Bone and Soft Tissue Blood Flow during Normobaric and Hyperbaric Oxygen Breathing in Healthy Divers

Agneta C. Larsson^1,2, Johan Uusijärvi^1,2, Jan E. Näslund¹, Iréne Lund¹, Peter Lindholm^1,3

¹Department of Physiology and Pharmacology, Karolinska Institute, Stockholm, Sweden.
²Department of Anaesthesia & Intensive Care, Division of Hyperbaric Medicine, Karolinska Hospital, Stockholm, Sweden.
³Department of Radiology, Karolinska Hospital, Stockholm, Sweden.

DOI: 10.4236/jbise.2014.712094                

Abstract

Purpose: The study aimed to investigate, using a photoplethysmographic (PPG) technique, how pulsatile blood flow within the patellar bone and skin over the patella reacts to normobaric (NBO) and hyperbaric oxygen breathing (HBO). Methods: Eleven healthy volunteers, breathed air or oxygen. Subjects were blinded to breathing gas. A range of partial pressures of oxygen were administered in 10 minute intervals: 21 kPa, 101 kPa (NBO), 21 kPa, (compression to 280 kPa), 59 kPa, 280 kPa (HBO), 59 kPa, (decompression), and 21 kPa. Changes were measured continuously for each individual. Results: Hyperoxia decreased pulsatile patellar blood flow ~32 resp. 38% and skin blood flow ~36 resp. 42% during the first 2 - 3 minutes of NBO resp. HBO. This decrease was normalized within 5 minutes after exposure. The results were similar when switching from air to NBO (101 kPa) and from air at pressure (59 kPa) to HBO (280 kPa). Conclusions: The study shows that pulsatile patellar skin and bone blood flow, decreases significantly as a reaction to oxygen breathing in healthy subjects. The results suggest that a non-invasive PPG technique could be used to monitor blood flow changes in bone during oxygen treatment.

Keywords

Photopletysmography, Hyperbaric Oxygen, Bone, Osteomyelitis, Blood Flow

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	Brinker, M.R., Lippton, H.L., Cook, S.D. and Hyman, A.L. (1990) Pharmacological Regulation of the Circulation of Bone. The Journal of Bone and Joint Surgery, 72A, 964-975.
[2]	Frost, M.L., C.G., Blake, G.M., Marsden, P.K., Benatar, N.A. and Fogelman, I. (2003) A Prospective Study on Regional Bone Metabolism and Blood Flow at the Lumbar Spine Measured by 18F Fluoride Positron Emission Tomography. Journal of Bone and Mineral Research, 18, 2215-2222. http://dx.doi.org/10.1359/jbmr.2003.18.12.2215
[3]	Brookes, M.R.W. (1998) Blood Supply of Bone. Springer, London. http://dx.doi.org/10.1007/978-1-4471-1543-4
[4]	Dayan, L., Keidar, Z., Israel, O., Milloul, V., Sachs, J. and Jacob, G. (2008) SPECT/CT-Plethysmography—Non-Invasive Quantitation of Bone and Soft Tissue Blood Flow. Journal of Orthopaedic Surgery and Research, 3, 36. http://dx.doi.org/10.1186/1749-799X-3-36
[5]	Shim, S.S., Copp, D.H. and Patterson, F.P. (1967) An Indirect Method of Bone Blood-Flow Measurement Based on the Bone Clearance of a Circulating Bone-Seeking Radioisotope. The Journal of Bone and Joint Surgery, 49, 693-702.
[6]	Gross, P.M., Marcus, M.L. and Heistad, D.D. (1981) Measurement of Blood Flow to Bone and Marrow in Experimental Animals by Means of the Microsphere Technique. The Journal of Bone and Joint Surgery, 63, 1028-1031.
[7]	Stuhr, L.E., Bergo, G.W. and Tyssebotn, I. (1994) Systemic Hemodynamics during Hyperbaric Oxygen Exposure in Rats. Aviation, Space, and Environmental Medicine, 65, 531-538.
[8]	Bergo, G.W. and Tyssebotn, I. (1995) Effect of Exposure to Oxygen at 101 and 150 kPa on the Cerebral Circulation and Oxygen Supply in Conscious Rats. European Journal of Applied Physiology and Occupational Physiology, 71, 475-484. http://dx.doi.org/10.1007/BF00238548
[9]	Hink, J., Thom, S.R., Simonsen, U., Rubin, I. and Jansen, E. (2006) Vascular Reactivity and Endothelial NOS Activity in Rat Thoracic Aorta during and after Hyperbaric Oxygen Exposure. American Journal of Physiology, Heart and Circulatory Physiology, 291H, 1988-1998. http://dx.doi.org/10.1152/ajpheart.00145.2006
[10]	Rousseau, A., Steinwall, I., Woodson, R.D. and Sjoberg, F. (2007) Hyperoxia Decreases Cutaneous Blood Flow in High-Perfusion Areas. Microvascular Research, 74, 15-22. http://dx.doi.org/10.1016/j.mvr.2007.02.001
[11]	Meirovithz, E., Sonn, J. and Mayevsky, A. (2007) Effect of Hyperbaric Oxygenation on Brain, Emodynamics, Hemoglobin Oxygenation and Mitochondrial NADH. Brain Research Reviews, 54, 294-304. http://dx.doi.org/10.1016/j.brainresrev.2007.04.004
[12]	Larsson, A., Engstrom, M., Uusijarvi, J., Kihlstrom, L., Lind, F. and Mathiesen, T. (2008) Hyperbaric Oxygen Treatment of Postoperative Neurosurgical Infections. Neurosurgery, 62, 652-671. http://dx.doi.org/10.1227/01.neu.0000316260.67220.cf
[13]	Marx, R.E. (2007) Bone and Bone Graft Healing. Oral and Maxillofacial Surgery Clinics of North America, 19, 455-466. http://dx.doi.org/10.1016/j.coms.2007.07.008
[14]	Marx, R.E., Ehler, W.J., Tayapongsak, P. and Pierce, L.W. (1990) Relationship of Oxygen Dose to Angiogenesis Induction in Irradiated Tissue. The American Journal of Surgery, 160, 519-524. http://dx.doi.org/10.1016/S0002-9610(05)81019-0
[15]	Granstrom, G., Tjellstrom, A. and Branemark, P.I. (1999) Osseointegrated Implants in Irradiated Bone: A Case-Controlled Study Using Adjunctive Hyperbaric Oxygen Therapy. Journal of Oral and Maxillofacial Surgery, 57, 493-499. http://dx.doi.org/10.1016/S0278-2391(99)90059-9
[16]	Edwards, M.L. (2010) Hyperbaric Oxygen Therapy. Part 2: Application in Disease. Journal of Veterinary Emergency and Critical Care, 20, 289-297. http://dx.doi.org/10.1111/j.1476-4431.2010.00535_1.x
[17]	Kamal, A.A., Harness, J.B., Irving, G. and Mearns, A.J. (1989) Skin Photoplethysmography—A Review. Computer Methods and Programs in Biomedicine, 28, 257-269. http://dx.doi.org/10.1016/0169-2607(89)90159-4
[18]	Zhang, Q., Lindberg, L.G., Kadefors, R. and Styf, J. (2001) A Non-Invasive Measure of Changes in Blood Flow in the Human Anterior Tibial Muscle. European Journal of Applied Physiology, 84, 448-452. http://dx.doi.org/10.1007/s004210100413
[19]	Allen, J. (2007) Photoplethysmography and Its Application in Clinical Physiological Measurement. Physiological Measurement, 28, R1. http://dx.doi.org/10.1088/0967-3334/28/3/R01
[20]	Turcott, R.G. and Pavek, T.J. (2008) Hemodynamic Sensing Using Subcutaneous Photoplethysmography. American Journal of Physiology, Heart and Circulatory Physiology, 295, H2560-H2572. http://dx.doi.org/10.1152/ajpheart.00574.2008
[21]	Naslund, J., Pettersson, J., Lundeberg, T., Linnarsson, D. and Lindberg, L.G. (2006) Non-Invasive Continuous Estimation of Blood Flow Changes in Human Patellar Bone. Medical & Biological Engineering & Computing, 44, 501-509. http://dx.doi.org/10.1007/s11517-006-0070-0
[22]	Naslund, J., Waldén, M. and Lindberg, L.G. (2007) Decreased Pulsatile Blood Flow in the Patella in Patellofemoral Pain Syndrome. The American Journal of Sports Medicine, 35, 1668-1673. http://dx.doi.org/10.1177/0363546507303115
[23]	Naslund, J.E., Naslund, S., Lundeberg, T., Linnarsson, D., Lindberg, L.G. and Lund, I. (2011) Bone Blood Flow Is Influenced by Muscle Contractions. Journal of Biomedical Science and Engineering, 4, 490-496. http://dx.doi.org/10.4236/jbise.2011.47062
[24]	Gross, P.M., Heistad, D.D. and Marcus, M.L. (1979) Neurohumoral Regulation of Blood Flow to Bones and Marrow. The American Journal of Physiology, 237, H440-H448.
[25]	Colleran, P.N., Wilkerson, M.K., Bloomfield, S.A., Suva, L.J., Turner, R.T. and Delp, M.D. (2000) Alterations in Skeletal Perfusion with Simulated Microgravity: A Possible Mechanism for Bone Remodeling. Journal of Applied Physiology, 89, 1046-1054.
[26]	Hansen, M., Jacobsen, E. and Madsen, J. (1976) Influence of Hypoxia and Hyperoxia on Subcutaneous Adipose Tissue Blood Flow in Man. Scandinavian Journal of Clinical Laboratory Investigation, 36, 655-660.
[27]	Katusic, Z.S. and Vanhoutte, P.M. (1989) Superoxide Anion Is an Endothelium-Derived Contracting Factor. The American Journal of Physiology, 257, H33-H37.
[28]	Rocco, M., Antonelli, M., Letizia, V., Alampi, D., Spadetta, G., Passariello, M., Conti, G., Serio, P. and Gasparetto, A (2001) Lipid Peroxidation, Circulating Cytokine and Endothelin 1 Levels in Healthy Volunteers Undergoing Hyperbaric Oxygenation. Minerva Anestesiologica, 67, 393-400.
[29]	Vucetic, M., Jensen, P.K. and Jansen, E.C. (2004) Diameter Variations of Retinal Blood Vessels during and after Treatment with Hyperbaric Oxygen. The British Journal of Ophthalmology, 88, 771-775. http://dx.doi.org/10.1136/bjo.2003.018788
[30]	Atochin, D.N., Demchenko, I.T., Astern, J., Boso, A.E., Piantadosi, C.A. and Huang, P.L. (2003) Contributions of Endothelial and Neuronal Nitric Oxide Synthases to Cerebrovascular Responses to Hyperoxia. Journal of Cerebral Blood Flow and Metabolism, 23, 1219-1226. http://dx.doi.org/10.1097/01.WCB.0000089601.87125.E4
[31]	Thom, S.R., Bhopale, V., Fisher, D., Manevich, Y., Huang, P.L. and Buerk, D.G. (2002) Stimulation of Nitric Oxide Synthase in Cerebral Cortex Due to Elevated Partial Pressures of Oxygen: An Oxidative Stress Response. Journal of Neurobiology, 51, 85-100. http://dx.doi.org/10.1002/neu.10044
[32]	Oriani, G., Marroni, A. and Wattel, F. (1996) Handbook of Hyperbaric Medicine. Springer, Berlin. http://dx.doi.org/10.1007/978-88-470-2198-3
[33]	Jain, K. (1999) Textbook of Hyperbaric Medicine. H & H.
[34]	Larsson, A., Uusijarvi, J., Eksborg, S. and Lindholm, P. (2010) Tissue Oxygenation Measured with Near-Infrared Spectroscopy during Normobaric and Hyperbaric Oxygen Breathing in Healthy Subjects. European Journal of Applied Physiology, 109, 757-761. http://dx.doi.org/10.1007/s00421-010-1403-0
[35]	Pedersen, P.K., Kiens, B. and Saltin, B. (1999) Hyperoxia Does Not Increase Peak Muscle Oxygen Uptake in Small Muscle Group Exercise. Acta Physiologica Scandinavica, 166, 309-318. http://dx.doi.org/10.1046/j.1365-201x.1999.00575.x
[36]	Iida, S., Harada, Y., Ikenoue, S. and Moriya, H. (1999) Measurement of Bone Marrow Blood Volume in the Knee by Positron Emission Tomography. Journal of Orthopaedic Science, 4, 216-222. http://dx.doi.org/10.1007/s007760050096
[37]	Zhen, G., Zhang, Z. and Xu, Y. (2003) The Role of Endogenous Carbon Monoxide in the Hypoxic Vascular Remodeling of Rat Model of Hypoxic Pulmonary Hypertension. Journal of Huazhong University of Science and Technology, 23, 356-368.
[38]	Hughes, S.S., Cammarata, A., Steinmann, S.P. and Pellegrini Jr., V.D. (1998) Effect of Standard Total Knee Arthroplasty Surgical Dissection on Human Patellar Blood Flow in Vivo: An Investigation Using Laser Doppler Flowmetry. Journal of the Southern Orthopaedic Association, 7, 198-204.
[39]	Hagblad, J., Lindberg, L.G., Andersson, A.K., Bergstrand, S., Lindgren, M., Ek, A.C., Folke, M. and Linden, M. (2010) A Technique Based on Laser Doppler Flowmetry and Photoplethysmography for Simultaneously Monitoring Blood Flow at Different Tissue Depths. Medical & Biological Engineering & Computing, 48, 415-422. http://dx.doi.org/10.1007/s11517-010-0577-2
[40]	Stirban, A., Lentrodt, S., Nandrean, S., Pop, A., Tschoepe, D. and Scherbaum, W.A. (2009) Functional Changes in Microcirculation during Hyperbaric and Normobaric Oxygen Therapy. Undersea & Hyperbaric Medicine: Journal of the Undersea and Hyperbaric Medical Society, Inc, 36, 381-390.