Impact of Anthropogenic Activities on the Dissemination of ARGs in the Environment—A Review
Abstract
:1. Introduction
2. Materials and Methods
2.1. Data Sources
2.2. Search Strategy
3. Results
3.1. Municipal Facilities as Reservoirs of ARGs
3.1.1. WWTPs
3.1.2. Landfills
3.1.3. Biogas Plants
3.2. The Impact of Agriculture and Animal Husbandry on the Presence of Drugs, ARB and ARGs in the Environment
3.2.1. Agriculture
3.2.2. Animal Husbandry
3.3. Co-Selection of ARGs by Other Anthropogenic Pollutants
3.3.1. Heavy Metals
3.3.2. Microplastics
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Type of Wastewater | Country of Research | Dominant Bacterial Phyla (Percentage) | Reference |
---|---|---|---|
influent | Germany | Firmicutes (52.2%), Proteobacteria (37.8%), Bacteroidetes (4.9%), Actinobacteria (2.2%) | [55] |
effluent | Proteobacteria (54.8%), Bacteroidetes (15.7%), Firmicutes (14.3%), Planctomycetes (2.9%), Actinobacteria (2.6%), Verrucomicrobia (2.1%) | ||
influent | China | Firmicutes (54%), Proteobacteria (34%), Actinobacteria (7%), Bacteroidetes (2%) | [56] |
effluent | Proteobacteria (44%), Actinobacteria (13%), Bacteroidetes (12%), Firmicutes (6%) | ||
influent | China | Proteobacteria (51.3%), Firmicutes (16.4%), Actinobacteria (4.7%), Verrucomicrobia (1.8%) | [57] |
effluent | Proteobacteria (31.2%), Firmicutes (1.1%), Actinobacteria (8.1%), Verrucomicrobia (2.5%) | ||
influent | Poland | Proteobacteria (55.13%), Firmicutes (25.6%), Bacteroidetes (6.3%), Actinobacteria (10.65%) | [58] |
effluent | Proteobacteria (39.06%), Firmicutes (10.1%), Bacteroidetes (19.62%), Actinobacteria (26.26%), Verrucomicrobia (2.54%) |
Antimicrobial Class | Antimicrobial Substance | Concentration [ng L−1] | Reference |
---|---|---|---|
beta-lactam | amoxicillin | 232–5698 | [65] |
ampicillin | 306–4120 | [65] | |
penicillin G | 120–2230 | [66] | |
fluoroquinolone | ciprofloxacin | 475–913 | [67,68] |
ofloxacin | 130–730 | [66,69], | |
imidazole | metronidazole | 4.83–161.0 | [67,70] |
macrolide | clarithromycin | 904–7.3 × 106 | [67,68,71] |
erythromycin | 5–2300 | [71,72] | |
sulfonamide | sulfamethoxazole | 387–5.3 × 106 | [67,68,71] |
sulfadiazine | 326–1072 | [71] | |
tetracycline | tetracycline | 26.23–4160 | [66,70] |
doxycycline | 16.44–97.91 | [70] |
Type of Wastewater | Type of Samples | ARGs | The Relative Abundance of ARGs (Number of Copies Normalized against 1 mL of Sample or Gene 16S rRNA) | Ref. |
---|---|---|---|---|
Hospital wastewater | Influent | blaGES-1 | from 4.6 × 10−5 to 1.4 × 10−3 | [53] |
blaTEM-1 | from 8.6 × 10−5 to 1.3 × 10−4 | |||
blaOXA-1 | from 7.5 × 10−4 to 1.2 × 10−3 | |||
qnrS | from 8.2 × 10−7 to 1.7 × 10−5 | |||
qnA | from 5.5 × 10−6 to 1.2 × 10−6 | |||
Effluent | blaGES-1 | from 6.3 × 10−5 to 1.6 × 10−3 | ||
blaTEM-1 | from 6.4 × 10−6 to 5.4 × 10−4 | |||
blaOXA-1 | from 5.1 × 10−4 to 1.0 × 10−4 | |||
qnrS | from 5.3 × 10−7 to 1.3 × 10−6 | |||
qnrA | from 9.3 × 10−7 to 2.6 × 10−6 | |||
gene copies/16S rRNA | ||||
Effluent | blaTEM, ermB, qnrS, sul1, tetW | range from 104 to 107 gene copies in 1 mL of sample | [81] | |
Effluent | blaNDM, blaKPC, blaCTX-M, blaSHV, sul1, aac(6′)-Ib | range from 104 to 109 gene copies in 1 mL of sample | [88] | |
Effluent | blaSHV, blaTEM, blaCTX, blaOXA, blaKPC, blaNDM, ermB, sul1, sul2, tetA, tetB, tetC, tetO, tetW, tetM | range from 10−5 to 10−2 gene copies/16S rRNA | [89] | |
Municipal wastewater | Influent | blaTEM, tetA, sul1 | In winter: from 2.56 × 104 to 1.19 × 109 In autumn: from 2.23 × 102 to 3.56 × 107 gene copies in 1 mL of sample | [78] |
Influent | blaSHV, tetA, aac(6′)-Ib-cr | from 104 to 108 gene copies in 1 mL of sample | [82] | |
Effluent | tetM, | 1.9 × 104 | [83] | |
tetO | 7.7 × 104 | |||
tetW | 1.0 × 104 | |||
sul1 | 5.4 × 106 | |||
sul2 | 7 × 105 | |||
gene copies in 1 mL of sample | ||||
Influent/effluent | aadA, strB, blaOXA, ermF, sul2 tetW, qacH | na a | [84] | |
Influent/effluent | ampR, blaCIT, blaCTX-M, blaFOX, blaGES, blaIMP, blaNPS, blaOXA, blaSHV, blaTEM, blaVIM, mecA, ermB, ermF, macB, mefA, mph, mel, gyrA, parC, qnr, dfr, sul1, sul2, sul3, tet, acrB, acrD, mdt, mex | na | [74] | |
Influent/effluent | blaTEM, qnrA, qnrS, sul1, ermB, intI1 | na | [85] | |
Effluent | qnrS, blaTEM, sul1, ermB, blaOXA-58, tetM, intl1 | na | [86] | |
Effluent | qnrD, qnrS, ermA, ermB, tetA, tetQ, sul1, sul2 | na | [87] | |
Influent | blaTEM, ermB, qnrS, sul1, tetW | range from 104 to 107 gene copies in 1 mL of sample | [81] | |
Effluent | blaTEM, ermB, qnrS, sul1, tetW | range from 102 to 104 gene copies in 1 mL of sample |
Antimicrobial Class and Antimicrobial Substances | Ref. | Dominant Bacterial Phyla and Genera | Ref. | ARGs | Ref. |
---|---|---|---|---|---|
Fluoroquinolone: ofloxacin [0.5–7950 μg kg−1], norfloxacin [75.5–21,335 μg kg−1], ciprofloxacin [<1–4720 μg kg−1], enrofloxacin [<1–77.5 μg kg−1], sarafloxacin [<1–14.6 μg kg−1], fleroxacin [≤1840 μg kg−1], lomefloxacin [≤502 μg kg−1] Sulfonamide: sulfadiazine [≤51.9 μg kg−1], sulfamethoxazole [≤17 μg kg−1], sulfapyridine [≤47.7 μg kg−1], sulfamethazine [≤11.7 μg kg−1], sulfamerazine [≤3.7 μg kg−1] Macrolide: erythromycin [≤55.8 μg kg−1], roxithromycin [≤342 μg kg−1], tylosin [≤33.8 μg kg−1], spiramycin [≤13.3 μg kg−1] Tetracycline: oxytetracycline [174.2–36,650 μg kg−1], tetracycline [101–2943 μg kg−1], chlortetracycline [5.95–3843.7 μg kg−1], doxycycline [127.45–2104.2 μg kg−1] | [91,92,93,94,95] | Proteobacteria (Acinetobacter, Aeromonas, Alcaligenes, Comamonas, Brevundimonas, Methylobacterium, Stenotrophomonas), Bacteroidetes (Bacteroides, Cloacibacterium, Paludibacter, Sphingobacterium, Flavobacterium), Firmicutes (Clostridium, Bacillus) Actinobacteria (Propionibacterium, Mycobacterium), Acidobacteria, Saccharibacteria, Spirochaetes (Treponema) | [96,97,98,99,100] | aadA, blaTEM, blaOXA, tetC, tetG, ermB, ermC, ermF, sul1, sul2, bexA, qepA, aac(6′)-Ib-cr, tetM, blaCTX-M, blaIMP, qnrS, aac(3)-1, dfrA1, dfrA5, dfrA7, dfrA12, | [96,100,101,102,103] |
Country | Production of Sewage Sludge (Thousand Mg) |
---|---|
Germany | 1749.86 |
Poland | 574.64 |
Austria | 233.56 |
Romania | 230.59 |
Hungary | 227.89 |
Czech Republic | 221.09 |
Norway | 141.35 |
Albania | 96.20 |
Ireland | 58.63 |
Slovakia | 54.83 |
Lithuania | 39.94 |
Slovenia | 34.80 |
Estonia | 24.94 |
Latvia | 24.18 |
Croatia | 20.65 |
Malta | 9.69 |
Serbia | 9.60 |
Bosnia and Herzegovina | 9.50 |
Luxembourg | 8.89 (e) a |
Antimicrobial Class | Antimicrobial Substance | Concentration [ng L−1] |
---|---|---|
macrolide | azithromycin | from 13.5 to 50.2 |
erythromycin | from 12.0 to 39,800.5 | |
roxithromycin | from 7.8 to 4745.8 | |
beta-lactam | cefotaxime | from 3.1 to 72.3 |
cephalosporin | from 11.77 to 537 | |
penicillin G | from 22 to 160 | |
fluoroquinolone | ciprofloxacin | from 4.9 to 4482.5 |
norfloxacin | from 25.9 to 21,033.33 | |
ofloxacin | from 8.7 to 190,000 | |
sulfonamide | sulfadiazine | from 15.3 to 29,208 |
sulfamethoxazole | from 0.7 to 8488 | |
sulfamonomethoxine | from 9.8 to 2750 | |
tetracycline | doxycycline | <228 |
oxytetracycline | <3245.0 | |
tetracycline | from 0.2 to 19,000 |
Dominant Microorganisms | ARGs | The Relative Abundance of ARGs (Number of Copies Normalized against 16S rRNA or ngDNA) | Ref. |
---|---|---|---|
Genera: Acholeplasma, Aminivibrio, Candidatus Cloacamonas, Petrimonas, Sedimentibacter, Tissierella | sul1, sul2, ermF, aadA, bacA, | >1.0 × 10−1/16S rRNA | [124] |
na a | qnrA | 1.1/16S rRNA | [116] |
qnrB | 1.13 × 10−5/16S rRNA | ||
qnrD | 4.95 × 10−6/16S rRNA | ||
blaOXA10 | 3.86 × 10−4/16S rRNA | ||
penA | 10−6–10−5/16S rRNA | ||
na | tetO | from 4.1 × 10−5 to 4.2 × 10−2/16S rRNA | [125] |
tetW | from 5.7 × 10−5 to 4.9 × 10−3/16S rRNA | ||
blaTEM | from 3.7 × 10−5 to 3.9 × 10−2/16S rRNA | ||
sul1 | from 4.5 × 10−5 to 3.1 × 10−2/16S rRNA | ||
sul2 | from 1.4 × 10−4 to 6.2 × 10−2/16S rRNA | ||
Phyla: Proteobacteria, Firmicutes, Chloroflexi, Actinobacteria, Bacteroidetes, Acidobacteria | sul1 | 5.6 ± 0.9 log10/ng DNA | [126] |
aadA1 | 5.5 ± 0.8 log10/ng DNA | ||
blaCTX-M | 4.1 ± 0.7 log10/ng DNA | ||
na | tetM | from 2.99 × 10−3 to 2.16 × 10−2/16S rRNA | [127] |
tetX | |||
sul1 | |||
sul2 |
Source | Country | ARB a in Samples | AAs of ARGs b (in 1 gD c−1) | Antibiotics Persistent in Sample (µg g−1) | Ref. |
sewage sludge digestate | Poland | na d | blaOXA and blaTEM from 104 to 107; tetA, tetM and tetQ from 103 to 107; sul1 107−108; ermF, linA and mefA from 104 to 108 | 0.26 of MET e; 2.91 of SMX f; 1.25 of CEF g; 4.55 of DOC h; 1.25 of OXY i; 1.74 of CIP j; 2.07 of NA k | [96] |
corn shredded, triticale, soya, cotton seeds, corn flour and fresh zoological waste digestate | Italy | na | aac-(6′)-Ib-cr up to 105; qnrS up to 107; qepA up to 106 | 7.5 of CIP; 0.25 of SMX | [139] |
sewage sludge digestate | Türkiye | na | na | 1.49 of CLAR l; 1.49 of AZYT m; 5.03 of CIP; 5.35 of DOXY; from 0.22 to 3.63 of OXY; 2.57 of SMX; 0.07–2.52 of CHLOR n; 0.03–1.30 of ERY o; 6.63 of SMX; 4.34 of TRIM p | [142] |
cattle manure digestate | Poland | na | from 104 to 105 of blaTEM and blaOXA; from 105 to 107 of cfxA; from 107 to 109 of tetA, from 108 to 109 of tetM; from 107 to 109 of tetQ; from 105 to 108 of ermF; from 105 to 106 of linA, from 106 to 107 of mefA; from 107 to 108 of sul1; from 105 to 107 of aac(6′)-Ib-cr; from 105 of 109 of qepA; from 106 to 107 of intI1; from 106 to 108 of intI2 | 0.02 of MET; 4.35 of ENR; 0.24 of SMX; 9.62 of OXY; 1.63 of CHLOR; 5.07 of TET r | [143] |
food waste and slurry digestate | China | Pedobacter, Fluviicola, Devosia, and Desulfatiglans | from 101 to 103 of ermB, tetM, tetW and intI1; from 104 to 106 of blaTEM, ermB, tetM, tetW and ermF | na | [144] |
dairy manure digestate | China | na | tetW, sul2 and intI2 > 109 copies g dry solid −1; tetC, tetM, tetQ and tetX > 107 copies g dry solid −1 | na | [145] |
swine slurries and their digestates | Spain | na | from 1010 to 1011 of intI1, sul1 and tetM; lower than 0,1% of blaTEM, blaCTX-M-32, blaOXA-58, qnrS and mecA. | na | [146] |
dairy manure and effluent digestate | USA | na | from 103 to104 sul1, sul2, tetM and tetG | na | [147] |
Source | Country of Research | ARB a in Samples | AAs b of ARGs c (in 1 gD d−1) | Antibiotics Persistent in Sample | Ref. |
---|---|---|---|---|---|
Soil and lettuce | Australia | na e | 144 different ARGs to beta-lactam, aminoglycoside, macrolide-lincoside-streptogramine B (MLSB) and tetracycline from 4.37 × 109 to 2.02 × 1010 g−1 (soil); from 7.45 × 106 to 8.24 × 107 g−1 (lettuce) | na | [21] |
Groundwater | Poland | na | intI1 from 3.60 × 101 to 8.73 × 103; intI2 from 9.88 × 102 to 9.73 × 103; sul2 4.32 × 104; sul1 1.98 × 104; blaTEM 1.58 × 103; aadA9 1.63 × 101; dfrA1 9.73 | 1.01 × 10−2–9.09 × 10−2 ng mL−1 SMX f | [18] |
Crops cultivated on manure-amended plots | sul2 6.54 × 1011; tetA 1.94 × 1011; tetM 2.80 × 1010; sul1 3.10 × 109 | na | |||
Parsley roots and leaves | blaTEM parsley roots from 5.25 × 105 to 1.41 × 107; in parsley leaves from 3.56 × 105 to 9.21 × 105; sul1 from 1.75 × 106 to 7.18 × 106 (roots) and from 1.03 × 106 to 3.33 × 106 (leaves) aadA9 from 6.66 × 104 to 1.06 × 105 (roots). | from 2.28 ng gdm−1 g to 6.02 ng gdm−1 of DOXY h (roots) | |||
Seeds of Pakchoi–vegetable endophytic systems | China | Antibiotic-resistant endophytic bacteria 103 CFU i·g−1 | tetX, blaCTX-M, sul1 and sul2~10−6 copies per 16S rRNA | na | [160] |
lettuce leaves, roots, and soil, | China | na | intI1, tetW, ermF, ermX, and sul1 ranged from 102 to 109 | na | [161] |
soil, rhizospheric soil, broad beans, lettuce Lactuca sativa L. cv. Batavia, roots, leaves and beans in tomatoes Lycopersicon esculentum Mill. | Spain | na | sul1, tetM, qnrS1, blaCTX-M-32, blaOXA-58, mecA (except broad beans), blaTEM ranged from 1 to 106 | na | [162] |
carrot tuber fertilized with pig manure | China | na | mdtH_2, blaCMY_1, vanSB, sul2, intI1_cli, mexF, catB8, floR, tetT, aac(6′)-Ib, aadA2_3~4.8 × 104 | na | [163] |
Source | Country of Research | ARB a in Samples | Antibiotics Persistent in Sample | References |
---|---|---|---|---|
Milk | Bangladesh | na b | 61.2 and 124 μg L−1 respectively for OXY c and AMO d | [178] |
Chicken, beef and pork | Republic of South Africa | na | 20.7–82.1, 41.8–320.8, 65.2–952.2 and 32.8–95.6 μg kg−1, respectively, for SUL e, TET f, STREP g and CIP h | [177] |
Chicken and fish | Bangladesh | na | 508.4 mg kg−1 AMO (chicken) 515.4 mg kg−1 AMO (fish) | [179] |
Chicken | Indonesia | na | up to 275 ng g−1 CIP up to 242 ng g−1 ENRO i | [176] |
Broiler meat and liver | Bangladesh | Campylobacter jejuni i Campylobacter coli | 10–155; 25–135 and 50–115 μg kg−1, respectively, for OXY, CIP and ENRO | [180] |
Meat of the sea bream (Sparus aurata) and sea brass fish (Dicentrarchus labrax) | Türkiye | na | 4.25 ng kg−1 CHLOR j | [181] |
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Czatzkowska, M.; Wolak, I.; Harnisz, M.; Korzeniewska, E. Impact of Anthropogenic Activities on the Dissemination of ARGs in the Environment—A Review. Int. J. Environ. Res. Public Health 2022, 19, 12853. https://doi.org/10.3390/ijerph191912853
Czatzkowska M, Wolak I, Harnisz M, Korzeniewska E. Impact of Anthropogenic Activities on the Dissemination of ARGs in the Environment—A Review. International Journal of Environmental Research and Public Health. 2022; 19(19):12853. https://doi.org/10.3390/ijerph191912853
Chicago/Turabian StyleCzatzkowska, Małgorzata, Izabela Wolak, Monika Harnisz, and Ewa Korzeniewska. 2022. "Impact of Anthropogenic Activities on the Dissemination of ARGs in the Environment—A Review" International Journal of Environmental Research and Public Health 19, no. 19: 12853. https://doi.org/10.3390/ijerph191912853