Inflammatory bowel disease (IBD) is profoundly associated with extraintestinal manifestations (EIM) that can involve almost every organ in our body. Although the exact etiology of IBD is still poorly understood, it is generally characterized by an overly aggressive inflammatory response in the intestinal mucosa. Renal damage is one of the manifestations encountered in Crohn’s disease (CD) and ulcerative colitis (UC) and it accounts for 4% - 23% of IBD patients. The common renal complications of IBD include: glomerulonephritis, tubulointerstitial nephritis, nephrolithiasis, amyloidosis and iatrogenic complications of IBD treatment. Several hypotheses have emerged to explain the pathogenic mechanisms underlying the prevalence of IBD-induced kidney injuries. The present work aims to elucidate the pathological principles that drive secondary renal injury in individuals with IBD and highlight the currently used therapeutic strategies for evaluating, monitoring and treating kidney complications-related IBD.
References
[1]
Levine, J.S. and Burakoff, R. (2011). Extraintestinal Manifestations of Inflammatory Bowel Disease. Gastroenterology and Hepatology, 7, 235-241.
[2]
Bamias, G., Nyce, M.R., De La Rue, S.A., et al. (2005) New Concepts in the PATHOPHYSIOLogy of Inflammatory Bowel Disease. Annals of Internal Medicine, 143, 895-904. https://doi.org/10.7326/0003-4819-143-12-200512200-00007
[3]
Katsanos, K.H. and Tsianos, E.V. (2002) The Kidneys in Inflammatory Bowel Disease. Annals of Gastroenterology, 15, 41-52.
[4]
Corica, D. and Romano, C. (2016) Renal Involvement in Inflammatory Bowel Diseases. Journal of Crohn’s and Colitis, 10, 226-235.
https://doi.org/10.1093/ecco-jcc/jjv138
[5]
Prattis, S. and Jurjus, A. (2015) Spontaneous and Transgenic Rodent Models of Inflammatory Bowel Disease. Laboratory Animal Research, 31, 47-68.
https://doi.org/10.5625/lar.2015.31.2.47
[6]
Xu, X.-R., Liu, C.-Q., Feng, B.-S., et al. (2014) Dysregulation of Mucosal Immune Response in Pathogenesis of Inflammatory Bowel Disease. World Journal of Gastroenterology, 20, 3255-3264. https://doi.org/10.3748/wjg.v20.i12.3255
[7]
Fuss, I.J., Heller, F., Boirivant, M., et al. (2004) Non Classical CD1d-Restricted NK T Cells That Produce IL-13 Characterize an Atypical Th2 Response in Ulcerative Colitis. Journal of Clinical Investigation, 113, 1490-1497.
https://doi.org/10.1172/JCI19836
[8]
Gálvez, J. (2014) Role of Th17 Cells in the Pathogenesis of Human IBD. ISRN inflammation, 928461. https://doi.org/10.1155/2014/928461
[9]
Rivera-Nieves, J., Bamias, G., Vidrich, A., et al. (2003) Emergence of Perianal Fistulizing Disease in the SAMP1/YitFc Mouse, a Spontaneous Model of Chronic Ileitis. Gastroenterology, 124, 972-982. https://doi.org/10.1053/gast.2003.50148
[10]
McGeachy, M.J., Bak-Jensen, K.S., Chen, Y., et al. (2007) TGF-Beta and IL-6 Drive the Production of IL-17 and IL-10 by T Cells and Restrain T(H)-17 Cell-Mediated Pathology. Nature Immunology, 8, 1390-1397. https://doi.org/10.1038/ni1539
[11]
Bettelli, E., Oukka, M. and Kuchroo, V.K. (2007) T(H)-17 Cells in the Circle of Immunity and Autoimmunity. Nature Immunology, 8, 345-350.
https://doi.org/10.1038/ni0407-345
[12]
Veny, M., Esteller, M., Ricart, E., et al. (2010) Late Crohn’s Disease Patients Present an Increase in Peripheral Th17 Cells and Cytokine Production Compared with Early Patients. Alimentary Pharmacology & Therapeutics, 31, 561-572.
https://doi.org/10.1111/j.1365-2036.2009.04209.x
[13]
Omenetti, S. and Pizarro, T.T. (2015) The Treg/Th17 Axis: A Dynamic Balance Regulated by the Gut Microbiome. Frontiers in Immunology, 6, 639.
https://doi.org/10.3389/fimmu.2015.00639
[14]
Ogura, Y., Bonen, D.K., Inohara, N., et al. (2001) A Frameshift Mutation in NOD2 Associated with Susceptibility to Crohn’s Disease. Nature, 411, 603-606.
https://doi.org/10.1038/35079114
[15]
Al Nabhani, Z., Dietrich, G., Hugot, J.P., et al. (2017) Nod2: The Intestinal Gate Keeper. PLOS Pathogens, 13, e1006177.
https://doi.org/10.1371/journal.ppat.1006177
[16]
Jurjus, A.R., Khoury, N.N. and Reimund, J.M. (2004) Animal Models of Inflammatory Bowel Disease. Journal of Pharmacological and Toxicological Methods, 50, 81-92.
[17]
Franke, A., Balschun, T., Karlsen, T.H., et al. (2008) Sequence Variants in IL10, ARPC2 and Multiple Other Loci Contribute to Ulcerative Colitis Susceptibility. Nature Genetics, 40, 1319-1323.
[18]
M?zes, G., Molnár, B., Tulassay, Z., et al. (2012) Changes of the Cytokine Profile in Inflammatory Bowel Diseases. World Journal of Gastroenterology, 18, 5848-5861.
[19]
Boirivant, M., Pallone, F., Di Giacinto, C., et al. (2006) Inhibition of Smad7 with a Specific Antisense Oligonucleotide Facilitates TGF-beta1-Mediated Suppression of Colitis. Gastroenterology, 131, 1786-1798.
[20]
Marek, A., Brodzicki, J., Liberek, A., et al. (2002) TGF-Beta (Transforming Growth Factor-Beta) in Chronic Inflammatory Conditions—A New Diagnostic and Prognostic Marker? Medical Science Monitor, 8, RA145-RA151.
[21]
Kallel, L., Nijaa, N., Fatma, L.B., Rais, L., et al. (2009) Familial Cases of Glomerulonephritis Complicating Crohn’s Disease. Journal of Crohn’s and Colitis, 3, 125-127.
[22]
Ko?ak, E., K?klü, S., Akbal, E., Huddam, B., et al. (2010) Development of Glomerulonephritis Early in the Course of Crohn’s Disease. Inflammatory Bowel Diseases, 16, 548-549. https://doi.org/10.1002/ibd.21044
[23]
Ambruzs, J.M., Walker, P.D. and Larsen, C.P. (2014) The Histopathologic Spectrum of Kidney Biopsies in Patients with Inflammatory Bowel Disease. Clinical Journal of the American Society of Nephrology, 9, 265-270.
https://doi.org/10.2215/CJN.04660513
[24]
Choi, J.Y., Yu, C.H., Jung, H.Y., Jung, M.K., et al. (2012) A Case of Rapidly Progressive IgA Nephropathy in a Patient with Exacerbation of Crohn’s Disease. BMC Nephrology, 13, 84.
[25]
Terasaka, T., Uchida, H.A., Umebayashi, R., Tsukamoto, K., Tanaka, K., Kitagawa, M., et al. (2016) The Possible Involvement of Intestine-Derived IgA1: A Case of IgA Nephropathy Associated with Crohn’s Disease. BMC Nephrology, 17, 122.
[26]
Wang, J., Anders, R.A., Wang, Y., et al. (2005) The Critical Role of LIGHT in Promoting Intestinal Inflammation and Crohn’s Disease. The Journal of Immunology, 174, 8173-8182.
[27]
Wang, J., Anders, R.A., Wu, Q., et al. (2004) Dysregulated LIGHT Expression on T Cells Mediates Intestinal Inflammation and Contributes to IgA Nephropathy. Journal of Clinical Investigation, 113, 826-835.
[28]
Kiryluk, K., Li, Y., Scolari, F., Sanna-Cherchi, S. and Choi, M. (2014) Discovery of New Risk Loci for IgA Nephropathy Implicates Genes Involved in Immunity against Intestinal Pathogens. Nature Genetics, 46, 1187-1196.
[29]
Onime, A., Agaba, E.I., Sun, Y., Parsons, R.B., et al. (2006) Immunoglobulin A Nephropathy Complicating Ulcerative Colitis. International Urology and Nephrology, 38, 349-353. https://doi.org/10.1007/s11255-006-0061-y
[30]
Takemura, T., Okada, M., Yagi, K., Kuwajima, H. and Yanagida, H. (2002) An Adolescent with IgA Nephropathy and Crohn Disease: Pathogenetic Implications. Pediatric Nephrology, 17, 863-866.
[31]
Pozzi, C., Andrulli, S., Del Vecchio, L., Melis, P., et al. (2004) Corticosteroid Effectiveness in IgA Nephropathy: Long-Term Results of a Randomized, Controlled Trial. Journal of the American Society of Nephrology, 15, 157-163.
[32]
Khosroshahi, H.T. and Shoja, M.M. (2006) Tubulointerstitial Disease and Ulcerative Colitis. Nephrology Dialysis Transplantation, 21, 2340.
[33]
Tokuyama, H., Wakino, S., Konishi, K., Hashiguchi, A., et al. (2010) Acute Interstitial Nephritis Associated with Ulcerative Colitis. Clinical and Experimental Nephrology, 14, 483-486. https://doi.org/10.1007/s10157-010-0294-z
[34]
Tadic, M., Grgurevic, I., Scukanec-Spoljar, M., et al. (2005) Acute Interstitial Nephritis due to Mesalazine. Nephrology, 10, 103-105.
[35]
Sato, H., Umemura, K., Yamamoto, T. and Sato, H. (2017) Interstitial Nephritis Associated with Ulcerative Colitis in Monozygotic Twins. BMJ Case Reports.
https://doi.org/10.1136/bcr-2016-218346
[36]
Stanton, B., Caza, T., Huang, D. and Beg, M.B. (2017) Tubulointerstitial Nephritis as the Initial Presentation of Crohn’s Disease and Successful Treatment with Infliximab. ACG Case Reports Journal, 4, e24.
[37]
Herrlinger, K.R., Noftz, M.K., Fellermann, K., et al. (2002) Minimal Renal Dysfunction in Inflammatory Bowel Disease Is Related to Disease Activity But Not to 5-ASA Use. Alimentary Pharmacology & Therapeutics, 15, 363-369.
https://doi.org/10.1046/j.1365-2036.2001.00940.x
Heidt, J., Ooms, E.C., van der Werf, S.D. and Groeneveld, J.H. (2010) Tubulo-Interstitial Nephritis in Inflammatory Bowel Disease: Extra-Intestinal Manifestation or Drug Toxicity? Nederlands Tijdschrift Voor Geneeskunde, 154, A1647.
[40]
Fraser, J.S., Muller, A.F., Smith, D.J., Newman, D.J. and Lamb, E.J. (2001) Renal Tubular Injury Is Present in Acute Inflammatory Bowel Disease Prior to the Introduction of Drug Therapy. Alimentary Pharmacology & Therapeutics, 15, 1131-1137.
[41]
Kreisel, W., Wolf, L.M., Grotz, W. and Grieshaber, M. (1996) Renal Tubular Damage: An Extraintestinal Manifestation of Chronic Inflammatory Bowel Disease. European Journal of Gastroenterology & Hepatology, 8, 461-468.
[42]
Poulou, A.C., Goumas, K.E., Dandakis, D.C., Tyrmpas, I., et al. (2006) Microproteinuria in Patients with Inflammatory Bowel Disease: Is It Associated with the Diseaseactivity or the Treatment with 5-Aminosalicylic Acid? World Journal of Gastroenterology, 12, 739-746. https://doi.org/10.3748/wjg.v12.i5.739
[43]
Henry, C.B. and Duling, B.R. (2000) TNF-Alpha Increases Entry of Macromolecules into Luminal Endothelial Cell Glycocalyx. American Journal of Physiology-Heart and Circulatory Physiology, 279, H2815-H2823.
[44]
Mathy, N.L., Scheuer, W., Lanzend?rfer, M., et al. (2000) Interleukin-16 Stimulates the Expression and Production of Pro-Inflammatory Cytokines by Human Monocytes. Immunology, 100, 63-69.
[45]
Ranganathan, P., Jayakumar, C., Santhakumar, M., et al. (2013) Netrin-1 Regulates Colon-Kidney Cross Talk through Suppression of IL-6 Function in a Mouse Model of DSS-Colitis. American Journal of Physiology-Renal Physiology, 304, F1187-F1197.
[46]
Cury, D.B., Moss, A.C. and Schor, N. (2013) Nephrolithiasis in Patients with Inflammatory Bowel Disease in the Community. International Journal of Nephrology and Renovascular Disease, 6, 139-142.
[47]
Fagagnini, S., Heinrich, H., Rossel, J.B., Biedermann, L., et al. (2017) Risk Factors for Gallstones and Kidney Stones in a Cohort of Patients with Inflammatory Bowel Diseases. PLoS ONE, 12, e0185193.
[48]
Mukewar, S., Hall, P., Lashner, B.A., Lopez, R., et al. (2013) Risk Factors for Nephrolithiasis in Patients with Ileal Pouches. Journal of Crohn’s and Colitis, 7, 70-78.
[49]
Ganji-Arjenaki, M., Nasri, H. and Rafieian-Kopaei, M. (2017) Nephrolithiasis as a Common Urinary System Manifestation of Inflammatory Bowel Diseases; A Clinical Review and Meta-Analysis. Journal of Nephropathology, 6, 264-269.
https://doi.org/10.15171/jnp.2017.42
[50]
Nazzal, L., Puri, S. and Goldfarb, D.S. (2016) Enteric Hyperoxaluria: An Important Cause of End-Stage Kidney Disease. Nephrology Dialysis Transplantation, 3, 375-382. https://doi.org/10.1093/ndt/gfv005
[51]
Caudarella, R., Rizzoli, E., Pironi, L., et al. (1993) Renal Stone Formation in Patients with Inflammatory Bowel Disease. Scanning Microscopy, 7, 371-379.
[52]
Evan, A.P., Lingeman, J.E., Worcester, E.M., Bledsoe, S.B., et al. (2010) Renal Histopathology and Crystal Deposits in Patients with Small Bowel Resection and Calcium Oxalate Stone Disease. Kidney International, 78, 310-317.
[53]
Jonassen, J.A., Kohjimoto, Y., Scheid, C.R., et al. (2005) Oxalate Toxicity in Renal Cells. Urological Research, 33, 329-339. https://doi.org/10.1007/s00240-005-0485-3
[54]
Knauf, F., Asplin, J.R., Granja, I., Schmidt, I.M., et al. (2013) NALP3-Mediated Inflammation Isa Principal Cause of Progressive Renal Failure in Oxalate Nephropathy. Kidney International, 84, 895-901. https://doi.org/10.1038/ki.2013.207
[55]
Rodgers, A.L., Allie-Hamdulay, S., Jackson, G.E. and Sutton, R.A. (2014) Enteric Hyperoxaluria Secondary to Small Bowel Resection: Use of Computer Simulation to Characterize Urinary Risk Factors for Stone Formation and Assess Potential Treatment Protocols. Journal of Endourology, 28, 985-994.
[56]
Gkentzis, A., Kimuli, M., Cartledge, J., Traxer, O. and Biyani, C.S. (2016) Urolithiasis in Inflammatory Bowel Disease and Bariatric Surgery. World Journal of Nephrology, 5, 538-546.
[57]
Guardiola-Arévalo, A., Alcántara-Torres, M., Valle-Mu?oz, J., et al. (2011) Amyloidosis and Crohn’s Disease. Revista Espanola De Enfermedades Digestivas, 103, 268-274. https://doi.org/10.4321/S1130-01082011000500009
[58]
Cabezuelo, J.B., Egea, J.P., Ramos, F., et al. (2012) Infliximab in the Treatment of Amyloidosis Secondary to Crohn’s Disease. Nefrologia, 32, 385-388.
[59]
Powell-Tuck, J. (1986) Protein Metabolism in Inflammatory Bowel Disease. Gut, 27, 67-71. https://doi.org/10.1136/gut.27.Suppl_1.67
[60]
Dinarello, C.A., Simon, A. and van der Meer, J. (2012) Treating Inflammation by Blocking Interleukin-1 in a Broad Spectrum of Diseases. Nature Reviews Drug Discovery, 11, 633-652. https://doi.org/10.1038/nrd3800
[61]
Topaloglu, R., Batu, E.D., Orhan, D., Ozen, S. and Besbas, N. (2015) Anti-Interleukin 1 Treatment in Secondary Renal Amyloidosis Associated with Autoinflammatory Diseases. Pediatric Rheumatology Online Journal, 13, 149.
https://doi.org/10.1186/1546-0096-13-S1-P149
[62]
Azad Khan, A.K., Piris, J. and Truelove, S.C. (1977) An Experiment to Determine the Active Therapeutic Moiety of Sulphasalazine. The Lancet, 2, 892-895.
https://doi.org/10.1016/S0140-6736(77)90831-5
[63]
Rousseaux, C., Lefebvre, B., Dubuquoy, L., Lefebvre, P., et al. (2005) Intestinal Antiinflammatory Effect of 5-Aminosalicylic Acid Is Dependent on Peroxisome Proliferator-Activated Receptor-Gamma. The Journal of Experimental Medicine, 201, 1205-1215. https://doi.org/10.1084/jem.20041948
[64]
Iacucci, M., de Silva, S. and Ghosh, S. (2010) Mesalazine in Inflammatory Bowel Disease: A Trendy Topic Once Again? Canadian Journal of Gastroenterology, 24, 127-133. https://doi.org/10.1155/2010/586092
[65]
World, M.J., Stevens, P.E., Ashton, M.A. and Rainford, D.J. (1996) Mesalazine-Associated Interstitial Nephritis. Nephrology Dialysis Transplantation, 11, 614-621. https://doi.org/10.1093/oxfordjournals.ndt.a027349
[66]
Ransford, R.A. and Langman, M.J. (2002) Sulphasalazine and Mesalazine: Serious Adverse Reactions Re-Evaluated on the Basis of Suspected Adverse Reaction Reports to the Committee on Safety of Medicines. Gut, 51, 536-539.
https://doi.org/10.1136/gut.51.4.536
[67]
Muller, A.F., Stevens, P.E., McIntyre, A.S., Ellison, H. and Logan, R.F. (2005) Experience of 5-Aminosalicylate Nephrotoxicity in the United Kingdom. Alimentary Pharmacology & Therapeutics, 21, 1217-1224.
https://doi.org/10.1111/j.1365-2036.2005.02462.x
[68]
Schreiber, S., H?mling, J., Zehnter, E., Howaldt, S., Daerr, W., et al. (1997) Renal Tubular Dysfunction in Patients with Inflammatory Bowel Disease Treated with Aminosalicylate. Gut, 40, 761-766. https://doi.org/10.1136/gut.40.6.761
[69]
Corrigan, G. and Stevens, P.E. (2000) Review Article: Interstitial Nephritis Associated with the Use of Mesalazine in Inflammatory Bowel Disease. Alimentary Pharmacology & Therapeutics, 14, 1-6.
https://doi.org/10.1046/j.1365-2036.2000.00683.x
[70]
Cunliffe, R.N. and Scott, B.B. (2002) Review Article: Monitoring for Drug Side-Effects in Inflammatory Bowel Disease. Alimentary Pharmacology & Therapeutics, 16, 647-662. https://doi.org/10.1046/j.1365-2036.2002.01216.x
[71]
Verschueren, P., Lensen, F., Lerut, E., Claes, K., et al. (2003) Benefit of Anti-TNFalpha Treatment for Nephrotic Syndrome in a Patient with Juvenile Inflammatory Bowel Disease Associated Spondyloarthropathy Complicated with Amyloidosis and Glomerulonephritis. Annals of the Rheumatic Diseases, 62, 368-369.
https://doi.org/10.1136/ard.62.4.368
[72]
Sakellariou, G.T., Vounotrypidis, P. and Berberidis, C. (2007) Infliximab Treatment in Two Patients with Psoriatic Arthritis and Secondary IgA Nephropay. Clinical Rheumatology, 26, 1132-1133. https://doi.org/10.1007/s10067-006-0422-z
[73]
Sokumbi, O., Wetter, D.A., Makol, A. and Warrington, K.J. (2012) Vasculitis Associated with Tumor Necrosis Factor-α Inhibitors. Mayo Clinic Proceedings, 87, 739-745. https://doi.org/10.1016/j.mayocp.2012.04.011
[74]
Chin, G., Luxton, G. and Harvey, J.M. (2005) Infliximab and Nephrotic Syndrome. Nephrology Dialysis Transplantation, 20, 2824-2826.
https://doi.org/10.1093/ndt/gfi180
[75]
den Broeder, A.A., Assmann, K.J., van Riel, P.L. and Wetzels, J.F. (2003) Nephrotic Syndrome as a Complication of Anti-TNFalpha in a Patient with Rheumatoid Arthritis. The Netherlands Journal of Medicine, 61, 137-141.
[76]
Villemaire, M., Cartier, J.C., Mathieu, N., Maurizi, J., et al. (2014) Renal Sarcoid-Like Granulomatosis during Anti-TNF Therapy. Kidney International, 86, 215.
https://doi.org/10.1038/ki.2013.452
[77]
Yoo, Y.J., Chung, S.Y., Gu, D.H., Ko, G.J., et al. (2014) A Case of Late Onset-Acute Tubulointerstitial Nephritis with Infliximab and Mesalazine Treatment in a Patient with Crohn’s Disease. The Korean Journal of Gastroenterology, 63, 308-312.
https://doi.org/10.4166/kjg.2014.63.5.308
[78]
Dumitrescu, G., Dahan, K., Treton, X., Corcos, O., et al. (2015) Nephrotic Syndrome after Infliximab Treatment in a Patient with Ulcerative Colitis. Journal of Gastrointestinal and Liver Diseases, 24, 249-251.
[79]
Charles, P.J., Smeenk, R.J., De Jong, J., Feldmann, M. and Maini, R.N. (2000) Assessment of Antibodies to Double-Stranded DNA Induced in Rheumatoid Arthritis Patients Following Treatment with Infliximab, a Monoclonal Antibody to Tumor Necrosis Factor Alpha: Findings in Open-Label and Randomized Placebo-Controlled Trials. Arthritis & Rheumatology, 43, 2383-2390.
https://doi.org/10.1002/1529-0131(200011)43:11<2383::AID-ANR2>3.0.CO;2-D
[80]
Ziolkowska, M. and Maslinski, W. (2003) Laboratory Changes on Anti-Tumor Necrosis Factor Treatment in Rheumatoid Arthritis. Current Opinion in Rheumatology, 15, 267-273. https://doi.org/10.1097/00002281-200305000-00014
[81]
English, J., Evan, A., Houghton, D.C. and Bennett, W.M. (1987) Cyclosporine-Induced Acute Renal Dysfunction in the Rat. Evidence of Arteriolar Vasoconstriction with Preservation of Tubular Function. Transplantation, 44, 135-141.
https://doi.org/10.1097/00007890-198707000-00027
[82]
Kon, V., Sugiura, M., Inagami, T., Harvie, B.R., et al. (1990) Role of Endothelin in Cyclosporine-Induced Glomerular Dysfunction. Kidney International, 37, 1487-1491. https://doi.org/10.1038/ki.1990.139
[83]
Bobadilla, N.A. and Gamba, G. (2007) New Insights into the Pathophysiology of Cyclosporine Nephrotoxicity: A Role of Aldosterone. American Journal of Physiology-Renal Physiology, 293, F2-F9. https://doi.org/10.1152/ajprenal.00072.2007
[84]
Snanoudj, R., Royal, V., Elie, C., Rabant, M., et al. (2011) Specificity of Histological Markers of Long-Term CNI Nephrotoxicity in Kidney-Transplant Recipients under Low-Dose Cyclosporine Therapy. American Journal of Transplantation, 11, 2635-2646. https://doi.org/10.1111/j.1600-6143.2011.03718.x
[85]
Shang, M.H., Yuan, W.J., Zhang, S.J., Fan, Y. and Zhang, Z. (2008) Intrarenal Activation of Renin Angiotensin System in the Development of Cyclosporine a Induced Chronic Nephrotoxicity. Chinese Medical Journal, 121, 983-988.
[86]
Sereno, J., Rodrigues-Santos, P., Vala, H., Rocha-Pereira, P., Alves, R., et al. (2014) Transition from Cyclosporine-Induced Renal Dysfunction to Nephrotoxicity in an in Vivo Rat Model. International Journal of Molecular Sciences, 15, 8979-8997.
https://doi.org/10.3390/ijms15058979
[87]
Sandborn, W.J. (1995) Cyclosporine Therapy for Inflammatory Bowel Disease: Definitive Answers and Remaining Questions. Gastroenterology, 109, 1001-1003.
https://doi.org/10.1016/0016-5085(95)90413-1
[88]
Feagan, B.G., McDonald, J.W., Rochon, J., Laupacis, A., et al. (1994) Low-Dose Cyclosporine for the Treatment of Crohn’s Disease. The Canadian Crohn’s Relapse Prevention Trial Investigators. The New England Journal of Medicine, 330, 1846-1851. https://doi.org/10.1056/NEJM199406303302602
[89]
Sandborn, W.J., Tremaine, W.J. and Lawson, G.M. (1996) Clinical Response Does Not Correlate with Intestinal or Blood Cyclosporine Concentrations in Patients with Crohn’s Disease Treated with High-Dose Oral Cyclosporine. The American Journal of Gastroenterology, 91, 37-43.
[90]
Oikonomou, K.A., Kapsoritakis, A.N., Stefanidis, I. and Potamianos, S.P. (2011) Drug-Induced Nephrotoxicity in Inflammatory Bowel Disease. Nephron Clinical Practice, 119, c89-c94. https://doi.org/10.1159/000326682
[91]
Ogata, H., Matsui, T., Nakamura, M., Iida, M., et al. (2006) A Randomised Dose Finding Study of Oral Tacrolimus (FK506) Therapy in Refractory Ulcerative Colitis. Gut, 55, 1255-1262. https://doi.org/10.1136/gut.2005.081794
[92]
Wingard, J.R., Nash, R.A., Przepiorka, D., Klein, J.L., et al. (1998) Relationship of Tacrolimus (FK506) Whole Blood Concentrations and Efficacy and Safety after HLA-Identical Sibling Bone Marrow Transplantation. Biology of Blood and Marrow Transplantation, 4, 157-163. https://doi.org/10.1016/S1083-8791(98)50005-5
[93]
Sandborn, W.J., Present, D.H., Isaacs, K.L., Wolf, D.C., et al. (2003) Tacrolimus for the Treatment of Fistulas in Patients with Crohn’s Disease: A Randomized, Placebo-Controlled Trial. Gastroenterology, 125, 380-388.
https://doi.org/10.1016/S0016-5085(03)00877-1
[94]
Hosoi, K., Arai, K., Matsuoka, K., Shimizu, H., et al. (2017) Prolonged Tacrolimus for Pediatric Gastrointestinal Disorder: Double-Edged Sword? Pediatrics International, 59, 588-592. https://doi.org/10.1111/ped.13211
[95]
Asada, A., Bamba, S., Morita, Y., Takahashi, K., et al. (2017) The Effect of CYP3A5 Genetic Polymorphisms on Adverse Events in Patients with Ulcerative Colitis Treated with Tacrolimus. Digestive and Liver Disease, 49, 24-28.
https://doi.org/10.1016/j.dld.2016.09.008
[96]
Meissner, Y., Pellequer, Y. and Lamprecht, A. (2006) Nanoparticles in Inflammatory Bowel Disease: Particle Targeting versus pH-Sensitive Delivery. International Journal of Pharmaceutics, 316, 138-143.
https://doi.org/10.1016/j.ijpharm.2006.01.032
[97]
Lamprecht, A., Yamamoto, H., Ubrich, N., Takeuchi, H., et al. (2005) FK506 Microparticles Mitigate Experimental Colitis with Minor Renal Calcineurin Suppression. Pharmaceutical Research, 22, 193-199.
https://doi.org/10.1007/s11095-004-1186-2
