ACCLIMATIZATION YOU DON'T WANT...
Carbon Dioxide
Effects of carbon dioxide retention in diving.
Could you be a retainer?
by Jolie Bookspan, Ph.D. and Rev. Edward H. Lanphier, M.D.
Many attempts have been made to identify carbon dioxide retainers. Such people could be at unexpected risk of
CO2 blackout, unusual degrees of nitrogen narcosis or susceptibility to oxygen toxicity.
In a U.S. Navy experimental facility, testing for new decompression schedules was under way using nitrox
mixtures with a higher concentration of oxygen than the 21 percent in air. The Navy investigators first used 100
percent O2 at various pressures to work out tolerance limits for oxygen itself. They established a tentative "limit
curve" based upon presumably reliable data. The actual tests were carried to 25 percent longer times than on the
limit curve. No serious toxicity was observed inside the limit curve, so this was accepted as safe.
It seemed rational to assume that partial pressure of oxygen, or PO2, was the only crucial variable to derive limits
for mixtures. Simply translating the limits for 100 percent O2 into curves for different nitrox mixtures on the basis
of oxygen partial pressures meant the mixtures should have been all right. But in the first experiment to test test
nitrox mixtures, the diver convulsed. After that, there were problems suggesting early oxygen poisoning and other
strange effects where no difficulties were expected.
WHAT'S GOING ON WITH MIXED GAS?
The year was 1952 at the U.S. Navy Experimental Diving Unit. The EDU, then located in Washington, D.C., was
ordered to work out a system using "mixed gas" to reduce decompression requirements for applications like
clearing mines from a harbor. Project Officer Lt. Cmdr. J.V. Dwyer and Assistant Medical Officer Lt. E.H.
Lanphier (MC) took major responsibility for this work.
Dives with nitrox mixtures appeared to produce an unusual number of problems compared with those using
previously worked-out oxygen limits. Furthermore, these problems did not occur when using helium-oxygen
mixtures with the same oxygen pressure. The only plausible explanation involved carbon dioxide. There was no
CO2 in the mixes, and dead space in the breathing apparatus was minimal; but data from an earlier study (1)
indicated that, at depth, some divers breathed
less than others during similar exertion. Divers who breathed much less probably did not eliminate CO2
adequately. This was of particular concern from the standpoint of susceptibility to oxygen
convulsions. CO2 excess increases brain blood flow, and that increases the "dose" of oxygen to the brain.
Lanphier and Dwyer experimentally verified that some EDU divers breathed less than others during equivalent
work. They sampled end-tidal gas, or the last gas breathed out in a normal expiration, ideally consisting only of
alveolar gas. This provided an estimate of levels of CO2 in arterial blood. At depth, end-tidal CO2 was definitely
high in certain individuals, particularly when N2-O2
mixtures were used (2). It is sometimes possible, however, for end-tidal CO2 samples to overestimate arterial
levels with certain breathing patterns, most notably slow, deep breathing. For this reason, studies using end-tidal
gas readings should cross-verify against arterial samples, as was done in this study.
An independent study in 1995 repeated the EDU conditions and confirmed the results. Investigators looked at
CO2 retention during hyperbaric exercise while breathing 40/60 nitrox. They determined that CO2 retention "is
not expected to be globally aggravated by breathing nitrox down to 30 meters, but that some individuals could be
so affected." (3)
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STARTLING RESULTS WITH HELIUM-OXYGEN MIXTURES
Continued work it made it clear that while breathing nitrogen-oxygen mixtures at depth, carbon dioxide retention
occurred, whereas with helium-oxygen, ventilation was essentially unimpaired and CO2 levels stayed close to
normal. Conclusions reached following the 1956 and 1957 studies (4) included the following:
(1) Retention of carbon dioxide during working dives at moderate depth is a definite reality.
(2) Only when the breathing medium is a helium-oxygen mixture is an increase in body carbon dioxide tension
absent or small.
(3) Although increased breathing resistance and dead space both favor carbon dioxide retention, keeping these
factors to a practical minimum does not eliminate the problem.
(4) Some individuals are much more likely to develop high carbon dioxide tensions than others, but all individuals
show a tendency in this direction especially when breathing a nitrogen-oxygen mixture. There is no sharp dividing
line between "retainers" and "normals."
(5) The most effective method of minimizing the complications caused by carbon dioxide retention is to use
helium-oxygen mixtures for "mixed gas" dives.
The recommendations of Research Report 7-58 [ June, 1958] can be reproduced verbatim:
"It is recommended that:
(1) Attempts to use high-oxygen nitrogen-oxygen mixtures be abandoned as a means of reducing the
requirements of decompression.
(2) Studies leading to the use of helium-oxygen mixtures for "mixed gas" diving be carried forward as
rapidly as possible."
See figure 1: USN Experimental Diving Unit - Nitrogen-Oxygen Mixture Physiology 1955-7.
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WHY IS CO2 RETENTION A PROBLEM?
As early as 1878, physiologist Paul Bert demonstrated 'auto-intoxication' of animals by their own carbon dioxide in
a super-oxygenated environment. He was also aware of the possible connection
between carbon dioxide and oxygen toxicity (5). CO2 retention at depth was once suggested as the sole cause of
nitrogen narcosis (6, 7). Another, less prominent idea, was that only CO2 retainers might suffer oxygen toxicity
during exertion more readily than others (8). Carbon dioxide retention is now viewed as a contributor to oxygen
toxicity and nitrogen narcosis, suspected as a contributor to decompression sickness, and implicated in incidents of
underwater confusion and loss of consciousness.
During World War II, British Royal Navy torpedo divers using oxygen rebreathers were passing out without
warning. The term "shallow-water blackout" was used in 1944 by Barlow and MacIntosh (9) for blackout
suspected, and later confirmed, from too high CO2 levels, or hypercapnia. It was termed "shallow-water" because
oxygen rebreathers could not be used in deep water because of their high oxygen content.
Most of the cases weren't deep enough to have been O2 toxicity, which had previously been the prime suspect.
The problem subsided after improving carbon dioxide absorption canisters. Although the term "shallow water
blackout" had the established meaning of CO2 retention-induced blackout, it was later applied to unconsciousness
from too low oxygen, or hypoxia, in breath-hold diving, especially following excessive hyperventilation. The mix-up
has continued into common use.
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NORMAL CO2 PRODUCTION AND REMOVAL
Normally, arterial CO2 is held, almost without exception, within 3 mmHg during both rest and exercise, a very
tight range. How does your body do this? How much, and how deeply you breathe, is regulated by your arterial
oxygen pressure, carbon dioxide tension, pH, by reflexes in your lung and chest wall, and through control by your
brain.
Having not enough oxygen in your breathing mixture enhances the ventilatory drive; there is a hypoxic drive to
breathe. CO2 is an even more profound respiratory stimulant. Of all the various inputs, your arterial CO2 is the
most influential. Rising production of CO2 with exercise increases how much and how fast you breathe,
regulating your CO2, so that CO2 does not normally rise at all, even during heavy exercise.
In the normal population, CO2 is also constant at rest, only rising a bit during sleep. An important exception
involves the condition of sleep-apnea. Sleep apnea is a sleep disorder involving snoring, in which the snorer stops
breathing during sleep because of upper airway obstruction, resulting in repeated shortage of oxygen to the brain.
Carbon dioxide levels rise, due to absence of ventilation
for varying periods, sometimes hundreds of times per night. Sleep apnea sufferers are often overweight, heavy
necked males. For long-term treatment, losing weight is often very effective.
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MECHANISMS OF CO2 RETENTION
Normally, no great rise in your CO2 level occurs during rest or exercise. Sometimes it does rise, however. Why is
this? Several variables seem to impair the CO2 response during underwater work. Lanphier found three main
contributors: Having high partial pressures of inspired oxygen (elevated PiO2), inadequate ventilatory response
during exertion, and increased work of breathing (10).
High PiO2 decreases ventilation in some situations. Lanphier found that increased inspiratory oxygen pressure
accounts for about 25 percent of the elevation of CO2 at the end of exhalation. Lambertsen ( 11) demonstrated
that exercise while breathing hyperbaric oxygen decreases ventilation significantly. Other authors find that at a
given work rate below the anaerobic threshold, (steady-state exercise) ventilation is not appreciably different
between 100 percent O2 breathing, and air breathing (12, 13, 14). Your respiratory centers respond to CO2 to the
extent that it keeps things
level whether working or at rest, with some modifications. Working hard enough to produce lactic acid will
change that to compensate for the metabolic acidosis, but high inspired oxygen levels knock out the
chemoreceptor response to lactic acid, which helps explain CO2 retention in working divers who at least are
verging on anaerobic threshold. Most of the elevation of partial pressures of carbon dioxide, or PC02, in the blood
is accounted for by the increased work of breathing at depth.
Work of breathing is made more difficult by the higher gas density at depth. Your body compensates by reducing
ventilation - easily demonstrated by trying to breathe through a narrow tube. In a 1977 study of tolerance to
various gases at extreme densities, Lambertsen found a "prominent reduction of total and alveolar ventilation (15).
Response was unrelated to any narcotic properties of the gases in questions, demonstrating that ventilatory
suppression was not a function of narcotic depression. It was the gas density and work of breathing limited
pulmonary function. The early work at EDU seemed to show that the critical factor in the CO2 problems was the
higher gas
density of the nitrogen mixtures compared to helium mixtures.
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WHY CO2 ACCLIMATIZATION?
Ordinarily, rising levels of CO2 produce an increasingly uncomfortable desire to breathe more. However, there is
a great range of response. Some people have a normal response, others are remarkable in retaining CO2 to a
large extent; they just don't have much response to CO2. The question behind carbon dioxide retention is, why do
some subjects not increase ventilation to regulate their rising CO2 levels?
There is evidence that the tendency to retain CO2 increases with chronic exposure to high CO2 environments,
such as those encountered during specific diving situations. The body gets used to higher levels, allowing them to
occur without the usual autoregulation that would correct the situation.
In the first EDU studies, almost all of the subjects had been experienced "hard hat" divers. The volumes of air
needed for adequate ventilation of a helmet are very great, particularly at significant
depth. Adequate ventilation of a helmet is unlikely, so acclimatization to CO2 may have been an occupational
necessity.
Divers often had other reasons for repeated elevation of their arterial PCO2 such as repeated deep breath-hold
diving in submarine escape training. Schaefer (16) found that submarine escape tank instructors retained more
CO2 than the average untrained man. He suggested a possible adaptation effect. Kerem (17) found that both
diver and non-diver subjects exhibited similar resting CO2 arterial levels, but when exercising, arterial CO2 was
higher in divers. This was confirmed in a later study of CO2 retention during nitrox breathing (3). MacDonald and
Pilmanis (18) found a moderate, consistent elevated CO2 level and characteristic hypoventilation in all 10 male
divers tested on open-circuit scuba during open-water dives.
There may be some sort of selection, where those who tolerated high CO2 levels via a blunted chemoreceptor or
other adaptive response, self-select to continue with their diving career. That situation must be less prevalent
today, so the number of CO2-tolerant divers from that source may be considerably smaller. Perhaps, a number of
the CO2-retaining divers are sleep-apneics, who routinely experience high carbon dioxide levels during sleep. The
large, heavy, body types of many divers suggests this.
In some cases, CO2 retention occurs in subjects with no experience with high-CO2 environments, but who may
be exposed in other ways, most notably a learned adaptation from breathing patterns that regularly produce
elevated internal CO2 levels. When scuba diving first became prevalent, "skip breathing" was often taught or
popularized by word of mouth as a means of conserving the air supply in open-circuit scuba.
Educational efforts to discourage skip breathing have had some effect, so it is likely that fewer divers have
become CO2-tolerant in this way. Some CO2 retainers lack any history of probable acclimatization. There are a
few individuals who retain CO2 with no suggestion that this is an adaptive response. A 1995 study by Clark (19)
found increased levels of arterial CO2 with increasing exertion in normal subjects exposed to 2 atmospheres of
oxygen on dry land.
Still, CO2 acclimatization is not as cut-and-dried as it may sound. A recent book on the control of respiration (20)
makes this statement: "... significant, sustained CO2 retention is extremely rare in health, even under the most
extreme conditions of exercise intensity and flow limitation." One of the editors, Jerome Dempsey, acknowledges
that this statement does not necessarily apply to individuals who have had some reason for adaptation to CO2.
Dempsey (21) says that in a career of exercise-related research, he has encountered only one or two individuals
who would be classified as "CO2 retainers" in terms of our definition.
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IDENTIFICATION OF RETAINERS
Many attempts have been made to identify carbon dioxide retainers. Such people could be at unexpected risk of
CO2 blackout, unusual degrees of nitrogen narcosis, or susceptibility to oxygen toxicity. Identification, for that
reason, would be a helpful screening.
The main hope at EDU originally was that outstanding CO2 retainers could be identified and kept from hazardous
exposures. If so, others could take advantage of the benefits of nitrox diving. A dry-land test of ventilatory
response to various levels of inspired CO2 was set up ( 3). There was a great spread of results, which were
compared with the CO2 levels that the divers developed spontaneously at depth. In about 60 percent of cases,
high CO2 at depth corresponded to low response to inspired CO2; but in remaining 40 percent, such a relationship
was not seen. The correlation was not good enough for a fair, reliable selection test.
See figure 2: USN Experimental Diving Unit Carbon Dioxide Response Study 1957
In other work involving tethered swimming at submaximal work rate, 11 of 19 subjects developed elevated CO2
levels. A CO2 rebreathing test did not clearly identify these people, leading to the conclusion that identification of
CO2 retainers may require a test with exercise (22). A tethered fin-swimming test is an example.
David Elliott recommends screening tests be developed for compressed air divers for working divers doing heavy
work deeper than 120 feet who might be at risk of unconsciousness (23). There seems there is no easy, reliable
method of identifying retainers in advance. However, unusually low air-use rates would arouse our suspicions.
The need for better and more accurate tests is evident.
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AVOIDING CO2 RETENTION
If the solution of the CO2 retention problem does not lie in personnel selection, what other avenues are open?
Avoiding "skip breathing" and any other attempt to conserve air seems obvious, but this may be easier to
recommend than to accomplish. Providing ventilatory assistance to divers may deserve investigation.
Another solution would be to use He-O2 mixtures instead of N2-O2. There is work supporting that CO2 retention
is minimal or non-existent when the breathing medium is a helium-oxygen mixture (2, 4) (e.g., 7-55 & 7-58). In
the probable range of depths and times, helium should not be much less desirable than N2-O2 from the standpoint
of decompression. Some advantages of nitrox would be lost if heliox were to be adopted, but safety may be
considered a deciding factor.
The material in this article was presented at the 13th Meeting of the United States - Japan Cooperative
Program in Natural Resources (UJNR) Panel on Diving Physiology in Yokosuka, Japan, 23-25 October
1995.
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LITERATURE CITED
1. Report of the Cooperative Underwater Swimmer Project (CUSP). (Jan 1953) National Research Council
Committee on Amphibious Operations Report NRC:CAO:0033.
2. Lanphier EH. (1955). Nitrogen-Oxygen Mixture Physiology, Phases I and 2. Formal Report 7-55, Washington:
Navy Experimental Diving Unit.
3. Kerem D, Daskalovic YI, Arieli R, Shupak A. (1995). CO2 retention during hyperbaric exercise while
breathing 40/60 nitrox. Undersea & Hyperbaric Medicine 22(4): 339-346.
4. Lanphier EH. (June 1958). Nitrogen-Oxygen Mixture Physiology, Phases 4 and 6. Research Report 7-58.
Navy Experimental Diving Unit. Panama City, Florida 32407.
5. Bert P. (1878) La Pression Marometrique. G. Masson, Paris.
6. Bean JW. (1950). Tensional changes of alveolar gas in reactions too rapid compression and decompression and
question of nitrogen narcosis. Am J Physiol 16, 417-425.
7. Seusing J and Drube HC. (1960). The significance of hypercapnia for the occurrence of depth intoxication.
Klin Wschr 38, 1088-1090.
8. Lambertsen CJ, Owen SG, Wendel H, Stroud MW, Lurie AA, Lochner W, and Clark GF. (1959). Respiratory
cerebral circulatory control during exercise at 0.21 and 2.0 atmospheres inspired PO2. J Applied Physiol 14,
966-982.
9. Barlow HB, and MacIntosh FC. (1944). Shallow water black-out. Royal Navy Physiological Laboratory Report
R.N.P. 44/125 UPS 48a.
10. Lanphier, EH, Lambertsen CJ, Funderbunk LR. (1956). Nitrogen- oxygen mixture physiology Phase 3. End
tidal gas sampling system carbon dioxide regulation in divers carbon dioxide sensitivity tests. Research report
2-56. Dept of the Navy. Navy Experimental Diving Unit. Panama City, Florida 32407.
11. Lambertsen CJ. (1955). Respiratory and circulatory action of high oxygen pressure. Proc. Underwater
Physiol. Symposium. Pubn. 377, Nat. Ac Sc & Nat Res C. Washington, DC.
12. Asmussen E and Nielsen M. (1946). Studies on the regulation of respiration in heavy work Acta Physiol
Scand. 12, 171-178.
13. Wasserman K. (1976). Testing regulation of ventilation with exercise. Chest, 70, 173S-178S.
14. Welch, Mullin, Wilson, and Lewis. (1974). Effects of breathing O2-enriched mixtures on metabolic rate during
exercise. Med Sci Sports, 6, 26-32.
15. Lambertsen CJ, Gelfand R, Peterson R, Strauss R, Wright WB, Dickson JG, Puglia C, and Hamilton RW.
Human tolerance to He, Ne, and N2 at respiratory gas densities equivalent to He-O2 breathing at depths to 1200,
2000, 3000, 4000, and 5000 feet of sea water (predictive studies III). Aviat, Space and Env Med. 48 (9): 843-855.
16. Schaefer KE (1965). Adaptation to breath-hold diving. In Physiology of breath-hold diving and the Ama of
Japan. Pub 1342, p 237-251, NRC-NAS, Washington, DC.
17. Kerem D, Melamed Y and Moran A. (1980). Alveolar PCO2 during rest and exercise in divers and
non-divers breathing O2 at 1 ATA. Undersea Biomed Res 7, 17-26.
18. MacDonald JW and Pilmanis AA. (1980). Carbon Dioxide retention with underwater work in the open ocean.
In The Unconscious Diver. 25th Undersea Medical Society Workshop Madison Wisconsin 18-20 September
1980. E.H. Lanphier (ed). UMS Bethesda, MD.
19. Clark JM, Gelfand R, Lambertsen CJ, Stevens WC, Beck, G. Jr., and Fisher DG. (1995). Human tolerance
and physiological responses to exercise while breathing oxygen at 2.0 ATA. Aviat. Space, Environ. Med. 66:
336-345.
20. Dempsey J, and A Pack, Editors. (1995). Regulation of Breathing. Second Edition. Marcel Deckker, Inc. NY,
Basel, Hong Kong.
21. Dempsey, Jerome. Personal communication, August 1995.
22. Hashimoto, A, Daskalovic L, Reddan WG, and Lanphier EH. (1981). Detection and modification of CO2
retention in divers. Undersea Biomed Res (Suppl.) 8, 47 (abstract 68).
23. Elliott D. (1990) Loss of consciousness underwater. In Diving Accident Management: Proc. Forty-first
Undersea and Hyperbaric Medical Society Workshop, pp 301-310, Durham, NC.
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