IgG4-related Ocular Adnexal Disease Mimicking Thyroid-associated Orbitopathy
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1 CASE REPORT IgG4-related Ocular Adnexal Disease Mimicking Thyroid-associated Orbitopathy Hidefumi Inaba 1, Takahiro Hayakawa 1, Waka Miyamoto 1,KenTakeshima 1, Hiroyuki Yamaoka 1, Yasushi Furukawa 1, Hiromichi Kawashima 1, Hiroyuki Ariyasu 1, Hisao Wakasaki 1, Hiroto Furuta 1, Masahiro Nishi 1, Taisei Nakao 1, Hideyuki Sasaki 1, Yuka Okada 2, Kazuto Matsunaga 3, Yasushi Nakamura 4 and Takashi Akamizu 1 Abstract A 72-year-old man presented with bilateral eyelid swelling and redness. An orbital CT scan showed bilateral proptosis, extraocular muscle enlargement and swollen lacrimal glands, mimicking thyroid-associated orbitopathy (TAO) with Hashimoto s thyroiditis (HT). During the patient s clinical course, spontaneous remission of lung consolidation (35 26 mm) was seen. A diagnosis of IgG4-related disease (IgG4-RD) was made based on an elevated serum IgG4 level (1,020 mg/dl; normal, 4-108), predominance of IgG4-positive plasma cells (IgG4/IgG: 35/70 in HPF) in the lacrimal glands and typical features of Mikulicz s disease. This report provides a novel description of this unusual disease entity among HT, TAO and IgG4-RD. Key words: IgG4, ocular adnexal disease, thyroid-associated orbitopathy, Hashimoto s thyroiditis () () Introduction Thyroid-associated orbitopathy (TAO) is an extrathyroidal manifestation of autoimmune thyroid diseases (1). Proptosis, swollen extraocular muscles, increased orbital fat and lacrimal gland enlargement are typically observed in TAO patients. The disease preferentially occurs in patients with Graves disease (GD). Although in the minority, TAO also occurs in patients with Hashimoto s thyroiditis (HT). IgG4- related disease (IgG4-RD) is a new entity characterized by lymphoplasmacytic infiltration and tissue fibrosis causing organ dysfunction (2, 3). It typically affects the lacrimal glands, orbits, salivary glands, lungs, pancreas, biliary ducts and retroperitoneal tissue. Recently, a novel subtype of HT with an increased level of IgG4-bearing plasmacytes in the thyroid was proposed (4), thus suggesting a common mechanism in HT and IgG4-RD. We herein discuss a case of IgG4-related ocular adnexal disease mimicking TAO with HT in autoimmune aspects, constituting a unique clinical entity. This report also suggests that 1) measuring the serum IgG4 level, 2) conducting histological examinations with IgG4 immunostaining and 3) performing laboratory tests and assessments of systemic manifestations is necessary in order to make an accurate diagnosis of IgG4-RD. Case Report A 72-year-old man presented with bilateral eyelid swelling and redness in addition to bronchial asthma begining nine years earlier. His areas of eyelid swelling had gradually enlarged, and he was referred to our hospital one year previously. He had been healthy until nine years before the referral. Both eyelids were swollen with redness (Fig. 1A). He had been treated with inhaled corticosteroids (fluticasone propionate at a dose of 200 μg/day) for bronchial asthma for nine years. He had no history of smoking or remarkable fa- The First Department of Medicine, Wakayama Medical University, Japan, Department of Ophthalmology, Wakayama Medical University, Japan, Department of Respiratory Medicine, Wakayama Medical University, Japan and Department of Clinical Laboratory Medicine, Wakayama Medical University, Japan Received for publication May 1, 2013; Accepted for publication July 7, 2013 Correspondence to Dr. Hidefumi Inaba, inaba@wakayama-med.ac.jp 2545
2 A B Figure 1. A: The patient on admission. Redness and swelling of the bilateral lacrimal glands were observed. B: The patient four weeks after admission. The redness and swelling had mildly improved. Table 1. Laboratory Data on Admission Figure 2. An ultrasonographic examination showed a diffusely swollen thyroid gland with a dishomogeneous course and slightly hypoechogenic pattern. milial history. His body height was 171 cm, and his body weight was 68 kg (body mass index; 23.3 kg/m 2 ). His blood pressure was 118/72 mmhg, his heart rate was 78 beats/min and regular and his body temperature was His thyroid gland was firm and diffusely enlarged (5.5 cm in diameter). No abnormal heart or lung sounds were detected. No special findings were observed on abdominal examinations. The superficial lymph nodes were not palpable. The findings of a neurological examination were completely normal, including the results of eye movement and visual field tests. No diplopia was observed. The degree of exophthalmos measured with the Hertel exophthalmometer was 16 mm in both eyes. The clinical activity score (CAS) for orbitopathy was 2: eyelid swelling and redness (5). A laboratory test revealed that the serum free thyroid hormones (FT3 and FT4) and TSH levels were within the normal ranges (Table 1). Antithyroid peroxidase antibodies (TPOAb) were positive (18.4 U/mL: normal value, <16.0). Anti-thyroglobulin antibodies (TgAb), anti-tsh receptor antibodies (TRAb-3rd) and thyroid-stimulating antibodies (TSAb) were all negative. TRAb-1st and TRAb-2nd were also negative. A complete blood count revealed an elevated eosinophil concentration of 10% (absolute count: 690/μL), hemoglobin level of 10.9 g/dl and normal platelet count. Serum electrolyte, renal function and liver function tests were normal. The level of serum C-reactive protein (CRP) was marginally elevated (0.65 mg/dl, normal; <0.30 mg/dl). The serum IgG level was elevated to 3,451 mg/dl (normal: 870-1,700). The serum IgG4 level was also elevated (1,020 mg/dl; 4-108), WBC 6900 / Eos 10.0 % Hb 10.9 Plt / TP 8.8 g/d Alb 3.9 AST 34 IU/ A T 27 IU/ BUN 15 mg/d Cr 0.83 mg/d H 185 IU/ T-bil 1.0 mg/d CK 123 IU/ Na 138 meq/ K 4.0 meq/ Cl 100 meq/ Ca 9.4 mg/ CRP 0.65 mg/ (<0.30) Underlines denote abnormal values. IgG 3451 mg/ ( ) IgG mg/ (4-108) IgA 175 mg/ ( ) IgM 118 mg/ (35-220) IgE 1345 IU/m (0-361) ANA <40 C3 113 mg/ (65-135) C4 25 mg/ (13-35) CH U/m (30-50) SS-A (-) SS-B (-) RF 8.0 IU/m (<20) P-ANCA <1.3 U/m (<2) C-ANCA 2.3 U/m (<3.5) K U/m (<500) SP-A 21.4 ng/m (<43.8) SP ng/m (<110) 987 U/m ( ) Table 2. Endocrinological and Immunological Tests on Admission TSH 3.94 /ml ( ) FT pg/ml ( ) FT ng/dl ( ) TRAb <1.0 L (<2.0) TSAb 93 % (<180) TgAb 16.1 L (<28.0) TPOAb 18.4 L (<16.0) - <0.1 ml (<0.1) -5 <3.9 pg/ml (<3.9) pg/ml (<6.0) pg/ml (<4.0) -13 <3.1 pg/ml (<3.1) TGF ng/ml ( ) derlines denote abnormal values. TSH: thyrotropin, FT3: Triiodothyronine, FT4: Thyroxine, TRAb: TSH receptor antibody (third generation), TSAb: thyroid stimulating antibody, TgAb: anti-thyroglobulin antibody, TPOAb: antithyroid peroxidase antibody, interferon L- : interleukin-, TGF: transforming growth factor. and an elevated serum IgE level was observed. The soluble IL-2 receptor (sil2r) level was mildly elevated. Antinuclear antibodies were negative. P-ANCA and C-ANCA were negative. The level of serum angiotensin converting enzyme (ACE) was within the normal range. The results of stool tests were negative for parasitic infections, and a urinalysis was normal. The results of bone marrow aspiration were negative for malignancy. Cultures of the blood and sputum 2546
3 A B C D E F G H I Figure 3. An orbital CT coronal image showed bilateral superior rectus and left lateral rectus muscle swelling (A: arrows). On an axial image, the left lateral rectus muscle was swollen (B: arrow). The bilateral lacrimal glands and subcutaneous tissue in the eyelids were swollen (C: arrows). Bilateral proptosis and increased orbital fat were observed on T1- and T2-weighted MRI (D and E, respectively). The swollen extraocular muscles exhibited isointensity on both T1- and T2-weighted MRI. On FDG-PET, tracer uptake was observed in the bilateral lacrimal glands and extraocular muscles (arrows, SUVmax=3.13) (F). Twelve weeks later, the bilateral superior and left lateral rectus muscles remained swollen on coronal (G: arrows) and axial CT images (H: arrow). The bilateral lacrimal gland and eyelid swelling had slightly improved (I: arrows). were also negative. In addition, the serum cytokine levels were measured (Table 2). The serum IL-4, IL-6 and plasma transforming growth factor (TGF)-β levels were elevated. On a cervical ultrasound evaluation, the thyroid gland was found to be enlarged with a heterogeneous, course and a slightly hypoechogenic pattern (Fig. 2). In addition to the positive level of antithyroid peroxidase antibodies, a diagnosis of HT was considered (6). Orbital CT showed markedly swollen bilateral superior rectus and left lateral rectus muscles (Fig. 3A, B). The bilateral lacrimal glands and eyelids were swollen, and bilateral proptosis and increased orbital fat were observed (Fig. 3C). On T1- and T2-weighted magnetic resonance imaging (MRI), isointense extraocular muscles were observed (Fig. 3D, E, respectively). [F-18]-2-fluoro-2-deoxy-D-glucose (FDG) accumulation was seen in the bilateral lacrimal glands, extraocular muscles and orbits on positron emission tomography (PET) (SUVmax=3.13) (Fig. 3F). On cervical CT, symmetrical parotid gland swelling was observed. On chest CT, mediastinal lymphadenopathy with thickening of the perilymphatic interstitial region and subpleural peribronchovascular consolidation (35 26 mm) was seen in S10 of the right lung (Fig. 4A), suggesting IgG4-related lung disease (7). On a bronchoalveolar lavage fluid examination, the level of 2547
4 A B C D Figure 4. On chest CT, mediastinal lymphadenopathy with subpleural peribronchovascular consolidation (35 26 mm) was observed in S10 of the right lung (A). On FDG-PET, tracer uptake was seen in the lymph nodes in addition to consolidation (B). Histological examinations of the right lung consolidation (C; Hematoxylin and Eosin staining, 200). The interalveolar septum was diffusely thickened. Lymphoid follicular and lymphoplasmacytic infiltration with fibrosis was observed. Eosinophils were noted. On chest CT obtained after eight weeks, the lung consolidation had disappeared (D). A B C Figure 5. Histological examinations of the lacrimal glands. Lymphoid follicular and lymphoplasmacytic infiltration with storiform fibrosis was observed. Eosinophils were noted. (A; Hematoxylin and Eosin staining, 200). On immunostaining with IgG, IgG-positive plasmacytes were stained preferentially around the lymphoid follicles (B; 200). On immunostaining with IgG4, IgG4-positive plasmacytes were abundantly observed, and the ratio of IgG4/IgG was 35/70/HPF (C; 200). eosinophils was not increased. The pancreas was not enlarged on abdominal CT. Lung consolidation and FDG uptake in the bilateral lacrimal glands, parotid glands and multiple lymph nodes were observed on PET (Fig. 4B). The accumulation in the thyroid was mild. To reach an accurate diagnosis, the patient underwent a histological examination. Both eyelid specimens exhibited diffuse lymphoplasmacytic infiltration containing IgG4- positive plasma cells (the ratio of IgG4/IgG was 35/70 in HPF), storiform fibrosis and infiltration of eosinophils (Fig. 5A-C). Immunostaining for bcl-2 and bcl-6 was negative. In addition, a transbronchial lung biopsy specimen demonstrated massive lymphoplasmacytic and eosinophilic infiltration with fibrosis (Fig. 4C). Since no eosinophilic abscess formation or proliferation of blood capillaries were observed among the lymphoid follicles, diagnoses of Kimura s disease (8) and angiolymphoid hyperplasia with eosinophilia (ALHE) were less likely. As the platelet count was not increased and the serum CRP and IL-6 levels were not remarkably elevated, Castleman s disease was also excluded (9). Considering the findings of chest CT and the laboratory tests, allergic bronchopulmonary aspergillosis and Churg-Strauss syndrome were also excluded. Based on the results of the bronchoalveolar lavage fluid, eosinophilic pneumonia was unlikely; however, the coexistence of systemic allergic diseases with hypereosinophilia could not be completely ruled out. A diagnosis of IgG4-RD was made due to the elevated serum IgG4 level, preferential infiltration of IgG4-positive plasma cells in the lacrimal glands and typical features of Mikulicz s disease, with the exception of lymphocyte proliferation similar to that observed in eosinophilic diseases, such as Wegener s granulomatosis and sarcoidosis. Within a couple of months during the period approaching the diagnosis, although the bilateral superior and left lateral rectus muscles remained swollen (Fig. 3G, H), the lung consolidation spontaneously improved (Fig. 4D), and partial shrinkage of the eyelid swelling and reduction of proptosis (Right: 13 mm, and Left: 14 mm) were observed (Fig. 1B, 3I), without any further treatment. In addition, the level of eosinophilia decreased (from 10% to 7.8%), and the serum levels of CRP, IgG, IgG4 and IL2R improved to 0.14 mg/dl, 2,628 mg/dl, 897 mg/dl and 835 U/mL, respectively (Table 3). After an additional one year, no further 2548
5 Table 3. Laboratory Data during the Course 8 weeks before admission on admission 12 weeks after admission TSH IU/mL FT3 pg/ml FT4 ng/dl TRAb IU/mL <1.0 <1.0 <1.0 TSAb % ND 93 ND TgAb IU/mL TPOAb U/mL IgG mg/dl IgG4 mg/dl ND IgE IU/mL Eos (/μl, %) 802, 9.0% 690, 10% 490, 7.8% sil2r U/mL CRP mg/dl Underlines denote abnormal values. ND: not determined amelioration of the eye symptoms or lung consolidation was evident. Discussion In addition to the typical histological findings in the lacrimal glands with prominent IgG4-bearing plasmacytic and lymphocytic infiltration and storiform fibrosis concomitant with an elevated serum IgG4 level, a diagnosis of IgG4-RD was made based on systemic manifestations, including those of the parotid glands, lymphoid tissue and pulmonary masses (2, 3). The spontaneous improvement of the eyelid swelling and lung consolidation was also suggestive of IgG4-RD. Moreover, the laboratory results, including the serum IL-6, CRP and platelet levels, supported the diagnosis. We speculate that the elevation of IgG4 is associated with increased plasmacytes in affected organs (lacrimal glands, extraocular muscles, parotid glands, lungs, lymphoid tissues and thyroid). The serum IgG4 and IL2R levels are considered to be disease markers. Recently, a novel subtype of HT defined as IgG4- thyroiditis was proposed, which is characterized by parenchymal fibrosis, lymphoplasmacytic infiltration and follicular cell degeneration (4). With other organ manifestations of IgG4-RD, our case may be considered a case of HT associated with IgG4-RD, sharing a common etiology as an autoimmune-like disease (2, 3). Komatsu et al. reported that 26.8% of patients with autoimmune pancreatitis (AIP) have a hypothyroid status, further suggesting thyroid involvement in IgG4-RD (10). In patients with TAO, 1) redness of the conjunctiva and eyelid retraction are often observed, as well as extraocular muscle enlargement and increased orbital tissue, and 2) the most frequently affected muscle is the inferior rectus muscle, with preferential swelling in the belly. In addition, histological examinations indicated dacryoadenitis, myositis and orbital inflammation due to IgG4-RD rather than TAO in our case. However, some clinical features and orbital CT and MRI findings were similar to those of TAO, including bilateral disease with a chronic onset, multiple areas of muscle enlargement, increased orbital fat, lacrimal gland enlargement, the absence of orbital masses and sinus involvement (1, 11, 12). A substantial proportion of cases of idiopathic orbital pseudotumors (11) or infraorbital nerve enlargement (13) in fact represent ocular adnexal manifestations of IgG4-RD; such symptoms were not seen in our patient. Therefore, definitively discriminating between TAO and IgG4-RD is difficult, possibly because the conditions are closely associated, sharing common autoimmune mechanisms. In fact, a case of TAO-like orbitopathy concomitant with AIP has been reported (14). Although the precise pathophysiology of TAO remains unclear, the disease reflects sensitized T lymphocytes and autoantibodies (1, 15). In our patient, the occurrence of TAO-like orbitopathy in association with IgG4-RD raises the question of which antigens are involved in the autoimmune process and whether some of these antigens are shared by the extraocular muscles, orbit, parotid glands, thyroid and potentially affected organs. The autoantigens involved in the pathogenesis of IgG4-RD remain to be fully identified. Notably, in patients with TAO, alpha fodrin may be one of the autoantigens involved in both the salivary glands and orbit (16) and thus may have been responsible for the symptoms observed in our patient. In addition, calsequestrin, collagen XIII, IGF-1 receptor and TSH receptor have been proposed to be antigens involved in the pathogenesis of TAO (17, 18). Further investigations are warranted to identify common autoantigens among autoimmune thyroid diseases, ocular adnexal diseases and IgG4-RD. Thyroid autoantibodies have been reported to not be correlated with the clinical activity or thickness of the extraocular muscles in patients with TAO (19). In patients with IgG4, Fab-arm exchange may be associated with bispecificity for two individual antigens. In our case, TPOAb and certain antibodies against the ocular adnexal organs are speculated to be involved in the immune disorder. Although the exact role of IgG4 in various diseases remains to be clarified (20), inhibition of immune complexes and complement activity by other IgGs may play immune-defensive roles. In fact, Guo et al. reported that the IgG1 present in TPOAb is related to cell damage, whereas its IgG4 subclass is not (21). The TPOAb in the sera of patients with HT are predominantly associated with IgG1 (22). In contrast, IgG2 is the dominant subtype of TgAb in patients with HT (23). Antigen presentation on the surface of HLA-DR molecules plays an important role in autoimmunity. HLA-DRB1*0405 is reported to be associated with IgG4-RD (24). Certain HLA-DR complexes, such as HLA- DR5, are susceptible to HT (25). Further investigation of HLA-DR molecules in relation to IgG4-RD, HT and TAO may clarify the role of the antigen presentation and T-cellmediated autoimmunity involved in these disorders. 2549
6 Zen et al. reported elevated levels of Th2 cytokines and regulatory cytokines in patients with IgG4-RD (26). In our patient, the serum levels of Th2 cytokines (IL-4 and IL-6) and TGF-β were elevated, consistent with a diagnosis of IgG4-RD. Although the usual treatment for IgG4-RD is oral steroid administration (2), the side effects of this agent are sometimes critical. Half of patients with asymptomatic segmental AIP do not require steroid therapy (27). Moreover, spontaneous remission is observed in certain patients with IgG4- RD (2) or IgG4-related pulmonary disease (7). Similarly, a wait-and-see policy is also recommended in patients with mild TAO (CAS 2) (15). Therefore, symptomatic therapy, such as the appropriate administration of eye drops, in the management of IgG4-related ocular adnexal disease may be appropriate, unless progressive deterioration of eye symptoms is observed. A case of ocular adnexal malignant lymphoma developing in a patient with IgG4-RD during the follow-up period has been reported (28). Therefore, conducting periodical physical examinations, laboratory tests and imaging tests is warranted. In summary, our case of IgG4-RD mimicking TAO suggests a common etiology as an autoimmune-like disease among AITD, TAO and IgG4-RD. With respect to making an accurate diagnosis and providing optimal treatment, the current case highlights the importance of 1) measuring the serum IgG4 level, 2) conducting histological examinations of the affected organs and 3) performing laboratory tests and assessments of systemic manifestations. The authors state that they have no Conflict of Interest(COI). Acknowledgement We are greatly thankful to Tomomi Funahashi, Takayuki Ota, Takeshi Shimada, Kaori Miyata, Tatsuya Ishibashi, Shohei Matsuno, Tomoyuki Takagi, Takayuki Nakagawa, Asako Doi and the members of The First Department of Medicine for providing valuable clinical and technical assistance. Hidefumi Inaba and Takahira Hayakawa contributed equally to this work. References 1. Bahn RS. Graves orbitopathy. N Engl J Med 362: , Stone JH, Zen Y, Deshpande V. IgG4-related disease. N Engl J Med 366: , Umehara H, Okazaki K, Masaki Y, et al. Comprehensive diagnostic criteria for IgG4-related disease (IgG4-RD), Mod Rheumatol 22: 21-30, Li Y, Nishihara E, Hirokawa M, Taniguchi E, Miyauchi A, Kakudo K. Distinct clinical, serological, and sonographic characteristics of Hashimoto s thyroiditis based with and without IgG4- positive plasma cells. J Clin Endocrinol Metab 95: , Bartalena L, Baldeschi L, Dickinson A, et al. Consensus statement of the European Group on Graves Orbitopathy (EUGOGO) on management of GO. Eur J Endocrinol 158: , DeGroot LJ, Quintans J. The causes of autoimmune thyroid disease. Endocr Rev 10: , Matsui S, Hebisawa A, Sakai F, et al. Immunoglobulin G4-related lung disease: clinicoradiological and pathological features. Respirology 18: , Abuel-Haija M, Hurford MT. Kimura disease. Arch Pathol Lab Med 131: , Takeuchi M, Sato Y, Takata K, et al. Cutaneous multicentric Castleman s disease mimicking IgG4-related disease. Pathol Res Pract 208: , Komatsu K, Hamano H, Ochi Y, et al. High prevalence of hypothyroidism in patients with autoimmune pancreatitis. Dig Dis Sci 50: , Wallace ZS, Khosroshahi A, Jakobiec FA, et al. IgG4-related systemic disease as a cause of idiopathic orbital inflammation, including orbital myositis, and trigeminal nerve involvement. Surv Ophthalmol 57: 26-33, Fujita A, Sakai O, Chapman MN, Sugimoto H. 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