Use of cocoa ethanolic extract for treatment of Staphylococcal infection in rabbit-skin model
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Table 1. Inhibition zone of test substance in bacteria-seeded agar plate
Table 2. Length of wound opening with respect to bacteria infection
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Apr 30, 2016
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Abstract
In septic condition, the skin normal flora Staphylococcal spp. may trigger local and sistemic skin infection. In this study antibacterial activity of cocoa ethanolic extract (CEE) against Staphylococcus aureus and Staphylococcus epidermidis infections was observed in vitro and in vivo. Ethanolic extract from unfermented cocoa beans was prepared as solution in the in vitro testing, while for in vivo testing the extract was prepared as cream. Agar well diffusion assay showed that CEE ranging from 7.8 mg/mL to 1000 mg/mL demonstrated inhibitory activity against growth of either S. aureus and S. epidermidis. Inhibitory activity of CEE was in concentration dependent manner, and was less potential than either cephalexin 4 x 10 -3 mg/mL or cefotaxime 8 x 10 -3 mg/mL. Linear regression of CEE concentration plotted against inhibition zone values ha dpredicted the minimum inhibitory concentrations (MIC) of CEE towards S. aureus and S. epidermidis were at 341.9 mg/mL and 359.7 mg/mL, respectively. Topical application of cream containing CEE at several concentrations (2%, 4%, and 8%) demonstrated healing properties towards incision wound infected with S. aureus and S. epidermidis cultures in rabbit-skin model. CEE cream promoted wound contraction and higher recovery rate than of base cream (negative control) but lower than mupirocin 2% cream. In S. aureus and S. epidermidis infected wound models, CEE cream 8% improved wound recovery to 72.7% and 86.1% from original rates of 23.5% and 34.7% (base cream application). Catechin and procyanidis are suggested playing roles in alleviation of wound inflammation and stimulation of extracellular matrix accumulation, thus accelerate the wound healing process. This study proposes utilization of cocoa bean as source of active ingredient for skin care products.
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Tunjung-Sari, A., Wahyudi, T., Chusna Mufida, D., Tamarizki, M., Perwitahati, D., Kartika Syamsuddin, I., & Jati, M. (2016). Use of cocoa ethanolic extract for treatment of Staphylococcal infection in rabbit-skin model. Pelita Perkebunan (a Coffee and Cocoa Research Journal), 32(1), 34-42. https://doi.org/10.22302/iccri.jur.pelitaperkebunan.v32i1.214
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References
Al-Habib, A., Al-Saleh, E., Safer, A.-M., & Afzal, M. (2010). Bactericidal effect of grape seed extract on methicillin-resistant Staphylococcus aureus (MRSA). The Journal of Toxicological Sciences, 35(3), 357-364.
Ali, N. H., Faizi, S., & Kazmi, S. U. (2011). Antibacterial activity in spices and local medicinal plants against clinical isolates of Karachi, Pakistan. Pharmaceutical Biology, 49(8), 833-839.
Bandele, O. J., Clawson, S. J., & Osheroff, N. (2008). Dietary polyphenols as topoisomerase II poisons: B ring and C ring substituents determine the mechanism of enzyme-mediated DNA cleavage enhancement. Chemical research in toxicology, 21(6), 1253-1260.
Bao, P., Kodra, A., Tomic-Canic, M., Golinko, M. S., Ehrlich, H. P., & Brem, H. (2009). The role of vascular endothelial growth factor in wound healing. Journal of Surgical Research, 153(2), 347-358.
Bell, S. M., Pham, J. N., & Nguyen, T. T. (2011). Antibiotic susceptibility testing by the CDS method: a manual for medical and veterinary laboratories 2011 (pp. 97).
Bernal, P., Lemaire, S., Pinho, M. G., Mobashery, S., Hinds, J., & Taylor, P. W. (2010). Insertion of epicatechin gallate into the cytoplasmic membrane of methicillin-resistant Staphylococcus aureus disrupts penicillin-binding protein (PBP) 2A-mediated β-lactam resistance by delocalizing PBP2. Journal of Biological Chemistry, 285(31), 24055-24065.
Coutinho, H. D., Costa, J. G., Lima, E. O., Falcão-Silva, V. S., & Siqueira, J. P. (2009). Herbal therapy associated with antibiotic therapy: potentiation of the antibiotic activity against methicillin–resistant Staphylococcus aureus by Turnera ulmifolia L. BMC Complementary and Alternative Medicine, 9(1), 13.
Crozier, S. J., Preston, A. G., Hurst, J. W., Payne, M. J., Mann, J., Hainly, L., & Miller, D. L. (2011). Cacao seeds are a “Super Fruit": A comparative analysis of various fruit powders and products. Chemistry Central Journal, 5(5), 1-6.
Demidova-Rice, T. N., Hamblin, M. R., & Herman, I. M. (2012). Acute and impaired wound healing: pathophysiology and current methods for drug delivery, part 1: normal and chronic wounds: biology, causes, and approaches to care. Advances in Skin and Wound Care, 25(7), 304-314.
Dillinger, T. L., Barriga, P., Escárcega, S., Jimenez, M., Lowe, D. S., & Grivetti, L. E. (2000). Food of the gods: cure for humanity? a cultural history of the medicinal and ritual use of chocolate. Journal of Nutrition, 130(8), 2057-2072.
Dryden, M. S. (2009). Skin and soft tissue infection: microbiology and epidemiology. International Journal of Antimicrobial Agents, 34(1), 2-7.
García-Lafuente, A., Guillamón, E., Villares, A., Rostagno, M. A., & Martínez, J. A. (2009). Flavonoids as anti-inflammatory agents: implications in cancer and cardiovascular disease. Inflammation Research, 58(9), 537-552.
Gasser, P., Lati, E., Peno‐Mazzarino, L., Bouzoud, D., Allegaert, L., & Bernaert, H. (2008). Cocoa polyphenols and their influence on parameters involved in ex vivo skin restructuring. International Journal of Cosmetic Science, 30(5), 339-345.
Hall-Stoodley, L., Costerton, J. W., & Stoodley, P. (2004). Bacterial biofilms: from the natural environment to infectious diseases. Nature Reviews Microbiology, 2(2), 95-108.
Hay, R. J., Johns, N. E., Williams, H. C., Bolliger, I. W., Delavalle, B., Margolis, D. J., . . . Naghavi, M. (2013). The Global Burden of Skin Disease in 2010: An Analysis of the Prevalence and Impact of Skin Conditions. Journal of Investigative Dermatology. http://dx.doi.org/10.1038/jid.2013.446 doi:10.1038/jid.2013.446
He, L., Mu, C., Shi, J., Zhang, Q., Shi, B., & Lin, W. (2011). Modification of collagen with a natural cross-linker, procyanidin. International Journal of Biological Macromolecules, 48(2), 354-359.
Johnson, B. J., Delehanty, J. B., Lin, B., & Ligler, F. S. (2008). Immobilized proanthocyanidins for the capture of bacterial lipopolysaccharides. Analytical Chemistry, 80(6), 2113-2117.
Kapoor, M., Howard, R., Hall, I., & Appleton, I. (2004). Effects of epicatechin gallate on wound healing and scar formation in a full thickness incisional wound healing model in rats. The American Journal of Pathology, 165(1), 299-307.
Lee, K. W., Kim, Y. J., Lee, H. J., & Lee, C. Y. (2003). Cocoa has more phenolic phytochemicals and a higher antioxidant capacity than teas and red wine. Journal of Agricultural and Food Chemistry, 51(25), 7292-7295.
Li, K., Diao, Y., Zhang, H., Wang, S., Zhang, Z., Yu, B., . . . Yang, H. (2011). Tannin extracts from immature fruits of Terminalia chebula Fructus Retz. promote cutaneous wound healing in rats. BMC Complementary and Alternative Medicine, 11(1), 86.
Lippi, D. (2009). Chocolate and medicine: Dangerous liaisons? Nutrition, 25(11), 1100-1103.
Luciano-Montalvo, C., Boulogne, I., & Gavillán-Suárez, J. (2013). A screening for antimicrobial activities of Caribbean herbal remedies. BMC Complementary and Alternative Medicine, 13(1), 126.
Madhan, B., Krishnamoorthy, G., Rao, J. R., & Nair, B. U. (2007). Role of green tea polyphenols in the inhibition of collagenolytic activity by collagenase. International Journal of Biological Macromolecules, 41(1), 16-22.
Matsumoto, Y., Kaihatsu, K., Nishino, K., Ogawa, M., Kato, N., & Yamaguchi, A. (2012). Antibacterial and antifungal activities of new acylated derivatives of epigallocatechin gallate. Frontiers in Microbiology, 3(53), 1-10.
Miller, K. B., Hurst, W. J., Payne, M. J., Stuart, D. A., Apgar, J., Sweigart, D. S., & Ou, B. (2008). Impact of alkalization on the antioxidant and flavanol content of commercial cocoa powders. Journal of Agricultural and Food Chemistry, 56(18), 8527-8533.
Misnawi, Selamat, J., Bakar, J., & Saari, N. (2002). Oxidation of polyphenols in unfermented and partly fermented cocoa beans by cocoa polyphenol oxidase and tyrosinase. Journal of the Science of Food and Agriculture, 82(5), 559-566.
Muller, M., Trocme, C., Lardy, B., Morel, F., Halimi, S., & Benhamou, P. (2008). Matrix metalloproteinases and diabetic foot ulcers: the ratio of MMP‐1 to TIMP‐1 is a predictor of wound healing. Diabetic Medicine, 25(4), 419-426.
Mwaura, B., Mahendran, B., Hynes, N., Defreitas, D., Avalos, G., Adegbola, T., . . . Sultan, S. (2006). The impact of differential expression of extracellular matrix metalloproteinase inducer, matrix metalloproteinase-2, tissue inhibitor of matrix metalloproteinase-2 and PDGF-AA on the chronicity of venous leg ulcers. European Journal of Vascular and Endovascular Surgery, 31(3), 306-310.
Naveed, R., Hussain, I., Tawab, A., Tariq, M., Rahman, M., Hameed, S., . . . Iqbal, M. (2013). Antimicrobial activity of the bioactive components of essential oils from Pakistani spices against Salmonella and other multi-drug resistant bacteria. BMC Complementary and Alternative Medicine, 13(1), 265.
Neukam, K., Stahl, W., Tronnier, H., Sies, H., & Heinrich, U. (2007). Consumption of flavanol-rich cocoa acutely increases microcirculation in human skin. European Journal of Nutrition, 46(1), 53-56.
Oh, J., Conlan, S., Polley, E. C., Segre, J. A., & Kong, H. H. (2012). Shifts in human skin and nares microbiota of healthy children and adults. Genome Medicine, 4(10), 77.
Otto, M. (2009). Staphylococcus epidermidis—the'accidental'pathogen. Nature Reviews Microbiology, 7(8), 555-567.
Otto, M. (2012). Molecular basis of Staphylococcus epidermidis infections. Paper presented at the Seminars in immunopathology.
Puupponen-Pimiä, R., Nohynek, L., Alakomi, H.-L., & Oksman-Caldentey, K.-M. (2005). Bioactive berry compounds: novel tools against human pathogens. Applied Microbiology and Biotechnology, 67(1), 8-18.
Radulovic, N., Blagojevic, P., Stojanovic-Radic, Z., & Stojanovic, N. (2013). Antimicrobial plant metabolites: structural diversity and mechanism of action. Current Medicinal Chemistry, 20(7), 932-952.
Schierle, C. F., De la Garza, M., Mustoe, T. A., & Galiano, R. D. (2009). Staphylococcal biofilms impair wound healing by delaying reepithelialization in a murine cutaneous wound model. Wound Repair and Regeneration, 17(3), 354-359.
Singh, R., Ray, P., Das, A., & Sharma, M. (2010). Penetration of antibiotics through staphylococcus aureus and staphylococcus epidermidis biofilms. Journal of Antimicrobial Chemotherapy, 65(9), 1955-1958.
Suriyanarayanan, B., Shanmugam, K., & Santhosh, R. S. (2013). Synthetic quercetin inhibits mycobacterial growth possibly by interacting with DNA gyrase. Romanian Biotechnological Letters, 18(5), 8587-8593.
Tang, H., Covington, A. D., & Hancock, R. (2003). Structure–activity relationships in the hydrophobic interactions of polyphenols with cellulose and collagen. Biopolymers, 70(3), 403-413.
Zhai, W.-y., Jia, C.-p., Zhao, H., & Xu, Y.-s. (2011). Procyanidins inhibit tumor angiogenesis by crosslinking extracellular matrix. Chinese Journal of Cancer Research, 23(2), 99-106.
Zhang, Q., Kelly, A. P., Wang, L., French, S. W., Tang, X., Duong, H. S., . . . Le, A. D. (2006). Green tea extract and (−)-epigallocatechin-3-gallate inhibit mast cell-stimulated type I collagen expression in keloid fibroblasts via blocking PI-3K/Akt signaling pathways. Journal of Investigative Dermatology, 126(12), 2607-2613.
Ali, N. H., Faizi, S., & Kazmi, S. U. (2011). Antibacterial activity in spices and local medicinal plants against clinical isolates of Karachi, Pakistan. Pharmaceutical Biology, 49(8), 833-839.
Bandele, O. J., Clawson, S. J., & Osheroff, N. (2008). Dietary polyphenols as topoisomerase II poisons: B ring and C ring substituents determine the mechanism of enzyme-mediated DNA cleavage enhancement. Chemical research in toxicology, 21(6), 1253-1260.
Bao, P., Kodra, A., Tomic-Canic, M., Golinko, M. S., Ehrlich, H. P., & Brem, H. (2009). The role of vascular endothelial growth factor in wound healing. Journal of Surgical Research, 153(2), 347-358.
Bell, S. M., Pham, J. N., & Nguyen, T. T. (2011). Antibiotic susceptibility testing by the CDS method: a manual for medical and veterinary laboratories 2011 (pp. 97).
Bernal, P., Lemaire, S., Pinho, M. G., Mobashery, S., Hinds, J., & Taylor, P. W. (2010). Insertion of epicatechin gallate into the cytoplasmic membrane of methicillin-resistant Staphylococcus aureus disrupts penicillin-binding protein (PBP) 2A-mediated β-lactam resistance by delocalizing PBP2. Journal of Biological Chemistry, 285(31), 24055-24065.
Coutinho, H. D., Costa, J. G., Lima, E. O., Falcão-Silva, V. S., & Siqueira, J. P. (2009). Herbal therapy associated with antibiotic therapy: potentiation of the antibiotic activity against methicillin–resistant Staphylococcus aureus by Turnera ulmifolia L. BMC Complementary and Alternative Medicine, 9(1), 13.
Crozier, S. J., Preston, A. G., Hurst, J. W., Payne, M. J., Mann, J., Hainly, L., & Miller, D. L. (2011). Cacao seeds are a “Super Fruit": A comparative analysis of various fruit powders and products. Chemistry Central Journal, 5(5), 1-6.
Demidova-Rice, T. N., Hamblin, M. R., & Herman, I. M. (2012). Acute and impaired wound healing: pathophysiology and current methods for drug delivery, part 1: normal and chronic wounds: biology, causes, and approaches to care. Advances in Skin and Wound Care, 25(7), 304-314.
Dillinger, T. L., Barriga, P., Escárcega, S., Jimenez, M., Lowe, D. S., & Grivetti, L. E. (2000). Food of the gods: cure for humanity? a cultural history of the medicinal and ritual use of chocolate. Journal of Nutrition, 130(8), 2057-2072.
Dryden, M. S. (2009). Skin and soft tissue infection: microbiology and epidemiology. International Journal of Antimicrobial Agents, 34(1), 2-7.
García-Lafuente, A., Guillamón, E., Villares, A., Rostagno, M. A., & Martínez, J. A. (2009). Flavonoids as anti-inflammatory agents: implications in cancer and cardiovascular disease. Inflammation Research, 58(9), 537-552.
Gasser, P., Lati, E., Peno‐Mazzarino, L., Bouzoud, D., Allegaert, L., & Bernaert, H. (2008). Cocoa polyphenols and their influence on parameters involved in ex vivo skin restructuring. International Journal of Cosmetic Science, 30(5), 339-345.
Hall-Stoodley, L., Costerton, J. W., & Stoodley, P. (2004). Bacterial biofilms: from the natural environment to infectious diseases. Nature Reviews Microbiology, 2(2), 95-108.
Hay, R. J., Johns, N. E., Williams, H. C., Bolliger, I. W., Delavalle, B., Margolis, D. J., . . . Naghavi, M. (2013). The Global Burden of Skin Disease in 2010: An Analysis of the Prevalence and Impact of Skin Conditions. Journal of Investigative Dermatology. http://dx.doi.org/10.1038/jid.2013.446 doi:10.1038/jid.2013.446
He, L., Mu, C., Shi, J., Zhang, Q., Shi, B., & Lin, W. (2011). Modification of collagen with a natural cross-linker, procyanidin. International Journal of Biological Macromolecules, 48(2), 354-359.
Johnson, B. J., Delehanty, J. B., Lin, B., & Ligler, F. S. (2008). Immobilized proanthocyanidins for the capture of bacterial lipopolysaccharides. Analytical Chemistry, 80(6), 2113-2117.
Kapoor, M., Howard, R., Hall, I., & Appleton, I. (2004). Effects of epicatechin gallate on wound healing and scar formation in a full thickness incisional wound healing model in rats. The American Journal of Pathology, 165(1), 299-307.
Lee, K. W., Kim, Y. J., Lee, H. J., & Lee, C. Y. (2003). Cocoa has more phenolic phytochemicals and a higher antioxidant capacity than teas and red wine. Journal of Agricultural and Food Chemistry, 51(25), 7292-7295.
Li, K., Diao, Y., Zhang, H., Wang, S., Zhang, Z., Yu, B., . . . Yang, H. (2011). Tannin extracts from immature fruits of Terminalia chebula Fructus Retz. promote cutaneous wound healing in rats. BMC Complementary and Alternative Medicine, 11(1), 86.
Lippi, D. (2009). Chocolate and medicine: Dangerous liaisons? Nutrition, 25(11), 1100-1103.
Luciano-Montalvo, C., Boulogne, I., & Gavillán-Suárez, J. (2013). A screening for antimicrobial activities of Caribbean herbal remedies. BMC Complementary and Alternative Medicine, 13(1), 126.
Madhan, B., Krishnamoorthy, G., Rao, J. R., & Nair, B. U. (2007). Role of green tea polyphenols in the inhibition of collagenolytic activity by collagenase. International Journal of Biological Macromolecules, 41(1), 16-22.
Matsumoto, Y., Kaihatsu, K., Nishino, K., Ogawa, M., Kato, N., & Yamaguchi, A. (2012). Antibacterial and antifungal activities of new acylated derivatives of epigallocatechin gallate. Frontiers in Microbiology, 3(53), 1-10.
Miller, K. B., Hurst, W. J., Payne, M. J., Stuart, D. A., Apgar, J., Sweigart, D. S., & Ou, B. (2008). Impact of alkalization on the antioxidant and flavanol content of commercial cocoa powders. Journal of Agricultural and Food Chemistry, 56(18), 8527-8533.
Misnawi, Selamat, J., Bakar, J., & Saari, N. (2002). Oxidation of polyphenols in unfermented and partly fermented cocoa beans by cocoa polyphenol oxidase and tyrosinase. Journal of the Science of Food and Agriculture, 82(5), 559-566.
Muller, M., Trocme, C., Lardy, B., Morel, F., Halimi, S., & Benhamou, P. (2008). Matrix metalloproteinases and diabetic foot ulcers: the ratio of MMP‐1 to TIMP‐1 is a predictor of wound healing. Diabetic Medicine, 25(4), 419-426.
Mwaura, B., Mahendran, B., Hynes, N., Defreitas, D., Avalos, G., Adegbola, T., . . . Sultan, S. (2006). The impact of differential expression of extracellular matrix metalloproteinase inducer, matrix metalloproteinase-2, tissue inhibitor of matrix metalloproteinase-2 and PDGF-AA on the chronicity of venous leg ulcers. European Journal of Vascular and Endovascular Surgery, 31(3), 306-310.
Naveed, R., Hussain, I., Tawab, A., Tariq, M., Rahman, M., Hameed, S., . . . Iqbal, M. (2013). Antimicrobial activity of the bioactive components of essential oils from Pakistani spices against Salmonella and other multi-drug resistant bacteria. BMC Complementary and Alternative Medicine, 13(1), 265.
Neukam, K., Stahl, W., Tronnier, H., Sies, H., & Heinrich, U. (2007). Consumption of flavanol-rich cocoa acutely increases microcirculation in human skin. European Journal of Nutrition, 46(1), 53-56.
Oh, J., Conlan, S., Polley, E. C., Segre, J. A., & Kong, H. H. (2012). Shifts in human skin and nares microbiota of healthy children and adults. Genome Medicine, 4(10), 77.
Otto, M. (2009). Staphylococcus epidermidis—the'accidental'pathogen. Nature Reviews Microbiology, 7(8), 555-567.
Otto, M. (2012). Molecular basis of Staphylococcus epidermidis infections. Paper presented at the Seminars in immunopathology.
Puupponen-Pimiä, R., Nohynek, L., Alakomi, H.-L., & Oksman-Caldentey, K.-M. (2005). Bioactive berry compounds: novel tools against human pathogens. Applied Microbiology and Biotechnology, 67(1), 8-18.
Radulovic, N., Blagojevic, P., Stojanovic-Radic, Z., & Stojanovic, N. (2013). Antimicrobial plant metabolites: structural diversity and mechanism of action. Current Medicinal Chemistry, 20(7), 932-952.
Schierle, C. F., De la Garza, M., Mustoe, T. A., & Galiano, R. D. (2009). Staphylococcal biofilms impair wound healing by delaying reepithelialization in a murine cutaneous wound model. Wound Repair and Regeneration, 17(3), 354-359.
Singh, R., Ray, P., Das, A., & Sharma, M. (2010). Penetration of antibiotics through staphylococcus aureus and staphylococcus epidermidis biofilms. Journal of Antimicrobial Chemotherapy, 65(9), 1955-1958.
Suriyanarayanan, B., Shanmugam, K., & Santhosh, R. S. (2013). Synthetic quercetin inhibits mycobacterial growth possibly by interacting with DNA gyrase. Romanian Biotechnological Letters, 18(5), 8587-8593.
Tang, H., Covington, A. D., & Hancock, R. (2003). Structure–activity relationships in the hydrophobic interactions of polyphenols with cellulose and collagen. Biopolymers, 70(3), 403-413.
Zhai, W.-y., Jia, C.-p., Zhao, H., & Xu, Y.-s. (2011). Procyanidins inhibit tumor angiogenesis by crosslinking extracellular matrix. Chinese Journal of Cancer Research, 23(2), 99-106.
Zhang, Q., Kelly, A. P., Wang, L., French, S. W., Tang, X., Duong, H. S., . . . Le, A. D. (2006). Green tea extract and (−)-epigallocatechin-3-gallate inhibit mast cell-stimulated type I collagen expression in keloid fibroblasts via blocking PI-3K/Akt signaling pathways. Journal of Investigative Dermatology, 126(12), 2607-2613.
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