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. 2021 Oct 14;18(20):10806. doi: 10.3390/ijerph182010806

Table 1.

Remarkable achievements in 3D bioprinting of skin tissue. Articles from 2016 to 2018 and from 2019 to 2020.

Tissue Cell Type Biomaterial Printed Model Outcome Reference
Skin
2016–2018
Human dermal endothelial cells Sodium alginate, chitosan, gelatin, gellan gum, collagen I (core materials), pure alginate (shell material) Core/shell construct
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    Biological, physical and mechanical characterization of the construct (with or without loaded growth factors)

 Akkineni et al. 2016
Human fibroblasts (hFB) and keratinocytes (hKC) obtained from skin biopsies of healthy donors Plasma-derived fibrin scaffold Skin: dermis + epidermis
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    Stratification and differentiation of dermis and epidermis

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    Morphological similarities to native human skin

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    Fast bioprinting process (<35 min)

 Cubo et al. 2016
Human primary dermal fibroblasts, human primary epidermal keratinocytes Newly-developed ECM-like bioInk Skin model
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    Proof of concept study, with the aim to set a bioprinting approach “for industrial routine application”

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    Viable and proliferating cells

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    Assessment of differentiation and stratification by histological evaluations (not fully achieved)

 Rimann et al. 2016
Amniotic fluid-derived stem (AFS) cells Photo-cross-linkable heparin-conjugated hyaluronic acid (HA-HP) hydrogel In situ skin graft
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    Enhanced re-epithelialization and wound healing using HA-HP hydrogel + ASF

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    Improved vascularization of the regenerating skin tissue

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    ECM components secreted

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    In vivo study

 Skardal et al. 2016
Fibroblasts Collagen hydrogel Dermal construct
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    Seeding of fibroblasts in a multi-layered structure of collagen hydrogel

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    Evaluation of the construct permeability to silica nanoparticles for drug testing: permeability rate similar to native dermal layer

 Hou et al. 2017
Human fibroblasts and human keratinocytes Unique bioink of alginate, gelatin, fibrinogen Skin: dermis + epidermis
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    Biological/structural similarity with human normal skin

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    Formation of desmosomes and hemidesmosomes, epithelial maturation

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    Bioprinting of complex architectures (proof of concept)

 Pourchet et al. 2017
Human primary skin cells (fibroblasts and keratinocytes) Collagen, gelatin. PCL (prevents collagen shrinkage) Skin: dermis + epidermis
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    Thick and stratified epidermis

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    Stretched fibroblasts

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    Expression of dermal and epidermal markers (collagen I, K10, involucrin)

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    Superior yield of KCs maturation (vs. manual seeding)

 Kim et al. 2017
Keratinocytes (KCs), melanocytes (MCs) and fibroblasts (FBs) (from three different Caucasian skin donors) Collagen, PVP (Polyvinylpyrrolidone) polymer Pigmented skin: bioprinting vs. manual-cast approach
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    KCs and MCs markers of proliferation and differentiation, MCs anchoring at the basement membrane in the bioprinted skin

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    More homogeneous distribution of epidermal cells in the bioprinted pigmented skin

 Ng et al. 2018
Endothelial progenitor cells (EPCs) and adipose-derived stem cells (ASCs) added to HDF (human dermal fibroblast) and HEK (human epidermal keratinocyte) Skin-derived extracellular matrix (S-dECM) bioink, collagen I matrix (as a control) Skin patch
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    Promotion of cellular differentiation and maturation (better properties than Collagen I) by dECM

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    Promotion of re-epithelialization, wound closure and neovascularization in vivo by the bioprinted pre-vascularized patch (ASCSs + EPCs in dECM)

 Kim et al. 2018
Fibroblasts, melanocytes and keratinocytes Collagen hydrogel Pigmented skin model (dermal + epidermal layer)
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    Stratification of dermis and epidermis, and pigmentation spots

 Min et al. 2018
Human melanocytes (HEM), human keratinocytes (HaCat) and human dermal fibroblasts (HDF) Gelatin methacrylamide (GelMA) and collagen (Col)+ tyrosinase (Ty) Living skin model
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    In vitro characterization of the bioink both from a mechanical (degradation rate, viscosity and rheological properties) and a cellular (proliferation rate, cell viability, cell migration) point of views

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    Promotion of melanocytes viability and proliferation by Ty

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    Enhanced wound healing using Ty doped bioink in in vivo studies

 Shi et al. 2018
2019–2020
Fibroblasts and keratinocytes Hydrogel (fibrinogen, collagen I, trombin) In situ skin bioprinting
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    Wound healing with re-epithelialization and vascularization, preventing scar formation (histological analysis)

  • -

    Wounding and treatment of murine and porcine models with the developed in situ approach

 Albanna et al. 2019
Neonatal human dermal fibroblasts and neonatal normal human epithelial keratinocytes Gelatin, fibrinogen, collagen, elastin (dermal hydrogel) Skin equivalent
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    Bioprinting of three different layers (dermal, basal and epidermal layers)

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    In vitro culture of the skin construct

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    Histological analysis: morphological and molecular similarities with native human skin

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    Structural evaluations: electrical conductivity, permeability and barrier function assessment

 Derr et al. 2019
Human fibroblasts, keratinocytes, human umbilical vein endothelial cells (HUVECs), preadipocytes dECM-based bioinks, gelatin hydrogel. PCL transwell system (supportive mesh) A vascularized tri-layered skin model (epidermis, dermis, and hypodermis)
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    Well differentiated and stratified skin equivalent, similar to native human skin.

  • -

    Presence of epidermal-dermal junction and vascular channels.

  • -

    Investigation of skin stemness markers

 Kim et al. 2019
Human amniotic epithelial cells (AECs), Wharton’s jelly-derived mesenchymal stem cells (WJMSCs) Alginate/gelatin composite hydrogels Skin bilayered construct
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    High printing precision and cell viability

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    Investigation on the rheological properties of the bioinks

 Liu et al. 2019
No cells PCL and silk sericin for epidermis + CS_SA hydrogel for dermis (CS, chitosan; SA, sodium alginate) Composite skin construct:
three-dimensional skin asymmetric construct (3D_SAC)
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    Morphological, mechanical and structural characterization of 3D_SAC

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    Analysis of 3D_SAC cytotoxic profile and antimicrobial properties

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    Potential application for wound dressing

 Miguel et al. 2019
Human dermal fibroblasts (HDFs) Skin decellularized extracellular matrix (dECM) Bioprinted 3D construct
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    Derivation of a bioink from decellularized ECM

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    High bioactivity of the biomaterial, promoting skin development and morphogenesis

 Won et al. 2019
Neonatal human dermal fibroblasts (NHDFs), immortalized human keratinocyte cell line (HaCaT) and human umbilical vein endothelial cells (HUVECs) Methacrylated gelatin (GelMA) and succinylated chitosan/dextran aldehyde Prevascularized core/shell construct for wound healing
  • -

    In vitro analysis: accelerated wound healing (twofold rate compared to the control)

 Turner et al. 2020
Human-derived skin fibroblasts (hSF) Bioink made of nanofibrillated cellulose (NFC), alginate (ALG) and carboxymethyl cellulose (CMC) Dermal construct
  • -

    Optimization of a bioink with the desired rheological properties and the proper printability

  • -

    High cell viability and proliferation

 Zidaric et al. 2020