changes in cardiac rhythm in man during underwater submersion and swimming studied by ecg telemetry

Eur J Appl Physiol (1993) 66:43-48 European Applied Journal of

Physiology and Occupational Physiology @ Springer-Verlag 1993

Changes in cardiac rhythm in man during underwater submersion and swimming studied by ECG telemetry

Hisao Yamaguchi, Hiroyuki Tanaka, Shigeru Obara, Shingo Tanabe, Noboru Utsuyama, Akira Takahashi, Jun Nakahira, Yoshihiko Yamamoto, Zhen-Lin Jiang, Jufang He, Eizo Bando, and Hiroshi Miyamoto

Department of Physiology, School of Medicine, The University of Tokushima, Kuramoto-cho, Tokushima 770, Japan

Accepted August 19, 1992

Summary. A previously reported method for electrocardiographic (ECG) telemetry in water using frequency- modulated current was improved to obtain more stable ECGs. The ECGs of seven healthy men were monitored using the improved method during and after whole-body submersion or underwater swimming. Bradycardia and arrhythmias were observed during the submersion, and transient tachycardia was detected after the start of underwater swimming, followed by bradycardia with arrhythmias. Three different types of arrhythmias were observed: sinus arrhythmia (SA), supraventricular extrasystole (SE) and ventricular extrasystole (VE). SA and SE tended to develop during the latter half of the period of submersion or underwater swimming, and especially after the restart of breathing. VEs were detected in only one subject during submersion, whereas they occurred in most subjects during and after underwater swimming. Individual variations were found in development of arrhythmias, one subject showing no arrhythmia. Brady- cardia, SA and SE could depend on vagal suppression in underwater conditions, and VE may be related to the effect of muscular movement on cardiac function in addition to vagal inhibiton.

Key words: Arrhythmia - Bradycardia - Breath holding - Extrasystole - Heart rate

Introduction

Changes in the heart rate (fc) such as bradycardia during simple breath holding (Oldridge et al. 1978), submersion or underwater exercise including synchronized swimming (Asmussen and Kristiansson 1968; Gemma and Wells 1987; Graig and Medd 1968; Irving 1963; Stromme et al. 1970) and tachycardia associated with the Valsalva manoeuvre on land (Campbell et al. 1969) have been extensively investigated in the last 20 years

Correspondence to: H. Miyamoto

and have been reviewed recently by Manley (1990). The mechanisms of these changes, especially the bradycardia, are not well understood. The occurrence of arrhythmias during simple breath holding, submersion of the face or the whole body in water and dividing into water have also been reported. These arrhythmias have been found to result from many types of cardiac disorders produced at various locations in the heart (Lamb et al. 1958; Olsen et al. 1962; Paulev 1969).

In most studies, the electrocardiogram (ECG) and fc have been measured during resting submersion, underwater vertical dividing like that of the ama, the profes- sional woman skin diver for gathering shellfish and sea- weed (Hong et al. 1967; Sasamoto 1965), or simulated swimming while breath holding (Paulev et al. 1990). Changes in fc during underwater swimming for relatively long distances at a constant depth have, however, not been reported, since recording the ECG by the wired method is technically difficult. Moreover, the wired method is occasionally hazardous in water, as will be discussed later. Routine telemetry systems which use radio waves as ECG carriers cannot be employed at depths of 20 cm or more in water. On the other hand, telemetry using sonic or ultrasonic waves is excellent in the open sea, because the waves are not easily attenuated in water and because the method is suitable for long-distance transmission (Kanwisher et al. 1974; Slater et al. 1969). However, this method is not practicable in swimming pools due to the extreme signal distortion caused by complex wave reflections from the walls of the pools.

We have reported an ECG telemetry system using two methods for carrying ECG signals which can be switched automatically (Utsuyama et al. 1988). The signals are carried by a frequency-modulated, very high frequency (FM-VHF) electromagnetic wave in air and by an FM electric current in water, i.e. amphibious telemetry. The ECGs of subjects are monitored in real time and recorded on the audio track of an 8-mm videotape simultaneously with the recording of the subjects' behaviour on a vision track.

In the present study, we first attempted to improve the telemetry system to obtain more stable and less noisy

44

E C G signals w i t h o u t res t r i c t ing f ree m o v e m e n t o f the s u b j e c t ' s b o d y . W e t h e n a n a l y s e d the s ignals to inves t i - ga t e t i m e - d e p e n d e n t changes in fo a n d the a p p e a r a n c e o f a r r h y t h m i a s d u r i n g s u b m e r s i o n a n d u n d e r w a t e r swimming .

Methods

Subjects. Anthropometric data on the seven healthy men studied are summarized in Table 1. The subjects had no history of cardiac disorder and showed no abnormalities of circulatory function on physical examination. They were not especially trained in breath holding or underwater swimming. We explained the purposes and details of the study to them and obtained their consent to partici- pate in experiments. Before submersion, each subject rested on land for about 10 min and then stood upright in a swimming pool (50m long, 140cm deep, 28-30°C) for about 5 min at chest, depth to test that the chest electrodes were waterpoof. To deter- mine a suitable period of submersion, the subject inspired a mod- erate amount of air and submerged his whole body to the bottom of the pool, with his face downward. To achieve complete submersion, each subject put on a plastic belt which six lead blocks weighing a total of 6 kg were attached. When the subject wished to stand he unfastened the belt. In measurements of the duration of underwater swimming, the subjects did not use the weighted belt. In measurements of swimming distances, the subjects started from one side of the pool by kicking off from the wall. Table 1 suggests that the swimming speeds of the subjects varied.

Telemetry systems. The amphibious telemetry systems, one for use on land and the other for use in water, were as reported previously (Utsuyama et al. 1988) with the modifications described in the following. Three electrodes instead of the two reported previously were used as chest leads for the ECG (Fig. 1). Two of these electrodes, E1 and E2, were attached to the skin at similar positions to those used for the routine CM5 lead (Blackburn 1969). The third electrode E0, an indifferent electrode used for the first time in the present study, was connected to the earth of amplifiers A1 and A2. The additional use of E0 stabilized the amplifiers and significantly reduced fluctuation of the ECG base line during underwater exercise. Noise, mainly 60 Hz AC from external sources, was also markedly reduced. In view of the larger numer of chest electrodes, an adhesive foam pad (8 cm square; Nihon Kohden, To- kyo, Japan) was used instead of surgical sheets to cover the electrodes.

Telemetry on land was mediated by a main carrier electromagnetic wave of FM-VHF of 79 MHz central frequency (frequency deviation 50 kHz, modulation frequency 4.6 kHz); that in water by a main carrier of FM current with a central frequency of

Table 1. Characteristics of subjects

Subject Age Height Mass Maximal Maximal no. (years) (cm) (kg) breath diving

hold distance time (s) (m)

1 27 165.3 57.2 107 32 2 26 168.5 75.8 121 34 3 26 177.0 68.2 95 50 4 25 165.1 57.5 95 35 5 35 173.2 65.2 80 35 6 41 174.0 68.5 100 35 7 22 165.0 62.7 100 25 Mean (SD) 29 (6) 169.7 (4.6) 65.0 (6.1) 100 (12) 35 (7)

~ Ant

Fig. 1. Scheme of a modified transmitter system for amphibious electrocardiogram (ECG) telemetry. EO, Reference electrode; E/and E2, chest ECG electrodes; A1 and A2, preamplifiers; A3 and A4, power amplifiers; F1, F2 and F3, low pass filters; M1, 4.6 kHz FM modulator; M2, 79 MHz FM-VHF modulator; M3, 77 kHz FM modulator; EL and ER, left and right lumbar electrodes for transmitting 77 kHz FM current

77kHz (frequency deviation 2kHz, modulation frequency 4.6 kHz). The transmitter was equipped with a constant voltage circuit to avoid frequency shifts in the carrier waves when the source voltage changed. In response to a change in the ECG input of -+ 1 mV, the modulation frequency of 4.6 kHz changed by +- 125 Hz, the FM-VHF of 79 MHz changed by +50 kHz and the FM current of 77 kHz changes by +200 Hz. In concert with the increase in the number of chest electrodes from two to three, the transmitter was also improved as shown in Fig. 1. The input impedance of the amplifier A1, which is normally kept high, was decreased to less than 10 kf2 in the present apparatus to achieve stability, since the amplifiers tend to be unstable when the resistance between the electrodes changes in water. An important modification was the insertion of low-pass filters F2 and F3. Filter F2 pre- vented deformation of the ECG signals and protected the 77 kHz current from mixing with the modulator M1 that produces a sub- carrier of 4.6 kHz FM. Filter F3 was used to avoid the 79 MHz FM radio wave interfering with the 77 kHz main carrier. An other minor modification was a change in the capacitance of the con- densers from 0.01 gF to 0.02 ~tF to reduce output impedance. The improvements of the transmitter resulted in the QRS complex and T wave of the ECG being more sharply discriminated and the T wave appearing more clearly than before. Calculated values of electric and magnetic field strengths and power density of the FM- VHF wave in air were the same with those reported previously. The power density of the FM current in water was estimated to be less than 0.2-2 mW/cm 2. This is far less than the maximum safety limit of 100 mW/cm 2 proposed by the American Natural Science Institute.

The FM current of the ECG signal was received by two parallel underwater antennas, which were, in principle, the same as those used before. However, when the conductivity of the pool water increased slightly due to dissolved salts, leakage of the ECG signals from the naked copper wire antennas to the water before reaching the receiver became marked. To reduce signal loss, we improved the antennas by employing three copper wires: a 17-m- long naked wire (about one-third of 50 m), and 34- and 50-m-long wires which were vinyl coated, except for the last 17 m which remained naked. The advantage of this was that a test subject swimming from one side of the pool to the other was always close to one of the naked parts of the wires. This part received the ECG signal current and transmitted it to the receiver via the coated part without substantial loss. The receiver and reproducer systems were almost the same as those used previously. All instruments for ECG recording were operated by direct current from 12 V batteries to ensure safety. The ECG and the subjects' behaviour were monitored and recorded using the same systems as reported previously.

45

Resu l t s

An example of the time-dependent changes in f~ of a subject (no. 3) during and after underwater submersion is shown in Fig. 2A. The results were obtained in eight trials. The fo before submersion was between 70 and 85 beats, min-1, which was higher than that at rest on land (data not shown) because the subject had finished warm-up exercises and was stressed by waiting in the water for the signal to begin submersion. The fc began to decrease immediately after the start of submersion to about 40-50 beats.min-1 i.e. bradycardia, within some 30-40 s, and then remained almost unchanged during further submersion. When the subject began to breath at the end of submersion, the mean fo increased abruptly, returning almost to the original level, but the marked variance in this period indicated the occurrence of arrhythmias. This variance gradually decreased with time. As the duration of submersion differed in different trials, time is expressed as a percentage of the total submersion period. In this way we were able to compare time-dependent changes infc in different trials on a normalized scale as in Fig. 2B. Relatively large variations of fo before the occurrence of bradycardia were observed in a few trials.

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Fig. 2A-D. Time courses of change in heart rate before, during and after submersion or underwater swimming. A, B Submersion. The time of breath holding in water is expressed in seconds in A and as a percentage of the total aponeic period in B. C, D Under- water swimming. Times in C are expressed in seconds, in D as a percentage of the total apnoeic period

Time-dependent changes in fo during underwater swimming by the same subject are shown in Fig. 2C. The fc before swimming was very similar to that before submersion. However, a temporary increase in fc, i.e. tachycardia, was observed for 10-15 s after the start of swimming. This was followed by a rapidly developing bradycardia up to 30 s; typical patterns of arrhythmias appeared subsequently. The duration of swimming was shorter than that of submersion in all the subjects. When breathing restarted at the end of swimming f¢ increased abruptly with a relatively large variance and then returned to the same level as before swimming. To compare the time-dependent changes in f¢ and times of emergence of arrhythmias in the trials, the data in Fig. 2C are shown on a normalized scale in Fig. 2D. It can be seen that arrhythmias tend to appear in the second half of the period.

The ECGs of all the subjects at rest on land were normal, but various types of arrhythmias were observed during submersion and underwater swimming. Typical ECGs obtained during and after submersion or swimming are shown in Fig. 3, in which the high stability of the base lines may also be seen. The ECGs in Fig. 3A and B show bradycardia during submersion. The arrow in Fig. 3B shows the beginning of disappearance of the P wave, indicating the occurrence of an atrioventricular (AV) junctional rhythm due to vagal escape, occurring with extreme bradycardia. The regions between the dotted lines and arrows in opposite directions in Fig. 3C represent the accelerated AV junctional rhythm during submersion. The ECG in Fig. 3D shows a typical tachycardia after the start of underwater swimming. Signifi- cant bradycardia during swimming is shown in Fig. 3E, the arrow indicating the appearance of a ventricular extrasystole (VE). Small oscillations, probably resulting from muscular to the electrical activity during swimming, sometimes interfered with the P wave as shown in Fig. 3E, but in most cases the abnormal ECG pattern could be distinguished. An example of nodal escape during submersion is shown in Fig. 3F; the arrow shows reappearance of the P wave, indicating restoration of the normal ECG pattern following arrhythmia immediately after the end of submersion. The arrows in Fig. 3G show loss of the P waves and the QRS complexes, i.e. sinus arrhythmia (SA), after the end of submersion. The ECG in Fig. 3H shows two types of extrasystole, VE and supraventricular extrasystole (SE), appearing after the end of underwater swimming. Thus, various types of arrhythmias seem to appear during and especially after submersion or underwater swimming. No correlations were found between different types of arrhythmias and the times of their appearance.

The arrhythmias that developed during and after submersion or underwater swimming were classified into the three types mentioned above: SA, SE and VE. The frequency distributions of these arrhythmias are shown in Fig. 4 as the percentage occurrence in the total number of trials for each subject. The frequencies were low- est during submersion (Fig. 4A), but relatively high in one subject (no. 5), whose arrhythmia was characteristic of SA. SE appeared in two subjects, but the other four

46

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! i lll l!rtl'l r r Fig. 3A-It. Examples of changes in the heart rate and various types of arrhythmias that emerged during submersion or underwater swimming as recorded in the ECG. Vertical arrows and horizontal solid lines indicate sinus arrhythmias or supraventricular extrasystoles; horizontal arrous and dotted lines indicate ventricular extrasystoles. A Bradycardia during submersion; B atrioventricular (AV) junctional rhythm during submersion; 12 accelerated AV junctional rhythms during submersion occurred in the two regions indicated by the two pairs of horizontal arrows; D tachycardia during underwater swimming; E ventricular extrasystole during underwater swimming; F recovery of the P wave after submersion; G sinus arrhythmias after submersion; It supraventricular and ventricular extrasystoles after underwater swimming

did not exhibit any extrasystols. After submersion, the frequencies of arrhythmias increased, but VE did not occur (Fig. 4B). High incidences of SA and SE were observed in six subjects: the frequency of SA was 100% in subject 5 and about 80% in subject 6. The latter did not show any extrasystoles during submersion. Arrhythmias were more pronounced during underwater swimming than during submersion (Fig. 4C). Five of the seven subjects showed SE, the frequency being 80% in subject 2. VE developed in two subjects (nos. 1 and 2) and SA in two others (nos. 3 and 4), but with a low incidence. Aft- er underwater swimming, the sum of the frequencies of SA and SE became much higher than during swimming (Fig. 4D). The frequency of SA was lower, but the incidences of SE seemed to be higher than those after submersion. The arrhythmias in this period were character- ized by a relatively high incidence of VE, which appeared in five of the seven subjects. The frequency of

1oo A 1°°r B 1

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Fig. 4A-D. Frequency distribution of arrhythmias in individual subjects during and after submersion or underwater swimming. Bars represent the percentage occurrence of each type of arrhythmia in the total number of trials for each subject. Classification of arrhythmias: sinus arrhythmia, II; supraventricular extrasystole, n; and ventricular extrasystole, k~. A During submersion; B after submersion; C during underwater swimming; D after underwater swimming

VE was highest in subject 2, who showed this type of extrasystole during swimming and even submersion. Subject 5 showed a relatively high frequency of SA without VE both after submersion and after underwater swimming. Subject 7 showed no arrhythmia under the four different conditions. Thus, individual differences in the frequencies and types of arrhythmias were seen in the subjects.

Time-dependent changes in incidence of extrasystoles during submersion and underwater swimming are shown in Fig. 5A and B respectively. The time of apnoea is shown as a percentage of the total period because the durations of trials differed, while the time after restart- ing breathing is indicated in seconds. No specific time was observed for appearance of arrhythmias during submersion: SA and/or SE began within the first 30% of the period of apnoea and were observed at a steady rate of 1-2 per 10% interval throughout submersion, but VE emerged only once per 10% interval at 40-50% and 50- 60%. After recommencing breathing, the total incidence of SE and SA increased abruptly to 64 within 10 s and 17 within the next 10 s. Thereafter, the incidence of arrhythmias rapidly decreased with time to 1-2 per 10 s f rom 30 s. The incidences of arrhythmias during and after submersion cannot be compared directly, because times in the two conditions are expressed in different

47

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Fig. 5A, B. Time-dependent changes in the incidence of arrhythmias during and after submersion or underwater swimming. The time after the start of apnoea in water is indicated as a percentage of the total duration of breath holding; the time after the restart of breathing is expressed in seconds. A Submersion; B underwater swimming; sinus arrhythmia, I ; supraventricular extrasystole, [3; ventricular extrasystole, []

units. The pattern of appearance of SE during underwater swimming seems similar to that during submersion, but its frequency was higher during swimming with a peak of 13 per 10% time interval at about 80°7o of the swimming period. When breathing was restarted, 3 SA and 26 SE appeared per 10 s interval, resembling the frequencies observed after submersion. In addition and in contrast to submersion, 15 VE per 10 s interval also appeared. The incidence of arrythmias abruptly decreased to about 5-10 per 10 s from 20 s, but VE still contin- ued.

Discussion

In the present study, a method for amphibious ECG telemetry reported previously (Utsuyama et al. 1988) was improved. The improvements consisted of an additional reference chest electrode E0 to reduce fluctuations in the base line of ECG signals and improvement of the underwater antennas to prevent loss of the signal current before reaching the receiver system. When a subject exercises not only on land but also in water, the ECG can be monitored in real time and recorded for later re- production. Use of the routine wired method in water inhibits free body movement of the subject and may

even be dangerous because of the possibility of a short- circuit in the chest electrodes of the ECG in water and of electric shock from the high-voltage alternating current used in the recorder system. This danger could be avoided by use of a waterproof ECG recorder of the Holter type driven by low-voltage batteries (Bonneau et al. 1989). However, with this it is not possible to moni- tor the ECG and observe changes in cardiac activity in real time. A routine telemetry system mediated by me- dium frequency waves eliminates these faults, but ECG signals cannot be obtained when subjects are more than about 20 cm below the surface of the water. Our improved apparatus overcame these difficulties and ena- bled us to obtain ECG wave forms that could be used for analytical purposes. As only one chest lead, - the CM5 lead - was used in the present method, the ECG signals obtained were rather unsatisfactory for detailed classification of arrhythmias. Therefore, at least two chest leads should be employed in future studies.

The occurrence of bradycardia during submersion has been pointed out by many investigators. This bradycardia results from immersion of the body, and especially the face, in water while breath holding. In contrast to this bradycardia, we observed transient tachycardia in all of the subjects after the start of underwater swimming. This transient tachycardia may result from the vagal excitation being initially insufficient to inhibit the increase in fo resulting from vigorous exercise. The exercise consisted of muscular movements including the kick-off from the side of the pool at the start of swimming. This might cause an increase in transmural tho- racic pressure, which is reported to induce tachycardia (Paulev 1968). Similar transient tachycardia has been demonstrated upon breath holding during exercise and movement during diving (Olsen et al. 1962). The relatively high temperature of the water in the pool might also be related to the observed tachycardia, because tachycardia is reported not to occur upon immersion of the face in water of below 24°C (Magel et al. 1982). However, bradycardia gradually took the place of tachycardia during underwater submersion, as has been observed by others (Harding et al. 1965). In a study on the Japanese ama, who dive to the sea bottom, the ini- tial increase in fc caused by dividing movements was found not to be completely suppressed by vagal excitation, though bradycardia subsequently developed (Sasa- moto 1965). The effect of the decrease in blood pressure associated with the Valsalva manoeuvre on the arterial baroreceptor is also considered to initiate tachycardia (Harding et al. 1965). Conversely, breath holding has been shown to raise arterial blood pressure (Lin 1982). However, the vagal influence inducing bradycardia increased with time. The appearance of bradycardia seems to be enhanced by cold (Magel et al. 1982; Speck and Bruce 1978), whereas the level of the minimum fo is reported not to depend on the water temperature (Hay- ward et al. 1984). In the present study the water temperature was above 27 ° C, the threshold below which temperature is held to potentiate bradycardia (Olsen et al. 1962). The hydrostatic pressure is also important in relation to the effects of submersion on diving bradycardia,

48

but reports on its effects are conflicting. The pressure could change significantly during a vertical dive, as in area diving, but in the present study submersion and underwater swimming were studied at a constant depth of about 140 cm. Hence, the influence of pressure on the subjects was constant, irrespective of movement in the water.

Our results showed, first, that the incidence of arrhythmias was higher during underwater swimming than during simple submersion and, second, that is was higher after the restart of breathing than during submersion or underwater swimming. A third finding was that only SE and SA occurred after submersion, but that VE also appeared during, and especially after, underwater swimming. Similar findings have been observed in studies on skin divers (Bonneau et al. 1989).

Among the arrhythmias, SA and SE were associated with bradycardia and could be attributed to imbalance of the autonomic nerves involving vagal inhibition of sinus rhythm. This possibility was supported by the results from subject 7. In this subject, fo did not fall below 70 bea t s .min- 1, nor did any type of arrhythmia occur in any trial. This indicates the significance of bradycardia as a key phenomenon leading to SA or SE. Stimula- tion of autonomic nerves to the AV nodal area of the dog heart has been shown to induce AV junctional rhythms, suggesting that sympathetic-parasympathetic imbalance may unmask subsidiary pacemaking activity (Furukawa et al. 1990).

The aetiology of VE under apnoeic conditions seems to be more complicated than that of SE. Olsen et al. (1962) reported the frequent occurrence of VE arising from at least two foci during simple breath holding; Bonneau et al. (1989) observed no correlation between the degree of bradycardia and the appearance or disappearance of VE. Contrary to these results, in the present study VE did not emerge alone, but in association with SA, SE or both, in all cases. Moreover, in all but one subject VE was observed during underwater swimming but not during resting submersion. These findings sug- gest that vagal inhibition of cardiac activity during underwater exercise and an unknown influence of muscular movements on the inhibition are necessary for gener- ating VE. Exercise is known to generate VE with some degree of reproducibility in normal men and patients with cardiopathological symptoms (Faris et al. 1976). Therefore, muscular movement may stimulate production of VE during underwater swimming.

Acknowledgements. This study was supported in part by a grant for scientific research given to one of the authors from the Uehara Memorial Foundation.

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changes in cardiac rhythm in man during underwater submersion and swimming studied by ecg telemetry

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