnosed preoperatively. There were no false-negative results for both CT and FDG–PET in seven patients with thymoma presented as anterior mediastinal mass. However, PET scan predicted thymic carcinoma in one patient. PET was superior to CT scan in localization of recurrent thymoma in two patients, and equal to CT in detecting metastatic lesions in six patients during the follow-up after thymoma excision. Conclusions: In myasthenia gravis, selective use of FDG–PET is useful in differentiating thymoma from hyperplasia, especially when CT scan is controversial, but fails to recognize ectopic thymic tissue. FDG–PET may differentiate thymoma from thymic carcinoma. FDG–PET is also useful in follow-up patients, who underwent thymoma excision, when there is suspicion of recurrence or metastasis.

Key Words: Thymoma • Thymic hyperplasia • Thymic carcinoma • Positron emission tomography • Computed tomography


   1. Introduction
Top
 Abstract
 1. Introduction
2. Materials and methods
 3. Results
 4. Discussion
 5. Conclusion
 Appendix A
 References
 
Thymectomy has been an established treatment modality for both myasthenia gravis (MG) and patients with thymic tumors.

In MG, efforts were made to determine predictors of response to thymectomy in order to maximize benefit through careful patient selection. Of those predictors, thymic histology was found to correlate statistically with patient outcome after thymectomy [1].

Thymic tumors, in the form of thymoma or thymic carcinoma, are common neoplasms in the anterior mediastinum. Several proposed classifications have been designed to correlate the histopathology and the clinical course of these tumors to anticipate prognosis. Rosai and Sobin [2] published the world health organization (WHO) histologic classification of thymic epithelial tumors. The WHO histologic classification [2,3] and the clinico-pathologic staging system proposed by Masaoka et al. [4] have been reported to reflect the oncological behavior of thymoma and hence the prognosis.

Preoperative identification of the histologic subtype and stage of thymic pathology has important implications on the management strategy. The preoperative radiological evaluation plays a major role in differentiation between thymic hyperplasia, thymoma, and thymic carcinoma.

Computed tomography (CT) imaging of the mediastinum provides fairly accurate information about benign and neoplastic lesions of the thymus. However, definite differentiation between histologic subtypes of thymic pathology by CT is occasionally difficult.

Positron emission tomography (PET) using fluorine-18 flourodeoxyglucose (FDG) has emerged as a diagnostic tool for staging and restaging of several neoplasms.

The purpose of our study is to evaluate the role of FDG–PET in differentiation of various thymic pathologies and to evaluate its impact on management.


   2. Materials and methods
Top
 Abstract
 1. Introduction
 2. Materials and methods
3. Results
 4. Discussion
 5. Conclusion
 Appendix A
 References
 
During the 2-year period, from July 2003 to July 2005, 25 consecutive patients with thymic pathology, undergoing thymectomy or related surgical resection, were included in our study. There were 19 females (74%) and 6 males (24%), with an average age of 35.1 ± 14.34 years (range from 14 to 72 years).

All patients were evaluated by history, clinical examination, chest X-ray and CT chest before surgery. For all myasthenic patients, in addition to radiological evaluation, our policy is to perform Tensilon test and anti-acetylcholine receptor antibodies test.

Eight patients (32%) were asymptomatic. There was coincidental finding of anterior mediastinal mass on chest X-ray in two patients (8%). The remaining six patients (24%) were diagnosed to have metastasis during follow-up after surgery for invasive thymoma.

Twelve patients (48%) presented with symptoms and signs of MG. In 10 patients (40%), myasthenic symptoms and signs were their first presentation. In two patients, symptoms and signs of myasthenia gravis did not improve after surgical excision of invasive thymoma.

Other symptoms included chest pain (5/25, 20%), dyspnea (2/25, 8%), and weight loss in one patient (4%). Table 1 shows the clinical characteristics, CT diagnosis, FDG–PET findings, and final histopathological results.


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  		Table 1 Patient characteristics, CT findings, FDG–PET findings, postoperative histopathological reports and staging
 
The CT criteria for diagnosis of thymic hyperplasia, thymoma, and thymic carcinoma were reported by Tomiyama et al., Han et al., and Jeong et al. [5–7].

The chest radiologists assessed the CT scans for the location, size, shape, marginal characteristics, homogenicity, attenuation (compared with chest wall muscle), and degree of tumor enhancement. The presence of tumor necrosis and calcification and associated findings, if any, were also recorded.

Surgical approaches included, median sternotomy and maximal thymectomy in 16 patients, and median sternotomy and excision of mediastinal mass, anterior surface of pericardium, anterior left and right mediastinal pleurae, and pericardial and diaphragmatic fat in 1 patient diagnosed with thymic carcinoma. Redo-sternotomy was performed in two patients with mediastinal recurrence of myasthenia gravis. Right thoracotomy was performed in six patients with thymoma recurrence. Metastectomy was performed in five patients, and metastectomy and middle lobectomy in one patient.

The 25 patients included in our study had FDG–PET scans before surgery. All surgical specimens were subjected to histopathological examination. Preoperative radiological observations from CT, intraoperative data, and histopathology results were compared with FDG–PET findings.

Masaoka classified thymoma as stage I completely encapsulated thymoma without microscopic invasion of the capsule; stage II macroscopic invasion of the mediastinal fat or pleura (IIa) or microscopic invasion of the capsule (IIb); stage III macroscopic invasion of the pericardium, great vessels or lung; and stage IV pleural or pericardial dissemination (IVa) and lymphatic or hematogenous metastasis (IVb). Stage I thymomas are noninvasive.

2.1 PET protocol
The patients fasted for at least 4 h prior to scanning. The blood glucose level was measured 30 min prior to study. There were no patients with blood glucose level more than 8 mmol in this study. 370 MBq (10 mCmi) of FDG was injected intravenously. The patients rest for about 45–60 min prior to scanning. The patients were scanned for about 1 h from the base of the skull to mid-thigh region with arms up. Imaging fields were about 3–6 bed positions. Time per bed was about 8 min (5 min emission, 3 min transmission). The region of interest (ROI) was measured using standardized uptake value (SUV).


   3. Results
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
4. Discussion
 5. Conclusion
 Appendix A
 References
 
The patients were classified into three groups based on clinical and radiological data. The first group included patients with MG. The second group included patients with anterior mediastinal mass. The third group included patients who were followed up after surgery for thymic pathology. These patients either had recurrence of MG or were diagnosed to have metastasis.

In patients with myasthenia gravis (n = 10), histopathological examination of the surgical specimen showed that two patients had stage IIa thymoma. One patient had ectopic thymic tissue in the mediastinal fat. The remaining eight patients had hyperplasia of the thymus.

In the second group with anterior mediastinal mass (n = 7), the histopathology results of surgical specimen proved that six patients had thymoma stages I, II, and III, and one patient had thymic carcinoma (Table 1).

In the third group (n = 8), two patients had persistent myasthenic symptoms. The histopathology showed local recurrence of thymoma. The remaining six patients who had surgical excision in the past for either invasive thymoma (n = 4) or thymic carcinoma (n = 2) were found to have metastasis that was proved histologically.

In group I with myasthenic symptoms, CT could not differentiate between thymic hyperplasia and thymic neoplasm in two patients. In case 4, FDG–PET observation showed homogenous diffuse uptake in the anterior mediastinum with SUV of 2.1, suggestive of hyperplasia. Patient underwent thymectomy and histopathological examination of the surgical specimen confirmed the presence of hyperplasia. In case 9, FDG–PET was in favor of invasive thymoma (Table 1) that was confirmed postoperatively to be invasive thymoma stage IIa due to invasion of the capsule and contiguous pleura (Fig. 1 ).


Figure 1
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  		Fig. 1. A 33-year-old female with stage IIa thymoma (case 9). (A) Axial CT shows solid homogenous mass in the anterior mediastinum. (B) FDG–PET shows intense FDG uptake in the anterior mediastinum and contiguous pleura suggesting thymoma.

 
In case 2, histopathological examination of the surgical specimen after maximal thymectomy detected ectopic thymic tissue in the mediastinal fat. PET did not show uptake in the area corresponding to the reported ectopic thymic tissue.

In the second group, FDG–PET detected more lesions than CT. In case 12, FDG–PET showed multiple foci of increased uptake in the main tumor, contiguous pleura, and pericardium. CT demonstrated a well-defined, rather noninvasive, anterior mediastinal mass. On excision, the tumor was invading the adjacent pleura and lung. It was histologically proved to be lympho-epithelial predominant type, stage III thymoma.

In patients with thymic hyperplasia, PET showed diffuse homogenous uptake of FDG, with SUV ranging from 0.7 to 2.5 with a mean value of 1.89 ± 0.58. In patients with thymoma, either non-invasive or invasive, PET showed more intense uptake in the tumor and metastatic foci. SUV in thymoma ranged from 3.1 to 6.1 with mean value of 4.75 ± 0.88.

CT findings in two patients with persistent myasthenic symptoms after excision of invasive thymoma were inconclusive for local recurrence and suggested postoperative changes. FDG–PET showed abnormal FDG uptake in the mediastinum indicating recurrence (Fig. 2 ). Operative findings and histopathology results were consistent with FDG–PET results.


Figure 2
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  		Fig. 2. A 28-year-old female with persistent myasthenic symptoms after thymectomy (case 21). (A) CT of the mediastinum could not predict recurrence. (B) FDG–PET shows uptake in the mediastinum consistent with recurrence of thymoma.

 
During follow-up, FDG–PET and CT were comparable in detecting metastasis after excision of thymic neoplasm. Metastases presented as right pleural nodule(s) (n = 3), middle lobe nodule (n = 1) (Fig. 3 ), pedunculated right diaphragmatic nodule (n = 1), right diaphragmatic copula and liver invasion (n = 1), and two metastatic nodules in the right lower lobe (n = 1). Histopathological examination of the resected specimens proved thymic carcinoma metastasis in two and invasive thymoma in four patients.


Figure 3
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  		Fig. 3. A 46-year old female with middle lobe metastatic lesion (case 23). (A) CT shows right diaphragmatic nodule. (B) FDG–PET focus of moderate to intense uptake in diaphragmatic metastasis.

 

   4. Discussion
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
5. Conclusion
 Appendix A
 References
 
Preoperative histological diagnosis of thymic pathology has an important implication on the management strategy and on predicting prognosis [8–9]. MG is frequently associated with different thymic abnormalities. Lymphoid follicular hyperplasia occurring in 60–77% and thymoma in 15–30% of patients [10]. In non-thymoma patients with MG, the benefit of maximal thymectomy was estimated to be 86%, while 14% did not improve at a mean follow-up period of 7.6 years. Age, thymic histology, and ectopic thymic tissue are significant prognostic factors for outcome [8]. In a retrospective study, 30 children with myasthenia gravis underwent maximal thymectomy. After long-term follow-up, maximal thymectomy appears to provide high rate of remission (43.4%) and improvement (46.6%) for this group of patients [11].

Different imaging techniques may help in detection and characterization of thymus related pathology. CT is considered superior in detecting lesions in the anterior mediastinum and may help to diagnose and differentiate between various thymic pathologies. However, the CT characteristics of the various subtypes of thymic epithelial tumor may overlap [7]. One report described the sensitivity and specificity of CT of the mediastinum in predicting the histological findings in patients with MG referred for thymectomy, to be 75% and 62%, respectively [12].

Fluorine-18 fluorodeoxyglucose positron emission tomography has emerged as a strong diagnostic tool for the diagnosis and staging of various neoplasms [13]. PET assesses the biological, metabolic, and functional aspects better than the morphologic features of the tumor, and hence, the malignant nature of tumors can be better identified. In this study, we utilized FDG–PET scan to differentiate thymic hyperplasia from thymoma and to diagnose residual disease and recurrence.

The patients with MG and thymic hyperplasia had homogenous FDG uptake. The mean value of SUVs for FDG uptake in patients with thymoma was significantly higher than that in patients with thymic hyperplasia (4.75 and 1.89, respectively).

Our results are consistent with those reported by Liu et al. [14], who showed that FDG–PET clearly distinguishes thymomas from thymic hyperplasia by utilizing tumor/lung ratio (TLR) approach. They also stated that differentiation of malignant and benign thymoma was better assessed by the pattern of abnormal FDG distribution than quantitative measurement of the FDG uptake. Sasaki et al. [15] found a mean SUV of 7.2 ± 2.9 for patients with thymic carcinoma. This value was significantly greater than the values for invasive thymoma (3.8 ± 1.3) and noninvasive thymoma (3.0 ± 1.0). By using SUV of 5.0 as a cutoff, the authors achieved reasonable sensitivity (84%), specificity (92.3%), and accuracy (88.5%). They found no statistically significant difference in SUV between invasive and noninvasive thymomas.

As described by Ashour [16], the prevalence of ectopic thymic tissue could reach up to 39.5% in myasthenic patients. Ectopic thymic tissue modifies some of the clinical parameters of myasthenia gravis and serves as a prognostic factor in predicting the outcome of operation.

In one case, FDG–PET failed to detect ectopic thymic tissue. False-negative imaging results or underestimation of the metabolic activity of lesions may occur in the case of small nodules less than 7 mm in diameter [17].

Ruffini et al. [18] reported 30 recurrences in a series of 266 resected thymomas (11.2%). The rate of recurrence was lowest in stage I thymoma (5%) and highest in stage IV (33%). Early detection and exact localization of tumor recurrence is important for planning of further therapeutic modalities (i.e. reoperation, chemotherapy, radiotherapy). CT scan may not differentiate residual and recurrent disease from fibrosis and scar tissue, especially when located in the anterior mediastinum at the previous surgery site, whereas PET is sensitive and specific in diagnosing residual disease and recurrence [19].

In our study, two patients had persistent myasthenic symptoms after resection of invasive thymoma. CT was inconclusive in differentiating recurrence from postoperative changes. Abnormal FDG uptake in the mediastinum predicted the recurrence. The recurring lesions were excised. The histopathological examination confirmed the recurrence. FDG–PET was superior to CT in detecting local recurrence of thymoma.


   5. Conclusion
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 5. Conclusion
Appendix A
 References
 
In myasthenia gravis, selective use of FDG–PET is useful in differentiating thymic hyperplasia from thymoma, especially when CT scan is controversial. Due to the limited number of patients in our study, the role of FDG–PET in myasthenia gravis patients and in detecting ectopic thymic tissue needs to be explored. FDG–PET is a very sensitive diagnostic tool in detecting residual, recurrence, and metastatic disease in patients who underwent thymoma excision.


   Appendix A
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 5. Conclusion
 Appendix A
References
 
Conference discussion

Dr M. Lanuti (Boston, Massachusetts, USA): How are the SUV cutoffs determined for hyperplasia versus thymoma?

Dr Al-Kattan: I think there were bigger studies done in that field, and we have established this with our nuclear physicians, that they can differentiate between aggressive malignancies and thymoma, which is intermediate malignancy, and hyperplasia uptake, and we have utilized a cutoff sign of 3 to be suggestive of nonmalignant features, which is hyperplasia, and a range between 3 and 6 for the intermediate tumors, which is thymoma. I believe these were actually fairly accurate in their presentation and we didn’t have an overlap that this is suggestive of hyperplasia versus thymoma, but I think also this was supported by previous studies done within that field to estimate a range of each pathology with the SUV values.

Dr Lanuti: And did this correlate or carry over to younger patients, whom we know often have elevated SUV in the thymic bed, perhaps suggestive of thymic hyperplasia. Does the SUV cutoff of 3 carry over into young patients?

Dr Al-Kattan: One of our patients was 14 years old and I think the hyperplasia was correlating with the SUV of 2.3. Probably during childhood, the thymus morphology and function is different from adults but falls within the range detected by SUV for PET scan.

Dr A. End (Vienna, Austria): Did you find any other incidental pathologies when performing the whole-body PET scan?

Dr Al-Kattan: Not incidental, but I think the importance of this is when we have a patient with myasthenia gravis and the CT is not suggestive of thymoma, the indication is usually treatment of myasthenia gravis rather than treatment of thymoma. I think in those patients, when you are in doubt and you do a PET scan that suggests thymoma, then the indication for surgery will completely differ.


   Footnotes
 
\#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.


   References
Top
 Abstract
 1. Introduction
 2. Materials and methods
 3. Results
 4. Discussion
 5. Conclusion
 Appendix A
 References
 

  1. Budde JM, Morris CD, Gal AA, Mansour KA, Miller Jr. JI. Predictors of outcome in thymectomy for myasthenia gravis. Ann Thorac Surg 2001;72(1):197-202.[Abstract/Free Full Text]
  2. Rosai J, Sobin LH. Histological typing of tumours of the thymus. In International histological classification of tumours. 2nd ed.. New York: Springer; 1999.
  3. Sonobe S, Myamoto H, Izumi H, Nobukawa B, Futagawa T, Yamazaki A, Oh T, Ukosa T, Abe H, Suda K. Clinical usefulness of the WHO histological classification of thymoma. Ann Thorac cardiovasc Surg 2005;11(6):367-373.[Medline]
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  6. Han J, Lee KS, Yi CA, Kim TS, Shim YM, Kim J, Kim Kkwon OJ. Thymic epithelial tumors classified according to a newly established WHO scheme: CT and MR findings. Korean J Radiol 2003;4(1):46-53.[Medline]
  7. Jeong YJ, Lee KS, Kim J, Shim YM, Han J, Kwon OJ. Does CT of thymic epithelial tumors enable us to differentiate histologic subtypes and predict prognosis. AJR Am J Roentgenol 2004;183(2):283-289.[Abstract/Free Full Text]
  8. El-Medany Y, Hajjar W, Essa M, Al-Kattan K, Hariri Z, Ashour M. Predictors of outcome for myasthenia gravis after thymectomy. Asian Cardiovasc Thorac Ann 2003;11(4):323-327.[Abstract/Free Full Text]
  9. Budde JM, Morris CD, Gal AA, Mansour KA, Miller JI. Predictors of outcome in thymectomy for myasthenia gravis. Ann Thorac Surg 2001;72:197-202.[Abstract/Free Full Text]
  10. Pirronti T, Rinaldi P, Evoli A, Schino C, Marano P. Thymic lesions and myathenia gravis, diagnosis based on mediastinal imaging and pathological findings. Acta Radiologica 2002;43:380-384.[CrossRef][Medline]
  11. Essa M, El-Medany Y, Hajjar W, Hariri Z, Al-Mulhim F, Salih M, Ashour M, Al-Kattan K. Maximal thymectomy in children with myasthenia gravis. Eur J Cardiothorac Surg 2003;24(2):187-189.[Abstract/Free Full Text]
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  15. Sasaki M, Kuwabara Y, Ichiya Y, Akashi Y, Yoshida T, Nakagawa M, Murayama S, Masuda K. Differential diagnosis of thymic tumors using a combination of 11C-methionine PET and FDG PET. J Nucl Med 1999;40:1595-1601.[Abstract/Free Full Text]
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