3D Bioprinting in Nipple-Areola Complex Reconstruction

  • Michael P. ChaeEmail author
  • David J. Hunter-Smith
  • Sean V. Murphy
  • Warren Matthew Rozen


Nipple-areola complex (NAC) constitutes an important landmark on a breast, and its loss due to breast cancer treatment can be devastating. In order to achieve cure, an increasing number of women are opting for aggressive mastectomy early, and evidences demonstrate that postmastectomy breast reconstruction significantly improves the patient well-being. Similarly, evidences demonstrate that significant improvement in psychosexual well-being and patient satisfaction can be achieved following a successful NAC reconstruction. Historically various reconstructive options have been reported, such as local flaps, pigmented skin grafts, tattooing, local flaps with autologous, allograft, or alloplastic graft augmentation. However, current reconstructive techniques have inconsistent long-term outcomes regarding maintenance of the neo-nipple projection, color, size, shape, and texture, leading to polarizing patient satisfaction rates. To this effect, novel regenerative medicine technology, three-dimensional (3D) bioprinting, which combines the conventional tissue engineering with 3D printing platform, has been touted as a potential solution. In comparison to other tissue types, reconstructing a 3D solid organ, such as a NAC, undoubtedly commands a higher degree of complexity. Various tissue-engineered NAC reconstructions using synthetic or decellularized allograft scaffolds have been reported. Recently, TeVido BioDevices company has begun developing an entirely 3D-printed NAC graft, but the results are currently limited to preclinical studies.


  1. 1.
    DeSantis C, Ma J, Bryan L, Jemal A. Breast cancer statistics, 2013. CA Cancer J Clin. 2014;64:52–62.PubMedCrossRefGoogle Scholar
  2. 2.
    Shons AR, Mosiello G. Postmastectomy breast reconstruction: current techniques. Cancer Control. 2001;8:419–26.PubMedCrossRefGoogle Scholar
  3. 3.
    Zhong T, Hu J, Bagher S, Vo A, OʼNeill AC, Butler K, Novak CB, Hofer SO, Metcalfe KA. A comparison of psychological response, body image, sexuality, and quality of life between immediate and delayed autologous tissue breast reconstruction: a prospective long-term outcome study. Plast Reconstr Surg. 2016;138:772–80.PubMedCrossRefGoogle Scholar
  4. 4.
    Duraes EF, Durand P, Duraes LC, Orra S, Moreira-Gonzalez A, Sousa JB, Djohan RS, Zins J, Bernard S, Schwarz GS. Comparison of preoperative quality of life in breast reconstruction, breast aesthetic and non-breast plastic surgery patients: a cross-sectional study. J Plast Reconstr Aesthet Surg. 2016;69(11):1478–85.PubMedCrossRefGoogle Scholar
  5. 5.
    Ng SK, Hare RM, Kuang RJ, Smith KM, Brown BJ, Hunter-Smith DJ. Breast reconstruction post mastectomy: patient satisfaction and decision making. Ann Plast Surg. 2016;76(6):640–4.PubMedCrossRefGoogle Scholar
  6. 6.
    Didier F, Arnaboldi P, Gandini S, Maldifassi A, Goldhirsch A, Radice D, Minotti I, Ballardini B, Luini A, Santillo B, Rietjens M, Petit JY. Why do women accept to undergo a nipple sparing mastectomy or to reconstruct the nipple areola complex when nipple sparing mastectomy is not possible? Breast Cancer Res Treat. 2012;132:1177–84.PubMedCrossRefGoogle Scholar
  7. 7.
    Peled AW, Wang F, Foster RD, Alvarado M, Ewing CA, Sbitany H, Esserman LJ. Expanding the indications for total skin-sparing mastectomy: is it safe for patients with locally advanced disease? Ann Surg Oncol. 2016;23:87–91.PubMedCrossRefGoogle Scholar
  8. 8.
    Sisco M, Kyrillos AM, Lapin BR, Wang CE, Yao KA. Trends and variation in the use of nipple-sparing mastectomy for breast cancer in the United States. Breast Cancer Res Treat. 2016;160:111–20.PubMedCrossRefGoogle Scholar
  9. 9.
    Amanti C, Vitale V, Lombardi A, Maggi S, Bersigotti L, Lazzarin G, Nuccetelli E, Romano C, Campanella L, Cristiano L, Bartoloni A, Argento G. Importance of perforating vessels in nipple-sparing mastectomy: an anatomical description. Breast Cancer. 2015;7:179–81.PubMedPubMedCentralGoogle Scholar
  10. 10.
    Shimo A, Tsugawa K, Tsuchiya S, Yoshie R, Tsuchiya K, Uejima T, Kojima Y, Shimo A, Hayami R, Nishikawa T, Yabuki Y, Kawamoto H, Sudo A, Fukuda M, Kanemaki Y, Maeda I. Oncologic outcomes and technical considerations of nipple-sparing mastectomies in breast cancer: experience of 425 cases from a single institution. Breast Cancer. 2015;23(6):851–60.PubMedCrossRefGoogle Scholar
  11. 11.
    De La Cruz L, Moody AM, Tappy EE, Blankenship SA, Hecht EM. Overall survival, disease-free survival, local recurrence, and nipple-areolar recurrence in the setting of nipple-sparing mastectomy: a meta-analysis and systematic review. Ann Surg Oncol. 2015;22:3241–9.CrossRefGoogle Scholar
  12. 12.
    Ou KW, Yu JC, Ho MH, Chiu WK, Ou KL, Chen TM, Chen SG. Oncological safety and outcomes of nipple-sparing mastectomy with breast reconstruction: a single-centered experience in Taiwan. Ann Plast Surg. 2015;74(Suppl 2):S127–31.PubMedCrossRefGoogle Scholar
  13. 13.
    Adam H, Bygdeson M, de Boniface J. The oncological safety of nipple-sparing mastectomy–a Swedish matched cohort study. Eur J Surg Oncol. 2014;40:1209–15.PubMedCrossRefGoogle Scholar
  14. 14.
    van Verschuer VM, Mureau MA, Gopie JP, Vos EL, Verhoef C, Menke-Pluijmers MB, Koppert LB. Patient satisfaction and nipple-areola sensitivity after bilateral prophylactic mastectomy and immediate implant breast reconstruction in a high breast cancer risk population: nipple-sparing mastectomy versus skin-sparing mastectomy. Ann Plast Surg. 2016;77:145–52.Google Scholar
  15. 15.
    Krajewski AC, Boughey JC, Degnim AC, Jakub JW, Jacobson SR, Hoskin TL, Hieken TJ. Expanded indications and improved outcomes for nipple-sparing mastectomy over time. Ann Surg Oncol. 2015;22:3317–23.PubMedCrossRefGoogle Scholar
  16. 16.
    Cho JW, Yoon ES, You HJ, Kim HS, Lee BI, Park SH. Nipple-areola complex necrosis after nipple-sparing mastectomy with immediate autologous breast reconstruction. Arch Plast Surg. 2015;42:601–7.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Bingol UA, Cinar C. Skin necrosis in a patient with factor v leiden mutation following nipple sparing mastectomy. Plast Reconstr Surg Glob Open. 2015;3:e529.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Sisti A, Grimaldi L, Tassinari J, Cuomo R, Fortezza L, Bocchiotti MA, Roviello F, D’Aniello C, Nisi G. Nipple-areola complex reconstruction techniques: a literature review. Eur J Surg Oncol. 2016;42:441–65.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Losken A, Duggal CS, Desai KA, McCullough MC, Gruszynski M, Carlson GW. Time to completion of nipple reconstruction: what factors are involved? Ann Plast Surg. 2013;70:530–2.CrossRefPubMedGoogle Scholar
  20. 20.
    Wellisch DK, Schain WS, Noon RB, Little JW III. The psychological contribution of nipple addition in breast reconstruction. Plast Reconstr Surg. 1987;80:699–704.CrossRefPubMedGoogle Scholar
  21. 21.
    Delay E, Mojallal A, Vasseur C, Delaporte T. Immediate nipple reconstruction during immediate autologous latissimus breast reconstruction. Plast Reconstr Surg. 2006;118:1303–12.CrossRefPubMedGoogle Scholar
  22. 22.
    Chattopadhyay D, Gupta S, Jash PK, Murmu MB, Gupta S. Skin sparing mastectomy with preservation of nipple areola complex and immediate breast reconstruction in patients with breast cancer: a single centre prospective study. Plast Surg Int. 2014;2014:589068.PubMedPubMedCentralGoogle Scholar
  23. 23.
    Momoh AO, Colakoglu S, de Blacam C, Yueh JH, Lin SJ, Tobias AM, Lee BT. The impact of nipple reconstruction on patient satisfaction in breast reconstruction. Ann Plast Surg. 2012;69:389–93.CrossRefPubMedGoogle Scholar
  24. 24.
    Nimboriboonporn A, Chuthapisith S. Nipple-areola complex reconstruction. Gland Surg. 2014;3:35–42.PubMedPubMedCentralGoogle Scholar
  25. 25.
    Jabor MA, Shayani P, Collins DR Jr, Karas T, Cohen BE. Nipple-areola reconstruction: satisfaction and clinical determinants. Plast Reconstr Surg. 2002;110:457–63.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Murphy SV, Atala A. 3D bioprinting of tissues and organs. Nat Biotechnol. 2014;32:773–85.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Atala A, Kasper FK, Mikos AG. Engineering complex tissues. Sci Transl Med. 2012;4:160rv112.CrossRefGoogle Scholar
  28. 28.
    Atala A, Bauer SB, Soker S, Yoo JJ, Retik AB. Tissue-engineered autologous bladders for patients needing cystoplasty. Lancet. 2006;367:1241–6.PubMedCrossRefGoogle Scholar
  29. 29.
    Raya-Rivera A, Esquiliano DR, Yoo JJ, Lopez-Bayghen E, Soker S, Atala A. Tissue-engineered autologous urethras for patients who need reconstruction: an observational study. Lancet. 2011;377:1175–82.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Raya-Rivera AM, Esquiliano D, Fierro-Pastrana R, López-Bayghen E, Valencia P, Ordorica-Flores R, Soker S, Yoo JJ, Atala A. Tissue-engineered autologous vaginal organs in patients: a pilot cohort study. Lancet. 2014;384:329–36.PubMedCrossRefGoogle Scholar
  31. 31.
    Amini AR, Laurencin CT, Nukavarapu SP. Bone tissue engineering: recent advances and challenges. Crit Rev. Biomed Eng. 2012;40:363–408.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Bichara DA, O’Sullivan NA, Pomerantseva I, Zhao X, Sundback CA, Vacanti JP, Randolph MA. The tissue-engineered auricle: past, present, and future. Tissue Eng Part B Rev. 2012;18:51–61.PubMedCrossRefGoogle Scholar
  33. 33.
    Ostrovidov S, Hosseini V, Ahadian S, Fujie T, Parthiban SP, Ramalingam M, Bae H, Kaji H, Khademhosseini A. Skeletal muscle tissue engineering: methods to form skeletal myotubes and their applications. Tissue Eng Part B Rev. 2014;20:403–36.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Lee YB, Polio S, Lee W, Dai G, Menon L, Carroll RS, Yoo SS. Bio-printing of collagen and VEGF-releasing fibrin gel scaffolds for neural stem cell culture. Exp Neurol. 2010;223:645–52.PubMedCrossRefGoogle Scholar
  35. 35.
    Jain RK, Au P, Tam J, Duda DG, Fukumura D. Engineering vascularized tissue. Nat Biotechnol. 2005;23:821–3.PubMedCrossRefGoogle Scholar
  36. 36.
    Mikos AG, Herring SW, Ochareon P, Elisseeff J, Lu HH, Kandel R, Schoen FJ, Toner M, Mooney D, Atala A, Van Dyke ME, Kaplan D, Vunjak-Novakovic G. Engineering complex tissues. Tissue Eng. 2006;12:3307–39.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Lee W, Debasitis JC, Lee VK, Lee JH, Fischer K, Edminster K, Park JK, Yoo SS. Multi-layered culture of human skin fibroblasts and keratinocytes through three-dimensional freeform fabrication. Biomaterials. 2009;30:1587–95.PubMedCrossRefGoogle Scholar
  38. 38.
    Boland T, Xu T, Damon B, Cui X. Application of inkjet printing to tissue engineering. Biotechnol J. 2006;1:910–7.PubMedCrossRefGoogle Scholar
  39. 39.
    Dahms SE, Piechota HJ, Dahiya R, Lue TF, Tanagho EA. Composition and biomechanical properties of the bladder acellular matrix graft: comparative analysis in rat, pig and human. Br J Urol. 1998;82:411–9.PubMedCrossRefGoogle Scholar
  40. 40.
    Chen F, Yoo JJ, Atala A. Acellular collagen matrix as a possible “off the shelf” biomaterial for urethral repair. Urology. 1999;54:407–10.PubMedCrossRefGoogle Scholar
  41. 41.
    Probst M, Dahiya R, Carrier S, Tanagho EA. Reproduction of functional smooth muscle tissue and partial bladder replacement. Br J Urol. 1997;79:505–15.PubMedCrossRefGoogle Scholar
  42. 42.
    Brown BN, Valentin JE, Stewart-Akers AM, McCabe GP, Badylak SF. Macrophage phenotype and remodeling outcomes in response to biologic scaffolds with and without a cellular component. Biomaterials. 2009;30:1482–91.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Moroni L, de Wijn JR, van Blitterswijk CA. 3D fiber-deposited scaffolds for tissue engineering: influence of pores geometry and architecture on dynamic mechanical properties. Biomaterials. 2006;27:974–85.PubMedCrossRefGoogle Scholar
  44. 44.
    Kretlow JD, Mikos AG. Founder’s award to Antonios G. Mikos, ph.D., 2011 society for biomaterials annual meeting and exposition, Orlando, Florida, April 13–16, 2011: bones to biomaterials and back again–20 years of taking cues from nature to engineer synthetic polymer scaffolds. J Biomed Mater Res A. 2011;98:323–31.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Tan JY, Chua CK, Leong KF. Fabrication of channeled scaffolds with ordered array of micro-pores through microsphere leaching and indirect rapid prototyping technique. Biomed Microdevices. 2013;15:83–96.PubMedCrossRefGoogle Scholar
  46. 46.
    Hutmacher DW. Scaffolds in tissue engineering bone and cartilage. Biomaterials. 2000;21:2529–43.PubMedCrossRefGoogle Scholar
  47. 47.
    Hollister SJ. Porous scaffold design for tissue engineering. Nat Mater. 2005;4:518–24.PubMedCrossRefGoogle Scholar
  48. 48.
    Derby B. Printing and prototyping of tissues and scaffolds. Science. 2012;338:921–6.PubMedCrossRefGoogle Scholar
  49. 49.
    Cabodi M, Choi NW, Gleghorn JP, Lee CS, Bonassar LJ, Stroock AD. A microfluidic biomaterial. J Am Chem Soc. 2005;127:13788–9.PubMedCrossRefGoogle Scholar
  50. 50.
    Ling Y, Rubin J, Deng Y, Huang C, Demirci U, Karp JM, Khademhosseini A. A cell-laden microfluidic hydrogel. Lab Chip. 2007;7:756–62.PubMedCrossRefGoogle Scholar
  51. 51.
    Stachowiak AN, Bershteyn A, Tzatzalos E, Irvine DJ. Bioactive hydrogels with an ordered cellular structure combine interconnected macroporosity and robust mechanical properties. Adv Mater. 2005;17:399–403.CrossRefGoogle Scholar
  52. 52.
    Mironov V, Visconti RP, Kasyanov V, Forgacs G, Drake CJ, Markwald RR. Organ printing: tissue spheroids as building blocks. Biomaterials. 2009;30:2164–74.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Jones N. Science in three dimensions: the print revolution. Nature. 2012;487:22–3.PubMedCrossRefGoogle Scholar
  54. 54.
    Ferris CJ, Gilmore KG, Wallace GG, In het Panhuis M. Biofabrication: an overview of the approaches used for printing of living cells. Appl Microbiol Biotechnol. 2013;97:4243–58.PubMedCrossRefGoogle Scholar
  55. 55.
    Xu T, Zhao W, Zhu JM, Albanna MZ, Yoo JJ, Atala A. Complex heterogeneous tissue constructs containing multiple cell types prepared by inkjet printing technology. Biomaterials. 2013;34:130–9.PubMedCrossRefGoogle Scholar
  56. 56.
    Durmus NG, Tasoglu S, Demirci U. Bioprinting: functional droplet networks. Nat Mater. 2013;12:478–9.PubMedCrossRefGoogle Scholar
  57. 57.
    Chae MP, Rozen WM, McMenamin PG, Findlay MW, Spychal RT, Hunter-Smith DJ. Emerging applications of bedside 3D printing in plastic surgery. Front Surg. 2015;2:25.PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Chae MP, Hunter-Smith DJ, Rozen WM. Image-guided 3D-printing and haptic modeling in plastic surgery. In: Saba L, Rozen WM, Alonso-Burgos A, Ribuffo D, editors. Imaging in plastic surgery. London, UK: CRC Taylor and Francis Press; 2014.Google Scholar
  59. 59.
    Gerstle TL, Ibrahim AM, Kim PS, Lee BT, Lin SJ. A plastic surgery application in evolution: three-dimensional printing. Plast Reconstr Surg. 2014;133:446–51.PubMedCrossRefGoogle Scholar
  60. 60.
    Goiato MC, Santos MR, Pesqueira AA, Moreno A, dos Santos DM, Haddad MF. Prototyping for surgical and prosthetic treatment. J Craniofac Surg. 2011;22:914–7.PubMedCrossRefGoogle Scholar
  61. 61.
    Levy GN, Schindel R, Kruth JP. Rapid manufacturing and rapid tooling with layer manufacturing (LM) technologies, state of the art and future perspectives. CIRP Ann-Manuf Techn. 2003;52:589–609.CrossRefGoogle Scholar
  62. 62.
    Sealy W. Additive manufacturing as a disruptive technology: how to avoid the pitfall. Am J Eng Technol Res. 2011;11:86–93.Google Scholar
  63. 63.
    Hoy MB. 3D printing: making things at the library. Med Ref Serv Q. 2013;32:93–9.CrossRefGoogle Scholar
  64. 64.
    Klein GT, Lu Y, Wang MY. 3D printing and neurosurgery--ready for prime time? World Neurosurg. 2013;80:233–5.PubMedCrossRefGoogle Scholar
  65. 65.
    Crump SS. Apparatus and method for creating three-dimensional objects. 1992; US Patent No. 5,121,329: June 9.Google Scholar
  66. 66.
    Peltola SM, Melchels FP, Grijpma DW, Kellomaki M. A review of rapid prototyping techniques for tissue engineering purposes. Ann Med. 2008;40:268–80.PubMedCrossRefGoogle Scholar
  67. 67.
    Fong EL, Watson BM, Kasper FK, Mikos AG. Building bridges: leveraging interdisciplinary collaborations in the development of biomaterials to meet clinical needs. Adv Mater. 2012;24:4995–5013.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Lu L, Zhu X, Valenzuela RG, Currier BL, Yaszemski MJ. Biodegradable polymer scaffolds for cartilage tissue engineering. Clin Orthop Relat Res. 2001;(391 Suppl):S251–70.CrossRefGoogle Scholar
  69. 69.
    Butler DL, Goldstein SA, Guldberg RE, Guo XE, Kamm R, Laurencin CT, McIntire LV, Mow VC, Nerem RM, Sah RL, Soslowsky LJ, Spilker RL, Tranquillo RT. The impact of biomechanics in tissue engineering and regenerative medicine. Tissue Eng Part B Rev. 2009;15:477–84.PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Silva NA, Cooke MJ, Tam RY, Sousa N, Salgado AJ, Reis RL, Shoichet MS. The effects of peptide modified gellan gum and olfactory ensheathing glia cells on neural stem/progenitor cell fate. Biomaterials. 2012;33:6345–54.PubMedCrossRefGoogle Scholar
  71. 71.
    Vidal G, Blanchi T, Mieszawska AJ, Calabrese R, Rossi C, Vigneron P, Duval JL, Kaplan DL, Egles C. Enhanced cellular adhesion on titanium by silk functionalized with titanium binding and RGD peptides. Acta Biomater. 2013;9:4935–43.PubMedCrossRefGoogle Scholar
  72. 72.
    Engelhardt EM, Micol LA, Houis S, Wurm FM, Hilborn J, Hubbell JA, Frey P. A collagen-poly(lactic acid-co-varepsilon-caprolactone) hybrid scaffold for bladder tissue regeneration. Biomaterials. 2011;32:3969–76.PubMedCrossRefGoogle Scholar
  73. 73.
    Phipps MC, Xu Y, Bellis SL. Delivery of platelet-derived growth factor as a chemotactic factor for mesenchymal stem cells by bone-mimetic electrospun scaffolds. PLoS One. 2012;7:e40831.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Serrano MC, Pagan R, Vallet-Regi M, Peña J, Rámila A, Izquierdo I, Portolés MT. In vitro biocompatibility assessment of poly(epsilon-caprolactone) films using L929 mouse fibroblasts. Biomaterials. 2004;25:5603–11.PubMedCrossRefGoogle Scholar
  75. 75.
    Sun H, Mei L, Song C, Cui X, Wang P. The in vivo degradation, absorption and excretion of PCL-based implant. Biomaterials. 2006;27:1735–40.PubMedCrossRefGoogle Scholar
  76. 76.
    Chang CC, Boland ED, Williams SK, Hoying JB. Direct-write bioprinting three-dimensional biohybrid systems for future regenerative therapies. J Biomed Mater Res B Appl Biomater. 2011;98:160–70.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Lippens E, Swennen I, Girones J, Declercq H, Vertenten G, Vlaminck L, Gasthuys F, Schacht E, Cornelissen R. Cell survival and proliferation after encapsulation in a chemically modified Pluronic(R) F127 hydrogel. J Biomater Appl. 2013;27:828–39.PubMedCrossRefGoogle Scholar
  78. 78.
    Schuurman W, Khristov V, Pot MW, van Weere PR, Dhert WJ, Malda J. Bioprinting of hybrid tissue constructs with tailorable mechanical properties. Biofabrication. 2011;3:021001.PubMedCrossRefGoogle Scholar
  79. 79.
    Shim JH, Lee JS, Kim JY, Cho DW. Bioprinting of a mechanically enhanced three-dimensional dual cell-laden construct for osteochondral tissue engineering using a multi-head tissue/organ building system. J Micromech Microeng. 2012;22:085014.CrossRefGoogle Scholar
  80. 80.
    Fedorovich NE, De Wijn JR, Verbout AJ, Alblas J, Dhert WJ. Three-dimensional fiber deposition of cell-laden, viable, patterned constructs for bone tissue printing. Tissue Eng Part A. 2008;14:127–33.PubMedCrossRefGoogle Scholar
  81. 81.
    Jakab K, Neagu A, Mironov V, Markwald RR, Forgacs G. Engineering biological structures of prescribed shape using self-assembling multicellular systems. Proc Natl Acad Sci U S A. 2004;101:2864–9.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Landers R, Hubner U, Schmelzeisen R, Mulhaupt R. Rapid prototyping of scaffolds derived from thermoreversible hydrogels and tailored for applications in tissue engineering. Biomaterials. 2002;23:4437–47.PubMedCrossRefGoogle Scholar
  83. 83.
    Joddar B, Garcia E, Casas A, Stewart CM. Development of functionalized multi-walled carbon-nanotube-based alginate hydrogels for enabling biomimetic technologies. Sci Rep. 2016;6:32456.PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Kang HW, Lee SJ, Ko IK, Kengla C, Yoo JJ, Atala A. A 3D bioprinting system to produce human-scale tissue constructs with structural integrity. Nat Biotechnol. 2016;34:312–9.PubMedCrossRefGoogle Scholar
  85. 85.
    Brivanlou AH, Gage FH, Jaenisch R, Jessell T, Melton D, Rossant J. Stem cells. Setting standards for human embryonic stem cells. Science. 2003;300:913–6.PubMedCrossRefGoogle Scholar
  86. 86.
    Condic ML, Rao M. Regulatory issues for personalized pluripotent cells. Stem Cells. 2008;26:2753–8.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Hochedlinger K, Jaenisch R. Nuclear transplantation, embryonic stem cells, and the potential for cell therapy. N Engl J Med. 2003;349:275–86.PubMedCrossRefGoogle Scholar
  88. 88.
    Bae H, Puranik AS, Gauvin R, Edalat F, Carrillo-Conde B, Peppas NA, Khademhosseini A. Building vascular networks. Sci Transl Med. 2012;4:160ps123.CrossRefGoogle Scholar
  89. 89.
    Lovett M, Lee K, Edwards A, Kaplan DL. Vascularization strategies for tissue engineering. Tissue Eng Part B Rev. 2009;15:353–70.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Cilento BG, Freeman MR, Schneck FX, Retik AB, Atala A. Phenotypic and cytogenetic characterization of human bladder urothelia expanded in vitro. J Urol. 1994;152:665–70.PubMedCrossRefGoogle Scholar
  91. 91.
    Zhang YY, Ludwikowski B, Hurst R, Frey P. Expansion and long-term culture of differentiated normal rat urothelial cells in vitro. In Vitro Cell Dev Biol Anim. 2001;37:419–29.PubMedCrossRefGoogle Scholar
  92. 92.
    Caplan AI, Correa D. The MSC: an injury drugstore. Cell Stem Cell. 2011;9:11–5.PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Lam MT, Longaker MT. Comparison of several attachment methods for human iPS, embryonic and adipose-derived stem cells for tissue engineering. J Tissue Eng Regen Med. 2012;6(Suppl 3):s80–6.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Klebe RJ. Cytoscribing: a method for micropositioning cells and the construction of two- and three-dimensional synthetic tissues. Exp Cell Res. 1988;179:362–73.PubMedCrossRefGoogle Scholar
  95. 95.
    Xu T, Jin J, Gregory C, Hickman JJ, Boland T. Inkjet printing of viable mammalian cells. Biomaterials. 2005;26:93–9.PubMedCrossRefGoogle Scholar
  96. 96.
    Cui X, Boland T, D'Lima DD, Lotz MK. Thermal inkjet printing in tissue engineering and regenerative medicine. Recent Pat Drug Deliv Form. 2012;6:149–55.CrossRefGoogle Scholar
  97. 97.
    Cohen DL, Malone E, Lipson H, Bonassar LJ. Direct freeform fabrication of seeded hydrogels in arbitrary geometries. Tissue Eng. 2006;12:1325–35.PubMedCrossRefGoogle Scholar
  98. 98.
    Iwami K, Noda T, Ishida K, Morishima K, Nakamura M, Umeda N. Bio rapid prototyping by extruding/aspirating/refilling thermoreversible hydrogel. Biofabrication. 2010;2:014108.PubMedCrossRefGoogle Scholar
  99. 99.
    Shor L, Guceri S, Chang R, Gordon J, Kang Q, Hartsock L, An Y, Sun W. Precision extruding deposition (PED) fabrication of polycaprolactone (PCL) scaffolds for bone tissue engineering. Biofabrication. 2009;1:015003.PubMedCrossRefGoogle Scholar
  100. 100.
    Barron JA, Wu P, Ladouceur HD, Ringeisen BR. Biological laser printing: a novel technique for creating heterogeneous 3-dimensional cell patterns. Biomed Microdevices. 2004;6:139–47.PubMedCrossRefGoogle Scholar
  101. 101.
    Guillemot F, Souquet A, Catros S, Guillotin B, Lopez J, Faucon M, Pippenger B, Bareille R, Rémy M, Bellance S, Chabassier P, Fricain JC, Amédée J. High-throughput laser printing of cells and biomaterials for tissue engineering. Acta Biomater. 2010;6:2494–500.PubMedCrossRefGoogle Scholar
  102. 102.
    Guillotin B, Souquet A, Catros S, Duocastella M, Pippenger B, Bellance S, Bareille R, Rémy M, Bordenave L, Amédée J, Guillemot F. Laser assisted bioprinting of engineered tissue with high cell density and microscale organization. Biomaterials. 2010;31:7250–6.PubMedCrossRefGoogle Scholar
  103. 103.
    Okamoto T, Suzuki T, Yamamoto N. Microarray fabrication with covalent attachment of DNA using bubble jet technology. Nat Biotechnol. 2000;18:438–41.PubMedCrossRefGoogle Scholar
  104. 104.
    Goldmann T, Gonzalez JS. DNA-printing: utilization of a standard inkjet printer for the transfer of nucleic acids to solid supports. J Biochem Biophys Methods. 2000;42:105–10.PubMedCrossRefGoogle Scholar
  105. 105.
    Xu T, Kincaid H, Atala A, Yoo JJ. High-throughput production of single-cell microparticles using an inkjet printing technology. J Manuf Sci Eng. 2008;130:021017.CrossRefGoogle Scholar
  106. 106.
    Cui X, Dean D, Ruggeri ZM, Boland T. Cell damage evaluation of thermal inkjet printed Chinese hamster ovary cells. Biotechnol Bioeng. 2010;106:963–9.PubMedCrossRefGoogle Scholar
  107. 107.
    Tekin E, Smith PJ, Schubert US. Inkjet printing as a deposition and patterning tool for polymers and inorganic particles. Soft Matter. 2008;4:703–13.CrossRefGoogle Scholar
  108. 108.
    Tasoglu S, Demirci U. Bioprinting for stem cell research. Trends Biotechnol. 2013;31:10–9.PubMedCrossRefGoogle Scholar
  109. 109.
    Murphy SV, Skardal A, Atala A. Evaluation of hydrogels for bio-printing applications. J Biomed Mater Res A. 2013;101:272–84.PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Khalil S, Sun W. Biopolymer deposition for freeform fabrication of hydrogel tissue constructs. Mater Sci Eng C. 2007;27:469–78.CrossRefGoogle Scholar
  111. 111.
    Skardal A, Mack D, Kapetanovic E, Atala A, Jackson JD, Yoo J, Soker S. Bioprinted amniotic fluid-derived stem cells accelerate healing of large skin wounds. Stem Cells Transl Med. 2012;1:792–802.PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Cui X, Breitenkamp K, Finn MG, Lotz M, D’Lima DD. Direct human cartilage repair using three-dimensional bioprinting technology. Tissue Eng Part A. 2012;18:1304–12.PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    De Coppi P, Bartsch G Jr, Siddiqui MM, Xu T, Santos CC, Perin L, Mostoslavsky G, Serre AC, Snyder EY, Yoo JJ, Furth ME, Soker S, Atala A. Isolation of amniotic stem cell lines with potential for therapy. Nat Biotechnol. 2007;25:100–6.PubMedCrossRefGoogle Scholar
  114. 114.
    Fedorovich NE, Swennen I, Girones J, Moroni L, van Blitterswijk CA, Schacht E, Alblas J, Dhert WJ. Evaluation of photocrosslinked Lutrol hydrogel for tissue printing applications. Biomacromolecules. 2009;10:1689–96.PubMedCrossRefGoogle Scholar
  115. 115.
    Chang R, Nam J, Sun W. Effects of dispensing pressure and nozzle diameter on cell survival from solid freeform fabrication-based direct cell writing. Tissue Eng Part A. 2008;14:41–8.PubMedCrossRefGoogle Scholar
  116. 116.
    Jakab K, Damon B, Neagu A, Kachurin A, Forgacs G. Three-dimensional tissue constructs built by bioprinting. Biorheology. 2006;43:509–13.PubMedGoogle Scholar
  117. 117.
    Visser J, Peters B, Burger TJ, Boomstra J, Dhert WJ, Melchels FP, Malda J. Biofabrication of multi-material anatomically shaped tissue constructs. Biofabrication. 2013;5:035007.PubMedCrossRefGoogle Scholar
  118. 118.
    Marga F, Jakab K, Khatiwala C, Shepherd B, Dorfman S, Hubbard B, Colbert S, Gabor F. Toward engineering functional organ modules by additive manufacturing. Biofabrication. 2012;4:022001.PubMedCrossRefGoogle Scholar
  119. 119.
    Mironov V, Kasyanov V, Markwald RR. Organ printing: from bioprinter to organ biofabrication line. Curr Opin Biotechnol. 2011;22:667–73.PubMedCrossRefGoogle Scholar
  120. 120.
    Smith CM, Stone AL, Parkhill RL, Stewart RL, Simpkins MW, Kachurin AM, Warren WL, Williams SK. Three-dimensional bioassembly tool for generating viable tissue-engineered constructs. Tissue Eng. 2004;10:1566–76.PubMedCrossRefGoogle Scholar
  121. 121.
    Duan B, Hockaday LA, Kang KH, Butcher JT III. Bioprinting of heterogeneous aortic valve conduits with alginate/gelatin hydrogels. J Biomed Mater Res A. 2013;101:1255–64.PubMedCrossRefGoogle Scholar
  122. 122.
    Norotte C, Marga FS, Niklason LE, Forgacs G. Scaffold-free vascular tissue engineering using bioprinting. Biomaterials. 2009;30:5910–7.PubMedPubMedCentralCrossRefGoogle Scholar
  123. 123.
    Xu F, Celli J, Rizvi I, Moon S, Hasan T, Demirci U. A three-dimensional in vitro ovarian cancer coculture model using a high-throughput cell patterning platform. Biotechnol J. 2011;6:204–12.PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    Bohandy J, Kim B, Adrian F. Metal deposition from a supported metal film using an excimer laser. J Appl Phys. 1986;60:1538–9.CrossRefGoogle Scholar
  125. 125.
    Barron JA, Ringeisen BR, Kim H, Spargo BJ, Chrisey DB. Application of laser printing to mammalian cells. Thin Solid Films. 2004;453:383–7.CrossRefGoogle Scholar
  126. 126.
    Ringeisen BR, Kim H, Barron JA, Krizman DB, Chrisey DB, Jackman S, Auyeung RY, Spargo BJ. Laser printing of pluripotent embryonal carcinoma cells. Tissue Eng. 2004;10:483–91.PubMedCrossRefGoogle Scholar
  127. 127.
    Chrisey DB. Materials processing: the power of direct writing. Science. 2000;289:879–81.PubMedCrossRefGoogle Scholar
  128. 128.
    Colina M, Serra P, Fernandez-Pradas JM, Sevilla L, Morenza JL. DNA deposition through laser induced forward transfer. Biosens Bioelectron. 2005;20:1638–42.PubMedCrossRefGoogle Scholar
  129. 129.
    Hopp B, Smausz T, Kresz N, Barna N, Bor Z, Kolozsvári L, Chrisey DB, Szabó A, Nógrádi A. Survival and proliferative ability of various living cell types after laser-induced forward transfer. Tissue Eng. 2005;11:1817–23.PubMedCrossRefGoogle Scholar
  130. 130.
    Gruene M, Deiwick A, Koch L, Schlie S, Unger C, Hofmann N, Bernemann I, Glasmacher B, Chichkov B. Laser printing of stem cells for biofabrication of scaffold-free autologous grafts. Tissue Eng Part C Methods. 2011;17:79–87.PubMedCrossRefGoogle Scholar
  131. 131.
    Koch L, Kuhn S, Sorg H, Gruene M, Schlie S, Gaebel R, Polchow B, Reimers K, Stoelting S, Ma N, Vogt PM, Steinhoff G, Chichkov B. Laser printing of skin cells and human stem cells. Tissue Eng Part C Methods. 2010;16:847–54.PubMedCrossRefGoogle Scholar
  132. 132.
    Guillotin B, Guillemot F. Cell patterning technologies for organotypic tissue fabrication. Trends Biotechnol. 2011;29:183–90.PubMedCrossRefGoogle Scholar
  133. 133.
    Michael S, Sorg H, Peck CT, Koch L, Deiwick A, Chichkov B, Vogt PM, Reimers K. Tissue engineered skin substitutes created by laser-assisted bioprinting form skin-like structures in the dorsal skin fold chamber in mice. PLoS One. 2013;8:e57741.PubMedPubMedCentralCrossRefGoogle Scholar
  134. 134.
    Keriquel V, Guillemot F, Arnault I, Guillotin B, Miraux S, Amédée J, Fricain JC, Catros S. In vivo bioprinting for computer- and robotic-assisted medical intervention: preliminary study in mice. Biofabrication. 2010;2:014101.PubMedCrossRefGoogle Scholar
  135. 135.
    O’Connor NE, Mulliken JB, Banks-Schlegel S, Kehinde O, Green H. Grafting of burns with cultured epithelium prepared from autologous epidermal cells. Lancet. 1981;1:75–8.CrossRefGoogle Scholar
  136. 136.
    Gerlach JC, Johnen C, Ottomann C, Bräutigam K, Plettig J, Belfekroun C, Münch S, Hartmann BV. Method for autologous single skin cell isolation for regenerative cell spray transplantation with non-cultured cells. Int J Artif Organs. 2011;34:271–9.PubMedCrossRefGoogle Scholar
  137. 137.
    Wood FM, Giles N, Stevenson A, Rea S, Fear M. Characterisation of the cell suspension harvested from the dermal epidermal junction using a ReCell(R) kit. Burns. 2012;38:44–51.PubMedCrossRefGoogle Scholar
  138. 138.
    Carsin H, Ainaud P, Le Bever H, et al. Cultured epithelial autografts in extensive burn coverage of severely traumatized patients: a five year single-center experience with 30 patients. Burns. 2000;26:379–87.PubMedCrossRefGoogle Scholar
  139. 139.
    Centanni JM, Straseski JA, Wicks A, Hank JA, Rasmussen CA, Lokuta MA, Schurr MJ, Foster KN, Faucher LD, Caruso DM, Comer AR, Allen-Hoffmann BL. StrataGraft skin substitute is well-tolerated and is not acutely immunogenic in patients with traumatic wounds: results from a prospective, randomized, controlled dose escalation trial. Ann Surg. 2011;253:672–83.PubMedPubMedCentralCrossRefGoogle Scholar
  140. 140.
    Bottcher-Haberzeth S, Biedermann T, Reichmann E. Tissue engineering of skin. Burns. 2010;36:450–60.PubMedCrossRefGoogle Scholar
  141. 141.
    Langer A, Rogowski W. Systematic review of economic evaluations of human cell-derived wound care products for the treatment of venous leg and diabetic foot ulcers. BMC Health Serv Res. 2009;9:115.PubMedPubMedCentralCrossRefGoogle Scholar
  142. 142.
    Fagerholm P, Lagali NS, Merrett K, Jackson WB, Munger R, Liu Y, Polarek JW, Söderqvist M, Griffith M. A biosynthetic alternative to human donor tissue for inducing corneal regeneration: 24-month follow-up of a phase 1 clinical study. Sci Transl Med. 2010;2:46ra61.PubMedCrossRefGoogle Scholar
  143. 143.
    Fagerholm P, Lagali NS, Carlsson DJ, Merrett K, Griffith M. Corneal regeneration following implantation of a biomimetic tissue-engineered substitute. Clin Transl Sci. 2009;2:162–4.PubMedPubMedCentralCrossRefGoogle Scholar
  144. 144.
    Palmer DA, Marcello PW, Zinman LN, Vanni AJ. Urethral reconstruction with rectal mucosa graft onlay: a novel, minimally invasive technique. J Urol. 2016;196:782–6.PubMedCrossRefGoogle Scholar
  145. 145.
    Lv X, Xu YM, Xie H, Feng C, Zhang J. The selection of procedures in one-stage urethroplasty for treatment of coexisting urethral strictures in anterior and posterior urethra. Urology. 2016;93:197–202.PubMedCrossRefGoogle Scholar
  146. 146.
    Bayramicli M, Akdeniz ZD. Urethra reconstruction with lateral pectoral flap in female-to-male transsexual patients. J Plast Reconstr Aesthet Surg. 2016;69(11):1558–60.PubMedCrossRefGoogle Scholar
  147. 147.
    Shin’oka T, Imai Y, Ikada Y. Transplantation of a tissue-engineered pulmonary artery. N Engl J Med. 2001;344:532–3.PubMedCrossRefGoogle Scholar
  148. 148.
    L’Heureux N, McAllister TN, de la Fuente LM. Tissue-engineered blood vessel for adult arterial revascularization. N Engl J Med. 2007;357:1451–3.PubMedCrossRefGoogle Scholar
  149. 149.
    Dahl SL, Kypson AP, Lawson JH, et al. Readily available tissue-engineered vascular grafts. Sci Transl Med. 2011;3:68ra69.CrossRefGoogle Scholar
  150. 150.
    Scriven SD, Booth C, Thomas DF, Trejdosiewicz LK, Southgate J. Reconstitution of human urothelium from monolayer cultures. J Urol. 1997;158:1147–52.PubMedCrossRefGoogle Scholar
  151. 151.
    Soler R, Fullhase C, Atala A. Regenerative medicine strategies for treatment of neurogenic bladder. Therapy. 2009;6:177–84.PubMedPubMedCentralCrossRefGoogle Scholar
  152. 152.
    Oberpenning F, Meng J, Yoo JJ, Atala A. De novo reconstitution of a functional mammalian urinary bladder by tissue engineering. Nat Biotechnol. 1999;17:149–55.PubMedCrossRefGoogle Scholar
  153. 153.
    De Filippo RE, Bishop CE, Filho LF, Yoo JJ, Atala A. Tissue engineering a complete vaginal replacement from a small biopsy of autologous tissue. Transplantation. 2008;86:208–14.PubMedCrossRefGoogle Scholar
  154. 154.
    Pashuck ET, Stevens MM. Designing regenerative biomaterial therapies for the clinic. Sci Transl Med. 2012;4:160sr164.CrossRefGoogle Scholar
  155. 155.
    Cuomo AV, Virk M, Petrigliano F, Morgan EF, Lieberman JR. Mesenchymal stem cell concentration and bone repair: potential pitfalls from bench to bedside. J Bone Joint Surg Am. 2009;91:1073–83.PubMedCrossRefGoogle Scholar
  156. 156.
    Lokmic Z, Thomas JL, Morrison WA, Thompson EW, Mitchell GM. An endogenously deposited fibrin scaffold determines construct size in the surgically created arteriovenous loop chamber model of tissue engineering. J Vasc Surg. 2008;48:974–85.PubMedCrossRefGoogle Scholar
  157. 157.
    Findlay MW, Dolderer JH, Trost N, Craft RO, Cao Y, Cooper-White J, Stevens G, Morrison WA. Tissue-engineered breast reconstruction: bridging the gap toward large-volume tissue engineering in humans. Plast Reconstr Surg. 2011;128:1206–15.PubMedCrossRefGoogle Scholar
  158. 158.
    Lin SD, Wang KH, Kao AP. Engineered adipose tissue of predefined shape and dimensions from human adipose-derived mesenchymal stem cells. Tissue Eng Part A. 2008;14:571–81.PubMedCrossRefGoogle Scholar
  159. 159.
    Chhaya MP, Melchels FP, Holzapfel BM, Baldwin JG, Hutmacher DW. Sustained regeneration of high-volume adipose tissue for breast reconstruction using computer aided design and biomanufacturing. Biomaterials. 2015;52:551–60.PubMedCrossRefGoogle Scholar
  160. 160.
    Reichert JC, Cipitria A, Epari DR, Saifzadeh S, Krishnakanth P, Berner A, Woodruff MA, Schell H, Mehta M, Schuetz MA, Duda GN, Hutmacher DW. A tissue engineering solution for segmental defect regeneration in load-bearing long bones. Sci Transl Med. 2012;4:141ra193.CrossRefGoogle Scholar
  161. 161.
    Rohner D, Hutmacher DW, Cheng TK, Oberholzer M, Hammer B. In vivo efficacy of bone-marrow-coated polycaprolactone scaffolds for the reconstruction of orbital defects in the pig. J Biomed Mater Res B Appl Biomater. 2003;66:574–80.PubMedCrossRefGoogle Scholar
  162. 162.
    Schantz JT, Lim TC, Ning C, et al. Cranioplasty after trephination using a novel biodegradable burr hole cover: technical case report. Neurosurgery. 2006;58:ONS-E176.Google Scholar
  163. 163.
    Rai B, Oest ME, Dupont KM, Ho KH, Teoh SH, Guldberg RE. Combination of platelet-rich plasma with polycaprolactone-tricalcium phosphate scaffolds for segmental bone defect repair. J Biomed Mater Res A. 2007;81:888–99.PubMedCrossRefGoogle Scholar
  164. 164.
    Stevens MM, Marini RP, Schaefer D, Aronson J, Langer R, Shastri VP. In vivo engineering of organs: the bone bioreactor. Proc Natl Acad Sci U S A. 2005;102:11450–5.PubMedPubMedCentralCrossRefGoogle Scholar
  165. 165.
    Lanza RP, Chung HY, Yoo JJ, Wettstein PJ, Blackwell C, Borson N, Hofmeister E, Schuch G, Soker S, Moraes CT, West MD, Atala A. Generation of histocompatible tissues using nuclear transplantation. Nat Biotechnol. 2002;20:689–96.PubMedCrossRefGoogle Scholar
  166. 166.
    Orlando G, Farney AC, Iskandar S, Mirmalek-Sani SH, Sullivan DC, Moran E, AbouShwareb T, De Coppi P, Wood KJ, Stratta RJ, Atala A, Yoo JJ, Soker S. Production and implantation of renal extracellular matrix scaffolds from porcine kidneys as a platform for renal bioengineering investigations. Ann Surg. 2012;256:363–70.PubMedCrossRefGoogle Scholar
  167. 167.
    Chen KL, Eberli D, Yoo JJ, Atala A. Bioengineered corporal tissue for structural and functional restoration of the penis. Proc Natl Acad Sci U S A. 2010;107:3346–50.PubMedCrossRefGoogle Scholar
  168. 168.
    Ott HC, Matthiesen TS, Goh SK, Black LD, Kren SM, Netoff TI, Taylor DA. Perfusion-decellularized matrix: using nature’s platform to engineer a bioartificial heart. Nat Med. 2008;14:213–21.PubMedCrossRefGoogle Scholar
  169. 169.
    Baptista PM, Siddiqui MM, Lozier G, Rodriguez SR, Atal A, Soker S. The use of whole organ decellularization for the generation of a vascularized liver organoid. Hepatology. 2011;53:604–17.PubMedCrossRefGoogle Scholar
  170. 170.
    De Carlo E, Baiguera S, Conconi MT, Vigolo S, Grandi C, Lora S, Martini C, Maffei P, Tamagno G, Vettor R, Sicolo N, Parnigotto PP. Pancreatic acellular matrix supports islet survival and function in a synthetic tubular device: in vitro and in vivo studies. Int J Mol Med. 2010;25:195–202.PubMedGoogle Scholar
  171. 171.
    Fedorovich NE, Schuurman W, Wijnberg HM, Prins HJ, van Weeren PR, Malda J, Alblas J, Dhert WJ. Biofabrication of osteochondral tissue equivalents by printing topologically defined, cell-laden hydrogel scaffolds. Tissue Eng Part C Methods. 2012;18:33–44.PubMedCrossRefGoogle Scholar
  172. 172.
    Xu T, Olson J, Zhao WX, Atala A, Zhu JM, Yoo JJ. Characterization of cell constructs generated with inkjet printing technology using in vivo magnetic resonance imaging. J Manuf Sci Eng Trans ASME. 2008;130:021013.CrossRefGoogle Scholar
  173. 173.
    Zhao W, Xu T, Aboushwareb T, Atala A, Yoo J. In vivo generation of functional tissues using the inkjet printing technology for reconstructive surgery. J Am Coll Surg. 2010;211:S87.CrossRefGoogle Scholar
  174. 174.
    Warnke PH, Springer IN, Wiltfang J, Acil Y, Eufinger H, Wehmöller M, Russo PA, Bolte H, Sherry E, Behrens E, Terheyden H. Growth and transplantation of a custom vascularised bone graft in a man. Lancet. 2004;364:766–70.PubMedCrossRefGoogle Scholar
  175. 175.
    Warnke PH, Wiltfang J, Springer I, Acil Y, Bolte H, Kosmahl M, Russo PA, Sherry E, Lützen U, Wolfart S, Terheyden H. Man as living bioreactor: fate of an exogenously prepared customized tissue-engineered mandible. Biomaterials. 2006;27:3163–7.PubMedCrossRefGoogle Scholar
  176. 176.
    Malafaya PB, Silva GA, Reis RL. Natural-origin polymers as carriers and scaffolds for biomolecules and cell delivery in tissue engineering applications. Adv Drug Deliv Rev. 2007;59:207–33.PubMedCrossRefGoogle Scholar
  177. 177.
    Berson MI. Construction of pseudoareola. Surgery. 1946;20:808.PubMedPubMedCentralGoogle Scholar
  178. 178.
    Little JW III, Spear SL. The finishing touches in nipple-areolar reconstruction. Perspect Plast Surg. 1988;2:1–22.Google Scholar
  179. 179.
    Anton LE, Hartrampf CR. Nipple reconstruction with local flaps: star and wrap flaps. Perspect Plast Surg. 1991;5:67–78.Google Scholar
  180. 180.
    Jones G, Bostwic J. Nipple-areolar reconstruction. Oper Tech Plast Reconstr Surg. 1994;1:35–8.CrossRefGoogle Scholar
  181. 181.
    Mori H, Hata Y. Modified C–V flap in nipple reconstruction. J Plast Reconstr Aesthet Surg. 2008;61:1109–10.PubMedPubMedCentralCrossRefGoogle Scholar
  182. 182.
    Brackley PT, Iqbal A. Enhancing your C-V flap nipple reconstruction. J Plast Reconstr Aesthet Surg. 2009;62:128–30.PubMedPubMedCentralCrossRefGoogle Scholar
  183. 183.
    El-Ali K, Dalal M, Kat CC. Modified C-V flap for nipple reconstruction: our results in 50 patients. J Plast Reconstr Aesthet Surg. 2009;62:991–6.PubMedPubMedCentralCrossRefGoogle Scholar
  184. 184.
    Witt P, Dujon DG. The V-V flap--a simple modification of the C-V flap for nipple reconstruction. J Plast Reconstr Aesthet Surg. 2013;66:1009–10.PubMedPubMedCentralCrossRefGoogle Scholar
  185. 185.
    Elizabeth Clark S, Turton E. The CC-V flap: a novel technique for augmenting a C-V nipple reconstruction using a free dermal graft. World J Plast Surg. 2014;3:8–12.PubMedPubMedCentralGoogle Scholar
  186. 186.
    Salgarello M, Cavalcanti P, Barone-Adesi L. Atypical patterns in C-V flap nipple reconstruction: a customisation of the C-V flap. J Plast Reconstr Aesthet Surg. 2014;67:1598–9.PubMedCrossRefGoogle Scholar
  187. 187.
    Temiz G, Yesiloglu N, Sirinoglu H, Sarici M. A new modification of C-V flap technique in nipple reconstruction: rolled triangular dermal-fat flaps. Aesthet Plast Surg. 2015;39:173–5.CrossRefGoogle Scholar
  188. 188.
    Adams WM. Labial transplant for correction of loss of the nipple. Plast Reconstr Surg. 1949;4:295–8.CrossRefGoogle Scholar
  189. 189.
    Gruber RP. Nipple-areola reconstruction: a review of techniques. Clin Plast Surg. 1979;6:71–83.PubMedGoogle Scholar
  190. 190.
    Millard DR Jr. Nipple and areola reconstruction by split-skin graft from the normal side. Plast Reconstr Surg. 1972;50:350–3.PubMedPubMedCentralCrossRefGoogle Scholar
  191. 191.
    Dean NR, Neild T, Haynes J, Goddard C, Cooter RD. Fading of nipple-areolar reconstructions: the last hurdle in breast reconstruction? Br J Plast Surg. 2002;55:574–81.PubMedCrossRefGoogle Scholar
  192. 192.
    Haslik W, Nedomansky J, Hacker S, Nickl S, Schroegendorfer KF. Objective and subjective evaluation of donor-site morbidity after nipple sharing for nipple areola reconstruction. J Plast Reconstr Aesthet Surg. 2015;68:168–74.PubMedPubMedCentralCrossRefGoogle Scholar
  193. 193.
    Collis N, Garrido A. Maintenance of nipple projection using auricular cartilage. Plast Reconstr Surg. 2000;105:2276–7.CrossRefPubMedGoogle Scholar
  194. 194.
    Bernard RW, Beran SJ. Autologous fat graft in nipple reconstruction. Plast Reconstr Surg. 2003;112:964–8.CrossRefPubMedGoogle Scholar
  195. 195.
    Guerra AB, Khoobehi K, Metzinger SE, Allen RJ. New technique for nipple areola reconstruction: arrow flap and rib cartilage graft for long-lasting nipple projection. Ann Plast Surg. 2003;50:31–7.CrossRefPubMedGoogle Scholar
  196. 196.
    Gamboa-Bobadilla GM. Nipple reconstruction: the top hat technique. Ann Plast Surg. 2005;54:243–6.PubMedPubMedCentralGoogle Scholar
  197. 197.
    Hammond DC, Khuthaila D, Kim J. The skate flap purse-string technique for nipple-areola complex reconstruction. Plast Reconstr Surg. 2007;120:399–406.CrossRefPubMedGoogle Scholar
  198. 198.
    Garramone CE, Lam B. Use of AlloDerm in primary nipple reconstruction to improve long-term nipple projection. Plast Reconstr Surg. 2007;119:1663–8.CrossRefPubMedGoogle Scholar
  199. 199.
    Zenn MR, Garofalo JA. Unilateral nipple reconstruction with nipple sharing: time for a second look. Plast Reconstr Surg. 2009;123:1648–53.PubMedPubMedCentralCrossRefGoogle Scholar
  200. 200.
    Wong WW, Hiersche MA, Martin MC. The angel flap for nipple reconstruction. Can J Plast Surg. 2013;21:e1–4.PubMedPubMedCentralCrossRefGoogle Scholar
  201. 201.
    Grosdidier A, Lebeau J, Ochala C, Payan R, Bettega G. “double flag” flap nipple reconstruction. Clinical evaluation on 70 cases. Ann Chir Plast Esthet. 2014;59:123–9.PubMedPubMedCentralCrossRefGoogle Scholar
  202. 202.
    Yang JD, Ryu JY, Ryu DW, Kwon OH, Bae SG, Lee JW, Choi KY, Chung HY, Cho BC. Our experiences in nipple reconstruction using the Hammond flap. Arch Plast Surg. 2014;41:550–5.PubMedPubMedCentralCrossRefGoogle Scholar
  203. 203.
    Halvorson EG, Cormican M, West ME, Myers V. Three-dimensional nipple-areola tattooing: a new technique with superior results. Plast Reconstr Surg. 2014;133:1073–5.PubMedPubMedCentralCrossRefGoogle Scholar
  204. 204.
    Cheng MH, Ho-Asjoe M, Wei FC, Chuang DC. Nipple reconstruction in Asian females using banked cartilage graft and modified top hat flap. Br J Plast Surg. 2003;56:692–4.CrossRefPubMedGoogle Scholar
  205. 205.
    Heitland A, Markowicz M, Koellensperger E, Allen R, Pallua N. Long-term nipple shrinkage following augmentation by an autologous rib cartilage transplant in free DIEP-flaps. J Plast Reconstr Aesthet Surg. 2006;59:1063–7.PubMedCrossRefGoogle Scholar
  206. 206.
    Cheng MH, Rodriguez ED, Smartt JM, Cardenas-Mejia A. Nipple reconstruction using the modified top hat flap with banked costal cartilage graft: long-term follow-up in 58 patients. Ann Plast Surg. 2007;59:621–8.PubMedPubMedCentralCrossRefGoogle Scholar
  207. 207.
    Lipa JE, Addison PD, Neligan PC. Patient satisfaction following nipple reconstruction incorporating autologous costal cartilage. Can J Plast Surg. 2008;16:85–8.PubMedPubMedCentralCrossRefGoogle Scholar
  208. 208.
    Mori H, Uemura N, Okazaki M. Nipple reconstruction with banked costal cartilage after vertical-type skin-sparing mastectomy and deep inferior epigastric artery perforator flap. Breast Cancer. 2015;22:95–7.PubMedCrossRefGoogle Scholar
  209. 209.
    Brent B, Bostwick J. Nipple-areola reconstruction with auricular tissues. Plast Reconstr Surg. 1977;60:353–61.PubMedGoogle Scholar
  210. 210.
    Tanabe HY, Tai Y, Kiyokawa K, Yamauchi T. Nipple-areola reconstruction with a dermal-fat flap and rolled auricular cartilage. Plast Reconstr Surg. 1997;100:431–8.CrossRefPubMedGoogle Scholar
  211. 211.
    Norton S, Akhavani MA, Kang N. The ‘hamburger’ technique for harvesting cartilage grafts in nipple reconstruction. J Plast Reconstr Aesthet Surg. 2007;60:957–9.PubMedCrossRefGoogle Scholar
  212. 212.
    Jones AP, Erdmann M. Projection and patient satisfaction using the “hamburger” nipple reconstruction technique. J Plast Reconstr Aesthet Surg. 2012;65:207–12.PubMedCrossRefGoogle Scholar
  213. 213.
    Breuing KH, Warren SM. Immediate bilateral breast reconstruction with implants and inferolateral AlloDerm slings. Ann Plast Surg. 2005;55:232–9.PubMedPubMedCentralCrossRefGoogle Scholar
  214. 214.
    Nahabedian MY. Secondary nipple reconstruction using local flaps and AlloDerm. Plast Reconstr Surg. 2005;115:2056–61.CrossRefPubMedGoogle Scholar
  215. 215.
    Wong AK, Schonmeyr B, Singh P, Carlson DL, Li S, Mehrara BJ. Histologic analysis of angiogenesis and lymphangiogenesis in acellular human dermis. Plast Reconstr Surg. 2008;121:1144–52.PubMedCrossRefGoogle Scholar
  216. 216.
    Rao SS, Seaman BJ, Davison SP. The acellular dermal matrix onlay graft for areolar reconstruction. Ann Plast Surg. 2014;72:508–12.PubMedCrossRefGoogle Scholar
  217. 217.
    Tierney BP, Hodde J, Changkuo DI. Biologic collagen cylinder with skate flap technique for nipple reconstruction. Plast Surg Int. 2014;2014:194087.PubMedPubMedCentralGoogle Scholar
  218. 218.
    Jankau J, Jaskiewicz J, Ankiewicz A. A new method for using a silicone rod for permanent nipple projection after breast reconstruction procedures. Breast. 2011;20:124–8.PubMedCrossRefGoogle Scholar
  219. 219.
    Jankau J. Use of silicone rod for permanent nipple projection after breast reconstruction procedures. In: Shiffman MA, editor. Breast reconstruction: art, science and new clinical techniques. Berlin: Springer; 2016. p. 987–93.CrossRefGoogle Scholar
  220. 220.
    McCarthy CM, VanLaeken N, Lennox P, Scott AM, Pusic AL. The efficacy of Artecoll injections for the augmentation of nipple projection in breast reconstruction. Eplasty. 2010;10:e7.PubMedPubMedCentralGoogle Scholar
  221. 221.
    Yanaga H. Nipple-areola reconstruction with a dermal-fat flap: technical improvement from rolled auricular cartilage to artificial bone. Plast Reconstr Surg. 2003;112:1863–9.CrossRefPubMedGoogle Scholar
  222. 222.
    Nishiyama T, Nakajima T, Yoshimura Y, Nakanishi Y. Utilizing solid models for preoperative shaping of HAP-TCP ceramic bone substitute: application for craniomaxillofacial surgery. Eur J Plast Surg. 1994;17:173.CrossRefGoogle Scholar
  223. 223.
    Evans KK, Rasko Y, Lenert J, Olding M. The use of calcium hydroxylapatite for nipple projection after failed nipple-areolar reconstruction: early results. Ann Plast Surg. 2005;55:25–9.CrossRefPubMedGoogle Scholar
  224. 224.
    Holbrook A, Lee S, Soo MS. Mammographic appearance of calcium hydroxylapatite (RadiesseTM) injected into the breast for nipple reconstruction. Breast J. 2013;19:104–13.PubMedCrossRefGoogle Scholar
  225. 225.
    Germano D, De Biasio F, Piedimonte A, Parodi PC. Nipple reconstruction using the fleur-de-lis flap technique. Aesthet Plast Surg. 2006;30:399–402.CrossRefGoogle Scholar
  226. 226.
    Cronin TD, Upton J, McDonough JM. Reconstruction of the breast after mastectomy. Plast Reconstr Surg. 1977;59:1–14.CrossRefPubMedGoogle Scholar
  227. 227.
    Gruber RP. Method to produce better areolae and nipples on reconstructed breasts. Plast Reconstr Surg. 1977;60:505–13.PubMedCrossRefGoogle Scholar
  228. 228.
    Cao YL, Lach E, Kim TH, Rodriguez A, Arevalo CA, Vacanti C. A. Tissue-engineered nipple reconstruction. Plast Reconstr Surg. 1998;102:2293–8.PubMedPubMedCentralCrossRefGoogle Scholar
  229. 229.
    Cerqueira B, Cornell L. NovoThelium LLC. Tissue engineered nipples for breast reconstruction. Accessed 23 Oct 2016.
  230. 230.
    Bosworth L, Collins S, Boland T. TeVido BioDevices. Accessed 23 Oct 2016.
  231. 231.
    Chae MP, Hunter-Smith DJ, Spychal RT, Rozen WM. 3D volumetric analysis for planning breast reconstructive surgery. Breast Cancer Res Treat. 2014;146:457–60.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2018

Authors and Affiliations

  • Michael P. Chae
    • 1
    Email author
  • David J. Hunter-Smith
    • 1
    • 2
  • Sean V. Murphy
    • 3
  • Warren Matthew Rozen
    • 1
    • 2
  1. 1.Department of Plastic and Reconstructive SurgeryFrankston Hospital, Peninsula HealthFrankstonAustralia
  2. 2.Department of SurgerySchool of Clinical Science at Monash Health, Monash UniversityClaytonAustralia
  3. 3.Wake Forest Institute for Regenerative MedicineWake Forest University School of MedicineWinston-SalemUSA

Personalised recommendations