Abstract
Ziziphus spina-christi and Z. lotus are very important medicinal plants of the family Rhamnaceae. The need for accurate identification and authentication of powdered crude drug samples in the face of growing world demand for herbal products cannot be over-emphasized. The aim of this study was to determine the content of essential nutrients and phytochemical compounds (total phenolics, flavonoids, tannins and anthocyanins) in the fruits, pulps, seeds and almonds of the two species of Ziziphus (Z. spina-christi and Z. lotus). Six-phase sequential extraction using six different solvents was done to totally and efficiently extract the phytochemical components from the different parts of the plants and then the filtrates were pooled together to produce the powders which were thereafter analyzed. The proximate composition showed that Z. spina-christi fruit and pulp had higher moisture content, while its almonds had higher lipid and crude protein contents (13.78 and 30.15% respectively), and seed had higher ash content (4.91%) as compared to those of Z. lotus. The highest carbohydrate content was observed in the fruit and pulp of Z. lotus (83%). The greatest levels of polyphenols and tannins were found in aqueous extract of the seeds and almonds of Z. spina-christi. Flavonoid and anthocyanins contents were found to be highest in methanolic extract of the seeds and almonds of Z. lotus. Results obtained in this study may be used for identification and authentication purposes, and in the development of a monograph for these medicinal plants.
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References
A. Hosane, H. Abul, K. Mahbuba, Taxonomic study of the genus Ziziphus mill. (Rhamnaceae). Bangladesh J. Plant Taxon. 15(1), 47–61 (2008)
N. Rsaissi, M. Bouhache, La lutte chimique contre le jujubier. Programme National de transfert de Technologie en Agriculture (PNTTA), DERD (Ed). N 0 94. Rabat (2002)
M. Adeli, V. Samavati, Studies on the steady shear flow behavior and chemical properties of water-soluble polysaccharide from Ziziphus lotus fruit. Int. J. Biol. Macromol. 72, 580–587 (2015)
J.E. Richardson, L.W. Chatrou, J.B. Mols, R.H.J. Erkens, M.D. Pirie, Historical biogeography of two cosmopolitan families of flowering plants: Annonaceae and Rhamnaceae. Philos. Trans. R. Soc. B 359, 1495–1508 (2004)
M. Maraghni, M. Gorai, M. Neffati, Seed germination at different temperatures and water stress levels, and seedling emergence from different depths of Zizyphus lotus. S. Afr. J. Bot. 7, 453–459 (2010)
C. Benammar, A. Hichami, A. Yessoufou, A.M. Simonin, M. Belarbi, H. Allali, N.A. Khan, Zizyphus lotus L. (Desf.) modulates antioxidant activity and human T-cell proliferation. BMC Complement. Altern. Med. 10(54), 1–9 (2010)
M. Amara, K.A. Benabdeli, Geobotanical and phenological study of Zizyphus lotus in the Naama region (South-Western of Algeria). J. Appl. Environ. Biol. Sci. 7(11), 1–8 (2017)
R. Claudine, Le nom de l’arbre: le gnenadier, le caroubier, le jujubier, le pistachier et l’arbousier. Actes sud le Majan, 1er Edition. France. pp. 45–62 (2007)
W. Borgi, A. Bouraoui, N. Chouchane, Antiulcerogenic activity of Zizyphus lotus (L.) extracts. J. Ethnopharmacol. 12, 228–231 (2007)
M. Abdeddaim, O. Lombarkia, A. Bacha, D. Fahloul, D.I. Abdeddaim, R. Farhat, M. Saadoudi, Y. Noui, A. Lekbir, Biochemical characterization and nutritional properties of Zizyphus lotus L. fruits in Aures region, Northeastern of Algeria. Ann. Food Sci. Technol. 15, 75–81 (2014)
B. Adzu, S. Amos, M.B. Amizan, K. Gamaniel, Evaluation of the antidiarrhoeal effects of Zizyphus spina-christi stem bark inrats. ActaTropica 87(2), 245–250 (2003)
J. Lunn, H.E. Theobald, The health effects of dietary unsaturated fatty acids. Nutr. Bull. 31, 178–224 (2006)
J. Zhao, S.P. Li, F.Q. Yang, P. Li, Y.T. Wang, Simultaneous determination of saponins and fatty acids in Ziziphus jujube (Suanzaoren) by high performance liquid chromatography-evaporative light scattering detection and pressurized liquid extraction. J. Choromatogr. A. 1108, 188–194 (2006)
W. Borgi, M.C. Recio, J.L. Rios, N. Chouchane, Anti-inflammatory and analgesic activities of flavonoid and saponin fractions from Zizyphus lotus (L.) Lam. S. Afr. J. Bot. 14, 320–324 (2008)
M. Lahlou, M. El Mahi, J. Hamamouchi, Evaluation des activités antifongiques et molluscide de Zizyphus lotus (L.) Desf.du Maroc. J Ann. Pharm. Fr. 60, 410–414 (2002)
B. Mahboba, O. Rabia, A.N. Abil, Y. Asma, Evaluation of antibacterial and antioxidant activities of Artemisia campestris (Astraceae) and Ziziphus lotus (Rhamnacea). Arab. J. Chem. 3, 79–84 (2010)
A. Zargari, Medicinal Plants, vol. 2 (Tehran University Press, Tehran, 1988) pp. 42
J. Asgarpanah, J. Haghighat, Phytochemistry and pharmacologic properties of Ziziphus spina christi (L.) Willd. Afr. J. Pharm. Pharmacol. 6(31), 2332–2339 (2012)
B. Adzu, S. Amos, C. Wambebe, K. Gamaniel, Antinociceptive activity of Zizyphus spina-christi root bark extract. Fitoterapia 72(4), 344–350 (2001)
K. Kadioglu, J. Onat, B.T. Stefan, N. Stefan, S. Janine, K. Mohamed, M. Hassan, T. Irmgard, P. Eckhardt, E. Tanja, Evaluating ancient Egyptian prescriptions today: anti-inflammatory activity of Ziziphus spina-christi. Phytomedicine (2016). https://doi.org/10.1016/j.phymed.2016.01.004
M. Dkhil, S. Al-Quraishy, M. Abdel, Ziziphus spina-christi leaf extract pretreatment inhibits liver and spleen injury in a mouse model of sepsis via antioxidant and anti-inflammatory effects. Inflammopharmacology (2018). https://doi.org/10.1007/s10787-017-0439-8
M.E. Abalaka, S.Y. Daniyan, A. Mann, Evaluation of the antimicrobial activities of two Ziziphus species (Ziziphus mauritiana L. and Ziziphus spina-christi L.) on some microbial pathogens. Afr. J. Pharm. Pharmacol. 4(4), 135–139 (2010)
M. EL-Hefny, S. Mamoun, M. El-Kareem, M. Ali, Chemical composition, antioxidant capacity and antibacterial activity against some potato bacterial pathogens of fruit extracts from Phytolacca dioica and Ziziphus spina-christi grown in Egypt. Sci. Hortic. (2018). https://doi.org/10.1016/j.scienta.2018.01.046
H.H. El-Kamali, S.A. Mahjoub, Antibacterial activity of Francoeuria crispa, Pulicaria undulata, Ziziphus spina-christi and Cucurbita pepo against seven standard pathogenic bacteria. Ethnobot. Leafl. 13, 722–733 (2009)
N. Essam, R. Saravanan, L. Syed, M. Sherif, R. Jamal, Phytochemical, antimicrobial and cytotoxic evaluation of Ziziphus spina christi (L.) stem bark. Biomed. Res. 28(15), 6646–6653 (2017)
G.M. Tom, H.B. Yesufu, F.I. Abdulrahman, Antimicrobial screening and effect of the pulp extracts of Zizyphus spina-christi (Linnaeus Desf) on some biochemical parameters in rats. J. Pharm. Bioresour. 6(2), 58–64 (2009)
B. Adzu, S. Amos, C. Wambeb, K. Gamaniel, Antinociceptive activity of Ziziphus spina christi root bark extract. Fitoterapia 72, 334–350 (2001)
A.A. Shahat, L. Pieters, S. Apers, N.M. Nazeif, N.S. Abdel-Azim, D.W. Bergh, Chemical and biological investigations on Zizyphus spina-christi L. Phytother. Res. 15(7), 593–597 (2001)
A.O. Ghafoor, H.K. Qadir, N.A. Fakhri, Analysis of phenolic compounds in extracts of Ziziphus spina-christi using RPHPLC method. J. Chem. Pharm. Res. 4(6), 3158–3163 (2012)
M.E. Abalaka, A. Mann, S.O. Adeyemo, Studies on in-vitro antioxidant and free radical scavenging potential and phytochemical screening of leaves of Ziziphus mauritiana L. and Ziziphus spina-christi L. compared with ascorbic acid. J. Med. Genet. Genom. 3(2), 28–34 (2011)
A.O. Abdel-Zaher, S.Y. Salim, M.H. Assaf, R.H. Abdel-Hady, Antidiabetic activity and toxicity of Zizyphus spina-christi leaves. J. Ethnopharmacol. 101(1–3), 129–138 (2005)
B. Adzu, S. Amos, C. Wambebe, K. Gamaniel, Antinociceptive activity of Ziziphus spina christi root bark extract. Fitoterapia 72, 334–350 (2001)
B. Adzu, S. Amos, M. Amizan, K. Gamaniel, Evaluation of the antidiarrhoeal effects of Ziziphus spina christi stem bark in rats. Acta Trop. 87(2), 245–250 (2003)
B. Adzu, A.K. Haruna, M. Ilyas, U.U. Pateh, F.D. Tarfa, B.A. Chindo, K.S. Gamaniel, Structural characterization of ZS–2A: an antiplasmodial compound isolated from Zizyphus spina-christi root bark. J. Pharm. Nutr. Sci. 1, 48–53 (2011)
H.M. Hussein, E.M. El-Sayed, A.A. Said, Antihyperglycemic, antihyperlipidemic and antioxidant effects of Zizyphus spina christi and Zizyphus jujube in alloxan diabetic rats. Int. J. Pharmacol. 2(5), 563–570 (2006)
A.M. Waggas, R.H. Al-Hasani, Neurophysiological study on possible protective and therapeutic effects of Sidr (Zizyphus spina-christi L.) leaf extract in male albino rats treated with pentylenetetrazol. Saudi J. Biol. Sci. 5(3), 1–6 (2010)
H.E. Yossef, A.A. Khedr, M.Z. Mahran, Hepatoprotective activity and antioxidant effects of El Nabka (Zizyphus spina-christi) fruits on rat’s hepatotoxicity hepatotoxicity induced by carbon tetrachloride. Nat. Sci. 9(2), 1–7 (2011)
M. Tripathi, M.B. Pandey, R.N. Jha, V.B. Pandey, P.N. Tripathi, J.P. Singh, Cyclopeptide alkaloids from Zizyphus jujube. Fitoterapia 72(5), 507–510 (2001)
F. Alhakmani, S. Alam Khan, A.F. Ahmad, Determination of total phenol, in-vitro antioxidant and anti-inflammatory activity of seeds and fruits of Zizyphus spina-christi grown in Oman. Asian Pac. J. Trop. Biomed. (2014). https://doi.org/10.12980/APJTB.4.2014APJTB-2014-0273
AOCS, in Official Methods and Recommended Practices of the American Oil Chemists Society, 4th edn. ed. by AOCS (AOCS, Champaign, 2006) (Official Method, Cd. 3–25 reapproved)
Y. Békro, J. Békro, B. Boua, H. Tra, E. Ehilé, Etude ethnobotanique et screening phytochimique de Caesalpinia benthamiana (Baill.) Herend. et Zarucchi (Caesalpiniaceae). Rev. Sci. Nat. 4, 217–225 (2006)
D. Chothani, N. Patel, Preliminary phytochemical screening, pharmacognostic and physicochemical evalution of leaf of Gmelina arborea. Asian Pac. J. Trop. Biomed. 2(Suppl 3), S1333–S1337 (2012)
E.J. Cho, T. Yokozawa, D.Y. Rhyu, Study on the inhibitory effects of Korean medicinal plants and their main compounds on the 1,1-diphenyl-2-picrylhydrazyl radical. Phytomedicine 10(6–7), 544–551 (2003)
N. Motohashi, H. Wakabayashi, T. Kurihara, Biological activity of Brabados cherry (acerola fruits, fruits of Malphigia emarginata DC) extracts and fractions. Phytother. Res. 18, 212–223 (2012)
E. Osorio-Esquivel, O. Alicia, V.B. Álvarez, L. Dorantes-Álvarez, M.M. Giusti, Phenolics, betacyanins and antioxidant activity in Opuntia joconostle fruits. Food Res. Int. 44, 2160–2168 (2011)
C. Chang, M. Yang, H. Wen, Estimation of total flavonoid content in propolis by two complementary colorimetric methods. J. Food Drug Anal. 10, 178182 (2002)
T.C. Dinis, V.M. Madeira, L.M. Almeida, Action of phenolic derivatives (acetaminophen, salicylate, and 5-aminosalicylate) as inhibitors of membrane lipid peroxidation and as peroxyl radical scavengers. Arch. Biochem. Biophys. 315, 161–169 (1994)
M.M. Giusti, R.E. Wrolstad, Characterization and Measurement of Anthocyanins by UV-Visible Spectroscopy, Current Protocols in Food Analytical Chemistry (Wiley, New York. 2001)
I. Amoo, O. Jokotagba, Comparative analysis of proximate, minerals and functional properties of Tamarindus indica pulp and Zizyphus spina-christi fruit and seed. Greener J. Agric. Sci. 2(1), 21–25 (2012)
A. Magdi, A. Mohammed, Chemical and proximate composition of (Zizyphus spina-christi) nabag fruit. Nutr. Food Sci. 39, 70–75 (2009)
A. Onilud, O. Igbinadolor, S. Wakil, Effect of varying relative humidity on the rancidity of cashew (Anacardium occidentale L.) kernel oil by lipolytic organisms. Afr. J. Biotechnol. 9(31), 4890–4896 (2010)
K. Agnieszka, G. Krzysztof, Criteria of Determination of Safe Grain Storage Time—A Review (InTech, Rijeka, 2013)
B. Soussen, H. Leila, Z. Sara, B. Houda, Composition minérale et vitaminique des fruits de cinq espèces sous exploitées en Algérie: Celtis australis L., Crataegus azarolus L., Crataegus monogyna Jacq., Elaeagnus angustifolia L. et Zizyphus lotus L. Fruits (Paris) 65, 75–84 (2010)
M. Montiel, S. Campista, L. Camacho, A. Rios, F. Delgado, Physicochemical and nutritional characteristics of fruits of Ziziphus sonorensis Wats (Rhamnaceae). Int. J. Food Sci. Nutr. 56(8), 587–596 (2005)
A.M.A. Abdalla, H. Baballa Gasmalla Elzebeir, Variation of physicochemical characteristics of Ziziphus spina-christi fruits from three geographical sites in Sudan. in Proceeding of the 5th Annual Conference of Postgraduate Studies and Scientific Research, Khartoum, Sudan, 2014. https://www.researchgate.net/publication/272351439_Variation_of_Physicochemical_Characteristics_of_Ziziphus_spina-christi_Fruits_from_Three_Geographical_Sites_in_Sudan
A. Jokotagba, F. Azim, A. Nour, R. A-Halim, A chemical study of Zizyphus spina-christi (Nabag) fruit grown in Sudan. Trop. Sci. 27, 271–273 (1987)
S.M. Saw, F.J. Nieto, J. Katz, S.J. Chew, Family risk scores and the relationship with myopia progression in Singapore children. Paper read at the VII International Myopia Conference, Taiwan. (1998)
M. Chouaibi, N. Mahfoudhi, L. Rezig, F. Donsì, G. Ferrari, S. Hamdi, Nutritional composition of Zizyphus lotus L. seeds. J. Sci. Food Agric. 92(6), 1171–1177 (2012)
P. Reinald, Membrane phospholipids, lipoxidative damage and molecular integrity: a causal role in aging and longevity. Biochim. Biophys. Acta (BBA)—Bioenerg. 1777(10), 1249–1262 (2008)
M. Abdeddaim, O. Lombarkia, A. Bacha, D. Fahloul, D. Abdeddaim, R. Farhat, M. Saadoudi, Y. Noui, A. Lekbir, Biochemical characterization and nutritional properties of Zizyphus lotus L. fruits in Aures region, Northeastern of Algeria. Ann. Food Sci. Technol. 15, 75–81 (2014)
M. Saadoudi, L. Hambaba, M. Abdeddaim, A. Lekbir, A. Bacha, S. Boudraa, S. Zidani, Nutritional composition, physical properties and sensory evaluation of biscuit produced from jujubes (fruits of Zizyphus lotus L.). Ann. Food Sci. Technol. 18(3) (2017). http://afst.valahia.ro/images/documente/2017/issue3/I.8_Saadoudi.pdf
C. Catoire, H. Zwang, C. Bouet, Les jujubiers ou le Ziziphus, Fruits oubliés n° 1 (1999)
A. El-Khateeb, E. Elsherbiny, L. Tadros, S. Ali, H. Hamed, Phytochemical analysis and antifungal activity of fruit leaves extracts on the mycelial growth of fungal plant pathogens. J. Plant Pathol. Microbiol. 4, 199 (2013)
A. Maciuk, C. Lavaud, P. Thépenier, M. Jacquier, K. Ghédira, M. Zèches-Hanrot, Four new dammarane saponins from Zizyphus lotus. J. Nat. Prod. 67(10), 1639–1643 (2004)
M. Hassan, A. Oyewale, J. Amupitan, M. Abduallahi, E. Okonkwo, Preliminary phytochemical and antibacterial investigation of crude extracts of the root bark of Detarium microcarpum. J. Chem. Soc. Nigeria 29(1), 26–29 (2004)
M. Ghalem, S. Merghache, M. Belarbi, Study on the antioxidant activities of root extracts of Zizyphus lotus from the western region of Algeria. Pharmacogn. J. 6(4), 32–42 (2014)
J. Renault, K. Ghedira, P. Thepenier, C. Lavaud, M. Zeches-Hanrot, Dammarane saponins from Zizyphus lotus. Phytochemistry 44(7), 1321–1327 (1997)
C. Rice-Evans, Flavonoids and isoflavones: absorption, metabolism and bioactivity. Free Radic. Biol Med. 36(7), 827–828 (2004)
A.M. Pawlowska, F. Camangi, A. Bader, A. Braca, Flavonoids of Zizyphus jujuba L. and Zizyphus spina-christi. (L.) Willd (Rhamnaceae) fruits. Food Chem. 112(4), 858–862 (2008)
M. Nawwar, M.S. Ishak, H.N. Michael, J. Buddrust, Leaf flavonoids of Ziziphus spina-christi. Phytochemistry. 23(9), 2110–2111 (1983)
M. Naczk, F. Shahidi, Phenolics in cereals, fruits and vegetables: occurrence, extraction and analysis. J. Pharm. Biomed. Anal. 41, 1523–1542 (2006)
E. Tan, A. Aminah, H. Khalid, M. Maskat, M. Ghani, Antioxidant properties of three banana cultivars (Musa acuminata‘Berangan’, ‘Mas’ and ‘Raja’) extracts. Sains Malays. 41, 319–324 (2012)
M. Alothman, A. Rajeev, A. Karim, Antioxidant capacity and phenolic content of selected tropical fruits from Malaysia, extracted with different solvents. Food Chem. 115, 785–788 (2009)
S. Jassabi, M. Abdullah, Extraction, purification and characterization of antioxidant fractions from Zizyphus spina-christi fruits. Am.-Eur. J. Toxicol. Sci. 5(3), 66–71 (2013)
S. Himesh, S. Sarvesh, P. Sharan, A. Singhai, Preliminary phytochemical screening and HPLC analysis of flavonoid from methanolic extract of leaves of Annona squamosa. Int. Res. J. Pharm. 2(5), 242–246 (2011)
R. Abraham, N. Carty, D. DuFour, M. Pincus, Clinical enzymology, in Henrys Clinical Diagnosis and Management by Laboratory Methods, 21 edn., Chap. 20, ed. by R. McPherson, M. Pincus (Sunders Elsevier, Philadelphia, 2006)
S. Lin, D. Traver, H. Zhu, K. Dooley, B. Paw, R.L. Zon, Analysis of Thrombocyte development in CD41-GFP transgenic zebrafish. Blood 106, 3803–3810 (2005)
U. Mallavadhani, A. Sudhakar, K. Sathyanarayana, A. Mahapatra, A. Li, B. Richard, Chemical and analytical screening of some edible mushrooms. Food Chem. 95, 58–64 (2006)
M. Tanaka, C. Kuie, Y. Nagashima, T. Taguchi, Applications of antioxidative maillard reaction products from histidine and glucose to sardine products. Nippon Suisan Gakaishi 54, 1409–1414 (1998)
G. Cheng, Y. Bai, Y. Zhao, J. Tao, Y. Liu, G. Tu, L. Ma, N. Liao, X. Xu, Flavonoids from Ziziphus jujube Mill var. spinosa. Tetrahedron 56, 8915–8920 (2000)
J. Jiang, X. Huang, J. Chen, Q. Lin, Comparison of the sedative and hypnotic effects of flavonoids, saponins, and polysaccharides extracted from Semen Ziziphus jujube. Nat. Prod. Res. 21, 310–320 (2007)
A. Pawlowska, F. Camangi, A. Bader, A. Braca, Flavonoids of Zizyphus jujube L. and Zizyphus spina-christi (L.) Willd (Rhamnaceae) fruits. Food Chem. 112, 858–862 (2009)
A. Schubert, D. Pereira, F. Zanin, S. Alves, R. Beck, M. Athayde, Comparison of antioxidant activities and total polyphenolic and methylxanthine contents between the unripe fruit and leaves of Ilex paraguariensis A. St. Hil. Pharm. Sci. 62, 876–880 (2007)
N. Turkmen, F. Sari, Y. Velioglu, Effects of extraction solvents on concentration and antioxidant activity of black and black mate tea polyphenols determined by ferrous tartrate and Folin-Ciocalteu methods. Food Chem. 99, 835–841 (2006)
M. Hertog, E. Feskens, D. Kromhout, P. Hollman, K. Katan, Dietary antioxidant flavonoids and risk of coronary heart disease: the Zutphen elderly study. Lancet 342, 1007–1011 (1993)
H. Mehansho, L. Butler, D. Carlson, Dietary tannins and salivary proline-rich proteins: interactions, induction, and defense mechanisms. Annu. Rev. Nutr. 7, 423–440 (1987)
W.C. Eric, S.Y. Eu, T.P. Pei, P. Yon, Antioxidant and antibacterial properties of green, black, and herbal teas of Camellia sinensis. Pharmacogn. Res. 3(4), 266–267 (2011)
A. Akinwumi, J. Faleye, Phytochemical quantification and in vitro antioxidant activity of the leaves, stem-bark and root of Nauclea latifolia Smith. FUW Trends Sci. Technol. J. 2(2)960–996 (2017)
A. Stapleton, Ultraviolet radiation and plants: burning questions. Plant Cell 4(11), 1353–1358 (1992)
P.T. Mpiana, K.N.N. Ngbolua, M.T. Bokota, T.K. Kasonga, E.K. Atibu, D.S. Tshibangu, V. Mudogo, In vitro effects of anthocyanin extracts from Justicia secunda Vahl on the solubility of haemoglobin S and membrane stability of sickle erythrocytes. Blood Transfus. 8(4), 248–254 (2010)
P. Mpiana, V. Mudogo, D.S.T. Tshibangu, E. Kitwa, A. Kanangila, J. Lumbu, K. Ngbolua, E. Atibu, M. Kakule, Antisickling activity of anthocyanins from Bombax pentadrum, Ficus capensis and Ziziphus mucronata: photodegradation effect. J. Ethnopharmacol. 120, 413–418 (2008)
P. Mpiana, V. Mudogo, D.T.S. Tshibangu, E. Kitwa, A. Kanangila, J. Lumbu, K. Ngbolua, E. Atibu, M. Kakule, Activité antifalcémiante et thermodégradation d’une fraction d’anthocyanes extraits de Zizyphus mucronata. Ann. Afr. Méd. 2, 91–97 (2009)
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El Maaiden, E., El Kharrassi, Y., Moustaid, K. et al. Comparative study of phytochemical profile between Ziziphus spina christi and Ziziphus lotus from Morocco. Food Measure 13, 121–130 (2019). https://doi.org/10.1007/s11694-018-9925-y
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DOI: https://doi.org/10.1007/s11694-018-9925-y