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Effect of veterinary antibiotics on methane yield from livestock manure anaerobic digestion: an analytical review of the evidence

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Abstract

Antibiotics are administered to livestock animals as medications and, in some jurisdictions, as growth promotors. This review examines the impact of veterinary antibiotics on methane production from manure anaerobic digestion (AD). The animals excrete about 17–90% of the administered antibiotics in manure unchanged or as metabolites, which adversely affect microorganisms catalyzing the manure AD, thereby reducing methane yields. Different antibiotics influence methane production to different extents (0–80%). The results from studies on manure artificially spiked with antibiotics differ from those on manure from antibiotic-fed animals, likely due to the effect of other bioactive substances in the manure. Over time, the microbial culture might adapt to the antibiotics, altering its composition, and further affecting the methane yield. Such adaptation indicates that short-term studies might not fully capture the antibiotic’s long-term effects on AD. Effects of oxytetracycline and chlortetracycline on methane production are debatable, with chlortetracycline generally believed to have a slightly stronger inhibition. Correlation, nonlinear modeling/simulation, and principal component analysis (PCA) reveal that the antibiotic effects on methane yield are complex and depend on various parameters such as antibiotic type, concentration, application mode, duration, specific microbial communities, and digester conditions. The PCA showed that the temperature and concentration rather than the manure origin (pigs vs cows) dictate the magnitude of methane production inhibition. Data on the kinetics of antibiotics’ impact, isomerization, and effects of operation strategies are missing. This review summarizes the main knowledge gaps concerning AD of antibiotics-containing manure and suggestions for operational strategies and future research.

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Source: the data provided in Table 3

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Abbreviations

16S rRNA:

16S ribosomal Ribonucleic acid (RNA)

23S rRNA:

23S ribosomal Ribonucleic acid (RNA)

AD:

Anaerobic digestion

AMP:

Ampicillin

ARB:

Antibiotic-resistant bacteria

ARG:

Antibiotic resistance genes

ASBR:

Anaerobic sequence batch reactor

ASBR:

Anaerobic sludge blanket reactor

BMP:

Biomethane potential

CFR:

Ceftiofur

CH4 :

Methane

CIP:

Ciprofloxacin

CO2 :

Carbon dioxide

CPL:

Chloramphenicol

CSTR:

Continuous stirred tank reactor

CTC:

Chlortetracycline

CZN:

Cefazolin

DFN:

Danofloxacin

DHA:

Dihydrofloric acid

DIF:

Difluoxacin

DIN:

Difluoxacin

DM:

Dry matter

DNA:

Deoxyribonucleic acid

DT90:

Detention time at which 90% of the antibiotic was removed

ENO:

Enrofloxacin

ETH:

Erythromycin

EU/EEA:

European Union/European Economic Area

FFL:

Florfenicol

GEN:

Gentamicin

H2 :

Hydrogen

HRT:

Hydraulic retention time

IC10:

Concentration of the antibiotic which reduces methane yield by 10%

IC20:

Concentration of the antibiotic which reduces methane yield by 20%

IC25:

Concentration of the antibiotic which reduces methane yield by 25%

IC50:

Concentration of the antibiotic which reduces methane yield by 50%

KANA:

Kanamycin

MET:

Metronidazole

MSE:

Micospectone

NEO:

Neomycin

NOVO:

Novobiocin

OTC:

Oxytetracycline

PABA:

P-aminobenzoic acid

PCA:

Principal components analysis

PEN:

Penicillin

RIF:

Rifampicin

RNA:

Ribonucleic acid

ROX:

Roxithromycin

SAR:

Sarafloxacin

SDE:

Sulfadimidine

SFM:

Sulfamethoxazole

SFZ:

Sulfadiazine

SMA:

Specific methanogenic activity

SMN:

Streptomycin

SMOD:

Sulfamethoxydiazine

SPEC:

Spectinomycin

SPL:

Sulfachloropyridazine

SQL:

Sulfaquinoxaline

SZE:

Sulfamethazine

t1/2 :

Half-life

TA:

Tylosin A

TC:

Tetracycline

THA:

Tetrahydrofloric acid

TIN:

Tilmicosin

TS:

Total solids

VFA:

Volatile fatty acids

VS:

Volatile solids

VSS:

Volatile suspended solids

References

  • Abel Zur Wiesch P, Abel S, Gkotzis S, Ocampo P, Engelstadter J, Hinkley T, Magnus C, Waldor MK, Udekwu K, Cohen T (2015) Classic reaction kinetics can explain complex patterns of antibiotic action. Sci Transl Med 7:287ra273

    Article  Google Scholar 

  • Alvarez JA, Otero L, Lema JM, Omil F (2010) The effect and fate of antibiotics during the anaerobic digestion of pig manure. Bioresour Technol 101:8581–8586

    Article  CAS  PubMed  Google Scholar 

  • Amin MM, Zilles JL, Greiner J, Charbonneau S, Raskin L, Morgenroth E (2006) Influence of the antibiotic erythromycin on anaerobic treatment of a pharmaceutical wastewater. Environ Sci Technol 40:3971–3977

    Article  ADS  CAS  PubMed  Google Scholar 

  • Andremont A, Tancrede C (1981) Reduction of the aerobic Gram negative bacterial flora of the gastro-intestinal tract and prevention of traveller’s diarrhea using oral erythromycin. Ann Microbiol (Paris) 132:419–427

    PubMed  Google Scholar 

  • Andriamanohiarisoamanana FJ, Ihara I, Yoshida G, Umetsu K (2020) Kinetic study of oxytetracycline and chlortetracycline inhibition in the anaerobic digestion of dairy manure. Bioresour Technol 315:123810

    Article  CAS  PubMed  Google Scholar 

  • Angenent LT, Mau M, George U, Zahn JA, Raskin L (2008) Effect of the presence of the antimicrobial tylosin in swine waste on anaerobic treatment. Water Res 42:2377–2384

    Article  CAS  PubMed  Google Scholar 

  • Arikan OA, Sikora LJ, Mulbry W, Khan SU, Rice C, Foster GD (2006) The fate and effect of oxytetracycline during the anaerobic digestion of manure from therapeutically treated calves. Process Biochem 41:1637–1643

    Article  CAS  Google Scholar 

  • Arikan OA, Sikora LJ, Mulbry W, Khan SU, Foster GD (2007) Composting rapidly reduces levels of extractable oxytetracycline in manure from therapeutically treated beef calves. Bioresour Technol 98:169–176

    Article  CAS  PubMed  Google Scholar 

  • Arikan OA, Mulbry W, Rice C (2009) Management of antibiotic residues from agricultural sources: use of composting to reduce chlortetracycline residues in beef manure from treated animals. J Hazard Mater 164:483–489

    Article  CAS  PubMed  Google Scholar 

  • Aziz A, Sengar A, Basheer F, Farooqi IH, Isa MH (2022) Anaerobic digestion in the elimination of antibiotics and antibiotic-resistant genes from the environment–A comprehensive review. J Environ Chem Eng 10(1):106423

    Article  CAS  Google Scholar 

  • Bai Y, Xu R, Wang QP, Zhang YR, Yang ZH (2019) Sludge anaerobic digestion with high concentrations of tetracyclines and sulfonamides: dynamics of microbial communities and change of antibiotic resistance genes. Bioresour Technol 276:51–59

    Article  CAS  PubMed  Google Scholar 

  • Bauer A, Lizasoain J, Nettmann E, Bergmann I, Mundt K, Klocke M, Rincón M, Amon T, Piringer G (2014) Effects of the antibiotics chlortetracycline and enrofloxacin on the anaerobic digestion in continuous experiments. Bioenerg Res 7:1244–1252

    Article  CAS  Google Scholar 

  • Beneragama N, Lateef SA, Iwasaki M, Yamashiro T, Umetsu K (2013) The combined effect of cefazolin and oxytertracycline on biogas production from thermophilic anaerobic digestion of dairy manure. Bioresour Technol 133:23–30

    Article  CAS  PubMed  Google Scholar 

  • Berendsen BJA, Lahr J, Nibbeling C, Jansen LJM, Bongers IEA, Wipfler EL, Van De Schans MGM (2018) The persistence of a broad range of antibiotics during calve, pig and broiler manure storage. Chemosphere 204:267–276

    Article  ADS  CAS  PubMed  Google Scholar 

  • Bound JP, Voulvoulis N (2004) Pharmaceuticals in the aquatic environment–A comparison of risk assessment strategies. Chemosphere 56:1143–1155

    Article  ADS  CAS  PubMed  Google Scholar 

  • Boxall AB, Fogg LA, Blackwell PA, Blackwell P, Kay P, Pemberton EJ, Croxford A (2004) Veterinary medicines in the environment. Rev Environ Contam Toxicol 180:1–91. https://doi.org/10.1007/0-387-21729-0_1

    Article  CAS  PubMed  Google Scholar 

  • Brueck CL, Nason SL, Multra MG, Prasse C (2023) Assessing the fate of antibiotics and agrochemicals during anaerobic digestion of animal manure. Sci Total Environ 856:159156

    Article  ADS  CAS  PubMed  Google Scholar 

  • Burboa-Charis VA, Alvarez LH (2020) Methane production from antibiotic bearing swine wastewater using carbon-based materials as electrons’ conduits during anaerobic digestion. Int J Energ Res 44:10996–11005

    Article  CAS  Google Scholar 

  • Campagnolo ER, Johnson KR, Karpati A, Rubin CS, Kolpin DW, Meyer MT, Esteban JE, Currier RW, Smith K, Thu KM, Mcgeehin M (2002) Antimicrobial residues in animal waste and water resources proximal to large-scale swine and poultry feeding operations. Sci Total Environ 299:89–95

    Article  ADS  CAS  PubMed  Google Scholar 

  • Camprubi MJ, Paris M, Casas C (1988) Effects of antimicrobial agents and feed additives on the performance of piggery waste anaerobic treatment. In: Hobson PN (ed) 5th International Symposium on Anaerobic Digestion. Pergamon Press, Bologna, pp 239–248

    Google Scholar 

  • Cavicchioli VQ, Carvalho OV, Paiva JC, Todorov SD, Silva Junior A, Nero LA (2018) Inhibition of herpes simplex virus 1 (HSV-1) and poliovirus (PV-1) by bacteriocins from lactococcus lactis subsp. Lactis and enterococcus durans strains isolated from goat milk. Int J Antimicrob Agents 51:33–37

    Article  CAS  PubMed  Google Scholar 

  • Cha J, Carlson KH (2019) Biodegradation of veterinary antibiotics in lagoon waters. Process Saf Environ 127:306–313

    Article  CAS  Google Scholar 

  • Cheikhyoussef A, Pogori N, Chen HQ, Zhao JX, Tang J, Chen W, Zhang H (2009) Comparison of three different methods for the isolation of bacteriocin-like inhibitory substances from bifidobacterium Infantis Bcrc 14602. J Rapid Meth Aut Mic 17:182–194

    Article  CAS  Google Scholar 

  • Chelliapan S, Wilby T, Sallis PJ, Yuzir A (2011) Tolerance of the antibiotic tylosin on treatment performance of an up-flow anaerobic stage reactor (UASR). Water Sci Technol 63:1599–1606

    Article  CAS  PubMed  Google Scholar 

  • Chen YR (1983) Kinetic-analysis of anaerobic-digestion of pig manure and its design implications. Agr Wastes 8:65–81

    Article  CAS  Google Scholar 

  • Chen M, Wolin MJ (1979) Effect of monensin and lasalocid-sodium on the growth of methanogenic and rumen saccharolytic bacteria. Appl Environ Microbiol 38:72–77

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen YS, Zhang HB, Luo YM, Song J (2012) Occurrence and assessment of veterinary antibiotics in swine manures: a case study in East China. Chin Sci Bull 57:606–614

    Article  CAS  Google Scholar 

  • Chen JF, Yang YW, Liu YY, Tang MZ, Wang RJ, Hu HW, Wang HY, Yang PP, Xue HH, Zhang X (2020) Effects caused by chlortetracycline and oxytetracycline in anaerobic digestion treatment of real piggery wastewater: treatment efficiency and bacterial diversity. Int J Hydrogen Energ 45:9222–9230

    Article  CAS  Google Scholar 

  • Chenxi W, Spongberg AL, Witter JD (2008) Determination of the persistence of pharmaceuticals in biosolids using liquid-chromatography tandem mass spectrometry. Chemosphere 73:511–518

    Article  ADS  CAS  PubMed  Google Scholar 

  • Coban H, Ertekin E, Ince O, Turker G, Akyol C, Ince B (2016) Degradation of oxytetracycline and its impacts on biogas-producing microbial community structure. Bioprocess Biosyst Eng 39:1051–1060

    Article  CAS  PubMed  Google Scholar 

  • Congilosi JL, Aga DS (2021) Review on the fate of antimicrobials, antimicrobial resistance genes, and other micropollutants in manure during enhanced anaerobic digestion and composting. J Hazard Mater 405:123634

    Article  CAS  PubMed  Google Scholar 

  • Czatzkowska M, Harnisz M, Korzeniewska E, Rusanowska P, Bajkacz S, Felis E, Jastrzebski JP, Paukszto L, Koniuszewska I (2021) The impact of antimicrobials on the efficiency of methane fermentation of sewage sludge, changes in microbial biodiversity and the spread of antibiotic resistance. J Hazard Mater 416:125773

    Article  CAS  PubMed  Google Scholar 

  • Czatzkowska M, Harnisz M, Korzeniewska E, Wolak I, Rusanowska P, Paukszto Ł, Bajkacz S (2022) Long-term, simultaneous impact of antimicrobials on the efficiency of anaerobic digestion of sewage sludge and changes in the microbial community. Energies 15(5):1826

    Article  CAS  Google Scholar 

  • De Liguoro M, Cibin V, Capolongo F, Halling-Sorensen B, Montesissa C (2003) Use of oxytetracycline and tylosin in intensive calf farming: evaluation of transfer to manure and soil. Chemosphere 52:203–212

    Article  ADS  PubMed  Google Scholar 

  • Do TM, Choi D, Oh S, Stuckey DC (2022) Anaerobic membrane bioreactor performance with varying feed concentrations of ciprofloxacin. Sci Total Environ 803:150108

    Article  ADS  CAS  PubMed  Google Scholar 

  • Dolliver HA, Gupta SC (2008) Antibiotic losses from unprotected manure stockpiles. J Environ Qual 37:1238–1244

    Article  CAS  PubMed  Google Scholar 

  • Dreher TM, Mott HV, Lupo CD, Oswald AS, Clay SA, Stone JJ (2012) Effects of chlortetracycline amended feed on anaerobic sequencing batch reactor performance of swine manure digestion. Bioresour Technol 125:65–74

    Article  CAS  PubMed  Google Scholar 

  • Drlica K, Zhao X (1997) DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiol Mol Biol Rev 61(3):377–392. https://doi.org/10.1128/mmbr.61.3.377-392.1997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fedler CB, Day DL (1985) Anaerobic digestion of swine manure containing an antibiotic inhibitor. Trans ASAE 28:523–530

    Google Scholar 

  • Feng L, Casas ME, Ottosen LDM, Moller HB, Bester K (2017) Removal of antibiotics during the anaerobic digestion of pig manure. Sci Total Environ 603–604:219–225

    Article  ADS  PubMed  Google Scholar 

  • Fischer JR, Iannotti EL, Sievers DM (1981) Anaerobic-digestion of manure from swine fed on various diets. Agr Wastes 3:201–214

    Article  CAS  Google Scholar 

  • Flores-Orozco D, Patidar R, Levin DB, Sparling R, Kumar A, Cicek N (2020) Effect of ceftiofur on mesophilic anaerobic digestion of dairy manure and the reduction of the cephalosporin-resistance gene cmy-2. Bioresour Technol 301:122729

    Article  CAS  PubMed  Google Scholar 

  • Fountoulakis M, Drillia P, Stamatelatou K, Lyberatos G (2004) Toxic effect of pharmaceuticals on methanogenesis. Water Sci Technol 50:335–340

    Article  CAS  PubMed  Google Scholar 

  • Fountoulakis MS, Stamatelatou K, Lyberatos G (2008) The effect of pharmaceuticals on the kinetics of methanogenesis and acetogenesis. Bioresour Technol 99:7083–7090

    Article  CAS  PubMed  Google Scholar 

  • Gaballah MS, Guo J, Sun H, Aboagye D, Sobhi M, Muhmood A, Dong R (2021) A review targeting veterinary antibiotics removal from livestock manure management systems and future outlook. Bioresour Technol 333:125069

    Article  CAS  PubMed  Google Scholar 

  • Gamal-El-Din H (1986) In: El-Halwagi, M. M. (Editor). Biogas technology, transfer and diffusion: state of the art. Proceedings of of the international conference held at the National Research Centre, Cairo, Egypt, 1984. Vol. Meeting Date 1984, Elsevier, London, UK, pp 480–487. ISBN: 9781851660001, 1851660003.

  • García-Sánchez L, Garzón-Zúñiga MA, Buelna G, Estrada-Arriaga EB (2015) Tylosin effect on methanogenesis in an anaerobic biomass from swine wastewater treatment. Water Sci Technol 73:445–452

    Article  Google Scholar 

  • Gartiser S, Urich E, Alexy R, Kummerer K (2007) Anaerobic inhibition and biodegradation of antibiotics in ISO test schemes. Chemosphere 66:1839–1848

    Article  ADS  CAS  PubMed  Google Scholar 

  • Guo J, Ostermann A, Siemens J, Dong R, Clemens J (2012) Short term effects of copper, sulfadiazine and difloxacin on the anaerobic digestion of pig manure at low organic loading rates. Waste Manag 32:131–136

    Article  CAS  PubMed  Google Scholar 

  • Gurmessa B, Pedretti EF, Cocco S, Cardelli V, Corti G (2020) Manure anaerobic digestion effects and the role of pre- and post-treatments on veterinary antibiotics and antibiotic resistance genes removal efficiency. Sci Total Environ 721:137532

    Article  ADS  CAS  PubMed  Google Scholar 

  • Haffiez N, Chung TH, Zakaria BS, Shahidi M, Mezbahuddin S, Hai FI, Dhar BR (2022) A critical review of process parameters influencing the fate of antibiotic resistance genes in the anaerobic digestion of organic waste. Bioresour Technol 354:127189

    Article  CAS  PubMed  Google Scholar 

  • Hamscher G, Pawelzick HT, Hoper H, Nau H (2005) Different behavior of tetracyclines and sulfonamides in sandy soils after repeated fertilization with liquid manure. Environ Toxicol Chem 24:861–868

    Article  CAS  PubMed  Google Scholar 

  • Han Z, Shao B, Lei L, Pang R, Wu D, Tai J, Xie B, Su Y (2023) The role of pretreatments in handling antibiotic resistance genes in anaerobic sludge digestion–A review. Sci Total Environ 869:161799

    Article  ADS  CAS  PubMed  Google Scholar 

  • Henderson C, Stewart CS, Nekrep FV (1981) The effect of monensin on pure and mixed cultures of rumen bacteria. J Appl Bacteriol 51:159–169

    Article  CAS  Google Scholar 

  • Hilpert R, Winter J, Hammes W, Kandler O (1981) The sensitivity of archaebacteria to antibiotics. Zbl Bakt Mik Hyg I C 2:11–20

    CAS  Google Scholar 

  • Hilpert R, Winter J, Kandler O (1984) Agricultural feed additives and disinfectants as inhibitory factors in anaerobic-digestion. Agr Wastes 10:103–116

    Article  CAS  Google Scholar 

  • Hu XG, Luo Y, Zhou QX, Xu L (2008) Determination of thirteen antibiotics residues in manure by solid phase extraction and high performance liquid chromatography. Chinese J Anal Chem 36:1162–1166

    Article  CAS  Google Scholar 

  • Hu F, Zhai H, Yang Y, Tian Y, Wang J, Qiang H (2022) The effects of chlortetracycline on anaerobic digestion of chicken manure and the role of extracellular polymeric substances. J Clean Prod 367:133014

    Article  CAS  Google Scholar 

  • Huang L, Wen X, Wang Y, Zou Y, Ma B, Liao X, Liang J, Wu Y (2014) Effect of the chlortetracycline addition method on methane production from the anaerobic digestion of swine wastewater. J Environ Sci (china) 26:2001–2006

    Article  PubMed  Google Scholar 

  • Huang W, Yang F, Huang W, Lei Z, Zhang Z (2019) Enhancing hydrogenotrophic activities by zero-valent iron addition as an effective method to improve sulfadiazine removal during anaerobic digestion of swine manure. Bioresour Technol 294:122178

    Article  CAS  PubMed  Google Scholar 

  • Hummel H, Bär U, Heller G, Böck A (1985) Antibiotic sensitivity pattern of in vitro polypeptide synthesis systems from Methanosarcina barkeri and Methanospirillum hungatei. Syst Appl Microbiol 6:125–131

    Article  CAS  Google Scholar 

  • Ince B, Coban H, Turker G, Ertekin E, Ince O (2013) Effect of oxytetracycline on biogas production and active microbial populations during batch anaerobic digestion of cow manure. Bioprocess Biosyst Eng 36:541–546

    Article  CAS  PubMed  Google Scholar 

  • IRENA, IRENASTAT power capacity and generation, (2022) International Renewable Energy Agency, https://www.irena.org/Data/Downloads/IRENASTAT (accessed Nov.14, 2023).

  • Jacobsen AM, Halling-Sorensen B (2006) Multi-component analysis of tetracyclines, sulfonamides and tylosin in swine manure by liquid chromatography-tandem mass spectrometry. Anal Bioanal Chem 384:1164–1174

    Article  CAS  PubMed  Google Scholar 

  • Ke X, Wang CY, Li RD, Zhang Y (2014) Effects of oxytetracycline on methane production and the microbial communities during anaerobic digestion of cow manure. J Integr Agr 13:1373–1381

    Article  CAS  Google Scholar 

  • Kemper N, Farber H, Skutlarek D, Krieter J (2008) Analysis of antibiotic residues in liquid manure and leachate of dairy farms in Northern Germany. Agr Water Manage 95:1288–1292

    Article  Google Scholar 

  • Koniuszewska I, Harnisz M, Korzeniewska E, Czatzkowska M, Jastrzębski JP, Paukszto Ł, Bajkacz S, Felis E, Rusanowska P (2021) The effect of antibiotics on mesophilic anaerobic digestion process of cattle manure. Energies 14(4):1125

    Article  CAS  Google Scholar 

  • Krishnasamy V, Otte J, Silbergeld E (2015) Antimicrobial use in Chinese swine and broiler poultry production. Antimicrob Resist Infect Control 4:17

    Article  PubMed  PubMed Central  Google Scholar 

  • Kumar K, Gupta SC, Chander Y, Singh AK (2005) Antibiotic use in agriculture and its impact on the terrestrial environment. Adv Agron 87:1–54

    Article  CAS  Google Scholar 

  • Kümmerer K, Alexy R, Hüttig J, Schöll A (2004) Standardized tests fail to assess the effects of antibiotics on environmental bacteria. Water Res 38:2111–2116

    Article  PubMed  Google Scholar 

  • Lallai A, Mura G, Onnis N (2002) The effects of certain antibiotics on biogas production in the anaerobic digestion of pig waste slurry. Bioresour Technol 82:205–208

    Article  CAS  PubMed  Google Scholar 

  • Lee C, Jeong S, Ju M, Kim JY (2020) Fate of chlortetracycline antibiotics during anaerobic degradation of cattle manure. J Hazard Mater 386:121894

    Article  CAS  PubMed  Google Scholar 

  • Lins P, Reitschuler C, Illmer P (2015) Impact of several antibiotics and 2-bromoethanesulfonate on the volatile fatty acid degradation, methanogenesis and community structure during thermophilic anaerobic digestion. Bioresour Technol 190:148–158

    Article  CAS  PubMed  Google Scholar 

  • Loftin KA, Henny C, Adams CD, Surampali R, Mormile MR (2005) Inhibition of microbial metabolism in anaerobic lagoons by selected sulfonamides, tetracyclines, lincomycin, and tylosin tartrate. Environ Toxicol Chem 24:782–788

    Article  CAS  PubMed  Google Scholar 

  • Loke ML, Ingerslev F, Halling-Sorensen B, Tjornelund J (2000) Stability of Tylosin A in manure containing test systems determined by high performance liquid chromatography. Chemosphere 40:759–765

    Article  ADS  CAS  PubMed  Google Scholar 

  • Luo L, Zhang C, Zhang Z, Peng J, Han Y, Wang P, Kong X, Rizwan HM, Zhang D, Su P, Liu Y (2020) Differences in tetracycline antibiotic resistance genes and microbial community structure during aerobic composting and anaerobic digestion. Front Microbiol 11:583995

    Article  PubMed  PubMed Central  Google Scholar 

  • Luo J, Wei Z, Cheng X, Liu X, Wang F, Huang W, Fang S, Wu J, Wu Y, Liu J, Zhang L (2023) Surfactant and antibiotic co-occurrence reshaped the acidogenic process for volatile fatty acids production during sludge anaerobic fermentation. Sci Total Environ 905:167064

    Article  ADS  CAS  PubMed  Google Scholar 

  • Ma JW, Shu LX, Mitchell SM, Yu L, Zhao QB, Frear C (2021) Effects of different antibiotic operation modes on anaerobic digestion of dairy manure: focus on microbial population dynamics. J Environ Chem Eng 9:105521

    Article  CAS  Google Scholar 

  • Mai DT, Stuckey DC, Oh S (2018) Effect of ciprofloxacin on methane production and anaerobic microbial community. Bioresour Technol 261:240–248

    Article  CAS  PubMed  Google Scholar 

  • Marounek M, Suchorska O, Savka O (1999) Effect of substrate and feed antibiotics on in vitro production of volatile fatty acids and methane in caecal contents of chickens. Anim Feed Sci Tech 80:223–230

    Article  CAS  Google Scholar 

  • Martinez-Carballo E, Gonzalez-Barreiro C, Scharf S, Gans O (2007) Environmental monitoring study of selected veterinary antibiotics in animal manure and soils in Austria. Environ Pollut 148:570–579

    Article  CAS  PubMed  Google Scholar 

  • Massé DI, Lu D, Masse L, Droste RL (2000) Effect of antibiotics on psychrophilic anaerobic digestion of swine manure slurry in sequencing batch reactors. Bioresour Technol 75:205–211

    Article  Google Scholar 

  • Masse DI, Saady NM, Gilbert Y (2014) Potential of biological processes to eliminate antibiotics in livestock manure: an overview. Animals (basel) 4:146–163

    Article  PubMed  Google Scholar 

  • Mckenna M. Antibiotic use in US farm animals was falling. Now It’s Not, <https://www.motherjones.com/food/2021/12/antibiotics-america-farm-animals-livestock-poultry-fda-report/> (2021).

  • Mitchell SM, Ullman JL, Teel AL, Watts RJ, Frear C (2013) The effects of the antibiotics ampicillin, florfenicol, sulfamethazine, and tylosin on biogas production and their degradation efficiency during anaerobic digestion. Bioresour Technol 149:244–252

    Article  CAS  PubMed  Google Scholar 

  • Mulchandani R, Wang Y, Gilbert M, Van Boeckel TP (2023) Global trends in antimicrobial use in food-producing animals: 2020 to 2030. PLOS Glob Public Health 3:e0001305

    Article  PubMed  PubMed Central  Google Scholar 

  • Mustapha NA, Sakai K, Shirai Y, Maeda T (2016) Impact of different antibiotics on methane production using waste-activated sludge: mechanisms and microbial community dynamics. Appl Microbiol Biotechnol 100:9355–9364

    Article  CAS  PubMed  Google Scholar 

  • Ni BJ, Zeng S, Wei W, Dai X, Sun J (2020) Impact of roxithromycin on waste activated sludge anaerobic digestion: methane production, carbon transformation and antibiotic resistance genes. Sci Total Environ 703:134899

    Article  ADS  CAS  PubMed  Google Scholar 

  • Nguyen F, Starosta AL, Arenz S et al (2014) Tetracycline antibiotics and resistance mechanisms. Biol Chem 395:559–575

    Article  CAS  PubMed  Google Scholar 

  • Nnorom M-A, Saroj D, Avery LM, Hough R, Guo B (2023) A review of the impact of conductive materials on antibiotic resistance genes during the anaerobic digestion of sewage sludge and animal manure. J Hazard Mater 446:130628

    Article  CAS  PubMed  Google Scholar 

  • Oleinick NL. in Mechanism of action of antimicrobial and antitumor agents. Vol. Antibiotics. (eds J.W. Corcoran & F.E. Hahn) (Springer-Verlag, 1975).

  • Paesen J, Cypers W, Busson R, Roets E, Hoogmartens J (1995) Isolation of decomposition products of tylosin using liquid chromatography. J Chromatogr A 699:99–106

    Article  CAS  PubMed  Google Scholar 

  • Pan X, Qiang Z, Ben W, Chen M (2011) Residual veterinary antibiotics in swine manure from concentrated animal feeding operations in Shandong Province, China. Chemosphere 84:695–700

    Article  ADS  CAS  PubMed  Google Scholar 

  • Poels J, Vanassche P, Verstraete W (1984) Effects of disinfectants and antibiotics on the anaerobic-digestion of piggery waste. Agr Wastes 9:239–247

    Article  CAS  Google Scholar 

  • Rani J, Pandey KP, Kushwaha J, Priyadarsini M, Dhoble AS (2022) Antibiotics in anaerobic digestion: investigative studies on digester performance and microbial diversity. Bioresour Technol 361:127662

    Article  CAS  PubMed  Google Scholar 

  • Reyes-Contreras C, Vidal G (2015) Methanogenic toxicity evaluation of chlortetracycline hydrochloride. Electron J Biotechn 18:445–450

    Article  Google Scholar 

  • Saady NMC (2013) Homoacetogenesis during hydrogen production by mixed cultures dark fermentation: unresolved challenge. Int J Hydrog Energy 38(30):13172–13191

    Article  CAS  Google Scholar 

  • Samuelsen OB, Torsvik V, Ervik A (1992) Long-range changes in oxytetracycline concentration and bacterial-resistance towards oxytetracycline in a fish farm sediment after medication. Sci Total Environ 114:25–36

    Article  ADS  CAS  PubMed  Google Scholar 

  • Sandkvist A, Hagelberg M, Mathisen B (1984) Effect of antibiotics and chemotherapeutics on biogas production from piggery waste. In: Bioenergy 84. Proceedings of conference 15–21 June 1984, Göteborg, Sweden. Vol. III. Biomass conversion. Elsevier, Applied Science Publishers, pp 422–426.

  • Sanz JL, Rodriguez N, Amils R (1996) The action of antibiotics on the anaerobic digestion process. Appl Microbiol Biotechnol 46:587–592

    Article  CAS  PubMed  Google Scholar 

  • Sara P, Giuliana DI, Michele P, Maurizio C, Luca C, Fabrizio A (2013) Effect of veterinary antibiotics on biogas and bio-methane production. Int Biodeter Biodegr 85:205–209

    Article  Google Scholar 

  • 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

    Article  ADS  CAS  PubMed  Google Scholar 

  • Schlusener MP, Bester K (2006) Persistence of antibiotics such as macrolides, tiamulin and salinomycin in soil. Environ Pollut 143:565–571

    Article  PubMed  Google Scholar 

  • Shea KM (2003) Antibiotic resistance: what is the impact of agricultural uses of antibiotics on children’s health? Pediatrics 112:253–258

    Article  PubMed  Google Scholar 

  • Shi JC, Liao XD, Wu YB, Liang JB (2011) Effect of antibiotics on methane arising from anaerobic digestion of pig manure. Anim Feed Sci Tech 166–167:457–463

    Article  Google Scholar 

  • Shimada T, Zilles JL, Morgenroth E, Raskin L (2008) Inhibitory effects of the macrolide antimicrobial tylosin on anaerobic treatment. Biotechnol Bioeng 101:73–82

    Article  CAS  PubMed  Google Scholar 

  • Smith P, Samuelsen OB (1996) Estimates of the significance of out-washing of oxytetracycline from sediments under Atlantic salmon sea-cages. Aquaculture 144:17–26

    Article  CAS  Google Scholar 

  • Stone JJ, Clay SA, Zhu Z, Wong KL, Porath LR, Spellman GM (2009) Effect of antimicrobial compounds tylosin and chlortetracycline during batch anaerobic swine manure digestion. Water Res 43:4740–4750

    Article  CAS  PubMed  Google Scholar 

  • Stone JJ, Clay SA, Spellman GM (2010) Tylosin and chlortetracycline effects during swine manure digestion: influence of sodium azide. Bioresour Technol 101:9515–9520

    Article  CAS  PubMed  Google Scholar 

  • Stone JJ, Oswald AS, Lupo CD, Clay SA, Mott HV (2011) Impact of chlortetracycline on sequencing batch reactor performance for swine manure treatment. Bioresour Technol 102:7807–7814

    Article  CAS  PubMed  Google Scholar 

  • Storteboom HN, Kim SC, Doesken KC, Carlson KH, Davis JG, Pruden A (2007) Response of antibiotics and resistance genes to high-intensity and low-intensity manure management. J Environ Qual 36:1695–1703

    Article  CAS  PubMed  Google Scholar 

  • Sukul P, Lamshöft M, Kusari S, Zühlke S, Spiteller M (2009) Metabolism and excretion kinetics of 14C-labeled and non-labeled difloxacin in pigs after oral administration, and antimicrobial activity of manure containing difloxacin and its metabolites. Environ Res 109(3):225–231

    Article  CAS  PubMed  Google Scholar 

  • Syafiuddin A, Boopathy R (2021) Role of anaerobic sludge digestion in handling antibiotic resistant bacteria and antibiotic resistance genes–A review. Bioresour Technol 330:124970

    Article  CAS  PubMed  Google Scholar 

  • Tang R, Yuan SJ, Chen FQ, Zhan XM, Wang W, Hu ZH (2019) Effects of roxarsone and sulfadiazine on biogas production and their degradation during anaerobic digestion. Int Biodeter Biodegr 140:113–118

    Article  CAS  Google Scholar 

  • Tang T, Liu M, Du Y, Chen Y (2023) Mechanism of action of single and mixed antibiotics during anaerobic digestion of swine wastewater: microbial functional diversity and gene expression analysis. Environ Res 219:115119

    Article  CAS  PubMed  Google Scholar 

  • Teeter JS, Meyerhoff RD (2003) Aerobic degradation of tylosin in cattle, chicken, and swine excreta. Environ Res 93:45–51

    Article  PubMed  Google Scholar 

  • Tiseo K, Huber L, Gilbert M, Robinson TP, Van Boeckel TP (2020) Global trends in antimicrobial use in food animals from 2017 to 2030. Antibiotics (basel) 9:918

    Article  PubMed  Google Scholar 

  • Turker G, Ince O, Ertekin E, Akyol C, Ince B (2013) Changes in performance and active microbial communities due to single and multiple effects of mixing and solid content in anaerobic digestion process of OTC medicated cattle manure. Int J Renew Energ Res 3:144–148

    Google Scholar 

  • Umetsu K, Toyoda K, Ihara I, Kitazono Y (2015) Degradation of veterinary antibiotics during anaerobic digestion of dairy manure. Water Pract 10:532–537

    Article  Google Scholar 

  • Renewable Energy Market Update - June 2023 – Analysis - IEA. [accessed 2024 January 17]. https://www.iea.org/reports/renewable-energy-market-update-june-2023

  • Upmanyu N, Malviya VN (2020) Antibiotics: mechanisms of action and modern challenges. Microorganisms for Sustainable Environment and Health. Elsevier, Amsterdam, pp 367–382

    Chapter  Google Scholar 

  • Van Epps A, Blaney L (2016) Antibiotic residues in animal waste: occurrence and degradation in conventional agricultural waste management practices. Curr Pollut Rep 2:135–155

    Article  Google Scholar 

  • Van Nevel CJ, Demeyer DI (1988) Manipulation of the rumen fermentation. In: Hobson PN (ed) The Rumen Microbial Ecosystem. Elsevier Applied Sciences, London, UK, pp 387-443. ISBN 1851661883. https://cir.nii.ac.jp/crid/1130000796869349504 

    Google Scholar 

  • Van Boeckel TP, Brower C, Gilbert M, Grenfell BT, Levin SA, Robinson TP, Teillant A, Laxminarayan R (2015) Global trends in antimicrobial use in food animals. Proc Natl Acad Sci USA 112:5649–5654

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  • Varel VH, Hashimoto AG (1981) Effect of dietary monensin or chlortetracycline on methane production from cattle waste. Appl Environ Microbiol 41:29–34

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Vester B, Douthwaite S (2001) Macrolide resistance conferred by base substitutions in 23S rRNA. J Antimicrob Agents 45(1):1–12

    Article  CAS  Google Scholar 

  • Virolle M-J (2020) A challenging view: antibiotics play a role in the regulation of the energetic metabolism of the producing bacteria. Antibiotics 9:83–83

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Walsh TR, Toleman MA, Poirel L, Nordmann P (2005) Metallo-β-Lactamases: the Quiet before the Storm? Clin Microbiol Rev 18:306–325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang R, Zhang J, Liu J, Yu D, Zhong H, Wang Y, Chen M, Tong J, Wei Y (2018) Effects of chlortetracycline, Cu and their combination on the performance and microbial community dynamics in swine manure anaerobic digestion. J Environ Sci (china) 67:206–215

    Article  CAS  PubMed  Google Scholar 

  • Wei M, Wang CM, Zhao XL, Wu K, Boualy V, Liu J, Yang H, Liu SQ, Yin F, Zhang WD (2020) Effective difference of oxytetracycline concentrations on anaerobic batch digestion of pig manure. Energ Source Part A 42:2082–2089

    Article  Google Scholar 

  • Wen Q, Yang S, Chen Z (2021) Mesophilic and thermophilic anaerobic digestion of swine manure with sulfamethoxazole and norfloxacin: dynamics of microbial communities and evolution of resistance genes. Front Environ Sci Eng 15:1–12

    Article  Google Scholar 

  • Winckler C, Grafe A (2001) Use of veterinary drugs in intensive animal production evidence for persistence of tetracycline in pig slurry. J Soils Sedim 1:66–70

    Article  CAS  Google Scholar 

  • Xian Q, Hu L, Chen H, Chang Z, Zou H (2010) Removal of nutrients and veterinary antibiotics from swine wastewater by a constructed macrophyte floating bed system. J Environ Manage 91:2657–2661

    Article  CAS  PubMed  Google Scholar 

  • Xiao L, Wang Y, Lichtfouse E, Li Z, Kumar PS, Liu J, Feng D, Yang Q, Liu F (2020) Effect of antibiotics on the microbial efficiency of anaerobic digestion of wastewater: a review. Front Microbiol 11:611613

    Article  PubMed  Google Scholar 

  • Yao B, Liu M, Tang T, Hu X, Yang C, Chen Y (2023) Enhancement of anaerobic digestion of ciprofloxacin wastewater by nano zero-valent iron immobilized onto biochar. Bioresour Technol 385:129462

    Article  CAS  PubMed  Google Scholar 

  • Yin FB, Dong HM, Zhang WQ, Zhu ZP, Shang B, Wang Y (2019) Removal of combined antibiotic (florfenicol, tylosin and tilmicosin) during anaerobic digestion and their relative effect. Renew Energ 139:895–903

    Article  CAS  Google Scholar 

  • Yin F, Dong H, Zhang W, Wang S, Shang B, Zhu Z (2021) Ability of anaerobic digestion to remove antibiotics contained in swine manure. Biosys Eng 212:175–184

    Article  CAS  Google Scholar 

  • Yuan Q, Sui M, Qin C, Zhang H, Sun Y, Luo S, Zhao J (2022) Migration, transformation and removal of macrolide antibiotics in the environment: a review. Environ Sci Pollut Res Int 29:26045–26062

    Article  CAS  PubMed  Google Scholar 

  • Yun MK, Wu Y, Li Z et al (2012) Catalysis and sulfa drug resistance in dihydropteroate synthase. Science 335:1110–1114

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang HM, Zhang MK, Gu GP (2008) Residues of tetracyclines in livestock and poultry manures and agricultural soils from north Zhejiang Province. J Ecol Rural Environ 24:69–73

    Google Scholar 

  • Zhang J, Mao F, Loh KC, Gin KY, Dai Y, Tong YW (2018) Evaluating the effects of activated carbon on methane generation and the fate of antibiotic resistant genes and class I integrons during anaerobic digestion of solid organic wastes. Bioresour Technol 249:729–736

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Gu J, Wang X, Zhang K, Yin Y, Zhang R, Zhang S (2019) Effects of tylosin, ciprofloxacin, and sulfadimidine on mcrA gene abundance and the methanogen community during anaerobic digestion of cattle manure. Chemosphere 221:81–88

    Article  ADS  CAS  PubMed  Google Scholar 

  • Zheng W, Yu Z, Xia Y, Wen X (2017) Influence of polyaluminum chloride on microbial characteristics in anaerobic membrane bioreactors for sludge digestion. Appl Microbiol Biotechnol 102(2):1005–1017

    Article  PubMed  Google Scholar 

  • Zitomer DH, Burns RT, Duran M, Vogel DS (2007) Effect of sanitizers, rumensin, and temperature on anaerobic digester biomass. Trans ASABE 50:1807–1813

    Article  Google Scholar 

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Funding

This research was funded by the Natural Sciences and Engineering Research Council of Canada (NSERC) through the Discovery Grant program for anaerobic digestion of nitrogen-rich feedstock (RGPIN-2019-04128), and the Government of Newfoundland and Labrador through the Canadian Agriculture Partnership administrated by the Department of Fisheries, Forestry, and Agriculture.

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Authors and Affiliations

  1. Department of Civil Engineering, Memorial University, St. John’s, NL, A1B 3X5, Canada

    Noori M. Cata Saady & Subramaniyasharma Sivaraman

  2. Centre for Bioenergy, School of Chemical and Biotechnology, SASTRA Deemed University, Thirumalaisamudram, Thanjavur, 613401, India

    Subramaniyasharma Sivaraman & Ponnusami Venkatachalam

  3. Department of Process Engineering, Memorial University, St. John’s, NL, A1B 3X5, Canada

    Sohrab Zendehboudi & Yan Zhang

  4. Faculty of Chemical Engineering, Autonomous University of Yucatan, Periférico Norte Km. 33.5, Tablaje Catastral 13615, Col. Chuburná de Hidalgo Inn, C.P., 97203, Merida, Mexico

    Rosimary Yañez Palma & Juan E. Ruiz Espinoza

  5. Department of Biosystems Engineering, Auburn University, Auburn, 36849, AL, USA

    Saravanan Ramiah Shanmugam

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  1. Noori M. Cata Saady
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Contributions

Conceptualization, NMCS; literature review, NMCS, SS, SZ, YZ, PV, JERE; analysis of the literature data, NMCS, RYP, SZ; writing—original draft preparation, NMCS, SZ, and SS; writing—review and editing, NMCS, PV, SRS, SZ, YZ, and JERE; visualization, SS; funding acquisition, NMCS. All authors have read and agreed to the published version of the manuscript.

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Correspondence to Noori M. Cata Saady.

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Saady, N.M.C., Sivaraman, S., Venkatachalam, P. et al. Effect of veterinary antibiotics on methane yield from livestock manure anaerobic digestion: an analytical review of the evidence. Rev Environ Sci Biotechnol 23, 133–161 (2024). https://doi.org/10.1007/s11157-024-09683-6

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