Paper VI

SCIENTIFIC ARTICLE
Wear Particles and Osteolysis in Patients With
Total Wrist Arthroplasty
Michel E. H. Boeckstyns, MD, Anders Toxvaerd, MD, Manjula Bansal, MD, Lars Soelberg Vadstrup, MD
Purpose To determine whether the amount of polyethylene debris in the interphase tissue
between prosthesis and bone in patients with total wrist arthroplasty correlated with the degree
of periprosthetic osteolysis (PPO); and to investigate the occurrence of metal particles in the
periprosthetic tissue, the level of chrome and cobalt ions in the blood, and the possible role of
infectious or rheumatoid activity in the development of PPO.
Methods Biopsies were taken from the implantebone interphase in 13 consecutive patients
with total wrist arthroplasty and with at least 3 years’ follow-up. Serial annual radiographs
were performed prospectively for the evaluation of PPO. We collected blood samples for
white blood cell count, C-reactive protein, and metallic ion level.
Results A radiolucent zone of greater than 2 mm was observed juxta-articular to the radial
component in 4 patients and at the carpal component in 3. The magnitude of the radiolucent
zone tended to level out over time. We observed subsidence of the implant in 3 patients on the
carpal side and in none on the radial side. The amount of polyethylene and metallic debris was
generally small and did not correlate with the width of the radiolucent zone. The blood levels of
chrome and cobalt ions were normal. There was no evidence of infectious or rheumatoid activity.
Conclusions Polyethylene wear has been accepted as a major cause of osteolysis in total hip
arthroplasty, and metallic debris has also been cited to be an underlying cause. However,
our hypothesis that polyethylene debris correlated with the degree of PPO could not be
confirmed. Also, metallic debris and infectious or rheumatoid activity did not correlate
with PPO. (J Hand Surg Am. 2014;39(12):2396e2404. Copyright Ó 2014 by the American
Society for Surgery of the Hand. All rights reserved.)
Type of study/level of evidence Prognostic I.
Key words Wrist arthroplasty, osteolysis, histopathology, interphase.
P
ERIPROSTHETIC OSTEOLYSIS (PPO) is a biological
process of bone resorption seen as radiolucent
lines or areas on radiographs. Polyethylene wear
has been accepted as a major cause of osteolysis in
total hip arthroplasty. Particles, which occur because of
abrasive wear, are considered to stimulate a foreign
body response resulting in bone loss mainly mediated
by macrophages that lead through complex cellular
interactions to the recruitment and activation of
osteoclasts.1e3 Metallic debris has also been cited as an
underlying cause, and abnormal chrome (Cr) and cobalt
(Co) levels in blood can be found in patients with metalon-metal total hip arthroplasty.4e7 Osteolysis may be
silent, and loosening of the implants may be incomplete
From the Clinic of Hand Surgery, Gentofte Hospital, and the Department of Pathology, Herlev
Hospital, University of Copenhagen, Denmark; and the Department of Pathology, Hospital for
Special Surgery, New York, NY.
Corresponding author: Michel E. H. Boeckstyns, MD, Clinic of Hand Surgery, Gentofte
Hospital, University of Copenhagen, Niels Andersens Vej 65, 2900 Hellerup, Denmark;
e-mail: mibo@dadlnet.dk.
Received for publication May 14, 2014; accepted in revised form July 23, 2014.
0363-5023/14/3912-0007$36.00/0
http://dx.doi.org/10.1016/j.jhsa.2014.07.046
M.E.H.B. received support from Gentofte Hospital, Clinic for Hand Surgery.
No benefits in any form have been received or will be received related directly or indirectly
to the subject of this article.
2396
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Ó 2014 ASSH
r
Published by Elsevier, Inc. All rights reserved.
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WEAR PARTICLES AND OSTEOLYSIS AFTER TOTAL WRIST ARTHROPLASTY
with the implant remaining steadily anchored in the
bone.3
Periprosthetic osteolysis with or without complete
loosening occurs in other joints as well and has been
frequently reported after total wrist arthroplasty
(TWA).8e13 Since 2003, we have been using the
Re-motion TWA (SBI, Inc, Morrisville, PA) as an
alternative to total wrist arthrodesis for the reconstruction of severely destroyed and painful wrists.
This implant contains an articular component made of
conventional polyethylene that articulates with a
metallic CreCo component.
Our hypothesis was that the occurrence of polyethylene debris in the interphase tissue between
prosthesis or cement and bone was correlated with
the degree of PPO. A secondary aim of the study was
to investigate the occurrence of metal particles in the
periprosthetic tissue, the level of Cr and Co ions in
the blood of patients, and the possible role of infectious or rheumatoid activity in the development of
PPO.
MATERIALS AND METHODS
Ethics
The study conformed to the ethical guidelines of the
1975 Helsinki Declaration. The Scientific Ethical
Committee for the Capital Region in Denmark
approved the study (Study H-2-2013-032). We obtained written informed consent from all patients.
Selection of patients
Re-motion TWA is an elliptical ball and socket
design consisting of radial and carpal CreCo components that are titanium coated and an intercalated
polyethylene ball. It mainly articulates with the radial
component in an unconstrained link but also permits
a rotational articulation of 20 with the carpal plate. It
requires minimal bone resection and is designed to
act much like a surface replacement. The carpal plate
is fixated to the carpus by its stem and 2 screws. The
polyethylene in the carpal ball is of a conventional,
not highly cross-linked type. All patients in whom a
Re-motion TWA was implanted at Gentofte Hospital,
Denmark, between September 2003 and April 2010
(21 patients) were eligible for this study.
We excluded wrists that had been revised to a new
TWA or arthrodesis (3 patients), those who were
unable to participate for geographical reasons (2 patients), those who had not given informed consent
(1 patient), those with conditions that contraindicated
the surgical procedure (one patient: recent ipsilateral
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TABLE 1.
Included
Demographics of the 13 Patients
Age, y (mean [range])
Sex
Mean follow-up, y
(mean [range])
68 (53e87)
2 male, 11 female
6 (3e10)
Diagnosis
Rheumatoid arthritis
6
Idiopathic osteoarthritis
4
Posttraumatic arthritis
3
Fixation technique
2 cemented, 11 not cemented*
*Cemented fixation was used when the bone was considered too
fragile to support uncemented implant components.
shoulder fracture), and those who were already
included with the contralateral wrist (one patient).
Thus, 13 patients were included. Table 1 shows the
demographics. We obtained tissue samples from the
implantebone or implantecementebone interphase,
collected blood samples, obtained plain x-ray examinations, and updated the clinical status in June 2013.
Surgical procedure
We used Bier block for anesthesia, made a 2- to 3-cm
straight incision in the existing dorsal surgical scar,
and approached the dorsal wrist capsule between the
third and fourth extensor compartments. Through
windows in the capsule we collected samples from the
soft tissue surrounding the implant for bacteriological
cultures. From the dorsal interphase area between the
radial component and the radius and from the interphase area between the carpal plate and the carpus, we
collected tissue samples for histopathological examination. In one patient we also collected tissue under an
ulnar head component; but to avoid a potential confounding influence, we did not include this in the analyses aimed at testing our hypothesis. We closed the
wound with resorbable sutures in the capsule and
nonresorbable sutures in the skin. Patients were
allowed to mobilize the wrist without delay.
Histopathological examination
After fixation in 10% buffered formaldehyde all tissue
samples were sectioned and embedded in paraffin.
Sections cut at 2 mm thickness were prepared, stained
with hematoxylineeosin, and examined by light and
polarized microscopy. The amount of foreign body
particles was graded semi-quantitatively from 0 to 3, in
which 0 represented no particles; 1, particles present
but hard to find; 2, no problem in identifying particles;
and 3, a marked amount of particles as seen on
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WEAR PARTICLES AND OSTEOLYSIS AFTER TOTAL WRIST ARTHROPLASTY
high-field magnification. Two pathologists (AT and
MBa) blinded to the study protocol, who had experience in examining implantebone interphases,
reviewed the biopsies independently; after a general
common discussion, they performed an independent
second look examination. The reliability (ie, agreement between the 2 investigators) was assessed.
Radiology
According to our protocol for TWA, plain radiographs were obtained within 6 weeks after the index
operation, then 6 months later, and annually thereafter. If the last of these radiographs were older than
3 months, new radiographs were obtained in view of
the present study. Two senior hand surgeons (MBo
and LSV), who were blinded with respect to the
clinical and the histological findings, examined the
radiographs independently. On all serial posteroanterior radiographs, we measured the width of the
radiolucent area (if present) at selected spots (Fig. 1)
and calculated the mean of the width at spots 1/2/3,
4/5, 6/7/8, and 9/10 (expressed in millimeters). We
correlated these mean values with the histopathological, clinical, and serological findings. Furthermore, we established the evolution of radiolucency in
function of time in the individual patients. To evaluate angulation and subsidence, we measured the
angle between the radial component and the radial
diaphysis and the angle between the carpal component and the third metacarpal. We also measured the
distance from the tip of the radial component to the
tip of the radial styloid and the distance from the tip
of the central carpal peg to the third carpometacarpal
joint on all radiographs. The digitalized measurement
systems were provided by Sectra’s IDS5/web (Sectra
AB, Linköbing, Sweden). We considered a progressive and consistent change of distances from the first
postoperative to the latest radiograph of 3 mm or
greater as indicating subsidence and a corresponding
change of angulation of 5 or greater as indicating
tilting of the implants.14 The inter-observer reliability
of the measurements was also calculated.
Bacteriology
Bacteriological examination of the samples included
direct microscopy and aerobic as well as anaerobic
cultures.
Blood analyses
We determined C-reactive protein values and
white blood cell count to evaluate possible ongoing
infection. We also measured the concentration of
Cr and Co in whole blood according to the EPA
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FIGURE 1: Spots for measurement of the width of radiolucency
on serial posteroanterior radiographs. In this example, a small
radiolucent area is visible at spot 4 (maximal width, 1.4 mm).
200.7þ8-ICP/AES/SFMS method (Swedish Board
for Accreditation and Conformity Assessment, Borås,
Sweden), expressed as micrograms per liter.
Clinical examination
Patients expressed the general level of wrist pain on a
visual analog scale (0e100) with 0 indicating no
pain and 100 indicating maximal pain. We recorded
grip strength in kilograms and used the Quicke
Disabilities of the Arm, Shoulder, and Hand questionnaire as a validated outcomes measure.
Statistics
For correlations of values on interval scales, we used
Pearson correlation coefficient and for values on
ordinal scales, Spearman rho correlation coefficient.
To evaluate the reliability of the radiological measurements, we used Pearson correlation coefficient and
the intra-class coefficient (ICC3, single, fixed raters).15
We considered correlation coefficients between 0.8
and 1.0 to indicate a very strong correlation, between
0.6 and 0.79 a strong correlation, between 0.4 and 0.59
a moderate correlation, between 0.2 and 0.39 a weak
correlation, and between 0.0 and 0.19 a very weak or
absent correlation. To evaluate the histopathological
findings, we used Cohen kappa, in which values less
than 0.40 indicated poor agreement, 0.40 to 0.75 fair
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WEAR PARTICLES AND OSTEOLYSIS AFTER TOTAL WRIST ARTHROPLASTY
TABLE 2.
Interobserver Reliability of Measurements on Serial Radiographs
Measurements per
Observer, n
Pearson Correlation
Coefficient
Intra-class
Coefficient
Width of radiolucent zone at all spots (IeX)
820
0.85
0.85
Width of radiolucent zone at spots 4 and 5
164
0.81
0.81
Width of radiolucent zone at spots 9 and 10
164
0.81
0.80
Tilt of radial component
78
0.96
0.96
Subsidence of radial component
78
0.90
0.89
Tilt of carpal component
78
0.87
0.87
Subsidence of carpal component
78
0.98
0.98
FIGURE 2: Evolution of radiolucency. Each graph represents an individual patient. A Mean width at zones 4 and 5. B Mean of width at
zones 9 and 10.
to good agreement, and greater than 0.75 excellent
agreement.
We calculated that the required sample size to
reveal strong correlations (r ¼ 0.7) was 11 with a
power of 0.8 and a ¼ .05.
RESULTS
Complications
There were no complications related to harvesting of
biopsies in terms of infection, pain, or deterioration of
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function. Surgical wounds healed uneventfully within
2 weeks in all patients.
Radiology
Reliability of the measurements was very strong
(Table 2), and we used the measurements of the senior author (MBo) for further analyses. Radiolucency
was not seen in zones 1 to 3 and only in 2 patients
in zones 6 to 8 (0.3 and 0.4 mm, respectively). Some
degree of radiolucency was seen in 10 patients in
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WEAR PARTICLES AND OSTEOLYSIS AFTER TOTAL WRIST ARTHROPLASTY
FIGURE 3: Radiographs in a patient undergoing total wrist arthroplasty. A Two weeks after surgery. The peg penetrates the third
metacarpal, which does not comply with usual recommendations but resulted from an unusually large carpal resection. B Four years after
the operation. A large area of periprosthetic osteolysis has developed under the radial component. The mean width of radiolucency was
8.5 mm at spots 4 and 5. No radiolucency at spots 1, 2, or 3. Osteolysis is also present under the carpal plate and around the screws and
central peg. The carpal component has not subsided since surgery. C Computed tomography scan. The radiolucent lines seen at zone 2
and 3are artifacts caused by the imaging software. Bone condensation is present at the tip of the radial component where load is
transmitted maximally from implant to bone.
TABLE 3. Reliability of Histological Findings
(Agreement Between 2 Pathologists)
Findings
Necrotic tissue
k
0.68
Metal particles
0.59
Polyethylene debris
0.78
Preponderance of macrophages
compared with lymphocytes
1.00
Foreign body reaction
0.74
zone 4 to 5 (Fig. 2). In 6 of these, the width remained
less than 2 mm throughout the observation period.
In 3 patients it increased initially to between 3 and
4 mm and then stabilized. In one patient it increased
rapidly but seemed to stabilize between 8 and 9 mm
after 4 years (Fig. 3). In zones 9 to 10 radiolucency
was seen in 7 patients (Fig. 2). In 4 of these the width
remained less than 1 mm. In 3 patients it increased to
between 3 and 4 mm. There was no evidence of
radial component loosening in any patient. In 3 patients subsidence of the carpal component was
evident. None of the cemented components had
subsided.
Histopathology
We harvested 13 samples at the radial component, 10 at
the carpal component, and 1 at a metallic ulnar head
implant. Table 3 shows the interobserver agreement
of the histological findings. Foreign body giant cell
J Hand Surg Am.
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reaction was a common finding, encountered by at least
one of the pathologists in 15 of the 24 specimens.
Macrophages were predominant compared with lymphocytes in 22 specimens. Necrotic tissue was seen in 17.
Polyethylene debris was detected in 17 specimens
by both investigators and in another 2 specimens
by at least one investigator (Fig. 4). In 11 of these,
the polyethylene particles were sparse and small
or minute. No marked amount of particles was
encountered in any case. In 5 cases no polyethylene
was identified by either of the investigators (Fig. 4).
The amount of polyethylene at the radial component
correlated very weakly or not at all with the width
of radiolucency according to both pathologists
(Spearman r, e0.16 and 0.18, respectively) (Fig. 5).
On the carpal side, the correlation was negative
(Spearman r, e0.55 and -0.69 respectively) (Fig. 6).
The same applied to the metallic particles (Fig. 4):
Spearman r ¼ e0.26 and 0.12, respectively, on the
radial side and e0.18 and e0.26, respectively, on the
carpal side.
Blood analyses
Mean blood level of Cr was 0.264 mg/L (SD, 0.384)
and of Co 0.253 mg/L (SD, 0.275). There was no
correlation between the blood level of Cr and the
width of the radiolucent zones 4 to 5 and 9 to 10 and
a reversed weak or moderate correlation for the blood
level of Co.
White blood cell count was normal in all patients,
and the C-reactive protein level was normal in all but
one patient.
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WEAR PARTICLES AND OSTEOLYSIS AFTER TOTAL WRIST ARTHROPLASTY
2401
FIGURE 4: Examples of histology. A Polarized light microscopy (x200 magnification). Polyethylene fragments engulfed by multinucleated foreign body giant cells (arrows), semi-quantitatively estimated as 2 on a scale of 0 to 3 for the amount of foreign body
particles. B Polarized light microscopy ( 100 magnification). No polyethylene fragments or particles could be demonstrated in this
specimen. C Hematoxylineeosin staining ( 200 magnification). Only sparse metal particles were demonstrable (arrows).
Bacteriology
All samples were negative with respect to direct microscopy and culture for bacteria.
Clinical findings
QuickeDisabilities of the Arm, Shoulder, and Hand
and the visual analog scale scores and grip strength
did not correlate with radiolucency (all correlation
coefficients lower than 0.10).
DISCUSSION
Periprosthetic osteolysis has been reported frequently
after TWA.16 In a series of Biaxial implants (DePuy
Orthopedics, Inc., Warsaw, IN), a periprosthetic
radiolucent zone of at least 2 mm was found in 12 of
32 cases (mean follow-up, 6 y).8 In a Re-motion series, periprosthetic radiolucency more than 2 mm in
width was found in 16 of 44 cases on the radial side
and in 7 on the carpal side.17 In a series of cemented
Universal I TWA (KMI Inc., San Diego, CA) in
rheumatoid patients, 9 of 19 patients seen at followup of more than 5 years after the operation had received
revisions because of loosening of the carpal component.12 Among the remaining ten, 3 had radiographic
subsidence and/or osteolysis. The Biaxial, Re-motion,
and Universal TWA are metal-on-polyethylene implants but similar PPO has also been demonstrated in
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metal-on-metal TWA18 and even in metallic single
component implants such as ulnar head replacement
devices.19
The histology of PPO has been investigated in
other joints. Kepler et al20 studied 52 patients who
underwent revision total shoulder arthroplasty at a
mean of 4.5 years after the index surgery. Ten patients (19%) had radiographic evidence of osteolysis
at the glenoid component. Histological specimens
taken at the time of revision surgery demonstrated no
significant differences between patients with or
without osteolysis with respect to the presence of
metallic, polyethylene, or cement debris particles or
with the presence of inflammatory reactions. Dalat
et al21 revised 25 total ankle arthroplasties. Radiographically, all patients showed tibial and talar
osteolytic lesions, and in 25% the implant had
collapsed into the osteolytic cysts. Histological examination of the biopsies showed granulomatous
response associated with a foreign body giant cell
reaction in all cases. The cysts contained necrotic
material. Implant material, primarily polyethylene,
was identified in 95% of the specimens and metallic
debris in 60% of patients.
Generally, it has been hypothesized that the
macrophage phagocytosis of particulate debris from
component abrasive and adhesive wear activates
the macrophages and other inflammatory cells with
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WEAR PARTICLES AND OSTEOLYSIS AFTER TOTAL WRIST ARTHROPLASTY
FIGURE 5: Scatterplot showing the width of radiolucency in
zones 4 and 5 versus the amount of polyethylene fragments in the
samples taken at the interphase between the radial component and
the radius: A According to pathologist AT. B According to
pathologist MBa.
FIGURE 6: Scatterplot showing the width of radiolucency in
zones 9 and 10 versus the amount of polyethylene fragments in
the samples taken at the interphase between the carpal component
and the carpal: A According to pathologist AT. B According to
pathologist MBa.
cytokine release that in turn activate the osteoclasts, but
other possible mechanisms have been proposed. According to Skoglund and Aspenberg,22 the much less
studied osteolytic effects of pressure could be far more
important, and stress shielding is also considered a
potent stimulator of bone resorption.19,23,24
The main strength of our study is that it investigated a consecutive group of patients with TWA,
regardless of their clinical or radiological status,
and that we followed these patients prospectively
with annual clinical and radiographical examinations. Another strength of this study was that 2
pathologists investigated all specimens independently and in a blinded manner. Our results confirm
that the histopathological findings may be subject to
differences of interpretation and interobserver variation that deserve consideration and discussion.
Thus, the relative disagreement between the 2 pathologists concerning the presence of metallic particles may be because in several cases the metallic
particles were minute and sparse and on occasion
could be confused with corrosion products. Generally, however, interobserver agreement was good to
excellent.
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WEAR PARTICLES AND OSTEOLYSIS AFTER TOTAL WRIST ARTHROPLASTY
The hypothesis in the current study was that the
presence and severity of PPO correlated with the
presence and degree of polyethylene and metallic
debris. We showed that this was not the case.
Moreover, foreign body giant cell reaction was seen
as frequently in patients with no or minimal PPO as
in those with pronounced PPO. The patient with the
most marked osteolytic lesion at the radial component
(Fig. 3) had no detectable polyethylene debris in the
collected specimen at all according to one pathologist
and only minimal amounts according to the other.
Only one of the pathologists considered a foreign
body giant cell reaction to be present in this specimen, whereas both pathologists considered the
presence of metallic particles minimal or very small.
In most cases PPO was associated with a low
amount of metallic debris. Also, metallic wear did not
cause elevated levels of metallic ions in the blood
samples. The values were far below the proposed
acceptable upper limits of 2.56 mg/L for Cr and 2.02
mg/L for Co in whole blood, based on the studies by
Hart et al.25 According to Trace Elements LaboratoryeLondon Health Sciences Centre, the reference
values for Cr in whole blood is 0.40 to 1.60 mg/L and
for Co, 0.032 to 0.290 mg/L . The only patient with a
Co value exceeding this reference had a bilateral
TWA and a bilateral total knee arthroplasty. In a
systematic study of the literature concerning Cr and
Co ion concentrations in blood and serum after
various types of metal-on-metal hip arthroplasties,
Jantzen et al26 found that the average Cr concentration ranged between 0.5 and 2.5 mg/L in blood. For
Co, the range was 0.7 to 3.4 mg/L.
Our series was underpowered because of the small
number of cases; conversely, however, it represents a
broad spectrum of histopathological findings
(amounts of debris) as well as radiological findings
(width of radiolucency) and the lack of correlations
was unequivocal. Moreover, the sample size was
reasonable according to our calculations. Our evaluation of the osteolytic areas may not represent the
volume of bone resorption correctly because we used
a 2-dimensional surrogate for a 3-dimensional space.
Nevertheless, our method was highly reproducible
and corresponded to the method described by Cobb
et al14 and Takwale et al.10 None of the radial components collapsed into the osteolytic area, which
consequently was intact for evaluation.
The PPO tended to level out in time and rarely
caused gross loosening of the components. In light of
the lack of correlation between particulate debris and
PPO and the absence of rheumatoid or infectious
activity, we suggest that the PPO we describe can be
J Hand Surg Am.
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2403
at least partially attributed to stress shielding of the
bony structures by the implants. The fact that bone
resorption occurred at the edges of the components
nearest to the joint, where load is transmitted through
the implant components, is consistent with this hypothesis. There is a need for further investigation,
however, including radiostereographical methods and
serial focal bone mineral density measurements. For
the time being, we recommend close and continued
observation of patients with marked asymptomatic
PPO. Bisphosphonates, denosumab, strontium, ranelate, and parathyroid hormone have been reported as
possible treatment agents with regard to maintaining
more periprosthetic bone mineral density, but clinical
documentation is limited.27
We find that there is currently no need to change
conventional polyethylene in the Re-motion implant
to the more resistant highly cross-linked polyethylene
because the occurrence of polyethylene debris was
low.
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