Fertilizing with Animal Manure Disseminates Antibiotic Resistance Genes to the Farm Environment.

The dissemination of antibiotic resistance genes to the environment is an important factor causing increased prevalence of resistant pathogens. Manure is an important fertilizer, but it contains diverse resistance genes. Therefore, its application to fields may lead to increased abundance of resistance genes in the environment. Farming environments exposed to animal manure have not been studied extensively in countries with comparably low antibiotic use, such as Finland. The effects of manure storage and application to fields on the abundance of resistance genes were studied on two dairy cattle farms and two swine farms in southern Finland. Samples were taken from farms during the 2013 cropping season. Copy numbers of carbapenem (), sulfonamide (), and tetracycline () resistance genes were measured with quantitative polymerase chain reaction, and the data were analyzed using linear mixed models. The relative abundance of antibiotic resistance genes increased about fourfold in soil after manure application. Carbapenemase encoding was detected on all of the studied farms, which indicated that the gene is dispersed in the farm environment. The relative abundance of antibiotic resistance genes increased in stored manure compared with fresh manure roughly fivefold. This study shows that antibiotic resistance genes are disseminated on Finnish production animal farms. The spreading of resistance genes in farm-associated environments could possibly be limited by experimenting with new manure handling methods that could reduce the abundance of the genes in manure used for land application.

[1]  M. Braga,et al.  Exploratory Data Analysis , 2018, Encyclopedia of Social Network Analysis and Mining. 2nd Ed..

[2]  susan E. Aiello,et al.  The Merck Veterinary Manual , 2016 .

[3]  D. Bates,et al.  Linear Mixed-Effects Models using 'Eigen' and S4 , 2015 .

[4]  A. Pruden,et al.  Elevation of antibiotic resistance genes at cold temperatures: implications for winter storage of sludge and biosolids , 2014, Letters in applied microbiology.

[5]  C. Ying,et al.  Prevalence of sulfonamide-resistant bacteria, resistance genes and integron-associated horizontal gene transfer in natural water bodies and soils adjacent to a swine feedlot in northern Taiwan. , 2014, Journal of hazardous materials.

[6]  S. Solomon,et al.  Antibiotic resistance threats in the United States: stepping back from the brink. , 2014, American family physician.

[7]  L. Sandegren,et al.  Selection of antibiotic resistance at very low antibiotic concentrations , 2014, Upsala journal of medical sciences.

[8]  P. Higgins,et al.  Worldwide dissemination of acquired carbapenem-hydrolysing class D β-lactamases in Acinetobacter spp. other than Acinetobacter baumannii. , 2014, International journal of antimicrobial agents.

[9]  T. Pasanen,et al.  Rapid Molecular Characterization of Acinetobacter baumannii Clones with rep-PCR and Evaluation of Carbapenemase Genes by New Multiplex PCR in Hospital District of Helsinki and Uusimaa , 2014, PloS one.

[10]  Bodo Winter,et al.  Linear models and linear mixed effects models in R with linguistic applications , 2013, ArXiv.

[11]  Timothy A. Johnson,et al.  Diverse and abundant antibiotic resistance genes in Chinese swine farms , 2013, Proceedings of the National Academy of Sciences.

[12]  K. Poole Bacterial stress responses as determinants of antimicrobial resistance. , 2012, The Journal of antimicrobial chemotherapy.

[13]  K. Gibson,et al.  Measuring and mitigating inhibition during quantitative real time PCR analysis of viral nucleic acid extracts from large-volume environmental water samples. , 2012, Water research.

[14]  G. Dantas,et al.  The Shared Antibiotic Resistome of Soil Bacteria and Human Pathogens , 2012, Science.

[15]  S. Levy,et al.  Food Animals and Antimicrobials: Impacts on Human Health , 2011, Clinical Microbiology Reviews.

[16]  Hadley Wickham,et al.  The Split-Apply-Combine Strategy for Data Analysis , 2011 .

[17]  M. Schloter,et al.  Accumulation of Sulfonamide Resistance Genes in Arable Soils Due to Repeated Application of Manure Containing Sulfadiazine , 2011, Applied and Environmental Microbiology.

[18]  Satoru Suzuki,et al.  Tetracycline resistance genes persist at aquaculture farms in the absence of selection pressure. , 2011, Environmental science & technology.

[19]  Heather K. Allen,et al.  Call of the wild: antibiotic resistance genes in natural environments , 2010, Nature Reviews Microbiology.

[20]  A. Pühler,et al.  Detection of 140 clinically relevant antibiotic-resistance genes in the plasmid metagenome of wastewater treatment plant bacteria showing reduced susceptibility to selected antibiotics. , 2009, Microbiology.

[21]  S. Koike,et al.  Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. , 2009, Journal of environmental quality.

[22]  V. Beneš,et al.  The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. , 2009, Clinical chemistry.

[23]  F. Baquero,et al.  Antibiotics and antibiotic resistance in water environments. , 2008, Current opinion in biotechnology.

[24]  Mark Johnson,et al.  NCBI BLAST: a better web interface , 2008, Nucleic Acids Res..

[25]  Sudeshna Ghosh,et al.  The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria , 2007, The ISME Journal.

[26]  Xian-Zhi Li,et al.  β-Lactam resistance and β-lactamases in bacteria of animal origin , 2007 .

[27]  W. Seinen,et al.  Tetracyclines and Tetracycline Resistance in Agricultural Soils: Microcosm and Field Studies , 2006, Microbial Ecology.

[28]  P. Nordmann,et al.  OXA-58, a Novel Class D β-Lactamase Involved in Resistance to Carbapenems in Acinetobacter baumannii , 2005, Antimicrobial Agents and Chemotherapy.

[29]  S. Levy,et al.  Antibacterial resistance worldwide: causes, challenges and responses , 2004, Nature Medicine.

[30]  M. Cotta,et al.  Isolation, characterization and comparison of bacteria from swine faeces and manure storage pits. , 2003, Environmental microbiology.

[31]  Kathleen A. Smith,et al.  Antimicrobial residues in animal waste and water resources proximal to large-scale swine and poultry feeding operations. , 2002, The Science of the total environment.

[32]  W. Witte Ecological impact of antibiotic use in animals on different complex microflora: environment. , 2000, International journal of antimicrobial agents.

[33]  F. Baquero,et al.  Antibiotic-selective environments. , 1998, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[34]  F. Aarestrup,et al.  Avoparcin used as a growth promoter is associated with the occurrence of vancomycin-resistant Enterococcus faecium on Danish poultry and pig farms. , 1997, Preventive veterinary medicine.

[35]  J. Davies,et al.  Origins and Evolution of Antibiotic Resistance , 1996, Microbiology and Molecular Biology Reviews.

[36]  A. Uitterlinden,et al.  Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA , 1993, Applied and environmental microbiology.

[37]  D. M. Ward,et al.  16S rRNA sequences reveal numerous uncultured microorganisms in a natural community , 1990, Nature.

[38]  H. Blöcker,et al.  Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. , 1989, Nucleic acids research.

[39]  J. Mcgowan,et al.  Antimicrobial resistance in hospital organisms and its relation to antibiotic use. , 1983, Reviews of infectious diseases.

[40]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[41]  Cedric E. Ginestet ggplot2: Elegant Graphics for Data Analysis , 2011 .

[42]  G. Owens,et al.  Occurrence and Environmental Fate of Veterinary Antibiotics in the Terrestrial Environment , 2011 .

[43]  A. Andremont Commensal Flora May Play Key Role in Spreading Antibiotic Resistance We need to learn more about commensal flora if we are to better manage this particular window of vulnerability to antibiotic resistance , 2003 .