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10 Frailty andMobility Degeneration inDiabetes andDiabetic Foot Ulceration
135
Fig. 10.2 Diabetes, frailty, and cognitive dysfunction are
closely related to the mechanisms of aging. It is estimated
that between 10% and 25% of older adults with diabetes
are frail. Insulin resistance, chronic inammation, oxidative stress, and mitochondrial dysfunction may be common mechanisms shared by diabetes, frailty, and cognitive
impairment. Hyperglycemia, hypoglycemia, obesity, vas-
Frailty andBiomechanics ofLower
Extremities
Frailty and aging could alter the biomechanics of
lower extremities, which in turn may increase the
risk of diabetic foot ulcer (DFU) among older
individuals with diabetes. Figure10.3 is a summary illustration of age-related factors affecting
lower extremity biomechanics reported in a systematic review by Neville and colleagues [22]. In
summary, aging has been shown to alter the biomechanical properties of the skin and plantar soft
tissue of the foot. These soft tissues, which
anchor the plantar skin to the underlying bony
architecture of the foot, serve as a protection to
the underlying neurovascular structures, provide
resistance against frictional shear force, and
attenuate the pressure and force during collision
impact [23]. Because of aging, the dermoepidermal junction of the skin, which provides
cular factors, physical inactivity, and malnutrition are
important risk factors for frailty in older adults with diabetes. Having one of these clinical syndromes can signicantly increase the risk for another one and will
signicantly impose a substantial personal and public
health burden
resistance against shear stress, becomes attened,
thinner, dehydrated, and loss of elasticity with
aging [22]. This in turn could reduce skin reliance against pressure and shear and thus early
skin breakdown with a lower magnitude of pressure and shear forces. In addition to the changes
in the skin noted above, there are also changes in
the tissue properties interfacing with the plantar
surface of the foot causing higher tissue stiffness
due to aging that in turn could be one of the factors for the high prevalence of foot problems (e.g.
foot pain and foot deformity) in frail older adults
as reported by Muchna and colleagues [24].
Furthermore, the increase in soft tissue stiffness
could be postulated to contribute to the decrease
in tactile sensation and limit sensory feedback
[25]. Over time this change can reduce the loadbearing capacity of the plantar soft tissues, which
might result in reduced shock absorption as well
as slower recovery after compression [26]. This
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Fig. 10.3 The impact of frailty on lower extremity biomechanics and its association with increased risk of DFU
B. Naja and G. E. Kang
can increase plantar pressure [27] leading to foot
pain and foot deformity [28]. A systematic review
by Wrobel and Naja [25] demonstrated that the
changes in the properties of soft tissues led to
impaired gait function and adaptation to uneven
or irregular surfaces, which may result in falls
and increased risk of DFU. In addition, Naja
and colleagues linked poor plantar sensory feedback with poor balance [29].
The impact of aging is not limited to soft tissue and skin properties. Neville and colleagues
reported age-related changes in the musculoskeletal properties occurring at specic joints in the
foot and ankle negatively impact balance and gait
in older adults [22]. Furthermore, loss of muscle
mass particularly in type II muscle bers affects
the lower limb strength and results in a decline in
force and power production, slower muscle
responses, and the reduction in ability developing
rapid muscle activation and power [30]. These
lower extremity biomechanical changes in the
aging population are anticipated to be magnied
because of frailty, which in turn may increase the
likelihood of joint deformities and joint rigidity,
leading to alerted gait, inability to absorb collision shock during walking, higher likelihood of
developing callus and lower resilience to pres-
sure and shear, thus increasing likelihood of DFU
in response to a lower magnitude of pressure and
shear force compared to non-frail and younger
populations [22, 24, 25].
Mobility Degeneration inDiabetes
andDiabetic Foot Ulceration
Frailty and sarcopenia result in a severe reduction
in functional mobility in people with diabetes
[31], which can further speed up the progression
of frailty [32]. A common manifestation of
frailty-related mobility degeneration is impaired
gait performance [25]. For example, Petrofsky
and colleagues found that people with diabetes
walk slower and take shorter and wider steps than
people without diabetes [33]. However, interestingly, in terms of walking activity under natural
circumstances, often measured by daily step
counts, studies have reported mixed results.
Tudor-Locke and Bassett reported that daily step
counts for people with diabetes (approximately
6660 steps per day) are not necessarily lower
than those for healthy adults (between 6000 and
7000 steps per day) [34, 35]. However, Morrato
and colleagues reported that approximately 40%
10 Frailty andMobility Degeneration inDiabetes andDiabetic Foot Ulceration
137
of people with diabetes are engaged in a minimum of 30 min of moderate exercise (3 days/
week), but approximately 60% of healthy people
are engaged in the same amount of moderate
exercise [36].
In people with DFU, in general, mobility
impairment worsens compared to those without
diabetes and those with diabetes but without foot
ulceration. For example, Yavuzer and colleagues
reported slower gait speed and cadence in people
with diabetic peripheral neuropathy compared to
people with diabetes but without peripheral
neuropathy and normal controls [37]. Naja and
colleagues demonstrated that 4weeks’ immobilization of the foot after treatment for DFU caused
a reduction of daily walking duration by an average of 44% and a reduction of the total number of
steps by an average of 23% [38]. A similar observation was reported by Fernando and colleagues:
the average daily step counts were reduced from
7762 ± 3590 steps for people with diabetic
peripheral neuropathy (DPN) to 3729 ± 2042
steps for people with DFU treated by irremovable
ofoading devices [39]. This reduction in the
level of activity could be due to muscle wasting
caused by irremovable ofoading, as suggested
by de Oliveira and Moore [40]. Interestingly, the
level of activity observed in people treated by
irremovable ofoading devices was similar to
activity levels in a frail population as observed in
another study performed by Schwenk and colleagues [41]. They reported average daily steps in
non-frail, pre-frail, and frail older adults (age
65years or older) were 6030±3075, 3869±1996,
and 3869 ± 1996 steps, respectively. This may
suggest that the treatment of DFU by irremovable
ofoading may lead to frailty, particularly among
older patients.
Frailty could signicantly impact gait performance, which in turn may increase the risk of
DFU in people with diabetes. Rahemi and colleagues analyzed gait performance of 161 older
adults (age 65 years and older) using wearable
sensors to explore gait parameters among frail
and non-frail participants [42]. They used the
frailty phenotype criteria developed by Fried and
colleagues [43] to determine the frailty status of
participants. According to these criteria, 49 individuals were classied as non-frail, 92 as prefrail, and 20 as frail. The gait parameters
associated with propulsion characteristics including propulsion duration and propulsion acceleration had the largest effect size (Cohen’s
d= 1.28–1.95) to distinguish between frail and
non-frail individuals. More specically, their
results suggest that frail individuals have an earlier heel-off phase leading to longer propulsion
duration on average by 58% and less efcient
propulsion (lower propulsion acceleration) on
average by 45% compared to non-frail
individuals.
The early heel-off phase in frail individuals
could be explained by muscle loss from sarcopenia or fat inltration and loss of muscle quality
and force production capacity in older adults. In
a conference paper, Naja and colleagues
reported that treating people with DFU using
irremovable ofoading for a duration of longer
than 4 weeks could lead to reduced propulsion
performance with similar characteristics reported
in Rahemi and colleagues [44]. Additionally,
they found, compared to plantar pressure with an
age-matched non-frail individual, peak plantar
pressure was 109% higher in people with DFU
treated with irremovable ofoading probably
because of inefcient propulsion, joint rigidity,
and reduced area of contact. Thus, irremovable
ofoading could enhance wound healing outcomes. It may have long-term consequences such
as muscle wasting, poor gait, and physical activity reduction, which in turn could increase risk of
recurrence of ulcers, increase the risk of falling,
and frailty. This speculation however needs to be
conrmed by future studies.
Screening Frailty
Frailty is a multidimensional construct including
clinical manifestation of cognitive decline or
functional decline or both, also referred to as
“cognitive frailty” [45]. Although frailty is not
routinely screened in primary care settings, due
to the impact of frailty on clinical outcomes, it is
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Fig. 10.4 Although more than 20 different methods for
frailty assessment have been suggested in literature, two
of the most popular methods are frailty phenotype and
frailty index. The frailty phenotype, proposed by Fried
and colleagues, assesses ve physical components: unintentional weight loss, slowness, weakness, exhaustion,
and low physical activity. The frailty index, proposed by
Rockwood and colleagues, considers health decits
(symptoms, signs, disabilities, diseases, etc.). The frailty
index is represented as a ratio between the number of presented decits and the number of considered decits.
Also, there are several digital health-based technologies
that facilitate objective screening of frailty
becoming more critical to properly screen frailty
in the primary care setting to early identify when
a person starts being frail. Until now, there is no
consensus made on how to best measure frailty,
but there are several widely used approaches and
some recently emerging approaches. Although
more than 20 different methods for frailty assessment have been suggested in literature, two of the
most popular methods are frailty phenotype and
frailty index described in the following.
Additionally, recently the use of digital technology facilitates monitoring frailty and its severity
based on quick and simple assessment of motor
performance (Fig.10.4).
B. Naja and G. E. Kang
Frailty Phenotypes andFrailty Index
One approach that is widely used is the frailty
phenotype proposed by Fried and colleagues
[9]. The frailty phenotype primarily measures
functional decline and consists of ve criteria of
weight loss, weakness (i.e., weak grip strength),
exhaustion, slowness (i.e., slow gait speed), and
reduced physical activity and classies people
into three categories of robust (those who meet
0 criteria), pre-frail (those who meet 1 or 2 criteria), and frail (those who meet 3 or more criteria). Numerous studies demonstrated frailty
assess using the frailty phenotypes is a strong
predictor of mortality in a population with specic health condition such as cardiovascular
disease and a community-dwelling population
[46, 47].
However, administration of frailty using the
frailty phenotype can be challenging in patients
with limited mobility, or bed-bound patients in
the hospital setting. An example is a person with
peripheral arterial disease, often with rest pain,
foot ulcers, foot gangrene, or previous limb
amputations; these issues may make usual assessments of frailty impractical or invalid [48].
Moreover, assessing slowness could be invalid or
inaccurate in those with concurrent parental IV
therapies, fractures, presence of wounds, need of
walking assistance, or on ventilator support. An
additional challenge in the hospital setting is
allocating space for distance-specic testing. In
the absence of complete phenotype assessment,
interpretation of frailty results can be narrow, and
the predictive power might be reduced [49, 50].
For example, Rockwood et al. [51] showed
patients who were missing performance-based
measures had a risk of mortality 3 times higher
over the span of 5years than those who were not.
10 Frailty andMobility Degeneration inDiabetes andDiabetic Foot Ulceration
139
Furthermore, evaluation of frailty using frailty
phenotype requires trained personnel to conduct
the assessment, especially when evaluating
patients with cognitive impairment, limiting their
ability to respond to the questionnaires (e.g.,
inactivity, weight loss, and exhaustion of
questionnaires).
Another popular approach is the frailty index
proposed by Rockwood and colleagues [52]. The
frailty index measures decits in physical performance, health state, and self- and familial history
of diseases including cognitive impairment and is
based on cumulative decits in overall state (total
70 items). The frailty index is calculated as a
fraction of the number of existing decits (e.g.,
seven decits out of 70 items=0.1), which results
in a continuous scale between 0 (“no decit”) and
1 (“decits in all 70 items”). Studies demonstrated the frailty is a strong predictor of mortality across clinical conditions [53]. However,
since it consists of a high number of general signs
or symptoms, it mainly serves as a “red ag” for
potential problems but cannot be used to determine immediate effect of preventive or therapeutic interventions since it is not sensitive to change
over short time intervals [54].
Emerging Technologies
The development of wearable technology
enhances screening frailty in both clinical and
research settings [55]. For example, Toosizadeh
and colleagues developed a single wearable sensor worn on the wrist and successfully assessed
some of the frailty phenotypes (e.g., slowness,
weakness, and exhaustion) as well as other movement characteristics that are associated with
frailty (e.g., rigidity) from a 20-s elbow exion–
extension movement (i.e., frailty meter) [56–58].
Wearable technology is also used to measure
gait and balance performance under supervised
(e.g., lab setting) and unsupervised conditions
(e.g., home setting), which is another way of
screening frailty. Kang and colleagues examined
characteristics of gait initiation in older adults
with DPN in comparison with non-diabetic older
adults and successfully differentiate the gait initiation phase between the two groups [59]. Kang
and colleagues also examined the combining
effects of cognitive and functional status on gait
and balance performance during single-task gait
and dual-task gait in older adults with DPN using
wearable sensors and successfully demonstrated
cognitive decline exacerbates the risk of physical
injury [60].
More recently, with increasing needs of telemedicine in the era of COVID-19, image analysis
of human motion is being developed to identify
frailty status of older adults during the telemedicine service. Zahiri and colleagues used the 20-s
elbow exion–extension movement and developed an image analysis system to measure frailty
state of older adults and successfully identied
slowness, weakness, and exhaustion as well as
rigidity [61] (Fig.10.5).
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B. Naja and G. E. Kang
cd
e
Fig. 10.5 (a–e) Recent advances in articial intelligence
and image processing allow a new generation of frailty
meter over telemedicine. Above is a solution proposed by
Zahiri etal. in which frailty and its key phenotypes including weakness, slowness, exhaustion, and exibility could
be measured by a 20-s repetitive elbow exion–extension
test in front of a camera. Using a deep-learning image pro-
cessing algorithm and a machine learning model, the
frailty index and each phenotype are measured from this
20-s test. This method could open an opportunity to
remotely assess frailty over telemedicine. (This gure is
recreated using one of the gures reported in Zahiri etal.
study [60])
10 Frailty andMobility Degeneration inDiabetes andDiabetic Foot Ulceration
The Impact ofFrailty inDiabetes
Once an individual starts being frail, it further
exacerbates aging process, further deteriorates
diabetes itself, and develops diabetic complications, which eventually results in signicant
reduction in functional abilities, independency,
and mortality [62, 63]. To this end, although the
association between frailty and diabetes is not
fully understood, some studies have reported the
impact of frailty state on adverse health outcomes
in diabetes and DFU. Examples of the adverse
health outcomes include the development of biomechanical risk factors, occurrence of postoperative complications, and delayed wound healing,
which will be discussed in the next paragraph
(Fig.10.6).
Takeji and colleagues investigated the impact
of frailty on clinical outcomes (all-cause mortality and major amputation after 2years) of patients
with critical limb ischemia who underwent either
endovascular therapy or bypass surgery [64]. In
their study, frailty was assessed using the frailty
index [52]. They found the frailty index was independently correlated with all-cause mortality and
major amputation after 2years. O’Donovan and
colleagues compared psychosocial wellbeing and
morality among four groups of people (diabetes
and frail, diabetes and non-frail, frail and nondiabetic, and non-diabetic and non-frail) [65].
They found the lowest quality of life for the diabetic and frail group followed by the diabetic and
non-frail group, the frail and non-diabetic group,
and the non-diabetic and non-frail group. They
also found similar mortality rate at 2year between
the diabetic and frail group, and the frail and nondiabetic group (approximately 15%), which was
signicantly higher than the diabetic and nonfrail group (7.3%) and the non-diabetic and nonfrail group (2.7%). Bąk and colleagues
investigated the impact of frailty on quality of life
and depression in older adults with type 2 diabetes [66]. They found frail older adults with type 2
diabetes have signicantly higher depression and
lower quality of life compared to robust older
adults with type 2 diabetes. Naja and colleagues
investigated if preoperative frailty state measured
Fig. 10.6 Screening of frailty could be useful to evaluate
risk of surgical intervention like revascularization for our
patients, it could also help to better determine biomechanical risk factors associated with diabetic foot ulcer; it may
be also helpful for predicting chronic and hard to health
wounds
Fig. 10.7 Naja and colleagues demonstrated that using
a sensor-based frailty meter based on a 20-s elbow repetitive exion–extension test is a practical test to quickly
determine physical frailty in a hospital setting and predict
adverse events in people with critical limb-threatening
ischemia after lower extremity revascularization [13]
using a single wearable sensor can predict 30-day
major adverse events (i.e., myocardial infarction,
stroke, all-cause mortality) in people with critical
limb-threatening ischemia after lower extremity
revascularization [13] (Fig.10.7). They found the
frailty state was able to distinguish the occurrence of 30-day major adverse events. Kang and
Naja used a single wearable sensor to measure
biomechanical characteristics during normal
daily activities [67]. They found lower level of
activity, which is also considered as a domain of
frailty, was a strong predictor of the risk of all
among older adults with diabetic foot. In another
study, Van Epps and colleagues found that frailty
is a strong predictor and a better predictor than
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B. Naja and G. E. Kang
age for inammation and thrombosis in older
adults [68]. Although their study was not necessarily on people with diabetes, it provides enough
implications on potential impact of frailty in
diabetes.
Potential Solutions toImprove
Outcomes Among Frail andPre-frail
Diabetic Patients
Then, this question arises: What can we do to prevent (or reverse) frailty or to improve health outcomes in frail or pre-frail diabetic patients?
Although frailty has been traditionally considered
non-treatable and non-reversible, in 2013, in a
consensus conference, it was agreed that frailty
state may be reversed with exercise and nutritional
solutions [69]. Furthermore, some studies reported
possible reverse of frailty in older adults [70, 71].
In this section, we summarize previous methods
that researcher has used to improve frailty or a
domain of frailty in people with diabetes or diabetic complications, or those at risk of diabetes.
Armstrong and colleagues examined the effect
of electrical stimulation on pain level in people
with diabetic foot [72]. They reported the
electrical stimulation signicantly improved pain
level after 4weeks. Naja and colleagues used
plantar electrical stimulation and investigated its
effect on postural balance and plantar numbness
in people with diabetic foot [73]. They found that
daily use of electrical stimulation for 6 weeks
signicantly improved both postural balance and
plantar numbness. Zulbaran-Rojas and colleagues investigated the effect of electrical stimulation on wound healing in people with type 2
diabetes with chronic non-healing wounds [74].
They reported that daily use of electrical stimulation for 4 weeks signicantly reduced wound
area (22% reduction on average). Another poten-
tial solution is mechanical stimulation. For example, Kang and colleagues tested the effect of
home- based mechanical stimulation applied to
the plantar side of the feet on gait, balance and
plantar numbness in people with diabetic foot
[75]. They found that daily use of the home-based
mechanical stimulation for 4 weeks is effective
improving gait speed, balance control, and plantar numbness.
Several studies investigated the effect of exercise on frailty or a domain of frailty in diabetes.
Geirsdottir and colleagues investigated the effect
of a 12-week resistance exercise intervention on
muscle strength and physical function in older
adults with prediabetes and type 2 diabetes [76].
They found that the exercise intervention signicantly improved muscle strength and physical
function. Some recent studies combined the exercise intervention with an interactive computer
game, the so-called exergame (Fig.10.8). Zhou
and colleagues investigated the effect of an intradialytic exergame program on psychological distress in people who undergo hemodialysis [77].
They found the exergame program is effective in
improving psychological distress. Rahemi and
colleagues evaluated the exergame program in
improving femoral venous parameters in healthy
individuals [78]. They found the exergame program signicantly increased the femoral vein
mean ow volume and mean velocity and showed
its potential in preventing deep venous thrombosis. Grewal and colleagues investigated the effect
of exergame on balance control in people with
diabetic foot [79]. They reported people with diabetic foot had signicant improvement in balance
control after the exergame. Despite these studies,
we were not able to identify a study that proposed
a potential solution that will reverse comprehensive domains of frailty in people with diabetic
foot. As such, future research is recommended on
this aspect.
10 Frailty andMobility Degeneration inDiabetes andDiabetic Foot Ulceration
143
Fig. 10.8 Zhou and colleagues have suggested the use of
low intensity and gamied non-weight bearing foot and
ankle exercise as intradialytic exercise program [62].
These exercises could be tailored for people with limited
Conclusion
Frailty is highly prevalent among people with
diabetes and has signicant negative impact on
health outcomes. Previous research emphasized
the importance of appropriate screening of frailty
to prevent further deterioration in health state in
people with diabetes. Although frailty assessment is not occurring in routine care setting, the
development of new technologies may enhance
the screening process in the future. Although
frailty may be reversed by exercise or other
adjunctive treatment, most of the studies in diabetes were limited to report changes in a partial
domain of frailty and lack the possibility of
reverse in the aspect of comprehensive frailty
domain.
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