Doublet stimulation protocol to minimize musculoskeletal stress during paralyzed quadriceps muscle testing

Abstract

With long-term electrical stimulation training, paralyzed muscle can serve as an effective load delivery agent for the skeletal system. Muscle adaptations to training, however, will almost certainly outstrip bone adaptations, exposing participants in training protocols to an elevated risk for fracture. Assessing the physiological properties of the chronically paralyzed quadriceps may transmit unacceptably high shear forces to the osteoporotic distal femur. We devised a two-pulse doublet strategy to measure quadriceps physiological properties while minimizing the peak muscle force. The purposes of the study were 1) to determine the repeatability of the doublet stimulation protocol, and 2) to compare this protocol among individuals with and without spinal cord injury (SCI). Eight individuals with SCI and four individuals without SCI underwent testing. The doublet force-frequency relationship shifted to the left after SCI, likely reflecting enhancements in the twitch-to-tetanus ratio known to exist in paralyzed muscle. Posttetanic potentiation occurred to a greater degree in subjects with SCI (20%) than in non-SCI subjects (7%). Potentiation of contractile rate occurred in both subject groups (14% and 23% for SCI and non-SCI, respectively). Normalized contractile speed (rate of force rise, rate of force fall) reflected well-known adaptations of paralyzed muscle toward a fast fatigable muscle. The doublet stimulation strategy provided repeatable and sensitive measurements of muscle force and speed properties that revealed meaningful differences between subjects with and without SCI. Doublet stimulation may offer a unique way to test muscle physiological parameters of the quadriceps in subjects with uncertain musculoskeletal integrity.

Figures

Fig. 1

Schematic representation of the stimulation protocol. (Interpulse intervals are to scale, but rest periods between the conditions are truncated.) Five repetitions were performed of each single-twitch condition (1t, 1t2, 1t3). Three repetitions were performed of each train (5t, bracket) and doublet condition (5d, 6d, 7d, etc). Each repetition was separated by 1 s (1t, 1t2, and 1t3) or by 2 s (train and doublet conditions) to ensure force returned to baseline before the next stimulation.

Fig. 2

Method of determination of dependent variables. Top: a single twitch is depicted. On the ascending limb of the twitch, the rate of force rise was defined as the quotient of 1) the force developed in the rectangular region (80% of peak minus 20% of peak), and 2) the elapsed time of the rectangular region (ms). On the descending limb of the twitch the rate of force fall was defined as the quotient of 1) the force decay in the rectangular region (80% of peak minus 20% of peak), and 2) the elapsed time of the rectangular region (ms). For each twitch response, rate of force rise and rate of force fall were divided by the peak force of that twitch to yield normalized rates in ms−1. Bottom: a 10-Hz doublet response, with stimulus pulses at 0 and 100 ms, is depicted. To analyze twitch difference, the force record was partitioned into 2 events based on the onset/offset of the stimulus pulses (denoted “A” and “B”). Twitch difference was defined as the maximum force developed in event B minus the maximum force developed in event A. The twitch difference was normalized by peak force to yield the fusion ratio. Bottom, inset:a doublet at 30 Hz is depicted. Note that the short interpulse interval causes event A to contain almost no force data, undermining the validity of the fusion ratio. Fusion ratio is therefore not reported for doublets with small interpulse intervals (15, 20, and 30 Hz).

Fig. 3

Representative example of force response to doublet stimulation at several frequencies (subject SCI 2, Table 1). SCI, spinal cord injury.

Fig. 4

Mean (SE) normalized quadriceps force elicited by twitches (1t, 1t2, 1t3), 5-Hz trains (5t), and various doublet stimulation frequencies (6d, 7d, etc.). SCI and non-SCI refer to subjects with and without spinal cord injury, respectively.

Fig. 5

Contractile speed properties for pretetanic (1t), posttetanic (1t2), and postdoublet (1t3) twitches. Top: normalized rate of force rise. *Greater than 1t (P < 0.05); **Greater than 1t and 1t2 (P < 0.05). Bottom: normalized rate of force fall. *Less than 1t2 and 1t3 (P < 0.05); **Less than 1t3 (P < 0.05).

Fig. 6

Twitch difference (top) demonstrates the relative contribution of the two doublet pulses (A and B) to the overall force. Note that the force contributed by the A pulse varies little across frequencies, while the force contributed by the B pulse is subject to summation of force. The fusion ratio (bottom) demonstrates the specific contribution of the B pulse, normalized to peak force. A higher fusion ratio denotes a greater relative influence of summation of force between doublet pulses.