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Article

Co-Application of Sewage Sludge, Chinese Medicinal Herbal Residue and Biochar Attenuated Accumulation and Translocation of Antibiotics in Soils and Crops

by
Min Pan
1,*,
Shing Him Lee
2,
Liwen Luo
3,
Xun Wen Chen
4 and
Yik Tung Sham
5
1
Department of Applied Science, School of Science and Technology, Hong Kong Metropolitan University, Hong Kong SAR, China
2
Department of Social Sciences, Education University of Hong Kong, Hong Kong SAR, China
3
Institute of Bioresource and Agriculture, Department of Biology, Hong Kong Baptist University, Hong Kong SAR, China
4
Guangdong Provincial Research Centre for Environment Pollution Control and Remediation Materials, Department of Ecology, College of Life Science and Technology, Jinan University, Guangzhou 510632, China
5
Department of Construction and Quality Management, School of Science and Technology, Hong Kong Metropolitan University, Hong Kong SAR, China
*
Author to whom correspondence should be addressed.
Sustainability 2023, 15(8), 6972; https://doi.org/10.3390/su15086972
Submission received: 31 March 2023 / Revised: 18 April 2023 / Accepted: 18 April 2023 / Published: 21 April 2023
(This article belongs to the Special Issue Advances in Ecosystem Services and Urban Sustainability)
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Abstract

:
Sewage sludge (SL), Chinese medicinal herbal residues (CMHRs) and the raw materials of biochar (BC) are normally treated as wastes. However, SL, CMHRs and BC are potential candidates for soil amendments. The performances of soils amended with three different proportions (5%, 10% and 20% on a dry-weight basis) of SL-BC and SL-CMHR-BC in terms of ameliorating soil properties and attenuating antibiotics in soil–plant systems were investigated with two common crop species: carrot and lettuce. The amended soils in general showed higher nutrient levels than the control soils, and particularly for the 20% SL-CMHR-BC. The soils with 10% or 20% SL-BC or SL-CMHR-BC apparently retarded the germination performances of the two crop species, but the negative effects were not noticeable after a growing period. Six target antibiotics, amoxicillin (AMX), tetracycline (TC), sulfamethazine (SMX), norfloxacin (NOR), erythromycin (ERY) and chloramphenicol (CAP), were applied for growing the crops by using irrigation water with 3 μg L−1 (IW3) and 30 μg L−1 (IW30) of each antibiotic. The amended soils led to lower levels of antibiotics in the soils and crop tissues as compared with the control, with the 20% SL-CMHR-BC soils showing the most pronounced effect. The effects of the soil amendments on the bioconcentration factor (BCF) varied, but generally with lower values in the amended soils. Both SL-BC and SL-CMHR-BC were proven in the study as potential soil amendments for alleviating the environmental dispersal and human exposure risks of different antibiotics, and specifically 20% SL-CMHR-BC.

1. Introduction

Rapid urbanisation and industrialisation have led to the increased generation of different types of waste and, hence, have induced enormous challenges for waste management all over the world. To reduce the pressure of landfills, transforming waste into useful resources has been a favourable alternative option for waste management. The conversion of solid waste into soil amendments is one example. Biochar (BC) and sewage sludge (SL) are two rather representative examples of waste-derived soil amendments, and their individual effects on soils and plants have been widely studied. BC is usually derived from waste materials with high carbon contents through pyrolysis. While the properties of BC vary with the raw materials and process methods, in principle, using it as a soil amendment improves soil fertility through the addition and retention of nutrients, as well as through the promotion of soil microbial activity, and enhances the water-holding capacity of soils [1,2,3]. SL is the by-product of wastewater treatment. The generation of SL is continuously increasing due to population growth and the demand for water quality. To utilise SL as a soil amendment, it should be treated through various methods, such as aerobic and anaerobic digestion, composting, stabilisation and thermal drying, to minimise the pathogen level [4,5]. The processed products are commonly known as “biosolids”. On the one hand, SL may have high contents of toxic metals and therefore the soil application of it can pose environmental and health risks. On the other hand, it is a valuable nutrient source due to its high contents of organic matter and inorganic nutrients, such as phosphorus, nitrogen and microelements [6]. It is well documented that applying SL to soils improves their physical, chemical and biological properties [7]. In recent years, some studies have started to evaluate the co-application of BC and SL as soil amendments and have shown promising results. It is suggested that the high adsorption capacity of BC can reduce the bioavailability and mobility of polycyclic aromatic hydrocarbons and potentially toxic elements, such as heavy metals in soils. Accordingly, the incorporation of BC with SL alleviates the negative properties of SL [8,9,10,11,12]. Alternatively, SL has a good effect on soil nutrient enrichment [13]. The addition of BC was found to enhance the nutrient retention of SL-amended soils [10]. It has been seen that the co-application of BC and SL provides a complementary effect. Chinese medicinal herbal residues (CMHRs) are a great contributor to solid waste in China. They have been receiving increasing yet still limited attention for their potential application in improving soil properties [14]. Approximately 70 million tons of Chinese medicinal plants are consumed annually in China, and the dregs are usually handled as wastes [15]. CMHRs are nutrient-rich [16] and contain phytochemicals that provide excellent antipathogenic properties [17]. These properties suggest the substantial potential of CMHRs as organic fertilisers to improve soils and plant growth. It has been proposed that CMHRs are a good substitute for manure due to their lower potential to cause heavy-metal pollution [18].
The respective properties of SL, BC and CMHRs hint at the potential benefits of their co-application. In addition to the modification of soil properties, the capacity to alleviate antibiotic contamination in terrestrial environments is another important aspect to be considered. Antibiotics have been widely adopted for decades as livestock and human medicines for their prevention of bacterial infections and diseases [19]. They are bioactive compounds that can enter the environment in the form of parent compounds or metabolites through discharged excreta, urine, wastewater and pharmaceutical wastes, such as amoxicillin and tetracycline [20,21]. Wastewater irrigation is one major cause of the dissemination of antibiotics in soil–plant systems [22]. Once antibiotics are spiked into soils, they persist in the fields [23] and are absorbed by crops. The antibiotics are bioaccumulated and ultimately consumed by humans or other organisms. Their widespread use is therefore a noteworthy problem for agricultural soils today.
The application of SL is associated with the risk of transferring antibiotics to the soil environment [24,25]. Bair et al. [26] applied walnut shell biochar to biosolid-amended soil and identified the positive effects on reducing the plant uptake of antibiotics. Meanwhile, the effectiveness of BC at reducing the concentrations of antibiotics in both soils and plants has been proven in various studies [27,28,29]. Yet, the performance of the co-application of SL and BC in attenuating antibiotics in soil–plant systems is still scarcely studied. While the effects of CMHR-derived biochar as a potential sorbent of antibiotics in soils have been investigated in some previous studies [30,31], there is no known information on the effects of the co-application of SL, CMHRs and BC on antibiotics.
Accordingly, this study aimed at addressing the abovementioned current knowledge gaps. It could contribute to the understanding of the application potential of two types of soil amendments, SL-BC and SL-CHMR-BC, as well as their efficacies at reducing the risk of the dispersal of antibiotics in soils. Carrot (Daucus carota) and lettuce (Lactuca sativa) were the two crops used in the study, and six types of antibiotics from different classes were involved. The two specific objectives of the study were as follows: (1) to appraise the physicochemical properties of SL-BC and SL-CMHR-BC-amended soils; (2) to assess the inhibitory effect of the two types of soil amendments on the antibiotic bioavailability in soils and crops, as well as their bioaccumulation and translocation in different crops.

2. Materials and Methods

2.1. Preparation of Soil Amendments and Soil Mixture

Two types of soil amendments (SL-BC and SL-CMHR-BC) were collected from a secondary sewage treatment works in Hong Kong, the Stanley Sewage Treatment Works. The SL was biologically and chemically stabilised through aerobic fermentation and drying in a solar dryer, and the detailed process can be referred to in Pan et al. [32]. The CMHR was collected from a local company that produces herbal teas (Herbaceous Teas Co., Ltd., Hong Kong). It was then oven-dried at 105 °C for 24 h in the laboratory. The BC (8–20 mesh, CAS No. 7440-44-0), which was ready for application, was obtained from Sigma-Aldrich (Merck Ltd., Taipei, Taiwan). It was immersed in river water to enable the growth of a thin layer of microbes. Ionic water was used to remove the impurities. It was later dried at 105 °C and heated to 600 °C for 2 h. The SL-BC and SL-CMHR-BC were prepared by mixing the different materials in ratios of 1:1 and 1:1:1 on a dry-weight basis, respectively. The different soil treatments were prepared by mixing the soil matrix with 5%, 10% and 20% SL-BC and 5%, 10% and 20% SL-CMHR-BC on a dry-weight basis. Therefore, there were a total of six different treatments of soil amendments. The soil matrix was sandy loam soil made up of 80.4% sand, 15.4% silt and 6.2% clay, imitating the soil conditions in Hong Kong [33]. A control soil without the addition of any soil amendments was included in the experiment.

2.2. Seed Germination Test

The seed germination test was carried out according to the OECD procedures [34]. The seed germination of the two target crop species, carrot and lettuce, was conducted. Twenty seeds were placed on 20 g of moist soil with different treatments in Petri dishes (90 × 20 mm). The Petri dishes were covered with lids and kept in an incubator (JSPC-300C, growth chamber). The environment of the incubator was maintained at 25 ± 0.5 °C and 80% humidity, and in total darkness. Water loss in Petri dishes was monitored every day by weighing, and distilled water was added when necessary. A seed was counted as germinated when the radicle was over 2.0 mm in length. The percentage of seed germination, as well as the root and shoot lengths, were measured after 7 days of incubation. There were five replicates for each treatment.

2.3. Planting Experiment

2.3.1. Greenhouse Plantation

The plantation method followed the method in [35]. Carrot (Daucus carota L.) and lettuce (Lactuca sativa) are crop species across Asia and Southeast Asia. Therefore, they were selected for the study, and the crop seeds were purchased from Brighten Floriculture, a local urban farmland in Hong Kong. The seeds were planted in pots with antibiotic-free soils. After seed emergence, they were transplanted into individual pots with 3–4 kg of antibiotic-free soil, with three replicates for each group. The pots were irrigated with 200 mL of wastewater with two initial antibiotic concentrations (see Section 2.3.2 below): 3 μg L−1 (IW3) and 30 μg L−1 (IW30). The two concentrations were in the range of the commonly detected concentrations of target antibiotics in surface water [36,37]. The planting medium was maintained at 25 ± 2 °C and a 70% water-holding capacity throughout the experiment period.

2.3.2. Selection of Antibiotics

Amoxicillin (AMX), tetracycline (TC), sulfamethazine (SMX), norfloxacin (NOR), erythromycin (ERY) and chloramphenicol (CAP) were selected as the target antibiotics in the study. They are commonly used in human therapy and animal husbandry [38]. These antibiotics are representatives from different antibiotic classes, having varying physicochemical properties (Table 1). Because these antibiotics are commonly featured in medicinal use in both the human body and livestock, they were chosen for this study.

2.3.3. Measurement of Soil Properties

The soil properties of the amended soils, including the pH value, conductivity, water-holding capacity, total organic carbon (TOC), total N, P and K and available N, P, K, Ca, Mg and Na, were measured before and after the planting experiment. The measurement method followed Pan et al. [32,46]. They were determined according to methods of the American Society for Testing and Materials (ASTM) [47,48,49]. The soil pH was measured with a pH meter. The maximum water-holding capacity was determined according to the guidelines of the International Organization for Standardization [50]. The TOC was measured with a TOC analyser (Shimadzu, Japan). The available forms and total forms of the nutrients were extracted and analysed by atomic absorption spectroscopy (AAS) and continuous fluid analysis (CFA).

2.3.4. Determination of Antibiotic Concentrations in Soil–Plant Systems

All soils and crop tissues, including the roots and leaves/shoots, were sampled after the crops reached the optimum marketable size (90 days for lettuce and 120 days for carrot). The antibiotic concentrations of the samples were analysed. The extraction and determination methods for soil samples and leaching water were modified from our previous study [51].
For the soil samples, the internal standards of each target antibiotic were spiked in 1 g of freeze-dried sample (1 mg L−1). Extraction buffer (acetonitrile and 0.2 M citric acid, v:v = 1:1, pH 4.4) was added to the samples. The samples were then vortex-mixed, extracted using ultrasonication and centrifuged. The combined supernatant was evaporated to near dryness. Solid-phase extraction (SPE) was used for the extraction. Methanol and Milli-Q water were used for preconditioning in Oasis HLB cartridges (Waters, Milford, MA, USA). Methanol was then used to elute the target analytes from the cartridges. The analytes were concentrated under a gentle nitrogen stream and redissolved in methanol. Finally, the extract was filtered into an amber glass vial and stored at −18 °C. For the crop samples, internal standards (1 mg L−1) were added to the samples before extraction for the antibiotic concentration calculation. Crop tissues were extracted three times with a mixed solution of acidified acetonitrile and acetone, and the other extraction and purification steps were similar to those for the soil samples. The extracts of the samples of soils and crop tissues were analysed by HPLC–MS/MS (Agilent Liquid Chromatography 1100 series HPLC system coupled to an Agilent 6410 triple quadrupole MS) equipped with an electrospray ionisation (ESI) source (Agilent, Santa Clara, CA, USA) in multiple-reaction monitoring (MRM) mode. The chromatographic column was a Waters BEH T3 (2.1 × 100 mm, 1.7 µm) column with a Poroshell 120 pre-column filter (3.0 mm, 0.2 mm). For ESI+, 5 mM acetic acid and 0.1% formic acid were used as mobile phase A, and 5 mM acetic acid and acetonitrile were used as mobile phase B. Gradient conditions were set as follows: 0 min, 20% B; 4.5 min, 35% B; 5 min, 60% B; 10 min, 70% B; 11 min, 100% B; 13.1 min, 20% B. The recoveries of the target compounds were 73–126% and 79–114%, respectively. The limits of quantification (LOQs) of the target compounds were 0.70–4.63 mg kg−1 for soils and 0.25–2.64 mg kg−1 for crop tissues. To calculate the calibration curves (r2 > 0.999), ten concentrations (0.5–500 mg L−1) were used for each antibiotic.
The calculation of the relative quantities of antibiotics in the leaching water, soils and crop tissues followed our previous study [51]. The bioconcentration factor (BCF) is the ratio of the antibiotic concentration in the root (BCFroot) or leaf/shoot (BCFleaf/shoot) to that in the soil. It is a measure of the tendency of a compound to accumulate in the root or leaf/shoot with respect to the soil environment.

2.4. Statistical Analysis

A one-way ANOVA test followed by Dunnett’s post hoc test was conducted for the data to compare the properties and effects of the amended soils with those of the control soils. The data were analysed using R, and p < 0.05 was considered a significant difference.

3. Results and Discussion

3.1. Effects of Soil Amendments on Soil Properties

The varying physiochemical properties of the control and different amended soils are shown in Table S1. Before the plantation experiment, all types of the amended soils generally had higher values for all the measured soil physicochemical properties as compared with the control soils, especially at a higher proportion of soil amendments, including the total and available N, P and K. At the same proportion of soil amendments, the SL-CMHR-BC led to higher increments of the total and available nutrients than the SL-BC. After the plantation experiment, the concentrations of the available nutrients decreased. The 20% SL-CMHR-BC soils showed the highest absolute reduction in available N, as compared with the other treatments. In general, the amended soils usually still had higher levels of available and total nutrients than the control soils after the plantation experiment. Moreover, the SL-CMHR-BC soils generally showed higher total N, P and K than the same proportion of SL-BC soils, particularly at the proportion of 20% (199–207 vs. 104–168 g kg−1 for N; 201–308 vs. 95–251 g kg−1 for P; 240–439 vs. 157–200 g kg−1 for K). Moreover, the contents of total nutrients were usually positively associated with the increased proportions of the soil amendments. For the available nutrients, the trend was less obvious.
The results show that the soil amendments had significant effects on the nutrient enrichment, particularly for the 20% SL-CMHR-BC. Both SL and CHMRs are promising for enhancing soil nutrients, as supported by previous studies [7,18], while BC can reduce the leaching of available nutrients in soils [52]. In addition, both SL-BC and SL-CMHR-BC soils have better effects on nutrient addition than chicken manure and food waste compost, according to our previous data (Table S2). The strong effect of SL-CMHR-BC matched with the findings of Ma et al. [16]: CMHRs have a significant effect on improving soil nutrients. Therefore, SL-BC and SL-CMHR-BC should be comparable or even superior nutrient sources for soils compared with some organic fertilisers in terms of the quantitative provision of nutrients.

3.2. Effects of Soil Amendments on Seed Germination

The seed germination percentages of the carrot and lettuce in all the different groups of amended soils (84–89%) were only slightly lower than those of the control soils (92–96%) (Table S3). Both the 5% SL-BC and SL-CMHR-BC promoted or were not detrimental to the root and shoot growth of both species. Alternatively, 10% or 20% of either type of soil amendment resulted in a decrease in the elongation of shoots (10%: 13.3–22.6% reduction; 20%: 26.7–50.9% reduction) and roots (10%: 4.6–10.6% reduction; 20%: 13.8–34.3% reduction) as compared with the control soils, except for the 10% SL-CMHR-BC on the shoot elongation of lettuce. The inhibition effect was stronger for a higher proportion of soil amendments, while it was comparable between the SL-BC and SL-CMHR-BC. The seed germination performance of the lettuce was more adversely affected by the soil amendments than the carrot overall.
High doses of individual applications of SL, CMHRs and BC have been associated with a reduction in the promotion effects or even net-negative effects on germination or plant growth in some previous studies [5,16,53]. However, the final sizes of both the carrot and lettuce were not significantly affected by the soil amendments by visual observation. This suggested that the suppression effects of the soil amendments on crop growth were limited to the early stage. For example, it has been proposed that the phytotoxic effects of SL may be temporary and could disappear in the long term [54]. Moreover, it has been proposed that antibiotics could inhibit the shoot and root elongation of crops at the germination stage [45]. Therefore, the reduction effect of soil amendments on antibiotic concentrations (see Section 3.3 below) may counteract the effect of the inhibition on germination by the soil amendments themselves.

3.3. Effects of Soil Amendments on Antibiotic Dissipation in Soils

Overall, NOR (140.2–1592.4 ng g−1) showed the highest concentration in the soils, followed by ERY (40.3–791.8 ng g−1) and TC (24.4–529.7 ng g−1). Their high concentrations matched with the findings of Cycoń et al. [55]. They concluded that the antibiotic classes fluoroquinolones, macrolides and tetracyclines were characterised by high DT50 or half-life values. In our previous study with a similar experimental design, TC was found to be the most abundant antibiotic in the soils, followed by NOR and CAP [35]. The differences can be attributed to the difference in soil texture, as clay loam was used in the previous study, and TC is strongly adsorbed by clay [56]. While it has been suggested that NOR had a high degradation rate in soils [45], the accumulation of NOR due to regular irrigation may slow down its degradation [57]. All the antibiotics had higher concentrations in the IW30 soils, but to different extents. The TC and ERY in the IW30 treatments were around 10-fold of those of the IW3 treatments, followed by from 4- to 8-fold for the CAP and NOR, and less than 3-fold for the AMX and SMZ.
Overall, both the SL-BC and SL-CMHR-BC soils had detectable and significantly lower concentrations of all the studied antibiotics compared with the control soils after the plantation experiment (Figure 1). Higher proportions of SL-BC or SL-CMHR-BC led to increased reductions in the antibiotic concentrations in the soils. Moreover, the SL-CMHR-BC had a stronger attenuation effect on the antibiotics than the SL-BC at the same proportion. In other words, the 20% SL-CMHR-BC soils showed the best performance in antibiotic dissipation in the soils. For example, the percentage decreases in the antibiotic concentrations for the IW30 carrot soils as compared with the control soils were 7.7–28.8% for 5% SL-BC, 8.2–35.1% for 10% SL-BC, and 9.7–38.8% for 20% SL-BC, and 18.8–37.4% for 5% SL-CMHR-BC, 26.1–43.0% for 10% SL-CMHR-BC, and 32.7–48.8% for 20% SL-CMHR-BC. A similar trend was found under the IW3 treatments, but the degree of reduction was smaller. For example, the percentage decreases in the antibiotic concentrations for the IW3 carrot soils as compared with the control soils were 11.3–15.8% for 5% SL-BC, 15.7–24.6% for 10% SL-BC, and 26.3–32.9% for 20% SL-BC, and 21.8–28.8% for 5% SL-CMHR-BC, 29.2–32.1% for 10% SL-CMHR-BC, and 34.1–47.5% for 20% SL-CMHR-BC.
Antibiotics are lost from soils three main ways: leaching, degradation and plant absorption. As antibiotics were not detected in the leachate in this study, the observed decreases in the antibiotic concentrations in the soils can be attributed to increases in degradation and/or plant absorption. BC has been proven to promote the dissipation of antibiotics in soils [27,58]. This is because BC provides living space and nutrients for the colonisation of bacteria, and hence, facilitates the degradation of antibiotics [59]. Besides promoting the biotic degradation of antibiotics, it has also been suggested that BC is able to enhance their abiotic dissipation, which is possibly a result of the irreversible binding of antibiotics with BC [60].
Further, the stronger antibiotic attenuation effects of the SL-CMHR-BC soils than the SL-BC soils in the results was probably due to the differences in the soil properties. The nutrient test demonstrated that a higher proportion of soil amendments and SL-CMHR-BC provided more nutrients to the soil environment. This, in turn, produced a more favourable environment for the growth of the soil microorganisms and consequently promoted the biotic degradation of the antibiotics.

3.4. Effect of Soil Amendments on Antibiotic Dissipation in Plant Tissues

As a whole, NOR (1.63–41.1 ng g−1) and CAP (0.78–24.7 ng g−1) had the highest concentrations in the root tissues, followed by TC (0.6–18.3 ng g−1) and ERY (0.5–17.0 ng g−1). NOR was the most abundant antibiotic in the carrot root tissues of both the IW3 and IW30 soils, as well as in the lettuce of the IW30 soils. CAP had the highest concentration in the root tissues of the lettuce of the IW3 soils among the six antibiotics. AMX and SMZ had very low concentrations (<2.1 ng g−1) or even undetectable amounts in the root tissues. For the leaf/shoot tissues, NOR (5.0–76.0 ng g−1) showed the highest concentration, followed by TC (1.1–21.8 ng g−1) and then CAP (0.7–9.25 ng g−1). AMX, ERY and SMZ showed rather low (<3.6 ng g−1) or even undetectable concentrations. The concentrations of the different types of antibiotics in the root tissues and leaf/shoot tissues of the IW30 soils were higher than those in the IW3 soils.
Similar to the effects on soils, the addition of the soil amendments significantly reduced the antibiotic concentrations in the plant tissues in general. Higher proportions of the soil amendments led to more prominent effects in the reduction. Moreover, the SL-CMHR-BC soils showed a better performance than the SL-BC soils in attenuating antibiotics in the plant tissues (Figure 2 and Figure 3). For instance, the NOR concentrations in the root and leaf/shoot tissues of the IW30 SL-CMHR-BC carrot soils were 24.0% and 23.1% lower for the 5% SL-CMHR-BC, respectively, 31.8% and 29.9% lower for the 10% SL-CMHR-BC, respectively, and 45.5% and 53.9% lower for the 20% SL-CMHR-BC, respectively, as compared with the control soils. Meanwhile, the NOR concentrations in the root and leaf/shoot tissues of the IW30 SL-BC carrot soils were 12.1% and 13.4% lower for the 5% SL-BC soils, respectively, 28.9% and 17.6% lower for the 10% SL-BC soils, respectively, and 31.9% and 19.1% lower for the 20% SL-BC soils, respectively, as compared with the control soils. Within the same treatment group, the degree of antibiotic reduction was similar between the antibiotics with relatively higher concentrations (i.e., CAP, TC and NOR). For instance, the reductions in the concentrations of CAP, TC and NOR in the carrot root tissues of the IW30 SL-CHMR-BC soils were 23.3–25.0% for the 5% SL-CHMR-BC, 27.9–31.8% for the 10% SL-CHMR-BC and 45.5–56.1% for the 20% SL-CHMR-BC. Similarly, the concentrations of CAP, TC and NOR in the carrot leaf/shoot tissues of the IW30 SL-CHMR-BC soils were reduced by 21.0–24.1% for the 5% SL-CHMR-BC, 29.9–33.7% for the 10% SL-CHMR-BC and 49.3–54.4% for the 20% SL-CHMR-BC.
The overall amount of antibiotics in plant tissues is affected by the absorption from soils and the metabolism in plants. Meanwhile, the relative allocation of antibiotics in the aboveground and belowground parts is mainly determined by the translocation behaviours. The generally high concentrations of NOR and low/undetectable concentrations of SMZ and ERY across the different plant tissues accorded with the findings of Pan and Chu [35]. The high retention rate of NOR in the soils was likely one main contributing factor to the high concentration of this antibiotic in the plant tissues. The physiochemical properties of the antibiotics also affect their potential to be absorbed by plants and cause accumulation in plant tissues [61].
Based on the data, the dose–response effect may be one main reason for the variation in the reductions in the antibiotic concentrations in the plant tissues by the presence of different concentrations and types of soil amendments. The exposure amount has been found to be positively linked with the plant uptake amount [62,63]. A lower concentration in soils means a lower availability of antibiotics for absorption. The higher concentrations of antibiotics in the plant tissues for the IW30 soils than the IW3 soils also support that the concentrations of antibiotics in soils are positively related to those in plant tissues. Therefore, the greater degradation of antibiotics in soils, as promoted by the addition of soil amendments, and particularly at a high proportion (20%) of SL-CMHR-BC, can accordingly lead to lower concentrations of antibiotics in plant tissues.

3.5. Effects of Soil Amendments on Bioconcentration Factors of Antibiotics

The BCFs of the antibiotics in the roots (BCFroot) (Figure 4) and leaves/shoots (BCFleaf/shoot) (Figure 5) varied a lot among the different antibiotics. TC had the highest BCFleaf/shoot among the antibiotics across all treatments (0.04–0.10), and CAP had the highest BCFroot (0.03–0.13). The variations were expectable due to the variations in the physio-chemical properties of the different antibiotics. For example, the high lipophilicity of CAP, as reflected by its relatively high log Kow, may favour its accumulation in the roots as the partition to root lipids [64]. The BCFleaf/shoot is affected by the translocation potential of the antibiotics from roots to leaves/shoots. All the studied antibiotics had BCFroot values less than 0.15 and BCFleaf/shoot values less than 0.11 in this study, which were rather low as compared with our previous field study, in which the BCFroot of TC was as high as 0.3, and the BCFleaf/shoot of CAP reached 0.6. Some possible causes include the differences in the soil amendments and antibiotic degradation between the studies.
Regarding the effects of the different soil amendments, a consistent observation was that the 20% SL-CMHR-BC usually resulted in a significantly lower BCF for plant tissues as compared with the control soils. There were also some other noteworthy results. The BCFleaf/shoot of CAP for the carrots of the IW3 20% SL-BC soils was significantly lower than that of the control soils. The BCFleaf/shoot values of the AMX, ERY, CAP and TC for the carrots of the IW30 20% SL-BC soils were all significantly lower than those of the control soils. The BCFleaf/shoot values of TC and NOR for the lettuce were higher for the control soils compared with the IW3 5% and 10% SL-CMHR-BC soils. Similarly, the BCFleaf/shoot values of CAP, TC and NOR for the lettuce were higher for the control soils compared with those of the IW30 5% and 10% SL-CMHR-BC soils. Regarding the BCFroot, the 10% and 20% SL-BC both led to lower BCFroot values of AMX and SMZ for the carrots of the IW3 soils compared with the control soils. The IW30 10% and 20% SL-BC soils, in general, led to significantly lower BCFroot values of CAP, AMX and NOR for the carrot, while the IW3 10% and 20% SL-BC soils led to lower BCFroot values of ERY, TC and NOR for the lettuce. For the IW30 soils, higher BCFroot values of AMX and CAP were found for both crops of soils with the 5% and 10% soil amendments, except for CAP in the 10% SL-BC soils.
One main reason for the lower antibiotic concentrations in the plant tissues of the amended soils was the attenuated antibiotic concentrations in the soils, as discussed above. However, the observed significant variations in the BCFs suggest that some additional factors (e.g., the translocation factor in plants) contributed to the final concentrations of antibiotics in the plant tissues. Meanwhile, the soil amendments altered the soil physicochemical properties that play a substantial role in altering the soil adsorption capacity and plant availability [20]. The above complex and counteracting factors caused by the soil amendments led to the BCF variation. Nevertheless, despite the varying BCF, there was an overall decrease in the antibiotic bioaccumulation in the plant tissues.

3.6. Implications of Co-Application of SL, CMHRs and BC as Soil Amendment

The lower retention rates of antibiotics in soils implies a reduction in the dispersal risk of antibiotics in the terrestrial environment. Meanwhile, the lower amounts of antibiotics accumulated in edible plant tissues, such as the roots of carrot and the leaves/shoots of lettuce, mean a lower risk of human exposure to antibiotics. The addition of either SL-BC or SL-CMHR-BC is therefore promising for reducing the environmental dispersal risk and human exposure risk of antibiotics, according to the results. At the same time, the studied soil amendments can also improve the soil properties, especially the soil nutrients. This further demonstrates the prospect of SL-BC and SL-CMHR-BC for soil application. Particularly, the effects of a 20% SL-CMHR-BC application are predicted to be most notable. Moreover, it is expected that CMHRs can offer antipathogenic properties [17], which further suggests the advantages of SL-CMHR-BC over SL-BC. The positive results of the inclusion of CMHRs supports the more extensive use of these waste materials in soil application. The potential of the co-application of SL, CHMRs and BC to agricultural soils should be further explored with different crop species and soil textures. In this study, the ratio of SL, CMHR and BC was 1:1:1 on a dry-weight basis; the effects of different ratios can be evaluated in the future. Such soil amendments could be listed among the currently identified methods related to the recycling of waste materials in the promotion of sustainable agriculture and soil management [65].

4. Conclusions

The findings in this study prove the substantial potential of the co-application of SL, CMHRs and BC in soils. The positive impacts include nutrient enrichment and alleviating the risks of antibiotics. Both SL-BC and SL-CMHR-BC significantly improved the soil nutrient contents. Although high proportions of the soil amendments had negative effects on the seed germination, the influences were not noticeable in the long term. In addition, SL-BC and SL-CMHR-BC both resulted in significant overall reductions in the antibiotic concentrations in the soil–plant systems for the six studied antibiotics from a range of antibiotic classes and with a range of physiochemical properties under soil environments with either high or low levels of antibiotic contamination. A higher proportion of soil amendments and SL-CMHR-BC led to more pronounced reductions than a lower proportion of soil amendments and SL-BC. In other words, 20% SL-CMHR-BC was the best formulation for minimizing the risk of antibiotics. The effects of the soil amendments on the BCF values of the antibiotics were less consistent and more complex. These were due to the counteracting effects that resulted from the changes in the concentrations of the antibiotics in the soil environment and plant tissues, and the modified soil physiochemical properties as caused by the soil amendments. Nevertheless, the studied soil amendments brought overall reductions in the antibiotic concentrations in the soil–plant systems. The attenuation of the antibiotic concentrations in the soils was probably the main contributor to the resultant net reduction in the antibiotic amounts in the plant tissues. As a whole, the incorporation of CMHR and SL-BC further enhanced the antibiotic attenuation effects in the soils and crop tissues, probably by bringing more significant improvements to the soil nutrient contents and microorganism activities. These findings provide valuable guidance for repurposing SL-CMHR-BC in arable lands, with 20% SL-CMHR-BC as an effective application rate.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/su15086972/s1, Table S1: The soil physiochemical properties of the control and six soil treatments before and after growing the two crop species (carrot and lettuce) with irrigation of wastewater with 3 μg/L (IW3) and 30 μg/L (IW30) antibiotics (n = 3).; Table S2: Initial nutrient content of soils amended with chicken manure and food waste compost and in different proportions.; Table S3: Effects of different proportions of BC-SL and BC-CMHR-SL on the germination of carrot and lettuce.

Author Contributions

Conceptualisation, M.P.; methodology, M.P.; validation, M.P., S.H.L. and L.L.; formal analysis, M.P., S.H.L. and Y.T.S.; investigation, M.P.; resources, M.P.; data curation, M.P.; writing—original draft preparation, M.P., S.H.L. and Y.T.S.; writing—review and editing, M.P. and X.W.C.; visualisation, L.L. and Y.T.S.; supervision, M.P.; project administration, M.P.; funding acquisition, M.P. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Research Grants Council of Hong Kong, grant numbers UGC/FDS25(16)/M02/19 and UGC/FDS25(16)/M01/20, and by a Hong Kong Metropolitan University research grant (No. RD/2022/2.4).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The datasets used during the current study are available from the corresponding author upon reasonable request.

Conflicts of Interest

The authors declare no conflict of interest.

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Sustainability 15 06972 g001 550
Figure 1. Mean concentrations of target antibiotics in carrot and lettuce soils with irrigation of wastewater with 3 ug L−1 (IW3) and 30 ug L−1 (IW30) antibiotics. * indicates significance at p < 0.05 compared with the controls. Error bars represent the standard deviation (n = 3).
Figure 1. Mean concentrations of target antibiotics in carrot and lettuce soils with irrigation of wastewater with 3 ug L−1 (IW3) and 30 ug L−1 (IW30) antibiotics. * indicates significance at p < 0.05 compared with the controls. Error bars represent the standard deviation (n = 3).
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Sustainability 15 06972 g002 550
Figure 2. Mean concentrations of target antibiotics in roots of carrot and lettuce with irrigation of wastewater with 3 μg L−1 (IW3) and 30 μg L−1 (IW30) antibiotics. * indicates significance at p < 0.05 compared with the controls. Error bars represent the standard deviation of all data (n = 3).
Figure 2. Mean concentrations of target antibiotics in roots of carrot and lettuce with irrigation of wastewater with 3 μg L−1 (IW3) and 30 μg L−1 (IW30) antibiotics. * indicates significance at p < 0.05 compared with the controls. Error bars represent the standard deviation of all data (n = 3).
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Sustainability 15 06972 g003 550
Figure 3. Mean concentrations of target antibiotics in leaves/shoots of carrot and lettuce with irrigation of wastewater with 3 μg L−1 (IW3) and 30 μg L−1 (IW30) antibiotics. * indicates significance at p < 0.05 compared with the controls. Error bars represent the standard deviation of all data (n = 3).
Figure 3. Mean concentrations of target antibiotics in leaves/shoots of carrot and lettuce with irrigation of wastewater with 3 μg L−1 (IW3) and 30 μg L−1 (IW30) antibiotics. * indicates significance at p < 0.05 compared with the controls. Error bars represent the standard deviation of all data (n = 3).
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Sustainability 15 06972 g004 550
Figure 4. Mean bioconcentration factors of antibiotics of roots (BCFroot) of carrot and lettuce with irrigation of wastewater with 3 ug L−1 (IW3) and 30 ug L−1 (IW30) antibiotics. * indicates significance at p < 0.05 compared with the controls. Error bars represent the standard deviation of all data (n = 3).
Figure 4. Mean bioconcentration factors of antibiotics of roots (BCFroot) of carrot and lettuce with irrigation of wastewater with 3 ug L−1 (IW3) and 30 ug L−1 (IW30) antibiotics. * indicates significance at p < 0.05 compared with the controls. Error bars represent the standard deviation of all data (n = 3).
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Sustainability 15 06972 g005 550
Figure 5. Mean bioconcentration factors of antibiotics of leaves/shoots (BCFleaf/shoot) of carrot and lettuce with irrigation of wastewater with 3 ug L−1 (IW3) and 30 ug L−1 (IW30) antibiotics. * indicates significance at p < 0.05 compared with the controls. Error bars represent the standard deviation of all data (n = 3).
Figure 5. Mean bioconcentration factors of antibiotics of leaves/shoots (BCFleaf/shoot) of carrot and lettuce with irrigation of wastewater with 3 ug L−1 (IW3) and 30 ug L−1 (IW30) antibiotics. * indicates significance at p < 0.05 compared with the controls. Error bars represent the standard deviation of all data (n = 3).
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Table
Table 1. Physicochemical properties of the six target antibiotics used in this study.
Table 1. Physicochemical properties of the six target antibiotics used in this study.
Compound/ClassMolecular FormulaStructureMolecular WeightpKaLog Kow [23,39]Koc (L kg−1) [23,39]
Amoxicillin (AMX)/
β-lactam		C16H19N3O5SSustainability 15 06972 i001365.403.2; 7.43 [40]0.87108
Tetracycline (TC)/
Tetracyclines		C22H24N2O8Sustainability 15 06972 i002444.433.3;
7.7;
9.6 [41]		−1.31.37 × 105
Sulfamethazine (SMZ)/
Sulphonamides		C12H14N4O2SSustainability 15 06972 i003278.332.79;
7.45 [42]		0.76165
Norfloxacin (NOR)/
Quinolones		C16H18FN3O3Sustainability 15 06972 i004319.333.11; 6.1; 8.6 [43]−1.037.48 × 104
Erythromycin (ERY)/
Macrolides		C37H67NO13Sustainability 15 06972 i005733.938.88;
12.91 [44]		Not
available		1.63 × 104
Chloramphenicol (CAP)/
Chloramphenicol		C11H12Cl2N2O5Sustainability 15 06972 i006323.135.5 [43]; 9.61 [45]0.92128
Kow: octanol/water partition coefficient; Koc: soil adsorption coefficient.
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Pan, M.; Lee, S.H.; Luo, L.; Chen, X.W.; Sham, Y.T. Co-Application of Sewage Sludge, Chinese Medicinal Herbal Residue and Biochar Attenuated Accumulation and Translocation of Antibiotics in Soils and Crops. Sustainability 2023, 15, 6972. https://doi.org/10.3390/su15086972

AMA Style

Pan M, Lee SH, Luo L, Chen XW, Sham YT. Co-Application of Sewage Sludge, Chinese Medicinal Herbal Residue and Biochar Attenuated Accumulation and Translocation of Antibiotics in Soils and Crops. Sustainability. 2023; 15(8):6972. https://doi.org/10.3390/su15086972

Chicago/Turabian Style

Pan, Min, Shing Him Lee, Liwen Luo, Xun Wen Chen, and Yik Tung Sham. 2023. "Co-Application of Sewage Sludge, Chinese Medicinal Herbal Residue and Biochar Attenuated Accumulation and Translocation of Antibiotics in Soils and Crops" Sustainability 15, no. 8: 6972. https://doi.org/10.3390/su15086972

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