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46 D. Dixon and M. Edmonds
prevention of amputations may be facilitated by individual therapeutic
innovations in technology, such advances have to be co-ordinated into organised
multidisciplinary treatment of the diabetic foot ulcer to realistically benefit the
patient.
Keywords
Foot ulcerNeuropathyDiagnosisTreatmentRisk factorsPlantar pressure
Skin temperature Fluorescence
Introduction
The diabetic foot is one of the most destructive complications of diabetes. Foot
complications in diabet es are considered a leading cause of the global burden of
disability (Lazzarini et al. 2018). In the United Kingdom Diabetic foot problems are
the most frequent cause of diabetes related admission to hospital (Kerr et al. 2014).
Two overwhelming pathologi es come together in the diabetic foot: neuropathy and
ischaemia, which result in the characteristic features of neuropathic and ischaemic
foot ulceration: 19–34% of people with diabetes will encounter a diabetic foot ulcer
(DFU) at least once in their life. More than 50% of these people wi ll have a
recurrence within three years (Armstrong et al. 2017).
Almost 25% of diabetic foot ulcers lead to some form of amputation. Every 20 s,
a lower limb is amputated due to diabetes and 84% of all amputations in persons
with diabetes are preceded by a foot ulcer (Pecoraro et al. 1990). Overall, the risk of
a person with diabetes having a lower extremity amputation is reckoned to be 23
times that of a person without diabetes (Brownrigg et al. 2013). The prevalence of
major amputation has been reported as 1.6% in the age range 18–44 years, 3.4% in
those aged 45–64 years, and 3.6% in persons older than 65 years (Katsilambros
et al. 2011)
lower limb amputations were reported in England between 2017 and 2020 (Public
Health England 2021). Furthermore, the cost of health care for ulceration and
amputation in diabetes has been estimated at almost one billion pounds per year
(Digital 2019).
Persons with
twenty-first century facing a continual challenge to avoid ulceration and amputation. There has always been a continuous drive to improve diabetic foot care and
this chapter discusses the evidence for the contribution of technology to the prevention and treatment of diabetic foot ulceration. The objective is to highlight
where technology has played an important role in diagnosis as well as treatment.
The effect of the Covid 19 pandemic on accelerating the development of techno logy
with respect to foot care will also be considered. Although neuropathy and
ischaemia are important pathologies leading to different subgroups of the diabetic
even-thousand nine-hundred and fifty-seven (7957) major diabetic
. S
diabetes and their health care professionals find themselves in the
The Diabetic Foot, Its Complications, Role of Technology … 47
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foot, namely the neuropathic foot, the neuroischaemic foot and ischaemic foot, this
chapter will concentrate mainly on the value of technological advances in the
diagnosis and treatment of the neuropathic foot ulcer/wound although there is some
overlap with the neuroischaemic foot. The use of technology in the assessment and
management of the ischaemic foot is considered in the chapter on the role of
technology in managing vascular wounds.
Overall,this
terms “ulcer” and “wound” are used interchangeably.
the
chapte
r isdivided
into
twoparts:
diagno
sis
and
manag
ement
and
Diagnosis
In this section, evidence for the usefulness of technology will be discussed in the
• Assessment of neuropathy as a predisposing factor to ulceration,
• Measurement of pressure abnormalities of the foot as precipitants of ulceration,
• Detection of skin temperature rise as an immediate prelude to ulceration,
• Characterisation of infection, which often complicates ulceration.
Assessment of Neuropathy as a Predisposing Factor
to Ulceration
Neuropathy is one of the most common complications of diabetes (International
Diabetes Federation 2017). Almost 90% of diabetic foot ulcers are due to neuropathy or neuropathy with ischaemia (Mottolini 2022). The peripheral nervous
system essentially acts as an alarm system and is programmed to respond to
maintain homeostasis in the presence of internal faults or external injuries
(Edmonds and Foster 2014). Thus, it is important to detect neuropathy so that
patients and their carers can be warned that they have lost nature’s protection and
will not sense external or internal insults.
Although neuropathy may present with tingling and a feeling of numbness, it is
asymptomatic in the majority of patients and neuropathy will only be detected by
clinical examination and investigations. However, clinical examination will only
detect signs of neuropathy late in the natural history of neuropathy. Technology has
been introduced to detect and measure subclinical neuropathy and thus to warn
patients and inform the health c are professionals of the presence of early nerve
damage Furthermore technology allows the characterisation of the neuropathy.
Peripheral nerve fibre impairment can be classified into large and small fibre
neuropathy according to the involvement of large myelinated fibres or small
unmyelinated fibres.
48 D. Dixon and M. Edmonds
Use of Technology to Assess Large Fibre Neuropathy
Large nerve fibres are heavily myelinated and include A-alpha fibres, which
mediate motor strength, and A-beta fibres, which convey vibratory and touch
sensation and proprioception. Medium-sized fibres, known as A-gamma fibres, are
also myelinated and carry messages to muscle spindles. Large fibre loss can be
identified using a monofilament or a vibratory stimulus.
Monofilament
Large fibre impairment can be detected using a 10 g monofilament which, when
applied perpendicular to the foot, buckles at a given force of 10 g. Ability to feel
that level of pressure ensures protective sensation against foot ulceration. The 10 g
monofilament has been shown to have a sensitivity between 41 and 93%, and
specificity between 68 and 100% in the detection of distal sensory peripheral
neuropathy (Dros et al. 2009). In addition, it allows for the detection of loss of
protective sensation and thus the foot at-risk of ulceration. Insensitivity to 10 g
monofilament has been shown to confer a 1.8–7.7 times increased risk of diabetic
foot ulceration (Tan 2010). The number of sites used differs according to different
protocols. Sites examined include the plantar aspects of the first toe, the first, third
and fifth metatarsal heads, the plantar surface of the heel and the dorsum of the foot.
The filament should not be applied at any site until callus has been removed. If the
patient cannot feel the filament at any of the tested areas, then protective pain
sensation is lost, indicating susceptibility to foot ulceration The 10 g monofilament
may become inaccurate after use on many occasions and should be replaced regularly. A study to test the longevity and recovery of monofilaments was carried out
using a calibrated load cell. Each monofilament was subjected to 10 mechanical
bucklings. The monofilaments were mounted vertically and were compressed in the
vertical plane by 10 mm while the load cell detected the maximal buckling force.
Longevity was tested by subjecting them to continuous compression until the
buckling force was less than 9 g. The study suggested that after use on 10 consecutive patients, the monofilament needed 24 h recovery time before further usage
to maintain diagnostic accuracy’ (Booth and Young 2000).
Vibration Perception Threshold (VPT)
on perception threshold (VPT) is a measure of large fibre function that can
Vibrati
be semi quantified by the use of the neurothesiometer. It increases with age and thus
should be corrected for age. Standards for normal subjects, their satisfactory
reproducibility and relationship to age has been described. VPT has a sensitivity of
70% for the detection of mild distal sensory peripheral neuropathy and a VPT of
>25 V has been shown to give an 8 times increased risk for developing neuropathic
foot ulceration, compared to a VPT of <15 V (Young et al. 1994)
.
The Vibratip™ is a small electronic vibratory device, with an amplitude and
frequency similar to a 128 Hz tuning fork, and has also been shown to be comparable to the monofilament and therefore could be considered as an alternative for
peripheral neuropathy assessment (Willits et al. 2015).
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Finally, electrophysiological studies can demonstrate loss of large myelinated
fibres as decreased or absent sensory nerve action potentials or mild slowing of
conduction ve locity in sensory nerves but these demand the skills and technologies
of the electrophysiologist.
Use of Technology to Assess Small Fibre Neuropathy
Small fibres include myelinated A-delta fibres which subserve cold perception, pain
and autonomic impulses and unmyelinated C fibres which transmit warm perception, pain and autonomic impulses. These fibres innervate skin (somatic fibres) and
involuntary muscles, including cardiac and smooth muscles (autonomic fibres).
Small fibre neuropathy is the selective impairment of small myelinated A-delta and
unmyelinated C fibres. It is characterised by impairment of pain and temperature
sensation. Autonomic fibres are commonly affected together with small somatic
fibres. Investigations for small fibre neuropathy include:
• Quantitative sensory tests of thermal and pain perception which can provide a
temperature perception threshold to hot and cold and thermal pain (Shy et al.
2003) include Axon-reflex mediated microvascular flare response (LDI flare) to
identify between endothelium and non-endothelium dependent responses (Vas
and Rayman 2013).
• Skin biopsy with measurement of intraepidermal nerve fibre density (IENFD)
which allows for the assessment of small fibre structural abnormalities and is
considered the gold standard test although it is minimally invasive (Lauria et al.
2010).
• In-vivo corneal confocal microscopy (IV-CCM), which can evaluate small fibre
structure, non-invasively, by visualising the small nerves in the corneal sub-basal
plexus (Tavakoli et al. 2010). The sensitivity and specificity of CCM for diagnosis of distal sensory peripheral neuropathy has been reported as 82% and 52%
respectively (Tavakoli et al. 2010).
• Autonomic and sudomotor funct ions can also be measured (Vas et al. 2015). The
Neuropad test is a measure of sudomotor dysfunction. A plaster is attached on
the sole of the foot for 10 min. Sweat production leads to the colour change of a
Cobalt II compound from blue to pink. The test is normal when there is complete
colour change from blue to pink and abnormal when there is an absent or
incomplete colour change.
Screening for Neuropathy
Assessment of neuropathy is an important part of screening for the at-risk foot, thus
determining which feet are at risk from ulceration and amputation. In a study
assessing the various modalities suitable for screening, the expected range of
variation in readings for the neurothesiometer was 5 log hertz which was considered
by the investigators to be too large to allow the neurothesiometer to be an
acceptable screening instrument (Klenerman et al. 1996). Also, the range of
reproducibility for palpation of the four pedal pulses, varied from 68 to 81% which
50 D. Dixon and M. Edmonds
was also not acceptable. However, 85% of the results for the monofilaments were
similar between the first and second measurement.
Nevertheless, in a comparison between monofilament, tuning fork and vibration
perception tests for screening patients at risk of foot complication,
whilst the
monofilament test identified patients with the greatest risk of foot complications, a
further group of 37 more patients were identified to be at risk from a VTP > 25 V
(Gin et al. 2002). These patients had not been detected to be at risk using the
monofilament test. Furthermore, the VTP test provides numerical values which can
help to follow the course of neuropathy and determine the intensity and follow-up
of the at-risk group.
Screening can accurately predict outcomes experienced at different levels of risk
but the value of screening in subsequently reducing the frequency of ulcers and
amputations has not been fully established.
The Value of Screening to Predict Outcome
Screening with the monofilament together with palpation of foot pulses and a
previous history of ulcers or amputation has become part of a validated assessment
of feet at risk of ulceration from which a clinical prediction rule has been developed
and also validated (Chappell et al. 2021).
The tool assigns points to each of these 3 pieces of information:
• 0 points: no problem on any test
• 1 point: insensitivity to 10 g monofilament
• 1 point: if any pedal pulse is absent
• 2 points: previous history of ulcers or amputation
The overall score indicates the risk of developing a foot ulcer within 2 years as
in the following
• 0 points = 2% risk of ulcers
• 1 point = 6% risk
• 2 points = 14% risk
• 3 points = 29% risk
• 4 points = 51% risk.
The tool was tested in the UK using data from 3324 adults. The tool correctly
identified people who would develop ulcers, and people who would not, at 83% of
the time.
The Value of Screening to Affect Outcome
In an early study comparing the outcomes at 2-year follow-up, of a screened index
group with that of a control group, there were 7 amputations (1 major, 6 minor) in
the index group and 23 (12 major and 13 minor) in the control group (McCabe et al.
1998). The differences were not statistically significant for minor amputations (or
for ulceration) but significant for major amputations (p < 0.01).
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However, in a study at a local level of Primary Care Trusts, there was no
correlation between foot review and amputation incidence although It is not known
what percentage of patients received appropriate follow-on to the screening (Kerr
2012). In a further study, also at the local level of Clinical Commissioning Groups,
there was little or no correlation between foot review performance and amputation
incidence (Kerr 2017). There may be possible explanations for this, including a
delay between identification of risk and the actual reduction in amputations.
However, there may also be limitations in the quality of the foot examination, and a
problem in referring high risk patients to follow-on services (Kerr 2012). Foot
screening is one of the most common preventative actions in daily clinical foot
practice globally. Despite its widespread application in clinical practice, “the evidence underlying foot screening is limited” (Bus et al. 2020).
Measurement of Pressure Abnormalities of the Foot
as Precipitants of Ulceration
Paul Brand, who treated patients with leprosy and diabetes established the basic
concepts of the ‘pathomechanics’ of tissue breakdown, stating that “The whole
problem is really one of mechanics not medicine” (Bauman and Brand 1963).
He described four mechanical ways in which the soft tissues of the foot break
down when a person has neuropathy.
1. Repetitive moderate stresses to the plantar surface at sites of high pressure are
not sensed because of the neuropathy leading to build up of callus followed by
inflammation leading to breakdown of the neuropathic ulcer.
2. Low pressure maintained constantly causing tissue destruction by ischaemic
necrosis resulting in the neuroischaemic ulcer.
3. Very high force leading to penetrating injury.
4. Moderate press ure in the presence of an ulcer and infection.
Elevated levels of dynamic plantar pressure while walking, are a significant risk
factor in the development of neuropathic plantar foot ulcers. Plantar pressure
measurements showed that foot ulcers in patients with leprosy occurred at sites of
highest plantar pressure (Bauman and Brand 1963). Further studies demonstrated an
association between high plantar pressure and foot ulceration in persons with
diabetes (Pham et al. 2000). Although vertical plantar pressures measured in the
shoe are lower than barefoot analysis, subjects who ulcerate still have greater
in-shoe vertical pressures than cohorts who remain free from ulceration (Chatwin
et al. 2020). Whilst studies of the predictive value of foot pressure indicate that
elevated foot pressure is an important risk factor for foot ulceration, foot pressure
itself is a poor tool by itself to forecast foot ulcers (Lavery et al. 2003). Vertical
plantar pressure alone has been shown to be a poor predictor of DFU in prospective
studies (Chatwin et al. 2020). A plantar pressure threshold that predicts foot
ulceration has not been identified (SiA et al. 2013; Ulbrecht et al. 2014). However,
a comprehensive analysis of foot loading based on biomechanics, ambulatory
52 D. Dixon and M. Edmonds
activity levels and footwear adherence is lacking. Further studies are awaited in the
DIALOAD project (Bus et al. 2022). Up until recently, plantar pressures have been
measured while standing or walking and only provide a “snapshot” assessment but
ideally plantar pressures should be evaluated throughout the day to reflect everyday
life. In a recent prospective, randomised proof-of-concept trial, participa nts wore an
innovative, smart insole system, which provided visual and auditory plantar pressure feedback to the intervention group during daily-life activities (Abbott et al
2019). Feedback came from eight sensor sites on both feet and was provided via a
wrist-worn smart watch to the intervent ion group. A control group had the same
sensors without receiving any pressure feedback. The smart insole system resulted
in a 71% reduction in foot ulcer recurrence in the intervention group and this rose to
an 86% reduction in the most highly compliant participants. The control group
underwent more high-pressure bouts over time than the intervention group,
involving all areas of the foot. Differences between groups were noted after
16 weeks of wearing the device suggesting that by then, patients wer e recognising
the activities which generated high-pressure, and pro-actively avoiding them to
prevent further alerts.
Detection of Skin Temperature Rise as an Immediate Prelude
to Ulceration
It is important to detect ulcer formation early. Classical observations by Paul Brand
indicated that before the skin breaks down the subcutaneous tissues heat up. Such
heating is due to inflammation and enzymatic autolysis of tissue caused by mild to
moderate repetitive stress on the foot during walking (Bergtholdt and Brand 1975)
(Armstrong et al. 1997). The usefulness of infrared thermometry applied to the foot
to prevent ulcers has been assessed in several randomized controlled trials) (Lavery
Arm
et al. 2004, 2007;
infrared thermometer measured skin temperature on a daily basis at identical
regions at risk on both feet. A 2.2 °C difference between corresponding regions on
both feet was used as a significant threshold at which the patient should decrease
walking activity. If a temperature difference persisted despite this, the patient was
advised to consult a healthcare professional and if necessary, undergo a change in
offloading treatment. Foot skin temperature monitor ing was effective in preventing
a first or a recurrent foot ulcer in high-risk patients at between 65 and 75% compared with usual care.
However, in a recent study using the same hand-held thermometer, at-home foot
temperature monitoring did not significantly reduce the incidence of diabetic foot
ulcer recurrence at or adjacent to measurement sites when compared with usual
care, unless participants decreased walking activity when hotspots are found. Thus,
a crucial factor is adherence to measuring temperature and adequately following
subsequent instructions: in the recent study, this was only 28.9% (Bus et al. 2021)
Another approach to thermography, has been the use of a Smart mat platform
technology. A multicentre evaluation of an in-home telemedicine system designed
strong et al. 2007). In these studies a simple handheld
.
.
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to enable remote temperature asymmetry monitoring, investigated the accuracy for
predicting impending diabetic foot ulcers (DFU) in a cohort of patients with previously healed diabetic foot ulcer (Frykberg et al. 2017). Using an asymmetry
threshold of 2.22 °C, the mat was able to detect 97% of nontraumatic foot ulcers
with an average lead time of 37 days before they presented to the participant and/or
clinician. However, recent meta-analyses have stated some uncertainty over the
Alahakoon et al.
effect of home temperature monitoring (Crawford et al.
2020;
2020; Ena et al. 2021). Also, at present, platform-like devices work only for the
plantar side of the foot.
In a further approach which
assessed monthly intervention with thermal imaging
at four sites, no significant reduction in ulcer recurrence rate or increased ulcer-free
survival in a cohort at high risk of foot ulcers was noted (Petrova et al. 2020).
However, infrared thermography continues to be actively explored with various
techniques to establish its place in the detection of the very early signs of skin
breakdown. These techniques include personalised 3D-printed wearables, sensors,
automatic detection of diabetic foot complications with infrared thermography by
asymmetric analysis and low-cost smartphone-based thermal cameras (Beach et al.
2021; Liu et al. 2015; van Doremalen et al. 2019).
Characterisation of Infection, Which Often Complicates
Ulceration
Despite numerous guidelines and advanced therapies, up to 60% of DFUs will
experience an infection at some point (Lipsky et al. 2020; Jia et al. 2017). Current
guidelines recommend that wound sampling and microbiological analysis be performed only if an infection is suspected. This allows antibiotic therapy to be targeted; however, microbiological investig ations are hindered by the use of
superficial sampling methods, unreliable semi-quantitative wound cultures, the
difficulties in culturing anaerobes and bacteria encased in b iofilms (especially when
antibiotics are already dispensed), and delays in receiving microbiological culture
results (Serena et al. 2021). In some patients, subclinical infection may hamper
wound healing (Lantis et al. 2013). Point-of-care fluorescence imaging
(FL-imaging) has been developed as an objective and sensitive method of identifying h igh bacterial loads in wounds by employing endogenous fluorescence signals produced by bacterial metabolites and virulence factors (Le et al. 2021;
Raizman et al. 2021; Jones et al. 2020). This technology can identify presence of
planktonic bacteria as well as biofilm-encased bacteria which is critical considering
prevalence and pathogenicity of biofilm in diabetic foot ulcers (Johani et al. 2017).
FL-imaging has been introduced into wound care regimes to enable non-invasive
localization of the presence of most live bacterial species (including Gram-positive,
Gram-negative, aerobic, and anaerobic bacteria) at clinically-relevant levels
4
CFU/g) (Oropallo et al. 2021). The first randomized controlled trial evalu-
(>10
ating fluorescence informed care was reported in 2022 by Rahma et al. who
demonstrated a doubling of 12-week wound healing rates over the control arm
54 D. Dixon and M. Edmonds
(45% vs. 22%) (Rahma et al. 2022). A stepwise increase in wound area reduction at
12-weeks was observed, in favour of patients with negative baseline FL, followed
by patients with positive baseline FL who received additional care (primarily further debridement), and finally patients with positive baseline FL who did not
receive additional care. Overall, healing improved when clinicians had objective
information on the bacterial load and location(s) to consider in their treatment plans.
Wound Management
The main features of diabetic foot wound management are debridement, wound
applications to accelerate healing, and off-loading. The evidence for the usefulness
of technology in these aspects of management are described with reference to
mainly neuropathic ulcers but some studies also include neuroischaemic feet.
Wound Debridement
One of the cornerstones of wound management is debridement. Surgical or sharp
debridement is a part of standard wound care. However, there are forms of
non-surgical debridement including autolytic, enzymatic and maggot induced as
well as mechanical, which have been investigated and used to aid wound healing.
In 2010, a Cochrane review of methods for debriding diabetic foot ulcers,
reviewed
standard therapy with non-surgical debridement (weight bearing relief and regular
dressing changes). This concluded that hydrogels are more effective in healing
diabetic foot ulcers than gauze (Edwards and Stapley 2010). It also showed no
significant benefit in using surgical debridement over standard therapy. Whilst the
specific authors who compared surgical debridement over standard therapy concluded that surgical treatment of neuropathic foot ulcers in diabetic patients was
significantly more effective compared with conventional treatment, the authors of
the Cochrane review stated that the study was low in power due to its small size
(Piaggesi et al. 1998). However, although the authors of this Cochrane review
concluded that there was no evidence from RCTs that surgical debridement heals
diabetic foot ulcers more rapidly than conservative care, in real life practice, sharp
debridement has become a cornerstone of care. The International Working Group
on the Diabetic Foot (IWGDF) Consensus 2019 noted one study on sharp
debridement which showed benefit, but this was a post hoc subgroup analysis of
cases from an RCT of another intervention (Rayman et al. 2020; Saap and Falanga
2002).
6 RCTs comparing hydrogels, larval therapy, surgical debridement and
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Innovative Technologies in Wound Debridement
Microwater Jet Technology
Hydrosurgical techniques have been designed to create highly pressuris ed saline or
any other sterile solution and emit a jet of solution from the tip of a handheld device
with nozzle. The high-pressure stream facilitates removal of non-viable tissue from
wound beds (Lullove and Point-Counterpoint 2019). It allows preci se removal of
tissue but there is risk of cross contamination of wound beds if there are multiple
wounds in close proximity. The drawbacks of this technology include the inability
to remove hard eschar and debride bone. There is also a risk of contamination to the
operator from the mist generated during debridement (Lullove and
Point-Counterpoint 2019). Studies looking at the use of microwater jet technology
in debridement have shown efficacy in outpatient care in a retrospective study over
3 years (Reber and Nussbaumer 2018). A small study, reported in 2022, looking at
alternative methods for debridement, enrolled 50 patients into a two-arm randomised controlled trial comparing treatment of ulcers with weekly microjet wound
debridement to standard sharp debridement. The ulcers included were non-healing
neuropathic ulcers at 4 weeks with no clinical evidence of infection or
osteomyelitis. At 16 weeks, there was a significantly increased rate of healing in the
group managed with the microwater jet (72% vs. 40% p = 0.023 (unadjusted)
(Armstrong and Zelen 2022). There was also a larger area reduction in the
microwater jet group (86.5% vs. 35.1%) p = 0.021 (Armstrong and Zelen 2022).
Ultrasound Assisted Wound Debridement
Ultrasound assisted wound (UAW) debridement is useful in patients with poor
vascular supply where sharp or surgical debridement may be contraindicated.
Ultrasound waves promote wound debridement by using cavitation and
micro-streaming. Ultrasound waves cause oscillating gas microbubbles in a fluid
medium. The microbubbles expand, contract and implode, which allows easy
removal of non-viable tissue without damaging healthy tissue (Ruby Chang et al.
2017) Micro-streaming is observed when there is flow of interstitial fluid caused by
the vibrations generated from the ultrasound device. Cell membrane permeability
and secondary messenger activity is altered, leading to neo-angiogenesis and
fibroblast stimulation at the wound site (Swanson et al. 2020). There are 2 types of
UAW—non-contact and contact. Contact UAW delivers ultrasound energy to the
wound bed through a fine mist of sterile saline applied from 5 to 15 mm away from
the wound. There is no difference on the impact of wound healing and debridement
time between the two methods (Swanson et al. 2020) In an open label, single arm
study of 15 patients ultrasonic debridement demonstrated efficacy in safely preserving viable tissue with low complication rates and complete wound healing
(Campitiello et al. 2018). A meta-analysis reviewi ng all studies comparing UAW to
standard of care or placebo found a greater reduction in wound area in the UAW
group. However, it observed a high risk of bias in the blinding of patients and
professionals in the studies (Flores-Escobar et al. 2022).
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