Skip to main content

Cultured Meat: Meat Industry Hand in Hand with Biomedical Production Methods

Abstract

Meat is the main protein source of the human diet in many cultures. Because of the increasing population growth and welfare, the conventional meat industry cannot follow consumer demands worldwide. Besides, some of the environmental, sustainability-related, and ethical concerns associated with the traditional meat industry have directed scientists to develop new strategies to tackle these negative effects. Culturing meat from cell culture is an emerging bioprocess that will revolutionize the industrial animal agriculture. Many tissue engineering techniques can be utilized for this rising field, although its further development faces important cell culture challenges as well as scale-up limitations. The invention of innovative tools for large-scale in vitro meat production will concurrently advance the technology for biomedical and therapeutic applications. This review highlights vital factors and fundamental cell biology parameters for designing a bioprocess to produce an environmentally friendly meat product that will be accepted by consumers. New applications of current biomedical products and concepts will form the groundwork for future academic research and novel designs enabling large-scale production of cultured meat.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  1. Abmayr SM, Pavlath GK (2012) Myoblast fusion: lessons from flies and mice. Development. 139(4):641–656

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Abraham E, Gupta S, Jung S, McAfee E (2017) Chapter 6 - bioreactor for scale-up: process control. In: Viswanathan S, Hematti P (eds) Mesenchymal stromal cells: translational pathways to clinical adoption. P^pp 139–178. Elsevier

  3. Ahmadi F, Oveisi Z, Samani SM, Amoozgar Z (2015) Chitosan based hydrogels: characteristics and pharmaceutical applications. Res Pharm Sci 10(1):1–16

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Allan SJ, De Bank PA, Ellis MJ (2019) Bioprocess design considerations for cultured meat production with a focus on the expansion bioreactor. Front Sustain Food Syst 3:44

    Google Scholar 

  5. Ansari S, Chen C, Xu X, Annabi N, Zadeh HH, Wu BM, Khademhosseini A, Shi S, Moshaverinia A (2016) Muscle tissue engineering using gingival mesenchymal stem cells encapsulated in alginate hydrogels containing multiple growth factors. Ann Biomed Eng 44(6):1908–1920

    PubMed  PubMed Central  Google Scholar 

  6. Arshad MS, Javed M, Sohaib M, Saeed F, Imran A, Amjad Z (2017) Tissue engineering approaches to develop cultured meat from cells: a mini review. Cogent Food Agric 3(1):1320814

    Google Scholar 

  7. Bach AD, Beier JP, Stern-Staeter J, Horch RE (2004) Skeletal muscle tissue engineering. J Cell Mol Med 8(4):413–422

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Basciano L, Nemos C, Foliguet B, de Isla N, de Carvalho M, Tran N, Dalloul A (2011) Long term culture of mesenchymal stem cells in hypoxia promotes a genetic program maintaining their undifferentiated and multipotent status. BMC Mol Cell Biol 12(1):12

    CAS  Google Scholar 

  9. Bekker GA, Fischer ARH, Tobi H, van Trijp HCM (2017) Explicit and implicit attitude toward an emerging food technology: the case of cultured meat. Appetite. 108:245–254

    PubMed  Google Scholar 

  10. Ben-Arye T, Levenberg S (2019) Tissue engineering for clean meat production. Front Sustain Food Syst 3:46

    Google Scholar 

  11. Benjaminson MA, Gilchriest JA, Lorenz M (2002) In vitro edible muscle protein production system (mpps): stage 1, fish. Acta Astronautica 51(12):879–889

    CAS  PubMed  Google Scholar 

  12. Bhat ZF, Morton JD, Mason SL, Bekhit AEDA, Bhat HF (2019) Technological, regulatory, and ethical aspects of in vitro meat: a future slaughter-free harvest. Compr Rev Food Sci Food Saf 18(4):1192–1208

    CAS  Google Scholar 

  13. Blanton JR Jr, Grant AL, McFarland DC, Robinson JP, Bidwell CA (1999) Isolation of two populations of myoblasts from porcine skeletal muscle. Muscle Nerve 22(1):43–50

    PubMed  Google Scholar 

  14. Bodiou V, Moutsatsou P, Post MJ (2020) Microcarriers for upscaling cultured meat production. Front Nutr 7:10

    PubMed  PubMed Central  Google Scholar 

  15. Boonen KJ, Langelaan ML, Polak RB, van der Schaft DW, Baaijens FP, Post MJ (2010) Effects of a combined mechanical stimulation protocol: value for skeletal muscle tissue engineering. J Biomech 43(8):1514–1521

    PubMed  Google Scholar 

  16. Boonen KJ, Rosaria-Chak KY, Baaijens FP, van der Schaft DW, Post MJ (2009) Essential environmental cues from the satellite cell niche: optimizing proliferation and differentiation. Am J Phys Cell Phys 296(6):C1338–C1345

    CAS  Google Scholar 

  17. Boonen KJ, van der Schaft DW, Baaijens FP, Post MJ (2011) Interaction between electrical stimulation, protein coating and matrix elasticity: a complex effect on muscle fibre maturation. J Tissue Eng Regen Med 5(1):60–68

    CAS  PubMed  Google Scholar 

  18. Breukers RD, Gilmore KJ, Kita M, Wagner KK, Higgins MJ, Moulton SE, Clark GM, Officer DL, Kapsa RM, Wallace GG (2010) Creating conductive structures for cell growth: growth and alignment of myogenic cell types on polythiophenes. J Biomed Mater Res A 95(1):256–268

    CAS  PubMed  Google Scholar 

  19. Bryant C, Barnett J (2018) Consumer acceptance of cultured meat: a systematic review. Meat Sci 143:8–17

    PubMed  Google Scholar 

  20. Burton NM, Vierck J, Krabbenhoft L, Bryne K, Dodson MV (2000) Methods for animal satellite cell culture under a variety of conditions. Methods Cell Sci 22(1):51–61

    CAS  PubMed  Google Scholar 

  21. Casteilla L, Cousin B, Carmona M (2007) PPARs and adipose cell plasticity. PPAR Res 2007:68202

    PubMed  PubMed Central  Google Scholar 

  22. Catts O, Zurr I (2002) Growing semi-living sculptures: the tissue culture and art project. Leonardo. 35(4):365–370

    Google Scholar 

  23. Cerino G, Gaudiello E, Grussenmeyer T, Melly L, Massai D, Banfi A, Martin I, Eckstein F, Grapow M, Marsano A (2016) Three dimensional multi-cellular muscle-like tissue engineering in perfusion-based bioreactors. Biotechnol Bioeng 113(1):226–236

    CAS  PubMed  Google Scholar 

  24. Chen S, Nakamoto T, Kawazoe N, Chen G (2015) Engineering multi-layered skeletal muscle tissue by using 3D microgrooved collagen scaffolds. Biomaterials. 73:23–31

    CAS  PubMed  Google Scholar 

  25. Cheng CS, El-Abd Y, Bui K, Hyun YE, Hughes RH, Kraus WE, Truskey GA (2014) Conditions that promote primary human skeletal myoblast culture and muscle differentiation in vitro. Am J Phys Cell Phys 306(4):C385–C395

    CAS  Google Scholar 

  26. Claeys E, De Smet S, Balcaen A, Raes K, Demeyer D (2004) Quantification of fresh meat peptides by SDS–PAGE in relation to ageing time and taste intensity. Meat Sci 67(2):281–288

    CAS  PubMed  Google Scholar 

  27. Collinsworth AM, Zhang S, Kraus WE, Truskey GA (2002) Apparent elastic modulus and hysteresis of skeletal muscle cells throughout differentiation. Am J Phys Cell Phys 283(4):C1219–C1227

    CAS  Google Scholar 

  28. Daskalova A (2019) Farmed fish welfare: stress, post-mortem muscle metabolism, and stress-related meat quality changes. Int Aquat Res 11(2):113–124

    Google Scholar 

  29. Datar I, Betti M (2010) Possibilities for an in vitro meat production system. Innovative Food Sci Emerg Technol 11(1):13–22

    CAS  Google Scholar 

  30. Dennis RG, Smith B, Philp A, Donnelly K, Baar K (2009) Bioreactors for guiding muscle tissue growth and development. Adv Biochem Eng Biotechnol 112:39–79

    CAS  PubMed  Google Scholar 

  31. Dodson MV, Martin EL, Brannon MA, Mathison BA, McFarland DC (1987) Optimization of bovine satellite cell-derived myotube formation in vitro. Tissue Cell 19(2):159–166

    CAS  PubMed  Google Scholar 

  32. Dodson MV, McFarland DC, Grant AL, Doumit ME, Velleman SG (1996) Extrinsic regulation of domestic animal-derived satellite cells. Domest Anim Endocrinol 13(2):107–126

    CAS  PubMed  Google Scholar 

  33. Dodson MV, McFarland DC, Martin EL, Brannon MA (1986) Isolation of satellite cells from ovine skeletal muscles. J Tissue Cult Methods 10(4):233–237

    Google Scholar 

  34. Dokmanovic M, Baltic ZM, Markovic R, Boskovic M, Loncina J, Glamoclija N, Dordevic M (2014) Relationships among pre-slaughter stress, rigor mortis, blood lactate, and meat and carcass quality in pigs. Acta Veterinaria 64(1):124–137

    Google Scholar 

  35. Dusterhoft S, Pette D (1990) Effects of electrically induced contractile activity on cultured embryonic chick breast muscle cells. Differentiation. 44(3):178–184

    CAS  PubMed  Google Scholar 

  36. Edelman PD, McFarland DC, Mironov VA, Matheny JG (2005) Commentary: in vitro-cultured meat production. J Tissue Eng 11(5–6):659–662

    CAS  Google Scholar 

  37. Elkasrawy MN, Hamrick MW (2010) Myostatin (GDF-8) as a key factor linking muscle mass and skeletal form. J Musculoskelet Neuronal Interact 10(1):56–63

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Engler AJ, Griffin MA, Sen S, Bonnemann CG, Sweeney HL, Discher DE (2004) Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments. J Cell Biol 166(6):877–887

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Feiner G (2006) Meat products handbook: practical science and technology. Elsevier

  40. Fraeye I, Kratka M, Vandenburgh H, Thorrez L (2020) Sensorial and nutritional aspects of cultured meat in comparison to traditional meat: much to be inferred. Front Nutr 7:35

    PubMed  PubMed Central  Google Scholar 

  41. Fujita H, Nedachi T, Kanzaki M (2007) Accelerated de novo sarcomere assembly by electric pulse stimulation in C2C12 myotubes. Exp Cell Res 313(9):1853–1865

    CAS  PubMed  Google Scholar 

  42. Fuoco C, Petrilli LL, Cannata S, Gargioli C (2016) Matrix scaffolding for stem cell guidance toward skeletal muscle tissue engineering. J Orthop Surg Res 11(1):86

    PubMed  PubMed Central  Google Scholar 

  43. Gaydhane MK, Mahanta U, Sharma CS, Khandelwal M, Ramakrishna S (2018) Cultured meat: state of the art and future. Biomanufacturing Rev 3(1):1

    Google Scholar 

  44. Gholobova D, Gerard M, Decroix L, Desender L, Callewaert N, Annaert P, Thorrez L (2018) Human tissue-engineered skeletal muscle: a novel 3D in vitro model for drug disposition and toxicity after intramuscular injection. Sci Rep 8(1):12206

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Gielen FL, Wallinga-de Jonge W, Boon KL (1984) Electrical conductivity of skeletal muscle tissue: experimental results from different muscles in vivo. Med Biol Eng Comput 22(6):569–577

    CAS  PubMed  Google Scholar 

  46. Gilbert PM, Havenstrite KL, Magnusson KE, Sacco A, Leonardi NA, Kraft P, Nguyen NK, Thrun S, Lutolf MP, Blau HM (2010) Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science. 329(5995):1078–1081

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Goldspink DF, Cox VM, Smith SK, Eaves LA, Osbaldeston NJ, Lee DM, Mantle D (1995) Muscle growth in response to mechanical stimuli. Am J Phys 268(2 Pt 1):E288–E297

    CAS  Google Scholar 

  48. Goto S, Miyazaki K, Funabiki T, Yasumitsu H (1999) Serum-free culture conditions for analysis of secretory proteinases during myogenic differentiation of mouse C2C12 myoblasts. Anal Biochem 272(2):135–142

    CAS  PubMed  Google Scholar 

  49. Guthridge M, Wilson M, Cowling J, Bertolini J, Hearn MT (1992) The role of basic fibroblast growth factor in skeletal muscle regeneration. Growth Factors 6(1):53–63

    CAS  PubMed  Google Scholar 

  50. Heher P, Maleiner B, Pruller J, Teuschl AH, Kollmitzer J, Monforte X, Wolbank S, Redl H, Runzler D, Fuchs C (2015) A novel bioreactor for the generation of highly aligned 3D skeletal muscle-like constructs through orientation of fibrin via application of static strain. Acta Biomater 24:251–265

    CAS  PubMed  Google Scholar 

  51. Helbo S, Weber RE, Fago A (2013) Expression patterns and adaptive functional diversity of vertebrate myoglobins. Biochim Biophys Acta 1834(9):1832–1839

    CAS  PubMed  Google Scholar 

  52. Hervy M, Weber JL, Pecheul M, Dolley-Sonneville P, Henry D, Zhou Y, Melkoumian Z (2014) Long term expansion of bone marrow-derived hMSCs on novel synthetic microcarriers in xeno-free, defined conditions. PLoS One 9(3):e92120

    PubMed  PubMed Central  Google Scholar 

  53. Hoang YT, Vu AT (2016) Sodium benzoate and potassium sorbate in processed meat products collected in Ho Chi Minh City, Vietnam. Int J Adv Sci Eng Inf Technol 6(4):477–482

    Google Scholar 

  54. Hocquette J-F (2016) Is in vitro meat the solution for the future? Meat Sci 120:167–176

    PubMed  Google Scholar 

  55. Ismaeel A, Kim JS, Kirk JS, Smith RS, Bohannon WT, Koutakis P (2019) Role of transforming growth factor-beta in skeletal muscle fibrosis: a review. Int J Mol Sci 20(10):2446

    PubMed Central  Google Scholar 

  56. Gordon Betts JKAY, James A. Wise, Eddie Johnson, Brandon Poe, Dean H. Kruse, Oksana Korol, Jody E. Johnson, Mark Womble, Peter DeSaix (2013) Chapter 10 - muscle tissue. In: Anatomy and Physiology p^pp 10–10.10. OpenStax

  57. Kadim IT, Mahgoub O, Baqir S, Faye B, Purchas R (2015) Cultured meat from muscle stem cells: a review of challenges and prospects. J Integr Agric 14(2):222–233

    CAS  Google Scholar 

  58. Kaji H, Ishibashi T, Nagamine K, Kanzaki M, Nishizawa M (2010) Electrically induced contraction of C2C12 myotubes cultured on a porous membrane-based substrate with muscle tissue-like stiffness. Biomaterials. 31(27):6981–6986

    CAS  PubMed  Google Scholar 

  59. Kamanga-Sollo E, Pampusch MS, White ME, Hathaway M, Dayton WR (2005) Insulin-like growth factor binding protein (IGFBP)-3 and IGFBP-5 mediate TGF-β-and myostatin-induced suppression of proliferation in porcine embryonic myogenic cell cultures. Exp Cell Res 311(1):167–176

    CAS  PubMed  Google Scholar 

  60. Kanatous SB, Mammen PP (2010) Regulation of myoglobin expression. J Exp Biol 213(Pt 16):2741–2747

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Khodabukus A, Baar K (2014) The effect of serum origin on tissue engineered skeletal muscle function. J Cell Biochem 115(12):2198–2207

    CAS  PubMed  Google Scholar 

  62. Khodabukus A, Baar K (2015) Streptomycin decreases the functional shift to a slow phenotype induced by electrical stimulation in engineered muscle. Tissue Eng A 21(5–6):1003–1012

    CAS  Google Scholar 

  63. Khodabukus A, Baar K (2016) Factors that affect tissue-engineered skeletal muscle function and physiology. Cells Tissues Organs 202(3–4):159–168

    PubMed  Google Scholar 

  64. Kim J, Lee J (2017) Role of transforming growth factor-beta in muscle damage and regeneration: focused on eccentric muscle contraction. J Exerc Rehabil 13(6):621–626

    PubMed  PubMed Central  Google Scholar 

  65. Kim M, Choi YS, Yang SH, Hong HN, Cho SW, Cha SM, Pak JH, Kim CW, Kwon SW, Park CJ (2006) Muscle regeneration by adipose tissue-derived adult stem cells attached to injectable PLGA spheres. Biochem Biophys Res Commun 348(2):386–392

    CAS  PubMed  Google Scholar 

  66. Kong D, Gentz R, Zhang J (1998) Long-term stable production of monocyte-colony inhibition factor (M-CIF) from CHO microcarrier perfusion cultures. Cytotechnology. 26(2):131–138

    CAS  PubMed  PubMed Central  Google Scholar 

  67. Kook SH, Choi KC, Son YO, Lee KY, Hwang IH, Lee HJ, Chang JS, Choi IH, Lee JC (2006) Satellite cells isolated from adult Hanwoo muscle can proliferate and differentiate into myoblasts and adipose-like cells. Mol Cell 22(2):239–245

    CAS  Google Scholar 

  68. Kues WA, Petersen B, Mysegades W, Carnwath JW, Niemann H (2005) Isolation of murine and porcine fetal stem cells from somatic tissue. Biol Reprod 72(4):1020–1028

    CAS  PubMed  Google Scholar 

  69. Langelaan ML, Boonen KJ, Rosaria-Chak KY, van der Schaft DW, Post MJ, Baaijens FP (2011) Advanced maturation by electrical stimulation: differences in response between C2C12 and primary muscle progenitor cells. J Tissue Eng Regen Med 5(7):529–539

    PubMed  Google Scholar 

  70. Langelaan MLP, Boonen KJM, Polak RB, Baaijens FPT, Post MJ, van der Schaft DWJ (2010) Meet the new meat: tissue engineered skeletal muscle. Trends Food Sci Technol 21(2):59–66

    CAS  Google Scholar 

  71. Lassar AB, Skapek SX, Novitch B (1994) Regulatory mechanisms that coordinate skeletal muscle differentiation and cell cycle withdrawal. Curr Opin Cell Biol 6(6):788–794

    CAS  PubMed  Google Scholar 

  72. Lawson MA, Purslow PP (2000) Differentiation of myoblasts in serum-free media: effects of modified media are cell line-specific. Cells Tissues Organs 167(2–3):130–137

    CAS  PubMed  Google Scholar 

  73. Lepper C, Fan CM (2010) Inducible lineage tracing of Pax7-descendant cells reveals embryonic origin of adult satellite cells. Genesis. 48(7):424–436

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Levenberg S, Rouwkema J, Macdonald M, Garfein ES, Kohane DS, Darland DC, Marini R, van Blitterswijk CA, Mulligan RC, D'Amore PA, Langer R (2005) Engineering vascularized skeletal muscle tissue. Nat Biotechnol 23(7):879–884

    CAS  PubMed  Google Scholar 

  75. Lian T, Wang L, Liu Y (2013) A new insight into the role of calpains in post-mortem meat tenderization in domestic animals: a review. Asian Australas J Anim Sci 26(3):443–454

    CAS  PubMed  PubMed Central  Google Scholar 

  76. Liao IC, Liu JB, Bursac N, Leong KW (2008) Effect of electromechanical stimulation on the maturation of myotubes on aligned electrospun fibers. Cell Mol Bioeng 1(2–3):133–145

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Listrat A, Lebret B, Louveau I, Astruc T, Bonnet M, Lefaucheur L, Picard B, Bugeon J (2016) How muscle structure and composition influence meat and flesh quality. Sci World J 2016:3182746

    Google Scholar 

  78. Lonergan EH, Zhang W, Lonergan SM (2010) Biochemistry of postmortem muscle—lessons on mechanisms of meat tenderization. Meat Sci 86(1):184–195

    PubMed  Google Scholar 

  79. Lu D, Luo C, Zhang C, Li Z, Long M (2014) Differential regulation of morphology and stemness of mouse embryonic stem cells by substrate stiffness and topography. Biomaterials. 35(13):3945–3955

    CAS  PubMed  Google Scholar 

  80. Ma YN, Wang B, Wang ZX, Gomez NA, Zhu MJ, Du M (2018) Three-dimensional spheroid culture of adipose stromal vascular cells for studying adipogenesis in beef cattle. Animal 12(10):1–7

    Google Scholar 

  81. Maley MA, Davies MJ, Grounds MD (1995) Extracellular matrix, growth factors, genetics: their influence on cell proliferation and myotube formation in primary cultures of adult mouse skeletal muscle. Exp Cell Res 219(1):169–179

    CAS  PubMed  Google Scholar 

  82. Martin I, Wendt D, Heberer M (2004) The role of bioreactors in tissue engineering. Trends Biotechnol 22(2):80–86

    CAS  PubMed  Google Scholar 

  83. Mattick CS, Landis AE, Allenby BR (2015) A case for systemic environmental analysis of cultured meat. J Integr Agric 14(2):249–254

    Google Scholar 

  84. McFarland DC, Pesall JE, Norberg JM, Dvoracek MA (1991) Proliferation of the Turkey myogenic satellite cell in a serum-free medium. Comp Biochem Physiol A Physiol 99(1–2):163–167

    Google Scholar 

  85. Mehdizadeh H, Lauri D, Karry KM, Moshgbar M, Procopio-Melino R, Drapeau D (2015) Generic Raman-based calibration models enabling real-time monitoring of cell culture bioreactors. Biotechnol Prog 31(4):1004–1013

    CAS  PubMed  Google Scholar 

  86. Mehta F, Theunissen R, Post MJ (2019) Adipogenesis from bovine precursors. Methods Mol Biol 1889:111–125

    CAS  PubMed  Google Scholar 

  87. Miller RK (2012) Sensory evaluation of beef flavor. In: Nollet LM (ed) handbook of meat, poultry and seafood quality. P^pp 173-191

  88. du Moon G, Christ G, Stitzel JD, Atala A, Yoo JJ (2008) Cyclic mechanical preconditioning improves engineered muscle contraction. Tissue Eng A 14(4):473–482

    CAS  Google Scholar 

  89. Moritz MSM, Verbruggen SEL, Post MJ (2015) Alternatives for large-scale production of cultured beef: a review. J Integr Agric 14(2):208–216

    CAS  Google Scholar 

  90. Mottram DS (1998) Flavour formation in meat and meat products: a review. Food Chem 62(4):415–424

    CAS  Google Scholar 

  91. Mozetic P, Giannitelli SM, Gori M, Trombetta M, Rainer A (2017) Engineering muscle cell alignment through 3D bioprinting. J Biomed Mater Res A 105(9):2582–2588

    CAS  PubMed  Google Scholar 

  92. Murgia M, Nagaraj N, Deshmukh AS, Zeiler M, Cancellara P, Moretti I, Reggiani C, Schiaffino S, Mann M (2015) Single muscle fiber proteomics reveals unexpected mitochondrial specialization. EMBO Rep 16(3):387–395

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Nath SC, Nagamori E, Horie M, Kino-Oka M (2017) Culture medium refinement by dialysis for the expansion of human induced pluripotent stem cells in suspension culture. Bioprocess Biosyst Eng 40(1):123–131

    CAS  PubMed  Google Scholar 

  94. Naumann K, Pette D (1994) Effects of chronic stimulation with different impulse patterns on the expression of myosin isoforms in rat myotube cultures. Differentiation. 55(3):203–211

    CAS  PubMed  Google Scholar 

  95. O'Mara P, Farrell A, Bones J, Twomey K (2018) Staying alive! Sensors used for monitoring cell health in bioreactors. Talanta. 176:130–139

    CAS  PubMed  Google Scholar 

  96. Ohlendieck K (2011) Skeletal muscle proteomics: current approaches, technical challenges and emerging techniques. Skelet Muscle 1(1):6

    PubMed  PubMed Central  Google Scholar 

  97. Ohlson S, Branscomb J, Nilsson K (1994) Bead-to-bead transfer of Chinese-hamster ovary cells using macroporous microcarriers. Cytotechnology. 14(1):67–80

    CAS  PubMed  Google Scholar 

  98. Pette D, Sketelj J, Skorjanc D, Leisner E, Traub I, Bajrovic F (2002) Partial fast-to-slow conversion of regenerating rat fast-twitch muscle by chronic low-frequency stimulation. J Muscle Res Cell Motil 23(3):215–221

    CAS  PubMed  Google Scholar 

  99. Phillips BW, Horne R, Lay TS, Rust WL, Teck TT, Crook JM (2008) Attachment and growth of human embryonic stem cells on microcarriers. J Biotechnol 138(1–2):24–32

    CAS  PubMed  Google Scholar 

  100. Pirosa A, Gottardi R, Alexander PG, Tuan RS (2018) Engineering in-vitro stem cell-based vascularized bone models for drug screening and predictive toxicology. Stem Cell Res Ther 9(1):112

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Post M (2018) Chapter 11 - proteins in cultured beef. In: proteins in food processing. P^pp 289-298. Elsevier

  102. Post M & Hocquette J-F (2017) Chapter 16 - new sources of animal proteins: cultured meat. In: new aspects of meat quality. P^pp 425-441. Elsevier

  103. Post MJ (2012) Cultured meat from stem cells: challenges and prospects. Meat Sci 92(3):297–301

    Google Scholar 

  104. Post MJ (2014a) An alternative animal protein source: cultured beef. Ann N Y Acad Sci 1328:29–33

    CAS  PubMed  Google Scholar 

  105. Post MJ (2014b) Cultured beef: medical technology to produce food. J Sci Food Agric 94(6):1039–1041

    CAS  PubMed  Google Scholar 

  106. Powell CA, Smiley BL, Mills J, Vandenburgh HH (2002) Mechanical stimulation improves tissue-engineered human skeletal muscle. Am J Phys Cell Phys 283(5):C1557–C1565

    CAS  Google Scholar 

  107. Powell RL, Dodson MV, Cloud JG (1989) Cultivation and differentiation of satellite cells from skeletal muscle of the rainbow trout Salmo gairdneri. J Exp Zool 250(3):333–338

    Google Scholar 

  108. Purslow PP, Oiseth S, Hughes J, Warner RD (2016) The structural basis of cooking loss in beef: variations with temperature and ageing. Food Res Int 89(Pt 1):739–748

    CAS  PubMed  Google Scholar 

  109. Qazi TH, Mooney DJ, Pumberger M, Geissler S, Duda GN (2015) Biomaterials based strategies for skeletal muscle tissue engineering: existing technologies and future trends. Biomaterials. 53:502–521

    CAS  PubMed  Google Scholar 

  110. Radisic M, Euloth M, Yang L, Langer R, Freed LE, Vunjak-Novakovic G (2003) High-density seeding of myocyte cells for cardiac tissue engineering. Biotechnol Bioeng 82(4):403–414

    CAS  PubMed  Google Scholar 

  111. Radisic M, Marsano A, Maidhof R, Wang Y, Vunjak-Novakovic G (2008) Cardiac tissue engineering using perfusion bioreactor systems. Nature protocoIs 3(4):719–738

    CAS  Google Scholar 

  112. Rafiq QA, Coopman K, Hewitt CJ (2013) Scale-up of human mesenchymal stem cell culture: current technologies and future challenges. Curr Opin Chem Eng 2(1):8–16

    Google Scholar 

  113. Rafiq QA, Ruck S, Hanga MP, Heathman TRJ, Coopman K, Nienow AW, Williams DJ, Hewitt CJ (2018) Qualitative and quantitative demonstration of bead-to-bead transfer with bone marrow-derived human mesenchymal stem cells on microcarriers: utilising the phenomenon to improve culture performance. Biochem Eng J 135:11–21

    CAS  Google Scholar 

  114. Ramboer E, De Craene B, De Kock J, Vanhaecke T, Berx G, Rogiers V, Vinken M (2014) Strategies for immortalization of primary hepatocytes. J Hepatol 61(4):925–943

    CAS  PubMed  Google Scholar 

  115. Ramboer E, Vanhaecke T, Rogiers V, Vinken M (2015) Immortalized human hepatic cell lines for in vitro testing and research purposes. Methods Mol Biol 1250:53–76

    CAS  PubMed  PubMed Central  Google Scholar 

  116. Rangarajan S, Madden L, Bursac N (2014) Use of flow, electrical, and mechanical stimulation to promote engineering of striated muscles. Ann Biomed Eng 42(7):1391–1405

    PubMed  Google Scholar 

  117. Renault V, Thornell LE, Butler-Browne G, Mouly V (2002) Human skeletal muscle satellite cells: aging, oxidative stress and the mitotic clock. Exp Gerontol 37(10–11):1229–1236

    CAS  PubMed  Google Scholar 

  118. Rischer H, Szilvay GR, Oksman-Caldentey KM (2020) Cellular agriculture - industrial biotechnology for food and materials. Curr Opin Biotechnol 61:128–134

    CAS  PubMed  Google Scholar 

  119. Rodriguez BL, Larkin LM (2018) Chapter 12 - functional three-dimensional scaffolds for skeletal muscle tissue engineering. In: Deng Y, Kuiper J (eds) Functional 3D tissue engineering scaffolds. P^pp 279–304. Woodhead Publishing

  120. Rowley J, Abraham E, Campbell A, Brandwein H, Oh S (2012) Meeting lot-size challenges of manufacturing adherent cells for therapy. BioProcess Int 10(3):16–22

    CAS  Google Scholar 

  121. Rubio D, Garcia-Castro J, Martin MC, de la Fuente R, Cigudosa JC, Lloyd AC, Bernad A (2005) Spontaneous human adult stem cell transformation. Cancer Res 65(8):3035–3039

    CAS  PubMed  Google Scholar 

  122. Rubio NR, Fish KD, Trimmer BA, Kaplan DL (2019) In vitro insect muscle for tissue engineering applications. ACS Biomater Sci Eng 5(2):1071–1082

    CAS  Google Scholar 

  123. Sassoli C, Pini A, Chellini F, Mazzanti B, Nistri S, Nosi D, Saccardi R, Quercioli F, Zecchi-Orlandini S, Formigli L (2012) Bone marrow mesenchymal stromal cells stimulate skeletal myoblast proliferation through the paracrine release of VEGF. PLoS One 7(7):e37512

    CAS  PubMed  PubMed Central  Google Scholar 

  124. Serena E, Flaibani M, Carnio S, Boldrin L, Vitiello L, De Coppi P, Elvassore N (2008) Electrophysiologic stimulation improves myogenic potential of muscle precursor cells grown in a 3D collagen scaffold. Neurol Res 30(2):207–214

    CAS  PubMed  Google Scholar 

  125. Shahidi F, Rubin LJ, D'Souza LA, Teranishi R, Buttery RG (1986) Meat flavor volatiles: a review of the composition, techniques of analysis, and sensory evaluation. Crit Rev Food Sci Nutr 24(2):141–243

    CAS  PubMed  Google Scholar 

  126. Shepon A, Eshel G, Noor E, Milo R (2018) The opportunity cost of animal based diets exceeds all food losses. Proc Natl Acad Sci U S A 115(15):3804–3809

    CAS  PubMed  PubMed Central  Google Scholar 

  127. Shit SC, Shah PM (2014) Edible polymers: challenges and opportunities. J Polymers 2014:1–13

    Google Scholar 

  128. Simsa R, Yuen J, Stout A, Rubio N, Fogelstrand P, Kaplan DL (2019) Extracellular heme proteins influence bovine myosatellite cell proliferation and the color of cell-based meat. Foods. 8(10):521

    CAS  PubMed Central  Google Scholar 

  129. Slade P (2018) If you build it, will they eat it? Consumer preferences for plant-based and cultured meat burgers. Appetite. 125:428–437

    PubMed  Google Scholar 

  130. Specht EA, Welch DR, Clayton EMR, Lagally CD (2018) Opportunities for applying biomedical production and manufacturing methods to the development of the clean meat industry. Biochem Eng J 132:161–168

    Google Scholar 

  131. Stephens N, Di Silvio L, Dunsford I, Ellis M, Glencross A, Sexton A (2018) Bringing cultured meat to market: technical, socio-political, and regulatory challenges in cellular agriculture. Trends Food Sci Technol 78:155–166

    CAS  PubMed  PubMed Central  Google Scholar 

  132. Thompson J (2002) Managing meat tenderness. Meat Sci 62(3):295–308

    PubMed  Google Scholar 

  133. Thorrez L, Vandenburgh H (2019) Challenges in the quest for ‘clean meat’. Nat Biotechnol 37(3):215–216

    CAS  PubMed  Google Scholar 

  134. Van Eelen WF (2007) Industrial production of meat using cell culture methods, US7270829B2. USA Patent

  135. Vandenburgh H, Kaufman S (1979) In vitro model for stretch-induced hypertrophy of skeletal muscle. Science. 203(4377):265–268

    CAS  PubMed  Google Scholar 

  136. Vandenburgh HH, Karlisch P (1989) Longitudinal growth of skeletal myotubes in vitro in a new horizontal mechanical cell stimulator. Vitro Cell Dev Biol 25(7):607–616

    CAS  Google Scholar 

  137. Vandenburgh HH, Swasdison S, Karlisch P (1991) Computer-aided mechanogenesis of skeletal muscle organs from single cells in vitro. FASEB J 5(13):2860–2867

    CAS  PubMed  Google Scholar 

  138. Verbruggen S, Luining D, van Essen A, Post MJ (2018) Bovine myoblast cell production in a microcarriers-based system. Cytotechnology. 70(2):503–512

    CAS  PubMed  Google Scholar 

  139. Vettor R, Milan G, Franzin C, Sanna M, De Coppi P, Rizzuto R, Federspil G (2009) The origin of intermuscular adipose tissue and its pathophysiological implications. Am J Physiol Endocrinol Metab 297(5):E987–E998

    CAS  PubMed  Google Scholar 

  140. Wang L, Wu Y, Guo B, Ma PX (2015) Nanofiber yarn/hydrogel core–shell scaffolds mimicking native skeletal muscle tissue for guiding 3D myoblast alignment, elongation, and differentiation. ACS Nano 9(9):9167–9179

    CAS  PubMed  Google Scholar 

  141. Warner RD (2019) Review: analysis of the process and drivers for cellular meat production. Animal 13(12):3041–3058

    CAS  PubMed  Google Scholar 

  142. Wehrle U, Dusterhoft S, Pette D (1994) Effects of chronic electrical stimulation on myosin heavy chain expression in satellite cell cultures derived from rat muscles of different fiber-type composition. Differentiation. 58(1):37–46

    CAS  PubMed  Google Scholar 

  143. Wilschut KJ, Jaksani S, Van Den Dolder J, Haagsman HP, Roelen BA (2008) Isolation and characterization of porcine adult muscle-derived progenitor cells. J Cell Biochem 105(5):1228–1239

    CAS  PubMed  Google Scholar 

  144. Witt R, Weigand A, Boos AM, Cai A, Dippold D, Boccaccini AR, Schubert DW, Hardt M, Lange C, Arkudas A, Horch RE, Beier JP (2017) Mesenchymal stem cells and myoblast differentiation under HGF and IGF-1 stimulation for 3D skeletal muscle tissue engineering. BMC Mol Cell Biol 18(1):15

    CAS  Google Scholar 

  145. Wood JD, Enser M, Fisher AV, Nute GR, Richardson RI, Sheard PR (1999) Manipulating meat quality and composition. Proc Nutr Soc 58(2):363–370

    CAS  PubMed  Google Scholar 

  146. Wood JD, Richardson RI, Nute GR, Fisher AV, Campo MM, Kasapidou E, Sheard PR, Enser M (2004) Effects of fatty acids on meat quality: a review. Meat Sci 66(1):21–32

    CAS  PubMed  Google Scholar 

  147. Yablonka-Reuveni Z, Quinn LS, Nameroff M (1987) Isolation and clonal analysis of satellite cells from chicken pectoralis muscle. Dev BioI 119(1):252–259

    CAS  Google Scholar 

  148. Yamasaki K, Hayashi H, Nishiyama K, Kobayashi H, Uto S, Kondo H, Hashimoto S, Fujisato T (2009) Control of myotube contraction using electrical pulse stimulation for bio-actuator. J Artificial Organs 12(2):131–137

    CAS  Google Scholar 

  149. Zeng L, Rahrmann E, Hu Q, Lund T, Sandquist L, Felten M, O'Brien TD, Zhang J, Verfaillie C (2006) Multipotent adult progenitor cells from swine bone marrow. Stem Cells 24(11):2355–2366

    CAS  PubMed  Google Scholar 

  150. Zhang GQ, Zhao XR, Li XL, Du GC, Zhou JW, Chen J (2020) Challenges and possibilities for bio-manufacturing cultured meat. Trends Food Sci Technol 97:443–450

    CAS  Google Scholar 

  151. Zhao L, Fu HY, Zhou WC, Hu WS (2015) Advances in process monitoring tools for cell culture bioprocesses. Eng Life Sci 15(5):459–468

    CAS  Google Scholar 

  152. Zheng JK, Wang Y, Karandikar A, Wang Q, Gai H, Liu AL, Peng C, Sheng HZ (2006) Skeletal myogenesis by human embryonic stem cells. Cell Res 16(8):713–722

    CAS  PubMed  Google Scholar 

Download references

Funding

The authors acknowledge the financial support from the Slovenian Research Agency for Research (grant numbers P3-0036, J3-1762, and I0-0029); the Ministry for Education, Science and Sport (grant numbers Raziskovalci-2.1-UM-MF-952027 and Raziskovalci-2.1-UM-MF-952028); and through the Young Researcher Programme.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Tanja Zidarič or Uroš Maver.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Zidarič, T., Milojević, M., Vajda, J. et al. Cultured Meat: Meat Industry Hand in Hand with Biomedical Production Methods. Food Eng Rev 12, 498–519 (2020). https://doi.org/10.1007/s12393-020-09253-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12393-020-09253-w

Keywords

  • Cultured meat
  • Skeletal muscle tissue engineering
  • Culturing conditions
  • Growth stimulation
  • Bioreactor
  • Nutritional value