Exploring the Role of Adipose Tissue Dysregulation in Vitiligo Pathogenesis: A Body Composition Analysis
DOI:
https://doi.org/10.2340/actadv.v104.41018Keywords:
adipokines, adipose tissue, body composition analysis, dual-energy X-ray absorptiometry, vitiligoAbstract
Vitiligo is a commonly acquired pigmentary disease characterized by the progressive destruction of melanocytes. The role of adipose tissue in vitiligo remains unclear. To investigate the role of adipose tissue in the pathogenesis of vitiligo, 50 patients newly diagnosed with vitiligo and 40 age- and sex-matched healthy controls were enrolled, and fat mass and distribution using dual-energy X-ray absorptiometry (DXA) and serum adipokine levels using enzyme-linked immunosorbent assay were assessed. The trunk and whole-body fat mass and the trunk/limb fat mass ratio were significantly higher in patients with vitiligo. Higher leptin and resistin levels and lower adiponectin levels were observed. Positive correlation of the trunk fat mass index with vitiligo area scoring index scores (r = 0.38, p = 0.0071) was found. Additionally, plasma adiponectin levels were negatively correlated with vitiligo disease activity scores (r = –0.307, p < 0.05). Receiver operating characteristic curve analysis showed that the percentage of limb lean tissue mass, trunk/limb fat mass ratio, and serum adipokine levels achieved a high area under the curve score for distinguishing patients with vitiligo from healthy controls. In conclusion, the incidence of central obesity and adipokine dysregulation was higher in patients with vitiligo. The potential role of adipose tissue in the pathogenesis of vitiligo should be emphasized.
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Ezzedine K, Eleftheriadou V, Whitton M, van Geel N. Vitiligo. Lancet 2015; 386: 74-84.
https://doi.org/10.1016/S0140-6736(14)60763-7 DOI: https://doi.org/10.1016/S0140-6736(14)60763-7
Chen J, Li S, Li C. Mechanisms of melanocyte death in vitiligo. Med Res Rev 2021; 41: 1138-1166.
https://doi.org/10.1002/med.21754 DOI: https://doi.org/10.1002/med.21754
Gandhi K, Ezzedine K, Anastassopoulos KP, Patel R, Sikirica V, Daniel SR, et al. Prevalence of vitiligo among adults in the United States. JAMA Dermatol 2022; 158: 43-50.
https://doi.org/10.1001/jamadermatol.2021.4724 DOI: https://doi.org/10.1001/jamadermatol.2021.4724
Krüger C, Schallreuter KU. A review of the worldwide prevalence of vitiligo in children/adolescents and adults. Int J Dermatol 2012; 51: 1206-1212.
https://doi.org/10.1111/j.1365-4632.2011.05377.x DOI: https://doi.org/10.1111/j.1365-4632.2011.05377.x
Taneja K, Taneja J, Kaur C, Patel S, Haldar D. Lipid risk factors in vitiligo: homocysteine the connecting link? Clin Lab 2020; 66.
https://doi.org/10.7754/Clin.Lab.2020.200120 DOI: https://doi.org/10.7754/Clin.Lab.2020.200120
Kammeyer A, Willemsen KJ, Ouwerkerk W, Bakker WJ, Ratsma D, Pronk SD, et al. Mechanism of action of 4-substituted phenols to induce vitiligo and antimelanoma immunity. Pigment Cell Melanoma Res 2019; 32: 540-552.
https://doi.org/10.1111/pcmr.12774 DOI: https://doi.org/10.1111/pcmr.12774
Li S, Zhu G, Yang Y, Jian Z, Guo S, Dai W, et al. Oxidative stress drives CD8+ T-cell skin trafficking in patients with vitiligo through CXCL16 upregulation by activating the unfolded protein response in keratinocytes. J Allergy Clin Immunol 2017; 140: 177-189.e9.
https://doi.org/10.1016/j.jaci.2016.10.013 DOI: https://doi.org/10.1016/j.jaci.2016.10.013
Sahoo A, Lee B, Boniface K, Seneschal J, Sahoo SK, Seki T, et al. MicroRNA-211 regulates oxidative phosphorylation and energy metabolism in human vitiligo. J Invest Dermatol 2017; 137: 1965-1974.
https://doi.org/10.1016/j.jid.2017.04.025 DOI: https://doi.org/10.1016/j.jid.2017.04.025
Tavoletti G, Avallone G, Conforti C, Roccuzzo G, Maronese CA, Mattioli MA et al. Topical ruxolitinib: a new treatment for vitiligo. J Eur Acad Dermatol Venereol 2023; 37: 2222-2230.
https://doi.org/10.1111/jdv.19162 DOI: https://doi.org/10.1111/jdv.19162
Tanacan E, Atakan N. Higher incidence of metabolic syndrome components in vitiligo patients: a prospective cross-sectional study. An Bras Dermatol 2020; 95: 165-172.
https://doi.org/10.1016/j.abd.2019.07.006 DOI: https://doi.org/10.1016/j.abd.2019.07.006
Ye Z, Chen J, Du P, Ni Q, Li B, Zhang Z, et al. Metabolomics signature and potential application of serum polyunsaturated fatty acids metabolism in patients with vitiligo. Front Immunol 2022; 13: 839167.
https://doi.org/10.3389/fimmu.2022.839167 DOI: https://doi.org/10.3389/fimmu.2022.839167
Wu M, Wang L, Wu H, Yang M, He Z, Chen Y, et al. Leptin deficiency in CD8+ T cells ameliorates non-segmental vitiligo by reducing interferon-γ and granzyme B. Front Immunol 2023; 14: 1158883.
https://doi.org/10.3389/fimmu.2023.1158883 DOI: https://doi.org/10.3389/fimmu.2023.1158883
De A, Choudhary N, Sil A, Sarda A, Hasanoor Raja AH. A cross-sectional study of the levels of cytokines IL-6, TNF-α, and IFN-γ in blood and skin (lesional and uninvolved) of vitiligo patients and their possible role as biomarkers. Indian J Dermatol 2023; 68: 67-72.
https://doi.org/10.4103/ijd.ijd_27_22 DOI: https://doi.org/10.4103/ijd.ijd_27_22
Zhou SS, Li D, Zhou YM, Cao JM. The skin function: a factor of anti-metabolic syndrome. Diabetol Metab Syndr 2012; 4: 15.
https://doi.org/10.1186/1758-5996-4-15 DOI: https://doi.org/10.1186/1758-5996-4-15
Unamuno X, Gómez-Ambrosi J, Rodríguez A, Becerril S, Frühbeck G, Catalán V. Adipokine dysregulation and adipose tissue inflammation in human obesity. Eur J Clin Investig 2018; 48: e12997.
https://doi.org/10.1111/eci.12997 DOI: https://doi.org/10.1111/eci.12997
Polito R, Nigro E, Messina A, Monaco ML, Monda V, Scudiero O, et al. Adiponectin and orexin-a as a potential immunity link between adipose tissue and central nervous system. Front Physiol 2018; 9: 982.
https://doi.org/10.3389/fphys.2018.00982 DOI: https://doi.org/10.3389/fphys.2018.00982
Versini M, Jeandel PY, Rosenthal E, Shoenfeld Y. Obesity in autoimmune diseases: not a passive bystander. Autoimmun Rev 2014; 13: 981-1000.
https://doi.org/10.1016/j.autrev.2014.07.001 DOI: https://doi.org/10.1016/j.autrev.2014.07.001
Sterry W, Strober BE, Menter A, International Psoriasis Council. Obesity in psoriasis: the metabolic, clinical and therapeutic implications. Report of an interdisciplinary conference and review. Br J Dermatol 2007; 157: 649-655.
https://doi.org/10.1111/j.1365-2133.2007.08068.x DOI: https://doi.org/10.1111/j.1365-2133.2007.08068.x
Wong Y, Nakamizo S, Tan KJ, Kabashima K. An update on the role of adipose tissues in psoriasis. Front Immunol 2019; 10: 1507.
https://doi.org/10.3389/fimmu.2019.01507 DOI: https://doi.org/10.3389/fimmu.2019.01507
Han B, Wu WH, Bae JM, Son SJ, Lee JH, Han TY. Serum leptin and adiponectin levels in atopic dermatitis (AD) and their relation to disease severity. J Am Acad Dermatol 2016; 75: 629-631.
https://doi.org/10.1016/j.jaad.2016.04.036 DOI: https://doi.org/10.1016/j.jaad.2016.04.036
Kyriakou A, Patsatsi A, Sotiriadis D, Goulis DG. Serum leptin, resistin, and adiponectin concentrations in psoriasis: a meta-analysis of observational studies. Dermatology 2017; 233: 378-389.
https://doi.org/10.1159/000481882 DOI: https://doi.org/10.1159/000481882
Mahieu MA, Ramsey-Goldman R. Candidate biomarkers for fatigue in systemic lupus erythematosus: a critical review. Curr Rheumatol Rev 2017; 13: 103-112.
https://doi.org/10.2174/1573397112666161029224953 DOI: https://doi.org/10.2174/1573397112666161029224953
Dragoni F, Conti R, Cazzaniga S, Colucci R, Pisaneschi L, Naldi L, et al. No association between vitiligo and obesity: a case-control study. Med Princ Pract 2017; 26: 421-426.
https://doi.org/10.1159/000481436 DOI: https://doi.org/10.1159/000481436
Rodríguez-Martín M, de Paz NM, Mehtani P, Ferrer PC, Eliche MP, Martín BR, et al. Patients with vitiligo present fewer cardiovascular risk factors: results from a case-control study. J Eur Acad Dermatol Venereol 2013; 27: 124-125.
https://doi.org/10.1111/j.1468-3083.2011.04392.x DOI: https://doi.org/10.1111/j.1468-3083.2011.04392.x
Messina C, Albano D, Gitto S, Tofanelli L, Bazzocchi A, Ulivieri FM, et al. Body composition with dual energy X-ray absorptiometry: from basics to new tools. Quant Imaging Med Surg 2020; 10: 1687-1698.
https://doi.org/10.21037/qims.2020.03.02 DOI: https://doi.org/10.21037/qims.2020.03.02
Komen L, da Graça V, Wolkerstorfer A, de Rie MA, Terwee CB, van der Veen JP. Vitiligo Area Scoring Index and Vitiligo European Task Force assessment: reliable and responsive instruments to measure the degree of depigmentation in vitiligo. Br J Dermatol 2015; 172: 437-443.
https://doi.org/10.1111/bjd.13432 DOI: https://doi.org/10.1111/bjd.13432
He K, Wu W, Wang X, Dai W, Wang S, Li C, et al. Circulatory levels of alarmins in patients with non-segmental vitiligo: potential biomarkers for disease diagnosis and activity/severity assessment. Front Immunol 2022; 13: 1069196.
https://doi.org/10.3389/fimmu.2022.1069196 DOI: https://doi.org/10.3389/fimmu.2022.1069196
Hotamisligil GS, Shargill NS, Spiegelman BM. Adipose expression of tumor necrosis factor-alpha: direct role in obesity-inked insulin resistance. Science 1993; 259: 87-91.
https://doi.org/10.1126/science.7678183 DOI: https://doi.org/10.1126/science.7678183
Kang YE, Kim JM, Joung KH, Lee JH, You BR, Choi MJ, et al. The roles of adipokines, proinflammatory cytokines, and adipose tissue macrophages in obesity-associated insulin resistance in modest obesity and early metabolic dysfunction. PLoS One 2016; 11: e0154003.
https://doi.org/10.1371/journal.pone.0154003 DOI: https://doi.org/10.1371/journal.pone.0154003
Ouchi N, Parker JL, Lugus JJ, Walsh K. Adipokines in inflammation and metabolic disease. Nat Rev Immunol 2011; 11: 85-97.
https://doi.org/10.1038/nri2921 DOI: https://doi.org/10.1038/nri2921
Ibrahim S, El-Tahlawi S, Mogawer RM, El Ansary M, Esmat S, El-Hawary M. Different vitiligo characteristics as predictors of increased risk of metabolic syndrome and insulin resistance: a case-control study. J Cosmet Dermatol 2022; 21: 7170-7177.
https://doi.org/10.1111/jocd.15446 DOI: https://doi.org/10.1111/jocd.15446
Kang P, Zhang WG, Ji ZH, Shao ZJ, Li CY. Association between vitiligo and relevant components of metabolic syndrome: a systematic review and meta-analysis. J Dtsch Dermatol Ges 2022; 20: 629-641.
https://doi.org/10.1111/ddg.14717 DOI: https://doi.org/10.1111/ddg.14717
El-Hawary M, El-Tahlawi S, Ibrahim S, El Ansary M, Mogawer RM. Possible enigmatic link between serum leptin and vitiligo with its metabolic derangements: a comparative controlled study. J Cosmet Dermatol 2022; 21: 2971-2976.
https://doi.org/10.1111/jocd.14490 DOI: https://doi.org/10.1111/jocd.14490
Lauria MW, Moreira LM, Machado-Coelho GL, Neto RM, Soares MM, Ramos AV. Ability of body mass index to predict abnormal waist circumference: receiving operating characteristics analysis. Diabetol Metab Syndr 2013; 5: 74.
https://doi.org/10.1186/1758-5996-5-74 DOI: https://doi.org/10.1186/1758-5996-5-74
Flegal KM, Shepherd JA, Looker AC, Graubard BI, Borrud LG, Ogden CL, et al. Comparisons of percentage body fat, body mass index, waist circumference, and waist-stature ratio in adults. Am J Clin Nutr 2009; 89: 500-508.
https://doi.org/10.3945/ajcn.2008.26847 DOI: https://doi.org/10.3945/ajcn.2008.26847
Lukaski HC. Soft tissue composition and bone mineral status: evaluation by dual-energy X-ray absorptiometry. J Nutr 1993; 123: 438-443.
https://doi.org/10.1093/jn/123.suppl_2.438 DOI: https://doi.org/10.1093/jn/123.suppl_2.438
Swainson MG, Batterham AM, Tsakirides C, Rutherford ZH, Hind K. Prediction of whole-body fat percentage and visceral adipose tissue mass from five anthropometric variables. PLoS One 2017; 12: e0177175.
https://doi.org/10.1371/journal.pone.0177175 DOI: https://doi.org/10.1371/journal.pone.0177175
Zhang L, Yang XQ, Cheng J, Hui RS, Gao TW. Increased Th17 cells are accompanied by FoxP3(+) Treg cell accumulation and correlated with psoriasis disease severity. Clin Immunol 2010; 135: 108-117.
https://doi.org/10.1016/j.clim.2009.11.008 DOI: https://doi.org/10.1016/j.clim.2009.11.008
Zhang K, Guo Y, Ge Z, Zhang Z, Da Y, Li W, et al. Adiponectin suppresses T helper 17 cell differentiation and limits autoimmune CNS inflammation via the SIRT1/PPARγ/RORγt pathway. Mol Neurobiol 2017; 54: 4908-4920.
https://doi.org/10.1007/s12035-016-0036-7 DOI: https://doi.org/10.1007/s12035-016-0036-7
Surendar J, Frohberger SJ, Karunakaran I, Schmitt V, Stamminger W, Neumann AL, et al. Adiponectin limits IFN-γ and IL-17 producing CD4 T cells in obesity by restraining cell intrinsic glycolysis. Front Immunol 2019; 10: 2555.
https://doi.org/10.3389/fimmu.2019.02555 DOI: https://doi.org/10.3389/fimmu.2019.02555
Takahashi H, Honma M, Ishida-Yamamoto A, Iizuka H. Adiponectin and leptin modulate cell proliferation and cytokine secretion of normal human keratinocytes and T lymphocytes. J Dermatol Sci 2010; 59: 143-145.
https://doi.org/10.1016/j.jdermsci.2010.06.004 DOI: https://doi.org/10.1016/j.jdermsci.2010.06.004
Aryanian Z, Shirzadian A, Farzaneh S, Goodarzi A, Azizpour A, Hatami P. Metabolic derangement in patients with vitiligo: a cross-sectional study. J Investig Med 2022; 70: 963-966.
https://doi.org/10.1136/jim-2021-002062 DOI: https://doi.org/10.1136/jim-2021-002062
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