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Scientific Article   |    
In Vitro and in Vivo Models of Cartilage Injury
Darryl D. D'Lima, MD; Sanshiro Hashimoto, MD; Peter C. Chen, PhD; Martin K. Lotz, MD; Clifford W. ColwellJr., MD
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Darryl D. D’Lima, MD
Peter C. Chen, PhD
Clifford W. Colwell Jr., MD
Division of Orthopaedic Surgery, Scripps Clinic, MS126, 11025 North Torrey Pines Road, Suite 140, La Jolla, CA 92037. E-mail address for D.D. D’Lima: ddlima@scripps.edu. E-mail address for C.W. Colwell Jr.: colwell@scripps.edu

Sanshiro Hashimoto, MD
Martin K. Lotz, MD
Division of Arthritis Research, The Scripps Research Institute, MEM 161, 10550 North Torrey Pines Road, La Jolla, CA 92037

In support of their research or preparation of this manuscript, one or more of the authors received grants or outside funding from Orthopaedic Research and Education Foundation Grant 98-052, National Institutes of Health Grant AG07996, the ALSAM Foundation, and the Skaggs Institute for Research. None of the authors received payments or other benefits or a commitment or agreement to provide such benefits from a commercial entity. No commercial entity paid or directed, or agreed to pay or direct, any benefits to any research fund, foundation, educational institution, or other charitable or nonprofit organization with which the authors are affiliated or associated.

The Journal of Bone & Joint Surgery.  2001; 83:S22-24 
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Our previous study1 demonstrated that chondrocytes undergo apoptotis in response to mechanical injury to full-thickness cartilage explants. To validate this response, several models of injury across species and in vivo were examined.
 
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+1:Full-thickness bovine and human explants had higher percentages of apoptotic cells at ninety-six hours after injury.
 
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+Fig. 2:A whole human patella after impact injury, showing superficial cartilage damage.
 
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+Fig. 3:Increased levels of apoptotic cells were seen after injury of whole rabbit and human patellae.
 
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+Fig. 4-A:Figs. 4-A and 4-B Bovine explants with a drill-hole in the center were harvested and then cultured for ninety-six hours.
 
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+Fig. 4-B:Figs. 4-A and 4-B Bovine explants with a drill-hole in the center were harvested and then cultured for ninety-six hours.
 
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+Fig. 5:Explants with a drill-hole defect had higher levels of apoptotic cells, which were largely concentrated at the margins of the drill-hole.
 
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+Fig. 6:Areas of impacted cartilage were harvested and were compared with adjacent normal cartilage and cartilage from the contralateral knee.
 
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+Fig. 7:In vivo impacted cartilage had levels of apoptosis similar to that seen in the in vitro injury experiments of whole rabbit patellae.
Full-thickness cartilage explants were harvested from weight-bearing portions of adult bovine femoral condyles, and 5-mm-diameter disks were punched out with a dermal punch. Explants were allowed to stabilize in Dulbecco modified Eagle medium supplemented with 10% fetal bovine serum for forty-eight hours. Explants were then divided into two groups: load and control. The load group underwent a single 500-msec injury load of 30% strain in radially unconfined compression. The control group was not loaded. A 30% strain was found to generate a more consistent injury than the previous loading protocol1. At ninety-six hours after injury, explants underwent histologic examination and the number of apoptotic cells was counted with use of TUNEL (terminal deoxynucleotidyl transferase-mediated dUTP nick-end labeling). Apoptosis was confirmed in selected samples by electron microscopy and immunostaining of a neo-epitope of cytokeratin. The experiment was repeated with use of normal human articular cartilage harvested from the femoral condyles of postmortem donors.
Osteochondral model: To determine whether the presence of subchondral bone affected the cartilage response, whole rabbit patellae and whole human patellae from donor cadavers were harvested. Relatively flat areas were subjected to a load of 20 MPa. The areas of loading were documented with use of pressure-sensitive film. Explants were harvested from the injured sites and from adjacent, uninjured cartilage and were maintained in Dulbecco modified Eagle medium for ninety-six hours, at the end of which apoptosis levels were measured.
Cartilage defect model: Full-thickness 3-mm drill-holes were made at regular intervals in the weight-bearing portions of adult bovine femoral condyles. Cartilage disks of 5 mm in diameter were harvested such that the drill-hole was centrally located. Disks were cultured for ninety-six hours, at the end of which apoptosis levels were measured.
In vivo rabbit impact model: After the approval of our Institutional Animal Review Committee was obtained, eight rabbits were anesthetized and one patellofemoral joint was subjected to an impact of 3 kg from a height of 50 cm in a drop-tower apparatus. Ninety-six hours after injury, the rabbits were killed and the patellar cartilage was harvested. Apoptotic levels in the injured patellar cartilage were compared with those in the adjacent, uninjured cartilage and on the contralateral, uninjured side.
All of the loaded samples in each injury model demonstrated significantly higher apoptosis rates when compared with the matched controls.
Full-thickness cartilage explants: Bovine cartilage explants demonstrated a higher mean apoptosis rate (37%±11%) compared with control samples (12%±5%) (Fig. 1). Human cartilage explants also demonstrated a higher mean apoptosis rate (32%±9%) compared with control samples (9.1%±3%) (Fig. 1).
Osteochondral models: Both rabbit and human whole patellae (Figs. 2 and 3) demonstrated a similar apoptotic response to injury (15%±4% and 11%±3%, respectively). Thus, when the subchondral bone had been left intact, apoptosis still occurred, although at a lower rate than when full-thickness cartilage explants were used.
Cartilage defect model: All of the defect explants demonstrated apoptosis rates that were higher than those at the adjacent, control sites. The edges of the lesion contained matrix debris and fragmented cells. The overall apoptotic rates were 24%±9% for the defect explants and 9%±4% for control explants (Figs. 4-A, 4-B, and 5). The apoptotic rate was significantly higher (55%±30%) in the 0.5-mm region immediately surrounding the defect. However, some apoptosis was also seen extending throughout the 5-mm-diameter explant.
In vivo rabbit impact model: The apoptotic rate in the patellar cartilage from the impacted knees was 11%&plusmn;3%, whereas it was <1%&plusmn;2% in the contralateral patellar cartilage (Figs. 6 and 7).
The results of this study support the hypothesis that mechanical injury induces chondrocyte death in the form of apoptosis. Cartilage from a variety of sources displayed a similar response. Three different modes of injury were modeled in this study: brief static compression, blunt impact, and injury leading to loss of cartilage. Three different species were tested: rabbit, bovine, and human. In addition, the apoptotic response was seen in experiments ranging from full-thickness cartilage explants to intact joints in vivo. These models have been validated clinically by the observance of significant apoptosis in patients with cartilage lesions associated with trauma2. The models may therefore be used to investigate the cellular events leading to apoptosis, subsequent repair, and degeneration, and to explore agents that may modulate these phenomena. There are data supporting the premise that chondrocyte apoptosis can be inhibited in vitro3. This opens the possibility of an alternative therapeutic approach to chondroprotection.
D’Lima DD, Hashimoto S, Chen PC, Lotz MK,Colwell CW Jr. Cartilage injury induces chondrocyte apoptosis. J Bone Joint Surg Am,2001;83(Suppl 2): 19-21. 83(Suppl 2)19  2001 
 
ColwellC, D’Lima D, Hoenecke H, Fronek J, Chung C, Pulido-Thompson P, Morris B,Lotz M. Cartilage injury: arthroscopic, histologic and MRI findings. Trans Orthop Res Soc,2001;26: 363. 26363  2001 
 
D’Lima DD, Hashimoto S, Chen P, Colwell C,Lotz M. Chondrocyte protective agents in mechanical injury. Trans Orthop Res Soc,2000;25: 210. 25210  2000 
 

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Anchor for JumpAnchor for Jump
+1:Full-thickness bovine and human explants had higher percentages of apoptotic cells at ninety-six hours after injury.
Anchor for JumpAnchor for Jump
+Fig. 2:A whole human patella after impact injury, showing superficial cartilage damage.
Anchor for JumpAnchor for Jump
+Fig. 3:Increased levels of apoptotic cells were seen after injury of whole rabbit and human patellae.
Anchor for JumpAnchor for Jump
+Fig. 4-A:Figs. 4-A and 4-B Bovine explants with a drill-hole in the center were harvested and then cultured for ninety-six hours.
Anchor for JumpAnchor for Jump
+Fig. 4-B:Figs. 4-A and 4-B Bovine explants with a drill-hole in the center were harvested and then cultured for ninety-six hours.
Anchor for JumpAnchor for Jump
+Fig. 5:Explants with a drill-hole defect had higher levels of apoptotic cells, which were largely concentrated at the margins of the drill-hole.
Anchor for JumpAnchor for Jump
+Fig. 6:Areas of impacted cartilage were harvested and were compared with adjacent normal cartilage and cartilage from the contralateral knee.
Anchor for JumpAnchor for Jump
+Fig. 7:In vivo impacted cartilage had levels of apoptosis similar to that seen in the in vitro injury experiments of whole rabbit patellae.
D’Lima DD, Hashimoto S, Chen PC, Lotz MK,Colwell CW Jr. Cartilage injury induces chondrocyte apoptosis. J Bone Joint Surg Am,2001;83(Suppl 2): 19-21. 83(Suppl 2)19  2001 
 
ColwellC, D’Lima D, Hoenecke H, Fronek J, Chung C, Pulido-Thompson P, Morris B,Lotz M. Cartilage injury: arthroscopic, histologic and MRI findings. Trans Orthop Res Soc,2001;26: 363. 26363  2001 
 
D’Lima DD, Hashimoto S, Chen P, Colwell C,Lotz M. Chondrocyte protective agents in mechanical injury. Trans Orthop Res Soc,2000;25: 210. 25210  2000 
 
Accreditation Statement
These activities have been planned and implemented in accordance with the Essential Areas and policies of the Accreditation Council for Continuing Medical Education (ACCME) through the joint sponsorship of the American Academy of Orthopaedic Surgeons and The Journal of Bone and Joint Surgery, Inc. The American Academy of Orthopaedic Surgeons is accredited by the ACCME to provide continuing medical education for physicians.
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