Bioassay Directed Identification of Royal Jelly’s Active Compounds against the Growth of Bacteria Capable of Infecting Cutaneous Wounds

Mariana C. Garcia, Mónica S. Finola, Juan M. Marioli

.
Departamento de Química, Universidad Nacional de Río Cuarto, Río Cuarto, Argentina.

DOI: 10.4236/aim.2013.32022                

Abstract

Antibiotic-resistant bacteria continue to be of major health concern world-wide. Thus, it is of great interest to study the biological properties and determine active compounds in natural products likely to be used as new health remedies. Therefore, the main objective of this work is to test the antibacterial activity of royal jelly samples, defatted royal jelly samples and their ethyl ether extracts against bacteria capable of infecting cutaneous wounds in humans and animals, and to recognize major bioactive compounds by using bioassay directed identification. The microorganisms used in the study were Staphylococcus aureus (including Methicillin-resistant and sensitive strains), Staphylococcus epidermidis, Micrococcus luteus, Streptococcus uberis, Enterococcus faecalis, Pseudomonas aeruginosa, Escherichia coli, and Klebsiella pneumoniae. The activity of royal jelly samples to inhibit bacterial growth was assessed by using well-difussion tests. Direct bioautography was used to identify bioactivity, and uv-visible spectroscopy and gas chromatography-mass spectrometry were used to identify bioactive compounds. Overall, royal jelly samples showed higher growth inhibition activity against Gram positive bacteria as compared to Gram negative bacteria. The growth of bacterial strains belonging to the Enterococcus and Streptococcus genders was less affected by the presence of royal jelly than bacterial strains of the Staphylococcus gender did. Compounds with antibacterial activity were found in the ethyl ether extract of royal jelly samples. 10-hydroxy-2-decenoic acid was the major component identified in the purified fraction obtained by bioassay guided fractionation of the ethyl ether extract. In conclusion, bioactivity of royal jelly samples is mainly due to their 10-hydroxy-2-decenoic acid content.

Keywords

Royal Jelly; Antibacterial Activity; 10-Hydroxy-2-decenoic Acid; Bioautography

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	C. Valgas, S. Machado de Souza, E. F. A. Smania and A. Smania Jr., “Screening Methods to Determine Antibacterial Activity of Natural Products,” Brazilian Journal of Microbiology, Vol. 38, No. 2, 2007, pp. 369-380. doi:10.1590/S1517-83822007000200034
[2]	G. Reid, “Probiotic Agents to Protect the Urogenital Tract against Infection,” American Journal of Clinical Nutrition, Vol. 73, No. 2, 2001, pp. 437S-443S.
[3]	S. Petti, G. Tarsitani and A. Simonetti D’Arca, “Antibacterial Activity of Yoghurt against Viridans Streptococci in Vitro,” Archives of Oral Biology, Vol. 53, No. 10, 2008, pp. 985-990. doi:10.1016/j.archoralbio.2008.04.009
[4]	A. T. Serra, A. A. Matias, A. V. M. Nunes, M. C. Leitao, D. Brito, R. Bronze, et al., “In Vitro Evaluation of Olive- and Grape-Based Natural Extracts as Potential Preservatives for Food,” Innovative Food Science and Emerging Technologies, Vol. 9, No. 3, 2008, pp. 311-319. doi:10.1016/j.ifset.2007.07.011
[5]	Y. H. Yau, B. Ho, N. S. Tan, M. L. Ng and J. L. Ding, “High Therapeutic Index of Factor C Sushi Peptides: Potent Antimicrobials against Pseudomonas aeruginosa,” Antimicrobial Agents and Chemotherapy, Vol. 45, No. 10, 2001, pp. 2820-2825. doi:10.1128/AAC.45.10.2820-2825.2001
[6]	M. T. Chomnawang, S. Surassmo, K. Wongsariya, N. Bunyapraphatsara, “Antibacterial Activity of Thai Medicinal Plants against Methicillin-Resistant Staphylococcus aureus,” Fitoterapia, Vol. 80, No. 2, 2009, pp. 102-104. doi:10.1016/j.fitote.2008.10.007
[7]	M. J. González and J. M. Marioli, “Antibacterial Activity of Water Extracts and Essential Oils of Various Aromatic Plants against Paenibacillus larvae, the Causative Agent of American Foulbrood,” Journal of Invertebrate Pathology, Vol. 104, No. 3, 2010, pp. 209-213. doi:10.1016/j.jip.2010.04.005
[8]	K. Leite Rodrigues, L. R. Gaudino Caputo, J. C. Tavares Carvalho, J. Evangelista and J. M. Schneedorf, “Antimicrobial and Healing Activity of Kefir and Kefiran Extract,” International Journal of Antimicrobial Agents, Vol. 25, No. 5, 2005, pp. 404-408.
[9]	P. Molan, “Not All Honeys Are the Same for Wound Healing,” European Tissue Repair Society Bulletin, Vol. 9, No. 1, 2002, pp. 5-6.
[10]	C. Basualdo, V. Sgroy, M. S. Finola and J. M. Marioli, “Comparison of the Antibacterial Activity of Honey from Different Provenance against Bacteria Usually Isolated from Skin Wounds,” Veterinary Microbiology, Vol. 124, No. 3-4, 2007, pp. 375-381. doi:10.1016/j.vetmic.2007.04.039
[11]	A. C. H. F. Sawaya, K. S. Souza, M. C. Marcucci, I. B. S. Cunha and M. T. Shimizu, “Analysis of the Composition of Brazilian Propolis Extracts by Chromatography and Evaluation of Their in Vitro Activity against Gram-Positive Bacteria,” Brazilian Journal of Microbiology, Vol. 35, No. 1-2, 2004, pp. 104-109. doi:10.1590/S1517-83822004000100017
[12]	S. Eshraghi, “An Evaluation of the Potent Inhibitory Effects of Royal Jelly Fractions against Streptomyces Bacteria,” Pakistan Journal of Medical Sciences, Vol. 21, No. 1, 2005, pp. 63-68.
[13]	M. C. Garcia, M. S. Finola and J. M. Marioli, “Antibacterial Activity of Royal Jelly against Bacteria Capable of Infecting Cutaneous Wounds,” Journal of ApiProducts and ApiMedical Science, Vol. 2, No. 3, 2010, pp. 93-99. doi:10.3896/IBRA.4.02.3.02
[14]	B. Schmidt, D. M. Ribnicky, A. Poulev, S. Logendra, W. T. Cefalu and I. Raskin, “A Natural History of Botanical Therapeutics,” Metabolism Clinical and Experimental, Vol. 57, No. 1, 2008, pp. S3-S9. doi:10.1016/j.metabol.2008.03.001
[15]	A. G. Sabatini, G. L. Marcazzan, M. F. Caboni, S. Bogdanov and L. B. de Almeida-Muradian, “Quality and Standarisation of Royal Jelly,” Journal of ApiProducts and ApiMedical Science, Vol. 1, No. 1, 2009, pp. 16-21. doi:10.3896/IBRA.4.01.1.04
[16]	T. Nagai and R. Inoue, “Preparation and the Functional Properties of Water Extract and Alkaline Extract of Royal Jelly,” Food Chemistry, Vol. 84, No. 2, 2004, pp. 181-186. doi:10.1016/S0308-8146(03)00198-5
[17]	E. Melliou and I. Chinou, “Chemistry and Bioactivity of Royal Jelly from Greece,” Journal of Agricultural and Food Chemistry, Vol. 53, No. 23, 2005, pp. 8987-8992. doi:10.1021/jf051550p
[18]	M. E. Jones, J. A. Karlowsky, D. C. Draghi, C. Thornsberry, D. F. Sahm and D. Nathwani, “Epidemiology and Antibiotic Susceptibility of Bacteria Causing Skin and Soft Tissue Infections in the USA and Europe: A Guide to Appropriate Antimicrobial Therapy,” International Journal of Antimicrobial Agents, Vol. 22, No. 4, 2003, pp. 406-419. doi:10.1016/S0924-8579(03)00154-7
[19]	L. Halcón and K. Milkus, “Staphylococcus aureus and Wounds: A Review of Tea Tree Oil as a Promising Antimicrobial,” American Journal of Infection Control, Vol. 32, No. 7, 2004, pp. 402-408. doi:10.1016/j.ajic.2003.12.008
[20]	C. Vuong and M. Otto, “Staphylococcus Epidermidis Infections,” Microbes and Infection, Vol. 4, No. 4, 2002, pp. 481-489. doi:10.1016/S1286-4579(02)01563-0
[21]	S. Nasser, A. Mabrouk and A. Maher, “Colonization of Burn Wounds in Ain Shams University Burn Unit,” Burns, Vol. 29, No. 3, 2003, pp. 229-233. doi:10.1016/S0305-4179(02)00285-1
[22]	U. Altoparlak, F. Aktas, D. Celebi, Z. Ozkurt and M. N. Akcay, “Prevalence of Metallo-β-Lactamase among Pseudomonas aeruginosa and Actinobacter baumanii Isolated from Burn Wounds and in Vitro Activities of Antibiotic Combinations against These Isolates,” Burns, Vol. 31, No. 6, 2005, pp. 707-710. doi:10.1016/j.burns.2005.02.017
[23]	A. A. Código, X. Capítulo and A. Alimentos, “Art. 784,” 2010. http://www.anmat.gov.ar/alimentos/normativas_alimentos_caa.asp
[24]	R Development Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. 2010. http://www.R-project.org
[25]	A. Stocker, “Isolation and Characterization of Substances from Royal Jelly,” 2003.
[26]	C. S. McCleskey and R. M. Melampy, “Bactericidal Properties of Royal Jelly of Honeybee,” Journal of Economic Entomology, Vol. 32, No. 4, 1939, pp. 581-587.
[27]	N. Sauerwald, J. Polster, E. Bengsch, L. Niessen and R. Vogel, “Combined Antibacterial and Antifungal Properties of Water Soluble Fractions of Royal Jelly,” Advances in Food Science, Vol. 20, No. 1-2, 1998, pp. 46-52.
[28]	G. Lercker, P. Capella, L. S. Conte, F. Ruini and G. Giordani, “Components of Royal Jelly: I. Identification of Organic Acids,” Lipids, Vol. 16, No. 12, 1981, pp. 912-919. doi:10.1007/BF02534997