Do Cytokines Associate Periodontitis with Metabolic Disorders? An
Overview of Current Documents

Reza      Aref Nezhad; Hossein      Motedayyen; Hossein      Roghani-Shahraki
doi:10.2174/1871530322666220119112026
Abstract

Periodontitis is an oral chronic inflammatory condition affecting the adult population worldwide. Many microorganisms act as initiators for inducing inflammatory immune responses, which participate in the destruction of connective tissue surrounding the teeth, thereby resulting in tooth loss. Cytokines may have indispensable roles in its pathogenesis by enhancing inflammatory and immune responses. Cytokines can affect the functions of some cells of different tissues, such as the cells of the pancreas, liver, and adipose tissues. Evidence suggests that periodontitis is associated with metabolic disorders like liver cirrhosis, obesity, and diabetes mellitus. Hence, this review focused on determining how cytokines can participate in the correlation of periodontitis with metabolic disorders.
Keywords: Periodontitis, inflammatory cytokines, liver cirrhosis, obesity, diabetes mellitus, metabolic disorders.
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Graphical Abstract

[1] 
Grossi, S.G.; Genco, R.J. Periodontal disease and diabetes mellitus: A two-way relationship. Ann. Periodontol.,  1998, 3(1), 51-61.
[http://dx.doi.org/10.1902/annals.1998.3.1.51] [PMID: 9722690] 
[2] 
Sattari, M.; Taheri, R.A. ArefNezhad, R.; Motedayyen, H. The expression levels of MicroRNA-146a, RANKL and OPG after non-surgical periodontal treatment. BMC Oral Health,  2021, 21(1), 1-7.
[http://dx.doi.org/10.1186/s12903-021-01883-8] [PMID: 33388028] 
[3] 
Fenesy, K.E. Periodontal disease: An overview for physicians. Mt. Sinai J. Med.,  1998, 65(5-6), 362-369.
[PMID: 9844364] 
[4] 
Eke, P.I.; Dye, B.A.; Wei, L.; Thornton-Evans, G.O.; Genco, R.J. Prevalence of periodontitis in adults in the United States: 2009 and 2010. J. Dent. Res.,  2012, 91(10), 914-920.
[http://dx.doi.org/10.1177/0022034512457373] [PMID: 22935673] 
[5] 
Nahid, M.A.; Rivera, M.; Lucas, A.; Chan, E.K.; Kesavalu, L. Polymicrobial infection with periodontal pathogens specifically enhances microRNA miR-146a in ApoE-/- mice during experimental periodontal disease. Infect. Immun.,  2011, 79(4), 1597-1605.
[http://dx.doi.org/10.1128/IAI.01062-10] [PMID: 21263019] 
[6] 
Motedayyen, H.; Ghotloo, S.; Saffari, M.; Sattari, M.; Amid, R. Evaluation of microRNA‐146a and its targets in gingival tissues of patients with chronic periodontitis. J. Periodontol.,  2015, 86(12), 1380-1385.
[http://dx.doi.org/10.1902/jop.2015.150319] [PMID: 26313020] 
[7] 
Popova, C.; Mlachkova, A. Gingival tissue Il-1β and pge2 levels in patients with chronic periodontitis after additional therapy with non-steroidal anti-inflammatory drugs. J IMAB.,  2010, 16(4), 27-30.
[http://dx.doi.org/10.5272/jimab.1642010_27-30] 
[8] 
Xie, Y.F.; Shu, R.; Jiang, S.Y.; Liu, D.L.; Zhang, X.L. Comparison of microRNA profiles of human periodontal diseased and healthy gingival tissues. Int. J. Oral Sci.,  2011, 3(3), 125-134.
[http://dx.doi.org/10.4248/IJOS11046] [PMID: 21789961] 
[9] 
Ramadan, D.E.; Hariyani, N.; Indrawati, R.; Ridwan, R.D.; Diyatri, I. Cytokines and chemokines in periodontitis. Eur. J. Dent.,  2020, 14(3), 483-495.
[http://dx.doi.org/10.1055/s-0040-1712718] [PMID: 32575137] 
[10] 
Di Benedetto, A.; Gigante, I.; Colucci, S.; Grano, M. Periodontal disease: linking the primary inflammation to bone loss. Clinical and Developmental Immunology,  2013, 2013, 503754.
[http://dx.doi.org/10.1155/2013/503754] 
[11] 
Wang, C; Guan, Y; Yang, J Cytokines in the progression of pancreatic β-cell dysfunction. International journal of endocrinology,  2010, 2010
[12] 
Niederreiter, L.; Tilg, H. Cytokines and fatty liver diseases. Liver Res.,  2018, 2(1), 14-20.
[http://dx.doi.org/10.1016/j.livres.2018.03.003] 
[13] 
Tavares, C.O.; Rost, F.L.; Silva, R.B.M.; Dagnino, A.P.; Adami, B.; Schirmer, H.; de Figueiredo, J.A.P.; Souto, A.A.; Maito, F.D.M.; Campos, M.M. Cross talk between apical periodontitis and metabolic disorders: experimental evidence on the role of intestinal adipokines and Akkermansia muciniphila. J. Endod.,  2019, 45(2), 174-180.
[http://dx.doi.org/10.1016/j.joen.2018.10.013] [PMID: 30711174] 
[14] 
Costa, F.O.; Lages, E.J.P.; Lages, E.M.B.; Cota, L.O.M. Periodontitis in individuals with liver cirrhosis: A case-control study. J. Clin. Periodontol.,  2019, 46(10), 991-998.
[http://dx.doi.org/10.1111/jcpe.13172] [PMID: 31336404] 
[15] 
Gulati, N.N.; Masamatti, S.S.; Chopra, P. Association between obesity and its determinants with chronic periodontitis: A cross-sectional study. J. Indian Soc. Periodontol.,  2020, 24(2), 167-172.
[http://dx.doi.org/10.4103/jisp.jisp_157_19] [PMID: 32189846] 
[16] 
Preshaw, P.M.; Alba, A.L.; Herrera, D.; Jepsen, S.; Konstantinidis, A.; Makrilakis, K.; Taylor, R. Periodontitis and diabetes: A two-way relationship. Diabetologia,  2012, 55(1), 21-31.
[http://dx.doi.org/10.1007/s00125-011-2342-y] [PMID: 22057194] 
[17] 
Deo, V.; Bhongade, M. Pathogenesis of periodontitis: role of cytokines in host response. Dentistry today,  2010, 29(9), 60-62.
[18] 
Graves, D.T.; Cochran, D. The contribution of interleukin-1 and tumor necrosis factor to periodontal tissue destruction. J. Periodontol.,  2003, 74(3), 391-401.
[http://dx.doi.org/10.1902/jop.2003.74.3.391] [PMID: 12710761] 
[19] 
Zeytun, A; Chaudhary, A; Pardington, P; Cary, RB; Gupta, G Induction of cytokines and chemokines by toll-like receptor signaling: strategies for control of infammation. Critical Reviews™ in Immunology,  2010, 30(1), 53-67.
[http://dx.doi.org/10.1615/CritRevImmunol.v30.i1.40] 
[20] 
Sabroe, I.; Parker, L.; Dower, S.; Whyte, M. The role of TLR activation in inflammation. J. Pathol.,  2008, 214(2), 126-135.
[http://dx.doi.org/10.1002/path.2264] 
[21] 
Kantarci, A.; Van Dyke, T.E. Neutrophil-mediated host response to Porphyromonas gingivalis. J. Int. Acad. Periodontol.,  2002, 4(4), 119-125.
[PMID: 12670091] 
[22] 
Gurav, A.N. Periodontitis and insulin resistance: casual or causal relationship? Diabetes Metab. J.,  2012, 36(6), 404-411.
[http://dx.doi.org/10.4093/dmj.2012.36.6.404] [PMID: 23275933] 
[23] 
Waddington, R.J.; Moseley, R.; Embery, G. Reactive oxygen species: A potential role in the pathogenesis of periodontal diseases. Oral Dis.,  2000, 6(3), 138-151.
[http://dx.doi.org/10.1111/j.1601-0825.2000.tb00325.x] [PMID: 10822357] 
[24] 
Ghotloo, S.; Motedayyen, H.; Amani, D.; Saffari, M.; Sattari, M. Assessment of microRNA-146a in generalized aggressive periodontitis and its association with disease severity. J. Periodontal Res.,  2019, 54(1), 27-32.
[http://dx.doi.org/10.1111/jre.12538] [PMID: 30328616] 
[25] 
Stashenko, P.; Dewhirst, F.E.; Peros, W.J.; Kent, R.L.; Ago, J.M. Synergistic interactions between interleukin 1, tumor necrosis factor, and lymphotoxin in bone resorption. J. Immunol.,  1987, 138(5), 1464-1468.
[PMID: 3492553] 
[26] 
Gilbert, L.; He, X.; Farmer, P.; Boden, S.; Kozlowski, M.; Rubin, J.; Nanes, M.S. Inhibition of osteoblast differentiation by tumor necrosis factor-α Endocrinology,  2000, 141(11), 3956-3964.
[http://dx.doi.org/10.1210/endo.141.11.7739] [PMID: 11089525] 
[27] 
Brunetti, G.; Colucci, S.; Pignataro, P.; Coricciati, M.; Mori, G.; Cirulli, N.; Zallone, A.; Grassi, F.R.; Grano, M. T cells support osteoclastogenesis in an in vitro model derived from human periodontitis patients. J. Periodontol.,  2005, 76(10), 1675-1680.
[http://dx.doi.org/10.1902/jop.2005.76.10.1675] [PMID: 16253089] 
[28] 
Mogi, M.; Otogoto, J.; Ota, N.; Togari, A. Differential expression of RANKL and osteoprotegerin in gingival crevicular fluid of patients with periodontitis. J. Dent. Res.,  2004, 83(2), 166-169.
[http://dx.doi.org/10.1177/154405910408300216] [PMID: 14742657] 
[29] 
Öngöz Dede, F. Gökmenoğlu, C.; Deveci, E.T.; Çelen, S.; Avci, B.; Kara, C.; Çanakçi, V. Increased levels of interleukin-32 isoforms alpha, beta, gamma, and delta in the gingival crevicular fluid and plasma of the patients with periodontitis. J. Periodontal Res.,  2021, 56(1), 83-92.
[http://dx.doi.org/10.1111/jre.12796] [PMID: 32890410] 
[30] 
Tymkiw, K.D.; Thunell, D.H.; Johnson, G.K.; Joly, S.; Burnell, K.K.; Cavanaugh, J.E.; Brogden, K.A.; Guthmiller, J.M. Influence of smoking on gingival crevicular fluid cytokines in severe chronic periodontitis. J. Clin. Periodontol.,  2011, 38(3), 219-228.
[http://dx.doi.org/10.1111/j.1600-051X.2010.01684.x] [PMID: 21198766] 
[31] 
Dutzan, N.; Vernal, R.; Vaque, J.P.; García-Sesnich, J.; Hernandez, M.; Abusleme, L.; Dezerega, A.; Gutkind, J.S.; Gamonal, J. Interleukin-21 expression and its association with proinflammatory cytokines in untreated chronic periodontitis patients. J. Periodontol.,  2012, 83(7), 948-954.
[http://dx.doi.org/10.1902/jop.2011.110482] [PMID: 22181687] 
[32] 
Jing, L.; Kim, S.; Sun, L.; Wang, L.; Mildner, E.; Divaris, K.; Jiao, Y.; Offenbacher, S. IL-37-and IL-35/IL-37-producing plasma cells in chronic periodontitis. J. Dent. Res.,  2019, 98(7), 813-821.
[http://dx.doi.org/10.1177/0022034519847443] [PMID: 31050915] 
[33] 
Kim, J-Y.; Kim, H-N. Changes in inflammatory cytokines in saliva after non-surgical periodontal therapy: a systematic review and meta-analysis. Int. J. Environ. Res. Public Health,  2020, 18(1), 194.
[http://dx.doi.org/10.3390/ijerph18010194] [PMID: 33383828] 
[34] 
Mazurek-Mochol, M.; Kozak, M.; Malinowski, D.; Safranow, K.; Pawlik, A. IL-17F Gene rs763780 and IL-17A rs2275913 Polymorphisms in Patients with Periodontitis. Int. J. Environ. Res. Public Health,  2021, 18(3), 1081.
[http://dx.doi.org/10.3390/ijerph18031081] [PMID: 33530501] 
[35] 
Palanivel, R.; Maida, A.; Liu, Y.; Sweeney, G. Regulation of insulin signalling, glucose uptake and metabolism in rat skeletal muscle cells upon prolonged exposure to resistin. Diabetologia,  2006, 49(1), 183-190.
[http://dx.doi.org/10.1007/s00125-005-0060-z] [PMID: 16341686] 
[36] 
Chavey, C.; Fajas, L. CXCL5 drives obesity to diabetes, and further. Aging (Albany NY),  2009, 1(7), 674-677.
[http://dx.doi.org/10.18632/aging.100064] [PMID: 20157549] 
[37] 
Gieling, R.G.; Wallace, K.; Han, Y-P. Interleukin-1 participates in the progression from liver injury to fibrosis. Am. J. Physiol. Gastrointest. Liver Physiol.,  2009, 296(6), G1324-G1331.
[http://dx.doi.org/10.1152/ajpgi.90564.2008] [PMID: 19342509] 
[38] 
Daniluk, J.; Szuster-Ciesielska, A.; Drabko, J. Kandefer-Szerszeń M. Serum cytokine levels in alcohol-related liver cirrhosis. Alcohol,  2001, 23(1), 29-34.
[http://dx.doi.org/10.1016/S0741-8329(00)00134-8] [PMID: 11282449] 
[39] 
Ataseven, H.; Bahcecioglu, I.; Kuzu, N. The levels of ghrelin, leptin, TNF-. Mediators Inflamm.,  2006, 4, 78380.
[40] 
Król, K., Ed.; Reactive oxygen species and antioxidant mechanisms in the pathogenesis of periodontitis; Annales Academiae Medicae Stetinensis, 2004. 
[41] 
Wang, P.; Duan, D.; Zhou, X.; Li, X.; Yang, J.; Deng, M.; Xu, Y. Relationship between expression of human gingival beta-defensins and levels of periodontopathogens in subgingival plaque. J. Periodontal Res.,  2015, 50(1), 113-122.
[http://dx.doi.org/10.1111/jre.12187] [PMID: 24814979] 
[42] 
Ishikawa, I.; Cimasoni, G.; Ahmad-Zadeh, C. Possible role of lysosomal enzymes in the pathogenesis of periodontitis: A study on cathepsin D in human gingival fluid. Arch. Oral Biol.,  1972, 17(1), 111-117.
[http://dx.doi.org/10.1016/0003-9969(72)90138-0] [PMID: 4558389] 
[43] 
Kırzıoğlu, F.Y.; Fentoğlu, Ö.; Bulut, M.T.; Doğan, B.; Özdem, M.; Özmen, Ö.; Çarsancaklı, S.A.; Ergün, A.G.; Orhan, H. Is a cholestrolenriched diet a risk factor for alveolar bone loss? J. Periodontol.,  2016, 87(5), 529-538.
[http://dx.doi.org/10.1902/jop.2016.150509] [PMID: 26751342] 
[44] 
Sigusch, B.; Klinger, G.; Glockmann, E.; Simon, H.U. Early-onset and adult periodontitis associated with abnormal cytokine production by activated T lymphocytes. J. Periodontol.,  1998, 69(10), 1098-1104.
[http://dx.doi.org/10.1902/jop.1998.69.10.1098] [PMID: 9802707] 
[45] 
Voskresenskiĭ O.N.; Tkachenko, E.K. The role of lipid peroxidation in the pathogenesis of periodontitis. Stomatologia (Mosk.),  1991, (4), 5-10.
[PMID: 1780934] 
[46] 
Okui, T.; Aoki, Y.; Ito, H.; Honda, T.; Yamazaki, K. The presence of IL-17+/FOXP3+ double-positive cells in periodontitis. J. Dent. Res.,  2012, 91(6), 574-579.
[http://dx.doi.org/10.1177/0022034512446341] [PMID: 22522772] 
[47] 
Rajendran, M.; Looney, S.; Singh, N.; Elashiry, M.; Meghil, M.M.; El-Awady, A.R.; Tawfik, O.; Susin, C.; Arce, R.M.; Cutler, C.W. Systemic antibiotic therapy reduces circulating inflammatory dendritic cells and Treg–Th17 plasticity in periodontitis. J. Immunol.,  2019, 202(9), 2690-2699.
[http://dx.doi.org/10.4049/jimmunol.1900046] [PMID: 30944162] 
[48] 
Schuppan, D.; Afdhal, N.H. Liver cirrhosis. Lancet,  2008, 371(9615), 838-851.
[http://dx.doi.org/10.1016/S0140-6736(08)60383-9] [PMID: 18328931] 
[49] 
Ueki, T.; Kaneda, Y.; Tsutsui, H.; Nakanishi, K.; Sawa, Y.; Morishita, R.; Matsumoto, K.; Nakamura, T.; Takahashi, H.; Okamoto, E.; Fujimoto, J. Hepatocyte growth factor gene therapy of liver cirrhosis in rats. Nat. Med.,  1999, 5(2), 226-230.
[http://dx.doi.org/10.1038/5593] [PMID: 9930873] 
[50] 
Banerjee, M.; Saxena, M. Interleukin-1 (IL-1) family of cytokines: role in type 2 diabetes. Clin. Chim. Acta,  2012, 413(15-16), 1163-1170.
[http://dx.doi.org/10.1016/j.cca.2012.03.021] [PMID: 22521751] 
[51] 
Åberg, F.; Helenius-Hietala, J.; Meurman, J.; Isoniemi, H. Association between dental infections and the clinical course of chronic liver disease. Hepatol. Res.,  2014, 44(3), 349-353.
[http://dx.doi.org/10.1111/hepr.12126] [PMID: 23607641] 
[52] 
Esser, N.; Legrand-Poels, S.; Piette, J.; Scheen, A.J.; Paquot, N. Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res. Clin. Pract.,  2014, 105(2), 141-150.
[http://dx.doi.org/10.1016/j.diabres.2014.04.006] [PMID: 24798950] 
[53] 
Wiwanitkit, V.; Suwansaksri, N.; Suwansaksri, J. Causative agents of liver abscess in those with liver cirrhosis: A 10-year case review of hospitalized patients in Thailand. Ann. Trop. Med. Parasitol.,  2002, 96(5), 513-516.
[http://dx.doi.org/10.1179/000349802125001212] [PMID: 12194712] 
[54] 
Guarner, C.; Runyon, B.A. Macrophage function in cirrhosis and the risk of bacterial infection. Hepatology,  1995, 22(1), 367-369.
[http://dx.doi.org/10.1002/hep.1840220149] [PMID: 7601431] 
[55] 
Raghava, K.V.; Shivananda, H.; Mundinamane, D.; Boloor, V.; Thomas, B. Evaluation of periodontal status in alcoholic liver cirrhosis patients: A comparative study. J. Contemp. Dent. Pract.,  2013, 14(2), 179-182.
[http://dx.doi.org/10.5005/jp-journals-10024-1296] [PMID: 23811642] 
[56] 
Thomas, H.E.; Irawaty, W.; Darwiche, R.; Brodnicki, T.C.; Santamaria, P.; Allison, J.; Kay, T.W. IL-1 receptor deficiency slows progression to diabetes in the NOD mouse. Diabetes,  2004, 53(1), 113-121.
[http://dx.doi.org/10.2337/diabetes.53.1.113] [PMID: 14693705] 
[57] 
Movin, S. Relationship between periodontal disease and cirrhosis of the liver in humans. J. Clin. Periodontol.,  1981, 8(6), 450-458.
[http://dx.doi.org/10.1111/j.1600-051X.1981.tb00894.x] [PMID: 6949918] 
[58] 
Oettinger-Barak, O.; Barak, S.; Machtei, E.E.; Ardekian, L.; Baruch, Y.; Peled, M. Periodontal changes in liver cirrhosis and post-transplantation patients. I: clinical findings. J. Periodontol.,  2001, 72(9), 1236-1240.
[http://dx.doi.org/10.1902/jop.2000.72.9.1236] [PMID: 11577956] 
[59] 
Jaiswal, G.; Deo, V.; Bhongade, M.; Jaiswal, S. Serum alkaline phosphatase: A potential marker in the progression of periodontal disease in cirrhosis patients. Quintessence Int.,  2011, 42(4), 345-348.
[PMID: 21516281] 
[60] 
Alexandraki, K.; Piperi, C.; Kalofoutis, C.; Singh, J.; Alaveras, A.; Kalofoutis, A. Inflammatory process in type 2 diabetes: The role of cytokines. Ann. N. Y. Acad. Sci.,  2006, 1084(1), 89-117.
[http://dx.doi.org/10.1196/annals.1372.039] [PMID: 17151295] 
[61] 
Lu, J.; Liu, J.; Li, L.; Lan, Y.; Liang, Y. Cytokines in type 1 diabetes: mechanisms of action and immunotherapeutic targets. Clin. Transl. Immunology,  2020, 9(3), e1122.
[http://dx.doi.org/10.1002/cti2.1122] [PMID: 32185024] 
[62] 
Hasnain, S.Z.; Borg, D.J.; Harcourt, B.E.; Tong, H.; Sheng, Y.H.; Ng, C.P.; Das, I.; Wang, R.; Chen, A.C.; Loudovaris, T.; Kay, T.W.; Thomas, H.E.; Whitehead, J.P.; Forbes, J.M.; Prins, J.B.; McGuckin, M.A. Glycemic control in diabetes is restored by therapeutic manipulation of cytokines that regulate beta cell stress. Nat. Med.,  2014, 20(12), 1417-1426.
[http://dx.doi.org/10.1038/nm.3705] [PMID: 25362253] 
[63] 
Nonogaki, K.; Fuller, G.M.; Fuentes, N.L.; Moser, A.H.; Staprans, I.; Grunfeld, C.; Feingold, K.R. Interleukin-6 stimulates hepatic triglyceride secretion in rats. Endocrinology,  1995, 136(5), 2143-2149.
[http://dx.doi.org/10.1210/endo.136.5.7720663] [PMID: 7720663] 
[64] 
O’Rourke, R.W. Inflammation in obesity-related diseases. Surgery,  2009, 145(3), 255-259.
[http://dx.doi.org/10.1016/j.surg.2008.08.038] [PMID: 19231576] 
[65] 
Hino, K.; Nagata, H. Screening for adiponectin secretion regulators. Vitam. Horm.,  2012, 90, 125-141.
[http://dx.doi.org/10.1016/B978-0-12-398313-8.00005-1] [PMID: 23017714] 
[66] 
Arboleda, S.; Vargas, M.; Losada, S.; Pinto, A. Review of obesity and periodontitis: An epidemiological view. Br. Dent. J.,  2019, 227(3), 235-239.
[http://dx.doi.org/10.1038/s41415-019-0611-1] [PMID: 31399683] 
[67] 
Culebras-Atienza, E.; Silvestre, F-J.; Silvestre-Rangil, J. Possible association between obesity and periodontitis in patients with Down syndrome. Med. Oral Patol. Oral Cir. Bucal,  2018, 23(3), e335-e343.
[http://dx.doi.org/10.4317/medoral.22311] [PMID: 29680852] 
[68] 
Zuza, E.P.; Garcia, V.G.; Theodoro, L.H.; Ervolino, E.; Favero, L.F.V.; Longo, M.; Ribeiro, F.S.; Martins, A.T.; Spolidorio, L.C.; Zuanon, J.A.S.; de Toledo, B.E.C.; Pires, J.R. Influence of obesity on experimental periodontitis in rats: histopathological, histometric and immunohistochemical study. Clin. Oral Investig.,  2018, 22(3), 1197-1208.
[http://dx.doi.org/10.1007/s00784-017-2207-y] [PMID: 28929308] 
[69] 
Damanaki, A.; Memmert, S.; Nokhbehsaim, M.; Sanyal, A.; Gnad, T.; Pfeifer, A.; Deschner, J. Impact of obesity and aging on crestal alveolar bone height in mice. Ann. Anat.,  2018, 218, 227-235.
[http://dx.doi.org/10.1016/j.aanat.2018.04.005] [PMID: 29730468] 
[70] 
Perlstein, M.I.; Bissada, N.F. Influence of obesity and hypertension on the severity of periodontitis in rats. Oral Surg. Oral Med. Oral Pathol.,  1977, 43(5), 707-719.
[http://dx.doi.org/10.1016/0030-4220(77)90055-X] [PMID: 266151] 
[71] 
Sahukari, R.; Punabaka, J.; Bhasha, S.; Ganjikunta, V.S.; Ramudu, S.K.; Kesireddy, S.R. Plant Compounds for the Treatment of Diabetes, a Metabolic Disorder: NF-κB as a Therapeutic Target. Curr. Pharm. Des.,  2020, 26(39), 4955-4969.
[http://dx.doi.org/10.2174/1381612826666200730221035] [PMID: 32744961] 
[72] 
Prabhakar, P.K. Pathophysiology of secondary complications of diabetes mellitus. Pathophysiology,  2016, 9(1), 32-36.
[73] 
Jansson, H.; Lindholm, E.; Lindh, C.; Groop, L.; Bratthall, G. Type 2 diabetes and risk for periodontal disease: A role for dental health awareness. J. Clin. Periodontol.,  2006, 33(6), 408-414.
[http://dx.doi.org/10.1111/j.1600-051X.2006.00929.x] [PMID: 16677329] 
[74] 
Westfelt, E.; Rylander, H.; Blohmé, G.; Jonasson, P.; Lindhe, J. The effect of periodontal therapy in diabetics. Results after 5 years. J. Clin. Periodontol.,  1996, 23(2), 92-100.
[http://dx.doi.org/10.1111/j.1600-051X.1996.tb00540.x] [PMID: 8849844] 
[75] 
Dinarello, C.A. Proinflammatory cytokines. Chest,  2000, 118(2), 503-508.
[http://dx.doi.org/10.1378/chest.118.2.503] [PMID: 10936147] 
[76] 
Muche, A.A.; Olayemi, O.O.; Gete, Y.K. Prevalence and determinants of gestational diabetes mellitus in Africa based on the updated international diagnostic criteria: A systematic review and meta-analysis. Arch. Public Health,  2019, 77(1), 36.
[http://dx.doi.org/10.1186/s13690-019-0362-0] [PMID: 31402976] 
[77] 
Chaparro, A.; Zúñiga, E.; Varas-Godoy, M.; Albers, D.; Ramírez, V.; Hernández, M.; Kusanovic, J.P.; Acuña-Gallardo, S.; Rice, G.; Illanes, S.E. Periodontitis and placental growth factor in oral fluids are early pregnancy predictors of gestational diabetes mellitus. J. Periodontol.,  2018, 89(9), 1052-1060.
[http://dx.doi.org/10.1002/JPER.17-0497] [PMID: 29790168] 
[78] 
Chávarry, N.G.M.; Vettore, M.V.; Sansone, C.; Sheiham, A. The relationship between diabetes mellitus and destructive periodontal disease: A meta-analysis. Oral Health Prev. Dent.,  2009, 7(2), 107-127.
[PMID: 19583037] 
[79] 
Tack, C.J.; Stienstra, R.; Joosten, L.A.; Netea, M.G. Inflammation links excess fat to insulin resistance: the role of the interleukin-1 family. Immunol. Rev.,  2012, 249(1), 239-252.
[http://dx.doi.org/10.1111/j.1600-065X.2012.01145.x] [PMID: 22889226] 
[80] 
Khumaedi, A.I.; Purnamasari, D.; Wijaya, I.P.; Soeroso, Y. The relationship of diabetes, periodontitis and cardiovascular disease. Diabetes Metab. Syndr.,  2019, 13(2), 1675-1678.
[http://dx.doi.org/10.1016/j.dsx.2019.03.023] [PMID: 31336540] 
[81] 
Rabinovitch, A. An update on cytokines in the pathogenesis of insulin-dependent diabetes mellitus. Diabetes Metab. Rev.,  1998, 14(2), 129-151.
[http://dx.doi.org/10.1002/(SICI)1099-0895(199806)14:2<129:AID-DMR208>3.0.CO;2-V] [PMID: 9679667] 
[82] 
Rabinovitch, A.; Suarez-Pinzon, W.L. Role of cytokines in the pathogenesis of autoimmune diabetes mellitus. Rev. Endocr. Metab. Disord.,  2003, 4(3), 291-299.
[http://dx.doi.org/10.1023/A:1025160614313] [PMID: 14501180] 
[83] 
Martin, I.V.; Borkham-Kamphorst, E.; Zok, S.; van Roeyen, C.R.; Eriksson, U.; Boor, P.; Hittatiya, K.; Fischer, H.P.; Wasmuth, H.E.; Weiskirchen, R.; Eitner, F.; Floege, J.; Ostendorf, T. Platelet-derived growth factor (PDGF)-C neutralization reveals differential roles of PDGF receptors in liver and kidney fibrosis. Am. J. Pathol.,  2013, 182(1), 107-117.
[http://dx.doi.org/10.1016/j.ajpath.2012.09.006] [PMID: 23141925] 
[84] 
Zhou, W-C.; Zhang, Q-B.; Qiao, L. Pathogenesis of liver cirrhosis. World J. Gastroenterol.,  2014, 20(23), 7312-7324.
[http://dx.doi.org/10.3748/wjg.v20.i23.7312] [PMID: 24966602] 
[85] 
Ramadan, M.E.; Ramadan, M.E.E.; Yousef, M.S.M. Role of TNF alpha in schistosoma mansoni infection and cirrhotic liver. Int. J. Pharm. Med. Res.,  2013, 1(1), 6-12.
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DOI https://dx.doi.org/10.2174/1871530322666220119112026	Print ISSN 1871-5303
Publisher Name Bentham Science Publisher	Online ISSN 2212-3873
Endocrine, Metabolic & Immune Disorders - Drug Targets

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