Resistance to Change: AMR Gene Dynamics on a Commercial Pig Farm with High Antimicrobial Usage

Overview

Journal Sci Rep

Specialty Science

Date 2020 Feb 5

PMID 32015392

Citations 23

Authors

Jolinda Pollock

Adrian Muwonge

Michael R Hutchings

Geoffrey Mainda

Barend M Bronsvoort

David L Gally

Alexander Corbishley

Affiliations

Soon will be listed here.

Abstract

Group antimicrobial administration is used to control disease in livestock, but we have little insight into how this impacts antimicrobial resistance (AMR) gene dynamics. Here, a longitudinal study was carried out during a single production cycle on a commercial pig unit with high historic and current antimicrobial usage. Quantitative PCR, 16S rRNA gene metabarcoding and shotgun metagenomic sequencing were used to track faecal AMR gene abundance and diversity and microbiome alpha diversity. Shotgun metagenomic sequencing identified 144 AMR genes in total, with higher AMR gene diversity present in young pigs compared to dry sows. Irrespective of in-feed antibiotic treatment or changes in microbiome diversity, mean AMR gene copy number was consistently high, with some AMR genes present at copy numbers comparable to the bacterial 16S rRNA gene. In conclusion, AMR gene prevalence and abundance were not influenced by antibiotic use, either during the production cycle or following whole-herd medication. The high levels of certain genes indicate they are widely disseminated throughout the microbial population, potentially aiding stability. Despite the high and relatively stable levels of resistance genes against the main antimicrobials used, these compounds continue to control production limiting diseases on this unit.

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References

Singer R, Reid-Smith R, Sischo W . Stakeholder position paper: epidemiological perspectives on antibiotic use in animals. Prev Vet Med. 2005; 73(2-3):153-61. DOI: 10.1016/j.prevetmed.2005.09.019. View

Novais C, Freitas A, Silveira E, Antunes P, Silva R, Coque T . Spread of multidrug-resistant Enterococcus to animals and humans: an underestimated role for the pig farm environment. J Antimicrob Chemother. 2013; 68(12):2746-54. DOI: 10.1093/jac/dkt289. View

Smith T, Gebreyes W, Abley M, Harper A, Forshey B, Male M . Methicillin-resistant Staphylococcus aureus in pigs and farm workers on conventional and antibiotic-free swine farms in the USA. PLoS One. 2013; 8(5):e63704. PMC: 3646818. DOI: 10.1371/journal.pone.0063704. View

Khanna T, Friendship R, Dewey C, Weese J . Methicillin resistant Staphylococcus aureus colonization in pigs and pig farmers. Vet Microbiol. 2007; 128(3-4):298-303. DOI: 10.1016/j.vetmic.2007.10.006. View

Su J, Wei B, Ou-Yang W, Huang F, Zhao Y, Xu H . Antibiotic resistome and its association with bacterial communities during sewage sludge composting. Environ Sci Technol. 2015; 49(12):7356-63. DOI: 10.1021/acs.est.5b01012. View

Calero-Caceres W, Melgarejo A, Colomer-Lluch M, Stoll C, Lucena F, Jofre J . Sludge as a potential important source of antibiotic resistance genes in both the bacterial and bacteriophage fractions. Environ Sci Technol. 2014; 48(13):7602-11. DOI: 10.1021/es501851s. View

Lugsomya K, Yindee J, Niyomtham W, Tribuddharat C, Tummaruk P, Hampson D . Antimicrobial Resistance in Commensal Escherichia coli Isolated from Pigs and Pork Derived from Farms Either Routinely Using or Not Using In-Feed Antimicrobials. Microb Drug Resist. 2018; 24(7):1054-1066. PMC: 6154756. DOI: 10.1089/mdr.2018.0154. View

Chantziaras I, Boyen F, Callens B, Dewulf J . Correlation between veterinary antimicrobial use and antimicrobial resistance in food-producing animals: a report on seven countries. J Antimicrob Chemother. 2013; 69(3):827-34. DOI: 10.1093/jac/dkt443. View

Bednorz C, Oelgeschlager K, Kinnemann B, Hartmann S, Neumann K, Pieper R . The broader context of antibiotic resistance: zinc feed supplementation of piglets increases the proportion of multi-resistant Escherichia coli in vivo. Int J Med Microbiol. 2013; 303(6-7):396-403. DOI: 10.1016/j.ijmm.2013.06.004. View

10.

Cavaco L, Hasman H, Stegger M, Andersen P, Skov R, Fluit A . Cloning and occurrence of czrC, a gene conferring cadmium and zinc resistance in methicillin-resistant Staphylococcus aureus CC398 isolates. Antimicrob Agents Chemother. 2010; 54(9):3605-8. PMC: 2934997. DOI: 10.1128/AAC.00058-10. View

11.

Aarestrup F, Cavaco L, Hasman H . Decreased susceptibility to zinc chloride is associated with methicillin resistant Staphylococcus aureus CC398 in Danish swine. Vet Microbiol. 2009; 142(3-4):455-7. DOI: 10.1016/j.vetmic.2009.10.021. View

12.

Quintana-Hayashi M, Thakur S . Longitudinal study of the persistence of antimicrobial-resistant campylobacter strains in distinct Swine production systems on farms, at slaughter, and in the environment. Appl Environ Microbiol. 2012; 78(8):2698-705. PMC: 3318812. DOI: 10.1128/AEM.07723-11. View

13.

Medardus J, Molla B, Nicol M, Morrow W, Rajala-Schultz P, Kazwala R . In-feed use of heavy metal micronutrients in U.S. swine production systems and its role in persistence of multidrug-resistant salmonellae. Appl Environ Microbiol. 2014; 80(7):2317-25. PMC: 3993138. DOI: 10.1128/AEM.04283-13. View

14.

Amachawadi R, Shelton N, Shi X, Vinasco J, Dritz S, Tokach M . Selection of fecal enterococci exhibiting tcrB-mediated copper resistance in pigs fed diets supplemented with copper. Appl Environ Microbiol. 2011; 77(16):5597-603. PMC: 3165251. DOI: 10.1128/AEM.00364-11. View

15.

Birkegard A, Halasa T, Folkesson A, Clasen J, Graesboll K, Toft N . Persistence of antimicrobial resistance genes from sows to finisher pigs. Prev Vet Med. 2018; 149:10-14. DOI: 10.1016/j.prevetmed.2017.11.007. View

16.

Munk P, Knudsen B, Lukjancenko O, Duarte A, Van Gompel L, Luiken R . Abundance and diversity of the faecal resistome in slaughter pigs and broilers in nine European countries. Nat Microbiol. 2018; 3(8):898-908. DOI: 10.1038/s41564-018-0192-9. View

17.

Burow E, Simoneit C, Tenhagen B, Kasbohrer A . Oral antimicrobials increase antimicrobial resistance in porcine E. coli--a systematic review. Prev Vet Med. 2014; 113(4):364-75. DOI: 10.1016/j.prevetmed.2013.12.007. View

18.

Pollock J, Gally D, Glendinning L, Tiwari R, Hutchings M, Houdijk J . Analysis of temporal fecal microbiota dynamics in weaner pigs with and without exposure to enterotoxigenic Escherichia coli1,2. J Anim Sci. 2018; 96(9):3777-3790. PMC: 6127793. DOI: 10.1093/jas/sky260. View

19.

Schloss P, Westcott S, Ryabin T, Hall J, Hartmann M, Hollister E . Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol. 2009; 75(23):7537-41. PMC: 2786419. DOI: 10.1128/AEM.01541-09. View

20.

Leranth C, Hamori J . "Dark" Purkinje cells of the cerebellar cortex. Acta Biol Acad Sci Hung. 1970; 21(4):405-19. View