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Development of pulmonary sarcoidosis in Crohn’s disease patient under infliximab biosimilar treatment after long-term original infliximab treatment: a case report and literature review

BMC Gastroenterology volume 21, Article number: 373 (2021) Cite this article

Abstract

Background

Inflammatory bowel disease (IBD) is chronic inflammation of the gastrointestinal tract, although its etiology has largely been unclear. Tumor necrosis factor inhibitors (TNF-I) are effective for the treatment. Recently, biosimilars of TNF-I, such as CT-P13, have been developed and are thought to possess equal efficacy and safety to the original TNF-I. Sarcoidosis is also a systemic granulomatous disease of unknown etiology. In steroid-resistant cases of sarcoidosis, TNF-I have been reported effective for achieving resolution. However, the progression of sarcoidosis due to the TNF-I also has been reported. We herein report a case of pulmonary sarcoidosis with a Crohn’s disease (CD) patient developed after a long period administration (15 years) of TNF-I.

Case presentations

A 37-year-old woman with CD who had been diagnosed at 22 years old had been treated with the TNF-I (original infliximab; O-IFX and infliximab biosimilar; IFX-BS). Fifteen years after starting the TNF-I, she developed a fever and right chest pain. Chest computed tomography (CT) revealed clustered small nodules in both lungs and multiple enlarged hilar lymph nodes. Infectious diseases including tuberculosis were negative. Bronchoscopic examination was performed and the biopsy specimens were obtained. A pathological examination demonstrated noncaseating granulomatous lesions and no malignant findings. TNF-I were discontinued because of the possibility of TNF-I-related sarcoidosis. After having discontinued for four months, her symptoms and the lesions had disappeared completely. Fortunately, despite the discontinuation of TNF-I, she has maintained remission.

Conclusions

To our knowledge, this is the first case in which sarcoidosis developed after switching from O-IFX to IFX-BS. To clarify the characteristics of the cases with development of sarcoidosis during administration of TNF-I, we searched PubMed and identified 106 cases. When developing an unexplained fever, asthenia, uveitis and skin lesions in patients with TNF-I treatment, sarcoidosis should be suspected. Once the diagnosis of sarcoidosis due to TNF-I was made, the discontinuation of TNF-I and administration of steroid therapy should be executed promptly. When re-starting TNF-I, another TNF-I should be used for disease control. Clinicians should be aware of the possibility of sarcoidosis in patients under anti-TNF therapy.

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Background

Inflammatory bowel disease (IBD) is chronic inflammation of the entire gastrointestinal tract, although its etiology has largely been unclear. Tumor necrosis factor (TNF) inhibitors are known to be effective treatment for treating IBD patients with moderate to severe activity. The cost-effectiveness and efficacy of TNF inhibitors (TNF-I) has been demonstrated through their reduction in the rates of hospitalization and surgery [1]. Recently, biosimilars of TNF-I, such as CT-P13, have been developed and are thought to possess equal efficacy and safety to the original with dramatic cost benefits. Switching from the original to a biosimilar is thus considered an acceptable treatment [2, 3].

Similar to IBD, sarcoidosis is a systemic granulomatous disease of unknown etiology, affecting various organs, including the lung, heart, lymphatic system and skin. In many cases of sarcoidosis, steroids are effective for treatment, and in case of steroid resistance, TNF-I are reported to be effective. While some studies have reported that the administration of TNF-I caused the progression of sarcoidosis, no reports regarding the relationship between sarcoidosis and infliximab biosimilar (IFX-BS) have been published.

We herein report a case of pulmonary sarcoidosis in a Crohn’s disease (CD) patient during fifteen years administration of IFX-BS after switching from original infliximab (O-IFX). To our knowledge, this is the first case of sarcoidosis developing after switching from O-IFX to IFX-BS in a CD patient.

Case presentation

A 37-year-old Japanese woman was diagnosed with CD at 22 years of age. She had no relevant family history. At the onset of CD, she had symptoms of fever, abdominal pain, and frequent diarrhea. On total colonoscopy, she was found to have multiple longitudinal ulcers in the terminal ileum with stricture. Her symptoms were severe; thus, we administered O-IFX first, without steroid therapy. Clinical remission was obtained after 3 months of O-IFX treatment. She had maintained clinical remission without any adverse events for twelve years after the administration of O-IFX, and then O-IFX was switched to IFX-BS (CT-P13) after obtaining informed consent, because IFX-BS demonstrated equivalent efficacy and safety in the treatment of CD and the drug price was approximately half that of O-IFX in Japan. After switching to IFX-BS, clinical remission was still maintained for three years.

Fifteen years after starting the TNF-I (O-IFX and CT-P13), she developed a fever and right chest pain but had no respiratory symptoms, such as cough or sputum. Laboratory findings showed total bilirubin, 1.5 mg/dL; alanine aminotransferase, 248 U/L; aspartate aminotransferase, 105 U/L; gamma glutamyl aminotransferase, 192 U/L; alkaline phosphatase, 489 U/L; C-reactive protein (CRP), 0.44 mg/dL; anti-nuclear antibody, 1:160. Hepatitis B and C were negative. Chest X-ray and computed tomography (CT) revealed clustered small nodules in both lungs and multiple enlarged hilar lymph nodes (Fig. 1). The interferon gamma release assay and an acid-fast bacilli antibody were negative. A tuberculosis polymerase chain reaction (PCR) assay and bacterium culture of her sputum were both negative. Subsequently, a bronchoscopic examination was performed, and biopsy specimens were obtained from the middle and lower lobes of the right lung. A pathological examination demonstrated noncaseating granulomatous lesions and no malignant findings (Fig. 2). The serum angiotensin-converting enzyme and lysozyme levels were within normal limits, and soluble interleukin-2 receptor (sIL-2R) was increased to 627 U/mL (reference range 122–496 U/mL). Thus, the diagnosis of sarcoidosis was made. Her symptoms (low-grade fever and slight chest pain) could be sufficiently managed by the administration of an analgesic antipyretic. Therefore, we did not use steroids and, considering the possibility of TNF-I related sarcoidosis, TNF-I was discontinued. Subsequently, her symptoms improved gradually. In addition, the abnormal laboratory findings, including hepatobiliary enzymes, improved naturally without any treatment after one month. After having discontinued TNF-I for four months, her symptoms of sarcoidosis and the lesions detected by chest CT had disappeared completely (Fig. 3). Fortunately, despite the discontinuation of TNF-I, she has maintained clinical and endoscopic remission for 18 months after the discontinuation of TNF-I.

Fig. 1
figure 1

CT scan showing multiple nodular lung lesions and mediastinal and hilar lymphadenopathies

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Fig. 2
figure 2

Histological findings of the lung. Histology demonstrated noncaseating granulomatous lesions and no malignant findings (X100)

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Fig. 3
figure 3

The nodular lung lesions disappeared after discontinuation of IFX-BS in CT scan

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Discussions and conclusions

We herein report the pulmonary sarcoidosis after the long-term use of TNF-inhibitors in a CD patient.

Two possible causes were considered responsible for the development of sarcoidosis in our case: the long-term IFX administration and the switching from the original agent to its biosimilar. To confirm the involvement of these causes and clarify the characteristics of patients likely to develop sarcoidosis under TNF-I therapy, we searched for case reports in PubMed concerning sarcoidosis due to TNF-I using the combination of the heading terms ‘infliximab’, ‘adalimumab’, ‘etanercept’, ‘certolizumab’, ‘golimumab’, ‘infliximab biosimilar’, with or without ‘Crohn’s disease’, combined with ‘sarcoidosis’. We identified 6 articles concerning 7 cases using the word combination with CD [4,5,6,7,8,9] and 65 articles concerning 99 cases using the word combination without CD (details in Additional file 1: Table 1) [10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74]. Regarding the impact of long-term TNF-I administration, in 103 cases, the median duration of developing sarcoidosis was 21 (range 1–90) months, and the maximum period was 90 months, according to previous reports. However, since those reports contained various diseases, we reviewed the seven cases with CD (excluding our own case). The median duration to the development of sarcoidosis was 24 (range 7–90) months, and the maximum period was 90 months. Our case was administered O-IFX for 144 months and then IFX-BS for 36 months. Based on the previous reports, the duration of 180 months until the development of sarcoidosis in our case was the longest, exceeding the longest period in previous reports by more than 7 years. Long-term IFX administration may affect the development of sarcoidosis, as the administration of TNF-I presumably induces cytokine imbalance (TNF-α suppression and excessive Interferon-α production) [75]. It took a very long time to for the patient to develop sarcoidosis; however, it may have been a possible complication as the time to the induction of cytokine imbalance seems to show individual differences. In addition, infection is suggested to be a cause of sarcoidosis, and the treatment with TNF-I increases the risk of various infections [10,11,12], which can lead to the onset of sarcoidosis. Prudent follow-up should thus be performed, including observation of CD patients under long-term IFX administration. Regarding the impact of switching from O-IFX to IFX-BS, we thought that the possibility of sarcoidosis caused by changing O-IFX to IFX-BS would be quite low because of the very slight differences in the sugar chain sequences of O-IFX and IFX-BS and their almost equivalent immunogenicity [76].

Regarding other characteristics of CD patients, the median age was 30 (range 21–44) years, and the male:female ratio was 5:3 when including our case. The causative TNF inhibitors were adalimumab (ADA) (n = 4, 50.0%, including a case switching from IFX to ADA) and IFX (n = 4, 50%, including our case). The symptoms depended on the organs involved. Our case showed an unexplained fever and chest pain because of pleuritis. Asthenia, uveitis, and skin lesions were also reported. There were no specific symptoms.

In this case, the serum ACE level was normal. It was reported that serum ACE shows low sensitivity and specificity in the diagnosis of sarcoidosis [77]. In addition, it is known that the serum ACE level is affected by genetic polymorphism [78, 79]. Clinicians should recognize that the serum ACE levels alone are not enough to diagnose sarcoidosis.

We also investigated the difference in the duration until the development of sarcoidosis under IFX and ADA therapy in the six CD cases without switching cases. The median duration to the development of sarcoidosis in CD patients under IFX (n = 3) and ADA (n = 3) therapy was 12 and 24 months, respectively. Patients receiving ADA therapy showed a longer duration until development than those receiving IFX, which might have influenced the difference in antibody type, such as chimeric human-mouse IgG monoclonal antibody and fully human monoclonal antibody. However, the number of such cases has been limited so far, so the accumulation of more cases will be required to verify whether or not differences in antibodies affects the development of sarcoidosis.

Regarding the therapy delivered after the development of sarcoidosis, six of eight cases discontinued TNF-I, two without steroid and four with additional steroid, and two cases continued TNF-I therapy while adding steroid therapy or topical therapy. All six cases who discontinued TNF-I with/without steroids showed the resolution of sarcoidosis. In one case, in which the patient continued TNF-I with steroid treatment, improvement of the lung lesion was observed. In one case in which the patient continued TNF-I with topical steroid treatment, improvement of the lung lesion, but not the skin lesion, was observed. In CD patients who develop sarcoidosis, discontinuation of TNF-I seems to be a feasible treatment. Among 107 cases with various diseases, 47 discontinued TNF-I without the addition of steroid therapy, and sarcoidosis was improved or resolved in 43 (91.5%), while 49 cases discontinued TNF-I with the addition of steroid therapy, and 46 (93.9%) showed improvement or resolution of sarcoidosis. These data support the notion that discontinuing TNF-I is effective for treating patients with chronic inflammatory disease, but the efficacy of additional steroid therapy is unclear.

Our case has maintained remission despite having discontinued TNF-I; however, TNF-I may be key drugs for CD patients. Thus, whether or not TNF-I can be re-initiated for these patients is important to clarify. Only one CD patient re-initiated the same TNF inhibitor (O-IFX) with no recurrence of sarcoidosis observed [8]. When expanding target diseases to include rheumatoid arthritis, ankylosing spondylitis, psoriatic arthritis, spondyloarthropathy, psoriasis, CD, juvenile idiopathic arthritis, SAPHO (synovitis, pustulosis, acne, hyperostosis, osteitis), ulcerative colitis, 25 patients re-initiated TNF-I. Of 25 patients, 7 were administered the same TNF-I, and sarcoidosis consequently recurred in 4 cases (57.1%) [8, 11, 23, 27, 39, 63]. Eighteen cases started another TNF-I, and sarcoidosis recurred in 3 cases (16.7%) [13, 27, 64,65,66,67,68,69,70,71,72,73,74]. These data suggested that another TNF-I should be administered when re-initiating TNF-I in such patients.

In conclusion, should be aware that TNF-I can cause several drug related complications, including sarcoidosis. Sarcoidosis due to TNF-I can be caused by IFX-BS and develop even after long-term administration. Clinicians should be aware of the possibility of sarcoidosis in patients under anti-TNF therapy. The efficacy of additional steroid therapy remains unclear; however, TNF-I should be discontinued as soon as possible, even in CD patients who maintain long-term remission with TNF-I. When re-starting TNF-I, another TNF-I should be used for disease control, as relapse of sarcoidosis is frequent when patients are treated with the same TNF-I (Table 1).

Table 1 The characteristics of sarcoidosis in CD patients receiving TNF inhibitor therapy
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Availability of data and materials

The datasets used and/or analyzed during the current study available from the corresponding author on reasonable request.

Abbreviations

IBD:

Inflammatory bowel disease

TNF:

Tumor necrosis factor

TNF-I:

TNF inhibitor

CD:

Crohn’s disease

O-IFX:

Original infliximab

IFX-BS:

Infliximab biosimilar

CT:

Computed tomography

ADA:

Adalimumab

References

  1. van der Valk ME, Mangen MJJ, Leenders M, et al. Health care costs of inflammatory bowel disease have shifted from hospitalisation and surgery towards anti-TNFα therapy: results from the COIN study. Gut. 2014;63:72–9.

    Article  PubMed  Google Scholar 

  2. Feagan BG, Lam G, Ma C, et al. Systematic review: efficacy and safety of switching patients between reference and biosimilar infliximab. Aliment Pharmacol Ther. 2019;49:31–40.

    Article  CAS  PubMed  Google Scholar 

  3. Ye BD, Pesegova M, Alexeeva O, et al. Efficacy and safety of biosimilar CT-P13 compared with originator infliximab in patients with active Crohn’s disease: an international, randomised, double-blind, phase 3 non-inferiority study. Lancet. 2019;393(10182):1699–707.

    Article  CAS  PubMed  Google Scholar 

  4. Simonetto DA, Papadakis KA. New-onset paresthesias in inflammatory bowel disease. Gastroenterology. 2015;148:906–7.

    Article  PubMed  Google Scholar 

  5. McDonnell MJ, Rutherford RM, O’Regan A. Sarcoidosis complicating treatment with adalimumab for Crohn’s disease. J Crohns Colitis. 2014;8:1140–1.

    Article  CAS  PubMed  Google Scholar 

  6. Kotze PG, de Barcelos IF, da Silva Kotze LM. Sarcoidosis during therapy with adalimumab in a Crohn’s disease patient: a paradoxical effect. J Crohns Colitis. 2013;7:e599-600.

    Article  PubMed  Google Scholar 

  7. Takahashi H, Kaneta K, Honma M, et al. Sarcoidosis during infliximab therapy for Crohn’s disease. J Dermatol. 2010;37:471–4.

    Article  CAS  PubMed  Google Scholar 

  8. Tae KK, Sun HK, Hee SM, et al. Pulmonary sarcoidosis that developed during the treatment of a patient with Crohn disease by using infliximab. Ann Coloproctol. 2017;33:74–7.

    Article  Google Scholar 

  9. Decock A, Van Assche G, Vermeire S, et al. Sarcoidosis-like lesions: another paradoxical reaction to anti-TNF therapy? J Crohns Colitis. 2017;11:378–83.

    PubMed  Google Scholar 

  10. Dhaille F, Viseux V, Caudron A, et al. Cutaneous sarcoidosis occurring during anti-TNF-alpha treatment: report of two cases. Dermatology. 2010;220:234–7.

    Article  CAS  PubMed  Google Scholar 

  11. Van Der Stoep D, Braunstahl G, Van Zeben J, Wouters J. Sarcoidosis during anti-tumor necrosis factor-α therapy: no relapse after rechallenge in rheumatology and related fields. J Rheumatol. 2009; 36.

  12. Toussirot É, Pertuiset É, Kantelip B, Wendling D. Sarcoidosis occuring during anti-TNF-α treatment for inflammatory rheumatic diseases: report of two cases. Clin Exp Rheumatol. 2008;26:471–5.

    CAS  PubMed  Google Scholar 

  13. Daïen CI, Monnier A, Claudepierre P, Constantin A, et al. Sarcoid-like granulomatosis in patients treated with tumor necrosis factor blockers: 10 cases. Rheumatology (Oxford). 2009;48:883–6.

    Article  CAS  Google Scholar 

  14. Massara A, Cavazzini L, La Corte R, Trotta F. Sarcoidosis appearing during anti-tumoical phenomenon. Two case reports and literature review. Semin Arthritis Rheum. 2010;39:313–9.

    Article  CAS  PubMed  Google Scholar 

  15. Scailteux L-M, Guedes C, Polard E, Perdriger A. Sarcoidosis after adalimumab treatment in inflammatory rheumatic diseases: a report of two cases and literature review. Presse Med. 2015;44:4–10.

    Article  PubMed  Google Scholar 

  16. Miyagi R, Ideguchi H, Soga T, et al. Development of pulmonary and cardiac sarcoidosis during etanercept therapy. Int J Rheum Dis. 2014;17:810–2.

    Article  PubMed  CAS  Google Scholar 

  17. Watrin A, Royer M, Legrand E, et al. Severe hypercalcemia revealing sarcoidosis precipitated by etanercept. Rev Mal Respir. 2014;31:255–8.

    Article  CAS  PubMed  Google Scholar 

  18. Durel C-A, Feurer E, Pialat J-B, et al. Etanercept may induce neurosarcoidosis in a patient treated for rheumatoid arthritis. BMC Neurol. 2013;13:212.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Alhajri M, Aljumaah S, Aleyouni Y, et al. Granulomatous disease in a child treated with etanercept. Int J Rheum Dis. 2013;16:472–4.

    Article  PubMed  Google Scholar 

  20. Christoforidou A, Goudakos J, Bobos M, et al. Sarcoidosis-like granulomatosis of the hypopharynx as a complication of anti-TNF therapy. Am J Otolaryngol. 2013;34:268–72.

    Article  PubMed  Google Scholar 

  21. Unterstell N, Bressan AL, Serpa LA, et al. Systemic sarcoidosis induced by etanercept: first Brazilian case report. An Bras Dermatol. 2013;88(6 Suppl 1):197–9.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Lamrock E, Brown P. Development of cutaneous sarcoidosis during treatment with tumour necrosis alpha factor antagonists. Australas J Dermatol. 2012;53:e87-90.

    Article  PubMed  Google Scholar 

  23. Tong D, Manolios N, Howe G, et al. New onset sarcoid-like granulomatosis developing during anti-TNF therapy: an under-recognised complication. Intern Med J. 2012;42:89–94.

    Article  CAS  PubMed  Google Scholar 

  24. Fok KC, Ng WWS, Henderson CJ, et al. Cutaneous sarcoidosis in a patient with ulcerative colitis on infliximab. J Crohns Colitis. 2012;6:708–12.

    Article  PubMed  Google Scholar 

  25. Seve P, Varron L, Broussolle C, et al. Sarcoid-related uveitis occurring during adalimumab therapy. Ocul Immunol Inflamm. 2012;20:59–60.

    Article  CAS  PubMed  Google Scholar 

  26. Fonollosa A, Artaraz J, Les I, et al. Sarcoid intermediate uveitis following etanercept treatment: a case report and review of the literature. Ocul Immunol Inflamm. 2012;20:44–8.

    Article  CAS  PubMed  Google Scholar 

  27. Skoie IM, Wildhagen K, Omdal R. Development of sarcoidosis following etanercept treatment: a report of three cases. Rheumatol Int. 2012;32:1049–53.

    Article  CAS  PubMed  Google Scholar 

  28. Haroon M, Ryan JG, Harney S. Development of sarcoidosis 6-month post discontinuation of etanercept: coincidence or real association? Clin Rheumatol. 2011;30:1095–8.

    Article  PubMed  Google Scholar 

  29. Gifre L, Ruiz-Esquide V, Xaubet A, et al. Lung sarcoidosis induced by TNF antagonists in rheumatoid arthritis: a case presentation and a literature review. Arch Bronconeumol. 2011;47:208–12.

    Article  PubMed  Google Scholar 

  30. Salvatierra J, Magro-Checa C, Rosales-Alexander JL, et al. Acute sarcoidosis as parotid fever in rheumatoid arthritis under anti-tumor necrosis factor-alpha therapy. Rheumatology (Oxford). 2011;50:1346–8.

    Article  Google Scholar 

  31. Kerjouan M, Jouneau S, Lena H, et al. Pulmonary sarcoidosis developing during treatment with etanercept. Rev Mal Respir. 2011;28:360–4.

    Article  CAS  PubMed  Google Scholar 

  32. Kanellopoulou T, Filiotou A, Kranidioti H, et al. Sarcoid-like granulomatosis in patients treated with anti-TNFα factors. A case report and review of the literature. Clin Rheumatol. 2011;30:581–3.

    Article  PubMed  Google Scholar 

  33. Cuchacovich R, Hagan J, Khan T, et al. Tumor necrosis factor-alpha (TNF-α)-blockade-induced hepatic sarcoidosis in psoriatic arthritis (PsA): case report and review of the literature. Clin Rheumatol. 2011;30:133–7.

    Article  PubMed  Google Scholar 

  34. Clementine RR, Lyman J, Zakem J, et al. Tumor necrosis factor-alpha antagonist-induced sarcoidosis. J Clin Rheumatol. 2010;16:274–9.

    Article  PubMed  Google Scholar 

  35. Pink AE, Fonia A, Smith CH, et al. The development of sarcoidosis on antitumour necrosis factor therapy: a paradox. Br J Dermatol. 2010;163:648–9.

    Article  CAS  PubMed  Google Scholar 

  36. Marcella S, Welsh B, Foley P. Development of sarcoidosis during adalimumab therapy for chronic plaque psoriasis. Australas J Dermatol. 2011;52:e8-11.

    Article  PubMed  Google Scholar 

  37. Takatori S, Kamata Y, Murosaki T, et al. Abrupt development of sarcoidosis with a prodromal increase in plasma osteopontin in a patient with rheumatoid arthritis during treatment with etanercept. J Rheumatol. 2010;37:210–1.

    Article  PubMed  Google Scholar 

  38. Samimi M, Lorette G, Machet L, et al. Facial granulomatous nodules during etanercept treatment for psoriasis. Int J Dermatol. 2009;48:1025–7.

    Article  PubMed  Google Scholar 

  39. Toussirot E, Berthelot JM, Pertuiset E, et al. Pulmonary nodulosis and aseptic granulomatous lung disease occurring in patients with rheumatoid arthritis receiving tumor necrosis factor-alpha-blocking agent: a case series. J Rheumatol. 2009;36:2421–7.

    Article  PubMed  Google Scholar 

  40. Suzuki J, Goto H. Uveitis associated with sarcoidosis exacerbated by etanercept therapy. Jpn J Ophthalmol. 2009;53:439–40.

    Article  PubMed  Google Scholar 

  41. Josse S, Klemmer N, Moreno-Swirc S, et al. Infliximab induced skin and pulmonary sarcoidosis in a rheumatoid arthritis patient. Joint Bone Spine. 2009;76:718–9.

    Article  PubMed  Google Scholar 

  42. Ishiguro T, Takayanagi N, Kurashima K, et al. Development of sarcoidosis during etanercept therapy. Intern Med. 2008;47:1021–5.

    Article  PubMed  Google Scholar 

  43. Louie GH, Chitkara P, Ward MM. Relapse of sarcoidosis upon treatment with etanercept. Ann Rheum Dis. 2008;67:896–8.

    Article  CAS  PubMed  Google Scholar 

  44. Farah M, Al Rashidi A, Owen DA, et al. Granulomatous hepatitis associated with etanercept therapy. J Rheumatol. 2008;35:349–51.

    PubMed  Google Scholar 

  45. Farah RE, Shay MD. Pulmonary sarcoidosis associated with etanercept therapy. Pharmacotherapy. 2007;27:1446–8.

    Article  CAS  PubMed  Google Scholar 

  46. Sturfelt G, Christensson B, Bynke G, et al. Neurosarcoidosis in a patient with rheumatoid arthritis during treatment with Silverman featuring research articles on clinical subjects from scientists working in rheumatology and related fields. J Rheumatol. 2007;34:12–6.

    Google Scholar 

  47. Verschueren K, Van Essche E, Verschueren P, et al. Development of sarcoidosis in etanercept-treated rheumatoid arthritis patients. Clin Rheumatol. 2007;26:1969–71.

    Article  PubMed  Google Scholar 

  48. Almodóvar R, Izquierdo M, Zarco P, et al. Pulmonary sarcoidosis in a patient with ankylosing spondylitis treated with infliximab. Clin Exp Rheumatol. 2007;25:99–101.

    PubMed  Google Scholar 

  49. Bachmeyer C, Blum L, Petitjean B, et al. Granulomatous tattoo reaction in a patient treated with etanercept. J Eur Acad Dermatol Venereol. 2007;21:550–2.

    CAS  PubMed  Google Scholar 

  50. Kudrin A, Chilvers ER, Ginawi A, et al. Sarcoid-like granulomatous disease following etanercept treatment for RA. J Rheumatol. 2007;34:648–9.

    PubMed  Google Scholar 

  51. González-López MA, Blanco R, González-Vela MC, et al. Development of sarcoidosis during etanercept therapy. Arthritis Rheum. 2006;55:817–20.

    Article  PubMed  Google Scholar 

  52. O’Shea FD, Marras TK, Inman RD. Pulmonary sarcoidosis developing during infliximab therapy. Arthritis Rheum. 2006;55:978–81.

    Article  PubMed  CAS  Google Scholar 

  53. Hashkes PJ, Shajrawi I. Sarcoid-related uveitis occurring during etanercept therapy. Clin Exp Rheumatol. 2003;21:645–6.

    CAS  PubMed  Google Scholar 

  54. Hübscher O, Re R, Iotti R. Pulmonary rheumatoid nodules in an etanercept-treated patient. Arthritis Rheum. 2003;48:2077–8.

    Article  PubMed  Google Scholar 

  55. Peno-Green L, Lluberas G, Kingsley T, et al. Lung injury linked to etanercept therapy. Chest. 2002;122:1858–60.

    Article  PubMed  Google Scholar 

  56. Morgane V, Jean-Charles C, Nicolas M, et al. Renal sarcoid-like granulomatosis during anti-TNF therapy. Kidney Int. 2014;86:215.

    Article  CAS  PubMed  Google Scholar 

  57. Dorta ZK, Ochieng P, Donald F, et al. Pulmonary sarcoidosis and latent tuberculosis in a patient with psoriasis treated with adalimumab. Dermatol Online J. 2015.

  58. Nnodum BN, Hariri LP, Mavrommati D, Dudley L, et al. A case of severe symptomatic central nervous system sarcoidosis secondary to treatment with adalimumab. Case Rep Rheumatol. 2019;8:7121539.

    Google Scholar 

  59. Leventaki V, Flerlage J. Sarcoid-like granulomatosis in a patient receiving anti-TNFα for psoriasis. Am J Hematol. 2018;93:722–3.

    Article  PubMed  Google Scholar 

  60. Sim JK, Lee SY, Shim JJ, Kang KH, et al. Pulmonary sarcoidosis induced by adalimumab: a case report and literature review. Yonsei Med J. 2016;57:272–3.

    Article  CAS  PubMed  Google Scholar 

  61. Gîlcă GE, Diaconescu S, Bălan GG, Timofte O, Ştefănescu G, et al. Sarcoidosis associated with infliximab therapy in ulcerative colitis: a case report. Medicine (Baltimore). 2017;96:6156.

    Article  Google Scholar 

  62. Wladis EJ, Tarasen AJ, Roth ZJ, et al. Orbital sarcoid-like granulomatosis after inhibition of tumor necrosis factor-α. Ophthalmic Plast Reconstr Surg. 2016;32:e30–2.

    Article  PubMed  Google Scholar 

  63. Turkowski Y, Konnikov N, Mahalingam M. Necrotizing granulomas in a patient with psoriasis and sarcoidosis after adalimumab-medication-induced reaction or reactivation of latent disease? Am J Dermatopathol. 2019;41:661–6.

    Article  PubMed  Google Scholar 

  64. Dragnev D, Barr D, Kulshrestha M, et al. Sarcoid panuveitis associated with etanercept treatment, resolving with adalimumab. BMJ Case Rep. 2013;2013:bcr2013200552.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Mao-Draayer Y, Cash T. Neurosarcoidosis in a patient treated with tumor necrosis factor alpha inhibitors. J Neurol. 2013;260:651–3.

    Article  PubMed  Google Scholar 

  66. Burns AM, Green PJ, Pasternak S. Etanercept-induced cutaneous and pulmonary sarcoid-like granulomas resolving with adalimumab. J Cutan Pathol. 2012;39:289–93.

    Article  PubMed  Google Scholar 

  67. Olivier A, Gilson B, Lafontaine S, et al. Pulmonary and renal involvement in a TNFα antagonist drug-induced sarcoidosis. Rev Med Interne. 2012;33:e25–7.

    Article  CAS  PubMed  Google Scholar 

  68. Ognenovski VM, Ojo TC, Fox DA. Etanercept-associated pulmonary granulomatous inflammation in patients with rheumatoid arthritis. J Rheumatol. 2008;35:2279–82.

    Article  PubMed  Google Scholar 

  69. Dubosc AE, Perroud A-M, Bagot M, et al. Cutaneous granulomas during infliximab therapy for spondyloarthropathy. J Rheumatol. 2008;35:1222–3.

    PubMed  Google Scholar 

  70. Phillips K, Weinblatt M. Granulomatous lung disease occurring during etanercept treatment. Arthritis Rheum. 2005;53:618–20.

    Article  PubMed  Google Scholar 

  71. Ando T, Kamiya K, Maekawa T, et al. Adalimumab as a successful alternative for the treatment of infliximab-induced sarcoidosis. J Dermatol. 2019;46:e360-362.

    Article  PubMed  Google Scholar 

  72. Berrios I, Jun-Oonnell A, Ghiran S, Ionete C, et al. A case of neurosarcoidosis secondary to treatment of etanercept and review of the literature. BMJ Case Rep. 2015;2015:bcr2014208188.

    Article  PubMed  PubMed Central  Google Scholar 

  73. Jung JH, Kim J-H, Song GG. Adalimumab-induced pulmonary sarcoidosis not progressing upon treatment with etanercept. Z Rheumatol. 2017;76:372–4.

    Article  CAS  PubMed  Google Scholar 

  74. Vigne C, Tebib J-G, Pacheco Y, et al. Sarcoidosis: an underestimated and potentially severe side effect of anti-TNF-alpha therapy. Joint Bone Spine. 2013;80:104–7.

    Article  PubMed  Google Scholar 

  75. Cleynen I, Vermeire S. Paradoxical inflammation induced by anti-TNF agents in patients with IBD. Nat Rev Gastroenterol Hepatol. 2012;9:496–503.

    Article  CAS  PubMed  Google Scholar 

  76. Jung SK, Lee KH, Jeon JW, et al. Physicochemical characterization of Remsima. MAbs. 2014;6:1163–77.

    Article  PubMed  PubMed Central  Google Scholar 

  77. Bargagli E, Mazzi A, Rottoli P. Markers of inflammation in sarcoidosis: blood, urine, BAL, sputum, and exhaled gas. Clin Chest Med. 2008;29:445–58.

    Article  CAS  PubMed  Google Scholar 

  78. Rigat B, Hubert C, Alhenc-Gelas F, et al. An insertion/deletion polymorphism in the angiotensin I-converting enzyme gene accounting for half the variance of serum enzyme levels. J Clin Invest. 1990;86:1343–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Biller H, Zissel G, Ruprecht B, et al. Genotype-corrected reference values for serum angiotensin-converting enzyme. Eur Respir J. 2006;28:1085–90.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

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Authors and Affiliations

  1. Division of Metabolism and Biosystemic Science, Gastroenterology, and Hematology/Oncology, Department of Medicine, Asahikawa Medical University, 2-1 Midorigaoka-higashi, Asahikawa, Hokkaido, 078-8510, Japan

    Shin Kashima, Kentaro Moriichi, Katsuyoshi Ando, Nobuhiro Ueno, Hiroki Tanabe & Mikihiro Fujiya

  2. Department of Diagnostic Pathology, Asahikawa Medical University Hospital, 2-1 Midorigaoka-higashi, Asahikawa, Hokkaido, 078-8510, Japan

    Sayaka Yuzawa

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  1. Shin Kashima
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  2. Kentaro Moriichi
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  4. Nobuhiro Ueno
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  7. Mikihiro Fujiya
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Contributions

SK and KM drafted the initial and final version of the manuscript and were involved in the care of this patient as gastroenterologists. KA and NU provided an intellectual review of the manuscript and were involved in the medical management of this patient as physicians in charge. HT were involved in the medical management of this patient as gastroenterologists and contributed to the intellectual review of the manuscript. SY were involved in the pathological evaluation and contributed to the intellectual review of the manuscript. MF contributed to the critical revision for important intellectual content. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Shin Kashima.

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Ethics approval and consent to participate

This is a case report, and we did not receive any approval from the ethics review board. We obtained the patient's written informed consent to publish the material.

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Written informed consent was obtained from the patient for the publication of this case report and accompanying images.

Competing interests

Dr. Fujiya reports grants and personal fees from Nippon Kayaku Co., Ltd., and Mitsubishi Tanabe Pharma Corporation as well as grants from AYUMI Pharmaceutical Corporation.

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Additional file 1

. To confirm the involvement of these causes and clarify the characteristics of patients likely to develop sarcoidosis under TNF inhibitor therapy, we searched for case reports in PubMed concerning sarcoidosis due to TNF inhibitor using the combination of the heading terms ‘infliximab’, ‘adalimumab’, ‘etanercept’, ‘certolizumab’, ‘golimumab’, ‘infliximab biosimilar’, without ‘Crohn’s disease’, combined with ‘sarcoidosis’.

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Kashima, S., Moriichi, K., Ando, K. et al. Development of pulmonary sarcoidosis in Crohn’s disease patient under infliximab biosimilar treatment after long-term original infliximab treatment: a case report and literature review. BMC Gastroenterol 21, 373 (2021). https://doi.org/10.1186/s12876-021-01948-6

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  • DOI: https://doi.org/10.1186/s12876-021-01948-6

Keywords

  • Crohn’s disease
  • Sarcoidosis
  • TNF-inhibitors
  • Original infliximab
  • Infliximab biosimilar

BMC Gastroenterology

ISSN: 1471-230X

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