Skip to main content

Advertisement

SpringerLink
Log in

Estimation of the Effect of Body Weight on the Development of Osteoarthritis Based on Cumulative Stresses in Cartilage: Data from the Osteoarthritis Initiative

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

Evaluation of the subject-specific biomechanical effects of obesity on the progression of OA is challenging. The aim of this study was to create 3D MRI-based finite element models of the knee joints of seven obese subjects, who had developed OA at 4-year follow-up, and of seven normal weight subjects, who had not developed OA at 4-year follow-up, to test the sensitivity of cumulative maximum principal stresses in cartilage in quantitative risk evaluation of the initiation and progression of knee OA. Volumes of elements with cumulative stresses over 5 MPa in tibial cartilage were significantly (p < 0.05) larger in obese subjects as compared to normal weight subjects. Locations of high peak cumulative stresses at the baseline in most of the obese subjects showed a good agreement with the locations of the cartilage loss and MRI scoring at follow-up. Simulated weight loss (to body mass index 24 kg/m2) in obese subjects led to significant reduction of the highest cumulative stresses in tibial and femoral cartilages. The modeling results suggest that an analysis of cumulative stresses could be used to evaluate subject-specific effects of obesity and weight loss on cartilage responses and potential risks for the progression of knee OA.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  1. Aaboe, J., H. Bliddal, S. Messier, T. Alkjaer, and M. Henriksen. Effects of an intensive weight loss program on knee joint loading in obese adults with knee osteoarthritis. Osteoarthr. Cartil. 19:822–828, 2011.

    Article  CAS  PubMed  Google Scholar 

  2. Anandacoomarasamy, A., G. Smith, S. Leibman, I. Caterson, B. Giuffre, M. Fransen, P. Sambrook, and L. March. Cartilage defects are associated with physical disability in obese adults. Rheumatology (Oxford) 48:1290–1293, 2009.

    Article  Google Scholar 

  3. Anderson, J. J., and D. T. Felson. Factors associated with osteoarthritis of the knee in the first national Health and Nutrition Examination Survey (HANES I). Evidence for an association with overweight, race, and physical demands of work. Am. J. Epidemiol. 128:179–189, 1988.

    Article  CAS  PubMed  Google Scholar 

  4. Angrisani, L., G. Formisano, A. Santonicola, A. Hasani, and A. Vitiello. Bariatric surgery worldwide. In: Bariatric and Metabolic Surgery, edited by L. Angrisani. New York: Springer, 2017, pp. 19–24.

    Chapter  Google Scholar 

  5. Bellucci, G., and B. Seedhom. Mechanical behaviour of articular cartilage under tensile cyclic load. Rheumatology 40:1337–1345, 2001.

    Article  CAS  PubMed  Google Scholar 

  6. Bergmann, G., A. Bender, F. Graichen, J. Dymke, A. Rohlmann, A. Trepczynski, M. O. Heller, and I. Kutzner. Standardized loads acting in knee implants. PLoS ONE 9:e86035, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Braun, H. J., and G. E. Gold. Diagnosis of osteoarthritis: imaging. Bone 51:278–288, 2012.

    Article  PubMed  Google Scholar 

  8. Cicuttini, F., C. Ding, A. Wluka, S. Davis, P. R. Ebeling, and G. Jones. Association of cartilage defects with loss of knee cartilage in healthy, middle-age adults: a prospective study. Arthritis Rheum. 52:2033–2039, 2005.

    Article  PubMed  Google Scholar 

  9. Clements, K., Z. Bee, G. Crossingham, M. Adams, and M. Sharif. How severe must repetitive loading be to kill chondrocytes in articular cartilage? Osteoarthr. Cartil. 9:499–507, 2001.

    Article  CAS  PubMed  Google Scholar 

  10. Coggon, D., I. Reading, P. Croft, M. McLaren, D. Barrett, and C. Cooper. Knee osteoarthritis and obesity. Int. J. Obes. Relat. Metab. Disord. 25(2):622, 2001.

    Article  CAS  PubMed  Google Scholar 

  11. Danso, E., J. Honkanen, S. Saarakkala, and R. Korhonen. Comparison of nonlinear mechanical properties of bovine articular cartilage and meniscus. J. Biomech. 47:200–206, 2014.

    Article  CAS  PubMed  Google Scholar 

  12. Danso, E., J. Mäkelä, P. Tanska, M. Mononen, J. Honkanen, J. Jurvelin, J. Töyräs, P. Julkunen, and R. Korhonen. Characterization of site-specific biomechanical properties of human meniscus—importance of collagen and fluid on mechanical nonlinearities. J. Biomech. 48(8):1499–1507, 2015.

    Article  CAS  PubMed  Google Scholar 

  13. Dillon, C. F., E. K. Rasch, Q. Gu, and R. Hirsch. Prevalence of knee osteoarthritis in the United States: arthritis data from the Third National Health and Nutrition Examination Survey 1991–1994. J. Rheumatol. 33:2271–2279, 2006.

    PubMed  Google Scholar 

  14. Ding, C., V. Parameswaran, F. Cicuttini, J. Burgess, G. Zhai, S. Quinn, and G. Jones. Association between leptin, body composition, sex and knee cartilage morphology in older adults: the Tasmanian older adult cohort (TASOAC) study. Ann. Rheum. Dis. 67:1256–1261, 2008.

    Article  CAS  PubMed  Google Scholar 

  15. Doyle, J. F. Modern Experimental Stress Analysis: Completing the Solution of Partially Specified Problems. Chichester: Wiley, 2004.

    Book  Google Scholar 

  16. Elliott, D. M., D. A. Narmoneva, and L. A. Setton. Direct measurement of the poisson’s ratio of human patella cartilage in tension. J. Biomech. Eng. 124:223–228, 2002.

    Article  PubMed  Google Scholar 

  17. Felson, D. T. The epidemiology of knee osteoarthritis: results from the framingham osteoarthritis study. Semin. Arthritis Rheum. 20:42–50, 1990.

    Article  CAS  PubMed  Google Scholar 

  18. Felson, D. T., Y. Zhang, J. M. Anthony, A. Naimark, and J. J. Anderson. Weight loss reduces the risk for symptomatic knee osteoarthritis in women: the framingham study. Ann. Intern. Med. 116:535–539, 1992.

    Article  CAS  PubMed  Google Scholar 

  19. Goertzen, D., D. Budney, and J. Cinats. Methodology and apparatus to determine material properties of the knee joint meniscus. Med. Eng. Phys. 19:412–419, 1997.

    Article  CAS  PubMed  Google Scholar 

  20. Haight, D. J., Z. F. Lerner, W. J. Board, and R. C. Browning. A comparison of slow, uphill and fast, level walking on lower extremity biomechanics and tibiofemoral joint loading in obese and nonobese adults. J. Orthop. Res. 32:324–330, 2014.

    Article  PubMed  Google Scholar 

  21. Henriksen, M., R. Christensen, B. Danneskiold-Samsøe, and H. Bliddal. Changes in lower extremity muscle mass and muscle strength after weight loss in obese patients with knee osteoarthritis: a prospective cohort study. Arthritis Rheum. 64:438–442, 2012.

    Article  PubMed  Google Scholar 

  22. Hunter, D. J., A. Guermazi, G. H. Lo, A. J. Grainger, P. G. Conaghan, R. M. Boudreau, and F. W. Roemer. Evolution of semi-quantitative whole joint assessment of knee OA: MOAKS (MRI Osteoarthritis Knee Score). Osteoarthr. Cartil. 19:990–1002, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Hunter, D., W. Zhang, P. G. Conaghan, K. Hirko, L. Menashe, L. Li, W. Reichmann, and E. Losina. Systematic review of the concurrent and predictive validity of MRI biomarkers in OA. Osteoarthr. Cartil. 19:557–588, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Jiang, L., W. Tian, Y. Wang, J. Rong, C. Bao, Y. Liu, Y. Zhao, and C. Wang. Body mass index and susceptibility to knee osteoarthritis: a systematic review and meta-analysis. Jt. Bone Spine 79:291–297, 2012.

    Article  Google Scholar 

  25. Kazemi, M., Y. Dabiri, and L. P. Li. Recent advances in computational mechanics of the human knee joint. Comput. Math. Methods Med. 2013. https://doi.org/10.1155/2013/718423.

    PubMed  PubMed Central  Google Scholar 

  26. Kellgren, J. H., and J. S. Lawrence. Radiological assessment of osteoarthrosis. Ann. Rheum. Dis. 16:494–502, 1957.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Klets, O., M. E. Mononen, P. Tanska, M. T. Nieminen, R. K. Korhonen, and S. Saarakkala. Comparison of different material models of articular cartilage in 3D computational modeling of the knee: data from the osteoarthritis initiative (OAI). J. Biomech. 49:3891–3900, 2016.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Kozanek, M., A. Hosseini, F. Liu, S. K. Van de Velde, T. J. Gill, H. E. Rubash, and G. Li. Tibiofemoral kinematics and condylar motion during the stance phase of gait. J. Biomech. 42:1877–1884, 2009.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Kutzner, I., B. Heinlein, F. Graichen, A. Bender, A. Rohlmann, A. Halder, A. Beier, and G. Bergmann. Loading of the knee joint during activities of daily living measured in vivo in five subjects. J. Biomech. 43:2164–2173, 2010.

    Article  CAS  PubMed  Google Scholar 

  30. Li, L., M. Buschmann, and A. Shirazi-Adl. A fibril reinforced nonhomogeneous poroelastic model for articular cartilage: inhomogeneous response in unconfined compression. J. Biomech. 33:1533–1541, 2000.

    Article  CAS  PubMed  Google Scholar 

  31. Liukkonen, M. K., M. E. Mononen, P. Vartiainen, P. Kaukinen, T. Bragge, J. Suomalainen, M. K. Malo, S. Venesmaa, P. Käkelä, and J. Pihlajamäki. Evaluation of the effect of bariatric surgery-induced weight loss on knee gait and cartilage degeneration. J. Biomech Eng 2017. https://doi.org/10.1115/1.4038330.

    PubMed  Google Scholar 

  32. Losina, E., R. P. Walensky, C. L. Kessler, P. S. Emrani, W. M. Reichmann, E. A. Wright, H. L. Holt, D. H. Solomon, E. Yelin, A. D. Paltiel, and J. N. Katz. Cost-effectiveness of total knee arthroplasty in the United States: patient risk and hospital volume. Arch. Intern. Med. 169:1113–1121; discussion 1121–1122, 2009.

  33. MacLean, K. F., J. P. Callaghan, and M. R. Maly. Effect of obesity on knee joint biomechanics during gait in young adults. Cogent Med. 3:1173778, 2016.

    Article  Google Scholar 

  34. Messier, S. P., D. J. Gutekunst, C. Davis, and P. DeVita. Weight loss reduces knee-joint loads in overweight and obese older adults with knee osteoarthritis. Arthritis Rheum. 52:2026–2032, 2005.

    Article  PubMed  Google Scholar 

  35. Mononen, M. E., J. S. Jurvelin, and R. K. Korhonen. Implementation of a gait cycle loading into healthy and meniscectomised knee joint models with fibril-reinforced articular cartilage. Comput. Methods Biomech. Biomed. Eng. 18:141–152, 2015.

    Article  Google Scholar 

  36. Mononen, M. E., P. Tanska, H. Isaksson, and R. K. Korhonen. A novel method to simulate the progression of collagen degeneration of cartilage in the knee: data from the osteoarthritis initiative. Sci. Rep. 6:21415, 2016.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Mow, V. C., W. Y. Gu, and F. H. Chen. Structure and function of articular cartilage and meniscus. In: Basic Orthopaedic Biomechanics & Mechano-Biology, edited by V. C. Mow, and R. Huiskes. Sydney: Lippincott Williams & Wilkins, 2005, pp. 181–258.

    Google Scholar 

  38. Mow, V. C., and R. Huiskes. Basic Orthopaedic Biomechanics & Mechano-Biology. Sydney: Lippincott Williams & Wilkins, 2005.

    Google Scholar 

  39. Mow, V. C., and A. Ratcliffe. Structure and function of articular cartilage and meniscus. Basic Orthop. Biomech. 2:113–177, 1997.

    Google Scholar 

  40. Nevitt, M. C., and D. T. Felson. Sex hormones and the risk of osteoarthritis in women: epidemiological evidence. Ann. Rheum. Dis. 55:673–676, 1996.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Patwari, P., D. M. Cheng, A. A. Cole, K. E. Kuettner, and A. J. Grodzinsky. Analysis of the relationship between peak stress and proteoglycan loss following injurious compression of human post-mortem knee and ankle cartilage. Biomech. Model. Mechanobiol. 6:83–89, 2007.

    Article  PubMed  Google Scholar 

  42. Räsänen, L. P., P. Tanska, M. E. Mononen, E. Lammentausta, Š. Zbýň, M. S. Venäläinen, P. Szomolanyi, C. C. van Donkelaar, J. S. Jurvelin, and S. Trattnig. Spatial variation of fixed charge density in knee joint cartilage from sodium MRI–implication on knee joint mechanics under static loading. J. Biomech. 49:3387–3396, 2016.

    Article  PubMed  Google Scholar 

  43. Ravaud, P., B. Giraudeau, G. R. Auleley, C. Chastang, S. Poiraudeau, X. Ayral, and M. Dougados. Radiographic assessment of knee osteoarthritis: reproducibility and sensitivity to change. J. Rheumatol. 23:1756–1764, 1996.

    CAS  PubMed  Google Scholar 

  44. Seedhom, B. B. Conditioning of cartilage during normal activities is an important factor in the development of osteoarthritis. Rheumatology (Oxford) 45:146–149, 2006.

    Article  CAS  Google Scholar 

  45. Segal, N. A., C. Findlay, K. Wang, J. C. Torner, and M. C. Nevitt. The longitudinal relationship between thigh muscle mass and the development of knee osteoarthritis. Osteoarthr. Cartil. 20:1534–1540, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Shirazi, R., and A. Shirazi-Adl. Computational biomechanics of articular cartilage of human knee joint: effect of osteochondral defects. J. Biomech. 42:2458–2465, 2009.

    Article  CAS  PubMed  Google Scholar 

  47. Sowers, M. R., and C. A. Karvonen-Gutierrez. The evolving role of obesity in knee osteoarthritis. Curr. Opin. Rheumatol. 22:533–537, 2010.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Sturm, R., and A. Hattori. Morbid obesity rates continue to rise rapidly in the United States. Int. J. Obes. 37:889–891, 2013.

    Article  CAS  Google Scholar 

  49. Twells, L. K., D. M. Gregory, J. Reddigan, and W. K. Midodzi. Current and predicted prevalence of obesity in Canada: a trend analysis. CMAJ Open 2:E18–E26, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Vaziri, A., H. Nayeb-Hashemi, A. Singh, and B. A. Tafti. Influence of meniscectomy and meniscus replacement on the stress distribution in human knee joint. Ann. Biomed. Eng. 36:1335–1344, 2008.

    Article  PubMed  Google Scholar 

  51. Vismara, L., M. Romei, M. Galli, A. Montesano, G. Baccalaro, M. Crivellini, and G. Grugni. Clinical implications of gait analysis in the rehabilitation of adult patients with “Prader-Willi” Syndrome: a cross-sectional comparative study (“Prader-Willi” Syndrome vs matched obese patients and healthy subjects). J. Neuroeng. Rehabil. 4:14, 2007.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Wilson, W., C. Van Donkelaar, B. Van Rietbergen, K. Ito, and R. Huiskes. Stresses in the local collagen network of articular cartilage: a poroviscoelastic fibril-reinforced finite element study. J. Biomech. 37:357–366, 2004.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The research leading to results in the manuscript has received funding from the University of Oulu (strategic funding), the Medical Research Center of University of Oulu and Oulu University Hospital, Academy of Finland (Grants 286526, 268378 and 305138), Sigrid Juselius Foundation, and Finnish Cultural Foundation (North Savo regional fund, Grant No. 65142194). The OAI is a public–private partnership comprised of five contracts (N01-AR-2-2258; N01-AR-2-2259; N01-AR-2-2260; N01-AR-2-2261; N01-AR-2-2262) funded by the National Institutes of Health, a branch of the Department of Health and Human Services, and conducted by the OAI Study Investigators. Private funding partners include Merck Research Laboratories; Novartis Pharmaceuticals Corporation, GlaxoSmithKline; and Pfizer, Inc. Private sector funding for the OAI is managed by the Foundation for the National Institutes of Health. This manuscript was prepared using an OAI public use data set and does not necessarily reflect the opinions or views of the OAI investigators, the NIH, or the private funding partners.

Author information

Authors and Affiliations

  1. Research Unit of Medical Imaging, Physics and Technology, University of Oulu, P.O. Box 8000, 90014, Oulu, Finland

    Olesya Klets, Miika T. Nieminen & Simo Saarakkala

  2. Medical Research Center Oulu, University of Oulu, P.O. Box 8000, Oulu, Finland

    Olesya Klets, Miika T. Nieminen & Simo Saarakkala

  3. Department of Applied Physics, University of Eastern Finland, PL 1627, Kuopio, Finland

    Mika E. Mononen, Mimmi K. Liukkonen & Rami K. Korhonen

  4. Department of Diagnostic Radiology, Oulu University Hospital, P.O. Box 50, Oulu, Finland

    Mika T. Nevalainen, Miika T. Nieminen & Simo Saarakkala

  5. Diagnostic Imaging Centre, Kuopio University Hospital, P.O. Box 100, Kuopio, Finland

    Rami K. Korhonen

Authors
  1. Olesya Klets
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mika E. Mononen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mimmi K. Liukkonen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mika T. Nevalainen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Miika T. Nieminen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Simo Saarakkala
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Rami K. Korhonen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Olesya Klets.

Additional information

Associate Editor Estefanía Peña oversaw the review of this article.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 607 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Klets, O., Mononen, M.E., Liukkonen, M.K. et al. Estimation of the Effect of Body Weight on the Development of Osteoarthritis Based on Cumulative Stresses in Cartilage: Data from the Osteoarthritis Initiative. Ann Biomed Eng 46, 334–344 (2018). https://doi.org/10.1007/s10439-017-1974-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-017-1974-6

Keywords

Search

Navigation