by Peter Lindholm, M.D., Ph.D.
Swedish Defence Research Agency, Centre for Environmental Physiology, Karolinska Institutet, Stockholm, Sweden
A freediver has to avoid drowning by surfacing before hypoxia causes loss of consciousness – commonly referred to as freediver blackout. Unfortunately, freedivers drown every year. Safe limits can be exceeded by employing various physiological mechanisms that enable individuals to hold their breath until syncope. This paper is a review of physiological mechanisms that may interact with ventilatory sensitivity to hypoxia or hypercapnia to increase the ability to breath-hold until loss of consciousness (LOC) or freediver blackout. These factors include: hyperventilation, hypoxia of ascent, fasting and prolonged exercise, and individual variation in the strength of the diving response.
Carbohydrate depletion: Prolonged periods of physical work deplete the carbohydrate stores (glycogen) in the body, which forces the body to compensate by increasing the rate of lipid (fat) metabolism. When the human body burns fat to produce energy, it uses 8% more oxygen than if it metabolizes carbohydrates. Also, 30% less CO2 is produced by fat metabolism than carbohydrate metabolism. Thus, a breath-hold diver who has depleted his glycogen stores will become hypoxic faster, but the CO2 driven stimulus to breathe will be delayed. A dive that could safely be performed in a rested and well-fed state may be dangerous after a long day of exertion from diving (11). A carbohydrate rich meal has been shown to reduce breath-hold durations (due to higher CO2 levels and stronger urge to breathe from the higher RER) in subjects who had fasted for 18 h, suggesting that that the risk could be reduced by proper energy intake (13) and that breath-hold diving on an empty stomach may be dangerous.
Hyperventilation: Hyperventilation reduces the blood CO2 content without increasing the oxygen content to the same extent, because the oxygen stores in the body are maintained constantly with normal breathing. Initiating the BH dive with a reduced carbon dioxide level makes it easier maintain breath-hold, enabling some divers with strong motivation (or a high tolerance to discomfort) to hold their breath until unconsciousness. Craig (3) showed that the prolonged breath hold times after hyperventilation were associated with lower oxygen levels in the blood going to the brain; these levels were low enough to cause hypoxic loss of consciousness. This was a particular problem if the diver exercised (swam) during the breath-hold.
Ascent blackout: The partial pressure of oxygen in the lungs (not the fractional percent) affects oxygen loading of the blood and therefore the oxygen delivery to the brain. A critical oxygen pressure (PAO2) of 30 mm Hg (values as low as 23 mm Hg have recently been reported (14) will sustain consciousness when breathing is resumed after a breath-hold (dive). At the surface, this equates to about 4% oxygen in the lungs and 45% oxygen saturation of the arterial blood. While a diver at the surface would be unconscious with an pulmonary oxygen content of 2% (PAO2: 15 mm Hg), a diver swimming at 30 m (98 ft) with 2% oxygen in the lungs would feel comfortable, since the oxygen pressure would be 60 mm Hg (due to the surrounding pressure of four atmospheres absolute pressure). Recall Dalton’s Law of Partial Pressure: the partial pressure of a gas equals the absolute pressure times the fraction of the gas: 4 ATA (3040 mm Hg) * 2 % oxygen = 60 mm Hg PAO2. This diver, who is still able to swim at 30 m (98 ft), would become unconscious during his ascent to the surface because the partial pressure of oxygen in the lungs would be reduced along with the absolute pressure. If we disregard the oxygen consumption of swimming, the diver will reach the critical oxygen level at a depth of 10 m (33 ft) where the absolute pressure is 2 ATA and the oxygen pressure will be 30 mm Hg (1520 mm Hg * 2% = 30 mm Hg). Thus, a breath-hold diver is most likely to suffer loss of consciousness near the surface during the ascent (5,6). The term ‘shallow water blackout,’ originally coined for CO2 intoxication in diving with closed circuit breathing gear, is sometimes inappropriately used to describe hypoxia of ascent.
Diving response and oxygen conservation during exercise: The diving response has been shown to be highly variable among humans (10). These cardiovascular mechanisms may temporarily conserve oxygen during apnea with concomitant exercise (2,7,9) (i.e., temporarily reduce oxygen uptake in muscles). The strength of the response could be a factor, together with lung volume and swimming economy to render some humans more likely to survive long breath-hold dives. Inter-individual differences in bradycardia, vasoconstriction during exercise and apnea correlated significantly with arterial oxygen saturation (7); a stronger response resulted in a slower uptake of oxygen from the lungs. This effect was evident during both dry steady state exercise and immersed intermittent exercise concomitant with apnea (8). Thus it appears that certain individuals are able to reduce blood flow to the working muscles during apnea and thus conserve oxygen for the central nervous system that (unlike muscle) cannot function without aerobic metabolism.
Competitive diving: During competitions in breath-hold diving, most divers hyperventilate extensively and determine the duration of their breath-hold by means other than the hypercapnic ventilatory drive. Some seem to react to hypoxia via the urge to breathe, while others actively decide to abort the breath-hold when vision starts to falter, described as ‘greyout’ (personal communication with elite divers). While testing a group of competitive breath-hold divers performing static apnea, it was shown that end-tidal CO2 was about 20 mm Hg prior to apnea (after 5-20 min of hyperventilation) and was still within normocapnic values, at around 38 mm Hg, upon termination of apnea (with breath-hold durations approaching five minutes). Subjects managed to surface without symptoms of severe loss of motor control (LMC) or LOC (12) exhaling gas samples with PO2 as low as 23 mm Hg (14). Two subjects suffered LMC, exhaling samples of 20 and 21 mm Hg (14).
There are other possible explanations for LOC during breath-hold diving.
Arrhythmia: The bradycardia triggered by apnea will result in various arrhythmias in humans (16), and it has been suggested that some individuals may be more sensitive to drowning accidents due to a mutation in a cardiac potassium channel (1).
Glossopharyngeal Insufflation: Breath-hold divers use glossopharyngeal insufflation (GI) ‘lungpacking’ to increase the volume of air in the lungs. This technique may cause syncope, most likely due to reduced venous return and therefore a loss of arterial pressure. There are numerous accounts of LOC with GI, with one incident where arterial blood pressure was measured simultaneously by finger plethysmography showing a loss of pulse pressure and thereafter LOC while performing GI (15).
Dejours (4) suggested that the urge to breathe may not be a safe determination of breath-hold duration, something that should be remembered, considering that much of today’s teaching focuses on the safety of breath-hold diving as it regards CO2 and hyperventilation. The general practice of discouraging hyperventilation prior to breath-hold diving will not make diving completely safe. Also, since competitive divers regularly hyperventilate prior to diving, the ‘old’ recommendations may fall into disuse. Education about the various mechanisms and safety procedures seems more beneficial for the future.
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DR. FEINER: Two comments and questions. As a father watching kids do breath-holds at swim meets, my interest has returned to breath-hold diving. The effects of hyperventilation start with the first few breaths. You increase the oxygen scores, alveolar PO2 from 120 to 130 mmHg on the first few deep breaths while actually having minimal effect on CO2 elimination. If we were to look at the CO2 about 30 s later, it would be almost the same. And that improvement in oxygen store would actually be theoretically beneficial for safety.
I wonder if we switch to that, a few deep breaths is actually probably better because the breakpoint is likely to occur at a higher saturation. That is one comment. And these people that you are showing really are going at pretty steady state levels based on what their final CO2 is at breath-hold breakpoint.
If you look at variation, I think it is always what makes people different, and you talk about variation in human apneic response. There is huge variation in ventilatory drives. The normal variation in hypoxic ventilatory drive and hypercapnic ventilatory drive are easily a three to four-fold range, with a huge difference in susceptibility. You showed differences in cardiovascular response. There is a reasonable chance actually that those responses are somewhat linked, and that the effect you are showing on saturation may also be related to a ventilatory drive. Have you studied the cardiovascular response and hypoxic and hypercapnic ventilatory drive in the same subjects?
DR. LINDHOLM: No. I have not studied hypercapnic or hypoxic ventilatory drive in those subjects. A comment on the other two things. Three to four deep breaths before breath-hold diving has long been generally recommended and is usually not considered as hyperventilation. As you point out, you get most of the benefit from the increased oxygen stores in the lungs from a couple of deep breaths. So the increase after that is, I guess, minor, but it is probably quite a bit anyway. It seems to be, why should they otherwise do it?
DR. FEINER: I think the competitive breath-hold divers’ improvement in venous oxygen saturation is probably very, very significant and they are probably benefiting from that because they are going to extreme levels. Whereas most breath-hold divers in pools actually are not getting low enough to really extract from hemoglobin. So there are differences between safety and benefit at the extreme level. I would agree that there is probably significant benefit for hyperventilation for the extreme diver.
DR. LINDHOLM: A normal person that holds his breath usually breaks with over 90% saturation if they do not hyperventilate extensively, so they are nowhere near any hypoxia.
In terms of your comment on the variability of their ventilatory drive, Kirk Krack, who is sitting here, he told me of a diver he met who did not get any urge to breathe at all. He could just hold his breath until he passed out. So there are always going to be individuals. I do not know if Mr Krack wants to comment any more of that?
MR. KRACK: It is just he would not show any signs of hypoxia or even hypercapnia. One minute he is signaling you every 15 s and the next minute he is not. And there is no contraction. There is nothing. The only thing we could base his safety on would be signals. One minute he is there, 15 s later he is not signaling and he has blacked out. He cannot describe any idea of what is what is going on.
DR. LUNDGREN: What keeps him alive?
MR KRACK: We have come across a couple of people.
UNIDENTIFIED SPEAKER: So I was intrigued by these low end-tidal PCO2s. I am wondering why do they end their breath-hold?
DR. LINDHOLM: The hypoxia produces a respiratory drive as well. It is not considered as strong as the hypercapnic ventilatory drive. But these two work in agreement together, and it has been studied in altitude medicine, for example. So you could say that they got hypoxic ventilatory drive that they get an urge to breathe from, but some of them use other cues.
I had one of the divers who managed to surface at 23 mm Hg, stating that he came up because he wanted to come up clean. He tried to do an extended breath-hold afterwards when he tried a little longer and he did not come up clean (unfortunately, he inhaled a little bit before he blew in the tube so we did not get that measurement). He showed signs of LMC.
None of these divers passed out during the experiments, but exactly how they know how to come up, you are free to ask. You have a few here in the audience. I have heard some say they feel something in the head, and some say the vision. And I know one that states that the grayout (vision) is not the end point, he can go a little longer than the grayout and still surface clean, he states that he then feel something in the head and if he goes past that, then he pass out. These are anecdotes. What exactly that refers to, I do not know.
UNIDENTIFIED SPEAKER: Is it possible that the end-tidal PCO2s are not representing what is going on in the alveoli or the blood?
DR. LINDHOLM: End-tidal PCO2s are supposed to be quite reliable in this situation (subjects do a maximal exhalation from a full lung volume after a breath-hold). In certain situations with an extended breath-hold, there is actually a reverse flow of CO2 from the lungs into the blood since CO2 is concentrated due to the shrinkage of the lung volume [Lindholm et al. 2002 EJAP].
DR. BENNETT: I want to come back to loss of consciousness and the lack of warning. I got involved with a case quite recently of a young boy who chose to breath-hold in a swimming pool where the people who should be watching, lifeguards, did not see him. Just laid underwater like that and held his breath. And he died, just like that. With no warning at all, no indication of change, like the apneic people here where they tap him on the shoulder all the time.
I would like the opportunity here to make one case that the one up, one down is very important in any breath-hold that is going on. You must have someone over the individual who is trying to breath-hold.
It is becoming in Europe, of course, very strong apneic sport, as they call it. And if it starts as I think it is beginning to start in this country, there is a lot of interest in breath-hold diving in a lot of areas. And we have to be very careful to have someone observing that individual because unconsciousness can occur very, very easily without warning.
DR. LINDHOLM: Yes, it is a teaching problem. There have, to my knowledge, not been any casualties among those who practice the competitive breath-hold diving according to the suggestions and rules of the sport. Whether they have had other accidents, we do not know. But there have been no accidents in organized competitions or organized training events or courses. They have a very strict safety protocol. Kirk Krack and his Performance Freediving team are going to talk more about this tomorrow.
DR. MACRIS: How do you explain the difference in the cognitive function of an athlete who is at the 50 to 60 mm Hg PCO2 point where you describe the alteration in thinking and maybe fogginess and the patient with chronic lung disease that we see all the time who may be an engineer or a professional person who actually functions fairly well at a PO2 of 50 to 60 mm Hg, although their PCO2 is chronically elevated? How do you describe the difference?
DR. LUNDGREN: If I may interject. The chronic one is like the mountain climber who spends a month in base camp before going to the peak. Messner and Habeler climbed to the peak of Mount Everest with a calculated PO2 somewhere on the order of 35 mm Hg, where other people would lie flat.
DR. MACRIS: There has to be an adaptive phenomenon. Have you looked at that?
DR. LINDHOLM: We have a presentation coming up where Lynne Ridgway is going to talk a little bit more about those cognitive effects. I think we should continue. I want to make a point that some of you may have thought of. It would seem like Peter Lindholm has put to rest or rather contradicted what our mothers told us. That you do not go swimming immediately after having lunch.
When we talk about food, perhaps we should be a little more precise and take note of what Peter said. It is a matter of what your RER is rather than whether there is food in your stomach. And mother might still have been right because if you have a very full stomach and go swimming, the pressure distribution of the body from the abdomen and outwards is conducive to regurgitation.
NOTE: To access the entire proceedings of the UHMS DAN 2006 Breath-hold Proceedings, visit Divers Alert Network.
In: Lindholm P, Pollock NW, Lundgren CEG, eds. Breath-hold diving. Proceedings of the Undersea and Hyperbaric Medical Society/Divers Alert Network 2006 June 20-21 Workshop. Durham, NC: Divers Alert Network; 2006.