4,680
Views
19
CrossRef citations to date
0
Altmetric
Original Article

Beneficial effects of natural eggshell membrane (NEM) on multiple indices of arthritis in collagen-induced arthritic rats

, , , ORCID Icon &
Pages 838-848 | Received 18 Aug 2016, Accepted 07 Nov 2016, Published online: 21 Dec 2016

References

  • Erickson AR, Cannella AC, Mikuls TR. Clinical features of rheumatoid arthritis. In: Firestein GS, Budd RC, Gabriel SE, McInnes IB, O’Dell JR, eds. Kelley and Firestein’s textbook of rheumatology. 10th ed. Philadelphia: Elsevier; 2016:1167–86.
  • Firestein GS. Etiology and pathogenesis of rheumatoid arthritis. In: Firestein GS, Budd RC, Gabriel SE, McInnes IB, O’Dell JR, eds. Kelley and Firestein’s textbook of rheumatology. 10th ed. Philadelphia: Elsevier; 2016:1115–66.e7.
  • Cross M, Smith E, Hoy D, Carmona L, Wolfe F, Vos T, et al. The global burden of rheumatoid arthritis: estimates from the global burden of disease 2010 study. Ann Rheum Dis. 2014;73:1316–22.
  • Gibofsky A. Overview of epidemiology, pathophysiology, and diagnosis of rheumatoid arthritis. Am J Manag Care. 2012;18:S295–S302.
  • Doran MF, Pond GR, Crowson CS, O’Fallon WM, Gabriel SE. Trends in incidence and mortality in rheumatoid arthritis in Rochester, Minnesota, over a forty-year period. Arthritis Rheum. 2002;46:625–31.
  • Zampeli E, Vlachoyiannopoulos PG, Tzioufas AG. Treatment of rheumatoid arthritis: unraveling the conundrum. J Autoimmun. 2015;65:1–18.
  • Finckh A, Bansback N, Marra CA, Anis AH, Michaud K, Lubin S, et al. Treatment of very early rheumatoid arthritis with symptomatic therapy, disease-modifying antirheumatic drugs, or biologic agents: a cost-effectiveness analysis. Ann Intern Med. 2009;151:612–21.
  • Rossi D, Modena V, Sciascia S, Roccatello D. Rheumatoid arthritis: biological therapy other than anti-TNF. Int Immunopharmacol. 2015;27:185–8.
  • Gupta SC, Patchva S, Aggarwal BB. Therapeutic roles of curcumin: lessons learned from clinical trials. AAPS J. 2013;15:195–218.
  • Rosenbaum CC, O’Mathuna DP, Chavez M, Shields K. Antioxidants and antiinflammatory dietary supplements for osteoarthritis and rheumatoid arthritis. Altern Ther Health Med. 2010;16:32–40.
  • Reed GW, Leung K, Rossetti RG, Vanbuskirk S, Sharp JT, Zurier RB. Treatment of rheumatoid arthritis with marine and botanical oils: an 18-month, randomized, and double-blind trial. Evid Based Complement Alternat Med. 2014;2014:857456.
  • Al-Nahain A, Jahan R, Rahmatullah M. Zingiber officinale: a potential plant against rheumatoid arthritis. Arthritis. 2014;2014:159089.
  • Trentham DE, Townes AS, Kang AH. Autoimmunity to type II collagen an experimental model of arthritis. J Exp Med. 1977;146:857–68.
  • Bendele A, McComb J, Gould T, McAbee T, Sennello G, Chlipala E, et al. Animal models of arthritis: relevance to human disease. Toxicol Pathol. 1999;27:134–42.
  • Bendele A. Animal models of rheumatoid arthritis. J Musculoskelet Neuronal Interact. 2001;1:377–85.
  • Bendele A, McAbee T, Sennello G, Frazier J, Chlipala E, McCabe D. Efficacy of sustained blood levels of interleukin-1 receptor antagonist in animal models of arthritis: comparison of efficacy in animal models with human clinical data. Arthritis Rheum. 1999;42:498–506.
  • Ruff KJ, DeVore DP, Leu MD, Robinson MA. Eggshell membrane: a possible new natural therapeutic for joint and connective tissue disorders. Results from two open-label human clinical studies. Clin Interv Aging. 2009;4:235–40.
  • Ruff KJ, Winkler A, Jackson RW, DeVore DP, Ritz BW. Eggshell membrane in the treatment of pain and stiffness from osteoarthritis of the knee: a randomized, multicenter, double-blind, placebo-controlled clinical study. Clin Rheumatol. 2009;28:907–14.
  • Danesch U, Seybold M, Rittinghausen R, Triebel W, Bitterlich N. NEM® brand eggshell membrane effective in the treatment of pain associated with knee and hip osteoarthritis: results from a six center, open label German clinical study. J Arthritis. 2014;3:1000136–41.
  • Brunello E, Masini A. NEM® brand eggshell membrane effective in the treatment of pain and stiffness associated with osteoarthritis of the knee in an Italian study population. Int J Clin Med. 2016;7:169–75.
  • Wedekind KJ, Coverdale JA, Hampton TR, Atwell CA, Sorbet RH, Lunnemann J, et al. Efficacy of an equine joint supplement, and the synergistic effect of its active ingredients (chelated trace minerals and natural eggshell membrane), as demonstrated in equine, swine, and an osteoarthritis rat model. Open Access Anim Physiol. 2015;7:1–15.
  • Dierenfeld ES, Baum D, Hampe L, Jensen J, Atwell C, Wedekind KJ. Evaluation of a nutraceutical joint supplement in camels (Camelus species). Am Holis Veterin Med Assoc J. 2014;36:59–66.
  • Bauer KL, Dierenfeld ES, Hartup BK. Evaluation of a nutraceutical joint supplement in cranes. Proc N Am Crane Workshop. 2014;12:27–32.
  • Ruff KJ, DeVore DP. Reduction of pro-inflammatory cytokines in rats following 7-day oral supplementation with a proprietary eggshell membrane-derived product. Mod Res Inflamm. 2014;3:19–25.
  • Sim BY, Bak JW, Lee HJ, Jun JA, Choi HJ, Kwon CJ, et al. Effects of natural eggshell membrane (NEM) on monosodium iodoacetate-induced arthritis in rats. J Nutr Health. 2015;48:310.
  • Committee for the Update of the Guide for the Care and Use of Laboratory Animals. Guide for the care and use of laboratory animals. 8th ed. Washington (DC): National Academies Press; 2011.
  • Cannella AC, O’Dell JR. Traditional DMARDs: methotrexate, leflunomide, sulfasalazine, hydroxychloroquinone, and combination therapies. In: Firestein GS, Budd RC, Gabriel SE, McInnes IB, O’Dell JR, eds. Kelley and Firestein’s textbook of rheumatology. 10th ed. Philadelphia: Elsevier; 2016:958–82.e7.
  • Reagan-Shaw S, Nihal M, Ahmad N. Dose translation from animal to human studies revisited. FASEB J. 2008;22:659–61.
  • Ruff KJ, Endres JR, Clewell AE, Szabo JR, Schauss AG. Safety evaluation of a natural eggshell membrane-derived product. Food Chem Toxicol. 2012;50:604–11.
  • Landewe RB, Geusens P, van der Heijde DM, Boers M, van der Linden SJ, Garnero P. Arthritis instantaneously causes collagen type I and type II degradation in patients with early rheumatoid arthritis: a longitudinal analysis. Ann Rheum Dis. 2006;65:40–4.
  • Young-Min S, Cawston T, Marshall N, Coady D, Christgau S, Saxne T, et al. Biomarkers predict radiographic progression in early rheumatoid arthritis and perform well compared with traditional markers. Arthritis Rheum. 2007;56:3236–47.
  • Landewe RB, Geusens P, Boers M, van der Heijde D, Lems W, te KJ, et al. Markers for type II collagen breakdown predict the effect of disease-modifying treatment on long-term radiographic progression in patients with rheumatoid arthritis. Arthritis Rheum. 2004;50:1390–9.
  • Rousseau JC, Delmas PD. Biological markers in osteoarthritis. Nat Clin Pract Rheumatol. 2007;3:346–56.
  • Valdes AM, Meulenbelt I, Chassaing E, Arden NK, Bierma-Zeinstra S, Hart D, et al. Large scale meta-analysis of urinary C-terminal telopeptide, serum cartilage oligomeric protein and matrix metalloprotease degraded type II collagen and their role in prevalence, incidence and progression of osteoarthritis. Osteoarthritis Cartil. 2014;22:683–9.
  • Saxne T, Heinegard D. Cartilage oligomeric matrix protein: a novel marker of cartilage turnover detectable in synovial fluid and blood. Br J Rheumatol. 1992;31:583–91.
  • Morozzi G, Fabbroni M, Bellisai F, Pucci G, Galeazzi M. Cartilage oligomeric matrix protein level in rheumatic diseases: potential use as a marker for measuring articular cartilage damage and/or the therapeutic efficacy of treatments. Ann N Y Acad Sci. 2007;1108:398–407.
  • Tseng S, Reddi AH, Di Cesare PE. Cartilage oligomeric matrix protein (COMP): a biomarker of arthritis. Biomark Insights. 2009;4:33–44.
  • Andersson ML, Svensson B, Petersson IF, Hafstrom I, Albertsson K, Forslind K, et al. Early increase in serum-COMP is associated with joint damage progression over the first five years in patients with rheumatoid arthritis. BMC Musculoskelet Disord. 2013;14:229.
  • Skoumal M, Kolarz G, Klingler A. Serum levels of cartilage oligomeric matrix protein. A predicting factor and a valuable parameter for disease management in rheumatoid arthritis. Scand J Rheumatol. 2003;32:156–61.
  • Crnkic M, Mansson B, Larsson L, Geborek P, Heinegard D, Saxne T. Serum cartilage oligomeric matrix protein (COMP) decreases in rheumatoid arthritis patients treated with infliximab or etanercept. Arthritis Res Ther. 2003;5:R181–5.
  • Kawashiri SY, Kawakami A, Ueki Y, Imazato T, Iwamoto N, Fujikawa K, et al. Decrement of serum cartilage oligomeric matrix protein (COMP) in rheumatoid arthritis (RA) patients achieving remission after 6 months of etanercept treatment: comparison with CRP, IgM-RF, MMP-3 and anti-CCP Ab. Joint Bone Spine. 2010;77:418–20.
  • Yamamoto M, Takahashi H, Ohara M, Suzuki C, Naishiro Y, Yamamoto H, et al. Evidence of cartilaginous benefit of treatment with infliximab in rheumatoid arthritis using measurement of serum COMP. Nihon Rinsho Meneki Gakkai Kaishi. 2007;30:41–7.
  • Skoumal M, Haberhauer G, Feyertag J, Kittl EM, Bauer K, Dunky A. Serum levels of cartilage oligomeric matrix protein (COMP): a rapid decrease in patients with active rheumatoid arthritis undergoing intravenous steroid treatment. Rheumatol Int. 2006;26:1001–4.
  • Rehman AA, Ahsan H, Khan FH. α-2-Macroglobulin: a physiological guardian. J Cell Physiol. 2013;228:1665–75.
  • Tchetverikov I, Verzijl N, Huizinga TW, TeKoppele JM, Hanemaaijer R, DeGroot J. Active MMPs captured by alpha 2 macroglobulin as a marker of disease activity in rheumatoid arthritis. Clin Exp Rheumatol. 2003;21:711–8.
  • Wu SM, Pizzo SV. alpha(2)-Macroglobulin from rheumatoid arthritis synovial fluid: functional analysis defines a role for oxidation in inflammation. Arch Biochem Biophys. 2001;391:119–26.
  • Zapico I, Coto E, Rodriguez A, Alvarez C, Torre JC, Alvarez V. A DNA polymorphism at the alpha2-macroglobulin gene is associated with the severity of rheumatoid arthritis. J Rheumatol. 2000;27:2308–11.
  • Cavalli G, Dinarello CA. Treating rheumatological diseases and co-morbidities with interleukin-1 blocking therapies. Rheumatology (Oxford). 2015;54:2134–44.
  • Mertens M, Singh JA. Anakinra for rheumatoid arthritis: a systematic review. J Rheumatol. 2009;36:1118–25.
  • Vincent TL, Williams RO, Maciewicz R, Silman A, Garside P. Mapping pathogenesis of arthritis through small animal models. Rheumatology (Oxford). 2012;51:1931–41.
  • Haleagrahara N, Swaminathan M, Chakravarthi S, Radhakrishnan A. Therapeutic efficacy of vitamin E δ-tocotrienol in collagen-induced rat model of arthritis. Biomed Res Int. 2014;2014:539540.
  • Amdekar S, Singh V, Singh R, Sharma P, Keshav P, Kumar A. Lactobacillus casei reduces the inflammatory joint damage associated with collagen-induced arthritis (CIA) by reducing the pro-inflammatory cytokines: Lactobacillus casei: COX-2 inhibitor. J Clin Immunol. 2011;31:147–54.
  • Beren J, Hill SL, Diener-West M, Rose NR. Effect of pre-loading oral glucosamine HCl/chondroitin sulfate/manganese ascorbate combination on experimental arthritis in rats. Exp Biol Med (Maywood). 2001;226:144–51.
  • Zhang Y, Xu W, Li H, Zhang X, Xia Y, Chu K, et al. Therapeutic effects of total alkaloids of Tripterygium wilfordii Hook f. on collagen-induced arthritis in rats. J Ethnopharmacol. 2013;145:699–705.
  • Lv QW, Zhang W, Shi Q, Zheng WJ, Li X, Chen H, et al. Comparison of Tripterygium wilfordii Hook F with methotrexate in the treatment of active rheumatoid arthritis (TRIFRA): a randomised, controlled clinical trial. Ann Rheum Dis. 2015;74:1078–86.
  • Benson KF, Ruff KJ, Jensen GS. Effects of natural eggshell membrane (NEM) on cytokine production in cultures of peripheral blood mononuclear cells: increased suppression of tumor necrosis factor-alpha levels after in vitro digestion. J Med Food. 2012;15(4):360–8.
  • Ruff KJ, Durham PL, O’Reilly A, Long FD. Eggshell membrane hydrolyzates activate NF-κB in vitro: possible implications for in vivo efficacy. J Inflamm Res. 2015;8:49–57.
  • Stancikova M, Stancik R, Gubzova Z, Rovensky J. Collagen in the treatment of rheumatic diseases – oral tolerance. Bratisl Lek Listy. 1999;100:567–71.
  • Min SY, Park KS, Cho ML, Kang JW, Cho YG, Hwang SY, et al. Antigen-induced, tolerogenic CD11c+, CD11b + dendritic cells are abundant in Peyer's patches during the induction of oral tolerance to type II collagen and suppress experimental collagen-induced arthritis. Arthritis Rheum. 2006;54:887–98.
  • Park KS, Park MJ, Cho ML, Kwok SK, Ju JH, Ko HJ, et al. Type II collagen oral tolerance; mechanism and role in collagen-induced arthritis and rheumatoid arthritis. Mod Rheumatol. 2009;19:581–9.
  • Atomi Y, Shimizu M, Hasebe Y, inventors. Insulin resistance-improving agent containing eggshell membrane component, and composition using the same. US Patent 20150150916 A1. United States Patent Office. Washington, DC, USA. 2015.
  • Williams RO. Collagen-induced arthritis in mice: a major role for tumor necrosis factor-alpha. Methods Mol Biol. 2007;361:265–84.
  • Visser K, van der Heijde DM. Risk and management of liver toxicity during methotrexate treatment in rheumatoid and psoriatic arthritis: a systematic review of the literature. Clin Exp Rheumatol. 2009;27:1017–25.
  • Barrera P, Laan RF, van Riel PL, Dekhuijzen PN, Boerbooms AM, van de Putte LB. Methotrexate-related pulmonary complications in rheumatoid arthritis. Ann Rheum Dis. 1994;53:434–9.
  • Genestier L, Paillot R, Fournel S, Ferraro C, Miossec P, Revillard JP. Immunosuppressive properties of methotrexate: apoptosis and clonal deletion of activated peripheral T cells. J Clin Invest. 1998;102:322–8.
  • Seideman P, Muller-Suur R. Renal effects of aspirin and low dose methotrexate in rheumatoid arthritis. Ann Rheum Dis. 1993;52:613–15.
  • Alarcon GS, Tracy IC, Strand GM, Singh K, Macaluso M. Survival and drug discontinuation analyses in a large cohort of methotrexate treated rheumatoid arthritis patients. Ann Rheum Dis. 1995;54:708–12.
  • Yamanaka H. TNF as a target of inflammation in rheumatoid arthritis. Endocr Metab Immune Disord Drug Targets. 2015;15:129–34.
  • Taylor PC, Feldmann M. Anti-TNF biologic agents: still the therapy of choice for rheumatoid arthritis. Nat Rev Rheumatol. 2009;5:578–82.
  • Houseman M, Potter C, Marshall N, Lakey R, Cawston T, Griffiths I, et al. Baseline serum MMP-3 levels in patients with rheumatoid arthritis are still independently predictive of radiographic progression in a longitudinal observational cohort at 8 years follow up. Arthritis Res Ther. 2012;14:R30.
  • Uemura Y, Hayashi H, Takahashi T, Saitho T, Umeda R, Ichise Y, et al. MMP-3 as a biomarker of disease activity of rheumatoid arthritis. Rinsho Byori. 2015;63:1357–64.
  • Yoshioka Y, Takahashi N, Kaneko A, Hirano Y, Kanayama Y, Kanda H, et al. Disease activity early in treatment as a predictor of future low disease activity in RA patients treated with iguratimod. Mod Rheumatol. 2016;26:169–74.
  • Okamura K, Yonemoto Y, Okura C, Kobayashi T, Takagishi K. Efficacy of the clinical use of iguratimod therapy in patients with rheumatoid arthritis. Mod Rheumatol. 2015;25:235–40.
  • Okamura K, Yonemoto Y, Suto T, Okura C, Takagishi K. Efficacy at 52 weeks of daily clinical use of iguratimod in patients with rheumatoid arthritis. Mod Rheumatol. 2015;25:534–9.
  • Tanaka K, Yamaguchi T, Hara M. Iguratimod for the treatment of rheumatoid arthritis in Japan. Expert Rev Clin Immunol. 2015;11:565–73.