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AGE

, 36:9669 | Cite as

Life-long caloric restriction does not alter the severity of age-related osteoarthritis

  • Jenna N. McNeill
  • Chia-Lung Wu
  • Karyne N. Rabey
  • Daniel Schmitt
  • Farshid GuilakEmail author
Article

Abstract

Chronic adipose tissue inflammation and its associated adipokines have been linked to the development of osteoarthritis (OA). It has been shown that caloric restriction may decrease body mass index and adiposity. The objectives of this study were to investigate the effect of lifelong caloric restriction on bone morphology, joint inflammation, and spontaneously occurring OA development in aged mice. C57BL/NIA mice were fed either a calorie-restricted (CR) or ad libitum (AL) diet starting at 14 weeks of age. All mice were sacrificed at 24 months of age. Adipose tissue and knee joints were then harvested. Bone parameters of the joints were analyzed by micro-CT. OA and joint synovitis were determined using histology and semiquantitative analysis. Lifelong caloric restriction did not alter the severity of OA development in C57BL/NIA aged mice, and there was no difference in the total joint Mankin score between CR and AL groups (p = 0.99). Mice also exhibited similar levels of synovitis (p = 0.54). The bone mineral density of the femur and the tibia was comparable between the groups with a small increase in cancellous bone volume fraction in the lateral femoral condyle of the CR group compared with the AL group. Lifelong caloric restriction did not alter the incidence of OA or joint synovitis in C57BL/NIA mice, indicating that a reduction of caloric intake alone was not sufficient to prevent spontaneous age-related OA. Nonetheless, early initiation of CR continued throughout a life span did not negatively impact bone structural properties.

Keywords

Osteoarthritis Bone density Synovitis Inflammation Osteoporosis 

Notes

Acknowledgments

The authors would like to thank Steve Johnson for assistance with animal handling and Dr. Mark Hamrick with his assistance in acquiring the mice. This study was supported in part by NIH grants AG46927, AR50245, AG15768, AR48852, and AR48182.

References

  1. Ageberg E, Engstrom G, Gerhardsson de Verdier M, Rollof J, Roos EM, Lohmander LS (2012) Effect of leisure time physical activity on severe knee or hip osteoarthritis leading to total joint replacement: a population-based prospective cohort study. BMC Musculoskelet Disord 13:73. doi: 10.1186/1471-2474-13-73 PubMedCentralPubMedCrossRefGoogle Scholar
  2. Amin S et al (2007) Cigarette smoking and the risk for cartilage loss and knee pain in men with knee osteoarthritis. Ann Rheum Dis 66:18–22. doi: 10.1136/ard.2006.056697 PubMedCentralPubMedCrossRefGoogle Scholar
  3. Aspden RM (2011) Obesity punches above its weight in osteoarthritis. Nat Rev Rheumatol 7:65–68. doi: 10.1038/nrrheum.2010.123 PubMedCrossRefGoogle Scholar
  4. Athanasiou KA, Zhu CF, Wang X, Agrawal CM (2000) Effects of aging and dietary restriction on the structural integrity of rat articular cartilage. Ann Biomed Eng 28:143–149PubMedCrossRefGoogle Scholar
  5. Bendele AM, Hulman JF (1991) Effects of body weight restriction on the development and progression of spontaneous osteoarthritis in guinea pigs. Arthritis Rheum 34:1180–1184PubMedCrossRefGoogle Scholar
  6. Brochmann EJ, Duarte ME, Zaidi HA, Murray SS (2003) Effects of dietary restriction on total body, femoral, and vertebral bone in sencar, C57BL/6, and DBA/2 mice. Metab Clin Exp 52:1265–1273PubMedCrossRefGoogle Scholar
  7. Costello KE, Guilak F, Setton LA, Griffin TM (2010) Locomotor activity and gait in aged mice deficient for type IX collagen. J Appl Physiol 109:211–218. doi: 10.1152/japplphysiol.00056.2010 PubMedCentralPubMedCrossRefGoogle Scholar
  8. Felson DT et al (2000) Osteoarthritis: new insights. Part 1: the disease and its risk factors. Ann Intern Med 133:635–646PubMedCrossRefGoogle Scholar
  9. Felson DT, Niu J, Clancy M, Sack B, Aliabadi P, Zhang Y (2007) Effect of recreational physical activities on the development of knee osteoarthritis in older adults of different weights: the framingham study. Arthritis Rheum 57:6–12. doi: 10.1002/art.22464 PubMedCrossRefGoogle Scholar
  10. Fernandes JC, Martel-Pelletier J, Pelletier JP (2002) The role of cytokines in osteoarthritis pathophysiology. Biorheology 39:237–246PubMedGoogle Scholar
  11. Fontana L, Klein S (2007) Aging, adiposity, and calorie restriction. JAMA:J Am Med Assoc 297:986–994. doi: 10.1001/jama.297.9.986 CrossRefGoogle Scholar
  12. Forster MJ, Lal H (1999) Estimating age-related changes in psychomotor function: influence of practice and of level of caloric intake in different genotypes. Neurobiol Aging 20:167–176PubMedCrossRefGoogle Scholar
  13. Garrett IR, Boyce BF, Oreffo RO, Bonewald L, Poser J, Mundy GR (1990) Oxygen-derived free radicals stimulate osteoclastic bone resorption in rodent bone in vitro and in vivo. J Clin Invest 85:632–639. doi: 10.1172/JCI114485 PubMedCentralPubMedCrossRefGoogle Scholar
  14. Goldring MB (2012) Articular cartilage degradation in osteoarthritis. HSS J: Musculoskelet J Hosp Spec Surg 8:7–9. doi: 10.1007/s11420-011-9250-z CrossRefGoogle Scholar
  15. Griffin TM et al (2010) Diet-induced obesity differentially regulates behavioral, biomechanical, and molecular risk factors for osteoarthritis in mice. Arthritis Res Ther 12:R130. doi: 10.1186/ar3068 PubMedCentralPubMedCrossRefGoogle Scholar
  16. Griffin TM, Guilak F (2008) Why is obesity associated with osteoarthritis? insights from mouse models of obesity. Biorheology 45:387–398PubMedCentralPubMedGoogle Scholar
  17. Griffin TM, Huebner JL, Kraus VB, Guilak F (2009) Extreme obesity due to impaired leptin signaling in mice does not cause knee osteoarthritis. Arthritis Rheum 60:2935–2944. doi: 10.1002/art.24854 PubMedCentralPubMedCrossRefGoogle Scholar
  18. Griffin TM, Huebner JL, Kraus VB, Yan Z, Guilak F (2012) Induction of osteoarthritis and metabolic inflammation by a very high-fat diet in mice: effects of short-term exercise. Arthritis Rheum 64:443–453. doi: 10.1002/art.33332 PubMedCentralPubMedCrossRefGoogle Scholar
  19. Guilak F (2011) Biomechanical factors in osteoarthritis. Best Pract Res Clin Rheumatol 25:815–823. doi: 10.1016/j.berh.2011.11.013 PubMedCentralPubMedCrossRefGoogle Scholar
  20. Hawkins J, Cifuentes M, Pleshko NL, Ambia-Sobhan H, Shapses SA (2010) Energy restriction is associated with lower bone mineral density of the tibia and femur in lean but not obese female rats. J Nutr 140:31–37. doi: 10.3945/jn.109.111450 PubMedCentralPubMedCrossRefGoogle Scholar
  21. Huck JL et al (2009) A longitudinal study of the influence of lifetime food restriction on development of osteoarthritis in the canine elbow. Vet Sur: VS 38:192–198. doi: 10.1111/j.1532-950X.2008.00487.x CrossRefGoogle Scholar
  22. Hugle T, Geurts J, Nuesch C, Muller-Gerbl M, Valderrabano V (2012) Aging and osteoarthritis: an inevitable encounter? J Aging Res 2012:950192. doi: 10.1155/2012/950192 PubMedCentralPubMedCrossRefGoogle Scholar
  23. Hunter DJ et al (2007a) Cartilage markers and their association with cartilage loss on magnetic resonance imaging in knee osteoarthritis: the boston osteoarthritis knee study. Arthritis Research & Therapy 9:R108. doi: 10.1186/ar2314 CrossRefGoogle Scholar
  24. Hunter DJ et al (2007b) Knee alignment does not predict incident osteoarthritis: the framingham osteoarthritis study. Arthritis Rheum 56:1212–1218. doi: 10.1002/art.22508 PubMedCrossRefGoogle Scholar
  25. Kalichman L, Zhang Y, Niu J, Goggins J, Gale D, Felson DT, Hunter D (2007a) The association between patellar alignment and patellofemoral joint osteoarthritis features—an MRI study. Rheumatology (Oxford) 46:1303–1308. doi: 10.1093/rheumatology/kem095 CrossRefGoogle Scholar
  26. Kalichman L, Zhu Y, Zhang Y, Niu J, Gale D, Felson DT, Hunter D (2007b) The association between patella alignment and knee pain and function: an MRI study in persons with symptomatic knee osteoarthritis. Osteoar Cartil/OARS, Osteoarthr Res Soc 15:1235–1240. doi: 10.1016/j.joca.2007.04.014 CrossRefGoogle Scholar
  27. Kealy RD, Lawler DF, Ballam JM, Lust G, Biery DN, Smith GK, Mantz SL (2000) Evaluation of the effect of limited food consumption on radiographic evidence of osteoarthritis in dogs Journal of the American Veterinary Medical Association 217:1678–1680Google Scholar
  28. Kealy RD et al (2002) Effects of diet restriction on life span and age-related changes in dogs. J Am Vet Med Assoc 220:1315–1320PubMedCrossRefGoogle Scholar
  29. Lawler DF et al (2008) Diet restriction and ageing in the dog: major observations over two decades. Br J Nutr 99:793–805. doi: 10.1017/S0007114507871686 PubMedCrossRefGoogle Scholar
  30. Louer CR, Furman BD, Huebner JL, Kraus VB, Olson SA, Guilak F (2012) Diet-induced obesity significantly increases the severity of posttraumatic arthritis in mice. Arthritis Rheum 64:3220–3230. doi: 10.1002/art.34533 PubMedCentralPubMedCrossRefGoogle Scholar
  31. Masoro EJ (2005) Overview of caloric restriction and ageing. Mech Ageing Dev 126:913–922. doi: 10.1016/j.mad.2005.03.012 PubMedCrossRefGoogle Scholar
  32. McCay C, Crowell MF, Maynard L (1935) The effect of retarded growth upon the length of life span and upon the ultimate body size. J Nutr 10:63–79Google Scholar
  33. Means LW, Higgins JL, Fernandez TJ (1993) Mid-life onset of dietary restriction extends life and prolongs cognitive functioning. Physiol Behav 54:503–508PubMedCrossRefGoogle Scholar
  34. O'Conor CJ, Griffin TM, Liedtke W, Guilak F (2013) Increased susceptibility of Trpv4-deficient mice to obesity and obesity-induced osteoarthritis with very high-fat diet. Ann Rheum Dis 72:300–304. doi: 10.1136/annrheumdis-2012-202272 PubMedCentralPubMedCrossRefGoogle Scholar
  35. Paolisso G et al (1998) Advancing age and insulin resistance: role of plasma tumor necrosis factor-alpha. Am J Physiol 275:E294–E299PubMedGoogle Scholar
  36. Pou KM et al (2007) Visceral and subcutaneous adipose tissue volumes are cross-sectionally related to markers of inflammation and oxidative stress: the Framingham. Heart Study Circ 116:1234–1241. doi: 10.1161/CIRCULATIONAHA.107.710509 Google Scholar
  37. Runge JJ et al (2008) The effects of lifetime food restriction on the development of osteoarthritis in the canine shoulder. Veterinary Surgery: VS 37:102–107. doi: 10.1111/j.1532-950X.2007.00354.x CrossRefGoogle Scholar
  38. Schmitt D, Zumwalt AC, Hamrick MW (2010) The relationship between bone mechanical properties and ground reaction forces in normal and hypermuscular mice. J Exp Zool A Ecol Genet Physiol 313:339–351. doi: 10.1002/jez.604 PubMedCentralPubMedCrossRefGoogle Scholar
  39. Silberberg M, Silberberg R (1950) Effects of a high fat diet on the joints of aging mice. AMA Arch Pathol 50:828–846PubMedGoogle Scholar
  40. Silberberg R (1976) Obesity and joint disease. Gerontology 22:135–140PubMedCrossRefGoogle Scholar
  41. Talbott SM, Cifuentes M, Dunn MG, Shapses SA (2001) Energy restriction reduces bone density and biomechanical properties in aged female rats. The Journal of Nutrition 131:2382–2387PubMedCentralPubMedGoogle Scholar
  42. Turturro A, Witt WW, Lewis S, Hass BS, Lipman RD, Hart RW (1999) Growth curves and survival characteristics of the animals used in the biomarkers of aging program. J Gerontol A: Biol Med Sci 54:B492–B501CrossRefGoogle Scholar
  43. Weiss EP, Fontana L (2011) Caloric restriction: powerful protection for the aging heart and vasculature. Am J Physiol Heart Circ Physiol 301:H1205–H1219. doi: 10.1152/ajpheart.00685.2011 PubMedCentralPubMedCrossRefGoogle Scholar
  44. Westerbeek ZW, Hepple RT, Zernicke RF (2008) Effects of aging and caloric restriction on bone structure and mechanical properties. J Gerontol A: Biol Med Sci 63:1131–1136CrossRefGoogle Scholar
  45. Wu CL, Diekman BO, Jain D, Guilak F (2013) Diet-induced obesity alters the differentiation potential of stem cells isolated from bone marrow, adipose tissue and infrapatellar fat pad: the effects of free fatty acids. Int J Obes (Lond) 37:1079–1087. doi: 10.1038/ijo.2012.171 CrossRefGoogle Scholar
  46. You T, Sonntag WE, Leng X, Carter CS (2007) Lifelong caloric restriction and interleukin-6 secretion from adipose tissue: effects on physical performance decline in aged rats. J Gerontol A: Biol Med Sci 62:1082–1087CrossRefGoogle Scholar

Copyright information

© American Aging Association 2014

Authors and Affiliations

  • Jenna N. McNeill
    • 1
  • Chia-Lung Wu
    • 1
    • 3
  • Karyne N. Rabey
    • 2
  • Daniel Schmitt
    • 2
  • Farshid Guilak
    • 1
    • 3
    Email author
  1. 1.Department of Orthopaedic SurgeryDuke University Medical CenterDurhamUSA
  2. 2.Department of Evolutionary AnthropologyDuke University Medical CenterDurhamUSA
  3. 3.Department of Biomedical EngineeringDuke University Medical CenterDurhamUSA

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