Abstract
The subchondral bone is a key component of the osteochondral unit as it provides mechanical and biological support for the overlying articular cartilage. It has the capability to undergo structural adaptation in response to changes in the biomechanical environment of the joint. Several pathologic conditions affecting the cartilage surface originate in the subchondral layer, such as osteonecrosis and stress fractures due to mechanical overload. The purpose of this chapter was to review the different pathologic entities derived from the subchondral bone and discuss the characteristics, treatment indications, outcomes, and complications of different approaches for the treatment of each subchondral bone pathology.
Keywords
Avascular necrosis, Cartilage, Knee, Meniscectomy, Osteonecrosis, SPONK, Subchondral bone
Introduction
Although cartilage research has grown exponentially, basic science and clinical studies focusing on its foundation, namely the subchondral bone, have not received the same attention. The subchondral bone provides mechanical and biological support for the overlying articular cartilage, and it undergoes constant adaptation in response to changes in the biomechanical environment of the joint. It is noticeably involved in several chondral entities such as osteochondritis dissecans, osteoarthritis, and focal chondral defects.
Consequently, subchondral bone lesions are commonly associated with cartilage lesions. To better understand the pathology of the subchondral bone, a thorough understanding of the anatomy, morphology, and physiology of the subchondral bone and its function is required. The articular cartilage consists of 5 different zones, which can be distinguished based on the morphology and orientation of collagen fibrils. In the superficial zone, the collagen fibers are tangentially oriented into tightly packed parallel laminae that radiate vertically from the calcified zone. Zone two, or intermediate zone, contains randomly oriented collagen fibrils. Zone three, which is also referred to as the radial zone, is the thickest layer with the highest amount of proteoglycans and water. The tidemark serves as the junction between the calcified and uncalcified cartilage matrix (zone 4). Finally, the zone of calcification (zone 5) serves as an anchor to a complex network of collagen fibrils ( Fig. 12.1 ).
The definition of subchondral bone is still a subject of debate. The most accepted definition is that the subchondral plate is as a zone that divides the articular cartilage from the marrow cavity. It comprises two parts: (1) the calcified region of the articular cartilage and (2) a layer of lamellar bone. The subchondral bone is located deep to the calcified layer and includes an arterial plexus that has branches to the calcified layer ( Fig. 12.2 ). The blood flow in this zone is 3–10 times higher than that in cancellous bone. Likewise, the venous systems contain a plexus of vessels that are vulnerable to compressive and shear forces. The cortical endplate contains perforations that form channels to allow communication with the basal cartilage. These channels are dynamic and change in response to compressive forces that act on the cartilage and subchondral bone.
The purpose of this chapter is to review the different pathologic entities originating from the subchondral bone; define the characteristics of each; and discuss treatment indications, outcomes, and complications of different approaches for the treatment of each subchondral bone pathology.
Osteonecrosis
Spontaneous osteonecrosis of the knee (SPONK) was first described by Ahlback in 1968, in 40 patients with severe sudden onset of pain. It is defined as a disease of the subchondral bone that leads to focal ischemia, with subsequent necrosis, and possible structural collapse if not addressed properly. Although the etiology is not always clearly defined (idiopathic in most of the cases), patient features as well as underlying risk factors can help classify the type of osteonecrosis (ON) and therefore guide treatment. In this regard, ON of the knee can be divided into three categories: (1) primary or SPONK, (2) secondary ON (SON), and (3) postarthroscopic ON. Irrespective of the type of ON, the treatment goals for this disease are to stop further progression and delay the onset of end-stage arthritis of the knee. Once considerable joint surface collapse has occurred or advanced osteoarthritis has developed, arthroplasty is often the most appropriate treatment option.
Spontaneous ON of the knee
SPONK classically presents in the older population with a reported incidence of 9.4% in patients older than 55 years. It affects females three to five times more than males and typically presents in the medial femoral condyle. The medial femoral condyle is typically affected in 94% of the times. This can be caused because of a relatively diminished extraosseous and intraosseous blood supply to the medial femoral condyle, with apparent watershed areas making it more vulnerable to a vascular insult. Despite the varying blood supply, the lateral condyle, tibial condyles, as well as the patella can also be affected. Though the true incidence is not well established, it may be more prevalent than SON.
Although the precise etiology of spontaneous ON remains tenuous, various etiologies have been proposed. In ON of the hip, it is widely accepted that a vascular insult precipitates bone death. However, this has not been demonstrated in the knee as of yet. Several authors have reported that a traumatic event leads to microfractures in a debilitated subchondral bone (osteopenic) resulting in accumulated fluid in the space created by the subchondral microfractures. The fluid accumulation results in increased intraosseous pressure and bone marrow edema, decreased blood perfusion, and eventual focal osseous ischemia. Although a traumatic etiology has been implicated, only a minority of patients can specifically recall an injury. However, given the demographics of the affected patients and the high incidence of insufficiency fractures among postmenopausal women, associating an insidious precipitating event with the onset of knee pain can be challenging ( Fig. 12.3 ).
Tears involving the medial meniscus, specifically the posterior meniscal root, have been proposed as a potential etiologic factor for SPONK. Robertson et al. identified 30 consecutive patients with spontaneous ON of the medial femoral condyle. The radiographs and magnetic resonance imaging (MRI) were reviewed, and 80% of the patients were found to have a medial meniscal root tear. The authors suggested that the loss of hoop stress results in an increased load in the compartment (similar to a total meniscectomized state), inducing a subchondral insufficiency fracture. Moreover, early detection of these lesions is crucial because knee biomechanics can be restored to a near-native state if this lesion is properly diagnosed and treated in a timely fashion, and the progression to ON and ultimately to osteoarthritis can be significantly slowed. This theory is supported by a study demonstrating that there was a positive association between low bone mineral density and the incidence of SPONK in women older than 60 years.
Clinical presentation and diagnosis
Patients with SPONK typically present with a sudden onset of medial-sided knee pain, which is not precipitated by trauma. Pain is worse at night and with weight bearing. Range of motion may be somewhat limited secondary to pain or effusion, but usually not due to a mechanical reason. Focal tenderness over the medial femoral condyle is the most common finding on physical examination. Ligamentous examination is usually normal in these patients. The intense pain associated with the acute phase of SPONK may last up to 6 weeks. Patients who improve after 6 weeks typically have smaller lesions (less than 40% of the width of the femoral condyle) and commonly have a satisfactory result, although mild symptoms could persist for up to a year. Patients experiencing persistent symptoms even after 6 weeks are more likely to remain symptomatic. In these cases, imaging will often demonstrate a rapid progression with collapse and the development of degenerative changes.
Imaging is crucial for the diagnosis of SPONK and typically includes radiographs and MRI. Initial radiographic evaluation of patients with SPONK includes weight bearing anteroposterior, flexion posteroanterior (Rosenberg), lateral, and skyline or merchant view. Radiographic findings in patients with SPONK can vary depending on the stage of the disease. In early stages of the process, plain X-rays could be normal despite the presence of significant symptoms, and therefore, a high level of suspicion is necessary. In later stages a radiolucent lesion with a surrounding sclerotic halo can be seen. If not properly addressed, radiographs may reveal subtle flattening of the involved femoral condyle to significant subchondral collapse and secondary degenerative changes ( Fig. 12.4 ).
MRI is the gold standard for detection of incipient changes of the disease because of its high sensitivity. T1 imaging shows a discrete low-signal area often surrounded by an area of intermediate signal intensity (structural changes can be seen in a more detailed manner). A serpiginous low-signal line is often present at the margin of the lesion, delineating the necrotic area from the adjacent area of bone marrow edema. Areas affected by SPONK will demonstrate a high signal intensity in the region of the bone marrow edema with T2 imaging (more sensitivity than T1) ( Fig. 12.5 ).
Classification and prognosis
Staging of the disease constitutes the main factor when deciding which treatment algorithm to follow in each specific case. In addition, size of the lesions and overall status of the joint should be considered as well. These factors also aid in predicting the clinical course and prognosis of the patient. The Koshino staging system takes clinical and radiographic parameters into consideration. Symptomatic patients with normal radiographic findings are classified as stage I. Stage II demonstrates the weight-bearing area with flattening and subchondral radiolucencies surrounded by osteosclerosis. Stage III demonstrates extension of the radiolucencies around the affected area and subchondral collapse. Finally, stage IV is the degenerative phase with osteosclerosis and osteophyte formation around the condyles.
Lotke et al. developed a method of determining the size of the osteonecrotic lesion on anteroposterior (AP) radiographs using a percentage of the affected femoral condyle. A ratio of the width of the lesion compared with the overall width of the femoral condyle is calculated as a percentage. They reported that in patients with lesions involving 32% of the medial femoral condyle, only 6 of 23 knees required surgical management. If the lesion involved more than 50% of the medial femoral condyle, all required prosthetic arthroplasty ( Fig. 12.6 ).
Nonoperative management
As a working algorithm, it can be stated that most small lesions (typically <3.5 cm squared) can be approached with nonoperative management, whereas most large lesions (>5 cm squared) should be treated operatively to prevent progress to collapse. Medium-sized lesion (3.5–5.0 cm squared) can have an unpredictable course and should be evaluated on a case-by-case basis.
For small lesions, protected weight bearing for 4–6 weeks constitutes the most important measure to avoid collapse, and analgesics are provided as needed. Lotke et al. reported that 88.9% of patients with stage I disease can expect complete resolution of their symptoms after a course of conservative treatment. Bisphosphonates have demonstrated a potential role in the reduction of pain and prevention of subchondral collapse associated with ON of the hip by inhibition of osteoclastic resorption of necrotic bone. Bisphosphonates bind to bone, which subsequently is resorbed by osteoclasts. Once internalized by the osteoclast, the bisphosphonate then interferes with the cellular metabolism, leading to apoptosis and ultimately inhibition of bone resorption. Jureus et al. evaluated bisphosphonate use for a minimum of 6 months in 17 patients with SPONK. Although three patients progressed to subchondral collapse, they noted that 2 of the 3 patients who failed treatment ended their medication regimen prematurely. Conversely, Meier et al. found no difference in pain scores and radiographic outcome measurements in those treated with bisphosphonates versus placebo in early stage SPONK. Another nonoperative approach described in the literature is pulsed electromagnetic field therapy (PEMF). PEMF therapy has been reported to produce anti-inflammatory and bone-healing effects by decreasing the production of free radicals and stimulating osteoblasts. A recent study reported on 28 patients who had a significant reduction in pain, size of the necrotic lesion, as well as the mean femoral bone marrow lesion’s area at 6 months of follow-up.
Surgical management
Patients who demonstrate radiographic evidence of a large initial, or rapidly progressing, lesion or those who have failed a trial of conservative management for at least 3 months may benefit from joint-preserving procedures or prosthetic replacement. Joint-preserving techniques such as core decompression, osteochondral allograft transplantation, and osteotomies can potentially avoid or postpone the need for joint replacement. Arthroscopic debridement has a limited role in the management of SPONK because of the inability to alter the natural history of the disease. However, those with identifiable mechanical symptoms due to unstable chondral fragments or loose bodies may experience symptomatic relief. A recent systematic review reported that core decompression prevented additional surgical treatment in precollapse knees with a failure rate of 10.4% and that osteochondral grafts decreased the need for additional surgery in both precollapse and postcollapse knees ( Fig. 12.7 ).
Core decompression of osteonecrotic lesions of the knee was first introduced by Jacobs el al. in 1989. The reported mechanism of action is to relieve elevated intraosseous pressure and stimulate vascularity within the lesion through extra-articular drilling. Several authors have reported successful treatment using this technique in the knee. Core decompression has been shown to slow the rate of symptomatic progression of avascular necrosis and may extend the symptom-free interval in certain patients with the hope of delaying more extensive procedures. In a series of 16 patients (15 type I and 1 type II lesions), it was shown that normalization of bone marrow signal at 3-year follow-up could be obtained, along with symptomatic relief after core decompression. Deie et al. treated 12 subjects with Koshino stage II or III disease with core decompression and calcium hydroxyapatite artificial bone grafting. All patients in this series reported improved knee pain and avoided total knee arthroplasty (TKA) at a mean follow-up of 25 months.
Osteochondral autografting has demonstrated favorable results in patients who have progressed to subchondral collapse by restoration of the cartilage surface. Duany et al. reported excellent outcomes in 9 patients who underwent osteochondral autografts for the treatment of SPONK. Similarly, Tanaka et al. reported on 6 patients, who had SPONK, undergoing osteochondral autograft, in which all patients reported favorable pain relief after a mean follow-up of 28 months.
High tibial osteotomy (HTO) is a reliable procedure to offload the affected compartment, thereby decreasing the effective intraosseous pressure within the lesion in an attempt to slow or prevent progression. Concomitant procedures to promote healing such as core decompression and supplementation with bone substitutes or biologics can also be performed. Koshino et al. demonstrated improved outcomes when an HTO was performed with concomitant drilling and bone grafting with an anatomical axis correction to at least 10 degrees of anatomic valgus alignment.
Finally, patients who are not candidates for joint-preserving procedures or fail the treatments previously discussed can be treated with unicompartmental arthroplasty (UKA) or standard TKA. Given the high frequency of unicompartmental involvement in SPONK, UKA may be an attractive option because of preservation of bone stock and functioning cruciate ligaments compared with TKA. Advocates of this treatment report a shorter rehabilitation period and less postoperative pain in patients undergoing UKA versus TKA, with less challenging future revisions options. A meta-analysis of results from five reports for UKA for SPONK reported 92% good outcomes and 6% poor outcomes, with 3% of revisions in 64 knees over a mean follow-up period of 5 years. However, Ritter et al. reported that patients treated for SPONK had less pain relief (82% vs. 90%) and a higher incidence of revision surgery (17% vs. 0%) than patients who underwent UKA for osteoarthritis. In patients with extensive disease affecting multiple compartments, TKA may be the only alternative. Bergman and Rand evaluated patients who underwent standard TKA for SPONK and found good to excellent results in 87% of patients at 4 years. They also reported 85% implant survivorship at 5 years with revision surgery defined as the end point. However, when moderate or severe pain was used as the end point, survivorship was only 68%. They believed that the persistent pain experienced may have been due to foci of necrotic bone which support the implant.
Secondary osteonecrosis
SON typically presents in patients younger than 55 years of age. Unlike SPONK, SON presents with multiple foci of bone marrow involvement with extension into the metaphysis and diaphysis. Both condyles are usually involved, and patients typically have involvement of the contralateral joint in more than 80% of cases. Involvement of other joints such as the hip or proximal humerus can be seen. Therefore the clinician should have an index of suspicion regardless of the symptoms. Mont et al. demonstrated that 67% of patients with SON of the knee had disease in one or both the hips.
In contrast to SPONK, numerous conditions and risk factors have been implicated in the development of SON of the knee. Corticosteroid use and alcohol abuse are the two most common associated risk factors in up to 90% of those diagnosed with SON. Both corticosteroid use and alcohol consumption increase intraosseous adipocyte size and proliferation, leading to displacement of bone marrow. The increase in pressure within a nonexpansile compartment leads to vascular collapse and ischemia. Several other known risk factors for SON include caisson decompression sickness, sickle cell disease, Gaucher’s disease, leukemia, myeloproliferative disorders, thrombophilia, and hypofibrinolysis. The common theme among these conditions is the underlying vaso-occlusive characteristics. Gaucher’s disease, leukemia, and myeloproliferative disorders are thought to increase intraosseous pressure through bone marrow displacement. Studies have shown that patients with inherited coagulation disorders are also at high risk of SON, and it is recommended that those diagnosed early undergo pharmacologic treatment. Liu et al. identified an autosomal dominant gene mutation in type II collagen in carrier families that developed SON.
Unlike the sudden onset of pain seen with spontaneous ON, patients with SON will usually describe a gradual onset of pain over the affected area. The pain is generally localized over the femoral condyle, but in approximately 20% of cases, the tibial condyle may also be involved. A thorough history should be taken to assess for associated risk factors. Initial evaluation begins with weight-bearing plain radiographs looking for any evidence of joint-space narrowing and subchondral collapse. MRI is the study of choice much as it is for SPONK because of its sensitivity in the detection of bone marrow edema, especially in the early stages of the disease. Many reactive processes can also cause bone marrow edema, and the MRI findings can be nonspecific. SON will typically show serpentine lesions with a well-demarcated border with multiple foci of involvement. Bone scans have been shown to be less effective than MRI and are therefore not recommended for SON. Mont et al. reported that bone scans identified disease in only 37 of 58 patients (64%), whereas MRI detected all histopathologically confirmed lesions.
Classification, operative, and nonoperative treatment
Two staging classification systems used for SON of the knee include the Koshino staging system, which was originally developed for SPONK, and the Modified Ficat and Arlet staging system. The modified Ficat system for the knee was extrapolated from the original version described for femoral head ON. Using plain radiographs, four stages are used to categorize the progression of disease based on joint-space narrowing, subchondral collapse, and trabecular pattern. Stages I and II have a normal joint space with no evidence of subchondral collapse. Stage II will display some evidence of sclerosis in the trabeculae in the subchondral region. Stage III typically demonstrates slightly narrowed joint space with subchondral collapse and a crescent sign. Stage IV has both joint-space narrowing and subchondral collapse with evidence of secondary degenerative changes.
Unfortunately, symptomatic patients with SON will frequently require surgery, as nonsurgical management is typically recommended only for those patients who are asymptomatic. To limit stress on the affected joint, nonoperative management typically involves a period of protected weight bearing and analgesics as required for pain. Unfortunately, the effectiveness of this treatment method is limited. Mont et al. reported that 19% (8 of 41) of the patients who had symptomatic lesions that were managed with observation had satisfactory outcomes at a mean follow-up of 8 years.
Many of the joint-preserving techniques previously described for SPONK overlap with SON; however, the indications, effectiveness, and outcomes differ. Core decompression has demonstrated success in treating SON in cases without subchondral collapse. Woehnl and Naziri and Lee and Goodman described techniques using small-diameter (3.2 mm) percutaneous drills, using multiple passes under fluoroscopic guidance. Given the diffuse involvement seen with SON, a percutaneous technique reduces morbidity and improves outcomes by reducing structural compromise of the bone and permitting immediate mobilization after surgery. Marulanda et al. reported a 92% success rate with percutaneous techniques combined with limited weight bearing for 4–6 weeks.
Bone impaction grafting has also been used to restore the structural integrity and chondral continuity of the articular surface in patients with SON. The necrotic area is excised, and the defect is then reconstructed by impacting autograft or fresh frozen allograft bone to recreate the sphericity of the femoral condyle. In patients with multiple osteonecrotic lesions affecting both condyles, this alternative is unpractical. Several studies have reported promising results using this technique; however, many are limited to retrospective small patient cohorts. Despite this, grafting may be a useful treatment method in a young, carefully selected patient with intact articular cartilage.
Standard TKA is the most appropriate surgical option in patients who have failed conservative measures and present with subchondral bone collapse (Ficat stage III and IV disease). Owing to the frequent involvement of multiple condyles, unicompartmental arthroplasty is not indicated in SON. Mont et al. reported a 97% survival rate at mean follow-up of 9 years in patients undergoing TKA for SON. Parratte et al. demonstrated a survivorship of 96.7% at 7 years. A meta-analysis looked at outcome results for patients undergoing TKA for SON and found 74% good outcomes with a 20% revision rate in 150 patients at a mean follow-up of 8 years. However, when those performed before 1985 were excluded, good outcomes occurred in 97% of cases. This is likely the result of advances in surgical techniques, modern implants, improved implant fixation techniques, and better perioperative medical management. Finally, Görtz et al. reported that osteochondral allografting is a reasonable salvage option for ON of the femoral condyles. TKA was avoided in 27 of the 28 knees at last follow-up.
Postarthroscopic ON
Postarthroscopic ON has been described after arthroscopic meniscectomy, shaver-assisted chondroplasty, anterior cruciate ligament reconstruction, and laser- or radiofrequency-assisted debridement. Although a rare condition, given the large number of arthroscopic procedures being performed each year, the reported incidence rate of postarthroscopic ON has found to be 4%. Postarthroscopic ON has a predilection to affect the medial femoral condyle (82% of cases) ; however, the lateral femoral condyle is the second most frequently affected site. In rare cases the medial and lateral tibial plateau as well as the patella can be affected. The epiphyseal region of the operative knee involving a single condyle is typically affected. On average, symptoms have been reported to develop at a mean time of approximately 24 weeks after surgery.
The pathophysiology of ON after these procedures is not completely understood. However, several theories exist on the various etiologies of postarthroscopic ON. Pape et al. proposed that altered biomechanics and hoop stresses after meniscectomy lead to increased contact pressures and potential insufficiency fractures causing the development of ON. Thermal energy or photoacoustic shock has been implicated in inciting ON of the knee. Several reports have postulated that laser- or radiofrequency-assisted arthroscopic surgery may result in ON through direct thermal injury or photoacoustic shock. Thermal damage is thought to lead to an inflammatory response causing bone edema, ischemia, and eventual necrosis. In photoacoustic shock, rapid vaporization of cellular contents and intracellular water produces an expanding gas. The expanding gas results in a shock wave that penetrates and damages subchondral bone, inciting an inflammatory response leading to necrosis. Patients typically present with pain early in the recovery period, which is commonly mistaken as normal postoperative healing. MRI as well as AP and lateral radiographs are recommended in patients with suspected postarthroscopic ON. On T1-weighted magnetic resonance images, these lesions have an appearance similar to that of spontaneous ON of the knee, with linear foci of low signal surrounded by diffuse marrow edema adjacent to the meniscectomized compartment. Initial treatment for postarthroscopic ON is with protected weight bearing and analgesics as required. Few reports of the use of joint-preserving procedures to manage postarthroscopic ON exist.
Joint-preserving surgery may be a reasonable approach in persons who have failed nonsurgical treatment; however, most of the data on outcomes are extrapolated from SPONK and SON. TKA and UKA are recommended for patients with end-stage osteoarthritis who fail nonoperative management and progress to collapse.
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