Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-23T00:57:48.780Z Has data issue: false hasContentIssue false
  • English
  • Français

Egyptian propolis and selenium nanoparticles against murine trichinosis: a novel therapeutic insight

Published online by Cambridge University Press:  20 July 2022

M.H. Sarhan ,
A. Farghaly ,
N.F. Abd El-Aal Open the ORCID record for N.F. Abd El-Aal [Opens in a new window] ,
S. Mohammed Farag ,
A. Ahmed Ali  and
T.I. Farag
M.H. Sarhan
Affiliation:
Department of Medical Parasitology, Faculty of Medicine, Zagazig University, Zagazig 44519, Egypt
A. Farghaly
Affiliation:
Department of Medical Parasitology, Faculty of Medicine, Zagazig University, Zagazig 44519, Egypt
N.F. Abd El-Aal*
Affiliation:
Department of Medical Parasitology, Faculty of Medicine, Zagazig University, Zagazig 44519, Egypt
S. Mohammed Farag
Affiliation:
Department of Medical Parasitology, Faculty of Medicine, Zagazig University, Zagazig 44519, Egypt
A. Ahmed Ali
Affiliation:
Department of Pathology, Faculty of Veterinary Medicine, Zagazig University, Zagazig 44519, Egypt
T.I. Farag
Affiliation:
Department of Medical Parasitology, Faculty of Medicine, Zagazig University, Zagazig 44519, Egypt
*
Author for correspondence: N. F. Abd El-Aal, E-mail: naglaa_fathy220@yahoo.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Trichinosis is a serious zoonotic disease that causes human morbidity and mortality. New effective natural remedies with minimal side effects that are well tolerated are needed to treat both enteral and parenteral trichinosis. This study evaluated the efficacy of selenium (Se), Se nanoparticles (SeNPs) and Egyptian propolis compared with albendazole as antiparasitic, anti-inflammatory and anti-angiogenic agents for treating murine trichinosis. We used parasitological, histopathological and immunohistochemical assays, as well as scanning electron microscopy, to examine adult worms. Overall, 80 Swiss albino male mice were divided into eight groups, with ten mice in each group, as follows: negative control, positive control, albendazole, propolis, Se, combination of propolis and Se, SeNPs and combination of SeNPs and propolis. Mice were slaughtered seven and 35 days after infection to examine the intestinal and muscular phases, respectively. This study demonstrated the efficacy of the combination of SeNPs and propolis. As revealed by electron microscopy, this combination caused damage to the adult worm cuticle. Additionally, compared with albendazole, it resulted in a significant reduction in adult worm and total larval counts; moreover, it caused a decrease in the number of larvae deposited in muscles, with a highly significant decrease in the inflammatory cell infiltrate around the larvae and a considerable decrease in the expression of the angiogenic marker vascular endothelial growth factor in muscles. In conclusion, the combination of SeNPs and propolis had antiparasitic, anti-inflammatory and anti-angiogenic effects on trichinosis. Consequently, this combination could be used as a natural alternative therapy to albendazole for treating trichinosis.

Keywords

AngiogenesisVEGFmurine trichinosisscanning electron microscopyseleniumselenium nanoparticlespropolis
Type
Research Paper
Information
Journal of Helminthology , Volume 96 , 2022 , e50
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abdulrhman, M, Elbarbary, NS, Amin, DA and Ebrahim, RS (2012) Honey and a mixture of honey, beeswax, and olive oil-propolis extract in treatment of chemotherapy-induced oral mucositis: a randomized controlled pilot study. Pediatric Hematology and Oncology 29(3), 285–292.CrossRefGoogle Scholar
Abu El Ezz, NM (2005) Effects of Nigella sativa and Allium cepa oils on Trichinella spiralis in experimentally infected rats. Journal of the Egyptian Society of Parasitology 35(2), 511–523.Google ScholarPubMed
Al-Attar, TA, El-Kersh, WM, Sadek, GS, Harba, NM, Osheiba, SF and Brakat, RM (2020) A study of immunotherapeutic efficacy of Trichinella spiralis excretory-secretory proteins in murine trichinellosis. Journal of the Egyptian Society of Parasitology 50(2), 281–292.CrossRefGoogle Scholar
Al-Ghandour, AMF, Ahmed, HK, Salem, AE, Tealeb, AM, Mohamed, RMSM and Yousef, AM (2020) Efficacy of olibanum and propolis medicinal extracts versus metronidazole in Giardia lamblia experimentally infected mice. Microbes and Infectious Diseases 1(3), 209–220.CrossRefGoogle Scholar
Ashour, DS and Elbakary, RH (2011) Pathogenesis of restricted movements in trichinellosis: an experimental study. Experimental Parasitology 128(4), 414–418.CrossRefGoogle ScholarPubMed
Attia, RAH, Mahmoud, AE, Farrag, HMM, Makboul, R, Mohamed, ME and Ibraheim, Z (2015) Effect of myrrh and thyme on Trichinella spiralis enteral and parenteral phases with inducible nitric oxide expression in mice. Memórias do Instituto Oswaldo Cruz 110(8), 1035–1041.CrossRefGoogle ScholarPubMed
Azab, KS, Hanafy, SM, El Fateh, NM and Badr, NM (2015) Antiangiogenic effects of the apigenin and/or selenium on Ehrlish bearing mice. Research Journal of Applied Biotechnology 1(1), 21–43.CrossRefGoogle Scholar
Bae, M and Kim, H (2020) The roles of vitamin C, vitamin D, and selenium in the immune system against COVID-19. Molecules 25(22), 5346.CrossRefGoogle ScholarPubMed
Bass, DA and Szejda, P (1979) Eosinophils versus neutrophils in host defense. Killing of newborn larvae of Tricinella spiralis by human granulocytes in vitro. The Journal of Clinical Investigation 64(5), 1415–1422.CrossRefGoogle Scholar
Basyoni, MM and El-Sabaa, AA (2013) Therapeutic potential of myrrh and ivermectin against experimental Trichinella spiralis infection in mice. The Korean Journal of Parasitology 51(3), 297–304.CrossRefGoogle ScholarPubMed
Berry, A, Balard, P, Coste, A, et al. (2007) IL-13 induces expression of CD36 in human monocytes through PPAR γ activation. European Journal of Immunology 37(6), 1642–1652.CrossRefGoogle Scholar
Bhardwaj, R, Saudagar, P and Dubey, VK (2012) Nanobiosciences: a contemporary approach in antiparasitic drugs. Molecular and Cellular Pharmacology 4(3), 97–103.Google Scholar
Bortoleti, BTDS, Tomiotto-Pellissier, F, Gonçalves, MD, et al. (2019) Caffeic acid has antipromastigote activity by apoptosis-like process; and anti-amastigote by TNF-α/ROS/NO production and decreased of iron availability. Phytomedicine 57, 262–270.CrossRefGoogle ScholarPubMed
Bruschi, F and Chiumiento, L (2011) Trichinella inflammatory myopathy: host or parasite strategy? Parasites & Vectors 4, 42.CrossRefGoogle ScholarPubMed
Bruschi, F and Murrell, KD (2002) New aspects of human trichinellosis: the impact of new trichinella species. Postgraduate Medical Journal 78(915), 15–22.CrossRefGoogle ScholarPubMed
Bughdadi, FA (2010) Ultrastructural studies on the parasitic worm Trichinella spiralis. Journal of Taibah University for Science 3(1), 33–38.CrossRefGoogle Scholar
Caner, A, Döşkaya, M, Değirmenci, A, Can, H, Baykan, Ş, Üner, A, Başdemir, G, Zeybek, U and Gürüz, Y (2008) Comparison of the effects of Artemisia vulgaris and Artemisia absinthium growing in western Anatolia against trichinellosis (Trichinella spiralis) in rats. Experimental Parasitology 119(1), 173–179.CrossRefGoogle ScholarPubMed
Cannon, CP and Cannon, PJ (2012) Physiology.COX-2 inhibitors and cardiovascular risk. Science 336(6087), 1386–1387.CrossRefGoogle ScholarPubMed
Capó, VA, Despommier, DD and Polvere, RI (1998) T. spiralis: vascular endothelial growth factor is up-regulated within the nurse cell during the early phase of its formation. The Journal of Parasitology 84(2), 209–214.CrossRefGoogle ScholarPubMed
Compton, SJ, Celum, CL, Lee, C, Thompson, D, Sumi, SM, Fritsche, TR and Coombs, RW (1993) Trichinosis with ventilatory failure and persistent myocarditis. Clinical Infectious Diseases 16(4), 500–504.CrossRefGoogle ScholarPubMed
Dkhil, MA, Al-Quraishy, S and Wahab, R (2015) Anticoccidial and antioxidant activities of zinc oxide nanoparticles on Eimeria papillata-induced infection in the jejunum. International Journal of Nanomedicine 10, 1961–1968.CrossRefGoogle ScholarPubMed
Dkhil, MA, Bauomy, AA, Diab, MSM and Al-Quraishy, S (2016) Protective role of selenium nanoparticles against Schistosoma mansoni induced hepatic injury in mice. Biomedical Research 27(1), 214–219.Google Scholar
Dkhil, MA, Khalil, MF, Diab, MSM, Bauomy, AA, Santourlidis, S, Al-Shaebi, EM and Al-Quraishy, S (2019) Evaluation of nanoselenium and nanogold activities against murine intestinal schistosomiasis. Saudi Journal of Biological Sciences 26(7), 1468–1472.CrossRefGoogle ScholarPubMed
Drescher, N, Klein, A, Neumann, P, Yanez, O and Leonhardt, SD (2017) Inside honeybee hives: impact of natural propolis on the ectoparasitic mite Varroa destructor and viruses. Insects 8(1), 15.CrossRefGoogle ScholarPubMed
Dunn, IJ and Wright, KA (1985) Cell injury caused by Trichinella spiralis in the mucosal epithelium of B10A mice. The Journal of Parasitology 71(6), 757–766.CrossRefGoogle ScholarPubMed
Dwivedi, C, Shah, CP, Singh, K, Kumar, M and Bajaj, PN (2011) An organic acid induced synthesis and characterization of selenium nanoparticles. Journal of Nanotechnology 2011, 651971.CrossRefGoogle Scholar
El Temsahy, MM, Ibrahim, IR, Mossallam, SF, Mahrous, H, Abdel Bary, A and Abdel Salam, SA (2015) Evaluation of newly isolated probiotics in the protection against experimental intestinal trichinellosis. Veterinary Parasitology 214, 303–314.CrossRefGoogle ScholarPubMed
Gabrashanska, M, Teodorova, SE, Petkova, S, Mihov, L, Anisimova, M and Ivanov, D (2010) Selenium supplementation at low doses contributes to the antioxidant status in Trichinella spiralis-infected rats. Parasitology Research 106(3), 561–570.CrossRefGoogle Scholar
García, A, Leonardi, D, Vasconi, MD, Hinrichsen, LI and Lamas, MC (2014) Characterization of albendazole-randomly methylated-β- cyclodextrin inclusion complex and in vivo evaluation of its antihelmitic activity in a murine model of trichinellosis. PLoS One 9, e113296.CrossRefGoogle Scholar
Gilleard, J and Beech, RN (2007) Population genetics of anthelmintic resistance in parasitic nematodes. Parasitology 134, 1133–1147.CrossRefGoogle ScholarPubMed
Gottstein, B, Pozio, E and Nöckler, K (2009) Epidemiology, diagnosis, treatment, and control of trichinellosis. Clinical Microbiology Reviews 22(1), 127–145.CrossRefGoogle ScholarPubMed
Gou, HF, Chen, XC, Zhu, J, Jiang, M, Yang, Y, Cao, D and Hou, M (2011) Expressions of COX-2 and VEGF-C in gastric cancer: correlations with lymphangiogenesis and prognostic implications. Journal of Experimental & Clinical Cancer Research 30(1), 14.CrossRefGoogle ScholarPubMed
Hassan, SE, Abou-El-Dobal, SKA and Hegazi, AG (2016) Bioassay of Egyptian propolis on Toxocara vitulorum adult worms. World Applied Sciences Journal 34(3), 283–289.Google Scholar
Hegazi, AG (2012) Medical importance of bee products. ARI BİLİMİ/BEE SCIENCE 12(4), 136–146.Google Scholar
Hegazi, AG, Farghali, AA and Abd El Hady, FK (2004) Antiviral activity and chemical composition of European and Egyptian propolis. Egyptian Journal of Veterinary Science 38, 11–22.Google Scholar
Hegazi, AG, Abd El Hady, FK and Shalaby, HA (2007) An in vitro effect of propolis on adult worms of Fasciola gigantica. Veterinary Parasitology 144, 279–286.CrossRefGoogle Scholar
Hoffmann, PR and Berry, MJ (2008) The influence of selenium on immune responses. Molecular Nutrition & Food Research 52(11), 1273–1280.CrossRefGoogle ScholarPubMed
Huang, H, Yao, J, Liu, K, et al. (2020) Sanguinarine has anthelmintic activity against the enteral and parenteral phases of Trichinella infection in experimentally infected mice. Acta Tropica 201, 105226.CrossRefGoogle ScholarPubMed
Hughes, HP (1988) Oxidative killing of intracellular parasites mediated by macrophages. Parasitology Today 4(12), 340–347.CrossRefGoogle ScholarPubMed
Issa, RM (2007) Schistosoma mansoni: the prophylactic and curative effects of propolis in experimentally infected mice. Rawal Medical Journal 32(2), 94–98.Google Scholar
Kandil, OM, Nassar, SA, Nasr, SM, Shalaby, HA, Hendawy, S and El Moghazy, FM (2015) Synergetic effect of Egyptian propolis in immunization BALB/c mice against bovine cysticercosis. Asian Pacific Journal of Tropical Biomedicine 5, 324–330.CrossRefGoogle Scholar
Kim, JD, Liu, L, Guo, W and Meydani, M (2006) Chemical structure of flavonols in relation to modulation of angiogenesis and immune-endothelial cell adhesion. The Journal of Nutritional Biochemistry 17(3), 165–176.CrossRefGoogle ScholarPubMed
Krishnan, M, Ranganathan, K, Maadhu, P, Thangavelu, P, Kundan, S and Arjunan, N (2020) Leaf extract of Dillenia indica as a source of selenium nanoparticles with larvicidal and antimicrobial potential toward vector mosquitoes and pathogenic microbes. Coatings 10(7), 626.CrossRefGoogle Scholar
Kumar, N, Garg, AK, Mudgal, V, Dass, RS, Chaturvedi, VK and Varshney, VP (2008) Effect of different levels of selenium supplementation on growth rate, nutrient utilization, blood metabolic profile, and immune response in lambs. Biological Trace Element Research 126(Suppl 1), 44–56.CrossRefGoogle ScholarPubMed
Martin, RJ, Robertson, AP and Bjorn, H (1997) Target sites of anthelmintics. Parasitology 114(Suppl 1), 111–124.CrossRefGoogle ScholarPubMed
McKenzie, RC, Rafferty, TS and Beckett, GJ (1998) Selenium: an essential element for immune function. Immunology Today 19(8), 342–345.CrossRefGoogle ScholarPubMed
Mirzoeva, OK and Calder, PC (1996) The effect of propolis and its components on eicosanoid production during the inflammatory response. Prostaglandins Leukot Essent Fat Acids 55(6), 441–449.CrossRefGoogle ScholarPubMed
Muñoz-Carrillo, JL, Maldonado-Tapia, C, López-Luna, A, Muñoz-Escobedo, JJ, Flores-De La Torre, JA and Moreno-García, A (2018) Current aspects in Trichinellosis. In Bastidas, G (Ed)Parasites and Parasitic Diseases. London, IntechOpen. doi: 10.5772/intechopen.80372.Google Scholar
Neghina, R, Neghina, AM, Marincu, I and Iacobiciu, I (2011) Reviews on trichinellosis (I): renal involvement. Foodborne Pathogens and Disease 8(2), 179–188.CrossRefGoogle ScholarPubMed
Nelson, SM, Shay, AE, James, JL, Carlson, BA, Urban, JF Jr and Prabhu, KS (2016) Selenoprotein expression in macrophages is critical for optimal clearance of parasitic helminth Nippostrongylus brasiliensis. Journal of Biological Chemistry 291(6), 2787–2798.CrossRefGoogle ScholarPubMed
Ock, MS, Cha, HJ and Choi, YH (2013) Verifiable hypotheses for thymosin β4-dependent and independent angiogenic induction of T. spiralis-triggered nurse cell formation. International Journal of Molecular Sciences 14(12), 23492–23498.CrossRefGoogle ScholarPubMed
Ohta, T, Kunimasa, K, Kobayashi, T, Sakamoto, M and Kaji, K (2008) Propolis suppresses tumor angiogenesis by inducing apoptosis in tube-forming endothelial cells. Bioscience, Biotechnology and Biochemistry 72(9), 2436–2440.CrossRefGoogle ScholarPubMed
Othman, AA, Abou Rayia, DM, Ashour, DS, Saied, EM, Zineldeen, DH and El-Ebiary, AA (2016) Atorvastatin and metformin administration modulates experimental Trichinella spiralis infection. Parasitology International 65(2), 105–112.CrossRefGoogle ScholarPubMed
Pahlavani, N, Malekahmadi, M, Firouzi, S, Rostami, D, Sedaghat, A, Moghaddam, AB, Ferns, GA, Navashenaq, JG, Reazvani, R, Safarian, M and Ghayour-Mobarhan, M (2020) Molecular and cellular mechanisms of the effects of Propolis in inflammation, oxidative stress and glycemic control in chronic diseases. Nutrition and Metabolism 17, 65.CrossRefGoogle ScholarPubMed
Parolia, A, Thomas, MS, Kundabala, M and Mohan, M (2010) Propolis and its potential uses in oral health. International Journal of Medicine and Medical Sciences 2(7), 210–215.Google Scholar
Peng, D, Zhang, J, Liu, Q and Taylor, E (2007) Size effect of elemental selenium nanoparticles (Nano-Se) at supranutritional levels on selenium accumulation and glutathione S-transferase activity. Journal of Inorganic Biochemistry 101(10), 1457–1463.CrossRefGoogle ScholarPubMed
Priotti, J, Codina, AV, Leonardi, D, Vasconi, MD, Hinrichsen, LI and Lamas, MC (2017) Albendazole microcrystal formulations based on chitosan and cellulose derivatives: physicochemical characterization and in vitro parasiticidal activity in Trichinella spiralis adult worms. AAPS PharmSciTech 18(4), 947–956.CrossRefGoogle ScholarPubMed
Rajkumar, K, Sandhya, MVS, Koganti, S and Burgula, S (2020) Selenium nanoparticles synthesized using Pseudomonas stutzeri (MH191156) show antiproliferative and anti-angiogenic activity against cervical cancer cells. International Journal of Nanomedicine 15, 4523–4540.CrossRefGoogle ScholarPubMed
Rayman, MP (2012) Selenium and human health. The Lancet 379(9822), 1256–1268.CrossRefGoogle ScholarPubMed
Ren, S-X, Zhang, B, Lin, Y, Ma, D-S and Yan, H (2019) Selenium nanoparticles dispersed in phytochemical exert anti-inflammatory activity by modulating catalase, GPx1, and COX-2 gene expression in a rheumatoid arthritis Rat model. Clinical Research 25, 991–1000.Google Scholar
Ren, Y, Qin, Y, Zhang, X, Zheng, L, Dai, X, Wu, H, Dong, Y and Cui, Y (2018) Killing the muscular larvae of Trichinella spiralis and the anti-fibrotic effect of the combination of wortmannilatone F and recombinant G31P in a murine model. Biomedicine & Pharmacotherapy 108, 934–940.CrossRefGoogle ScholarPubMed
Salama, MAM, Mostafa, NE, Abd EL-Aal, NF, Mostafa, EM, Hammad, SK, Adel, R and Moawad, HSF (2021) Capsicum frutescens and Citrus limon: a new take on therapy against experimental trichinellosis. Journal of Helminthology 95(e26), 1–11.CrossRefGoogle Scholar
Schmahl, G, Mehlhorn, H, Harder, A, Klimpel, S and Krieger, K (2007) Efficacy of a combination of imidacloprid plus moxidectin against larva and adult stages of nematodes (Trichuris muris, Angiostrongylus cantonensis) in rodents. Parasitology Research 101, 85–92.CrossRefGoogle Scholar
Sforcin, JM (2016) Biological properties and therapeutic applications of propolis. Phytotherapy Research 30(6), 894–905.CrossRefGoogle ScholarPubMed
Shalaby, HA, El Namaky, AH, Khalil, FA and Kandil, OM (2012) Efficacy of methanolic extract of Balanites aegyptiaca fruits on Toxocara vitulorum. Veterinary Parasitology 183, 386–392.CrossRefGoogle ScholarPubMed
Shalaby, MA, Moghazy, FM, Shalaby, HA and Nasr, SM (2010) Effect of methanolic extract of Balanites aegyptiaca fruits on enteral and parenteral stages of Trichinella spiralis in rats. Parasitology Research 107(1), 17–25.CrossRefGoogle ScholarPubMed
Shoheib, ZS, Shamloula, MM, Abdin, AA and El-Segai, O (2006) Role of α-chymotrypsin and colchicine as adjuvant therapy in experimental muscular trichinellosis: parasitological, biochemical and immunohistochemical study. Egyptian Journal of Medical Microbiology 15, 773–790.Google Scholar
Sowndarya, P, Ramkumar, G and Shivakumar, M (2017) Green synthesis of selenium nanoparticles conjugated Clausena dentata plant leaf extract and their insecticidal potential against mosquito vectors. Artificial Cells Nanomedicine and Biotechnology 45(8), 1490–1495.CrossRefGoogle ScholarPubMed
Stitt, AW and Fairweather, I (1993) Fasciola hepatica: tegumental surface changes in adult and juvenile flukes following treatment in vitro with the sulphoxide metabolite of triclabendazole (Fasinex). Parasitology Research 79(7), 529–536.CrossRefGoogle Scholar
Sung, SH, Choi, GH, Lee, NW and Shin, BC (2017) External use of propolis for oral, skin and genital diseases: a systematic review and meta-analysis. Evidence-Based Complementary and Alternative Medicine 2017, 8025752.CrossRefGoogle ScholarPubMed
Talas, ZS, Ozdemir, I, Yilmaz, I, Gok, Y and Orun, I (2008) The investigation of the antioxidative properties of the novel synthetic organoselenium compounds in some rat tissues. Experimental Biology and Medicine 233(5), 575–589.CrossRefGoogle Scholar
Wiesman, Z and Chapagain, BP (2006) Larvicidal activity of saponin containing extracts and fractions of fruit mesocarp of Balanites aegyptiaca. Fitoterapia 77, 420–424.CrossRefGoogle ScholarPubMed
Yadav, AK and Temjenmongla, (2006) Anthelmintic activity of Gynura angulosa DC against Trichinella spiralis infections in mice. Pharmacologyonline 2, 299–306.Google Scholar
Yadav, AK and Temjenmongla, (2012) Efficacy of Lasia spinosa leaf extract in treating mice infected with Trichinella spiralis. Parasitology Research 110(1), 493–498.CrossRefGoogle ScholarPubMed
Zabaiou, N, Fouache, A, Trousson, A, Baron, S, Zellagui, A, Lahouel, M and Lobaccaro, JA (2017) Biological properties of propolis extracts: something new from an ancient product. Chemistry and Physics of Lipids 207, 214–222.CrossRefGoogle ScholarPubMed