EXPERIMENTAL ANIMAL MODELS IN DIABETIC WOUND HEALING: AN OVERVIEW

Muhammad Hafizh Abiyyu Fathin Fawwazi; Farida Hayati; Arba Pramundita Ramadani; Lutfi Chabib; Arief Rahman Hakim

doi:10.46903/gjms/22.04.1536

EXPERIMENTAL ANIMAL MODELS IN DIABETIC WOUND HEALING: AN OVERVIEW

Muhammad Hafizh Abiyyu Fathin Fawwazi, Farida Hayati, Arba Pramundita Ramadani, Lutfi Chabib, Arief Rahman Hakim

Abstract

Diabetes mellitus (DM) is one of the factors that affects the wound healing process associated with elevated blood glucose. Wound healing in diabetics is impaired due to the inhibition of cell proliferation and collagen formation. This condition presents a challenge to diabetic wound healing. Restrictions on experiments directly involving humans due to ethical concerns are another challenge. Therefore, the use of experimental animals is one of the options to study diabetic wound healing because they have similarities with humans. Studies on the development of animal models in the diabetic wound healing process, from the cellular level to advanced biochemistry, have increased significantly in the last few decades. These efforts were made to improve clinical practice. The following literature review describes the advantages and disadvantages of animal models and induction methods. It is expected to inform the development of animal models for diabetic wound healing.

Keywords

Diabetic Mellitus; Diabetic wounds; Experimental animals; Wound healing; Similarities with humans.

Full Text:

PDF

References

Bekele F, Chelkeba L. Amputation rate of diabetic foot ulcer and associated factors in diabetes mellitus patients admitted to Nekemte referral hospital, western Ethiopia: prospective observational study. J Foot Ankle Res. 2020;13(1):65. https://doi.org/10.1186/s13047-020-00433-9

Grada A, Mervis J, Falanga V. Research techniques made simple: animal models of wound healing. J Invest Dermatol. 2018;138(10):2095-105.e1. https://doi.org/10.1016/j.jid.2018.08.005

Meyers DS, Andrade TAM, Caetano GF, Guimaraes FR, Leite MN, Leite SN, et al. Experimental models and methods for cutaneous wound healing assessment. Int J Exp Pathol. 2020;101(1-2):21-37. https://doi.org/10.1111/iep.12346

Swindle MM, Makin A, Herron AJ, Clubb FJ, Frazier KS. Swine as models in biomedical research and toxicology testing. Vet Pathol. 2012;49(2):344-56. https://doi.org/10.1177/0300985811402846

Darniwa AV, Cahyanto T, Hidayah SN. Effect of mango leaf shoot extract (Mangifera indica L.) on zebrafish (Danio rerio) cell regeneration induced by hyperglycemia. 2021;15. https://doi.org/10.17977/um061v5i22021p43-57

Cho H, Blatchley MR, Duh EJ, Gerecht S. Acellular and cellular approaches to improve diabetic wound healing. Adv Drug Deliv Rev. 2019;146:267-88. https://doi.org/10.1016/j.addr.2018.07.019

Spampinato SF, Caruso GI, De Pasquale R, Sortino MA, Merlo S. The treatment of impaired wound healing in diabetes: looking among old drugs. Pharmaceuticals. 2020;13(4):60. https://doi.org/10.3390/ph13040060

Sanapalli BKR, Yele V, Singh MK, Thaggikuppe Krishnamurthy P, Karri VVSR. Preclinical models of diabetic wound healing: a critical review. Biomed Pharmacother. 2021;142:111946. https://doi.org/10.1016/j.biopha.2021.111946

Bryda EC. The mighty mouse: the impact of rodent on advances in biomedical research. Mo Med. 2013;110(3):207-11.

Burmeister DM, Supp DM, Clark RA, Tredget EE, Powell HM, Enkhbaatar P, et al. Advantages and disadvantages of using small and large animals in burn research: proceedings of the 2021 research special interest group. J Burn Care Res. 2022;43(5):1032-41. https://doi.org/10.1093/jbcr/irac091

Chen JS, Longaker MT, Gurtner GC. Murine models of human wound healing. In: Gourdie RG, Myers TA, editors. Wound regeneration and repair [Internet]. Totowa, NJ: Humana Press; 2013. p. 265-74. https://doi.org/10.1007/978-1-62703-505-7_15

Chouhan D, Das P, Thatikonda N, Nandi SK, Hedhammar M, Mandal BB. Silkworm silk matrices coated with functionalized spider silk accelerate healing of diabetic wounds. ACS Biomater Sci Eng. 2019;5(7):3537-48. https://doi.org/10.1021/acsbiomaterials.9b00514

Jara N, Cifuentes M, Martínez F, González-Chavarría I, Salazar K, Ferrada L, et al. Vitamin C deficiency reduces neurogenesis and proliferation in the SVZ and lateral ventricle extensions of the young guinea pig brain. Antioxidants (Basel). 2022;11(10):2030. https://doi.org/10.3390/antiox11102030

Seaton M, Hocking A, Gibran NS. Porcine models of cutaneous wound healing. ILAR J. 2015;56(1):127-38. https://doi.org/10.1093/ilar/ilv016

Wilhelm KP, Wilhelm D, Bielfeldt S. Models of wound healing: an emphasis on clinical studies. Skin Res Technol. 2017;23(1):3-12. https://doi.org/10.1111/srt.12317

Hu Q, Chai J, Hu S, Fan J, Wang H, Ma L, et al. Development of an animal model for burn-blast combined injury and cardiopulmonary system changes in the early shock stage. Indian J Surg. 2015;77(S3):977–84. https://doi.org/10.1007/s12262-014-1095-5

Richardson R, Slanchev K, Kraus C, Knyphausen P, Eming S, Hammerschmidt M. Adult zebrafish as a model system for cutaneous wound-healing research. J Invest Dermatol. 2013;133(6):1655–65. https://doi.org/10.1038/jid.2013.16

Wibowo I, Utami N, Anggraeni T, Barlian A, Putra RE, Indriani AD, et al. Propolis can improve caudal fin regeneration in zebrafish (Danio rerio) induced by the combined administration of alloxan and glucose. Zebrafish. 2021;18(4):274–81. https://doi.org/10.1089/zeb.2020.1969

Jung EC, Maibach HI. Animal models for percutaneous absorption. J Appl Toxicol. 2014;35(1):1–10. https://doi.org/10.1002/jat.3004

Lodhi S, Singhai AK. Wound healing effect of flavonoid rich fraction and luteolin isolated from Martynia annua Linn. on streptozotocin-induced diabetic rats. Asian Pac J Trop Med. 2013;6(4):253–9. https://doi.org/10.1016/S1995-7645(13)60053-X

Cheng KY, Lin ZH, Cheng YP, Chiu HY, Yeh NL, Wu TK, et al. Wound healing in streptozotocin-induced diabetic rats using atmospheric-pressure argon plasma jet. Sci Rep. 2018;8(1):12214. https://doi.org/10.1038/s41598-018-30597-1

Shao Y, Dang M, Lin Y, Xue F. Evaluation of wound healing activity of plumbagin in diabetic rats. Life Sci. 2019;231:116422. https://doi.org/10.1016/j.lfs.2019.04.048

Yadav JP, Patel DK, Dubey NK, Mishra MK, Verma A, Grishina M, et al. Wound healing and antioxidant potential of Neolamarckia cadamba in streptozotocin-nicotinamide-induced diabetic rats. Phytomedicine Plus. 2022;2(2):100274. https://doi.org/10.1016/j.phyplu.2022.100274

Chen LY, Cheng HL, Kuan YH, Liang TJ, Chao YY, Lin HC. Therapeutic potential of luteolin on impaired wound healing in streptozotocin-induced rats. Biomedicines. 2021;9(7):761. https://doi.org/10.3390/biomedicines9070761

Al-Romaima A, Guan X, Qin X, Liao Y, Qin G, Tang S, et al. Topical application of Chinese formula Yeliangen promotes wound healing in streptozotocin-induced diabetic rats. J Diabetes Res. 2022;2022:1–14. https://doi.org/10.1155/2022/1193392

Bardaa S, Makni K, Boudaouara O, Bardaa T, Ktari N, Hachicha S, et al. Development and evaluation of the wound healing effect of a novel topical cream formula based on Ginkgo biloba extract on wounds in diabetic rats. Biomed Res Int. 2021;2021:1–12. https://doi.org/10.1155/2021/6474706

Zomer HD, Trentin AG. Skin wound healing in humans and mice: Challenges in translational research. J Dermatol Sci. 2018;90(1):3–12. https://doi.org/10.1016/j.jdermsci.2017.12.009

Borges PA, Waclawiak I, Georgii JL, Fraga-Junior V da S, Barros JF, Lemos FS, et al. Adenosine diphosphate improves wound healing in diabetic mice through P2Y12 receptor activation. Front Immunol. 2021;12:651740. https://doi.org/10.3389/fimmu.2021.651740

Nguyen VT, Farman N, Palacios-Ramirez R, Sbeih M, Behar-Cohen F, Aractingi S, et al. Cutaneous wound healing in diabetic mice is improved by topical mineralocorticoid receptor blockade. J Invest Dermatol. 2019;140(1):223-34.e7. https://doi.org/10.1016/j.jid.2019.04.030

Fang L, Wu H, Li X, Fang J, Zhu Y. Improvement of skin wound healing for diabetic mice with thermosensitive hydrogel combined with insulin injection. Int J Endocrinol. 2022;2022:1-10. https://doi.org/10.1155/2022/7847011

Mazumdar S, Ghosh AK, Dinda M, Das AK, Das S, Jana K, et al. Evaluation of wound healing activity of ethanol extract of Annona reticulata L. leaf both in vitro and in diabetic mice model. J Tradit Complement Med. 2021;11(1):27-37. https://doi.org/10.1016/j.jtcme.2019.12.001

Zhao M, Zhou J, Chen YH, Yuan L, Yuan MM, Zhang XQ, et al. Folic acid promotes wound healing in diabetic mice by suppression of oxidative stress. J Nutr Sci Vitaminol (Tokyo). 2018;64(1):26-33. https://doi.org/10.3177/jnsv.64.26

Singh A, Singh PK, Singh RK. Antidiabetic and wound healing activity of Catharanthus roseus L. in streptozotocin-induced diabetic mice. Am J Phytomedicine Clin Ther. 2014;2(6):686-92.

Sutthammikorn N, Supajatura V, Yue H, Takahashi M, Chansakaow S, Nakano N, et al. Topical Gynura procumbens as a novel therapeutic improves wound healing in diabetic mice. Plants. 2021;10(6):1122. https://doi.org/10.3390/plants10061122

He W, Yao Z, Huang Y, Luo G, Wu J. A biological membrane-based novel excisional wound-splinting model in mice (with video). Burns Trauma. 2014;2(4):196. https://doi.org/10.4103/2321-3868.143625

Ren HT, Hu H, Li Y, Jiang HF, Hu XL, Han CM. Endostatin inhibits hypertrophic scarring in a rabbit ear model. J Zhejiang Univ Sci B. 2013;14(3):224-30. https://doi.org/10.1631/jzus.B1200077

Chouhan D, Janani G, Chakraborty B, Nandi SK, Mandal BB. Functionalized PVA silk blended nanofibrous mats promote diabetic wound healing via regulation of extracellular matrix and tissue remodelling. J Tissue Eng Regen Med. 2018;12(3):e2581. https://doi.org/10.1002/term.2581

Masood N, Ahmed R, Tariq M, Ahmed Z, Masoud MS, Ali I, et al. Silver nanoparticle impregnated chitosan-PEG hydrogel enhances wound healing in diabetes-induced rabbits. Int J Pharm. 2019;559:23-36. https://doi.org/10.1016/j.ijpharm.2019.01.019

Pradhan Nabzdyk L, Kuchibhotla S, Guthrie P, Chun M, Auster ME, Nabzdyk C, et al. Expression of neuropeptides and cytokines in a rabbit model of diabetic neuroischemic wound healing. J Vasc Surg. 2013;58(3):766-75.e12. https://doi.org/10.1016/j.jvs.2012.11.095

Rosyidul M, Nasution TH, Andarini S. Pengaruh ekstrak daun kersen (Muntingia calabura) terhadap derajat eritema pada proses inflamasi marmut (Cavia porcellus). J Ilmu Keperawatan. 2013;1(2).

Kusmayani KN, Warditha AAGJ, Berata IK. Aktivitas angiogenesis gel extract biji cacao pada penyembuhan luka insisi gusi marmut. Bul Vet Udayana. 2022;14(3):295. https://doi.org/10.24843/bulvet.2022.v14.i03.p14

Mohamed NAH, Mokhtar RH, Al-Ani IM, Ayob A, Misran M. Improved skin wound healing activity of insulin cream as evidenced from the morphological evaluation in guinea pigs. Makara J Health Res. 2018;22(2):in-press. https://doi.org/10.7454/msk.v22i2.9714

Miladiyah I, Prabowo BR. Ethanolic extract of Anredera cordifolia (Ten.) Steenis leaves improved wound healing in guinea pigs. Universa Med. 2012;31(1).

Tippaya K, Ngasaman R, Chukiatsiri K. The efficiency of herbal on blood clotting and wound healing of ear notched pigs. Thai J Vet Med. 2021;51(3):481-7. https://doi.org/10.56808/2985-1130.3143

Irons RF, Cahill KW, Rattigan DA, Marcotte JH, Fromer MW, Chang S, et al. Acceleration of diabetic wound healing with adipose-derived stem cells, endothelial-differentiated stem cells, and topical conditioned medium therapy in a swine model. J Vasc Surg. 2018;68(6 Suppl):115S-25S. https://doi.org/10.1016/j.jvs.2018.01.065

James I, Bourne D, Silva M, Havis E, Albright K, Zhang L, et al. Adipose stem cells enhance excisional wound healing in a porcine model. J Surg Res. 2018;229:243-53. https://doi.org/10.1016/j.jss.2018.03.068

Abu-Seida AM. Effect of propolis on experimental cutaneous wound healing in dogs. Vet Med Int. 2015;2015:1-4. https://doi.org/10.1155/2015/672643

Teame T, Zhang Z, Ran C, Zhang H, Yang Y, Ding Q, et al. The use of zebrafish (Danio rerio) as biomedical models. Anim Front. 2019;9(3):68-77. https://doi.org/10.1093/af/vfz020

Holtzman NG, Iovine MK, Liang JO, Morris J. Learning to fish with genetics: A primer on the vertebrate model Danio rerio. Genetics. 2016;203(3):1069-89. https://doi.org/10.1534/genetics.116.190843

Yuniarto A, Sukandar EY, Fidrianny I, Adnyana IK. Aplikasi zebrafish (Danio rerio) pada beberapa model penyakit eksperimental. MPI Media Pharm Indones. 2017;1(3):116-26. https://doi.org/10.24123/mpi.v1i3.215

Sarras MP, Leontovich AA, Olsen AS, Intine RV. Impaired tissue regeneration corresponds with altered expression of developmental genes that persists in the metabolic memory state of diabetic zebrafish: Gene expression analysis of diabetic zebrafish. Wound Repair Regen. 2013;21(2):320-8. https://doi.org/10.1111/wrr.12027

Azevedo AS, Sousa S, Jacinto A, Saúde L. An amputation resets positional information to a proximal identity in the regenerating zebrafish caudal fin. BMC Dev Biol. 2012;12:24. https://doi.org/10.1186/1471-213X-12-24

Tripathi V, Verma J. Different models used to induce diabetes: A comprehensive review. Int J Pharm Pharm Sci. 2014;6(6).

DOI: https://doi.org/10.46903/gjms/22.04.1536