Fig. 1 Various strategies employed for stimulating T-B junction healing
Scan for full text
Department of Orthopaedic Surgery, the Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou 310009, China
Department of Orthopaedic Research, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts 02115, USA
Department of Orthopaedic Surgery, the Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou 310009, China
1.Department of Orthopaedic Surgery, the Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou 310009, China
2.Department of Orthopaedic Research, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts 02115, USA
Published: 2012-12 ,
Received: 04 May 2012 ,
Revised: 30 October 2012 ,
Accepted: 05 August 2012
Cite this article
Zhi-min Ying, Tiao Lin, Shi-gui Yan. Low-intensity pulsed ultrasound therapy: a potential strategy to stimulate tendon-bone junction healing. [J]. Journal of Zhejiang University-SCIENCE B (Biomedicine & Biotechnology) 13(12):955-963(2012)
Zhi-min Ying, Tiao Lin, Shi-gui Yan. Low-intensity pulsed ultrasound therapy: a potential strategy to stimulate tendon-bone junction healing. [J]. Journal of Zhejiang University-SCIENCE B (Biomedicine & Biotechnology) 13(12):955-963(2012) DOI: 10.1631/jzus.B1200129.
Department of Orthopaedic Surgery, the Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou 310009, China
Department of Orthopaedic Research, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts 02115, USA
Department of Orthopaedic Surgery, the Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou 310009, China
Incorporation of a tendon graft within the bone tunnel represents a challenging clinical problem. Successful anterior cruciate ligament (ACL) reconstruction requires solid healing of the tendon graft in the bone tunnel. Enhancement of graft healing to bone is important to facilitate early aggressive rehabilitation and a rapid return to pre-injury activity levels. No convenient, effective or inexpensive procedures exist to enhance tendon-bone (T-B) healing after surgery. Low-intensity pulsed ultrasound (LIPUS) improves local blood perfusion and angiogenesis, stimulates cartilage maturation, enhances differentiation and proliferation of osteoblasts, and motivates osteogenic differentiation of mesenchymal stem cells (MSCs), and therefore, appears to be a potential non-invasive tool for T-B healing in early stage of rehabilitation of ACL reconstruction. It is conceivable that LIPUS could be used to stimulate T-B tunnel healing in the home, with the aim of accelerating rehabilitation and an earlier return to normal activities in the near future. The purpose of this review is to demonstrate how LIPUS stimulates T-B healing at the cellular and molecular levels, describe studies in animal models, and provide a future direction for research.
Grafted tendon healing within the bone tunnel after anterior cruciate ligament (ACL) reconstruction is a complicated, poorly clarified biological process. The osteointegration of tendon grafts used for ACL replacement may be unsatisfactory and may be associated with postoperative anterior-posterior laxity. Tendon-bone (T-B) healing in bone tunnel occurs through bone incorporation into the fibrovascular interface tissue that initially forms between the tendon and bone. Increasing the integrity of the healing of T-B interface has been attempted by adopting a number of different augmentation strategies (Fig.
Fig. 1 Various strategies employed for stimulating T-B junction healing
The T-B junction has been described in humans and many animal models as healing between tendon and bone (Rodeo et al.,
Sufficient vascular invasion is a fundamental prerequisite for endochondral bone formation, fracture healing, and soft tissue repair (Bolander,
Fig. 2 Bioeffects of the LIPUS enhancing the healing of the T-B interface
(a) Accelerating angiogenesis through stimulating the production of angiogenesis-related cytokines; (b) Stimulating cartilage maturation by bone cell differentiation and calcified matrix production; (c) Enhancing osteoblast growth through nutrient exchange and regulating correlative signal molecules; (d) Motivating MSCs osteogenic differentiation by upregulating chondrogenic differentiation of MSCs
Several investigations have confirmed that LIPUS stimulates osteogenesis during bone growth and repair (Warden et al.,
The specific mechanisms by which ultrasound stimulation works on bone cell activities are still unknown. However, in terms of the physical mechanism, ultrasound provides a mechanical force to the cellular system. It is shown that the acoustic cavitations induced by ultrasound are considered to be strongly dependent on ultrasound frequency (Yoichiro et al.,
MSCs are multipotent stem cells that differentiate into a variety of cell types including osteoblasts, chondrocytes, and adipocytes. However, the degree to which the culture will differentiate varies among individuals and according to how differentiation is induced, e.g., chemically vs. mechanically, or physically. Lim et al. (
LIPUS is recommended for a daily application of about 20 to 30 min for acceleration of fracture healing, treatment of delayed or nonunion and bone lengthening (Busse et al.,
When ultrasonic waves propagate in the body, ultrasonic energy is absorbed at a rate proportional to the density of the tissue. Absorption of the ultrasound signal results in an increase in the temperature of the body tissue (Liu et al.,
The cavitation phenomenon is the largest nonthermal effect created by ultrasound energy (Doktycz and Suslick,
Ultrasound enhances the movement of the liquid medium which precipitates mass transfer and reaction rates in both multiphase and homogeneous systems (Bar,
How to stimulate bone formation and enhance mineralization at the T-B junction is of clinical importance. One of the possible approaches is to use biophysical intervention, such as LIPUS, mechanical stimuli, and electromagnetic fields. These modalities serve to accelerate healing of bone fractures and soft tissue. LIPUS exerts its effect on fracture healing (Einhorn,
Study | Animal model | Treatment | Outcome |
---|---|---|---|
Lovric et al. ( Reference 2012 | Wethers (the infraspinatus tendon was repaired with a transosseous-equivalent suture-bridge construct using medial row and lateral push-in suture anchors) | 20 min/d for 28 d | Histology: generally a thicker region of newly formed woven bone, morphologically resembling trabecular bone, with increased osteoblast activity along the bone surface, was noted at the T-B interface in the LIPUS-treated group compared to the controls |
Immunohistochemistry: expression patterns of VEGF and RUNX2 both showed a significant difference between the control and the LIPUS-treated groups | |||
Lu C.C. et al. ( Reference 2009 | Rabbits (the extensor digitorum longus tendons of rabbits were transplanted into bone tunnels in both proximal tibias) | 20 min/d for 12 weeks | Biomechanical test: at two weeks postoperatively, the mean maximal tensile strength of the LIPUS group was significantly higher than that in the control group |
Histological findings: at 12 weeks the T-B interface presented a transition zone of new bone formation from bone to mineralized cartilage and nonmineralized fibrocartilage in the LIPUS group | |||
Lu M.H. et al. ( Reference 2009 | Rabbits (established transverse partial patellectomy was performed in rabbits) | 20 min/d for 6 weeks | New bone size measured on radiographs: the size of radiographic new bone from the remaining patella showed that significantly more new bone was formed in the LIPUS group compared with that in controls at Week 18 |
BMD measured by pQCT: the LIPUS treatment group showed significantly higher volumetric BMD in the new bone at Week 6 than that did in the controls | |||
Stiffness measured by ultrasound water-jet indentation system: the stiffness of patellar cartilage of LIPUS group was found to be significantly higher than that in controls at postoperative Week 6 | |||
Lu et al. ( Reference 2008 | Rabbits (standard partial patellectomy was conducted in rabbits) | 20 min/d for 16 weeks | VEGF expression: at Week 4, chondrocytes and osteoblasts expressed significantly more VEGF in the LIPUS group than that in the control group |
Cartilage formation: an LIPUS treatment group showed significantly thicker fibrocartilage zone when compared with that in the control group at Week 16 | |||
Walsh et al. ( Reference 2007 | Sheeps (single digital extensor tendon autografts from the right hoof of the sheeps were transplanted into both tibial and femoral bone tunnels) | 20 min/d for 3, 6, and 12 weeks | Mechanical testing: LIPUS treatment resulted in a significantly greater peak load and stiffer compared with the controls at Week 26 |
Histology: evidence of new bone at the interface in the LIPUS-treated group at Week 26 revealed significant differences compared with that in controls | |||
Lu et al. ( Reference 2006 | Rabbits (standard partial patellectomy was conducted in rabbits) | 20 min/d for 2, 4, 8, and 16 weeks | Biomechanical testing: LIPUS significantly improved the tensile mechanical properties of the T-B junction compared with that in the control group |
Histologic analysis: a fluorescence microscopic evaluation revealed earlier and increased newly formed bone at Weeks 8 and 16 in LIPUS treatment specimens compared with that in the control group | |||
New bone formation: significantly more newly formed bone was found in the LIPUS group when compared with that in the controls at both Weeks 8 and 16 | |||
Qin et al. ( Reference 2006a | Rabbits (standard partial patellectomy was conducted in rabbits) | 20 min/d for 8 and 16 weeks | New bone area measured on radiographs: the LIPUS group induced significantly more new bone formation when compared with the control at both Weeks 8 and 16 |
Vickers hardness obtained from micro-indentation: compared with the control group, the Vickers hardness of the newly regenerated fibrocartilage zone, healing tendon, and cartilaginous metaplasia in the LIPUS group was found to be significantly higher at Week 16 | |||
Qin et al. ( Reference 2006b | Rabbits (standard partial patellectomy was conducted in rabbits) | 20 min/d for 8 and 16 weeks | New bone size measured on radiographs: significant more new bone was formed in the LIPUS group compared with non-treated controls both at Weeks 8 and 16 |
BMD measured by pQCT: LIPUS treatment group showed significantly higher volumetric BMD in new bone at Week 8 compared with the control group | |||
Descriptive histology: fluorescence microscopic observations revealed more xylenol orange labeling compared with calcein green labeling at Week 8 LIPUS-treated sample compared with the control sample |
VEGF: vascular endothelial growth factor; RUNX2: runt-related transcription factor 2; BMD: bone mineral density; pQCT: peripheral quantitative computed tomography systems
ACL reconstruction using semitendinosus and gracilis tendons has become popular in recent years. However, failure to incorporate the biological graft into the bone tunnel continues to occur (George et al.,
Researches, including in vitro and in vivo have shown encouraging results, with LIPUS able to promote healing at the interface of T-B. The effect on the bone-tendon junction, however, may be primarily on bone. However, current animal model studies do not reproduce the complex intra-articular environment that occurs during the ACL reconstruction in humans, due to the presence of synovial fluid. Furthermore the optimal LIPUS treatment modality for patients undergoing ACL reconstruction surgery is still to be determined. Future studies are not only needed to establish the indications for applying LIPUS but also to identify the effects and appropriate duration of LIPUS in animal model experiments and clinical trials. Adequately high quality evidence in human studies with standardization of intensities and dosages of LIPUS for the T-B junction are needed. It is conceivable that LIPUS could be used to stimulate T-B tunnel healing at home, with the aim of accelerating rehabilitation and an earlier return to normal life.
SR Angle, K Sena, DR Sumner, AS Virdi. Osteogenic differentiation of rat bone marrow stromal cells by various intensities of low-intensity pulsed ultrasound. Ultrasonics, 2011. 51(3):281-288. 20965537DOI:10.1016/j.ultras.2010.09.004. [Baidu Scholar]
R Bar. Ultrasound-enhanced bioprocesses: cholesterol oxidation by Rhodococcus erythropolis. Biotechnol Bioeng, 1988. 32(5):655-663. 18587766DOI:10.1002/bit.260320510. [Baidu Scholar]
ME Bolander. Regulation of fracture repair by growth factors. Proc Soc Exp Biol Med, 1992. 200(2):165-170. . [Baidu Scholar]
JW Busse, J Kaur, B Mollon, M Bhandari, 3rdP Tornetta, HJ Schunemann, GH Guyatt. Low intensity pulsed ultrasonography for fractures: systematic review of randomised controlled trials. BMJ, 2009. 338b35119251751DOI:10.1136/bmj.b351. [Baidu Scholar]
XZ Cai, SG Yan, HB Wu, RX He, XS Dai, HX Chen, RJ Yan, XH Zhao. Effect of delayed pulsed-wave ultrasound on local pharmacokinetics and pharmacodynamics of vancomycin-loaded acrylic bone cement in vivo. Antimicrob Agents Chemother, 2007. 51(9):3199-3204. 17620385DOI:10.1128/AAC.01465-06. [Baidu Scholar]
CH Chen. Strategies to enhance tendon graft-bone healing in anterior cruciate ligament reconstruction. Chang Gung Med J, 2009. 32(5):483-493. 19840505. [Baidu Scholar]
B Chung, JP Wiley. Extracorporeal shockwave therapy: a review. Sports Med, 2002. 32(13):851-865. 12392445DOI:10.2165/00007256-200232130-00004. [Baidu Scholar]
J Clark, DJ Stechschulte. The interface between bone and tendon at an insertion site: a study of the quadriceps tendon insertion. J Anat, 1998. 192(4):605-616. 9723987DOI:10.1046/j.1469-7580.1998.19240605.x. [Baidu Scholar]
JH Cui, SR Park, K Park, BH Choi, BH Min. Preconditioning of mesenchymal stem cells with low-intensity ultrasound for cartilage formation in vivo. Tissue Eng, 2007. 13(2):351-360. 17518569DOI:10.1089/ten.2006.0080. [Baidu Scholar]
B Demirag, B Sarisozen, O Ozer, T Kaplan, C Ozturk. Enhancement of tendon-bone healing of anterior cruciate ligament grafts by blockage of matrix metalloproteinases. J Bone Joint Surg Am, 2005. 87(11):2401-2410. 16264114DOI:10.2106/JBJS.D.01952. [Baidu Scholar]
N Doan, P Reher, S Meghji, M Harris. In vitro effects of therapeutic ultrasound on cell proliferation, protein synthesis, and cytokine production by human fibroblasts, osteoblasts, and monocytes. J Oral Maxillofac Surg, 1999. 57(4):409-419. 10199493DOI:10.1016/S0278-2391(99)90281-1. [Baidu Scholar]
SJ Doktycz, KS Suslick. Interparticle collisions driven by ultrasound. Science, 1990. 247(4946):1067-1069. 2309118DOI:10.1126/science.2309118. [Baidu Scholar]
TA Einhorn. Enhancement of fracture-healing. J Bone Joint Surg Am, 1995. 77(6):940-956. 7782368. [Baidu Scholar]
H El-Mowafi, M Mohsen. The effect of low-intensity pulsed ultrasound on callus maturation in tibial distraction osteogenesis. Int Orthop, 2005. 29(2):121-124. 15685456DOI:10.1007/s0026-004-0625-3. [Baidu Scholar]
JrLB Feril, T Kondo. Biological effects of low intensity ultrasound: the mechanism involved, and its implications on therapy and on biosafety of ultrasound. J Radiat Res, 2004. 45(4):479-489. 15635256DOI:10.1269/jrr.45.479. [Baidu Scholar]
MS George, WR Dunn, KP Spindler. Current concepts review: revision anterior cruciate ligament reconstruction. Am J Sports Med, 2006. 34(12):2026-2037. 17092921DOI:10.1177/0363546506295026. [Baidu Scholar]
LV Gulotta, D Kovacevic, L Ying, JR Ehteshami, S Montgomery, SA Rodeo. Augmentation of tendon-to-bone healing with a magnesium-based bone adhesive. Am J Sports Med, 2008. 36(7):1290-1297. 18319348DOI:10.1177/0363546508314396. [Baidu Scholar]
M Hadjiargyrou, K McLeod, JP Ryaby, C Rubin. Enhancement of fracture healing by low intensity ultrasound. Clin Orthop Relat Res, 1998. 355(Suppl.):S216-S229. 9917641DOI:10.1097/00003086-199810001-00022. [Baidu Scholar]
Y Hashimoto, G Yoshida, H Toyoda, K Takaoka. Generation of tendon-to-bone interface “enthesis” with use of recombinant BMP-2 in a rabbit model. J Orthop Res, 2007. 25(11):1415-1424. 17557323DOI:10.1002/jor.20447. [Baidu Scholar]
X Huangfu, J Zhao. Tendon-bone healing enhancement using injectable tricalcium phosphate in a dog anterior cruciate ligament reconstruction model. Arthroscopy, 2007. 23(5):455-462. 17478274DOI:10.1016/j.arthro.2006.12.031. [Baidu Scholar]
YJ Ju, T Muneta, H Yoshimura, H Koga, I Sekiya. Synovial mesenchymal stem cells accelerate early remodeling of tendon-bone healing. Cell Tissue Res, 2008. 332(3):469-478. 18418628DOI:10.1007/s00441-008-0610-z. [Baidu Scholar]
LJ Juffermans, O Kamp, PA Dijkmans, CA Visser, RJ Musters. Low-intensity ultrasound-exposed microbubbles provoke local hyperpolarization of the cell membrane via activation of BK (Ca) channels. Ultrasound Med Biol, 2008. 34(3):502-508. DOI:10.1016/j.ultrasmedbio.2007.09.010. [Baidu Scholar]
T Kanazawa, T Soejima, H Murakami, T Inoue, M Katouda, K Nagata. An immunohistological study of the integration at the bone-tendon interface after reconstruction of the anterior cruciate ligament in rabbits. J Bone Joint Surg Br, 2006. 88(5):682-687. 16645121DOI:10.1302/0301-620X.88B5.17198. [Baidu Scholar]
S Karaoglu, C Celik, P Korkusuz. The effects of bone marrow or periosteum on tendon-to-bone tunnel healing in a rabbit model. Knee Surg Sports Traumatol Arthrosc, 2009. 17(2):170-178. 18941736DOI:10.1007/s00167-008-0646-3. [Baidu Scholar]
R Karshafian, PD Bevan, R Williams, S Samac, PN Burns. Sonoporation by ultrasound-activated micro-bubble contrast agents: effect of acoustic exposure parameters on cell membrane permeability and cell viability. Ultrasound Med Biol, 2009. 35(5):847-860. 19110370DOI:10.1016/j.ultrasmedbio.2008.10.013. [Baidu Scholar]
T Kokubu, N Matsui, H Fujioka, M Tsunoda, K Mizuno. Low intensity pulsed ultrasound exposure increases prostaglandin E2 production via the induction of cyclooxygenase-2 mRNA in mouse osteoblasts. Biochem Biophys Res Commun, 1999. 256(2):284-287. 10079177DOI:10.1006/bbrc.1999.0318. [Baidu Scholar]
CM Korstjens, PA Nolte, EH Burger, GH Albers, CM Semeins, IH Aartman, SW Goei, J Klein-Nulend. Stimulation of bone cell differentiation by low-intensity ultrasound: a histomorphometric in vitro study. J Orthop Res, 2004. 22(3):495-500. 15099626DOI:10.1016/j.orthres.2003.09.011. [Baidu Scholar]
D Kovacevic, AJ Fox, A Bedi, L Ying, XH Deng, RF Warren, SA Rodeo. Calcium-phosphate matrix with or without TGF-β3 improves tendon-bone healing after rotator cuff repair. Am J Sports Med, 2011. 39(4):811-819. 21406666DOI:10.1177/0363546511399378. [Baidu Scholar]
HJ Lee, BH Choi, BH Min, YS Son, SR Park. Low-intensity ultrasound stimulation enhances chondrogenic differentiation in alginate culture of mesenchymal stem cells. Artif Organs, 2006. 30(9):707-715. 16934100DOI:10.1111/j.1525-1594.2006.00288.x. [Baidu Scholar]
KS Leung, L Qin, LK Fu, CW Chan. A comparative study of bone to bone repair and bone to tendon healing in patella-patellar tendon complex in rabbits. Clin Biomech, 2002. 17(8):594-602. DOI:10.1016/S0268-0033(02)00075-X. [Baidu Scholar]
KS Leung, WS Lee, HF Tsui, PP Liu, WH Cheung. Complex tibial fracture outcomes following treatment with low-intensity pulsed ultrasound. Ultrasound Med Biol, 2004. 30(3):389-395. 15063521DOI:10.1016/j.ultrasmedbio.2003.11.008. [Baidu Scholar]
JK Lim, J Hui, L Li, A Thambyah, J Goh, EH Lee. Enhancement of tendon graft osteointegration using mesenchymal stem cells in a rabbit model of anterior cruciate ligament reconstruction. Arthroscopy, 2004. 20(9):899-910. 15525922DOI:10.1016/j.arthro.2004.06.035. [Baidu Scholar]
X Liu, C Yin, X Gong, W Cao. Theoretical and experimental study on temperature elevation behind ribs caused by weakly focused ultrasound. Ultrasound Med Biol, 2010. 36(10):1704-1712. 20800959DOI:10.1016/j.ultrasmedbio.2010.07.018. [Baidu Scholar]
Y Liu, H Miyoshi, M Nakamura. Encapsulated ultrasound microbubbles: therapeutic application in drug/gene delivery. J Control Release, 2006. 114(1):89-99. 16824637DOI:10.1016/j.jconrel.2006.05.018. [Baidu Scholar]
V Lovric, M Ledger, J Goldberg, W Harper, N Bertollo, MH Pelletier, RA Oliver, Y Yu, WR Walsh. The effects of low-intensity pulsed ultrasound on tendon-bone healing in a transosseous-equivalent sheep rotator cuff model. Knee Surg Sports Traumatol Arthrosc, 2012. Epub ahead of printDOI:10.1007/s00167-012-1972-z. [Baidu Scholar]
CC Lu, YC Liu, YM Cheng, TT Chih, YC Tien. Augmentation of tendon-bone interface healing with low-intensity pulsed ultrasound. Orthopedics, 2009. 32(3):17319309059DOI:10.3928/01477447-20090301-19. [Baidu Scholar]
H Lu, L Qin, P Fok, W Cheung, K Lee, X Guo, W Wong, K Leung. Low-intensity pulsed ultrasound accelerates bone-tendon junction healing: a partial patellectomy model in rabbits. Am J Sports Med, 2006. 34(8):1287-1296. 16567453DOI:10.1177/0363546506286788. [Baidu Scholar]
H Lu, L Qin, W Cheung, K Lee, W Wong, K Leung. Low-intensity pulsed ultrasound accelerated bone-tendon junction healing through regulation of vascular endothelial growth factor expression and cartilage formation. Ultrasound Med Biol, 2008. 34(8):1248-1260. 18378382DOI:10.1016/j.ultrasmedbio.2008.01.009. [Baidu Scholar]
MH Lu, YP Zheng, QH Huang, 等. Low Intensity Pulsed Ultrasound Increases the Mechanical Properties of the Healing Tissues at Bone-Tendon Junction. Engineering in Medicine and Biology Society, 2009. EMBC 2009. 2009. Annual International Conference of the IEEE. 2141-2144. DOI:10.1109/IEMBS.2009.5333960. [Baidu Scholar]
H Mutsuzaki, M Sakane, H Fujie, S Hattori, H Kobayashi, N Ochiai. Effect of calcium phosphate-hybridized tendon graft on biomechanical behavior in anterior cruciate ligament reconstruction in a goat model: novel technique for improving tendon-bone healing. Am J Sports Med, 2011. 39(5):1059-1066. 21220545DOI:10.1177/0363546510390427. [Baidu Scholar]
PA Nolte, A van der Krans, P Patka, IM Janssen, JP Ryaby, GH Albers. Low-intensity pulsed ultrasound in the treatment of nonunions. J Trauma, 2001. 51(4):693-702. discussion 702-70311586161DOI:10.1097/00005373-200110000-00012. [Baidu Scholar]
CD Ohl, M Arora, R Ikink, N de Jong, M Versluis, M Delius, D Lohse. Sonoporation from jetting cavitation bubbles. Biophys J, 2006. 91(11):4285-4295. 16950843DOI:10.1529/biophysj.105.075366. [Baidu Scholar]
W Petersen, H Laprell. Insertion of autologous tendon grafts to the bone: a histological and immunohistochemical study of hamstring and patellar tendon grafts. Knee Surg Sports Traumatol Arthrosc, 2000. 8(1):26-31. 10663316DOI:10.1007/s001670050006. [Baidu Scholar]
WG Pitt, SA Ross. Ultrasound increases the rate of bacterial cell growth. Biotechnol Prog, 2003. 19(3):1038-1044. 12790676DOI:10.1021/bp0340685. [Baidu Scholar]
T Prozorov, R Prozorov, KS Suslick. High velocity interparticle collisions driven by ultrasound. J Am Chem Soc, 2004. 126(43):13890-13891. 15506727DOI:10.1021/ja049493o. [Baidu Scholar]
L Qin, KS Leung, CW Chan, LK Fu, R Rosier. Enlargement of remaining patella after partial patellectomy in rabbits. Med Sci Sports Exerc, 1999. 31(4):502-506. 10211843DOI:10.1097/00005768-199904000-00002. [Baidu Scholar]
L Qin, P Fok, H Lu, S Shi, Y Leng, K Leung. Low intensity pulsed ultrasound increases the matrix hardness of the healing tissues at bone-tendon insertion-a partial patellectomy model in rabbits. Clin Biomech, 2006. 21(4):387-394. DOI:10.1016/j.clinbiomech.2005.11.008. [Baidu Scholar]
L Qin, H Lu, P Fok, W Cheung, Y Zheng, K Lee, K Leung. Low-intensity pulsed ultrasound accelerates osteogenesis at bone-tendon healing junction. Ultrasound Med Biol, 2006. 32(12):1905-1911. 17169702DOI:10.1016/j.ultrasmedbio.2006.06.028. [Baidu Scholar]
P Reher, N Doan, B Bradnock, S Meghji, M Harris. Effect of ultrasound on the production of IL-8, basic FGF and VEGF. Cytokine, 1999. 11(6):416-423. 10346981DOI:10.1006/cyto.1998.0444. [Baidu Scholar]
P Reher, M Harris, M Whiteman, HK Hai, S Meghji. Ultrasound stimulates nitric oxide and prostaglandin E2 production by human osteoblasts. Bone, 2002. 31(1):236-241. 12110440DOI:10.1016/S8756-3282(02)00789-5. [Baidu Scholar]
H Robert, J Es-Sayeh, D Heymann, N Passuti, S Eloit, E Vaneenoge. Hamstring insertion site healing after anterior cruciate ligament reconstruction in patients with symptomatic hardware or repeat rupture: a histologic study in 12 patients. Arthroscopy, 2003. 19(9):948-954. 14608313DOI:10.1016/j.arthro.2003.09.007. [Baidu Scholar]
SA Rodeo, SP Arnoczky, PA Torzilli, C Hidaka, RF Warren. Tendon-healing in a bone tunnel. A biomechanical and histological study in the dog. J Bone Joint Surg Am, 1993. 75(12):1795-1803. 8258550. [Baidu Scholar]
C Rubin, M Bolander, JP Ryaby, M Hadjiargyrou. The use of low-intensity ultrasound to accelerate the healing of fractures. J Bone Joint Surg Am, 2001. 83A(2):259-270. . [Baidu Scholar]
K Sasaki, R Kuroda, K Ishida, S Kubo, T Matsumoto, Y Mifune, K Kinoshita, K Tei, T Akisue, Y Tabata, 等. Enhancement of tendon-bone osteointegration of anterior cruciate ligament graft using granulocyte colony-stimulating factor. Am J Sports Med, 2008. 36(8):1519-1527. 18413678DOI:10.1177/0363546508316282. [Baidu Scholar]
A Shimazaki, K Inui, Y Azuma, N Nishimura, Y Yamano. Low-intensity pulsed ultrasound accelerates bone maturation in distraction osteogenesis in rabbits. J Bone Joint Surg Br, 2000. 82(7):1077-1082. 11041605DOI:10.1302/0301-620X.82B7.9948. [Baidu Scholar]
M Sivakumar, K Tachibana, AB Pandit, K Yasui, T Tuziuti, A Towata, Y Iida. Transdermal drug delivery using ultrasound-theory, understanding and critical analysis. Cell Mol Biol, 2005. 51(Suppl.):OL767-OL784. 16171576. [Baidu Scholar]
MY Soon, A Hassan, JH Hui, JC Goh, EH Lee. An analysis of soft tissue allograft anterior cruciate ligament reconstruction in a rabbit model: a short-term study of the use of mesenchymal stem cells to enhance tendon osteointegration. Am J Sports Med, 2007. 35(6):962-971. 17400750DOI:10.1177/0363546507300057. [Baidu Scholar]
JS Sun, RC Hong, WH Chang, LT Chen, FH Lin, HC Liu. In vitro effects of low-intensity ultrasound stimulation on the bone cells. J Biomed Mater Res, 2001. 57(3):449-456. 11523040DOI:10.1002/1097-4636(20011205)57:3<449::AID-JBM1188>3.0.CO;2-0. [Baidu Scholar]
WR Walsh, P Stephens, F Vizesi, W Bruce, J Huckle, Y Yu. Effects of low-intensity pulsed ultrasound on tendon-bone healing in an intra-articular sheep knee model. Arthroscopy, 2007. 23(2):197-204. 17276228DOI:10.1016/j.arthro.2006.09.003. [Baidu Scholar]
CJ Wang, LH Weng, WY Chou, SL Hsu, JY Ko, SF Ko, CC Huang. Extracorporeal shock wave therapy enhances early tendon-bone healing and reduces bone tunnel enlargement in hamstring autograft anterior cruciate ligament reconstruction. Am J Sports Med, 2011. 40(7):NP1421531863DOI:10.1177/0363546511404201. [Baidu Scholar]
FS Wang, YR Kuo, CJ Wang, KD Yang, PR Chang, YT Huang, HC Huang, YC Sun, YJ Yang, YJ Chen. Nitric oxide mediates ultrasound-induced hypoxia-inducible factor-1alpha activation and vascular endothelial growth factor-an expression in human osteoblasts. Bone, 2004. 35(1):114-123. 15207747DOI:10.1016/j.bone.2004.02.012. [Baidu Scholar]
SJ Warden, KL Bennell, JM McMeeken, JD Wark. Acceleration of fresh fracture repair using the sonic accelerated fracture healing system (SAFHS): a review. Calcif Tissue Int, 2000. 66(2):157-163. 10652965DOI:10.1007/s002230010031. [Baidu Scholar]
HG Welgus, JJ Jeffrey, AZ Eisen. Human skin fibroblast collagenase. Assessment of activation energy and deuterium isotope effect with collagenous substrates. J Biol Chem, 1981. 2569516-9521. 6270090. [Baidu Scholar]
CY Wen, L Qin, KM Lee, KM Chan. The use of brushite calcium phosphate cement for enhancement of bone-tendon integration in an anterior cruciate ligament reconstruction rabbit model. J Biomed Mater Res B Appl Biomater, 2009. 89B(2):466-474. DOI:10.1002/jbm.b.31236. [Baidu Scholar]
NW Wong, L Qin, KM Lee, KO Tai, WS Chong, KS Leung, KM Chan. Healing of bone tendon junction in a bone trough: a goat partial patellectomy model. Clin Orthop Relat Res, 2003. 413291-302. 12897621DOI:10.1097/01.blo.0000076802.53006.5b. [Baidu Scholar]
SG Yan, LY Huang, XZ Cai. Low-intensity pulsed ultrasound: a potential non-invasive therapy for femoral head osteonecrosis. Med Hypotheses, 2011. 76(1):4-7. 20826064DOI:10.1016/j.mehy.2010.08.016. [Baidu Scholar]
M Yoichiro, S John, Allen, Y Shin, I Teiichiro, K Yukio. Medical ultrasound with microbubbles. Exp Therm Fluid Sci, 2005. 29(3):255-265. DOI:10.1016/j.expthermflusci.2004.05.008. [Baidu Scholar]
SR Young, M Dyson. The effect of therapeutic ultrasound on angiogenesis. Ultrasound Med Biol, 1990. 16(3):261-269. 1694604DOI:10.1016/0301-5629(90)90005-W. [Baidu Scholar]
48
Views
0
Downloads
3
CSCD
Publicity Resources
Related Articles
Related Author
Related Institution