Abstract
Adipocytokines, including adiponectin, resistin, and visfatin may play an important role in the pathophysiology of osteoarthritis (OA). Spa therapy is one of the most commonly used non-pharmacological approaches for OA, but its mechanisms of action are not completely known. The aim of the present study was to assess whether a cycle of mud-bath therapy (MBT) influences the serum levels of adiponectin, resistin, and visfatin in patients with knee OA. As part of a prospective randomized, single blind-controlled trial evaluating the efficacy of MBT in knee OA, we included in this study 95 outpatients. One group (n = 49) received a cycle of MBT at the spa center of Chianciano Terme (Italy) in addition to the usual treatment, and one group (control group; n = 46) continued their regular care routine alone. Patients were assessed at basal time and at the end of the study (15 days) for clinical and biochemical parameters. Clinical assessments included spontaneous pain on a visual analog scale (VAS) score and the Western Ontario and McMaster Universities index (WOMAC) subscores for knee OA evaluated as total pain score (W-TPS), total stiffness score (W-TSS), and total physical function score (W-TPFS). Adiponectin, resistin and visfatin serum levels were assessed by enzyme immunoassay methods. At the end of the mud-bath therapy, serum adiponectin levels showed a significant decrease (p < 0.001), while no significant modifications were found in the control group at day 15. Serum resistin showed a significant decrease (p < 0.0001) in the MBT group at the end of the study and a significant increase in the control patients (p < 0.001). No significant modifications of visfatin were found in MBT. Furthermore, we tested the relationships between demographic and clinical parameters and adipocytokine concentrations measured in the MBT group at basal and at the end of the study. In conclusion, the present study shows that a cycle of MBT can modify serum levels of adiponectin and resistin but not the circulating levels of visfatin. In view of the recent evidences about the involvement of adiponectin and resistin in the pathogenesis and progression of OA, the decrease of these adipokines after mud-bath therapy may play a protective role in the course of the disease. However, it remains to be clarified which of the mechanisms of action of MBT may have determined the changes in serum levels of adiponectin and resistin that we observed.
Similar content being viewed by others
Abbreviations
- OA:
-
Osteoarthritis
- IL-1β:
-
Interleukin-1β
- TNF-α:
-
Tumor necrosis factor-α
- MMPS :
-
Metalloproteinases
- PGE2:
-
Prostaglandin E2
- ADAMTS:
-
Thrombospondin motifs
- PBEF:
-
Pre-B cell colony-enhancing factor
- Nampt:
-
Nicotinalide phosphoribosyltransferase
- MBT:
-
Mud-bath therapy
- hs-CRP:
-
High-sensitivity C-reactive protein
- ACR:
-
American College of Rheumatology
- BMI:
-
Body mass index
- NSAIDs:
-
Non-steroidal anti-inflammatory drugs
- SYSADOA:
-
Symptomatic slow-acting drugs for OA
- VAS:
-
Visual analog scale
- WOMAC:
-
Western Ontario and McMaster Universities index
- W-TPS:
-
Total pain score
- W-TSS:
-
Total stiffness score
- W-TPFS:
-
Total physical function score
- HDL-C:
-
High-density lipoprotein cholesterol
- LDL-C:
-
Low-density lipoprotein cholesterol
References
Altman R, Asch E, Bloch D et al (1986) Development of criteria for the classification and reporting of osteoarthritis. Classification of osteoarthritis of the knee. Diagnostic and Therapeutic Criteria Committee of the American Rheumatism Association. Arthritis Rheum 29:1039–1049
Bellamy N (2009) WOMAC osteoarthritis index: user guide IX. WOMAC, Queensland
Bellamy N, Buchanan WW, Goldsmith CH, Campbell J, Stitt LW (1998) Validation study of WOMAC: a health status instrument for measuring clinically important patient relevant outcomes to antirheumatic drug therapy in patients with osteoarthritis of the hip or knee. J Rheumatol 15:1833–1840
Bellometti S, Cecchettin M, Galzigna L (1997) Mud pack therapy in osteoarthrosis. Changes in serum levels of chondrocyte markers. Clin Chim Acta 268:101–106
Bellometti S, Galzigna L, Richelmi P, Gregotti C, Bertè F (2002) Both serum receptors of tumor necrosis factor are influenced by mud pack treatment in osteoarthrotic patients. Int J Tissue React 24:57–64
Cantarini L, Brucato A, Simonini G et al (2013) Leptin, adiponectin, resistin, visfatin serum levels and idiopathic recurrent pericarditis: biomarkers of disease activity? A preliminary report. Clin Exp Rheumatol 31:207–212
Cima L, Cozzi F, Giusti P, Guidetti G, Todesco S (1992) Neuroendocrin effects of a cycle of fangotherapy. Pharmacol Rhes 26(suppl 1):302
Conde J, Scotece M, Gómez R, Lopez V, Gómez-Reino JJ, Gualillo O (2011) Adipokines and osteoarthritis: novel molecules involved in the pathogenesis and progression of disease. Arthritis 2011:203901. doi:10.1155/2011/203901
Delaigle AM, Jonas JC, Bauche IB, Cornu O, Brichard SM (2004) Induction of adiponectin in skeletal muscle by inflammatory cytokines: in vivo and in vitro studies. Endocrinology 145:5589–5597
Fantuzzi G (2005) Adipose tissue, adipokines, and inflammation. J Allergy Clin Immunol 115:911–919
Fioravanti A, Cantarini L, Guidelli GM, Galeazzi M (2011a) Mechanisms of action of spa therapies in rheumatic diseases: what scientific evidence is there? Rheumatol Int 31:1–8. doi:10.1007/s00296-010-1628-6
Fioravanti A, Cantarini L, Bacarelli MR, de Lalla A, Ceccatelli L, Blardi P (2011b) Effects of spa therapy on serum leptin and adiponectin levels in patients with knee osteoarthritis. Rheumatol Int 31:879–882. doi:10.1007/s00296-010-1401-x
Fioravanti A, Adamczyk P, Pascarelli NA, Giannitti C, Urso R, Tołodziecki M, Ponikowska I (2014) Clinical and biochemical effects of a 3-week program of diet combined with spa therapy in obese and diabetic patients: a pilot open study. Int J Biometeorol
Fioravanti A, Bacaro G, Giannitti C, Tenti S, Cheleschi S, Guidelli GM, Pascarelli NA, Galeazzi M (2014) One year follow-up of mud-bath therapy in patients with bilateral knee osteoarthritis: a randomized, single-blind controlled trial. Int J Biometeorol [Accepted]
Francin PJ, Abot A, Guillaume C et al (2014) Association between adiponectin and cartilage degradation in human osteoarthritis. Osteoarthr Cartil 22:519–526. doi:10.1016/j.joca.2014.01.002
Fukuhara A, Matsuda M, Nishizawa M et al (2005) Visfatin: a protein secreted by visceral fat that mimics the effects of insulin. Science 307:426–430
Gabay O, Berenbaum F (2009) Adipokines in arthritis: new kids on the block. Curr Rheumatol Rev 5:226–232
Gomez R, Conde J, Scotece M, Gomez-Reino JJ, Lago F, Gualillo O (2011) What’s new in our understanding of the role of adipokines in rheumatic diseases? Nat Rev Rheumatol 7:528–536
Gonzalez-Gay MA, Llorca J, Garcia-Unzueta MT et al (2008) High-grade inflammation, circulating adiponectin oncentrations and cardiovascular risk factors in severe rheumatoid arthritis. Clin Exp Rheumatol 26:596–603
Goossens GH, Jocken JW, van Baak MA, Jansen EH, Saris WH, Blaak EE (2008) Short-term beta-adrenergic regulation of leptin, adiponectin and interleukin-6 secretion in vivo in lean and obese subjects. Diabetes Obes Metab 10:1029–1038. doi:10.1111/j.1463-1326.2008.00856.x
Gosset M, Berenbaum F, Salvat C, Sautet A, Pigenet A, Tahiri K, Jacques C (2008) Crucial role of visfatin/pre-B cell colony enhancing factor in matrix degradation and prostaglandin E2 synthesis in chondrocytes: possible influence on osteoarthritis. Arthritis Rheum 58:1399–1409. doi:10.1002/art.23431
Hochberg MC, Altman RD, April KT, American College of Rheumatology et al (2012) Recommendations for the use of nonpharmacologic and pharmacologic therapies in osteoarthritis of the hand, hip, and knee. Arthritis Care Res 64:465–474
Hu PF, Bao JP, Wu LD (2011) The emerging role of adipokines in osteoarthritis: a narrative review. Mol Biol Rep 38:873–878. doi:10.1007/s11033-010-0179-y
Imbeault P, Dépault I, Haman F (2009) Cold exposure increases adiponectin levels in men. Metabolism 58:552–559. doi:10.1016/j.metabol.2008.11.017
Iwen KA, Wenzel ET, Ott V et al (2011) Cold-induced alteration of adipokine profile in humans. Metabolism 60:430–437. doi:10.1016/j.metabol.2010.03.011
Jankovic A, Korac A, Buzadzic B et al (2013) Endocrine and metabolic signaling in retroperitoneal white adipose tissue remodeling during cold acclimation. J Obes 2013:937572. doi:10.1155/2013/937572
Jensen MP, Karoly P, Braver S (1986) The measurement of clinical pain intensity: a comparison of six methods. Pain 27:117–126
Kadowaki T, Yamauchi T, Kubota N, Hara K, Ueki K, Tobe K (2006) Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome. J Clin Invest 116:1784–1792
Kaser S, Kaser A, Sandhofer A, Ebenbichler CF, Tilg H, Patsch JR (2003) Resistin messenger-RNA expression is increased by proinflammatory cytokines in vitro. Biochem Biophys Res Commun 309:286–290
Kellgren JH, Lawrence JS (1957) Radiological assessment of osteoarthrosis. Ann Rheum Dis 16:494–502
Koskinen A, Juslin S, Nieminen R, Moilanen T, Vuolteenaho K, Moilanen E (2011) Adiponectin associates with markers of cartilage degradation in osteoarthritis and induces production of proinflammatory and catabolic factors through mitogen activated protein kinase pathways. Arthritis Res Ther 13:R184. doi:10.1186/ar3512
Koskinen A, Vuolteenaho K, Moilanen T, Moilanen E (2014) Resistin as a factor in osteoarthritis: synovial fluid resistin concentrations correlate positively with interleukin 6 and matrix metalloproteinases MMP-1 and MMP-3. Scand J Rheumatol 43:249–253. doi:10.3109/03009742.2013.853096
Laatikainen T, Salminen K, Kohvakka A, Pettersson J (1988) Response of plasma endorphins, prolactin and catecholamines in women to intense heat in a sauna. Eur J Appl Physiol Occup Physiol 57:98–102
Lago R, Gomez R, Otero M et al (2008) A new player in cartilage homeostasis: adiponectin induces nitric oxide synthase type II and pro-inflammatory cytokines in chondrocytes. Osteoarthr Cartil 16:1101–1109. doi:10.1016/j.joca.2007.12.008
Laiguillon MC, Houard X, Bougault C et al (2014) Expression and function of visfatin (Nampt), an adipokine-enzyme involved in inflammatory pathways of osteoarthritis. Arthritis Res Ther 16:R38. doi:10.1186/ar4467
Lee JH, Ort T, Ma K et al (2009) Resistin is elevated following traumatic joint injury and causes matrix degradation and release of inflammatory cytokines from articular cartilage in vitro. Osteoarthr Cartil 17:613–620. doi:10.1016/j.joca.2008.08.007
Matsuzawa Y (2005) Adiponectin: identification, physiology and clinical relevance in metabolic and vascular disease. Atheroscler Suppl 6:7–14
McConnell S, Kolopack P, Davis AM (2001) The Western Ontario and McMaster Universities Osteoarthritis index (WOMAC): a review of its utility and measurement properties. Arthritis Rheum 45:453–461
Oliveria SA, Felson DT, Cirillo PA, Reed JI, Walker AM (1999) Body weight, body mass index, and incident symptomatic osteoarthritis of the hand, hip, and knee. Epidemiology 10:161–166
Ouchi N, Shibata R, Walsh K (2006) Cardioprotection by adiponectin. Trends Cardiovasc Med 16:141–146
Poonpet T, Honsawek S (2014) Adipokines: biomarkers for osteoarthritis? World J Orthop 5:319–327. doi:10.5312/wjo.v5.i3.319
Presle N, Pottie P, Dumond H et al (2006) Differential distribution of adipokines between plasma and synovial fluid in patients with osteoarthritis. Contribution of joint tissues to their articular production. Osteoarthr Cartil 14:690–695
Puenpatom RA, Victor TW (2009) Increased prevalence of metabolic syndrome in individuals with osteoarthritis: an analysis of NHANES III data. Postgrad Med 121:9–20. doi:10.3810/pgm.2009.11.2073
Puerta M, Abelenda M, Rocha M, Trayhurn P (2002) Effect of acute cold exposure on the expression of the adiponectin, resistin and leptin genes in rat white and brown adipose tissues. Horm Metab Res 34:629–634
Punzi L, Ramonda R, Deberg M, Frallonardo P, Campana C, Musacchio E, Henrotin Y (2012) Coll2-1, Coll2-1NO2 and myeloperoxidase serum levels in erosive and non-erosive osteoarthritis of the hands. Osteoarthr Cartil 20:557–561. doi:10.1016/j.joca.2012.02.638
Salaffi F, Leardini G, Canesi B et al (2003) Reliability and validity of the Western Ontario and McMaster Universities (WOMAC) osteoarthritis index in Italian patients with osteoarthritis of the knee. Osteoarthr Cartil 11:551–560
Senolt L, Housa D, Vernerova Z et al (2007) Resistin in rheumatoid arthritis synovial tissue, synovial fluid and serum. Ann Rheum Dis 66:458–463
Shimodozono M, Matsumoto S, Ninomiya K et al (2012) Acute effects of a single warm-water bath on serum adiponectin and leptin levels in healthy men: a pilot study. Int J Biometeorol 56:933–939. doi:10.1007/s00484-011-0502-x
Srámek P, Simecková M, Janský L, Savlíková J, Vybíral S (2000) Human physiological responses to immersion into water of different temperatures. Eur J Appl Physiol 81:436–442
Steppan CM, Lazar MA (2002) Resistin and obesity-associated insulin resistance. Trends Endocrinol Metab 13:18–23
Steppan CM, Bailey ST, Bhat S et al (2001) The hormone resistin links obesity to diabetes. Nature 409:307–312
Sukenik S, Flusser D, Abu-Shakra M (1999) The role of spa therapy in various rheumatic diseases. Rheum Dis Clin N Am 25:883–897
Sun Z, Lei H, Zhang Z (2013) Pre-B cell colony enhancing factor (PBEF), a cytokine with multiple physiological functions. Cytokine Growth Factor Rev 24:433–442. doi:10.1016/j.cytogfr.2013.05.006
Tilg H, Moschen AR (2006) Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat Rev Immunol 6:772–783
Verhagen AP, Bierma-Zeinstra SM, Boers M et al (2007) Balneotherapy for osteoarthritis. Cochrane Database Syst Rev 17, CD006864
Woolf AD, Pfleger B (2003) Burden of major musculoskeletal conditions. Bull World Health Organ 81:646–656
Yusuf E, Nelissen RG, Ioan-Facsinay A et al (2010) Association between weight or body mass index and hand osteoarthritis: a systematic review. Ann Rheum Dis 69:761–765
Competing interest statement
None.
Funding
This study was funded by Regione Toscana. This study sponsor did not participate in the study design, in the collection, analysis, or the interpretation of data.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 12 kb)
Rights and permissions
About this article
Cite this article
Fioravanti, A., Giannitti, C., Cheleschi, S. et al. Circulating levels of adiponectin, resistin, and visfatin after mud-bath therapy in patients with bilateral knee osteoarthritis. Int J Biometeorol 59, 1691–1700 (2015). https://doi.org/10.1007/s00484-015-0977-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00484-015-0977-y