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Changes in Tissue Composition and Load Response After Transtibial Amputation Indicate Biomechanical Adaptation

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Despite the potential for biomechanical conditioning with prosthetic use, the soft tissues of residual limbs following lower-limb amputation are vulnerable to damage. Imaging studies revealing morphological changes in these soft tissues have not distinguished between superficial and intramuscular adipose distribution, despite the recognition that intramuscular fat levels indicate reduced tolerance to mechanical loading. Furthermore, it is unclear how these changes may alter tissue tone and stiffness, which are key features in prosthetic socket design. This study was designed to compare the morphology and biomechanical response of limb tissues to mechanical loading in individuals with and without transtibial amputation, using magnetic resonance imaging in combination with tissue structural stiffness. The results revealed higher adipose infiltrating muscle in residual limbs than in intact limbs (residual: median 2.5% (range 0.2-8.9%); contralateral: 1.7% (0.1-5.1%); control: 0.9% (0.4-1.3%)), indicating muscle atrophy and adaptation post-amputation. The intramuscular adipose content correlated negatively with daily socket use, although there was no association with time post-amputation. Residual limbs were significantly stiffer than intact limbs at the patellar tendon site, which plays a key role in load transfer across the limb-prosthesis interface. The tissue changes following amputation can have relevance in the clinical understanding of prosthetic socket design variables and soft tissue damage risk in this vulnerable group.
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Original Article
Changes in Tissue Composition and Load Response After Transtibial
Amputation Indicate Biomechanical Adaptation
J. L. BRAMLEY,
1
P. R. WORSLEY,
2
D. L. BADER,
2
C. EVERITT,
3
A. DAREKAR,
3
L. KING,
3
and A. S. DICKINSON
1
1
School of Engineering, Faculty of Engineering and Physical Sciences, University of Southampton, Mailpoint M7, University
Road, Southampton SO17 1BJ, UK;
2
School of Health Sciences, Faculty of Environmental and Life Sciences, University of
Southampton, Southampton, UK; and
3
University Hospital Southampton NHS Foundation Trust, Southampton, UK
(Received 20 April 2021; accepted 20 August 2021)
Associate Editor Stefan M Duma oversaw the review of the article.
AbstractDespite the potential for biomechanical condi-
tioning with prosthetic use, the soft tissues of residual limbs
following lower-limb amputation are vulnerable to damage.
Imaging studies revealing morphological changes in these
soft tissues have not distinguished between superficial and
intramuscular adipose distribution, despite the recognition
that intramuscular fat levels indicate reduced tolerance to
mechanical loading. Furthermore, it is unclear how these
changes may alter tissue tone and stiffness, which are key
features in prosthetic socket design. This study was designed
to compare the morphology and biomechanical response of
limb tissues to mechanical loading in individuals with and
without transtibial amputation, using magnetic resonance
imaging in combination with tissue structural stiffness. The
results revealed higher adipose infiltrating muscle in residual
limbs than in intact limbs (residual: median 2.5% (range 0.2–
8.9%); contralateral: 1.7% (0.1–5.1%); control: 0.9% (0.4–
1.3%)), indicating muscle atrophy and adaptation post-
amputation. The intramuscular adipose content correlated
negatively with daily socket use, although there was no
association with time post-amputation. Residual limbs were
significantly stiffer than intact limbs at the patellar tendon
site, which plays a key role in load transfer across the limb-
prosthesis interface. The tissue changes following amputation
have relevance in the clinical understanding of prosthetic
socket design variables and soft tissue damage risk in this
vulnerable group.
KeywordsTranstibial amputation, Magnetic resonance
imaging, Infiltrating adipose, Remodelling, Muscle atrophy.
INTRODUCTION
Following lower limb amputation, the residual skin
and soft tissues form a critical interface with the be-
spoke ‘socket’ component of a prosthetic limb. These
tissues are vulnerable to damage, particularly during
the early rehabilitation phase, prior to adequate
biomechanical conditioning arising from mechanical
loading.
35
The resulting tissue deformations may cause
skin and soft tissue damage, with reported prevalence
between 36 and 66%.
12,35,36
Experimental and numerical models indicate that
large deformations over short periods of time represent
the most important factor in the causal pathway for
Deep Tissue Injury (DTI), which initiates in muscle
tissues.
8,15,3133,39,40,53,54
By contrast, superficial pres-
sure ulcers (PUs) are generally caused by external
pressures and shear forces. The tissue tolerance to
loading magnitude and duration varies between indi-
viduals,
19
and is influenced by many intrinsic factors.
10
There has been relatively little research into skin
damage in individuals with lower limb amputations,
despite the specific risk factors and high prevalence in
this group.
18
Indeed the residual limbs are exposed to
challenging biomechanical conditions, impaired load
tolerance due to comorbidities, considerable variability
in anatomy and surgical reconstruction, and the pres-
ence of scar tissue over vulnerable sites.
41
Tissue loading at the residuum-prosthesis interface
is influenced by the socket design, with the prosthetist
considering both the morphology of the local tissues
and their load tolerance.
28,42,46
These characteristics
change post-amputation due to oedema, muscle atro-
Address correspondence to A. S. Dickinson, School of Engi-
neering, Faculty of Engineering and Physical Sciences, University of
Southampton, Mailpoint M7, University Road, Southampton SO17
1BJ, UK. Electronic mail: alex.dickinson@soton.ac.uk
Annals of Biomedical Engineering (2021)
https://doi.org/10.1007/s10439-021-02858-0
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2021 The Author(s)
phy and tissue remodelling in biomechanical adapta-
tion to prosthetic load bearing. The oedematous
response to the trauma of amputation decreases
gradually in the months following surgery.
29
Physio-
therapy exercises are prescribed to promote range of
motion in the residual limb joints, and reduce muscle
atrophy and oedema.
43
Despite these interventions,
residual muscles atrophy due to denervation and dis-
use, with a subsequent infiltration of adipose or fibrous
tissues.
51,58
In addition, the superficial tissues adapt in
response to increased repetitive loading, with pressures
and shear stresses at the limb-prosthesis interface
ranging widely, from 4 to 938 mmHg (0.5 to 125 kPa)
and 8 to 389 mmHg (1 to 52 kPa), respectively.
56,62,63
The skin and subdermal tissues may thicken, and callus
is formed to adapt their vascular function. Such
changes have been reported using optical coherence
tomography, with an increased epidermal thickness in
transtibial residua compared to the contralateral limb,
and higher microvascular function.
55
To date there is limited evidence of how biomechan-
ical loading affects the vulnerable residuum muscle and
adipose tissues during early rehabilitation. Volume
imaging modalities have been used to observe residual
limb adaptation. These include Magnetic Resonance
Imaging (MRI) to visualise muscle morphology changes
and differentiate between changes due to oedema and
muscular atrophy,
28
and computed tomography (CT) to
determine the proportion of muscle and fat mass in the
residual limb compared to contralateral limbs.
50
MRI
has been used to evaluate fatty infiltration in other tis-
sues,
20,21
but previous studies have not quantified adi-
pose tissue or distinguished between superficial and
intramuscular distribution in amputees. This is despite
the recognition that intramuscular fat levels represent an
indicator of the risk for severe pressure ulcers, as
observed in the gluteal region of individuals with spinal
cord injury prone to DTI.
59
Furthermore, it remains
unclear how these changes may alter tissue tone and
stiffness, which represent key biomechanical character-
istics at the interface with the prosthetic socket, likely to
influence residuum-socket load transfer patterns and in
turn the soft tissue damage risk. Indeed, these properties
have been shown to change due to a range of factors
relevant to the amputee population including ageing,
stroke, exercise and post-exercise massage,
2,9,14,25
as
well as in the spinal cord injury population.
48
Changes in both soft tissue morphology and
mechanical response to loading following amputation
have clinical relevance to the understanding of effective
prosthetic socket designs. Research has identified the
potential application of prosthesis-limb interface sen-
sors and/or numerical predictions to support the pre-
vention of soft tissue damage.
11,45
However, there is still
limited research which assesses the composition and
structural features which are critical in determining tis-
sue tolerance to mechanical loading. Accordingly, this
study was designed to characterise residual limb soft
tissue morphology, composition and mechanical
response to representative prosthetic loading. To assess
changes arising from amputation and prosthetic limb
use, the study compared residual and intact limbs of
individuals with unilateral transtibial amputation, and
intact controls. This involved characterising the pro-
portions of both superficial adipose and adipose infil-
trating muscle tissue using MRI, their deformation and
gross strain under in situ mechanical loading with
indenters, and measuring the structural stiffness of the
combined soft tissue layers.
METHODOLOGY
Study Design and Recruitment
An observational comparison study was conducted
with participants recruited from the local community
population, including those with and without unilat-
eral transtibial amputation. Inclusion criteria involved
participants over 18 years of age, in good health with
no active skin-related conditions at sites relevant to the
study. Participants without amputation had additional
exclusion criteria of neurological and vascular
pathologies. Local Ethics Committee approval for the
test protocol was granted by the University of
Southampton (ERGO IDs: 29696 and 41864) and
participants provided informed consent in writing.
Test Protocol
Pressure was applied to the right proximal calf of
control participants without amputation, and both
calves of participants with unilateral transtibial
amputation using an inflatable cuff (Ref 0124 Aneroid
Sphygmomanometer, Bosch + Sohn GmbH, Ger-
many) according to a previous publication.
6
A pros-
thetic liner (6mm ContexGel Liner, NMA21L200/
XXL, RSL Steeper, UK) was positioned underneath
the cuff to provide a representative material to inter-
face with the skin. Three 50 mm square sites were se-
lected for measurement on each limb representing load
bearing regions of differing tissue composition, namely
the patellar tendon, lateral calf, and posterior calf
(Fig. 1a). Cylindrical polymer indenters of 17 mm
diameter and 15 mm height were positioned under-
neath the cuff at the three measurement sites, con-
taining sunflower oil capsules to facilitate identification
within the MR images (Fig. 1b).
Participants were scanned supine, feet-first using a
3T MRI scanner (MAGNETOM Skyra, Siemens,
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BRAMLEY ET AL
Germany), with their test-limb elevated and resting on
foam supports. MR images were acquired using an 18-
channel body array coil placed on top of the test limb,
as well as the spine coil in the scanner couch under-
neath the limb. Images were acquired at baseline and
at a cuff inflation pressure of 60 mmHg (8 kPa) to
characterise direct tissue deformation and visualise
morphology and tissue composition
6
(Fig. 1c). Volu-
metric MRI data were acquired using a 3D T1 DIXON
sequence
34
with an echo time (TE) of 6.15 ms and a
repetition time (TR) of 17.10 ms, a 134 mm field of
view, an in-slice resolution of 0.6 mm 90.6 mm and a
corresponding slice thickness of 1.2 mm. The acquisi-
tion time was 5 min 19 s. This sequence generates a set
of 4 volumetric axial image datasets, each with a dif-
ferent contrast: in-phase, opposed-phase, fat-only and
fat-suppressed (water-only) images.
The volume of both superficial- and muscle-infil-
trating adipose tissue was quantified by processing the
MR images in ImageJ 1.52p (Rasband, W. National
Institute of Health, US). Background noise was
removed by subtracting a pixel intensity of 10, and
binary images created with the Auto Threshold Stack
tool. Masks were created representing the whole soft
tissue area, tibia, fibula and muscle, and Boolean
operations were applied to generate superficial- and
muscle-infiltrating adipose tissue masks whose areas
were calculated (Fig. 2). Gross deformation and com-
pressive strain under each indenter was estimated by
selecting single MR slices corresponding to the centre
of the measurement sites, measuring the normal dis-
tance from the indenter surface to the nearest bony
prominence and comparing these values at both un-
loaded baseline (0 kPa) and inflated cuff test condi-
tions (8 kPa). Deformation was calculated as
d¼d0d8
ðÞand strain as e¼d0d8
ðÞ=d0.
Prior to imaging, interface pressure and soft tissue
stiffness measurements were recorded for each partici-
pant in a seated position on a commercial hospital bed
with adjustable backrest (Enterprise, Arjo Huntleigh,
Bedforshire, UK), with their test-limb elevated and
resting on foam supports. Indenter-skin interface pres-
sures were measured using a pneumatic pressure moni-
toring system (Mk III, Talley Medical, Romsey, UK)
with 28 mm diameter measurement cells, which have a
reported mean error of 12 ±1% and a repeatability of
FIGURE 1. (a) Measurement sites on the right lower limb, each of area 50 350 mm; (b) 3D printed indenter positioned at each
measurement site via adhesive fixation ring, enclosed by a pressure cuff with the limb in the supported test position (middle) and
MRI test set up prior to imaging (bottom), (c) Timeline of the MRI test protocol.
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Tissue Composition and Load Response After Amputation
±0.53 mmHg.
4
The cuff and liner were then doffed, and
the MyotonPro (Myoton AS, Talinn, Estonia) device
was used to apply a 15 ms, 0.4 N mechanical impulse at
each of the measurement sites in order to estimate the
superficial tissue structural stiffness. This device esti-
mates dynamic stiffness using S¼amax mprobe =Dl,
where amax is the impulse probe’s maximum accelera-
tion, mprobe is its mass and Dlis its displacement at the
point of maximum acceleration. The MyotonPRO has
been demonstrated to show reliable lower limb skeletal
muscle structural stiffness measurements
3
which corre-
late with shear wave elastography.
23
Data Analysis
Raw data from each of the measurement techniques
were processed and analysed using MATLAB (Math-
Works, USA) and SPSS Statistics (IBM, USA). After
testing for normality, MRI data were analysed using non-
parametric descriptors (median, quartiles and range),
whereas interface pressure and tissue stiffness data were
analysed using parametric descriptors (mean and stan-
dard deviation). Differences in tissue composition,
deformation and strain between control, contralateral
and residual limb groups (non-parametric) were assessed
for statistical significance using a Mann-Whitney-U test,
and differences between structural stiffness (parametric)
were assessed using T-Tests. Relationships between per-
centage of infiltrating and superficial adipose tissue, the
time since amputation, socket use, structural stiffness and
deformation were evaluated using scatter plots and
Spearman’s correlation. Differences wereconsidered to be
statistically significant at the 5% level (p<0.05).
RESULTS
Ten participants without amputation and 10 par-
ticipants with unilateral transtibial amputation were
recruited (Table 1). The control group was younger
than the group with amputation and presented with a
lower median weight and BMI. There was a variety of
causes of amputation in the latter group, and a wide
range of time since amputation, from 1 to 35 years.
Soft Tissue Composition
Residual limbs were observed to have a smaller
cross-sectional area and a less consistently round shape
than intact limbs, although the residual limbs often
revealed distorted shape artefacts resulting from the
foam support (Fig. 3). Figures in the Supplementary
Data detail the percentage volumes of superficial adi-
pose tissue, adipose infiltrating muscle and muscle
tissue across the limb sections for all participants.
Residual limbs displayed greater adipose tissue infil-
trating muscle than intact limbs (Fig. 3), reaching
significance (p<0.05) when compared to the residual
and control limbs (Fig. 4).
Correlation analysis was performed between the per-
centage volumes of adipose tissue, and three intrinsic
factors, namely BMI, time since amputation and daily
socket use (Fig. 5, Table 2). A significant positive corre-
lation was observed between the levels of both adipose
tissue types in the residual and contralateral limbs
(Fig. 5a and b). There was a negative correlation between
adipose infiltrating muscleand estimated daily socket use
in both contralateral and residual limbs, although this
was only statistically significant for the former (r=
20.87, p<0.01, Fig. 5c). In contrast, no correlation was
evident between the adipose infiltrating muscle values
and the time since amputation (r=20.05, p=0.88,
Fig. 5d). It was also interesting to note that there was a
positive trend between the adipose infiltrating muscle
tissue and the BMI in the control, non-amputated group,
although the correlation was not statistically significant
(r=0.46, p=0.18). With respect to superficial adi-
pose values, there were no significant correlations with
any of the three intrinsic factors (Table 2).
FIGURE 2. Image processing steps applied to the axial MRI
fat-only slice of the lower limb at the posterior calf
measurement site, showing (a) original image, and (b) after
binarization and masking. (c) superficial adipose mask
(yellow) and muscle-infiltrating adipose mask (red)
superimposed over the corresponding opposed-phase
image at same slice, and (d) superimposed outlines of limb
under uninflated cuff baseline (solid line) and 8 kPa inflated
cuff (dashed line) conditions. Example measures are shown
for calculating the displacement and gross strain arising from
cuff inflation between the posterior calf indenter to the
nearest bony prominence, uninflated (d
0
) and at 8 kPa
inflation (d
8
).
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Interface Pressure
At a cuff inflation pressure of 60 mmHg, the mean
interface pressures ranged from 66 to 74 mmHg, 70 to
75 mmHg and 72 to 84 mmHg in control, residual and
contralateral limbs, respectively (Table 3). The highest
pressures and variability generally occurred at the
patellar tendon, which represented the measurement
site with the lowest soft tissue coverage over the
underlying bony anatomy.
Soft Tissue Deformation and Strain
The soft tissue shape changes from baseline to a cuff
pressure of 60 mmHg (8 kPa), visualised from MR
images (Figures in the Supplementary Data) were
converted into two parameters, gross tissue deforma-
tion and strain. These data revealed that deformation
was significantly higher (p<0.01) in control limbs
than residual limbs at all three sites (Fig. 6). Defor-
mation was also higher in control limbs than the
contralateral limbs, with statistically significant dif-
ferences at the patellar tendon (p<0.01) and the
posterior calf (p<0.05). Within the individuals with
amputation, deformation was significantly different
between their residual and contralateral limbs at the
lateral (p<0.01) and posterior calf sites (p<0.05).
Strain results revealed similar trends to that of defor-
mation. However, there were no significant differences
between groups at the posterior calf site, with all three
sites observed to demonstrate similar strain magni-
tudes. The high deformation at the posterior calf site
produced relatively low strains owing to its high soft
tissue layer thickness. Few notable correlations were
revealed between either gross tissue deformation or
compressive strain and percentage volume of superfi-
cial adipose or time since amputation (Supplementary
Data Table S1).
Soft Tissue Stiffness
Structural stiffness values were highest at the
patellar tendon site, which has the least soft tissue
coverage, adjacent to a bony prominence (Fig. 7). The
highest stiffness values (mean 740 ±190 N/m) were
observed in the residual limb group at the patella site,
which were significantly higher than those estimated
from the control group (p<0.05). No differences were
observed between groups in the lateral calf or posterior
calf, and few notable correlations were revealed
between structural stiffness and percentage volume of
superficial adipose or time since amputation (Supple-
mentary Data Table S2).
TABLE 1. Participant characteristics, reported as median (range).
Characteristic
Controls Participants with Amputation
All (n=10) Male (n=6) Female (n=4)
All (n=10)
Male (n=8) Female (n=2)
Age (years) 28 (23–36) 26 (23–34) 28 (27–36) 41 (25–62) 45 (25–62) 38 (30–46)
Height (m) 1.78 (1.60–1.92) 1.82 (1.75–1.92) 1.66 (1.60–1.76) 1.76 (1.63–1.88) 1.79 (1.65–1.88) 1.65 (1.63–1.68)
Mass (kg) 66 (56–90) 78 (66–90) 58 (56–64) 79 (51–127) 79 (73–127) 76 (51–100)
BMI (kg/m
2
) 22.1 (18.3–29.4) 23.6 (18.3–29.4) 21.5 (18.4–23.5) 27.3 (19.2–37.5) 27.3 (20.7–37.5) 27.4 (19.2–35.6)
Max Calf Circumference (mm)
Residual 290 (250–450) 300 (260–450) 270 (250–290)
Contralateral 360 (320–410) 390 (350–410) 360 (320–360) 390 (340–530) 390 (350–530) 390 (340–440)
Residual limb length (mm) 150 (100–300) 150 (100–300) 210 (140–270)
Time since amputation (years) 7.5 (1–35) 5.0 (1–35) 18.5 (8–29)
Amputation cause
CRPD 2 1 1
Congenital 2 1 1
Trauma 5 5 0
PVD –––1 10
Daily socket use (h) 12.5 (6–16) 11.5 (6–616) 14.5 (14-15)
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FIGURE 3. Exemplar transverse MRI slices in the calf with superficial adipose (yellow) and adipose infiltrating muscle (red) tissue
overlays. Images represent the right control limb of ten participants without amputation (left columns #1-10), and both the control
(C) and residual (R) limbs for ten participants with transtibial amputation (right columns, #1A-#10A).
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DISCUSSION
This study was designed to investigate residual limb
soft tissue composition and how loading affects tissue
deformation. It presents, for the first time, the com-
bination of MRI data and structural stiffness mea-
surements using a commercial device. Two cohorts
were recruited, with and without transtibial amputa-
tion, and they were imaged using MRI prior to and
during the application of representative mechanical
loads via a pressure cuff. The results revealed signifi-
cant changes to soft tissue composition in the residual
limb, with a higher proportion of muscle-infiltrating
adipose tissue, which was associated with the amount
of daily socket use. A critical load bearing site, the
patellar tendon, was also shown to demonstrate sig-
nificantly increased stiffness in the residual limb com-
pared to intact control limbs.
Measurements and Analysis
MRI data enabled clear visualisation of the soft
tissues with the specific distinction of bone, muscle and
adipose tissues (Figs. 3,4). Comparison between the
control and amputee groups demonstrates how
pathology resulted in a markedly increased variability
in limb tissue composition and morphology. Residual
limbs contained approximately three times more infil-
trating adipose tissue than control limbs of partici-
pants without amputation. Adipose infiltrating muscle
was particularly apparent in more established residual
limbs (#4A, #6A and #9A), and in two people with
shorter time since amputation (#1A and #5A). One of
these participants (#1A) used a wheelchair for mobility
for several years prior to amputation which may have
caused additional atrophy in the lower limb muscles,
and the other (#5A) had Type 1 diabetes which has
been associated with increased adipose infiltrating
muscle.
5
These observations reflect the well-established
changes in tissue composition associated with muscle
atrophy post-amputation associated with denervation
and disuse.
28,51,58
However, this study has proved no-
vel in discriminating between superficial and adipose
infiltrating muscle tissues in residual limbs, thus pro-
viding insight into the potential for both disease pro-
gression
1,20,21
and an enhanced risk for DTI.
37,52,57
Correlation analysis provided insights into the
relationships between tissue composition in the con-
tralateral and residual limbs and intrinsic factors
associated with the individuals post-amputation (Ta-
ble 2). Residual limb adipose was observed to correlate
significantly with contralateral limb adipose for both
superficial and infiltrating types (Fig. 5top). However,
a high percentage volume of superficial adipose tissue
did not necessarily correspond with high infiltrating
adipose indicating that various factors may be
responsible for the infiltration. It is of note that
superficial adipose did not correlate with BMI, time
since amputation or estimated hours of prosthesis use.
By contrast, a significant negative correlation was re-
vealed between infiltrating adipose in contralateral
limbs and estimated daily prosthesis usage, which
supports the suggestion that infiltrating adipose may
represent a biomechanical adaptation, namely muscu-
lar atrophy due to disuse. More active limbs presented
with more lean muscle mass, and the lack of correla-
tion for residual limbs may indicate the influence of
other factors such as gait compensations where par-
ticipants favour their intact limb.
30
Adipose tissues
change in size and function in response to a number of
factors including loading, exercise, temperature and
nutrition, with hypertrophy observed under static
tension.
27,61
This may have influenced the structural
stiffness values measured and is worthy of further
exploration.
The composition and status of soft tissues will affect
how they respond to and tolerate mechanical loading.
The pressure cuff was used to apply pressure repre-
sentative of PPAM aid use during rehabilitation.
47
Loading was applied through a 60 mmHg cuff infla-
tion, with some non-uniformity of interface pressures.
The patellar tendon, with its relatively thin soft tissue
coverage, demonstrated the highest pressures. Low,
non-zero pressure was measured between the indenters
FIGURE 4. Median, interquartile range (IQR) and range in
percentage of tissue constituents of the overall limb, in a
60mm segment distal from the tibial plateau. + indicates
outliers; * indicates significance at p£0.05; ** indicates
significance at p£0.01.
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and limb at baseline (0mmHg cuff pressure) although
these were within the reported errors of the pressure
measurement system.
4
Using MRI to evaluate tissue
deformation pre- and post-loading, and resulting gross
compressive strain, revealed the lowest values at the
residual limb patellar tendon site. This corresponded
to the highest tissue stiffness measurements (Fig. 7),
and is the location at which many prosthetists focus
loading (i.e. using patella tendon bearing socket de-
signs
44
), and could be attributed to local biomechani-
cal adaptation in response to repetitive loading at this
location. Residual limbs were also generally smaller
than contralateral limbs, resulting in higher compres-
sive strains for equivalent deformations at residual
limb sites (Fig. 6). At the calf sites, the highest stiffness
values were observed in the contralateral limbs, which
could again indicate adaptation in response to com-
pensatory gait patterns, prior to- or following ampu-
tation.
30
Though the MyotonPRO assesses the
superficial tissues only, it produced structural stiffness
results consistent with gross mechanical indentation in
the transtibial amputated limb’s anterior aspect (ap-
proximately 400–500 N/m).
49
The recorded structural
stiffness values were in the same range as reported in
other myotonometry studies of skeletal muscles in the
lower limb. These studies reported mean values rang-
FIGURE 5. Positive correlations were observed between residual limb and contralateral limb superficial adipose (a) and
infiltrating adipose (b). Negative correlation was observed between percentage volume of infiltrating adipose tissue in contralateral
limbs and estimated daily socket use (c), though no correlation was seen between contralateral limb infiltrating adipose and time
since amputation (d). Number indicates participant ID.
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ing from approximately 275–450 N/m for the gas-
trocnemius,
13,22,24,26
and 350–400 N/m for the tibialis
anterior,
24,26
which correspond with the present
study’s posterior calf and lateral calf sites, respectively.
Literature studies reporting MyotonPro assessment of
the patella tendon have primarily recruited athletes, for
whom the stiffness values might be elevated. However,
neglecting elite athlete studies and considering control
groups, mean values have been reported ranging from
780 to 900 N/m,
7,60
consistent with the present study’s
results.
During periods of loading application, the magni-
tude and duration of mechanical strain is considered to
represent the most important factor in the causal
pathway for damage of soft tissue.
8,15,3133,39,40,53,54
The largest strains observed in this study were between
20 and 30%, applied over a 15 minute period. These
conditions represent a lower range than that observed
in examining tissue damage in model systems
17
and in
clinical situations.
Limitations
The study’s generalisability is limited by its small
sample size and heterogeneity of the individuals with
amputation. The group has a substantial range in time
since amputation (1–35 years), although this variety is
largely representative of the community accessing
prosthetics services in our Southern UK area.
Accepting this limitation, the study was designed to
evaluate the heterogeneous nature of a cohort with
lower limb amputations with a wide range of individ-
ual demographics, reasons for amputation and asso-
ciated tissue morphologies and responses. Accordingly,
the study used correlation analysis and prioritised
comparison between the residual and contralateral
limbs. Thus, the present study has provided insight
TABLE 2. Correlation analysis for selected intrinsic factors (BMI, time since amputation and estimated daily socket use) and the
percentage volume of infiltrating and superficial adipose from the tibial plateau to 60mm distally, in the right control limbs of ten
participants without amputation and the contralateral and residual limbs of ten participants with unilateral transtibial amputation.
Bold text and ** represents significance at the 1% level.
Correlation between Limb Correlation rSignificance p
Percentage volume of infiltrating adipose and: BMI Control 0.46 0.18
Contralateral 0.35 0.33
Residual 0.12 0.75
Time Since Amputation Contralateral 20.05 0.88
Residual 0.45 0.19
Est. Daily Socket Use Contralateral 20.87 <0.001*
Residual 20.34 0.34
Percentage volume of superficial adipose and: BMI Control 0.12 0.75
Contralateral 0.08 0.83
Residual 20.19 0.60
Time Since Amputation Contralateral 0.12 0.75
Residual 0.20 0.59
Est. Daily Socket Use Contralateral 0.09 0.82
Residual 20.04 0.92
TABLE 3. Interface pressure at three measurement sites, at baseline and a cuff pressure of 60mmHg, applied to the right control
limb of 10 participants without amputation and both residual and contralateral limbs of 10 participants with unilateral transtibial
amputation
Measurement site
Mean (S.D.) interface pressure at applied cuff pressure
0 mmHg (Baseline) 60 mmHg
Control limbs Patella Tendon 13.1 (7.4) 73.7 (8.2)
Lateral Calf 4.7 (2.9) 72.6 (5.5)
Posterior Calf 0.5 (1.3) 66.2 (5.0)
Contralateral limbs Patella Tendon 17.7 (15.2) 83.6 (34.3)
Lateral Calf 7.7 (11.1) 75.1 (6.7)
Posterior Calf 2.8 (6.3) 72.0 (11.7)
Residual limbs Patella Tendon 13.6 (13.4) 73.1 (21.6)
Lateral Calf 13.9 (12.4) 75.1 (11.4)
Posterior Calf 11.9 (13.4) 69.9 (12.7)
BIOMEDICAL
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Tissue Composition and Load Response After Amputation
into the factors that can affect tissue adaptation and
load tolerance post-amputation, with further studies
needed to explore how these differences could affect
their tolerance to prosthetic loading. The two cohorts
were not matched by their demographics (age, weight
and BMI in particular) and this may substantially af-
fect the comparisons observed between the people with
amputations and the intact controls. However, the
intact control data are interesting to assess the soft
tissue characteristics of a young, healthy group of
people without amputations, whose lower limb soft
tissues might represent the start point of prosthetic
rehabilitation in cases of amputation due to trauma or
neoplasia. The sample size is a recurring issue for lower
limb prosthetics studies with a small population of
eligible participants, so the presented data do not cover
the full variance of physiological conditions experi-
enced in the wider population of people who use
prosthetics. The present findings provide focus for
further study on more homogeneous groups of par-
ticular interest or concern.
During the testing sessions it was often difficult to
support residual limbs in a consistent manner, and
participants with short residual limbs and knee flexion
contracture required support from below. These fac-
tors dictated the length of all the limbs which could be
consistently imaged, at 60 mm. With respect to
structural measurements, although limbs were kept in
a consistently supported position, relaxation of the
muscles was not achieved objectively. Indeed, con-
tracted muscles could have presented with higher
stiffness and elasticity values.
14
Furthermore, the
MyotonPRO measurement system is mainly designed
for measuring the stiffness of superficial tissues, so any
adaptation of deeper muscular tissues may be less
apparent in participants with higher superficial adipose
tissue.
9
Considering tissue strain measurement, the
reported values are equivalent to a measure of engi-
neering strain. Therefore, these estimates are not di-
rectly comparable to the principal and shear Green-
Lagrange strain components most commonly em-
ployed in imaging and finite element analysis (FEA)
estimation of tissue damage risk thresholds.
8,31,32,54
The paired, aligned MR images collected in this study
would enable Green-Lagrange strain prediction using
FEA but this was outside the present scope.
Summary and Clinical Implications
A higher proportion of muscle-infiltrating adipose
was observed in residual limbs compared to intact
limbs, indicating muscle atrophy post-amputation.
Residual limbs were also stiffer at the patellar tendon
site and demonstrated less strain under external pres-
sure than intact limbs. Understanding the changes in
tissue composition can provide clinicians with new
insights into how residual limb tissues adapt to repre-
sentative prosthetic loading and could offer strategies
FIGURE 6. Median, interquartile range (IQR) and range of
lower limb soft tissue deformation under 60mmHg pressure
cuff loading for all participant groups. * indicates significance
at p£0.05 and ** indicates significance at p£0.01.
FIGURE 7. Mean values of tissue structural stiffness at three
measurement sites on the right control limb of eight
participants without amputation and both contralateral and
residual limbs of ten participants with unilateral transtibial
amputation. * indicates p£0.05.
BIOMEDICAL
ENGINEERING
SOCIETY
BRAMLEY ET AL
to prevent skin and sub-dermal damage, which is
common in this population.
The evidence of superficial tissue biomechanical
adaptation in response to increased mechanical loads,
notably at the patellar tendon, extends evidence from case
studies reporting increased soft tissue tolerance to ische-
mia under loading at this critical location which is
exploited by prosthetists for residuum-prosthesis load
transfer.
6
The results also show indicators of muscle
atrophy, presenting as elevated adipose infiltrating mus-
cle tissue in residual limbs. This is a well-established
marker of pressure ulcer risk in individuals with spinal
cord injury, and accumulates over time,
16
so this evidence
contributes to our understanding of these individuals’
risk of deep tissue injury, as well as metabolic syndrome,
cardiovascular disease and related mortality.
38
This study demonstrates how residual limb soft
tissues can change post-amputation in a small popu-
lation with a range of amputation causes, and longi-
tudinal studies could help to determine more predictive
variables that affect tissue composition and tolerance
to loading post-amputation. This insight will help to
further understanding of how the soft tissues adapt to
tolerate prosthetic loading, to help reduce the risk of
tissue damage during prosthetic use.
AUTHOR CONTRIBUTIONS
JLB: Conceived and designed research; Per-
formed experiments; Analyzed data; Interpreted results
of experiments; Prepared figures; Drafted manuscript;
Edited and revised manuscript; Approved final version
of manuscript. ASD: Conceived and designed research;
Analyzed data; Interpreted results of experiments;
Prepared figures; Drafted manuscript; Edited and
revised manuscript; Approved final version of manu-
script. PRW, DLB: Conceived and designed research;
Analyzed data; Interpreted results of experiments;
Edited and revised manuscript; Approved final version
of manuscript. CE, AD, LK: Conceived and designed
research; Performed experiments; Approved final ver-
sion of manuscript.
CONFLICT OF INTEREST
Each author (1) made an important contribution to the
conception and design, acquisition of data, or analysis
and interpretation of data in the study; (2) drafted or
revised the manuscript critically for intellectual con-
tent; and (3) approved the final version of the sub-
mitted manuscript. None of the authors has any
conflict of interest to declare. Raw data are openly
available from the University of Southampton reposi-
tory at https://doi.org/10.5258/SOTON/D1941.
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 appro-
priate 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 article are included in the
article’s Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is
not included in the article’s Creative Commons licence
and your intended use is 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://crea
tivecommons.org/licenses/by/4.0/.
ACKNOWLEDGMENTS
The authors would like to thank the following for
their financial support: JLB: the University of
Southampton’s Institute for Life Sciences (IfLS), and
EPSRC Doctoral Training Program (ref EP/N509747/
1). PRW, DLB: the EPSRC-NIHR ‘‘Medical Device
and Vulnerable Skin Network’’ (ref EP/N02723X/1),
ASD: the Royal Academy of Engineering, UK, (ref
RF/130). Ethics Committee approval for this protocol
was granted by the University of Southampton
(ERGO ID: 29696 and 41864). We would like to thank
all of the individuals who participated in this study.
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Tissue Composition and Load Response After Amputation
... In transtibial amputees, increases in limb stiffness have been recorded at the patellar tendon while decreases in limb stiffness are found in posterior and lateral positions. Residual limbs also have higher adipose composition compared with contralateral limbs [24]. If biological machinery allowing skin adaptation to loading exists within non-plantar skin, in the same manner observed in plantar skin, recordings of increased stratum corneum thickness and increased stiffness in indentation should be observed and contribute positively to load bearing. ...
... However, lower limb amputees suffer a disproportionately higher skin injury rate (65%) when compared with the general population [25]. It has been shown that in transtibial amputees there is muscle atrophy, increased adipose infiltration and subsequent softening of residual limbs with respect to intact contralateral limbs [24], but morphology was only recorded on the sub-dermal scale and not the epidermal scale. ...
... Our results indicate that residuum skin actually becomes softer in indentation as a result of prosthesis use (figure 2g), suggesting greater susceptibility to injury from device use owing to higher internal strains. A reduction of residuum mechanical properties has previously been reported in deep tissue with greater infiltrating adipose tissue in transtibial amputees and softer mechanics observed in the residuum than intact limbs [24]. Our findings support these previous observations, and show that this reduction in mechanical properties is also coupled with increased friction, a finding our results support across our recruitment sample of both transtibial and transfemoral amputees. ...
Article
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Following lower limb amputation residuum skin from the lower leg is used to reconstruct the residual limb. Unlike skin on the sole of the foot (plantar skin), leg skin is not inherently load bearing. Despite this, leg skin is required to be load bearing in the prosthetic socket. Current hypotheses propose that lower limb amputee skin can adapt to become load bearing with repeated prosthesis use. Here, we show using confocal Raman spectroscopy, mechanical characterization and cytokine analysis that adaptations occur which actually result in impaired barrier function, higher baseline inflammation, increased coefficient of friction and reduced stiffness. Our results demonstrate that repeated frictional trauma does not confer beneficial adaptations in amputee skin. We hypothesize that non-plantar skin lacks the biological capabilities to respond positively to repeated mechanical trauma in the same manner observed in plantar skin. This finding highlights the need for improved therapies as opposed to current mechanical conditioning or product solutions that directly relate to improving load-bearing capacity on the skin of lower limb amputees. This study also highlights the importance of measuring multiple parameters of application-specific skin at different scales for skin tribology applications.
... Secondary data analysis ethical approval was sought and granted by the University of Southampton's Ethics Committee (ERGO II 65748). Subject data consisted of MRI scans of 11 people with residual limbs from transtibial amputations using 3 different sources, collected in previously published research and/or provided to the authors under data sharing agreements [26], [27], [28]. The participants covered a range of amputation causes, age and time since amputation. ...
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Poor socket fit is the leading cause of prosthetic limb discomfort. However, currently clinicians have limited objective data to support and improve socket design. Prosthesis fit could be predicted by finite element analysis to help improve the fit, but this requires internal and external anatomy models. While external 3D surface scans are often collected in routine clinical computer aided design practice, detailed imaging of internal anatomy (e.g. MRI or CT) is not. This paper presents a prototype Statistical Shape Model (SSM) describing the transtibial amputated residual limb, generated using a sparse dataset of 10 MRI scans. To describe the maximal shape variance, training scans are size-normalised to their estimated intact tibia length. A mean limb is calculated, and Principal Component Analysis used to extract the principal modes of shape variation. In an illustrative use case, the model is interrogated to predict internal bone shapes given a skin surface shape. The model attributes ∼82% of shape variance to amputation height and ∼7.5% to soft tissue profile. Leave-One-Out cross-validation allows mean shape reconstruction with 0.5–3.1mm root-mean-squared-error (RMSE) surface deviation (median 1.0mm), and left-out-shape reconstruction with 4.8–8.9mm RMSE (median 6.1mm). Linear regression between mode scores from skin- only- and full-model SSMs allowed prediction of bone shapes from the skin surface with 4.9–12.6mm RMSE (median 6.5mm). The model showed the feasibility of predicting bone shapes from skin surface scans, which will enable more representative prosthetic biomechanics research, and address a major barrier to implementing simulation within clinical practice. Impact Statement The presented Statistical Shape Model answers calls from the prosthetics community for residual limb shape descriptions to support prosthesis structural testing that is representative of a broader population. The SSM allows definition of worst-case residual limb sizes and shapes, towards testing standards. Further, the lack of internal anatomic imaging is one of the main barriers to implementing predictive simulations for prosthetic ‘socket’ interface fitting at the point-of-care. Reinforced with additional data, this model may enable generation of estimated finite element analysis models for predictive prosthesis fitting, using 3D surface scan data already collected in routine clinical care. This would enable prosthetists to assess their design choices and predict a socket’s fit before fabrication, important improvements to a time-consuming process which comes at high cost to healthcare providers. Finally, few researchers have access to residual limb anatomy imaging data, and there is a cost, inconvenience, and risk associated with putting the small community of eligible participants through CT or MRI scanning. The presented method allows sharing of representative synthetic residual limb shape data whilst protecting the data contributors’ privacy, adhering to GDPR. This resource has been made available at https://github.com/abel-research/openlimb , open access, providing researchers with limb shape data for biomechanical analysis.
... These deformations of stump tissues will cause stress within these tissues 5 , potentially resulting in discomfort, pain, and tissue breakdown. Over time, these issues could lead to disuse and reduced functioning 2,5 . ...
... These deformations of stump tissues will cause stress within these tissues 5 , potentially resulting in discomfort, pain, and tissue breakdown. Over time, these issues could lead to disuse and reduced functioning 2,5 . ...
Article
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Transtibial prosthetic users do often struggle to achieve an optimal prosthetic fit, leading to residual limb pain and stump-socket instability. Prosthetists face challenges in objectively assessing the impact of prosthetic adjustments on residual limb loading. Understanding the mechanical behaviour of the pseudo-joint formed by the residual bone and prosthesis may facilitate prosthetic adjustments and achieving optimal fit. This study aimed to assess the feasibility of using B-mode ultrasound to monitor in vivo residual bone movement within a transtibial prosthetic socket during different stepping tasks. Five transtibial prosthesis users participated, and ultrasound images were captured using a Samsung HM70A system during five dynamic conditions. Bone movement relative to the socket was quantified by tracking the bone contour using Adobe After-Effect. During the study a methodological adjustment was made to improve data quality, and the first two participants were excluded from analysis. The remaining three participants exhibited consistent range of motion, with a signal to noise ratio ranging from 1.12 to 2.59. Medial–lateral and anterior–posterior absolute range of motion varied between 0.03 to 0.88 cm and 0.14 to 0.87 cm, respectively. This study demonstrated that it is feasible to use B-mode ultrasound to monitor in vivo residual bone movement inside an intact prosthetic socket during stepping tasks.
... Extraneous adipose tissue in residual muscle could have filtered EMG and reduced MU sizes recorded. There can be a higher percentage of adipose tissue infiltrating residual muscle compared to intact muscle, but large intersubject variability exists [90]. Studies measuring tissue composition with MU behavior are needed to determine if this effect is significant compared to other factors discussed. ...
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Objective. Neural signals in residual muscles of amputated limbs are frequently decoded to control powered prostheses. Yet myoelectric controllers assume muscle activities of residual muscles are similar to that of intact muscles. This study sought to understand potential changes to motor unit (MU) properties after limb amputation. Approach. Six people with unilateral transtibial amputation were recruited. Surface electromyogram (EMG) of residual and intact tibialis anterior (TA) and gastrocnemius (GA) muscles were recorded while subjects traced profiles targeting up to 20% and 35% of maximum activation for each muscle (isometric for intact limbs). EMG was decomposed into groups of MU spike trains. MU recruitment thresholds, action potential amplitudes (MU size), and firing rates were correlated to model Henneman’s size principle, the onion-skin phenomenon, and rate-size associations. Organization (correlation) and modulation (rates of change) of relations were compared between intact and residual muscles. Main results. The residual TA exhibited significantly lower correlation and flatter slopes in the size principle and onion-skin, and each outcome covaried between the MU relations. The residual GA was unaffected for most subjects. Subjects trained prior with myoelectric prostheses had minimally affected slopes in the TA. Rate-size association correlations were preserved, but both residual muscles exhibited flatter decay rates. Significance. We showed peripheral neuromuscular damage also leads to spinal-level functional reorganizations. Our findings suggest models of MU recruitment and discharge patterns for residual muscle EMG generation need reparameterization to account for disturbances observed. In the future, tracking MU pool adaptations may also provide a biomarker of neuromuscular control to aid training with myoelectric prostheses.
... Although a small effect, some EMG information 515 in the GA may have been contaminated with synaptic inputs 516 unrelated to torque output in the intact limb task. Similarly, 517 for residual muscles, we attempted to minimize crosstalk in 518 our sensor placement, but following conventional surgeries, 519 antagonist muscles can be closer in proximity with greater 520 proportions of local subcutaneous adipose tissue compared 521 to intact muscle [42]. Together, there is a higher probability 522 of crosstalk occurring compared to intact muscles [43], [44]. ...
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There has been increased interest in using residual muscle activity for neural control of powered lower-limb prostheses. However, only surface electromyography (EMG)-based decoders have been investigated. This study aims to investigate the potential of using motor unit (MU)-based decoding methods as an alternative to EMG-based intent recognition for ankle torque estimation. Eight people without amputation (NON) and seven people with amputation (AMP) participated in the experiments. Subjects conducted isometric dorsi- and plantarflexion with their intact limb by tracing desired muscle activity of the tibialis anterior (TA) and gastrocnemius (GA) while ankle torque was recorded. To match phantom limb and intact limb activity, AMP mirrored muscle activation with their residual TA and GA. We compared neuromuscular decoders (linear regression) for ankle joint torque estimation based on 1) EMG amplitude (aEMG), 2) MU firing frequencies representing neural drive (ND), and 3) MU firings convolved with modeled twitch forces (MUDrive). In addition, sensitivity analysis and dimensionality reduction of optimization were performed on the MUDrive method to further improve its practical value. Our results suggest MUDrive significantly outperforms (lower root-mean-square error) EMG and ND methods in muscles of NON, as well as both intact and residual muscles of AMP. Reducing the number of optimized MUDrive parameters degraded performance. Even so, optimization computational time was reduced and MUDrive still outperformed aEMG. Our outcomes indicate integrating MU discharges with modeled biomechanical outputs may provide a more accurate torque control signal than direct EMG control of assistive, lower-limb devices, such as exoskeletons and powered prostheses.
... Prior work has demonstrated that high levels of fatty infiltration (i.e., non-contractile tissue) within musculature impair muscle strength and functional performance [18,19,28,39,51]. Quantification of muscular fatty infiltration within the TFA population is lacking, though prior work within the transtibal population has demonstrated increased fatty infiltration of the amputated limb musculature [8]. In patients with TFA, a previous study by Sherk et al. showed increased fatty infiltration in distal residual limb musculature [46]; however, distal residual limb musculature contributes minimally to hip joint loading. ...
Article
Patients with transfemoral amputation (TFA) are at an increased risk of secondary musculoskeleteal comorbidities, primarily due to asymmetric joint loading. Amputated limb muscle weakness is also prevalent in the TFA population, yet all factors that contribute to muscle strength and thus joint loading are not well understood. Our objective was to bilaterally compare gluteus medius (GMED) muscle factors (volume, fatty infiltration, moment arm) that all contribute to joint loading in patients with TFA. Quantitative magnetic resonance (MR) images of the hip were collected from eight participants with unilateral TFA (2M/6F; age: 47.3 ± 14.7 y/o; BMI: 25.4 ± 5.3 kg/m2; time since amputation: 20.6 ± 15.0 years) and used to calculate normalized GMED muscle volume and fatty infiltration. Six participants participated in an instrumented gait analysis session that collected whole-body kinematics during overground walking. Subject-specific musculoskeletal models were used to calculate bilateral GMED (anterior, middle, posterior) moment arms and frontal plane hip joint angles across three gait cycles. Differences in volume, fatty infiltration, hip adduction–abduction angle, and peak moment arms were compared between limbs using paired Cohen’s d effect sizes. Volume was smaller by 36.3 ± 18.8% (d = 1.7) and fatty infiltration was greater by 6.4 ± 7.8% (d = 0.8) in the amputated limb GMED compared to the intact limb. The amputated limb GMED abduction moment arms were smaller compared to the intact limb for both overground walking (anterior: d = 0.9; middle: d = 0.1.2) and during normal range of motion (anterior: d = 0.8; middle: d = 0.8) while bilateral hip adduction–abduction angles were similar during overground walking (d = 0.5). These results indicate that in patients with TFA, the amputated limb GMED is biomechanically disadvantaged compared to the intact limb, which may contribute to the etiology of secondary comorbidities. This population might benefit from movement retraining to lengthen the amputated limb GMED abduction moment arm during gait.
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The formation of a functional tibial stump after combat injuries with extensive tissue damage is sometimes difficult. We describe a case of reconstruction of the tibial stump after a mine-blast injury. In this case, the fibula was completely removed as a result of fracture, and the tibia was amputated at the border of the upper and middle thirds. To create a stable platform with a larger bearing surface area and reduce the load on the distal fossa, the Ilizarov method was used. For the first time, the area of the bearing surface of the tibia stump was increased by more than 2 times in the case of the removed fibula. Thanks to the original surgery technique, the mushroom shape of the stump end was also obtained for the first time. In the process of prosthetics, this geometry actually increases the bearing surface area and has advantages over the Ertl technique, where the cylindrical end of the stump due to muscle atrophy and thinning of the fibro-skin lining can lead to bursitis and even ulcers. The spherical shape of the stump end causes less soft tissue trauma, increases the load-bearing capacity and durability of the results. According to the data of the GaitRite system, the walking performance in the long-term period practically corresponded to that of a healthy person. The technique of the operation is described in detail, including petal decortication, two oblique corticotomies of the tibia, formation of bone and periosteum fragments, distraction. The result is a highly functional stump with the possibility of using end support and full prosthetics. The proposed technique can be used in reconstructive operations on the tibia and femur stumps.
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BACKGROUND: The timely provision of load-bearing prostheses significantly reduces healthcare costs and lowers post-amputation mortality risk. However, current methods for assessing residuum health remain subjective, underscoring the need for standardized, evidence-based approaches incorporating physical biomarkers to evaluate residual limb healing and determine readiness for prosthetic rehabilitation. OBJECTIVE(S): This review aimed to identify predictive, diagnostic, and indicative physical biomarkers of healing of the tissues and structures found in the residual limbs of adults with amputation. METHODOLOGY: A scoping review was conducted following Joanna Briggs Institute (JBI) and PRISMA-ScR guidance. Searches using “biomarkers”, “wound healing”, and “amputation” were performed on May 6, 2023, on Web of Science, Ovid MEDLINE, Ovid Embase, Scopus, Cochrane, PubMed, and CINAHL databases. Inclusion criteria were: 1) References to physical biomarkers and healing; 2) Residuum tissue healing; 3) Clear methodology with ethical approval; 4) Published from 2017 onwards. Articles were assessed for quality (QualSyst tool) and evidence level (JBI system), and categorized by study, wound, and model type. Physical biomarkers that were repeated not just within categories, but across more than one of the study categories were reported on. FINDINGS: The search strategy identified 3,306 sources, 157 of which met the inclusion criteria. Histology was the most frequently repeated physical biomarker used in 64 sources, offering crucial diagnostic insights into cellular healing processes. Additional repeated indicative and predictive physical biomarkers, including ankle-brachial index, oxygenation measures, perfusion, and blood pulse and pressure measurements, were reported in 25, 19, 13, and 12 sources, respectively, providing valuable data on tissue oxygenation and vascular health. CONCLUSION: Ultimately, adopting a multifaceted approach that integrates a diverse array of physical biomarkers (accounting for physiological factors and comorbidities known to influence healing) may substantially enhance our understanding of the healing process and inform the development of effective rehabilitation strategies for individuals undergoing amputation. Layman's Abstract Providing prosthetic limbs soon after amputation reduces healthcare costs and lowers mortality risk. However, current methods for evaluating the health of the remaining limb often rely on subjective judgment, highlighting the need for a standardized, evidence-based approach using physical biomarkers to assess healing and readiness for prosthetics. This review aimed to identify physical biomarkers that can predict, diagnose, or indicate healing in amputated limbs. On May 6, 2023, a comprehensive review was conducted across multiple databases, including Web of Science, Ovid MEDLINE, Ovid Embase, Scopus, Cochrane, PubMed, and CINAHL, to find studies using search terms like “biomarkers”, “wound healing”, and “amputation”. To be included, studies had to focus on biomarkers related to healing in residual limbs, use clear research methods, have ethical approval, and be published after 2017. The quality of the studies was evaluated, and biomarkers found across multiple studies were reported. Of 3,306 sources identified, 157 focused on physical biomarkers, with histology (tissue analysis) being the most commonly reported, allowing healing progress to be diagnosed at the cellular level. Other frequently mentioned biomarkers included the ankle-brachial index and oxygenation measures, which are used to assess tissue oxygen levels and blood flow, therefore predicting or indicating healing. Using a combination of different physical markers (while considering things like overall health and existing medical conditions) can give us a much better understanding of how healing works. This approach can also help create more effective rehabilitation plans for people who have had an amputation. Article PDF Link: https://jps.library.utoronto.ca/index.php/cpoj/article/view/43716/33400 How To Cite: Williams-Reid H, Johannesson A, Buis A. Wound management, healing, and early prosthetic rehabilitation: Part 2 - A scoping review of physical biomarkers. Canadian Prosthetics & Orthotics Journal. 2024; Volume 7, Issue 2, No.3. https://doi.org/10.33137/cpoj.v7i2.43716 Corresponding Author: Professor Arjan Buis, PhDDepartment of Biomedical Engineering, Faculty of Engineering, University of Strathclyde, Glasgow, Scotland.E-Mail: arjan.buis@strath.ac.ukORCID ID: https://orcid.org/0000-0003-3947-293X
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BACKGROUND: Following lower limb amputation, timely prosthetic fitting enhances mobility and quality of life. However, inconsistent definitions of surgical site healing complicate prosthesis readiness assessment and highlight the need for objective wound management measures. OBJECTIVE: This review aimed to compile definitions of healing and non-healing provided in the literature investigating biomarkers of healing of the tissues and structures found in the residual limbs of adults with amputation. METHODOLOGY: A scoping review was conducted following JBI and PRISMA-ScR guidance. Searches using “biomarkers,” “wound healing,” and “amputation” were performed on May 6, 2023, on Web of Science, Ovid MEDLINE, Ovid Embase, Scopus, Cochrane, PubMed, and CINAHL databases. Inclusion criteria were: 1) References to biomarkers and healing; 2) Residuum tissue healing; 3) Clear methodology with ethical approval; 4) Published from 2017 onwards. Articles were assessed for quality (QualSyst tool) and evidence level (JBI system). FINDINGS: Of 3,306 articles screened, 219 met the inclusion criteria and are reviewed in this article, with 77% rated strong quality. 43% of all included sources did not define healing, while the remainder used specific criteria including epithelialization (14%), wound size reduction (28%), gradings scales (3%), scarring (1%), absence of wound complications (2%), hydroxyproline levels (0.5%), no amputation (0.5%), or neovascularization (0.5%). 84% of included sources did not provide definitions of non-healing. Studies defining non-healing used criteria like wound complications (4%), the need for operative interventions (4%), or lack of wound size reduction (1%). For 10% of included sources, healing and non-healing definitions were considered not applicable given the research content. Total percentages exceed 100% for both healing and non-healing definitions because some sources used two definition classifications, such as epithelialization and wound size reduction. The findings indicate a lack of standardized definitions irrespective of study type. CONCLUSION: This review reveals significant gaps in current definitions of healing and non-healing, often based on superficial assessments that overlook deeper tissue healing and mechanical properties essential for prosthesis use. It emphasizes the need for comprehensive definitions incorporating biomarkers and psychosocial factors to improve wound management and post-amputation recovery. Layman's Abstract After a lower limb amputation, early prosthetic fitting can significantly improve quality of life. However, different definitions of surgical site healing make deciding when a prosthetic can be used difficult. This scoping review collected and compared definitions of healing and non-healing found in research about biological markers (biomarkers) that are used for tracking residual limb healing. On May 6, 2023, searches were conducted using terms like “biomarkers,” “wound healing,” and “amputation” across several databases. Studies were included if they discussed biomarkers, focused on residual limb healing, had clear methods and ethical approval, and were published during or after 2017. Of 3,306 articles screened, 219 met the criteria, with 77% rated as high quality. 43% of the included sources did not define healing. Definitions provided included new skin growth (14%), reduction in wound size (28%), grading scales (3%), scarring (1%), no complications (2%), hydroxyproline levels (0.5%), no need for amputation (0.5%), or new blood vessel formation (0.5%). 84% of sources did not define non-healing, with the remainder based on healing complications (4%), the need for more surgery (4%), or no reduction in wound size (1%). In 10% of included sources healing and non-healing definitions were considered not relevant to their research. Total percentages for healing and non-healing definitions exceeds 100% because some sources used two definitions, for example, new skin growth and reduction in wound size. Overall, the review shows gaps in definitions, many of which are too basic and ignore deeper tissue healing and factors needed for prosthetic use. More thorough definitions that include the physical, mental, and social sides of healing are needed to improve recovery. Article PDF Link: https://jps.library.utoronto.ca/index.php/cpoj/article/view/43715/33312 How To Cite: Williams-Reid H, Johannesson A, Buis A. Wound management, healing, and early prosthetic rehabilitation: Part 1 - A scoping review of healing and non-healing definitions. Canadian Prosthetics & Orthotics Journal. 2024; Volume 7, Issue 2, No.1. https://doi.org/10.33137/cpoj.v7i2.43715 Corresponding Author: Professor Arjan Buis, PhDDepartment of Biomedical Engineering, Faculty of Engineering, University of Strathclyde, Glasgow, Scotland.E-Mail: arjan.buis@strath.ac.ukORCID ID: https://orcid.org/0000-0003-3947-293X
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Study aim : This study aimed to investigate the influence of combined plyometric and resistance training of lower limbs when administered for a shorter duration of six weeks on the stiffness of Achilles and patellar tendons as well as the jump height. Materials and methods: Twenty recreational athletes were administered six weeks of a single session of lower limb resistance training and one session of plyometric training every week for a total duration of six weeks. Tendon stiffness was measured using MyotonPro, and vertical jump height was derived from the force plate at baseline and six weeks after the intervention. Results: There was a statistically significant difference (p < 0.01) between the baseline and post-training measures of patellar and Achilles tendons stiffness as well as the squat jump (SJ) and countermovement jump (CMJ) height. Conclusion : Both resistance and plyometric training may be incorporated into the training session as combined training showed significant improvements in jump height and tendon stiffness after six weeks of combined RT and PT.
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The present study was performed to assess the relationship between hand-held myotonometer MyotonPRO and shear wave elastography (SWE) measurements of lower limb muscle stiffness during resting and active voluntary contraction. Forty healthy young adults, (20 males and 20 females) participated in the study. The stiffness of each subject’s rectus femoris (RF), biceps femoris (BF), tibialis anterior (TA), and medial gastrocnemius (MG) was measured repeatedly by MyotonPRO and SWE. Moderate to strong correlations between the two methods’ measurements were found for both resting and active voluntary contraction. (r = 0.416–0.669, p < 0.05; r = 0.398–0.594, p < 0.05, respectively). Muscle stiffness at rest was significantly lower compared contraction in all four muscles measured by both methods (p < 0.05). Intra-rater reliabilities were generally lower when measurements were taken during contraction. Additionally, when compared by gender, muscle stiffness measured by MyotonPRO was significantly higher at rest in men compared to women, except for the TA. However, a significant difference was found in TA muscle stiffness by gender when measured with SWE. When muscles were contracted, all muscles showed significantly higher stiffness in men compared to women. There were moderate to good correlations in muscle stiffness between measurements of SWE and MyotonPRO at rest and during active voluntary contraction. Additionally, both instruments showed good intra-rater reliability.
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Background: The soft tissue of the residual limb in transtibial prosthetic users encounters unique biomechanical challenges. Although not intended to tolerate high loads and deformation, it becomes a weight-bearing structure within the residuum-prosthesis-complex. Consequently, deep soft tissue layers may be damaged, resulting in Deep Tissue Injury (DTI). Whilst considerable effort has gone into DTI research on immobilised individuals, only little is known about the aetiology and population-specific risk factors in amputees. This scoping review maps out and critically appraises existing research on DTI in lower-limb prosthetic users according to (1) the population-specific aetiology, (2) risk factors, and (3) methodologies to investigate both. Results: A systematic search within the databases Pubmed, Ovid Excerpta Medica, and Scopus identified 16 English-language studies. The results indicate that prosthetic users may be at risk for DTI during various loading scenarios. This is influenced by individual surgical, morphological, and physiological determinants, as well as the choice of prosthetic componentry. However, methodological limitations, high inter-patient variability, and small sample sizes complicate the interpretation of outcome measures. Additionally, fundamental research on cell and tissue reactions to dynamic loading and on prosthesis-induced alterations of the vascular and lymphatic supply is missing. Conclusion: We therefore recommend increased interdisciplinary research endeavours with a focus on prosthesis-related experimental design to widen our understanding of DTI. The results have the potential to initiate much-needed clinical advances in surgical and prosthetic practice and inform future pressure ulcer classifications and guidelines.
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Background: Strength and coordination of lower muscle groups typically identified in healthy subjects are two prerequisites to performing functional activities. These physical qualities can be impaired following a neurological insult. A static dynamometer apparatus that measures lower limb joint moments during directional efforts at the foot was developed to recruit different patterns of muscular activity. The objectives of the present study were to 1) validate joint moments estimated by the apparatus, and 2) to characterize lower limb joint moments and muscular activity patterns of healthy subjects during progressive static efforts. Subjects were seated in a semi-reclined position with one foot attached to a force platform interfaced with a laboratory computer. Forces and moments exerted under the foot were computed using inverse dynamics, allowing for the estimation of lower limb joint moments.To achieve the study's first objective, joint moments were validated by comparing moments of various magnitudes of force applied by turnbuckles on an instrumented leg equipped with strain gauges with those estimated by the apparatus. Concurrent validity and agreement were assessed using Pearson correlation coefficients and Bland and Altman analysis, respectively. For the second objective, joint moments and muscular activity were characterized for five healthy subjects while exerting progressive effort in eight sagittal directions. Lower limb joint moments were estimated during directional efforts using inverse dynamics. Muscular activity of eight muscles of the lower limb was recorded using surface electrodes and further analyzed using normalized root mean square data. Results: The joint moments estimated with the instrumented leg were correlated (r > 0.999) with those measured by the dynamometer. Limits of agreement ranged between 8.5 and 19.2% of the average joint moment calculated by both devices. During progressive efforts on the apparatus, joint moments and patterns of muscular activity were specific to the direction of effort. Patterns of muscular activity in four directions were similar to activation patterns reported in the literature for specific portions of gait cycle. Conclusion: This apparatus provides valid joint moments exerted at the lower limbs. It is suggested that this methodology be used to recruit muscular activity patterns impaired in neurological populations.
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The prevalence of pressure ulcers in patients with spinal cord injuries has been estimated to be between 30% and 47%. Individuals with spinal cord injuries sit for a majority of the time, increasing the risk of developing pressure ulcers in the buttocks and thighs due to large internal stresses. Human body models have been developed to study the formation of pressure ulcers, yet a persistent limitation in these models has been the material properties used to represent the soft tissues in the buttocks and thighs. Specifically, soft tissue material property data have not included wheelchair users, such as those with spinal cord injuries. The goals of this research were 1) to determine the in-vivo material properties of soft tissue in the thighs and buttocks of individuals with spinal cord injuries and 2) compare these to properties obtained from able-bodied people. Results indicated that the proximal and middle thigh regions of those who had a spinal cord injury were softer than the same regions as able-bodied individuals, while the distal thigh regions were stiffer. These findings are vital because they indicate that models developed using properties from able-bodied individuals will not produce internal stress or strain magnitudes that represent individuals who have a spinal cord injury. This information suggests that models should obtain material property data sets from their desired population. Human body models must represent the population being studied if they are to inform clinical assessments and make accurate patient predictions.
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The human–prosthesis interface is one of the most complicated challenges facing the field of prosthetics, despite substantive investments in research and development by researchers and clinicians around the world. The journal of the International Society for Prosthetics and Orthotics, Prosthetics and Orthotics International, has contributed substantively to the growing body of knowledge on this topic. In celebrating the 50th anniversary of the International Society for Prosthetics and Orthotics, this narrative review aims to explore how human–prosthesis interfaces have changed over the last five decades; how research has contributed to an understanding of interface mechanics; how clinical practice has been informed as a result; and what might be potential future directions. Studies reporting on comparison, design, manufacturing and evaluation of lower limb prosthetic sockets, and osseointegration were considered. This review demonstrates that, over the last 50 years, clinical research has improved our understanding of socket designs and their effects; however, high-quality research is still needed. In particular, there have been advances in the development of volume and thermal control mechanisms with a few designs having the potential for clinical application. Similarly, advances in sensing technology, soft tissue quantification techniques, computing technology, and additive manufacturing are moving towards enabling automated, data-driven manufacturing of sockets. In people who are unable to use a prosthetic socket, osseointegration provides a functional solution not available 50 years ago. Furthermore, osseointegration has the potential to facilitate neuromuscular integration. Despite these advances, further improvement in mechanical features of implants, and infection control and prevention are needed.
Article
Introduction: Mechanically induced skin breakdown is a significant problem for many lower-limb prosthesis users. It is known that skin can adapt to the mechanical stresses of prosthesis use thereby reducing the risk of breakdown, yet little is understood about the biology behind skin adaptation. This is a proof-of-concept study for the use of novel, noninvasive optical coherence tomography (OCT) imaging techniques to investigate skin adaptation. Methods: Two OCT imaging-based tests were used to evaluate features of the skin that may be involved in adaptation to limb-socket interface stresses. The tests were used to assess the function and structure of the cutaneous microvasculature, respectively. Epidermal thickness was also quantified. Tests were run on three lower-limb prosthesis users in a region of the residual limb believed to be highly stressed within the prosthetic socket. The measurements were compared with measurements taken at a location-matched site on the contralateral limb. Results: Two of three participants demonstrated a faster time-to-peak and larger peakmagnitude reactive hyperemia response in their residual limb compared with their contralateral limb. Two of three participants also demonstrated a larger magnitude vessel density at maximum dilation in their residual limb versus contralateral limb. The epidermal thickness was greater in the residual limb versus contralateral limb for all participants. Conclusions: This study demonstrated the utility of two novel OCT imaging techniques for investigating skin adaptation in users of lower-limb prostheses. If we are able to confirm these findings on a larger subject population, we will better understand the biology behind mechanically induced skin adaptation. These findings, along with the noninvasive OCT imaging methods introduced here, would have the potential to improve clinical practice by enabling the development of rehabilitation techniques and therapeutics to better strengthen skin, thereby reducing the incidence of harmful skin breakdown.
Article
Background Skin breakdown due to limb‐socket interface stress is a significant problem for lower limb prosthesis users. While it is known that skin can adapt to stress to become more resistant to breakdown, little is understood about skin adaptation and few methods exist to noninvasively investigate it. In this study, we present novel, noninvasive imaging methods using Optical Coherence Tomography (OCT) to assess key features of the cutaneous microvasculature that may be involved in skin adaptation. Materials and Methods Eight able‐bodied participants wore a modified below‐knee prosthetic socket for two weeks to stress the skin of their lower limb. Two OCT‐based imaging tests were used to assess the function and structure, respectively, of the cutaneous microvasculature at multiple time points throughout the socket wear protocol. Results A measurable reactive hyperemia response was reliably induced in the skin of study participants in the vascular function assessment test. The vascular structure assessment demonstrated excellent field‐of‐view repeatability, providing rich data sets of vessel structure. No statistically significant differences were found in any of the measurements when compared between time points of the adaptation protocol. The participants’ limbs were likely not stressed enough by the able‐bodied socket to induce measurable skin adaptation. Conclusion This study introduced new techniques to investigate skin adaptation to mechanical stress. If the key limitations are addressed, these methods have the potential to provide insight into the function and structure of the cutaneous microvasculature that previously could not be attained noninvasively.
Article
Secondary analysis of a cross-sectional observation study. To determine the relationship between skin ultrasound images and muscle damage in wheelchair basketball athletes, using skin blotting examinations of the ischial regions. Community, Japan. Fourteen elite wheelchair basketball athletes were recruited. We obtained data regarding participants’ characteristics. We undertook ultrasonographic images and quantitative skin blotting of the ischial region before and after training, and after rest. We identified Category II and III pressure injuries in 2 of the 12 participants. Structural features were classified into four categories based on ultrasonographic features, namely, normal skin structure, unclear superficial and deep fascia, cloudy fat layer, and fat infiltration and low-echoic lesion/anechoic lesions. The muscle-type creatinine kinase (CK-M) level (median [interquartile range: IQR], 2.98 [2.80–3.47]) in the fat infiltration and low-echoic lesion/anechoic lesion group was significantly higher (1.43 [1.41–1.49]) than in a nonfat infiltration and low-echoic lesion/anechoic lesion group after training (p = 0.03). The interleukin-6 (IL-6) level (median [IQR], 23.5 [16.15–58.97]) in the fat infiltration and low-echoic lesion/anechoic lesion group was significantly higher (1.94 [1.74–4.44]) than in the nonfat infiltration and low-echoic lesion/anechoic lesion group after rest (mean difference = −25.4, 95% CI −61.1 to 10.7, p = 0.03). The combination of ultrasonographic images and skin blotting using CK-M and IL-6, could detect early deep tissue damage in wheelchair athletes. These techniques could be potentially useful in the treatment and prevention of pressure injuries. This study was supported in part by YAMAHA Motor Foundation for Sports.
Article
Background: post-amputation, residual limb soft tissues have not been mechanically conditioned to support load and are vulnerable to damage from prosthetic use. However, there is limited quantitative knowledge of skin and soft tissue response to prosthetic loading. Methods: an in-vivo protocol was developed to establish suitable measures to assess tissue tolerance during loading representative of early prosthesis use. Ten participants without amputation were recruited, with pressure applied to their calf in increments from 20 to 60 mmHg. Measurements were recorded at relevant skin sites, including interface pressures, transcutaneous oxygen (TCPO2) and carbon dioxide (TCPCO2) tensions and the inflammatory biomarkers. Findings: at the maximum cuff pressure, mean interface pressures were between 66-74 mmHg, associated with decreased TCPO2 values. On the release of pressure, the ischaemic response was reversed. Significant upregulation (p<0.05) in an inflammatory biomarker, IL-1α, and its antagonist, IL-1RA, were observed at all sites immediately following loading. Interpretation: the protocol was successful in applying representative prosthetic loads to lower limb tissues and monitoring the physiological response, both in terms of tissue ischemia and skin inflammation. Results indicated that the measurement approaches were sensitive to changes in interface conditions, offering a promising approach to monitor tissue status for people with amputation.