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Two-Stage Cementless Revision Total Hip Arthroplasty for Infected Primary Hip Arthroplasties
The Journal of Arthroplasty xxx (2015) xxx–xxx
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Two-Stage Cementless Revision Total Hip Arthroplasty for Infected Primary Hip Arthroplasties Yalkin Camurcu, MD a, Hakan Sofu, MD b, Abdul Fettah Buyuk, MD c, Sarper Gursu, MD d, Mehmet Akif Kaygusuz d, Vedat Sahin b a
Devrek State Hospital, Zonguldak, Turkey Erzincan University Faculty of Medicine, Erzincan, Turkey Dogubeyazit State Hospital, Agri, Turkey d Baltalimani Bone and Joint Diseases Hospital, Istanbul, Turkey b c
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Article history: Received 7 January 2015 Accepted 30 March 2015 Available online xxxx Keywords: hip arthroplasty infection two-stage revision teicoplanin
a b s t r a c t The main purpose of the present study was to analyze the clinical features, the most common infective agents, and the results of two-stage total hip revision using a teicoplanin-impregnated spacer. Between January 2005 and July 2011, 41 patients were included. At the clinical status analysis, physical examination was performed, Harris hip score was noted, isolated microorganisms were recorded, and the radiographic evaluation was performed. The mean Harris hip score was improved from 38.9 ± 9.6 points to 81.8 ± 5.8 points (P b 0.05). Infection was eradicated in 39 hips. Radiographic evidence of stability was noted in 37 acetabular revision components, and all femoral stems. Two-stage revision of the infected primary hip arthroplasty is a time-consuming but a reliable procedure with high rates of success. © 2015 Elsevier Inc. All rights reserved.
More than 600.000 hip arthroplasty surgeries are carried out worldwide each year and 90% of recipients are over 65 years old [1]. The increasing numbers of hip arthroplasty surgery have been unfortunately accompanied by an unavoidable increasing incidence of complications. Periprosthetic infection following primary total hip arthroplasty (THA) is a serious complication which generally requires revision arthroplasty [2]. The prevalence of infection following hip arthroplasty surgery has been reported as 1%–2% in primary THA and 3%–4% in revision THA [3]. The diagnosis of deep persistent infection, ideal surgical treatment approach, and duration of antibiotic therapy are still controversial in the literature [4]. Different therapeutic strategies including long-term antibiotic suppression, surgical debridement, one-stage revision, twostage revision, Girdlestone resection arthroplasty, arthrodesis, and amputation have been described in the literature as the management of an infected THA [5–13]. Many authors have recommended two-stage revision surgery as the first choice in the management of late onset prosthetic joint infection, and reported success rates above 90% [14–16]. Different agents such as gentamycin, vancomycin, tobramycin or clindamycin have been used in different studies analyzing the clinical results of two-stage revisions. The main purpose of the present study was to analyze the clinical, functional and radiographic outcomes of two-stage revision THA using
No author associated with this paper has disclosed any potential or pertinent conflicts which may be perceived to have impending conflict with this work. For full disclosure statements refer to doi: http://dx.doi.org/10.1016/j.arth.2015.03.040. Reprint requests: Hakan Sofu, Erzincan University Faculty of Medicine Basbaglar mahallesi, 24030, Erzincan, Turkey.
a teicoplanin-impregnated cement-spacer in a series of infected primary total hip arthroplasties. Materials and Methods Between January 2005 and July 2011, 44 consecutive patients who underwent two-stage revision THA with a diagnosis of deep persistent prosthetic joint infection were included in our study. Three patients were excluded from the study because 2 of them died due to chronic medical problems unrelated to the periprosthetic joint infection and its treatment, and the other one was lost to follow-up. Therefore the present study evaluated the clinical and functional outcomes of 41 patients. The indication for THA was primary coxarthrosis in 37 hips (90.2%), femoral neck fracture in 2 hips (4.9%), and avascular necrosis of the femoral head in 2 hips (4.9%). A periprosthetic joint infection was considered as evident according to the criteria defined by the standardized American Academy of Orthopedic Surgeons (AAOS) consensus guidelines for periprosthetic joint infection (Table 1) [17]. Clinical data of our patients were evaluated retrospectively after having approval from the local ethical research committee. The patients included 23 males and 18 females with a mean age of 62 ± 14.1 years (range, 28–87 years). The mean post-operative followup time was 4.5 ± 1.9 years (range, 2–8 years). All cases were unilateral. Twenty-one patients had left hip involvement whereas 20 patients had right hip involvement. The implants removed during the first stage surgery included 16 cemented and 25 cementless designs. Two surgeons performed all surgeries included in the study. A cementless press-fit revision THA composite with metal-on-polyethylene weightbearing surface
http://dx.doi.org/10.1016/j.arth.2015.03.040 0883-5403/© 2015 Elsevier Inc. All rights reserved.
Please cite this article as: Camurcu Y, et al, Two-Stage Cementless Revision Total Hip Arthroplasty for Infected Primary Hip Arthroplasties, J Arthroplasty (2015), http://dx.doi.org/10.1016/j.arth.2015.03.040
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Y. Camurcu et al. / The Journal of Arthroplasty xxx (2015) xxx–xxx
Table 1 The Criteria Defined by the Standardized AAOS Consensus Guidelines for Periprosthetic Joint Infection. Defining Periprosthetic Joint Infection 1. A sinus tract communicating with the prosthesis; or 2.A pathogen isolated by culture from two separate tissue or fluid samples obtained from the affected prosthetic joint; or 3.Four of the following criteria exist: a. Elevated serum erythrocyte sedimentation rate (ESR) or C-reactive protein (CRP) concentration b. Elevated synovial white blood cell (WBC) count c. Elevated synovial neutrophil percentage (PMN%) d. Presence of purulence in the affected joint e. Isolation of a microorganism in one culture periprosthetic tissue or fluid f. Greater than five neutrophils per high-power field in five high-power fields observed from histologic analysis of periprosthetic tissue at 400 times magnification
design and monoblock revision type femoral stem was implanted in all hips as the second stage of the treatment. Surgical Technique All patients were operated in lateral decubitus position and posterolateral approach with elevation of the vastus lateralis was preferred in all hips. In the first stage of revision, any active draining sinus was excised following skin incision, any tendons of short external rotators that could be identified were tagged for latter reattachment, and pseudocapsules with soft tissue scars were excised and kept in a sterile container for histo-pathologic evaluation as well as the laboratory cultivation. Hip was dislocated posteriorly. Additional scar tissues were excised circumferentially from the host-implant interface of both components. Joint fluid, soft tissue and bone tissue specimens were obtained for microbiological culture via extensive surgical debridement. Removal of all implants and cement was performed. Following debridement of all necrotic and infectious tissues, antibiotic-impregnated cement spacer was placed in the articular space. We applied teicoplanin-impregnated polymethylmethacrylate (PMMA) (Cemex Isoplastic, Tecres spa, Italy) cement spacer which was fashioned intra-operatively as hand-mixed for 5 min. Hand-mixing technique was preferred to increase porosity of the cement and improve elution of the antibiotic. All spacers were in the form of a hemi-arthroplasty construct reinforced with inclusion of a Steinmann wire to prevent breakage. The spacer contained an average of 7.2 ± 2.6 g (range, 4–16 g) of teicoplanin for all hips. One gram of intravenous Cefazolin-sodium administration at 8 h intervals was routine prophylactic antibiotherapy until the microbiological culture results were obtained post-operatively. After obtaining the microbiological culture results, intravenous antibiotic therapy was rearranged according to antibiotics sensitivity tests of the isolated microorganism. The antibiotic therapy continued during hospital stay and
after discharge from the hospital, until the serum CRP and ESR levels decreased. Prophylactic low molecular weight heparin (Enoxaparin-sodium) was started 12 h following the operation with 60 mg/day dosage administered subcutaneously, and continued at least four weeks postoperatively for all patients. The patients were discharged with outpatient parenteral antibiotic treatment following the agreed decision of the orthopedic surgeon and infectious diseases specialist, and were requested to follow-up weekly to check serum CRP and ESR levels. Antibiotic treatment was discontinued at the end of an average 8 ± 4 week period (range, 4 to 20 weeks) post-operatively. The reason for prolonged antibiotic treatment in some patients was resistant elevated serum levels of CRP and/or clinical symptoms of infection. We did not perform routine or selected joint aspirations after antibiotics were discontinued. The mean time period past from the first stage to revision surgery was 6 ± 3 months (range, 1–13 months). In the second-stage, cement spacer block was removed and a new debridement was performed first to remove all necrotic tissue during revision surgery. Intra-operative soft and osseous tissue sampling for microbiologic culture was repeated, and cementless revision prosthetic components (Echelon Revision Hip System, Smith and Nephew Orthopedics Inc, Memphis, TN, USA; Solution Revision Hip System, DePuy Orthopedics Inc, Warsaw, IN, USA) were then implanted following the preparation of the acetabular cavity and the femoral canal (Fig. 1). Post-operative antibiotic therapy determined according to the microorganism isolated in the first stage cultures was administered and continued up to 4 weeks according to the consultations with infectious diseases department. Low molecular weight heparin (Enoxaparin-sodium) was also administered and continued as the same protocol applied during the first stage of the treatment. Data Collection Following revision THA, clinical as well as the radiographic evaluation was carried-out at the eighth week, third, sixth and twelfth months, and annually thereafter. At the clinical status analysis, physical examination of the operated hip joint was performed, the patients were observed for any limping, and the Harris hip score was noted. Isolated microorganisms from surgical samples were recorded. Limping status of the patients was assessed by one of the authors at the latest clinical follow-up, and determined according to the ‘Limp’ section of Harris hip score. Clinical cure of the infection, with no clinical signs of inflammation as well as normalized CRP and ESR findings, was assessed by one of the authors at the latest clinical follow-up. We did not perform joint aspiration routinely at the latest follow-up. However, a joint aspiration was performed to exclude a septic loosening of the components for the patients with suspected radiographic signs. Aseptic loosening was determined according to the presence of all the criteria including the absence of any clinical symptoms of infection, normal serum CRP and ESR
Fig. 1. Radiographic images of infected primary total hip arthroplasty pre-operatively (A), following implant removal (B), and after the revision surgery (C).
Please cite this article as: Camurcu Y, et al, Two-Stage Cementless Revision Total Hip Arthroplasty for Infected Primary Hip Arthroplasties, J Arthroplasty (2015), http://dx.doi.org/10.1016/j.arth.2015.03.040
Y. Camurcu et al. / The Journal of Arthroplasty xxx (2015) xxx–xxx
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levels, presence of radiological signs of loosening, and negative aspiration culture. Radiographic data included any femoral or acetabular component migration, and presence of any osteolysis. The stability of the acetabular component was defined according to presence of radiolucent lines exceeding 2 mm in all three zones. Femoral component stability was defined according to Engh et al as fixation by bony ingrowth, stable fibrous ingrowth and unstable implant [18]. Statistical Analysis The Wilcoxon signed rank-sum test was used to compare preoperative and post-operative Harris hip scores. The end points for survival were defined as re-infection or unsuccessful eradication of the infection, and radiographic findings of loosening in either of the components at the latest follow-up. Kaplan–Meier survival analysis was used to construct the cumulative survival rate of implants at four years. P values of b0.05 were considered as significant. Results Fig. 2. Kaplan–Meier survival curve.
Pre-operatively, bacteria in the aspiration fluid were detected in 16 hips, active draining fistula in 12 hips, and purulent synovial fluid without any bacteria detected in 7 hips. Microbiologic cultures of the soft tissue and osseous samples obtained intra-operatively during the first stage surgery remained sterile with no isolated bacterial agent in 13 of 41 hips (31.7%). In this group of patients with no isolated bacteria, the criteria to decide periprosthetic joint infection were either having an active draining fistula communicating with the prosthesis pre-operatively or the presence of abscess formation around the prosthetic components detected intra-operatively. Methicillin-resistant Staphylococcus epidermidis (MRSE) was the most frequent pathogen which was isolated in 12 of 41 hips (29.3%). The other microorganisms isolated from the intraoperative cultures were listed in Table 2. More than one species were detected in 2 hips (4.9%). One of these cases required additional intervention to revise the antibiotic-impregnated cement-spacer, whereas the other one did not require any additional intervention. Infection was eradicated in 39 of 41 hips (95.1%). One of the two patients with failed eradication of the prosthetic joint infection had Girdlestone procedure. Unfortunately, no microorganism could be isolated from the cultures of tissue samples obtained during both stages in this patient. The second patient was determined as having reinfection at the latest follow-up despite three times surgical debridement with revision of the spacer block performed before the second stage. Finally, Girdlestone procedure was also planned for this case but not yet performed while this paper was being prepared. The microorganism was Enterobacter cloacae in this patient, and it was isolated from the tissue samples of both stages. Additional surgical interventions were performed in 6 of 39 hips between the two stages. The indication for additional surgical interventions was active drainage from the wound side accompanied with elevated serum levels of the CRP despite intravenous antibiotic therapy. Revision of the antibiotic-impregnated cement-spacer in 4 hips and repeated surgical irrigations in 2 hips
Table 2 List of Isolated Pathogens at Positive Intra-Operative Cultures. Isolated Pathogens Methicillin-resistant Staphylococcus epidermidis Methicillin-resistant Staphylococcus aureus Methicillin-sensitive Staphylococcus aureus Methicillin-sensitive Staphylococcus epidermidis Enterobacter cloacae Staphylococcus haemolyticus Pseudomonas aeruginosa Serratia marcescens Escherichia coli
Number of Positive Cultures 12 4 4 3 3 1 1 1 1
were the additional surgical interventions carried out after the first stage. Teicoplanin was again the antibiotic of choice in revised spacers. Intraoperative femoral fracture either during implant removal or revision THA was stabilized by using cables in 10 hips (24.3%). These patients did not have any union problem or early stem loosening due to femoral fracture. One patient had a periprosthetic femoral fracture which was successfully treated by performing plate and cable fixation 13 months after revision THA. Union of the fracture was achieved in 4 months without any clinical problem and the prosthetic components were radiologically stable at the latest follow-up. The mean Harris hip score was improved from 38.9 ± 9.6 points (range, 22.8–49 points) pre-operatively to 81.8 ± 5.8 points at the latest follow-up (P b 0.05). At the latest follow-up, severe limpinag was detected in one patient for whom the two-stage revision resulted in Girdlestone procedure due to failed eradication of the infection. Moderate limping was noted in 1 patient who was diagnosed as re-infection, and slight limping in 2 patients with aseptic loosening of the acetabular component. At the latest follow-up, radiolucent lines exceeding 2 mm in all zones around the acetabular component were detected in 3 of 40 hips with revision arthroplasty (1 of 41 hips underwent Girdlestone resection arthroplasty). Radiographic evidence of stability was noted in 37 (92.5%) acetabular revision components that remained in situ after the two-stage revision surgery. All femoral revision components were radiographically stable with the evidence of stability including bony ingrowth detected at the latest follow-up. When we reviewed the 3 radiographically unstable acetabular components; 1 patient was accepted as re-infection, and the other 2 patients had aseptic loosening causing slight limping observed at the latest follow-up but without any significant complaints restricting daily living of the individuals. According to Kaplan–Meier survival analysis, the cumulative four-year survival rate in infected primary THA treated with two-stage revision surgery was 87.9% (95% confidence interval, 75.9% to 96.8%) with re-infection or unsuccessful eradication of the infection, and radiographic findings of loosening in either of the components at the latest follow-up as the end points (Fig. 2). Discussion Surgical treatment of the patients with deep prosthetic joint infection following a primary hip arthroplasty remains a challenge for orthopedic surgeons. Ideal treatment approach providing the most successful clinical results is still controversial [4]. The main objectives of the treatment process are eradication of the infection and restoration of the functions. Removal of the implants with excision of all infected pathologic tissues via thorough surgical debridement is required to cure the
Please cite this article as: Camurcu Y, et al, Two-Stage Cementless Revision Total Hip Arthroplasty for Infected Primary Hip Arthroplasties, J Arthroplasty (2015), http://dx.doi.org/10.1016/j.arth.2015.03.040
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infection. One or two-stage revision arthroplasty is the main treatment option. It has been reported that one-stage cementless revision THA in selected patients who were non-immunocompromised, without previous hip infection, without chronic consumptive disease, without any sign of acute systemic infection, without a discharging sinus, and with an adequate soft tissue and bone stock revealed high rates of success [2,19]. Although studies evaluating one-stage revision arthroplasty with comparable results have been published in the literature, many authors have recommended two-stage revision surgery as the first choice in the management of late onset prosthetic joint infection [14,15,20,21]. According to Kelm et al, the benefit and superiority of two-stage revision are immediate treatment of the source of infection by reaching high antibiotic levels locally [22]. In their study evaluating the clinical results of two-stage uncemented revision total hip arthroplasty in 50 consecutive cases, Haddad et al reported that satisfactory clinical and radiological outcome was obtained in all except 2 patients in a mediumterm follow-up [14]. According to Stockley et al, similar rates of eradication of the infection could be achieved without prolonged antibiotic therapy during two-stage revision [23]. In recent systematic reviews of the literature about infected THAs, similar reinfection rates were detected in both one-stage and two-stage revisions [24,25]. On the other hand, in the last decade the prevalence of infections caused by resistant microorganisms such as Methicillin-resistant Staphylococcus epidermidis (MRSE) and Methicillin-resistant Staphylococcus aureus (MRSA) has become increasingly common [14,26]. Jackson and Schmalzried mentioned that the factors associated with failure in onestage revision surgery included: (1) polymicrobial infection; (2) gramnegative organisms, especially Pseudomonas species; and (3) certain gram-positive organisms such as MRSE and Group D Streptococcus [26]. Leung et al reported a 21% failure rate of eradicating the infection in patients with MRSA and MRSE infection following two-stage revision [27]. VanDiemen et al noted that reinfection occurred in 13% of their patients and Coagulase Negative Staphylococcus (CNS) was isolated in 67% of their cases [28]. In the present study, 22 of 28 hips (78.5%) with a positive microbiologic culture were infected either by gram-positive Methicillin-resistant species or gram-negative microorganisms with high virulence such as Pseudomonas aeruginosa, Enterobacter cloacae, or Escherichia coli. Eradication of the infection was achieved in 39 of 41 hips by performing two-stage revision procedure. Analysis of the relationship between the virulence of isolated microorganisms and resistant infection in 6 patients who underwent additional procedures such as revision of the spacer and repeated surgical irrigations of the wound between the two stages revealed Methicillin-resistant pathogens (MRSE and MRSA) in 5 patients, and Pseudomonas in the other. The findings of the present study also suggest that difficulty in controlling or eradicating the infection was directly related to the virulence of infecting organism. Independently from the surgical technique, improvement in the functional status of the patients undergoing revision surgery for the treatment of deep prosthetic hip joint infection is considered as one of the crucial points of the treatment process. Several scoring systems have been described and can be used as an instrument to assess the clinical outcomes. Harris hip score is one of the most commonly used instruments for the functional status evaluation following hip joint procedures. Different studies demonstrated significant increase in the Harris hip score following twostage revision THA [19,20,29]. Ibrahim et al reported that the Harris hip score was improved from 38 to 81.2 points following two-stage revision [20]. On the other hand, according to the results of their study evaluating two-stage revision of the hip arthroplasties infected by Methicillinresistant species, Leung et al mentioned that the functional scores for their patients were lower than those reported in the literature [27]. In the present study, although 74% of the infecting microorganisms included Methicillin-resistant species or gram-negative agents with high virulence; the mean Harris hip score improved similarly to the previous studies in the literature. At the latest follow-up, various degrees of limping were detected in 4 patients. One of them was due to Girdlestone procedure, the other one was due to re-infection, and 2 were due to aseptic loosening.
Radiographic evaluation of the stability of revision components at the latest follow-up is also considered as another critical criterion in the assessment of success rate following revision THA. Yoo et al reported 83.3% successful results following one-stage revision THA while recurrence of the infection and component loosening were regarded as failure [19]. Haddad et al also reported satisfying clinical and radiological outcomes following cementless revision THA [14]. According to Kaplan–Meier survival analysis, the cumulative survival rate in the present study was 87.9%. Survival rate of the components as well as the success rate in eradication of the infection was consistent with the studies evaluating the results of two-stage revision THA in the literature. Aseptic loosening of the acetabular component was detected in 2 hips. Although slight limping was noted at the latest follow-up in these patients with acetabular component loosening, they were doing well with the situation without any significant disturbance in daily living activities. Another controversial issue regarding the revision process of the infected primary hip arthroplasties is the type and amount of antibiotics that should be mixed into the cement spacers. To date, there have been no prospectively designed, randomized, controlled trials comparing the antibiotic-impregnated cement spacer options with adequate numbers of patients and long-term follow-up to guide the clinical practice. In vivo/in vitro studies demonstrated that teicoplanin-impregnated cement spacers were found to be effective in the treatment of infected joint arthroplasties [30–32]. Teicoplanin covers only the Grampositive microorganisms and this may be considered as a disadvantage when used in antibiotic impregnated cement spacer during the first stage. On the other hand, several studies in the literature revealed that the majority of infected primary THAs undergoing two-stage revision surgery were infected by a Gram-positive microorganism [14,26,28]. One of the main purposes of this study was to test the effectiveness and clinical results of teicoplanin impregnated cement-spacer. Therefore, if another additional antibiotic (such as an aminoglycoside) had been impregnated together with teicoplanin, we could not have been able to assess the effectiveness of it correctly. Because of multifactorial reasons it is hard to prove the amount of antibiotic dose in cement spacers. In a study evaluating preformed antibiotic-loaded cement spacers for two-stage revision arthroplasty, dose dependency was not detected for spacers when low-dose antibiotics were compared with high-dose [33]. It has been demonstrated that at least 3.6 g of antibiotic per 40 g of PMMA is desirable for effective elution kinetics and sustained therapeutic levels of antibiotic for local implantations [34]. Chang et al conclude that 4 g of teicoplanin mixed in 40 g PMMA provided a 40-day antibacterial effect [32]. Minimum dose of teicoplanin mixed in cement spacer was 4 g in the present study. Because in some patients, more than 40 g bone cement was needed to fill-in the defect and obtain appropriate contact between the osseous surfaces and the spacer following removal of the implants, dose of the antibiotic showed substantial variations. In the current study, any adverse effect of teicoplanin usage in intra-operatively fashioned antibiotic-impregnated cement spacer was not observed; however, its main disadvantage is that its spectrum is similar to Vancomycin, covering only the Gram-positive microorganisms. There are some limitations of this study. First, it was a retrospective evaluation of a prospectively followed patient group. Second, the follow-up period is still short to mid-term. On the other hand, despite the relatively small sample size, all cases were infected primary THAs without any re-revision cases, surgical procedure was identical for all hips, antibiotic-impregnated cement spacer was identical in the aspect of type of the antibiotic included, and the implant design was also identical in all hips. We recommend that the durability of these complex reconstructions must continue to be assessed in long-term comparative studies.
Conclusion Two-stage revision of the infected primary hip arthroplasty by using a teicoplanin-impregnated cement spacer at the first stage and
Please cite this article as: Camurcu Y, et al, Two-Stage Cementless Revision Total Hip Arthroplasty for Infected Primary Hip Arthroplasties, J Arthroplasty (2015), http://dx.doi.org/10.1016/j.arth.2015.03.040
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cementless metal-on-polyethylene implant design at the second stage revealed satisfactory clinical and radiological results. References 1. Brown AS. Hip new world. Mech Eng 2006;128:28. 2. Winkler H, Stoiber A, Kaudela K, et al. One stage uncemented revision of infected total hip replacement using cancellous allograft bone impregnated with antibiotics. J Bone Joint Surg (Br) 2008;90(12):1580. 3. Garvin KL, Hanssen AD. Infection after total hip arthroplasty. Past, present, and future. J Bone Joint Surg Am 1995;77:1576. 4. Kuzyk PR, Dhotar HS, Sternheim A, et al. Two-stage revision arthroplasty for management of chronic periprosthetic hip and knee infection: techniques, controversies, and outcomes. J Am Acad Orthop Surg 2014;22(3):153. 5. Callaghan JJ, Katz RP, Johnston RC. One-stage revision surgery of the infected hip: a minimum 10-year follow-up study. Clin Orthop Relat Res 1999;369:139. 6. Buchholz HW, Elson RA, Engelbrecht E, et al. Management of deep infection of total hip replacement. J Bone Joint Surg (Br) 1981;63:342. 7. Haleem AA, Berry DJ, Hanssen AD. Mid-term to long-term followup of two-stage reimplantation for infected total knee arthroplasty. Clin Orthop Relat Res 2004;428:35. 8. Crockarell JR, Hanssen AD, Osmon DR, et al. Treatment of infection with debridement and retention of the components following hip arthroplasty. J Bone Joint Surg Am 1998;80:1306. 9. Goulet JA, Pellicci PM, Brause BD, et al. Prolonged suppression of infection in total hip arthroplasty. J Arthroplasty 1988;3:109. 10. Kantor GS, Osterkamp JA, Dorr LD, et al. Resection arthroplasty following infected total hip replacement arthroplasty. J Arthroplasty 1986;1:83. 11. Kostuik J, Alexander D. Arthrodesis for failed arthroplasty of the hip. Clin Orthop Relat Res 1984;188:173. 12. Masri BA, Panagiotopoulos KP, Greidanus NV, et al. Cementless two-stage exchange arthroplasty for infection after total hip arthroplasty. J Arthroplasty 2007;22:72. 13. Lieberman JR, Callaway GH, Salvati EA, et al. Treatment of the infected total hip arthroplasty with a two-stage reimplantation protocol. Clin Orthop Relat Res 1994; 301:205. 14. Haddad FS, Muirhead-Allwood SK, Manktelow AR, et al. Two-stage uncemented revision hip arthroplasty for infection. J Bone Joint Surg (Br) 2000;82:689. 15. Fink B, Grossmann A, Fuerst M, et al. Two-stage cementless revision of infected hip endoprostheses. Clin Orthop Relat Res 2009;467:1848. 16. Macheras GA, Koutsostathis SD, Kateros K, et al. A two stage re-implantation protocol for the treatment of deep periprosthetic hip infection. Mid to long-term results. Hip Int 2012;22(Suppl. 8):54. 17. Parvizi J, Zmistowski B, Berbari EF, et al. New definition for periprosthetic joint infection: from the Workgroup of the Musculoskeletal Infection Society. Clin Orthop Relat Res 2011;469(11):2992.
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Please cite this article as: Camurcu Y, et al, Two-Stage Cementless Revision Total Hip Arthroplasty for Infected Primary Hip Arthroplasties, J Arthroplasty (2015), http://dx.doi.org/10.1016/j.arth.2015.03.040
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Two-Stage Cementless Revision Total Hip Arthroplasty for Infected Primary Hip Arthroplasties Yalkin Camurcu, MD a, Hakan Sofu, MD b, Abdul Fettah Buyuk, MD c, Sarper Gursu, MD d, Mehmet Akif Kaygusuz d, Vedat Sahin b a
Devrek State Hospital, Zonguldak, Turkey Erzincan University Faculty of Medicine, Erzincan, Turkey Dogubeyazit State Hospital, Agri, Turkey d Baltalimani Bone and Joint Diseases Hospital, Istanbul, Turkey b c
a r t i c l e
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Article history: Received 7 January 2015 Accepted 30 March 2015 Available online xxxx Keywords: hip arthroplasty infection two-stage revision teicoplanin
a b s t r a c t The main purpose of the present study was to analyze the clinical features, the most common infective agents, and the results of two-stage total hip revision using a teicoplanin-impregnated spacer. Between January 2005 and July 2011, 41 patients were included. At the clinical status analysis, physical examination was performed, Harris hip score was noted, isolated microorganisms were recorded, and the radiographic evaluation was performed. The mean Harris hip score was improved from 38.9 ± 9.6 points to 81.8 ± 5.8 points (P b 0.05). Infection was eradicated in 39 hips. Radiographic evidence of stability was noted in 37 acetabular revision components, and all femoral stems. Two-stage revision of the infected primary hip arthroplasty is a time-consuming but a reliable procedure with high rates of success. © 2015 Elsevier Inc. All rights reserved.
More than 600.000 hip arthroplasty surgeries are carried out worldwide each year and 90% of recipients are over 65 years old [1]. The increasing numbers of hip arthroplasty surgery have been unfortunately accompanied by an unavoidable increasing incidence of complications. Periprosthetic infection following primary total hip arthroplasty (THA) is a serious complication which generally requires revision arthroplasty [2]. The prevalence of infection following hip arthroplasty surgery has been reported as 1%–2% in primary THA and 3%–4% in revision THA [3]. The diagnosis of deep persistent infection, ideal surgical treatment approach, and duration of antibiotic therapy are still controversial in the literature [4]. Different therapeutic strategies including long-term antibiotic suppression, surgical debridement, one-stage revision, twostage revision, Girdlestone resection arthroplasty, arthrodesis, and amputation have been described in the literature as the management of an infected THA [5–13]. Many authors have recommended two-stage revision surgery as the first choice in the management of late onset prosthetic joint infection, and reported success rates above 90% [14–16]. Different agents such as gentamycin, vancomycin, tobramycin or clindamycin have been used in different studies analyzing the clinical results of two-stage revisions. The main purpose of the present study was to analyze the clinical, functional and radiographic outcomes of two-stage revision THA using
No author associated with this paper has disclosed any potential or pertinent conflicts which may be perceived to have impending conflict with this work. For full disclosure statements refer to doi: http://dx.doi.org/10.1016/j.arth.2015.03.040. Reprint requests: Hakan Sofu, Erzincan University Faculty of Medicine Basbaglar mahallesi, 24030, Erzincan, Turkey.
a teicoplanin-impregnated cement-spacer in a series of infected primary total hip arthroplasties. Materials and Methods Between January 2005 and July 2011, 44 consecutive patients who underwent two-stage revision THA with a diagnosis of deep persistent prosthetic joint infection were included in our study. Three patients were excluded from the study because 2 of them died due to chronic medical problems unrelated to the periprosthetic joint infection and its treatment, and the other one was lost to follow-up. Therefore the present study evaluated the clinical and functional outcomes of 41 patients. The indication for THA was primary coxarthrosis in 37 hips (90.2%), femoral neck fracture in 2 hips (4.9%), and avascular necrosis of the femoral head in 2 hips (4.9%). A periprosthetic joint infection was considered as evident according to the criteria defined by the standardized American Academy of Orthopedic Surgeons (AAOS) consensus guidelines for periprosthetic joint infection (Table 1) [17]. Clinical data of our patients were evaluated retrospectively after having approval from the local ethical research committee. The patients included 23 males and 18 females with a mean age of 62 ± 14.1 years (range, 28–87 years). The mean post-operative followup time was 4.5 ± 1.9 years (range, 2–8 years). All cases were unilateral. Twenty-one patients had left hip involvement whereas 20 patients had right hip involvement. The implants removed during the first stage surgery included 16 cemented and 25 cementless designs. Two surgeons performed all surgeries included in the study. A cementless press-fit revision THA composite with metal-on-polyethylene weightbearing surface
http://dx.doi.org/10.1016/j.arth.2015.03.040 0883-5403/© 2015 Elsevier Inc. All rights reserved.
Please cite this article as: Camurcu Y, et al, Two-Stage Cementless Revision Total Hip Arthroplasty for Infected Primary Hip Arthroplasties, J Arthroplasty (2015), http://dx.doi.org/10.1016/j.arth.2015.03.040
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Table 1 The Criteria Defined by the Standardized AAOS Consensus Guidelines for Periprosthetic Joint Infection. Defining Periprosthetic Joint Infection 1. A sinus tract communicating with the prosthesis; or 2.A pathogen isolated by culture from two separate tissue or fluid samples obtained from the affected prosthetic joint; or 3.Four of the following criteria exist: a. Elevated serum erythrocyte sedimentation rate (ESR) or C-reactive protein (CRP) concentration b. Elevated synovial white blood cell (WBC) count c. Elevated synovial neutrophil percentage (PMN%) d. Presence of purulence in the affected joint e. Isolation of a microorganism in one culture periprosthetic tissue or fluid f. Greater than five neutrophils per high-power field in five high-power fields observed from histologic analysis of periprosthetic tissue at 400 times magnification
design and monoblock revision type femoral stem was implanted in all hips as the second stage of the treatment. Surgical Technique All patients were operated in lateral decubitus position and posterolateral approach with elevation of the vastus lateralis was preferred in all hips. In the first stage of revision, any active draining sinus was excised following skin incision, any tendons of short external rotators that could be identified were tagged for latter reattachment, and pseudocapsules with soft tissue scars were excised and kept in a sterile container for histo-pathologic evaluation as well as the laboratory cultivation. Hip was dislocated posteriorly. Additional scar tissues were excised circumferentially from the host-implant interface of both components. Joint fluid, soft tissue and bone tissue specimens were obtained for microbiological culture via extensive surgical debridement. Removal of all implants and cement was performed. Following debridement of all necrotic and infectious tissues, antibiotic-impregnated cement spacer was placed in the articular space. We applied teicoplanin-impregnated polymethylmethacrylate (PMMA) (Cemex Isoplastic, Tecres spa, Italy) cement spacer which was fashioned intra-operatively as hand-mixed for 5 min. Hand-mixing technique was preferred to increase porosity of the cement and improve elution of the antibiotic. All spacers were in the form of a hemi-arthroplasty construct reinforced with inclusion of a Steinmann wire to prevent breakage. The spacer contained an average of 7.2 ± 2.6 g (range, 4–16 g) of teicoplanin for all hips. One gram of intravenous Cefazolin-sodium administration at 8 h intervals was routine prophylactic antibiotherapy until the microbiological culture results were obtained post-operatively. After obtaining the microbiological culture results, intravenous antibiotic therapy was rearranged according to antibiotics sensitivity tests of the isolated microorganism. The antibiotic therapy continued during hospital stay and
after discharge from the hospital, until the serum CRP and ESR levels decreased. Prophylactic low molecular weight heparin (Enoxaparin-sodium) was started 12 h following the operation with 60 mg/day dosage administered subcutaneously, and continued at least four weeks postoperatively for all patients. The patients were discharged with outpatient parenteral antibiotic treatment following the agreed decision of the orthopedic surgeon and infectious diseases specialist, and were requested to follow-up weekly to check serum CRP and ESR levels. Antibiotic treatment was discontinued at the end of an average 8 ± 4 week period (range, 4 to 20 weeks) post-operatively. The reason for prolonged antibiotic treatment in some patients was resistant elevated serum levels of CRP and/or clinical symptoms of infection. We did not perform routine or selected joint aspirations after antibiotics were discontinued. The mean time period past from the first stage to revision surgery was 6 ± 3 months (range, 1–13 months). In the second-stage, cement spacer block was removed and a new debridement was performed first to remove all necrotic tissue during revision surgery. Intra-operative soft and osseous tissue sampling for microbiologic culture was repeated, and cementless revision prosthetic components (Echelon Revision Hip System, Smith and Nephew Orthopedics Inc, Memphis, TN, USA; Solution Revision Hip System, DePuy Orthopedics Inc, Warsaw, IN, USA) were then implanted following the preparation of the acetabular cavity and the femoral canal (Fig. 1). Post-operative antibiotic therapy determined according to the microorganism isolated in the first stage cultures was administered and continued up to 4 weeks according to the consultations with infectious diseases department. Low molecular weight heparin (Enoxaparin-sodium) was also administered and continued as the same protocol applied during the first stage of the treatment. Data Collection Following revision THA, clinical as well as the radiographic evaluation was carried-out at the eighth week, third, sixth and twelfth months, and annually thereafter. At the clinical status analysis, physical examination of the operated hip joint was performed, the patients were observed for any limping, and the Harris hip score was noted. Isolated microorganisms from surgical samples were recorded. Limping status of the patients was assessed by one of the authors at the latest clinical follow-up, and determined according to the ‘Limp’ section of Harris hip score. Clinical cure of the infection, with no clinical signs of inflammation as well as normalized CRP and ESR findings, was assessed by one of the authors at the latest clinical follow-up. We did not perform joint aspiration routinely at the latest follow-up. However, a joint aspiration was performed to exclude a septic loosening of the components for the patients with suspected radiographic signs. Aseptic loosening was determined according to the presence of all the criteria including the absence of any clinical symptoms of infection, normal serum CRP and ESR
Fig. 1. Radiographic images of infected primary total hip arthroplasty pre-operatively (A), following implant removal (B), and after the revision surgery (C).
Please cite this article as: Camurcu Y, et al, Two-Stage Cementless Revision Total Hip Arthroplasty for Infected Primary Hip Arthroplasties, J Arthroplasty (2015), http://dx.doi.org/10.1016/j.arth.2015.03.040
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levels, presence of radiological signs of loosening, and negative aspiration culture. Radiographic data included any femoral or acetabular component migration, and presence of any osteolysis. The stability of the acetabular component was defined according to presence of radiolucent lines exceeding 2 mm in all three zones. Femoral component stability was defined according to Engh et al as fixation by bony ingrowth, stable fibrous ingrowth and unstable implant [18]. Statistical Analysis The Wilcoxon signed rank-sum test was used to compare preoperative and post-operative Harris hip scores. The end points for survival were defined as re-infection or unsuccessful eradication of the infection, and radiographic findings of loosening in either of the components at the latest follow-up. Kaplan–Meier survival analysis was used to construct the cumulative survival rate of implants at four years. P values of b0.05 were considered as significant. Results Fig. 2. Kaplan–Meier survival curve.
Pre-operatively, bacteria in the aspiration fluid were detected in 16 hips, active draining fistula in 12 hips, and purulent synovial fluid without any bacteria detected in 7 hips. Microbiologic cultures of the soft tissue and osseous samples obtained intra-operatively during the first stage surgery remained sterile with no isolated bacterial agent in 13 of 41 hips (31.7%). In this group of patients with no isolated bacteria, the criteria to decide periprosthetic joint infection were either having an active draining fistula communicating with the prosthesis pre-operatively or the presence of abscess formation around the prosthetic components detected intra-operatively. Methicillin-resistant Staphylococcus epidermidis (MRSE) was the most frequent pathogen which was isolated in 12 of 41 hips (29.3%). The other microorganisms isolated from the intraoperative cultures were listed in Table 2. More than one species were detected in 2 hips (4.9%). One of these cases required additional intervention to revise the antibiotic-impregnated cement-spacer, whereas the other one did not require any additional intervention. Infection was eradicated in 39 of 41 hips (95.1%). One of the two patients with failed eradication of the prosthetic joint infection had Girdlestone procedure. Unfortunately, no microorganism could be isolated from the cultures of tissue samples obtained during both stages in this patient. The second patient was determined as having reinfection at the latest follow-up despite three times surgical debridement with revision of the spacer block performed before the second stage. Finally, Girdlestone procedure was also planned for this case but not yet performed while this paper was being prepared. The microorganism was Enterobacter cloacae in this patient, and it was isolated from the tissue samples of both stages. Additional surgical interventions were performed in 6 of 39 hips between the two stages. The indication for additional surgical interventions was active drainage from the wound side accompanied with elevated serum levels of the CRP despite intravenous antibiotic therapy. Revision of the antibiotic-impregnated cement-spacer in 4 hips and repeated surgical irrigations in 2 hips
Table 2 List of Isolated Pathogens at Positive Intra-Operative Cultures. Isolated Pathogens Methicillin-resistant Staphylococcus epidermidis Methicillin-resistant Staphylococcus aureus Methicillin-sensitive Staphylococcus aureus Methicillin-sensitive Staphylococcus epidermidis Enterobacter cloacae Staphylococcus haemolyticus Pseudomonas aeruginosa Serratia marcescens Escherichia coli
Number of Positive Cultures 12 4 4 3 3 1 1 1 1
were the additional surgical interventions carried out after the first stage. Teicoplanin was again the antibiotic of choice in revised spacers. Intraoperative femoral fracture either during implant removal or revision THA was stabilized by using cables in 10 hips (24.3%). These patients did not have any union problem or early stem loosening due to femoral fracture. One patient had a periprosthetic femoral fracture which was successfully treated by performing plate and cable fixation 13 months after revision THA. Union of the fracture was achieved in 4 months without any clinical problem and the prosthetic components were radiologically stable at the latest follow-up. The mean Harris hip score was improved from 38.9 ± 9.6 points (range, 22.8–49 points) pre-operatively to 81.8 ± 5.8 points at the latest follow-up (P b 0.05). At the latest follow-up, severe limpinag was detected in one patient for whom the two-stage revision resulted in Girdlestone procedure due to failed eradication of the infection. Moderate limping was noted in 1 patient who was diagnosed as re-infection, and slight limping in 2 patients with aseptic loosening of the acetabular component. At the latest follow-up, radiolucent lines exceeding 2 mm in all zones around the acetabular component were detected in 3 of 40 hips with revision arthroplasty (1 of 41 hips underwent Girdlestone resection arthroplasty). Radiographic evidence of stability was noted in 37 (92.5%) acetabular revision components that remained in situ after the two-stage revision surgery. All femoral revision components were radiographically stable with the evidence of stability including bony ingrowth detected at the latest follow-up. When we reviewed the 3 radiographically unstable acetabular components; 1 patient was accepted as re-infection, and the other 2 patients had aseptic loosening causing slight limping observed at the latest follow-up but without any significant complaints restricting daily living of the individuals. According to Kaplan–Meier survival analysis, the cumulative four-year survival rate in infected primary THA treated with two-stage revision surgery was 87.9% (95% confidence interval, 75.9% to 96.8%) with re-infection or unsuccessful eradication of the infection, and radiographic findings of loosening in either of the components at the latest follow-up as the end points (Fig. 2). Discussion Surgical treatment of the patients with deep prosthetic joint infection following a primary hip arthroplasty remains a challenge for orthopedic surgeons. Ideal treatment approach providing the most successful clinical results is still controversial [4]. The main objectives of the treatment process are eradication of the infection and restoration of the functions. Removal of the implants with excision of all infected pathologic tissues via thorough surgical debridement is required to cure the
Please cite this article as: Camurcu Y, et al, Two-Stage Cementless Revision Total Hip Arthroplasty for Infected Primary Hip Arthroplasties, J Arthroplasty (2015), http://dx.doi.org/10.1016/j.arth.2015.03.040
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infection. One or two-stage revision arthroplasty is the main treatment option. It has been reported that one-stage cementless revision THA in selected patients who were non-immunocompromised, without previous hip infection, without chronic consumptive disease, without any sign of acute systemic infection, without a discharging sinus, and with an adequate soft tissue and bone stock revealed high rates of success [2,19]. Although studies evaluating one-stage revision arthroplasty with comparable results have been published in the literature, many authors have recommended two-stage revision surgery as the first choice in the management of late onset prosthetic joint infection [14,15,20,21]. According to Kelm et al, the benefit and superiority of two-stage revision are immediate treatment of the source of infection by reaching high antibiotic levels locally [22]. In their study evaluating the clinical results of two-stage uncemented revision total hip arthroplasty in 50 consecutive cases, Haddad et al reported that satisfactory clinical and radiological outcome was obtained in all except 2 patients in a mediumterm follow-up [14]. According to Stockley et al, similar rates of eradication of the infection could be achieved without prolonged antibiotic therapy during two-stage revision [23]. In recent systematic reviews of the literature about infected THAs, similar reinfection rates were detected in both one-stage and two-stage revisions [24,25]. On the other hand, in the last decade the prevalence of infections caused by resistant microorganisms such as Methicillin-resistant Staphylococcus epidermidis (MRSE) and Methicillin-resistant Staphylococcus aureus (MRSA) has become increasingly common [14,26]. Jackson and Schmalzried mentioned that the factors associated with failure in onestage revision surgery included: (1) polymicrobial infection; (2) gramnegative organisms, especially Pseudomonas species; and (3) certain gram-positive organisms such as MRSE and Group D Streptococcus [26]. Leung et al reported a 21% failure rate of eradicating the infection in patients with MRSA and MRSE infection following two-stage revision [27]. VanDiemen et al noted that reinfection occurred in 13% of their patients and Coagulase Negative Staphylococcus (CNS) was isolated in 67% of their cases [28]. In the present study, 22 of 28 hips (78.5%) with a positive microbiologic culture were infected either by gram-positive Methicillin-resistant species or gram-negative microorganisms with high virulence such as Pseudomonas aeruginosa, Enterobacter cloacae, or Escherichia coli. Eradication of the infection was achieved in 39 of 41 hips by performing two-stage revision procedure. Analysis of the relationship between the virulence of isolated microorganisms and resistant infection in 6 patients who underwent additional procedures such as revision of the spacer and repeated surgical irrigations of the wound between the two stages revealed Methicillin-resistant pathogens (MRSE and MRSA) in 5 patients, and Pseudomonas in the other. The findings of the present study also suggest that difficulty in controlling or eradicating the infection was directly related to the virulence of infecting organism. Independently from the surgical technique, improvement in the functional status of the patients undergoing revision surgery for the treatment of deep prosthetic hip joint infection is considered as one of the crucial points of the treatment process. Several scoring systems have been described and can be used as an instrument to assess the clinical outcomes. Harris hip score is one of the most commonly used instruments for the functional status evaluation following hip joint procedures. Different studies demonstrated significant increase in the Harris hip score following twostage revision THA [19,20,29]. Ibrahim et al reported that the Harris hip score was improved from 38 to 81.2 points following two-stage revision [20]. On the other hand, according to the results of their study evaluating two-stage revision of the hip arthroplasties infected by Methicillinresistant species, Leung et al mentioned that the functional scores for their patients were lower than those reported in the literature [27]. In the present study, although 74% of the infecting microorganisms included Methicillin-resistant species or gram-negative agents with high virulence; the mean Harris hip score improved similarly to the previous studies in the literature. At the latest follow-up, various degrees of limping were detected in 4 patients. One of them was due to Girdlestone procedure, the other one was due to re-infection, and 2 were due to aseptic loosening.
Radiographic evaluation of the stability of revision components at the latest follow-up is also considered as another critical criterion in the assessment of success rate following revision THA. Yoo et al reported 83.3% successful results following one-stage revision THA while recurrence of the infection and component loosening were regarded as failure [19]. Haddad et al also reported satisfying clinical and radiological outcomes following cementless revision THA [14]. According to Kaplan–Meier survival analysis, the cumulative survival rate in the present study was 87.9%. Survival rate of the components as well as the success rate in eradication of the infection was consistent with the studies evaluating the results of two-stage revision THA in the literature. Aseptic loosening of the acetabular component was detected in 2 hips. Although slight limping was noted at the latest follow-up in these patients with acetabular component loosening, they were doing well with the situation without any significant disturbance in daily living activities. Another controversial issue regarding the revision process of the infected primary hip arthroplasties is the type and amount of antibiotics that should be mixed into the cement spacers. To date, there have been no prospectively designed, randomized, controlled trials comparing the antibiotic-impregnated cement spacer options with adequate numbers of patients and long-term follow-up to guide the clinical practice. In vivo/in vitro studies demonstrated that teicoplanin-impregnated cement spacers were found to be effective in the treatment of infected joint arthroplasties [30–32]. Teicoplanin covers only the Grampositive microorganisms and this may be considered as a disadvantage when used in antibiotic impregnated cement spacer during the first stage. On the other hand, several studies in the literature revealed that the majority of infected primary THAs undergoing two-stage revision surgery were infected by a Gram-positive microorganism [14,26,28]. One of the main purposes of this study was to test the effectiveness and clinical results of teicoplanin impregnated cement-spacer. Therefore, if another additional antibiotic (such as an aminoglycoside) had been impregnated together with teicoplanin, we could not have been able to assess the effectiveness of it correctly. Because of multifactorial reasons it is hard to prove the amount of antibiotic dose in cement spacers. In a study evaluating preformed antibiotic-loaded cement spacers for two-stage revision arthroplasty, dose dependency was not detected for spacers when low-dose antibiotics were compared with high-dose [33]. It has been demonstrated that at least 3.6 g of antibiotic per 40 g of PMMA is desirable for effective elution kinetics and sustained therapeutic levels of antibiotic for local implantations [34]. Chang et al conclude that 4 g of teicoplanin mixed in 40 g PMMA provided a 40-day antibacterial effect [32]. Minimum dose of teicoplanin mixed in cement spacer was 4 g in the present study. Because in some patients, more than 40 g bone cement was needed to fill-in the defect and obtain appropriate contact between the osseous surfaces and the spacer following removal of the implants, dose of the antibiotic showed substantial variations. In the current study, any adverse effect of teicoplanin usage in intra-operatively fashioned antibiotic-impregnated cement spacer was not observed; however, its main disadvantage is that its spectrum is similar to Vancomycin, covering only the Gram-positive microorganisms. There are some limitations of this study. First, it was a retrospective evaluation of a prospectively followed patient group. Second, the follow-up period is still short to mid-term. On the other hand, despite the relatively small sample size, all cases were infected primary THAs without any re-revision cases, surgical procedure was identical for all hips, antibiotic-impregnated cement spacer was identical in the aspect of type of the antibiotic included, and the implant design was also identical in all hips. We recommend that the durability of these complex reconstructions must continue to be assessed in long-term comparative studies.
Conclusion Two-stage revision of the infected primary hip arthroplasty by using a teicoplanin-impregnated cement spacer at the first stage and
Please cite this article as: Camurcu Y, et al, Two-Stage Cementless Revision Total Hip Arthroplasty for Infected Primary Hip Arthroplasties, J Arthroplasty (2015), http://dx.doi.org/10.1016/j.arth.2015.03.040
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Please cite this article as: Camurcu Y, et al, Two-Stage Cementless Revision Total Hip Arthroplasty for Infected Primary Hip Arthroplasties, J Arthroplasty (2015), http://dx.doi.org/10.1016/j.arth.2015.03.040