EFFECT of WATER TEMPERATURE on BRADYCARDIA DURING NONAPNEIC FACIAL IMMERSION in MAN Bradycardia During Submersion Has Long Been

J. Physiol., 23, 613-624, 1973

EFFECT OF WATER TEMPERATURE ON BRADYCARDIA DURING NONAPNEIC FACIAL IMMERSION IN MAN

SyOiti KOBAYASI and Tokuo OGAWA*

Department of Physiology, Niigata University School of Medicine, Niigata, Japan

Summary Bradycardiac response to nonapneic facial immersion in man was examined at water temperatures of 10, 20, 30, 35, 40, and 47•Ž. The response was mainly dependent on the water temperature. In

general, the colder the water, the greater the response. However, the least response was noted at 40•Ž; at 47•Ž the bradycardia was greater than at 40•Ž. The bradycardiac response was generally more marked

in trained swimmers and divers than in subjects unaccustomed to swimming. The magnitude of changes in facial skin temperature appeared to

have an additional influence on the cardiac slowing. Heart rate reached the minimum value in 20-30 sec, then tended to return toward the initial rate during immersion. Stimulation of cutaneous cold receptors is assumed to be most responsible for the development of bradycardia on nonapneic facial immersion, and the return of heart rate during immersion may be attributed to adaptation of these receptors.

Bradycardia during submersion has long been known in diving animals (ANDERSEN,1966). In man also heart rate decreases during diving (IRVING,1963). Total immersion of the body with breath holding is sufficient but not essential for initiating bradycardia in man. Slowing of heart rate can be elicited either by immersion of the face alone with snorkel breathing or by body immersion with the head above water. Facial immersion is more effective than immersion of any other part of the body (KOBAYASIet al., 1971). It has been generally recognized that bradycardia during apneic diving in man originates from the following two factors; hemodynamic changes induced by breath holding and by changes in hydrostatic pressure and cutaneous stimulation by water. The hemodynamic factors could be eliminated by nonapneic facial immersion procedure.

Received for publication August 1, 1973 * Present address: Department of Physiology , Aichi Medical University, Nagakute, Aichi Prefecture. 小林庄一, 小川徳雄*

613 614 S. KOBAYASI and T. OGAWA

In a previous report, we stated that the extent of bradycardia in response to nonapneic facial immersion was largely dependent on water temperature (KOBA- YASIet al., 1971). In the present study the magnitude and the pattern of bradycardiac response to nonapneic facial immersion was examined more precisely at various water temperatures, so that the effect of water temperature on the bradycardiac response was evaluated. Differences in the responses of subjects accustomed and unaccustomed to swimming were also examined .

METHODS

Observations were made on 8 trained male swimmers or divers and 5 healthy men unaccustomed to swimming. No significant differences in physical character- istics were found between the two groups. Heart rate , facial skin temperature, and ventilatory movement were recorded on a pen-writing oscillograph and on a magnetic recorder. The electrocardiogram was taken with electrodes placed over the top right margin and the lower left margin of the sternum . The number of heart beats was counted to one decimal place in every 5 sec and converted to the rate per minute. In a few cases, the RR intervals were determined by means of an analogue computer (ATAC 501-20 , Nihon Kohden Co., Ltd., Tokyo). Facial skin temperature was sensed by a copper-constantan thermojunction placed below the right cheek bone. Changes in ventilatory movement were monitored by an electric stethograph at the lower part of the chest. In a few experiments on 3 subjects, systolic blood pressure was sphygmomanometrically measured at the left arm, and a reflection photoelectric plethysmogram at the tip of the right index finger was recorded with a time constant of 2 sec . The subject, lightly clothed, was directed to lie prone on a bench with the head protruding over the edge, being supported by a canvas sling on the forehead . A basin filled with water was placed right under the head . The subject put on a nose-clip and breathed quietly through a two-way snorkel . After a control recording period of 1 min, the basin was pulled up through a pulley to immerse the face up to the level just ventral to the ears. The immersion lasted for 2 min in the majority of cases, then the basin was lowered. The recording was continued for 2 min after emersion of the, face. The water temperatures applied in most cases were 10, 20, 30, 35, 40, or 47•Ž. Subsequent immersion was done only after the skin temperature was stabilized at or near the original level , i.e., there was an interval of at least 3 min between immersions. The room temperature was not controlled, but was kept amply warm, between 25-29•Ž.

RESULTS

Tracings of RR intervals, ventilatory movements, and facial skin temperature obtained from an amateur diver are presented in Fig. 1. The figure shows ap- parent increases in RR interval, i.e., decreases in heart rate, during nonapneic IMMERSION BRADYCARDIA AND WATER TEMPERATURE 615 facial immersion at certain water temperatures. Transient irregularity in ventilatory movements was noted upon immersion and emersion, but in no case was reflex apnea observed.

Fig. 1. Cardiac responses to nonapneic facial immersion of a trained subject. In each panel the traces are, from the top downward, time signal in 50 sec, the RR interval converted by an analogue computer from a magnetically memorized electrocardiogram, the ventilatory movement, and the facial skin temperature. The water temperature is indicated at the lower right corner of each panel.

The bradycardiac response showed considerable individual differences,

but daily variations were rarely found within an individual. The mean heart

rate changes for each test temperature in each group are summarized in Fig. 2, where percent changes in heart rate of every subject have been averaged for

each 5 sec and plotted against the time with standard deviations. When two or more experiments were done on a single subject, the average value for that

subject was obtained and used in the calculation of the group average. The decrease in heart rate during immersion was statistically significant at every water

temperature tested in both trained and untrained groups (Table 1, uppermost row). The bradycardiac response appeared to be greater in trained subjects than

in untrained ones. The resting heart rate, however, showed no significant difference between the two groups: 67.3•}11.04 beats/min in untrained subjects and

70.3•}13.20 in trained swimmers. Further, no distinct relationship was found 616 S. KOBAYASI and T. OGAWA

Fig. 2. Average responses of heart rate to nonapneic facial immersion in water of varied temperatures. Heart rates are shown in percent changes from the mean control rate before immersion. Standard deviations are illustrated above and below the tracing of the mean heart rate. The beginning and the end of facial immersion are indicated by the two vertical lines. Left column, trained subjects; right column, untrained subjects.

between the resting heart rate and the percent changes in heart rate during immersion at any water temperature in either groups.

Effects of water temperature

A general trend was suggested that the magnitude of bradycardiac response to facial immersion without apnea is dependent on the water temperature (Fig. 2). The relation between the water temperature and the maximum fall in heart rate

during facial immersion is shown in Fig. 3. Although, in general, the colder the

water was, the greater was the response elicited, the least response was noted at 40•Ž, and the bradycardia was greater at 47•Ž than 40•Ž. Statistical comparison

of the maximum falls during immersion among different water temperatures re- vealed a significant temperature dependency of cardiac response in the group of trained subjects, but no significant dependency was noted in the group of untrained subjects (Table 1). The maximum bradycardiac response was significantly less in untrained subjects than in trained ones at water temperatures of 47, 20, and 10•Ž (P<0.05, <0.025, and <0.025, respectively). IMMERSION BRADYCARDIA AND WATER TEMPERATURE 617

Fig. 3. Heart rate response and facial skin temperature during nonapneic facial immersion at varied water temperatures. Circles denote the maximum percent falls in heart rate, triangles indicate the facial skin temperatures during immersion, and squares the facial skin temperatures before immersion. Solid symbols are values for trained subjects and open ones for untrained subjects. Vertical bars indicate standard errors.

Table 1. P-values estimated by paired t-tests on differences in the maximum percent fall in heart rate between the cardiac responses to nonapneic facial immersion of different water temperatures.

ns indicates P>0.05

In two cases of trained subjects, the face was precooled by an immersion in water of 10•Ž for 4 min. The test immersion at 20•Ž was begun 2 min later, when the facial temperature remained at a level considerably lower than the con- 618 S. KOBAYASI and T. OGAWA trol, while the heart rate, which had decreased during the cooling immersion, had returned almost to the resting rate. In these cases the drop of facial temperature was less, though its level during immersion was lower than in the control immersion without previous cooling; and the bradycardia elicited was less than in the control immersion (Fig. 4).

Fig. 4. Effect of facial temperature before the immersion upon the degree of immersion bradycardia. Results from 3 immersions in water of 20•Ž are presented, of which

one (crosses) was done 2 min after cooling of the facial skin by a previous immersion at 10•Ž for 4 min, and the others (open and solid circles) were done without precooling.

Details in text.

Pattern of changes in heart rate Slowing of heart rate began almost immediately upon immersion and pro- ceeded for 20-30 sec in most cases. Heart rate then showed a tendency to turn toward the resting level, while the facial skin temperature remained almost un- changed or continued to approach gradually the water temperature (Figs. 1 and 2). This tendency in heart rate was significant (P<0.01) whenever the bradycardiac response was distinct, according to paired t-tests on differences between the heart rate at the point of maximum fall and that at the end of immersion. The returning tendency of heart rate was more evident in experiments of 4-min immersion, as illustrated in Fig. 5. In cases of immersion at 47•Ž, the heart rate recovered quickly, often exceeding the resting level within 2 min of the immersion period and diminishing gradually after emersion (Figs. 1 and 2). The excess, however, was not statistically significant. Stirring the water with a water pump failed to change significantly the degree or the pattern of bradycardia. IMMERSION BRADYCARDIA AND WATER TEMPERATURE 619

Fig. 5. Heart rate and facial skin temperature during nonapneic facial immersions for 2 and 4 min. Closed circles indicate the results from 2-min immersion and open circles, 4- min immersion.

Hemodynamic changes No appreciable changes in systolic blood pressure were noted during facial immersion at any water temperature, with rare occurrences of a transitory increase upon immersion. Peripheral vascular responses were estimated by observation of changes in the amplitude of the pulse wave recorded on a fingertip photoplethysmogram. Pulse waves tended to show a steady gradual increase in amplitude during facial immersion. Only occasionally, a transitory increase in blood pressure or peripheral vasoconstriction preceded the bradycardiac response during facial immersion. Examples are illustrated in Fig. 6.

Electrocardiagraphic findings Slowing of the heart rate developed through the prolongation of PP interval, i.e., sinus slowing. The P wave was often suppressed and occasionally disappeared. Respiratory arrhythmia was usually intensified concomitantly with the development of bradycardia (Fig. 1). Neither the PQ nor QT interval was lengthened, irrespective of the increase of PP or PR interval. Supraventricular premature beats were occasionally observed at lower water temperatures, but no ventricular premature beats were noted in the present experiments with nonapneic facial immersion.

DISCUSSION The reduction of heart rate during nonapneic water immersion in man has been considered to be a reflex vagal inhibition of the heart originating from stimulation of certain sensory elements in the skin (PRICK, 1966; WHAYNEand KILLIP, 1967; PAULEV,1968; KOBAYASIet al., 1971). If the falls in heart rate during nonapneic facial immersion reported in the literature (BRICK, 1966; CORRIOLet al., 620 S. KOBAYASI and T. OGAWA

Fig. 6. Heart rate, systolic blood pressure, and amplitude of photoplethysmogram of the fingertip. Large circles indicate the percent changes in heart rate (MLR.), triangles systolic blood pressure in torr (B. P.), and small circles the amplitude of the finger plethysmogram in arbiturary units (F. P.).

1966; KAWAKAMI et al., 1967; WHAYNE and KILLIP, 1967; CORRIOL and ROHNER, 1968; PAULEV, 1968; KOBAYASI et al., 1971) are plotted against water temperature, the trend is obvious that the decrease in heart rate is least at around 35-40•Ž and is progressively greater as water temperature is lowered (Fig. 7). Such temperature-dependency of immersion bradycardia has been suggested (CRAIG, 1963; WHAYNE and KILLIP, 1967; SONG et al., 1969), and the receptors sensitive to cold in the facial skin have been considered to be most responsible for the development of the cardiac response to facial immersion (KAWAKAMI et al., 1967; PAULEV, 1968).

Systematic observations on this problem have been made by CORRIOL and IMMERSION BRADYCARDIA AND WATER TEMPERATURE 621

ROHNER (1968). According to them, the subjects felt comfortable, neither cold

nor warm, at water temperature of 30•Ž, where the responses were mild. Below 20•Ž, the colder the water, the greater the response, and at a higher temperature

(40•Ž) the bradycardia was less in degree than that at the comfortable temperatures (open squares in Fig. 7). They explained these observations as follows:

Bradycardia observed at an indifferent temperature might result from stimulation

Fig. 7. Relation of the degree of bradycardia during nonapneic facial immersion to water temperature. Survey of the data from the literature.

of certain mechanoreceptors in the facial skin sensitive to touching water, which might be confused with cold receptors. At a lower temperature the response

would be potentiated by stimulation of cold receptors, while at a higher tem-

perature it would be attenuated by an intervention of nociceptive acceleration of heart rate. The indifferent temperature range described by CORRIOL and ROHNER

(1968), however, seems to be rather low. KAWAKAMI et al. (1967) noted that the neutral water temperature for facial skin was approximately 34•Ž. In the present experiments subjects felt indifferent to water temperatures of 35-40•Ž, where the

least cardiac response was observed. Afferent impulses from cold receptors of mammals (Dour and ZOTTERMAN, 1952; BOMAN, 1958), including man (HENSEL

and BOMAN, 1960), generally disappear around these temperatures. These observations may suggest an important role of cutaneous cold receptors in the initiation of bradycardia during facial immersion.

Our previous (1971) and present observations demonstrated a bradycardiac response to nonapneic facial immersion in water of 42-45•Ž and also of 47•Ž.

The decrease in heart rate during immersion in hot water may be attributed to paradoxical excitation of cold receptors (Dour and ZOTTERMAN, 1952). 622 S. KOBAYASI and T. OGAWA

In the present experiments the least response was observed not at the water

temperature where the change in facial temperature was minimum, but in the

range of water temperature to which the subjects felt indifferent (Fig.3). On the other hand, precooling of the face lessened the bradycardiac response to facial immersion in cold water (Fig.4). These observations suggest that the cardiac

response to nonapneic facial immersion may be mainly dependent upon the level

of skin temperature, and the magnitude of change of the temperature may have some influence.

The slight bradycardia observed at an indifferent temperature (Fig.3) may be attributed to the stimulation of cutaneous mechanoreceptors sensitive to

touching water. These receptors, however, may not have so much bearing on the immersion bradycardia, since stirring of water had no significant effect on features of the response.

Labyrinthine reflex may be suspected to participate in the bradycardiac response during diving. However, it was demonstrated in an previous paper

(KOBAYASI et al., 1971) that bowing the head upon facial immersion had no influence on bradycardiac response of sitting subjects. In the present experiments,

possible intervention of labyrinthine reflex was excluded, for the head of the subject was not moved by the immersion procedure.

Another possibility remains that the bradycardiac response to facial immer-

sion may be secondary to hemodynamic changes associated with cooling of the face. The present results, however, failed to show consistent peripheral vaso-

constriction or rise in blood pressure of appreciable degree in association with the development of bradycardia (Fig.6).

Reversion of the heart rate toward the resting level in the course of face immersion has drawn little attention from previous authors; only short descriptions

have been made by BRICK (1966) and ASMUSSEN and KRISTIANSSON (1968). COR- RIOL and ROHNER (1968), on the other hand, failed to note such reversion of heart rate during nonapneic facial immersion of 90-sec duration, unless the water temperature was extremely low (5 and 0•Ž). At these low temperatures a slight rise in heart rate was found which was attributed to a nociceptive reaction. The lowest temperature applied in the present study was 10•Ž, which is unlikely to be a noxious stimulus. The recovery of heart rate is so gradual that the trend may be more evident with immersion of a longer duration, as in our experiments with 4-min immersion (Fig.5). The gradual recovery of the decreased heart rate during immersion may be attributed to the adapting process in cutaneous cold receptors. The time course of changes in heart rate during nonapneic facial immersion may correspond to that of discharge frequency of facial cold fibers, as was observed in rats by BOMAN (1958). Heart rate recovery in excess of the control level during immersion at 47•Ž, however, cannot be fully ascribed to the adapting process. Some other processes such as warm reception and nociception may take part in this overshoot. IMMERSION BRADYCARDIA AND WATER TEMPERATURE 623

The bradycardiac response to immersion is greater in trained swimmers than in those unaccustomed to swimming (IRVING,1963; ANDERSEN,1966; WHAYNE and KILLIP, 1967; KOBAYASIet al., 1971). This difference may be attributable to physical training, since the heart rate is one of a few physiologic variables that have been shown to change with intensive physical training. A decreased heart rate at rest is a characteristic often observed in trained athletes. WHAYNEand KILLIP (1967) reported, however, that the percent changes in heart rate during facial immersion observed in highly trained oarsmen were virtually identical with those in untrained subjects, though the resting heart rate was lower in the former than in the latter. In the present observations, bradycardia during facial immersion was greater in trained swimmers than in untrained subjects, but no significant difference in the resting heart rate was found between the two groups. Further, no distinct relationship was observed between the resting heart rate and the extent of immersion bradycardia. Hence, the greater bradycardiac response observed in trained swimmers or divers could not be directly attributed to general physical training. Some investigators emphasized the emotional or psycho- physiological effect of immersion (ASMUSSENand KRISTIANSSON,1968; PAULEV, 1968; CAMPBELLet al., 1969). For instance, PAULEV(1968) stated that the more pronounced cold bradycardia in accomplished swimmers may simply be due to less psychic excitation, such as fear and anxiety, which attenuate the degree of bradycardia. Another possibility to be considered is that inherent or constitutional factors may be related to the degree of bradycardia. In diving vertebrates immersion is accompanied by an integrated oxygen-conserving reflex, which intensively slows down the heart rate, maintains central arterial pressure, and redistributes blood flow (ANDERSEN,1966). Diving bradycardia in man may be considered to be a vestige of this reflex, though whether it is helpful in swimming for man has not been ascertained. If the bradycardia is an advantage in man's swimming, those who develop a pronounced bradycardia will be more readily attracted and accustomed to swimming than those who show a poor bradycardiac response. From this point of view a marked bradycardiac response in accustomed swimmers may be a result of a constitutional selection. This work was done as a part of IBP, and was partly supported by the specialresearch grant No.499114from the Ministryof Educationof Japan.

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