Abstract
In regenerative medicine, despite the chances of graft-rejection, scaffolds prepared from extracellular matrices of various mammalian organs/tissues are widely used. Graft-assisted healing of full thickness skin-wounds is a major use of these bioscaffolds. Therefore, considering its prospective clinical use as a wound healing matrix, this study evaluated the healing potential of porcine cholecyst-derived scaffold (CDS) prepared by a non-detergent/enzymatic method for treating naturally occurring full thickness lacerated wounds in dogs. The CDS caused, in comparison with a commercial-grade bioscaffold prepared out of bovine dermal collagen (BDC), faster healing with respect to the wound healing parameters like peripheral tissue oedema, necrosis (amount and type), indurations, granulation tissue formation and the extent of re-epithelialisation. After 28 days of the treatment, the wound area (mean + SE) reduced from 27.60 ± 8.96 cm2 to 0.19+ 0.18 cm2 and 21.39 ± 5.48 to 6.59 ± 2.60 cm2 in CDS and BDC treated animals, with a reduction in wound sizes by 98.95 ± 2.09% and 54.53 ± 15.90 respectively. By this time, complete wound healing was observed in at least 75% of the former and 25% of the later groups. The CDS was deemed as a candidate bioscaffold for treating full thickness lacerated skin wounds in dogs.
Similar content being viewed by others
References
Anilkumar TV, Vineetha VP, Revi D, Muhamed J, Rajan A (2014) Biomaterial properties of cholecyst-derived scaffold recovered by a non-detergent/enzymatic method. J Biomed Mater Res Part B Appl 102:1506–1516. https://doi.org/10.1002/jbm.b.33131 PMID:24596163
Anoop S, Pallavi KS, Syam K V, Devanand C B, Joyous S Anilkumar TV (2017) Cholecyst derived collagen as an extracellular matrix scaffold graft for the management of corneal injuries in dogs: a report of three cases. Indian J. Vet. Surg (Accepted for publication)
Badylak SF, Gilbert WT (2008) Immune response to biologic scaffold materials. Semin Immunol 20:109–116. https://doi.org/10.1016/j.smim.2007.11.003 PMCID: PMC2605275
Badylak SF, Freytes DO, Gilbert TW (2009) Extracellular matrix as a biological scaffold material: structure and function. Acta Biomater 5(1):1–13. https://doi.org/10.1016/j.actbio.2008.09.013
Balsa IM, Culp WT (2015) Wound care. Vet Clin North Am Small Anim Pract 45(5):1049–1065. https://doi.org/10.1016/j.cvsm.2015.04.009 PMID:26022525
Basha SK, Kumar RVS, Haragopal V, Srilatha C, Sastry TP, Vidyavathi M (2011) Effects of fish scales extracted collagen biocasings on cutaneous wound healing in dogs. Research journal of pharmaceutical, biological and chemical sciences. RJPBCS 2:36–48
Blakeman JM (1983) The skin biopsy. Cam Fam Physician 29:971–974
Brody S, McMahon J, Yao L, O’Briena M, Dockeryc P, Pandit A (2007) The effect of cholecyst-derived extracellular matrix on the phenotypic behaviour of valvular endothelial and valvular interstitial cells. Biomaterials 28:1461–1469. https://doi.org/10.1016/j.biomaterials.2006.11.030 PMID:17174391
Brown EM, Cutshall WD, Hiles MC (2002) A new biomaterial derived from small intestine submucosa and developed into a wound matrix device. Wounds 14(4):150–166
Burugapalli K, Pandit A (2007) Characterisation of tissue response and in vivo degradation of cholecyst–derived extracellular matrix. Biomacromolecules 8:3439–3451. https://doi.org/10.1021/bm700560k PMID:1791899
Burugapalli K, Thapasmuttu A, Chan CYJ, Yao L, Brody S, Kelly LJ, Pandit A (2007) Scaffold with a natural mesh like architecture: Isolation,structural and Invivo characterization. Biomacromolecules 8:928–936. https://doi.org/10.1021/bm061088x PMID:17309297
Burugapalli K, Chan JCY, Kelly JL, Pandit A (2008) Buttressing staples with cholecyst-derived extracellular matrix (CEM) reinforces staple lines in an ex vivo peristaltic inflation model. Obes Surg 18:1418–1423. https://doi.org/10.1007/s11695-008-9518-7 PMID:18459017
Burugapalli K, Chan CYJ, Kelly LJ, Pandit AS (2014) Efficacy of crosslinking on tailoring in vivo biodegradability of fibro-porous decellularized extracellular matrix and restoration of native tissue structure: a quantitative study using stereology methods. Macromol Biosci 14(2):244–256. https://doi.org/10.1002/mabi.201300195 PMID: 24106216
Crapo PM, Gilbert WT, Badylak FS (2011) An overview of tissue and whole organ decellularization processes. Biomaterials 32:3233–3243. https://doi.org/10.1016/j.biomaterials.2011.01.057 PMCID: PMC3084613
Ferrari R, Boracchi P, Stefanello D (2015) Application of hyaluronic acid in the healing of non-experimental open wounds: a pilot study on 12 wounds in 10 client-owned dogs. Vet World:1247–1259. https://doi.org/10.14202/vetworld.2015.1247-1259 PMID:27047026
Jothi NA, Thilagar S, Omar ARS, Kamaruddin MD, Shanthi G, Goh YM, Sabri MY (2007) Effects of biomaterials keratin-gelatin and basic fibroblast growth factor-gelatin composite film on wound healing in dogs. J Vet Malaysia 18(1):21–26
Keane TJ, Londono R, Turner NJ, Badylak SF (2012) Consequences of ineffective decellularization of biologic scaffolds on the host response. Biomaterials 33:1771–1781. https://doi.org/10.1016/j.biomaterials.2011.10.054 PMID:22137126
Khademhosseini A, Vacanti JP, Langer R (2009) Progress in tissue engineering. Sciam 300:64–71. https://doi.org/10.1038/scientificamerican0509-64 PMID:19438051
Malcarney HL, Bonar F, Murrell GA (2005) Early inflammatory reaction after rotator cuff repair with a porcine small intestine submucosal implant. Am J Sports Med 33:907–911. https://doi.org/10.1177/0363546504271500 PMID:15827358
Marquis A, Packer RA, Borgens BR, Duerstock SB (2015) Increase in oxidative stress biomarkers in dogs with ascending–descending myelomalacia following spinal cord injury. J Neurol Sci 353(1–2):63–69. https://doi.org/10.1016/j.jns.2015.04.003 PMID:25912174
Mostow EN, Haraway GD, Dalsing M (2005) Effectiveness of an extracellular matrix graft (OASIS wound matrix) in the treatment of chronic leg ulcers: a randomized clinical trial. J Vasc Surg 41:837–843. https://doi.org/10.1016/j.jvs.2005.01.042 PMID:15886669
Muhamed J, Revi D, Rajan A, Geetha S, Anilkumar TV (2015a) Biocompatibility and Immunophenotypic characterization of a porcine Cholecyst-derived scaffold implanted in rats. Toxicol Pathol 43(4):536–545. https://doi.org/10.1177/0192623314550722 PMID:25318959
Muhamed J, Revi D, Rajan A, Anilkumar TV (2015b) Comparative local immunogenic potential of scaffolds prepared from porcine cholecyst, jejunum, and urinary bladder in rat subcutaneous model. J Biomed Mater Res B Appl Biomater 103(6):1302–1311. https://doi.org/10.1002/jbm.b.33296 PMID:25370716
Nair RS, Ameer JM, Alison MR, Anilkumar TV (2017) A gold nanoparticle coated porcine cholecyst-derived bioscaffold for cardiac tissue engineering. Colloids Surf B: Biointerfaces 157:130–137. https://doi.org/10.1016/j.colsurfb.2017.05.056
Revi D, Vineetha PV, Muhamed J, Rajan A, Anilkumar VT (2013) Porcine cholecyst-derived scaffold promotes full-thickness wound healing in rabbit. J Tissue Engng 4, 1:–17. https://doi.org/10.1177/2041731413518060 PMID:24555014
Revi D, Vineetha VP, Muhamed J, Surendran GC, Rajan A, Kumary TV, Anilkumar TV (2015) Wound healing potential of scaffolds prepared from porcine jejunum and urinary bladder by a non-detergent/enzymatic method. J Biomater Appl 29(9):1218–1212. https://doi.org/10.1177/0885328214560218 PMID:25425562
Revi D, Geetha C, Thekkuveetti IA, Anilkumar TV (2016) Fibroblast-loaded cholecyst-derived scaffold induces faster healing of full thickness burn wound in rabbit. J Biomater Appl 30(7):1036–1048. https://doi.org/10.1177/0885328215615759 PMID:26589297
Schallberger SP, Stanley BJ, Hauptman JG, Steficek BA (2008) Effect of porcine small intestinal submucosa on acute full-thickness wounds in dogs. Vet Surg 37:515–524. https://doi.org/10.1111/j.1532-950X.2008.00398.x PMID:19134100
Slatter D (2002) Textbook of small animal surgery, 3rd edn. Saunders, Philadelphia
Turner NJ, Badylak SF (2015) The use of biologic scaffolds in the treatment of chronic nonhealing wounds. Adv wound care 4(80):490–500. https://doi.org/10.1089/wound.2014.0604 PMCID: PMC4505760
Vacanti JP, Langer R (1993) Tissue engineering. Science 260:920–926. https://doi.org/10.1126/science PMID: 8493529
Zheng MH, Chen J, Kirilak Y, Willers C, Xu J, Wood D (2005) Porcine small intestine submucosa (SIS) is not an acellular collagenous matrix and contains porcine DNA: possible implications in human implantation. J. Biomed. Mater. Res. Part B Appl 73:61–67. https://doi.org/10.1002/jbm.b.30170 PMID:15736287
Acknowledgements
The authors received funding from Kerala Science Technology and Environment Committee (No. 1275/2014/KSCSTE). The authors would also like to thank the Kerala Veterinary and Animal Sciences University for providing facilities to do this research work.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed: approval (No. AD/12/41/MVM/2014/SR) of the Institutional Animal Ethics Committee at the College of Veterinary and Animal Sciences, Mannuthy.
“All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.”
Conflict of interest
The authors did not declare any conflict of interests.
Rights and permissions
About this article
Cite this article
Karthika, S., Anoop, S., Devanand, C.B. et al. A porcine-cholecyst-derived scaffold for treating full thickness lacerated skin wounds in dogs. Vet Res Commun 42, 233–242 (2018). https://doi.org/10.1007/s11259-018-9731-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11259-018-9731-3