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The Inhibition Effects of Eugenol and Pulegone on Stenotrophomonas maltophilia: an Opportunistic Pathogen

Year 2019, Volume 16, Issue 1, 23 - 29, 25.03.2019
https://doi.org/10.32707/ercivet.538021

Abstract

Aerobic, non-fermentative and Gram-negative Stenotrophomonas maltophilia is a multidrug-resistant bacilli that is known to be pathogen for human and animals. S. maltophilia has been isolated from different animal species and also found in a variety of environments including soil, water, and plants. S. maltophilia, which has the ability to form biofilms on surfaces that cause environmental problems, is resistant to many antibiotic classes such as cephalosporins, carbapenems, and aminoglycosides. Here in this study, its aimed to determine the inhibition activities of natural phenolic compounds eugenol and pulegone against S. maltophilia MU69. Antibacterial activities of eugenol and pulegone were initially determined by disc diffusion method. Minimum Inhibitory Concentration (MIC) and Minimum Bactericidal Concentration (MBC) were also determined by tube dilution assay. Antibiofilm activities of the compounds were investigated by crystal violet staining and also monitorized using Scanning Electron Microscopy (SEM). Zone of inhibition measurements were found to be 39 mm and 28 mm for eugenol and pulegone, respectively. MIC and MBC values were found to be 3.12 mg/mL for eugenol while these were 2.5 mg/mL and 5 mg/mL for pulegone, respectively. The highest antibiofilm activity was found to be 56.30±0.45% for MIC of eugenol. To our knowledge, this is the first report of the antibacterial and antibiofilm activity of eugenol and pulegone against S. maltophilia. According to the biological activity results, it can be concluded that these natural agents may be potentially used for veterinary sciences, food industry or pharmaceutical applications that aim to manage S. maltophilia biofilm.

References

  • 1.Albini S, Abril C, Franchini M, Hüssy D, Filioussis G. Stenotrophomonas maltophilia isolated from the airways of animals with chronic respiratory disease. Schweiz Arch Tierheilkd 2009; 151(7): 323-8. 2.Ali SM, Khan AA, Ahmed I, Musaddiq M, Ahmed KS, Polasa H, Ahmed N. Antimicrobial activities of Eugenol and Cinnamaldehyde against the human gastric pathogen Helicobacter pylori. Ann Clin Microbiol Antimicrob 2005; 4(20): 1-7. 3.Alonso A, Martinez JL. Multiple antibiotic resistance in Stenotrophomonas maltophilia. Antimicrob Agents Chemother 1997; 41:1140–2. 4.Al-Shabib NA, Husain FM, Ahmad I, Baig MH. Eugenol inhibits quorum sensing and biofilm of toxigenic MRSA strains isolated from food handlers employed in Saudi Arabia. Biotechnol Biotechnol Equip 2017; 31(2): 387-96. 5.Avison MB, Higgins CS, von Heldreich CJ, Bennett PM, Walsh TR. Plasmid location and molecular heterogeneity of the L1 and L2-lactamase genes of Stenotrophomonas maltophilia. Antimicrob Agents Chemother 2001; 45(2):413-9. 6.Avison MB, von Heldreich CJ, Higgins CS, Bennett PM, Walsh TR. ATEM-2_-lactamase encoded on an active Tn1-like transposon in the genome of a clinical isolate of Stenotrophomonas maltophilia. J Antimicrob Chemother 2000; 46(6): 879-84. 7.Bassolé IHN, Juliani HR. Essential oils in combination and their antimicrobial properties. Molecules 2012; 17(4): 3989-4006. 8.Baygar T, Ugur A. In vitro Evaluation of Antimicrobial and Antibiofilm Potentials of Silver Nanoparticles Biosynthesized by Streptomyces griseorubens. IET Nanobiotechnol 2017; 11(6): 667-81. 9.Brooke JS. Stenotrophomonas maltophilia: an emerging global opportunistic pathogen. Clin Microbiol Rev 2012; 25(1): 2-41. 10.Chung HS, Hong SG, Kim YR, Shin KS, Whang DH, Ahn JY, Lee HS. Antimicrobial susceptibility of Stenotrophomonas maltophilia isolates from Korea, and the activity of antimicrobial combinations against the isolates. J Korean Med Sci 2013;28 (1): 62-6. 11.CLSI-Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. Sixteenth Informational Supplement. Document M100-S16, Wayne, PA: Clinical and Laboratory Standards Institute, 2011. 12.Collins CH, Lyne PM, Grange JM, eds, Microbiological Methods, 7th ed, Butterworths, London, 1995; p.493. 13.Crossman LC, Gould VC, Dow JM, Vernikos GS, Okazaki A, Sebaihia M, Adlem E. The complete genome, comparative and functional analysis of Stenotrophomonas maltophilia reveals an organism heavily shielded by drug resistance determinants. Genome Biol 2008; 9(4): 1-13. 14.Çıkman A, Parlak M, Bayram Y, Güdücüoğlu A, Berktaş M. Antibiotics resistance of Stenotrophomonas maltophilia strains isolated from various clinical specimens. Afr Health Sci 2016; 16 (1): 149-152. 15.de Oliveira-Garcia D, Dall'Agnol M, Rosales M, Azzuz A, Alcántara N, Martinez M, Girón J. Fimbriae and adherence of Stenotrophomonas maltophilia to epithelial cells and to abiotic surfaces. Cell Microbiol 2003; 5: 625-36. 16.Devi KP, Nisha SA, Sakthivel R, Pandian SK. Eugenol (an essential oil of clove) acts as an antibacterial agent against Salmonella typhi by disrupting the cellular membrane. J Ethnopharmacol 2010; 130(1): 107-115. 17.Draper CS, Walker RD, Lawler HE. Patterns of oral bacterial infection in captive snakes. J Am Vet Med Assoc 1981; 179(11): 1223-6. 18.Duru ME, Öztürk M, Uğur A, Ceylan Ö. The constituents of essential oil and in vitro antimicrobial activity of Micromeria cilicica from Turkey. J Ethnopharmacol 2004; 94(1): 43-8. 19.El Abed N, Kaabi B, Smaali MI, Chabbouh M, Habibi K, Mejri M, Ben Hadj Ahmed S. Chemical composition, antioxidant and antimicrobial activities of Thymus capitata essential oil with its preservative effect against Listeria monocytogenes inoculated in minced beef meat. Evid Based Complement Alternat Med 2014; 2014:1-12. 20.Filgueiras CT, Vanetti MCD. Effect of eugenol on growth and listeriolysin o production by Listeria monocytogenes. Braz arch biol technol 2006; 49(3): 405-9. 21.Geng Y, Wang K, Chen D, Huang X, He M, Yin Z. Stenotrophomonas maltophilia, an emerging opportunist pathogen for cultured channel catfish, Ictalurus punctatus, in China. Aquaculture 2010; 308(3): 132-5. 22.Harborne JB, Baxter H, Moss GP. Dictionary of Plant Toxins. Chichester. John Wiley and Sons, 1996; p. 310-1. 23.Harris NB, Rogers DG. Septicemia associated with Stenotrophomonas maltophilia in a West African dwarf crocodile (Osteolaemus tetraspis subsp. tetraspis). J Vet Diagn Investig 2001; 13(3): 255-8. 24.Hu LF, Chang X, Ye Y, Wang ZX, Shao YB, Shi W, Li JB. Stenotrophomonas maltophilia resistance to trimethoprim/sulfamethoxazole mediated by acquisition of sul and dfrA genes in a plasmid-mediated class 1 integron. Int J Antimicrob Agents 2011; 37(3): 230-4. 25.Ito M, Murakami K, Yoshino M. Antioxidant action of eugenol compounds: role of metal ion in the inhibition of lipid peroxidation. Food Chem Toxicol 2005; 43(3): 461-6. 26.Johnson EH, Busaidy R, Hameed MS. An outbreak of lymphadenitis associated with Stenotrophomonas (Xanthomonas) maltophilia in Omani goats. J Vet Med B 2003; 50(2): 102-4. 27.Kapetanovic D, Kurtovic B, Vardic I, Teskeredtzic E, Teskeredzic Z. Gill disease in a gilthead sea bream (Sparus aurata L.). Medycyna Wet 2006; 62(11): 1239–41. 28.Khalil AA, ur Rahman U, Khan MR, Sahar A, Mehmood T, Khan M. Essential oil eugenol: sources, extraction techniques and nutraceutical perspectives. RSC Advances 2017; 7(52): 32669-81. 29.Kim SS, Oh OJ, Min HY, Park EJ, Kim Y, Park HJ, Lee SK (2003). Eugenol suppresses cyclooxygenase-2 expression in lipopolysaccharide-stimulated mouse macrophage RAW264. 7 cells. Life sciences 2003; 73(3): 337-48. 30.Liaw SJ, Lee YL, Hsueh PR. Multidrug resistance in clinical isolates of Stenotrophomonas maltophilia: roles of integrons, efflux pumps, phosphoglucomutase (SpgM), and melanin and biofilm formation. Int J Antimicrob Agents 2010; 35(2): 126-30. 31.MacDiarmid JA, Burrell DH. Characterization of Pseudomonas maltophilia isolates from fleece rot. Appl Environ Microbiol 1986; 51(2): 346-8. 32.Mah TFC, O'Toole GA. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 2001; 9(1): 34-9. 33.Merritt JH, Kadouri DE, O'Toole GA. Growing and analyzing static biofilms. Curr Protoc Microbiol 2005; 22(1): 1-18. 34.Mkaddem M, Bouajila J, Ennajar M, Lebrihi A, Mathieu F, Romdhane M. Chemical composition and antimicrobial and antioxidant activities of Mentha (longifolia L. and viridis) essential oils. J Food Sci 2009; 74(7): 358-63. 35.Prasad SN. Neuroprotective efficacy of eugenol and isoeugenol in acrylamide-induced neuropathy in rats: behavioral and biochemical evidence. Neurochem Res 2013; 38(2): 330-45. 36.Rauscher FM, Sanders RA, Watkins JB. Effects of isoeugenol on oxidative stress pathways in normal and streptozotocin‐induced diabetic rats. J Biochem Mol Toxicol 2001; 15(3): 159-164. 37.Soković M, Glamočlija J, Marin PD, Brkić D, van Griensven LJ. Antibacterial effects of the essential oils of commonly consumed medicinal herbs using an in vitro model. Molecules 2010; 15(11): 7532-46. 38.Sousa DPD, Nóbrega FF, de Lima MR, Almeida RND. Pharmacological activity of (R)-(+)-pulegone, a chemical constituent of essential oils. Z Naturforsch C 2011; 66(7-8): 353-9. 39.Srinivasan S, Sathish G, Jayanthi M, Muthukumaran J, Muruganathan U, Ramachandran V. Ameliorating effect of eugenol on hyperglycemia by attenuating the key enzymes of glucose metabolism in streptozotocin-induced diabetic rats. Mol Cell Biochem 2014; 385(1-2): 159-168. 40.Upadhyay A, Upadhyaya I, Kollanoor-Johny A, Venkitanarayanan K. Antibiofilm effect of plant derived antimicrobials on Listeria monocytogenes. Food microbiology 2013; 36(1): 79-89. 41.Vartivarian S, Anaissie E, Bodey G, Sprigg H, Rolston KA changing pattern of susceptibility of Xanthamonas maltophilia to antimicrobial agents: implications for therapy. Antimicrob Agents Chemother 1994; 38:624–7. 42.Venkadeswaran K, Muralidharan AR, Annadurai T, Ruban VV, Sundararajan M, Anandhi R, Geraldine P. Antihypercholesterolemic and antioxidative potential of an extract of the plant, Piper betle, and its active constituent, eugenol, in triton WR-1339-Induced hypercholesterolemia in experimental rats. Evid Based Complementary Altern Med 2014: 1-11. 43.Vidhy N, Devaraj SN. Induction of apoptosis by eugenol in human breast cancer cells. Indian J Exp Biol 2011; 49(11): 871-78. 44.Walsh SE, Maillard JY, Russell AD, Catrenich CE, Charbonneau DL, Bartolo RG. Activity and mechanisms of action of selected biocidal agents on Gram‐positive and‐negative bacteria. J Appl Microbiol 2003; 94(2): 240-7. 45.Yogalakshmi B, Viswanathan P, Anuradha CV. Investigation of antioxidant, anti-inflammatory and DNA-protective properties of eugenol in thioacetamide-induced liver injury in rats. Toxicology 2010; 268(3): 204-12. 46.Zhang L, Xian-Zhi L, Poole K. Multiple Antibiotic Resistance in Stenotrophomonas maltophilia: Involvement of a Multidrug Efflux System. Antimicrob Agents Chemother 2000; 44(2): 287-93. 47.Zhou YC, Zhu, CH, Zhang B. Isolation and prevention of the pathogen causing large scale death on Trachinotus ovatus. Mar Sci 2001; 25(4): 40-4.

Year 2019, Volume 16, Issue 1, 23 - 29, 25.03.2019
https://doi.org/10.32707/ercivet.538021

Abstract

References

  • 1.Albini S, Abril C, Franchini M, Hüssy D, Filioussis G. Stenotrophomonas maltophilia isolated from the airways of animals with chronic respiratory disease. Schweiz Arch Tierheilkd 2009; 151(7): 323-8. 2.Ali SM, Khan AA, Ahmed I, Musaddiq M, Ahmed KS, Polasa H, Ahmed N. Antimicrobial activities of Eugenol and Cinnamaldehyde against the human gastric pathogen Helicobacter pylori. Ann Clin Microbiol Antimicrob 2005; 4(20): 1-7. 3.Alonso A, Martinez JL. Multiple antibiotic resistance in Stenotrophomonas maltophilia. Antimicrob Agents Chemother 1997; 41:1140–2. 4.Al-Shabib NA, Husain FM, Ahmad I, Baig MH. Eugenol inhibits quorum sensing and biofilm of toxigenic MRSA strains isolated from food handlers employed in Saudi Arabia. Biotechnol Biotechnol Equip 2017; 31(2): 387-96. 5.Avison MB, Higgins CS, von Heldreich CJ, Bennett PM, Walsh TR. Plasmid location and molecular heterogeneity of the L1 and L2-lactamase genes of Stenotrophomonas maltophilia. Antimicrob Agents Chemother 2001; 45(2):413-9. 6.Avison MB, von Heldreich CJ, Higgins CS, Bennett PM, Walsh TR. ATEM-2_-lactamase encoded on an active Tn1-like transposon in the genome of a clinical isolate of Stenotrophomonas maltophilia. J Antimicrob Chemother 2000; 46(6): 879-84. 7.Bassolé IHN, Juliani HR. Essential oils in combination and their antimicrobial properties. Molecules 2012; 17(4): 3989-4006. 8.Baygar T, Ugur A. In vitro Evaluation of Antimicrobial and Antibiofilm Potentials of Silver Nanoparticles Biosynthesized by Streptomyces griseorubens. IET Nanobiotechnol 2017; 11(6): 667-81. 9.Brooke JS. Stenotrophomonas maltophilia: an emerging global opportunistic pathogen. Clin Microbiol Rev 2012; 25(1): 2-41. 10.Chung HS, Hong SG, Kim YR, Shin KS, Whang DH, Ahn JY, Lee HS. Antimicrobial susceptibility of Stenotrophomonas maltophilia isolates from Korea, and the activity of antimicrobial combinations against the isolates. J Korean Med Sci 2013;28 (1): 62-6. 11.CLSI-Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing. Sixteenth Informational Supplement. Document M100-S16, Wayne, PA: Clinical and Laboratory Standards Institute, 2011. 12.Collins CH, Lyne PM, Grange JM, eds, Microbiological Methods, 7th ed, Butterworths, London, 1995; p.493. 13.Crossman LC, Gould VC, Dow JM, Vernikos GS, Okazaki A, Sebaihia M, Adlem E. The complete genome, comparative and functional analysis of Stenotrophomonas maltophilia reveals an organism heavily shielded by drug resistance determinants. Genome Biol 2008; 9(4): 1-13. 14.Çıkman A, Parlak M, Bayram Y, Güdücüoğlu A, Berktaş M. Antibiotics resistance of Stenotrophomonas maltophilia strains isolated from various clinical specimens. Afr Health Sci 2016; 16 (1): 149-152. 15.de Oliveira-Garcia D, Dall'Agnol M, Rosales M, Azzuz A, Alcántara N, Martinez M, Girón J. Fimbriae and adherence of Stenotrophomonas maltophilia to epithelial cells and to abiotic surfaces. Cell Microbiol 2003; 5: 625-36. 16.Devi KP, Nisha SA, Sakthivel R, Pandian SK. Eugenol (an essential oil of clove) acts as an antibacterial agent against Salmonella typhi by disrupting the cellular membrane. J Ethnopharmacol 2010; 130(1): 107-115. 17.Draper CS, Walker RD, Lawler HE. Patterns of oral bacterial infection in captive snakes. J Am Vet Med Assoc 1981; 179(11): 1223-6. 18.Duru ME, Öztürk M, Uğur A, Ceylan Ö. The constituents of essential oil and in vitro antimicrobial activity of Micromeria cilicica from Turkey. J Ethnopharmacol 2004; 94(1): 43-8. 19.El Abed N, Kaabi B, Smaali MI, Chabbouh M, Habibi K, Mejri M, Ben Hadj Ahmed S. Chemical composition, antioxidant and antimicrobial activities of Thymus capitata essential oil with its preservative effect against Listeria monocytogenes inoculated in minced beef meat. Evid Based Complement Alternat Med 2014; 2014:1-12. 20.Filgueiras CT, Vanetti MCD. Effect of eugenol on growth and listeriolysin o production by Listeria monocytogenes. Braz arch biol technol 2006; 49(3): 405-9. 21.Geng Y, Wang K, Chen D, Huang X, He M, Yin Z. Stenotrophomonas maltophilia, an emerging opportunist pathogen for cultured channel catfish, Ictalurus punctatus, in China. Aquaculture 2010; 308(3): 132-5. 22.Harborne JB, Baxter H, Moss GP. Dictionary of Plant Toxins. Chichester. John Wiley and Sons, 1996; p. 310-1. 23.Harris NB, Rogers DG. Septicemia associated with Stenotrophomonas maltophilia in a West African dwarf crocodile (Osteolaemus tetraspis subsp. tetraspis). J Vet Diagn Investig 2001; 13(3): 255-8. 24.Hu LF, Chang X, Ye Y, Wang ZX, Shao YB, Shi W, Li JB. Stenotrophomonas maltophilia resistance to trimethoprim/sulfamethoxazole mediated by acquisition of sul and dfrA genes in a plasmid-mediated class 1 integron. Int J Antimicrob Agents 2011; 37(3): 230-4. 25.Ito M, Murakami K, Yoshino M. Antioxidant action of eugenol compounds: role of metal ion in the inhibition of lipid peroxidation. Food Chem Toxicol 2005; 43(3): 461-6. 26.Johnson EH, Busaidy R, Hameed MS. An outbreak of lymphadenitis associated with Stenotrophomonas (Xanthomonas) maltophilia in Omani goats. J Vet Med B 2003; 50(2): 102-4. 27.Kapetanovic D, Kurtovic B, Vardic I, Teskeredtzic E, Teskeredzic Z. Gill disease in a gilthead sea bream (Sparus aurata L.). Medycyna Wet 2006; 62(11): 1239–41. 28.Khalil AA, ur Rahman U, Khan MR, Sahar A, Mehmood T, Khan M. Essential oil eugenol: sources, extraction techniques and nutraceutical perspectives. RSC Advances 2017; 7(52): 32669-81. 29.Kim SS, Oh OJ, Min HY, Park EJ, Kim Y, Park HJ, Lee SK (2003). Eugenol suppresses cyclooxygenase-2 expression in lipopolysaccharide-stimulated mouse macrophage RAW264. 7 cells. Life sciences 2003; 73(3): 337-48. 30.Liaw SJ, Lee YL, Hsueh PR. Multidrug resistance in clinical isolates of Stenotrophomonas maltophilia: roles of integrons, efflux pumps, phosphoglucomutase (SpgM), and melanin and biofilm formation. Int J Antimicrob Agents 2010; 35(2): 126-30. 31.MacDiarmid JA, Burrell DH. Characterization of Pseudomonas maltophilia isolates from fleece rot. Appl Environ Microbiol 1986; 51(2): 346-8. 32.Mah TFC, O'Toole GA. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 2001; 9(1): 34-9. 33.Merritt JH, Kadouri DE, O'Toole GA. Growing and analyzing static biofilms. Curr Protoc Microbiol 2005; 22(1): 1-18. 34.Mkaddem M, Bouajila J, Ennajar M, Lebrihi A, Mathieu F, Romdhane M. Chemical composition and antimicrobial and antioxidant activities of Mentha (longifolia L. and viridis) essential oils. J Food Sci 2009; 74(7): 358-63. 35.Prasad SN. Neuroprotective efficacy of eugenol and isoeugenol in acrylamide-induced neuropathy in rats: behavioral and biochemical evidence. Neurochem Res 2013; 38(2): 330-45. 36.Rauscher FM, Sanders RA, Watkins JB. Effects of isoeugenol on oxidative stress pathways in normal and streptozotocin‐induced diabetic rats. J Biochem Mol Toxicol 2001; 15(3): 159-164. 37.Soković M, Glamočlija J, Marin PD, Brkić D, van Griensven LJ. Antibacterial effects of the essential oils of commonly consumed medicinal herbs using an in vitro model. Molecules 2010; 15(11): 7532-46. 38.Sousa DPD, Nóbrega FF, de Lima MR, Almeida RND. Pharmacological activity of (R)-(+)-pulegone, a chemical constituent of essential oils. Z Naturforsch C 2011; 66(7-8): 353-9. 39.Srinivasan S, Sathish G, Jayanthi M, Muthukumaran J, Muruganathan U, Ramachandran V. Ameliorating effect of eugenol on hyperglycemia by attenuating the key enzymes of glucose metabolism in streptozotocin-induced diabetic rats. Mol Cell Biochem 2014; 385(1-2): 159-168. 40.Upadhyay A, Upadhyaya I, Kollanoor-Johny A, Venkitanarayanan K. Antibiofilm effect of plant derived antimicrobials on Listeria monocytogenes. Food microbiology 2013; 36(1): 79-89. 41.Vartivarian S, Anaissie E, Bodey G, Sprigg H, Rolston KA changing pattern of susceptibility of Xanthamonas maltophilia to antimicrobial agents: implications for therapy. Antimicrob Agents Chemother 1994; 38:624–7. 42.Venkadeswaran K, Muralidharan AR, Annadurai T, Ruban VV, Sundararajan M, Anandhi R, Geraldine P. Antihypercholesterolemic and antioxidative potential of an extract of the plant, Piper betle, and its active constituent, eugenol, in triton WR-1339-Induced hypercholesterolemia in experimental rats. Evid Based Complementary Altern Med 2014: 1-11. 43.Vidhy N, Devaraj SN. Induction of apoptosis by eugenol in human breast cancer cells. Indian J Exp Biol 2011; 49(11): 871-78. 44.Walsh SE, Maillard JY, Russell AD, Catrenich CE, Charbonneau DL, Bartolo RG. Activity and mechanisms of action of selected biocidal agents on Gram‐positive and‐negative bacteria. J Appl Microbiol 2003; 94(2): 240-7. 45.Yogalakshmi B, Viswanathan P, Anuradha CV. Investigation of antioxidant, anti-inflammatory and DNA-protective properties of eugenol in thioacetamide-induced liver injury in rats. Toxicology 2010; 268(3): 204-12. 46.Zhang L, Xian-Zhi L, Poole K. Multiple Antibiotic Resistance in Stenotrophomonas maltophilia: Involvement of a Multidrug Efflux System. Antimicrob Agents Chemother 2000; 44(2): 287-93. 47.Zhou YC, Zhu, CH, Zhang B. Isolation and prevention of the pathogen causing large scale death on Trachinotus ovatus. Mar Sci 2001; 25(4): 40-4.

Details

Primary Language English
Journal Section Articles
Authors

Tuba BAYGAR (Primary Author)
0000-0002-1238-3227

Publication Date March 25, 2019
Application Date December 19, 2017
Acceptance Date July 6, 2018
Published in Issue Year 2019, Volume 16, Issue 1

Cite

Bibtex @research article { ercivet538021, journal = {Erciyes Üniversitesi Veteriner Fakültesi Dergisi}, issn = {1304-7280}, eissn = {2667-5498}, address = {}, publisher = {Erciyes University}, year = {2019}, volume = {16}, pages = {23 - 29}, doi = {10.32707/ercivet.538021}, title = {The Inhibition Effects of Eugenol and Pulegone on Stenotrophomonas maltophilia: an Opportunistic Pathogen}, key = {cite}, author = {Baygar, Tuba} }
APA Baygar, T. (2019). The Inhibition Effects of Eugenol and Pulegone on Stenotrophomonas maltophilia: an Opportunistic Pathogen . Erciyes Üniversitesi Veteriner Fakültesi Dergisi , 16 (1) , 23-29 . DOI: 10.32707/ercivet.538021
MLA Baygar, T. "The Inhibition Effects of Eugenol and Pulegone on Stenotrophomonas maltophilia: an Opportunistic Pathogen" . Erciyes Üniversitesi Veteriner Fakültesi Dergisi 16 (2019 ): 23-29 <https://dergipark.org.tr/en/pub/ercivet/issue/44121/538021>
Chicago Baygar, T. "The Inhibition Effects of Eugenol and Pulegone on Stenotrophomonas maltophilia: an Opportunistic Pathogen". Erciyes Üniversitesi Veteriner Fakültesi Dergisi 16 (2019 ): 23-29
RIS TY - JOUR T1 - The Inhibition Effects of Eugenol and Pulegone on Stenotrophomonas maltophilia: an Opportunistic Pathogen AU - Tuba Baygar Y1 - 2019 PY - 2019 N1 - doi: 10.32707/ercivet.538021 DO - 10.32707/ercivet.538021 T2 - Erciyes Üniversitesi Veteriner Fakültesi Dergisi JF - Journal JO - JOR SP - 23 EP - 29 VL - 16 IS - 1 SN - 1304-7280-2667-5498 M3 - doi: 10.32707/ercivet.538021 UR - https://doi.org/10.32707/ercivet.538021 Y2 - 2018 ER -
EndNote %0 Journal of The Faculty of Veterinary Medicine Erciyes University The Inhibition Effects of Eugenol and Pulegone on Stenotrophomonas maltophilia: an Opportunistic Pathogen %A Tuba Baygar %T The Inhibition Effects of Eugenol and Pulegone on Stenotrophomonas maltophilia: an Opportunistic Pathogen %D 2019 %J Erciyes Üniversitesi Veteriner Fakültesi Dergisi %P 1304-7280-2667-5498 %V 16 %N 1 %R doi: 10.32707/ercivet.538021 %U 10.32707/ercivet.538021
ISNAD Baygar, Tuba . "The Inhibition Effects of Eugenol and Pulegone on Stenotrophomonas maltophilia: an Opportunistic Pathogen". Erciyes Üniversitesi Veteriner Fakültesi Dergisi 16 / 1 (March 2019): 23-29 . https://doi.org/10.32707/ercivet.538021
AMA Baygar T. The Inhibition Effects of Eugenol and Pulegone on Stenotrophomonas maltophilia: an Opportunistic Pathogen. Erciyes Üniv Vet Fak Derg. 2019; 16(1): 23-29.
Vancouver Baygar T. The Inhibition Effects of Eugenol and Pulegone on Stenotrophomonas maltophilia: an Opportunistic Pathogen. Erciyes Üniversitesi Veteriner Fakültesi Dergisi. 2019; 16(1): 23-29.
IEEE T. Baygar , "The Inhibition Effects of Eugenol and Pulegone on Stenotrophomonas maltophilia: an Opportunistic Pathogen", Erciyes Üniversitesi Veteriner Fakültesi Dergisi, vol. 16, no. 1, pp. 23-29, Mar. 2019, doi:10.32707/ercivet.538021