Antibiotic Resistance Profile of Bacterial Isolates from Animal Farming Aquatic Environments and Meats in a Peri-Urban Community in South Korea
The increasing usage of antibiotics in the animal
farming industry is an emerging worldwide problem contributing to
the development of antibiotic resistance. The purpose of this work was
to investigate the prevalence and antibiotic resistance profile of
bacterial isolates collected from aquatic environments and meats in a
peri-urban community in Daejeon, Korea. In an antibacterial
susceptibility test, the bacterial isolates showed a high incidence of
resistance (~ 26.04 %) to cefazolin, tetracycline, gentamycin,
norfloxacin, erythromycin and vancomycin. The results from a test for
multiple antibiotic resistance indicated that the isolates were
displaying an approximately 5-fold increase in the incidence of
multiple antibiotic resistance to combinations of two different
antibiotics compared to combinations of three or more antibiotics.
Most of the isolates showed multi-antibiotic resistance, and the
resistance patterns were similar among the sampling groups.
Sequencing data analysis of 16S rRNA showed that most of the
resistant isolates appeared to be dominated by the classes
Betaproteobacteria and Gammaproteobacteria in the phylum
Proteobacteria.
[1] Alanis, A.J. 2005. Resistance to antibiotics: are we in the post-antibiotic
era? Arch Med Res 36:697-705.
[2] Levy, S.B., and Marshall, B. 2004. Antibacterial resistance worldwide:
causes, challenges and responses. Nat Med 10:S122-129.
[3] Mathew, A.G., Cissell, R., and Liamthong, S. 2007. Antibiotic resistance
in bacteria associated with food animals: a United States perspective of
livestock production. Foodborne Pathog Dis 4:115-133.
[4] Shryock, T.R., and Richwine, A. 2010. The interface between veterinary
and human antibiotic use. Ann N Y Acad Sci 1213:92-105.
[5] Ding, C., and He, J. 2010. Effect of antibiotics in the environment on
microbial populations. Appl Microbiol Biotechnol 87:925-941.
[6] Davies, J. 1994. Inactivation of antibiotics and the dissemination of
resistance genes. Science 264:375-382.
[7] Davison, J. 1999. Genetic exchange between bacteria in the environment.
Plasmid 42:73-91.
[8] Alekshun, M.N., and Levy, S.B. 2007. Molecular mechanisms of
antibacterial multidrug resistance. Cell 128:1037-1050.
[9] Kimiran-Erdem, A., Arslan, E.O., Sanli Yurudu, N.O., Zeybek, Z.,
Dogruoz, N., and Cotuk, A. 2007. Isolation and identification of
enterococci from seawater samples: assessment of their resistance to
antibiotics and heavy metals. Environ Monit Assess 125:219-228.
[10] Servais, P., and Passerat, J. 2009. Antimicrobial resistance of fecal
bacteria in waters of the Seine river watershed (France). Sci Total Environ
408:365-372.
[11] Witte, W. 2000. Ecological impact of antibiotic use in animals on
different complex microflora: environment. Int J Antimicrob Agents
14:321-325.
[12] Kilonzo-Nthenge, A., Nahashon, S.N., Chen, F., and Adefope, N. 2008.
Prevalence and antimicrobial resistance of pathogenic bacteria in chicken
and guinea fowl. Poult Sci 87:1841-1848.
[13] Bauer, A.W., Kirby, W.M., Sherris, J.C., and Turck, M. 1966. Antibiotic
susceptibility testing by a standardized single disk method. Am J Clin
Pathol 45:493-496.
[14] Reboucas, R.H., de Sousa, O.V., Lima, A.S., Vasconcelos, F.R., de
Carvalho, P.B., and Vieira, R.H. 2011. Antimicrobial resistance profile of
Vibrio species isolated from marine shrimp farming environments
(Litopenaeus vannamei) at Ceara, Brazil. Environ Res 111:21-24.
[15] Cho, S.H., Han, J.H., Ko, H.Y., and Kim, S.B. 2008. Streptacidiphilus
anmyonensis sp. nov., Streptacidiphilus rugosus sp. nov. and
Streptacidiphilus melanogenes sp. nov., acidophilic actinobacteria
isolated from Pinus soils. Int J Syst Evol Microbiol 58:1566-1570.
[16] Hur, J., Choi, Y.Y., Park, J.H., Jeon, B.W., Lee, H.S., Kim, A.R., and Lee,
J.H. 2011. Antimicrobial resistance, virulence-associated genes, and
pulsed-field gel electrophoresis profiles of Salmonella enterica subsp.
enterica serovar Typhimurium isolated from piglets with diarrhea in
Korea. Can J Vet Res 75:49-56.
[17] Kang, M.S., Kim, A., Jung, B.Y., Her, M., Jeong, W., Cho, Y.M., Oh,
J.Y., Lee, Y.J., Kwon, J.H., and Kwon, Y.K. 2010. Characterization of
antimicrobial resistance of recent Salmonella enterica serovar Gallinarum
isolates from chickens in South Korea. Avian Pathol 39:201-205.
[18] Nam, H.M., Lim, S.K., Moon, J.S., Kang, H.M., Kim, J.M., Jang, K.C.,
Kang, M.I., Joo, Y.S., and Jung, S.C. 2010. Antimicrobial resistance of
enterococci isolated from mastitic bovine milk samples in Korea.
Zoonoses Public Health 57:e59-64.
[19] Oh, E.G., Son, K.T., Yu, H., Lee, T.S., Lee, H.J., Shin, S., Kwon, J.Y.,
Park, K., and Kim, J. 2011. Antimicrobial resistance of Vibrio
parahaemolyticus and Vibrio alginolyticus strains isolated from farmed
fish in Korea from 2005 through 2007. J Food Prot 74:380-386.
[20] Unno, T., Han, D., Jang, J., Lee, S.N., Kim, J.H., Ko, G., Kim, B.G., Ahn,
J.H., Kanaly, R.A., Sadowsky, M.J., et al. 2010. High diversity and
abundance of antibiotic-resistant Escherichia coli isolated from humans
and farm animal hosts in Jeonnam Province, South Korea. Sci Total
Environ 408:3499-3506.
[21] Lim, S.K., Lee, H.S., Nam, H.M., Cho, Y.S., Kim, J.M., Song, S.W.,
Park, Y.H., and Jung, S.C. 2007. Antimicrobial resistance observed in
Escherichia coli strains isolated from fecal samples of cattle and pigs in
Korea during 2003-2004. Int J Food Microbiol 116:283-286.
[22] Li, D., Yu, T., Zhang, Y., Yang, M., Li, Z., Liu, M., and Qi, R. 2010.
Antibiotic resistance characteristics of environmental bacteria from an
oxytetracycline production wastewater treatment plant and the receiving
river. Appl Environ Microbiol 76:3444-3451.
[23] Joseph, S.W., Hayes, J.R., English, L.L., Carr, L.E., and Wagner, D.D.
2001. Implications of multiple antimicrobial-resistant enterococci
associated with the poultry environment. Food Addit Contam
18:1118-1123.
[24] Hammerum, A.M., Lester, C.H., and Heuer, O.E. 2010.
Antimicrobial-resistant enterococci in animals and meat: a human health
hazard? Foodborne Pathog Dis 7:1137-1146.
[25] Heuer, O.E., Hammerum, A.M., Collignon, P., and Wegener, H.C. 2006.
Human health hazard from antimicrobial-resistant enterococci in animals
and food. Clin Infect Dis 43:911-916.
[26] Butaye, P., Devriese, L.A., Goossens, H., Ieven, M., and Haesebrouck, F.
1999. Enterococci with acquired vancomycin resistance in pigs and
chickens of different age groups. Antimicrob Agents Chemother
43:365-366.
[27] Butaye, P., Devriese, L.A., and Haesebrouck, F. 1999. Comparison of
direct and enrichment methods for the selective isolation of
vancomycin-resistant enterococci from feces of pigs and poultry. Microb
Drug Resist 5:131-134.
[28] Bates, J. 1997. Epidemiology of vancomycin-resistant enterococci in the
community and the relevance of farm animals to human infection. J Hosp
Infect 37:89-101.
[29] Bates, J., Jordens, J.Z., and Griffiths, D.T. 1994. Farm animals as a
putative reservoir for vancomycin-resistant enterococcal infection in man.
J Antimicrob Chemother 34:507-514.
[30] Knapp, C.W., Engemann, C.A., Hanson, M.L., Keen, P.L., Hall, K.J., and
Graham, D.W. 2008. Indirect evidence of transposon-mediated selection
of antibiotic resistance genes in aquatic systems at low-level
oxytetracycline exposures. Environ Sci Technol 42:5348-5353.
[31] Fan, C., Lee, P.K., Ng, W.J., Alvarez-Cohen, L., Brodie, E.L., Andersen,
G.L., and He, J. 2009. Influence of trace erythromycin and
eryhthromycin-H2O on carbon and nutrients removal and on resistance
selection in sequencing batch reactors (SBRs). Appl Microbiol Biotechnol
85:185-195.
[32] Esiobu, N., Armenta, L., and Ike, J. 2002. Antibiotic resistance in soil and
water environments. Int J Environ Health Res 12:133-144.
[33] Biyela, P.T., Lin, J., and Bezuidenhout, C.C. 2004. The role of aquatic
ecosystems as reservoirs of antibiotic resistant bacteria and antibiotic
resistance genes. Water Sci Technol 50:45-50.
[34] Schwartz, T., Kohnen, W., Jansen, B., and Obst, U. 2003. Detection of
antibiotic-resistant bacteria and their resistance genes in wastewater,
surface water, and drinking water biofilms. FEMS Microbiol Ecol
43:325-335.
[1] Alanis, A.J. 2005. Resistance to antibiotics: are we in the post-antibiotic
era? Arch Med Res 36:697-705.
[2] Levy, S.B., and Marshall, B. 2004. Antibacterial resistance worldwide:
causes, challenges and responses. Nat Med 10:S122-129.
[3] Mathew, A.G., Cissell, R., and Liamthong, S. 2007. Antibiotic resistance
in bacteria associated with food animals: a United States perspective of
livestock production. Foodborne Pathog Dis 4:115-133.
[4] Shryock, T.R., and Richwine, A. 2010. The interface between veterinary
and human antibiotic use. Ann N Y Acad Sci 1213:92-105.
[5] Ding, C., and He, J. 2010. Effect of antibiotics in the environment on
microbial populations. Appl Microbiol Biotechnol 87:925-941.
[6] Davies, J. 1994. Inactivation of antibiotics and the dissemination of
resistance genes. Science 264:375-382.
[7] Davison, J. 1999. Genetic exchange between bacteria in the environment.
Plasmid 42:73-91.
[8] Alekshun, M.N., and Levy, S.B. 2007. Molecular mechanisms of
antibacterial multidrug resistance. Cell 128:1037-1050.
[9] Kimiran-Erdem, A., Arslan, E.O., Sanli Yurudu, N.O., Zeybek, Z.,
Dogruoz, N., and Cotuk, A. 2007. Isolation and identification of
enterococci from seawater samples: assessment of their resistance to
antibiotics and heavy metals. Environ Monit Assess 125:219-228.
[10] Servais, P., and Passerat, J. 2009. Antimicrobial resistance of fecal
bacteria in waters of the Seine river watershed (France). Sci Total Environ
408:365-372.
[11] Witte, W. 2000. Ecological impact of antibiotic use in animals on
different complex microflora: environment. Int J Antimicrob Agents
14:321-325.
[12] Kilonzo-Nthenge, A., Nahashon, S.N., Chen, F., and Adefope, N. 2008.
Prevalence and antimicrobial resistance of pathogenic bacteria in chicken
and guinea fowl. Poult Sci 87:1841-1848.
[13] Bauer, A.W., Kirby, W.M., Sherris, J.C., and Turck, M. 1966. Antibiotic
susceptibility testing by a standardized single disk method. Am J Clin
Pathol 45:493-496.
[14] Reboucas, R.H., de Sousa, O.V., Lima, A.S., Vasconcelos, F.R., de
Carvalho, P.B., and Vieira, R.H. 2011. Antimicrobial resistance profile of
Vibrio species isolated from marine shrimp farming environments
(Litopenaeus vannamei) at Ceara, Brazil. Environ Res 111:21-24.
[15] Cho, S.H., Han, J.H., Ko, H.Y., and Kim, S.B. 2008. Streptacidiphilus
anmyonensis sp. nov., Streptacidiphilus rugosus sp. nov. and
Streptacidiphilus melanogenes sp. nov., acidophilic actinobacteria
isolated from Pinus soils. Int J Syst Evol Microbiol 58:1566-1570.
[16] Hur, J., Choi, Y.Y., Park, J.H., Jeon, B.W., Lee, H.S., Kim, A.R., and Lee,
J.H. 2011. Antimicrobial resistance, virulence-associated genes, and
pulsed-field gel electrophoresis profiles of Salmonella enterica subsp.
enterica serovar Typhimurium isolated from piglets with diarrhea in
Korea. Can J Vet Res 75:49-56.
[17] Kang, M.S., Kim, A., Jung, B.Y., Her, M., Jeong, W., Cho, Y.M., Oh,
J.Y., Lee, Y.J., Kwon, J.H., and Kwon, Y.K. 2010. Characterization of
antimicrobial resistance of recent Salmonella enterica serovar Gallinarum
isolates from chickens in South Korea. Avian Pathol 39:201-205.
[18] Nam, H.M., Lim, S.K., Moon, J.S., Kang, H.M., Kim, J.M., Jang, K.C.,
Kang, M.I., Joo, Y.S., and Jung, S.C. 2010. Antimicrobial resistance of
enterococci isolated from mastitic bovine milk samples in Korea.
Zoonoses Public Health 57:e59-64.
[19] Oh, E.G., Son, K.T., Yu, H., Lee, T.S., Lee, H.J., Shin, S., Kwon, J.Y.,
Park, K., and Kim, J. 2011. Antimicrobial resistance of Vibrio
parahaemolyticus and Vibrio alginolyticus strains isolated from farmed
fish in Korea from 2005 through 2007. J Food Prot 74:380-386.
[20] Unno, T., Han, D., Jang, J., Lee, S.N., Kim, J.H., Ko, G., Kim, B.G., Ahn,
J.H., Kanaly, R.A., Sadowsky, M.J., et al. 2010. High diversity and
abundance of antibiotic-resistant Escherichia coli isolated from humans
and farm animal hosts in Jeonnam Province, South Korea. Sci Total
Environ 408:3499-3506.
[21] Lim, S.K., Lee, H.S., Nam, H.M., Cho, Y.S., Kim, J.M., Song, S.W.,
Park, Y.H., and Jung, S.C. 2007. Antimicrobial resistance observed in
Escherichia coli strains isolated from fecal samples of cattle and pigs in
Korea during 2003-2004. Int J Food Microbiol 116:283-286.
[22] Li, D., Yu, T., Zhang, Y., Yang, M., Li, Z., Liu, M., and Qi, R. 2010.
Antibiotic resistance characteristics of environmental bacteria from an
oxytetracycline production wastewater treatment plant and the receiving
river. Appl Environ Microbiol 76:3444-3451.
[23] Joseph, S.W., Hayes, J.R., English, L.L., Carr, L.E., and Wagner, D.D.
2001. Implications of multiple antimicrobial-resistant enterococci
associated with the poultry environment. Food Addit Contam
18:1118-1123.
[24] Hammerum, A.M., Lester, C.H., and Heuer, O.E. 2010.
Antimicrobial-resistant enterococci in animals and meat: a human health
hazard? Foodborne Pathog Dis 7:1137-1146.
[25] Heuer, O.E., Hammerum, A.M., Collignon, P., and Wegener, H.C. 2006.
Human health hazard from antimicrobial-resistant enterococci in animals
and food. Clin Infect Dis 43:911-916.
[26] Butaye, P., Devriese, L.A., Goossens, H., Ieven, M., and Haesebrouck, F.
1999. Enterococci with acquired vancomycin resistance in pigs and
chickens of different age groups. Antimicrob Agents Chemother
43:365-366.
[27] Butaye, P., Devriese, L.A., and Haesebrouck, F. 1999. Comparison of
direct and enrichment methods for the selective isolation of
vancomycin-resistant enterococci from feces of pigs and poultry. Microb
Drug Resist 5:131-134.
[28] Bates, J. 1997. Epidemiology of vancomycin-resistant enterococci in the
community and the relevance of farm animals to human infection. J Hosp
Infect 37:89-101.
[29] Bates, J., Jordens, J.Z., and Griffiths, D.T. 1994. Farm animals as a
putative reservoir for vancomycin-resistant enterococcal infection in man.
J Antimicrob Chemother 34:507-514.
[30] Knapp, C.W., Engemann, C.A., Hanson, M.L., Keen, P.L., Hall, K.J., and
Graham, D.W. 2008. Indirect evidence of transposon-mediated selection
of antibiotic resistance genes in aquatic systems at low-level
oxytetracycline exposures. Environ Sci Technol 42:5348-5353.
[31] Fan, C., Lee, P.K., Ng, W.J., Alvarez-Cohen, L., Brodie, E.L., Andersen,
G.L., and He, J. 2009. Influence of trace erythromycin and
eryhthromycin-H2O on carbon and nutrients removal and on resistance
selection in sequencing batch reactors (SBRs). Appl Microbiol Biotechnol
85:185-195.
[32] Esiobu, N., Armenta, L., and Ike, J. 2002. Antibiotic resistance in soil and
water environments. Int J Environ Health Res 12:133-144.
[33] Biyela, P.T., Lin, J., and Bezuidenhout, C.C. 2004. The role of aquatic
ecosystems as reservoirs of antibiotic resistant bacteria and antibiotic
resistance genes. Water Sci Technol 50:45-50.
[34] Schwartz, T., Kohnen, W., Jansen, B., and Obst, U. 2003. Detection of
antibiotic-resistant bacteria and their resistance genes in wastewater,
surface water, and drinking water biofilms. FEMS Microbiol Ecol
43:325-335.
@article{"International Journal of Biological, Life and Agricultural Sciences:53057", author = "Hyunjin Rho and Bongjin Shin and Okbok Lee and Yu-Hyun Choi and Jiyoung Lee and Jaerang Rho", title = "Antibiotic Resistance Profile of Bacterial Isolates from Animal Farming Aquatic Environments and Meats in a Peri-Urban Community in South Korea", abstract = "The increasing usage of antibiotics in the animal
farming industry is an emerging worldwide problem contributing to
the development of antibiotic resistance. The purpose of this work was
to investigate the prevalence and antibiotic resistance profile of
bacterial isolates collected from aquatic environments and meats in a
peri-urban community in Daejeon, Korea. In an antibacterial
susceptibility test, the bacterial isolates showed a high incidence of
resistance (~ 26.04 %) to cefazolin, tetracycline, gentamycin,
norfloxacin, erythromycin and vancomycin. The results from a test for
multiple antibiotic resistance indicated that the isolates were
displaying an approximately 5-fold increase in the incidence of
multiple antibiotic resistance to combinations of two different
antibiotics compared to combinations of three or more antibiotics.
Most of the isolates showed multi-antibiotic resistance, and the
resistance patterns were similar among the sampling groups.
Sequencing data analysis of 16S rRNA showed that most of the
resistant isolates appeared to be dominated by the classes
Betaproteobacteria and Gammaproteobacteria in the phylum
Proteobacteria.", keywords = "Antibiotics, Antibiotic resistance, Antimicrobial
resistance, Multi-resistance", volume = "5", number = "12", pages = "891-6", }
