Abstract
The objective of this study was to evaluate the antibacterial effect of sophorolipid in combination with lactic acid against relevant bacteria isolated from the poultry industry. Staphylococcus aureus, Listeria monocytogenes, Salmonella enterica, and Escherichia coli were isolated from chicken meat and antibacterial tests with sophorolipid and lactic acid were performed. Checkerboard, time-kill, and scanning electron microscopy analyses were used to confirm the antibacterial action and the combined effects. Although no inhibitory effects were observed for E. coli and Salmonella, these compounds presented antibacterial activity against L. monocytogenes and S. aureus. Additionally, sophorolipid and lactic acid were not cytotoxic at the concentrations used in the tests. The combination of sophorolipid and lactic acid resulted in an additive interaction, reducing the concentration of the active compounds needed for effectiveness against S. aureus and L. monocytogenes, to 50% and 75%, respectively. These findings lead to the possibility of develo** a new, sustainable, and natural antimicrobial solution that is considered noncytotoxic and has wide applicability in the poultry industry to reduce substantial losses in this sector.
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References
Venkitanarayanan K, Thakur S, Ricke SC (2019) Food safety in poultry meat production. Springer International Publishing, Griffith
World Health Organization (2015) WHO estimates of the global burden of foodborne diseases: Foodborne Disease Burden Epidemiology. Reference Group 2007–2015. World Health Organization, Geneva
Rouger A, Tresse O, Zagorec M (2017) Bacterial contaminants of poultry meat : sources, species and dynamics. Microorganisms 5:E50. https://doi.org/10.3390/microorganisms5030050
Zhang X, Ashby RD, Solaiman DKY, Liu Y, Fan X (2017) Antimicrobial activity and inactivation mechanism of lactonic and free acid sophorolipids against Escherichia coli O157:H7. Biocatal Agric Biotechnol 11:176–182. https://doi.org/10.1016/j.bcab.2017.07.002
Mahami T, Togby-Tetteh W, Kottoh DI, Amoakoah-Twum L, Gasu E, Annan SNY, Larbi D, Adjei I, Adu-Gyamfi A (2019) Microbial food safety risk to humans associated with poultry feed: the role of irradiation. Int J Food Sci 19:6915736. https://doi.org/10.1155/2019/6915736
Chen SH, Fegan N, Kocharunchitt C, Bowman JP, Duffy LL (2020) Effect of peracetic acid on Campylobacter in food matrices mimicking commercial poultry processing. Food Control 113:107185. https://doi.org/10.1016/j.foodcont.2020.107185
Kataria J, Morey A (2020) Antimicrobial interventions in poultry processing to improve shelf life and safety of poultry meat: a review with special attention to Salmonella spp. J Food Qual Hazards Control 7:52–59. https://doi.org/10.18502/jfqhc.7.2.2884
Moye ZD, Das CR, Tokman JI, Fanelli B, Karathia H, Hasan NA, Marek PJ, Senecal AG, Sulakvelidze A (2020) Treatment of fresh produce with a Salmonella-targeted bacteriophage cocktail is compatible with chlorine or peracetic acid and more consistently preserves the microbial community on produce. J Food Saf 40:e12763. https://doi.org/10.1111/jfs.12763
Micciche AC, Feye KM, Rubinelli PM, Wages JA, Knueven CJ, Ricke SC (2018) The implementation and food safety issues associated with poultry processing reuse water for conventional poultry production systems in the United States. Front Sustain Food Syst 2:70. https://doi.org/10.3389/fsufs.2018.00070
Aidara-Kane A, Angulo FJ, Conly J, Minato Y, Silbergeld EK, Mcewen SA, Collignon PJ (2018) World Health Organization (WHO) guidelines on use of medically important antimicrobials in food-producing animals. Antimicrob Resist Infect Control 7:1–8. https://doi.org/10.1186/s13756-017-0294-9
Zhang X, Ashby R, Solaiman D, Uknalis J, Fan X (2016) Inactivation of Salmonella spp. and Listeria spp. by palmitic, stearic, and oleic acid sophorolipids and thiamine dilauryl sulfate. Front Microbiol 7:2076. https://doi.org/10.3389/fmicb.2016.02076
Valotteau C, Banat IM, Mitchell CA, Lydon H, Marchant R, Babonneau F, Pradier CM, Baccile N, Humblot V (2017) Antibacterial properties of sophorolipid-modified gold surfaces against Gram positive and Gram negative pathogens. Colloids Surf B 157:325–334. https://doi.org/10.1016/j.colsurfb.2017.05.072
Olanya OM, Ukuku DO, Solaiman DKY, Ashby RD, Niemira BA, Mukhopadhyay S (2018) Reduction in Listeria monocytogenes, Salmonella enterica and Escherichia coli O157:H7 in vitro and on tomato by sophorolipid and sanitiser as affected by temperature and storage time. Int J Food Sci Technol 53:1303–1315. https://doi.org/10.1111/ijfs.13711
Silveira VAI, Queiroz CAU, Celligoi MAPC (2018) Antimicrobial applications of sophorolipid from Candida bombicola: a promising alternative to conventional drugs. J Appl Biol Biotechnol 6:87–90. https://doi.org/10.7324/JABB.2018.60614
Naughton PJ, Marchant R, Naughton V, Banat IM (2019) Microbial biosurfactants: current trends and applications in agricultural and biomedical industries. J Appl Microbiol 127:12–28. https://doi.org/10.1111/jam.14243
Chen J, Liu X, Fu S, An Z, Feng Y, Wang R, Ji P (2020) Effects of sophorolipids on fungal and oomycete pathogens in relation to pH solubility. J Appl Microbiol 128:1754–1763. https://doi.org/10.1111/jam.14594
Mani-López E, García HS, López-Malo A (2012) Organic acids as antimicrobials to control Salmonella in meat and poultry products. Food Res Int 45:713–721. https://doi.org/10.1016/j.foodres.2011.04.043
Dubal ZB, Paturkar AM, Waskar VS, Zende RJ, Latha C, Rawool DB, Kadam MM (2004) Effect of food grade organic acids on inoculated S. aureus, L. monocytogenes, E. coli and S. Typhimurium in sheep/goat meat stored at refrigeration temperature. Meat Sci 66:817–821. https://doi.org/10.1016/j.meatsci.2003.08.004
Stanojević-Nikolić S, Dimić G, Mojović L, Pe** J, Djukić-Vuković A, Kocić-Tanackov S (2016) Antimicrobial activity of lactic acid against pathogen and spoilage microorganisms. J Food Process Pres 40:990–998. https://doi.org/10.1111/jfpp.12679
Silveira VAI, Nishio EK, Queiroz CAU, Amador IR, Kobayashi RKT, Caretta TO, Macedo F, Celligoi MAPC (2019) Production and antimicrobial activity of sophorolipid against Clostridium perfringens and Campylobacter jejuni and their additive interaction with lactic acid. Biocatal Agric Biotechnol 21:101287. https://doi.org/10.1016/j.bcab.2019.101287
Joshi-Navare K, Prabhune A (2013) A biosurfactant-sophorolipid acts in synergy with antibiotics to enhance their efficiency. BioMed Res Int 512495:1–8. https://doi.org/10.1155/2013/512495
Sen S, Borah SN, Bora A, Deka S (2017) Production, characterization, and antifungal activity of a biosurfactant produced by Rhodotorula babjevae YS3. Microb Cell Fact 16:95. https://doi.org/10.1186/s12934-017-0711-z
Elshikh M, Moya-Ramírez I, Moens H, Roelants S, Soetaert W, Marchant R, Banat IM (2017) Rhamnolipids and lactonic sophorolipids: natural antimicrobial surfactants for oral hygiene. J Appl Microbiol 123:1111–1123. https://doi.org/10.1111/jam.13550
International Organization for Standardization (2017) Microbiology of the food chain- Horizontal method for the detection and enumeration of Listeria monocytogenes and other Listeria spp.-Part 1: detection method; International Standard; ISO 1129–1, 2017, International Organization for Standardization, Geneva
International Organization for Standardization (2017) Microbiology of the food chain and animal feeding stuffs – Horizontal method for the detection, enumeration and seroty** of Salmonella - Part 1: detection of Salmonella spp.; International Standard; ISO 6579, 2017, International Organization for Standardization, Geneva
International Organization for Standardization (2001) Microbiology of food and animal feeding stuffs - Horizontal method for the enumeration of beta-glucuronidase-positive Escherichia coli - Part 2: colony-count technique at 44 degrees C using 5-bromo-4-chloro-3-indolyl beta-D-glucuronide; International Standard; ISO 16649–2, 2001, International Organization for Standardization, Geneva
International Organization for Standardization (2003) Microbiology of food and animal feeding stuffs - Horizontal method for the enumeration of coagulase-positive Staphylococci (Staphylococcus aureus and other species). Part 3: detection and MPN technique for low numbers; International Standard; ISO 6888–3, 2003, International Organization for Standardization, Geneva
Fontoura ICC, Saikawa GIA, Silveira VAI, Pan NC, Amador IR, Baldo C, Rocha SPD, Celligoi MAPC (2020) Antibacterial activity of sophorolipids from Candida bombicola against human pathogens. Braz Arch Biol Technol 63:e20180568. https://doi.org/10.1590/1678-4324-2020180568
Clinical and Laboratory Standards Institute CLSI (2012) Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically (M07-A9); approved standard — ninth edition. CLSI, Wayne. https://doi.org/10.4103/0976-237X.91790
Traub WH, Kleber I (1975) In vitro additive effect of polymyxin B and rifampin against Serratia marcescens. Antimicrob Agents Chemother 7:874–876. https://doi.org/10.1128/aac.7.6.874
Chin NX, Weitzman I, Della-Latta P (1997) In vitro activity of fluvastatin, a cholesterol-lowering agent, and synergy with fluconazole and itraconazole against Candida species and Cryptococcus neoformans. Antimicrob Agents Chemother 41:850–852
National Committee for Clinical Laboratory Standards NCCLS (1999) Methods for determining bactericidal activity of antimicrobial agents; approved guideline (M26-A). CLSI, Wayne (19(18))
Scandorieiro S, Camargo LC, Lancheros CAC, Yamada-Ogatta SF, Nakamura CV, Oliveira AG, Andrade CGTJ, Duran N, Nakazato G, Kobayashi RKT (2016) Synergistic and additive effect of oregano essential oil and biological silver nanoparticles against multidrug-resistant bacterial strains. Front Microbiol 7:760. https://doi.org/10.3389/fmicb.2016.00760
Aquino I, Tsuboy MS, Marcarini JC, Mantovani MS, Perazzo FF, Maistro EL (2013) Genotoxic evaluation of the antimalarial drugs artemisinin and artesunate in human HepG2 cells and effects on CASP3 and SOD1 gene expressions. Genet Mol Res 12:2517–2527. https://doi.org/10.4238/2013.July.24.6
Solaiman DKY, Ashby RD, Uknalis J (2017) Characterization of growth inhibition of oral bacteria by sophorolipid using a microplate-format assay. J Microbiol Methods 136:21–29. https://doi.org/10.1016/j.mimet.2017.02.012
Kim K, Dalsoo Y, Youngbum K, Baekseok L, Doonhoon S, Eun-Ki K (2002) Characteristics of sophorolipid as an antimicrobial agent. J Microbiol Biotechnol 12:235–241
Dengle-Pulate V, Chandorkar P, Bhagwat S, Prabhune AA (2013) Antimicrobial and SEM studies of sophorolipids synthesized using lauryl alcohol. J Surfactants Deterg 17:543–552. https://doi.org/10.1007/s11743-013-1495-8
Pontes C, Alves M, Santos C, Ribeiro MH, Gonçalves L, Bettencourt AF, Ribeiro IAC (2016) Can sophorolipids prevent biofilm formation on silicone catheter tubes? Int J Pharm 513:697–708. https://doi.org/10.1016/j.ijpharm.2016.09.074
Valotteau C, Calers C, Casale S, Berton J, Stevens CV, Babonneau F, Pradier CM, Humblot V, Baccile N (2015) Biocidal properties of a glycosylated surface: sophorolipids on Au(111). ACS Appl Mater Interfaces 7:18086–18095. https://doi.org/10.1021/acsami.5b05090
Diaz de Rienzo MA, Stevenson PS, Marchant R, Banat IM (2015) Antibacterial properties of biosurfactants against selected Gram positive and negative bacteria. FEMS Microbiol Lett 363:ID fnv224. https://doi.org/10.1093/femsle/fnv224
Hoa NLH, Loan LQ, Eun-Ki K, Ha TT, Duy ND, Khanh HQ, Dung NH (2017) Production and characterization of sophorolipids produced by Candida bombicola using sugarcane molasses and coconut oil. Asia Pac J Sci Technol 22. https://doi.org/10.14456/apst.2017.11
Van Bogaert INA, Saerens K, De Muynck C, Develter D, Soetaert W, Vandamme EJ (2007) Microbial production and application of sophorolipids. Appl Microbiol Biotechnol 76:23–34. https://doi.org/10.1007/s00253-007-0988-7
Dubey P, Selvaraj K, Prabhune A (2013) Sophorolipids: in self assembly and nanomaterial synthesis. World J Pharm Pharm Sci 2:1107–1133
Ricke S (2003) Perspectives on the use of organic acids and short chain fatty acids as antimicrobials. Poultry Sci 82:632–639. https://doi.org/10.1093/ps/82.4.632
Mohamed HMH, Abdel-Naeem HHS (2018) Enhancing the bactericidal efficacy of lactic acid against Salmonella typhimurium attached to chicken skin by sodium dodecyl sulphate addition. LWT - Food Sci Technol 87:464–469. https://doi.org/10.1016/j.lwt.2017.09.022
Alakomi HL, Skyttä E, Saarela M, Mattila-Sandholm T, Latva-Kala K, Helander IM (2000) Lactic acid permeabilizes Gram-negative bacteria by disrupting the outer membrane. Appl Environ Microb 66:2001–2005. https://doi.org/10.1128/aem.66.5.2001-2005.2000
Chen J, Song X, Zhang H, Qu Y (2006) Production, structure elucidation and anticancer properties of sophorolipid from Wickerhamiella domercqiae. Enzyme Microb Technol 39:501–506. https://doi.org/10.1016/j.enzmictec.2005.12.022
Rashad MM, Nooman MU, Ali MM, Mahmoud AE (2014) Production, characterization and anticancer activity of Candida bombicola sophorolipids by means of solid state fermentation of sunflower oil cake and soybean oil. Grasas Aceites 65:1–11. https://doi.org/10.3989/gya.098413
Dubey P, Raina P, Prabhune A, Kaul-Ghanekar R (2016) Cetyl alcohol and oleic acid sophorolipids exhibit anticancer activity. Int J Pharm Pharm Sci 8:399–402
Li H, Guo W, Ma X, Li J, Song X (2017) In vitro and in vivo anticancer activity of sophorolipids to human cervical cancer. Appl Biochem Biotechnol 181:1372–1387. https://doi.org/10.1007/s12010-016-2290-6
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This work was supported by the National Council for Scientific and Technological Development (CNPq) and Coordination for the Improvement of Higher Education Personnel (CAPES).
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Victória Akemi Itakura Silveira: conceptualization, formal analysis, investigation, methodology, visualization, writing—original draft preparation, writing—review & editing. Renata Katsuko Takayama Kobayashi: conceptualization, methodology, resources, writing—review & editing. Admilton Gonçalves de Oliveira Junior: conceptualization, methodology, resources, writing—review & editing. Mario Sérgio Mantovani: conceptualization, methodology, resources, writing—review & editing. Gerson Nakazato: conceptualization, methodology, resources, writing—review & editing. Maria Antonia Pedrine Colabone Celligoi: conceptualization, funding acquisition, methodology, project administration, resources, supervision, writing—review & editing.
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Silveira, V.A.I., Kobayashi, R.K.T., de Oliveira Junior, A.G. et al. Antimicrobial effects of sophorolipid in combination with lactic acid against poultry-relevant isolates. Braz J Microbiol 52, 1769–1778 (2021). https://doi.org/10.1007/s42770-021-00545-9
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DOI: https://doi.org/10.1007/s42770-021-00545-9