Bone blood flow is influenced by muscle contractions
ABSTRACT
Forces acting on the skeleton could be divided into those originating from gravitational loading and those originating from muscle loading. Flat bones in a non-weight-baring segment of the skeleton probably experience forces mostly generated by muscle contractions. One purpose of muscle contractions is to generate blood flow within skeletal tissues. The present study aimed to investigate the pulsatile patellar bone blood flow after low and high intensity leg extension exercises. Forty-two healthy individuals volunteered for the study. Dynamic isotonic one leg extension/flexion exercises were performed in a leg extension machine. Randomly, the exercises were performed with the left or right leg with either 10 repetition maximum (10 RM) continuously without any resting periods (high intensity muscle work), or 20 RM with a 2 second rest between contractions (low intensity muscle work). The work load, expressed in kilograms totally lifted, was identical in both legs. The pulsatile patellar blood flow was recorded continuously using a photoplethysmographic technique. Blood pressure was measured continuously during muscle work by a non-invasive method (Finapress). The patellar pulsatile bone blood flow increased significantly more after high intensity muscle work (61%) compared to the same work load performed using a lower intensity (22%), p = 0.000073. Systolic blood pressure changed equally during and after both interventions. Post-exercise bone hyperaemia appears to be correlated to the intensity of muscle contractions in the muscle compartment attached to the bone.
Forces acting on the skeleton could be divided into those originating from gravitational loading and those originating from muscle loading. Flat bones in a non-weight-baring segment of the skeleton probably experience forces mostly generated by muscle contractions. One purpose of muscle contractions is to generate blood flow within skeletal tissues. The present study aimed to investigate the pulsatile patellar bone blood flow after low and high intensity leg extension exercises. Forty-two healthy individuals volunteered for the study. Dynamic isotonic one leg extension/flexion exercises were performed in a leg extension machine. Randomly, the exercises were performed with the left or right leg with either 10 repetition maximum (10 RM) continuously without any resting periods (high intensity muscle work), or 20 RM with a 2 second rest between contractions (low intensity muscle work). The work load, expressed in kilograms totally lifted, was identical in both legs. The pulsatile patellar blood flow was recorded continuously using a photoplethysmographic technique. Blood pressure was measured continuously during muscle work by a non-invasive method (Finapress). The patellar pulsatile bone blood flow increased significantly more after high intensity muscle work (61%) compared to the same work load performed using a lower intensity (22%), p = 0.000073. Systolic blood pressure changed equally during and after both interventions. Post-exercise bone hyperaemia appears to be correlated to the intensity of muscle contractions in the muscle compartment attached to the bone.
Cite this paper
nullNäslund, J. , Näslund, S. , Lundeberg, E. , Lindberg, L. and Lund, I. (2011) Bone blood flow is influenced by muscle contractions. Journal of Biomedical Science and Engineering, 4, 490-496. doi: 10.4236/jbise.2011.47062.
nullNäslund, J. , Näslund, S. , Lundeberg, E. , Lindberg, L. and Lund, I. (2011) Bone blood flow is influenced by muscle contractions. Journal of Biomedical Science and Engineering, 4, 490-496. doi: 10.4236/jbise.2011.47062.
References
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Journal of Biomechanics, 36, 1439-1451. doi:10.1016/S0021-9290(03)00241-0 [17] N?slund, J., Lindberg, L., Lundeberg, T. and Linnarsson, D. (2006) Non-invasive continuous estimation of blood flow in human patella bone. Medical & Biological Engineering & Computing, 44, 501-509. doi:10.1007/s11517-006-0070-0 [18] Kamal, A., Harness, J., Irving, G. and Mearns, A. (1989) Skin photoplethysmography—A review. Computer Me- thods and Programs in Biomedicine, 28, 257-269. doi:10.1016/0169-2607(89)90159-4 [19] Zhang, Q., Lindberg, L., Kadefors, R. and Styf, J. (2001) A noninvasive measure of changes in blood flow of the human anterior tibial muscle. European Journal of Applied Physiology, 85, 567-571. doi:10.1007/s004210100496 [20] Allen, J. (2007) Photoplethysmography and its application in clinical physiological measurement. Physiological Measurement, 28, R1-39. doi:10.1088/0967-3334/28/3/R01 [21] Turcott, R. and Pavek, T. (2008) Hemodynamic sensing using subcutaneous photoplethysmography. American Journal of Physiology. Heart and Circulatory Physiology, 295, 2560-2572. doi:10.1152/ajpheart.00574.2008 [22] N?slund, J., Waldén, M. and Lindberg, L. (2007) Decreased pulsatile blood flow in the patella in patellofemoral pain. American Journal of Sports Medicine, 35, 1668-1673. doi:10.1177/0363546507303115 [23] Polito, M., Farinattia, P., Lirad, V. and Nobregac, A. (2007) Blood pressure assessment during resistance exercise: Comparison between auscultation and finapres. Blood Pressure Monitoring, 12, 81-86. doi:10.1097/MBP.0b013e32809ef9f1 [24] Hughes, S., Cammarata, A., Steinmann, S. and Pellegrini, V. (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. [25] Br?nemark, P. (1959) Vital microscopy of bone marrow in the rabbit. Scandinavian Journal of Clinical and Laboratory Investigation. Supplementum, 11, 5-82. [26] Banfi, G., Lombardi, G., Colombini, A. and Lippi, G. (2010) Bone metabolism markers in sports medicine. Sports Medicine (Auckland, N.Z.), 40, 697-714. doi:10.2165/11533090-000000000-00000 [27] Lester, M., Urso, M., Evans, R., Pierce, J., Spiering, B., Maresh, C., Hatfield, D., Kraemer, W. and Nindl, B. (2009) Influence of exercise mode and osteogenic index on bone biomarker responses during short-term physical training. Bone, 45, 768-776. doi:10.1016/j.bone.2009.06.001 [28] Kalliokoski, K., Kemppainen, J., Larmola, K., Takala, T., Peltoniemi, P., Oksanen, A., Ruotsalainen, U., Cobelli, C., Knuuti, J. and Nuutila, P. (2000) Muscle blood flow and flow heterogeneity during exercise studied with positron emission tomography in humans. European Journal of Applied Physiology, 83, 395-401. doi:10.1007/s004210000267 [29] Recek, C. (2010) Venous pressure gradients in the lower extremity and the hemodynamic consequences. VASA. Journal for vascular diseases, 39, 292–297. [30] Boushel, R. (2010) Muscle metaboreflex control of the circulation during exercise. Acta Physiologica, 199, 367-383. doi:10.1111/j.1748-1716.2010.02133.x [31] Shim, S. and Patterson, F. (1967) A direct method of qualitative study of bone blood circulation. Surgery, Gynecology & Obstetrics, 125, 261-268. [32] Gross, P., Heistad, D. and Marcus, M. (1979) Neurohumoral regulation of blood flow to bones and marrow. American Journal of Physiology, 237, 440-448. [33] Hagblad, J., Lindberg, L., Kaisdotter-Andersson, A., Bergstrand, S., Lindgren, M., Ek-Folke, M. and Lindén, M. (2010) A technique based on laser Doppler flowmetry and photoplethysmography for simultaneously moni- toring blood flow at different tissue depths. Medical & Biological Engineering & Computing, 48, 415-422. doi:10.1007/s11517-010-0577-2 [34] Jago, J. and Murray, A. (1988) Repeatability of peripheral pulse measurements on ears, fingers and toes using photoelectric plethysmography. Clinical Physics and Physiological Measurement, 9, 319-330. doi:10.1088/0143-0815/9/4/003 [35] Hempfing, A., Schoeniger, R., Koch, P., Bischel, O. and Thomsen, M. (2007) Patellar blood flow during knee arthroplasty surgical exposure: inoperative monitoring by laser Doppler flowmetry. Journal of Orthopaedic Res- earch, 25, 1389-1394. doi:10.1002/jor.20416 [36] Mathieu, D. and Mani, R. (2007) A review of the clinical significance of tissue hypoxia measurements in lower extremity wound management. The International Journal of Lower Extremity Wounds, 6, 273-283. doi:10.1177/1534734607310299 [37] Colleran, N., Wilkerson, M., Bloomfield, S., Suva, L., Turner, R. and Delp, M. (2000) Alterations in skeletal perfusion with simulated microgravity: A possible mechanism for bone remodeling. Journal of Applied Physiology, 89, 1046-1054.
[1] Piekarski, K. and Munro, M. (1977) Transport mechanism operating between blood supply and steocytes in long bones. Nature, 269, 80-82. doi:10.1038/269080a0 [2] Fritton, S. and Weinbaum, S. (2009) Fluid and solute transport in bone: Flow-induced mechanotransduction. Annual Review of Fluid Mechanics, 41, 347-374. doi:10.1146/annurev.fluid.010908.165136 [3] Robling, A., Castillo, A. and Turner, C. (2006) Biomechanical and molecular regulation of bone remodeling. Annual Review of Biomedical Engineering, 8,455-498. doi:10.1146/annurev.bioeng.8.061505.095721 [4] Judex, S. and Carlson, K. (2009) Is bone’s response to mechanical signals dominated by gravitational loading? Medicine and Science in Sports and Exercise, 41, 2037-2043. doi:10.1249/MSS.0b013e3181a8c6e5 [5] Gross, T., Poliachik, S., Prasad, J. and Bain, S. (2010) The effect of muscle dysfunction on bone mass and morphology. Journal of Musculoskeletal & Neuronal Interactions, 10, 25-34. [6] Frost, H. (2003) Bone’s mechanostat: A 2003 update. The Anatomical Record. Part A, Discoveries in Molecular, Cellular, and Evolutionary Biology, 275, 1081-1101. doi:10.1002/ar.a.10119 [7] Hamrick, M. (2010) Basic science and mechanisms of muscle-bone interactions. Journal of Musculoskeletal & Neuronal Interactions, 10, 1-2. [8] Qin, Y. and Lam, H. (2009) Intramedullary pressure and matrix strain induced by oscillatory skeletal muscle stimulation and its potential in adaptation. Journal of Biomechanics, 42, 140-145. doi:10.1016/j.jbiomech.2008.10.018 [9] Brookes, M. and Revell, W.J. (1998) Blood supply of bone. Scientific aspects. Springer, London, 70-74, 291- 303. [10] Laughlin, H. (2005) The muscle pump. What question do we want to answer? Journal of Applied Physiology, 99, 774. doi:10.1152/japplphysiol.00578.2005 [11] Winet, H. (2003) A bone fluid flow hypothesis for muscle pump-driven capillary filtration: II proposed role for exercise in erodible scaffold implant incorporation. European Cells & Materials, 6, 1-11. [12] Qin, Y., Lam, H., Ferreri, S. and Rubin, C. (2010) Dynamic skeletal muscle stimulation and its potential in bone adaptation. Journal of Musculoskeletal & Neuronal Interactions, 10, 12-24. [13] Laughlin, H. and Joyner, M. (2003) Closer to the edge? Contractions, pressures, waterfalls and blood flow to contracting skeletal muscle. Journal of Applied Physiology, 94, 3-5. [14] Li, W., Gardinier, J., Price, C. and Wang, L. (2010) Does blood pressure enhance solute transport in bone lacunar-canalicular system? Bone, 47, 353-359. doi:10.1016/j.bone.2010.05.005 [15] Wang, L., Ciani, C., Doty, S. and Fritton, S. (2004) Delineating bone’s interstitial fluid pathway in vivo. Bone, 34, 499-509. doi:10.1016/j.bone.2003.11.022 [16] Wang, L., Fritton, S., Weinbaum, S. and Cowin, S. (2003) On bone adaption due to venous stasis. Journal of Biomechanics, 36, 1439-1451. doi:10.1016/S0021-9290(03)00241-0 [17] N?slund, J., Lindberg, L., Lundeberg, T. and Linnarsson, D. (2006) Non-invasive continuous estimation of blood flow in human patella bone. Medical & Biological Engineering & Computing, 44, 501-509. doi:10.1007/s11517-006-0070-0 [18] Kamal, A., Harness, J., Irving, G. and Mearns, A. (1989) Skin photoplethysmography—A review. Computer Me- thods and Programs in Biomedicine, 28, 257-269. doi:10.1016/0169-2607(89)90159-4 [19] Zhang, Q., Lindberg, L., Kadefors, R. and Styf, J. (2001) A noninvasive measure of changes in blood flow of the human anterior tibial muscle. European Journal of Applied Physiology, 85, 567-571. doi:10.1007/s004210100496 [20] Allen, J. (2007) Photoplethysmography and its application in clinical physiological measurement. Physiological Measurement, 28, R1-39. doi:10.1088/0967-3334/28/3/R01 [21] Turcott, R. and Pavek, T. (2008) Hemodynamic sensing using subcutaneous photoplethysmography. American Journal of Physiology. Heart and Circulatory Physiology, 295, 2560-2572. doi:10.1152/ajpheart.00574.2008 [22] N?slund, J., Waldén, M. and Lindberg, L. (2007) Decreased pulsatile blood flow in the patella in patellofemoral pain. American Journal of Sports Medicine, 35, 1668-1673. doi:10.1177/0363546507303115 [23] Polito, M., Farinattia, P., Lirad, V. and Nobregac, A. (2007) Blood pressure assessment during resistance exercise: Comparison between auscultation and finapres. Blood Pressure Monitoring, 12, 81-86. doi:10.1097/MBP.0b013e32809ef9f1 [24] Hughes, S., Cammarata, A., Steinmann, S. and Pellegrini, V. (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. [25] Br?nemark, P. (1959) Vital microscopy of bone marrow in the rabbit. Scandinavian Journal of Clinical and Laboratory Investigation. Supplementum, 11, 5-82. [26] Banfi, G., Lombardi, G., Colombini, A. and Lippi, G. (2010) Bone metabolism markers in sports medicine. Sports Medicine (Auckland, N.Z.), 40, 697-714. doi:10.2165/11533090-000000000-00000 [27] Lester, M., Urso, M., Evans, R., Pierce, J., Spiering, B., Maresh, C., Hatfield, D., Kraemer, W. and Nindl, B. (2009) Influence of exercise mode and osteogenic index on bone biomarker responses during short-term physical training. Bone, 45, 768-776. doi:10.1016/j.bone.2009.06.001 [28] Kalliokoski, K., Kemppainen, J., Larmola, K., Takala, T., Peltoniemi, P., Oksanen, A., Ruotsalainen, U., Cobelli, C., Knuuti, J. and Nuutila, P. (2000) Muscle blood flow and flow heterogeneity during exercise studied with positron emission tomography in humans. European Journal of Applied Physiology, 83, 395-401. doi:10.1007/s004210000267 [29] Recek, C. (2010) Venous pressure gradients in the lower extremity and the hemodynamic consequences. VASA. Journal for vascular diseases, 39, 292–297. [30] Boushel, R. (2010) Muscle metaboreflex control of the circulation during exercise. Acta Physiologica, 199, 367-383. doi:10.1111/j.1748-1716.2010.02133.x [31] Shim, S. and Patterson, F. (1967) A direct method of qualitative study of bone blood circulation. Surgery, Gynecology & Obstetrics, 125, 261-268. [32] Gross, P., Heistad, D. and Marcus, M. (1979) Neurohumoral regulation of blood flow to bones and marrow. American Journal of Physiology, 237, 440-448. [33] Hagblad, J., Lindberg, L., Kaisdotter-Andersson, A., Bergstrand, S., Lindgren, M., Ek-Folke, M. and Lindén, M. (2010) A technique based on laser Doppler flowmetry and photoplethysmography for simultaneously moni- toring blood flow at different tissue depths. Medical & Biological Engineering & Computing, 48, 415-422. doi:10.1007/s11517-010-0577-2 [34] Jago, J. and Murray, A. (1988) Repeatability of peripheral pulse measurements on ears, fingers and toes using photoelectric plethysmography. Clinical Physics and Physiological Measurement, 9, 319-330. doi:10.1088/0143-0815/9/4/003 [35] Hempfing, A., Schoeniger, R., Koch, P., Bischel, O. and Thomsen, M. (2007) Patellar blood flow during knee arthroplasty surgical exposure: inoperative monitoring by laser Doppler flowmetry. Journal of Orthopaedic Res- earch, 25, 1389-1394. doi:10.1002/jor.20416 [36] Mathieu, D. and Mani, R. (2007) A review of the clinical significance of tissue hypoxia measurements in lower extremity wound management. The International Journal of Lower Extremity Wounds, 6, 273-283. doi:10.1177/1534734607310299 [37] Colleran, N., Wilkerson, M., Bloomfield, S., Suva, L., Turner, R. and Delp, M. (2000) Alterations in skeletal perfusion with simulated microgravity: A possible mechanism for bone remodeling. Journal of Applied Physiology, 89, 1046-1054.