Prophylactic Effect of Opuntia ficus indica Fruit Peel Extract against Irradiation-Induced Colon Injury in Rats

Salma A. Elsawi; Rasha R. Radwan; Marwa M. Elbatanony; Amal M. El-Feky; N. H. Sherif

doi:10.1055/a-1019-9801

Planta Medica, Table of Contents

Planta Med 2020; 86(01): 61-69
DOI: 10.1055/a-1019-9801

Biological and Pharmacological Activity

Original Papers

Georg Thieme Verlag KG Stuttgart · New York

Prophylactic Effect of Opuntia ficus indica Fruit Peel Extract against Irradiation-Induced Colon Injury in Rats

Authors

Salma A. Elsawi

¹Pharmacognosy Department, National Research Centre, Giza, Egypt
Rasha R. Radwan

²Drug Radiation Research Department, National Center for Radiation Research and Technology (NCRRT), Atomic Energy Authority, Cairo, Egypt
Marwa M. Elbatanony

¹Pharmacognosy Department, National Research Centre, Giza, Egypt
Amal M. El-Feky

¹Pharmacognosy Department, National Research Centre, Giza, Egypt
N. H. Sherif

²Drug Radiation Research Department, National Center for Radiation Research and Technology (NCRRT), Atomic Energy Authority, Cairo, Egypt

³Department of Pharmacognosy, Faculty of Pharmacy, Nahda University, Beni Suef, Egypt

Abstract

Opuntia ficus-indica extract has been used in traditional folk medicine for several purposes and exhibits anti-inflammatory properties. This study was directed to explore the prophylactic effect of O. ficus-indica fruit peel extract against irradiation-induced colitis in rats. GC/MS analysis of the petroleum ether extract led to recognition of 33 compounds in the unsaponifiable fraction and 15 fatty acid methyl esters in the saponifiable part. Thirteen terpenes and sterols were isolated and identified from which ten compounds were not isolated from any part of this species before. Data showed that irradiation induced colon injury as manifested by elevated contents of malondialdehyde, nitric oxide, myeloperoxidase, intercellular adhesion molecule-1, cyclooxygenase-2, tumor necrosis factor alpha, and nuclear factor kappa B, while it reduced superoxide dismutase activity and interleukin 10 content in colonic tissues, which was confirmed by histopathological examination. Pretreatment with O. ficus-indica extract attenuated the alteration in the measured parameters. It could be concluded that O. ficus-indica fruit peel extract can be regarded as a potential agent in limiting colonic complications due to irradiation, possibly by its antioxidant and anti-inflammatory properties.

Key words

Opuntia ficus-indica - Cactaceae - γ radiation - colitis - triterpenes

Full Text

References

References
1 El-Mostafa K, El Kharrassi Y, Badreddine A, Andreoletti P, Vamecq J, El Kebbaj MH, Latruffe N, Lizard G, Nasser B, Cherkaoui-Malki M. Nopal cactus (Opuntia ficus-indica) as a source of bioactive compounds for nutrition, health and disease. Molecules 2014; 19: 14879-14901
2 Benayad Z, Martinez-Villaluenga C, Frias J, Gomez-Cordoves C, Es-Safi NE. Phenolic composition, antioxidant and anti-inflammatory activities of extracts from Moroccan Opuntia ficus-indica flowers obtained by different extraction methods. Ind Crop Prod 2014; 62: 412-420
3 Berraaouan A, Abderrahim Z, Hassane M, Abdelkhaleq L, Mohammed A, Mohamed B. Evaluation of protective effect of cactus pear seed oil (Opuntia ficus-indica L. MILL.) against alloxan-induced diabetes in mice. Asian Pac J Trop Med 2015; 8: 532-537
4 Zou DM, Brewer M, Garcia F, Feugang JM, Wang J, Zang R, Liu H, Zou C. Cactus pear: a natural product in cancer chemoprevention. Nutr J 2005; 4: 25-36
5 Livrea MA, Tesoriere L. Antioxidant Activities of prickly Pear (Opuntia ficus indica) Fruit and its Betalains: Betanin and Indicaxanthin. In: Packer L, Nam OC, Halliwell B. Herbal and traditional Medicine. New York, USA: CRC Press; 2004: 562-581
6 Ramadan MF, Mörsel JT. Recovered lipids from prickly pear [Opuntia ficus-indica (L.) Mill] peel: a good source of polyunsaturated fatty acids, natural antioxidant vitamins and sterols. Food Chem 2003; 83: 447-456
7 Garg S, Wang W, Prabath BG, Boerma M, Wang J, Zhou D, Hauer-Jensen M. Bone marrow transplantation helps restore the intestinal mucosal barrier after total body irradiation in mice. Radiat Res 2014; 181: 229-239
8 Stacey R, Green JT. Radiation-induced small bowel disease: latest developments and clinical guidance. Ther Adv Chronic Dis 2014; 5: 15-29
9 Linard C, Ropenga A, Vozenin-Brotons M, Chapel A, Mathe D. Abdominal irradiation increases inflammatory cytokine expression and activates NF-κB in rat ileal muscularis layer. Am J Physiol Gastrointest Liver Physiol 2003; 285: G556-G565
10 Makhija D, Somani R, Chavan A. Synthesis and pharmacological evaluation of antiinflammatory mutual amide prodrugs. Indian J Pharm Sci 2013; 75: 353-357
11 Adams R. Identification of essential Oils by Ion Trap Mass Spectroscopy. San Diego, California: Academic Press; 1989: 1-302
12 El-Said NM, Nagib AI, Rahman ZA, Deraz SF. Prickly pear [Opuntia ficus-indica (L.) Mill] peels: chemical composition, nutritional value, and protective effects on liver and kidney functions and cholesterol in rats. Funct Plant Sci Biotechnol 2011; 5: 30-35
13 Nishimoto K, Ito M, Natori S, Ohmoto T. The structures of arundoin, cylindrin and fernenol: triterpenoids of fernane and arborane groups of Imperata cylindrica var. Koenigii. Tetrahedron 1968; 24: 735-752
14 Stiti N, Hartmann MA. Nonsterol triterpenoids as major constituents of Olea europaea . J Lipids 2012; 2012: 1-13
15 Fingolo C, Santos T, Kaplan M. Triterpene esters: natural products from Dorstenia arifolia (Moraceae). Molecules 2013; 18: 4247-4256
16 Assimopoulou A, Papageorgiou V. GC-MS analysis of penta-and tetra-cyclic triterpenes from resins of Pistacia species. Part I. Pistacia lentiscus var. Chia . Biomed Chromatogr 2005; 19: 285-311
17 Orhon ZN, Uzal C, Kanter M, Erboga M, Demiroglu M. Protective effects of Nigella sativa on gamma radiation-induced jejunal mucosal damage in rats. Pathol Res Pract 2016; 212: 437-443
18 Fernández-Gil B, Moneim AEA, Ortiz F, Shen YQ, Soto-Mercado V, Mendivil-Perez M, Guerra-Librero A, Acuña-Castroviejo D, Molina-Navarro MM, García-Verdugo JM. Melatonin protects rats from radiotherapy-induced small intestine toxicity. PLoS One 2017; 12: e0174474
19 Haton C, François A, Vandamme M, Wysocki J, Griffiths NM, Benderitter M. Imbalance of the antioxidant network of mouse small intestinal mucosa after radiation exposure. Radiat Res 2007; 167: 445-453
20 Radwan RR, Mohamed HA. Nigella sativa oil modulates the therapeutic efficacy of mesenchymal stem cells against liver injury in irradiated rats. J Photochem Photobiol B 2018; 178: 447-456
21 Oliveira A, Barbosa G, Verdam M, Ohana D, Mendonça M, Meira R. Analgesic and anti-inflammatory effect of the aqueous extract of “trevo-roxo” (Scutellaria agrestis A. St.-Hil. ex Benth.-Lamiaceae) leaves in rodents. Rev Bras Plantas Med 2014; 16: 174-181
22 Pinto ME, Araujo SG, Morais MI, Sá NP, Lima CM, Rosa CA, Siqueira EP, Johann S, Lima LA. Antifungal and antioxidant activity of fatty acid methyl esters from vegetable oils. An Acad Bras Ciênc 2017; 89: 1671-1681
23 El-Razek FHA, El-Metwally EM, Shehab GM, Hassan AA, Gomaa AM. Effects of cactus pear (Opuntia ficus indica) juice on oxidative stress in diabetic cataract rats. Saudi J Health Sci 2012; 1: 23-29
24 Salem HA, Wadie W. Effect of niacin on inflammation and angiogenesis in a murine model of ulcerative colitis. Sci Rep 2017; 7: 7139-7146
25 Deniz M, Atasoy BM, Dane F, Can G, Erzik C, Çetinel Ş, Yeğen BÇ. Radiation-induced oxidative injury of the ileum and colon is alleviated by glucagon-like peptide-1 and-2. J Radiat Res Appl Sci 2015; 8: 234-242
26 Ikeda Y, Ito M, Matsuu M, Shichijo K, Fukuda E, Nakayama T, Nakashima M, Naito S, Sekine I. Expression of ICAM-1 and acute inflammatory cell infiltration in the early phase of radiation colitis in rats. J Radiat Res 2000; 41: 279-291
27 Yeoh E. Radiotherapy: long-term effects on gastrointestinal function. Curr Opin Support Palliat Care 2008; 2: 40-44
28 Prakash V. Terpenoids as source of anti-inflammatory compounds. Asian J Pharm Clin Res 2017; 10: 68-76
29 Tsai JC, Peng WH, Chiu TH, Lai SC, Lee CY. Anti-inflammatory effects of Scoparia dulcis L. and betulinic acid. Am J Chin Med 2011; 39: 943-956
30 Okunieff P, Cornelison T, Mester M, Liu W, Ding I, Chen Y, Zhang H, Williams JP, Finkelstein J. Mechanism and modification of gastrointestinal soft tissue response to radiation: role of growth factors. Int J Radiat Oncol Biol Phys 2005; 62: 273-278
31 Kountouras J, Zavos C. Recent advances in the management of radiation colitis. World J Gastroenterol 2008; 14: 7289-7301
32 Izcue A, Coombes JL, Powrie F. Regulatory lymphocytes and intestinal inflammation. Annu Rev Immunol 2009; 27: 313-338
33 Nakamura K, Honda K, Mizutani T, Akiho H, Harada N. Novel strategies for the treatment of inflammatory bowel disease: selective inhibition of cytokines and adhesion molecules. World J Gastroenterol 2006; 12: 4628-4635
34 Wazea SA, Wadie W, Bahgat AK, El-Abhar HS. Galantamine anti-colitic effect: Role of alpha-7 nicotinic acetylcholine receptor in modulating Jak/STAT3, NF-κB/HMGB1/RAGE and p-AKT/Bcl-2 pathways. Sci Rep 2018; 8: 5110-5119
35 Frondoza CG, Sohrabi A, Polotsky A, Phan PV, Hungerford DS, Lindmark L. An in vitro screening assay for inhibitors of proinflammatory mediators in herbal extracts using human synoviocyte cultures. In Vitro Cell Dev Biol Anim 2004; 40: 95-101
36 Odabasi M, Gokdemir S, Muftuoglu T, Aktekin A, Saglam A, Aker F. Prophylactic and therapeutic effects of oral budesonide for acute radiation-induced enteritis and colitis in rats. Int J Clin Exp Med 2014; 7: 940-946
37 Stahl E. Apparatus and general Techniques in TLC. In: Stahl E. Thin-layer Chromatography. Berlin, Heidelberg, New York: Springer; 1969: 52-86
38 Tsuda K, Sakai K, Tanabe K, Kishida Y. Isolation of 22-dehydrocholesterol from Hypnea japonica . Chem Pharm Bull 1959; 7: 747-747
39 Finar L. Organic Chemistry, Volume 1. In: Finar L. Modern Arene Chemistry. London: Longmans Green and Co. Ltd.; 1967: 212
40 Toklu HZ, Şehİrlİ Ö, Özyurt H, Mayadagli AA, Ekşİoğlu-Demİralp E, Çetİnel Ş, Şahİn H, Yeğen BÇ, Dumlu MU, Gökmen V, Şener G. Punica granatum peel extract protects against ionizing radiation-induced enteritis and leukocyte apoptosis in rats. J Radiat Res 2009; 50: 345-353
41 Kim SH, Jeon BJ, Kim DH, Kim TI, Lee HK, Han DS, Lee JH, Kim TB, Kim JW, Sung SH. Prickly pear cactus (Opuntia ficus indica var. saboten) protects against stress-induced acute gastric lesions in rats. J Med Food 2012; 15: 968-973
42 Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979; 95: 351-358
43 Marklund S, Marklund G. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 1974; 47: 469-474
44 Montgomery H, Dymock JF. Determination of nitrite in water. Analyst 1961; 86: 414-416
45 Bradley PP, Priebat DA, Christensen RD, Rothstein G. Measurement of cutaneous inflammation: estimation of neutrophil content with an enzyme marker. J Invest Dermatol 1982; 78: 206-209