Comparison of sensitivity and plantar cutaneous temperature of patients with stroke and Diabetes Mellitus: A pilot case-control study

Abstract

BACKGROUND:

Stroke combined with Diabetes Mellitus may cause sensibility and vascular alterations.

OBJECTIVE:

To determine whether sensitivity and plantar cutaneous temperature of clinically controlled patients with stroke and DM are different from those of patients with stroke only.

METHODS:

This is a cross-sectional case-control study. The volunteers were assessed for sensitivity by monofilament esthesiometry in their plantar region, and for temperature by infrared thermal imaging. The data was presented as means and standard deviations and comparisons were conducted with the Mann-Whitney statistical test, with statistical significance set at $p<$ 0.05.

RESULTS:

Five cases and 11 controls were included according to the eligibility and pairing criteria. There were no discrepancies between the plegic and contralateral sides regarding temperature and sensibility of both cases and controls. However, in the control group, there was an observable tendency for different temperatures between the plegic and the contralateral sides, with $p<$ 0.05 in most of the comparisons.

CONCLUSIONS:

There is no evidence that the cases and controls have different plantar sensibility nor different plantar temperature on their plegic and contralateral sides. However, significant temperature discrepancies between both plegic and contralateral sides were observed in the control group.

Keywords

Stroke cutaneous sensitivity body temperature evaluation esthesiometry thermography

1. Introduction

Cutaneous temperature has been investigated in patients with diabetes (DM) [1, 2] and stroke [3]. Regarding the evaluation of the temperature pattern of patients with DM, it is known that infrared thermography may be useful for identifying health related problems. Once this technique can evaluate the blood flow and see whenever an ischemia is ongoing, the blood perfusion may be diminished, especially in the extremities, such as hand and feet [1]. As temperature sensation changes are evident in patients with stroke [3], understanding plantar cutaneous temperature and sensitivity status of patients with stroke and DM combined may be relevant. To the best of our knowledge, both diseases were not addressed simultaneously regarding their cutaneous temperature and sensitivity. Therefore, the objective of this study was to show whether the plantar cutaneous temperature and sensitivity of patients with stroke associated with clinically controlled DM differ from those found in patients with stroke only.

2. Method

This cross-sectional observational study was conducted at the Institute of Physical Medicine and Rehabilitation and was approved by the Ethics Committee.

The case group was composed of patients who had a stroke and DM, were 18 years of age or older, and the time after the stroke ranged from 3 to 36 months. The control group was composed of patients with the same inclusion criteria, except for the presence of DM. Also, the control group was paired with the case group regarding sex, age, body mass index (BMI), time after stroke, and physical rehabilitation time.

Patients were assessed regarding physical function by the Fugl-Meyer Assessment Scale (FMA) [4, 5].

The plantar sensitivity was evaluated by aesthesiometry, a technique in which standardized nylon monofilaments are used to cause a pressure on the skin (Semmes-Weistein Monofilaments, SORRI Bauru – Brazil) [6, 7]. These monofilaments are tested in an ascending fashion, from the smallest to the largest caliber in order to widely classify and to detect minimal changes in sensibility. Both feet were assessed and the analyzed in the following areas: digital surface of the hallux, third and fifth toes, the respective metatarsal regions, as suggested by Ueda and Carpes [6].

The infrared thermography was conducted at the Thermography Lab of the Institute. The image caption conditions was standardized according to the literature [1, 3, 8, 9, 10, 11] and the evaluations were carried out in the morning.

Thermal images were captured by an infrared sensor (FLIR, model T650SC ${}^{\@setsize{\scriptsize}{9.5pt}{\viiipt}{\@viiipt}{\textregistered}}$ ) from anterior and posterior angles, and were analyzed by the software FLIR Tools ${}^{\@setsize{\scriptsize}{9.5pt}{\viiipt}{\@viiipt}\textregistered}$ .

The images comprised the total plantar region of both feet, therefore, the patients were required to stay in supine position with a slight dorsiflexion so that the camera could be placed at a perpendicular angle. Also, the camera was placed at a distance of 1.5 meters, as described by Gatt et al. [12]. The evaluated regions of interest were the calcaneus, the hallux, third and fifth toes, and their respective metatarsal regions.

3. Data analysis

Firstly, variables such as sex, age, BMI, time after stroke, and rehabilitation time were paired between cases and controls. Pairing of sex was carried out by maintaining similar proportions of men and women in both groups. As for age, BMI, time after stroke, and rehabilitation time, the means and 95% confidence interval (CI95%) were analyzed so that the means of the controls would not exceed the CI95% of the cases.

Data regarding temperature and sensitivity were grouped into distal extremity (hallux, third, and fifth toes) and proximal extremity (first, third, and fifth metatarsus), and these groups were analyzed combined and isolated, so that relevant proximal-distal alterations, if any, could be shown in this population. The difference between the plegic and contralateral sides were calculated as contralateral minus (-) plegic.

The $t$ -test was used for checking whether the pairing of the groups was successful, and no statistically significant difference was found between these comparisons.

The descriptive analysis was presented as means and standard deviations, given the sample sizes of cases and controls. Any result was considered statistically significant whenever $p\leqslant$ 0.05. The analysis was conducted by Stata 11 ${}^{\@setsize{\scriptsize}{9.5pt}{\viiipt}{\@viiipt}{\textregistered}}$ statistical package.

4. Results

The cases, which were formed by 5 individuals, were the first group included in this study. Then, from 44 possible control patients, 11 met both the inclusion and the pairing criteria as described in the methods section. The proportion of males and females was not balanced between groups (Table 1).

Table 1
Demographic characteristics

	Cases	Controls
Patients, N	5	11
Female, N (%)	2 (40%)	6 (54.5%)
Age, mean years (SD)	56.4 (4.72)	53.54 (5.48)
BMI, mean (SD)	26.09 (5.29)	26.52 (2.54)
Stroke type, ischemic (%)	3 (60%)	6 (54.5%)
Time after stroke, mean months (SD)	28 (6.20)	28 (4.60)
Rehabilitation time, mean months (SD)	15.6 (11.01)	17.27 (9.05)
Plegic side, right (%)	3 (60%)	6 (54.5%)
Fugl-Meyer for sensibility	12.6 (2.97)	12 (5.06)

Cases, patients with stroke and Diabetes Mellitus associated; Controls, patients with stroke only; SD, standard deviation; BMI, body mass index.

In the statistical inferences, we found that the difference between both sides (contralateral-plegic), either regarding temperature or regarding sensitivity, was not statistically significant, despite the larger absolute diferences between sides observed in the control group, it did not statistically differ from the cases. As for sensitivity, it was not possible to observe differences between both groups (Table 2).

Table 2

Intergroup results of the contralateral-plegic differences

Contralateral-plegic*	Cases	Controls	$p$ -value†
Temperature of toes and metatarsus combined	0.04 (0.68)	0.66 (1.00)	0.395
Temperature of toes	0.12 (0.87)	0.59 (1.16)	0.461
Temperature of metatarsus	$-$ 0.05 (0.68)	0.72 (0.88)	0.126
Sensitivity of toes and metatarsus combined	$-$ 0.90 (1.18)	$-$ 0.89 (0.62)	0.733
Sensitivity of toes	$-$ 1.13 (1.57)	$-$ 0.85 (0.70)	0.864
Sensitivity of metatarsus	$-$ 0.33 (0.94)	$-$ 0.54 (0.75)	0.689

*Means and standard deviations; †, Mann-Whitney unpaired test; Cases, patients with stroke and Diabetes Mellitus associated; Controls, patients with stroke only.

Concerning intragroup analysis, we observed an evident trend of greater balance of temperature and sensitivity between both sides (plegic and contralateral) in the group of cases, given their difference did not reach statistical significance ( $p>$ 0.17), as opposed to the control group. Regarding the controls, however, greater and relevant differences were found between both sides, as the plegic side was on average colder and less sensible, for which p-values were either less then or close to 0.05 in most of the comparisons, as shown in Table 3.

Table 3

Intragroup analysis of the plegic and contralateral sides

	Plegic		Contralateral		$p$ -value $\dagger$
Cases*
Metatarsus and toes temperature combined	26.58	(3.20)	26.62	(3.54)	0.686
Toes temperature only	25.7	(3.27)	25.82	(3.92)	0.774
Metatarsus temperature only	27.46	(3.12)	27.41	(3.17)	0.893
Metatarsus and toes sensitivity combined	3.93	(0.90)	3.03	(0.34)	0.174
Toes sensibility only	4.27	(1.44)	3.13	(0.18)	0.218
Metatarsus sensitivity only	3.6	(0.43)	3.27	(0.64)	0.585
Controls*
Metatarsus and toes temperature combined	25.83	(1.59)	26.48	(1.80)	0.075
Toes temperature only	24.99	(1.40)	25.58	(1.68)	0.328
Metatarsus temperature only	26.66	(1.80)	27.38	(1.97)	0.026
Metatarsus and toes sensitivity combined	3.41	(0.89)	2.51	(0.62)	0.004
Toes sensibility only	3.39	(1.03)	2.54	(0.62)	0.005
Metatarsus sensitivity only	3.42	(0.78)	2.88	(0.70)	0.058

*Means and standard deviations; $\dagger$ , paired Mann-Whitney test; Cases, patients with stroke and Diabetes Mellitus associated; Controls, patients with stroke only.

Finally, the plegic side of cases and controls were compared and this analysis did not evidence significant differences, as shown in Table 4.

Table 4

Intergroup analysis of the plegic side

Plegic side*	Cases	Controls	$p$ -value
Metatarsus and toes temperature combined	26.58 (3.19)	25.83 (1.59)	0.865
Toes temperature only	25.70 (3.27)	24.99 (1.40)	0.955
Metatarsus temperature only	27.46 (3.12)	26.66 (1.80)	0.522
Metatarsus and toes sensitivity combined	3.93 (0.90)	3.41 (0.89)	0.249
Toes sensitivity only	4.27 (1.44)	3.39 (1.03)	0.185
Metatarsus sensitivity only	3.60 (0.43)	3.42 (0.78)	0.386

*Means and standard deviations; Cases, patients with stroke and Diabetes Mellitus associated; Controls, patients with stroke only.

5. Discussion

This study sought to understand relevant matters of two important associated diseases: stroke and Diabetes Mellitus (DM), given the crucial need they impose towards healthcare and the disability they may cause, not only to the patient but to families and society as a whole. Also, DM is known to be a modifiable risk factor for stroke, therefore the combination of both diseases must be investigated, so other disorders involving sensitivity loss and vascular alterations arising from these diseases are closely monitored and controlled [13, 14].

A matter that deserves attention is that, even though no statistically significant differences in temperature and sensitivity were found between both groups, the group of cases had lower calcaneal sensitivity and higher cutaneous temperature. This greater temperature difference was about 0.71 ${}^{\circ}$ C between the analyzed surfaces. However, when the symmetry of both sides of each group was compared, it was evidenced that the cases had greater symmetry.

Regarding temperature, an expected result was the different temperature of both lower limb sides, the plegic and the contralateral, of the control group. This statistically significant difference of metatarsal region shows that patients with stroke tend to have a colder plegic side [3]. The cutaneous sensitivity of these patients was also different, what shows that their tactile accuracy is diminished.

Despite the limitations of the study design and low statistical power (22% for the current sample size) it is believed that the use of thermography in patients with DM associated with stroke should be part of the routine, as indicated by this pilot study. Such an evaluation, which has proven to be an easy access method due to portability and cost-effectiveness, can aid the monitoring of various clinical cases [11].

6. Conclusion

In the sample of patients evaluated, there is no evidence that patients with stroke and Diabetes Mellitus (DM) combined have different sensitivity or cutaneous temperature of the lower limb extremities, either in the plegic or in the contralateral side, when compared to patients with stroke only. Nonetheless, it was possible to observe significant differences in temperature between plegic and contralateral sides of the lower limbs extremities of patients with stroke.

Footnotes

Conflict of interest

The authors declare that there is no conflict of interest regarding the publication of this paper.

References

Ring

. Thermal imaging today and its relevance to diabetes. J Diabetes Sci Technol. 2010 Jul 1; 4(4): 857-62.

Balbinot

Robinson

Achaval

Zaro

Brioschi

. Repeatability of infrared plantar thermography in diabetes patients: a pilot study. J Diabetes Sci Technol 2013; 7(5): 1130-7.

Alfieri

Massaro

Filippo

Portes

Battistella

. Evaluation of body temperature in individuals with stroke. NeuroRehabilitation. 2017; 40(1): 119-128.

Michaelsen

Rocha

Knabben

Rodrigues

Fernandes

CGC

. Translation, adaptation and inter-rater reliability of the administration manual of Fugl-Meyer assessment/Tradução, adaptação e confiabilidade interexaminadores do manual de administração da escala de Fugl-Meyer. Rev Bras Fisioter. 2011; 15(1): 80-8.

Maki

Quagliato

EMAB

Cacho

EWA

Paz

LPS

Nascimento

Inoue

MMEA

, et al. Estudo de confiabilidade da aplicação da escala de Fugl-Meyer no Brasil. Rev Bras Fisioter. 2006; 10(2): 177-83.

Ueda

Campos

. Relação entre sensibilidade plantar e controle postural em jovens e idosos. Rev Bras Cineantropom Desempenho Hum. 2013; 15(2): 215-224.

Patel

Magnusson

Kristinsdottir

Fransson

. The contribution of mechanoreceptive sensation on stability and adaptation in the young and elderly. Eur J Appl Physiol. 2009 Jan; 105(2): 167-73.

Zaproudina

Varmavuo

Airaksinen

Närhi

. Reproducibility of infrared thermography measurements in healthy individuals. Physiol Meas 2008; 29: R33-46.

Marins

Fernandes

Cano

Moreira

da Silva

Costa

et al. Thermal body patterns for healthy Brazilian adults (male and female). J Therm Biol. 2014; 42: 1-8.

10.

Fernández-Cuevas

Bouzas Marins

Arnáiz Lastras

Gómez Carmona

Piñonosa Cano

García-Concepción

MÁ

Sillero-Quintana

. Classification of factors influencing the use of infrared thermography in humans: A review. Infrared Physics & Technology. 2015; 71: 28-55.

11.

Alfieri

Battistella

. Body temperature of healthy men evaluated by thermography: A study of reproducibility. Technol Health Care. 2018; 26(3): 559-564.

12.

Gatt

Formosa

Cassar

Camilleri

De Raffaele

Mizzi

Azzopardi

Mizzi

Falzon

Cristina

Chockalingam

. Thermographic patterns of the upper and lower limbs: baseline data. Int J Vasc Med. 2015; 2015: 831369.

13.

Renero-C

. The thermoregulation of healthy individuals, overweight-obese, and diabetic from the plantar skin thermogram: a clue to predict the diabetic foot. Diabet Foot Ankle. 2017; 8(1): 1361298.

14.

Chen

Ovbiagele

Feng

. Diabetes and Stroke: Epidemiology, Pathophysiology, Pharmaceuticals and Outcomes. Am J Med Sci. 2016 Apr; 351(4): 380-6.