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Sodium Regulating Hormones at High Altitude: Basal and Post-Exercise Levels¹

Institute of Semeiotica Medica, Sport Medicine Unit (M.Z., S.R., M.V., G.O.), University of Padua, Padua; Division of Cardiology (D.N.), USL 13 Mirano, Italy

Address correspondence and requests for reprints to: Prof. M. Zaccaria, Sport Medicine Unit, Institute of Semeiotica Medica, Via Ospedale Civile, 105, 35123 Padua, Italy.

	Abstract

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High altitude (HA)-induced diuresis is associated with marked changes in sodium and water regulating hormones, particularly the renin-angiotensin-aldosterone system (RAAS) and atrial natriuretic hormone (ANH). These hormones are also strongly stimulated by physical exercise, which is a major component of daily activity at HA. In spite of the numerous studies in literature, a clear relationship between hormonal changes, HA diuresis, and physical exercise has not yet been established. We therefore evaluated the response of sodium regulating hormones to exhaustive exercise in a group of seven males exposed to prolonged HA hypoxia. The study was divided into four phases: sea level (SL1), after 7 (P1) and after 21 (P2) days at 5050 m (Italian National Research Council Pyramid Laboratory, Nepal), and back at sea level (SL2). At each phase plasma hematocrit (Ht), total body water (TBW), 24-hr sodium excretion (uNa), and urinary volume (uV) were evaluated together with PRA, plasma aldosterone, and ANH, in samples drawn basally from patients in upright position, and at the end of graded step-wise (30 W/2 min) maximal exercise.

Levels of uNa and uV were raised at P1 and then declined at P2, with a parallel decrease in TBW and an increase in Ht. Basal PRA and aldosterone levels were suppressed both at P1 and P2 (from 1.9 ± 0.4 to 0.08 ± 0.03 and 0.5 ± 0.1 ng/mL/3 h, and from 7.9 ± 1.8 to 3.9 ± 0.4 and 4.5 ± 0.4 ng/dL, respectively; P < .05). Exhaustive exercise at HA did not induce any significant response in PRA and aldosterone, unlike SL1. Otherwise, at P1 ANH levels remained unchanged both basally and during exercise, while at P2 they decreased significantlyvs. SL1, both basally and after exercise (from 13.3 ± 5.7 to 3.5 ± 1.2 and from 40.2 ± 10.2 to 17.5 ± 8.3, respectively; P < .05).

Our data show that PRA and aldosterone levels were constantly suppressed at HA and were unresponsive to exercise, whereas the ANH response was significantly stimulated during acute HA exposure, but not during chronic exposure. This suggests that hypoxia-induced chemoreceptor stimulation may cause the natriuretic phenomenon through direct suppression of the RAAS.

	Introduction

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EXPOSURE to high altitude (HA) hypoxia increases sodium and water diuresis, bringing about a depletion of circulating volume and a relative increase in hematocrit (Ht) to counterbalance the reduced supply of oxygen to peripheral tissues.

The mechanism underlying the natriuretic and diuretic effect of hypoxia is not yet well understood. Studies in hypobaric chambers, or using pharmacological agents such as almitrine (1, 2), suggest that hypoxic stimulation of peripheral arterial chemoreceptors is the main drive for HA sodium and water diuresis, while changes in renal perfusion pressure and the glomerular filtration rate seem to be less important (3, 4, 5, 6, 7).

Although differences in experimental conditions probably explain the contradictory data in literature on the hormonal control of sodium and water at HA, most of the studies available show a decrease in sodium retaining hormones, particularly renin-angiotensin-aldosterone system (RAAS) (8, 9, 10). On the other hand, atrial natriuretic hormone (ANH) levels have been found to be unchanged (11) or increased (12), mainly in subjects with acute mountain sickness (13).

Hormones involved in water and sodium balance are also markedly influenced by physical exercise, and in general by stressor activity, which acts as a potent stimulator both for sodium retaining hormones, such as renin or aldosterone, and for sodiuretic hormones, such as ANH (14, 15, 16, 17). However, this pattern has not been observed in the majority of known physiological situations, such as posture, dehydration, or changes in sodium intake, in which RAAS variations are followed by opposite ANH changes (18). Several studies, performed in a hypoxic environment to investigate the relationship between physical exercise and ANH secretion obtained different results, particularly during acute exposure. Likewise, contradictory results have also been reported for the relationship between ANH and RAAS responses during exercise (19, 20).

To further clarify these aspects, and to evaluate HA sodium and water balance and the role of its related hormones, we investigated a group of male climbers, in basal conditions and after exercise, before, during, and after a three-week period of residing at 5040 m.

	Subjects and Methods

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Seven healthy male trained volunteers (aged 24.5 ± 0.6 yr) participated in the study after giving their informed consent. The research was part of the Italian high altitude project, EV-K²-CNR. All subjects flew from Kathmandu (1, 300 m, Nepal) to Lukla (2, 866 m) and than trekked for 5 days until reaching an altitude of 5,050 m (Pyramid Laboratory of Italian Research Council). They underwent an incremental exhaustive exercise test (30W/2 min) by bicycle-ergometer at sea level (SL1), at 1 (P1), and at 4 (P2) weeks after their arrival at HA, and again at sea level between the 10th and 14th day after leaving the Pyramid Laboratory (SL2). In the period from P1 to P2 six of the subjects climbed Mount Pumori (7, 135 m), while the last one remained in the laboratory, carrying out a regular daily activity. During the high altitude expedition, the subjects were on free sodium and water diet.

Subjects underwent tests at the same time in the morning: sea level tests were performed in the laboratory of the Sport Medicine Unit of the University of Padua (12 m; 760 Torr), while HA tests were performed in the Pyramid laboratory (5,050 m; 409 Torr), of the Italian National Research Council (CNR) on the Lobuche tableland (Nepal).

In each phase, total body water (TBW) was determined using the bioelectric impedance method (BIA 101 RJL/Akern Systems, Detroit, MI), already proven to be reliable for this purpose (21). Blood samples were obtained before exercise, at the end of exercise, and after a 15-min recovery period, being drawn from an antecubital vein, kept open by continuous saline infusion, for the measurement of PRA, aldosterone, ANH, ACTH, cortisol, electrolytes, and Ht. Basal samples were collected after subjects had been sitting in a quiet room for 3 h in similar environmental conditions. On the day before exercise, samples were also taken for the measurement of 24-h diuresis and urinary electrolytes, aldosterone, and cortisol. After collection, plasma and urine samples were stored frozen at -70 C when at sea level and at -20 C when at HA, until the return to sea level.

All hormonal assays were performed using commercial RIA kits, except for ANH, which was assayed by RIA (Peninsula/Technogenetics) (normal values: supine 25 ± 12 pg/mL, upright 16 ± 7 pg/mL) in extracted plasma, as described in detail elsewhere (22). Ht values were determined by standard laboratory techniques both at sea level and high altitude.

The data are presented as mean ± SE. A two-way ANOVA analysis was performed. All comparisons were based on a confidence level of at least 95% or more (P < 0.05).

	Results

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Water-sodium balance

Urinary volume and sodium concentrations markedly increased during the acute phase (P1) of HA exposure (from 1064 ± 129.4 at SL1 to 2450 ± 255 mL/24 h at P1; P < 0.05, and from 166.8 ± 34 to 427.8 ± 46 mEq/24 h; P < 0.05, respectively); after acclimatization (P2) the increase was less evident (1655 ± 235 mL/24 h and 257 ± 34, 8 mEq/24 h), and similar values were maintained after the subjects returned to sea level (SL2) (1685 ± 232 mL/24 h and 228 ± 33.7 mEq/24 h) (Table 1).

Finally, body weight showed a progressive decrease (from 71.8 ± 2 on SL1 to 70.3 ± 1.8 Kg at P1), reaching a significant value at P2 (67.3 ± 1.5 kg; P < 0.05), while at SL2 the loss was partially regained (69.9 ± 1.6 kg) (Table 1).

Hormones

PRA and aldosterone were significantly suppressed during permanence at HA (Fig. 1) basal PRA values falling from 1.9 ± 0.4 at SL1 to 0.08 ± 0.03 at P1, and to 0.51 ± 0.1 ng/dL/3 h at P2 (P < 0.005). These variations were paralleled by similar variations in both plasma (from 7.9 ± 1.8 to 3.9 ± 0.4 at P1 and 4.5 ± 0.4 ng/dL at P2; P < 0.005) (Fig. 1) and urinary aldosterone (from 11.4 ± 1.2 at SL1 to 5.7 ± 0.4 at P1 and 5.5 ± 0.77 µg/24 h at P2; P < 0.005) (Table 1). At SL2, both PRA and aldosterone plasma levels returned to values similar to those found at SL1 (3.08 ± 0.5 ng/dL/3 h and 7.9 ± 1 ng/dL, respectively) (Fig. 1).

View larger version (32K): [in this window] [in a new window]   Figure 1. PRA, aldosterone, and ANH in seven subjects at sea level (SL1), after one (P1) and three weeks (P2) of high altitude exposure, and again at sea level after exposure (SL2). The hormones were evaluated basally (B), at the end (E) of maximal exercise, and after 15 min of recovery period (R). * P < .05 vs. basal values (0); § P < .05 vs. SL1.

On the other hand, plasma ACTH and cortisol showed an increasing trend at P1 (from 17.5 ± 1.9 to 30 ± 10 pg/ml; P < 0.05, and from 9.1 ± 1.3 to 13.4 ± 1.5 µg/dL, respectively) (Fig. 2), while a significant increase was observed only for urinary cortisol (from 46.7 ± 8.9 to 82 ± 6.9 µg/24 h; P < 0.05) (Table 1).

View larger version (51K): [in this window] [in a new window]   Figure 2. Plasma ACTH and cortisol in seven subjects at sea level (SL1), after one (P1) and three weeks (P2) of high altitude exposure, and again at sea level after exposure (SL2). The hormones were evaluated basally (B), at the end(E), and after 15 min of recovery period (R). * P < .05 vs. basal values (0); § P < .05 vs. SL1.

Total work capacity (TWC), measured as kgm, was significantly reduced at HA, decreasing from 19967 ± 415 to 11295 ± 761 at P1 (P < 0.01) and to 11945 ± 708 kgm at P2 (P < 0.01), and then being completely restored at SL2 (18467 ± 798 kgm) (Fig. 3).

View larger version (44K): [in this window] [in a new window]   Figure 3. Total work capacity (measured in Kgm) in seven subjects during the different phases of the study (see Materials and Methods). * P < .05 vs. SL1.

At HA, there was neither PRA (0.56 ± 0.14 at P1 and 1.29 ± 0.3 mg/mL/3 h at P2) nor aldosterone (and 5.4 ± 0.6 at P1 and 7.3 ± 1.2 ng/mL at P2) response to exercise. ANH levels showed a normal response to exercise at P1 (35.4 ± 10.8 pg/mL; P < 0.05), but during chronic HA exposure (P2) this response was not significant (17.5 ± 8.3 pg/ml; P = ns). At SL2, response to exercise was restored for all hormones (Fig. 1).

To rule out effects of the physiological work capacity reduction on hormonal secretion observed during hypoxia (23), we calculated the ratio between TWC and hormonal response (peak-basal level) (Fig. 4). At sea level, an increase of 1 ng/dl of aldosterone requires a work capacity of 1650 ± 221 Kgm. At HA a 3 to 5 fold increase in TWC would be required to obtain the same response from aldosterone and PRA observed at sea level. A different pattern was observed in the case of ANH, the ratio being reduced at P1, thus indicating that ANH was more responsive to physical exercise, while the 3-fold increase in the ratio at P2, due to the great interindividual variability, was not significant.

View larger version (27K): [in this window] [in a new window]   Figure 4. Ratio between TWC (Kgm) and hormonal response (peak-basal level). Ratio values are inversely proportional to the stimulability of the hormone to physical exercise. * P < .05 vs. SL1.

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Natriuresis and diuresis are the more important homeostatic mechanisms in the water and salt balance acquired during HA exposure, and a failure in these mechanisms has a pathogenic role in HA related disorders (24).

Our findings confirm that during the first phase of acclimatization there is an increase in water and sodium excretion together with Ht. In our study protocol it was extremely difficult to achieve an accurate control of water and sodium intake, since subjects climbed Mount Pumori in the period between P1 and P2. We cannot rule out an effect from an unbalanced water and sodium intake. However, at HA there was a constant decrease in TBW without any significant variation in free water clearance (25), thus suggesting that diuresis was not consequent to an increased water intake. This finding is in agreement with those in other studies performed in animals in hypoxic conditions, which showed a reduction in voluntary water and sodium intake (1, 26), and in climbers in whom it was observed that dietary manipulations do not prevent water loss (27). On the other hand, it has been shown that renal flow and glomerular filtration rate are not changed at altitude, suggesting that HA diuresis and natriuresis depend mainly on the effect of hormonal factors on renal tubules (26).

The main finding of our study was that HA exposure induces not only a marked decrease in resting PRA and aldosterone concentrations but also a suppression of their response to exhaustive exercise. Moreover, during acute HA exposure, resting and post-exercise ANH concentrations were similar to those found at sea level, while during chronic HA exposure the ANH response to exercise was less pronounced.

In our subjects, urinary sodium and volume were significantly higher only in the first week at P1, while at P2 they returned to sea level values, despite a further decrease in TBW and an increase in the hematocrit. Thus, during acute HA exposure the marked suppression of PRA and aldosterone was associated with an increase in water and sodium excretion; RAAS suppression, unlike diuresis, lasted throughout HA exposure, indicating that hypoxia kept the system in a low grade of activity also when a new fluid and salt equilibrium was achieved. So this effect may be useful in preventing sodium retention, which is potentially dangerous for the organism in these conditions. This hypothesis is supported by the observation that RAAS is constantly inhibited also during maximal exercise.

It is known that physical exercise powerfully stimulates both PRA and aldosterone secretion, probably by the activation of catecholamines and ACTH and by fluid loss, linked to the increased body temperature (18, 28, 29). In our subjects, maximal exercise activated RAAS at sea level, before and after HA exposure, but it failed to do so in hypoxic conditions, in which PRA remained suppressed and aldosterone levels did not increase. These data only partially agree with those of other authors who show that PRA increases during exercise both during acute and chronic HA exposure (29, 30) or that there is a dissociated response between PRA and aldosterone (19, 20, 30); other authors suggest that there may be a possible reduction in the adrenal response to angiotensin or, alternatively, a reduced ACE activity (8). We found that PRA and aldosterone were inhibited in a similar manner, and it is reasonable to assume that HA hypoxia might exert a similar suppression in all components of RAAS. Our findings do not confirm that ACTH modulates aldosterone secretion in hypoxia, as suggested elsewhere (10). In fact, we found that at HA, despite aldosterone suppression, cortisol was significantly increased by exercise.

Other factors that may influence RAAS at HA are the changes in work capacity or in sympathoadrenergic activity. The latter, a well-known stimulator of renin secretion (29), has been shown to increase during HA hypoxia exposure (31). Moreover, a relationship between PRA response and work performed by exercise has also been observed (29). As work capacity was reduced at HA, we calculated the ratio between TWC and hormonal response to exercise to see whether RAAS suppression was simply caused by this phenomenon, and we observed a lack of PRA and aldosterone response even for the same working load that was able to stimulate a clear-cut response at sea level. These findings support the idea that the suppression of RAAS is an important primary event occurring early after exposure to HA, and it may explain HA natriuresis and diuresis.

In spite of preliminary reports showing an increase in ANH at HA (12) and suggesting it may play a pivotal role in altitude-induced natriuresis (30, 32, 33), it was recently demonstrated that ANH increase is present mainly in subjects with AMS (11, 13). It has been therefore pointed out that ANH may be triggered in pathological conditions in which natriuresis is impaired (18).

Despite a reduction in PRA and aldosterone, in our subjects mean ANH basal values did not significantly change at P1. However, the high interindividual variability observed by us at resting conditions was attenuated by maximal exercise, which put all subjects in a more reproducible situation: ANH values were significantly stimulated by maximal exercise at P1 but not at P2.

Although obtained in different experimental conditions, the data of Rock et al. (32) show a similar ANH pattern without a contemporary RAAS suppression. Other studies have shown no changes or small increases in ANH responses to hypoxic exercise, suggesting that hypoxia can influence ANH and aldosterone in a similar manner (16, 20, 31, 32, 33, 34).

We believe that the different ANH response is an adjunctive control mechanism that can play a role mainly in the first phase of acclimatization. ANH may play also a role in the regulation of altitude water balance during physical exercise. This suggestion is also confirmed by the reduction in its responsiveness during chronic exposure to HA, when the diuretic-natriuretic mechanism loses its central importance in the regulation of adaptive mechanisms to hypoxia. In this phase, ANH secretion may reflect the reduction in cardiac atrial diameters consequent to a decreased circulating volume (35).

In conclusion, our study confirms the importance of the hormonal mechanism in mediating altitude-diuresis and altitude-natriuresis. In particular, hormones related to sodium and water balance showed a different regulation, depending on the particular phase of HA exposure: the most impressive event was the profound suppression of the renin-angiotensin-aldosterone system found by us also after maximal exercise whereas, at least in the acute phase, ANH is not reduced and remains responsive to hypoxic exercise.

Although an interplay with other unknown factors cannot currently be ruled out, our data support the idea that hypoxia-induced chemoreceptor stimulation causes the natriuretic phenomenon through the direct suppression of RAAS.

	Acknowledgments

 
Authors wish to thank the six climbers of "Scoiattoli di Cortina" for making the study possible, and as well as Dr. A. Ponchia for ascertaining contributions of experience and ability. Moreover the excellent technical assistance given by A. Daniele and C. Centobene is gratefully acknowledged.

	Footnotes

 
¹ This work was supported by CNR Grants N. 92.04642.ST74 and N. 92.007230CT04, and by the President of the Veneto Region.

Received April 30, 1997.

Revised October 20, 1997.

Accepted October 30, 1997.

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This Article Abstract Full Text (PDF) Submit a related Letter to the Editor 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 PubMed Alert me to new issues of the journal Download to citation manager Request Copyright Permission Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Zaccaria, M. Articles by Opocher, G. Search for Related Content PubMed PubMed Citation Articles by Zaccaria, M. Articles by Opocher, G.