A pilot study on biomarkers for tendinopathy: Lower levels of serum TNF-α and other cytokines in females but not males with Achilles tendinopathy

BMC Sports Science, Medicine and Rehabilitation

Volumn 8, Issue 1, 2016, Pages

  Gaida, James E ^a,b   Alfredson, Håkan ^b,c   Forsgren, Sture ^b   Cook, Jill L ^d  

^a UNIVERSITY OF CANBERRA   (Australia)

^b UMEÅ UNIVERSITY   (Sweden)

^c UNIVERSITY COLLEGE HOSPITAL   (United Kingdom)

^d LA TROBE UNIVERSITY   (Australia)

Author keywords

Biomarkers; Cytokines; Musculoskeletal pain; Tumor necrosis factor alpha

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR RECEPTOR; BIOLOGICAL MARKER; CYTOKINE; GAMMA INTERFERON; GROWTH FACTOR; INTERLEUKIN 1; INTERLEUKIN 1BETA; PLATELET DERIVED GROWTH FACTOR BB; TUMOR NECROSIS FACTOR; VASCULOTROPIN;

ACHILLES TENDINITIS; ACHILLES TENDON; ARTICLE; BODY MASS; CASE CONTROL STUDY; CLINICAL ARTICLE; CLINICAL EVALUATION; COMPARATIVE STUDY; CONCENTRATION PROCESS; CONTROLLED STUDY; DISEASE DURATION; FASTING; FEMALE; HUMAN; MALE; PHYSICAL ACTIVITY; PILOT STUDY; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; SEX DIFFERENTIATION; TENDINITIS; TENOCYTE;

EID: 85032634579     PISSN: None     EISSN: 20521847     Source Type: Journal    
DOI: 10.1186/s13102-016-0026-0     Document Type: Article

References (43)

1. Kujala UM, Sarna S, Kaprio J. Cumulative incidence of achilles tendon rupture and tendinopathy in male former elite athletes. Clin J Sport Med. 2005;15(3):133–5.
2. Kvist M. Achilles tendon injuries in athletes. Ann Chir Gynaecol. 1991;80(2):188–201.
3. Van Ginckel A, Thijs Y, Hesar NG, Mahieu N, De Clercq D, Roosen P, et al. Intrinsic gait-related risk factors for Achilles tendinopathy in novice runners: a prospective study. Gait Posture. 2009;29(3):387–91. doi:10.1016/j.gaitpost.2008. 10.058.
4. Fernandez-Palazzi F, Rivas S, Mujica P. Achilles tendinitis in ballet dancers. Clin Orthop Relat Res. 1990;257:257–61.
5. Reule CA, Alt WW, Lohrer H, Hochwald H. Spatial orientation of the subtalar joint axis is different in subjects with and without Achilles tendon disorders. Br J Sports Med. 2011;45(13):1029–34. doi:10.1136/bjsm.2010.080119.
6. Mahieu NN, Witvrouw E, Stevens V, Van Tiggelen D, Roget P. Intrinsic risk factors for the development of achilles tendon overuse injury: a prospective study. Am J Sports Med. 2006;34(2):226–35. doi:10.1177/0363546505279918.
7. Ranger TA, Wong AMY, Cook JL, Gaida JE. Is there an association between tendinopathy and diabetes mellitus? A systematic review with meta-analysis. Br J Sports Med. 2015:in press. doi:10.1136/bjsports-2015-094735.
8. Tilley BJ, Cook JL, Docking SI, Gaida JE. Is higher serum cholesterol associated with altered tendon structure or tendon pain? A systematic review. Br J Sports Med. 2015;49(23):1504–9.
9. Kapczinski F, Dal-Pizzol F, Teixeira AL, Magalhaes PV, Kauer-Sant’Anna M, Klamt F, et al. Peripheral biomarkers and illness activity in bipolar disorder. J Psychiatr Res. 2011;45(2):156–61. doi:10.1016/j.jpsychires.2010.05.015.
10. Al-shair K, Kolsum U, Dockry R, Morris J, Singh D, Vestbo J. Biomarkers of systemic inflammation and depression and fatigue in moderate clinically stable COPD. Respir Res. 2011;12:3. doi:10.1186/1465-9921-12-3.
11. Spoettl T, Hausmann M, Klebl F, Dirmeier A, Klump B, Hoffmann J, et al. Serum soluble TNF receptor I and II levels correlate with disease activity in IBD patients. Inflamm Bowel Dis. 2007;13(6):727–32. doi:10. 1002/ibd.20107.
12. Black RA, Rauch CT, Kozlosky CJ, Peschon JJ, Slack JL, Wolfson MF, et al. A metalloproteinase disintegrin that releases tumour-necrosis factor-alpha from cells. Nature. 1997;385(6618):729–33. doi:10.1038/385729a0.
13. Aderka D, Engelmann H, Maor Y, Brakebusch C, Wallach D. Stabilization of the bioactivity of tumor necrosis factor by its soluble receptors. J Exp Med. 1992;175(2):323–9.
14. Hanai H, Watanabe F, Yamada M, Sato Y, Takeuchi K, Iida T, et al. Correlation of serum soluble TNF-alpha receptors I and II levels with disease activity in patients with ulcerative colitis. Am J Gastroenterol. 2004;99(8):1532–8. doi:10. 1111/j.1572-0241.2004.30432.x.
15. Saxne T, Palladino Jr MA, Heinegard D, Talal N, Wollheim FA. Detection of tumor necrosis factor alpha but not tumor necrosis factor beta in rheumatoid arthritis synovial fluid and serum. Arthritis Rheum. 1988;31(8):1041–5.
16. Barrera P, Boerbooms AM, Janssen EM, Sauerwein RW, Gallati H, Mulder J, et al. Circulating soluble tumor necrosis factor receptors, interleukin-2 receptors, tumor necrosis factor alpha, and interleukin-6 levels in rheumatoid arthritis. Longitudinal evaluation during methotrexate and azathioprine therapy. Arthritis Rheum. 1993;36(8):1070–9.
17. Gaida JE, Bagge J, Purdam C, Cook J, Alfredson H, Forsgren S. Evidence of the TNF-alpha system in the human Achilles tendon: expression of TNFalpha and TNF receptor at both protein and mRNA levels in the tenocytes. Cells Tissues Organs. 2012;196(4):339–52. doi:10.1159/000335475.
18. Townsend JR, Hoffman JR, Fragala MS, Jajtner AR, Gonzalez AM, Wells AJ, et al. TNF-alpha and TNFR1 responses to recovery therapies following acute resistance exercise. Front Physiol. 2015;6:48. doi:10.3389/fphys.2015.00048.
19. Andersson J, Jansson JH, Hellsten G, Nilsson TK, Hallmans G, Boman K. Effects of heavy endurance physical exercise on inflammatory markers in non-athletes. Atherosclerosis. 2010;209(2):601–5. doi:10.1016/j.atherosclerosis. 2009.10.025.
20. Andersson H, Bohn SK, Raastad T, Paulsen G, Blomhoff R, Kadi F. Differences in the inflammatory plasma cytokine response following two elite female soccer games separated by a 72-h recovery. Scand J Med Sci Sports. 2010;20(5):740–7. doi:10.1111/j.1600-0838.2009.00989.x.
21. Holbrook TC, McFarlane D, Schott II HC. Neuroendocrine and non-neuroendocrine markers of inflammation associated with performance in endurance horses. Equine Vet J Suppl. 2010;38:123–8. doi:10.1111/j.2042-3306.2010.00256.x.
22. MacKinnon LT. Special feature for the Olympics: effects of exercise on the immune system: overtraining effects on immunity and performance in athletes. Immunol Cell Biol. 2000;78(5):502–9. doi:10.1111/j.1440-1711.2000. t01-7-.x.
23. Bagge J, Gaida JE, Danielson P, Alfredson H, Forsgren S. Physical activity level in Achilles tendinosis is associated with blood levels of pain-related factors: a pilot study. Scand J Med Sci Sports. 2011;21(6):e430–8. doi:10. 1111/j.1600-0838.2011.01358.x.
24. Gouveia-Figueira S, Nording ML, Gaida JE, Forsgren S, Alfredson H, Fowler CJ. Serum levels of oxylipins in achilles tendinopathy: an exploratory study. PLoS ONE. 2015;10(4), e0123114. doi:10.1371/journal.pone.0123114.
25. Carp SJ, Barr AE, Barbe MF. Serum biomarkers as signals for risk and severity of work-related musculoskeletal injury. Biomark Med. 2008;2(1):67–79. doi:10. 2217/17520363.2.1.67.
26. Friedenreich CM, Courneya KS, Neilson HK, Matthews CE, Willis G, Irwin M, et al. Reliability and validity of the past year total physical activity questionnaire. Am J Epidemiol. 2006;163(10):959–70. doi:10.1093/aje/kwj112.
27. Gold JE, Mohamed FB, Ali S, Barbe MF. Serum and MRI biomarkers in mobile device texting: a pilot study. Hum Factors. 2014;56(5):864–72. doi:10. 1177/0018720813507953.
28. Pingel J, Fredberg U, Mikkelsen LR, Schjerling P, Heinemeier KM, Kjaer M, et al. No inflammatory gene-expression response to acute exercise in human Achilles tendinopathy. Eur J Appl Physiol. 2013;113(8):2101–9. doi:10. 1007/s00421-013-2638-3.
29. Ostrowski K, Rohde T, Asp S, Schjerling P, Pedersen BK. Pro- and anti-inflammatory cytokine balance in strenuous exercise in humans. J Physiol. 1999;515(Pt 1):287–91.
30. Moldoveanu AI, Shephard RJ, Shek PN. Exercise elevates plasma levels but not gene expression of IL-1beta, IL-6, and TNF-alpha in blood mononuclear cells. J Appl Physiol. 2000;89(4):1499–504.
31. Steensberg A, Keller C, Starkie RL, Osada T, Febbraio MA, Pedersen BK. IL-6 and TNF-alpha expression in, and release from, contracting human skeletal muscle. Am J Physiol Endocrinol Metab. 2002;283(6):E1272–8. doi:10.1152/ ajpendo.00255.2002.
32. Jeukendrup AE, Vet-Joop K, Sturk A, Stegen JH, Senden J, Saris WH, et al. Relationship between gastro-intestinal complaints and endotoxaemia, cytokine release and the acute-phase reaction during and after a long-distance triathlon in highly trained men. Clin Sci (Lond). 2000;98(1):47–55.
33. Febbraio MA, Steensberg A, Starkie RL, McConell GK, Kingwell BA. Skeletal muscle interleukin-6 and tumor necrosis factor-alpha release in healthy subjects and patients with type 2 diabetes at rest and during exercise. Metabolism. 2003;52(7):939–44.
34. Straczkowski M, Kowalska I, Dzienis-Straczkowska S, Stepien A, Skibinska E, Szelachowska M, et al. Changes in tumor necrosis factor-alpha system and insulin sensitivity during an exercise training program in obese women with normal and impaired glucose tolerance. Eur J Endocrinol. 2001;145(3):273–80.
35. Klimcakova E, Polak J, Moro C, Hejnova J, Majercik M, Viguerie N, et al. Dynamic strength training improves insulin sensitivity without altering plasma levels and gene expression of adipokines in subcutaneous adipose tissue in obese men. J Clin Endocrinol Metab. 2006;91(12):5107–12. doi:10. 1210/jc.2006-0382.
36. Reynolds TH, Supiano MA, Dengel DR. Resistance training enhances insulin-mediated glucose disposal with minimal effect on the tumor necrosis factor-alpha system in older hypertensives. Metabolism. 2004;53(3):397–402.
37. Ho SS, Dhaliwal SS, Hills AP, Pal S. Effects of chronic exercise training on inflammatory markers in Australian overweight and obese individuals in a randomized controlled trial. Inflammation. 2013;36(3):625–32. doi:10.1007/ s10753-012-9584-9.
38. Scott A, Lian O, Bahr R, Hart DA, Duronio V. VEGF expression in patellar tendinopathy: a preliminary study. Clin Orthop Relat Res. 2008;466(7):1598–604. doi:10.1007/s11999-008-0272-x.
39. Hess A, Axmann R, Rech J, Finzel S, Heindl C, Kreitz S, et al. Blockade of TNFalpha rapidly inhibits pain responses in the central nervous system. Proc Natl Acad Sci U S A. 2011;108(9):3731–6. doi:10.1073/pnas.1011774108.
40. Pradillo JM, Romera C, Hurtado O, Cardenas A, Moro MA, Leza JC, et al. TNFR1 upregulation mediates tolerance after brain ischemic preconditioning. J Cereb Blood Flow Metab. 2005;25(2):193–203. doi:10. 1038/sj.jcbfm.9600019.
41. Cook EB, Stahl JL, Graziano FM, Barney NP. Regulation of the receptor for TNFalpha, TNFR1, in human conjunctival epithelial cells. Invest Ophthalmol Vis Sci. 2008;49(9):3992–8. doi:10.1167/iovs.08-1873.
42. Gold JE, Hallman DM, Hellstrom F, Bjorklund M, Crenshaw AG, Djupsjobacka M, et al. Systematic review of biochemical biomarkers for neck and upper-extremity musculoskeletal disorders. Scand J Work Environ Health. 2015. doi: 10.5271/sjweh.3533.
43. Ohberg L, Lorentzon R, Alfredson H. Neovascularisation in Achilles tendons with painful tendinosis but not in normal tendons: an ultrasonographic investigation. Knee Surg Sports Traumatol Arthrosc. 2001;9(4):233–8.