Abstract
Echinococcosis is a common and endemic disease that affects both humans and animals. In this study, the in vitro activities of methanolic extracts of Ruta graveolens, Peganum harmala aerial parts, and Citrullus colocynthis seeds against protoscolosis and isolated bacterial strains from hydatid cysts were assessed using disc diffusion methods and Minimum Inhibitory Concentration (MIC). The chemical composition of three methanolic extracts was studied using LC–MS. After 3 h of exposure to 40 mg/mL R. graveolens extract, a tenfold protoscolocidal effect was seen when compared to the convintional medication (ABZ) for the same duration (P < 0.05). The bacteria listed below were isolated from hydatid cyst fluid collected from a variety of sick locations, including the lung and liver. Micrococcus spp., E. coli, Klebsiella oxytoca, Enterobacter aerogenes, Enterobacter amnigenus, Pseudomonas aeruginosa, Staphylococcus xylosus, and Achromobacter xylosoxidans are among the bacteria that have been identified. The most effective extract was R. graveolens, followed by P. harmala and C. colocynthis, according to the results of antibacterial activity using the disc diffusion method. R. graveolens extract had the lowest MIC values (less than 2 mg/mL) against all microorganisms tested. This shows that the R. graveolens extract has additional properties, such as the ability to be both scolocidal and bactericidal. Because these bacteria are among the most prevalent pathogenic bacteria that increase the risk of secondary infection during hydatid cysts, the results of inhibitory zones and MICs of the R. graveolens methanol extract are considered highly promising.
Similar content being viewed by others
References
Abdullah M, Ali I, Haleem KS, Rehman AU, Qayyum S, Niaz Z, Sultana N (2021) Molecular and biochemical characterization of Echinococcus spp. In hydatid cyst fluid collected from human and livestock in northern khyber pakhtunkhwa and gilgit baltistan. J Anim Plant Sci 31(5):1293–1301
Ahmed CN, Hamad KK, Qadir FA (2019) Haemonchus contortus as a model in assessing activity of Citrullus colocynthis fruit extract to control benzimidazole-resistant parasitic nematodes. ZANCO J Pure Appl Sci 31(5):61–70
Ahmed AB, Ras R, Mahmoud AF, El-Ghazaly E, Widmer G, Dahshan H, Elsohaby I (2021) Prevalence and bacterial isolation from hydatid cysts in dromedary camels (Camelus dromedarius) slaughtered at Sharkia abattoirs. Egypt J Parasit Dis 45(1):236–243
Aitken MM, Jones PW, Hall GA, Hughes DL, Collis KA (1978) Effects of experimental Salmonella dublin infection in cattle given Fasciola hepatica thirteen weeks previously. J Comp Pathol 88(1):75–84
Al-Arabi FY, Mehdi MAH, Farooqui M, Pradhan V (2019) The effect of Aloe vera extracts on the viability of Echinococcus granulosus protoscolices. Int Res J Pharm 10(4):184–189
Al-Asoufi A, Khlaifat A, Tarawneh AA, Alsharafa K, Al-Limoun M, Khleifat K (2017) Bacterial quality of urinary tract infections in diabetic and non diabetics of the population of Ma’an province. Jordan Pak J Biol Sci 20(4):179–188
Ali SA, Dawood KA, Al-Oumashi GB (2012) Hydatidosis of cattle with secondary bacterial invaders. Kufa J Vet Med Sci 3(2):104–110
Ali AA, Alian MA, Elmahi HA (2013) Phytochemical analysis of some chemical metabolites of Colocynth plant [Citrullus colocynthis L.] and its activities as antimicrobial and antiplasmidial. J Basic Appl Sci Res 3(5):228–236
Allaq AA, Sidik NJ, Abdul-Aziz A, Alkamil AMA, Elengoe A, Yahya EB, Abdulsamad MA (2021) Epidemiological studies of the novel Coronavirus (COVID-19) in Libya. Pak J Biol Sci 18(1–2):7–16
Al-Shuneigat JM, Al-Tarawneh IN, Al-Qudah MA, Al-Sarayreh SA, Al-Saraireh YM, Alsharafa KY (2015) The chemical composition and the antibacterial properties of Ruta graveolens L. essential oil grown in Northern Jordan. Jordan J Biological Sci 8(2):139–143
Alzoreky NS, Nakahara K (2003) Antibacterial activity of extracts from some edible plants commonly consumed in Asia. Int J Food Microbiol 80(3):223–230
Amabye TG, Shalkh TM (2015) Phytochemical screening and evaluation of antibacterial activity of Ruta graveolens L.—A medicinal plant grown around Mekelle, Tigray, Ethiopia. Nat Prod Chem Res 3:195. https://doi.org/10.4172/2329-6836.1000195
Asgarpanah J, Khoshkam R (2012) Phytochemistry and pharmacological properties of Ruta graveolens L. J Med Plants Res 6(23):3942–3949
Blanton RE, Wachira TM, Zeyhle EE, Njoroge EM, Magambo JK, Schantz PM (1998) Oxfendazole treatment for cystic hydatid disease in naturally infected animals. Antimicrob Agents Chemother 42(3):601–605
Boes J, Helwigh AB (2000) Animal models of intestinal nematode infections of humans. Parasitology 121(S1):S97–S111
Bourhia M, Messaoudi M, Bakrim H, Mothana RA, Sddiqui NA, Almarfadi OM, Benbacer L (2020) Citrullus colocynthis (L.) Schrad: chemical characterization, scavenging and cytotoxic activities. Open Chem 18(1):986–994
Bourhia M, Bouothmany K, Bakrim H, Hadrach S, Salamatullah AM, Alzahrani A, Laglaoui A (2021) Chemical profiling, antioxidant, antiproliferative, and antibacterial potentials of chemically characterized extract of Citrullus colocynthis L. Seeds Sep 8(8):114
Darabpour E, Bavi AP, Motamedi H, Nejad SMS (2011) Antibacterial activity of different parts of Peganum harmala L. growing in Iran against multi-drug resistant bacteria. EXCLI J 10:252
de Carvalho LSA, Queiroz LS, Alves Junior IJ, Almeida AC, Coimbra ES, de Faria Pinto P, Da Silva Filho AA (2019) In vitro schistosomicidal activity of the alkaloid-rich fraction from Ruta graveolens L (Rutaceae) and its characterization by UPLC-QTOF-MS. Evid-Based Complement Altern Med 2:2
De Queiroz AC, Dias T, Da Matta CBB, Cavalcante Silva LHA, de Araújo-Júnior JX, de Araújo GB, Alexandre-Moreira MS (2014) Antileishmanial activity of medicinal plants used in endemic areas in northeastern Brazil. Evid-Based Complement Altern Med 2:2
Dhakad PK, Sharma PK, Kumar S (2017) A review on phytochemical studies and biological potential of Citrullus colocynthis (L.) Schrad (Cucurbitaceae). J Bioeng Biosci 5(4):55–64
dos Santos PRD, de Lima Moreira D, Guimarães EF, Kaplan MAC (2001) Essential oil analysis of 10 Piperaceae species from the Brazilian Atlantic forest. Phytochemistry 58(4):547–551
Doskaliyev A, Seidakhmetova R, Tutai DS, Goldaeva K, Surov VK, Adekenov SM (2021) Alkaloids of Peganum harmala L. and their pharmacological activity. Open Access Maced J Med Sci 9:766–775
Durgadevi PSKS, Saravanan A, Uma S (2019) Antioxidant potential and antitumour activities of Nendran banana peels in breast cancer cell line. Indian J Pharm Sci 81(3):464–473
Elansary HO, Szopa A, Kubica P, Ekiert H, El-Ansary DO, Al-Mana A, Mahmoud EA (2020) Polyphenol content and biological activities of Ruta graveolens L. and Artemisia abrotanum L. in northern Saudi Arabia. Processes 8(5):531
El-Zayat MM, Eraqi MM, Alfaiz FA, Elshaer MM (2021) Antibacterial and antioxidant potential of some Egyptian medicinal plants used in traditional medicine. J King Saud Univ Sci 33(5):101466
Esiyok D, Otles S, Akcicek E (2004) Herbs as a food source in Turkey. Asian Pac J Cancer Prev 5(3):334–339
Fallah M, Kavand A, Mashouf RY (2014) Infected hydatid cysts bacteria in slaughtered livestock and their effects on protoscoleces degeneration. Jundishapur J Microbiol 7(6):e10135
Fatma B, Fatiha M, Elattafia B, Noureddine D (2016) Phytochemical and antimicrobial study of the seeds and leaves of Peganum harmala L. against urinary tract infection pathogens. Asian Pac J Trop Dis 6(10):822–826
Friedman ND, Kaye KS, Stout JE, McGarry SA, Trivette SL, Briggs JP, Walton AL (2002) Health care–associated bloodstream infections in adults: a reason to change the accepted definition of community-acquired infections. Ann Intern Med 137(10):791–797
Hadadi Z, Nematzadeh GA, Ghahari S (2020) A study on the antioxidant and antimicrobial activities in the chloroformic and methanolic extracts of 6 important medicinal plants collected from North of Iran. BMC Chem. 14(1):1–11
Hijjawi NS, Al-Radaideh AM, Rababah EM, Al-Qaoud KM, Bani-Hani KE (2018) Cystic echinococcosis in Jordan: a review of causative species, previous studies, serological and radiological diagnosis. Acta Trop 179:10–16
Ivanova A, Mikhova B, Najdenski H, Tsvetkova I, Kostova I (2005) Antimicrobial and cytotoxic activity of Ruta graveolens. Fitoterapia 76(3–4):344–347
JahedKhaniki GR, Kia EB, Raei M (2013) Liver condemnation and economic losses due to parasitic infections in slaughtered animals in Iran. J Parasit Dis 37(2):240–244
Khleifat K, Abboud M, Al-Shamayleh W, Jiries A, Tarawneh K (2006) Effect of chlorination treatment on gram negative bacterial composition of recycled wastewater. Pak J Biol Sci 9:1660–1668
Khleifat KM, Tarawneh KA, Ali Wedyan M, Al-Tarawneh AA, Al Sharafa K (2008) Growth kinetics and toxicity of Enterobacter cloacae grown on linear alkylbenzene sulfonate as sole carbon source. Currt Microbiol 57(4):364–370
Khleifat KM, Halasah RA, Tarawneh KA, Halasah Z, Shawabkeh R, Wedyan MA (2010) Biodegradation of linear alkylbenzene sulfonate by Burkholderia sp.: effect of some growth conditions. Int J Agr Biol 12:17–25
Kumar VP, Chauhan NS, Padh H, Rajani M (2006) Search for antibacterial and antifungal agents from selected Indian medicinal plants. J Ethnopharm 107(2):182–188
Malekifard F, Keramati F (2018) Susceptibility of protoscoleces of hydatid cyst to various concentrations of oak gall (quercus infectoria olivier) extract at different exposure times in vitro. Zahedan. J Res Med Sci 20:5
Mamedov NA, Pasdaran A, Mamadalieva NZM (2018) Pharmacological studies of Syrian rue (Peganum harmala L., Zygophyllaceae). Int J Second Metab 5(1):1–6
Moazeni M, Larki S, Saharkhiz MJ, Oryan A, AnsaryLari M, MootabiAlavi A (2014) In vivo study of the efficacy of the aromatic water of Zataria multiflora on hydatid cysts. Antimicrob Agents Chemother 58(10):6003–6008
Moazeni M, SaadatyArdakani ZS, Saharkhiz MJ, Jalaei J, Khademolhoseini AA, Abad SE (2017) In vitro ovicidal activity of Peganum harmala seeds extract on the eggs of Fasciola hepatica. J Paras Dis 41(2):467–472
Molnar M, Tomić M, Pavić V (2018) Coumarinyl thiosemicarbazides as antimicrobial agents. Pharm Chem J 51(12):1078–1081
Moloudizargari M, Mikaili P, Aghajanshakeri S, Asghari MH, Shayegh J (2013) Pharmacological and therapeutic effects of Peganum harmala and its main alkaloids. Pharmacogn Rev 7(14):199
Monteiro DU, Azevedo MI, Weiblen C, Botton SDA, Funk NL, Da Silva CDB, De La Rue ML (2017) In vitro and ex vivo activity of Melaleuca alternifolia against protoscoleces of Echinococcus ortleppi. Parasitology 144(2):214–219
Mounira K, Farah R, Rachida B, Halima A (2021) Preliminary phytochemical screening, quantification of phenolic compounds, of plant extract from Chenopodium quinoa. Alger J Biosci 2(01):42–45
Nabaei M, Mesbah AR, Ghavami H, Saeidinia A, Keihanian F (2014) Effects of Ruta graveolens extract on histopathologic changes in mice livers. Int J Pharm Res Schol 3(2):675–680
Najim TM, Shahooth MA, Khamees AS (2020) Isolation of bacteria associated with hepatic hydatid cyst of iraqi sheep. Eur J Mol Clin Med 7(11):972–976
Nasrieh MA, Abdel-Hafez SK, Kamhawi SA, Craig PS, Schantz PM (2003) Cystic echinococcosis in Jordan: socioeconomic evaluation and risk factors. Parasitol Res 90(6):456–466
Nenaah G (2010) Antibacterial and antifungal activities of (beta)-carboline alkaloids of Peganum harmala (L) seeds and their combination effects. Fitoterapia 81(7):779–782
Niroumand MC, Farzaei MH, Amin G (2015) Medicinal properties of Peganum harmala L. in traditional Iranian medicine and modern phytotherapy: a review. J Tradit Chin Med 35(1):104–109
Oran SA (2014) The status of medicinal plants in Jordan. J Agric Sci Technol A 4:6
Oran SA, Al-Eisawi DM (1998) Check-list of medicinal plants in Jordan. Dirasat 25(2):84–112
Patel MH, Patel AM, Patel SM, Ninama GL, Patel KR, Lavingia BC (2011) Antifungal susceptibility testing to determine mic of amphotericine b, fluconazole and ketoconazole against ocular fungal infection. Nat J Comm Med 2:302–305
Pathak S, Multani AS, Banerji P, Banerji P (2003) Ruta 6 selectively induces cell death in brain cancer cells but proliferation in normal peripheral blood lymphocytes: A novel treatment for human brain cancer. Int J Oncol 23(4):975–982
Pavić V, Flačer D, Jakovljević M, Molnar M, Jokić S (2019) Assessment of total phenolic content, in vitro antioxidant and antibacterial activity of Ruta graveolens L. extracts obtained by choline chloride based natural deep eutectic solvents. Plants 8(3):69
Qaralleh H, Khleifat KM, Al-Limoun MO, Alzedaneen FY, Al-Tawarah N (2019) Antibacterial and synergistic effect of biosynthesized silver nanoparticles using the fungi Tritirachium oryzae W5H with essential oil of Centaurea damascena to enhance conventional antibiotics activity. Adv Nat Sci Nanosci. Nanotechnol 10(2):025016
Rezaee M, Hajighasemi F (2019) Sensitivity of hematopoietic malignant cells to Peganum harmala seed extract in vitro. J Basic Clin Physiol Pharmacol 7(1):21–26
Romero CD, Chopin SF, Buck G, Martinez E, Garcia M, Bixby L (2005) Antibacterial properties of common herbal remedies of the southwest. J Ethnopharm 99(2):253–257
Smyth JD, Barrett NJ (1980) Procedures for testing the viability of human hydatid cysts following surgical removal, especially after chemotherapy. Trans R Soc Trop Med Hyg 74(5):649–652
Sohrabi R, Moghaddam MT, Maghsood AH, Matini M, Moradkhani S, Fallah M (2018) Scolicidal effects of barberry (Berberis vulgaris), wild rue seed (Peganom harmala) and shirazian thyme (Zataria multiflora) extracts on protoscolices of hydatid cysts Zahedan. J Res Med Sci 20:12
Uma C, Sekar KG (2014) Phytochemical analysis of a folklore medicinal plant Citrullus colocynthis L. (bitter apple). Int J Pharmacogn Phytochem Res 2:6
Wang B, Jiang Y, Wang Z, Li F, Xing G, Peng X, Lv H (2015) Arsenic trioxide negatively affects Echinococcus granulosus. Antimicrob Agents Chemother 59(11):6946–6951
Wani I, Bhat Y, Khan N, Mir F, Nanda S, Shah OJ (2010) Concomitant rupture of hydatid cyst of liver in hepatic duct and gallbladder: case report. Gastroenterol Res 3(4):175
Wink M (2012) Medicinal plants: a source of anti-parasitic secondary metabolites. Molecules 17(11):12771–12791
Wolters B, Eilert U (1981) Antimicrobial substances in callus cultures of Ruta graveolens. Planta Med 43(10):166–174
Yones DA, Taher GA, Ibraheim ZZ (2011) In vitro effects of some herbs used in Egyptian traditional medicine on viability of protoscolices of hydatid cysts. Korean J Parasitol 49(3):255
Zeghir-Bouteldja R, Amri M, Aitaissa S, Bouaziz S, Mezioug D, Touil-Boukoffa C (2009) In vitro study of nitric oxide metabolites effects on human hydatid of Echinococcus granulosus. J Parasitol Res 2:1
Ziino G, Giuffrida A, Panebianco A, Bilei S (2009) Bacteria isolated from 25 hydatid cysts in sheep, cattle and goats. Vet Rec 165(8):234–236
Funding
The authors has received no funding for this research.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing Interests
The authors declare no competing interests.
Additional information
Communicated by Erko Stackebrandt.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Al Qaisi, Y.T., Khleifat, K.M., Oran, S.A. et al. Ruta graveolens, Peganum harmala, and Citrullus colocynthis methanolic extracts have in vitro protoscolocidal effects and act against bacteria isolated from echinococcal hydatid cyst fluid. Arch Microbiol 204, 228 (2022). https://doi.org/10.1007/s00203-022-02844-7
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-022-02844-7