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Published in final edited form as: Dysphagia. 2019 Jun 17;35(2):301–307. doi: 10.1007/s00455-019-10029-6

Transcutaneous Electrical Stimulation on the Submental Area: The Relations of Biopsychological Factors with Maximum Amplitude Tolerance and Perceived Discomfort Level

Ali Barikroo 1, Karen Hegland 2, Giselle Carnaby 3, Donald Bolser 4, Todd Manini 5, Michael Crary 3
PMCID: PMC8394858  NIHMSID: NIHMS1733228  PMID: 31209638

Abstract

Transcutaneous Electrical Stimulation (TES) is a frequently used adjunctive modality in dysphagia rehabilitation. Stimulating deeper swallowing muscles requires higher TES amplitude. However, TES amplitude is limited by maximum amplitude tolerance (MAT). Previous studies have reported high interindividual variability regarding MAT and perceived discomfort. This variability might be one of the potential reasons of conflicting outcomes in TES-based swallowing studies. MAT and perceived discomfort are influenced by a variety of biopsychological factors. The influence of these factors related to swallow applications is poorly understood. This study explored the relation of biopsychological factors with MAT and perceived discomfort related to TES in the submental area. A convenience sample of thirty community-dwelling older adults between 60 to 70 years of age provided data for this study. Gender, submental adipose tissue thickness, perceptual pain sensitivity, and pain coping strategies were evaluated for each subject. Subsequently, MAT and perceived discomfort level were determined using TES on the submental area. Relation of different biopsychological variables with MAT and discomfort level was examined using Pearson and Spearman correlation, and Mann–Whitney U test. Results indicated that neither gender nor adipose thickness was related to MAT and perceived discomfort. Among studied pain coping strategies, catastrophizing was significantly related to MAT(r = −.552, P<.002). Distraction was significantly related to perceived discomfort level (r = −.561, P<.002). Given the negative impact of pain catastrophizing on MAT and the positive impact of distraction on perceiving discomfort, these coping strategies should be considered as amplitude-limiting and discomfort-moderating factors in TES-based dysphagia rehabilitation.

Keywords: Maximum Amplitude Tolerance, Biopsychological factors, Discomfort, Deglutition, Deglutition disorders

Introduction

Transcutaneous Electrical Stimulation (TES) has been one of the most studied modalities in dysphagia rehabilitation. TES intends to improve the movement of swallowing structures through inducing muscle contractions. TES amplitude is the primary parameter that determines the strength of muscle contraction [1]. Studies on limb muscles have shown that the ability to tolerate higher amplitude levels is associated with greater muscle contractions [2,3]. Furthermore, recent TES studies on submental region showed that tolerating higher amplitude level can increase the effect of TES on lingual depressor muscles and subsequently decrease the lingual-palatal pressure during swallowing [4,5]. The authors indicated that this TES-lowering effect has a potential to be used as a resistive exercise paradigm to strengthen the lingual muscles during swallowing. In another TES study on submental region, Barikroo et al. [6] showed that using short pulse duration (300 μs) can enhance maximum amplitude tolerance (MAT) compared with long pulse duration (700 μs) without changing the perceived discomfort level. The authors concluded that this enhanced MAT level has a potential to increase the depth of electrical current penetration and further improve the swallowing muscle strengths. Beyond the effect of TES parameters, biopsychological characteristics of each subject might also influence MAT and perceived discomfort level. Since many pain nerve fibers are located near the skin surface, increasing TES amplitude can become noxious and uncomfortable at some point [7,8]. Previous studies have reported high interindividual variability regarding MAT and perceived discomfort level associated with higher TES amplitudes [9,10]. This interindividual variability might be one of the potential reasons of equivocal evidence regarding the effectiveness of TES compared with other conventional modalities in this field [11]. Factors affecting this interindividual variability in MAT and perceived discomfort can potentially be investigated using the biopsychological model of pain perception [12]. According to this model, pain experience incorporates biopsychological dimensions. The biological dimension refers to the subject’s biological characteristics that mediate the impact of noxious stimuli. For example, experimental pain studies indicate that being male [13], older [14], and having greater body mass index (BMI) [15] are related to higher pain tolerance and less perceived intensity of pain. The psychological dimension incorporates emotional-affective status and cognitive-evaluative strategies that each individual may rely on to interpret the pain experience. Outcomes of studies relating to emotional-affective status suggest that subjects with greater fear of pain [16,17], anxiety [18,19], and depressive symptoms [20-22] usually demonstrate lower pain tolerance and higher discomfort. Theoretically, negative emotional-affective status may heighten somatic tension (e.g., muscle tension), which subsequently amplifies receptive sensory perception and reduces pain tolerance [23,24]. In addition to emotional-affective status, cognitive-evaluative strategies have also been shown to modulate pain tolerance and discomfort. During pain exposure, each individual primarily uses these strategies to evaluate the significance of the pain in terms of it being threatening, benign, or irrelevant. Subsequently, the person will evaluate the controllability of pain using cognitive-evaluative strategies [12]. The tendency of individuals to rely on positive or negative cognitive-evaluative strategies during a pain experience can strongly affect an individual’s pain tolerance and perceived discomfort. For example, the tendency to exaggerate the threat value of pain, known as pain catastrophizing, is associated with reduced pain tolerance and a heightened discomfort level [25,26], while reliance on positive coping strategies, such as diverting one’s attention, ignoring the pain sensation, reinterpreting the pain sensation, and self-efficacy, may enhance pain tolerance and moderate perceived discomfort levels [27,28].

Despite the widespread application of biopsychological factors for predicting pain tolerance and discomfort in different medical fields, limited information exists regarding relationship of these factors with MAT and discomfort level. In a single study on quadriceps muscles, Piva et al. [10] investigated the relation of biopsychological attributes and MAT in a cohort of patients with rheumatoid arthritis. BMI, disability condition, the use of pain coping strategies (i.e., self-statements and catastrophizing), and anxiety were significant predictors of MAT. Furthermore, a recent study applying TES in the submental area investigated the relation of limited biopsychological factors with MAT and discomfort [6]. The results indicated that submental adipose tissue thickness positively relates to the MAT. Moreover, pain sensitivity negatively related to MAT but positively related to the perceived discomfort level. However, a strong theoretical basis was required to investigate the relation of biopsychological factors with MAT and discomfort level using a systematic model of pain perception. Based on this model, additional variables should be taken into account to inclusively investigate the relation of biopsychological variables with MAT and perceived discomfort level in the anterior neck region.

Thus, the aim of this study was to evaluate potential relations between biopsychological characteristics, MAT, and perceived discomfort level in healthy older adults. Studies on healthy adults are a good first step in that we have a better understanding of swallowing function in healthy adults. The reason that this study focused on healthy older adults derives from the epidemiologic reports indicating that risk of dysphagia increases with age [29]. Furthermore, recent TES studies have shown that TES has distinctive physiologic effects on swallowing across age groups [30,5]. As we gain knowledge on those parameters that impact maximum amplitude tolerance and its impact on the healthy swallowing mechanism we plan to apply these strategies toward the rehabilitation of adults with various types of swallowing impairment. We hypothesized that being male and having higher subcutaneous adipose tissue thickness, less pain sensitivity, higher reliance on positive pain coping strategies and less reliance on negative pain coping strategies is related with higher MAT and less perceived discomfort level.

Materials and Methods:

Participants

Thirty self-reported healthy community-dwelling older adults between 60 and 70 years of age (15 males and 15 females) with a mean age of 64.27 years (SD = 2.70 years) were enrolled in this study. All participants were recruited via convenience sampling. All participants reported having a regular diet with no current or previous history of dysphagia or any condition known to be associated with dysphagia. The study protocol was approved by the local Institutional Review Board.

Biological Factors

Gender

Participant sex (male/female) was recorded as part of an initial health history questionnaire.

Submental adipose tissue thickness

Submental adipose tissue thickness was measured objectively using the Digital Body Fat Caliper (Ningbo Sunshine International Co, Zhejiang, Ningbo, China). The examiner took a diagonal fold of submental skin and placed the caliper approximately 1 cm above the fingers to measure its thickness. Three measurements were obtained and mean of three measures was reported.

Psychological Factors

Emotional-affective measure: pain sensitivity

The Pain Sensitivity Questionnaire (PSQ) was used to evaluate pain sensitivity [31,32]. PSQ is a validated self-rating questionnaire for the assessment of perceptual pain sensitivity. This questionnaire comprises 17 items, each relating to a series of simulated situations. Respondents are asked to rate how painful each situation would be from 0 (not painful at all) to 10 (worst pain imaginable). The items contain a wide array of intended pain intensities along with different types of pain (i.e. hot, cold, sharp, etc.) in various body locations.

Cognitive-evaluative measure: pain coping strategies

Pain coping strategies refer to cognitive strategies used to manage pain tolerance. This study assessed the use of pain coping strategies via the Coping Strategies Questionnaire-Revised Version (CSQ-R) [33]. The CSQ-R consists of 27 items and measures the following six cognitive-based coping categories: diverting attention, reinterpreting pain sensation, coping self-statements, ignoring pain sensation, praying or hoping, and catastrophizing. Each category is composed of the sum of 3–6 items measured with a numerical rating scale ranging from 0 (never do that) to 6 (always do that) indicating how frequently the strategy is used to cope with pain. Higher scores represent greater reliance on that coping strategy to decrease pain. Based on the instruction manual, if subjects had no pain or meaningful experience with pain, the investigator asked them to imagine what coping strategy they tend to use if pain occurs. The CSQ-R has good internal consistency coefficients in subscales ranging from α = 0.72–0.86 and has been validated in different age groups, including in older adults.

Maximum Amplitude Tolerance Measurement

TES was provided using the VitalStim Experia Electrotherapy System through two pairs of stimulating electrodes (VitalStim; DJO Global, Vista, CA, USA). The electrodes were placed obliquely above the hyoid bone on the submental region of the neck. TES was presented with fixed pulse duration (700 μs), and pulse frequency (80 HZ). To identify MAT, the stimulation amplitude was increased gradually by 1 mA at five-second intervals until the participant notified the investigator (i.e., raised their hand) that further increase in stimulation amplitude would not be tolerated for any reason. This amplitude level was defined as MAT.

TES-Induced Discomfort Measurement

Participants were asked to rate any discomfort level in the submental area after reaching MAT using the Visual Analogue Scale (VAS) [34]. The VAS is a validated tool that has been used frequently for appraising and comparing the intensity of pain and discomfort levels. The tool comprised of a 100 mm continuous scale ranging from “No Discomfort” to “Worst Discomfort Ever.”

Statistical analysis

Bivariate correlational analyses were performed using Pearson's correlation coefficient to examine relationship between submental adipose tissue thickness with MAT and perceived discomfort level. Since both PSQ and CSQ comprised ordinal items, the relation of pain sensitivity and pain coping strategies with MAT and perceived discomfort level were examined using Spearman's correlation coefficient. Furthermore, since gender is a dichotomous variable, a Mann–Whitney U (non-parametric t-test) test was conducted to determine the association of gender with MAT and perceived discomfort level. The Bonferroni correction test was applied to adjust the alpha level by the number of tests that were performed (p<0.05/18) and the significance level was set at p<0.003. IBM SPSS Statistics 22.0 (IBM Corporation, Somers, NY) was used for all statistical analyses.

Results:

The data were first examined for normal distribution. All variables met parametric assumptions. The mean MAT was 7.00 mA (SD= ±3.67) ranging from 3 to 18 mA. In addition, the mean reported perceived discomfort level was 6.47 out of 10 (±1.24) ranging from 3.7 to 8.9. No significant differences were found across gender on any of the variables. The descriptive results of other biopsychological measures are presented in Table 1. Inferential results are as follows:

Table 1.

Means and standard deviation (SD) of maximum amplitude tolerance, discomfort level, submental adipose tissue thicknesses, pain sensitivity and pain coping strategies across gender and in total.

Variables Male Female Total
Mean (SD) Range Mean Range Mean Range
SM Adipose Tissue Thickness (mm) 14.17 (5.37) 9.1-23.3 16.76 (7.20) 7.9-34.2 15.55 (6.44) 7.9-34.2
Pain Sensitivity (Out of 10) 4.43 (1.30) 2.4-6.5 3.99 (2.06) 0.9-9.1 4.20 (.317) 0.9-9.1
Pain Coping Strategies
Distraction 14.21 (7.58) 3-27 13.00 (9.15) 0-30 13.57 (8.34) 0-30
Catastrophizing 4.36 (4.56) 0-14 3.94 (6.00) 0-23 4.13 (9.67) 0-23
Ignoring 14.07 (6.02) 6-26 15.19 (8.23) 0-30 14.67 (1.31) 0-30
Distancing 5.71 (4.93) 0-13 6.19 (7.05) 0-24 5.97 (1.10) 0-24
Coping 15.29 (5.22) 6-23 16.19 (5.61) 0-24 15.77 (.979) 0-24
Praying 10.07 (6.65) 0-18 7.81 (7.22) 0-18 8.87 (1.26) 0-18

Biopsychological Factors and MAT

Catastrophizing was inversely related to MAT (r = −.552, P<.002). No significant relationship was found between pain sensitivity, distraction, catastrophizing, ignoring, distancing, coping, and praying with MAT at the 0.003 level. In terms of biological factors, the relation between MAT and submental adipose tissue thickness did not reach statistical significance (Table 2). Likewise, gender was not significantly associated with MAT (U = 344.500, p < .124).

Table 2.

Relationship between biopsychological factors with maximum amplitude tolerance (MAT), and perceived discomfort.

MAT Discomfort
Biopsychological factors r p r p
Pain Sensitivity −.350 .068 .156 .419
SM Adipose Tissue Thickness .114 .562 −.111 .566
Distraction −.446 .017 −.561* .002
Catastrophizing −.552* .002 −.118 .554
Ignoring −.044 .823 −.114 .556
Distancing −.275 .157 −.349 .063
Coping −.247 .205 −.263 .168
Praying −.149 .449 .148 .442
*

Correlation is significant at the 0.003 level.

Biopsychological Factors and Perceived Discomfort Level

Distraction was inversely related to perceived discomfort level (r = −.561, P<.002). However, the relation between other psychological factors and perceived discomfort level did not reach the specified significance level of .003. Regarding the biological factors, submental adipose tissue thickness had a non-significant relationship with perceived discomfort level (Table 2). Similarly, gender was not significantly associated with perceived discomfort level (U = 406.500, p < .538).

Discussion:

The primary aim of this study was to evaluate relations of biopsychological factors with MAT and perceived discomfort level. The primary finding was that catastrophizing was negatively related with MAT. Moreover, distraction was inversely related to perceived discomfort level. No significant relationship was identified between other biopsychological variables with MAT or perceived discomfort level.

Catastrophizing was inversely related to MAT. Specifically, subjects who tended to rely more on catastrophizing strategies during pain experience, demonstrated lower MAT. This finding is consistent with Piva et al.’s study [10], indicating an inverse relationship between catastrophizing and MAT in the limbs. In a broader context, this finding also supports previous experimental pain studies reporting an opposite relationship between catastrophizing and pain tolerance [35,36]. Catastrophizing is a negative coping strategy during which an individual tends to focus on and exaggerate the threat value of nociceptive stimuli [37]. Relying on this strategy may increase the attentional focus on pain and/or emotional responses to pain, which subsequently reduces pain tolerance [38].

Distraction was negatively related to perceived discomfort level. Specifically, subjects who relied more on distraction strategies perceived less discomfort level. In a broader context, this result was consistent with Ruscheweyh et al.’s experimental pain study [39] that demonstrated the positive effect of distraction strategies on reducing pain perception in healthy adults. Distraction has been known as a positive pain coping strategy that comprises diverting attentional resources to a non-painful perceptual stimulus in order to modulate the perceived pain endurance. While the mechanism of effect is still not fully understood, some neuroimaging studies have demonstrated that distraction strategies may reduce perceived discomfort level via activating the inhibitory pain control system [40,41].

Except catastrophizing and distraction, other pain coping strategies were not related with MAT and perceived discomfort level. This finding also is consistent with other TES study [10], which was performed on patients with rheumatoid arthritis. Despite differences between study populations and TES locations (quadriceps muscles vs submental muscles in current study), most of pain coping strategies in two studies were not related to MAT and discomfort. One potential reason is that some of the tested pain coping strategies such as praying and pain distancing strategies are more likely to be used under chronic and/or life-threatening conditions rather experimental pain conditions [42].

Pain sensitivity and submental adipose tissue thickness were neither related with MAT nor perceived discomfort level. These findings were not consistent with Barikroo et al.’s study [6] that was performed on the submental region. Specifically, they reported that Pain sensitivity was inversely related to MAT and directly related to perceived discomfort level. Furthermore, they reported a positive relationship between adipose tissue thickness and MAT. Methodological differences may explain disparity in the results. Specifically, MAT from the current study was taken from a single TES protocol while the MAT for the other study was calculated based on the mean of four different TES protocols with varied pulse durations and pulse frequencies. Given the notion that pulse durations influences MAT, future studies should investigate how pain sensitivity and adipose tissue thickness interact with MATs from different TES protocols.

Gender was not associated with either MAT or perceived discomfort level. This finding replicates the results of Barikroo et al.’s study [6]. In a broader context, this finding is also consistent with a recent systematic review indicating a lack of gender effect on pain tolerance [13]. As a result, it seems that gender is not a strong biological factor for predicting interindividual differences in MAT and perceived discomfort level.

This study was conducted on a small cohort of healthy older adults. As a result, the probability of making a type-one error was inevitable especially for variables that showed a trending relationship with MAT and perceived discomfort level (i.e. pain sensitivity, distancing). Using multivariate analysis, additional biopsychological variables should be examined to better understand the impact of different biopsychological variables on MAT and perceived discomfort level. Furthermore, this study used the CSQ-R [33] to explore relations of cognitive-evaluative strategies with MAT and perceived discomfort level. Since this questionnaire was originally designed for clinical and chronic pain conditions, the content of some items (i.e., I feel my life does not worth living) and/or subscales (i.e., praying) may not be well suited to this type of study. Future studies should also be directed towards developing validated pain sensitivity and pain coping strategy tools that can predict MAT and perceived discomfort level in the submental and infrahyoid areas. Developing these tools needs additional effort in identifying appropriate biopsychological variables that are related with MAT and discomfort level in the submental region. Given the inverse relationships between catastrophizing and MAT as well as distraction and perceived discomfort level, future studies should also explore whether controlling negative coping strategies (i.e. catastrophizing) or the utilization of positive coping strategies (i.e. distracting from pain) will increase MAT or decrease discomfort level.

Conclusion:

Results of the present study suggest that catastrophizing is a primary coping strategy inversely related to MAT. Furthermore, distraction was inversely related to perceived discomfort level. Additional studies are required to identify other biopsychological variable that can predict MAT and perceived discomfort level. In addition, larger samples and more rigorous statistics (i.e. multivariate) are required to better discern the impact of more biopsychological variables on MAT/perceived discomfort level. The long-range goal of these studies is to create a clinical protocol in which clinicians can use higher TES amplitude levels toward the goal of stimulating deeper muscles of swallowing.

Funding

This study was partially supported by the National Center For Advancing Translational Sciences of the National Institutes of Health under Award Number UL1TR001427. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Footnotes

Conflict of Interest The authors declare that they have no conflict of interest.

Ethical approval All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed Consent Informed consent was obtained from all individual participants included in the study

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