Biomaterials 19 (1998) 1579 — 1586

Review of the biological response to a novel bone cement containing

poly(ethyl methacrylate) and n-butyl methacrylate
P.A. Revell!,*, M. Braden", M.A.R. Freeman#
! Department of Histopathology, Royal Free Hospital School of Medicine, Rowland Hill Street, London NW3 2PF, UK
" IRC in Biomedical Materials, Queen Mary & Westfield College, Mile End Road, London El 4NS, UK
# Bone & Joint Research Unit, Royal London Hospital, Whitechapel El 1BB, UK
Received 5 September 1995

Abstract

This review describes work published independently elsewhere in which the biological reactions to poly(ethyl methacrylate) n-butyl
methacrylate (PEMBMA) have been studied. This material has been compared throughout with conventional poly(methyl methac-
rylate) (PMMA). Butyl methacrylate monomer used in PEMBMA was slightly less toxic than methyl methacrylate monomer used in
PMMA when injected intraperitoneally in mice. No differences in cardiorespiratory effects were found between n-butyl and methyl
monomer infused intravenously into anaesthetized rabbits. The tissue reaction to the beaded polymers of poly(methyl methacrylate)
and poly(ethyl methacrylate) implanted subcutaneously was identical. The surface appearance of the two materials differed
significantly when viewed by scanning electron microscopy, showing a series of elevations resembling tightly packed spheres in the
case of PMMA, but a smooth surface with only occasional smooth elevations in the case of PEMBMA. Intramuscular implantation
showed more fibrous tissue and tissue damage in relation to PMMA cured in situ compared with PEMBMA and there was more bone
necrosis and a thicker fibrous tissue layer adjacent to PMMA than PEMBMA when cured intraosseously. ( 1998 Elsevier Science
Ltd. All rights reserved

Keywords: Bone cement; Review; Toxicity; Biological response; Implants

1. Introduction methacrylate (PEMBMA), having some improved mechan-

The biological disadvantages of conventional bone
cement, which is poly(methyl methacrylate) (PMMA), are
well established. This acrylic is known to cause some
death of bone at the site of implantation due to either the
heat of polymerization or the local effects of methyl
methacrylate monomer leaching out of the material as it
cures in situ [1, 2]. Other toxic effects at the time of
implantation involve distant organs, namely the heart
and lungs. Such cardiopulmonary changes have been
described in man and experimental animals, and are
thought to be mainly related to the effects of circulating
methyl methacrylate monomer [3—6], though air and fat
embolisms to the lung have also been implicated [7].
A novel bone cement, poly(ethyl methacrylate)/n-butyl
ical properties over this conventional PMMA has been
developed [8]. The purpose of this article is to review the
effects of PEMBMA on biological systems from a series
of previously reported experimental studies in animal
models.
Toxicity studies of a new bone cement material have to
include an evaluation of the monomer as well as the
cured polymer and the effects of the curing process in
vivo. The latter studies were performed by subcutaneous,
intramuscular and intraosseous implantation methods.
Details of the individual areas of study and results are
given below.
2. Toxicity of n-butyl methacrylate monomer compared
with methylmethacrylate monomer [9]

The monomer used in PEMBMA is n-butyl methac-

* Corresponding author. rylate which contains 2.5 vol% dimethyl p-toluidine.

0142-9612/98/$ — See front matter ( 1998 Elsevier Science Ltd. All rights reserved.
PII S 0 1 4 2 - 9 6 1 2 ( 9 7 ) 0 0 1 1 8 - X
1580 P.A. Revell et al. / Biomaterials 19 (1998) 1579—1586

While experiments to measure the lethal dose for 50% of

animals receiving the monomer (LD50 studies) may no
longer be considered necessary or appropriate, at the
time that this cement was being developed, it was
considered important to use this method. Accordingly,
n-butyl monomer with p-toluidine was injected intra-
peritoneally into Balb/C mice in groups of 20, after
a series of preliminary experiments to determine the
dose range on which to base the definitive experiments.
Over the dose range 1.0 to 2.0 ml Kg~1 body weight, the
LD50 for n-butyl methacrylate was found to be between
1.0 and 1.2 ml Kg~1 in two different experiments using
identical methods and group sizes, while that for methyl
methacrylate monomer was 1.2 ml Kg~1 in a single
study [9]. Large numbers of animals (20 per group) and
numerous different treatment groups were used in
these studies. Our finding differs from those of a previous
study of acrylic monomers in which the LD50 for n-butyl
methacrylate monomer was 1.66 ml Kg~1 while that
for methylacrylate monomer was 1.20 ml Kg~1. In Fig. 1. Median change in blood pressure in methyl methacrylate and
other words, our own results suggested that the n-butyl n-butyl methacrylate aminals at three different cumulative dose levels.
monomer was the same or slightly less toxic compared
with the methyl monomer, while that of others suggested
a small difference with the butyl monomer being less
toxic [10]. tent of the hypotensive response was dose-related at
One of the chief concerns in human implantation of doses of either methyl or butyl monomer over
bone cement is the cardiorespiratory effects of monomer 60 mg Kg~1 (Fig. 1), and these cardiorespiratory values
leaching from the material as it cures in situ at the time of did not return to normal, rather the rabbits developed
implantation. In order to study this, we compared the cardiac arrhythmias. Cumulative doses of 90 mg Kg~1
effects of methylmethacrylate monomer with those of were fatal for either monomer. No statistically significant
n-butyl methacrylate monomer on slow intravenous infu- difference using a non-parametric Wild—Wolfowitz runs
sion into anaesthetized New Zealand white rabbits, using test was found between these two monomers with respect
two different anaesthetic regimes because one agent to effects on the cardiovascular and respiratory systems
(Urethane) is known itself to have a depressant effect on in these tests [9]. It is known that conventional bone
cardiorespiratory function, while the other (Althesin) cements may cause hypotensive episodes during the im-
does not [9]. After anaesthetic induction, femoral and plantation of prosthetic joints [3—6], but our studies
jugular veins were catheterized and arterial and central suggest that the butyl monomer is no more dangerous in
venous pressures measured with calibrated electro- this regard than the methyl monomer. The levels of
manometers, d.c. amplifiers and chart recorders. Heart monomer administered in our study were similar to those
rate was monitored from the femoral artery trace while used by others in dogs for methyl methacrylate monomer
body temperature was measured with a rectal thermistor [3]. Allowing for species differences and making calcu-
and respiration rate and end-tidal pCO were taken from lations from data available in the literature about blood
2
the output of a CO analyser. Single injections of either levels of methyl methacrylate in man and dogs at the time
2
methyl or butyl methacrylate monomer produced car- of implantation [5, 11], we estimated that the dose we
diorespiratory changes which were indistinguishable in had administered intravenously to our rabbits was one
both nature and magnitude. For both monomers, there hundered times greater than the highest levels occurring
was increased frequency and decreased depth of respir- in man. We therefore concluded that n-butyl methac-
ation with an increased end-tidal pCO , increased central rylate monomer was no more toxic than conventional
2
venous pressure and transient fall in arterial blood pres- methyl methacrylate monomer [9].
sure. Each of the rabbits which received the Althesin
anaesthetic survived at least 1 h after a single injection at
a dose of 1 ml per animal given over 1 min for either 3. Effect of polymer powder in tissues [12]
monomer [9]. When cumulative doses of the monomer
were administered sequentially to Urethane-anaesthe- Occasionally there is incomplete mixing of polymer
tized rabbits, there was also arterial hypotension, raised powder and monomer so that separate particles of poly-
venous pressure and increased respiratory rate. The ex- mer are left in the tissues after the bone cement has cured
 P.A. Revell et al. / Biomaterials 19 (1998) 1579—1586
in situ at operation. To study the effects of the polymer
alone, the dry powder of polymer beads of PEMBMA
was inserted under direct vision into the flank of six
Sprague-Dawley rats in a subcutaneous position. Beaded
conventional methyl methacrylate polymer powder was
inserted in an identical way in six further rats. Samples of
the subcutaneous tissue were excised after six weeks and
examined by routine paraffin wax embedded histology.
No differences were observed in the cellular reaction to
the two types of polymer bead when the sections were
examined blindly. There were macrophages and foreign
body giant cells present in response to both materials
with no evidence of tissue necrosis or of polymorpho-
nuclear leucocytes or lymphocytes as evidence of acute or
chronic inflammation [12] (Fig. 2).
Fig. 2. Macrophage and giant cell response to the presence of beads of
polymer in the subcutaneous tissues, in the case of: (a) poly(methyl
methacrylate); (b) poly(ethyl methacrylate). There is no difference in the
histological features present. Bar"100 lm.
1581
4. Surface appearance of polymerized bone cements
by scanning electron microscopy (SEM) [12]
In order to examine the surface characteristics of
PMMA and PEMBMA, pre-cured spherical pellets
(5 mm diameter) (4.9 to 5.1 mm range) were mounted on
aluminimum stubs, gold sputter-coated in an atmosphere
of argon to a coating thickness of 40 lm then examined
in an ISI Alpha [9] scanning electron microscope. The
pellets were rolled on a glass surface into a spherical
shape from dough. Pellets prepared in an identical way
were also examined by SEM after intramuscular im-
plantation (see below). The surface of PMMA comprised
a series of rounded protruberances resembling tightly
packed spheres, with the diameter of individual beads
being up to 120 lm but with most measuring 70—80 lm.
The PEMBMA had a completely different appearance
showing a smooth surface with only occasional elev-
ations suggesting the presence of beads just beneath the
surface [12] (Fig. 3). The appearances of both materials
after implantation were identical with those for the
respective cements cured in vitro. The smoother surface
of PEMBMA is an inherent characteristic of this material
and results because the poly(ethyl methacrylate) bead-
ed particles dissolve almost completely in the n-butyl
methacrylate monomer before the onset of polymeri-
zation [12].
5. Intramuscular implantation of PMMA and PEMBMA
bone cements [12, 13]
Spherical pellets of precured PMMA and PEMBMA
bone cements were implanted by direct surgery into the
paraspinal musculature of Sprague-Dawley rats under
general anaesthetic. The diameter of the pellets was care-
fully controlled and varied between 4.9 and 5.1 mm.
Implants were measured for diameter at the time of
implantation with a caliper and only those within this
range were used. Pellets of identical size range were
prepared by mixing pre-aliquoted samples of PMMA or
PEMBMA (polymers and monomers) including
dimethyl p-toluidine in correct proportions but inserted
in dough form so that they cured in situ. Six samples of
each type were implanted in a protocol in which bilateral
implants were made (PMMA cured in situ, PMMA cured
in vitro, PEMBMA cured in situ, PEMBMA cured
in vitro). The implants were removed after 6 weeks, and
a blind histological assessment of the tissue reaction was
performed. There were numerous macrophages and
foreign body giant cells present associated with PMMA
cured in situ, with fewer such cells next to PMMA cured
in vitro (precured, hard pellet). The appearances of the
cellular reaction adjacent to PEMBMA, regardless of
whether it had been cured in vitro or in situ, resembled
that seen with the PMMA cured in vitro (Fig. 4). The
1582 P.A. Revell et al. / Biomaterials 19 (1998) 1579—1586
Fig. 3. Scanning electron micrographs of the surfaces of cured bone
cements: (a) poly(methyl methacrylate), showing the presence of numer-
ous tightly packed spheres and; (b) poly(ethyl methacrylate)/n-butyl
methacrylate, showing relatively smooth appearance with occasional
low profile protrusions. Bar"10 lm.
tissue—biomaterial interface had a smoother outline in
the case of PEMBMA than with PMMA. The PMMA
tissue interface had a booselated appearance. This obser-
vation is in keeping with the SEM appearances of the two
materials already noted above. A blind quantitative as-
sessment was made of various features (smooth surface,
thickness of fibrous capsule, macrophage covered sur-
face, giant cell covered surface) at the biomaterial—tissue
interface. Measurements of the thickness of the fibrous
tissue layer were made with a calibrated eyepiece
graticule while measurements of the features of the sur-
face interface were performed using a digitizing tablet
with a video-capture system linked to a microcomputer.
The results are shown in Table 1. Significantly less of the
interface with PMMA cured in situ was smooth com-
Fig. 4. Tissue adjacent to intramuscular implant of bone cement cured
in situ and left in place for 6 weeks: (a) poly(methyl methacrylate),
showing irregular outline of the cement surface, large number of cells
with macrophages and giant cells as well as the presence of inflammat-
ory cells extending into adjacent muscle; (b) poly(ethyl methacrylate)/n-
butyl methacrylate, by contrast, shows a smooth surface, absence of
macrophages and gaint cells and no inflammatory cells extending into
the muscle. Bar"100 lm.
pared with other samples (P(0.001, Student’s t-test)
and the thickness of the fibrous layer around significantly
less of the interface with PMMA cured in situ was
smooth compared with the other samples (P(0.001,
Student’s t-test) and the thickness of the fibrous tissue
layer around this in situ cured material was also signifi-
cantly thicker (P(0.001, Student’s t-test). More macro-
phages and giant cells were recruited to the surface of
PMMA cured in situ. No differences were noted between
 P.A. Revell et al. / Biomaterials 19 (1998) 1579—1586 1583

Table 1
Quantitative assessment of the features of the tissue interface, fibrous layer thickness and cellular reaction adjacent to implants of PMMA and
PEMBMA cement in paraspinal musculature of rats!

Cement implanted Percentage Thickness Macrophages Giant cells

smooth of fibrous (cells per mm (cells per mm
interface layer (lm) of surface) of surface)

PMMA, cured in situ 35.7 $ 16.3 85.2 $ 23.6 72.2 $ 23.4 3.20 $ 1.71
PMMA, cured in vitro 72.5 $ 11.3 28.1 $ 9.0 43.3 $ 14.0 0.30 $ 0.17
PEMBMA, cured in situ 73.3 $ 12.1 33.7 $ 9.9 39.2 $ 22.5 0.52 $ 0.37
PEMBMA, cured in vitro 70.8 $ 19.1 32.4 $ 8.8 23.5 $ 13.5 0.35 $ 0.24

! The thickness of the fibrous layer was measured with an eyepiece graticule; the surface measurements were made using computerized analysis and
digitization procedures on video-captured images.

the materials cured in vitro before insertion or between

these and PEMBMA cured in situ [12].

6. Intraosseous implantation of PMMA and PEMBMA

bone cements [14]

Apart from the generalized problem of cardio-respira-

tory depression, local difficulties with bone death occur
in relation to conventional PMMA. Such osteonecrosis is
thought to be due to the heat of polymerization of the
cement dough as it cures in situ [15—17]. In order to
study the osseous changes adjacent to PEMBMA cured
in situ, implants were made into lower femur of the dog
under Briertal anaesthesia by an intraarticular approach
and a hole drilled upwards between the femoral condyles
with a slow speed drill and water irrigation during the
procedure (Fig. 5). This hole, which was 5 mm in dia-
meter, was filled with conventional PMMA or
PEMBMA inserted as a dough to cure within the bone.
The joint and skin were closed with sutures. A total of 23
dogs was used and 30 implants placed intraosseously,
some animals receiving bilateral implants. Different ma-
terials were always used on the two sides. Preliminary
studies in two dogs showed that no differences in his-
tological appearance resulted after 3 weeks from PMMA
implantation when unilateral or bilateral (with
a PEMBMA contralateral) procedures were performed.
Animals were killed after 3, 6 and 12 weeks, so that there
were 3 PMMA implants and 4 PEMBMA implants at
3 weeks, 4 PMMA and 6 PEMBMA implants at 6 weeks
and 4 PMMA and 9 PEMBMA implants at 12 weeks.
The lower femur of the dogs was excised and decalcified
before paraffin wax embedded histological section and
staining with haematoxylin and eosin. Both bone ce-
ments dissolved out during the tissue processing through
the use of xylene which is part of the routine preparative
procedure. A total of 30 implants was made with tissue
from 11 PMMA and 19 PEMBMA sites examined his-
tologically without knowledge at the time of assessment
as to the type of material. Some local bone death was
Fig. 5. Lower end of rabbit femur cut longitudinally after exicision to
show hole drilled between femoral condyles and filled with bone ce-
ment, in this case poly(ethyl methacrylate)/n-butyl methacrylate.
observed adjacent to both materials at all periods of
implantation. Such a change is inevitable with any im-
plantation procedure involving the drilling of bone, al-
beit at slow speed, and insertion of a material which cures
in situ. By 3 weeks, there was already evidence of heal-
ing adjacent to both materials with new bone formation
(Fig. 6). This took the form of appositional new bone
growth on the surface of existing bone trabeculae and
was seen at all time periods (3, 6 and 12 weeks) after
implantation. The trabeculae on which this new bone
was formed showed more evidence of necrosis with
empty osteocyte lacunae where the implant was PMMA
than where it was PEMBMA (Figs. 6 and 7). Viable
original bone and bone marrow with no evidence
of an established thick layer of fibrous tissue were
seen where PEMBMA implants had been made (Figs. 6
and 7). Such an appearance was unusual with PMMA
which was separated from the surrounding marrow and
osseous tissues by a fibrous tissue membrane. A blind
1584 P.A. Revell et al. / Biomaterials 19 (1998) 1579—1586
Fig. 6. Tissue adjacent to bone cement implanted intraosseously to
cure in situ, examined 3 weeks after implantation: (a) poly(methyl
methacrylate) showing dead bone trabecula (empty osteocyte lacunae)
and necrotic fibrotic bone marrow (top right) and appositional new
bone formation around the trabecula; (b) poly(ethyl methacrylate)/n-
butyl methacrylate showing viable original bone trabecula (right) un-
dergoing some resorption, new appositional bone and woven bone
formation and viable marrow tissue up to the cement—tissue interface.
Bar"100 lm.
quantitative study was performed in which the thickness
of the fibrous layer after 12 weeks was measured in
relation to both types of implant together with the
amount of bone—implant contact and the proportion of
bone which showed evidence of necrosis within a 1 mm
distance of the implant. This assessment was performed
using eye-piece graticules in a Leica DM light micro-
scope at a magnification of ]200. The results are shown
in Table 2. They demonstrate that the presence of bone
Fig. 7. Tissue adjacent to bone cement implanted intraosseously to cure
in situ, examined 6 weeks after implantation: (a) poly(methyl meth-
acrylate) showing a dense fibrous tissue layer adjacent to the cement
(space, top left) and new bone formation outside this fibrous tissue
(bottom); (b) poly(ethyl methacrylate)/n-butyl methacrylate showing
viable original bone and vascular loose connective tissue contain-
ing a small amount of newly formed bone lying parallel with the
cement—tissue interface. Bar"100 lm.
necrosis within 1 mm of the cement was greater in the
neighbourhood of PMMA and that the maximum thick-
ness of the fibrous tissue layer was greater in relation to
this material than PEMBMA. Viable bone and bone
marrow were seen adjacent to both bone cements but
were present to a much greater extent in the case of
PEMBMA. In the human, the area of fibrosis may extend
for 3 to 5 mm from the bone—cement junction in the case
of PMMA [1, 18]. Examination of dog bones in this
 P.A. Revell et al. / Biomaterials 19 (1998) 1579—1586
Table 2
Quantitative results from the study of bone in relation to intraosseous
implants of PMMA and PEMBMA after 12 weeks!
Percentage of Percentage viable Thickness of fibrous
contact of bone bone within 1 mm reaction mm (range)
with cement of the implant
PMMA 13$8 49$24 2.4$1.9
(0.1—6.8)
PEMBMA 35$12 92$7 0.4$0.3
((0.1—1.7)
! The measurements were made with digitized video-captured images
using computerized analysis techniques.
study showed a similar appearance, though the extent of
damage was less marked. Whether the damage to bone is
due to the heat of polymerization [15—17] or leaching of
monomer [19—21] has been discussed by others. The
exotherm of the PEMBA, at 50 to 60°C, is much lower
than that of PMMA (80—90°C) [22]. Since the drilling
and reaming process was the same in all dogs, the differ-
ences in bone damage are likely to be due to these local
temperature differences. Further evidence for the biolo-
gical advantage of a lower exotherm in lessening local
tissue damage comes from the intramuscular implanta-
tion experiments described above. While a local effect
due to monomer cannot be excluded, the other studies
reported in this paper using n-butyl and methyl mono-
mers suggest that such toxicity is unlikely to be a signifi-
cant factor. It may be though that there are differences in
the amount of monomer released from the two cements
even when mixed in the correct proportions. There is
a large initial release of methyl monomer from PMMA
during polymerization that is six times greater than the
release of n-butyl monomer from PEMBMA [23]. Over-
all, intraosseous implantation studies have demonstrated
that PEMBMA has qualities preferable to PMMA in
terms of its biological effects.
7. Conclusions
This article summarizes previous work performed to
test the biological acceptability of a new bone cement
material, poly(ethyl methacrylate)/butyl methacrylate
(PEMBMA). Studies of the monomers used in this new
and the standard PMMA system have shown the n-butyl
monomer to be no more toxic than the methyl monomer.
There are no differences in the soft tissue reaction to the
two types of beaded polymer inserted as particles. Intra-
muscular and intraosseous implantation for comparison
of PEMBMA with PMMA show less local tissue damage
reaction and less inflammatory response (in the case of
muscle implantation) for PEMBMA. More new bone
formation and better survival of bone and bone marrow
1585
was observed with PEMBMA placed in bone. The results
confirm that the new PEMBMA material is biologically
suitable for implantation into bone in man. The mechan-
ical properties of this material have been reported pre-
viously [24].
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