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Current Pharmaceutical Design

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ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

General Review Article

Circulating Insulin-like Growth Factor-1 Levels in Patients with Rheumatoid Arthritis: A Meta-analysis

Author(s): Yu-Lan Zhao, Jun Wu, Tian-Ping Zhang, Qian-Yao Cheng, Xue-Ping Wang, Ming-Ming Gu, Hai-Feng Pan and Dong-Qing Ye*

Volume 25, Issue 10, 2019

Page: [1091 - 1098] Pages: 8

DOI: 10.2174/1381612825666190319124009

Price: $65

Abstract

Background and Objectives: Insulin-like growth factor-1 (IGF-1) levels have been investigated in rheumatoid arthritis (RA), however, produced inconsistent results. The purpose of this meta-analysis was to derive a more precise conclusion about serum/plasma IGF-1 levels in RA patients.

Methods: PubMed, Embase and the Cochrane Library databases were searched up to December 2018 in English, and the studies comparing serum/plasma IGF-1 levels between RA group and healthy control group were what we are interested in. The Newcastle-Ottawa Scale (NOS) was used to assess the methodological quality of the included studies. The heterogeneity test was performed by the Cochrane Q statistic and I2 –statistic. The publication bias was evaluated by the funnel plot and Egger’s test. The standard mean difference (SMD) with 95% confidence interval (CI) was calculated by the fixed-effects or random-effects model.

Results: A total of eleven articles with 334 cases and 261 controls were finally included. Compared with the healthy group, the RA group had lower circulating IGF-1 levels (pooled SMD= -0.936, 95% CI= -1.382 to -0.489, p<0.001). The subgroup analysis showed that RA patients from Asia (SMD= -0.645, 95% CI= -1.063 to -0.228, p= 0.002) and Europe (SMD= -1.131, 95% CI= -1.767 to -0.495, p<0.001) had lower circulating IGF-1 levels, no significant difference in plasma/serum IGF-1 levels was observed in RA patients from America. Sensitivity analysis indicated the stability and credibility of the overall effect sizes.

Conclusion: Patients with RA have lower circulating IGF-1 level than healthy controls, particularly for patients from Asia and Europe. Further studies are necessary to elucidate the role of IGF-1 in the pathological process of RA.

Keywords: Insulin-like growth factor-1, Rheumatoid arthritis, Autoimmune diseases, Meta-analysis, Cytokine, Pathogenesis.

[1]
Scott DL, Wolfe F, Huizinga TW. Rheumatoid arthritis. Lancet 2010; 376(9746): 1094-108.
[http://dx.doi.org/10.1016/S0140-6736(10)60826-4] [PMID: 20870100]
[2]
Orr C, Vieira-Sousa E, Boyle DL, et al. Synovial tissue research: a state-of-the-art review. Nat Rev Rheumatol 2017; 13(8): 463-75.
[http://dx.doi.org/10.1038/nrrheum.2017.115] [PMID: 28701760]
[3]
van der Helm-van Mil AH, Wesoly JZ, Huizinga TW. Understanding the genetic contribution to rheumatoid arthritis. Curr Opin Rheumatol 2005; 17(3): 299-304.
[http://dx.doi.org/10.1097/01.bor.0000160780.13012.be] [PMID: 15838240]
[4]
Andersson KME, Wasen C, Juzokaite L, et al. Inflammation in the hippocampus affects IGF1 receptor signaling and contributes to neurological sequelae in rheumatoid arthritis 2018; 115: E12063-72.
[http://dx.doi.org/10.1073/pnas.1810553115]
[5]
Lee SD, Chen LM, Kuo WW, et al. Serum insulin-like growth factor-axis and matrix metalloproteinases in patients with rheumatic arthritis or rheumatic heart disease. Clin Chim Acta 2006; 367(1-2): 62-8.
[http://dx.doi.org/10.1016/j.cca.2005.11.015] [PMID: 16406300]
[6]
Olejnik A, Franczak A, Krzywonos-Zawaazka A, Kaluzna-Oleksy M. Iwona-Bil-Lula. Biological Role of Klotho Protein in the Development of Cardiovascular Diseases. BioMed Res Int 2018; 20185171945.
[7]
Clemmons DR. Metabolic actions of insulin-like growth factor-I in normal physiology and diabetes. Endocrinol Metab Clin North Am 2012; 41(2): 425-43.
[PMID: 22682639]
[8]
Kooijman R, Hooghe-Peters EL, Hooghe R. Prolactin, growth hormone, and insulin-like growth factor-I in the immune system. Adv Immunol 1996; 63: 377-454.
[http://dx.doi.org/10.1016/S0065-2776(08)60860-3] [PMID: 8787635]
[9]
Heemskerk VH, Daemen MA, Buurman WA. Insulin-like growth factor-1 (IGF-1) and growth hormone (GH) in immunity and inflammation. Cytokine Growth Factor Rev 1999; 10(1): 5-14.
[http://dx.doi.org/10.1016/S1359-6101(98)00022-7] [PMID: 10379908]
[10]
Verschure PJ, Van Noorden CJ, Van Marle J, Van den Berg WB. Articular cartilage destruction in experimental inflammatory arthritis: insulin-like growth factor-1 regulation of proteoglycan metabolism in chondrocytes. Histochem J 1996; 28(12): 835-57.
[http://dx.doi.org/10.1007/BF02331388] [PMID: 9015706]
[11]
McQuillan DJ, Handley CJ, Campbell MA, Bolis S, Milway VE, Herington AC. Stimulation of proteoglycan biosynthesis by serum and insulin-like growth factor-I in cultured bovine articular cartilage. Biochem J 1986; 240(2): 423-30.
[http://dx.doi.org/10.1042/bj2400423] [PMID: 3545187]
[12]
Doré S, Pelletier JP, DiBattista JA, Tardif G, Brazeau P, Martel-Pelletier J. Human osteoarthritic chondrocytes possess an increased number of insulin-like growth factor 1 binding sites but are unresponsive to its stimulation. Possible role of IGF-1-binding proteins. Arthritis Rheum 1994; 37(2): 253-63.
[http://dx.doi.org/10.1002/art.1780370215] [PMID: 7510486]
[13]
Sakurai H, Kohsaka H, Liu MF, et al. Nitric oxide production and inducible nitric oxide synthase expression in inflammatory arthritides. J Clin Invest 1995; 96(5): 2357-63.
[http://dx.doi.org/10.1172/JCI118292] [PMID: 7593623]
[14]
Dey P, Panga V, Raghunathan S. A Cytokine Signalling Network for the Regulation of Inducible Nitric Oxide Synthase Expression in Rheumatoid Arthritis. PLoS One 2016; 11(9): e0161306.
[http://dx.doi.org/10.1371/journal.pone.0161306] [PMID: 27626941]
[15]
Aktan F. iNOS-mediated nitric oxide production and its regulation. Life Sci 2004; 75(6): 639-53.
[http://dx.doi.org/10.1016/j.lfs.2003.10.042] [PMID: 15172174]
[16]
Cannon GW, Openshaw SJ, Hibbs JB Jr, Hoidal JR, Huecksteadt TP, Griffiths MM. Nitric oxide production during adjuvant-induced and collagen-induced arthritis. Arthritis Rheum 1996; 39(10): 1677-84.
[http://dx.doi.org/10.1002/art.1780391010] [PMID: 8843858]
[17]
Palma Zochio Tozzato G, Taipeiro EF, Spadella MA, et al. Collagen-induced arthritis increases inducible nitric oxide synthase not only in aorta but also in the cardiac and renal microcirculation of mice. Clin Exp Immunol 2016; 183(3): 341-9.
[http://dx.doi.org/10.1111/cei.12728] [PMID: 26456019]
[18]
Bolduc JA, Collins JA, Loeser RF. Reactive oxygen species, aging and articular cartilage homeostasis. Free Radic Biol Med 2019; 132: 73-82.
[http://dx.doi.org/10.1016/j.freeradbiomed.2018.08.038] [PMID: 30176344]
[19]
Lotz M. The role of nitric oxide in articular cartilage damage. Rheum Dis Clin North Am 1999; 25(2): 269-82.
[http://dx.doi.org/10.1016/S0889-857X(05)70067-3] [PMID: 10356417]
[20]
Mazzetti I, Grigolo B, Pulsatelli L, et al. Differential roles of nitric oxide and oxygen radicals in chondrocytes affected by osteoarthritis and rheumatoid arthritis. Clin Sci (Lond) 2001; 101(6): 593-9.
[http://dx.doi.org/10.1042/cs1010593] [PMID: 11724645]
[21]
van de Loo FA, Arntz OJ, van Enckevort FH, van Lent PL, van den Berg WB. Reduced cartilage proteoglycan loss during zymosan-induced gonarthritis in NOS2-deficient mice and in anti-interleukin-1-treated wild-type mice with unabated joint inflammation. Arthritis Rheum 1998; 41(4): 634-46.
[http://dx.doi.org/10.1002/1529-0131(199804)41:4<634:AID-ART10>3.0.CO;2-1] [PMID: 9550472]
[22]
van den Berg WB, van de Loo F, Joosten LA, Arntz OJ. Animal models of arthritis in NOS2-deficient mice. Osteoarthritis Cartilage 1999; 7(4): 413-5.
[http://dx.doi.org/10.1053/joca.1999.0228] [PMID: 10419784]
[23]
Isenovic ER, Meng Y, Divald A, Milivojevic N, Sowers JR. Role of phosphatidylinositol 3-kinase/Akt pathway in angiotensin II and insulin-like growth factor-1 modulation of nitric oxide synthase in vascular smooth muscle cells. Endocrine 2002; 19(3): 287-92.
[http://dx.doi.org/10.1385/ENDO:19:3:287] [PMID: 12624428]
[24]
Jin C, Guo J, Qiu X, et al. IGF-1 induces iNOS expression via the p38 MAPK signal pathway in the anti-apoptotic process in pulmonary artery smooth muscle cells during PAH. J Recept Signal Transduct Res 2014; 34(4): 325-31.
[http://dx.doi.org/10.3109/10799893.2014.903417] [PMID: 24673524]
[25]
Baker JF, Von Feldt JM, Mostoufi-Moab S, Kim W, Taratuta E, Leonard MB. Insulin-like Growth Factor 1 and Adiponectin and Associations with Muscle Deficits, Disease Characteristics, and Treatments in Rheumatoid Arthritis. J Rheumatol 2015; 42(11): 2038-45.
[http://dx.doi.org/10.3899/jrheum.150280] [PMID: 26329340]
[26]
Boström EA, Svensson M, Andersson S, et al. Resistin and insulin/insulin-like growth factor signaling in rheumatoid arthritis. Arthritis Rheum 2011; 63(10): 2894-904.
[http://dx.doi.org/10.1002/art.30527] [PMID: 21739426]
[27]
Stanilova SA, Ivanova MG, Karakolev IA, Stoilov RM, Rashkov RK, Manolova IM. Association of +3179G/A insulin-like growth factor-1 receptor polymorphism and insulin-like growth factor-1 serum level with systemic lupus erythematosus. Lupus 2013; 22(13): 1388-93.
[http://dx.doi.org/10.1177/0961203313502860] [PMID: 23989734]
[28]
Suzuki S, Morimoto S, Fujishiro M, et al. Inhibition of the insulin-like growth factor system is a potential therapy for rheumatoid arthritis. Autoimmunity 2015; 48(4): 251-8.
[http://dx.doi.org/10.3109/08916934.2014.976631] [PMID: 25352179]
[29]
Denko CW, Malemud CJ. Role of the growth hormone/insulin-like growth factor-1 paracrine axis in rheumatic diseases. Semin Arthritis Rheum 2005; 35(1): 24-34.
[http://dx.doi.org/10.1016/j.semarthrit.2005.03.001] [PMID: 16084221]
[30]
Engvall IL, Elkan AC, Tengstrand B, Cederholm T, Brismar K, Hafstrom I. Cachexia in rheumatoid arthritis is associated with inflammatory activity, physical disability, and low bioavailable insulin-like growth factor. Scand J Rheumatol 2008; 37(5): 321-8.
[http://dx.doi.org/10.1080/03009740802055984] [PMID: 18666027]
[31]
Wells G, Shea BJ, O’Connell D, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of non-randomized studies in meta-analysis. The Ottawa Hospital Research Institute 2014; pp. 1-4.
[32]
Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med 2002; 21(11): 1539-58.
[http://dx.doi.org/10.1002/sim.1186] [PMID: 12111919]
[33]
Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ 2003; 327(7414): 557-60.
[http://dx.doi.org/10.1136/bmj.327.7414.557] [PMID: 12958120]
[34]
Mantel N, Haenszel W. Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst 1959; 22(4): 719-48.
[PMID: 13655060]
[35]
DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986; 7(3): 177-88.
[http://dx.doi.org/10.1016/0197-2456(86)90046-2] [PMID: 3802833]
[36]
Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997; 315(7109): 629-34.
[http://dx.doi.org/10.1136/bmj.315.7109.629] [PMID: 9310563]
[37]
Denko CW, Boja B, Moskowitz RW. Growth factors, insulin-like growth factor-1 and growth hormone, in synovial fluid and serum of patients with rheumatic disorders. Osteoarthritis Cartilage 1996; 4(4): 245-9.
[http://dx.doi.org/10.1016/S1063-4584(05)80102-5] [PMID: 11048621]
[38]
Fernihough JK, Billingham ME, Cwyfan-Hughes S, Holly JM. Local disruption of the insulin-like growth factor system in the arthritic joint. Arthritis Rheum 1996; 39(9): 1556-65.
[http://dx.doi.org/10.1002/art.1780390916] [PMID: 8814068]
[39]
Davies UM, Jones J, Reeve J, et al. Juvenile rheumatoid arthritis. Effects of disease activity and recombinant human growth hormone on insulin-like growth factor 1, insulin-like growth factor binding proteins 1 and 3, and osteocalcin. Arthritis Rheum 1997; 40(2): 332-40.
[http://dx.doi.org/10.1002/art.1780400218] [PMID: 9041945]
[40]
Lemmey A, Maddison P, Breslin A, et al. Association between insulin-like growth factor status and physical activity levels in rheumatoid arthritis. J Rheumatol 2001; 28(1): 29-34.
[PMID: 11196538]
[41]
Neidel J. Changes in systemic levels of insulin-like growth factors and their binding proteins in patients with rheumatoid arthritis. Clin Exp Rheumatol 2001; 19(1): 81-4.
[PMID: 11247331]
[42]
Denko CW, Malemud CJ. The serum growth hormone to somatostatin ratio is skewed upward in rheumatoid arthritis patients. Front Biosci 2004; 9: 1660-4.
[http://dx.doi.org/10.2741/1354] [PMID: 14977577]
[43]
Ishigami S, Nakajima A, Tanno M, Matsuzaki T, Suzuki H, Yoshino S. Effects of mirthful laughter on growth hormone, IGF-1 and substance P in patients with rheumatoid arthritis. Clin Exp Rheumatol 2005; 23(5): 651-7.
[PMID: 16173241]
[44]
Häkkinen A, Pakarinen A, Hannonen P, et al. Effects of prolonged combined strength and endurance training on physical fitness, body composition and serum hormones in women with rheumatoid arthritis and in healthy controls. Clin Exp Rheumatol 2005; 23(4): 505-12.
[PMID: 16095120]
[45]
Toussirot E, Nguyen NU, Dumoulin G, Aubin F, Cédoz JP, Wendling D. Relationship between growth hormone-IGF-I-IGFBP-3 axis and serum leptin levels with bone mass and body composition in patients with rheumatoid arthritis. Rheumatology (Oxford) 2005; 44(1): 120-5.
[http://dx.doi.org/10.1093/rheumatology/keh421] [PMID: 15466894]
[46]
Kurtais Y, Tur BS, Elhan AH, Erdogan MF, Yalçin P. Hypothalamic-pituitary-adrenal hormonal responses to exercise stress test in patients with rheumatoid arthritis compared to healthy controls. J Rheumatol 2006; 33(8): 1530-7.
[PMID: 16881110]
[47]
Blackman MR, Muniyappa R, Wilson M, et al. Diurnal secretion of growth hormone, cortisol, and dehydroepiandrosterone in pre- and perimenopausal women with active rheumatoid arthritis: a pilot case-control study. Arthritis Res Ther 2007; 9(4): R73.
[http://dx.doi.org/10.1186/ar2271] [PMID: 17662149]
[48]
Walsh PT, Smith LM, O’Connor R. Insulin-like growth factor-1 activates Akt and Jun N-terminal kinases (JNKs) in promoting the survival of T lymphocytes. Immunology 2002; 107(4): 461-71.
[http://dx.doi.org/10.1046/j.1365-2567.2002.01525.x] [PMID: 12460191]
[49]
Himpe E, Degaillier C, Coppens A, Kooijman R. Insulin-like growth factor-1 delays Fas-mediated apoptosis in human neutrophils through the phosphatidylinositol-3 kinase pathway. J Endocrinol 2008; 199(1): 69-80.
[http://dx.doi.org/10.1677/JOE-08-0028] [PMID: 18653623]
[50]
Isaacs JD. Therapeutic T-cell manipulation in rheumatoid arthritis: past, present and future. Rheumatology (Oxford) 2008; 47(10): 1461-8.
[http://dx.doi.org/10.1093/rheumatology/ken163] [PMID: 18503092]
[51]
Weigent DA. Lymphocyte GH-axis hormones in immunity. Cell Immunol 2013; 285(1-2): 118-32.
[http://dx.doi.org/10.1016/j.cellimm.2013.10.003] [PMID: 24177252]
[52]
Osta B, Benedetti G, Miossec P. Classical and Paradoxical Effects of TNF-α on Bone Homeostasis. Front Immunol 2014; 5: 48.
[http://dx.doi.org/10.3389/fimmu.2014.00048] [PMID: 24592264]
[53]
Szeremeta A, Olczyk K. Tumor necrosis factor α antagonists in the treatment of the patients with rheumatoid arthritis. Reumatologia 2012; 5: 438-43.
[http://dx.doi.org/10.5114/reum.2012.31407]
[54]
O’Connor JC, McCusker RH, Strle K, Johnson RW, Dantzer R, Kelley KW. Regulation of IGF-I function by proinflammatory cytokines: at the interface of immunology and endocrinology. Cell Immunol 2008; 252(1-2): 91-110.
[http://dx.doi.org/10.1016/j.cellimm.2007.09.010] [PMID: 18325486]
[55]
Frost RA, Lang CH. Alteration of somatotropic function by proinflammatory cytokines. J Anim Sci 2004; 82(E-Suppl): E100-109.
[56]
van den Berg WB. The role of cytokines and growth factors in cartilage destruction in osteoarthritis and rheumatoid arthritis. Z Rheumatol 1999; 58(3): 136-41.
[http://dx.doi.org/10.1007/s003930050163] [PMID: 10441840]

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