Antibiotic Use in Agriculture and Its Consequential Resistance in Environmental Sources: Potential Public Health Implications
Abstract
:1. Introduction
2. Antibiotics in Agriculture
2.1. Antibiotics’ Introduction into the Environment
2.2. Animal-Derived Products and Antibiotic Pollution vs Public Health
3. The Great Challenge: Antibiotics Resistance
- The countries have just a few laboratories with the potential to conduct quality-assured microbiology and drug sensitivity testing. Ǻrdal et al. [203] strongly affirmed that collection and reporting of data and the strengthening of laboratory capacity are the two related issues in surveillance.
- Due to the high burden of infectious diseases and low socioeconomic status of these countries, there is a lack of available resources [204]. According to Nasir et al. [169], the developing countries lack the funds to purchase reagents and consumables essential for testing antibiotic resistance, thus lack necessary plans for the surveillance of antibiotic-resistant bacteria. The cost necessary for the adequate surveillance, together with the small margin profits in the veterinary sector presents a financial drawback to support surveillance in the veterinary and agricultural sector [166].
- There is a discrepancy in the selection of isolates. Most of the isolates are from clinical cases that are sick individuals (human or animals). Therefore, the sample of isolates is biased toward a more resistant isolate, owing to the previous antibiotic therapy administered. Also, only a few isolates are involved, since the veterinarian decides on the individual animals to refer to the laboratory. Consequently, the proportion of the isolates is not a representative of the bacteria strains under survey taken from animals [200].
- Either at the regional, national, and local levels, there exists variation in obtaining data, owing to differences in laboratory protocols, conditions employed for testing, personnel conducting the drug sensitivity assay, antibiotic policies, quality control and assurance of the laboratory, and considerations regarding breakpoints. In reality, there are no well-known breakpoints for the animal, which results in the adoption of breakpoints values from human medicines. Nevertheless, the standard protocols and breakpoints from the Clinical Laboratory Standard Institute (CLSI) have been adopted by most countries [200].
- These countries also lack stringent and comprehensive policies and plans to circumvent antibiotic resistance. They lack enforcement of regulations regarding prudent antibiotic use, since many are still faced with the problem of purchasing drugs over the counter or without a prescription [161], and the presence of counterfeit drugs [158,196]. Nevertheless, even if some data are collected, they fail to translate the surveillance data into policy, especially in South Africa [9].
- At the national level, there is a lack of collaborative measures between the different laboratories regarding surveillance of antibiotic resistance, which might hamper efforts to track emerging resistance and also limit the chances of systematic comparison and evaluation of national activities directed toward the containment of antibiotic resistance.
3.1. Antibiotic Resistance in Livestock Farming
3.2. Antibiotic Resistance in the Soil Environment
3.3. Antibiotic Resistance in the Water Environment
4. Conclusions
5. Recommendations on Ways to Reduce the Overall Level of Antibiotic Resistance in Agricultural Settings
Acknowledgments
Author Contributions
Conflicts of Interest
References
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Antibiotic Residue | Concentration | Sample | Consequences in Humans/Animals | Country | Literature |
---|---|---|---|---|---|
Oxytetracycline | Chicken | Carcinogenicity, cytotoxicity in the bones of broiler chickens. Presence of residues cause technological challenges during milk processing. | Tanzania | Kimeria et al. [85] | |
2604.1 ± 703.7 μg/kg | Muscle | ||||
3434.4 ± 604.4 μg/kg | Liver | ||||
3533.1 ± 803.6 μg/kg | kidney | ||||
Beef | Nigeria | Olufemi and Agboola [76] | |||
51.8 ± 90.53 μg/kg | Muscle | ||||
372.7 ± 366.8 μg/kg | Kidney | ||||
1197.7± 718.9 μg/kg | Liver | ||||
Cattle | Ethiopia | Bedada et al. [86] | |||
15.92 to 108.34 μg/kg | Muscle | ||||
99.02 to 112.53 μg/kg | kidney | ||||
Enrofloxacin | 0.73 and 2.57 μg/kg | Chicken tissues | Allergic hypersensitivity reactions or toxic effects, phototoxic skin reactions, chondrotoxic), and tendon rupture | Iran | Tavakoli et al. [87] |
Chloramphenicol | 1.34 and 13.9 μg/kg | Bone marrow toxicity, optic neuropathy, brain abscess | |||
Penicillin | 0.87 and 1.3 μg/kg | Calves muscles | Allergy, affect starter cultures to produce fermented milk product | ||
Oxytetracycline | 3.5 and 4.61 μg/kg | Carcinogenicity, cytotoxicity in the bones of broiler chickens | |||
Quinolones | 30.81 ± 0.45 μg/kg | Chicken | Allergic hypersensitivity reactions or toxic effects (phototoxic skin reactions, chondrotoxic) and tendon rupture | Turkey | Er et al. [88] |
6.64 ± 1.11μg/kg | Beef | ||||
Tetracyclines | Chicken | Primary and permanent teeth discolouration in children and infants, allergic reactions and teratogenicity during the first trimester of pregnancy, nephrotoxicity, carcinogenic, hepatoxocity, and disturbance of the normal microflora of the intestines. It equally causes skin hyperpigmentation of areas exposed to the sun, proximal and distal renal tubular acidosis, hypersensitivity reactions | Egypt | Salama et al. [89] | |
124 to 5812 μg/kg | Breast | ||||
107–6010 μg/kg | Thigh | ||||
103 to 8148 μg/kg | Livers | ||||
Chicken | Cameroon | Guetiya-Wadoum et al. [25] | |||
150 ± 30 μg/g | Liver | ||||
62.4 ± 15.3 μg/g | muscle | ||||
Beef | Kenya | Muriuki et al. [90] | |||
50 to 845μg/kg | Kidney | ||||
50 to 573 μg/kg | Liver | ||||
23–560 μg/kg | muscles | ||||
Amoxicillin | 9.8 to 56.16 μg/mL | Milk | Carcinogenic, teratogenic, and mutagenic effects | Bangladesh | Chowdhury et al. [91] |
10.46 to 48.8 μg/g | Eggs | ||||
Sulfonamides | 16.28μg/kg | Raw milk | Carcinogenicity, allergic reactions | China | Zheng et al. [92] |
Quinolones | 23.25 μg/kg | Allergic hypersensitivity reactions or toxic effects (phototoxic skin reactions, chondrotoxic) and tendon rupture | |||
Oxytetracycline | 199.6 ± 46 ng/g | Beef | Carcinogenicity, allergic reactions | Zambia | Nchima et al. [93] |
Sulphamethazine | 86.5 ± 8.7 ng/g | ||||
Penicillin G | 15.22 ± 0.61 μg/L | Fresh milk | Allergy (hypersensitivity reaction) ranging from mild skin rash to life-threatening anaphylaxis | Nigeria | Olatoye et al. [94] |
7.60 ± 0.60 μg/L | Cheese (wara) | ||||
8.24 ± 0.50 μg/L | Fermented milk (nono) | ||||
Sulphonamides | Chicken | Carcinogenic potential and mild skin rash to severe toxiderma, epidermal toxic necrolysis, blood dyscrasias | Malaysia | Cheong et al. [95] | |
0.08–0.193 μg/g | Liver | ||||
0.006–0.062 μg/g | Breast | ||||
Tetracycline | >0.1 μg/mL | Raw milk | Primary and permanent discolouration of teeth in children and infants, teratogenicity during the first trimester in pregnancy, etc. | India | Nirala et al. [96] |
Oxytetracycline | Carcinogenicity and cytotoxicity in bone marrow of broiler chickens | ||||
Sulfadimidine | Carcinogenicity and allergic reactions | ||||
Sulfamethoxazole |
Pathogens | Antibiotic Resistance | Resistance Genes | Source | Diseases Caused/Symptoms | Country | Literature |
---|---|---|---|---|---|---|
Escherichia coli | Multidrug resistance | bla CTX-M-9, qnr S | Drinking water | Diarrhoea, septicaemia, urinary tract infections, neonatal meningitis, abdominal pain, fever, pneumonia, hemolytic uraemic syndrome, nosocomial bacteraemia | India | Purohit et al. [290] |
bla CTX, bla TEM | Vegetables, raw eggs, raw chicken, unpasteurized milk, raw meat | Rasheed et al. [105] | ||||
bla CTX-M-15, bla OXA-1, bla CMY-2, qnr S, qnr B | Household water supply | Bangladesh | Talukdah et al. [291] | |||
NA | Bird cloacae | Saudi Arabia | Shobrak and Abo-Amer [206] | |||
bla CTX, bla SHV, bla TEM, bla CTX-M + bla TEM, bla CTX-M + bla SHV, bla CTXM + bla SHV + bla TEM, bla TEM + bla SHV | Poultry swab | Zambia | Chishimba et al. [292] | |||
tet, dfr A, bla TEM-1 | Animal feces | Zimbabwe | Mercat et al. [293] | |||
Sul I, Sul II, bla PSE1, AmpC | Zoo lake | Brazil | De Faria et al. [294] | |||
NA | Animal feces | Zambia | Mainda et al. [295] | |||
bla TEM, bla CMY-2 | Milk, water | Thailand | Hinthong et al. [296] | |||
NA | Drinking water | Ghana | Adzitey et al. [297] | |||
Escherichia coli | Multidrug resistance | bla TEM, bla OXA-1, tet A, Sul 1, Sul 2, Sul 3, dfrA1-Sat1-aadA1-orfX gene cassette, Sat-psp-aadA2-cmlA1-caadA1-qacH-IS440-Sul3 | Chicken and turkey meat | Diarrhoea, septicaemia, urinary tract infections, neonatal meningitis, abdominal pain, fever, pneumonia, hemolytic uraemic syndrome, nosocomial bacteraemia | Tunisia | Soufi et al. [298] |
NA | Curds, pasteurized milk, déguè | Burkina Faso | Bagré et al. [299] | |||
bla TEM-1, bla CTX-M, bla SHV, tet A, tet B | Drinking water, | Tanzania | Lyimo et al. [300] | |||
bla TEM, Sul 2, Sul 3, aad A, str A, str B, cat A1, cml A1, tet A, tet B, qnrS | Waste, litter, soil and water samples from poultry farms | Nigeria | Adewolo et al. [301] | |||
NA | Vegetables | Iran | Bonyadian et al. [227] | |||
bla CTX-M, bla TEM-1 | Soil, feces | China | Gao et al. [108] | |||
bla CTX-M, DHA-1(AmpC) | Retail food Pearl river | Ye et al. [302] | ||||
Sstr A, aad A, cat 1, bla TEM, tet A, tet B, tet C, tet D, tet K, tet M | Effluent from wastewater treatment facilities | South Africa | Adefisoye and Okoh [268] | |||
Salmonella sp. | Multidrug resistance | tet A, Sul 1 | Water, soil, meat, vegetables, dry foods | Salmonellosis (diarrheal disease), bacteraemia | Kenya | Christabel et al. [303] |
Escherichia coli | ||||||
Shigella sp. | Shigellosis (bacillary dysentery) | |||||
Salmonella enteritidis | Multidrug resistance | NA | Food | Salmonellosis, bacteraemia | Brazil | Oliveira et al. [304] |
Salmonella typhimurium | Multidrug resistance | bla TEM, tet A, tet C, Sul 1, Sul 3, cat 1, flo R, dfrA12, orf F, aad A2 | Chicken (liver, intestinal contents, gall bladder | Salmonellosis, bacteraemia | Egypt | El-Sharkawy et al. [305] |
Staphylococcus aureus | Multidrug resistance | mec A, bla Z, tet K | Broiler chicken (caecum, feces, retail meat | Bovine mastitis, endocarditis, osteomyelitis, furunculosis, necrotizing pneumonia, toxin syndromes, gastroenteritis, abscess formation | South Africa | Mkize et al. [306] |
NA | Milk | Ateba et al. [307] | ||||
Salmonella enterica | Multidrug resistance | NA | Feces of poultry, swine and hedgedogs | Salmonellosis (diarrhoeal disease), bacteraemia | Burkina Faso | Kagambèga et al. [130] |
Salmonella enterica subsp. enterica | Food, water, and animal | Sudan | Elmadiena et al. [308] | |||
Enterococcus faecium | Multidrug resistance | Tet M, tet L, erm B | Chicken feces and residual water | Neonatal meningitis, vancomycin-resistant enterococci (VRE) infections, nosocomial infections | Angola | Martins et al. [309] |
Vibrio species | Multidrug resistance | bla P1, dfr A15, aad A2 cassettes | Surface urban water, shell fish | Diarrhoea, cholera/profuse watery stool (rice water stool) | Mozambique | Taviani et al. [310] |
Enterococcus species | Multidrug resistance | vanA, vanC1, vanc2 | Meat, fish, vegeatbles, pasteurized milk, cheese | Nosocomial infections, neonatal meningitis, urinary and wound infections | Egypt | Raafat et al. [311] |
erm B, tet M-tetK, aph(3′)-III, ant(6), van C2, aac(6′)-aph(2′′) | Vegetables | Tunisia | Said et al. [312] | |||
Said et al. [313] | ||||||
tet M, tet L, erm B, cat gene, aph(3)-IIa gene, aac(6′)-aph(2′′) and ant(6)-1a | Seafoods | |||||
Staphylococcus sp. | Multidrug resistance | NA | Starch, meat, salad, vegetables | Skin infections, bovine mastitis, infections associated with prosthetic devices and catheters, gastroenteritis, abscess formation | Botswana | Loeto et al. [314] |
bla Z, tet M | Milk and traditional cheese and kashk | Iran | Jamali et al. [315] | |||
Campylobacter sp. | Multidrug resistance | NA | Chickens | Campylobacteriosis, post infectious irritable bowel syndrome | South Africa | Bester and Essack [33] |
Pseudomonas sp. | Multidrug resistance | tet A, Sul 1, bla TEM, (aadA2, aadA1), dfr A15, dfr 1 | Treated and untreated water | Infections of the blood, bone, urinary tract, central nervous system, and wounds endocarditis, pneumonia (nosocomial infections) | Nigeria | Adesoji et al. [316] Igbinosa and Obuekwe [317] |
P. aeruginosa | Multidrug resistance | bla OXA, bla IMP, bla AMPC, bla TEM, tet C | Abattoir environment | |||
Salmonella sp. | Multidrug resistance | NA | Meat, meat product | Salmonellosis (diarrheal disease), bacteraemia | Uganda | Bosco et al. [211] |
pse-1, tet A, ant(3′′)-1a, tet B tet A, Sul1, Sul2, ant(3′′)-1a, pse-1, tet B | Broiler’s chicken (South Africa) Broiler’s chicken (Brazil) | South Africa | Zishiri et al. [318] | |||
NA | Raw meat, minced meat, burger samples, raw eggs, raw milk | Ethiopia | Ejo et al. [104] | |||
dfrA12-aadA2, aadA2-lin G, qnr S | Pigs, retail pork | Thailand & Laos | Sinwat et al. [319] | |||
NA | Raw chicken | Senegal | Bada-Alambedji et al. [320] | |||
NA | Beef | Namibia | Shilangale [321] | |||
Salmonella sp. | Multidrug resistance | NA | Street foods including macaroni, salad, bean cooked in sauce, rice in sauce | As indicated above | Benin Republic | Sina et al. [322] |
Staphylococcus aureus | ||||||
Escherichia coli | Multidrug resistance | NA | Turkey meat | As indicated above | Morocco | Abdellah et al. [323] |
Staphylococcus aureus | ||||||
Aeromonas sp. | Multidrug resistance | NA | Surface water, wastewater effluent | Gastroenteritis and wound infections | South Africa | Olaniran et al. [324] |
Listeria sp. | Listeriosis | |||||
Aeromonas sp. | Multidrug resistance | NA | Surface water, drinking water | As indicated above | Mulamattathil et al. [243] | |
Pseudomonas sp. | As indicated above | |||||
Salmonella typhimurium | Multidrug resistance | NA | Animal feces, eggs | Salmonellosis(diarrheal disease), bacteraemia | Kenya | Nyabundi et al. [325] |
Salmonella enteritidis | ||||||
Escherichia coli | Multidrug resistance | bla TEM, aadA, bla CTX-M, bla SHV | Hospital effluent, wastewater, urban rivers | As indicated above | Democratic Republic of Congo | Laffite et al. [326] |
Enterococcus sp. | ||||||
Pseudomonas sp. | ||||||
Bacillus sp. | Multidrug resistance | NA | Oluwa river | Meningitis, anthrax, pneumonia, food poisoning | Nigeria | Ayandiran et al. [327] |
Staphylococcus sp. | ||||||
Streptococcus sp. | ||||||
Pseudomonas sp. | As indicated above | |||||
Micrococcus sp. | Pulmonary infection, septic shock, recurrent bacteraemia | |||||
Klebsiella oxytoca | Multidrug resistance | NA | Surface water | Septic shock, urinary tract infection | Mexico | Delgado-Gardèa et al. [328] |
Escherichia coli | As indicated above | |||||
Enterobacter cloacae | Intra-abdominal tract infections, septic arthritis, ophthalmic infections, bacteraemia, UTI | |||||
Enterobacter cloacae | Multidrug resistance | dfr A1, dfr A5, dfr A7, dfr A12, dfr A15, dfr A17, dfr A25, aad A1, aad A2, aad A5, aad A7, aad A12, aad A22, aac(3)-Id, cml A, ere A2, arr3, bla TEM, bla SHV, bla CTX-M, bla OXA, flo R, qnr S, aac(6)-Id-cr | Milk | Bovine mastitis, pulmonary pneumonia, septic shock, nosocomial infections, urinary tract infections, septicaemia, wound infection, bacteraemia, hepatic, pancreatic and biliary disease, nosocomial inefctions (UTI, wounds, blood and lower respiratory tract | Egypt | Ahmed and Shimamoto [329] |
Klebsiella pneumoniae | ||||||
Klebsiella oxytoca | ||||||
Escherichia coli | ||||||
Citrobacter freundii | ||||||
Citrobacter sp. | Multidrug resistance | bla TEM, tet A, mef A, erm B, Sul 1, int 1 | Drinking water | Variety of nosocomial infections | Uganda | Soge et al. [330] |
Escherichia coli | As indicated above | |||||
Enterobacter spp. | ||||||
Klebsiella sp. | ||||||
Morgnella morganii | Neonatal sepsis, arthritis, UTI | |||||
Proteus spp. | UTI and formation of stones | |||||
Providencia rettgeri | Cystitis, complicated UTI | |||||
Pseudomonas sp. | As indicated above | |||||
Salmonella sp. | ||||||
Serratia odorifera | Not involved in any invasive disease |
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Manyi-Loh, C.; Mamphweli, S.; Meyer, E.; Okoh, A. Antibiotic Use in Agriculture and Its Consequential Resistance in Environmental Sources: Potential Public Health Implications. Molecules 2018, 23, 795. https://doi.org/10.3390/molecules23040795
Manyi-Loh C, Mamphweli S, Meyer E, Okoh A. Antibiotic Use in Agriculture and Its Consequential Resistance in Environmental Sources: Potential Public Health Implications. Molecules. 2018; 23(4):795. https://doi.org/10.3390/molecules23040795
Chicago/Turabian StyleManyi-Loh, Christy, Sampson Mamphweli, Edson Meyer, and Anthony Okoh. 2018. "Antibiotic Use in Agriculture and Its Consequential Resistance in Environmental Sources: Potential Public Health Implications" Molecules 23, no. 4: 795. https://doi.org/10.3390/molecules23040795
APA StyleManyi-Loh, C., Mamphweli, S., Meyer, E., & Okoh, A. (2018). Antibiotic Use in Agriculture and Its Consequential Resistance in Environmental Sources: Potential Public Health Implications. Molecules, 23(4), 795. https://doi.org/10.3390/molecules23040795