Alveolar gas composition and exchange during deep breath-hold diving and dry breath holds in elite divers GUIDO FERRETTI, MARIO COSTA, MASSIMO FERRIGNO, BRUNO GRASSI, CLAUDIO MARCONI, CLAES E. G. LUNDGREN, AND PAOLO CERRETELLI Department of Physiology, Centre Mkdical Universitaire, Universite’ de Gene’ve, 1211 Geneva 4, Switzerland; Istituto di Technologie Biomediche Avanzate Section of Physiology, Consiglio Nazionale de& Ricerche, 20100 Milan, Italy; and Center for Research in Special Environments, State University of New York, Buffalo, New York 14214 FERRETTI, GUIDO, MARIO COSTA, MASSIMO FERRIGNO, sition and exchange as well as energetics of deep breathBRIJNOGRASSI,CLAUDIOMARCONI, CLAES E.G. LUNDGREN, hold diving. ANDPAOLOCERRETELLI.Alveolar gas composition and exchange The aims of the present study, conducted on three very
during deep breath-hold diving and dry breath holds in elite divers. J. Appl. Physiol. 70(2): 794-802, 1991.-End tidal 0,
cooperative elite divers (ED), were 1) to assess alveolar gas exchange during and alveolar gas composition at the end of deep dives and resting dry breath holds (BHs), 2) to evaluate the contribution of oxidative and anaerobic (lactic) energy sources to the overall energy expenditure during the dives, and 3) to compare the results obtained during BHs on ED with those on nondiver control subjects (C). The authors of this study are obviously aware of the danger inherent in extreme breath-hold diving and do not endorse record attempts as being medically safe.
and CO, (PETIT ) pressures,expired volume, blood lactate concentration ([Lab\), and arterial blood O2saturation [dry breath holds (BHs) only] were assessedin three elite breath-hold divers (ED) before and after deep dives and BH and in nine control subjects(C; BH only). After the dives (depth 40-70 m, duration 88-151 s), end-tidal 0, pressuredecreasedfrom - 1.40 Torr to a minimum of 30.6 Torr, PETIT, increasedfrom -25 Torr to a maximum of 47.0 Torr, and expired volume (BTPS) ranged from 1.32 to 2.86 liters. Pulmonary 0, exchange was 4551,006 ml. CO, output approached zero. [La,] increased from - 1.2 mM to at most 6.46 mM. Estimated power output during diveswas513-929 ml O,/min, i.e., -2O-30% of maximal METHODS 0, consumption. During BH, alveolar PO, decreased from -130 to ~30 Torr in ED and from 125to 45 Torr in C. PETIT, Subjects. The experiments were conducted on the increasedfrom -30 to -50 Torr in both ED and C. Contrary three Majorcas, a male (EM) and his two daughters (RM to C, pulmonary 0, exchange in ED was lessthan resting 0, and PM), in the course of deep breath-hold dives and consumption, whereas CO, output approached zero in both during resting BHs in the supine position. EM estabgroups. [La,l was unchanged. Arterial blood 0, saturation dediving in 1960, creasedmore in ED than in C. ED are characterized by in- lished his first world record in breath-hold when he reached the depth of 45 m. He was then the first creasedanaerobic metabolism likely due to the existence of a man to dive to 50,80, and 90 m below the sea surface. His diving reflex. latest record (101 m) was established on July 30,1988. He end-tidal oxygen and carbon dioxide pressures;lung volumes; aerobic and anaerobic metabolism; arterial oxygen saturation; blood lactate; oxygen-carbon dioxide diagram
INTEREST in the physiology of deep breath-hold diving was recently renewed when Enzo Majorca and one of his daughters performed record breath-hold dives of 101 and 80 m, respectively. The current world records were established in late 1989 and are held by A. Bandini, a woman from Italy, and F. Ferreira, from Cuba, at 107 and 112 m, respectively. The Majorcas, as well as Bandini and Ferreira, emerged conscious from their deep dives despite the prediction of extremely low end-tidal oxygen tension (PET& values at emergence that could be made from the PETIT values found by several authors (7,9,27, 31) at the end of shorter and shallower dives. The recent exceptional achievements in breath-hold diving have raised a number of physiological questions concerning circulatory changes and alveolar gas compo794
0161-7567191
$1.50 Copyright
is one of the few individuals known to have dived below 100 m in controlled conditions while holding his breath. RM and PM have personal depth records of 80 and 70 m, respectively. The BH experiments were performed also on nine sex- and age-matched C (3 males and 6 females with no prior diving experience). The subjects gave informed consent before participating in the study. The physical characteristics of the subjects appear in Table 1. Vital capacity was measured by standard spirometry. Residual volume (RV) was determined by the nitrogen washout method. Blood hemoglobin concentration and hematocrit were obtained by standard laboratory techniques. Oxygen uptake (VO& and carbon dioxide output at the steady state were measured by a standard open-circuit method. Maximal 60, was determined during running (RIM and PM) or walking (EM) on a treadmill at increasing speeds. Maximal VO, was defined as the VO, level not followed by a further increase in VO, (>2%) with a subsequent l-km/h increase in speed. Deep dives. The experiments were carried out from a boat in the open sea during training breath-hold dives.
0 1991 the American
Physiological
Society
Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on September 4, 2018. Copyright © 1991 American Physiological Society. All rights reserved.
GAS EXCHANGE TABLE 1. Physiological Subj
EM RM PM
Age, Yr
57 28 30 33+_16
Height, cm
173 159 160 167k8
characteristics
IN ELITE DIVERS
795
of subjects
Weight, kg
W liters
RV, liters
Rest vo2, ml/min
Maximal Tjo2, l/min
78.1 60.7 61.4 63.2t12.4
4.91 4.43 4.62
2.20 1.14 1.26
273 220 260
2.88 2.80 2.91
4.42t0.16
1.58t0.32
257t37
Values for C are means ~frSD of 9 subjects. VC, vital capacity; ho,,
CO, production;
The subjects were assisted by a team of experienced scuba divers, their physician, and a skilled diving tender. Each dive was preceded by two or three hyperventilation maneuvers (separated by lo-min intervals) consisting of series of deep breaths @O-90% of vital capacity) at a frequency of 4-5 breaths/min over a period of 8 min. The hyperventilation immediately preceding the dive was performed while the subject was partially immersed in water (midthigh level). The dives started at a lung volume close to the subject’s total lung capacity (TLC) and were performed with an assisted technique. During the descent, the diver was pulled by a weight running along a vertically suspended tight rope. Most of the weight was that of a platform on which the diver could stand (EM and PM) or that could be held onto with one hand while descending head first (R2M). To facilitate ear clearing, the diver could interrupt the descent by applying a brake at selected depths. During ascent, the divers were pulled up by a gas-filled balloon, which was released just before emersion (14). End-expiratory gas composition and expired air volume at the end of the dives were determined as follows
/
F-W 9 iid1
205 170 192
148 143 137
223k38
146&B
[Hb], hemoglobin concentration.
(Fig. 1). Expired air was collected in a &liter anesthesia bag connected to a three-way stopcock by a l&m-long 25-mm-diam rubber tube. A mouthpiece was attached on one arm of the stopcock. Two unidirectional valves were inserted along the tube to prevent air mixing between bag and tube and/or contamination with ambient air. One valve was positioned just downstream from the stopcock and the other at a distance of 85 cm from the stopcock, thus comprising a volume of ~400 ml where end-expiratory air could be trapped. Two clamps were also applied to the tube. Clamp A was near the valve close to the stopcock. Clamp B was just downstream from the second valve. The tube was prepared so that clamp A was closed and the stopcock and clamp B were open. At emersion, an operator handed the mouthpiece to the diver and released clamp A. The diver expired into the bag to RV, and clamp A and stopcock were then closed. Nose breathing was prevented by the wearing of a tightly fitting mask. Aboard a support boat, end-expiratory air samples were drawn into four 50-ml glass syringes that were then sealed with rubber stoppers and brought to the laboratory in a thermically insulated bag. The plungers of the
UNIDIRECTIONAL VALVE
I
Rest ko,, ml/min
UNIDIRECTIONAL VALVE w4OOml “END-TIDAL”AlR
1
STOPCOCK
ET@ * 1 &TO2
F,Tco 2 1 FTC02
FIG. 1. Setup used for collection of end-expiratory air at end of deep breath-hold dives. FETE, and FETED,, end-tidal O2 and CO, fractions, respectively. A and B refer to clumps A and B, respectively. Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on September 4, 2018. Copyright © 1991 American Physiological Society. All rights reserved.
796 TABLE
GAS EXCHANGE
IN ELITE
DIVERS
2. Dive data
Subj
Dive Depth, m
Dive Duration,
s
EM 70 70 60
144 151 115
45 50 40 50
107 131 88 91
45 50
110 88
RM
PM
PETo,, Torr
PETCOp Torr
VE, liters BTPS
134.8 39.4 30.6 39.2 134.5 56.3 33.5 55.2 46.9 143.8 72.5 93.6
23.7 47.0 46.9 44.1 24.2 29.3 42.8 31.3 30.2 26.2 31.6 26.5
4.50 1.74 1.32 2.02 4.12 2.39 2.86 2.59 2.03 4.50 2.75 2.50
A-o29 ml
Gas Exchange Ratio
Abop ml
819 1006 800
42 0 -36
0.05 0.00 -0.05
552 627 541 603
-23 55 10 34
-0.04 0.09 0.02 0.06
573 455
-23 39
-0.04 0.09
v-41, mM
1.46 4.41 6.46 3.25 1.04 4.02 5.68 2.46 3.85 1.20 2.36 1.71
PETq, PETco2, and VE were measured before and at end of dives. AVL,, AVL~~~, and gas exchange ratio were measured during dives. [Lab] was measured before and during recovery from dives (peak values).
End-expiratory gas samples before dives were obtained on the boat. At the end of a hyperventilation maneuver identical to the last hyperventilation performed before diving, the subsequent expired volume to RV (VE) was collected with the same technique used after the dives. The overall lung volumes (VE + RV) and the corresponding O2 and CO, fractions were assumed to be equal to the pulmonary volume and end-tidal gas fractions, respectively, at the start of dives. Blood lactic acid concentration ( [Lab]) was determined by an electroenzymatic method (23) by use of a Kontron 640 lactate analyzer. Twenty-microliter capillary blood samples were taken from the earlobe before and at different times between the 3rd and 15th min of the recovery after the dives and were analyzed within l-2 h in the laboratory. BHs. BHs were carried out at rest in the supine position. The subject performed a series of BHs of increasing
duration, starting from 30 s. Each BH was preceded by 1 min of hyperventilation ending with a maximal inspiration so that all BHs started close to the subject’s TLC. At the end of BH, the subject performed a maximal expiration. Each successive BH up to the maximal (BH,,) was 30 s longer than the preceding one and followed it after a 5-min interval. The latter time appears sufficient to allow recovery of CO, stores before the start of the next BH, because most CO, is stored in fast-equilibrating tissues. PO, and PCO, throughout the respiratory cycle before and after each BH were monitored by the rapid gas analyzers and recorded on paper. The expired volume at the end of each BH was measured by a Tissot spirometer connected to the expiratory side of a two-way unidirectional valve whose inspiratory side was open to the ambient. Low-resistance turbine flowmeters (SensorMedits) were placed on both inspiratory and expiratory sides. Any small movement of the turbine indicated that the subject was not really holding his breath, in which case the experiment was repeated. Arterial 0, saturation (Sa,,) was continuously recorded by an ear oximeter (Biox IIA). [La,] before and after BH,,, was determined as described above. The same variables were also measured at 0 s BH with and without hyperventilation. The volume expired at 0 BH was used to calculate the initial lung volume, which,
TABLE 3. PETIT during BHs preceded by 60 s of hyperventilation
TABLE 4. PETITEduring BHs preceded by of hyperventilatzon
syringes had been lubricated with a saturated LiCl solution to prevent drying during transport (9). The volume of gas contained in the bag was measured by a dry gas meter (SIM Brunt). The 0, and CO, fractions in the syringes were determined by fast-responding (90% of response time
during deep breath-hold diving and dry breath holds in elite divers. J. Appl. Physiol. 70(2): 794-802, 1991.-End tidal 0,
cooperative elite divers (ED), were 1) to assess alveolar gas exchange during and alveolar gas composition at the end of deep dives and resting dry breath holds (BHs), 2) to evaluate the contribution of oxidative and anaerobic (lactic) energy sources to the overall energy expenditure during the dives, and 3) to compare the results obtained during BHs on ED with those on nondiver control subjects (C). The authors of this study are obviously aware of the danger inherent in extreme breath-hold diving and do not endorse record attempts as being medically safe.
and CO, (PETIT ) pressures,expired volume, blood lactate concentration ([Lab\), and arterial blood O2saturation [dry breath holds (BHs) only] were assessedin three elite breath-hold divers (ED) before and after deep dives and BH and in nine control subjects(C; BH only). After the dives (depth 40-70 m, duration 88-151 s), end-tidal 0, pressuredecreasedfrom - 1.40 Torr to a minimum of 30.6 Torr, PETIT, increasedfrom -25 Torr to a maximum of 47.0 Torr, and expired volume (BTPS) ranged from 1.32 to 2.86 liters. Pulmonary 0, exchange was 4551,006 ml. CO, output approached zero. [La,] increased from - 1.2 mM to at most 6.46 mM. Estimated power output during diveswas513-929 ml O,/min, i.e., -2O-30% of maximal METHODS 0, consumption. During BH, alveolar PO, decreased from -130 to ~30 Torr in ED and from 125to 45 Torr in C. PETIT, Subjects. The experiments were conducted on the increasedfrom -30 to -50 Torr in both ED and C. Contrary three Majorcas, a male (EM) and his two daughters (RM to C, pulmonary 0, exchange in ED was lessthan resting 0, and PM), in the course of deep breath-hold dives and consumption, whereas CO, output approached zero in both during resting BHs in the supine position. EM estabgroups. [La,l was unchanged. Arterial blood 0, saturation dediving in 1960, creasedmore in ED than in C. ED are characterized by in- lished his first world record in breath-hold when he reached the depth of 45 m. He was then the first creasedanaerobic metabolism likely due to the existence of a man to dive to 50,80, and 90 m below the sea surface. His diving reflex. latest record (101 m) was established on July 30,1988. He end-tidal oxygen and carbon dioxide pressures;lung volumes; aerobic and anaerobic metabolism; arterial oxygen saturation; blood lactate; oxygen-carbon dioxide diagram
INTEREST in the physiology of deep breath-hold diving was recently renewed when Enzo Majorca and one of his daughters performed record breath-hold dives of 101 and 80 m, respectively. The current world records were established in late 1989 and are held by A. Bandini, a woman from Italy, and F. Ferreira, from Cuba, at 107 and 112 m, respectively. The Majorcas, as well as Bandini and Ferreira, emerged conscious from their deep dives despite the prediction of extremely low end-tidal oxygen tension (PET& values at emergence that could be made from the PETIT values found by several authors (7,9,27, 31) at the end of shorter and shallower dives. The recent exceptional achievements in breath-hold diving have raised a number of physiological questions concerning circulatory changes and alveolar gas compo794
0161-7567191
$1.50 Copyright
is one of the few individuals known to have dived below 100 m in controlled conditions while holding his breath. RM and PM have personal depth records of 80 and 70 m, respectively. The BH experiments were performed also on nine sex- and age-matched C (3 males and 6 females with no prior diving experience). The subjects gave informed consent before participating in the study. The physical characteristics of the subjects appear in Table 1. Vital capacity was measured by standard spirometry. Residual volume (RV) was determined by the nitrogen washout method. Blood hemoglobin concentration and hematocrit were obtained by standard laboratory techniques. Oxygen uptake (VO& and carbon dioxide output at the steady state were measured by a standard open-circuit method. Maximal 60, was determined during running (RIM and PM) or walking (EM) on a treadmill at increasing speeds. Maximal VO, was defined as the VO, level not followed by a further increase in VO, (>2%) with a subsequent l-km/h increase in speed. Deep dives. The experiments were carried out from a boat in the open sea during training breath-hold dives.
0 1991 the American
Physiological
Society
Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on September 4, 2018. Copyright © 1991 American Physiological Society. All rights reserved.
GAS EXCHANGE TABLE 1. Physiological Subj
EM RM PM
Age, Yr
57 28 30 33+_16
Height, cm
173 159 160 167k8
characteristics
IN ELITE DIVERS
795
of subjects
Weight, kg
W liters
RV, liters
Rest vo2, ml/min
Maximal Tjo2, l/min
78.1 60.7 61.4 63.2t12.4
4.91 4.43 4.62
2.20 1.14 1.26
273 220 260
2.88 2.80 2.91
4.42t0.16
1.58t0.32
257t37
Values for C are means ~frSD of 9 subjects. VC, vital capacity; ho,,
CO, production;
The subjects were assisted by a team of experienced scuba divers, their physician, and a skilled diving tender. Each dive was preceded by two or three hyperventilation maneuvers (separated by lo-min intervals) consisting of series of deep breaths @O-90% of vital capacity) at a frequency of 4-5 breaths/min over a period of 8 min. The hyperventilation immediately preceding the dive was performed while the subject was partially immersed in water (midthigh level). The dives started at a lung volume close to the subject’s total lung capacity (TLC) and were performed with an assisted technique. During the descent, the diver was pulled by a weight running along a vertically suspended tight rope. Most of the weight was that of a platform on which the diver could stand (EM and PM) or that could be held onto with one hand while descending head first (R2M). To facilitate ear clearing, the diver could interrupt the descent by applying a brake at selected depths. During ascent, the divers were pulled up by a gas-filled balloon, which was released just before emersion (14). End-expiratory gas composition and expired air volume at the end of the dives were determined as follows
/
F-W 9 iid1
205 170 192
148 143 137
223k38
146&B
[Hb], hemoglobin concentration.
(Fig. 1). Expired air was collected in a &liter anesthesia bag connected to a three-way stopcock by a l&m-long 25-mm-diam rubber tube. A mouthpiece was attached on one arm of the stopcock. Two unidirectional valves were inserted along the tube to prevent air mixing between bag and tube and/or contamination with ambient air. One valve was positioned just downstream from the stopcock and the other at a distance of 85 cm from the stopcock, thus comprising a volume of ~400 ml where end-expiratory air could be trapped. Two clamps were also applied to the tube. Clamp A was near the valve close to the stopcock. Clamp B was just downstream from the second valve. The tube was prepared so that clamp A was closed and the stopcock and clamp B were open. At emersion, an operator handed the mouthpiece to the diver and released clamp A. The diver expired into the bag to RV, and clamp A and stopcock were then closed. Nose breathing was prevented by the wearing of a tightly fitting mask. Aboard a support boat, end-expiratory air samples were drawn into four 50-ml glass syringes that were then sealed with rubber stoppers and brought to the laboratory in a thermically insulated bag. The plungers of the
UNIDIRECTIONAL VALVE
I
Rest ko,, ml/min
UNIDIRECTIONAL VALVE w4OOml “END-TIDAL”AlR
1
STOPCOCK
ET@ * 1 &TO2
F,Tco 2 1 FTC02
FIG. 1. Setup used for collection of end-expiratory air at end of deep breath-hold dives. FETE, and FETED,, end-tidal O2 and CO, fractions, respectively. A and B refer to clumps A and B, respectively. Downloaded from www.physiology.org/journal/jappl by ${individualUser.givenNames} ${individualUser.surname} (192.236.036.029) on September 4, 2018. Copyright © 1991 American Physiological Society. All rights reserved.
796 TABLE
GAS EXCHANGE
IN ELITE
DIVERS
2. Dive data
Subj
Dive Depth, m
Dive Duration,
s
EM 70 70 60
144 151 115
45 50 40 50
107 131 88 91
45 50
110 88
RM
PM
PETo,, Torr
PETCOp Torr
VE, liters BTPS
134.8 39.4 30.6 39.2 134.5 56.3 33.5 55.2 46.9 143.8 72.5 93.6
23.7 47.0 46.9 44.1 24.2 29.3 42.8 31.3 30.2 26.2 31.6 26.5
4.50 1.74 1.32 2.02 4.12 2.39 2.86 2.59 2.03 4.50 2.75 2.50
A-o29 ml
Gas Exchange Ratio
Abop ml
819 1006 800
42 0 -36
0.05 0.00 -0.05
552 627 541 603
-23 55 10 34
-0.04 0.09 0.02 0.06
573 455
-23 39
-0.04 0.09
v-41, mM
1.46 4.41 6.46 3.25 1.04 4.02 5.68 2.46 3.85 1.20 2.36 1.71
PETq, PETco2, and VE were measured before and at end of dives. AVL,, AVL~~~, and gas exchange ratio were measured during dives. [Lab] was measured before and during recovery from dives (peak values).
End-expiratory gas samples before dives were obtained on the boat. At the end of a hyperventilation maneuver identical to the last hyperventilation performed before diving, the subsequent expired volume to RV (VE) was collected with the same technique used after the dives. The overall lung volumes (VE + RV) and the corresponding O2 and CO, fractions were assumed to be equal to the pulmonary volume and end-tidal gas fractions, respectively, at the start of dives. Blood lactic acid concentration ( [Lab]) was determined by an electroenzymatic method (23) by use of a Kontron 640 lactate analyzer. Twenty-microliter capillary blood samples were taken from the earlobe before and at different times between the 3rd and 15th min of the recovery after the dives and were analyzed within l-2 h in the laboratory. BHs. BHs were carried out at rest in the supine position. The subject performed a series of BHs of increasing
duration, starting from 30 s. Each BH was preceded by 1 min of hyperventilation ending with a maximal inspiration so that all BHs started close to the subject’s TLC. At the end of BH, the subject performed a maximal expiration. Each successive BH up to the maximal (BH,,) was 30 s longer than the preceding one and followed it after a 5-min interval. The latter time appears sufficient to allow recovery of CO, stores before the start of the next BH, because most CO, is stored in fast-equilibrating tissues. PO, and PCO, throughout the respiratory cycle before and after each BH were monitored by the rapid gas analyzers and recorded on paper. The expired volume at the end of each BH was measured by a Tissot spirometer connected to the expiratory side of a two-way unidirectional valve whose inspiratory side was open to the ambient. Low-resistance turbine flowmeters (SensorMedits) were placed on both inspiratory and expiratory sides. Any small movement of the turbine indicated that the subject was not really holding his breath, in which case the experiment was repeated. Arterial 0, saturation (Sa,,) was continuously recorded by an ear oximeter (Biox IIA). [La,] before and after BH,,, was determined as described above. The same variables were also measured at 0 s BH with and without hyperventilation. The volume expired at 0 BH was used to calculate the initial lung volume, which,
TABLE 3. PETIT during BHs preceded by 60 s of hyperventilation
TABLE 4. PETITEduring BHs preceded by of hyperventilatzon
syringes had been lubricated with a saturated LiCl solution to prevent drying during transport (9). The volume of gas contained in the bag was measured by a dry gas meter (SIM Brunt). The 0, and CO, fractions in the syringes were determined by fast-responding (90% of response time
