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Assessing the benefits of composting poultry manure in reducing antimicrobial residues, pathogenic bacteria, and antimicrobial resistance genes: a field-scale study

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Abstract

The poultry industry in the European Union produces 13 million tons of manure annually, which represents a major health and environmental challenge. Composting is an environmental-friendly technique for the management of manure, but there are few studies about antibiotic residues and antimicrobial resistances at a field scale. The goal of this study was to determine if the composting of poultry manure at a field scale would result in the reduction of antibiotic residues, pathogenic bacteria, and antibiotic resistance genes (ARGs) in the final fertilizer product. A 10-week composting of poultry manure spiked with enrofloxacin, doxycycline, and ciprofloxacin was performed. The determination of antibiotics residues and 22 selected ARGs was carried out together with the identification of bacteria by metagenomics. In the case of ciprofloxacin and doxycycline, a 90% decrease was observed after composting for 3 weeks. Sixteen ARGs were detected at the beginning of the experiment; 12 of them decreased from week 0 to week 10 (reduction of 73.7–99.99%). The presence of potentially pathogenic bacteria, such as, Campylobacter coli or commensal bacteria such as Escherichia coli decreases along the composting process. In conclusion, 10-week composting of poultry manure promotes the reduction of antibiotic residues and most of the ARGs and pathogenic bacteria.

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References

  • Antunes LP, Martins LF, Pereira RV, Thomas AM, Barbosa D, Lemos LN, Silva GMM, Moura LMS, Epamino GWC, Digiampietri LA (2016) Microbial community structure and dynamics in thermophilic composting viewed through metagenomics and metatranscriptomics. Sci Rep 6:38915

    CAS  Google Scholar 

  • APHA, AWWA, WPCF (2005) Standard methods for the examination of water and wastewater, 21st edn. American Public Health Association, American Water Works Association and Water Environment Federation, Washington

    Google Scholar 

  • Augère-Granier ML (2019) The EU poultry meat and egg sector: main features, challenges and prospects. https://www.europarl.europa.eu/RegData/etudes/IDAN/2019/644195/EPRS_IDA(2019)644195_EN.pdf. Accessed 26 February 2020.

  • Bengtsson-Palme J, Larsson DG (2016) Concentrations of antibiotics predicted to select for resistant bacteria: proposed limits for environmental regulation. Environ Int 86:140–149

    CAS  Google Scholar 

  • Berry ED, Millner PD, Wells JE, Kalchayanand N, Guerini MN (2013) Fate of naturally occurring Escherichia coli O157:H7 and other zoonotic pathogens during minimally managed bovine feedlot manure composting processes. J Food Prot 76:1308–1321

    Google Scholar 

  • Bouissou-Schurtz C, Houeto P, Guerbet M, Bachelot M, Casellas C, Mauclaire AC, Panetier P, Delval C, Masset D (2014) Ecological risk assessment of the presence of pharmaceutical residues in a French national water survey. Regul Toxicol Pharmacol 69:296–303

    CAS  Google Scholar 

  • Bremner J, Mulvaney C (1982) Nitrogen—Total. In: Page et al.(ed.) Methods of soil analysis. Part 2. Agron. Monogr. 9. ASA and SSSA, Madison, pp 595–624

  • Cevidanes A, Esperón F, Di Cataldo S, Neves E, Sallaberry-Pincheira N, Millán J (2020) Antimicrobial resistance genes in Andean foxes inhabiting anthropized landscapes in central Chile. Sci Total Environ 724:138247

    CAS  Google Scholar 

  • Chee-Sanford JC, Mackie RI, Koike S, Krapac IG, Lin YF, Yannarell AC, Maxwell S, Aminov RI (2009) Fate and transport of antibiotic residues and antibiotic resistance genes following land application of manure waste. J Environ Qual 38:1086–1108

    CAS  Google Scholar 

  • Cheng W, Chen H, Su C, Yan S (2013) Abundance and persistence of antibiotic resistance genes in livestock farms: a comprehensive investigation in eastern China. Environ Int 61:1–7

    CAS  Google Scholar 

  • Clewell DB, Flannagan SE (1993) The conjugative transposons of Gram-positive bacteria. In: Clewell DB (ed) Bacterial conjugation. Plenum Press, New York, pp 369–393

    Google Scholar 

  • Cui E, Wu Y, Zuo Y, Chen H (2016) Effect of different biochars on antibiotic resistance genes and bacterial community during chicken manure composting. Bioresour Technol 203:11–17

    CAS  Google Scholar 

  • Dorival-Garcia N, Labajo-Recio C, Zafra-Gomez A, Juarez-Jimenez B, Vilchez JL (2015) Improved sample treatment for the determination of 17 strong sorbed quinolone antibiotics from compost by ultra high performance liquid chromatography tandem mass spectrometry. Talanta 138:247–257

    CAS  Google Scholar 

  • EC - European Commission (2003) Technical Guidance Document (TGD). Part II. Ispra (IT): Joint Research Centre. EUR 2020418 EN/2. https://echa.europa.eu/documents/10162/16960216/tgdpart2_2ed_en.pdf

  • Edrington TS, Fox WE, Callaway TR, Anderson RC, Hoffman DW, Nisbet DJ (2009) Pathogen prevalence and influence of composted dairy manure application on antimicrobial resistance profiles of commensal soil bacteria. Foodborne Pathog Dis 6:217–224

    CAS  Google Scholar 

  • EMA - European Medicines Agency (2019) Sales of veterinary antimicrobial agents in 31 European countries in 2017: Trends from 2010 to 2017. Ninth ESVAC report. EMA/294674/2019. https://www.ema.europa.eu/en/documents/report/sales-veterinary-antimicrobial-agents-31-european-countries-2017_en.pdf. Accessed 26 February 2020

  • EMEA - European Medicines Agency (2006) Guideline on the environmental risk assessment of medicinal products for human use. London (UK): Committee for Medicinal Products for Human Use (CHMP), EMEA. Final report: EMEA/CHMP/SWP/4447/00 corr 2

  • Erickson MC, Smith C, Jiang X, Flitcroft ID, Doyle MP (2015) Manure source and age affect survival of zoonotic pathogens during aerobic composting at sublethal temperatures. J Food Prot 78:302–310

    Google Scholar 

  • Ernervik A (2011) A risk analysis of the potential harm on the soil environment caused by antibiotics in biosolids. Lund University, Bachelor Degree. Available at lup.lub.lu.se/student-papers/record/2343139/file/2343175.pdf

  • Fealy R, Schröder JJ (2008) Assessment of manure transport distances and their impact on economic and energy costs. Proceedings 642, International Fertiliser Society (IFS), York

  • Foged H, Flotats Ripoll X, Bonmatí Blasi A, Palatsi Civit J, Magrí Aloy A, Schelde KM (2012a) Inventory of manure processing activities in Europe. Technical Report No. I concerning “Manure Processing Activities in Europe” to the European Commission, Directorate-General Environment. 138 pp

  • Foged H, Flotats Ripoll X, Bonmatí Blasi A, Palatsi Civit J, Magrí Aloy A (2012b) Assessment of economic feasibility and environmental performance of manure processing technologies. Technical Report No. IV to the European Commission, Directorate-General Environment. Unpublished draft. 130 pp.

  • Foged H, Flotats Ripoll X, Bonmatí Blasi A, Palatsi Civit J, Magrí Aloy A (2012c) End and by-products from livestock manure processing-general types, chemical composition, fertilising quality and feasibility for marketing. Technical Report No. I concerning “Manure Processing Activities in Europe” to the European Commission, Directorate-General Environment. 78 pp

  • Ghosh S, LaPara TM (2007) The effects of subtherapeutic antibiotic use in farm animals on the proliferation and persistence of antibiotic resistance among soil bacteria. ISME J 1:191–203

    CAS  Google Scholar 

  • Hamidian M, Holt KE, Hall RM (2015) Genomic resistance island AGI1 carrying a complex class 1 integron in a multiply antibiotic-resistant ST25 Acinetobacter baumannii isolate. J Antimicrob Chemother 70:2519–2523

    CAS  Google Scholar 

  • He LY, Liu YS, Su HC, Zhao JL, Liu SS, Chen J, Liu WR, Ying GG (2014) Dissemination of antibiotic resistance genes in representative broiler feedlots environments: Identification of indicator ARGs and correlations with environmental variables. Environ Sci Technol 48:13120–13129

    CAS  Google Scholar 

  • Hesse PR (1971) Total nitrogen: the Kjeldahl Process. A Texbook of soil chemical analysis. Murray, London

  • Huhe JC, Wu Y, Cheng Y (2017) Bacterial and fungal communities and contribution of physicochemical factors during cattle farm waste composting. Microbiol Open 6:e518

    Google Scholar 

  • Ikem A, Lin CH, Broz B, Kerley M, Thi HL (2017) Occurrence of enrofloxacin in overflows from animal lot and residential sewage lagoons and a receiving-stream. Heliyon 3:e00409

    Google Scholar 

  • Jones-Dias D, Manageiro V, Ferreira E, Barreiro P, Vieira L, Moura IB, Canica M (2016) Architecture of Class 1, 2, and 3 Integrons from Gram negative bacteria recovered among fruits and vegetables. Front Microbiol 7:1400

    Google Scholar 

  • Karadag D, Özkaya B, Ölmez E, Nissilä ME, Çakmakçı M, Yıldız Ş, Puhakka JA (2013) Profiling of bacterial community in a full-scale aerobic composting plant. Int Biodeterior Biodegradation 77:85–90

    CAS  Google Scholar 

  • Keener HM, Dick WA, Hoitink HA (2000) Composting and beneficial utilization of composted by-product materials. Soil Science Society of America Book Series 315-342.

  • Kheiri R, Akhtari L (2016) Antimicrobial resistance and integron gene cassette arrays in commensal Escherichia coli from human and animal sources in IRI. Gut Pathog 8:40

    Google Scholar 

  • Koczura R, Krysiak N, Taraszewska A, Mokracka J (2015) Coliform bacteria isolated from recreational lakes carry class 1 and class 2 integrons and virulence-associated genes. J Appl Microbiol 119:594–603

    CAS  Google Scholar 

  • Le Devendec L, Mourand G, Bougeard S, Leaustic J, Jouy E, Keita A, Couet W, Rousset N, Kempf I (2016) Impact of colistin sulfate treatment of broilers on the presence of resistant bacteria and resistance genes in stored or composted manure. Vet Microbiol 194:98–106

    Google Scholar 

  • Leal RM, Figueira RF, Tornisielo VL, Regitano JB (2012) Occurrence and sorption of fluoroquinolones in poultry litters and soils from Sao Paulo State, Brazil. Sci Total Environ 432:344–349

    CAS  Google Scholar 

  • Li B, Yang Y, Ma L, Ju F, Guo F, Tiedje JM, Zhang T (2015) Metagenomic and network analysis reveal wide distribution and co-occurrence of environmental antibiotic resistance genes. ISME J 9:2490–2502

    CAS  Google Scholar 

  • Li H, Duan M, Gu J, Zhang Y, Qian X, Ma J, Zhang R, Wang X (2017) Effects of bamboo charcoal on antibiotic resistance genes during chicken manure composting. Ecotoxicol Environ Saf 140:1–6

    Google Scholar 

  • Lillenberg M, Litvin S, Nei L, Roasto M, Sepp K (2010) Enrofloxacin and ciprofloxacin uptake by plants from soil. Agron Res 8:807–814

    Google Scholar 

  • Lin M, Liang J, Zhang X, Wu X, Yan Q, Luo Z (2015) Genetic diversity of three classes of integrons in antibiotic-resistant bacteria isolated from Jiulong River in southern China. Environ Sci Pollut Res 22:11930–11939

    CAS  Google Scholar 

  • Lopes GV, Michael GB, Cardoso M, Schwarz S (2014) Identification and characterization of Salmonella enterica subsp. enterica serovar Derby isolates carrying a new aadA26 gene cassette in a class 1 integron obtained at pig slaughterhouses. FEMS Microbiol Lett 356:71–78

    CAS  Google Scholar 

  • Mao H, Wang K, Wang Z, Peng J, Ren N (2020) Metabolic function, trophic mode, organics degradation ability and influence factor of bacterial and fungal communities in chicken manure composting. Bioresour Technol 302:122883

    CAS  Google Scholar 

  • MAPA-Ministerio de Agricultura Pesca y Alimentación (2019) El sector de la avicultura de carne en cifras: Principales indicadores económicos. https://www.mapa.gob.es/es/ganaderia/temas/produccion-y-mercados-ganaderos/indicadoresaviculturacarneparapublicar2018_tcm30-419674.pdf. Accessed 26 February 2020

  • McKay TL, Ko J, Bilalis Y, DiRienzo JM (1995) Mobile genetic elements of Fusobacterium nucleatum. Plasmid 33:15–25

    CAS  Google Scholar 

  • Mignard S, Flandrois JP (2006) 16S rRNA sequencing in routine bacterial identification: a 30-month experiment. J Microbiol Methods 67:574–581

    CAS  Google Scholar 

  • Nieto-Claudin A, Esperón F, Blake S, Deem SL (2019) Antimicrobial resistance genes present in the faecal microbiota of free-living Galapagos tortoises (Chelonoidis porteri). Zoonoses Public Health 66:900–908

    CAS  Google Scholar 

  • Ou Q, Li W, Li B, Yu C (2017) Prevalence of carbapenem-resistant Klebsiella Pneumoniae (CRKP) and the distribution of Class 1 integron in their strains isolated from a hospital in Central China. Chin Med Sci J 32:107–102

    Google Scholar 

  • Pikkemaat M, Yassin H, Fels-Klerkx H, Berendsen B (2016) Antibiotic residues and resistance in the environment. RIKILT Wageningen UR

  • Qian X, Sun W, Gu J, Wang XJ, Zhang YJ, Duan ML, Li HC, Zhang RR (2016) Reducing antibiotic resistance genes, integrons, and pathogens in dairy manure by continuous thermophilic composting. Bioresour Technol 220:425–432

    CAS  Google Scholar 

  • Ren G, Xu X, Qu J, Zhu L, Wang T (2016) Evaluation of microbial population dynamics in the co-composting of cow manure and rice straw using high throughput sequencing analysis. World J Microbiol Biotechnol 32:101

    Google Scholar 

  • Riaz L, Mahmood T, Khalid A, Rashid A, Ahmed Siddique MB, Kamal A, Coyne MS (2018) Fluoroquinolones (FQs) in the environment: a review on their abundance, sorption and toxicity in soil. Chemosphere 191:704–720

    CAS  Google Scholar 

  • Rice LB (1998) Tn916 family conjugative transposons and dissemination of antimicrobial resistance determinants. Antimicrob Agents Chemother 42:1871–1877

    CAS  Google Scholar 

  • Rusu A, Hancu G, Uivaroşi V (2015) Fluoroquinolone pollution of food, water and soil, and bacterial resistance. Environ Chem Lett 13:21–36

    CAS  Google Scholar 

  • Sacristán I, Esperón F, Acuña F, Aguilar E, García S, López MJ, Cevidanes A, Neves E, Cabello J, Hidalgo-Hermoso E, Poulin E, Millán J, Napolitano C (2020) Antibiotic resistance genes as landscape anthropization indicators: using a wild felid as sentinel in Chile. Sci Total Environ 703:134900

    Google Scholar 

  • Santonja GG, Georgitzikis K, Scalet BM, Montobbio P, Roudier S, Sancho LD (2017) Best available techniques (BAT) Reference document for the intensive rearing of poultry or pigs EUR 28674 EN. https://doi.org/10.2760/020485

  • Sharma M, Reynnells R (2016) Importance of soil amendments: survival of bacterial pathogens in manure and compost used as organic fertilizers. Microbiol Spectrum 4: PFS-0010-2015

  • Shi H, Wang XC, Li Q, Jiang S (2016) Degradation of typical antibiotics during human feces aerobic composting under different temperatures. Environ Sci Pollut Res 23:15076–15087

    CAS  Google Scholar 

  • Singha P, Chanda D, Maurya A, Paul D, Chakravarty A, Bhattacharjee A (2016) Distribution of Class II integrons and their contribution to antibiotic resistance within Enterobacteriaceae family in India. Indian J Med Microbiol 34:303–307

    CAS  Google Scholar 

  • Slana M, Zigon D, Sollner-Dolenc M (2017) Enrofloxacin degradation in broiler chicken manure under field conditions and its residuals effects to the environment. Environ Sci Pollut Res 24:13722–13731

    CAS  Google Scholar 

  • Song C, Li M, Jia X, Wei Z, Zhao Y, Xi B, Zhu C, Liu D (2014) Comparison of bacterial community structure and dynamics during the thermophilic composting of different types of solid wastes: anaerobic digestion residue, pig manure and chicken manure. Microb Biotechnol 7:424–433

    CAS  Google Scholar 

  • Tkachuk VL, Krause DO, Knox NC, Hamm AC, Zvomuya F, Ominski KH, McAllister TA (2014) Targeted 16S rRNA high-throughput sequencing to characterize microbial communities during composting of livestock mortalities. J Appl Microbiol 116:1181–1194

    CAS  Google Scholar 

  • Toleman MA, Bennett PM, Walsh TR (2006) ISCR elements: Novel gene-capturing systems of the 21st century? Microbiol Mol Biol Rev 70:296–316

    CAS  Google Scholar 

  • Vazquez-Roig P, Andreu V, Blasco C, Pico Y (2012) Risk assessment on the presence of pharmaceuticals in sediments, soils and waters of the Pego-Oliva Marshlands (Valencia, eastern Spain). Sci Total Environ 440:24–32

    CAS  Google Scholar 

  • Videnska P, Rahman MM, Faldynova M, Babak V, Matulova ME, Prukner-Radovcic E, Krizek I, Smole-Mozina S, Kovac J, Szmolka A, Nagy B, Sedlar K, Cejkova D, Rychlik I (2014a) Characterization of egg laying hen and broiler fecal microbiota in poultry farms in Croatia, Czech Republic, Hungary and Slovenia. PLoS One 9:e110076

    Google Scholar 

  • Videnska P, Sedlar K, Lukac M, Faldynova M, Gerzova L, Cejkova D, Sisak F, Rychlik I (2014b) Succession and replacement of bacterial populations in the caecum of egg laying hens over their whole life. PLoS One 9:e115142

    Google Scholar 

  • Wang M, Sun Y, Liu P, Sun J, Zhou Q, Xiong W, Zeng Z (2017) Fate of antimicrobial resistance genes in response to application of poultry and swine manure in simulated manure-soil microcosms and manure-pond microcosms. Environ Sci Pollut Res 24:20949–20958

    CAS  Google Scholar 

  • White PA, McIver CJ, Rawlinson WD (2001) Integrons and gene cassettes in the Enterobacteriaceae. Antimicrob Agents Chemother 45:2658–2661

    CAS  Google Scholar 

  • Xia W, Xu T, Qin T, Li P, Liu Y, Kang H, Gu B, Ma P (2016) Characterization of integrons and novel cassette arrays in bacteria from clinical isloates in China, 2000-2014. J Biomed Res 30:292–303

    Google Scholar 

  • Xie WY, Yang XP, Li Q, Wu LH, Shen QR, Zhao FJ (2016) Changes in antibiotic concentrations and antibiotic resistome during commercial composting of animal manures. Environ Pollut 219:182–190

    CAS  Google Scholar 

  • Yang B, Meng L, Xue N (2018) Removal of five fluoroquinolone antibiotics during broiler manure composting. Environ Technol 39:373–381

    CAS  Google Scholar 

  • Zhao JY, Mu XD, Zhu YQ, Xi L, Xiao Z (2015) Identification of an integron containing the quinolone resistance gene qnrA1 in Shewanella xiamenensis. FEMS Microbiol Lett 362:fnv146

  • Zhou X, Qiao M, Wang F-H, Zhu Y-G (2017) Use of commercial organic fertilizer increases the abundance of antibiotic resistance genes and antibiotics in soil. Environ Sci Pollut Res 24:701–710

    CAS  Google Scholar 

  • Zhu L, Liao R, Wu N, Zhu G, Yang C (2019) Heat stress mediates changes in fecal microbiome and functional pathways of laying hens. Appl Microbiol Biotechnol 103:461–472

    CAS  Google Scholar 

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Acknowledgments

The authors also want to thank Elena Neves for her technical support.

Funding

This work has been funded by the Spanish Government (RTA2014-00012).

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Authors and Affiliations

  1. Animal Health Research Center (INIA-CISA), Ctra Algete a El Casar s/n, 28130, Valdeolmos, Madrid, Spain

    Fernando Esperón, Matilde Carballo & Ana de la Torre

  2. Department of Environment and Agronomy (INIA), Ctra La Coruña Km. 7.5, 28040, Madrid, Spain

    Beatriz Albero, José Luis Tadeo & María del Mar Delgado

  3. VISAVET Health Surveillance Centre, Complutense University of Madrid, Avda. Puerta de Hierro, s/n, 28040, Madrid, Spain

    María Ugarte-Ruíz, Lucas Domínguez & Miguel Ángel Moreno

  4. Department of Animal Health, Veterinary Faculty, Complutense University of Madrid, Ada. Puerta de Hierro, s/n, Madrid, Spain

    Lucas Domínguez & Miguel Ángel Moreno

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  1. Fernando Esperón
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  2. Beatriz Albero
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  3. María Ugarte-Ruíz
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  4. Lucas Domínguez
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  5. Matilde Carballo
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  6. José Luis Tadeo
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  7. María del Mar Delgado
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  8. Miguel Ángel Moreno
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  9. Ana de la Torre
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Correspondence to Fernando Esperón.

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Esperón, F., Albero, B., Ugarte-Ruíz, M. et al. Assessing the benefits of composting poultry manure in reducing antimicrobial residues, pathogenic bacteria, and antimicrobial resistance genes: a field-scale study. Environ Sci Pollut Res 27, 27738–27749 (2020). https://doi.org/10.1007/s11356-020-09097-1

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