Research Article
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Biofilm Production and Antimicrobial Susceptibility Profiles of Bacillus spp. from Meats

Year 2018, , 1674 - 1682, 01.12.2018
https://doi.org/10.16984/saufenbilder.395016

Abstract

The genus Bacillus
is frequently found in soil, water and food. Bacillus cereus and Bacillus
anthracis
are the main pathogens causing foodborne diseases and serious
infections in humans. A total of 52 Bacillus
spp. from meat samples was tested for determination of biofilm production, antimicrobial
resistance pattern and beta-lactamase activity. The 24 (46.1%) Bacillus isolates were found to be for
biofilm production. Of the 24 (46.1%) biofilm producer Bacillus isolates, 13 (25%), 6 (11.5%) and 5 (9.6%) were considered
as strong, moderate and weak biofilm producer, respectively. The most common species
for the production of biofilm was Bacillus
thuringiensis
(80%). Antimicrobial disk susceptibility tests of Bacillus spp. revealed high resistance
to ampicillin (84.6%) followed by penicillin (75%), cefepime (34.6%), and
cefoxitin (26.9%). A multidrug resistance to at least 3 or more antimicrobials
was observed in the 25 isolates (48.1%). All Bacillus spp. were sensitive to vancomycin, gentamicin, amikacin, ciprofloxacin,
and imipenem. The susceptibility rate to streptomycin, chloramphenicol, and
trimethoprim-sulphamethoxazole was 94.2%. Among the isolates, the 6 (11.5%) isolates
were found to be sensitive to all antimicrobial agents tested. Besides, only
one isolate from meat was found to be positive for beta-lactamase test. The
existence of biofilm production as a virulence factor and of multidrug
resistance in bacteria isolated from food should not be underestimated in terms
of food safety, public health and economic concerns.

References

  • [1] W.E Farrar, and A. C. Reboli, “The Genus Bacillus-Medical”. In: Dworkin, M, Falkow S. Rosenberg E, Stackebrandt E, Schleifer KH. (Eds.), The Prokaryotes, vol.4. Springer, Minneapolis, pp. 609-630, 2006.[2] A.K. Bhunia, “Foodborne microbial pathogens: mechanisms and pathogenesis”, Springer, New York, 2008.[3] N.A. Logan, A. R. Hoffmaster, S. V. Shadomy, K. E. Stauffer, “Bacillus and other aerobic endospore forming bacteria”. In. Versalovic J, Carroll, KC, Funke G, Jorgensen JH, Landry, ML, Warnock DW. (Eds.), Manual of Clinical Microbiology, 10th edn, Vol. 1, Washington DC, American Society for Microbiology, pp. 381–402. 2011.[4] L. V. Poulsen, “Microbial biofilm in food processing”, Lebensmittel-Wissenschaft and Technologie, vol. 32, pp. 321-326, 1999.[5] R. M. Donlan and J. W. Costerton JW. “Biofilms: survival mechanisms of clinically relevant microorganisms”, Clinical Microbiology Reviews, vol. 15, pp. 167-193, 2002.[6] A. Cherif-Antar, B. Moussa Boudjemaa, N. Didouh, K. Medjahdi, B. Mayo , and A.B. Florez, “Diversity and biofilm-forming capability of bacteria recovered from stainless steel pipes of a milk-processing dairy plant”. Dairy Science and Technology, vol. 96, pp. 27–38, 2016[7] T.F. Mah, and G. A. O’Toole, “Mechanisms of biofilm resistance to antimicrobial agents”, Trends in Microbiology, vol. 9, pp. 34-39, 2001.[8] J. D. Brooks, and S. H. Flint, “Biofilms in the food industry: problems and potential solutions”, International Journal of Food Science and Technology, vol. 43 no. 12, pp. 2163–2176, 2008.[9] P.F. McDermott, S. Zhao, D.D. Wagner, S. Simjee, R.D. Walker, D.G. White. “The food safety perspective of antibiotic resistance”, Animal Biotechnology, 13:71–84. 2002.[10] J. Romero, C. G. Feijoó and P. Navarrete, “Antibiotics in Aquaculture – Use, Abuse and Alternatives”, Health and Environment in Aquaculture, 10.5772/28157, 2012.[11] C. U. Tuazon, H. W. Murray, C. Levy, M. N. Solny, J. A. Curtin, and J. N. Sheagren, “Serious infections from Bacillus sp. ” Journal of the American Medical Association, 241:1137-1140, 1979.[12] D. Djordjevic, M. Wiedmann, and L. A. McLandsborough, “Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation”. Applied and Environmental Microbiology, vol. 68, pp. 2950-2958, 2002.[13] S. Stepanovic, D. Vukovic, I Dakic, B. Savic, and M. Svabic-Vlahovic, “A modified microtiter-plate test for quantification of staphylococcal biofilm formation” Journal of Microbiological Methods, vol.40, pp. 175–179, 2000.[14] Clinical and Laboratory Standards Institute. “Performance standards for antimicrobial disk susceptibility tests; approved standard-11th ed CLSI document M02-A1”, vol. 32, no.1, Clinical and Laboratory Standards Institute, Wayne, PA, 2012.[15] T.R. Oberhofer, D. W. Towle, “Evaluation of the rapid penicillinase paper strip test for detection of beta-lactamase” Journal of Clinical Microbiology, vol.15, pp. 196-199, 1982.[16] R. Kuroki , K. Kawakami , L. Qin, C. Kaji , K. Watanabe, Y. Kimura, C. Ishiguro, S. Tanimura, Y. Tsuchiya, I. Hamaguchi, M. Sakakura, S. Sakabe S, K. Tsuji, M. Inoue, and H. Watanabe, “Nosocomial bacteremia caused by biofilm-forming Bacillus cereus and Bacillus thuringiensis” Internal Medicine Journal, vol. 48, pp. 791–796, 2009.[17] M. Morikawa, S. Kagihiro, M. Haruki, K. Takano, S. Branda, R. Kolter, and S. Kanaya, “Biofilm formation by a Bacillus subtilis strain that produces ɣ-polyglutamate”, Microbiology, vol.152, pp. 2801-2807, 2006. [18] R. Majed, C. Faille, M. Kallassy, and M. Gohar, “Bacillus cereus biofilms-same only different”, Frontiers in Microbiology, vol.7, 1054. doi: 10.3389/fmicb.2016.01054, 2016.[19] H. Y. Done, A. K. Venkatesan, and R.U. Halden. “Does the recent growth of aquaculture create antibiotic resistance threats different from those associated with land animal production in agriculture?”, Journal of the American Association of Pharmaceutical Scientists, vol.17, no.3, pp. 513-24, 2015. [20] O. Kursun, A. Guner, and G. Ozmen, “Prevalence of Bacillus cereus in rabbit meat consumed in Burdur-Turkey, its enterotoxin producing ability and antibiotic susceptibility”, Kafkas Universitesi Veteriner Fakultesi Dergisi, vol. 17 (Suppl A): S31-S35, 2011.[21] J.H. Yim, K. Y. Kim, J. W. Chon, D. H. Kim, H. S. Kim, D. S. Choi, I. S. Choi, and K.H. Seo, “Incidence, antibiotic susceptibility, and toxin profiles of Bacillus cereus sensu lato isolated from Korean fermented soybean products”. Journal of Food Science, vol.80, no.6, M1266-67, 2015.[22] I. Chaabouni, I. Barkallah, C. Hamdi, A. Jouini, M. Saidi, J. Mahillon, and A. Cherif, “Metabolic capacities and toxigenic potential as key drivers of Bacillus cereus ubiquity and adaptation”. Annals of Microbiology, vol. 65, pp. 975-983, 2015.[23] G. M. Noor Uddin, M. H. Larsen, H. Christensen, F. M. Aarestrup, T. M. Phu, and A. Dalsgaard, “Identification and antimicrobial resistance of bacteria isolated from probiotic products used in shrimp culture”, Plos One vol. 10, no. 7, e0132338. https://doi.org/10.1371/journal.pone.0132338, 2015.[24] B. A. Mohammadou, G. Le Blay, C. M. Mbofung, G. Barbier G, “Antimicrobial activities, toxinogenic potential and sensitivity to antibiotics of Bacillus strains isolated from Mbuja, an Hibiscus sabdariffa fermented seeds from Cameroon”. African Journal of Biotechnology, vol.13, no. 35, pp. 3617-3627, 2014.[25] M. Ikeda, Y. Yagihara, K. Tatsuno, M. Okazaki, S. Okugawa, and K. Moriya, “Clinical characteristics and antimicrobial susceptibility of Bacillus cereus blood stream infection”, Annals of Clinical Microbiology and Antimicrobials, vol.14, 43, doi 10.1186/s12941-015-0104-2, 2015.
Year 2018, , 1674 - 1682, 01.12.2018
https://doi.org/10.16984/saufenbilder.395016

Abstract

References

  • [1] W.E Farrar, and A. C. Reboli, “The Genus Bacillus-Medical”. In: Dworkin, M, Falkow S. Rosenberg E, Stackebrandt E, Schleifer KH. (Eds.), The Prokaryotes, vol.4. Springer, Minneapolis, pp. 609-630, 2006.[2] A.K. Bhunia, “Foodborne microbial pathogens: mechanisms and pathogenesis”, Springer, New York, 2008.[3] N.A. Logan, A. R. Hoffmaster, S. V. Shadomy, K. E. Stauffer, “Bacillus and other aerobic endospore forming bacteria”. In. Versalovic J, Carroll, KC, Funke G, Jorgensen JH, Landry, ML, Warnock DW. (Eds.), Manual of Clinical Microbiology, 10th edn, Vol. 1, Washington DC, American Society for Microbiology, pp. 381–402. 2011.[4] L. V. Poulsen, “Microbial biofilm in food processing”, Lebensmittel-Wissenschaft and Technologie, vol. 32, pp. 321-326, 1999.[5] R. M. Donlan and J. W. Costerton JW. “Biofilms: survival mechanisms of clinically relevant microorganisms”, Clinical Microbiology Reviews, vol. 15, pp. 167-193, 2002.[6] A. Cherif-Antar, B. Moussa Boudjemaa, N. Didouh, K. Medjahdi, B. Mayo , and A.B. Florez, “Diversity and biofilm-forming capability of bacteria recovered from stainless steel pipes of a milk-processing dairy plant”. Dairy Science and Technology, vol. 96, pp. 27–38, 2016[7] T.F. Mah, and G. A. O’Toole, “Mechanisms of biofilm resistance to antimicrobial agents”, Trends in Microbiology, vol. 9, pp. 34-39, 2001.[8] J. D. Brooks, and S. H. Flint, “Biofilms in the food industry: problems and potential solutions”, International Journal of Food Science and Technology, vol. 43 no. 12, pp. 2163–2176, 2008.[9] P.F. McDermott, S. Zhao, D.D. Wagner, S. Simjee, R.D. Walker, D.G. White. “The food safety perspective of antibiotic resistance”, Animal Biotechnology, 13:71–84. 2002.[10] J. Romero, C. G. Feijoó and P. Navarrete, “Antibiotics in Aquaculture – Use, Abuse and Alternatives”, Health and Environment in Aquaculture, 10.5772/28157, 2012.[11] C. U. Tuazon, H. W. Murray, C. Levy, M. N. Solny, J. A. Curtin, and J. N. Sheagren, “Serious infections from Bacillus sp. ” Journal of the American Medical Association, 241:1137-1140, 1979.[12] D. Djordjevic, M. Wiedmann, and L. A. McLandsborough, “Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation”. Applied and Environmental Microbiology, vol. 68, pp. 2950-2958, 2002.[13] S. Stepanovic, D. Vukovic, I Dakic, B. Savic, and M. Svabic-Vlahovic, “A modified microtiter-plate test for quantification of staphylococcal biofilm formation” Journal of Microbiological Methods, vol.40, pp. 175–179, 2000.[14] Clinical and Laboratory Standards Institute. “Performance standards for antimicrobial disk susceptibility tests; approved standard-11th ed CLSI document M02-A1”, vol. 32, no.1, Clinical and Laboratory Standards Institute, Wayne, PA, 2012.[15] T.R. Oberhofer, D. W. Towle, “Evaluation of the rapid penicillinase paper strip test for detection of beta-lactamase” Journal of Clinical Microbiology, vol.15, pp. 196-199, 1982.[16] R. Kuroki , K. Kawakami , L. Qin, C. Kaji , K. Watanabe, Y. Kimura, C. Ishiguro, S. Tanimura, Y. Tsuchiya, I. Hamaguchi, M. Sakakura, S. Sakabe S, K. Tsuji, M. Inoue, and H. Watanabe, “Nosocomial bacteremia caused by biofilm-forming Bacillus cereus and Bacillus thuringiensis” Internal Medicine Journal, vol. 48, pp. 791–796, 2009.[17] M. Morikawa, S. Kagihiro, M. Haruki, K. Takano, S. Branda, R. Kolter, and S. Kanaya, “Biofilm formation by a Bacillus subtilis strain that produces ɣ-polyglutamate”, Microbiology, vol.152, pp. 2801-2807, 2006. [18] R. Majed, C. Faille, M. Kallassy, and M. Gohar, “Bacillus cereus biofilms-same only different”, Frontiers in Microbiology, vol.7, 1054. doi: 10.3389/fmicb.2016.01054, 2016.[19] H. Y. Done, A. K. Venkatesan, and R.U. Halden. “Does the recent growth of aquaculture create antibiotic resistance threats different from those associated with land animal production in agriculture?”, Journal of the American Association of Pharmaceutical Scientists, vol.17, no.3, pp. 513-24, 2015. [20] O. Kursun, A. Guner, and G. Ozmen, “Prevalence of Bacillus cereus in rabbit meat consumed in Burdur-Turkey, its enterotoxin producing ability and antibiotic susceptibility”, Kafkas Universitesi Veteriner Fakultesi Dergisi, vol. 17 (Suppl A): S31-S35, 2011.[21] J.H. Yim, K. Y. Kim, J. W. Chon, D. H. Kim, H. S. Kim, D. S. Choi, I. S. Choi, and K.H. Seo, “Incidence, antibiotic susceptibility, and toxin profiles of Bacillus cereus sensu lato isolated from Korean fermented soybean products”. Journal of Food Science, vol.80, no.6, M1266-67, 2015.[22] I. Chaabouni, I. Barkallah, C. Hamdi, A. Jouini, M. Saidi, J. Mahillon, and A. Cherif, “Metabolic capacities and toxigenic potential as key drivers of Bacillus cereus ubiquity and adaptation”. Annals of Microbiology, vol. 65, pp. 975-983, 2015.[23] G. M. Noor Uddin, M. H. Larsen, H. Christensen, F. M. Aarestrup, T. M. Phu, and A. Dalsgaard, “Identification and antimicrobial resistance of bacteria isolated from probiotic products used in shrimp culture”, Plos One vol. 10, no. 7, e0132338. https://doi.org/10.1371/journal.pone.0132338, 2015.[24] B. A. Mohammadou, G. Le Blay, C. M. Mbofung, G. Barbier G, “Antimicrobial activities, toxinogenic potential and sensitivity to antibiotics of Bacillus strains isolated from Mbuja, an Hibiscus sabdariffa fermented seeds from Cameroon”. African Journal of Biotechnology, vol.13, no. 35, pp. 3617-3627, 2014.[25] M. Ikeda, Y. Yagihara, K. Tatsuno, M. Okazaki, S. Okugawa, and K. Moriya, “Clinical characteristics and antimicrobial susceptibility of Bacillus cereus blood stream infection”, Annals of Clinical Microbiology and Antimicrobials, vol.14, 43, doi 10.1186/s12941-015-0104-2, 2015.
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Details

Primary Language English
Subjects Structural Biology
Journal Section Research Articles
Authors

Fatma Özdemir 0000-0002-4804-936X

Seza Arslan 0000-0002-2478-6875

Publication Date December 1, 2018
Submission Date February 14, 2018
Acceptance Date April 17, 2018
Published in Issue Year 2018

Cite

APA Özdemir, F., & Arslan, S. (2018). Biofilm Production and Antimicrobial Susceptibility Profiles of Bacillus spp. from Meats. Sakarya University Journal of Science, 22(6), 1674-1682. https://doi.org/10.16984/saufenbilder.395016
AMA Özdemir F, Arslan S. Biofilm Production and Antimicrobial Susceptibility Profiles of Bacillus spp. from Meats. SAUJS. December 2018;22(6):1674-1682. doi:10.16984/saufenbilder.395016
Chicago Özdemir, Fatma, and Seza Arslan. “Biofilm Production and Antimicrobial Susceptibility Profiles of Bacillus Spp. From Meats”. Sakarya University Journal of Science 22, no. 6 (December 2018): 1674-82. https://doi.org/10.16984/saufenbilder.395016.
EndNote Özdemir F, Arslan S (December 1, 2018) Biofilm Production and Antimicrobial Susceptibility Profiles of Bacillus spp. from Meats. Sakarya University Journal of Science 22 6 1674–1682.
IEEE F. Özdemir and S. Arslan, “Biofilm Production and Antimicrobial Susceptibility Profiles of Bacillus spp. from Meats”, SAUJS, vol. 22, no. 6, pp. 1674–1682, 2018, doi: 10.16984/saufenbilder.395016.
ISNAD Özdemir, Fatma - Arslan, Seza. “Biofilm Production and Antimicrobial Susceptibility Profiles of Bacillus Spp. From Meats”. Sakarya University Journal of Science 22/6 (December 2018), 1674-1682. https://doi.org/10.16984/saufenbilder.395016.
JAMA Özdemir F, Arslan S. Biofilm Production and Antimicrobial Susceptibility Profiles of Bacillus spp. from Meats. SAUJS. 2018;22:1674–1682.
MLA Özdemir, Fatma and Seza Arslan. “Biofilm Production and Antimicrobial Susceptibility Profiles of Bacillus Spp. From Meats”. Sakarya University Journal of Science, vol. 22, no. 6, 2018, pp. 1674-82, doi:10.16984/saufenbilder.395016.
Vancouver Özdemir F, Arslan S. Biofilm Production and Antimicrobial Susceptibility Profiles of Bacillus spp. from Meats. SAUJS. 2018;22(6):1674-82.

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