Skip to main content
Top
Published in: Gut Pathogens 1/2015

Open Access 01-12-2015 | Short Report

High dietary zinc supplementation increases the occurrence of tetracycline and sulfonamide resistance genes in the intestine of weaned pigs

Authors: Wilfried Vahjen, Dominika Pietruszyńska, Ingo C. Starke, Jürgen Zentek

Published in: Gut Pathogens | Issue 1/2015

Login to get access

Abstract

Background

Dietary zinc oxide is used in pig nutrition to combat post weaning diarrhoea. Recent data suggests that high doses (2.5 g/kg feed) increase the bacterial antibiotic resistance development in weaned pigs. Therefore, the aim of this study was to investigate the development of enterobacterial antibiotic resistance genes in the intestinal tract of weaned pigs.

Findings

Weaned pigs were fed diets for 4 weeks containing 57 (low), 164 (intermediate) or 2425 (high) mg kg−1 analytical grade ZnO. DNA extracts from stomach, mid-jejunum, terminal ileum and colon ascendens were amplified by qPCR assays to quantify copy numbers for the tetracycline (tetA) and sulfonamide (sul1) resistance genes in Gram-negative bacteria. Overall, the combined data (n = 336) showed that copy numbers for tetracycline and sulfonamide resistance genes were significantly increased in the high zinc treatment compared to the low (tetA: p value < 10−6; sul1: p value = 1 × 10−5) or intermediate (tetA: P < 1.6 × 10−4; sul1: P = 3.2 × 10−4) zinc treatment. Regarding the time dependent development, no treatment effects were seen 1 week after weaning, but significant differences between high and low/intermediate zinc treatments evolved 2 weeks after weaning. The increased number of tetA and sul1 copies was not confined to the hind gut, but was already present in stomach contents.

Conclusions

The results of this study suggest that the use of high doses of dietary zinc beyond 2 weeks after weaning should be avoided in pigs due to the possible increase of antibiotic resistance in Gram-negative bacteria.
Appendix
Available only for authorised users
Literature
1.
go back to reference Pettigrew JE (2006) Reduced use of antibiotic growth promoters in diets fed to weanling pigs; dietary tools, part 1. Anim Biotechnol 17:207–215CrossRefPubMed Pettigrew JE (2006) Reduced use of antibiotic growth promoters in diets fed to weanling pigs; dietary tools, part 1. Anim Biotechnol 17:207–215CrossRefPubMed
2.
go back to reference Starke IC, Pieper R, Neumann K, Zentek J, Vahjen W (2014) The impact of high dietary zinc oxide on the development of the intestinal microbiota in weaned piglets. FEMS Microbiol Ecol 87:416–427CrossRefPubMed Starke IC, Pieper R, Neumann K, Zentek J, Vahjen W (2014) The impact of high dietary zinc oxide on the development of the intestinal microbiota in weaned piglets. FEMS Microbiol Ecol 87:416–427CrossRefPubMed
3.
go back to reference Vahjen W, Pieper R, Zentek J (2010) Bar-coded pyrosequencing of 16S rRNA gene amplicons reveals changes in ileal porcine bacterial communities due to high dietary zinc intake. Appl Environ Microbiol 76:6689–6691PubMedCentralCrossRefPubMed Vahjen W, Pieper R, Zentek J (2010) Bar-coded pyrosequencing of 16S rRNA gene amplicons reveals changes in ileal porcine bacterial communities due to high dietary zinc intake. Appl Environ Microbiol 76:6689–6691PubMedCentralCrossRefPubMed
4.
go back to reference Broom LJ, Miller HM, Kerr KG, Knapp JS (2006) Effects of zinc oxide and Enterococcus faecium SF68 dietary supplementation on the performance, intestinal microbiota and immune status of weaned piglets. Res Vet Sci 80:45–54CrossRefPubMed Broom LJ, Miller HM, Kerr KG, Knapp JS (2006) Effects of zinc oxide and Enterococcus faecium SF68 dietary supplementation on the performance, intestinal microbiota and immune status of weaned piglets. Res Vet Sci 80:45–54CrossRefPubMed
5.
go back to reference Hojberg O, Canibe N, Poulsen HD, Hedemann MS, Jensen BB (2005) Influence of dietary zinc oxide and copper sulfate on the gastrointestinal ecosystem in newly weaned piglets. Appl Environ Microb 71:2267–2277CrossRef Hojberg O, Canibe N, Poulsen HD, Hedemann MS, Jensen BB (2005) Influence of dietary zinc oxide and copper sulfate on the gastrointestinal ecosystem in newly weaned piglets. Appl Environ Microb 71:2267–2277CrossRef
6.
go back to reference Vahjen W, Pieper R, Zentek J (2011) Increased dietary zinc oxide changes the bacterial core and enterobacterial composition in the ileum of piglets. J Anim Sci 89:2430–2439CrossRefPubMed Vahjen W, Pieper R, Zentek J (2011) Increased dietary zinc oxide changes the bacterial core and enterobacterial composition in the ileum of piglets. J Anim Sci 89:2430–2439CrossRefPubMed
7.
go back to reference Bednorz C, Oelgeschläger K, Kinnemann B, Hartmann S, Neumann K, Pieper R, Bethe A, Semmler T, Tedin K, Schierack P, Wieler LH, Guenther S (2013) 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 303:396–403CrossRefPubMed Bednorz C, Oelgeschläger K, Kinnemann B, Hartmann S, Neumann K, Pieper R, Bethe A, Semmler T, Tedin K, Schierack P, Wieler LH, Guenther S (2013) 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 303:396–403CrossRefPubMed
9.
go back to reference Rayamajhi N, Cha SB, Kang ML, Lee SI, Lee HS, Yoo HS (2009) Inter- and intraspecies plasmid-mediated transfer of florfenicol resistance in Enterobacteriaceae isolates from swine. Appl Environ Microbiol 75:5700–5703PubMedCentralCrossRefPubMed Rayamajhi N, Cha SB, Kang ML, Lee SI, Lee HS, Yoo HS (2009) Inter- and intraspecies plasmid-mediated transfer of florfenicol resistance in Enterobacteriaceae isolates from swine. Appl Environ Microbiol 75:5700–5703PubMedCentralCrossRefPubMed
11.
go back to reference Martin L, Pieper R, Schunter N, Vahjen W, Zentek J (2013) Performance, organ zinc concentration, jejunal brush border membrane enzyme activities and mRNA expression in piglets fed with different levels of dietary zinc. Arch Anim Nutr 67:248–261CrossRefPubMed Martin L, Pieper R, Schunter N, Vahjen W, Zentek J (2013) Performance, organ zinc concentration, jejunal brush border membrane enzyme activities and mRNA expression in piglets fed with different levels of dietary zinc. Arch Anim Nutr 67:248–261CrossRefPubMed
12.
go back to reference Holzel CS, Muller C, Harms KS, Mikolajewski S, Schafer S, Schwaiger K, Bauer J (2012) Heavy metals in liquid pig manure in light of bacterial antimicrobial resistance. Environ Res 113:21–27CrossRefPubMed Holzel CS, Muller C, Harms KS, Mikolajewski S, Schafer S, Schwaiger K, Bauer J (2012) Heavy metals in liquid pig manure in light of bacterial antimicrobial resistance. Environ Res 113:21–27CrossRefPubMed
13.
go back to reference Cavaco LM, Hasman H, Aarestrup FM (2011) Zinc resistance of Staphylococcus aureus of animal origin is strongly associated with methicillin resistance. Vet Microbiol 150:344–348CrossRefPubMed Cavaco LM, Hasman H, Aarestrup FM (2011) Zinc resistance of Staphylococcus aureus of animal origin is strongly associated with methicillin resistance. Vet Microbiol 150:344–348CrossRefPubMed
16.
go back to reference Jacela JY, DeRouchey JM, Tokach MD, Goodband RD, Nelssen JL, Renter DG, Dritz SS (2010) Feed additives for swine: fact sheets—high dietary levels of copper and zinc for young pigs, and phytase. J Swine Health Prod 18:87–91 Jacela JY, DeRouchey JM, Tokach MD, Goodband RD, Nelssen JL, Renter DG, Dritz SS (2010) Feed additives for swine: fact sheets—high dietary levels of copper and zinc for young pigs, and phytase. J Swine Health Prod 18:87–91
17.
go back to reference Durosoy S. President of Anime, Sillingy, France. (2014) Personal communication on the use of zinc oxide in pig nutrition. Contact: sdurosoy@animine.eu Durosoy S. President of Anime, Sillingy, France. (2014) Personal communication on the use of zinc oxide in pig nutrition. Contact: sdurosoy@animine.eu
18.
go back to reference Speer BS, Shoemaker NB, Salyers AA (1992) Bacterial resistance to tetracycline: mechanisms, transfer, and clinical significance. Clin Microbiol Rev 5:387–399PubMedCentralPubMed Speer BS, Shoemaker NB, Salyers AA (1992) Bacterial resistance to tetracycline: mechanisms, transfer, and clinical significance. Clin Microbiol Rev 5:387–399PubMedCentralPubMed
20.
go back to reference Seiler C, Berendonk TU (2006) Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front Microbiol 3:399 Seiler C, Berendonk TU (2006) Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front Microbiol 3:399
21.
go back to reference Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV (2006) Co-selection of antibiotic and metal resistance. Trends Microbiol 14:176–182CrossRefPubMed Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV (2006) Co-selection of antibiotic and metal resistance. Trends Microbiol 14:176–182CrossRefPubMed
22.
23.
go back to reference Suckling CJ, Sweeney JR, Wood HC (1977) Dihydropteroate synthase: purification by affinity chromatography and mechanism of action. J Chem Soc Perk 4:439–442CrossRef Suckling CJ, Sweeney JR, Wood HC (1977) Dihydropteroate synthase: purification by affinity chromatography and mechanism of action. J Chem Soc Perk 4:439–442CrossRef
24.
go back to reference Leser TD, Amenuvor JZ, Jensen TK, Lindecrona RH, Boye M, Møller K (2002) Culture-independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Appl Environ Microbiol 68:673–690PubMedCentralCrossRefPubMed Leser TD, Amenuvor JZ, Jensen TK, Lindecrona RH, Boye M, Møller K (2002) Culture-independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Appl Environ Microbiol 68:673–690PubMedCentralCrossRefPubMed
25.
go back to reference Dintzis FR, Laszlo JA, Nelsen TC, Baker FL, Calvert CC (1995) Free and total ion concentrations in pig digesta. J Anim Sci 73:1138–1146PubMed Dintzis FR, Laszlo JA, Nelsen TC, Baker FL, Calvert CC (1995) Free and total ion concentrations in pig digesta. J Anim Sci 73:1138–1146PubMed
Metadata
Title
High dietary zinc supplementation increases the occurrence of tetracycline and sulfonamide resistance genes in the intestine of weaned pigs
Authors
Wilfried Vahjen
Dominika Pietruszyńska
Ingo C. Starke
Jürgen Zentek
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2015
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-015-0071-3

Other articles of this Issue 1/2015

Gut Pathogens 1/2015 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.