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Open Access 01-12-2018 | Research article

Obesity alters the in vivo mechanical response and biochemical properties of cartilage as measured by MRI

Authors: Amber T Collins, Micaela L Kulvaranon, Hattie C Cutcliffe, Gangadhar M Utturkar, Wyatt A R Smith, Charles E Spritzer, Farshid Guilak, Louis E DeFrate

Published in: Arthritis Research & Therapy | Issue 1/2018

Abstract

Background

Obesity is a primary risk factor for the development of knee osteoarthritis (OA). However, there remains a lack of in vivo data on the influence of obesity on knee cartilage mechanics and composition. The purpose of this study was to determine the relationship between obesity and tibiofemoral cartilage properties.

Methods

Magnetic resonance images (3T) of cartilage geometry (double-echo steady-state) and T1rho relaxation of the knee were obtained in healthy subjects with a normal (n = 8) or high (n = 7) body mass index (BMI) before and immediately after treadmill walking. Subjects had no history of lower limb injury or surgery. Bone and cartilage surfaces were segmented and three-dimensional models were created to measure cartilage thickness and strain. T1rho relaxation times were measured before exercise in both the tibial and femoral cartilage in order to characterize biochemical composition. Body fat composition was also measured.

Results

Subjects with a high BMI exhibited significantly increased tibiofemoral cartilage strain and T1rho relaxation times (P <0.05). Tibial pre-exercise cartilage thickness was also affected by BMI (P <0.05). Correlational analyses revealed that pre-exercise tibial cartilage thickness decreased with increasing BMI (R² = 0.43, P <0.01) and body fat percentage (R² = 0.58, P <0.01). Tibial and femoral cartilage strain increased with increasing BMI (R² = 0.45, P <0.01; R² = 0.51, P <0.01, respectively) and increasing body fat percentage (R² = 0.40, P <0.05; R² = 0.38, P <0.05, respectively). Additionally, tibial T1rho was positively correlated with BMI (R² = 0.39, P <0.05) and body fat percentage (R² = 0.47, P <0.01).

Conclusions

Strains and T1rho relaxation times in the tibiofemoral cartilage were increased in high BMI subjects compared with normal BMI subjects. Additionally, pre-exercise tibial cartilage thickness decreased with obesity. Reduced proteoglycan content may be indicative of pre-symptomatic osteoarthritic degeneration, resulting in reduced cartilage thickness and increased deformation of cartilage in response to loading.

Felson DT. Relation of obesity and of vocational and avocational risk factors to osteoarthritis. J Rheumatol. 2005;32:1133–5. http://www.ncbi.nlm.nih.gov/pubmed/15977343.PubMed

Runhaar J, Koes BW, Clockaerts S, Bierma-Zeinstra SM. A systematic review on changed biomechanics of lower extremities in obese individuals: a possible role in development of osteoarthritis. Obes Rev. 2011;12:1071–82. https://doi.org/10.1111/j.1467-789X.2011.00916.x.CrossRefPubMed

Felson DT. Weight and osteoarthritis. J Rheumatol Suppl. 1995;43:7–9. http://www.ncbi.nlm.nih.gov/pubmed/7752143.PubMed

Murphy L, Schwartz TA, Helmick CG, Renner JB, Tudor G, Koch G, et al. Lifetime risk of symptomatic knee osteoarthritis. Arthritis Rheum. 2008;59:1207–13. https://doi.org/10.1002/art.24021.CrossRefPubMedPubMedCentral

Powell A, Teichtahl AJ, Wluka AE, Cicuttini FM. Obesity: a preventable risk factor for large joint osteoarthritis which may act through biomechanical factors. Br J Sports Med. 2005;39:4–5. https://doi.org/10.1136/bjsm.2004.011841.CrossRefPubMedPubMedCentral

Felson DT. Does excess weight cause osteoarthritis and, if so, why? Ann Rheum Dis. 1996;55:668–70. http://www.ncbi.nlm.nih.gov/pubmed/8882146.CrossRef

Griffin TM, Guilak F. Why is obesity associated with osteoarthritis? Insights from mouse models of obesity. Biorheology. 2008;45:387–98. http://www.ncbi.nlm.nih.gov/pubmed/18836239.PubMedPubMedCentral

Aspden RM. Obesity punches above its weight in osteoarthritis. Nat Rev Rheumatol. 2011;7:65–8. https://doi.org/10.1038/nrrheum.2010.123.CrossRefPubMed

Grotle M, Hagen KB, Natvig B, Dahl FA, Kvien TK. Obesity and osteoarthritis in knee, hip and/or hand: an epidemiological study in the general population with 10 years follow-up. BMC Musculoskelet Disord. 2008;9:132. https://doi.org/10.1186/1471-2474-9-132.CrossRefPubMedPubMedCentral

10.

Oliveria SA, Felson DT, Cirillo PA, Reed JI, Walker AM. Body weight, body mass index, and incident symptomatic osteoarthritis of the hand, hip, and knee. Epidemiology. 1999;10:161–6. https://www.ncbi.nlm.nih.gov/pubmed/10069252.CrossRef

11.

Hurwitz D, Sumner D, Andriacchi T, Sugar D. Dynamic knee loads during gait predict proximal tibial bone distribution. J Biomech. 1998;31:423–30.CrossRef

12.

Landry SC, McKean KA, Hubley-Kozey CL, Stanish WD, Deluzio KJ. Knee biomechanics of moderate OA patients measured during gait at a self-selected and fast walking speed. J Biomech. 2007;40:1754–61. http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=17084845.CrossRef

13.

Fregly BJ, D’Lima DD, Colwell CW Jr. Effective gait patterns for offloading the medial compartment of the knee. J Orthop Res. 2009;27:1016–21. https://doi.org/10.1002/jor.20843.CrossRefPubMedPubMedCentral

14.

Cher WL, Utturkar GM, Spritzer CE, Nunley JA, DeFrate LE, Collins AT. An analysis of changes in in vivo cartilage thickness of the healthy ankle following dynamic activity. J Biomech. 2016;49:3026–30. https://doi.org/10.1016/j.jbiomech.2016.05.030.CrossRefPubMedPubMedCentral

15.

Lad NK, Liu B, Ganapathy PK, Utturkar GM, Sutter EG, Moorman CT 3rd, et al. Effect of normal gait on in vivo tibiofemoral cartilage strains. J Biomech. 2016;49:2870–6. https://doi.org/10.1016/j.jbiomech.2016.06.025.CrossRefPubMedPubMedCentral

16.

Liu B, Lad NK, Collins AT, Ganapathy PK, Utturkar GM, McNulty AL, et al. In vivo tibial cartilage strains in regions of cartilage-to-cartilage contact and cartilage-to-meniscus contact in response to walking. Am J Sports Med. 2017;45:2817–23. https://doi.org/10.1177/0363546517712506.CrossRefPubMedPubMedCentral

17.

Eckstein F, Lemberger B, Gratzke C, Hudelmaier M, Glaser C, Englmeier KH, et al. In vivo cartilage deformation after different types of activity and its dependence on physical training status. Ann Rheum Dis. 2005;64:291–5. https://doi.org/10.1136/ard.2004.022400.CrossRefPubMedPubMedCentral

18.

Widmyer MR, Utturkar GM, Leddy HA, Coleman JL, Spritzer CE, Moorman CT 3rd, et al. High body mass index is associated with increased diurnal strains in the articular cartilage of the knee. Arthritis Rheum. 2013;65:2615–22. https://doi.org/10.1002/art.38062.CrossRefPubMedPubMedCentral

19.

Coleman JL, Widmyer MR, Leddy HA, Utturkar GM, Spritzer CE, Moorman CT 3rd, et al. Diurnal variations in articular cartilage thickness and strain in the human knee. J Biomech. 2013;46:541–7. https://doi.org/10.1016/j.jbiomech.2012.09.013.CrossRefPubMed

20.

Tsushima H, Okazaki K, Takayama Y, Hatakenaka M, Honda H, Izawa T, et al. Evaluation of cartilage degradation in arthritis using T1rho magnetic resonance imaging mapping. Rheumatol Int. 2012;32:2867–75. https://doi.org/10.1007/s00296-011-2140-3.CrossRefPubMed

21.

Li X, Benjamin Ma C, Link TM, Castillo DD, Blumenkrantz G, Lozano J, et al. In vivo T(1rho) and T(2) mapping of articular cartilage in osteoarthritis of the knee using 3 T MRI. Osteoarthritis Cartilage. 2007;15:789–97. https://doi.org/10.1016/j.joca.2007.01.011.CrossRefPubMedPubMedCentral

22.

Keenan KE, Besier TF, Pauly JM, Han E, Rosenberg J, Smith RL, et al. Prediction of glycosaminoglycan content in human cartilage by age, T1rho and T2 MRI. Osteoarthritis Cartilage. 2011;19:171–9. https://doi.org/10.1016/j.joca.2010.11.009.CrossRefPubMed

23.

Li X, Pai A, Blumenkrantz G, Carballido-Gamio J, Link T, Ma B, et al. Spatial distribution and relationship of T1rho and T2 relaxation times in knee cartilage with osteoarthritis. Magn Reson Med. 2009;61:1310–8. https://doi.org/10.1002/mrm.21877.CrossRefPubMedPubMedCentral

24.

Souza RB, Kumar D, Calixto N, Singh J, Schooler J, Subburaj K, et al. Response of knee cartilage T1rho and T2 relaxation times to in vivo mechanical loading in individuals with and without knee osteoarthritis. Osteoarthritis Cartilage. 2014;22:1367–76. https://doi.org/10.1016/j.joca.2014.04.017.CrossRefPubMedPubMedCentral

25.

Taylor KA, Cutcliffe HC, Queen RM, Utturkar GM, Spritzer CE, Garrett WE, et al. In vivo measurement of ACL length and relative strain during walking. J Biomech. 2013;46:478–83. https://doi.org/10.1016/j.jbiomech.2012.10.031.CrossRefPubMed

26.

Alexander RM, Jayes AS. A dynamic similarity hypothesis for the gaits of quadrupedal mammals. J Zool. 1983;201:135–52 <Go to ISI>://WOS:A1983RH79100010.CrossRef

27.

von Hurst PR, Walsh DCI, Conlon CA, Ingram M, Kruger R, Stonehouse W. Validity and reliability of bioelectrical impedance analysis to estimate body fat percentage against air displacement plethysmography and dual-energy X-ray absorptiometry. Nutr Diet. 2016;73:197–204. https://doi.org/10.1111/1747-0080.12172.CrossRef

28.

Okafor EC, Utturkar GM, Widmyer MR, Abebe ES, Collins AT, Taylor DC, et al. The effects of femoral graft placement on cartilage thickness after anterior cruciate ligament reconstruction. J Biomech. 2014;47:96–101. https://doi.org/10.1016/j.jbiomech.2013.10.003.CrossRefPubMed

29.

Van de Velde SK, Bingham JT, Hosseini A, Kozanek M, DeFrate LE, Gill TJ, et al. Increased tibiofemoral cartilage contact deformation in patients with anterior cruciate ligament deficiency. Arthritis Rheum. 2009;60:3693–702. https://doi.org/10.1002/art.24965.CrossRefPubMedPubMedCentral

30.

Borthakur A, Wheaton A, Charagundla SR, Shapiro EM, Regatte RR, Akella SV, et al. Three-dimensional T1rho-weighted MRI at 1.5 Tesla. Journal of magnetic resonance imaging. JMRI. 2003;17:730–6. https://doi.org/10.1002/jmri.10296.CrossRefPubMed

31.

Hatcher CC, Collins AT, Kim SY, Michel LC, Mostertz WC 3rd, Ziemian SN, et al. Relationship between T1rho magnetic resonance imaging, synovial fluid biomarkers, and the biochemical and biomechanical properties of cartilage. J Biomech. 2017;55:18–26. https://doi.org/10.1016/j.jbiomech.2017.02.001.CrossRefPubMedPubMedCentral

32.

Wheaton AJ, Dodge GR, Borthakur A, Kneeland JB, Schumacher HR, Reddy R. Detection of changes in articular cartilage proteoglycan by T(1rho) magnetic resonance imaging. J Orthop Res. 2004;23:102–8. https://doi.org/10.1016/j.orthres.2004.06.015.CrossRef

33.

DeVita P, Hortobagyi T. Obesity is not associated with increased knee joint torque and power during level walking. J Biomech. 2003;36:1355–62. https://www.ncbi.nlm.nih.gov/pubmed/12893044.CrossRef

34.

Harding GT, Dunbar MJ, Hubley-Kozey CL, Stanish WD, Astephen Wilson JL. Obesity is associated with higher absolute tibiofemoral contact and muscle forces during gait with and without knee osteoarthritis. Clin Biomech (Bristol, Avon). 2016;31:79–86. https://doi.org/10.1016/j.clinbiomech.2015.09.017.CrossRef

35.

DeVita P, Rider P, Hortobagyi T. Reductions in knee joint forces with weight loss are attenuated by gait adaptations in class III obesity. Gait Posture. 2016;45:25–30. https://doi.org/10.1016/j.gaitpost.2015.12.040.CrossRefPubMed

36.

Liukkonen MK, Mononen ME, Vartiainen P, Kaukinen P, Bragge T, Suomalainen JS, et al. Evaluation of the effect of bariatric surgery-induced weight loss on knee gait and cartilage degeneration. J Biomech Eng. 2018;140(4). https://doi.org/10.1115/1.4038330.CrossRef

37.

Anandacoomarasamy A, Leibman S, Smith G, Caterson I, Giuffre B, Fransen M, et al. Weight loss in obese people has structure-modifying effects on medial but not on lateral knee articular cartilage. Ann Rheum Dis. 2012;71:26–32. https://doi.org/10.1136/ard.2010.144725.CrossRefPubMed

38.

Setton LA, Elliott DM, Mow VC. Altered mechanics of cartilage with osteoarthritis: human osteoarthritis and an experimental model of joint degeneration. Osteoarthritis Cartilage. 1999;7:2–14. https://doi.org/10.1053/joca.1998.0170.CrossRefPubMed

39.

Griffin TM, Fermor B, Huebner JL, Kraus VB, Rodriguiz RM, Wetsel WC, et al. Diet-induced obesity differentially regulates behavioral, biomechanical, and molecular risk factors for osteoarthritis in mice. Arthritis Res Ther. 2010;12:R130. https://doi.org/10.1186/ar3068.CrossRefPubMedPubMedCentral

40.

Sanchez-Adams J, Leddy HA, McNulty AL, O’Conor CJ, Guilak F. The mechanobiology of articular cartilage bearing the burden of osteoarthritis. Curr Rheumatol Rep. 2014;16:451. https://doi.org/10.1007/s11926-014-0451-6.CrossRefPubMedPubMedCentral

41.

Coleman MC, Ramakrishnan PS, Brouillette MJ, Martin JA. Injurious loading of articular cartilage compromises chondrocyte respiratory function. Arthritis Rheumatol. 2016;68:662–71. https://doi.org/10.1002/art.39460.CrossRefPubMedPubMedCentral

42.

Lee W, Leddy HA, Chen Y, Lee SH, Zelenski NA, McNulty AL, et al. Synergy between Piezo1 and Piezo2 channels confers high-strain mechanosensitivity to articular cartilage. Proc Natl Acad Sci U S A. 2014;111:E5114–22. https://doi.org/10.1073/pnas.1414298111.CrossRefPubMedPubMedCentral

43.

Mohanraj B, Meloni GR, Mauck RL, Dodge GR. A high-throughput model of post-traumatic osteoarthritis using engineered cartilage tissue analogs. Osteoarthritis Cartilage. 2014;22:1282–90. https://doi.org/10.1016/j.joca.2014.06.032.CrossRefPubMedPubMedCentral

44.

Honda K, Ohno S, Tanimoto K, Ijuin C, Tanaka N, Doi T, et al. The effects of high magnitude cyclic tensile load on cartilage matrix metabolism in cultured chondrocytes. Eur J Cell Biol. 2000;79:601–9. https://doi.org/10.1078/0171-9335-00089.CrossRefPubMed

45.

Guilak F. Biomechanical factors in osteoarthritis. Best Pract Res Clin Rheumatol. 2011;25:815–23. https://doi.org/10.1016/j.berh.2011.11.013.CrossRefPubMedPubMedCentral

46.

Carman WJ, Sowers M, Hawthorne VM, Weissfeld LA. Obesity as a risk factor for osteoarthritis of the hand and wrist: a prospective study. Am J Epidemiol. 1994;139:119–29. https://www.ncbi.nlm.nih.gov/pubmed/8296779.CrossRef

47.

Aygun AD, Gungor S, Ustundag B, Gurgoze MK, Sen Y. Proinflammatory cytokines and leptin are increased in serum of prepubertal obese children. Mediat Inflamm. 2005;2005:180–3. https://doi.org/10.1155/MI.2005.180.CrossRef

48.

Wellen KE, Hotamisligil GS. Inflammation, stress, and diabetes. J Clin Invest. 2005;115:1111–9. https://doi.org/10.1172/JCI25102.CrossRefPubMedPubMedCentral

49.

Messier SP, Mihalko SL, Legault C, Miller GD, Nicklas BJ, DeVita P, et al. Effects of intensive diet and exercise on knee joint loads, inflammation, and clinical outcomes among overweight and obese adults with knee osteoarthritis: the IDEA randomized clinical trial. JAMA. 2013;310:1263–73. https://doi.org/10.1001/jama.2013.277669.CrossRefPubMedPubMedCentral

50.

Huebner JL, Landerman LR, Somers TJ, Keefe FJ, Guilak F, Blumenthal JA, et al. Exploratory secondary analyses of a cognitive-behavioral intervention for knee osteoarthritis demonstrate reduction in biomarkers of adipocyte inflammation. Osteoarthritis Cartilage. 2016;24:1528–34. https://doi.org/10.1016/j.joca.2016.04.002.CrossRefPubMedPubMedCentral

51.

McNulty AL, Miller MR, O’Connor SK, Guilak F. The effects of adipokines on cartilage and meniscus catabolism. Connect Tissue Res. 2011;52:523–33. https://doi.org/10.3109/03008207.2011.597902.CrossRefPubMedPubMedCentral

52.

Hui W, Litherland GJ, Elias MS, Kitson GI, Cawston TE, Rowan AD, et al. Leptin produced by joint white adipose tissue induces cartilage degradation via upregulation and activation of matrix metalloproteinases. Ann Rheum Dis. 2012;71:455–62. https://doi.org/10.1136/annrheumdis-2011-200372.CrossRefPubMed

53.

Eckstein F, Tieschky M, Faber S, Englmeier KH, Reiser M. Functional analysis of articular cartilage deformation, recovery, and fluid flow following dynamic exercise in vivo. Anat Embryol. 1999;200:419–24. http://www.ncbi.nlm.nih.gov/pubmed/10460479.CrossRef

Title: Obesity alters the in vivo mechanical response and biochemical properties of cartilage as measured by MRI
Authors: Amber T Collins
Micaela L Kulvaranon
Hattie C Cutcliffe
Gangadhar M Utturkar
Wyatt A R Smith
Charles E Spritzer
Farshid Guilak
Louis E DeFrate
Publication date: 01-12-2018
Publisher: BioMed Central
Published in: Arthritis Research & Therapy / Issue 1/2018
Electronic ISSN: 1478-6362
DOI: https://doi.org/10.1186/s13075-018-1727-4

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Obesity alters the in vivo mechanical response and biochemical properties of cartilage as measured by MRI

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