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Letters to the Editor   |    
Osteolysis and Ceramic Bearing Surfaces
Jonathan P. Garino, M.D.; Laurent Sedel, M.D.; Remy Nizard, M.D.; Pascal Bizot, M.D.; Bengt Mjöberg, M.D.Ph.D.; Taek Rim Yoon, M.D.; Sung Man Rowe, M.D.; Sung Taek Jung, M.D.; Kwang Jin Seon, M.D.; William J. Maloney, M.D.; Charles R. Clark, M.D.
View Disclosures and Other Information
Department of Orthopaedic Surgery, Hospital of the University of Pennsylvania, 3400 Spruce Street, Silverstein Two, Philadelphia, Pennsylvania 19104-4283
Corresponding author: Laurent Sedel, M.D., H󯨴al Lariboisi籥, 2, rue Ambroise-Par窠75475 Paris, Cedex 10, France
Department of Orthopedics, Uppsala University Hospital, SE-751 85 Uppsala, Sweden
Corresponding author: Taek Rim Yoon, M.D., Department of Orthopaedics, Chonnam University Hospitalm, 8 Hakdong, Kwangju 501-757, Korea, E-mail address: tryoon@chonnam.ac.kr
Deputy Editor for Adult Reconstruction, The Journal of Bone and Joint Surgery, 20 Pickering Street, Needham, Massachusetts 02492-3157

The Journal of Bone & Joint Surgery.  2000; 82:1518-1518 
5 Recommendations (Recommend) | 3 Comments | Saved by 3 Users Save Case
To The Editor:
I read with great interest the article "Osteolysis in Association with a Total Hip Arthroplasty with Ceramic Bearing Surfaces" (80-A: 1459-1468, Oct. 1998), by Yoon et al. Although this is not the first article to demonstrate the potentially reactive nature of ceramic particles in and around total hip replacements, it represents the first thorough examination of a series of patients with a ceramic-on-ceramic articulation demonstrating such a high degree of osteolysis.
My main issue is with the editorial board of The Journal for accepting this paper in its current form, as it does not place proper perspective on ceramic-on-ceramic articulations. There is no question that the scientific work presented here is outstanding and that if ceramic particles reach, or are available in, the proper size, they too can activate the immune system and generate the inflammatory response leading to osteolysis, which is so commonly attributed to polyethylene. The problem is that this study is based on a device that could not obtain Food and Drug Administration approval in its current form and that was abandoned in the United States nearly a decade ago because of its high rate of failure. Not only does the acetabular component migrate frequently but that migration, coupled with a skirted ceramic ball head in many circumstances, frequently leads to ceramic-on-ceramic impingement. This ceramic-on-ceramic impingement was unique to this system. It led to the generation of ceramic debris at the point of impingement. Many of those particles found their way into the articulation where severe body wear was the end result and, I might add, not an unexpected result given the circumstances. Once in the articulation, small ceramic fragments can convert this stable articulation into a debris-production machine. The authors note that osteolysis of the pelvis did not occur in patients without acetabular migration. Although different types of compounds elicit immunological responses in varying degrees, particle size may be the most important variable. Any foreign material - ceramic, plastic, or metal - that is of the proper size will create osteolysis in a substantial percentage of patients. This type of osteolysis has not been reported in association with ceramic prosthetic components that have more favorable design characteristics14, but it has been reported when ceramic particles, whether they are from an articulating surface or are used as an opacifying agent in cement, are present in the proper size and in sufficient numbers9.
In the Discussion, the authors suggest that the diagnosis of avascular necrosis was a reason for the early failures and cite several articles from over a decade ago, when inferior techniques (first-generation cementing techniques) were used and age-matched controls were scant. Although they cite one recent paper, by Piston et al.15, another, more modern series of total hip arthroplasties performed with cement has suggested that patients with avascular necrosis can expect a rate of survival that is similar to that of age-matched controls with osteoarthritis5. The failures in the series of Yoon et al. were overwhelmingly due to component design, not diagnosis.
I am disappointed in The Journal's editorial staff for choosing to publish this article, given the known poor track record of this device. I would say that although the results are interesting, they are simply not relevant to any of the ceramic systems currently being developed for use in this country, in which ceramic-on-ceramic impingement is not possible. I am disappointed that the authors did not go beyond the clinical relevance relative to a decade ago and point out how many of the design shortcomings of the prostheses contributed to the osteolysis in their study as well as how they have been addressed in more modern designs. For these reasons, there is a strong danger that the readership of The Journal will fail to appreciate these design flaws and will attribute the debris production and subsequent osteolysis to the ceramic-on-ceramic articulation alone.
Jonathan P. Garino, M.D.
Department of Orthopaedic Surgery Hospital of the University of Pennsylvania 3400 Spruce Street, Silverstein Two Philadelphia, Pennsylvania 19104-4283
To The Editor:
We were very interested in the article "Osteolysis in Association with a Total Hip Arthroplasty with Ceramic Bearing Surfaces" (80-A: 1459-1468, Oct. 1998), by Yoon et al. As we implant ceramic-on-ceramic material every day in young and active people with hip disease, we are very aware of the details and conclusions that the authors describe.
Their study contained some excellent material, but we also believe that it included many overstatements and much speculation. They described a series of 169 total hips implanted in 143 patients between 1983 and 1989. By the time of the study, the Mittelmeier prosthesis, Autophor, had already been shown in Europe to be associated with too many failures related to mechanical aseptic loosening of both the cementless socket and the stem. These failures were attributed in part to impingement of the neck of the prosthesis on the ceramic and to the threaded shape of the cups inserted without cement. The fact that Yoon et al. observed many instances of socket loosening and many radiolucent lines at this level could easily have been predicted. Of the 169 hips, only 103 were followed for a five-year period. The authors did not present their material regarding survivorship analysis, which considers patients who drop out and allows comparison with other studies. All of the results were presented in percentages, which is far from acceptable when so many cases had dropped out.
The authors considered radiolucent lines or bone-implant demarcation as osteolysis. We suggest that this is an overstatement because the majority of the cases that were not revised were not examined histologically. They showed slow migration of an alumina cementless socket surrounded by a fibrocytic material without any sign of osteoclastic activity, which typically defines an osteolytic lesion. In effect, what they described in the few histological sections that were examined was more of a fibrocytic reaction than an aggressive foreign-body reaction. No osteoclastic activity was recorded, nor were trap-sensitive cells quantified. Some macrophagic activity and a few giant cells should not be considered as very aggressive. It could also have been related, as we have already demonstrated, to metallic debris resulting from alumina-stem impingement.
The stem of the prosthesis was made of a porous-coated cobalt-chromium alloy. But in contrast to others4 who used metal-on-polyethylene sliding material, Yoon et al. recorded no osteolysis in the diaphysis. Only metaphyseal bone destruction was noted, and it could have been related to stress-shielding or eventually to a high quantity of debris related to the mushroom-shaped ceramic head, as shown in Figs. 3-A and 3-B (page 1462), which was abandoned by Mittelmeier many decades ago. It is not surprising that some expansile osteolysis was noticed at the diaphyseal level in only two cases, both of which had this head configuration. We believe that only these two cases could be called osteolysis. The others were radiolucent lines in the acetabulum or at the proximal level of the femur.
Finally, the study of ten acetabular membranes obtained after mechanical failure of the screw-in design and three membranes obtained from proximal tissues surrounding the calcar region demonstrated that considerable ceramic debris was found in conjunction with metallic debris. This is not a surprise, and some years ago many investigators demonstrated that the surrounding tissues removed at revision operations involving ceramic hips contained some amount of alumina debris9. What was also demonstrated by us and many other investigators was that the biological responses to this debris were relatively benign and did not give rise to osteolysis except in some cases in which this debris was massively produced, as in these three samples. Moreover, in clinical practice, many authors from different parts of the world have made the same conclusions2. Failures of the ceramic components were mechanical, and osteolysis was encountered only in very specific cases. In our series, for example, a socket had been loose for one decade with titanium-on-ceramic impingement. A massive foreign-body reaction was encountered in this case. In Yoon et al.'s study of the retrieved material, we do not know how long the implants had been loose. It is not a surprise that a mushroom-shaped head design and a screw-in cup resulted in early loosening. This combination of implant designs often creates some degree of impingement and gives rise to accelerated wear of the ceramic components due to high contact stresses. All of this information has already been very well documented. In addition, it has also been demonstrated that stable, well fixed ceramic material does not give rise to osteolysis. This is not the case with other sliding materials16.
Overall, the article appears to be a negative endorsement of ceramic-on-ceramic material. We suggest that the authors were aware of this because their conclusions are similar to ours: the etiology of acetabular component loosening was mechanical, and no osteolysis was encountered at the diaphyseal level. Then why did they focus on linear osteolysis, which we consider to be an overstatement of the diagnosis of osteolysis? The reader must realize that even if some exceptional cases of osteolysis were described in conjunction with a ceramic-on-ceramic material, this pales in comparison with the great number described with metal-on-ultra high molecular weight polyethylene.
Alumina-on-alumina sliding components remain, as far as we know, the best answer for active and young people because of the material's remarkable biological tolerance at very long-term follow-up10,17. It is not a magic material, and surgical technique, component orientation, and design play a major role and are perhaps less forgiving than those associated with other implanted materials. This might have been the conclusion of their paper. We believe that the title would have been acceptable if it had been something like "Another Study of a Mittelmeier-Type Prosthesis."
Laurent Sedel, M.D. Remy Nizard, M.D. Pascal Bizot, M.D.
Corresponding author: Laurent Sedel, M.D. H󯨴al Lariboisiç±¥ 2, rue Ambroise-Parç??75475 Paris, Cedex 10, France
To The Editor:
Yoon et al., in their article "Osteolysis in Association with a Total Hip Arthroplasty with Ceramic Bearing Surfaces" (80-A: 1459-1468, Oct. 1998), report on periprosthetic osteolysis in stable as well as in unstable uncemented ceramic-on-ceramic hip prostheses and suggest that their study supports the prevalent dogma of wear-particle-induced osteolysis. Although their study contains interesting information, their theoretical framework may be deceptive. Some confusion seems to depend on the fact that, for years, loose prosthetic components may appear to be stable on conventional radiography.
It seems justified to call attention to an alternative explanation12,13, in which prosthetic loosening is postulated to be initiated at an early stage, either by insufficient initial fixation or by early loss of fixation. The initially slight loosening of the prosthetic component, resulting from either cause, is then influenced by the degree of stress during normal human activity, which is variable in different patients (because of differing body weight and level of physical activity) and for different components (because of differing prosthetic design, positioning, friction, and wear). Micromovements of the slightly loose prosthetic component cause joint fluid (and wear particles) to be pumped in and out of the bone-implant interface (where the smallest wear particles would penetrate farthest to the leading edge of bone resorption). The resulting pressure waves (up to 200 millimeters of mercury1) may devitalize a layer of bone1,18. The devitalized bone is resorbed. (Indeed, macrophages and giant cells in the interface membrane around failed cemented prostheses are found mainly in areas adjacent to the bone surface as opposed to the cement surface8.) The bone resorption may expand locally and cause focal osteolysis. The ejected joint fluid will be partially resorbed, and the inspissated wear debris may be invaded by granulation tissue. This explains the high concentration of wear debris found in these granulomatous lesions6.
It is interesting to note that an analogous mechanism has been described for the development of subchondral bone cysts in osteoarthritis7, in which joint fluid and pieces of cartilage are forced through a small fissure into the subchondral bone, forming a bone cyst. Granulation tissue subsequently invades the cyst - without participation of any foreign wear particles. Indeed, the periprosthetic accumulation of the wear debris in the tissue around loose prosthetic components may essentially be an epiphenomenon.
Bengt Mjöberg, M.D., Ph.D.
Department of Orthopedics Uppsala University Hospital SE-751 85 Uppsala, Sweden
T. R. Yoon, S. M. Rowe, S. T. Jung, K. J. Seon, and W. J. Maloney reply:
We are responding to the three letters concerning our article. As Dr. Garino noted, the implant system that was used and reported on in this study was abandoned in the United States approximately one decade ago. However, The Journal of Bone and Joint Surgery is an international journal, and this implant system is still in use in some parts of the world. It was used in South Korea until a few years ago and has now been abandoned there as well. Although the majority of published results with this implant system are poor, this is not universally true11. In addition, the purpose of this study was not to report a survivorship analysis with this implant system.
The purpose of this study was, as Dr. Garino noted, to report on the histological response associated with osteolysis secondary to ceramic wear particles. This system provided us with a unique opportunity to do so since no polyethylene and no bone cement were used in these implants. In addition, the vast majority of the extensively porous-coated stems were stable. Energy-dispersive analysis of radiographs demonstrated little or no metallic debris, and thus we were comfortable attributing the periprosthetic osteolysis to the ceramic debris.
The purpose of this study was not to impugn ceramic articulations. We agree, as stated in our Discussion, that the high rate of aseptic loosening of the socket was related to the design. We also agree that the diagnosis, young age, and high activity level of these particular patients, although contributory to the high failure rate, were not the primary reasons for failure.
Finally, Dr. Garino states that ceramic-on-ceramic systems in which ceramic-on-ceramic impingement is not possible are currently being developed in the United States. There is no doubt that both the manufacturing techniques and the implant design of ceramic components are improving. However, surgical implantation with respect to the angle of inclination, edge-loading, and neck-socket impingement (metal on ceramic) will continue to make the use of such devices somewhat more technically demanding. In addition, only long-term results will prove to the orthopaedic community that these design changes represent an improvement.
With regard to the comments of Professor Sedel et al., we have already addressed some of them above. Again, the purpose of our study was to report on the radiographic and biological response to a failed ceramic implant, not to present a survivorship analysis, which has already been done by several other authors. As such, the drop-out rate in this study is meaningless.
Professor Sedel et al. dispute our definition of osteolysis. On that point, we are quite comfortable. The pattern of osteolysis (linear compared with expansile) is determined by a variety of factors, the most important of which is the bone-remodeling pattern around a given implant system. This then determines access and the path of least resistance for joint fluid and wear particles from the articulation. Although the bias of Professor Sedel et al. toward what is and what is not osteolysis is widely held in orthopaedic surgery, we believe that it is incorrect. In all revised cases, there was granulation tissue and histologically demonstrated foreign-body reaction in the regions described radiographically as being osteolytic. They are incorrect in stating that we described "a fibrocytic material without any sign of osteoclastic activity." Furthermore, in the samples examined with energy-dispersive x-ray analysis, metallic debris was not significant. Histologically, metallic debris was noted in one out of three femoral membranes and zero out of ten acetabular membranes. We also disagree that "some macrophagic activity and a few giant cells should not be considered as very aggressive." This statement is contrary to a large body of work that has been done over the past decade. In the absence of wear particles, tissue macrophages are uncommon at the implant-bone interface. Their presence is synonymous with the presence of foreign-body particles. The presence of giant cells is more related to particle size and is not a factor in determining whether osteolysis will or will not develop. In these specimens, it was rare to find ceramic particles greater than ten micrometers in size, which we feel explains the paucity of giant cells seen in this tissue.
The metaphyseal bone destruction here was not related to stress-shielding but to particle-induced bone resorption. As an aside, it should be noted that even though there were some suggestions that stress-shielding makes the femur more prone to osteolysis, it is not universally true3. However, when osteolysis does develop with extensively and circumferentially coated femoral components, it is almost always limited to the metaphysis, provided that the implant is stabilized by bone ingrowth.
Again, we agree that design certainly played a role in the failure rate of this particular implant. Professor Sedel et al., in their letter, noted that the mushroom-shaped head design was likely contributory. However, only three of the implants reported in this series had that particular design.
Finally, we appreciate the extensive experience of Professor Sedel et al. with ceramic articulations and respect their opinion when they state that "alumina-on-alumina sliding components remain, as far as we know, the best answer for active and young people." They may well be right; however, it is not currently the most widely practiced technique.
Dr. Mjöberg suggests a potential alternative explanation for the development of osteolysis in these patients. His concept is suggested by the title of his recent article12, "Theories of Wear and Loosening in Hip Prostheses. Wear-Induced Loosening vs. Loosening-Induced Wear - a Review." We agree that both loosening and wear are probably playing a role, as it is our opinion that, with this socket design and fixation surface, osseointegration is not likely to occur in a high percentage of cases. When an implant is not osseointegrated, motion at the implant-bone interface with physiological load can result in the production of wear debris. This in turn can lead to periprosthetic bone resorption that, along with motion-induced bone resorption, can lead to further destabilization of the implant. We do not feel that this mechanism played an important role in the osteolysis in the proximal part of the femur, as most of the femoral components were stable.
The histology of pressure-induced osteolysis is quite different from that of particle-induced osteolysis. With pressure-induced osteolysis, there is bone resorption in association with necrosis. In contrast, particle-induced osteolysis is characterized by a foreign-body granuloma with activated osteoclasts. Bone necrosis is not a prominent feature. We believe that these represent two different mechanisms that have similar end points but are pathophysiologically quite different.
In terms of the mechanism for the development of a subchondral bone cyst in osteoarthritis, we would make two points. First, the role of fluid pressure in osteoclast activation in bone resorption is a hypothesis and not a proven fact. Second, it is important to note that with osteoarthritis there is likely to be cartilage debris in the joint. Cartilage debris is a potent stimulator of the inflammatory pathway and can of itself lead to secretion of bone-resorbing enzymes and cytokines.
We would like to express our thanks again to Dr. Garino, Professor Sedel et al., and Dr. Mjöberg for their interest and comments.
Taek Rim Yoon, M.D. Sung Man Rowe, M.D. Sung Taek Jung, M.D. Kwang Jin Seon, M.D. William J. Maloney, M.D.
Corresponding author: Taek Rim Yoon, M.D. Department of Orthopaedics Chonnam University Hospital 8 Hakdong Kwangju 501-757, Korea E-mail address: tryoon@chonnam.ac.kr
Editor's note:
In response to Dr. Garino's comments impugning the editors of The Journal for publishing this manuscript, I believe that Dr. Yoon's comments, as well as some of the points stated in his own letter, are appropriate. First of all, as Dr. Yoon correctly points out, The Journal of Bone and Joint Surgery is an international journal, and this implant is still in use in some parts of the world. More importantly, there is valuable information contained and conveyed in this work; as Dr. Garino acknowledged, "there is no question that the scientific work presented here is outstanding." Further, The Journal's editorial staff does not choose to publish articles based on the good or poor track record of a particular device. Rather, articles are chosen on the basis of scientific merit through a rigorous process of peer review, and, indeed, I wish to assure Dr. Garino that this was the case with this manuscript. Lastly, I believe that the readership of The Journal is enlightened enough to appreciate the design features of this particular device and their relationship to debris production. As Dr. Yoon succinctly points out in his reply, the purpose of this study was to report on the histological response, "not to impugn ceramic articulations."
Charles R. Clark, M.D.
Deputy Editor for Adult Reconstruction The Journal of Bone and Joint Surgery 20 Pickering Street Needham, Massachusetts 02492-3157
Anthony, P. P.; Gie, G. A.; Howie, C. R.;; and Ling, R. S. M.: Localised endosteal bone lysis in relation to the femoral components of cemented total hip arthroplasties. J. Bone and Joint Surg.,72-B(6): 971-979, 1990.72-B(6)971  1990 
 
Boehler, M.; Knahr, K.; Plenk, H., Jr.; Walter, A.; Salzer, M.; and Schreiber, V.: Long-term results of uncemented alumina acetabular implants. J. Bone and Joint Surg.,76-B(1): 53-59, 1994.76-B(1)53  1994 
 
Bugbee, W. D.; Culpepper, W. J., II; Engh, C. A., Jr.; and Engh, C. A., Sr.: Long-term clinical consequences of stress-shielding after total hip arthroplasty without cement. J. Bone and Joint Surg.,79-A: 1007-1012, July 1997.79-A1007  1997 
 
Engh, C. A., Jr.; Culpepper, W. J., II; and Engh, C. A.: Long-term results of use of the anatomic medullary locking prosthesis in total hip arthroplasty. J. Bone and Joint Surg.,79-A: 177-184, Feb. 1997.79-A177  1997 
 
Garino, J. P., and Steinberg, M. E.: Total hip arthroplasty in patients with avascular necrosis of the femoral head. A 2- to 10-year followup. Clin. Orthop.,334: 108-115, 1997.334108  1997  [PubMed]
 
Huo, M. H.; Salvati, E. A.; Lieberman, J. R.; Betts, F.; and Bansal, M.: Metallic debris in femoral endosteolysis in failed cemented total hip arthroplasties. Clin. Orthop.,276: 157-168, 1992 7.276157  1992 7  [PubMed]
 
Landells, J. W.:: The bone cysts of osteoarthritis. J. Bone and Joint Surg., 35-B(4): 643-649, 1953. 35-B(4)643  1953 
 
Lennox, D. W.; Schofield, B. H.; McDonald, D. F.; and Riley, L. H., Jr.: A histologic comparison of aseptic loosening of cemented, press-fit, and biologic ingrowth prostheses. Clin. Orthop.,,225: 171-191, 1987.225171  1987 
 
Lerouge, S.; Huk, O.; Yahia, L. H.; Witvoet, J.; and Sedel, L.: Ceramic-ceramic and metal-polyethylene total hip replacements. Comparison of pseudomembranes after loosening. J. Bone and Joint Surg., ,79-B(1): 135-139, 1997.79-B(1)135  1997 
 
Meunier, A.; Nizard, R.; Bizot, P.; and Sedel, L.: Clinical results of ceramic bearings in Europe. In Symposium on Alternative Bearing Surfaces in Total Joint Replacement. ASTM STP 1346, pp. 213-234. Edited by J. J. Jacobs and T. L. Craig. West Conshohocken, Pennsylvania, American Society for Testing and Materials, 1998. 
 
Mittelmeier, H., , and Heisel, J.: Sixteen-years' experience with ceramic hip prostheses. Clin. Orthop.,282: 64-72, 1992.28264  1992  [PubMed]
 
Mjöberg, B.: Theories of wear and loosening in hip prostheses. Wear-induced loosening vs. loosening-induced wear - a review. Acta Orthop. Scandinavica,65: 361-371, 1994.65361  1994 
 
Mjöberg, B.: The theory of early loosening of hip prostheses. Orthopedics,20: 1169-1175, 1997.201169  1997  [PubMed]
 
Nizard, R. S.; Sedel, L.; Christel, P.; Meunier, A.; Soudry, M.; and Witvoet, J.: Ten-year survivorship of cemented ceramic-ceramic total hip prosthesis. Clin. Orthop.,282: 53-63, 1992.28253  1992  [PubMed]
 
Piston, R. W.; Engh, C. A.; De Carvalho, P. I.; and Suthers, K.: Osteonecrosis of the femoral head treated with total hip arthroplasty without cement. J. Bone and Joint Surg.,76-A: 202-214, Feb 1994.76-A202  1994 
 
Sedel, L., and Cabanela, M. E. [editors]: Hip Surgery Materials and Developments. London, Martin Dunitz, 1998. 
 
Sedel, L.; Nizard, R.; Jaquot, F.; and Witvoet, J.: The cemented ceramic-on-ceramin bearing surface. In Total Hip Arthroplasty Outcomes, pp. 229-247. Edited by G. A. M. Finerman, F. J. Dorey, P. Grigoris, and H. A. McKellop. New York, Churchill Livingstone, 1998. 
 
van der Vis, H.; Aspenberg, P.; de Kleine, R.; Tigchelaar, W.; and van Noorden, C. J.: Short periods of oscillating fluid pressure directed at a titanium-bone interface in rabbits lead to bone lysis. Acta Orthop. Scandinavica,69: 5-10, 1998.695  1998 
 
 
 
 
 

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Anthony, P. P.; Gie, G. A.; Howie, C. R.;; and Ling, R. S. M.: Localised endosteal bone lysis in relation to the femoral components of cemented total hip arthroplasties. J. Bone and Joint Surg.,72-B(6): 971-979, 1990.72-B(6)971  1990 
 
Boehler, M.; Knahr, K.; Plenk, H., Jr.; Walter, A.; Salzer, M.; and Schreiber, V.: Long-term results of uncemented alumina acetabular implants. J. Bone and Joint Surg.,76-B(1): 53-59, 1994.76-B(1)53  1994 
 
Bugbee, W. D.; Culpepper, W. J., II; Engh, C. A., Jr.; and Engh, C. A., Sr.: Long-term clinical consequences of stress-shielding after total hip arthroplasty without cement. J. Bone and Joint Surg.,79-A: 1007-1012, July 1997.79-A1007  1997 
 
Engh, C. A., Jr.; Culpepper, W. J., II; and Engh, C. A.: Long-term results of use of the anatomic medullary locking prosthesis in total hip arthroplasty. J. Bone and Joint Surg.,79-A: 177-184, Feb. 1997.79-A177  1997 
 
Garino, J. P., and Steinberg, M. E.: Total hip arthroplasty in patients with avascular necrosis of the femoral head. A 2- to 10-year followup. Clin. Orthop.,334: 108-115, 1997.334108  1997  [PubMed]
 
Huo, M. H.; Salvati, E. A.; Lieberman, J. R.; Betts, F.; and Bansal, M.: Metallic debris in femoral endosteolysis in failed cemented total hip arthroplasties. Clin. Orthop.,276: 157-168, 1992 7.276157  1992 7  [PubMed]
 
Landells, J. W.:: The bone cysts of osteoarthritis. J. Bone and Joint Surg., 35-B(4): 643-649, 1953. 35-B(4)643  1953 
 
Lennox, D. W.; Schofield, B. H.; McDonald, D. F.; and Riley, L. H., Jr.: A histologic comparison of aseptic loosening of cemented, press-fit, and biologic ingrowth prostheses. Clin. Orthop.,,225: 171-191, 1987.225171  1987 
 
Lerouge, S.; Huk, O.; Yahia, L. H.; Witvoet, J.; and Sedel, L.: Ceramic-ceramic and metal-polyethylene total hip replacements. Comparison of pseudomembranes after loosening. J. Bone and Joint Surg., ,79-B(1): 135-139, 1997.79-B(1)135  1997 
 
Meunier, A.; Nizard, R.; Bizot, P.; and Sedel, L.: Clinical results of ceramic bearings in Europe. In Symposium on Alternative Bearing Surfaces in Total Joint Replacement. ASTM STP 1346, pp. 213-234. Edited by J. J. Jacobs and T. L. Craig. West Conshohocken, Pennsylvania, American Society for Testing and Materials, 1998. 
 
Mittelmeier, H., , and Heisel, J.: Sixteen-years' experience with ceramic hip prostheses. Clin. Orthop.,282: 64-72, 1992.28264  1992  [PubMed]
 
Mjöberg, B.: Theories of wear and loosening in hip prostheses. Wear-induced loosening vs. loosening-induced wear - a review. Acta Orthop. Scandinavica,65: 361-371, 1994.65361  1994 
 
Mjöberg, B.: The theory of early loosening of hip prostheses. Orthopedics,20: 1169-1175, 1997.201169  1997  [PubMed]
 
Nizard, R. S.; Sedel, L.; Christel, P.; Meunier, A.; Soudry, M.; and Witvoet, J.: Ten-year survivorship of cemented ceramic-ceramic total hip prosthesis. Clin. Orthop.,282: 53-63, 1992.28253  1992  [PubMed]
 
Piston, R. W.; Engh, C. A.; De Carvalho, P. I.; and Suthers, K.: Osteonecrosis of the femoral head treated with total hip arthroplasty without cement. J. Bone and Joint Surg.,76-A: 202-214, Feb 1994.76-A202  1994 
 
Sedel, L., and Cabanela, M. E. [editors]: Hip Surgery Materials and Developments. London, Martin Dunitz, 1998. 
 
Sedel, L.; Nizard, R.; Jaquot, F.; and Witvoet, J.: The cemented ceramic-on-ceramin bearing surface. In Total Hip Arthroplasty Outcomes, pp. 229-247. Edited by G. A. M. Finerman, F. J. Dorey, P. Grigoris, and H. A. McKellop. New York, Churchill Livingstone, 1998. 
 
van der Vis, H.; Aspenberg, P.; de Kleine, R.; Tigchelaar, W.; and van Noorden, C. J.: Short periods of oscillating fluid pressure directed at a titanium-bone interface in rabbits lead to bone lysis. Acta Orthop. Scandinavica,69: 5-10, 1998.695  1998 
 
 
 
 
 
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