Korean J. Soil Sci. Fert. Vol.53, No.2, pp , 2020 Korean Journal of Soil Science and Fertilizer Article

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1 Korean J. Soil Sci. Fert. Vol.53, No.2, pp , 2020 Korean Journal of Soil Science and Fertilizer Article pissn : eissn : Occurrence of Veterinary Antibiotics in the Agro-Environment Jin Wook Kim 1, Young Kyu Hong 2, and Sung Chul Kim 3 * 1 Master's Student, Department of Bio Environmental Chemistry, Chungnam National University, Daejeon 34134, Korea 2 Doctoral Student, Department of Bio Environmental Chemistry, Chungnam National University, Daejeon 34134, Korea 3 Professor, Department of Bio Environmental Chemistry, Chungnam National University, Daejeon 34134, Korea *Corresponding author: sckim@cnu.ac.kr A B S T R A C T Received: May 27, 2020 Revised: May 29, 2020 Accepted: May 29, 2020 ORCID Sung Chul Kim Veterinary antibiotics (Vas) in agro-environment has been concerned because of antibiotic resistance genes (ARGs) production. The objective of this research was to monitor VAs in the agro-environment such as soil, sediment, and surface water near at the confined animal feeding operation (CAFOs). Total of 6 VAs including tetracycline (TC), chlortetracycline (CTC), oxytetracycline (OTC), sulfamethazine (SMT), sulfamethoxazole (SMX), and sulfathiazole (STZ) were monitored. Extraction of VAs was conducted with solid phase extraction (SPE) and quantified with high performance liquid chromatography mass spectrometry (HPLC/MS/MS). Result showed that only SMX was observed among 6 VAs and concentration range was following: soil ( µg kg -1 ), sediment ( µg kg -1 ), surface water ( µg L -1 ). Correlation analysis showed that soil ph was negatively correlated with SMX concentration in soil (correlation coefficient: -0.66) indicating that less SMX was observed as soil ph was increased. The reason for negative correlation between soil ph and SMX concentration in soil was that SMX was negatively charged at higher soil ph and electric repulsion could be occurred between soil particles and SMX. However, more detailed research would be necessary to verify the occurrence, fate, and transport of VAs in agro-environment. Keywords: Antibiotics, Emerging contaminants, Environment, Sulfonamide, Tetracycline Descriptive explanation of sulfamethoxazole (SMX) in the agro-environment. C The Korean Society of Soil Science and Fertilizer. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non- Commercial License ( which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

2 Occurrence of Veterinary Antibiotics in the Agro-Environment 223 Introduction 전세계적으로가축사육수가증가함에따라가축의질병예방및치료, 그리고성장촉진등을위해항생제소비량이증가하고있다 (Yao et al., 2017). 선행연구에따르면 2030년까지전세계항생제의소비가 2010년과비교하여약 67% 정도증가할수있다는예측보고가있으며 (Van Boeckel et al., 2015) 국내의경우가축에사용되는항생제가 2009년부터 2018년까지평균 950톤 (820-1,046톤 ) 가량소비되었다 (Seo et al., 2018a, 2018b). 항생제의오남용은항생제저항유전자 (Antibiotic resistance genes) 를생성할수있으며특히농업환경에서는체외로배출된항생제가환경중에잔류할수있는확률이높아진다 (Awad et al., 2015; Kim et al., 2019). 가축에게투여된항생제는가축의체내에서 10-20% 정도만이사용되고나머지는체외로배출되는특성이있다 (Hong et al., 2019; Jjemba, 2002). 체외로배출된항생제는주로분뇨에잔류하며농업환경에서작물의공급및토양질개선등을위해분뇨는퇴비화되어농경지에사용된다 (Larney et al., 2006). 이과정에서퇴비에잔류하는항생제가토양에유입되며강우에의해지하수또는지표수로유입되어잔류하게된다 (Kummerer, 2009; Qiao et al., 2012; Boy-Roura et al., 2018). 또한농경지에잔류한항생제는작물재배시작물체로전이하여작물체내에축적되거나생장을억제하기도한다 (Kong et al., 2007; Hillis et al., 2011; Pan and Chu, 2016, 2017). 농업환경에잔류하는항생제의농도는항생제종류및지역별특성에따라매우상이하다. 네덜란드의가축농장지역지하수를대상으로잔류항생제를분석한결과 sulfamethazine는 ng L -1 의범위로 22개항생물질중가장많은지역에서검출되었고, sulfamethoxazole의경우최대 18 ng L -1 까지검출되었다 (Kivits et al., 2018). 중국의경우축사주변환경에서잔류항생제에대한모니터링결과분뇨와토양에서각각최대 mg kg -1, 1, µg kg -1 의 chlortetracycline을검출하였다 (An et al., 2015). 국내의경우농업환경중토양과저니토에서각각 sulfamethazine ( µg kg -1 ), tetracycline ( µg kg -1 ), chlortetracycline ( µg kg -1 ) 등이검출되었고 (Kim et al., 2017), 지하수에서 sulfamethazine ( ng L -1 ) 이검출되었다 (Hong et al., 2019). 본연구의목적은농업환경에잔류하는항생제의잔류농도를모니터링하기위해가축농장인근농경지토양과하천수및저니토내잔류항생제를모니터링하고토양의이화학적특성중항생제의잔류특성에영향을미치는인자를규명하고자하였다. Materials and Methods Chemicals 본시험에서는테트라사이클라인 (Tetracycline, TCs) 계열항생제 3종류, 테트라사이클라인 (TC), 클로르테트라사이클라인 (CTC), 옥시테트라사이클라인 (OTC) 과설폰아마이드 (sulfonamide, SAs) 계열항생제 3 종류, 설파메타진 (SMT), 설파메토자졸 (SMX), 설파티아졸 (STZ) 을대상으로모니터링을실시하였다. 각항생제의표준품 (stock) 은순도가 90-99% 인분말형태의시약을사용하였으며표준용액 (standard solution) 은표준품 10 mg을 10 ml의메탄올 (MeOH) 에용해시켜 1,000 mg L -1 의농도로제조한후증류수에희석하여실험에사용하였다. 모든표준용액은 4 C 에서냉장보관하였다. Sample collection 농촌지역의항생제잔류농도를모니터링하기위해경기지역에위치한가축농장을중심으

224 Korean Journal of Soil Science and Fertilizer Vol. 53, No. 2, 2020 로반경 0.5 Km 이내주변농경지토양 8 지점, 저니토 2지점, 그리고하천수 2 지점을선별하였으며대조구는산림토양을채취하였다 (Fig. 1). 각시료지점에대한설명은 Table 1에정리하였다.

3 224 Korean Journal of Soil Science and Fertilizer Vol. 53, No. 2, 2020 로반경 0.5 Km 이내주변농경지토양 8 지점, 저니토 2지점, 그리고하천수 2 지점을선별하였으며대조구는산림토양을채취하였다 (Fig. 1). 각시료지점에대한설명은 Table 1에정리하였다. 토양시료는휴대용토양채취기를이용하여표토 (0-15 cm) 를채취하였으며각시료채취지점당 3-5개의시료를채취한후하나의시료로합쳐대표시료를만들었다. 하천수시료는샘플용기를하천수로 2-3회세척한후기포가생기지않도록채수병을가득채워시료를채취하였다. 저니토시료는하천수시료를채취한동일지점에서채취하였으며휴대용시료채취기를이용하여 Fig. 1. Sampling locations for veterinary antibiotic analysis. S, SE, and SW represent soil, sediment, and surface water respectively. CAFO stands for confined animal feeding operation. Table 1. Site description and chemical properties of samples. Sample ID Description ph EC OM P 2 O 5 NO 3 -N (1:5) ds m -1 g kg -1 mg kg -1 mg kg -1 C Control (Forest) S1 Upland S2 Upland S3 Upland S4 Paddy S5 Upland S6 Paddy S7 Paddy S8 Orchard SE1 Sediment SE2 Sediment SW1 Surface water SW2 Surface water All values are average of triplicate measurement.

4 Occurrence of Veterinary Antibiotics in the Agro-Environment 225 주변저니토 2-3지점의시료를하나로합쳐대표시료를만들었다. 채취된시료는얼음이채워진아이스박스에옮겨실험실로운반한후토양과저니토시료는암조건에서풍건하였으며풍건된시료는 2 mm로체거름하여상온 (20 C) 에서보관하였다. 하천수시료는 0.45 µm 공극크기의여과지로여과한후 4 C에서냉장보관하였다. Chemical analysis 토양과저니토의화학적특성분석은국립농업과학원의토양및식물체분석법을참조하였으며하천수의화학적특성분석은수질오염공정시험법 (MOE, 2004) 을참조하였다. 토양과저니토의 ph와전기전도도 (EC) 는각각 ph (MP 220 Mettler Toledo, USA) 와 EC meter (Mettler Toledo, S230, USA) 를사용하여측정하였다. 유기물함량과유효인산농도는각각 Walkley Black 방법과 Bray No.1 방법을이용하여전처리후 UV/vis spectrometry (UV 240, Schimadzu, Japan) 의 610, 660 nm 파장에서비색정량하였다. 토양과저니토의 NO 3 -N 농도는습토 10 g을 2M KCl 50 ml로 30분간진탕한후 Whatman No. 2 여과지로여과한후자동원소분석기 (Thermo Fisher, Gallery, USA) 를이용하여측정하였다 (Lee et al., 2017). 하천수의 ph, EC, NO 3 -N은모두동일기기를사용하여측정하였다. Sample preparation and solid phase extraction (SPE) 토양, 저니토, 및하천수내잔류항생제분석을위한전처리과정과고형상추출법 (SPE) 방법은선행연구를참조하였다 (Kim et al., 2019). 토양및저니토시료 1 g을튜브에넣고 Mcllvaine 완충용액을이용하여 2번추출한후총 40 ml의추출제에증류수를혼합하여총 120 ml이되도록한후 0.45 µm 공극의여과지를이용하여감압추출하였다. 하천수의경우시료 120 ml를 250 ml 삼각플라스크에넣고 40% (v/v) 로희석한황산 (H 2 SO 4 ) 용액을이용하여시료의 ph를 으로조절하였다. 그후 5% Na 2 EDTA (w/v) 0.5 ml를넣고 15분동안 150 rpm에서교반하였다. 전처리된토양및저니토시료와교반된하천수시료는 manifold (Visiprep, Supelco, USA) 를이용하여고형상추출 (SPE) 을시행하였다. 고형상추출에사용된카트리지는 Oasis HLB (3cc/60 mg, Waters, USA) 였으며시료를포집하기전메탄올 (MeOH), 0.5N (v/v) 염산용액, 증류수를각각 3 ml씩순차적으로카트리지에흘려주어카트리지를활성화시켰다. 시료의포집속도는 3 ml min -1 정도로유지하였으며포집이끝난후에는증류수를이용하여 3 ml 씩 3회 ( 총 9 ml) 세척하였다. 카트리지에포집된항생제를추출하기위해 15 ml 튜브 (conical bottom centrifuge tube) 에내부표준물질 (internal standard) 인 simeton (0.24 mg L -1 ) 0.05 ml를넣고메탄올 5 ml로용리 (elution) 하였다. 용리된시료는질소농축기 (N-Evap-11. OASYS, USA) 에서 50 C 항온조건을유지하여 50 µl까지농축후 70 µl의이동상용액 (mobile phase A, 0.1% formic acid % HPLC water) 을넣고진동혼합후기기분석에사용하였다. HPLC/MS/MS analysis 항생제정량을위한분석기기는액체크로마토그래피 (Agilent 1200, USA) 와질량분석기 (API, 6000 Q TRAP, ABSCIEX, Canada) 를사용하였으며컬럼은공극크기가 3.5 µm이며, 내경이 4.6mm인 ZORBAX Eclipse Plus C 18 컬럼을사용하였다. 이동상 (Mobile phase) A는 99.9% D.I water + 0.1% formic acid, B 는 99.9% acetonitrile + 0.1% formic acid를사용하였으며유속은 0.7 ml min -1 으로조절하였다. 내부표준물질과 6 종류의항생제는다성분분석을통해동시분석하였으며총분석시간은 15분이소요되었다.

5 226 Korean Journal of Soil Science and Fertilizer Vol. 53, No. 2, 2020 QA/QC and statistical analysis 항생제정량을위한분석조건의정도관리 (QA/QC) 를위해회수율 (recovery) 과정량한계 (LOD, Limit of Quantification) 를산출하였다. 회수율검증과정량한계산출방법은선행연구 (Kim et al., 2019) 를참조하였다. 모든분석결과는 3반복실험결과의평균값을이용하였으며유의성검정을위해유의수준 95% 수준 (p < 0.05) 에서 ANOVA 분석을실시하여각결과값의유의성을검증하였다. Results and Discussion Chemical properties of groundwater 토양, 저니토, 및하천수의화학적특성은 Table 1에정리하였다. 토양의 ph는 의범위를나타냈으며논토양의 ph ( ) 가밭토양 ( ) 또는과수원토양 (6.41) 의 ph에비해낮게조사되었다. 국내논토양의평균 ph는 범위를나타내며밭토양및과수원토양의평균 ph 는 의범위를나타내어조사지점의토양 ph는국내농경지토양의평균범위에포함되었다 (Choi et al., 2018). 전기전도도역시논토양의 EC ( ds m -1 ) 가밭토양 ( ds m -1 ) 과과수원토양 (0.57 ds m -1 ) 의 EC 값에비해낮았다. 논토양의 ph와 EC는담수여부에따라변화가나타나며담수조건에서산성토양의경우토양 ph가상승하는경향이있는반면비담수조건에서는토양 ph가낮아지는경향이있다. 시료채취시기가비담수기간 (3월) 인점을고려하였을경우논토양의 ph가밭토양또는과수원토양에비해낮은경향을나타내었다. 토양의유기물함량과유효인산의농도는각각 g kg -1, mg kg -1 의범위로조사되었다. 국내농경지토양의적정유기물함량은 g kg -1 이며유효인산농도의경우논토양 ( mg kg -1 ), 밭토양과과수원토양 ( mg kg -1 ) 을감안할경우조사지역의유기물함량은 S1과 S3 지점을제외하고는적정범위에비해높은함량을가지고있었으며유효인산의경우논토양에서는적정범위보다높은농도의유효인산농도가함유되었으나밭토야에서는적정범위에비해낮은함량의유효인산이포함된것으로조사되었다. Recovery and limit of quantification of antibiotics 토양, 저니토, 그리고하천수의잔류항생제정량을위한분석조건의회수율과정량한계는 Table 2에정리하였다. 총 6 종류의항생제에대한정량곡선은 mg L -1 범위에서산정하였고 R 2 값은 6 종류모두 로계산되었다. 각항생제의회수율은하천수 (89-112%), 토양 (72-90%), 저니토 (72-86%) 범위에서산출되었으며정량한계는하천수 (0.02 µg L -1 ), 토양과저니토 ( (µg kg -1 ) 로산출되었다. Table 2. Summary of QA and QC for quantification of antibiotics (n=3). Recovery (%) LOQ (µg L -1 / µg kg -1 ) Antibiotics Range of calibration curve (mg kg -1 ) R 2 Water Soil Sediment (Water/Soil and Sediment) TC /0.25 CTC /0.19 OTC /0.24 SMT /0.02 SMX /0.15 STZ /0.07

6 Occurrence of Veterinary Antibiotics in the Agro-Environment 227 (a) (b) Fig. 2. Occurrence of veterinary antibiotics (SMX) in (a) soil and sediment, and (b) surface water. Occurrence of veterinary antibiotics 농촌지역가축농장을중심으로인근토양및저니토와지표수내의잔류항생제농도는 Fig. 2에정리하였다. 총 6 종류의항생제중 SMX만이모든토양및저니토와지표수에서검출되었다. 토양의경우 SMX의검출농도는 µg kg -1 의범위였으며저니토에서의 SMX 검출농도는 µg kg -1, 그리고하천수에서의 SMX 검출농도는 µg kg -1 수준이었다. 가축농장을기준으로가장아래지점에위치해있는 S6 지점의토양내 SMX 농도가 0.11 µg kg -1 로가장높았으며 S1, S2 지점의 SMX 농도가 0.04, 0.03 µg kg -1 로가장낮았다. 설폰아마이드계열의항생제는약산성의극성 (polar) 을나타내며물에잘녹고 K ow ( 물-유기용매분배계수 ) 의값 (log K ow : ) 이낮아주변하천수또는지하수로유입가능성이높은계열의항생제이다 (Wang and Wang, 2015; Chen et al., 2017; Chen and Xie, 2018). 국내농촌지역의토양내잔류항생제농도를보면 SAs의경우 µg kg -1 의범위에서검출되었으며 SMX와 STZ의검출빈도가가장높았다 (Kim et al., 2019). 국외의경우설파메타진 (SMT) 의토양내잔류농도가 ND (not detected) µg kg -1 의범위에서검출되었으며 (Ostermann et al., 2014) Garcia-Galan et al. (2013) 의연구에의하면총 16 종류 SAs의토양내검출농도를모니터링결과총 17개지점의샘플중에서 47% 인 8개의샘플에서 SAs가검출되었고평균검출농도는 µg kg -1 의범위로조사되었다 (Garcia-Galan et al., 2013). 국내외농업환경에서의 SAs 항생제검출분포결과를비교하였을경우지역별특성에따라검출농도는상이하였으며이는지역에따른사용되는항생제의종류, 항생제의환경유출경로, 그리고항생제의환경내거동특성에따라다를수있다는점을나타낸다. Correlation between chemical properties and veterinary antibiotics in the groundwater 토양의화학적특성과 SMX의상관관계는 Table 3에정리하였다. SMX의토양내잔류특성과상관관계가가장높은화학적특성은토양 ph로역의상관관계 (-0.66) 를나타냈으며 95% 신뢰수준 (p-value = 0.03) 에서통계적으로유의하였다. 항생제는토양의 ph에따라양이온, zwitter 이온, 그리고음이온으로존재가가능하다 (Wang and Wang, 2015). SAs 계열의항생제경우 2개의 pka (pk a1 : 1.7, pk a2 : 5.6) 를가지고있으며토양의 ph에따라 SAs의존재형태가달라지고이에따른흡착특성이달라진다.

7 228 Korean Journal of Soil Science and Fertilizer Vol. 53, No. 2, 2020 Table 3. Correlation analysis between chemical properties of soil and SMX. ph EC OMP 2 O 5 NO 3 -N SMX ph 1.00 EC OM P 2 O ** 1.00 NO 3 -N ** 1.00 SMX -0.66* *Denotes that correlation was significantly different at p < ** Denotes that correlation was significantly different at p < 토양의 ph가 5.6 이상인경우 SAs는음이온의형태로존재하며토양의 ph가 1.7과 5.6 사이에서는중성의형태로존재한다 (Chen et al., 2017). 따라서토양의 ph가증가함에따라 SAs의흡착은감소하게된다 (Wang and Wang, 2015; Park and Huwe, 2016). 토양내유기물함량또한항생제의토양잔류특성에영향을나타낸다. SAs 계열의항생제는아닐린 (aniline) 그룹과아마이드 (amide) 그룹의작용기를포함하고있다. 두그룹의작용기는토양에흡착하는특성이높지않으며 SAs 와유기물의흡착은 SAs 계열에함유되어있는알킬그룹 (R-SAs) 과유기물의양이온교환 (cationic exchange) 메커니즘으로주로발생한다 (Gao and Pedersen, 2005). SMX의경우토양내흡착계수 (K d ) 가 ,383.3 L kg -1 의넓은범위를나타내며이는토양내용존탄소 (DOC, Dissolved Organic Carbon) 함량과상관관계가있어용존탄소함량이높을수록 SMX의토양흡착계수는증가하였다 (Chen et al., 2017). 하지만본연구에서는토양내유기물함량과 SMX의상관계수가 0.19로통계적으로유의한상관관계 (p-value = 0.59) 는없었지만양의상관관계를나타내어유기물함량이증가할수록 SMX의잔류확률도증가하였다는것을알수있었다. Conclusions 농촌지역의가축농장을중심으로토양, 저니토, 그리고하천수에서의잔류항생제를모니터링하였다. 총 6종류의 TCs와 SAs 항생제중 SMX 만이토양, 저니토, 하천수에서검출되었다. SMX의검출농도는토양 ( µg kg -1 ), 저니토 ( µg kg -1 ), 그리고하천수 ( µg kg -1 ) 였으며가축농장과의거리적상관성은없었다. 토양의화학적특성과 SMX의잔류농도에대한상관관계분석결과토양 ph가 SMX의잔류농도와통계적으로유의한음의상관관계 (-0.66, p-value = 0.03) 를나타내어토양의 ph가증가할수록 SMX의잔류농도는감소함을알수있었다. 이는 SMX의 pk a 값에따라토양 ph가 pk a2 값보다높을경우 SMX는음이온의형태로환경에잔류하게되고토양 ph가높아짐에따라전기인력적반발력에의해 SMX의토양흡착이감소하게되어 SMX의잔류농도는감소하였다. Acknowledgement This study was financially supported by research fund of Chungnam National University in 2018.

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