Anti-Leishmanial Effects of a Novel Biocompatible Non-Invasive Nanofibers Containing Royal Jelly and Propolis against Iranian Strain of Leishmania major (MRHO/IR/75/ER): an In-Vitro Study
-
Mohsen Mahmoudi
,
Bita Mehravi
,
Mohammad Shabani
,
Ramtin Hadighi
,
Alireza Badirzadeh
,
Ahmad Dehdast
,
Ghazale Chizari Fard
,
Vahid Pirhajati Mahabadi
,
Sekineh Akbari
,
Fatemeh Tabatabaie
,
Mehdi Mohebali
Abstract
Background: Current medications especially the pentavalent antimonial compounds have been used as the first line treatment of cutaneous leishmaniasis (CL), but they have limitations due to serious side effects such as drug resistance, cardio and nephrotoxicity, and high costs. Hence, the demand to find more usable drugs is evident. Synthesis and development of natural, effective, biocompatible, and harmless compounds against Leishmania major is the principal priority of this study.
Methods: By electrospinning method, a new type of nanofiber were synthesized from royal jelly and propolis with different ratios. Nanofibers were characterized by Scanning Electron Microscope (SEM), Transmission Electron Microscopy (TEM), Thermogravimetric Analysis (TGA), Contact angle, and Fourier-transform infrared spectroscopy (FTIR). The Half-maximal inhibitory concentration (IC50), Half-maximal effective concentration (EC50) and the 50% cytotoxic concentration (CC50) for different concentrations of nanofibers were determined using quantitative calorimetric methods. Inductively coupled plasma-optical emission spectrometry (ICP-OES) and flow cytometry were performed as complementary tests.
Results: The results showed that the proposed formulas provide a new achievement that, despite the significant killing activity on L. major, has negligible cytotoxicity on the host cells. Royal jelly nanofibers have significantly shown the best 72 hours results (IC50= 35 μg/ml and EC50=16.4 μg/ml) and the least cytotoxicity.
Conclusion: This study presents a great challenge to introduce a new low-cost treatment method for CL, accelerate wound healing, and reduce scarring with minimal side effects and biocompatible materials. Royal jelly and propolis nanofibers significantly inhibit the growth of L. major in-vitro.
1. Torres-Guerrero E, Quintanilla-Cedillo MR, Ruiz-Esmenjaud J, Arenas R (2017) Leish¬maniasis: a review. 1(6): 750.
2. Izri A, Bendjaballah-Laliam A, Sereno D, Ak¬houndi M (2021) Updates on geo-graph¬ical dispersion of Leishmania parasites causing cutaneous affections in Algeria. Pathogens. 10(3): 0267.
3. Haldar AK, Sen P, Roy S (2011) Use of an¬timony in the treatment of leishmaniasis: current status and future directions. Mol Biol Int. 2011: 571242.
4. Frézard F, Demicheli C, Ribeiro RR (2009) Pentavalent antimonials: new per-spectives for old drugs. Molecules. 14(7): 2317–2336.
5. Nabas Z, Haddadin MS, Haddadin J, Nazer IK (2014) Chemical composition of roy¬al jelly and effects of synbiotic with two different locally isolated probiotic strains on antioxidant activities. Pol J Food Nutr Sci. 64(3): 171–180.
6 Brudzynski K, Sjaarda C (2015) Honey glycoproteins containing antimicrobial pep-tides, Jelleins of the Major Royal Jelly Pro¬tein 1, are responsible for the cell wall lytic and bactericidal activities of honey. PLoS One. 10(4): e0120238.
7. Gu L, Zeng H, Maeda K (2017) 10-Hy-droxy-2-decenoic acid in royal jelly ex-tract induced both filaggrin and amino ac¬id in a cultured human three-dimen-sion¬al epidermis model. Cosmetics. 4(4): 48.
8. Cornara L, Biagi M, Xiao J, Burlando B (2017) Therapeutic properties of bioac-tive compounds from different honeybee products. Front Pharmacol. 8: 412.
9. Garcia-Amoedo LH, Almeida-Muradian LBd (2007) Physicochemical composition of pure and adulterated royal jelly. Quím. Nova. 30(2): 257–259.
10. Pasupuleti VR, Sammugam L, Ramesh N, Gan SH (2017) Honey, propolis, and roy¬al jelly: a comprehensive review of their biological actions and health bene-fits. Ox¬id Med Cell Longev. 2017: 1259510.
11. Viuda‐Martos M, Ruiz‐Navajas Y, Fer-nán¬dez‐López J, Pérez‐Álvarez J (2008) Func¬tional properties of honey, propolis, and royal jelly. J Food Sci. 73(9): 117–124.
12. Marcucci MC (1995) Propolis: chemical com¬position, biological properties and ther¬apeutic activity. Apidologie. 26(2): 83–99.
13. Huang S, Zhang C-P, Wang K, Li GQ, Hu F-L (2014) Recent advances in the chem¬ical composition of propolis. Molecules. 19(12): 19610–19632.
14. Ratajczak M, Kaminska D, Matuszewska E, Hołderna-Kedzia E, Rogacki J, Matysi¬ak J (2021) Promising antimicrobial prop¬erties of bioactive compounds from dif¬ferent honeybee products. Molecules. 26 (13): 4007.
15. Astrada A, Nakagami G, Jais S, Sanada H (2019) Successful treatment of a dia¬bet-ic foot ulcer with exposed bone using Trig¬ona honey: a case study. J Wound Care. 128.(Sup12): S4–S8.
16. Krupp T, Dos Santos BD, Gama LA, Sil¬va JR, Arrais-Silva WW, de Souza NC, Américo MF, de Souza Souto PC (2019) Natural rubber-propolis membrane im-proves wound healing in second-degree burning model. Int J Biol Macromol. 131: 980–988.
17 Oryan A, Alemzadeh E, Moshiri A (2018) Potential role of propolis in wound heal-ing: Biological properties and thera¬peu-tic activities. Biomed Pharmacother. 98: 469–483.
18. Likitpongpipat N, Sangmaneedet S, Klanrit P, Noisombut R, Krisanaprakornkit S, Chail¬ertvanitkul P (2019) Promotion of dental pulp wound healing in New Zea¬land white rabbits’ teeth by Thai prop¬olis product. J Vet Dent. 36(1): 17–24.
19. Silva-Carvalho R, Baltazar F, Almeida-Aguiar C (2015) Propolis: a complex nat¬ural product with a plethora of bio-logi¬cal activities that can be explored for drug development. Evid Based Complement Alternat Med. 2015: 206439
20. Cai Z, Li F, Rong M, Lin L, Yao Q, Huang Y, Chen Xi, Wang Xia (2019) Novel Na¬nomaterials for Biomedical, Environ¬men¬tal and Energy Applications. Micro-Nano Technologies(MNT). pp. 1–36.
21. Balusamy B, Senthamizhan A, Uyar T (2017) Electrospun nanofibrous mate¬ri-als for wound healing applications. Elec-tro¬spun Materials for Tissue Engineering and Biomedical Applications: Research, De¬sign and Commercialization. pp. 147–177.
22. Wang J, Windbergs M (2017) Functional electrospun fibers for the treatment of hu¬man skin wounds. Eur J Pharm Bio-pharm. 119: 283–299.
23. Joshi VB, Geary SM, Salem AK (2013) Biodegradable particles as vaccine anti-gen delivery systems for stimulating cel-lular immune responses. Hum Vaccin Im¬munother. 9(12): 2584–2590.
24. Haider A, Haider S, Kang I-K (2018) A comprehensive review summarizing the effect of electrospinning parameters and potential applications of nanofibers in bi-omedical and biotechnology. Arab J Chem. 11(8): 1165–1188.
25. Xue J, Wu T, Dai Y, Xia Y (2019) Elec-trospinning and electrospun nanofibers: Methods, materials, and applications. Chem Rev. 119(8): 5298–5415.
26. Lu H, Wang J, Wang T, Zhong J, Bao Y, Hao H (2016) Recent progress on nanostruc¬tures for drug delivery appli¬ca-tions. J Nanomater. 2016: 5762431.
27. Wu J, Zhu YJ, Cao SW, Chen F (2010) Hierachically nanostructured mesopo-rous spheres of calcium silicate hydrate: Sur¬factant‐free sonochemical synthesis and drug‐delivery system with ultrahigh drug‐ loading capacity. Adv Mater. 22(6): 749–753.
28. Purohit G, Sakthivel T, Florence AT (2003) The interaction of cationic dendrons with albumin and their diffusion through cel¬lulose membranes. Int J Pharm. 254(1): 37–41.
29. Mansur HS, Sadahira CM, Souza AN, Man¬sur AA (2008) FTIR spectroscopy char¬acterization of poly (vinyl alcohol) hy¬dro¬gel with different hydrolysis degree and chemically crosslinked with glutaral¬de¬hyde. Mater Sci Eng: C. 28(4): 539–548.
30. Cebi N, Bozkurt F, Yilmaz MT, Sagdic O (2020) An evaluation of FTIR spec¬tros-copy for prediction of royal jelly content in hive products. J Apic Res. 59(2): 146–155.
31. Salam A, Khan MQ, Hassan T, Hassan N, Nazir A, Hussain T, Azeem M, Kim IS (2020) In-vitro assessment of appro¬pri-ate hydrophilic scaffolds by co-electrospin¬ning of poly (1, 4 cyclohexane iso¬sorbide terephthalate)/polyvinyl alcohol. Sci Rep. 10(1): 1–9.
32. Razavizadeh BM, Niazmand R (2020) Char¬acterization of polyamide-6/ propolis blend¬ed electrospun fibers. Heliyon. 6 (8): e04784.
33. Tian H, Yuan L, Wang J, Wu H, Wang H, Xiang A, Ashok B, Rajulu AV (2019) Electrospinning of polyvinyl alcohol into crosslinked nanofibers: an approach to fab¬ricate functional adsorbent for heavy met¬als. J Hazard Mater. 378: 120751.
34. Torabi N, Mohebali M, Shahverdi AR, Re-zayat SM, Edrissian Gh H, Esmaeili J, Charehdar S (2012) Nanogold for the treat¬ment of zoonotic cutaneous leish-man¬ia¬sis caused by Leishmania major (MRHO/ IR/75/ER): An animal trial with methanol ex¬tract of Eucalyptus camaldulensis. JPHS. 1(1): 13–16.
35. Mahmoudi M, Shabani M, Dehdast SA, Saberi S, Elmi T, Chiari Fard G, Tabat-abaie F, Akbari S (2022) The Charac-terization and Antileishmanial Evalu¬a-tion on Leishmania Major with Chitosan/ Zno Bio-Nanocomposite as Drug Delivery Systems. J Nanomed Res. 7(2): 140–149.
36. Farah ME, Maia M, Penha FM, Rodrigues EB (2016) The use of vital dyes during vitreoretinal surgery-chromovitrectomy. Dev Ophthalmol. 55: 365–375.
37. Garcia A, Amaral AF, Azevedo MM, Lopes BS, Alviano CS, Pinheiro AS, Vermelho AB, Rodriguesa IA (2017) Cytotoxicity and anti-Leishmania amazonensis activ¬ity of Citrus sinensis leaf extracts. Pharm Biol. 55(1): 1780–1786.
38. Khademvatan S, Gharavi MJ, Rahim F, Saki J (2011) Miltefosine-induced apop-totic cell death on Leishmania major and L. tropica strains. Korean J Parasi-tol. 49(1): 17–23.
39. Wu Y-W, Sun S-Q, Zhao J, Li Y, Zhou Q (2008) Rapid discrimination of extracts of Chinese propolis and poplar buds by FT-IR and 2D IR correlation spec¬tros-copy. J Mol Struct. 883: 48–54.
40. Rassu G, Cossu M, Langasco R, Carta A, Cavalli R, Giunchedi P, Gavini E (2015) Propolis as lipid bioactive nano-carrier for topical nasal drug delivery. Colloids Surf B Biointerfaces. 136: 908–917.
41. Coates J (2006) Interpretation of infrared spectra, a practical approach, Encyclo¬pe-dia of Analytical Chemistry: Applica-tions, Theory and Instrumentation, pp. 10815–10837.
42. Lazarevska S, Makreski P (2015) Insights into the infrared and Raman spectra of fresh and lyophilized royal jelly and pro-tein degradation IR spectroscopy study during heating. Maced J Chem Chem Eng. 34(1): 87–93.
43. Cebi N, Durak MZ, Toker OS, Sagdic O, Arici M (2016) An evaluation of Fourier transforms infrared spectroscopy method for the classification and discrimination of bovine, porcine and fish gelatins. Food Chem. 190: 1109–1115.
44. Zia M, Mannani R, Mahmoodi M, Bayat M, Mohaghegh F (2009) The effects of alcoholic extract of propolis obtained from Iran bee hives on the growth of Tri¬chophyton mentagrophytis, Tri-chophyton rubrum and Trichophyton verrucosum. J Isfahan Med Sch. 27(95): 232–241.
45. Diba K, Mahmoodi M, Hashemi J (2018) In-vitro activity of Propolis alcoholic ex-tract on opportunistic pathogenic fungi. Int J Res Appl Basic Med Sci. 4(2): 68–73.
46. Hamzeh Pour S, Khodavaisy S, Mahmoudi S, Vaziri S, Soltan Dallal MM, Oliya S, Getso M, Rezaie S (2020) The effect of royal jelly and propolis alone and in com¬bination on inhibition of Aspergillus par¬asiticus growth, aflatoxin production, and aflR gene expression. J Food Saf. 40(4): e12815.
47. Mahmoudi M, Mohebali M, Irandoust H, Hejazi S, Abdoli H, Shirani-Bidabadi L, Charehdar S, Shareghi N, Akhavan AA (2009) Therapeutic effects of propolis hy¬droalcoholic extract in the treatment of cutaneous leishmaniasis in Balb/c. J Sch Public Health Inst Public Health Res. 6 (3 and 4): 19–26.
48. Goonoo N, Laetitia Huët MA, Chummun I, Karuri N, Badu K, Gimié F, Bergrath J, Schulze M, Müller M, Bhaw-Lux¬imon A (2022) Nanomedicine-based strate¬gies to improve treatment of cutaneous leish-maniasis. R Soc Open Sci. 9(6): 220058.
49. Torabi N, Mohebali M, Shahverdi AR, Rezayat SM, Edrissian GH, Esmaeili J, Charehdar S (2011) Nanogold for the treat¬ment of zoonotic cutaneous leish-man¬ia¬sis caused by Leishmania major (MRHO/IR/75/ER): an animal trial with methanol extract of Eucalyptus camal-dulensis. J Pharm Sci. 1: 113–116.
50. Mohebali M, Rezayat M, Gilani K, Sarkar S, Akhoundi B, Esmaeili J, Satvat T, Elikaee S, Charehdar S, Hooshyar H (2015) Nanosilver in the treatment of localized cutaneous leishmaniasis caused by Leishmania major (MRHO/IR/75/ER): an in-vitro and in vivo study. DARU J Pharm Sci. 17(4): 285–289.
51. Mohtasebi S, Mohebali M, Elikaee S, Ak-houndi B, Foroushani AR, Teimouri A, Yarizadeh H (2019) In-vitro and in vivo anti-parasitic activity of biogenic anti-mo¬ny sulfide nanoparticles on Leish¬ma-nia major (MRHO/IR/75/ER). Parasi¬tol Res. 118(9): 2669–2678.
52. Mostafa G, Nahid J, Alireza D, Ebrahim SS (2021) Effect of Foeniculum Vulgare Aqueous and Alcoholic Seed Extract against Zoonotic Cutaneous Leishman¬i-asis. Ethiop J Health Sci. 31(2): 401–408.
53. Badirzadeh A, Heidari-Kharaji M, Fallah-Omrani V, Dabiri H, Araghi A, Salimi Chirani A (2020) Antileishmanial activ-ity of Urtica dioica extract against zo¬on-otic cutaneous leishmaniasis. PLoS Negl Trop Dis. 14(1): e0007843
54. Najm M, Hadighi R, Heidari-Kharaji M, Alipour M, Hajizadeh M, Rafiei-Sefiddash¬ti R, Heidari A, Badirzadeh A (2021) Anti-Leishmanial Activity of Ar-temisia persica, A. spicigera, and A. fra-grance against Leishmania major. Iran J Parasitol. 16(3): 464–473.
2. Izri A, Bendjaballah-Laliam A, Sereno D, Ak¬houndi M (2021) Updates on geo-graph¬ical dispersion of Leishmania parasites causing cutaneous affections in Algeria. Pathogens. 10(3): 0267.
3. Haldar AK, Sen P, Roy S (2011) Use of an¬timony in the treatment of leishmaniasis: current status and future directions. Mol Biol Int. 2011: 571242.
4. Frézard F, Demicheli C, Ribeiro RR (2009) Pentavalent antimonials: new per-spectives for old drugs. Molecules. 14(7): 2317–2336.
5. Nabas Z, Haddadin MS, Haddadin J, Nazer IK (2014) Chemical composition of roy¬al jelly and effects of synbiotic with two different locally isolated probiotic strains on antioxidant activities. Pol J Food Nutr Sci. 64(3): 171–180.
6 Brudzynski K, Sjaarda C (2015) Honey glycoproteins containing antimicrobial pep-tides, Jelleins of the Major Royal Jelly Pro¬tein 1, are responsible for the cell wall lytic and bactericidal activities of honey. PLoS One. 10(4): e0120238.
7. Gu L, Zeng H, Maeda K (2017) 10-Hy-droxy-2-decenoic acid in royal jelly ex-tract induced both filaggrin and amino ac¬id in a cultured human three-dimen-sion¬al epidermis model. Cosmetics. 4(4): 48.
8. Cornara L, Biagi M, Xiao J, Burlando B (2017) Therapeutic properties of bioac-tive compounds from different honeybee products. Front Pharmacol. 8: 412.
9. Garcia-Amoedo LH, Almeida-Muradian LBd (2007) Physicochemical composition of pure and adulterated royal jelly. Quím. Nova. 30(2): 257–259.
10. Pasupuleti VR, Sammugam L, Ramesh N, Gan SH (2017) Honey, propolis, and roy¬al jelly: a comprehensive review of their biological actions and health bene-fits. Ox¬id Med Cell Longev. 2017: 1259510.
11. Viuda‐Martos M, Ruiz‐Navajas Y, Fer-nán¬dez‐López J, Pérez‐Álvarez J (2008) Func¬tional properties of honey, propolis, and royal jelly. J Food Sci. 73(9): 117–124.
12. Marcucci MC (1995) Propolis: chemical com¬position, biological properties and ther¬apeutic activity. Apidologie. 26(2): 83–99.
13. Huang S, Zhang C-P, Wang K, Li GQ, Hu F-L (2014) Recent advances in the chem¬ical composition of propolis. Molecules. 19(12): 19610–19632.
14. Ratajczak M, Kaminska D, Matuszewska E, Hołderna-Kedzia E, Rogacki J, Matysi¬ak J (2021) Promising antimicrobial prop¬erties of bioactive compounds from dif¬ferent honeybee products. Molecules. 26 (13): 4007.
15. Astrada A, Nakagami G, Jais S, Sanada H (2019) Successful treatment of a dia¬bet-ic foot ulcer with exposed bone using Trig¬ona honey: a case study. J Wound Care. 128.(Sup12): S4–S8.
16. Krupp T, Dos Santos BD, Gama LA, Sil¬va JR, Arrais-Silva WW, de Souza NC, Américo MF, de Souza Souto PC (2019) Natural rubber-propolis membrane im-proves wound healing in second-degree burning model. Int J Biol Macromol. 131: 980–988.
17 Oryan A, Alemzadeh E, Moshiri A (2018) Potential role of propolis in wound heal-ing: Biological properties and thera¬peu-tic activities. Biomed Pharmacother. 98: 469–483.
18. Likitpongpipat N, Sangmaneedet S, Klanrit P, Noisombut R, Krisanaprakornkit S, Chail¬ertvanitkul P (2019) Promotion of dental pulp wound healing in New Zea¬land white rabbits’ teeth by Thai prop¬olis product. J Vet Dent. 36(1): 17–24.
19. Silva-Carvalho R, Baltazar F, Almeida-Aguiar C (2015) Propolis: a complex nat¬ural product with a plethora of bio-logi¬cal activities that can be explored for drug development. Evid Based Complement Alternat Med. 2015: 206439
20. Cai Z, Li F, Rong M, Lin L, Yao Q, Huang Y, Chen Xi, Wang Xia (2019) Novel Na¬nomaterials for Biomedical, Environ¬men¬tal and Energy Applications. Micro-Nano Technologies(MNT). pp. 1–36.
21. Balusamy B, Senthamizhan A, Uyar T (2017) Electrospun nanofibrous mate¬ri-als for wound healing applications. Elec-tro¬spun Materials for Tissue Engineering and Biomedical Applications: Research, De¬sign and Commercialization. pp. 147–177.
22. Wang J, Windbergs M (2017) Functional electrospun fibers for the treatment of hu¬man skin wounds. Eur J Pharm Bio-pharm. 119: 283–299.
23. Joshi VB, Geary SM, Salem AK (2013) Biodegradable particles as vaccine anti-gen delivery systems for stimulating cel-lular immune responses. Hum Vaccin Im¬munother. 9(12): 2584–2590.
24. Haider A, Haider S, Kang I-K (2018) A comprehensive review summarizing the effect of electrospinning parameters and potential applications of nanofibers in bi-omedical and biotechnology. Arab J Chem. 11(8): 1165–1188.
25. Xue J, Wu T, Dai Y, Xia Y (2019) Elec-trospinning and electrospun nanofibers: Methods, materials, and applications. Chem Rev. 119(8): 5298–5415.
26. Lu H, Wang J, Wang T, Zhong J, Bao Y, Hao H (2016) Recent progress on nanostruc¬tures for drug delivery appli¬ca-tions. J Nanomater. 2016: 5762431.
27. Wu J, Zhu YJ, Cao SW, Chen F (2010) Hierachically nanostructured mesopo-rous spheres of calcium silicate hydrate: Sur¬factant‐free sonochemical synthesis and drug‐delivery system with ultrahigh drug‐ loading capacity. Adv Mater. 22(6): 749–753.
28. Purohit G, Sakthivel T, Florence AT (2003) The interaction of cationic dendrons with albumin and their diffusion through cel¬lulose membranes. Int J Pharm. 254(1): 37–41.
29. Mansur HS, Sadahira CM, Souza AN, Man¬sur AA (2008) FTIR spectroscopy char¬acterization of poly (vinyl alcohol) hy¬dro¬gel with different hydrolysis degree and chemically crosslinked with glutaral¬de¬hyde. Mater Sci Eng: C. 28(4): 539–548.
30. Cebi N, Bozkurt F, Yilmaz MT, Sagdic O (2020) An evaluation of FTIR spec¬tros-copy for prediction of royal jelly content in hive products. J Apic Res. 59(2): 146–155.
31. Salam A, Khan MQ, Hassan T, Hassan N, Nazir A, Hussain T, Azeem M, Kim IS (2020) In-vitro assessment of appro¬pri-ate hydrophilic scaffolds by co-electrospin¬ning of poly (1, 4 cyclohexane iso¬sorbide terephthalate)/polyvinyl alcohol. Sci Rep. 10(1): 1–9.
32. Razavizadeh BM, Niazmand R (2020) Char¬acterization of polyamide-6/ propolis blend¬ed electrospun fibers. Heliyon. 6 (8): e04784.
33. Tian H, Yuan L, Wang J, Wu H, Wang H, Xiang A, Ashok B, Rajulu AV (2019) Electrospinning of polyvinyl alcohol into crosslinked nanofibers: an approach to fab¬ricate functional adsorbent for heavy met¬als. J Hazard Mater. 378: 120751.
34. Torabi N, Mohebali M, Shahverdi AR, Re-zayat SM, Edrissian Gh H, Esmaeili J, Charehdar S (2012) Nanogold for the treat¬ment of zoonotic cutaneous leish-man¬ia¬sis caused by Leishmania major (MRHO/ IR/75/ER): An animal trial with methanol ex¬tract of Eucalyptus camaldulensis. JPHS. 1(1): 13–16.
35. Mahmoudi M, Shabani M, Dehdast SA, Saberi S, Elmi T, Chiari Fard G, Tabat-abaie F, Akbari S (2022) The Charac-terization and Antileishmanial Evalu¬a-tion on Leishmania Major with Chitosan/ Zno Bio-Nanocomposite as Drug Delivery Systems. J Nanomed Res. 7(2): 140–149.
36. Farah ME, Maia M, Penha FM, Rodrigues EB (2016) The use of vital dyes during vitreoretinal surgery-chromovitrectomy. Dev Ophthalmol. 55: 365–375.
37. Garcia A, Amaral AF, Azevedo MM, Lopes BS, Alviano CS, Pinheiro AS, Vermelho AB, Rodriguesa IA (2017) Cytotoxicity and anti-Leishmania amazonensis activ¬ity of Citrus sinensis leaf extracts. Pharm Biol. 55(1): 1780–1786.
38. Khademvatan S, Gharavi MJ, Rahim F, Saki J (2011) Miltefosine-induced apop-totic cell death on Leishmania major and L. tropica strains. Korean J Parasi-tol. 49(1): 17–23.
39. Wu Y-W, Sun S-Q, Zhao J, Li Y, Zhou Q (2008) Rapid discrimination of extracts of Chinese propolis and poplar buds by FT-IR and 2D IR correlation spec¬tros-copy. J Mol Struct. 883: 48–54.
40. Rassu G, Cossu M, Langasco R, Carta A, Cavalli R, Giunchedi P, Gavini E (2015) Propolis as lipid bioactive nano-carrier for topical nasal drug delivery. Colloids Surf B Biointerfaces. 136: 908–917.
41. Coates J (2006) Interpretation of infrared spectra, a practical approach, Encyclo¬pe-dia of Analytical Chemistry: Applica-tions, Theory and Instrumentation, pp. 10815–10837.
42. Lazarevska S, Makreski P (2015) Insights into the infrared and Raman spectra of fresh and lyophilized royal jelly and pro-tein degradation IR spectroscopy study during heating. Maced J Chem Chem Eng. 34(1): 87–93.
43. Cebi N, Durak MZ, Toker OS, Sagdic O, Arici M (2016) An evaluation of Fourier transforms infrared spectroscopy method for the classification and discrimination of bovine, porcine and fish gelatins. Food Chem. 190: 1109–1115.
44. Zia M, Mannani R, Mahmoodi M, Bayat M, Mohaghegh F (2009) The effects of alcoholic extract of propolis obtained from Iran bee hives on the growth of Tri¬chophyton mentagrophytis, Tri-chophyton rubrum and Trichophyton verrucosum. J Isfahan Med Sch. 27(95): 232–241.
45. Diba K, Mahmoodi M, Hashemi J (2018) In-vitro activity of Propolis alcoholic ex-tract on opportunistic pathogenic fungi. Int J Res Appl Basic Med Sci. 4(2): 68–73.
46. Hamzeh Pour S, Khodavaisy S, Mahmoudi S, Vaziri S, Soltan Dallal MM, Oliya S, Getso M, Rezaie S (2020) The effect of royal jelly and propolis alone and in com¬bination on inhibition of Aspergillus par¬asiticus growth, aflatoxin production, and aflR gene expression. J Food Saf. 40(4): e12815.
47. Mahmoudi M, Mohebali M, Irandoust H, Hejazi S, Abdoli H, Shirani-Bidabadi L, Charehdar S, Shareghi N, Akhavan AA (2009) Therapeutic effects of propolis hy¬droalcoholic extract in the treatment of cutaneous leishmaniasis in Balb/c. J Sch Public Health Inst Public Health Res. 6 (3 and 4): 19–26.
48. Goonoo N, Laetitia Huët MA, Chummun I, Karuri N, Badu K, Gimié F, Bergrath J, Schulze M, Müller M, Bhaw-Lux¬imon A (2022) Nanomedicine-based strate¬gies to improve treatment of cutaneous leish-maniasis. R Soc Open Sci. 9(6): 220058.
49. Torabi N, Mohebali M, Shahverdi AR, Rezayat SM, Edrissian GH, Esmaeili J, Charehdar S (2011) Nanogold for the treat¬ment of zoonotic cutaneous leish-man¬ia¬sis caused by Leishmania major (MRHO/IR/75/ER): an animal trial with methanol extract of Eucalyptus camal-dulensis. J Pharm Sci. 1: 113–116.
50. Mohebali M, Rezayat M, Gilani K, Sarkar S, Akhoundi B, Esmaeili J, Satvat T, Elikaee S, Charehdar S, Hooshyar H (2015) Nanosilver in the treatment of localized cutaneous leishmaniasis caused by Leishmania major (MRHO/IR/75/ER): an in-vitro and in vivo study. DARU J Pharm Sci. 17(4): 285–289.
51. Mohtasebi S, Mohebali M, Elikaee S, Ak-houndi B, Foroushani AR, Teimouri A, Yarizadeh H (2019) In-vitro and in vivo anti-parasitic activity of biogenic anti-mo¬ny sulfide nanoparticles on Leish¬ma-nia major (MRHO/IR/75/ER). Parasi¬tol Res. 118(9): 2669–2678.
52. Mostafa G, Nahid J, Alireza D, Ebrahim SS (2021) Effect of Foeniculum Vulgare Aqueous and Alcoholic Seed Extract against Zoonotic Cutaneous Leishman¬i-asis. Ethiop J Health Sci. 31(2): 401–408.
53. Badirzadeh A, Heidari-Kharaji M, Fallah-Omrani V, Dabiri H, Araghi A, Salimi Chirani A (2020) Antileishmanial activ-ity of Urtica dioica extract against zo¬on-otic cutaneous leishmaniasis. PLoS Negl Trop Dis. 14(1): e0007843
54. Najm M, Hadighi R, Heidari-Kharaji M, Alipour M, Hajizadeh M, Rafiei-Sefiddash¬ti R, Heidari A, Badirzadeh A (2021) Anti-Leishmanial Activity of Ar-temisia persica, A. spicigera, and A. fra-grance against Leishmania major. Iran J Parasitol. 16(3): 464–473.
| Files | ||
| Issue | Vol 17 No 4 (2023) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v17i4.15294 | |
| Keywords | ||
| Leishmania major Nanofiber Propolis Royal jelly In-vitro | ||
| Rights and permissions | |
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Mahmoudi M, Mehravi B, Shabani M, Hadighi R, Badirzadeh A, Dehdast A, Chizari Fard G, Pirhajati Mahabadi V, Akbari S, Tabatabaie F, Mohebali M. Anti-Leishmanial Effects of a Novel Biocompatible Non-Invasive Nanofibers Containing Royal Jelly and Propolis against Iranian Strain of Leishmania major (MRHO/IR/75/ER): an In-Vitro Study. J Arthropod Borne Dis. 2023;17(4):299–320.
