The Open Rheumatology Journal




ISSN: 1874-3129 ― Volume 13, 2019

LETTER TO THE EDITOR Atypical Granulomatous Myositis and Pulmonary Sarcoidosis



Renata Siciliani Scalco*, 1, 2, Stefen Brady 2, Jefferson Becker 1, Irenio Gomes 1, Janice L Holton 2, Henrique L Staub 3
1 Department of Neurology, Pontifical Catholic University of Rio Grande do Sul (PUCRS), Porto Alegre, Brazil
2 MRC Centre for Neuromuscular Diseases and Division of Neuropathology, Institute of Neurology, University College London, London, UK
3 Department of Rheumatology, PUCRS, Porto Alegre, Brazil


Article Information


Identifiers and Pagination:

Year: 2015
Volume: 9
First Page: 57
Last Page: 59
Publisher Id: TORJ-9-57
DOI: 10.2174/1874312901409010057

Article History:

Received Date: 26/1/2015
Revision Received Date: 27/5/2015
Acceptance Date: 9/6/2015
Electronic publication date: 10/7/2015
Collection year: 2015

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© Scalco et al.; Licensee Bentham Open.

open-access license: This is an open access article licensed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted, non-commercial use, distribution and reproduction in any medium, provided the work is properly cited.


* Address correspondence to this author at the Institute of Neurology, First Floor, London, WC1N 3BG, UK; Tel: 02034484391; E-mail: renata_scalco@hotmail.com




SIR,

Up to 80% of patients with sarcoidosis show muscular involvement, but symptomatic myopathy (sarcoid myopathy, SM) is rare [1Balageas A, Sanguinet F, Lequen L, Delbrel X. [Muscular sarcoidosis: a case report of muscle and fascia involvement and literature] Rev Med Interne 2013; 34(11): 706-12.
[http://dx.doi.org/10.1016/j.revmed.2013.02.008] [PMID: 24367812]
, 2Takami K, Suzuki M, Horiuchi T. [Muscular sarcoidosis] Nippon Rinsho 1994; 52(6): 1599-602.
[PMID: 8046848]
]. We herein report an interesting case of a patient with long history of muscle weakness diagnosed with SM who presented pulmonary sarcoidosis at a later stage.

A 45-year-old Brazilian white female was admitted with a four-year history of progressive proximal muscle weakness and myalgia. A chest radiogram was normal at the beginning of the clinical presentation. A few weeks before hospital admission, she developed diffuse weakness, dysphagia and exertion dyspnea. A physical examination showed weakness of facial and proximal muscles and severe wasting of hand muscles. Her family history was negative for neuromuscular diseases. The erythrocyte sedimentation rate was 92 mm in the first hour, and the serum creatine kinase level was high (6,683 IU/L, with a normal range being up to 176 IU/L). Antinuclear antibodies (1/640, granular pattern) and circulating anti-Ro/SSA antibodies (56.7 IU) were present. No other autoantibodies were found. A dried blood spot test for Pompe disease was negative. Neurophysiology assessment showed myopathic changes. A muscle biopsy performed 4 years after disease onset showed increased variation in fibre size, increased connective tissue, internal nuclei, occasional atrophic fibres and necrotic fibres. There was a prominent endomysial and perimysial inflammatory infiltrate composed of lymphoctes and macrophages with the formation of non-necrotic granulomas including small numbers of multinucleate giant cells (Fig. 1). A second piece of tissue taken from the same muscle showed no inflammatory features. Investigations for tuberculosis, fungi and brucellosis were negative. Lung computed tomography performed after 4 years of disease onset showed typical bilateral hilar lymphadenopathy and interstitial pneumonitis (“ground-glass” aspect in lower lobes) compatible with sarcoidosis. A restrictive pattern was seen on spirometry. Following the diagnosis, she received high doses of steroids. She has received IV immunoglobulin, and immunosuppressant (IV cyclophosphamide pulse therapy) since the beginning of the clinical presentation with no clinical response. Unfortunately, the patient died from bronchopneumonia approximately 5 years after initial presentation.

Fig. (1)

Muscle biopsy showing inflammatory infiltration of the perimysium and endomysium including non-necrotic granulomas (A). Multinucleate giants cells are seen within the granuloma (B). The bar represents 50 μm in A; and 20 μm in B.



The described patient presented muscle weakness as the main manifestation of systemic sarcoidosis. An early muscle biopsy is highly recommended to diagnose SM. Three different forms of SM are described: acute myositis, palpable muscle nodules and chronic myopathy. Our patient presented the latter, which is the most common [1Balageas A, Sanguinet F, Lequen L, Delbrel X. [Muscular sarcoidosis: a case report of muscle and fascia involvement and literature] Rev Med Interne 2013; 34(11): 706-12.
[http://dx.doi.org/10.1016/j.revmed.2013.02.008] [PMID: 24367812]
, 2Takami K, Suzuki M, Horiuchi T. [Muscular sarcoidosis] Nippon Rinsho 1994; 52(6): 1599-602.
[PMID: 8046848]
]. The cause of her muscle symptoms was probably SM/granulomatous myositis (GM), which later progressed to pulmonary sarcoidosis refractory to immunosuppressive therapy. ANA and anti-Ro/SSA were detected by the time the systemic disease was evident, but the patient did not show mucosal features typical of Sjögren syndrome. Anti-Ro/SSA antibodies have indeed been rarely reported in patients with sarcoidosis in the absence of Sjögren syndrome [3Amital H, Klemperer I, Blank M, et al. Analysis of autoantibodies among patients with primary and secondary uveitis: high incidence in patients with sarcoidosis Int Arch Allergy Immunol 1992; 99(1): 34-6.
[http://dx.doi.org/10.1159/000236332] [PMID: 1483065]
]. As opposed to descriptions in pulmonary sarcoidosis, whereby a Th1 cytokine response is characteristic, a dominant Th2 pattern is reported in patients with SM [4Prokop S, Heppner FL, Goebel HH, Stenzel W. M2 polarized macrophages and giant cells contribute to myofibrosis in neuromuscular sarcoidosis Am J Pathol 2011; 178(3): 1279-86.
[http://dx.doi.org/10.1016/j.ajpath.2010.11.065] [PMID: 21356378]
].

GM is a rare disorder, which can be idiopathic, but more frequently is related to sarcoidosis [5Prieto-González S, Grau JM. Diagnosis and classification of granulomatous myositis Autoimmun Rev 2014; 13(4-5): 372-4.
[http://dx.doi.org/10.1016/j.autrev.2014.01.017] [PMID: 24424169]
]. The clinical features of GM are non-specific including myalgia and weakness presenting a diagnostic challenge. Distal muscle involvement in GM may simulate inclusion body myositis [6Larue S, Maisonobe T, Benveniste O, et al. Distal muscle involvement in granulomatous myositis can mimic inclusion body myositis J Neurol Neurosurg Psychiatry 2011; 82(6): 674-7.
[http://dx.doi.org/10.1136/jnnp.2009.190751] [PMID: 20562458]
]. GM can also mimic slowly progressive lower motor neuron disease [7Gdynia HJ, Osterfeld N, Dorst J, Ludolph AC, von Arnim CA, Sperfeld AD. Granulomatous myositis mimicking slowly progressive lower motor neuron disease Eur J Med Res 2008; 13(7): 330-1.
[PMID: 18700190]
] and polymyalgia rheumatic [8Collins S, McKelvie P, Dennett X, Byrne E. Idiopathic granulomatous myositis: does the clinical spectrum include polymyalgia rheumatica? J Clin Neurosci 1999; 6(3): 255-9.
[http://dx.doi.org/10.1016/S0967-5868(99)90517-9] [PMID: 18639165]
], or be associated with myasthenia gravis [9Pascuzzi RM, Roos KL, Phillips LH II. Granulomatous inflammatory myopathy associated with myasthenia gravis. A case report and review of the literature Arch Neurol 1986; 43(6): 621-3.
[http://dx.doi.org/10.1001/archneur.1986.00520060079025] [PMID: 3718292]
] and mixed connective tissue disease [10Tanaka M, Senoh Y, Okamato K, Morimatsu M, Hirai S. [A case of granulomatous polymyositis associated with mixed connective tissue disease] Rinsho Shinkeigaku 1985; 25(9): 1039-45.
[PMID: 4092400]
]. GM has also been reported in patients with graft-versus-host disease [11Bagdasaryan R, Donahue JE. Granulomatous myositis in association with chronic graft vs. host disease Med Health R I 2007; 90(9): 287.
[PMID: 17970330]
], Crohn disease [12Ménard DB, Haddad H, Blain JG, Beaudry R, Devroede G, Massé S. Granulomatous myositis and myopathy associated with crohn’s colitis N Engl J Med 1976; 295(15): 818-9.
[http://dx.doi.org/10.1056/NEJM197610072951506] [PMID: 958278]
], primary biliary cirrhosis, pancytopenia, and thymoma [13Herrmann DN, Blaivas M, Wald JJ, Feldman EL. Granulomatous myositis, primary biliary cirrhosis, pancytopenia, and thymoma Muscle Nerve 2000; 23(7): 1133-6.
[http://dx.doi.org/10.1002/1097-4598(200007)23:7<1133::AID-MUS20>3.0.CO;2-E] [PMID: 10883012]
]. Of note, GM was the first manifestation of an aggressive CD30+ extra-nodal NK/T-cell lymphoma [14Min HS, Hyun CL, Paik JH, et al. An autopsy case of aggressive CD30+ extra-nodal NK/T-cell lymphoma initially manifested with granulomatous myositis Leuk Lymphoma 2006; 47(2): 347-52.
[http://dx.doi.org/10.1080/10428190500288545] [PMID: 16321870]
]. Infection diseases should be excluded including brucellosis [15Kojan S, Alothman A, Althani Z, et al. Granulomatous myositis associated with brucellosis: a case report and literature review Muscle Nerve 2012; 45(2): 290-3.
[http://dx.doi.org/10.1002/mus.22261] [PMID: 22246889]
], Pneumocystis carinii [16Pearl GS, Sieger B. Granulomatous Pneumocystis carinii myositis presenting as an intramuscular mass Clin Infect Dis 1996; 22(3): 577-8.
[http://dx.doi.org/10.1093/clinids/22.3.577] [PMID: 8852986]
], and tuberculosis [17Wang WY, Lin FC, Tsao TY, Lu JJ. Tuberculous myositis: an unusual presentation of extrapulmonary tuberculosis J Microbiol Immunol Infect 2007; 40(1): 79-82.
[PMID: 17332912]
].

Four out of 10 GM patients with myopathy reported in 1998 had systemic sarcoidosis [18Mozaffar T, Lopate G, Pestronk A. Clinical correlates of granulomas in muscle J Neurol 1998; 245(8): 519-24.
[http://dx.doi.org/10.1007/s004150050236] [PMID: 9747915]
]. Such patients had severe proximal weakness and were steroid-responsive as opposed to patients with idiopathic GM who had mostly distal involvement and were refractory to steroids [18Mozaffar T, Lopate G, Pestronk A. Clinical correlates of granulomas in muscle J Neurol 1998; 245(8): 519-24.
[http://dx.doi.org/10.1007/s004150050236] [PMID: 9747915]
]. A second GM series of symptomatic cases was published in 2007 [19Le Roux K, Streichenberger N, Vial C, et al. Granulomatous myositis: a clinical study of thirteen cases Muscle Nerve 2007; 35(2): 171-7.
[http://dx.doi.org/10.1002/mus.20683] [PMID: 17068767]
]. The authors described 8 SM cases [19Le Roux K, Streichenberger N, Vial C, et al. Granulomatous myositis: a clinical study of thirteen cases Muscle Nerve 2007; 35(2): 171-7.
[http://dx.doi.org/10.1002/mus.20683] [PMID: 17068767]
]. Distal involvement was also rare among the SM cases [19Le Roux K, Streichenberger N, Vial C, et al. Granulomatous myositis: a clinical study of thirteen cases Muscle Nerve 2007; 35(2): 171-7.
[http://dx.doi.org/10.1002/mus.20683] [PMID: 17068767]
]. Our patient showed an atypical form of SM, considering the presence of generalized muscle weakness with facial and distal muscle involvement, pulmonary sarcoidosis and anti-Ro/SSA antibodies.

A number of pathological findings have been reported in GM and SM including granulomatous endomysial and perimysial inflammation without necrosis. Typical inflammatory cells present are macrophages and T4 lymphocytes surrounded by T8 lymphocytes in mature lesions [18Mozaffar T, Lopate G, Pestronk A. Clinical correlates of granulomas in muscle J Neurol 1998; 245(8): 519-24.
[http://dx.doi.org/10.1007/s004150050236] [PMID: 9747915]
, 20Tews DS, Pongratz DE. Immunohistological analysis of sarcoid myopathy J Neurol Neurosurg Psychiatry 1995; 59(3): 322-5.
[http://dx.doi.org/10.1136/jnnp.59.3.322] [PMID: 7673968]
]. Necrotic and regenerating fibres may be seen. The pathological findings can be patchy and therefore may not be observed in the biopsy [18Mozaffar T, Lopate G, Pestronk A. Clinical correlates of granulomas in muscle J Neurol 1998; 245(8): 519-24.
[http://dx.doi.org/10.1007/s004150050236] [PMID: 9747915]
]. Sarcolemmal MHC class I up-regulation has been variably reported [4Prokop S, Heppner FL, Goebel HH, Stenzel W. M2 polarized macrophages and giant cells contribute to myofibrosis in neuromuscular sarcoidosis Am J Pathol 2011; 178(3): 1279-86.
[http://dx.doi.org/10.1016/j.ajpath.2010.11.065] [PMID: 21356378]
, 20Tews DS, Pongratz DE. Immunohistological analysis of sarcoid myopathy J Neurol Neurosurg Psychiatry 1995; 59(3): 322-5.
[http://dx.doi.org/10.1136/jnnp.59.3.322] [PMID: 7673968]
]. Chronic disease may progress to muscle fibrosis [4Prokop S, Heppner FL, Goebel HH, Stenzel W. M2 polarized macrophages and giant cells contribute to myofibrosis in neuromuscular sarcoidosis Am J Pathol 2011; 178(3): 1279-86.
[http://dx.doi.org/10.1016/j.ajpath.2010.11.065] [PMID: 21356378]
]. Muscle magnetic resonance imaging and ultrasound may help in the selection of biopsy site, differentiation of SM types and monitoring of therapy [21Karadeli E, Ulu EM. Acute sarcoid myositis with unusual radiologic findings Diagn Interv Radiol (Ank) 2010; 16(3): 232-5.
[PMID: 19838983]
]. Whole body fluorodeoxyglucose positron emission tomography can also be useful to direct biopsies in suspected sarcoidosis by revealing areas of increased metabolism [22Dufour JF, Billotey C, Streichenberger N, Bouhour F, Broussolle C, Sève P. [Sarcoidosis demonstrated by fluorodeoxyglucose positron emission tomography in a case of granulomatous myopathy] Rev Med Interne 2007; 28(8): 568-70.
[http://dx.doi.org/10.1016/j.revmed.2007.03.003] [PMID: 17445952]
].

In conclusion, the reported case suggests that SM/GM may precede systemic sarcoidosis. Presentation may be atypical as in our patient, who showed facial and distal muscle involvement and anti-Ro/SSA antibodies.

CONFLICT OF INTEREST

The authors confirm that this article content has no conflict of interest.

ACKNOWLEDGEMENTS

Declared none.

References

[1] Balageas A, Sanguinet F, Lequen L, Delbrel X. [Muscular sarcoidosis: a case report of muscle and fascia involvement and literature] Rev Med Interne 2013; 34(11): 706-12.
[http://dx.doi.org/10.1016/j.revmed.2013.02.008] [PMID: 24367812]
[2] Takami K, Suzuki M, Horiuchi T. [Muscular sarcoidosis] Nippon Rinsho 1994; 52(6): 1599-602.
[PMID: 8046848]
[3] Amital H, Klemperer I, Blank M, et al. Analysis of autoantibodies among patients with primary and secondary uveitis: high incidence in patients with sarcoidosis Int Arch Allergy Immunol 1992; 99(1): 34-6.
[http://dx.doi.org/10.1159/000236332] [PMID: 1483065]
[4] Prokop S, Heppner FL, Goebel HH, Stenzel W. M2 polarized macrophages and giant cells contribute to myofibrosis in neuromuscular sarcoidosis Am J Pathol 2011; 178(3): 1279-86.
[http://dx.doi.org/10.1016/j.ajpath.2010.11.065] [PMID: 21356378]
[5] Prieto-González S, Grau JM. Diagnosis and classification of granulomatous myositis Autoimmun Rev 2014; 13(4-5): 372-4.
[http://dx.doi.org/10.1016/j.autrev.2014.01.017] [PMID: 24424169]
[6] Larue S, Maisonobe T, Benveniste O, et al. Distal muscle involvement in granulomatous myositis can mimic inclusion body myositis J Neurol Neurosurg Psychiatry 2011; 82(6): 674-7.
[http://dx.doi.org/10.1136/jnnp.2009.190751] [PMID: 20562458]
[7] Gdynia HJ, Osterfeld N, Dorst J, Ludolph AC, von Arnim CA, Sperfeld AD. Granulomatous myositis mimicking slowly progressive lower motor neuron disease Eur J Med Res 2008; 13(7): 330-1.
[PMID: 18700190]
[8] Collins S, McKelvie P, Dennett X, Byrne E. Idiopathic granulomatous myositis: does the clinical spectrum include polymyalgia rheumatica? J Clin Neurosci 1999; 6(3): 255-9.
[http://dx.doi.org/10.1016/S0967-5868(99)90517-9] [PMID: 18639165]
[9] Pascuzzi RM, Roos KL, Phillips LH II. Granulomatous inflammatory myopathy associated with myasthenia gravis. A case report and review of the literature Arch Neurol 1986; 43(6): 621-3.
[http://dx.doi.org/10.1001/archneur.1986.00520060079025] [PMID: 3718292]
[10] Tanaka M, Senoh Y, Okamato K, Morimatsu M, Hirai S. [A case of granulomatous polymyositis associated with mixed connective tissue disease] Rinsho Shinkeigaku 1985; 25(9): 1039-45.
[PMID: 4092400]
[11] Bagdasaryan R, Donahue JE. Granulomatous myositis in association with chronic graft vs. host disease Med Health R I 2007; 90(9): 287.
[PMID: 17970330]
[12] Ménard DB, Haddad H, Blain JG, Beaudry R, Devroede G, Massé S. Granulomatous myositis and myopathy associated with crohn’s colitis N Engl J Med 1976; 295(15): 818-9.
[http://dx.doi.org/10.1056/NEJM197610072951506] [PMID: 958278]
[13] Herrmann DN, Blaivas M, Wald JJ, Feldman EL. Granulomatous myositis, primary biliary cirrhosis, pancytopenia, and thymoma Muscle Nerve 2000; 23(7): 1133-6.
[http://dx.doi.org/10.1002/1097-4598(200007)23:7<1133::AID-MUS20>3.0.CO;2-E] [PMID: 10883012]
[14] Min HS, Hyun CL, Paik JH, et al. An autopsy case of aggressive CD30+ extra-nodal NK/T-cell lymphoma initially manifested with granulomatous myositis Leuk Lymphoma 2006; 47(2): 347-52.
[http://dx.doi.org/10.1080/10428190500288545] [PMID: 16321870]
[15] Kojan S, Alothman A, Althani Z, et al. Granulomatous myositis associated with brucellosis: a case report and literature review Muscle Nerve 2012; 45(2): 290-3.
[http://dx.doi.org/10.1002/mus.22261] [PMID: 22246889]
[16] Pearl GS, Sieger B. Granulomatous Pneumocystis carinii myositis presenting as an intramuscular mass Clin Infect Dis 1996; 22(3): 577-8.
[http://dx.doi.org/10.1093/clinids/22.3.577] [PMID: 8852986]
[17] Wang WY, Lin FC, Tsao TY, Lu JJ. Tuberculous myositis: an unusual presentation of extrapulmonary tuberculosis J Microbiol Immunol Infect 2007; 40(1): 79-82.
[PMID: 17332912]
[18] Mozaffar T, Lopate G, Pestronk A. Clinical correlates of granulomas in muscle J Neurol 1998; 245(8): 519-24.
[http://dx.doi.org/10.1007/s004150050236] [PMID: 9747915]
[19] Le Roux K, Streichenberger N, Vial C, et al. Granulomatous myositis: a clinical study of thirteen cases Muscle Nerve 2007; 35(2): 171-7.
[http://dx.doi.org/10.1002/mus.20683] [PMID: 17068767]
[20] Tews DS, Pongratz DE. Immunohistological analysis of sarcoid myopathy J Neurol Neurosurg Psychiatry 1995; 59(3): 322-5.
[http://dx.doi.org/10.1136/jnnp.59.3.322] [PMID: 7673968]
[21] Karadeli E, Ulu EM. Acute sarcoid myositis with unusual radiologic findings Diagn Interv Radiol (Ank) 2010; 16(3): 232-5.
[PMID: 19838983]
[22] Dufour JF, Billotey C, Streichenberger N, Bouhour F, Broussolle C, Sève P. [Sarcoidosis demonstrated by fluorodeoxyglucose positron emission tomography in a case of granulomatous myopathy] Rev Med Interne 2007; 28(8): 568-70.
[http://dx.doi.org/10.1016/j.revmed.2007.03.003] [PMID: 17445952]

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