Risk factors and the natural history of accelerated knee osteoarthritis: a narrative review

Jeffrey B Driban, Matthew S Harkey, Mary F Barbe, Robert J Ward, James W MacKay, Julie E Davis, Bing Lu, Lori Lyn Price, Charles B Eaton, Grace H Lo, Timothy E McAlindon, Jeffrey B Driban, Matthew S Harkey, Mary F Barbe, Robert J Ward, James W MacKay, Julie E Davis, Bing Lu, Lori Lyn Price, Charles B Eaton, Grace H Lo, Timothy E McAlindon

Abstract

Background: Osteoarthritis is generally a slowly progressive disorder. However, at least 1 in 7 people with incident knee osteoarthritis develop an abrupt progression to advanced-stage radiographic disease, many within 12 months. We summarize what is known - primarily based on findings from the Osteoarthritis Initiative - about the risk factors and natural history of accelerated knee osteoarthritis (AKOA) - defined as a transition from no radiographic knee osteoarthritis to advanced-stage disease < 4 years - and put these findings in context with typical osteoarthritis (slowly progressing disease), aging, prior case reports/series, and relevant animal models. Risk factors in the 2 to 4 years before radiographic manifestation of AKOA (onset) include older age, higher body mass index, altered joint alignment, contralateral osteoarthritis, greater pre-radiographic disease burden (structural, symptoms, and function), or low fasting glucose. One to 2 years before AKOA onset people often exhibit rapid articular cartilage loss, larger bone marrow lesions and effusion-synovitis, more meniscal pathology, slower chair-stand or walking pace, and increased global impact of arthritis than adults with typical knee osteoarthritis. Increased joint symptoms predispose a person to new joint trauma, which for someone who develops AKOA is often characterized by a destabilizing meniscal tear (e.g., radial or root tear). One in 7 people with AKOA onset subsequently receive a knee replacement during a 9-year period. The median time from any increase in radiographic severity to knee replacement is only 2.3 years. Despite some similarities, AKOA is different than other rapidly progressive arthropathies and collapsing these phenomena together or extracting results from one type of osteoarthritis to another should be avoided until further research comparing these types of osteoarthritis is conducted. Animal models that induce meniscal damage in the presence of other risk factors or create an incongruent distribution of loading on joints create an accelerated form of osteoarthritis compared to other models and may offer insights into AKOA.

Conclusion: Accelerated knee osteoarthritis is unique from typical knee osteoarthritis. The incidence of AKOA in the Osteoarthritis Initiative and Chingford Study is substantial. AKOA needs to be taken into account and studied in epidemiologic studies and clinical trials.

Keywords: Knee; Magnetic resonance imaging; Meniscus; Natural history; Osteoarthritis; Phenotype; Radiography; Risk factors.

Conflict of interest statement

JBD, MFB, and MSH are members of the Editorial Board of BMC Musculoskeletal Disorders. JBD also reported payment for lectures from Pfizer, Inc. and consultancy from Pfizer/Lilly. TEM reported consultancy from Pfizer, Sanofi Aventis US, Kolon Tissuegene, Samumed, Seikagaku, Kiniksa Pharmaceuticals, and Anika Therapeutics. The other authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
The distribution people across groups that develop accelerated, typical, or no knee osteoarthritis (KOA). The distribution of subsets of people in the Osteoarthritis Initiative defined by age, body mass index, and injury across groups that develop accelerated, typical, or no knee osteoarthritis (KOA) [10]. The percentages in the data table are based on the percent of people with accelerated, typical, or no KOA that are in each subset (each column adds to ~ 100% due to rounding) [10]
Fig. 2
Fig. 2
Phases of the Natural History of Accelerated Knee Osteoarthritis

References

    1. Driban JB, Eaton CB, Lo GH, Ward RJ, Lu B, McAlindon TE. Association of knee injuries with accelerated knee osteoarthritis progression: data from the osteoarthritis initiative. Arthritis Care Res (Hoboken) 2014;66(11):1673–1679.
    1. Driban JB, Bannuru RR, Eaton CB, Spector TD, Hart DJ, McAlindon TE, Lu B, Lo GH, Arden NK. The incidence and characteristics of accelerated knee osteoarthritis among women: the Chingford cohort. BMC Musculoskelet Disord. 2020;21(1):60.
    1. Driban JB, Stout AC, Lo GH, Eaton CB, Price LL, Lu B, Barbe MF, McAlindon TE. Best performing definition of accelerated knee osteoarthritis: data from the osteoarthritis initiative. Ther Adv Musculoskelet Dis. 2016;8(5):165–171.
    1. Riddle DL, Stratford PW, Perera RA. The incident tibiofemoral osteoarthritis with rapid progression phenotype: development and validation of a prognostic prediction rule. Osteoarthr Cartil. 2016;24(12):2100–2107.
    1. Driban JB, Price LL, Eaton CB, Lu B, Lo GH, Lapane KL, McAlindon TE. Individuals with incident accelerated knee osteoarthritis have greater pain than those with common knee osteoarthritis progression: data from the osteoarthritis initiative. Clin Rheumatol. 2016;35(6):1565–1571.
    1. Davis J, Eaton CB, Lo GH, Lu B, Price LL, McAlindon TE, Barbe MF, Driban JB. Knee symptoms among adults at risk for accelerated knee osteoarthritis: data from the osteoarthritis initiative. Clin Rheumatol. 2017;36(5):1083–1089.
    1. Davis JE, Liu SH, Lapane K, Harkey MS, Price LL, Lu B, Lo GH, Eaton CB, Barbe MF, McAlindon TE, et al. Adults with incident accelerated knee osteoarthritis are more likely to receive a knee replacement: data from the osteoarthritis initiative. Clin Rheumatol. 2018;37(4):1115–1118.
    1. Driban JB, Davis JE, Lu B, Price LL, Ward RJ, MacKay JW, Eaton CB, Lo GH, Barbe MF, Zhang M, et al. Accelerated knee osteoarthritis is characterized by destabilizing meniscal tears and Preradiographic structural disease burden. Arthritis Rheumatol. 2019;71(7):1089–1100.
    1. Davis JE, Price LL, Lo GH, Eaton CB, McAlindon TE, Lu B, Barbe MF, Driban JB. A single recent injury is a potent risk factor for the development of accelerated knee osteoarthritis: data from the osteoarthritis initiative. Rheumatol Int. 2017;37(10):1759–1764.
    1. Driban JB, Eaton CB, Lo GH, Price LL, Lu B, Barbe MF, McAlindon TE. Overweight older adults, particularly after an injury, are at high risk for accelerated knee osteoarthritis: data from the osteoarthritis initiative. Clin Rheumatol. 2016;35(4):1071–1076.
    1. Price LL, Harkey MS, Ward RJ, MacKay JW, Zhang M, Pang J, Davis JE, McAlindon TE, Lo GH, Amin M, et al. Role of magnetic resonance imaging in classifying individuals who will develop accelerated radiographic knee osteoarthritis. J Orthop Res. 2019;37(11):2420–2428.
    1. Driban JB, McAlindon TE, Amin M, Price LL, Eaton CB, Davis JE, Lu B, Lo GH, Duryea J, Barbe MF. Risk factors can classify individuals who develop accelerated knee osteoarthritis: data from the osteoarthritis initiative. J Orthop Res. 2018;36(3):876–880.
    1. Driban JB, Eaton CB, Amin M, Stout AC, Price LL, Lu B, Lo GH, McAlindon TE, Barbe MF. Glucose homeostasis influences the risk of incident knee osteoarthritis: data from the osteoarthritis initiative. J Orthop Res. 2017;35(10):2282–2287.
    1. Driban JB, Stout AC, Duryea J, Lo GH, Harvey WF, Price LL, Ward RJ, Eaton CB, Barbe MF, Lu B, et al. Coronal tibial slope is associated with accelerated knee osteoarthritis: data from the osteoarthritis initiative. BMC Musculoskelet Disord. 2016;17:299.
    1. Harkey MS, Davis JE, Lu B, Price LL, Ward RJ, MacKay JW, Eaton CB, Lo GH, Barbe MF, Zhang M, et al. Early pre-radiographic structural pathology precedes the onset of accelerated knee osteoarthritis. BMC Musculoskelet Disord. 2019;20(1):241.
    1. Davis JE, Ward RJ, MacKay JW, Lu B, Price LL, McAlindon TE, Eaton CB, Barbe MF, Lo GH, Harkey MS, et al. Effusion-synovitis and infrapatellar fat pad signal intensity alteration differentiate accelerated knee osteoarthritis. Rheumatology (Oxford) 2019;58(3):418–426.
    1. Stout AC, Barbe MF, Eaton CB, Amin M, Al-Eid F, Price LL, Lu B, Lo GH, Zhang M, Pang J, et al. Inflammation and glucose homeostasis are associated with specific structural features among adults without knee osteoarthritis: a cross-sectional study from the osteoarthritis initiative. BMC Musculoskelet Disord. 2018;19(1):1.
    1. Wang X, Jin X, Han W, Cao Y, Halliday A, Blizzard L, Pan F, Antony B, Cicuttini F, Jones G, et al. Cross-sectional and longitudinal associations between knee joint effusion Synovitis and knee pain in older adults. J Rheumatol. 2016;43(1):121–130.
    1. Javaid MK, Kiran A, Guermazi A, Kwoh CK, Zaim S, Carbone L, Harris T, McCulloch CE, Arden NK, Lane NE, et al. Individual magnetic resonance imaging and radiographic features of knee osteoarthritis in subjects with unilateral knee pain: the health, aging, and body composition study. Arthritis Rheum. 2012;64(10):3246–3255.
    1. Hunter DJ, Zhang W, Conaghan PG, Hirko K, Menashe L, Li L, Reichmann WM, Losina E. Systematic review of the concurrent and predictive validity of MRI biomarkers in OA. Osteoarthr Cartil. 2011;19(5):557–588.
    1. Yusuf E, Kortekaas MC, Watt I, Huizinga TW, Kloppenburg M. Do knee abnormalities visualised on MRI explain knee pain in knee osteoarthritis? A systematic review. Ann Rheum Dis. 2011;70(1):60–67.
    1. Wang X, Jin X, Blizzard L, Antony B, Han W, Zhu Z, Cicuttini F, Wluka AE, Winzenberg T, Jones G, et al. Associations between knee effusion-synovitis and joint structural changes in patients with knee osteoarthritis. J Rheumatol. 2017;44(11):1644–1651.
    1. Roemer FW, Guermazi A, Felson DT, Niu J, Nevitt MC, Crema MD, Lynch JA, Lewis CE, Torner J, Zhang Y. Presence of MRI-detected joint effusion and synovitis increases the risk of cartilage loss in knees without osteoarthritis at 30-month follow-up: the MOST study. Ann Rheum Dis. 2011;70(10):1804–1809.
    1. Palmieri RM, Weltman A, Edwards JE, Tom JA, Saliba EN, Mistry DJ, Ingersoll CD. Pre-synaptic modulation of quadriceps arthrogenic muscle inhibition. Knee Surg Sports TraumatolArthrosc. 2005;13(5):370–376.
    1. Palmieri RM, Tom JA, Edwards JE, Weltman A, Saliba EN, Mistry DJ, Ingersoll CD. Arthrogenic muscle response induced by an experimental knee joint effusion is mediated by pre- and post-synaptic spinal mechanisms. J ElectromyogrKinesiol. 2004;14(6):631–640.
    1. Palmieri RM, Ingersoll CD, Edwards JE, Hoffman MA, Stone MB, Babington JP, Cordova ML, Krause BA. Arthrogenic muscle inhibition is not present in the limb contralateral to a simulated knee joint effusion. Am J Phys Med Rehabil. 2003;82(12):910–916.
    1. Hovis KK, Alizai H, Tham S-C, Souza RB, Nevitt MC, McCulloch CE, Link TM. Non-traumatic anterior cruciate ligament abnormalities and their relationship to osteoarthritis using morphological grading and cartilage T2 relaxation times: data from the osteoarthritis initiative (OAI) Skelet Radiol. 2012;41(11):1435–1443.
    1. Guermazi A, Hayashi D, Jarraya M, Roemer FW, Zhang Y, Niu J, Crema MD, Englund M, Lynch JA, Nevitt MC, et al. Medial posterior meniscal root tears are associated with development or worsening of medial tibiofemoral cartilage damage: the multicenter osteoarthritis study. Radiology. 2013;268(3):814–821.
    1. Krych AJ, Reardon PJ, Johnson NR, Mohan R, Peter L, Levy BA, Stuart MJ. Non-operative management of medial meniscus posterior horn root tears is associated with worsening arthritis and poor clinical outcome at 5-year follow-up. Knee Surg Sports Traumatol Arthrosc. 2017;25(2):383–389.
    1. Driban JB, Barr AE, Amin M, Sitler MR, Barbe MF. Joint inflammation and early degeneration induced by high force reaching are attenuated by ibuprofen in an animal model of work-related musculoskeletal disorder. J Biomed Biotechnol. 2011;2011:691412.
    1. Harkey MS, Davis JE, Lu B, Price LL, Eaton CB, Lo GH, Barbe MF, Ward RJ, Zhang M, Liu SH, et al. Diffuse tibiofemoral cartilage change prior to the development of accelerated knee osteoarthritis: data from the osteoarthritis initiative. Clin Anat. 2019;32(3):369–378.
    1. Davis JE, Harkey MS, Ward RJ, Mackay JW, Lu B, Price LL, Eaton CB, Barbe MF, Lo GH, McAlindon TE, et al. Characterizing the distinct structural changes associated with self-reported knee injury among individuals with incident knee osteoarthritis: data from the osteoarthritis initiative. Clin Anat. 2018;31(3):330–334.
    1. Glasson SS, Blanchet TJ, Morris EA. The surgical destabilization of the medial meniscus (DMM) model of osteoarthritis in the 129/SvEv mouse. Osteoarthr Cartil. 2007;15(9):1061–1069.
    1. Ma HL, Blanchet TJ, Peluso D, Hopkins B, Morris EA, Glasson SS. Osteoarthritis severity is sex dependent in a surgical mouse model. Osteoarthr Cartil. 2007;15(6):695–700.
    1. McNulty MA, Loeser RF, Davey C, Callahan MF, Ferguson CM, Carlson CS. Histopathology of naturally occurring and surgically induced osteoarthritis in mice. Osteoarthr Cartil. 2012;20(8):949–956.
    1. Meckes JK, Carames B, Olmer M, Kiosses WB, Grogan SP, Lotz MK, D'Lima DD. Compromised autophagy precedes meniscus degeneration and cartilage damage in mice. Osteoarthr Cartil. 2017;25(11):1880–1889.
    1. Huang H, Skelly JD, Ayers DC, Song J. Age-dependent changes in the articular cartilage and Subchondral bone of C57BL/6 mice after surgical destabilization of medial meniscus. Sci Rep. 2017;7:42294.
    1. Datta P, Zhang Y, Parousis A, Sharma A, Rossomacha E, Endisha H, Wu B, Kacprzak I, Mahomed NN, Gandhi R, et al. High-fat diet-induced acceleration of osteoarthritis is associated with a distinct and sustained plasma metabolite signature. Sci Rep. 2017;7(1):8205.
    1. Driban JB, Ward RJ, Eaton CB, Lo GH, Price LL, Lu B, McAlindon TE. Meniscal extrusion or subchondral damage characterize incident accelerated osteoarthritis: data from the osteoarthritis initiative. Clin Anat. 2015;28(6):792–799.
    1. Foreman SC, Neumann J, Joseph GB, Nevitt MC, McCulloch CE, Lane NE, Link TM. Longitudinal MRI structural findings observed in accelerated knee osteoarthritis: data from the osteoarthritis initiative. Skelet Radiol. 2019.
    1. Jain NX, Barr-Gillespie AE, Clark BD, Kietrys DM, Wade CK, Litvin J, Popoff SN, Barbe MF. Bone loss from high repetitive high force loading is prevented by ibuprofen treatment. J Musculoskelet Neuronal Interact. 2014;14(1):78–94.
    1. Li H, Li J, Zou Z, Fok AS. Fracture simulation of restored teeth using a continuum damage mechanics failure model. Dent Mater. 2011;27(7):e125–e133.
    1. Turner CH. Biomechanics of bone: determinants of skeletal fragility and bone quality. Osteoporosis international : a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA. 2002;13(2):97–104.
    1. Gallagher S, Schall MC., Jr Musculoskeletal disorders as a fatigue failure process: evidence, implications and research needs. Ergonomics. 2017;60(2):255–269.
    1. Davis JE, Harkey MS, Liu S-H, Lapane K, Price LL, Lu B, Lo GH, Eaton CB, Barbe MF, McAlindon TE et al: Adults With Incident Accelerated Knee Osteoarthritis Are More Likely to Use Pharmacological Treatment Options and Receive Arthroscopic Knee Surgery: Data From the Osteoarthritis Initiative. ACR Open Rheumatology 2019, 0(0).
    1. Roemer FW, Hayes CW, Miller CG, Hoover K, Guermazi A. Imaging atlas for eligibility and on-study safety of potential shoulder adverse events in anti-NGF studies (part 3) Osteoarthr Cartil. 2015;23(Suppl 1):S59–S68.
    1. Wesseling J, Bierma-Zeinstra SM, Kloppenburg M, Meijer R, Bijlsma JW. Worsening of pain and function over 5 years in individuals with 'early' OA is related to structural damage: data from the osteoarthritis initiative and CHECK (Cohort hip & Cohort Knee) study. Ann Rheum Dis. 2015;74(2):347–353.
    1. Neogi T., Niu J., Duryea J., Lynch J., Zhang Y. Identifying trajectories of medial joint-space width loss and associated risk factors. Osteoarthritis and Cartilage. 2012;20:S182–S183.
    1. Bartlett Susan J., Ling Shari M., Mayo Nancy E., Scott Susan C., Bingham Clifton O. Identifying common trajectories of joint space narrowing over two years in knee osteoarthritis. Arthritis Care & Research. 2011;63(12):1722–1728.
    1. Lequesne M. Les coxopathies rapidement destructices inattendues. La Presse Med. 1970;78.
    1. Hochberg MC. Serious joint-related adverse events in randomized controlled trials of anti-nerve growth factor monoclonal antibodies. Osteoarthr Cartil. 2015;23(Suppl 1):S18–S21.
    1. Roemer FW, Hayes CW, Miller CG, Hoover K, Guermazi A. Imaging atlas for eligibility and on-study safety of potential knee adverse events in anti-NGF studies (part 1) Osteoarthr Cartil. 2015;23(Suppl 1):S22–S42.
    1. Hochberg MC, Tive LA, Abramson SB, Vignon E, Verburg KM, West CR, Smith MD, Hungerford DS: When Is Osteonecrosis Not Osteonecrosis?: Adjudication of Reported Serious Adverse Joint Events in the Tanezumab Clinical Development Program. Arthritis & rheumatology (Hoboken, NJ) 2016, 68(2):382–391.
    1. Driban J.B., Eaton C.B., Lo G.H., Barbe M.F., Ward R.J., Lu B., McAlindon T.E. Knee injuries are associated with the onset of rapid knee osteoarthritis: data from the osteoarthritis initiative. Osteoarthritis and Cartilage. 2014;22:S32–S33.
    1. Flemming DJ, Gustas-French CN. Rapidly progressive osteoarthritis: a review of the clinical and radiologic presentation. Curr Rheumatol Rep. 2017;19(7):42.
    1. Roemer FW, Hayes CW, Miller CG, Hoover K, Guermazi A. Imaging atlas for eligibility and on-study safety of potential hip adverse events in anti-NGF studies (part 2) Osteoarthr Cartil. 2015;23(Suppl 1):S43–S58.
    1. Karsdal MA, Verburg KM, West CR, Bay-Jensen AC, Keller DS, Arends R. Serological biomarker profiles of rapidly progressive osteoarthritis in tanezumab-treated patients. Osteoarthr Cartil. 2019;27(3):484–492.
    1. Davis JE, Schaefer LF, McAlindon TE, Eaton CB, Roberts MB, Haugen IK, Smith SE, Duryea J, Lu B, Driban JB. Characteristics of accelerated hand osteoarthritis: data from the osteoarthritis initiative. J Rheumatol. 2019;46(4):422–428.

Source: PubMed

3
Subskrybuj