A Case of Sarcoidosis That Improved upon Discontinuation of Etanercept
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1 Journal of Rheumatic Diseases Vol. 23,. 3, June, Case Report A Case of Sarcoidosis That Improved upon Discontinuation of Etanercept Ji-Hyoun Kang, Joon-Ho Ahn, Ji-Eun Yu, Ji-Eun Kim, Yi-Rang Yim, Jeong-Won Lee, Kyung-Eun Lee, Dong-Jin Park, Lihui Wen, Yong-Wook Park, Shin-Seok Lee Division of Rheumatology, Department of Internal Medicine, Chonnam National University Hospital, Chonnam National University Medical School, Gwangju, Korea A 31-year-old man who had been prescribed etanercept over a 3-year period for treatment of ankylosing spondylitis presented with newly developed dry cough, chills, myalgia, and weight loss. Chest computed tomography showed multiple reticulonodular pulmonary infiltrates and bilateral mediastinal, hilar, and peribronchial lymphadenopathy. Biopsy of a paratracheal lymph node revealed chronic granulomatous inflammation without necrosis, and the serum angiotensin-converting enzyme level was elevated. Sarcoidosis was diagnosed. His laboratory and radiological findings, and clinical symptoms improved only after discontinuation of etanercept without treatment. Although etanercept-induced sarcoidosis is rare, this case report suggests that sarcoidosis should be considered in the differential diagnosis of patients treated with the tumor necrosis factor inhibitor. (J Rheum Dis 2016;23: ) Key Words. Etanercept, Sarcoidosis, Ankylosing spondylitis INTRODUCTION Sarcoidosis is a multisystemic disease of unknown etiology presenting with various clinical manifestations [1]. The condition is characterized by the formation of noncaseating granulomas and is associated with increased production of cytokines including interleukin (IL)-12, IL-18, and tumor necrosis factor (TNF) [2]. TNF inhibitors appear to be effective when used to treat granulomatous diseases such as sarcoidosis. They serve as useful treatment options in refractory cases exhibiting inadequate responses or when unacceptable side effects develop upon prescription of glucocorticoids or diseasemodifying anti-rheumatic drugs [3]. However, some paradoxical cases of sarcoidosis developing secondary to prescription of TNF inhibitors have been reported in the West [4,5]. Our present case report suggests that an association may exist between etanercept therapy and sarcoidosis development in patients with ankylosing spondylitis (AS). CASE REPORT Our patient was a 31-year-old man who presented with a dry cough, chills, myalgia, and weight loss of approximately 5 kg over a period of 1 month. His medical history included AS 3 years in duration; AS had been diagnosed using the modified New York criteria [6]. The patient did not drink alcohol, was a nonsmoker, and had no relevant family medical history. He commenced treatment with ibuprofen, which was changed to naproxen (500 mg) and acetaminophen/tramadol (650 mg/75 mg) twice daily after 1 month. Despite continuous medication for more than 3 months, the lower back pain worsened. At 3 months, the patient had a Bath Ankylosing Spondylitis Disease Activity Index (BASDAI) score of 6.5 and a C-reactive protein (CRP) level of 0.26 mg/dl. Etanercept Received:July 2, 2015, Revised:(1st) August 7, 2015, (2nd) August 22, 2015, Accepted:August 24, 2015 Corresponding to:shin-seok Lee, Division of Rheumatology, Department of Internal Medicine, Chonnam National University Hospital, Chonnam National University Medical School, 42 Jebong-ro, Dong-gu, Gwangju 61469, Korea. shinseok@chonnam.ac.kr pissn: X, eissn: Copyright c 2016 by The Korean College of Rheumatology. All rights reserved. This is a Free Access article, which permits unrestricted non-commerical use, distribution, and reproduction in any medium, provided the original work is properly cited. 187
2 Ji-Hyoun Kang et al. therapy was commenced (50 mg subcutaneously once weekly from vember 2011). The nonsteroidal anti-inflammatory drugs were discontinued. After etanercept was commenced, the BASDAI score fell to 2.0. On physical examination, crackles in the right upper and lower lobes were evident during auscultation. The white blood cell count and total serum calcium level were within normal ranges, but the CRP level was elevated to 1.97 mg/dl. Sputum staining and culture for mycobacteria, and tuberculosis-specific real-time polymerase chain reaction of lymph node material and sputum, were negative. The level of angiotensin-converting enzyme was elevated to 73.8 U/L. X-ray and computed tomography (CT) of the chest revealed multiple reticulonodular pulmonary infiltrates and ground-glass opacification in both the upper and right lower lobes. Also, bilateral mediastinal, hilar, and peribronchial lymphadenopathy was evident (Figures 1B and 2A). Endobronchial, ultrasoundguided, transbronchial needle aspiration was performed to biopsy a paratracheal lymph node, and histological examination revealed chronic granulomatous inflammation without necrosis (Figure 3). These findings were consistent with a diagnosis of sarcoidosis that developed after etanercept treatment. As the clinical, laboratory, and radiological findings indicated that no other organ was invaded, etanercept was discontinued after a total duration of 2 years and 9 months. Six months later, chest CT revealed that the multireticulonodular lesion had decreased in size, as had the lymphadenopathy, and the cough, chill, and myalgia had improved (Figures 1C and 2B). The patient complained of back pain during follow-up in the outpatient clinic 1 month after discontinuation of etanercept. We commenced naproxen 500 mg twice daily; this afforded good pain control. DISCUSSION Etanercept (Enbrel; Immunex, Newbury Park, CA, Figure 1. Radiographic images. (A) Before etanercept treatment, (B) after treatment, (C) after discontinuation of etanercept. Figure 2. (A) Chest computed tomography scan exhibit multiple ground-glass opacities (white arrow) and mediastinal and hilar lymphadenopathy (black arrow). (B) Six months after discontinuation of etanercept, the radiological findings had improved. 188 J Rheum Dis Vol. 23,. 3, June, 2016
3 A Case of Sarcoidosis That Improved upon Discontinuation of Etanercept Figure 3. The right paratracheal lymph node exhibits chronic granulomatous inflammation without necrosis, suggestive of sarcoidosis (H&E; A: 100, B: 200). USA), a soluble TNF receptor protein fused to immunoglobulin G1, has been used worldwide for many years to treat rheumatological diseases, including AS. Various side-effects of TNF inhibitors have been reported; these include infections and malignancy. Granulomatous disease, such as sarcoidosis, is a rare side effect. In Korea, two cases of sarcoidosis were earlier reported: adalimumab-induced disease in a patient with rheumatoid arthritis [7] and etanercept-induced sarcoidosis in a patient with AS [8]. A literature search identified 45 cases of sarcoidosis (including Korean cases) [5,7-10] that developed during anti-tnf therapy. The mean patient age was years, and the male-to-female ratio was 2:3. The mean time from commencement of etanercept to sarcoidosis onset was 21.4 months. Anti-TNF therapy was ceased in 43 cases (95.6%). Of all cases, 31 were induced by etanercept, and 7 by adalimumab or infliximab. Of all cases, 75.5% (34) affected the lungs and most of these cases (20) were treated by withdrawing both the TNF inhibitors and other drugs such as steroids or anti-tuberculous medications. Prognoses were favorable in 35 cases, all of whom achieved complete resolution. However, 10 cases exhibited no improvement or relapsed. Twelve patients were re-commenced on TNF inhibitors and, of these, four relapsed (Table 1). In our case, complete resolution was evident only after discontinuation of etanercept. To the best of our knowledge, this is the first case exhibiting improvement of sarcoidosis after discontinuation of etanercept only (thus not any other drug) in Korea. Sarcoidosis is characterized by the appearance of proinflammatory activated CD 4 T lymphocytes secreting cytokines such as IL-2, IL-12, IL-18, interferon (IFN)-γ, and TNF-α. These cytokines are likely to play important roles in granuloma formation and development [2]. TNF inhibitors may modulate granulomatous inflammation and, indeed, have been recently used to treat several refractory cases of sarcoidosis. However, several cases of sarcoidosis paradoxically developing after prescription of TNF inhibitors have been described. The cause is unclear; several hypotheses have been advanced. TNF inhibitors exhibit different pharmacokinetics and mechanisms of action, creating variations in drug efficacy and the frequencies of adverse events. Anti-TNF-α monoclonal antibodies such as infliximab and adalimumab bind to both soluble and transmembranous forms of TNF-α with high avidity, and may cause cytotoxic complementinduced lysis of cells expressing TNF-α. However, etanercept binds principally to soluble TNF and does not induce cell lysis [9]. Etanercept exhibits both high-on and high-off binding kinetics, which may trigger TNF-α redistribution. TNF-α can move from sites of production to areas of low concentration without complete blockade of bioactivity [11]. These observations may explain differences in the clearance rates of etanercept and infliximab, the concentrations and steady-state levels of which are higher than those of other TNF-α inhibitors. Also, the former drugs are associated with higher fre189
4 Ji-Hyoun Kang et al. Table 1. Literature review: Development of sarcoidosis during anti-tnf therapy First author (year/journal) Miyagi (2014/Int J Rheum Dis) Skoie (2012/Rheumatol Int) Lee (2011/Tuberc Respir Dis) Park (2011/J Rheum Dis) Cuchacovich (2011/Clin Rheumatol) Kerjouan (2011/Rev Mal Respir) Massara (2010/Rheumatology) Daïen (2009/Rheumatology) Toussirot (2009/J Rheumatol) Josse (2009/Joint Bone Spine) Ishiguro (2008/Intern Med) Ognenovski (2008/J Rheumatol) Louie (2008/Ann Rheum Dis) Farah (2007/Pharmacotherapy) Kudrin (2007/J Rheumatol) Age (yr)/ sex/disease Drug/ duration (mo) Affected organ Treatment Outcome Readministration of anti-tnf agent 65/F/RA ETN/9, steroids 42/M/AS ETN/12 Salivary gl, eye, steroids, AZA 29/F/JIA ETN/24 Salivary gl, eye Relapse ETN 48/F/RA ETN/36, steroids 48/F/RA /5, steroids 42/F/AS ETN/60, steroids 52/F/PsA ETN/? Liver 54/M/AS ETN/24, steroids 45/M/PsA 30/F/RA 46/F/PsA 72/F/RA 69/F/RA 38/F/AS 49/F/RA 54/F/AS 50/M/AS 27/M/AS 53/F/RA 51/F/SAPHO 57/M/RA 70/F/RA 56/M/RA 45/F/RA 52/M/RA 54/M/RA 42/M/RA 54/M/RA IFX/25 /27 ETN/2 ETN/18 ETN/27 ETN/18 ETN/26 IFX/14 IFX/51 IFX/17 /21 /1 /12 ETN/9 ETN/13 /12 ETN/36 ETN/31 /17 ETN/6, eye, steroids, steroids, anti-tb Tx, steroids, steroids, anti-tb Tx Relapse Relapse Relapse ETN Rituximab Rituximab 55/F/RA IFX/33, lung Rituximab 65/F/RA ETN/21 60/M/RA 60/F/RA 66/F/RA 50/F/RA 35/F/AS ETN/9 ETN/48 ETN/47 ETN/60 ETN/1, eye, steroids, steroids, steroids, steroids 40/M/PsA ETN/10, steroids 52/F/RA ETN/1.5, steroids 190 J Rheum Dis Vol. 23,. 3, June, 2016
5 A Case of Sarcoidosis That Improved upon Discontinuation of Etanercept Table 1. Continued First author (year/journal) Almodóvar (2007/Clin Exp Rheumatol) Verschueren (2007/Clin Rheumatol) O Shea (2006/Arthritis Rheum) González-López (2006/Arthritis Rheum) Phillips (2005/Arthritis Rheum) Hübscher (2003/Arthritis Rheum) Hashkes (2003/Clin Exp Rheumatol) Age (yr)/ sex/disease Drug/ duration (mo) Affected organ Treatment Outcome Readministration of anti-tnf agent 34/M/AS IFX/24 46/F/RA ETN/12, skin 53/F/RA ETN/6, steroids 34/M/PsA IFX/57, steroids 70/M/AS ETN/21, lung 37/M/PsA ETN/18, antibiotics 41/F/RA ETN/19, antibiotics 7/M/JIA ETN/1, skin, eye, steroids Partial resolution : adalimumab, AS: ankylosing spondylitis, AZA: azathioprine, ETN: etanercept, F: female, gl: gland, IFX: infliximab, JIA: juvenile idiopathic arthritis, M: male, PsA: psoriatic arthritis, RA: rheumatoid arthritis, SAPHO: synovitis, acne, pustulosis, hyperostosis, and osteitis, TB: tuberculosis, TNF: tumor necrosis factor, Tx: treatment. quencies of sarcoidosis, possibly attributable to more effective prolonged suppression of TNF-α action [12]. Another possible explanation is that etanercept significantly increases the proportions of CD 4 and CD 8 lymphocytes that produce IFN-γ, which plays a pivotal role in granuloma formation and is present in high concentrations in patients with sarcoidosis [11]. An earlier randomized controlled trial showed that infliximab improved the predicted functional vital capacity in patients with severe symptomatic sarcoidosis [13]. In contrast, etanercept was considered to be less effective or to even worsen the sarcoidosis [14]. These observations may explain the higher risk of granulomatous reactions when etanercept rather than anti-tnf monoclonal antibodies is prescribed. It is possible that the risk of sarcoidosis development is greater when etanercept rather than other TNF inhibitors is given. It is difficult to accurately determine the number of cases of sarcoidosis triggered by use of TNF inhibitors. Further study on the pathogenesis of TNF inhibitor-induced sarcoidosis is required to clarify the clinical outcomes and treatment responses by individual conditions. SUMMARY We report a case of sarcoidosis in a patient with AS during etanercept therapy and complete remission were observed after withdrawal of the drug. The frequency of such paradoxical side-effects has increased as TNF inhibitors become more commonly prescribed, suggesting that a class effect may be in play. It is thus important that physiccians consider sarcoidosis among other more common adverse effects when a patient undergoing anti- TNF therapy and also the incidence of sarcoidosis differs by the type of anti-tnf agent prescribed. CONFLICT OF INTEREST potential conflict of interest relevant to this article was reported. REFERENCES 1. Hunninghake GW, Costabel U, Ando M, Baughman R, Cordier JF, du Bois R, et al. ATS/ERS/WASOG statement on sarcoidosis. American Thoracic Society/European Respiratory Society/World Association of sarcoidosis and other granulomatous disorders. Sarcoidosis Vasc Diffuse Dis 1999;16: Antoniu SA. Targeting the TNF-alpha pathway in sarcoidosis. Expert Opin Ther Targets 2010;14: Crommelin HA, Vorselaars AD, van Moorsel CH, Korenromp IH, Deneer VH, Grutters JC. Anti-TNF therapeutics for the treatment of sarcoidosis. Immunotherapy 2014;6: Vigne C, Tebib JG, Pacheco Y, Coury F. Sarcoidosis: an underestimated and potentially severe side effect of anti-tnf-alpha therapy. Joint Bone Spine 2013;80: Miyagi R, Ideguchi H, Soga T, Yamakawa Y, Otsuki H, Niino 191
6 Ji-Hyoun Kang et al. H, et al. Development of pulmonary and cardiac sarcoidosis during etanercept therapy. Int J Rheum Dis 2014;17: van der Linden S, Valkenburg HA, Cats A. Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria. Arthritis Rheum 1984;27: Lee SH, Kim SI, Song JS, Kim TH, Sohn JW, Kim SH, et al. Sarcoidosis induced by adalimumab in rheumatoid arthritis. Tuberc Respir Dis 2011;71: Park SY, Kim EK, Hwang DW, Lee KW, Paik SS, Jung KH, et al. A case of development of sarcoidosis during tumor necrosis factor-alpha antagonist therapy. J Rheum Dis 2011;18: Massara A, Cavazzini L, La Corte R, Trotta F. Sarcoidosis appearing during anti-tumor necrosis factor alpha therapy: a new "class effect" paradoxical phenomenon. Two case reports and literature review. Semin Arthritis Rheum 2010; 39: Daïen CI, Monnier A, Claudepierre P, Constantin A, Eschard JP, Houvenagel E, et al. Sarcoid-like granulomatosis in patients treated with tumor necrosis factor blockers: 10 cases. Rheumatology (Oxford) 2009;48: Wallis RS, Ehlers S. Tumor necrosis factor and granuloma biology: explaining the differential infection risk of etanercept and infliximab. Semin Arthritis Rheum 2005;34(5 Suppl 1): Furst DE, Wallis R, Broder M, Beenhouwer DO. Tumor necrosis factor antagonists: different kinetics and/or mechanisms of action may explain differences in the risk for developing granulomatous infection. Semin Arthritis Rheum 2006;36: Baughman RP, Drent M, Kavuru M, Judson MA, Costabel U, du Bois R, et al. Infliximab therapy in patients with chronic sarcoidosis and pulmonary involvement. Am J Respir Crit Care Med 2006;174: Utz JP, Limper AH, Kalra S, Specks U, Scott JP, Vuk-Pavlovic Z, et al. Etanercept for the treatment of stage II and III progressive pulmonary sarcoidosis. Chest 2003;124: J Rheum Dis Vol. 23,. 3, June, 2016
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