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Na⁺ secretion rate increases proportionally more than the Na⁺ reabsorption rate with increases in sweat rate

¹Department of Biology and ²School of Exercise and Nutritional Sciences, San Diego State University, San Diego, California

Submitted 7 April 2008 ; accepted in final form 18 July 2008

	ABSTRACT

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The purpose of this study was to measure the in vivo Na⁺ secretion and Na⁺ reabsorption rates of the human eccrine sweat gland with increases in sweat rate. Such data should help to elucidate the physiological mechanism responsible for the previously reported linear relationship between increases in sweat rate and Na⁺ concentration in sweat. On 5 days, each subject (n = 10) completed a 30-min exercise bout in an environmental chamber set at 35°C and 40% relative humidity. The intensity for the five exercise bouts in the heat was set to approximate 50, 60, 70, 80, and 90% of age-predicted maximum heart rate. Forearm sweat samples and capillary blood samples were collected during each of the five 30-min exercise bouts. The sweat and blood samples were analyzed for Na⁺ concentration in sweat and serum, which were used to calculate the rate of Na⁺ secretion and Na⁺ reabsorption. The mean correlation between sweat rate and Na⁺ concentration in sweat was found to be r = 0.73. Within the sweat rate range of the present study, both Na⁺ secretion rate and Na⁺ reabsorption rate increased linearly; however, the Na⁺ secretion rate increased almost twice as fast (slope = 141 vs. 80). Thus the rate at which Na⁺ escaped reabsorption increased with increases in sweat rate and was significantly (P < 0.05) correlated to the Na⁺ concentration in sweat (mean r = 0.90). Such results strongly suggest that the physiological mechanism responsible for the previously reported linear increase in Na⁺ concentration in sweat seen with increases in sweat rate is that the Na⁺ secretion rate increases proportionally more than the Na⁺ reabsorption rate.

sodium reabsorption; sodium secretion; eccrine sweat gland; sweat sodium concentration

Most previous studies (1, 2, 4, 11, 15, 32) have shown that the Na⁺ concentration in sweat ([Na⁺]_sweat) increases linearly with increases in sweat rate. For example, Inoue et al. (11) reported significant positive correlations (r = 0.67–0.98) between local sweat rate and [Na⁺]_sweat measured on the chest, back, forearm, and thigh. Over the years, three different physiological mechanisms have been proposed in the literature to explain this relationship. Taylor (30) hypothesized that increases in sweat rate will increase [Na⁺]_sweat because of a reduction in ductal Na⁺ reabsorption. Next, several investigators (2, 4, 22, 27) suggested that Na⁺ reabsorption has a maximum limit that becomes saturated with increases in sweat rate, thus causing an increase in [Na⁺]_sweat. Finally, it has been proposed that with increases in sweat rate the sweat Na⁺ reabsorption rate increases proportionally less than the Na⁺ secretion rate, thus resulting in an elevated [Na⁺]_sweat (11, 16). Therefore, depending on the reference chosen, it could be argued that increases in sweat rate will cause the Na⁺ reabsorption rate to either 1) decrease, 2) become saturated and thus demonstrate a plateau effect, or 3) increase. However, such data have not been previously measured in the human eccrine sweat gland. Thus the purpose of this study was to measure the in vivo sweat Na⁺ secretion and reabsorption rates with increasing sweat rates. Such data should help to elucidate the physiological mechanism responsible for the previously reported linear relationship between increases in sweat rate and [Na⁺]_sweat.

	METHODS

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The subjects for the study were 10 healthy volunteers (4 men and 6 women). They had a mean ± SE age, height, weight, and body surface area of 25 ± 1 yr, 168.7 ± 2.4 cm, 66.5 ± 3.6 kg, and 1.76 ± 0.06 m², respectively. The subjects were recruited from the San Diego area using posted flyers and via word of mouth. They were all recreationally active; however, none was formally heat acclimated. They were instructed to refrain from initiating new exercise programs during the duration of the study. No restrictions were placed on their diet; however, the subjects were asked to report to the laboratory well hydrated and to not have exercised in the preceding 12 h. The study was approved by the San Diego State University Institutional Review Board, and written informed consent was obtained from each subject before participation in the study.

On 5 days, during a 2-wk period of time, each subject completed a 30-min exercise bout in an environmental chamber set at 35°C and 40% relative humidity. Before each exercise bout the subject's urinary specific gravity was measured and had to be <1.028 to ensure that they were not dehydrated before the start of each trial. This was done because dehydration is known to affect [Na⁺]_sweat (15). In addition, water was allowed ad libitum during each of the five exercise trials. The intensity for the five exercise bouts in the heat was set to approximate 50, 60, 70, 80, and 90% of age-predicted maximum heart rate (220 minus age). The absolute workloads were not critical and were simply designed to produce various sweat rates, ranging from very low to very high, from each of the subjects. Heart rate was continuously measured during exercise using a Polar heart rate monitor. The order of the five exercise bouts was randomly assigned for all subjects.

Forearm sweat samples were collected for 20 min (from minute 10 to minute 30) during each of the five 30-min exercise bouts using macroduct sweat collectors (Wescor, Logan, UT). This protocol was designed to allow the subjects to start sweating before the initiation of sweat collection and has been successfully used in the past (25). The collectors were placed on the flexor surface of the proximal forearm and were held in place by a Velcro strap that prevented leakage and sample contamination. The collection site was identified so that the macroduct could be placed at the same location for all trials. The skin was cleaned with deionized water and dried immediately before securing each collector. Forearm sweat rate, for the approximate 5-cm² area under the macroduct sweat collector, was calculated by the change in volume within the sample collection tubing and expressed in milligrams per square centimeter per minute. Following collection into the sample tubing, sweat was expressed into a test tube using a positive-pressure air bellows and stored frozen for later analysis. The sweat samples were analyzed, in duplicate, for [Na⁺]_sweat using a calibrated flame photometer (Cole-Palmer, Chicago, IL).

Blood samples were collected from free-flowing fingertip punctures at minute 20 of each exercise bout. They were allowed to clot and centrifuged for 10 min to obtain samples that were analyzed for Na⁺ concentration in serum ([Na⁺]_serum) using flame photometry.

Because it has been previously shown (5, 24, 25) that precursor sweat is isosmotic to serum and that Na⁺ concentration of precursor sweat is independent of sweat rate (24), the Na⁺ secretion rate, expressed in nanomoles per square centimeter per minute, was calculated as the product of sweat rate and [Na⁺]_serum. Ductal Na⁺ reabsorption rate, expressed in nanomoles per square centimeter per minute, was calculated according to the following formula developed by Sato (23):

Last, the rate at which Na⁺ escaped reabsorption was calculated as the difference between the Na⁺ secretion rate minus the Na⁺ reabsorption rate.

For the previously mentioned dependent variables, Pearson product-moment correlations were calculated for each subject and the mean r was the average of the 10 values. A two x five repeated-measures ANOVA was used to compare mean Na⁺ secretion vs. reabsorption data, while a one-way repeated-measures ANOVA was used to analyze the mean relative Na⁺ reabsorption rate data. Post hoc analyses were conducted using dependent t-tests and were adjusted using the Bonferonni correction. Overall significance was set at the P < 0.05 level.

	RESULTS

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In agreement with numerous past studies (1, 2, 4, 11, 14, 27, 32) the results showed that within the range studied there was a significant linear relationship between sweat rate and [Na⁺]_sweat. There were no differences in responses between men and women; thus all data were grouped together. As can be seen in Fig. 1 the mean r was 0.73. At the lowest sweat rate, the mean ± SE [Na⁺]_sweat was 19 ± 5 mmol/l, whereas at the highest sweat rate it increased to 59 ± 10 mmol/l. These values are similar in magnitude to other studies that sampled sweat locally (1, 2, 4). Figure 2 shows that the rate at which Na⁺ was secreted into the coil and the Na⁺ reabsorption rate during passage of sweat down the distal duct of the eccrine gland both increased linearly with increases in sweat rate. However, the Na⁺ secretion rate increased significantly faster, as evidenced by a significant interaction (P < 0.05) and by having a slope that was almost twice as great (141 vs. 80) as the Na⁺ reabsorption rate. Conversely, as shown in Fig. 3, the mean relative Na⁺ reabsorption rate, expressed as a percentage of Na⁺ secreted during precursor sweat formation, decreased significantly with increases in sweat rate. Specifically, 86 ± 3% of the secreted Na⁺ was reabsorbed at the lowest sweat rate, and this decreased to 65 ± 6% at the highest sweat rate.

View larger version (7K): [in this window] [in a new window]   Fig. 1. Sweat sodium ion concentration vs. sweat rate relationship. Values are means ± SE for 10 subjects. The mean r for the group was 0.73 (P < 0.05). y = 59.7(x) + 6.7. Sweat rate in mg·cm–2·min–1 can be converted to g·m–2·min–1 by multiplying by 10.

View larger version (13K): [in this window] [in a new window]   Fig. 2. Rates of sodium ion secretion during precursor sweat formation and sodium ion reabsorption from the distal duct vs. sweat rate relationships. Values are means ± SE for 10 subjects. Na+ secretion = 140.9(x) – 1.1. Na+ reabsorption = 79.9(x) + 8.4. There was a significant (P < 0.05) interaction between the 2 relationships. *Significant (P < 0.05) difference between the rate of Na+ secretion and reabsorption at that sweat rate.

View larger version (8K): [in this window] [in a new window]   Fig. 3. Mean ± SE sodium ion reabsorption expressed as a percentage of Na+ secretion for the 10 subjects. *Value was significantly (P < 0.05) different than value obtained at the lowest sweat rate.

View larger version (8K): [in this window] [in a new window]   Fig. 4. Rate of Na+ escaping reabsorption vs. the sweat sodium ion concentration relationship. Values are means ± SE for 10 subjects. The mean r for the group was 0.90 (P < 0.05). y·16(x) + 16.

	DISCUSSION

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It could be argued that possibly the sweat rates attained with the present study were not large enough and thus failed to elicit a plateau effect in Na⁺ reabsoption. However, the mean forearm sweat rate produced by the most intense workload (i.e., 90% of maximal heart rate) in the present study (0.82 mg·cm^–2·min^–1) was similar in magnitude to previous results that were produced by exercise in the heat or maximal pharmacological stimulation (5, 8, 10, 18, 19). For example, Gonzalez et al. (10) reported a mean forearm sweat rate of 0.75 mg·cm^–2·min^–1 in six healthy men during exercise in a hot (40°C) humid (90% relative humidity) environment that produced a mean esophageal temperature of 38.9°C. In addition, Crandall et al. (8) reported that pharmacological-induced maximal forearm sweat rate was 0.63 mg·cm^–2·min^–1. Thus lower than expected forearm sweat rates do not seem to be the likely cause for not observing a plateau in the Na⁺ reabsorption vs. sweat rate relationship data presented in Fig. 2.

Rather the present data suggest that within the range of sweat rates studied, the absolute rate of Na⁺ reabsorption from the distal duct increases continuously with increases in sweat rate. However, when expressed as a relative percentage of Na⁺ secretion, it decreases with increases in sweat rate. Specifically, Fig. 2 shows that the absolute rate of Na⁺ reabsorption at the highest sweat rate was almost three times that seen during the lowest sweat rate (77 vs. 29 nmol·cm^–2·min^–1). However, as can be seen in Fig. 3, at the lowest sweat rate 86 ± 3% of the Na⁺ secreted during precursor sweat formation were able to be reabsorbed during passage along the distal duct of the eccrine gland. This value was significantly reduced to 65 ± 6% at the highest sweat rate. Such data clearly show that the faster the precursor sweat travels along the distal duct (i.e., the greater the sweat rate) the smaller the percentage of total Na⁺ secreted that can be reabsorbed. This decrease in relative Na⁺ reabsorption with increases in sweat rate could be the result of a number of factors, including decreased contact time of the fluid column with the luminal membrane of the distal duct, a decreased lumen-intracellular diffusion gradient, and/or saturation of various transport proteins. An alternate mechanism may involve the fact that decreases in the cytoplasmic pH have been shown (6) to reduce the activity of the amiloride-sensitive epithelium Na⁺ channel (ENaC), which is the primary luminal path used for ductal Na⁺ reabsorption. Because glycolysis appears to be the predominate way that eccrine sweat glands resynthesize ATP (23), it is not unreasonable to hypothesize that the cytosolic pH could decrease with increases in sweat rate, thus reducing ENaC activity. Such a scenario could explain the decreased relative Na⁺ reabsorption vs. sweat rate relationship seen in the present study. Interestingly, the mean relative Na⁺ reabsorption data presented in Fig. 3 are quantitatively similar to the in vitro results presented by Mangos (13) collected using isolated human distal ducts. He reported that following microperfusion at a rate approximately equivalent to a sweat rate of 0.5 mg·cm^–2·min^–1 with an isotonic solution containing 145 mmol/l of Na⁺, that the mean relative Na⁺ reabsorption was 77%. This agrees quite favorably with the results of the present study presented in Fig. 3.

Theoretically, the difference between the rate of Na⁺ secretion and the rate of Na⁺ reabsorption, or the rate at which Na⁺ escaped reabsorption, should be highly related to the [Na⁺]_sweat. As can be seen in Fig. 4, these two variables were linearly related and had a mean r of 0.90. Thus the more Na⁺ that escaped reabsorption during passage along the distal duct the higher the mean [Na⁺]_sweat. Interestingly, as can be seen by examining the x- and y-axis, the rate of Na⁺ escaping reabsorption increased about sixfold, whereas the [Na⁺]_sweat only increased about twofold. At first glance this seems illogical; however, it must be remembered that during the same time the sweat rate also increased threefold. Thus a sixfold increase in Na⁺ escaping reabsorption should only increase the [Na⁺]_sweat about twofold, if the sweat rate simultaneously increased threefold.

There are three assumptions that were made in the present study that need to be further addressed. First, it was assumed that the measured [Na⁺]_serum provides a valid measure of the precursor [Na⁺]_sweat. The support for this assumption is based on the fact that numerous previous studies, using three different techniques, have all shown that precursor sweat is isosmotic to serum. Specifically, Sato and Dobson (25) using the backward extrapolation technique reported that the mean ± SE precursor [Na⁺]_sweat in the forearm of 14 healthy volunteers was 140 ± 1.8 mmol/l. Additionally, precursor sweat samples collected directly from the secretory coil were shown to be isosmotic to serum (24), having a mean Na⁺ concentration of 142 mmol/l. Finally, sweat samples collected following the application of amiloride, which selectively inhibits Na⁺ reabsorption from the distal duct, were isosmotic to serum (20). Taken together these three studies clearly support the validity of using [Na⁺]_serum as a surrogate for precursor [Na⁺]_sweat.

The second assumption made in the present study was that following reabsoption from the distal duct, Na⁺ have little, if any, backdiffusion. Theoretically, this seems defensible since in the human eccrine sweat gland the ENaC is only expressed in the luminal membrane, whereas the ouabain-sensitive Na⁺-K⁺ ATPase is localized to the basolateral membrane (21, 23). Furthermore, the one study (13) that has directly measured Na⁺ backdiffusion using radioactive ²²Na reported that at sweat rates comparable with those reported in the present study only 8% of the reabsorbed Na⁺ reentered the distal duct via backdiffusion, presumably via a paracellular pathway.

The third assumption was that leaching of Na⁺ from the stratum corneum into the collected sweat sample was minimal. Because it has been previously shown (7, 9, 19) that K⁺ concentration in sweat stays relatively constant, regardless of sweat rate, Weschler (31) has recommended comparing K⁺ concentration in sweat vs. serum as an indicator of potential leaching. In the present study, 18 randomly selected paired sweat and serum samples were analyzed for K⁺ concentration using flame photometry. The mean K⁺ concentrations in sweat and. serum were both 5.1 mmol/l. These data strongly suggest that leaching of Na⁺ was negligible in the current study.

In conclusion, the results of the present study provide insight into the physiological mechanism responsible of the well documented increase in [Na⁺]_sweat with increasing sweat rates. The results show that within the sweat rate range of the current study the absolute rates of both Na⁺ secretion and Na⁺ reabsorption increase linearly with increases in sweat rate. However, Na⁺ secretion increases proportionally faster, thus, the rate at which Na⁺ escape reabsorption during passage along the distal duct of the sweat gland increases at higher sweat rates. Lastly, the rate of Na⁺ escaping reabsorption was linearly related to the [Na⁺]_sweat. Such data strongly support that with increasing sweat rates, the rate of Na⁺ secretion during precursor sweat formation increases faster than Na⁺ reabsorption in the distal duct. This difference allows for a greater percentage of the secreted Na⁺ to escape reabsorption, thus causing [Na⁺]_sweat to increase.

	FOOTNOTES

 

Address for reprint requests and other correspondence: M. J. Buono, San Diego State Univ., Mail Code 7251, San Diego, CA 92182-7251 (e-mail: mbuono{at}mail.sdsu.edu)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

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This Article Abstract Full Text (PDF) Free All Versions of this Article: 105/4/1044    most recent 90503.2008v1 Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Buono, M. J. Articles by Wong, J. Search for Related Content PubMed PubMed Citation Articles by Buono, M. J. Articles by Wong, J.