Clinical and pathogenetic significance of the microvascular component of bone tissue

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Abstract

Bone tissue’s blood circulation and microcirculation are critical to its metabolic and reparative processes. Without the participation of the bone microcirculatory tissue system, it is difficult to exchange oxygen and carbon dioxide, transport of nutrients, and excrete metabolic products. The regeneration of bone tissue is characterized by the pairing of angiogenesis and osteogenesis, which allows the use of microcirculation indicators as additional criteria for the state of reparative processes. Non-invasive approaches for detecting the state of peripheral circulation and microcirculation, which would enable assessing the dynamics of the vascular factor in bone pathology, including after fractures, are most practical in the clinic.

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About the authors

Anastasia A. Agafonova

Priorov National Medical Research Center for Traumatology and Orthopedics

Author for correspondence.
Email: nastyaloseva@yandex.ru
ORCID iD: 0000-0002-4675-4313
SPIN-code: 8341-0713

Post-Graduate Student, Traumatologist-Orthopedist, Ultrasound Diagnostic

Russian Federation, Moscow

Alexander I. Krupatkin

Priorov National Medical Research Center for Traumatology and Orthopedics

Email: ale.ale02@yandex.ru
ORCID iD: 0000-0001-5582-5200
SPIN-code: 3671-5540

MD, Dr. Sci. (Med.), Professor, Neurologist

Russian Federation, Moscow

Alexander I. Dorokhin

Priorov National Medical Research Center for Traumatology and Orthopedics

Email: a.i.dorokhin@mail.ru
ORCID iD: 0000-0003-3263-0755
SPIN-code: 1306-1729

MD, Dr. Sci. (Med.), Traumatologist-Orthopedist

Russian Federation, Moscow

References

  1. Prisby RD. Bone Marrow Microvasculature. Compr Physiol. 2020;10(3):1009–1046. doi: 10.1002/cphy.c190009
  2. Abboud C. Human bone marrow microvascular endothelial cells: Elusive cells with unique structural and functional properties. Exp Hematol. 1995;23(1):1–3.
  3. Morikawa T, Tamaki S, Fujita S, Suematsu M, Takubo K. Identification and local manipulation of bone marrow vasculature during intravital imaging. Scientific Reports. 2020;10(1):6422. doi: 10.1038/s41598-020-63533-3
  4. Acar M, Kocherlakota KS, Murphy MM, Peyer JG, Oguro H, Inra CN, Zhao Z, Luby-Phelps K, Morrison SJ. Deep imaging of bone marrow shows non-dividing stem cells are mainly perisinusoidal. Nature. 2015;526(7571):126–130. doi: 10.1038/nature15250
  5. De Saint-Georges L, Miller SC. The microcirculation of bone and marrow in the diaphysis of the rat hemopoietic long bones. Anat Rec. 1992;233(2):169–177. doi: 10.1002/ar.1092330202
  6. Kusumbe AP, Ramasamy SK, Adams RH. Coupling of angiogenesis and osteogenesis by a specific vessel subtype in bone. Nature. 2014;507(7492):323–328. doi: 10.1038/nature13145
  7. Asghar A, Kumar A, Narayan RK, Naaz S. Is the cortical capillary renamed as the transcortical vessel in diaphyseal vascularity? Anat Rec (Hoboken). 2020;303(11):2774–2784. doi: 10.1002/ar.24461
  8. Xu Z, Kusumbe AP, Cai H, Wan Q, Chen J. Type H blood vessels in coupling angiogenesis-osteogenesis and its application in bone tissue engineering. Theranostics. 2020;10(1):426–436. doi: 10.7150/thno.34126.eCollection 2020
  9. Ramasamy SK, Kusumbe AP, Itkin T, Gur-Cohen S, Lapidot T, Adams RH. Regulation of hematopoiesis and osteogenesis by blood vessel-derivedsignals. Annu Rev Cell Dev Biol. 2016;(32):649–675. doi: 10.1146/annurev-cellbio-111315-124936
  10. Grüneboom A, Hawwari I, Weidner D, Culemann S, Müller S, Henneberg S, Gunzer M. A network of trans-cortical capillaries as mainstay for blood circulation in long bones. Nat Metab. 2019;1(2):236–250. doi: 10.1038/s42255-018-0016-5
  11. Qin Q, Lee S, Patel N, Walden K, Gomes-Salazar M, Levi B, James AW. Neurovascular coupling in bone regeneration. Exp Mol Med. 2022;54(11):1844–1849. doi: 10.1038/s12276-022-00899-6
  12. Panin MA, Zagorodny NV, Abakirov MD, Boyko AV, Ananyin DA. Decompression of the femoral head necrosis focus. Literature review. N.N. Priorov Journal of Traumatology and Orthopedics. 2021;28(1):65−76. (In Russ). doi: 10.17816/vto59746
  13. Stegen S, Carmeliet G. The skeletal vascular system — Breathing life into bone tissue. Bone. 2018;(115):50–58. doi: 10.1016/j.bone.2017.08.022
  14. Schindeler A, McDonald MM, Bokko P, Little DG. Bone remodeling during fracture repair: the cellular picture. Semin. Cell Dev. Biol. 2008;19(5):459–466. doi: 10.1016/j.semcdb.2008.07.004
  15. Street J, Winter D, Wang JH, Wakai A, McGuinness A, Redmond HP. Is human fracture hematoma inherently angiogenic? Clin. Orthop. Relat. Res. 2000;(378):224–237. doi: 10.1097/00003086-200009000-00033
  16. Sivaraj KK, Adams RH. Blood vessel formation and function in bone. Development. 2016;143(15):2706–2715. doi: 10.1242/dev.136861
  17. Chim SM, Tickner J, Chow ST, Kuek V, Guo B, Zhang G, Xu J. Angiogenic factors in bone local environment. Cytokine and Growth Factor Reviews. 2013;24(3):297–310. doi: 10.1016/j.cytogfr.2013.03.008
  18. Street J, Bao M, Guzman L, Bunting S, Peale FV, Ferrara N. Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc Natl Acad Sci U. S. A. 2002;99(15):9656–9661. doi: 10.1073/pnas.152324099
  19. Maes C, Carmeliet G, Schipani E. Hypoxia-driven pathways in bone development,regeneration and disease. Nat Rev Rheumatol. 2012;8(6):358–366. doi: 10.1038/nrrheum.2012.3
  20. Meertens R, Casanova F, Knapp KM, Thorn C, Strain WD. Use of near-infrared systems for investigations of hemodynamics in human in vivo bone tissue: A systematic review. J Orthop Res. 2018;36(10):2595–2603. doi: 10.1002/jor.24035
  21. Peng H, Wright V, Usas A, Gearhart B, Shen H, Cummin J, Huard J. Synergistic enhancement of bone formation and healing by stem cell-expressed VEGF and bone morphogenetic protein-4. J Clin Invest. 2002;110(6):751–759. doi: 10.1172/JCI15153
  22. Batpenov ND, Rakhimov SK, Stepanov AA, Orazbaev DA, Manekenova KB, Smilova GK. Morphofunctional bone tissue reconstruction in periprosthetic fractures in the area of the femoral component of the endoprosthesis. N.N. Priorov Journal of Traumatology and Orthopedics. 2020;27(2):24–29. (In Russ). doi: 10.17816/vto202027224-29
  23. Mironov SP, Eskin NA, Krupatkin AI, Kesyan GA, Urazgildeev RZ, Arsenyev IG. Pathophysiological aspects of soft tissue microhemocirculation in the projection of false joints of long bones. N.N. Priorov Journal of Traumatology and Orthopedics. 2012;(4):22–26. (In Russ).
  24. Patent RUS № 2501526/20.12.2013. Mironov SP, Eskin NA, Krupatkin AI, Kesyan GA, Urazgildeev RZ, Arsenyev IG. Sposob prognozirovaniya techeniya reparativnogo osteogeneza pri hirurgicheskom lechenii lozhnyh sustavov dlinnyh trubchatyh kostej. Available from: http://allpatents.ru/patent/2501526.html?ysclid=lloy82reqc265613020 (In Russ).
  25. Shchurov VA. Dynamics of blood flow velocity through the arteries of bone regenerate limbs and cerebral blood flow when performing functional tests and changing the treatment regimen. Regional blood circulation and microcirculation. 2018;17(4):51–56. (In Russ). doi: 10.24884/1682-6655-2018-17-4-51-56
  26. Pisarev VV, Lvov SE, Vasin IV. Indicators of regional hemodynamics of the early postoperative period in osteosynthesis of fractures of the lower leg bones. Bulletin of the Ivanovo Medical Academy. 2012;17(4):34–37. (In Russ).
  27. Aziz SM, Khambatta F, Vaithianathan T, Thomas JC, Clark JM, Marshall R. A near infrared instrument to monitor relative hemoglobin concentrations of human bone tissue in vitro and in vivo. Rev Sci Instrum. 2010;81(4):043111. doi: 10.1063/1.3398450
  28. Ganse B, Bohle F, Pastor T, Gueorguiev B, Altgassen S, Gradl G, Kim B, Modabber A, Nebelung S, Hildebrand F, Knobe M. Microcirculation after trochanteric femur fractures: a prospective cohort study using non-invasive laser-doppler spectrophotometry. Front Physiol. 2019;(10):236. doi: 10.3389/fphys.2019.00236
  29. Hughes SS, Cammarata A, Steinmann SP, Pellegrini VD. Effect of standard total knee arthroplasty surgical dissection on human patellar blood flow in vivo: an investigation using laser doppler flowmetry. J South Orthop Assoc. 1998;7(3):198–204.
  30. Nicholls RL, Green D, Kuster MS. Patella intraosseous blood flow disturbance during a medial or lateral arthrotomy in total knee arthroplasty: a laser Doppler flowmetry study. Knee Surg Sports Traumatol Arthrosc. 2006;14(5):411–416. doi: 10.1007/s00167-005-0703-0
  31. Cai ZG, Zhang J, Zhang JG, Zhao FY, Yu GY, Li Y, Ding HS. Evaluation of near infrared spectroscopy in monitoring postoperative regional tissue oxygen saturation for fibular flaps. J Plast Reconstr Aesthet Surg. 2008;61(3):289–96. doi: 10.1016/j.bjps.2007.10.047
  32. Duwelius PJ, Schmidt AH. Assessment of bone viability in patients with osteomyelitis: preliminary clinical experience with laser Doppler flowmetry. J Orthop Trauma. 1992;6(3):327–332. doi: 10.1097/00005131-199209000-00010
  33. Beaule PE, Campbell P, Shim P. Femoral head blood flow during hip resurfacing. Clin Orthop Relat Res. 2007;(456):148–152. doi: 10.1097/01.blo.0000238865.77109.af
  34. Bassett GS, Barton KL, Skaggs DL. Laser Doppler flowmetry during open reduction for developmental dysplasia of the hip. Clin Orthop Relat Res. 1997;(340):158–164. doi: 10.1097/00003086-199707000-00020
  35. Meertens R, Knapp K, Strain D, Casanova F, Ball S, Fulford J, Thorn C. In vivo Measurement of Intraosseous Vascular Haemodynamic Markers in Human Bone Tissue Utilising Near Infrared Spectroscopy. Front Physiol. 2021;(12):738239. doi: 10.3389/fphys.2021.738239
  36. Krupatkin AI. Oscillatory processes and diagnostics of the state of microcirculatory and tissue systems. Regional blood circulation and microcirculation. 2018;17(3):4. (In Russ).
  37. Krupatkin AI. Fluctuations of blood flow — a new diagnostic language in the study of microcirculation. Regional blood circulation and microcirculation. 2014;13(1):83–99. (In Russ). doi: 10.24884/1682-6655-2014-13-1-83-99
  38. Patent RUS № 2514110/27.04.2014. Mironov SP, Krupatkin AI, Kesyan GA, Urazgildeev RZ, Dan IM, Arsenyev IG. Sposob opredeleniya stepeni metabolicheskoj zrelosti geterotopicheskih ossifikatov pered ih hirurgicheskim lecheniem. Available from: https://yandex.ru/patents/doc/RU2514110C1_20140427?ysclid=lloz22zi55248599167 (In Russ).
  39. Vekovtsev AA, Tohirien B, Slizovsky GV, Poznyakovsky VM. Clinical trials of vitamin and mineral complex for the treatment of children with a traumatological profile. Bulletin of the VGUIT. 2019;81(2):147–153. (In Russ). doi: 10.20914/2310-1202-2019-2-147-153
  40. Dorokhin AI, Krupatkin AI, Adrianova AA, Khudik VI, Sorokin DS, Kuryshev DA, Bukchin LB. Closed fractures of the distal tibia. A variety of forms and treatments (using the example of older age groups). Immediate results. Physical and rehabilitation medicine, medical rehabilitation. 2021;3(1):11–23. (In Russ). doi: 10.36425/rehab63615
  41. Baker WB, Parthasarathy AB, Busch DR, Mesquita RC, Greenberg JH, Yodh AG. Modified Beer-Lambert law for blood flow. Biomed Opt Express. 2014;5(11):4053–75. doi: 10.1364/BOE.5.004053
  42. Bläsius FM, Link BC, Beeres FJ, Iselin LD, Leu BM, Gueorguiev B, Knobe M. Impact of surgical procedures on soft tissue microcirculation in calcaneal fractures: a prospective longitudinal cohort study. Injury. 2019;50(12):2332–2338. doi: 10.1016/j.injury.2019.10.004
  43. Becker RL, Siamwala JH, Macias BR, Hargens AR. Tibia Bone Microvascular Flow Dynamics as Compared to Anterior Tibial Artery Flow During Body Tilt. Aerospace Medicine and Human Performance. 2018;89(4):357–364. doi: 10.3357/amhp.4928.2018
  44. Pifferi A, Torricelli A, Taroni P, Bassi A, Chikoidze E, Giambattistelli E, Cubeddu R. Optical biopsy of bone tissue: a step toward the diagnosis of bone pathologies. J Biomed Opt. 2004;9(3):474–80. doi: 10.1117/1.1691029
  45. Sekar SV, Pagliazzi M, Negredo E, Martelli F, Farina A, Dalla Mora A, Lindner C, Farzam P, Perez-Alvarez N, Puig J, Taroni P, Pifferi A, Durduran T. In vivo, non-invasive characterization of human bone by hybrid broadband (600–1200 nm) diffuse optical and correlation spectroscopies. PLoS One. 2016;11(12):e0168426. doi: 10.1371/journal.pone.0168426
  46. Naslund J, Pettersson J, Lundeberg T, Linnarsson D, Lindberg LG. Noninvasive continuous estimation of blood flow changes in human patellar bone. Med Biol Eng Comput. 2006;44(6):501–9. doi: 10.1007/s11517-006-0070-0
  47. Siamwala JH, Lee PC, Macias BR, Hargens AR. Lower-body negative pressure restores leg bone microvascular flow to supine levels during head-down tilt. J Appl Physiol. 2015;119(2):101–9. doi: 10.1152/japplphysiol.00028.2015
  48. Mateus J, Hargens AR. Photoplethysmography for non-invasive in vivo measurement of bone hemodynamics. Physiol Meas. 2012;33(6):1027–1042. doi: 10.1088/0967-3334/33/6/1027

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