Environmental Technology & Innovation 15 (2019) 100403

Contents lists available at ScienceDirect

Environmental Technology & Innovation

journal homepage: www.elsevier.com/locate/eti

Urea-impregnated HAP encapsulated by lignocellulosic

biomass-extruded composites: A novel slow-release fertilizer
Chirâa Elidrissi Elhassani a , Younes Essamlali b , Meryem Aqlil a , Annie
∗
Moussemba Nzenguet a , Ikram Ganetri b , Mohamed Zahouily a,b ,
a
Laboratoire de Matériaux, Catalyse et Valorisation des Ressources Naturelles (MaCaVa), URAC 24, FST Mohammedia B. P. 146,
20650, Université Hassan II Casablanca, Morocco
b
MAScIR Foundation, Nanotechnologie, VARENA Center, Rabat Design center, Rue Mohamed El Jazouli, Madinat El
Irfane 10100, Rabat, Morocco

highlights graphical abstract

• Coated urea with calcium phosphate

encapsulated woodchip is effective
to obtain fertilizer.
• Fertilizer nanocomposites were pro-
duced by pressing/extrusion.
• Calcination temperature and microstruc-
ture of the encapsulating material
are major factors affecting the re-
lease rate of urea.
• Urea/HAP encapsulated by lignin was
found to be versatile and smart slow
release fertilizer.

article info a b s t r a c t

Article history: In the present work, novel composite materials based on coated urea with calcium
Received 6 February 2019 phosphate encapsulated woodchip species were developed to be used as nitrogen-
Accepted 2 June 2019 loaded slow release fertilizers. Urea supported calcium phosphate was used as the basic
Available online 17 June 2019
fertilizer, whereas sugarcane bagasse (Saccharum officinarum L.) and its derivatives such
Keywords: as lignin and cellulose were used as the wood-based coating. The synthesized composite
Urea-modified hydroxyapatite fertilizers were characterized in relation to their structural properties by means of
Slow release nitrogen fertilizer X-ray diffraction and FTIR analysis. The obtained products were evaluated by means
Coating of laboratory tests for solubility in water for 60 days. It was found that the rate of
Sugar cane bagasse urea release in water was slower in the case of coated fertilizer than in the uncoated
Cellulose urea/HAP fertilizer and that the rate of the nutrient release process was noticeably
Lignin controlled by the coating material type and the calcination temperature of the HAP
support. Importantly, the Water immersion release experiments demonstrated that the

∗ Corresponding author at: Laboratoire de Matériaux, Catalyse et Valorisation des Ressources Naturelles (MaCaVa), URAC 24, FST Mohammedia
B. P. 146, 20650, Université Hassan II Casablanca, Morocco.
E-mail address: m.zahouily@mascir.com (M. Zahouily).

https://doi.org/10.1016/j.eti.2019.100403
2352-1864/© 2019 Published by Elsevier B.V.
2 C.E. Elhassani, Y. Essamlali, M. Aqlil et al. / Environmental Technology & Innovation 15 (2019) 100403

developed fertilizer displayed a subsequent slow-release of nitrogen even after 60 days

of release compared to the pure urea fertilizer, which released rapidly and prematurely
all its nitrogen content. The best slow release pattern of urea occurred with the urea
coated mesoporous HAP encapsulated by lignin over 60 days of release experiment.
© 2019 Published by Elsevier B.V.

1. Introduction

Fertilizers are one of the most important vital input materials for crop production. They are applied to the soil to
provide the specific nutrients necessary for each plant growth. Nitrogen, the most widely applied element for good
soil fertility, has commonly been considered to be the key macronutrient source in agriculture. Among the nitrogen
fertilizers, urea is one of the most commonly used commercial fast-release nitrogen fertilizers because of its high nitrogen
content (46wt%) and comparatively low cost of production (Trenkel, 2010). Since the urea is a neutral organic molecule,
it cannot be absorbed by plants easily before being hydrolyzed, thus, resulting in a significant loss of urea by leaching
and volatilization leading to low nitrogen utilization efficiency (Ni et al., 2011). It is estimated that about 40%–70% of
nitrogen of the applied fertilizers is lost to the environment rather than being absorbed by plants causing not only severe
economic and resource losses but also serious environmental hazards (Akelah, 1996; Pereira et al., 2015). These issues
justify the great interest in developing more efficient alternatives that may reduce environmental impact and boost the
plant productivity by delivering nitrogen in slow and sustained manner.
One possible alternative to reduce the fertilizer nutrient losses and to improve nutrients use efficiency while reducing
the environmental hazards involves the use of slow-release fertilizer (SRF). The SRFs have been demonstrated to be an
advantageous alternative to conventional fertilizer since they could overcome problems associated to soluble chemical
fertilizer. Such advantages involve decreasing fertilizer loss rate, supplying nutrients sustainably, lowering application
frequency and minimizing potential negative effects associated to the over dosage which result in better plant’s growth
performance (Al-Zahrani, 2000; Guo et al., 2006). Polymer-coated fertilizers are one of the most widely used approaches
to manufacture slow release fertilizer, which can significantly improve nutrient use efficiency and boost the plant
productivity (Naz and Sulaiman, 2016). However, petroleum-based coatings are usually non-degradable and may release
toxic gases harmful to the soil and to the atmospheric environments. To overcome such issues, the development
of environmentally friendly and renewable sources as coating materials has attracted special interest from health,
environmental and ecological points of view. In this context, great interest has been devoted to the development of
new composite fertilizer to control the urea supply to sustain the agricultural crops. Among the developed strategies,
the immobilization of urea on the mineral supports was found to be an efficient approach for slow and sustained
nitrogen release. These hybrid materials are considered to be efficient nanoscale reservoirs for the immobilization of
urea molecule in order to increase the nitrogen utilization efficiency by the plants (Kandil et al., 2010). Hence, several
research studies have attempted to formulate urea-based controlled release system; some examples include urea exchange
layered materials such as layered double hydroxides (LDHs) and montmorillonite clays (MMT) (Kottegoda et al., 2014),
urea modified mesoporous hydroxyapatite (Kottegoda et al., 2017), urea modified hydroxyapatite encapsulated in the
porous cavities of wood matrix (Glyricidia sepium) (Kottegoda et al., 2011), urea exchange montmorillonite extruded
nanocomposites (Pereira et al., 2012), urea fertilizer exchange bentonite (Xiaoyu et al., 2013), urea intercalated into the
layered structure of kaolinite encapsulated with arabic gum (Sempeho et al., 2015), urea and urea-formaldehyde exchange
montmorillonite extruded nanocomposites (Yamamoto et al., 2016).
Woodchips based slow release fertilizers are receiving great attention in the agriculture sector because they are
biodegradable and compatible with soil composition. Furthermore, the woodchip itself can acts as an organic fertilizer
upon decomposition of the plant cell which increases the organic matter content in soil (Ahmed and Chun, 2007;
Ahmed et al., 2011). Among the formulated SRF, formulations based on woodchips represent a new dimension of
wood and its derivatives uses. For example, Ahmed and Chun (2007) and Ahmed et al. (2011) formulated a new
slow release NPK fertilizer based on ammonium nitrate (NH4 NO3 ) and potassium pyrophosphate (K4 P2 O7 ) impregnated
three tree kinds of woodchips: Pinus koraiensis Sieb. et Zucc., Larix kaempferi Carr. and eunsasi poplar (Populus
tomentiglandulosa T. Lee). Four years later, these authors explored a new slow-release nitrogen formulation based on
ammonium-nitrate-impregnated three kinds of woodchips: Japanese red pine (Pinus densiflora S. et Z.), eunsasi poplar
(Populus tomentiglandulosa T. Lee), and konara oak (Quercus serrata Thunb.). Alternatively, Kottegoda et al. (2011) have
developed a new slow-release fertilizer of urea-modified with hydroxyapatite (HAP) encapsulated by Gliricidia sepium
soft wood. These studies demonstrated that woodchip derivatives not only carryout their role as a capsule for the
fertilizer solution but also act as an organic fertilizer upon decomposition of plant cells. Accordingly, the storage of
macronutrients into cavities present in Woodchip substrates seems to be an attractive approach for slow release and
sustained fertilizer manufacturing from both economical and environmental points of view. Among woodchip resources,
sugarcane bagasse (SCB) is one of the most abundant solid fibrous agro-industrial residues produced by the sugar and
alcohol cane industry. This low-cost lignocellulosic material has been considered as a potential fuel source for power
 C.E. Elhassani, Y. Essamlali, M. Aqlil et al. / Environmental Technology & Innovation 15 (2019) 100403 3

generation in sugarcane factories. Fresh SCB is mainly composed of about 50wt% cellulose, 25wt% hemicellulose and 18wt%
lignin (Sun et al., 2004). Due to its numerous advantages: low-cost, abundance, renewability and biodegradability, there
is a tremendous interest to explore novel applications of this agricultural residue that can unlock the potential of this
underutilized renewable material. Chemically, cellulose, the major constituent of SCB (Shankarappa and Geeta, 2013),
is a linear natural polymer of anhydroglucose units linked at carbon atom number one and four by β -glycosidic bonds
(Mandal and Chakrabarty, 2011). It possesses very promising properties, such as good mechanical properties, low density,
thermal stability, biocompatibility and biodegradability. Thus, cellulose has been widely applied in various industrials
applications. Lignin is considered to be the second most abundant natural polymer after cellulose. The chemical structure
and the degree of cross-linkages of this renewable material depend on the type and the age of the plants from which
it is extracted (hardwood, softwood, grasses, etc.). Until now, only a small part of the total available amount of lignin is
exploited (Gosselink et al., 2004). Owing to its interesting functional properties and hydrophobic nature, lignin was used
as the main component in controlled-release formulations particularly for application in soil together with conventional
mineral fertilizers. For example, Fernández-Pérez et al. (2008) prepared a lignin-based controlled release urea formulation
by mixing urea and lignin followed by milling to obtain the desired size range of controlled release particles. Thus, the
lignocellulosic materials can be suitable candidates for use in agriculture applications as encapsulating materials to the
design of a new generation of slow release fertilizers. To the best of our knowledge, there has been no reported work on the
use of SCB and its derivatives as encapsulating agents for slow release of nitrogen fertilizer. The scope of our research work
is the development of new composite fertilizers based on urea coated HAP encapsulated into micro/nanoporous cavities
of SCB and its derivatives namely cellulose microfibrils and lignin. The hybrid composite fertilizer was prepared through
a pressing/extrusion method. Unmodified hydroxyapatite, urea-modified hydroxyapatite and the prepared slow release
fertilizers were subject to structural and morphological characterizations in order to better understand the interaction
between hydroxyapatite and urea. The nutrient element release behavior of the above-mentioned composites was also
investigated to evaluate the feasibility of using urea-modified hydroxyapatite encapsulated by SCB and its derivatives as
efficient slow-release formulations.

2. Materials and methods

2.1. Materials

Sugarcane bagasse (SCB, collected from a local company in southern Morocco) used as coating and raw material was
milled, dried at 105 ◦ C for 12 h, and then sieved through a 100 mesh screen. The moisture content of the used sugarcane
bagasse fibers was about 7wt%. Technical grade urea ((NH2 )2 CO, 99%) was supplied by Sigma-Aldrich Company. Analytical
grade chemicals used for lignin and cellulose extraction were purchased from Sigma-Aldrich and were used as received.
Chemical reagents for hydroxyapatite and fluorapatite preparation were of analytical grade and all the solutions were
prepared in distilled water.

2.2. Synthesis of calcium phosphate nanomaterials

In a typical synthesis process, a first solution was prepared by dissolving 1.82 g of cetyltrimethylammonium bromide
(CTAB) used as a surfactant in 150 mL of distilled water followed by the addition of 7.92 g of (NH4 )2 HPO4 . The mixture
was stirred for 30 min until the formation of a clear solution. Similarly, a second solution was prepared by dissolving
23.615 g of Ca(NO3 )2 .4H2 O in 50 mL of distilled water. The pH of the phosphate solution was adjusted to 12 by adding
ammonia solution. The calcium solution was then dropwise added to the phosphate solution under vigorous stirring. The
obtained milky suspension was then stirred and heated at 80 ◦ C for 5 h. The solution was then left to cool down and to
precipitate for another 24 h, followed by centrifugation and washing by distilled water. The precipitated white powder
was dried at 80 ◦ C and calcined at different temperature before being used.
For fluorapatite synthesis, 1 g of NH4 F, as a source of fluorine, was added to the phosphate solution by employing the
same synthesis conditions as used in the first procedure.

2.3. Lignin and cellulose extraction

The process used for lignin and cellulose extraction was divided into two important steps, according to our previous
works (Aqlil et al., 2017; El Miri et al., 2015). Firstly, the raw SCB was ground and sieved using a 150 µm sieve size to
remove the small particles and fine powders. Lignin was extracted from the ground raw SCB through an alkali treatment
process consisting of three main steps. Firstly, SCB (5wt%) was subjected to repeated washing by hot water (60 ◦ C, 120
min) under strong mechanical stirring in order to remove the water-soluble components particularly hemicelluloses. The
residue obtained was thoroughly hydrolyzed by an alkali solution of NaOH at 15wt% at 80 ◦ C for 2 h under vigorous
mechanical stirring and the filtrate conventionally designated as black liquor was acidified with an acidic solution of
H2 SO4 at 5N until pH of 2. The precipitated lignin was recovered by centrifugation followed by several washing steps and
finally ground in a mortar to obtain a uniform powder.
4 C.E. Elhassani, Y. Essamlali, M. Aqlil et al. / Environmental Technology & Innovation 15 (2019) 100403

Fig. 1. Extruded urea/HAP-SCB, urea/HAP-Lignin and urea/HAP-CMF composite fertilizers.

For cellulose extraction, the fibrous residue obtained after alkaline treatment was bleached using solution constituted
of equal parts of acetate buffer, aqueous chlorite (1.7wt% in water), and distilled water. The bleaching treatment was
performed at 80 ◦ C for 4 h under mechanical stirring and was repeated four times. After each treatment, the fibers were
filtered and gently washed with distilled water before being subjected to a new bleaching treatment. Finally, the obtained
bleached cellulose fibers, also called cellulose microfibrils (CMF), were oven-dried at 60 ◦ C to remove excess water.

2.4. Slow release composite fertilizer formulation

The typical procedure for slow-release fertilizers preparation consisted of three steps: mixing, pressing, and drying.
The preparation of urea/HAP was carried via simple impregnation process. In a typical experimental procedure, the as-
prepared HAP (2 g) were firstly dispersed in distilled water (8 mL) and sonicated for 45 min to achieve a homogeneous
white dispersion. The resulting HAP suspension was slowly added to a fully saturated aqueous solution of urea (8 ml)
under vigorous stirring at 25 ◦ C for 12 h. The resulting suspension was allowed to settle and the excess liquid was
decanted. The precipitate was filtered, washed repeatedly with distilled water to remove unreacted urea and finally dried
in a vacuum oven at 50 ◦ C to remove excess water. The urea/HAP powder was characterized using XRD and FTIR.
A series of slow-release fertilizers with different coating type were prepared at laboratory scale using urea/HAP powder
as the base fertilizer and sugarcane bagasse (SCB), cellulose and lignin as a wood-derived coating. In a typical procedure,
a predetermined amount of the SCB was introduced in the above-prepared urea-modified HAP aqueous dispersion and
the mixture was allowed to soak for 2 h at room temperature. The resulting mixture was introduced in a cylindrical
mold and then pressurized up to 10 bar and converted into cylindrical pellets of approximately 1 cm of diameter.
Different trials were carried out at 3, 5, 7, 9 and 10 bars respectively for 10 min to determine the optimum pressure
allowing better cohesion of the fertilizer components. The slow-release behavior of the as-prepared fertilizers pellets
was determined after being dried overnight at 60 ◦ C. The same procedure was repeated for the preparation of all the
encapsulating material studied in this research particularly cellulose and lignin. The weight ratio between urea-modified
HAP and the encapsulating material (70/30wt%) was the same for all produced fertilizers. The produced composite
fertilizers were designated as urea/HAP-SCB, urea/HAP-CMF and urea/HAP-lignin for urea-modified HAP encapsulated
by sugarcane bagasse, cellulose microfibrils and lignin, respectively. For comparison, a blank sample with only urea-
modified hydroxyapatite, codded as urea/HAP, was also prepared under the same conditions. The digital images of the
urea/HAP-SCB, urea/HAP-Lig. and urea/HAP-CMF fertilizes are shown in Fig. 1.

2.5. Characterization techniques

FTIR spectra were collected using an ABB Bomem FTLA 2000 spectrometer fitted with attenuated total reflectance (ATR)
accessory. The solid samples were analyzed in a spectral region between 4000 and 400 cm−1 with a 16 cm−1 resolution,
while the obtained spectra were averaged over 32 scans. Thermal stability analysis of the samples was performed on TA
Q500 apparatus. About 20 mg of the sample was heated at a heating rate of 10 ◦ C/min, from room temperature up to 800 ◦ C
under air atmosphere. patterns were recorded on a Bruker AXS D-8 diffractometer using Cu-Kα radiation (λ = 0.154 nm)
in Bragg–Brentano geometry (θ –2θ ). SCB, lignin and cellulose microfibrils morphology was examined using a scanning
electron microscopy (FEI Quanta 200). Zeta-potential of the unmodified hydroxyapatite and the conveniently modified
hydroxyapatite was monitored in water at pH = 7 using Zetasizer Nano ZS (Malvern Instruments, UK) instrument. A
minimum of 3 measurements readings were recorded for each sample.
The release rate of urea as a function of time for each prepared fertilizer was examined at room temperature following
the method adapted from Tomaszewska and Jarosiewicz with slight modifications (Tomaszewska and Jarosiewicz, 2002).
Before release experiments, the total nitrogen content of each formulation was determined by the Kjeldahl method (ASTM
International, 2015). Briefly, a known mass of each encapsulated fertilizer pellets was placed in a beaker containing 50
mL of water. The beakers were properly covered and incubated for different periods at room temperature. Measurements
 C.E. Elhassani, Y. Essamlali, M. Aqlil et al. / Environmental Technology & Innovation 15 (2019) 100403 5

were taken at an interval of 24 h by drawing 5 mL of the solution from the beaker followed by addition of another 5
mL to keep the volume of the solution constant. Pure urea was also tested as a control experiment. The release rate was
estimated as the amount of urea released after time ‘‘t’’ in relation to the initial concentration of this component in the
fertilizer. The amount of urea released in water was determined by UV–Vis spectrophotometry according to the method
reported by Basova et al. (2011). This method involves several steps: First, 5 mL aliquot of sample free from solid matter
was transferred to a 25 mL volumetric flask containing 10 mL of p-dimethylamino benzaldehyde (DMABA) reagent with
a concentration of 20 g/L; then 5 mL of acetic acid (CH3 COOH) was added and stirred vigorously followed by the addition
of 5 mL of hydrochloric acid (0.6M); the total volume of solutions was 25 mL. After 5 min of stirring, the color of the
solution turned into yellow in which the color intensity is related to the concentration of the urea in the solution. The
absorbency of the sample solution at 420 nm was compared against a blank solution. Calculations were then performed
according to the calibration curve of urea.

3. Results and discussion

The physical aspect of the sugarcane bagasse (SCB), alkali-treated bagasse (ATB) and cellulose microfibrils (CMF) is
shown in Fig. 2 (a, b and c). Visually, the SCB (Fig. 2a) is mainly composed of yellow-brown fibers in which each fiber is
constituted of several fibrils. The compact structure of SCB originated from the fact that the fibrils are associated in small
bundles and cemented by non-cellulosic compounds which resulted in an alignment in the fiber axis direction as shown
by SEM analysis (Fig. 3d). Alkali treatment of the raw SCB fibers resulted in the formation of yellow colored ATB fibers
(Fig. 2b). The gravimetric analysis revealed that this treatment yielded about 45wt% of ATB. This chemical treatment leads
to a partial elimination of the whole non-cellulosic components, particularly the lignin, the hemicelluloses, and the pectin.
After the bleaching treatment, the bleached cellulose fibers (Fig. 2c) show a clear white color, confirming that the residual
non-cellulosic elements were totally removed during the bleaching treatment. This bleaching treatment resulted also in
a partial defibrillation of fibers into individual smaller cellulose microfibrils. The bleaching treatment yielded about 33%
of white cellulose fibers in regard to the initial amount of SCB.
The morphological aspect of the raw SCB, ATB, and CMF samples was studied by scanning electron microscopy (SEM).
From SEM micrographs of raw SCB, ATB and CMF illustrated in Fig. 2(d, e and f), changes in the morphology of raw SCB can
clearly be seen after alkaline treatment and bleaching. Among all the analyzed samples, SCB exhibited the highest fibers
diameter (181−236 µm) and each fiber is mainly composed of several fibrils associated in small bundles and linked by
non-cellulosic compounds giving rise to a typical highly compact architecture of cell walls (Fig. 2d). Moreover, the surface
of untreated SCB fibers presented a smoother surface because of the presence of waxes. Once the hemicellulose and lignin
were removed by washing and alkaline treatment, the SCB fibers were fragmented into individual microfibrils as it can
be seen from the micrograph shown in Fig. 2e. The diameter of the isolated microfibers was found to be 12−20 µm.
Moreover, the chemical structure of the treated fibers becomes more organized than that of the raw SCB. However, after
the bleaching treatment, the micrographs show an aggregated structure of the microfibrils, forming a highly entangled
soft-flat shape (Fig. 2f) due to the high amount of free hydroxyl groups in the isolated bleached cellulose fibers. These
microfibrils were released and individualized after removal of all non-cellulosic compounds, especially the lignin and
hemicellulose molecules. The figure showed that fibers were separated into individual fibers with a diameter below
12 µm.
FT-IR spectra of untreated SCB, extracted lignin and bleached cellulose fibers are depicted in Fig. 3(a–c). The FTIR
spectrum of untreated SCB (Fig. 3a) showed several characteristic peaks at around 3322, 2893, 1732, 1596, 1454, 1242
and 1023 cm−1 , which are attributed to the stretching vibration of -OH groups of cellulose, and the C-H stretching of
cellulose, acetyl and uronic ester groups of hemicelluloses, C=C stretching vibrations of aromatic ring in lignin also
observed in Fig. 3b, C-H deformation of lignin or hemicelluloses, -COO out of plane stretching vibration of acetyl groups in
hemicelluloses or the aryl group in lignin and C-O-C stretching vibration of the skeletal ring of pyranose, respectively (Neto
et al., 2013; Han et al., 2013). After delignification and bleaching treatments, the FTIR spectrum of the bleached cellulose
(Fig. 3c) revealed that the intensity of the peaks located at 1596 cm−1 , 1454 cm−1 and 1242 cm−1 was decreased or rather
fully disappeared in the spectrum of the bleached cellulose fibers (Fig. 3c), thus, indicating the total extraction of lignin and
hemicelluloses molecules by water-washing and alkaline treatment. In addition, the FTIR spectrum of bleached cellulose
shows a typical characteristic peak at 902 cm−1 associated to the β -glycosidic linkages of glucose ring in cellulose (Wong
Sak Hoi and Martincigh, 2013).
The X-ray diffraction patterns of untreated SCB, alkaline treated SCB and bleached cellulose are shown in Fig. 4. These
patterns are typical of semi-crystalline materials with an amorphous broad hump and crystalline peaks. As it can be
observed, all the analyzed samples exhibited typical cellulose diffraction peaks, where the highest peak corresponds to
the 002 crystallographic planes. In addition, the peaks intensity became more intense upon different chemical treatments
suggesting that the crystallinity of these materials was enhanced. The degree of crystallinity of these fibrous materials,
determined by X-ray diffraction, was found to increase from 19% to 36% to 45% for SCB, alkaline treated SCB and bleached
cellulose, respectively. This increase of the crystallinity index in the treated samples was attributed to the successful
removal of the amorphous fractions mainly hemicelluloses and lignin. It should be noted that lignin molecule is amorphous
in nature and the corresponding XRD pattern do not show any characteristic diffraction peaks (spectra not shown in Fig. 4).
The HAP and the conveniently modified urea/HAP were characterized by means of XRD and FTIR techniques. The typical
XRD patterns of these materials are depicted in Fig. 5. As shown in this figure, the XRD pattern of the HAP (Fig. 5a) is
6 C.E. Elhassani, Y. Essamlali, M. Aqlil et al. / Environmental Technology & Innovation 15 (2019) 100403

Fig. 2. Photographs of (a) raw SCB (b) ATB and (c) CMF samples and SEM micrographs of (d) raw SCB, (e) ATB and (f) CMF samples.

Fig. 3. FT-IR spectra of (a) untreated SCB fibers, (b) lignin molecule and (c) bleached cellulose fibers.

in perfect agreement with that reported in the JCPDS file N◦ 008-4759, corresponding to the well crystalline HAP with a
hexagonal structure. All the diffraction peaks of the HAP sample are similar in position and intensity to those ascribed
in this file. The XRD pattern of the urea/HAP exhibited typical diffraction peaks related to the HAP structure and the
tetragonal urea (marked by* in Fig. 5b) according to the JCPDS file N◦ 083-1436, suggesting the successful immobilization
of the urea on the HAP support. It should be noted that the diffraction peaks of the urea persisted even after thorough
washing, thus indicating the occurrence of strong interaction between urea and HAP. Moreover, it is worth noting that
no significant shifting in the positions of the HAP peaks was observed before and after impregnation with urea, which
suggests that the overall structure of the HAP was not substantially modified. In addition, the diffraction patterns of
urea/HAP-SCB (Fig. 5c) revealed the presence of typical diffraction peaks of HAP and urea. However, no typical diffraction
peaks of SCB were detected due to the low crystallinity of this fibrous residue. For urea/HAP-Cellulose composites, the XRD
pattern in Fig. 5d is quite similar to that corresponding to the urea/HAP added to it the typical characteristic diffraction
peaks of crystalline cellulose (marked by + in Fig. 5d). The decrease in the intensity of the cellulose peaks in the XRD
pattern suggests that urea/HAP is the dominating component of the composite.
 C.E. Elhassani, Y. Essamlali, M. Aqlil et al. / Environmental Technology & Innovation 15 (2019) 100403 7

Fig. 4. XRD patterns of (a) untreated SCB fibers, (b) alkaline treated SCB and (c) bleached cellulose fibers.

Fig. 5. XRD patterns of (a) HAP, (b) urea/HAP, (c) urea/HAP encapsulated by SCB and (d) Urea/HAP encapsulated by cellulose fibers.

The thermal stability of the urea/HAP and urea/HAP encapsulated by sugarcane bagasse and cellulose was investigated
by TGA. The thermogravimetric (TG) curve of the urea-modified hydroxyapatite shown in Fig. 6a exhibited the typical
thermal decomposition profile of urea. As shown in this figure, the thermal decomposition of the urea starts before
the melting point (132.5 ◦ C) until its complete oxidation at around 500 ◦ C and about 67.5wt% residue was left at this
temperature, thus indicating that approximately 32.5wt% of urea was successfully immobilized on the HAP support. It
should be mentioned that the thermal decomposition of urea has been accelerated when it was supported by the HAP,
suggesting that the HAP could not only act as a simple support but also as a catalyst for thermal degradation of urea.
TGA was also used to check the thermal stability of urea/HAP-SCB and urea/HAP-Cellulose composites compared to
the fibrous materials SCB and CB, which enabled us to observe some interactions between composite’s constituents. TG
profiles of the composite fertilizers are shown in Fig. 6b. For SCB, two distinct weight losses can be differentiated and
assigned to the decomposition of the different fractions mainly non-cellulosic and cellulosic components, with peaks
around 214–375 ◦ C and 400–420 ◦ C respectively. Instead of two degradation processes for SCB, the thermal degradation
of bleached cellulose (BC) occurred in only one single step (at a maximal temperature of 260 ◦ C) mainly due to the
depolymerization and thermal decomposition of pure cellulose. It is noteworthy to mention that thermal degradations of
the produced urea/HAP-SCB and urea/HAP-Cellulose correspond to the superposition of the thermal degradation processes
of urea and SCB and urea and cellulose, respectively.
8 C.E. Elhassani, Y. Essamlali, M. Aqlil et al. / Environmental Technology & Innovation 15 (2019) 100403

Fig. 6. TGA curves of (a) pure urea and urea/HAP and (b) urea/HAP encapsulated by SCB and Urea/HAP encapsulated by cellulose microfibrils.

FTIR analysis was conducted in order to better understand the nature of the interactions between the urea and HAP.
The possible interfacial interaction between urea and HAP were monitored through the possible bands shifting. The FTIR
spectra of HAP, as shown in Fig. 7b, exhibited typical characteristic bands of apatite structure. The sharp and intense
absorption bands located at 1090 and 1020 cm−1 are attributed to phosphates groups (PO4 )3− stretching. The signals at
964 and 470 cm−1 are due to P-O symmetrical and asymmetrical stretching vibrations, respectively. And the peaks at
600 and 561 cm−1 are characteristic of P-O deformation vibrations (Wang et al., 2007). The band observed at 3571 cm−1
was characteristics of the stretching vibration of the hydroxyl groups of HAP structure. The Fourier transform infrared
spectra of urea and urea coated hydroxyapatite are shown in Fig. 7(a,c). As shown in this figure, the Fourier transform
infrared spectrum of the urea coated HAP showed N-H stretching and deformation bands at about 3432 and 1613 cm−1
respectively. C=O stretching peak was observed at around 1673 cm−1 and the C-N stretching peak at approximately
1457 cm−1 . It should be mentioned that the absorption bands observed at around 3426 and 1588 cm−1 , pertaining to
stretching and deformation vibrations of N-H bond in pure urea, were shifted to higher frequencies to 3432 and 1613 cm−1
in the spectrum of urea coated HAP, thus suggesting the occurrence of strong hydrogen bandings between N-H groups of
urea and O-H groups of HAP. According to the FTIR results, it can be concluded that urea is bonded to the HAP through its
carbonyl and amine groups (Kottegoda et al., 2017). The FTIR spectrum of the pressurized urea coated mesoporous HAP
encapsulated by SCB fibers (Fig. 8) revealed the presence of typical characteristic peaks of urea and HAP, together with
those ascribed to the skeletal structure of the SCB carbohydrate. The absorption peaks at 2923 and 2853 cm−1 correspond
to the alkyl and aromatic CH2 stretching vibrations, the C-H bending vibration at 1459 cm−1 overlaps with the absorption
peak of the N-C-N of the urea and the absorption peak of C=O stretching vibration is seen at 1728 cm−1 .
The possible interfacial interaction between HAP and urea was further evidenced by measuring the zeta potential of
the HAP before and after coating by urea. The obtained results showed that the surface of HAP is negatively charged
(−23.1 mV) and becomes positively charged (+40.1 mV) after impregnation with the urea. This observation confirms
the presence of ammonium groups of the urea on the surface of the HAP, corroborating, hence, the existence of strong
interactions between urea and HAP. According to the FTIR and zeta potential results, it can be established that the urea
 C.E. Elhassani, Y. Essamlali, M. Aqlil et al. / Environmental Technology & Innovation 15 (2019) 100403 9

Fig. 7. FTIR spectra of (a) urea (b) HAP and (c) urea coated HAP.

Fig. 8. FTIR spectra of urea coated HAP encapsulated by SCB pressurized at: (a) 2 bars, (b) 4 bar, (c) 6 bars, (d) 8 bars and (e) 10 bars.

has coordinated with HAP through its oxygen and nitrogen atoms in C=O and N-H groups of urea molecule, respectively,
resulting in the formation of several binding modes of unequal binding strengths.
In order to find out the optimum pressure allowing the achievement of the maximum loading of organic nitrogen,
the prepared slow release urea coated HAP encapsulated by SCB fertilizer were pressurized at different pressure levels
ranging from 2 to 10 bar and were subsequently digested and analyzed for N content quantification. According to the
obtained results (Table 1), the optimum pressure required to achieve the maximum nitrogen loading is about 6 bars. The
samples pressurized above this pressure have a very low N content compared to those obtained at very low-pressure
level (Table 1) probably due to the destruction of cell walls cavities of the SCB at high pressure. These findings are in
agreement with the results of Kottegoda et al. (2011).
In our first release experiment, we first examined the effect of the calcination temperature of the HAP support on
the release pattern of the urea-modified hydroxyapatite encapsulated by SCB fibers. In Fig. 10, the release rate of the
as-prepared slow release fertilizer is plotted versus the calcination temperatures of the HAP support. It is obvious that
calcination temperature of the HAP support is an important factor affecting the interactions urea-HAP as well as the urea
release pattern. The amount of urea released increases with increasing calcination temperature in a specific period of
time. Indeed, at low calcination temperature, the release pattern of urea was much slower than that obtained at high
calcination temperatures. As shown in Fig. 9, the fertilizer-based HAP calcined at 500 ◦ C has released out more than
10 C.E. Elhassani, Y. Essamlali, M. Aqlil et al. / Environmental Technology & Innovation 15 (2019) 100403

Table 1
The N content in Urea coated HAP encapsulated by SCB pressurized at different
pressure values.
Urea/HAP and SCB Shaping pressure Nitrogen content
ratio (wt%) (bar) (mgN2 /g)
Urea/HAP-SCB 1 70 2 72.33
Urea/HAP-SCB 2 70 4 82.13
Urea/HAP-SCB 3 70 6 84.93
Urea/HAP-SCB 4 70 8 74.66

Fig. 9. Effect of calcination temperature of the HAP on the pattern of urea release of the urea/HAP-SCB fertilizer in distilled water compared to pure
urea.

35.97, 54.25 and 95.86% within 15, 30 and 45 days (Fig. 9), respectively, while the fertilizer-based HAP calcined dried
at 100 ◦ C released approximately 24.71, 44.37 and 94.81% of urea within 15, 30 and 45 days, respectively. The fastest
urea release rate was obtained for fertilizers prepared using HAP calcined at 500 ◦ C. Accordingly, it was suggested that at
low calcination temperature, the urea molecules are attached to the HAP through relatively strong bonds which reduces
the urea’s release rate, while at higher calcination temperature, the interactions between urea and HAP was not strong
enough to slow urea’s release rate. Such results were expected since the surface area, pore size and pore volume of the HAP
support were significantly reduced from 82.34 m2 /g, 21.23 nm and 0.406 cm3 /g to 59.41 m2 /g, 17.63 nm and 0.212 cm3 /g,
respectively, by increasing the calcination temperature from 100 to 500 ◦ C.
The release pattern of urea, urea/HAP and urea/HAP encapsulated by SCB, cellulose and lignin fertilizers in water were
investigated using a rapid water release test to check their potential application as slow release fertilizers. Urea release
profiles in water of the three produced fertilizers compared to those corresponding to pure urea and urea coated HAP are
shown in Fig. 10. It should be noted that this full immersion experiment is very aggressive and may not correspond to real
conditions in the field, where the moisture level is limited by the water retention capacity of the soil; never the less, this
method allows us to accurately compare the release behavior of the as-prepared fertilizers under accelerated conditions.
According to the data in Fig. 10, the urea release rate of the urea/HAP fertilizer was significantly reduced compared to that
of pure urea in which the dissolution occurred quickly (in just < 1 day), due to the solution saturation around the urea
granule. Furthermore, it was observed that all the produced fertilizers, even non-encapsulated urea coated HAP, displayed
a retard in the urea release compared to pristine urea. In this case, the presence of the HAP causes the fertilizer to release
the urea in a slower manner due to the strong interfacial interactions between urea and HAP. The slow release behavior of
the urea-HAP system is comparable to that reported for urea-montmorillonite composites (Pereira et al., 2012; Park et al.,
2004) and urea HAP composite obtained by simple impregnation method (Kottegoda et al., 2011) or synthesized using a
one-step in situ approach (Kottegoda et al., 2017). The decrease in urea’s release rate, when supported on the HAP, was
mainly due to the relatively strong interactions established between the N-H of the urea and C=O of the HAP. Moreover,
as shown in Fig. 10, the different encapsulated fertilizers exhibited a significantly reduced release pattern over time owing
to the microstructural differences among the used wood species. Indeed, once the urea-modified HAP are encapsulated by
SCB and its derivatives, the fertilizer components were stored within the wood species cavities which become reservoirs
for storage of urea-modified HAP and results in a significant reduction of the release properties and the encapsulated
urea/HAP system liberate the urea in a more controlled manner than that with the urea-modified HAP system. For the
pellets encapsulated by SCB, a marked slow release of urea occurred incrementally during the experiment compared to
 C.E. Elhassani, Y. Essamlali, M. Aqlil et al. / Environmental Technology & Innovation 15 (2019) 100403 11

Fig. 10. Pattern of urea release from different urea/HAP encapsulated fertilizers in distilled water compared to pure urea.

urea/HAP. For example, during the first 30 days of complete immersion in water, the release rate was relatively slow
in urea/HAP-SCB, only 59% of urea was released compared to the urea/HAP system (78.8%). In the case of the fertilizer
encapsulated with cellulose, the rate of urea release was significantly slower than that of fertilizer encapsulated by SCB.
After 40 days of complete immersion in water, only 53.48% of urea was released compared to 84.14% for the fertilizer
encapsulated by SCB. The urea modified-HAP encapsulated by lignin biopolymer showed the slowest urea release of the
three-wood species studied. After 30 days of incubation, urea modified-HAP encapsulated by lignin biopolymer, urea
modified-HAP encapsulated by cellulose fibers and urea modified-HAP encapsulated by SCB fibers were found to have
released only about 59, 45.48 and 21.64%, respectively, of their impregnated urea. The differences in the release rate
of urea were associated to the porous structure of the woodchip species used as coating material. Furthermore, such
difference was expected since the lignin molecule is well known to exhibit a hydrophobic nature, thus this molecule
soaks and absorbs water slowly and produce a retard in the check-out process of urea contained in the fertilizer pellets.
We assumed that the mechanism of the urea release from the produced composite fertilizers occurs in three steps.
First, water penetrates into the cavities of the woodchips species wherein the urea-modified hydroxyapatite is stored. The
urea is successively desorbed from the HAP support through the weakening of the interfacial interaction between urea
and HAP and dissolved in the solution and finally, the solution containing dissolved urea diffuses through the woodchip
cavities due to the driving force of the diffusion phenomenon.
It is well known that the support plays an important role in the success of urea adsorption (Kottegoda et al., 2017;
Pereira et al., 2012). It can act as a simple dispersant or by developing strong interactions with the immobilized urea
component. Besides the hydroxyapatite, fluorapatite (FAP) is another calcium phosphate compound capable of undergoing
strong interaction with urea molecule owing to its reactive surface functional groups. In our experimental setup, we also
compared the slow release behavior of the composite manufactured by encapsulating urea coated HAP by SCB, cellulose
and lignin and those produced by encapsulation urea coated FAP into SCB, cellulose and lignin compounds. It should be
noted that the FAP-based slow release fertilizers were prepared following the same procedure adopted for the preparation
of the HAP-based ones. The pattern of urea release in water as a function of time fora period of 60 days was then
investigated and summarized in Fig. 11.
In the case of urea-modified fluorapatite encapsulated by SCB, 79.73% of urea was released after 30 days of testing. In
comparison with the urea/HAP encapsulated by SCB (Fig. 10), the release of urea was increased by about 20.73%. The shape
of the release curves suggests that the release of urea was clearly influenced by the support used for the immobilization of
urea. In addition, for urea/FAP encapsulated by lignin, the urea release rate was slowing down within the first 25 days of
testing (Fig. 11), probably due to the hydrophobic nature of lignin, since then, the release pattern become similar to that
observed for the fertilizer encapsulated by SCB. As seen in Fig. 11, the amount of urea released from the developed slow
release fertilizers was not the same for each encapsulating material. The rates of urea release from urea/FAP-cellulose and
urea/HAP-SCB during the first three weeks of incubation were greater than that for urea/FAP-lignin (Fig. 11). For example,
with the urea/FAP-lignin, at approximately 20 days after incubation, 32% of urea still remaining in the urea/FAP-lignin
fertilizer compared to 21.97% and 11.33% for urea/FAP encapsulated by SCB and cellulose, respectively. As explained earlier,
this effect was associated to the porous structure of the woodchip species used as a coating material, more precisely the
size of the wood cavities as well as the morphology of the coatings. The fertilizer encapsulated by lignin was probably
more compact and hydrophobic, thereby hindering the diffusion of water into the fertilizer pellets thus slowing down the
dissolution of urea and its transfer outside the encapsulated fertilizer.
12 C.E. Elhassani, Y. Essamlali, M. Aqlil et al. / Environmental Technology & Innovation 15 (2019) 100403

Fig. 11. Pattern of urea release from different urea/FAP encapsulated fertilizers in distilled water compared to pure urea.

4. Conclusion

In our research work, we successfully synthesized novel composite fertilizers composed of urea, hydroxyapatite
and woodchip species with different formulations. Our findings suggest that the immobilization of urea up on HAP
leads to a functionalized fertilizer with slow release properties owing to the strong interfacial interactions established
between amine functions of the urea and carbonyl groups present on the surface of HAP. The non-encapsulated urea/HAP
proved advantageous slow release pattern but was not as effective as the woodchips encapsulated pellets fertilizers.
Water immersion experiments demonstrated that the urea-modified HAP-encapsulated by sugarcane bagasse, cellulose
and lignin composite displays a slow and sustained release of nitrogen compared to the urea-modified HAP over a
period of 60 days. Moreover, it was demonstrated that the nature and calcination temperature of the support as well
as the microstructure of the encapsulating material are major factors affecting the release rate of urea. The urea/HAP
encapsulated by lignin was found to be versatile and smart slow release fertilizer capable of supplying the enormous
demand for novel efficient nitrogen fertilizers due to their efficiency and ease processing.

Acknowledgment

Funding

The financial assistance of the MAScIR Foundation, Morocco toward this research is hereby acknowledged. We
acknowledge also the financial assistance of the CNRST, Morocco (Grant PPR2 Project, Category B).

Declaration of competing interest

The authors declare no competing financial interest.

References

Ahmed, S.A., Chun, S.K., 2007. Effects of environmental friendly slow-releasing woodchip fertilizer on cabbage production. For. Stud. China 9, 246–250.
Ahmed, S.A., Kim, J.I., Park, K.M., Chun, S.K., 2011. Ammonium nitrate-impregnated woodchips: a slow-release nitrogen fertilizer for plants. J. Wood
Sci. 57, 295–301.
Akelah, A., 1996. Novel utilizations of conventional agrochemicals by controlled release formulation. Mater. Sci. Eng. 4, 83–98.
Al-Zahrani, S.M., 2000. Utilization of polyethylene and paraffin waxes as controlled delivery systems for different fertilizers. Ind. Eng. Chem. Res. 39,
367–371.
Aqlil, M., Nzenguet, A.M., Essamlali, Y., Snik, A., Larzek, M., Zahouily, M., 2017. Graphene oxide filled lignin/starch polymer bionanocomposite:
structural, physical and mechanical studies. J. Agric. Food Chem. 65, 10571–10581.
ASTM International, 2015. Standard Test Method for Total Nitrogen in Organic Materials by Modified Kjeldahl Method, ASTM E258.
Basova, E.M., Bulanova, M.A., Ivanov, V.M., 2011. Photometric detection of urea in natural waters. Moscow Univ. Chem. Bull. 66, 345–350.
El Miri, N., Abdelouahdi, K., Zahouily, M., Fihri, A., Barakat, A., Solhy, A., El Achaby, M., 2015. Bionanocomposite films based on cellulose nanocrystals
filled polyvinyl alcohol/chitosan polymer blend. J. Appl. Polym. Sci. 132, 42004.
Fernández-Pérez, M., Garrido-Herrera, F.J., González-Pradas, E., Villafranca-Sánchez, M., Flores-Céspedes, F., 2008. Lignin and ethylcellulose as polymers
in controlled release formulations of urea. J. Appl. Polym. Sci. 108, 3796–3803.
Gosselink, R.J.A., Abächerli, A., Semke, H., Malherbe, R., Käuper, P., Nadif, A., Van Dam, J.E.G., 2004. Analytical protocols for characterisation of
sulphur-free lignin. Ind. Crops Prod. 19, 271–281.
 C.E. Elhassani, Y. Essamlali, M. Aqlil et al. / Environmental Technology & Innovation 15 (2019) 100403 13

Guo, M., Liu, M., Liang, R., Niu, A., 2006. Granular urea-formaldehyde slow-release fertilizer with superabsorbent and moisture preservation. J. Appl.
Polym. Sci. 99, 3230–3235.
Han, J., Zhou, C., Wu, Y., Liu, F., Wu, Q., 2013. Self-assembling behavior of cellulose nanoparticles during freeze-drying: Effect of suspension
concentration, particle size, crystal structure, and surface charge. Biomacromolecules 14, 1529–1540.
Kandil, E.A., Fawzi, M.I.F., Shahin, M.F.M., 2010. Delayed release of n-fertilizers. J. Amer. Sci. 6, 195–201.
Kottegoda, N., Munaweera, I., Madusanka, N., Karunaratne, V., 2011. A green slow-release fertilizer composition based on urea-modified hydroxyapatite
nanoparticles encapsulated wood. Curr. Sci. India 101, 73–78.
Kottegoda, N., Sandaruwan, C., Perera, P., Madusanka, N., Karunaratne, V., 2014. Modified layered nanohybrid structures for the slow release of urea.
Nanosci. Nanotechnol.-Asia 4, 94–102.
Kottegoda, N., Sandaruwan, C., Priyadarshana, G., Siriwardhana, A., Rathnayake, U.A., Arachchige, D.M.B., Kumarasinghe, A.R., Dahanayake, D.,
Karunaratne, V., Amaratung, G.A.J., 2017. Urea-hydroxyapatite nanohybrids for slow release of nitrogen. ACS Nano 11, 1214–1221.
Mandal, A., Chakrabarty, D., 2011. Isolation of nanocellulose from waste sugarcane bagasse (SCB) and its characterization. Carbohydr. Polymers 86,
1291–1299.
Naz, M.Y., Sulaiman, S.A., 2016. Slow release coating remedy for nitrogen loss from conventional urea: A review. J. Control Release 225, 109–120.
Neto, W.P.F., Silvério, H.A., Dantas, N.O., Pasquini, D., 2013. Extraction and characterization of cellulose nanocrystals from agro-industrial residue-soy
hulls. Ind. Crop. Prod. 42, 480–488.
Ni, B., Liu, M., Liu, S., Xie, L., Wang, Y., 2011. Environmentally friendly slow release nitrogen fertilizer. J. Agric. Food Chem. 59, 10169–10175.
Park, M., Kim, C.Y., Lee, D.H., Choi, C.L., Choi, J., Lee, S.R., Choy, J.H., 2004. Intercalation of magnesium-urea complex into swelling clay. J. Phys. Chem.
Solids 65, 409–412.
Pereira, E.I., da Cruz, C.C.T., Solomon, A., Le, A., Cavigelli, M.A., Ribeiro, C., 2015. Novelslow release nanocomposite nitrogen fertilizers: the impact of
polymers on nanocomposite properties and function. Ind. Eng. Chem. Res. 54, 3717–3725.
Pereira, E.I., Minussi, F.B., da Cruz, C.C.T., Bernardi, A.C.C., Ribeiro, C., 2012. Urea-montmorillonite extruded nanocomposites: A novel slow-release
material. J. Agric. Food Chem. 60, 5267–5272.
Sempeho, S.I., Kim, H.T., Mubofu, E., Pogrebnoi, A., Shao, G., Hilonga, A., 2015. Encapsulated urea-kaolinite nanocomposite for controlled release
fertilizer formulations. J. Chem. 2015, 1–17.
Shankarappa, T.H., Geeta, G.S., 2013. Alkali and autohydrolysis pretreatments for effective delignification and recovery of cellulose and hemicellulose
in selected agro residues, Karnataka. J. Agric. Sci. 26, 67–75.
Sun, J.X., Sun, X.F., Zhao, H., Sun, R.C., 2004. Isolation and characterization of cellulose from sugarcane bagasse. Polym. Degrad. Stab. 84, 331–339.
Tomaszewska, M., Jarosiewicz, A., 2002. Use of polysulfone in controlled-release NPK fertilizer formulations. J. Agric. Food Chem. 50, 4634–4639.
Trenkel, M.E., 2010. Slow-and Controlled-Release and Stabilized Fertilizers: An Option for Enhancing Nutrient Use Efficiency in Agriculture. IFA,
International Fertilizer Industry Association, Paris.
Wang, A., Liu, D., Yin, H., Wu, H., Wada, Y., Ren, M., Jiang, T., Cheng, X., Xu, Y., 2007. Size-controlled synthesis of hydroxyapatite nanorodsbychemical
precipitationin the presence of organic modifiers. Mater. Sci. Eng. 27, 865–869.
Wong Sak Hoi, L., Martincigh, B.S., 2013. Sugar cane plant fibers: Separation and characterisation. Ind. Crops Prod. 47, 1–12.
Xiaoyu, N., Yuejin, W., Zhengyan, W., Lin, W., Guannan, Q., Lixiang, Y., 2013. A novel slow-release urea fertiliser: Physical and chemical analysis of
its structure and study of its release mechanism. Biosyst. Eng. 115, 274–282.
Yamamoto, C.F., Pereira, E.I., Mattoso, Mat sunak, L.H.C.a.T., Ribeiro, C., 2016. Slow release fertilizers based on urea/urea–formaldehyde polymer
nanocomposites. Chem. Eng. J. 287, 390–397.