Journal of Polymers and the Environment

https://doi.org/10.1007/s10924-019-01391-5

ORIGINAL PAPER

Starch:Pectin Acidic Sachets Development for Hydroxyapatite

Nanoparticles Storage to Improve Phosphorus Release
Camila R. Sciena1,5 · Maria F. dos Santos2,5 · Francys K. V. Moreira3 · Alfredo R. Sena Neto4 · José M. Marconcini5 ·
Daniel S. Correa5 · Elaine C. Paris5 

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Abstract
The importance of fertilizers in boosting crop production has motivated the development of novel high-performance systems
capable of improving the phosphorus release in the soil. For instance, methods capable of increasing the surface area of
fertilizer particles and promoting the solubilization of low-solubility compounds, including phosphates, are highly pursued.
This study was aimed at synthesizing hydroxyapatite nanoparticles and investigating their solubility in relation to crystallin-
ity, size, and morphology for phosphorous fertilizer applications. To improve the phosphate ions release, the hydroxyapatite
nanoparticles were storage in biodegradable sachets composed of thermoplastic starch/pectin blends with different polymer
ratios. The results showed that the smallest and less crystalline hydroxyapatite nanoparticles presented the highest solubility.
After storage in polymeric thermoplastic starch:pectin sachets, solubility for all samples was greatly improved, enhancing
the phosphorus release due to pH decrease, independent on the nanoparticle size, shape, and crystallinity. The results high-
light that the use of acidic sachets is a valuable approach for enhancing phosphorus and other macronutrients release from
fertilizers with basic surface properties, aiming at increasing agricultural crop productivity.
Graphical Abstract

Keywords  Hydroxyapatite · Starch · Sachet · Biodegradable · Nanoparticles

Extended author information available on the last page of the article

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Introduction
The production of agricultural commodities is extremely
dependent on chemical fertilizers, whose uncontrolled use
has led to environmental problems, threating both human
health and the environment [1, 2]. In addition, some
important mineral fertilizers, such as oxides, and apatites,
present low solubility, minimizing the release of nutrients
and consequently their absorption by plants. An alterna-
tive to improve the availability of nutrients to plants and
reduce the fertilizer application costs is the enhancement
of mineral fertilizer sources [3]. In this way, the develop-
ment of methods for increasing mineral fertilizer solubility
could lead to an improvement of agricultural production.
The solubility of a material can be enhanced by increas-
ing its surface area, which makes the use of nanoparticles
extremely relevant in this context [4]. On the other hand,
nanoparticles can be easily dispersed either in air or water,
causing accidental inhalation or lost by leaching. The use
of adequate biodegradable storage systems for nanoparti-
cles could solve this issue as well as controlling nanopar-
ticles solubility.
Phosphorus (P) is one of the macronutrients that are
required for growth and development of plants and cannot
be replaced by any other mineral [5]. Phosphorus defi-
ciency in plants is a major restraint in the global agricul-
tural production as it affects seed production, development,
and plant growth [6]. The traditional phosphate fertilizers
are based on the chemical processing of phosphate rock,
an insoluble material with a high phosphorus concen-
tration [7]. This expensive process creates a by-product
called phosphogypsum, or calcium sulfate, a contributor
to environmental problems, since large quantities of this
compound have been stored without application [8]. In
this context, the direct use of natural phosphate rock could
offer the opportunity to reduce the environmental impact
caused by the phosphate fertilizer production [9, 10].The
apatite group presents low water-solubility and it needs to
be applied in acidic soils due to its basic character, or in
controlled fungi and/or bacteria concentration to improve
its solubilization [11, 12]. Particle size is another factor for
solubility enhancement, since solubility increases expo-
nentially with the nanoparticle size decrease, according to
Ostwald-Freundlich theory [13]. This is a crucial aspect
in the apatite solubilization field that could enable the use
of apatite as a particulate fertilizer.
Apatite is the most abundant phosphate rock and belong
to the calcium phosphates family [3]. This class is sub-
divided into groups according to the present anion, such
as hydroxyapatite, which contains the hydroxyl anion [3].
Hydroxyapatite, ­Ca10(PO4)6(OH)2, (HAP) is a bioceramic
material found in nature in the hexagonal and monoclinic
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Journal of Polymers and the Environment
forms [14]. This mineral is a potential candidate for
improving phosphorus concentration in soil, hence ben-
efiting crop production [15].
The use of hydroxyapatite obtained by coprecipitation as a
fertilizer has been previously investigated [15–20]. Bala et al.
[20] obtained HAP nanoparticles with 15–30 nm diameter
and observed that the use of these nanoparticles in suspen-
sion increased chickpea germination and growth, when com-
pared to a control without phosphorus addition. Other results
reported by Liu and Lal [17] showed that a carboxymethyl
cellulose/hydroxyapatite nanoparticles (15–30 nm) suspension
increased by 30% the soybean plant growth compared to the
use of a commercial phosphorous fertilizer.
Systems based on microorganisms to improve mineral fer-
tilizer solubility have also been studied [21–26]. Cabello et al.
[21] studied the solubility behavior of phosphate rocks (PR)
in presence of G. mosseae fungus. The plant in a soil contain-
ing the fungus/phosphate rock mixture presented the highest
phosphorus fixation compared to a PR-cultivated control plant.
Methods based on the addition of microorganisms to improve
phosphorus solubility have been effective; however, the soil
treatment becomes more expensive and laborious.
The development of controlled release methods has also
been found in the literature [27–34]. Qiao et al. [31] encapsu-
lated urea in two layers, the first one consisting of ethyl cel-
lulose and the second one of starch, obtained from several
different sources. The capsules achieved a high water retention
level and the nitrogen release rate from urea reduced signifi-
cantly when compared to urea release without coating. Giroto
et al. [16] produced hydroxyapatite, urea, and starch compos-
ites in pellet forms using torque rheometer processing. The
dissolution of the material in citric acid solution evidenced
an increase in the phosphorus release and a decrease in nitro-
gen release when compared to pure hydroxyapatite and urea.
These processes aimed at the retention of the fertilizers and the
prolonged release of nutrients instead of increasing their dis-
solution rate, which is also necessary for the mineral fertilizer
effectiveness.
Therefore, the present work was aimed at enhancing the
release of phosphorus from hydroxyapatite (HAP) nanopar-
ticles displaying different sizes, crystallinity, and shapes.
This was attempted with the use of a biodegradable acidic
sachet composed of thermoplastic starch/pectin blends. To the
best of our knowledge, the use of biodegradable sachets to
enhance the use of HAP as a phosphorous fertilizer has not
been reported yet.
Journal of Polymers and the Environment

Experimental
Synthesis of Hydroxyapatite Nanoparticles
Hydroxyapatite (HAP) nanoparticles were synthesized
using the wet coprecipitation method. The masses of the
reagents were calculated according to the HAP stoichiom-
etry. In brief, an aqueous dibasic ammonium phosphate
solution (0.005 M) (Synth—98%) was slowly added drop-
wise to a calcium nitrate tetrahydrate solution (0.01 M)
(Synth—99%) under constant stirring and ­N2 atmosphere.
The pH was held at 11 with controlled addition of ammo-
nium hydroxide (Synth—27%). The white precipitated
was washed until neutral pH, centrifuged and dried in an
oven at 40 °C. To obtain the hydrothermally-treated HAP
nanoparticles, the white precipitated was first heated at
150 °C for different times (12, 24, 36, 48, 60, 72, 84, and
96 h) and then washed, centrifuged and dried at 40 °C.
The HAP nanoparticles were also synthesized by hydro-
thermal treatment for 36 h at 150 °C using urea (0.1 mol,
Synth—99%) as a precursor in the wet coprecipitation
step. Further morphological analysis was performed by
comparing the following samples: the coprecipitated HAP
without hydrothermal treatment (0 h), coprecipitated HAP
with hydrothermal treatment for 36 h (36 h), coprecipi-
tated HAP using urea with hydrothermal treatment for 36 h
(U36 h), and a commercial HAP (Sigma-Aldrich—90%).
The HAP samples were characterized by XRD (Shi-
madzu XRD6000 at 30 kV/30 mA with Cu Kα radiation
and scanning speed at 1°min−1), Zeta Potential (Malvern
Instruments—Zetasizer Nano ZS90), N ­ 2 adsorption/des-
orption isotherms (ASAP 2200 heating rate of 10°min−1
until 70 °C), FEG-SEM (JEOL- JSM 6701F) and TEM
(FEI TECNAI G2 F20) techniques.
Then, the sachet was filled with 0.05 g of HAP and the last
opened side was sealed. The hot pressing was carefully
done to avoid exposure of the HAP nanoparticles to heat-
ing during the sachets mounting.
Phosphorus Release Experiments
To evaluate the HAP nanoparticles solubility, 0.05 g HAP
were placed in 250 mL of deionized water and stored in an
oven at 40 °C. Next, aliquots (5 mL) were taken at different
times (4, 8, 12, 24, 36, and 48 h). The phosphorus concen-
tration was determined by the molybdenum blue method
[36] using an UV–Vis spectrophotometer (Perkin Elmer—
Lambda 25). Each HAP-filled sachet was also stored in
250 mL of deionized water at 40 °C. Aliquots were col-
lected until 240 h for phosphorus quantification using the
same method. All experiments were performed in triplicate.
Results and Discussion
Characterization of HAP Nanoparticles
The structure and phase formation of HAP samples were
evaluated by X-ray diffraction (XRD). Figure 1 shows HAP
single-phase formation in a hexagonal structure according
to the Joint Committee on Powder Diffraction Standards
(JCPDS) card No. 09-0432. Secondary phases, such as cal-
cium carbonate were not found. XRD patterns also suggested
that the HAP nanoparticles obtained in all conditions were
monophasic with crystallinity improved with the increasing
hydrothermal treatment time. This is indicated by the better
peak definition in the patterns, mainly the reflection (002).

Preparation of Starch:Pectin Sachets

Starch:pectin blends were prepared according to Moreira

et al. [35]. Starch (4001—provided by Ingredion) and Pec-
tin (Genu USP B—purchased from CP Kelco) were used
without any previous treatment. Different starch:pectin
ratios (100:0; 75:25; 50:50; 25:75; 0:100) were prepared
with further addition of glycerol and stearic acid. All com-
ponents were processed in a Haake mixer using 160 rpm
speed and temperature of 130 °C for 4 min. The samples
were shaped into films by hot pressing for 7 min at 140 °C.
Starch:pectin blend films were characterized by XRD (Shi-
madzu – XRD-6000) and FEG-SEM (Jeol – JSM 6710F).
To prepare the starch:pectin sachets, the films were cut
into two 2 × 2 cm squares, which were mounted as a sachet
by sealing three of their sides by hot pressing at 140 °C. Fig. 1  X-ray diffraction patterns of HAP nanoparticles obtained by
coprecipitation and hydrothermal treatment at 150 °C (0 to 96 h)

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 Journal of Polymers and the Environment

Studies were carried out using the ­N2 adsorption/des-

orption technique by BET method (Fig. 2d) to evaluate the
surface area of the HAP nanoparticles. There was a signifi-
cant surface area difference between the 0 h HAP sample
­(SBET = 92.3 m2 g−1) and the HAP sample hydrothermally
treated for 12 h ­(SBET = 52.3 m2 g−1), whose average diam-
eters were 12 and 24 nm, respectively. The variations of
surface area for the samples hydrothermally treated from 12
to 96 h could be attributed to particle agglomeration/aggre-
gation effects (Fig. 2b, c) induced by the synthesis method,
since none surfactant was applied to minimize the interac-
tions between the HAP nanoparticles in solution.

Characterization of Starch:Pectin Sachets

Fig. 2  FEG-SEM images of HAP nanoparticles obtained without 0 h

Figure 3 illustrates the XRD patterns of the starch (TPS):
(a) and hydrothermal treatment for 48 h (b) and 96 h (c). The average pectin (PEC) blend films with different TPS:PEC ratios. All
diameter and BET surface area (d) diffractograms presented a characteristic broad band from 10
to 25° of 2θ, suggesting low crystallinity for TPS and PEC.
No peaks were found in the XRD pattern of the 100PEC
Such results are in accordance with Mobasherpour et al. sample, indicating a non-crystalline material. These results
[37], who obtained HAP using the coprecipitation method corroborate with Kumar et.al. [39], who observed a broad
followed by sintering, and also observed a better definition band for pectin extracted from apple. The diffractogram of
of XRD reflections for the samples submitted to thermal the 100TPS film displayed four reflections at 2θ of 13°, 17°,
treatment. 19.7° and 22.3°, attributed to the amylopectin recrystalli-
The FEG-SEM images in Fig. 2 show HAP nanoparticles zation in TPS [40]. In general, the XRD patterns (Fig. 3)
with rod-like shape and different diameters. These results showed that the relative reflection intensity was propor-
are in agreement with those reported by Liu et al. [18], who tional to the TPS content in the formulation, supporting the
obtained HAP rods with 8–20 nm diameter using coprecipi- expected starch:pectin blend compositions.
tation and hydrothermal treatment at 140 °C for 24 h. Fig- Figure  4a–c show  SEM images of the cryogenically-
ure 2a–c show that the diameters of the HAP nanoparticles fractured cross-sectional  surfaces of samples  100PEC,
obtained without hydrothermal treatment (0 h) were smaller 50TPS:50PEC, and 100TPS. The images show
than those of the hydrothermally-treated samples, ranging
between 7 and 17 nm, and 10 and 40 nm, respectively. This
illustrates the dependence of the HAP nanoparticle growth
on the hydrothermal treatment time. This trend agrees with
the data reported in the literature for europium-doped HAP
nanoparticles synthesized through this similar two-step
approach [38].
Figure 2d shows the relation between HAP nanoparti-
cle size and hydrothermal treatment time. The HAP nano-
particles hydrothermally-treated for 12 h presented sizes
two-fold larger in relation to the untreated ones (0 h). For
hydrothermal periods exceeding 24 h, little variations in the
average HAP nanoparticle size were observed, which may
be explained by several solubilization/recrystallization steps
that occurred in the hydrothermal reactor [19]. It can also be
noticed that the standard deviation values were high for all
samples, suggesting that the HAP nanoparticle size distribu-
tions are not homogeneous. Such behavior could be associ-
Fig. 3  X-ray diffraction patterns of starch (TPS):pectin (PEC) blend
ated with the fact that the particle nucleation and growth
films with different starch:pectin ratios: 100TPS, 75TPS:25PEC,
processes did not occur homogeneously over the coprecipita- 50TPS:50PEC, 25TPS:75PEC, and 100PEC. Reflections correspond-
tion and solubilization/recrystallization stages. ing to the sample holder are indicated by arrows

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Journal of Polymers and the Environment
Fig. 4  SEM images of cryogen-
ically-fractured cross-sectional
surfaces of samples (a) 100TPS,
(b) 50TPS:50PEC, and (c)
100PEC films
Fig. 5  Film dissolution in water along  days  (1–10): (a) 100TPS,
(b) 75TPS:25PEC, (c) 50TPS:50PEC, (d) 25TPS:75PEC, and (e)
100PEC
characteristic surfaces for TPS (Fig. 4a) and PEC (Fig. 4c)
resulting from carbonic chains accommodation. The image
of the 50TPS:50PEC film (Fig. 4b) presented starch and
pectin specific regions, indicating formation of an immis-
cible blend. The blend film thickness varied from 0.20 to
0.55 mm, which was measured using a digital paquimeter.
Such a film thickness range favored both the film handling
to produce sachets and film maintenance during processing.
The starch:pectin sachets solubility was evaluated in
water (Fig. 5a–e) in order to use them for HAP nanoparti-
cles storage. The 100PEC film dissolved within 24 h, but its
solubilization resistance was improved due to the blending
with TPS. The 50TPS:50PEC and 25TPS:75PEC blend films
showed cracks after the first days of water immersion, which
made them improper for use as storage sachets. This was
due to the higher solubility of PEC in water (Fig. 5e). The
100TPS film (Fig. 5a) presented the highest water-resist-
ance, remaining physically intact for 10 days. Furthermore,
the 75TPS:25PEC blend film showed no cracks during the
first days of water immersion and were less durable than the
100TPS film. Hence, the 75TPS:25PEC blend was selected
to produce the sachets for phosphorus release.
HAP particle size, crystallinity, and pH of the medium
were varied to verify  the HAP nanoparticle solubility
(phosphorus release) in aqueous solution. HAP phosphorus
concentration was determined by UV–Vis absorption spec-
troscopy, using the molybdenum blue method [41] (Fig. 6).
Figure 6a illustrates the phosphomolybdate complex absorp-
tion spectra formed from soluble phosphorus released from
HAP nanoparticles. The typical phosphomolybdate complex
absorptions occur more strongly at around 880 nm and more
weakly at 700 nm [36]. From these results, the phosphorus
concentration versus time curves (Fig. 6b) were obtained for
each HAP nanoparticle sample.
The untreated HAP sample (0 h) presented higher solu-
bility compared to the 12 to 96 h hydrothermally treated
samples. This is related to its smallest particle size (Fig. 2)
and lower crystallinity (Fig. 1). This result is confirmed from
the previous report [42], which concluded that HAP showing
lowest crystallinity degree presents the highest water-solu-
bility. Moreover, it is observed in Fig. 6b that the phospho-
rus concentration released from the hydrothermally treated
HAP nanoparticles was similar for all treatment times. This
is due to the similar morphologies and sizes observed by
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 Journal of Polymers and the Environment

Fig. 6  (a) Blue phosphomo-

lybdenum complex absorption
spectrum. (b) Phosphorus
release profiles from HAP nano-
particles in aqueous medium as
a function of time. (c) Phospho-
rus release profiles from HAP-
filled starch:pectin sachets in
aqueous medium as a function
of time. (d) Visual aspect of
the HAP-filled sachets: 100TPS
(top), 75TPS:25PEC (middle),
and 100PEC (down)

FEG-SEM (Fig. 2) and the crystallinity behavior verified environment created by the pectin-containing biodegradable
by XRD (Fig. 1). sachets. Therefore, the low pH influence on the phosphorus
The solubility variation of the HAP nanoparticles (0, 48 release from HAP nanoparticles with different shapes was
and 96 h hydrothermal treatment) stored in the starch:pectin evaluated.
sachets as a function of time is illustrated in Fig. 6c. The Further experiments were carried out to analyze the phos-
hydrothermally-treated HAP nanoparticles showed a phos- phorus release from HAP particles with different shapes.
phorus release behavior similar to the untreated HAP nano- XRD results for commercial HAP, untreated HAP (0 h),
particle (0 h) when they were stored in the starch:pectin and hydrothermally-treated HAP nanoparticles (36 h) with
sachets, indicating that the HAP solubility was favored by
the medium. Furthermore, it was observed that the phos-
phorus concentration values increased substantially for the
same collection rate period. These HAP nanoparticle solu-
bility changes observed in the presence of the starch:pectin
sachets could be attributed to the medium pH decrease from
7 to 4 due to pectin solubilization, and its acidic character.
Higher HAP solubility observed in acidic medium is due
to ­OH− ions consumption by ­H3O+ ions provided by pectin
solubilization, which caused an equilibrium displacement
(Eq. 1), thus favoring the HAP nanoparticle dissolution.
) H2 O
Ca10 PO4 6 OH2 (s) ⇌ 10Ca2+ + 6PO3+ + 2OH−(aq)
( )(
(aq) 4(aq)
(1)
Image of the HAP nanoparticle-filled sachets with differ-
ent starch:pectin ratios used in the phosphorus release tests
are seen in Fig. 6d.
The results showed that the HAP nanoparticle size
and crystallinity factors are suppressed by the acidic Fig. 7  X-ray diffraction patterns of commercial HAP, 0  h  HAP,
36 h HAP, and 36 h HAP coprecipitated with urea

13
Journal of Polymers and the Environment
and without urea are seen in Fig. 7. In general, the hydro-
thermally treated samples showed more defined peaks, sug-
gesting a higher crystallinity. The untreated sample (0 h)
presented less peak definition, indicating its poor crystallin-
ity compared to the commercial and hydrothermally treated
HAP nanoparticles. All samples presented the HAP hexago-
nal crystalline structure, agreeing with Fig. 1. However, the
commercial sample presented additional peaks at 2θ 26°,
30°, and 41°, which were identified as a hydrogen calcium
phosphate ­(CaHPO4) secondary phase, monetite, according
to the JCPDS No. 01-077-0128, thus evidencing the com-
mercial sample impurity.
Transmission electron microscopy (TEM) was performed
on the commercial HAP, untreated HAP (0 h), and HAP and
urea-based HAP hydrothermally treated for 36 h samples for
morphological analysis (Fig. 8). The 0 h HAP is rod-shaped,
corroborating with its FEG-SEM image (Fig. 2). The urea-
based 36 h HAP sample presented tape-like shape, attrib-
uted to the urea interaction at the particle surface during its
growth. The commercial HAP was similar to the 0 h sample,
that is, it presented rod-like shape.
Phosphorus release tests were carried out for the indi-
vidual HAP nanoparticle samples (Fig.  9a), and for the
Fig. 8  Transmission electronic
microscopy (TEM) images of
(a) 0 h HAP, (b) 36 h HAP,
(c) 36 h HAP coprecipitade
with urea, and (d) commer-
cial nanoparticles
corresponding HAP-filled starch:pectin sachets (Fig. 9b).
The 0 h and commercial HAP samples presented higher
solubility (from 2 to 4 ppm approximately) compared to
the 36 h hydrothermally-treated HAP with and without urea
(from 0 to 1 ppm). This result agrees with the XRD patterns
(Fig. 7), suggesting that the high crystallinity of the HAP
nanoparticles submitted to hydrothermal aging resulted in
an average diameter increase. This result corroborates with
the literature [42], which indicated a solubility decrease with
the increasing HAP crystallinity and particle size.
Additionally, the maximum phosphorus release occurred
between 12 and 24 h for all samples, and then the HAP
solubilization remains practically constant, indicating an
equilibrium-prone behavior.
The phosphorus release test was evaluated for the nano-
particles packed in the 75:25 starch:pectin sachet. Figure 9b
reveals that the maximum phosphorus release occurred
from 48 to 120 h for all systems, with values between 24
and 36  ppm, which corresponded to 65 and 97% of the
expected maximum value, respectively. The phosphorus
release may be attributed to the start of a sachet dissolu-
tion, allowing phosphorus ions diffusion to the aqueous
medium. For periods longer than 168 h there were no system
13

Fig. 9  Phosphorus release
profile in aqueous medium
from the 0 h HAP and com-
mercial HAP nanoparticles
(a) and from the respective
HAP-filled 75TPS:25PEC
starch:pectin sachet (b)
behavior changes, suggesting that the HAP solubility limit
was reached.
In general, the methods used to produce polymer-coated
fertilizers involve simultaneous polymers/fertilizer pro-
cessing. In this way, the processing conditions such as tem-
perature, solvents, and others, can influence the fertilizer
structure and morphology, modifying its initial characteris-
tics. An important difference involving the use of polymer
sachets in relation to the other methods is that the fertilizer is
not processed alongside the sachet material, remaining unal-
tered after the sachet production. In addition, the polymer
sachets composition can be modulated according to the type
of fertilizer to control its solubility, making them potential
systems for rational nutrient release in the agriculture.
The results obtained in this work show that the size and
crystallinity of HAP nanoparticles obtained by coprecipi-
tation followed by hydrothermal treatment directly influ-
ence their solubility in water. Accordingly, the phosphorus
release showed that the hydrothermal treatment reduces the
solubility of the HAP nanoparticles due to the increase of
particle size and crystallinity. However, the storage of the
HAP nanoparticles in the starch:pectin sachets made the
hydrothermally treated HAP nanoparticles as soluble as the
untreated nanoparticles due to pH decrease caused by the
pectin dissolution. These results demonstrated a new path
for the strategic use of HAP nanoparticles as a suitable phos-
phorous fertilizer, regardless of nanoparticle size, crystallin-
ity and shape. Acidic polymer sachets are potential solubility
enhancers for low-solubility nanoparticles with basic surface
properties.
Acknowledgements  The authors thank the financial support given by
CNPq, SISNANO/MCTI, CAPES, and AgroNano research network.
References
1. Tang J, Hong J, Liu Y (2018) J Polym Environ 26:1930
2. Jia X, Ma ZY, Zhang GX, Hu JM, Liu ZY, Wang HY, Zhou F
(2013) J Agric Food Chem 61(12):2919
13
Journal of Polymers and the Environment
3. Treinyte J, Grazuleviciene V, Paleckiene R (2018) J Polym Envi-
ron 26:543
4. Merisko-Liversidge EM, Liversidge GG (2008) Toxicol Pathol
36:43
5. Haygarth PM, Jarvis SC (1999) Adv Agron 66:195
6. Haygarth PM, Heathwaite AL, Jarvis SC, Harrod TR (2000)
Adv Agron 69:153
7. Petkova V, Yaneva V (2010) J Therm Anal Calorim 99:179
8. Pérez-López R, Macías F, Cánovas CR, Sarmiento AM, Pérez-
Moreno SM (2016) Sci Total Environ 553:42
9. Hart MR, Quin BF, Nguyen ML (2004) J Environ Qual 33:1954
10. Mihajlovic M, Perisic N, Pezo L, Stojanovic M, Milojkovic J,
Lopicic Z, Petrovic M (2014) J Agric Food Chem 62:9965
11. Rajan SSS, Watkinson JH, Sinclair AG (1996) Adv Agronl
57:77
12. Welch SA, Taunton AE, Banfield JF (2002) Geomicrobiol J
19(3):343
13. Kwon GS (2008) Nanotechnology in drug delivery. Springer,
New York
14. Wei X, Yates MZ (2012) Chem Mat 24:1738
15. Montalvo D, McLaughlin MJ, Degryse F (2015) Soil Sci Soc
Am J 79:551
16. Giroto AS, Fidelis SC, Ribeiro C (2015) Rsc Adv 5:104179
17. Liu RQ, Lal R (2014) Sci Rep 4:6
18. Liu J, Ye X, Wang H, Zhu M,  Wang B, Yan H (2003) Ceram
Int 29(6):629
19. de Oliveira MAR, Paris EC, Ribeiro C (2013) Quim Nova
36:790
20. Bala N, Dey A, Das S, Basu R, Nandy P Iran J Plant Physiol 4(3)
21. Cabello M, Irrazabal G, Bucsinszky AM, Saparrat M, Schala-
muk S (2005) J Basic Microbiol 45(3):182
22. Yadav H, Fatima R, Sharma A, Mathur S (2017) Appl Soil Ecol
113:80
23. Narsian V, Patel HH (2000) Soil Biol Biochem 32:559
24. Goenadi DH, Siswanto Y, Sugiarto Y (2000) Soil Sci Soc Am
J 64:927
25. Chien SH, Sale PWG, Friesen DK (1990) Fertil Res 24:149
26. Chien SH, Prochnow LI, Cantarella H (2009) Adv Agron 102:267
27. Tyliszczak B, Polaczek J, Pielichowski K (2009) Pol J Environ
Stud 18:475
28. Jin SP, Yue GR, Feng L, Han YQ, Yu XH, Zhang ZH (2011) J
Agric Food Chem 59:322
29. Xiao XM, Yu L, Xie FW, Bao XY, Liu HS, Ji ZL, Chen L (2017)
Chem Eng J 309:607
30. Jin SP, Wang YS, He JF, Yang Y, Yu XH, Yue GR (2013) J Appl
Polym Sci 128:407
31. Qiao DL, Liu HS, Yu L, Bao XY, Simon GP, Petinakis E, Chen
L (2016) Carbohydr Polyms 147:146
Journal of Polymers and the Environment

3 2. Sharma J, Kaith B, Bhatti M (2018) J Polym Environ 26:518
33. León O, Muñoz-Bonilla A, Soto D, Ramirez J, Marquez Y, Colina
M, Fernández-García M (2018) J Polym Environ 26:728
34. Chen S, Yang M, Ba C, Yu S, Jiang Y, Zou H, Zhang Y (2018)
Sci Total Environ 615:431
35. Moreira FKV, Marconcini JM, Mattoso LHC (2012) Polym Bull
69:561
36. Murphy J, Riley JP (1962) Anal Chim Acta 27:31
37. Mobasherpour I, Heshajin MS, Kazemzadeh A, Zakeri M (2007)
J Alloy Compd 430:330
38. André RS, Paris EC, Gurgel  MFC, Rosa ILV, Paiva-Santos CO,
Li MS, Varela JA, Longo E (2012) J Alloys Compd 531:50
39. Kumar AC, GS (2010) Carbohydr Polym 82:454
40. Corradini EL, Medeiros ES, Carvalho AJF, Curvelo AAS, Mat-
toso LHC (2005) Polímeros 15:268
41. McLaughlin MM, McBeath TM, Smernik R, Stacey SP, Ajiboye
B, Guppy C (2011) Plant Soil 349:69
42. Fulmer MT, Ison IC, Hankermayer CR, Constantz BR, Ross J
(2002) Biomaterials 23:751
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Affiliations

Camila R. Sciena1,5 · Maria F. dos Santos2,5 · Francys K. V. Moreira3 · Alfredo R. Sena Neto4 · José M. Marconcini5 ·

Daniel S. Correa5 · Elaine C. Paris5 

3
* Elaine C. Paris Department of Materials Engineering, Federal University
elaine.paris@embrapa.br of São Carlos, Rod. Washington Luís, Km 235, São Carlos,
SP Zip code 13565‑905, Brazil
1
Department of Chemistry, Federal University of São 4
Department of Engineering, Federal University of Lavras,
Carlos, Rod. Washington Luís, Km 235, São Carlos,
Lavras, MG 200‑000, Brazil
SP Zip code 13565‑905, Brazil
5
2 Nanotechnology National Laboratory for Agriculture
Programa de Pós‑Graduação em Biotecnologia (PPG‑Biotec),
(LNNA), Embrapa Instrumentação, XV de Novembro St.,
Centro de Ciências Exatas e Tecnologia (CCET), Federal
1452, São Carlos, SP Zip code 13560‑970, Brazil
University of São Carlos, Rod. Washington Luís, Km 235,
São Carlos, SP Zip code 13565‑905, Brazil

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