The basic science of the subchondral bone

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.

[1]  T. Hedman,et al.  The Effect of Fibular Malreduction on Contact Pressures in an Ankle Fracture Malunion Model* , 1997, The Journal of bone and joint surgery. American volume.

[2]  T D Cooke,et al.  Distribution of bone strength in the proximal tibia. , 1988, The Journal of arthroplasty.

[3]  M Müller-Gerbl,et al.  Computed tomography-osteoaboorptiometry: a method of assessing the mechanical condition of the major joints in a living subject. , 1990, Clinical biomechanics.

[4]  L. L. Johnson Arthroscopic Abrasion Arthroplasty: A Review , 2001, Clinical orthopaedics and related research.

[5]  J. Steadman,et al.  Microfracture: surgical technique and rehabilitation to treat chondral defects. , 2001, Clinical orthopaedics and related research.

[6]  R. Putz,et al.  The thickness of the subchondral plate and its correlation with the thickness of the uncalcified articular cartilage in the human patella , 1995, Anatomy and Embryology.

[7]  Won C. Bae,et al.  Increased hydraulic conductance of human articular cartilage and subchondral bone plate with progression of osteoarthritis. , 2008, Arthritis and rheumatism.

[8]  J. Harvey,et al.  Precise evaluation of the reduction of severe ankle fractures. , 1974, The Journal of bone and joint surgery. American volume.

[9]  T. Malinin,et al.  Articular cartilage nutrition is mediated by subchondral bone: a long-term autograft study in baboons. , 2000, Osteoarthritis and cartilage.

[10]  R. Haut,et al.  Analysis of acute mechanical insult in an animal model of post-traumatic osteoarthrosis. , 1998, Journal of biomechanical engineering.

[11]  R M Rose,et al.  Elastic and viscoelastic properties of trabecular bone: dependence on structure. , 1973, Journal of biomechanics.

[12]  D. Kohn,et al.  Imaging of early stages of osteonecrosis of the knee. , 2004, The Orthopedic clinics of North America.

[13]  D. J. Kubinski,et al.  Examination of subchondral bone architecture in experimental osteoarthritis by microscopic computed axial tomography. , 1988, Arthritis and rheumatism.

[14]  R. Udén,et al.  Radiocolloid uptake in spontaneous osteonecrosis of the knee. A case report. , 1993, Clinical orthopaedics and related research.

[15]  Ivan Hvid,et al.  Density changes at the proximal tibia after medial meniscectomy , 1990 .

[16]  Lyne Ed,et al.  Osteochondritis dissecans of the talus: case report on , 1984 .

[17]  R. Cruess Osteonecrosis of Bone Current Concepts as to Etiology and Pathogenesis , 1986, Clinical orthopaedics and related research.

[18]  P. Bullough,et al.  Topographical variations in the morphology and biochemistry of adult canine tibial plateau articular cartilage , 1985, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[19]  R. Haut,et al.  Blunt impact causes changes in bone and cartilage in a regularly exercised animal model , 1998, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[20]  A. Bhosale,et al.  Articular cartilage: structure, injuries and review of management. , 2008, British medical bulletin.

[21]  M. Glimcher,et al.  Biochemical studies on repair cartilage resurfacing experimental defects in the rabbit knee. , 1980, The Journal of bone and joint surgery. American volume.

[22]  R M Rose,et al.  Quantitative studies of human subchondral cancellous bone. Its relationship to the state of its overlying cartilage. , 1974, The Journal of bone and joint surgery. American volume.

[23]  J. Mcclure,et al.  The tidemark of the chondro-osseous junction of the normal human knee joint , 2005, Journal of Molecular Histology.

[24]  S. Jimenez,et al.  Osteoarthritis cartilage histopathology: grading and staging. , 2006, Osteoarthritis and cartilage.

[25]  S. Goodman,et al.  Autologous chondrocyte transplantation of the knee. , 2003, TEC bulletin.

[26]  K Remberger,et al.  Enhanced repair of articular cartilage defects in vivo by transplanted chondrocytes overexpressing insulin-like growth factor I (IGF-I) , 2005, Gene Therapy.

[27]  R. Putz,et al.  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? , 1997, The Anatomical record.

[28]  M. Zengerink,et al.  The natural history of osteochondral lesions in the ankle. , 2010, Instructional course lectures.

[29]  H. V. Bonde,et al.  The area of the tidemark in osteoarthritis – a three‐dimensional stereological study in 21 patients , 2005, APMIS : acta pathologica, microbiologica, et immunologica Scandinavica.

[30]  D. E. Holmdahl,et al.  DER BAU DES GELENKKNORPELS UNTER VERSCHIEDENEN FUNKTIONELLEN VERHÄLTNISSEN , 1948 .

[31]  H. Imhof,et al.  Importance of subchondral bone to articular cartilage in health and disease. , 1999, Topics in magnetic resonance imaging : TMRI.

[32]  A. Georgoulis,et al.  Idiopathic Osteonecrosis of the Medial Femoral Condyle; Classification and Treatment , 1997, Clinical orthopaedics and related research.

[33]  J. Clark,et al.  The structure of the human subchondral plate. , 1990, The Journal of bone and joint surgery. British volume.

[34]  U. Jørgensen,et al.  Bone bruise in the acutely injured knee , 2002, Knee Surgery, Sports Traumatology, Arthroscopy.

[35]  I. Harris,et al.  Osteochondritis dissecans of the talus in identical twins. , 1995, The Journal of bone and joint surgery. British volume.

[36]  M. Müller-Gerbl,et al.  [Stress on the radiocarpal joint. CT studies of subchondral bone density in vivo]. , 1997, Handchirurgie, Mikrochirurgie, plastische Chirurgie : Organ der Deutschsprachigen Arbeitsgemeinschaft fur Handchirurgie : Organ der Deutschsprachigen Arbeitsgemeinschaft fur Mikrochirurgie der Peripheren Nerven und Gefasse : Organ der V....

[37]  J. Riddle,et al.  The tibial subchondral plate. A scanning electron microscopic study. , 1987, The Journal of bone and joint surgery. American volume.

[38]  Felix Eckstein,et al.  Direct comparison of contact areas, contact stress and subchondral mineralization in human hip joint specimens , 1997, Anatomy and Embryology.

[39]  J. Fiechtner,et al.  Roman arches, human joints, and disease , 1980 .

[40]  J. Healy,et al.  Magnetic resonance imaging of bone bruising in the acutely injured knee--short-term outcome. , 2004, Clinical radiology.

[41]  R. Rose,et al.  Role of Subchondral Bone in the Initiation and Progression of Cartilage Damage , 1986, Clinical orthopaedics and related research.

[42]  I L Paul,et al.  Does cartilage compliance reduce skeletal impact loads? The relative force-attenuating properties of articular cartilage, synovial fluid, periarticular soft tissues and bone. , 1970, Arthritis and rheumatism.

[43]  A. Greenwald,et al.  Subchondral Pathways to the Superior Surface of the Human Talus , 1986, Foot & ankle.

[44]  R Putz,et al.  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 , 1992, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[45]  S. Doty,et al.  In situ measurement of transport between subchondral bone and articular cartilage , 2009, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[46]  T. Sculco,et al.  Subchondral fracture following arthroscopic knee surgery. A series of eight cases. , 2008, The Journal of bone and joint surgery. American volume.

[47]  Abraham G. Novick,et al.  Classification and Treatment , 1958 .

[48]  T. Heston,et al.  Subchondral architecture in bones of the canine shoulder. , 1991, Journal of anatomy.

[49]  M. Steinlechner,et al.  Subchondral bone density in the human elbow assessed by computed tomography osteoabsorptiometry: A reflection of the loading history of the joint surfaces , 1995, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[50]  Erik Schulte,et al.  Computed tomography-osteoabsorptiometry for assessing the density distribution of subchondral bone as a measure of long-term mechanical adaptation in individual joints , 2004, Skeletal Radiology.

[51]  村岡 智也 Role of subchondral bone in osteoarthritis development: a comparative study of two strains of guinea pigs with and without spontaneously occurring osteoarthritis , 2008 .

[52]  P. Bullough,et al.  Spontaneous Osteonecrosis of the Knee: The Result of Subchondral Insufficiency Fracture* , 2000, The Journal of bone and joint surgery. American volume.

[53]  C. Clark Surgery of the Musculoskeletal System. Ed. 2. , 1990 .

[54]  Y. Takakura,et al.  Cartilage thickness of the talar dome. , 2005, Arthroscopy : the journal of arthroscopic & related surgery : official publication of the Arthroscopy Association of North America and the International Arthroscopy Association.

[55]  C. Ohlsson,et al.  Treatment of deep cartilage defects in the knee with autologous chondrocyte transplantation. , 1994, The New England journal of medicine.

[56]  M J Glimcher,et al.  Cell origin and differentiation in the repair of full-thickness defects of articular cartilage. , 1993, The Journal of bone and joint surgery. American volume.

[57]  A. Weiler,et al.  Influence of Scaffold Stiffness on Subchondral Bone and Subsequent Cartilage Regeneration in an Ovine Model of Osteochondral Defect Healing , 2008, The American journal of sports medicine.

[58]  D. Zurakowski,et al.  Improved tissue repair in articular cartilage defects in vivo by rAAV-mediated overexpression of human fibroblast growth factor 2. , 2005, Molecular therapy : the journal of the American Society of Gene Therapy.

[59]  T. Koshino,et al.  Arthroscopy in spontaneous osteonecrosis of the knee. , 1979, The Orthopedic clinics of North America.

[60]  L. Johnson Clinical methods of cartilage repair : Arthroscopic abrasion arthroplasty-A review , 2001 .

[61]  G. Meachim,et al.  Topographical variation in the calcified zone of upper femoral articular cartilage. , 1984, Journal of anatomy.

[62]  D. Zurakowski,et al.  Local stimulation of articular cartilage repair by transplantation of encapsulated chondrocytes overexpressing human fibroblast growth factor 2 (FGF‐2) in vivo , 2006, The journal of gene medicine.

[63]  A M Jackson,et al.  Anterior knee pain. , 2001, The Journal of bone and joint surgery. British volume.

[64]  T. Krosshaug,et al.  Natural history of bone bruises after acute knee injury: clinical outcome and histopathological findings , 2006, Knee Surgery, Sports Traumatology, Arthroscopy.

[65]  I. Hvid Mechanical strength of trabecular bone at the knee. , 1988, Danish medical bulletin.

[66]  W. T. Green,et al.  Microradiographic study of the calcified layer of articular cartilage. , 1970, Archives of pathology.

[67]  E. Radin,et al.  Microfractures and microcracks in subchondral bone: are they relevant to osteoarthrosis? , 2003, Rheumatic diseases clinics of North America.

[68]  Stephen Quinn,et al.  Correlates of Subchondral BMD: A Cross‐Sectional Study , 2009, Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research.

[69]  P. Bullough,et al.  The vascularity and remodelling of subchondrial bone and calcified cartilage in adult human femoral and humeral heads. An age- and stress-related phenomenon. , 1977, Journal of Bone and Joint Surgery-british Volume.

[70]  P. Aspenberg,et al.  Migration, particles, and fluid pressure. A discussion of causes of prosthetic loosening , 1998 .

[71]  J. Buckwalter Articular cartilage injuries. , 2002, Clinical orthopaedics and related research.

[72]  S. Goldstein,et al.  The elastic moduli of human subchondral, trabecular, and cortical bone tissue and the size-dependency of cortical bone modulus. , 1990, Journal of biomechanics.

[73]  R. Price,et al.  Topographical variation within the articular cartilage and subchondral bone of the normal ovine knee joint: a histological approach. , 1995, Osteoarthritis and cartilage.

[74]  E. Hunziker,et al.  Repair of Partial-Thickness Defects in Articular Cartilage: Cell Recruitment from the Synovial Membrane* , 1996, The Journal of bone and joint surgery. American volume.

[75]  P. Dewire,et al.  Subchondral plate thickness reflects tensile stress in the primate acetabulum , 1996, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[76]  F Eckstein,et al.  Distribution of subchondral bone density and cartilage thickness in the human patella. , 1992, Journal of anatomy.

[77]  K. Alexander,et al.  Studies of tibial subchondral bone density and its significance. , 1985, The Journal of bone and joint surgery. American volume.

[78]  N. Adachi,et al.  Intraosseous Hypertension and Venous Congestion in Osteonecrosis of the Knee , 2001, Clinical orthopaedics and related research.

[79]  D. W. Jackson,et al.  Spontaneous Repair of Full-Thickness Defects of Articular Cartilage in a Goat Model: A Preliminary Study , 2001, The Journal of bone and joint surgery. American volume.

[80]  R. Putz,et al.  [Change in subchondral mineralization after reconstruction of the anterior cruciate ligament of the sheep]. , 1994, Der Unfallchirurg.

[81]  M. Müller-Gerbl Introduction (Review of Literature) , 1998 .

[82]  S. Canale,et al.  Osteochondral lesions of the talus. , 1980, The Journal of bone and joint surgery. American volume.

[83]  I. Singh The architecture of cancellous bone. , 1978, Journal of anatomy.

[84]  M. Müller-Gerbl The Subchondral Bone Plate , 1998, Advances in Anatomy Embryology and Cell Biology.

[85]  A. M. Ahmed,et al.  In-vitro measurement of static pressure distribution in synovial joints--Part I: Tibial surface of the knee. , 1983, Journal of biomechanical engineering.

[86]  J. Mcclure,et al.  The normal human chondro-osseous junctional region: evidence for contact of uncalcified cartilage with subchondral bone and marrow spaces , 2006, BMC musculoskeletal disorders.

[87]  Tetsuji Yamamoto,et al.  Use of hydroxyapatite to fill cavities after excision of benign bone tumours , 2000 .

[88]  B B Seedhom,et al.  Thickness of human articular cartilage in joints of the lower limb , 1999, Annals of the rheumatic diseases.

[89]  F. Roemer,et al.  Long-term osseous sequelae after acute trauma of the knee joint evaluated by MRI , 2002, Skeletal Radiology.

[90]  W C Hayes,et al.  Mechanical properties of metaphyseal bone in the proximal femur. , 1991, Journal of biomechanics.

[91]  König,et al.  Ueber freie Körper in den Gelenken , 1888, Deutsche Zeitschrift für Chirurgie.

[92]  H. Inoue Alterations in the collagen framework of osteoarthritic cartilage and subchondral bone , 2004, International Orthopaedics.

[93]  A. Vellet,et al.  Occult posttraumatic osteochondral lesions of the knee: prevalence, classification, and short-term sequelae evaluated with MR imaging. , 1991, Radiology.

[94]  D R Pedersen,et al.  An axisymmetric model of acetabular components in total hip arthroplasty. , 1982, Journal of biomechanics.

[95]  C. P. Winlove,et al.  Solute transport in the deep and calcified zones of articular cartilage. , 2008, Osteoarthritis and cartilage.

[96]  M. Ecker,et al.  Osteonecrosis of the knee. , 1985, The Orthopedic clinics of North America.

[97]  Michael Harty,et al.  Transchondral fractures (osteochondritis dissecans) of the talus. , 1959, The Journal of bone and joint surgery. American volume.

[98]  A. Hulth Does osteoarthrosis depend on growth of the mineralized layer of cartilage? , 1993, Clinical orthopaedics and related research.

[99]  H. Pasternak,et al.  Pelvic lymphocele complicating total hip replacement after renal transplantation. , 1977, The Journal of bone and joint surgery. American volume.

[100]  R. Marti,et al.  Fluid Pressure Causes Bone Resorption in a Rabbit Model of Prosthetic Loosening , 1998, Clinical orthopaedics and related research.

[101]  T D Brown,et al.  The apparent elastic modulus of the juxtaricular subchondral bone of the femoral head , 1984, Journal of orthopaedic research : official publication of the Orthopaedic Research Society.

[102]  R. Putz,et al.  Quantitative morphology of the subchondral plate of the tibial plateau. , 1994, Journal of anatomy.