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Primary thyroid mucosa-associated lymphoid tissue lymphoma; a clinicopathological study of seven cases

Purpose Primary thyroid mucosa-associated lymphoid tissue (MALT) lymphoma is a very rare subgroup of thyroid lymphoma, accounting for about 6 to 28% of all primary thyroid lymphomas. The purpose of this study was to evaluate its clinicopathological features and treatment outcomes. Methods We identified seven patients with thyroid MALT lymphoma who were treated between January 1997 and December 2007, and reviewed their clinicopathological features and follow-up outcomes. Results There were five female and two male patients, and their mean age was 73 years. All patients presented with palpable neck mass. Two patients had hoarseness and dyspnea. All patients had a history of Hashimoto's thyroiditis with a mean of 175 months. Malignant lymphoma was suspected in only three patients using core needle biopsy. Four patients underwent thyroidectomy in the absence of preoperative pathologic confirmation, and histologic diagnosis was obtained after surgery. As initial treatment, complete surgical resection was performed in five patients, radiotherapy in one, and a combination of chemotherapy and radiotherapy in one. Six patients were alive for the mean follow-up period of 66 months and one patient died of unrelated causes. There were neither recurrences nor disease-specific mortalities. Conclusion When primary thyroid MALT lymphoma occurs in the thyroid or is confined to the neck, it responds well to local treatment such as surgical resection and external beam radiation therapy.


INTRODUCTION
Primary thyroid lymphoma is a rare condition accounting for 1 to 5% of all thyroid malignancies and approximately 2% of all malignant extranodal lymphomas [1].
Mucosa-associated lymphoid tissue (MALT) lymphoma is one of the rare variants, first described by Isaacson and Wright in 1984 [2]. Pure thyroid MALT lymphomas comprise about 6 to 28% of primary thyroid lymphomas, and are recognized as extranodal marginal zone B-cell lymphomas in the Revised European American Lymphoma classification of 1994 and the World Health Organization classification of 1999 [3][4][5]. Strictly, the thyroid gland is not a mucosal organ, being of foregut origin, and the lym-

METHODS
We identified seven patients with a pathologic diag- lymphomas with dissemination to other extranodal sites [9]. Although this study was not primarily focused on staging, some authors insist that primary thyroid lymphoma is defined as a lymphoma that only involves the thythesurgery.or.kr roid gland or the thyroid gland with its adjacent lymph nodes [10], restricting its stage to either stage IE or IIE under the Ann Arbor staging system. The mean follow-up period was 66 months (range, 10 to 148 months).

RESULTS
The patients' characteristics are listed in Table 1 Fig. 1. As initial treatment, complete surgical resection was performed in five cases, radiotherapy alone in one case, and a combination of chemotherapy and radiotherapy was given in one case.
Among the patients that underwent surgery, there were two cases of total thyroidectomy, two cases of total thyroidectomy with modified radical neck dissection, and one case of hemithyroidectomy. The radiotherapy-only case was performed using a dose of 4,500 cGy to the neck area.
In the case of the patient that underwent combined chemo-therapy and radiotherapy, CHOP (cyclophosphamide, doxorubicin, vincristine, prednisolone) regimen was performed and the radiation dose was 4,500 cGy at the lesion.
Using the Ann Arbor staging system, five patients were stage IE and two patients were stage IIE. All of the patients achieved complete remission. One patient expired due to an unrelated cause (pancreatic cancer), and there were no disease-specific mortalities.
Two types of MALT can be identified in disparate organs that do not correspond to peripheral sites of the immune system. The native type consists of lymphoid tissue physiologically present in the gut (e.g., Peyer's patches), whereas acquired MALT develops in sites of inflammation in response to either infectious conditions such as Helicobacter pylori gastritis, or autoimmune processes such as Hashimoto's thyroiditis [19,20]. In addition to being a causal factor of primary thyroid MALT lymphoma, it has been hypothesized that Hashimoto's thyroiditis may further develop into aggressive lymphomas [6,21]. This is the basis for treatment of primary thyroid MALT lymphomas, even though they have a better response to local treatment and a more favorable prognosis compared to diffuse large cell lymphomas.
Normally, FNAB is a widely accepted technique for the diagnosis of thyroid nodules. However, primary thyroid lymphomas can be difficult to diagnose with FNAB alone.
While the diagnostic accuracy of FNAB is quite low for diffuse large B-cell lymphomas, it is even lower in the case of thyroid MALT lymphomas because the differentiation of MALT lymphomas from Hashimoto's thyroiditis can be difficult by cytomorphology alone [22]. Core needle biopsy, though not considered a first-line method for the diag-nosis of lymphomas, has been reported to have a higher diagnostic yield, with a sensitivity of 94.3%, a specificity of 100%, and an accuracy of 95.2% [23]. As a method for diagnostic confirmation, core needle biopsy would be an alternative with a high priority along with FNAB. In our study, surgery was performed on a total of four cases prior to pathological confirmation, with a single case of FNAB and three cases of core needle biopsy. Clinically, when a patient with a past history of Hashimoto's thyroiditis displays signs of abrupt thyroid enlargement or compression symptoms, the possibility of thyroid MALT lymphoma should be considered. This is especially true for the patients with a history over 5 years.
The optimal treatment modality for primary thyroid MALT lymphoma remains yet to be defined.  [7,25,26]. Considering the results of the current study and previous reports, the most important modality for the treatment of localized primary thyroid MALT lymphoma will be complete loco-regional control of disease including surgical removal and radiation therapy. Currently, there are no set protocols concerning follow-up evaluations after the treatment of primary thyroid MALT lymphoma. There are cases where fluorine-18 fluorodeoxyglucose-positron emission tomography scans were used in the evaluation of recurrences, but its utility is yet to be determined [27].
In conclusion, when primary thyroid MALT lymphoma is suspected, core needle biopsy along with FNAB should be considered as a first-line histologic diagnostic tool. As initial treatment, local treatment, such as complete surgical resection and radiotherapy, should be performed when the disease is localized in the thyroid or when the metastasis is limited to the regional lymph nodes. The role of adjuvant radiotherapy and chemotherapy is still undetermined and is in need of further research.

CONFLICTS OF INTEREST
No potential conflict of interest relevant to this article was reported.