Article Text
Abstract
Objective: Several stressors such as cold water immersion, hyperoxic exposure and decompression-induced circulating bubbles can alter arterial circulation after a dive. The aim of this study was to investigate the arterial modifications induced by a specific diving training including repeated hyperbaric exposures and physical training.
Method: Arterial pressure measurement and pulse wave velocity (PWV) recordings were performed in 12 student military divers before and after 15 weeks’ training. The results were compared with the same investigations performed in 12 non-diver healthy subjects.
Results: A decrease in systolic blood pressure and pulse pressure was observed at both upper and lower limbs in student military divers after the training. Non-significant decreases in both carotido-femoral PWV and carotido-pedal PWV were found after the training. When the pulse time transit was divided by the cardiac cycle length between two R peaks ((RR) interval), a significant increase was observed between the carotid and femoral sensors. On the other hand, some differences were noticed between military divers and controls. Controls and divers were matched appropriately according to age and height, although the divers had a higher aerobic capacity as well as lower resting heart rate and lower pulse wave velocity.
Conclusion: In trained military subjects, a training which includes repeated diving exposures and endurance exercises leads to vascular modifications suggesting an increase in central arterial compliance. There was no sign of arterial alteration induced by repeated diving exposures.
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During a dive, subjects undergo environmental stressors such as immersion, ventilation through the SCUBA, cold exposure and increased ambient pressure. All of these stressors may be responsible for changes in arterial peripheral circulation. Immersion in water induces a shift of the peripheral venous blood that increases central blood volume and cardiac output.1 2 This increase in volaemia induces stimulation of arterial baroreceptors. In cold water, peripheral vasoconstriction increases blood translocation. Furthermore, during recreational SCUBA diving, subjects breathe air at high pressure through the regulator. Increased ambient pressure generates an increase in oxygen partial pressure (PO2). Consequently, even in air SCUBA diving, the subjects are exposed to hyperoxia. Numerous studies have demonstrated that cardiovascular responses to acute hyperoxia include a reduction in heart rate and cardiac index and an increase in mean arterial pressure, systemic vascular resistance, and large artery stiffness.3 4 During decompression, the formation of nitrogen bubbles is recognised as the basis for decompression illness but such bubbles are also commonly detected in the venous circulation of asymptomatic divers.5 Experimental studies have demonstrated that circulating bubbles activate leucocytes and platelets, adversely affect blood rheology and induce an activation of the complement system and a release of kinins.6 7 Circulating gas bubbles may damage the vascular endothelium through mechanical effects as well as through activation of leucocytes.8–10
As the result of these different stressors an acute arterial endothelial dysfunction has been demonstrated after a single hyperbaric exposure.11 12
Although it is well recognised that acute exposure leads to peripheral circulation changes, little is known on long-term vascular changes induced by repeated diving exposures. An increase in IL8 suggesting an activation of endothelial cells has been observed after a 2 months’ training diving period.13
French Navy student military divers experience a specific diving training. This training consists of daily SCUBA dives and an endurance physical training including both running and swimming. The aim of this study was to assess the vascular modifications induced by this specific diving training. Our hypothesis was that the stressors experienced by military divers could modify their arterial compliance.
METHODS
All experimental procedures were conducted in accordance with the Declaration of Helsinki, and were approved by the local ethics committee. Each method and the potential risks were explained to the participants in detail and they all gave written informed consent before the experiment. The investigations were performed in the morning in a quiet room with controlled temperature, after 10 h in fasting condition. All subjects refrained from smoking and drinking caffeinated beverages at least 24 h before measurements. Furthermore, volunteers had not dived or exercised for at least 48 h.
Subjects
Twelve male military student divers (age 24 (SD 3) years, height 180 (SD 4) cm) were included in the study. Their physical activity was assessed by a questionnaire. In order to determine individual exercise aptitude, each subject performed an incremental cycle ergometry test using an Excalibur Sport (Medical Technology, Gronigen, Netherland). Gas exchange was measured using a breath-by-breath system (Quark, Pulmonary Function Testing-Exercise testing, ergo, Cosmed, Roma, Italy), which was calibrated before each test. VO2max was defined as the highest value of oxygen uptake despite increased workload. Military divers underwent two cardiovascular examinations, the first one in basal conditions, and the second after 15 weeks of the specific diving training.
This training consisted of daily (once to three times) open sea SCUBA diving. The breathing mixture was air and the decompression procedures were conducted according to the MN 90 Tables. The diving profiles were limited to 20 msw depth at the beginning of the training. Thereafter, student military divers performed dives with maximal depths in the range 50–60 metres sea water (msw). Furthermore, military divers engaged in a physical endurance training including running and swimming with a total duration of 6 h per week.
Twelve healthy male controls (age 24 (SD 3) years, height 178 (SD 5) cm) without regular SCUBA diving activity were studied. They were subjected to the same examinations as the military divers.
Cardiovascular investigations
Investigations were performed in a quiet room with a stable environmental temperature (25–28°C). Subjects remained at rest for 10 min before the examinations. All subjects were investigated in supine position.
Blood pressure measurements
Blood pressure measurements were obtained using an automatic device (Omron HEM-705CP, ORMO HEALTHCARE Company, Japan). This automated device was validated by the British Hypertension Society (BHS) and the Association for the Advancement of Medical Instrumentation (AAMI).14
Two values of systolic (SBP) and diastolic blood pressures (DBP) on the two arms (brachial blood pressure – B BP) and on the two ankles (ankle blood pressure – A BP) were recorded. Blood pressures were similar on the two sides for both upper and lower limbs; consequently the mean of the two values of brachial and ankle blood pressures on the right side was used for the statistical analyses. Pulse pressure (PP) was defined as systolic minus diastolic blood pressure: PP = SAP − SDP. Ankle brachial index was calculated by the ratio of the ankle systolic blood pressure to the brachial systolic blood pressure (A SBP/B SBP).
Pulse wave velocity study
Pulse wave velocity (PWV) which is inversely related to arterial wall distensibility,15 16 was recorded using a Complior device (Complior® SP - ARTECH MEDICAL, Colson Garges-les-Gonnesses, France). The technical characteristics of this device and the measurement method of PWV have been previously described.17 Briefly, PWV is calculated by measuring the pulse transit time (PTT) and the distance travelled by the pulse between two recording sites: PWV = distance (metres)/pulse transit time (seconds). Three transcutaneous sensors were positioned: one at the base of the neck for the right common carotid artery, one over the right femoral artery and one on the right foot over the right pedal artery. Consequently, carotid–femoral PTT and carotid–pedal PTT were recorded. In our study, the same observer performed three successive sequences of measurements on each subject and the mean was used in the statistical analysis. The distances between the different sensors were recorded during the first examination to reproduce exactly the same position before and after the training.
Statistical analysis
Preliminary study: assessment of the reproducibility
In order to assess the reproducibility of the pulse wave velocity recorded by the Complior, a preliminary study was performed.
Special precautions were taken to ensure that the position and the surface distance between the different sensors were similar in military divers before and after the training. Furthermore, the recording of the pulse transit time by the Complior being automatic and as the same investigator performed the whole study, we only assessed the within-observer reproducibility of the pulse transit time.
Two series of measurements were performed on 60 healthy male subjects (age 28 (SD 7) years, height 178 (6) cm and weight 74 (8) kg) with an interval of at least 1 day between the two measurements.
Pearson’s correlation analysis and Bland–Altman plotting were performed in order to assess the reproducibility. The two series of paired measurements were analysed in two steps according to the recommendations of Bland and Altman.18 First, the correlation between measurement values (equation of the linear relationship, correlation coefficient r and p value) was investigated. The first step was used to gauge the degree of agreement between two series of measurements. Secondly, the relative (positive or negative) differences between each pair of measures were plotted against the mean of the pair. Data were analysed using Bland–Altman plots and reproducibility was expressed in terms of the mean difference (SD) between paired measurements. Moreover, previous studies have demonstrated that heart rate changes induced PWV changes. Consequently, reproducibility of the pulse transit time divided by the RRi intervals, recorded during the PWV measurement, was also studied.
Main study
Continuous variables were expressed as mean (SD). Statistical tests were run on Sigma Stat software (SPSS Inc., Chicago, USA). The data distribution was analysed with a Kolmogorov–Smirnov test. Differences were considered significant at p<0.05.
Comparison between divers and controls
For a normal distribution, differences among divers and controls were compared using an unpaired Student t test. In the case of cohorts of variables not having a normal distribution, comparisons were made with the Mann–Whitney test.
Effect of the specific diving training
In the student military divers, a paired t test was employed to investigate the modifications induced by the specific diving training. In the case of cohorts of variables not having a normal distribution, comparisons were done using a Wilcoxon test.
RESULTS
Preliminary study: assessment of the reproducibility
The mean CF PTT was 79 (12) ms (range 58−114) and the mean CP PTT was 192 (31) ms (range 111−274).
The correlation between the two measurements was highly significant for CF PTT (r = 0.91, p<0.001), CP PPTT (r = 0.94, p<0.001), CF PTT/RRi (r = 0.90, p<0.001) and CP PTT/RRi (r = 0.98, p<0.001). The differences between the two different measurements plotted against their mean value according to Bland and Altman are represented in figs 1, 2, 3 and 4.
The within-observer differences were 0.68 (5.30) ms and 0.94 (14.00) ms for CF PTT and CP PTT respectively. Most of the values were within two standard deviations of the mean.
Using PTT/RRi the within observer differences were −0.6 (4.4×10−3) ms and 1.7 (1.03×10−2) ms for CF PTT/RRi and CP PTT/RRi respectively. In only three circumstances for CF PTT/RR, and one for CP PTT/RR, were the differences between measurements outside the limits of agreement.
The mean percentage of the within observer differences was 4.05% for CF PTT, 3.58% for CF PTT/RRi, 4.70% for CP PTT and 2.93% for CP PTT/RRi.
Main study
Military divers and civilian non-diver controls were matched appropriately for age, height, and weight (table 1).
Before the beginning of the specific diving training, student military divers performed various sporting activities such as swimming, running, cycling, or fighting sports. Most of the control subjects engaged in physical activities such as distance running, cycling, swimming or tennis. In total, the duration of the sporting activities performed by military divers was significantly longer than that of the controls (4 (SD 1) h vs 2 (SD 1) h per week; p = 0.02). At peak exercise, maximal values of VO2/weight were significantly higher in military divers than in controls.
During the specific diving training the duration of the sporting activities was significantly increased in student divers (6 h per week; p<0.001). After training a mean weight loss of 1.5 kg was observed in military subjects (p = 0.02).
Heart rate was significantly greater in controls than in student military divers. There was no significant difference in brachial blood pressures (systolic, diastolic or pulse pressure), ankle blood pressures and ankle brachial index between the diver and control groups (table 2). On the other hand, significant decreases in SBP and PP recorded at both brachial and ankle levels were observed in military divers after the training. Diastolic blood pressure and ABI were not modified after the training in comparison with the reference measurement.
Carotido-femoral PWV was significantly higher in controls than in military divers before or after their training. There were no significant differences in carotido-pedal PWV between divers and controls.
In student military divers, a non significant decrease in CF PWV and CP PWV was found after the training. When the PTT was divided by the RRi intervals, a significant increase was found between the carotid and femoral sensors after the training compared with the reference examination. The pulse transit time/RRi between carotidal and pedal sensors was longer after the training but did not reach significance.
DISCUSSION
The specific diving training experienced by student military subjects induced some cardiovascular modifications. A decrease in systolic blood pressure and pulse pressure was observed at both upper and lower limbs. On the other hand, the pulse wave velocity study showed no significant changes after the training.
The reproducibility of the device used in this work was assessed in a preliminary study. The results indicate that PWV measurements were highly reproducible. Furthermore, values for reproducibility accord with those reported by a previous study using the same device.17 Arterial compliance indices such as pulse wave velocity and augmentation index are affected by heart rate.19–22
The mechanism involved in the association between reduction in central arterial compliance and increase in heart rate remains hypothetical.
Sympathetic hyperactivity could be involved in the increase in heart rate. Indeed, previous studies have demonstrated that sympathetic vascular smooth muscle activation promotes a decrease in arterial compliance.23 24
Some authors, however, have shown an increase in PWV when heart rate is increased by cardiac pacing,19 20 22 suggesting that sympathetic activity is not the sole mechanism involved. An alternate hypothesis, the shortening of the time available for recoil, has been suggested to explain the tachycardia-induced vessel stiffening.19 Consequently, it is important to standardise PWV for HR. In our work, changes in the pulse transit time divided by RR intervals (PTT/RRi) have been performed to decrease the influence of the heart rate changes on the PWV recorded in the same subjects before and after the training.
When the reproducibility of the PTT divided by the RR intervals was assessed, the bias remained weak and a decrease in the number of values outside two standard deviations of the mean was observed. Consequently, and as suggested by the Bland–Altman plot (figs 1–4), reproducibility could be slightly improved using this standardisation.
An increase in PTT/RRi was found between carotidal and femoral sensors. This change as well as the pulse pressure decrease both suggested an increase in central arterial compliance.15 25
Previous studies have demonstrated that physical training could modify arterial wall properties. Vascular modifications induced by physical training vary according to the training modalities. Regular endurance exercise increases central arterial compliance,26–28 whereas resistance training has no effect or, rather, decreases it.29–31 The increase in arterial compliance induced by endurance training is attributed to changes in vascular endothelium-derived factors. Indeed, previous studies have observed in endurance-trained men a decrease in plasma concentrations of endothelin-1, a potent vasoconstrictor peptide produced by vascular endothelial cells.31 32 Furthermore, an increase in plasma concentration of NO, the main vasodilator produced by vascular endothelial cells, and an improvement in NO bioavailability have been associated with endurance training.32–34
Consequently, in our work, the increase in central arterial compliance could be linked with the endurance physical training experienced by the military divers.
Previous studies have shown that a single dive can induce acute endothelial alteration.11 12 The exact mechanism is not fully understood, but several stressors experienced by divers, such as cold water immersion, repeated hyperoxic exposures, SCUBA breathing and decompression-induced circulating bubbles, could be involved. In a recent study, Ersson et al13 have found, after a 2 months’ diving training period, an increase in the plasma levels of neutrophil gelatinase-associated lipocalcin and interleukin L8. This suggests an activation of neutrophils and endothelial cells. Consequently, one could hypothesise that repeated dives might generate long-term endothelial alterations. Reduced bioavailability of nitric oxide is an important consequence of endothelial damage and leads to an alteration in arterial compliance. In our work, no sign of endothelial alteration was found, since an increase in central arterial compliance was observed in the student military divers after a 15 weeks’ training period. However, according to the results of the comparative study between student military divers and controls, we had to be careful while interpreting our results. In fact, although controls and divers were matched appropriately according to age and weight, military divers had higher aerobic capacity and both lower resting heart rate and lower pulse wave velocity before training. Furthermore, a high level of fitness is required for physically demanding diving activities such as military or professional diving. Consequently, the specific diving training organised by the French military navy included an endurance physical training. This physical training may have counteracted any diving-related alteration in arterial compliance in the military student diver group. Further studies, including a less physically trained group such as recreational SCUBA divers, should be considered in order to focus on repeated diving exposure effects alone.
What is already known on this topic.
During SCUBA diving, environmental stressors such as water immersion, hyperoxic exposure, hyperbaric exposure and decompression induce acute cardiovascular modifications.
One previous human study has suggested that endothelial alteration could be induced by SCUBA diving.
Therefore, a human study has found activation of endothelial cells after 2 months’ hyperbaric exposure in divers.
A physical endurance programme leads to an increase in arterial compliance.
What this study adds.
Specific diving training including repetitive dives and endurance training lead to a decrease in arterial blood pressure and an increase in central arterial compliance.
These modifications are similar to cardiovascular modifications observed after a physical endurance programme. No sign of arterial alteration was found.
Furthermore, our study demonstrates that the reproducibility of pulse wave velocity (PWV) is improved when the measurement of pulse time transit (PTT) was divided by the corresponding RR interval (RRi).
Acknowledgments
The authors would like to express their gratitude to the military commandment of Saint Mandrier.
REFERENCES
Footnotes
Competing interests: None declared.