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Physical activity and exercise on diabetic foot related outcomes: A systematic

review

Article  in  Diabetes Research and Clinical Practice · February 2018

DOI: 10.1016/j.diabres.2018.02.020

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 DIAB 7233 No. of Pages 10, Model 7
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1
Contents available at ScienceDirect

Diabetes Research
and Clinical Practice
journal homepage: www.elsevier.com/locat e/dia bre s

2 Review
6
4
7
Physical activity and exercise on diabetic foot
5 related outcomes: A systematic review

8 Monica Matos a,*, Romeu Mendes b,c,d, André B. Silva e, Nelson Sousa a,b
a
9 Research Center in Sports Sciences, Health Sciences and Human Development, Vila Real, Portugal
b
10 University of Trás-os-Montes e Alto Douro, Vila Real, Portugal
c
11 Public Health Unit, ACES Douro I – Marão e Douro Norte, Vila Real, Portugal
d
12 EPIUnit – Instituto de Saúde Pública, Universidade do Porto, Porto, Portugal
e
13 Centro Hospitalar Tondela Viseu, Ophthalmology Department, Portugal
14

15
16
A R T I C L E I N F O A B S T R A C T
1
3 8
1
32
19 Article history: Background: Diabetic foot is one of the most common complications of diabetes. It has the
33
20 Received 17 October 2017 potential risk of pathologic consequences including infection, ulceration and amputation,
34
21 Received in revised form but a growing body of evidence suggests that physical activity and exercise may improve
35
22 1 February 2018 diabetic foot outcomes.
36
23 Accepted 13 February 2018 Objective: To analyze de effects of exercise and physical activity interventions on diabetic
37
24 Available online xxxx foot outcomes.
38 Methods: A comprehensive and systematic search was conducted according to PRISMA rec-
39 ommendations. Only controlled clinical trials with patients with diabetes were included.
25 Keywords:
40 Results: Six studies, involving 418 patients with diabetes, were included. Two studies used
26 Physical activity
41 only aerobic exercise; two studies combined aerobic, resistance and balance exercise; and
27 Exercise
42 two studies combined aerobic and balance exercise by Thai Chin Chuan methods. Physical
28 Diabetic foot
43 activity and exercise significantly improved nerve velocity conduction, peripheral sensory
29 Diabetes
44
30 function and foot peak pressure distribution. Moreover, the ulcers incidence rate per year
45 was lower in the interventional groups, compared with the control [0.02 vs. 0.12].
46 Conclusion: This review suggests evidence that physical activity and exercise is an effective
47 non-pharmacological intervention to improve diabetic foot related outcomes. Combined
48 multi-disciplinary treatments are more effective in the prevention of foot complications
49 in patients with diabetes.
50 ! 2018 Elsevier B.V. All rights reserved.
51

52

53

* Corresponding author at: CIDESD, Universidade de Trás-os-Montes e Alto Douro, Parque Desportivo da UTAD, 5000-801 Vila Real,
Portugal.
E-mail addresses: m.s.matos8@gmail.com (M. Matos), romeuduartemendes@gmail.com (R. Mendes), andreborgessilva@outlook.com
(A.B. Silva), nelsons@utad.pt (N. Sousa).
https://doi.org/10.1016/j.diabres.2018.02.020
0168-8227/! 2018 Elsevier B.V. All rights reserved.

Please cite this article in press as: Matos M et al. Physical activity and exercise on diabetic foot related outcomes: A systematic review. Diabetes
Res Clin Pract (2018), https://doi.org/10.1016/j.diabres.2018.02.020
 DIAB 7233 No. of Pages 10, Model 7
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54 Contents

55 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
56 1.1. Background . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
57 1.1. Background . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
58 1.2. Purpose of this review . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
59 2. Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
60 2.1. Data sources and search strategy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
61 2.1. Data sources and search strategy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
62 2.2. Study selection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
63 2.3. Data extraction and quality assessment. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
64 3. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
65 3.1. Selection of studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
66 3.2. Assessment of risk of bias . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
67 3.3. Key characteristics of included trials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
68 3.4. Primary outcomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
69 3.5. Secondary outcomes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
70 4. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
71 4.1. Limitations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
72 4.2. Recommendations for future research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
73 5. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
74 5.1. Practice recommendations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
75 6. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
76 Contributorship . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
77 Funding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
78 Conflicts of interest . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
79 Disclaimer. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
80 Appendix A. Supplementary material. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
81 References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00
82
83
84 1. Introduction with diabetes by 80%. Foot ulcers, with or without signs of 109
infections, and amputations are major causes of morbidity 110
85 1.1. Background [19–23] and disability in these patients, leading to significantly 111
lower daily activity [24,25] and is even correlated with a higher 112
86 Diabetic foot ulcer is defined as a full-thickness wound that risk of death [20,21,23,26]. The management of ulcers and 113
87 destroys the deep tissues and develops at a level distal to their prevention is important to ensure quality of life and 114
88 the ankle and is associated with neurological abnormalities decrease comorbidities and death [19]. 115
89 in patients with diabetes [1–3] These ulcers can be classified
90 as neuropathic, ischemic or neuro-ischemic [4–6]. The neuro-
91 pathic, commonly occur on the plantar surface of the meta- 1.2. Purpose of this review 116
92 tarsal heads, or in areas overlying a bone deformity and is
93 usually induced by foot deformity and high foot pressures, There is an establish evidence of a positive association 117
94 provoking tissue damage. Once the tissue breakdown, the between exercise and diabetes, particularly by improving gly- 118
95 resultant ulceration becomes chronic as the insensate foot cemic control, and insulin sensitivity in individuals with type 119
96 fails to convey nociceptive stimuli which are necessary to pro- 2 diabetes, along with positive effects on lipids, blood pres- 120
97 voke protective behavior [7–9] as a consequence of nerve sure, cardiovascular events, mortality, and quality of life 121
98 damage, affecting peripheral sensation and fine vasomotor [27,28]. However, less is known about the effects of physical 122
99 control of the pedal circulation [1,10,11]. Ischemic ulceration activity and exercise in diabetic foot outcomes. Recent studies 123
100 can be represented as an absence of foot pulses, mainly have suggested that physical activity and exercise may 124
101 because of macrovascular or microvascular disease [12,13] improve the distribution of dynamic plantar loading, nerve 125
102 causing a hard healing of the wound, result of an inadequate velocity conduction and foot mobility function, reflecting a 126
103 vascular perfusion in the lower limb [14,15] and frequently better involvement of the whole foot during walking process 127
104 occurs on the tips of the toes or on the lateral border of the [29,30] and decreasing the incidence of foot ulcer or lesion 128
105 foot [16,17]. The neuro-ischemic ulceration has both neuro- [31–33]. 129
106 pathic and ischemic and it develops on the margins of the Therefore, the purpose of this systematic review was to 130
107 foot and toes usually from the pressure of poorly fitted shoes analyze the effects of exercise and physical activity interven- 131
108 [18]. Foot ulcer precedes the major of amputations in patients tions on diabetic foot outcomes. 132

Please cite this article in press as: Matos M et al. Physical activity and exercise on diabetic foot related outcomes: A systematic review. Diabetes
Res Clin Pract (2018), https://doi.org/10.1016/j.diabres.2018.02.020
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133 2. Methods Online Library; Web of Science and Scopus. The following 142
keywords were used: ((feet OR foot) [title] AND (diabetes OR 143
134 This systematic review was conducted in accordance with the diabetic OR neuropathy OR ulcer*) [title] AND (‘‘physical activ- 144
135 Preferred Reporting Items for Systematic Review and Meta- ity” OR exercise OR training OR walking OR jogging OR cycling 145
136 Analyses (PRISMA) guidelines. OR running OR swimming OR pilates OR yoga OR rowing OR 146
climbing) [title]). Electronic databases were searched from 147
137 2.1. Data sources and search strategy the beginning until July 2017. 148

138 Comprehensive and systematic searches were conducted in 2.2. Study selection 149
139 February 2017 by two independent authors [MM and NS] using
140 the following electronic databases and a combination of med- Two authors [MM and NS] independently screened the title 150
141 ical subject headings and keywords: PubMed; The Cochrane and abstract of every citation found in our literature search. 151
Studies of potential relevance were the target of a search for 152
the full text version, and eligibility criteria were applied. 153
According to PRISMA recommendations, inclusion and exclu- 154
sion criteria are based on relevant study characteristics (par- 155
ticipants, intervention, comparator, outcome, study design). 156
Studies were included if: (i) the population was composed 157
by patients with a diagnosis of diabetes regardless of etiology, 158
or a clinical diagnosis of diabetic peripheral neuropathy, 159
polyneuropathy or diabetic foot ulcer; (ii) the intervention 160
was any form of supervised physical activity at a care center 161
or at home; (iii) the comparator was daily-life physical activity 162
(absence of supervised physical activity or exercise regimen) 163
and/or usual foot care education. 164
Non-human articles were excluded from this systematic 165
review as well as studies lacking original data (e.g. letters, 166
review articles or editorials), articles on unrelated topics, 167
studies not reporting outcome of interest and studies con- 168
taining <10 participants. In addition, clinical trials with no 169
control group were also excluded as well as clinical trials with 170
nonspecific exercise intervention. 171

2.3. Data extraction and quality assessment 172

Eligible studies were examined independently by two collabo- 173

rators [MM and NS], and any disagreement was settled via 174
discussion among the authors. The study features extracted 175
from each paper include: first author, year of publication, pre- 176
disposing factor, number of participants in the intervention 177
and control groups, mean or range age of participants, dura- 178
tion of intervention, a description of the intervention and 179
control groups, primary and secondary outcomes, and main 180
results. A meta-analysis was deemed unfeasible because of 181
the small number of studies and heterogeneous outcome 182
measures. 183
Risk of bias was assessed independently by two research- 184
ers [MM and NS], who were blinded to each others’ quality 185
assessment. All studies were scored using the PEDro critical 186
appraisal tool for experimental studies. 187
PEDro is a reliable tool consisting of 11 items [34]. Item 1 is 188
related to external validity and is not used in the scoring, as 189
described in the PEDro guidelines. Each criterion can be 190
answered with ‘yes’ or ‘no’. ‘Yes’ was rated with 1 point, 191
‘no’ with 0 points. The possible maximum score is 10 points. 192

Fig. 1 – Flow diagram of the included studies. Studies with a total PEDro score of at least 5 points were con- 193

Please cite this article in press as: Matos M et al. Physical activity and exercise on diabetic foot related outcomes: A systematic review. Diabetes
Res Clin Pract (2018), https://doi.org/10.1016/j.diabres.2018.02.020
 4
Res Clin Pract (2018), https://doi.org/10.1016/j.diabres.2018.02.020
Please cite this article in press as: Matos M et al. Physical activity and exercise on diabetic foot related outcomes: A systematic review. Diabetes

Table 1 – Characteristics of the included studies.

23 February 2018
DIAB 7233
Authors/study Participants (N) and Predisposing factor Primary outcome Secondary outcome Intervention group Control group Intervention-duration Results
design mean age (years ±
SD)

Balducci et al. [32] IG – N = 31; Diabetic patients NCV, DL and NAPA Blood pressure Supervised aerobic Did not perform 4 years Improvements:
Randomized 49 ± 15.5 y type 1 or 2 without for: PMN and sural BMI exercises (treadmill) supervised physical 4 h weekly PMN IG: DL < 0.9% (N.S.), NAPA < 13.5% (N.S),
controlled trial CG – N = 47; symptoms of DPN SSN FBG 50–85% of the heart activity NCV > 3.9% (p < 0.05);
52.9 ± 13.4 y VPT at malleolus FFM rate reserve SSN IG: DL < 4.7% (N.S.), NAPA > 0.9% (N.S.),
and hallux %FM NCV > 0.8% (N.S.)
HbA1c PMN and SSN p < 0.001 between groups
Lipid profile Sensory neuropathy IG > 6.4%, CG > 29.8%, (p <
Microalbuminuria 0.05)
MLTPA VPT: IG > 12.9%, CG > 21.3%, (p < 0.05)
Waist circumference No changes:
Secondary outcomes (N.S.)

diabetes research and clinical practice

LeMaster et al. [31] IG – N = 41; Diabetic patients Foot lesions/ulcers Daily steps at baseline From 1 to 3 months – From 1 to 3 months – 12 months Improvements:
Randomized con- 66.6 ± 10.4 y type 1 or 2 with PN were photographed and at 3, 6, 12 months by performed 3 at- 8 therapist session IR: all lesions IG < 44.6%, CG < 31.1%
trolled trial CG – N = 38; and examined ankle accelerometers for home sessions with at-home only to IR: lesion episodes IG < 43.0%, CG < 37.8%
64.8 ± 9.4 y IR 14 days (TDS, S30-min therapist, weekly for examine feet IR: full-thickness ulcer episodes IG < 47.2%, CG
and WWBA) 1 h (lower-extremity From 1 to 12 months < 19.0%
Ambulatory minutes per muscles – diabetic foot care IR: weight-bearing full-thickness plantar
week strengthening and education, regular ulcers < 60.0% IG, >76.0 CG
6MWT balance exercises) foot care. IR: weight-bearing ulcers risk 0.02 in IG, 0.12 in
From 1 to 12 months CG
– self-monitored TDS: CG < 13.1% (p < 0.05) and IG < 4.6% (N.S.)
walking program S30-min IG > 13.7% at 6 months, (p < 0.05) and
and motivational CG < 6.1% (N.S.), p < 0.01 between groups
telephone calls No changes:
every 2 weeks 6MWT
+ Ambulatory minutes IG < 3.7% (N.S.),
diabetic foot care CG < 15.3%, (p < 0.05)
education, regular
foot care
Hung et al. [36] IG – N = 28; IG – Diabetic NCV of bilateral FBG Tai Chi Chuan No exercise 12 weeks Improvements:
Controlled clinical 58.1 ± 13.4 y patients type 2 (6 motor: median, IRI exercises 3 times weekly NCV
trial CG – N = 32; with neuropathy) ulnar, peroneal, and Light to moderate 1 h session Right motor median: IG > 2.3%, CG < 0.9%
56.6 ± 13.3 y CG (healthy adults) tibial nerves intensity (p = 0.037)
NCV of bilateral Left motor median: IG > 2.1%, CG < 0.2%

x x x ( 2 0 1 8 ) x x x –x x x
sensory: median and (p = 0.043)
ulnar Right motor tibial: IG > 4.8%, CG < 0.4%
DL bilateral: motor (p = 0.027)
median, ulnar, Left motor tibial: IG > 2.7%, CG < 0.2%
peroneal and tibial. (p = 0.036)
DL for sensory: IG: Right NVC’s p = 0.046, left NVC’s p = 0.041)
median and ulnar DL sensory:
Proximal amplitude Right ulnar: IG < 5.6%, CG < 0.5% (p = 0.044);
of the motor/ Left ulnar: IG < 5.0%, CG < 0.5% (p = 0.047)
sensory response FBG: IG < 11.3%, CG < 0.6% (p = 0.035)
No changes:
DL bilateral: motor median, ulnar, peroneal
and tibial. DL sensory median. Proximal
amplitude
IRI: IG < 23.2%, CG < 10.5% (N.S.)

No. of Pages 10, Model 7

Ahn & Song [35] IG – N = 30; Diabetic patients SWME FBS Tai Chi Chuan Routine education 12 weeks Improvements:
Quasi-experimental 66.05 ± 6.42 y type 2 with TSS HbA1c exercises on diabetes, diet, twice weekly SWME: IG < 2.6%, CG < 6.1% (p = 0.535)
study CG – N = 29; neuropathy Single-leg stance Low-to-moderate exercise, foot care, 1hour session TSS: improvements for IG (19.5%), (p = 0.042)
62.73 ± 7.53 y Quality of life (Korean SF- intensity and medication 3 months follow-up compared CG
36v2) + twice during study FBS: IG < 9.0%, CG > 8.3% (p = 0.036)
routine education period HbA1c: IG < 6.0%, CG > 3.7% (p = 0.004)
on diabetes, diet, Dropout N = 10 Single leg stance: IG > 34.2%, CG < 9.2%
exercise, foot care, (p = 0.044)
and medication Korean SF-36 IG: physical functioning > 7.0%,
twice during study bodily pain > 17.6%, physical role limitation >
period 29.0%, emotional role limitation > 30.3%, social
Dropout N = 10 functioning > 15.6%
 Table 1 – (continued)
Res Clin Pract (2018), https://doi.org/10.1016/j.diabres.2018.02.020
Please cite this article in press as: Matos M et al. Physical activity and exercise on diabetic foot related outcomes: A systematic review. Diabetes

23 February 2018
DIAB 7233
Authors/study Participants (N) and Predisposing factor Primary outcome Secondary outcome Intervention group Control group Intervention-duration Results
design mean age (years ±
SD)

Dixit et al. [33] IG – N = 40; Diabetic patients NVC in PMN and BMI Education for foot Education for foot 8 weeks Improvements:
Randomized con- 54.40 ± 1.24 y type 2 with PN SSN by Hip circumference care, diabetic diet care, diabetic diet 3–6 days weekly NVC
trolled trial CG – N = 47; Electromyogram Waist circumference and standard and standard PMN: IG > 7.3%, CG < 0.5% (p = 0.03)
59.45 ± 1.16 y MDNS Waist to hip ratio medical care medical care SSN: IG > 32.6%, CG > 1.1% (p < 0.001)
± ± MDNS scores IG < 44.1%, CG > 7.5% (p < 0.001)
treadmill exercises Telephone calls No changes:
(40–60% Heart rate every second week BMI, hip circumference, waist circumference
reserve) moderate of the month and and waist to hip ratio
intensity evaluated for
Dropout N = 11 medical care at
fourth and eight

diabetes research and clinical practice

Sartor et al. [30] IG – N = 26; 59 ± 4 y Diabetic patients MNSI questionnaire ABC Scale
Randomized CG – N = 29; 60 ± 12 y type 1 or 2 with MNSI physical MF: extensor digitorum
controlled trial polyneuropathy assessment of feet longus and brevis;
PP, TPP, PTI, COP extensor halluces longus
(heel, midfoot, and brevis; flexor
medial forefoot, digitorum brevis; flexor
lateral forefoot, hallucis brevis; lumbrical;
hallux and toes) interosseous; tibialis
anterior; triceps surae
FT: ankle flexion, ankle
extension, toes flexion,
toes extension
KK: Sagittal ankle range
of motion; sagittal ankle
angle; sagittal peak of
extensor; sagittal peak of
flexor
weeks
Dropout N = 10
Physical therapy and Didn’t receive any 12 weeks Improvements:
instructions to physical therapy, twice weekly PP: IG < 23.3% midfoot (p < 0.01), <8.8% lateral
exercise at home, for instructions or 40-60 min/session forefoot (p < 0.01) follow-up
foot–ankle and gait intervention Follow-up: IG assessed at TPP: IG > 1.7% heel (p = 0.03), <2.1% lateral
((a) increase foot and Only received week 24 forefoot (p = 0.01) interaction effects
ankle range of customized medical PTI: IG > 9.3% medial forefoot, >16.7% hallux
motion, (b) care after 12 weeks (p < 0.01). Interaction effects
strengthen foot and midfoot (p = 0.03)
ankle muscles, (c) COP: IG < 20.0% midfoot (p = 0.03), total foot
increase foot and area < 25.0% (p = 0.05) interaction effect
ankle performance Total COP IG: follow up p < 0.001
through functional MF: IG > 25.0% flexor digitorum brevis, >25.0%
exercises, and (d) tibialis anterior
increase walking No changes:
skills and foot MF: Extensor digitorium longus and brevis,
rollover training) extensor hallucis longus and brevis, flexor
hallucis brevis, lumbrical, interosseous, triceps
surae
FT, KK, MNSI questionnaire, MNSI physical
assessment, ABC

Legend: ABC – activities-specific balance confidence; BMI – body mass index; CG – control group; COP – mean velocity center of pressure; DFU – diabetic foot ulcer; DL – distal latency; DPN – diabetic

x x x ( 2 0 1 8 ) x x x –x x x
peripheral neuropathy; FFM – fat free mass; FM – fat mass; FT – functional test; HbA1c – glycated hemoglobin; IG – intervention group; IR – incidence rate; IRI – insulin resistance index; KK – kinetic
and kinematic; MDNS – Michigan diabetic neuropathy score; MF – muscle function; MLTPA – Minnesota leisure time physical activity questionnaire; MNSI – Michigan neuropathy screening
instrument; NAPA – nerve action potential amplitude; N.S – non significant; NVC – nerve velocity conduction; PMN – peroneal motor nerve; PN – peripheral neuropathy; PP – peak pressure; PTI –
pressure time integral; SSN – sural sensory nerve; SWME – Semmes-Weinstein 10-g monofilament examination; S30-min – steps 30 min exercise; TDS – total daily steps; TPP – time to peak pressure;
TSS – total symptom score; VPT – vibration perception threshold; WWBA – minutes per week of weight-bearing activity; 6MWT – 6 min walk test.

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sidered to have low risk of bias. Disagreement between the 194

total score reviewers regarding the quality score of an article was dis- 195
cussed until consensus was reached. If necessary, a third 196
PEDro

opinion was sought [RM]. 197

10
6
9
5
6
6
of variability

3. Results
group results measures/

198
measures
5. Blinding 6. Blinding 7. Blinding 8. Outcome 9. Intention 10. Between 11. Point

3.1. Selection of studies 199

1
1
0
1
1
1
We identified a total of 173 articles by our search strategy. 200
From the 173 articles, 58 duplicated references were excluded, 201
remaining 115 articles. In total, 24 articles were assessed for 202
eligibility and a total of 91 articles were excluded based on 203
title. The study selection process and the reasons for exclusion 204
1
1
1
1
1
1

of the articles are shown in Fig. 1. At the end of the research we 205
identified 13 eligible articles but not all of them could be 206
data > 85% to treat

included due to a lack of a control group or due to a nonspecific 207

exercise intervention. Therefore, six clinical trials were 208
0
1
0
1
0
1

included in our systematic review: three studies with type 2 209

diabetes participants, and three studies with both type 1 and 210
type 2 diabetes participants (see Table 1). There was complete 211
agreement between reviewers regarding study selection. 212
1
1
1
1
0
1

3.2. Assessment of risk of bias 213

therapist assessor

Risk of bias scores for included studies is shown in Table 2. 214

0
0
1
0
1
1

There was total agreement for PEDro scores of all reviewed 215
studies. Two studies had a PEDro score equal to or greater 216
than seven, indicating a high methodological quality; four 217
studies scored between five and seven, indicating a moderate 218
0
0
0
0
0
0

methodological quality. The highest PEDro rating was 10, with 219
an average of seven among the included studies. 220
comparability subject
Table 2 – Risk of bias assessment of the included studies by the PEDro score.

3.3. Key characteristics of included trials 221

0
1
1
0
0
1

A summary of eligible studies is shown in Table 1. The interven- 222

1. Eligibility 2. Random 3. Concealed 4. Baseline

tion programs ranged from 8 weeks to 4 years. The articles were 223
published between 2006 and 2014. A total of 418 participants 224
were elected – 196 of which were allocated to the intervention 225
1
1
0
1
1
1

group and 222 to the control group; 41 of these participants 226

dropped out across all studies. The mean age among partici- 227
allocation allocation

pants ranged from 49 ± 15.5 to 66.6 ± 10.4 years. Predisposing 228

factors for the studies were: clinical diagnosis of diabetic neu- 229
ropathy [31,33,35], with polyneuropathy [30], without symptoms 230
0
1
0
0
0
1

of diabetic peripheral neuropathy [32] and one study only refer 231
six patients with neuropathy due to diabetes mellitus [36]. 232
The treatment approach (exercise) differed among studies: 233
two studies used only aerobic exercise, walking-based [32,33]; 234
1
1
0
0
1
1

two studies combined aerobic exercise walking-based, resis- 235

tance exercises for the lower limbs muscles, and balance 236
criterion

exercise [30,31], and two studies combined aerobic and bal- 237
ance exercise by Thai Chin Chuan methods [35,36]. In addi- 238
1
1
1
1
1
1

tion, some trials used a system of education for foot care 239
LeMaster et al. [31]
Balducci et al. [32]

plus routine education on diet [31,33,35,37]. 240

Ahn & Song [35]

Sartor et al. [30]

Hung et al. [36]

Dixit et al. [33]

1 = Yes; 0 = No.

3.4. Primary outcomes 241

Study

Nerve velocity conduction was measured in three studies (see 242

Table 1) using a Medelec MS 928 Neurostar electrorecorder 243

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244 [32], a Nicolet Viking IV electrorecorder [36], and the RMS One study [30] measured peak pressure, time to peak pres- 304
245 Aleron 201 electromyogram/NCV machine [33]. All three stud- sure and center of pressure over plantar surface by the Pedar- 305
246 ies found significant improvements in the intervention group, X System. The authors reported significant reductions in time 306
247 while no differences were detected in the control group. One to peak pressure on heel by 1.7% (p = 0.03) and lateral forefoot 307
248 of them reported significant improvements in intervention by 2.1% (p = 0.01), as wells as a significant reduction in peak 308
249 group in nerve velocity conduction of peroneal motor nerve pressure after follow-up at midfoot (23.3%, p < 0.01) and at lat- 309
250 compared to controls (p = 0.03) and the same was observed eral forefoot (8.8%, p < 0.01) in the intervention group. The 310
251 for sural sensory nerve (p < 0.001) after 8 weeks of a super- same group also achieved significant differences in center of 311
252 vised walking program [33]. In the other study [32], authors pressure in midfoot (20.0% reduction, p = 0.03), and differ- 312
253 reported significant differences between groups in peroneal ences in total foot area (25.0% reduction, p = 0.05), at 12 weeks 313
254 motor nerve (p < 0.001) and sural sensory nerve (p < 0.001) showing a better control of the foot-flattening (see Table 1). 314
255 during the four years of study period. Also, authors found a Total center of pressure after follow-up had significant differ- 315
256 significantly increased in intervention group for peroneal ences (p < 0.001). After 12 weeks of combined exercise, inter- 316
257 nerve velocity conduction (p < 0.05) and a non-significant vention group increased muscle function in flexor digitorum 317
258 decreased in controls. For sural there was no significant brevis (25.0%) and tibialis anterior (25.0%) suggesting that 318
259 increase in intervention group. The third study [36] reported exercise may slow down the prognosis of diabetes chronic 319
260 significant improvements in nerve velocity conduction after complications. All functional testes except ankle extension, 320
261 12 weeks of a Tai Chi Chuan intervention program (right showed a difference between groups after 12 weeks, which 321
262 motor nerves p = 0.046; and left motor nerves p = 0.041) while points to an improvement in intervention group and a wors- 322
263 no significant improvements were detected in control group. ening in control group. 323
264 Authors attribute better results in nerve velocity conduction One study measured the incidence rate of foot lesions by 324
265 to bilateral median (right p = 0.037; and left p = 0.043) and tib- taking photographs of the foot and making an examination 325
266 ial (right p = 0.027; and left p = 0.036) reaching a significant of patient’s foot [31]. The authors reported that incidence 326
267 improvement after Tai Chi Chuan. The authors of this study rates of all lesions decreased in intervention in 44.6% from 327
268 also found that exercise decreased distal latency in interven- 6 months to 12 months and decreased in controls only 328
269 tion group by 5.6% in right sensory ulnar and 5.0% in left sen- 31.1%. Also, the incidence rate of weight-bearing full- 329
270 sory ulnar showing that the interval between the stimulation thickness plantar ulcers decreased in intervention by 60.0% 330
271 of a compound muscle and the observed response was faster. and increased in controls by 76.0%, showing a risk of 0.02 ul 331
272 Peripheral sensory function was measured in two studies cers/person-year in the intervention group and a risk of 0.1 332
273 (see Table 1) through the vibration perception threshold at 2 ulcers/person-year in controls. Ulcer rates on plantar 333
274 the Malleolus and Hallux by means of a Biothesiometer [32], weight-bearing areas, total foot ulcer and foot lesions inci- 334
275 and by the Semmes-Weinstein 10-g monofilament examina- dence rates did not differ significantly between groups after 335
276 tion [35]. One study reported no differences between groups 6 or 12 months of combined exercise. 336
277 in peripheral sensory function after 12 weeks of a Tai Chi
278 Chuan intervention program, but reported significant 3.5. Secondary outcomes 337
279 improvements (by 19.5%) in total symptom score for periph-
280 eral neuropathy (p = 0.042) in the intervention group [35]. Regarding secondary outcomes, statistical significance was 338
281 Also, the development of vibration perception threshold ana- reached in fasting blood glucose (p = 0.036 [35]; p = 0.035 339
282 lyzed in one study was significantly higher in the control [36]), and glycated hemoglobin (p = 0.004 [35]) after the train- 340
283 group than in the intervention group (12.9% vs. 21.3%, p < ing program in patients with type 2 diabetes compared to 341
284 0.05), showing greater sensory dysfunction and suggesting controls. Although the insulin resistance index decreased by 342
285 that long-term aerobic exercise training can prevent the onset 23.2% in intervention and only 10.5% in controls, these results 343
286 or modify the natural history of diabetic peripheral neuropa- were not statistically significant [36]. 344
287 thy [32]. Regarding functional fitness, the results are inconsistent. 345
288 Two studies controlled the scores of Michigan Neuropathy In one study [31], there were significant differences between 346
289 Screening Instrument (MNSI). Sartor et al. [30] reported no sig- groups (exercise program vs. control) on the number of steps 347
290 nificant differences between groups for the MNSI question- counts per 30-min (p < 0.01), in which the intervention group 348
291 naire and foot physical examination (Table 1). However, in increased 13.7% steps counts (p < 0.05) whereas the control 349
292 the experimental group, there was a significant reduction of group decreased 6.1%. However, the authors did not found 350
293 2 points in the MNSI questionnaire, which remained after differences in the 6-min walk test between baseline and six 351
294 the 12 week follow-up (improvement of 33.3%), improving or 12 months. Also, there was no difference between groups 352
295 the clinical condition of the patients, and a reduction of the in ambulatory physical activity per week from baseline and 353
296 score for the physical examination of the feet from 4.5 to 4 six or 12 months. Balducci et al. [32] also found no differences 354
297 points at the follow-up assessment compared to the corre- neither between groups or after four years of aerobic exer- 355
298 sponding scores after 12 weeks (improvement of 11.11%) but cises in total physical activity. In other study [34], the perfor- 356
299 not significant. In the other study, Dixit et al. [33] reported sig- mance of single leg stance was significant different between 357
300 nificant differences in the Michigan Diabetic Neuropathy groups (p = 0.044), as intervention group increased their bal- 358
301 Score (MDNS) after eight weeks (p < 0.001) with a decreased ance by 34.2% and controls decreased by 9.2%. Although Sar- 359
302 in score by 44.1% in the intervention group and an increase tor et al. [30], found improvements in balance controlled by 360
303 of 7.5% for control group. Activities-specific Balance Confidence (ABC) Scale, reporting 361

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362 an increase of 2.4% after 12 weeks of exercise intervention ings suggest that exercise may positively enhance peripheral 419
363 and 6.0% after 24 weeks of follow up, these results were not circulation and reduce peak plantar pressures, and therefore 420
364 significant. The same authors found no differences after 12 reducing diabetic foot ulcer risk and improving diabetic foot 421
365 weeks in intervention group in muscle function, but the con- outcomes. 422
366 trol group worsened in this parameter. In the present review, two studies [35,36] demonstrated an 423
367 Quality of life was controlled by The Korean SF-36 v2 improvement in fasting blood glucose and glycated hemoglo- 424
368 instrument showed better results in life scores on domains bin levels, but these benefits are currently well documented 425
369 of physical functioning (7.0%, p = 0.028), bodily pain (17.6%, in the literature [28,42–45]. Concerning physical function, 426
370 p = 0.009), physical role limitation (29.0%, p = 0.006), emo- the amount of steps taken within this patients after an inter- 427
371 tional role limitation (30.3%, p = 0.002), and social functioning vention program, suggests that they are liable to increase 428
372 (15.6%, p = 0.001) in diabetic patients who did the Tai Chi exercise performance [31]. Also, patients in a Tai Chi Chuan 429
373 Chuan program [35]. program increased their balance in single leg stance [35] 430
374 For the remaining clinical outcomes, such as body mass and another intervention group had an improvement in scale 431
375 index, waist circumference, waist to hip ratio, fat mass per- for Activities-specific Balance Confidence [30]. 432
376 centage, free fat mass, microalbuminuria, lipid profile and In every study analyzed in this review, the exercise pro- 433
377 bone densitometry [32] there were no significant changes, gram implemented was safe for the participants without 434
378 but exercise did not cause a deterioration in the assessed inducing or increasing risk of diabetic foot. Also, none of 435
379 parameters. the controlled outcomes worsen at the end of the studies. 436
Furthermore, patients in exercise programs have demon- 437

380 4. Discussion strated a better quality of life regarding physical, emotional 438
and social domains [35]. 439
381 The main finding of this systematic review is that exercise is a However, there is still insufficient data regarding the best 440
382 beneficial non-pharmacological treatment in diabetic foot treatment approach for this patient population. There is a 441
383 outcomes, particularly in increasing nerve velocity conduc- wide range of effective exercise interventions (Table 1) such 442
384 tion of the lower limbs. Additional benefits can be induced as balance, strength-based, aerobic exercises or even a 443
385 by exercise in patients with diabetes, such as skin sensitivity multi-modality treatment (exercise and education for foot 444
386 and intraepidermal nerve fiber density, which can delay the care) that may help reduce or delay the risk of ulceration. 445
387 usual course of diabetic peripheral neuropathy and delay skin The studies included in this review reported long-term 446
388 damage and ulceration. [31,32] and medium-term [30,33,35,36] of exercise programs. 447
389 It is well known that patients with diabetes and neu- In addition, the frequency of physical activity over time is also 448
390 ropathies are associated with low nerve velocity conduction essential, i.e., patients who attended more in exercise weekly 449
391 owing to demyelination and loss of large myelinated fibers, were more likely to be associated with successful results in 450
392 and a decrease in nerve action potentials owing to loss of accordance with international guidelines, however, some 451
393 axons [38–41], but the present review showed that aerobic studies did not describe the intensity of the interventions 452
394 exercise can improve, for example, nerve velocity conduction [30,31]. 453
395 in peroneal motor nerve by 3.9% and 0.8% in sural sensory
396 nerve, also decreasing distal latency by 0.9% [32]. Moreover,
397 Tai Chi Chuan exercises improved nerve velocity conduction 4.1. Limitations 454

398 by 2.3% in right motor median and 2.1% in left motor median,
399 as well as 4.8% in right motor tibial and 2.7% in left motor tib- A key limitation of this systematic review was the large 455

400 ial, reducing overall distal latency by 5% facing greater gains heterogeneity of the instruments to measure diabetic foot 456

401 [36]. However, a combined exercise program with aerobic, foot related outcomes and this heterogeneity remained very 457

402 care education, diabetic diet and standard medical care broadly defined in the current literature, making it difficult 458

403 showed a higher impact, with gains in nerve velocity conduc- to compare results. Another limitation is the lack of informa- 459

404 tion by 7.3% in peroneal motor nerve and 32.6% in sural sen- tion about the intensity of the exercise programs in some 460

405 sory nerve [33]. Similar intervention with combined training studies [30,31]. Also, the lack of studies about this theme, 461

406 program for lower-extremity muscles strengthening, balance involving physical activity or exercise in risk of ulceration 462

407 and walking plus diabetic foot care education demonstrated within patients with diabetes are quite few in literature, so 463

408 to reduce long-term incidence rate of foot lesions by 44.6% more studies are required. 464

409 [31].
410 Moreover, most of the participants in this review had 4.2. Recommendations for future research 465

411 symptoms of neuropathies but none of them reported pain

412 or reported skin infections during the studies. The majority This systematic review combined the results of six trials, but 466

413 of participants presented in the studies (Table 1), showed more practice and methodologic work is needed to prove how 467

414 improvements in total symptom score for peripheral neu- physical activity and exercise can involve a better treatment 468

415 ropathy [35] and vibration perception threshold [32] as well for diabetic foot. An easy and homogeneous outcome to be 469

416 as a better physiological foot rollover which reflects in a better easily accessed is required, intended to be effectively applied 470

417 redistribution of plantar pressure [30]. Weight-bearing activi- for non-clinical experts. An homogeneous outcome would 471

418 ties did not increase risk of foot re-ulceration [31]. These find- facilitate the execution of meta-analyses. 472

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473 5. Conclusion Conflicts of interest 519

474 This systematic review suggests physical activity and exercise Monica Matos, Romeu Mendes, André Borges Silva and Nel- 520
475 as an efficient intervention to reduce the risk of diabetic foot. son Sousa declare that they have no conflicts of interest rele- 521
476 Although the variety of physical activity and exercise meth- vant to the content of this review. 522
477 ods implemented in the trials, like aerobic exercise or com-
478 bined modes of exercise, all have brought benefits in Disclaimer 523
479 diabetic foot related outcomes.
480 Moreover, multi-disciplinary treatments, such as physical The views expressed in the submitted article express solely 524
481 activity, diet routine and foot care education, all combined, the views of the contributing authors. 525
482 are more effective in the improvement of diabetic foot out-
483 comes than singular interventions. Appendix A. Supplementary material 526

484 5.1. Practice recommendations Supplementary data associated with this article can be found, 527
in the online version, at https://doi.org/10.1016/j.diabres.2018. 528
485 Long-term physical activity and exercise is an effective tool to 02.020. 529
486 reduce risk of diabetic foot. Apart from the standard medical
487 care, medication, diet and education for foot care, exercise is
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Please cite this article in press as: Matos M et al. Physical activity and exercise on diabetic foot related outcomes: A systematic review. Diabetes
Res Clin Pract (2018), https://doi.org/10.1016/j.diabres.2018.02.020
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