The Journal of Bone & Joint Surgery

The Journal of Bone & Joint Surgery, Volume 79, Issue 3

Articles | March 01, 1997

The Role of Access of Joint Fluid to Bone in Periarticular Osteolysis: A Report of Four Cases*

THOMAS P. SCHMALZRIED, M.D.†; KENNETH H. AKIZUKI, M.D.‡; ALEXANDER N. FEDENKO, M.D.†; JOSEPH MIRRA, M.D.†, LOS ANGELES, CALIFORNIA

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Investigation performed at the Joint Replacement Institute at Orthopaedic Hospital, Los Angeles

J Bone Joint Surg Am, 1997 Mar 01;79(3):447-52

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In 1976, Harris et al. reported on four patients who had extensive, localized osteolysis after a total hip replacement¹⁴. This erosive or cavitary form of bone resorption has become a major problem that threatens the survival of otherwise successful total hip and knee replacements. Osteolysis has been associated with prosthetic arthroplasties since their introduction. Various etiologies of osteolysis have included infection⁵ and a foreign-body inflammatory reaction to particulate bone cement²⁵, metal particles^32,42, or polyethylene particles³⁷.

Figures in this Article

Introduction

Introduction | Case Reports | Discussion | References

While there is substantial evidence that small particles and activated macrophages play an important role in osteolysis, the pathophysiology of this condition has been incompletely defined. The mechanism needs to account for osteolysis that occurs in the absence of a discernible periprosthetic particulate burden³², that develops around femoral endoprostheses inserted without cement²⁷, and that occurs around metal-on-metal total hip replacements^38,43. The lesions described in the present report are examples of a defined pathological entity know as osteoarthrotic cysts, or geodes^3,35. This periarticular, cavitary form of bone resorption occurs in the absence of prosthetic implants. The findings presented here, combined with a review of the related pathology and pathophysiology, demonstrate that the most fundamental factor in the development of osteolysis in association with osteoarthrosis and total joint arthroplasty appears to be the access of joint fluid to bone.

*No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. Funds were received in total or partial support of the research or clinical study presented in this article. The funding source was the Los Angeles Orthopaedic Foundation.

†Joint Replacement Institute at Orthopaedic Hospital (T. P. S.) and Department of Pathology (A. N. F. and J. M.), Orthopaedic Hospital, 2400 South Flower Street, Los Angeles, California 90007.

‡Harbor/University of California at Los Angeles Medical Center, 1000 West Carson Street, Torrance, California 90509.

†Joint Replacement Institute at Orthopaedic Hospital (T. P. S.) and Department of Pathology (A. N. F. and J. M.), Orthopaedic Hospital, 2400 South Flower Street, Los Angeles, California 90007.

‡Harbor/University of California at Los Angeles Medical Center, 1000 West Carson Street, Torrance, California 90509.

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Figs. 1-A through 3: Case 1. Fig. 1-A: Anteroposterior radiograph of the right hip, made in 1990, demonstrating multiple cysts in the femoral head. The arrows indicate two of the larger cysts.

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Fig. 1-B: Anteroposterior radiograph, made in 1994, demonstrating dramatic enlargement of the cysts (arrows).

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Fig. 2-A Photograph of the femoral head, demonstrating full-thickness loss of articular cartilage and a surface defect (arrow) that was communicating with the cysts.

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Fig. 2-B Section of a specimen with multiple periarticular cysts, which were communicating with the intra-articular surface.

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Fig. 3 Light photomicrograph of the margin of a cyst, demonstrating fibrovascular tissue with several multinuclear cells (osteoclasts) actively resorbing lamellar bone (hematoxylin and eosin; original magnification x 250).

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Figs. 4-A and 4-B: Case 2. Fig. 4-A: Anteroposterior radiograph of the right hip. There is a large supra-acetabular iliac cyst and cysts in the femoral head (straight arrows). There is also an apparent absence of a portion of the acetabular dome (curved arrow).

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Fig. 4-B: Arthrogram made after exercise. The contrast medium has filled the joint space (small arrow), has passed through a defect in the acetabular dome (curved arrow), and has pooled in the supra-acetabular cyst (large arrows).

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Fig. 5 Case 3. Anteroposterior and lateral radiographs of the right knee. A large cyst, which appears to originate from the articular surface, occupies most of the medial femoral condyle (arrows). There is complete loss of the joint space.

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Fig. 6 Case 3. Gross specimen showing the distal (left) and posterior (right) femoral cuts made at the time of a total knee arthroplasty. There is full-thickness loss of cartilage and a defect in the bone leading to the cyst (arrow).

Case Reports

Introduction | Case Reports | Discussion | References

CASE 1. In 1990, radiographs of a seventy-four-year-old man demonstrated multiple cysts in the right femoral head (Fig. 1-A). Radiographs made in 1994 demonstrated dramatic enlargement of these cysts (Fig. 1-B). Pain gradually increased, and the patient had a total hip replacement. Examination of the femoral head revealed extensive full-thickness loss of articular cartilage and focal loss of subchondral bone; a thin fibrous membrane covered the entrance into the large cysts (Fig. 2-A). Serial sections of the specimen confirmed the presence of multiple cysts, which were communicating with the intra-articular surface (Fig. 2-B). Histological examination of the cysts revealed a lining composed predominantly of fibrovascular tissue with occasional lymphocytes. The margins of the cysts were characterized by a mix of necrotic and viable bone with focal regions of scalloped erosions into necrotic bone. In other regions, multinuclear cells (osteoclasts) were actively resorbing lamellar bone (Fig. 3).

CASE 2. Post-traumatic osteoarthrosis developed in the right hip of a forty-five-year-old man. Radiographs demonstrated loss of superior articular cartilage, a large Eggers supra-acetabular iliac cyst⁸, and cysts in the femoral head (Fig. 4-A). An arthrogram demonstrated free flow of contrast medium into, and accumulation of medium within, the supra-acetabular cyst (Fig. 4-B). Increasing pain led the patient to have a total hip replacement. A thin fibrous membrane partially covered the base of the supra-acetabular cyst, which was filled with fluid and a friable yellow-tan material that was grossly similar to that seen in osteolytic lesions after total hip arthroplasty. Sections of the femoral head confirmed the presence of a large cyst that communicated with the intra-articular surface. Histological examination of the contents of the supra-acetabular and femoral cysts demonstrated a mixture of necrotic and fibrotic tissue with rare lymphocytes and histiocytes.

CASE 3. A sixty-nine-year-old woman had pain in the right knee for eight years. Radiographs demonstrated varus alignment with loss of articular cartilage in the medial compartment. A large cyst was noted in the medial femoral condyle. It appeared to originate from the articular surface (Figs. 5-A and 5-B). The distal and posterior femoral cuts for total knee replacement transected the cyst, which was filled with a friable yellow-to-green-gray tissue. Gross examination of the cut surfaces showed full-thickness loss of cartilage as well as a defect in the bone leading to the cyst (Fig. 6). Histological examination of the cyst revealed findings similar to those of the previous patients.

CASE 4. Post-traumatic osteoarthrosis developed in the right knee of a fifty-five-year-old man. Radiographs demonstrated a valgus deformity with loss of articular cartilage in the lateral compartment. A large cyst, measuring 3.0 by 1.7 millimeters on the anteroposterior radiograph, was noted in the lateral aspect of the proximal end of the tibia. The cyst appeared to extend as far as the proximal tibial articular surface. At the time of total knee replacement, a punctate lesion in the posteromedial aspect of the lateral tibial plateau was found to communicate with the cyst. The cyst contained friable yellow-green tissue. The histological findings were similar to those of the other patients.

Discussion

Introduction | Case Reports | Discussion | References

The lesions described in this report are striking examples of periarticular, cavitary bone resorption, which has been called osteolysis^3,14. The term geode has been applied to these periarticular erosions, which are a defined pathological entity noted in association with several joint abnormalities, including osteoarthrosis and rheumatoid arthritis^3,35. In osteoarthrosis, geodes occur in areas of degenerated cartilage, often in a paired, or so-called kissing, position on both sides of the joint. Frequently, a defect in the articular surface is found to communicate with the cyst. The cyst may be filled with fluid but also may contain variable amounts of fibrovascular tissue and fragments of articular cartilage. A sclerotic margin is characteristic, but osteoclastic bone resorption may be seen at the margins of the cavity^3,36.

Two fundamental theories have been proposed for the etiology of geodes: intrusion of synovial fluid (the hydrodynamic theory) and osseous contusion (the mechanical overload theory)³⁵. Freund¹⁰ appears to have been the first to suggest that elevated intra-articular fluid pressure could lead to intrusion of joint fluid into cancellous bone through gaps in degenerated articular cartilage. Landells²⁸ suggested that osteoarthrotic cysts always originate from a communication with the joint space and that they are not due to primary degenerative changes in the bone. Landells proposed that the pressure of the joint fluid leads to progressive bone resorption, and he cited the increase of synovial fluid that is seen in association with osteoarthrosis and the rounded outlines of the cysts as being indicative of the role of fluid pressure. Landells also proposed that the relatively low compliance of the capsule of the hip compared with that of the knee could predispose the hip to larger (and more frequent) cysts. Mechanical overload sufficient to cause osteonecrosis may be critical for the initiation of geodes. Regardless of the primary event, our observations as well as those of other investigators support the roles of fluid pressure and intrusion of joint fluid in the enlargement of geodes.

Intracapsular fluid pressure is a function of many variables, including capsular compliance, fluid compartmentalization, joint position, and muscle action²⁹. The compliance of the joint capsule is reduced in association with osteoarthrosis. Conversely, joint-fluid pressures are increased in association with osteoarthrosis and vary with use of the joint. During gait, cyclical variations in intra-articular pressures of the normal knee are subatmospheric. In contrast, the osteoarthrotic knee has consistently positive pressures that increase with contraction of the muscles^{9,18,20-22,29,30,34}. Intracapsular increases in fluid pressure may be transmitted to geodes, and transmitted pressures of as much as 250 millimeters of mercury (33.33 kilopascals) have been recorded²². Failure of the pressure to return to the baseline level suggests a one-way valve that maintains the elevated pressure, which in turn could contribute to enlargement of the cyst²².

In normal synovial joints, such as the hip or the knee, bone is not exposed to joint fluid. The joint boundaries are defined by the capsule, and within the capsule bone is covered by cartilage or synovial tissue^31,39. In disease processes, such as osteoarthrosis, the normal anatomical and physiological compartmentalization of a synovial joint can be disrupted. Degradation of articular cartilage can allow direct communication of joint fluid with bone, resulting in an extension of the joint space. Inflammation of the joint is accompanied by an effusion¹². The effusion, either with or without decreased capsular compliance³⁰, results in increased intracapsular fluid pressures^18,20,34. There is evidence that the combination of the access of joint fluid to bone and the transmission of elevated joint-fluid pressures contributes to the enlargement of geodes^3,8,10,22. Increased fluid pressures may disrupt the local circulation. Necrosis in geodes has been reported previously^3,19,35 and was a consistent feature of the specimens in the present report.

A similar process appears to occur in association with prosthetic arthroplasty. The normal anatomical and physiological compartmentalization of the joint is disrupted during the implantation procedure. Operative exposure is accompanied by variable disruption of the capsule and the synovial tissue. Resection of the native articular surfaces and preparation of the bone for attachment of the prosthesis results in a variable degree of communication between the initial joint space and bone. In joint arthroplasty, the so-called effective joint space can be quite extensive³⁷. Further, periprosthetic inflammation is accompanied by an effusion as well as fibrosis of the pseudocapsule³⁷. The pathophysiology of geodes indicates that the transmission of elevated joint-fluid pressure to bone can have a physical effect that results in the erosion of bone²². Through a similar mechanism, the expansile nature of osteolytic lesions adjacent to prosthetic joints may, at least in part, be due to a physical effect resulting from the transmission of elevated joint-fluid pressures^1,16,37. A difference in the pathological findings in the region around geodes and those in the area of localized bone resorption around prosthetic joints is activated macrophages; geodes develop without this foreign-body response to prosthetic particles.

On the basis of the pathophysiology of geodes and the findings of investigations of osteolysis in total joint arthroplasty, we propose that joint-fluid pressure has a role in the pathophysiology of osteolysis. Wear particles are released into joint fluid and are distributed variably throughout the effective joint space³⁷. These particles cause inflammation and contribute to the development of an effusion. Chronic inflammation causes fibrosis and decreased capsular compliance, which can result in the elevation of intracapsular joint-fluid pressures. In patients who have prosthetic joints, intracapsular fluid pressures may exceed 750 millimeters of mercury (99.98 kilopascals)¹⁶ and can be transmitted to regions distant from the articulation. A fluid pressure of 198 millimeters of mercury (26.39 kilopascals) has been measured in an osteolytic cavity in the femoral diaphysis¹. The flow of joint fluid is an active process driven by fluctuations in joint-fluid pressures that occur with activities of daily living¹⁶ and that can contribute to progressive expansion of the effective joint space³⁷. In contrast to an osteoarthrotic joint, a well fixed and otherwise well functioning prosthetic joint may not be associated with symptoms; as a result, the patient remains active and maintains the driving forces for osteolysis, which may account for the progression and extreme size of some osteolytic lesions associated with total joint arthroplasty.

The effective joint space can expand into soft tissue as well as bone^{2,6,15,17,33,40}. This expansion into soft tissue is recognized less frequently, at least in part because imaging of the soft tissues is not routinely performed. Increased joint-fluid pressures may be painful and may result in rupture of the joint capsule or the formation of synovial cysts^12,23. Synovial cysts may have a protective function; specifically, by accommodating fluid volume and limiting the increase in intra-articular pressure, such cysts may protect bone from damage due to pressure. An inverse relationship has been demonstrated between the occurrence of periarticular bone cysts (geodes) and that of synovial cysts¹¹. The natural hip joint can communicate with the iliopsoas bursa⁴. Pressure-driven synovial fluid may be pumped into the bursa; this causes distension, which may be symptomatic². Similar events can occur after total hip arthroplasty^17,33. In the effective joint space, joint fluid seeks the path of least resistance; this path is variable and includes soft tissue as well as bone³⁷.

Soluble factors capable of directly or indirectly effecting bone resorption have been identified in joint fluid; these factors include prostaglandins, interleukins, and matrix metalloproteinases^7,13,26,41. Elevated levels of these factors may play a central role in rapidly destructive arthropathy of the hip²⁶. Cytokines and matrix metalloproteinases have been identified in interfacial and pseudocapsular tissues from around loose total joint replacements^7,13. While proteolytic enzyme activity in interfacial tissue contributes to local bone resorption, pseudocapsular tissues also release bone-resorbing factors into joint fluid⁴¹. Levels of cytokines and matrix metalloproteinases can be elevated in the fluid around total joint replacements⁷ and could effect bone resorption at distant sites. There are similar cytokine profiles in osteoarthrotic cysts and in osteolytic lesions around total joint implants²⁴.

In summary, these observations suggest that a fundamental factor in the development of geodes in association with osteoarthrosis and of osteolysis in association with total joint arthroplasty is access of joint fluid to bone. A limitation of current prosthetic arthroplasty is the variable disruption of the anatomy and physiology of the joint that occurs as a result of the implantation procedure. In addition to the physical effect of pressure as seen with geodes, the fluid around prosthetic joints also carries wear particles and increased levels of soluble factors that are capable of stimulating bone resorption at distant sites. While a reduction in the particulate burden is desirable, we believe that limitation of access of joint fluid to bone is necessary to prevent osteolysis.

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Introduction | Case Reports | Discussion | References

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Topics

bone resorption ; articular cartilage ; cyst ; hip joint ; knee joint ; osteoarthritis ; osteolysis ; synovial fluid ; articular space

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THOMAS P. SCHMALZRIED, KENNETH H. AKIZUKI, ALEXANDER N. FEDENKO, JOSEPH MIRRA; The Role of Access of Joint Fluid to Bone in Periarticular Osteolysis: A Report of Four Cases*. The Journal of Bone & Joint Surgery. 1997 Mar;79(3):447-52.

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