Display options
Cite
Bruce CD, Vanden Berg ER, Pfoh JR, et al. Prior oxygenation, but not chemoreflex responsiveness, determines breath-hold duration during voluntary apnea. Physiol Rep. 2021;9(1):e14664doi: 10.14814/phy2.14664.
Bruce, C. D., Vanden Berg, E. R., Pfoh, J. R., Steinback, C. D., & Day, T. A. (2021). Prior oxygenation, but not chemoreflex responsiveness, determines breath-hold duration during voluntary apnea. Physiological reports, 9(1), e14664. https://doi.org/10.14814/phy2.14664
Bruce, Christina D, et al. "Prior oxygenation, but not chemoreflex responsiveness, determines breath-hold duration during voluntary apnea." Physiological reports vol. 9,1 (2021): e14664. doi: https://doi.org/10.14814/phy2.14664
Bruce CD, Vanden Berg ER, Pfoh JR, Steinback CD, Day TA. Prior oxygenation, but not chemoreflex responsiveness, determines breath-hold duration during voluntary apnea. Physiol Rep. 2021 Jan;9(1):e14664. doi: 10.14814/phy2.14664. PMID: 33393725; PMCID: PMC7780234.
Copy Download .nbib Format: NLM
Share it on

Physiol Rep. 2021 Jan;9(1):e14664. doi: 10.14814/phy2.14664.

Prior oxygenation, but not chemoreflex responsiveness, determines breath-hold duration during voluntary apnea.

Physiological reports

Christina D Bruce, Emily R Vanden Berg, Jamie R Pfoh, Craig D Steinback, Trevor A Day

Affiliations

  1. Department of Biology, Faculty of Science and Technology, Mount Royal University, Calgary, AB, Canada.
  2. School of Health and Exercise Sciences, Centre for Heart, Lung and Vascular Health, Faculty of Health and Social Development, University of British Columbia, Kelowna, BC, Canada.
  3. Department of Biology, Faculty of Science, University of Victoria, Victoria, BC, Canada.
  4. Faculty of Kinesiology, Sport, and Recreation, University of Alberta, Edmonton, AB, Canada.

PMID: 33393725 PMCID: PMC7780234 DOI: 10.14814/phy2.14664

Abstract

Central and peripheral respiratory chemoreceptors are stimulated during voluntary breath holding due to chemostimuli (i.e., hypoxia and hypercapnia) accumulating at the metabolic rate. We hypothesized that voluntary breath-hold duration (BHD) would be (a) positively related to the initial pressure of inspired oxygen prior to breath holding, and (b) negatively correlated with respiratory chemoreflex responsiveness. In 16 healthy participants, voluntary breath holds were performed under three conditions: hyperoxia (following five normal tidal breaths of 100% O

© 2021 The Authors. Physiological Reports published by Wiley Periodicals LLC on behalf of The Physiological Society and the American Physiological Society.

Keywords: breath-hold duration; hypoxic ventilatory response; oxygen; peripheral respiratory chemoreflex; respiratory chemoreceptors; steady-state chemoreflex drive

References

  1. Ainslie, P. N., & Duffin, J. (2009). Integration of cerebrovascular CO2 reactivity and chemoreflex control of breathing: Mechanisms of regulation, measurement, and interpretation. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, 296(5), R1473-R1495. - PubMed
  2. Ainslie, P. N., Lucas, S. J., & Burgess, K. R. (2013). Breathing and sleep at high altitude. Respiratory Physiology & Neurobiology, 188, 233-256. https://doi.org/10.1016/j.resp.2013.05.020 - PubMed
  3. Ainslie, P. N., Shaw, A. D., Smith, K. J., Willie, C. K., Ikeda, K., Graham, J., & Macleod, D. B. (2014). Stability of cerebral metabolism and substrate availability in humans during hypoxia and hyperoxia. Clinical Science (London), 126(9), 661-670. - PubMed
  4. Alpher, V. S., Nelson, R. B., & Blanton, R. L. (1986). Effects of cognitive and psychomotor tasks on breath-holding span. Journal of Applied Physiology, 1149, 1152. https://doi.org/10.1152/jappl.1986.61.3.1149 - PubMed
  5. Bain, A. R., Barak, O. F., Hoiland, R. L., Drvis, I., Bailey, D. M., Dujic, Z., Mijacika, T., Santoro, A., DeMasi, D. K., MacLeod, D. B., & Ainslie, P. N. (2017). Forced vital capacity and not central chemoreflex predicts maximal hyperoxic breath-hold duration in elite apneists. Respiratory Physiology & Neurobiology, 242, 8-11. - PubMed
  6. Borle, K. J., Pfoh, J. R., Boulet, L. M., Abrosimova, M., Tymko, M. M., Skow, R. J., Varner, A., & Day, T. A. (2017). Intra-individual variability in cerebrovascular and respiratory chemosensitivity: Can we characterize a chemoreflex “reactivity profile”? Respiratory Physiology & Neurobiology, 242, 30-39. https://doi.org/10.1016/j.resp.2017.02.014 - PubMed
  7. Bruce, C. D., Saran, G., Pfoh, J. R., Leacy, J. K., Zouboules, S. M., Mann, C. R., Peltonen, J. D. B., Linares, A. M., Chiew, A. E., O’Halloran, K. D., Sherpa, M. T., & Day, T. A. (2018). What is the point of the peak? Assessing steady-state chemoreflex drive in high attitude field studies. InGauda, E. (Ed.). Arterial chemoreceptors: New directions and translational perspectives. Advances in Experimental Medicine and Biology. vol. 1071, Chapter 2. : Springer. - PubMed
  8. Bruce, C. D., Steinback, C. D., Chauhan, U. V., Pfoh, J. R., Abrosimova, M., Vanden Berg, E. R., Skow, R. J., Davenport, M. H., & Day, T. A. (2016). Quantifying cerebrovascular reactivity in anterior and posterior cerebral circulations during voluntary breath holding. Experimental Physiology, 101(12), 1517-1527. - PubMed
  9. Campbell, E. J., Freedman, S., Clark, T. J., Robson, J. G., & Norman, J. (1966). Effect of curarisation on breath-holding time. Lancet, 2(7456), 207. - PubMed
  10. Campbell, E. J., Freedman, S., Clark, T. J., Robson, J. G., & Norman, J. (1967). The effect of muscular paralysis induced by tubocurarine on the duration and sensation of breath-holding. Clinical Science, 32(3), 425-432. - PubMed
  11. Campbell, E. J., Godfrey, S., Clark, T. J., Freedman, S., & Norman, J. (1969). The effect of muscular paralysis induced by tubocurarine on the duration and sensation of breath-holding during hypercapnia. Clinical Science, 36(2), 323-328. - PubMed
  12. Davidson, J. T., Whipp, B. J., Wasserman, K., Koyal, S. N., & Lugliani, R. (1974). Role of carotid bodies in breath holding. New England Journal of Medicine, 290, 819-822. - PubMed
  13. Douglas, N. J., White, D. P., Weil, J. V., Pickett, C. K., & Zwillich, C. W. (1982). Hypercapnic ventilatory response in sleeping adults. American Review of Respiratory Disease, 126, 758-762. - PubMed
  14. Dujic, Z., & Breskovic, T. (2012). Impact of breath holding on cardiovascular respiratory and cerebrovascular health. Sports Medicine, 42, 459-472 - PubMed
  15. Dujic, Z., Breskovic, T., & Bakovic, D. (2013). Breath-hold diving as a brain survival response. Journal of Translational Neuroscience, 4, 302-313. - PubMed
  16. Engan, H., Richardson, M. X., Lodin-Sundström, A., van Beekvelt, M., & Schagatay, E. (2013). Effects of two weeks of daily apnea training on diving response, spleen contraction, and erythropoiesis in novel subjects. Scandinavian Journal of Medicine and Science in Sports, 23, 340-348. - PubMed
  17. Engel, G. L., Ferris, E. B., Webb, J. P., & Stevens, C. D. (1946). Voluntary Breathholding. II. The relation of the maximum time of breathholding to the oxygen tension of the inspired air. Journal of Clinical Investigation, 25(5), 729-733. - PubMed
  18. Feiner, J. R., Bickler, P. E., & Severinghaus, J. W. (1995). Hypoxic ventilatory response predicts the extent of maximal breath-holds in man. Respiration Physiology, 100, 213-222. - PubMed
  19. Ferris, E. B., Engel, G. L., Stevens, C. D., & Webb, J. (1946). Voluntary breathholding. III. The relation of the maximum time of breathholding to the oxygen and carbon dioxide tensions of arterial blood, with a note on its clinical and physiological significance. Journal of Clinical Investigation, 25(5), 734-743. https://doi.org/10.1172/jci101757 - PubMed
  20. Fitzgerald, R. S., & Parks, D. C. (1971). Effect of hypoxia on carotid chemoreceptor response to carbon dioxide in cats. Respiration Physiology, 12, 218-229. - PubMed
  21. Flume, P. A., Eldridge, F. L., Edwards, L. J., & Houser, L. M. (1994). The Fowler breathholding study revisited: Continuous rating of respiratory sensation. Respiration Physiology, 95(1), 53-66. - PubMed
  22. Fowler, W. S. (1954). Breaking point of breath-holding. Journal of Applied Physiology, 6(9), 539-545. - PubMed
  23. Godfrey, S., & Campbell, E. J. (1968). The control of breath holding. Respiratory Physiology, 5, 385-400. - PubMed
  24. Godfrey, S., & Campbell, E. J. M. (1969). Mechanical and chemical control of breath holding. Journal of Experimental Physiology and Cognate Medical Sciences, 54, 117-128. - PubMed
  25. Goncharov, A. O., Dyachenko, A. I., Shulagin, Y. A., & Ermolaev, E. S. (2017). Mathematical modeling of a chemoreceptor mechanism and the breakpoint of breath holding and experimental evaluation of the model. Biophysics, 62(4), 650-656. - PubMed
  26. Guz, A., Noble, M. I. M., Widdicombe, J. G., Trenchard, D., Mushin, W. W., & Makey, A. R. (1966). The role of vagal and glossopharyngeal afferent nerves in respiratory sensation, control of breathing and arterial pressure regulation in conscious man. Clinical Science, 30, 161-170. - PubMed
  27. Hagbarth, K. E., & Vallbo, A. B. (1968). Pulse and respiratory grouping of sympathetic impulses in human muscle nerves. Acta Physiologica Scandinavica, 74(1-2), 96-108. - PubMed
  28. Joulia, F., Lemaitre, F., Fontanari, P., Mille, M. L., & Barthelemy, P. (2009). Circulatory effects of apnoea in elite breath-hold divers. Acta Physiologica, 197(1), 75-82. - PubMed
  29. Kiwull-Schone, H., Kiwull, P., Muckenhoff, K., & Both, W. (1976). The role of carotid chemoreceptors in the regulation of arterial oxygen transport under hypoxia with and without hypercapnia. Advances in Experimental Medicine and Biology, 75, 469-476. - PubMed
  30. Klocke, F. J., & Rahn, H. (1959). Breath holding after breathing of oxygen. Journal of Applied Physiology, 14, 689-693. - PubMed
  31. Lahiri, S., & DeLaney, R. G. (1975). Stimulus interaction in the responses of carotid body chemoreceptor single afferent fibers. Respiration Physiology, 24(3), 249-266. - PubMed
  32. Lahiri, S., Mokashi, A., DeLaney, R. G., & Fishman, A. P. (1978). Arterial PO2 and PCO2 stimulus threshold for carotid chemoreceptors and breathing. Respiration Physiology, 34, 359-375. - PubMed
  33. Leacy, J. K., Linares, A. M., Zouboules, S. M., Rampuri, Z. H., Bird, J. D., Herrington, B. A., Mann, L. M., Soriano, J. E., Thrall, S. F., Kalker, A., Brutsaert, T. D., O'Halloran, K. D., Sherpa, M. T., & Day, T. A. (2020). Cardiorespiratory hysteresis during incremental high-altitude ascent-descent quantifies the magnitude of ventilatory acclimatization. Experimental Physiology. Epub ahead of print. https://doi.org/10.1113/EP088488 - PubMed
  34. Lin, Y. C. (1982). Breath-hold diving in terrestrial mammals. Exercise and Sport Sciences Reviews, 10, 270-307. - PubMed
  35. Lin, Y. C., Lally, D. A., Moore, T. A., & Hong, S. K. (1974). Physiological and conventional breath-hold break points. Journal of Applied Physiology, 37, 291-296. - PubMed
  36. López-Barneo, J., González-Rodríguez, P., Gao, L., Fernández-Agüera, M. C., Pardal, R., & Ortega-Sáenz, P. (2016). Oxygen sensing by the carotid body: Mechanisms and role in adaptation to hypoxia. American Journal of Physiology. Cell Physiology, 310(8), C629-C642. - PubMed
  37. Macnutt, M. J., De Souza, M. J., Tomczak, S. E., Homer, J. L., & Sheel, A. W. (2012). Resting and exercise ventilatory chemosensitivity across the menstrual cycle. Journal of Applied Physiology, 112(5), 737-747. - PubMed
  38. Mathew, L., Gopinathan, P. M., Purkayastha, S. S., Gupta, J. S., & Nayar, H. S. (1983). Chemoreceptor sensitivity and maladaptation to high altitude in man. European Journal of Applied Physiology, 51(1), 137-144. - PubMed
  39. Messineo, L., Taranto-Montemurro, L., Azarbarzin, A., Oliveira Marques, M. D., Calianese, N., White, D. P., Wellman, A. & Sands, A. S. (2018). Breath-holding as a means to estimate the loop gain contribution to obstructive sleep apnoea. Journal of Physiology, 596(17), 4043-4056. - PubMed
  40. Nielsen, M., & Smith, H. (1952). Studies on the regulation of respiration in acute hypoxia; with an appendix on respiratory control during prolonged hypoxia. Acta Physiologica Scandinavia., 24(4), 293-313. - PubMed
  41. Parkes, M. J. (2006). Breath-holding and its breakpoint. Experimental Physiology, 91(1), 1-15. - PubMed
  42. Pedersen, M. E. F., Fatemian, M., & Robbins, P. A. (1999). Identification of fast and slow ventilatory responses to carbon dioxide under hypoxic and hyperoxic conditions in humans. Journal of Physiology, 521(1), 273-287. - PubMed
  43. Pfoh, J. R., & Day, T. A. (2016). Considerations for the use of transient tests of the peripheral chemoreflex in humans: The utility is in the question and the context. Experimental Physiology, 101(6), 778-779. - PubMed
  44. Pfoh, J. R., Steinback, C. D., Vanden Berg, E. R., Bruce, C. D., & Day, T. A. (2017). Assessing chemoreflexes and oxygenation in the context of acute hypoxia: Implications for field studies. Respiratory Physiology & Neurobiology, 246, 67-75. - PubMed
  45. Pfoh, J. R., Tymko, M. M., Abrosimova, M., Boulet, L. M., Foster, G. E., Bain, A. R., Ainslie, P. N., Steinback, C. D., Bruce, C. D., & Day, T. A. (2016). Comparing and characterizing transient and steady-state tests of the peripheral chemoreflex in humans. Experimental Physiology, 101, 432-447. - PubMed
  46. Rebuck, A. S., Kangalee, M., Pengelly, L. D., & Campbell, E. J. (1973). Correlation of ventilatory responses to hypoxia and hypercapnia. Journal of Applied Physiology, 35, 173-177. - PubMed
  47. Severinghaus, J. W. (1979). Simple, accurate equations for human blood O2 dissociation computations. Journal of Applied Physiology: Respiratory, Environmental and Exercise Physiology, 46(3), 599-602. - PubMed
  48. Severinghaus, J. W., Bainton, C. R., & Carcelen, A. (1966). Respiratory insensitivity to hypoxia in chronically hypoxic man. Respiration Physiology, 1(3), 308-334. - PubMed
  49. Sin, D., Fitzgerald, F., Parker, J., Newton, G., Floras, J., & Bradley, T. (1999). Risk factors for central and obstructive sleep apnea in 450 men and women with congestive heart failure. American Journal of Respiratory and Critical Care Medicine, 160, 1101-1106. - PubMed
  50. Skow, R. J., Day, T. A., Fuller, J. E., Bruce, C. D., & Steinback, C. D. (2015). The ins and outs of breath holding: simple demonstrations of complex respiratory physiology. Advances in Physiology Education, 39(3), 223-231. - PubMed
  51. Smith, K. J., MacLeod, D., Willie, C. K., Lewis, N. C., Hoiland, R. L., Ikeda, K., Tymko, M. M., Donnelly, J., Day, T. A., MacLeod, N., Lucas, S. J., & Ainslie, P. N. (2014). Influence of high altitude on cerebral blood flow and fuel utilization during exercise and recovery. Journal of Physiology, 592(24), 5507-5527. - PubMed
  52. Solin, P., Roebuck, T., Johns, D. P., Walters, E. H., & Naughton, M. T. (2000). Peripheral and central ventilatory responses in central sleep apnea with and without congestive heart failure. American Journal of Respiratory and Critical Care Medicine, 162(6), 2194-2200. - PubMed
  53. Steinback, C. D., & Poulin, M. J. (2007). Ventilatory responses to isocapnic and poikilocapnic hypoxia in humans. Respiratory Physiology & Neurobiology, 155(2), 104-113. - PubMed
  54. Steinback, C. D., & Poulin, M. J. (2008). Cardiovascular and cerebrovascular responses to acute isocapnic and poikilocapnic hypoxia in humans. Journal of Applied Physiology, 104(2):482-489. - PubMed
  55. Steinback, C. D., Salzer, D., Medeiros, P. J., Kowalchuk, J., & Shoemaker, J. K. (2009). Hypercapnic vs. hypoxic control of cardiovascular, cardiovagal, and sympathetic function. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, 296(2), R402-R410. - PubMed
  56. Trembach, N., & Zabolotskikh, I. (2017). Breath-holding test in evaluation of peripheral chemoreflex sensitivity in healthy subjects. Respiratory Physiology & Neurobiology, 235, 79-82. - PubMed
  57. Trivedi, N. S., Ghouri, A. F., Shah, N. K., Lai, E., & Barker, S. J. (1997). Pulse oximeter performance during desaturation and resaturation: A comparison of seven models. Journal of Clinical Anesthesia, 9(3), 184-188. - PubMed
  58. van Beek, J. H., Berkenbosch, A., De Goede, J., & Olievier, C. N. (1983). Influence of peripheral O2 tension on the ventilatory response to CO2 in cats. Respiration Physiology, 51, 379-390. - PubMed
  59. Willie, C. K., Macleod, D. B., Shaw, A. D., Smith, K. J., Tzeng, Y. C., Eves, N. D., Ikeda, K., Graham, J., Lewis, N. C., Day, T. A., & Ainslie, P. N. (2012). Regional brain blood flow in man during acute changes in arterial blood gases. Journal of Physiology, 590(14), 3261-3275. - PubMed

Publication Types