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Challenging Mimickers in the Diagnosis of Sarcoidosis: a Case Study

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Challenging Mimickers in the Diagnosis of Sarcoidosis: a Case Study diagnostics Article Challenging Mimickers in the Diagnosis of Sarcoidosis: A Case Study Thomas El Jammal 1, Yvan Jamilloux 1 , Mathieu Gerfaud-Valentin 1 , Gaëlle Richard-Colmant 1, Emmanuelle Weber 1, Arthur Bert 1,Géraldine Androdias 2 and Pascal Sève 1,3,* 1 Department of Internal Medicine, Lyon University Hospital, 69004 Lyon, France; [email protected] (T.E.J.); [email protected] (Y.J.); [email protected] (M.G.-V.); [email protected] (G.R.-C.); [email protected] (E.W.); [email protected] (A.B.) 2 Department of Neurology, Service Sclérose en Plaques, Pathologies de la Myéline et Neuro-Inflammation, Hôpital Neurologique Pierre Wertheimer, Lyon University Hospital, F-69677 Bron, France; [email protected] 3 Research on Healthcare Performance (RESHAPE), INSERM U1290, 69373 Lyon, France * Correspondence: [email protected]; Tel.: +33-426-732-636 Abstract: Sarcoidosis is a systemic granulomatous disease of unknown cause characterized by a wide variety of presentations. Its diagnosis is based on three major criteria: a clinical presentation compati- ble with sarcoidosis, the presence of non-necrotizing granulomatous inflammation in one or more tissue samples, and the exclusion of alternative causes of granulomatous disease. Many conditions may mimic a sarcoid-like granulomatous reaction. These conditions include infections, neoplasms, immunodeficiencies, and drug-induced diseases. Moreover, patients with sarcoidosis are at risk of Citation: El Jammal, T.; Jamilloux, Y.; developing opportunistic infections or lymphoma. Reliably confirming the diagnosis of sarcoidosis Gerfaud-Valentin, M.; and better identifying new events are major clinical problems in daily practice. To address such Richard-Colmant, G.; Weber, E.; Bert, issues, we present seven emblematic cases, seen in our department, over a ten-year period along A.; Androdias, G.; Sève, P. with a literature review about case reports of conditions misdiagnosed as sarcoidosis. Challenging Mimickers in the Diagnosis of Sarcoidosis: Keywords: sarcoidosis; diagnosis; lymphoma; opportunistic infections A Case Study. Diagnostics 2021, 11, 1240. https://doi.org/10.3390/ diagnostics11071240 Academic Editor: Claudio Tana 1. Introduction Sarcoidosis was first described by Jonathan Hutchinson, an English physician, in 1877 [1]. Received: 16 June 2021 This multi-systemic disease is characterized by the infiltration of various tissues by non- Accepted: 7 July 2021 necrotizing granulomas [2]. Although the mechanisms of granuloma formation are more Published: 12 July 2021 and more clearly understood, there is currently no known cause of sarcoidosis (if there is any). Sarcoidosis can affect a wide variety of people, from the youngest to the oldest, Publisher’s Note: MDPI stays neutral regardless of ethnicity. Nevertheless, sarcoidosis is more common in young adults and with regard to jurisdictional claims in classically starts earlier in men than women. In total, 70% of patients are aged between published maps and institutional affil- 25 and 40 years at presentation. A second peak of incidence is observed in women over iations. 50 years old [3]. Its annual incidence is estimated between 2.3 and 11/100,000 while the estimated prevalence varies from 2 to 160 cases per 100,000 individuals. This large range for prevalence relies on the variability in diagnostic tools between studies as well as differences in the relative proportions of different ethnicities [4]. About two thirds Copyright: © 2021 by the authors. of sarcoidosis patients experience a self-remitting disease without immunosuppressants, Licensee MDPI, Basel, Switzerland. while the remaining third evolve through a chronic disease in which corticosteroids are the This article is an open access article cornerstone of the treatment [4–6]. distributed under the terms and The diagnosis of sarcoidosis is still based on a set of arguments represented by three conditions of the Creative Commons major criteria: clinical compatibility with the diagnosis of sarcoidosis, the absence of a dif- Attribution (CC BY) license (https:// ferential diagnosis that is at least as likely, and the demonstration of epithelioid granulomas creativecommons.org/licenses/by/ on histology [6]. Indeed, sarcoidosis can mimic other conditions which, if misdiagnosed as 4.0/). Diagnostics 2021, 11, 1240. https://doi.org/10.3390/diagnostics11071240 https://www.mdpi.com/journal/diagnostics Diagnostics 2021, 11, 1240 2 of 36 sarcoidosis, may result in a delay in diagnosis or treatment that is harmful to the patient especially in case of neoplastic or infectious diseases. These conditions include infections (e.g., tuberculosis, Bartonella spp.), neoplastic disorders (e.g., lymphomas), systemic dis- eases with granulomatosis (e.g., granulomatosis with polyangiitis (GPA), Crohn’s disease [CD]), common variable immunodeficiency (CVID) and drug-induced (DI) sarcoid-like reactions (SLR). Before starting invasive investigations or initiating an immunosuppressive treatment, the clinician has to pay attention to these mimickers. Moreover, sarcoidosis patients are at increased risk of developing infections [7] and more specifically opportunis- tic infections which could mimic sarcoidosis or imitate a sarcoidosis flare [8]. The risk of developing solid neoplasia or hematological malignancies is increased in sarcoidosis patients [9]. This statement emphasizes the need for the clinician to pay attention to these differentials in that a delayed diagnosis can have negative consequences for the patient. We hereby describe selected cases that came to our attention after referral to our inter- nal medicine department for a suspected sarcoidosis diagnosis. In all cases, the physical examination, radiological examinations and the advanced microbiological or histological approaches allowed the identification of these differentials. We have chosen to focus on seven sarcoid mimickers and to summarize their main clinical features in light of their misleading or atypical presentation and the associated diagnostic approach. 2. Materials and Methods This article is a series of original cases and adheres to the principles of the Declaration of Helsinki of 1964 and its latest amendments. The informed consent of all participants was obtained, and the study was approved by the Local Institutional Review Board. The case reports were chosen among consecutive patients referred to our internal medicine department. Each case report was selected as it was considered by the authors to be representative of the diagnostic issues faced by the clinician. This study received approval from the local ethics committee in February 2019 (No 19–31). In order to describe the updated diagnosis of these diseases, we conducted a review of the English and French medical literature on the Medline database, using the keywords “sarcoidosis”, “mimickers”, “misdiagnosed” and “differential diagnosis”. We excluded articles written in languages other than English or French. 3. Clinical Cases 3.1. Infectious Diseases 3.1.1. Case Description A 70-year-old man was referred to our internal medicine department for suspected oral sarcoidosis. He had a past medical history of type 2 diabetes treated with insulin, and prostate cancer in remission treated with radical prostatectomy along with adjuvant radiation therapy. He reported a trip to India four months after the onset of symptoms, with no medical issues at the time. He noticed the appearance of an ulceration around tooth 38 in June 2016. A first gingi- val biopsy was performed by his dentist three months later, finding giant-cell granuloma without necrosis. A second biopsy was performed in a maxillofacial surgery department, showing again a non-necrotizing giant-cell granuloma pattern. Neither sample was tested for mycobacteria (Ziehl Nielsen staining, culture or polymerase chain reaction [PCR]). Of note, a few days after returning from India (a trip the patient took after the onset of oral ulceration), he developed dry cough which led to further investigations. A thoracic CT scan showed interstitial lung disease with diffuse micronodules, retractive consolidations, and traction bronchiectasis. There was no mediastino-hilar adenopathy. This pattern was initially considered to be consistent with thoracic sarcoidosis. Oral corticosteroid therapy 40 mg/day was then started, which improved the dry cough, but with significant corticos- teroid dependence and corticosteroids side effects such as decompensation of his diabetes. The patient was then referred to our internal medicine department for further management of his atypical, presumed sarcoidosis. Diagnostics 2021, 11, 1240 3 of 36 Detailed patient interview did not reveal any recent altered general condition nor extra- respiratory symptoms. A magnetic resonance imaging (MRI) of the jaw was performed and evidenced a left mandibular lesion extending to the cheek, with numerous satellite enlarged lymph nodes, including a necrotic one. Biological examinations revealed an inflammatory syndrome with an elevated C-reactive protein (16.9 mg/L), and a positive interferon-gamma release assay (TB GOLD TEST QUANTIFERON: 5.66). There was no elevation of angiotensin-converting enzyme levels. A bronchial fibroscopy was performed. The bronchial biopsy evidenced nothing except aspecific inflammation without granuloma. Finally, the bronchoalveolar lavage fluid culture revealed the presence of Mycobac- terium tuberculosis (Mtb). The search for rpoB mutations was positive,
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