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Histological Findings in a Proximal Femoral Structural Allograft Ten Years Following Revision Total Hip Arthroplasty A Case Report
Moussa Hamadouche, MD; Cinderella Blanchat, BS; Alain Meunier, PhD; Luc Kerboull, MD; Marcel Kerboull, MD
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Investigation performed at the Orthopaedic Research Laboratory, Paris, France

Moussa Hamadouche, MD
Luc Kerboull, MD
Marcel Kerboull, MD
Department of Orthopaedic and Reconstructive Surgery, Service A, Centre Hospitalo-Universitaire Cochin-Port Royal, 27 rue du Faubourg Saint Jacques, 75014 Paris, France

Cinderella Blanchat, BS
Alain Meunier, PhD
Orthopaedic Research Laboratory, Faculté de Médecine Lariboisière Saint-Louis, Université D. Diderot, Paris VII, UPRES A CNRS 7052, 10 avenue de Verdun, 75010 Paris, France

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. No funds were received in support of this study.

The Journal of Bone & Joint Surgery.  2002; 84:269-273 
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Failure of the femoral component with progressive bone loss is an important long-term complication of total hip arthroplasty. Among the different methods that have been advocated for dealing with massive femoral structural defects, bone-grafting is the only currently available procedure for restoring bone stock1-7. At the institution of the senior one of us (M.K.), a method to deal with deficient proximal femoral cortical bone was developed in 1987 and has been in use since that time8. This technique consists of impaction of a proximal femoral structural allograft into the host femur. A femoral component of standard length then is cemented only into the allograft. The clinical and radiographic results have been satisfactory, with one revision among twenty-seven procedures after a mean of five years of follow-up8. However, the underlying process of incorporation of a massive allograft remains unknown. To the best of our knowledge, there are no reports in the literature of the long-term results of histological evaluation of a massive allograft following revision total hip arthroplasty. The aim of this report is to address the issue of long-term incorporation and remodeling of a femoral structural allograft.
 
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+Fig. 1-A:Figs. 1-A, 1-B, and 1-C Serial anteroposterior radiographs of the patient. Fig. 1-A Preoperative radiograph showing major structural bone loss on the femoral side with deficient proximal part of the femur.
 
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+Fig. 1-B:Fig. 1-B One year after the arthroplasty, the graft has healed to the host (arrows).
 
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+Fig. 1-C:Fig. 1-C At ten years, there has been resorption of the proximal portion of the allograft (arrow). No migration of the femoral stem is seen.
 
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+Fig. 2:Microradiograph of a transverse section obtained at the graft-host junction. There are differences in pore size and density between the host bone (1) and the allograft (3). No demarcation line is present, indicating that the graft has healed to the host. However, remodeling has not proceeded more than a few millimeters into the graft (2).
 
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+Fig. 3:Photomicrograph of an unremodeled area of the allograft, showing empty lacunae (black arrows) and microfractures (white arrows). Cellular debris is present in the middle of the image (Stevenel blue and van Gieson picrofuchsin, 100).
 
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+Fig. 4:Low-magnification photomicrograph of the allograft-host junction. Newly formed bone (white arrow) is present on the allograft surface bridged to the host. The microfractures (black arrows) are parallel or perpendicular to the newly formed osteons (van Gieson picrofuchsin, 40).
A sixty-nine-year-old woman with an initial diagnosis of hip dysplasia was referred to our department in 1989 because of intractable pain in the groin related to a loose total hip prosthesis. She had had multiple procedures about the hip, including a revision total hip arthroplasty performed in 1982, which had resulted in 7 cm of shortening. At the seven-year follow-up evaluation, the functional outcome, based upon the findings of the clinical examination9, was poor. Both components were loose, and there was extensive bone loss on the femoral side (Fig. 1-A). Laboratory tests (C-reactive protein level and sedimentation rate) and a hip-joint aspiration showed no sign of infection.
The arthroplasty was revised, and both components were found to be grossly loose. On the acetabular side, a type-III defect according to the classification of the American Academy of Orthopaedic Surgeons10 was reconstructed with allograft and supported with a Kerboull acetabular reinforcement device11 (Benoist Gerard, Howmedica, Hérouville Saint Clair, France). There was substantial loss of the proximal part of the femur. A whole proximal femoral allograft, 16 cm in length, was shaped and tightly press-fit into the remaining, distal part of the femur. In order to reduce the leg-length discrepancy, only the distal 11 cm of the graft was impacted into the host femur. The allograft was obtained from the bone bank at our institution, which is in compliance with national standards for screening, culture, and storage of bone tissue. The allograft had been irradiated at 25 kGy and was deep-frozen at —80°C. A standard-length femoral prosthesis (CMK; Benoist Gerard, Howmedica) was cemented with use of CMW type-1 bone cement (DePuy, Devon, England) into the allograft only, with use of a bone plug placed 1 cm distal to the tip of the stem. The greater trochanter was attached to the allograft.
Postoperative treatment included anticoagulation therapy, systemic antibiotics, and nonsteroidal anti-inflammatory drugs (ketoprofen, 100 mg/day) to prevent heterotopic ossification. Immediately postoperatively, passive-motion exercises for the involved joint were undertaken. The patient was free to walk with two supports and to bear partial weight (10 kg) after three days. Full weight-bearing was delayed until the third month. The greater trochanter did not unite. However, at one year the hip was graded as very good (pain-free, 90° of flexion, and a mild limp that required the patient to use a cane for walking long distances) according to the functional score of Merle d’Aubigné9. The graft had united radiographically to the host bone, as suggested by the presence of a callus at the allograft-host bone interface (Fig. 1-B). The functional outcome continued to be satisfactory despite a mild limp. However, progressive resorption of the proximal femoral allograft was observed.
At the ten-year follow-up visit, the first 5 cm of the graft (the portion not in contact with host bone) had been resorbed almost completely (Fig. 1-C). To avoid a fatigue fracture of the stem, which was still well fixed in the distal portion of the allograft, the patient had a repeat revision with insertion of another proximal femoral allograft. The distal part of the first allograft was left inside the medullary canal. Multiple specimens were harvested from the remaining proximal portion of the graft, with the patient’s informed consent obtained prior to the procedure. In addition, at the graft-host junction, circumferential transverse sections were obtained. The biopsy specimens were fixed in 10% formalin, dehydrated in a graded series of ethanol, cleared in xylol, and embedded in methylmethacrylate. Serial transverse sections were obtained with use of a water-cooled diamond saw (Leica model 1600; Leica, Nussloch, Germany), ground to a thickness of 100 m (EXAKT-MicroGrinding System; Exakt, Norderstedt, Germany), and surface-stained with Stevenel blue and van Gieson picrofuchsin for standard and polarized light microscopy. Microradiographs were made to evaluate the density of the allograft.
There was no evidence of deep infection, and all of the cultures remained sterile. During the repeat revision, the femoral stem was judged to be stable on intraoperative examination. Macroscopically, the allograft appeared as viable bleeding bone surrounded by host bone. It had united to the host bone, creating cortices of normal thickness; however, it was distinguishable from the recipient bone, as it appeared denser. This was confirmed by microradiographic analysis, which showed the allograft to be more densely mineralized and to have a smaller pore size than the host bone (Fig. 2).
Histological analysis revealed three zones in the allograft. The inner layer, which was in contact with the bone cement, was composed of trabeculae of dead bone and cellular debris. The trabeculae had empty lacunae, and there was no remodeling activity (Fig. 3). The interfacial layer, which was in contact with the host bone, was composed of areas of remodeling bone and normal cells consisting of osteoclasts, osteoblasts, and fatty bone marrow (Fig. 4). Newly formed bone and osteoid also were present in this layer, as it was undergoing creeping substitution. In between these two layers, a sparsely cellular layer containing unremodeled areas with resorption was seen. Revascularization of the graft had occurred through the formation of woven bone to a depth of 5 mm. No fibrous membrane between the allograft and the host femur was observed.
Of note was the fact that the unremodeled area of the allograft contained numerous microfractures, which were not present in the remodeled area (Fig. 4). At a higher magnification, the difference between the newly formed bone and the unremodeled area was even more perceptible. The microfractures in the allograft were either parallel or perpendicular to the bone lamellae; however, they bypassed the newly formed osteons at the level of the cement line.
Little is known about the long-term histological features of allograft bone incorporation following revision total hip arthroplasty. Some authors have reported evidence of incorporation of morselized graft following impaction grafting12-15. Most of the histological data about massive allografts pertain to specimens retrieved from patients who underwent reconstruction following en bloc resection of a tumor16,17. We are aware of only one report on incorporation of structural allografts following revision of the femoral component; in that study, specimens were obtained from five irradiated bone allograft struts that had been implanted two to twenty-seven months previously18. The authors noted a time-dependent incorporation process, with the most marked osteoclastic resorption seen in the samples that had been obtained soon after implantation. Remodeling and new-bone formation were most marked in the specimens that had been in situ for longer periods. The extent of revascularization into the allograft was not indicated18.
In our patient, at the ten-year follow-up evaluation, the massive allograft was partly revascularized where it was in contact with host bone. The incorporation process had been very slow, as newly formed bone was not observed beyond a depth of 5 mm into the graft. The allograft’s density and relatively small surface area may explain its slow and incomplete revascularization. The portions of the allograft that were not in contact with host bone were mostly resorbed.
The presence of microfractures in the unremodeled area of the allograft cannot be attributed to artifacts as microfractures were not present in remodeled areas or in host bone. It is also unlikely that they were related to the sterilization process19,20. We believe that they were of mechanical origin, as hypothesized by Gouin et al.17. Irradiation at a standard dose does not alter the elasticity of the material, but it has been proven to diminish the bone’s capacity to withstand load21,22. This results in a loss of the plastic behavior of the graft (embrittlement), with a reduction in the hoop strength of the structure, perhaps explaining the formation of microfractures through a fatigue mechanism.
While this is a single case report, our findings suggest that, when a structural femoral graft is utilized during revision hip arthroplasty, the host femur should be retained in order to enhance allograft incorporation.
Note: The authors are very grateful to Miguel E. Cabanela, MD, and Daniel J. Berry, MD, of the Mayo Clinic, Rochester, Minnesota, for their comments.
Allan DG, Lavoie GJ, McDonald S, Oakeshott R,Gross AE. Proximal femoral allografts in revision hip arthroplasty. J Bone Joint Surg Br,1991;73: 235-40. 73235  1991  [PubMed]
 
Chandler H, Clark J, Murphy S, McCarthy J, Penenberg B, Danylchuck K,Roehr B. Reconstruction of major segmental loss of the proximal femur in revision total hip arthroplasty. Clin Orthop,1994;298: 67-74. 29867  1994  [PubMed]
 
Emerson RH Jr, Malinin TI, Cuellar AD, Head WC,Peters PC. Cortical strut allografts in the reconstruction of the femur in revision total hip arthroplasty. A basic science and clinical study. Clin Orthop,1992;285: 35-44. 28535  1992  [PubMed]
 
Gross AE,Hutchison CR. Proximal femoral allografts for reconstruction of bone stock in revision arthroplasty of the hip. Orthop Clin North Am,1998;29: 313-7. 29313  1998  [PubMed]
 
Haddad FS, Garbuz DS, Masri BA,Duncan CP. Structural proximal femoral allografts for failed total hip replacements: a minimum review of five years. J Bone Joint Surg Br,2000;82: 830-6. 82830  2000  [PubMed]
 
Head WC,Malinin TI. Results of onlay allografts. Clin Orthop,2000;371: 108-12. 371108  2000  [PubMed]
 
Slooff TJ, Buma P, Schreurs BW, Schimmel JW, Huiskes R,Gardeniers J. Acetabular and femoral reconstruction with impacted graft and cement. Clin Orthop,1996;324: 108-15. 324108  1996  [PubMed]
 
Kerboull M. Traitement des descellements fémoraux aseptiques des prothèses totales de hanche. In: Cahiers d’enseignement de la SOFCOT. Paris: Expansion Scientifique Française; 1996. p 1-17 
 
Merle d’Aubigné R. Numerical evaluation of hip function. Rev Chir Orthop Reparatrice Appar Mot,1970;56: 481-6. French56481  1970  [PubMed]
 
D’Antonio JA, Capello WN, Borden LS, Bargar WL, Bierbaum BF, Boettcher WG, Steinberg ME, Stulberg SD,Wedge JH. Classification and management of acetabular abnormalities in total hip arthroplasty. Clin Orthop,1989;243: 126-37. 243126  1989  [PubMed]
 
Kerboull M, Hamadouche M,Kerboull L. The Kerboull acetabular reinforcement device in major acetabular reconstructions. Clin Orthop,2000;378: 155-68. 378155  2000  [PubMed]
 
Ling RS, Timperley AJ,Linder L. Histology of cancellous impaction grafting in the femur. A case report. J Bone Joint Surg Br,1993;75: 693-6. 75693  1993  [PubMed]
 
Mikhail WE, Weidenhielm LR, Wretenberg P, Mikhail N,Bauer TW. Femoral bone regeneration subsequent to impaction grafting during hip revision: histologic analysis of a human biopsy specimen. J Arthroplasty,1999;14: 849-53. 14849  1999  [PubMed]
 
Nelissen RG, Bauer TW, Weidenhielm LR, LeGolvan DP,Mikhail WE. Revision hip arthroplasty with the use of cement and impaction grafting. Histological analysis of four cases. J Bone Joint Surg Am,1995;77: 412-22. 77412  1995  [PubMed]
 
Ullmark G,Linder L. Histology of the femur after cancellous impaction grafting using a Charnley prosthesis. Arch Orthop Trauma Surg,1998;117: 170-2. 117170  1998  [PubMed]
 
Enneking WF,Mindell ER. Observations on massive retrieved human allografts. J Bone Joint Surg Am,1991;73: 1123-42. 731123  1991  [PubMed]
 
Gouin F, Passuti N, Verriele V, Delecrin J,Bainvel JV. Histological features of large bone allografts. J Bone Joint Surg Br,1996;78: 38-41. 7838  1996  [PubMed]
 
Hamer AJ, Suvarna SK,Stockley I. Histologic evidence of cortical allograft bone incorporation in revision hip surgery. J Arthroplasty,1997;12: 785-9. 12785  1997  [PubMed]
 
Pelker RR, Friedlaender GE. Biomechanical considerations in ostechondral grafts. In: Friedlaender GE, Goldberg VM, editors. Bone and cartilage allografts. Park Ridge, IL: American Academy of Orthopaedic Surgeons; 1991. p 155-62 
 
Pelker RR, McKay J Jr, Troiano N, Panjabi MM,Friedlaender GE. Allograft incorporation: a biomechanical evaluation in a rat model. J Orthop Res,1989;7: 585-9. 7585  1989  [PubMed]
 
Godette GA, Kopta JA,Egle DM. Biomechanical effects of gamma irradiation on fresh frozen allografts in vivo. Orthopedics,1996;19: 649-53. 19649  1996  [PubMed]
 
Hamer AJ, Strachan JR, Black MM, Ibbotson CJ, Stockley I,Elson RA. Biomechanical properties of cortical allograft bone using a new method of bone strength measurement. A comparison of fresh, fresh-frozen and irradiated bone. J Bone Joint Surg Br,1996;78: 363-8. 78363  1996  [PubMed]
 

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Anchor for JumpAnchor for Jump
+Fig. 1-A:Figs. 1-A, 1-B, and 1-C Serial anteroposterior radiographs of the patient. Fig. 1-A Preoperative radiograph showing major structural bone loss on the femoral side with deficient proximal part of the femur.
Anchor for JumpAnchor for Jump
+Fig. 1-B:Fig. 1-B One year after the arthroplasty, the graft has healed to the host (arrows).
Anchor for JumpAnchor for Jump
+Fig. 1-C:Fig. 1-C At ten years, there has been resorption of the proximal portion of the allograft (arrow). No migration of the femoral stem is seen.
Anchor for JumpAnchor for Jump
+Fig. 2:Microradiograph of a transverse section obtained at the graft-host junction. There are differences in pore size and density between the host bone (1) and the allograft (3). No demarcation line is present, indicating that the graft has healed to the host. However, remodeling has not proceeded more than a few millimeters into the graft (2).
Anchor for JumpAnchor for Jump
+Fig. 3:Photomicrograph of an unremodeled area of the allograft, showing empty lacunae (black arrows) and microfractures (white arrows). Cellular debris is present in the middle of the image (Stevenel blue and van Gieson picrofuchsin, 100).
Anchor for JumpAnchor for Jump
+Fig. 4:Low-magnification photomicrograph of the allograft-host junction. Newly formed bone (white arrow) is present on the allograft surface bridged to the host. The microfractures (black arrows) are parallel or perpendicular to the newly formed osteons (van Gieson picrofuchsin, 40).
Allan DG, Lavoie GJ, McDonald S, Oakeshott R,Gross AE. Proximal femoral allografts in revision hip arthroplasty. J Bone Joint Surg Br,1991;73: 235-40. 73235  1991  [PubMed]
 
Chandler H, Clark J, Murphy S, McCarthy J, Penenberg B, Danylchuck K,Roehr B. Reconstruction of major segmental loss of the proximal femur in revision total hip arthroplasty. Clin Orthop,1994;298: 67-74. 29867  1994  [PubMed]
 
Emerson RH Jr, Malinin TI, Cuellar AD, Head WC,Peters PC. Cortical strut allografts in the reconstruction of the femur in revision total hip arthroplasty. A basic science and clinical study. Clin Orthop,1992;285: 35-44. 28535  1992  [PubMed]
 
Gross AE,Hutchison CR. Proximal femoral allografts for reconstruction of bone stock in revision arthroplasty of the hip. Orthop Clin North Am,1998;29: 313-7. 29313  1998  [PubMed]
 
Haddad FS, Garbuz DS, Masri BA,Duncan CP. Structural proximal femoral allografts for failed total hip replacements: a minimum review of five years. J Bone Joint Surg Br,2000;82: 830-6. 82830  2000  [PubMed]
 
Head WC,Malinin TI. Results of onlay allografts. Clin Orthop,2000;371: 108-12. 371108  2000  [PubMed]
 
Slooff TJ, Buma P, Schreurs BW, Schimmel JW, Huiskes R,Gardeniers J. Acetabular and femoral reconstruction with impacted graft and cement. Clin Orthop,1996;324: 108-15. 324108  1996  [PubMed]
 
Kerboull M. Traitement des descellements fémoraux aseptiques des prothèses totales de hanche. In: Cahiers d’enseignement de la SOFCOT. Paris: Expansion Scientifique Française; 1996. p 1-17 
 
Merle d’Aubigné R. Numerical evaluation of hip function. Rev Chir Orthop Reparatrice Appar Mot,1970;56: 481-6. French56481  1970  [PubMed]
 
D’Antonio JA, Capello WN, Borden LS, Bargar WL, Bierbaum BF, Boettcher WG, Steinberg ME, Stulberg SD,Wedge JH. Classification and management of acetabular abnormalities in total hip arthroplasty. Clin Orthop,1989;243: 126-37. 243126  1989  [PubMed]
 
Kerboull M, Hamadouche M,Kerboull L. The Kerboull acetabular reinforcement device in major acetabular reconstructions. Clin Orthop,2000;378: 155-68. 378155  2000  [PubMed]
 
Ling RS, Timperley AJ,Linder L. Histology of cancellous impaction grafting in the femur. A case report. J Bone Joint Surg Br,1993;75: 693-6. 75693  1993  [PubMed]
 
Mikhail WE, Weidenhielm LR, Wretenberg P, Mikhail N,Bauer TW. Femoral bone regeneration subsequent to impaction grafting during hip revision: histologic analysis of a human biopsy specimen. J Arthroplasty,1999;14: 849-53. 14849  1999  [PubMed]
 
Nelissen RG, Bauer TW, Weidenhielm LR, LeGolvan DP,Mikhail WE. Revision hip arthroplasty with the use of cement and impaction grafting. Histological analysis of four cases. J Bone Joint Surg Am,1995;77: 412-22. 77412  1995  [PubMed]
 
Ullmark G,Linder L. Histology of the femur after cancellous impaction grafting using a Charnley prosthesis. Arch Orthop Trauma Surg,1998;117: 170-2. 117170  1998  [PubMed]
 
Enneking WF,Mindell ER. Observations on massive retrieved human allografts. J Bone Joint Surg Am,1991;73: 1123-42. 731123  1991  [PubMed]
 
Gouin F, Passuti N, Verriele V, Delecrin J,Bainvel JV. Histological features of large bone allografts. J Bone Joint Surg Br,1996;78: 38-41. 7838  1996  [PubMed]
 
Hamer AJ, Suvarna SK,Stockley I. Histologic evidence of cortical allograft bone incorporation in revision hip surgery. J Arthroplasty,1997;12: 785-9. 12785  1997  [PubMed]
 
Pelker RR, Friedlaender GE. Biomechanical considerations in ostechondral grafts. In: Friedlaender GE, Goldberg VM, editors. Bone and cartilage allografts. Park Ridge, IL: American Academy of Orthopaedic Surgeons; 1991. p 155-62 
 
Pelker RR, McKay J Jr, Troiano N, Panjabi MM,Friedlaender GE. Allograft incorporation: a biomechanical evaluation in a rat model. J Orthop Res,1989;7: 585-9. 7585  1989  [PubMed]
 
Godette GA, Kopta JA,Egle DM. Biomechanical effects of gamma irradiation on fresh frozen allografts in vivo. Orthopedics,1996;19: 649-53. 19649  1996  [PubMed]
 
Hamer AJ, Strachan JR, Black MM, Ibbotson CJ, Stockley I,Elson RA. Biomechanical properties of cortical allograft bone using a new method of bone strength measurement. A comparison of fresh, fresh-frozen and irradiated bone. J Bone Joint Surg Br,1996;78: 363-8. 78363  1996  [PubMed]
 
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