Does strength and quality of life correctly classify people with diabetes according to neuropathy assessments?

Abstract

Background

Diabetes Mellitus (DM) cause a high burden to health systems. Information pertaining to health-related quality of life could be useful towards a better understanding between DM and functioning.

Objective

To investigate the association between muscle strength and quality of life according to the severity of neuropathy in people with DM using different classification methods.

Methods

A total of 67 participants were recruited in a rehabilitation centre and stratified into groups. Isometric ankle dorsiflexor muscle strength was assessed using a portable dynamometer and quality of life (utility) was assessed by the EQ-5D-3L questionnaire. Neuropathy was assessed using The Michigan Neuropathy Screening Instrument (MNSI) and the Neuropathy Disability Score (NDS). A multinomial logistic regression was performed to estimate the association between a set of variables, and the neuropathy classification methods.

Results

Most participants were women aged >60 years, with a mean diagnosis of DM of 16.1 years. The mean utility was 0.66, with those with neuropathy having the worst utility. Female gender was associated with a lower chance of developing neuropathy when compared with individuals with mild (OR: 0.15) and moderate (OR: 0.11) neuropathy. Increased ankle dorsiflexor strength was associated with a lower chance of developing neuropathy compared to those without loss of sensation (OR:0.62).

Conclusion

Women with diabetes were less likely to be classified as having loss of sensitivity and had a lower utility compared with men. Individuals with neuropathy reported the worst utility scores. Moreover, increased ankle dorsiflexion strength was associated with lower chance of having neuropathy.

Keywords

muscle strength rehabilitation diabetes mellitus diabetic neuropathies quality of life

Introduction

Diabetes Mellitus (DM) is a major burden for individuals and healthcare systems. In 2021, data from the 10th edition of the International Diabetes Federation estimated that the number of cases would rise from 643 million in 2030 to 783 million in 2045.¹ Accordingly, peripheral neuropathy is one the most incapacitating aspects of DM, as it may cause pain, cramps, and absence of deep tendon reflexes and/or absence of vibratory and/or sensitivity in the lower limbs.^2,3

Approximately 50% of DM neuropathies are asymptomatic, and the later the diagnosis, the greater the risk of injury and plantar ulcers.^3,4 In addition, one of the major consequences is loss of muscle strength and mobility, especially in the lower limbs.⁵ Furthermore, information on health-related quality of life could be useful to determine the health status of this population to better understand the relationship between DM and clinical and functional aspects.⁶ Quality of life is widely recognised as a relevant outcome to consider in addition to the traditional morbidity and mortality outcomes used in DM, including quality-adjusted life years.⁶

However, we raise a question whether changes in muscle strength and quality of life are associated with sensory classification in relation to the presence of neuropathy. Although previous studies have shown an association between reduced muscle strength and the occurrence of neuropathy,^7,8 the diagnosis of neuropathy is made when subjects have already lost the protective sensitivity of the foot. Conversely, in more subtle cases of decreased sensitivity, it is not known whether there is a relevant loss of muscle strength.

Currently, different classification methods are used to classify individuals with DM according to sensory loss. These methods are widely adopted, however, to the best of our knowledge there is a lack of information on the association of relevant outcomes, such as strength and quality of life, with sensory loss, and whether they might be useful in helping clinicians to anticipate treatment goals based on an expected level of sensory loss. Therefore, the overall aim of this study was to investigate the association between muscle strength and quality of life according to the severity of neuropathy in people with DM using different classification methods.

Method

Study design

Cross-sectional study in which data was collected from March to November 2022 at a Rehabilitation Centre for Diabetes, Specialised Centre for Diabetes, Obesity and Hypertension (Centro Especializado em Diabetes, Obesidade e Hipertensão arterial – CEDOH, in Brazilian Portuguese) in the city of Brasília, Brazil. The study was reported in accordance with the STROBE guideline.

Participants

Participants were users attending the Rehabilitation Centre and recruited at random during their routine appointments. Participants were included if they were: (1) diagnosed with type 2 diabetes mellitus for 5 years or more; (2) male or female; (3) 18 years of age or older; and (4) not pregnant for at least 12 months prior to the study.

The exclusion criteria were: (a) changes in muscle strength, such as neurological, orthopaedic, or rheumatological diseases; (b) active foot ulcers; (c) amputation of any level in the lower limbs; and (d) non-attendance to assessments.

The study was granted approval by the Institutional Ethics Committee under protocol 4.974.078 and 5.217.470, and participants gave their signed informed consent.

Assessments

Participants attended the rehabilitation centre for a single 50-minute face-to-face assessment of sociodemographic information and body mass index (BMI) measurements. Clinical data (most recent glycated haemoglobin - HbA1c values, associated comorbidities, previous screening tests for diabetic neuropathy and retinopathy) were extracted from each participant’s medical record.

Neuropathy screening

This study used two neuropathy screening tools, that is, the Michigan Neuropathy Screening Instrument (MNSI) and the Neuropathy Disability Score (NDS) questionnaires.

The MNSI⁹ is a valid and reliable self-administered instrument consisting of two parts. Part 1 contains 15 questions that add 1 point to each answer ‘Yes’ for questions 1–3, 5–6, 8–9, 11–12, and 14–15, or ‘No’ for questions 7 and 13. Questions 4 and 10 do not score as they deal with the measure of circulatory insufficiency, and measure of general asthenia. A score ≥7 was considered abnormal. Part 2 comprised a physical examination bilaterally, each positive finding on inspection and presence of an ulcer received 1 point bilaterally and on physical examination each finding was scored 0.5 when decreased (vibration, reflex, monofilament sensitivity) and 1 point when absent. Neuropathy was defined by a score >2.0 on the MNSI.

The second screening instrument was the short version of the NDS questionnaire, validated and adapted to the Brazilian Portuguese.¹⁰ The scores for painful, thermal, and vibratory sensations in the tests were (0) if present, and (1) if reduced/absent. For the reflex, the scores were (0) if normal, (1) if present with reinforcement, or (2) if absent, bilaterally. The NDS physical examination score is classified as normal (0–2), mild (3–5), moderate (6–8), or severe (9–10).

Tactile sensitivity assessment

The sensitivity assessment was performed with the Semmes-Weinstein SORRI-Bauru^® nylon monofilament aesthesiometer set,¹¹ which is the gold standard, and a valid and reliable instrument. The instrument was applied with the participant in the supine position and eyes closed, on the plantar region in four recommended areas, namely, point 1 (hallux and distal phalanx) and points 4, 5, and 6 (1st, 3rd, and 5th metatarsals), bilaterally and perpendicular to the skin at 1–2 cm.

The participants were instructed to verbally respond with ‘Yes’ in case of sensitivity in the tested area. The monofilaments in the kit range from 0.07 g to 300 g, with the 10.0 g monofilament being able to detect gross fibre alteration and assess plantar protective sensitivity.

Based on the results, participants were stratified into the following groups of sensitivity: Group 1 – Normal or altered sensitivity for the hand and foot with difficulty with shape and temperature discrimination (0.07 g, 0.2 g, and 2.0 g); Group 2 – Loss of protective sensitivity and hot/cold discrimination (4.0 g and 10g); and Group 3 – Neuropathy, presenting loss of sensitivity to deep pressure, but feel pain (300g).

Strength assessment

Lower limb muscle strength was assessed in kilogram-force (kgf) with a portable Hoggan microFET2^® dynamometer (Hoggan Scientific, LLC, Salt Lake City, UT, USA),¹² based on previous studies.^13–15 The final value used for analysis was the average of three consecutive attempts. The portable dynamometer has inter- and intra-assessor reliability and was considered valid for muscle strength assessments.^13,16

The participant was positioned in supine position with the ankle relaxed and hips and knees extended. After positioning, they were instructed to perform a maximum voluntary ankle dorsiflexion isometric contraction lasting 5 seconds, with a 30-second interval between three attempts.

Quality of life assessment

The Brazilian Portuguese validated version of the Euroqol EQ-5D-3L was used.¹⁷ The questionnaire is self-administered, and measures five health dimensions: Mobility, Self-Care, Usual Activities, Pain/Discomfort, and Anxiety/Depression. These are classified into 3 levels of severity with the response options: (1) no problems, (2) some problems, and (3) extreme problems. The result represents the dimensions evaluated by this system that allows describing a total of 243 possible health states, translated into codes representing utility values ranging from 1 (perfect health) to −0.176.

Data analysis

Assumptions of data normality were confirmed using the Shapiro-Wilk test. Data were analysed descriptively using mean and standard deviation, absolute and relative frequencies.

We adopted a multinomial logistic regression with a backward stepwise method to estimate the association between the predictive variables age, gender, dorsiflexion strength, utility, glycated haemoglobin, and time since the diagnosis, and different diagnosis methods (categorical dependent variable). For regression model 1, we adopted the filament method as the independent variable, and for regression model 2, we adopted the NDS method as the independent variable to investigate whether the set of predictive variables corrected classified the participants. We used the monofilaments and the NDS as independent variables, because of two main reasons: (a) the monofilaments are the gold standard measure of neuropathy, and (b) the NDS is widely used in the healthcare system, especially in the rehabilitation centre where we recruited the participants.

Collinearity assumptions between the independent variables were confirmed in an exploratory analysis, using a correlation matrix. Data were checked for outliers through a scatter plot and residual analysis. In the data analysis, Nagelkerke’s pseudo R² was calculated. In the backward stepwise method selection, each variable was automatically removed based on the significance, and the model considered only those variables presenting significant contributions (p<0.05). We also checked the Akaike information criterion (AIC), for which lower values indicated a more adequate fit of the data.

The statistical significance was set at 5% (p<0.05), with a confidence interval of 95%. The SPSS software version 29.0 was used for all analyses.

Results

A total of 80 people with type 2 diabetes mellitus (T2DM) were assessed for eligibility. Thirteen participants were excluded (four due to the presence of an ulcer, five due to amputation of any part of the lower limb, and four participants did not wish to participate). The final sample consisted of 67 participants.

The main participant’s characteristics are presented in Table 1. The overall mean age of was 62.6 ± 8.2 years. Thirty-five participants were female (52.2%), and the mean time since diagnosis was 16.1 ± 7.6 years. The mean glycated haemoglobin (HbA1c) value of the participants was 8.8 ± 1.7%. Fifty participants (78.2%) had HbA1c values above 7%. The mean BMI was 29.1 Kg/m², 29 individuals (43.2%) were classified as overweight (BMI >25 Kg/m²) and 24 (35.8%) were classified as obese (BMI >30 Kg/m²).

Table 1.

Characteristics of the study’s participants.

Gender (N, %)			CI 95%
Female	35	52.2	—
Male	32	47.8	—
Age (mean, SD)
Overall	62.6	8.2	60.6; 64.7
Female	61.6	8.9	58.5; 64.7
Male	63.8	7.4	61.1; 66.5
Self-declared race (N, %)
White	26	38.8	28.4; 50.7
Black	20	29.9	19.4; 40.3
Brown	16	23.9	14.9; 34,3
Asian	3	4.5	0; 9.0
Others	2	3	0; 7.5
Educational level (N, %)
Illiterate	7	10.4	4.5; 19.4
Elementary to middle school	34	50.7	37.4; 62.7
High school	16	23.9	14.9; 35.8
Bachelor’s/graduate degree	10	14.9	6; 23.9
Occupation (N, %)
Employed	17	25.4	16.4; 35.8
Unemployed	10	14.9	7.5; 23.9
Retired	40	59.7	49.3; 71.6
Family income (N, %)
1 to 2x minimum wage	43	64.2	52.2; 74; 6
3 to 4x minimum wage	9	13.4	6; 22.4
>4x minimum wage	15	22.4	11.9; 32.8
Diabetic foot treatment (N, %)
None	58	88.6	—
Medical treatment	3	4.5	—
Surgical treatment	4	6	—
Physical therapy treatment	2	3	—
Gait assistive device (N, %)
Yes	3	4.5	0; 10.4
No	58	86.6	77.6; 94
Adapted shoe	6	9	3; 16.4

SD: standard deviation; CI 95% confidence interval of 95%.

The frequency of twice-daily blood glucose monitoring was somewhat higher in 21 participants (30%), and 63 participants (94%) were taking insulin. Retinopathy was reported by 26 participants (16 with mild and 4 with severe non-proliferative retinopathy, and 6 with proliferative retinopathy). The most common comorbidities found were hypertension (78.1%), followed by dyslipidemia (48.7%), and obesity (n = 10; 15.6%).

The mean score in the MNSI was 4.4 ± 2.5. According to the MNSI, neuropathy was detected in 52 participants (77.6%). According to the NDS, neuropathy was diagnosed in 31 participants (46.2%) for those individuals with >2 points in the final score (mild or moderate neuropathy classification according to the instrument), while 19 (28.3%) neuropathic individuals were identified when considering the monofilament analysis as shown in Table 2.

Table 2.

Classification of participants’ neuropathy according to the instruments used in the study.

Groups by monofilaments	N	%	Groups by NDS	N	%
Without sensitivity loss	29	43.2	Regular	36	53.7
With sensitivity loss	19	28.3	Mild	23	34.3
Neuropathy	19	28.3	Moderate	8	11.9

Monofilament diagnostic method using the Semmes-Weinstein SORRI-Bauru^® aesthesiometer; Neuropathy Disability Score (NDS); % percentage of participants classified using the instrument.

The average utility was 0.660, as presented in Table 3. We found that 11% of the participants reported a state of perfect health, and individuals with neuropathy reported the worst utility values. When stratified by gender, men showed higher utility values than women. Individuals with neuropathy also reported the worst mean scores for both genders. The dimensions mobility and pain/discomfort presented the highest frequency of problems (Table 3).

Table 3.

Data on the utility scores and EQ-5D-3L dimensions of the participants, stratified by sensitivity loss and gender.

	Overall	No sensitivity loss^a	With sensitivity loss^b	Neuropathy^c
Overall
EQ-5D-3L score (mean, SD)	0.66 (0.2)	0.64 (0.2)	0.74 (0.2)	0.62 (0.2)
Gender
Female (N, %)	35 (52.2)	21 (31.3)	7 (10.4)	7 (10.4)
Utility (mean, SD)	0.598 (0.16)	0.619 (0.15)	0.693 (0.09)	0.442 (0.13)
Male (N, %)	32 (47.8)	8 (11.9)	12 (17.9)	12 (17.9)
Utility (mean, SD)	0.739 (0.17)	0.725 (0.14)	0.803 (0.20)	0.684 (0.13)
Dimensions affected (N, %)
Mobility	15 (22.4)	10 (14.9)	5 (7.5)	12 (17.9)
Self-care	9 (13.4)	6 (9)	1 (1.5)	6 (9)
Usual activities	14 (20.9)	11 (16.4)	3 (4.5)	9 (13.4)
Pain/discomfort	15 (22.4)	18 (26.9)	9 (13.4)	11 (16.4)
Anxiety/depression	10 (14.9)	11 (16.4)	8 (11.9)	8 (11.9)

EQ-5D-3L EuroQol five-dimension three levels; SD standard deviation.

^agroup 1.

^bgroup 2.

^cgroup 3; % percentage of reported problem in each dimension.

The regression analysis including the monofilament method is shown in Table 4. We found that 59.4% of participants were correctly classified in this model. Gender was the only significant predictor within the sensory loss category, showing that female subjects were less likely to have sensory loss (OR: 0.15 and OR: 0.11, respectively). Gender and ankle dorsiflexion strength were significant predictors in the neuropathy category. Increases in ankle dorsiflexion strength and female gender were associated with a lower chance of being classified as neuropathic (OR: 0.619 and OR: 0.119, respectively).

Table 4.

Regression model 1 with monofilament diagnosis method.

	OR	B (SE)	95% CI	p-value
With sensitivity loss
Gender
Female	0.155	−1.886 (0.706)	0.039; 0.617	0.008
Male*
Dorsiflexion strength	0.956	−0.045 (0.139)	0.728; 1.255	0.745
Neuropathy
Gender
Female	0.119	−2.132 (0.765)	0.026; 0.531	0.005
Male*
Dorsiflexion strength	0.619	−0.480 (0.167)	0.446; 0.858	0.004
Pseudo R² (Negelkerk): 0.334

OR: odds ratio; SE: standard error; CI: confidence interval; *reference categories.

Data on the regression analysis with the NDS method are presented in Table 5. We found that 65.6% of the cases were classified correctly in this model. Ankle dorsiflexion muscle strength within the moderate classification was the only significant predictor, showing that increases in dorsiflexion strength were associated with a lower chance of being classified as moderate neuropathy (OR: 0.612).

Table 5.

Regression model 2 with neuropathy disability score diagnostic method.

	OR	B (SE)	95% CI	p-value
Mild
Gender
Female	0.315	−1.155 (0.606)	0.96; 1.034	0.057
Male*
Dorsiflexion strength	0.869	−0.140 (0.123)	0.683; 1.107	0.256
HbA1c	0.701	−0.355 (0.199)	0.475; 1.037	0.075
Moderate
Gender
Female	0.202	−1.598 (0.971)	0.30; 1.357	0.100
Male*
Dorsiflexion strength	0.612	−0.491 (0.211)	0.405; 0.926	0.020
HbA1c	1.341	0.293	0.728; 2.468	0.347
Pseudo R² (Negelkerke): 0.262

OR: odds ratio; CI: confidence interval; HbA1c: Glycated haemoglobin; *reference categories.

Discussion

We investigated the association between a set of clinical and functioning variables in individuals with type 2 diabetes in accordance with different sensory classification methods. Participants with neuropathy, especially women, had lower utility scores compared to those with and without sensory loss. We found associations between reduced muscle strength, gender, and impaired sensitivity. Females were less likely to be classified with loss of sensitivity, compared to males. In addition, increased ankle dorsiflexion strength was associated with a lower chance of having neuropathy.

We found a higher frequency of female individuals, who underwent insulin treatment, with a mean age of 61.6 years. Those findings are corroborated by previous studies, in which people without neuropathy were older and presented higher levels of HbA1c.¹⁸ This is relevant, as a risk factor for neuropathy is age >60 years.^19–21 Furthermore, a proportion of the participants (22%) in the present study reported mobility limitations. This is important because with increasing age there is an increase in comorbidities related to muscle mass and mobility loss. For instance, more than 70% of adults with DM have limited mobility, in addition to functional decline and risk of falling.^22,23 In the present study, the most common comorbidities were hypertension, obesity, and dyslipidemia, corroborating a previous study.²⁴ Moreover, the HbA1c profile was higher than 7%, which is recommended for the prevention of long-term vascular complications.²⁵ Glycaemic control, as well as the treatment of modifiable risk factors such as blood pressure and lipid control, may modestly slow the progression of neuropathy.²⁶

We found a lower mean utility score compared with previously reported data in individuals with DM.²⁷ Individuals with neuropathy, especially women, had worse utility values. Currie, Poole²⁸ reported that quality of life in hospitalised individuals with DM presented no significant differences between gender or type of DM. However, the authors reported a deterioration of quality of life as the severity of neuropathy increased. These data show a relevant association between severe symptoms of neuropathy and worsening quality of life in individuals with DM, which corroborates our findings. It is possible to assume that the severity of neuropathy is strongly associated with frailty and mobility limitations linked to muscle mass loss and decreased gait speed.^5,29 The presence of impaired mobility was also reported by IJzerman, Schaper (5) (e.g. impairments in the timed up and go test; six-minute walk test) and was associated with loss in muscle strength and lower quality of life in this population.

We found that women had a lower chance of being classified with loss of sensitivity, compared to men. This finding might be explained by different health seeking behaviours and improved self-care of women compared with men. This is corroborated by a previous study³⁰ investigating the type of health service sought (prevention vs treatment/diagnosis), in which out of 205,529 individuals, 17.54% reported seeking health services mostly for treatment and diagnosis. Another recurring aspect is that health services characteristics are predominantly aimed at the female public, such as structure, organisation, decoration, and communication, which may explain why women are more susceptible to seek preventive services and health promotion.³¹

Our findings showed that for each unit increase in muscle strength, women presented a lower chance of being classified as neuropathic. Hyperglycemia, an early manifestation for the development of DM, is associated with the development of frailty and limited mobility linked to loss of muscle mass.²³ Higher levels of HbA1c, and longer duration of diabetes is also associated with worsening muscle quality and lower quadriceps strength in adults >50 years.³² This is interesting because lower limb muscle weakness related to DM has shown greater impairment in ankle and knee muscles regardless of the presence of neuropathy.^{14,29,33–35} Thus, data on the severity of neuropathy and its influences on dorsiflexors muscles strength are relevant for recommending self-care and prevention strategies by physiotherapists in the population with DM.³⁶

Scarton, Jonkers³⁷ investigated lower limb muscle strength, as well as joint kinetics and kinematics in people with neuropathy. The authors reported a decrease in hip joint mobility with a greater angle of pelvic rotation at the end of the gait cycle, as well as reduced strength in the hip flexor muscles. Individuals with neuropathy also showed reduced ankle flexion/extension range of motion in the support phase, and reduced muscle strength of the muscles involved in ankle plantar flexion, compared to controls. The authors highlighted the function of the posterior tibial muscle in the stabilisation of the ankle and in the support of the medial foot arch. Thus, the decrease in muscle strength could affect gait and balance, contributing to the risk of falling.²² This confirms the clinical relevance of our findings, particularly the relevance of measuring the ankle dorsiflexor strength in this population. This is interesting because people with DM are more likely to have accelerated loss of muscle mass and strength in the lower extremities compared to people without DM.^23,32

One strength of this study was the adoption of a real-world approach by recruiting participants in a clinical rehabilitation setting. Nevertheless, due to restrictions within this setting we were not able to perform a sample size calculation, which might present some limitations regarding statistical power and generalisation to other populations. In addition, because we used a cross-sectional design, we were limited to draw conclusions regarding predictive analysis.

Conclusion

Our results showed that women with diabetes were less likely than men to be classified as having tactile sensitivity loss. Additionally, increased ankle dorsiflexion muscle strength was associated with a lower chance of having neuropathy. The results also showed that participants with neuropathy, especially women, had lower utility scores compared to those with and without sensitivity loss.

Footnotes

Acknowledgements

The authors would like to thank Alexandra Rubim Camara Sete and Eliziane Brandão Leite for allowing the research to be carried out during service hours in the CEDOH (Centro Especializado em Diabetes, Obesidade e Hipertensão). We also would like to thank Silvio César Parente, Luz Marina Alfonso Dutra, and Danyelle Lorrane Carneiro Veloso for their support during the participants’ recruiting.

Ethical approval

The study was granted approval by the Institutional Ethics Committee under protocol 4.974.078 and 5.217.470, and participants gave their signed informed consent.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code (001); UnB/DPI/DPG; and Fundação de Apoio à Pesquisa do Distrito Federal (FAPDF). The funding source was not involved in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; and in the decision to submit the article for publication.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

References

IDF. International Diabetes Federation . IDF diabetes atlas. 10th edn. Brussels, Belgium: International Diabetes Federation, 2021. Available at: https://www.diabetesatlas.org

Scheffel

Bortolanza

Weber

, et al. [Prevalence of micro and macroangiopatic chronic complications and their risk factors in the care of out patients with type 2 diabetes mellitus]. Rev Assoc Med Bras 2004; 50(3): 263–267.

Marathe

Gao

. American diabetes association standards of medical care in diabetes 2017. J Diabetes 2017; 9(4): 320–324.

Souza

Nery

CAS

Marciano

LHSC

, et al. Avaliação da neuropatia periférica: correlação entre a sensibilidade cutânea dos pés, achados clínicos e eletroneuromiográficos. Acta Fisiatr 2005; 12(3): 87–93.

Ijzerman

Schaper

Melai

, et al. Lower extremity muscle strength is reduced in people with type 2 diabetes, with and without polyneuropathy, and is associated with impaired mobility and reduced quality of life. Diabetes Res Clin Pract 2012; 95(3): 345–351.

Bagattini

ÂM

Camey

Miguel

, et al. Electronic version of the EQ-5D quality-of-life questionnaire: adaptation to a Brazilian population sample. Value Health Reg Issues 2018; 17: 88–93.

Andreassen

Jakobsen

Andersen

. Muscle weakness: a progressive late complication in diabetic distal symmetric polyneuropathy. Diabetes 2006; 55(3): 806–812.

Andreassen

Jakobsen

Ringgaard

, et al. Accelerated atrophy of lower leg and foot muscles--a follow-up study of long-term diabetic polyneuropathy using magnetic resonance imaging (MRI). Diabetologia 2009; 52(6): 1182–1191.

Feldman

Stevens

Thomas

, et al. A practical two-step quantitative clinical and electrophysiological assessment for the diagnosis and staging of diabetic neuropathy. Diabetes Care 1994; 17(11): 1281–1289.

10.

Moreira

Castro

Papelbaum

, et al. [Translation into Portuguese and assessment of the reliability of a scale for the diagnosis of diabetic distal polyneuropathy]. Arq Bras Endocrinol Metabol 2005; 49(6): 944–950.

11.

Mayfield

Sugarman

. The use of the Semmes-Weinstein monofilament and other threshold tests for preventing foot ulceration and amputation in persons with diabetes. J Fam Pract 2000; 49(11 Suppl): S17–S29.

12.

Lee

Tsai

Liao

, et al. Reactive balance control in older adults with diabetes. Gait Posture 2018; 61: 67–72.

13.

Mentiplay

Perraton

Bower

, et al. Assessment of lower limb muscle strength and power using hand-held and fixed dynamometry: a reliability and validity study. PLoS One 2015; 10(10): e0140822.

14.

Ferreira

Sartor

Leal

ÂM

, et al. The effect of peripheral neuropathy on lower limb muscle strength in diabetic individuals. Clin Biomech 2017; 43: 67–73.

15.

Clarke

Ni Mhuircheartaigh

Walsh

, et al. Intra-tester and inter-tester reliability of the MicroFET 3 hand-held dynamometer. Physiother Pract Res 2011; 32: 13–18.

16.

Stark

Walker

Phillips

, et al. Hand-held dynamometry correlation with the gold standard isokinetic dynamometry: a systematic review. Pm r 2011; 3(5): 472–479.

17.

Santos

Cintra

Monteiro

, et al. Brazilian valuation of EQ-5D-3L health states: results from a saturation study. Med Decis Mak 2016; 36(2): 253–263.

18.

Adler

Boyko

Ahroni

, et al. Risk factors for diabetic peripheral sensory neuropathy. Results of the Seattle Prospective Diabetic Foot Study. Diabetes Care 1997; 20(7): 1162–1167.

19.

Braffett

Gubitosi-Klug

Albers

, et al. Risk factors for diabetic peripheral neuropathy and cardiovascular autonomic neuropathy in the diabetes control and complications trial/epidemiology of diabetes interventions and complications (DCCT/EDIC) study. Diabetes 2020; 69(5): 1000–1010.

20.

Pop-Busui

Boulton

Feldman

, et al. Diabetic neuropathy: a position statement by the American diabetes association. Diabetes Care 2017; 40(1): 136–154.

21.

Wang

Bakhotmah

, et al. Prevalence and correlates of diabetic peripheral neuropathy in a Saudi Arabic population: a cross-sectional study. PLoS One 2014; 9(9): e106935.

22.

Brown

Handsaker

Bowling

, et al.

Do patients with diabetic neuropathy use a higher proportion of their maximum strength when walking?

J Biomech 2014; 47(15): 3639–3644.

23.

Kalyani

Corriere

Ferrucci

. Age-related and disease-related muscle loss: the effect of diabetes, obesity, and other diseases. Lancet Diabetes Endocrinol 2014; 2(10): 819–829.

24.

Callaghan

Reynolds

Banerjee

, et al. Dietary weight loss in people with severe obesity stabilizes neuropathy and improves symptomatology. Obesity 2021; 29(12): 2108–2118.

25.

Pititto

Dias

Moura

, et al. Metas no tratamento do diabetes. Diretriz Oficial da Sociedade Brasileira de Diabetes. 2023. DOI: 10.29327/557753.2022-3.

26.

ElSayed

Aleppo

Aroda

, et al. 12. Retinopathy, neuropathy, and foot care: standards of care in diabetes-2023. Diabetes Care 2023; 46(Suppl 1): S203–S215.

27.

Wong

ELY

Cheung

AWL

. Measurement of health-related quality of life in patients with diabetes mellitus using EQ-5D-5L in Hong Kong, China. Qual Life Res 2020; 29(7): 1913–1921.

28.

Currie

Poole

Woehl

, et al. The health-related utility and health-related quality of life of hospital-treated subjects with type 1 or type 2 diabetes with particular reference to differing severity of peripheral neuropathy. Diabetologia 2006; 49(10): 2272–2280.

29.

Andersen

Nielsen

Mogensen

, et al. Muscle strength in type 2 diabetes. Diabetes 2004; 53(6): 1543–1548.

30.

Silva

Torres

Peixoto

. [Factors associated with preventive health services search among Brazilian adults: national Health Survey, 2013]. Cien Saude Colet 2020; 25(3): 783–792.

31.

Gutmann

VLR

Santos

Silva

, et al. Reasons that take women and men to seek the basic health units. J Nurs Health 2022; 12(2): 2212220880.

32.

Kalyani

Metter

Egan

, et al. Hyperglycemia predicts persistently lower muscle strength with aging. Diabetes Care 2015; 38(1): 82–90.

33.

Almurdhi

Reeves

Bowling

, et al. Reduced lower-limb muscle strength and volume in patients with type 2 diabetes in relation to neuropathy, intramuscular fat, and vitamin D levels. Diabetes Care 2016; 39(3): 441–447.

34.

Van Eetvelde

BLM

Lapauw

Proot

, et al. The impact of diabetic neuropathy on the distal versus proximal comparison of weakness in lower and upper limb muscles of patients with type 2 diabetes mellitus: a cross-sectional study. J Musculoskelet Neuronal Interact 2021; 21(4): 464–474.

35.

Stouge

Khan

Kristensen

, et al. MRI of skeletal muscles in participants with type 2 diabetes with or without diabetic polyneuropathy. Radiology 2020; 297(3): 608–619.

36.

Błażkiewicz

Sundar

Healy

, et al. Assessment of lower leg muscle force distribution during isometric ankle dorsi and plantar flexion in patients with diabetes: a preliminary study. J Diabetes Complications 2015; 29(2): 282–287.

37.

Scarton

Jonkers

Guiotto

, et al. Comparison of lower limb muscle strength between diabetic neuropathic and healthy subjects using OpenSim. Gait Posture 2017; 58: 194–200.