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FEMORAL HEAD VIABILITY AFTER FREE VASCULARIZED FIBULAR GRAFTING FOR OSTEONECROSIS: SPECT/CT STUDY

CESAR G. FONTECHA, M.D. Ph.D,1 ISABEL ROCA, M.D.,2 IGNASI BARBER, M.D.,3 MARIANO E. MENENDEZ, M.D.,4 DIEGO COLLADO, M.D. Ph.D,5 VASCO V. MASCARENHAS, M.D.,6 SERGIO BARRERA-OCHOA, M.D., Ph.D,7 and FRANCISCO SOLDADO, M.D. Ph.D8*

Purpose: To evaluate femoral head bone viability following free vascularized fibular grafting (FVFG) for osteonecrosis using SPECT/CT imaging. Methods: Ten (9 patients) with osteonecrosis of the femoral head (ONFH) undergoing FVFG were prospectively enrolled. Four cases showed ARCO stage II, while six showed ARCO stage III. The mean age at surgery was 15.7 years (range, 13–22 years). Harris Score (HHS) was measured pre- and post-operative. Bone scintigraphy with SPECT/CT was performed at 2 weeks and 6 months following surgery. Results: Mean follow-up was 4.0 years (range, 2–5.9 years). Mean HHS increased from 37.2 to 92.3. SPECT/ CT findings revealed a progressive increase of femoral head uptake in all cases, suggesting subchondral graft bone viability. No progres- sive deformation of the femoral head was evidenced in radiographic evaluation at final follow-up. Conclusions: This study demonstrates FVFG’s capacity for revitalizing femoral head subchondral bone grafting in patients with ONFH, surgically treated following Urbaniak’s technique. VC 2015 Wiley Periodicals, Inc. Microsurgery 00:000–000, 2015.

Osteonecrosis of the femoral head (ONFH) is a dis- Bone single-photon emission computed tomography abling condition, with an unclear pathophysiology and (SPECT/CT) has recently been described as a valuable challenging treatment.1–3 Among young patients, free imaging modality in the diagnosis of ONFH,12 and could vascularized fibular grafting (FVFG) stands as an effec- also perhaps determine femoral head viability following tive treatment, delaying the need for .4–9 surgery. We therefore sought to assess post-FVFG femo- Vascularized bone grafts have also been obtained from ral head bone viability through use of bone SPECT/CT other sites.10 in 10 adolescent patients with ONFH. As described by Urbaniak et al.7 FVFG surgical tech- nique entails removal of the subchondral necrotic bone of the femoral head, filling the gap with iliac crest bone, PATIENTS AND METHODS and transplantation of the vascularized fibular graft. The In 2006, after implementation of FVFG for the treat- rationale behind this microsurgical technique is to pro- ment of ONFH in our institution, a prospective data vide adequate revascularization to the new subchondral register was designed for its evaluation. Our Institutional bone while maintaining appropriate mechanical support Review Board approved the study. of the femoral head.6,7,11 To our knowledge, however, A total of nine patients with ONFH (10 hips) were there are no imaging studies analyzing the viability of included. Each was treated with FVFG, as described by the grafted bone and its healing potential. Urbaniak et al.,7 and followed for a minimum of 2 years. The indications for surgery were 1) osteonecrosis ARCO (Association Research Circulation Osseous) stages II or 1Pediatric Orthopaedic Unit, Hospital Universitari Vall D’hebron, Barcelona, III, and 2) disabling hip pain severely affecting quality of Spain life. Five males and four females were studied, with a 2Nuclear Medicine Department, Hospital Universitari Vall D’hebron, Barce- lona, Spain mean age of 15.7 years (range, 13–22 years). All patients 3Pediatric Radiology Department, Hospital Universitari Vall D’hebron, Barce- were entered into the study prospectively. Follow-up visits lona, Spain took place at 1 week, 3 weeks, 3 months, 6 months, 9 4Department of Orthopaedic Surgery, Massachusetts General Hospital, Bos- ton, MA months, and 12 months post surgery. After the first year, 5Hip Surgery Unit, Hospital Universitari Vall D’hebron, Barcelona, Spain patients were followed up on a yearly basis. Preoperative 6Radiology Department, UIME, Hospital Da Luz, Lisboa, Portugal and postoperative clinical assessment included the Hip 7Hand Surgery, Hospital Universitari Vall D’hebron, Barcelona, Spain 13 8 Harris Score (HHS). Graft failure was defined as conver- Pediatric Hand Surgery and Microsurgery, Hospital Sant Joan De Deu. Uni- 12 versitat De Barcelona., Spain sion to, or on the waiting list for, total hip replacement. Grant sponsor: Fundac¸ao~ Santa-Maria-Silva. Seven patients (77%) had steroid-induced ONFH, six *Correspondence to: Soldado Francisco, M.D. Ph.D., Hospital Sant Joan de of these as a consequence of immunosuppressive treat- Deu, Passeig Sant Joan de Deu, 2, 08950 Esplugues de Llobregat Barcelona Spain. E-mail: [email protected] ment for hematologic cancer, and one due to lung trans- Received 25 December 2014; Revision accepted 13 May 2015; Accepted plant immunosuppression secondary to cystic fibrosis. 6 July 2015 Published online 00 Month 2015 in Wiley Online Library One patient had ONFH as a consequence of radiotherapy (wileyonlinelibrary.com). DOI: 10.1002/micr.22452 treatment for rhabdomyosarcoma. The last patient

Ó 2015 Wiley Periodicals, Inc. 2 Fontecha et al. sustained a traumatic -dislocation that eventu- ally led to ONFH. Preoperative bone SPECT/CT imaging was acquired 2 hours after intravenous administration of technecium99m- methylene diphosphonate (Tc99m-MDP) (Hawkeye SPECT/CT, GE Healthcare, Boston, MA). Phase III of the bone scan was used, since it represents bone metabolic activity and patency of bone vasculature.14 Additional pre- operative bilateral hip imaging included standard plain radiographs (posteroanterior and axial projections) and magnetic resonance imaging (MRI), with multiplanar T1- and T2-weighted images and evaluation of bone enhance- ment after Gadolinium administration. Postoperative bone SPECT/CT was performed at 2 weeks and 6 months following surgery. A scoring system was developed to evaluate bone graft viability. The fibular Figure 1. Bilateral ONFH graded as ARCO stage III for the right grafts were divided into three regions for the scoring sys- hip and ARCO stage II for the left. The right hip is 6 months post tem: greater , , and femoral head.14 surgical treatment; the left is in the immediate postoperative stage. We compared the fibular graft SPECT/CT signal intensity with the intensity at the ipsilateral proximal femoral dia- uptake to the adjacent femoral bone (score 5 2), while the physis.14 A graft intensity lower than that of the proximal femoral head had an increased uptake (score 5 3) (Fig. 3). femoral diaphyseal cortex was given a score of 1; equal intensity in both was given a score of 2, and a higher intensity in the bone graft was given a score of 3.14 DISCUSSION Statistics were limited to a descriptive analysis. Dif- Bone SPECT/CT has been shown to be a valid imag- ferences between patients related to etiology or predictive ing test for diagnosing ONFH, yet its utility in detecting values were not considered, due to the limited sample femoral head bone viability and monitoring the healing size. process after FVFG remains unknown. In this study, bone SPECT/CT showed increasing femoral head uptake RESULTS in all 10 cases of adolescent ONFH treated with FVFG, Mean follow-up was 4.0 years (range, 2–5.9 years). suggesting subchondral bone viability. No patient was lost to follow-up. The satisfactory long-term clinical and radiographic According to ARCO’s classification for osteonecrosis, outcomes associated with FVFG treatment of ONFH radiographic imaging revealed four cases of ARCO stage stem largely from its potential for bone revitalization II (normal shape of femoral head) and six cases of while still maintaining proper mechanical support of the 6–10 ARCO stage III (alteration of femoral head), all with femoral head. The importance of the revitalizing [mt]50% involvement14,15; none showed hip joint degen- effect has been elucidated by studies comparing non- 16,17 erative changes. Bone scintigraphy and MRI findings vascularized and vascularized fibular grafts. Plaksey- 17 16 were consistent with ONFH in all cases. chuk et al. and Kim et al. have reported that vascu- The average preoperative HHS was 37.2 (range, 28– larized fibular grafting is associated with decreased 42), and the average at final follow-up was 92.3 (range, incidence of radiographic progression and collapse of the 78–100), with excellent outcomes (scores > 90) in all femoral head, when compared with the results of non- hips. All hips showed a noticeable decrease in pain inten- vascularized fibular grafting. sity and a decreased need for pain medication. No pro- Bone scanning has been used to assess and predict gressive deformation of the femoral head was evidenced bone viability in frostbite injuries, burns, and meningo- in radiographic evaluation at final follow-up (Fig. 1). coccal septicemic injuries.18–20 Although the use of bone Early postoperative SPECT/CT at 2-week follow-up scans for diagnosis of ONFH remains controversial,12–23 showed an increased radiotracer uptake in the fibular dia- it has been successfully utilized in assessing bone viabil- physis (score 5 3) along the femoral neck, and a ity after FVFG.24 The femoral head is anatomically diffi- decreased uptake in the cancellous subchondral bone cult to evaluate in detail by planar studies. The addition graft (score 5 1) (Fig. 2). of CT to the SPECT refines this exploration, providing Late postoperative SPECT/CT at 6-month follow-up improved anatomical detail. In our study, bone SPECT/ revealed that the fibular diaphysis had a comparable CT allowed us to determine 1) the viability of the FVFG

Microsurgery DOI 10.1002/micr Revascularization of Femoral Head With FVFG in Osteonecrosis 3

Figure 2. SPECT/CT of the right hip shown in Figure 1, performed 2 weeks post surgical treatment. Maximum radiotracer uptake is local- ized in the fibular diaphysis (score 5 3) along the femoral neck.

(microanastomosis patency), and 2) the viability of the results showed that the subchondral bone graft had a subchondral femoral head bone graft. lower activity early post-surgery than in later SPECT/CT Scintigraphy directly determines osteocyte viability, scans, suggesting bone graft viability induced by the vas- and indirectly determines vascular supply.24 For Tc99m- cularized fibular graft. The present study’s results support MDP uptake to occur, the presence of both adequate per- Urbaniak’s hypothesis concerning the relevance of vascu- fusion and metabolically active osteocytes is required. lar supply for subchondral bone graft viability. Digital Scintigraphy has been used previously in assessing FVFG subtraction angiography has been used for preoperative bone viability in mandibular reconstruction, and is consid- assessment of femoral head vascularity in ONFH.27 This ered a valid tool for assessing patency of microanastomo- technique might also be used to assess postoperative ses.25,26 Similarly, in our study, scintigraphy combined bone viability, and, combined with SPECT/CT, might with SPECT/CT showed all FVFGs to be viable. allow better-substantiated conclusions to be drawn. To our knowledge, no studies to date have evaluated Our results regarding clinical improvement of the treated subchondral bone graft activity using scintigraphy. Our patients are similar to those in multiple previous reports.

Microsurgery DOI 10.1002/micr 4 Fontecha et al.

Figure 3. SPECT/CT of the right hip shown in Figure 1, performed 6 months post surgical treatment. Maximum radiotracer uptake is local- ized in cancellous subchondral bone graft (score 5 3) within the femoral head.

This study’s limitations include the small number of CONCLUSIONS cases treated, and the heterogeneity of their ONFH etiol- This study demonstrates the efficacy of FVFG for ogies; a larger-cohort study is required. Another limita- revitalization of femoral head subchondral bone grafting tion is the study’s relatively brief follow-up period. in patients with ONFH, surgically treated following Urbaniak et al.7 showed 11% conversion to total hip Urbaniak’s technique. arthroplasty within 5 years after FVFG in an adult sam- ple, while Dean et al.4 reported a 16% conversion rate in adolescents. In our study, no hip progressed to collapse or required further surgical treatment. Long-term out- REFERENCES come analysis is necessary to adequately study post- 1. Lieberman JR, Berry DJ, Mont MA, Aaron RK, Callaghan JJ, FVFG changes of the femoral head, and their clinical Rajadhyaksha AD, Urbaniak JR. Osteonecrosis of the hip: Manage- and imaging outcomes. ment in the 21st century. Instr Course Lect 2003;52:337–355.

Microsurgery DOI 10.1002/micr Revascularization of Femoral Head With FVFG in Osteonecrosis 5

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Microsurgery DOI 10.1002/micr