Abstract
Clarisia racemosa Ruiz & Pav is a neotropical species found in humid forests from southern Mexico to southern Brazil. There are few studies related to the ethnopharmacological use of C. racemosa. Our objective was to evaluate the hydroalcoholic extract of C. racemosa as a potential antiparasitic agent. For this, we performed in vitro assays against strains of Leishmania amazonensis, Trypanosoma cruzi, Plasmodium falciparum, and Schistosoma mansoni. At the same time, immunomodulatory activity tests were carried out. The results demonstrated that the extract was able to stimulate and activate immune cells. In preliminary antiparasitic tests, structural modifications were observed in the promastigote form of L. amazonensis and in adult worms of S. mansoni. The extract was able to inhibit the growth of trypomastigote form of T. cruzi and finally showed low antiparasitic activity against strains of P. falciparum. It is pioneering work and these results demonstrate that C. racemosa extract is a promising alternative and contributes to the arsenal of possible forms of treatment to combat parasites.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The authors made available the data presented in this work.
References
Abd-Allah M, Abdelwahab M, Aly NS, Amer OS, Sarhan M (2022) In vitro schistosomicidal activity of five common species of red sea cone snail muscle extracts. Al-Azhar Bull Sci 33(2C):111–119. https://doi.org/10.21608/ABSB.2022.140291.1187
Albuquerque Nerys LL, Jacob ITT, Silva AR, Oliveira AM, Rocha WRV, Pereira DTM, Lima MDCA (2022) Photoprotective, biological activities and chemical composition of the non-toxic hydroalcoholic extract of Clarisia racemosa with cosmetic and pharmaceutical applications. Ind Crops Prod 180:114762. https://doi.org/10.1016/j.indcrop.2022.114762
Almeida LMSD, Farani PGS, Tosta LA, Silvério MS, Sousa OVD, Mattos ACAD, Faria-Pinto P (2012) In vitro evaluation of the schistosomicidal potential of Eremanthus erythropappus (DC) McLeisch (Asteraceae) extracts. Nat Prod Res 26(22):2137–2143. https://doi.org/10.1080/14786419.2011.631135
Araújo DMF, Cruz Filho IJ, Santos T, Pereira DTM, Marques DSC, de Lima ADCA, Nogueira F (2022) Biological activities and physicochemical characterization of alkaline lignins obtained from branches and leaves of Buchenavia viridiflora with potential pharmaceutical and biomedical applications. Int J Biol Macromol 219:224–245. https://doi.org/10.1016/j.ijbiomac.2022.07.225
Barusrux S, Phiboonchaiyanan PP, Khamphio M, Weerapreeyakul N, Siriamornpun S (2018) Effects of jujube fruit extract on peripheral blood mononuclear cell proliferation, cytokine productions and intracellular hydrogen peroxide level. Walailak J Sci Technol (WJST) 15(8):561–568
Biswas N, Mandal L (2023) Treatment strategies against selected common tropical parasitic diseases. In: Viral, parasitic, bacterial, and fungal infections. Academic Press, pp 383–388. https://doi.org/10.1016/B978-0-323-85730-7.00058-8
Castañeda JS, Suta-Velásquez M, Mateus J, Pardo-Rodriguez D, Puerta CJ, Cuéllar A, Cuervo C (2021) Preliminary chemical characterization of ethanolic extracts from Colombian plants with promising anti-Trypanosoma cruzi activity. Exp Parasitol 223:108079. https://doi.org/10.1016/j.exppara.2021.108079
Christina YI, Rifa’i M, Widodo N, Djati MS (2022) Comparative study of antiproliferative activity in different plant parts of Phaleria macrocarpa and the underlying mechanism of action. Sci World J. https://doi.org/10.1155/2022/3992660
Cruz-Filho IJ, Silva Barros BR, Souza Aguiar LM, Navarro CDC, Ruas JS, de Lorena VMB, Maior AMS (2019) Lignins isolated from prickly pear cladodes of the species Opuntia fícus-indica (Linnaeus) Miller and Opuntia cochenillifera (Linnaeus) Miller induces mice splenocytes activation, proliferation and cytokines production. Int J Biol Macromol 123:1331–1339
Cruz-Filho IJ, Duarte DMFA, Lima DDCA, Marques DSC, dos Santos FAB, Alves LC, Lima MDCA (2023) In vitro evaluation of alkaline lignins as antiparasitic agents and their use as an excipient in the release of benznidazole. Int J Biol Macromol. https://doi.org/10.1016/j.ijbiomac.2023.123339
Da Rocha RET, De Almeida Júnior ASA, Júnior NCP, Do Nascimento AV, Leite NMS, De Oliveira JF, Alves LC (2022) Synthesis, in vitro schistosomicidal activity and ultrastructural alterations caused by thiosemicarbazones and thiazolidinones against juvenile and adult Schistosoma mansoni worms (Sambon, 1907). Mol Biochem Parasitol 252:111520. https://doi.org/10.1016/j.molbiopara.2022.111520
Daltro SRT, Santos IP, Barros PL, Moreira DRM, Tomassini TCB, Ribeiro IM, Soares MBP (2021) In vitro and in vivo immunomodulatory activity of physalis angulata concentrated ethanolic extract. Planta Med 87(01/02):160–168. https://doi.org/10.1055/a-1237-4268
Ding S, Jiang H, Fang J (2018) Regulation of immune function by polyphenols. J Immunol Res. https://doi.org/10.1155/2018/1264074
Djouwoug CN, Gounoue RK, Ngueguim FT, NankapTsakem JM, Gouni CD, Kandeda AC, Dimo T (2021) In vitro and in vivo antiplasmodial activity of hydroethanolic bark extract of Bridelia atroviridis müll. Arg. (Euphorbiaceae) and lc-ms-based phytochemical analysis. J Ethnopharmacol 66:113424. https://doi.org/10.1016/j.jep.2020.113424
Duvall RH, DsWitt WB (1967) An improved perfusion technique for recovering adult schistosomes from laboratory animals. ASTMH 16(4):483–486
El-Seedi HR, Khalifa SA, Mohamed AH, Yosri N, Zhao C, El-Wakeil N, Verpoorte R (2022) Plant extracts and compounds for combating schistosomiasis. Phytochem Rev. https://doi.org/10.1007/s11101-022-09836-x
Ferreira LL, de Moraes J, Andricopulo AD (2022) Approaches to advance drug discovery for neglected tropical diseases. Drug Discov Today 27(8):2278–2287. https://doi.org/10.1016/j.drudis.2022.04.004
Gouveia AL, Santos FA, Alves LC, Cruz-Filho IJ, Silva PR, Jacob IT, Alves de Lima MDC (2022) Thiazolidine derivatives: in vitro toxicity assessment against promastigote and amastigote forms of Leishmania infantum and ultrastructural study. Exp Parasitol 236:108253. https://doi.org/10.1016/j.exppara.2022.108253
Gutiérrez-Rebolledo GA, Drier-Jonas S, Jiménez-Arellanes MA (2017) Natural compounds and extracts from Mexican medicinal plants with anti-leishmaniasis activity: an update. Asian Pac J Trop Med 10(12):1105–1110. https://doi.org/10.1016/j.apjtm.2017.10.016
Igoli JO, Teles YC, Atawodi SE, Ferro VA, Watson DG (2022) ethnopharmacological strategies for drug discovery against African neglected diseases. Front Pharmacol. https://doi.org/10.3389/fphar.2022.851064
Jansen O, Tchinda AT, Loua J, Esters V, Cieckiewicz E, Ledoux A, Frédérich M (2017) Antiplasmodial activity of Mezoneuron benthamianum leaves and identification of its active constituents. J Ethnopharmacol 203:20–26. https://doi.org/10.1016/j.jep.2017.03.021
Khalil LM, Azzam AM, Mohamed HA, Aboueldahab MM, Taha HA, Soliman MI (2016) In vitro effects of the stem extracts of the plant Calotropis procera on Schistosoma mansoni adult worms. Egypt J Zoology 66(66):217–230
Kurnia Hartati F, Bambang Widjanarko S, Dewanti Widyaningsih T, Rifa’i M (2017) Antioxidant activity and immunomodulator of Indonesia black rice (Oryza sativa L. indica) extract. J Global Pharma Technol 176–182
Kwansa-Bentum B, Agyeman K, Larbi-Akor J, Anyigba C, Appiah-Opong R (2019) In vitro assessment of antiplasmodial activity and cytotoxicity of Polyalthia longifolia leaf extracts on Plasmodium falciparum strain NF54. Malar Res Treat. https://doi.org/10.1155/2019/6976298
Lima-Aires A, Ximenes ECPA, Barbosa VX, Silva Góes AJ, Souza VMO, Azevedo Albuquerque MCP (2014) β-lapachone: a naphthoquinone with promising antischistosomal properties in mice. Phytomedicine 21(3):261–267. https://doi.org/10.1016/j.phymed.2013.08.012
Magalhães LM, Gollob KJ, Zingales B, Dutra WO (2022) Pathogen diversity, immunity, and the fate of infections: lessons learned from Trypanosoma cruzi human–host interactions. Lancet Microbe 3(9):711-e722. https://doi.org/10.1016/S2666-5247(21)00265-2
Mariano RL, Montagnini DL, Manuquian HA, Katchborian-Neto A, Ribeiro Cavallari PSDS, de Almeida SG, Silva MLAE (2022) Antileishmanial activity and chemical composition of hydroalcoholic extracts from different parts of Handroanthus impetiginosus (Ipê-Roxo). Rev Bras Farmacogn 32:851–857. https://doi.org/10.1007/s43450-022-00313-2
Martín-Escolano J, Marín C, Rosales MJ, Tsaousis AD, Medina-Carmona E, Martín-Escolano R (2022) An updated view of the trypanosoma cruzi life cycle: intervention points for an effective treatment. ACS Infect Dis 8(6):1107–1115. https://doi.org/10.1021/acsinfecdis.2c00123
Mashhadi F, Ghorbani Nohooji M, Yaraee R (2021) Immunomodulatory effects of Origanum vulgare L. and Origanum Majorana L. ethanolic extracts in vitro. Immunoregulation 4(1):21–32
Meira CS, Guimarães ET, Dos Santos JAF, Moreira DRM, Nogueira RC, Tomassini TCB, Soares MBP (2015) In vitro and in vivo antiparasitic activity of Physalis angulata L. concentrated ethanolic extract against Trypanosoma cruzi. Phytomedicine 22(11):969–974. https://doi.org/10.1016/j.phymed.2015.07.004
Mengarda AC, Iles B, Longo JPF, de Moraes J (2023) Recent approaches in nanocarrier-based therapies for neglected tropical diseases. Wiley Interdiscip Rev Nanomed Nanobiotechnol 15(2):e1852. https://doi.org/10.1002/wnan.1852
Mileo AM, Nisticò P, Miccadei S (2019) Polyphenols: immunomodulatory and therapeutic implication in colorectal cancer. Front Immunol 10:729. https://doi.org/10.3389/fimmu.2019.00729
Moradin N, Descoteaux A (2012) Leishmania promastigotes: building a safe niche within macrophages. Front Cell Infect 2:121
PAHO (2023) Organização Pan-Americana da Saúde. Leishmaniose. https://www.paho.org/pt/topicos/leishmaniose. Accessed 23 Mar 2003
Parbat AY, Malode GP, Shaikh AR, Panchale WA, Manwar JV, Bakal RL (2021) Ethnopharmacological review of traditional medicinal plants as immunomodulator. WJBPHS 6(2):043–055
Pereira IO, Marques MJ, Pavan ALR, Codonho BS, Barbiéri CL, Beijo LA, Dos Santos MH (2010) Leishmanicidal activity of benzophenones and extracts from Garcinia brasiliensis Mart. fruits. Phytomedicine 17(5):339–345. https://doi.org/10.1016/j.phymed.2009.07.020
Pereira KL, Vasconcelos NB, Braz JV, Inacio JD, Estevam CS, Correa CB, Scher R (2020) Ethanolic extract of Croton blanchetianus ball induces mitochondrial defects in Leishmania amazonensis promastigotes. An Acad Bras Ciênc. https://doi.org/10.1590/0001-3765202020180968
Quintero-Pertuz H, Veas-Albornoz R, Carrillo I, González-Herrera F, Lapier M, Carbonó-Delahoz E, Maya JD (2022) Trypanocidal effect of alcoholic extract of Castanedia santamartensis (Asteraceae) leaves is based on altered mitochondrial function. Biomed Pharmacother 148:112761. https://doi.org/10.1016/j.biopha.2022.112761
Ramirez B, Bickle Q, Yousif F, Fakorede F, Mouries MA, Nwaka S (2007) Schistosomes: challenges in compound screening. Expert Opin Drug Discov 2(sup1):S53–S61. https://doi.org/10.1517/17460441.2.S1.S53
Renslo AR, McKerrow JH (2006) Drug discovery and development for neglected parasitic diseases. Nat Chem Biol 2(12):701–710. https://doi.org/10.1038/nchembio837
Rieger AM, Nelson KL, Konowalchuk JD, Barreda DR (2011) Modified annexin V/propidium iodide apoptosis assay for accurate assessment of cell death. JoVE (j vis Exp) 50:e2597. https://doi.org/10.3791/2597
Santos LS, Fernandes CC, Santos LS, Candido ACBB, Magalhães LG, Andrade G, Miranda MLD (2022) Phenolic compounds and biological activities of ethanolic extract from Capsicum chinense unripe fruit (var. bode pepper). Mediterr J Chem 12(1):31–37
Silva RS, Nascimento Santos DKD, Sousa GF, Araújo Sobral M, de Miranda PHO, de Sousa BR, Melo CML (2021) Antifungical and immunomodulatory activities from Caesalpinia pulcherrima extracts. Sci Electron Arch. https://doi.org/10.36560/14920211454
Silva Alves RR, Rodrigues JGM, Teles-Reis A, Nogueira RA, Licá ICL, Lira MGS, Miranda GS (2020) Antiparasitic effects of ethanolic extracts of Piper arboreum and Jatropha gossypiifolia leaves on cercariae and adult worms of Schistosoma mansoni. Parasitology 147(14):1689–1699. https://doi.org/10.1017/S003118202000181X
Smithers SR, Terry RJ (1965) The infection of laboratory hosts with cercariae of Schistosoma mansoni and the recovery of the adult worms. Parasitology 55(4):695–700. https://doi.org/10.1017/S0031182000086248
Sousa GF, Santos DKDDN, Silva RS, Barros BRDS, Cruz-Filho IJ, Ramos BDA, Lagos de Melo CM (2021) Evaluation of cytotoxic, immunomodulatory effects, antimicrobial activities and phytochemical constituents from various extracts of Passiflora edulis F. flavicarpa (Passifloraceae). Nat Prod Res 35(24):5862–5866. https://doi.org/10.1080/14786419.2020.1798660
Van Assche T, Deschacht M, da Luz RAI, Maes L, Cos P (2011) Leishmania–macrophage interactions: insights into the redox biology. Free Radic Biol Med 51(2):337–351. https://doi.org/10.1016/j.freeradbiomed.2011.05.011
WHO. World Health Organization. World chagas disease day 2022 https://www.who.int/campaigns/world-chagas-disease-day/2022. Accessed 30 Mar 2023a
WHO. World Health Organization. World malaria report 2022 https://www.who.int/teams/global-malaria-programme/reports/world-malaria-report-2022. Accessed 30 Mar 2023b
WHO. World Health Organization. Schistosomiasis https://www.who.int/news-room/fact-sheets/detail/schistosomiasis Accessed 30 Mar 2023c
Yones DA, Badary DM, Sayed H, Bayoumi SA, Khalifa AA, El-Moghazy AM (2016) Comparative evaluation of anthelmintic activity of edible and ornamental pomegranate ethanolic extracts against Schistosoma mansoni. BioMed Res Int. https://doi.org/10.1155/2016/2872708
Acknowledgements
The authors thank the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for a grant and M.C.A. Lima Fellowship (Process 306865/612020-3); Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES—Finance Code N° 001) and the Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE). J.V.R. Rocha and I.J. Cruz Filho would like to thank FACEPE for the Graduate Scholarship (Process PBPG-1832-4.01/22) and Researcher Fixation Scholarships (Process BFP-0038-4.03/21), respectively. In addition, M.C.A. Lima and A.L. Aires would like to thank FACEPE Research Project Aid (Process APQ-0498-4.03/19) and (Process APQ-Emergent 1181-4.03/22), respectively. We would like to thank Mil Madeiras Preciosas, a subsidiary of the Swiss group Precious Woods (http://preciouswoods.com.br/) for supplying the Clarisia racemosa trunks. Thanks to MR4, who provided us with the Plasmodium falciparum MRA-1029 strain provided by Andrew Talman, Robert Sinden that we used in the trials. The work was partially supported by the FCT project reference CIRCNA/BRB/0281/2019_AMAZING and GHTM-UID/Multi/04413/2013.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could appear to influence the work reported in this article.
Ethical approval
The study was approved by the UFPE Animal Ethics Committee (n° 0060/2019 CEUA/UFPE).
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
da Cruz Filho, I.J., Duarte, D.M.F.A., Marques, D.S.C. et al. Evaluation of the hydroalcoholic extract of Clarisia racemosa as an antiparasitic agent: an in vitro approach. 3 Biotech 13, 391 (2023). https://doi.org/10.1007/s13205-023-03799-2
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-023-03799-2