Analysis of collagen organization in mouse achilles tendon using high-frequency ultrasound imaging

Journal of Biomechanical Engineering

Volumn 136, Issue 2, 2014, Pages

  Riggin, Corinne N ^a   Sarver, Joseph J ^a,b   Freedman, Benjamin R ^a   Thomas, Stephen J ^a,c   Soslowsky, Louis J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b DREXEL UNIVERSITY   (United States)

^c NEUMANN UNIVERSITY   (United States)

Author keywords

Achilles tendon; collagen organization; high frequency ultrasound

Indexed keywords

ACHILLES TENDONS; COLLAGEN ORGANIZATIONS; CROSSED POLARIZERS; HIGH FREQUENCY ULTRASOUNDS; HIGH-FREQUENCY ULTRASOUND; HIGH-FREQUENCY ULTRASOUND IMAGING; LOADING ENVIRONMENT; STRUCTURAL MEASURES;

COLLAGEN; EXPERIMENTS; HYDRAULIC FLUIDS; LOADING; MAMMALS; REPAIR; ULTRASONIC IMAGING;

TENDONS;

COLLAGEN;

ACHILLES TENDON; ANIMAL TISSUE; ARTICLE; CAMERA; COMPUTER SYSTEM; CONTROLLED STUDY; ECHOGRAPHY; GENERAL MEDICAL DEVICE; HIGH FREQUENCY ULTRASOUND; IMAGE ANALYSIS; IMAGING; LINEAR BACKLIGHT; MOUSE; NONHUMAN; POLARIZER SHEET; TISSUE STRUCTURE; ULTRASOUND SCANNER; ULTRASOUND TRANSDUCER; ANIMAL; C57BL MOUSE; COMPUTER ASSISTED DIAGNOSIS; CONFORMATION; IN VITRO STUDY; PATHOLOGY; PROCEDURES; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY; TENDON INJURY; ULTRASTRUCTURE; VALIDATION STUDY;

ACHILLES TENDON; ANIMALS; COLLAGEN; IMAGE INTERPRETATION, COMPUTER-ASSISTED; IN VITRO TECHNIQUES; MICE; MICE, INBRED C57BL; MOLECULAR CONFORMATION; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; TENDON INJURIES; ULTRASONOGRAPHY;

EID: 84896788745     PISSN: 01480731     EISSN: 15288951     Source Type: Journal    
DOI: 10.1115/1.4026285     Document Type: Article

References (39)

1. Suchak, A. A., Bostick, G., Reid, D., Blitz, S., and Jomha, N., 2005, "The Incidence of Achilles Tendon Ruptures in Edmonton, Canada," Foot Ankle Int., 26(11), pp. 932-936. (Pubitemid 41572122)
2. Houshian, S., Tscherning, T., and Riegels-Nielsen, P., 1998, "The Epidemiology of Achilles Tendon Rupture in a Danish County," Injury, 29(9), pp. 651-654. (Pubitemid 29000741)
3. Moller, A., Astron, M., and Westlin, N., 1996, "Increasing Incidence of Achilles Tendon Rupture," Acta Orthop. Scand., 67(5), pp. 479-481. (Pubitemid 26393542)
4. Lin, T. W., Cardenas, L., and Soslowsky, L. J., 2004, "Biomechanics of Tendon Injury and Repair," J. Biomech., 37(6), pp. 865-877. (Pubitemid 38521208)
5. Saxena, A., Ewen, B., and Maffulli, N., 2011, "Rehabilitation of the Operated Achilles Tendon: Parameters for Predicting Return to Activity," J. Foot Ankle Surg., 50(1), pp. 37-40.
6. Mullaney, M. J., McHugh, M. P., Tyler, T. F., Nicholas, S. J., and Lee, S. J., 2006, "Weakness in End-Range Plantar Flexion After Achilles Tendon Repair," Am. J. Sports Med., 34(7), pp. 1120-1125. (Pubitemid 43979648)
7. Robinson, J. M., Cook, J. L., Purdam, C., Visentini, P. J., Ross, J., Maffulli, N., Taunton, J. E., and Khan, K. M., 2001, "The VISA-A Questionnaire: A Valid and Reliable Index of the Clinical Severity of Achilles Tendinopathy," Br. J. Sports Med., 35(5), pp. 335-341. (Pubitemid 32929821)
8. Silbernagel, K. G., Nilsson-Helander, K., Thomee, R., Eriksson, B. I., and Karlsson, J., 2010, "A New Measurement of Heel-Rise Endurance With the Ability to Detect Functional Deficits in Patients With Achilles Tendon Rupture," Knee Surg. Sports Traumatol. Arthrosc., 18(2), pp. 258-264.
9. Chinn, L., and Hertel, J., 2010, "Rehabilitation of Ankle and Foot Injuries in Athletes," Clin. Sports Med., 29(1), pp. 157-167.
10. Miller, K. S., Connizzo, B. K., Feeney, E., and Soslowsky, L. J., 2012, "Characterizing Local Collagen Fiber Re-Alignment and Crimp Behavior Throughout Mechanical Testing in a Mature Mouse Supraspinatus Tendon Model," J. Biomech., 45(12), pp. 2061-2065.
11. Miller, K. S., Edelstein, L., Connizzo, B. K., and Soslowsky, L. J., 2012, "Effect of Preconditioning and Stress Relaxation on Local Collagen Fiber Realignment: Inhomogeneous Properties of Rat Supraspinatus Tendon," ASME J. Biomech. Eng., 134(3), p. 031007.
12. Gimbel, J. A., Van Kleunen, J. P., Mehta, S., Perry, S. M., Williams, G. R., and Soslowsky, L. J., 2004, "Supraspinatus Tendon Organizational and Mechanical Properties in a Chronic Rotator Cuff Tear Animal Model," J. Biomech., 37(5), pp. 739-749. (Pubitemid 38445036)
13. Dourte, L. M., Perry, S. M., Getz, C. L., and Soslowsky, L. J., 2010, "Tendon Properties Remain Altered in a Chronic Rat Rotator Cuff Model," Clin. Orthop. Relat. Res., 468(6), pp. 1485-1492.
14. Lake, S. P., Miller, K. S., Elliott, D. M., and Soslowsky, L. J., 2009, "Effect of Fiber Distribution and Realignment on the Nonlinear and Inhomogeneous Mechanical Properties of Human Supraspinatus Tendon Under Longitudinal Tensile Loading," J. Orthop. Res., 27(12), pp. 1596-1602.
15. Quinn, K. P., and Winkelstein, B. A., 2008, "Altered Collagen Fiber Kinematics Define the Onset of Localized Ligament Damage During Loading," J. Appl. Physiol., 105(6), pp. 1881-1888.
16. Quinn, K. P., Bauman, J. A., Crosby, N. D., and Winkelstein, B. A., 2010, "Anomalous Fiber Realignment During Tensile Loading of the Rat Facet Capsular Ligament Identifies Mechanically Induced Damage and Physiological Dysfunction," J. Biomech., 43(10), pp. 1870-1875.
17. Thomopoulos, S., Williams, G. R., Gimbel, J. A., Favata, M., and Soslowsky, L. J., 2003, "Variation of Biomechanical, Structural, and Compositional Properties Along the Tendon to Bone Insertion Site," J. Orthop. Res., 21(3), pp. 413-419. (Pubitemid 36546807)
18. Franchi, M., Torricelli, P., Giavaresi, G., and Fini, M., 2013, "Role of Moderate Exercising on Achilles Tendon Collagen Crimping Patterns and Proteoglycans," Connect. Tissue Res., 54, pp. 267-274.
19. Lau, T. Y., Ambekar, R., and Toussaint, K. C., 2012, "Quantification of Collagen Fiber Organization Using Three-Dimensional Fourier Transform-Second-Harmonic Generation Imaging," Opt. Express, 20(19), pp. 21821-21832.
20. Gusachenko, I., Tran, V., Houssen, Y. G., Allain, J. M., and Schanne-Klein, M. C., 2012, "Polarization-Resolved Second-Harmonic Generation in Tendon Upon Mechanical Stretching," Biophys. J., 102(9), pp. 2220-2229.
21. Abraham, T., Fong, G., and Scott, A., 2011, "Second Harmonic Generation Analysis of Early Achilles Tendinosis in Response to in vivo Mechanical Loading," BMC Musculoskelet. Disord., 12, p. 26.
22. Vidal Bde, C., and Mello, M. L., 2011, "Collagen Type I Amide I Band Infrared Spectroscopy," Micron, 42(3), pp. 283-289.
23. Alfredson, H., Masci, L., and Ohberg, L., 2011, "Partial Mid-portion Achilles Tendon Ruptures: New Sonographic Findings Helpful for Diagnosis," Br. J. Sports Med., 45(5), pp. 429-432.
24. Maranho, D. A., Nogueira-Barbosa, M. H., Simao, M. N., and Volpon, J. B., 2009, "Ultrasonographic Evaluation of Achilles Tendon Repair After Percutaneous Sectioning for the Correction of Congenital Clubfoot Residual Equinus," J. Pediatr. Orthop., 29(7), pp. 804-810.
25. Mangat, K. S., Kanwar, R., Johnson, K., Korah, G., and Prem, H., 2010, "Ultrasonographic Phases in Gap Healing Following Ponseti-Type Achilles Tenotomy," J. Bone Joint Surg. Am., 92(6), pp. 1462-1467.
26. Vadala, A., De Carli, A., Vulpiani, M. C., Iorio, R., Vetrano, M., Scapellato, S., Suarez, T., Di Salvo, F., and Ferretti, A., 2012, "Clinical, Functional and Radiological Results of Achilles Tenorraphy Surgically Treated With Mini-open Technique," J. Sports Med. Phys. Fitness, 52(6), pp. 616-621.
27. Poposka, A., Georgieva, D., and Dzoleva-Tolevska, R., 2012, "Significance of Ultrasound in the Diagnosis and Treatment of Achilles Tendon Rupture," Prilozi, 33(1), pp. 209-216.
28. Chamberlain, C. S., Duenwald-Kuehl, S. E., Okotie, G., Brounts, S. H., Baer, G. S., and Vanderby, R., 2013, "Temporal Healing in Rat Achilles Tendon: Ultrasound Correlations," Ann. Biomed. Eng., 41(3), pp. 477-487.
29. Duenwald-Kuehl, S., Lakes, R., and Vanderby, R., Jr., 2012, "Strain-Induced Damage Reduces Echo Intensity Changes in Tendon During Loading," J. Biomech., 45(9), pp. 1607-1611.
30. Bashford, G. R., Tomsen, N., Arya, S., Burnfield, J. M., and Kulig, K., 2008, "Tendinopathy Discrimination by Use of Spatial Frequency Parameters in Ultrasound B-Mode Images," IEEE Trans. Med. Imaging, 27(5), pp. 608-615. (Pubitemid 351634369)
31. Kulig, K., Landel, R., Chang, Y. J., Hannanvash, N., Reischl, S. F., Song, P., and Bashford, G. R., 2013, "Patellar Tendon Morphology in Volleyball Athletes With and Without Patellar Tendinopathy," Scand. J. Med. Sci. Sports, 23(2), pp. e81-e88.
32. Chen, X. M., Cui, L. G., He, P., Shen, W. W., Qian, Y. J., and Wang, J. R., 2013, "Shear Wave Elastographic Characterization of Normal and Torn Achilles Tendons: A Pilot Study," J. Ultrasound Med., 32(3), pp. 449-455.
33. Shah, S. A., Santago, P., and Rubin, B. K., 2005, "Quantification of Biopolymer Filament Structure," Ultramicroscopy, 104(3-4), pp. 244-254. (Pubitemid 40982467)
34. Gimbel, J. A., Mehta, S., Van Kleunen, J. P., Williams, G. R., and Soslowsky, L. J., 2004, "The Tension Required at Repair to Reappose the Supraspinatus Tendon to Bone Rapidly Increases After Injury," Clin. Orthop. Rela.t Res., 4(26), pp. 258-265. (Pubitemid 39167139)
35. Garcia, T., Hornof, W. J., and Insana, M. F., 2003, "On the Ultrasonic Properties of Tendon," Ultrasound Med. Biol., 29(12), pp. 1787-1797. (Pubitemid 38091728)
36. Khoury, V., Guillin, R., Dhanju, J., and Cardinal, E., 2007, "Ultrasound of Ankle and Foot: Overuse and Sports Injuries," Semin. Musculoskelet. Radiol., 11(2), pp. 149-161.
37. VisualSonics, 2007, VisualSonics 700-Series RMV Scanhead Selector, Visual-Sonics, Toronto.
38. Hansen, P., Haraldsson, B. T., Aagaard, P., Kovanen, V., Avery, N. C., Qvortrup, K., Larsen, J. O., Krogsgaard, M., Kjaer, M., and Peter Magnusson, S., 2010, "Lower Strength of the Human Posterior Patellar Tendon Seems Unrelated to Mature Collagen Cross-Linking and Fibril Morphology," J. Appl. Physiol., 108(1), pp. 47-52.
39. Ros, S. J., Andarawis-Puri, N., and Flatow, E. L., 2013, "Tendon extracellular matrix damage detection and quantification using automated edge detection analysis," J. Biomech., 46(16), pp. 2844-2847.