Polydopamine microcapsules from cellulose nanocrystal stabilized Pickering emulsions for essential oil and pesticide encapsulation

Colloids and Surfaces A 570 (2019) 403–413

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Polydopamine microcapsules from cellulose nanocrystal stabilized Pickering emulsions for essential oil and pesticide encapsulation

T

Chunxia Tanga, Yingzhan Lib, Jason Puna, Ahmed Sameh Mohamed Osmana, Kam C. Tama,

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a

Department of Chemical Engineering, Waterloo Institute for Nanotechnology, University of Waterloo, 200 University Avenue, Waterloo, ON N2L 3G1, Canada Key Lab of Science & Technology of Eco-textile, Ministry of Education, College of Chemistry, Chemical Engineering and Biotechnology, Donghua University, Shanghai 201620, China

b

GRAPHICAL ABSTRACT

ARTICLE INFO

ABSTRACT

Keywords: Polydopamine microcapsules Pickering emulsions Cellulose nanocrystals Pesticides encapsulation Essential oil Slow release

The development of microcapsule for crop protection is highly desirable as it reduces environmental pollution, ensures safe handling of pesticides, protects active ingredients (AI) from early degradation as well as increases pest control efficiency. Polydopamine (PDA) microcapsule possesses many attractive properties, such as good adhesion, biodegradability, UV resistance, as well as facile preparation process. However, most preparation methods of PDA capsules rely on either etching the hard templates using harsh acid/solvent or on soft templates containing toxic solvents/emulsifiers, that are not environmentally friendly. In this study, we developed PDA microcapsules templated by Pickering emulsions stabilized by cinnamoyl chloride modified cellulose nanocrystals for essential oil and pesticides encapsulation. The essential oil (turpentine) functions as botanical pesticides as well as solvent for the herbicide (model drug 2,4-D) resulting in high AI encapsulation efficiency. Such system minimizes the use of toxic solvent and synthetic surfactant, improves AI encapsulation efficiency, displays multi-AI encapsulation, adhesive and UV resistance properties, all of which constitute an effective and promising approach for the delivery of agrochemicals for pest control.

1. Introduction Global crop production suffers considerable loss each year due to weeds, pathogens and pest, which is associated with 90% of the

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pesticides running off to the environment or decomposing before reaching the target [1–3]. Ineffective use of pesticides further causes a series of problems, such as soil/water pollution, pest resistance, ecological and environment issues [4]. Several reasons contributed to the

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

https://doi.org/10.1016/j.colsurfa.2019.03.049 Received 27 January 2019; Received in revised form 8 March 2019; Accepted 16 March 2019 Available online 18 March 2019 0927-7757/ © 2019 Elsevier B.V. All rights reserved.

C. Tang, et al.

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poor efficiency of pesticide delivery: (1) most of the active ingredients (AI) are insoluble in water, and the conventional pesticide formulations display poor foliar retention/adhesion properties; (2) AI in conventional formulation are not properly protected, where early degradation may occur especially for environmentally sensitive pesticides; (3) limitation of spraying systems, such as spray drifting [5–7]. Currently, there is a trend to develop smart and safe water-based pesticide formulations, which aims at improving the pesticide effectiveness and handling safety for human [1,6]. As most of the AI are water-insoluble compounds, many strategies have been developed to improve their water dispersibility. These include incorporating them in carriers [8,9], emulsifiers [10], and solvents within the formulations [3]. The formation of the products involves capsules [11–13], spheres [14], micelles [15,16], suspensions [17], emulsions [10], and mesoporous silicas [13,18–20]. Among them, capsules have attracted increasing attention due to their core-shell structure, where the AI can be encapsulated within the inner core [6]. In addition, the shell materials are versatile, which are usually composed of biodegradable polymers, such as polyvinyl alcohol (PVA) [21], polyethylene glycol (PEG) [3], chitosan [22], polyurethane (PU) [23] and lignin [11,12,24,25]. Polydopamine (PDA) as a mussel inspired natural polymer, displays many attractive properties, such as good adhesion, biodegradability, and UV resistance [26–30]. Recently, PDA capsules have been widely used for drug [30–32], fertilizer [33,34], as well as pesticide delivery [13,14,35–38]. DA can easily self-assemble on various templates such as; (1) hard templates: calcium carbonate (CaCO3) particles, polystyrene (PS) spheres, silica (SiO2) particles; and (2) soft templates: emulsions, such as dimethyldiethoxysilane (DMDES). The PDA capsules can be obtained by etching the templates, which is a straightforward and effective method [14,39–46]. Emulsion templated PDA capsules possess many advantages, as the AI can be dissolved in the emulsions prior to the PDA deposition, thereby improving the encapsulation efficiency [13,40,41]. In addition, many reported studies on PDA capsules are based on hard templates, where high pesticide concentration was used to generate sufficient concentration gradient to increase the loading efficiency [28,37,46]. However, the adsorption is time consuming and the efficiency is dominated by concentration gradient, shell thickness, surface charges, etc. Conventional emulsions for pesticide formulations have many drawbacks, namely the rampant use of synthetic emulsifiers (e.g. alkylphenol ethoxylates) and organic phase (e.g. toluene and xylene), both are very toxic to mammals [1,6,10,47]. Therefore, new pesticide formulations using sustainable and green processes and materials are desirable. Emulsions stabilized by solid particles, known as Pickering emulsions as alternatives to surfactant stabilized emulsions have attracted increasing attention [48–52]. They require less emulsifier, more stable, and possess other advantages compared to emulsions stabilized by surfactants [53,54]. Cellulose nanocrystals (CNC), derived via acid hydrolysis of biomass, are one type of nanoparticles that are being exploited for such application [55]. Due to their renewable and “green” characteristics, and the presence of functional groups on their surface allowing for easy modification, new and functional systems have been developed [56]. Hence, this sustainable material has been used in a wide range of applications, such as drug carrier [57], composite nanofiller, as well as Pickering emulsifier [51,58,59]. The use of botanical pesticides as an alternative instead of synthetic pesticides for pest control is generally accepted as an environmentally friendly strategy [60,61]. Essential oil is a common active botanical compound for pest control, which has been reported widely [61,62]. Encapsulation of essential oil is a very effective and common approach in commercial pesticide formulations [63,64]. The novelty of this work compared to previous studies concerning PDA capsules include the followings: (1) Pickering emulsions were used as templates instead of polystyrene beads/CaCO3, hence the etching step is avoided; (2) sustainable nanomaterial, i.e. CNC was used as the

emulsifier instead of a synthetic surfactant to prepare the emulsion template; (3) encapsulation of the herbicide was achieved in a single step during the emulsification and dopamine polymerization, which is straightforward and efficient to achieve good loading capacity; (4) most previous studies reported the loading of pesticides in PDA capsules via diffusion by immersing the capsules in a concentrated pesticide solution, which is time consuming and not effective to achieve good loading capacity; (5) essential oil was used as the oil phase, instead of conventional solvent, such as toluene and xylene. In this paper, we synthesized cinnamoyl chloride (CC) modified CNC (CNC-CC) as an emulsifier to prepare oil-in-water emulsions, which act as a template to produce PDA capsules for AI encapsulation. The advantages of this system include: (1) CNC is a green emulsifier for oil-in-water emulsions; (2) cinnamate moieties display unique UV blocking properties, therefore, the PDA capsules containing dense layer of CNC-CC block UV irradiation; (3) the oil phase is composed of a model essential oil (oil of turpentine) and 1-butyl alcohol, where the oil mixture functions as a botanical pesticide and serve as a good solvent for 2,4-D (a model herbicide); (4) the AI (2,4-D) is encapsulated in the capsules before DA polymerization, which increases the encapsulation efficiency. 2. Experiments 2.1. Materials Sulfated cellulose nanocrystals were kindly provided by Celluforce Inc. Cinnamoyl chloride (CC), N,N-dimetheyl formamide (DMF, anhydrous 99.8%), 4-(dimethylamino) pyridine (DMAP), triethylamine (TEA), tetrahydrofuran (THF, anhydrous 99.9%), acetone, oil of turpentine (Turpentine), 1-Butyl alcohol (BA), potassium bromide (KBr), dopamine hydrochloride (DA), Tris(hydroxymethyl)aminomethane hydrochloride (Tris), 2,4-Dichlorophenoxyacetic acid (2,4-D), regent alcohol and Nile red were purchased from Sigma Aldrich unless specified otherwise. All chemicals were used without additional purification unless stated otherwise. Milli-Q water (resistivity of 18.2 MΩ cm) was used to prepare the aqueous dispersions. 2.2. Methods 2.2.1. Preparation of surface modified cellulose nanocrystals The hydrophobically modified CNC was prepared according to Zhang et al. [65]. Briefly, 1.0 g CNC was dispersed in 80 mL DMF via sonication. Then, 20 mL DMF mixture containing cinnamoyl chloride (1.0 g), 1.3 ml TEA and 1.0 g of DMAP were added dropwise to initiate the esterification reaction. The reaction was conducted at room temperature for 24 h, and the resultant product was recovered via centrifugation in THF (3 times) and acetone (1 time), followed by dialysis in deionized water for 3 days. The cinnamoyl chloride modified CNC (CNC-CC) was finally obtained after freeze-drying. 2.2.2. Preparation of Pickering emulsion templates All the emulsions were prepared using the CNC-CC dispersions (0.5–1.5 wt%) as the water phase, oil of turpentine (Turpentine) and 1butyl alcohol (BA) mixture of different ratios as the organic phase. The emulsions were prepared using an ultrasonic probe (MisonixMicroscon-XL2000), unless otherwise stated. All the emulsions were produced in 1 mL of organic and aqueous phase respectively in various concentrations of CNC-CC. The power setting was calibrated using DI water, achieving a 10 W power output when partially immersed in DI water. The mixtures were premixing by hand and then subjected to sonication for 1 min. The obtained Pickering emulsion was kept at room temperature for 24 h and was subsequently used as the stock emulsion. 404

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2.2.3. Preparation of Pickering emulsion templated polydopamine microcapsules The capsules were prepared by depositing polydopamine (PDA) on the Pickering emulsion template by oxidative self-polymerization in alkaline condition. Briefly, 1 mL stock emulsion was dispersed into 100 mL Milli-Q water, and Tris was dissolved in the dispersion to adjust the pH to 8.5. Then, various amounts of dopamine hydrochloride (DA) was introduced to the dispersion and the coating polymerization was performed for 24 h at room temperature. The products were recovered and purified by glass filtration using a 0.1-μm membrane filter and washed several times with DI water until the filtrate turned colorless. The concentrated polydopamine microcapsule was vacuum-dried and stored for subsequent use.

and subjected to UV–vis analysis at a wavelength of 284 nm. The concentration of 2,4-D in the filtrate was determined by the UV–vis standard curve. The loading and encapsulated amount of 2,4-D in PDA capsules was calculated using Eqs. (2) and (3). Experiments were carried out in triplicate, and the average values were reported.

mass of 2,4 D loaded in capsules × 100% mass of capsules

2,4

D loading =

2,4

D encapsulation =

(1)

mass of 2,4 D loaded in capsules × 100% mass of 2,4 D (2)

2.2.7. In vitro release study To investigate the effect of DA content on the release behavior, PDA capsules (produced using 2000, 1200, and 800 mg DA, respectively) containing 40 mg 2,4-D were added to 5 mL ethanol/water mixture (5/ 5, v/v). The mixture was then transferred to a dialysis bag (cut off Mw of 12,000–14,000 Da), followed by the addition of 65 mL ethanol/water mixture (5/5, v/v). The solution was stirred at 200 rpm at room temperature and 3 mL of the supernatant was removed at regular intervals, and the concentration of 2,4-D was measured with a UV spectrometer at a wavelength of 284 nm, and the cumulative release ratio was plotted against the time. Similarly, to study the effect of ethanol and water ratio on the release behavior, 15 mg capsules (produced with 1200 mg DA and 2.0 mg 2,4-D) were placed in 50 mL of ethanol/water mixture (ethanol:water = 3:7, 5:5, and 10:0, respectively), and the cumulative release ratio was obtained using the same procedure described previously. All the tests were performed in triplicate, and the average values were reported. For the essential oil release study, 1000 mg of vacuum dried PDA capsules (produced with 1200 mg DA) were conditioned at 40 ℃. As a control, 10 g of turpentine oil was evaporated at room temperature (R.T.), 30 and 40 ℃, respectively. The weight of sample was added at set time intervals, and triplicate tests were performed and the average values were reported.

2.2.4. Characterization of modified CNC nanoparticles The samples were prepared by dispersing the freeze-dried powders in water and homogenized to yield a uniform dispersion. Dynamic light scattering (DLS) and ζ-potential experiments were conducted on 0.04 wt% CNC and CNC-CC dispersions using a Malvern Instrument Zetasizer Nanoseries. The zeta potentials were determined from 3 measurements consisting of 12 repeated runs per measurement. Fourier transform infrared spectroscopy (FTIR) spectra were obtained using the Bruker Tensor 27 spectrometer FT-IR spectrometer with a resolution of 4 cm–1 and a scanning number of 32 from 400 to 4000 cm–1. Briefly, pellets were prepared by mixing the freeze-dried samples with KBr, ground in mortar and pestle and compressed into a pellet. UV–vis spectrum was recorded in the Hewlett Packard 845× spectroscopy with a wavelength of 279 nm for the 0.046 wt% dispersion. Additionally, 0.01 wt% aqueous samples were prepared by spraying onto copper grids (200 mesh coated with copper) and allowed to dry for TEM characterization (Philips CM10). Contact angle measurements were performed using an optical tensiometer to examine the wettability of the CNC before and after chemical modification. All samples were prepared at 3.0 wt%, which were further coated on a glass slide by drop casted to obtain a film. 2.2.5. Characterization of Pickering emulsion and PDA capsules Creaming index is defined as the height ratio of the creaming layer over the total emulsion height. Photographs of the vials containing the emulsions were recorded using a P1 digital camera (Olympus), and the height of the creaming layer was measured with a digital caliper. The emulsions were visualized by an inverted optical microscope (Nikon Elipse Ti-S) equipped with a CCD camera (QImaging ReTIGA 2000R). A total of 10 μL of the Pickering emulsion was added to the glass slide, then a single drop of water was added to dilute the emulsions, which was then visualized in a microscope. The droplet diameter was measured using an image analysis “ImageJ” software. A total of at least 300 droplets were measured and the surface mean diameter D (3,2) (the Sauter diameter) was reported as the average diameter. The morphology of PDA capsules was characterized by TEM (Philips CM10) and Hitachi TM-3000 scanning electron microscopy (SEM) (Japan).

2.2.8. Release kinetics The release kinetics of 2,4-D from PDA capsules was analyzed using the Higuchi and Korsmeyer–Peppas models described by Eqs. (3) and (4): Higuchi model: Mt/M∞ = kt1/2 Korsmeyer–Peppas model: Mt/M∞ = kt

(3) n

(4)

where Mt/M∞ is the fraction of 2,4-D released at time t, k is kinetic rate constant, and n is an index that provides information on the release mechanism; i.e. Fickian diffusion (n < 0.43), non-Fickian or anomalous diffusion (0.43 < n < 0.85), and case II transport (n > 0.85). 3. Results and discussion

2.2.6. 2,4-D loading and encapsulation efficiency determination To determine the pesticide loading and encapsulation efficiency of these PDA capsules, 450 mg 2,4-D (a model herbicide) was dissolved in 3.33 mL oil mixture (Turpentine: BA = 0.7:0.3) and subjected to emulsification with 3.33 mL CNC-CC (1.5 wt%). Then, 1 mL emulsion (containing 67.56 mg 2,4-D) was dispersed in 100 mL Milli-Q water, followed by the introduction of 500, 800, 1200, 1500, 2000 and 2500 mg DA to the mixture, respectively. The polymerization was conducted at room temperature for 24 h and the products were recovered by filtration as described in 2.2.3. The cake was allowed to vacuum dried overnight at 45 ℃. For each sample, certain amount of dried PDA capsules was dispersed in ethanol via probe sonication, followed by constant shaking at room temperature for 48 h. Then, the dispersion was filtered, and the filtrate of each sample was collected

3.1. Characterization of modified CNC Pristine CNC possesses abundant negative charges, hence they are incapable of stabilizing oil-water emulsion due to the strong electrostatic repulsion between the nanoparticles. Surface modifications are commonly performed to enhance the emulsion stability. Cinnamate groups display strong UV absorption characteristics, and they are nontoxic and biocompatible [65–67]. Cinnamoyl chloride (CC) moieties were grafted onto CNC (CNC-CC), endowing the CNC with hydrophobic and UV protection characteristics. The synthetic procedure CNC is shown in Scheme 1. CC was grafted to the CNC to introduce hydrophobic functionality to the surface of CNC. TEA and DMAP were catalysts to promote the esterification reaction. The FTIR spectroscopy was conducted to confirm the presence of the esterification agents. As 405

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Scheme 1. Preparation procedure of cinnamoyl chloride modified CNC.

Fig. 1. (A) Infrared spectra of CNC and CNC-CC; (B) UV absorbance of a 0.046 wt% suspension of CNC-CC and CNC nanoparticles.

shown in Fig. 1A, both CNC and CC modified CNC possessed the following characteristic peaks: the hydrogen bonded −OH stretching at 3340.7 cm−1, the CeH stretching at 2891.3 cm−1, the −CH2 bending situated at 1427.3 cm−1, and the CeH bending at 1369.4 cm−1. After the esterification reactions, CNC-CC displayed the characteristic peak at 1721 cm-1 (highlighted in orange), which confirmed that the hydrophobic functional groups were successful introduced to the CNC. Since cinnamoyl chloride displayed a specific UV absorption peak at 279 nm, the UV spectroscopy was used to confirm the presence of CC. From Fig. 1B, an obvious peak was observed for CC modified CNC (0.046 wt %) at the wavelength of 279 nm, and this absorption was attributed to cinnamate moieties. From the TEM images (Fig. 2A and B), the morphologies associated with the hydrophobic modification were evident, where CNC-CC particles displayed significant aggregation compared to CNC due to the benzyl groups. DLS results (see Fig. 2C) further confirmed this, where CNC had an average hydrodynamic diameter of 78.8 nm, and it increased to 113.5 nm after cinnamoyl chloride modification. CNC and CNC-CC possessed a zeta potential of −35.9 mV and −27.3 mV, respectively (Table 1). The differences in the zeta potential could be attributed to the hydrophobicity of the esterification compound, and the variation of surface hydrophobicity can induce the differences in the water contact angle, which provides information on its wettability. In Fig. 2D and E, we observe that CNC-CC displayed a larger water contact angle of 38.55° than CNC (29.10°), and it could stabilize oil-in-water emulsion since its water contact angle was smaller than 90°.

hampered by its volatility and low affinity for hydrophobic compounds. Encapsulation is an effective strategy to minimize the evaporation of turpentine [64,69]. In this study, a multi-AI encapsulation was developed, where 1-butyl alcohol was chosen as the adjuvant solvent due to its high solubility for 2,4-D and low toxicity [13]. CNC-CC stabilized oilwater emulsions are shown in Fig. S1, and in 1.0 wt% CNC-CC and 1 mL BA, stable emulsion could not be prepared as evident by the oil layer above the water interface (Fig. S1A). In contrast, 1.0 wt% CNC-CC was sufficient to stabilize 1 mL turpentine (Fig. S1E). The differences may be caused by the polarity of the solvent, where turpentine is a non-polar solvent and BA is a polar solvent. Thus, we investigated the capability of CNC-CC to stabilize various proportions of BA and turpentine. When 0.5 mL BA was added to the solvent mixture, no emulsions were formed at CNC-CC concentration of 1.0 wt% (Fig. S1B), however, when the concentration CNC-CC was increased to 1.5 wt%, stable emulsion was formed (Fig. S1C). The volume of BA was further reduced to 0.3 mL with 1.5 wt% of CNC-CC as emulsifiers, and stable emulsions with no coalescence was observed (Fig. S1D). To examine the emulsion stability, the oil to water ratio was set at 1:1 with the oil mixture containing 0.7 mL turpentine and 0.3 mL BA. The creaming indexes of the emulsions with CNC-CC content ranging from 0.5 to 1.5 wt% were measured and shown in Fig. 3. It is evident that emulsions with 0.5 wt% of CNC-CC began to cream in 5 min after sonication, while emulsions containing 1.2 wt% of CNC-CC only creamed after 60 min. The creaming process is due to the density difference between the oil and water. From Fig. 3A, we observed that with increasing CNC-CC concentration, the creaming rate decreased, and the creaming rate is associated with the Stokes’s law, which was described previously for many Pickering emulsions [59,70]. The viscosity of the system increased when more CNC-CC nanoparticles were added. All the emulsions approached a creaming index of 61.5% after 24 h. The morphologies of the emulsions were visualized with an optical microscope and reported in Fig. 4. The emulsions possessed an average droplet size of around 8 μm in 0.5 mL BA (1.5 wt% CNC-CC) (Fig. 4A). A fluorescent dye (Nile red) was used as a marker to identify the oil phase. The interior of the emulsions displayed a green color confirming the oil-

3.2. Characterization of CNC-CC stabilized Pickering emulsions To investigate the capability of CNC-CC to stabilize oil/water emulsions, turpentine, 1-butyl alcohol and their mixture were used as the oil phase, and the water phase comprised of various amounts of CNC-CC. The volume of oil and water was kept at 1 mL, unless stated otherwise. Turpentine (one type of essential oil) is composed of αpinene, β-pinene, limonene and camphene, which is very effective for the control of pest [68]. However, its widespread applications are 406

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Fig. 2. TEM images of CNC (A) and CNC-CC (B); Number distribution of a 0.04 wt% suspension of CNC and CNC-CC nanoparticles measured by DLS (C); Water contact angle of CNC (D) and CNC-CC (E). Scale bar 200 nm for (A) and (B).

turpentine and 0.3 mL BA was then stabilized in water in the presence of 1 mL of 1.5 wt% CNC-CC.

Table 1 A summary about the average size, zeta-potential and contact angle of the nanoparticles. Nanoparticle

Average Size (nm)

ζ-potential (mV)

Contact angle (°)

CNC CNC-CC

78.82 113.5

−35.9 −27.3

29.10 38.55

3.3. Characterization of PDA capsules To synthesize PDA capsules, a 1 mL stock emulsion was added to 100 mL water, followed by the introduction of various amounts of DA and Tris powder to the mixture according to Table 2. It is evident from Fig. 5 that the emulsion droplets aggregated after the addition of DA in contrast the stable emulsions shown in Fig. 4G. We know that DA could self-oxidize in weak alkaline condition, yielding polydopamine (PDA) with good adhesive properties, that promoted the formation of clusterlike emulsion droplets [31,13]. With increasing amounts of DA, the aggregation of the droplets was enhanced as evident from Fig. 5. The morphologies of the PDA capsules were examined by TEM and SEM. In Fig. 6A and B, the capsules were not robust when less than 480 mg of DA was added, where they fragmented, revealing a PDA network coated on CNC. Intact capsules were produced by increasing DA content to 960 mg, and fewer fragmented capsules were evident (Fig. 6C). Thus, more DA was used, and the capsules prepared with 1200 mg, 2000 mg and 2500 mg DA are shown in Fig. 6D, E and F, respectively. More robust capsules were produced compared to those

in-water emulsion (Fig. 4B), where the hydrophobic oil phase of BA and turpentine was stabilized by the CNC-CC nanoparticles. In order to reduce the droplet size, we kept the oil ratio as 7:3 (0.7 mL turpentine and 0.3 mL BA), and Fig. 4C to 4H show the emulsions stabilized by 0.5–1.5 wt% CNC-CC. Clearly, the emulsion droplets size decreased with increasing CNC-CC concentrations. When the CNC-CC content was increased from 1.2 (Fig. 4F) to 1.5 wt% (Fig. 4G), the average droplets size was around 3.8 μm and remained unchanged. The average droplet size was close to that formed by 1 mL turpentine and 1.5 wt% CNC-CC (Fig. 4I). Similarly, Nile red was used as maker to identify the oil phase, which confirmed that the emulsion was oil in water systems (Fig. 4H). The emulsions shown in Fig. 4G were extremely stable and did not coalescence over 3 months, and the oil phase containing 0.7 mL 407

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Fig. 3. Creaming index profile of turpentine/BA oil in water emulsions stabilized by CNC-CC at room temperature as a function of different CNC-CC concentrations (A); digital pictures of the Pickering emulsions at various time intervals (B). The oil phase was labeled with a hydrophobic dye (Nile red) (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article).

shown in Fig. 6A, B and C. However, there are no clear differences between capsules prepared with 1200 mg (Fig. 6D), 2000 mg (Fig. 6E) and 2500 mg (Fig. 6F). Additional morphological analyses using SEM were performed to examine the topographic of the capsules and to verify the optimal amount of DA required. Fig. 7 shows that all the capsules contained hollow structure (highlighted in red arrows) with smooth inner surface. From the above results, several key observations were recorded, namely; (1) the DA polymerization occurred only at the oil-water interface; (2) 1.5 wt% CNC-CC particles were sufficient to fully coat the

oil droplets to maintain the shape of emulsion droplets during DA polymerization. The capsules possessed a shell thickness of around 95 nm (Fig. 7A, D) when 1200 mg DA was used, which increased to 154 nm (Fig. 7B, E) and 230 nm (Fig. 7C, F) when 2000 mg and 2500 mg when DA was used, respectively. Excess DA would self-oxidize to form irregular PDA spheres that were deposited on the surface of capsules (highlighted in red circles). Thus, we concluded that 1200 mg DA is sufficient to prepare 1 mL Pickering emulsion with robust capsules.

Fig. 4. Optical microscope images of oil in water Pickering emulsions formed by different oil ratios and various CNC-CC concentrations. (A) and (B): Turpentine: BA = 5:5, CNC-CC 1.5 wt%; (C) to (H): Turpentine: BA = 7:3, CNC-CC from 0.5 wt% to 1.5 wt%; (I): Turpentine: BA = 10:0, CNC-CC 1.5 wt%. Scale bar (A)–(I): 20 μm. 408

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3.5. In vitro release behavior kinetic model study

Table 2 Details of dopamine polymerization recipes.

Fig. 5A Fig. 5B Fig. 5C Fig. 5D Fig. 6A Fig. 6B Fig. 6C Fig. 6D/Fig. 7A, D Fig. 6E/Fig. 7B, E Fig. 6F/Fig. 7C, F

Stock Emulsion (mL)

Oil volume (mL)

Dopamine (mg)

Tris (mg)

1 1 1 1 1 1 1 1 1 1

0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5 0.5

40 80 120 160 240 480 960 1200 2000 2500

24.228 48.456 72.684 96.912 145.368 290.736 581.472 726.84 1211.4 1514.25

PDA capsules produced with 1200 mg DA was used to study the 2,4D release behavior in different solvents: 100% ethanol (v/v), 50% ethanol (v/v), and 30% ethanol (v/v). The release rate decreased with decreasing ethanol ratio (Fig. 9), and it was more rapid in the first 10 h for all the three solvents. 2,4-D released from microcapsules in pure ethanol solvent approached a plateau after 10 h, while a slower release rate was observed in solvents with a lower ethanol ratio, which is associated to the lower solubility of 2,4-D. To investigate the effect of DA amount on the release behavior, PDA microcapsules prepared with 800, 1200, and 2000 mg DA were placed in mixtures containing 50% ethanol respectively. All the capsules displayed sustained release behavior (Fig. 10), and the capsules with 800 mg DA possessed the fastest release rate, followed by capsules produced with 1200 and 2000 mg DA. The difference is likely to be associated with the difference in the thickness of the PDA shell as shown in Fig. 7. Capsules prepared with 2000 mg DA possessed the thickest shell, and it displayed the lowest release rates. To further investigate the 2,4-D release mechanism, the release profiles for the capsules prepared with varying DA content was fitted to the Higuchi and Korsmeyer–Peppas models. The results from Higuchi model are not shown as a low regression coefficients (R2) was observed, signifying a poor fit. The fitted parameters and R2 from Korsmeyer–Peppas model are shown in Table 3 and Fig. S2. All the indexes (n) were lower than 0.43, indicating that the release of 2,4-D from PDA capsules could be described by the Fickian diffusion mechanism, where the 2,4-D release is diffusion controlled. Additionally, we studied the release profile of turpentine from the PDA capsules. The evaporation of turpentine oil without the PDA shell increased linearly with time (Fig. 11), and the evaporation rate was enhanced by increasing the temperature. However, the evaporation rate was reduced significantly with PDA coating (1200 mg DA). For example, at 40 °C, only 0.6% of turpentine from capsule with PDA shell was evaporated in 9 h, while 8.0% of turpentine was evaporated in the absence of PAD shell (Fig. 11). Thus, the encapsulation of essential oil with PDA capsules is an effective approach to control the release rate.

3.4. 2,4-D loading and encapsulation efficiency determination The 2,4-D loading and encapsulation efficiency as a function of DA content was plotted and shown in Fig. 8. The encapsulation efficiency increased with DA content ranging from 500 to 1500 mg and approached a plateau at around 90%. While the loading efficiency increased slightly from 14.1 to 14.7% when the DA amount was increased from 500 to 800 mg, which then rapidly decreased to around 7.5%. This trend is consistent with the PDA capsules morphologies shown in Figs. 6 and 7. As 500 mg DA was insufficient to prepare 1 mL of Pickering emulsion, 61.6% of 2,4-D was lost during the polymerization process, and this was reduced when more DA were added to yield robust PDA capsules. The loading efficiency at 800 mg of DA was slightly higher than 500 mg DA, due to the increased 2,4-D encapsulation. However, excess amount of DA would increase the shell thickness of the capsules that resulted in capsules with more mass, and this contributed to the reduction in the loading efficiency. The loading and encapsulation efficiencies are two important indices in pesticides formulations, and we could achieve higher 2,4-D loading efficiency by adding more 2,4-D or increasing the BA volume in the solvent mixture.

Fig. 5. Optical microscope images of oil in water emulsions after addition of various amounts of DA. (A) 40 mg DA; (B) 80 mg DA; (C) 120 mg DA; (D) 160 mg DA. Scale bar (A)–(D): 10 μm.

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Fig. 6. TEM images of PDA capsules templated by 1 mL Pickering emulsions with different amount of DA. (A) 240 mg DA; (B) 480 mg DA; (C) 960 mg DA; (D) 1200 mg DA; (E) 2000 mg DA; (F) 2500 mg DA. Scale bar (A)–(F): 2 μm.

Fig. 7. SEM images of PDA capsules templated by 1 mL Pickering emulsions with different amount of DA. (A) (D) 1200 mg DA; (B) (E) 2000 mg DA; (C) (F) 2500 mg DA; (D), (E) and (F) are close view of (A), (B) and (C), respectively. Scale bar: (A)–(C) 30 μm, (D)–(F) 10 μm.

4. Conclusions

emulsion droplet size of 4 μm. For 1 mL Pickering emulsions, 1200 mg DA was sufficient to produce robust PDA capsules containing a shell thickness of approximately 95 nm. The PDA capsules exhibited excellent multi-AI encapsulation properties, where turpentine functioned as botanical pesticides as well as a solvent for the herbicide (2,4-D). The loading and encapsulation efficiency of 2,4-D could be adjusted by controlling the DA content, where 13.4% loading and 74.9% and encapsulation efficiency were achieved when 1200 mg DA was used. Such

An approach to prepare PDA microcapsules from templated Pickering emulsions stabilized by cinnamoyl chloride modified cellulose nanocrystals (CNC-CC) is proposed. A mixture containing 0.7 mL turpentine and 0.3 mL 1-butyl alcohol (a good solvent for model pesticide (2,4-D) was selected as the oil phase. We observed that 1 mL CNC-CC (1.5 wt%) was sufficient to stabilize 1 mL of oil mixture with an 410

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Table 3 Kinetic parameters of 2,4-D released from PDA microcapsules. Korsmeyer–Peppas model

2000 mg DA 1200 mg DA 800 mg DA

k

n

R2

10.53 13.76 18.87

0.3970 0.3760 0.3958

0.9798 0.9801 0.9812

Fig. 8. 2,4-D loading and encapsulation efficiency in PDA capsules prepared by various DA. Experiments were carried out in triplicate, and the averages are reported.

Fig. 11. Evaporation profiles of turpentine oil without PDA encapsulation at r.t., 30 °C, 40 °C, and turpentine oil with PDA encapsulation at 40 °C.

system showed a sustained release behavior for AI, which has great potential in crop protection, AI encapsulation and controlled delivery of active chemical compound. Acknowledgements We wish to acknowledge CelluForce Inc. for providing the cellulose nanocrystals. The research funding from CelluForce and FP Innovations facilitated the research on CNC. K. C. Tam wishes to acknowledge funding from CFI and NSERC.

Fig. 9. 2,4-D release profiles in different solvents.

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Fig. 10. 2,4-D release profiles from PDA microcapsules produced by different amount of DA. Solvent was composed of ethanol: water (5:5, v/v).

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