|Year : 2021 | Volume
| Issue : 1 | Page : 19-25
Risk factors for focal osteolysis in a stainless-steel limb-lengthening device
Oliver Charles Sax, Janet D Conway, Shawn C Standard, Michael Assayag, John E Herzenberg, Philip Kraus McClure
International Center for Limb Lengthening, Rubin Institute for Advanced Orthopedics, Sinai Hospital of Baltimore, Baltimore, Maryland, USA
|Date of Submission||03-May-2021|
|Date of Acceptance||06-Jul-2021|
|Date of Web Publication||30-Jun-2021|
Dr. Philip Kraus McClure
International Center for Limb Lengthening, Rubin Institute for Advanced Orthopedics, Sinai Hospital of Baltimore, 2401 West Belvedere Avenue, Baltimore, Maryland 21215
Source of Support: None, Conflict of Interest: None
Background: Magnetic, telescoping intramedullary lengthening devices are widely used for treatment of limb length discrepancies. However, a routine radiographic review of a stainless-steel device demonstrated soft tissue and bony changes suggestive of osteolysis. Therefore, we sought to examine all patients implanted with a stainless-steel limb-lengthening nail. We specifically asked: (1) what is the incidence of periosteal reaction osteolysis? (2) Is a new biologic reaction classification system valid and reliable? and (3) Are there predictive factors for the development of osteolysis? We hypothesized that higher patient weight and femoral insertion would be risk factors for lysis, due to increased bending moments on the implants. Materials and Methods: A retrospective review of all patients implanted with a stainless-steel limb-lengthening nail between December 2018 and December 2020 was conducted at a single institution. A total of 57 nails in 44 patients were radiographically examined with an average follow-up of 6.2 months (range: 1–21 months). The incidence of osteolysis was calculated through review of patient radiographs. These were then classified according to a novel system by five fellowship-trained orthopedic surgeons with agreement assessed using an intraclass correlation coefficient (ICC). Logistic regression measured predictive factors for this phenomenon. A separate histologic analysis of two bone/soft-tissue biopsies at the time of routine explantation was conducted by an independent pathologist. Results: The incidence of periosteal reaction and osteolysis was 36.8% and 17.5%, respectively. Nails with progression to osteolysis increased to 34.6% (9/26) when examining nails with at least a 6-month follow-up. ICC testing yielded good inter-rater agreement for the novel classification system (average measure: 0.860, 95% confidence interval 0.828–0.888). Age >16 years (P = 0.024) and body weight >150 pounds (P = 0.038) were predictors of osteolysis. Histologic analysis of the biopsies demonstrated an abundance of particulate debris suggestive of chromium reaction. Conclusions: The modular junction of a stainless-steel lengthening device is susceptible to osteolytic changes, and this appears to be associated with increased age and weight. This phenomenon has an apparent time dependence: osteolysis increases with greater follow-up.
Keywords: Distraction osteogenesis, intramedullary lengthening, Osteolysis, limb lengthening
|How to cite this article:|
Sax OC, Conway JD, Standard SC, Assayag M, Herzenberg JE, McClure PK. Risk factors for focal osteolysis in a stainless-steel limb-lengthening device. J Limb Lengthen Reconstr 2021;7:19-25
|How to cite this URL:|
Sax OC, Conway JD, Standard SC, Assayag M, Herzenberg JE, McClure PK. Risk factors for focal osteolysis in a stainless-steel limb-lengthening device. J Limb Lengthen Reconstr [serial online] 2021 [cited 2021 Dec 8];7:19-25. Available from: https://www.jlimblengthrecon.org/text.asp?2021/7/1/19/320029
| Introduction|| |
Distraction osteogenesis is widely employed for patients who require limb lengthening and deformity correction (LLDC). Ilizarov's innovations and circular fixator opened a new world of possibilities., Advancements in intramedullary lengthening rods have greatly mitigated complications such as pin tract and skin infections, pain, and joint stiffness.,,, Mechanical intramedullary lengthening nails (MILNs) have become the preferred treatment device.,,,,,, These rods lengthen for several months by external remote-controlled distraction at a modular junction between male and female parts at a rate and rhythm dictated by the operating surgeon. Although implanted as a single unit, the junction of the male and female components can be compared to many tribology couplings found in orthopedic devices, notably the conventional metal on polyethylene or metal on metal-bearing surface in total hip arthroplasty (THA) given the potential for particulate debris from the interaction of surfaces with relative motion.,, Whereas osteolysis is an understood mechanism of failure in THA, this process has not been investigated in limb lengthening using MILN.
While only recently reported in lengthening devices, a comparable surface of relative motion has been widely reported in the past. In a retrospective review of modular stainless-steel femoral intramedullary nails, Jones et al. found that osteolysis occurred in 19 out of 23 modular junctions in a stainless-steel trauma nail. They also found a periosteal reaction in 13 modular junctions. Based on their findings, the authors abandoned the use of this device, as numerous viable alternatives (non-modular designs) existed. A small case series found metallosis and pseudocapsule formation in explanted growing titanium rods to correct scoliosis, but associated metabolic response in the bone was not seen.
We observed patients with incidental osteolysis at the modular junction between the male and female parts of a stainless-steel MILN (Stryde, Nuvasive, Inc., San Diego, California). Subsequently, a formal review of all patients who received this rod in our institution identified additional patients with osteolysis and periosteal inflammation. The purpose of this study was to examine osteolysis in all patients who received a femoral or tibial stainless-steel MILN for LLDC. We specifically asked: (1) what is the incidence of osteolysis? (2) Is a new osteolysis classification system valid and reliable? and (3) Are there predictive factors for the development of osteolysis? We hypothesized that higher patient weight and femoral insertion would be risk factors for lysis, due to increased bending moments on the implants.
| Materials and Methods|| |
A retrospective database review was conducted to identify all consecutive patients who underwent a limb-lengthening procedure with a stainless-steel intramedullary nail (Precice Stryde Nail, Nuvasive, Inc., San Diego, California) at a single institution between December 2018 and December 2020. Local Institutional Review Board exemption status was approved for this retrospective review of confidential patient medical records and in accordance with the International Council for Harmonization Guidelines for Good Clinical Practice.
The Stryde nail system was FDA cleared in 2018 and is comprised of a magnetic, telescoping high chromium, low nickel stainless-steel alloy (Biodur 108, Pioneer Surgical Technology, Inc., Marquette, MI), nail with solid (male) and cylindrical (female) ends joining at a telescoping junction. A gasket ring enveloping the telescoping junction is a composite of ethylene-propylene-diene-monomer rubber coated with silicone. The system is activated to distract or compress by an external remote controller. An internal magnet in the rod is induced to rotate by an oscillating external magnetic field, creating distraction through a series of planetary step-down gears linked to a threaded lead screw distraction rod.
A total of 57 consecutive nails were implanted in 44 patients during the study. Inclusion criteria consisted of (1) lower limb-lengthening surgery using the Stryde intramedullary limb-lengthening system, (2) follow-up clinical notes available, and (3) follow-up radiographs available. Demographics and baseline characteristics were captured and included age at the time of surgery, sex, etiology, laterality, and lengthening site. Nail characteristics were captured and included femoral or tibial nail insertion site, nail length/diameter, final intraoperative reamer size, target length, and final reamer size. The outcomes measured were follow-up in clinical office (months), lengthening latency (days between surgery and start of lengthening), lengthening time (days of lengthening after surgery), rate of lengthening (mm/day), distraction index (DI; the length achieved in mm divided by lengthening duration in days), and consolidation index (CI; the number of days from surgery until consolidation healing divided by the length of the regenerate in centimeter). Consolidation was defined as at least three healed cortices determined by standing anterior-posterior and lateral films. Postoperative complications were reviewed and included implant failures, hip/knee contractures, deep vein thromboses (DVTs), neurologic symptoms, osteomyelitis, and osteolysis. Implant failure was defined as a catastrophic failure, crack, or bending of the nail and/or locking nails requiring revision of components. Neurologic symptoms were defined as pain, numbness, or tingling secondary to neurologic etiology. Osteolysis was defined as radiographic loss of cortical density in the postoperative period.
Biologic reaction classification system
We developed a novel classification system for biologic reaction in MILN [Table 1] and [Figure 1]: Class I was defined as periosteal reaction without osteolysis at (a) male-sided locking screw, (b) modular junction, or (c) both; Class II was defined as osteolysis around modular junction without cortical penetration; Class III was defined as osteolysis around modular junction with cortical penetration [Figure 2]. This classification was based on radiographic review of all available radiographs of patients following implantation. At our institution, radiographs were routinely ordered and reviewed according to healing phase: every 2 weeks during lengthening; every month during consolidation; and every 3 months thereafter. Nails are routinely removed at 1 year, provided full healing of all cortices in the regenerate bone. Two patients in the study had perimodular junction biopsies taken during routine nail explantation. Before biopsy, all patients were notified that a change was present in the bone that required evaluation. Radiographic patients were discussed with the patients at the time of identification.
|Table 1: Biologic reaction classification for magnetic intramedullary limb lengthening nails|
Click here to view
|Figure 1: Artist's rendition of the novel biologic reaction classification for magnetic intramedullary limb lengthening nails|
Click here to view
|Figure 2: Radiograph (135% magnification) of left femur 5 months following lengthening nail implantation demonstrating osteolysis at the male-female modular junction with associated lateral cortical penetration (black arrows). Sinus tract with proximal migration can also be appreciated (white arrowheads). Classified as grade III osteolysis|
Click here to view
Biopsies were sent for a formal histologic review by an independent pathologist. The biopsies were processed using routine histology procedures including formalin fixation, xylene-based tissue processing, embedding in paraffin wax, and staining with hematoxylin and eosin.
Demographics and nail characteristics
The average age of patients with the studied implanted lengthening nail was 24 years old (range: 9–62 years) [Table 2]. The majority were male (73.7%), required lengthening due to a congenital etiology (84%), and had the right (65%) femur (67%) corrected. A majority of patients with femur and tibia lengthening underwent a greater trochanter (79%) and suprapatellar (53%) approach, respectively [Table 3]. The mean target length was 4.4 centimeters (cm) (range: 1–8.5 cm), median nail length was 305 mm (mm) (range: 235–365 mm), median nail diameter was 11.5 mm (range: 10–13 mm), and mean final reamer size was 12.5 cm (range: 10–15 cm).
We performed an intraclass correlation coefficient (ICC) using absolute agreement to measure interrater agreement for the proposed osteolysis/periosteal hypertrophy classification system. In addition, we performed a multivariate binomial logistic regression analysis to examine predictive factors for the development of osteolysis. Factors examined included age >16 years old at time of implantation, male gender, weight >150 pounds at the time of implantation, femoral implantation site, postoperative time to full weight bearing >75 days, postoperative thigh/leg pain at least 3 months after surgery, and implant failure. All factors were identified from electronic medical records and clinical documentation. All analysis was performed through SPSS (version 24, Chicago, Illinois, USA) with significance defined as P < 0.05.
| Results|| |
Periosteal reactions and osteolysis
Periosteal reactions at the modular junction and/or distal locking screws developed in 21/57 (36.8%) nails. The incidence of osteolysis with nails having at least a 3-month follow-up was 10/57 (17.5%) nails [Table 4]. The incidence of osteolysis with nails having at least 6-month follow-up was 9/26 (34.6%) nails. The interrater agreement as calculated by an ICC was very good with an average measure of 0.860% and a 95% confidence interval between 0.828 and 0.888) [Table 5]. Multiple risk factors were assessed to predict the development of osteolysis. Age >16 years old (P = 0.024) and weight >150 pounds (P = 0.038) were statistically significant predictors of osteolysis. Other measured factors included male sex (P = 0.715), femoral nail implantation P = 0.738), time to full weight bearing >75 days (P = 0.085), postoperative thigh/leg pain after 3 months from surgery (P = 0.919), and implant failure (P = 0.328) [Table 6].
|Table 5: Intraclass correlation coefficient of osteolysis classification for magnetic intramedullary limb lengthening nails|
Click here to view
|Table 6: Multivariate regression model evaluation risk factors for osteolysis after stainless steel lengthening nail implantation|
Click here to view
Other outcome and complications
The mean follow-up from surgery in the clinical office was 6.2 months (range: 1–21 months). The mean lengthening latency was 8.0 days (range: 4–19 days), median lengthening time was 68 days (range: 15–297 days), and mean rate of initial lengthening was 0.98 mm/day (range: 0.6–1.25 mm/day). The mean DI was 0.61 mm/day (range: 0.09–0.94 mm/day) and the mean CI was 31.6 days/cm (range: 10.9–59.3 days/cm). Postoperative complications consisted of hip/knee contractures (10.5%), DVTs (3.5%), and neurologic symptoms (3.5%). Implant failures occurred in 4/57 (7.0%) nails at either the proximal portion of the nail or at the distal locking screws. Of the four implant failures, three cases developed distal locking screw failures (two in one patient). Since both patients with distal locking screw failures developed slight collapse of the regenerate, revision of the intramedullary nail to compress the regenerate and induce healing was performed. Another patient developed rod-related implant failure through nontraumatic means. Exchange nailing with a static nail and implantation of new distal locking screws were then administered. No postoperative complications were reported following these treatments. Osteomyelitis developed in 2/57 nails (3.5%), both occurring in the same patient (simultaneous ipsilateral femur and tibia) and subsequently resolved with irrigation/debridement and static nail exchange. This patient did not present with radiographic signs of osteolysis, however.
Two patients in this study, who were found to have radiographic evidence of osteolysis underwent a soft tissue and bone biopsy at a site adjacent to the modular junction during routine nail removal. Microscopic sections showed an abundance of particulate debris including fine brown-to-black particles taken up by macrophages, as well as large crystalline fragments with a green-yellow color. These larger fragments are similar to those previously described, which were found to contain chromium, consistent with stainless-steel components. In one patient, there was also abundant clear, refractile, and nonbirefringent material consistent with silicone debris. Postoperative evaluation of the corresponding patient's explanted nail demonstrated significant corrosion at the modular junction. Silicone debris was not seen in the second patient's biopsies.
| Discussion|| |
The modular component design of MILN shares many similarities to the design of many orthopedic implants. However, peri-implant osteolysis and soft-tissue adverse reactions are poorly understood in patients requiring limb-lengthening procedures. We sought to examine the rate of osteolysis and periosteal tissue reaction in patients receiving a stainless-steel MILN. The incidence of osteolysis and/or periosteal reaction was found to be present in a significant proportion of patients after nail implantation and was even higher among those with greater follow-up. Age >16 and weight >150 pounds were associated with the development of osteolysis. This leads us to believe that the fretting of the implant components at the male–female junction creates wear debris that induces an inflammatory reaction, leading to focal bone resorption. A novel osteolysis/periosteal reaction classification system was also introduced and was demonstrated to have very good inter-rater agreement.
This study has limitations. The patient diagnoses and postoperative complications identified through ICD 10 codes and pulled from surgeon operative and clinical office notes are subject to errors of classification. However, incorrect coding rates among Medicare and Medicaid payers have been estimated to be <1.0%, and similar rates likely exist among private payers. Further, the primary outcome (osteolysis) was identified and classified with agreement among five fellowship-trained orthopedic surgeons, despite varying surgical volumes. We assessed stainless-steel rod implantations in a small sample size which may not allow for adequate power to analyze differences reported. However, given the scant literature regarding osteolysis in MILN, this is the largest examination of osteolysis and periosteal soft-tissue reaction in limb-lengthening patients. This study advances the current knowledge on nails utilized in limb-lengthening procedures and will provide foundation for future utility of certain limb-lengthening rods.
The classic example of osteolysis is reported in arthroplasty literature secondary to the micromotion between two surfaces, especially in metal-on-metal hips.,,,,, The natural progression to pelvic osteolysis after THA has been reported to average 1.3 years. In a recent study, Rölfing et al. identified thirty bone segments in 27 patients who developed adverse bone reactions including osteolysis (19/30) and periosteal reaction (12/30). Unlike our findings, pain was found to be prominent among those who developed these bony changes. The time of onset for radiographic changes ranged from 15 to 48 days. Interestingly, our study shows that patients who developed osteolysis showed radiographic evidence of bony changes at 3 months with a median onset of 202 days (range: 123–663 days) [Table 4]. Despite the development of osteolysis in arthroplasty, it is important to consider the intra-articular nature of the bearing surface in arthroplasty. This may limit direct comparison to our study patients. In the only other report of osteolysis in a stainless-steel intramedullary nail, Jones et al. evaluated a modular trauma nail and found periosteal reaction at an average of 9 months, osteolysis at 13 months, and cortical thickening at 14 months. The relatively earlier findings of osteolysis in our patients may be due to the possibility of an accelerated and more severe reaction. This may be accounted for by several differences. The lengthening junction in telescopic nails has more motion than a press-fit modular taper, which increases the stress on implant surfaces. In addition, distraction of the osteotomy increases the stress on the implant relative to fracture fixation. The bending moment present during ambulation may lead to severe edge loading at the tip of the female component, accelerating wear at that level. An additional factor requiring study is the increased chromium content of the alloy used in the stainless-steel lengthening nail relative to the modular trauma nail. Biodur alloy is high in manganese and chromium, with lower nickel. As chromium particles have been implicated in osteolysis previously, this is concerning. Our biopsy findings are indicative of the same particles. As we did not quantify the degree of particles present, we cannot comment on particulate concentrations. While manganese has not previously been implicated in osteolysis, the particles identified are similar to chromium particles in previous research.
Third body wear is a known risk factor for accelerated particle formation, leading to more rapid degradation of implants. The presence of silicone debris on one but not both biopsy specimens indicates that it is unlikely to be the source of the osteolysis. Based on histological characteristics, the silicone identified was likely in amorphous state and not crystalline, further decreasing the likelihood of its contribution to the osteolysis.
Within the hip arthroplasty literature, multiple studies suggest an association between wear rates and osteolysis;,, however, to our knowledge, associations between increased age/weight and osteolysis progression have not been reported. Given the inherent differences of the intra-articular motion in arthroplasty versus movement at a modular junction in lengthening nail, wear rates cannot and have not been described in the latter operation. Increased mechanical loading is known to stimulate bone formation at the molecular level and has utility in fracture repair. However, an increased load in the setting of a lengthening nail may accentuate edge loading, as mentioned above, and may contribute to progression of wear.
We also introduce a novel classification system for osteolysis in limb lengthening nails with very good inter-rater agreement (ICC testing of 0.860). This system is practical and is may be clinically relevant for other groups who may be studying this phenomenon of limb-lengthening nails. This is the first proposed classification system to identify osteolysis/periosteal reaction in limb-lengthening patients and has the potential to be a catalyst for future study as patient follow-up increases. Within the proposed system, Grade 1 may be explained by a rapid transition in segmental stiffness, which is a known risk factor for a stress response within the bone. Periosteal reaction and subsequent lysis at the male–female junction are more difficult to justify as a purely biomechanical response, and this is supported by the presence of particles known to induce osteolysis at the level of the junction during biopsy. While increased patient age and weight were shown to be a factor in osteolysis, the hypothesis of femoral implantation as a risk factor was not supported in our statistical results.
A significant portion of patients with implanted stainless-steel intramedullary nails was found to develop osteolysis after 3 months from operation. This number significantly increased when assessing patients with at least 6-month of follow-up, indicating a time-dependent factor in the development of osteolysis. Associated factors found to be predictive of this phenomenon included increased age and weight, indicating some role for biomechanics in the process. The proposed classification system had very good inter-rater agreement with the potential to be highly impactful in the clinical setting. Changes should be monitored every 2–3 months, and we recommend removal if there is progression of osteolysis or if the osteolysis has reached Grade 3. We do not recommend taking intraoperative biopsies for either patients who have not yet reached the organic stage of implant removal or patient who is already at this stage for reasons of avoiding the small possibility of tissue morbidity associated with biopsy collection. Given that standard of care is to remove intramedullary lengthening nails at 1 year, future studies should focus on patient follow-up postexplantation.
| Conclusion|| |
In Conclusion, we recommend caution with weightbearing stainless steel intramedullary limb lengthening devices, as our experience mirrors that of others with a high prevalence of osteolysis and periosteal reaction. We recommend careful monitoring of patients, and consideration for early removal when changes are progressive. Consideration for exchange to static nails should be considered when defects are large, perforate the cortex, or when inadequate regenerate healing is present.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Ilizarov GA. The tension-stress effect on the genesis and growth of tissues. Part I. The influence of stability of fixation and soft-tissue preservation. Clin Orthop Relat Res 1989;238:249-81.
Ilizarov GA. The tension-stress effect on the genesis and growth of tissues: Part II. The influence of the rate and frequency of distraction. Clin Orthop Relat Res 1989;239:263-85.
Rozbruch SR, Kleinman D, Fragomen AT, Ilizarov S. Limb lengthening and then insertion of an intramedullary nail: A case-matched comparison. Clin Orthop Relat Res 2008;466:2923-32.
Paley D. Problems, obstacles, and complications of limb lengthening by the Ilizarov technique. Clin Orthop Relat Res 1990;250:81-104.
Baumgart R, Betz A, Schweiberer L. A fully implantable motorized intramedullary nail for limb lengthening and bone transport. Clin Orthop Relat Res 1997;343:135-43.
Baumgart R, Zeiler C, Kettler M, Weiss S, Schweiberer L. Fully implantable intramedullary distraction nail in shortening deformity and bone defects. Spectrum of indications. Orthopade 1999;28:1058-65.
Makarewich CA, Herzenberg JE, McClure PK. Latest advances in limb lengthening using magnetically controlled intramedullary lengthening nails. Surg Technol Int 2020;36:404-11.
Szymczuk VL, Hammouda AI, Gesheff MG, Standard SC, Herzenberg JE. Lengthening With monolateral external fixation versus magnetically motorized intramedullary nail in congenital femoral deficiency. J Pediatr Orthop 2019;39:458-65.
Olesen UK, Nygaard T, Prince DE, Gardner MP, Singh UM, McNally MA, et al.
Plate-assisted bone segment transport with motorized lengthening nails and locking plates: A technique to treat femoral and tibial bone defects. J Am Acad Orthop Surg Glob Res Rev 2019;3:e064.
Hammouda AI, Jauregui JJ, Gesheff MG, Standard SC, Conway JD, Herzenberg JE. Treatment of post-traumatic femoral discrepancy with PRECICE magnetic-powered intramedullary lengthening nails. J Orthop Trauma 2017;31:369-74.
Landge V, Shabtai L, Gesheff M, Specht SC, Herzenberg JE. Patient satisfaction after limb lengthening with internal and external devices. J Surg Orthop Adv 2015;24:174-9.
Shabtai L, Specht SC, Standard SC, Herzenberg JE. Internal lengthening device for congenital femoral deficiency and fibular hemimelia. Clin Orthop Relat Res 2014;472:3860-8.
Rozbruch SR, Birch JG, Dahl MT, Herzenberg JE. Motorized intramedullary nail for management of limb-length discrepancy and deformity. J Am Acad Orthop Surg 2014;22:403-9.
Gittings DJ, Dattilo JR, Hardaker W, Sheth NP. Evaluation and treatment of femoral osteolysis following total hip arthroplasty. JBJS Rev 2017;5:e9.
Hu CY, Yoon TR. Recent updates for biomaterials used in total hip arthroplasty. Biomater Res 2018;22:33.
Sheth NP, Rozell JC, Paprosky WG. Evaluation and treatment of patients with acetabular osteolysis after total hip arthroplasty. J Am Acad Orthop Surg 2019;27:e258-67.
Rölfing JD, Kold S, Nygaard T, Mikuzis M, Brix M, Faergemann C, et al.
Pain, osteolysis, and periosteal reaction are associated with the STRYDE limb lengthening nail: a nationwide cross-sectional study. Acta Orthop. 2021:1-6. doi: 10.1080/17453674.2021.1903278. Epub ahead of print. PMID: 33757381.
Jones DM, Marsh JL, Nepola JV, Jacobs JJ, Skipor AK, Urban RM, et al.
Focal osteolysis at the junctions of a modular stainless-steel femoral intramedullary nail. J Bone Joint Surg Am 2001;83:537-48.
Teoh KH, Von Ruhland C, Evans SL, James SH, Jones A, Howes J, et al
. Metallosis following implantation of magnetically controlled growing rods in the treatment of scoliosis a case series. Bone Joint J 2016;98:1662-7.
Doorn PF, Campbell PA, Amstutz HC. Metal versus polyethylene wear particles in total hip replacements. A review. Clin Orthop Relat Res. 1996 Aug;(329 Suppl):S206-16. doi: 10.1097/00003086-199608001-00018. PMID: 8769335.
Kadoya Y, Revell PA, Kobayashi A, al-Saffar N, Scott G, Freeman MA. Wear particulate species and bone loss in failed total joint arthroplasties. Clin Orthop Relat Res. 1997:118-29. doi: 10.1097/00003086-199707000-00016. PMID: 922424.
Howie DW. Tissue response in relation to type of wear particles around failed hip arthroplasties. J Arthroplasty 1990;5:337-48.
Kitamura N, Sychterz-Terefenko CJ, Engh CA Sr. The temporal progression of pelvic osteolysis after uncemented total hip arthroplasty. J Arthroplasty 2006;21:791-5.
Dowd JE, Sychterz CJ, Young AM, Engh CA. Characterization of long-term femoral-head-penetration rates. Association with and prediction of osteolysis. J Bone Joint Surg Am 2000;82:1102-7.
Orishimo KF, Claus AM, Sychterz CJ, Engh CA. Relationship between polyethylene wear and osteolysis in hips with a second-generation porous-coated cementless cup after seven years of follow-up. J Bone Joint Surg Am 2003;85:1095-9.
Kadoya Y, Kobayashi A, Ohashi H. Wear and osteolysis in total joint replacements. Acta Orthop Scand Suppl 1998;278:1-16.
Klein-Nulend J, Bacabac RG, Bakker AD. Mechanical loading and how it affects bone cells: The role of the osteocyte cytoskeleton in maintaining our skeleton. Eur Cell Mater 2012;24:278-91.
[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]