Protective effect of royal jelly against diclofenac-induced hepato-renal damage and gastrointestinal ulcerations in rats
Loading...
Date
2020-02
Journal Title
Journal ISSN
Volume Title
Type
Article
Publisher
Elsevier
Series Info
Heliyon;Volume 6, Issue 2, February 2020, Article number e03330
Doi
Scientific Journal Rankings
Abstract
Royal jelly; Diclofenac; Hepatic; Renal; Gastrointestinal; Inflammation; Rats; Pharmaceutical science; Biochemistry; Molecular biology; Gastrointestinal system; Renal system; Pathology; Pharmacology; Toxicology © 2020
Objective: Evaluation of traditionally used royal jelly (RJ) for the management of hepato-renal damage and gastrointestinal ulcerations caused by diclofenac. Methods: Forty adult male Wistar rats were allocated into four groups. Rats of the 1st group received only saline and served as normal group. The remaining 3 groups received diclofenac (50 mg/kg/day, I.P.) for 7 days. Group 2 served as diclofenac-control group. Groups 3 and 4 received RJ (150 and 300 mg/kg/day, P.O.) respectively for 30 days. Twenty-four hours after the last treatment, blood samples were collected, rats were sacrificed, and livers, kidneys, stomachs & intestines were harvested. Stomachs and intestines were tested for ulcer counts. Serum levels of AST, ALT, creatinine and urea were investigated. Hepatic, renal, gastric and intestinal tissue contents of myeloperoxidase (MPO) and prostaglandin-E2 (PGE2) were measured. Histopathological examinations were also performed followed by immunohistochemical determination of cyclooxygenase-2 (COX-2) and inducible nitric oxide synthase (iNOS) expression. Results: Diclofenac administration caused significant deterioration of all the above mentioned parameters. RJ improved hepatic and renal functions. Gastric and intestinal ulcer counts were significantly ameliorated. Hepatic, renal, gastric and intestinal tissue PGE-2 contents and COX-2 expression were significantly elevated. RJ also significantly reduced MPO content and iNOS expression as compared to diclofenac-control group. Improvements of the histopathological pictures of hepatic, renal, gastric and intestinal tissues were also apparent. Conclusion: The study demonstrates promising protective effects of RJ against diclofenac-induced hepato-renal damage and gastrointestinal ulceration in rats.
Description
scopus
Keywords
Toxicology, Royal jelly, Renal system, Renal, Rats, Pharmacology, Pharmaceutical science, Pathology, Molecular biology, Inflammation, Hepatic, Gastrointestinal system, Gastrointestinal, Diclofenac, Biochemistry
Citation
Abdel-Hafez, S.M.N., Rifaai, R.A., Abdelzaher, W.Y. Possible protective effect of royal jelly against cyclophosphamide induced prostatic damage in male albino rats; a biochemical, histological and immuno-histo-chemical study (2017) Biomedicine and Pharmacotherapy, 90, pp. 15-23. Cited 8 times. www.elsevier.com/locate/biomedpharm doi: 10.1016/j.biopha.2017.03.020 View at Publisher 2 Adeyemi, W.J., Olayaki, L.A. Diclofenac – induced hepatotoxicity: Low dose of omega-3 fatty acids have more protective effects (Open Access) (2018) Toxicology Reports, 5, pp. 90-95. Cited 13 times. http://www.journals.elsevier.com/toxicology-reports/ doi: 10.1016/j.toxrep.2017.12.002 View at Publisher 3 Ahmad, I., Jimenez, H., Yaacob, N.S., Yusuf, N. Tualang honey protects keratinocytes from ultraviolet radiation-induced inflammation and DNA damage (2012) Photochemistry and Photobiology, 88 (5), pp. 1198-1204. Cited 26 times. doi: 10.1111/j.1751-1097.2012.01100.x View at Publisher 4 Ahmed, W.M.S., Khalaf, A.A., Moselhy, W.A., Safwat, G.M. Royal jelly attenuates azathioprine induced toxicity in rats (2014) Environmental Toxicology and Pharmacology, 37 (1), pp. 431-437. Cited 11 times. doi: 10.1016/j.etap.2013.12.010 View at Publisher 5 Aslan, Z., Aksoy, L. Anti-inflammatory effects of royal jelly on ethylene glycol induced renal inflammation in rats (Open Access) (2015) International Braz J Urol, 41 (5), pp. 1008-1013. Cited 15 times. http://www.scielo.br/pdf/ibju/v41n5/1677-5538-ibju-41-5-1008.pdf doi: 10.1590/S1677-5538.IBJU.2014.0470 View at Publisher 6 Baker, W.L. NSAIDs and Cardiovascular Toxicity (2018) Comprehensive Toxicology: Third Edition, 13-15, pp. 341-355. Cited 2 times. http://www.sciencedirect.com/science/book/9780081006016 ISBN: 978-008100612-2; 978-008100601-6 doi: 10.1016/B978-0-12-801238-3.95640-X View at Publisher 7 Bancroft, J., Stevens, A., Turner, D. Theory and Practice of Histological Techniques (1996) , p. 766. Cited 5618 times. Churchill Livingstone New York 8 Beck, W.S., Schneider, H.T., Dietzel, K., Nuernberg, B., Brune, K. Gastrointestinal ulcerations induced by anti-inflammatory drugs in rats - Physicochemical and biochemical factors involved (1990) Archives of Toxicology, 64 (3), pp. 210-217. Cited 99 times. doi: 10.1007/BF02010727 View at Publisher 9 Bernardi, A., Zilberstein, A.A.C.C.V., Jäger, E., Campos, M.M., Morrone, F.B., Calixto, J.B., Pohlmann, A.R., (...), Battastini, A.M.O. Effects of indomethacin-loaded nanocapsules in experimental models of inflammation in rats (2009) British Journal of Pharmacology, 158 (4), pp. 1104-1111. Cited 90 times. doi: 10.1111/j.1476-5381.2009.00244.x View at Publisher 10 Bevaart, L., Vervoordeldonk, M.J., Tak, P.P. Evaluation of therapeutic targets in animal models of arthritis: How does it relate to rheumatoid arthritis? (2010) Arthritis and Rheumatism, 62 (8), pp. 2192-2205. Cited 135 times. http://www3.interscience.wiley.com/cgi-bin/fulltext/123344154/PDFSTART doi: 10.1002/art.27503 View at Publisher 11 Bjarnason, I., Scarpignato, C., Holmgren, E., Olszewski, M., Rainsford, K.D., Lanas, A. Mechanisms of Damage to the Gastrointestinal Tract From Nonsteroidal Anti-Inflammatory Drugs (Open Access) (2018) Gastroenterology, 154 (3), pp. 500-514. Cited 66 times. http://www.journals.elsevier.com/gastroenterology/ doi: 10.1053/j.gastro.2017.10.049 View at Publisher 12 Blanca-Lopez, N., Canto, M.G., Blanca, M. Other NSAIDs Reactions (2018) Drug Allergy Testing, pp. 177-196. Cited 2 times. http://www.sciencedirect.com/science/book/9780323485517 ISBN: 978-032349707-7; 978-032348551-7 doi: 10.1016/B978-0-323-48551-7.00018-3 View at Publisher 13 Bradley, P.P., Priebat, D.A., Christensen, R.D., Rothstein, G. Measurement of cutaneous inflammation: Estimation of neutrophil content with an enzyme marker (Open Access) (1982) Journal of Investigative Dermatology, 78 (3), pp. 206-209. Cited 2674 times. doi: 10.1111/1523-1747.ep12506462 View at Publisher 14 Cemek, M., Aymelek, F., Büyükokuroĝlu, M.E., Karaca, T., Büyükben, A., Yilmaz, F. Protective potential of Royal Jelly against carbon tetrachloride induced-toxicity and changes in the serum sialic acid levels (2010) Food and Chemical Toxicology, 48 (10), pp. 2827-2832. Cited 64 times. doi: 10.1016/j.fct.2010.07.013 View at Publisher 15 Chan, Q.W.T., Melathopoulos, A.P., Pernal, S.F., Foster, L.J. The innate immune and systemic response in honey bees to a bacterial pathogen, Paenibacillus larvae (Open Access) (2009) BMC Genomics, 10, art. no. 387. Cited 79 times. doi: 10.1186/1471-2164-10-387 View at Publisher 16 Devi, R.S., Narayan, S., Vani, G., Shyamala Devi, C.S. Gastroprotective effect of Terminalia arjuna bark on diclofenac sodium induced gastric ulcer (2007) Chemico-Biological Interactions, 167 (1), pp. 71-83. Cited 60 times. doi: 10.1016/j.cbi.2007.01.011 View at Publisher 17 El-Maddawy, Z.K., El-Ashmawy, I.M. Hepato-renal and hematological effects of diclofenac sodium in rats (2013) Global Journal of Pharmacology, 7 (2), pp. 123-132. Cited 26 times. http://www.idosi.org/gjp/7(2)13/5.pdf doi: 10.5829/idosi.gjp.2013.7.2.72171 View at Publisher 18 El-Nekeety, A.A., El-Kholy, W., Abbas, N.F., Ebaid, A., Amra, H.A., Abdel-Wahhab, M.A. Efficacy of royal jelly against the oxidative stress of fumonisin in rats (2007) Toxicon, 50 (2), pp. 256-269. Cited 72 times. doi: 10.1016/j.toxicon.2007.03.017 View at Publisher 19 El-Yazbi, A.F., Eid, A.H., El-Mas, M.M. Cardiovascular and renal interactions between cyclosporine and NSAIDs: Underlying mechanisms and clinical relevance (2018) Pharmacological Research, 129, pp. 251-261. Cited 7 times. http://www.elsevier.com/inca/publications/store/6/2/2/9/3/1/index.htt doi: 10.1016/j.phrs.2017.11.029 View at Publisher 20 Erdal, T., Sefa, L. Investigation of possible cardiac side effects of diclofenac in exercise-treated rats (2017) Biomedical Research (India), 28 (17), pp. 7675-7678. http://www.biomedres.info/biomedical-research/investigation-of-possible-cardiac-side-effects-of-diclofenac-in-exercisetreated-rats.pdf 21 Gan, T.J. Diclofenac: An update on its mechanism of action and safety profile (2010) Current Medical Research and Opinion, 26 (7), pp. 1715-1731. Cited 194 times. http://informahealthcare.com/loi/cmo doi: 10.1185/03007995.2010.486301 View at Publisher 22 Ghanbari, E., Nejati, V., Azadbakht, M. Protective effect of royal jelly against renal damage in streptozotocin induced diabetic rats (2015) Iran. J. Toxicol., 9 (28), pp. 1258-1263. Cited 10 times. 23 Peter S, J., Basha S, K., Giridharan, R., Lavinya B, U., Sabina, E.P. Suppressive effect of Spirulina fusiformis on diclofenac-induced hepato-renal injury and gastrointestinal ulcer in Wistar albino rats: A biochemical and histological approach (2017) Biomedicine and Pharmacotherapy, 88, pp. 11-18. Cited 15 times. www.elsevier.com/locate/biomedpharm doi: 10.1016/j.biopha.2017.01.032 View at Publisher 24 Huang, T., Zhang, G., Chong, S., Liu, Y., Zhang, N., Fang, S., Zhu, J. Effects and mechanism of diclofenac degradation in aqueous solution by US/Zn0 (2017) Ultrasonics Sonochemistry, 37, pp. 676-685. Cited 7 times. www.elsevier.com/inca/publications/store/5/2/5/4/5/1 doi: 10.1016/j.ultsonch.2017.02.032 View at Publisher 25 Ibrahim, A. Immunomodulatory effects of royal jelly on aorta CD3, CD68 and eNOS expression in hypercholesterolaemic rats (2014) J. Basic Appl. Zool., 67, pp. 140-148. Cited 7 times. 26 Ibrahim, A., Eldaim, M.A.A., Abdel-Daim, M.M. Nephroprotective effect of bee honey and royal jelly against subchronic cisplatin toxicity in rats (2016) Cytotechnology, 68 (4), pp. 1039-1048. Cited 23 times. http://www.springer.com/chemistry/biotech/journal/10616 doi: 10.1007/s10616-015-9860-2 View at Publisher 27 Ilic, S., Drmic, D., Franjic, S., Kolenc, D., Coric, M., Brcic, L., Klicek, R., (...), Sikiric, P. Pentadecapeptide BPC 157 and its effects on a NSAID toxicity model: Diclofenac-induced gastrointestinal, liver, and encephalopathy lesions (2011) Life Sciences, 88 (11-12), pp. 535-542. Cited 36 times. doi: 10.1016/j.lfs.2011.01.015 View at Publisher 28 Kanbur, M., Eraslan, G., Beyaz, L., Silici, S., Liman, B.C., Altinordulu, S., Atasever, A. The effects of royal jelly on liver damage induced by paracetamol in mice (2009) Experimental and Toxicologic Pathology, 61 (2), pp. 123-132. Cited 61 times. doi: 10.1016/j.etp.2008.06.003 View at Publisher 29 Karaca, T., Bayiroglu, F., Yoruk, M., Kaya, M.S., Uslu, S., Comba, B., Mis, L. Effect of royal jelly on experimental colitis induced by acetic acid and alteration of mast cell distribution in the colon of rats (Open Access) (2010) European Journal of Histochemistry, 54 (4), pp. 158-161. Cited 15 times. http://www.ejh.it/index.php/ejh/article/viewFile/ejh.2010.e35/1924 doi: 10.4081/ejh.2010.e35 View at Publisher 30 Karaca, T., Şimşek, N., Uslu, S., Kalkan, Y., Can, I., Kara, A., Yörük, M. The effect of royal jelly on CD3+, CD5+, CD45+ T-cell and CD68+ cell distribution in the colon of rats with acetic acid-induced colitis (2012) Allergologia et Immunopathologia, 40 (6), pp. 357-361. Cited 15 times. doi: 10.1016/j.aller.2011.09.004 View at Publisher 31 Karaca, T., Uz, Y.H., Demirtas, S., Karaboga, I., Can, G. Protective effect of royal jelly in 2,4,6 trinitrobenzene sulfonic acid-induced colitis in rats (2015) Iranian Journal of Basic Medical Sciences, 18 (4), pp. 370-379. Cited 9 times. http://ijbms.mums.ac.ir/pdf_4286_bda319ebeacacd60c57dac499c123a58.html 32 Karadeniz, A., Simsek, N., Karakus, E., Yildirim, S., Kara, A., Can, I., Kisa, F., (...), Turkeli, M. Royal jelly modulates oxidative stress and apoptosis in liver and kidneys of rats treated with cisplatin (Open Access) (2011) Oxidative Medicine and Cellular Longevity, art. no. 981793. Cited 71 times. doi: 10.1155/2011/981793 View at Publisher 33 Kaynar, L., Cetin, A., Hacioglu, S.K., Eser, B., Koçyigit, I., Canöz, Ö., Tasdemir, A., (...), Silici, S. Efficacy of royal jelly on methotrexate-induced systemic oxidative stress and damage to small intestine in rats (Open Access) (2012) African Journal of Traditional, Complementary and Alternative Medicines, 9 (3), pp. 412-417. Cited 10 times. http://www.bioline.org.br/pdf?tc12057 doi: 10.4314/ajtcam.v9i3.17 View at Publisher 34 Khan, M.I., Khan, M.R. Gastroprotective Potential of Dalbergia sissoo Roxb. Stem Bark against Diclofenac-Induced Gastric Damage in Rats (Open Access) (2013) Osong Public Health and Research Perspectives, 4 (5), pp. 271-277. Cited 10 times. doi: 10.1016/j.phrp.2013.09.006 View at Publisher 35 Khan, R.A. Natural products chemistry: The emerging trends and prospective goals (Open Access) (2018) Saudi Pharmaceutical Journal, 26 (5), pp. 739-753. Cited 9 times. http://www.sciencedirect.com/science/journal/13190164 doi: 10.1016/j.jsps.2018.02.015 View at Publisher 36 Kohno, K., Okamoto, I., Sano, O., Arai, N., Iwaki, K., Ikeda, M., Kurimoto, M. Royal jelly inhibits the production of proinflammatory cytokines by activated macrophages (2004) Bioscience, Biotechnology and Biochemistry, 68 (1), pp. 138-145. Cited 137 times. doi: 10.1271/bbb.68.138 View at Publisher 37 Lanas, A. Role of nitric oxide in the gastrointestinal tract (Open Access) (2008) Arthritis Research and Therapy, 10 (SUPPL. 2), art. no. S4. Cited 76 times. doi: 10.1186/ar2465 View at Publisher 38 Mansour, D.F., Saleh, D.O., Mostafa, R.E. Genistein ameliorates cyclophosphamide - induced hepatotoxicity by modulation of oxidative stress and inflammatory mediators (Open Access) (2017) Open Access Macedonian Journal of Medical Sciences, 5 (7), pp. 836-843. Cited 9 times. https://www.id-press.eu/mjms/article/download/oamjms.2017.093/1690 doi: 10.3889/oamjms.2017.093 View at Publisher 39 Masubuchi, Y., Nakayama, S., Horie, T. Role of mitochondrial permeability transition in diclofenac-induced hepatocyte injury in rats (2002) Hepatology, 35 (3), pp. 544-551. Cited 131 times. http://onlinelibrary.wiley.com/journal/10.1002/(ISSN)1527-3350 doi: 10.1053/jhep.2002.31871 View at Publisher 40 Mohamed, A.A.-R., Galal, A.A.A., Elewa, Y.H.A. Comparative protective effects of royal jelly and cod liver oil against neurotoxic impact of tartrazine on male rat pups brain (2015) Acta Histochemica, 117 (7), pp. 649-658. Cited 32 times. www.urbanfischer.de/journals/actahist/acthist.htm doi: 10.1016/j.acthis.2015.07.002 View at Publisher 41 Mostafa, R.E. Potential anti-oxidant and anti-inflammatory effects of losartan against thioacetamide-induced hepatic damage in rats (2018) Latin American Journal of Pharmacy, 37 (6), pp. 1089-1096. http://www.latamjpharm.org/download_file.php?idt=3912&hax=WOI9RERDOH 42 Mostafa, R.E., Saleh, D.O., Mansour, D.F. Cisplatin-induced nephrotoxicity in rats: Modulatory role of simvastatin and rosuvastatin against apoptosis and inflammation (Open Access) (2018) Journal of Applied Pharmaceutical Science, 8 (4), pp. 43-50. Cited 2 times. http://www.japsonline.com/admin/php/uploads/2598_pdf.pdf doi: 10.7324/JAPS.2018.8406 View at Publisher 43 Mózsik, Gy., Morón, F., Jávor, T. Cellular mechanisms of the development of gastric mucosal damage and of gastrocytoprotection induced by prostacyclin in rats. A pharmacological study (1982) Prostaglandins, Leukotrienes and Medicine, 9 (1), pp. 71-84. Cited 72 times. doi: 10.1016/0262-1746(82)90074-9 View at Publisher 44 Nathan, C. Inducible nitric oxide synthase: What difference does it make? (Open Access) (1997) Journal of Clinical Investigation, 100 (10), pp. 2417-2423. Cited 796 times. http://www.jci.org doi: 10.1172/JCI119782 View at Publisher 45 Nouri, A., Heidarian, E., Nikoukar, M. Effects of N-acetyl cysteine on oxidative stress and TNF-α gene expression in diclofenac-induced hepatotoxicity in rats (2017) Toxicology Mechanisms and Methods, 27 (8), pp. 561-567. Cited 15 times. doi: 10.1080/15376516.2017.1334732 View at Publisher 46 Oka, H., Emori, Y., Kobayashi, N., Hayashi, Y., Nomoto, K. Suppression of allergic reactions by royal jelly in association with the restoration of macrophage function and the improvement of Th1/Th2 cell responses (2001) International Immunopharmacology, 1 (3), pp. 521-532. Cited 73 times. doi: 10.1016/S1567-5769(00)00007-2 View at Publisher 47 S, J.P., Evan Prince, S. Diclofenac-induced renal toxicity in female Wistar albino rats is protected by the pre-treatment of aqueous leaves extract of Madhuca longifolia through suppression of inflammation, oxidative stress and cytokine formation (2018) Biomedicine and Pharmacotherapy, 98, pp. 45-51. Cited 8 times. www.elsevier.com/locate/biomedpharm doi: 10.1016/j.biopha.2017.12.028 View at Publisher 48 Pyrzanowska, J., Piechal, A., Blecharz-Klin, K., Joniec-Maciejak, I., Graikou, K., Chinou, I., Widy-Tyszkiewicz, E. Long-term administration of Greek Royal Jelly improves spatial memory and influences the concentration of brain neurotransmitters in naturally aged Wistar male rats (2014) Journal of Ethnopharmacology, 155 (1), pp. 343-351. Cited 11 times. www.elsevier.com/locate/jethpharm doi: 10.1016/j.jep.2014.05.032 View at Publisher 49 Ramm, S., Mally, A. Role of drug-independent stress factors in liver injury associated with diclofenac intake (2013) Toxicology, 312 (1), pp. 83-96. Cited 24 times. doi: 10.1016/j.tox.2013.08.002 View at Publisher 50 Ratliff, B.B., Abdulmahdi, W., Pawar, R., Wolin, M.S. Oxidant mechanisms in renal injury and disease (Open Access) (2016) Antioxidants and Redox Signaling, 25 (3), pp. 119-146. Cited 107 times. www.liebertonline.com/ars doi: 10.1089/ars.2016.6665 View at Publisher 51 Silici, S., Ekmekcioglu, O., Kanbur, M., Deniz, K. The protective effect of royal jelly against cisplatin-induced renal oxidative stress in rats (2011) World Journal of Urology, 29 (1), pp. 127-132. Cited 59 times. doi: 10.1007/s00345-010-0543-5 View at Publisher 52 Sullivan, G.W., Sarembock, I.J., Linden, J. The role of inflammation in vascular diseases (2000) Journal of Leukocyte Biology, 67 (5), pp. 591-602. Cited 216 times. http://jlb.onlinelibrary.wiley.com/hub/journal/10.1002/(ISSN)1938-3673/ doi: 10.1002/jlb.67.5.591 View at Publisher 53 Takeuchi, K., Tanaka, A., Kato, S., Amagase, K., Satoh, H. Roles of COX inhibition in pathogenesis of NSAID-induced small intestinal damage (2010) Clinica Chimica Acta, 411 (7-8), pp. 459-466. Cited 74 times. doi: 10.1016/j.cca.2009.12.026 View at Publisher 54 Teixeira, R.R., de Souza, A.V., Peixoto, L.G., Machado, H.L., Caixeta, D.C., Vilela, D.D., Baptista, N.B., (...), Espindola, F.S. Royal jelly decreases corticosterone levels and improves the brain antioxidant system in restraint and cold stressed rats (Open Access) (2017) Neuroscience Letters, 655, pp. 179-185. Cited 15 times. www.elsevier.com/locate/neulet doi: 10.1016/j.neulet.2017.07.010 View at Publisher 55 Yasmeen, T., Qureshi, G.S., Perveen, S. Adverse effects of Diclofenac sodium on renal parenchyma of adult albino rats (2007) Journal of the Pakistan Medical Association, 57 (7), pp. 349-351. Cited 15 times. 56 Zhang, S., Nie, H., Shao, Q., Hassanyar, A.K., Su, S. RNA-Seq analysis on effects of royal jelly on tumour growth in 4T1-bearing mice (2017) Journal of Functional Foods, 36, pp. 459-466. http://www.elsevier.com/wps/find/journaldescription.cws_home/717426/description#description doi: 10.1016/j.jff.2017.07.010