Japanese female pearl divers called Ama specialize in free diving in the cold sea for collecting foods and pearls in oysters. Exercising in the water combined with marked bradycardia and pressor responses provides a circulatory challenge to properly buffer or cushion elevated cardiac pulsations. Because Ama perform repeated free dives throughout their lives, it is possible that they may have adapted similar arterial structure and function to those seen in diving mammals. We compared arterial stiffness of lifelong Japanese pearl divers with age-matched physically inactive adults living in the same fishing villages. A total of 115 Japanese female pearl divers were studied. Additionally, 50 physically inactive adults as well as 33 physically active adults (participating in community fitness programs) living in the same coastal villages were also studied. There were no differences in age (∼65 yr), body mass index, and brachial blood pressure between the groups. Measures of arterial stiffness, cardio-ankle vascular index and β-stiffness index were lower (P < 0.05) in pearl divers and physically active adults than in their physically inactive peers. Augmentation pressure and augmentation index adjusted for the heart rate of 75 beats/min were lower (P < 0.05) in pearl divers than in other groups. These results indicate that lifelong Japanese pearl divers demonstrate reduced arterial stiffness and arterial wave reflection compared with age-matched physically inactive peers living in the same fishing villages.
- arterial compliance
- diving reflex
- physical exercise
the ama are Japanese female divers who specialize in free diving in the cold sea for collecting foods and pearls. In the ancient times, women were thought to be able to hold breath longer and better suited to diving in the cold water as they possess an extra layer of fat for insulation. The history of Ama dates back almost 2,000 years ago as it is referenced in the Gishi-Wajin-Den published in 268 BC. Even today Ama dive into cold water without any modern diving equipment to reduce the risk of overfishing and to protect the ecosystems. In a typical day, Ama perform ∼100–150 free dives holding breath for up to 2 min at a time (3, 13).
From the physiological standpoint, each diving maneuver evokes the diving reflex, a complex cardiorespiratory response to water immersion (19). The diving responses are initiated by apnea and consist of sympathetically mediated peripheral vasoconstriction and a dramatic increase in arterial blood pressure (6). The resultant stimulation of arterial baroreceptors produces vagally induced bradycardia (5, 12). These hemodynamic changes are accelerated by cooling of the faces in the cold sea and/or hypoxia in prolonged breath holding. The diving bradycardia is fairly substantial getting reduced to 50% of the resting heart rate and persists despite the vigorous underwater swimming performed by Ama (20).
Exercising in the water combined with marked bradycardia and high blood pressure provides a circulatory challenge to properly buffer or cushion elevated cardiac pulsations (14). Typically, this is the role of arterial compliance/stiffness embedded in the cardiothoracic arteries since arterial compliance reflects the ability of an elastic artery to expand and recoil with cardiac pulsation and relaxation (27). In the diving conditions, the organism has to adapt to augment the arterial compliance function. Indeed diving mammals, such as seals and whales, have adapted the arterial structure such that the ascending aorta is about three to four times larger than their descending aorta (17, 21). This structural adaptation not only enhances the compliance function of the aorta but also serves to maintain arterial flow during the protracted diastole of bradycardia by giving the aorta the properties of a Windkessel, a German word meaning elastic reservoir (10). The mechanical properties of arteries have a substantial ability and plasticity to adapt to the chronic physiological loads that are accumulated over the years (25). Because Ama perform repeated free dives and experience diving-induced bradycardia (20) throughout their lives, it is possible to hypothesize that they may have adapted similar arterial structure and function and demonstrate a favorable phenotype of enhanced arterial compliance. However, currently there is no information available to address this hypothesis. Pulse pressure has been used as a rough index of arterial stiffness (2). It is interesting to note that Ama divers demonstrate a significantly lower pulse pressure compared with age- and gender-matched non-Ama living in the same village (26).
With this information as background, the primary aim of the present study was to determine arterial structure and function of Ama divers compared with age-matched non-Ama living in the same fishing villages. We hypothesized that Ama divers would demonstrate a reduced arterial stiffness compared with non-Ama.
A total of 115 Japanese pearl divers were studied. The comparison groups included physically inactive adults and physically active adults living in the same fishing villages. All the subjects were free of overt cardiovascular diseases as assessed by medical history questionnaire. Pearl divers had been in the profession for 38 ± 8 yr and had not performed other modes of regular exercise. Physically active adults had been exercising regularly in the city-operated exercise and fitness programs. All procedures were approved by the Institutional Review Board, and written informed consent was obtained from each individual before participation.
Before the measurements, subjects abstained from caffeine, fasted for 3 h, and abstained from exercise for at least 24 h. Height, body mass, and body mass index (BMI) were measured with conventional methods. Body fat was estimated by bioelectrical impedance technique.
After subjects had rested in a supine position, heart rate, brachial blood pressure, ankle-brachial pressure index (ABI), and cardio-ankle vascular index (CAVI), an index of systemic arterial stiffness, were measured with a semiautomated vascular screening system (VaSera, Fukuda Denshi, Tokyo, Japan) (22). Additionally, local (i.e., carotid) arterial stiffness was measured. Briefly, the B-mode longitudinal ultrasound images of the left common carotid were recorded using an ultrasound device with a high-resolution (14 MHz) linear transducer (CX50xMATRIX; Philips Ultrasound, Bothell, WA) and were analyzed offline by using automatic edge-detection software (Vascular Tool 5; Medical Imaging Applications, Coralville, IA). The pressure waveforms were obtained from the common carotid artery with a pencil-type probe incorporating a high-fidelity strain-gauge transducer (SPT-301, Millar Instruments, Houston, TX). Those were calibrated by equating the carotid mean arterial and diastolic blood pressure to the brachial artery values. β-Stiffness index, an index of arterial stiffness adjusted for distending pressure, was calculated by use of the following equation: ln(P1/P0)/[(D1 − D0)/D0], where D1 and D0 are the maximal and minimum diameters and P1 and P0 are the highest and lowest blood pressures (11).
Pulse wave analysis.
Aortic blood pressure was estimated from carotid artery pressure waveforms via the generalized transfer function-based central blood pressure measurement device (SphygmoCor, AtCor Medical, Sydney, Australia). Contoured aortic blood pressure waveform was calibrated by equating the aortic mean and diastolic blood pressure to the brachial artery values. Augmentation pressure (defined as the height of the peak above the shoulder of the wave) and the augmentation index [the ratio of augmented pressure/pulse pressure × 100 (%)] were obtained (9). The area under the aortic diastolic and systolic pressure-time curves (both measured from 0 mmHg) were calculated as diastolic time integral (DTI) and tension time integral (TTI) for estimates of myocardial perfusion and oxygen consumption (4). Subendocardial viability ratio (SEVR) was then calculated as the ratio of DTI/TTI × 100 (%). This index is related to subendocardial-to-subepicardial blood flow ratio and analogous to subendocardial perfusion (4).
Vital volume, forced vital volume, forced respiratory volume, and expiration peak flow were evaluated with conventional method using a spirometer (SP-370COPD, Fukuda Denshi, Tokyo, Japan).
One-way ANOVA was used to evaluate group differences. In the case of a significant F value, Fischer's least significance difference testing was performed to determine significant group differences. Data are reported as means ± SD unless indicated otherwise. Statistical significance was set at P < 0.05.
The physically inactive, physically active, and pearl diver groups were not different in age, height, BMI, and medication status (Table 1). Brachial blood pressure, aortic blood pressure, and ankle-brachial index were not different among the groups (Table 2). Brachial pulse pressure was lower and SEVR was higher in the physically active and pearl diver groups than in the physically inactive group. Augmentation pressure and augmentation index adjusted for the heart rate of 75 beats/min were lower (P < 0.05) in pearl divers than the other groups. As shown in Fig. 1, arterial stiffness as measured by CAVI and β-stiffness index was lower (P < 0.05) in the physically active and pearl diver groups than in the physically inactive group. Average forced vital capacity recorded in the present study (2.4–2.6 liters) was similar to typical values predicted for Japanese women of similar age and height (∼2.6 liters). There was no group difference in vital capacity and forced expiratory volume (Table 3). Peak flow was lower (P < 0.05) in pearl divers than in the other groups.
The primary finding of the present study is that Japanese pearl divers demonstrated a significantly lower arterial stiffness as assessed by CAVI and β-stiffness index compared with their age-matched physically inactive peers living in the same fishing village. Additionally, lifelong pearl divers exhibited lower values in indices of arterial wave reflection and higher values in subendocardial perfusion as estimated by SEVR. Rather surprisingly, pulmonary function of pearl divers was not particularly high and even lower than their physically inactive peers in some measures. Collectively, these results suggest that the lifelong profession of pearl diving is associated with favorable adaptations in arterial elasticity and wave reflection.
Japanese female pearl divers are one of the most fascinating elements of Japanese culture. However, the number of pearl divers is steadily decreasing in recent years dropping to one-eighth of the population of 60 years ago. It is estimated that less than 2,000 pearl divers presently remain in the entire Japan, and the profession is on the verge of extinction. The diminishing number of Ama is primarily due to a lack of influx of young new pearl divers into this hard profession performed in the cold ocean frequently under the intense sunlight. As a result, the average age of the pearl divers is above the Japanese standard retirement age of 65 yr as reflected in the mean age in the present study. Importantly, most pearl divers remained relatively healthy and were able to keep diving to a very old age. This preservation has provided an opportunity for us to capture and study female pearl divers who had been performing this profession for many decades. We found that lifelong pearl divers demonstrated significantly reduced arterial stiffness as measured by multiple assessment modalities. Their values were compared with the age-matched physically inactive peers living in the same coastal villages. The comparison group was provided to control for dietary and environmental influences on outcome measures because the comparison of pulse-wave velocity between inhabitants of fishing and farming villages in Japan revealed that the population with higher fish consumption demonstrated lower arterial stiffness (8).
Regular physical activity, more specifically aerobic exercise, has been associated with the prevention and treatment of arterial stiffening that occurs with advancing age (23, 24). We have recently demonstrated that regular swimming could also exert destiffening effects on central elastic arteries in middle-aged and older adults with elevated blood pressure (15) and in patients with osteoarthritis (1). In the present study, we determined the influence of chronic diving maneuvers on arterial elasticity using lifelong Japanese Ama divers. The pearl diving is unique from other modes of exercise as it involves diving reflexes superimposed on cardiovascular responses typically experienced during physical exercise. Arterial stiffness of pearl divers was not different from those of physically active adults. As such, it is not clear whether the lower arterial stiffness of pearl divers is attributed to regular exercise involved in diving or aortic adaptation to cope with the unique physiological diving responses.
As elegantly described by Scholander (19) as “the master switch of life,” submersion into water through diving produces very unique physiological responses to the threat of asphyxia. Theses diving responses are found in human divers as well as in diving mammals (20). The comparative physiology literature indicated that diving mammals exhibit two to three time greater internal radius in the ascending aorta than that in the descending thoracic aorta (17, 21). Interestingly, virtually all of the arterial compliance function is concentrated in the aortic arch in these diving mammals as arterial stiffness rises dramatically from the ascending aorta to the abdominal aorta (7). This abrupt transition could produce a large impedance mismatch that can exert substantial impact on arterial wave reflection and hemodynamics. Unfortunately, the differential measurement of stiffness at the aortic arch and the descending thoracic aorta could not be made in the present study. As such, it remains unknown if this sudden transition in arterial stiffness exists in lifelong pearl divers. But we assessed arterial wave reflection and its hemodynamic sequelae in an attempt to gain insight into this question. Augmentation pressure and augmentation index adjusted for the heart rate of 75 beats/min were lower in pearl divers than other groups. Additionally, subendocardial perfusion was greater in pearl divers than in their physically inactive peers. Reduced arterial wave reflection as well as increased subendocardial perfusion are associated with lower cardiac events (16, 18). Thus regularly performed diving maneuvers appear to provide favorable influences on cardiovascular disease risks through its influence on arterial wave reflection.
A rather surprising finding of the present study is the pulmonary function of the pearl divers as assessed by the spirometry. Because of the repeated breath-hold diving that they perform, their pulmonary function would be expected to be substantially greater. However, the pearl divers did not demonstrate superior pulmonary function. Their numbers were rather low and lower than their physically inactive peers in some measures. The pearl divers have developed a unique breathing method during their diving maneuvers. After surfacing from the ocean, they open their mouths slightly letting out a loud and low whistle slowly on expiration. This maneuver is thought to protect their lungs and prevent excessive hyperventilation that could lead to unconsciousness. Lower pulmonary function in the pearl divers may be related to the lifelong routine practice of this breathing pattern as many of the pearl divers could not perform forced expiration required for the spirometer testing despite a number of attempts.
Perspectives and Significance
The present study evaluated arterial stiffness of lifelong pearl divers who had been in this profession for many decades. As hypothesized, their arterial stiffness was significantly lower in Ama divers than in non-Ame living in the same village to be suitable for dealing with repeated diving responses. Additionally, arterial wave reflection was lower and subendocardial perfusion was higher creating hemodynamically favorable conditions in Ama divers. Currently, the population of Japanese pearl divers is on the verge of extinction as few young women come into this profession. Unless we revive this fascinating profession, the present study could potentially be the last large-scale physiological study to investigate the arterial health of the Japanese pearl divers.
The present study was supported in part by the grant from the Japan Society of Promotion of Science (S15718 to H. Tanaka).
No conflicts of interest, financial or otherwise, are declared by the author(s).
Author contributions: H.T. and J.S. conception and design of research; H.T., T.T., K.K., and J.S. performed experiments; H.T., T.T., and J.S. analyzed data; H.T., K.K., and J.S. interpreted results of experiments; H.T. drafted manuscript; H.T., T.T., K.K., and J.S. edited and revised manuscript; H.T., T.T., K.K., and J.S. approved final version of manuscript; J.S. prepared figures.
The authors thank Takashi Kuwayama, Kyohei Fukatani, and Tetsuya Ito from Fukuda Denshi for technical support and assistance with the testing. The Vasera equipment was provided by the Fukuda Denshi free of charge during the investigation.
- Copyright © 2016 the American Physiological Society