J Orthop Sci (2006) 11:632–637 DOI 10.1007/s00776-006-1067-0
Case report Histopathological study of osteonecrosis 19 years after transtrochanteric rotational osteotomy Akihisa Yamashita1,2, Takuaki Yamamoto2, Seiya Jingushi2, Yukihide Iwamoto2, Yoichi Sugioka2, and Katsuo Sueishi1 1
Division of Pathophysiological and Experimental Pathology, Department of Pathology, Graduate School of Medical Science, Kyushu University, 3-1-1 Maidashi, Higashi-ku, Fukuoka 812-8582, Japan 2 Department of Orthopedic Surgery, Graduate School of Medical Science, Kyushu University, Fukuoka, Japan
Introduction Aseptic and nontraumatic osteonecrosis of the femoral head of unknown etiology mainly affects young and middle-aged patients. At the weight-bearing portion of the necrotic femoral head, a subchondral fracture, a socalled collapse lesion,1,2 often occurs, in the joint surface being focally depressed. Owing to joint incongruity, the collapsed femoral head progresses to secondary arthritis. Transtrochanteric anterior/posterior rotational osteotomy, a joint-preserving procedure, was developed by Sugioka in 1978.3 This procedure involves transposing the intact area to a weight-bearing portion of the joint, resulting in transfer of the necrotic area to a nonweight-bearing portion, which can reduce instability at the boundary between the necrotic and intact areas.3,4 Long-term satisfactory clinical results have been reported with this procedure.5–7 Sugioka and co-workers reported that two cases of osteonecrosis treated by transtrochanteric rotational osteotomy were completely healed by viable fibrous tissue at the time of the salvage operation.6 Moreover, using biopsy samples, Yasunaga and colleagues performed histological analyses of nine femoral heads at a mean of 2.5 years after transtrochanteric anterior rotational osteotomy; they reported that in seven of the nine femoral heads the necrotic area was replaced by vascular-rich fibrous tissue, and new bone covered the dead trabeculae. However, these repair processes were considerably limited; that is, they did not extend over the entire necrotic area.8 Their reports nonetheless suggest that the necrotic area removed from weight-bearing by transtrochanteric anterior/posterior rotational osteotomy seemed to be repaired and remodeled histopathologically. However, that study did not address the long-term (i.e., more than Offprint requests to: K. Sueishi Received: March 10, 2006 / Accepted: August 10, 2006
10 years) repair and remodeling effects in the entire femoral head after transtrochanteric rotational osteotomy. The purpose of this report was to describe the histopathological findings about repair processes following osteonecrosis, as observed 19 years after transtrochanteric anterior rotational osteotomy.
Case report A 32-year-old man with a diagnosis of bilateral osteonecrosis of the femoral head was referred to our department in 1981. No history of corticosteroid therapy could be elicited, but alcohol abuse was noted (the quantity consumed, converted to pure ethanol, was 1000 ml per week). Radiographs of the bilateral hip joints revealed collapse of the femoral head, band-like sclerosis, and a cystic lesion (Fig. 1A,B), which was classified as type Ic and stage III according to the Japanese Ministry of Health and Welfare classification9,10 and the Ficat and Arlet staging system,11 respectively. The necrotic area was limited to the anterior portion of the femoral head, and the posterior portion remained intact. A left transtrochanteric posterior rotational osteotomy was immediately performed, followed by a right transtrochanteric anterior rotational osteotomy 1 month after the initial surgery. Radiographs obtained immediately after each operation revealed that the weight-bearing portion was replaced by the intact area and the necrotic area was transposed to the anteroinferior portion of the femoral head by 75° of anterior rotation with intentional varus positioning (Fig. 1C–E). The postoperative ratios of transposed intact articular surface of the femoral head to the weight-bearing surface of the acetabulum on the anteroposterior-view “intact area” of the right and left femoral head were 40% and 38%, respectively.6 Postoperative treatment was well tolerated and administered
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without complications. The patient walked using crutches for only 2 years after the surgery. The patient’s hip joint function gradually improved, and his symptoms disappeared. No re-collapse was observed at any of the follow-up radiological examinations, which were performed annually for at least 5 years after the treatment (Fig. 1F–H). Other imaging studies, such as bone scans, computed tomography (CT), or magnetic resonance imaging (MRI), were not performed because the patient did not consent to them. Unfortunately, the patient had not continued with the yearly examinations because he was pain-free. We later received information about his symptoms of right coxalgia related to long-distance walking that appeared about 15 years after the surgery. At 19 years after the operation, when he was 51 years of age, he was diagnosed with right coxalgia that had appeared spontaneously and left hip dullness associated with gait and joint motion. On radiological examination, the bilateral hip joints, but particularly on the right side, showed secondary osteoarthritis, including narrowing of the joint space, sclerosis of the subchondral bone, and marked osteophyte formation (Fig. 1I, J). Because of the gradually increasing right coxalgia, the patient underwent right total hip arthroplasty after an 11-month observation period. The patient was informed that data concerning the case would be submitted for publication.
Pathologic findings Grossly, the removed right femoral head showed marked deformity due to osteoarthritic changes. Serial sections (2 mm thick) along the sagittal plane were obtained using a band saw. Examination of the cut sections revealed that the bone marrow was yellow and focally replaced by white fibrous tissue in an area that generally overlapped the original necrotic area (Fig. 2A). There was no wedge-shaped opaque yellow region, which is commonly seen in cases of osteonecrosis. A soft X-ray photograph using Softex imaging equipment (CMB-2; Softex, Tokyo, Japan) of a 22-mm section from the medial edge of the femoral head revealed regularly distributed thin bone trabeculae, a cystic lesion at the site of the original necrotic area, and thick bone trabeculae, which were distributed in a laminar pattern and ran parallel to the surface of the femoral head (Fig. 2B). Microscopically, in the original region of osteonecrosis, the subchondral area consisted of viable bone trabeculae and matured fatty marrow tissue; there was no histopathological evidence of osteonecrosis (e.g., empty lacunae or pyknotic osteocyte nuclei) or necrotic marrow tissue (Fig. 3B). Chondroid metaplasia focally lined with osteoblast-like cells was also seen in the
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subchondral bone tissue, which may have been a sign of remnant subchondral fracture (Fig. 3C). A pseudocyst consisting of fibroadipose connective tissue containing sequestrated bone fragments was also noted (Fig. 3D). In the current weight-bearing portion of the joint, the articular cartilage was focally denuded and showed marked fibrillation and irregular distribution of chondrocytes. Some cystic lesions were noted in the subchondral region. These histopathological findings were compatible with those of secondary osteoarthritis (Fig. 3E).
Discussion Osteonecrosis of the femoral head is usually associated with morbid conditions involving the use of corticosteroids, in particular pulse therapy or highdose therapy mainly for autoimmune diseases.1,2 Some hypotheses regarding the etiology of this disease have been suggested (e.g., arterial thrombosis,12,13 fat embolism,12,14 venous outflow obstruction,15 increased interosseous pressure,16 enlargement of fat cell size,16 accumulation of lipid in osteocytes,17 and intravascular coagulation activated by several conditions including bacterial endotoxic reactions18) both experimentally and histopathologically; and yet the pathogenesis remains unclear. It is also likely that the development of this disease is due to several reciprocal factors among those mentioned above. We considered the possibility that the osteonecrosis observed in the present case might have been replaced and repaired by fibrous granulation tissue or bone tissue followed by bone remodeling. Unfortunately, osteonecrosis usually develops at the weight-bearing portion of the hip joint, and collapse following subchondral microfracture occurs. As a consequence of collapse, the hip joint is misaligned and develops secondary osteoarthritis. Sugioka’s transtrochanteric anterior/posterior rotational osteotomy was developed as a joint-preserving operation for patients with osteonecrosis of the femoral head.3,6 Sugioka and co-workers studied the clinical and radiological outcomes of transtrochanteric anterior rotational osteotomy in 295 hips with follow-up periods ranging from 3 to 16 years. They reported that the clinical and radiological outcomes chiefly depended on the transposed intact area/acetabular weight-bearing portion ratio after osteotomy and that the transposed intact area should amount to more than 36% of the acetabular weight-bearing area.6 Recently, Miyanishi et al. studied the correlation between the prevention of progressive collapse and the ratio of intact articular surface after transtrochanteric rotational osteotomy in 125 hips. To prevent progressive radiological collapse over a 10-year period, a minimum postoperative intact ratio of 34%
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was required.19 In our case, the postoperative ratios of the intact right and left femoral head were 40% and 38%, respectively. Therefore, the durability and survival of the bilateral femoral heads in the present case lasted 19 years, supporting our criteria for the osteotomy. Yasunaga and colleagues reported that the necrotic area was replaced by vascular-rich fibrous tissue with the presence of the dead trabeculae in part and covered by new bone formation, suggesting a repair process at a mean of 2.5 years after transtrochanteric rotational osteotomy.8 They noted that bone regeneration is an extremely slow process and originates in invasion and replacement of fibrous connective tissue. In our case, the original necrotic area consisted of viable bone trabeculae and matured fatty marrow tissue entirely, and there was no evidence of current osteonecrosis, such as necrotic bone trabeculae and marrow tissue; therefore it was thought that the repair process had been accomplished except for a pseudocyst described below. Because the pseudocyst, located in the original necrotic area, consisted of fibroadipose connec-
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tive tissue focally containing sequestrated bone fragments and amorphous debris and was covered by additional thick bone trabeculae, we speculated that its formation seemed to be remnant of the necrotized marrow tissue. These histopathological findings suggest that when osteotomy is performed with the appropriate indications and technique long-term repair processes that are mainly based on fibrous and vascular-rich granulation tissue are induced. Nevertheless, because this patient had not been examined 5 years after the osteotomy and we had received no information about radiological findings until 19 years later, it is possible that other factors took part in the repair processes in the necrotic area. Probably radiological osteoarthritic changes would have been seen earlier in this patient had he be examined. It was thought that the remodeling processes, based on secondary osteoarthritis, seemed to affect the repair processes to some extent, in addition to the fibrogranulation tissue-induced repair process. To date, the following primary reasons or conditions for failure of the osteotomy have been reported: (1) the
B Fig. 2. Gross appearance of the resected femoral head. A Cut section shows yellow marrow tissue focally replaced by white fibrous tissue, approximately covering the region of the original necrotic area (arrowheads). B Soft X-ray radiograph
shown in A demonstrates regularly distributed thin bone trabeculae and a cystic lesion in the original necrotic area as well as thick bone trabeculae distributed in a laminar pattern (arrows)
䉳 Fig. 1. A,B Preoperative radiographs of the right (A) and left (B) hip joints. Both femoral heads show collapse of the articular surface (arrows), band-like sclerosis, and a cystic lesion (asterisk). C–E Radiographs taken immediately after transtrochanteric anterior rotational osteotomy. C Right hip, anteroposterior (AP) view. D Right hip, Lauenstein view. E Left hip, AP view. Each osteonecrotic area was transposed to the anteroinferior portion, and the weight-bearing portions of each femoral head were replaced by intact areas. F–H Radiographs taken 5 years after osteotomy. F Right hip, AP
view. G Right hip, Lauenstein view. H Left hip, AP view. Joint spaces were almost completely preserved. No secondary arthritic changes were noted at the time. On the right side (F,G), the articular surface of the femoral head seemed to be irregular, but no apparent re-collapse was noted. I,J Radiographs taken 19 years after osteotomy. On the right side (I), marked osteoarthritic changes were seen (e.g., joint space narrowing, sclerosis of subchondral bone, osteophyte formation). On the left side (J), the joint space was moderately narrowed. Osteoarthritic change was also noted
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extent of necrotic area was too vast5,6,19,20; (2) the depth of the collapse was too great21; (3) vascular obliteration or flow failure occurred because of the stretching or twisting of nutrient arteries of the femoral head (e.g., the posterior column artery and the ligamentum teres6,22,23); (4) subcapital fatigue fracture24; and (5) nonunion of the osteotomy site.6 However, a secondary reason for failure was the development of degenerative changes leading to osteoarthritis.5,6,21 In the present case, we considered the potential explanations for why the femoral head turned osteoarthritic. We speculated, with a leap of logic, that unavoidable mechanical stress
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Fig. 3. Histopathological findings of the resected right femoral head. A Photomicrograph of a section. B Viable bone trabeculae and mature fatty marrow tissue in the previous original necrotic area. C Chondroid metaplasia, which may have been a remnant of subchondral fracture, can be seen (arrow in A). D The pseudocyst (asterisk in A) lined with viable thick bone trabeculae consists of fibrous connective tissue containing sequestrated bone fragments and amorphous debris. E In the current weight-bearing portion, the articular cartilage was focally denuded and revealed marked fibrillation; some cystic lesions were noted in the subchondral area. These findings are compatible with those of secondary osteoarthritis. (H&E; A ×4, B ×100, C ×100, D ×100, E ×33)
was applied to the femoral head while the hip joint was flexed during activities such as walking up and down steps, crouching, squatting, and so on. In particular, in the flexed hip position, the anterior portion of the femoral head, which was the necrotic and rotated area, was transferred into a weight-bearing position; the joint instability due to the incongruity brought about degenerative changes and the femoral head developed osteoarthritis during the course of 19 years. Further study is necessary to understand the repair mechanism and the remodeling processes involved in postsurgical osteotomy cases.
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Conclusion Based on histopathological findings, it is suggested that transtrochanteric anterior/posterior rotational osteotomy can support the remodeling process, particularly fibrous renovation promoting repair of osteonecrotic damage. Acknowledgments. We thank Mr. Hiroshi Fujii for his excellent technical advice. Language assistance was provided by KN International, Inc. (Iowa City, IA, USA).
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