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The effect of neuromuscular electrical stimulation on skin temperature in individuals with spinal cord injury: A prospective noncontrolled intervention study

The effect of neuromuscular electrical stimulation on skin temperature in individuals with spinal... DE GRUYTER Current Directions in Biomedical Engineering 2022;8(3): 13-16 Janaina Tancredo*, Rafael Tambascia, Karla Pithon, Alberto Cliquet Junior The effect of neuromuscular electrical stimulation on skin temperature in individuals with spinal cord injury: A prospective non- controlled intervention study Neuromuscular electrical stimulation on skin temperature https://doi.org/10.1515/cdbme-2022-2004 1 Introduction Abstract: The research on the effect of neuromuscular electrical stimulation (NMES) protocol on skin temperature Spinal cord injury (SCI) causes many changes reflected in (Tsk) in individuals with spinal cord injury (SCI) is a motor, sensory, and autonomic nervous system damage [1]. prospective non-controlled intervention study. 47 individuals Regarding the autonomic nervous system, thermoregulation with SCI were recruited from the outpatient clinic. NMES was dysfunction occurs in lesions above sympathetic flow (T4–T6) applied to the tibial anterior (TA) muscles. Four assessments by interruption of neural transmission of thermoregulatory were performed: baseline, shortly after the end of NMES information, in which the hypothalamus is unable to control session (t0), 10 min after the end of NMES (t10) and 20 min cutaneous blood flow [2,3]. after the end of NMES (t20). The intensity used was 1.5 mA Skin temperature (Tsk) is different from the internal RMS (root mean square) depending on the individuals. The temperature, and exhibits variations according to ambient variables were Tsk at forehead, dermatome C2 and L5 temperature. Compared with central core temperature, Tsk is bilaterally. The dermatome C2 and forehead were measured lower [4]. It is influenced by blood flow to the skin and the only at baseline and t20. The measurement device was a non- microcirculation. In addition, there are variations in contact infrared thermometer. Results of this study temperature in relation to the anatomy, such as tendon regions, demonstrated that after NMES the stimulated dermatome (L5), ligaments, muscles, and bone [5,6]. Due to limb inactivity or showed an increase in local Tsk. In addition, the t20 showed paralysis, individuals with SCI exhibit vascular changes, such that the Tsk did not drop to the baseline, being still significant as decreases in the diameter of the arterial duct, decreased in the analyzed group. The implications for rehabilitation capillarization, and deficient microcirculation [7-10]. practice and the positive effects of NMES are fundamental to Studies have shown that neuromuscular electrical improvement of the blood microcirculation and local stimulation (NMES) of paralyzed muscles in individuals with metabolism. SCI can provide several benefits, such as histochemical changes, activation of paralyzed neuromuscular units, Keywords: Neuromuscular Electrical Stimulation, Skin improved muscle hypertrophy and fatigue resistance, Temperature, Spinal Cord Injury. increased local blood flow, facilitated venous return and reduced spasticity [8,9,11-13]. We hypothesized that NMES will induce an increase in local blood flow and, in turn, Tsk. An increase in Tsk, even for a short time, improves the condition of the tissue, muscle fiber(s), and cold sensation in the lower limbs reported by ______ many patients. With the application of NMES, the blood *Corresponding author: Janaina Tancredo: State University of circulation of the skin increases and consequently the Tsk, Campinas, Tessália Vieira de Camargo, 126, Campinas, Brazil, e- mail: rolandtancredo@gmail.com providing beneficial effects for tissue cells and muscle fibers. Rafael Tambascia: State University of Campinas, Campinas, The literature is comprehensive and reports that the use of Brazil Karla Pithon: State University of Bahia Southwest, Jequie, Brazil NMES in SCI has several beneficial effects in the short and Alberto Cliquet Junior: State University of Campinas, Campinas, long term, but with regard to Tsk, there are still not many Brazil Open Access. © 2022 The Author(s), published by De Gruyter. This work is licensed under the Creative Commons Attribution 4.0 International License. 13 studies evaluating precisely how it behaves with NMES. Therefore, the aim of the present study was to observe the effect of NMES protocol on Tsk in SCI patients, which could possibly be a new tool for assessing autonomic dysfunction. The Results reported here support the benefit that NMES protocol applied to the TA muscles for individuals with SCI, as a therapeutic intervention and assessment of autonomic dysfunction induced an increase in local blood flow, leading Figure 1: Neuromuscular Electrical Stimulation in TA muscle to consequent increases in Tsk and local metabolism. The dependent variables measured included forehead, dermatome C2 and L5 bilaterally (see Figure 2). 2 Methods A convenience sample of 47 individuals with SCI was recruited. All volunteers presented a good response to NMES, verified by ankle dorsiflexion yielded by the stimulation, always absent in both tetraplegic and paraplegic of our sample. The level of lesions ranged from C4 to T10. Data were collected in the Spinal Cord Injury Rehabilitation Outpatients Clinic of the University Hospital, in a climatized room by only one researcher. Individuals with fever, sun exposure before the test, engaged in strenuous activity, smokers, caffeine < 1 h before the test, autonomic dysreflexia during the test, active urinary tract infection, inflammation or skin lesions were excluded. To evaluate Tsk, an infrared thermometer (IRT; TG-165, FLIR Systems Inc., Orlando, FL, USA) was used. The IRT, featuring a FLIR Lepton® micro-thermal sensor. Figure 2: The dependent variables measured: forehead, dermatome C2 and L5 bilaterally. Measurement accuracy of the IRT is ±1.5°C, with a measuring range of -25°C to 380°C. This device has been approved by The dermatome C2 and forehead were measured only at the United States Food and Drug Administration, and is baseline and t20. furnished with the appropriate certification document (6, Four steps of measurements were used to collect data from 14,15). The emissivity of the apparatus was adjusted to the the dependent variables. The “outcome measures section”: skin (0.98). Baseline 1: initial data collection. Room temperature and humidity were controlled using a t0: collection of data shortly after the end of NMES. thermo-hygrometer device (MT-240, Minipa Electronics Inc., t10: collection of data 10 min after the end of NMES. Houston, TX, USA). It has an internal sensor (range 0°C to t20: collection of data 20 min after the end of NMES. +60°C) with a basic accuracy of ± 5%. The temperature was The NMES protocol for the TA muscle was performed for 23.7 ± 0.25 ⸰C (mean ± SD) and Internal humidity was 62.7 ± 20 min. In the exercise mode, stimulation is ON for 4 seconds 6.7%. and OFF for 8 seconds, duty cicle of 33%. Dorsiflexion comes For the application of the NMES protocols, a 2-channel on every 4seconds. electrical stimulator was used at a frequency of 25 Hz, with single-phase rectangular pulses with a duration of 300 μs, and an amplitude ranging from 70–150 V (1 kΩ load), up to 1.5 3 Statistical analysis mA RMS (root mean square), depending on the individuals. The self-adhesive NMES surface electrodes (Valutrode, The variables analyzed included Tsk at the forehead and Axelgaard Manufacturing Co. Ltd., Fallbrook, CA, USA). For dermatomes C2 and L5. Each variable is expressed as mean, NMES to the tibial anterior (TA) muscle, a self-adhesive SD, median and corresponding 95% confidence interval (CI). electrode, measuring 5 cm × 9 cm, was applied to the distal Both paraplegic and tetraplegic individuals presented a good thigh (QD), and a smaller 3.0 cm diameter circular electrode response to NMES, verified by performing ankle dorsiflexion. was used near the head of the fibula (see Figure 1). The normality test of Shapiro-Wilk was done. The Friedman test was used for all analyses. The level of significance adopted in all analyses was 5% (i.e., p ≤ 0.05). 14 4 Results SCI characteristics of the individuals recruited in the research (table 1). The confidence intervals of the mean Tsk difference to forehead and dermatome C2 were presented in table 2. The dermatome C2 and forehead were measured only at baseline Figure 3: Images obtained by the Infrared thermometer FLIR-TG and t20. 165 of the Tsk of the L5 dermatome before and after the NMES protocol. Table 1: SCI characteristics. ___________________________________________________ 5 Discussion Variables Mean ± SD ___________________________________________________ Age, yrs 38.89 ± 9.35 The thermoregulatory control reflex causes changes in Time of injury, yrs 11.94 ± 6.45 Body Mass Index, kg/m 23.37 ± 3.49 microcirculation, which may be localized, and/or temperatures ____________________________________________________ throughout the body [16]. Individuals with SCI exhibit microvascular endothelial dysfunction as compromised Table 2: Confidence interval (95%) of the mean Tsk differences cutaneous blood flow [17]. before (baseline) and after the end of NMES (t20) for forehead and dermatome C2 bilaterally and median. The infrared thermometry used in the present study is a ____________________________________________________ technology that detects radiation emitted by a hot surface, and Side Median Confidence interval provides an estimate of the measured surface temperature [7]. ____________________________________________________ It allows many benefits to individuals including hygiene, rapid Forehead - 34.3 0.2 ; 0.54 C2 Right 33.73 0.27 ; 0.66 measurement, non-invasiveness, and comfort. C2 Left 34.13 0.41 ; 0.81 Results of this study have shown no actual changes in the ____________________________________________________ forehead and dermatome C2 Tsk. In contrast, in the stimulated dermatome, an increase in local Tsk occurred. This may have Table 3 shows Tsk for baseline, t0, t10 and t20. In the occurred due to increased blood perfusion at the stimulation NMES of the TA muscle, a greater increase was observed in Tsk (p<0.05). The highest temperature variation found site, therefore, demonstrating a global metabolic effect due to the deficit in thermoregulation after SCI. In the literature, individually, after NMES, in the sample of recruited individuals was 6.1ºC. some studies show the benefits of applying the NMES, as well as in Abram SE. (1980), who evaluated the relationship Table 3: Confidence interval of the mean Tsk differences before between Tsk and the use of transcutaneous electrical and after NMES protocol in TA muscle in dermatome L5. Data are stimulation in patients with pain. He only observed an increase reported as mean of differences in Tsk before and after NMES in Tsk in individuals who had pain relief. protocol. (95% CI) *p <0.05. Abbreviation: t0, Time soon after the end of the NMES; t10, Time of 10 minutes after the end of the The difference in Tsk after NMES is due to the heat NMES; t20, Time of 20 minutes after the end of the NMES. emitted by the joule effect and muscle contraction. Thus, high- ____________________________________________________ frequency broad-pulse NMES interacts with more organized Dermatome Protocol Median Confidence interval ____________________________________________________ neuronal groups resulting in better muscle contraction L5 Right Baseline 29.83 0.01 ; 0.4* response, higher temperature and, consequently, lower L5 Right t0 33.03 -3.35 ; -2.52* L5 Right t10 32.93 -3.11 ; -2.3* metabolic demand. L5 Right t20 32.05 -2.7 ; -1.81* Tissue damage occurs at temperatures above 44°C, at 51°C L5 Left Baseline 29.96 0.3 ; 0.57* it will cause almost immediate destruction of the epidermis L5 Left t0 33.03 -3.04 ; -2.23* L5 Left t10 32.83 -2.94 ; -2.08* [19]. In our study, the highest temperature value found after L5 Left t20 32.4 -2.42 ; -1.55* NMES was 34.2 ºC. ____________________________________________________ In peripheral regions SCI individuals often have a lower temperature. When the cutaneous circulation when deficient, After NMES, an increase in Tsk was observed in results in a lower perfusion of the skin and consequently a stimulated L5 dermatomes and, considering t20, a Tsk was still decrease in the regional temperature due to vasoconstriction higher than the baseline value. [20,21]. Therefore, it was chosen to perform the NMES in the Figure 3 shows the temperature and color change related L5 dermatome, which is an extremity region. to the increase in Tsk in the L5 dermatome. The inability of the voluntary contraction caused by SCI reduces the efficiency of the venous pump, located in the calf region [22]. Therefore, considering the results of our study, that due to the inefficiency of the venous pump, the Tsk in the 15 [6] Maniar N, Bach AJE, Stewart IB, Costello JT. The effects of TA muscle at t10 and t20, was still higher after the protocol. using different regions of interest on local and mean skin This research main limitation is that the accuracy of the temperature. Journal of Thermal Biology 2015; 49-50, 33-38. infrared thermometer is estimated in ±1.5°C. To minimized [7] Tang YL; He Y, Shao HW, Mizera I. Skin temperature oscillation model for assessing vasomotion of microcirculation. the error, the protocol was realized in a climatized room, with Acta Mechanica Sinica 2015; 31 (1): 132-138. the room temperature controlled, the data collection was done [8] Bochkezanian V, Newton RU, Trajano GS, Blazevich AJ. in the same day, by the same researcher and the main results Effects of Neuromuscular Electrical Stimulation in People with Spinal Cord Injury. Medicine & Science in Sports & Exercise were the comparation of the individuals with themselves. Results of the current study demonstrated that NMES [9] Carvalho DC, Martins CL, Cardoso SD, Cliquet A. protocol applied to the TA muscles altered Tsk in individuals Improvement of metabolic and cardiorespiratory responses through treadmill gait training with neuromuscular electrical with SCI. We observed a significant increase in Tsk in the stimulation in quadriplegic subjects. Artificial Organs 2006; muscle, which corroborates the hypothesis NMES induces an 30:56– 63. [10] Van Duijnhoven NT, Janssen TW, Green DJ, Minson CT, increase in local blood flow, leading to consequent increases Hopman MT, Thijssen DH. Effect of functional in Tsk and local metabolism, as demonstrated and electrostimulation on impaired skin vasodilator responses to hypothesized in our study. And according to the literature, local heating in spinal cord injury. J Appl Physiol (1985) 2009;106(4):1065-71. every 0.6ºC increase in temperature causes a 10% increase in [11] Bittar CK and Cliquet A. Effects of quadriceps and anterior metabolism [23]. tibial muscles electrical stimulation on the feet and ankles of As the Tsk in the L5 dermatome increased, future studies patients participants with spinal cord injuries. Spinal Cord 2010; 48, 881–885. would be interesting evaluating the complete or incomplete [12] Tancredo JR, Maria RM, Azevedo ERF, Alonso KC, Varoto SCI, by measuring the sensation of increased temperature in R, Cliquet A. Clinical assessment of spasticity in individuals the stimulated dermatome. with spinal cord injury. Acta Ortop Bras [online] 2013; 21(6):310-4. [13] Gorgey AS, Dolbow DR, Dolbow JD, Khalil RK, Gater DR. The effects of electrical stimulation on body composition and Author Statement metabolic profile after spinal cord injury – Part II. The Journal Research funding: The authors thank the CNPq -National of Spinal Cord Medicine 2015, 38 (1): 23-37. Council for Science and Technological Development # [14] Alexander J, Richards J, Attah O, Cheema S, Snook J, 140215 / 2014-0. Wisdell C, May Selfe, J. Delayed effects of a 20-min crushed ice application on knee joint position sense assessed by a Conflict of interest: Authors state no conflict of interest. functional task during a re-warming period. Gait & Posture Informed consent: Informed consent has been obtained from 2018; 62, 173–178. [15] Rossignoli I, Fernández-Cuevas I, Benito PJ, Herrero AJ. all individuals included in this study. Ethical approval: The Relationship between shoulder pain and skin temperature research related to human use complies with all the relevant measured by infrared thermography in a wheelchair national regulations, institutional policies and was performed propulsion test. Infrared Physics & Technology 2016:76251– in accordance with the tenets of the Helsinki Declaration, and [16] Johnson JM, Kellogg DL, Jr. Local thermal control of the has been approved by the authors’ institutional review board human cutaneous circulation. J Appl Physiol 1985; or equivalent committee. 2010;109(4):1229-38. [17] Byrne DW, Salzberg CA. Major risk factors for pressure ulcers in the spinal cord disabled: a literature review. Spinal cord References 1996;34(5):255-63. [18] Abram SE, Asiddao CB, and Reynolds AC, Increased Skin Temperature during Transcutaneous Electrical Stimulation. [1] Hamid R, Averbeck MA, Chiang H, Garcia A, Al Mousa RT, Anesthesia and Analgesia. 1980; 59: 5922-25. Oh SJ et al. Epidemiology and pathophysiology of neurogenic [19] B.B. Ong, Injury, Fatal and Nonfatal | Burns and bladder after spinal cord injury. World Journal of Urology Scalds,Editor(s): Jason Payne-James,Encyclopedia of Forensic and Legal Medicine,Elsevier,2005,Pages 90-98 [2] Griggs K.E.; Leicht C.A.; Price M.J.; Goosey-Tolfrey V.L.; [20] Lima A. Bakker J. Noninvasive monitoring of peripheral Thermoregulation during intermittent exercise in athletes with perfusion. Intensive care Med. 2005; 31: 1316-26. a spinal cord injury. International Journal of Sports Physiology [21] Tancredo JR, Tambascia RA, Borges M, Fukuchi CA, Cliquet and Performance 2015; 10(4), pp.469-475. Junior A. Development of a skin temperature map for [3] McAllen, R. M., & McKinley, M. J. (2018). Efferent dermatomes in individuals with spinal cord injury: a cross- thermoregulatory pathways regulating cutaneous blood flow sectional study. Spinal Cord. 2020 Oct;58(10):1090-1095. and sweating. Thermoregulation: From Basic Neuroscience to Epub 2020 May 5. Clinical Neurology Part I, 305–316. [22] Song YG, Won YH, Park SH, Ko MH, Seo JH. Changes in [4] Khan S, Plummer M, Martinez-Arizala A, Banovac K. Body Temperature in Incomplete Spinal Cord Injury by Digital Hypothermia in patients participants with chronic spinal Cord Infrared Thermographic Imaging. Annals of Rehabilitation injury. The Journal of Spinal Cord Medicine 2007; 30 (1): 27- Medicine 2015;39(5):696-704. [23] Beutler B, Beutler SM. The pathogenesis of fever. In: [5] van Marken Lichtenbelt WD, Westerterp-Plantenga MS, van Goldman, Bennett and all, editors. Cecil textbook of medicine. Hoydonck P. Individual variation in the relation between body W.B. Saunders Company, 21st edition: 1565-1567. temperature and energy expenditure in response to elevated ambient temperature. Physiology & Behavior 2001; 73. 235- http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Current Directions in Biomedical Engineering de Gruyter

The effect of neuromuscular electrical stimulation on skin temperature in individuals with spinal cord injury: A prospective noncontrolled intervention study

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DE GRUYTER Current Directions in Biomedical Engineering 2022;8(3): 13-16 Janaina Tancredo*, Rafael Tambascia, Karla Pithon, Alberto Cliquet Junior The effect of neuromuscular electrical stimulation on skin temperature in individuals with spinal cord injury: A prospective non- controlled intervention study Neuromuscular electrical stimulation on skin temperature https://doi.org/10.1515/cdbme-2022-2004 1 Introduction Abstract: The research on the effect of neuromuscular electrical stimulation (NMES) protocol on skin temperature Spinal cord injury (SCI) causes many changes reflected in (Tsk) in individuals with spinal cord injury (SCI) is a motor, sensory, and autonomic nervous system damage [1]. prospective non-controlled intervention study. 47 individuals Regarding the autonomic nervous system, thermoregulation with SCI were recruited from the outpatient clinic. NMES was dysfunction occurs in lesions above sympathetic flow (T4–T6) applied to the tibial anterior (TA) muscles. Four assessments by interruption of neural transmission of thermoregulatory were performed: baseline, shortly after the end of NMES information, in which the hypothalamus is unable to control session (t0), 10 min after the end of NMES (t10) and 20 min cutaneous blood flow [2,3]. after the end of NMES (t20). The intensity used was 1.5 mA Skin temperature (Tsk) is different from the internal RMS (root mean square) depending on the individuals. The temperature, and exhibits variations according to ambient variables were Tsk at forehead, dermatome C2 and L5 temperature. Compared with central core temperature, Tsk is bilaterally. The dermatome C2 and forehead were measured lower [4]. It is influenced by blood flow to the skin and the only at baseline and t20. The measurement device was a non- microcirculation. In addition, there are variations in contact infrared thermometer. Results of this study temperature in relation to the anatomy, such as tendon regions, demonstrated that after NMES the stimulated dermatome (L5), ligaments, muscles, and bone [5,6]. Due to limb inactivity or showed an increase in local Tsk. In addition, the t20 showed paralysis, individuals with SCI exhibit vascular changes, such that the Tsk did not drop to the baseline, being still significant as decreases in the diameter of the arterial duct, decreased in the analyzed group. The implications for rehabilitation capillarization, and deficient microcirculation [7-10]. practice and the positive effects of NMES are fundamental to Studies have shown that neuromuscular electrical improvement of the blood microcirculation and local stimulation (NMES) of paralyzed muscles in individuals with metabolism. SCI can provide several benefits, such as histochemical changes, activation of paralyzed neuromuscular units, Keywords: Neuromuscular Electrical Stimulation, Skin improved muscle hypertrophy and fatigue resistance, Temperature, Spinal Cord Injury. increased local blood flow, facilitated venous return and reduced spasticity [8,9,11-13]. We hypothesized that NMES will induce an increase in local blood flow and, in turn, Tsk. An increase in Tsk, even for a short time, improves the condition of the tissue, muscle fiber(s), and cold sensation in the lower limbs reported by ______ many patients. With the application of NMES, the blood *Corresponding author: Janaina Tancredo: State University of circulation of the skin increases and consequently the Tsk, Campinas, Tessália Vieira de Camargo, 126, Campinas, Brazil, e- mail: rolandtancredo@gmail.com providing beneficial effects for tissue cells and muscle fibers. Rafael Tambascia: State University of Campinas, Campinas, The literature is comprehensive and reports that the use of Brazil Karla Pithon: State University of Bahia Southwest, Jequie, Brazil NMES in SCI has several beneficial effects in the short and Alberto Cliquet Junior: State University of Campinas, Campinas, long term, but with regard to Tsk, there are still not many Brazil Open Access. © 2022 The Author(s), published by De Gruyter. This work is licensed under the Creative Commons Attribution 4.0 International License. 13 studies evaluating precisely how it behaves with NMES. Therefore, the aim of the present study was to observe the effect of NMES protocol on Tsk in SCI patients, which could possibly be a new tool for assessing autonomic dysfunction. The Results reported here support the benefit that NMES protocol applied to the TA muscles for individuals with SCI, as a therapeutic intervention and assessment of autonomic dysfunction induced an increase in local blood flow, leading Figure 1: Neuromuscular Electrical Stimulation in TA muscle to consequent increases in Tsk and local metabolism. The dependent variables measured included forehead, dermatome C2 and L5 bilaterally (see Figure 2). 2 Methods A convenience sample of 47 individuals with SCI was recruited. All volunteers presented a good response to NMES, verified by ankle dorsiflexion yielded by the stimulation, always absent in both tetraplegic and paraplegic of our sample. The level of lesions ranged from C4 to T10. Data were collected in the Spinal Cord Injury Rehabilitation Outpatients Clinic of the University Hospital, in a climatized room by only one researcher. Individuals with fever, sun exposure before the test, engaged in strenuous activity, smokers, caffeine < 1 h before the test, autonomic dysreflexia during the test, active urinary tract infection, inflammation or skin lesions were excluded. To evaluate Tsk, an infrared thermometer (IRT; TG-165, FLIR Systems Inc., Orlando, FL, USA) was used. The IRT, featuring a FLIR Lepton® micro-thermal sensor. Figure 2: The dependent variables measured: forehead, dermatome C2 and L5 bilaterally. Measurement accuracy of the IRT is ±1.5°C, with a measuring range of -25°C to 380°C. This device has been approved by The dermatome C2 and forehead were measured only at the United States Food and Drug Administration, and is baseline and t20. furnished with the appropriate certification document (6, Four steps of measurements were used to collect data from 14,15). The emissivity of the apparatus was adjusted to the the dependent variables. The “outcome measures section”: skin (0.98). Baseline 1: initial data collection. Room temperature and humidity were controlled using a t0: collection of data shortly after the end of NMES. thermo-hygrometer device (MT-240, Minipa Electronics Inc., t10: collection of data 10 min after the end of NMES. Houston, TX, USA). It has an internal sensor (range 0°C to t20: collection of data 20 min after the end of NMES. +60°C) with a basic accuracy of ± 5%. The temperature was The NMES protocol for the TA muscle was performed for 23.7 ± 0.25 ⸰C (mean ± SD) and Internal humidity was 62.7 ± 20 min. In the exercise mode, stimulation is ON for 4 seconds 6.7%. and OFF for 8 seconds, duty cicle of 33%. Dorsiflexion comes For the application of the NMES protocols, a 2-channel on every 4seconds. electrical stimulator was used at a frequency of 25 Hz, with single-phase rectangular pulses with a duration of 300 μs, and an amplitude ranging from 70–150 V (1 kΩ load), up to 1.5 3 Statistical analysis mA RMS (root mean square), depending on the individuals. The self-adhesive NMES surface electrodes (Valutrode, The variables analyzed included Tsk at the forehead and Axelgaard Manufacturing Co. Ltd., Fallbrook, CA, USA). For dermatomes C2 and L5. Each variable is expressed as mean, NMES to the tibial anterior (TA) muscle, a self-adhesive SD, median and corresponding 95% confidence interval (CI). electrode, measuring 5 cm × 9 cm, was applied to the distal Both paraplegic and tetraplegic individuals presented a good thigh (QD), and a smaller 3.0 cm diameter circular electrode response to NMES, verified by performing ankle dorsiflexion. was used near the head of the fibula (see Figure 1). The normality test of Shapiro-Wilk was done. The Friedman test was used for all analyses. The level of significance adopted in all analyses was 5% (i.e., p ≤ 0.05). 14 4 Results SCI characteristics of the individuals recruited in the research (table 1). The confidence intervals of the mean Tsk difference to forehead and dermatome C2 were presented in table 2. The dermatome C2 and forehead were measured only at baseline Figure 3: Images obtained by the Infrared thermometer FLIR-TG and t20. 165 of the Tsk of the L5 dermatome before and after the NMES protocol. Table 1: SCI characteristics. ___________________________________________________ 5 Discussion Variables Mean ± SD ___________________________________________________ Age, yrs 38.89 ± 9.35 The thermoregulatory control reflex causes changes in Time of injury, yrs 11.94 ± 6.45 Body Mass Index, kg/m 23.37 ± 3.49 microcirculation, which may be localized, and/or temperatures ____________________________________________________ throughout the body [16]. Individuals with SCI exhibit microvascular endothelial dysfunction as compromised Table 2: Confidence interval (95%) of the mean Tsk differences cutaneous blood flow [17]. before (baseline) and after the end of NMES (t20) for forehead and dermatome C2 bilaterally and median. The infrared thermometry used in the present study is a ____________________________________________________ technology that detects radiation emitted by a hot surface, and Side Median Confidence interval provides an estimate of the measured surface temperature [7]. ____________________________________________________ It allows many benefits to individuals including hygiene, rapid Forehead - 34.3 0.2 ; 0.54 C2 Right 33.73 0.27 ; 0.66 measurement, non-invasiveness, and comfort. C2 Left 34.13 0.41 ; 0.81 Results of this study have shown no actual changes in the ____________________________________________________ forehead and dermatome C2 Tsk. In contrast, in the stimulated dermatome, an increase in local Tsk occurred. This may have Table 3 shows Tsk for baseline, t0, t10 and t20. In the occurred due to increased blood perfusion at the stimulation NMES of the TA muscle, a greater increase was observed in Tsk (p<0.05). The highest temperature variation found site, therefore, demonstrating a global metabolic effect due to the deficit in thermoregulation after SCI. In the literature, individually, after NMES, in the sample of recruited individuals was 6.1ºC. some studies show the benefits of applying the NMES, as well as in Abram SE. (1980), who evaluated the relationship Table 3: Confidence interval of the mean Tsk differences before between Tsk and the use of transcutaneous electrical and after NMES protocol in TA muscle in dermatome L5. Data are stimulation in patients with pain. He only observed an increase reported as mean of differences in Tsk before and after NMES in Tsk in individuals who had pain relief. protocol. (95% CI) *p <0.05. Abbreviation: t0, Time soon after the end of the NMES; t10, Time of 10 minutes after the end of the The difference in Tsk after NMES is due to the heat NMES; t20, Time of 20 minutes after the end of the NMES. emitted by the joule effect and muscle contraction. Thus, high- ____________________________________________________ frequency broad-pulse NMES interacts with more organized Dermatome Protocol Median Confidence interval ____________________________________________________ neuronal groups resulting in better muscle contraction L5 Right Baseline 29.83 0.01 ; 0.4* response, higher temperature and, consequently, lower L5 Right t0 33.03 -3.35 ; -2.52* L5 Right t10 32.93 -3.11 ; -2.3* metabolic demand. L5 Right t20 32.05 -2.7 ; -1.81* Tissue damage occurs at temperatures above 44°C, at 51°C L5 Left Baseline 29.96 0.3 ; 0.57* it will cause almost immediate destruction of the epidermis L5 Left t0 33.03 -3.04 ; -2.23* L5 Left t10 32.83 -2.94 ; -2.08* [19]. In our study, the highest temperature value found after L5 Left t20 32.4 -2.42 ; -1.55* NMES was 34.2 ºC. ____________________________________________________ In peripheral regions SCI individuals often have a lower temperature. When the cutaneous circulation when deficient, After NMES, an increase in Tsk was observed in results in a lower perfusion of the skin and consequently a stimulated L5 dermatomes and, considering t20, a Tsk was still decrease in the regional temperature due to vasoconstriction higher than the baseline value. [20,21]. Therefore, it was chosen to perform the NMES in the Figure 3 shows the temperature and color change related L5 dermatome, which is an extremity region. to the increase in Tsk in the L5 dermatome. The inability of the voluntary contraction caused by SCI reduces the efficiency of the venous pump, located in the calf region [22]. Therefore, considering the results of our study, that due to the inefficiency of the venous pump, the Tsk in the 15 [6] Maniar N, Bach AJE, Stewart IB, Costello JT. The effects of TA muscle at t10 and t20, was still higher after the protocol. using different regions of interest on local and mean skin This research main limitation is that the accuracy of the temperature. Journal of Thermal Biology 2015; 49-50, 33-38. infrared thermometer is estimated in ±1.5°C. To minimized [7] Tang YL; He Y, Shao HW, Mizera I. Skin temperature oscillation model for assessing vasomotion of microcirculation. the error, the protocol was realized in a climatized room, with Acta Mechanica Sinica 2015; 31 (1): 132-138. the room temperature controlled, the data collection was done [8] Bochkezanian V, Newton RU, Trajano GS, Blazevich AJ. in the same day, by the same researcher and the main results Effects of Neuromuscular Electrical Stimulation in People with Spinal Cord Injury. Medicine & Science in Sports & Exercise were the comparation of the individuals with themselves. Results of the current study demonstrated that NMES [9] Carvalho DC, Martins CL, Cardoso SD, Cliquet A. protocol applied to the TA muscles altered Tsk in individuals Improvement of metabolic and cardiorespiratory responses through treadmill gait training with neuromuscular electrical with SCI. We observed a significant increase in Tsk in the stimulation in quadriplegic subjects. Artificial Organs 2006; muscle, which corroborates the hypothesis NMES induces an 30:56– 63. [10] Van Duijnhoven NT, Janssen TW, Green DJ, Minson CT, increase in local blood flow, leading to consequent increases Hopman MT, Thijssen DH. Effect of functional in Tsk and local metabolism, as demonstrated and electrostimulation on impaired skin vasodilator responses to hypothesized in our study. And according to the literature, local heating in spinal cord injury. J Appl Physiol (1985) 2009;106(4):1065-71. every 0.6ºC increase in temperature causes a 10% increase in [11] Bittar CK and Cliquet A. Effects of quadriceps and anterior metabolism [23]. tibial muscles electrical stimulation on the feet and ankles of As the Tsk in the L5 dermatome increased, future studies patients participants with spinal cord injuries. Spinal Cord 2010; 48, 881–885. would be interesting evaluating the complete or incomplete [12] Tancredo JR, Maria RM, Azevedo ERF, Alonso KC, Varoto SCI, by measuring the sensation of increased temperature in R, Cliquet A. Clinical assessment of spasticity in individuals the stimulated dermatome. with spinal cord injury. Acta Ortop Bras [online] 2013; 21(6):310-4. [13] Gorgey AS, Dolbow DR, Dolbow JD, Khalil RK, Gater DR. The effects of electrical stimulation on body composition and Author Statement metabolic profile after spinal cord injury – Part II. The Journal Research funding: The authors thank the CNPq -National of Spinal Cord Medicine 2015, 38 (1): 23-37. Council for Science and Technological Development # [14] Alexander J, Richards J, Attah O, Cheema S, Snook J, 140215 / 2014-0. Wisdell C, May Selfe, J. Delayed effects of a 20-min crushed ice application on knee joint position sense assessed by a Conflict of interest: Authors state no conflict of interest. functional task during a re-warming period. Gait & Posture Informed consent: Informed consent has been obtained from 2018; 62, 173–178. [15] Rossignoli I, Fernández-Cuevas I, Benito PJ, Herrero AJ. all individuals included in this study. Ethical approval: The Relationship between shoulder pain and skin temperature research related to human use complies with all the relevant measured by infrared thermography in a wheelchair national regulations, institutional policies and was performed propulsion test. 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Journal

Current Directions in Biomedical Engineering – de Gruyter

Published: Sep 1, 2022

Keywords: Neuromuscular Electrical Stimulation; Skin Temperature; Spinal Cord Injury

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