Research Article
Determination of time dependent antibacterial activities of curcumin, carvacrol and styrax liquidus on Salmonella Enteritidis
Abstract
Salmonella Enteritidis is amongst the most common causes of foodborne salmonellosis. Multi-drug resistant Salmonella strains has been associated with treatment failures. Plant-derived phytochemicals may be an alternative to antibiotics in combating these bacteria. The purpose of this study is to investigate the antibacterial activity of curcumin, carvacrol and styrax liquidus on S. Enteritidis and S. Enteritidis PT4. Minimum inhibitory concentration (MIC) values of these substances were detected at 1.5, 3, 7.5 and 24 h by broth microdilution method to evaluate their time-dependent antibacterial activities. The findings of the present study showed that MIC values of carvacrol, curcumin and styrax liquids for both S. Enteritidis and S. Enteritidis PT4 were 125.0 μg/mL, 132.5 μg/mL, 31.3 mg/mL for 24 h, respectively. Also, a time-dependent change was observed in the MIC values of curcumin. Carvacrol, curcumin and styrax liquidus can be used to provide antimicrobial effect on S. Enteritidis and S. Enteritidis PT4 in food applications, taking into account the MIC values and contact times.
Supporting Institution
This work was supported by TUBITAK (The Scientific and Technological Research Council of Türkiye) in the framework of the Career Development Program (3501) (Grant number: 119O672).
Project Number
119O672
References
- Adamczak A, Ożarowski M, Karpiński TM (2020): Curcumin, a Natural Antimicrobial Agent with Strain-Specific Activity. Pharmaceuticals, 13, 153.
- Akram M, Shahab-Uddin AA, Usmanghani K, et al (2010): Curcuma longa and curcumin: a review article. Rom J Biol Plant Biol, 55, 65-70.
- Arslan MB, Şahin HT (2016): Unutulan Bir Orman Ürünü Kaynağı: Anadolu Sığla Ağacı (Liquidambar Orientalis Miller). Bartın Orman Fakültesi Dergisi, 18, 103-117.
- Bintsis T (2017): Foodborne pathogens. AIMS Microbiol, 3, 529-563.
- Božik M, Hovorková P, Klouček P (2018): Antibacterial Effect of Carvacrol and Coconut Oil on Selected Pathogenic Bacteria. Scientia Agriculturae Bohemica, 49, 46-52.
- Cabarkapa I, Colovic R, Duragic O, et al (2019): Anti-biofilm activities of essential oils rich in carvacrol and thymol against Salmonella Enteritidis. Biofouling, 35, 361-375.
- Chouhan S, Sharma K, Guleria S (2017): Antimicrobial Activity of Some Essential Oils—Present Status and Future Perspectives. Medicines, 4, 58.
- Clinical and Laboratory Sandards Institute (2018): Performance Standards for Antimicrobial Susceptibility Testing. 26th ed Pennsylvania, USA M100S.
- Demirtas A, Ozturk H, Sudagidan M, et al (2019): Effects of commercial aldehydes from green leaf volatiles (green odour) on rumen microbial population and fermentation profile in an artificial rumen (Rusitec). Anaerobe, 55, 83-92.
- Eng S-K, Pusparajah P, Ab Mutalib N-S, et al (2015): Salmonella: a review on pathogenesis, epidemiology and antibiotic resistance. Frontiers in Life Science, 8, 284-293.
- Engel JB, Heckler C, Tondo EC, et al (2017): Antimicrobial activity of free and liposome-encapsulated thymol and carvacrol against Salmonella and Staphylococcus aureus adhered to stainless steel. Int J Food Microbiol, 252, 18-23.
- Erdem Y, Gisho H, Ekrem S, et al (1993): Traditional medicine in Turkey IV. Folk medicine in the Mediterranean subdivision. J Ethnopharmacol, 39, 31-38.
- Gong J, Xu M, Zhu C, et al (2013): Antimicrobial resistance, presence of integrons and biofilm formation of Salmonella Pullorum isolates from Eastern China (1962-2010). Avian Pathol, 42, 290-294.
- Gunes H, Gulen D, Mutlu R, et al (2016): Antibacterial effects of curcumin: An in vitro minimum inhibitory concentration study. Toxicol Ind Health, 32, 246-250.
- Gupta PD, Birdi TJ (2017): Development of botanicals to combat antibiotic resistance. J Ayurveda Integr Med, 8, 266-275.
- Gurbuz I, Yesilada E, Demirci B, et al (2013): Characterization of volatiles and anti-ulcerogenic effect of Turkish sweetgum balsam (Styrax liquidus). J Ethnopharmacol, 148, 332-336.
- Honda G, Yeşilada E, Tabata M, et al (1996): Traditional medicine in Turkey VI. Folk medicine in West Anatolia: Afyon, Kütahya, Denizli, Muğla, Aydin provinces. J Ethnopharmacol, 53, 75-87.
- Howard ZR, O'Bryan CA, Crandall PG, et al (2012): Salmonella Enteritidis in shell eggs: Current issues and prospects for control. Food Res Int, 45, 755-764.
- Iramiot JS, Kajumbula H, Bazira J, et al (2020): Antimicrobial resistance at the human-animal interface in the Pastoralist Communities of Kasese District, South Western Uganda. Sci Rep, 10, 14737.
- İstek A (1995): Sığla Yağı (Storax)’nın Kimyasal Bileşenleri. Master Thesis. Graduate Institute of Natural and Applied Sciences, Trabzon.
- Kang MS, Oh JS, Kang IC, et al (2008): Inhibitory effect of methyl gallate and gallic acid on oral bacteria. J Microbiol, 46, 744-750.
- Karagoz A, Tutun H, Altintas L, et al (2020): Molecular typing of drug-resistant Mycobacterium tuberculosis strains from Turkey. J Glob Antimicrob Resist, 23, 130-134.
- Keyvan E, Tutun H (2019): Effects of carvacrol on Staphylococcus aureus isolated from bulk tank milk. Med Weter, 75, 238-241.
- Khameneh B, Iranshahy M, Soheili V, et al (2019): Review on plant antimicrobials: a mechanistic viewpoint. Antimicrob Resist Infect Control, 8, 118.
- Kharat M, Du Z, Zhang G, et al (2017): Physical and Chemical Stability of Curcumin in Aqueous Solutions and Emulsions: Impact of pH, Temperature, and Molecular Environment. J Agric Food Chem, 65, 1525-1532.
- Kocaadam B, Sanlier N (2017): Curcumin, an active component of turmeric (Curcuma longa), and its effects on health. Crit Rev Food Sci Nutr, 57, 2889-2895.
- Kuang X, Hao H, Dai M, et al (2015): Serotypes and antimicrobial susceptibility of Salmonella spp. isolated from farm animals in China. Front Microbiol, 6, 602-602.
- Marathe SA, Ray S, Chakravortty D (2010): Curcumin Increases the Pathogenicity of Salmonella enterica Serovar Typhimurium in Murine Model. PLoS One, 5, e11511.
- Marchese A, Orhan IE, Daglia M, et al (2016): Antibacterial and antifungal activities of thymol: A brief review of the literature. Food Chem, 210, 402-414.
- Nathan C, Cars O (2014): Antibiotic resistance--problems, progress, and prospects. N Engl J Med, 371, 1761-1763.
- Özdemir H, Keyvan E (2016): Isolation and characterisation of Staphylococcus aureus strains isolated from beef, sheep and chicken meat. Ankara Univ Vet Fak Derg, 63, 333-338.
- Palombo EA (2011): Traditional Medicinal Plant Extracts and Natural Products with Activity against Oral Bacteria: Potential Application in the Prevention and Treatment of Oral Diseases. Evid Based Complement Alternat Med, 2011, 680354.
- Porter JA, Morey A, Monu EA (2020): Antimicrobial efficacy of white mustard essential oil and carvacrol against Salmonella in refrigerated ground chicken. Poult Sci, 99, 5091-5095.
- Rudramurthy GR, Swamy MK, Sinniah UR, et al (2016): Nanoparticles: Alternatives Against Drug-Resistant Pathogenic Microbes. Molecules, 21, 836.
- Sagdic O, Ozkan G, Ozcan M, et al (2005): A study on inhibitory effects of Sigla tree (Liquidambar orientalis Mill. var. orientalis) storax against several bacteria. Phytother Res, 19, 549-551.
- Sandikci Altunatmaz S, Yilmaz Aksu F, Issa G (2016): Antimicrobial effects of curcumin against L. monocytogenes, S. aureus, S. Typhimurium and E. coli O157: H7 pathogens in minced meat. Vet Med (Praha), 61, 256-262.
- Silva J, Abebe W, Sousa SM, et al (2003): Analgesic and anti-inflammatory effects of essential oils of Eucalyptus. J Ethnopharmacol, 89, 277-283.
- Silva ACD, Santos PDF, Palazzi NC, et al (2017): Production and characterization of curcumin microcrystals and evaluation of the antimicrobial and sensory aspects in minimally processed carrots. Food Funct, 8, 1851-1858.
- Stanić Z (2017): Curcumin, a Compound from Natural Sources, a True Scientific Challenge - A Review. Plant Foods Hum Nutr, 72, 1-12.
- Tariq S, Wani S, Rasool W, et al (2019): A comprehensive review of the antibacterial, antifungal and antiviral potential of essential oils and their chemical constituents against drug-resistant microbial pathogens. Microb Pathog, 134, 103580.
- Tutun H, Koç N, Kart A (2018): Plant essential oils used against some bee diseases. TURJAF, 6, 34-45.
- Tyagi P, Singh M, Kumari H, et al (2015): Bactericidal activity of curcumin I is associated with damaging of bacterial membrane. PLoS One, 10, e0121313.
- Ugurlu E, Secmen O (2008): Medicinal plants popularly used in the villages of Yunt Mountain(Manisa-Turkey). Fitoterapia, 79, 126-131.
- Ultee A, Kets EP, Smid EJ (1999): Mechanisms of action of carvacrol on the food-borne pathogen Bacillus cereus. Appl Environ Microbiol, 65, 4606-4610.
- Ultee A, Bennik MHJ, Moezelaar R (2002): The phenolic hydroxyl group of carvacrol is essential for action against the food-borne pathogen Bacillus cereus. Appl Environ Microbiol, 68, 1561-1568.
- Wells J, Butterfield J (1999): Incidence of Salmonella on fresh fruits and vegetables affected by fungal rots or physical injury. Plant Dis, 83, 722-726.
- White PL, Naugle AL, Jackson CR, et al (2007): Salmonella Enteritidis in meat, poultry, and pasteurized egg products regulated by the US Food Safety and Inspection Service, 1998 through 2003. J Food Prot, 70, 582-591.
- World-Health-Organization (2021): Food safety. Available at https://www.who.int/news-room/fact-sheets/detail/food-safety. (Accessed January 10, 2021).
Year 2022,
Volume: 69 Issue: 4, 355 - 360, 30.09.2022
Abstract
Project Number
119O672
References
- Adamczak A, Ożarowski M, Karpiński TM (2020): Curcumin, a Natural Antimicrobial Agent with Strain-Specific Activity. Pharmaceuticals, 13, 153.
- Akram M, Shahab-Uddin AA, Usmanghani K, et al (2010): Curcuma longa and curcumin: a review article. Rom J Biol Plant Biol, 55, 65-70.
- Arslan MB, Şahin HT (2016): Unutulan Bir Orman Ürünü Kaynağı: Anadolu Sığla Ağacı (Liquidambar Orientalis Miller). Bartın Orman Fakültesi Dergisi, 18, 103-117.
- Bintsis T (2017): Foodborne pathogens. AIMS Microbiol, 3, 529-563.
- Božik M, Hovorková P, Klouček P (2018): Antibacterial Effect of Carvacrol and Coconut Oil on Selected Pathogenic Bacteria. Scientia Agriculturae Bohemica, 49, 46-52.
- Cabarkapa I, Colovic R, Duragic O, et al (2019): Anti-biofilm activities of essential oils rich in carvacrol and thymol against Salmonella Enteritidis. Biofouling, 35, 361-375.
- Chouhan S, Sharma K, Guleria S (2017): Antimicrobial Activity of Some Essential Oils—Present Status and Future Perspectives. Medicines, 4, 58.
- Clinical and Laboratory Sandards Institute (2018): Performance Standards for Antimicrobial Susceptibility Testing. 26th ed Pennsylvania, USA M100S.
- Demirtas A, Ozturk H, Sudagidan M, et al (2019): Effects of commercial aldehydes from green leaf volatiles (green odour) on rumen microbial population and fermentation profile in an artificial rumen (Rusitec). Anaerobe, 55, 83-92.
- Eng S-K, Pusparajah P, Ab Mutalib N-S, et al (2015): Salmonella: a review on pathogenesis, epidemiology and antibiotic resistance. Frontiers in Life Science, 8, 284-293.
- Engel JB, Heckler C, Tondo EC, et al (2017): Antimicrobial activity of free and liposome-encapsulated thymol and carvacrol against Salmonella and Staphylococcus aureus adhered to stainless steel. Int J Food Microbiol, 252, 18-23.
- Erdem Y, Gisho H, Ekrem S, et al (1993): Traditional medicine in Turkey IV. Folk medicine in the Mediterranean subdivision. J Ethnopharmacol, 39, 31-38.
- Gong J, Xu M, Zhu C, et al (2013): Antimicrobial resistance, presence of integrons and biofilm formation of Salmonella Pullorum isolates from Eastern China (1962-2010). Avian Pathol, 42, 290-294.
- Gunes H, Gulen D, Mutlu R, et al (2016): Antibacterial effects of curcumin: An in vitro minimum inhibitory concentration study. Toxicol Ind Health, 32, 246-250.
- Gupta PD, Birdi TJ (2017): Development of botanicals to combat antibiotic resistance. J Ayurveda Integr Med, 8, 266-275.
- Gurbuz I, Yesilada E, Demirci B, et al (2013): Characterization of volatiles and anti-ulcerogenic effect of Turkish sweetgum balsam (Styrax liquidus). J Ethnopharmacol, 148, 332-336.
- Honda G, Yeşilada E, Tabata M, et al (1996): Traditional medicine in Turkey VI. Folk medicine in West Anatolia: Afyon, Kütahya, Denizli, Muğla, Aydin provinces. J Ethnopharmacol, 53, 75-87.
- Howard ZR, O'Bryan CA, Crandall PG, et al (2012): Salmonella Enteritidis in shell eggs: Current issues and prospects for control. Food Res Int, 45, 755-764.
- Iramiot JS, Kajumbula H, Bazira J, et al (2020): Antimicrobial resistance at the human-animal interface in the Pastoralist Communities of Kasese District, South Western Uganda. Sci Rep, 10, 14737.
- İstek A (1995): Sığla Yağı (Storax)’nın Kimyasal Bileşenleri. Master Thesis. Graduate Institute of Natural and Applied Sciences, Trabzon.
- Kang MS, Oh JS, Kang IC, et al (2008): Inhibitory effect of methyl gallate and gallic acid on oral bacteria. J Microbiol, 46, 744-750.
- Karagoz A, Tutun H, Altintas L, et al (2020): Molecular typing of drug-resistant Mycobacterium tuberculosis strains from Turkey. J Glob Antimicrob Resist, 23, 130-134.
- Keyvan E, Tutun H (2019): Effects of carvacrol on Staphylococcus aureus isolated from bulk tank milk. Med Weter, 75, 238-241.
- Khameneh B, Iranshahy M, Soheili V, et al (2019): Review on plant antimicrobials: a mechanistic viewpoint. Antimicrob Resist Infect Control, 8, 118.
- Kharat M, Du Z, Zhang G, et al (2017): Physical and Chemical Stability of Curcumin in Aqueous Solutions and Emulsions: Impact of pH, Temperature, and Molecular Environment. J Agric Food Chem, 65, 1525-1532.
- Kocaadam B, Sanlier N (2017): Curcumin, an active component of turmeric (Curcuma longa), and its effects on health. Crit Rev Food Sci Nutr, 57, 2889-2895.
- Kuang X, Hao H, Dai M, et al (2015): Serotypes and antimicrobial susceptibility of Salmonella spp. isolated from farm animals in China. Front Microbiol, 6, 602-602.
- Marathe SA, Ray S, Chakravortty D (2010): Curcumin Increases the Pathogenicity of Salmonella enterica Serovar Typhimurium in Murine Model. PLoS One, 5, e11511.
- Marchese A, Orhan IE, Daglia M, et al (2016): Antibacterial and antifungal activities of thymol: A brief review of the literature. Food Chem, 210, 402-414.
- Nathan C, Cars O (2014): Antibiotic resistance--problems, progress, and prospects. N Engl J Med, 371, 1761-1763.
- Özdemir H, Keyvan E (2016): Isolation and characterisation of Staphylococcus aureus strains isolated from beef, sheep and chicken meat. Ankara Univ Vet Fak Derg, 63, 333-338.
- Palombo EA (2011): Traditional Medicinal Plant Extracts and Natural Products with Activity against Oral Bacteria: Potential Application in the Prevention and Treatment of Oral Diseases. Evid Based Complement Alternat Med, 2011, 680354.
- Porter JA, Morey A, Monu EA (2020): Antimicrobial efficacy of white mustard essential oil and carvacrol against Salmonella in refrigerated ground chicken. Poult Sci, 99, 5091-5095.
- Rudramurthy GR, Swamy MK, Sinniah UR, et al (2016): Nanoparticles: Alternatives Against Drug-Resistant Pathogenic Microbes. Molecules, 21, 836.
- Sagdic O, Ozkan G, Ozcan M, et al (2005): A study on inhibitory effects of Sigla tree (Liquidambar orientalis Mill. var. orientalis) storax against several bacteria. Phytother Res, 19, 549-551.
- Sandikci Altunatmaz S, Yilmaz Aksu F, Issa G (2016): Antimicrobial effects of curcumin against L. monocytogenes, S. aureus, S. Typhimurium and E. coli O157: H7 pathogens in minced meat. Vet Med (Praha), 61, 256-262.
- Silva J, Abebe W, Sousa SM, et al (2003): Analgesic and anti-inflammatory effects of essential oils of Eucalyptus. J Ethnopharmacol, 89, 277-283.
- Silva ACD, Santos PDF, Palazzi NC, et al (2017): Production and characterization of curcumin microcrystals and evaluation of the antimicrobial and sensory aspects in minimally processed carrots. Food Funct, 8, 1851-1858.
- Stanić Z (2017): Curcumin, a Compound from Natural Sources, a True Scientific Challenge - A Review. Plant Foods Hum Nutr, 72, 1-12.
- Tariq S, Wani S, Rasool W, et al (2019): A comprehensive review of the antibacterial, antifungal and antiviral potential of essential oils and their chemical constituents against drug-resistant microbial pathogens. Microb Pathog, 134, 103580.
- Tutun H, Koç N, Kart A (2018): Plant essential oils used against some bee diseases. TURJAF, 6, 34-45.
- Tyagi P, Singh M, Kumari H, et al (2015): Bactericidal activity of curcumin I is associated with damaging of bacterial membrane. PLoS One, 10, e0121313.
- Ugurlu E, Secmen O (2008): Medicinal plants popularly used in the villages of Yunt Mountain(Manisa-Turkey). Fitoterapia, 79, 126-131.
- Ultee A, Kets EP, Smid EJ (1999): Mechanisms of action of carvacrol on the food-borne pathogen Bacillus cereus. Appl Environ Microbiol, 65, 4606-4610.
- Ultee A, Bennik MHJ, Moezelaar R (2002): The phenolic hydroxyl group of carvacrol is essential for action against the food-borne pathogen Bacillus cereus. Appl Environ Microbiol, 68, 1561-1568.
- Wells J, Butterfield J (1999): Incidence of Salmonella on fresh fruits and vegetables affected by fungal rots or physical injury. Plant Dis, 83, 722-726.
- White PL, Naugle AL, Jackson CR, et al (2007): Salmonella Enteritidis in meat, poultry, and pasteurized egg products regulated by the US Food Safety and Inspection Service, 1998 through 2003. J Food Prot, 70, 582-591.
- World-Health-Organization (2021): Food safety. Available at https://www.who.int/news-room/fact-sheets/detail/food-safety. (Accessed January 10, 2021).
There are 48 citations in total.
Details
| Primary Language | English |
|---|---|
| Subjects | Veterinary Surgery |
| Journal Section | Research Article |
| Authors | |
| Project Number | 119O672 |
| Publication Date | September 30, 2022 |
| Published in Issue | Year 2022Volume: 69 Issue: 4 |
