Abstract
Purpose
Young and physically active patients have mainly received metal-on-metal (MoM) total hip arthroplasty (THA) and resurfacing hip arthroplasty (RHA). However, the correlation between daily physical activity (PA) levels, serum-ion concentrations of chromium and cobalt and pseudotumours formation of patients who underwent MoM THA/RHA is insufficiently explored.
Methods
Ninety-nine patients with 134 hip articulations, 71 MoM THA/RHA and 63 MoP THA participated in a cross-sectional study at XXX University Hospital, Denmark, at mean 7.3 (range: 0.4–21.7) years after surgery. Patients' daily PA was monitored during a two-week period using a triaxial accelerometer. Metal artefact reduction sequence magnetic resonance imaging scans, estimation of serum-ion concentrations of chromium and cobalt and the Copenhagen Hip and Groin Outcome Score (HAGOS) questionnaire were completed on Day 14.
Results
Patients with a pseudotumour who underwent MoM THA/RHA had a higher average cadence of median 101.4 [interquartile range (IQR: 95.5–105)] steps/min than patients without a pseudotumor, median 96.7 (IQR: 92.2–103) steps/min (p = 0.02). Serum-ion concentrations of chromium and cobalt were higher in patients with a pseudotumour who underwent MoM THA/RHA, median 2.57 (IQR: 1.4–3.4) μg/L and 1.80 (IQR: 1.2–2.6) μg/L, respectively, than in patients without a pseudotumour, median 1.85 (IQR: 1.1–3.2) μg/L and 1.34 (IQR: 0.9–2.2) μg/L in MoM THA/RHA (p = 0.04 and p = 0.03). There was no statistical difference in these parameters between patients with and without a pseudotumour who underwent MoP THA. Daily PA levels of patients who underwent MoM THA/RHA were significantly correlated with serum-ion concentrations of chromium (p = 0.0002, r = 0.44) and cobalt (p = 0.005, r = 0.34), whereas no correlations were seen among patients who underwent MoP THA (p > 0.12).
Conclusion
The daily PA level of patients who underwent MoM THA/RHA influences the serum-ion concentrations of chromium and cobalt and the risk of pseudotumour formation.
Translational potential of this article
Results of this article add important knowledge on potential recommendations of prosthesis selection for patients with a high level of physical activity.
Keywords: 3D accelerometer, Clinical outcome measures, Metal-on-metal, Magnetic resonance imaging, Metal-ion concentrations, Resurfacing hip arthroplasty, Total hip arthroplasty
Introduction
The orthopaedic community had big expectations to the third generation of large-head metal-on-metal (MoM) total hip articulations (THA) and resurfacing hip articulations (RHA) which were considered an excellent treatment option for young and physically active patients for whom the survival of conventional metal-on-polyethylene (MoP) THA was not sufficient [1], [2]. However, during 2006–2008, an increasing number of reports revealed that the metal wear debris generated from the bearing surfaces was associated with undesirable side effects such as cystic, mixed and solid pseudotumours [3], [4], [5] and high systemic concentrations of cobalt and chromium metal ions [6], [7]. Polyethylene wear has been reported to be an outcome of use in patients who underwent MoP THA [8], and it has been hypothesized that increased patient activity might lead to higher metal-ion concentrations in patients who underwent MoM THA/RHA [9], [10]. However, information on this topic is limited, conflicting and insufficiently explored in larger study populations with MoM hip articulations. Gleizes et al [11] found a 10% rise in cobalt levels in two patients with Metasul 28-mm bearings after completing 800 m of walking, and two hip simulator studies that imitated “jogging” found a rise in wear rates [12], [13]. Furthermore, it was recently reported that patients with the Birmingham Hip Modular Head system who had high University of California Los Angeles activity scores had higher levels of chromium than those with low University of California Los Angeles activity scores [14]. Contrasting, no difference was found in chromium and cobalt levels in seven patients who participated in a high-activity week and a low-activity week [15]. Pseudotumours have been described in patients with increased metal wear debris [16] and high systemic levels of chromium and cobalt [17], [18]; however, they have also been found in patients with low systemic levels of chromium and cobalt [19], [20]. A deeper knowledge on the correlation between patient activity, metal-ion concentrations and pseudotumour formation would be valuable for orthopaedic surgeons when advising patients with MoM hip articulations on the effect of activity on metal-ion fluctuations and pseudotumour formation. Thus, the primary aim of this cross-sectional study was to investigate (1) the correlation between patients’ daily physical activity (PA) levels and metal-ion concentrations of chromium and cobalt and (2) the differences in PA parameters between patients with a pseudotumour and patients without a pseudotumour who underwent MoM THA/RHA and MoP THA.
Materials and methods
Patients and articulations
A total of 99 patients with 134 THAs (61 females and 73 males) participated in a cross-sectional study between August 19th and October 17th 2014 at Aarhus University Hospital, Denmark, at mean 7.3 (range: 0.4–21.7) years after surgery. Patients were identified and recruited from five former local research projects on MoM and MoP hip arthroplasties [21], [22], [23], [24]. A detailed description of the inclusion and exclusion criteria in each study can be found in the following publications [21], [22], [23], [24]. Shortly, the overall inclusion criteria of the five studies were primary osteoarthritis of the hip, acceptable bone mineral density on preoperative dual-energy X-ray absorptiometry (DXA) scan (T-score > 1), age between 18 and 65 years and a written informed consent to participate. The overall exclusion criteria of the five studies were vascular or neuromuscular disease in the operated leg; fracture sequelae; avascular necrosis of the femoral head; women planning pregnancy; alcohol abuse and daily intake of nonsteroidal antiinflammatory drugs, K-vitamin antagonists or loop diuretics. In the present study, patients were divided into two groups; (1) MoM hip articulations (n = 71) (MoM THA (n = 29) and MoM RHA (n = 42)) and (2) MoP THA (n = 63). Descriptive baseline characteristics of all patients and arthroplasties are presented in Table 1 and Figure 1. For insertion of all MoM and MoP THAs, the posterior surgical approach was used. For insertion of the MoM RHAs, either a posterior (ad modum Moore) [25] (n = 37) or an anterolateral (ad modum Watson) [25] (n = 6) surgical approach was used.
Table 1.
Descriptive baseline characteristics of patients with metal-on-metal (MoM) total hip arthroplasty (THA)/ resurfacing hip arthroplasty (RHA) and metal-on-polyethylene (MoP) THA.
| Articulation | MoM THA/HRA | MoP THA | p |
|---|---|---|---|
| Patients and implants | |||
| Number of patients | 71 | 63 | — |
| Sex (male/female) | 46/25 | 27/36 | 0.01a |
| Age at follow-up | 59.4 (51.6–64.6) | 68.5 (61.2–70.2) | 0.0001b |
| Years since operation | 7.4 (4.9–7.9) | 8.5 (4.4–11.0) | 0.0001b |
| Implant side, right/left | 42/29 | 28/35 | 0.92a |
| Inclination cup angle (°) | 43.7 (30.4–57.1) | 43.8 (28.9–57.7) | 0.93a |
| Anteversion cup angle (°) | 19.1 (4.9–36.9) | 23.9 (7.9–44.3) | 0.002a |
| HAGOS | |||
| Symptoms | 96.4 (83.9–100) | 92.9 (85.7–100) | 0.52 b |
| Pain | 100 (90–100) | 100 (92.5–100) | 0.86 b |
| Function in daily living | 100 (85–100) | 97.5 (85–100) | 0.44 b |
| Sport and recreation | 98 (75–100) | 84.4 (68.8–93.8) | 0.12 b |
| Physical activities | 87.5 (50–100) | 75 (50–100) | 0.56 b |
| Hip-related quality of life | 95 (67.5–100) | 90 (70–100) | 0.61 b |
HAGOS = Hip and Groin Outcome Score.
Analysis of variance. Values are represented as mean (range)
Two-sample Wilcoxon rank-sum (Mann–Whitney) test. Values are median (interquartile range).
Figure 1.
Presentation of the different types and brands of hip articulations included in the study.
All patients gave informed consent to participate in this study, and all examinations were performed in accordance with the Helsinki Declaration II. The study was approved by the Danish Committee on Biomedical Research Ethics (03.17.2014; jr. nr.: 1-10-72-65-14) and by the Danish Data Protection Agency (02.17.2014; jr. nr.: 2007-58-0010, Trial nr.: 1-16-02-87-14).
Metal artefact reduction sequence magnetic resonance imaging scans
As formerly described [26], [27], an MRI protocol with five sequences was used (Table 2) to scan the pelvis and proximal one-third of both femurs. The metal artefact reduction sequence (MARS) magnetic resonance imaging (MRI) scans were performed using two identical 1.5 T Philips Ingenia MRI scanners (Koninklijke Philips Electronics NV, Eindhoven, the Netherlands), and patients were placed in standardized positions: supine, body parallel with the examination table, feet fixated with a band and first toes pointing towards each other. The MRI scans were assessed on a PACS work station (Agfa Impax, Belgium, version 6.3.1.8000). Two observers evaluated the scans in consensus; one experienced musculoskeletal radiologist (LR) and one PhD student (MHH). The observers were blinded to patients' clinical details, radiographs and serum-ion concentrations.
Table 2.
Details of magnetic resonance imaging parameters used in this study.
| Pulse sequence name | TE (ms) | TR (ms) | TI (ms) | ST (mm) /gab (mm) |
FOV | Matrix size | BW (Hz/pixel) | Coil |
|---|---|---|---|---|---|---|---|---|
| Coronal T1W MARS | 15 | 450–650 | — | 2.5/1 | 360 × 450 | 380 × 356 | 438.6 | Sense Body 16ch |
| Coronal STIR MARS | 40 | 4000–8000 | 130 | 3.5/1 | 400 × 454 | 364 × 320 | 434.7 | Sense Body 16ch |
| Coronal T2W MARS | 80 | 3000–7000 | — | 2.5/1 | 360 × 450 | 380 × 316 | 438.6 | Sense Body 16ch |
| Axial T1W MARS | 16 | 450–650 | — | 2.5/1.5 | 400 × 454 | 420 × 348 | 437.7 | Sense Body 16ch |
| Axial STIR MARS | 40 | 4000–8000 | 130 | 3.5/1.5 | 360 × 447 | 276 × 272 | 435.5 | Sense Body 16ch |
BW = band width; FOV = field of view; MARS = Metal artefact reduction sequence; ST = slice thickness (mm, millimetre); STIR = short tau inversion recovery; TE = time of echo (ms, millisecond); TI = time of inversion (ms, millisecond); TR = time of repetition (ms, millisecond); TSE = turbo spin echo; W = weighted.
The Anderson pseudotumour grading system was used to classify pseudotumour findings. This classification has proved the highest intraobserver and interobserver reliability of the currently used systems [28], [29]. The Anderson grading system consists of three categories, A, B and C. Category A is equivalent to “normal or acceptable”, Category B is equivalent to “infection” and Category C is divided into three subgroups: C1 indicates “mild MoM disease”, C2 indicates “moderate MoM disease” and C3 indicates “severe MoM disease”. Besides pseudotumour classification according to the Anderson grading system, we recorded pseudotumour type (fluid/mixed or solid) and anatomical location (anterolateral or posterolateral to the greater trochanter or located to the iliopsoas bursa). Different from the Anderson grading system, patients with a C1 lesion and muscle atrophy or oedema in any other muscles than the short external rotators were not classified as C2 [30].
Assessment of PA
As described in a previous study [27], a commercially available accelerometer (Axivity, Newcastle upon Tyne, England), which determines the acceleration of body parts in three planes, was used to measure and classify PA. The accelerometer was set to monitor at 100 Hz and ±8 g. The patients were instructed to wear it during wake hours and to mount the accelerometer on the lateral side on the right thigh with Fixomull tape (3M, USA). The accelerometers were worn for a minimum of 8 h of wear time per day for a mean of 15 (range: 10–21) days. All accelerometer-based activity data were analyzed by one person. The raw acceleration signal was analyzed using the inclinometer function of the accelerometer and algorithm-based peak detection methods in Matlab (MATLAB R2010a; The Mathworks Inc., Natick, Massachusetts, USA), based on previously published principles [31], [32]. Briefly, calibration of the accelerometer's orientation was performed within a period of level walking, which was manually selected. Within this walking period, the average magnitudes of the three acceleration vectors and the gait cycle frequency (Hz) were derived to allow further differentiation between activities. Differentiation between standing periods and sitting periods was based on the direction of the gravitation vector. Walking was differentiated from other upright activities (all classified as standing) by application of heuristic rules to the gait cycle frequency. A walking period was classified when at least five consecutive heel strike peaks were detected, with 0.6 Hz and 5-min walking bouts. More detailed information of the accelerometer and its clinical application has been described in a previous study [33].
Cup position, serum-ion measurements and clinical outcome scores
At postoperative, mean 7.3 (range: 0.4–21.7) years' follow-up, standardized, weight-bearing anteroposterior pelvic and lateral hip radiographs were obtained. Cup inclination and anteversion angles were estimated digitally (PolyWare 3D Digital, version 5.10; Draftware Developers, Conway, SC) [34], [35]. Blood samples for metal-ion investigations were collected according to the present guidelines [36]. Analyses were undertaken using an inductively coupled plasma–mass spectrometry (ICP-MS) at XXX Hospital, XXX. All patients had normal renal function as determined by serum creatinine levels and estimated glomerular filtration rate. Patients completed The Copenhagen Hip and Groin Outcome Score (HAGOS) questionnaire (0-100 scale, where a high score indicates a good outcome) [37]. Patients with bilateral hip articulations completed two questionnaires (one for each hip).
Statistical analysis
Data were checked for normality using the Shapiro–Wilk test combined with Q–Q plot and histograms. Nonparametric data were natural logarithm transformed to allow parametric testing. Logistic regression was used to analyze the effect of the activity parameters on pseudotumour formation. We adjusted for sex, inclination angels and bearing type (MoM THA/RHA) as these variables have been shown to affect serum metal-ion concentrations of chromium and cobalt and pseudotumour prevalence [38], [39], [40], [41]. Subanalysis between MoM THA and MoM RHA showed that pseudotumours were present in 9 of 29 (31%) MoM THAs and in 13 of 42 (31%) MoM RHAs. Pearson's correlation was used to investigate the correlation between activity parameters and serum-ion concentrations of chromium and cobalt. Outcome scores of the HAGOS questionnaire were not normally distributed after natural logarithm transformation, and therefore, the nonparametric two-sample Wilcoxon rank-sum (Mann–Whitney) test was used to compare scores between patients who underwent MoM THA/RHA and patients who underwent MoP THA. P-values less than 0.05 were considered statistically significant for the hypotheses tests. All analyses were performed using STATA software, version 13 (StataCorp LP, College Station, Texas).
Results
MARS MRI scans
MRI scans, conventional radiographs and blood samples were obtained from all patients. Accelerometer data from five patients could not be analysed due to technical problems, and 11 patients did not return the HAGOS questionnaire.
MARS MRI evaluations showed that pseudotumours or “MoM disease” were present in 22 of 71 (31%) MoM THA/RHAs and in 25 of 63 (40%) MoP THAs. Mixed or solid pseudotumours were found in two patients who underwent MoM THA (one male and one female) and in eight patients who underwent MoP THA (four males and four females). A detailed description of the MRI evaluations according to the Anderson grading system is presented in Table 3 and Figure 2, Figure 3.
Table 3.
Results of the MARS MRI evaluations according to the Anderson classification.
| Articulation | MoM THA/RHA | MoP THA |
|---|---|---|
| Total number of hips | 71 | 63 |
| Total number of pseudotumours | 22 | 25 |
| Grade A “normal or acceptable” | 49 | 38 |
| Grade B “infection” | 0 | 0 |
| Grade C1 “mild MoM disease” | 12 | 14 |
| Male/female | 8/4 | 5/9 |
| Fluid/mixed or solid | 11/1 | 11/2 |
| Location (PL/ILB/AL) | 11/0/1 | 6/8/0 |
| Grade C2 “moderate MoM disease” | 9 | 10 |
| Male/female | 8/1 | 7/3 |
| Fluid/mixed or solid | 8/1 | 5/5 |
| Location (PL/ILB/AL) | 7/0/2 | 5/5/0 |
| Grade C3 “severe MoM disease” | 1 | 1 |
| Male/female | 1/0 | 1/0 |
| Fluid/mixed or solid | 1/0 | 0/1 |
| Location (PL/ILB/AL) | 0/0/1 | 0/1/0 |
In addition to the Anderson classification, pseudotumour appearance (fluid or mixed/solid) and location were recorded.
Location: The anatomical location of the pseudotumour: AL = anterolateral of the greater trochanter; PL = posterolateral of the greater trochanter; ILB = located at the iliopsoas bursa.
MARS = Metal artefact reduction sequence; MoM = metal-on-metal; MoP = metal-on-polyethylene; MRI = magnetic resonance imaging; RHA = resurfacing hip arthroplasty; THA = total hip arthroplasty.
Figure 2.
(A) Coronal and (B) axial MARS MRIs of a 54-year-old male with right-side MoM THA (M2a-Magnum, BiMetric Stem) and a mixed pseudotumour located at the iliopsoas bursa. His serum metal-ion levels of chromium and cobalt were 1.4 μg/L and 2.8 μg/L, respectively.
MARS = Metal artefact reduction sequence; MoM = metal-on-metal; MRI = magnetic resonance imaging; RHA = resurfacing hip arthroplasty; THA = total hip arthroplasty.
Figure 3.
(A) Coronal and (B) axial MARS MRIs of a 64-year-old male with bilateral MoP THA (Right side: Mallory Head, Exeeter Stem, and left side: Pinnacle cup, Corail stem). The pseudotumour on the right side is of mixed type, and on the left side, it is of cystic type.
MARS = Metal artefact reduction sequence; MoP = metal-on-polyethylene; MRI = magnetic resonance imaging; RHA = resurfacing hip arthroplasty; THA = total hip arthroplasty.
Correlation between PA, serum ions and pseudotumours
Patients with a pseudotumour who underwent MoM THA/RHA had a significantly higher average cadence of median 101.4 (IQR: 95.5–105) steps/min. than patients without a pseudotumour, median 96.7 (IQR: 92.2–103) steps/min. (p = 0.02). Patients with a pseudotumour who underwent MoM THA/RHA had significantly higher serum-ion concentrations of chromium and cobalt of median 2.57 (IQR: 1.4–3.4) μg/L and 1.80 (IQR: 1.2–2.6) μg/L compared to median 1.85 (IQR: 1.1–3.2) μg/L and 1.34 (IQR: 0.9–2.2) μg/L in patients without a pseudotumour, respectively (p = 0.04 and 0.03) (Table 4). There was no difference in the activity parameters in patients with and without a pseudotumour who underwent MoP THA (Table 4). Daily PA level of patients who underwent MoM THA/RHA was significantly correlated with serum-ion concentrations of chromium (p = 0.0002; r = 0.44) and cobalt (p = 0.005; r = 0.34), and this relationship was not seen in patients who underwent MoM THA (p > 0.12) (Table 5).
Table 4.
Differences in activity parameters and serum ions of chromium between patients with a pseudotumour and patients without a pseudotumour.
| Output | Pseudotumour | Nonpseudotumour | p a |
|---|---|---|---|
| MoM THA/RHA | |||
| Average cadence (steps/min) | 101.4 (95.5–105) | 96.7 (92.2–103) | 0.02 |
| All activities b (%) | 41.3 (36.2–46.9) | 37.8 (29.3–48.4) | 0.26 |
| All inactivities c (%) | 56.8 (53.1–63.7) | 58.8 (51.5–70.7) | 0.54 |
| Walking time (%) | 12.1 (11–15) | 10.8 (8.9–13.8) | 0.26 |
| Bicycling time (%) | 0.45 (0.2–1.6) | 0.20 (0.1–0.36) | 0.09 |
| High-impact activity (%) | 0.02 (0.001–0.14) | 0.005 (0.001–0.01) | 0.08 |
| Sitting or lying down (%) | 56.8 (53.1–63.7) | 58.8 (51.5–70.7) | 0.54 |
| Standing time (%) | 27.5 (21.7–30.4) | 25.6 (19.7–34.8) | 0.41 |
| Chromium (μg/L) | 2.57 (1.4–3.4) | 1.85 (1.1–3.2) | 0.04 |
| Cobalt (μg/L) | 1.80 (1.2–2.6) | 1.34 (0.9–2.2) | 0.03 |
| MoP THA | |||
| Average cadence (steps/min) | 93.4 (89.2–99.6) | 95.7 (90.7–103.3) | 0.30 |
| All activities b (%) | 41.2 (36.7–45.7) | 38.3 (29.9–47.4) | 0.32 |
| All inactivities c (%) | 57.7 (54.3–63.3) | 58.5 (52.5–70.2) | 0.79 |
| Walking time (%) | 12.0 (9.5–15.6) | 11.3 (9.0–15.9) | 0.51 |
| Bicycling time (%) | 0.40 (0.14–1.82) | 0.12 (0.14–0.92) | 0.05 |
| High-impact activity (%) | 0.01 (0.00–0.04) | 0.01 (0.00–0.28) | 0.70 |
| Sitting (%) | 57.7 (54.3–63.3) | 58.5 (52.5–70.2) | 0.79 |
| Standing time (%) | 27.4 (23.1–29.2) | 25.4 (19.4–35.1) | 0.32 |
| Chromium (μg/L) | 0.75 (0.59–0.72) | 0.86 (0.59–1.16) | 0.34 |
| Cobalt (μg/L) | 0.75 (0.59–0.65) | 0.95 (0.59–0.67) | 0.12 |
MoM = metal-on-metal; MoP = metal-on-polyethylene; RHA = resurfacing hip arthroplasty; THA = total hip arthroplasty.
Logistic regression (adjusting for risk factors of sex, inclination angle and the type of arthroplasty in the MoM THA/RHA group). Values are represented as median (interquartile range).
All activities defined as walking, standing, bicycling and high-impact activity
All inactivities defined as sitting and lying down
Table 5.
Correlations between accelerometer variables and values of chromium and cobalt in all patients. Estimates are Pearson's r (p-value).
| AM parameters | Cobalt, Pearson's r (p-value) | Chromium, Pearson's r (p-value) |
|---|---|---|
| MoM THA/RHA | ||
| Average cadence (steps/min) | 0.02 (0.89) | 0.08 (0.54) |
| All activities a (%) | 0.34 (0.005) | 0.44 (0.0002) |
| All inactivities b (%) | −0.35 (0.004) | −0.44 (0.0002) |
| Walking time (%) | 0.22 (0.08) | 0.30 (0.01) |
| Cycling time (%) | 0.11 (0.40) | 0.14 (0.28) |
| High-impact activity (%) | 0.03 (0.88) | −0.09 (0.60) |
| Sitting (%) | −0.35 (0.004) | −0.44 (0.0002) |
| Standing time (%) | 0.31 (0.01) | 0.44 (0.001) |
| MoP THA | ||
| Average cadence (steps/min) | −0.01 (0.99) | −0.44 (0.75) |
| All activities a (%) | −0.19 (0.15) | −0.13 (0.32) |
| All inactivities b (%) | 0.15 (0.27) | 0.09 (0.51) |
| Walking time (%) | −0.07 (0.59) | −0.13 (0.33) |
| Cycling time (%) | −0.21 (0.45) | −0.14 (0.32) |
| High-impact activity (%) | −0.10 (0.15) | 0.07 (0.61) |
| Sitting (%) | 0.15 (0.27) | 0.09 (0.51) |
| Standing time (%) | 0.34 (0.12) | 0.02 (0.94) |
AM, accelerometer; MoM = metal-on-metal; MoP = metal-on-polyethylene; RHA = resurfacing hip arthroplasty; THA = total hip arthroplasty.
All activities defined as walking, standing, cycling and high-impact activity.
All inactivities defined as sitting and lying down.
Discussion
We investigated the relationship of PA parameters on serum-ion concentrations of chromium and cobalt and pseudotumour formation in a relatively large study population of both patients who underwent MoM THA/RHA and MoP THA. Interestingly, we found significant correlations between patients' daily PA levels and serum-ion concentrations of chromium and cobalt in patients who underwent MoM THA/RHA, but not in the group of patients who underwent MoP THA. Furthermore, patients with a pseudotumour who underwent MoM THA/RHA had higher average cadence and higher serum-ion concentrations of chromium and cobalt than patients without a pseudotumour who underwent MoM THA/RHA, and this difference was not present in patients who underwent MoP THA. These results indicate that the daily PA level of patients who underwent MoM THA/RHA influence the serum-ion concentrations of chromium and cobalt and the risk of pseudotumour formation. Information on this topic may by relevant for the orthopaedic surgeon when advising patients with MoM hip articulations on the consequences of activity on serum-ion concentrations and pseudotumor formation—especially because many patients' MoM hip articulations are characterized by a high level of PA.
Previous studies of activity-related changes in serum-ion concentrations of chromium and cobalt after MoM THA or RHA have yielded varying results. An “in vitro” hip simulator study reported a 20-fold increase in metal-ion wear particles when imitating fast jogging compared to normal walking [42]. Similar results have been described in an “in vivo” study by Khan et al [43] who investigated 15 patients with three different MoM bearing types (Birmingham Hip Resurfacing, Cormet 2000 resurfacing and Metasul THA) and found that 1 h of running or fast walking on a treadmill resulted in a mean rise of serum chromium of 11% and of serum cobalt of 13%.
In contrast, Heisel et al. monitored seven patients with MoM hip articulations at 7 to 25 months postoperatively during a two-week period; in the first week, patients were instructed to limit their activity levels, and the next week, patients were encouraged to raise their activity levels, and they completed a 1-h treadmill test. However, no significant differences were found in mean serum cobalt and chromium levels between the low-exercise week (cobalt, 1.4 ppb; SD, 0.85; chromium, 2.08 ppb; SD, 0.9) and the high-exercise week (cobalt, 1.29 ppb; SD. 0.63; chromium, 2.12 ppb; SD, 0.87) [15]. In addition, a triathlete with a Birmingham hip resurfacing hip articulation had his serum-ion concentrations of chromium and cobalt, and urine chromium measured seven days before, during and after a triathlon race. There was no significant change in serum-ion concentrations of chromium or cobalt, but urine chromium levels were significantly elevated immediately after and until 6 days after the race [44]. It is complex to provide an exact clarification for these different findings. However, differences in the analytical serum-ion measurement techniques might play a role. Our study and the study by Khan et al. used inductively coupled plasma–mass spectrometry (ICP-MS), which has a detection limit of 0.02 μg/L for chromium and 0.005 μg/L for cobalt in serum [45], whereas Heisel et al [15] used graphite furnace atomic absorption, which has a detection limit of 0.03 μg/L for chromium and 0.3 μg/L for cobalt in serum. Furthermore, De Hann et al collected their blood samples on the day after the race, by which time the metal ions could have returned to their preexercise levels and thus biased the results. One limitation of the aforementioned studies was small study populations (15, 7 and 1 patient). However, because we investigated 71 MoM hip articulations, our results add strength to the hypothesis that the activity level in patients with MoM hip articulations does influence serum-ion concentrations of chromium and cobalt. Furthermore, the validity of our findings in MoM THA/RHA patients was supported by the insignificant correlations between activity levels and serum-ion concentrations of chromium and cobalt found in patients who underwent MoP THA.
All bearing surfaces experience some degree of wear debris. The dominant source of wear debris in MoM THA/RHA origins from the cobalt–chromium alloy bearing [46]. In THA, corrosion at the taper–trunnion junction also plays a significant role in the generation of metal-ion wear debris [47], [48], [49]. This leads to elevated serum-ion concentrations in MoM THA compared to MoM RHA [50], [51] and may also lead to high serum-ion concentrations and soft-tissue reactions with pseudotumours in MoP THA [52], [53], [54], [55]. We observed pseudotumours in 22 of 71 (31%) patients who underwent MoM THA/RHA and in 25 of 63 (40%) patients who underwent MoP THA. Patients with a pseudotumour who underwent MoM THA/RHA had significant higher serum-ion concentrations of chromium and cobalt and a higher average cadence than patients without a pseudotumour. Former studies have additionally described pseudotumours in patients with high levels of metal wear debris [16] and high systemic levels of chromium and cobalt metal ions [17], [18]. However, pseudotumours have also been described in patients with low systemic levels of chromium and cobalt metal ions [19], [56]. These conflicting results might be due to various blood sampling procedures (e.g., specimen collection, processing, analysis and storage) and various definitions of pseudotumours and pseudotumour-grading systems [19], [29], [56], [57], [58], which makes it difficult to compare results between studies directly.
In MoP THA, it has been shown that patients with high polyethylene wear rates (mean, 0.134 mm/year) have a 17% higher average cadence than patients with low polyethylene wear rates (mean, 0.047 mm/year) [59]. This is similar to our results of the patients with a pseudotumour who underwent MoM THA/RHA, who had a significant higher average cadence along with higher serum-ion concentrations of chromium and cobalt, compared to patients without a pseudotumour who underwent MoM THA/RHA.
We recognize the limitations of our study. First, the study was limited by the relatively small sample size investigated. Second, we did not monitor fluid output and intake, and patients might have been dehydrated or overhydrated at the time point of blood sampling. Third, the two groups were not matched and different in anteversion angle, time since operation and age. However, because there was no difference between groups in the HAGOS score, we believe that patients had similar physical capacity.
Finally, patients did not follow an activity protocol, and it is uncertain whether an acute increase in activity or longer changes in activity would have affected the serum-ion concentrations. However, the aim of the study was to measure patient's daily PA levels in an uncontrolled environment, and just four days of activity monitoring has been shown to reflect the general activity level of individuals [60].
Conclusion
Our results suggest that the daily PA levels of patients who underwent MoM THA/RHA influence the serum-ion concentrations of chromium and cobalt and the risk of pseudotumour formation. At the same time, we do not neglect that other factors such as implant orientation, head size, clearance, edge loading, manufacturing process, type of coating, shell thickness, use of adaptor sleeve and the female gender may also play a role. Nevertheless, our results add new and important knowledge to the literature and valuable information for the orthopaedic surgeon when advising patients with MoM hip articulations on the consequences of activity on serum-ion concentrations of chromium and cobalt and pseudotumour formation—especially because many patients were selected to undergo MoM hip arthroplasty due to their high activity level.
Funding
This study was not supported by any funding.
Conflict of interest
None of the authors have financial or institutional disclosures to report related to the research in this article.
Authors’ contributions
M.H., M.S., I.M., L.R. and K.S. were involved in the follow-up examinations. M.H., I.M. and M.S. performed the statistical analyses and interpretation. M.H. wrote the initial manuscript, and M.S., I.M., L.R. and K.S. helped revise it. All authors approved the final manuscript.
Ethical approval and informed consent
All patients gave informed consent to participate in this study, and all examinations were performed in accordance with the Helsinki Declaration II. The study was approved by the Danish Committee on Biomedical Research Ethics (03.17.2014; jr. nr.: 1-10-72-65-14) and by the Danish Data Protection Agency (02.17.2014; jr. nr.: 2007-58-0010, Trial nr.: 1-16-02-87-14).
Acknowledgements
The authors thank Lone Loevgren, Rikke Moerup, Peter Bo Joergensen and Inger Krog-Mikkelsen for their help in arranging the follow-up.
Contributor Information
Mette Holm Hjorth, Email: mettehh20@gmail.com.
Inger Mechlenburg, Email: inger.mechlenburg@clin.au.dk.
Kjeld Soballe, Email: kjeld@soballe.com.
Lone Roemer, Email: lone.roemer@dadlnet.dk.
Maiken Stilling, Email: maiken.stilling@clin.au.dk.
References
- 1.McMinn D.J. Development of metal/metal hip resurfacing. Hip Int J Clin Exp Res Hip Pathol Ther. 2003;13:41–53. doi: 10.1177/112070000301302s09. [DOI] [PubMed] [Google Scholar]
- 2.Amstutz H.C., Grigoris P., Dorey F.J. Evolution and future of surface replacement of the hip. J Orthop Sci Off J Jpn Orthop Ass. 1998;3:169–186. doi: 10.1007/s007760050038. [DOI] [PubMed] [Google Scholar]
- 3.Pandit H., Glyn-Jones S., McLardy-Smith P., Gundle R., Whitwell D., Gibbons C.L. Pseudotumours associated with metal-on-metal hip resurfacings. JBone Joint SurgBr. 2008;90:847–851. doi: 10.1302/0301-620X.90B7.20213. [DOI] [PubMed] [Google Scholar]
- 4.Gruber F.W., Bock A., Trattnig S., Lintner F., Ritschl P. Cystic lesion of the groin due to metallosis: a rare long-term complication of metal-on-metal total hip arthroplasty 1. J Arthroplasty. 2007;22:923–927. doi: 10.1016/j.arth.2006.10.002. [DOI] [PubMed] [Google Scholar]
- 5.Boardman D.R., Middleton F.R., Kavanagh T.G. A benign psoas mass following metal-on-metal resurfacing of the hip. J Bone Joint Surg Br Vol. 2006;88:402–404. doi: 10.1302/0301-620X.88B3.16748. [DOI] [PubMed] [Google Scholar]
- 6.De S.K., de H.R., Calistri A., Campbell P.A., Ebramzadeh E., Pattyn C. Metal ion measurement as a diagnostic tool to identify problems with metal-on-metal hip resurfacing. JBone Joint Surg Am. 2008;90(Suppl 4):202–208. doi: 10.2106/JBJS.H.00672. [DOI] [PubMed] [Google Scholar]
- 7.Langton D.J., Jameson S.S., Joyce T.J., Webb J., Nargol A.V. The effect of component size and orientation on the concentrations of metal ions after resurfacing arthroplasty of the hip. JBone Joint SurgBr. 2008;90:1143–1151. doi: 10.1302/0301-620X.90B9.20785. [DOI] [PubMed] [Google Scholar]
- 8.Schmalzried T.P., Shepherd E.F., Dorey F.J., Jackson W.O., dela Rosa M., Fa'vae F. The John Charnley Award. Wear is a function of use, not time. Clin Orthop Relat Res. 2000:36–46. doi: 10.1097/00003086-200012000-00005. [DOI] [PubMed] [Google Scholar]
- 9.De H.R., Campbell P., Reid S., Skipor A.K., De S.K. Metal ion levels in a triathlete with a metal-on-metal resurfacing arthroplasty of the hip 7. JBone Joint SurgBr. 2007;89:538–541. doi: 10.1302/0301-620X.89B4.18563. [DOI] [PubMed] [Google Scholar]
- 10.Pattyn C.A., Lauwagie S.N., Verdonk R.C. Whole blood metal ion concentrations in correlation with activity level in three different metal-on-metal bearings 18. J Arthroplasty. 2011;26:58–64. doi: 10.1016/j.arth.2009.11.007. [DOI] [PubMed] [Google Scholar]
- 11.Gleizes V., Poupon J., Lazennec J.Y., Chamberlin B., Saillant G. [Value and limits of determining serum cobalt levels in patients with metal on metal articulating prostheses] Revue de chirurgie orthopedique et reparatrice de l'appareil moteur. 1999;85:217–225. [PubMed] [Google Scholar]
- 12.Jacobs J.J., Skipor A.K., Patterson L.M., Hallab N.J., Paprosky W.G., Black J. Metal release in patients who have had a primary total hip arthroplasty. A prospective, controlled, longitudinal study. J Bone Joint Surg Am Vol. 1998;80:1447–1458. doi: 10.2106/00004623-199810000-00006. [DOI] [PubMed] [Google Scholar]
- 13.Chan F.W., Bobyn J.D., Medley J.B., Krygier J.J., Tanzer M. The Otto Aufranc Award. Wear and lubrication of metal-on-metal hip implants. Clin Orthop Relat Res. 1999:10–24. doi: 10.1097/00003086-199912000-00003. [DOI] [PubMed] [Google Scholar]
- 14.Kasparek M.F., Renner L., Faschingbauer M., Waldstein W., Weber M., Boettner F. Predictive factors for metal ion levels in metal-on-metal total hip arthroplasty. Arch Orthop Trauma Surg. 2018;138:281–286. doi: 10.1007/s00402-017-2856-y. [DOI] [PubMed] [Google Scholar]
- 15.Heisel C., Silva M., Skipor A.K., Jacobs J.J., Schmalzried T.P. The relationship between activity and ions in patients with metal-on-metal bearing hip prostheses. J Bone Joint Surg Am Vol. 2005;87:781–787. doi: 10.2106/JBJS.D.01820. [DOI] [PubMed] [Google Scholar]
- 16.Kwon Y.M., Glyn-Jones S., Simpson D.J., Kamali A., McLardy-Smith P., Gill H.S. Analysis of wear of retrieved metal-on-metal hip resurfacing implants revised due to pseudotumours. JBone Joint SurgBr. 2010;92:356–361. doi: 10.1302/0301-620X.92B3.23281. [DOI] [PubMed] [Google Scholar]
- 17.Bosker B.H., Ettema H.B., van Rossum M., Boomsma M.F., Kollen B.J., Maas M. Pseudotumor formation and serum ions after large head metal-on-metal stemmed total hip replacement. Risk factors, time course and revisions in 706 hips. Arch Orthop Trauma Surg. 2015;135:417–425. doi: 10.1007/s00402-015-2165-2. [DOI] [PubMed] [Google Scholar]
- 18.Chang E.Y., McAnally J.L., Van Horne J.R., Van Horne J.G., Wolfson T., Gamst A. Relationship of plasma metal ions and clinical and imaging findings in patients with ASR XL metal-on-metal total hip replacements. J Bone Joint Surg Am Vol. 2013;95:2015–2020. doi: 10.2106/JBJS.L.01481. [DOI] [PubMed] [Google Scholar]
- 19.Matthies A.K., Skinner J.A., Osmani H., Henckel J., Hart A.J. Pseudotumors are common in well-positioned low-wearing metal-on-metal hips. Clin Orthop Relat Res. 2012;470:1895–1906. doi: 10.1007/s11999-011-2201-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Fehring T.K., Odum S., Sproul R., Weathersbee J. High frequency of adverse local tissue reactions in asymptomatic patients with metal-on-metal THA. Clin Orthop Relat Res. 2014;472:517–522. doi: 10.1007/s11999-013-3222-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Hjorth M.H., Stilling M., Soballe K., Bolvig L.H., Thyssen J.P., Mechlenburg I. No association between pseudotumors, high serum-ion levels and metal hypersensitivity in large-head MoM THA at 5-7 year follow-up. Skeletal Radiol. 2016;45:115–125. doi: 10.1007/s00256-015-2264-8. [DOI] [PubMed] [Google Scholar]
- 22.Hjorth M.H., Kold S., Soballe K., Langdahl B.L., Nielsen P.T., Christensen P.H. Preparation of the femoral bone cavity for cementless stems: broaching vs compaction. A five-year randomized radiostereometric analysis and dual energy X-ray absorption study. J Arthroplasty. 2017;32:1894–1901. doi: 10.1016/j.arth.2016.12.029. [DOI] [PubMed] [Google Scholar]
- 23.Hjorth M.H., Lorenzen N.D., Soballe K., Jakobsen S.S., Stilling M. Equal primary fixation of resurfacing Stem, but inferior cup fixation with anterolateral vs posterior surgical approach. A 2-year blinded randomized radiostereometric and dual-energy X-ray absorptiometry study of metal-on-metal hip resurfacing arthroplasty. J Arthroplasty. 2017;32(11):3412–3420. doi: 10.1016/j.arth.2017.05.034. [DOI] [PubMed] [Google Scholar]
- 24.Hjorth M.H., Stilling M., Nielsen P.T., Christensen P.H., Kold S. Preparation of the femoral bone cavity in cementless stems: broaching versus compaction. J Arthroplasty. 2017;32(6):1894–1901. doi: 10.1016/j.arth.2016.12.029. [DOI] [PubMed] [Google Scholar]
- 25.De Smet K., Campbell P. 2013. The hip resurfacinf handbook. A practical guide to the use and management of modern hip resurfacing. [Google Scholar]
- 26.Hjorth M.H., Mechlenburg I., Soballe K., Roemer L., Jakobsen S.S., Stilling M. Higher prevalence of mixed or solid pseudotumors in metal-on-polyethylene total hip arthroplasty compared with metal-on-metal total hip arthroplasty and resurfacing hip arthroplasty. J Arthroplasty. 2018;33(7):2279–2286. doi: 10.1016/j.arth.2018.02.011. [DOI] [PubMed] [Google Scholar]
- 27.Hjorth M.H., Mechlenburg I., Soballe K., Jakobsen S.S., Roemer L., Stilling M. Physical activity is associated with the level of chromium but not with changes in pseudotumor size in patients with metal-on-metal hip arthroplasty. J Arthroplasty. 2018;33(9):2932–2939. doi: 10.1016/j.arth.2018.04.039. [DOI] [PubMed] [Google Scholar]
- 28.van der Weegen W., Brakel K., Horn R.J., Wullems J.A., Das H.P., Pilot P. Comparison of different pseudotumor grading systems in a single cohort of metal-on-metal hip arthroplasty patients. Skeletal Radiol. 2014;43:149–155. doi: 10.1007/s00256-013-1755-8. [DOI] [PubMed] [Google Scholar]
- 29.Anderson H., Toms A.P., Cahir J.G., Goodwin R.W., Wimhurst J., Nolan J.F. Grading the severity of soft tissue changes associated with metal-on-metal hip replacements: reliability of an MR grading system. Skeletal Radiol. 2011;40:303–307. doi: 10.1007/s00256-010-1000-7. [DOI] [PubMed] [Google Scholar]
- 30.Agten C.A., Sutter R., Dora C., Pfirrmann C.W. MR imaging of soft tissue alterations after total hip arthroplasty: comparison of classic surgical approaches. Eur Radiol. 2017;27:1312–1321. doi: 10.1007/s00330-016-4455-7. [DOI] [PubMed] [Google Scholar]
- 31.Mathie M.J., Celler B.G., Lovell N.H., Coster A.C. Classification of basic daily movements using a triaxial accelerometer. Med Biol Eng Comput. 2004;42:679–687. doi: 10.1007/BF02347551. [DOI] [PubMed] [Google Scholar]
- 32.Preece S.J., Goulermas J.Y., Kenney L.P., Howard D., Meijer K., Crompton R. Activity identification using body-mounted sensors--a review of classification techniques. Physiol Meas. 2009;30:R1–R33. doi: 10.1088/0967-3334/30/4/R01. [DOI] [PubMed] [Google Scholar]
- 33.Schotanus M.G., Bemelmans Y.F., Grimm B., Heyligers I.C., Kort N.P. Physical activity after outpatient surgery and enhanced recovery for total knee arthroplasty. Knee Surg Sports Traumatol Arthrosc. 2016;25(11):3366–3371. doi: 10.1007/s00167-016-4256-1. [DOI] [PubMed] [Google Scholar]
- 34.Devane P.A., Bourne R.B., Rorabeck C.H., Hardie R.M., Horne J.G. Measurement of polyethylene wear in metal-backed acetabular cups. I. Three-dimensional technique. Clin Orthop Relat Res. 1995:303–316. [PubMed] [Google Scholar]
- 35.Devane P.A., Bourne R.B., Rorabeck C.H., MacDonald S., Robinson E.J. Measurement of polyethylene wear in metal-backed acetabular cups. II. Clinical application. Clin Orthop Relat Res. 1995:317–326. [PubMed] [Google Scholar]
- 36.MacDonald S.J., Brodner W., Jacobs J.J. A consensus paper on metal ions in metal-on-metal hip arthroplasties. J Arthroplasty. 2004;19:12–16. doi: 10.1016/j.arth.2004.09.009. [DOI] [PubMed] [Google Scholar]
- 37.Thorborg K., Holmich P., Christensen R., Petersen J., Roos E.M. The copenhagen hip and groin outcome score (HAGOS): development and validation according to the COSMIN checklist. Br J Sports Med. 2011;45:478–491. doi: 10.1136/bjsm.2010.080937. [DOI] [PubMed] [Google Scholar]
- 38.Bishop N., Witt F., Pourzal R., Fischer A., Rutschi M., Michel M. Wear patterns of taper connections in retrieved large diameter metal-on-metal bearings. J Orthop Res Off Publ Orthop Res Soc. 2013;31:1116–1122. doi: 10.1002/jor.22326. [DOI] [PubMed] [Google Scholar]
- 39.Bayley N., Khan H., Grosso P., Hupel T., Stevens D., Snider M. What are the predictors and prevalence of pseudotumor and elevated metal ions after large-diameter metal-on-metal THA? Clin Orthop Relat Res. 2015;473:477–484. doi: 10.1007/s11999-014-3824-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Hart A.J., Muirhead-Allwood S., Porter M., Matthies A., Ilo K., Maggiore P. Which factors determine the wear rate of large-diameter metal-on-metal hip replacements? Multivariate analysis of two hundred and seventy-six components. JBone Joint SurgAm. 2013;95:678–685. doi: 10.2106/JBJS.J.01447. [DOI] [PubMed] [Google Scholar]
- 41.Hart A.J., Skinner J.A., Henckel J., Sampson B., Gordon F. Insufficient acetabular version increases blood metal ion levels after metal-on-metal hip resurfacing. Clin Orthop Relat Res. 2011;469:2590–2597. doi: 10.1007/s11999-011-1930-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42.Bowsher J.G., Hussain A., Williams P.A., Shelton J.C. Metal-on-metal hip simulator study of increased wear particle surface area due to 'severe' patient activity. Proc IME H J Eng Med. 2006;220:279–287. doi: 10.1243/09544119JEIM93. [DOI] [PubMed] [Google Scholar]
- 43.Khan M., Takahashi T., Kuiper J.H., Sieniawska C.E., Takagi K., Richardson J.B. Current in vivo wear of metal-on-metal bearings assessed by exercise-related rise in plasma cobalt level. J Orthop Res Off Publ Orthop Res Soc. 2006;24:2029–2035. doi: 10.1002/jor.20206. [DOI] [PubMed] [Google Scholar]
- 44.De H.R., Campbell P., Reid S., Skipor A.K., De S.K. Metal ion levels in a triathlete with a metal-on-metal resurfacing arthroplasty of the hip 6. J Bone Joint SurgBr. 2007;89:538–541. doi: 10.1302/0301-620X.89B4.18563. [DOI] [PubMed] [Google Scholar]
- 45.Krachler M., Heisel C., Philippe Kretzer J. Validation of ultratrace analysis of Co, Cr, Mo and Ni in whole blood, serum and urine using ICP-SMS. J Anal Atomic Spectrom. 2009;24:605–610. [Google Scholar]
- 46.Skipor A.K., Campbell P.A., Patterson L.M., Anstutz H.C., Schmalzried T.P., Jacobs J.J. Serum and urine metal levels in patients with metal-on-metal surface arthroplasty. J Mater Sci Mater Med. 2002;13:1227–1234. doi: 10.1023/a:1021179029640. [DOI] [PubMed] [Google Scholar]
- 47.Lavigne M., Belzile E.L., Roy A., Morin F., Amzica T., Vendittoli P.A. Comparison of whole-blood metal ion levels in four types of metal-on-metal large-diameter femoral head total hip arthroplasty: the potential influence of the adapter sleeve 21. JBone Joint SurgAm. 2011;93(Suppl 2):128–136. doi: 10.2106/JBJS.J.01885. [DOI] [PubMed] [Google Scholar]
- 48.Junnila M., Kostensalo I., Virolainen P., Remes V., Matilainen M., Vahlberg T. Hip resurfacing arthroplasty versus large-diameter head metal-on-metal total hip arthroplasty: comparison of three designs from the Finnish Arthroplasty Register. Scand J Surg Off Organ Fin Surg Soc Scand Surg Soc. 2014;103:54–59. doi: 10.1177/1457496913495345. [DOI] [PubMed] [Google Scholar]
- 49.Hjorth M.H., Egund N., Mechlenburg I., Gelineck J., Jakobsen S.S., Soballe K. Does a titanium sleeve reduce the frequency of pseudotumors in metal-on-metal total hip arthroplasty at 5-7years follow-up? Orthop traumatol Surg Res. 2016;102:1035–1041. doi: 10.1016/j.otsr.2016.08.020. [DOI] [PubMed] [Google Scholar]
- 50.Beaule P.E., Kim P.R., Hamdi A., Fazekas A. A prospective metal ion study of large-head metal-on-metal bearing: a matched-pair analysis of hip resurfacing versus total hip replacement 5. Orthop Clin North Am. 2011;42:251–257. doi: 10.1016/j.ocl.2011.01.005. [DOI] [PubMed] [Google Scholar]
- 51.Garbuz D.S., Tanzer M., Greidanus N.V., Masri B.A., Duncan C.P. The John Charnley Award: metal-on-metal hip resurfacing versus large-diameter head metal-on-metal total hip arthroplasty: a randomized clinical trial 43. Clin Orthop Relat Res. 2010;468:318–325. doi: 10.1007/s11999-009-1029-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 52.Cooper H.J., Della Valle C.J., Berger R.A., Tetreault M., Paprosky W.G., Sporer S.M. Corrosion at the head-neck taper as a cause for adverse local tissue reactions after total hip arthroplasty. J Bone Joint Surg Am Vol. 2012;94:1655–1661. doi: 10.2106/JBJS.K.01352. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 53.Whitehouse M.R., Endo M., Zachara S., Nielsen T.O., Greidanus N.V., Masri B.A. Adverse local tissue reactions in metal-on-polyethylene total hip arthroplasty due to trunnion corrosion: the risk of misdiagnosis. J Bone Joint Surg. 2015;97-b:1024–1030. doi: 10.1302/0301-620X.97B8.34682. [DOI] [PubMed] [Google Scholar]
- 54.Scully W.F., Teeny S.M. Pseudotumor associated with metal-on-polyethylene total hip arthroplasty. Orthopedics. 2013;36:e666–e670. doi: 10.3928/01477447-20130426-33. [DOI] [PubMed] [Google Scholar]
- 55.Svensson O., Mathiesen E.B., Reinholt F.P., Blomgren G. Formation of a fulminant soft-tissue pseudotumor after uncemented hip arthroplasty. A case report. J Bone Joint Surg Am Vol. 1988;70:1238–1242. [PubMed] [Google Scholar]
- 56.Chang E.Y., McAnally J.L., Van Horne J.R., Statum S., Wolfson T., Gamst A. Metal-on-metal total hip arthroplasty: do symptoms correlate with MR imaging findings? Radiology. 2012;265:848–857. doi: 10.1148/radiol.12120852. [DOI] [PubMed] [Google Scholar]
- 57.Hart A.J., Satchithananda K., Liddle A.D., Sabah S.A., McRobbie D., Henckel J. Pseudotumors in association with well-functioning metal-on-metal hip prostheses: a case-control study using three-dimensional computed tomography and magnetic resonance imaging. JBone Joint SurgAm. 2012;94:317–325. doi: 10.2106/JBJS.J.01508. [DOI] [PubMed] [Google Scholar]
- 58.Hauptfleisch J., Pandit H., Grammatopoulos G., Gill H.S., Murray D.W., Ostlere S. A MRI classification of periprosthetic soft tissue masses (pseudotumours) associated with metal-on-metal resurfacing hip arthroplasty. Skeletal Radiol. 2012;41:149–155. doi: 10.1007/s00256-011-1329-6. [DOI] [PubMed] [Google Scholar]
- 59.Senden R. Book THA wear and activity. AHORSE Research Foundation; 2013. THA wear and activity. [Google Scholar]
- 60.Troiano R.P., Berrigan D., Dodd K.W., Masse L.C., Tilert T., McDowell M. Physical activity in the United States measured by accelerometer. Med Sci Sports Exerc. 2008;40:181–188. doi: 10.1249/mss.0b013e31815a51b3. [DOI] [PubMed] [Google Scholar]