Ball milled biochar effectively removes sulfamethoxazole and sulfapyridine antibiotics from water and wastewater

Environmental Pollution 258 (2020) 113809

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Ball milled biochar effectively removes sulfamethoxazole and sulfapyridine antibiotics from water and wastewater* Jinsheng Huang a, Andrew R. Zimmerman b, Hao Chen c, Bin Gao a, * a

Department of Agricultural and Biological Engineering, University of Florida, Gainesville, FL, 32611, USA Department of Geological Sciences, University of Florida, Gainesville, FL, USA c Department of Agriculture, University of Arkansas at Pine Bluff, Pine Bluff, AR, 71601, USA b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 29 September 2019 Received in revised form 12 December 2019 Accepted 13 December 2019 Available online xxx

Release of antibiotics into the environment, which often occurs downstream of wastewater treatment plants, poses a human health threat due to the potential development of bacterial antibiotic resistance. In this study, laboratory experiments were conducted to evaluate the performance of ball milled biochar on the removal of two sulfonamide antibiotics, sulfamethoxazole (SMX) and sulfapyridine (SPY) from water and wastewater. Aqueous batch sorption experiment using both pristine and ball milled biochar derived from bagasse (BG), bamboo (BB) and hickory chips (HC), made at three pyrolysis temperatures (300, 450, 600
C), showed that ball milling greatly enhanced the SMX and SPY adsorption. The 450
C ball milled HC biochar and BB biochar exhibited the best removal efficiency for SMX (83.3%) and SPY (89.6%), respectively. A range of functional groups were produced by ball milling, leading to the conclusion that the adsorption of sulfonamides on the biochars was controlled by multiple mechanisms including hydrophobic interaction, pep interaction, hydrogen bonding, and electrostatic interaction. Due to the importance of electrostatic interaction, SMX and SPY adsorption was pH dependent. In laboratory water solutions, the Langmuir maximum adsorption capacities of SMX and SPY reached 100.3 mg/g and 57.9 mg/g, respectively. When tested in real wastewater solution, the 450
C ball milled biochar still performed well, especially in the removal of SPY. The maximum adsorption capacities of SMX and SPY in wastewater were 25.7 mg/g and 58.6 mg/g, respectively. Thus, ball milled biochar has great potential for SMX and SPY removal from aqueous solutions including wastewater. © 2019 Elsevier Ltd. All rights reserved.

Keywords: Ball mill Biochar Adsorption Wastewater treatment Sulfonamide antibiotics

1. Introduction Antibiotics are widely used in the prevention of infectious diseases in humans and animals (Inyang et al., 2015; Yao et al., 2018). However, they may enter the environment during manufacture and through wastewater treatment plant and aqua farming discharges (Ahmed et al., 2015; Tian et al., 2013). As a consequence, bacterial communities may undergo selection pressures, leading to rapid antibiotic resistance development, and posing an unprecedented health risk (Larsson, 2014). The major types of antibiotics include fluoroquinolones, chloramphenicols, tetracylines, and sulfonamides. Within the latter group, sulfamethoxazole (SMX) and sulfapyridine (SPY) are

* This paper has been recommended for acceptance by Charles Wong. * Corresponding author. E-mail address: bg55@ufl.edu (B. Gao).

https://doi.org/10.1016/j.envpol.2019.113809 0269-7491/© 2019 Elsevier Ltd. All rights reserved.

commonly used for disease treatment in humans and added to animal feed (Ahmed et al., 2015; Chen et al., 2015). However, if used or disposed of improperly, they can pose threats such as carcinogen risk (Shao et al., 2005), ecological bioaccumulation in aquatic organisms (Peiris et al., 2017), and skin allergic reactions (ChoquetKastylevsky et al., 2002). Making matters worse, sulfonamide antibiotics are only weakly degraded in the environment so can be widely dispersed via leaching into soil, groundwater and surface water. Common environmental sources of sulfonamides include reclaimed water irrigation and antibiotic-treated animal excretion (Tian et al., 2013; Yao et al., 2012). Thus, it would be of great benefit to develop novel methods to remove antibiotics especially sulfonamides efficiently from wastewater. Among existing technologies to remove antibiotics from water, including adsorption (Moussavi et al., 2013), reverse osmosis n et al., 2008) (Kosutic et al., 2007), photocatalytic oxidation (Beltra and ion exchange (Wang et al., 2017b), adsorption has been regarded as one of the most convenient, affordable and

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environment-friendly methods. It is even acknowledged by the U.S. Environmental Protection Agency (USEPA) as a favored method with respect to activated carbon adsorption (Fayazi et al., 2015; Lyu et al., 2018b). Biochar is one of the most commonly used low-cost sorbents for removing many types of contaminants from aqueous solutions (Tan et al., 2015). It has several advantages in terms of cost, performance, and sustainability over other typical sorbents such as activated carbon (Rivera-Utrilla et al., 2009), clay minerals (Gao and Pedersen, 2005), humic acid and manure (Kahle and Stamm, 2007), and graphene oxide (Gao et al., 2012). Biochar is a solid carbon material made by heating animal or plant biomass under oxygen-limited atmosphere (Brown, 2012). Its high specific surface area and porosity, and abundance and diversity of surface functional groups, aid in removal of contaminants from aqueous solution (Tan et al., 2015). To better its sorption capacity, scientists have engineered biochar by forming composites with nanoscale zerovalent iron (Wang et al., 2017a), MgO (Zhang et al., 2012), or nanotubes (Inyang et al., 2014), and treatments with steam (Rajapaksha et al., 2015), carbon dioxide (Xiong et al., 2013), acid (Xue et al., 2012), or anaerobic digestion (Inyang et al., 2010). However, most methods are either expensive in operation or harmful in by-product pollution and little attention has been raised in regards to avoiding those disadvantages (Lyu et al., 2018a). Unlike many chemical modification methods, ball milling is an environmentally friendly and cost-effective approach and has been widely employed in industry, especially in nanomaterials composite production (Lyu et al., 2018b). It reduces particles to nanoscale sizes mechanically, with low energy expenditure, and increases the specific surface area and oxygen-containing functional group abundance on the surfaces and edges of particles (Richard et al., 2016; Xing et al., 2013). Previous research has investigated the influences of ball mill on graphene sheets (Wang et al., 2016) and activated carbon (Ramanujan et al., 2007) to adsorb uranium and for biomedical applications, respectively. Ball milling is reported to boost the ability of biochar to sorb organic dye such as methylene blue (Lyu et al., 2018b) and synthetic musk fragrance such as galaxolide (Zhang et al., 2019). Additionally, ball milled magnetic biochar was shown to effectively sorb the pharmaceuticals carbamazepine and tetracycline (Shan et al., 2016). However, to date, the sorption of a sulfonamide by ball milled biochar has not been quantified, and no studies have examined the removal of any organic contaminants from real wastewater solutions by ball milled biochar. The overarching goal of this work is to evaluate ball milled biochar as a low-cost adsorbent of sulfonamides in water and wastewater. Nine types of biochars, derived from three types of biomass, at three pyrolysis temperatures were ball milled. Batch sorption experiments were carried out to determine the adsorption behaviors of ball milled biochars to two representative sulfonamides (SMX and SPY) in laboratory-prepared water and real wastewater solutions. 2. Materials and methods 2.1. Materials Raw bamboo (BB) and bagasse (BG) were obtained locally in Florida and hickory chips (HC) were purchased from Cowboy Charcoal Company (Stockton, CA). BB, BG, and HC are commonly used as feedstock for biochar production and some of the biochars have been applied to remove sulfonamides in aqueous solutions (Inyang et al., 2015; Yao et al., 2012). Each biomass was air-dried and milled into 0.5e1 mm particles prior to biochar production. The antibiotics, SMX and SPY, were purchase from Sigma-Aldrich

(St. Louis, MO, USA) and Acros Organics (Geel, Belgium), respectively. The physicochemical properties of these compounds are shown in Supporting Information (Table S1). Stock solution of SMX (100 mg/L) and SPY (50 mg/L), and their diluted working solutions, were made with deionized (DI) water (Thermo Scientific Barnstead Nanopure), sonicated and stored at 4
C in the dark. All other chemicals were of analytical grade. Secondary treated wastewater samples were collected from the wastewater treatment plant of University of Florida. They were filtered through 0.45 mm membrane filters (GE cellulose nylon) and stored at 4
C in a dark environment prior to use. The major components in the wastewater, measured previously (Zheng et al., 2019), can be found in Supporting Information (Table S2). 2.2. Preparation of adsorbents Biochar production method was based on a previous study (Sun et al., 2014). In brief, the 80
C oven-dried BG, BB, and HC were pyrolyzed at three different temperatures (300, 450, and 600
C) for 1.5 h in a N2-filled tubular furnace (Olympic, 1823HE). The obtained biochar samples were labeled according to their biomass and pyrolysis temperature (e.g. HC300 for hickory wood at 300
C). To obtain the ball milled samples, 1.8 g of each biochar was added into a 500 mL agate jar with 180 g of grinding balls (diameter ¼ 6 mm and mass ratio of ball/biochar ¼ 100:1). The jars were then placed in a planetary ball mill (PQ-N2, Across International products, NJ, USA), which was operated at 300 rpm for 12 h with a rotation direction change every 3 h. The ball milled biochars were labeled with the addition of a ‘BM’ prefix. 2.3. Sorbent characterization The surface organic functional groups of biochar and ball milled biochar were analyzed by the Fourier transform infrared spectroscopy (FTIR, Bruker Tensor 27, USA). The zeta potentials of ball milled biochars were measured using a Zetasizer Nano analyzer (Malvern Instrument Inc., UK). 2.4. Adsorption of SMX and SPY in laboratory solutions Initial assessment of the sorbents was conducted at room temperature (25 ± 0.5
C) by adding 10 mg of pristine or ball milled biochars into 10 mg/L solutions of SMX or SPY, made by dilution of DI water, in 50 mL conical centrifuge vessels (Thermo Scientific Nunc). In order to explore and compare the full sorption ability of the biochar samples, the concentrations of SMX and SPY used this work were way higher than their naturally occurring concentrations. The vessels were agitated on a mechanical shaker at 250 rpm for 24 h (predetermined sorption equilibrium). Samples were collected using sterile syringes (Fisher Scientific Inc., USA) and then filtered through 0.22 mm nylon membrane filters (GE cellulose) immediately. The concentrations of aqueous phase SMX and SPY were measured on a UVeVis spectrophotometer (EVO-60, Thermo Fisher Scientific) at a wavelength of 260 nm. Similar treatments, but without the sorbent, were used as controls. The removal efficiency and capacity of SMX/SPY were determined according to the difference between its initial and final aqueous concentrations. Adsorption kinetics were determined for the biochars that showed the highest sorption capacity (BM-HC450 for SMX and BMBB450 for SPY), using the experimental conditions described above, but retrieving samples at different time intervals (0.17, 0.5, 1, 2, 4, 8, 12, 16 and 24 h). Replicate vessels were sacrificially sampled and analyzed for aqueous sulfonamide concentration. Adsorption isotherm were determined for the same two biochars (BM-HC450 for SMX and BM-BB450 for SPY) by adding biochars of different

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dosages (5e70 mg for BM-HC450 and 3e30 mg for BM-BB450) into 10 mg/L solutions of SMX or SPY. The effect of pH on removal efficiency was determined for the same two biochar using the experimental conditions described above, except pH was adjusted to five different pH values (3.5, 5, 6.5, 7.5 and 8.5) with additions of HCl (0.1 N) or NaOH (0.1 N) solution. Ball milled biochar was added to vessels after stable pH values were reached and pH values monitored before and after the sorption experiment, exhibited little difference (<5%). 2.5. Adsorption of SMX and SPY in real wastewater To simulate SMX and SPY pollution in wastewater, the collected wastewater samples were spiked with stock solutions of SMX (100 mg/L) or SPY (50 mg/L) to obtain a final concentration of 10 mg/L prior to use. The adsorption isotherm and kinetics of SMX and SPY in real wastewater were obtained using the methods mentioned described above in section 2.4. All the experiments were performed in triplicate and the mean values and standard deviation are reported. Further experiments were implemented if two measurements showed a difference greater than 5%. The potential degradation of the two sulfonamides was ignored in this study (Yao et al., 2018). The equations used in modeling the kinetic and isotherm data are given in the supporting information accompanying this manuscript. 3. Results and discussion 3.1. Initial assessment and potential adsorption mechanisms All the ball milled biochars exhibited excellent removal efficiencies of SMX from 33.4% to 83.3% and SPY from 39.8% to 89.6% while un-milled biochars showed almost no sorption of the two sulfonamide antibiotics (Fig. 1). Thus, ball milling greatly enhanced SMX and SPY adsorption. This may be due to the increase of either surface functional groups or to specific surface area (Table S3) on biochar upon ball milling, or both (Lyu et al., 2018b). Previous studies have demonstrated that high pyrolysis temperature can increase surface area of biochar and thus may enhance the sorption capacity by promoting the hydrophobic interaction and the pep interaction between sulfonamides and carbon surfaces (Peiris et al., 2017; Yao et al., 2012). However, in this study, whereas sulfonamide sorption was much always much greater for the ball milled samples, surface area was, in many cases, only slightly greater (Table S3). Further, there was no significant correlation between sulfonamide sorption and surface area for ball milled biochars (Fig. S1). In addition, the surface area values of BM-HC450 and BMBB450, which displayed the greatest sorption of SMX (83.3%) and SPY (89.6%), respectively, were high and ranked the second and third among all the samples in surface area. All of this suggests that other mechanisms in addition to the hydrophobic and pep interactions may also contribute to the high sulfonamide sorption onto ball milled biochars. FTIR spectra (Fig. 2), show that, for both HC and BB, ball milling significantly increased surface functional groups, particularly at wavelengths indicating eCH2 (2920 cm1), aromatic C]O/C]C (1696 and 1597 cm1), and eCO (1262 cm1), but not aromatic CeH (at 882, 820 and 762 cm1) groups (Chen et al., 2008). Most of these are oxygen-containing functional groups, thus would have affinity for polar potions of SMX and SPY to form hydrogen bonds (Zheng et al., 2013), which could enhance the adsorption of the sulfonamides on BM-HC450 and BM-BB450. Electrostatic interactions between the sulfonamides and biochar surface could also affect the adsorption process (Chen et al., 2015; Peiris et al., 2017). As shown in Fig. 3, the surfaces of both BM-

Fig. 1. Removal efficiency of (a) SMX and (b) SPY from water by different sorbents.

BB450 and BM-HC450 were negatively charged at all pH values tested (3.5e8.5). Meanwhile, SMX (pKa of 1.8 and 5.6, Table S1) would occur as both neutral and anionic species (Tian et al., 2013; Zheng et al., 2013) at the experimental pH of around 6 in this study. Thus, there were electrostatic repulsions between SMX and biochar surface, which would inhibit the adsorption (Rajapaksha et al., 2015; Rajapaksha et al., 2014). Further experiments of the pH effect confirmed the importance of electrostatic interactions to sulfonamide adsorption on ball milled biochars. As shown in Fig. 4, the removal efficiencies of SMX and SPY (pKa of 2.3 and 8.4, Table S1) remained almost unchanged when the pH increased from 3.5 to 5 and 6.5, respectively. At these pH values, the main species of SMX and SPY are neutral, and thus there was no electrostatic interactions between the sulfonamides and the biochar adsorbents. Further increase of solution pH increased the anionic species of the sulfonamides and triggered electrostatic repulsion. As a result, it reduced the removal efficiencies of the sulfonamides, especially SMX, which showed no removal at pH of 8.5.

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Fig. 4. Removal efficiency of SMX by BM-HC450 and SPY by BM-BB450 as a function of pH.

Fig. 2. FTIR spectra of (a) HC450 and BM-HC450 and (b) BB450 and BM-BB450.

3.2. Adsorption kinetics and isotherms of sulfonamides in water In DI water, SMX adsorption onto BM-HC450 showed a gradual increasing process and reached equilibrium within 8e12 h (Fig. 5a). About 75% of SMX was removed within 8 h. Similarly, around 80% of

Fig. 5. Adsorption Kinetics (a) and isotherms (b) of SMX adsorption onto BM-HC450 (open circles) and SPY adsorption onto BM-BB450 (open triangles) in water. Symbols are experimental data and lines are model results. Fig. 3. Zeta potential of BM-HC450 and BM-BB450 at different pH conditions.

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SPY was removed within 8 h, by BM-BB450 and reached equilibrium within 12 h (Fig. 5a). Three kinetic models including the pseudo-first-order (PFO), the pseudo-second-order (PSO), and the Elovich models (described in S1 of supporting information) were applied to simulate the SMX and SPY adsorption onto the ball milled biochars. For both SMX and SPY, the Elovich model closely described the experimental data (Table 1, R2 > 0.96), but not the PSO and PFO models. These results confirm that the adsorption of sulfonamides onto the ball milled biochar was controlled by multiple mechanisms. The Langmuir and Freundlich model were used to simulate sorption isotherms (described in S2 of supporting information). The Langmuir isotherm provided the best fit for both SMX (R2 ¼ 0.98) and SPY (R2 ¼ 0.96) (Table 1), thus are shown in Fig. 5b. This model suggests a surface adsorption mechanism for these sulfonamides and is consistent with the reported removal of methylene blue adsorption from aqueous solution by monolayer adsorption onto the surface of saw dust biochar (Sun et al., 2015). The Langmuir model maximum adsorption capacities (Smax) were 100.3 mg/g and 57.9 mg/g for SMX and SPY in laboratory solutions, respectively (Table 1). Those are higher than the reported maximum adsorption capacities of other biochar-based adsorbents including giant reed biochar (4.99 mg/g of SMX) (Zheng et al., 2013), H3PO4-activated bamboo biochar (88.10 mg/g of SMX) (Ahmed et al., 2017), carbon nanotube-modified biochar (27.90 mg/g of SPY) (Inyang et al., 2015), and anaerobic digested bagasse biochar (8.60 mg/g of SPY) (Yao et al., 2018).

3.3. Adsorption of sulfonamides in wastewater In wastewater, SMX adsorption gradually increased and reached equilibrium within 8e12 h (Fig. 6a). While the overall equilibrium removal rate of SMX in wastewater was much lower than that in water, the two kinetic curves showed similar trends, reflecting similar SMX adsorption rates in the two systems (Figs. 5a and 6a). For SPY in wastewater, around 85% was removed within 8 h and the removal rate reached equilibrium at 12 h (Fig. 6a), which is similar to that of SPY in water (Fig. 5a). These results indicate that the governing rate-limiting factor of sulfonamide adsorption onto the biochars was a physical process such as diffusion rather than a

Fig. 6. Adsorpiton Kinetics (a) and isotherms (b) of SMX adsorption onto BM-HC450 (open circles) and SPY adsorption onto BM-BB450 (open triangles) in wastewater. Symbols are experimental data and lines are model results.

Table 1 Best-fit parameters of adsorpiton kinetics and isotherms models examined in this study. Sorbate/Sorbent/Solution

Model

Parameter 1

Parameter 2

R2

SMX/BM-HC450/water

PFO PSO Elovich Langmuir Freundlich PFO PSO Elovich Langmuir Freundlich PFO PSO Elovich Langmuir Freundlich PFO PSO Elovich Langmuir Freundlich

k1 ¼ 3.430 (1/h) k2 ¼ 0.136 (g/mg/h) b ¼ 0.256 (mg/g) K ¼ 0.329 (L/mg) Kf ¼ 24.450 (mg(1n)Ln/g) k1 ¼ 1.314 (1/h) k2 ¼ 0.052 (g/mg/h) b ¼ 0.179 (mg/g) K ¼ 1.818 (L/mg) Kf ¼ 38.040 (mg(1n)Ln/g) k1 ¼ 1.947 (1/h) k2 ¼ 0.127 (g/mg/h) b ¼ 0.334 (mg/g) K ¼ 5.683 (L/mg) Kf ¼ 18.700 (mg(1n)Ln/g) k1 ¼ 3.414 (1/h) k2 ¼ 0.125 (g/mg/h) b ¼ 0.242 (mg/g) K ¼ 6.207 (L/mg) Kf ¼ 40.920 (mg(1n)Ln/g)

qe ¼ 36.30 (mg/g) qe ¼ 38.30 (mg/g) a ¼ 6615.80 (mg/g) Smax ¼ 100.30 (mg/g) n ¼ 0.57 qe ¼ 39.10 (mg/g) qe ¼ 41.50 (mg/g) a ¼ 638.20 (mg/g) Smax ¼ 57.90 (mg/g) n ¼ 0.18 qe ¼ 23.60 (mg/g) qe ¼ 24.90 (mg/g) a ¼ 945.00 (mg/g) Smax ¼ 24.30 (mg/g) n ¼ 0.14 q e ¼ 38.40 (mg/g) qe ¼ 40.50 (mg/g) a ¼ 6467.50 (mg/g) Smax ¼ 53.70 (mg/g) n ¼ 0.16

0.493 0.797 0.967 0.981 0.977 0.685 0.858 0.976 0.963 0.860 0.676 0.875 0.958 0.788 0.984 0.770 0.935 0.939 0.748 0.951

SPY/BM-BB450/water

SMX/BM-HC450/wastewater

SPY/BM-BB450/wastewater

Note: Information of parameters (qe, k1, k2, a, b, K, Smax, Kf, n and R2) can be found in the Supporting Infromation S1 and S2.

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chemical process in which the additional ions in wastewater might have competed for adsorption sites (Ho et al., 2000). Again, the Elovich model was the best fit for both SMX and SPY (R2 ¼ 0.96 and 0.94, respectively, Table 1), suggesting the adsorption of sulfonamides on the ball milled biochars in wastewater was also controlled by multiple mechanisms. Adsorption of SPY onto BM-BB450 in wastewater was similar to that in DI water, whereas adsorption of SMX by BM-HC450 was much less in wastewater compared to that in DI water (Figs. 5b and 6b). Unlike for SMX and SPY adsorption in DI water, the Freundlich model described the wastewater sorption experimental data better for both (R2 ¼ 0.98 and 0.95, respectively, Table 1). This suggests that the complexity of wastewater chemistry made the mechanisms of sulfonamide adsorption in wastewater more heterogeneous than that in water. In wastewater, the Langmuir maximum adsorption capacity derived from the experimental data were 25.7 mg/g for SMX (Table 1), much lower than that in water (100.3 mg/g). This dramatic reduction can be attributed to two factors related the different chemistry of water and wastewater. The pH of wastewater (7.6, Table S2) was higher than that of water (6.0), which could be the main factor. As shown in Fig. 4, adsorption of SMX on biochar was pH-dependent at this pH range and its removal efficiency decreased with increasing pH (e.g., 63% at pH 6.5 and 12% at pH 7.5) due to electrostatic repulsion between SMX and biochar. Additionally, since dissolved organic matter (DOM) was present in wastewater (4.1e9.4 mg/L, Table S2), competitive adsorption between negatively charged DOM (organic acids) and the dominant anionic species of SMX in wastewater could also reduce SMX removal by ball milled biochar (Lian et al., 2015; Xie et al., 2014). There was no significant change in maximum adsorption capacity of SPY adsorption in wastewater (58.6 mg/g) compared to that of water (57.9 mg/g). This may be due to the predominantly neutral speciation of SPY at this pH range (6.0 in water and 7.6 in wastewater). Thus, no electrostatic repulsion between biochar and the sorbate occurred. 4. Conclusions Ball milling greatly enhanced the ability of biochar to sorb SMX and SPY in water (pH of 6.0). For each biomass, 450
C ball milled biochar showed the best removal efficiency for both SMX and SPY. Comparison of the physiochemical properties of the ball milled biochars and the sulfonamide removal efficiencies revealed that the adsorption was controlled by multiple mechanisms. Solution pH strongly affected sulfonamide adsorption through variations in electrostatic interaction. Nevertheless, when tested in wastewater (pH of 7.6), the 450
C ball milled biochar still performed well, especially for SPY adsorption. Due to the greater pH of wastewater, SMX sorption capacity of BM-HC450 dramatically declined but still removed a considerable amount. Findings of this work indicate that ball milled biochar has great potential as an adsorbent capable of removing sulfonamides from wastewater in field applications. Because of its promising physicochemical and sorptive properties, ball milled biochar should be further evaluated as a remediant of various emerging contaminants and tested under environmentally relevant conditions. CRediT authorship contribution statement Jinsheng Huang: Methodology, Formal analysis, Investigation, Writing - original draft. Andrew R. Zimmerman: Formal analysis, Writing - review & editing. Hao Chen: Conceptualization, Writing review & editing. Bin Gao: Conceptualization, Methodology, Formal analysis, Writing - review & editing.

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