Abstract
Purpose
Propolis (bee glue) is a resinous mixture of different plant exudates that possesses a wide range of biological and antimicrobial activities and has been used as a food supplement and in complementary medicine for centuries. Some researchers have proposed that propolis could be a potential curative compound against microbial agents such as protozoan parasitic infections by different and occasionally unknown mechanisms due to the immunoregulatory function and antioxidant capacity of this natural product.
Methods
In this review, we concentrate on in vitro and in vivo anti-protozoan activities of propolis extracts/fractions in the published literature.
Results
In Leishmania, propolis inhibits the proliferation of promastigotes and produces an anti-inflammatory effect via the inhibition of nitric oxide (NO) production. In addition, it increases macrophage activation, TLR-2, TNF-α, IL-4, IL-17 production, and downregulation of IL-12. In Plasmodium and Trypanosoma, propolis inhibits the parasitemia, improving anemia and increasing the IFN-γ, TNF-α, and GM-CSF cytokines levels, most likely due to its strong immunomodulatory activity. Moreover, propolis extract arrests proliferation of T. cruzi, because it has aromatic acids and flavonoids. In toxoplasmosis, propolis increases the specific IgM and IgG titers via decreasing the serum IFN-γ, IL-1, and IL-6 cytokines levels in the rats infected with T. gondii. In Cryptosporidium and Giardia, it decreases oocysts shedding due to phytochemical constituents, particularly phenolic compounds, and increases the number of goblet cells. Propolis inhibits the growth of Blastocystis, possibly by apoptotic mechanisms like metronidazole. Unfortunately, the mechanism action of propolis’ anti-Trichomonas and anti-Acanthamoeba is not well-known yet.
Conclusion
Reviewing the related literature could highlight promising antimicrobial activities of propolis against intracellular and extracellular protozoan parasites; this could shed light on the exploration of more effective drugs for the treatment of protozoan parasitic infections in the near future.
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References
Oda JM, Fujita TC, Pitz AD, Amarante MK, Felipe I, Saridakis HO, Sforcin JM, Watanabe MA, Costa IC (2011) Ação do extrato de própolis na Leishmaniose. Semina: Ciências Biológicas e da Saúde 32(1):111–121
Teixeira ÉW, Negri G, Meira RM, Salatino A (2005) Plant origin of green propolis: bee behavior, plant anatomy and chemistry. Evid Based Complement Altern Med 2(1):85–92. https://doi.org/10.1093/ecam/neh055
Bankova V (2005) Chemical diversity of propolis and the problem of standardization. J Ethnopharmacol 100:114–117
Abdulkhani A, Hosseinzadeh J, Ashori A, Esmaeeli H (2017) Evaluation of the antibacterial activity of cellulose nanofibers/polylactic acid composites coated with ethanolic extract of propolis. Polym Compos 38:13–19
Simone-Finstrom M, Spivak M (2010) Propolis and bee health: the natural history and significance of resin use by honey bees. Apidologie 41:295–311
Wagh VD (2013) Propolis: a wonder bee's product and its pharmacological potentials. Adv Pharmacol Sci. https://doi.org/10.1155/2013/308249(Article ID 308249)
Ristivojević P, Trifković J, Andrić F, Milojković-Opsenica D (2015) Poplar-type propolis: chemical composition, botanical origin and biological activity. Nat Prod Commun 10:1869–1876
Machado JL, Assunçao AK, da Silva MC, Reis AS, Costa GC, Arruda DD, Rocha BA, Vaz MM, Paes AM, Guerra RN, Berretta AA (2012) Brazilian green propolis: anti-inflammatory property by an immunomodulatory activity. Evid Based Complement Altern Med. https://doi.org/10.1155/2012/157652
Nina V, Quispe C, Jimenez-Aspee F, Theoduloz C, Gimenez A, Schmeda-Hirschmann G (2016) Chemical profiling and antioxidant activity of Bolivian propolis. J Sci Food Agric 96:2142–2153
Amarante MK, Watanabe MA, Conchon-Costa I, Fiori LL, Oda JM, Búfalo MC, Sforcin JM (2012) The effect of propolis on CCL5 and IFN-γ expression by peripheral blood mononuclear cells from leishmaniasis patients. J Pharm Pharmacol 64:154–160
Sforcin JM, Bankova V, Kuropatnicki AK (2017) Medical benefits of honeybee products. Evid Based Complement Altern Med. https://doi.org/10.1155/2017/2702106(Article ID 2702106)
Bankova V (2010) New biologically active compounds from Kenyan propolis. Fitoterapia 81:509–514
Brito GAB, Chaves MH (2010) β - amyrin, a natural triterpenoidameliorates L-arginine-induced acute pancreatitis in rats. World J Gastroenterol 16:4272–4280
De Mendonca IC, Porto IC, do Nascimento TG, de Souza NS, Oliveira JM, Arruda RE, Mousinho KC, dos Santos AF, Basilio-Junior ID, Parolia A, Barreto FS (2015) Brazilian red propolis: phytochemical screening, antioxidant activity and effect against cancer cells. BMC Complement Altern Med 15:357
Zabaiou N, Fouache A, Trousson A, Baron S, Zellagui A, Lahouel M, Lobaccaro JM (2017) Biological properties of propolis extracts: something new from an ancient product. Chem Phys Lipids 207:214–222
Olczyk P, Wisowski G, Komosinska-Vassev K, Stojko J, Klimek K, Olczyk M, Kozma EM (2013) Propolis modifies collagen types I and III accumulation in the matrix of burnt tissue. Evid Based Complement Alternat Med. https://doi.org/10.1155/2013/423809(Article ID 423809)
Bueno-Silva B, Alencar SM, Koo H, Ikegaki M, Silva GV, Napimoga MH, Rosalen PL (2013) Anti-inflammatory and antimicrobial evaluation of neovestitol and vestitol isolated from Brazilian red propolis. J Agric Food Chem 61:4546–4550
Sforcin JM (2016) Biological properties and therapeutic applications of propolis. Phytother Res 30:894–905
Hegazi AG, El Hady FK, Allah FA (2000) Chemical composition and antimicrobial activity of European propolis. Z Naturforsch 55c:70–75
Prytzyk E, Dantas AP, Salomão K, Pereira AS, Bankova VS, De Castro SL, Neto FR (2003) Flavonoids and trypanocidal activity of Bulgarian propolis. J Ethnopharmacol 88:189–193
Banskota AH, Tezuka Y, Kadota S (2001) Recent progress in pharmacological research of propolis. Phytother Res 15:561–571
Sundar S, Chakravarty J (2013) Leishmaniasis: an update of current pharmacotherapy. Expert Opin Pharmacother 14:53–63
Martinotti S, Ranzato E (2015) Propolis: a new frontier for wound healing? Burns Trauma 3:9
Ramos A, Miranda JD (2007) Propolis: a review of its anti-inflammatory and healing actions. J Venomous Anim Toxins Incl Trop Dis 13:697–710
Trusheva B, Trunkova D, Bankova V (2007) Different extraction methods of biologically active components from propolis: a preliminary study. Chem Cent J 1(1):13
Suzuki S, Amano K, Suzuki K (2009) Effect of propolis volatiles from a stingless honeybee (Apidae: Meliponinae) on the immune system of elderly residents in a nursing home. Int J Indust Entomol 19:193–197
Rebouças-Silva J, Celes FS, Lima JB, Barud HS, de Oliveira CI, Berretta AA, Borges VM (2017) Parasite killing of leishmania (V) braziliensis by standardized propolis extracts. Evid Based Complement Altern Med. https://doi.org/10.1155/2017/6067172(Article ID 6067172)
de Castro Oliveira LG, Brito LM, de Moraes Alves MM, Amorim LV, Sobrinho-Júnior EP, de Carvalho CE, da Franca Rodrigues KA, Arcanjo DD, das Graças Lopes Citó AM, de Amorim Carvalho FA (2017) In vitro effects of the neolignan 2, 3-dihydrobenzofuran against leishmania amazonensis. Basic Clin Pharmacol Toxicol 120:52–58
da Silva SS, Mizokami SS, Fanti JR, Miranda MM, Kawakami NY, Teixeira FH, Araújo EJ, Panis C, Watanabe MA, Sforcin JM, Pavanelli WR (2016) Propolis reduces Leishmania amazonensis-induced inflammation in the liver of BALB/c mice. Parasitol Res 115:1557–1566
Do Nascimento TG, Da Silva PF, Azevedo LF, Da Rocha LG, de Moraes Porto IC, de Moura TF, Basílio-Júnior ID, Grillo LA, Dornelas CB, da Silva Fonseca EJ, de Jesus Oliveira E (2016) Polymeric nanoparticles of Brazilian red propolis extract: preparation, characterization, antioxidant and leishmanicidal activity. Nanoscale Res Lett 11:301
Nina N, Lima B, Feresin GE, Giménez A, Salamanca Capusiri E, Schmeda-Hirschmann G (2016) Antibacterial and leishmanicidal activity of Bolivian propolis. Lett Appl Microbiol 62:290–296
Miranda MM, Panis C, Cataneo AH, da Silva SS, Kawakami NY, de Franca Lopes LG, Morey AT, Yamauchi LM, de Jesus Andrade CG, Cecchini R, da Silva JJ (2015) Nitric oxide and Brazilian propolis combined accelerates tissue repair by modulating cell migration, cytokine production and collagen deposition in experimental leishmaniasis. PLoS ONE 10:e0125101
Ferreira FM, Castro RA, Batista MA, Rossi FM, Silveira-Lemos D, Frézard F, Moura SA, Rezende SA (2014) Association of water extract of green propolis and liposomal meglumine antimoniate in the treatment of experimental visceral leishmaniasis. Parasitol Res 113:533–543
Duran N, Muz M, Culha G, Duran G, Ozer B (2011) GC-MS analysis and antileishmanial activities of two Turkish propolis types. Parasitol Res 108:95–105
Duran G, Duran N, Culha G, Ozcan B, Oztas H, Ozer B (2008) In vitro antileishmanial activity of Adana propolis samples on Leishmania tropica: a preliminary study. Parasitolo Res 102:1217–1225
Ayres DC, Fedele TA, Marcucci MC, Giorgio S (2011) Potential utility of hyperbaric oxygen therapy and propolis in enhancing the leishmanicidal activity of glucantime. Rev Inst Med Trop Sao Paulo 53:329–334
Da Silva SS, Thomé GD, Cataneo AH, Miranda MM, Felipe I, Andrade CG, Watanabe MA, Piana GM, Sforcin JM, Pavanelli WR, Conchon-Costa I (2013) Brazilian propolis antileishmanial and immunomodulatory effects. Evid Based Complement Altern Med. https://doi.org/10.1155/2013/673058
Pontin K, Da Silva Filho AA, Santos FF, e Silva ML, Cunha WR, Nanayakkara ND, Bastos JK, de Albuquerque S (2008) In vitro and in vivo antileishmanial activities of a Brazilian green propolis extract. Parasitol Res 103:487–492
dos Santos Thomazelli AP, Tomiotto-Pellissier F, da Silva SS, Panis C, Orsini TM, Cataneo AH, Miranda-Sapla MM, Custódio LA, Tatakihara VL, Bordignon J, Silveira GF (2017) Brazilian propolis promotes immunomodulation on human cells from American tegumentar leishmaniasis patients and healthy donors infected with L. braziliensis. Cell Immunol 311:22–27
Soufy H, Nadia M, Nasr SM, El-Aziz TH, Khalil FA, Ahmed YF, Zeina HA (2017) Effect of Egyptian propolis on cryptosporidiosis in immunosuppressed rats with special emphasis on oocysts shedding, leukogram, protein profile and ileum histopathology. Asian Pac J Trop med 10:253–262
El-Beih NM, Soufy H, Nasr SM, Khalil FA, Sharaf M (2014) Effect of Egyptian propolis on lipid profile and oxidative status in comparison with nitazoxanide in immunosuppressed rats infected with Cryptosporidium spp. Glob Vet 13:17–27
AlGabbani Q, Mansour L, Elnakady YA, Al-Quraishy S, Alomar S, Al-Shaebi EM, Abdel-Baki AA (2017) In vivo assessment of the antimalarial and spleen-protective activities of the Saudi propolis methanolic extract. Parasitol Res 116:539–547
Dewi RM (2009) Immunomodulatory and in vivo antiplasmodial activities of propolis extracts. Am J Pharmacol Toxicol 4:75–79
Nweze NE, Okoro HO, Al Robaian M, Omar RM, Tor-Anyiin TA, Watson DG, Igoli JO (2017) Effects of Nigerian red propolis in rats infected with Trypanosoma brucei brucei. Comp Clin Path 26:1129–1133
Salomao K, de Souza EM, Henriques-Pons A, Barbosa HS, de Castro SL (2011) Brazilian green propolis: effects in vitro and in vivo on Trypanosoma cruzi. Evid Based Complement Altern Med. https://doi.org/10.1093/ecam/nep014(Article ID 185918)
Silva RP, Machado BA, de Abreu Barreto G, Costa SS, Andrade LN, Amaral RG, Carvalho AA, Padilha FF, Barbosa JD, Umsza-Guez MA (2017) Antioxidant, antimicrobial, antiparasitic, and cytotoxic properties of various Brazilian propolis extracts. PLoS ONE 12:e0172585
Monzote L, Cuesta-Rubio O, Campo Fernandez M, Márquez Hernandez I, Fraga J, Pérez K, Kerstens M, Maes L, Cos P (2012) In vitro antimicrobial assessment of Cuban propolis extracts. Mem Inst Oswaldo Cruz 107:978–984
Siheri W, Zhang T, Ebiloma GU, Biddau M, Woods N, Hussain MY, Clements CJ, Fearnley J, Ebel RE, Paget T, Muller S (2016) Chemical and antimicrobial profiling of propolis from different regions within Libya. PLoS ONE 11:e0155355
Mokhtar AB, El-Gayar EK, Habib ES (2016) In vitro anti-protozoal activity of propolis extract and cysteine proteases inhibitor (phenyl vinyl sulfone) on Blastocystis species. J Egypt Soc Parasitol 240:1–2
Kolören Z, Ertürk Ö, Karaman Ü (2017) Amoebicidal Activity of Propolis collected from Different Regions within Turkey. In: Proceeding in the 3rd international symposium on EuroAsian biodiversity July 2017, Minsk – BELARUS
Vural A, Polat ZA, Topalkara A, Toker MI, Erdogan H, Arici MK, Cetin A (2007) The effect of propolis in experimental Acanthamoeba keratitis. Clin Exp Ophthalmol 35:749–754
David ÉB, de Carvalho TB, Oliveira CM, Coradi ST, Sforcin JM, Guimarães S (2012) Characterisation of protease activity in extracellular products secreted by Giardia duodenalis trophozoites treated with propolis. Nat Prod Res 26:370–374
Alday-Provencio S, Diaz G, Rascon L, Quintero J, Alday E, Robles-Zepeda R, Garibay-Escobar A, Astiazaran H, Hernandez J, Velazquez C (2015) Sonoran propolis and some of its chemical constituents inhibit in vitro growth of Giardia lamblia trophozoites. Planta Med 81:742–747
Sena-Lopes A, Bezerra FS, das Neves RN, de Pinho RB, de Oliveira Silva MT, Savegnago L, Collares T, Seixas F, Begnini K, Henriques JA, Ely MR (2018) Chemical composition, immunostimulatory, cytotoxic and antiparasitic activities of the essential oil from Brazilian red propolis. PLoS ONE 13:e0191797
de Oliveira Dembogurski DS, Trentin DS, Boaretto AG, Rigo GV, da Silva RC, Tasca T, Macedo AJ, Carollo CA, Silva DB (2018) Brown propolis-metabolomic innovative approach to determine compounds capable of killing Staphylococcus aureus biofilm and Trichomonas vaginalis. Food Res Int 111:661–673
Hegazi AG, El-Fadaly HA, Barakat AM, Abou-El-Doubal SK (2014) In vitro effects of some bee products on T. gondii Tachyzoites. Glob Vet 13:1043–1050
Hegazi AG, Al Guthami FM, Al Gethami AF, Barakat AM (2017) Egyptian propolis 12: influence of propolis on cytokines of toxoplasma gondii infected rats. Int J Curr Microbiol 6:202–211
Ok ÜZ, Balcıoğlu İC, Özkan AT, Özensoy S, Özbel Y (2002) Leishmaniasis in Turkey. Acta Trop 84:43–48
Desjeux P (2004) Leishmaniasis: current situation and new perspectives. Comp Immunol Microbiol Infect Dis 27:305–318
Olivier M, Gregory DJ, Forget G (2005) Subversion mechanisms by which Leishmania parasites can escape the host immune response: a signaling point of view. Clin Microbiol 18:293–305
Reiner SL, Locksley RM (1995) The regulation of immunity to Leishmania major. Annu Rev Immunol 13:151–177
Sacks D, Noben-Trauth N (2002) The immunology of susceptibility and resistance to Leishmania major in mice. Nat Rev Immunol 2:845
Babior BM (2000) Phagocytes and oxidative stress. Am J Med 109:33–44
Cunningham AC (2002) Parasitic adaptive mechanisms in infection by Leishmania. Exp Mol Pathol 72:132–141
Van Assche T, Deschacht M, da Luz RA, Maes L, Cos P (2011) Leishmania macrophage interactions: insights into the redox biology. Free Radic Biol Med 51:337–351
Olekhnovitch R, Ryffel B, Müller AJ, Bousso P (2014) Collective nitric oxide production provides tissue-wide immunity during Leishmania infection. J Clin Invest 124:1711–1722
Silva AL, Adade CM, Shoyama FM, Neto CP, Padrón TS, de Almeida MV, de Magalhães Rezende CA, Silva CV, Souza MA (2012) In vitro leishmanicidal activity of N-dodecyl-1, 2-ethanediamine. Biomed Pharmacother 66:180–186
Sosa N, Pascale JM, Jiménez AI, Norwood JA, Kreishman-Detrick M, Weina PJ, Lawrence K, McCarthy WF, Adams RC, Scott C, Ransom J (2019) Topical paromomycin for new world cutaneous leishmaniasis. PLoS Negl Trop Dis 13:e0007253
Croft SL, Coombs GH (2003) Leishmaniasis current chemotherapy and recent advances in the search for novel drugs. Trends Parasitol 19:502–508
Aksoy A, Duran N, Toroglu S, Koksal F (2007) Short-term effect of mastic gum on salivary concentrations of cariogenic bacteria in orthodontic patients. Angle Orthod 77:124–128
Orsatti CL, Missima F, Pagliarone AC, Bachiega TF, Búfalo MC, Araújo JP Jr, Sforcin JM (2010) Propolis immunomodulatory action in vivo on Toll-like receptors 2 and 4 expression and on pro-inflammatory cytokines production in mice. Phytother Res 24:1141–1146
Silva SS, Miranda MM, Costa IN, Watanabe MA, Pavanelli WR, Felipe I, Sforcin JM, Conchon-Costa I (2015) Leishmanicidal activity of brazilian propolis hydroalcoholic extract in Leishmania amazonensis. Semina cienc biol Saude 25:35–44
Freitas SF, Shinohara L, Sforcin JM, Guimarães S (2006) In vitro effects of propolis on Giardia duodenalis trophozoites. Phytomedicine 13:170–175
Deeks ED (2019) Fexinidazole: first global approval. Drugs 79:215–220
Munday JC, Eze AA, Baker N, Glover L, Clucas C, Aguinaga Andrés D, Natto MJ, Teka IA, McDonald J, Lee RS, Graf FE (2014) Trypanosoma brucei aquaglyceroporin 2 is a high-affinity transporter for pentamidine and melaminophenyl arsenic drugs and the main genetic determinant of resistance to these drugs. J Antimicrob Chemother 69:651–663
Salomão K, Dantas AP, Borba CM, Campos LC, Machado DG, Aquino Neto FR, De Castro SL (2004) Chemical composition and microbicidal activity of extracts from Brazilian and Bulgarian propolis. Lett Appl Microbiol 38:87–92
Sant'Anna C, Pereira MG, Lemgruber L, de Souza W, Cunha e Silva NL (2008) New insights into the morphology of Trypanosoma cruzi reservosome. Microsc Res Tech 71:599–605
World Health Organization (2016) World Malaria Report 2015. World Health Organization, Geneva
Cowell AN, Istvan ES, Lukens AK, Gomez-Lorenzo MG, Vanaerschot M, Sakata-Kato T, Flannery EL, Magistrado P, Owen E, Abraham M, LaMonte G (2018) Mapping the malaria parasite druggable genome by using in vitro evolution and chemogenomics. Science 359:191–199
Hafiz TA, Mubaraki MA, Al-Quraishy S, Dkhil MA (2016) The potential role of Punica granatum treatment on murine malaria-induced hepatic injury and oxidative stress. Parasitolo Res 115:1427–1433
Adegbolagun OM, Emikpe BO, Woranola IO, Ogunremi Y (2013) Synergistic effect of aqueous extract of Telfaria occidentalis on the biological activities of artesunate in Plasmodium berghei infected mice. Afr Health Sci 13:970–976
Jabbarzare M, Voon Kin CH, Talib H, Mun Fei YA, Siti Khadijah AD, Hassan H, Majid RA, Taib CN, Moklas MA, Hidayat MT, Sidek HM (2015) Interleukin-18 antagonism improved histopathological conditions of malaria infection in mice. Iran J Parasitol 10:389
Kawakita SW, Giedlin HS, Nomoto K (2005) Immunomodulators from higher plants. J Nat Med 46:34–38
Yoneto T, Yoshimoto T, Wang CR, Takahama Y, Tsuji M, Waki S, Nariuchi H (1999) Gamma interferon production is critical for protective immunity to infection with blood-stage Plasmodium berghei XAT but neither NO production nor NK cell activation is critical. Infect Immun 67:2349–2356
Szliszka E, Kucharska AZ, Sokół-Łętowska A, Mertas A, Czuba ZP, Król W (2013) Chemical composition and anti-inflammatory effect of ethanolic extract of Brazilian green propolis on activated J774A. 1 macrophages. Evid Based Complement Alternat Med. https://doi.org/10.1155/2013/976415(Article ID 976415)
Gao W, Wu J, Wei J, Pu L, Guo C, Yang J, Yang M, Luo H (2014) Brazilian green propolis improves immune function in aged mice. J Clin Biochem Nutr 55:7–10
Lima LD, Andrade SP, Campos PP, Barcelos LS, Soriani FM, Moura SA (2014) Brazilian green propolis modulates inflammation, angiogenesis and fibrogenesis in intraperitoneal implant in mice. BMC Complement Altern Med 14:177
Olayemi KI (2014) Therapeutic potentials of Nigerian insect-propolis against the malarial parasite, Plasmodium berghei (Haemosporida: Plasmodidae). Am J Drug Disc 4:241–247
Kalia P, Kumar NR, Harjai K (2014) Studies on the effect of ethanolic extract of propolis in BALB/c mice. J App Nat Sci 6:638–643
Lawal B, Shittu OK, Abubakar AN, Haruna GM, Saidu S, Ossai PC (2015) Haematopoetic effect ofmethanol extract ofNigerian honey bee (Apis mellifera) propolis in mice. J Coast Life Med 3:648–651
Lawal B, Shittu OK, Kabiru AY, Jigam AA, Umar MB, Berinyuy EB, Alozieuwa BU (2015) Potential antimalarials from African natural products: a review. J Intercult Ethnopharmacol 4:318–343
Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, Faruque AS (2013) Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382:209–222
Steele MI, Kuhls TL, Nida K, Meka CS, Halabi IM, Mosier DA, Elliott W, Crawford DL, Greenfield RA (1995) A Cryptosporidium parvum genomic region encoding hemolytic activity. Infect Immun 63:3840–3845
Amadi B, Mwiya M, Sianongo S, Payne L, Watuka A, Katubulushi M, Kelly P (2009) High dose prolonged treatment with nitazoxanide is not effective for cryptosporidiosis in HIV positive Zambian children: a randomised controlled trial. BMC Infect Dis 9:195
Nassar SA, Mohamed AH, Soufy H, Nasr SM, Mahran KM (2012) Immunostimulant effect of Egyptian propolis in rabbits. Sci World J. https://doi.org/10.1100/2012/901516
Bourlioux P, Koletzko B, Guarner F, Braesco V (2003) The intestine and its microflora are partners for the protection of the host: report on the danone symposium ‘The Intelligent Intestine’, held in Paris, June 14, 2002. Am J Clin Nutr 78:675–683
Hegazi AG, Abd El Hady FK (2002) Egyptian propolis: 3. Antioxidant, antimicrobial activities and chemical composition of propolis from reclaimed lands. Z Naturforsch C 57:395–402
Zenner L, Callait MP, Granier C, Chauve C (2003) In vitro effect of essential oils from Cinnamomum aromaticum, Citrus limon and Allium sativum on two intestinal flagellates of poultry, Tetratrichomonas gallinarum and Histomonas meleagridis. Parasite 10:153–157
Innes EA (2010) A brief history and overview of Toxoplasma gondii. Zoonoses Public Health 57:1–7
Robert-Gangneux F, Dardé M (2012) Epidemiology of and diagnostic strategies for Toxoplasmosis. Clin Microbiol Rev 25:264–296
Ansell BR, McConville MJ, Ma'ayeh SY, Dagley MJ, Gasser RB, Svärd SG, Jex AR (2015) Drug resistance in Giardia duodenalis. Biotechnol Adv 33:888–901
Abdel-Fattah NS, Nada OH (2007) Effect of propolis versus metronidazole and their combined use in treatment of acute experimental giardiasis. J Egypt Soc Parasitol 37:691–710
Valencia D, Alday E, Robles-Zepeda R, Garibay-Escobar A, Galvez-Ruiz JC, Salas-Reyes M, Jiménez-Estrada M, Velazquez-Contreras E, Hernandez J, Velazquez C (2012) Seasonal effect on chemical composition and biological activities of Sonoran propolis. Food Chem 131:645–651
de Brum VP, Tasca T, Evan Secor W (2017) Challenges and persistent questions in the treatment of Trichomoniasis. Curr Top Med Chem 17:1249–1265
Muzny CA, Schwebke JR (2013) The clinical spectrum of Trichomonas vaginalis infection and challenges to management. Sex Transm Infect 89:423–425
El Sayed H, Ahmad TA (2012) The use of propolis as vaccine's adjuvant. Vaccine 31:31–39
Wachter B, Syrowatka M, Obwaller A, Walochnik J (2014) In vitro efficacy of curcumin on Trichomonas vaginalis. Wien Klin Wochenschr 126:32–36
Kuk S, Yazar S, Dogan S, Çetinkayaü Ü, Sakalar Ç (2013) Molecular characterization of Acanthamoeba isolated from Kayseri well water. Turk J Med Sci 43:1–6
Topalkara A, Vural A, Polat Z, Toker MI, Arici MK, Ozan F, Cetin A (2007) In vitro amoebicidal activity of propolis on Acanthamoeba castellanii. J Ocul Pharmacol Ther 23:40–45
Alfellani MA, Stensvold CR, Vidal-Lapiedra A, Onuoha ES, Fagbenro-Beyioku AF, Clark CG (2013) Variable geographic distribution of Blastocystis subtypes and its potential implications. Acta Trop 126:11–18
Coyle CM, Varughese J, Weiss LM, Tanowitz HB (2012) Blastocystis: to treat or not to treat. Clin Infect Dis 54:105–110
Atkinson HJ, Babbitt PC, Sajid M (2009) The global cysteine peptidase landscape in parasites. Trends Parasitol 25:573–581
Vital PG, Rivera WL (2009) Antimicrobial activity and cytotoxicity of Chromolaena odorata (L. f.) King and Robinson and Uncaria perrottetii (A. Rich) Merr. Extracts J Med Plant Res 3:511–518
Nasirudeen AM, Hian YE, Singh M, Tan KS (2004) Metronidazole induces programmed cell death in the protozoan parasite Blastocystis hominis. Microbiol 150:33–43
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We also would like to thank of financial support by Vice Chancellors for Research of Mazandaran University of Medical Sciences, Sari, Iran (Grant number: 6873).
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MF and MK designed the study and revised the manuscript. SA wrote the draft of the manuscript. JA performed paper selection processing and critical review. All authors read and approved the final manuscript.
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This study was reviewed and approved by the ethical committee at Mazandaran University of Medical Sciences (IR.MAZUMS.REC.1398. 6873).
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Asfaram, S., Fakhar, M., Keighobadi, M. et al. Promising Anti-Protozoan Activities of Propolis (Bee Glue) as Natural Product: A Review. Acta Parasit. 66, 1–12 (2021). https://doi.org/10.1007/s11686-020-00254-7
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DOI: https://doi.org/10.1007/s11686-020-00254-7