Comparison of peripheral sudomotor sensitivity to acetylcholine in endurance and non-endurance trained male subjects

Young Oh Shin, PhD,1 Jeong Beom Lee, MD, PhD2

1

Department of Healthcare, Global Graduate School, Soonchunhyang University, Asan,

Republic of Korea 2

Department of Physiology, College of Medicine, Soonchunhyang University, Cheonan,

Republic of Korea

Running title: Sudomotor sensitivity in trained subjects

One Table and five Figures



Corresponding author;

Professor Jeong-Beom Lee, M.D., Ph. D.

Department of Physiology, College of Medicine, Soonchunhyang University 366-1 Ssang yong-dong, Cheonan 330-090, Republic of Korea E-mail: [email protected] Tel.: +82-19-423-5317 and +82-41-570-2436; Fax: +82-41-570-2430

This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process which may lead to differences between this version and the Version of Record. Please cite this article as an ‘Accepted Article’, doi: 10.1002/mus.24173

Muscle & Nerve

ABSTRACT: Introduction: We investigated the effect of endurance and non-endurance training on peripheral sudomotor sensitivity. Methods: The quantitative sudomotor axon reflex test (QSART) was performed. Results: Endurance-trained subjects (ET, long-distance runners) had a significantly shorter onset time of sweating, greater sweat volume, increased density of activated sweat glands and sweat gland output per single activated gland, greater volume of transepidermal water loss, and higher skin temperature compared with those in the other 2 groups [non-endurance-trained group (NET), sedentary control group (CT)]. NET subjects (baseball players) had a tendency to increase in these variables; thus, some values were greater than control subjects. Conclusions: Our results suggest that endurance training much more effectively modifies sudomotor sensitivity than non-endurance training. Keywords: QSART · acetylcholine · sweat · sudomotor · axon reflex · endurance training

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INTRODUCTION Heat dissipation via sweating is critical for mammalian survival during exercise and under heat conditions. Heat acclimation is characterized by improving the heat dissipation response mechanism, thereby allowing an individual to contain a rise in core temperature within acceptable physiological limits during exercise in a hot environment.1 Physical training increases sweat production, including the density of activated sweat glands (ASG) or cholinergic sensitivity of sweat glands, and sweat gland output (SGO) per single activated gland.2-8 The additional thermal load during exercise that is proportional to the intensity of the exercise results in a higher core temperature. Elevated internal temperature increases sweat rate. Previous studies have demonstrated that endurance training generally enhances sweat rate. However, few studies have compared the effects of endurance and non-endurance training on sudomotor sensitivity. Only Irion investigated whether athletes who train primarily for endurance activities have a better sweat response, as a parameter that explains exercise adaptation to heat, than athletes trained for anaerobic activities.1 However, that study did not show quantitative differences in sudomotor sensitivity. Therefore, we investigated peripheral sweat mechanisms between endurance and non-endurance trained subjects. Sweating is regulated centrally by the preoptic area and anterior hypothalamus of the brain and peripherally by sympathetic postganglionic innervation, where the primary neuro-glandular

transmitter

is

acetylcholine

(ACh).9

ACh

is

the

primary

neurotransmitter released from cholinergic sudomotor nerves and binds to muscarinic receptors on the eccrine sweat gland to evoke sweat secretion.10-13 Peripheral sudomotor axon reflex-mediated (AXR) and directly-activated (DIR) sweating can also occur via 3 John Wiley & Sons, Inc.

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exogenous iontophoretic administration of ACh.14-17 We used the quantitative sudomotor axon reflex test (QSART) to evaluate peripheral sudomotor sensitivity. The QSART measures postganglionic sympathetic C-fiber function by ACh iontophoresis to quantify AXR and DIR sweating. We measured onset time of the axon reflex, AXR and DIR sweat volume, ASG density, SGO per single activated gland, transepidermal water loss (TEWL), and skin temperature on the forearm.

METHODS Participants Following approval of the experimental protocol from the University of Soonchunhyang Institutional Review Board and after obtaining written informed consent, 62 healthy male subjects [endurance-trained group (ET), 5,000–10,000 m runners, n=20; nonendurance-trained group (NET), baseball players, n=17; sedentary control group (CT), n=25] were enrolled in this study. All exercise-trained subjects were athletes playing sports at the university level. They normally participated in exercise training at least 2 h per day, 5 days per week, throughout their career (8–9 years). The CT subjects were students from the same university who had not performed regular physical exercise for at least 2 years before the study. Participants did not consume caffeine, smoke, or consume alcohol 48 h before the test, and refrained from intense physical activities 24 h before the test. The physical and physiological characteristics of the subjects are shown in Table 1. All trained subjects had a significantly greater maximal oxygen uptake than that of control subjects.

Measurements and procedures 4 John Wiley & Sons, Inc.

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Maximum oxygen consumption (VO2max) was determined for each subject during graded treadmill tests by analyzing expired gases (COSMED; Quark Pulmonary Function Testing Lung Volumes Module 2 ergo, Rome, Italy). A Polar monitor (Polar CIC, Port Washington, NY, USA) was used to measure heart rate (HR). The criteria for determining VO2max were that the respiratory exchange ratio was 1.1, VO2 leveled off despite increasing workload, and HR reached the age-predicted maximal value.

Quantitative sudomotor axon reflex test All experiments were performed in a thermoneutral climate chamber (ambient temperature, 24±0.5°C; relative humidity, 40% ± 3%; air velocity, < 1 m/sec) as described above. Upon arrival in the climate chamber, each subject wore light indoor clothing and sat on a chair in a relaxed mood for 60 min before commencing the experiments. The QSART technique has been described previously in detail.14,17-19 The QSART sweat capsule consists of 2 concentric compartments. Ach, placed in the outer compartment, is transported iontophoretically into the skin where it directly stimulates the underlying sweat glands (DIR), while the glands of the skin in the central compartment of the capsule are activated indirectly by an ACh-induced axon reflex (AXR). The DIR response is induced by the action of ACh on the muscarinic receptors of the sweat gland cells. In addition, ACh activates nicotinic receptors of the sudomotor efferent fibers, and the resulting excitation spreading across the sudomotor nerve fiber endings produces the AXR. The AXR response measured during iontophoresis of 10% ACh (Ovisot, Daiichi Pharmaceutical Co., Ltd., Tokyo, Japan) at 2 mA for 5 min was defined as AXR1. After removing the 10% ACh solution from the outer compartment,

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both the DIR of the skin underlying the outer compartment and the AXR response in the central compartment, which was termed AXR2, were measured simultaneously. Two sets of QSART capsules were attached to the volar aspect of the forearm with rubber bands. The outer compartment of capsule 1 was filled with a 10% ACh solution, whereas capsule 2 was held in reserve. Two mA of direct current were applied for 5 min between the electrode in the ACh cell of capsule 1 (anode) and a flexible plate-electrode (cathode; HV-BIGPAD, Omron, Kyoto, Japan) attached to the forearm skin just proximal to the wrist joint. AXR1 sweating was determined in the central compartment of capsule 1 during the 5 min period of ACh iontophoresis. Immediately after stopping the current, capsule 1 was detached, the skin under capsule 1 was wiped dry, the positions of the 2 capsules were swapped, and measurements were continued with capsule 2. These procedures took < 20 sec. Sweating data were acquired up to minute 11 to simultaneously observe DIR and AXR sweating. Sweat production was determined using the capacitance hygrometer-ventilated capsule method.17,20-22 In brief, nitrogen gas was passed through each capsule compartment at a constant flow rate of 0.3 l/min, and the change in relative humidity of the effluent gas was detected with a hygrometer (H211; Technol Seven, Yokohama, Japan). The oral and skin temperatures in the vicinity of capsule 1 were monitored using thermistors (PXK67; Technol Seven) connected to a data logger (K-720; Technol Seven). Sweating rates were fed into a PC (PC9801, NEC, Tokyo, Japan) every 5 sec. The density of ASG was measured using the iodine-impregnated paper method. The iodine-starch paper was then opposed to the skin surface where the ACh was applied. The blue-black pigmented spots in 0.5 × 0.5 cm areas were counted under a microscope in triplicate, and the average sweat gland density (count/cm2) was calculated. SGO per activated single gland 6 John Wiley & Sons, Inc.

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(µg/min/gland) was obtained by dividing the DIR sweating rate (mg·cm−2 min−1) by the ASG density.17,20 TEWL (µg·cm−2·min−1) was measured with tewameter model no. TM 210 (Courage and Khazaka, Cologne Germany) according to the manufacturer’s recommendations and as described in detail by Pinnagoda et al.23 Briefly, the measurement involved placing the device containing a probe on the volar aspect of the forearm skin.17,19

Statistical analysis Values are presented as means ± standard deviations. Statistical significance was assessed by of one-way analysis of variance with the Tukey post-hoc test for comparison of mean values among the 3 groups. A P-value < 0.05 was significant.

RESULTS Skin temperature increased significantly during ACh iontophoresis in all groups (P

Comparison of peripheral sudomotor sensitivity to acetylcholine in endurance and non-endurance trained male subjects.

We investigated the effect of endurance and non-endurance training on peripheral sudomotor sensitivity...
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