1Federal Education Institute, Science and Technology of Maranhão, Codó, Brazil
2Medicinal Plants Research Center, Health Sciences Center, Federal University of Piauí, Teresina, Brazil
3Federal Education Institute, Science and Technology of Maranhão, Caxias, Brazil
4Analytical Chemistry, Nutrition and Food Science Department, Faculty of Pharmacy, University of Santiago de Compostela, Santiago de Compostela, Spain
The gastric ulcer is definited as erosion of the stomach's mucosal wall, which affects over 4.6 million people per year. The objective was to investigate the phenolic profile and the antioxidant activity of Melipona compressipes fasciculata pot-pollen collected at seasons rainy (PPMF1) and dry (PPMF2), as well as the gastroprotective and ulcer healing activities of PPMF2, as PPMF1 did not have a gastroprotective effect in screening protocols. The phenolic profile revealed compounds such as caffeic acid, quercetin, myricetin and naringenin. In models of gastric lesions by ethanol, ischemia/reperfusion (I/R) and acetic acid, PPMF2 reduced the lesion area (at doses 3 to 80 mg/kg, p.o.) and volume at doses (3 to 24 mg/kg, p.o.) with protection at percent 52 to 92%. PPMF2 too, significantly (p<0.05) elevated mucus and non-protein sulfhydryl groups (SH-NP) with an increase of 122% and 92% respectivelly compared to vehicle group, and decreased malonaldehyde (MDA) in rats (36% compared to vehicle group). As for cicatrizant activity in acetic acid-induced ulcer, PPMF2 promoted healing rates until 97%, caused significant microscopic gastric recovery, elevation of SH-NP (103%), attenuation of MDA (84%) levels and improvement of biochemical profile (p<0.05). This is a relevant and pioneering research associating stingless bee (M. compressipes fasciculata) in gastroprotective activity studies.
| [1] | Idris, S., Mishra, A., Khushtar, M. Phytochemical Estimation and Therapeutic Amelioration of Aesculus hippocastanum L. Seeds Ethanolic Extract in Gastric Ulcer in Rats Possibly by Inhibiting Prostaglandin Synthesis. Chinese Journal of Integrative Medicine, 2023.View Article PubMed |
| [2] | Sales, I.R.P., Formiga, R.O., Machado, F.D.F., Nascimento, R.F., Pessoa, M.M.B., Barrosa, M.E.F.X., Vieira, G.C., Gadelha, F.A.A.F., Marinho, A.F., Barbosa Filho, J.M., Raimundo Júnior, F.A., Antunes, A.A., Batista, L.M. Cytoprotective, antioxidant and anti-inflammatory mechanism related to antiulcer activity of Cissampelos sympodialis Eichl. in animal models. Journal of Ethnopharmacology, 222, 190-200. 2018.View Article PubMed |
| [3] | Yibirin, M., De Oliveira, D., Valera, R., Plitt, A.E., Lutgen, S. Adverse Effects Associated with Proton Pump Inhibitor Use. Cureus, 13, e12759. 2021.View Article |
| [4] | Boutemine, I. M., Amri, M., Amir, Z. C., Fitting, C., Mecherara-Idjeri, S., Layaida, K., Sennoun, N., Berkane, S., Cavaillon, J. M., Touil-Boukoffa, C. Gastro-protective, therapeutic and anti-inflammatory activities of Pistacia lentiscus L. fatty oil against ethanol-induced gastric ulcers in rats. Journal of Ethnopharmacology, 224, 273-282. 2018.View Article PubMed |
| [5] | Karkar, B., Şahin, S., Güneş, M. E. Antioxidative effect of turkish chestnut bee pollen on DNA oxidation system and its phenolic compounds. GIDA/The Journal of FOOD, 43, 34-42. 2018.View Article |
| [6] | Lychkova, A. E., Kasyanenko, V. I., Puzikov, A. M. Gastroprotective effect of honey and bee pollen. Eksperimental'naia i klinicheskaia gastroenterologiia= Experimental & Clinical Gastroenterology, 9, 72-74. 2014. |
| [7] | Pascoal, A., Rodrigues, S., Teixeira, A., Feás, X., Estevinho, L. M. Biological activities of commercial bee pollens: Antimicrobial, antimutagenic, antioxidant and anti-inflammatory. Food and Chemical Toxicology, 63, 233-239. 2014.View Article PubMed |
| [8] | Zuluaga, C. M., Serrato, J. C., Quicazán, M. C. Valorization alternatives of colombian bee pollen for Its use as food resource - A structured review. Vitae. 21, 237-247. 2014.View Article |
| [9] | Vit, P., Pedro, S. R., Roubik, D. W. Pot-Pollen in Stingless Bee Melittology, 2018 (481), March 2018 [Online].View Article |
| [10] | Tomás, A., Falcão, S. I., Russo-Almeida, P., Vilas-Boas, M. Potentialities of beebread as a food supplement and source of nutraceuticals: Botanical origin, nutritional composition and antioxidant activity. Journal of Apicultural Research, 56, 219-230. 2017.View Article |
| [11] | Kerr, W. E., Carvalho, G. A., Nascimento, V. A. Abelha uruçu: biologia, manejo e conservação, 2, Fundação Acangaú. 1996. |
| [12] | Kieliszek, M., Piwowarek, K., Kot, A. M., Błażejak, S., Chlebowska-Śmigiel, A., Wolska, I. Pollen and bee bread as new health-oriented products: A review. Trends in Food Science & Technology, 71, 170-180. 2018.View Article |
| [13] | Devi, A., Kumar, N.R., Kaur, J. Evaluation of the antioxidative potential of bee products: pollen and bee bread against Staphylococcus aureus infected Balb/c mice. Journal of Chemical and Pharmaceutical Research, 4, 1-5. 2016. |
| [14] | Bobiş, O., Dezmirean, D., Mărghitaş, L.A., Bonta, V., Mărgăoan, R., Paşca, C., Urcan, A., Singh Bandhari, P. Beebread from Apis mellifera and Apis dorsata. Comparative Chemical Composition and Bioactivity. Bulletin of the University of Agricultural Sciences & Veterinary Medicine Cluj-Napoca. Animal Science & Biotechnologies, 74. 2017.View Article |
| [15] | Bogdanov S. Pollen: production, nutrition and health: a review. Bee Product Science. 3, 1-36. 2017. [Online]. Available: http://www.bee-hexagon.net/files/file/fileE/Health/PollenBook2Review.pdf/. [Accessed October 30, 2018]. |
| [16] | Bakour, M., Fernandes, Â., Barros, L., Sokovic, M., Ferreira, I. C. Bee bread as a functional product: Chemical composition and bioactive properties. LWT, 19.2019.View Article |
| [17] | Urcan, A., Mărghitaș, L. A., Dezmirean, D. S., Bobiș, O., Bonta, V., Mureșan, C. I., Mărgăoan, R. Chemical Composition and Biological Activities of Beebread-Review. Bulletin of the University of Agricultural Sciences & Veterinary Medicine Cluj-Napoca. Animal Science & Biotechnologies, 74(1). 2017. |
| [18] | Martínez-Casas, L., Lage-Yusty, M., & López-Hernández, J. Changes in the aromatic profile, sugars, and bioactive compounds when purple garlic is transformed into black garlic. Journal of Agricultural and Food Chemistry, 65(49), 10804-10811. 2017.View Article PubMed |
| [19] | Quirós, A.R.B., Lage-Yusty, M.A., López-Hernández, J. HPLC-analysis of polyphenolic compounds in Spanish white wines and determination of their antioxidant activity by radical scavenging assay. Food Research International, 42(8), 1018-1022. 2009.View Article |
| [20] | Robert, A., Nezamis, J.E., Lancaster, C., Hanchar, A.J. Cytoprotection by prostaglandins in rats: Prevention of gastric necrosis produced by alcohol, HCl, NaOH, hypertonic NaCl, and thermal injury. Gastroenterology, 77(3), 433-443. 1979.View Article PubMed |
| [21] | Bhargava, K.P., Gupta, M.B., Tangri, K.K. Mechanism of ulcerogenic activity of indomethacin and oxyphenbutazone. European Journal of Pharmacology, 22, 191-195. 1973.View Article PubMed |
| [22] | Ueda, S., Okada, Y. Acid secretagogues induce Ca2+ mobilization coupled to K+ conductance activation in rat parietal cells in tissue culture. Biochimica et Biophysica Acta (BBA)-Molecular Cell Research, 1012, 254-260. 1989.View Article |
| [23] | Visscher, F.E., Seay, P.H., Tazelaar, A.P., Veldkamp, W., Vander Brook, M.J. Pharmacology of pamine bromide. Journal of Pharmacology and Experimental Therapeutics, 110, 188-204. 1954. |
| [24] | Corne, S.J., Morrisey, S.M., Woods, R.J. A method for the quantitative estimation of gastric barrier mucus. Journal of Physiology, 242, 116-117. 1974. |
| [25] | Okabe, S., Pfeiffer, C.J. Chronicity of acetic acid ulcer in the rat stomach. The American Journal of Digestive Diseases, 17, 619-629. 1972.View Article PubMed |
| [26] | Potrich, F.B., Allemand, A., Da Silva, L.M., Dos Santos, A.C., Baggio, C.H., Freitas, C.S., Mendes, D.A.G.B., Andre, E., Werner, M.F.P., Marques, M. C. A. Antiulcerogenic activity of hydroalcoholic extract of Achillea millefolium L.: involvement of the antioxidant system. Journal of Ethnopharmacology, 130, 85-92. 2010.View Article PubMed |
| [27] | Mahmoud, Y.I., El-Ghffar, E.A.A. Spirulina ameliorates aspirin-induced gastric ulcer in albino mice by alleviating oxidative stress and inflammation. Biomedicine & Pharmacotherapy, 109, 314-321. 2019.View Article PubMed |
| [28] | Sedlak, J., Lindsay, R.H. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent. Analytical Biochemistry, 25, 192-205.1968.View Article PubMed |
| [29] | Ohkawa, H., Ohishi, N., Yagi, K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry, 95, 351-358. 1979.View Article PubMed |
| [30] | Nurdianah, H. F., Firdaus, A. A., Azam, O. E., Adnan, W.W. Antioxidant activity of bee pollen ethanolic extracts from Malaysian stingless bee measured using DPPH-HPLC assay. International Food Research Journal, 23, 403-405, 2016. |
| [31] | Silva, T., Camara, C.A., Lins, A., Agra, M.D.F., Silva, E., Reis, I.T., Freitas, B.M. Chemical composition, botanical evaluation and screening of radical scavenging activity of collected pollen by the stingless bees Melipona rufiventris (Uruçu-amarela). Anais da Academia Brasileira de Ciências, 81, 173-178. 2009.View Article PubMed |
| [32] | Leja, M., Mareczek, A., Wyżgolik, G., Klepacz-Baniak, J., Czekońska, K. Antioxidative properties of bee pollen in selected plant species. Food Chemistry, 100, 237-240. 2007.View Article |
| [33] | Sakanaka, S., Ishihara, Y. Comparison of antioxidant properties of persimmon vinegar and some other commercial vinegars in radical-scavenging assays and on lipid oxidation in tuna homogenates. Food Chemistry, 107, 739-744. 2008.View Article |
| [34] | Caliskan, O., Radusiene, J., Temizel, K.E., Staunis, Z., Cirak, C., Kurt, D., Odabas, M.S. The effects of salt and drought stress on phenolic accumulation in greenhouse-grown Hypericum pruinatum. Italian Journal of Agronomy, 12. 2017.View Article |
| [35] | Kocot, J., Kiełczykowska, M., Luchowska-Kocot, D., Kurzepa, J., Musik, I. Antioxidant potential of propolis, bee pollen, and royal jelly: Possible medical application. Oxidative Medicine and Cellular Longevity, 2018, 1-29. 2018.View Article PubMed |
| [36] | Ares, A.M., Valverde, S., Bernal, J.L., Nozal, M.J., Bernal, J. Extraction and determination of bioactive compounds from bee pollen. Journal of Pharmaceutical and Biomedical Analysis, 147, 110-124. 2018.View Article PubMed |
| [37] | Isidorov, V.A., Isidorova, A.G., Sczczepaniak, L., Czyżewska, U. Gas chromatographic–mass spectrometric investigation of the chemical composition of beebread. Food Chemistry, 115, 1056-1063. 2009.View Article |
| [38] | Urcan, A., Criste, A., Dezmirean, D., Mărgăoan, R., Caeiro, A., Graça Campos, M. Similarity of Data from Bee Bread with the Same Taxa Collected in India and Romania. Molecules, 23, 2491. 2018.View Article PubMed |
| [39] | Negri, G., Barreto, L.M.R.C., Sper, F.L., Carvalho, C.D., Campos, M.D.G.R. Phytochemical analysis and botanical origin of Apis mellifera bee pollen from the municipality of Canavieiras, Bahia State, Brazil. Brazilian Journal of Food Technology, 21, 1-17. 2018.View Article |
| [40] | Mărghitaş, L.A., Stanciu, O.G., Dezmirean, D.S., Bobiş, O., Popescu, O., Bogdanov, S., Campos, M.G. In vitro antioxidant capacity of honeybee-collected pollen of selected floral origin harvested from Romania. Food Chemistry, 115, 878-883. 2009.View Article |
| [41] | Barros, M.P., Lemos, M., Maistro, E.L., Leite, M.F., Sousa, J.P.B., Bastos, J.K., de Andrade, S.F. Evaluation of antiulcer activity of the main phenolic acids found in Brazilian Green Propolis. Journal of Ethnopharmacology, 120, 372-377. 2008.View Article PubMed |
| [42] | Kakkar, S., Bais, S.A review on protocatechuic acid and its pharmacological potential. ISRN Pharmacology, 2014, 1-9. 2014.View Article PubMed |
| [43] | La Casa, C., Villegas, I., De La Lastra, C.A., Motilva, V., Calero, M.M. Evidence for protective and antioxidant properties of rutin, a natural flavone, against ethanol induced gastric lesions. Journal of Ethnopharmacology, 71, 45-53. 2000.View Article PubMed |
| [44] | Kahraman, A., Erkasap, N., Köken, T., Serteser, M., Aktepe, F., Erkasap, S. The antioxidative and antihistaminic properties of quercetin in ethanol-induced gastric lesions. Toxicology, 183, 133-142. 2003.View Article PubMed |
| [45] | Yang, J., Zhou, W., Gu, Y., Dai, J., Li, X., Tai, P., Li, Y., Ma, X., & Zhang, Y. Protective effect of Pu-erh tea extracts against ethanol-induced gastric mucosal damage in rats. Biomedical Reports, 8, 335-342. 2018.View Article |
| [46] | Souza, M.C., Vieira, A.J., Beserra, F.P., Pellizzon, C.H., Nóbrega, R.H., Rozza, A. L. Gastroprotective effect of limonene in rats: influence on oxidative stress, inflammation and gene expression. Phytomedicine, 53, 37-42. 2019.View Article PubMed |
| [47] | Rujjanawate, C., Kanjanapothi, D., Amornlerdpison, D., Pojanagaroon, S. Anti-gastric ulcer effect of Kaempferia parviflora. Journal of ethnopharmacology, 102, 120-122. 2005.View Article PubMed |
| [48] | Chauhan, A.K., Kang, S.C. Therapeutic potential and mechanism of thymol action against ethanol-induced gastric mucosal injury in rat model. Alcohol, 49, 739-745. 2015.View Article PubMed |
| [49] | Zimmerman, B.J. Oxygen free radicals and the gastrointestinal tract: role of ischemia-reperfusion injury. Hepatogastroenterology, 41, 337-342.1994. |
| [50] | Granger, J.P., Alexander, B.T., Llinas, M.T., Bennett, W.A., Khalil, R.A. Pathophysiology of hypertension during preeclampsia linking placental ischemia with endothelial dysfunction. Hypertension, 38, 718-722. 2001.View Article PubMed |
| [51] | Kitano, H., Nishimura, H., Tachibana, H., Yoshikawa, H., Matsuyama, T. ORP150 ameliorates ischemia/reperfusion injury from middle cerebral artery occlusion in mouse brain. Brain Research, 1015, 122-128. 2004.View Article PubMed |
| [52] | Ibrahim, M., Hassan, W., Meinerz, D.F., de Oliveira Leite, G., Nogueira, C.W., Rocha, J.B. Ethanol-induced oxidative stress: the role of binaphthyl diselenide as a potent antioxidant. Biological Trace Element Research, 147, 309-314. 2012.View Article PubMed |
| [53] | Yeo, D., Hwang, S.J., Kim, W.J., Youn, H.J., Lee, H.J. The aqueous extract from Artemisia capillaris inhibits acute gastric mucosal injury by inhibition of ROS and NF-kB. Biomedicine & Pharmacotherapy, 99, 681-687. 2018.View Article PubMed |
| [54] | Sidahmed, H.M.A., Vadivelu, J., Loke, M.F., Arbab, I.A., Abdul, B., Sukari, M.A., Abdelwahab, S.I. Anti-ulcerogenic activity of dentatin from clausena excavata Burm. f. against ethanol-induced gastric ulcer in rats: Possible role of mucus and anti-oxidant effect. Phytomedicine, 55, 31-39. 2019.View Article PubMed |
| [55] | Ligumsky, M., Sestieri, M., Okon, E., Ginsburg, I. Antioxidants inhibit ethanol-induced gastric injury in the rat: role of manganese, glycine, and carotene. Scandinavian Journal of Gastroenterology, 30, 854-860. 1995.View Article PubMed |
| [56] | Dekanski, D., Ristić, S., Mitrović, D.M. Antioxidant effect of dry olive (Olea europaea L.) leaf extract on ethanol-induced gastric lesions in rats. Mediterranean Journal of Nutrition and Metabolism, 2, 205-211, 2009.View Article |
| [57] | Neamati, S., Alirezaei, M., Kheradmand, A. Ghrelin acts as an antioxidant agent in the rat kidney. International Journal of Peptide Research and Therapeutics, 17, 239. 2011.View Article |
| [58] | Szabo, S., Trier, J.S., & Frankel, P.W. Sulfhydryl compounds may mediate gastric cytoprotection. Science, 214, 200-202. 1981.View Article PubMed |
| [59] | Bilici, D., Süleyman, H., Banoğlu, Z.N., Kiziltunç, A., Avci, B., Çiftçioğlu, A., Bilici, S. Melatonin prevents ethanol-induced gastric mucosal damage possibly due to its antioxidant effect. Digestive Diseases and Sciences, 47, 856-861. 2002.View Article PubMed |
| [60] | Avila, J.R., De La Lastra, C.A., Martín, M.J., Motilva, V., Luque, I., Delgado, D., Esteban, J., Herrerias, J. Role of endogenous sulphydryls and neutrophil infiltration in the pathogenesis of gastric mucosal injury induced by piroxicam in rats. Inflammation Research, 45(2), 83-88. 1996.View Article PubMed |
| [61] | Karakoyun, B., Yüksel, M., Ercan, F., Erzik, C., Yeğen, B.Ç. Alpha-lipoic acid improves acetic acid-induced gastric ulcer healing in rats. Inflammation, 32, 37-46. 2009.View Article PubMed |
| [62] | Hayes, J.D., Mclellan, L.I. Glutathione and glutathione-dependent enzymes represent a co-ordinately regulated defence against oxidative stress. Free Radical Research, 31, 273-300. 1999.View Article PubMed |
| [63] | Kimura, M., Goto, S., Ihara, Y., Wada, A., Yahiro, K., Niidome, T., Aoyagi, H., Hirayama, T., & Kondo, T. Impairment of glutathione metabolism in human gastric epithelial cells treated with vacuolating cytotoxin fromHelicobacter pylori. Microbial Pathogenesis, 31, 29-36. 2001.View Article PubMed |
| [64] | Vajdovich, P. Free radicals and antioxidants in inflammatory processes and ischemia-reperfusion injury. Veterinary Clinics of North America: Small Animal Practice, 38, 31-123. 2008.View Article PubMed |
| [65] | Liju, V.B., Jeena, K., Kuttan, R. Gastroprotective activity of essential oils from turmeric and ginger. Journal of Basic and Clinical Physiology and Pharmacology, 26, 95-103. 2015.View Article PubMed |
| [66] | Tu, P.S., Tung, Y.T., Lee, W.T., Yen, G.C. Protective effect of camellia oil (Camellia oleifera Abel.) against ethanol-induced acute oxidative injury of the gastric mucosa in mice. Journal of Agricultural and Food Chemistry, 65, 4932-4941. 2017.View Article PubMed |
| [67] | Okabe, S., Amagase, K. An Overview of Acetic Acid Ulcer Models—The History and State of the Art of Peptic Ulcer Research—. Biological and Pharmaceutical Bulletin, 28, 1321-1341. 2005.View Article PubMed |
| [68] | Kangwan, N., Park, J.M., Kim, E.H., Hahm, K.B. Quality of healing of gastric ulcers: natural products beyond acid suppression. World journal of Gastrointestinal Pathophysiology, 5, 40-47. 2014.View Article PubMed |
| [69] | Tarnawski, A.S. Cellular and molecular mechanisms of gastrointestinal ulcer healing. Digestive Diseases and Sciences, 50, 24-33. 2005.View Article PubMed |
| [70] | Escobedo-Hinojosa, W.I., Gomez-Chang, E., García-Martínez, K., Guerrero Alquicira, R., Cardoso-Taketa, A., Romero, I. Gastroprotective Mechanism and Ulcer Resolution Effect of Cyrtocarpa procera Methanolic Extract on Ethanol-Induced Gastric Injury. Evidence-Based Complementary and Alternative Medicine, 2018, 1-12. 2018.View Article PubMed |
| [71] | Mei, X.T., Xu, D.H., Xu, S.K., Zheng, Y.P., Xu, S.B. Zinc (II)-curcumin accelerates the healing of acetic acid-induced chronic gastric ulcers in rats by decreasing oxidative stress and downregulation of matrix metalloproteinase-9. Food and Chemical Toxicology, 60, 448-454. 2013.View Article PubMed |
| [72] | Khalil, F.A., El-Sheikh, N.M. The effects of dietary Egyptian propolis and bee pollen supplementation against toxicity if sodium fluoride in rats. Journal of American Science, 11, 310-316. 2010. |
