Friction ISSN 2223-7690

https://doi.org/10.1007/s40544-023-0822-y CN 10-1237/TH
RESEARCH ARTICLE

Experimental study on boundary lubricity of superficial area of

articular cartilage and synovial fluid
Wenxiao LI1,*, Takehiro MORITA1,2, Yoshinori SAWAE1,2,3
1
Departure of Mechanical Engineering, Kyushu University, Fukuoka 8190395, Japan
2
International Institute for Carton-Neutral Energy Research, Kyushu University, Fukuoka 8190395, Japan
3
Advanced Research Center for Biomechanics, Kyushu University, Fukuoka 8190395, Japan
Received: 08 March 2023 / Revised: 09 August 2023 / Accepted: 30 August 2023
© The author(s) 2023.

Abstract: The boundary lubrication mechanism at the articulating surface of natural synovial joints has been
the subject of much discussion in tribology. In this study, to elucidate the lubricating function of the superficial
area of articular cartilage and synovial fluid (SF), cartilage specimens were processed with four different
treatments: gentle and severe washing with detergent, incubation in NaCl solution, and trypsin digestion to
selectively remove certain constituents from the cartilage surface. Subsequently, the frictional characteristics
were examined in phosphate-buffered saline (PBS) and SF against glass. Angularly reciprocating sliding tests
with a spherical glass probe and square articular cartilage specimens were performed at low contact loads in
the mN range to extract the frictional behavior in the superficial area of the cartilage specimens. Meanwhile,
the cartilage surface was observed to confirm the effects of treatments on the morphology of the cartilage
surface using a fluorescence microscope and water-immersion methods. The coefficient of friction (COF) of the
prepared cartilage specimens was varied from 0.05 to over 0.3 in PBS. However, a certain group of cartilage
specimens exhibited a low COF of less than 0.1 with limited variation. For the low COF group of specimens, all
four treatments increased the COF in PBS to different extents, and fluorescence microscopy revealed that the
integrity of the cartilage surface was deteriorated by treatments. This means that the intact cartilage surface had
lubricating constituents to maintain low friction, and the removal of such constituents resulted in the loss of the
intrinsic boundary lubricity of the cartilage surface. The variation in the COF of the cartilage specimens was
suppressed in SF because it had a clear boundary lubrication effect on the cartilage surface. The lubricating
effect of SF could be confirmed even after degenerative treatment.

Keywords: articular cartilage; synovial fluid; the uppermost superficial layer; boundary lubrication

1 Introduction covered with an acellular boundary layer, called

The articular surfaces of natural synovial joints
are covered with compliant and highly hydrated
articular cartilage and lubricated with synovial fluid
(SF) [1]. Since its structure and composition changes
continuously from the bottom to the surface, articular
cartilage can be divided into four zones: the calcified
cartilage zone, the deep zone, the middle zone, and
the superficial zone [2, 3]. The superficial zone is
the uppermost superficial surface layer or lamina
splendens [4, 5]. The lamina splendens is a continuous
biomembrane structure composed of a phospholipid
bilayer, proteins, glycoproteins, and proteoglycan
[4, 6, 7]. SF secreted from the synovial membrane
contains many biological macromolecules, including
hyaluronic acid (HA), phospholipids, albumin,
globulin, lubricin, and glycosaminoglycans [8–11].
The extremely smooth nature of synovial joint

* Corresponding author: Wenxiao LI, E-mail: li.wenxiao.345@s.kyushu-u.ac.jp

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movements, with the Ra of the cartilage measured in
the range of 1 μm, has attracted significant interest in
tribology [12]. In the past several decades, numerous
studies have been conducted to unravel the detailed
mechanisms of synovial joint lubrication, such as
boundary [13, 14], multimode [15], elastohydrodynamic
[16, 17], hydrodynamic [18], weeping [19], boosted
[20], and biphasic lubrication mechanisms [21, 22].
In 1959, McCutchen [19] reported that the interstitial
fluid contained in porous articular cartilage flows
through the pores, and the pressurized fluid supports
most of the applied load; this is called weeping
lubrication. Ten years later, the lubrication effect
of this model was demonstrated by Mow et al. [23]
through a complicated mathematical analysis. Walker’s
boosted lubrication [20] hypothesis states that in
contrast to weeping lubrication, small molecular
weight solutes, such as water, in the SF flow into the
porous cartilage, and large macromolecular weight
solutes, such as HA, are retained on the cartilage
surface as boundary lubricants. Subsequently, the
biphasic lubrication mechanism was elucidated.
Ateshian et al. [21, 22, 24] proposed and validated a
boundary friction model based on biphasic lubrication
to predict the friction behavior of articular cartilage,
including its time-, velocity-, and load-dependent
responses. Mixed and multimode lubrication [4, 15]
have also been developed.
Owing to the low relative motion speed and large
applied load between the articulating surfaces, some
scientists believe that the lubrication mechanism
between cartilage surfaces is boundary lubrication, as
supported by experimental evidence. In 1959, Charnley
[13] designed a pendulum machine with a cadaver
joint as the fulcrum and found that the friction
resistance was independent of the speed. In 1968,
Linn et al. [25] demonstrated that adding trypsin to
SF significantly increased the coefficient of friction
(COF), whereas the addition of hyaluronidase had a
limited effect on COF.
Over the past few decades, several studies have
focused on the boundary lubrication mechanism of
the molecular boundary layer coating the superficial
area of the cartilage surface. Ishikawa et al. [26]
showed that the proteoglycan gel layer on the cartilage
surface contributes to low-friction characteristics.
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After absorbing water, proteoglycan aggregates bind
with hyaluronic acid, which in turn adheres to the
collagen network located on the surface of the
cartilage. The contact load between natural synovial
joint surfaces is supported to some extent by water
molecules, which involves osmotic pressure. Lin et al.
[27] introduced a complex paradigm of hydration
lubrication, where phospholipid tails adhere to one
another while their hydrated phosphocholine heads
create a low-shear sliding interface on the cartilage
surface through hydration lubrication.
Some studies have focused on the individual
influence of SF components and investigated the
constituents that are responsible for the ultra-low
friction of articular cartilage. Murakami et al. [28],
using a reciprocating tester, showed the COF between
a lower reciprocating flat glass plate and a stationary
upper cartilage specimen under macroscale load
conditions and clarified the effect of synovial
constituents on the lubrication mechanism. Bonnevie
et al. [29], using a custom-built tribometer, reported
that the COF between cartilage and a polished glass
plate was significantly reduced by the addition of
lubricin to a HA solution. However, macroscopic
friction involves the interaction of many microscale
factors over a large contact area. Therefore, the
influence of some small factors on the friction behavior
will be ignored, such as the local damage of the
initial cartilage surface and molecular structure. It is
difficult to understand the effects of unique factors
on friction behavior. These friction measurement
results contain interstitial fluid effects owing to
the biphasic nature of the cartilage. Therefore, the
effect of SF constituents cannot be isolated from these
results.
Seror et al. [30] used atomic force microscopy to
demonstrate that the addition of lipids to HA-coated
mica resulted in a low COF (0.001) at pressure >100 atm.
Chang et al. [31] found that friction between
hydrophobic surfaces significantly reduced because
of the addition of lubricin, whereas friction between
hydrophilic surfaces slightly increased. The friction
between the model surfaces with a mixture of lubricin
and HA solutions did not change. It is believed that
the microscale contact force is too small to pressurize
the cartilage. Therefore, microscale contact provides
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a unique perspective for studying cartilage boundary
friction behavior without fluid pressurization.
In boundary lubrication, there is a growing realization
that the synergistic effects of the constituents of the
superficial area of the cartilage surface and SF play a
predominant role in the COF. Recently, Jahn et al. [32]
proposed the structure of the cartilage boundary
lubricant layer to explain the effects of the constituents
of the cartilage surface and SF on the friction behavior.
In this mechanism, the hydrated lubrication product
near the phosphocholine head of the phospholipid
absorbs the water molecule and supports the contact
load. This indicates that lubricin plays a key role in
the boundary lubrication of the articular cartilage
and in linking HA to the cartilage. However, this
is simply an experiment on a mica surface, whose
physical characteristics are different from those of
natural articular cartilage.
As mentioned above, the boundary lubrication
mechanism of natural synovial joints, particularly the
lubricating functions existing in the superficial area
of the cartilage surface and SF, is still subject to active
debate. Because the purpose of this study was to
experimentally identify the boundary lubricity of
molecular layers on the articular cartilage surface, the
friction behavior of the surface was evaluated at
extremely low contact loads to minimize contributions
from the bulk of the cartilage tissue. Four different
degenerative treatments were used to remove specific
lubricating elements from the cartilage surface and
elucidate their lubricating function. We also examined
the friction behavior of treated and untreated cartilage
specimens under SF lubrication to elucidate the
synergistic effect of the lubricating elements existing
in the superficial area of the articular cartilage and SF
constituents.
2 Materials and methods
2.1 Cartilage specimen preparation and degenerative
treatments
Cartilage specimens were prepared from fresh bovine
metacarpal-phalangeal joints, from animals that were
approximately 20 months, obtained from a local
abattoir within 24 h of sacrifice. Using a micro cutter
(MC-201, MARUTO, Japan), the osteochondral block
3
was harvested from the proximal end of the middle
phalanx and shaped into an 8 × 8 mm square plate
specimen with a thickness of 2 mm, consisting of
roughly 1-mm thick cartilage tissue and underlying
subchondral bone. All the specimens were carefully
prepared to prevent damage to the cartilage surface.
The surfaces of the prepared plate specimens were
observed by the naked eye, and those without
fissures or chondral defects were selected and used
for sliding tests.
In this study, four different degenerative treatments
for articular cartilage were selected based on a literature
survey and were employed to remove specific
lubricating elements from the cartilage surface. A
solution of 10% (v/v) detergent (Triton-X-100) was used
to remove adsorbed lipids and protein molecules
from the cartilage surface [15, 33, 34]. The first group
of cartilage specimens, called the gentle-wash group,
was gently washed with detergent solution for 30 min
using a tube mixer. The second group of cartilage
specimens was also washed with the detergent solution
for 30 min; however, in this case, it was washed
intensively using an ultrasonic cleaner and was referred
to as the severe wash group. These cartilage specimens
were subsequently rinsed with phosphate-buffered
saline (PBS) three times and stored in PBS at room
temperature until the sliding experiment. The third
group, called the NaCl group, was immersed in a 1.5 M
NaCl solution for 20 min, rinsed three times, and
re-equilibrated in PBS for 1 h to remove lubricin from
the cartilage surface [35–37]. Trypsin digestion was
used to remove proteoglycans and lubricin from
the superficial area of the cartilage specimen [38, 39].
For the last group, bovine cartilage specimens were
incubated in 30 mL of the reaction mixture (0.2 M
Tris-HCl buffer, pH = 7.3; 500 units mL–1 trypsin (Sigma))
at 37 °C for 20 min. Subsequently, 1 mg trypsin
inhibitor (Sigma) was added to the mixture. The final
group of cartilage specimens was called the trypsin
group.
Fresh SF was extracted from healthy bovine
metacarpal–phalangeal joints. The SF obtained from
several joints were mixed to minimize sample-to-sample
variability. If potential blood contamination was
identified, a certain amount of SF was excluded from
the sliding test.
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4 Friction
2.2 Friction tests
Rotational reciprocating sliding tests with an angular
amplitude of 30° were performed using a ball-on-
plate-type tribometer (Anton Paar NTR3, Austria)
with a smooth glass probe (Ra ≈ 0.045 μm) of 2 mm
diameter to evaluate the frictional characteristics
of the cartilage–glass contact. Photographs of the
tribometer are shown in Fig. 1. The tribometer used
in this study was developed to precisely investigate
the surface friction of compliant materials under
low-contact loads. The cartilage specimen was placed
in a liquid bath and was fully immersed in the
test lubricant. The glass probe was connected to
the cantilevers for force measurement through a
stainless-steel stem and mounted on a piezo-actuator
integrated in the tribometer. A dual quad-beam
cantilever with two separate high-resolution capacitive
sensors was used to measure the normal and frictional
forces exerted between the glass probe and the
cartilage surface. A piezo-actuator reads the normal
force measured by the sensor in real time and instantly
adjusts the vertical position of the glass probe to
maintain a constant normal force during the sliding
test. Subsequently, the COF was recorded as the ratio
of the frictional force to the normal force measured
by the sensors.
To evaluate the surface friction of each specimen,
the glass probe was pressed against the cartilage
surface at a constant load, and the specimen in the
liquid bath was rotated by a servo motor at constant
speed. Initially, the contact load and sliding speed
were set to 5 mN and 0.05 mm/s, respectively. The
sliding speed was subsequently increased to 0.1, 0.2,
0.5, 1.0, and 2.0 mm/s in a stepwise manner, and the
COF was recorded for five cycles at each sliding
Fig. 1 Photograph of the tribometer used in this study.
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speed. After finishing the friction measurement at
5 mN, the same procedure was repeated at increased
contact loads of 20 and 100 mN.
In the first series of experiments, the frictional
behavior of the untreated cartilage specimens was
evaluated in this contact. Each experiment consisted
of three steps: the surface friction of the fresh specimen
was evaluated immediately after preparation in PBS
(Step 1). Next, the specimen was kept in a liquid bath
filled with PBS for 1.5 h, and its surface friction in
PBS was examined again to confirm the effect of
stabilization in PBS (Step 2). The COF obtained in
Step 2 was used as the control data in the subsequent
second series of experiments. For selected specimens,
PBS in the liquid bath was replaced with SF after
Step 2, and the cartilage specimen was equilibrated
in SF for 1.5 h. Then, friction measurements were
performed in SF (Step 3).
The second series of experiments examined the
effects of degenerative treatments on the surface
friction of articular cartilage. The specimen was first
stabilized in PBS for 1.5 h after preparation. Then,
the surface friction before degenerative treatment
was characterized in PBS (Step 1). The specimen
was subsequently processed with one of the four
degenerative treatments and equilibrated for 1 h in
PBS after the treatment before measuring the surface
friction again in PBS (Step 2). Finally, the treated
specimens were equilibrated in SF for 1.5 h, and their
surface friction in SF was examined (Step 3).
The process of the friction measurements is
summarized schematically in Fig. 2. All experimental
procedures were conducted at room temperature.
2.3 Rheological test
To determine the rheological characteristics of SF
Friction 5

Fig. 2 Schematic representation of the overall experimental design.

extracted from bovine metacarpal–phalangeal joints, using a fluorescence microscope equipped with a
a rotational rheometer (Physica MCR 301; Anton Paar, water-immersion objective.
Austria) with a cone-on-plate configuration was
employed. Sampled SF was cast between a flat plate 2.5 Statistical analysis
and shallow cone with a diameter of 50 mm and an Statistical analysis was conducted using one-way
apex angle of 0.5°, and the viscosity was measured at ANOVA for significance with Dunnett’s multiple
a constant shear rate of 1 × 104 s–1 at 25 °C. comparison test. Data and error bars are presented as
2.4 Staining and histology mean±the standard error of the mean (SEM). The
threshold for significance was set at P < 0.05.
Fluorescent staining was used to visualize the surface
morphology of the cartilage specimens and to confirm
3 Results
the damage to the surface caused by degenerative
treatments. A small section was obtained from the 3.1 Rheological test
surfaces of the treated and untreated specimens and
washed with 1% bovine serum albumin (BSA, Sigma) The viscosities of PBS and SF were plotted as functions
in PBS for 30 min before fluorescence staining with of shear rate on a log scale, as shown in Fig. 3. Bovine
keratan sulfate, which is a major side-chain component
of proteoglycan molecules. BSA was used as a
blocking agent to prevent non-specific binding of the
antibody to the cartilage tissue. The cartilage sections
were incubated with the primary antibody of
anti-keratan sulfate (MAB2022, Sigma; diluted 1:400
in PBS) at room temperature for 1.5 h in the dark. Then,
the sections were rinsed with PBS and subsequently
incubated with a secondary antibody solution consisting
of Alexa Flour 568 conjugated Goat anti-mouse IgG2b
(A-21144, ThermoFisher; diluted 1:400 in PBS) for 1 h
in the dark. The stained cartilage surface was imaged Fig. 3 Lubricant viscosity measurements of PBS and bovine SF.

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6 Friction

SF showed a characteristic shear-thinning behavior,
reflected by a decrease in viscosity with increasing
shear rate. In contrast, PBS viscosity exhibited
Newtonian behavior. At the lowest shear rate, the
viscosity of SF was approximately 1,000 times higher
than that of PBS. However, as the shear rate was
increased to 104 s–1, the viscosity of SF decreased to
0.01 Pa·s, the difference in viscosity between PBS and
SF became smaller, and the viscosity of SF became six
times higher than that of PBS. The actual range of
shear rates in the synovial joints extends from rest
to 106 Pa·s [40]. This value is much higher than the
range of the shear rates in our rheological measurement.
The viscosity of SF was similar to that of PBS at this
high shear rate. Therefore, the viscous effect of the SF
may be much lower at a high shear rate in the actual
synovial joint.
3.2 Fluorescence observation
Fluorescence images of the cartilage specimen
surfaces are shown in Fig. 4. The surface of the fresh
specimen was consistently and uniformly smooth
(Fig. 4(a)). This represents the ideal appearance of the
intact uppermost superficial layer of the articular
cartilage. However, a slightly uneven surface was
observed after stabilization in PBS for 1.5 h (Fig. 4(b)).
The gently washed cartilage maintained a relatively
smooth surface; however, randomly distributed dark
spots of different sizes were observed (Fig. 4(c)). These
dark spots might be defects caused in the superficial
area of the cartilage surface by gentle washing in
detergent solution. The severe wash group completely
lost its original smooth surface morphology, and rough
and uneven surfaces with uniformly distributed small
dents were observed (Fig. 4(d)). The surface of the
NaCl group appeared to be slightly modified and
had some similarities to that of the gentle-wash
group (Fig. 4(e)). Meanwhile, the collagen fiber network
was exposed by trypsin digestion, and black areas
became dominant on the cartilage surface as a result
of proteoglycan removal (Fig. 4(f)).
3.3 Frictional characteristics of untreated cartilage
specimens
Figures 5(a)–5(c) shows the COF obtained from the
untreated cartilage specimens in Steps 1, 2, and 3,
respectively, as a function of the sliding speed on a log
scale at different normal loads. In all steps, a visible
effect on the sliding speed was observed. The COF
decreased with increasing sliding speed. The COF
in Steps 1 and 3 remained almost constant with
increasing normal load (Figs. 5(a) and 5(c)). Meanwhile,
the COF in Step 2 exhibited a clear dependence on
the contact load and decreased with an increase in
the contact load (Fig. 5(b)). Consequently, the highest
COF was obtained at the lowest sliding speed and
contact load.
In Figs. 6(a) and 6(b), the highest COF of each

Fig. 4 Fluorescent images of the articular cartilage surfaces for treated and untreated cartilage specimens in PBS. (a) Fresh specimen;
(b) control specimen; (c) gentle wash group; (d) severe wash group; (e) NaCl group; (f) trypsin group. (Scale bars: 250 μm.)

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Fig. 5 Average values of the COF as a function of the sliding
speed for the fresh specimen in (a) Step 1, (b) Step 2, and (c) Step 3
under normal loads of 5 (blue), 20 (orange), and 100 (black) mN
in PBS. (n = 15 for Step 1 and 2; n = 8 for Step 3.)
Fig. 6 Variation of the COF in (a) PBS (Step 2) and (b) bovine
SF (Step 3) with the initial condition (Step 1) between the glass
probe and cartilage surface for the fresh and control specimens
at 5 mN and 0.05 mm/s in PBS. (n = 15 for the fresh and control
specimens in PBS; n = 8 for the fresh and control specimens
in SF.)
7
untreated specimen obtained in Steps 2 and 3 is plotted
against the highest COF in Step 1, respectively. There
was a certain variation in the highest COF of the
freshly prepared cartilage specimens (Step 1) obtained
at the lowest load of 5 mN and sliding speed of
0.05 mm/s. This might have been caused by variations
in the surface integrity of the prepared cartilage
specimens. The quality of the test specimens prepared
from animal tissues is inevitably affected by the
condition of the source animals, and it is difficult
to obtain uniform specimens. Such a difference in
specimen quality is responsible for the non-negligible
variation in the experimental data from biological
tissue specimens in most cases. After stabilization in
PBS (Step 2), the variation in the highest COF was
enhanced (Fig. 6(a)), particularly when the highest
COF in Step 1 exceeded 0.1. However, the effect of
PBS stabilization was limited for the untreated cartilage
specimens, which showed a relatively low COF of
<0.1. In this case, the cartilage specimen might have
had a preferable surface condition after the preparation
process and could preserve surface integrity during
the storage period in PBS. Subsequently, it showed
low COF, even under low-load and low-speed
conditions in Step 2. However, if the cartilage surface
was not perfect and had damage, its lubricating
function deteriorated and became vulnerable to storage
in PBS. Subsequently, some cartilage specimens
exhibited a notably high COF during Step 2.
In contrast, the highest COF under SF lubrication
(Step 3) showed limited variation. It ranged from
0.07 to 0.20, and some specimens showed a reduced
COF compared to that in Step 1. These results clearly
indicate the lubricating function of the SF. Even if
the cartilage specimens had some damage to their
surface, the SF could compensate for it and reduce
the COF.
3.4 Effect of degenerative treatments
From the results of the second series of experiments,
the COF at the lowest sliding speed (0.05 mm/s)
was chosen to evaluate the effect of degenerative
treatments on the boundary lubrication function of
the cartilage surface and was compared with the
COF of untreated cartilage specimens under different
loads in Figs. 7(a), 7(b), and 7(c). As indicated in the
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8 Friction
first series of experiments, the COF at the lowest sliding
speed was sensitive to the initial condition of the
cartilage surface. Therefore, the effect of degenerative
treatments was examined using only selected cartilage
specimens whose maximum COF in Step 1 was <0.1.
At the lowest load of 5 mN, all treated specimens
exhibited a significant increase in the COF compared
with the untreated cartilage, except for the trypsin
group. Even when the load was increased to 20 and
100 mN, the treated cartilage exhibited a significantly
higher COF than the untreated cartilage, except
for the severe wash group at 100 mN. However, the
difference in COF decreased with an increase in the
Fig. 7 Comparison of the COFs for all specimens lubricated
with PBS at the lowest sliding speed (0.05 mm/s) under different
normal loads. (a) 5, (b) 20, and (c) 100 mN. *P<0.05, **P<0.01,
***
P<0.001, and ****P<0.0001 for differences from control specimen.
(n = 6 for the fresh and control specimens; n = 4 for the gentle
wash, severe wash, and NaCl groups; n = 2 for the trypsin group
in PBS.)
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contact load. The highest average COF was observed
in the severe wash group for all contact loads.
Meanwhile, the average COFs of the gentle-wash
and NaCl groups were very similar, regardless of the
load level.
3.5 Lubricating role of SF
In Figs. 8(a)–8(e), the COFs at 5 mN and 0.05 mm/s in
PBS and SF were compared for each cartilage specimen
regardless of the COF in Step 1 to demonstrate the
lubrication effect of SF. The COF in PBS was highly
dependent on the initial condition of the cartilage
surface and exhibited significant variation. However,
the COF variation in SF was comparatively smaller
(Fig. 6). This result indicates the lubricating effect
of the SF. The COF of most specimens in SF was
lower than that in PBS, particularly for the control
specimen and severe wash- and NaCl groups. The
average COF of the control specimen decreased
from 0.21 to 0.12 (Fig. 8(a)). This reduction in COF
was due to the SF constituents adsorbed on the
cartilage surface.
The average COF of the NaCl group (Fig. 8(d))
Fig. 8 Comparison of the COFs of the control and treated
specimens lubricated with PBS and SF at 0.05 mm/s and 5 mN.
(a) Control specimen; (b) gentle wash group; (c) severe wash group;
(d) NaCl group; (e) trypsin group. (n = 8 for the control specimen;
n = 4 for the gentle wash and severe wash groups; n = 8 for the
NaCl and trypsin groups in PBS.)
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decreased from 0.28 to 0.18, whereas the average
COFs of the gentle-wash (Fig. 8(b)) and trypsin groups
(Fig. 8(e)) only decreased from 0.20 to 0.18 and 0.23
to 0.17, respectively. The average COF of the severe
wash group in the SF was 0.11, which was lower
than that of the untreated control group. However, a
limited number of severely washed specimens could
be tested in SF, and the sample number was only
three. The gentle-wash, NaCl, and trypsin groups
showed approximately similar average COFs that were
larger than that of the control group in the SF. This
may be because the degenerative treatments removed
certain molecules linked to the boundary lubrication
mechanism at the cartilage surface.
4 Discussion
Our research confirmed the influence of the sliding
speed and applied contact load on the friction behavior
of the cartilage surface in contact with a glass probe.
The COF decreased with an increase in the sliding
speed. This is the typical frictional behavior of
lubricated bearings under the mixed-lubrication
condition suggested in the conventional Stribeck
curve [41]. However, it is also widely known that
compliant elastomers and hydrogels vary their friction
significantly with sliding speed [42–44]. Therefore,
the COF between the compliant and highly hydrated
articular cartilage and the glass probe may decrease
with increasing sliding speed, even under boundary
lubrication conditions. Bonnevie et al. [45] reported
similar experimental results: the COF between articular
cartilage and a ridged spherical probe decreased with
increasing sliding speed. They reported that the COF
was proportional to the contact area, which decreased
with increasing sliding speed because the stiffness
of the cartilage surface increased and this was
accompanied by a decrease in the ploughing (hysteresis)
component of the friction force. Delavoipière et al.
[46] demonstrated a similar frictional behavior with
thin hydrated hydrogel layers confined within contacts
between rigid glass substrates. They confirmed
experimentally that frictional force and contact size
depended on the Péclet number defined by the ratio
of the migration speed of the contact point on the gel
surface to the flow rate of interstitial water within the
9
hydrogel layer. If the Péclet number exceeds a certain
threshold, the contact size starts decreasing, and the
COF decreases simultaneously. This phenomenon can
be attributed to the insufficient time for the interstitial
water to be squeezed out from the contact area and
activated biphasic lubrication mechanism under
high sliding speeds [21, 47]. Based on the results of
previous studies [42–46], we presumed that the COF
between the cartilage specimen and glass probe was
evaluated under the boundary to mixed lubrication
condition between sliding surfaces in this series of
experiments. The COF decrease with increasing sliding
speed can be attributed to hydrodynamic fluid film
formation and enhanced fluid load support by the
water content of articular cartilage, even under the
lowest contact load of 5 mN.
Furthermore, the COF of the control sample with a
partially damaged uppermost superficial layer increased
as the applied contact load decreased in PBS, as shown
in Fig. 5(b). The observed load dependency on the
COF between the cartilage specimen and glass probe
is consistent with the results of previous studies
[48–50]. However, the fresh cartilage specimen with
an intact surface did not show such load dependency
on the COF (Fig. 5(a)). Consequently, the observed
load dependency is believed to be caused by the
partial depletion of the uppermost superficial layer
on the cartilage surface.
As shown in Fig. 7, the specimens after degenerative
treatments also showed a load dependency of their
COF, and the effects of degenerative treatments were
significantly pronounced by reducing the contact
load to 5 mN. Based on this finding, the average
value and standard deviation of COFs shown in Fig. 7
were calculated for each specimen group and plotted
against the applied contact load in Fig. 9 to elucidate
the influence of degenerative treatments on the load
dependency of COFs. As shown in Fig. 9, each
degenerative treatment had a clear and intrinsic
impact on the load dependency of COF, and a distinct
relationship between the applied load and the COF
was demonstrated for each specimen group.
As previously mentioned, all sliding tests in this
study were conducted under boundary to mixed
lubrication conditions, and the COF decreased
with increasing sliding speed. The COF of the fresh
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10
Fig. 9 Average values of COF as a function of the normal load
for cartilage specimens with sliding speed of 0.05 mm/s in PBS.
cartilage specimen increased with increasing contact
load. However, the control specimen showed an
inconsistent load dependence: the COF was the highest
under 5 mN load and decreased as the load increased
to 20 mN. Subsequently, it remained almost constant,
even when the load was increased to 100 mN. The
increase in COF under the lowest contact load was
further emphasized for the gentle-wash and NaCl
groups. The two groups exhibited similar friction
characteristics. The COF at 5 mN was three times higher
than that of fresh cartilage and decreased considerably
as the load increased to 20 mN. The significant
difference in the load dependency mentioned above
should be linked to the difference in the condition of
the superficial area of cartilage specimens demonstrated
by fluorescence observation (Fig. 4).
Fresh cartilage has a smooth surface, as shown in
Fig. 4(a), and the characteristic layered structure of
the cartilage superficial area has been reported in
numerous previous studies [5, 51]. As revealed by
several researchers, the uppermost surface of intact
Fig. 10 Schematic representation of articular cartilage surfaces of all treated and untreated specimens after the treatment process. (a) Fresh
specimen; (b) control specimen; (c) gentle wash group; (d) severe wash group; (e) NaCl group; (f) trypsin group. The dark blue: the
adsorbed phospholipids film; light blue: the lamina splendens; orange: denatured lamina splendens.
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articular cartilage is covered by the lamina splendens
[3, 6, 7, 52, 53]. The lamina splendens is an acellular
boundary layer that consists of an upper layer of an
amorphous substance and a lower layer of collagen
fibrils oriented parallel to the surface to provide the
highest possible tensile and shear strength [54–56].
Sawae et al. [57] confirmed that the amorphous
upper layer of lamina splendens mainly consists of
hydrated proteoglycan molecules. Furthermore, the
presence of adsorbed phospholipid bilayers on top
of the lamina splendens was confirmed by transmission
electron microscope (TEM) observations [7]. Jahn et al.
[32, 58] suggested that hydrated phosphocholine
heads aligned on phospholipid bilayers established
a low-shear sliding interface through the hydration
lubrication mechanism and provided boundary
lubrication.
In this study, we chose cartilage specimens whose
initial friction coefficient was < 0.1, even under the
lowest load and speed conditions, to examine the
effects of degenerative treatments. We assumed that
the selected specimens maintained their surface
integrity even after the specimen preparation process
and retained intact lamina splendens and adsorbed
phospholipid films [1, 4, 28] (Fig. 10(a)). The
absorption of water by the hydrophilic phosphocholine
heads in the phospholipid molecule results in hydration
lubrication [30, 59, 60]. In this lubrication mechanism,
the well-preserved adsorbed phospholipid film can
reduce attractive molecular interactions between
the surfaces, such as van der Waals forces, thereby
decreasing the adhesive force between the cartilage
and glass probe surfaces. Therefore, the COF of the
fresh specimens was the lowest among all the tested
groups. On the other hand, fluorescence observation
of the control specimen surface showed a slightly
Friction
uneven morphology (Fig. 4(b)). This may indicate that
the absorbed phospholipid film was partially removed
from the cartilage surface (Fig. 10(b)). The imperfect
adsorbed film could not suppress the adhesive
interaction between the surfaces and increased the
COF under the lowest contact load. According to the
Johnson–Kendall–Roberts (JKR) theory, the contact
area is influenced by the applied contact load and the
adhesive force between the rigid sphere and the
compliant surface [61]. As the contact load decreases,
the relative contribution of the adhesive force to
surface friction increased because of the significant
deformation of the compliant cartilage surface by the
adhesive force [62].
In the gentle-wash and NaCl groups, the cartilage
surface was washed out by the detergent or NaCl
solution and lost its integrity, as shown in Figs. 4(c)
and 4(e). Jones et al. [37] demonstrated that NaCl
treatment could remove lubricin from the cartilage
surface, while the overall tissue proteoglycan content
was hardly changed. Jahn et al. [58] suggested
that lubricin play an important role in maintaining
adsorbed phospholipids and HA complexes on
the cartilage surface. Consequently, the adsorbed
phospholipid film could be removed from the cartilage
surface by NaCl treatment. Therefore, the removal
of the adsorbed phospholipid film by NaCl treatment
and gentle washing with the detergent might result
in the exposure of the more compliant lamina
splendens with much lower stiffness, more than
inactivating the hydration lubrication by phospholipid
films (Figs. 10(c) and 10(e)) [4, 63]. Consequently, the
effect of the adhesive interaction was further enhanced
by the larger deformation of the compliant lamina
splendens, which caused a marked increase in the
COF under the lowest contact load. Based on the JKR
theory, the relative contribution of the adhesive force
to the exerted friction should be emphasized at low
contact loads [61, 62].
As shown in Fig. 4(d), severe washing with the
ultrasonic cleaner completely changed the morphology
of the cartilage surface. It is likely that ultrasonication
caused a significant temperature increase and induced
the denaturation of proteins on the cartilage surface.
Therefore, the original layered structure on the cartilage
surface was severely damaged, and the chemical
and physical properties of the lamina splendens were
11
significantly altered (Fig. 10(d)). As a result, the cartilage
surface loses its intrinsic lubricating function and
exhibits high COF.
Trypsin group was digested by enzyme which
removed proteoglycans from the cartilage surface and
exposed the collagen network (Fig. 4(f)) [39, 64–66].
Therefore, the cartilage specimens in this group lost
their intrinsic lubrication function and exhibited
higher COF. Some previous studies reported that a
trend of increased adhesion force can be observed in
trypsin-treated cartilage [66, 67]. However, removal
of the compliant lamina splendens diminished the
marked increase in COF under the lowest contact
load.
Figure 11 shows the COF of the gently washed and
NaCl groups at 5 mN, 0.05 mm/s and 5 mN, 2 mm/s
in SF. At 5 mN and 2 mm/s, the COF decreased
significantly and showed a minimum COF compared
with that at 5 mN, 0.05 mm/s. The gentle-wash group
exhibited the same COF as the NaCl group at the
lowest speed and contact load. However, the COF of
the NaCl group was larger than that of the gentle-wash
group at the highest speed and contact load tested.
Based on Figs. 4(a) and 4(e), it is clear that the
processing treatment by NaCl may have removed
something that is necessary to activate the lubrication
effect of the fluid film.
We applied extremely low loads between the glass
and cartilage to evaluate the friction behavior in the
superficial layer on the cartilage surface, attempting
to minimize contributions from the bulk of the
cartilage tissue. Higher contact loads lead to greater
surface deformation in the cartilage and greater energy
dissipation due to the viscoelastic deformation of the
cartilage tissue. In addition, cartilage deformation
can lead to increased interstitial fluid support. As
mentioned above, the Péclet number represents the
Fig. 11 Average COF values of gentle wash group and NaCl
group at (a) 5 mN, 0.05 mm/s and (b) 5 mN, 2 mm/s in SF.
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12
ratio of the sliding velocity to the velocity of the
interstitial fluid flow relative to the solid matrix.
It can be used to estimate the magnitude of the
interstitial fluid load support. The contact radius is
positively correlated with the Péclet number. Therefore,
reducing the contact load decreased the Péclet number
and minimized the effect of biphasic lubrication by
interstitial water in the cartilage tissue. However, 5 mN
was the minimum contact load that could be applied
in this study because significant data instability was
observed at contact loads below 5 mN. The Péclet
number was calculated from Pe  Va /H  A k where V is
sliding speed, a is the contact radius, H  A is aggregate
modulus, and k is permeability. According to the
Hertz contact theory [43], the contact radius between
the cartilage surface and glass probe can be estimated
as 0.236–0.641 mm. If we assume H  A = 13 MPa [68]
and k  6  10 16 m4/(N·s) [68], when the applied load
varies between 5 and 100 mN and the sliding speed
changes between 0.05 and 2 mm/s, Pe ranges from
1.5 to 164.1, still greater than 1. This indicates that
biphasic lubrication still influenced the friction results
obtained here. In addition, the elastic deformation
of the cartilage tissue produced by contact with
the glass probe and viscoelastic energy dissipation
should contribute to the friction result. These factors
represent the limitations of our experiment, leading
to discrepancies between our results and those of
other studies. For example, Shoaib et al. [69] applied
a contact pressure of less than 1 kPa and a sliding
velocity of 1 μm/s between lamina splendens and mica.
In this scenario, using a surface-force apparatus,
the COF in PBS was found to be in the range of 0.003.
However, the results showed that the COF of the fresh
samples in PBS reached 0.1 in our experiment, even
for the samples with an intact uppermost superficial
layer. According to the Hertz contact theory [43], the
contact pressure in the center of the contact area
between the cartilage surface and glass probe can
be estimated as 42.8–116.2 kPa. This was a significant
increase compared to Shoaib’s experiment. Consequently,
there should be contributions from cartilage bulk
deformation, viscoelastic energy dissipation, or fluid
flow inside the cartilage tissue. Another potential
limitation of this study is that friction measurements
were performed between the cartilage and glass rather
than against the cartilage. The unevenness of the
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Friction
cartilage surface makes it challenging to achieve a
perfect cartilage–cartilage contact pair.
We applied a range of sliding speeds to study
the frictional behavior of the cartilage surface. As the
sliding velocity increases, the flow resistance of
water and the associated viscous drag force typically
increase [70]. However, we observed a decrease in
the tangential force with an increase in the sliding
velocity (Fig. 9). The viscosities of both PBS and
SF are very low. Consequently, the contribution of the
drag force could be considered negligible compared
with that of the force detected in the current
experiments.
5 Conclusions
The friction characteristics of treated and untreated
cartilage specimens in contact with a smooth glass
surface were evaluated using an angular reciprocating
sliding test with a range of low contact loads and
sliding speeds in PBS and SF. To confirm the effects
of the treatments on the morphology of the cartilage
surface, a fluorescence microscope and water
immersion objectives were used.
The notable findings of this work can be
summarized as follows:
1) A certain variation was observed in the highest
COF of the freshly prepared cartilage specimens
obtained at the lowest load and sliding speed. The
condition of the original source animals may be
responsible for this variation. Such differences in
specimen quality in most biological tissue tests should
be considered.
2) The COF of the treated specimens increased
significantly after the degenerative treatments. This
may be due to the deterioration of the integrity of the
cartilage surface caused by degenerative treatments.
3) Compared with PBS, SF exhibited an obvious
boundary lubrication effect on the cartilage surface,
even for the treated specimens.
4) The untreated and treated cartilage specimens
exhibited different friction characteristics at the
lowest sliding speed and normal load. The different
adhesion forces acting between the untreated and
treated cartilage surfaces and glass probe surfaces
may be responsible for these results.
Friction
Acknowledgements
Financial support was given by the Grant-in Aid for
Scientific Research (A) of Japan Society for the
Promotion of Science (21H04535).
Declaration of competing interest
The authors have no competing interests to declare
that are relevant to the content of this article.
Open Access This article is licensed under a Creative
Commons Attribution 4.0 International License, which
permits use, sharing, adaptation, distribution and
reproduction in any medium or format, as long as
you give appropriate credit to the original author(s)
and the source, provide a link to the Creative Commons
licence, and indicate if changes were made.
The images or other third party material in this
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not permitted by statutory regulation or exceeds the
permitted use, you will need to obtain permission
directly from the copyright holder.
To view a copy of this licence, visit
http://creativecommons.org/licenses/by/4.0/.
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University in Japan, under the supervision of Prof.
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biomechanics of articular cartilage.
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16 Friction

Takehiro MORITA. He received Departure of Mechanical Engineering, Faculty of

his master’s degree in mechanical Engineering, Kyushu university, Japan. His major
engineering from Kumamoto research areas include friction and wear of prosthetic
University, Japan, in 1982. He is joint materials and polymer tribology in hydrogen
currently an associate professor at atmosphere.

Yoshinori SAWAE. He received Engineering, Faculty of Engineering, Kyushu university,

his Ph.D. degree in mechanical Japan. His major research areas include friction and
engineering from Kyushu University, wear of prosthetic joint materials, biomechanics of
Japan, in 1996. He is currently a articular cartilage and chondrocytes, and polymer
professor at Departure of Mechanical tribology in hydrogen atmosphere.

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