The Journal of Bone and Joint Surgery 80:1459-67 (1998)
© 1998 The Journal of Bone and Joint Surgery, Inc.
Osteolysis in Association with a Total Hip Arthroplasty with Ceramic Bearing Surfaces*
TAEK RIM YOON, M.D. ,
SUNG MAN ROWE, M.D.,
SUNG TAEK JUNG, M.D.,
KWANG JIN SEON, M.D., KWANGJU, KOREA and
WILLIAM J. MALONEY, M.D. , ST. LOUIS, MISSOURI
Investigation performed at the Chonnam University Hospital, Kwangju
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Abstract
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The results of 103 total hip arthroplasties performed with insertion of a ceramic femoral head and acetabular component in ninety-six patients were reviewed to determine the radiographic prevalence of osteolysis. After a mean duration of follow-up of ninety-two months (range, sixty to 125 months), femoral osteolysis was observed in twenty-three hips (22 per cent), in one of two distinct patterns: linear osteolysis (twelve hips) or scalloping expansile-type osteolysis (eleven hips). The most common locations of osteolysis in the femur were in zones I and VII as described by Gruen et al. Serial radiographs demonstrated that the extent of the osteolysis progressed over time. Osteolysis of the pelvis, noted in forty-nine hips, was always associated with migration of the acetabular socket. No focal osteolysis was observed in association with the stable sockets.
Ten patients (ten hips) had a revision because of loosening and migration of the acetabular component. In three of these patients, the femoral stem also was revised. Gross examination revealed evidence of wear of the ceramic bearing surface in all ten patients. Scanning electron microscopy showed cracking and wear marks on the weight-bearing surface.
Histological evaluation of the tissue in the periprosthetic membrane demonstrated abundant ceramic wear particles. The interface membrane was composed of a vascularized fibrous connective tissue with macrophages. Ultrastructurally, the macrophages contained numerous phagosomes of various sizes, with electron-dense material within the cytoplasm of the cell. The mean size of the ceramic particles, as determined with scanning electron microscopy, was 0.71 micrometer (range, 0.13 to 7.20 micrometers). This study supports the concept that ceramic wear particles can stimulate a foreign-body response and periprosthetic osteolysis.
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Introduction
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Periprosthetic osteolysis is regarded as an important factor in the long-term durability of a total hip prosthesis1,17. Harris et al. were apparently the first to describe localized femoral osteolysis in association with loose total hip prostheses that had been inserted with cement18. Subsequently, Jasty et al.20, Maloney et al.29, and Anthony et al.2 reported focal femoral osteolysis in patients who had a stable femoral component that had been inserted with cement. Implants designed to be inserted without cement were introduced in part with the hope that they would prevent osteolysis, then referred to as cement disease. However, it has become clear that osteolysis can occur regardless of the type of fixation of the implant. Brown and Ring were the first authors, to our knowledge, to report osteolytic changes in the proximal part of the femur in association with extensively porous-coated implants that had been inserted without cement6. Metaphyseal osteolysis in these patients resulted in avulsion fractures of the trochanter. Maloney et al. subsequently described sixteen patients who had osteolysis around a radiographically stable femoral component that was made of either titanium or cobalt-chromium alloy and had been inserted without cement31. In all but one patient, the osteolysis first was noted at least two years after the index operation. More recent studies have demonstrated that the prevalence of osteolysis in hips with components that have been inserted without cement increases over time28,47.
Osteolysis has been attributed to the biological response to particles of wear debris1,14,27, and polyethylene particles have been implicated as a major etiological agent associated with modern designs of prosthetic components30,39,41,50. Histological analysis of the soft-tissue membranes of osteolytic lesions has revealed findings similar to those that were reported previously in association with aseptic loosening of components inserted with cement7,14,31,39,40. Investigators who previously examined wear particles from failed prostheses that had been inserted without cement focused mainly on polyethylene and metal implants32,33,42.
Boutin was the first author, to our knowledge, to report the use of alumina ceramics in total hip arthroplasty, in 19724. There have been many subsequent reports regarding the use of ceramic total hip systems15,26,36,44,46,48,51. It has been suggested that, in principle, ceramics have the potential for low rates of wear, and alumina-ceramic bearings have demonstrated the lowest rates of in vivo wear of any bearing combination to date. Walter reported a mean rate of wear of 1.8 micrometers per year for an alumina-ceramic femoral head component and of 2.1 micrometers per year for an alumina-ceramic acetabular component48. Boutin and Blanquaert reported a mean rate of wear of nine micrometers per year for the femoral head and six micrometers per year for the acetabular socket with use of a ceramic-on-ceramic bearing surface5. However, because of the high modulus of elasticity and the hardness of the material, the wear characteristics are sensitive to design, manufacturing, and implantation-related variables, and rapid wear also has been observed48,49.
Although ceramic implants have been in use for many years, there are scant data concerning the inflammatory nature of ceramic particles. The purpose of the current study is to describe the prevalence of periprosthetic osteolysis in a consecutive series of patients who had a ceramic-on-ceramic total hip replacement. The histological characteristics of ceramic wear particles obtained from the interface membrane of prostheses that failed also are described.
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Materials and Methods
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One hundred and forty-three patients (169 hips) had a total hip arthroplasty without cement with use of the Mittelmeier total hip system between 1983 and 1989. This system consists of a truncated alumina-ceramic acetabular component, an alumina-ceramic femoral head (Biolox; Osteo AG, Selzach, Switzerland), and a fully porous-coated cobalt-chromium-alloy femoral stem (Autophor, Osteo AG). Twelve of the original patients died, and fifteen were lost to follow-up. An additional twenty patients were excluded from the study because they had had less than five years of radiographic follow-up. An effort was made to have each patient return for follow-up; however, for many of the patients in this series, returning would have caused a major economic hardship. It is unlikely that patients who were lost to follow-up or who did not have sufficient radiographic follow-up would have had a revision operation at another institution.
Ninety-six patients (103 hips) who had been followed radiographically for at least five years were included in the study. The mean duration of follow-up was ninety-two months (range, sixty to 125 months). There were eighty-eight men (ninety-five hips) and eight women (eight hips). Seven patients had bilateral total hip replacement, with the procedures performed sequentially. The mean age of the patients at the time of the index operation was forty-nine years (range, twenty-one to sixty-six years), and the mean weight was sixty-three kilograms (range, forty-five to eighty-seven kilograms). The diagnosis was osteonecrosis in eighty-nine hips; rheumatoid arthritis in four; primary osteoarthrosis in three; secondary osteoarthrosis due to sequelae of infection in two; congenital dysplasia in two; and an old fracture, Perthes disease, and an old slipped capital femoral epiphysis in one hip each.
The immediate postoperative and all follow-up anteroposterior radiographs were reviewed. Sockets that had a complete radiolucent line at the bone-implant interface and those that had migrated were considered loose. Migration was measured with use of the technique described by Massin et al.34. Briefly, vertical migration was measured along a perpendicular line from the center of the femoral head to the interteardrop line.
The stability of the femoral component was graded according to the criteria of Engh et al.11. The component was defined as stable with bone ingrowth when no subsidence and minimum formation of a radiopaque line around the stem were noted, as stable with fibrous ingrowth when there was no progressive subsidence but extensive parallel radiopaque lines were noted around the stem, and as unstable when progressive subsidence and divergent radiopaque lines around the stem were noted. Subsidence of the femoral component was determined by comparison of measurements of the distance between the collar and the lesser trochanter on serial radiographs. The presence of osteolysis on the femoral side was recorded with use of the zones described by Gruen et al.16. Expansile, erosive, ballooning osteolytic lesions were designated as scalloping osteolysis. Scalloping osteolysis was distinguished from a linear pattern of bone resorption at the bone-implant interface, which was designated as linear osteolysis.
Tissue samples were obtained for examination from the membrane at the interface between the bone and the acetabular component from ten hips and from the membrane at the interface between the bone and the femoral component from three hips after revision of the respective components. The samples were fixed in 10 per cent phosphate-buffered formalin and were embedded in paraffin. Three-micrometer-thick serial sections were stained with hematoxylin and eosin and were examined with light microscopy. An image-analysis system (IBAS 2000; Kontron, Munich, Germany) was used to determine the sizes of 100 particles from at least five fields of each specimen. Both the long and short dimensions were recorded for all particles.
Specimens of the membrane at the interface between the bone and the acetabular component from four hips also were examined with use of transmission electron microscopy. One by one-millimeter sections were fixed in half-strength Karnovsky solution for twelve hours21. The sections then were washed with cold 0.1-molar cacodylate buffer and were post-fixed in 1 per cent osmium tetroxide at 4 degrees Celsius for one hour according to the method of Millonig35. The specimens then were dehydrated in graded alcohol and were embedded in Epon. Serial sections, approximately eighty nanometers thick, were cut with a diamond knife on an ultramicrotome (Sovall MT-5000; Dupont, Newtown, Connecticut) and were stained with uranyl acetate and lead citrate. Electron micrographs were made with a JEM 1200-EX electron microscope (JEOL, Tokyo, Japan) at eighty kilovolts.
Inductively coupled plasma atomic-emission spectrophotometry (ICPS-1000 III; Shimatzu, Kyoto, Japan) was used to determine the presence of free metal ions in three tissue samples. Approximately 2.5 grams of tissue (wet weight) was dissolved in ten milliliters of ultrapure concentrated nitric acid and was heated on a hot plate at a temperature of 93 degrees Celsius. This solution was evaporated to approximately one to two milliliters. Two milliliters of concentrated nitric acid and one milliliter of HClO4 then were added, and the solution was heated overnight on a hot plate. After it had cooled to room temperature, two milliliters of hydrochloric acid was added and the sample was again heated until the solvent had decreased to approximately two milliliters. Distilled water then was added to bring the total volume to fifty milliliters. This resulted in dissolution of the membranes and release of wear particles in all samples. Scanning electron-microscopic examination with energy-dispersive x-ray spectrophotometric analysis then was performed on isolated particles from the three samples. Both elemental composition and particle size were analyzed further with use of the scanning electron microscope with an x-ray spectrometry system (Series 2; Noran, Middleton, Wisconsin).
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Results
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Only thirty-four hips were identified as having a stable socket on the basis of the radiographic analysis. In twenty hips, the socket was graded as unstable because of a complete radiolucent line at the bone-implant interface with minimum migration (less than two millimeters) (Figs. 1-A, 1-B, 2-A, 2-B, 3-A and 3-B). An additional forty-nine hips were graded as having an unstable socket on the basis of progressive migration (two to twenty-two millimeters). The femoral component was graded as stable with bone ingrowth in ninety-four hips, stable with fibrous ingrowth in four, and unstable in five. Ten patients (ten hips) had had a revision of the socket because of loosening and osteolysis; in three of the ten, the femoral component had been unstable and also had been revised. These three components represent three of the five unstable femoral components.
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FIG1-A: Figs. 1-A through 3-B: Radiographs made after total hip arthroplasties with a ceramic-on-ceramic articulation.
Fig. 1-A: Radiograph made immediately postoperatively.
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FIG1-B: Fig. 1-B: Nine years after the index operation, there is osteolysis around the acetabular component (arrows) and a linear pattern of osteolysis around the femoral component (arrows). Both components have migrated.
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FIG2-B: Fig. 2-B: Nine years after the index operation, there is osteolysis around the acetabular component (arrows) and an expansile pattern of osteolysis in the calcar region adjacent to the femoral component (arrows). The acetabular component has migrated.
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FIG3-B: Fig. 3-B: Seven years after the index operation, there is an expansile pattern of osteolysis in the diaphysis of the femur (arrows).
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Femoral osteolysis was noted in twenty-three hips (22 per cent) (Figs. 1-A, 1-B, 2-A, 2-B, 3-A and 3-B). In twelve hips, the pattern of osteolysis was linear. In eight of the twelve, the osteolysis was restricted to zones I and VII of Gruen et al.16, and in the other four the osteolysis extended into zone II or VI. Scalloping osteolysis was noted in eleven hips. In nine of these hips, the osteolysis was noted in zone I or VII; only two hips had lesions distal to this region. Examination of the ceramic femoral heads and acetabular components that were removed at the revisions revealed visible wear and damage to the load-bearing surfaces of all components (Fig. 4-A). Scanning electron microscopy revealed cracking of the surface with wear marks. Both grooves and smearing of the articular bearing surfaces were noted (Fig. 4-B).
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FIG4-A: Figs. 4-A and 4-B: A damaged alumina-ceramic femoral head that was removed seven years after implantation.
Fig. 4-A: Photograph showing demarcation between the wear-damaged region and the region with a normal surface finish (arrows).
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FIG4-B: Fig. 4-B Scanning electron micrograph showing cracking of the surface with wear marks on the left side and a normal surface finish on the right side.
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Histological evaluation of the interface membranes demonstrated vascularized fibrous connective tissue with some areas of dystrophic calcification. Sheets of granular macrophages were seen within the fibrous stroma, and ceramic wear particles that appeared as granule-like brownish-red material were noted within the cytoplasm of the macrophages (Figs. 5-A and 5-B). Multinucleated giant cells were noted but were uncommon, as were lymphocytes and plasma cells. The mean size of the ceramic wear particles, as determined by light microscopy with use of an image-analysis system, was 1.4 micrometers in the short dimension and 3.1 micrometers in the long dimension. Metallic particles also were noted in one of the three membranes at the bone-femoral component interface.
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FIG5-A: Fig. 5-A Photomicrograph of a specimen from an acetabular membrane, demonstrating abundant ceramic debris (arrows) (hematoxylin and eosin, x 100).
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FIG5-B: Fig. 5-B Photomicrograph of a specimen from a femoral membrane, demonstrating abundant ceramic debris (arrows) (hematoxylin and eosin, x 320).
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Ultrastructurally, the macrophages had an indented nucleus and well developed intracytoplasmic microorganelles. Numerous phagosomes of various sizes containing electron-dense material were seen within the cytoplasm of the macrophages (Fig. 5-C). The soft-tissue digest revealed numerous irregularly shaped ceramic wear particles (Fig. 6). The mean size of the particles, as measured with scanning electron microscopy, was 0.71 micrometer (range, 0.13 to 7.20 micrometers).
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FIG5-C: Fig. 5-C Scanning electron micrograph demonstrating numerous irregularly shaped phagosomes of various sizes containing electron-dense material (arrows) within the cytoplasm of a macrophage.
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FIG6: Fig. 6 Scanning electron micrograph showing ceramic wear particles after tissue digestion (x 5000).
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As already noted, electron microprobe analysis was performed on three soft-tissue samples. One of these samples was from a membrane at a bone-femoral component interface, and the other two were from membranes at bone-acetabular component interfaces. Histological analysis of the membrane from the femoral component revealed both ceramic and metallic wear particles. This finding was confirmed on electron microprobe analysis, which demonstrated that each gram of the sample contained 29.9 micrograms of aluminum, 23.9 micrograms of iron, 22.0 micrograms of cobalt, 10.3 micrograms of chromium, and 0.4 microgram of molybdenum. In contrast, analysis of the two membranes from the acetabular components revealed markedly elevated levels of aluminum with only trace amounts of cobalt and chromium. Each gram of sample 1 contained 735.1 micrograms of aluminum, 68.1 micrograms of iron, and 0.2 microgram of chromium, and each gram of sample 2 contained 524.5 micrograms of aluminum, 32.4 micrograms of iron, 0.3 microgram of chromium, and 0.4 microgram of cobalt.
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Discussion
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In the current study, we found a high rate of failure (primarily of the fixation of the acetabular component) after total hip arthroplasty with a ceramic femoral head and acetabular socket. In addition, we report a high prevalence of osteolysis in the pelvis and, to a lesser extent, on the femoral side. The high rate of mechanical failure is probably multifactorial and related to the design of the socket, the diagnosis, and the patient's level of activity. Many of our patients were farmers and although their level of activity was not quantitated it was probably high. Most of the patients had avascular necrosis, which is the most common diagnosis for patients who have a total hip arthroplasty in South Korea. Historically, total hip replacement in patients who have avascular necrosis has not been as successful as it has been in patients who have other diagnoses. Stauffer reported failure in five of ten hips of patients who had osteonecrosis in a series of 231 total hip arthroplasties that had been performed with cement45. In a study of 103 hip replacements that had been performed with cement, Ranawat et al. reported 90 per cent good results overall; however, of the twelve patients who had osteonecrosis, eleven had a result that was considered a failure38. Similarly poor results were reported by Cornell et al., who found failure in eleven (39 per cent) of twenty-eight patients who had had a total hip arthroplasty with cement because of non-traumatic osteonecrosis10. Piston et al. reported on thirty patients (thirty-five hips) with osteonecrosis who had had a total hip arthroplasty with use of porous-coated components (AML; DePuy, Warsaw, Indiana) inserted without cement; at a mean of 7.5 years after the operation, only one stem and two sockets had been revised37. The Autophor stem is similar to the AML stem in that it is an extensively porous-coated cobalt-chromium-alloy component; however, the Autophor socket has several obvious differences compared with a hemispherical porous-coated socket22. A similarly high rate of failure with use of a titanium-alloy threaded truncated cone acetabular component (T-TAP; Biomet, Warsaw, Indiana) was reported recently by Fox et al.; at six years, twenty-six (38 per cent) of sixty-eight cups had failed13. Because of the high rate of failure, those authors recommended that this design not be used.
Alumina ceramic is an attractive material for the articulation in total hip arthroplasty as it can provide an ultrasmooth finish9. Its ionic structure creates a hydrophilic surface with higher wetability than metals, thus facilitating lubrication. It also has low frictional and high wear properties. There have been many reports regarding the use of ceramic total hip systems and, as noted earlier, the rates of wear in general have been very low. The source of the ceramic wear particles in the periprosthetic tissues that were analyzed in the current study was at least in part the articulation, as determined on the basis of visual and electron-microscopic evidence of wear. However, there are other potential sources of wear particles, including the back of the acetabular component and the head-neck junction. Although there was no gross visual damage to these regions of the retrieved implants, they were not examined with scanning electron microscopy.
The particles of debris that we noted histologically were identified as ceramic-based on the basis of their characteristic brownish-red color. This appearance is distinctly different from that of metallic debris, which appears black under light microscopy. The elemental composition of the ceramic particles was confirmed with use of energy-dispersive spectrophotometric analysis. The size of the ceramic particles was similar to that reported previously for both polyethylene and metallic particles32,33,42. According to light microscopy, the mean size of the ceramic particles was 3.1 micrometers, whereas according to scanning electron microscopy it was 0.71 micrometer. This apparent discrepancy has been noted previously. Lee et al. evaluated the size of polyethylene particles with use of light microscopy and reported a particle size of eight to thirteen micrometers24. Subsequent studies with use of scanning electron microscopy showed that most polyethylene wear particles were smaller than one micrometer32,33,42. Particles smaller than one micrometer can be difficult to identify with light microscopy; thus, light microscopic analysis is likely to overestimate mean particle size and to underestimate particle load. Lerouge et al. recently analyzed wear particles from the pseudomembranes of loose acetabular components, inserted either with or without cement, of prostheses that had a ceramic-on-ceramic articulation25. Of the three types of debris—metal, alumina ceramic, and zirconia—alumina was present in the least amounts, representing 12 per cent of the particle load. In contrast, alumina-ceramic particles were abundant in the soft-tissue membranes that had been obtained from loose sockets in the current study. In the study by Lerouge et al., the mean size of the alumina-ceramic particles was 0.44 micrometer, which is in the same range as the sizes reported in the current study.
The biological reaction to the ceramic wear particles in the current study was histologically similar to the cellular reaction that has been documented with regard to other types of wear debris from implants. In the presence of ceramic wear particles, the histological features of the periprosthetic tissue are characteristic of a foreign-body granuloma. A granuloma forms in response to material that is resistant to degradation or removal, or both. Christel, in his review of the biocompatibility of surgical-grade polycrystalline alumina, noted that alumina particles of less than five micrometers have been found within macrophages in animal studies8. Alumina was less reactive than titanium and polyethylene. Alumina particles were inconsistently found in biopsy specimens retrieved from hip capsules during revisions of aseptically loose cups that had been inserted without cement. Christel concluded that the overall foreign-body reaction to ceramic particles from loose alumina-alumina prostheses is less intense than the reaction to other orthopaedic biomaterials such as polyethylene, metal, or bone cement. The intensity of the cellular response in the current study was similar to what has been reported in association with other particulate materials. The difference between the findings in the current study and those in the study of Christel may be related to particle load.
We found little information in the literature concerning osteolysis in association with ceramic articulations. Huo et al., in their report on total hip replacement in which a prosthesis with a ceramic-on-ceramic bearing was inserted without cement, found no evidence of acetabular or femoral osteolysis at a mean of nine years after the operation19. However, Kummer et al. previously noted the potential for wear of implants with ceramic bearing surfaces23. They obtained samples from synovial tissue adjacent to six Autophor components that were removed because of failure, due primarily to mechanical loosening, eight to fifty-four months after the operation. Histological analysis revealed surface roughness on both the femoral head and the acetabulum. The amount of wear ranged from ten micrometers to more than three millimeters. Histological analysis showed inflammation with multiple histiocytes and fibrosis. Scanning electron microscopy demonstrated marked cratering and complete destruction of the polished surface in the areas of roughness. There were numerous particles in the tissue, and the mean particle diameter was approximately five micrometers23. There have been only a few reports of osteolysis associated with ceramic bearing surfaces. Borssen et al. described a patient who had severe osteolysis after a ceramic-on-ceramic total hip arthroplasty3. Shih et al. subsequently reported localized femoral osteolysis in eight (6 per cent) of 134 hips at a mean of nine years after a hip replacement with a ceramic prosthesis43. The prevalence of femoral osteolysis in the current series, in which the follow-up was shorter, was four times greater than that reported by Shih et al.
The pattern of osteolysis in the pelvis that we noted in association with loose ceramic sockets was similar to that commonly seen in association with loose sockets that have been inserted with cement51. Initially, a complete radiolucency forms at the bone-implant interface; as bone resorption occurs, the socket tends to migrate into the radiolucency. Bone loss is reflected by the progressive migration of the socket on serial radiographs. This is in contrast to the expansile pattern of osteolysis most commonly seen in association with porous-coated acetabular components that have been inserted without cement51. On the femoral side, the pattern of osteolysis was similar to that reported in association with other extensively porous-coated stems. Engh et al. reported an overall prevalence of osteolysis of 39 per cent (fifty-four hips) in association with an anatomic medullary locking (AML) prosthesis (DePuy) after a mean duration of follow-up of eleven years12. Nineteen per cent of the lesions were larger than 1.5 square centimeters. Osteolytic lesions in the femur were confined to the metaphysis. No diaphyseal osteolysis was noted.
In the current study, only two stems were associated with osteolysis in the diaphysis, and both were loose. On the basis of our data, it appears that bone growth into a circumferentially porous-coated stem offers some protection against osteolysis in the femoral diaphysis.
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Footnotes
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*One or more of the authors has received or will receive benefits for personal or professional use from a commercial party related directly or indirectly to the subject of this article. No funds were received in support of this study.
Department of Orthopaedic Surgery, Chonnam University Hospital, 8 Hak-dong, Kwangju 501-757, Korea. E-mail address for Dr. Yoon: tryoon@orion.chonnam.ac.kr.
Department of Orthopaedic Surgery, Barnes-Jewish Hospital, One Barnes Hospital Plaza, Suite 11300, West Pavilion, St. Louis, Missouri 63110.
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Abstract
Introduction
