The effects of poliomyelitis on motor unit behavior during repetitive muscle actions: a case report

Acute paralytic polio is a disease caused by the poliovirus that typically occurs in young children. The poliovirus spreads along nerve pathways and primarily destroys motorneurons of the anterior horns[1]. The poliovirus usually results in asymmetrical paralysis with muscle atrophy and weakness occurring in the lower limbs more so than the upper limbs[2]. Numerous studies have used indwelling electromyography (EMG) to investigate the denervation and reinnervation characteristics of the affected muscle (i.e., motor unit number and amplitude, motor unit firings, conduction velocity, etc.)[3–8]. For example, Larsson et al.[7] reported that healthy participants had greater motor unit (MU) firing rates of the tibialis anterior muscle than the poliomyelitis participants during slowly increasing isometric voluntary muscle actions. In addition, McComas et al.[9] reported a reduction in motor unit number after an acute bout of poliomyelitis at twice the rate than healthy subjects aged > 60 years, whereas, Herda and Cooper[10] reported a reduction in MUs recruited above 20% of maximal voluntary contraction (MVC) for a poliomyelitis patient in comparison to healthy participants.

Recently, De Luca et al.[11] developed technology able to decompose the raw surface EMG signals recorded during isometric muscle actions into its constituent MU action potential trains with the Precision Decomposition (PD) III algorithm. The resulting output allows for the examination of the firing instances for each detected MU. The PD III algorithm has typically detected 30-40 MUs and occasionally up to 60 MUs during a single isometric trapezoid muscle action at various force levels (5 – 100% MVC). Previously, De Luca et al.[11] and Nawab et al.[12] validated the PD III algorithm and reconstruct-and-test (used for testing accuracy of MU action potential trains) algorithms. This decomposition technology has been used to examine the MU control scheme, which states that lower threshold MUs have higher firing rates than higher threshold MUs during isometric muscle actions[13–15]. However, there is limited information available regarding the use of EMG decomposition in clinical populations[10, 16]. It would be expected that an acute bout of paralytic polio would influence the overall MU control scheme and be detectable by the EMG decomposition technique developed by De Luca et al.[11], which was supported by Herda and Cooper[10].

Previous studies have utilized repetitive isometric muscle actions to further elucidate mechanisms of fatigue on MU behavior[17, 18]. For example, Carpentier et al.[18] indicated that central drive intensified, as measured by EMG amplitude, while MU discharge rates decreased progressively during the repetitive muscle actions of the first dorsal interosseous at 50% MVC. In addition, the authors reported that the level of change in MU behavior was related to recruitment threshold (low- versus high-threshold), which was also supported by Farina et al.[17]. To date, it is unknown the influence of poliomyelitis on MU firing rates and other EMG parameters (amplitude and center frequency) during repetitive muscle actions. Since polio patients have far less motorneurons as a result of the denervation and reinnervation process, it is conceivable that their MU behavior during the repetitive tasks would be altered in comparison to healthy subjects. Therefore, the purpose of this study was to examine the MU control scheme and EMG amplitude and frequency of the vastus lateralis (VL) during 20 repetitive isometric muscle actions at 50% MVC for healthy individuals and one individual that acquired acute paralytic poliomyelitis.

In this case report, we present one participant that acquired acute type III spinal poliomyelitis (mean ± standard deviation [SD], Caucasian male, age = 29 yrs, weight = 63.4 kg, height = 150.7 cm) at 3 months of age and three healthy participants (Caucasian females, age = 19.7 ± 2.1 yrs, weight = 67.5 ± 9.4 kg, height = 170.7 ± 2.3 cm). Previous research has reported no sex-related differences in EMG amplitude, EMG frequency, or MU behavior during fatiguing contractions[19–25].

The participant with acute type III spinal poliomyelitis (PO) reported neuromuscular deficiencies as a result of disease in the hips, knees, buttocks, thighs, and lower legs. None of the healthy (HE) participants reported any current or ongoing neuromuscular diseases or musculoskeletal injuries. Each participant signed a written informed consent document. This study was approved by the Human Subjects Committee – Lawrence at the University of Kansas.

Previously, Larsson et al.[7] reported differences in MU firing rates between healthy and prior polio patients during “slowly increasing isometric voluntary contractions”^(p.190). The y-intercept from the MFR versus recruitment threshold relationships theoretically represents a maximal firing rate sustainable by the lowest threshold MUs[14]. In the present study, the MFRs for the HE were higher (y-intercept range: 33.42 ± 2.41 – 29.12 ± 1.83 pps) than the PO (y-intercept range: 25.64 - 23.48 pps) for each repetition (Figure 2). Negative slopes were reported from the linear regressions for each participant and contraction and, thus, earlier recruited MUs tended to have greater firing rates than the later recruited MUs. Referring to Table 1 and Figure 2, there were no observed differences between the slopes between PO and HE participants. Therefore, the inverse relationship between the firing rate and recruitment threshold typically reported in healthy muscle was present for the PO muscle[14]. The overall MU control scheme (i.e., negative slopes) was similar between the PO and HE participants, however, the MFRs were less (i.e., y-intercepts) for the PO than the HE participants. High-threshold MUs are typically described as fast fatiguing for the VL. De Luca and Hostage[14] suggested that if the high-threshold MUs discharged at relatively higher rates, high-threshold MUs would fatigue more quickly and force will not be maintained. Since it has been reported that there are far less motorneurons in the PO than HE participants as a result of denervation[5, 8], the lower MFRs throughout the force spectrum for the PO is possibly a fatigue protecting mechanism.

EMG RMS is a global measure of MU recruitment and firing rates while EMG MPF reflects the average muscle fiber conduction velocity[28]. Classically, muscle fatigue has been monitored with these EMG parameters and indicators of fatigue are believed to be evident by increases in RMS and decreases in MPF[29]. An increase in EMG RMS is the result of synchronization of active MUs and the recruitment of new MUs while the decrease in MPF has been primarily attributed to a reduction in muscle fiber conduction velocity[30]. For the 1^st to 10^th repetition, the HE had an increase (17.7%) in EMG RMS while EMG MPF declined (10.0%). Concurrently, the y-intercepts from the MFR versus recruitment threshold relationships decreased (12.4%) for the HE participants and, thus, would suggest that the HE participants recruited additional MUs and/or had greater MU synchronization during the 10^th repetition in comparison to the 1^st repetition. In contrast, the y-intercepts from the MFR versus recruitment threshold relationships and EMG RMS decreased (8.4% and 6.6%) simultaneously while EMG MPF (+1.8%) remained stable from the 1^st to 10^th repetition for the PO participant. For the 10^th to 20^th repetition, there was relatively no change in the y-intercepts (0.5%) or EMG MPF (-1.7%), however, EMG RMS increased 9.3% for the HE. For the PO, the y-intercept from the MFR versus recruitment threshold and EMG RMS returned to baseline levels (i.e., increased) during the 20^th repetition. The EMG parameters indicated that MU behavior differed between the PO and HE during the repetitive muscle actions. Subsequently, MU firing rates and EMG RMS responded in a similar manner for the PO, in contrast, MU firing rates and EMG MPF decreased while EMG RMS increased during the repetitive muscle actions for the HE. Future studies may want to consider normalizing these parameters to an MVC rather than a submaximal muscle action as in the present study to further elucidate neural mechanisms of fatigue.

Previously, Larsson et al.[7] reported that polio patients used muscle fibers in an all or none manner during slowly increasing isometric voluntary muscle actions. In the present study, the changes in EMG RMS mirrored the changes in the y-intercepts from the MFR versus recruitment threshold relationships with relatively no change in MPF for the PO, which tentatively suggested that all MUs were recruited during each muscle action at 50% MVC. Since EMG RMS is the concurrent representation of MU recruitment and firing rates, the increase in EMG RMS with a corresponding decrease in MFR would suggest that HE relied on recruitment of additional MUs and/or synchronization of MU during the repetitive tasks. However, the mirrored changes between EMG RMS and MFR for the PO suggested that no additional MUs were recruited nor was there an increase in MU synchronization during the repetitive tasks. Interestingly, HE participants were able to complete all 20 contractions with a moderate (10.3%) reduction in post-MVC strength. Although the PO had fewer changes in all parameters measured (MU MFR, EMG RMS and MPF), the decrease in post MVC for the PO was much greater than the HE (28.0% vs. 10.3%). Thus, EMG parameters changed during the repetitive tasks despite a lack of fatigue in the HE as indicated by the successful completion of the tasks with only a moderate reduction in strength.

In summary, the denervation and reinnervation process as a result of an acute bout of poliomyelitis altered MU behavior in comparison to the HE participants. Specifically, the PO participants had lower MFRs and the y-intercepts from the MFR versus recruitment threshold relationships mirrored changes in EMG RMS from the 1^st to 20^th repetition, unlike the HE participants. Thus, suggesting that all MUs were recruited during each contraction for the PO participant. In addition, caution is warranted when examining EMG RMS and MPF and MU MFR behavior as indicators of muscular fatigue during repetitive muscle actions since the parameters changed in the HE despite successfully completing all muscle actions with only a moderate decrease in strength. Future research should examine the influence of high-intensity exercise training on the fatigability of polio patients as it is evident that the alterations in MU control scheme provide a mechanism to respond to such training despite the denervation and reinnervation process.

Written informed consent was obtained from all participants for publication of this Case Report. A copy of the written consent is available for review by the Editor-in-Chief of this journal.