Impact of Obesity on the Course of Management of Inflammatory Bowel Disease—A Review
Abstract
:1. Introduction
2. IBD and Its Metabolic Background—A Relationship Not to Be Neglected
3. Adipose Tissue as an Endocrine Organ Involved in Metabolic and Inflammatory Pathologies
4. Apelin—Epithelium and Lymphatic Vessels in the Scope of IBD
5. Leptin and Its Pleiotropic Function
6. Adiponectin in the Setting of Metabolic and Inflammatory Disorders
7. Resistin—A Significant Marker of Systemic Inflammation
8. Chemerin—A Powerful Chemoattractant
9. Other Adipokines
10. IBD and Adipose Tissue—Take It or Leave It?
11. General Idea of Mesenteric Adipose Tissue
12. Adipose Tissue and IBD—Where Is the Exact Beginning?
13. Adipose Tissue-Related Implications in the Clinics of IBD
14. T Cells, Creeping Fat and Here the Story Goes
15. IBD, Adipose Tissue, and Pharmacological Treatment—Associations and Speculations
16. Biologics, Obesity, and IBD—What Do We Know?
17. Body Mass and Its Clinical Value in the Management of IBD Patients
18. IBD and Anti-Inflammatory Diets—Are There any Reliable Changes in Front of Us?
19. Novel Potential Options of Treatment in IBD Patients from the Perspective of Adipose Tissue
20. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Adolph, T.E.; Meyer, M.; Schwärzler, J.; Mayr, L.; Grabherr, F.; Tilg, H. The metabolic nature of inflammatory bowel diseases. Nat. Rev. Gastroenterol. Hepatol. 2022. Online ahead of print. [Google Scholar] [CrossRef] [PubMed]
- Chang, J.T. Pathophysiology of Inflammatory Bowel Diseases. N. Engl J. Med. 2020, 383, 2652–2664. [Google Scholar] [CrossRef] [PubMed]
- Uhlig, H.H.; Powrie, F. Translating Immunology into Therapeutic Concepts for Inflammatory Bowel Disease. Annu. Rev. Immunol. 2018, 36, 755–781. [Google Scholar] [CrossRef]
- Guan, Q. A Comprehensive Review and Update on the Pathogenesis of Inflammatory Bowel Disease. J. Immunol. Res. 2019, 2019, 7247238. [Google Scholar] [CrossRef] [PubMed]
- Losurdo, G.; La Fortezza, R.F.; Iannone, A.; Contaldo, A.; Barone, M.; Ierardi, E.; Di Leo, A.; Principi, M. Prevalence and associated factors of obesity in inflammatory bowel disease: A case-control study. World J. Gastroenterol. 2020, 26, 7528–7537. [Google Scholar] [CrossRef] [PubMed]
- Blain, A.; Cattan, S.; Beaugerie, L.; Carbonnel, F.; Gendre, J.P.; Cosnes, J. Crohn’s disease clinical course and severity in obese patients. Clin. Nutr. 2002, 21, 51–57. [Google Scholar] [CrossRef]
- Seminerio, J.L.; Koutroubakis, I.E.; Ramos-Rivers, C.; Hashash, J.G.; Dudekula, A.; Regueiro, M.; Baidoo, L.; Barrie, A.; Swoger, J.; Schwartz, M.; et al. Impact of Obesity on the Management and Clinical Course of Patients with Inflammatory Bowel Disease. Inflamm. Bowel Dis. 2015, 21, 2857–2863. [Google Scholar] [CrossRef]
- Steed, H.; Walsh, S.; Reynolds, N. A brief report of the epidemiology of obesity in the inflammatory bowel disease population of Tayside, Scotland. Obes. Facts 2009, 2, 370–372. [Google Scholar] [CrossRef]
- Bhagavathula, A.S.; Clark, C.C.T.; Rahmani, J.; Chattu, V.K. Impact of Body Mass Index on the Development of Inflammatory Bowel Disease: A Systematic Review and Dose-Response Analysis of 15.6 Million Participants. Healthcare 2021, 9, 35. [Google Scholar] [CrossRef]
- Chan, S.S.M.; Chen, Y.; Casey, K.; Olen, O.; Ludvigsson, J.F.; Carbonnel, F.; Oldenburg, B.; Gunter, M.J.; Tjønneland, A.; Grip, O.; et al. Obesity is Associated With Increased Risk of Crohn’s disease, but not Ulcerative Colitis: A Pooled Analysis of Five Prospective Cohort Studies. Clin. Gastroenterol. Hepatol. 2022, 20, 1048–1058. [Google Scholar] [CrossRef]
- Harper, J.W.; Zisman, T.L. Interaction of obesity and inflammatory bowel disease. World J. Gastroenterol. 2016, 22, 7868–7881. [Google Scholar] [CrossRef] [PubMed]
- Harpsøe, M.C.; Basit, S.; Andersson, M.; Nielsen, N.M.; Frisch, M.; Wohlfahrt, J.; Nohr, E.A.; Linneberg, A.; Jess, T. Body mass index and risk of autoimmune diseases: A study within the Danish National Birth Cohort. Int. J. Epidemiol. 2014, 43, 843–855. [Google Scholar] [CrossRef] [PubMed]
- Khalili, H.; Ananthakrishnan, A.N.; Konijeti, G.G.; Higuchi, L.M.; Fuchs, C.S.; Richter, J.M.; Chan, A.T. Measures of obesity and risk of Crohn’s disease and ulcerative colitis. Inflamm. Bowel Dis. 2015, 21, 361–368. [Google Scholar] [CrossRef] [PubMed]
- Yan, X.; Huang, Y.; Wang, H.; Du, M.; Hess, B.W.; Ford, S.P.; Nathanielsz, P.W.; Zhu, M.J. Maternal obesity induces sustained inflammation in both fetal and offspring large intestine of sheep. Inflamm. Bowel Dis. 2011, 17, 1513–1522. [Google Scholar] [CrossRef]
- Bibi, S.; Kang, Y.; Du, M.; Zhu, M.J. Maternal high-fat diet consumption enhances offspring susceptibility to DSS-induced colitis in mice. Obesity 2017, 25, 901–908. [Google Scholar] [CrossRef]
- Ng, S.C.; Shi, H.Y.; Hamidi, N.; Underwood, F.E.; Tang, W.; Benchimol, E.I.; Panaccione, R.; Ghosh, S.; Wu, J.C.Y.; Chan, F.K.L.; et al. Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: A systematic review of population-based studies. Lancet 2017, 390, 2769–2778, Erratum in Lancet 2020, 3, e56. [Google Scholar] [CrossRef]
- Stamatiou, D.; Naumann, D.N.; Foss, H.; Singhal, R.; Karandikar, S. Effects of ethnicity and socioeconomic status on surgical outcomes from inflammatory bowel disease. Int. J. Colorectal Dis. 2022, 37, 1367–1374. [Google Scholar] [CrossRef]
- Yang, S.K.; Loftus, E.V., Jr.; Sandborn, W.J. Epidemiology of inflammatory bowel disease in Asia. Inflamm. Bowel Dis. 2001, 7, 260–270. [Google Scholar] [CrossRef]
- Alghoul, Z.; Yang, C.; Merlin, D. The Current Status of Molecular Biomarkers for Inflammatory Bowel Disease. Biomedicines 2022, 10, 1492. [Google Scholar] [CrossRef]
- Liu, C.; Zhan, S.; Tian, Z.; Li, N.; Li, T.; Wu, D.; Zeng, Z.; Zhuang, X. Food Additives Associated with Gut Microbiota Alterations in Inflammatory Bowel Disease: Friends or Enemies? Nutrients 2022, 14, 3049. [Google Scholar] [CrossRef]
- Gubatan, J.; Boye, T.L.; Temby, M.; Sojwal, R.S.; Holman, D.R.; Sinha, S.R.; Rogalla, S.R.; Nielsen, O.H. Gut Microbiome in Inflammatory Bowel Disease: Role in Pathogenesis, Dietary Modulation, and Colitis-Associated Colon Cancer. Microorganisms 2022, 10, 1371. [Google Scholar] [CrossRef] [PubMed]
- Murtagh, A.; Cooney, L.; Higginbotham, C.; Heavey, P. Dietary practices, beliefs and behaviours of adults with inflammatory bowel disease: A cross-sectional study. Ir. J. Med. Sci. 2022. Online ahead of print. [Google Scholar] [CrossRef] [PubMed]
- Jiang, K.; Chen, B.; Lou, D.; Zhang, M.; Shi, Y.; Dai, W.; Shen, J.; Zhou, B.; Hu, J. Systematic review and meta-analysis: Association between obesity/overweight and surgical complications in IBD. Int. J. Colorectal Dis. 2022, 37, 1485–1496. [Google Scholar] [CrossRef] [PubMed]
- Chan, S.S.; Luben, R.; Olsen, A.; Tjonneland, A.; Kaaks, R.; Teucher, B.; Lindgren, S.; Grip, O.; Key, T.; Crowe, F.L.; et al. Body mass index and the risk for Crohn’s disease and ulcerative colitis: Data from a European Prospective Cohort Study (The IBD in EPIC Study). Am. J. Gastroenterol. 2013, 108, 575–582. [Google Scholar] [CrossRef] [PubMed]
- Gubatan, J.; Barber, G.E.; Nielsen, O.H.; Juhl, C.B.; Maxwell, C.; Eisenberg, M.L.; Streett, S.E. Paternal Medications in Inflammatory Bowel Disease and Male Fertility and Reproductive Outcomes: A Systematic Review and Meta-Analysis. Clin. Gastroenterol. Hepatol. 2022, S1542-3565(22)00675-9, Epub ahead of print. [Google Scholar] [CrossRef]
- Patel, A.; Krishna, S.G.; Patel, K.; Gray, D.M., 2nd; Mumtaz, K.; Stanich, P.P.; Hinton, A.; Hussan, H. Rising Rates of Severe Obesity in Adults Younger Than 50 Correspond to Rise in Hospitalizations for Non-malignant Gastrointestinal Disease. Dig. Dis. Sci. 2022. Epub ahead of print. [Google Scholar] [CrossRef]
- Tarar, Z.I.; Farooq, U.; Zafar, M.U.; Saleem, S.; Nawaz, A.; Kamal, F.; Ghous, G.; Inayat, F.; Ghouri, Y.A. A national study of pregnancy-related maternal and fetal outcomes in women with inflammatory bowel disease. Int. J. Colorectal Dis. 2022, 37, 1535–1543. [Google Scholar] [CrossRef]
- Chan, J.; Telang, R.; Kociszewska, D.; Thorne, P.R.; Vlajkovic, S.M. A High-Fat Diet Induces Low-Grade Cochlear Inflammation in CD-1 Mice. Int. J. Mol. Sci. 2022, 23, 5179. [Google Scholar] [CrossRef]
- Hyun, C.K. Molecular and Pathophysiological Links between Metabolic Disorders and Inflammatory Bowel Diseases. Int. J. Mol. Sci 2021, 22, 9139. [Google Scholar] [CrossRef]
- Yorulmaz, E.; Adali, G.; Yorulmaz, H.; Ulasoglu, C.; Tasan, G.; Tuncer, I. Metabolic syndrome frequency in inflammatory bowel diseases. Saudi J. Gastroenterol. 2011, 17, 376–382. [Google Scholar] [CrossRef]
- Zamani, M.; Alizadeh-Tabari, S.; Singh, S.; Loomba, R. Meta-analysis: Prevalence of, and risk factors for, non-alcoholic fatty liver disease in patients with inflammatory bowel disease. Aliment. Pharmacol. Ther. 2022, 55, 894–907. [Google Scholar] [CrossRef] [PubMed]
- Noorian, S.; Jeon, Y.; Nguyen, M.T.; Sauk, J.; Limketkai, B.N. The Impact of NAFLD on Hospitalization Outcomes in Patients With Inflammatory Bowel Diseases: Nationwide Analysis. Inflamm. Bowel Dis. 2022, 28, 878–887. [Google Scholar] [CrossRef] [PubMed]
- Jovanovic, M.; Simovic Markovic, B.; Gajovic, N.; Jurisevic, M.; Djukic, A.; Jovanovic, I.; Arsenijevic, N.; Lukic, A.; Zdravkovic, N. Metabolic syndrome attenuates ulcerative colitis: Correlation with interleukin-10 and galectin-3 expression. World J. Gastroenterol. 2019, 25, 6465–6482. [Google Scholar] [CrossRef]
- De Filippis, A.; Ullah, H.; Baldi, A.; Dacrema, M.; Esposito, C.; Garzarella, E.U.; Santarcangelo, C.; Tantipongpiradet, A.; Daglia, M. Gastrointestinal Disorders and Metabolic Syndrome: Dysbiosis as a Key Link and Common Bioactive Dietary Components Useful for their Treatment. Int. J. Mol. Sci. 2020, 21, 4929. [Google Scholar] [CrossRef]
- Lees, C.W.; Barrett, J.C.; Parkes, M.; Satsangi, J. New IBD genetics: Common pathways with other diseases. Gut 2011, 60, 1739–1753. [Google Scholar] [CrossRef]
- Doğan, A.N.; Kahraman, R.; Akar, T. Evaluation of insulin resistance and beta cell activity in patients with inflammatory bowel disease. Eur. Rev. Med. Pharmacol. Sci. 2022, 26, 3989–3994. [Google Scholar] [CrossRef]
- Sang, M.M.; Sun, Z.L.; Wu, T.Z. Inflammatory bowel disease and diabetes: Is there a link between them? World J. Diabetes 2022, 13, 126–128. [Google Scholar] [CrossRef] [PubMed]
- Jarmakiewicz-Czaja, S.; Sokal, A.; Pardak, P.; Filip, R. Glucocorticosteroids and the Risk of NAFLD in Inflammatory Bowel Disease. Can. J. Gastroenterol. Hepatol. 2022, 2022, 4344905. [Google Scholar] [CrossRef]
- Rodriguez-Duque, J.C.; Calleja, J.L.; Iruzubieta, P.; Hernández-Conde, M.; Rivas-Rivas, C.; Vera, M.I.; Garcia, M.J.; Pascual, M.; Castro, B.; García-Blanco, A.; et al. Increased risk of MAFLD and Liver Fibrosis in Inflammatory Bowel Disease Independent of Classic Metabolic Risk Factors. Clin. Gastroenterol. Hepatol. 2022, S1542-3565(22)00093-3, Epub ahead of print. [Google Scholar] [CrossRef]
- Spagnuolo, R.; Abenavoli, L.; Corea, A.; Larussa, T.; Mancina, R.M.; Cosco, C.; Luzza, F.; Doldo, P. Multifaceted pathogenesis of liver steatosis in inflammatory bowel disease: A systematic review. Eur. Rev. Med. Pharmacol. Sci. 2021, 25, 5818–5825. [Google Scholar] [CrossRef]
- Perez-Carreras, M.; Casis-Herce, B.; Rivera, R.; Fernandez, I.; Martinez-Montiel, P.; Villena, V. Non-alcoholic fatty liver disease in patients with intestinal, pulmonary or skin diseases: Inflammatory cross-talk that needs a multidisciplinary approach. World J. Gastroenterol. 2021, 27, 7113–7124. [Google Scholar] [CrossRef] [PubMed]
- Gibiino, G.; Sartini, A.; Gitto, S.; Binda, C.; Sbrancia, M.; Coluccio, C.; Sambri, V.; Fabbri, C. The Other Side of Malnutrition in Inflammatory Bowel Disease (IBD): Non-Alcoholic Fatty Liver Disease. Nutrients 2021, 13, 2772. [Google Scholar] [CrossRef]
- Galic, S.; Oakhill, J.S.; Steinberg, G.R. Adipose tissue as an endocrine organ. Mol. Cell Endocrinol. 2010, 316, 129–139. [Google Scholar] [CrossRef] [PubMed]
- Trayhurn, P.; Wood, I.S. Adipokines: Inflammation and the pleiotropic role of white adipose tissue. Br. J. Nutr. 2004, 92, 347–355. [Google Scholar] [CrossRef] [PubMed]
- Axelsson, J.; Heimbürger, O.; Lindholm, B.; Stenvinkel, P. Adipose tissue and its relation to inflammation: The role of adipokines. J. Ren. Nutr. 2005, 15, 131–136. [Google Scholar] [CrossRef]
- Conde, J.; Scotece, M.; Gómez, R.; López, V.; Gómez-Reino, J.J.; Lago, F.; Gualillo, O. Adipokines: Biofactors from white adipose tissue. A complex hub among inflammation, metabolism, and immunity. Biofactors 2011, 37, 413–420. [Google Scholar] [CrossRef]
- Fantuzzi, G. Adipose tissue, adipokines, and inflammation. J. Allergy Clin. Immunol. 2005, 115, 911–920. [Google Scholar] [CrossRef]
- Lago, F.; Dieguez, C.; Gómez-Reino, J.; Gualillo, O. Adipokines as emerging mediators of immune response and inflammation. Nat. Clin. Pract. Rheumatol. 2007, 3, 716–724. [Google Scholar] [CrossRef]
- Khakoo, N.S.; Ioannou, S.; Khakoo, N.S.; Vedantam, S.; Pearlman, M. Impact of Obesity on Inflammatory Bowel Disease. Curr. Gastroenterol. Rep. 2022, 24, 26–36. [Google Scholar] [CrossRef]
- Johnson, A.M.; Loftus, E.V. Obesity in inflammatory bowel disease: A review of its role in the pathogenesis, natural history, and treatment of IBD. Saudi J. Gastroenterol. 2021, 27, 183–190. [Google Scholar] [CrossRef]
- Han, S.; Wang, G.; Qiu, S.; de la Motte, C.; Wang, H.Q.; Gomez, G.; Englander, E.W.; Greeley, G.H., Jr. Increased colonic apelin production in rodents with experimental colitis and in humans with IBD. Regul. Pept. 2007, 142, 131–137. [Google Scholar] [CrossRef] [PubMed]
- Ge, Y.; Li, Y.; Chen, Q.; Zhu, W.; Zuo, L.; Guo, Z.; Gong, J.; Cao, L.; Gu, L.; Li, J. Adipokine apelin ameliorates chronic colitis in Il-10-/- mice by promoting intestinal lymphatic functions. Biochem. Pharmacol. 2018, 148, 202–212. [Google Scholar] [CrossRef] [PubMed]
- Weidinger, C.; Ziegler, J.F.; Letizia, M.; Schmidt, F.; Siegmund, B. Adipokines and Their Role in Intestinal Inflammation. Front. Immunol. 2018, 9, 1974. [Google Scholar] [CrossRef] [PubMed]
- Morshedzadeh, N.; Rahimlou, M.; Asadzadeh Aghdaei, H.; Shahrokh, S.; Reza Zali, M.; Mirmiran, P. Association between Adipokines Levels with Inflammatory Bowel Disease (IBD): Systematic Reviews. Dig. Dis. Sci. 2017, 62, 3280–3286. [Google Scholar] [CrossRef]
- Carbone, F.; La Rocca, C.; Matarese, G. Immunological functions of leptin and adiponectin. Biochimie 2012, 94, 2082–2088. [Google Scholar] [CrossRef]
- Lima, T.F.N.; Nackeeran, S.; Rakitina, E.; Lima, G.F.N.; Arora, H.; Kargi, A.Y.; Ramasamy, R. Association of Leptin with Total and Free Testosterone: Results from the National Health and Nutrition Examination Surveys. Androg. Clin. Res. Ther. 2020, 1, 94–100. [Google Scholar] [CrossRef]
- Childs, G.V.; Odle, A.K.; MacNicol, M.C.; MacNicol, A.M. The Importance of Leptin to Reproduction. Endocrinology 2021, 162, bqaa204. [Google Scholar] [CrossRef]
- Hellström, L.; Wahrenberg, H.; Hruska, K.; Reynisdottir, S.; Arner, P. Mechanisms behind gender differences in circulating leptin levels. J. Intern. Med. 2000, 247, 457–462. [Google Scholar] [CrossRef]
- Misch, M.; Puthanveetil, P. The Head-to-Toe Hormone: Leptin as an Extensive Modulator of Physiologic Systems. Int. J. Mol. Sci. 2022, 23, 5439. [Google Scholar] [CrossRef]
- Al-Hussaniy, H.A.; Alburghaif, A.H.; Naji, M.A. Leptin hormone and its effectiveness in reproduction, metabolism, immunity, diabetes, hopes and ambitions. J. Med. Life 2021, 14, 600–605. [Google Scholar] [CrossRef]
- Andreasson, A.N.; Undén, A.L.; Elofsson, S.; Brismar, K. Leptin and adiponectin: Distribution and associations with cardiovascular risk factors in men and women of the general population. Am. J. Hum. Biol. 2012, 24, 595–601. [Google Scholar] [CrossRef] [PubMed]
- Kralisch, S.; Sommer, G.; Deckert, C.M.; Linke, A.; Bluher, M.; Stumvoll, M.; Fasshauer, M. Adipokines in diabetes and cardiovascular diseases. Minerva Endocrinol. 2007, 32, 161–171. [Google Scholar] [PubMed]
- Reis, J.P.; Macera, C.A.; Wingard, D.L.; Araneta, M.R.; Lindsay, S.P.; Marshall, S.J. The relation of leptin and insulin with obesity-related cardiovascular risk factors in US adults. Atherosclerosis 2008, 200, 150–160. [Google Scholar] [CrossRef]
- Fernández-Riejos, P.; Najib, S.; Santos-Alvarez, J.; Martín-Romero, C.; Pérez-Pérez, A.; González-Yanes, C.; Sánchez-Margalet, V. Role of leptin in the activation of immune cells. Mediators Inflamm. 2010, 2010, 568343. [Google Scholar] [CrossRef] [PubMed]
- Busso, N.; So, A.; Chobaz-Péclat, V.; Morard, C.; Martinez-Soria, E.; Talabot-Ayer, D.; Gabay, C. Leptin signaling deficiency impairs humoral and cellular immune responses and attenuates experimental arthritis. J. Immunol. 2002, 168, 875–882. [Google Scholar] [CrossRef]
- Otero, M.; Lago, R.; Gomez, R.; Dieguez, C.; Lago, F.; Gomez-Reino, J.; Gualillo, O. Towards a pro-inflammatory and immunomodulatory emerging role of leptin. Rheumatology 2006, 45, 944–950. [Google Scholar] [CrossRef]
- Otero, M.; Lago, R.; Gómez, R.; Lago, F.; Gómez-Reino, J.J.; Gualillo, O. Leptin: A metabolic hormone that functions like a proinflammatory adipokine. Drug News Perspect. 2006, 19, 21–26. [Google Scholar] [CrossRef]
- Izquierdo, A.G.; Crujeiras, A.B.; Casanueva, F.F.; Carreira, M.C. Leptin, Obesity, and Leptin Resistance: Where Are We 25 Years Later? Nutrients 2019, 11, 2704. [Google Scholar] [CrossRef]
- Ahima, R.S.; Osei, S.Y. Adipokines in obesity. Front. Horm. Res. 2008, 36, 182–197. [Google Scholar] [CrossRef]
- De Rosa, V.; Procaccini, C.; Calì, G.; Pirozzi, G.; Fontana, S.; Zappacosta, S.; La Cava, A.; Matarese, G. A key role of leptin in the control of regulatory T cell proliferation. Immunity 2007, 26, 241–255. [Google Scholar] [CrossRef] [Green Version]
- Kiernan, K.; MacIver, N.J. The Role of the Adipokine Leptin in Immune Cell Function in Health and Disease. Front. Immunol. 2021, 11, 622468. [Google Scholar] [CrossRef] [PubMed]
- Hasenkrug, K.J. The leptin connection: Regulatory T cells and autoimmunity. Immunity 2007, 26, 143–145. [Google Scholar] [CrossRef] [PubMed]
- Bradley, D.; Shantaram, D.; Smith, A.; Hsueh, W.A. Adipose Tissue T Regulatory Cells: Implications for Health and Disease. Adv. Exp. Med. Biol. 2021, 1278, 125–139. [Google Scholar] [CrossRef]
- Gualillo, O.; Eiras, S.; Lago, F.; Diéguez, C.; Casanueva, F.F. Elevated serum leptin concentrations induced by experimental acute inflammation. Life Sci. 2000, 67, 2433–2441. [Google Scholar] [CrossRef]
- Granowitz, E.V.; Porat, R.; Dinarello, C.A. Circulating leptin during experimental endotoxemia in humans. J. Infect. Dis. 1999, 179, 1313–1314. [Google Scholar] [CrossRef] [PubMed]
- Bornstein, S.R.; Licinio, J.; Tauchnitz, R.; Engelmann, L.; Negrão, A.B.; Gold, P.; Chrousos, G.P. Plasma leptin levels are increased in survivors of acute sepsis: Associated loss of diurnal rhythm, in cortisol and leptin secretion. J. Clin. Endocrinol. Metab. 1998, 83, 280–283. [Google Scholar] [CrossRef] [PubMed]
- Yousef, A.A.; Amr, Y.M.; Suliman, G.A. The diagnostic value of serum leptin monitoring and its correlation with tumor necrosis factor-alpha in critically ill patients: A prospective observational study. Crit Care 2010, 14, R33. [Google Scholar] [CrossRef] [PubMed]
- Carlson, G.L.; Saeed, M.; Little, R.A.; Irving, M.H. Serum leptin concentrations and their relation to metabolic abnormalities in human sepsis. Am. J. Physiol. 1999, 276, E658–E662. [Google Scholar] [CrossRef]
- Adrych, K.; Smoczynski, M.; Goyke, E.; Stelmanska, E.; Swierczynski, J. Decreased serum leptin concentration in patients with chronic pancreatitis. Pancreas 2007, 34, 417–422. [Google Scholar] [CrossRef]
- Popa, C.; Netea, M.G.; de Graaf, J.; van den Hoogen, F.H.; Radstake, T.R.; Toenhake-Dijkstra, H.; van Riel, P.L.; van der Meer, J.W.; Stalenhoef, A.F.; Barrera, P. Circulating leptin and adiponectin concentrations during tumor necrosis factor blockade in patients with active rheumatoid arthritis. J. Rheumatol. 2009, 36, 724–730. [Google Scholar] [CrossRef]
- Fazolini, N.P.; Cruz, A.L.; Werneck, M.B.; Viola, J.P.; Maya-Monteiro, C.M.; Bozza, P.T. Leptin activation of mTOR pathway in intestinal epithelial cell triggers lipid droplet formation, cytokine production and increased cell proliferation. Cell Cycle 2015, 14, 2667–2676. [Google Scholar] [CrossRef] [PubMed]
- Biesiada, G.; Czepiel, J.; Ptak-Belowska, A.; Targosz, A.; Krzysiek-Maczka, G.; Strzalka, M.; Konturek, S.J.; Brzozowski, T.; Mach, T. Expression and release of leptin and proinflammatory cytokines in patients with ulcerative colitis and infectious diarrhea. J. Physiol. Pharmacol. 2012, 63, 471–481. [Google Scholar]
- Tuzun, A.; Uygun, A.; Yesilova, Z.; Ozel, A.M.; Erdil, A.; Yaman, H.; Bagci, S.; Gulsen, M.; Karaeren, N.; Dagalp, K. Leptin levels in the acute stage of ulcerative colitis. J. Gastroenterol. Hepatol. 2004, 19, 429–432. [Google Scholar] [CrossRef] [PubMed]
- Kahraman, R.; Calhan, T.; Sahin, A.; Ozdil, K.; Caliskan, Z.; Bireller, E.S.; Cakmakoglu, B. Are adipocytokines inflammatory or metabolic mediators in patients with inflammatory bowel disease? Ther. Clin. Risk Manag. 2017, 13, 1295–1301. [Google Scholar] [CrossRef]
- Mello, J.D.C.; Gomes, L.E.M.; Silva, J.F.; Siqueira, N.S.N.; Pascoal, L.B.; Martinez, C.A.R.; Ayrizono, M.D.L.S.; Leal, R.F. The role of chemokines and adipokines as biomarkers of Crohn’s disease activity: A systematic review of the literature. Am. J. Transl Res. 2021, 13, 8561–8574. [Google Scholar]
- Paul, G.; Schaer, A.; Neumeier, M.; Furst, A.; Bataillle, F.; Buechler, C.; Muller-Ladner, U.; Scholmerich, J.; Rogler, G.; Herfarth, H. Profiling adipocytokine secretion from creeping fat in Crohn’s disease. Inflamm. Bowel Dis. 2006, 12, 471–477. [Google Scholar] [CrossRef] [PubMed]
- Trejo-Vazquez, F.; Garza-Veloz, I.; Villela-Ramirez, G.A.; Ortiz-Castro, Y.; Mauricio-Saucedo, P.; Cardenas-Vargas, E.; Diaz-Baez, M.; Cid-Baez, M.A.; Castañeda-Miranda, R.; Ortiz-Rodriguez, J.M.; et al. Positive association between leptin serum levels and disease activity on endoscopy in inflammatory bowel disease: A case-control study. Exp. Ther. Med. 2018, 15, 3336–3344. [Google Scholar] [CrossRef]
- Karmiris, K.; Koutroubakis, I.E.; Xidakis, C.; Polychronaki, M.; Voudouri, T.; Kouroumalis, E.A. Circulating levels of leptin, adiponectin, resistin, and ghrelin in inflammatory bowel disease. Inflamm. Bowel Dis. 2006, 12, 100–105. [Google Scholar] [CrossRef]
- Nishi, Y.; Isomoto, H.; Ueno, H.; Ohnita, K.; Wen, C.Y.; Takeshima, F.; Mishima, R.; Nakazato, M.; Kohno, S. Plasma leptin and ghrelin concentrations in patients with Crohn’s disease. World J. Gastroenterol. 2005, 11, 7314–7317. [Google Scholar] [CrossRef]
- Singh, U.P.; Singh, N.P.; Guan, H.; Busbee, B.; Price, R.L.; Taub, D.D.; Mishra, M.K.; Fayad, R.; Nagarkatti, M.; Nagarkatti, P.S. Leptin antagonist ameliorates chronic colitis in IL-10−/− mice. Immunobiology 2013, 218, 1439–1451. [Google Scholar] [CrossRef]
- Siegmund, B.; Sennello, J.A.; Jones-Carson, J.; Gamboni-Robertson, F.; Lehr, H.A.; Batra, A.; Fedke, I.; Zeitz, M.; Fantuzzi, G. Leptin receptor expression on T lymphocytes modulates chronic intestinal inflammation in mice. Gut 2004, 53, 965–972. [Google Scholar] [CrossRef] [PubMed]
- Koerner, A.; Kratzsch, J.; Kiess, W. Adipocytokines: Leptin—The classical, resistin—The controversical, adiponectin—The promising, and more to come. Best Pract Res. Clin. Endocrinol. Metab. 2005, 19, 525–546. [Google Scholar] [CrossRef]
- Robinson, K.; Prins, J.; Venkatesh, B. Clinical review: Adiponectin biology and its role in inflammation and critical illness. Crit. Care 2011, 15, 221. [Google Scholar] [CrossRef] [PubMed]
- Whitehead, J.P.; Richards, A.A.; Hickman, I.J.; Macdonald, G.A.; Prins, J.B. Adiponectin—A key adipokine in the metabolic syndrome. Diabetes Obes. Metab. 2006, 8, 264–280. [Google Scholar] [CrossRef] [PubMed]
- Aljafary, M.A.; Al-Suhaimi, E.A. Adiponectin System (Rescue Hormone): The Missing Link between Metabolic and Cardiovascular Diseases. Pharmaceutics 2022, 14, 1430. [Google Scholar] [CrossRef] [PubMed]
- Dyck, D.J.; Heigenhauser, G.J.; Bruce, C.R. The role of adipokines as regulators of skeletal muscle fatty acid metabolism and insulin sensitivity. Acta Physiol. 2006, 186, 5–16. [Google Scholar] [CrossRef]
- Xu, A.; Vanhoutte, P.M. Adiponectin and adipocyte fatty acid binding protein in the pathogenesis of cardiovascular disease. Am. J. Physiol. Heart Circ. Physiol. 2012, 302, H1231–H1240. [Google Scholar] [CrossRef]
- Ohashi, K.; Parker, J.L.; Ouchi, N.; Higuchi, A.; Vita, J.A.; Gokce, N.; Pedersen, A.A.; Kalthoff, C.; Tullin, S.; Sams, A.; et al. Adiponectin promotes macrophage polarization toward an anti-inflammatory phenotype. J. Biol. Chem. 2010, 285, 6153–6160. [Google Scholar] [CrossRef]
- Ohashi, K.; Ouchi, N.; Matsuzawa, Y. Anti-inflammatory and anti-atherogenic properties of adiponectin. Biochimie 2012, 94, 2137–2142. [Google Scholar] [CrossRef]
- Polyzos, S.A.; Toulis, K.A.; Goulis, D.G.; Zavos, C.; Kountouras, J. Serum total adiponectin in nonalcoholic fatty liver disease: A systematic review and meta-analysis. Metabolism 2011, 60, 313–326. [Google Scholar] [CrossRef]
- Weyer, C.; Funahashi, T.; Tanaka, S.; Hotta, K.; Matsuzawa, Y.; Pratley, R.E.; Tataranni, P.A. Hypoadiponectinemia in obesity and type 2 diabetes: Close association with insulin resistance and hyperinsulinemia. J. Clin. Endocrinol. Metab. 2001, 86, 1930–1935. [Google Scholar] [CrossRef] [PubMed]
- Nishimura, S.; Manabe, I.; Nagai, R. Adipose tissue inflammation in obesity and metabolic syndrome. Discov. Med. 2009, 8, 55–60. [Google Scholar]
- Guerre-Millo, M. Adiponectin: An update. Diabetes Metab. 2008, 34, 12–18. [Google Scholar] [CrossRef] [PubMed]
- Ouchi, N.; Walsh, K. Adiponectin as an anti-inflammatory factor. Clin. Chim. Acta 2007, 380, 24–30. [Google Scholar] [CrossRef]
- Fantuzzi, G. Adiponectin and inflammation: Consensus and controversy. J. Allergy Clin. Immunol. 2008, 121, 326–330. [Google Scholar] [CrossRef]
- Giles, J.T.; van der Heijde, D.M.; Bathon, J.M. Association of circulating adiponectin levels with progression of radiographic joint destruction in rheumatoid arthritis. Ann. Rheum. Dis. 2011, 70, 1562–1568. [Google Scholar] [CrossRef]
- Li, L.; Wu, L.L. Adiponectin and interleukin-6 in inflammation-associated disease. Vitam Horm. 2012, 90, 375–395. [Google Scholar] [CrossRef] [PubMed]
- Toussirot, É.; Binda, D.; Gueugnon, C.; Dumoulin, G. Adiponectin in autoimmune diseases. Curr. Med. Chem. 2012, 19, 5474–5480. [Google Scholar] [CrossRef] [PubMed]
- Choi, H.M.; Doss, H.M.; Kim, K.S. Multifaceted Physiological Roles of Adiponectin in Inflammation and Diseases. Int. J. Mol. Sci. 2020, 21, 1219. [Google Scholar] [CrossRef]
- Brezovec, N.; Perdan-Pirkmajer, K.; Čučnik, S.; Sodin-Šemrl, S.; Varga, J.; Lakota, K. Adiponectin Deregulation in Systemic Autoimmune Rheumatic Diseases. Int. J. Mol. Sci. 2021, 22, 4095. [Google Scholar] [CrossRef]
- Michalak, A.; Mosińska, P.; Fichna, J. Common links between metabolic syndrome and inflammatory bowel disease: Current overview and future perspectives. Pharmacol. Rep. 2016, 68, 837–846. [Google Scholar] [CrossRef] [PubMed]
- Yamamoto, K.; Kiyohara, T.; Murayama, Y.; Kihara, S.; Okamoto, Y.; Funahashi, T.; Ito, T.; Nezu, R.; Tsutsui, S.; Miyagawa, J.I.; et al. Production of adiponectin, an anti-inflammatory protein, in mesenteric adipose tissue in Crohn’s disease. Gut 2005, 54, 789–796. [Google Scholar] [CrossRef] [PubMed]
- Fayad, R.; Pini, M.; Sennello, J.A.; Cabay, R.J.; Chan, L.; Xu, A.; Fantuzzi, G. Adiponectin deficiency protects mice from chemically induced colonic inflammation. Gastroenterology 2007, 132, 601–614. [Google Scholar] [CrossRef] [PubMed]
- Nishihara, T.; Matsuda, M.; Araki, H.; Oshima, K.; Kihara, S.; Funahashi, T.; Shimomura, I. Effect of adiponectin on murine colitis induced by dextran sulfate sodium. Gastroenterology 2006, 131, 853–861. [Google Scholar] [CrossRef]
- Ogunwobi, O.O.; Beales, I.L. Adiponectin stimulates proliferation and cytokine secretion in colonic epithelial cells. Regul. Pept. 2006, 134, 105–113. [Google Scholar] [CrossRef]
- Sideri, A.; Stavrakis, D.; Bowe, C.; Shih, D.Q.; Fleshner, P.; Arsenescu, V.; Arsenescu, R.; Turner, J.R.; Pothoulakis, C.; Karagiannides, I. Effects of obesity on severity of colitis and cytokine expression in mouse mesenteric fat. Potential role of adiponectin receptor 1. Am. J. Physiol. Gastrointest. Liver Physiol. 2015, 308, G591–G604. [Google Scholar] [CrossRef]
- Obeid, S.; Wankell, M.; Charrez, B.; Sternberg, J.; Kreuter, R.; Esmaili, S.; Ramezani-Moghadam, M.; Devine, C.; Read, S.; Bhathal, P.; et al. Adiponectin confers protection from acute colitis and restricts a B cell immune response. J. Biol. Chem. 2017, 292, 6569–6582. [Google Scholar] [CrossRef]
- Steppan, C.M.; Bailey, S.T.; Bhat, S.; Brown, E.J.; Banerjee, R.R.; Wright, C.M.; Patel, H.R.; Ahima, R.S.; Lazar, M.A. The hormone resistin links obesity to diabetes. Nature 2001, 409, 307–312. [Google Scholar] [CrossRef]
- Barnes, K.M.; Miner, J.L. Role of resistin in insulin sensitivity in rodents and humans. Curr. Protein Pept. Sci. 2009, 10, 96–107. [Google Scholar] [CrossRef]
- Schwartz, D.R.; Lazar, M.A. Human resistin: Found in translation from mouse to man. Trends Endocrinol. Metab. 2011, 22, 259–265. [Google Scholar] [CrossRef]
- Filková, M.; Hulejová, H.; Kuncová, K.; Pleštilová, L.; Cerezo, L.A.; Mann, H.; Klein, M.; Zámečník, J.; Gay, S.; Vencovský, J.; et al. Resistin in idiopathic inflammatory myopathies. Arthritis Res. Ther. 2012, 14, R111. [Google Scholar] [CrossRef] [PubMed]
- Jiang, C.Y.; Wang, W.; Yin, Y.L.; Yuan, Z.R.; Wang, L.B. Expression of the adipocytokine resistin and its association with the clinicopathological features and prognosis of pancreatic ductal adenocarcinoma. Oncol. Lett. 2012, 4, 960–964. [Google Scholar] [CrossRef] [PubMed]
- Jamaluddin, M.S.; Weakley, S.M.; Yao, Q.; Chen, C. Resistin: Functional roles and therapeutic considerations for cardiovascular disease. Br. J. Pharmacol. 2012, 165, 622–632. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Filková, M.; Haluzík, M.; Gay, S.; Senolt, L. The role of resistin as a regulator of inflammation: Implications for various human pathologies. Clin. Immunol. 2009, 133, 157–170. [Google Scholar] [CrossRef]
- Beier, J.I.; Guo, L.; von Montfort, C.; Kaiser, J.P.; Joshi-Barve, S.; Arteel, G.E. New role of resistin in lipopolysaccharide-induced liver damage in mice. J. Pharmacol. Exp. Ther. 2008, 325, 801–808. [Google Scholar] [CrossRef]
- Baker, J.F.; Morales, M.; Qatanani, M.; Cucchiara, A.; Nackos, E.; Lazar, M.A.; Teff, K.; von Feldt, J.M. Resistin levels in lupus and associations with disease-specific measures, insulin resistance, and coronary calcification. J. Rheumatol. 2011, 38, 2369–2375. [Google Scholar] [CrossRef]
- Stofkova, A. Resistin and visfatin: Regulators of insulin sensitivity, inflammation and immunity. Endocr. Regul. 2010, 44, 25–36. [Google Scholar] [CrossRef]
- Ellington, A.A.; Malik, A.R.; Klee, G.G.; Turner, S.T.; Rule, A.D.; Mosley, T.H., Jr.; Kullo, I.J. Association of plasma resistin with glomerular filtration rate and albuminuria in hypertensive adults. Hypertension 2007, 50, 708–714. [Google Scholar] [CrossRef]
- Menzaghi, C.; Salvemini, L.; Fini, G.; Thompson, R.; Mangiacotti, D.; Di Paola, R.; Morini, E.; Giorelli, M.; De Bonis, C.; De Cosmo, S.; et al. Serum resistin and kidney function: Afamily-based study in non-diabetic, untreated individuals. PLoS ONE 2012, 7, e38414. [Google Scholar] [CrossRef]
- Axelsson, J.; Bergsten, A.; Qureshi, A.R.; Heimbürger, O.; Bárány, P.; Lönnqvist, F.; Lindholm, B.; Nordfors, L.; Alvestrand, A.; Stenvinkel, P. Elevated resistin levels in chronic kidney disease are associated with decreased glomerular filtration rate and inflammation, but not with insulin resistance. Kidney Int. 2006, 69, 596–604. [Google Scholar] [CrossRef]
- Deng, Y.; Scherer, P.E. Adipokines as novel biomarkers and regulators of the metabolic syndrome. Ann. N. Y. Acad. Sci. 2010, 1212, E1–E19. [Google Scholar] [CrossRef] [PubMed]
- Al-Suhaimi, E.A.; Shehzad, A. Leptin, resistin and visfatin: The missing link between endocrine metabolic disorders and immunity. Eur. J. Med. Res. 2013, 18, 12. [Google Scholar] [CrossRef] [PubMed]
- Konrad, A.; Lehrke, M.; Schachinger, V.; Seibold, F.; Stark, R.; Ochsenkühn, T.; Parhofer, K.G.; Göke, B.; Broedl, U.C. Resistin is an inflammatory marker of inflammatory bowel disease in humans. Eur. J. Gastroenterol. Hepatol. 2007, 19, 1070–1074. [Google Scholar] [CrossRef] [PubMed]
- Karmiris, K.; Koutroubakis, I.E.; Xidakis, C.; Polychronaki, M.; Kouroumalis, E.A. The effect of infliximab on circulating levels of leptin, adiponectin and resistin in patients with inflammatory bowel disease. Eur. J. Gastroenterol. Hepatol. 2007, 19, 789–794. [Google Scholar] [CrossRef]
- Soomro, S.; Venkateswaran, S.; Vanarsa, K.; Kharboutli, M.; Nidhi, M.; Susarla, R.; Zhang, T.; Sasidharan, P.; Lee, K.H.; Rosh, J.; et al. Predicting disease course in ulcerative colitis using stool proteins identified through an aptamer-based screen. Nat. Commun. 2021, 12, 3989. [Google Scholar] [CrossRef]
- Karásková, E.; Kubickova, V.; Velganova-Veghova, M.; Geryk, M.; Foltenova, H.; Karasek, D. Circulating levels of WISP-1 (Wnt1-inducible signaling pathway protein 1) and other selected adipokines in children with inflammatory bowel disease. Physiol. Res. 2022, 71, 275–284. [Google Scholar] [CrossRef]
- Wittamer, V.; Franssen, J.D.; Vulcano, M.; Mirjolet, J.F.; Le Poul, E.; Migeotte, I.; Brézillon, S.; Tyldesley, R.; Blanpain, C.; Detheux, M.; et al. Specific recruitment of antigen-presenting cells by chemerin, a novel processed ligand from human inflammatory fluids. J. Exp. Med. 2003, 198, 977–985. [Google Scholar] [CrossRef]
- Jacenik, D.; Fichna, J. Chemerin in immune response and gastrointestinal pathophysiology. Clin. Chim. Acta 2020, 504, 146–153. [Google Scholar] [CrossRef]
- Sochal, M.; Mosińska, P.; Fichna, J. Diagnostic value of chemerin in lower gastrointestinal diseases-a review. Peptides 2018, 108, 19–24. [Google Scholar] [CrossRef]
- Weigert, J.; Obermeier, F.; Neumeier, M.; Wanninger, J.; Filarsky, M.; Bauer, S.; Aslanidis, C.; Rogler, G.; Ott, C.; Schäffler, A.; et al. Circulating levels of chemerin and adiponectin are higher in ulcerative colitis and chemerin is elevated in Crohn’s disease. Inflamm. Bowel Dis. 2010, 16, 630–637. [Google Scholar] [CrossRef]
- Buechler, C. Chemerin, a novel player in inflammatory bowel disease. Cell Mol. Immunol. 2014, 11, 315–316. [Google Scholar] [CrossRef] [PubMed]
- Dranse, H.J.; Rourke, J.L.; Stadnyk, A.W.; Sinal, C.J. Local chemerin levels are positively associated with DSS-induced colitis but constitutive loss of CMKLR1 does not protect against development of colitis. Physiol. Rep. 2015, 3, e12497. [Google Scholar] [CrossRef] [PubMed]
- Lin, Y.; Cai, Q.; Luo, Y.; Li, B.; Chen, Y.; Yang, X.; Xuan, Y.; Yang, H.; He, R. Epithelial chemerin-CMKLR1 signaling restricts microbiota-driven colonic neutrophilia and tumorigenesis by up-regulating lactoperoxidase. Proc. Natl. Acad. Sci. USA 2022, 119, e74119. [Google Scholar] [CrossRef] [PubMed]
- Lin, Y.; Yang, X.; Yue, W.; Xu, X.; Li, B.; Zou, L.; He, R. Chemerin aggravates DSS-induced colitis by suppressing M2 macrophage polarization. Cell Mol. Immunol. 2014, 11, 355–366. [Google Scholar] [CrossRef] [PubMed]
- Versini, M.; Jeandel, P.Y.; Rosenthal, E.; Shoenfeld, Y. Obesity in autoimmune diseases: Not a passive bystander. Autoimmun. Rev. 2014, 13, 981–1000. [Google Scholar] [CrossRef] [PubMed]
- Terzoudis, S.; Malliaraki, N.; Damilakis, J.; Dimitriadou, D.A.; Zavos, C.; Koutroubakis, I.E. Chemerin, visfatin, and vaspin serum levels in relation to bone mineral density in patients with inflammatory bowel disease. Eur. J. Gastroenterol. Hepatol. 2016, 28, 814–819. [Google Scholar] [CrossRef]
- Waluga, M.; Hartleb, M.; Boryczka, G.; Kukla, M.; Zwirska-Korczala, K. Serum adipokines in inflammatory bowel disease. World J. Gastroenterol. 2014, 20, 6912–6917. [Google Scholar] [CrossRef]
- Dogan, S.; Guven, K.; Celikbilek, M.; Deniz, K.; Saraymen, B.; Gursoy, S. Serum Visfatin Levels in Ulcerative Colitis. J. Clin. Lab. Anal. 2016, 30, 552–556. [Google Scholar] [CrossRef]
- Saadoun, M.M.; Nosair, N.A.E.; Abdel-Azeez, H.A.; Sharaf, S.M.; Ahmed, M.H. Serum Visfatin as a Diagnostic Marker of Active Inflammatory Bowel Disease. J. Gastrointestin. Liver Dis. 2021, 30, 339–345. [Google Scholar] [CrossRef]
- Moschen, A.R.; Kaser, A.; Enrich, B.; Mosheimer, B.; Theurl, M.; Niederegger, H.; Tilg, H. Visfatin, an adipocytokine with proinflammatory and immunomodulating properties. J. Immunol. 2007, 178, 1748–1758. [Google Scholar] [CrossRef]
- Fasshauer, M.; Bluher, M. Adipokines in health and disease. Trends Pharmacol. Sci. 2015, 36, 461–470. [Google Scholar] [CrossRef] [PubMed]
- Morisaki, T.; Takeshima, F.; Fukuda, H.; Matsushima, K.; Akazawa, Y.; Yamaguchi, N.; Ohnita, K.; Isomoto, H.; Takeshita, H.; Sawai, T.; et al. High serum vaspin concentrations in patients with ulcerative colitis. Dig. Dis. Sci. 2014, 59, 315–321. [Google Scholar] [CrossRef] [PubMed]
- Ohashi, K.; Shibata, R.; Murohara, T.; Ouchi, N. Role of anti-inflammatory adipokines in obesity-related diseases. Trends Endocrinol. Metab. 2014, 25, 348–355. [Google Scholar] [CrossRef]
- Yin, J.; Hou, P.; Wu, Z.; Nie, Y. Decreased levels of serum omentin-1 in patients with inflammatory bowel disease. Med. Sci. Monit. 2015, 21, 118–122. [Google Scholar]
- Lu, Y.; Zhou, L.; Liu, L.; Feng, Y.; Lu, L.; Ren, X.; Dong, X.; Sang, W. Serum omentin-1 as a disease activity marker for Crohn’s disease. Dis. Mark. 2014, 2014, 162517. [Google Scholar] [CrossRef] [PubMed]
- Rao, R.R.; Long, J.Z.; White, J.P.; Svensson, K.J.; Lou, J.; Lokurkar, I.; Jedrychowski, M.P.; Ruas, J.L.; Wrann, C.D.; Lo, J.C. Meteorin-like is a hormone that regulates immune-adipose interactions to increase beige fat thermogenesis. Cell 2014, 157, 1279–1291. [Google Scholar] [CrossRef]
- Zheng, S.L.; Li, Z.Y.; Song, J.; Liu, J.M.; Miao, C.Y. Metrnl: A secreted protein with new emerging functions. Acta Pharmacol. Sin. 2016, 37, 571–579. [Google Scholar] [CrossRef] [PubMed]
- Zuo, L.; Ge, S.; Ge, Y.; Li, J.; Zhu, B.; Zhang, Z.; Jiang, C.; Li, J.; Wang, S.; Liu, M. The adipokine metrnl ameliorates chronic colitis in Il-10–/–mice by attenuating mesenteric adipose tissue lesions during spontaneous colitis. J. Crohn’s Colitis 2019, 13, 931–941. [Google Scholar] [CrossRef]
- Tiaka, E.K.; Manolakis, A.C.; Kapsoritakis, A.N.; Potamianos, S.P. Unraveling the link between leptin, ghrelin and different types of colitis. Ann. Gastroenterol. 2011, 24, 20–28. [Google Scholar]
- Konturek, P.C.; Brzozowski, T.; Engel, M.; Burnat, G.; Gaca, P.; Kwiecien, S.; Pajdo, R.; Konturek, S.J. Ghrelin ameliorates colonic inflammation. Role of nitric oxide and sensory nerves. J. Physiol. Pharmacol. 2009, 60, 41–47. [Google Scholar]
- Sales, K.M.O.; Cavalcanti, R.F.; Nobre E Souza, M.A.; Saraiva, L.G.M.; Braga, L.L.B.C.; de Castro, M.; Oliveira, R.B.; Souza, M.H.L.P. Gastroduodenal Symptoms in Inflammatory Bowel Disease Are Correlated with Gastric Emptying and Serum Levels of Active Ghrelin. Dig. Dis. 2019, 37, 226–233. [Google Scholar] [CrossRef] [PubMed]
- Zhang, W.; Zhao, L.; Lin, T.R.; Chai, B.; Fan, Y.; Gantz, I.; Mulholland, M.W. Inhibition of Adipogenesis by Ghrelin. Mol. Biol. Cell 2004, 15, 2484–2491. [Google Scholar] [CrossRef] [PubMed]
- Bilski, J.; Mazur-Bialy, A.; Wojcik, D.; Surmiak, M.; Magierowski, M.; Sliwowski, Z.; Pajdo, R.; Kwiecien, S.; Danielak, A.; Ptak-Belowska, A.; et al. Role of Obesity, Mesenteric Adipose Tissue, and Adipokines in Inflammatory Bowel Diseases. Biomolecules 2019, 9, 780. [Google Scholar] [CrossRef] [PubMed]
- Drouet, M.; Dubuquoy, L.; Desreumaux, P.; Bertin, B. Visceral fat and gut inflammation. Nutrition 2012, 28, 113–117. [Google Scholar] [CrossRef] [PubMed]
- White, R.T.; Damm, D.; Hancock, N.; Rosen, B.S.; Lowell, B.B.; Usher, P.; Flier, J.S.; Spiegelman, B.M. Human adipsin is identical to complement factor D and is expressed at high levels in adipose tissue. J. Biol. Chem. 1992, 267, 9210–9213. [Google Scholar] [CrossRef]
- Hotamisligil, G.S.; Shargill, N.S.; Spiegelman, B.M. Adipose expression of tumor necrosis factor-alpha: Direct role in obesity-linked insulin resistance. Science 1993, 259, 87–91. [Google Scholar] [CrossRef] [PubMed]
- Crohn, B.B.; Ginzburg, L.; Oppenheimer, G.D. Landmark article Oct 15, 1932. Regional ileitis. A pathological and clinical entity. By Burril B. Crohn, Leon Ginzburg, and Gordon D. Oppenheimer. JAMA 1984, 251, 73–79. [Google Scholar] [CrossRef] [PubMed]
- Karaskova, E.; Velganova-Veghova, M.; Geryk, M.; Foltenova, H.; Kucerova, V.; Karasek, D. Role of Adipose Tissue in Inflammatory Bowel Disease. Int. J. Mol. Sci. 2021, 22, 4226. [Google Scholar] [CrossRef]
- Mao, R.; Kurada, S.; Gordon, I.O.; Baker, M.E.; Gandhi, N.; McDonald, C.; Coffey, J.C.; Rieder, F. The Mesenteric Fat and Intestinal Muscle Interface: Creeping Fat Influencing Stricture Formation in Crohn’s Disease. Inflamm. Bowel Dis. 2019, 25, 421–426. [Google Scholar] [CrossRef]
- Mao, R.; Doyon, G.; Gordon, I.O.; Li, J.; Lin, S.; Wang, J.; Le, T.H.N.; Elias, M.; Kurada, S.; Southern, B.; et al. Activated intestinal muscle cells promote preadipocyte migration: A novel mechanism for creeping fat formation in Crohn’s disease. Gut 2022, 71, 55–67. [Google Scholar] [CrossRef]
- Karrasch, T.; Schaeer, A. Adipokines and the role of visceral adipose tissue in inflammatory bowel disease. Ann. Gastroenterol. 2016, 29, 424–438. [Google Scholar] [CrossRef] [PubMed]
- Batra, A.; Pietsch, J.; Fedke, I.; Glauben, R.; Okur, B.; Stroh, T.; Zeitz, M.; Siegmund, B. Leptin-dependent toll-like receptor expression and responsiveness in preadipocytes and adipocytes. Am. J. Pathol. 2007, 170, 1931–1941. [Google Scholar] [CrossRef]
- Barbier, M.; Vidal, H.; Desreumaux, P.; Dubuguoy, L.; Bourreille, A.; Colombel, J.F.; Cherbut, C.; Galmiche, J.P. Overexpression of leptin mRNA in mesenteric adipose tissue in inflammatory bowel diseases. Gastroenterol. Clin. Biol. 2003, 1221, 987–991. [Google Scholar] [CrossRef]
- Eder, P.; Adler, M.; Dobrowolska, A.; Kamhieh-Milz, J.; Witowski, J. The Role of Adipose Tissue in the Pathogenesis and Therapeutic Outcomes of Inflammatory Bowel Disease. Cells 2019, 8, 628. [Google Scholar] [CrossRef] [PubMed]
- Elhag, D.A.; Kumar, M.; Saadaoui, M.; Akobeng, A.K.; Al-Mudahka, F.; Elawad, M.; Al Khodor, S. Inflammatory Bowel Disease Treatments and Predictive Biomarkers of Therapeutic Response. Int. J. Mol. Sci. 2022, 23, 6966. [Google Scholar] [CrossRef]
- Liu, S.; Ding, X.; Maggiore, G.; Pietrobattista, A.; Satapathy, S.K.; Tian, Z.; Jing, X. Sarcopenia is associated with poor clinical outcomes in patients with inflammatory bowel disease: A prospective cohort study. Ann. Transl. Med. 2022, 10, 367. [Google Scholar] [CrossRef]
- Shaban, N.; Hoad, C.L.; Naim, I.; Alshammari, M.; Radford, S.J.; Clarke, C.; Marciani, L.; Moran, G. Imaging in inflammatory bowel disease: Current and future perspectives. Frontline Gastroenterol. 2022, 13, e28–e34. [Google Scholar] [CrossRef]
- Faye, A.S.; Dodson, J.A.; Shaukat, A. Sarcopenia as a Risk Prediction Tool in Inflammatory Bowel Disease. Inflamm. Bowel Dis. 2022, izac069, Epub ahead of print. [Google Scholar] [CrossRef]
- Campbell, J.P.; Teigen, L.; Manski, S.; Blumhof, B.; Guglielmo, F.F.; Shivashankar, R.; Shmidt, E. Sarcopenia Is More Prevalent Among Inflammatory Bowel Disease Patients Undergoing Surgery and Predicts Progression to Surgery Among Medically Treated Patients. Inflamm. Bowel Dis. 2022, izac013, Epub ahead of print. [Google Scholar] [CrossRef]
- Singh, A.; Wall, C.; Levine, A.; Midha, V.; Mahajan, R.; Sood, A. Nutritional screening and assessment in inflammatory bowel disease. Indian J. Gastroenterol. 2022, 41, 5–22. [Google Scholar] [CrossRef]
- Rocha, R.; de Santos, J.G.; Santana, G. Influence of nutritional status in the postoperative period of patients with inflammatory bowel disease. World J. Gastrointest. Pharmacol. Ther. 2021, 12, 90–99. [Google Scholar] [CrossRef] [PubMed]
- Weidinger, C.; Hegazy, A.N.; Siegmund, B. The role of adipose tissue in inflammatory bowel diseases. Curr. Opin. Gastroenterol. 2018, 34, 183–186. [Google Scholar] [CrossRef] [PubMed]
- Kreuter, R.; Wankell, M.; Ahlenstiel, G.; Hebbard, L. The role of obesity in inflammatory bowel disease. Biochim. Biophys. Acta Mol. Basis Dis. 2019, 1865, 63–72. [Google Scholar] [CrossRef]
- Tsai, Y.W.; Fu, S.H.; Dong, J.L.; Chien, M.W.; Liu, Y.W.; Hsu, C.Y.; Sytwu, H.K. Adipokine-Modulated Immunological Homeostasis Shapes the Pathophysiology of Inflammatory Bowel Disease. Int. J. Mol. Sci. 2020, 21, 9564. [Google Scholar] [CrossRef] [PubMed]
- Pietsch, J.; Batra, A.; Stroh, T.; Fedke, I.; Glauben, R.; Okur, B.; Zeitz, M.; Siegmund, B. Toll-like receptor expression and response to specific stimulation in adipocytes and preadipocytes: On the role of fat in inflammation. Ann. N. Y. Acad. Sci. 2006, 1072, 407–409. [Google Scholar] [CrossRef]
- Lin, Y.; Lee, H.; Berg, A.H.; Lisanti, M.P.; Shapiro, L.; Scherer, P.E. The lipopolysaccharide-activated toll-like receptor (TLR)-4 induces synthesis of the closely related receptor TLR-2 in adipocytes. J. Biol. Chem. 2000, 11, 24255–24263. [Google Scholar] [CrossRef] [Green Version]
- Schaeer, A.; Gross, P.; Buettner, R.; Bollheimer, C.; Buechler, C.; Neumeier, M.; Kopp, A.; Schoelmerich, J.; Falk, W. Fatty acid-induced induction of Toll-like receptor-4/nuclear factor-B pathway in adipocytes links nutritional signalling with innate immunity. Immunology 2009, 126, 233–245. [Google Scholar]
- Coman, D.; Coales, I.; Roberts, L.B.; Neves, J.F. Helper-Like Type-1 Innate Lymphoid Cells in Inflammatory Bowel Disease. Front. Immunol. 2022, 13, 903688. [Google Scholar] [CrossRef]
- Kopp, A.; Buechler, C.; Neumeier, M.; Weigert, J.; Aslanidis, C.; Scholmerich, J.; Schaer, A. Innate immunity and adipocyte function: Ligand-specific activation of multiple Toll-like receptors modulates cytokine, adipokine, and chemokine secretion in adipocytes. Obesity 2009, 17, 648–656. [Google Scholar] [CrossRef]
- Kredel, L.I.; Jödicke, L.J.; Scheffold, A.; Gröne, J.; Glauben, R.; Erben, U.; Kühl, A.A.; Siegmund, B. T-cell Composition in Ileal and Colonic Creeping Fat. Separating Ileal from Colonic Crohn’s Disease. J. Crohns Colitis 2019, 13, 79–91. [Google Scholar] [CrossRef]
- Zhang, Y.; Si, X.; Yang, L.; Wang, H.; Sun, Y.; Liu, N. Association between intestinal microbiota and inflammatory bowel disease. Anim. Model Exp. Med. 2022, 5, 311–322. [Google Scholar] [CrossRef]
- Andoh, A.; Nishida, A. Alteration of the Gut Microbiome in Inflammatory Bowel Disease. Digestion 2022, 1–8. [Google Scholar] [CrossRef]
- Gonçalves, P.; Magro, F.; Martel, F. Metabolic inflammation in inflammatory bowel disease: Crosstalk between adipose tissue and bowel. Inflamm. Bowel Dis. 2015, 21, 453–467. [Google Scholar] [CrossRef] [PubMed]
- Wan, Y.; Zhang, D.; Xing, T.; Liu, Q.; Chi, Y.; Zhang, H.; Qian, H. The impact of visceral obesity on chronic constipation, inflammation, immune function and cognitive function in patients with inflammatory bowel disease. Aging 2021, 13, 6702–6711. [Google Scholar] [CrossRef] [PubMed]
- Sheehan, A.L.; Warren, B.F.; Gear, M.W.; Shepherd, N.A. Fat-wrapping in Crohn’s disease: Pathological basis and relevance to surgical practice. Br. J. Surg. 1992, 79, 955–958. [Google Scholar] [CrossRef] [PubMed]
- Uko, V.; Vortia, E.; Achkar, J.P.; Karakas, P.; Fiocchi, C.; Worley, S.; Kay, M.H. Impact of abdominal visceralmadipose tissue on disease outcome in pediatric Crohn’s disease. Inflamm. Bowel Dis. 2014, 20, 2286–2291. [Google Scholar] [CrossRef]
- Erhayiem, B.; Dhingsa, R.; Hawkey, C.J.; Subramanian, V. Ratio of visceral to subcutaneous fat area is a biomarker of complicated Crohn’s disease. Clin. Gastroenterol. Hepatol. 2011, 9, 684–687. [Google Scholar] [CrossRef]
- Van Der Sloot, K.W.; Joshi, A.D.; Bellavance, D.R.; Gilpin, K.K.; Stewart, K.O.; Lochhead, P.; Garber, J.J.; Giallourakis, C.; Yajnik, V.; Ananthakrishnan, A.N.; et al. Visceral Adiposity, Genetic Susceptibility, and Risk of Complications Among Individuals with Crohn’s Disease. Inflamm. Bowel Dis. 2017, 23, 82–88. [Google Scholar] [CrossRef]
- Frivolt, K.; Hetterich, H.; Schwerd, T.; Hajji, M.S.; Bufler, P.; Coppenrath, E.; Koletzko, S. Increase of Intra-abdominal Adipose Tissue in Pediatric Crohn Disease. J. Pediatr. Gastroenterol. Nutr. 2017, 65, 633–638. [Google Scholar] [CrossRef]
- Connelly, T.M.; Juza, R.M.; Sangster, W.; Sehgal, R.; Tappouni, R.F.; Messaris, E. Volumetric fat ratio and not body mass index is predictive of ileocolectomy outcomes in Crohn’s disease patients. Dig. Surg. 2014, 31, 219–224. [Google Scholar] [CrossRef]
- Li, Y.; Zhu, W.; Zuo, L.; Shen, B. The Role of the Mesentery in Crohn’s Disease: The Contributions of Nerves, Vessels, Lymphatics, and Fat to the Pathogenesis and Disease Course. Inflamm. Bowel Dis. 2016, 22, 1483–1495. [Google Scholar] [CrossRef] [PubMed]
- Osterman, M.T.; Kundu, R.; Lichtenstein, G.R.; Lewis, J.D. Association of 6-thioguanine nucleotide levels and inflammatory bowel disease activity: A meta-analysis. Gastroenterology 2006, 130, 1047–1053. [Google Scholar] [CrossRef] [PubMed]
- Holt, D.Q.; Strauss, B.J.; Moore, G.T. Weight and Body Composition Compartments do Not Predict Therapeutic Thiopurine Metabolite Levels in Inflammatory Bowel Disease. Clin. Transl. Gastroenterol. 2016, 7, e199. [Google Scholar] [CrossRef] [PubMed]
- Bassi, M.; Singh, S. Impact of Obesity on Response to Biologic Therapies in Patients with Inflammatory Bowel Diseases. BioDrugs 2022, 36, 197–203. [Google Scholar] [CrossRef]
- Levine, L.J.; Gaidos, J.K.J.; Proctor, D.D.; Viana, A.V.; Al-Bawardy, B. Effect of obesity on vedolizumab response in inflammatory bowel disease. Ann. Gastroenterol. 2022, 35, 275–280. [Google Scholar] [CrossRef]
- Kurnool, S.; Nguyen, N.H.; Proudfoot, J.; Dulai, P.S.; Boland, B.S.; Vande Casteele, N.; Evans, E.; Grunvald, E.L.; Zarrinpar, A.; Sandborn, W.; et al. High body mass index is associated with increased risk of treatment failure and surgery in biologic-treated patients with ulcerative colitis. Aliment. Pharmacol. Ther. 2018, 47, 1472–1479. [Google Scholar] [CrossRef]
- Singh, S.; Proudfoot, J.; Xu, R.; Sandborn, W. Obesity and Response to Infliximab in Patients with Inflammatory Bowel Diseases: Pooled Analysis of Individual Participant Data from Clinical Trials. Am. J. Gastroenterol. 2018, 113, 883–889. [Google Scholar] [CrossRef]
- Shen, W.; Cao, L.; Li, Y.; Cai, X.; Ge, Y.; Zhu, W. Visceral fat is Associated with Mucosal Healing of Infliximab Treatment in Crohn’s Disease. Dis. Colon Rectum 2018, 61, 706–712. [Google Scholar] [CrossRef]
- Lodhia, N.; Rao, S. Updates in therapeutic drug monitoring in inflammatory bowel disease. World J. Gastroenterol. 2022, 28, 2282–2290. [Google Scholar] [CrossRef] [PubMed]
- Rowan, C.R.; McManus, J.; Boland, K.; O’Toole, A. Visceral adiposity and inflammatory bowel disease. Int. J. Colorectal Dis. 2021, 36, 2305–2319. [Google Scholar] [CrossRef]
- Stromsnes, K.; Correas, A.G.; Lehmann, J.; Gambini, J.; Olaso-Gonzalez, G. Anti-Inflammatory Properties of Diet: Role in Healthy Aging. Biomedicines 2021, 9, 922. [Google Scholar] [CrossRef] [PubMed]
- Szilagyi, A. Relationship(s) between obesity and inflammatory bowel diseases: Possible intertwined pathogenic mechanisms. Clin. J. Gastroenterol. 2020, 13, 139–152. [Google Scholar] [CrossRef] [PubMed]
- Ramos, G.P.; Papadakis, K.A. Mechanisms of disease: Inflammatory bowel diseases. Mayo Clin.Clin. Proc. 2019, 94, 155–165. [Google Scholar] [CrossRef]
- Pilarczyk-Zurek, M.; Strus, M.; Adamski, P.; Heczko, P.B. The dual role of Escherichia coli in the course of ulcerative colitis. BMC Gastroenterol. 2016, 16, 128. [Google Scholar] [CrossRef] [PubMed]
- Hall, A.B.; Yassour, M.; Sauk, J.; Garner, A.; Jiang, X.; Arthur, T.; Lagoudas, G.K.; Vatanen, T.; Fornelos, N.; Wilson, R.; et al. A novel Ruminococcus gnavus clade enriched in inflammatory bowel disease patients. Genome Med. 2017, 9, 103. [Google Scholar] [CrossRef] [PubMed]
- Bischoff, S.C.; Barazzoni, R.; Busetto, L.; Campmans-Kuijpers, M.; Cardinale, V.; Chermesh, I.; Eshraghian, A.; Kani, H.T.; Khannoussi, W.; Lacaze, L.; et al. European guideline on obesity care in patients with gastrointestinal and liver diseases. Joint European Society for Clinical Nutrition and Metabolism/United European Gastroenterology guideline. United Eur. Gastroenterol. J. 2022, 10, 663–720. [Google Scholar] [CrossRef]
- Bertani, L.; Ribaldone, D.G.; Bellini, M.; Mumolo, M.G.; Costa, F. Inflammatory Bowel Diseases: Is There a Role for Nutritional Suggestions? Nutrients 2021, 13, 1387. [Google Scholar] [CrossRef]
- Bodini, G.; Zanella, C.; Crespi, M.; Lo Pumo, S.; Demarzo, M.G.; Savarino, E.; Savarino, V.; Giannini, E.G. A randomized, 6-wk trial of a low FODMAP diet in patients with inflammatory bowel disease. Nutrition 2019, 67–68, 110542. [Google Scholar] [CrossRef]
- Cox, S.R.; Prince, A.C.; Myers, C.E.; Irving, P.M.; Lindsay, J.O.; Lomer, M.C.; Whelan, K. Fermentable Carbohydrates [FODMAPs] Exacerbate Functional Gastrointestinal Symptoms in Patients with Inflammatory Bowel Disease: A Randomised, Double-blind, Placebo-controlled, Cross-over, Re-challenge Trial. J. Crohn’s Colitis 2017, 11, 1420–1429. [Google Scholar] [CrossRef]
- Cox, S.R.; Lindsay, J.O.; Fromentin, S.; Stagg, A.J.; McCarthy, N.E.; Galleron, N.; Ibraim, S.B.; Roume, H.; Levenez, F.; Pons, N.; et al. Effects of Low FODMAP Diet on Symptoms, Fecal Microbiome, and Markers of Inflammation in Patients with Quiescent Inflammatory Bowel Disease in a Randomized Trial. Gastroenterology 2020, 158, 176–188. [Google Scholar] [CrossRef]
- Peng, Z.; Yi, J.; Liu, X. A Low-FODMAP Diet Provides Benefits for Functional Gastrointestinal Symptoms but Not for Improving Stool Consistency and Mucosal Inflammation in IBD: A Systematic Review and Meta-Analysis. Nutrients 2022, 14, 2072. [Google Scholar] [CrossRef]
- Simões, C.D.; Maganinho, M.; Sousa, A.S. FODMAPs, inflammatory bowel disease and gut microbiota: Updated overview on the current evidence. Eur. J. Nutr. 2022, 61, 1187–1198. [Google Scholar] [CrossRef] [PubMed]
- Peyrin-Biroulet, L.; Chamaillard, M.; Gonzalez, F.; Beclin, E.; Decourcelle, C.; Antunes, L.; Gay, J.; Neut, C.; Colombel, J.F.; Desreumaux, P. Mesenteric fat in Crohn’s disease. A pathogenetic hallmark or an innocent bystander? Gut 2007, 56, 577–583. [Google Scholar] [CrossRef] [PubMed]
- Lefterova, M.I.; Haakonsson, A.K.; Lazar, M.A.; Mandrup, S. PPAR and the Global Map of Adipogenesis and Beyond. Trends Endocrinol. Metab. 2014, 25, 293–302. [Google Scholar] [CrossRef] [PubMed]
- Peyrin-Biroulet, L.; Beisner, J.; Wang, G.; Nuding, S.; Oommen, S.T.; Kelly, D.; Parmentier-Decrucq, E.; Dessein, R.; Merour, E.; Chavatte, P.; et al. Peroxisome proliferator-activated receptor gamma activation is required for maintenance of innate antimicrobial immunity in the colon. Proc. Natl. Acad. Sci. USA 2010, 107, 8772–8777. [Google Scholar] [CrossRef]
- Annese, V.; Rogai, F.; Settesoldi, A.; Bagnoli, S. PPAR in Inflammatory Bowel Disease. PPAR Res. 2012, 2012, 620839. [Google Scholar] [CrossRef]
- Torres, J.; Danese, S.; Colombel, J.F. New therapeutic avenues in ulcerative colitis: Thinking out of the box. Gut 2013, 62, 1642–1652. [Google Scholar] [CrossRef] [Green Version]
- Celinski, K.; Dworzanski, T.; Fornal, R.; Korolczuk, A.; Madro, A.; Brzozowski, T.; Slomka, M. Comparison of anti-inflammatory properties of peroxisome proliferator-activated receptor gamma agonists rosiglitazone and troglitazone in prophylactic treatment of experimental colitis. J. Physiol. Pharmacol. 2013, 64, 587–595. [Google Scholar]
- Lewis, J.D.; Lichtenstein, G.R.; Deren, J.J.; Sands, B.E.; Hanauer, S.B.; Katz, J.A.; Lashner, B.; Present, D.H.; Chuai, S.; Ellenberg, J.H.; et al. Rosiglitazone for active ulcerative colitis: A randomized placebo-controlled trial. Gastroenterology 2008, 134, 688–695. [Google Scholar] [CrossRef]
- Rosen, C.J. Revisiting the rosiglitazone story-lessons learned. N. Engl. J. Med. 2010, 363, 803–806. [Google Scholar] [CrossRef]
- Pirat, C.; Farce, A.; Lebegue, N.; Renault, N.; Furman, C.; Millet, R.; Yous, S.; Speca, S.; Berthelot, P.; Desreumaux, P.; et al. Targeting peroxisome proliferator-activated receptors (PPARs): Development of modulators. J. Med. Chem. 2012, 55, 4027–4061. [Google Scholar] [CrossRef] [PubMed]
- Speca, S.; Rousseaux, C.; Dubuquoy, C.; Rieder, F.; Vetuschi, A.; Sferra, R.; Giusti, I.; Bertin, B.; Dubuquoy, L.; Gaudio, E.; et al. Novel PPARgamma Modulator GED-0507-34 Levo Ameliorates Inflammation-driven Intestinal Fibrosis. Inflamm. Bowel Dis. 2016, 22, 279–292. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Michalak, A.; Kasztelan-Szczerbińska, B.; Cichoż-Lach, H. Impact of Obesity on the Course of Management of Inflammatory Bowel Disease—A Review. Nutrients 2022, 14, 3983. https://doi.org/10.3390/nu14193983
Michalak A, Kasztelan-Szczerbińska B, Cichoż-Lach H. Impact of Obesity on the Course of Management of Inflammatory Bowel Disease—A Review. Nutrients. 2022; 14(19):3983. https://doi.org/10.3390/nu14193983
Chicago/Turabian StyleMichalak, Agata, Beata Kasztelan-Szczerbińska, and Halina Cichoż-Lach. 2022. "Impact of Obesity on the Course of Management of Inflammatory Bowel Disease—A Review" Nutrients 14, no. 19: 3983. https://doi.org/10.3390/nu14193983