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Wan S, Chen H, Liu S, Fan Z, Fan J. Infliximab may contribute to remit rapidly progressive of IgA nephropathy secondary to Crohn's disease: A case report. Technol Health Care 2025:9287329251340770. [PMID: 40371441 DOI: 10.1177/09287329251340770] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Indexed: 05/16/2025]
Abstract
BackgroundIgA nephropathy (IgAN) is a glomerulonephritis characterized by IgA deposition in the mesangial of the glomerulus, and it is the most common glomerulonephritis. However, many patients with inflammatory bowel disease (IBD) also have secondary IgAN. Compared with primary IgAN, the secondary IgAN may be more complex. Many novel therapies, such as anti-TNFα therapy, have been shown to influence IgAN while controlling IBD.Case presentationA 52-year-old woman had been treated with infliximab and azathioprine for Crohn's disease, and taking entecavir for hepatitis B. Recently, the patient developed gross hematuria, acute renal insufficiency, and positive blood anti-GBM antibody after the exacerbation of Crohn's disease. Renal biopsies were performed after infliximab dosage was increased. Although the patient presented clinically as rapidly progressive glomerulonephritis, renal biopsy revealed IgAN with acute tubulointerstitial injury and crescent formation. Subsequently, the patient experienced spontaneous remission with decrease in both hematuria and creatinine. We then gave the patient a routine dose of methylprednisolone, and her condition remained stable during follow-up.ConclusionIn our case, IgAN may expose antigen by causing local inflammatory response to GBM, induce anti-GBM antibody production, and cause acute renal insufficiency in the patient. However, anti-TNF-α therapy may promote the remission of hematuria and renal insufficiency by inhibiting the inflammatory response in renal tissues. Therefore, more studies are needed to understand the specific role of anti-TNFα therapy in IgAN.
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Affiliation(s)
- Songyan Wan
- Department of Nephrology, The First Affiliated Hospital of Zhejiang Chinese Medical University (Zhejiang Provincial Hospital of Chinese Medicine), Hangzhou, China
| | - Han Chen
- Department of Nephrology, The First Affiliated Hospital of Zhejiang Chinese Medical University (Zhejiang Provincial Hospital of Chinese Medicine), Hangzhou, China
| | - Siqi Liu
- Department of Nephrology, The First Affiliated Hospital of Zhejiang Chinese Medical University (Zhejiang Provincial Hospital of Chinese Medicine), Hangzhou, China
| | - Zhenliang Fan
- Department of Nephrology, The First Affiliated Hospital of Zhejiang Chinese Medical University (Zhejiang Provincial Hospital of Chinese Medicine), Hangzhou, China
| | - Junfen Fan
- Department of Nephrology, The First Affiliated Hospital of Zhejiang Chinese Medical University (Zhejiang Provincial Hospital of Chinese Medicine), Hangzhou, China
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Lee IWZ, Baikunje S, Tan PH, Guo W. Case report: Crescentic IgA nephropathy with anti-neutrophil cytoplasmic antibodies, in a patient on golimumab. Int J Rheum Dis 2024; 27:e15330. [PMID: 39239851 DOI: 10.1111/1756-185x.15330] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [MESH Headings] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 06/13/2024] [Revised: 08/17/2024] [Accepted: 08/25/2024] [Indexed: 09/07/2024]
Affiliation(s)
- Ivan Wei Zhen Lee
- Department of Renal Medicine, Sengkang General Hospital, Singapore, Singapore
| | - Shashidhar Baikunje
- Department of Renal Medicine, Sengkang General Hospital, Singapore, Singapore
| | | | - Weiwen Guo
- Department of Renal Medicine, Sengkang General Hospital, Singapore, Singapore
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Baptista A, Macedo AM, Marreiros A, Coelho A, Perazella MA. Drug-Related Glomerular Phenotypes: A Global Pharmacovigilance Perspective. J Clin Med 2024; 13:4869. [PMID: 39201010 PMCID: PMC11355908 DOI: 10.3390/jcm13164869] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/26/2024] [Revised: 08/14/2024] [Accepted: 08/16/2024] [Indexed: 09/02/2024] Open
Abstract
Introduction: Adverse drug reactions are a significant problem in modern society, stemming from the increase in prescribed medications, over-the-counter drugs, and overall polypharmacy. Glomerular disorders are one of the frequently reported renal conditions associated with medication use. VigiBase is a significant tool for evaluating events associated with drug use, and, to the authors' knowledge, no study has yet assessed this database to identify the primary medications associated with glomerular disorders. Materials and Methods: We collected data from VigiBase for 54 years and evaluated data based on global frequencies, disproportionality (IC025 values), nephrotoxic potential, and physiopathological mechanisms. Results: Over the evaluation period, 33.932.051 spontaneous notifications of adverse drug reactions reported in VigiBase were assessed, from which 106.775 notifications of drug-associated glomerular disorders were extracted. The isolated medications were classified as 'potential nephrotoxins' (47.0%), with 40% of the medications lacking scientific references to report any association with the development of glomerular disorders. Among the evaluated medications, Inotersen (IC025 of 8.3), Penicillamine (IC025 6.8), Bevacizumab (IC025 5.9) and Lenvatinib (IC025 5.4) were identified as having the strongest association with these glomerular disorders. For medications classified as 'non-nephrotoxic', a high disproportionality index was observed, suggesting drugs that might be considered as new potential nephrotoxins. Conclusions: Drug-induced glomerular disorders were significantly associated with medications that had no established nephrotoxic role but demonstrated a high disproportionality index in VigiBase. These newly alleged nephrotoxic drugs warrant further evaluation in dedicated studies to assess their true nephrotoxic potential.
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Affiliation(s)
- Alexandre Baptista
- School of Medicine and Biomedical Sciences, Algarve University (UAlg), 8005-139 Faro, Portugal; (A.M.M.); (A.M.)
- Algarve Biomedical Centre (ABC), 8005-139 Faro, Portugal
| | - Ana M. Macedo
- School of Medicine and Biomedical Sciences, Algarve University (UAlg), 8005-139 Faro, Portugal; (A.M.M.); (A.M.)
- Algarve Biomedical Centre (ABC), 8005-139 Faro, Portugal
| | - Ana Marreiros
- School of Medicine and Biomedical Sciences, Algarve University (UAlg), 8005-139 Faro, Portugal; (A.M.M.); (A.M.)
- Algarve Biomedical Centre (ABC), 8005-139 Faro, Portugal
| | - André Coelho
- Health & Technology Research Center, Escola Superior de Tecnologia da Saúde de Lisboa, Instituto Politécnico de Lisboa, 1990-096 Lisboa, Portugal;
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Shimizu A, Tsuboi N, Haruhara K, Shirai I, Ogawa K, Miura A, Oshiro K, Ueda H, Yokote S, Okabe M, Sasaki T, Ikeda M, Yokoo T. Active flare of IgA nephropathy during long-term therapy with anti-tumor necrosis factor-α antibody drugs for Crohn's disease: three case reports and literature review. CEN Case Rep 2024; 13:249-257. [PMID: 38032436 PMCID: PMC11294508 DOI: 10.1007/s13730-023-00836-0] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/25/2023] [Accepted: 10/30/2023] [Indexed: 12/01/2023] Open
Abstract
In recent years, increasing numbers of reports have described new onset or active disease flare of IgA nephropathy (IgAN) during administration of TNF-α inhibitor (TNFi) therapy for chronic inflammatory diseases. Crohn's disease (CD) is the most common indication for TNFi therapy in this clinical setting, but the underlying etiology of IgAN in such patients remains unclear. We report our experience with three patients who developed acute worsening of preexisting urinalysis abnormalities and kidney dysfunction approximately 2 to 6 years after TNFi administration for CD. Kidney biopsies at the time of kidney disease flare revealed IgAN in two patients and IgAN complicated by acute tubulointerstitial nephritis in one patient. The CD and IgAN in all three patients were successfully managed with additional corticosteroid therapy and tonsillectomy without discontinuing TNFi therapy. The clinical course of our patients and similar patients described in the literature suggests that TNFi therapy for CD is associated with a relatively high risk for new onset or disease flare of IgAN. This report discusses the possible involvement of Th1/Th2 imbalance on the immunological background of CD or IgAN.
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Affiliation(s)
- Akihiro Shimizu
- Division of Nephrology and Hypertension, Department of Internal Medicine, The Jikei University Kashiwa Hospital, 163-1, Kashiwashita, Kashiwa-shi, Chiba, 277-8567, Japan.
| | - Nobuo Tsuboi
- Division of Nephrology and Hypertension, Department of Internal Medicine, The Jikei University School of Medicine, Tokyo, Japan
| | - Kotaro Haruhara
- Division of Nephrology and Hypertension, Department of Internal Medicine, The Jikei University Kashiwa Hospital, 163-1, Kashiwashita, Kashiwa-shi, Chiba, 277-8567, Japan
| | - Izumi Shirai
- Division of Nephrology and Hypertension, Department of Internal Medicine, The Jikei University Kashiwa Hospital, 163-1, Kashiwashita, Kashiwa-shi, Chiba, 277-8567, Japan
| | - Kyohei Ogawa
- Division of Nephrology and Hypertension, Department of Internal Medicine, The Jikei University Kashiwa Hospital, 163-1, Kashiwashita, Kashiwa-shi, Chiba, 277-8567, Japan
| | - Akane Miura
- Division of Nephrology and Hypertension, Department of Internal Medicine, The Jikei University Kashiwa Hospital, 163-1, Kashiwashita, Kashiwa-shi, Chiba, 277-8567, Japan
| | - Kentaro Oshiro
- Division of Nephrology and Hypertension, Department of Internal Medicine, The Jikei University Kashiwa Hospital, 163-1, Kashiwashita, Kashiwa-shi, Chiba, 277-8567, Japan
| | - Hiroyuki Ueda
- Division of Nephrology and Hypertension, Department of Internal Medicine, The Jikei University School of Medicine, Tokyo, Japan
| | - Shinya Yokote
- Division of Nephrology, Kawaguchi Municipal Medical Center, Kawaguchi, Japan
| | - Masahiro Okabe
- Division of Nephrology and Hypertension, Department of Internal Medicine, The Jikei University Daisan Hospital, Tokyo, Japan
| | - Takaya Sasaki
- Division of Nephrology, Kawaguchi Municipal Medical Center, Kawaguchi, Japan
| | - Masato Ikeda
- Division of Nephrology and Hypertension, Department of Internal Medicine, The Jikei University Kashiwa Hospital, 163-1, Kashiwashita, Kashiwa-shi, Chiba, 277-8567, Japan
| | - Takashi Yokoo
- Division of Nephrology and Hypertension, Department of Internal Medicine, The Jikei University School of Medicine, Tokyo, Japan
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Larson C, Munir N, Rao P, Farkash E, Kathuria P, Romain D, Berinstein J. Crohn's Disease Associated With IgA Nephropathy Effectively Treated With the Interleukin-23 Inhibitor Risankizumab. ACG Case Rep J 2024; 11:e01437. [PMID: 39021716 PMCID: PMC11254109 DOI: 10.14309/crj.0000000000001437] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 01/08/2024] [Accepted: 06/14/2024] [Indexed: 07/20/2024] Open
Abstract
Extraintestinal manifestations (EIMs) are common in inflammatory bowel disease (IBD). Renal EIMs, including immunoglobulin A nephropathy (IgAN), are relatively rare. EIMs are important to consider when developing a treatment plan for IBD. Studies differ on whether IBD disease activity correlates with IgAN disease activity. Published guidance on effective therapies for IBD-associated IgAN is limited. This case report suggests that risankizumab, an effective therapy for Crohn's disease, may also be effective in treating Crohn's disease-associated IgAN.
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Affiliation(s)
- Charlotte Larson
- Department of Internal Medicine, University of Michigan, Ann Arbor, MI
| | | | - Panduranga Rao
- Department of Nephrology, University of Michigan, Ann Arbor, MI
| | - Evan Farkash
- Department of Pathology, University of Michigan, Ann Arbor, MI
| | - Priya Kathuria
- Department of Internal Medicine, University of Michigan, Ann Arbor, MI
| | - Dustin Romain
- Department of Internal Medicine, University of Michigan, Ann Arbor, MI
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Tamura H. IgA nephropathy associated with Crohn's disease. World J Methodol 2023; 13:67-78. [PMID: 37456980 PMCID: PMC10348078 DOI: 10.5662/wjm.v13.i3.67] [Citation(s) in RCA: 2] [Impact Index Per Article: 1.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 03/24/2023] [Revised: 04/16/2023] [Accepted: 05/12/2023] [Indexed: 06/20/2023] Open
Abstract
The relationship between IgA nephropathy (IgAN) and Crohn’s disease was reported. IgAN is the most common primary glomerulonephritis and one of the leading causes of chronic kidney disease and end-stage renal failure, and up to 50% of cases progressed to end-stage renal disease within 25 years after IgAN diagnosis. However, specific and effective therapeutic strategies are still lacking. In this review, we discuss the possibility of the mechanism involved in IgAN associated with Crohn’s disease based on the findings of basic and clinical studies. Although the etiology of IgAN associated with Crohn’s disease is not permanent and various factors are thought to be involved, the stabilization of the disease condition of Crohn’s disease is believed to help treat IgAN.
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Affiliation(s)
- Hiroshi Tamura
- Department of Pediatrics, Kumamoto University, Kumamoto 8608556, Japan
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Doumas SA, Tsironis C, Bolaji AA, Garantziotis P, Frangou E. Glomerulonephritis and inflammatory bowel disease: A tale of gut-kidney axis dysfunction. Autoimmun Rev 2023; 22:103327. [PMID: 36990134 DOI: 10.1016/j.autrev.2023.103327] [Citation(s) in RCA: 3] [Impact Index Per Article: 1.5] [Reference Citation Analysis] [Abstract] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/08/2023] [Accepted: 03/22/2023] [Indexed: 03/30/2023]
Abstract
The incidence and prevalence of Inflammatory Bowel Disease (IBD) has increased over the past decades, imposing a growing socioeconomic burden on healthcare systems globally. Most of the morbidity and mortality related to IBD is typically attributed to gut inflammation and its complications; yet the disease is characterized by various extraintestinal manifestations that can be severe. Glomerulonephritis (GN) is of particular interest since a significant proportion of patients evolve into end-stage kidney disease, requiring kidney replacement therapy and associated with high morbidity and mortality. Herein, we review the GN landscape in IBD and define the clinical and pathogenic associations reported to date in the literature. Underlying pathogenic mechanisms suggest either the initiation of antigen-specific immune responses in the inflamed gut that cross react with non-intestinal sites, such as the glomerulus, or that extraintestinal manifestations are gut-independent events that occur due to an interaction between common genetic and environmental risk factors. We present data associating GN with IBD either as a bona fide extraintestinal manifestation or reporting it as an extraneous co-existing entity, involving various histological subtypes, such as focal segmental glomerulosclerosis, proliferative GN, minimal change disease, crescentic GN, but most emphatically IgA nephropathy. Supporting the pathogenic interplay between gut inflammation and intrinsic glomerular processes, enteric targeting the intestinal mucosa with budesonide reduced IgA nephropathy-mediated proteinuria. Elucidating the mechanisms at play would provide insight not only into IBD pathogenesis but also into the gut's role in the development of extraintestinal diseases, such as glomerular diseases.
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Uedono H, Tsuda A, Ueno N, Natsuki Y, Nakaya R, Nishide K, Machiba Y, Fujimoto K, Nakatani S, Mori K, Emoto M. Seronegative Full-house Nephropathy with Crohn's Disease. Intern Med 2022; 61:3553-3558. [PMID: 35527024 PMCID: PMC9790786 DOI: 10.2169/internalmedicine.8820-21] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 01/07/2023] Open
Abstract
Systemic lupus erythematosus (SLE) is a chronic autoimmune inflammatory disease. Lupus nephritis (LN) is a major risk factor for mortality in SLE, and glomerular "full-house" immunofluorescence staining is a well-known characteristic of LN. However, some cases of non-lupus glomerulonephritis can also present with a "full-house" immunofluorescence pattern. We recently encountered a patient with full-house nephropathy (FHN) during adalimumab administration for Crohn's disease. IgA nephropathy or idiopathic FHN was diagnosed, and treatment with steroids was started, after which there was improvement in proteinuria. The prognosis of FHN has been reported to be poor; therefore, aggressive treatment is required for such patients.
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Affiliation(s)
- Hideki Uedono
- Department of Metabolism, Endocrinology and Molecular Medicine, Osaka City University Graduate School of Medicine, Japan
| | - Akihiro Tsuda
- Department of Metabolism, Endocrinology and Molecular Medicine, Osaka City University Graduate School of Medicine, Japan
| | - Noriko Ueno
- Department of Metabolism, Endocrinology and Molecular Medicine, Osaka City University Graduate School of Medicine, Japan
| | - Yuka Natsuki
- Department of Metabolism, Endocrinology and Molecular Medicine, Osaka City University Graduate School of Medicine, Japan
| | - Rino Nakaya
- Department of Metabolism, Endocrinology and Molecular Medicine, Osaka City University Graduate School of Medicine, Japan
| | - Kozo Nishide
- Department of Metabolism, Endocrinology and Molecular Medicine, Osaka City University Graduate School of Medicine, Japan
| | - Yuri Machiba
- Department of Metabolism, Endocrinology and Molecular Medicine, Osaka City University Graduate School of Medicine, Japan
| | - Kenta Fujimoto
- Department of Metabolism, Endocrinology and Molecular Medicine, Osaka City University Graduate School of Medicine, Japan
| | - Shinya Nakatani
- Department of Metabolism, Endocrinology and Molecular Medicine, Osaka City University Graduate School of Medicine, Japan
| | - Katsuhito Mori
- Department of Nephrology Medicine, Osaka City University Graduate School of Medicine, Japan
| | - Masanori Emoto
- Department of Metabolism, Endocrinology and Molecular Medicine, Osaka City University Graduate School of Medicine, Japan
- Department of Nephrology Medicine, Osaka City University Graduate School of Medicine, Japan
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Yuan Q, Tang B, Zhang C. Signaling pathways of chronic kidney diseases, implications for therapeutics. Signal Transduct Target Ther 2022; 7:182. [PMID: 35680856 PMCID: PMC9184651 DOI: 10.1038/s41392-022-01036-5] [Citation(s) in RCA: 181] [Impact Index Per Article: 60.3] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/24/2022] [Revised: 05/20/2022] [Accepted: 05/24/2022] [Indexed: 12/11/2022] Open
Abstract
Chronic kidney disease (CKD) is a chronic renal dysfunction syndrome that is characterized by nephron loss, inflammation, myofibroblasts activation, and extracellular matrix (ECM) deposition. Lipotoxicity and oxidative stress are the driving force for the loss of nephron including tubules, glomerulus, and endothelium. NLRP3 inflammasome signaling, MAPK signaling, PI3K/Akt signaling, and RAAS signaling involves in lipotoxicity. The upregulated Nox expression and the decreased Nrf2 expression result in oxidative stress directly. The injured renal resident cells release proinflammatory cytokines and chemokines to recruit immune cells such as macrophages from bone marrow. NF-κB signaling, NLRP3 inflammasome signaling, JAK-STAT signaling, Toll-like receptor signaling, and cGAS-STING signaling are major signaling pathways that mediate inflammation in inflammatory cells including immune cells and injured renal resident cells. The inflammatory cells produce and secret a great number of profibrotic cytokines such as TGF-β1, Wnt ligands, and angiotensin II. TGF-β signaling, Wnt signaling, RAAS signaling, and Notch signaling evoke the activation of myofibroblasts and promote the generation of ECM. The potential therapies targeted to these signaling pathways are also introduced here. In this review, we update the key signaling pathways of lipotoxicity, oxidative stress, inflammation, and myofibroblasts activation in kidneys with chronic injury, and the targeted drugs based on the latest studies. Unifying these pathways and the targeted therapies will be instrumental to advance further basic and clinical investigation in CKD.
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Affiliation(s)
- Qian Yuan
- Department of Nephrology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China
| | - Ben Tang
- Department of Nephrology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China
| | - Chun Zhang
- Department of Nephrology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, 430022, China.
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Guillo L, Delanaye P, Flamant M, Figueres L, Karam S, Lemoine S, Benezech A, Pelletier AL, Amiot A, Caron B, Stefanescu C, Boschetti G, Bouguen G, Rahier JF, Gornet JM, Hugot JP, Bonnet J, Vuitton L, Nachury M, Vidon M, Uzzan M, Serrero M, Dib N, Seksik P, Hebuterne X, Bertocchio JP, Mariat C, Peyrin-Biroulet L. Kidney function monitoring in inflammatory bowel disease: The MONITORED consensus. Dig Liver Dis 2022; 54:309-315. [PMID: 34866011 DOI: 10.1016/j.dld.2021.11.008] [Citation(s) in RCA: 19] [Impact Index Per Article: 6.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/06/2021] [Revised: 11/09/2021] [Accepted: 11/10/2021] [Indexed: 12/11/2022]
Abstract
BACKGROUND AND AIMS Patients with inflammatory bowel diseases (IBD) are exposed to drug-related nephrotoxicity and kidney-related extra-intestinal manifestations (EIMs). Patients should be monitored but guidance is lacking in current international recommendations. The objective of the Kidney Function Monitoring in Inflammatory Bowel Disease (MONITORED) initiative was to achieve an expert consensus about monitoring kidney function in IBD. METHODS A literature review was first conducted. Then, an expert consensus meeting, involving 28 attendees representing French-speaking gastroenterologists and nephrologists, was held as part of an academic initiative on May 28, 2021. An anonymous Delphi process was used to discuss and vote on statements. Agreement was defined as at least 75% of participants voting for any one statement. RESULTS Experts reached consensus on 11 criteria for referral to the nephrologist. Concerning kidney function monitoring, participants unanimously validated the use of serum creatinine with estimation of the glomerular filtration rate via the MDRD or CKD-EPI equations. A blood ionogram and a urine sample with measurement of a protein-to-creatinine ratio were also broadly agreed validated. Experts recommended performing this monitoring at IBD diagnosis, prior introducing a new treatment, and annually for EIMs screening and evaluation of treatment tolerance. An evaluation 3 months after starting mesalamine and then every 6 months was felt necessary, while for biologics an annually monitoring was deemed sufficient. CONCLUSION The MONITORED consensus proposed guidelines on how to monitor kidney function in IBD. These recommendations should be considered in clinical practice to preserve kidney function and ensure the best approach to our patients.
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Affiliation(s)
- Lucas Guillo
- Department of Gastroenterology, University Hospital of Marseille Nord, University of Aix-Marseille, Marseille, France.
| | - Pierre Delanaye
- Department of Nephrology-Dialysis-Transplantation, University of Liège (ULiege), CHU Sart Tilman, Liège, Belgium; Department of Nephrology-Dialysis-Apheresis, Hôpital Universitaire Carémeau, Nîmes, France
| | - Martin Flamant
- Physiologie-Explorations Fonctionnelles, FHU APOLLO, Assistance Publique Hôpitaux de Paris, Hôpital Bichat-Claude Bernard, Université de Paris, CRI, INSERM F-75018, Paris, France
| | - Lucile Figueres
- Université de Nantes, Institut de Transplantation Urologie Néphrologie (ITUN), CHU Nantes, Service de néphrologie-immunologie clinique, CHU de Nantes, France
| | - Sabine Karam
- Division of Nephrology and Hypertension, Saint-George Hospital University Medical Center, Beirut, Lebanon
| | - Sandrine Lemoine
- Service de Néphrologie, dialyse, hypertension et exploration fonctionnelle rénale, Hôpital Edouard Herriot, Lyon, France
| | - Alban Benezech
- Departement of Gastroenterology, Henri Duffaut Hospital, Avignon, France
| | | | - Aurélien Amiot
- Department of Gastroenterology, Groupe Hospitalier Henri Mondor-Albert Chennevier, APHP, EC2M3-EA7375, University of Paris Est Créteil, Créteil, France
| | - Bénédicte Caron
- Department of Gastroenterology and Inserm NGERE U1256, University Hospital of Nancy, University of Lorraine, Vandoeuvre-lès-Nancy, France
| | - Carmen Stefanescu
- Department of Gastroenterology, IBD unit, Beaujon Hospital, APHP, Clichy, France
| | - Gilles Boschetti
- Department of Gastroenterology, Hospices Civils de Lyon, Lyon-Sud Hospital, Pierre Bénite, and INSERM U1111 - CIRI, Lyon, France
| | - Guillaume Bouguen
- Department of Gastroenterology, Centre Hospitalier Universitaire Pontchaillou, Rennes, France
| | | | - Jean-Marc Gornet
- Department of Gastroenterology, Saint-Louis Hospital, APHP, Paris, France
| | - Jean-Pierre Hugot
- Department of Pediatric Gastroenterology, Hôpital Universitaire Robert Debré, Assistance Publique Hôpitaux de Paris, Université de Paris, Paris, France
| | - Joëlle Bonnet
- Department of Gastroenterology, Saint-Louis Hospital, APHP, Paris, France
| | - Lucine Vuitton
- Department of Gastroenterology, Besancon University Hospital, Besancon, France
| | - Maria Nachury
- Univ, Lille, Inserm, CHU Lille, U1286 - INFINITE - Institute for Translational Research in Inflammation, F-59000 Lille, France
| | - Mathias Vidon
- Department of gastroenterology, CHI Créteil, Créteil, France
| | - Mathieu Uzzan
- Department of Gastroenterology, IBD unit, Beaujon Hospital, APHP, Clichy, France
| | - Mélanie Serrero
- Department of Gastroenterology, University Hospital of Marseille Nord, University of Aix-Marseille, Marseille, France
| | - Nina Dib
- Hepato-Gastroenterology Department, Angers University Hospital, Angers, France; HIFIH Laboratory, UPRES 3859, SFR 4208, Angers University, Angers, France
| | - Philippe Seksik
- Department of Gastroenterology, Centre de recherche Saint-Antoine, Sorbonne Université, APHP, Hôpital Saint-Antoine, Paris, France
| | - Xavier Hebuterne
- Gastroenterology and Clinical Nutrition, CHU of Nice, University Côte d'Azur, Nice, France
| | - Jean-Philippe Bertocchio
- Nephrology Department, Pitié-Salpêtrière Hospital, Assistance Publique-Hôpitaux de Paris, Paris, France
| | - Christophe Mariat
- Service de Néphrologie, Dialyse, Transplantation Rénale, Hôpital Nord, CHU de Saint-Etienne, EA 3065, Université Jean MONNET, Saint-Etienne, France
| | - Laurent Peyrin-Biroulet
- Department of Gastroenterology and Inserm NGERE U1256, University Hospital of Nancy, University of Lorraine, Vandoeuvre-lès-Nancy, France
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Tofacitinib combined with leflunomide for treatment of psoriatic arthritis with IgA nephropathy: a case report with literature review. Clin Rheumatol 2022; 41:2225-2231. [PMID: 35192086 DOI: 10.1007/s10067-022-06113-2] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/29/2021] [Revised: 02/16/2022] [Accepted: 02/17/2022] [Indexed: 11/03/2022]
Abstract
Psoriasis is a systemic inflammatory disease that is associated with increased risk of several diseases, such as psoriatic arthritis (PsA), inflammatory bowel disease, and cardiovascular diseases. About 20 to 30% patients with psoriasis subsequently develop PsA. IgA nephropathy is the most common primary glomerular disease world-wide. Psoriasis and IgA nephropathy appear to be associated, but the mechanism underlying this connection is unclear. Tofacitinib and leflunomide are common treatments for psoriatic arthritis. We administered tofacitinib combined with leflunomide to a 38-year-old female patient who presented with PsA and IgA nephropathy. After treatment, she experienced significant reductions in the psoriatic lesions, pain in the right knee joint, and proteinuria. Administration of tofacitinib combined with leflunomide for treatment of a patient who had PsA complicated with IgA nephropathy led to significant resolution of the symptoms of both conditions. These results suggest similarities in the pathogenesis of PsA and IgA nephropathy and a possible new treatment for IgA nephropathy.
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Graziano F, Busè M, Cassata N, Lentini VL, Citrano M. IgA nephropathy in a child: Crohn's disease-associated or adalimumab induced? Curr Med Res Opin 2022; 38:139-143. [PMID: 34866503 DOI: 10.1080/03007995.2021.2015155] [Citation(s) in RCA: 4] [Impact Index Per Article: 1.3] [Reference Citation Analysis] [Abstract] [Key Words] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Indexed: 01/06/2023]
Abstract
In pediatric patients with Inflammatory Bowel Disease renal parenchymal disease is infrequent. There are only two reports about the association between IgA Nephropathy and Pediatric Crohn Disease. IgA Nephropathy is a rather uncommon complication of Tumor Necrosis Factor-alpha (TNF-α) inhibition. We describe a case of IgA Nephropathy which has arisen in a 11-year-old child 2 years after Crohn disease diagnosis, during therapy with anti-TNF-α. An ileal e jejunal Crohn disease was diagnosed at 9 years old, initially treated with prednisone, followed by biological therapy with anti-TNF-α (Adalimumab) due to severe disease activity, with gradual improvement of clinical conditions until clinical remission is achieved. Two years after the diagnosis, the child suddenly presented macroscopic hematuria. Subsequent laboratory examinations showed acute renal failure. So kidney biopsy was performed and IgA Nephropathy diagnosis was made. Adalimumab was discontinued and the child has been treated with steroids for sixth months associated with angiotensin-converting enzyme inhibitor resulted in clinical improvement over the following year and remission was maintained. To our knowledge the association of IgA Nephropathy and pediatric IBD during therapy with anti-TNF-α has never been reported. Careful monitoring of renal function, proteinuria, and autoantibodies is advised in patients treated with anti-TNF-α agents.
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Affiliation(s)
| | - Martina Busè
- UOSD Medical Genetics, Villa Sofia Cervello Hospital, Palermo, Italy
| | - Nicola Cassata
- Pediatric Unit, Villa Sofia Cervello Hospital, Palermo, Italy
| | | | - Michele Citrano
- Pediatric Unit, Villa Sofia Cervello Hospital, Palermo, Italy
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13
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Mertelj T, Smrekar N, Kojc N, Lindič J, Kovač D. IgA Nephropathy in a Patient Treated with Adalimumab. Case Rep Nephrol Dial 2021; 11:233-240. [PMID: 34595210 PMCID: PMC8436610 DOI: 10.1159/000515585] [Citation(s) in RCA: 3] [Impact Index Per Article: 0.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/22/2020] [Accepted: 03/02/2021] [Indexed: 12/16/2022] Open
Abstract
Immunoglobulin A (IgA) nephropathy (IgAN) is the most common glomerulonephritis worldwide, characterized by IgA deposits in the glomerular mesangium. It has a progressive nature and can eventually lead to end-stage kidney failure. It can occur as a potential side effect of treatment with tumor necrosis factor alpha antagonist that has been used for numerous chronic inflammatory conditions, such as Crohn's disease. In this study, the case of a 33-year-old man with renal dysfunction, nephrotic proteinuria, and erythrocyturia is described. He had had a history of Crohn's disease for 8 years and had been treated with adalimumab for the past 7 years. The diagnosis of IgAN was confirmed by kidney biopsy. After discontinuance of adalimumab and the induction of corticosteroid therapy, he made a remarkable recovery. Four years after the first presentation of IgAN and discontinuation of adalimumab, his renal function was normal with no proteinuria and only mild erythrocyturia.
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Affiliation(s)
- Tonja Mertelj
- Department of Internal Medicine, University Medical Centre Ljubljana, University of Ljubljana, Ljubljana, Slovenia
| | - Nataša Smrekar
- Department of Gastroenterology, University Medical Centre Ljubljana, University of Ljubljana, Ljubljana, Slovenia
| | - Nika Kojc
- Institute of Pathology, Medical Faculty, University of Ljubljana, Ljubljana, Slovenia
| | - Jelka Lindič
- Department of Nephrology, University Medical Centre Ljubljana, University of Ljubljana, Ljubljana, Slovenia
| | - Damjan Kovač
- Department of Nephrology, University Medical Centre Ljubljana, University of Ljubljana, Ljubljana, Slovenia
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14
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Petreski T, Piko N, Ekart R, Hojs R, Bevc S. Review on Inflammation Markers in Chronic Kidney Disease. Biomedicines 2021; 9:182. [PMID: 33670423 PMCID: PMC7917900 DOI: 10.3390/biomedicines9020182] [Citation(s) in RCA: 41] [Impact Index Per Article: 10.3] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 01/12/2021] [Revised: 02/04/2021] [Accepted: 02/09/2021] [Indexed: 02/07/2023] Open
Abstract
Chronic kidney disease (CKD) is one of the major health problems of the modern age. It represents an important public health challenge with an ever-lasting rising prevalence, which reached almost 700 million by the year 2017. Therefore, it is very important to identify patients at risk for CKD development and discover risk factors that cause the progression of the disease. Several studies have tackled this conundrum in recent years, novel markers have been identified, and new insights into the pathogenesis of CKD have been gained. This review summarizes the evidence on markers of inflammation and their role in the development and progression of CKD. It will focus primarily on cytokines, chemokines, and cell adhesion molecules. Nevertheless, further large, multicenter studies are needed to establish the role of these markers and confirm possible treatment options in everyday clinical practice.
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Affiliation(s)
- Tadej Petreski
- Department of Nephrology, Clinic for Internal Medicine, University Medical Centre Maribor, Ljubljanska Ulica 5, 2000 Maribor, Slovenia; (T.P.); (N.P.); (R.H.)
- Department of Internal Medicine and Department of Pharmacology, Faculty of Medicine, University of Maribor, Taborska Ulica 8, 2000 Maribor, Slovenia
| | - Nejc Piko
- Department of Nephrology, Clinic for Internal Medicine, University Medical Centre Maribor, Ljubljanska Ulica 5, 2000 Maribor, Slovenia; (T.P.); (N.P.); (R.H.)
- Department of Dialysis, Clinic for Internal Medicine, University Medical Centre Maribor, Ljubljanska Ulica 5, 2000 Maribor, Slovenia;
| | - Robert Ekart
- Department of Internal Medicine and Department of Pharmacology, Faculty of Medicine, University of Maribor, Taborska Ulica 8, 2000 Maribor, Slovenia
- Department of Dialysis, Clinic for Internal Medicine, University Medical Centre Maribor, Ljubljanska Ulica 5, 2000 Maribor, Slovenia;
| | - Radovan Hojs
- Department of Nephrology, Clinic for Internal Medicine, University Medical Centre Maribor, Ljubljanska Ulica 5, 2000 Maribor, Slovenia; (T.P.); (N.P.); (R.H.)
- Department of Internal Medicine and Department of Pharmacology, Faculty of Medicine, University of Maribor, Taborska Ulica 8, 2000 Maribor, Slovenia
| | - Sebastjan Bevc
- Department of Nephrology, Clinic for Internal Medicine, University Medical Centre Maribor, Ljubljanska Ulica 5, 2000 Maribor, Slovenia; (T.P.); (N.P.); (R.H.)
- Department of Internal Medicine and Department of Pharmacology, Faculty of Medicine, University of Maribor, Taborska Ulica 8, 2000 Maribor, Slovenia
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15
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Joher N, Gosset C, Guerrot D, Pillebout E, Hummel A, Boffa JJ, Faguer S, Rabant M, Higgins S, Moktefi A, Delmas Y, Karras A, Lapidus N, Amiot A, Audard V, El Karoui K. IgA nephropathy in association with inflammatory bowel diseases: results from a national study and systematic literature review. Nephrol Dial Transplant 2021; 37:531-539. [PMID: 33416845 DOI: 10.1093/ndt/gfaa378] [Citation(s) in RCA: 23] [Impact Index Per Article: 5.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 07/20/2020] [Indexed: 01/24/2023] Open
Abstract
BACKGROUND Little is known about clinical characteristics and kidney outcome in patients with biopsy-proven immunoglobulin A nephropathy (IgAN) in a context of inflammatory bowel disease (IBD). METHODS We conducted a retrospective multicenter study with centralized histological review, to analyze the presentation, therapeutic management and outcome of 24 patients suffering from IBD associated IgAN relative to a cohort of 134 patients with primary IgAN without IBD. RESULTS Crohn's disease and ulcerative colitis accounted for 75% and 25% of IBD-associated IgAN cases, respectively. IBD was diagnosed before IgAN in 23 cases (a mean of 9 years previously) and was considered active at IgAN onset in 23.6% of patients. Hypertension was present in 41.7% of patients. Urinary protein-to-creatinine ratio exceeded 100 mg/mmol in 70.8% of patients (mean: 254 mg/mmol). Estimated glomerular filtration rate (eGFR) exceeded 60 ml/min/1.73m2 in 13/24 patients and only one patient required dialysis. In the Oxford MEST-C classification of renal biopsies, 57% were M1, 48% E1, 76% S1, 57% T1+T2 and 38% C1+C2. Steroids were administered in 50% of cases. After a mean follow-up of 7.2 years, four patients (16.7%) had a poor kidney outcome: end-stage renal disease (n = 3) or a > 50% decrease in eGFR from initial values (n = 1). A similar evolution was observed in patients with primitive IgAN. CONCLUSIONS This first case series suggests that IBD-associated IgAN have frequent inflammatory lesions at onset and variable long-term outcome.
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Affiliation(s)
- Nizar Joher
- Département de Néphrologie et Transplantation, Centre de Référence Maladie Rare « Syndrome Néphrotique Idiopathique », Hôpital Universitaire Henri Mondor, Assistance Publique-Hôpitaux de Paris AP-HP, Créteil, France.,Université Paris Est Créteil UPEC, Institut National de la Santé et de la Recherche Médicale INSERM U955, Institut Mondor de Recherche Biomédicale IMRB, Equipe 21, Créteil, France
| | - Clément Gosset
- Département de Pathologie, Hôpital Saint Louis, Assistance Publique-Hôpitaux de Paris AP-HP, Paris, France
| | - Dominique Guerrot
- Département de Néphrologie, Hôpital Universitaire de Rouen, Rouen, France
| | - Evangeline Pillebout
- Département de Néphrologie, Hôpital Saint Louis, Assistance Publique-Hôpitaux de Paris, Paris, France
| | - Aurélie Hummel
- Département de Néphrologie, Hôpital Necker, Assistance Publique-Hôpitaux de Paris, Paris, France
| | - Jean-Jacques Boffa
- Département de Néphrologie, Hôpital Tenon, Assistance Publique-Hôpitaux de Paris, Paris, France
| | - Stanislas Faguer
- Département de Néphrologie, Hôpital Rangueil, Centre Hospitalo-Universitaire de Toulouse, Toulouse, France
| | - Marion Rabant
- Département de Pathologie, Hôpital Necker, Assistance Publique-Hôpitaux de Paris, Paris, France
| | - Sarah Higgins
- Département de Pathologie, Hôpital Necker, Assistance Publique-Hôpitaux de Paris, Paris, France
| | - Anissa Moktefi
- Département de Pathologie, Hôpital Henri Mondor, Assistance Publique-Hôpitaux de Paris, Créteil, France
| | - Yahsou Delmas
- Département de Néphrologie, Hôpital Universitaire de Bordeaux, Bordeaux, France
| | - Alexandre Karras
- Département de Néphrologie, Hôpital Européen Georges Pompidou, Paris, France
| | - Nathanaël Lapidus
- Département de Santé Publique, Hôpital Saint Antoine, Assistance Publique-Hôpitaux de Paris, Paris, France.,Institut Pierre Louis d'Epidémiologie et de Santé Publique IPLESP, INSERM, Sorbonne Université, F75012, Paris, France
| | - Aurélien Amiot
- Département de Gastro-Entérologie, Hôpital Henri Mondor, Assistance Publique-Hôpitaux de Paris, Créteil, France
| | - Vincent Audard
- Département de Néphrologie et Transplantation, Centre de Référence Maladie Rare « Syndrome Néphrotique Idiopathique », Hôpital Universitaire Henri Mondor, Assistance Publique-Hôpitaux de Paris AP-HP, Créteil, France.,Université Paris Est Créteil UPEC, Institut National de la Santé et de la Recherche Médicale INSERM U955, Institut Mondor de Recherche Biomédicale IMRB, Equipe 21, Créteil, France
| | - Khalil El Karoui
- Département de Néphrologie et Transplantation, Centre de Référence Maladie Rare « Syndrome Néphrotique Idiopathique », Hôpital Universitaire Henri Mondor, Assistance Publique-Hôpitaux de Paris AP-HP, Créteil, France.,Université Paris Est Créteil UPEC, Institut National de la Santé et de la Recherche Médicale INSERM U955, Institut Mondor de Recherche Biomédicale IMRB, Equipe 21, Créteil, France
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16
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IgA Nephropathy in the Setting of Anti-TNF-α Therapy for Inflammatory Bowel Disease. ACG Case Rep J 2020; 7:e00462. [PMID: 33062795 PMCID: PMC7526714 DOI: 10.14309/crj.0000000000000462] [Citation(s) in RCA: 8] [Impact Index Per Article: 1.6] [Reference Citation Analysis] [Abstract] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/13/2020] [Accepted: 07/10/2020] [Indexed: 01/19/2023] Open
Abstract
Tumor necrosis factor-α (TNF-α)-inhibiting agents are a standard therapy for moderate-to-severe inflammatory bowel disease (IBD). IgA nephropathy in the setting of prolonged exposure to TNF-α inhibitors is a rare, clinically significant adverse event often overlooked by gastroenterologists but well documented in the rheumatologic literature. We present a case series of 3 patients with IBD on TNF-α inhibitors who developed biopsy-proven IgA nephropathy. Clinicians prescribing TNF-α inhibitors to patients with IBD need to be aware of this potential side effect. Therapies with alternative mechanisms of action should instead be considered.
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17
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Champtiaux N, Lioté F, El Karoui K, Vigneau C, Miceli C, Cornec-Le Gall E, Rémy P, Choukroun G, Fakhouri F, Garrouste C, Veillon L, Pillebout E, Lobbedez T, Vuiblet V, Wynckel A, Guincestre T, Toussirot E, Thervet E, Rabant M, Karras A. Spondyloarthritis-Associated IgA Nephropathy. Kidney Int Rep 2020; 5:813-820. [PMID: 32518863 PMCID: PMC7271945 DOI: 10.1016/j.ekir.2020.03.012] [Citation(s) in RCA: 14] [Impact Index Per Article: 2.8] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Figures] [Journal Information] [Subscribe] [Scholar Register] [Received: 09/28/2019] [Revised: 02/20/2020] [Accepted: 02/25/2020] [Indexed: 12/27/2022] Open
Abstract
Introduction IgA nephropathy (IgAN) can be associated with spondyloarthritis (SpA). The course of SpA-associated IgAN remains largely unknown due to the absence of large cohorts. Methods This retrospective study included patients with biopsy-proven IgAN and definite SpA. Kidney biopsies were centrally examined and scored according to the IgAN Oxford Classification. Thirty-two patients fulfilled the inclusion criteria, with a male:female ratio of 9:1 and median age of 27 and 37 years at SpA and IgAN diagnosis, respectively. HLA-B27 was positive in 90% of cases, and most patients (60%) presented with ankylosing spondylitis. The mean baseline estimated glomerular filtration rate (eGFR) was 84 ± 26 ml/min per 1.73 m2, and the urine protein-to-creatinine ratio was 0.19 g/mmol. Results Renal biopsy revealed frequent presence of crescents (33%) and interstitial inflammation (18%). Despite almost constant use of renin-angiotensin system inhibitors, combined with steroids in 13 of 32 patients, renal outcome was particularly poor. After a median follow-up of 5.9 years, 4 patients (12.5%) reached end-stage renal disease and 41% of patients experienced a >50% decrease of eGFR. The mean annual eGFR decline rate was -4.3 ± 6.7 ml/min per 1.73 m2. The risk of reaching class IV or V chronic kidney disease (CKD) stage during follow-up was associated with the presence of hypertension, level of proteinuria, and baseline S- and T-scores of the Oxford. Conclusion SpA-associated IgAN is associated with a poor renal outcome, despite frequent use of steroids. Tumor necrosis factor (TNF)-α blockade did not appear to influence the rate of eGFR decline in this setting.
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Affiliation(s)
- Nicolas Champtiaux
- Department of Internal Medicine, Hôpital de la Pitié-Salpétrière, Assistance Pulique-Hopitaux de Paris, Paris, France.,Department of Nephrology, Hôpital Européen Georges-Pompidou, Assistance Publique-Hopitaux de Paris, Paris, France
| | - Frédéric Lioté
- Department of Rheumatology, Inserm UMR 1132, Centre Viggo Petersen, Hôpital Lariboisière, Assistance Publique-Hopitaux de Paris, Paris, France.,Paris Diderot University, Sorbonne Paris Cité, Paris, France
| | - Khalil El Karoui
- Department of Nephrology, Hôpital Necker, Assistance Pubique-Hopitaux de Paris, Paris, France
| | | | - Corinne Miceli
- Department of Rheumatology, Hôpital Bicêtre, Assistance Publique-Hopitaux de Paris, Le Kremlin Bicêtre, France
| | | | - Philippe Rémy
- Department of Nephrology, Hôpital Henri Mondor, Assistance Publique-Hopitaux de Paris, Créteil, France
| | - Gabriel Choukroun
- Department of Nephrology, Dialysis and Transplantation, CHU Amiens, Amiens, France.,UMR 1088 INSERM, University of Picardie Jules Verne, Amiens, France
| | - Fadi Fakhouri
- Department of Nephrology, CHU de Nantes, Nantes, France
| | - Cyril Garrouste
- Department of Nephrology, CHU de Clermont Ferrand, Clermont-Ferrand, France
| | - Laurent Veillon
- Department of Rheumatology, Hôpital Bicêtre, Assistance Publique-Hopitaux de Paris, Le Kremlin Bicêtre, France
| | - Evangeline Pillebout
- Department of Nephrology, Hôpital Saint Louis, Assistance Publique-Hopitaux de Paris, Paris, France
| | | | | | - Alain Wynckel
- Department of Nephrology, CHU de Reims, Reims, France
| | - Thomas Guincestre
- Department of Nephrology, Centre Hospitalier de Roubaix, Roubaix, France
| | - Eric Toussirot
- INSERM CIC-1431 Centre Investigation Clinique Biothérapie, Department of Rheumatology, CHRU de Besançon, Besançon, France
| | - Eric Thervet
- Department of Nephrology, Hôpital Européen Georges-Pompidou, Assistance Publique-Hopitaux de Paris, Paris, France.,Université de Paris, Paris, France
| | - Marion Rabant
- Department of Pathology, Hôpital Necker, Assistance Pubique-Hopitaux de Paris, Paris, France
| | - Alexandre Karras
- Department of Nephrology, Hôpital Européen Georges-Pompidou, Assistance Publique-Hopitaux de Paris, Paris, France.,Université de Paris, Paris, France
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