Relationship of the skin and subcutaneous tissue thickness in the tensiomyography response : a novel ultrasound observational study

BACKGROUND: The aim of the study was to describe and correlate the skin, subcutaneous tissue, and superficial fascia thickness assessed by ultrasonography (US) with the lumbar erector spinae muscles contractile properties evaluated by tensiomyography (TMG). METHODS: A cross-sectional descriptive study with 50 healthy participants was performed. The point of maximum lordosis in the lumbar region of the right erector spinae was evaluated by US and TMG. First, the skin, subcutaneous tissue, and superficial fascia thicknesses (cm) were assessed by US. Second, the five contractile TMG parameters were analyzed from the right erector spinae muscles belly displacement-time curves: maximal radial displacement (Dm), contraction time (Tc), sustain time (Ts), delay time (Td), and half-relaxation time (Tr). Finally, correlation analyses using Pearson (r for parametric data) and Spearman (rs for non-parametric data) coefficients were performed. RESULTS: A strong negative correlation was shown between Dm and subcutaneous tissue thickness (rs=-0.668; P<.001). Furthermore, moderate negative correlations were observed between Dm and skin thickness (r=-0.329; P=0.020) as well as Tr and subcutaneous tissue thickness (rs=-0.369; P=0.008). The rest of the parameters did not show statistically significant correlations (P > .05). CONCLUSION: Therefore, the lumbar erector spinae contractile properties during TMG assessments, especially Dm and Tr, may be widely correlated by the skin and subcutaneous tissue thickness.


INTRODUCTION
The structural properties, such as deformation, thickness and hardness, of the skin, subcutaneous tissue, and superficial fascia may influence the sensory system. 1 Furthermore, skin and subcutaneous tissue ultrasonography (US) features may be altered by postural changes in healthy subjects and different patient conditions, such as lymphedema. 1,2nsiomyography (TMG) appears as a new technological device for evaluating the contractile properties of skeletal muscles and has recently been applied to assess musculoskeletal conditions in the lumbar erector spinae muscles. 3Nevertheless, skin thickness distributions, as well as the local hypodermal/subcutaneous fat, and fascia distributions may disturb the trunk dorsum sensitivity and should be investigated through future work. 1 Therefore, the aim of this study was to describe and correlate the skin, subcutaneous tissue, and superficial fascia thickness assessed by US in the erector spinae muscles contractile properties evaluated by TMG.

Study Design
A cross-sectional descriptive study was carried out between October 2015 and December 2016, following the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guidelines and checklist. 4Previously, the review board of the European University of Madrid (CIPI/039/15) had approved this study.Informed consent forms were signed by all participants before the beginning of the study.Furthermore, the Helsinki Declaration and ethical standards in human experimentation were considered.This research was funded and supported by the Real Madrid -European University (Ref.: 2015/09RM) and the European University of Madrid (Ref.:2015/UEM04).

Sample
A convenience sample of 50 healthy participants was recruited from the Faculty of Health, Exercise and Sport of the European University of Madrid.The inclusion criteria were healthy subjects, aged between 18 and 60 years, without bilateral non-specific pain as well as structural, neurological, visceral, or red flag conditions in the lumbopelvic region (between the subcostal line and the popliteal fossa).The exclusion criteria were prior lumbopelvic pain or treatments (within the previous 6 weeks), or medical record of neuropathy, myopathy, rheumatoid arthritis, inability to follow instructions, cognitive impairments, dysmenorrhea, pregnancy, body mass index (BMI) greater than 31 kg/m 2 , high-level athlete self-reported activity, skin disorders, conditions (such as fracture, structural deformities or neoplasm) and surgeries in the lumbopelvic or lower limb regions. 3,6ciodemographic data Gender, age (y), height (cm), weight (kg), occupation (teacher, administrative staff, sports monitor, or other occupations) and BMI (kg/cm 2 ) calculated by the Quetelet index were registered. 7

Outcome measurements
Participants were placed in prone decubitus.Then, the point of maximum lordosis in the lumbar region of the right erector spinae (approximately 2 cm lateral to the 3 rd lumbar vertebrae) was marked on the skin with a grid of 4 perpendicular lines.Furthermore, the outcome measurement order for each point was TMG and US in order to avoid the influence of the US gel temperature on the electrical stimulus. 3irst, all US evaluations and measurements were performed by the same rater, who had over 4 years of experience.A diagnostic ultrasound system (Mindray Z6; Shenzhen Mindray Bio-Medical Electronics, Nansham, 518057, China) with a 5-10.0MHzrange linear transducer (7 L4P type; 38-mm footprint), a frequency of 10.0MHz, a total depth imaging of 4cm and the focus located with a depth of 0.5cm were used to assess the resting B-mode US.The center of the probe coincided with the center of the skin marks (point of maximum lordosis) in a transversal and perpendicular position to the erector spinae muscle fibers.Skin (more superficial hyperechogenic band), subcutaneous tissue (hypoechogenic band under the skin), and erector spinae superficial fascia (hyperechogenic band under the subcutaneous tissue) US thicknesses measurements (cm) were performed in the center of the probe footprint with the software of the US system (Fig. 1).In addition, 3 ultrasound images were captured at the same point, at the end of expiration.The mean of the 3 repeated measurements was used for the data analysis.Second, TMG was used to assess the contractile properties of erector spinae muscles. 3The five con-

Statistical analysis
SPSS version 22.0 for Windows (SPSS IBM, Chicago, IL, USA) was utilized for the data analysis.First, Kolmogorov-Smirnov test was carried out to identify normal distribution (height, weight, BMI, Dm and skin thickness) or non-normal distribution (age, Td, Tc, Ts, Tr, subcutaneous tissue and superficial fascia thicknesses).Second, descriptive statistics were calculated depending on parametric (mean and standard deviation, SD) and non-parametric (median and interquartile range, IR) data.Finally, correlation analyses using Pearson (r for parametric data) and Spearman (r s for non-parametric data) coefficients were performed to evaluate the relationship between the outcome measurements.Correlations were interpreted as weak (0.00−0.30), moderate (0.31−0.60), or strong (0.61−1.00). 3,11A 95% confidence interval (P<0.05) was considered for all data analyses.

RESULTS
A sample of 50 participants, 29 (58%) men and 21 (42%) women, with an age median (IR) of 36 (11.50) years as well as height, weight and BMI mean (SD) of 172.94 (8.99) cm, 72.11 (15.05) kg and 23.91 (3.58) kg/cm 2 , respectively, was recruited.Regarding the occupations, there were 33 (63%) teachers, 7 (14%) members of administrative staff, 5 (10%) sports monitors, and 5 (10%) with other occupations.US measurements showed a skin thickness tractile objective parameters were analyzed from the right erector spinae muscle belly displacement-time curves: maximal radial displacement (Dm; mm of displacement secondary to the muscle belly electrical stimulus), contraction time (Tc; ms from 10% to 90% of Dm in the ascending curve), sustain time (Ts; ms from 50% of Dm on both sides of the curve), delay time (Td; ms from the onset of electrical stimulus to 10% of Dm), and half-relaxation time (Tr; ms from 90% to 50% of Dm on the descending curve).Interexaminer reliability from good to excellent was stated for these contractile parameters. 9The digital displacement transducer (GK 40, Panoptik d.o.o., Ljubljana, Slovenia) was placed perpendicular to the muscle belly on the point of maximum lordosis with an initial pressure of 1.5•10 -2 N•mm -2 , coinciding with the center of the skin marks. 10Two circular self-adhesive electrodes (Model 3100C, Uni Patch, Wabasha, USA) with a diameter of 3.2cm were placed symmetrically at 1.6cm distal and proximal to the sensor tip (interelectrode distance of 3.2cm), longitudinally to the right erector spinae muscle belly (Fig. 2   mean (SD) of 0.29 (0.04) cm as well as subcutaneous tissue and superficial fascia thickness medians (IR) of 0.30 (0.31) and 0.28 (0.12) cm, respectively.TMG measurements showed a Dm mean (SD) of 3.65 (1.98) mm as well as Td, Tc, Ts and Tr medians (IR) of 18.07 (2.80), 16.09 (3.42), 70.59 (322.34) and 39.93 (171.70)ms, respectively.As shown in the Table, a strong negative correlation was found between Dm and subcutaneous tissue thickness (r s =-0.668;P<0.001).In addition, moderate negative correlations were observed between Dm and skin thickness (r=-0.329;P=0.020), as well as Tr and subcutaneous tissue thickness (r s =-0.369;P=0.008).
The other parameters did not show statistically significant correlations (P>0.05).

DISCUSSION
This novel study supports the use of US during Dm and Tr TMG parameter assessment in order to evaluate the relationship of skin and subcutaneous tissue thicknesses in the evaluation of lumbar erector spinae contractile properties. Therefore, prior TMG studies may have been influenced by the thickness of these tissues in the lumbopelvic region. 3In addition, the spine postures between extension and flexion may alter the skin thickness from 12% to 38%.Consequently, such large structural deformations of the skin of the trunk dorsum should be considered in order to determine their influence in sensitivity assessments. 1

Limitations
As limitations of the present study, Tr has shown insufficient reliability compared to the inter-rater reliability for the rest of TMG contractile parameters. 9Furthermore, Dm may be modified depending on each muscle group, cross-sectional muscle area, and subject, according to the morphofunctional and training characteristics. 14Finally, the small sample size and correlations in lumbopelvic conditions should be considered in future research.

CONCLUSIONS
The lumbar erector spinae contractile properties during TMG assessments, especially Dm and Tr, may be widely correlated with the skin and subcutaneous tissue thickness.Therefore, we encourage authors to consider these tissues during intersubject evaluations in future TMG research.

CONFLICT OF INTEREST AND SOURCE OF FUNDING STATEMENT
This research was funded and supported by the Real Madrid -European University (Ref.: 2015/09RM) and the European University of Madrid (Ref.:2015/UEM04).

TABLE .
CORRELATIONS BETWEEN ERECTOR SPINAE TMG CONTRACTILE PROPERTIES AND THICKNESS US MEASUREMENTS OF THE SKIN, SUBCUTANEOUS, SUPERFICIAL FASCIA AND TOTAL TISSUES.