Bioactive Compounds and In Vitro Antioxidant and Anticoccidial Activities of Opuntia ficus-indica Flower Extracts
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant Material
2.2. Chemical Reagents
2.3. Extraction
2.4. Determination of Phenolic Compounds
2.4.1. Determination of Total Phenolic Content (TPC)
2.4.2. Determination of Flavonoid Content
2.5. Antioxidant Activities
2.5.1. DPPH Radical Scavenging Activity
2.5.2. Hydrogen Peroxide Scavenging Activity
2.6. Phenolic Compound Profile
2.7. Evaluation of the Anticoccidial Activity
2.7.1. Eimeria Oocysts Isolation and Purification
2.7.2. Effects of OFI Flower Extract on the Decrease in Oocysts Number
2.8. Statistical Analyses
3. Results and Discussion
3.1. Bioactive Compounds
3.2. Antioxidant Activities
3.3. Anticoccidial Activity
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Martins, M.; Ribeiro, M.H.; Almeida, C.M. Physicochemical, Nutritional, and Medicinal Properties of Opuntia ficus-indica (L.) Mill. and Its Main Agro-Industrial Use: A Review. Plants 2023, 12, 1512. [Google Scholar] [PubMed]
- Dubeux, J.C.B., Jr.; dos Santos, M.V.F.; da Cunha, M.V.; dos Santos, D.C.; de Almeida Souza, R.T.; de Mello, A.C.L.; de Souza, T.C. Cactus (Opuntia and Nopalea) nutritive value: A review. Anim. Feed Sci. Technol. 2021, 275, 114890. [Google Scholar]
- Aragona, M.; Lauriano, E.; Pergolizzi, S.; Faggio, C. Opuntia ficus-indica (L.) Miller as a source of bioactivity compounds for health and nutrition. Nat. Prod. Res. 2018, 32, 2037–2049. [Google Scholar]
- Ammar, I.; Ennouri, M.; Bouaziz, M.; Ben Amira, A.; Attia, H. Phenolic profiles, phytchemicals and mineral content of decoction and infusion of Opuntia ficus-indica flowers. Plant Foods Hum. Nutr. 2015, 70, 388–394. [Google Scholar] [PubMed]
- Ventura-Aguilar, R.I.; Bosquez-Molina, E.; Bautista-Baños, S.; Rivera-Cabrera, F. Cactus stem (Opuntia ficus-indica Mill): Anatomy, physiology and chemical composition with emphasis on its biofunctional properties. J. Sci. Food Agric. 2017, 97, 5065–5073. [Google Scholar]
- Majeed, S.; Zafar, M.; Ahmad, M.; Ozdemir, F.A.; Kilic, O.; Hamza, M.; Sultana, S.; Yaseen, G.; Lubna; Raza, J. Ethnobotany, medicinal utilization and systematics of opuntia species from deserts of Pakistan. In Opuntia spp.: Chemistry, Bioactivity and Industrial Applications; Ramadan, T.E., Ayoub, T.E.M., Rohn, S., Eds.; Springer: New York, NY, USA, 2021; pp. 49–80. [Google Scholar]
- Chahdoura, H.; Adouni, K.; Khlifi, A.; Dridi, I.; Haouas, Z.; Neffati, F.; Flamini, G.; Mosbah, H.; Achour, L. Hepatoprotective effect of Opuntia microdasys (Lehm.) Pfeiff flowers against diabetes type II induced in rats. Biomed. Pharmacother. 2017, 94, 79–87. [Google Scholar]
- Alimi, H.; Hfaiedh, N.; Bouoni, Z.; Hfaiedh, M.; Sakly, M.; Zourgui, L.; Rhouma, K.B. Antioxidant and antiulcerogenic activities of Opuntia ficus indica f. inermis root extract in rats. Phytomedicine 2010, 17, 1120–1126. [Google Scholar]
- Touiti, N.; Bousta, D.; Boukhira, S.; Chebaibi, M.; Achour, S. Phytochemical Screening, Acute and Sub-Acute Toxicity of Aqueous Extract from a Mixture of Some Recipe of Herniaria glabra L., Opuntia ficus-indica, Zea mays L. and Zizyphus lotus L. Used Traditionally against Renal Lithiases. Pharmacogn. Res. 2020, 12, 60–64. [Google Scholar]
- Amrane-Abider, M.; Nerín, C.; Tamendjari, A.; Serralheiro, M.L.M. Phenolic composition, antioxidant and antiacetylcholinesterase activities of Opuntia ficus-indica peel and flower teas after in vitro gastrointestinal digestion. J. Sci. Food Agric. 2022, 102, 4401–4409. [Google Scholar]
- Benayad, Z.; Martinez-Villaluenga, C.; Frias, J.; Gomez-Cordoves, C.; Es-Safi, N.E. Phenolic composition, antioxidant and anti-inflammatory activities of extracts from Moroccan Opuntia ficus-indica flowers obtained by different extraction methods. Ind. Crops Prod. 2014, 62, 412–420. [Google Scholar]
- Ammar, I.; Ennouri, M.; Khemakhem, B.; Yangui, T.; Attia, H. Variation in chemical composition and biological activities of two species of Opuntia flowers at four stages of flowering. Ind. Crops Prod. 2012, 37, 34–40. [Google Scholar] [CrossRef]
- El Tanbouly, N.; El Sayed, A.M.; Ali, Z.Y.; Wahab, S.A.; El Gayed, S.H.; Ezzat, S.M.; El Senousy, A.S.; Choucry, M.A.; Abdel-Sattar, E. Antidepressant-like effect of selected Egyptian cultivars of flaxseed oil on a rodent model of postpartum depression. Evid.-Based Complement. Altern. Med. eCAM 2017, 2017, 6405789. [Google Scholar] [CrossRef] [Green Version]
- Nićiforović, N.; Mihailović, V.; Mašković, P.; Solujić, S.; Stojković, A.; Muratspahić, D.P. Antioxidant activity of selected plant species; potential new sources of natural antioxidants. Food Chem. Toxicol. 2010, 48, 3125–3130. [Google Scholar]
- El-Hawary, S.S.; Sobeh, M.; Badr, W.K.; Abdelfattah, M.A.; Ali, Z.Y.; El-Tantawy, M.E.; Rabeh, M.A.; Wink, M. HPLC-PDA-MS/MS profiling of secondary metabolites from Opuntia ficus-indica cladode, peel and fruit pulp extracts and their antioxidant, neuroprotective effect in rats with aluminum chloride induced neurotoxicity. Saudi J. Biol. Sci. 2020, 27, 2829–2838. [Google Scholar]
- Mathew, J.; Jacob, A.; Shalmiya, S. Phytochemical Screening, Antioxidant, Antibacterial Activities And GC-MS Analysis of Methanolic Extract of Opuntia ficus-indica (L.) Mill. Fruit. J. Pharm. Negat. Results 2022, 13, 2607–2617. [Google Scholar]
- Brahmi, F.; Blando, F.; Sellami, R.; Mehdi, S.; De Bellis, L.; Negro, C.; Haddadi-Guemghar, H.; Madani, K.; Makhlouf-Boulekbache, L. Optimization of the conditions for ultrasound-assisted extraction of phenolic compounds from Opuntia ficus-indica [L.] Mill. flowers and comparison with conventional procedures. Ind. Crops Prod. 2022, 184, 114977. [Google Scholar]
- Chapman, H. Milestones in avian coccidiosis research: A review. Poult. Sci. 2014, 93, 501–511. [Google Scholar]
- Saeed, Z.; Alkheraije, K.A. Botanicals: A promising approach for controlling cecal coccidiosis in poultry. Front. Vet. Sci. 2023, 10, 1157633. [Google Scholar]
- Hussain, K.; Abbas, R.; Abbas, A.; Rehman, M.; Raza, M.; Rehman, T.; Hussain, R.; Mahmood, M.; Imran, M.; Zaman, M. Anticoccidial and biochemical effects of Artemisia brevifolia extract in broiler chickens. Braz. J. Poult. Sci. 2021, 23. [Google Scholar]
- Zhang, K.; Li, X.; Na, C.; Abbas, A.; Abbas, R.Z.; Zaman, M.A. Anticoccidial effects of Camellia sinensis (green tea) extract and its effect on Blood and Serum chemistry of broiler chickens. Pak. Vet. J. 2020, 40, 77–80. [Google Scholar]
- Debbou-Iouknane, N.; Nerín, C.; Amrane, M.; Ghemghar, M.; Madani, K.; Ayad, A. In vitro anticoccidial activity of olive pulp (Olea europaea L. var. chemlal) extract against Eimeria oocysts in broiler chickens. Acta Parasitol. 2019, 64, 887–897. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Debbou-Iouknane, N.; Nerín, C.; Amrane-Abider, M.; Ayad, A. In vitro anticoccidial effects of Olive Leaf (Olea europaea L. var. Chemlal) extract against broiler chickens Eimeria oocysts. Vet. Zootech. 2021, 79, 1–8. [Google Scholar]
- Amrane-Abider, M.; Nerin, C.; Cannelas, E.; Zeroual, B.; Hadjal, S.; Louaileche, H. Prickly pear (Opuntia ficus-indica) seeds as a source of phenolic compounds: Microwave-assisted extraction optimization and effect on food lipid oxidations. Ann. Univ. Dunarea De Jos Galati. Fascicle VI-Food Technol. 2018, 42, 23–35. [Google Scholar]
- Velioglu, Y.; Mazza, G.; Gao, L.; Oomah, B. Antioxidant activity and total phenolics in selected fruits, vegetables, and grain products. J. Agric. Food Chem. 1998, 46, 4113–4117. [Google Scholar] [CrossRef]
- Bahorun, T.; Luximon-Ramma, A.; Crozier, A.; Aruoma, O.I. Total phenol, flavonoid, proanthocyanidin and vitamin C levels and antioxidant activities of Mauritian vegetables. J. Sci. Food Agric. 2004, 84, 1553–1561. [Google Scholar] [CrossRef]
- Molyneux, P. The use of the stable free radical diphenylpicrylhydrazyl (DPPH) for estimating antioxidant activity. Songklanakarin J. Sci. Technol. 2004, 26, 211–219. [Google Scholar]
- Ruch, R.J.; Cheng, S.-j.; Klaunig, J.E. Prevention of cytotoxicity and inhibition of intercellular communication by antioxidant catechins isolated from Chinese green tea. Carcinogenesis 1989, 10, 1003–1008. [Google Scholar] [CrossRef]
- Carvalho, F.S.; Wenceslau, A.A.; Teixeira, M.; Carneiro, J.A.M.; Melo, A.D.B.; Albuquerque, G.R. Diagnosis of Eimeria species using traditional and molecular methods in field studies. Vet. Parasitol. 2011, 176, 95–100. [Google Scholar] [CrossRef] [Green Version]
- Ballesteros, L.F.; Ramirez, M.J.; Orrego, C.E.; Teixeira, J.A.; Mussatto, S.I. Optimization of autohydrolysis conditions to extract antioxidant phenolic compounds from spent coffee grounds. J. Food Eng. 2017, 199, 1–8. [Google Scholar] [CrossRef] [Green Version]
- Amrane-Abider, M.; Nerin, C.; Canellas, E.; Benkerrou, F.; Louaileche, H. Modeling and optimization of phenolic compounds extraction from prickly pear (Opuntia ficus-indica) seeds via ultrasound-assisted technique. Ann. Univ. Dunarea Jos Galati. Fascicle VI-Food Technol. 2018, 42, 109–121. [Google Scholar]
- Alexandre, E.M.; Araújo, P.; Duarte, M.F.; de Freitas, V.; Pintado, M.; Saraiva, J.A. High-pressure assisted extraction of bioactive compounds from industrial fermented fig by-product. J. Food Sci. Technol. 2017, 54, 2519–2531. [Google Scholar] [CrossRef]
- Sedraoui, S.; Badr, A.; Barba, M.G.M.; Doyen, A.; Tabka, Z.; Desjardins, Y. Optimization of the ultrahigh-pressure–assisted extraction of phenolic compounds and antioxidant activity from palm dates (Phoenix dactylifera L.). Food Anal. Methods 2020, 13, 1556–1569. [Google Scholar] [CrossRef]
- Benkerrou, F.; Bachir bey, M.; Amrane, M.; Louaileche, H. Ultrasonic-assisted extraction of total phenolic contents from Phoenix dactylifera and evaluation of antioxidant activity: Statistical optimization of extraction process parameters. J. Food Meas. Charact. 2018, 12, 1910–1916. [Google Scholar] [CrossRef]
- Bansod, S.P.; Parikh, J.K.; Sarangi, P.K. Pineapple peel waste valorization for extraction of bio-active compounds and protein: Microwave assisted method and Box Behnken design optimization. Environ. Res. 2023, 221, 115237. [Google Scholar] [CrossRef]
- Tsiaka, T.; Lantzouraki, D.Z.; Polychronaki, G.; Sotiroudis, G.; Kritsi, E.; Sinanoglou, V.J.; Kalogianni, D.P.; Zoumpoulakis, P. Optimization of Ultrasound-and Microwave-Assisted Extraction for the Determination of Phenolic Compounds in Peach Byproducts Using Experimental Design and Liquid Chromatography–Tandem Mass Spectrometry. Molecules 2023, 28, 518. [Google Scholar] [CrossRef]
- Alara, O.R.; Abdurahman, N.H.; Ukaegbu, C.I. Extraction of phenolic compounds: A review. Curr. Res. Food Sci. 2021, 4, 200–214. [Google Scholar] [CrossRef]
- Wen, C.; Zhang, J.; Zhang, H.; Dzah, C.S.; Zandile, M.; Duan, Y.; Ma, H.; Luo, X. Advances in ultrasound assisted extraction of bioactive compounds from cash crops—A review. Ultrason. Sonochem. 2018, 48, 538–549. [Google Scholar] [CrossRef]
- Berrabah, H.; Taïbi, K.; Ait Abderrahim, L.; Boussaid, M. Phytochemical composition and antioxidant properties of prickly pear (Opuntia ficus-indica L.) flowers from the Algerian germplasm. J. Food Meas. Charact. 2019, 13, 1166–1174. [Google Scholar] [CrossRef]
- De Leo, M.; De Abreu, M.B.; Pawlowska, A.; Cioni, P.; Braca, A. Profiling the chemical content of Opuntia ficus-indica flowers by HPLC–PDA-ESI-MS and GC/EIMS analyses. Phytochem. Lett. 2010, 3, 48–52. [Google Scholar] [CrossRef]
- García-Cayuela, T.; Gómez-Maqueo, A.; Guajardo-Flores, D.; Welti-Chanes, J.; Cano, M.P. Characterization and quantification of individual betalain and phenolic compounds in Mexican and Spanish prickly pear (Opuntia ficus-indica L. Mill) tissues: A comparative study. J. Food Compos. Anal. 2019, 76, 1–13. [Google Scholar] [CrossRef]
- Ammar, I.; Salem, M.B.; Harrabi, B.; Mzid, M.; Bardaa, S.; Sahnoun, Z.; Attia, H.; Ennouri, M. Anti-inflammatory activity and phenolic composition of prickly pear (Opuntia ficus-indica) flowers. Ind. Crops Prod. 2018, 112, 313–319. [Google Scholar] [CrossRef]
- de Wit, M.; Hugo, A.; Shongwe, N. South African cactus pear seed oil: A comprehensive study on 42 spineless Burbank Opuntia ficus-indica and Opuntia robusta cultivars. Eur. J. Lipid Sci. Technol. 2018, 120, 1700343. [Google Scholar]
- Yeh, H.-y.; Chuang, C.-h.; Chen, H.-c.; Wan, C.-j.; Chen, T.-l.; Lin, L.-y. Bioactive components analysis of two various gingers (Zingiber officinale Roscoe) and antioxidant effect of ginger extracts. LWT-Food Sci. Technol. 2014, 55, 329–334. [Google Scholar] [CrossRef]
- Choe, E.; Min, D.B. Mechanisms of antioxidants in the oxidation of foods. Compr. Rev. Food Sci. Food Saf. 2009, 8, 345–358. [Google Scholar] [CrossRef]
- Alfadda, A.A.; Sallam, R.M. Reactive oxygen species in health and disease. J. Biomed. Biotechnol. 2012, 2012, 936486. [Google Scholar] [CrossRef] [Green Version]
- Naveena, B.; Sen, A.; Vaithiyanathan, S.; Babji, Y.; Kondaiah, N. Comparative efficacy of pomegranate juice, pomegranate rind powder extract and BHT as antioxidants in cooked chicken patties. Meat Sci. 2008, 80, 1304–1308. [Google Scholar] [CrossRef]
- de Gonzalez, M.N.; Hafley, B.; Boleman, R.; Miller, R.; Rhee, K.; Keeton, J. Antioxidant properties of plum concentrates and powder in precooked roast beef to reduce lipid oxidation. Meat Sci. 2008, 80, 997–1004. [Google Scholar] [CrossRef]
- Chougui, N.; Louaileche, H.; Mohedeb, S.; Mouloudj, Y.; Hammoui, Y.; Tamendjari, A. Physico-chemical characterisation and antioxidant activity of some Opuntia ficus-indica varieties grown in North Algeria. Afr. J. Biotechnol. 2013, 12, 299–307. [Google Scholar] [CrossRef] [Green Version]
- Chaalal, M.; Louaileche, H.; Touati, N.; Bey, M.B. Phytochemicals, in vitro antioxidant capacity and antiradical potential of whole and ground seeds of three prickly pear varieties: A comparative study. Ind. Crops Prod. 2013, 49, 386–391. [Google Scholar]
- Brewer, M. Natural antioxidants: Sources, compounds, mechanisms of action, and potential applications. Compr. Rev. Food Sci. Food Saf. 2011, 10, 221–247. [Google Scholar] [CrossRef]
- Nahed, A.; Abd El-Hack, M.E.; Albaqami, N.M.; Khafaga, A.F.; Taha, A.E.; Swelum, A.A.; El-Saadony, M.T.; Salem, H.M.; El-Tahan, A.M.; AbuQamar, S.F. Phytochemical control of poultry coccidiosis: A review. Poult. Sci. 2022, 101, 101542. [Google Scholar]
- Peek, H.; Landman, W. Coccidiosis in poultry: Anticoccidial products, vaccines and other prevention strategies. Vet. Q. 2011, 31, 143–161. [Google Scholar] [CrossRef]
- Daiba, A.R.; Kagira, J.M.; Ngotho, M.; Kimotho, J.; Maina, N. In vitro anticoccidial activity of nanoencapsulated bromelain against Eimeria spp. oocysts isolated from goats in Kenya. Vet. World 2022, 15, 397. [Google Scholar] [CrossRef]
- Bǎieş, M.-H.; Györke, A.; Cotuţiu, V.-D.; Boros, Z.; Cozma-Petruț, A.; Filip, L.; Vlase, L.; Vlase, A.-M.; Crişan, G.; Spînu, M. The In Vitro Anticoccidial Activity of Some Herbal Extracts against Eimeria spp. Oocysts Isolated from Piglets. Pathogens 2023, 12, 258. [Google Scholar] [CrossRef]
- Khoshnejad, A.; Yakhchali, M.; Malekifard, F. Study oneffects of plant extracts of Camellia sinensis and Thymus vulgaris on sporulation of Eimeria oocysts of broiler chicken under laboratory conditions. Iran. J. Anim. Sci. 2023, 54, 93–104. [Google Scholar]
- Remmal, A.; Achahbar, S.; Bouddine, L.; Chami, N.; Chami, F. In vitro destruction of Eimeria oocysts by essential oils. Vet. Parasitol. 2011, 182, 121–126. [Google Scholar] [CrossRef]
- Abbas, R.Z.; Abbas, A.; Raza, M.A.; Khan, M.K.; Saleemi, M.K.; Saeed, Z. In vitro anticoccidial activity of Trachyspermum ammi (Ajwain) extract on oocysts of Eimeria species of Chicken. Adv. Life Sci. 2019, 7, 44–47. [Google Scholar]
- Sharma, U.N.S.; Fernando, D.D.; Wijesundara, K.K.; Manawadu, A.; Pathirana, I.; Rajapakse, R.J. Anticoccidial effects of Phyllanthus emblica (Indian gooseberry) extracts: Potential for controlling avian coccidiosis. Vet. Parasitol. Reg. Stud. Rep. 2021, 25, 100592. [Google Scholar]
- Udo, E.; Abba, A. Comparative Study of in-vitro anticoccidial efficacy of Allium sativum and Carica papaya. J. Zool. Res. 2018, 2, 10–14. [Google Scholar]
- Quiroz-Castañeda, R.E. Avian coccidiosis, new strategies of treatment. In Farm Animals Diseases, Recent Omic Trends and New Strategies of Treatment; IntechOpen: London, UK, 2018; p. 119. [Google Scholar]
- Yao, L.H.; Jiang, Y.-M.; Shi, J.; Tomas-Barberan, F.; Datta, N.; Singanusong, R.; Chen, S. Flavonoids in food and their health benefits. Plant Foods Hum. Nutr. 2004, 59, 113–122. [Google Scholar] [CrossRef]
- Dai, Y.; Liu, Y.; Rakotondraibe, L.H. Novel bioactive natural products isolated from madagascar plants and marine organisms (2009–2017). Chem. Pharm. Bull. 2018, 66, 469–482. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Sun, W.; Shahrajabian, M.H. Therapeutic potential of phenolic compounds in medicinal plants—Natural health products for human health. Molecules 2023, 28, 1845. [Google Scholar] [CrossRef] [PubMed]
- Zaman, M.A.; Iqbal, Z.; Abbas, R.Z.; Khan, M.N. Anticoccidial activity of herbal complex in broiler chickens challenged with Eimeria tenella. Parasitology 2012, 139, 237–243. [Google Scholar] [CrossRef] [PubMed]
- Kayser, O.; Kiderlen, A.F.; Croft, S.L. Natural products as potential antiparasitic drugs. Stud. Nat. Prod. Chem. 2002, 26, 779–848. [Google Scholar]
- Abdel-Tawab, H.; Abdel-Haleem, H.M.; Abdel-Baki, A.-A.S.; Al-Quraishy, S.; El-Mallah, A.M. Anticoccidial and antioxidant activities of Moringa oleifera leaf extract on murine intestinal eimeriosis. Acta Parasitol. 2020, 65, 823–830. [Google Scholar] [CrossRef]
- Kerboeuf, D.; Riou, M.; Guégnard, F. Flavonoids and related compounds in parasitic disease control. Mini Rev. Med. Chem. 2008, 8, 116–128. [Google Scholar] [CrossRef]
- Jin, H.; Xu, Z.; Cui, K.; Zhang, T.; Lu, W.; Huang, J. Dietary flavonoids fisetin and myricetin: Dual inhibitors of Plasmodium falciparum falcipain-2 and plasmepsin II. Fitoterapia 2014, 94, 55–61. [Google Scholar] [CrossRef]
- Cornelio, V.E.; Maluf, F.V.; Fernandes, J.B.; da Silva, M.F.G.; Oliva, G.; Guido, R.V.; Vieira, P.C. Isolation of tiliroside from Spiranthera odoratissima as inhibitor of Trypanosoma cruzi glyceraldehyde-3-phosphate dehydrogenase by using bioactivity-guided fractionation. J. Braz. Chem. Soc. 2017, 28, 512–519. [Google Scholar] [CrossRef]
- Scotti, L.; Ishiki, H.; Mendonca, F.; Da Silva, M.; Scotti, M. In-silico analyses of natural products on leishmania enzyme targets. Mini Rev. Med. Chem. 2015, 15, 253–269. [Google Scholar] [CrossRef]
- Tiwari, K.; Kumar, R.; Dubey, V.K. Biochemical characterization of dihydroorotase of Leishmania donovani: Understanding pyrimidine metabolism through its inhibition. Biochimie 2016, 131, 45–53. [Google Scholar] [CrossRef]
Factor | Level | ||
---|---|---|---|
−1 | 0 | +1 | |
X1 | 40 | 60 | 80 |
X2 | 30 | 40 | 50 |
X3 | 30 | 90 | 150 |
X4 | 400 | 700 | 1000 |
Run | TPC (mg GAE/g DW) | Flavonoid (mg QE/g DW) | DPPH (mg GAE/g DW) | H2O2 (mg GAE/g DW) | |||||
---|---|---|---|---|---|---|---|---|---|
Pattern X1 X2 X3 X4 | Observed | Predicted | Observed | Predicted | Observed | Predicted | Observed | Predicted | |
1 | + 0 + 0 | 23.854 | 22.172 | 20.212 | 20.292 | 32.606 | 33.429 | 7.225 | 7.342 |
2 | − 0 + 0 | 11.592 | 10.086 | 08.598 | 08.262 | 34.574 | 34.559 | 7.637 | 7.754 |
3 | 00 + + | 13.039 | 15.362 | 11.075 | 09.371 | 37.321 | 37.524 | 7.327 | 6.919 |
4 | + 00 − | 23.322 | 24.292 | 17.907 | 17.136 | 33.254 | 32.809 | 6.636 | 6.495 |
5 | + + 00 | 25.780 | 25.344 | 25.716 | 25.896 | 32.056 | 31.997 | 7.924 | 8.115 |
6 | + 0 − 0 | 24.165 | 26.318 | 20.013 | 19.342 | 33.693 | 33.774 | 7.543 | 7.193 |
7 | − − 00 | 11.488 | 10.704 | 10.545 | 11.920 | 31.398 | 31.128 | 7.184 | 7.209 |
8 | 0 − + 0 | 14.938 | 15.450 | 10.518 | 10.640 | 34.782 | 34.600 | 6.833 | 6.991 |
9 | − + 00 | 25.787 | 26.722 | 19.194 | 20.823 | 31.874 | 32.551 | 6.183 | 6.375 |
10 | − 00 + | 16.054 | 14.658 | 09.935 | 10.160 | 32.610 | 33.318 | 6.402 | 6.560 |
11 | + − 00 | 25.834 | 24.679 | 22.079 | 22.004 | 31.452 | 30.445 | 5.870 | 5.895 |
12 | 0+ − 0 | 34.663 | 33.725 | 21.207 | 20.539 | 35.475 | 35.921 | 7.053 | 6.911 |
13 | 0−0− | 24.057 | 24.523 | 15.136 | 14.442 | 34.352 | 35.389 | 6.630 | 6.280 |
14 | 0000 | 21.092 | 22.979 | 16.447 | 17.316 | 36.282 | 37.780 | 6.993 | 7.126 |
15 | 0 − − 0 | 22.289 | 22.399 | 17.336 | 16.288 | 34.013 | 34.879 | 6.366 | 6.558 |
16 | 0 + 0 − | 28.416 | 28.211 | 20.858 | 19.531 | 37.904 | 38.414 | 7.453 | 7.270 |
17 | − 0 0 − | 24.020 | 24.443 | 17.371 | 15.567 | 38.191 | 37.848 | 7.277 | 7.135 |
18 | 0 0 − + | 30.280 | 29.170 | 17.326 | 17.542 | 40.922 | 40.819 | 7.688 | 7.713 |
19 | 0 + 0 + | 29.349 | 29.530 | 21.755 | 21.442 | 37.737 | 36.766 | 7.135 | 7.252 |
20 | 0000 | 25.964 | 22.979 | 18.664 | 17.316 | 38.529 | 37.780 | 7.293 | 7.126 |
21 | 0 0− − | 31.172 | 28.629 | 09.011 | 12.270 | 37.999 | 37.467 | 5.242 | 5.867 |
22 | + 00 + | 28.256 | 27.407 | 22.492 | 23.749 | 36.512 | 37.119 | 7.468 | 7.626 |
23 | 0 ++ 0 | 21.344 | 20.808 | 18.683 | 19.184 | 37.135 | 36.533 | 8.199 | 8.024 |
24 | 0000 | 21.881 | 22.979 | 16.838 | 17.316 | 38.529 | 37.780 | 7.093 | 7.126 |
25 | 00 + − | 21.683 | 22.572 | 12.099 | 13.437 | 41.322 | 41.096 | 8.017 | 8.208 |
26 | 0 − 0 + | 15.684 | 16.535 | 13.416 | 13.736 | 37.261 | 36.817 | 6.905 | 6.855 |
27 | − 0 − 0 | 23.478 | 25.806 | 17.303 | 16.215 | 34.639 | 33.881 | 6.706 | 6.356 |
Model | TPC | Flavonoid | DPPH | H2O2 |
---|---|---|---|---|
DF | 14 | 14 | 14 | 14 |
SS | 871.601 | 525.810 | 193.409 | 10.070 |
F value | 14.340 | 13.167 | 14.336 | 6.333 |
p value | <0.0001 * | <0.0001 * | <0.0001 * | <0.001 * |
Lack of fit | ||||
DF | 10 | 10 | 10 | 10 |
SS | 38.422 | 41.427 | 8.197 | 1.316 |
F value | 0.5619 | 2.244 | 0.487 | 5.641 |
p value | >0.782 | >0.347 | >0.821 | 0.160 |
Pure error | ||||
DF | 2 | 2 | 2 | 2 |
SS | 13.676 | 2.800 | 3.366 | 0.046 |
R2 | 0.94 | 0.94 | 0.94 | 0.880 |
R2Adj | 0.88 | 0.87 | 0.88 | 0.740 |
Compounds | [M-H] | Retention Time (min) | Concentration (±SD, µg/g) | Molecular Formula | Fragment Ions (m/z) | |
---|---|---|---|---|---|---|
1 | Quinic acid | 191 | 0.80 | 109.30 ± 0.39 | C7H12O6 | 173 (87), 129 (69) 134 (58), 174 (28) |
2 | Coumaricacid | 163 | 2.24 | 58.06 ± 0.17 | C9H8O3 | 119 (100), 163 (22), 91 (2) |
3 | Piscidic acid | 255 | 2.78 | 62.65 ± 0.10 | C11H11O7 | 193 (100), 165 (48), 135 (30), 119 (18), 107 (3) |
4 | Eucomic acid | 239 | 3.07 | 289.25 ± 0.21 | C11H12O6 | 131 (75), 103 (5), 72 (1) |
5 | Isorhamnetin | 315 | 3.91 | 80.68 ± 0.10 | C16H12O7 | 315 (100), 301 (7), 297 (6), 285 (2) |
6 | Kaempferol-3-O-rutinoside | 593 | 4.25 | 139.03 ± 0.05 | C27H30O15 | 287 (100), 146 (7) |
7 | Kaempferol 3-O-arabinoside | 417 | 5.45 | 89.98 ± 0.17 | C20H18O10 | 285 (100), 227 (20), 417 (60) |
8 | Quercetin | 301 | 6.79 | 258.16 ± 0.01 | C15H10O7 | 273 (13), 179 (62), 151 (95), 155 (6), 121 (26) |
9 | Isoquercetin | 463 | 6.99 | 226.05 ± 0.05 | C21H20O12 | 301 (100), 300 (42), 179 (77) |
10 | Isorhamnetin 3-O-rutinoside | 623 | 7.35 | 295.14 ± 0.01 | C28H32O16 | 315 (42), 314 (100) |
11 | Isorhamnetin 3-O-glucoside | 477 | 7.63 | 213.45 ± 0.11 | C22H22O12 | 315 (100), 300 (80) |
12 | Quercetin-3-O-rutinoside | 609 | 8.11 | 265.41 ± 0.04 | C27H30O16 | 303 (100), 300 (55), 151 (12) |
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Amrane-Abider, M.; Imre, M.; Herman, V.; Debbou-Iouknane, N.; Zemouri-Alioui, S.; Khaled, S.; Bouiche, C.; Nerín, C.; Acaroz, U.; Ayad, A. Bioactive Compounds and In Vitro Antioxidant and Anticoccidial Activities of Opuntia ficus-indica Flower Extracts. Biomedicines 2023, 11, 2173. https://doi.org/10.3390/biomedicines11082173
Amrane-Abider M, Imre M, Herman V, Debbou-Iouknane N, Zemouri-Alioui S, Khaled S, Bouiche C, Nerín C, Acaroz U, Ayad A. Bioactive Compounds and In Vitro Antioxidant and Anticoccidial Activities of Opuntia ficus-indica Flower Extracts. Biomedicines. 2023; 11(8):2173. https://doi.org/10.3390/biomedicines11082173
Chicago/Turabian StyleAmrane-Abider, Meriem, Mirela Imre, Viorel Herman, Nedjima Debbou-Iouknane, Salima Zemouri-Alioui, Souad Khaled, Cilia Bouiche, Cristina Nerín, Ulaș Acaroz, and Abdelhanine Ayad. 2023. "Bioactive Compounds and In Vitro Antioxidant and Anticoccidial Activities of Opuntia ficus-indica Flower Extracts" Biomedicines 11, no. 8: 2173. https://doi.org/10.3390/biomedicines11082173
APA StyleAmrane-Abider, M., Imre, M., Herman, V., Debbou-Iouknane, N., Zemouri-Alioui, S., Khaled, S., Bouiche, C., Nerín, C., Acaroz, U., & Ayad, A. (2023). Bioactive Compounds and In Vitro Antioxidant and Anticoccidial Activities of Opuntia ficus-indica Flower Extracts. Biomedicines, 11(8), 2173. https://doi.org/10.3390/biomedicines11082173