Functional analysis of limb recovery following autograft treatment of volumetric muscle loss in the quadriceps femoris

Journal of Biomechanics

Volumn 47, Issue 9, 2014, Pages 2013-2021

  Li, Mon Tzu A ^a,b   Willett, Nick J ^a,c   Uhrig, Brent A ^a,c   Guldberg, Robert E ^a,c   Warren, Gordon L ^d  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^b Emory University   (United States)

^c GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^d GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Gait analysis; Muscle autograft; Muscle functional testing; Preclinical model; Volumetric muscle loss

Indexed keywords

DEFECTS; FUNCTION EVALUATION; GAIT ANALYSIS; RECOVERY;

FUNCTIONAL RECOVERY; FUNCTIONAL TESTING; HISTOLOGICAL SECTION; MUSCLE FUNCTION; MUSCLE STRENGTH; MUSCLE TISSUES; OUTCOME MEASURES; SKELETAL MUSCLE;

MUSCLE;

ANALYSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOGRAFT; CONTROLLED STUDY; FEMALE; FUNCTIONAL ANALYSIS; FUNCTIONAL ASSESSMENT; GAIT; HISTOPATHOLOGY; LIMB; MUSCLE CONTRACTION; MUSCLE FUNCTION; MUSCLE GRAFT; MUSCLE INJURY; MUSCLE REGENERATION; MUSCLE STRENGTH; MYOFIBROSIS; NONHUMAN; PRIORITY JOURNAL; QUADRICEPS FEMORIS MUSCLE; RAT;

GAIT ANALYSIS; MUSCLE AUTOGRAFT; MUSCLE FUNCTIONAL TESTING; PRECLINICAL MODEL; VOLUMETRIC MUSCLE LOSS;

ANIMALS; AUTOGRAFTS; FEMALE; GAIT; MUSCLE CONTRACTION; MUSCLE STRENGTH; QUADRICEPS MUSCLE; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; REGENERATION;

EID: 84901605064     PISSN: 00219290     EISSN: 18732380     Source Type: Journal    
DOI: 10.1016/j.jbiomech.2013.10.057     Document Type: Article

References (45)

1. Bierinx A.S., Sebille A. Mouse sectioned muscle regenerates following auto-grafting with muscle fragments: a new muscle precursor cells transfer?. Neurosci. lett. 2008, 431:211-214.
2. Bozkurt A., Deumens R., Scheffel J., O'Dey D.M., Weis J., Joosten E.A., Fuhrmann T., Brook G.A., Pallua N. Catwalk gait analysis in assessment of functional recovery after sciatic nerve injury. J. Neurosci. Methods 2008, 173:91-98.
3. Burke R.E., Levine D.N., Tsairis P., Zajac F.E. Physiological types and histochemical profiles in motor units of the cat gastrocnemius. J. Physiol. 1973, 234:723-748.
4. Carlson B.M., Gutmann E. Development of contractile properties of minced muscle regenerates in the rat. Exp. Neurol. 1972, 36:239-249.
5. Castillo R.C., MacKenzie E.J., Wegener S.T., Bosse M.J. Prevalence of chronic pain seven years following limb threatening lower extremity trauma. Pain 2006, 124:321-329.
6. Corona B.T., Garg K., Ward C.L., McDaniel J.S., Walters T.J., Rathbone C.R. Autologous minced muscle grafts: a tissue engineering therapy for the volumetric loss of skeletal muscle. American journal of physiology. Cell Physiol 2013.
7. Deumens R., Jaken R.J., Marcus M.A., Joosten E.A. The CatWalk gait analysis in assessment of both dynamic and static gait changes after adult rat sciatic nerve resection. J. Neurosci. Methods 2007, 164:120-130.
8. Duda G.N., Taylor W.R., Winkler T., Matziolis G., Heller M.O., Haas N.P., Perka C., Schaser K.D. Biomechanical, microvascular, and cellular factors promote muscle and bone regeneration. Exercise Sport Sci. Rev. 2008, 36:64-70.
9. Fischer M.D., Gustilo R.B., Varecka T.F. The timing of flap coverage, bone-grafting, and intramedullary nailing in patients who have a fracture of the tibial shaft with extensive soft-tissue injury. J. Bone Joint Surg. Am. 1991, 73:1316-1322.
10. Giannoudis P.V., Harwood P.J., Kontakis G., Allami M., Macdonald D., Kay S.P., Kind P. Long-term quality of life in trauma patients following the full spectrum of tibial injury (fasciotomy, closed fracture, grade IIIB/IIIC open fracture and amputation). Injury 2009, 40:213-219.
11. Gillies A.R., Lieber R.L. Structure and function of the skeletal muscle extracellular matrix. Muscle Nerve 2011, 44:318-331.
12. Godina M., Bajec J., Baraga A. Salvage of the mutilated upper extremity with temporary ectopic implantation of the undamaged part. Plast. Reconstr. Surg. 1986, 78:295-299.
13. Gopal S., Majumder S., Batchelor A.G., Knight S.L., De Boer P., Smith R.M. Fix and flap: the radical orthopaedic and plastic treatment of severe open fractures of the tibia. J. Bone Joint Surg. Br 2000, 82:959-966.
14. Grogan B.F., Hsu J.R. Volumetric muscle loss. J. Am Acad. Orthop. Surg. 2011, 19(Suppl. 1):S35-37.
15. Hamers F.P., Lankhorst A.J., van Laar T.J., Veldhuis W.B., Gispen W.H. Automated quantitative gait analysis during overground locomotion in the rat: its application to spinal cord contusion and transection injuries. J. Neurotrauma 2001, 18:187-201.
16. Huh J., Stinner D.J., Burns T.C., Hsu J.R. Infectious complications and soft tissue injury contribute to late amputation after severe lower extremity trauma. J. Trauma 2011, 71:S47-51.
17. Kaariainen M., Kauhanen S. Skeletal muscle injury and repair: the effect of disuse and denervation on muscle and clinical relevance in pedicled and free muscle flaps. J. Reconstructive Microsurgery 2012, 28:581-587.
18. Lee Y.S., Kwon S.T., Kim J.O., Choi E.S. Serial MR imaging of intramuscular hematoma: experimental study in a rat model with the pathologic correlation. Korean J. Radiol.: Off. J. Korean Radiol. Soc. 2011, 12:66-77.
19. Lowe D.A., Warren G.L., Ingalls C.P., Boorstein D.B., Armstrong R.B. Muscle function and protein metabolism after initiation of eccentric contraction-induced injury. J. Appl. Physiol. 1995, 79:1260-1270.
20. MacKenzie E.J., Bosse M.J., Kellam J.F., Burgess A.R., Webb L.X., Swiontkowski M.F., Sanders R.W., Jones A.L., McAndrew M.P., Patterson T.M., McCarthy M.L. Characterization of patients with high-energy lower extremity trauma. J. Orthop. Trauma 2000, 14:455-466.
21. MacKenzie E.J., Bosse M.J., Pollak A.N., Webb L.X., Swiontkowski M.F., Kellam J.F., Smith D.G., Sanders R.W., Jones A.L., Starr A.J., McAndrew M.P., Patterson B.M., Burgess A.R., Castillo R.C. Long-term persistence of disability following severe lower-limb trauma. Results of a seven-year follow-up. J. Bone Joint Surg. Am. 2005, 87:1801-1809.
22. MacKenzie E.J., Jones A.S., Bosse M.J., Castillo R.C., Pollak A.N., Webb L.X., Swiontkowski M.F., Kellam J.F., Smith D.G., Sanders R.W., Jones A.L., Starr A.J., McAndrew M.P., Patterson B.M., Burgess A.R. Health-care costs associated with amputation or reconstruction of a limb-threatening injury. J. Bone Joint Surg. Am. 2007, 89:1685-1692.
23. Masini B.D., Waterman S.M., Wenke J.C., Owens B.D., Hsu J.R., Ficke J.R. Resource utilization and disability outcome assessment of combat casualties from operation Iraqi freedom and operation enduring freedom. J. Orthop. Trauma 2009, 23:261-266.
24. Merritt E.K., Cannon M.V., Hammers D.W., Le L.N., Gokhale R., Sarathy A., Song T.J., Tierney M.T., Suggs L.J., Walters T.J., Farrar R.P. Repair of traumatic skeletal muscle injury with bone-marrow-derived mesenchymal stem cells seeded on extracellular matrix. Tissue Eng. Part A 2010, 16:2871-2881.
25. Merritt E.K., Hammers D.W., Tierney M., Suggs L.J., Walters T.J., Farrar R.P. Functional assessment of skeletal muscle regeneration utilizing homologous extracellular matrix as scaffolding. Tissue Eng. Part A 2010, 16:1395-1405.
26. Meyer G.A., Lieber R.L. Elucidation of extracellular matrix mechanics from muscle fibers and fiber bundles. J. Biomech. 2011, 44:771-773.
27. Oswald T.M., Zhang F., Lei M.P., Gerzenshtein J., Lineaweaver W.C. Muscle flap mass preservation with end-to-side neurorrhaphy: an experimental study. J. Reconstructive Microsurgery 2004, 20:483-488.
28. Owens B.D., Kragh J.F., Macaitis J., Svoboda S.J., Wenke J.C. Characterization of extremity wounds in Operation Iraqi freedom and operation enduring freedom. J. Orthop. Trauma 2007, 21:254-257.
29. Page R.L., Malcuit C., Vilner L., Vojtic I., Shaw S., Hedblom E., Hu J., Pins G.D., Rolle M.W., Dominko T. Restoration of skeletal muscle defects with adult human cells delivered on fibrin microthreads. Tissue Eng. Part A 2011, 17:2629-2640.
30. Pollak A.N., McCarthy M.L., Burgess A.R. Short-term wound complications after application of flaps for coverage of traumatic soft-tissue defects about the tibia. The Lower Extremity Assessment Project (LEAP) study group. J. Bone Joint Surg. Am. 2000, 82-A:1681-1691.
31. Richards R.R., Schemitsch E.H. Effect of muscle flap coverage on bone blood flow following devascularization of a segment of tibia: an experimental investigation in the dog. J. Orthop. Res. 1989, 7:550-558.
32. Rossi C.A., Flaibani M., Blaauw B., Pozzobon M., Figallo E., Reggiani C., Vitiello L., Elvassore N., De Coppi P. In vivo tissue engineering of functional skeletal muscle by freshly isolated satellite cells embedded in a photopolymerizable hydrogel. FASEB J.: Off. Pub. Fed. Am. Soc. Exp. Biol. 2011, 25:2296-2304.
33. Schemitsch E.H., Weinberg J.A., McKee M.D., Richards R.R. The relative importance of intramedullary, intracortical, and extraosseous soft-tissue blood flow to the repair of devascularized canine tibial cortex. Ann. Plast. Surg. 1997, 38:623-631.
34. Sicari B.M., Agrawal V., Siu B.F., Medberry C.J., Dearth C.L., Turner N.J., Badylak S.F. A murine model of volumetric muscle loss and a regenerative medicine approach for tissue replacement. Tissue Eng. Part A 2012, 18:1941-1948.
35. Turner N.J., Badylak J.S., Weber D.J., Badylak S.F. Biologic scaffold remodeling in a dog model of complex musculoskeletal injury. J. Surgical Res. 2012, 176:490-502.
36. Turner N.J., Yates A.J., Weber D.J., Qureshi I.R., Stolz D.B., Gilbert T.W., Badylak S.F. Xenogeneic extracellular matrix as an inductive scaffold for regeneration of a functioning musculotendinous junction. Tissue Eng. Part A 2010, 16:3309-3317.
37. Uhrig B.A., Clements I.P., Boerckel J.D., Huebsch N., Bellamkonda R.V., Guldberg R.E. Characterization of a composite injury model of severe lower limb bone and nerve trauma. J. Tissue Eng. Regenerative Med 2012, 10.1002/term.1537.
38. Warren G.L., Stallone J.L., Allen M.R., Bloomfield S.A. Functional recovery of the plantarflexor muscle group after hindlimb unloading in the rat. Eur. J. Appl. Physiol. 2004, 93:130-138.
39. Willett N.J., Li M.T., Uhrig B.A., Boerckel J.D., Huebsch N., Lundgren T.L., Warren G.L., Guldberg R.E. Attenuated human bone morphogenetic protein-2-mediated bone regeneration in a rat model of composite bone and muscle injury. Tissue Eng. Part C, Methods 2013, 19:316-325.
40. Winkler T., von Roth P., Matziolis G., Schumann M.R., Hahn S., Strube P., Stoltenburg-Didinger G., Perka C., Duda G.N., Tohtz S.V. Time course of skeletal muscle regeneration after severe trauma. Acta Orthop. 2011, 82:102-111.
41. Yoshitatsu S., Matsuda K., Yano K., Hosokawa K., Tomita K. Muscle flap mass preservation by sensory reinnervation with end-to-side neurorrhaphy: an experimental study in rats. J. Reconstructive Microsurgery 2008, 24:479-487.
42. Zahir K.S., Syed S.A., Zink J.R., Restifo R.J., Thomson J.G. Comparison of the effects of ischemic preconditioning and surgical delay on pedicled musculocutaneous flap survival in a rat model. Ann. Plast. Surg. 1998, 40:422-428. (discussion 428-429).
43. Zahir K.S., Syed S.A., Zink J.R., Restifo R.J., Thomson J.G. Ischemic preconditioning improves the survival of skin and myocutaneous flaps in a rat model. Plast. Reconstr. Surg. 1998, 102:140-150. (discussion 151-142).
44. Zahir T.M., Zahir K.S., Syed S.A., Restifo R.J., Thomson J.G. Ischemic preconditioning of musculocutaneous flaps: effects of ischemia cycle length and number of cycles. Ann. Plast. Surg. 1998, 40:430-435.
45. Zhang F., Lineaweaver W.C., Ustuner T., Kao S.D., Tonken H.P., Campagna-Pinto D., Buncke H.J. Comparison of muscle mass preservation in denervated muscle and transplanted muscle flaps after motor and sensory reinnervation and neurotization. Plast. Reconstr. Surg. 1997, 99:803-814.