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Manuscript ID : JAPAD-2301-1211 (R1) Visit : 52 Page: 65 - 82

Article Type: Original Research

The healing effect of earthworm’s hydro-alcoholic body extract on skin wound in goldfish (Carassius auratus gibelio)

Subject Areas :

Mehran  Arabi 1 (Department of Animal Sciences, Faculty of Basic Sciences, Shahrekord University, ُShahrekord, Iran.)
AliReza  ShamsAbadi 2 (Department of Animal Sciences, Faculty of Basic Sciences, Shahrekord University, Shahrekord, Iran.)

Received: 2023-01-20 Accepted : 2023-02-27 Published : 2023-04-21

Keywords: fish, Earthworm, Wound,

Abstract :

Background & aim: Wound healing is a complex programmed sequence of cellular and molecular processes. The objective of the present study was to evaluate the ability of earthworm’s hydro-alcoholic body extract (EBE) to heal the experimental skin wound in goldfish (Carassius auratus gibelio).Materials and Methods: Fish (independent triplicate, 14/group), for 14 days, were divided into 5 groups 1) negative control (Unwounded); 2) pseudo-control (sham): wound treated with EBE carrier (mixture of castor oil and white vaseline); 3) Positive control: wound treated with sodium phenytoin 1%; 4) 1 mg/gr EBE-treated wound, 5) 10 mg/gr EBE-treated wound. In this study, macroscopic and microscopic evaluations and collagen turnover (Hydroxyproline content) in the skin, along with determination of lysozyme activity in blood sera were carried out. Results: In fish in group 4 (1 mg/gr EBE-treated wound), an increase in the epithelium diameter, good presence and appropriate synthesis of collagen with and low edema in dermis; increased hydroxyproline content; and elevated blood lysozyme activity were observed comparing to other groups.Conclusion: Our results revealed that application of 1 mg/gr EBE might be as an effective medicinal material in the process of animal wound healing particularly in aquatics.

References:


  1. Diegelmann RF, Evans MC. Wound healing: and overview of acute, fibrotic and delayed healing. Frontiers in Bioscience. 2004; 9(1-3): 283-9.
    2.
  2. Lux CN. Wound healing in animals: a review of physiology and clinical evaluation. Veterinary Dermatology. 2022; 33(1); 91-e27.
    3.
  3. Barchitta M, Maugeri A, Favara G, San Lio RM, Evola, G., Agodi A, et al. Nutrition and Wound Healing: An Overview Focusing on the Beneficial Effects of Curcumin. International Journal of Molecular Sciences. 2019; 20: 1119.
    4.
  4. Fontenot DK, Neiffer DL. Wound management in teleost fish: biology of the healing process, evaluation, and treatment. Veterinary Clinics of North America: Exotic Animal Practice. 2004; 7: 57-86.
    5.
  5. Le Guellec D, Morvan-Dubois G, Sire J. Skin development in bony fish with particular emphasis on collagen deposition in the dermis of the zebrafish (Danio rerio). International Journal of Developmental Biology. 2004; 48(2-3): 217-31.
    6.
  6. Ángeles Esteban M. An overview of the immunological defenses in fish skin. ISRN Immunology. 2012; 2012: 29.
    7.
  7. Richardson R, Slanchev K, Kraus C, Knyphausen P, Eming S, Hammerschmidt M. Adult zebrafish as a model system for cutaneous wound healing research. Journal of Investigative Dermatology. 2013; 133(6): 1655-65.
    8.
  8. Caldwell MD. Bacteria and antibiotics in wound healing. Surgical Clinics of North America. 2020; 100: 757-76.
    9.
  9. Halver JE. The role of ascorbic acid in fish disease and tissue repair. Bulletin of the Japanese Society for the Science of Fish. 1972; 38: 79-92.
    10.
  10. Hasanabadizadeh Z, Moradlou AAMH, Rasoul G, Rostami HAK, Narges S. The effects of vitamins injection (A, C, A+C and AD3E) on wound healing process and some hematological response in common carp, Cyprinus carpio. The Journal of Agriculture and Natural Resources Sciences. 2008; 15(6): 117-24.
    11.
  11. Lunder T, Sorum H, Holstad G, Steigerwalt AG, Mowinckel P, Brenner DJ. Phenotypic and genotypic characterization of Vibrio viscosus sp. Nov. and Vibrio wodanis sp. Nov. isolated from Atlantic salmon (Salmo salar) with winter ulcer. International Journal of Systematic and Evolutionary Microbiology. 2000; 50: 427-50.
    12.
  12. Wahli T, Verlhac V, Girling P, Gabaudan J, Aebischer C. Influence of dietary vitamin C on the wound healing process in rainbow trout (Oncorhynchus mykiss). Aquaculture. 2003; 225: 371-86.
    13.
  13. Nematollahi A, Bigham AS, Karimi I, Abbasi F. Reactions of goldfish (Carassius auratus) to three suture patterns following full thickness skin incisions. Research in Veterinary Science. 2010; 89(3): 451-4.
    14.
  14. Shaw J, Hughes CM, Lagan KM, Bell PM. The clinical effect of topical phenytoin wound healing: a systematic review. British Journal of Dermatology. 2007; 157(5): 997-1004.
    15.
  15. Vijayasingham SM, Dykes PJ, Marks R. Phenytoin has little effect on in-vitro models of wound healing. British Journal of Dermatology. 1991; 125: 136-139.
    16.
  16. Pereira, C.A.; Alchorne Ade, O. Assessment of the effect of phenytoin on
    17.

 

cutaneous healing from excision of melanocytic nevi on the face and on the back. BMC Dermatology. 2010; 10: 7.

  1. Prasad S, Prakash A, Patel S, Lunawat A, Mahore D. A comparative analysis of the efficacy of topical phenytoin with conventional wound dressing in healing of diabetic foot ulcers. International Surgery Journal. 2017; 4(4): 1389-1393.
    2.
  2. Heydari S, Arabi, M, Nematullahi A, Karimi E, Bigham Sadiq A. Comparative effects of earthworm body extract and sodium phenytoin on suture wound healing in goldfish Carassius auratus. Cells and tissues. 2015 Mar 1;5(4):361-8.
    3.
  3. Liu E, Gao H, Zhao Y, Pang Y, Yao Y, Yang Z, et al. The potential application of natural products in cutaneous wound healing: A review of preclinical evidence. Frontiers in Pharmacology. 2022; 13: 900439.
    4.
  4. Vitale S, Colanero S, Placidi M, Di Emidio G, Tatone C, Amicarelli F. Phytochemistry and Biological Activity of Medicinal Plants in Wound Healing: An Overview of Current Research. Molecules. 2022; 27(11): 3566.
    5.
  5. Cooper EL, Hrženjak T, Grdiša M. Alternative source of fibrinolytic, anticoagulative, antimicrobial and anticancer molecules. International Journal of Immunopathology and Pharmacology. 2004; 17: 237-44.
    6.
  6. Ahmed N, Al-Mutairi KA. Earthworms Effect on Microbial Population and Soil Fertility as Well as Their Interaction with Agriculture Practices. Sustainability. 2022; 14: 7803.
    7.
  7. Grdiša M, Gršić K, Grdiša MD. Earthworms-role in soil fertility to the use in medicine and as a food. Invertebrate Servival Journal. 2013; 10(1): 38-45.
    8.
  8. Cooper, E.L., Balamurugan, M., Huang, C.Y., Tsao, C.R., Heredia, J, Tommaseo-Ponzetta M, et al. Earthworms dilong: Ancient, inexpensive, noncontroversial models my help clarify approaches to integrated medicine emphasizing neuroimmune systems. Evidence-Based Complementary and Alternative Medicine. 2012; 2012: 164152.
    9.
  9. Prakash M, Balamurugan M, Parthasarathi K, Gunasekaran G, Cooper EL, Ranganathan LS. Anti-ulceral and anti-oxidative properties of earthworm paste of Lampito mauritii, Kinberg on Rattus norvegicus. European Review for Medical and Pharmacological Sciences. 2007; 11(1): 9-15.
    10.
  10. Balamurugan M, Parthasarathi K, Cooper EL, Ranganathan LS. Hypothetical mode of action of earthworm extract with hepatoprotective and antioxidant properties. Journal of Zhejiang University- Science B. 2008; 9: 141-7.
    11.
  11. Mira G, Terezija H. Glycolipoprotein extract of Eisenia foetida (G-90): A source of biological active molecules. European Journal of Soil Biology. 2007; 43: 104-9.
    12.
  12. Grdiša M, Popović M, Hrženjak T. Stimulation of growth factor synthesis in skin wounds using tissue extract (G-90) from the earthworm Eisenia foetida. Cell Biochemistry and function. 2004; 22: 373-8.
    13.
  13. Matausic-Pisl M, Cupic H, Kasuba V, Mikecin AM, Grdisa M. Tissue Extract from Eisenia foetida as a Wound-Healing Agent. European Review for Medical and Pharmacological Sciences. 2010; 14(3): 177-84.
    14.
  14. Grdisa M, Popovic M, Hrzenjak T. Glycolipoprotein extract (G-90) from earthworm Eisenia foetida exerts some antioxidative activity. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology. 2001; 128(4): 821-25.
    15.
  15. Hrzenjak T, Hrzenjak M, Kasuba V, Efenberger-Marinculić P, Levanat S. A new source of biologically active compounds-earthworm tissue (Eisenia fetida, Lumbricus rubelus). Comparative Biochemistry and


 

Physiology Part B, Biochemistry & Molecular Biology. 1992; 102(3); 441-447.

  1. Woessner J. The determination of hydroxyproline in tissue and protein samples containing small proportions of this amino acid. Archives of Biochemistry and Biophysics. 1961; 93: 440-7.
    2.
  2. Lie O, Evensen O, Sorensen A, Froysadal E. Study on lysozyme activity in some fish species. Diseases of Aquatic Organisms. 1989; 6: 1-5.
    3.
  3. Balamurugan M, Parthasarathi K, Cooper EL, Ranganathan LS. Earthworm paste (Lampito mauritii, Kinberg) alters inflammatory, oxidative, haematological and serum biochemical indices of inflamed rat. European Review for Medical and Pharmacological Sciences. 2007; 11: 77-90.
    4.
  4. Han CK, Kuo WW, Shen CY, Chen TS, Pai P, Tsai CH, et al. Dilong prevents the high-KCl cardioplegic solution administration-induced apoptosis in H9c2 cardiomyoblast cells mediated by MEK. American Journal of Chinese Medicine. 2014; 42: 1507-19.
    5.
  5. Wei S, Yin X, Kou Y, Jiang B. Lumbricus Extract Promotes the Regeneration of Injured Peripheral Nerve in Rats. Journal of Ethnopharmacology. 2009; 123(1): 51-4.
    6.
  6. Bigham-Sadegh A, Arabi M, Karimi E, Karimi I, Oryan A. Tendon Injury Healing with G-90 in a Rabbit Model: Biomechanical and Histopathological Evaluation. Veterinarski Arhiv. 2016; 86(3): 407-20.
    7.
  7. Bo SP, Pan YJ. Clinical Analysis of Earthworm Sugar Extract Combined with Local Oxygen Therapy to Promote Chronic Wound Healing in 35 Cases. China Practical Medical. 2012; 7(20): 169-70 (Chinese).
    8.
  8. Wang D, Ruan Z, Zhang R, Wang X, Wang R, Tang Z. Effect of Earthworm on Wound Healing: A Systematic Review and Meta-Analysis. Frontiers in Pharmacology. 2021; 12: 691742.
    9.
  9. Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson J. Molecular Biology of the Cells. NY, London: Garland Publishing; 1989.
    10.
  10. Coşkun S, Güleç EG, Balabanli B, Acartürk F. Effects of epidermal growth factor on lipid peroxidation and nitric oxide levels in oral mucosal ulcer healing: a time-course study. Surgery Today. 2007; 37(7): 570-4.
    11.
  11. Altavilla D, Galeano M, Bitto A, Minutoli L, Squadrito G, Seminara P, et al. Lipid peroxidation inhibition by raxofelast improves angiogenesis and wound healing in experimental burn wounds. Shock. 2005; 24(1): 85-91.
    12.
  12. Chang YM, Shih YT, Chen YS, Liu CL, Fang WK, Tasi CH, et al. Schwann Cell Migration Induced by Earthworm Extract via Activation of PAs and MMP2/9 Mediated through ERK1/2 and p38. Evidence-Based Complementary and Alternative Medicine. 2011; 2011: 395458.
    13.
  13. Song S, Wang Y, Ji K, Liang H, Ji A. Effect of earthworm active protein on fibroblast proliferation and its mechanism. Pharmaceutical Biology. 2016: 54(4): 732-739.
    14.
  14. Mathur A, Verma SK, Bhat R, Singh SK, Prakash A, GBKS Prasad, et al. Antimicrobial Activity of Earthworm Extracts. Journal of Chemical and Pharmaceutical Research. 2010; 2(4): 364-70.
    15.
  15. Bhorgin AJ, Uma K. Antimicrobial activity of Earthworm Powder (Lampito mauritii). International Journal of Current Microbiology and Applied Sciences. 2014; 3(1): 437-43.
    16.
  16. Punu GP, Ansari A, Jaikishun S, Seecharran D. Effect of Earthworm (Perionyx excavatus) Powder on Selected Bacteria and Fungi. Journal of Advances in Biology & Biotechnology. 2016; 5(2): 1-15.
    17.
  17. He M, Xie WQ, Cheng G, Li WP, Yu DJ, Jin HF, et al. The therapeutic effects of
    18.

 

earthworm extract on deep second-degree burn wound healing. Annals of Palliative Medicine. 2021; 10(3): 2869-79.

  1. Qiu L, Jin XQ, Xiang DL, Fu YX, Tian XF. Study on the collagen constitution of hyperplastic scar in different ages and its influencing factors. Zhonghua Shao Shang Za Zhi. 2003; 19(4): 236-40 (Chinese).
    2.
  2. Gurtner GC, Werner S, Barrandon Y, Longaker MT. Wound repair and regeneration. Nature. 2008; 453: 314-21.
    3.
  3. Reilly DM, Lozano J. Skin collagen through the life stages: Importance for skin health and beauty. Plastic Aesthetic Research. 2021; 8: 2.
    4.
  4. Song YH, Zhu YT, Ding J, Zhou FY, Xue JX, Hee J, et al. Distribution of fibroblast growth factors and their roles in skin fibroblast cell migration. Molecular Medicine Reports. 2016; 14(4): 3336-42.
    5.
  5. Anderson DP. Immunostimulants, adjuvants and vaccine carriers in fish, application to aquaculture. Annual Review of Fish Diseases. 1992; 2: 281-307.
    6.
  6. Kozinenko II, Isaeva NM, Balakhnin I. Humoral factors of nonspecific defense of fish. Journal of Ichthyology. 1999; 39: 394-400.
    7.

55. Mock A, Peters G. Lysozyme activity in rainbow trout, Oncorhynchus mykiss (Walbaum), stressed by handing, transport and water pollution. Fish Biology. 1990; 37: 873-85.

_||_

  1. Diegelmann RF, Evans MC. Wound healing: and overview of acute, fibrotic and delayed healing. Frontiers in Bioscience. 2004; 9(1-3): 283-9.
    2.
  2. Lux CN. Wound healing in animals: a review of physiology and clinical evaluation. Veterinary Dermatology. 2022; 33(1); 91-e27.
    3.
  3. Barchitta M, Maugeri A, Favara G, San Lio RM, Evola, G., Agodi A, et al. Nutrition and Wound Healing: An Overview Focusing on the Beneficial Effects of Curcumin. International Journal of Molecular Sciences. 2019; 20: 1119.
    4.
  4. Fontenot DK, Neiffer DL. Wound management in teleost fish: biology of the healing process, evaluation, and treatment. Veterinary Clinics of North America: Exotic Animal Practice. 2004; 7: 57-86.
    5.
  5. Le Guellec D, Morvan-Dubois G, Sire J. Skin development in bony fish with particular emphasis on collagen deposition in the dermis of the zebrafish (Danio rerio). International Journal of Developmental Biology. 2004; 48(2-3): 217-31.
    6.
  6. Ángeles Esteban M. An overview of the immunological defenses in fish skin. ISRN Immunology. 2012; 2012: 29.
    7.
  7. Richardson R, Slanchev K, Kraus C, Knyphausen P, Eming S, Hammerschmidt M. Adult zebrafish as a model system for cutaneous wound healing research. Journal of Investigative Dermatology. 2013; 133(6): 1655-65.
    8.
  8. Caldwell MD. Bacteria and antibiotics in wound healing. Surgical Clinics of North America. 2020; 100: 757-76.
    9.
  9. Halver JE. The role of ascorbic acid in fish disease and tissue repair. Bulletin of the Japanese Society for the Science of Fish. 1972; 38: 79-92.
    10.
  10. Hasanabadizadeh Z, Moradlou AAMH, Rasoul G, Rostami HAK, Narges S. The effects of vitamins injection (A, C, A+C and AD3E) on wound healing process and some hematological response in common carp, Cyprinus carpio. The Journal of Agriculture and Natural Resources Sciences. 2008; 15(6): 117-24.
    11.
  11. Lunder T, Sorum H, Holstad G, Steigerwalt AG, Mowinckel P, Brenner DJ. Phenotypic and genotypic characterization of Vibrio viscosus sp. Nov. and Vibrio wodanis sp. Nov. isolated from Atlantic salmon (Salmo salar) with winter ulcer. International Journal of Systematic and Evolutionary Microbiology. 2000; 50: 427-50.
    12.
  12. Wahli T, Verlhac V, Girling P, Gabaudan J, Aebischer C. Influence of dietary vitamin C on the wound healing process in rainbow trout (Oncorhynchus mykiss). Aquaculture. 2003; 225: 371-86.
    13.
  13. Nematollahi A, Bigham AS, Karimi I, Abbasi F. Reactions of goldfish (Carassius auratus) to three suture patterns following full thickness skin incisions. Research in Veterinary Science. 2010; 89(3): 451-4.
    14.
  14. Shaw J, Hughes CM, Lagan KM, Bell PM. The clinical effect of topical phenytoin wound healing: a systematic review. British Journal of Dermatology. 2007; 157(5): 997-1004.
    15.
  15. Vijayasingham SM, Dykes PJ, Marks R. Phenytoin has little effect on in-vitro models of wound healing. British Journal of Dermatology. 1991; 125: 136-139.
    16.
  16. Pereira, C.A.; Alchorne Ade, O. Assessment of the effect of phenytoin on
    17.

 

cutaneous healing from excision of melanocytic nevi on the face and on the back. BMC Dermatology. 2010; 10: 7.

  1. Prasad S, Prakash A, Patel S, Lunawat A, Mahore D. A comparative analysis of the efficacy of topical phenytoin with conventional wound dressing in healing of diabetic foot ulcers. International Surgery Journal. 2017; 4(4): 1389-1393.
    2.
  2. Heydari S, Arabi, M, Nematullahi A, Karimi E, Bigham Sadiq A. Comparative effects of earthworm body extract and sodium phenytoin on suture wound healing in goldfish Carassius auratus. Cells and tissues. 2015 Mar 1;5(4):361-8.
    3.
  3. Liu E, Gao H, Zhao Y, Pang Y, Yao Y, Yang Z, et al. The potential application of natural products in cutaneous wound healing: A review of preclinical evidence. Frontiers in Pharmacology. 2022; 13: 900439.
    4.
  4. Vitale S, Colanero S, Placidi M, Di Emidio G, Tatone C, Amicarelli F. Phytochemistry and Biological Activity of Medicinal Plants in Wound Healing: An Overview of Current Research. Molecules. 2022; 27(11): 3566.
    5.
  5. Cooper EL, Hrženjak T, Grdiša M. Alternative source of fibrinolytic, anticoagulative, antimicrobial and anticancer molecules. International Journal of Immunopathology and Pharmacology. 2004; 17: 237-44.
    6.
  6. Ahmed N, Al-Mutairi KA. Earthworms Effect on Microbial Population and Soil Fertility as Well as Their Interaction with Agriculture Practices. Sustainability. 2022; 14: 7803.
    7.
  7. Grdiša M, Gršić K, Grdiša MD. Earthworms-role in soil fertility to the use in medicine and as a food. Invertebrate Servival Journal. 2013; 10(1): 38-45.
    8.
  8. Cooper, E.L., Balamurugan, M., Huang, C.Y., Tsao, C.R., Heredia, J, Tommaseo-Ponzetta M, et al. Earthworms dilong: Ancient, inexpensive, noncontroversial models my help clarify approaches to integrated medicine emphasizing neuroimmune systems. Evidence-Based Complementary and Alternative Medicine. 2012; 2012: 164152.
    9.
  9. Prakash M, Balamurugan M, Parthasarathi K, Gunasekaran G, Cooper EL, Ranganathan LS. Anti-ulceral and anti-oxidative properties of earthworm paste of Lampito mauritii, Kinberg on Rattus norvegicus. European Review for Medical and Pharmacological Sciences. 2007; 11(1): 9-15.
    10.
  10. Balamurugan M, Parthasarathi K, Cooper EL, Ranganathan LS. Hypothetical mode of action of earthworm extract with hepatoprotective and antioxidant properties. Journal of Zhejiang University- Science B. 2008; 9: 141-7.
    11.
  11. Mira G, Terezija H. Glycolipoprotein extract of Eisenia foetida (G-90): A source of biological active molecules. European Journal of Soil Biology. 2007; 43: 104-9.
    12.
  12. Grdiša M, Popović M, Hrženjak T. Stimulation of growth factor synthesis in skin wounds using tissue extract (G-90) from the earthworm Eisenia foetida. Cell Biochemistry and function. 2004; 22: 373-8.
    13.
  13. Matausic-Pisl M, Cupic H, Kasuba V, Mikecin AM, Grdisa M. Tissue Extract from Eisenia foetida as a Wound-Healing Agent. European Review for Medical and Pharmacological Sciences. 2010; 14(3): 177-84.
    14.
  14. Grdisa M, Popovic M, Hrzenjak T. Glycolipoprotein extract (G-90) from earthworm Eisenia foetida exerts some antioxidative activity. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology. 2001; 128(4): 821-25.
    15.
  15. Hrzenjak T, Hrzenjak M, Kasuba V, Efenberger-Marinculić P, Levanat S. A new source of biologically active compounds-earthworm tissue (Eisenia fetida, Lumbricus rubelus). Comparative Biochemistry and


 

Physiology Part B, Biochemistry & Molecular Biology. 1992; 102(3); 441-447.

  1. Woessner J. The determination of hydroxyproline in tissue and protein samples containing small proportions of this amino acid. Archives of Biochemistry and Biophysics. 1961; 93: 440-7.
    2.
  2. Lie O, Evensen O, Sorensen A, Froysadal E. Study on lysozyme activity in some fish species. Diseases of Aquatic Organisms. 1989; 6: 1-5.
    3.
  3. Balamurugan M, Parthasarathi K, Cooper EL, Ranganathan LS. Earthworm paste (Lampito mauritii, Kinberg) alters inflammatory, oxidative, haematological and serum biochemical indices of inflamed rat. European Review for Medical and Pharmacological Sciences. 2007; 11: 77-90.
    4.
  4. Han CK, Kuo WW, Shen CY, Chen TS, Pai P, Tsai CH, et al. Dilong prevents the high-KCl cardioplegic solution administration-induced apoptosis in H9c2 cardiomyoblast cells mediated by MEK. American Journal of Chinese Medicine. 2014; 42: 1507-19.
    5.
  5. Wei S, Yin X, Kou Y, Jiang B. Lumbricus Extract Promotes the Regeneration of Injured Peripheral Nerve in Rats. Journal of Ethnopharmacology. 2009; 123(1): 51-4.
    6.
  6. Bigham-Sadegh A, Arabi M, Karimi E, Karimi I, Oryan A. Tendon Injury Healing with G-90 in a Rabbit Model: Biomechanical and Histopathological Evaluation. Veterinarski Arhiv. 2016; 86(3): 407-20.
    7.
  7. Bo SP, Pan YJ. Clinical Analysis of Earthworm Sugar Extract Combined with Local Oxygen Therapy to Promote Chronic Wound Healing in 35 Cases. China Practical Medical. 2012; 7(20): 169-70 (Chinese).
    8.
  8. Wang D, Ruan Z, Zhang R, Wang X, Wang R, Tang Z. Effect of Earthworm on Wound Healing: A Systematic Review and Meta-Analysis. Frontiers in Pharmacology. 2021; 12: 691742.
    9.
  9. Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson J. Molecular Biology of the Cells. NY, London: Garland Publishing; 1989.
    10.
  10. Coşkun S, Güleç EG, Balabanli B, Acartürk F. Effects of epidermal growth factor on lipid peroxidation and nitric oxide levels in oral mucosal ulcer healing: a time-course study. Surgery Today. 2007; 37(7): 570-4.
    11.
  11. Altavilla D, Galeano M, Bitto A, Minutoli L, Squadrito G, Seminara P, et al. Lipid peroxidation inhibition by raxofelast improves angiogenesis and wound healing in experimental burn wounds. Shock. 2005; 24(1): 85-91.
    12.
  12. Chang YM, Shih YT, Chen YS, Liu CL, Fang WK, Tasi CH, et al. Schwann Cell Migration Induced by Earthworm Extract via Activation of PAs and MMP2/9 Mediated through ERK1/2 and p38. Evidence-Based Complementary and Alternative Medicine. 2011; 2011: 395458.
    13.
  13. Song S, Wang Y, Ji K, Liang H, Ji A. Effect of earthworm active protein on fibroblast proliferation and its mechanism. Pharmaceutical Biology. 2016: 54(4): 732-739.
    14.
  14. Mathur A, Verma SK, Bhat R, Singh SK, Prakash A, GBKS Prasad, et al. Antimicrobial Activity of Earthworm Extracts. Journal of Chemical and Pharmaceutical Research. 2010; 2(4): 364-70.
    15.
  15. Bhorgin AJ, Uma K. Antimicrobial activity of Earthworm Powder (Lampito mauritii). International Journal of Current Microbiology and Applied Sciences. 2014; 3(1): 437-43.
    16.
  16. Punu GP, Ansari A, Jaikishun S, Seecharran D. Effect of Earthworm (Perionyx excavatus) Powder on Selected Bacteria and Fungi. Journal of Advances in Biology & Biotechnology. 2016; 5(2): 1-15.
    17.
  17. He M, Xie WQ, Cheng G, Li WP, Yu DJ, Jin HF, et al. The therapeutic effects of
    18.

 

earthworm extract on deep second-degree burn wound healing. Annals of Palliative Medicine. 2021; 10(3): 2869-79.

  1. Qiu L, Jin XQ, Xiang DL, Fu YX, Tian XF. Study on the collagen constitution of hyperplastic scar in different ages and its influencing factors. Zhonghua Shao Shang Za Zhi. 2003; 19(4): 236-40 (Chinese).
    2.
  2. Gurtner GC, Werner S, Barrandon Y, Longaker MT. Wound repair and regeneration. Nature. 2008; 453: 314-21.
    3.
  3. Reilly DM, Lozano J. Skin collagen through the life stages: Importance for skin health and beauty. Plastic Aesthetic Research. 2021; 8: 2.
    4.
  4. Song YH, Zhu YT, Ding J, Zhou FY, Xue JX, Hee J, et al. Distribution of fibroblast growth factors and their roles in skin fibroblast cell migration. Molecular Medicine Reports. 2016; 14(4): 3336-42.
    5.
  5. Anderson DP. Immunostimulants, adjuvants and vaccine carriers in fish, application to aquaculture. Annual Review of Fish Diseases. 1992; 2: 281-307.
    6.
  6. Kozinenko II, Isaeva NM, Balakhnin I. Humoral factors of nonspecific defense of fish. Journal of Ichthyology. 1999; 39: 394-400.
    7.

55. Mock A, Peters G. Lysozyme activity in rainbow trout, Oncorhynchus mykiss (Walbaum), stressed by handing, transport and water pollution. Fish Biology. 1990; 37: 873-85.

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