J Appl Biomed 12:179-189, 2014 | DOI: 10.1016/j.jab.2014.01.003

Evaluation of antibacterial activity of hexanedioic acid isolated from Hermetia illucens larvae

Won Hyung Choia,*, MeiHua Jiangb
a Department of Microbiology, College of Medicine, Soon Chun Hyang University, Cheonan, Chungnam 330-721, Republic of Korea
b Department of Biomedical Science, Kyung Hee University School of Medicine, 26 Kyunghee-daero, Dongdaemun-gu, Seoul 130-701, Republic of Korea

Hermetia illucens larvae have been used in Europe and America as a medical resource and medicinal insect for the treatment of skin damage such as burns and wound healing. This study was carried out to evaluate the effect of a new substance causing antibacterial activity against various pathogenic bacteria, including methicillin-resistant Staphylococcus aureus (MRSA). The antibacterial activity of hexanedioic acid was determined using different antimicrobial indicators such as turbidometric assay, resazurin assay, and agar disk diffusion. Hexanedioic acid showed the selective-growth inhibitory effects against the growth and proliferation of Staphylococcus aureus, MRSA, Klebsiella pneumonia, and Shigella dysenteriae in a concentration dependent manner. The growth inhibitory zones of bacteria treated with 80 μg/ml of hexanedioic acid for 24 h were measured as 18.27 ± 0.18, 23.35 ± 0.15, 16.62 ± 0.18, and 12.96 ± 0.24 mm, respectively. The minimum inhibitory concentration (MIC) values of hexanedioic acid against the viability of these bacteria for 24 h were measured as 140.377, 137.369, 139.117, and 139.704 μg/ml, respectively. These results demonstrate that hexanedioic acid has antibacterial properties that effectively inhibit the growth/proliferation of pathogenic bacteria. Furthermore, this study suggests novel aspects for the utilization of hexanedioic acid as a medicinal substance.

Keywords: Antibacterial activity; Zone of bacterial growth inhibition; MIC; Shigella dysenteriae; MRSA

Received: November 16, 2013; Revised: December 30, 2013; Accepted: January 6, 2014; Published: July 1, 2014  Show citation

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Hyung Choi W, Jiang M. Evaluation of antibacterial activity of hexanedioic acid isolated from Hermetia illucens larvae. J Appl Biomed. 2014;12(3):179-189. doi: 10.1016/j.jab.2014.01.003.
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    References

    1. American Thoracic Society, Infectious Diseases Society of, America, 2005. Guidelines for the management of adults with hospital-acquired, ventilator-associated, and healthcare-associated pneumonia. Am. J. Respir. Crit. Care Med. 171, 388-416. Go to original source... Go to PubMed...
    2. Andersen, A.S., Sandvang, D., Schnorr, K.M., Kruse, T., Neve, S., Joergensen, B., Karlsmark, T., Krogfelt, K.A., 2010. A novel approach to the antimicrobial activity of maggot debridement therapy. J. Antimicrob. Chemother. 65, 1646-1654. Go to original source... Go to PubMed...
    3. Ang, E.S., Pavlos, N.J., Chai, L.Y., Qi, M., Cheng, T.S., Steer, J.H., Joyce, D.A., Zheng, M.H., Xu, J., 2009. Caffeic acid phenethyl ester, an active component of honeybee propolis attenuates osteoclastogenesis and bone resorption via the suppression of RANKL-induced NF-kappaB and NFAT activity. J. Cell. Physiol. 221, 642-649. Go to original source... Go to PubMed...
    4. Armstrong, D.G., Mossel, J., Short, B., Nixon, B.P., Knowles, E.A., Boulton, A.J., 2002. Maggot debridement therapy: a primer. J. Am. Podiatr. Med. Assoc. 92, 398-401. Go to original source... Go to PubMed...
    5. Bexfield, A., Nigam, Y., Thomas, S., Ratcliffe, N.A., 2004. Detection and partial characterisation of two antibacterial factors from the excretions/secretions of the medicinal maggot Lucilia sericata and their activity against methicillinresistant Staphylococcus aureus (MRSA). Microbes Infect. 6, 1297-1304. Go to original source... Go to PubMed...
    6. Bexfield, A., Bond, A.E., Roberts, E.C., Dudley, E., Nigam, Y., Thomas, S., Newton, R.P., Ratcliffe, N.A., 2008. The antibacterial activity against MRSA strains and other bacteria of a
    7. Blueman, D., Bousfield, C., 2012. The use of larval therapy to reduce the bacterial load in chronic wounds. J. Wound Care 21, 244-253. Go to original source... Go to PubMed...
    8. Blumberg, H.M., Burman, W.J., Chaisson, R.E., Daley, C.L., Etkind, S.C., Friedman, L.N., Fujiwara, P., Grzemska, M., Hopewell, P. C., Iseman, M.D., Jasmer, R.M., Koppaka, V., Menzies, R.I., O'Brien, R.J., Reves, R.R., Reichman, L.B., Simone, P.M., Starke, J.R., Vernon, A.A., American Thoracic Society, Centers for Disease Control and Prevention and the Infectious Diseases Society, 2003. American Thoracic Society/Centers for Disease Control and Prevention/Infectious Diseases Society of America: treatment of tuberculosis. Am. J. Respir. Crit. Care Med. 167, 603-662. Go to original source... Go to PubMed...
    9. Boyanova, L., Mitov, I., 2013. Antibiotic resistance rates in causative agents of infections in diabetic patients: rising concerns. Expert Rev. Anti Infect. Ther. 11, 411-420. Go to original source... Go to PubMed...
    10. Calvino, M.A., Szczupak, L., 2008. Spatial-specific action of serotonin within the leech midbody ganglion. J. Comp. Physiol. A: Neuroethol. Sens. Neural. Behav. Physiol. 194, 523-531. Go to original source... Go to PubMed...
    11. Calvori, C., Frontali, L., Leoni, L., Tecce, G., 1965. Effect of rifamycin on protein synthesis. Nature 207, 417-418. Go to original source... Go to PubMed...
    12. Chambers, L., Woodrow, S., Brown, A.P., Harris, P.D., Phillips, D., Hall, M., Church, J.C., Pritchard, D.I., 2003. Degradation of extracellular matrix components by defined proteinases from the greenbottle larva Lucilia sericata used for the clinical debridement of non-healing wounds. Br. J. Dermatol. 148, 14-23. Go to original source... Go to PubMed...
    13. Chan, D.C., Fong, D.H., Leung, J.Y., Patil, N.G., Leung, G.K., 2007. Maggot debridement therapy in chronic wound care. Hong Kong Med. J. 13, 382-386. Go to PubMed...
    14. Choi, W.H., Park, H.D., Baek, S.H., Chu, J.P., Kang, M.H., Mi, Y.J., 2008. Cannabidiol induces cytotoxicity and cell death via apoptotic pathway in cancer cell lines. Biomol. Ther. 16, 87-94. Go to original source...
    15. Choi, W.H., Yun, J.H., Chu, J.P., Chu, K.B., 2012. Antibacterial effect of extracts of Hermetia illucens (Diptera: Stratiomyidae) larvae against Gram-negative bacteria. Entomol. Res. 42, 219-226. Go to original source...
    16. Choi, W.H., Jiang, M.H., Chu, J.P., 2013. Antiparasitic effects of Zingiber officinale (Ginger) extract against Toxoplasma gondii. J. Appl. Biomed. 11, 15-26. Go to original source...
    17. Daeschlein, G., Mumcuoglu, K.Y., Assadian, O., Hoffmeister, B., Kramer, A., 2007. In vitro antibacterial activity of Lucilia sericata maggot secretions. Skin Pharmacol. Physiol. 20, 112-115. Go to original source... Go to PubMed...
    18. Diener, S., Zurbrügg, C., Tockner, K., 2009. Conversion of organic material by black soldier fly larvae: establishing optimal feeding rates. Waste Manage. Res. 27, 603-610. Go to original source... Go to PubMed...
    19. Ding, P.L., Liao, Z.X., Huang, H., Zhou, P., Chen, D.F., 2006. (+)-12alpha-Hydroxysophocarpine, a new quinolizidine alkaloid and related anti-HBV alkaloids from Sophora flavescens. Bioorg. Med. Chem. Lett. 16, 1231-1235. Go to original source... Go to PubMed...
    20. Drusano, G.L., Standiford, H.C., Plaisance, K., Forrest, A., Leslie, J., Caldwell, J., 1986. Absolute oral bioavailability of ciprofloxacin. Antimicrob. Agents Chemother. 30, 444-446. Go to original source... Go to PubMed...
    21. Ednie, L.M., Visalli, M.A., Jacobs, M.R., Appelbaum, P.C., 1996. Comparative activities of clarithromycin, erythromycin, and azithromycin against penicillin-susceptible and penicillinresistant pneumococci. Antimicrob. Agents Chemother. 40, 1950-1952. Go to original source... Go to PubMed...
    22. El-Gendy, A.M., Mansour, A., Weiner, M.A., Pimentel, G., Armstrong, A.W., Young, S.Y., Elsayed, N., Klena, J.D., 2012. Genetic diversity and antibiotic resistance in Shigella dysenteriae and Shigella boydii strains isolated from children aged
    23. Feng, G.J., Zhu, Z.G., Yu, C.L., Zhang, Q., Chen, N.N., Lei, L.S., Wu, S.G., 2007. Study of anticoagulant activity of ethanol extracts from leech in vitro. Zhong Yao Cai 30, 909-911. Go to PubMed...
    24. Feng, X., Cheng, G., Chen, S.Y., Yang, H., Huang, W., 2010. Evaluation of the burn healing properties of oil extraction from housefly larva in mice. J. Ethnopharmacol. 130, 586-592. Go to original source... Go to PubMed...
    25. Fernandez Guerrero, M.L., Alvarez, B., Manzarbeitia, F., Renedo, G., 2012. Infective endocarditis at autopsy: a review of pathologic manifestations and clinical correlates. Medicine (Baltimore). 91, 152-164. Go to original source... Go to PubMed...
    26. Gilead, L., Mumcuoglu, K.Y., Ingber, A., 2012. The use of maggot debridement therapy in the treatment of chronic wounds in hospitalised and ambulatory patients. J. Wound Care 21, 82- 85 78, 80. Go to original source... Go to PubMed...
    27. Glik, J., Kawecki, M., Gazdzik, T., Nowak, M., 2012. The impact of the types of microorganisms isolated from blood and wounds on the results of treatment in burn patients with sepsis. Pol. Przegl. Chir. 84, 6-16. Go to original source... Go to PubMed...
    28. Goto, H., Takeda, H., Kawai, S., Watanabe, T., Okazaki, M., Shimada, K., Nakano, K., Yokouchi, H., Ikemoto, H., Mori, T., Igari, J., Oguri, T., et al., 2006. Susceptibilities of bacteria isolated from patients with lower respiratory infectious diseases to antibiotics (2004). Jpn. J. Antibiot. 59, 323-354.
    29. Hamoud, R., Zimmermann, S., Reichling, J., Wink, M., 2013. Synergistic interactions in two-drug and three-drug combinations (thymol, EDTA and vancomycin) against multi drug resistant bacteria including E. coli. Phytomedicine, http://dx.doi.org/10.1016/j.phymed.2013.10.016. Go to original source... Go to PubMed...
    30. Harrison, L.M., Cherla, R.P., van den Hoogen, C., van Haaften, W. C., Lee, S.Y., Tesh, V.L., 2005. Comparative evaluation of apoptosis induced by Shiga toxin 1 and/or lipopolysaccharides in human monocytic and macrophagelike cells. Microb. Pathog. 38, 63-76. Go to original source... Go to PubMed...
    31. Hoffmann, J.A., Reichhart, J.M., Hetru, C., 1996. Innate immunity in higher insects. Curr. Opin. Immunol. 8, 8-13. Go to original source... Go to PubMed...
    32. Hou, L., Shi, Y., Zhai, P., Le, G., 2007. Antibacterial activity and in vitro anti-tumor activity of the extract of the larvae of the housefly (Musca domestica). J. Ethnopharmacol. 111, 227-231. Go to original source... Go to PubMed...
    33. Jaklic, D., Lapanje, A., Zupancic, K., Smrke, D., GundeCimerman, N., 2008. Selective antimicrobial activity of maggots against pathogenic bacteria. J. Med. Microbiol. 57, 617-625. Go to original source... Go to PubMed...
    34. Kawabata, T., Mitsui, H., Yokota, K., Ishino, K., Oguma, K., Sano, S., 2010. Induction of antibacterial activity in larvae of the blowfly Lucilia sericata by an infected environment. Med. Vet. Entomol. 24, 375-381. Go to original source... Go to PubMed...
    35. Kerridge, A., Lappin-Scott, H., Stevens, J.R., 2005. Antibacterial properties of larval secretions of the blowfly, Lucilia sericata. Med. Vet. Entomol. 19, 333-337. Go to original source... Go to PubMed...
    36. Li, Q., Zheng, L., Qiu, N., Cai, H., Tomberlin, J.K., Yu, Z., 2011. Bioconversion of dairy manure by black soldier fly (Diptera: Stratiomyidae) for biodiesel and sugar production. Waste Manage. 31, 1316-1320. Go to original source... Go to PubMed...
    37. Mandell, L.A., Wunderink, R.G., Anzueto, A., Bartlett, J.G., Campbell, G.D., Dean, N.C., Dowell, S.F., File Jr., T.M., Musher, D.M., Niederman, M.S., Torres, A., Whitney, C.G., Infectious Diseases Society of America; American Thoracic Society, 2007. Infectious Diseases Society of America/American Thoracic Society consensus guidelines on the management of community-acquired pneumonia in adults. Clin. Infect. Dis. 44 (Suppl. 2), S27-S72. Go to original source... Go to PubMed...
    38. Marineau, M.L., Herrington, M.T., Swenor, K.M., Eron, L.J., 2011. Maggot debridement therapy in the treatment of complex diabetic wounds. Hawaii Med. J. 70, 121-124. Go to PubMed...
    39. Mathur, P., Singh, S., 2013. Multidrug resistance in bacteria: a serious patient safety challenge for India. J. Lab. Physicians 5, 5-10. Go to original source... Go to PubMed...
    40. Mesquita, M.L., Desrivot, J., Bories, C., Fournet, A., Paula, J.E., Grellier, P., Espindola, L.S., 2005. Antileishmanial and trypanocidal activity of Brazilian Cerrado plants. Mem. Inst. Oswaldo Cruz 100, 783-787. Go to original source... Go to PubMed...
    41. Mumcuoglu, K.Y., Ingber, A., Gilead, L., Stessman, J., Friedmann, R., Schulman, H., Bichucher, H., Ioffe-Uspensky, I., Miller, J., Galun, R., Raz, I., 1999. Maggot therapy for the treatment of intractable wounds. Int. J. Dermatol. 38, 623-627. Go to original source... Go to PubMed...
    42. Mumcuoglu, K.Y., Miller, J., Mumcuoglu, M., Friger, M., Tarshis, M., 2001. Destruction of bacteria in the digestive tract of the maggot of Lucilia sericata (Diptera: Calliphoridae). J. Med. Entomol. 38, 162-166. Go to original source... Go to PubMed...
    43. Myers, H.M., Tomberlin, J.K., Lambert, B.D., Kattes, D., 2008. Development of black soldier fly (Diptera: Stratiomyidae) larvae fed dairy manure. Environ. Entomol. 37, 11-15. Go to original source... Go to PubMed...
    44. O'Mahony, R., Al-Khtheeri, H., Weerasekera, D., Fernando, N., Vaira, D., Holton, J., Basset, C., 2005. Bactericidal and anti-adhesive properties of culinary and medicinal plants against Helicobacter pylori. World J. Gastroenterol. 11, 7499-7507. Go to original source... Go to PubMed...
    45. Pemberton, R.W., 1999. Insects and other arthropods used as drugs in Korean traditional medicine. J. Ethnopharmacol. 65, 207-216. Go to original source... Go to PubMed...
    46. Prete, P.E., 1997. Growth effects of Phaenicia sericata larval extracts on fibroblasts: mechanism for wound healing by maggot therapy. Life Sci. 60, 505-510. Go to original source... Go to PubMed...
    47. Qiu, L., Chen, K.P., 2013. Anti-HBV agents derived from botanical origin. Fitoterapia 84, 140-157. Go to original source... Go to PubMed...
    48. Ratcliffe, N.A., Mello, C.B., Garcia, E.S., Butt, T.M., Azambuja, P., 2011. Insect natural products and processes: new treatments for human disease. Insect Biochem. Mol. Biol. 41, 747-769. Go to original source... Go to PubMed...
    49. Rifflet, A., Gavalda, S., Téné, N., Orivel, J., Leprince, J., Guilhaudis, L., Génin, E., Vétillard, A., Treilhou, M., 2012. Identification and characterization of a novel antimicrobial peptide from the venom of the ant Tetramorium bicarinatum. Peptides 38, 363-370. Go to original source... Go to PubMed...
    50. Ruddock, P.S., Charland, M., Ramirez, S., López, A., Neil Towers, G.H., Arnason, J.T., Liao, M., Dillon, J.A., 2011. Antimicrobial activity of flavonoids from Piper lanceaefolium and other Colombian medicinal plants against antibiotic susceptible and resistant strains of Neisseria gonorrhoeae. Sex. Transm. Dis. 38, 82-88. Go to original source... Go to PubMed...
    51. Sipetic-Grujicic, S., Glusac, S., Ratkov, I., Maksimovic, J., Ratkov, E., Rakocevic, B., 2010. Shigellosis-epidemiological situation in Montenegro in period 1996-2005. Med. Pregl. 63, 554-557. Go to original source... Go to PubMed...
    52. Staljanssens, D., Van Camp, J., Herregods, G., Dhaenens, M., Deforce, D., Van de Voorde, J., Smagghe, G., 2011. Antihypertensive effect of insect cells: in vitro and in vivo evaluation. Peptides 32, 526-530. Go to original source... Go to PubMed...
    53. Tesh, V.L., 2010. Induction of apoptosis by Shiga toxins. Future Microbiol. 5, 431-453. Go to original source... Go to PubMed...
    54. Thomas, S., Andrews, A.M., Hay, N.P., Bourgoise, S., 1999. The anti-microbial activity of maggot secretions: results of a preliminary study. J. Tissue Viability 9, 127-132. Go to original source... Go to PubMed...
    55. Vercruysse, L., Van Camp, J., Morel, N., Rouge, P., Herregods, G., Smagghe, G., 2010. Ala-Val-Phe and Val Phe: ACE inhibitory peptides derived from insect protein with antihypertensive activity in spontaneously hypertensive rats. Peptides 31, 482-488. Go to original source... Go to PubMed...
    56. Wang, J., Wang, S., Zhao, G., Wang, Z., Lineaweaver, W.C., Zhang, F., 2006. Treatment of infected wounds with maggot therapy after replantation. J. Reconstr. Microsurg. 22, 277-280. Go to original source... Go to PubMed...
    57. Washida, K., Yasui, N., Kaneda, D., Suzuki, S., Kato, T., 2011. A case of Staphylococcus aureus meningitis-associated quadriparesis with its successful treatment with adrenocorticosteroid. Rinsho Shinkeigaku 51, 203-206. Go to original source... Go to PubMed...
    58. Weinstein, M.J., Luedemann, G.M., Oden, E.M., Wagman, G.H., Rosselet, J.P., Marquez, J.A., Coniglio, C.T., Charney, W., Herzog, H.L., Black, J., Gentamicin, A., 1963. New antimicrobial complex from micromonospora. J. Med. Chem. 6, 463-464. Go to original source... Go to PubMed...
    59. Xu, X.L., Wang, C.M., Geng, D., Zhang, L., Zhang, L., Hu, B., 2010. Effects of centipede extracts on normal mouse and S180, H22 bearing mouse. Zhong Yao Cai 33, 499-503. Go to PubMed...
    60. Zhou, Y.Q., Han, L., Liu, Z.Q., Du, K.C., Li, K.Y., 2011. Effect of centipede extract on cervical tumor of mice and its mechanism. Zhong Yao Cai 34, 859-864. Go to PubMed...

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