| Home | E-Submission | Sitemap | Contact Us |  
top_img
Environ Anal Health Toxicol > Volume 37:2022 > Article
Ajibola, Olatunji, and Bayode: Occurrence of veterinary antibiotics in poultry manure from two farms in Ibadan, Nigeria: Ecotoxicological implications in manure-amended soil

Abstract

Veterinary antibiotics are commonly used in poultry farming for preventing diseases and promoting growth. As a result of their incomplete metabolism in poultry birds, veterinary antibiotics are usually excreted and are frequently detected in poultry manures. Veterinary antibiotics in poultry manure applied onto soil may pose serious ecological effect to the terrestrial and aquatic environment. In the present work, the occurrence of three veterinary antibiotics (sulfamethoxazole, sulfadimidine and trimethoprim), categorized as veterinary antimicrobial agents of critical importance, was investigated in poultry manure from two poultry farms in Nigeria. The potential ecotoxicological risk of target veterinary antibiotics in poultry manure-amended soil was also assessed. A modified quick, easy, cheap, effective, rugged and safe (QuEChERS) extraction was adopted for the extraction of target veterinary antibiotics and instrumental analysis was achieved by high performance liquid chromatography. Sulfamethoxazole, sulfadimidine and trimethoprim were quantified in poultry manures from the poultry farms up to 12.7 μg g−1, 16.1 μg g−1 and 33.8 μg g−1, respectively. Sulfamethoxazole and trimethoprim in poultry manure-amended soil presented low risk to Eisenia fetida (earthworm). The ecological effect of sulfamethoxazole for the root length of rice was high in Farm B and medium in Farm A. Sulfamethoxazole presented high risk to aquatic organisms while sulfadimidine and trimethoprim posed medium risk and low risk, respectively to aquatic organisms. The results indicated that residual veterinary antibiotics in poultry manures could have adverse effects on crops after application to agricultural soil. There is a need for effective enlightenment programs for poultry farmers in Nigeria to bring about awareness on the environmental and toxicological impact of the excessive and uncontrolled use of veterinary antibiotics in poultry farming and the adverse ecological implications of poultry manure application on farmlands.

Introduction

Veterinary antibiotics are intensively used in poultry farming to prevent and treat microbial infections as well as to increase the efficiency of feeds in promoting the growth of poultry birds [1,2]. These antibiotics are not completely metabolized in the body tissues of poultry birds, they get deposited in poultry meat as parent compounds and are ultimately excreted via poultry droppings into the environment [3,4]. These poultry droppings are commonly applied as manures on farmlands [5]. Although poultry manure is a rich source of essential nutrients such as nitrogen and phosphorus to soil, other potential environmental toxic substances such as antibiotics, pathogens, hormones, and heavy metals are often present in the poultry droppings [3].
Special attention has been drawn around the globe to the potential harmful effect of antibiotic residues on the living environment [3,6]. The use of veterinary antibiotics has created public and environmental health concerns [1]. The release or accumulation of veterinary antibiotics through the application of manure on farmlands may increase the risk of spreading antibiotic-resistant genes in the environment [2,7]. The uptake of veterinary antibiotics by plants grown in manure-amended soil also raises potential human health concerns [2,8]. After the application of animal manure onto soil, veterinary antibiotics have the potential to still remain in the soil due to ineffective degradation and thus may pose risks to the terrestrial environment [9,10]. Residual antibiotics in poultry manure could also have adverse effects on crops after application to agricultural soil [11]. For example, sulfamethazine antibiotic in poultry manure can change carbon and nitrogen mineralization in soil [2].
Sulfonamides are a class of antibiotic substances widely used in treating bacterial diseases in animal husbandry [10]. Trimethoprim is also commonly used either individually or in combination with a sulfonamide in treating bacterial infections [12]. In the European Union, sulfonamides and trimethoprim were found to account for 11% and 1.6%, respectively of the total antibiotics consumption for food producing animals in 2012 [4,13]. Trimethoprim often acts as a bactericidal agent in the presence of sulfonamides (such as sulfadimidine and sulfamethoxazole) against Gram-positive and many Gram-negative bacteria through the inhibition of nucleic acid synthesis [14]. Despite the importance of veterinary antibiotics in poultry production, risk assessment of these antibiotics towards soil microbial communities and other soil dwelling organisms due to application of poultry manure onto soil is still lacking [4]. There are currently scarce studies on the concentration of antibiotics in the poultry litter and the residual antibiotic concentration in poultry manure used for agricultural purposes [14].
In Nigeria, veterinary antibiotics are routinely used in livestock and poultry production especially as additives to feed and water [15], and thus, the poultry production environment in Nigeria represents an important reservoir of antibiotics and antibiotic resistance genes that may spread to human populations via manure application on production farms [15]. Land application of poultry manure is a common practice in Nigeria because of its value in supplying nutrients to crops as well as being an inexpensive means of poultry waste disposal. This practice of land application of poultry manure poses potential risk to soil dwelling organisms, crops and possibly aquatic organisms. Hence, the occurrence of these antibiotics in poultry manure derived from poultry farms in Nigeria is worth investigating. To the best of our knowledge, no earlier study exists till date on the occurrence of veterinary antibiotics in poultry manure from poultry farms in Nigeria and ecotoxicological effect of the application of poultry manure on soil for agricultural purposes in Nigeria. Antibiotics were only recently determined in sewage sludge, hospital wastewater and dumpsite leachates in Nigeria [12,16,17].
The objective of this study was, therefore, to investigate the occurrence of three veterinary antibiotics sulfamethoxazole, sulfadimidine and trimethoprim which have been categorized as veterinary critically important antimicrobials [18] in poultry manures from two poultry farms in Ibadan, Nigeria. Potential ecotoxicological effect of these antibiotics in poultry manure-amended soil to terrestrial organisms (crops and soil dwelling organisms) and aquatic organisms due to land application of poultry manures from two farms in Nigeria was also investigated. A modified quick, easy, cheap, effective, rugged and safe (QuEChERS) extraction protocol was employed for the extraction of target antibiotics from the poultry manures while instrumental analysis was carried out by high performance liquid chromatography. To the best of our knowledge, first report is presented on the presence of veterinary antibiotics sulfamethoxazole, sulfadimidine and trimethoprim in poultry manure from poultry farms in Ibadan, Nigeria and their ecotoxicological risk assessment in poultry manure-amended soil.

Materials and Methods

Chemicals and reagents

Analytical standards of target antibiotics (sulfamethoxazole, sulfadimidine and trimethoprim) were of high purity (≥98%) and were purchased from Sigma Aldrich, (Steinheim, Germany). HPLC grade acetonitrile and methanol were obtained from Merck (Darmstadt, Germany). Citric acid monohydrate (C6H8O7·H2O), disodium hydrogen phosphate (Na2HPO4) and ethylenediaminetetraacetic acid disodium dihydrate (Na2EDTA·2H2O) salts of analytical grade were purchased from Sigma Aldrich (Steinheim, Germany). Sodium chloride, 99.5% for analysis and anhydrous magnesium sulfate (MgSO4) were obtained from ACROS OrganicsTM. Dispersive-SPE sorbent of primary and secondary amine (PSA) was purchased from Supelco (Bellefonte, USA) while octadecyl silica C18 (EC) sorbent was bought from International Sorbent Technology (IST) UK. Individual standard solutions of target antibiotics (sulfamethoxazole, sulfadimidine and trimethoprim) with a concentration of 1000 mg L−1 were prepared in acetonitrile. Stock solution (100 mg L−1) containing all three antibiotics was prepared from the individual standard solutions. Working standard solutions were prepared by serial dilution of the stock solution. McIlvaine buffer (pH 4) was prepared by dissolving 7.5 g disodium hydrogen phosphate dihydrate and 6.5 g citric acid monohydrate in 500 mL of water. 0.1 M Na2EDTA-McIlvaine buffer was prepared by dissolving 18.61 g Na2EDTA in 500 mL of McIlvaine buffer.

Samples collection and sample pre-treatment

Poultry litters were collected from two poultry farms (Farm A and Farm B) located at Egbeda-Awaye, Egbeda Local Government Area, Ibadan, Oyo State, South-Western Nigeria: Farm A (Lat.: 7.4481436, Long.: 4.0662889) and Farm B (Lat.: 7.44763, Long.: 4.0669977). Questionnaires were initially administered to interview the farmers if antibiotics were being used for their agricultural practices, types of antibiotics used, the dosage administered, the frequency of antibiotics administration and whether the poultry manures were used for crop production. Many poultry farms were visited for the interview in Ibadan metropolis. Farms A and B were selected for their practice of using antibiotics in treating their poultry birds and their use of waste excreta as poultry manure for growing vegetables and other crop produce. A map of the study location is shown in Figure 1.
Poultry manure samples were collected from each of the farms in the months of July and August 2019. From each sampling site and during each sampling, poultry litter samples from different locations along the pile were scooped into a polyethylene bag and thoroughly mixed together. To avoid degradation of target antibiotics, poultry litter samples were kept in a cooler containing ice and immediately transported under cooled conditions to the laboratory. The samples were air dried. The dried samples were ground using a mortar and pestle, wrapped in aluminum foil and stored in a refrigerator prior to extraction and instrumental analysis. Samples for the experiments on method performance were prepared by mixing together the samples from both sampling sites.

QuEChERS extraction

Extraction of target antibiotics was carried out employing the QuEChERS extraction procedure by Guo et al. [19] with slight modifications. Briefly, 1 g of sample was weighed into a 50 mL centrifuge tube. Samples for the experiments on method performance were spiked with appropriate volume of working standard solution while 100 μL of water was added to the samples for real analysis. The sample was stirred vigorously and then placed in darkness overnight. A total of 20 mL extracting solvent comprising methanol/acetonitrile/0.1 M Na2EDTA-McIlvaine buffer in a percentage fraction of 12.5/37.5/50 respectively was added to the sample in the centrifuge tube. The sample was vortex-mixed for 2 minutes and centrifuged for 25 minutes at 3500 rpm. After the centrifugation was complete, the supernatant was decanted into another 50 mL centrifuge tube. The extraction step was repeated. 20 mL of a mixture of methanol/acetonitrile/0.1 M Na2EDTA-McIlvaine buffer (12.5/37.5/50%) was added and the tube was vortex-mixed and centrifuged. The organic layer was then decanted once more into the centrifuge tube containing the previously decanted supernatant.

d-SPE clean-up

The supernatant in the centrifuge tube was then subjected to liquid-liquid partition with 1 g of NaCl and 4 g of MgSO4. The tube was capped and shaken by hand for 1 min to prevent formation of crystalline agglomerates during MgSO4 hydration. The tube was centrifuged for 10 minutes at 2500 rpm. The organic layer was transferred into another centrifuge tube containing clean-up sorbent (40 mg PSA and 20 mg C18), vortex-mixed for 1 minute and centrifuged for 10 minutes at 2500 rpm. The sample was gently evaporated, reconstituted with 1 mL mixture of acetonitrile and 0.1% formic acid (20:80, v/v) and transferred into a glass vial for HPLC analysis.

High performance liquid chromatographic analysis

Target antibiotics were analyzed using high performance liquid chromatography (HPLC), Agilent series 1100 equipped with ultraviolet (UV) and fluorescence detectors. The analytes were separated on a Zorbax Eclipse XDB-C18 (150 mm×4.6 mm, 5 μm) column. UV detection of the three antibiotics was achieved at 254 nm wavelength. Isocratic elution was used with a mobile phase containing an aqueous solution of 0.05 M potassium dihydrogen phosphate buffer (adjusted to pH 3.0 with 0.1% formic acid) and acetonitrile (40:60, v/v). Flow rate of mobile phase was 1.0 mL/min and the injection volume was 10 μL.

Quality assurance

Recovery and precision were determined by spiking manure matrix in replicates at 5 μg g−1 fortification level. The recovery of each analyte was estimated by using the following formula (Equation 1):
(1)
%Recovery=Concentration of antibiotic in spiked sample-Concentration of antibiotic in blank sampleOriginal concentration of antibiotic spiked×100
Precision of the method was appraised in terms of repeatability which was calculated as the percentage relative standard deviation (%RSD) of results obtained for each analyte after the replicate analysis. The limit of detection (LOD) and limit of quantification (LOQ) of the method were determined by spiking manure samples prior to extraction at concentration of 5 μg g−1. The LOD and LOQ for each analyte were calculated by multiplying standard deviation of the concentrations of replicate samples by a factor of 3.3 and 10 respectively divided by slope of the calibration curve. Linearity was checked using external calibration curves at four calibration points ranging from 12.5μg mL−1 to100 μg mL−1. Calibration curves were constructed by plotting the peak area of each analyte against the corresponding analyte concentration.

Ecotoxicological risk assessment in poultry manure-amended soil based on terrestrial toxicity data

Ecotoxicological risk of target antibiotics in poultry manure-amended soil was assessed. Toxicity data (EC50/LC50/NOEC) for terrestrial organisms were sourced from literature, and this includes toxicity data for earthworms and crop plants (root elongation and seedling heights). The terrestrial toxicity data are presented in Table 1.
Predicted-no-effect-concentration of target antibiotic based on terrestrial toxicity data (PNECsoil-terrestrial) was calculated by dividing toxicity data (EC50/LC50/NOEC) by a suitable assessment factor as shown in Table 1, using (Equation 2) with the calculated values provided in Table 1.
(2)
PNEC(soil-terrestrial)=EC50or LC50Assessment factor
Predicted environmental concentrations of target antibiotics in poultry manure-amended soil (PECsoil) were calculated by using the following equation (Equation 3) according to Ghirardini et al. [20] and the European Technical Guidance Document on risk assessment [21]:
(3)
PEC(soil)=Co(soil)+MEC(manure)×APP(manure)DEPTH(soil)×RHO(soil)
where Co(soil) represents the background concentration of antibiotic in the soil before application of poultry manure (was taken to be zero), MEC(manure) stands for the measured environmental concentration in poultry manure (μg kg−1), APP (manure) is the typical application rate of dry manure onto soil which is 0.5 kg m−2, DEPTH(soil) is the mixing depth of 0.2 m generally used for agricultural soil, RHO(soil) is the bulk density of wet soil (1700 kg m−3). Risk quotient of target antibiotics in poultry manure-amended soil for terrestrial organisms (RQsoil-terrestrial) was calculated using Equation 4.
(4)
RQ(soil-terrestrial)=PEC(soil)PNEC(soil-terrestrial)
Risk was categorized according to Ghirardini et al. [20]: high risk if RQ≥1, medium risk if 0.1<RQ<1, and low risk if RQ≤0.1.

Ecotoxicological risk assessment in poultry manure-amended soil based on aquatic toxicity data

Terrestrial toxicity data of target antibiotics are scarce in literature. Therefore, aquatic toxicity data were also used to estimate PNECsoil-aquatic through the equilibrium partition approach (Equation 5) in the European guidance on information requirements and chemical safety assessment (ECHA 2008, Chapter R.10) [25]. Aquatic toxicity data were collected for fish, daphnia and algae and are presented in Table 2. The lowest toxicity value out of the three values for each antibiotic was used to estimate the worst case scenario. PNECwater was calculated by dividing the lowest aquatic toxicity data by assessment factor of 1000.
(5)
PNEC(soil-aquatic)=Ksoil.waterRHOsoil×PNECwater×1000
where Ksoil.water is soil–water partition coefficient, RHOsoil stands for the bulk density of wet soil (1700 Kg m−3). Ksoil.water was calculated using Equation 6 according to the European Chemical Agency [26].
(5)
Ksoil.water=Fairsoil×Kair-water+Fwatersoil+Fsolidsoil×Foc(soil)×Koc1000×RHOsolid
where Fairsoil stands for the volume fraction air in soil (0.2), Kair-water represents the air-water partition coefficient (zero for non-volatile substances), Fwatersoil (0.2) and Fsolidsoil (0.6) represent the volume fraction water in soil and the fraction solid in soil, respectively. Foc(soil) is the weight fraction organic carbon in soil (0.02), Koc is the organic water partition coefficient in Table 2 while RHOsolid is the density of solid phase (2500 kg m−3). If all the default values in bracket are substituted into Equation 6, Ksoil.water can be calculated. Substituting the calculated value of Ksoil.water into Equation 5, the equilibrium partition equation is simplified into Equation 7:
(7)
PNEC(soil-aquatic)=(0.1176+0.01764×Koc)×PNECwater
where Koc stands for the organic carbon partition coefficient of antibiotic (as L kg−1). Table 2 shows the calculated PNECsoil–aquatic values for target antibiotics.
Risk quotient (RQ) of target antibiotics in poultry manure-amended soil based on aquatic toxicity data (RQsoil-aquatic) was calculated by using Equation 8:
(8)
RQ(soil-aquatic)=PEC(soil)PNEC(soil-aquatic)
Risk was categorized according to Ghirardini et al. [20]: high risk if RQ≥1, medium risk if 0.1<RQ< 1, and low risk if RQ≤0.1.

Results and Discussion

Quality assurance parameters

The analytical quality parameters for the determination of target antibiotics in poultry manure are provided in Table 3. Recoveries of target antibiotics at 5 μg g−1 spike level ranged from 77.4% to 136.5%. Hou et al. [39] also reported recoveries range between 63.1% and 79.6%. Precision in terms of percentage relative standard deviation (%RSD) was ≤ 24%. The LODs for the determination of sulfamethoxazole, sulfadimidine and trimethoprim were 0.46 μg g−1, 0.04 μg g−1 and 0.18 μg g−1, respectively while the corresponding LOQs for sulfamethoxazole, sulfadimidine and trimethoprim were 1.40 μg g−1, 0.13 μg g−1and 0.55 μg g−1, respectively. Similar LOD and LOQ values were reported for trimethoprim by Teglia and co-workers [40]. Good linearity of R2 greater than 0.994 was achieved in the calibration curves for all compounds.

Occurrence of target antibiotics in poultry manure and manure-amended soil

The measured environmental concentrations of the antibiotics in poultry manure from the two farms and predicted environmental concentrations in manure-amended soil are presented in Table 4. Sulfamethoxazole was measured up to 5.2 μg g1 and 12.7 μg g1 in poultry manure from the two farms in first and second sampling. Similar levels of sulfamethoxazole were also quantified in poultry manure in other studies, up to 7.11 μg g−1 by Li et al. [41] and 3.76 μg g−1 by Karci and Balcioglu [42]. Sulfadimidine was not detected in poultry manure from both farms in the second sampling and in Farm B in the first sampling. High concentration of 16.1 μg g−1 was, however, measured for sulfadimidine in poultry manure from Farm A in the first sampling. High concentrations of 8.62 μg g−1 and 5.650 μg g−1 were also measured for sulfadimidine in chicken manure by Ji et al. [43] and Zhou et al. [11], respectively but much lower concentrations of sulfadimidine in chicken manures have been reported by other researchers [39,4447]. Sulfadimidine was among the veterinary antibiotics investigated in poultry manure by Topi and Spahiu [48] but was not detected in the samples. Trimethoprim was quantified in this present study up to 8.7 μg g−1 in Farm A and 33.8 μg g−1 in Farm B. Lower amounts of trimethoprim were quantified in poultry litters in some previously published studies [39,40], and was not detected by Patyra et al. [49]. The predicted environmental concentrations (PECsoil) of target antibiotics in poultry manure-amended soil were generally low and are presented in Table 4. PECsoil values for sulfamethoxazole ranged between 0.0075 μg g−1 and 0.0187 μg g−1, while the PECsoil value was calculated up to 0.0237 μg g−1 and 0.0497 μg g−1 for sulfadimidine and trimethoprim, respectively.

Ecotoxicological risk in poultry manure-amended soil based on terrestrial toxicity data

The values of risk quotients of target antibiotics to terrestrial organisms (RQsoil-terrestrial) are presented in Table 5. Sulfamethoxazole in poultry-amended soil in Farm A and Farm B presented low risk to earthworms and medium ecological effects to the seedling height of rice and cucumber. The risk of sulfamethoxazole for the root length of rice was high in Farm B and medium in Farm A while low ecological effect was observed for the root length of cucumber. Sulfadimidine posed medium ecological effect to the seedling height and root length of rice in Farm A and low ecological effect to the seedling height and root length of cucumber in Farm A. In a study by Zhou et al. [11], sulfadimidine was found to pose high risk to rice roots and medium risk to rice seeds and cucumber while sulfamethoxazole presented medium risk to rice roots but low risk to rice seeds and cucumber [11]. Trimethoprim presented low ecological risk to earthworm in poultry manure-amended soils of Farm A and Farm B. Trimethoprim also posed low ecological effect to the seedling height and root length of both rice and cucumber in Farm A, but medium ecological effect to the seedling height and root length of both rice and cucumber in Farm B. The results indicated that residual antibiotics in poultry manure could have adverse effects on crops after their application to agricultural soil.

Ecotoxicological risk in poultry manure-amended soil based on aquatic toxicity data

The logarithms (to base 10) of risk quotient values (RQsoil-aquatic) of the target antibiotics in poultry manure-amended soil based on aquatic toxicity data are shown in Figure 2. RQsoil-aquatic values for sulfamethoxazole were greater than 1 in all poultry manure-amended soils. Our results showed that sulfamethoxazole presented high risk to aquatic organisms while sulfadimidine and trimethoprim posed medium risk and low risk, respectively to aquatic organisms. It should be made clear that toxicity data for soil dwelling organisms cannot be replaced by toxicity data for aquatic organisms because the effects on aquatic organisms can only be considered as effects on soil organisms that are exposed exclusively to the soil pore water of the soil [25]. A RQsoil-aquatic value of greater than one (>1) calculated from equilibrium partition approach implies tests with soil dwelling organisms should be considered an essential requirement for a refined hazard assessment. In this study, only sulfamethoxazole had RQsoil-aquatic greater than one and this antibiotic should be considered for tests with soil dwelling organisms. We evaluated RQsoil-terrestrial for sulfamethoxazole to Eisenia fetida the seedling height and root length of rice and cucumber. The RQsoil-terrestrial values were less than 0.005 for Eisenia fetida as presented in Table 5, indicating that the presence of this antibiotic in the poultry manure-amended soil posed no significant risk to earthworm. Low ecological effect of sulfamethoxazole to the seedling height and root length of cucumber was also observed. However, medium to high ecological effect of this antibiotic to the seedling height and root length of rice was likely.
Considering the benefits derived from the application of poultry manure on soil for agricultural practices but also the possible consequential threats to soil, terrestrial and aquatic environment, poultry manure should not be applied in excess and uncontrolled manner. Future studies on the occurrence and risk assessment should also include other relevant veterinary antibiotics commonly used in poultry production to have a more comprehensive overview of the effect veterinary antibiotics could pose to soil and terrestrial environment.

Conclusions

The concentration profile of three antibiotics (sulfamethoxazole, sulfadimidine and trimethoprim) was determined in poultry manure from two farms in Ibadan, Nigeria. Potential ecotoxicological risk of target antibiotics in poultry manure-amended soil, based on terrestrial toxicity data and aquatic toxicity data, was also investigated. The analytical quality parameters were satisfactory for the determination of target antibiotics in poultry manure. High levels of these antibiotics were quantified in poultry manures from the farms, up to 12.7 μg g−1, 16.1 μg g−1 and 33.8 μg g−1 for sulfamethoxazole, sulfadimidine and trimethoprim, respectively. Sulfamethoxazole and trimethoprim posed low risk to earthworms. Only sulfamethoxazole presented high risk to the aquatic organisms but may cause low ecotoxicological effect to crop plants except for the root length and seedling height of rice. We hereby recommend effective enlightenment programs for poultry farmers in Nigeria to bring about awareness on the environmental and toxicological impact of the excessive use of veterinary antibiotics in poultry farming and the adverse ecological implications of poultry manure application on farmlands.

Acknowledgement

Personnel of the investigated poultry farms are appreciated for their cooperation and assistance in the collection of poultry manure samples.

Conflict of interest

Conflict of interest
The authors declare that there is no conflict of interest

Notes

CRediT author statement
AA: Conceptualization, Methodology, Supervision, Data curation, Writing-Original draft preparation, Writing-Review & Editing; DSO: Investigation, Writing-Original draft preparation; OAB: Investigation, Writing-Original draft preparation.

References

1. Furtula V, Farrell EG, Diarrassouba F, Rempel H, Pritchard J, Diarra MS. Veterinary pharmaceuticals and antibiotic resistance of Escherichia coli isolates in poultry litter from commercial farms and controlled feeding trials. Poultry Science 2010;89(1):180-188 https://doi.org/10.3382/ps.2009-00198 .
crossref pmid
2. Awad YM, Ok YS, Igalavithana AD, Lee YH, Sonn YK, Usman AR, et al. Sulphamethazine in poultry manure changes carbon and nitrogen mineralisation in soils. Chemistry and Ecology 2016;32(10):899-918 https://doi.org/10.1080/02757540.2016.1216104 .
crossref
3. Muhammad J, Khan S, Su JQ, Hesham AEL, Ditta A, Nawab J, et al. Antibiotics in poultry manure and their associated health issues: a systematic review. J Soils Sediments 2020;20(1):486-497 https://doi.org/10.1007/s11368-019-02360-0 .
crossref
4. Quaik S, Embrandiri A, Ravindran B, Hossain K, Al-Dhabi NA, Arasu MV, et al. Veterinary antibiotics in animal manure and manure laden soil: Scenario and challenges in Asian countries. Journal of King Saud University-Science 2020;32(2):1300-1305 https://doi.org/10.1016/j.jksus.2019.11.015 .
crossref
5. Tian M, He X, Feng Y, Wang W, Chen H, Gong M, et al. Pollution by antibiotics and antimicrobial resistance in livestock and poultry manure in China, and countermeasures. Antibiotics 2021;10(5):539 https://doi.org/10.3390/antibiotics10050539 .
crossref
6. Kümmerer K. Antibiotics in the aquatic environment-a review–part I. Chemosphere 2009;75(4):417-434 https://doi.org/10.1016/j.chemosphere.2008.11.086 .
crossref pmid
7. Ding C, He J. Effect of antibiotics in the environment on microbial populations. Appl Microbiol Biotechnol 2010;87(3):925-941 https://doi.org/10.1007/s00253-010-2649-5 .
crossref pmid
8. Dolliver H, Kumar K, Gupta S. Sulfamethazine uptake by plants from manure-amended soil. J Environ Qual 2007;36(4):1224-1230 https://doi.org/10.2134/jeq2006.0266 .
crossref
9. Pan M, Chu LM. Phytotoxicity of veterinary antibiotics to seed germination and root elongation of crops. Ecotoxicology and Environmental Safety 2016;126: 228-237 http://dx.doi.org/10.1016/j.ecoenv.2015.12.027 .
crossref pmid
10. Osiński Z, Patyra E, Kwiatek K. HPLC-FLD-based method for the detection of sulfonamides in organic fertilizers collected from Poland. Molecules 2022;27(6):2031 https://doi.org/10.3390/molecules27062031 .
crossref pmid pmc
11. Zhou X, Wang J, Lu C, Liao Q, Gudda FO, Ling W. Antibiotics in animal manure and manure-based fertilizers: Occurrence and ecological risk assessment. Chemosphere 2020;255: 127006 https://doi.org/10.1016/j.chemosphere.2020.127006 .
crossref pmid
12. Ajibola AS, Awoyemi TE, Fasogbon OT, Adewuyi GO. QuEChERS-based analysis and ecotoxicological risk of select antibiotics in dumpsite leachates, hospital wastewater and effluent receiving water in Ibadan, Nigeria. Journal of Environmental Science and Health, Part A 2022;57(8):709-722 https://doi.org/10.1080/10934529.2022.2104064 .
crossref
13. Dróżdż D, Wystalska K, Malińska K, Grosser A, Grobelak A, Kacprzak M. Management of poultry manure in Poland-Current state and future perspectives. Journal of Environmental Management 2020;264: 110327 https://doi.org/10.1016/j.jenvman.2020.110327 .
crossref pmid
14. Manikandan M, Chun S, Kazibwe Z, Gopal J, Singh UB, Oh JW. Phenomenal bombardment of antibiotic in poultry: contemplating the environmental repercussions. Int J Environ Res Public Health 2020;17(14):5053 http://dx.doi.org/10.3390/ijerph17145053 .
crossref pmid pmc
15. Adelowo OO, Fagade OE, Agersø Y. Antibiotic resistance and resistance genes in Escherichia coli from poultry farms, southwest Nigeria. J Infect Dev Ctries 2014;8(9):1103-1112 https://doi.org/10.3855/jidc.4222 .
crossref
16. Ajibola AS, Tisler S, Zwiener C. Simultaneous determination of multiclass antibiotics in sewage sludge based on QuEChERS extraction and liquid chromatography-tandem mass spectrometry. Analytical Methods 2020;12(4):576-586 https://doi.org/10.1039/C9AY02188D .
crossref
17. Ajibola AS, Amoniyan OA, Ekoja FO, Ajibola FO. QuEChERS approach for the analysis of three fluoroquinolone antibiotics in wastewater: Concentration profiles and ecological risk in two Nigerian hospital wastewater treatment plants. Arch Environ Contam Toxicol 2021;80(2):389-401 https://doi.org/10.1007/s00244-020-00789-w .
crossref pmid
18. OIE (World Organisation for Animal Health). OIE list of antimicrobial agents of veterinary importance. 2021; Paris, France: Accessed on 01 September, 2022. https://www.oie.int/app/uploads/2021/06/a-oie-list-antimicrobials-june2021.pdf .

19. Guo C, Wang M, Xiao H, Huai B, Wang F, Pan G, et al. Development of a modified QuEChERS method for the determination of veterinary antibiotics in swine manure by liquid chromatography tandem mass spectrometry. J Chromatogr B 2016;1027: 110-118 https://doi.org/10.1016/j.jchromb.2016.05.034 .
crossref
20. Ghirardini A, Grillini V, Verlicchi P. A review of the occurrence of selected micropollutants and microorganisms in different raw and treated manure – Environmental risk due to antibiotics after application to soil. Sci Total Environ 2020;707: 136118 https://doi.org/10.1016/j.scitotenv.2019.136118 .
crossref pmid
21. EC-TGD. Technical Guidance Document on Risk Assessment in Support of Commission Directive 93/67/EEC on Risk Assessment for New Notified Substances, Commission Regulation (EC) No 1488/94 on Risk Assessment for Existing Substances and Directive 98/8/EC of the European Parliament and of the Council Concerning the Placing of Biocidal Products on the Market, Parts I, II and IV. European Communities 2003; EUR 20418 EN/1; https://echa.europa.eu/documents/10162/987906/tgdpart2_2ed_en.pdf/138b7b71-a069-428e-9036-62f4300b752f .

22. Pino MR, Val J, Mainar AM, Zuriaga E, Español C, Langa E. Acute toxicological effects on the earthworm Eisenia fetida of 18 common pharmaceuticals in artificial soil. Sci Total Environ 2015;518: 225-237 https://doi.org/10.1016/j.scitotenv.2015.02.080 .
crossref pmid
23. Liu F, Ying GG, Tao R, Zhao JL, Yang JF, Zhao LF. Effects of six selected antibiotics on plant growth and soil microbial and enzymatic activities. Environmental Pollution 2009;157(5):1636-1642 http://doi.org/10.1016/j.envpol.2008.12.021 .
crossref pmid
24. Ajibola AS, Zwiener C. Occurrence and risk assessment of antibiotic residues in sewage sludge of two Nigerian hospital wastewater treatment plants. Water Air Soil Pollut 2022;233: 405 https://doi.org/10.1007/s11270-022-05875-4 .
crossref
25. ECHA. 2008. Guidance on information requirements and chemical safety assessment chapter R.10: Characterization of dose [concentration] - response for environment (65); European Chemicals Agency; Helsinki, Finland: https://echa.europa.eu/documents/10162/13632/information_requirements_r10_en.pdf/bb902be7-a503-4ab7-9036-d866b8ddce69 .

26. ECHA. 2016. Guidance on information requirements and chemical safety assessment chapter R.16: Environmental exposure assessment. ECHA-16-G-03-EN (178); European Chemicals Agency; Helsinki, Finland: https://echa.europa.eu/documents/10162/13632/information_requirements_r16_en.pdf/b9f0f406-ff5f-4315-908e-e5f83115d6af .

27. Kim S, Aga DS. Potential ecological and human health impacts of antibiotics and antibiotic-resistant bacteria from wastewater treatment plants. Journal of Toxicology and Environmental Health, Part B 2007;10(8):559-573 https://doi.org/10.1080/15287390600975137 .
crossref pmid
28. Iatrou EI, Stasinakis AS, Thomaidis NS. Consumption-based approach for predicting environmental risk in Greece due to the presence of antimicrobials in domestic wastewater. Environmental Science & Pollution Research 2014;21(22):12941-12950 https://doi.org/10.1007/s11356-014-3243-7 .
crossref pmid
29. Isidori M, Lavorgna M, Nardelli A, Pascarella L, Parrella A. Toxic and genotoxic evaluation of six antibiotics on non-target organisms. Sci Total Environ 2005;346(1):87-98 https://doi.org/10.1016/j.scitotenv.2004.11.017 .
crossref pmid
30. Sanderson H, Johnson DJ, Wilson CJ, Brain RA, Solomon KR. Probabilistic hazard assessment of environmentally occurring pharmaceuticals toxicity to fish, daphnids and algae by ECOSAR screening. Toxicol Lett 2003;144(3):383-395 https://doi.org/10.1016/S0378-4274(03)00257-1 .
crossref pmid
31. De Liguoro M, Fioretto B, Poltronieri C, Gallina G. The toxicity of sulfamethazine to Daphnia magna and its additivity to other veterinary sulfonamides and trimethoprim. Chemosphere 2009;75(11):1519-1524 https://doi.org/10.1016/j.chemosphere.2009.02.002 .
crossref pmid
32. Yang Y, Owino AA, Gao Y, Yan X, Xu C, Wang J. Occurrence, composition and risk assessment of antibiotics in soils from Kenya, Africa. Ecotoxicology 2016;25(6):1194-1201 https://doi.org/10.1007/s10646-016-1673-3 .
crossref pmid
33. Eguchi K, Nagase H, Ozawa M, Endoh YS, Goto K, Hirata K, et al. Evaluation of antimicrobial agents for veterinary use in the ecotoxicity test using microalgae. Chemosphere 2004;57(11):1733-1738 https://doi.org/10.1016/j.chemosphere.2004.07.017 .
crossref pmid
34. Ilyas H, Masih I, van Hullebusch ED. The anaerobic biodegradation of emerging organic contaminants by horizontal subsurface flow constructed wetlands. Water Science & Technology 2021;83(11):2809-2828 https://doi.org/10.2166/wst.2021.178 .
crossref pmid
35. Thiele-Bruhn S. Pharmaceutical antibiotic compounds in soils-a review. Journal of Plant Nutrition and Soil Science 2003;166(2):145-167 https://doi.org/10.1002/jpln.200390023 .
crossref
36. Shigei M, Assayed A, Hazaymeh A, Dalahmeh SS. Pharmaceutical and antibiotic pollutant levels in wastewater and the waters of the Zarqa River, Jordan. Applied Sciences 2021;11(18):8638 https://doi.org/10.3390/app11188638 .
crossref
37. Verlicchi P, Zambello E. Pharmaceuticals and personal care products in untreated and treated sewage sludge Occurrence and environmental risk in the case of application on soil-A critical review. Sci Total Environ 2015;538: 750-767 https://doi.org/10.1016/j.scitotenv.2015.08.108 .
crossref
38. Barron L, Havel J, Purcell M, Szpak M, Kelleher B, Paull B. Predicting sorption of pharmaceuticals and personal care products onto soil and digested sludge using artificial neural networks. Analyst 2009;134(4):663-670 https://doi.org/10.1039/B817822D .
crossref pmid
39. Hou J, Wan W, Mao D, Wang C, Mu Q, Qin S, et al. Occurrence and distribution of sulfonamides, tetracyclines, quinolones, macrolides, and nitrofurans in livestock manure and amended soils of Northern China. Environ Sci Pollut Res 2015;22(6):4545-4554 https://doi.org/10.1007/s11356-014-3632-y .
crossref pmid
40. Teglia CM, Peltzer PM, Seib SN, Lajmanovich RC, Culzoni MJ, Goicoechea HC. Simultaneous multiresidue determination of twenty one veterinary drugs in poultry litter by modeling three-way liquid chromatography with fluorescence and absorption detection data. Talanta 2017;167: 442-452 http://dx.doi.org/10.1016/j.talanta.2017.02.030 .
crossref pmid
41. Li Y, Zhang X, Li W, Lu X, Liu B, Wang J. The residues and environmental risks of multiple veterinary antibiotics in animal faeces. Environ Monit Assess 2013;185(3):2211-2220 https://doi.org/10.1007/s10661-012-2702-1 .
crossref pmid
42. Karci A, Balcioglu IA. Investigation of the tetracycline, sulfonamide, and fluoroquinolone antimicrobial compounds in animal manure and agricultural soils in Turkey. Sci Total Environ 2009;407(16):4652-4664 https://doi.org/10.1016/j.scitotenv.2009.04.047 .
crossref pmid
43. Ji X, Shen Q, Liu F, Ma J, Xu G, Wang Y, et al. Antibiotic resistance gene abundances associated with antibiotics and heavy metals in animal manures and agricultural soils adjacent to feedlots in Shanghai; China. J Hazard Mater 2012;235: 178-185 https://doi.org/10.1016/j.jhazmat.2012.07.040 .
crossref pmid
44. Shevchenko LV, Dobrozhan YV, Mykhalska VM, Osipova TY, Solomon VV. Contamination of hen manure with nine antibiotics in poultry farms in Ukraine. Regulatory Mechanisms in Biosystems 2019;10(4):532-537 https://doi.org/10.15421/021978 .
crossref
45. Zhao L, Dong YH, Wang H. Residues of veterinary antibiotics in manures from feedlot livestock in eight provinces of China. Sci Total Environ 2010;408(5):1069-1075 https://doi.org/10.1016/j.scitotenv.2009.11.014 .
crossref pmid
46. Zheng Y, Fan L, Dong Y, Li D, Zhao L, Yuan X, et al. Determination of sulfonamide residues in livestock and poultry manure using carbon nanotube extraction combined with UPLC-MS/MS. Food Anal Methods 2020;14(4):641-652 https://doi.org/10.1007/s12161-020-01910-4 .
crossref
47. Xue J, Wu J, Hu Y, Sha C, Yao S, Li P, et al. Occurrence of heavy metals, antibiotics, and antibiotic resistance genes in different kinds of land-applied manure in China. Environ Sci Pollut Res 2021;28(29):40011-40021 https://doi.org/10.1007/s11356-021-13307-9 .
crossref pmid
48. Topi D, Spahiu J. Presence of veterinary antibiotics in livestock manure in two Southeastern Europe countries, Albania and Kosovo. Environ Sci Pollut Res 2020;27(35):44552-44560 https://doi.org/10.1007/s11356-020-10341-x .
crossref pmid
49. Patyra E, Kwiatek K, Nebot C, Gavilán RE. Quantification of veterinary antibiotics in pig and poultry feces and liquid manure as a non-invasive method to monitor antibiotic usage in livestock by liquid chromatography mass-spectrometry. Molecules 2020;25(14):3265 https://doi.org/10.3390/molecules25143265 .
crossref pmid pmc

Figure 1
Map showing the study location.
eaht-37-4-e2022038f1.jpg
Figure 2
RQsoil-aquatic of target veterinary antibiotics in poultry manure-amended soil based on aquatic toxicity data.
eaht-37-4-e2022038f2.jpg
Table 1
Terrestrial ecotoxicological data of target antibiotics.
Antibiotic Ecological endpoint Toxic effect Concentration (mg/kg) Referencesa Assessment factor PNECsoil-terrestrial (μg Kg−1) PNECsoil-terrestrial (μg Kg−1)
Sulfamethoxazole Eisenia fetida LC50 >4000 [22] 1000 4000 4
Rice Seedling height(EC50) 38 1000 38 0.038
Root length (EC50) 13 1000 13 0.013
Cucumber Seedling height(EC50) >300 [23] 1000 300 0.3
Root length (EC50) >300 1000 300 0.3
Sulfadimidine Rice Seedling height(EC50) 220 1000 220 0.22
Root length (EC50) 43 1000 43 0.043
Cucumber Seedling height(EC50) 300 [23] 1000 300 0.3
Root length (EC50) >300 1000 300 0.3
Trimethoprim Eisenia fetida LC50 >2000 [22] 1000 2000 2
Rice Seedling height (EC50) >300 1000 300 0.3
Root length (EC50) >300 [23] 1000 300 0.3
Cucumber Seedling height (EC50) >300 1000 300 0.3
Root length (EC50) >300 1000 300 0.3

a Toxicity data with references were adapted from Ajibola and Zwiener [24]

Table 2
Aquatic toxicity data (EC50/LC50) of target antibioticsa
Antibiotics Aquatic organisms Exposure time EC50/LC50 (mg/L) Referencesb KOC Kd (soil) PNEC soil-aquatic (ng g−1) PNEC soil-aquatic (μg g−1)

Value (L/kg) References Value (L/kg) References
Fish 96 h 562.5 [27,28]
Sulfamethoxazole Daphnia 7 days 0.21 [28,29] 258 [34] 37.6 [37] 0.14 0.00014
Algae 96 h 0.03 [28]
Fish 517 [30]
Sulfadimidine Daphnia 48 h 202 [31,32] 208 [35] 98.25 [37] 143.90 0.1439
Algae 38 [30]
Fish 96 h 1870.43 [28]
Trimethoprim Daphnia 48 h 92 [28] 905 [36] 26 [38] 1292.82 1.2928
Algae 96 h 80.39696 [28,33]

a Values (in bold) were used for calculating PNECwater

b Toxicity data, Koc and Kd(soil) values, and their corresponding references were adapted from Ajibola and Zwiener [24]

Table 3
Analytical quality parameters for determination of target antibiotics in poultry manure.
Antibiotics Recovery (%) (5 μg g−1 spike) Precision (%RSD) LOD (μg g−1) LOQ (μg g−1) R2
Sulfamethoxazole 77.4 24 0.46 1.40 0.9992
Sulfadimidine 136.5 13 0.04 0.13 0.9991
Trimethoprim 103.5 16 0.18 0.55 0.9948
Table 4
Measured environmental concentration (MEC) in poultry manure and Predicted Environmental Concentration (PEC) of antibiotics in poultry manure-amended soil.
MECmanure (μg g−1) PECsoil (μg g−1)
Antibiotics 1st sampling 2nd sampling 1st sampling 2nd sampling
Farm A Farm B Farm A Farm B Farm A Farm B Farm A Farm B
Sulfamethoxazole 5.2 12.7 5.1 9.9 0.0076 0.0187 0.0075 0.0145
Sulfadimidine 16.1 nd nd nd 0.0237 nc nc nc
Trimethoprim 8.7 nd 6.6 33.8 0.0128 nc 0.0097 0.0497

nd-not detected, nc-not calculated because compound was not detected in poultry manure.

Table 5
Risk quotients of antibiotics for terrestrial organisms (RQsoil-terrestrial) in poultry manure-amended soil.
Antibiotic Ecotoxicological end points PNECsoil-terrestrial (μg g−1) Risk quotient (RQsoil-terrestrial)
1st sampling 2nd sampling
Farm A Farm B Farm A Farm B
Eisenia fetida (earthworm) 4 0.002 0.005 0.002 0.004
Sulfamethoxazole Rice (Seedling height) 0.038 0.200 0.492 0.197 0.382
Rice (Root length) 0.013 0.585 1.438 0.577 1.115
Cucumber (Seedling height) 0.3 0.025 0.062 0.025 0.048
Cucumber (Root length) 0.3 0.025 0.062 0.025 0.048
Rice (Seedling height) 0.22 0.108 nc nc nc
Sulfadimidine Rice (Root length) 0.043 0.551 nc nc nc
Cucumber (Seedling height) 0.3 0.079 nc nc nc
Cucumber (Root length) 0.3 0.079 nc nc nc
Trimethoprim Eisenia fetida (earthworm) 2 0.006 nc 0.005 0.025
Rice/cucumber (seedling height) 0.3 0.043 nc 0.032 0.166
Rice/cucumber (Root length) 0.3 0.043 nc 0.032 0.166
TOOLS
PDF Links  PDF Links
PubReader  PubReader
ePub Link  ePub Link
XML Download  XML Download
Full text via DOI  Full text via DOI
Download Citation  Download Citation
  Print
Share:      
METRICS
4
Crossref
0
Scopus
3,715
View
53
Download
Editorial Office
Division of Environmental Science and Ecological Engineering, Korea University
145 Anam-ro, Seongbuk-gu, Seoul 02841, Korea
Tel : +82-32-560-7520   E-mail: envitoxic@gmail.com
About |  Browse Articles |  Current Issue |  For Authors and Reviewers
Copyright © 2024 by The Korean Society of Environmental Health and Toxicology & Korea Society for Environmental Analysis.     Developed in M2PI