氟喹諾酮類抗生素環(huán)境行為及其生態(tài)毒理研究進展

孟磊，楊兵，薛南冬

中國環(huán)境科學研究院 環(huán)境基準與風險評估國家重點實驗室，北京100012

氟喹諾酮類抗生素環(huán)境行為及其生態(tài)毒理研究進展

孟磊，楊兵，薛南冬*

中國環(huán)境科學研究院 環(huán)境基準與風險評估國家重點實驗室，北京100012

氟喹諾酮類抗生素(FQs)是治療人和動物細菌性感染的高效廣譜抗菌藥，隨著氟喹諾酮類抗生素在禽畜養(yǎng)殖業(yè)的廣泛使用，由此引起的環(huán)境污染受到人們的關注。本文綜述了氟喹諾酮類抗生素在水體、土壤/沉積物中的污染現(xiàn)狀、吸附降解環(huán)境行為及其生態(tài)毒理研究進展。FQs抗生素的環(huán)境行為和風險應從環(huán)境多介質層面進行評估，同時應加強對生態(tài)毒性機理以及與其他環(huán)境污染物的聯(lián)合毒性效應的研究。

氟喹諾酮；抗生素；污染現(xiàn)狀；環(huán)境行為；吸附和降解；生態(tài)毒理

氟喹諾酮類(fluoroquinolones, FQs)抗生素是一類由人工合成的廣譜類抗菌藥，是喹諾酮的哌嗪基派生物，它通過抑制細菌的DNA解旋酶II(topoisomerase II)和拓撲異構酶IV(topoisomerase IV)而影響細菌的DNA復制過程[1]。FQs藥物都具有酮酸的共同骨架結構(圖1)，F(xiàn)Qs抗生素是在喹諾酮類抗生素的基礎上，在第一代萘啶酸和第二代吡哌酸的引入氟原子開發(fā)出的。常用的FQs藥物主要有諾氟沙星(norfloxacin)、恩諾沙星(enrofloxacin)、環(huán)丙沙星(ciprofloxacin)、洛美沙星(lomefloxacin)、氧氟沙星(ofloxacin)、沙拉沙星(sarafloxacin)、培氟沙星(pefloxacin)、依諾沙星(enoxacin)、氟羅沙星(fleroxacin)和二氟沙星(difloxacin)等[2]。由于FQs抗生素在治療人和動物細菌性感染具有良好的藥物動力學特性及治療效果，應用廣、使用量大。據(jù)統(tǒng)計，喹諾酮藥物的使用量已位于抗感染藥物前列，2009年，占據(jù)全球抗生素17%的市場份額[3]。WHO(1998年)調查顯示[4]，據(jù)美國、日本、韓國和歐盟等國家和組織的統(tǒng)計，年消費喹諾酮類藥物中作為專用產品約有50 t，作為通用產品70 t，在中國分別為l 350 t和470 t。其中，諾氟沙星、環(huán)丙沙星和氧氟沙星的生產量最大[5]。而抗生素進入人或動物體內后40%～90%以母體或代謝物的形式隨畜禽糞便進入環(huán)境[6]。2010年，在中國排放到環(huán)境中畜禽糞便的量達45億t。環(huán)境調查發(fā)現(xiàn)，F(xiàn)Qs抗生素在水體、沉積物、土壤等多種環(huán)境介質中都有檢出[7-8]。在一些養(yǎng)殖場周圍的水體和土壤中，抗生素含量可達到異常高的水平[9-10]。目前，盡管國內外定期推出抗生素用藥使用原則，但尚無FQs抗生素的環(huán)境標準。研究表明，環(huán)境中抗生素可能導致生物毒性和致病菌產生抗藥性基因等環(huán)境風險和生態(tài)風險[11]，因此，抗生素引起的環(huán)境污染引起人們的高度關注和重視，對FQs抗生素的環(huán)境污染現(xiàn)狀、環(huán)境行為和生態(tài)毒性日益成為環(huán)境科學的研究熱點。本文介紹了FQs抗生素在環(huán)境多介質中的污染現(xiàn)狀，綜述了它們的環(huán)境行為和生態(tài)毒理研究進展。

圖1 氟喹諾酮類抗生素的分子結構Fig. 1 The molecular structure of the fluoroquinolone antibiotics

1 FQs抗生素污染(FQs antibiotics pollution)

1.1 水體FQs抗生素污染

不同水環(huán)境(污水處理廠、醫(yī)院廢水、養(yǎng)殖廢水、地表水、地下水、飲用水)中FQs抗生素種類及污染水平見表1。由表1可知，水環(huán)境中FQs抗生素以諾氟沙星、環(huán)丙沙星、氧氟沙星污染較為普遍，其濃度也較高。FQs抗生素在污廢水中的殘留量與污水的來源和特性有關，污水處理廠、醫(yī)院污水、養(yǎng)殖廢水中抗生素含量較高，濃度在μg·L-1級。如在美國在醫(yī)院廢水中檢出氧氟沙星的濃度達25.5～35.5 μg·L-1[12]。各地不同污水處理廠中FQs抗生素濃度差異很大，濃度范圍在0.013～13.625 μg·L-1之間。與污水相比，地表水和地下水中抗生素含量相對較低(濃度在ng·L-1級)。一般污水處理廠的抗生素去除效率在60%到90%，因此，盡管城市污水大部分進入污水處理系統(tǒng)，也可能存在抗生素對地表水、飲用水源和地下水污染[13]。

1.2 土壤/沉積物中FQs抗生素的污染

表2列出了不同地區(qū)土壤/沉積物中FQs抗生素的污染水平。由表2可以看出，不同國家和地區(qū)土壤/沉積物中FQs抗生素的種類和污染水平存在差異，這與抗生素的用量、畜禽糞肥的施用量、環(huán)境條件等差異相關[39]。土壤/沉積物中FQs抗生素以諾氟沙星、環(huán)丙沙星、恩諾沙星、氧氟沙星污染為主，含量在μg·kg-1～mg·kg-1數(shù)量級范圍。如在西班牙Morales-Muoz等[40]檢測到土壤中高濃度FQs抗生素，在施用糞肥的2處土壤中諾氟沙星濃度分別為6.2 mg·kg-1和9.8 mg·kg-1，環(huán)丙沙星的濃度分別為3 mg·kg-1和5.8 mg·kg-1。在瑞士Golet等[41]檢測到土壤中環(huán)丙沙星的濃度為1.96 mg·kg-1。中國山東省中北部和珠江三角洲菜地土壤中檢出諾氟沙星的最高濃度分別為288.3 μg·kg-1和150.2 μg·kg-1，環(huán)丙沙星的最高檢出濃度分別為651.6 μg·kg-1和119.8 μg·kg-1[42-43]。與其他環(huán)境介質相比，污泥中FQs抗生素的污染更重，中國污泥中氧氟沙星殘留濃度高達21 mg·kg-1[44]，其他國家FQs在污泥中檢出濃度在0.04～8.3 mg·kg-1范圍內。在畜禽糞便中，Zhao等[45]檢測到我國豬糞中恩諾沙星濃度為33.26 mg·kg-1，環(huán)丙沙星濃度為33.98 mg·kg-1。可見，我國土壤/沉積物中FQs抗生素污染相對較嚴重。

表1 水體中氟喹諾酮類抗生素的污染水平Table 1 The concentrations of fluoroquinolone antibiotics in water

表2 土壤/沉積物中氟喹諾酮類抗生素的污染水平Table 2 The concentrations of fluoroquinolone antibiotics in soils and sediments

2 FQs抗生素的環(huán)境行為(Environmental behaviorsof FQs antibiotics)

FQs抗生素按用途分為人用和獸用兩類。環(huán)境中FQs抗生素主要來源于工業(yè)排放、醫(yī)院排放、廢物垃圾、畜禽排泄、水產養(yǎng)殖等，進入環(huán)境中的抗生素經過吸附、遷移、轉化、降解(光解、水解和生物降解)等過程在土壤、水和沉積物等環(huán)境介質間再分配。圖2 環(huán)境中FQs抗生素的來源和遷移途徑示意圖。

圖2 環(huán)境中氟喹諾酮類抗生素的來源和遷移Fig. 2 Sources and pathways of fluoroquinolone antibiotics in environment

2.1 環(huán)境中FQs的吸附

抗生素進入土壤途徑主要包括施用含有抗生素的糞肥、污泥和含抗生素的污水灌溉[58-59]。進入土壤中的抗生素可通過吸附作用停留在土壤中，而影響其吸附的主要因素有土壤礦物質、有機質、多價態(tài)金屬陽離子及污泥等。FQs抗生素容易在土壤表層積累，向下層土的遷移很弱，這與-COOH對FQs抗生素吸附的貢獻較大有關[60-63]；喹諾酮類抗生素吸附系數(shù)(Kd)值較大，吸附能力較強，易在土壤中蓄積[64]。土壤對恩諾沙星具有較強的吸附作用，其中青紫泥田和黃泥砂田的Kd值較高, 分別在3 694～5 546 L·kg-1和3 800～4 696 L·kg-1之間，殘留在土壤中的低量恩諾沙星主要被吸附在固體顆粒上，不易釋放和隨水遷移[65]。一些多價態(tài)金屬陽離子是影響部分抗生素吸附行為的重要因素。FQs抗生素能和金屬離子(Ca2+、Mg2+、Fe3+或Al3+)形成絡合物，使其在環(huán)境介質中較穩(wěn)定存在[66]。水體和污水處理中的FQs抗生素也可以通過污泥吸附的方式去除。FQs從廢水中轉移到活性污泥中，從而達到去除目的[67]，環(huán)丙沙星通過污泥吸附去除率也達到60%[68]。

2.2 環(huán)境中FQs的降解

降解是環(huán)境抗生素重要的代謝途徑，包括光解、水解和生物降解。FQs抗生素在環(huán)境介質中主要發(fā)生光解和生物降解等降解過程，很難發(fā)生水解作用[69-70]。

FQs抗生素屬光降解敏感型，主要降解產物包括10多種有機物及F-和HCOO-等離子。FQs的光解路徑依賴于母體結構，對于哌嗪環(huán)N4-烷基取代的FQs，N4-烷基脫除為最主要的光解路徑，而對于N4-H結構的FQs，光導致脫羧和羥基化脫氟為重要的光解反應路徑[71-72]。FQs通過母體萘啶環(huán)上取代基的脫除而生成中間產物，易進入發(fā)光菌的細胞而產生毒性[73-74]。Yuan等[75]研究發(fā)現(xiàn)環(huán)丙沙星在一定紫外光強下的降解產物對費氏弧菌的毒性比母體化合物更強。表3列出了不同環(huán)境介質中FQs抗生素光解的半衰期。由表3可以看出，光解是地表水中的FQs抗生素主要降解方式[76-77]，但降解過程緩慢，導致在環(huán)境中的殘留時間比較久。沉積物中FQs的光解只發(fā)生在沉積物表層[78]，且相當緩慢。而土壤中吸附的FQs抗生素充分暴露于自然光下，能很好地促使它們降解[79]。Sturini等[80]研究了土壤中2種FQs抗生素恩諾沙星和麻保沙星的光解作用，實驗結果表明，經過50 h后2種FQs的降解率達到80%。

表3 環(huán)境中氟喹諾酮類抗生素光解的半衰期Table 3 Half-life of fluoroquinolone antibiotics photolysis in environment

生物降解是抗生素在環(huán)境中降解的重要的途徑。被生物降解的抗生素，可能轉化為生物體的組成部分或是最終轉化為無機或有機小分子。FQs的生物降解主要是母體結構脫-H2O、-HF、-CO2等，打斷哌嗪取代基，產生一系列的降解產物。Ailette Prieto等[84]研究了白腐真菌對環(huán)丙沙星和諾氟沙星的降解過程，環(huán)丙沙星的降解產物為Cip-1(C15H17FN3O3), Cip-2(C13H12FN2O3), Cip-3(C17H19FN3O4), Cip-4(C17H17FN3O5)等。Alexy等[85]在密閉瓶中模擬18種抗生素的降解實驗表明，氧氟沙星的生物降解率較低僅為7.5%，而其它類抗生素如芐青霉素和金霉素則被完全降解。Boxall等[86]報道了喹諾酮類抗生素在糞便中的半衰期為100 d。

廢水處理中FQs的生物降解研究發(fā)現(xiàn)，F(xiàn)Qs的生物降解<10%，幾乎可以忽略[87]；而在活性污泥反應器中進行生物降解試驗，結果表明添加250 μg·kg-1的環(huán)丙沙星，2.5 d之后，去除率達50%[88]；在硝化條件下，F(xiàn)Qs生物降解的去除率達60%[89]；Li和Zhang等[90]研究了污泥中環(huán)丙沙星、氧氟沙星、恩諾沙星的生物降解，48 h之后，去除率達40%。目前，研究者多認為，F(xiàn)Qs的主要去除機制是活性污泥的吸附，而非生物降解[91-92，87]。

3 FQs抗生素的生態(tài)毒理(Ecological toxicologyof FQs antibiotics)

相對較低濃度的恩諾沙星殘留對土壤微生物群落多樣性的影響不明顯，而相對較高濃度的恩諾沙星殘留則降低了其微生物群落的多樣性，即藥物濃度越高，則土壤微生物多樣性就越低[93]。馬驛等[94]發(fā)現(xiàn)恩諾沙星藥物濃度大于或等于0.1 μg·kg-1可顯著降低土壤微生物的豐富度和多樣性，藥物濃度越高，土壤微生物的豐富度和多樣性就越低。顯然，F(xiàn)Qs進入土壤環(huán)境中會導致土壤微生物多樣性的下降。

土壤呼吸作用反映了土壤微生物的總活性，可以用來作為監(jiān)測土壤生態(tài)環(huán)境變化的重要指標[95]。諾氟沙星在濃度為小于1 mg·kg-1時，對土壤微生物呼吸都有一定的抑制作用，濃度大于5 mg·kg-1為激活作用，激活作用隨著處理濃度的增加而升高，恩諾沙星對呼吸的影響隨濃度變化變化先激活后抑制[96]。恩諾沙星殘留在土壤中作用達2～4 d 時，較低濃度的恩諾沙星對土壤呼吸作用有刺激作用，較高濃度則對其產生抑制作用[97]。王麗平等[98]也發(fā)現(xiàn)，低質量分數(shù)的恩諾沙星(0.1 mg·kg-1)可刺激土壤中微生物的生長和呼吸作用，而高質量分數(shù)的恩諾沙星(2～20 mg·kg-1)會抑制土壤微生物活性和有機碳的礦化。恩諾沙星還影響土壤微生物功能，進而對土壤特性和土壤呼吸作用、纖維分解作用、以及氨化作用等生態(tài)過程造成影響。研究還發(fā)現(xiàn)，恩諾沙星可顯著抑制土壤脫氫酶和磷酸酶的活性，抑制土壤微生物的呼吸強度和硝化作用，土壤微生物群落功能多樣性(基于Biolog方法)隨恩諾沙星濃度升高顯著降低[99]?？梢酝茰y抗生素對土壤微生物呼吸的激活作用，可能因為抗生素被某些微生物利用作為自身生長的碳源，促進微生物的生長，對微生物呼吸起到促進作用[100-101]。要明確抗生素對土壤微生物的影響機理，需要通過生理生化測定方法和分子生物學手段來分析測定更多的指標來綜合評價。

環(huán)境中抗生素殘留對植物的生態(tài)毒性效應的研究目前報道的還較少且主要集中在實驗室模擬條件下水生植物和陸生植物的毒性研究。Migliore等[102]研究表明低濃度恩諾沙星(50～100 μg·L-1)促進了香瓜、萵苣、蘿卜和菜豆的生長，高濃度則顯著抑制了這4種作物主根、胚軸、子葉的長度，降低了葉片數(shù)量，其中對根的抑制效果最明顯，這可能與FQs抗生素在植物根部的蓄積量有關，在根部蓄積量最多，因此表現(xiàn)出對根生長的抑制作用最為顯著。Boxall等[103]研究發(fā)現(xiàn)，土培條件下1 mg·kg-1恩諾沙星顯著抑制胡蘿卜和萵苣生長，而相同濃度的阿莫西林、磺胺嘧啶、泰樂素、甲氧芐啶和氟苯尼考等其生長影響不顯著。金彩霞等[104]采用室內生長箱培養(yǎng)方法，研究了環(huán)丙沙星對小麥、白菜和番茄種子發(fā)芽、根伸長、芽伸長的影響，結果表明，作物根伸長和芽伸長的抑制率隨著土壤中環(huán)丙沙星含量的增高而增大，兩者呈正相關(P< 0.05)。與根伸長和芽伸長抑制相比, 植物種子發(fā)芽對抗生素脅迫的敏感性較弱。

FQs抗生素對水生生物藥害作用較強[105]。不同抗生素對水生生物的半最大效應濃度(EC50，μg·L-1)影響有差異。表4列出了FQs抗生素對不同水生生物體的EC50，由表可知EC50介于μg·L-1～ mg·L-1之間。藍藻在水生生物體中最為敏銳，藻類和植物比無脊椎動物和魚較敏銳。FQs濃度較高時，會對生物體產生急性毒性，但是長期暴露在低濃度下產生的副作用也不容被忽視[106-107]。Martins等[108]實驗表明，長期暴露在低濃度的環(huán)丙沙星下會對Daphnia magna產生慢性損害。

FQs抗生素誘發(fā)水生動物的毒性，魚類對FQs抗生素的代謝過程中會產生一些具有親電子活性的中間產物，可能誘導生物體內抗氧化酶活性的變化，進而造成機體的氧化應激效應[109]，導致機體代謝紊亂，引發(fā)其他疾病。有研究發(fā)現(xiàn)恩諾沙星會引起魚腦和肝臟內谷胱甘肽含量降低，過氧化氫酶和谷胱甘肽轉移酶活性發(fā)生變化，誘導魚體內脂質過氧化和神經功能障礙等疾病[109]，并證實在鱸魚體內恩諾沙星主要是通過細胞色素代謝為環(huán)丙沙星，且恩諾沙星對細胞色素具有明顯的抑制作用[110]。

表4 氟喹諾酮類抗生素對水生物種的半最大效應濃度(EC50)Table 4 The concentration for 50% of maximal effect of fluoroquinolone antibiotics on aquatic species

抗生素種類繁多，降解和代謝產物復雜，近年來，研究者對抗生素的聯(lián)合毒性作用主要集中在四環(huán)素和磺胺類抗生素[119-121]，對FQs抗生素研究甚少，環(huán)境中共存的FQs抗生素及其轉化產物之間的聯(lián)合毒性作用還有待進一步研究。

4 結論(Conclusion)

FQs抗生素作為環(huán)境中一類新型污染物，在環(huán)境中普遍存在，對人類健康和生態(tài)環(huán)境構成威脅。FQs抗生素水體含量在ng·L-1～μg·L-1之間，土壤/沉積物含量在μg·kg-1～mg·kg-1數(shù)量級，其中諾氟沙星、環(huán)丙沙星、恩諾沙星、氧氟沙星濃度相對較高。環(huán)境行為和生態(tài)毒理研究表明，F(xiàn)Qs抗生素在環(huán)境介質中吸附能力較強，在環(huán)境中主要通過光解和生物降解等途徑降解；FQs抗生素污染導致土壤微生物的多樣性下降和微生物活性降低，抑制植物的生長發(fā)育，對水生生物產生生態(tài)毒性效應。FQs抗生素的環(huán)境風險應從環(huán)境多介質層面進行評估，同時應加強對生態(tài)毒性機理以及與其他環(huán)境污染物的聯(lián)合毒性效應研究。

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A Review on Environmental Behaviors and Ecotoxicology of Fluoroquinolone Antibiotics

Meng Lei, Yang Bing, Xue Nandong*

State Key Laboratory of Environmental Criteria and Risk Assessment, Chinese Research Academy of Environmental Sciences, Beijing 100012, China

18 November 2014 accepted 7 January 2015

Fluoroquinolone antibiotics (FQs) were the broad-spectrum antibacterial drugs which were widely applied in livestock and poultry breeding industry to treat bacterial infection. The pollution of FQs in environment has been widely concerned. Environmental behaviors such as adsorption and desorption in water and soil/sediment and ecotoxicology of FQs were summarized in the paper. It is suggested that environmental behaviors and risk of FQs should be assessed at the level of environmental multimedia. More study should be conducted on ecological toxicity mechanism of FQs as well as on effects of the joint toxicity with other environmental pollutants.

fluoroquinolone; antibiotics; pollution situation; environmental behaviors; adsorption and desorption; ecotoxicology

國家高技術研究發(fā)展計劃(863)項目(2012AA06A304)

孟磊(1987-)，女，碩士，研究方向為土壤中有機污染物環(huán)境化學行為，E-mail: zimin616@163.com；

*通訊作者(Corresponding author)， E-mail: xuend@craes.org.cn

10.7524/AJE.1673-5897.20141118006

2014-11-18 錄用日期：2015-01-07

1673-5897(2015)2-76-13

X171.5

A

薛南冬(1964-)，男，理學博士，研究員，主要研究方向為土壤有機物污染及其環(huán)境修復，土壤化學品污染與控制等，發(fā)表學術論文90余篇。

孟磊, 楊兵, 薛南冬. 氟喹諾酮類抗生素環(huán)境行為及其生態(tài)毒理研究進展[J]. 生態(tài)毒理學報, 2015, 10(2): 76-88

Meng L, Yang B, Xue N D. A review on environmental behaviors and ecotoxicology of fluoroquinolone antibiotics [J]. Asian Journal of Ecotoxicology, 2015, 10(2): 76-88 (in Chinese)