Efficacy of different extracts of propolis against Salmonella enterica serovar Typhimurium: In vitro and in vivo study
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Abstract
Present study focussed on the antibacterial and antioxidative effect of honey bee propolis on typhoid causing bacteria i.e. Salmonella. Water, ethanol, methanol were used as solvents for making of extracts. Both Minimum Inhibitory Concentration (MIC) and Minimum Bactericidal Concentration (MBC) were calculated for all the three extracts. MIC of ethanolic extract of propolis was 160 mg/ml. It was 200 mg/ml for methanolic and 220mg/ml for wa-ter extracts respectively. Moreover, time kill analysis results confirmed that there was a significant reduction (p<0.05) in log count of bacteria when treated with ethanolic extraxt of propolis (3.98±0.15 log cfu/mL) and methanolic (4.66±0.05log cfu/mL) extract of propolis as compared to Salmonella control (7.72±0.03 log cfu/mL) in in vitro experiments. For the in vivo studies, BALB/c mice was used as an murine model of typhoid. Levels of different liver marker enzymes and antioxidants like Lipid peroxidation (LPO) and Reduced Glutathione (GSH) were observed in infected and all the treated groups. By comparing the results, it was concluded that ethanolic extract of propolis showed maximum antimicrobial activity as compare to the rest two. So the results of present study encourages the potential of ethanolic extract of propolis as an alternative treatment for typhoid and its use in combination with standard antibiotics can also be explored.
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Keywords
Antibacterial, Propolis, Salmonella, Typhoid
References
Al-Amoudi, W. (2015). Ameliorative role and antioxidant effect of propolis against hepatotoxicity of fenvalerate in albino rats. Journal of Cytology and Histology Research, 6: 303
Bankova, V., Christova, R., Popov, S., Marcucci, M. C., Tsvetkova, I. and Kujumgiev, A. (1999). Antibacterial activity of essential oils from Brazilian propolis. Fitoterpia, 70: 190-193
Bhavnani, S. M. and Ballow, C. H. (2000). New agents for Gram positive bacteria. Current Opinion in Microbiology, 3: 528-534
Chen, C. N., Weng, M.S., Wu, C. L. and Lin, J. K. (2004). Comparison of radical scavenging activity, cytotoxic effects and apoptosis induction in human melanoma cells by Taiwanese propolis from different sources. Evidence Based Complementary and Alternative Medicine, 1(2): 175-185.
Colledge, N. R., Waller, B. R. and Ralston, B. H. (2010). In: Davidson’s principles and practice of medicine. 21st Edn. Churchill Livingstone, Elsevier publs. pp. 334-335.
Cottica, S. M., Sawaya, A. C. H. F., Eberlin, M. N., Franco, S. L., Zeoula, L. M., Visentainer, J. V. (2011). Antioxidant activity and composition of propolis obtained by different methods of extraction. Journal of Brazilian Chemical Society, 22(5): 929-935
Cowan, M. M. (1999). Plant products as antimicrobial agents. Clinical Microbiology Review, 12: 564-582.
Cunha, I. B. S. , Sawayaa , A. C. H. F., Caetanob, F. M., Shimizua, M. T., Marcucci, M. C.. Drezza, F. T., Poviaa, G. S. and de O. Carvalh, P. (2004). Factors that Influence the yield and composition of Brazilian propolis extracts. Journal Brazilian Chemical Society, 15(6): 964-970
Daleprane, J. B. and Abdalla, D. S. (2013). Emerging roles of propolis: Antioxidant, cardioprotective and antiangiogenic actions. Evidence Based Complementary and Alternative Medicine, doi: http:..dx.doi.org/ 10.1155/2013/175135
Gajera, H. P., Patel, S. V. and Golakiya, B. A. (2005). Antioxidant properties of some therapeutically active medicinal plants—an overview. JMAPS., 27:91-100.
Grenho, L., Barros, J., Ferreira, C., Santos, V. R., Mointeiro, F. J., Ferraz, M. P. and Cortes, M. E. (2015). In vitro antimicrobial activity and biocompatibility of propolis containing nanohydroxypatite. Biomedical Materials, 18(2): 1-8
Harborne, J. B. (1973). Phytochemical Methods, 3th Edn, Chapman and Hall Ltd., London. pp 135-203.
Hasbun , J. Jr ., Osorio, R. and Hasbun, A. (2006). Hepatic dysfunction in typhoid fever during pregnancy. Infectious Diseases Obstetrics and Gynecology, 64828
Hasan, A. E. Z., Mangunwidjaja, D., Sunarti, T. C., Suparno, O. and Setiyono, A. (2014). Investigating the antioxidant and anticytotoxic activities of propolis collected from five regions of Indonesia and their abilities to induce apoptosis. Emirates Journal of Food Agriculture, 26(5): 390-398
Hepsen, I., Tilgen, F. and Er, H. (1996). Propolis: Medical properties and usage ophthalmic. Journal of Turgut Ozal Medical Center, 3: 386-391
Kalia, P., Kumar, N. R. and Harjai, K. (2013). Phytochemical screening and antibacterial activity of different extracts of propolis. International Journal of Pharmaceutical and Biological Research, 3(6): 219-222
Kalia, P., Kumar, N. R. and Harjai, K. (2014). Studies on the effect of ethanolic extract of propolis in BALB/c mice. Journal of Applied and Natural Sciences, 6(2): 638-643
Kalia, P., Kumar, N. R. and Harjai, K. (2015). The therapeutic potential of propolis against damage caused by Salmonella enterica serovar Typhimurium in mice liver: A biochemical and histological study. Archives of Biological Sciences, 67(3):807-16
Kalia, P., Kumar, N. R. and Harjai, K. (2016). Effect of propolis extract on the haematotoxicity and histological changes induced by Salmonella enterica serovar typhimurium in BALB/c mice. Archives of Biological Sciences; doi: 10.2298/ABS150902030K.
Kaur, R, Kalia, P, Kumar, N.R. and Harjai, K. (2013). Preliminary studies on different extracts of some honey bee products. Journal of Natural and Applied Sciences, 5(2):420-422.
Kaur, R, Kumar, N.R. and Harjai, K. (2014). Feeding bee pollen and bee bread to mice: Effect and antioxidant status. International Journal of Therapeutic Applications, 8:26-29
Kolankaya, D., Selmanoglu, G., Sorkun, K. and Salih, B. (2002). Protective effects of Turkish propolis on alcohol-induced serum lipid changes and liver injury in male rats. Food Chemistry, 78: 213–217
Kumar, N., Ahmad, M. K. K., Dang, R. and Husain, A. (2008). Antioxidant and antimicrobial activity of propolis from Tamil Nadu zone. Journal of Medicinal Plants Research, 2 (12): 361-364
Kumazawa, S., Hamasaka, T. and Nakayama, T. (2004). Antioxidant activity of propolis of various geographic origins. Food Chemistry, 84: 329-339
Luan, J., Wang, N. and Tian, L. (2000). Study on the pharmacologic effect of propolis. Zhong Yao Cai., 23(6): 346-348
Monroe, S. and Polk, R. (2000). Antimicrobial use and bacterial resistance. Current Opinion in Microbiology, 3: 496–501
Negi,B. S. and Dave, B. P. (2010). In vitro antimicrobial activity of Acacia catechu and its phytochemical analysis. Indian Journal of Microbiology, 50(4): 369-374
Newairy, A. A., Salama, A. F., Hussien, H. M. and Yousef, M. I. (2009). Propolis alleviates aluminium-induced lipid peroxidation and biochemical parameters in male rats. Food and Chemical Toxicology, 47:1093-1098
Ozkaya, H., Akcan, A. B., Aydemir, G., Aydinoz, S., Razia, Y., Gammon, S. T. and McKinney, J. (2012). Salmonella typhimurium infections in BALB/c mice: A comparison of tissue bioluminescence, tissue cultures and mice clinical scores. New Microbiologica, 35: 53-59
Ristivojevic, P., Dimic, I., Trifkovic, J., Beric, T. and Vovk, I. (2016). Antimicrobial activity of Serbian propolis evaluated by means of MIC, HPTLC, Bioautography and Chemometrics. Plos One, 11(6): e0157097.
Sahinler, N. (2000). Bee products and their importance in human health. Journal of Agricultural Faculty, 5:139-148
Saleh, E. M. (2012). Antioxidant effect of aqueous extract of propolis on hepatotoxicity induced by octylphenol in male rats. Acta Toxicology Argentina, 20: 68-81
Santos, F. A., Bastos, E., Maia, A., Uzeda, M., Carvalho, M., Farias, L. and Moreira, E. (2003). Brazilian propolis: physicochemical properties, plant origin and antibacterial activity on periodontopathogens. Phytotherapy
Research, 17:285-289
Santos, R. L., Zhang, S., Tsolis, R. M., Kingsley, R. A., Adams, L. G. and Baulmer, A. J. (2001). Animal models of Salmonella infections: enteritis versus typhoid fever. Microbes and Infection, 1335-1344
Sforcin, J. M. (2007). Propolis and the immune system: a review. Journal of Ethnopharmacology, 113: 1-14
Shinohara, R., Ohta, Y., Hayashi, T. and Ikeno, T. (2002). Evaluation of antilipid peroxidative action of propolis ethanol extract. Phytotherapy Research, 16: 340-347
Silici, S. and Kutluca, S. (2005). Chemical composition and antibacterial activity of propolis collected by three different races of honeybees in the same region. Journal of Ethnopharmacology, 99: 69-73
Tylkowski, B., Trusheva, B., Bankova, V., Giamberini, M., Peev, G. and Nikolova, A. (2010). Corrigendum to “Extraction of biologically active compounds from propolis and concentration of extract by nanofilteration. Journal of Membrane Science, 348:124-130
Virda-Martos, M., Ruiz-Navajas, Y., Fernandez-Lopez, J. and Perez-Alvarez , J.A. (2008). Functional properties of honey, propolis and royal jelly. Journal of Food Science, 73(9): 116-124.
Wagh, V. D. (2013). Propolis: A Wonder Bees Product and Its Pharmacological Potentials. Advances in Pharmacological Sciences, Article ID 308249, p: 11
Watanabe, M.A.E., Amarante, M.K., Conti, B.J. and Sforcin, J. M. (2011). Cytotoxic constituents of propolis inducing anticancer effects: A review. Journal of Pharmacy and Pharmacology, 63(11): 1378-1386
Yanpallewar , S. U., Sen, S., Tapas, S., Kumar, M., Raju, S. S. and Acharya , S.B. (2003). Effect of Azadirachta indica on paracetamol induced hepatic damage in albino rats. Phytomedicine, 10: 391- 396
Bankova, V., Christova, R., Popov, S., Marcucci, M. C., Tsvetkova, I. and Kujumgiev, A. (1999). Antibacterial activity of essential oils from Brazilian propolis. Fitoterpia, 70: 190-193
Bhavnani, S. M. and Ballow, C. H. (2000). New agents for Gram positive bacteria. Current Opinion in Microbiology, 3: 528-534
Chen, C. N., Weng, M.S., Wu, C. L. and Lin, J. K. (2004). Comparison of radical scavenging activity, cytotoxic effects and apoptosis induction in human melanoma cells by Taiwanese propolis from different sources. Evidence Based Complementary and Alternative Medicine, 1(2): 175-185.
Colledge, N. R., Waller, B. R. and Ralston, B. H. (2010). In: Davidson’s principles and practice of medicine. 21st Edn. Churchill Livingstone, Elsevier publs. pp. 334-335.
Cottica, S. M., Sawaya, A. C. H. F., Eberlin, M. N., Franco, S. L., Zeoula, L. M., Visentainer, J. V. (2011). Antioxidant activity and composition of propolis obtained by different methods of extraction. Journal of Brazilian Chemical Society, 22(5): 929-935
Cowan, M. M. (1999). Plant products as antimicrobial agents. Clinical Microbiology Review, 12: 564-582.
Cunha, I. B. S. , Sawayaa , A. C. H. F., Caetanob, F. M., Shimizua, M. T., Marcucci, M. C.. Drezza, F. T., Poviaa, G. S. and de O. Carvalh, P. (2004). Factors that Influence the yield and composition of Brazilian propolis extracts. Journal Brazilian Chemical Society, 15(6): 964-970
Daleprane, J. B. and Abdalla, D. S. (2013). Emerging roles of propolis: Antioxidant, cardioprotective and antiangiogenic actions. Evidence Based Complementary and Alternative Medicine, doi: http:..dx.doi.org/ 10.1155/2013/175135
Gajera, H. P., Patel, S. V. and Golakiya, B. A. (2005). Antioxidant properties of some therapeutically active medicinal plants—an overview. JMAPS., 27:91-100.
Grenho, L., Barros, J., Ferreira, C., Santos, V. R., Mointeiro, F. J., Ferraz, M. P. and Cortes, M. E. (2015). In vitro antimicrobial activity and biocompatibility of propolis containing nanohydroxypatite. Biomedical Materials, 18(2): 1-8
Harborne, J. B. (1973). Phytochemical Methods, 3th Edn, Chapman and Hall Ltd., London. pp 135-203.
Hasbun , J. Jr ., Osorio, R. and Hasbun, A. (2006). Hepatic dysfunction in typhoid fever during pregnancy. Infectious Diseases Obstetrics and Gynecology, 64828
Hasan, A. E. Z., Mangunwidjaja, D., Sunarti, T. C., Suparno, O. and Setiyono, A. (2014). Investigating the antioxidant and anticytotoxic activities of propolis collected from five regions of Indonesia and their abilities to induce apoptosis. Emirates Journal of Food Agriculture, 26(5): 390-398
Hepsen, I., Tilgen, F. and Er, H. (1996). Propolis: Medical properties and usage ophthalmic. Journal of Turgut Ozal Medical Center, 3: 386-391
Kalia, P., Kumar, N. R. and Harjai, K. (2013). Phytochemical screening and antibacterial activity of different extracts of propolis. International Journal of Pharmaceutical and Biological Research, 3(6): 219-222
Kalia, P., Kumar, N. R. and Harjai, K. (2014). Studies on the effect of ethanolic extract of propolis in BALB/c mice. Journal of Applied and Natural Sciences, 6(2): 638-643
Kalia, P., Kumar, N. R. and Harjai, K. (2015). The therapeutic potential of propolis against damage caused by Salmonella enterica serovar Typhimurium in mice liver: A biochemical and histological study. Archives of Biological Sciences, 67(3):807-16
Kalia, P., Kumar, N. R. and Harjai, K. (2016). Effect of propolis extract on the haematotoxicity and histological changes induced by Salmonella enterica serovar typhimurium in BALB/c mice. Archives of Biological Sciences; doi: 10.2298/ABS150902030K.
Kaur, R, Kalia, P, Kumar, N.R. and Harjai, K. (2013). Preliminary studies on different extracts of some honey bee products. Journal of Natural and Applied Sciences, 5(2):420-422.
Kaur, R, Kumar, N.R. and Harjai, K. (2014). Feeding bee pollen and bee bread to mice: Effect and antioxidant status. International Journal of Therapeutic Applications, 8:26-29
Kolankaya, D., Selmanoglu, G., Sorkun, K. and Salih, B. (2002). Protective effects of Turkish propolis on alcohol-induced serum lipid changes and liver injury in male rats. Food Chemistry, 78: 213–217
Kumar, N., Ahmad, M. K. K., Dang, R. and Husain, A. (2008). Antioxidant and antimicrobial activity of propolis from Tamil Nadu zone. Journal of Medicinal Plants Research, 2 (12): 361-364
Kumazawa, S., Hamasaka, T. and Nakayama, T. (2004). Antioxidant activity of propolis of various geographic origins. Food Chemistry, 84: 329-339
Luan, J., Wang, N. and Tian, L. (2000). Study on the pharmacologic effect of propolis. Zhong Yao Cai., 23(6): 346-348
Monroe, S. and Polk, R. (2000). Antimicrobial use and bacterial resistance. Current Opinion in Microbiology, 3: 496–501
Negi,B. S. and Dave, B. P. (2010). In vitro antimicrobial activity of Acacia catechu and its phytochemical analysis. Indian Journal of Microbiology, 50(4): 369-374
Newairy, A. A., Salama, A. F., Hussien, H. M. and Yousef, M. I. (2009). Propolis alleviates aluminium-induced lipid peroxidation and biochemical parameters in male rats. Food and Chemical Toxicology, 47:1093-1098
Ozkaya, H., Akcan, A. B., Aydemir, G., Aydinoz, S., Razia, Y., Gammon, S. T. and McKinney, J. (2012). Salmonella typhimurium infections in BALB/c mice: A comparison of tissue bioluminescence, tissue cultures and mice clinical scores. New Microbiologica, 35: 53-59
Ristivojevic, P., Dimic, I., Trifkovic, J., Beric, T. and Vovk, I. (2016). Antimicrobial activity of Serbian propolis evaluated by means of MIC, HPTLC, Bioautography and Chemometrics. Plos One, 11(6): e0157097.
Sahinler, N. (2000). Bee products and their importance in human health. Journal of Agricultural Faculty, 5:139-148
Saleh, E. M. (2012). Antioxidant effect of aqueous extract of propolis on hepatotoxicity induced by octylphenol in male rats. Acta Toxicology Argentina, 20: 68-81
Santos, F. A., Bastos, E., Maia, A., Uzeda, M., Carvalho, M., Farias, L. and Moreira, E. (2003). Brazilian propolis: physicochemical properties, plant origin and antibacterial activity on periodontopathogens. Phytotherapy
Research, 17:285-289
Santos, R. L., Zhang, S., Tsolis, R. M., Kingsley, R. A., Adams, L. G. and Baulmer, A. J. (2001). Animal models of Salmonella infections: enteritis versus typhoid fever. Microbes and Infection, 1335-1344
Sforcin, J. M. (2007). Propolis and the immune system: a review. Journal of Ethnopharmacology, 113: 1-14
Shinohara, R., Ohta, Y., Hayashi, T. and Ikeno, T. (2002). Evaluation of antilipid peroxidative action of propolis ethanol extract. Phytotherapy Research, 16: 340-347
Silici, S. and Kutluca, S. (2005). Chemical composition and antibacterial activity of propolis collected by three different races of honeybees in the same region. Journal of Ethnopharmacology, 99: 69-73
Tylkowski, B., Trusheva, B., Bankova, V., Giamberini, M., Peev, G. and Nikolova, A. (2010). Corrigendum to “Extraction of biologically active compounds from propolis and concentration of extract by nanofilteration. Journal of Membrane Science, 348:124-130
Virda-Martos, M., Ruiz-Navajas, Y., Fernandez-Lopez, J. and Perez-Alvarez , J.A. (2008). Functional properties of honey, propolis and royal jelly. Journal of Food Science, 73(9): 116-124.
Wagh, V. D. (2013). Propolis: A Wonder Bees Product and Its Pharmacological Potentials. Advances in Pharmacological Sciences, Article ID 308249, p: 11
Watanabe, M.A.E., Amarante, M.K., Conti, B.J. and Sforcin, J. M. (2011). Cytotoxic constituents of propolis inducing anticancer effects: A review. Journal of Pharmacy and Pharmacology, 63(11): 1378-1386
Yanpallewar , S. U., Sen, S., Tapas, S., Kumar, M., Raju, S. S. and Acharya , S.B. (2003). Effect of Azadirachta indica on paracetamol induced hepatic damage in albino rats. Phytomedicine, 10: 391- 396
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Efficacy of different extracts of propolis against Salmonella enterica serovar Typhimurium: In vitro and in vivo study. (2017). Journal of Applied and Natural Science, 9(1), 144-149. https://doi.org/10.31018/jans.v9i1.1162
