Sains Malaysiana 53(7)(2024): 1617-1630

http://doi.org/10.17576/jsm-2024-5307-11

Antioxidant Activities and Laxative Effect of Bioactive Compounds from Cynara cardunculusvar. sylvestris

(Aktiviti Antioksidan dan Kesan Laksatif Sebatian Bioaktif daripada Cynara cardunculusvar. sylvestris)

FATMA TAJINI*, AWATEF JELASSI, AMAL HAMDANI, ALI SALEM, OLA ABDELHEDI, ABID OUERGHUI & HICHEM SEBAI

Laboratory of Functional Physiology and Valorization of Bio-Resources – Higher Institute of Biotechnology of Béja, University of Jendouba, Avenue Habib Bourguiba, B.P. 382, ​​9000 Béja, Tunisia

Received: 19 January 2024/Accepted: 4 June 2024

Abstract

The present study aims to investigate the antioxidant and anti-constipation activities of the derived phenolic extracts in ribs wild cardoon (Cynara sylvestris). Analysed extracts (acetone, methanol and aqueous) exhibited high level of phenolic compounds and excellent antioxidant activities with significant IC₅₀ values (p ≤0.05), as assessed by the DPPH radical-scavenging activity (0.84±0.08 - 2.44±0.007 μg/mL), ABTS cationic radical test (0.96 ±0.01- 136.67±6.75 μg/mL) and β-carotene bleaching assay (2.09±0.02-51.12±1.32 μg/mL). Also, higher levels of insoluble dietary fibers were found (56.18 ± 0.91% DW of neutral detergent fiber). The in vivo investigation was performed on Wistar rats to explore the ability of C. sylvestris aqueous extract (CSAE) in the enhancement of the gastrointestinal transit and the treatment of induced constipation by Loperamide (commercialized as Idium). A significant increase of 15, 24.5 and 32.4% in gastrointestinal motility was recordedwhen doses of CSAE increased (75, 150 and 300 mg/kg b.w, respectively). Food intake, water consumption, number and weight of stools were also increased in a dose-dependent manner, compared to the positive control (untreated). Moreover, CSAE provided significantly (p ≤0.05) and dose-dependently protection against oxidative stress by preserving normal antioxidant enzymes activities (SOD and GPx) in intestinal and colonic mucosa, and resorted hepatic enzymes (AST and ALT) and renal (urea and creatinine) levels to normal values. These results can be explained by the abundance of phenolic compounds and insoluble fibers in this plant. Therefore, its use can be encouraged in alimentary and pharmaceutical applications as antioxidant and laxative food supplements.

Keywords: Anti-constipation; Cynara cardunculus var. sylvestris; gastrointestinal motility; oxidative stress; phenolic compounds

Abstrak

Penyelidikan ini bertujuan untuk mengkaji aktiviti antioksidan dan anti-sembelit daripada ekstrak fenol yang diperoleh dalam kadun liar rusuk (Cynara sylvestris). Ekstrak yang dianalisis (aseton, metanol dan akueus) menunjukkan tahap sebatian fenol yang tinggi dan aktiviti antioksidan yang sangat baik dengan nilai IC₅₀ yang ketara (p≤0.05), seperti yang dinilai oleh aktiviti penangkapan radikal DPPH (0.84±0.08 - 2.44±0.007 μg/mL), ujian radikal kationik ABTS (0.96 ±0.01- 136.67±6.75 μg/mL) dan ujian pelunturan β-karotena (2.09±0.02-51.12±1.32 μg/mL). Juga, paras serat makanan tidak larut yang lebih tinggi didapati (56.18 ± 0.91% DW serat detergen neutral). Penyelidikanin vivo telah dijalankan ke atas tikus Wistar untuk mengkaji keupayaan ekstrak akueus C. sylvestris (CSAE) dalampeningkatan transit gastro usus dan rawatan sembelit yang disebabkan oleh Loperamide (dikomersialkan sebagai Idium). Peningkatan ketara sebanyak 15, 24.5 dan 32.4% dalam motiliti gastro usus direkodkan apabila dos CSAE meningkat (masing-masing 75, 150 dan 300 mg/kg b.w). Pengambilan makanan, penggunaan air, bilangan dan berat najis juga dinaikkan secara kebergantungan dos, berbanding kawalan positif (tidak dirawat). Tambahan pula CSAE memberikan perlindungan yang ketara (p≤0.05) dan kebergantungan dos terhadap tekanan oksidatif dengan mengekalkan aktiviti enzim antioksidan normal (SOD dan GPx) dalam usus dan kolon mukosa dan menjadikan tahap enzim hepatik (AST dan ALT) dan buah pinggang (urea dan kreatinin) kepada nilai normal. Keputusan ini boleh dijelaskan oleh banyaknya sebatian fenol dan gentian tidak larut dalam tumbuhan ini. Oleh itu, penggunaannya boleh digalakkan dalam pengaplikasian makanan dan farmaseutikal sebagai makanan tambahan antioksidan dan laksatif.

Kata kunci: Anti-sembelit; Cynara cardunculus var. sylvestris; motiliti gastro usus; sebatian fenol; tekanan oksidatif

REFERENCES

Ali, B.H. & Bashir, A.A. 1993. The effect of some alpha 2-adrenoceptor agonists and antagonists on gastrointestinal transit in mice: Influence of morphine, castor oil and glucose. Clinical and Experimental Pharmacology and Physiology 20(1): 1-6.

Al-Subhi, F.M.M. 2020. Artichoke as a tool to naturalantioxidants for lowering diabetics and hypolipidemia parameters. Alexandria Science Exchange Journal 11: 46-54.

Arab, H., Haddi, M.L. & Mehennaoui, S. 2009. Evaluation de la valeur nutritive par la composition chimique des principaux fourrages des zones aride et semi-aride en Algérie. Sciences & Technologie. C, Biotechnologies 30: 50-58.

Badary, O.A., Awad, A.S., Sherief, M.A. & Hamada, F.M.A. 2006. In vitro and in vivo effects of ferulic acid on gastrointestinal motility: Inhibition of cisplatin-induced delay in gastric emptying in rats. World Journal of Gastroenterology12: 5363-5367.

Baribeau, H.H. 2014. Manger mieux pour être au top. Edition La Semaine. https://www.renaud-bray.com

Ben Ammar, I., Harzallah-Skhiri, F., Mohandes, A.l. & Dridi, B. 2014. Morphological variability of wild cardoon (Cynara cardunculus L. var. sylvestris) population in North of Tunisia. ISRN Agronomy2: 1-9.

Ben Salem, M., Affes, H., Dhouibi, R., Charfi, S., Turki, M., Hammami, S., Ayedi, F., Sahnoun, Z., Zeghal, K.M. & Ksouda, K. 2022. Effect of artichoke (Cynara scolymus) on cardiac markers, lipid profile and antioxidants levels in tissue of HFD-induced obesity. Archives of Physiology and Biochemistry 128: 184-194.

Bettaieb, R., Sriti, J., Besbess, B., Mkaddmini, H.K., Hamrouni, S.I., Marzouk, B. & Ksouri, R. 2016. Effet de la provenance et du solvant d’extraction sur la teneur en composés phénoliques et les potentialités antioxydantes des graines de fenouil (Foeniculum vulgarae Mill.). Journal of New Sciences, Agriculture and Biotechnology 27(4) : 1478-1487.

Blanco, E., Sabetta, W., Danzi, D., Negro, D., Passeri, V., De Lisi, A., Paolocci, F. & Sonnante, G. 2018. Isolation and characterization of the flavonol regulator CcMYB12 from the globe artichoke (Cynara cardunculus var. scolymus (L.) Fiori). Plant Metabolism and Chemodiversity9: 941.

Blois, M.S. 1958. Antioxidant determinations by the use of a stable free radical. Nature 181: 1199-1200.

Bonithon-Kopp, C., Kronborg, O., Giacosa, A., Räth, U. & Faivre, J. 2001. Calcium and fibre supplementation in prevention of colorectal adenoma recurrence: A randomised intervention trial. European Cancer Prevention Organisation Study Group. Lancet 356(9238): 1300-1306.

Costil, V. & Jouët, P. 2017. Fiche.  Diététique sur la constipation. CREGG et SNFGE. https://www.cregg.org/wordpress/wp-content/uploads/2012/06/documents-fiches-constipation.pdf

Djenidi, H., Khennouf, S. & Bouaziz, A. 2020. Antioxidant activity and phenolic content of commonly consumed fruits and vegetables in Algeria. Progress in Nutrition 22: 224-235. 

Draper, H.H. & Hadley, M. 1990. Malondialdehyde determination as index of lipid peroxidation. Methods in Enzymology186: 421-431.

Ellman, G. 1959. Tissue sulfhydryl groups. Archives of Biochemistry and Biophysics 82: 70-77.

European Medicines Agency. EMA/HMPC/194014/2017. Community herbal monograph on Cynara cardunculus L. (syn. Cynara scolymus L.), folium. https://www.ema.europa.eu/en/medicines/herbal/cynarae-folium Accessed on 5 October 2022.

Falleh, H., Ksouri, R., Chaieb, K., Karray-Bouraoui, N., Trabelsi, N., Boulaaba, M. & Abdelly, C. 2008. Phenolic composition of Cynara cardunculus L. organs, and their biological activities. Comptes Rendus Biologies 331: 372-379.

Favier, J.C., Ireland-Ripert, J., Toque, C. & Feinberg, M. 1995. Répertoire Général Des Aliments: Table de Composition = Composition Tables. Paris: Technique & Documentation; INRA. p. 927.

Ferro, Y., Pujia, R., Mazza, E., Lascala, L., Lodari, O., Maurotti, S., Pujia, A. & Montalcini, T. 2022. A new nutraceutical (Livogen Plus®) improves liver steatosis in adults with non-alcoholic fatty liver disease. Journal of Translational Medicine20: 377.

Flohé, L. & Günzler, W.A. 1984. Assays of glutathione peroxidase. Methods in Enzymology105: 114-120.

Gamal, S.E., Walaa, E., Mohammed, A. & Mostafa, A. 2022. Extraction, identification, and quantification of bioactive compounds from globe artichoke (Cynara cardunculus var. scolymus). Sains Malaysiana51(9): 2843-2855.

Graf, D., Cagno, R.D., Fåk, F., Flint, J.H., Nyman, M., Saarela, M. & Watzl, B. 2015 Contribution of diet to the composition of the human gut microbiota. Microbial Ecology in Health and Disease26: 26164.

Gominho, J., Fernandez, J. & Pereira, H. 2000. Cynara cardunculus L. - a new fibre crop for pulp and paper production. Industrial Crops and Products 13(1): 1-10.

Jabri, M.A., Wannes, D., Hajji, N., Sakly, M., Marzouki, L. & Sebai, H. 2017. Role of laxative and antioxidant properties of Malva sylvestris leaves in constipation treatment. Biomedicine & Pharmacotherapy 89: 29-35.

Khaldi, S., Khelifi, M. & El Gazzah, M. 2013. Analysis of genetic variability in six Tunisian wild cardoon (Cynara cardunculus L. subsp. Flavescens Wiklund) populations. Genetic Resources and Crop Evolution  60: 723-729.

Kim, J.E., Choi, Y.J., Lee, S.J., Gong, J.E., Lee, Y.J., Sung, J.E., Jung, Y.S., Lee, H.S., Hong, J.T. & Hwang, D.Y. 2021. Antioxidant activity and laxative effects of tannin-enriched extract of Ecklonia cava in loperamide-induced constipation of SD rats. PLoS ONE 16(2): e0246363.

Kim, J.E., Yun, W.B., Lee, M.L., Choi, J.Y., Park, J.J., Kim, H.R., Song, B.R., Hong, J.T., Song, H.K. & Hwang, D.Y. 2019. Synergic laxative effects of an herbal mixture of Liriope platyphylla, Glycyrrhiza uralensis, and Cinnamomum cassia in loperamide-induced constipation of Sprague Dawley rats. Journal of Medicinal Food 22(3): 294-304.

Koubaa, I. & Damak, M. 2003. A new dilignan from Cynara cardunculus. Fitoterapia 74: 18-22.

Kurutas, E.B. 2016. The importance of antioxidants which play the role in cellular response against oxidative/nitrosative stress: Current state. Nutrition 15(1): 71.

Mahmoudi, S., Khali, M. & Mahmoudi, N. 2013. Etude de L’extraction des composés phénoliques de différentes parties de la fleur d’artichaut (Cynara scolymus L.). Nature and Technologie 9: 35-40.

Marco, G.J. 1968. A rapid method for evaluation of antioxidants. Journal of the American Oil Chemists' Society 45: 594-598.

Misra, H.P. & Fridovich, I. 1972. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. Journal of Biological Chemistry247: 3170-3175.

Naczk, M. & Shahidi, F. 2006. Phenolics in cereals, fruits and vegetables: Occurrence, extraction and analysis. Journal of Pharmaceutical and Biomedical Analysis 41: 1523-1542.

National Research Council (N.R.C.). 1985. Guide for the Care and the Use of Laboratory Animals. Bethesda: National Institute of Health. 20: 85.

Olofinsan, K.A., Rafiat, A.L.A. & Ajiboye, T.O. 2019. Loperamide induced neurotoxicity in rats: Biochemical and histological evidence. International Journal of Biochemistry, Bioinformatics and Biotechnology Studies4: 12-21.

Price, M.L., Van Scoyoc, S. & Butler, L.G. 1978. A critical evaluation of the vanillin reaction as an assay for tannin in sorghum grain. Journal of Agricultural and Food Chemistry26: 1214-1218.

Porro, C., Benameur, T., Cianciulli, A., Vacca, M., Chiarini, M., De Angelis, M. & Panaro, M.A. 2024. Functional and therapeutic potential of Cynara scolymus in health benefits. Nutrients 16: 872.

Re, R., Pellegrini, N., Proteggente, A., Pannala, A., Yang, M. & Rice-Evans, C. 1999. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biology and Medicine 26: 1231-1237.

Rosaria, A., Malfa, G.A., Santangelo, R., Bianchi, S., Pappalardo, F., Taviano, M.F., Miceli, N., Di Giacomo, C. & Tomasello, B. 2023. Wild artichoke (Cynara cardunculussubsp. sylvestris, Asteraceae) leaf extract: Phenolic profile and oxidative stress inhibitory effects on HepG2 cells. Molecules 28: 2475.

Rtibi, K., Selmi, S.,Wannes, D., Jridi, M., Marzouki, L. & Sebai, H. 2019. The potentiality of Thymus vulgaris aqueous extract to protect against delayed gastric emptying and colonic constipation in rats. RSC Advances 9: 20593-20602.

Saboonchian, F., Jamai, R. & Sarghein, S.H. 2014. Phenolic and flavonoid content of Elaeagnus angustifolia L. (leaf and flower). Avicenna Journal of Phytomedicine4: 231-238.

Sanz, M., Ceriello, A., Buysschaert, M., Chapple, I., Demmer, R.T., Graziani, F., Herrera, D., Jepsen, S., Lione, L., Madianos, P., Mathur, M., Montanya, E., Shapira, L., Tonetti, M. & Vegh, D. 2018. Scientific evidence on the links between periodontal diseases and diabetes: Consensus report and guidelines of the joint workshop on periodontal diseases and diabetes by the International Diabetes Federation and the European Federation of Periodontology. J. Clin. Periodontol. 45(2): 139-149.

Sarr, S.O., Fall, A.D., Gueye, R., Diop, A., Sene, B., Diatta, K., Ndiaye, B. & Diop, Y.M. 2015. Evaluation de l’activité antioxydante des extraits des feuilles de Aphania senegalensis (Sapindaceae) et de Saba senegalensis (Apocynaceae). International Journal of Biological and Chemical Sciences 9: 2676-2684.

Silva, L.R., Jacinto, T.A. & Coutinho, P. 2022. Bioactive compounds from cardoon as health promoters in metabolic disorders. Foods 11: 336.

Suares, N.C. & Ford, A.C. 2011. Prevalence and risk factors for: Chronic idiopathic constipation in the community: Systematic review and meta-analysis. American Journal of Gastroenterology 106(9): 1582-1591.

Tajini, F., Boualy, Y. & Ouerghi, A. 2020. Etude de la qualité nutritionnelle de fruit de Phœnix dactyliferaL.: mesure des paramètres biochimiques. Revue Nature et Technologie 12(2): 39-49.

Van Soest, P.J., Robertson, J.B. & Lewis, B.A. 1991. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74: 3583-3597.

V.I.D.A.L. 2019. La phytothérapie dans le traitement de la constipation. https://www.vidal.fr/maladies/estomac-intestins/constipation-adulte/phytotherapie-plantes.html

Wood, W., Jacinto, A., Grose, R., Woolner, S., Gale, J., Wilson, C. & Martin, P. 2002. Wound healing recapitulates morphogenesis in Drosophila embryos. Nature Cell Biology4: 907-912.

Yahfoufi, N., Alsadi, N., Jambi, M. & Matar, C. 2018. The immunomo dulatory and anti-inflammatory role of polyphenols. Nutrients10(11): 1618. 

Zhou, J.F., Lou, J.G., Zhou, S.L. & Wang, J.Y. 2005. Potential oxidative stress in children with chronic constipation. World J. Gastroenterol. 11: 368-371.

Zongo, E., Busuioc, A., Meda, R.N.T., Botezatu, A.V., Mihaila, M.D., Mocanu, A.M., Avramescu, S.M., Koama, B.K., Kam, S.E., Belem, H., Somda, F.L.S., Ouedraogo, C., Ouedraogo, G.A. & Dinica, R.M. 2023. Exploration of the antioxidant and  anti-inflammatory potential of Cassia sieberianaDC and Piliostigma thonningii(Schumach.) Milne-Redh, traditionally used in the treatment of hepatitis in the Hauts-Bassins region of Burkina Faso. Pharmaceuticals 16(1): 133.

*Corresponding author; email: tajinifatma24@gmail.com