New insights into the interaction between heavy metals and struvite: Struvite as platform for heterogeneous nucleation of heavy metal hydroxide

Chemical Engineering Journal 365 (2019) 60–69

Contents lists available at ScienceDirect

Chemical Engineering Journal journal homepage: www.elsevier.com/locate/cej

New insights into the interaction between heavy metals and struvite: Struvite as platform for heterogeneous nucleation of heavy metal hydroxide

T

⁎

Chongjian Tanga,b, Zhigong Liua,b, Cong Penga,b,c, , Li-Yuan Chaia,b, Kensuke Kurodac, Masazumi Okidoc, Yu-Xia Songa,b a

School of Metallurgy and Environment, Central South University, Changsha, China Chinese National Engineering Research Centre for Control and Treatment of Heavy Metal Pollution, Changsha 410083, China c Institute of Materials and Systems for Sustainability, Nagoya University, Nagoya, Japan b

H I GH L IG H T S

G R A P H I C A L A B S T R A C T

Heavy metal hydroxide’s hetero• geneous nucleation on struvite was detected.

has enhancement effect in • Struvite heavy metal precipitation. △G were intensively abated through • heterogeneous nucleation on struvite. of sorption, nucleation, and • Model precipitation by struvite was estabi

lished.

A R T I C LE I N FO

A B S T R A C T

Keywords: Struvite Heavy metal Slow-release fertilizer Heterogeneous nucleation Sorption Precipitation

During the struvite (MgNH4PO4·6H2O) recovery from agricultural or industrial wastewater, the extensive existence of heavy metals would pose great threats to the planting and environment. This work revealed the association of kinds of heavy metals, as possible substances in the wastewater, with the struvite. The struvite has been synthesized in situ and employed to contact with both high and low concentration heavy metal (including Cu, Ni, Pb, Zn, Mn, Cr(III)) wastewater. The heavy metal precipitation rates under different pH values from 6.0 to 10.0, and under a series of struvite addition amount have been investigated. The precipitation of heavy metals without addition of struvite is functioned as control experiments. The struvite’s presence can enhance the heavy metal precipitation rate under all pH values. The Ni and Mn have relatively lower precipitation rate compared with other metals. For extremely low heavy metal concentration the precipitation rate is 99.1%, 97.9%, 99.9%, 98.9%, 96.9%, and 98.3%, which is much higher than that of control group (10.5%, 8.7%, 13.2%, 14.1%, 6.7%, and 10.5%). Through XPS and TEM & EDS analysis, the heavy metal hydroxides is found to be precipitated on the struvite surface. Based on TEM observations, it has been found the copper hydroxides had nucleation and growth on the struvite’s surface. The heterogeneous nucleation mechanism has been proposed, which provides relationship model of sorption, nucleation, and precipitation of heavy metals in the form of hydroxides on struvite surfaces. It has been calculated that the △Gi value that thermodynamic activation energy barrier constraints on the metal hydroxide formation can be intensively abated through heterogeneous nucleation on struvite.

⁎

Corresponding author. E-mail address: [email protected] (C. Peng).

https://doi.org/10.1016/j.cej.2019.02.034 Received 16 December 2018; Received in revised form 1 February 2019; Accepted 4 February 2019 Available online 05 February 2019 1385-8947/ © 2019 Elsevier B.V. All rights reserved.

Chemical Engineering Journal 365 (2019) 60–69

C. Tang et al.

of [Cu(NH3)4]2+ complex ion by struvite precipitation method. It was also found that there might be some interactions between Cu(OH)2 fine particles and struvite crystal, such as hydrogen bonding and electrostactic force, during the precipitation of struvite in the liquid phase [35–38]. In order to reveal the mechanism behind the simultaneous precipitation of heavy metals and struvite, it is critical to investigate the interact of different kinds of heavy metals with struvite crystal under the aqueous condition. In this study, struvite crystal was synthesized in situ and was employed for the investigation upon the interaction with heavy metals including Zn, Pb, Cu, Ni, Mn, Cr in the aqueous solution. The heavy metals of both high and low concentration in aqueous solution were considered. It was found that heavy metals’ precipitation on struvite was ubiquitous even for situation of low concentration, and the struvite promoted the metal hydroxide precipitation by lowering the barrier in metal hydroxide formation under low metal concentrations. Heterogeneous nucleation and growth of metal hydroxide on the struvite surface was firstly found, which can be the critical mechanism for the enhancement in the heavy metal precipitation from aqueous condition.

1. Introduction Fast economical growth and urbanization has triggered expansion in nutrient discharge [1]. Struvite crystallization has been gaining great interest as a method for phosphorous and nitrogen recovery [2–4]. Struvite, a crystalline substance which consists of magnesium, ammonium, and phosphorus in the same-molar concentrations (MgNH4PO4·6H2O), can be recovered from phosphorous and nitrogen rich sources including wastes and wastewaters to mitigate the total nitrogen (TAN) and P content therein [5–7]. Apart from disposed as the product generated from treatment of wastewater contamination by TAN and P, this mineral product can be functioned as sustainable source of phosphate fertilizer [8–10]. It has been considered as a high-quality fertilizer for its slow release rate of nutrients [11,12]. In the past decades, struvite used to be considered as troublesome substance in wastewater treatment plant since it existed as scale deposit causing maintenance problems and making negative effect to treatment efficiency [12]. In recent years, the centralized wastewater treatment plants are treating struvite as a profitable products for its nature of phosphorusrich slow-release fertilizer (SRFs) [13,14]. The SRFs has recently been applied to increase the agronomic effectiveness. The current SRFs are mainly consisted of polymer-coated soluble P material and the material that has intrinsic slow-release properties [15,16]. Struvite belongs to the latter one, as a recovery product from waste streams owning slowrelease properties arisen from quite low material solubility [17,18]. Recycling P and N in this way is quite important in modern agriculture, since it depends highly on nutrients, which is mined from the finite reserves [19–21]. Especially as the market price of P continuously increases, the struvite product from wastewater or dry sanitation sites can provide satisfactory revenue along with solving waste discharge problems by producing efficient SRFs [22–24]. Moreover, the struvite precipitation process has advantages of simplicity and high efficiency [25,26]. Thus, the struvite precipitation process has been widely studied for both simulated and actual wastes or wastewaters [3,24,26,27]. However, the hygienic and environmental quality of the struvite generated has still not been thoroughly studied and evaluated. Researchers have been focusing on the optimization of struvite recovery conditions, while there are less attention being paid to the possible contaminates existing in the wastewater that can interact with the struvite. During the struvite recovery process, the heavy metals, such as Zn and Cr, can co-exist with the nutrient containing water [28]. For example, the landfill leachate generated from municipal landfill site always contains a variety of heavy metals including Cu, Ni, Cr and so forth [13]. Steinmetz et al. reported a swine wastewater which contained 513 μg L−1 total Cr and still had 475 μg L−1 Cr after screening, and it was decreased to 37 μg L−1 only by passing through a 0.45 μm filter [29]. Ashaki A. Rouff et al. reported that the Zn concentration in urine can range from 0.07 to 0.537 mg L−1, and swine manure generally has total Zn content ranging from 12 to 40.6 mg L−1 [30]. The average Zn concentration in sewage sludge anaerobic digester effluent is 50.998 mg L−1 with Zn concentration of 0.063 mg L−1 in its corresponding liquid phase, and the struvite recovered from the liquid phase generally has Zn content of 13 mg Kg−1 [31]. As to the mechanism behind the heavy metals’ interact with struvite, it still has not been intensively studied. Some researchers have recently reported the co-precipitation phenomenon of struvite and heavy metals including Zn and Cr [32–34]. For example, Ashaki A. Rouff has studied the sorption of chromium with struvite during the process of phosphorus recovery. It was found via XAFS that Cr (OH)3·nH2O(am) was formed during Cr(III) removal, particularly, for relatively high Cr(III) concentrations of 50–100 μM, Cr(OH)3·nH2O was the dominant form of Cr(III) in the co-precipitate solids [34]. Struvite crystal contains abundant amino groups, hydroxyl groups and phosphate groups, which might help the adsorption of heavy metals by coordination or adherence of heavy metal hydroxide by hydrophilic interactions. Our previous researches have studied the decomposition

2. Materials and methods 2.1. Synthetic heavy metal wastewaters Six heavy metals were employed in this study, which included Cu (II), Ni(II), Zn(II), Pb(II), Mn(II), and Cr(III). The heavy metal concentrations used in this research referred to two different strengths real wastewaters. The high-strength wastewater was discharged from an industrial park in China and the low-strength wastewater was from an anaerobic digestate supernatant in a plant. The metal concentrations in the effluent from industrial park were Cu (40.2 mg/L), Ni (59.5 mg/L), Zn (50.1 mg/L), Pb (61.3 mg/L), Mn (28.6 mg/L) and Cr (19.7 mg/L), and that from anaerobic digestate supernatant included Cu (1.91 mg/ L), Ni (3.32 mg/L), Zn (0.81 mg/L), Pb (0.44 mg/L), Mn (1.40 mg/L) and Cr (0.90 mg/L), respectively. All the reagents were of analytical grade and were used without further purification. Ultrapure water (18 M) was used in all experiments. Concentrated sulfuric acid (H2SO4), ammonium sulfate ((NH4)2SO4), magnesium chloride hexahydrate (MgCl2·6H2O), disodium hydrogen phosphate (Na2HPO4), copper sulfate (CuSO4), nickel sulfate (NiSO4), zinc chloride (ZnCl2), lead nitrate (Pb(NO3)2), manganese chloride (MnCl2), chromium chloride (CrCl3), and sodium hydroxide (NaOH) were purchased from the Sinopharm Group Chemical Reagent Co., Ltd. The heavy metal solution was prepared by adding and mixing six kinds of heavy metals into the 0.1 M NaNO3 solutions. The 0.1 M NaNO3 electrolyte was employed as the background because these ions were the common major constituents in wastewaters. The struvite was in situ synthesized by adding magnesium and phosphorus into the ammonium solution, which would be elaborated in the following part of the paper. 2.2. Synthesis of struvite Firstly, 500 ml ammonium chloride solution (2 g/L count by N) was prepared in a 1 Liter-scale beaker. Then, Na2HPO4 (1 M) and MgCl2 (1 M) solution was added into the ammonium solution. The molar ratio between ammonium, magnesium, and phosphorus was in accordance with n(N):n(Mg):n(P) = 2:1:1. Meanwhile, 32 ml NaOH (0.5 M) was added into ammonium solution along with the magnesium and phosphorus, in order to achieve the final pH 9.0 in the system. The reaction was under magnetic stirring with stirring rate of 300 rpm over 10 min. Finally, the synthesized struvite crystal materials were rinsed by purewater for 5 times to remove the residual salts on the surface, and then was dried at 60 ℃ for 6 h. The characterizations of the synthesized 61

Chemical Engineering Journal 365 (2019) 60–69

C. Tang et al.

The samples were collected in the pattern of 20 s a time. After sample collecting, the carbon net along with the filter paper was dried under natural condition. After drying, the samples were transferred to the TEM tests.

struvite were described in detail in Supporting Information. (See Fig. S1, Fig. S2 and Fig. S3) 2.3. Study of heavy metal interaction with struvite

2.4. Analytical and characterization methods

2.3.1. Heavy metal precipitation from aqueous solution under different concentration and pH Experiments were carried out to study the heavy metals’ contact with struvite, and the heavy metals’ precipitation rates were investigated. Two heavy metal concentrations referring to two real wastewaters were applied, i,e., Cu (40.2 mg/L), Ni (59.5 mg/L), Zn (50.1 mg/L), Pb (61.3 mg/L), Mn (35.1 mg/L) and Cr (19.7 mg/L), which was registered as Solution1, and the other one contained Cu 1.91 mg/L), Ni (3.32 mg/L), Zn (0.81 mg/L), Pb (0.44 mg/L), Mn (1.40 mg/L) and Cr (0.90 mg/L), registered as Solution2. The struvite was added into the heavy metal solutions, under magnetic stirring (200 rpm), which was considered as the struvite contact group. As comparison, another experiments were conducted by adding only NaOH to the solution to precipitate heavy metal in hydroxide form, which was taken as the control group. Before introducing struvite into the solution, the struvite materials were ultrasonic dispersed, realized by adding pure-water into the struvite materials and then being transferred into ultrasonic equipment. The weight ratio between water and struvite was controlled as 2:1. In the first part of experiments, different amounts of struvite (0.5 g, 1.0 g, 1.5 g, 2.0 g and 3.0 g) were added into 400 ml Solution1. The pH was adjusted to 9.0 and was kept during the contact process. This process was divided as two parts, i.e., first 20 mins was under stirring condition, and the subsequent 10 mins was for precipitation. In the second part of the experiments, struvite (2.0 g) was applied to the Solution1 under different pH, to investigate the heavy metal precipitation rate at different pH in the range of 6.0–10.0. In this part, the heavy metal precipitation rate for the control group was investigated by only adjusting pH of the solution from 6.0 to 10.0, without struvite addition.

The precipitate samples from different addition amount of struvite, i.e. 1.0 g, 1.5 g, 2.0 g and 3.0 g, were collected for SEM and EDS analysis. Those from different pH conditions, i.e. 6.0, 7.0, 8.0 and 9.0 in struvite addition amount of 2.0 g, were collected for XRD analysis. To clarify the chemical composition of the heavy metals in the precipitate, the precipitate from pH 9.0 (with addition weight of 2.0 g) was employed for XPS detection. The concentration of the six heavy metals was measured by inductively coupled plasma (ICP-AES, IRIS Intrepid II XSP ThermoFisher). The pH value was measured by Mettler FE20K pH meter. The X-ray diffraction (XRD) patterns were obtained using a Rigaku D/Max-RB diffractometer with Cu-Ka radiation (40KV, 40 mA), from 10° to 60°. X-ray photoelectron spectroscopy (XPS) measurements were carried out on a Thermo Fisher Scientific K-Alpha 1063 using Al-Ka Xray as the excitation source with analysis chamber ≤10−10 Torr. FEI Quanta 650 FEG Scanning electron microscopy (SEM) was used to characterize the morphology of the precipitate, with accelerating voltages of 20 KV. EDS spectra was also collected on the FEI Quanta 650 FEG Scanning electron microscopy equipped with an energy-dispersive X-ray spectrometer. The TEM images were collected on a HR-TEM JEOL JEM-3010 transmission electron microscope with electron dispersive spectroscopy (EDS) mapping capability. 3. Results 3.1. Different heavy metals’ precipitation from high concentration Solution1 Table 1 shows the residual heavy metal concentrations after contact with struvite under different pH conditions. The heavy metals precipitation rate with presence of struvite was increased compared with the control group without presence of struvite (control group). Particularly in lower pH, the heavy metal precipitation rate in the presence of struvite was much higher than the control group, e.g. in pH 6.0, where the precipitation rate in the control group was quite low for kinds of heavy metals. The residual copper and zinc concentrations, for instance, were 13.25 and 41.89 mg/L after control treatment under pH 6.0, with corresponding precipitation rate of 67.6% and 16.4% respectively, while their concentrations after contact with struvite were 0.13 and 1.66 mg/L with precipitation rate of 99.7% and 96.7% respectively. As in higher pH 7.0–10.0, the precipitation rate of both the struvite contact group and the control group increased, but it is still easy to see higher precipitation rate for the struvite contact group than the control group. Particularly, even when pH reached 10.0, there were still large contents of residual heavy metal in the control group, while the struvite contact group had extremely low content of residual heavy metals under pH 10.0, where concentrations of the six heavy metals from copper to chromium were 0.01, 0.04, 0.00, 0.00, 0.13 and 0.004 mg/L, respectively. Fig. 1 shows the residual content of heavy metals against different addition amount of struvite, under pH 9.0. It can be seen in Fig. 1 that the heavy metal content in Solution1 decreased with increasing the amount of struvite from 0.5 g (1.25 g/L) to 3.0 g (7.5 g/L). The trend was the same for all the six heavy metals from copper to chromium, however, the precipitation rates of the heavy metals were different. The nickel and manganese had relatively lower precipitation rate under the same pH compared with other four heavy metals. It was probably due to the different thermodynamic equilibrium between the heavy metals. The solubility constant Ksp for copper hydroxide, nickel hydroxide, zinc hydroxide, manganese hydroxide, and chromium hydroxide are

2.3.2. Effect of contact time Moreover, the heavy metal precipitation rate as a function of time under different pH conditions based on contact with struvite was also studied. In this part, 15 samples from different contact time were collected from each beaker and filtered by filter paper (with pores ≤ 3 μm). One sample (2 ml) was collected per minute during the first 10 mins, and two mins a time during the following 10 mins. Similarly, 2 g struvite was also added to Solution 2 for investigating the precipitation of heavy metals under low concentrations. The pH was adjusted to 9.0 with other conditions being the same to the above. Still as comparison, the Solution 2 was treated by only adding NaOH to reach the same pH 9.0, as a control group. 2.3.3. Heterogeneous nucleation investigations via TEM observations Based on the experimental results and precipitate analysis, it was found that heterogeneous nucleation was the main mechanism for heavy metal and struvite’s co-precipitation from solution. To clarify the process of heavy metal nucleation and growth on the surface of struvite, TEM observations were conducted by capturing the surface characterization in different times. Since there can be difference in the growth kinetics of different heavy metals, only one heavy metal selected for this TEM observation would be more appropriate. In this experiment, copper was adopted as the representative heavy metal. To prepare the samples for TEM observations, 2 g struvite was added to copper containing solution (with Cu 40.2 mg/L, same concentration with Solution1) under stirring condition with speed of 400 rpm. Along with addition of struvite, 5 ml 0.5 M NaOH was also added into the system to realize the final pH of 8.0. Then, the samples from the system were collected by pipet with 3 mm-diameter nozzles and were dropped onto the specialized carbon net (placed on a filter paper) for TEM detection. 62

Chemical Engineering Journal 365 (2019) 60–69

C. Tang et al.

Table 1 Residual heavy metal concentrations after contact with struvite (weight of 2 g) under different pH from 6.0 to 10.0 (●-Struvite contact ○-control group). Heavy metals

Cu(II) (mg/L) Ni(II) (mg/L) Pb(II) (mg/L) Zn(II) (mg/L) Mn(II) (mg/L) Cr(III) (mg/L)

pH

● ○ ● ○ ● ○ ● ○ ● ○ ● ○

6.0

7.0

8.0

9.0

10.0

0.13 ± 0.04 13.25 ± 1.23 47.99 ± 2.11 58.78 ± 5.05 0.010 ± 0.01 11.66 ± 2.98 1.66 ± 0.20 41.89 ± 4.99 18.60 ± 1.35 29.76 ± 2.19 0.12 ± 0.04 2.43 ± 0.4

0.05 ± 0.01 5.46 ± 0.94 37.25 ± 2.12 48.92 ± 3.00 0.005 ± 0.000 4.73 ± 0.90 0.14 ± 0.04 9.56 ± 0.55 12.45 ± 1.01 16.52 ± 1.24 0.005 ± 0.002 1.55 ± 0.18

0.04 ± 0.02 1.90 ± 0.30 10.01 ± 0.33 14.55 ± 1.01 0.006 ± 0.003 1.59 ± 0.38 0.01 ± 0.01 4.99 ± 0.89 3.10 ± 0.53 4.96 ± 0.50 0.005 ± 0.002 1.37 ± 0.24

0.01 ± 0.005 1.81 ± 0.24 0.93 ± 0.01 3.98 ± 0.39 0.004 ± 0.000 1.33 ± 0.03 0.00 ± 0.00 4.13 ± 0.99 0.68 ± 0.19 3.11 ± 0.24 0.004 ± 0.002 0.98 ± 0.19

0.01 ± 0.006 1.78 ± 0.29 0.04 ± 0.05 1.79 ± 0.28 0.000 ± 0.000 1.16 ± 0.17 0.00 ± 0.00 3.31 ± 0.80 0.13 ± 0.09 3.76 ± 1.00 0.004 ± 0.002 1.04 ± 0.11

Fig. 2. Comparison of precipitation rate of heavy metals in Solution2. 1Struvite contact group and 2-control group. Fig. 1. Residual content of heavy metals against different addition amount (g/ L) of struvite.

precipitation rate of the control group can be caused by the low supersaturation for the low concentration of heavy metals in the formation of the hydroxides. The impetus for nucleation was quite weak due to low content of metal in the solution, leading to quite slow or incapability in the formation of metal hydroxide. Comparatively, the presence of struvite in the solution seemed to promote the nucleation and growth of hydroxide, and it might be realized through heterogeneous nucleation of heavy metal hydroxide on the surface of the struvite crystals.

2.2 × 10−20, 5.38 × 10−16, 1.43 × 10−20, 1.2 × 10−17, 1.9 × 10−13 and 6.3 × 10−31, respectively. It can be seen that the Ksp 5.38 × 10−16 and 1.9 × 10−13 of nickel hydroxide and manganese hydroxide are obviously higher than that of other four heavy metal hydroxides, suggesting that nickel and manganese need higher alkaline condition for the generation and growth of the corresponding hydroxide Ni(OH)2 and Mn(OH)2. For the lowest addition amount of 0.5 g (Fig. 1), the residual content from copper to chromium was 0.98, 3.44, 1.05, 2.80, 2.15 and 0.68 mg/ L, respectively, all of which were lower than the control group. So it can be summarized that through contact with struvite the precipitation of heavy metals in the solution was greatly enhanced.

3.3. Influence of contact time The time-concentration relationship experiments were done under different pH conditions. The results are shown in Fig. 3.The heavy metal concentrations in the solution decreased sharply in the 1st min, and then slowly decreased from the 2nd min to 7th or 8th min. Subsequently, their concentrations increased slowly and reached an equilibrium. For copper, lead, zinc and chromium, their equilibrium state came earlier than nickel and manganese, and their concentration was decreased to extremely low after 7–8 mins. Moreover, the large proportion was precipitated in the first two mins, indicating the fast reduction rate occurred in the heavy metal precipitation process. Under lower pH conditions, particularly 7.0, it can be seen the nickel and manganese slowly decreased within the test time from 1st min till 8–9th mins later, indicating the nickel and manganese underwent a slight different removal mechanism compared with other four heavy metals in lower pH. It is interesting to find that the magnesium content in the solution went up slowly during this test, and this phenomenon was

3.2. Different heavy metals’ precipitation from low concentration Solution2 To further confirm the effect of struvite in heavy metal precipitation enhancement, Solution2 with quite low heavy metal concentration was employed in this study. The results are shown in Fig. 2. It can be seen that more than 95% of heavy metals could be precipitated from the solution with struvite addition amount of 2 g. The precipitation rate was 99.1%, 97.9%, 99.9%, 98.9%, 96.9% and 98.3% respectively for copper, nickel, lead, zinc, manganese and chromium (III). However, the precipitation rates for the control group were much lower, with precipitation rate of 10.5%, 8.7%, 13.2%, 14.1%, 6.7% and 10.5%, respectively, from copper to chromium (III). So it can be inferred that through contact with struvite the heavy metals with extremely low concentration can be largely precipitated. The quite low 63

Chemical Engineering Journal 365 (2019) 60–69

C. Tang et al.

Fig. 3. Heavy metal residual concentration as a function of time after contact with struvite under different pH. (a) pH = 7.0; (b) pH = 8.0; (c) pH = 9.0; (d) pH = 10.0.

Fig. 4(a) to Fig. 4(d) it can be seen the surface was dotted with small precipitates. The SEM image with low magnification was shown in Fig. S4. According to EDS test, the area1 selected a smooth area where there was no small precipitate, while the area2 selected a tiny part of small precipitate. It can be seen the EDS test results that area2 has a significantly more heavy metal content than that of area1. It can be inferred that the small precipitates on struvite surface was heavy metal compounds, most probably metal hydroxides. It is noteworthy from Fig. 4(a)–(d) that the struvite had different quantities of precipitate on its surface against different struvite addition amount. As the addition amount of struvite increased from 1.0 to 3.0 g, the corresponding struvite surface had gradually less heavy metal precipitate. The struvite (1 g addition) in Fig. 4(a) was almost filled with heavy metal precipitates, while the struvite in Fig. 4(d) had obviously less precipitates. So it can be inferred that the struvite might be functioned as the bearing platform for the heavy metal precipitates, since more quantities of struvite would lead to decrease in the relative proportion of heavy metals. It can also be inferred that the precipitation of heavy metals occurred on the surface of the struvite. In order to clarify the heavy metal compound on the surface of struvite, the XPS tests were conducted by selecting the precipitate from test in condition of pH 9.0 and struvite addition of 2.0 g. The test results were shown in Fig. 5. The measured binding energies of Cu 2p3/2 and Cu 2p1/2 were equal to 935.0 and 955.1 eV, respectively. Meanwhile, two satellite peaks located at 944.2 and 963.2 eV were clearly observed, which well fitted the characteristic of CuO [39]. The Ni 2p region (Fig. 5(b)) comprised four easily discernible features: the Ni 2P3/2 main peak and its satellite at ～856.2 and 861.2 eV, and the Ni 2P1/2 main peak and its satellite at ～873.8 and 879.2 eV, indicating the Ni compound on the struvite surface was actually the Ni(OH)2 [40,41]. Fig. 6(c) shows that the characteristic peak of Pb appearing at 138.2 eV (assigned to Pb 4f7/2) and at 143.4 eV(assigned to Pb4f5/2), respectively, which agreed with the values reported for Pb(OH)2 [42]. From

pronounced in low pH value. Specifically, the magnesium content in the solution slowly increased from 13.1 mg/L (1st min) to 25.3 mg/L in the 18th min under pH 7.0, and increased even more slowly from 4.0 mg/L (1st min) to 7.5 mg/L in the 18th min under pH 10.0. Lowering the pH condition, the amount of the increased magnesium turned out to be higher. These seemingly strange results can be caused by the ion exchange occurred during the treatment process. It can be expressed by the Eq. (1):

M2 + + MgNH4 PO4 ·6H2 O→ MNH 4 PO4 ·6H2 O+ Mg2 + 2+

(1) 2+

2+

where M is heavy metal cation, and is most probably Ni or Mn . Under the lower pH conditions, large quantities of the nickel and manganese were still at ion state in the solution, due to the lower Ksp of Ni(OH)2 and Mn(OH)2. It would lead to slow ion exchange with Mg2+ in the crystal lattice of struvite. This inference would be further demonstrated in the following part of the paper. However, the ion exchange could not be the main reason for heavy metal removal from aqueous solution since its slow rate. The most probable reason was the formation of heavy metal hydroxide under the test pH conditions from 6.0 to 10.0. The heavy metals’ precipitation enhancement effect from struvite could be explained by the heterogeneous nucleation effect brought by the struvite, which would be elaborated in this text. 3.4. Characterization of co-precipitation products of struvite and heavy metals The characteristic of struvite for the experiments was tested by SEM. The precipitates from different addition of struvite from 1.0 to 3.0 g were also analyzed by SEM & EDS. As can be seen in Fig. 4, the rodshaped struvite had width about 3 μm and length about 10–20 μm. The surfaces were smooth and contained numerous gullies, which were useful for enlargement in specific surface area. After heavy metals treatment, the surface of the struvite had significant changes. From 64

Chemical Engineering Journal 365 (2019) 60–69

C. Tang et al.

Fig. 4. SEM photos and EDS results of precipitates under different struvite addition amount. a-Struvite addition amount of 1.0 g; b-Struvite addition amount of 1.5 g. c- Struvite addition amount of 2.0 g; d- Struvite addition amount of 3.0 g.

Fig. 5(d), the binding energy of Zn 2p3/2 peak was at ～1021.9 eV, and binding energy of Zn 2p1/2 was at ～1044.9 eV, which was in accordance with ZnO [43]. In Fig. 5(e), it has two main peaks at 641.2 eV and 653.3 eV, indicating the compound for manganese was Mn2O3 [44,45]. Fig. 5(f) shows the two main peaks of Cr 2p at 577.3 eV and 587.2 eV, which complied with XPS features of Cr(OH)3 [44,46]. The CuO and ZnO detected in the XPS spectra was caused by the dehydration of Cu(OH)2 and Zn(OH)2 during drying process (60 ℃) of the samples, since the XPS requires ultra-high vacuum condition and the samples need to be highly dried before transferred for the measurements. As to Mn(OH)2, it is quite likely to be both dehydrated and oxidized into Mn2O3 in air condition [47]. In addition, TEM images of precipitate sample collected from struvite’s contact with Solution1 and EDS results of the selected areas in the particles on the surface of struvite were shown in Fig. S5 and Fig. S6. The detailed calculations

upon the EDS results are in the Supporting Information. These tests further proved the composition of heavy metal precipitate on the surface of struvite were heavy metal hydroxides. Based on results of the heavy metal precipitation as a function of contact time, and SEM and XPS analysis above, it can be determined that the heavy metals were removed from aqueous solution by precipitating on the surface of struvite in the form of hydroxide. So heterogeneous nucleation was given the priority in the mechanism determination, but there might be ion exchange occurring during the treatment, particularly under the lower pH values (pH 6.0–7.0), which was analyzed in above text. To further confirm the existence of ion exchange, XRD tests for the precipitates from different pH in struvite contact group were carried out. Fig. 6 shows the XRD characteristics of samples upon different pH of 7.0, 9.0, 10.0 and the struvite (XRD pattern with a larger angular range of 10–60° is shown in Fig. S7). The

Fig. 5. High resolution XPS spectra of the six heavy metals in the precipitate (from struvite contact group with addition amount of 2.0 g and pH 9.0) (a) Cu 2p; (b) Ni 2p; (c) Pb 4f; (d) Zn 2p; (e) Mn 2p; (f) Cr 2p. 65

Chemical Engineering Journal 365 (2019) 60–69

C. Tang et al.

results clearly showed the copper hydroxides’ formation and growth on struvite surface, suggesting the struvite functioned as heterogeneous nucleation templates for copper hydroxide. 4.2. Study on mechanism of heavy metals’ interaction with struvite The metal hydrated cations [M(H2O)n]x+ in the solution can be adsorbed to the surface of struvite through coordination bonding, since the struvite has hydroxyl groups, ammonium groups, and phosphate groups, which can form coordination bonding with metal hydrated cations. The relationship between cation sorption and precipitation on struvite surfaces can be demonstrated by a progress of surface reactions divided into three stages. The initial stage was sorption stage associated with caption aggregation on struvite surface, followed by surface site saturation, and finally once the supersaturation had been reached, the precipitation on surfaces occurred. If such a progress of metal reactions occurred on struvite surfaces, these stages should have relationship between solid-phase concentration of metal and the concentration of metal remained in solution-phase. This relationship generalizing the reactions for heavy metal caption sorption and hydrolysis on struvite as follows:

Fig. 6. XRD patterns of in situ synthesized struvite and precipitates from struvite treatment under pH of 7.0, 9.0, and 10.0 (all with 2 g struvite addition).

SH + Mx + + (x − 1)H2 O ⇔ SM(OH)0x − 1 + xH+

precipitates of struvite treatment group under pH 9.0 and 10.0 have no significant shift in diffractions peaks. But that from pH 7.0 has a slight shift to higher degrees, indicating the ion exchange might happen in pH 7.0. As shown in Fig. 3, copper, lead, zinc, chromium was almost reduced in the first two to three mins, while the nickel and manganese had a quite slow reduction rate after the first several mins, with the gradual increase of magnesium. This could be arisen from the ion exchange with magnesium in the struvite crystal. The ion radius of nickel (0.069 nm) and manganese (0.067 nm) were smaller than that of magnesium (0.072 nm), so substituting with Mg2+ would lead to dwindling of the crystal lattice, leading to diminishing of interatomic spacing and thus cause diffraction peak to shift to higher degree [48,49].

(2)

x+

here, M is the heavy metal ions, SH represents a struvite surface site, and the SM(OH)0x−1 is struvite surface associated heavy metal. It gives ion concentration ratio [MD]/[H+]x that defines solubility equilibria for SM(OH)x−10.

kMs =

[SM(OH)0x − 1][H+]x [SH][MD]

(3)

In the transition from dissolved ions to surface precipitation as M (OH)x, equilibrium [MD]/[H+]X ratios increased beyond the solubility limits for the newly generated M(OH)X precipitates. The surface hydroxo complexes SM(OH)0x−1 are the intermediate during the transition into the solid precipitate. The formation of mononuclear M(x) hydrolysis species is relatively faster, while the transition of polynuclear hydroxo complexes as intermediate into solid precipitate M(OH)x is slower. The difference in the kinetic rate would lead to metastable supersaturation, which reflected the relatively slow transition of hydroxo complexes to precipitate M (OH)x and higher solubility of the extremely fine particles of M(OH)x. Eventually, the stable nuclei is formed on the surface of struvite that supported the crystal growth. The subsequent transformation of the initial heavy metal surface complexes into M(OH)x crystallites that was recognizable by TEM scanning was followed by the decrease in the equilibrium [MD]/[H+]X ratio, with increasing amount of solid-phase heavy metal M(s). In order to further clarify the precipitation of heavy metal on the surface of struvite, Cu(II) was selected as a representative for the following calculations. The solubility of the fine-sized Cu(II) precipitates can be described in quantity by Eq. (4) [50,51]:

4. Discussion 4.1. Copper hydroxide’s heterogeneous nucleation and precipitation on struvite surfaces In order to clarify the precipitation process of heavy metal on struvite surfaces, TEM tests were employed to detect the heavy metal hydroxides on struvite surface in several time spans. Since there can be difference in the growth kinetics of different heavy metals, only one heavy metal selected for this TEM observation would be more appropriate. In this experiment, copper was adopted as the representative heavy metal. The Fig. 7(a)–(f) show the TEM images of samples collected from the initial 0 s to 100 s, with 20 s a time. Fig. 7(h)–(j) and Fig. 7(l)–(n) show the corresponding EDS mapping for the element Cu, O and P in the selected area of sample collected in 40 s (Fig. 7(g)) and in 100 s (Fig. 7(k)), respectively. Evidently, the distribution of element Cu and element P had a clear boundary on the struvite surface, demonstrating the small precipitates on the surface of struvite was copper compounds and the phosphorus did not exist in the particles. Moreover, there was clear distribution of element O at both struvite area and area of the small precipitates. Thus, by combining the eds mapping results and analytical results above, it is clear that the precipitates attached to the struvite was the copper hydroxide. The struvite without copper hydroxide precipitates had a quite smooth and distinct boundary (Fig. 7(a)). In the 20 s, the copper hydroxide can be seen on the struvite surface and exhibited in the form of quite small nucleis (Fig. 7(b)). Subsequently, it grew up and showed bulk morphology after 40 s (Fig. 7(c)). The sustained development of precipitates can be detected from Fig. 7(c) to Fig. 7(f). In general, the TEM images and eds mapping

d ln k s0/dS = 2/3γ / RT

(4)

or ln K s0(S ) = ln K s0(S = 0) + (2/3/2.3RT )S

(5)

where γ is the mean free surface energy or the interfacial tension (J m−2) and S is the molar surface (m2− mol−1). The molar surface can be expressed by

S = (s / v )(Cup- 1)

(6)

here, s/v represents the surface area to the volume ratio of the stable critical nucleus that is required for precipitation, with unit of m2 L−1. The Cup is the concentration of precipitated Cu(II) (in mol/L). Assuming that all solid-phase Cu in the system was in the form of Cu (OH)2, Cup can be calculated by subtracting the CuD from the value of total copper. By considering the equilibrium of Cu(OH)2: 66

Chemical Engineering Journal 365 (2019) 60–69

C. Tang et al.

Fig. 7. TEM images for the samples collected in different times during heavy metal copper’s contact with struvite and EDS mapping for Cu, O and P elements in the selected area. Sample collected in 0 s; b-Sample collected in 20 s; c-Sample collected in the 40 s; d-Sample collected in 60 s; e-Sample collected in 80 s; f-collected in 100 s; g-selected area in sample collected in 40 s for EDS mapping; (h), (i), (j)-EDS mapping for Cu, O and P, respectively, in the selected area of sample collected in the 40 s; (k)-selected area in sample collected in 100 s for EDS mapping; (l), (m), (n)-EDS mapping for Cu, O and P, respectively, in the selected area of sample collected in the 100 s.

Cu(OH)2 + 2H + ⇔ Cu2 + + 2H2 O Ks0 =

[Cu2 +] [H+]2

Assuming that the interfacial surface tension for copper hydroxide of 0.9 J m−2 (Ionic crystals) [52], the s/v ratio was calculated using slope values determined for Eq. (8). The s can be estimated by dividing s/v values by the density of the solid phase Cu(OH)2, with a density of 3.360 g ml−3. △Gi values can be calculated by multiplying s by the formula weight of Cu(OH)2 and 2/3γ. These values are listed in Table 2. As shown in Table 2, the lower Cu(OH)2 surface area for struvite contact group than that of control group implied that the precipitates developed directly on the surface of struvite. Moreover, the interfacial free energies △Gi was the energy that has to be overcome for nucleation to occur in the solution (homogeneous nucleation) or on the solid surface (heterogeneous nucleation), or between the nascent crystal nucleus. The free energies of the precipitates were substantially reduced against the surface precipitation on the struvite surface (Table 2), with reduction scale of about 52-fold. It can be inferred from the substantial decrease in △Gi value that thermodynamic activation energy barrier constraints on the copper hydroxide

(7)

Through substituting for S from Eq. (6) and for ks0 from Eq. (7) into Eq. (5) leads to:

ln[CuD]/[H + ]2 = ln K S 0(S = 0) + (2/3γ /2.3RT)(s /v )(Cup- 1) + 2

(8)

−1

A diagram of ln[CuD]/[H ] versus Cup yields a slope of (2/3γ/ 2.3RT) (s/v), from which the surface area to volume ratio of the precipitate nuclei can be acquired and an intercept of lnKs0(S=0) can also be determined. The results were shown in Fig. 8. These results show that the ln[CuD]/[H+]2 versus Cup−1 agrees well both for struvite contact group and control group. All the statistical analyses were significant at the p less than 0.05level. But the slope (4.89 × 10−5) in the struvite contact group is much lower than that in control group (7.33 × 10−6), indicating that struvite enhanced the thermodynamic stability and the transformation process of nascent critical nuclei into the solid copper hydroxide precipitate. 67

Chemical Engineering Journal 365 (2019) 60–69

C. Tang et al.

Fig. 8. ln([CuD]/[H+]3) versus 1/Cup for the struvite contact group (a) and the control group (b). Note: The abscissa is 1/Cup, and the ordinate is ln([CuD]/[H+]3).

calculations upon copper hydroxide precipitation on struvite surface, the surface area to the volume ratio (s/v) of the stable critical nucleus is 0.0696, and the △Gi value is 0.156 KJ mol−1, which is substantially decreased compared with that of the control group. It indicates that the thermodynamic activation energy barrier constraints on the copper hydroxide formation are intensively abated through heterogeneous nucleation on struvite surface. It confirms that the heterogeneous nucleation of heavy metal hydroxide on struvite surface enhance the heavy metal precipitation.

Table 2 The calculated values of nucleation and precipitation parameters for copper hydroxide formation on the struvite and in the control group. Treatment

n

R2

s/v (m2 L−1)

S (m2 g−1)

△Gi (KJ mol−1)

Control Struvite

6 6

0.964 0.982

0.4644 0.0696

137.89 2.67

8.07 0.156

formation have been intensively abated through heterogeneous nucleation on struvite surface. So the results provide the relationship of sorption, nucleation, and precipitation of heavy metal hydroxides on struvite surfaces and realize the quantification of the ability of struvite in enhancing heavy metal precipitate formation. From abovementioned, the application of struvite as slow-release fertilizer must consider the association of the heavy metals with struvite during the precipitation from wastewater. The struvite can promote the heavy metal accumulation on its surface at relatively wide pH range. Even for the extremely low concentration of heavy metals, struvite can greatly increase the precipitation of the heavy metals from aqueous solution. The different metal cations have difference in the precipitation rate, i.e., the Ni and Mn have lower precipitation rate compared with other heavy metals including Cu, Zn, Pb, and Cr. The heterogeneous nucleation on struvite surface was found to substantially decrease the thermodynamic activation energy barrier constraints on metal hydroxide formation. In the real application of struvite recovery, the presence of heavy metals may limit the usage of struvite as slow-release fertilizers, for the heavy metals transferred to the soil leading to significant accumulation of heavy metals in the soil. The soil with accumulated heavy metals can affect its quality and pose risk to the health of human being and animals through food chain effect. Thus, it is vital to avoid or decrease the heavy metal presence in the wastewater before the application of struvite recovery process, and the pre-treatment of heavy metals even in low-concentration is necessary.

Acknowledgement We acknowledge the financial support provided by the National Natural Science Foundation of China (51674305), the Key Projects of Science and Technology of Hunan Province (2017SK2420), InnovationDriven Project (2017CX010) of Central South University, the Opening Fund of Jiangsu Key laboratory of Anaerobic Biotechnology (Jiangnan University) (JKLAB201706), China. This work is also partially supported by the Project of Creation of Life Innovation Materials for Interdisciplinary and International Researcher Development of the Ministry of Education, Culture, Sports, Science and Technology, Japan. Dr. Tang C.-J. is supported by the 2017 Huxiang Provincial Scholar Program (2017RS3005). Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.cej.2019.02.034. References [1] B. Li, I. Boiarkina, W. Yu, H.M. Huang, T. Munir, G.Q. Wang, B.R. Young, Phosphorous recovery through struvite crystallization: challenges for future design, Sci. Total Environ. 648 (2019) 1244–1256. [2] A. Sinha, A. Singh, S. Kumar, S.K. Khare, A. Ramanan, Microbial mineralization of struvite: a promising process to overcome phosphate sequestering crisis, Water Res. 54 (2014) 33–43. [3] F. Zeng, Q. Zhao, W. Jin, Y. Liu, K. Wang, D. Lee, Struvite precipitation from anaerobic sludge supernatant and mixed fresh/stale human urine, Chem. Eng. J. 344 (2018) 254–261. [4] Z. Wu, S. Zou, B. Zhang, L. Wang, Z. He, Forward osmosis promoted in-situ formation of struvite with simultaneous water recovery from digested swine wastewater, Chem. Eng. J. 342 (2018) 274–280. [5] X. Xu, R. Xiao, D.D. Dionysiou, R. Spinney, T. Fu, Q. Li, Z. Wang, D. Wang, Z. Wei, Kinetics and mechanisms of the formation of chlorinated and oxygenated polycyclic aromatic hydrocarbons during chlorination, Chem. Eng. J. 351 (2018) 248–257. [6] Y. Luo, H. Li, Y. Huang, T. Zhao, Q. Yao, S. Fu, G. Zhou, Bacterial mineralization of struvite using MgO as magnesium source and its potential for nutrient recovery, Chem. Eng. J. 351 (2018) 195–202. [7] H. Huang, J. Liu, C. Xu, F. Gao, Recycling struvite pyrolysate obtained at negative pressure for ammonia nitrogen removal from landfill leachate, Chem. Eng. J. 284 (2016) 1204–1211. [8] T. Zhao, H. Li, Y. Huang, Q. Yao, Y. Huan, G. Zhou, Microbial mineralization of struvite: salinity effect and its implication for phosphorus removal and recovery,

5. Conclusion The struvite has the potential to enhance heavy metal precipitation under wide pH ranges. For the high-concentration heavy metal ions, the heavy metal precipitation rate in struvite contact group is higher than that of control group, especially under pH 6.0. As to the extremely lowconcentration heavy metals, the precipitation rate of higher than 95% is achieved by struvite contact group, while it is only less than 15% for control group. It has been found that the heavy metals’ precipitate on the struvite’s surface in the form of hydroxide, although there would be a small part participating in ion exchange with magnesium under low pH (6.0–7.0). The TEM observations upon copper hydroxide on struvite prove the possibility of heterogeneous nucleation and continuous growth of heavy metal hydroxide on struvite surface. Based on 68

Chemical Engineering Journal 365 (2019) 60–69

C. Tang et al.

37 (2009) 239–244. [30] A.A. Rouff, K.M. Juarez, Zinc interaction with struvite during and after mineral formation, Environ. Sci. Technol. 48 (2014) 6342–6349. [31] A. Uysal, Y.D. Yilmazel, G.N. Demirer, The determination of fertilizer quality of the formed struvite from effluent of a sewage sludge anaerobic digester, J. Hazard. Mater. 181 (2010) 248–254. [32] S. Muryanto, A.P. Bayuseno, Influence of Cu2+ and Zn2+ as additives on crystallization kinetics and morphology of struvite, Powder Technol. 253 (2014) 602–607. [33] A.A. Rouff, M.V. Ramlogan, A. Rabinovich, Synergistic removal of zinc and copper in greenhouse waste effluent by struvite, ACS Sustain. Chem. Eng. 4 (2016) 1319–1327. [34] A.A. Rouff, Sorption of chromium with struvite during phosphorus recovery, Environ. Sci. Technol. 46 (2012) 12493–12501. [35] C. Peng, L. Chai, Y. Song, X. Min, C. Tang, Thermodynamics, kinetics and mechanism analysis of Cu(II) adsorption by in-situ synthesized struvite crystal, J. Cent. South Univ. 25 (2018) 1033–1042. [36] L. Chai, C. Peng, X. Min, C. Tang, Y. Song, Y. Zhang, J. Zhang, M. Ali, Two-sectional struvite formation process for enhanced treatment of copper-ammonia complex wastewater, T. Nonferr. Metal. Soc. 27 (2017) 457–466. [37] C. Peng, L. Chai, C. Tang, X. Min, Y. Song, C. Duan, C. Yu, Study on the mechanism of copper-ammonia complex decomposition in struvite formation process and enhanced ammonia and copper removal, J. Environ. Sci. 51 (2017) 222–233. [38] C. Peng, L. Chai, C. Tang, X. Min, M. Ali, Y. Song, W. Qi, Feasibility and enhancement of copper and ammonia removal from wastewater using struvite formation: a comparative research, J. Chem. Technol. Biot. 92 (2017) 325–333. [39] S.K. Chawla, N. Sankarraman, J.H. Payer, Diagnostic spectra for XPS analysis of CuO-S-H compounds, J. Electron Spectrosc. 61 (1992) 1–18. [40] M.A. Peck, M.A. Langell, Comparison of nanoscaled and bulk nio structural and environmental characteristics by XRD, XAFS, and XPS, Chem. Mater. 24 (2012) 4483–4490. [41] J. Hong, G. Ying, W. Tao, Z. Pengli, Y. Shuhui, Y. Yan, F. Xianzhu, S. Rong, W. Chingping, Electrochemical fabrication of Ni(OH)2/Ni 3D porous compositefilms as integrated capacitive electrodes, RSC Adv. 5 (2015) 12931–12936. [42] D. Xu, X. Tan, C. Chen, X. Wang, Removal of Pb(II) from aqueous solution by oxidized multiwalled carbon nanotubes, J. Hazard. Mater. 154 (2008) 407–416. [43] L.Q. Jing, Z.L. Xu, X.J. Sun, J. Shang, W.M. Cai, The surface properties and photocatalytic activities of ZnO ultrafine particles, Appl. Surf. Sci. 180 (2001) 308–314. [44] M.C. Biesinger, B.P. Payne, A.P. Grosvenor, L.W.M. Lau, A.R. Gerson, R.S.C. Smart, Resolving surface chemical states in XPS analysis of first row transition metals, oxides and hydroxides: Cr, Mn, Fe, Co and Ni. Appl. Surf. Sci. 257 (2011) 2717–2730. [45] Y. Guorui, Y. Wei, W. Jianan, Y. Honghui, Fabrication and formation mechanism of Mn2O3 hollow nanofibers by single-spinneret electrospinning, CrystEngComm 16 (2014) 6907–6913. [46] Z. Jinyang, X. Lining, L. Minxu, Z. Lei, C. Wei, Interaction effect between Cr(OH)3 passive layer formation and inhibitor adsorption on 3Cr steel surface, RSC Adv. 5 (2015) 18518–18522. [47] P. Roberto, G. Ana P, F. Juan C, R. Juan C, B. Simón, Synthesis of Mn2O3 from Manganese Sulfated Leaching Solutions, Ind. Eng. Chem. Res. 55 (2016) 9468–9475. [48] S. Aksoy, Y. Caglar, S. Ilican, M. Caglar, Sol-gel derived Li-Mg co-doped ZnO films: preparation and characterization via XRD, XPS, FESEM. J. Alloy. Compd. 512 (2012) 171–178. [49] M.M. Ba-Abbad, A.A.H. Kadhum, A.B. Mohamad, M.S. Takriff, K. Sopian, Visible light photocatalytic activity of Fe3+ doped ZnO nanoparticle prepared via sol-gel technique, Chemosphere 91 (2013) 1604–1611. [50] S. Wemer, M. James J, Aquatic Chemistry, 3rd edition, Wiley-Interscience, New York, 1996. [51] S. Wemer, Chemistry of the Solid-Water Interface, Wiley-Interscience, New York, 1992. [52] B. John C, An Introduction to Interfaces and Colloids, World Scientific, Singapore, 2010.

Chem. Eng. J. 358 (2019) 1324–1331. [9] H. Arslanoglu, Adsorption of micronutrient metal ion onto struvite to prepare slow release multielement fertilizer: copper(II) doped-struvite, Chemosphere 217 (2018) 393–401. [10] L. Wei, T. Hong, X. Li, M. Li, Q. Zhang, T. Chen, New insights into the adsorption behavior and mechanism of alginic acid onto struvite crystals, Chem. Eng. J. 358 (2019) 1074–1082. [11] S.P. Wei, F. van Rossum, G.J. van de Pol, M.H. Winkler, Recovery of phosphorus and nitrogen from human urine by struvite precipitation, air stripping and acid scrubbing: a pilot study, Chemosphere 212 (2018) 1030–1037. [12] H.N. Bischel, S. Schindelholz, M. Schoger, L. Decrey, C.A. Buckley, K.M. Udert, T. Kohn, Bacteria Inactivation during the Drying of Struvite Fertilizers Produced from Stored Urine, Environ. Sci. Technol. 50 (2016) 13013–13023. [13] H. Huang, L. Huang, Q. Zhang, Y. Jiang, L. Ding, Chlorination decomposition of struvite and recycling of its product for the removal of ammonium-nitrogen from landfill leachate, Chemosphere 136 (2015) 289–296. [14] Z. Ye, Y. Deng, Y. Lou, X. Ye, J. Zhang, S. Chen, Adsorption behavior of tetracyclines by struvite particles in the process of phosphorus recovery from synthetic swine wastewater, Chem. Eng. J. 313 (2017) 1633–1638. [15] H. Huang, J. Liu, J. Xiao, P. Zhang, F. Gao, Highly Efficient Recovery of Ammonium Nitrogen from Coking Wastewater by Coupling Struvite Precipitation and Microwave Radiation Technology, ACS Sustain. Chem. Eng. 4 (2016) 3688–3696. [16] X. Wang, A. Selvam, M. Chan, J.W.C. Wong, Nitrogen conservation and acidity control during food wastes composting through struvite formation, Bioresource Technol. 147 (2013) 17–22. [17] M.T. Munir, B. Li, I. Boiarkina, S. Baroutian, W. Yu, B.R. Young, Phosphate recovery from hydrothermally treated sewage sludge using struvite precipitation, Bioresour. Technol. 239 (2017) 171–179. [18] M. Everaert, F. Degryse, M.J. McLaughlin, D. De Vos, E. Smolders, Agronomic Effectiveness of Granulated and Powdered P-Exchanged Mg-Al LDH Relative to Struvite and MAP, J. Agr. Food Chem. 65 (2017) 6736–6744. [19] K. Yetilmezsoy, F. Ilhan, E. Kocak, H.M. Akbin, Feasibility of struvite recovery process for fertilizer industry: a study of financial and economic analysis, J. Clean. Prod. 152 (2017) 88–102. [20] Y. Lou, X. Ye, Z. Ye, P. Chiang, S. Chen, Occurrence and ecological risks of veterinary antibiotics in struvite recovered from swine wastewater, J. Clean. Prod. 201 (2018) 678–685. [21] R. Taddeo, M. Honkanen, K. Kolppo, R. Lepisto, Nutrient management via struvite precipitation and recovery from various agroindustrial wastewaters: process feasibility and struvite quality, J. Environ. Manage. 212 (2018) 433–439. [22] A. Muhmmod, S. Wu, J. Lu, Z. Ajmal, H. Luo, R. Dong, Nutrient recovery fromanaerobically digested chicken slurry via struvite: performance optimization and interactions with heavy metals and pathogens, Sci. Total Environ. 635 (2018) 1–9. [23] Y. Lou, Z.L. Ye, S. Chen, Q. Wei, J. Zhang, X. Ye, Influences of dissolved organic matters on tetracyclines transport in the process of struvite recovery from swine wastewater, Water Res. 134 (2018) 311–326. [24] I. Merino-Jimenez, V. Celorrio, D.J. Fermin, J. Greenman, I. Ieropoulos, Enhanced MFC power production and struvite recovery by the addition of sea salts to urine, Water Res. 109 (2017) 46–53. [25] D.S. Perwitasari, S. Muryanto, J. Jamari, A.P. Bayuseno, Kinetics and morphology analysis of struvite precipitated from aqueous solution under the influence of heavy metals: Cu2+, Pb2+, Zn2+, J. Environ. Chem. Eng. 6 (2018) 37–43. [26] J.H. Kim, B.M. An, D.H. Lim, J.Y. Park, Electricity production and phosphorous recovery as struvite from synthetic wastewater using magnesium-air fuel cell electrocoagulation, Water Res. 132 (2018) 200–210. [27] A. Muhmood, J. Lu, R. Kadam, R. Dong, J. Guo, S. Wu, Biochar seeding promotes struvite formation, but accelerates heavy metal accumulation, Sci. Total Environ. 652 (2018) 623–632. [28] H. Huang, B. Li, J. Li, P. Zhang, W. Yu, N. Zhao, G. Guo, B. Young, Influence of process parameters on the heavy metal (Zn2+, Cu2+ and Cr3+) content of struvite obtained from synthetic swine wastewater, Environ. Pollut. 245 (2019) 658–665. [29] R.L. Radis Steinmetz, A. Kunz, V.L. Drensler, E.M. de Moraes Flores, A.F. Martins, Study of metal distribution in raw and screened swine manure. clean-soil air, Water

69