Prevalence of extended-spectrum β-lactamases in the local farm environment and livestock: challenges to mitigate antimicrobial resistance

Figures & data

Table 1. Reported occurrences of ESBL-producing bacteria in livestock-related environmental niches.

Source	Effects	Reference
Soil
Soil near farm	18.3% of ESBLs (22/120) in soil located cattle farms	(Hartmann et al. 2012)
Intensive, extensive and organic soils	A positive correlation between AR and intensive soil	(Jones-Dias et al. 2016)
Undisturbed area	Isolation of the bacteria resistant to extended-spectrum β-lactams without selective pressure	(Upadhyay et al. 2016)
Manure
Cattle manure	A higher frequency of resistant bacteria in manure-amended soil	(Udikovic-Kolic et al. 2014)
Dairy cow manure	Identification of the multiple resistance genes including a novel clade of resistant gene	(Wichmann et al. 2014)
Cattle, swine, and chicken manure	Higher concentration of the veterinary antibiotic residues in swine and chicken than cattle manure	(Hou et al. 2015)
Water
Water supply in farm	Isolation of the ESBL-producing E. coli carrying TEM and CMY-2 genes (6/116, 5%)	(Hinthong et al. 2017)
Drinking water in a cattle pen	ESBLs, carbapenemase, and unique ARGs in the water trough	(Noyes et al. 2016)
Surface/wastewater	A higher prevalence of ESBLs in wastewater than surface water (27% (9/33) and 6.2% (7/113))	(Blaak et al. 2015)
Surface/wastewater	Higher ESBLs in wastewater than surface water (42.1% (24/57) and 1.7% (1/57))	(Said et al. 2016)
Surface water	High prevalence of ESBLs in surface water	(Zurfluh et al. 2013; Haque et al. 2014)
Air
Cattle farms	Isolation of a multidrug-resistant strain in both inside and outside air	(Navajas-Benito et al. 2017)
Swine farms	Occurrence of ESBL-producing E. coli from inside and outside air of the swine farms	(Gao et al. 2015)
Broiler farms	Fecal and airborne transfer of ESBL-producing bacteria	(Laube et al. 2014)
Wild animals
Songbirds on dairies	5.1% prevalence of CTX-M gene in wild songbirds on Ohio dairies	(Mathys et al. 2017)
Coastline birds	14% of prevalence of ESBLs in wild birds from Miami Beach, Florida	(Poirel et al. 2012)
Wild birds	A higher prevalence of ESBLs in cattle egret than other wild birds	(Hasan et al. 2016)
Flies	ESBL-producers from 9.1% of flies (123/1346) in urban and rural areas	(Schaumburg et al. 2016)
Flies	Isolation of ESBL-producing E. coli in flies at poultry farms (10.5%, 2/19) and cattle farms (12%, 20/159)	(Blaak et al. 2014; Usui et al. 2013)
Others	Investigation of diverse wild animals as important carriers of ESBLs	(Nhung et al. 2015; Cristóvão et al. 2017; Garcês et al. 2019; Schaufler et al. 2018; Wasyl et al. 2018)
Human
Human in a livestock-dense area	Identification of risk factors for ESBL/AmpC transmission	(Wielders et al. 2017)
Farmers	Identical MLST and CTX-M gene between human and cattle isolates from the same farm	(Dahms et al. 2015)
Farm workers	Isolation of ESBL-producing E. coli from cattle and farm workers	(Tamang et al. 2013)
Farm workers	Similar ESBL gene types and identical MLST and plasmid types between human and pig isolates within the same farm	(Dohmen et al. 2015)
Slaughterhouse workers	Association between the job title in the slaughterhouse and the prevalence of ESBL-E. coli in human	(Dohmen W et al. 2017b)
Others
Dust from a cattle farm	ESBL-producing E. coli from 15.4% (18/117) of dust from mixed and beef cattle farms	(Schmid et al. 2013)
Feed mixer, animal feed, bedding	ESBL-producing E. coli from water trough, feed mixer, feed, and bedding in dairy farms contained	(Braun et al. 2016)

Figure 1. Potential transmission routes of the ESBL genes and ESBL-producing bacteria at the interfaces of livestock and the environment. ESBL-producing bacteria in livestock can naturally occur and transmit through the environmental sources, such as manure, soil, water, air, wildlife, and human (especially farm workers) by horizontal gene transfer of the ESBL genes in chromosomal DNA and on plasmids medicated by IS elements or bacterial transmission.

Hartmann A, Amoureux L, Locatelli A, Depret G, Jolivet C, Gueneau E, Neuwirth C. 2012. Occurrence of CTX-M producing Escherichia coli in soils, cattle, and farm environment in France (Burgundy region). Front Microbiol. 3:83

 PubMed Web of Science ®Google Scholar

Jones-Dias D, Manageiro V, Caniça M. 2016. Influence of agricultural practice on mobile bla genes: IncI1‐bearing CTX‐M. Environ Microbiol. 18:260–272.

 PubMed Web of Science ®Google Scholar

Upadhyay S, Mustafa M, Joshi S. 2016. Naturally evolving extended spectrum cephalosporin resistance in soil borne isolates of Enterobacteriaceae. Natl Acad Sci Lett. 39(3):181–184.

 Web of Science ®Google Scholar

Udikovic-Kolic N, Wichmann F, Broderick NA, Handelsman J. 2014. Bloom of resident antibiotic-resistant bacteria in soil following manure fertilization. Proc Natl Acad Sci Usa. 111(42):15202–15207.

 PubMed Web of Science ®Google Scholar

Wichmann F, Udikovic-Kolic N, Andrew S, Handelsman J. 2014. Diverse antibiotic resistance genes in dairy cow manure. MBio. 5(2):e01017–01013.

 PubMed Web of Science ®Google Scholar

Hou J, Wan W, Mao D, Wang C, Mu Q, Qin S, Luo Y. 2015. Occurrence and distribution of sulfonamides, tetracyclines, quinolones, macrolides, and nitrofurans in livestock manure and amended soils of Northern China. Environ Sci Pollut Res Int. 22(6):4545–4554.

 PubMed Web of Science ®Google Scholar

Hinthong W, Pumipuntu N, Santajit S, Kulpeanprasit S, Buranasinsup S, Sookrung N, Chaicumpa W, Aiumurai P, Indrawattana N. 2017. Detection and drug resistance profile of Escherichia coli from subclinical mastitis cows and water supply in dairy farms in Saraburi Province, Thailand. PeerJ. 5:e3431.

 PubMed Web of Science ®Google Scholar

Noyes NR, Yang X, Linke LM, Magnuson RJ, Dettenwanger A, Cook S, Geornaras I, Woerner DE, Gow SP, McAllister TA, et al. 2016. Resistome diversity in cattle and the environment decreases during beef production. Elife. 5:e13195.

 PubMed Web of Science ®Google Scholar

Blaak H, Lynch G, Italiaander R, Hamidjaja RA, Schets FM, de Roda Husman AM. 2015. Multidrug-resistant and extended spectrum beta-lactamase-producing Escherichia coli in Dutch surface water and wastewater. PLoS One. 10(6):e0127752.

 PubMed Web of Science ®Google Scholar

Said LB, Jouini A, Alonso CA, Klibi N, Dziri R, Boudabous A, Slama KB, Torres C. 2016. Characteristics of extended-spectrum β-lactamase (ESBL)-and pAmpC beta-lactamase-producing Enterobacteriaceae of water samples in Tunisia. Sci Total Environ. 550:1103–1109.

 PubMed Web of Science ®Google Scholar

Zurfluh K, Hächler H, Nüesch-Inderbinen M, Stephan R. 2013. Characteristics of extended-spectrum beta-lactamase (ESBL)-and carbapenemase-producing Enterobacteriaceae isolated from rivers and lakes in Switzerland. Appl Environ Microbiol. 79(9):3021–3026.

 PubMed Web of Science ®Google Scholar

Haque A, Yoshizumi A, Saga T, Ishii Y, Tateda K. 2014. ESBL-producing Enterobacteriaceae in environmental water in Dhaka, Bangladesh. J Infect Chemother. 20(11):735–737.

 PubMed Web of Science ®Google Scholar

Navajas-Benito EV, Alonso CA, Sanz S, Olarte C, Martínez-Olarte R, Hidalgo-Sanz S, Somalo S, Torres C. 2017. Molecular characterization of antibiotic resistance in Escherichia coli strains from a dairy cattle farm and its surroundings. J Sci Food Agric. 97:362–365.

 PubMed Web of Science ®Google Scholar

Gao L, Tan Y, Zhang X, Hu J, Miao Z, Wei L, Chai T. 2015. Emissions of Escherichia coli carrying extended-spectrum β-lactamase resistance from pig farms to the surrounding environment. IJERPH. 12(4):4203–4213.

 Google Scholar

Laube H, Friese A, Von Salviati C, Guerra B, Rösler U. 2014. Transmission of ESBL/AmpC-producing Escherichia coli from broiler chicken farms to surrounding areas. Vet Microbiol. 172(3–4):519–527.

 PubMed Web of Science ®Google Scholar

Mathys DA, Mathys BA, Mollenkopf DF, Daniels JB, Wittum TE. 2017. Enterobacteriaceae harboring AmpC (blaCMY) and ESBL (blaCTX-M) in migratory and nonmigratory wild songbird populations on Ohio dairies. Vector Borne Zoonotic Dis. 17(4):254–259.

 PubMed Web of Science ®Google Scholar

Poirel L, Potron A, De La Cuesta C, Cleary T, Nordmann P, Munoz-Price LS. 2012. Wild coastline birds as reservoirs of broad-spectrum β-lactamase-producing Enterobacteriaceae, Miami Beach. Antimicrob Agents Chemother. 56(5):2756–2758.

 PubMed Web of Science ®Google Scholar

Hasan B, Laurell K, Rakib MM, Ahlstedt E, Hernandez J, Caceres M, Järhult JD. 2016. Fecal carriage of extended-spectrum β-lactamases in healthy humans, poultry, and wild birds in León, Nicaragua—a shared pool of blaCTX-M genes and possible interspecies clonal spread of extended-spectrum β-lactamases-producing Escherichia coli. Microb Drug Resist. 22(8):682–687.

 PubMed Web of Science ®Google Scholar

Schaumburg F, Onwugamba FC, Akulenko R, Peters G, Mellmann A, Köck R, Becker K. 2016. A geospatial analysis of flies and the spread of antimicrobial resistant bacteria. Int J Med Microbiol. 306(7):566–571.

 PubMed Web of Science ®Google Scholar

Blaak H, Hamidjaja RA, van Hoek AH, de Heer L, de Roda Husman AM, Schets FM. 2014. Detection of ESBL-producing Escherichia coli on flies at poultry farms. Appl Environ Microbiol. 80(1):239–246.

 PubMed Web of Science ®Google Scholar

Usui M, Iwasa T, Fukuda A, Sato T, Okubo T, Tamura Y. 2013. The role of flies in spreading the extended-spectrum β-lactamase gene from cattle. Microb Drug Resist. 19(5):415–420.

 PubMed Web of Science ®Google Scholar

Nhung NT, Cuong NV, Campbell J, Hoa NT, Bryant JE, Truc VNT, Kiet BT, Jombart T, Trung NV, Hien VB, et al. 2015. High levels of antimicrobial resistance among Escherichia coli isolates from livestock farms and synanthropic rats and shrews in the Mekong Delta of Vietnam. Appl Environ Microbiol. 81(3):812–820.

 PubMed Web of Science ®Google Scholar

Cristóvão F, Alonso CA, Igrejas G, Sousa M, Silva V, Pereira JE, Lozano C, Cortés-Cortés G, Torres C, Poeta P. 2017. Clonal diversity of extended-spectrum beta-lactamase producing Escherichia coli isolates in fecal samples of wild animals. FEMS Microbiol Lett. 364:fnx039.

 Web of Science ®Google Scholar

Garcês A, Correia S, Amorim F, Pereira JE, Igrejas G, Poeta P. 2019. First report on extended-spectrum beta-lactamase (ESBL) producing Escherichia coli from European free-tailed bats (Tadarida teniotis) in Portugal: a one-health approach of a hidden contamination problem. J Hazard Mater. 370:219–224.

 PubMed Web of Science ®Google Scholar

Schaufler K, Nowak K, Düx A, Semmler T, Villa L, Kourouma L, Bangoura K, Wieler LH, Leendertz FH, Guenther S. 2018. Clinically relevant ESBL-producing K. pneumoniae ST307 and E. coli ST38 in an urban west African rat population. Front Microbiol. 9:150.

 PubMed Web of Science ®Google Scholar

Wasyl D, Zając M, Lalak A, Skarżyńska M, Samcik I, Kwit R, Jabłoński A, Bocian Ł, Woźniakowski G, Hoszowski A, et al. 2018. Antimicrobial resistance in Escherichia coli isolated from wild animals in Poland. Microb Drug Resist. 24(6):807–815.

 PubMed Web of Science ®Google Scholar

Wielders CCH, van Hoek AHAM, Hengeveld PD, Veenman C, Dierikx CM, Zomer TP, Smit LAM, van der Hoek W, Heederik DJ, de Greeff SC, et al. 2017. Extended-spectrum β-lactamase-and pAmpC-producing Enterobacteriaceae among the general population in a livestock-dense area. Clin Microbiol Infect. 23(2):120.e1–e8.

 Web of Science ®Google Scholar

Dahms C, Hübner N-O, Kossow A, Mellmann A, Dittmann K, Kramer A. 2015. Occurrence of ESBL-producing Escherichia coli in livestock and farm workers in Mecklenburg-Western Pomerania, Germany. PLoS One. 10(11):e0143326.

 PubMed Web of Science ®Google Scholar

Tamang MD, Nam HM, Gurung M, Jang GC, Kim SR, Jung SC, Park YH, Lim SK. 2013. Molecular characterization of CTX-M β-lactamase and associated addiction systems in Escherichia coli circulating among cattle, farm workers, and farm environment. Appl Environ Microbiol. 79(13):3898–3905.

 PubMed Web of Science ®Google Scholar

Dohmen W, Bonten MJ, Bos ME, van Marm S, Scharringa J, Wagenaar JA, Heederik DJ. 2015. Carriage of extended-spectrum β-lactamases in pig farmers is associated with occurrence in pigs. Clin Microbiol Infect. 21(10):917–923.

 PubMed Web of Science ®Google Scholar

Dohmen W, Schmitt H, Bonten M, Heederik D. 2017. Air exposure as a possible route for ESBL in pig farmers. Environ Res. 155:359–364.

 PubMed Web of Science ®Google Scholar

Schmid A, Hörmansdorfer S, Messelhäusser U, Käsbohrer A, Sauter-Louis C, Mansfeld R. 2013. Prevalence of extended-spectrum β-lactamases producing Escherichia coli on Bavarian dairy and beef cattle farms. Appl Environ Microbiol. 79(9):3027–3032.

 PubMed Web of Science ®Google Scholar

Braun SD, Ahmed MF, El-Adawy H, Hotzel H, Engelmann I, Weiß D, Monecke S, Ehricht R. 2016. Surveillance of extended-spectrum beta-lactamase-producing Escherichia coli in dairy cattle farms in the Nile Delta, Egypt. Front Microbiol. 7:1020

 PubMed Web of Science ®Google Scholar