Evaluating body composition and resting energy expenditure after neuromuscular electrical stimulation therapy in persons with chronic spinal cord injury

A spinal cord injury (SCI) is damage to the spinal cord that causes devastating
changes in its function. SCI affects the conduction of sensory and motor
signals across the sites of injury, which leads to the loss of sensation and
muscle function. Thus, paralysis commonly occurs below the level of injury and
people with SCI can subsequently become physically inactive along with
paralyzed muscle atrophy and metabolic disorder. Because of these lifestyle and
physiological alterations, people with SCI suffer the decline of lean body mass
(LBM) and subsequently the decline of resting energy expenditure (REE) as well
as the increase of fat mass (FM) (Tanhoffer, Tanhoffer, Raymond, Hills, &
Davis, 2014). These changes in body composition can easily cause a higher risk
of obesity and many adverse metabolic sequelae such as insulin resistance,
hyperlipidemia, and cardiovascular diseases (Bauman, Adkins, Spungen, & Waters,
1999; Maki et al., 1995; Garshick et al., 2005). Meanwhile, the lower limbs
(LL), including gluteal and hamstring muscles which are two major muscle groups
in the control of hip and knee, are naturally exposed to those negative
pathological adaptations as a result of immobilization after injury (Gorgey &
Dudley, 2007; Spungen et al., 2003). Therefore, it is of great importance to
investigate whether there is an effective method that could counteract the
unfavourable trend in body composition, especially LL-body composition, and REE
after SCI.
Surface neuromuscular electrical stimulation (NMES) has been proposed as an
effective alternative method to exercise the paralyzed muscles below the level
of injury (Creasey et al., 2004; Dudley-Javoroski & Shields, 2008). It has been
shown that NMES could evoke skeletal muscle hypertrophy and decrease ectopic
adipose tissue in people with chronic spinal cord injury (Gorgey & Shepherd,
2010; Ryan, Brizendine, Backus, & McCully, 2013). Furthermore, as numerous
high-energy cost processes occur in organs and muscles, the increase of LBM
might lead to a higher REE (Buchholz, Rafii, & Pencharz, 2001). In fact, NMES
has already been used as a therapy program for people with chronic SCI in
overcoming muscle weakness and improving muscle mass and strength (Mc Cormack
et al., 2010; Dudley-Javoroski & Shields, 2008; Gorgey et al., 2012). However,
it has not been extensively evaluated to what extent NMES therapy could improve
body composition and subsequently REE.
Several techniques have been used to assess body composition such as
dual-energy X-ray absorptiometry (DXA), computed tomography (CT), magnetic
resonance imaging (MRI), bioelectrical impedance analysis (BIA), and
ultrasound. Ultrasound can measure changes in muscle architecture and
composition such as muscle thickness, muscle echogenicity, pennation angle and
fascicle length (Strasser, Draskovits, Praschak, Quittan, & Graf, 2013;
Stringer & Wilson, 2018). These parameters are related to muscle size and
strength. Kositsky et al. reported that ultrasound is a reliable and valid
measurement of hamstring muscles cross-sectional area in the general population
when compared with the gold standard MRI (Kositsky et al., 2020). An amenable
protocol was developed by Whittaker and Emery to investigate the morphology of
gluteal muscles in healthy adolescent soccer players using ultrasound
(Whittaker & Emery, 2014). Ultrasound has the benefits of portability,
cost-effectiveness and efficiency compared to the current gold standards: DXA,
CT and MRI. This could make it become a potential diagnostic tool in clinical
practice (Stringer & Wilson, 2018). Thus, measuring with ultrasound could be
valuable to evaluate the potential changes of LL muscles after NMES therapy.
Another method that is more practical and convenient with relatively reliable
results is BIA. Buchholz et al. suggested that after adding some relevant
parameters including age, gender, height, and weight to BIA results, the method
can be used as a standard for defining body composition in people with SCI
(Buchholz, McGillivray, & Pencharz, 2003). Numerous studies have already
started to use BIA as a standard to measure body composition in people with SCI
(Eriks-Hoogland et al., 2011; Han et al., 2015; Zwierzchowska et al., 2014).
Regarding REE measurement, the most commonly used method for measuring REE in
both laboratory and field settings is indirect calorimetry. It is considered as
an accurate, reliable and non-invasive measurement of REE nowadays (da Rocha,
Alves, & da Fonseca, 2006). Many studies about REE in people with SCI have used
indirect calorimetry as a reference method (Chun, Kim, & Shin, 2017; Farkas,
Gorgey, Dolbow, Berg, & Gater, 2019; Nightingale & Gorgey, 2018).

Primary Objective: To evaluate potential changes in body composition and REE
after NMES therapy at home for 12 weeks.

We hypothesize that NMES therapy would result in hypertrophy of gluteal and
hamstring muscles, and an increase in LL-LBM, total LBM, and REE, while a
decrease in LL-FM and total FM would take place.

The study is an exploratory prospective cohort study to evaluate the potential
effects of regular NMES therapy. Participants will receive NMES therapy for LL
which is part of their regular care in Reade, center for rehabilitation and
rheumatology. The regular NMES care normally consists of one screening session,
two or three instruction sessions in Reade and long-term NMES therapy at home.
The period of NMES therapy varies individually. Based on the NMES therapy
routine in Reade and previous papers, we set up the study period for 12 weeks
since the effects of NMES on body composition could be detected in 8-12 weeks
among people with chronic SCI (Carty et al. 2013; Gorgey et al. 2012).
Therefore, people with SCI who will receive LL NMES therapy for at least 12
weeks will be included. To evaluate the potential changes, body composition and
REE will be measured at baseline and after 6 and 12 weeks using ultrasound, BIA
and indirect calorimetry devices. These measurements are normally not included
in regular care, so participants will be asked to go to Reade for two extra
times (at 6 weeks and 12 weeks). Personal and lesion characteristics including
age, gender, lesion level, lesion completeness, time since injury will be
registered at the first visit.

NMES therapy for LL including the combination of strength and endurance
programs by an electrical muscle stimulator for 12 weeks.

NMES is part of the standard care at rehabilitation center Reade in Amsterdam.
Therefore, there are no additional risks present in this study. Benefits for
patients may be present when they have the opportunity to get a very accurate
insight into their body composition and REE and how these parameters change
during 12 weeks NMES. This might motivate them to continue NMES therapy in the
future. The burden for participants will be keeping therapy diaries after each
NMES, recording dietary intake before every measurement occasion, and the
measurements of body composition and REE.