Longitudinal screening of antibiotic residues, antibiotic resistance genes and zoonotic bacteria in soils fertilized with pig manure.
Agriculture
Antbiotic residues
Antibiotic resistance
Environment
Manure
Zoonotic pathogens
Journal
Environmental science and pollution research international
ISSN: 1614-7499
Titre abrégé: Environ Sci Pollut Res Int
Pays: Germany
ID NLM: 9441769
Informations de publication
Date de publication:
Aug 2020
Aug 2020
Historique:
received:
27
05
2019
accepted:
29
04
2020
pubmed:
16
5
2020
medline:
11
7
2020
entrez:
16
5
2020
Statut:
ppublish
Résumé
Fertilization with animal manure is one of the main routes responsible for the introduction of antibiotic residues, antibiotic resistance genes, and zoonotic bacteria into the environment. The aim of this study was to assess the effect of the use of pig (swine) manure as a fertilizer on the presence and fate of six antibiotic residues, nine antibiotic resistance genes, and bacteria (zoonotic bacteria Salmonella spp. and Campylobacter spp. and E. coli as indicator for Gram-negative bacterial species of the microbiota of livestock) on five fields. To the best of our knowledge, the present study is the first to assess a multitude of antibiotic residues and resistance to several classes of antibiotics in pig manure and in fertilized soil over time in a region with an intensive pig industry (Flanders, Belgium). The fields were sampled at five consecutive time points, starting before fertilization up to harvest. Low concentrations of antibiotic residues could be observed in the soils until harvest. The antibiotic resistance genes studied were already present at background levels in the soil environment prior to fertilization, but after fertilization with pig manure, an increase in relative abundance was observed for most of them, followed by a decline back to background levels by harvest-time on all of the fields studied. No apparent differences regarding the presence of antibiotic resistance genes in soils were observed between those fertilized with manure that either contained antibiotic residues or not. With regard to dissemination of resistance, the results presented in this study confirm that fertilization with animal manure directly adds resistance genes to the soil. In addition, it shows that this direct mechanism may be more important than possible selective pressure in soil-dwelling bacteria exerted by antibiotic residues present in the manure. These results also indicate that zoonotic bacteria detected in the manure could be detected in the soil environment directly after fertilization, but not after 1 month. In conclusion, although some antibiotic residues may be present in both manure and soil at concentrations to exert selective pressure, it seems that antibiotic resistance is mostly introduced directly to soil through fertilization with animal manure.
Identifiants
pubmed: 32410188
doi: 10.1007/s11356-020-09119-y
pii: 10.1007/s11356-020-09119-y
doi:
Substances chimiques
Anti-Bacterial Agents
0
Manure
0
Soil
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
28016-28029Subventions
Organisme : Agency for Innovation by Science and Technology in Flanders
ID : IWT-SB/141290
Références
Aabo S, Rasmussen OF, Rossen L et al (1993) Salmonella identification by the polymerase chain reaction. Mol Cell Probes 7:171–178
doi: 10.1006/mcpr.1993.1026
Agnoletti F, Brunetta R, Bano L et al (2018) Longitudinal study on antimicrobial consumption and resistance in rabbit farming. Int J Antimicrob Agents 51:197–205
doi: 10.1016/j.ijantimicag.2017.10.007
Aminov RI, Mackie RI (2001) Molecular Ecology of tetracycline resistance: development and validation of primers for detection of tetracycline resistance genes encoding ribosomal protection proteins Molecular Ecology of Tetracycline Resistance : development and validation of primers. Appl Environ Microbiol 67:22–23
doi: 10.1128/AEM.67.1.22-32.2001
Anonymous (2015a) ISO 13878:1998 Soil Quality -- Determination of Total Nitrogen Content by Dry Combustion (“elemental Analysis”)
Anonymous (2015b) ISO 10390:2005 Soil Quality -- Determination of PH
Anonymous (2016) ISO 10694:1995 Soil Quality -- Determination of Organic and Total Carbon after Dry Combustion (Elementary Analysis)
Anonymous (2017) International Standard 6579-1. Microbiology of the Food Chain — Horizontal Method for the Detection, Enumeration and Serotyping of Salmonella. Part 1: Detection of Salmonella Spp.
Baggot JD, Giguère S (2013) Principles of antimicrobial drug bioavailability and disposition. In: Giguère S, Prescott JF, Dowling PM (eds) Antimicrobial Therapy in Veterinary Medicine, Fifth Edition, Fifth edn. John Wiley & Sons, Inc., p 703
Baloda SB, Christensen L, Trajcevska S (2001) Persistence of a Salmonella enterica Serovar typhimurium DT12 clone in a piggery and in agricultural soil amended with Salmonella -contaminated slurry. Appl Environ Microbiol 67:2859–2862
doi: 10.1128/AEM.67.6.2859-2862.2001
Bengtsson-Palme J, Larsson DGJ (2016) Concentrations of antibiotics predicted to select for resistant bacteria: Proposed limits for environmental regulation. Environ Int 86:140–149
doi: 10.1016/j.envint.2015.10.015
Berendsen BJ, Wegh RS, Memelink J et al (2015) The analysis of animal faeces as a tool to monitor antibiotic usage. Talanta 132:258–268
doi: 10.1016/j.talanta.2014.09.022
Boxall A (2012) Fate and transport of antibiotics in soil systems. In: Keen P, Montforts M (eds) Antimicrobial Resistance in the Environment. Wiley-Blackwell, pp 309–324
Bui XT, Wolff A, Madsen M et al (2011) Fate and survival of Campylobacter coli in swine manure at various temperatures. Front Microbiol 2:1–8
doi: 10.3389/fmicb.2011.00262
Chander Y, Kumar K, Goyal SM et al (2005) Antibacterial activity of soil-bound antibiotics. J Environ Qual 34:1952
doi: 10.2134/jeq2005.0017
Chee-Sanford JC, Mackie RI, Koike S et al (2009) Fate and transport of antibiotic residues and antibiotic r resistance genes following land application of manure waste. J Environ Qual 38:1086
doi: 10.2134/jeq2008.0128
Chee-Sanford J, Maxwell S, Tsau K et al (2012) Antibiotic resistance in swine-manure-impacted environments. In: Keen P, Montforts M (eds) Antimicrobial Resistance in the Environment. Wiley-Blackwell, pp 203–223
Chopra I, Roberts M (2001) Tetracycline antibiotics: Mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev 65:232–260
doi: 10.1128/MMBR.65.2.232-260.2001
Cools D, Merckx R, Vlassak K et al (2001) Survival of E. coli and Enterococcus spp. derived from pig slurry in soils of different texture. Appl Soil Ecol 17:53–62
doi: 10.1016/S0929-1393(00)00133-5
D’Costa VM, King CE, Kalan L et al (2011) Antibiotic resistance is ancient. Nature 477:457–461
doi: 10.1038/nature10388
EUCAST (2020) “European Committee on Antimicrobial Susceptibility Testing”. Data from the EUCAST MIC distribution website, last accessed 07 April 2020. http://www.eucast.org
Gebreyes WA, Altier C (2002) Molecular characterization of multidrug-resistant Salmonella enterica subsp . enterica Serovar typhimurium isolates from swine. J Clin Microbiol 40:2813–2822
doi: 10.1128/JCM.40.8.2813-2822.2002
Hamscher G, Sczesny S, Höper H et al (2002) Determination of persistent tetracycline residues in soil fertilized with liquid manure by high-performance liquid chromatography with electrospray ionization tandem mass spectrometry. Anal Chem 74:1509–1518
doi: 10.1021/ac015588m
Hamscher G, Pawelzick HT, Hoper H et al (2005) Different behavior of tetracyclines and sulfonamides in sandy soils after repeated fertilization with liquid manure. Environ Toxicol Chem 24:861–868
doi: 10.1897/04-182R.1
Hanon J-B, Jaspers S, Butaye P et al (2015) A trend analysis of antimicrobial resistance in commensal Escherichia coli from several livestock species in Belgium (2011-2014). Prev Vet Med 122:443–452
doi: 10.1016/j.prevetmed.2015.09.001
Heuer H, Smalla K (2007) Manure and sulfadiazine synergistically increased bacterial antibiotic resistance in soil over at least two months. Environ Microbiol 9:657–666
doi: 10.1111/j.1462-2920.2006.01185.x
Heuer H, Kopmann C, Binh CTT et al (2009) Spreading antibiotic resistance through spread manure: characteristics of a novel plasmid type with low %G + C content. Environ Microbiol 11:937–949
doi: 10.1111/j.1462-2920.2008.01819.x
Heuer H, Schmitt H, Smalla K (2011a) Antibiotic resistance gene spread due to manure application on agricultural fields. Curr Opin Microbiol 14:236–243
doi: 10.1016/j.mib.2011.04.009
Heuer H, Solehati Q, Zimmerling U et al (2011b) Accumulation of sulfonamide resistance genes in arable soils due to repeated application of manure containing sulfadiazine. Appl Environ Microbiol 77:2527–2530
doi: 10.1128/AEM.02577-10
Holley RA, Arrus KM, Ominski KH et al (2006) Salmonella survival in manure-treated soils during simulated seasonal temperature exposure. J Environ Qual 35:1170
doi: 10.2134/jeq2005.0449
Hutchison ML, Walters LD, Moore T et al (2005) Fate of pathogens present in livestock wastes spread onto fescue plots. Appl Environ Microbiol 71:691–696
doi: 10.1128/AEM.71.2.691-696.2005
Jechalke S, Kopmann C, Rosendahl I et al (2013) Increased abundance and transferability of resistance genes after field application of manure from sulfadiazine-treated pigs. Appl Environ Microbiol 79:1704–1711
doi: 10.1128/AEM.03172-12
Jechalke S, Heuer H, Siemens J et al (2014) Fate and effects of veterinary antibiotics in soil. Trends Microbiol 22:536–545
doi: 10.1016/j.tim.2014.05.005
Knapp CW, Zhang W, Sturm BSM et al (2010) Differential fate of erythromycin and beta-lactam resistance genes from swine lagoon waste under different aquatic conditions. Environ Pollut 158:1506–1512
doi: 10.1016/j.envpol.2009.12.020
Kumar K, Gupta CS, Chander Y et al (2005) Antibiotic use in agriculture and its impact on the terrestrial environment. Adv Agron 87:1–54
doi: 10.1016/S0065-2113(05)87001-4
Leclercq SO, Wang C, Sui Z et al (2016) A multiplayer game: species of Clostridium, Acinetobacter, and Pseudomonas are responsible for the persistence of antibiotic resistance genes in manure-treated soils. Environ Microbiol 18:3494–3508
doi: 10.1111/1462-2920.13337
Lin JS, Tsen HY (1999) Development and use of polymerase chain reaction for the specific detection of Salmonella typhimurium in stool and food samples. J Food Prot 62:1103–1110
doi: 10.4315/0362-028X-62.10.1103
Linton D, Lawson AJ, Owen RJ et al (1997) PCR detection, identification to species level, and fingerprinting of Campylobacter jejuni and Campylobacter coli direct from diarrheic samples. J Clin Microbiol 35:2568–2572
doi: 10.1128/JCM.35.10.2568-2572.1997
Mannion C, Lynch PB, Egan J et al (2007) Seasonal effects on the survival characteristics of Salmonella typhimurium and Salmonella Derby in pig slurry during storage. J Appl Microbiol 103:1386–1392
doi: 10.1111/j.1365-2672.2007.03384.x
Marti R, Tien Y-C, Murray R et al (2014) Safely coupling livestock and crop production systems: how rapidly do antibiotic resistance genes dissipate in soil following a commercial application of swine or dairy anure? Appl Environ Microbiol 80:3258–3265
doi: 10.1128/AEM.00231-14
Miao V, Davies D, Davies J (2012) Path to resistance. In: Keen P, Montforts M (eds) Antimicrobial Resistance in the Environment. Wiley-Blackwell, pp 7–14
NEN (1998) Dierlijke Mest En Mestproducten - Bepaling van de Gehalten Aan Droge Stof En Organische Stof - Gravimetrische Methode.
Nicholson FA, Groves SJ, Chambers BJ (2005) Pathogen survival during livestock manure storage and following land application. Bioresour Technol 96:135–143
doi: 10.1016/j.biortech.2004.02.030
Patterson AJ, Colangeli R, Spigaglia P et al (2007) Distribution of specific tetracycline and erythromycin resistance genes in environmental samples assessed by macroarray detection. Environ Microbiol 9:703–715
doi: 10.1111/j.1462-2920.2006.01190.x
Peak N, Knapp CW, Yang RK et al (2007) Abundance of six tetracycline resistance genes in wastewater lagoons at cattle feedlots with different antibiotic use strategies. Environ Microbiol 9:143–151
doi: 10.1111/j.1462-2920.2006.01123.x
Pornsukarom S, Thakur S (2017) Horizontal dissemination of antimicrobial resistance determinants in multiple Salmonella serotypes following isolation from the environment of commercial swine operations after manure application. Appl Environ Microbiol 83:e01503–17
Rasschaert G, Elst DV, Colson L et al (2020) Antibiotic residues and antibiotic-resistant bacteria in pig slurry used to fertilize agricultural Fields. Antibiotics (Basel) 9(1):E34. https://doi.org/10.3390/antibiotics9010034
doi: 10.3390/antibiotics9010034
Roberts MC (2012) Mechanisms of bacterial antibiotic resistance and lessons learned from environmental tetracycline-resistant bacteria. In: Keen P, Montforts M (eds) Antimicrobial Resistance in the Environment. Wiley-Blackwell, pp 93–121
Roberts MC, Sutcliffe J, Courvalin P et al (1999) Nomenclature for macrolide and macrolide-lincosamide-streptogramin B resistance determinants. Antimicrob Agents Chemother 43:2823–2830
doi: 10.1128/AAC.43.12.2823
Sarmah AK, Meyer MT, Boxall AB (2006) A global perspective on the use, sales, exposure pathways, occurrence, fate and effects of veterinary antibiotics (VAs) in the environment. Chemosphere 65:725–759
doi: 10.1016/j.chemosphere.2006.03.026
Schmitt H, ter Laak T, Duis K (2017) Development and dissemination of antibiotic resistance in the environment under environmentally relevant concentrations of antibiotics and its risk assessment
Sengelov G, Agerso Y, Halling-Sorensen B et al (2003) Bacterial antibiotic resistance levels in Danish farmland as a result of treatment with pig manure slurry. Environ Int 28:587–595
doi: 10.1016/S0160-4120(02)00084-3
Sisak F, Havlickova H, Hradecka H et al (2006) Antibiotic resistance of Salmonella spp. isolates from pigs in the Czech Republic. Vet Med (Praha) 51:303–310
doi: 10.17221/5550-VETMED
Van den Meersche T, Van Pamel E, Van Poucke C et al (2016) Development, validation and application of an ultra high performance liquid chromatographic-tandem mass spectrometric method for the simultaneous detection and quantification of five different classes of veterinary antibiotics in swine manure. J Chromatogr A 1429:1–10
doi: 10.1016/j.chroma.2015.11.025
Van den Meersche T, Rasschaert G, Haesebrouck F et al (2019) Presence and fate of antibiotic residues, antibiotic resistance genes and zoonotic bacteria during biological swine manure treatment. Ecotoxicol Environ Saf 175:29–38
doi: 10.1016/j.ecoenv.2019.01.127
Vanholme L, Imberechts H, Braeye T et al (2015) Report on Zoonotic Agents in Belgium.
VITO (2015) Compendium bemonsterings- en analysemethodes voor mest, bodem en veevoeder (BAM)
Vlaamse Landmaatschappij (2017) Mestrapport 2017. Jaarlijks Rapport over Het Mestbeheer in Vlaanderen