Intramuscular connective tissue (IMCT) forms a series of continuous networks integrating muscle fibers and fascicles into a whole organ. The contributions of IMCT to cooked meat toughness have long been recognized. This review concentrates on () the potential to manipulate IMCT in the growing animal, () postmortem effects on structure and properties of IMCT, and () developments in techniques to quantify IMCT in meat. A new hypothesis can explain why IMCT is enzymatically degraded in postmortem aging; however, after cooking, no differences are seen in the IMCT contribution to toughness. This hypothesis proposes that heat-insoluble collagen occurs in a weak pool and a strong pool, where the weak pool is most easily degraded by both proteolysis and heat. Far from being a constant background feature, the IMCT contribution to cooked meat toughness can be varied and deserves fresh research on how to achieve this.


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Literature Cited

  1. Albrecht E, Teuscher F, Ender K, Wegner J. 2006. Growth- and breed-related changes of muscle bundle structure in cattle. J. Anim. Sci. 84:112959–64 [Google Scholar]
  2. An JY, Zheng JX, Li JY, Zeng D, Qu LJ. et al. 2010. Effect of myofiber characteristics and thickness of perimysium and endomysium on meat tenderness of chickens. Poultry Sci. 89:81750–54 [Google Scholar]
  3. Archile-Contreras A, Cha M, Mandell I, Miller S, Purslow PP. 2011. Vitamins E and C may increase collagen turnover by intramuscular fibroblasts. Potential for improved meat quality. J. Agric. Food Chem. 59:608–14 [Google Scholar]
  4. Archile-Contreras AC, Mandell IB, Purslow PP. 2010. Phenotypic differences in matrix metalloproteinase 2 activity between fibroblasts from three bovine muscles. J. Anim. Sci. 88:4006–15 [Google Scholar]
  5. Archile-Contreras AC, Purslow PP. 2011. Oxidative stress may affect meat quality by interfering with collagen turnover by muscle fibroblasts. Food Res. Int. 44:582–88 [Google Scholar]
  6. Avery NC, Sims TJ, Bailey AJ. 2009. Quantitative determination of collagen cross-links. Methods in Molecular Biology 522 Extracellular Matrix Protocols S Even-Ram, V Artym 103–21 New York: Humana [Google Scholar]
  7. Bailey AJ, Light ND. 1989. Connective Tissue in Meat and Meat Products London: Elsevier [Google Scholar]
  8. Bailey AJ, Paul RG, Knott L. 1998. Mechanisms of maturation and ageing of collagen. Mechanisms Ageing Dev. 106:1–56 [Google Scholar]
  9. Balcerzak D, Querengesser L, Dixon WT, Baracos VE. 2001. Coordinate expression of matrix-degrading proteinases and their activators and inhibitors in bovine skeletal muscle. J. Anim. Sci. 79:94–107 [Google Scholar]
  10. Bell RD, Shultz SJ, Wideman L, Heinrich VC. 2012. Collagen gene variants associated with anterior cruciate ligament injury risk are also associated with joint laxity. Sports Health: Multidiscip. Approach 4:312–18 [Google Scholar]
  11. Bendall JR. 1967. The elastin content of various muscles of beef animals. J. Sci. Food Agric. 18:553–58 [Google Scholar]
  12. Bernal VM, Stanley DW. 1987. Stability of bovine muscle connective tissues. J. Food Sci. 52:876–78 [Google Scholar]
  13. Blanco MR, Alonso CR. 2010. Collagen types I and III in bovine muscles: influence of age and breed. J. Muscle Foods 21:417–23 [Google Scholar]
  14. Bouton PE, Harris PV. 1972. The effects of some post-slaughter treatments on the mechanical properties of bovine and ovine muscle. J. Food Sci. 37:539–43. [Google Scholar]
  15. Bouton PE, Harris PV, Ratcliff D. 1981. Effect of cooking temperature and time on the shear properties of meat. J. Food Sci. 46:1082–87 [Google Scholar]
  16. Bouton PE, Harris PV, Shorthose WR. 1975. Possible relationships between shear, tensile, and adhesion properties. J. Texture Stud. 6:297–314 [Google Scholar]
  17. Bowman W. 1840. On the minute structure and movements of voluntary muscle. Phil. Trans. R. Soc. Lond. 130:457–501 [Google Scholar]
  18. Brüggemann DA, Brewer J, Risbo J, Bagatolli L. 2010. Second harmonic generation microscopy: a tool for spatially and temporally resolved studies of heat induced structural changes in meat. Food Biophys. 5:1–8 [Google Scholar]
  19. Camp RJ, Liles M, Beale J, Saeidi N, Flynn BP. et al. 2011. Molecular mechanochemistry: low force switch slows enzymatic cleavage of human type I collagen monomer. J. Am. Chem. Soc. 133:4073–78 [Google Scholar]
  20. Casas E, White SN, Wheeler TL, Shackelford SD, Koohmaraie M. et al. 2006. Effects of calpastatin and micro-calpain markers in beef cattle on tenderness traits. J. Anim. Sci. 84:520–25 [Google Scholar]
  21. Cassar-Malek I, Hocquette JF, Jurie C, Listrat A, Jailler R. et al. 2004. Muscle-specific metabolic, histochemical and biochemical responses to a nutritionally induced discontinuous growth path. Anim. Sci. 79:49–59 [Google Scholar]
  22. Cha MC, Purslow PP. 2010. Matrix metalloproteinases are less essential for the in-situ gelatinolytic activity in heart muscle than in skeletal muscle. Comp. Biochem. Physiol. A 156:518–22 [Google Scholar]
  23. Cha MC, Purslow PP. 2011. Epinephrine-induced MMP expression is different between fibroblasts and myoblasts. Cell Biochem. Funct. 29:603–9 [Google Scholar]
  24. Cha MC, Purslow PP. 2012. Expressions of the matrix metalloproteinase and its inhibitor are modified by beta-adrenergic agonist ractopamine in skeletal fibroblasts and myoblasts. Can. J. Anim. Sci. 92:159–66 [Google Scholar]
  25. Christensen L, Bertram HC, Aaslyng MD, Christensen M. 2011a. Protein denaturation and water–protein interactions as affected by low temperature long time treatment of porcine Longissimus dorsi. Meat Sci. 88:718–22 [Google Scholar]
  26. Christensen M, Ertbjerg P, Failla S, Sañudo C, Richardson RI. et al. 2011b. Relationship between collagen characteristics, lipid content and raw and cooked texture of meat from young bulls of fifteen European breeds. Meat Sci. 87:61–65 [Google Scholar]
  27. Das C, Roy BC, Oshima I, Miyachi H, Nishimura S. et al. 2010. Collagen content and architecture of the pectoralis muscle in male chicks and broilers reared under various nutritional conditions. Anim. Sci. J. 81:252–63 [Google Scholar]
  28. Dubost A, Micol D, Meunier B, Lethias C, Listrat A. 2013. Relationships between structural characteristics of bovine intramuscular connective tissue assessed by image analysis and collagen and proteoglycan content. Meat Sci. 93:378–86 [Google Scholar]
  29. El Jabri M, Abouelkaram S, Damez JL, Berge P. 2010. Image analysis study of the perimysial connective network, and its relationship with tenderness and composition of bovine meat. J. Food Eng. 96:316–22 [Google Scholar]
  30. Flynn BP, Bhole AP, Saeidi N, Liles M, Dimarzio CA, Ruberti JW. 2010. Mechanical strain stabilizes reconstituted collagen fibrils against enzymatic degradation by mammalian collagenase matrix metalloproteinase 8 (MMP-8). PLoS One 5:8e12337 [Google Scholar]
  31. Foegeding AE, Larick DK. 1986. Tenderization of beef with bacterial collagenase. Meat Sci. 18:201–14 [Google Scholar]
  32. Galvis L, Dunlop JWC, Duda G, Fratzl P, Masic A. 2013. Polarized Raman anisotropic response of collagen in tendon: towards 3D orientation mapping of collagen in tissues. PLoS One 8:5e63518 [Google Scholar]
  33. Gerrard DE, Jones SJ, Aberle ED, Lemenager RP, Judge MD. 1987. Collagen stability, testosterone secretion and meat tenderness in growing bulls and steers. J. Anim. Sci. 65:1236–42 [Google Scholar]
  34. Girard I, Aalhus JL, Basarab JA, Larsen IL, Bruce HL. 2011. Modification of muscle inherent properties through age at slaughter, growth promotants and breed crosses. Can. J. Anim. Sci. 91:635–48 [Google Scholar]
  35. Girard I, Bruce HL, Basarab JA, Larsen IL, Aalhus JL. 2012. Contribution of myofibrillar and connective tissue components to the Warner-Bratzler shear force of cooked beef. Meat Sci. 92:775–82 [Google Scholar]
  36. Ichinoseki S, Nishiumi T, Susuki A. 2006. Tenderizing effect of high hydrostatic pressure on bovine intramuscular connective tissue. J. Food Sci. 71:E276–81 [Google Scholar]
  37. Kang CK, Rice EE. 1970. Degradation of various meat fractions by tenderizing enzymes. J. Food Sci. 35:563–65 [Google Scholar]
  38. Kim JH, Pyun JA, Lee KJ, Cho SW, Kwack KB. 2011. Study on association between single nucleotide polymorphisms of MMP7, MMP8, MMP9 genes and development of gastric cancer and lymph node metastasis. Korean J. Gastroenterol. 58:245–51 [Google Scholar]
  39. Kjær M. 2004. Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading. Physiol. Rev. 84:649–98 [Google Scholar]
  40. Kjær M, Magnusson P, Krogsgaard M, Moller JB, Olesen J. et al. 2006. Extracellular matrix adaptation of tendon and skeletal muscle to exercise. J. Anat. 208:445–50 [Google Scholar]
  41. Kragstrup TW, Kjaer M, Mackey AL. 2011. Structural, biochemical, cellular, and functional changes in skeletal muscle extracellular matrix with aging. Scand. J. Med. Sci. Sports 21:749–57 [Google Scholar]
  42. Kristensen L, Therkildsen M, Riis B, Sorensen MT, Oksbjerg N. et al. 2002. Dietary-induced changes of muscle growth rate in pigs: effects on in vivo and postmortem muscle proteolysis and meat quality. J. Anim. Sci. 80:2862–71 [Google Scholar]
  43. Kronick P, Maleeff B, Carroll R. 1988. The locations of collagens with different thermal stabilities in fibrils of bovine reticular dermis. Connect. Tissue Res. 18:123–34 [Google Scholar]
  44. Kulmyrzaev A, Bertrand D, Lepetit J, Listrat A, Laguet A, Dufour E. 2012. Potential of a custom-designed fluorescence imager combined with multivariate statistics for the study of chemical and mechanical characteristics of beef meat. Food Chem. 131:1030–36 [Google Scholar]
  45. Lewis GJ, Purslow PP. 1990. Connective tissue differences in the strength of cooked meat across the muscle fibre direction due to test specimen size. Meat Sci. 28:183–94 [Google Scholar]
  46. Lewis GJ, Purslow PP, Rice AE. 1991. The effect of conditioning on the strength of perimysial connective tissue dissected from cooked meat. Meat Sci. 30:1–12 [Google Scholar]
  47. Light N, Champion AE, Voyle C, Bailey AJ. 1985. The role of epimysial, perimysial and endomysial collagen in determining texture in six bovine muscles. Meat Sci. 13:137–49 [Google Scholar]
  48. Lin C-C, Yang W-C, Chung M-Y, Lee P-C. 2010. Functional polymorphisms in matrix metalloproteinases-1, -3, -9 are associated with arteriovenous fistula patency in hemodialysis patients. J. Am. Soc. Nephrol. 5:1805–14 [Google Scholar]
  49. Listrat A, Lethias C, Hocquette JF, Renand G, Ménissier F. et al. 2000. Age related changes and location of types I, III, XII and XIV collagen during development of skeletal muscles from genetically different animals. Histochem. J. 32:349–56 [Google Scholar]
  50. Listrat A, Picard B, Geay Y. 1999. Age-related changes and location of type I, III, IV, V and VI collagens during development of four foetal skeletal muscles of double muscles and normal bovine muscles. Tissue Cell 31:17–27 [Google Scholar]
  51. Liu A, Nishimura T, Takahashi K. 1996. Relationship between structural properties of intramuscular connective tissue and toughness of various chicken skeletal muscles. Meat Sci. 43:43–49 [Google Scholar]
  52. Mahmoud-Ghoneim D, Bonny J-M, Renou J-P, De Certaines JD. 2005. Ex-vivo magnetic resonance image texture analysis can discriminate genotypic origin in bovine meat. J. Sci. Food Agric. 85:629–32 [Google Scholar]
  53. Mayne R, Sanderson RD. 1985. The extracellular matrix of skeletal muscle. Collagen Relat. Res. 5:449–68 [Google Scholar]
  54. McCormick RJ. 1994. The flexibility of the collagen compartment of muscle. Meat Sci. 36:79–91 [Google Scholar]
  55. McCormick RJ. 2009. Collagen. Applied Muscle Biology and Meat Science M Du, RJ McCormick 129–48 New York: CRC Press [Google Scholar]
  56. McMeekan CP. 1940. Growth and development in the pig, with special references to carcass quality characters. III. Effects of plane of nutrition on the form and composition of the bacon pig. J. Agric. Sci. 30:511–69 [Google Scholar]
  57. Møller AJ. 1980. Analysis of Warner-Bratzler shear pattern with regard to myofibrillar and connective tissue components of tenderness. Meat Sci. 5:247–60 [Google Scholar]
  58. Murphy G. 2010. Fell-Muir lecture: Metalloproteinases: from demolition squad to master regulators. Int. J. Exp. Pathol. 91:303–13 [Google Scholar]
  59. Nishimura T. 2010. The role of intramuscular connective tissue in meat texture. Anim. Sci. J. 81:21–27 [Google Scholar]
  60. Nishimura T, Fang S, Wakamatsu J, Takahashi K. 2009. Relationships between physical and structural properties of intramuscular connective tissue and toughness of raw pork. Anim. Sci. J. 80:85–90 [Google Scholar]
  61. Nishimura T, Liu A, Hattori A, Takahashi K. 1998. Changes in mechanical strength of intramuscular connective tissue during postmortem aging of beef. J. Anim. Sci. 76:528–32 [Google Scholar]
  62. Pambuka SE, Adebiyi AP, Muramoto K, Naudé RJ. 2007. Purification and partial characterisation of a matrix metalloproteinase from ostrich skeletal muscle, and its activity during meat maturation. Meat Sci. 76:481–88 [Google Scholar]
  63. Passerieux E, Rossignol R, Chopard A, Carnino A, Marini JF. et al. 2006. Structural organization of the perimysium in bovine skeletal muscle: Junctional plates and associated intracellular subdomains. J. Struct. Biol. 154:206–16 [Google Scholar]
  64. Pietrasik Z, Aalhus JL, Gibson LL, Shand PJ. 2010. Influence of blade tenderization, moisture enhancement and pancreatin enzyme treatment on the processing characteristics and tenderness of beef semitendinosus muscle. Meat Sci. 84:512–17 [Google Scholar]
  65. Prieto N, Roehe R, Lavín P, Batten G, Andrés S. 2009. Application of near infrared reflectance spectroscopy to predict meat and meat products quality: a review. Meat Sci. 83:175–86 [Google Scholar]
  66. Purslow PP. 1985. The physical basis of meat texture: observations on the fracture behaviour of cooked bovine M. semitendinosus. Meat Sci. 12:39–60 [Google Scholar]
  67. Purslow PP. 1987. The fracture properties and thermal analysis of collagenous tissue. Advances in Meat Research 4 AM Pearson, TR Dutson, AJ Bailey 187–208 New York: Van Nostrand Reinhold [Google Scholar]
  68. Purslow PP. 1999. The intramuscular connective tissue matrix and cell-matrix interactions in relation to meat toughness. Proceedings of the 45th International Congress of Meat Science and Technology (Yokohama)210–19 Yokohama, Jpn.: Jpn. Soc. Meat Sci. Technol. [Google Scholar]
  69. Purslow PP. 2002. The structure and functional significance of variations in the connective tissue within muscle. Comp. Biochem. Physiol. A 133:947–66 [Google Scholar]
  70. Purslow PP. 2005. Intramuscular connective tissue and its role in meat quality—a review. Meat Sci. 70:435–47 [Google Scholar]
  71. Purslow PP. 2008. The extracellular matrix of skeletal and cardiac muscle. Collagen: Structure and Mechanics P Fratzl 325–58 New York: Springer [Google Scholar]
  72. Purslow PP. 2010. Muscle fascia and force transmission. J. Bodyw. Mov. Ther. 14:411–17 [Google Scholar]
  73. Purslow PP, Archile-Contreras AC, Cha MC. 2012. Manipulating meat tenderness by increasing the turnover of intramuscular connective tissue. J. Anim. Sci. 90:950–59 [Google Scholar]
  74. Purslow PP, Delage J-P. 2012. General anatomy of the muscle fasciae. Fascia: The Tensional Network of the Human Body R Schleip, T Findley, L Chaitow, PA Huijing 5–10 London: Elsevier [Google Scholar]
  75. Purslow PP, McEwen PL. 2013. The effects of limited feeding and compensatory growth on growth performance, feed efficiency and meat quality in swine. Proceedings of the 50th Annual Meeting of the Brazilian Society of Animal Science (Campinas, SP, Brazil). Campinas, Brazil: Brazil. Soc. Anim. Sci. [Google Scholar]
  76. Purslow PP, Trotter JA. 1994. The morphology and mechanical properties of endomysium in series-fibred muscles: variations with muscle length. J. Muscle Res. Cell Motil. 15:299–304 [Google Scholar]
  77. Ricard-Blum S, Ruggiero F. 2005. The collagen superfamily: from the extracellular matrix to the cell membrane. Pathol. Biol. 53:430–42 [Google Scholar]
  78. Rompala RE, Jones. 1984. Changes in the solubility of bovine intramuscular collagen due to nutritional regime. Growth 48:466–72 [Google Scholar]
  79. Rowe RWD. 1981. Morphology of perimysial and endomysial connective tissue in skeletal muscle. Tissue Cell 13:681–90 [Google Scholar]
  80. Ruberti JW, Hallab NJ. 2005. Strain-controlled enzymatic cleavage of collagen in loaded matrix. Biochem. Biophys. Res. Commun. 336:483–89 [Google Scholar]
  81. Rutter JL, Mitchell TI, Butticè G, Meyers J, Gusella JF. et al. 1998. A single nucleotide polymorphism in the matrix metalloproteinase-1 promoter creates an ETS binding site and augments transcription. Cancer Res. 58:5321–25 [Google Scholar]
  82. Sahar A, Boubellouta T, Lepetit J, Dufour E. 2009. Front-face fluorescence spectroscopy as a tool to classify seven bovine muscles according to their chemical and rheological characteristics. Meat Sci. 83:672–77 [Google Scholar]
  83. Sanes JR. 2003. The basement membrane/basal lamina of skeletal muscle. J. Biol. Chem. 278:12601–4 [Google Scholar]
  84. Sifre L, Berge P, Engel E, Martin J-F, Bonny J-M. et al. 2005. Influence of the spatial organization of the perimysium on beef tenderness. J. Agric. Food Chem. 53:8390–99 [Google Scholar]
  85. Sikes A, Tornverg E, Tume R. 2010. A proposed mechanism of tenderizing post-rigor beef using high pressure-heat treatment. Meat Sci 84:390–99 [Google Scholar]
  86. Snowden JM, Bouton PE, Harris PV. 1977. Influence of constraint during heating and cooling on the mechanical properties of collagenous tissue. J. Food Sci. 42:890–94 [Google Scholar]
  87. Stanton C, Light N. 1988. The effects of conditioning on meat collagen: Part 2—Direct biochemical evidence for proteolytic damage in insoluble perimysial collagen after conditioning. Meat Sci. 23:179–99 [Google Scholar]
  88. Suelves M, López-Alemany R, Lluís F, Aniorte G, Serrano E, Parra M. 2002. Plasmin activity is required for myogenesis in vitro and skeletal muscle regeneration in vivo. Blood 99:2835–44 [Google Scholar]
  89. Sullivan GA, Calkins CR. 2010. Application of exogenous enzymes to beef muscle of high and low-connective tissue. Meat Sci. 85:730–34 [Google Scholar]
  90. Swatland HJ. 2005. A method for simultaneous fluorometry and rheology of connective tissue in bulk meat. Meat Sci. 70:605–11 [Google Scholar]
  91. Swatland HJ. 2006. Stratification of connective tissue toughness in beef roasts assessed by simultaneous fluorometry and penetrometry. Food Res. Int. 39:1106–9 [Google Scholar]
  92. Sylvestre MN, Balcerzak D, Feidt C, Baracos VE, Bellut JB. 2002. Elevated rate of collagen solubilization and postmortem degradation in muscles of lambs with high growth rates: possible relationship with activity of matrix metalloproteinases. J. Anim. Sci. 80:1871–78 [Google Scholar]
  93. Taylor RG. 2004. Connective tissue structure, function and influence on meat quality. Encyclopedia of Meat Sciences WK Jensen 306–13 Amsterdam: Elsevier [Google Scholar]
  94. Therkildsen M, Riis B, Karlsson A, Kristensen L, Ertbjerg P. et al. 2002. Compensatory growth response in pigs, muscle protein turn-over and meat texture: effects of restriction/realimentation period. Anim. Sci. 75:367–77 [Google Scholar]
  95. Trotter JA, Richmond FJR, Purslow PP. 1995. Functional morphology and motor control of series fibred muscles. Exercise and Sports Sciences Reviews 23 JO Holloszy 167–213 Baltimore: Williams-Watkins [Google Scholar]
  96. Velleman SG. 2012. Meat science and muscle biology symposium: extracellular matrix regulation of skeletal muscle formation. J. Anim. Sci. 90:936–41 [Google Scholar]
  97. Velleman SG, Shin J, Li X, Song Y. 2012. Review: the skeletal muscle extracellular matrix: possible roles in the regulation of muscle development and growth. Can. J. Anim. Sci. 92:1–10 [Google Scholar]
  98. Visse R, Nagase H. 2003. Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function and biochemistry. Circ. Res. 92:827–39 [Google Scholar]
  99. Voutila L, Mullen AM, Ruusunen M, Troy D, Puolanne E. 2007. Thermal stability of connective tissue from porcine muscles. Meat Sci. 76:474–80 [Google Scholar]
  100. Wang J-P, Yeh C-M, Tsai Y-C. 2006. Improved subtilisin YaB production in Bacillus subtilis using engineered synthetic expression control sequences. J. Agric. Food Chem. 54:9405–10 [Google Scholar]
  101. Xia JJ, Berg EP, Lee JW, Yao G. 2007. Characterizing beef muscles with optical scattering and absorption coefficients in VIS-NIR region. Meat Sci. 75:78–83 [Google Scholar]
  102. Ye S, Watts GF, Mandalia S, Humphries SE, Henney AM. 1995. Preliminary report: genetic variation in the human stromelysin promoter is associated with progression of coronary atherosclerosis. Br. Heart J. 73:209–15 [Google Scholar]
  103. Yeh C-M, Yang M-C, Tsai Y-C. 2002. Application potency of engineered G159 mutants on P1 substrate pocket of subtilisin YaB as improved meat tenderizers. J. Agric. Food Chem. 50:6199–204 [Google Scholar]
  104. Young OA, Barker GJ, Frost DA. 1996. Determination of collagen solubility and concentration in meat by near infrared spectroscopy. J. Muscle Foods 7:377–87 [Google Scholar]
  105. Zareian R, Church KP, Saeidi N, Flynn BP, Beale JW, Ruberti JW. 2010. Probing collagen/enzyme mechanochemistry in native tissue with dynamic, enzyme-induced creep. Langmuir 26:9917–26 [Google Scholar]
  106. Zhao G-Y, Zhou M-Y, Zhao H-L, Chen X-L, Xie B-B. et al. 2012. Tenderization effect of cold-adapted collagenolytic protease MCP-01 on beef meat at low temperature and its mechanism. Food Chem. 134:1738–44 [Google Scholar]

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