Abstract
In the past decades, considerable efforts have been made to propose experimental and clinical treatments for articular cartilage defects. Yet, the problem of cartilage defects extending deep in the underlying subchondral bone has not received adequate attention. A profound understanding of the basic anatomic aspects of this particular site, together with the pathophysiology of diseases affecting the subchondral bone is the key to develop targeted and effective therapeutic strategies to treat osteochondral defects. The subchondral bone consists of the subchondral bone plate and the subarticular spongiosa. It is separated by the cement line from the calcified zone of the articular cartilage. A variable anatomy is characteristic for the subchondral region, reflected in differences in thickness, density, and composition of the subchondral bone plate, contour of the tidemark and cement line, and the number and types of channels penetrating into the calcified cartilage. This review aims at providing insights into the anatomy, morphology, and pathology of the subchondral bone. Individual diseases affecting the subchondral bone, such as traumatic osteochondral defects, osteochondritis dissecans, osteonecrosis, and osteoarthritis are also discussed. A better knowledge of the basic science of the subchondral region, together with additional investigations in animal models and patients may translate into improved therapies for articular cartilage defects that arise from or extend into the subchondral bone.
Similar content being viewed by others
References
Ahmed AM, Burke DL (1983) In vitro measurement of static pressure distribution in synovial joints—part I: tibial surface of the knee. J Biomech Eng 105:216–225
Anderson DV, Lyne ED (1984) Osteochondritis dissecans of the talus: case report on two family members. J Pediatr Orthop 4:356–357
Anetzberger H, Muller-Gerbl M, Scherer MA, Metak G, Blumel G, Putz R (1994) Change in subchondral mineralization after reconstruction of the anterior cruciate ligament of the sheep. Unfallchirurg 97:655–660
Arkill KP, Winlove CP (2008) Solute transport in the deep and calcified zones of articular cartilage. Osteoarthr Cartil 16:708–714
Armstrong SJ, Read RA, Price R (1995) Topographical variation within the articular cartilage and subchondral bone of the normal ovine knee joint: a histological approach. Osteoarthr Cartil 3:25–33
Aspenberg P, Van der Vis H (1998) Migration, particles, and fluid pressure. A discussion of causes of prosthetic loosening. Clin Orthop Relat Res 352:75–80
Berndt AL, Harty M (1959) Transchondral fractures (osteochondritis dissecans) of the talus. J Bone Joint Surg Am 41-A:988–1020
Berry JL, Thaeler-Oberdoerster DA, Greenwald AS (1986) Subchondral pathways to the superior surface of the human talus. Foot Ankle 7:2–9
Bhosale AM, Richardson JB (2008) Articular cartilage: structure, injuries and review of management. Br Med Bull 87:77–95
Bonde HV, Talman ML, Kofoed H (2005) The area of the tidemark in osteoarthritis—a three-dimensional stereological study in 21 patients. Apmis 113:349–352
Braune W, Fischer O (1891) Die Bewegungen des Kniegelenks nach einer neuen Methode am lebenden Menschen gemessen. Abhandlungen der mathematisch-physischen Klasse der Königlich-Sächsischen Gesellschaft der Wissenschaften 17-2, Leipzig 1891, S Hirzel 75–150
Bretlau T, Tuxoe J, Larsen L, Jorgensen U, Thomsen HS, Lausten GS (2002) Bone bruise in the acutely injured knee. Knee Surg Sports Traumatol Arthrosc 10:96–101
Brittberg M, Lindahl A, Nilsson A, Ohlsson C, Isaksson O, Peterson L (1994) Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. N Engl J Med 331:889–895
Brown TD, Vrahas MS (1984) The apparent elastic modulus of the juxtarticular subchondral bone of the femoral head. J Orthop Res 2:32–38
Buckwalter JA (2002) Articular cartilage injuries. Clin Orthop Relat Res 402:21–37
Bullough PG, Yawitz PS, Tafra L, Boskey AL (1985) Topographical variations in the morphology and biochemistry of adult canine tibial plateau articular cartilage. J Orthop Res 3:1–16
Burr DB, Radin EL (2003) Microfractures and microcracks in subchondral bone: are they relevant to osteoarthrosis? Rheum Dis Clin North Am 29:675–685
Canale ST, Belding RH (1980) Osteochondral lesions of the talus. J Bone Joint Surg Am 62:97–102
Choi K, Kuhn JL, Ciarelli MJ, Goldstein SA (1990) The elastic moduli of human subchondral, trabecular, and cortical bone tissue and the size-dependency of cortical bone modulus. J Biomech 23:1103–1113
Clark JM, Huber JD (1990) The structure of the human subchondral plate. J Bone Joint Surg Br 72:866–873
Cruess RL (1986) Osteonecrosis of bone. Current concepts as to etiology and pathogenesis. Clin Orthop Relat Res 208:30–39
Cucchiarini M, Madry H, Ma C, Thurn T, Zurakowski D, Menger MD, Kohn D, Trippel SB, Terwilliger EF (2005) Improved tissue repair in articular cartilage defects in vivo by rAAV-mediated overexpression of human fibroblast growth factor 2. Mol Ther 12:229–238
Davies NH, Niall D, King LJ, Lavelle J, Healy JC (2004) Magnetic resonance imaging of bone bruising in the acutely injured knee–short-term outcome. Clin Radiol 59:439–445
Dewire P, Simkin PA (1996) Subchondral plate thickness reflects tensile stress in the primate acetabulum. J Orthop Res 14:838–841
Dore D, Quinn S, Ding C, Winzenberg T, Jones G (2009) Correlates of subchondral bone mineral density: a cross-sectional study. J Bone Miner Res 12:2007–2015
Duncan H, Riddle JM, Pitchford W (1985) Osteoarthritis and the subchondral plate. In: Verbruggen G, Veys EM (eds) Degenerative joints, vol 2. Elsevier, London, pp 181–197
Duncan H, Jundt J, Riddle JM, Pitchford W, Christopherson T (1987) The tibial subchondral plate. A scanning electron microscopic study. J Bone Joint Surg Am 69:1212–1220
Eckstein F, Muller-Gerbl M, Putz R (1992) Distribution of subchondral bone density and cartilage thickness in the human patella. J Anat 180(Pt 3):425–433
Eckstein F, Muller-Gerbl M, Steinlechner M, Kierse R, Putz R (1995) Subchondral bone density in the human elbow assessed by computed tomography osteoabsorptiometry: a reflection of the loading history of the joint surfaces. J Orthop Res 13:268–278
von Eisenhart-Rothe R, Eckstein F, Müller-Gerbl M, Landgraf J, Rock C, Putz R (1997) Direct comparison of contact areas, contact stress and subchondral mineralization in human hip joint specimens. Anat Embryol 195:279–288
Erban WK, Kolberg K (1981) Simultaneous mirror image osteochondrosis dissecans in identical twins. Rofo 135:357
Fischer H (1988) Darstellung und Anordnung der kollagenen Fibrillen in der Matrix des Gelenkknorpels. Dissertation, Albert-Ludwigs-Universitaet Freiburg, Freiburg i.Br., Germany
Furukawa T, Eyre DR, Koide S, Glimcher MJ (1980) Biochemical studies on repair cartilage resurfacing experimental defects in the rabbit knee. J Bone Joint Surg Am 62:79–89
Giunta R, Lower N, Kierse R, Wilhelm K, Muller-Gerbl M (1997) Stress on the radiocarpal joint. CT studies of subchondral bone density in vivo. Handchir Mikrochir Plast Chir 29:32–37
Goldring MB, Goldring SR (2007) Osteoarthritis. J Cell Physiol 213:626–634
Green WT Jr, Martin GN, Eanes ED, Sokoloff L (1970) Microradiographic study of the calcified layer of articular cartilage. Arch Pathol 90:151–158
Harada Y, Wevers HW, Cooke TD (1988) Distribution of bone strength in the proximal tibia. J Arthroplasty 3:167–175
Holmdahl DE, Ingelmark BE (1948) Der Bau des Gelenkknorpels unter verschiedenen funktionellen Verhaeltnissen. Experimentelle Untersuchungen am Kaninchen. Acta Anat 6:309–375
Hulth A (1993) Does osteoarthrosis depend on growth of the mineralized layer of cartilage? Clin Orthop Relat Res 287:19–24
Hunziker EB, Rosenberg LC (1996) Repair of partial-thickness defects in articular cartilage: cell recruitment from the synovial membrane. J Bone Joint Surg Am 78:721–733
Hvid I (1988) Mechanical strength of trabecular bone at the knee. Dan Med Bull 35:345–365
Hwang J, Bae WC, Shieu W, Lewis CW, Bugbee WD, Sah RL (2008) Increased hydraulic conductance of human articular cartilage and subchondral bone plate with progression of osteoarthritis. Arthritis Rheum 58:3831–3842
Imhof H, Breitenseher M, Kainberger F, Rand T, Trattnig S (1999) Importance of subchondral bone to articular cartilage in health and disease. Top Magn Reson Imaging 10:180–192
Inoue H (1981) Alterations in the collagen framework of osteoarthritic cartilage and subchondral bone. Int Orthop 5:47–52
Jackson DW, Lalor PA, Aberman HM, Simon TM (2001) Spontaneous repair of full-thickness defects of articular cartilage in a goat model. A preliminary study. J Bone Joint Surg Am 83:53–64
Johnson LL (2001) Arthroscopic abrasion arthroplasty: a review. Clin Orthop 391:306–317
Joy G, Patzakis MJ, Harvey JP Jr (1974) Precise evaluation of the reduction of severe ankle fractures. J Bone Joint Surg Am 56:979–993
Kaul G, Cucchiarini M, Arntzen D, Zurakowski D, Menger MD, Kohn D, Trippel SB, Madry H (2006) Local stimulation of articular cartilage repair by transplantation of encapsulated chondrocytes overexpressing human fibroblast growth factor 2 (FGF-2) in vivo. J Gene Med 8:100–111
Koenig F (1888) Ueber freie Koerper in den Gelenken. Deutsche Zeitschrift fuer Chirurgie 27:90–109
Koshino T, Okamoto R, Takamura K, Tsuchiya K (1979) Arthroscopy in spontaneous osteonecrosis of the knee. Orthop Clin North Am 10:609–618
Lane LB, Villacin A, Bullough PG (1977) The vascularity and remodelling of subchondrial bone and calcified cartilage in adult human femoral and humeral heads. An age- and stress-related phenomenon. J Bone Joint Surg Br 59:272–278
Layton MW, Goldstein SA, Goulet RW, Feldkamp LA, Kubinski DJ, Bole GG (1988) Examination of subchondral bone architecture in experimental osteoarthritis by microscopic computed axial tomography. Arthritis Rheum 31:1400–1405
Lotke PA, Ecker ML (1985) Osteonecrosis of the knee. Orthop Clin North Am 16:797–808
Lotz JC, Gerhart TN, Hayes WC (1991) Mechanical properties of metaphyseal bone in the proximal femur. J Biomech 24:317–329
Lyons TJ, Stoddart RW, McClure SF, McClure J (2005) The tidemark of the chondro-osseous junction of the normal human knee joint. J Mol Histol 36:207–215
Lyons TJ, McClure SF, Stoddart RW, McClure J (2006) The normal human chondro-osseous junctional region: evidence for contact of uncalcified cartilage with subchondral bone and marrow spaces. BMC Musculoskelet Disord 7:52
MacDessi SJ, Brophy RH, Bullough PG, Windsor RE, Sculco TP (2008) Subchondral fracture following arthroscopic knee surgery. A series of eight cases. J Bone Joint Surg Am 90:1007–1012
Madry H, Kaul G, Cucchiarini M, Stein U, Zurakowski D, Remberger K, Menger MD, Kohn D, Trippel SB (2005) Enhanced repair of articular cartilage defects in vivo by transplanted chondrocytes overexpressing insulin-like growth factor I (IGF-I). Gene Ther 12:1171–1179
Madry H, Pape D (2008) Autologous chondrocyte transplantation. Orthopade 37:756–763
Malinin T, Ouellette EA (2000) Articular cartilage nutrition is mediated by subchondral bone: a long-term autograft study in baboons. Osteoarthr Cartil 8:483–491
Meachim G, Allibone R (1984) Topographical variation in the calcified zone of upper femoral articular cartilage. J Anat 139(Pt 2):341–352
Milz S (1994) Lueckenbildungen der subchondralen Mineralisierungszone des Tibiaplateaus. Osteologie 3:110–118
Milz S, Putz R (1994) Quantitative morphology of the subchondral plate of the tibial plateau. J Anat 185(Pt 1):103–110
Milz S, Eckstein F, Putz R (1995) The thickness of the subchondral plate and its correlation with the thickness of the uncalcified articular cartilage in the human patella. Anat Embryol (Berl) 192:437–444
Milz S, Eckstein F, Putz R (1997) Thickness distribution of the subchondral mineralization zone of the trochlear notch and its correlation with the cartilage thickness: an expression of functional adaptation to mechanical stress acting on the humeroulnar joint? Anat Rec 248:189–197
Monro A (1856) Microgeologie. Th. Billroth, Berlin, p 236
Moyad TF, Minas T (2008) Opening wedge high tibial osteotomy: a novel technique for harvesting autograft bone. J Knee Surg 21:80–84
Muller-Gerbl M, Putz R, Hodapp N, Schulte E, Wimmer B (1989) Computed tomography-osteoabsorptiometry for assessing the density distribution of subchondral bone as a measure of long-term mechanical adaptation in individual joints. Skeletal Radiol 18:507–512
Muller-Gerbl M, Putz R, Hodapp N, Schulte E, Wimmer B (1990) Computed tomography-osteoabsorptiometry: a mehod of assessing the mechanical condition of the major joints in a living subject. Clinical Biomech 5:193–198
Müller-Gerbl M, Hodapp N, Reinbold WD, Putz R (1991) Can CT-osteoabsorptiometry be used to display the distribution of subchondral mineralization Calcif. Tissue Int 48(Suppl 1):68
Muller-Gerbl M, Putz R, Kenn R (1992) Demonstration of subchondral bone density patterns by three-dimensional CT osteoabsorptiometry as a noninvasive method for in vivo assessment of individual long-term stresses in joints. J Bone Miner Res 7(Suppl 2):S411–S418
Muller-Gerbl M (1998) The subchondral bone plate. Adv Anat Embryol Cell Biol 141:1–134
Muller-Gerbl M, Dalstra M, Ding M, Linsenmeier U, Putz R, Hvid I (1998) Distribution of strength and mineralization in the subchondral bone plate of human tibial heads. J Biomech 31(Suppl 1):123 Proceedings of the 11th conference of the european society of biomechanics
Muraoka T, Hagino H, Okano T, Enokida M, Teshima R (2007) Role of subchondral bone in osteoarthritis development: a comparative study of two strains of guinea pigs with and without spontaneously occurring osteoarthritis. Arthritis Rheum 56:3366–3374
Nakamae A, Engebretsen L, Bahr R, Krosshaug T, Ochi M (2006) Natural history of bone bruises after acute knee injury: clinical outcome and histopathological findings. Knee Surg Sports Traumatol Arthrosc 14:1252–1258
Newberry WN, Garcia JJ, Mackenzie CD, Decamp CE, Haut RC (1998) Analysis of acute mechanical insult in an animal model of post-traumatic osteoarthrosis. J Biomech Eng 120:704–709
Newberry WN, Mackenzie CD, Haut RC (1998) Blunt impact causes changes in bone and cartilage in a regularly exercised animal model. J Orthop Res 16:348–354
Noble J, Alexander K (1985) Studies of tibial subchondral bone density and its significance. J Bone Joint Surg Am 67:295–302
Odgaard A, Pedersen CM, Bentzen SM, Jorgensen J, Hvid I (1989) Density changes at the proximal tibia after medial meniscectomy. J Orthop Res 7:744–753
Paget J (1870) On the production of the loose bodies in joints. St. Bartholomew’s Hosp Rep 6:1
Pan J, Zhou X, Li W, Novotny JE, Doty SB, Wang L (2009) In situ measurement of transport between subchondral bone and articular cartilage. J Orthop Res 27:1347–1352
Pape D, Seil R, Kohn D, Schneider G (2004) Imaging of early stages of osteonecrosis of the knee. Orthop Clin North Am 35:293–303
Pedersen DR, Crowninshield RD, Brand RA, Johnston RC (1982) An axisymmetric model of acetabular components in total hip arthroplasty. J Biomech 15:305–315
Pridie KH (1959) A method of resurfacing knee joints. Proceedings of the British orthopaedic association. J Bone Joint Surg Br 41:618
Pritzker KP, Gay S, Jimenez SA, Ostergaard K, Pelletier JP, Revell PA, Salter D, van den Berg WB (2006) Osteoarthritis cartilage histopathology: grading and staging. Osteoarthr Cartil 14:13–29
Pugh JW, Rose RM, Radin EL (1973) Elastic and viscoelastic properties of trabecular bone: dependence on structure. J Biomech 6:475–485
Pugh JW, Radin EL, Rose RM (1974) Quantitative studies of human subchondral cancellous bone. Its relationship to the state of its overlying cartilage. J Bone Joint Surg Am 56:313–321
Radin EL, Paul IL (1970) Does cartilage compliance reduce skeletal impact loads? The relative force-attenuating properties of articular cartilage, synovial fluid, periarticular soft tissues and bone. Arthritis Rheum 13:139–144
Radin EL, Rose RM (1986) Role of subchondral bone in the initiation and progression of cartilage damage. Clin Orthop Relat Res 213:34–40
Roemer FW, Bohndorf K (2002) Long-term osseous sequelae after acute trauma of the knee joint evaluated by MRI. Skeletal Radiol 31:615–623
Rudberg U, Ahlback SO, Uden R, Rydberg J (1993) Radiocolloid uptake in spontaneous osteonecrosis of the knee. A case report. Clin Orthop Relat Res 287:25–29
Schlichting K, Schell H, Kleemann RU, Schill A, Weiler A, Duda GN, Epari DR (2008) Influence of scaffold stiffness on subchondral bone and subsequent cartilage regeneration in an ovine model of osteochondral defect healing. Am J Sports Med 36:2379–2391
Schunke M, Tillmann B, Schleicher A, Pointner H (1987) Biomechanische und histochemische Untersuchungen am Tibiaplateau des Menschen. Verh Anat Ges 81:451–453
Shapiro F, Koide S, Glimcher MJ (1993) Cell origin and differentiation in the repair of full-thickness defects of articular cartilage. J Bone Joint Surg Am 75:532–553
Shepherd DE, Seedhom BB (1999) Thickness of human articular cartilage in joints of the lower limb. Ann Rheum Dis 58:27–34
Simkin PA, Graney DO, Fiechtner JJ (1980) Roman arches, human joints, and disease: differences between convex and concave sides of joints. Arthritis Rheum 23:1308–1311
Simkin PA, Heston TF, Downey DJ, Benedict RS, Choi HS (1991) Subchondral architecture in bones of the canine shoulder. J Anat 175:213–227
Singh I (1978) The architecture of cancellous bone. J Anat 127:305–310
Soucacos PN, Xenakis TH, Beris AE, Soucacos PK, Georgoulis A (1997) Idiopathic osteonecrosis of the medial femoral condyle. Classification and treatment. Clin Orthop Relat Res 341:82–89
Steadman JR, Rodkey WG, Rodrigo JJ (2001) Microfracture: surgical technique and rehabilitation to treat chondral defects. Clin Orthop 391:S362–S369
Sugimoto K, Takakura Y, Tohno Y, Kumai T, Kawate K, Kadono K (2005) Cartilage thickness of the talar dome. Arthroscopy 21:401–404
Takeda M, Higuchi H, Kimura M, Kobayashi Y, Terauchi M, Takagishi K (2008) Spontaneous osteonecrosis of the knee: histopathological differences between early and progressive cases. J Bone Joint Surg Br 90:324–329
Thordarson DB, Motamed S, Hedman T, Ebramzadeh E, Bakshian S (1997) The effect of fibular malreduction on contact pressures in an ankle fracture malunion model. J Bone Joint Surg Am 79:1809–1815
Uchio Y, Ochi M, Adachi N, Nishikori T, Kawasaki K (2001) Intraosseous hypertension and venous congestion in osteonecrosis of the knee. Clin Orthop Relat Res 384:217–223
Van der Vis HM, Aspenberg P, Marti RK, Tigchelaar W, Van Noorden CJ (1998) Fluid pressure causes bone resorption in a rabbit model of prosthetic loosening. Clin Orthop Relat Res 350:201–208
van Dijk CN, Reilingh ML, Zengerink M, van Bergen CJG (2010) The natural history of osteochondral lesions in the ankle. JAAOS Instr Course Lect 59 (in press)
Vellet AD, Marks PH, Fowler PJ, Munro TG (1991) Occult posttraumatic osteochondral lesions of the knee: prevalence, classification, and short-term sequelae evaluated with MR imaging. Radiology 178:271–276
Woods K, Harris I (1995) Osteochondritis dissecans of the talus in identical twins. J Bone Joint Surg Br 77:331
Yamamoto T, Bullough PG (2000) Spontaneous osteonecrosis of the knee: the result of subchondral insufficiency fracture. J Bone Joint Surg Am 82:858–866
Acknowledgments
We thank Magali Cucchiarini, Ph.D. for helpful suggestions and Elke Dooley for help with the manuscript preparation. Supported in part by the Deutsche Forschungsgemeinschaft (DFG) and the Fonds National de la Recherche (FNR).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Madry, H., van Dijk, C.N. & Mueller-Gerbl, M. The basic science of the subchondral bone. Knee Surg Sports Traumatol Arthrosc 18, 419–433 (2010). https://doi.org/10.1007/s00167-010-1054-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00167-010-1054-z