Abstract
The use of reclaimed water in crop irrigation helps to mitigate water shortage. The fertilization of arable soils with sewage sludge, biosolids, or livestock manure reduces extensive application of synthetic fertilizers. However, both practices lead to the introduction of pharmaceutical active compounds (PhACs) in arable soil, known to host a wide range of living organisms, including microorganisms which are supporting numerous ecosystem services. In soils, the fate of PhACs is governed by different abiotic and biotic processes. Among them, soil sorption and microbial transformation are the most important ones and determine the fate, occurrence, and dispersion of PhACs into the different compartments of the environment. The presence of PhACs in soils can compromise the abundance, diversity, and activity of the soil microbial community which is one of the key players in a range of soil ecosystem services. This chapter reviews the current knowledge of the effects of PhACs, commonly found in wastewater effluents and derived organic fertilizers, on the soil microbial community.
Access provided by Autonomous University of Puebla. Download chapter PDF
Similar content being viewed by others
Keywords
1 Ways of Entrance of PhACs in Arable Soils
Every year, million tons of pharmaceutical active compounds (PhACs) are consumed worldwide for prophylaxis and curative treatments in human and veterinary medicines [1, 2]. Following their ingestion, formulated PhACs enter the body where they are partially assimilated by the organism and, thereafter, largely excreted through feces and urine [3, 4]. On the one hand, excreted residues of PhACs used in human medicine are collected in domestic and hospital sewage disposal systems to reach wastewater treatment plants [5, 6]. Direct dumping of unused or expired medication [7, 8] and illegal drugs [9] can also contribute to wastewater contamination. Since PhACs are relatively stable, conventional wastewater treatment plans have proven to be moderately effective at removing them [10]. As a result, complex mixtures of PhACs and their main metabolites are frequently found in treated wastewater effluents discharged directly in the river and/or in sewage sludge applied to arable soil as organic fertilizers [11, 12]. On the other hand, excreted veterinary PhACs accumulate in livestock manure [13,14,15,16] in concentrations that can be severalfold greater than in sewage sludge [17].
In arid or semiarid regions, such as the Mediterranean rim, where rainfalls are uneven and water resources limited, the use of treated wastewater in crop irrigation and groundwater recharge constitutes a promising alternative to release green water pressure on water cycle. Irrigation of crop with wastewater provides not only water but also nutrients to plant [18,19,20]. This agricultural practice may thereby reduce the application of agrochemical fertilizers, improve plant growth, and limit the wastewater discharged in rivers, thereby decreasing the PhACs pressure on surface water resources especially during the low-water period. Similarly, organic amendment of arable soils with livestock manure and/or sewage sludge/biosolid is also known to be beneficial for mineral fertilization of soil (especially nitrogen) and plant nutrition: it contributes to the maximization of crop yields [21, 22]. However, both practices lead to the release of numerous micro-pollutants including PhACs into arable soils with unknown consequences on both their abiotic and biotic components [23,24,25,26,27,28]. Although introduced PhACs concentrations are quite low, their repeated input in soil may lead to their accumulation, cause toxic effects to in soil living organisms, and transfer to surrounding aquatic compartments [29, 30].
In addition to diffuse contamination sources in arable soils, improper disposal of drugs or pharmaceutical waste products and accidental spills from pharmaceutical manufacturing plants and hospitals constitute important point sources of contamination. PhACs residues from these polluted sites [31,32,33,34] can contaminate water resources (runoff, surface water; leaching, groundwater), which can be used for crop irrigation, and indirectly contribute to both soil pollution and crop contamination.
2 Processes Involved in the Fate of PhACs in Arable Soils
As described above PhACs reach the environment via different entry routes. They reach soil via organic amendment (sewage sludge and farmyard manure) and crop irrigation (wastewater) and water resources via discharge of treated wastewater from wastewater plants in rivers and runoff and leaching from amended arable field. Once they enter the environment, the principal processes governing their fate are found at different degrees in both terrestrial and aquatic compartments. PhACs present in solid and liquid phases interact with both abiotic and biotic compartments of the environment.
In soils, PhACs are subject to several abiotic (sorption, photolysis, chemical transformation) and biotic (bioaccumulation and biotransformation) processes, which determine their ultimate distribution into the different environmental compartments [30, 35]. The rate and degree of each of those processes are determined by PhACs physicochemical characteristics as well as pedoclimatic conditions including temperature, humidity, and soil physiochemical characteristics [36,37,38].
Among the different mechanisms involved in the environmental fate of PhACs, sorption to soil components is by far one of the most important. It implies their close interactions with organic matter and mineral constituents of soils, involving ion exchange, surface adsorption to mineral constituents, hydrogen bonding, and formation of complexes with ions such as Ca2+, Mg2+, Fe+3, or Al3+ [30]. Examples of PhACs with a strong tendency to bind to soil particles are found among those that are poorly soluble such as the analgesic paracetamol, [39], the biocides triclosan and triclocarban, and some antibiotics such as tetracyclines, macrolides, sulfamethazine [40, 41], and quinolones, which form stable complexes through cation bridging to clay minerals. As a result, PhACs remain adsorbed in soils for a long period of time although lowly bioavailable to in soil living organisms [41,42,43,44,45,46,47,48,49,50,51].
On the contrary, the analgesics and anti-inflammatory compounds diclofenac, ibuprofen, and naproxen, the β-blocker propranolol, and some antibiotics such as sulfamethoxazole are less adsorbed to soils [38, 52,53,54] from where they can runoff to surface waters or leach to groundwater after a heavy rainfall event [25, 54,55,56,57,58]. This was also observed for carbamazepine, meprobamate, trimethoprim, and primidone applied to soil via crop irrigation with spiked wastewater, thereby confirming their low sorption to soil components and their relatively high mobility in soil [56, 59,60,61,62,63,64]. In addition, PhACs present in the soluble fraction are not only ready to leach to groundwater but also available for plant uptake [24, 65,66,67,68,69,70], macro- and mesofauna bioaccumulation [71,72,73], and/or microbiota uptake and further transformation [74].
Additionally, PhACs in soil can be transformed by biotic or abiotic reactions, leading to transformation products that can be more stable, more toxic, and persistent than their parent compounds [75, 76]. Among abiotic processes, photodegradation [77] and hydrolysis [78] are known to transform PhACs in aquatic media. The anti-inflammatory drugs diclofenac, naproxen, ibuprofen, and the diuretic agent amiloride were found to be transformed to hydroxyl metabolites, presenting higher toxicity, after a photocatalytic treatment [79,80,81,82,83,84]. Additionally, studies from Yamamoto et al. [85] reported a slow rate in sunlight photodegradation of acetaminophen, mefenamic acid, as well as ibuprofen and carbamazepine. In soils, photodegradation was observed for sulfonamides and tetracycline antibiotics which spread on the soil surface and pig slurry following first and biphasic kinetics, respectively [86].
Biotic transformation of PhACs is mainly achieved by microorganisms, which have developed during their long-lasting evolution an impressive enzymatic array able not only to detoxify their environment but also to get access to nutrients for their growth. PhACs biodegradation is achieved by two types of microbial guilds catalyzing two types of transformation: one the one hand, co-metabolic transformation is catalyzed by non-specific enzymes (such as P450 monooxygenase also involved in the biodegradation of other xenobiotics such as pesticides) [74, 87,88,89,90,91,92,93,94,95,96]. On the other hand, metabolic transformation is catalyzed by specific enzymes leading to partial or full mineralization of PhACs that are used as nutrients and energy sources for the growth of the degrading microbial guild [87, 90, 97,98,99,100,101,102,103,104,105,106,107,108,109,110,111,112]. From this point of view, transformation of PhACs by fungi and bacteria is a key process for their dissipation in the environment [113,114,115,116]. Since PhACs are designed to remain active after ingestion, most of them are relatively recalcitrant to biodegradation. However, it was shown that chronic or punctual exposure of soil microbial communities to PhACs can enhance their degrading capacities toward them [109, 117]. Biodegradation of PhACs in soils has been reported for naproxen [38, 74, 118]; ibuprofen [38, 114, 119, 120]; diclofenac [74, 114, 121,122,123]; paracetamol [39]; carbamazepine [62]; antibiotics such as sulfamethazine [109] and sulfadiazine [124]; triclosan [51, 125,126,127,128,129,130,131,132,133]; antifungals such as fluconazole, clotrimazole, and miconazole [25, 131, 134,135,136]; and caffeine [113].
3 Impact of PhACs on in Soil Living Microorganisms
Residues of human and veterinary PhACs enter terrestrial environments as complex liquid or solid biomixtures applied to crop as organic fertilizer or for watering. Like other active ingredients used for plant protection (pesticides), PhACs are relatively recalcitrant to biodegradation, active at rather low concentrations, and target key enzymes involved in essential biological functions that are widespread in the tree of life. During the last decades, the presence of pharmaceutical residues in the aquatic environment has raised special attention, and numerous studies have reported their effects on the aquatic living organisms and supported ecosystem services [137,138,139,140]. However, little is known regarding the effect of antibiotics and other PhACs on soil ecosystem services supported by microbial guilds. Soil microorganisms play a pivotal role in multiple ecosystem services. They contribute to soil health, mediate in biogeochemical cycles, and regulate climate change among other processes. Thus, the exposure of soil microorganisms to PhACs can influence their functioning with direct consequences on soil ecosystems. On the one hand, PhACs such as antibiotics and antifungals can inhibit specific microbial guilds and supported functions and thereby compromise the survival and growth of certain microbial guilds. On the other hand, some microorganisms can either develop mechanisms of defense against toxic PhACs (development of antimicrobial resistance, for instance) or use them as nutrient source (biodegradation) for their growth leading to the emergence of specific bacteria. It is noteworthy that some of the PhACs, such as the antibiotics, are particularly of concern because, when they are released in the environment, they exert a selection pressure favorable to the development and dissemination of antimicrobial resistance that can impair human and animal health [141].
Here we report some studies regarding the characterization of the ecotoxicological effects of some PhACs on soil microbial communities. The compounds were selected based on their ubiquitous detection in different environmental matrices and relevance.
3.1 Non-steroidal Anti-inflammatory Drugs (NSAID): Naproxen, Ibuprofen, and Diclofenac
Non-steroidal anti-inflammatory drugs (NSAID) are medicines used to relieve pain, decrease fever, and reduce inflammation. These compounds inhibit the cyclooxygenase (COX) enzyme, required to convert arachidonic acid into thromboxanes, prostaglandins, and prostacyclins, preventing the platelet adhesion, vasodilation, and increasing body temperature [142]. Among the different types, naproxen, ibuprofen, and diclofenac are the most frequently detected NSAIDs in wastewater effluents [143,144,145,146,147,148].
3.1.1 Naproxen
Naproxen is an acidic compound frequently found in wastewater effluents and receiving waters [143, 147, 149, 150]. It was found to be rapidly biodegraded in liquid microcosms containing either natural microbial communities from river water [151, 152] or bacteria, fungi, and algae [90, 91, 153,154,155,156,157]. To date, only three studies have addressed the dissipation of naproxen on agricultural soils, and little information is available regarding its ecotoxicological effects on microorganisms [158]. On soil microcosms carried out with three different agricultural soils (sandy loam, loam and silt) never exposed to this NSAID, Topp et al. showed a rapid mineralization of naproxen after application of liquid municipal biosolids [118]. Naproxen was also shown to be degraded in two soils collected from arid regions under aerobic conditions while it was more persistent under anaerobic conditions, suggesting that in terrestrial ecosystems its biodegradation is catalyzed by microorganisms under aerobic conditions. The differences in naproxen half-lives were attributed to specific soil types and microbial characteristics [38]. Studies from Grossberger et al. [74] on agricultural soils irrigated with reclaimed water showed a rapid dissipation of naproxen. Kinetics of dissipation were not enhanced in soils previously exposed to this NSAID, suggesting that in this experiment the naproxen was co-metabolically degraded.
Based on these studies, naproxen seems to be rapidly dissipated in soils where under aerobic conditions it does not remain for long period of time. However, as recurrent contaminant of reclaimed water that is repetitively applied in large volumes to irrigate various crops, it may persist long enough to impact in soil living microorganisms. Indeed, naproxen was found to irreversibly inhibit nitrite production in the ammonia oxidizing bacterium Nitrosomonas europeae following the loss of its membrane integrity, which can potentially compromise nitrogen removal in wastewater treatment plants [159]. Naproxen was also shown to change the abundance and the enzymatic activities of soil microorganisms inducing disturbances in soil functions [160].
3.1.2 Ibuprofen
Ibuprofen is a nonprescription drug widely used for the treatment of pain, fever, and rheumatic disorders. Ibuprofen is a chiral compound that contains two enantiomers, the S-enantiomer (pharmacologically active) and the R-enantiomer (inactive) [161,162,163]. During human metabolisms, R-ibuprofen undergoes chiral inversion, resulting in S-ibuprofen, which is excreted in urine [164, 165]. This pharmacokinetics transformation to S-enantiomer is consistent with the observation of a selective enrichment of S-ibuprofen not only in wastewater influents [166, 167] and effluents [168] but also in surface water [166, 169]. R-enantiomer biodegradation was reported in aquatic systems [169, 170]. However, the depletion of S-enantiomer was shown in wastewater effluents [167] and lake water microcosm spiked with ibuprofen [166] suggesting that ibuprofen enantiomerization may also happen after its release in in the environment.
The ability of both microbial communities [90] and pure microbial strain to degrade ibuprofen has been widely reported [171]. The bacterium Nocardia. sp. transforms ibuprofen to ibuprofenol and subsequently to the corresponding acetate derivative [172]. Sphingomonas sp. uses ibuprofen as a sole carbon and energy source via deoxygenation of the ring followed by meta-cleavage and catechol formation catalyzed by enzymes encoded by ipfABDEF genes [107, 108, 171]. Bacillus thuringiensis and Serratia marcescens degrade ibuprofen more efficiently in the presence of other carbons sources suggesting co-metabolic transformation [91, 92, 95]. Ibuprofen was also found to be degraded by white-rot fungi [153, 173] that yielded a number of transformation products more toxic than the parent compound. Ibuprofen degradation was negligible in anaerobic and sterile soil [174] and water-saturated soil [119], further indicating that it is degraded by microorganisms and principally under aerobic conditions.
Ibuprofen has been found in different terrestrial ecosystems [175, 176] at different concentrations ranging between 0.2 and 610 μg/kg. In soils ibuprofen is rapidly degraded under aerobic conditions with half-lives values between 30 to 34.3 days, 10 to 15 days, and 1 to 6 days, respectively [38, 114, 119]. Similar maximum mineralizable amounts of ibuprofen were shown in both aqueous and soil microcosms but with about 3.5 times lower mineralization rate in soil systems [120].
To our best knowledge, the effect of ibuprofen on microorganisms has only been studied in liquid cultures and aquatic populations, and not yet on soil microorganisms. Ibuprofen has antifungal activity against dermatophytes [177] and inhibits the growth of some Gram-positive species [178, 179]. Ibuprofen caused the decrease in the biomass of riverine biofilms and inhibited the growth of Cyanobacteria and of alpha, beta-proteobacteria, cytophaga-flavobacteria, and SRB385 populations [180]. Additionally, ibuprofen was also shown to significantly modify the growth of the microbial community of a river sediment incubated at different temperatures and light exposure [181]. Pollution-induced community tolerance (PICT) analysis performed on fluvial biofilms exposed to wastewater effluents showed that at the highest concentrations of ibuprofen and diclofenac, they acquired a tolerance to these components accompanied by an alteration of the algal composition and metabolic profile of microbial organisms [182]. Recently, a mixture of ibuprofen, naproxen, and diclofenac was shown to change the composition of the microbial community (increase in Actinobacteria and Bacteroidetes and a decrease of Micropruina and Nakamurella) but not the total nitrogen removal in batch reactors [183]. Although the environmental risk assessment concluded that ibuprofen represents a risk for the aquatic environment [184], it was not included in the list of priority substances under the Water Frame Directive due to a lack of sufficient evidence for its environmental toxicity [185].
3.1.3 Diclofenac
Diclofenac, the most used NSAID in the world, is poorly removed in conventional sewage treatment plants [186,187,188]. Hence, diclofenac residues are frequently detected in the environment [53, 175, 189,190,191,192]. As a consequence, it is considered as a contaminant of emerging concern, and it was added to environmental quality standards (EQS) with a threshold value of 0.1 μg/L (European Community document (COM(2011)876)). More recently, diclofenac was included in the list of priority substances (PSs) of the Directive 2013/39/EU and Watch List of Decision 2015/495/EU [193,194,195].
Diclofenac is a polar pharmaceutical compound poorly adsorbed to soil components and therefore easily transferable to surrounding environmental compartments via leachates and runoff [38]. In agricultural soils, under aerobic conditions, diclofenac is readily biodegradable [74, 114, 121,122,123] within 10 days, whereas it persists in sterile soils, indicating that soil microorganisms are responsible for its rapid dissipation. This was confirmed by the isolation and characterization of several fungal [156, 196,197,198,199,200] and bacterial strains able to degrade diclofenac as sole carbon source [87, 97, 201] or through cometabolism [87, 93, 94, 196, 202,203,204,205].
Ecotoxicity of diclofenac on Gram-positive [206, 207] and Gram-negative bacteria [208, 209] was reported because of the inhibition of DNA synthesis [210] or of the impairment of membrane activity [211, 212]. To date, only two studies have assessed the effects of diclofenac on soil microorganisms [123, 160]. Experiments performed by Cycon et al. [160] with different endpoints including substrate-induced respiration, soil enzyme activities, and enumeration of culturable bacteria and fungi showed that diclofenac exposure led to an increase in the number of culturable bacteria and fungi. At the highest dose (10 mg/kg), diclofenac increased soil respiration as well as the activity of some soil enzymes (acid and alkaline phosphatase, urease). On the contrary, it inhibited the activity of soil dehydrogenases, while it does not affect enzymatic activities (nitrification and ammonification) of N cycle. Experiments performed by Thelusmond et al. [213] by means of Illumina sequencing, STAMP and PiCRUST in agricultural soils observed an increase in Proteobacteria, Gemmatimonadetes, and Actinobacteria and identified four metabolic pathways positively impacted (propanoate, lysine, fatty acid, and benzoate metabolism) during diclofenac biodegradation.
3.2 Other Analgesics and Antipyretics: Paracetamol or Acetaminophen
Paracetamol or acetaminophen is one of the most widely used over-the-counter analgesic and antipyretic drug. The mechanism of action is complex and includes the inhibition of the cyclooxygenase isozyme COX-3 involved in the synthesis of prostaglandins and the activation of metabolites influencing cannabinoid receptors [214, 215]. As result of its popular use, paracetamol has been frequently found in wastewater treatment plants and in various environmental matrices all over the world [147, 175, 216,217,218,219,220,221,222,223,224,225,226,227].
Paracetamol is transformed by both fungal [228, 229] and bacterial cultures [96, 98, 99, 111, 230, 231]. In bacteria, two different biodegradation pathways via hydroquinone [101, 111] or pyrocatechol [232] have been characterized [233]. To date, only one study has addressed the fate of paracetamol in soil [39] showing that 17% of initial dose applied was mineralized in 120 days, while 73.4–93.3% was recovered as non-extractable residues. Additionally, eight different transformation products were identified, and new biodegradation pathways for paracetamol degradation in soil were proposed. In this study, paracetamol dissipation was mainly explained by the rapid formation of bound residues preventing the dispersion of paracetamol by leaching and/or runoff but accumulating in soil where it may represent a risk for in soil living organisms.
Although numerous studies have shown toxic effects of paracetamol on aquatic organisms [234,235,236], little information is available regarding its ecotoxicity toward microorganisms. Paracetamol has antibacterial properties on isolated Gram-positive strains [179]. In combination with doxycycline, it was found to inhibit the activity of nitrifying, denitrifying, and anaerobic ammonium oxidation (anammox) bacteria involved in N cycle from different batch reactors [237]. The microbial toxicity of paracetamol was assessed using the MARA (microbial assay for risk assessment), the Microtox, and the Ames microplate assay [96]. Gram-negative bacilli and Serratia were the most sensitive bacteria, while the most resistant were Enterococcus and yeast Pichia anomala. According to MARA performed with 11 different strains, the mean value of microbial toxic concentration (MTC equivalent of EC50) was 3,435.00 ± 129.90 mg/L, and the EC50 estimated values using Microtox with Aliivibrio fischeri were 7,923 mg/L and 9,487 mg/L after 5 and 15 min of paracetamol exposure, respectively. Ames assay concluded that paracetamol was non-mutagenic, according to the EPA standards [96].
3.3 Antidepressants: Fluoxetine (Prozac) and Citalopram Hydrobromide (Celexa)
Antidepressants are medications that can help ease symptoms of depression, anxiety, and affective disorders. Among them, selective serotonin reuptake inhibitors (SSRI) are the most commonly prescribed. They increase the levels of serotonin in the brain and block the reabsorption of serotonin into neurons. Examples of SSRI antidepressants are citalopram and fluoxetine, commonly marketed with diverse trade names such as Prozac and Celexa, respectively.
Citalopram is a chiral compound sold as a racemic mixture, but only the S-enantiomer (sold as Escitalopram) has the desired antidepressant effect. Similarly, fluoxetine is commercialized as a racemic mixture, with the S-enantiomer approximately 1.5 more potent than the R-enantiomer. In the human body, fluoxetine is metabolized to norfluoxetine. Several studies have found citalopram, fluoxetine, and its major metabolite norfluoxetine in different environmental matrices [222, 238,239,240,241,242]. Under laboratory conditions, citalopram and fluoxetine are relatively recalcitrant to hydrolysis, photolysis, and microbial degradation [243, 244]. Nonetheless, the biodegradation of fluoxetine by a single bacterium (preferably the R-enantiomer) [105] or microbial consortium has been reported [245, 246]. Fluoxetine biodegradation applied at 1 μg/L was reported in estuarine and coastal seawaters with half-lives ranging from 6 to 10 days [247]. Similarly, in activated sludge the biodegradation of citalopram was reported with 60% and 40% elimination rates under aerobic and anoxic conditions, respectively [248, 249]. In activated sludge [250], similar elimination rates (70%) of citalopram were observed under aerobic conditions, and this biotic transformation led to the formation of 14 different transformation products.
The ecotoxicity of fluoxetine and citalopram on aquatic organisms has been widely documented [251,252,253]. They affect the behavior, reproduction, development, and survival of aquatic invertebrates and vertebrates [254, 255]. On microbes, psychotropic drugs such as fluoxetine have been found to inhibit microbial activity [256]. In this regard, fluoxetine has significant antibacterial effect and potential antibiotic modulating activity against multiresistant bacteria [257]. Fluoxetine reduced the richness and increased the beta diversity of gut microbiota [258].
3.4 Antiepileptics: Carbamazepine
Carbamazepine is a relatively lipophilic antiepileptic drug used to control and prevent seizures [259, 260]. Due to its scarce removal in wastewater treatment plants [186, 188, 261,262,263], carbamazepine is frequently found in municipal effluents [63, 188, 260]. For this reason, it has been proposed as an anthropogenic marker of sewage contamination in aquatic environments [264,265,266]. Carbamazepine is also frequently detected in arable soils irrigated with wastewater, amended with biosolids or in soils where reclaimed water is used to recharge groundwater [239, 240, 267].
In soils carbamazepine was barely degraded (1.2% of mineralization after 120 days of incubation) and transformed to a range of transformation products not adsorbed to soil components (4.2% recoveries as non-extractable residues of initially applied carbamazepine) [62]. The persistence and accumulation of carbamazepine in soils have been reported by many authors [123, 268]. However, some fungi [153, 269,270,271,272,273], bacteria [102, 274, 275], or the combination of both [276] is able to degrade carbamazepine [277]. In this context, a recent study performed in four agricultural soils identified by means of shotgun sequencing the most abundant phytolypes (Rhodococcus, Streptomyces, and Pseudomonas) and associated functional genes [130]. The uptake and metabolism of carbamazepine by endophytic bacteria were studied by Sauvêtre et al. who reported a number of degrading endophytic isolates and identified several degradation products [278, 279].
The ecotoxicological effect of carbamazepine was studied on riverine biofilm communities where it was found to reduce the bacterial biomass and the abundance of gamma-proteobacteria, suppress the Cyanobacteria, and increase in algal biomass and abundance of beta-proteobacteria [180]. In soils, the ecotoxicological effects of carbamazepine on soil microorganism have been recently reported indicating an enrichment of Sphingomonadaceae, Xanthomonadaceae, and Rhodobacteraceae [213] and an increase in Proteobacteria and Verrucomicrobia possibly due to the emergence of carbamazepine degraders [123, 213]. In addition, the abundance of Flavobacterium, three genus incertae sedis and Bacteroidetes decreased [213] revealing the toxicity of carbamazepine toward these microorganisms.
It is noteworthy that carbamazepine applied at environmental concentrations can induce horizontal transfer of plasmids carrying antibiotic resistance among the bacteria community [280]. Given the co-occurrence of PhACs in environments, these findings pointed out the potential threat of carbamazepine in the environmental spread of antimicrobial resistance.
3.5 Antibiotics
Antibiotics are natural or synthetic substances that kill (bactericidal) or inhibit the growth (bacteriostatic) of bacteria [281]. They are commonly used in human and veterinary medicines [282] as well as in agriculture [283,284,285] and aquaculture [286, 287] to prevent or treat infections, as growth promoters [288, 289] and sometimes as food preservatives [290]. There are about 250 different antibiotics which can be classified on the basis of their mechanisms in four different groups [281] such as those that inhibit the:
-
Synthesis of the cell wall (beta-lactam and glycopeptides)
-
Biosynthesis of proteins (aminoglycosides, tetracyclines, chloramphenicol, macrolides, oxazolidinones)
-
DNA replication (quinolones)
-
Metabolism of folic acid (sulfonamides and trimethoprim)
As a result of their extensive use and their recalcitrance to degradation, antibiotics are frequently found in various matrices such as wastewater [291,292,293,294,295,296,297], biosolids [240, 298,299,300,301], sewage sludge [302,303,304,305,306,307,308], and farmyard manure [309,310,311,312,313,314,315,316,317,318,319,320]. Applications of these matrices to arable soils to water crop or as organic amendment can lead to the dispersion of antibiotic residues in both terrestrial and aquatic ecosystems [321, 322]. Indeed, antibiotics can runoff or leach from the soil polluting surface water and groundwater, respectively [25, 323, 324]. The ubiquitous detection of antibiotic residues in environmental matrices is cause for a great concern since even at rather low concentration they exert a selection pressure favorable to the emergence and further dispersion of antimicrobial resistances among environmental microbial communities [325,326,327,328,329,330].
In addition, antibiotic residues may also inhibit specific microbial guilds or functions and therefore disrupt critical processes for ecosystem functioning. Indeed, they have been shown to affect degrading microorganisms, thereby impairing the removal of organic matter and chemicals in sewage treatment plants [331,332,333,334]. In addition, antibiotic residues contaminating wastewater or biosolids/manure that are applied on arable soils can inhibit microbial populations involved in carbon and nitrogen geochemical cycling [335, 336], climate regulation [337], and degradation of xenobiotics and therefore may alter soil fertility and ecosystem health [338,339,340,341,342,343] .
In soils, antibiotics are subjected to microbial transformation with variable degrading rates depending on their molecular structure and physicochemical properties [48, 344]. Amoxicillin (beta-lactam) and chlortetracycline are easily degradable [345, 346], while ciprofloxacine, norfloxacine (fluoroquinolones), azithromycin (macrolides), and doxycycline (tetracyclines) are more recalcitrant to biodegradation remaining for a long period of time in soils [131]. Interestingly, in several studies performed on a long-term field experiment where various antibiotics were repeatedly applied, evidenced for enhanced dissipation of an impressive range of antibiotics (sulfamethazine, tylosin, chlortetracyclin, erythromycin, clarithromycin, and azithromycin) in exposed field plots as compared to control field plots [109, 117]. The number of studies reporting the degradation of different antibiotics in soils is important [124, 340]. Differences observed between studies for a given antibiotic are most likely due to variations in soil type, antibiotic concentrations, and environmental conditions.
Numerous bacterial strains able to degrade antibiotics have been isolated from various matrices including patient, animal, sediment, sludge, manure, and soil. For soils it includes strains belonging to the genera Microbacterium sp. (sulfamethazine, sulfadiazine, and sulfamethoxazole) [109, 347, 348], Bacillus sp. (penicillin) [110], Escherichia sp. (sulfonamides including sulfamethazine and sulfamethoxazole) [349], Stenotrophomonas sp., (tetracycline) [350], Ochrobactrum sp. (sulfamethoxazole and erythromycin) [351, 352], Labrys sp. (fluoroquinolones and sulfamethoxazole) [88, 351], and Gordonia sp. (sulfamethoxazole) [351]; the orders Burkholderiales, Caulobacterales, Xanthomonadales, Pseudomonadales, Enterobacteriales, and Rhizobiales; and the phyla Bacteroidetes (penicillin and neomycin) [112]. In this regard, bioaugmentation of sulfonamide-spiked soil microcosms with Microbacterium sp.C448 [109] was shown to reduce the persistence of antibiotic residues in soils and all associated side effects [353, 354].
3.6 Antiseptics and Disinfectants
Antiseptics and disinfectants, sometimes called biocides, are chemicals commonly used in a variety of medical and domestic settings to prevent or kill the growth of microorganisms. In general, biocides are less specific than antibiotics as their action mode has a broad spectrum of activity, generally not fully understood [355]. Among widely used biocides, triclosan has raised special concern due to its weak demonstrated benefit [356] and potential toxic effects on human health [357, 358]. At low concentrations, triclosan is a bacteriostatic, while at high concentrations, it is bactericidal agent effective against many types of Gram-positive and negative non-sporulating bacteria, some fungi, and certain parasites [359,360,361,362,363]. Although the use of triclosan was restricted in certain types of products [364,365,366], it is still found in many care products such as toothpaste, mouthwash, hand sanitizer, and surgical soaps. Due to its widespread use and incomplete removal from wastewater treatment plants [367,368,369], triclosan is frequently detected in several environmental matrices such as soil and surface waters [222, 370,371,372,373]. Triclosan was found to bioaccumulate in aquatic species, algae, snails, and earthworms [71, 373,374,375] in which it caused toxic effects [376,377,378,379,380,381,382,383]. Similarly, plants such as pumpkin, zucchini, onion, and tomato have been shown to bioaccumulate triclosan in the edible parts, thereby leading to the contamination of the food chain [384,385,386].
Although triclosan is an antimicrobial agent, some fungi [387, 388] and bacteria are able to degrade it co-metabolically or metabolically using it as sole carbon source for their growth [89, 100, 104, 106, 389,390,391,392,393]. In addition, repeated exposure to sublethal concentrations of triclosan may result in the development of resistant colonies [394, 395]. The mechanisms of triclosan microbial resistance share some similarities with those involved in antibiotic resistance [396, 397]. Several studies have demonstrated the development of cross-resistance between triclosan and antibiotics [398,399,400]. Therefore, triclosan like other biocides is suspected to take part to the selection pressure favorable to the emergence, spread, and maintenance of antibiotic resistances among environmental microbial communities [395, 401,402,403,404].
In soils, triclosan was reported to degrade to variable extent, with various half-lives depending on soil properties and conditions of incubation [51, 115, 125,126,127,128,129,130,131,132]. Regarding its ecotoxicological impact on soil microorganisms, triclosan was found to transiently inhibit microbial respiration, reduce microbial biomass [126], and sulfatase activity [405]. These effects were positively related to the dose of triclosan applied to the soil and inversely correlated with soil organic matter and clay content, suggesting that soil characteristics control its bioavailability and induced toxicity. Triclosan was also found to reduce the relative abundance of both Gram-positive and negative bacteria and fungi [406]. Recently, studies performed in four agricultural soils using shotgun sequencing observed an increase in Pseudomonas, Sphingomonas, Methylobacillus, and Stenotrophomonas and identified the most abundant functional genes associated with triclosan biodegradation [130].
3.7 Antifungals
Antifungals comprise a large and diverse group of drugs used to treat fungal diseases in humans, animals and plants. Based on their action mode, antifungals can be divided in three different classes: azoles, which inhibit the synthesis of ergosterol; polyenes, which physicochemically interact with fungal membrane sterols; and 5-fluorocytosine, which inhibits macromolecular synthesis [407]. Among the different azoles, of particular interest is the case of the triazoles, which constitute a synthetic group of heterocyclic compounds containing a five-membered ring of two carbon atoms and three nitrogen atoms commonly used for the control of fungal diseases in humans, animals, and plants. They include drugs such as fluconazole, clotrimazole, and miconazole and plant protection products such as tebuconazole and epoxiconazole. By inhibiting the activity of lanosterol 14α-demethylase (DMI), a member of the cytochrome P450 catalytic activity, triazoles alter the bioconversion of lanosterol to ergosterol, a fundamental component of the fungal cytoplasmic membrane, preventing fungal growth [407, 408]. Therefore, triazoles are fungistatic and not fungicidal, but although misleading, the term fungicide is commonly used in agriculture for this type of pesticide.
Due to their efficacy and broad spectrum of activity, triazoles are among the most common systemic fungicides used in the control of plant diseases [409]. Contrary to other available antimycotics, they are applied not only to prevent but also to treat plant fungal diseases. Triazoles have also been shown to promote the growth of plant leading to increase in the crop yield [410, 411].
In the medical field, synthetic antifungal agents are widely used for the treatment and prophylaxis of many mycoses [412]. As a consequence of their common use, substantial amounts of azoles reach the wastewater treatment plants [413,414,415,416]. There, as observed for many other PhACs, due to their intrinsic stability, triazoles can remain stable and active with only slight changes in their chemical structure. Studies investigating the occurrence of azole fungicides in wastewater are limited [413, 414, 417,418,419]. However, a number of studies have identified wastewater effluents as triazole pollution point source of surface waters and agricultural soil [134, 420,421,422,423,424,425].
The dissipation of triazole plant protection fungicides in soils has been widely documented. Pesticides such as tebuconazole [426,427,428,429,430,431,432,433], epoxiconazole [434, 435], propiconazole [436,437,438] and cyproconazole [439] have been shown to be relatively persistent in soil. In soil tebuconazole was shown to be transformed in 34 different transformation products [440]. To date Burkholderia sp. and Pseudomonas aeruginosa are the only two soil bacterial isolates known to degrade the fungicide propiconazole [441, 442].
Similarly, antifungal medicines are highly resistant to microbial degradation. Experiments performed in soil microcosms showed that fluconazole and clotrimazole were scarcely degraded, with half-lives in the range of 73 to 85 days for fluconazole and of 29 to 126 days or of 36.2 to 130.8 days for clotrimazole [135, 136]. In field conditions, a higher persistence was found in biosolid amended soils for the azole biocides climbazole, clotrimazole, and miconazole [25, 131, 134], with differences in dissipation half-lives attributed to soil types and biosolid application rates. To date, only one study has reported the ability of one edible fungal specie to degrade bifonazole and clotrimazole [443].
As observed with antibiotics, the intensive and repeated use of triazoles has led to the emergence of fungal resistances. Among the different mechanisms of resistance involved, the overexpression of the CYP51 gene that codes for the lanosterol 14α-demethylase, due to mutations (insertions or duplications) in the promoter region, and the increase in molecular efflux by ABC (ATP-binding cassette) transporters caused by the overexpression of genes coding for membrane transport have been mainly observed [407, 444,445,446]. Clinical isolates with observed resistance to triazoles include the species of Aspergillus, Candida, Fusarium, Zygomycetes, Trichosporon, Penicillium, Bipolaris, and Scedosporium, among others [447,448,449,450,451,452]. The majority of cases of azole-resistant diseases are due to resistant Aspergillus fumigatus which causes a variety of diseases in humans and animals ranging from allergic, chronic, and acute invasive diseases, the latter posing a significant threat to immunocompromised patients [453]. The surge of resistant fungi of human pathogens in the medical field has been related to the exposure to fungicides used in agroecosystems [454,455,456]. The important use of triazoles in agriculture may indeed exert a selective pressure favoring the survival of certain human pathogenic fungi, increasing the risks and chances for humans to encounter such resisting microbes. Pathogenic fungi that have their natural habitat in the environment are the fungi Coccidioides, Histoplasma, Aspergillus, Colletotrichum, and Cryptococcus [457,458,459,460,461].
While a number of studies have evaluated the ecotoxicological impact of triazole fungicides [462] (propiconazole [463, 464], tetraconazole [465], tebuconazole [429, 466,467,468,469,470,471,472,473]) on soil microorganisms, the effects of antifungal medicines on soil microorganisms have been scarcely documented [474]. Climbazole, an antidandruff and antimycotic agent, was shown to be toxic to algae, aquatic lentils (Lemna), and terrestrial plants and exhibited low toxicity toward the soil bacterium Arthrobacter globiformis with an EC50 of 456 mg/kg soil for inhibition of dehydrogenase activity [474].
4 Perspectives
Although PhACs are found as contaminants in almost all environmental matrices, including soils, their environmental fate and ecotoxicological impact on in soil living organisms and supported ecosystem services remain poorly described and scarcely understood. This evident lack of information is most likely due to the absence of regulatory requirements to monitor soil quality in the absence of a soil protection directive that was proposed almost 20 years ago to the European Commission, but that is still not adopted [475]. In addition, the current regulation to release on the market PhACs does not consider enough their possible effect on the environmental compartment, in particular on soil.
Most of the studies are laboratory experiments that consider contaminant one by one spiked at high concentration in microcosms. Only a few of them are done at field or environmental scale with complex mixture of contaminants but with the problem of the reference (normal operating range) to interpret the variations observed. Although it is the rule at the environmental scale, no studies consider the effect of complex mixtures of PhACs to soil [476]. Until now, there are no consensus to assess the fate and the ecotoxicological effects of PhACs on soil microorganisms and supported ecosystem services.
Given the fact that human and animal health are unambiguously link to environmental health under the concept of “One health,” it could be concluded that there is an urgent need to unify current regulations on the release on the market of PhACs, biocides, and plant protection products in close connection with the regulations to protect the environment such as the water framework directive, air quality framework directive, and national directives on soil protection (pending the publication of the soil protection directive). This unification has to be done under a holistic policy embracing both a priori and a posteriori environmental risk evaluation assessment by targeting specific protection goals, including microbial communities that support soil ecosystem services.
References
Hoebert J, Richard L, Peter S (2011) The world medicines situation 2011 – pharmaceutical consumption. WHO, Geneva, pp 1–17
Ruhoy IS, Daughton CG (2008) Beyond the medicine cabinet: an analysis of where and why medications accumulate. Environ Int 34:1157–1169. https://doi.org/10.1016/j.envint.2008.05.002
Daughton CG, Ruhoy IS (2009) Environmental footprint of pharmaceuticals: the significance of factors beyond direct excretion to sewers. Environ Toxicol Chem 28:2495–2521. https://doi.org/10.1897/08-382.1
Winker M, Faika D, Gulyas H, Otterpohl R (2008) A comparison of human pharmaceutical concentrations in raw municipal wastewater and yellow water. Sci Total Environ 399:96–104. https://doi.org/10.1016/j.scitotenv.2008.03.027
Kümmerer K (2008) Pharmaceuticals in the environment – a brief summary. In: Pharmaceuticals in the environment. Springer, Berlin, pp 3–21. https://doi.org/10.1007/978-3-540-74664-5_1
Kümmerer K (2001) Drugs in the environment: emission of drugs, diagnostic aids and disinfectants into wastewater by hospitals in relation to other sources – a review. Chemosphere 45:957–969. https://doi.org/10.1016/S0045-6535(01)00144-8
Paut Kusturica M, Tomas A, Sabo A (2017) Disposal of unused drugs: knowledge and behavior among people around the world. In: Reviews of environmental contamination and toxicology. Springer, New York, pp 71–104. https://doi.org/10.1007/398_2016_3
Tong AYC, Peake BM, Braund R (2011) Disposal practices for unused medications around the world. Environ Int 37:292–298. https://doi.org/10.1016/j.envint.2010.10.002
Yadav MK, Short MD, Aryal R, Gerber C, van den Akker B, Saint CP (2017) Occurrence of illicit drugs in water and wastewater and their removal during wastewater treatment. Water Res 124:713–727. https://doi.org/10.1016/j.watres.2017.07.068
Verlicchi P, Zambello E, Al Aukidy M (2013) Removal of pharmaceuticals by conventional wastewater treatment plants. In: Comprehensive analytical chemistry. Elsevier, Amsterdam, pp 231–286. https://doi.org/10.1016/B978-0-444-62657-8.00008-2
Castiglioni S, Bagnati R, Calamari D, Fanelli R, Zuccato E (2005) A multiresidue analytical method using solid-phase extraction and high-pressure liquid chromatography tandem mass spectrometry to measure pharmaceuticals of different therapeutic classes in urban wastewaters. J Chromatogr A 1092:206–215. https://doi.org/10.1016/j.chroma.2005.07.012
Heberer T (2002) Occurrence, fate, and removal of pharmaceutical residues in the aquatic environment: a review of recent research data. Toxicol Lett 131:5–17. https://doi.org/10.1016/S0378-4274(02)00041-3
Gros M, Mas-Pla J, Boy-Roura M, Geli I, Domingo F, Petrović M (2019) Veterinary pharmaceuticals and antibiotics in manure and slurry and their fate in amended agricultural soils: findings from an experimental field site (Baix Empordà, NE Catalonia). Sci Total Environ 654:1337–1349. https://doi.org/10.1016/j.scitotenv.2018.11.061
Nõlvak H, Truu M, Kanger K, Tampere M, Espenberg M, Loit E, Raave H, Truu J (2016) Inorganic and organic fertilizers impact the abundance and proportion of antibiotic resistance and integron-integrase genes in agricultural grassland soil. Sci Total Environ 562:678–689. https://doi.org/10.1016/j.scitotenv.2016.04.035
Song W, Guo M (2014) Residual veterinary pharmaceuticals in animal manures and their environmental behaviors in soils. In: Applied manure and nutrient chemistry for sustainable agriculture and environment. Springer, Amsterdam, pp 23–52. https://doi.org/10.1007/978-94-017-8807-6_2
Wohde M, Berkner S, Junker T, Konradi S, Schwarz L, Düring RA (2016) Occurrence and transformation of veterinary pharmaceuticals and biocides in manure: a literature review. Environ Sci Eur 28:23. https://doi.org/10.1186/s12302-016-0091-8
Maron DF, Smith TJS, Nachman KE (2013) Restrictions on antimicrobial use in food animal production: an international regulatory and economic survey. Global Health 9:48. https://doi.org/10.1186/1744-8603-9-48
Libutti A, Gatta G, Gagliardi A, Vergine P, Pollice A, Beneduce L, Disciglio G, Tarantino E (2018) Agro-industrial wastewater reuse for irrigation of a vegetable crop succession under Mediterranean conditions. Agric Water Manag 196:1–14. https://doi.org/10.1016/j.agwat.2017.10.015
Meli S, Porto M, Belligno A, Bufo SA, Mazzatura A, Scopa A (2002) Influence of irrigation with lagooned urban wastewater on chemical and microbiological soil parameters in a citrus orchard under Mediterranean condition. Sci Total Environ 285:69–77. https://doi.org/10.1016/S0048-9697(01)00896-8
Mohammad Rusan MJ, Hinnawi S, Rousan L (2007) Long term effect of wastewater irrigation of forage crops on soil and plant quality parameters. Desalination 215:143–152. https://doi.org/10.1016/j.desal.2006.10.032
Annicchiarico G, Caternolo G, Rossi E, Martiniello P (2011) Effect of manure vs. fertilizer inputs on productivity of forage crop models. Int J Environ Res Public Health 8:1893–1913. https://doi.org/10.3390/ijerph8061893
Hernández T, Moreno JI, Costa F (1991) Influence of sewage sludge application on crop yields and heavy metal availability. Soil Sci Plant Nutr 37:201–210. https://doi.org/10.1080/00380768.1991.10415030
Durán-Alvarez JC, Becerril-Bravo E, Castro VS, Jiménez B, Gibson R (2009) The analysis of a group of acidic pharmaceuticals, carbamazepine, and potential endocrine disrupting compounds in wastewater irrigated soils by gas chromatography-mass spectrometry. Talanta 78:1159–1166. https://doi.org/10.1016/j.talanta.2009.01.035
Fatta-Kassinos D, Kalavrouziotis IK, Koukoulakis PH, Vasquez MI (2011) The risks associated with wastewater reuse and xenobiotics in the agroecological environment. Sci Total Environ 409:3555–3563. https://doi.org/10.1016/j.scitotenv.2010.03.036
Gottschall N, Topp E, Metcalfe C, Edwards M, Payne M, Kleywegt S, Russell P, Lapen DR (2012) Pharmaceutical and personal care products in groundwater, subsurface drainage, soil, and wheat grain, following a high single application of municipal biosolids to a field. Chemosphere 87:194–203. https://doi.org/10.1016/j.chemosphere.2011.12.018
Montemurro N, Postigo C, Chirón S, Barcelò D, Pérez S (2019) Analysis and fate of 14 relevant wastewater-derived organic pollutants in long-term exposed soil. Anal Bioanal Chem 411:2687–2696. https://doi.org/10.1007/s00216-019-01715-3
Petrie B, Barden R, Kasprzyk-Hordern B (2015) A review on emerging contaminants in wastewaters and the environment: current knowledge, understudied areas and recommendations for future monitoring. Water Res 72:3–27. https://doi.org/10.1016/j.watres.2014.08.053
Vodyanitskii YN, Yakovlev AS (2016) Contamination of soils and groundwater with new organic micropollutants: a review. Eurasian Soil Sci 49:560–569. https://doi.org/10.1134/S1064229316050148
Barra Caracciolo A, Topp E, Grenni P (2015) Pharmaceuticals in the environment: biodegradation and effects on natural microbial communities. A review. J Pharm Biomed Anal 106:25–36. https://doi.org/10.1016/j.jpba.2014.11.040
Díaz-Cruz MS, López De Alda MJ, Barceló D (2003) Environmental behavior and analysis of veterinary and human drugs in soils, sediments and sludge. Trends Anal Chem 22:340–351. https://doi.org/10.1016/S0165-9936(03)00603-4
Ahel M, Jeličić I (2001) Phenazone analgesics in soil and groundwater below a municipal solid waste landfill. ACS Symp Ser 791:100–115. https://doi.org/10.1021/bk-2001-0791.ch006
Eckel WP, Ross B, Isensee RK (1993) Pentobarbital found in ground water. Groundwater 31:801–804. https://doi.org/10.1111/j.1745-6584.1993.tb00853.x
Holm JV, Rugge K, Bjerg PL, Christensen TH (1995) Occurrence and distribution of pharmaceutical organic compounds in the groundwater downgradient of a landfill (Grindsted, Denmark). Environ Sci Technol 29:1415–1420. https://doi.org/10.1021/es00005a039
Metzger JW (2004) Drugs in municipal landfills and landfill leachates. In: Pharmaceuticals in the environment. Springer, Berlin, pp 133–137. https://doi.org/10.1007/978-3-662-09259-0_10
Beausse J (2004) Selected drugs in solid matrices: a review of environmental determination, occurrence and properties of principal substances. Trends Anal Chem 23:753–761. https://doi.org/10.1016/j.trac.2004.08.005
Hiller E, Šebesta M (2017) Effect of temperature and soil pH on the sorption of ibuprofen in agricultural soil. Soil Water Res 12:78–85. https://doi.org/10.17221/6/2016-SWR
Li WC (2014) Occurrence, sources, and fate of pharmaceuticals in aquatic environment and soil. Environ Pollut 187:193–201. https://doi.org/10.1016/j.envpol.2014.01.015
Lin K, Gan J (2011) Sorption and degradation of wastewater-associated non-steroidal anti-inflammatory drugs and antibiotics in soils. Chemosphere 83:240–246. https://doi.org/10.1016/j.chemosphere.2010.12.083
Li J, Ye Q, Gan J (2014) Degradation and transformation products of acetaminophen in soil. Water Res 49:44–52. https://doi.org/10.1016/j.watres.2013.11.008
Awad YM, Ok YS, Igalavithana AD, Lee YH, Sonn YK, Usman ARA, Al-Wabel MI, Lee SS (2016) Sulphamethazine in poultry manure changes carbon and nitrogen mineralisation in soils. Chem Ecol 32:899–918. https://doi.org/10.1080/02757540.2016.1216104
Hamscher G, Pawelzick HT, Höper H, Nau H (2005) Different behavior of tetracyclines and sulfonamides in sandy soils after repeated fertilization with liquid manure. Environ Toxicol Chem 24:861–868. https://doi.org/10.1897/04-182r.1
Boxall ABA, Blackwell P, Cavallo R, Kay P, Tolls J (2002) The sorption and transport of a sulphonamide antibiotic in soil systems. Toxicol Lett 131:19–28. https://doi.org/10.1016/S0378-4274(02)00063-2
Leal RMP, Alleoni LRF, Tornisielo VL, Regitano JB (2013) Sorption of fluoroquinolones and sulfonamides in 13 Brazilian soils. Chemosphere 92:979–985. https://doi.org/10.1016/j.chemosphere.2013.03.018
Marengo JR, Kok RA, O’Brien K, Velagaleti RR, Stamm JM (1997) Aerobic biodegradation of (14C)-sarafloxacin hydrochloride in soil. Environ Toxicol Chem 16:462–471. https://doi.org/10.1002/etc.5620160311
Nowara A, Burhenne J, Spiteller M (1997) Binding of fluoroquinolone carboxylic acid derivatives to clay minerals. J Agric Food Chem 45:1459–1463. https://doi.org/10.1021/jf960215l
Rabølle M, Spliid NH (2000) Sorption and mobility of metronidazole, olaquindox, oxytetracycline and tylosin in soil. Chemosphere 40:715–722. https://doi.org/10.1016/S0045-6535(99)00442-7
Ter Laak TL, Gebbink WA, Tolls J (2006) The effect of pH and ionic strength on the sorption of sulfachloropyridazine, tylosin, and oxytetracycline to soil. Environ Toxicol Chem 25:904–911. https://doi.org/10.1897/05-232R.1
Thiele-Bruhn S (2003) Pharmaceutical antibiotic compounds in soils – a review. J Plant Nutr Soil Sci 166:145–167. https://doi.org/10.1002/jpln.200390023
Tolls J (2001) Sorption of veterinary pharmaceuticals in soils: a review. Environ Sci Technol 35:3397–3406. https://doi.org/10.1021/es0003021
Vaz S, Lopes WT, Martin-Neto L (2015) Study of molecular interactions between humic acid from Brazilian soil and the antibiotic oxytetracycline. Environ Technol Innov 4:260–267. https://doi.org/10.1016/j.eti.2015.09.004
Wu C, Spongberg AL, Witter JD (2009) Adsorption and degradation of triclosan and triclocarban in soils and biosolids-amended soils. J Agric Food Chem 57:4900–4905. https://doi.org/10.1021/jf900376c
Drillia P, Stamatelatou K, Lyberatos G (2005) Fate and mobility of pharmaceuticals in solid matrices. Chemosphere 60:1034–1044. https://doi.org/10.1016/j.chemosphere.2005.01.032
Monteiro CS, Boxall A (2010) Occurrence and fate of human pharmaceuticals in the environment. In: Reviews of environmental contamination and toxicology. Springer, New York, pp 53–154. https://doi.org/10.1007/978-1-4419-1157-5
Sabourin L, Beck A, Duenk PW, Kleywegt S, Lapen DR, Li H, Metcalfe CD, Payne M, Topp E (2009) Runoff of pharmaceuticals and personal care products following application of dewatered municipal biosolids to an agricultural field. Sci Total Environ 407:4596–4604. https://doi.org/10.1016/j.scitotenv.2009.04.027
Arye G, Dror I, Berkowitz B (2011) Fate and transport of carbamazepine in soil aquifer treatment (SAT) infiltration basin soils. Chemosphere 82:244–252. https://doi.org/10.1016/j.chemosphere.2010.09.062
Bondarenko S, Gan J, Ernst F, Green R, Baird J, McCullough M (2012) Leaching of pharmaceuticals and personal care products in turfgrass soils during recycled water irrigation. J Environ Qual 41:1268–1274. https://doi.org/10.2134/jeq2011.0355
Chefetz B, Mualem T, Ben-Ari J (2008) Sorption and mobility of pharmaceutical compounds in soil irrigated with reclaimed wastewater. Chemosphere 73:1335–1343. https://doi.org/10.1016/j.chemosphere.2008.06.070
Gibson R, Durán-Álvarez JC, Estrada KL, Chávez A, Jiménez Cisneros B (2010) Accumulation and leaching potential of some pharmaceuticals and potential endocrine disruptors in soils irrigated with wastewater in the Tula Valley, Mexico. Chemosphere 81:1437–1445. https://doi.org/10.1016/j.chemosphere.2010.09.006
Avisar D, Lester Y, Ronen D (2009) Sulfamethoxazole contamination of a deep phreatic aquifer. Sci Total Environ 407:4278–4282. https://doi.org/10.1016/j.scitotenv.2009.03.032
González-Naranjo V, Boltes K, Biel M (2013) Mobility of ibuprofen, a persistent active drug, in soils irrigated with reclaimed water. Plant, Soil Environ 59:68–73. https://doi.org/10.17221/590/2012-pse
Karnjanapiboonwong A, Suski JG, Shah AA, Cai Q, Morse AN, Anderson TA (2011) Occurrence of PPCPs at a wastewater treatment plant and in soil and groundwater at a land application site. Water Air Soil Pollut 216:257–273. https://doi.org/10.1007/s11270-010-0532-8
Li J, Dodgen L, Ye Q, Gan J (2013) Degradation kinetics and metabolites of carbamazepine in soil. Environ Sci Technol 47:3678–3684. https://doi.org/10.1021/es304944c
Pedersen JA, Soliman M, Suffet IH (2005) Human pharmaceuticals, hormones, and personal care product ingredients in runoff from agricultural fields irrigated with treated wastewater. J Agric Food Chem 53:1625–1632. https://doi.org/10.1021/jf049228m
Snyder SA, Leising J, Westerhoff P, Yoon Y, Mash HE, Vanderford BJ (2004) Biological and physical attenuation of endocrine disruptors and pharmaceuticals: implications for water reuse. Groundw Monit Remediat 24:108–118
Al-Farsi RS, Ahmed M, Al-Busaidi A, Choudri BS (2017) Translocation of pharmaceuticals and personal care products (PPCPs) into plant tissues: a review. Emerg Contam 3:132–137. https://doi.org/10.1016/j.emcon.2018.02.001
Boxall ABA, Johnson P, Smith EJ, Sinclair CJ, Stutt E, Levy LS (2006) Uptake of veterinary medicines from soils into plants. J Agric Food Chem 54:2288–2297. https://doi.org/10.1021/jf053041t
Carter LJ, Garman CD, Ryan J, Dowle A, Bergström E, Thomas-Oates J, Boxall ABA (2014) Fate and uptake of pharmaceuticals in soil-earthworm systems. Environ Sci Technol 48:5955–5963. https://doi.org/10.1021/es500567w
Carvalho PN, Basto MCP, Almeida CMR, Brix H (2014) A review of plant–pharmaceutical interactions: from uptake and effects in crop plants to phytoremediation in constructed wetlands. Environ Sci Pollut Res 21:11729–11763. https://doi.org/10.1007/s11356-014-2550-3
Kalaji HM, Rastogi A (2017) Pharmaceutical compounds: an emerging pollutant (a review on plant-pharmaceuticals interaction). Chiang Mai J Sci 44:287–297
Wu X, Dodgen LK, Conkle JL, Gan J (2015) Plant uptake of pharmaceutical and personal care products from recycled water and biosolids: a review. Sci Total Environ 536:655–666. https://doi.org/10.1016/j.scitotenv.2015.07.129
Kinney CA, Furlong ET, Kolpin DW, Burkhardt MR, Zaugg SD, Werner SL, Bossio JP, Benotti MJ (2008) Bioaccumulation of pharmaceuticals and other anthropogenic waste indicators in earthworms from agricultural soil amended with biosolid or swine manure. Environ Sci Technol 42:1863–1870. https://doi.org/10.1021/es702304c
Macherius A, Lapen DR, Reemtsma T, Römbke J, Topp E, Coors A (2014) Triclocarban, triclosan and its transformation product methyl triclosan in native earthworm species four years after a commercial-scale biosolids application. Sci Total Environ 472:235–238. https://doi.org/10.1016/j.scitotenv.2013.10.113
Zhao JL, Furlong ET, Schoenfuss HL, Kolpin DW, Bird KL, Feifarek DJ, Schwab EA, Ying GG (2017) Uptake and disposition of select pharmaceuticals by bluegill exposed at constant concentrations in a flow-through aquatic exposure system. Environ Sci Technol 51:4434–4444. https://doi.org/10.1021/acs.est.7b00604
Grossberger A, Hadar Y, Borch T, Chefetz B (2014) Biodegradability of pharmaceutical compounds in agricultural soils irrigated with treated wastewater. Environ Pollut 185:168–177. https://doi.org/10.1016/j.envpol.2013.10.038
Achermann S, Bianco V, Mansfeldt CB, Vogler B, Kolvenbach BA, Corvini PFX, Fenner K (2018) Biotransformation of sulfonamide antibiotics in activated sludge: the formation of pterin-conjugates leads to sustained risk. Environ Sci Technol 52:6265–6274. https://doi.org/10.1021/acs.est.7b06716
Achermann S, Falås P, Joss A, Mansfeldt CB, Men Y, Vogler B, Fenner K (2018) Trends in micropollutant biotransformation along a solids retention time gradient. Environ Sci Technol 52:11601–11611. https://doi.org/10.1021/acs.est.8b02763
Kawabata K, Sugihara K, Sanoh S, Kitamura S, Ohta S (2013) Photodegradation of pharmaceuticals in the aquatic environment by sunlight and UV-A, -B and -C irradiation. J Toxicol Sci 38:215–223. https://doi.org/10.2131/jts.38.215
Mitchell SM, Ullman JL, Teel AL, Watts RJ (2014) PH and temperature effects on the hydrolysis of three β-lactam antibiotics: ampicillin, cefalotin and cefoxitin. Sci Total Environ 466–467:547–555. https://doi.org/10.1016/j.scitotenv.2013.06.027
Calza P, Massolino C, Monaco G, Medana C, Baiocchi C (2008) Study of the photolytic and photocatalytic transformation of amiloride in water. J Pharm Biomed Anal 48:315–320. https://doi.org/10.1016/j.jpba.2008.01.014
Isidori M, Lavorgna M, Nardelli A, Parrella A, Previtera L, Rubino M (2005) Ecotoxicity of naproxen and its phototransformation products. Sci Total Environ 348:93–101. https://doi.org/10.1016/j.scitotenv.2004.12.068
Marotta R, Spasiano D, Di Somma I, Andreozzi R (2013) Photodegradation of naproxen and its photoproducts in aqueous solution at 254 nm: a kinetic investigation. Water Res 47:373–383. https://doi.org/10.1016/j.watres.2012.10.016
Méndez-Arriaga F, Esplugas S, Giménez J (2008) Photocatalytic degradation of non-steroidal anti-inflammatory drugs with TiO2 and simulated solar irradiation. Water Res 42:585–594. https://doi.org/10.1016/j.watres.2007.08.002
Packer JL, Werner JJ, Latch DE, McNeill K, Arnold WA (2003) Photochemical fate of pharmaceuticals in the environment: naproxen, diclofenac, clofibric acid, and ibuprofen. Aquat Sci 65:342–351. https://doi.org/10.1007/s00027-003-0671-8
Vulava VM, Cory WC, Murphey VL, Ulmer CZ (2016) Sorption, photodegradation, and chemical transformation of naproxen and ibuprofen in soils and water. Sci Total Environ 565:1063–1070. https://doi.org/10.1016/j.scitotenv.2016.05.132
Yamamoto H, Nakamura Y, Moriguchi S, Nakamura Y, Honda Y, Tamura I, Hirata Y, Hayashi A, Sekizawa J (2009) Persistence and partitioning of eight selected pharmaceuticals in the aquatic environment: laboratory photolysis, biodegradation, and sorption experiments. Water Res 43:351–362. https://doi.org/10.1016/j.watres.2008.10.039
Thiele-Bruhn S, Peters D (2007) Photodegradation of pharmaceutical antibiotics on slurry and soil surfaces. Landbauforsch Volkenrode 57:13–23
Aissaoui S, Ouled-Haddar H, Sifour M, Harrouche K, Sghaier H (2017) Metabolic and co-metabolic transformation of diclofenac by Enterobacter hormaechei D15 isolated from activated sludge. Curr Microbiol 74:381–388. https://doi.org/10.1007/s00284-016-1190-x
Amorim CL, Moreira IS, Maia AS, Tiritan ME, Castro PML (2014) Biodegradation of ofloxacin, norfloxacin, and ciprofloxacin as single and mixed substrates by Labrys portucalensis F11. Appl Microbiol Biotechnol 98:3181–3190. https://doi.org/10.1007/s00253-013-5333-8
Kim YM, Murugesan K, Schmidt S, Bokare V, Jeon JR, Kim EJ, Chang YS (2011) Triclosan susceptibility and co-metabolism – a comparison for three aerobic pollutant-degrading bacteria. Bioresour Technol 102:2206–2212. https://doi.org/10.1016/j.biortech.2010.10.009
Li Y, Wu B, Zhu G, Liu Y, Ng WJ, Appan A, Tan SK (2016) High-throughput pyrosequencing analysis of bacteria relevant to cometabolic and metabolic degradation of ibuprofen in horizontal subsurface flow constructed wetlands. Sci Total Environ 562:604–613. https://doi.org/10.1016/j.scitotenv.2016.04.020
Marchlewicz A, Domaradzka D, Guzik U, Wojcieszyńska D (2016) Bacillus thuringiensis B1(2015b) is a gram-positive bacteria able to degrade naproxen and ibuprofen. Water Air Soil Pollut 227:197–197. https://doi.org/10.1007/s11270-016-2893-0
Marchlewicz A, Guzik U, Smułek W, Wojcieszyńska D (2017) Exploring the degradation of ibuprofen by Bacillus thuringiensis B1(2015b): the new pathway and factors affecting degradation. Molecules 22:1676. https://doi.org/10.3390/molecules22101676
Moreira IS, Bessa VS, Murgolo S, Piccirillo C, Mascolo G, Castro PML (2018) Biodegradation of diclofenac by the bacterial strain Labrys portucalensis F11. Ecotoxicol Environ Saf 152:104–113. https://doi.org/10.1016/j.ecoenv.2018.01.040
Palyzová A, Zahradník J, Marešová H, Řezanka T (2019) Characterization of the catabolic pathway of diclofenac in Raoultella sp. KDF8. Int Biodeter Biodegr 137:88–94. https://doi.org/10.1016/j.ibiod.2018.11.013
Xu B, Xue G, Yang X (2018) Isolation and application of an ibuprofen-degrading bacterium to a biological aerated filter for the treatment of micro-polluted water. Front Environ Sci Eng 12:1–8. https://doi.org/10.1007/s11783-018-1080-5
Żur J, Wojcieszyńska D, Hupert-Kocurek K, Marchlewicz A, Guzik U (2018) Paracetamol – toxicity and microbial utilization. Pseudomonas moorei KB4 as a case study for exploring degradation pathway. Chemosphere 206:192–202. https://doi.org/10.1016/j.chemosphere.2018.04.179
Bessa VS, Moreira IS, Tiritan ME, Castro PML (2017) Enrichment of bacterial strains for the biodegradation of diclofenac and carbamazepine from activated sludge. Int Biodeter Biodegr 120:135–142. https://doi.org/10.1016/j.ibiod.2017.02.008
De Gusseme B, Vanhaecke L, Verstraete W, Boon N (2011) Degradation of acetaminophen by Delftia tsuruhatensis and Pseudomonas aeruginosa in a membrane bioreactor. Water Res 45:1829–1837. https://doi.org/10.1016/j.watres.2010.11.040
Dionisi D, Etteh CC (2019) Effect of process conditions on the aerobic biodegradation of phenol and paracetamol by open mixed microbial cultures. J Environ Chem Eng 7:103282. https://doi.org/10.1016/j.jece.2019.103282
Hay AG, Dees PM, Sayler GS (2001) Growth of a bacterial consortium on triclosan. FEMS Microbiol Ecol 36:105–112. https://doi.org/10.1111/j.1574-6941.2001.tb00830.x
Hu J, Zhang LL, Chen JM, Liu Y (2013) Degradation of paracetamol by Pseudomonas aeruginosa strain HJ1012. J Environ Sci Heal A Toxic/Hazardous Subst Environ Eng 48:791–799. https://doi.org/10.1080/10934529.2013.744650
Li A, Cai R, Cui D, Qiu T, Pang C, Yang J, Ma F, Ren N (2013) Characterization and biodegradation kinetics of a new cold-adapted carbamazepine-degrading bacterium, Pseudomonas sp. CBZ-4. J Environ Sci (China) 25:2281–2290. https://doi.org/10.1016/S1001-0742(12)60293-9
Martin-Laurent F, Topp E, Billet L, Batisson I, Malandain C, Besse-Hoggan P, Morin S, Artigas J, Bonnineau C, Kergoat L, Devers-Lamrani M, Pesce S (2019) Environmental risk assessment of antibiotics in agroecosystems: ecotoxicological effects on aquatic microbial communities and dissemination of antimicrobial resistances and antibiotic biodegradation potential along the soil-water continuum. Environ Sci Pollut Res 26:18930–18937. https://doi.org/10.1007/s11356-019-05122-0
Meade MJ, Waddell RL, Callahan TM (2001) Soil bacteria Pseudomonas putida and Alcaligenes xylosoxidans subsp. denitrificans inactivate triclosan in liquid and solid substrates. FEMS Microbiol Lett 204:45–48. https://doi.org/10.1111/j.1574-6968.2001.tb10860.x
Moreira IS, Bessa VS, Murgolo S, Piccirillo C, Mascolo G, Castro PML (2014) Enantioselective biodegradation of fluoxetine by the bacterial strain. Ecotoxicol Environ Saf 152:104–113. https://doi.org/10.1016/j.ecoenv.2018.01.040
Mulla SI, Wang H, Sun Q, Hu A, Yu CP (2016) Characterization of triclosan metabolism in Sphingomonas sp. strain YL-JM2C. Sci Rep 6:21965. https://doi.org/10.1038/srep21965
Murdoch RW, Hay AG (2013) Genetic and chemical characterization of ibuprofen degradation by Sphingomonas Ibu-2. Microbiol (United Kingdom) 159:621–632. https://doi.org/10.1099/mic.0.062273-0
Murdoch RW, Hay AG (2005) Formation of catechols via removal of acid side chains from ibuprofen and related aromatic acids. Appl Environ Microbiol 71:6121–6125. https://doi.org/10.1128/AEM.71.10.6121-6125.2005
Topp E, Chapman R, Devers-Lamrani M, Hartmann A, Marti R, Martin-Laurent F, Sabourin L, Scott A, Sumarah M (2013) Accelerated biodegradation of veterinary antibiotics in agricultural soil following long-term exposure, and isolation of a sulfamethazine-degrading Microbacterium sp. J Environ Qual 42:173–178. https://doi.org/10.2134/jeq2012.0162
Yang X, Li M, Guo P, Li H, Hu Z, Liu X, Zhang Q (2019) Isolation, screening, and characterization of antibiotic-degrading bacteria for penicillin V potassium (PVK) from soil on a pig farm. Int J Environ Res Public Health 16. https://doi.org/10.3390/ijerph16122166
Zhang L, Hu J, Zhu R, Zhou Q, Chen J (2013) Degradation of paracetamol by pure bacterial cultures and their microbial consortium. Appl Microbiol Biotechnol 97:3687–3698. https://doi.org/10.1007/s00253-012-4170-5
Zhang Q, Dick WA (2014) Growth of soil bacteria, on penicillin and neomycin, not previously exposed to these antibiotics. Sci Total Environ 493:445–453. https://doi.org/10.1016/j.scitotenv.2014.05.114
Topp E, Hendel JG, Lu Z, Chapman R (2006) Biodegradation of caffeine in agricultural soils. Can J Soil Sci 86:533–544. https://doi.org/10.4141/s05-064
Xu J, Wu L, Chang AC (2009) Degradation and adsorption of selected pharmaceuticals and personal care products (PPCPs) in agricultural soils. Chemosphere 77:1299–1305. https://doi.org/10.1016/j.chemosphere.2009.09.063
Ying GG, Yu XY, Kookana RS (2007) Biological degradation of triclocarban and triclosan in a soil under aerobic and anaerobic conditions and comparison with environmental fate modelling. Environ Pollut 150:300–305. https://doi.org/10.1016/j.envpol.2007.02.013
Yu Y, Liu Y, Wu L (2013) Sorption and degradation of pharmaceuticals and personal care products (PPCPs) in soils. Environ Sci Pollut Res 20:4261–4267. https://doi.org/10.1007/s11356-012-1442-7
Topp E, Renaud J, Sumarah M, Sabourin L (2016) Reduced persistence of the macrolide antibiotics erythromycin, clarithromycin and azithromycin in agricultural soil following several years of exposure in the field. Sci Total Environ 562:136–144. https://doi.org/10.1016/j.scitotenv.2016.03.210
Topp E, Hendel JG, Lapen DR, Chapman R (2008) Fate of the nonsteroidal anti-inflammatory drug naproxen in agricultural soil receiving liquid municipal biosolids. Environ Toxicol Chem 27:2005–2010. https://doi.org/10.1897/07-644.1
Carr DL, Morse AN, Zak JC, Anderson TA (2011) Biological degradation of common pharmaceuticals and personal care products in soils with high water content. Water Air Soil Pollut 217:127–134. https://doi.org/10.1007/s11270-010-0573-z
Girardi C, Nowak KM, Carranza-Diaz O, Lewkow B, Miltner A, Gehre M, Schäffer A, Kästner M (2013) Microbial degradation of the pharmaceutical ibuprofen and the herbicide 2,4-D in water and soil – use and limits of data obtained from aqueous systems for predicting their fate in soil. Sci Total Environ 444:32–42. https://doi.org/10.1016/j.scitotenv.2012.11.051
Al-Rajab AJ, Sabourin L, Lapen DR, Topp E (2010) The non-steroidal anti-inflammatory drug diclofenac is readily biodegradable in agricultural soils. Sci Total Environ 409:78–82. https://doi.org/10.1016/j.scitotenv.2010.09.020
Facey SJ, Nebel BA, Kontny L, Allgaier M, Hauer B (2018) Rapid and complete degradation of diclofenac by native soil microorganisms. Environ Technol Innov 10:55–61. https://doi.org/10.1016/j.eti.2017.12.009
Thelusmond JR, Kawka E, Strathmann TJ, Cupples AM (2018) Diclofenac, carbamazepine and triclocarban biodegradation in agricultural soils and the microorganisms and metabolic pathways affected. Sci Total Environ 640–641:1393–1410. https://doi.org/10.1016/j.scitotenv.2018.05.403
Chen J, Jiang X, Tong T, Miao S, Huang J, Xie S (2019) Sulfadiazine degradation in soils: dynamics, functional gene, antibiotic resistance genes and microbial community. Sci Total Environ 691:1072–1081. https://doi.org/10.1016/j.scitotenv.2019.07.230
Al-Rajab AJ, Sabourin L, Lapen DR, Topp E (2015) Dissipation of triclosan, triclocarban, carbamazepine and naproxen in agricultural soil following surface or sub-surface application of dewatered municipal biosolids. Sci Total Environ 512–513:480–488. https://doi.org/10.1016/j.scitotenv.2015.01.075
Butler E, Whelan MJ, Ritz K, Sakrabani R, van Egmond R (2011) Effects of triclosan on soil microbial respiration. Environ Toxicol Chem 30:360–366. https://doi.org/10.1002/etc.405
Cha J, Cupples AM (2010) Triclocarban and triclosan biodegradation at field concentrations and the resulting leaching potentials in three agricultural soils. Chemosphere 81:494–499. https://doi.org/10.1016/j.chemosphere.2010.07.040
Lozano N, Rice CP, Ramirez M, Torrents A (2013) Fate of triclocarban, triclosan and methyltriclosan during wastewater and biosolids treatment processes. Water Res 47:4519–4527. https://doi.org/10.1016/j.watres.2013.05.015
Lozano N, Rice CP, Ramirez M, Torrents A (2010) Fate of triclosan in agricultural soils after biosolid applications. Chemosphere 78:760–766. https://doi.org/10.1016/j.chemosphere.2009.10.043
Thelusmond JR, Strathmann TJ, Cupples AM (2019) Carbamazepine, triclocarban and triclosan biodegradation and the phylotypes and functional genes associated with xenobiotic degradation in four agricultural soils. Sci Total Environ 657:1138–1149. https://doi.org/10.1016/j.scitotenv.2018.12.145
Walters E, McClellan K, Halden RU (2010) Occurrence and loss over three years of 72 pharmaceuticals and personal care products from biosolids-soil mixtures in outdoor mesocosms. Water Res 44:6011–6020. https://doi.org/10.1016/j.watres.2010.07.051
Waria M, O’Connor GA, Toor GS (2011) Biodegradation of triclosan in biosolids-amended soils. Environ Toxicol Chem 30:2488–2496. https://doi.org/10.1002/etc.666
Ying GG, Yu XY, Kookana RS (2007) Biological degradation of triclocarban and triclosan in a soil under aerobic and anaerobic conditions and comparison with environmental fate modelling. Environ Pollut 150:300–305. https://doi.org/10.1016/j.envpol.2007.02.013
Chen ZF, Ying GG, Ma YB, Lai HJ, Chen F, Pan CG (2013) Occurrence and dissipation of three azole biocides climbazole, clotrimazole and miconazole in biosolid-amended soils. Sci Total Environ 452–453:377–383. https://doi.org/10.1016/j.scitotenv.2013.03.004
García-Valcárcel AI, Tadeo JL (2012) Influence of moisture on the availability and persistence of clotrimazole and fluconazole in sludge-amended soil. Environ Toxicol Chem 31:501–507. https://doi.org/10.1002/etc.1711
Sabourin L, Al-Rajab AJ, Chapman R, Lapen DR, Topp E (2011) Fate of the antifungal drug clotrimazole in agricultural soil. Environ Toxicol Chem 30:582–587. https://doi.org/10.1002/etc.432
Brodin T, Piovano S, Fick J, Klaminder J, Heynen M, Jonsson M (2014) Ecological effects of pharmaceuticals in aquatic systems – impacts through behavioural alterations. Philos Trans R Soc B Biol Sci 369. https://doi.org/10.1098/rstb.2013.0580
Fent K (2008) Effects of pharmaceuticals on aquatic organisms. In: Pharmaceuticals in the environment. Springer, Berlin, pp 175–203. https://doi.org/10.1007/978-3-540-74664-5_12
Gaw S, Thomas KV, Hutchinson TH (2014) Sources, impacts and trends of pharmaceuticals in the marine and coastal environment. Philos Trans R Soc B Biol Sci 369. https://doi.org/10.1098/rstb.2013.0572
Patel M, Kumar R, Kishor K, Mlsna T, Pittman CU, Mohan D (2019) Pharmaceuticals of emerging concern in aquatic systems: chemistry, occurrence, effects, and removal methods. Chem Rev 119:3510–3673. https://doi.org/10.1021/acs.chemrev.8b00299
Heuer H, Schmitt H, Smalla K (2011) Antibiotic resistance gene spread due to manure application on agricultural fields. Curr Opin Microbiol 14:236–243. https://doi.org/10.1016/j.mib.2011.04.009
Ghlichloo I, Gerriets V (2020) Nonsteroidal anti-inflammatory drugs (NSAIDs). In: Treatment of chronic pain conditions: a comprehensive handbook. Springer, New York, pp 77–79. https://doi.org/10.1007/978-1-4939-6976-0_21
Farré M, Ferrer I, Ginebreda A, Figueras M, Olivella L, Tirapu L, Vilanova M, Barceló D (2001) Determination of drugs in surface water and wastewater samples by liquid chromatography-mass spectrometry: methods and preliminary results including toxicity studies with Vibrio fischeri. J Chromatogr A:187–197. https://doi.org/10.1016/S0021-9673(01)01154-2
Kermia AEB, Fouial-Djebbar D, Trari M (2016) Occurrence, fate and removal efficiencies of pharmaceuticals in wastewater treatment plants (WWTPs) discharging in the coastal environment of Algiers. C R Chim 19:963–970. https://doi.org/10.1016/j.crci.2016.05.005
Madikizela LM, Chimuka L (2017) Occurrence of naproxen, ibuprofen, and diclofenac residues in wastewater and river water of KwaZulu-Natal Province in South Africa. Environ Monit Assess 189:348. https://doi.org/10.1007/s10661-017-6069-1
Santos JL, Aparicio I, Alonso E (2007) Occurrence and risk assessment of pharmaceutically active compounds in wastewater treatment plants. A case study: Seville city (Spain). Environ Int 33:596–601. https://doi.org/10.1016/j.envint.2006.09.014
Ternes TA (1998) Occurrence of drugs in German sewage treatment plants and rivers. Water Res 32:3245–3260. https://doi.org/10.1016/S0043-1354(98)00099-2
Tewari S, Jindal R, Kho YL, Eo S, Choi K (2013) Major pharmaceutical residues in wastewater treatment plants and receiving waters in Bangkok, Thailand, and associated ecological risks. Chemosphere 91:697–704. https://doi.org/10.1016/j.chemosphere.2012.12.042
Ghoshdastidar AJ, Fox S, Tong AZ (2015) The presence of the top prescribed pharmaceuticals in treated sewage effluents and receiving waters in southwest Nova Scotia, Canada. Environ Sci Pollut Res 22:689–700. https://doi.org/10.1007/s11356-014-3400-z
Öllers S, Singer HP, Fässler P, Müller SR (2001) Simultaneous quantification of neutral and acidic pharmaceuticals and pesticides at the low-ng/l level in surface and waste water. J Chromatogr A 911:225–234. https://doi.org/10.1016/S0021-9673(01)00514-3
Grenni P, Patrolecco L, Ademollo N, Di Lenola M, Barra Caracciolo A (2014) Capability of the natural microbial community in a river water ecosystem to degrade the drug naproxen. Environ Sci Pollut Res 21:13470–13479. https://doi.org/10.1007/s11356-014-3276-y
Grenni P, Patrolecco L, Ademollo N, Tolomei A, Barra Caracciolo A (2013) Degradation of gemfibrozil and naproxen in a river water ecosystem. Microchem J 107:158–164. https://doi.org/10.1016/j.microc.2012.06.008
Cruz-Morató C, Ferrando-Climent L, Rodriguez-Mozaz S, Barceló D, Marco-Urrea E, Vicent T, Sarrà M (2013) Degradation of pharmaceuticals in non-sterile urban wastewater by Trametes versicolor in a fluidized bed bioreactor. Water Res 47:5200–5210. https://doi.org/10.1016/j.watres.2013.06.007
Ding T, Lin K, Yang B, Yang M, Li J, Li W, Gan J (2017) Biodegradation of naproxen by freshwater algae Cymbella sp. and Scenedesmus quadricauda and the comparative toxicity. Bioresour Technol 238:164–173. https://doi.org/10.1016/j.biortech.2017.04.018
Marco-Urrea E, Pérez-Trujillo M, Blánquez P, Vicent T, Caminal G (2010) Biodegradation of the analgesic naproxen by Trametes versicolor and identification of intermediates using HPLC-DAD-MS and NMR. Bioresour Technol 101:2159–2166. https://doi.org/10.1016/j.biortech.2009.11.019
Rodarte-Morales AI, Feijoo G, Moreira MT, Lema JM (2012) Biotransformation of three pharmaceutical active compounds by the fungus Phanerochaete chrysosporium in a fed batch stirred reactor under air and oxygen supply. Biodegradation 23:145–156. https://doi.org/10.1007/s10532-011-9494-9
Wojcieszyńska D, Domaradzka D, Hupert-Kocurek K, Guzik U (2014) Bacterial degradation of naproxen – undisclosed pollutant in the environment. J Environ Manage 145:157–161. https://doi.org/10.1016/j.jenvman.2014.06.023
Wojcieszyńska D, Guzik U (2020) Naproxen in the environment: its occurrence, toxicity to nontarget organisms and biodegradation. Appl Microbiol Biotechnol 104:1849–1857. https://doi.org/10.1007/s00253-019-10343-x
Wang S, Gunsch CK (2011) Effects of selected pharmaceutically active compounds on the ammonia oxidizing bacterium Nitrosomonas europaea. Chemosphere 82:565–572. https://doi.org/10.1016/j.chemosphere.2010.10.007
Cycon M, Borymski S, Zolnierczyk B, Piotrowska-Seget Z (2016) Variable effects of non-steroidal anti-inflammatory drugs (NSAIDs) on selected biochemical processes mediated by soil microorganisms. Front Microbiol 7:1969. https://doi.org/10.3389/fmicb.2016.01969
Sanganyado E, Lu Z, Fu Q, Schlenk D, Gan J (2017) Chiral pharmaceuticals: a review on their environmental occurrence and fate processes. Water Res 124:527–542. https://doi.org/10.1016/j.watres.2017.08.003
Wong CS (2006) Environmental fate processes and biochemical transformations of chiral emerging organic pollutants. Anal Bioanal Chem 386:544–558. https://doi.org/10.1007/s00216-006-0424-3
Zhou Y, Wu S, Zhou H, Huang H, Zhao J, Deng Y, Wang H, Yang Y, Yang J, Luo L (2018) Chiral pharmaceuticals: environment sources, potential human health impacts, remediation technologies and future perspective. Environ Int 121:523–537. https://doi.org/10.1016/j.envint.2018.09.041
Baillie TA, Adams WJ, Kaiser DG, Olanoff LS, Halstead GW, Harpootlian H, Van Giessen GJ (1989) Mechanistic studies of the metabolic chiral inversion of (R)-ibuprofen in humans. J Pharmacol Exp Ther 249:517–523
Hao H, Wang G, Sun J (2005) Enantioselective pharmacokinetics of ibuprofen and involved mechanisms. Drug Metab Rev 37:215–234. https://doi.org/10.1081/dmr-200047999
Buser HR, Poiger T, Muller MD (1999) Occurrence and environmental behavior of the chiral pharmaceutical drug ibuprofen in surface waters and in wastewater. Environ Sci Technol 33:2529–2535. https://doi.org/10.1021/es981014w
Khan SJ, Wang L, Hashim NH, Mcdonald JA (2014) Distinct enantiomeric signals of ibuprofen and naproxen in treated wastewater and sewer overflow. Chirality 26:739–746. https://doi.org/10.1002/chir.22258
Camacho-Muñoz D, Kasprzyk-Hordern B (2015) Multi-residue enantiomeric analysis of human and veterinary pharmaceuticals and their metabolites in environmental samples by chiral liquid chromatography coupled with tandem mass spectrometry detection. Anal Bioanal Chem 407:9085–9104. https://doi.org/10.1007/s00216-015-9075-6
Moeder M, Schrader S, Winkler M, Popp P (2000) Solid-phase microextraction-gas chromatography-mass spectrometry of biologically active substances in water samples. J Chromatogr A 873:95–106. https://doi.org/10.1016/S0021-9673(99)01256-X
Winkler M, Lawrence JR, Neu TR (2001) Selective degradation of ibuprofen and clofibric acid in two model river biofilm systems. Water Res 35:3197–3205. https://doi.org/10.1016/S0043-1354(01)00026-4
Żur J, Piński A, Marchlewicz A, Hupert-Kocurek K, Wojcieszyńska D, Guzik U (2018) Organic micropollutants paracetamol and ibuprofen – toxicity, biodegradation, and genetic background of their utilization by bacteria. Environ Sci Pollut Res 25:21498–21524. https://doi.org/10.1007/s11356-018-2517-x
Chen Y, Rosazza JPN (1994) Microbial transformation of ibuprofen by a Nocardia species. Appl Environ Microbiol 60:1292–1296. https://doi.org/10.1128/aem.60.4.1292-1296.1994
Marco-Urrea E, Pérez-Trujillo M, Vicent T, Caminal G (2009) Ability of white-rot fungi to remove selected pharmaceuticals and identification of degradation products of ibuprofen by Trametes versicolor. Chemosphere 74:765–772. https://doi.org/10.1016/j.chemosphere.2008.10.040
Lin AY-C, Plumlee MH, Reinhard M (2006) Natural attenuation of pharmaceuticals and alkylphenol polyethoxylate metabolites during river transport: photochemical and biological transformation. Environ Toxicol Chem 25:1458. https://doi.org/10.1897/05-412R.1
Ashfaq M, Nawaz Khan K, Saif Ur Rehman M, Mustafa G, Faizan Nazar M, Sun Q, Iqbal J, Mulla SI, Yu CP (2017) Ecological risk assessment of pharmaceuticals in the receiving environment of pharmaceutical wastewater in Pakistan. Ecotoxicol Environ Saf 136:31–39. https://doi.org/10.1016/j.ecoenv.2016.10.029
Calderón-Preciado D, Matamoros V, Bayona JM (2011) Occurrence and potential crop uptake of emerging contaminants and related compounds in an agricultural irrigation network. Sci Total Environ 412–413:14–19. https://doi.org/10.1016/j.scitotenv.2011.09.057
Sanyal AK, Roy D, Chowdhury B, Banerjee AB (1993) Ibuprofen, a unique anti-inflammatory compound with antifungal activity against dermatophytes. Lett Appl Microbiol 17:109–111. https://doi.org/10.1111/j.1472-765X.1993.tb01436.x
Elvers KT, Wright SJL (1995) Antibacterial activity of the anti-inflammatory compound ibuprofen. Lett Appl Microbiol 20:82–84. https://doi.org/10.1111/j.1472-765X.1995.tb01291.x
Hussein A, AL-Janabi S (2010) In Vitro antibacterial activity of ibuprofen and acetaminophen. J Glob Infect Dis 2:105. https://doi.org/10.4103/0974-777x.62880
Lawrence JR, Swerhone GDW, Wassenaar LI, Neu TR (2005) Effects of selected pharmaceuticals on riverine biofilm communities. Can J Microbiol 51:655–669. https://doi.org/10.1139/w05-047
Veach A, Bernot MJ, Mitchell JK (2012) The influence of six pharmaceuticals on freshwater sediment microbial growth incubated at different temperatures and UV exposures. Biodegradation 23:497–507. https://doi.org/10.1007/s10532-011-9528-3
Corcoll N, Acuña V, Barceló D, Casellas M, Guasch H, Huerta B, Petrovic M, Ponsatí L, Rodríguez-Mozaz S, Sabater S (2014) Pollution-induced community tolerance to non-steroidal anti-inflammatory drugs (NSAIDs) in fluvial biofilm communities affected by WWTP effluents. Chemosphere 112:185–193. https://doi.org/10.1016/j.chemosphere.2014.03.128
Jiang C, Geng J, Hu H, Ma H, Gao X, Ren H (2017) Impact of selected non-steroidal anti-inflammatory pharmaceuticals on microbial community assembly and activity in sequencing batch reactors. PLoS One 12:e0179236. https://doi.org/10.1371/journal.pone.0179236
Stuer-Lauridsen F, Birkved M, Hansen LP, Holten Lützhøft HC, Halling-Sørensen B (2000) Environmental risk assessment of human pharmaceuticals in Denmark after normal therapeutic use. Chemosphere 40:783–793. https://doi.org/10.1016/S0045-6535(99)00453-1
European Commision (EC) (2012) Report from the Commission to the European parliament and the Council on the outcome of the review of Annex X to Directive 2000/60/EC of the European Parliament and of the Council on priority substances in the field of water policy [WWW Document]. Resources. https://doi.org/10.1007/s11837-012-0378-1
Joss A, Keller E, Alder AC, Göbel A, McArdell CS, Ternes T, Siegrist H (2005) Removal of pharmaceuticals and fragrances in biological wastewater treatment. Water Res 39:3139–3152. https://doi.org/10.1016/j.watres.2005.05.031
Paxéus N (2004) Removal of selected non-steroidal anti-inflammatory drugs (NSAIDs), gemfibrozil, carbamazepine, β-blockers, trimethoprim and triclosan in conventional wastewater treatment plants in five EU countries and their discharge to the aquatic environment. Water Sci Technol 50:253–260. https://doi.org/10.2166/wst.2004.0335
Zhang Y, Geißen SU, Gal C (2008) Carbamazepine and diclofenac: removal in wastewater treatment plants and occurrence in water bodies. Chemosphere 73:1151–1161. https://doi.org/10.1016/j.chemosphere.2008.07.086
Azzouz A, Ballesteros E (2012) Combined microwave-assisted extraction and continuous solid-phase extraction prior to gas chromatography-mass spectrometry determination of pharmaceuticals, personal care products and hormones in soils, sediments and sludge. Sci Total Environ 419:208–215. https://doi.org/10.1016/j.scitotenv.2011.12.058
Christou A, Karaolia P, Hapeshi E, Michael C, Fatta-Kassinos D (2017) Long-term wastewater irrigation of vegetables in real agricultural systems: concentration of pharmaceuticals in soil, uptake and bioaccumulation in tomato fruits and human health risk assessment. Water Res 109:24–34. https://doi.org/10.1016/j.watres.2016.11.033
Gavrilescu M, Demnerová K, Aamand J, Agathos S, Fava F (2015) Emerging pollutants in the environment: present and future challenges in biomonitoring, ecological risks and bioremediation. N Biotechnol 32:147–156. https://doi.org/10.1016/j.nbt.2014.01.001
Sathishkumar P, Meena RAA, Palanisami T, Ashokkumar V, Palvannan T, Gu FL (2020) Occurrence, interactive effects and ecological risk of diclofenac in environmental compartments and biota – a review. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2019.134057
Johnson AC, Dumont E, Williams RJ, Oldenkamp R, Cisowska I, Sumpter JP (2013) Do concentrations of ethinylestradiol, estradiol, and diclofenac in European rivers exceed proposed EU environmental quality standards? Environ Sci Technol 47:12297–12304. https://doi.org/10.1021/es4030035
Lonappan L, Brar SK, Das RK, Verma M, Surampalli RY (2016) Diclofenac and its transformation products: environmental occurrence and toxicity – a review. Environ Int 96:127–138. https://doi.org/10.1016/j.envint.2016.09.014
Sousa JCG, Ribeiro AR, Barbosa MO, Pereira MFR, Silva AMT (2018) A review on environmental monitoring of water organic pollutants identified by EU guidelines. J Hazard Mater. https://doi.org/10.1016/j.jhazmat.2017.09.058
Domaradzka D, Guzik U, Wojcieszyńska D (2015) Biodegradation and biotransformation of polycyclic non-steroidal anti-inflammatory drugs. Rev Environ Sci Biotechnol 14:229–239. https://doi.org/10.1007/s11157-015-9364-8
Hata T, Kawai S, Okamura H, Nishida T (2010) Removal of diclofenac and mefenamic acid by the white rot fungus Phanerochaete sordida YK-624 and identification of their metabolites after fungal transformation. Biodegradation 21:681–689. https://doi.org/10.1007/s10532-010-9334-3
Marco-Urrea E, Pérez-Trujillo M, Cruz-Morató C, Caminal G, Vicent T (2010) Degradation of the drug sodium diclofenac by Trametes versicolor pellets and identification of some intermediates by NMR. J Hazard Mater 176:836–842. https://doi.org/10.1016/j.jhazmat.2009.11.112
Rodarte-Morales AI, Feijoo G, Moreira MT, Lema JM (2011) Degradation of selected pharmaceutical and personal care products (PPCPs) by white-rot fungi. World J Microbiol Biotechnol 27:1839–1846. https://doi.org/10.1007/s11274-010-0642-x
Webster R, Pacey M, Winchester T, Johnson P, Jezequel S (1998) Microbial oxidative metabolism of diclofenac: production of 4′-hydroxydiclofenac using Epicoccum nigrum IMI354292. Appl Microbiol Biotechnol 49:371–376. https://doi.org/10.1007/s002530051184
Stylianou K, Hapeshi E, Vasquez MI, Fatta-Kassinos D, Vyrides I (2018) Diclofenac biodegradation by newly isolated Klebsiella sp. KSC: microbial intermediates and ecotoxicological assessment. J Environ Chem Eng 6:3242–3248. https://doi.org/10.1016/j.jece.2018.04.052
Domaradzka D, Guzik U, Hupert-Kocurek K, Wojcieszyńska D (2016) Toxicity of diclofenac and its biotransformation by Raoultella sp. DD4. Pol J Environ Stud 25:2211–2216. https://doi.org/10.15244/pjoes/62681
Ivshina IB, Tyumina EA, Kuzmina MV, Vikhareva EV (2019) Features of diclofenac biodegradation by Rhodococcus ruber IEGM 346. Sci Rep 9:1–13. https://doi.org/10.1038/s41598-019-45732-9
Osorio-Lozada A, Surapaneni S, Skiles GL, Subramanian R (2008) Biosynthesis of drug metabolites using microbes in hollow fiber cartridge reactors: case study of diclofenac metabolism by actinoplanes species. Drug Metab Dispos 36:234–240. https://doi.org/10.1124/dmd.107.019323
Palyzová A, Zahradník J, Marešová H, Sokolová L, Kyslíková E, Grulich M, Štěpánek V, Řezanka T, Kyslík P (2018) Potential of the strain Raoultella sp. KDF8 for removal of analgesics. Folia Microbiol (Praha) 63:273–282. https://doi.org/10.1007/s12223-017-0563-2
Dutta NK, Kumar KA, Mazumdar K, Dastidar SG, Ray R, Chakrabarty AN (2004) In vitro and in vivo antimycobacterial activity of antiinflammatory drug, diclofenac sodium. Indian J Exp Biol 42:922–927
Salem-Milani A, Balaei-Gajan E, Rahimi S, Moosavi Z, Abdollahi A, Zakeri-Milani P, Bolourian M (2013) Antibacterial effect of diclofenac sodium on Enterococcus faecalis. J Dent (Tehran) 10:16–22
Bhattacharya S, Akula Y, Mitongo GM, Khorram Q (2017) Comparison between effects of antibiotics, NSAIDs and their mixture on the growth of microorganisms. Porto Biomed J 2:176–177. https://doi.org/10.1016/j.pbj.2017.07.006
Mazumdar K, Dutta NK, Dastidar SG, Motohashi N, Shirataki Y (2006) Diclofenac in the management of E. coli urinary tract infections. In Vivo (Brooklyn) 20:613–620
Dastidar SG, Ganguly K, Chaudhuri K, Chakrabarty AN (2000) The anti-bacterial action of diclofenac shown by inhibition of DNA synthesis. Int J Antimicrob Agents 14:249–251. https://doi.org/10.1016/S0924-8579(99)00159-4
Dutta NK, Annadurai S, Mazumdar K, Dastidar SG, Kristiansen JE, Molnar J, Martins M, Amaral L (2007) Potential management of resistant microbial infections with a novel non-antibiotic: the anti-inflammatory drug diclofenac sodium. Int J Antimicrob Agents 30:242–249. https://doi.org/10.1016/j.ijantimicag.2007.04.018
Dutta NK, Mazumdar K, Dastidar SG, Park JH (2007) Activity of diclofenac used alone and in combination with streptomycin against Mycobacterium tuberculosis in mice. Int J Antimicrob Agents 30:336–340. https://doi.org/10.1016/j.ijantimicag.2007.04.016
Thelusmond JR, Strathmann TJ, Cupples AM (2016) The identification of carbamazepine biodegrading phylotypes and phylotypes sensitive to carbamazepine exposure in two soil microbial communities. Sci Total Environ 571:1241–1252. https://doi.org/10.1016/j.scitotenv.2016.07.154
Anderson BJ (2008) Paracetamol (Acetaminophen): mechanisms of action. Pediatr Anesth 18:915–921. https://doi.org/10.1111/j.1460-9592.2008.02764.x
Jozwiak-Bebenista M, Nowak JZ (2014) Paracetamol: mechanism of action, applications and safety concern. Acta Pol Pharm Drug Res 71:11–23
Bound JP, Voulvoulis N (2006) Predicted and measured concentrations for selected pharmaceuticals in UK rivers: implications for risk assessment. Water Res 40:2885–2892. https://doi.org/10.1016/j.watres.2006.05.036
Chinnaiyan P, Thampi SG, Kumar M, Mini KM (2018) Pharmaceutical products as emerging contaminant in water: relevance for developing nations and identification of critical compounds for Indian environment. Environ Monit Assess 190:1–13. https://doi.org/10.1007/s10661-018-6672-9
Gómez MJ, Martínez Bueno MJ, Lacorte S, Fernández-Alba AR, Agüera A (2007) Pilot survey monitoring pharmaceuticals and related compounds in a sewage treatment plant located on the Mediterranean coast. Chemosphere 66:993–1002. https://doi.org/10.1016/j.chemosphere.2006.07.051
Gros M, Petrović M, Barceló D (2006) Development of a multi-residue analytical methodology based on liquid chromatography-tandem mass spectrometry (LC-MS/MS) for screening and trace level determination of pharmaceuticals in surface and wastewaters. Talanta 70:678–690. https://doi.org/10.1016/j.talanta.2006.05.024
Grujić S, Vasiljević T, Laušević M (2009) Determination of multiple pharmaceutical classes in surface and ground waters by liquid chromatography-ion trap-tandem mass spectrometry. J Chromatogr A 1216:4989–5000. https://doi.org/10.1016/j.chroma.2009.04.059
Khetan SK, Collins TJ (2007) Human pharmaceuticals in the aquatic environment: a challenge to green chemistry. Chem Rev 107:2319–2364. https://doi.org/10.1021/cr020441w
Kolpin DW, Furlong ET, Meyer MT, Thurman EM, Zaugg SD, Barber LB, Buxton HT (2002) Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999-2000: a national reconnaissance. Environ Sci Technol 36:1202–1211. https://doi.org/10.1021/es011055j
Kosma CI, Lambropoulou DA, Albanis TA (2010) Occurrence and removal of PPCPs in municipal and hospital wastewaters in Greece. J Hazard Mater 179:804–817. https://doi.org/10.1016/j.jhazmat.2010.03.075
Luo Y, Guo W, Ngo HH, Nghiem LD, Hai FI, Zhang J, Liang S, Wang XC (2014) A review on the occurrence of micropollutants in the aquatic environment and their fate and removal during wastewater treatment. Sci Total Environ 473–474:619–641. https://doi.org/10.1016/j.scitotenv.2013.12.065
Mutiyar PK, Gupta SK, Mittal AK (2018) Fate of pharmaceutical active compounds (PhACs) from River Yamuna, India: an ecotoxicological risk assessment approach. Ecotoxicol Environ Saf 150:297–304. https://doi.org/10.1016/j.ecoenv.2017.12.041
Roberts PH, Thomas KV (2006) The occurrence of selected pharmaceuticals in wastewater effluent and surface waters of the lower Tyne catchment. Sci Total Environ 356:143–153. https://doi.org/10.1016/j.scitotenv.2005.04.031
Wiegel S, Aulinger A, Brockmeyer R, Harms H, Löffler J, Reincke H, Schmidt R, Stachel B, Von Tümpling W, Wanke A (2004) Pharmaceuticals in the river Elbe and its tributaries. Chemosphere 57:107–126. https://doi.org/10.1016/j.chemosphere.2004.05.017
Esterhuizen-Londt M, Schwartz K, Pflugmacher S (2016) Using aquatic fungi for pharmaceutical bioremediation: uptake of acetaminophen by Mucor hiemalis does not result in an enzymatic oxidative stress response. Fungal Biol 120:1249–1257. https://doi.org/10.1016/j.funbio.2016.07.009
Hart A, Orr DL (1975) The degradation of paracetamol (4-hydroxyacetanilide) and other substituted acetanilides by a Penicillium species. Antonie Van Leeuwenhoek 41:239–247. https://doi.org/10.1007/bf02565059
Chopra S, Kumar D (2020) Characterization, optimization and kinetics study of acetaminophen degradation by Bacillus drentensis strain S1 and waste water degradation analysis. Bioresour Bioprocess 7:9. https://doi.org/10.1186/s40643-020-0297-x
Hu J, Zhou L, Zhou Q, Wei F, Zhang L, Chen J (2012) Biodegradation of paracetamol by aerobic granules in a sequencing batch reactor (SBR). Adv Mat Res 441:531–535
Wei F, Zhou Q, Leng S, Zhang L, Chen J (2011) Isolation, identification and biodegradation characteristics of a new bacterial strain degrading paracetamol. Environ Sci 32:1813–1819
Wu S, Zhang L, Chen J (2012) Paracetamol in the environment and its degradation by microorganisms. Appl Microbiol Biotechnol 96:875–884. https://doi.org/10.1007/s00253-012-4414-4
De Oliveira LLD, Antunes SC, Gonçalves F, Rocha O, Nunes B (2016) Acute and chronic ecotoxicological effects of four pharmaceuticals drugs on cladoceran Daphnia magna. Drug Chem Toxicol 39:13–21. https://doi.org/10.3109/01480545.2015.1029048
Kim Y, Choi K, Jung J, Park S, Kim PG, Park J (2007) Aquatic toxicity of acetaminophen, carbamazepine, cimetidine, diltiazem and six major sulfonamides, and their potential ecological risks in Korea. Environ Int 33:370–375. https://doi.org/10.1016/j.envint.2006.11.017
Nunes B, Antunes SC, Santos J, Martins L, Castro BB (2014) Toxic potential of paracetamol to freshwater organisms: a headache to environmental regulators? Ecotoxicol Environ Saf 107:178–185. https://doi.org/10.1016/j.ecoenv.2014.05.027
Alvarino T, Katsou E, Malamis S, Suarez S, Omil F, Fatone F (2014) Inhibition of biomass activity in the via nitrite nitrogen removal processes by veterinary pharmaceuticals. Bioresour Technol 152:477–483. https://doi.org/10.1016/j.biortech.2013.10.107
Calisto V, Esteves VI (2009) Psychiatric pharmaceuticals in the environment. Chemosphere 77:1257–1274. https://doi.org/10.1016/j.chemosphere.2009.09.021
Kinney CA, Furlong ET, Werner SL, Cahill JD (2006) Presence and distribution of wastewater-derived pharmaceuticals in soil irrigated with reclaimed water. Environ Toxicol Chem 25:317. https://doi.org/10.1897/05-187R.1
Kinney CA, Furlong ET, Zaugg SD, Burkhardt MR, Werner SL, Cahill JD, Jorgensen GR (2006) Survey of organic wastewater contaminants in biosolids destined for land application. Environ Sci Technol 40:7207–7215. https://doi.org/10.1021/es0603406
Schultz MM, Furlong ET (2008) Trace analysis of antidepressant pharmaceuticals and their select degradates in aquatic matrixes by LC/ESI/MS/MS. Anal Chem 80:1756–1762. https://doi.org/10.1021/ac702154e
Silva LJG, Lino CM, Meisel LM, Pena A (2012) Selective serotonin re-uptake inhibitors (SSRIs) in the aquatic environment: an ecopharmacovigilance approach. Sci Total Environ 437:185–195. https://doi.org/10.1016/j.scitotenv.2012.08.021
Kwon J-W, Armbrust KL (2006) Laboratory persistence and fate of fluoxetine in aquatic environments. Environ Toxicol Chem 25:2561. https://doi.org/10.1897/05-613R.1
Styrishave B, Halling-Sørensen B, Ingerslev F (2011) Environmental risk assessment of three selective serotonin reuptake inhibitors in the aquatic environment: a case study including a cocktail scenario. Environ Toxicol Chem 30:254–261. https://doi.org/10.1002/etc.372
Ribeiro AR, Afonso CM, Castro PML, Tiritan ME (2013) Enantioselective HPLC analysis and biodegradation of atenolol, metoprolol and fluoxetine. Environ Chem Lett 11:83–90. https://doi.org/10.1007/s10311-012-0383-1
Velázquez YF, Nacheva PM (2017) Biodegradability of fluoxetine, mefenamic acid, and metoprolol using different microbial consortiums. Environ Sci Pollut Res 24:6779–6793. https://doi.org/10.1007/s11356-017-8413-y
Benotti MJ, Brownawell BJ (2009) Microbial degradation of pharmaceuticals in estuarine and coastal seawater. Environ Pollut 157:994–1002. https://doi.org/10.1016/j.envpol.2008.10.009
Suarez S, Lema JM, Omil F (2010) Removal of pharmaceutical and personal care products (PPCPs) under nitrifying and denitrifying conditions. Water Res 44:3214–3224. https://doi.org/10.1016/j.watres.2010.02.040
Suárez S, Reif R, Lema JM, Omil F (2012) Mass balance of pharmaceutical and personal care products in a pilot-scale single-sludge system: influence of T, SRT and recirculation ratio. Chemosphere 89:164–171. https://doi.org/10.1016/j.chemosphere.2012.05.094
Beretsou VG, Psoma AK, Gago-Ferrero P, Aalizadeh R, Fenner K, Thomaidis NS (2016) Identification of biotransformation products of citalopram formed in activated sludge. Water Res 103:205–214. https://doi.org/10.1016/j.watres.2016.07.029
Brooks BW, Foran CM, Richards SM, Weston J, Turner PK, Stanley JK, Solomon KR, Slattery M, La Point TW (2003) Aquatic ecotoxicology of fluoxetine. Toxicol Lett 142:169–183. https://doi.org/10.1016/S0378-4274(03)00066-3
Sehonova P, Svobodova Z, Dolezelova P, Vosmerova P, Faggio C (2018) Effects of waterborne antidepressants on non-target animals living in the aquatic environment: a review. Sci Total Environ 631–632:789–794. https://doi.org/10.1016/j.scitotenv.2018.03.076
Silva LJG, Pereira AMPT, Meisel LM, Lino CM, Pena A (2015) Reviewing the serotonin reuptake inhibitors (SSRIs) footprint in the aquatic biota: uptake, bioaccumulation and ecotoxicology. Environ Pollut 197:127–143. https://doi.org/10.1016/j.envpol.2014.12.002
Fong PP, Ford AT (2014) The biological effects of antidepressants on the molluscs and crustaceans: a review. Aquat Toxicol 151:4–13. https://doi.org/10.1016/j.aquatox.2013.12.003
Schultz MM, Painter MM, Bartell SE, Logue A, Furlong ET, Werner SL, Schoenfuss HL (2011) Selective uptake and biological consequences of environmentally relevant antidepressant pharmaceutical exposures on male fathead minnows. Aquat Toxicol 104:38–47. https://doi.org/10.1016/j.aquatox.2011.03.011
Munoz-Bellido JL, Munoz-Criado S, Garcìa-Rodrìguez JA (2000) Antimicrobial activity of psychotropic drugs. Selective serotonin reuptake inhibitors. Int J Antimicrob Agents 14:177–180. https://doi.org/10.1016/S0924-8579(99)00154-5
Karine de Sousa A, Rocha JE, Gonçalves de Souza T, Sampaio de Freitas T, Ribeiro-Filho J, Melo Coutinho HD (2018) New roles of fluoxetine in pharmacology: antibacterial effect and modulation of antibiotic activity. Microb Pathog 123:368–371. https://doi.org/10.1016/j.micpath.2018.07.040
Lukić I, Getselter D, Ziv O, Oron O, Reuveni E, Koren O, Elliott E (2019) Antidepressants affect gut microbiota and Ruminococcus flavefaciens is able to abolish their effects on depressive-like behavior. Transl Psychiatry 9:1–16. https://doi.org/10.1038/s41398-019-0466-x
Macdonald RL, McLean MJ (1986) Anticonvulsant drugs: mechanisms of action. Adv Neurol 44:713–736
Scheytt T, Mersmann P, Lindstädt R, Heberer T (2005) 1-Octanol/water partition coefficients of 5 pharmaceuticals from human medical care: carbamazepine, clofibric acid, diclofenac, ibuprofen, and propyphenazone. Water Air Soil Pollut 165:3–11. https://doi.org/10.1007/s11270-005-3539-9
Clara M, Strenn B, Gans O, Martinez E, Kreuzinger N, Kroiss H (2005) Removal of selected pharmaceuticals, fragrances and endocrine disrupting compounds in a membrane bioreactor and conventional wastewater treatment plants. Water Res 39:4797–4807. https://doi.org/10.1016/j.watres.2005.09.015
Matsuo H, Sakamoto H, Arizono K, Shinohara R (2011) Behavior of pharmaceuticals in waste water treatment plant in Japan. Bull Environ Contam Toxicol 87:31–35. https://doi.org/10.1007/s00128-011-0299-7
Miao XS, Yang JJ, Metcalfe CD (2005) Carbamazepine and its metabolites in wastewater and in biosolids in a municipal wastewater treatment plant. Environ Sci Technol 39:7469–7475. https://doi.org/10.1021/es050261e
Clara M, Strenn B, Kreuzinger N (2004) Carbamazepine as a possible anthropogenic marker in the aquatic environment: investigations on the behaviour of Carbamazepine in wastewater treatment and during groundwater infiltration. Water Res 38:947–954. https://doi.org/10.1016/j.watres.2003.10.058
Nakada N, Kiri K, Shinohara H, Harada A, Kuroda K, Takizawa S, Takada H (2008) Evaluation of pharmaceuticals and personal care products as water-soluble molecular markers of sewage. Environ Sci Technol 42:6347–6353. https://doi.org/10.1021/es7030856
Tran NH, Li J, Hu J, Ong SL (2014) Occurrence and suitability of pharmaceuticals and personal care products as molecular markers for raw wastewater contamination in surface water and groundwater. Environ Sci Pollut Res 21:4727–4740. https://doi.org/10.1007/s11356-013-2428-9
Williams CF, McLain JET (2012) Soil persistence and fate of carbamazepine, lincomycin, caffeine, and ibuprofen from wastewater reuse. J Environ Qual 41:1473–1480. https://doi.org/10.2134/jeq2011.0353
Maeng SK, Sharma SK, Abel CDT, Magic-Knezev A, Amy GL (2011) Role of biodegradation in the removal of pharmaceutically active compounds with different bulk organic matter characteristics through managed aquifer recharge: batch and column studies. Water Res 45:4722–4736. https://doi.org/10.1016/j.watres.2011.05.043
Buchicchio A, Bianco G, Sofo A, Masi S, Caniani D (2016) Biodegradation of carbamazepine and clarithromycin by Trichoderma harzianum and Pleurotus ostreatus investigated by liquid chromatography – high-resolution tandem mass spectrometry (FTICR MS-IRMPD). Sci Total Environ 557–558:733–739. https://doi.org/10.1016/j.scitotenv.2016.03.119
Golan-Rozen N, Seiwert B, Riemenschneider C, Reemtsma T, Chefetz B, Hadar Y (2015) Transformation pathways of the recalcitrant pharmaceutical compound carbamazepine by the white-rot fungus Pleurotus ostreatus: effects of growth conditions. Environ Sci Technol 49:12351–12362. https://doi.org/10.1021/acs.est.5b02222
Jelic A, Cruz-Morató C, Marco-Urrea E, Sarrà M, Perez S, Vicent T, Petrović M, Barcelo D (2012) Degradation of carbamazepine by Trametes versicolor in an air pulsed fluidized bed bioreactor and identification of intermediates. Water Res 46:955–964. https://doi.org/10.1016/j.watres.2011.11.063
Kang SI, Kang SY, Hur HG (2008) Identification of fungal metabolites of anticonvulsant drug carbamazepine. Appl Microbiol Biotechnol 79:663–669. https://doi.org/10.1007/s00253-008-1459-5
Rodríguez-Rodríguez CE, Marco-Urrea E, Caminal G (2010) Degradation of naproxen and carbamazepine in spiked sludge by slurry and solid-phase Trametes versicolor systems. Bioresour Technol 101:2259–2266. https://doi.org/10.1016/j.biortech.2009.11.089
Ha H, Mahanty B, Yoon S, Kim CG (2016) Degradation of the long-resistant pharmaceutical compounds carbamazepine and diatrizoate using mixed microbial culture. J Environ Sci Heal A Toxic/Hazardous Subst Environ Eng 51:467–471. https://doi.org/10.1080/10934529.2015.1128712
Kittelmann M, Lattmann R, Ghisalba O (1993) Preparation of 10,11-epoxy-carbamazepine and 10,11-dihydro-10-hydroxy-carbamazepine by microbial epoxidation and hydroxylation. Biosci Biotechnol Biochem 57:1589–1590. https://doi.org/10.1271/bbb.57.1589
Gauthier H, Cooper DG, Yargeau V (2008) Biodegradation of pharmaceuticals by common microorganisms. In: WIT transactions on ecology and the environment. WIT Press, Southampton, pp 263–271. https://doi.org/10.2495/WP080261
Nasir NM, Talib SA, Hashim SN, Tay CC (2018) Biodegradation of carbamazepine using fungi and bacteria. J Fundam Appl Sci 9:124. https://doi.org/10.4314/jfas.v9i6s.12
Sauvêtre A, May R, Harpaintner R, Poschenrieder C, Schröder P (2018) Metabolism of carbamazepine in plant roots and endophytic rhizobacteria isolated from Phragmites australis. J Hazard Mater 342:85–95. https://doi.org/10.1016/j.jhazmat.2017.08.006
Sauvêtre A, Schröder P (2015) Uptake of carbamazepine by rhizomes and endophytic bacteria of Phragmites australis. Front Plant Sci 6:83. https://doi.org/10.3389/fpls.2015.00083
Wang Y, Lu J, Mao L, Li J, Yuan Z, Bond PL, Guo J (2019) Antiepileptic drug carbamazepine promotes horizontal transfer of plasmid-borne multi-antibiotic resistance genes within and across bacterial genera. ISME J 13:509–522. https://doi.org/10.1038/s41396-018-0275-x
Kapoor G, Saigal S, Elongavan A (2017) Action and resistance mechanisms of antibiotics: a guide for clinicians. J Anaesthesiol Clin Pharmacol 33:300–305. https://doi.org/10.4103/joacp.JOACP_349_15
Moulin G, Cavalié P, Pellanne I, Chevance A, Laval A, Millemann Y, Colin P, Chauvin C, Antimicrobial Resistance ad hoc Group of the French Food Safety Agency (2008) A comparison of antimicrobial usage in human and veterinary medicine in France from 1999 to 2005. J Antimicrob Chemother 62:617–625. https://doi.org/10.1093/jac/dkn213
Chang Q, Wang W, Regev-Yochay G, Lipsitch M, Hanage WP (2015) Antibiotics in agriculture and the risk to human health: how worried should we be? Evol Appl 8:240–247. https://doi.org/10.1111/eva.12185
Manyi-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. https://doi.org/10.3390/molecules23040795
Stockwell VO, Duffy B (2012) Use of antibiotics in plant agriculture. OIE Rev Sci Tech 31:199–210. https://doi.org/10.20506/rst.31.1.2104
Lulijwa R, Rupia EJ, Alfaro AC (2019) Antibiotic use in aquaculture, policies and regulation, health and environmental risks: a review of the top 15 major producers. Rev Aquac 1–24. https://doi.org/10.1111/raq.12344
Vincent AT, Gauthier J, Derome N, Charette SJ (2019) The rise and fall of antibiotics in aquaculture. In: Microbial communities in aquaculture ecosystems. Springer, Cham, pp 1–19. https://doi.org/10.1007/978-3-030-16190-3_1
Dibner JJ, Richards JD (2005) Antibiotic growth promoters in agriculture: history and mode of action. Poult Sci 84:634–643. https://doi.org/10.1093/ps/84.4.634
Hao H, Cheng G, Iqbal Z, Ai X, Hussain HI, Huang L, Dai M, Wang Y, Liu Z, Yuan Z (2014) Benefits and risks of antimicrobial use in food-producing animals. Front Microbiol 5. https://doi.org/10.3389/fmicb.2014.00288
Jay JM (1995) Antimicrobial food preservatives. In: Handbook of biocide and preservative use. Springer, Dordrecht, pp 334–348. https://doi.org/10.1007/978-94-011-1354-0_12
Al-Jassim N, Hong P-Y (2017) Potential dissemination of ARB and ARGs into soil through the use of treated wastewater for agricultural irrigation: is it a true cause for concern? In: Hashmi M, Strezov V, V.A. (eds) Antibiotics and antibiotics resistance genes in soils. Soil biology, vol 51. Springer, Cham, pp 105–139. https://doi.org/10.1007/978-3-319-66260-2_7
Amador PP, Fernandes RM, Prudêncio MC, Barreto MP, Duarte IM (2015) Antibiotic resistance in wastewater: occurrence and fate of Enterobacteriaceae producers of class A and class C β-lactamases. J Environ Sci Heal A Tox Hazard Subst Environ Eng 50:26–39. https://doi.org/10.1080/10934529.2015.964602
Bouki C, Venieri D, Diamadopoulos E (2013) Detection and fate of antibiotic resistant bacteria in wastewater treatment plants: a review. Ecotoxicol Environ Saf 91:1–9. https://doi.org/10.1016/j.ecoenv.2013.01.016
Pan M, Chu LM (2017) Transfer of antibiotics from wastewater or animal manure to soil and edible crops. Environ Pollut 231:829–836. https://doi.org/10.1016/j.envpol.2017.08.051
Pazda M, Kumirska J, Stepnowski P, Mulkiewicz E (2019) Antibiotic resistance genes identified in wastewater treatment plant systems – a review. Sci Total Environ 697:134023. https://doi.org/10.1016/j.scitotenv.2019.134023
Schwartz T, Kohnen W, Jansen B, Obst U (2003) Detection of antibiotic-resistant bacteria and their resistance genes in wastewater, surface water, and drinking water biofilms. FEMS Microbiol Ecol 43:325–335. https://doi.org/10.1111/j.1574-6941.2003.tb01073.x
Wang W, Zhang W, Liang H, Gao D (2019) Occurrence and fate of typical antibiotics in wastewater treatment plants in Harbin, North-east China. Front Environ Sci Eng 13:1–10. https://doi.org/10.1007/s11783-019-1118-3
Ding Y, Zhang W, Gu C, Xagoraraki I, Li H (2011) Determination of pharmaceuticals in biosolids using accelerated solvent extraction and liquid chromatography/tandem mass spectrometry. J Chromatogr A 1218:10–16. https://doi.org/10.1016/j.chroma.2010.10.112
Jones-Lepp TL, Stevens R (2007) Pharmaceuticals and personal care products in biosolids/sewage sludge: the interface between analytical chemistry and regulation. In: Analytical and bioanalytical chemistry. Springer, New York, pp 1173–1183. https://doi.org/10.1007/s00216-006-0942-z
Munir M, Wong K, Xagoraraki I (2011) Release of antibiotic resistant bacteria and genes in the effluent and biosolids of five wastewater utilities in Michigan. Water Res 45:681–693. https://doi.org/10.1016/j.watres.2010.08.033
Yang L, Liu W, Zhu D, Hou J, Ma T, Wu L, Zhu Y, Christie P (2018) Application of biosolids drives the diversity of antibiotic resistance genes in soil and lettuce at harvest. Soil Biol Biochem 122:131–140. https://doi.org/10.1016/j.soilbio.2018.04.017
Cheng M, Wu L, Huang Y, Luo Y, Christie P (2014) Total concentrations of heavy metals and occurrence of antibiotics in sewage sludges from cities throughout China. J Soil Sediment 14:1123–1135. https://doi.org/10.1007/s11368-014-0850-3
Göbel A, Thomsen A, McArdell CS, Alder AC, Giger W, Theiß N, Löffler D, Ternes TA (2005) Extraction and determination of sulfonamides, macrolides, and trimethoprim in sewage sludge. J Chromatogr A 1085:179–189. https://doi.org/10.1016/j.chroma.2005.05.051
Hölzel CS, Schwaiger K, Harms K, Küchenhoff H, Kunz A, Meyer K, Müller C, Bauer J (2010) Sewage sludge and liquid pig manure as possible sources of antibiotic resistant bacteria. Environ Res 110:318–326. https://doi.org/10.1016/j.envres.2010.02.009
Li W, Shi Y, Gao L, Liu J, Cai Y (2013) Occurrence, distribution and potential affecting factors of antibiotics in sewage sludge of wastewater treatment plants in China. Sci Total Environ 445–446:306–313. https://doi.org/10.1016/j.scitotenv.2012.12.050
Lillenberg M, Yurchenko S, Kipper K, Herodes K, Pihl V, Lõhmus R, Ivask M, Kuu A, Kutti S, Litvin SV, Nei L (2010) Presence of fluoroquinolones and sulfonamides in urban sewage sludge and their degradation as a result of composting. Int J Environ Sci Technol 7:307–312. https://doi.org/10.1007/BF03326140
Núñez-Delgado A, Pousada-Ferradás Y, Álvarez-Rodríguez E, Fernández-Sanjurjo MJ, Conde-Cid M, Nóvoa-Muñoz JC, Arias-Estévez M (2019) Effects of microbiological and non-microbiological treatments of sewage sludge on antibiotics as emerging pollutants present in wastewater: a review. In: Microbial wastewater treatment. Elsevier, Amsterdam, pp 1–17. https://doi.org/10.1016/B978-0-12-816809-7.00001-4
Reinthaler FF, Posch J, Feierl G, Wüst G, Haas D, Ruckenbauer G, Mascher F, Marth E (2003) Antibiotic resistance of E. coli in sewage and sludge. Water Res 37:1685–1690. https://doi.org/10.1016/S0043-1354(02)00569-9
Berendsen BJA, Wegh RS, Memelink J, Zuidema T, Stolker LAM (2015) The analysis of animal faeces as a tool to monitor antibiotic usage. Talanta 132:258–268. https://doi.org/10.1016/j.talanta.2014.09.022
Chen YS, Zhang HB, Luo YM, Song J (2012) Occurrence and assessment of veterinary antibiotics in swine manures: a case study in East China. Chin Sci Bull 57:606–614. https://doi.org/10.1007/s11434-011-4830-3
Dolliver H, Gupta S, Noll S (2008) Antibiotic degradation during manure composting. J Environ Qual 37:1245–1253. https://doi.org/10.2134/jeq2007.0399
Martínez-Carballo E, González-Barreiro C, Scharf S, Gans O (2007) Environmental monitoring study of selected veterinary antibiotics in animal manure and soils in Austria. Environ Pollut 148:570–579. https://doi.org/10.1016/j.envpol.2006.11.035
Massé DI, Saady NMC, Gilbert Y (2014) Potential of biological processes to eliminate antibiotics in livestock manure: an overview. Animals 4:146–163. https://doi.org/10.3390/ani4020146
Olonitola OS, Fahrenfeld N, Pruden A (2015) Antibiotic resistance profiles among mesophilic aerobic bacteria in Nigerian chicken litter and associated antibiotic resistance genes. Poult Sci 94:867–874. https://doi.org/10.3382/ps/pev069
Pan X, Qiang Z, Ben W, Chen M (2011) Residual veterinary antibiotics in swine manure from concentrated animal feeding operations in Shandong Province, China. Chemosphere 84:695–700. https://doi.org/10.1016/j.chemosphere.2011.03.022
Quaik S, Embrandiri A, Ravindran B, Hossain K, Al-Dhabi NA, Arasu MV, Ignacimuthu S, Ismail N (2020) Veterinary antibiotics in animal manure and manure laden soil: scenario and challenges in Asian countries. J King Saud Univ – Sci 32:1300–1305. https://doi.org/10.1016/j.jksus.2019.11.015
Ray P, Chen C, Knowlton KF, Pruden A, Xia K (2017) Fate and effect of antibiotics in beef and dairy manure during static and turned composting. J Environ Qual 46:45–54. https://doi.org/10.2134/jeq2016.07.0269
Van Epps A, Blaney L (2016) Antibiotic residues in animal waste: occurrence and degradation in conventional agricultural waste management practices. Curr Pollut Reports 2:135–155. https://doi.org/10.1007/s40726-016-0037-1
Xie W-Y, Shen Q, Zhao FJ (2018) Antibiotics and antibiotic resistance from animal manures to soil: a review. Eur J Soil Sci 69:181–195. https://doi.org/10.1111/ejss.12494
Zhao L, Dong YH, Wang H (2010) Residues of veterinary antibiotics in manures from feedlot livestock in eight provinces of China. Sci Total Environ 408:1069–1075. https://doi.org/10.1016/j.scitotenv.2009.11.014
Kovalakova P, Cizmas L, McDonald TJ, Marsalek B, Feng M, Sharma VK (2020) Occurrence and toxicity of antibiotics in the aquatic environment: a review. Chemosphere 251:126351. https://doi.org/10.1016/j.chemosphere.2020.126351
Kraemer SA, Ramachandran A, Perron GG (2019) Antibiotic pollution in the environment: from microbial ecology to public policy. Microorganisms 7. https://doi.org/10.3390/microorganisms7060180
Dolliver H, Gupta S (2008) Antibiotic losses in leaching and surface runoff from manure-amended agricultural land. J Environ Qual 37:1227–1237. https://doi.org/10.2134/jeq2007.0392
Gottschall N, Topp E, Edwards M, Payne M, Kleywegt S, Russell P, Lapen DR (2013) Hormones, sterols, and fecal indicator bacteria in groundwater, soil, and subsurface drainage following a high single application of municipal biosolids to a field. Chemosphere 91:275–286. https://doi.org/10.1016/j.chemosphere.2012.10.108
Fahrenfeld N, Knowlton K, Krometis LA, Hession WC, Xia K, Lipscomb E, Libuit K, Green BL, Pruden A (2014) Effect of manure application on abundance of antibiotic resistance genes and their attenuation rates in soil: field-scale mass balance approach. Environ Sci Technol 48:2643–2650. https://doi.org/10.1021/es404988k
Finley RL, Collignon P, Larsson DGJ, McEwen SA, Li X-Z, Gaze WH, Reid-Smith R, Timinouni M, Graham DW, Topp E (2013) The scourge of antibiotic resistance: the important role of the environment. Clin Infect Dis 57:704–710. https://doi.org/10.1093/cid/cit355
Gullberg E, Cao S, Berg OG, Ilbäck C, Sandegren L, Hughes D, Andersson DI (2011) Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathog 7:e1002158. https://doi.org/10.1371/journal.ppat.1002158
Singer AC, Shaw H, Rhodes V, Hart A (2016) Review of antimicrobial resistance in the environment and its relevance to environmental regulators. Front Microbiol 7:1728. https://doi.org/10.3389/fmicb.2016.01728
Urra J, Alkorta I, Mijangos I, Epelde L, Garbisu C (2019) Application of sewage sludge to agricultural soil increases the abundance of antibiotic resistance genes without altering the composition of prokaryotic communities. Sci Total Environ 647:1410–1420. https://doi.org/10.1016/J.SCITOTENV.2018.08.092
Wolters B, Fornefeld E, Jechalke S, Su J-Q, Zhu Y-G, Sørensen SJ, Smalla K, Jacquiod S (2018) Soil amendment with sewage sludge affects soil prokaryotic community composition, mobilome and resistome. FEMS Microbiol Ecol. https://doi.org/10.1093/femsec/fiy193
Al-Ahmad A, Daschner FD, Kümmerer K (1999) Biodegradability of cefotiam, ciprofloxacin, meropenem, penicillin G, and sulfamethoxazole and inhibition of waste water bacteria. Arch Environ Contam Toxicol 37:158–163. https://doi.org/10.1007/s002449900501
Kümmerer K, Al-Ahmad A, Mersch-Sundermann V (2000) Biodegradability of some antibiotics, elimination of the genotoxicity and affection of wastewater bacteria in a simple test. Chemosphere 40:701–710. https://doi.org/10.1016/S0045-6535(99)00439-7
Tomlinson TG, Boon AG, Trotman CNA (1966) Inhibition of nitrification in the activated sludge process of sewage disposal. J Appl Bacteriol 29:266–291. https://doi.org/10.1111/j.1365-2672.1966.tb03477.x
Watkinson AJ, Murby EJ, Costanzo SD (2007) Removal of antibiotics in conventional and advanced wastewater treatment: implications for environmental discharge and wastewater recycling. Water Res 41:4164–4176. https://doi.org/10.1016/j.watres.2007.04.005
Rosendahl I, Siemens J, Kindler R, Groeneweg J, Zimmermann J, Czerwinski S, Lamshöft M, Laabs V, Wilke B-M, Vereecken H, Amelung W (2012) Persistence of the fluoroquinolone antibiotic difloxacin in soil and lacking effects on nitrogen turnover. J Environ Qual 41:1275–1283. https://doi.org/10.2134/jeq2011.0459
Thiele-Bruhn S (2005) Microbial inhibition by pharmaceutical antibiotics in different soils--dose-response relations determined with the iron(III) reduction test. Environ Toxicol Chem 24:869–876. https://doi.org/10.1897/04-166r.1
Semedo M, Song B, Sparrer T, Phillips RL (2018) Antibiotic effects on microbial communities responsible for denitrification and N2O production in grassland soils. Front Microbiol 9:2121. https://doi.org/10.3389/fmicb.2018.02121
Boxall ABA, Fogg LA, Blackwell PA, Blackwell P, Kay P, Pemberton EJ, Croxford A (2004) Veterinary medicines in the environment BT – reviews of environmental contamination and toxicology. In: Reviews of environmental contamination and toxicology. Springer, New York, pp 1–91. https://doi.org/10.1007/0-387-21729-0_1
Brandt KK, Sjøholm OR, Krogh KA, Halling-Sørensen B, Nybroe O (2009) Increased pollution-induced bacterial community tolerance to sulfadiazine in soil hotspots amended with artificial root exudates. Environ Sci Technol 43:2963–2968. https://doi.org/10.1021/es803546y
Cycoń M, Mrozik A, Piotrowska-Seget Z (2019) Antibiotics in the soil environment – degradation and their impact on microbial activity and diversity. Front Microbiol 10:338. https://doi.org/10.3389/fmicb.2019.00338
Grenni P, Ancona V, Barra Caracciolo A (2018) Ecological effects of antibiotics on natural ecosystems: a review. Microchem J 136:25–39. https://doi.org/10.1016/j.microc.2017.02.006
Martinez JL (2009) Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ Pollut 157:2893–2902. https://doi.org/10.1016/j.envpol.2009.05.051
Piotrowska-Długosz A (2017) The effects of antibiotics on the structure, diversity, and function of a soil microbial community. Springer, Cham, pp 283–312. https://doi.org/10.1007/978-3-319-66260-2_15
Pan M, Chu LM (2016) Adsorption and degradation of five selected antibiotics in agricultural soil. Sci Total Environ 545–546:48–56. https://doi.org/10.1016/j.scitotenv.2015.12.040
Braschi I, Blasioli S, Fellet C, Lorenzini R, Garelli A, Pori M, Giacomini D (2013) Persistence and degradation of new β-lactam antibiotics in the soil and water environment. Chemosphere 93:152–159. https://doi.org/10.1016/j.chemosphere.2013.05.016
Liu B, Li Y, Zhang X, Wang J, Gao M (2014) Combined effects of chlortetracycline and dissolved organic matter extracted from pig manure on the functional diversity of soil microbial community. Soil Biol Biochem 74:148–155. https://doi.org/10.1016/j.soilbio.2014.03.005
Ricken B, Fellmann O, Kohler HPE, Schäffer A, Corvini PFX, Kolvenbach BA (2015) Degradation of sulfonamide antibiotics by Microbacterium sp. strain BR1 – elucidating the downstream pathway. N Biotechnol 32:710–715. https://doi.org/10.1016/j.nbt.2015.03.005
Tappe W, Herbst M, Hofmann D, Koeppchen S, Kummer S, Thiele B, Groeneweg J (2013) Degradation of sulfadiazine by Microbacterium lacus strain SDZm4, isolated from lysimeters previously manured with slurry from sulfadiazine-medicated pigs. Appl Environ Microbiol 79:2572–2577. https://doi.org/10.1128/AEM.03636-12
Zhang WW, Wen YY, Niu ZL, Yin K, Xu DX, Chen LX (2012) Isolation and characterization of sulfonamide-degrading bacteria Escherichia sp. HS21 and Acinetobacter sp. HS51. World J Microbiol Biotechnol 28:447–452. https://doi.org/10.1007/s11274-011-0834-z
Leng Y, Bao J, Chang G, Zheng H, Li X, Du J, Snow D, Li X (2016) Biotransformation of tetracycline by a novel bacterial strain Stenotrophomonas maltophilia DT1. J Hazard Mater 318:125–133. https://doi.org/10.1016/j.jhazmat.2016.06.053
Mulla SI, Hu A, Sun Q, Li J, Suanon F, Ashfaq M, Yu CP (2018) Biodegradation of sulfamethoxazole in bacteria from three different origins. J Environ Manage 206:93–102. https://doi.org/10.1016/j.jenvman.2017.10.029
Zhang W, Qiu L, Gong A, Yuan X (2017) Isolation and characterization of a high-efficiency erythromycin A-degrading Ochrobactrum sp. strain. Mar Pollut Bull 114:896–902. https://doi.org/10.1016/j.marpolbul.2016.10.076
Deng Y, Li B, Zhang T (2018) Bacteria that make a meal of sulfonamide antibiotics: blind spots and emerging opportunities. Environ Sci Technol 52:3854–3868. https://doi.org/10.1021/acs.est.7b06026
Hirth N, Topp E, Dörfler U, Stupperich E, Munch JC, Schroll R (2016) An effective bioremediation approach for enhanced microbial degradation of the veterinary antibiotic sulfamethazine in an agricultural soil. Chem Biol Technol Agric 3:29. https://doi.org/10.1186/s40538-016-0080-6
Maillard J-Y (2002) Bacterial target sites for biocide action. J Appl Microbiol 92(Suppl):16S–27S
Kim SA, Moon H, Lee K, Rhee MS (2015) Bactericidal effects of triclosan in soap both in vitro and in vivo. J Antimicrob Chemother 70:3345–3352. https://doi.org/10.1093/jac/dkv275
Halden RU, Lindeman AE, Aiello AE, Andrews D, Arnold WA, Fair P, Fuoco RE, Geer LA, Johnson PI, Lohmann R, McNeill K, Sacks VP, Schettler T, Weber R, Zoeller RT, Blum A (2017) The Florence statement on triclosan and triclocarban. Environ Health Perspect 125. https://doi.org/10.1289/EHP1788
Weatherly LM, Gosse JA (2017) Triclosan exposure, transformation, and human health effects. J Toxicol Environ Heal B Crit Rev 20:447–469. https://doi.org/10.1080/10937404.2017.1399306
Dann AB, Hontela A (2011) Triclosan: environmental exposure, toxicity and mechanisms of action. J Appl Toxicol 31:285–311. https://doi.org/10.1002/jat.1660
Heath RJ, Rubin JR, Holland DR, Zhang E, Snow ME, Rock CO (1999) Mechanism of triclosan inhibition of bacterial fatty acid synthesis. J Biol Chem 274:11110–11114. https://doi.org/10.1074/jbc.274.16.11110
Jones RD, Jampani HB, Newman JL, Lee AS (2000) Triclosan: a review of effectiveness and safety in health care settings. Am J Infect Control 28:184–196. https://doi.org/10.1016/s0196-6553(00)90027-0
McLeod R, Muench SP, Rafferty JB, Kyle DE, Mui EJ, Kirisits MJ, Mack DG, Roberts CW, Samuel BU, Lyons RE, Dorris M, Milhous WK, Rice DW (2001) Triclosan inhibits the growth of Plasmodium falciparum and Toxoplasma gondii by inhibition of apicomplexan Fab I. Int J Parasitol 31:109–113. https://doi.org/10.1016/s0020-7519(01)00111-4
Russell AD (2004) Whither triclosan? J Antimicrob Chemother 53:693–695. https://doi.org/10.1093/jac/dkh171
ECHA (European Chemicals Agency) (2015) Biocidal Products Committee (BPC) opinion on the application for approval of the active substance: triclosan product-type: 1 3:1–11
European Commission (2016) COMMISSION IMPLEMENTING DECISION (EU) 2016/110 of 27 January 2016 not approving triclosan as an existing active substance for use in biocidal products for product- type 1. Euratom 2001:20–30. http://eur-lex.europa.eu/pri/en/oj/dat/2003/l_285/l_28520031101en00330037.pdf
FDA (U.S. Food and Drug Administration) (2016) Safety and effectiveness of health care antiseptics; topical antimicrobial drug products for over-the-counter human use. Final rule, Federal register
Davis EF, Klosterhaus SL, Stapleton HM (2012) Measurement of flame retardants and triclosan in municipal sewage sludge and biosolids. Environ Int 40:1–7. https://doi.org/10.1016/j.envint.2011.11.008
Heidler J, Halden RU (2007) Mass balance assessment of triclosan removal during conventional sewage treatment. Chemosphere 66:362–369. https://doi.org/10.1016/j.chemosphere.2006.04.066
Ogunyoku TA, Young TM (2014) Removal of triclocarban and triclosan during municipal biosolid production. Water Environ Res 86:197–203. https://doi.org/10.2175/106143013x13807328849378
Chalew TEA, Halden RU (2009) Environmental exposure of aquatic and terrestrial biota to triclosan and triclocarban. J Am Water Resour Assoc 45:4–13. https://doi.org/10.1111/j.1752-1688.2008.00284.x
Halden RU, Paull DH (2005) Co-occurrence of triclocarban and triclosan in U.S. water resources. Environ Sci Technol 39:1420–1426. https://doi.org/10.1021/es049071e
Higgins CP, Paesani ZJ, Abbott Chalew TE, Halden RU, Hundal LS (2011) Persistence of triclocarban and triclosan in soils after land application of biosolids and bioaccumulation in Eisenia foetida. Environ Toxicol Chem 30:556–563. https://doi.org/10.1002/etc.416
Olaniyan LWB, Mkwetshana N, Okoh AI (2016) Triclosan in water, implications for human and environmental health. Springerplus 5:1–17. https://doi.org/10.1186/s40064-016-3287-x
Coogan MA, La Point TW (2008) Snail bioaccumulation of triclocarban, triclosan, and methyltriclosan in a North Texas, USA, stream affected by wastewater treatment plant runoff. Environ Toxicol Chem 27:1788–1793. https://doi.org/10.1897/07-374.1
Prosser RS, Lissemore L, Topp E, Sibley PK (2014) Bioaccumulation of triclosan and triclocarban in plants grown in soils amended with municipal dewatered biosolids. Environ Toxicol Chem 33:975–984. https://doi.org/10.1002/etc.2505
Dhillon GS, Kaur S, Pulicharla R, Brar SK, Cledón M, Verma M, Surampalli RY (2015) Triclosan: current status, occurrence, environmental risks and bioaccumulation potential. Int J Environ Res Public Health 12:5657–5684. https://doi.org/10.3390/ijerph120505657
Gillis JD, Price GW, Prasher S (2017) Lethal and sub-lethal effects of triclosan toxicity to the earthworm Eisenia fetida assessed through GC–MS metabolomics. J Hazard Mater 323:203–211. https://doi.org/10.1016/j.jhazmat.2016.07.022
Orvos DR, Versteeg DJ, Inauen J, Capdevielle M, Rothenstein A, Cunningham V (2002) Aquatic toxicity of triclosan. Environ Toxicol Chem 21:1338–1349
Tatarazako N, Ishibashi H, Teshima K, Kishi K, Arizono K (2004) Effects of triclosan on various aquatic organisms. Environ Sci 11:133–140
Wang F, Xu R, Zheng F, Liu H (2018) Effects of triclosan on acute toxicity, genetic toxicity and oxidative stress in goldfish (Carassius auratus). Exp Anim 67:219–227. https://doi.org/10.1538/expanim.17-0101
Wang X, Liu Z, Wang W, Yan Z, Zhang C, Wang W, Chen L (2014) Assessment of toxic effects of triclosan on the terrestrial snail (Achatina fulica). Chemosphere 108:225–230. https://doi.org/10.1016/j.chemosphere.2014.01.044
Yueh M-F, Tukey RH (2016) Triclosan: a widespread environmental toxicant with many biological effects. Annu Rev Pharmacol Toxicol 56:251–272. https://doi.org/10.1146/annurev-pharmtox-010715-103417
Zaltauskaite J, Miskelyte D (2018) Biochemical and life cycle effects of triclosan chronic toxicity to earthworm Eisenia fetida. Environ Sci Pollut Res 25:18938–18946. https://doi.org/10.1007/s11356-018-2065-4
Aryal N, Reinhold DM (2011) Phytoaccumulation of antimicrobials from biosolids: impacts on environmental fate and relevance to human exposure. Water Res 45:5545–5552. https://doi.org/10.1016/j.watres.2011.08.027
Mendez MO, Valdez EM, Martinez EM, Saucedo M, Wilson BA (2016) Fate of triclosan in irrigated soil: degradation in soil and translocation into onion and tomato. J Environ Qual 45:1029–1035. https://doi.org/10.2134/jeq2015.07.0386
Pannu MW, Toor GS, O’Connor GA, Wilson PC (2012) Toxicity and bioaccumulation of biosolids-borne triclosan in food crops. Environ Toxicol Chem 31:2130–2137. https://doi.org/10.1002/etc.1930
Cajthaml T, Křesinová Z, Svobodová K, Möder M (2009) Biodegradation of endocrine-disrupting compounds and suppression of estrogenic activity by ligninolytic fungi. Chemosphere 75:745–750. https://doi.org/10.1016/j.chemosphere.2009.01.034
Hundt K, Martin D, Hammer E, Jonas U, Kindermann MK, Schauer F (2000) Transformation of triclosan by Trametes versicolor and Pycnoporus cinnabarinus. Appl Environ Microbiol 66:4157–4160. https://doi.org/10.1128/aem.66.9.4157-4160.2000
Chen X, Zhuang J, Bester K (2018) Degradation of triclosan by environmental microbial consortia and by axenic cultures of microorganisms with concerns to wastewater treatment. Appl Microbiol Biotechnol 102:5403–5417. https://doi.org/10.1007/s00253-018-9029-y
Lee DG, Chu KH (2013) Effects of growth substrate on triclosan biodegradation potential of oxygenase-expressing bacteria. Chemosphere 93:1904–1911. https://doi.org/10.1016/j.chemosphere.2013.06.069
Lee DG, Zhao F, Rezenom YH, Russell DH, Chu KH (2012) Biodegradation of triclosan by a wastewater microorganism. Water Res 46:4226–4234. https://doi.org/10.1016/j.watres.2012.05.025
Lolas IB, Chen X, Bester K, Nielsen JL (2012) Identification of triclosan-degrading bacteria using stable isotope probing, fluorescence in situ hybridization and microautoradiography. Microbiol (United Kingdom) 158:2796–2804. https://doi.org/10.1099/mic.0.061077-0
Roh H, Subramanya N, Zhao F, Yu CP, Sandt J, Chu KH (2009) Biodegradation potential of wastewater micropollutants by ammonia-oxidizing bacteria. Chemosphere 77:1084–1089. https://doi.org/10.1016/j.chemosphere.2009.08.049
Forbes S, Dobson CB, Humphreys GJ, McBain AJ (2014) Transient and sustained bacterial adaptation following repeated sublethal exposure to microbicides and a novel human antimicrobial peptide. Antimicrob Agents Chemother 58:5809–5817. https://doi.org/10.1128/AAC.03364-14
Russell AD (2003) Biocide use and antibiotic resistance: the relevance of laboratory findings to clinical and environmental situations. Lancet Infect Dis 3:794–803. https://doi.org/10.1016/S1473-3099(03)00833-8
Mcmurry LM, Oethinger M, Levy SB (1998) Overexpression of marA, soxS , or acrAB produces resistance to triclosan in laboratory and clinical strains of Escherichia coli. FEMS Microbiol Lett 166:305–309. https://doi.org/10.1111/j.1574-6968.1998.tb13905.x
Russell AD (2000) Do biocides select for antibiotic resistance? J Pharm Pharmacol 52:227–233. https://doi.org/10.1211/0022357001773742
Braoudaki M, Hilton AC (2004) Low level of cross-resistance between triclosan and antibiotics in Escherichia coli K-12 and E. coli O55 compared to E. coli O157. FEMS Microbiol Lett 235:305–309. https://doi.org/10.1016/j.femsle.2004.04.049
Chuanchuen R, Beinlich K, Hoang TT, Becher A, Karkhoff-Schweizer RR, Schweizer HP (2001) Cross-resistance between triclosan and antibiotics in Pseudomonas aeruginosa is mediated by multidrug efflux pumps: exposure of a susceptible mutant strain to triclosan selects nfxB mutants overexpressing MexCD-OprJ. Antimicrob Agents Chemother 45:428–432. https://doi.org/10.1128/AAC.45.2.428-432.2001
Karatzas KAG, Webber MA, Jorgensen F, Woodward MJ, Piddock LJV, Humphrey TJ (2007) Prolonged treatment of Salmonella enterica serovar Typhimurium with commercial disinfectants selects for multiple antibiotic resistance, increased efflux and reduced invasiveness. J Antimicrob Chemother 60:947–955. https://doi.org/10.1093/jac/dkm314
Carey DE, McNamara PJ (2015) The impact of triclosan on the spread of antibiotic resistance in the environment. Front Microbiol 5:1–11. https://doi.org/10.3389/fmicb.2014.00780
Russell AD, Tattawasart U, Maillard JY, Furr JR (1998) Possible link between bacterial resistance and use of antibiotics and biocides [2]. Antimicrob Agents Chemother 42:2151. https://doi.org/10.1128/aac.42.8.2151
Schweizer HP (2001) Triclosan: a widely used biocide and its link to antibiotics. FEMS Microbiol Lett 202:1–7. https://doi.org/10.1111/j.1574-6968.2001.tb10772.x
Yazdankhah SP, Scheie AA, Høiby EA, Lunestad BT, Heir E, Fotland TØ, Naterstad K, Kruse H (2006) Triclosan and antimicrobial resistance in bacteria: an overview. Microb Drug Resist 12:83–90. https://doi.org/10.1089/mdr.2006.12.83
Waller NJ, Kookana RS (2009) Effect of triclosan on microbial activity in Australian soils. Environ Toxicol Chem 28:65. https://doi.org/10.1897/08-224.1
Park I, Zhang N, Ogunyoku TA, Young TM, Scow KM (2013) Effects of Triclosan and biosolids on microbial community composition in an agricultural soil. Water Environ Res 85:2237–2242. https://doi.org/10.2175/106143012x13560205144335
Ghannoum MA, Rice LB (1999) Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clin Microbiol Rev 12:501–517. https://doi.org/10.1128/cmr.12.4.501
Shalini K, Kumar N, Drabu S, Sharma PK (2011) Advances in synthetic approach to and antifungal activity of triazoles. Beilstein J Org Chem 7:668–677. https://doi.org/10.3762/bjoc.7.79
Fletcher RA, Gilley A, Sankhla N, Davis TD (2010) Triazoles as plant growth regulators and stress protectants. In: Horticultural reviews. Wiley, Oxford, pp 55–138. https://doi.org/10.1002/9780470650776.ch3
Hof H (2001) Critical annotations to the use of azole antifungals for plant protection. Antimicrob Agents Chemother 45:2987–2990. https://doi.org/10.1128/AAC.45.11.2987-2990.2001
Kishorekumar A, Jaleel CA, Manivannan P, Sankar B, Sridharan R, Panneerselvam R (2007) Comparative effects of different triazole compounds on growth, photosynthetic pigments and carbohydrate metabolism of Solenostemon rotundifolius. Colloids Surf B Biointerfaces 60:207–212. https://doi.org/10.1016/j.colsurfb.2007.06.008
Peyton LR, Gallagher S, Hashemzadeh M (2015) Triazole antifungals: a review. Drugs Today 51:705–718. https://doi.org/10.1358/dot.2015.51.12.2421058
Huang Q, Yu Y, Tang C, Peng X (2010) Determination of commonly used azole antifungals in various waters and sewage sludge using ultra-high performance liquid chromatography-tandem mass spectrometry. J Chromatogr A 1217:3481–3488. https://doi.org/10.1016/j.chroma.2010.03.022
Kahle M, Buerge IJ, Hauser A, Müller MD, Poiger T (2008) Azole fungicides: occurrence and fate in wastewater and surface waters. Environ Sci Technol 42:7193–7200. https://doi.org/10.1021/es8009309
Van De Steene JC, Stove CP, Lambert WE (2010) A field study on 8 pharmaceuticals and 1 pesticide in Belgium: removal rates in waste water treatment plants and occurrence in surface water. Sci Total Environ 408:3448–3453. https://doi.org/10.1016/j.scitotenv.2010.04.037
Wick A, Fink G, Ternes TA (2010) Comparison of electrospray ionization and atmospheric pressure chemical ionization for multi-residue analysis of biocides, UV-filters and benzothiazoles in aqueous matrices and activated sludge by liquid chromatography-tandem mass spectrometry. J Chromatogr A 1217:2088–2103. https://doi.org/10.1016/j.chroma.2010.01.079
Assress HA, Nyoni H, Mamba BB, Msagati TAM (2020) Occurrence and risk assessment of azole antifungal drugs in water and wastewater. Ecotoxicol Environ Saf 187:109868. https://doi.org/10.1016/j.ecoenv.2019.109868
Peng X, Huang Q, Zhang K, Yu Y, Wang Z, Wang C (2012) Distribution, behavior and fate of azole antifungals during mechanical, biological, and chemical treatments in sewage treatment plants in China. Sci Total Environ 426:311–317. https://doi.org/10.1016/j.scitotenv.2012.03.067
Stamatis N, Hela D, Konstantinou I (2010) Occurrence and removal of fungicides in municipal sewage treatment plant. J Hazard Mater 175:829–835. https://doi.org/10.1016/j.jhazmat.2009.10.084
Chen ZF, Ying GG (2015) Occurrence, fate and ecological risk of five typical azole fungicides as therapeutic and personal care products in the environment: a review. Environ Int 84:142–153. https://doi.org/10.1016/j.envint.2015.07.022
Chen ZF, Ying GG, Jiang YX, Yang B, Lai HJ, Liu YS, Pan CG, Peng FQ (2014) Photodegradation of the azole fungicide fluconazole in aqueous solution under UV-254: kinetics, mechanistic investigations and toxicity evaluation. Water Res 52:83–91. https://doi.org/10.1016/j.watres.2013.12.039
Chen ZF, Ying GG, Ma YB, Lai HJ, Chen F, Pan CG (2013) Typical azole biocides in biosolid-amended soils and plants following biosolid applications. J Agric Food Chem 61:6198–6206. https://doi.org/10.1021/jf4013949
Lindberg RH, Fick J, Tysklind M (2010) Screening of antimycotics in Swedish sewage treatment plants – waters and sludge. Water Res 44:649–657. https://doi.org/10.1016/j.watres.2009.10.034
Richmond EK, Rosi EJ, Walters DM, Fick J, Hamilton SK, Brodin T, Sundelin A, Grace MR (2018) A diverse suite of pharmaceuticals contaminates stream and riparian food webs. Nat Commun 9:1–9. https://doi.org/10.1038/s41467-018-06822-w
Rossmann J, Schubert S, Gurke R, Oertel R, Kirch W (2014) Simultaneous determination of most prescribed antibiotics in multiple urban wastewater by SPE-LC-MS/MS. J Chromatogr B Analyt Technol Biomed Life Sci 969:162–170. https://doi.org/10.1016/j.jchromb.2014.08.008
Álvarez-Martín A, Sánchez-Martín MJ, Pose-Juan E, Rodríguez-Cruz MS (2016) Effect of different rates of spent mushroom substrate on the dissipation and bioavailability of cymoxanil and tebuconazole in an agricultural soil. Sci Total Environ 550:495–503. https://doi.org/10.1016/j.scitotenv.2016.01.151
Badawi N, Rosenbom AE, Jensen AMD, Sørensen SR (2016) Degradation and sorption of the fungicide tebuconazole in soils from golf greens. Environ Pollut 219:368–378. https://doi.org/10.1016/j.envpol.2016.10.045
Bromilow RH, Evans AA, Nicholls PH (1999) Factors affecting degradation rates of five triazole fungicides in two soil types: 2 field studies. Pestic Sci 55:1135–1142. https://doi.org/10.1002/(SICI)1096-9063(199912)55:12<1135::AID-PS73>3.0.CO;2-1
El Azhari N, Dermou E, Barnard RL, Storck V, Tourna M, Beguet J, Karas PA, Lucini L, Rouard N, Botteri L, Ferrari F, Trevisan M, Karpouzas DG, Martin-Laurent F (2018) The dissipation and microbial ecotoxicity of tebuconazole and its transformation products in soil under standard laboratory and simulated winter conditions. Sci Total Environ 637–638:892–906. https://doi.org/10.1016/j.scitotenv.2018.05.088
Herrero-Hernández E, Andrades MS, Marín-Benito JM, Sánchez-Martín MJ, Rodríguez-Cruz MS (2011) Field-scale dissipation of tebuconazole in a vineyard soil amended with spent mushroom substrate and its potential environmental impact. Ecotoxicol Environ Saf 74:1480–1488. https://doi.org/10.1016/j.ecoenv.2011.04.023
Papadopoulou ES, Karas PA, Nikolaki S, Storck V, Ferrari F, Trevisan M, Tsiamis G, Martin-Laurent F, Karpouzas DG (2016) Dissipation and adsorption of isoproturon, tebuconazole, chlorpyrifos and their main transformation products under laboratory and field conditions. Sci Total Environ 569–570:86–96. https://doi.org/10.1016/j.scitotenv.2016.06.133
Potter TL, Strickland TC, Joo H, Culbreath AK (2005) Accelerated soil dissipation of tebuconazole following multiple applications to peanut. J Environ Qual 34:1205–1213. https://doi.org/10.2134/jeq2004.0473
Strickland TC, Potter TL, Joo H (2004) Tebuconazole dissipation and metabolism in Tifton loamy sand during laboratory incubation. Pest Manag Sci 60:703–709. https://doi.org/10.1002/ps.860
Buerge IJ, Poiger T, Müller MD, Buser HR (2006) Influence of pH on the stereoselective degradation of the fungicides epoxiconazole and cyproconazole in soils. Environ Sci Technol 40:5443–5450. https://doi.org/10.1021/es060817d
Kaziem AE, Gao B, Li L, Zhang Z, He Z, Wen Y, Wang MH (2020) Enantioselective bioactivity, toxicity, and degradation in different environmental mediums of chiral fungicide epoxiconazole. J Hazard Mater 386:121951. https://doi.org/10.1016/j.jhazmat.2019.121951
Kim IS, Beaudette LA, Han Shim J, Trevors JT, Tack Suh Y (2002) Environmental fate of the triazole fungicide propiconazole in a rice-paddy-soil lysimeter. Plant and Soil 239:321–331. https://doi.org/10.1023/A:1015000328350
Kim IS, Shim JH, Suh YT (2003) Laboratory studies on formation of bound residues and degradation of propiconazole in soils. Pest Manag Sci 59:324–330. https://doi.org/10.1002/ps.642
Thorstensen CW, Lode O (2001) Laboratory degradation studies of bentazone, dichlorprop, MCPA, and propiconazole in Norwegian soils. J Environ Qual 30:947–953. https://doi.org/10.2134/jeq2001.303947x
White PM, Potter TL, Culbreath AK (2010) Fungicide dissipation and impact on metolachlor aerobic soil degradation and soil microbial dynamics. Sci Total Environ 408:1393–1402. https://doi.org/10.1016/j.scitotenv.2009.11.012
Storck V, Lucini L, Mamy L, Ferrari F, Papadopoulou ES, Nikolaki S, Karas PA, Servien R, Karpouzas DG, Trevisan M, Benoit P, Martin-Laurent F (2016) Identification and characterization of tebuconazole transformation products in soil by combining suspect screening and molecular typology. Environ Pollut 208:537–545. https://doi.org/10.1016/j.envpol.2015.10.027
Satapute P, Kaliwal B (2016) Biodegradation of propiconazole by newly isolated Burkholderia sp. strain BBK_9. 3 Biotech 6:110. https://doi.org/10.1007/s13205-016-0429-3
Satapute P, Kaliwal B (2016) Biodegradation of the fungicide propiconazole by Pseudomonas aeruginosa PS-4 strain isolated from a paddy soil. Ann Microbiol 66:1355–1365. https://doi.org/10.1007/s13213-016-1222-6
Kryczyk-Poprawa A, Żmudzki P, Maślanka A, Piotrowska J, Opoka W, Muszyńska B (2019) Mycoremediation of azole antifungal agents using in vitro cultures of Lentinula edodes. 3 Biotech 9:207. https://doi.org/10.1007/s13205-019-1733-5
Ammar GA, Tryono R, Dol̈l K, Karlovsky P, Deising HB, Wirsel SGR (2013) Identification of ABC transporter genes of Fusarium graminearum with roles in azole tolerance and/or virulence. PLoS One 8:1–13. https://doi.org/10.1371/journal.pone.0079042
Lelièvre L, Groh M, Angebault C, Maherault AC, Didier E, Bougnoux ME (2013) Azole resistant Aspergillus fumigatus: an emerging problem. Med Mal Infect 43:139–145. https://doi.org/10.1016/j.medmal.2013.02.010
Ma Z, Michailides TJ (2005) Advances in understanding molecular mechanisms of fungicide resistance and molecular detection of resistant genotypes in phytopathogenic fungi. Crop Prot 24:853–863. https://doi.org/10.1016/j.cropro.2005.01.011
Alastruey-Izquierdo A, Cuenca-Estrella M, Monzón A, Mellado E, Rodríguez-Tudela JL (2008) Antifungal susceptibility profile of clinical Fusarium spp. isolates identified by molecular methods. J Antimicrob Chemother 61:805–809. https://doi.org/10.1093/jac/dkn022
Buil JB, Hare RK, Zwaan BJ, Arendrup MC, Melchers WJG, Verweij PE (2019) The fading boundaries between patient and environmental routes of triazole resistance selection in Aspergillus fumigatus. PLoS Pathog 15:e1007858. https://doi.org/10.1371/journal.ppat.1007858
Chowdhary A, Kathuria S, Agarwal K, Sachdeva N, Singh PK, Jain S, Meis JF (2014) Voriconazole-resistant penicillium oxalicum: an emerging pathogen in immunocompromised hosts. Open Forum Infect Dis 1:1–7. https://doi.org/10.1093/ofid/ofu029
Pasqualotto AC, Thiele KO, Goldani LZ (2010) Novel triazole antifungal drugs: focus on isavuconazole, ravuconazole and albaconazole. Curr Opin Investig Drugs 11:164–174
Pfaller MA, Diekema DJ (2004) Rare and emerging opportunistic fungal pathogens: concern for resistance beyond Candida albicans and Aspergillus fumigatus. J Clin Microbiol 42:4419–4431. https://doi.org/10.1128/JCM.42.10.4419-4431.2004
Whaley SG, Berkow EL, Rybak JM, Nishimoto AT, Barker KS, Rogers PD (2017) Azole antifungal resistance in Candida albicans and emerging non-albicans Candida Species. Front Microbiol 7. https://doi.org/10.3389/fmicb.2016.02173
Verweij PE, Chowdhary A, Melchers WJG, Meis JF (2016) Azole resistance in aspergillus fumigatus: can we retain the clinical use of mold-active antifungal azoles? Clin Infect Dis 62:362–368. https://doi.org/10.1093/cid/civ885
Ribas e Ribas AD, Spolti P, Del Ponte EM, Donato KZ, Schrekker H, Fuentefria AM (2016) Is the emergence of fungal resistance to medical triazoles related to their use in the agroecosystems? A mini review. Braz J Microbiol 47:793–799. https://doi.org/10.1016/j.bjm.2016.06.006
Snelders E, Camps SMT, Karawajczyk A, Schaftenaar G, Kema GHJ, van der Lee HA, Klaassen CH, Melchers WJG, Verweij PE (2012) Triazole fungicides can induce cross-resistance to medical triazoles in aspergillus fumigatus. PLoS One 7:e31801. https://doi.org/10.1371/journal.pone.0031801
Verweij PE, Kema GHJ, Zwaan B, Melchers WJ (2013) Triazole fungicides and the selection of resistance to medical triazoles in the opportunistic mould Aspergillus fumigatus. Pest Manag Sci 69:165–170. https://doi.org/10.1002/ps.3390
Araújo GRDS, De Souza W, Frases S (2017) The hidden pathogenic potential of environmental fungi. Future Microbiol 12:1533–1540. https://doi.org/10.2217/fmb-2017-0124
Denham ST, Wambaugh MA, Brown JCS (2019) How environmental fungi cause a range of clinical outcomes in susceptible hosts. J Mol Biol 431:2982–3009. https://doi.org/10.1016/j.jmb.2019.05.003
O’Quinn RP, Hoffmann JL, Boyd AS (2001) Colletotrichum species as emerging opportunistic fungal pathogens: a report of 3 cases of phaeohyphomycosis and review. J Am Acad Dermatol 45:56–61. https://doi.org/10.1067/mjd.2000.113691
Shivaprakash MR, Appannanavar SB, Dhaliwal M, Gupta A, Gupta S, Gupta A, Chakrabarti A (2011) Colletotrichum truncatum: an unusual pathogen causing mycotic keratitis and endophthalmitis. J Clin Microbiol 49:2894–2898. https://doi.org/10.1128/JCM.00151-11
Tsitsopoulou A, Posso R, Vale L, Bebb S, Johnson E, White PL (2018) Determination of the prevalence of triazole resistance in environmental Aspergillus fumigatus strains isolated in South Wales, UK. Front Microbiol 9:1–8. https://doi.org/10.3389/fmicb.2018.01395
Satapute P, Kamble MV, Adhikari SS, Jogaiah S (2019) Influence of triazole pesticides on tillage soil microbial populations and metabolic changes. Sci Total Environ 651:2334–2344. https://doi.org/10.1016/j.scitotenv.2018.10.099
Ramudu AC, Mohiddin GJ, Srinivasulu M, Madakka M, Rangaswamy V (2011) Impact of fungicides chlorothalonil and propiconazole on microbial activities in groundnut (Arachis hypogaea L.) soils. ISRN Microbiol 2011:623404. https://doi.org/10.5402/2011/623404
Yen JH, Chang JS, Huang PJ, Wang YS (2009) Effects of fungicides triadimefon and propiconazole on soil bacterial communities. J Environ Sci Heal B Pestic Food Contam Agric Wastes 44:681–689. https://doi.org/10.1080/03601230903163715
Sułowicz S, Cycoń M, Piotrowska-Seget Z (2016) Non-target impact of fungicide tetraconazole on microbial communities in soils with different agricultural management. Ecotoxicology 25:1047–1060. https://doi.org/10.1007/s10646-016-1661-7
Anuradha B, Rekhapadmini A, Rangaswamy V (2016) Influence of tebuconazole and copper hydroxide on phosphatase and urease activities in red sandy loam and black clay soils. 3 Biotech 6:1–8. https://doi.org/10.1007/s13205-016-0367-0
Bending GD, Rodríguez-Cruz MS, Lincoln SD (2007) Fungicide impacts on microbial communities in soils with contrasting management histories. Chemosphere 69:82–88. https://doi.org/10.1016/j.chemosphere.2007.04.042
Cycoń M, Piotrowska-Seget Z, Kaczyńska A, Kozdrój J (2006) Microbiological characteristics of a sandy loam soil exposed to tebuconazole and λ-cyhalothrin under laboratory conditions. Ecotoxicology 15:639–646. https://doi.org/10.1007/s10646-006-0099-8
Ferreira EPDB, Dusi AN, Costa JR, Xavier GR, Rumjanek NG (2009) Assessing insecticide and fungicide effects on the culturable soil bacterial community by analyses of variance of their DGGE fingerprinting data. Eur J Soil Biol 45:466–472. https://doi.org/10.1016/j.ejsobi.2009.07.003
Karas PA, Baguelin C, Pertile G, Papadopoulou ES, Nikolaki S, Storck V, Ferrari F, Trevisan M, Ferrarini A, Fornasier F, Vasileiadis S, Tsiamis G, Martin-Laurent F, Karpouzas DG (2018) Assessment of the impact of three pesticides on microbial dynamics and functions in a lab-to-field experimental approach. Sci Total Environ 637–638:636–646. https://doi.org/10.1016/j.scitotenv.2018.05.073
Muñoz-Leoz B, Ruiz-Romera E, Antigüedad I, Garbisu C (2011) Tebuconazole application decreases soil microbial biomass and activity. Soil Biol Biochem 43:2176–2183. https://doi.org/10.1016/j.soilbio.2011.07.001
Storck V, Nikolaki S, Perruchon C, Chabanis C, Sacchi A, Pertile G, Baguelin C, Karas PA, Spor A, Devers-Lamrani M, Papadopoulou ES, Sibourg O, Malandain C, Trevisan M, Ferrari F, Karpouzas DG, Tsiamis G, Martin-Laurent F (2018) Lab to field assessment of the ecotoxicological impact of chlorpyrifos, isoproturon, or tebuconazole on the diversity and composition of the soil bacterial community. Front Microbiol 9:1412. https://doi.org/10.3389/fmicb.2018.01412
Wang C, Wang F, Zhang Q, Liang W (2016) Individual and combined effects of tebuconazole and carbendazim on soil microbial activity. Eur J Soil Biol 72:6–13. https://doi.org/10.1016/j.ejsobi.2015.12.005
Richter E, Wick A, Ternes TA, Coors A (2013) Ecotoxicity of climbazole, a fungicide contained in antidandruff shampoo. Environ Toxicol Chem 32:2816–2825. https://doi.org/10.1002/etc.2367
Van-Camp L, Bujarrabal B, Anna Rita G, Jones RJA, Montanarella L, Olazabal C, Selvaradjou S-K (2004) Reports of the technical working groups established under the thematic strategy for soil protection. Office Publications of the European Communities, Luxembourg. EUR 21319 EN/4, 872 p
Kümmerer K (2009) The presence of pharmaceuticals in the environment due to human use – present knowledge and future challenges. J Environ Manage 90:2354–2366. https://doi.org/10.1016/j.jenvman.2009.01.023
Acknowledgments
We would like to thank Damia Barcelo, Sandra Prez, and Serge Chiron for having and inviting us to participate to the project AWARE within the ERA-NET WATERWORKS 2015–2016 (contract no. ANR-16-WTW5-0011-05). Sara Gallego-Blanco was supported by this European Project. Fabrice Martin-Laurent was also supported by the ANTIBIOTOX project (contract no. ANR-17-CE34-0003).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2020 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Gallego, S., Martin-Laurent, F. (2020). Impact of PhACs on Soil Microorganisms. In: Pérez Solsona, S., Montemurro, N., Chiron, S., Barceló, D. (eds) Interaction and Fate of Pharmaceuticals in Soil-Crop Systems. The Handbook of Environmental Chemistry, vol 103. Springer, Cham. https://doi.org/10.1007/698_2020_616
Download citation
DOI: https://doi.org/10.1007/698_2020_616
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-61289-4
Online ISBN: 978-3-030-61290-0
eBook Packages: Chemistry and Materials ScienceChemistry and Material Science (R0)