Porcine skin is commonly used as a model for human skin injury and as a source material for biologic scaffold materials. Although remarkable similarities between porcine and human skin exist, regional anatomic variations present in human skin are also present in porcine skin. The objective of this study was to evaluate the structure of porcine skin from 11 different anatomic regions in the American Yorkshire crossbreed. Both qualitative and quantitative methods were used, with emphasis on epidermal and dermal thickness, hair follicle density, and collagen and elastin composition and distribution. The results showed that significant regional differences in skin histology exist, particularly with regard to the thickness of the dermis and epidermis and the amount of collagen and elastin within each tissue. Differences were also seen in the distribution of type I and type III collagen within the dermis. Therefore, while porcine skin shares many similarities with human skin, distinct regional differences in composition and morphology exist. This study highlights the importance of appreciating these regional differences to avoid misinterpretation of experimental results when using porcine skin as a human analogue.
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References
1.
HolbrookK.A., and OdlandG.F.Regional differences in the thickness (cell layers) of the human stratum corneum: an ultrastructural analysis. J Invest Dermatol, 62, 415, 1974.
2.
EnnaC.D., and DyerR.F.The histomorphology of the elastic tissue system in the skin of the human hand. Hand, 11, 144, 1979.
3.
UrmacherC.Histology of normal skin. Am J Surg Pathol, 14, 671, 1990.
4.
KanitakisJ.Anatomy, histology and immunohistochemistry of normal human skin. Eur J Dermatol, 12, 390; quiz 400, 2002.
5.
ChuenkongkaewT.Modification of split-thickness skin graft: cosmetic donor site and better recipient site. Ann Plast Surg, 50, 212, 2003.
6.
KimJ.S., ParkS.W., ChoiT.H., KimN.G., LeeK.S., KimJ.R., et al.The evaluation of relevant factors influencing skin graft changes in color over time. Dermatol Surg, 34, 32, 2008.
7.
HarrisonC.A., and MacNeilS.The mechanism of skin graft contraction: an update on current research and potential future therapies. Burns, 34, 153, 2008.
8.
NelsonC.V., MillerS.F., EppingerM., and FinleyR.K.Micrografts. II: Evaluation of 25:1, 50:1, and 100:1 expansion skin grafts in the porcine model. J Burn Care Rehabil, 16, 31, 1995.
9.
MeyerW., ZschemischN.H., and GodynickiS.The porcine ear skin as a model system for the human integument: influence of storage conditions on basic features of epidermis structure and function—a histological and histochemical study. Polish J Vet Sci, 6, 17, 2003.
10.
AvonS.L., and WoodR.E.Porcine skin as an in-vivo model for ageing of human bite marks. J Forensic Odontostomatol, 23, 30, 2005.
11.
JacobiU., KaiserM., TollR., MangelsdorfS., AudringH., OtbergN., et al.Porcine ear skin: an in vitro model for human skin. Skin Res Technol, 13, 19, 2007.
12.
BranskiL.K., MittermayrR., HerndonD.N., NorburyW.B., MastersO.E., HofmannM., et al.A porcine model of full-thickness burn, excision and skin autografting. Burns, 34, 1119, 2008.
13.
BrozynaA., WasilewskaK., WesierskaK., and ChwirotB.W.Porcine skin as a model system for studies of adverse effects of narrow-band UVB pulses on human skin. J Toxicol Environ Health A, 72, 789, 2009.
14.
PhilandrianosC., Andrac-MeyerL., MordonS., FeuersteinJ.M., SabatierF., VeranJ., et al.Comparison of five dermal substitutes in full-thickness skin wound healing in a porcine model. Burns, 38, 820, 2012.
15.
KimJ.W., LeeD.W., ChoiW.H., JeonY.R., KimS.H., ChoH., et al.Development of a porcine skin injury model and characterization of the dose-dependent response to high-dose radiation. J Radiat Res, 54, 823, 2013.
16.
MacLeodT.M., SarathchandraP., WilliamsG., SandersR., and GreenC.J.Evaluation of a porcine origin acellular dermal matrix and small intestinal submucosa as dermal replacements in preventing secondary skin graft contraction. Burns, 30, 431, 2004.
17.
HsuP.W., SalgadoC.J., KentK., FinneganM., PelloM., SimonsR., et al.Evaluation of porcine dermal collagen (Permacol) used in abdominal wall reconstruction. J Plast Reconstr Aesthet Surg, 62, 1484, 2008.
18.
MacLeodT.M., CambreyA., WilliamsG., SandersR., and GreenC.J.Evaluation of Permacol as a cultured skin equivalent. Burns, 34, 1169, 2008.
19.
XuH., WanH., ZuoW., SunW., OwensR.T., HarperJ.R., et al.A porcine-derived acellular dermal scaffold that supports soft tissue regeneration: removal of terminal galactose-alpha-(1,3)-galactose and retention of matrix structure. Tissue Eng Part A, 15, 1807, 2009.
20.
ReingJ.E., BrownB.N., DalyK.A., FreundJ.M., GilbertT.W., HsiongS.X., et al.The effects of processing methods upon mechanical and biologic properties of porcine dermal extracellular matrix scaffolds. Biomaterials, 31, 8626, 2010.
21.
ChangS.K., BrownieC., and RiviereJ.E.Percutaneous absorption of topical parathion through porcine skin: in vitro studies on the effect of environmental perturbations. J Vet Pharmacol Therapeut, 17, 434, 1994.
22.
NetzlaffF., SchaeferU.F., LehrC.M., MeiersP., StahlJ., KietzmannM., et al.Comparison of bovine udder skin with human and porcine skin in percutaneous permeation experiments. Altern Lab Anim, 34, 499, 2006.
23.
KaradzovskaD., BrooksJ.D., and RiviereJ.E.Experimental factors affecting in vitro absorption of six model compounds across porcine skin. Toxicol in vitro, 26, 1191, 2012.
24.
DebeerS., Le LuduecJ.B., KaiserlianD., LaurentP., NicolasJ.F., DuboisB., et al.Comparative histology and immunohistochemistry of porcine versus human skin. Eur J Dermatol, 23, 456, 2013.
25.
Kakasheva-MazhenkovskaL., MilenkovaL., GjokikG., and JanevskaV.Variations of the histomorphological characteristics of human skin of different body regions in subjects of different age. Prilozi/Makedonska akademija na naukite i umetnostite, Oddelenie za bioloski i medicinski nauki=Contributions/Macedonian Academy of Sciences and Arts, Section of Biological and Medical Sciences. 32, 119, 2011.
26.
SchmittS., SchaferU.F., DoblerL., and ReichlingJ.Variation of in vitro human skin permeation of rose oil between different application sites. Forschende Komplementarmedizin, 17, 126, 2010.
27.
RobertsonK., and ReesJ.L.Variation in epidermal morphology in human skin at different body sites as measured by reflectance confocal microscopy. Acta Derm Venereol, 90, 368, 2010.
28.
OtbergN., RichterH., SchaeferH., Blume-PeytaviU., SterryW., and LademannJ.Variations of hair follicle size and distribution in different body sites. J Invest Dermatol, 122, 14, 2004.
29.
Sandby-MollerJ., PoulsenT., and WulfH.C.Epidermal thickness at different body sites: relationship to age, gender, pigmentation, blood content, skin type and smoking habits. Acta Derm Venereol, 83, 410, 2003.
30.
LeeY., and HwangK.Skin thickness of Korean adults. Surg Radiol Anat, 24, 183, 2002.
31.
Ya-XianZ., SuetakeT., and TagamiH.Number of cell layers of the stratum corneum in normal skin—relationship to the anatomical location on the body, age, sex and physical parameters. Arch Dermatol Res, 291, 555, 1999.
32.
RichtersC.D., HoekstraM.J., van BaareJ., du PontJ.S., and KamperdijkE.W.Morphology of glycerol-preserved human cadaver skin. Burns, 22, 113, 1996.
33.
SugiharaT., OhuraT., HommaK., and IgawaH.H.The extensibility in human skin: variation according to age and site. Br J Plast Surg, 44, 418, 1991.
34.
MeyerW., SchwarzR., and NeurandK.The skin of domestic mammals as a model for the human skin, with special reference to the domestic pig. Curr Probl Dermatol, 7, 39, 1978.
35.
HultA.M., and GoltzR.W.The measurement of elastin in human skin and its quantity in relation to age. J Invest Dermatol, 44, 408, 1965.
36.
KirkJ.E., and ChieffiM.Variation with age in elasticity of skin and subcutaneous tissue in human individuals. J Gerontol, 17, 373, 1962.
37.
MatouskovaE., BucekS., VogtovaD., VeselyP., ChaloupkovaA., BrozL., et al.Treatment of burns and donor sites with human allogeneic keratinocytes grown on acellular pig dermis. Br J Dermatol, 136, 901, 1997.
38.
BuinewiczB., and RosenB.Acellular cadaveric dermis (AlloDerm): a new alternative for abdominal hernia repair. Ann Plast Surg, 52, 188, 2004.
39.
TangL.L., LiuH., WangY.L., XianC.Y., and SuA.H.Evaluation of the biocompatibility of acellular porcine dermis. Colloids Surf B Biointerfaces, 57, 215, 2007.
40.
GomelskyA., HaverkornR.M., SimoneauxW.J., BilelloS., and KubrichtW.S.3rd. Incidence and management of vaginal extrusion of acellular porcine dermis after incontinence and prolapse surgery. Int Urogynecol J Pelvic Floor Dysfunct, 18, 1337, 2007.
41.
BellowsC.F., AlboD., BergerD.H., and AwadS.S.Abdominal wall repair using human acellular dermis. Am J Surg, 194, 192, 2007.
42.
NgoM.D., AbermanH.M., HawesM.L., ChoiB., and GertzmanA.A.Evaluation of human acellular dermis versus porcine acellular dermis in an in vivo model for incisional hernia repair. Cell Tissue Bank, 12, 135, 2011.
43.
NasajpourH., LeBlancK.A., and SteeleM.H.Complex hernia repair using component separation technique paired with intraperitoneal acellular porcine dermis and synthetic mesh overlay. Ann Plast Surg, 66, 280, 2011.
44.
LarcherL., RimlS., CampisiC., LazzeriD., and HuemerG.M.Acellular dermis-assisted prosthetic breast reconstruction: mission accomplished? Plast Reconstr Surg, 130, 499e, 2012.
45.
HeyerK., BuckD.W.2nd, KatoC., KhanS.A., AlamM., and KimJ.Y.Reversed acellular dermis: failure of graft incorporation in primary tissue expander breast reconstruction resulting in recurrent breast cellulitis. Plast Reconstr Surg, 125, 66e, 2010.
46.
KimJ.Y., DavilaA.A., PersingS., ConnorC.M., JovanovicB., KhanS.A., et al.A meta-analysis of human acellular dermis and submuscular tissue expander breast reconstruction. Plast Reconstr Surg, 129, 28, 2012.
47.
ItoM., and CotsarelisG.Is the hair follicle necessary for normal wound healing? J Invest Dermatol, 128, 1059, 2008.
48.
JimenezF., PobletE., and IzetaA.Reflections on how wound healing-promoting effects of the hair follicle can be translated into clinical practice. Exp Dermatol [Epub ahead of print]; DOI: 10.1111/exd.12521, 2014.
49.
LeirosG.J., KusinskyA.G., DragoH., BossiS., SturlaF., CastellanosM.L., et al.Dermal papilla cells improve the wound healing process and generate hair bud-like structures in grafted skin substitutes using hair follicle stem cells. Stem Cells Transl Med, 10, 1209, 2014.
50.
UlrichM.M., VerkerkM., ReijnenL., VligM., van den BogaerdtA.J., and MiddelkoopE.Expression profile of proteins involved in scar formation in the healing process of full-thickness excisional wounds in the porcine model. Wound Repair Regen, 15, 482, 2007.
51.
ChenR.N., HoH.O., TsaiY.T., and SheuM.T.Process development of an acellular dermal matrix (ADM) for biomedical applications. Biomaterials, 25, 2679, 2004.
52.
TurnerN.J., PezzoneM.A., BrownB.N., and BadylakS.F.Quantitative multispectral imaging of Herovici's polychrome for the assessment of collagen content and tissue remodelling. J Tissue Eng Regen Med, 7, 139, 2013.
SchneiderC.A., RasbandW.S., and EliceiriK.W.NIH Image to ImageJ: 25 years of image analysis. Nat Methods, 9, 671, 2012.
55.
FeldmannR.J., and MaibachH.I.Regional variation in percutaneous penetration of 14C cortisol in man. J Invest Dermatol, 48, 181, 1967.
56.
OgisoT., ShirakiT., OkajimaK., TaninoT., IwakiM., and WadaT.Transfollicular drug delivery: penetration of drugs through human scalp skin and comparison of penetration between scalp and abdominal skins in vitro. J Drug Target, 10, 369, 2002.
57.
HeinrichW., LangeP.M., StirtzT., IancuC., and HeidemannE.Isolation and characterization of the large cyanogen bromide peptides from the alpha1- and alpha2-chains of pig skin collagen. FEBS Lett, 16, 63, 1971.
58.
RnjakJ., WiseS.G., MithieuxS.M., and WeissA.S.Severe burn injuries and the role of elastin in the design of dermal substitutes. Tissue Eng Part B Rev, 17, 81, 2011.
59.
BerthodF., GermainL., LiH., XuW., DamourO., and AugerF.A.Collagen fibril network and elastic system remodeling in a reconstructed skin transplanted on nude mice. Matrix Biol, 20, 463, 2001.
60.
MeyerW., NeurandK., and RadkeB.Elastic fibre arrangement in the skin of the pig. Arch Dermatol Res, 270, 391, 1981.
61.
VardaxisN.J., BransT.A., BoonM.E., KreisR.W., and MarresL.M.Confocal laser scanning microscopy of porcine skin: implications for human wound healing studies. J Anat, 190 (Pt 4), 601, 1997.
62.
JorJ.W., NielsenP.M., NashM.P., and HunterP.J.Modelling collagen fibre orientation in porcine skin based upon confocal laser scanning microscopy. Skin Res Technol, 17, 149, 2011.
63.
MeyerW., and NeurandK.The distribution of enzymes in the skin of the domestic pig. Lab Anim, 10, 237, 1976.
64.
MeyerW., NeurandK., and RadkeB.Collagen fibre arrangement in the skin of the pig. J Anat, 134, 139, 1982.
65.
TsukiseA., and MeyerW.Histochemistry of complex carbohydrates in the hairy skin of the domestic pig. Histochem J, 15, 845, 1983.
66.
ChanQ.E., HarveyJ.G., GrafN.S., GodfreyC., and HollandA.J.The correlation between time to skin grafting and hypertrophic scarring following an acute contact burn in a porcine model. J Burn Care Res, 33, e43, 2012.
67.
NortonL., and ChvapilM.Comparison of newer synthetic and biological wound dressings. J Trauma, 21, 463, 1981.
68.
MuangmanP., EngravL.H., HeimbachD.M., HarunariN., HonariS., GibranN.S., et al.Complex wound management utilizing an artificial dermal matrix. Ann Plast Surg, 57, 199, 2006.
69.
MorrisG.M., and HopewellJ.W.Epidermal cell kinetics of the pig: a review. Cell Tissue Kinet, 23, 271, 1990.
70.
JaitleyS., and SaraswathiT.Pathophysiology of Langerhans cells. J Oral Maxillofac Pathol, 16, 239, 2012.
71.
IgyartoB.Z., and KaplanD.H.The evolving function of Langerhans cells in adaptive skin immunity. Immunol Cell Biol, 88, 361, 2010.
72.
OrtonneJ.P.Normal and abnormal skin color. Annal Dermatol Venereol, 139Suppl 4, S125, 2012 (Article in French).
73.
SimonJ.D., and PelesD.N.The red and the black. Acc Chem Res, 43, 1452, 2010.
74.
SwindleM.M., and SmithA.C.Comparative anatomy and physiology of the pig. Scand J Lab Anim Sci, 25, 11, 1998.
75.
SwindleM.M.Comparative anatomy, physiology and surgical techniques in swine: applications to pharmacological investigations. Drug Metab Rev, 34, 41, 2002.
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