Bone char with antibacterial properties for fluoride removal: Preparation, characterization and water treatment

Journal of Environmental Management 201 (2017) 277e285

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Research article

Bone char with antibacterial properties for fluoride removal: Preparation, characterization and water treatment
ndez-Montoya a, *, Francisco J. Cervantes b, Lorena Delgadillo-Velasco a, Virginia Herna
n c, Diana Lira-Berlanga a Miguel A. Montes-Mora
gico de Aguascalientes, Av. Adolfo Lo
pez Mateos No. 1801 Ote., C.P. 20256, Aguascalientes, Ags., Mexico Instituto Tecnolo
n de Ciencias Ambientales, Instituto Potosino de Investigacio
n Científica y Tecnolo
gica (IPICyT), Camino a la Presa San Jos
Divisio e 2055, Col. Lomas 4a.
n, San Luis Potosí, SLP, 78216, Mexico Seccio c
n, INCAR-CSIC, Apartado 73, E-33080, Oviedo, Spain Instituto Nacional del Carbo a

b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 10 March 2017 Received in revised form 15 May 2017 Accepted 18 June 2017 Available online 1 July 2017

In the present work, it was established a new method for the preparation of bone chars with a double purpose, i.e., the removal of fluoride from water and the antibacterial character. These adsorbents were obtained by doping a commercial bone char with Ag using different reagents. The optimal conditions for the enrichment with silver were established by following the Taguchi method and using as response variable the removal of fluoride from water. Optimal bone chars were thus prepared and they were characterized using FT-IR spectroscopy, SEM/EDX analysis, adsorption isotherms of N2 at
196  C and Xray diffraction. All adsorbents were used in the removal of fluoride from water and the antibacterial character was assessed using the technique of total viable count employing standard solutions of Escherichia coli and drinking water. Results clearly indicated that doping of bone chars with silver provides with suitable antibacterial properties, however the fluoride adsorption capacity was not affected by the presence of Ag on the carbon surface. © 2017 Elsevier Ltd. All rights reserved.

Keywords: Antibacterial character Bone char Fluoride Silver Water

1. Introduction According to World Health Organization (WHO), fluoride is considered as a contaminant in water when its concentration exceeds the limit of 1.5 mg/L (Wang et al., 2017). Specifically, water consumption with a fluoride concentration above this limit for prolonged periods may have harmful health effects, such as dental fluorosis, skeletal fluorosis, muscle fiber degeneration and others (Mohapatra et al., 2009; Yadav et al., 2013; Hern
andez-Montoya et al., 2003; Bhatnagara et al., 2011). Fluoride can be found naturally in groundwater due to the slow dissolution of rocks and minerals, which contain it, for example: sellaite (MgF2), fluorspar (CaF2) and cryolite (Na3AlF6) (Mohapatra et al., 2009). Fluoride can also contaminate water sources through anthropogenic activities (Yadav et al., 2013), such as the use of pesticides and fertilizers
mez et al., 2013) or through the containing fluoride (Tovar-Go discharge of industrial effluents into water bodies (Mohapatra et al., 2009; Bhatnagara et al., 2011; Kameda et al., 2015). In many

* Corresponding author.
ndez-Montoya). E-mail address: [email protected] (V. Herna http://dx.doi.org/10.1016/j.jenvman.2017.06.038 0301-4797/© 2017 Elsevier Ltd. All rights reserved.

countries, groundwater is the main source of water supply for human consumption (Mohapatra et al., 2009; Bhatnagara et al., 2011). Currently, it is known that twenty six countries worldwide report high fluoride content in water (Yadav et al., 2013). Particularly in Mexico, the states of San Luis Potosi, Durango, Aguascalientes, Zacatecas and Jalisco, among others, have this problem. In Aguascalientes, 43.7% of the main sources of water supply have a fluoride concentration higher than 1.5 mg/L and some regions show
ndez-Montoya et al., 2003). values even higher than 10 mg/L (Herna In response to this problem, numerous studies have focused on the removal of fluoride from water. The treatment methods include membrane technologies (reverse osmosis, nanofiltration, dialysis, electro-dialysis, etc.) and adsorption (Mohapatra et al., 2009; Emamjomeh and Sivakumar, 2009). Although, membrane technologies can successfully reduce fluoride concentration in water to acceptable levels, adsorption, which is a technology that takes advantage of the surface composition of the adsorbents to retain fluoride from water, is considered the best alternative, due to its generally greater accessibility and lower cost (Mohapatra et al.,
mez et al., 2013). Adsorbents used for the removal 2009; Tovar-Go of fluoride from water are activated alumina (Mohapatra et al.,

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2009; Bhatnagara et al., 2011; Leyva-Ramos et al., 1999), alumina impregnated with lanthanum hydroxide (La(OH)3) (Leyva-Ramos et al., 1999), rare earth oxides (Mohapatra et al., 2009), activated clay (Mohapatra et al., 2009; Tchomgui-Kamga et al., 2010), carbonaceous materials (Mohapatra et al., 2009; Tchomgui-Kamga et al., 2010; Leyva-Ramos et al., 1999; Yadav et al., 2013), solid industrial wastes as red mud, spent catalysts and fly ash (Mohapatra et al., 2009), zeolites (Mohapatra et al., 2009; Leyva-Ramos et al., 1999), biosorbents (Leyva-Ramos et al., 1999; V
azquez-Guerrero et al., 2016; Ramanaiah et al., 2007), alum-impregnated activated alumina (Mohapatra et al., 2009; Leyva-Ramos et al., 1999), aluminum impregnated chitosan (Leyva-Ramos et al., 1999), as well as activated rice straw and fishbone charcoal (Mohapatra et al., 2009; Leyva-Ramos et al., 1999). Carbonaceous materials are one of the best options because they offer good results. There are different types of carbonaceous adsorbents with different performance in the fluoride uptake from water: bone char > coal charcoal > wood charcoal > carbon black > petroleum coke (Mohapatra et al., 2009). Bone char is considered a carbon material although is mainly composed of hydroxyapatite (Ca5(PO4)3(OH)) and this material has a high fluoride uptake capacity. During adsorption an ion exchange between hydroxyl ions of hydroxyap
mez et al., 2013; atite and fluoride ion from water occurs (Tovar-Go Mohan et al., 2014); the calcium in hydroxyapatite plays also an important role in the process through the formation of fluo
mez et al., 2013; Tchomgui-Kamga roapatite (Ca5(PO4)3F) (Tovar-Go et al., 2010). Nevertheless, bone char is a highly biocompatible material with environmental bacteria (McEvoy et al., 2013; Park and Jang, 2003; Pei et al., 2013), which can adhere and easily reproduce on this material, making it a pollutant (Park and Jang, 2003), therefore complicating its use as packing material in drinking water purifying systems. In this context, the use of bone char for the removal of fluoride from water is an economic and efficient alternative for developing communities in Mexico (Aguascalientes). For this reason, it is interesting to prepare new chars with antibacterial properties with the purpose to use them in water purification systems (fixed bed columns) during several cycles avoiding bacterial growth. Recently, the modification of different materials with silver salts has also been reported to take advantage of the antibacterial properties of silver. For example, activated carbon fiber impregnated with AgNO3 was used for the purification of water. In this case, a strong antibacterial activity and an inhibitory effect was found on the growth of Escherichia coli and Staphylococcus aureus (Park and Jang, 2003). In addition, carbon nanotube coating with silver nanoparticles was used in drinking water filtration, recording an antibacterial effect against Escherichia coli (Booshehri et al., 2013). In this context, various studies point out the use silver to add antibacterial properties to the adsorbents used for the removal of specific contaminants in both air and water systems (mostly dyes) and it report including the synthesis nanoparticles of silver to confer antibacterial properties at selected materials (Khatoon et al., 2015; Yang et al., 2004). However, to our knowledge, there are not studies describing the modification of bone char with silver for fluoride removal from water. Thus, the main purpose of this study was to modify a bone char with silver compounds to reduce the amount of bacteria present in water while removing fluoride. In this work, three commercial products with low concentration of Ag and low cost were selected. These products are used for the disinfection of fruits, vegetables and water. The optimal conditions of modification of carbons were obtained using the Taguchi method employing an L9 orthogonal array, considering as a response variable the fluoride adsorption from water in batch adsorption systems. Additionally, the stability of Ag on the modified carbons was monitored after several cycles of washing. The Ag washing

procedure was carried out until the Ag concentration was not detectable in the wash water and, consequently, it was less than 4.6  10
7 M (limit of concentration in bottled purified water according with Mexican regulations: NOM-041-SSA1-1993). Finally, the adsorbents obtained were characterized using different analytical techniques and the antibacterial effect of silver was studied using microbiological techniques. 2. Materials and methods 2.1. Preparation of antibacterial bone chars CARMEX bone char (BC) from Carbones Mexicanos Company (Mexico) was used as precursor in the preparation of antibacterial carbons. According to specifications from supplier, the composition of the material is tricalcium phosphate (80e85%) and carbon (10e15%). Preparation of antibacterial materials comprised two steps. The first step included a pre-treatment of BC, in which particles of BC were milled and sieved to obtain a particle size of ~0.7 mm. Afterwards, particles were washed with deionized water until constant pH and finally, they were dried at 110  C for 24 h. The second step comprised the impregnation of BC particles with a colloidal silver (Sigma-Aldrich, CAS Number 7440-22-4) solution followed by a thermal treatment. Modification was made according to the Taguchi method employing an L9 orthogonal array and considering the removal of fluoride as a response variable. Studied factors were the concentration of colloidal silver (Factor A), the impregnation temperature (Factor B), mass to volume ratio (Factor C) and the temperature of thermal treatment (Factor E). Levels of each factor are shown in Table 1. The modified bone chars were finally washed with deionized water for several cycles to remove excess of colloidal silver until the concentration of Ag in the washed water was less than 4.6  10
7 M (limit of Ag concentration in purified water according to Mexican regulations). Silver concentration was determined spectrophotometrically using a Hach DR5000 spectrophotometer employing the colorimetric method 8120 of Hach procedures. BC was also modified with two types of commercial products used in the disinfection of vegetables, M and G; which contain silver as active substance. Modifications were performed according to L9 orthogonal array of the Taguchi method (See Table S1 in supplementary information) and modified samples were washed using the procedure describe above (See Table S2 in supplementary information). In this case, the concentration used in the experimental design was delimited by the initial Ag concentration of products, which was 0.032 M for both commercial products. 2.2. Physicochemical and textural characterization of bone chars Samples of bone chars with and without modification were characterized using different analytical techniques. Functional groups in bone chars were determined by IR spectroscopy using a FT-IR spectrometer (Thermo Scientific NICOLET-8700) equipped with an ATR accessory. Also, morphology and surface composition of selected samples were obtained by SEM/EDX analyses using a FESEM system (Quanta FEG 650, FEI). Solid particles were dispersed on a graphite adhesive tab placed on an aluminum stub and no further coating was required. Additionally, bone chars were analyzed by X-ray diffraction and their diffraction patterns were recorded in a Bruker D8 Advance diffractometer equipped with a Cu € bel mirror Ka X-ray source operated at 40 kV and 40 mA. A single Go configuration was used to monochromatise and focus X-rays on samples, attaining highly efficient parallel beam geometry. Diffraction data were collected by step scanning with a step size of 0.02 2q and a scan step time of 5 s.

L. Delgadillo-Velasco et al. / Journal of Environmental Management 201 (2017) 277e285 Table 1 L9 orthogonal array of the Taguchi method used in the modification of BC employing colloidal silver (Ag) as modifying agent. Factors Experiment (Carbon B: A: Concentration C: Mass to D: Temperature of code) of colloidal silver Impregnation volume thermal treatment temperature ( C) (M) ratio  ( C) Ag-C-1 Ag-C-2 Ag-C-3 Ag-C-4 Ag-C-5 Ag-C-6 Ag-C-7 Ag-C-8 Ag-C-9

0.125 0.125 0.125 0.250 0.250 0.250 0.500 0.500 0.500

30 50 100 30 50 100 30 50 100

1:2 1:3 1:4 1:3 1:4 1:2 1:4 1:2 1:3

300 400 500 500 300 400 400 500 300

Finally, the principal textural parameters of bone chars were determined from nitrogen adsorption isotherms at
196  C using an automatic Micromeritics ASAP 2020 analyzer. Prior to measurement, samples were outgassed overnight by heating at 300  C under vacuum. The experimental data of adsorption isotherms were analyzed using the appropriated models and the selected textural parameters such as specific surface, total pore volume, micropore volume, etc., were determined.

2.3. Adsorption of fluoride on bone chars Adsorption of fluoride on bone chars, with and without modification was studied using two types of adsorptions tests. Test 1 was

279

used to find the optimum conditions for preparing modified bone chars according to the Taguchi method. This Test 1 was carried out using intermittent systems under constant stirring (150 rpm) at 30  C and using an initial fluoride concentration of 20 mg/L. Samples with and without modification (0.05 g) were mixed with 5 mL of fluoride solution for 72 h until equilibrium was achieved. Fluoride solution was prepared by dissolving sodium fluoride (SigmaAldrich, analytical grade) with deionized water and the concentration of fluoride in the initial and equilibrium solutions was determined by ion selective electrode according with the Standard Methods for the Examination of Water and Wastewater. Test 2 was carried out with the optimum bone chars for fluoride removal, according to the Taguchi method. For these materials, the fluoride adsorption isotherms were obtained under the following experimental conditions: batch systems with constant agitation (150 rpm), equilibrium time of 72 h, temperature 30  C, mass to volume ratio of 10 g/L. Additionally, solutions with different initial fluoride concentrations were used in the range from 5 to 50 mg/L. 2.4. Antibacterial effect of bone chars Antibacterial character of the best modified bone chars, as determined by the Taguchi method (optimum), and fresh, unmodified bone char (BC) was determined using batch and continuous systems. For batch systems, it was used a bacterial suspension (Standard solution 1) obtained from 10
10 dilution of a stock solution, which originally contained 1 colony forming unit (CFU) of Escherichia coli (E. coli) in 0.1 L of distilled water. The E. coli suspension was taken from a pure culture obtained from a mixed culture of coliform group of bacteria from “El Cedazo” wastewater treatment plant located in Aguascalientes (Mexico). Experimental

5. Water outlet from the packed-bed column

1. Water supply

O-G O-M 3. Packed-bed column

O-Ag

2. Container

BC

4. Water inlet to the packed-bed column

Fig. 1. Packed-bed columns system employed in the study for testing the antibacterial character of bone chars (BC, O-Ag, O-M and O-G).

L. Delgadillo-Velasco et al. / Journal of Environmental Management 201 (2017) 277e285

a)

b)

100

100

90

90

80

80

80

70

70

70

60

60

60

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50

40

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40

30

30

30

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20

10

10

10

0

0

0

BC BC-T M-1 M-2 M-3 M-4 M-5 M-6 M-7 M-8 M-9

90

BC BC-T Ag-C-1 Ag-C-2 Ag-C-3 Ag-C-4 Ag-C-5 Ag-C-6 Ag-C-7 Ag-C-8 Ag-C-9

Fluoride removal (%)

100

c)

BC BC-T G-1 G-2 G-3 G-4 G-5 G-6 G-7 G-8 G-9

280

Sample Fig. 2. Fluoride removal of bone chars prepared following a L9 orthogonal array of the Taguchi method and using as modifying agents: colloidal silver (a), M (b) and G (c).

conditions for batch tests were the following: 20 mL of bacterial suspension (dilution 10
10) were mixed with 0.2 g of bone char for 15 min at ambient temperature (25  C) and finally, the treated solution was decanted. Then, both the supernatant of the treated solution and a sample of the initial bacterial suspension (dilution 10
10) were analyzed using the technique of total viable count (TVC). TVC was carried out using 1 mL of sample (solution) and Petri dishes with 15 mL of standard methods agar (BIOXON) and finally, they were incubated at 35 ± 2  C for 48 h, prior to quantification. On the other hand, Fig. 1 shows the schematic representation of the system used in the continuous adsorption tests. The system has the following components: (1) water supply; (2) reservoir of water (container); (3) packed bed columns and water inlets and water outlets (4 and 5). Each column was packed with 0.4 g of bone char (with or without modification). Through all the columns, a flow of drinking water of 0.33 mL/min was kept constant for 11 or 17 days. Then, samples of water were analyzed by the TVC technique (see above). Also, the same continuous system was used under the same experimental conditions and a bacterial suspension of E. coli (Standard solution 2), which contain 3 CFU (obtained from the pure culture above mentioned) in 10 L of distilled water (instead of

drinking water). Finally, both the treated water and bacterial suspension were analyzed using the TVC method with the following experimental conditions: 1 mL of water sample, Petri dishes with 15 mL of standard methods agar, incubation at 35 ± 2  C for 48 h, prior to quantification. 3. Results and discussion 3.1. Fluoride adsorption capacities of modified bone chars The fluoride removal ability of different bone chars modified with Ag reagents (see Section 2.1) is shown in Fig. 2. This ability is expressed as the % of fluoride removed from the 20 mg/L initial solutions, after 72 h of exposure (see Test 1 conditions, Section 2.3). In general, silver enriched bone chars showed significantly higher removal amounts (~60%) than the control test carried out with BC (ca. 40%). Specifically, samples modified in experiments 2, 3, 4 and 6, 7, 8 of the experimental design described in Table 1 show the higher a removal percentages, in the range of 62e64%. This behavior was also similar when bone chars modified using M and G reagents were tested (Fig. 2b and c), with removal percentages ranging from 44 to 59% for M-modified bone chars and from 60 to

Table 2 Textural parameters of bone chars with and without modification with silver solutions, calculated from adsorption isotherms of N2 at
196  C. Sample BC O-Ag O-M O-G a b c d e f

a

SBET (m2/g) 65 59 57 77

b

Vt (cm3/g) 0.098 0.109 0.095 0.122

SBET: BET surface area. Vt: Total pore volume. VDR: DubinineRadushkevich micropore volume. VMes ¼ Vt
VDR. Microporous (%) ¼ (VDR/Vt)100. Mesoporous (%)¼ (VMes/Vt)100.

c

VDR (cm3/g) 0.029 0.025 0.027 0.026

d

VMes (cm3/g) 0.069 0.084 0.068 0.096

e

Microporous (%) 30 23 28 21

f

Mesoporous (%) 70 77 72 79

L. Delgadillo-Velasco et al. / Journal of Environmental Management 201 (2017) 277e285

Fig. 3. EDX analysis and SEM images (600  ) of BC (a,b), O-Ag (c,d), O-M (e,f) and O-G (g,h) bone chars.

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62% for G-modified bone chars. Additionally, it is clear that modified samples obtained from conditions of experiments 1, 5 and 9 yielded the lowest percentage of removal (38e45%), regardless the Ag reagent used. These bone chars were prepared using the lowest temperature during the thermal treatment (300  C), which would suggest that higher temperatures are required to incorporate Ag to the surface of the bone char. In this context, the adsorption results were analyzed in terms of a signal-to-noise ratio (S/N) approach and adopting the “larger the better” criteria in order to maximize
lez and the removal of fluoride by the bone chars (Elizalde-Gonza
ndez-Montoya, 2009; Dura
n-Jime
nez et al., 2014). Fig. S1 Herna shows the effects graphs of the three modifying agents (See Supplementary information). The best conditions to prepare efficient bone chars for the removal of fluoride using modification with silver solutions are A1, B1, C3, D2 for colloidal silver reagent, A2, B1, C2, D2 for M reagent and A1, B2, C1, D2 for G reagent. It is relevant to mention that for the three modifying reagents (colloidal silver, M and G) the temperature of the thermal treatment carried out after the impregnation is the same (Factor D, level 2: 400  C). This factor has the highest effect in the removal of fluoride according to the analysis of the variance of the adsorption results (see Table S3 in supplementary information). In this context, a new sample labelled BC-T was prepared by thermal treatment of BC at 400  C without Ag impregnation, with the purpose of confirming if the increase in the removal percentage of fluoride is due to the addition of Ag on the carbon surface or simply to thermal treatment of the bone chars. The fluoride adsorption results of BC-T are also shown in Fig. 2. The samples modified with Ag solutions and thermally treated have a similar removal percentage than the BC-T sample, i.e., silver deposited on the surface of the carbons seems to play a little role in the removal of fluoride. This conclusion agrees with the analysis of variance of the adsorption results (Table S3 in supplementary information). A similar influence of the thermal treatment on bovine bone chars on their final performance in fluoride removal has been recently reported (Nigri et al., 2017). A general fluoride adsorption mechanism can be thus established to be linked to the presence of hydroxyapatite, which is the principal component of bone chars studied in this work (see characterization results in section 3.2):

Ca10 ðPO4 Þ6 ðOHÞ2 þ 2F
/ Ca10 ðPO4 Þ6 F2 þ 2OH


information) shows those adsorption isotherms. Results are congruent with data shown in Fig. 2, where it is possible to observe that the optimal bone chars have an adsorption capacity almost 20% higher (~1.65 mg/g) than the sample without modification or thermal treatment. 3.2. Characterization of selected bone chars Optimal bone chars (O-Ag, O-M and O-G) and the original BC sample were characterized to identify changes on their surface due to the modification with silver solutions. Fig. S4 shows the adsorption isotherms of N2 at
196  C of the samples. According to the IUPAC classification, all isotherms are type IV, which are characteristic of mesoporous solids (See Supporting information). In general, all bone chars have low specific surface areas (SBET) (Table 2) and no significant change of the SBET of BC was observed after the modification. Total pore volumes are also small and, according to the isotherms shape already discussed, all bone chars are essentially mesoporous materials, with mesoporosity percentages ranging from 70% to 80% of the total pore volume. As for the SBET values, changes in the rest of the textural parameters after the modification of the BC sample are, in general, of little significance. This observation was corroborated by a variance analysis of one factor where null hypothesis (Ho) was “the chemical agent used in the modification of bone char does not produce a significant change in their textural parameters”. In this case, Ho was accepted. Morphology and surface composition of the bone chars were determined by SEM/EDX analysis, and the results obtained are

a)

b) (1)

This removal mechanism has been proposed by some authors reporting either the adsorption of fluoride from water on bone chars or the regeneration of this type of adsorbent (Kaseva, 2006; Medellin-Castillo et al., 2014; Nigri et al., 2017). Particularly, in the present work the samples saturated with fluoride were characterized by SEM/EDX analysis and the results confirm the presence of fluoride on the carbon surface. For example, Fig. S2 in supplementary information shows the presence of F (3.04 wt%) on the surface of BC saturated with an initial concentration of fluoride of 50 mg/L. As for the increment on the fluoride removal capacity of BC after the thermal treatment at 400  C, there is no clear explanation. It could be related to the irreversible loss of lattice water that is known to happen between 200 and 400  C, which causes changes in hydroxyapatite lattice dimensions (Liao et al., 1999). Also, rearrangement of the structural hydroxyl ions might occur as they should migrate to the surface prior to hydroxyapatite dehydroxylation that normally occurs at temperatures around 850  C (Liao et al., 1999). Finally, with the optimum conditions for the three Ag reagents, three optimum bone chars were prepared, namely O-Ag (colloidal silver), O-M and O-G (See Fig. S1 in supplementary information). The optimal bone chars were used to obtain the fluoride adsorption isotherms with the purpose to determine the maximum adsorption capacity (Test 2, see Section 2.3). Fig. S3 (in supplementary

Transmittance (%)

282

c)

d) 2915 3427

2015 1456 1418

869 1039

603

4000 3500 3000 2500 2000 1500 1000

565

500

-1

Wavenumber (cm ) Fig. 4. FT-IR spectra of the O-G (a), O-M (b), O-Ag (c) and BC (d) bone chars.

L. Delgadillo-Velasco et al. / Journal of Environmental Management 201 (2017) 277e285

1200 a) BC * Ca5(PO4)3(OH)

800 600

*

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*

Intensity (a.u.)

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600

° Ag

400

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° Ag

*

°* * * °* *

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°*

d)

O-G *Ca5(PO4)3(OH)

500

° Ag

*

* * * * ° *°

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10 20 30 40 50 60 70 80 90

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O-Ag * Ca5(PO4)3(OH)

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2-Theta - Scale Fig. 5. XRD patterns of BC (a), O-Ag (b), O-M (c) and O-G (d) bone chars.

presented in Fig. 3. In this case, all particles have a globular form with a heterogeneous surface and little macroporosity. Additionally, results of EDX indicated that BC is constituted principally by C, O, P and Ca, as expected from a mixed composition of residual carbon and hydroxyapatite (Ca5(PO4)3(OH)), which is the principal component of this bone char according to previous studies (Tovar
mez et al., 2013). These results agree with information obtained Go by FT-IR spectroscopy (Fig. 4), where the characteristic peaks of hydroxyapatite are evident in BC and no significant change is observed after the modification of the original bone char. The peaks observed in FT-IR spectra of all bone chars shown in Fig. 4 correspond to organic and inorganic phases of hydroxyapatite (RojasMayorga et al., 2013; Rojas-Mayorga et al., 2015; Ahmed et al., 2015; Ooi et al., 2007; Arsad et al., 2011; Patela et al., 2015; Joschek et al., 2000; Leyva-Ramos et al., 2015). Specifically, peaks at 3427 cm
1 can be assigned to the stretching vibration of O-H of
mez et al., 2013; Rojas-Mayorga et al., hydroxyl groups (Tovar-Go 2013; Rojas-Mayorga et al., 2015; Arsad et al., 2011); peak at 2915 cm
1 is related to the stretching vibration of C-H of methyl groups and signals at 565e603, 1039 and 2015 cm
1 are characteristics of stretching and bending vibrations of PO3
groups 4
mez et al., 2013; Ahmed et al., 2015; Ooi et al., 2007; (Tovar-Go Arsad et al., 2011). Additionally, the presence of Ag was observed on the surface of all optimal bone chars, especially on the sample obtained with colloidal silver (See Fig. 3ced). This information was corroborated by X-ray diffraction (See Fig. 5), where it was possible to identify the crystalline structure of metallic silver (Ag0) on the optimal bone chars (obtained by modification of BC with silver solutions). These

results are congruent with the EDX results, where the peaks corresponding to Ag are more evident in the sample obtained by modification with colloidal silver (O-Ag), due to the concentration used during the modification (0.125 M), which was much higher than that present in samples O-M (0.016 M) and O-G (0.008 M). 3.3. Antibacterial character of the bone chars The antibacterial character of optimal bone chars and BC (the original sample) was determined by tests in batch and continuous systems. Table 3 shows the obtained results in both systems and using two types of water (standard solution and drinking water). OAg and O-M samples showed an antibacterial character because no CFU were observed for the four studied conditions in contrast with the original bone char BC. Also, it is relevant to mention that when drinking water was tested, all optimal bone chars (including O-G) presented an antibacterial character, which was reflected on the CFU values (cero in all cases). On other hand, when the standard bacterial suspensions (either solution 1 in the batch system or solution 2 in the continuous system) were used in the experiments, only O-Ag and O-M showed an antibacterial character with respect to E. coli. This behavior should be related with the concentration of Ag on the surface of the bone char, which was lower for O-G (1.64 %w) in comparison with O-M (2.67 %w) and O-Ag (21.92 %w), as determined in the EDX analyses. Considering the conditions studied in this work, it is possible to establish a treatment mechanism for drinking water: BC can serve as filtering material because the initial bacterial concentration (55

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or 83 CFU/ml) decreased when water was treated with BC obtaining a decrease of 12 or 3 CFU/ml for 11 or 17 days, respectively. This behavior is also observed for O-Ag, O-M and O-G, because they are acting as filtering materials, but additionally, as antibacterial support because no CFU were detected in the treated water during 11 or 17 days. Fig. 6 shows the formation of colonies only in the initial water and the water treated with BC (see Fig. 6a and b), corroborating the antibacterial character of the optimal bone chars, which contain Ag on their surface (See Fig. 6cee). These results are congruent with data reported in the literature because silver has an antibacterial character (Nishioka et al., 2004), principally for bacteria, such as E. coli (Park and Jang, 2003; Tuan et al., 2011; Yu et al., 2014). Additionally, it is very important to note that this work is the first study that is reporting the synthesis, characterization and application of bone chars with a double purpose: as adsorbent for the removal of fluoride from water and as antibacterial filter. The obtained results indicate that with this new method of preparation of materials, it is possible to design one adsorption system, packed with the developed bone chars, for the removal of fluoride from

water avoiding the growth of microorganisms during repeated cycles of use. 4. Conclusions In the present work, it was demonstrated that it is possible to prepare adsorbents with antibacterial character for the removal of fluoride from water, using bone char as precursor material and silver solutions as modifying agent. According to the characterization results, the antibacterial effects of the adsorbents are related with the presence of metallic silver (Ag0) on their surface, which was fixed on the bone char during the modification process. The temperature of the thermal treatment at which samples were submitted after the impregnation step was found to be crucial to obtain an adequate deposition of Ag on the surface of the resulting bone chars. This conclusion can be sustained by the analysis of variance of Taguchi method, which indicates that thermal treatment (Factor D) has more effect on the modification of the original bone char and consequently, on the removal of fluoride from water.

Table 3 Number of colonies quantified in the standard solution of Escherichia coli, drinking water and the water treated with bone chars with and without modification with silver solutions, using batch and continuous systems. Sample

Batch system a

Initial solution Water treated with Water treated with Water treated with Water treated with a b

BC O-Ag O-M O-G

Continuous system

Solution 1

b

Drinking water

Solution 2

15 min CFU/ml

11 days CFU/ml

17 days CFU/ml

1 day CFU/ml

1 1 0 0 2

55 12 0 0 0

83 3 0 0 0

2 15 0 0 1

Standard solution 1 of Escherichia coli. Standard solution 2 of Escherichia coli.

Fig. 6. Test plates for colony counting using drinking water from continuous treated during 11 days, measured by TVC method, for initial (a), BC (b), O-Ag (c), O-M (d) and O-G (e) samples.

L. Delgadillo-Velasco et al. / Journal of Environmental Management 201 (2017) 277e285

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