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Vongsirinavarat et al.
Mantana Vongsirinavarat, Ph.D., Ratchanok Kraiwong, Ph.D.
Faculty of Physical erapy, Mahidol University, Nakhon Pathom 73170, ailand.
Falls among Older Adults with Type 2 Diabetes
Mellitus with Peripheral Neuropathy
ABSTRACT
Objective: e high incidence and prevalence of falls among older people with type 2 diabetes mellitus (ODM)
have been documented. e risk factors of falls among ODM were identied as poor diabetic control, diabetic
peripheral neuropathy (DPN) and balance impairment. is study aimed to investigate the contribution of DPN
to history of falls. e dierences of balance performance and lower limb muscle strength among ODM with and
without DPN were also explored.
Methods: is cross-sectional study interviewed 112 ODM for their falls occurrences within the previous 6 months.
DPN was determined by the score of the Michigan Neuropathy Screening Instrument. Balance performance tests
included Clinical Test of Sensory Interaction and Balance (mCTSIB), Functional Reach Test (FRT) and Timed
Up and Go Test (TUG). Leg muscle strength was also measured. e logistic regression analysis was performed.
Results: e history of falls was reported 30.6% of ODM with DPN and 10.4% of ODM without DPN. Presenting
of DPN inuenced falls with odds ratio of 3.46 among ODM. Dierences were found of mCTSIB in the condition
of eyes closed on rm and foam surfaces, FRT, and TUG between those with and without DPN. Knee extensor
strength diered between those with and without DPN.
Conclusion: DPN was more prominent among fallers. Balance performance and leg strength were lower in ones
with DPN. Falls prevention programs including balance training and therapeutic exercise to improve balance
performance and muscle strength should be emphasized among ODM, especially before the onset of DPN.
Keywords: Balance; diabetic peripheral neuropathy; elderly; falls; type 2 diabetes mellitus (Siriraj Med J 2021; 73: 92-98)
Corresponding author: Mantana Vongsirinavarat
E-mail: mantana.von@mahidol.edu
Received 14 July 2020 Revised 15 October 2020 Accepted 16 October 2020
ORCID ID: http://orcid.org/0000-0003-4008-1071
http://dx.doi.org/10.33192/Smj.2021.13
INTRODUCTION
Diabetes mellitus (DM) is a major metabolic condition
with several complications causing disabilities among
older adults i.e., people with age greater than 60 years.
High prevalence of older adults with Type 2 diabetes
mellitus (ODM) has been reported globally, 15-22%
worldwide
1
and 17.2% in ailand.
2
Compared with a
nondiabetic group, older adults with Type 2 diabetes
mellitus (ODM) reported greater falls occurrence
3
and
risk of falls.
4
Other important risk factors of falls among
ODM include balance impairments and reduced muscle
strength.
5
However, studies regarding falls risk among
ODM showed inconsistent ndings which might be
associated with the complications, duration of disease,
cognitive function, age and sex dierences.
4
Diabetic peripheral neuropathy (DPN) is a major
complication known to be associated with increasing falls
and reduced quality of life among ODM.
6
e overall
prevalence of DPN among ODM was 28% in the US
7
and 2.82% in ailand.
8
ODM with DPN exhibited
signicant decits in sensory-motor function, postural
instability and gait imbalance leading to a high fall
incidence.
9
e presence of DPN was associated with
poorer balance performance including the Berg Balance
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score (BBS), single leg stance test (SLS) and Timed Up
and Go Test (TUG). e severity of DPN reected by
MNSI score was reversely correlated with BBS score and
SLS time.
10
Although DPN aects both sensory and motor
functions,
11
the sensory decits specically exteroception
and proprioception are usually more prominent than
muscle dysfunction among ODM with DPN.
12
e early
clinical picture typically involves altered somatosensory
functions, while motor involvement usually manifests
in the later stages of DPN.
13
In more severe stages, the
motor deterioration presents as unilateral or bilateral
muscle weakness and atrophy of the proximal thigh
muscles.
14
The functional fallouts of sensory and motor
impairments such as postural instability, unsteady gait
and frequent falls were evident among ODM.
10,12,15
ese
adverse consequences could be inated in cases of ODM
with DPN. However, the eects of DPN concerning falls
among ODM still require more evidences. erefore,
this study aimed to determine the contribution of DPN
on the history of falls. Balance performance and lower
limb muscle strength were also compared between ODM
with and without DPN.
MATERIALS AND METHODS
is study employed a cross-sectional, comparative
design. e research settings were eight community
hospitals in the Mueang, Phuttamonthon, Nakornchaisri
and Sampran districts, Nakornpathom province. e
inclusion criteria were community dwellers, aged over 60
years and diagnosed with type 2 DM by medical doctors
for at least ve years. Two hundred and forty-eight
(n=247) ODM who were followed up in the diabetes
clinics of hospitals nearby their residents were enrolled
in the study. All participants were informed about the
study procedures and signed informed consent before
participating. is study was approved by the Mahidol
University Central Institutional Review Board (MU-
CIRB 2015/035.0303).
e participants were included if their vital signs
including heart rate, blood pressure and respiratory rate
were in normal range. e letter chart and visual acuity
conversation was used to conrm that all participants
had normal vision. They also had no complaints of
vertigo and dizziness, could understand and follow verbal
instruction and could walk independently at least 10
meters. e exclusion criteria were a history of central
nervous system dysfunction, cognitive impairment, lower
limb amputation or joint replacement and symptoms
aecting walking. One hundred and thirteen ODM were
nally included in the study and divided into ODM with
DPN (n=36) and ODM without DPN (n=77) groups for
analysis. Fig 1 presents the ow of participants.
Fig 1. Flow of Participants
Enrollment History of type 2 DM assessed for eligibility (n=247)
Allocation
Excluded (n=134)
Not meeting inclusion criteria (n=91)
Declined to participate (n=44)
Michigan Neuropathy Screening Instrument
Type 2 DM with
DPN (n=36)
Type 2 DM without
DPN (n=77)
Balance performance by mCTSIB, FRI, TUG, and Lower limb muscle strengh
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Vongsirinavarat et al.
Procedures
An experienced physical therapist recruited and
screened all participants. e data collection was undertaken
by four physical therapists trained by the investigators.
A handout for interview and assessment protocols was
used to ensure the consistency. Before collecting data,
the reliability was monitored using the participants
aged 60 and over. A minimum of 0.75 was achieved for
the values of Intraclass Correlation Coecient (ICC)
intertester and intratester reliability for all tests.
Participants’ information regarding age, sex, history
of type 2 DM and duration of DM exposure were recorded.
Venous blood was drawn on the day of testing to determine
fasting blood sugar (FBS) and hemoglobin A1c (HbA1c).
History of falls within the previous six months
based on participant recollection was monitored. Falls
was dened as an event resulting to a person coming
to rest inadvertently on the ground or oor or other
lower level.
16
e ai version of the Montreal cognitive
assessment (MOCA) was used for screening cognitive
impairment. is tool had good criterion validity and
good internal consistency (cronbach’s alpha = 0.914).
17
e Michigan Neuropathy Screening Instrument
(MNSI) ai version, was used to identify DPN.
18
is
instruments has good test-retest reliability (ICC=0.830)
and intertester reliability (ICC=0.780-0.869).
18
Positive
DPN was determined in cases scoring greater than 2 of
8 of the physical examination part, not including the
monolament test.
19
Balance performances were evaluated by the modied
Clinical Test of Sensory Interaction and Balance (mCTSIB),
Functional Reach Test (FRT) and TUG test. e procedures
of all measurements were also described as following.
e mCTSIB involves observing a participant’s
attempt to maintain static balance for 30 seconds.
Participants were asked to stand with feet together and
hands at sides in four conditions including eyes open
(EO) on a rm surface, eyes closed (EC) on a rm surface,
EO on a foam surface, and EC on a foam surface. e
foam was medium density, 24 inches in width and length
and 4 inches in height (SunMate Dynamic System Inc.,
Leicester, USA). ree trials were performed under each
condition.
20
e participants were allowed 60 seconds
rest between each condition to diminish the eects of
fatigue. Sway was defined as inability to stand with
feet together, moving upper extremity, opening eyes,
exing one or both knees, toes, or heels raised from
the oor and attempting to hold onto the tester during
test execution. is test had good interrater agreements
(Kappa = 0.57-0.72).
21
For the FRT, barefoot participants stood with their
right side close to a wall. e feet were apart at shoulder
width. e right shoulder was exed at 90 degrees with
the elbow extended. e 3
rd
metacarpal bone was the
landmark used to measure the distance between starting
and ending points. e participants were asked to reach
forward as far as possible without taking a step. ey
were allowed to practice once and performed the FRT
twice. e reaching distance comprised the averaged
value.
22
e FRT had been reported excellent test-retest
reliability (ICC=0.89-0.92) in community dwelling older
adults.
23
For the TUG, the participants sat on a 46-cm height
armchair with their back contacting the chair back support.
ey were asked to stand up, walk 3 meters as quickly
and safely as possible, turn around, walk back and sit
down. ey were allowed to use a gait assistive device
as preferred. e timing was started at the instruction
“go” and stopped when the participants sat with their
back touching back support. ey performed the TUG
twice, as a practice session and the latter as the test.
24
is test has been reported excellent test-retest reliability
(ICC = 0:96-0.98).
25
For muscle strength, knee extensors, knee exors,
ankle plantar exors and ankle dorsiexors were measured
using a hand-held dynamometer (Lafayette Instrument
Company, IN, USA). All muscle groups were tested in
midrange of joint motion. One practice trial was given
before measuring each movement. e average of three
trials was recorded.
Statistical analysis
Statistical analysis was performed using SPSS version
18 (IBM Corp., Armonk, NY, USA). e Kolmogorov-
Smirnov Goodness of Fit test was used to test the distribution
of the data. Demographic data and health information
were compared between groups. e Mann-Whitney
U test was used to examine dierences of non-normal
distributed data, while the independent t-test was used to
determine dierences of the normal distributed data. e
value of p<0.05 was considered statistically signicant.
e univariate logistic regression model was constructed
to identify the association between DPN and the history
of falls among ODM. e association of categorical
independent variables with balance impairment was
assessed using the Chi-square test, and the calibration
was performed using the Hosmer-Lemeshow goodness
of t test. Discrimination was determined using the area
under the receiver operating characteristics (AUROC)
to evaluate overall predictive accuracy of the model.
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RESULTS
e characteristics of participants with and without
DPN are presented in Table 1. ey did not dier in
terms of age, proportion of sex, duration of DM, levels
of FBS and HbA1C and cognitive function scores. e
overall prevalence of falls among ODM was 17.7%. e
prevalence of falls in the groups with and without DPN
was 30.6% and 11.7%, respectively (Table 1). Statistically,
the DPN had contribution on the fall occurrences among
ODM with Odds ratio of 3.46 (95% CI: 1.28-9.38, p =
0.015) with the AUROC value of 0.645.
Dierences between ODM with and without DPN
were observed in two conditions of the mCTSIB, eye
close on a rm surface (p < 0.001) and eye close on
a foam surface (p = 0.039), as well as the FRT (p = 0.022)
and TUG (p< 0.001) (Table 2). Of all lower limb muscles
tested, only knee extensors strength diered between
groups (p = 0.031) (Table 2).
DISCUSSION
is study aimed to explore the contribution of DPN
on the occurrence of falls and to compare the balance
performances and lower limb strengths among ODM
with and without DPN. e results showed that DPN
was a contributing factor of the history of falls. Poorer
balance performances and less knee extensor strength
were also observed among ODM with DPN compared
with those without DPN.
e history of falls within the previous six months
diered between ODM with and without DPN. Statistically,
DPN was a signicant predictor of falls. ODM with
DPN had the odds of having history of falls 3.46 times
more than the odds for ODM without DPN with 64.5%
prediction accuracy. e results agreed with a previous
longitudinal study reporting higher falls occurrences
among older adults with neuropathy compared with a
matched nonneuropathy group.
26
Other than DPN, patients
with diabetes usually developed retinopathy, vestibular
dysfunction, cognitive impairment and hypoglycemic
events with insulin use which might also contribute
to falls.
4
However, the participants in our study had
normal visual acuity, no cognitive impairment and did
not complain of vertigo and dizziness. erefore, falls
prevalence and balance impairment would be associated
with their DPN condition. e phenomenon of increased
falls also reportedly presented 3 to 5 years before the
neuropathy diagnosis and worsened rapidly over time,
rising from 23 to 56% over the course of a longitudinal
study.
26
us, falls is a crucial problem which should be
addressed in the management plan of ODM.
DPN
Parameters Yes (n=36) No (n=77)
Age (years) 70.42 ± 5.96 68.42 ± 7.10
Sex: male 12 (33.3%) 21 (27.3%)
female 24 (66.7%) 56 (72.7%)
Duration of DM (years) 12.44 ± 6.39 10.68 ± 5.98
FBS (mg/dL) 153.78 ± 64.95 141.38 ± 40.86
HbA1C (%) 8.10 ± 1.63 7.50 ± 1.43
MOCA 20.22 ± 4.329 18.69 ± 3.345
History of falls: Yes 11 (30.6%) 9 (11.7%)
No 25 (69.4%) 68 (88.3%)
TABLE 1. Characteristics of older adults with type 2 DM with and without DPN (n=113).
Values are presented as mean ± standard deviation or numbers and percentage. *p-value <0.05 signicant dierence pairwise comparison
without DPN group.
Abbreviations: DM, diabetes mellitus; DPN, diabetic peripheral neuropathy; FBS, fasting blood sugar; HBA1c, hemoglobin A1c (glycated
hemoglobin); MOCA, Montreal cognitive assessment score
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Vongsirinavarat et al.
DPN
Parameters Yes (n=36) No (n=77)
Muscle strength (kg)
Knee extensors 15.01 ± 5.02* 16.93 ± 5.07
Knee exors 11.06 ± 2.94 10.92 ± 3.36
Ankle plantar exors 15.51 ± 3.57 16.90 ± 4.87
Ankle dorsiexors 11.33 ± 2.88 11.78 ± 3.26
Balance performance
mCTSIB (s)
Condition 1 28.72 ± 4.90 29.91 ± 0.75
Condition 2 22.39 ± 11.26** 28.93 ± 4.47
Condition 3 22.37 ± 11.37 25.44 ± 8.43
Condition 4 10.15 ± 11.75* 14.63 ± 11.92
FRT (inches) 8.99 ± 2.79* 10.38 ± 3.06
TUG (s) 16.14 ± 6.59** 11.76 ± 3.45
TABLE 2. Lower limb muscle strength and balance performance among older adults with Type 2 DM with and
without DPN (n=113).
Values are presented as mean ± standard deviation. *p-value <0.05 signicant dierence pairwise comparison without DPN group. **p-value
<0.001 signicant dierence pairwise comparison without DPN group.
Abbreviations: DM, diabetes mellitus; DPN, diabetic peripheral neuropathy; mCTSIB, modied Clinical Test of Sensory Interaction and
Balance; FRT, Functional Reach Test; TUG, Timed Up and Go Test.
Sensory impairment and lower limb muscle weakness
are possibly the underlying causes of increased falls in
DPN. Somatosensory, visual function and vestibular
inputs play an important role in balance control.
27
Due
to impaired somatosensory and motor outputs, patients
with DPN demonstrated postural instability and gait
imbalance leading to higher fall incidence.
9,28
e nerve
damage in DPN is characterized by the development
of vascular abnormalities with a subsequent decline in
oxygen tension and hypoxia.
11
e mutilation progressively
alters the sensory and autonomic axons, and later the
motor axons, leading to sensory, autonomic as well as
motor losses.
11
Other than falls, patients with DPN could
also injure themselves from the reduced sensitivity of
touch and pain leading to foot ulceration, which could
become infected and lead to amputation.
10
However,
the diagnosis of DPN is oen delayed by the fact that
neuropathy oen develops slowly over time.
26
Consistent
monitoring of glycemic control and the complications
are therefore crucial concerns in ODM.
e ODM with DPN in this study also exhibited
less knee extensor strength compared with those without
DPN. e declined muscle strength of the knee and
ankle were reported among people with T2DM with and
without DPN compared with the nonDM control group.
29
e isometric performance of the knee extensors was
also suggested to be an assessment for fall risk among
ODM.
30
Poorer static and functional balance was observed
among ODM with DPN identied by mCTSIB, FRT and
TUG. ese impairments might also contribute to the
increased prevalence of falls in this study. During the
mCTSIB, dierences in dependency on sensory inputs
were identied, i.e., somatosensory during EO and EC
on a foam surface,
31
visual during EC on rm and foam
surfaces
32
and vestibular by EC standing on a foam
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surface.
33
ODM were found to be somatosensory dependent
because they presented impaired postural control during
somatosensory disruption
34,35
while ODM with DPN lost
their balance during deprived visual input.
34
Our results
implied an assumption similar to related studies,
34,36
i.e.,
ODM with DPN were visual dependent because they
tended to rely more on visual inputs to compensate for
their declined somatosensory inputs. ese patients
might be able to achieve acceptable postural control
using an appropriate compensatory strategy.
37
However,
in cases of the other sensory input limitations such as
dim light, an irregular trail or presenting of retinopathy
and vestibulopathy, the risk of fall among these patients
would be even higher.
e static balance reected by the FRT signicantly
diered between ODM with and without DPN. Lower FRT
values were observed among ODM with somatosensory
impairment.
38
e sensory threshold of hallux was reported
to be a predictor of reach distance and center of mass
displacement among patients with DM.
38
Considering
the manner of FRT performance, the strength of lower
limb muscles would also inuence the test results. In this
study, knee extensor muscle strength was reduced among
ODM with DPN. e ankle plantar exors, reported to
signicantly contribute to the center of mass displacement
during forward reach, also had a trend of decreased
strength among ODM with DPN.
38
In this study, the TUG signicantly diered between
groups. e TUG is a gait-based functional test with the
purpose to measure mobility, balance, walking ability,
locomotor performance and falls risk among older people.
24
In addition to the reduced proprioception, the dynamic
balance impairment among the participants with DPN might
have been associated with lower limb muscle weakness
reected by the reduced strength of knee extensors. e
correlation of TUG and knee extensor muscle strength
has been highlighted among older people.
35
In conclusion, this study presented the contribution
of DNP on higher fall occurrence among ODM with
DPN. e poorer performances of static and dynamic
balance as well as less knee extensor strength were also
found among ODM with DPN. e results suggested
that clinicians should systematically monitor and control
these impairments as an approach to prevent falls among
ODM.
is study had some limitations. e fall occurrence
data in this study was based on the interviews. Recall bias
is likely especially regarding self-reported falls among
ODM. Other factors reported to aect balance and falls in
DM including body mass index, medications, depression
and fear of falling were not assessed. We also did not
monitor the occurrence of hypoglycaemia and the severity
of the neuropathic pain. ese DM associated conditions
were postulated to lead to falls among individuals with
DM due to their eects on the attention decit, slow
psychomotor speed as well as orthostatic hypotension.
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