Chemical Engineering Journal 428 (2022) 131102

Contents lists available at ScienceDirect

Chemical Engineering Journal

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

Development and application of fish scale wastes as versatile

natural biomaterials
Di Qin a, 1, Shichao Bi a, b, 1, Xinguo You a, Mengyang Wang a, Xin Cong a, Congshan Yuan a,
Miao Yu a, Xiaojie Cheng a, *, Xi-Guang Chen a, b, *
a
College of Marine Life Science, Ocean University of China, Qingdao 266003, Shandong Province, PR China
b
Qingdao National Laboratory for Marine Science and Technology, Qingdao 266000, Shandong Province, PR China

A R T I C L E I N F O A B S T R A C T

Keywords: Fish scale is a unique natural biomaterial mainly composed of type I collagen and hydroxyapatite. The highly
Fish scales ordered hierarchical microstructures and composition of fish scales is similar to human hard tissues, which
Collagen endow its good biocompatibility, degradability, and excellent mechanical properties to fish scales for potential
Hydroxyapatite
applications including in tissue engineering, biological filling, sewage processing and flexible electronics.
Hierarchical microstructure
However, the practical application of fish scales is relatively limited owing to a lack of commercial value, thus
Tissue engineering
leading to serious problems including waste of materials and pollution of the environment. Therefore, the
conversion and reuse of fish scales could significantly reduce the pressure on the natural environment and bring
additional commercial value. Herein, we systematically introduce and discuss the composition and highly or­
dered hierarchical microstructures of fish scales, followed by the summary of their applications in wound
healing, bone repair, cell scaffold, cartilage repair, cornea regeneration, electrocatalysis, adsorption, sewage
purification, biological filling and bionics. In addition, we also discuss the commercial perspective of fish scales
and their derivatives in the near future.

1. Introduction
With the rapid development of materials science and technology,
artificial materials including polycaprolactone (PCL), polyglycolic acid
(PGA) and polylactic acid-glycolic acid copolymer (PLGA) have been
approved by the Food and Drug Administration (FDA) for a variety of
biological applications [1,2]. However, concerns regarding the envi­
ronmental pollution of these polymers significantly restrict their further
application in clinic [3–5]. In recent year, natural products including
proteins (such as collagen, gelatin, hyaluronic acid, keratin and silk),
polysaccharides (such as alginate, cellulose, chitin, chitosan chondroitin
sulfate and starch), terpenes (such as natural rubber) and lipids have
emerged as a novel choice for biomedical applications owing to their
great biocompatibility [5–7]. Biopolymers are reported to play impor­
tant roles in various biological organism. For instance, cellulose supports
the higher plants structure. Chitin forms exoskeletons of several mol­
lusks. Keratin provides heat insulation for hair. Collagen is the me­
chanical support of connective tissue. Silk is the strength fulcrum of
spider web [8]. Among various biopolymers, fish scales could meet the
multi-functional requirements of promoting and protecting fish via the
highly ordered microstructures [9], which may find broad applications
as novel engineering biomaterials with advanced properties [10].
Fish scales are the mineralized plates covering the dermis layer of the
epidermis as the unique skin protection for fish. Fish scales are
composed of various useful materials including ~41%-45% organic
components (collagen, fat, lecithin, sclerotin, vitamins, etc.), ~38%-
46% inorganic components (calcium-deficient hydroxyapatite, calcium
phosphate, etc.) and trace elements such as magnesium, iron, zinc,
calcium [11,12]. The component and structure of fish scales are similar
to human bones, teeth and mineralized tendons [13], which contributes
to them with great potential in antioxidant activity, wound healing
promotion, microbial proliferation inhibition, bone regeneration and
other physiological functions [14–16]. Fish scales usually contain three
different structural layers: Confinement layers are composed of
randomly distributed collagen fibers (30–50 nm) doped with hydroxy­
apatite crystals, which is considered as the first protective barrier and

* Corresponding authors at: College of Marine Life Science, Ocean University of China, 5# Yushan Road, Qingdao 266003, PR China.
E-mail addresses: xjcheng@ouc.edu.cn (X. Cheng), xgchen@ouc.edu.cn (X.-G. Chen).
1
These authors contributed equally to this work.

https://doi.org/10.1016/j.cej.2021.131102
Received 5 April 2021; Received in revised form 1 June 2021; Accepted 25 June 2021
Available online 2 July 2021
1385-8947/© 2021 Elsevier B.V. All rights reserved.
D. Qin et al.
the highly mineralized area in the fish scale [17]. External elasmodine
(basal plate, EE), as a laminate, is composed of unidirectional aligned
type I collagen fibers with a diameter between 100 and 160 nm [18,19].
In this layer an orthogonal plywood-like structure was formed by stag­
gered stacking and the thickness of the layer varies among different fish
species [20,21]. Based on the content of mineral, the elasmodine is often
divided into EE and internal elasmodine (IE) [9]. The mineralization
process exists throughout the life cycle of fish, and collagen fibers are
synthesized from subcutaneous nucleated cells which further form
plywood [21]. In addition, the c-axis orientation of the outer acicular or
lamellar hydroxyapatite crystal is parallel to the c-axis of the inner
collagen fiberboard crystal [22]. This highly ordered natural multi-
layered composite structure could significantly improve the mechani­
cal properties of fish scales [18,23–25], thus providing inspiration for
the development of various bionic functional materials.
In fact, fish scales are often considered as discarded waste from the
aquaculture sector such as fish canning, filleting, salting and smoking
[26]. It is estimated that about 7.2–12 million tons of fish waste are
discarded every year in the world. It should be noted that there is no
commercially utilization of fish scale waste produced in fish markets at
present [27,28]. The landfill disposal of fish scale waste may cause
serious environmental pollution problems and lead to a waste of re­
sources [29]. Therefore, converting waste fish scales into functional
materials (such as hydroxyapatite, collagen, polysaccharide and chitin)
[30–32] could minimize the impact on environmental pollution and
bring huge commercial value [33–35]. In addition, a full understanding
of the composition, structure and mechanical properties of fish scales
would provide a theoretical basis for the design and manufacture of next
generation bionic flexible bulletproof clothing [36]. In this study, the
composition, hierarchical microstructure, mechanical properties and
applications of fish scales are reviewed (Scheme) to provide some in­
sights for the recycling of fish scales and the development of novel
functional materials.
Scheme. 1. Schematic diagram of fish scales structures and their application in biomedicine such as wound healing, bone repair, cell scaffold, cartilage repair and
other fields like electrocatalysis and adsorption.
2
Chemical Engineering Journal 428 (2022) 131102
2. Hierarchical structure of fish scales
Fish scales, the solid plates attached to the skin of fish, exhibit a
unique balance of flexibility, strength and toughness, which is essential
to provide protection without hindering the movement of the fish [37].
The teleost fish scales are mainly composed of calcium-deficient hy­
droxyapatite inorganic phase, type I collagen, lecithin organic phase and
some other trace elements [12], exhibiting a highly ordered natural
micropatterned composite structure.
Fish scales may vary in shapes and ornamentations due to various
factors such as fish species, habits, ages and sizes, but it exhibits similar
characteristics in the overall structure [38]. The scales surface can be
divided into three areas: anterior, posterior and lateral [39]. The ante­
rior area of the scales is covered by the posterior area of the scales and
embedded in the skin. The whole fish scale is divided into different
scalloped areas by radial grooves. Interestingly, unlike Carassius auratus
scales, the scale ridges on the Channa argusand and C. carpio communis
scales appear only in the anterior area (Fig. 1A) [21,39,40]. The radial
grooves (radii) and circular ridge lines (circuli) of anterior and lateral
regions are formed around the central region (called focus) [41]. In cross
section, there are controversial views on the microstructure of fish
scales. Some researchers believe that fish scales consist of mineralized
bone layers and flexible collagen layers. The outer bone layer is arranged
in an ordered and continuous structure, which is rough and highly
mineralized, while the inner collagen layer is in a thin-layer plywood
structure with low degree of mineralization [42]. The thickness ratio of
fish scales bone layer/collagen layer in central position varies among
different fish scales, such as 1:1 of Carassius auratus, 2:1 of Mugil cephalus
and Pristipomoides sieboldii, and 1:3 of Cyprinus carpio (Fig. 1B), and the
thickness of the collagen layer gradually decreases to 0 at the anterior
and posterior locations of the scales [41].
Others believe that the fish scales can be divided into three areas of
different thickness in the longitudinal direction: the outer limiting layer
(LL), external elasmodine (EE) and internal elasmodine (IE) (Fig. 1C)
[43]. The LL with a random network structure is consisting by acid
glycoproteins, which corresponds to the relative mineralization. The EE
D. Qin et al. Chemical Engineering Journal 428 (2022) 131102

Fig. 1. Fish scales morphology and hierarchical structure. A) The morphology of (a) a fresh Carassius auratus fish scale with three regions and (b) the relative
orientation of fish scale and the fish body [21]. B) Hierarchical structures of (a) Cyprinus carpio, (b) Carassius auratus, (c) Mugil cephalus and (d) Pristipomoides sieboldii
fish scales [46]. C) Comparison of the Arapaima gigas, the tarpon (Megalops atlanticus) and the carp (Cyprinus carpio) fish scales. (a) SEM image of the cross-section of a
representative tarpon scale denoting the three distinct regions including the limiting layer (LL), external elasmodine (EE) and internal elasmodine (IE). (b) Com­
parison of single scales patterns from the arapaima, tarpon and carp (left to right) [20].

layer in which needle-like hydroxyapatite (HAP) crystals hybridize with
randomly arranged collagen fibers is first mineralized, followed by the
LL and IE are mineralized, respectively. In particular, the IE are
composed of multi-layer structure [44]. In each lamella, the highly or­
dered collagen fibers are closely aligned in one direction, and HAP
crystals are parallel to collagen fibrils [22]. In addition, collagen fibrils
are arranged vertically between adjacent layers to form plywood like
structure [23]. The average rotation angle between adjacent collagen
fiber layers is slightly different among various fish species. Fang et al.
found that the collagen fiber between adjacent layers in Carassius aur­
atus scales overlapped in a spiral ~ 60◦ instead of the general orthogonal
plywood structure or double stranded plywood structure, which was
similar to the inner layer of Arapaima gigas scales with the angle of 60-
75◦ [21,37,45], while the striped bass (Morone saxatilis) scales are
orthogonal plywood structure at 90◦ [17]. Besides, researchers
compared the hierarchies of four teleost fish scales from different water

Fig. 2. Comprison of the microstructural characteristics and the collagen fiber ply orientations of the fish scales. A) SEM image from a tarpon scale in the fish scale
middle region. B) Stacking sequence of the plies for the carp, tarpon and arapaima (from top to bottom). Scale bar = 50 μm. C) Comparison of a) total thickness, b)
limiting layer thickness and c) external elasmodine ratio of carp, tarpon and arapaima scales. External elasmodine ratio represents the ratio of the EE thickness to the
total elasmodine thickness [20].

3
D. Qin et al. Chemical Engineering Journal 428 (2022) 131102

regions in New Zealand and found that the minimum spiral orientation
angle between the adjacent collage piles exists in Cyprinus carpio scales
(45◦ ), and Mugil cephalus scales show the maximum spiral orientation
angle (80◦ ), while the spiral angle of collagen lamellae in Carassius
auratus and Pristipomoides sieboldii scales are is 60◦ [46].
In addition, Murcia et al compared the lamination pattern and
microstructure of scales from the Cyprinus carpio (carp), Megalops
atlanticus (tarpon), and the Arapaima gigas (arapaima) and found that the
thickness of scales varied at different positions among the three fish. The
mineralization degree of LL and EE layers is responsible for the differ­
ence in the thickness of fish scales. The LL thickness is almost uniform in
carp scales over the body, while in arapaima and tarpon LL decreases
and increases from head to tail, respectively (Fig. 2C). In EE, the
thickness of mineralized layer is significantly higher than non-
mineralized collagen layer, and arapaima scales have a thicker EE
layer. Moreover, Arapaima gigas and tarpon scales exhibited a twisted
plywood structure and repeated the stacking sequence every 5 plies,
while arapaima scales exhibit a double twisted structure with repeated
stacking sequence every 2 plies (Fig. 2) [20].
3. Mechanical behavior
Many creatures wear body armor to resist threats throughout its
natural evolution. The teleost is a typical example with lightweight,
flexible, transparent and collagen-based “plate-like” elastic scales for
advanced hydromechanical properties and resistance to penetration
[47,48]. The scales covering the surface of fish skin undergo millions of
years of evolution to show an amazing arrangement of various hierar­
chical structures. Those fish scales with a highly ordered microstructure
exhibit an excellent combination of mechanical strength and toughness
[49,50]. For example, Megalops Atlanticus (Atlantictarpon) fish scales
are anisotropic in mechanical behavior and have the highest mechanical
strength along the fish length [13]. The inner collagen layer composed of
collagen fibers acts as a soft cushion for the fish scales, exhibiting
amazing tensile strength and protecting the fish’s skin from the the at­
tacker’s teeth. The LL, which is highly mineralized by apatite, serves as
the first barrier against predator threats and plays an important role in
resistance to piercing [9].
The outstanding mechanical behavior of fish scales is closely related
to its highly ordered microstructure [51]. The protection mechanisms of
elasmoid scales in various fishes species, such as arapaima [42,52], red
sea bream [23], bass [53] and tarpon [13], could be attributed to the
following aspects: the LL and external layer are well-mineralized, which
can provide the fish scales with sufficient hardness to resist attackers;
the soft collagen enables huge deformation capacity to dissipate the
stored elastic energy through the collagen layer rotation and separation,
the collagen fibers stretching/compression, the fibrillar layering and
bridging [54]. The fish scales, which exhibited a twisted plywood
structure composed of lamellae of collagen fibrils in different orienta­
tions, and their highly mineralized outer layer fractured and exfoliated
first during tensile loading (Fig. 3A). With the increasing of loading, the
fish scales Bouligand-type lamellar internal base acts synergistically
through deformation mechanisms such as lamellar rotation, fibrillar
deformation and slippage, and the lamellar separation to effectively
dissipate the stored elastic energy and impart excellent toughness to the
fish scale (Fig. 3B&C) [54]. The defense strategy of fish scales could
provide ideas for the design and manufacture of new biomimetic
flexibility.

Fig. 3. Adaptive deformation mechanism of fish scales and their tensile behavior in different orientations and tensile load conditions. A) Schematic diagram of
adaptive deformation mechanism of fish scales under tensile loading condition. Fish scale is fractured and exfoliated with its highly mineralized outer layer during
tensile loading (a). With increasing loading, the lamellar inner base of fish scales Bouligand layer effectively dissipates stored elastic energy through deformation
mechanisms such as laminar rotation, fibrillar deformation and slippage, and lamellar separation (b-f). B) Uniaxial tensile stress–strain curves and representative
pictures of fish scales in different directions and displacements. C) Fish scales tensile behavior in different orientations and tensile load conditions [54].

4
D. Qin et al.
4. Whole fish scale application
The global fish processing industry generates a large number of fish
wastes every year, of which fish scales would account about 4% of the
share [27,28]. As a natural renewable resource, fish scales are easy-
made biological materials. Therefore, many researchers have devoted
to improve the commercial value of fish scales in a simple processing
and transforming procedure for potential applications as bone tissue
engineering materials, heavy metal ions and color dyes biosorbents,
catalysts and fillers, as showed in Fig. 4.
4.1. Bone tissue engineering
Fish scales are mainly composed of calcium-deficient hydroxyapatite
and type I collagen [12]. In addition, the presence of essential anions
such as Cl- and F- and cations such as Mg2+, Al3+, Sr2+, Zn2+, K+, and
Na+ as trace elements in fish scales could improve their biological per­
formance in bone repair in biomedicine values [55]. For instance, fish
scales not only have good biocompatibility with MC3T3-E1 cells, but its
microstructure could guide the cells proliferation and migration along
the channels of fish scales [21]. Natural or synthetic scales are widely
used as bone tissue engineering materials because of their high simi­
larity with human bones and teeth [23]. For example, fresh decellular­
ized grass carp fish scales have good biocompatibility with myoblastic
cell line C2C12 in vitro; meanwhile, bone nails made of decellularized
scales could further promote the New Zealand rabbits’ femoral fractures
healing. After 8 weeks of implantation, the bone nail fused with the
surrounding bone tissues and gradually synthesized new extracellular
matrix around the implant [56]. In addition, fish scales are also used to
prepare composite scaffold in combination with other polymer materials
bone tissue engineering. Kara et al. added Sparus aurata fish scales
powder in wet electrospun poly (3-hydroxybutyric acid-co-3-hydrox­
yvalerate) nanofibers, and successfully produced a three-dimensional
cotton wool-like nanofiber as composite scaffold for bone filling. The
composite scaffold not only has a high porosity, but the addition of fish
scales significantly improved the scaffold’s mechanical properties, bio­
mineralization tendency, cell viability and alkaline phosphatase activ­
ity, which significantly promoted the expression of type I collagen in
Fig. 4. Summary schematic of the fish scales and its hierarchical structures applications in bone tissue engineering, biological fillers, heavy metal ions and toxic color
dyes adsorption, and catalysis and energy materials.
5
Chemical Engineering Journal 428 (2022) 131102
MG-63 cells [57]. Chitosan/fish scale (CH/FS) scaffolds were prepared
by combining Sparus aurata scales powder with natural polymer chito­
san using ultrasound, freeze-drying and other techniques. The me­
chanical properties and biodegradation of CH/FS scaffolds was
promoted within creasing the amount of fish scales added. The results of
ALP activity and biomineralization showed that CH/FS scaffolds could
enhance osteogenic differentiation activity while no cytotoxicity to
Saos-2 cell line [58].
4.2. Biological filler
The reasonable conversion of fish scales can not only produce lighter
and cheaper composite materials, but also improve the properties of
polymers and realize its commercial value [59]. Chiarathanakrit et al.
calcined the fish scale powder at 700 ◦ C for 3 h and added it to the starch
foam to obtain a more expanded starch foam. The maximum load stress
was increased by nearly 50% with the addition of fish scale powder [60].
Furthermore, using fish scale waste as fillers to fill epoxy matrix com­
posites can improve its tensile strength and increase the biodegradation
rate of polypropylene and reduce the wear rate of epoxy matrix com­
posites [59,61–63]. In addition, fish scales have also attracted increasing
attention in paper industry. Ural et al. reported that fish scales could be
used as filler material for fabrication of brighter adjusted by controlling
the fish scale powder and input amount with appropriate particle size
[64]. The composite of catla fish scales and polypropylene by twin-screw
extrusion technology could improve the young’s modulus, bending
strength, density and hardness, and reduce the tensile strength, tensile
fracture and thermal deformation temperature of the composite mate­
rials [65]. In the poly(3-hydroxybutyrate-co-3-hydroxyvalerate) (PHBV)
composites containing fish scales (PHBV/FS), the tensile strength and
water resistance of the composite was significantly enhanced. At the
same time, the composite materials have no effects on the normal pro­
liferation and life cycle of fibroblasts, and have also showed good anti­
oxidant and antibacterial properties [57], indicating the great potential
of PHBV/FS composite material as a medical biological filler [66].
D. Qin et al. Chemical Engineering Journal 428 (2022) 131102

4.3. Fish scale-based biosorbent Table 1

Summary of different fish scale-based biosorbent processing ways and its
Fish scales are mainly composed of collagen fiber-hydroxyapatite applications.
complex, which have certain adsorption properties for metals and Fish species Processes Morphology Adsorbate Ref.
dyes and are a potential biological adsorbent [67]. The adsorption Pogonias 1) Tap water washing Powder Acid Red 1 [69]
properties of fish scales may be closely related to the chemical functional comes and air-dried; (AR1);
groups with dye binding ability, such as amide, carbonate, carboxyl, 2) Ground and sieved Acid Blue 45
carbonyl, hydroxyl and phosphate [68]. Therefore, the fish scale-based using 40, 60, 100, (AB45);
200 mesh filter. Acid Yellow
bioadsorbents obtained from different fish species using different pro­
127
cessing ways exhibit various forms, which show potential adsorption (AY127)
functions for heavy metal ions and toxic synthetic dyes, as listed in Oreochromis 1) Sodium Powder Reactive [67]
Table 1. niloticus hypochlorite (0.1%, Blue 5G
Heavy metal pollution caused by the global industrialization and v/v) and deionized (RB5G)
water washed in
mechanization development poses a serious threat to chronic environ­ turn;
mental problems and human health [81]. More and more studies have 2) 60 ◦ C dried;
shown that fish scales and their derivatives could effectively adsorb 3) Ground and sieved
heavy metal ions in wastewater or sediment. Fresh fish scales are using 6, 12, 16, 32,
100, 150 and 325
washed and dried in sequence and ground into fish scale powder with a
mesh filter;
particle size of 125–200 μm; then the samples are activated by sulfuric 4) or HCl (0.1 M)
acid and sodium hydroxide respectively, washed and neutralized treated
repeatedly with deionized water, and finally dry it to produce living fish Distilled water Complete fish [70]
scales (Fig. 5A). The activated fish scale powder was further used in the washed and 60 ◦ C scale
dried
chromium (III) removal experiments. The results showed that under the
Leporinus 1) Running water Powder (100 μm) Anionic [68]
activated fish scale powder 0.8 g, a solution pH of 5.0, a contact time of elongatus washed and NaOH Remazol
90 min, and initial chromium (III) ion concentration150 mg/L, fish (pH 9.0, 4 h)
scales could achieve 99.75% adsorption of chromium (III) metal ions immersed;
2) Double-distilled
[75]. Nanoscale zero-value iron was formed on fish-scale-based porous
water washed and
carbon of tilapia. This scale derivatives could remove Cr (VI) ions from 60 ◦ C dried
wastewater efficiently and rapidly, and the added of irons given the Labeo rohita 1) Distilled water Powder (100 Malachite [71]
material good magnetic separation performance [79]. In addition, the washed and 70 ◦ C to125 μm) Green (MG)
adsorption material of cerium supported on high porous carbon from dried;
2) ground and sieved
fish scales carp (Cyprinus carpio), nano-magnetic Fe3O4 material
Sardinella 1) Running water, Powder (0.088 to Reactive [72]
impregnated on fish scales and Oreochromis niloticus scales combined brasiliensis bathed in 0.1 M/L 0.177 mm) Turquoise
with dolomite all had been developed, which exhibited highly efficiency HCl solution and Blue 15
and spontaneous adsorption capacity for arsenate ions, copper ions and distilled water (RTB15);
washed again; Reactive
zinc ions in automobile battery wastewater under specific pH condi­
2) 80 ◦ C dried; Red 120
tions. It is worth mentioning that fish scales derived biosorbent mate­ 3) Ground and (RR120)
rials could be used for adsorption–desorption cycles [76,77,80]. The fish sieved;
scale bioadsorbent obtained by hydrothermal blending of fish scale and 4) Distilled water
acid also has sufficient adsorption capacity for cadmium and lead heavy washed and 80 ◦ C
dried again
in the sediment [78].
Tilapia 1) Tap water washing Powder Ponceau 4R [73]
In modern society, a large number of toxic synthetic dye wastewater and sun-dried;
is produced and discharged. Many research reports showed that fish 2) NaOH heated in an
scale, a natural, low-cost, environmentally friendly and degradable oil bath;
3) Water washing
biomaterial, could effectively absorb anions (acid dyes, direct dyes and
and 50 ◦ C dried;
reactive dyes), cations (basic dyes), non-ionic (disperse dyes) and other 4) Ground and sieved
dyes. Thermodynamic studies have showed that the biological adsorp­ using 160 mesh filter
tion process had spontaneous endothermic properties, and labeo rohita Oreochromis 1) Tap water Powder (0.2 mm) Azo dye [74]
scales could effectively adsorb malachite green dye [71]. Leporinus niloticus washing; (AB113 dye)
2) Hot and cold
elongatus and Sardinella brasiliensis scales has been utilized as biomass
deionized water
adsorbent to realize anionic dye remazol (blue, red and yellow) washed in turn;
adsorption and recovery [68,72]. Both Ribeiro et al. and Zhu et al. have 3) 50 ◦ C dried for 48
successfully adsorbed reactive blue 5G and ponceau 4R dyes by using h;
Oreochromis niloticus fish scales, and confirmed that the adsorption 4) Ground and sieved
using 200 mesh filter
process mainly through the surface adsorption of hydroxyapatite and Unknown 1) Water washing, Powder (125 to Chromium [75]
electrostatic adsorption mechanisms of collagen (Fig. 5B&C) [67,73]. soaked and 65 ◦ C 200 μm) with (III) metal
Interestingly, the Sebastes marinus scales could not only adsorb heavy drying for 24 h; honeycomb-like ions
metal ions and toxic dyes, but also effectively adsorb and recover prawn 2) Ground and sieved structures or
using mesh filte open pores
cyanin and other natural active components from marine industrial
(125–200 μm);
wastewater [82]. The fish scale bioadsorbent exhibits broad application 3) Acid-base
prospects in the adsorption of heavy metal ions, toxic dyes and the re­ activation in turn
covery of active ingredients. It provides an economic, environment using sulphuric acid
friendly and easily available natural renewable material for color dyes (0.1 M) and sodium
hydroxide (0.1 M);
and heavy metal ions adsorption in industrial wastewater. 4) Filter and wash to
(continued on next page)

6
D. Qin et al. Chemical Engineering Journal 428 (2022) 131102

Table 1 (continued ) porous structure and nitrogen doped surface properties of HLPC, the Pt/
Fish species Processes Morphology Adsorbate Ref. HLPC catalyst has higher current density, lower overpotential and
enhanced catalytic activity for oxidation–reduction reaction via direct
neutral using
distilled water, 80 ◦ C
four electron pathway [84]. Natural phosphate can catalyze trans­
dried. esterification of methyl benzoate with alcohol in heterogeneous media.
Rutilus kutum 1) Tap water and Flake-like micro- Cu2+ ion [76] Thermo-gravimetric analysis and X-ray diffraction (XRD) results showed
sodium hypochlorite particles that waste tilapia scales with hydroxyapatite as the main inorganic
(5 wt%) washing, (105–500 μm)
component could be successfully converted into β-triphosphate after
distilled water
washing and 80 ◦ C calcination at 600 ◦ C for 2 h; SEM showed that the morphology was
dried; porous fiber layer structure. Reusability results confirmed that the pre­
2) Ground and sieved pared catalyst with high specific surface area could be reemployed up to
using 35–140 mesh six times [85]. Ho et al. used composite material of titanium dioxide and
filte;
3) Nanomagnetic
fish scales as a photocatalyst to degrade methyl orange under sunlight.
(Fe3O4) loaded on The results showed that TiO2/FS had a synergistic effect in photo­
the surface using catalytic degradation, which means that fish scales could enhance the
chemical photocatalytic degradation of methyl orange. Interestingly, as the fish
precipitation
scale content in the composite increases, its photocatalytic activity will
technique
Cyprinus 1) Hydrogen High porous As(V) ions [77] decrease instead [86].
carpio peroxide (5%) and grain; Biomass (including bagasse, fish scale, rice, soybean, etc.) is called
deionized water Surface area: potential sustainable energy materials, which can be directly converted
washing and dried; 1067 m2/g; into heat, electricity or solid, liquid or gas fuel. It is the raw material for
2) Ground and sieved Pore volume:
using mesh filter 0.64 cm3/g;
electric energy production, fuel cell and gas turbine steam power gen­
(50–100 μm); Mean pore eration [87]. Fish scale biomass is characterized by high calorific value,
3) Cerium diameter:2.5 nm low sulfur content, high calcium content, etc. Therefore, it could be used
nanoparticles loaded Zeta potential: as a potential raw material for clean energy production through the heat
and precarbonized − 17.4 mV
conversion process (combustion and pyrolysis). Therefore, dissolving
under nitrogen
atmosphere at 330 ◦ C protein-rich fish and poultry manure with 0.75 M sodium hydroxide
for 3 h; electrolyte could form half of the oxidation and reduction battery,
4) KON activation thereby successfully manufacturing a rechargeable protein battery
and calcination [88,89]. In addition, the nitrogen-doped fish scale grade carbon, a fish
under nitrogen
scale derivative, has a high specific surface and a multi-layer porous
atmosphere
Labeo rohita 1) Water washing Power particles Cadmium [78] structure, which shows good stability in ionic liquid electrolytes and
and 60 ◦ C dried; (100, 300, and (Cd) and conventional media, and is a high-capacity negative electrode material
2) Ground and sieved 500 μm) lead (Pb) for lithium-ion batteries [90]. In addition, fish scales are also used to
using mesh filter; ions
improve the electrochemical performance of lithium-sulfur batteries
3) HCl (0.1 M)-NaOH
(0.1 M) chemical or after decalcification, pre-carbonization, and KOH activation treatments.
hydrothermal The decalcified sponge-like nitrogen-doped porous carbon with highly
physical activation hierarchical porous structure could not only provide enough accom­
4) Water washing modation space, but also improve the permeability of the electrolyte and
and 60 ± 5 ◦ C dried
promote the rapid transfer of lithium ions in Li-S batteries. Moreover,
Tilapia 1) 330 ◦ C Lump with Cr (VI) [79]
precarbonization and hierarchical the nitrogen doping also enhances the chemisorption of polysulfides
900 ◦ C activation lamellar porous [91]. Therefore, the environmentally friendly and economical decal­
with potassium carbon cified fish scale-based sponge-like nitrogen-doped porous carbon
hydroxide (KOH);
comprehensive strategy may become a novel trend in the development
2) Mixed with iron
chloride to form
of lithium-sulfur battery cathode materials.
paste;
3) 850 ◦ C calcinated 5. Fish scale derived hydroxyapatite application
for 2 h under N2
environment
Oreochromis 1) Distilled water Complete fish Zinc ions [80]
Hydroxyapatite, an inorganic material with good biocompatibility, is
niloticus washing and 60 ◦ C scale with widely distributed in the hard tissues of the organism and has a sup­
dried; heterogeneous porting effect on its main structure [92,93]. HAP has important appli­
2) Dolomitic lime cation values and significances in biomedical fields such as bone repair,
hybrid
tissue engineering biomaterials and adsorbents due to its good
biocompatibility [94–96], as showed in Fig. 6.
4.4. Catalysts and energy materials Recently, natural hydroxyapatite has been extracted from a variety
of biological wastes, such as eggshells, bovine bones and fish scales
In the polymer electrolyte membrane fuel cell, the ideal support [97–99], which is characterized by the advantages of biological safety
material for the electrocatalyst used in the oxidation–reduction reaction and low cost compared to chemical synthesis. For example, Mondal et al.
process should be characterized by suitable specific surface area and explored the technology of extracting hydroxyapatite from fresh water
surface chemistry, high stability, high conductivity, and suitable (Labeo rohita) scales after deproteinization system (HCl and NaOH so­
porosity [83]. Therefore, the nitrogen-doped hierarchical lamellar lution treatment), drying at 60 ◦ C and calcining at different tempera­
porous carbon (HLPC) synthesized with fish scales as support material tures. The results of X-ray diffraction showed that the hydroxyapatite
inspired by the natural hierarchical microstructure of fish scales was extracted from fish scale had one characteristic peak, which confirms the
used for platinum nanoparticle electrocatalysts toward the oxygen complete crystallization of the powder [100]. Deb et al. further explored
reduction reaction. Due to the high BET specific surface area, layered the effects of the three different deproteinization system pretreatment
processes on the physical and chemical properties and biological activity

7
D. Qin et al. Chemical Engineering Journal 428 (2022) 131102

Fig. 5. Preparation of bioadsorbent from waste fish scales. A) The fabrication processes of the fish scale adsorbent from Arbaminch Lake Ethiopia [75]. B) Schematic
of the Tilapia fish scale adsorbent fabrication and adsorption mechanism for Ponceau 4R. C) SEM images of untreated Tilapia fish scales (a and b), fish scale adsorbent
(c) and adsorbed Ponceau 4R fish scale adsorbent (d) [73].

Fig. 6. Summary schematic of the fish scale-derived hydroxyapatite applications in bone tissue engineering, periodontal repair, heavy metal ions and toxic color dyes
adsorption fields.

of hydroxyapatite extracted from Catla catla scales. XRD, FTIR,
elemental analysis and SEM results showed that the high crystallinity
hydroxyapatite could be obtained only by acid pretreatment for 24 h,
and it exhibited outstanding physical and chemical properties and good
biological activity in simulation body fluid (SBF) solution [101].
In addition, Huang et al. used enzymatic hydrolysis to extract hy­
droxyapatite from tilapia scales [98]. The cleaned and crushed fish
scales were hydrolyzed with 1% protease N and 0.5% flavor enzymes for
2.5 h and 0.5 h under the optimal pH and temperature conditions,
respectively. The dried residue was calcined at 800 ◦ C for 4 h to obtain

8
D. Qin et al.
nano granular hydroxyapatites. The calcium-phosphorus ratio (Ca/P) of
the extracted product is 1.76, the average particle size is 719.8 nm and
the porosity and surface roughness increase after calcination at high
temperature. In addition, the prepared materials could promote the
osteogenic differentiation and mineralization of MG-63 cells under the
osteogenic induction culture conditions [98]. Hydroxyapatite have also
been successfully extracted from carp fish (Cyprinidae) scales using ionic
liquid pretreatment technology. After cleaning, drying and grinding, the
fish scales were treated with 1-butyl-3-methylimidazolylacetate in
boiling water for 12 h, adding equal volume of water and adjusting the
pH of the solution to be alkaline. After centrifugation, the collected
hydroxyapatite showed microcrystalline hydroxyapatite particles with
different shapes, with a Ca/P ratio of 1.60 and an average particle size of
1870 nm and showed good biocompatibility to human embryonic kid­
ney cells (HEK) and Epidermoid carcinoma cell line (A431) [27].
Sathiskumar et al. used the Cirrhinus mrigala scales as the raw material
and synthesized green nano-hydroxyapatite (nHAp) with a Ca/P molar
ratio of 1.67 using a simple alkaline heat treatment process. Compared
with commercial HAp, nHAp has better cell activity and alkaline phos­
phatase (ALP) activity on MG-63 cells [102].
5.1. Bone tissue engineering
Hydroxyapatite has attracted much attention in bone tissue engi­
neering due to its biocompatibility, bone conductivity, bioactivity, and
non-biological toxicity [100]. The researchers compared the physico­
chemical, bioactivities and biological properties of hydroxyapatite
derived from fish scale with synthesized hydroxyapatite by chemical
solution coprecipitation. The results proposed that the hydroxyapatite
extracted from fish scale had more potential application value in bone
tissue engineering [103]. The results of bioactivity test showed that after
being incubated for 7 days in SBF, more new apatite could be formed on
the surface of hydroxyapatite extracted from fish scales than synthesized
[103]. Moreover, many researchers have confirmed that hydroxyapatite
extracted from fish scales characterized by good biocompatibility, pro­
moting cell migration, adhesion and increasing ALP activities of osteo­
blasts [21,100,103]. Mondal et al. successfully synthesized functional
hydroxyapatite with porous structure and good mechanical properties
using Labeo rohita and Catla catla fish scales. In vitro cells experimental
results showed that the hydroxyapatite scaffolds exhibited good cell
adhesion and no cytotoxicity to MG-63 osteoblasts with the increase of
time, whilst it also showed good bone conductivity in animals [104].
Deb et al. confirmed that hydroxyapatite extracted from the Puntius
conchonius scales had good mechanical strength and porosity, and also
exhibited good degradation performance. In addition, in vitro bioactivity
analysis confirmed that bone like apatite would be successfully formed
on the fish scale hydroxyapatite scaffold surface after 28 days of SBF
immersion [105].
In addition, many researchers combined hydroxyapatite extracted
from fish scales with other polymer materials to give its new functions
for bone scaffolds. Pon-On et al. prepared hydroxyapatite from fresh­
water fish (P. jullieni) scales and compounded with PLA/chitosan to
prepare composite bone scaffold materials with good mechanical
properties and microporous structure. In vitro studies found that the
composite scaffold had good biocompatibility for UMR-106 cells, and
improved cell viability and ALP activities [106]. Deb et al. extracted
hydroxyapatite from the dried Labeo rohita fish scales decalcified by
alkaline method and calcinated at 1000 ◦ C for 3 h. Finally, a porous bone
scaffold of hydroxyapatite and polyethylene glycol composite was suc­
cessfully prepared by solvent casting. The results of mechanical strength
test and SEM analysis showed that the composite scaffold had ideal
mechanical properties. Results showed that the composite scaffold ex­
hibits interconnected pores with a pore size greater than 167 μm and
ideal mechanical properties, which were more suitable for the bone cells
growth and provided potential application prospects for bone tissue
engineering and segmental bone defects regeneration [107].
9
Chemical Engineering Journal 428 (2022) 131102
5.2. Periodontal repair
Nano-hydroxyapatite has potential applications in enamel, bone
tissue regeneration and periodontal tissue regeneration [108,109].
Wijedasa et al. extracted hydroxyapatite from the Salmo salar scales and
Lutjanus campechanus scales respectively and blended it with functional
nano peptide fibers to prepare a new peptide based composite scaffold
for periodontal tissue regeneration. The results showed that the hy­
droxyapatite from Salmo salar scales exhibited higher mechanical
strength and Young’s modulus. In vitro experiments proved that the
scaffolds made by hydroxyapatite extracted from two different scales
could support cell proliferation and gingival fibroblast formation, but
the cells in Lutjanus campechanus scales hydroxyapatite scaffolds were
more orderly arranged, which was more conducive to osteoblast dif­
ferentiation [110], suggesting that it has important application value in
periodontal tissue regeneration.
5.3. Hydroxyapatite-based biosorbent
Hydroxyapatite is considered to be a promising adsorption material
due to its low water solubility, good availability, low cost, good stability,
and its strong adsorption capacity [34,44,111,112]. Chai et al. success­
fully synthesized AuNPs/HAP hybrid structure composite in the hier­
archical HAp nanostructures of natural tilapia fish scale templates,
which were carried out by the Au3+ ion chemisorption, reduction and
calcination processes. The AuNPs/HAp hybrid nanostructure exhibited
good protein adsorption behavior at the biological bovine serum albu­
min (Ab) concentration regions (1.5 M in the cell culture medium and
15.1 M in human blood) (Fig. 7A) [44]. Uzunoğlu et al. found that
extracted hydroxyapatite from the Dicentrarchus labrax scales could
achieve 291.5 mg/g adsorption capacity for acid blue 121 dye and could
be used for adsorption–desorption cycles [34]. In addition, the hy­
droxyapatite extracted from tilapia fish scales was combined with chi­
tosan or adhesive (1 wt% PVA and PEG) to prepared composite scaffold,
which exhibited good selective adsorption on lead ions [112,113]. Liaw
et al. prepared a hydroxyapatite/chitosan (HA/CS) composite scaffolds
with hierarchical porous structure using low-cost and environmentally
friendly hydroxyapatite extracted from Tilapia (Oreochromis mossambi­
cus) scales and chitosan by freezing casting and crosslinking (Fig. 7B). By
controlling the cooling rate of freeze casting, HA/CS composite scaffolds
with unidirectional channel structure of 10–100 μm were respectively
obtained at the cooling rate of 2 ◦ C/min, which was presented in Fig. 7C.
The adsorption kinetics results showed that the HA/CS composite scaf­
fold formed at a cooling rate of 2 ◦ C/min had a great removal capability
for different initial concentrations of Pb (П) whereas the decomposition
of samples deposited in 1000 mg/L Pb (П) solution is slightly faster
(Fig. 7D) [113], suggesting that fish scale-based composites were
effective enough to reduce the toxic heavy metal ions in industrial
wastewater (Fig. 4B). Kongsri et al. successfully prepared nano hy­
droxyapatite from Tilapia nilotica fish scales by alkaline heat treatment,
and confirmed that FHAP nanocrystalline (1520 nm) has better
adsorption capacity for Se (IV) ion in selenite than CHAP (commercial
hydroxyapatite) and CS [114]. Sricharoen et al. successfully obtained
nano hydroxyapatite (FHAP) from biowaste Tilapia scales using ultra­
sonic assisted method. Under ultrasonic condition, FHAP could effec­
tively remove Hg2+ from aqueous solution, and its maximum adsorption
capacity is 227.27 mg/g, suggesting that the FHAP could be an alter­
native adsorbent for the ultrasonic-assisted removal of Hg2+ in high
efficiency and within a very short period of time [115].
In conclusion, hydroxyapatite derived from fish scales of different
fish species using different synthesis/extraction methods including ionic
liquid pretreatment methods, alkaline heat treatment method and ho­
mogenous precipitation assisted with ultrasound energy method ex­
hibits different characteristics including porous structure, similar Ca/P
ratio with natural bone, excellent osteoconductivity and osteogenesis.
The natural fish scales show great markets and promising in future
D. Qin et al. Chemical Engineering Journal 428 (2022) 131102

Fig. 7. Preparation of fish scale derived-hydroxyapatite biosorbent with hierarchical porous structured and its application in heavy metal ion adsorption. A)
Schematic of AuNPs/HAp hybrid nanostructure preparation by AuNP-incorporated porous HAp derived from fish scale and subsequent Ab adsorption process [44]. B)
(a) Schematic of the HA/CS composite scaffold freezing casting process. Briefly, the pre-cooled HA/CS slurry at 4 ◦ C is poured into a PTFE mold of a specific shape,
and the size of the bracket channel is controlled by adjusting the cooling rate. After freeze-drying, crosslink with 1% glutaraldehyde for 2 h, and after fully replacing
the crosslinking agent with deionized water, the HA/CS composite scaffold is formed after dried at 60 ◦ C for 12 h. (b) The scheme of fixed bed process. (c) Photograph
and illustration of the inner and outer regions. C) The pore distribution (a) and the SEM images of outer region (b), inner region(c), interstitial particles (d) of HA/CS
composite scaffolds. D) SEM images of (a, c) outer region and (b, d) inner region for HA/CS scaffolds placed in 100 mg/L or 1000 mg/L Pb (II) solution for 10 min, 1
day, and 10 days [113].

biomedical including bone regeneration, cell scaffolds, cartilage resto­
ration and other fields such as electrocatalysis and adsorption applica­
tion, as summarized in Table 2. It is also beneficial for the full utilization
of resources and the sustainable development of the environment in the
future.
6. Fish scale collagen application
collagen in fresh water fish is higher than that in sea water fish. COL-I
derived from Rohu (Labeo rohita) and Catla (Catla catla) at a denatur­
ation temperature of 36.5 ◦ C was more similar to the denaturation
temperature of mammalian collagen, so it had good biomedical appli­
cation prospects [127]. At present, COL-I has been widely used in drug
delivery, skin replacement, soft tissue regeneration, sutures, and tissue
engineering matrix at present [128,129], as showed in Fig. 8.

Collagen, especially type I collagen (COL-I), as an extracellular ma­
trix plays an important role in cell adhesion, cell scalability and cell
growth [119]. Fish collagen has become a suitable substitute for
collagen in mammals (such as pigs, cattle, etc.) due to the low risk of
zoonosis [120]. Fish scales are mainly composed of COL-I and hy­
droxyapatite in a ratio of about 1:1 [23,121]. Compared with fish skin or
other fishery waste, fish scale could produce collagen with higher purity,
which may be a stable source of fish collagen [122]. COL-I in fish scales
is usually composed of three α subunits (2α1 + α2) [123], and the
peptide chains are combined with each other by covalent bonds,
hydrogen bonds, and van der Waals forces to form a right-handed
supercoiled structure [32]. COL-I structure is characterized by a tri­
peptide repeats Gly-X-Y, in which X and Y are frequently taken by
proline (Pro) and hydroxyproline (Hyp), respectively. The denaturation
temperature of COL-I is closely related to the content of Hyp [124], and
the higher the overall content of Hyp, the higher the thermal stability of
COL-I. The thermal stability of collagen is also related to the physio­
logical temperature of fish [125,126], so the collagen from tropical and
subtropical fish has higher thermal stability, and the thermal stability of
6.1. Corneal tissue engineering
The corneal stroma is composed of multiple layers, each layer of
COL- I fibers is closely arranged and parallel to each other. However, the
collagen is orthogonally oriented to form an orthogonal plywood
structure in the two adjacent collagen layers, which is presented in
Fig. 9A. This highly regulated three-dimensional collagen fiber
arrangement provides an important contribution to the strength and
transparency of the corneal stroma. Interestingly, the similar highly
ordered arrangement of collagen fibers is also observed on the substrate
of the teleost fish scales (Fig. 9B), which provides a theoretical basis for
the fish scale collagen in corneal engineering application [130]. More­
over, fish scales are considered to be the most promising biomaterials to
replace corneal stroma because of their strong regeneration ability and
low possibility of zoonosis. Fish scales collagen, a substitute for cornea,
has shown great application potential in the field of corneal engineering
due to its good biocompatibility, transparency and mechanical strength
[131,132]. The waste fish scales can still maintain its natural three-
dimensional and highly ordered micro pattern structure after

10
D. Qin et al. Chemical Engineering Journal 428 (2022) 131102

Table 2
Hydroxyapatite from fish scale with difference synthetic ways and its applications.
Fish species Synthetic ways Analysis Characteristics Applications Ref.

Labeo rohita; 1)Tap water washing 2) Thermo gravimetric analysis Crystallite size 76.62 nm; Tissue engineering [116]
Catla catla hydrochloric (TGA); Ca/P ratio 1.6; scaffold
acid (HCl, 1 N) and sodium XRD; Particle size 507 nm;
hydroxide (NaOH, 1 N) treated for FTIR; Around 30–35% porosity;
24 h; Particle sizes; Enhanced BMSCs cellular viability and
3) Distilled water washing and 60 ◦ C SEM; promoted cellular attachment and
dried; Cytotoxicity, cellular proliferation
4) Calcium chloride dehydrate proliferation and morphology
treated at 75 ◦ C and calcined at study
800 ◦ C for 1 h
Labeo rohita 1) Water washing and XRD; Similar characteristics to pure Porous HAp scaffold [100]
deproteinizing; FTIF; hydroxyapatite; for Wistar rat
2) Calcined at 700–800 ◦ C Field emission scanning electron 30% porosity and high compressive femoral defect
microscopy (FE-SEM) and strength;
Energy dispersive X-ray No cytotoxic effects on macrophage-like
spectroscopy (EDS); RAW cell line;
TEM; Good biocompatibility and supporting cell
Mechanical properties; lines to adhere and proliferate
Cytotoxicity (MTT assay)
Probarbus jullieni 1) Water washing and XRD; Flat-plate nanocrystal forms (width size bone scaffold or [103,106]
deproteinization using 4% FTIR; about 15–20 nm, length about 100 nm) regenerative
hydrochloric acid for 15 min; SEM; with porous morphology, large surface material in bone
2) Hydroxyapatite-rich slurry Transmission electron area and higher surface roughness; tissue engineering
obtained by hydroxide (NaOH) microscope (TEM); Ca/P ratio 2.01 (Ca-rich CaP);
treatment and filtration using 500 Mechanical properties; More new apatite formed after SBF in
μm membrane; EDS; incubation;
3) 100 ◦ C boiled for 30 min to Bioactivity, MTT assay Higher cell adhesion and proliferation on
deactivate the enzymes and dried at and ALP activity analysis the HA fish surface. Cells were able to
60 ◦ C spread.
Significant increases the osteogenic
activity
Labeo rohita and 1) Washed scales were washed with XRD analysis; Crystal structure similar to cortical bone; Bone tissue [104]
Catla catla HCl (1 N) to deproteinize; FTIR analysis; Ca/P ratio about 1.70–1.71; engineering due to
2) Acetic acid treatment to remove Field Emission FESEM with EDX 35% interconnected porosity; trauma
collagen fibers and 60 ◦ C dried; analysis; Better mechanical properties such as
3) Calcined at 1000 ◦ C TEM analysis; hardness (~1.08 GPa), compressive
Mechanical performance strength (~0.8 GPa) and tensile strength
analysis; (~187 MPa)
Cellular cytotoxicity and cell In vitro: No cytotoxic effects on MG63 and
proliferation (MTT assay and RAW 264.7 and significant increases the
LDH assay); cell adhesion and proliferation;
Histological analysis In vivo: Showing better osteo-conductive
characteristics
Puntius 1) Deproteinization using HCl (1 N) Thermogravimetric analysis Combining with PMMA matrix exhibits Potential bone [105]
conchonius for 24 h; (TGA); porous morphology with interconnected substitute material in
2) Dried at 50 ◦ C for 12 h and FTIR; pores; tissue engineering
calcination at 1000 ◦ C for 4 h XRD; Suitable mechanical strength, porosity,
FE-SEM; degradation rate and water absorption;
Mechanical characterization; More new apatite formed after immersion
Structural analysis (Porosity, in SBF solution for 28 days
water absorption and
degradation);
In vitro bioactivity analysis
Catla catla and 1) Dried fish scales after washing FE-SEM; Crystalline pure phasic HAp; Potential application [117]
Oreochromis were soaked in 1 N HCl for 30 min; XRD; Thermally stable with minor degradation; for tissue
niloticus 2) Adding 6 N NaOH to adjust pH to FTIR; Presence of bonds supporting the cell- regeneration
11 and filtered; TGA; biomaterial interaction
3) Boiling for 0.5 h in water and Differential scanning calorimeter
− 80 ◦ C freezed for 12 h; (DSC)
4) 160 ◦ C incubated for 12 h and
sintered at 800 ◦ C for 2 h
Labeo rohita 1) Tap water washing and dried in FTIR; Crystalline HAp is thermally stable; Potential application [118]
ambient; XRD; Highly porous morphology; as a biomaterial in
2) Deproteinization using 1(N) HCl TGA; Polycrystalline HAp powder with particle bone tissue
for 24 h and 50 ◦ C dried after SEM; size 0.7–1.4 μm engineering
distilled water washing; TEM
3) Calcination at 1000 ◦ C for 4 h
Salmo salar and 1) DI water washed and 120 ◦ C SEM; Salmo salar scales derived hydroxyapatite Periodontal tissue [110]
Lutjanus dried; FTIR; displayed higher mechanical strength; regeneration
campechanus 2) 1 M HCl treated for 3 days at XRD; Supporting cellular proliferation,
60 ◦ C; EDS; organization, and differentiation of
3) DI water and ethanol washing; Cell viability (MTT assay); gingival fibroblasts whilst it promotes cell-
4) 1 M NaOH treated for 24 h at Alkaline phosphatase assay; scaffold matrix formation
Alizarin staining assay
(continued on next page)

11
D. Qin et al. Chemical Engineering Journal 428 (2022) 131102

Table 2 (continued )
Fish species Synthetic ways Analysis Characteristics Applications Ref.

60 ◦ C and 250 ◦ C for 3 h to crush it

into powder
Tilaipa 1) Immersed in H2O (pH 7.4, XRD; Ca/P ratio 1.95; Protein adsorption [44]
adjusted with 1 N NaOH) for 12 h; FTIR;
2) H2O washed for 10 s and statically SEM/EDS; HAp crystalline size:14.7 nm, 5.2 nm;
stand for 50 s; UV–Vis absorption spectra BET: 78 m2/g;
3) Immersed in Na2HPO4 (120 mM, analysis; BJH: 2.7 nm x16 nm × 24 nm
pH 9.2) for 5 min; Exhibiting preferential protein adsorption
4) H2O washed for 10 s and statically behavior
stand for 50 s;
5) Immersed in Tris (100 mM)-CaCl2
(200 mM) solution (pH 7.4) for 5
min;
6) Repeated ‘‘process 2–5′′ with 5
cycles, and 60 ◦ C dried for 12 h
7) Calcination at 250 ◦ C and then at
550 ◦ C.
Cyprinidae Ionic liquid pretreatment methods: FTIR; 32 ± 2% yield; Potential application [27]
1) Water washing, dried and ground; XRD; Various size and shapes with hexagonal in biomedical
2) 1-butyl-3-methylimidazolium TGA; nanocrystal;
acetate treatment for 12 h at 100 ◦ C; FE-SEM; Higher thermal degradation temperature;
3) NaOH solution (0.5 M) addition to EDX; Ca/P ratio 1.6;
adjust pH at 9.0 and centrifugation BET BET surface area: 37.38 m2/g
(11,000 rpm) for 30 min to collected Pore volume: 0.09 cm3/g
the supernatant; Pore sizes: 9.97 nm
4) NaCl solution (2 M) was added Good biocompatibility and cell viability
followed by adding HCl solution for HEK and A431 cells
(0.5 M) to bring the pH around 2;
5) Neutralization with NaOH (0.5 M)
and rotary evaporator to remove the
water
Cirrhinus mrigala Alkaline heat treatment method: XRD; Rod-like shape nanostructured particles Potential alternative [102]
1) Deproteinized fish scals were FTIR; with average size of 30–50 nm; biomaterial for the
washed with 0.1 M HCl; Thermal stability analysis; Thermally stable up to 900 ◦ C; better
2) 5% (w/v) NaOH treated for 7 h at TEM; Ca/P ratio 1.67; replacement of bones
70 ◦ C; EDS; Na+ and Mg2+ trace elements presence;
3) Neutralization and 70 ◦ C dried; Cell viability (MTT assay) and Higher cell viability, ALP activity and
4) 50% (w/v) NaOH treated for 2 h ALP activities analysis biocompatibility
at 100 ◦ C;
5) Neutralization and 100 ◦ C dried.
Dicentrarchus Alkaline heat treatment method: FTIR; Porous fish scales and -derived Acid Blue 121 dye [34]
labrax 1) Distilled water washing and dried; XRD; hydroxyapatite having meso- and adsorption
2) Deproteinized fish scals were SEM/EDX; macropores structure;
washed with 0.1 M HCl; BET (surface areas, pore Higher BET surface areas of fish scales and
3) 5% (w/v) NaOH treated for 3 h at volumes, pore widths and -derived hydroxyapatite than commercial
70 ◦ C; particle widths) analysis; hydroxyapatite;
4) Neutralization and 60 ◦ C dried; Adsorption equilibrium, kinetics, Effectively adsorb Acid Blue 121 dye
5) 50% (w/v) NaOH treated for 1 h thermodynamic analysis
Tilapia nilotica at 100 ◦ C; BET surface; Nanocrystal with high porosity; Selenium adsorption [114]
6) Neutralization and 60 ◦ C dried. TG/DTG/DTA; Higher BET surface, Langmuir surface, in aqueous solution
FTIR; Pore volume area and average pore size
XRD; than commercial hydroxyapatite;
TEM/EDX; Effectively adsorb selenite
Batch adsorption experiments for
the removal of selenite
Oreochromis 1) Collagen-extracted fish scale XRD; Particle sizes with 5.96 μm; Heavy metal ions [113]
mossambicus ultra-sonicated by 50 vol% alcohol Particle size analysis; Effectively remove Pb2+ ions Pb2+ removal from
solution and DI water consequently; SEM waste water
2) Calcination at 1000 ◦ C for 2 h;
3) Ground and sieved using 200
mesh filter
Nile tilapia Homogenous precipitation assisted XRD; Rice shape nanoparticles with 22.8 ± 2.9 An alternative [115]
with ultrasound energy method: SEM; nm in length and about 8.6 ± 2.4 nm in adsorbent for the
1) Water washing and dried; EDS; diameter; ultrasonic-assisted
2) 0.8 M HCl treated and sonicated at TEM; Under optimized conditions (pH = 8, removal of Hg2+
0.4 kw and 60 ◦ C of temperature for FTIR; ultrasonic power: 0.4 kW, adsorption time:
45 min; Brunauer-Emmett-Teller 20 min, adsorption temperature: 30 ◦ C),
3) Supernatant was adjusted to pH = the maximum removal of Hg2+ was
12 with NaOH and sonicated at 0.4 achieved at 0.02 g adsorbent dosage
kw and room temperature for 30
min;
4) Obtained granules were washed
with DI water, 60 ◦ C dried for 24 h
and ground.

12
D. Qin et al.
Fig. 8. Summary schematic of the fish scale-derived collagen applications in promoting soft tissue regeneration including skins, blood vessels, corneal, oral mucosa,
maxillofacial tissue and drug delivery systems.
decalcification treatment, which provides sufficient nutrients and oxy­
gen for the growth of corneal cells in the three-dimensional matrix of the
fish scales, and conducive to its rapid proliferation and migration of
high-density cells [133]. Essen et al. successfully prepared fish scale-
derived collagen matrix (FSCM) scaffold using decellularized and
decalcified tilapia (Oreochromis Niloticas) fish scales for corneal tissue
engineering. In vitro cell experiments showed that the fish scale-derived
collagen matrix scaffold had no cytotoxic to human corneal epithelial
cells and stromal cells, and also could promote the cell adhesion mole­
cules (integrin α6 and β4, laminin 332 and E-cadherin) expressions
(Fig. 9H), and there was no obvious sensitization and inflammatory
response to rats (Fig. 9E-G). The FSCM scaffold could keep the rabbit
cornea transparent and the epidermis healthy after the it was implanted
into the rabbit corneal stromal bag, without any immune cell infiltration
whilst it also remained stable for a long term and no signs of degradation
(Fig. 9I), which meets the basic conditions for corneal reconstruction
[134]. In addition, fish scales collagen matrix scaffolds showed no
obvious cytotoxicity to human corneal endothelial cells and maintained
the normal morphology of corneal endothelial cells. Therefore, fish scale
derived collagen scaffolds may become a promising corneal tissue en­
gineering material due to its good biocompatibility [135].
6.2. Soft tissue engineering
Collagen, the main protein component of extracellular matrix, is
characterized by high hydrophilicity and low antigenicity [136]. In
addition, COL-I is able to promote cell adhesion and proliferation
through its Arg-Gly-Asp (RGD) domain combined with integrin re­
ceptors on the cell membrane [137]. Previous studies have shown that
porcine skin-derived collagen without cytotoxicity could effectively
promote skin wound healing, but fish scale-derived collagen scaffolds
would provide a moist wound healing environment due to their high-
water absorption and air permeability, which was more conducive to
promoting scar-free skin wound healing [138]. At present, various
scaffolds based on fish scale collagen were not only studied for hard
13
Chemical Engineering Journal 428 (2022) 131102
tissue regeneration, but also widely studied in biomedical applications
for soft tissue regeneration, such as skin, blood vessel transplantation
and lymphatic vessel regeneration [139,140]. Shalaby et al. extracted
collagen from Tilapia and Grey Mullet scales, which was composed of
four subunits of β-chain, γ-chain and α1, α2 subunits, had obvious in­
hibition on Staphylococcus aureus (ATCC 25923), Streptococcus mutans
(ATCC 5175), Escherichia coli (ATCC 25922) and Bacillus subtills (ATCC
6633) and has positive effect on wound healing [32]. Pal et al. suc­
cessfully extracted acid soluble COL-1 and pepsin soluble COL-1 from
Cirrhinus cirrhosus scales, which were composed of two different α -
chains (α1 and α2). Its denaturation temperature was close to
mammalian collagen (35 ◦ C), which could promote cell growth and
proliferation, and the rapid healing of skin wounds in vivo as well [140].
In order to overcome the defects such as poor mechanical and
degradation stability of collagen scaffolds or give it new functional
properties, fish scale collagen scaffolds are often combined with various
synthetic or natural materials such as hydroxypropyl methyl cellulose
[141], carboxymethyl guar gum (CMGG)[16] and Macrotyloma uni­
florum extract [15] for skin wound healing. The composite membrane
prepared by combing the fish scale collagen and aminated CMGG
through non-covalent ions and chemical cross-linked showed good
mechanical properties, anti-swelling, biocompatibility, and has obvious
inhibiting effect against S. aureus and P. aeruginosa [16]. Feng et al.
successfully developed a hydrogel for enhancing acute full-thickness
wound healing by hybridizing oxidized sodium alginate (OSA), anti­
microbial peptides (polymyxin B sulfate and bacitracin) with poorly
immunogenic and highly biocompatible amino collagens (AC) prepared
from marine fish scales via Schiff base reaction (Fig. 10A). This cross-
linked hydrogel could efficacy against both E. coli and S. aureus in vitro
(Fig. 10B), whilst it promoted full-thickness wound healing via accel­
erating reepithelization, collagen deposition and angiogenesis (Fig. 10C)
[142]. In addition, the collagen sponge prepared by combining fish scale
collagen and Macrotyloma uniflorum extract maintains the three-
dimensional spiral structure, which can enhance its tensile strength
and stability to collagenase [15]. Meanwhile, curcumin-loaded fish scale
D. Qin et al.
collagen-hydroxypropyl methylcellulose nanogel can improve the me­
chanical and degradation stability of fish scale collagen while giving
nanohydrogel antioxidant function to promote rapid healing of skin
wounds [141].
Wang et al. carried out methylation modification and 1,4-butanediol
diglycidyl ether cross-linking modification on fish scale type I collagen
to solve its poor mechanical stability and degradation stability. In vivo
animal experiments results showed that the modified fish scale collagen
had good infiltration of cells, blood vessels and lymphatic vessels [139].
The full development of fish scale collagen shows a promising
application in soft tissue engineering, and it also increase the additional
benefits of marine fish resources during food processing.
6.3. Drug delivery system
Fish scale collagen is an important structural protein. Due to its
reliability, biodegradability and cell adhesion, it is often used as a matrix
material for medical tissue regeneration or as a drug carrier for drug
delivery systems. [141,143]. Pathan et al. prepared nano hydrogels as a
delivery vehicle by mixing the fish scale collagen and hydroxypropyl
methyl cellulose, which could significantly improve the bioavailability
of oral curcumin. Results showed that the nano-hydrogel slowed down
the release time of curcumin in fish scale and promoted the rapid healing
of skin wounds [141]. In addition, fish scale collagen was often made
14
Chemical Engineering Journal 428 (2022) 131102
Fig. 9. Schematic representation the structure of the
cornea and teleost fish scales and its application in
cornea. A) Schematic diagram of the cross-sectional
structure of the cornea. B) Fish scales surface struc­
ture view. C) Schematic diagram of the cross section
of the fish scale central region. D) Schematic diagram
of the cross section of the fish scale marginal region
[130]. E) Observation of clarity and neo­
vascularization of FSCMs implanted in rabbit cornea.
F&G) Corneal growth and inflammation using H&E
and RAW11 staining (Macrophages) analysis. H)
Immunofluorescence staining images of the primary
human corneal epithelial cells’ growth (CK3/12) and
cells adhesion (E-cadherin, integrin-α6, integrin-β4,
laminin 332 and p63) on FSCM. I) Long-term follow-
up of FSCM thickness stability and immunoreactivity
in the rabbit’s eyes [134].
into wound dressings such as sponges or films, which are used for the
delivery of antibacterial drugs such as mupirocin and ceftazidime. The
results exhibited that it could achieve continuous inhibition of micro­
organisms such as Staphylococcus aureus and Bacillus aeruginosa by
slowing the release of drugs from the dressings, so as to prevent skin
wound infection and promote skin wound healing [15,16].
Microneedle technology has become an effective and patient-
friendly drug delivery system with great potential in conventional
transdermal drug delivery [144]. The biodegradable microneedles pre­
pared from fish scale collagen could be used for percutaneous admin­
istration of aspirin, lidocaine and other drugs [143,144]. Fish scale
biopolymer microneedles could provide adhesive properties through
water activated self-adhesive properties, and promote the permeability
of lipophilic drugs such as aspirin and lidocaine in the skin [143–145].
Moreover, the hydrogel micro-needles based on fish scale hydrolyzed
collagen produced by low-temperature pressing method could with­
stand forces up to 0.136 N, which was enough to penetrate the skin. The
swelling of cross-linked microneedles in PBS was 340% of its original
weight, and the release of acetylsalicylic acid was 34.5% in 24 h [145].
6.4. Oral mucosa repair and maxillofacial tissue regeneration
Oral mucosa, as an epithelial tissue, has a microstructure called the
dermal epidermal junction, which is characterized by undulations/
D. Qin et al.
Fig. 10. Preparation of marine fish scale collagen hybrid hydrogel for advanced full-thickness wound healing. A) Schematic of the marine fish scale collagen hybrid
hydrogel design strategy and its application for full-thickness wounds. B) Photographs and cross-sectional SEM images of AC/OSA and AC/OSA-PB hybrid hydrogel.
C) Optical image and statistical analysis of AC/OSA-PB on E. coli and S. aureus. Scale bar = 10 mm. D) Photographs of AC/OSA and AC/OSA-PB hybrid hydrogel in
promoting full-thickness wound healing and H&E staining analysis [142].
interlacing of the epithelial cell layer and the underlying connective
tissue. The special microstructure not only facilitates the vascular free
epidermal layer to obtain nutrition from the capillary network in the
dermis, but also enhances the adhesion of the two layers due to the
increased surface area [146,147]. Therefore, the biomimetic tissue en­
gineering oral mucosa inspired by the its physiological structure and
surface morphology, especially the biomimetic collagen-based scaffold
with microstructure, is necessary for the oral mucosa regeneration.
Collagen derived from tilapia scales is often used in oral mucosa repair
and oral maxillofacial tissue regeneration due to its high safety, good
biocompatibility and degradability properties [148,149]. Tilapia-
derived type I collagen scaffolds with three-dimensional micro-
patterned structures constructed using micro-electro-mechanical system
technology and soft lithography facilitate the formation of epithelial
reticular ridge structures to promote oral mucosa regeneration [147].
Terada et al. successfully constructed a chitosan/ tilapia scales collagen
scaffold with well-developed fiber network and enough small pores for
oral mucosa regeneration, which could prevent keratinocytes from
growing in the scaffold. The tissue-engineered oral mucosa substitute
constructed with the scaffold had a more bionic epithelial regeneration
platform than the oral mucosa constructed by bovine collagen [120].
Suzuki et al. prepared a more biomimetic tissue-engineered oral mucosa
substitute containing 1% tilapia scales COL-I scaffold by semiconductor
technology and soft lithography technology, and its microstructure
could simulate the dermal epidermal junction of oral mucosa and oral
keratinocytes. Histological examination showed that a fully differenti­
ated and layered epithelial layer was formed on the fish scale collagen
scaffold, which indicated that the microstructure fish scale collagen
15
Chemical Engineering Journal 428 (2022) 131102
scaffold exhibited great potential in preparing clinically applied tissue
engineering oral mucosa substitutes [148]. In addition, tilapia scales
collagen and pig skin collagen had similar biocompatibility to mouse
odontoblast DPC-23, such as increased initial cell attachment, enhanced
ALP activity, up-regulated BSP gene expression and accelerated matrix
mineralization. Fish scale collagen could avoid zoonotic infectious dis­
eases, immunogenic reactions, and religion in the presence of
mammalian collagen, which may be a potential alternative to
mammalian COL-I in oral and maxillofacial tissue regeneration [149].
7. Gelatin
Gelatin is a soluble protein mixture obtained from the partial hy­
drolysis of collagen. Type A gelatin or type B gelatin can be extracted
from COL-I by acid or alkali hydrolysis, respectively [150]. Gelatin and
COL-I are mainly composed of Pro and Hyp. Compared with the content
of imino acid in mammal gelatin, the low content of imino acid (Pro +
Hyp) in cold water fish gelatin may be the main reason for its lower
melting point [151]. Gelatin is characterized by biocompatibility, film
formation and biodegradability, which has promoted its application in
the medicine, biomedicine and light-emitting devices fields.
Fish scale gelatin was successfully extracted from tilapia scales using
a combination of extrusion-pretreatment and hot water leaching.
Compared to pretreatment with double distilled water and acetic acid
solution before extrusion, citric acid pretreated fish scale gelatin is more
conducive to the adhesion and growth of keratinocytes HaCaT, and
protects cells from H2O2-induced oxidative damage [152]. The hydro­
thermal treated scales exhibited higher protein recovery rate (84.81%)
D. Qin et al. Chemical Engineering Journal 428 (2022) 131102

and degree of hydrolysis (12.88%) and released peptides more effi­
ciently than those of the conventional treatment. The angiotensin I-
converting enzyme inhibitory activity of the gelatin hydrolysate remains
stable at high temperature, pH and gastrointestinal protease, indicating
that the enzymatic hydrolysis after hydrothermal treatment could pro­
vide a potential solution for the preparation of gelatin hydrolysate
[153].
Electrospinning nanofiber scaffolds prepared with fish scale gelatin
and cross-linked by ultraviolet light not only have no cytotoxicity, but
also promote the adhesion, proliferation and migration of human ker­
atinocytes HaCaT, thereby accelerating skin wound healing [154]. Fish
scale gelatin hydrolysate can form stable colloidal composite nano­
particles by self-assembly with tannic acid [155]. Nanoparticles become
effective nano-biochelators and free radical scavengers due to the large
number of sites that interact with heavy metal ions and scavenge free
radicals. Therefore, the nanoparticles can improve the intestinal
epithelial tight junction dysfunction induced by Cu2+ in order to prevent
the activity of digestive enzymes from being inhibited [155]. In addi­
tion, fish scale gelatin (FG) film can also be made into a flexible
instantaneous alternating current electroluminescent (ACEL) device. In
the visible spectrum, the Ag NWs-FG device formed by the fish scale
gelatin film and silver nanowires ((Ag) NWs) is characterized by high
light transmittance, good flexibility, recyclability and degradability, as
shown in Fig. 11. Therefore, the FG film with sustainable, flexible and
transparent is a promising green and degradable substrate material in
flexible electronics, including foldable displays, wearable devices and
health monitoring [156].
However, the gelatin film has high brittleness and water sensitivity
due to the high hydrophilicity of gelatin, which limits its application. It
is found that these properties can be improved by physical, chemical or
enzymatic processes [150]. Nuamsrinuan adopted physical methods to
change the chemical and mechanical properties of the film by adjusting
the ratio of gelatin and chitosan. With the increase in the amount of
chitosan, the tensile strength of gelatin/chitosan film increased and the
elongation decreased [157]. The non-enzymatic reaction of fructose and
ascorbic acid was added into the film-forming formula of fish scale
gelatin, and the cross-linking induced by heat treatment could result in
higher barrier features of fish scale gelatin films [158]. Gelatin extracted
from fish scale was combined with dihydroxyphenol acid (caffeic acid)
by carbodiimide chemical reaction, and the modified fish scale gelatin
had the expected mechanical properties, biodegradation properties and
cell compatibility. The porous structure of glyoxylic acid modified
gelatin was conducive to cell adhesion and proliferation, and it could be
used as a substitute for tissue engineering and regenerative medicine
biomaterials [159]. Furthermore, nonwoven MPLA/FCSP/FSG nano­
fibers with antibacterial property, water resistance and good mechanical
properties could be developed by combining Mullet scales gelatin (FSG)
with modified polylactic acid (MPLA) and natural antibacterial agent of
freshwater clam (Corbicula fluminea Estefanía) shell powder (FCSP) using
electrospinning technique. Increasing the contents of FSG in the PLA/
FSG and MPLA/FCSP/FSG nanofibers showed positive effects on cell
proliferation and free radical scavenging [160]. Therefore, combining
fish scale gelatin with different fabrication processes including electro­
spinning nanofibers shows great promise for large-scale applications in
wound healing, food packaging, and bioprotective materials.
8. Collagen peptide
Fish-derived collagen peptide is the degradation product obtained by
enzymatic hydrolysis of fish collagen or gelatin, accompanied by various
biological activities such as antioxidant, anti-tumor, anti-aging skin,
promoting wound healing and epiphyseal growth [161–165].
The hydrolyzed collagen extracted from Tilapia scales with high
hydrophilicity and the best extracellular microenvironment provided by

Fig. 11. Sustainable degradable transparent FG film used in flexible electroluminescent devices. A) Flexible electroluminescent device based on sustainable and
transparent fish gelatin film. B) Schematic of the flexible alternating current electroluminescent devices manufacturing process. C) Schematic and SEM cross-sectional
image of ACEL devices. D) FG film recovery process diagram and comparison diagram of light transmittance of FG film after recovery. E) Images of FG film
degradation in soil for 24 days. F) Illumination diagram of LED bulbs with different bending angles in ACEL device [156].

16
D. Qin et al.
amino acids, could promote the differentiation of BMSCs cells into os­
teoblasts and endothelial cells but inhibits the differentiation of adipo­
cytes and chondrocytes by activating MAPK/ERK signal pathway in
BMSCs without any additional induce [166]. Fish scale collagen pep­
tides (FSCP) could prevent CoCl2/TNF-α-induced cytotoxicity and
inflammation by inhibiting MAPK and NF-κB signaling pathways acti­
vated by reactive oxygen species in keratinocyte HaCaT cells, which was
presented in Fig. 12. Fish scales collagen peptide provides a potential
candidate molecule for its use as an immunomodulator in the prevention
and treatment of various oxidative stress or inflammatory stress-related
inflammation and injury in inflammatory or immune-mediated skin
diseases [167]. Vigneswari et al. added FSCPs to the aminogenated poly
(3-hydroxybutyrate-co-4-hydroxybutyrate) (P-(3HB-co-4HB)) copol­
ymer scaffolds by ammonolysis reaction, which could solve the surface
hydrophobicity of P-(3HB-co-4HB) and less cell adhesion recognition
sites. Further research results showed that the chemically modified
FSCPs scaffold could promote the L929 cells attachment and growth on
its surface, which is beneficial to the closure of rat skin wound [168].
9. Fish scale-derived other biomaterials
Chitin is the most abundant polysaccharide in nature after cellulose,
which mainly exists in the exoskeleton of crustaceans (such as crabs,
shrimps, lobsters, etc.), as well as in various insects, worms, fungi and
mushrooms [169]. Chitin, a homopolymer of N-acetyl-D-glucosamine
linked by β-(1-4) glycoside bond, is a potential biomaterial for
biotechnology industry and tissue engineering due to the presence of
active groups, high adsorption capacity, antibacterial and antibacterial
activities [170,171]. It is also characterized by good biocompatibility,
biodegradability, bioabsorbability, low immunogenicity, antibacterial
and wound healing promotion. Chitosan is a deacetylated derivative of
chitin. Chitosan with free amino groups is often used as a binder, gelling
agent, thickener and stabilizer in chemical wastewater treatment, food
Fig. 12. Schematic diagram of FSCP regulating CoCl2/ TNF-α-induced oxidative stress and inflammation in HaCaT cells [167].
17
Chemical Engineering Journal 428 (2022) 131102
industry, and biomedical field [170]. Fish scale wastes as an interesting
natural material can also be used to extract active substances such as
chitin, chitosan and mucopolysaccharides [170,172]. Rumengan et al.
boiled the Chlourus sordidusand and Lutjanus argentimaculatus scales, and
obtained 45% and 33% chitin in their collagen mixture, respectively.
FTIR analysis further showed that the extract was characterized by a
typical marine chitin [171]. Kumari et al. successfully obtain chitin and
chitosan products using conventional treatments such as demineraliza­
tion, decolorization, and deacetylation form Labeo rohit fish scales with
diluted hydrochloric acid and sodium hydroxide [170]. Irawan et al.
successfully extracted deacetylated chitin derivative from Papuyu
(Anabas testudineus), and characterized and analyzed by FTIR and SEM.
The extract was further used as coagulant to coagulate and flocculate the
iron ions in groundwater, which showed that it was more effective than
commercial shrimp chitosan (93% deacetylation) at neutral pH and
room temperature [173]. Chitosan extracted from S. pilchardus as a new
marine source scales exhibited fibrous and porous structure whilst it was
characterized by 93% solubility, 5.86 kDa molecular weight, 310 fat
mass, and 510% water binding capacity [174].
Furthermore, the mucopolysaccharide (GAG) compounds, contain­
ing heparin like compounds in the extract, was extracted from the Rutilus
frisi kutum scales by using cetylpyridinium chloride cation salt, which
exhibited similar anticoagulant properties to synthetic anticoagulant
compounds (such as heparin). The extraction rate of GAG was about
23.8 mg/g. The results of anticoagulant activity showed that GAG
extracted from fish scales prolonged the coagulation time of human
plasma by increasing activated partial thromboplastin time [172].
The carbon and its derivatives from biomass residue have many
advantages, such as high utilization rate of solid waste, good availabil­
ity, low synthesis cost and high surface area, etc., which are widely used
in energy storage and wastewater treatment [28,35,90]. Marrakchi et al.
carbonized the fish scales in an electric furnace and then treated with
hydrochloric acid to obtain mesoporous carbon materials with
D. Qin et al.
mesoporous structure. The specific surface area of the materials was
213.8 m2/g and the average pore diameter was 5.1 nm, which had a high
adsorption capacity for reactive orange 16 dye (RO16) [28]. Sardinella
maderensis scales could also be prepared activated carbon with meso­
porous structure and particle size of 0.5–0.9 mm after being thermally
activated for 5 h at 700 ◦ C in muffle furnace. Its surface area was 1.8 m2/
g, and the average adsorption pore size could be increased to 12.8 nm,
which could effectively remove dyes and heavy metals from the
permeated wastewater [175]. Achieng et al. successfully prepared fish
scale biochar with different specific surface areas and particle sizes by
using tilapia (Oreochromis niloticus) fish scales by pyrolysis at
200 ◦ C–800 ◦ C. It could effectively remove the indigo carmine dye (ICD)
in the aqueous solution through a non-spontaneous adsorption process,
and the FSB prepared by pyrolysis at 600 ◦ C has the strongest adsorption
capacity for ICD [176].
Chloroapatite (Ca10 (PO4)6Cl2, ClAp) is a chlorine-substituted HAp,
and its hydroxyl group is completely replaced by chlorine, which can be
used as a phosphorescent material for electronic products due to its
fluorescence [177]. In addition, chloroapatite can also be used in
biomedicine due to the enhancement of absorbability, mechanical
properties and biological activity by chlorine substitution [178]. In
some cases, the high chlorine substituted HAP has more bioactivity than
the non-substituted HAP [179]. After the sardine scales were treated by
the combined cleaning-annealing process, the hydroxyl groups in the
sardine scales hydroxyapatite are replaced by chlorine in NaCl, indi­
cating the successfully preparation of chloroapatite [180]. Cavalcante
et al. treated Arapaima gigas fish scales with hydrochloric acid and so­
dium hydroxide, and then thermally decomposed them at 600 ◦ C,
800 ◦ C, and 1000 ◦ C, respectively, to obtain ClAp with a grain size of
1–5 μm. The crystallinity of chloroapatite obtained by heat treatment at
1000 ◦ C was as high as 84.27%, which could be used as a fluorescent
material in the field of electronics [181].
10. Future development trends and prospects
Considering the highly ordered hierarchical structure of fish scales
and its abundant value-added bio-compounds including organic
collagen, peptide, gelatin, chitin/chitosan, fish oil, enzyme and inor­
ganic hydroxyapatite. It can be widely used in food, medicine, cosmetics
and chemical industry. The micro-patterned structures on the fish scales
surface, as an external mechanical load, is suitable for stimulating
various cell behaviors, including cell migration, proliferation and dif­
ferentiation, especially osteogenesis. At the same time, the highly or­
dered hierarchical structure endows its excellent mechanical properties,
making it an ideal choice for the new biological protective equipment
development. Through deep excavation of the multiple deformation
mechanisms including fiber stretching, separation, reorientation,
delamination, twisting, shearing and fracturing, it can provide inspira­
tion for designing light, flexible and sufficiently flexible “armor”.
Various organic biopolymers derived from fish scales, such as
collagen and its derivatives, are not only similar in application value to
mammalian sources, but also have multiple functions such as blood
production, grooming, beauty, lipid-lowering, antioxidation and anti-
aging. Compared with mammals, fish scale-derived collagen and its
derivatives exhibit unique characteristics of low melting point, high
viscosity, high transparency and low zoonotic diseases. Therefore, fish
scale collagen and its derivatives show potential application value as
thickeners, emulsifiers, clarifiers, and stabilizers and moisturizers in
food processing and cosmetics industry. In addition, fish scale collagen
and its derivatives exhibit low antigenicity, good biocompatibility and
biodegradability, and promote cell adhesion and proliferation, which
provide great promise for its applications in wound dressings, soft tissue
regeneration with hemostatic agents, and cornea repair.
Hydroxyapatite extracted from fish scales using different proccessing
methods, as a fishery value-added product, can be used as an implant­
able material for tooth restoration, beauty, bone tissue regeneration
18
Chemical Engineering Journal 428 (2022) 131102
engineering, pharmaceutical and chemical industries due to its large
resources, good biocompatibility, high biological activity and high
safety. Choosing the best extraction technology should not only focus on
the final yield, especially in the case of compounds used for human
consumption, but should also maintain its safety and biological char­
acteristics as much as possible. Calcium ions in the hydroxyapatite lat­
tice undergo displacement reactions with heavy metals such as Pb, Cd,
and Cu at room temperature and show the ability to adsorb or deshielde
heavy metal ions or color dyes. Based on this characteristic, inexpensive
hydroxyapatite adsorbent products prepared from fish scales for the
treatment of wastewater are also promising. Recycling and utilization of
fish scale wastes to obtain fish by-products solves major environmental
pollution problems whilst it promotes the development of products with
high commercial value and promotes economic growth.
However, there are still huge challenges in the development and
application of fish scales. Firstly, the mature fish scale preparation and
processing system should be formulated and improved as soon as
possible. Second, the preparation of biomimetic fish scales biomaterials
with light, ultra-thin, high strength and toughness properties still a
challenge, which needs to further explore the toughness mechanism,
interstructureand biosynthetic process of fish scales. In addition, the
researchers should excavate and rationally use the effective ingredients
in fish scales, and conduct detailed and in-depth studies in vivo and in
vitro before clinical application. We have reason to believe the above
efforts will create huge commercial value and build a friendly natural
environment for human.
11. Conclusion
Fish scale is a natural renewable multi-layered composite biomate­
rial with highly ordered microstructure, which is mainly composed of
type I collagen and hydroxyapatite. Fish scales and fish scales centered
biocomposites have important application value in tissue engineering,
biological fillers, sewage treatment and flexible electronics fields
because of its excellent physical and chemical properties, such as
biocompatibility, biodegradability, hierarchical microstructure, multi­
ple active groups, high strength and toughness. Converting discarded
fish scales into functional materials can avoid waste of resources and
achieve great commercial value. In this review, we introduced the
microstructure, composition and derived functional materials of fish
scales, listed their potential applications in many fields, which provided
important references for the application of fish scales and their de­
rivatives in the future. Converting fish scale as byproducts of fish pro­
cessing into natural biopolymers including collagen, gelatin, chitin/
chitosan and inorganic components such as bioactive hydroxyapatite,
chloroapatite is a major advantage for fish scales waste management,
which would not only maximize the managers profits and reduce its
environmental pollutions, but they also show many advantages in
medical and health care including bone tissue regeneration, oral
mucosal repair, soft tissue regeneration such as skin and blood vessels
and other fields such as heavy metals ion and dyes adsorption, biomass
materials.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgements
This research was supported by the National Natural Science Foun­
dation of China NSFC (U1706212) and the National Natural Science
Foundation of China NSFC (81671828).
D. Qin et al. Chemical Engineering Journal 428 (2022) 131102

References [30] L. Boarin-Alcalde, G. Graciano-Fonseca, Alkali process for chitin extraction and
chitosan production from Nile tilapia (Oreochromis niloticus) scales, Latin
American Journal of Aquatic Research 44 (4) (2016) 683–688.
[1] H. Tian, Z. Tang, X. Zhuang, X. Chen, X. Jing, Biodegradable synthetic polymers:
[31] M. Tanvir, R.M. Habibur, B.H. Ara, R.M. Azizur, Chitosan and carboxymethyl
Preparation, functionalization and biomedical application, W. De Gruyter 37 (2)
chitosan from fish scales of Labeo rohita, Dhaka University Journal of Science 61
(2012) 237–280.
(1) (2013) 145–148.
[2] K. Ariga, A. Vinu, Y. Yamauchi, Q. Ji, J.P. Hill, Nanoarchitectonics for
[32] M. Shalaby, M. Agwa, H. Saeed, S.M. Khedr, O. Morsy, M.A. El-Demellawy, Fish
mesoporous materials, Bull. Chem. Soc. Jpn. 85 (1) (2012) 1–32.
scale collagen preparation, characterization and its application in wound healing,
[3] P.L. Hamilton, D.P. Arya, Natural product DNA major groove binders, Nat. Prod.
J. Polym. Environ. 28 (1) (2019) 166–178.
Rep. 29 (2) (2012) 134–143.
[33] M. Bilal, J.A. Shah, T. Ashfaq, S.M.H. Gardazi, A.A. Tahir, A. Pervez, H. Haroon,
[4] D.J. Newman, G.M. Cragg, Natural products as sources of new drugs over the 30
Q. Mahmood, Waste biomass adsorbents for copper removal from industrial
years from 1981 to 2010, J. Nat. Prod. 75 (3) (2012) 311–335.
wastewater—A review, J. Hazard. Mater. 263 (2013) 322–333.
[5] S.A. Sell, P.S. Wolfe, K. Garg, J.M. McCool, I.A. Rodriguez, G.L. Bowlin, The use
[34] D. Uzunoglu, A. Özer, Adsorption of Acid Blue 121 dye on fish (Dicentrarchus
of natural polymers in tissue engineering: A focus on electrospun extracellular
labrax) scales, the extracted from fish scales and commercial hydroxyapatite:
matrix analogues, Polymers 2 (4) (2010) 522–553.
equilibrium, kinetic, thermodynamic, and characterization studies, Desalin.
[6] A. Rogina, Electrospinning process: Versatile preparation method for
Water Treat. 57 (2016) 14109–14131.
biodegradable and natural polymers and biocomposite systems applied in tissue
[35] F. Yu, M. Wang, B. Huang, Q. Peng, Y. Huang, Acid-treatment effect on the N-
engineering and drug delivery, Appl. Surf. Sci. 296 (2014) 221–230.
doped porous carbon obtained from fish scales for Cr(VI) removal, Chem. Pap. 71
[7] S. Ramakrishna, K. Fujihara, W.-E. Teo, T. Yong, Z. Ma, R. Ramaseshan,
(11) (2017) 2261–2269.
Electrospun nanofibers: solving global issues, Mater. Today 9 (3) (2006) 40–50.
[36] P. Rawat, D. Zhu, M.Z. Rahman, F. Barthelat, Structural and mechanical
[8] J. Venkatesan, I. Bhatnagar, P. Manivasagan, K.-H. Kang, S.-K. Kim, Alginate
properties of fish scales for the bio-inspired design of flexible body armors: A
composites for bone tissue engineering: A review, Int. J. Biol. Macromol. 72
review, Acta Biomater. 121 (2021) 41–67.
(2015) 269–281.
[37] W. Yang, I.H. Chen, B. Gludovatz, E.A. Zimmermann, R.O. Ritchie, M.A. Meyers,
[9] D. Arola, S. Murcia, M. Stossel, R. Pahuja, T. Linley, A. Devaraj, M. Ramulu, E.
Natural flexible dermal armor, Adv. Mater. 25 (1) (2013) 31–48.
A. Ossa, J. Wang, The limiting layer of fish scales: structure and properties, Acta
[38] H.R. Esmaeili, F. Zarei, N. Sanjarani Vahed, M. Masoudi, Scale morphology and
Biomater.. 67 (2018) 319–330.
phylogenetic character mapping of scale-surface microstructures in sixteen
[10] U.G. Wegst, H. Bai, E. Saiz, A.P. Tomsia, R.O. Ritchie, Bioinspired structural
Aphanius species (Teleostei: Aphaniidae), Micron 119 (2019) 39–53.
materials, Nat. Mater. 14 (1) (2015) 23–36.
[39] M.L. Ravneet, H.P.S. Kang Sharma, High resolution scanning electron microscope
[11] N.T. Chinh, V.Q. Manh, V.Q. Trung, T.D. Lam, M.D. Huynh, N.Q. Tung, N.
examination of the fish scale: Inspiration for novel biomaterials, Journal of
D. Trinh, T. Hoang, Characterization of collagen derived from tropical freshwater
Biomimetics Biomaterials & Tissue, Engineering 4 (2009) 13–20.
Carp fish scale wastes and its amino acid sequence, Nat. Prod. Commun. 14 (7)
[40] W.T. Liu, Y. Zhang, G.Y. Li, Y.Q. Miao, X.H. Wu, Structure and composition of
(2019) 1934578–1986628.
teleost scales from snakehead Channa argus (Cantor) (Perciformes: Channidae),
[12] M. Holá, J. Kalvoda, H. Nováková, R. Škoda, V. Kanický, Possibilities of LA-ICP-
J. Fish Biol. 72 (4) (2008) 1055–1067.
MS technique for the spatial elemental analysis of the recent fish scales: Line scan
[41] L.A. Jawad, Comparative morphology of scales of four teleost fishes from Sudan
vs. depth profiling, Appl. Surf. Sci. 257 (6) (2011) 1932–1940.
and Yemen, J. Nat. Hist. 39 (28) (2005) 2643–2660.
[13] S. Gil-Duran, D. Arola, E.A. Ossa, Effect of chemical composition and
[42] W. Yang, V.R. Sherman, B. Gludovatz, M. Mackey, E.A. Zimmermann, E.
microstructure on the mechanical behavior of fish scales from Megalops
H. Chang, E. Schaible, Z. Qin, M.J. Buehler, R.O. Ritchie, Protective role of
Atlanticus, J. Mech. Behav. Biomed. Mater. 56 (2016) 134–145.
Arapaima gigas fish scales: Structure and mechanical behavior, Acta Biomater. 10
[14] J. Padrão, R. Machado, M. Casal, S. Lanceros-Méndez, L.R. Rodrigues,
(8) (2014) 3599–3614.
F. Dourado, V. Sencadas, Antibacterial performance of bovine lactoferrin-fish
[43] A.A. Schnbrner, G. Boivin, C.A. Baud, The mineralization processes in teleost fish
gelatine electrospun membranes, Int. J. Biol. Macromol. 81 (2015) 608–614.
scales, Cell Tissue Res. 202 (2) (1979) 203–212.
[15] T. Muthukumar, P. Prabu, K. Ghosh, T.P. Sastry, Fish scale collagen sponge
[44] Y. Chai, M. Nishikawa, M. Tagaya, Preparation of gold/hydroxyapatite hybrids
incorporated with Macrotyloma uniflorum plant extract as a possible wound/
using natural fish scale template and their effective albumin interactions, Adv.
burn dressing material, Colloids Surf.. B Biointerfaces 113 (2014) 207–212.
Powder Technol. 29 (5) (2018) 1198–1203.
[16] P. Jana, T. Mitra, T.K.R. Selvaraj, A. Gnanamani, P.P. Kundu, Preparation of guar
[45] P.Y. Chen, J. Schirer, A. Simpson, R. Nay, Y.S. Lin, W. Yang, M.I. Lopez, J. Li, E.
gum scaffold film grafted with ethylenediamine and fish scale collagen, cross-
A. Olevsky, M.A. Meyers, Predation versus protection: Fish teeth and scales
linked with ceftazidime for wound healing application, Carbohydr. Polym. 153
evaluated by nanoindentation, J. Mater. Res. 27 (1) (2012) 100–112.
(2016) 573–581.
[46] D. Zhu, C. Zhang, P. Liu, L.A. Jawad, Comparison of the morphology, structures
[17] D. Zhu, C.F. Ortega, R. Motamedi, L. Szewciw, F. Vernerey, F. Barthelat, Structure
and mechanical properties of teleost fish scales collected from New Zealand,
and mechanical performance of a “modern” fish scale, Adv. Eng. Mater. 14 (4)
J. Bionic Eng. 16 (2) (2019) 328–336.
(2012) B185–B194.
[47] I.H. Chen, J.H. Kiang, V. Correa, M.I. Lopez, P.Y. Chen, J. Mckittrick, M.
[18] A. Marino Cugno Garrano, G. La Rosa, D. Zhang, L.N. Niu, F.R. Tay, H. Majd,
A. Meyers, Armadillo armor: Mechanical testing and micro-structural evaluation,
D. Arola, On the mechanical behavior of scales from Cyprinus carpio, J. Mech.
J. Mech. Behav. Biomed. Mater. 4 (5) (2011) 713–722.
Behav. Biomed. Mater. 7 (2012) 17–29.
[48] H. Quan, W. Yang, E. Schaible, R.O. Ritchie, M.A. Meyers, Novel Defense
[19] L. Zylberberg, G. Nicolas, Ultrastructure of scales in a teleost (Carassius auratus
Mechanisms in the Armor of the Scales of the “Living Fossil” Coelacanth Fish,
L.) after use of rapid freeze-fixation and freeze-substitution, Cell Tissue Res.. 223
Adv. Funct. Mater. 28 (46) (2017) 1804237.
(1982) 349–367.
[49] P. Fratzl, F.G. Barth, Biomaterial systems for mechanosensing and actuation,
[20] S. Murcia, E. Lavoie, T. Linley, A. Devaraj, E.A. Ossa, D. Arola, The natural armors
Nature 462 (7272) (2009) 442–448.
of fish: A comparison of the lamination pattern and structure of scales, J. Mech.
[50] P. Fratzl, R. Weinkamer, Nature’s hierarchical materials, Prog. Mater Sci. 52 (8)
Behav. Biomed. Mater. 73 (2017) 17–27.
(2007) 1263–1334.
[21] Z. Fang, Y. Wang, Q. Feng, A. Kienzle, W.E. Muller, Hierarchical structure and
[51] S. Ghods, S. Waddell, E. Weller, C. Renteria, H.Y. Jiang, J.M. Janak, S.S. Mao, T.J.
cytocompatibility of fish scales from Carassius auratus, Mater. Sci. Eng. C Mater.
Linley, D. Arola, On the regeneration of fish scales: structure and mechanical
Biol. Appl. 43 (2014) 145–152.
behavior, J Exp Biol 223(Pt 10) (2020) jeb211144.
[22] A. Bigi, M. Burghammer, R. Falconi, M.H.J. Koch, S. Panzavolta, C. Riekel,
[52] E.A. Zimmermann, B. Gludovatz, E. Schaible, N. Dave, W. Yang, M.A. Meyers, R.
Twisted plywood pattern of collagen fibrils in teleost scales: An X-ray diffraction
O. Ritchie, Mechanical adaptability of the Bouligand-type structure in natural
investigation, J. Struct. Biol. 136 (2) (2001) 137–143.
dermal armour, Nat. Commun. 4 (2014) 2634.
[23] T. Ikoma, H. Kobayashi, J. Tanaka, D. Walsh, S. Mann, Microstructure,
[53] A. Khayer Dastjerdi, F. Barthelat, Teleost fish scales amongst the toughest
mechanical, and biomimetic properties of fish scales from Pagrus major, J. Struct.
collagenous materials, J. Mech. Behav. Biomed. Mater. 52 (2015) 95–107.
Biol. 142 (3) (2003) 327–333.
[54] H. Quan, W. Yang, M. Lapeyriere, E. Schaible, R.O. Ritchie, M.A. Meyers,
[24] B.J. Bruet, J. Song, M.C. Boyce, C. Ortiz, Materials design principles of ancient
Structure and mechanical adaptability of a modern elasmoid fish scale from the
fish armour, Nat. Mater. 7 (9) (2008) 748–756.
Common Carp, Matter 3 (3) (2020) 842–863.
[25] Y.S. Lin, C.T. Wei, E.A. Olevsky, M.A. Meyers, Mechanical properties and the
[55] L.C. Palmer, C.J. Newcomb, S.R. Kaltz, E.D. Spoerke, S.I. Stupp, Biomimetic
laminate structure of Arapaima gigas scales, J. Mech. Behav. Biomed. Mater. 4 (7)
systems for hydroxyapatite mineralization inspired by bone and enamel, Chem.
(2011) 1145–1156.
Rev. 108 (11) (2008) 4754–4783.
[26] C. Lopes, L.T. Antelo, A. Franco-Uria, A.A. Alonso, R. Perez-Martin, Valorisation
[56] C.H. Chou, Y.G. Chen, C.C. Lin, S.M. Lin, K.C. Yang, S.H. Chang, Bioabsorbable
of fish by-products against waste management treatments–Comparison of
fish scale for the internal fixation of fracture: a preliminary study, Tissue Eng.
environmental impacts, Waste Manag 46 (2015) 103–112.
Part A 20 (17–18) (2014) 2493–2502.
[27] N. Muhammad, Y. Gao, F. Iqbal, P. Ahmad, R. Ge, U. Nishan, A. Rahim, G. Gonfa,
[57] A. Kara, O.C. Gunes, A.Z. Albayrak, G. Bilici, G. Erbil, H. Havitcioglu, Fish scale/
Z. Ullah, Extraction of biocompatible hydroxyapatite from fish scales using novel
poly(3-hydroxybutyrate-co-3-hydroxyvalerate) nanofibrous composite scaffolds
approach of ionic liquid pretreatment, Sep. Purif. Technol. 161 (2016) 129–135.
for bone regeneration, J. Biomater. Appl. 34 (9) (2020) 1201–1215.
[28] F. Marrakchi, M.J. Ahmed, W.A. Khanday, M. Asif, B.H. Hameed, Mesoporous
[58] A. Kara, S. Tamburaci, F. Tihminlioglu, H. Havitcioglu, Bioactive fish scale
carbonaceous material from fish scales as low-cost adsorbent for reactive orange
incorporated chitosan biocomposite scaffolds for bone tissue engineering, Int. J.
16 adsorption, J. Taiwan Inst. Chem. Eng. 71 (2017) 47–54.
Biol. Macromol. 130 (2019) 266–279.
[29] B. Hoyer, A. Bernhardt, S. Heinemann, I. Stachel, M. Meyer, M. Gelinsky,
[59] A. Satapathy, A. Patnaik, M.K. Pradhan, A study on processing, characterization
Biomimetically mineralized salmon collagen scaffolds for application in bone
and erosion behavior of fish (Labeo-rohita) scale filled epoxy matrix composites,
tissue engineering, Biomacromolecules 13 (4) (2012) 1059–1066.
Mater. Des. 30 (2009) 2359–2371.

19
D. Qin et al.
[60] C. Chiarathanakrit, S.A. Riyajan, K. Kaewtatip, Transforming fish scale waste into
an efficient filler for starch foam, Carbohydr. Polym. 188 (2018) 48–53.
[61] A. Satapathy, M.K. Pradhan, D. Mishra, A. Patnaik, Fabrication, mechanical
characterization and FTIR spectroscopic analysis of fish scale reinforced epoxy
composites, Advanced Materials Research 445 (2012) 889–892.
[62] A. Nourbakhsh, A. Ashori, A. Kazemi Tabrizi, Characterization and
biodegradability of polypropylene composites using agricultural residues and
waste fish, Compos. B Eng. 56 (2014) 279–283.
[63] K. Ramesh Babu, V. Jayakumar, G. Bharathiraja, S. Madhu, Experimental
investigation of fish scale reinforced polymer composite, Mater. Today:. Proc. 22
(2020) 416–418.
[64] E. Ural, E.A. Kandirmaz, Potential of fish scales as a filling material in surface
coating of cellulosic paper, Journal of Applied Biomaterials & Functional
Materials 16 (1) (2018) 23–27.
[65] T.V. Aradhyula, D. Bian, A.B. Reddy, Y.R. Jeng, M. Chavali, E.R. Sadiku,
R. Malkapuram, Compounding and the mechanical properties of catla fish scales
reinforced-polypropylene composite - from biowaste to biomaterial, Adv.
Compos. Mater 29 (2) (2020) 115–128.
[66] C.S. Wu, Comparative assessment of the interface between poly(3-
hydroxybutyrate-co-3-hydroxyvalerate) and fish scales in composites:
Preparation, characterization, and applications, Mater Sci Eng C Mater Biol Appl
104 (2019), 109878.
[67] C. Ribeiro, F.B. Scheufele, F.R. Espinoza-Quiñones, A.N. Módenes, M.G.C. da
Silva, M.G.A. Vieira, C.E. Borba, Characterization of Oreochromis niloticus fish
scales and assessment of their potential on the adsorption of reactive blue 5G dye,
Colloids Surf. A 482 (2015) 693–701.
[68] E.F.S. Vieira, A.R. Cestari, W.A. Carvalho, C. dos, S. Oliveira, R.A. Chagas, The
use of freshwater fish scale of the species Leporinus elongatus as adsorbent for
anionic dyes, J. Therm. Anal. Calorim. 109 (3) (2012) 1407–1412.
[69] S.M.F. Kabir, T.U. Rashid, Negulescu, II, Gelation of textile dye solution treated
with fish scales, Gels 5 (3) (2019) 37.
[70] C.V. Neves, F.B. Scheufele, A.P. Nardino, M.G.A. Vieira, M.G.C. da Silva, A.
N. Modenes, C.E. Borba, Phenomenological modeling of reactive dye adsorption
onto fish scales surface in the presence of electrolyte and surfactant mixtures,
Environ. Technol. 39 (19) (2018) 2467–2483.
[71] S. Chowdhury, P.D. Saha, U. Ghosh, Fish (Labeo rohita) scales as potential low-
cost biosorbent for removal of malachite green from aqueous solutions, Biorem. J.
16 (4) (2012) 235–242.
[72] G. Niero, A.X.R. Correa, G. Trierweiler, A.J.F. Matos, R. Correa, H.A.G. Bazani, C.
M. Radetski, Using modified fish scale waste from Sardinella brasiliensis as a low-
cost adsorbent to remove dyes from textile effluents, J. Environ. Sci. Health A
Tox. Hazard. Subst. Environ. Eng. 54 (11) (2019) 1083–1090.
[73] K. Zhu, X. Gong, D. He, B. Li, D. Ji, P. Li, Z. Peng, Y. Luo, Adsorption of Ponceau
4R from aqueous solutions using alkali boiled Tilapia fish scales, RSC Adv. 3 (47)
(2013) 25221–25230.
[74] J. Ooi, L.Y. Lee, B.Y.Z. Hiew, S. Thangalazhy-Gopakumar, S.S. Lim, S. Gan,
Assessment of fish scales waste as a low cost and eco-friendly adsorbent for
removal of an azo dye: Equilibrium, kinetic and thermodynamic studies,
Bioresour. Technol. 245 (2017) 656–664.
[75] F. Teshale, R. Karthikeyan, O. Sahu, Synthesized bioadsorbent from fish scale for
chromium (III) removal, Micron 130 (2020), 102817.
[76] Z. Ahmadifar, A. Dadvand Koohi, Characterization, preparation, and uses of
nanomagnetic Fe3O4 impregnated onto fish scale as more efficient adsorbent for
Cu(2+) ion adsorption, Environ. Sci. Pollut. Res. Int. 25 (20) (2018)
19687–19700.
[77] Z.S. Veličković, R. Karkalić, Z.J. Bajić, A.D. Marinković, A. Nikolić, P. Otřísal4,
S. Florus, Cerium supported on high porous carbon from fish scals carp, as a novel
low cost adsorbent to remove As(V) ions from water, Mater. Methods Technol. 12
(1) (2018) 110–122.
[78] D. Pal, S.K. Maiti, An approach to counter sediment toxicity by immobilization of
heavy metals using waste fish scale derived biosorbent, Ecotoxicol. Environ. Saf.
187 (2020), 109833.
[79] C. Li, B. Huang, C. Li, X. Chen, Y. Huang, In situ formation of nanoscale zero-
value iron on fish-scale-based porous carbon for Cr(VI) adsorption, Water Sci.
Technol. 73 (9) (2016) 2237–2243.
[80] C. Ribeiroa, F.B. Scheufeleb, H.J. Alvesb, A.D. Kroumovc, F.
R. EspinozaQuiñonesa, A.N. Módenesa, C.E. Borba, Evaluation of hybrid
neutralization/biosorption process for zinc ions removal from automotive battery
effluent by dolomite and fish scales, Environ. Technol. 40 (2018) 2373–2388.
[81] W. Guo, A. Abdolali, Y. Liu, D. Dinh, L. Nguyen, Application of a breakthrough
biosorbent for removing heavy metals from synthetic and real wastewaters in a
lab-scale continuous fixed-bed column, Bioresour. Technol. 229 (2017) 78–87.
[82] P. Stepnowski, G. Ólafsson, H. Helgason, B. Jastorff, Recovery of astaxanthin from
seafood wastewater utilizing fish scales waste, Chemosphere 54 (3) (2004)
413–417.
[83] Q. Yan, M.L. Chang, Nanostructured catalysts in fuel cells, J. Mater. Chem. 21 (6)
(2011), 062001.
[84] H. Liu, Y. Cao, F. Wang, Y. Huang, Nitrogen-doped hierarchical lamellar porous
carbon synthesized from the fish scale as support material for platinum
nanoparticle electrocatalyst toward the oxygen reduction reaction, ACS Appl.
Mater. Interfaces 6 (2) (2014) 819–825.
[85] R. Chakraborty, S. Bepari, A. Banerjee, Application of calcined waste fish (Labeo
rohita) scale as low-cost heterogeneous catalyst for biodiesel synthesis, Bioresour.
Technol. 102 (3) (2011) 3610–3618.
20
Chemical Engineering Journal 428 (2022) 131102
[86] L.-N. Ho, S.-A. Ong, H. Osman, F.-M. Chong, Enhanced photocatalytic activity of
fish scale loaded TiO2 composites under solar light irradiation, J. Environ. Sci. 24
(6) (2012) 1142–1148.
[87] P. Mckendry, Energy production from biomass (part 1): overview of biomass,
Bioresour. Technol. 83 (1) (2002) 37–46.
[88] A.V.S. Silva, L.D.M. Torquato, G. Cruz, Potential application of fish scales as
feedstock in thermochemical processes for the clean energy generation, Waste
Manag 100 (2019) 91–100.
[89] Z. Hussain, A. Sardar, K.M. Khan, M.Y. Naz, S.A. Sulaiman, S. Shukrullah,
Construction of rechargeable protein battery from mixed-waste processing of fish
scales and chicken feathers, Waste Biomass Valorization 11 (5) (2018)
2129–2135.
[90] V. Selvamani, R. Ravikumar, V. Suryanarayanan, D. Velayutham, S. Gopukumar,
Fish scale derived nitrogen doped hierarchical porous carbon—a high rate
performing anode for lithium ion cell, Electrochim. Acta 182 (2015) 1–10.
[91] R. Yang, S. Liu, Y. Liu, L. Liu, L. Chen, W. Yu, Y. Yan, Z. Feng, Y. Xu, Decalcified
fish scale-based sponge-like nitrogen-doped porous carbon for lithium-sulfur
batteries, Ionics 27 (1) (2020) 165–174.
[92] M.J. Olszta, X. Cheng, S.J. Sang, R. Kumar, Y.Y. Kim, M.J. Kaufman, E.P. Douglas,
L.B. Gower, Bone structure and formation: A new perspective, Mater. Sci. Eng. R
58 (3–5) (2007) 77–116.
[93] A. Dey, P.H.H. Bomans, F.A. Mueller, J. Will, P.M. Frederik, G.D. With, N.A.J.
M. Sommerdijk, The role of prenucleation clusters in surface-induced calcium
phosphate crystallization, Nat. Mater. 9 (12) (2010) 1010–1014.
[94] L. Tercinier, A. Ye, S. Anema, A. Singh, H. Singh, Characterisation of milk protein
adsorption onto hydroxyapatite, Int. Dairy J. 66 (2017) 27–33.
[95] J. Brandt, S. Henning, G. Michler, W. Hein, A. Bernstein, M. Schulz,
Nanocrystalline hydroxyapatite for bone repair: an animal study, J. Mater. Sci. -
Mater. Med. 21 (1) (2010) 283–294.
[96] H. Zhou, J. Lee, Nanoscale hydroxyapatite particles for bone tissue engineering,
Acta Biomater. 7 (7) (2011) 2769–2781.
[97] N.A.M. Barakat, M.S. Khil, A.M. Omran, F.A. Sheikh, H.Y. Kim, Extraction of pure
natural hydroxyapatite from the bovine bones bio waste by three different
methods, J. Mater. Process. Technol. 209 (7) (2009) 3408–3415.
[98] Y.C. Huang, P.C. Hsiao, H.J. Chai, Hydroxyapatite extracted from fish scale:
Effects on MG63 osteoblast-like cells, Ceram. Int. 37 (6) (2011) 1825–1831.
[99] K.P. Sanosh, M.C. Chu, A. Balakrishnan, T.N. Kim, S.J. Cho, Utilization of
biowaste eggshells to synthesize nanocrystalline hydroxyapatite powders, Mater.
Lett. 63 (24–25) (2009) 2100–2102.
[100] S. Mondal, A. Mondal, N. Mandal, B. Mondal, S.S. Mukhopadhyay, S. Singh,
A. Dey, Physico-chemical characterization and biological response of Labeo
rohita-derived hydroxyapatite scaffold, Bioprocess. Biosyst. Eng. 37 (2014)
1233–1240.
[101] P. Deb, A.B. Deoghare, Effect of acid, alkali and alkali–acid treatment on
physicochemical and bioactive properties of hydroxyapatite derived from Catla
catla fish scales, Arabian J. Sci. Eng. 44 (9) (2019) 7479–7490.
[102] S. Sathiskumar, S. Vanaraj, D. Sabarinathan, S. Bharath, G. Sivarasan,
S. Arulmani, K. Preethi, V.K. Ponnusamy, Green synthesis of biocompatible
nanostructured hydroxyapatite from Cirrhinus mrigala fish scale – A biowaste to
biomaterial, Ceram. Int. 45 (2019) 7804–7810.
[103] W. Pon-On, P. Suntornsaratoon, N. Charoenphandhu, J. Thongbunchoo,
N. Krishnamra, I.M. Tang, Hydroxyapatite from fish scale for potential use as
bone scaffold or regenerative material, Mater. Sci. Eng. C Mater. Biol. Appl. 62
(2016) 183–189.
[104] B. Mondal, S. Mondal, A. Mondal, N. Mandal, Fish scale derived hydroxyapatite
scaffold for bone tissue engineering, Mater. Charact. 121 (2016) 112–124.
[105] P. Deb, E. Barua, A.B. Deoghare, S.D. Lala, Development of bone scaffold using
Puntius conchonius fish scale derived hydroxyapatite: Physico-mechanical and
bioactivity evaluations, Ceram. Int. 45 (8) (2019) 10004–10012.
[106] W. Pon-On, P. Suntornsaratoon, N. Charoenphandhu, J. Thongbunchoo,
N. Krishnamra, I.M. Tang, Synthesis and investigations of mineral ions-loaded
apatite from fish scale and PLA/chitosan composite for bone scaffolds, Mater.
Lett. 221 (2018) 143–146.
[107] P. Deb, A.B. Deoghare, E. Barua, Poly ethylene glycol/fish scale-derived
hydroxyapatite composite porous scaffold for bone tissue engineering, IOP Conf.
Ser.: Mater. Sci. Eng. 377 (2018), 012009.
[108] C.J. Wilcock, P. Gentile, P.V. Hatton, C.A. Miller, Rapid mix Preparation of
bioinspired nanoscale hydroxyapatite for biomedical applications, J Vis Exp (120)
(2017) 55343.
[109] K.T. Shalumon, S. Sowmya, D. Sathish, K.P. Chennazhi, S.V. Nair, R. Jayakumar,
Effect of incorporation of nanoscale bioactive glass and hydroxyapatite in PCL/
chitosan nanofibers for bone and periodontal tissue engineering, J. Biomed.
Nanotechnol. 9 (3) (2013) 430–440.
[110] N.P. Wijedasa, S.M. Broas, R.E. Daso, I.A. Banerjee, Varying fish scale derived
hydroxyapatite bound hybrid peptide nanofiber scaffolds for potential
applications in periodontal tissue regeneration, Mater Sci Eng C Mater Biol Appl
109 (2020), 110540.
[111] J.W. Shen, T. Wu, Q. Wang, H.H. Pan, Molecular simulation of protein adsorption
and desorption on hydroxyapatite surfaces, Biomaterials 29 (5) (2008) 513–532.
[112] W.-K. Liu, B.-S. Liaw, H.-K. Chang, Y.-F. Wang, P.-Y. Chen, From waste to health:
Synthesis of hydroxyapatite Sscaffolds from fish scales for lead ion removal, JOM
69 (4) (2017) 713–718.
[113] B.S. Liaw, T.T. Chang, H.K. Chang, W.K. Liu, P.Y. Chen, Fish scale-extracted
hydroxyapatite/chitosan composite scaffolds fabricated by freeze casting-An
innovative strategy for water treatment, J. Hazard. Mater. 382 (2020), 121082.
D. Qin et al.
[114] S. Kongsri, K. Janpradit, K. Buapa, S. Techawongstien, S. Chanthai,
Nanocrystalline hydroxyapatite from fish scale waste: Preparation,
characterization and application for selenium adsorption in aqueous solution,
Chem. Eng. J. 215–216 (2013) 522–532.
[115] P. Sricharoen, N. Limchoowong, P. Nuengmatcha, S. Chanthai, Ultrasonic-assisted
recycling of Nile tilapia fish scale biowaste into low-cost nano-hydroxyapatite:
Ultrasonic-assisted adsorption for Hg2+ removal from aqueous solution followed
by “turn-off” fluorescent sensor based on Hg2+graphene quantum dots,
Ultrasonics - Sonochemistry 63 (2020), 104966.
[116] N.N. Panda, K. Pramanik, L.B. Sukla, Extraction and characterization of
biocompatible hydroxyapatite from fresh water fish scales for tissue engineering
scaffold, Bioprocess Biosyst. Eng. 37 (3) (2013) 433–440.
[117] N.S.S.A. Buraiki, B. Ali Albadri, S. Alsheriqi, B. Alshabibi, S. Al-Mammari, S.
Premkumar, M.K. Sah, M.S. Sudhakar, Characterization of Catla catla and
Oreochromis niloticus fish scales derived hydroxyapatite scaffolds for
regenerative medicine, Materials Today: Proceedings 25(Part 3) (2019) 2609-
2616.
[118] P. Deb, E. Barua, S. Das Lala, A.B. Deoghare, Synthesis of hydroxyapatite from
Labeo rohita fish scale for biomedical application, Mater. Today:. Proc. 15 (2019)
277–283.
[119] W.D. Norris, J.G. Steele, G. Johnson, P.A. Underwood, Serum enhancement of
human endothelial cell attachment to and spreading on collagens I and IV does
not require serum fibronectin or vitronectin, J. Cell Sci. 95 (Pt 2)(2) (1990) 255.
[120] M. Terada, K. Izumi, H. Ohnuki, T. Saito, H. Kato, M. Yamamoto, Y. Kawano,
K. Nozawa-Inoue, H. Kashiwazaki, T. Ikoma, J. Tanaka, T. Maeda, Construction
and characterization of a tissue-engineered oral mucosa equivalent based on a
chitosan-fish scale collagen composite, J. Biomed. Mater. Res. B Appl. Biomater.
100 (7) (2012) 1792–1802.
[121] T. Ikoma, H. Kobayashi, J. Tanaka, D. Walsh, S. Mann, Physical properties of type
I collagen extracted from fish scales of Pagrus major and Oreochromis niloticas,
Int. J. Biol. Macromol. 32 (3–5) (2003).
[122] R. Matsumoto, T. Uemura, Z. Xu, I. Yamaguchi, T. Ikoma, J. Tanaka, Rapid
oriented fibril formation of fish scale collagen facilitates early osteoblastic
differentiation of human mesenchymal stem cells, J. Biomed. Mater. Res. Part A
103 (8) (2015) 2531–2539.
[123] H. Mori, Y. Tone, K. Shimizu, K. Zikihara, S. Tokutomi, T. Ida, H. Ihara, M. Hara,
Studies on fish scale collagen of Pacific saury (Cololabis saira), Mater Sci Eng C
Mater Biol Appl 33 (1) (2013) 174–181.
[124] T.D. Sutherland, Y.Y. Peng, H.E. Trueman, S. Weisman, S. Okada, A.A. Walker,
A. Sriskantha, J.F. White, M.G. Huson, J.A. Werkmeister, V. Glattauer,
V. Stoichevska, S.T. Mudie, V.S. Haritos, J.A. Ramshaw, A new class of animal
collagen masquerading as an insect silk, Sci. Rep. 3 (2013) 2864.
[125] P.L. Privalov, Stability of proteins: Proteins which do not present a single
cooperative system, Adv. Protein Chem. 35 (1982) 1–104.
[126] B.J. Rigby, Amino-acid composition and thermal stability of the dkin collagen of
the Antarctic ice-fish, Nature 219 (5150) (1968) 166–167.
[127] F. Pati, B. Adhikari, S. Dhara, Isolation and characterization of fish scale collagen
of higher thermal stability, Bioresour. Technol. 101 (10) (2010) 3737–3742.
[128] E.E. Antoine, P.P. Vlachos, M.N. Rylander, Review of collagen I hydrogels for
bioengineered tissue microenvironments: Characterization of mechanics,
structure, and transport, Tissue Engineering Part B Reviews 20 (6) (2014)
683–696.
[129] S.M. Oliveira, R.A. Ringshia, R.Z. Legeros, E. Clark, M.J. Yost, L. Terracio, C.
C. Teixeira, An improved collagen scaffold for skeletal regeneration, J. Biomed.
Mater. Res. Part A 94A (2) (2010) 371–379.
[130] Y. Takagi, K. Ura, Teleost fish scales: a unique biological model for the fabrication
of materials for corneal stroma regeneration, J. Nanosci. Nanotechnol. 7 (3)
(2007) 757–762.
[131] Y.J. Hsueh, D.H. Ma, K.S. Ma, T.K. Wang, C.H. Chou, C.C. Lin, M.C. Huang, L.
J. Luo, J.Y. Lai, H.C. Chen, Extracellular matrix protein coating of processed fish
scales improves human corneal endothelial cell adhesion and proliferation, Transl
Vis Sci Technol 8 (3) (2019) 27.
[132] F. Yuan, L. Wang, C.-C. Lin, C.-H. Chou, L. Li, A cornea substitute derived from
fish scale: 6-month followup on rabbit model, Journal of Ophthalmology 2014
(2014) 1–6.
[133] C.C. Lin, R. Ritch, S.M. Lin, M.H. Ni, Y.C. Chang, Y.L. Lu, H.J. Lai, F.H. Lin, A new
fish scale-derived scaffold for corneal regeneration, European Cells and Materials
19 (2010) 50–57.
[134] T.H. van Essen, L. van Zijl, T. Possemiers, A.A. Mulder, S.J. Zwart, C.H. Chou, C.
C. Lin, H.J. Lai, G.P.M. Luyten, M.J. Tassignon, N. Zakaria, A. El Ghalbzouri, M.
J. Jager, Biocompatibility of a fish scale-derived artificial cornea: Cytotoxicity,
cellular adhesion and phenotype, and in vivo immunogenicity, Biomaterials 81
(2016) 36–45.
[135] M. Parekh, B. Van den Bogerd, N. Zakaria, D. Ponzin, S. Ferrari, Fish scale-derived
scaffolds for culturing human corneal endothelial cells, Stem Cells Int 2018
(2018) 8146834.
[136] S. Huang, X. Fu, Naturally derived materials-based cell and drug delivery systems
in skin regeneration, J. Control. Release 142 (2) (2010) 149–159.
[137] H. Yoon, G. Kim, A three-dimensional polycaprolactone scaffold combined with a
drug delivery system consisting of electrospun nanofibers, J. Pharm. Sci. 100 (2)
(2011) 424–430.
[138] Y. Shi, H. Zhang, X. Zhang, Z. Chen, D. Zhao, J. Ma, A comparative study of two
porous sponge scaffolds prepared by collagen derived from porcine skin and fish
scales as burn wound dressings in a rabbit model, Regen Biomater 7 (1) (2020)
63–70.
21
Chemical Engineering Journal 428 (2022) 131102
[139] J.K. Wang, K.P. Yeo, Y.Y. Chun, T.T.Y. Tan, N.S. Tan, V. Angeli, C. Choong, Fish
scale-derived collagen patch promotes growth of blood and lymphatic vessels in
vivo, Acta Biomater. 63 (2017) 246–260.
[140] P. Pal, P.K. Srivas, P. Dadhich, B. Das, P.P. Maity, D. Moulik, S. Dhara,
Accelerating full thickness wound healing using collagen sponge of mrigal fish
(Cirrhinus cirrhosus) scale origin, Int. J. Biol. Macromol. 93 (2016) 1507–1518.
[141] I.B. Pathan, S.J. Mundea, S. Shelkeb, C.M. Settyd, Curcumin loaded fish scale
collagen-HPMC nanogel for wound healing application: Ex-vivo and In-vivo
evaluation, International Journal of Polymeric Materials and Polymeric
Biomaterials 68 (4) (2019) 165–174.
[142] X. Feng, X. Zhang, S. Li, Y. Zheng, X. Shi, F. Li, S. Guo, J. Yang, Preparation of
aminated fish scale collagen and oxidized sodium alginate hybrid hydrogel for
enhanced full-thickness wound healing, Int. J. Biol. Macromol. 164 (2020)
626–637.
[143] O. Olatunji, M. Olubowale, C. Okereke, Microneedle-assisted transdermal
delivery of acetylsalicylic acid (aspirin) from biopolymer films extracted from fish
scales, Polym. Bull. 75 (9) (2017) 4103–4115.
[144] P. Medhi, O. Olatunji, A. Nayak, C.T. Uppuluri, R.T. Olsson, B.N. Nalluri, D.
B. Das, Lidocaine-loaded fish scale-nanocellulose biopolymer composite
microneedles, AAPS PharmSciTech 18 (5) (2017) 1488–1494.
[145] O. Olatunji, A. Denloye, Production of hydrogel microneedles from fish scale
biopolymer, J. Polym. Environ. 27 (6) (2019) 1252–1258.
[146] E. Prina, M.H. Amer, L. Sidney, M. Tromayer, F. Rose, Bioinspired precision
engineering of three-imensional epithelial stem cell microniches, Adv. Biosyst. 4
(6) (2020), e2000016.
[147] A. Suzuki, Y. Kodama, K. Miwa, K. Kishimoto, K. Izumi, Manufacturing
micropatterned collagen scaffolds with chemical-crosslinking for development of
biomimetic tissue-engineered oral mucosa, Sci. Rep. 10 (1) (2020) 22192.
[148] A. Suzuki, H. Kato, T. Kawakami, Y. Kodama, M. Shiozawa, H. Kuwae, K. Miwa,
E. Hoshikawa, K. Haga, A. Shiomi, A. Uenoyama, I. Saitoh, H. Hayasaki,
J. Mizuno, K. Izumi, Development of microstructured fish scale collagen scaffolds
to manufacture a tissue-engineered oral mucosa equivalent, J. Biomater. Sci.
Polym. Ed. 31 (5) (2020) 578–600.
[149] J. Tang, T. Saito, Biocompatibility of novel type I collagen purified from Tilapia
fish scale: An in vitro comparative study, Biomed Res. Int. 2015 (2015), 139476.
[150] M.C. Gómez-Guillén, M. Pérez-Mateos, J. Gómez-Estaca, E. López-Caballero,
B. Giménez, P. Montero, Fish gelatin: a renewable material for developing active
biodegradable films, Trends Food Sci. Technol. 20 (1) (2009).
[151] A. Etxabide, K. de la Caba, P. Guerrero, A novel approach to manufacture porous
biocomposites using extrusion and injection moulding, Eur. Polym. J.
S0014305716301847 (2016).
[152] C.Y. Huang, T.C. Wu, Y.H. Hong, S.L. Hsieh, H.R. Guo, R.H. Huang, Enhancement
of cell adhesion, cell growth, wound healing, and oxidative protection by gelatins
extracted from extrusion-pretreated Tilapia (Oreochromis sp.) fish scale,
Molecules 23 (10) (2018) 2406.
[153] Y. Zhang, D. Tu, Q. Shen, Z. Dai, Fish scale valorization by hydrothermal
pretreatment followed by enzymatic hydrolysis for gelatin hydrolysate
production, Molecules 24 (16) (2019) 2998.
[154] A. Beishenaliev, S.S. Lim, K.Y. Tshai, P.S. Khiew, H.N. Moh’d Sghayyar, H.-S. Loh,
Fabrication and preliminary in vitro evaluation of ultraviolet-crosslinked
electrospun fish scale gelatin nanofibrous scaffolds, J. Mater. Sci. - Mater. Med. 30
(6) (2019) 62.
[155] S.-J. Wu, Y.-C. Ho, S.-Z. Jiang, F.-L. Mi, Effect of tannic acid–fish scale gelatin
hydrolysate hybrid nanoparticles on intestinal barrier function and α-amylase
activity, Food Funct. 6 (7) (2015) 2283–2292.
[156] X. Zhang, T. Ye, X. Meng, Z. Tian, L. Pang, Y. Han, H. Li, G. Lu, F. Xiu, H.D. Yu,
J. Liu, W. Huang, Sustainable and transparent fish gelatin films for flexible
electroluminescent devices, ACS Nano 14 (4) (2020) 3876–3884.
[157] N. Nuamsrinuan, N. Suttisiri, E. Hoonnivathana, P. Limsuwan, K. Naemchanthara,
Effect of fish scales gelatin and mixing ratio on chemical and mechanical
characteristics of gelatin/chitosan films, Appl. Mech. Mater. 866 (2017) 8–11.
[158] P. Guerrero, I. Zugasti, A. Etxabide, H.N.D. Bao, T. Trang Si, M. Penalba, K. de la
Caba, Effect of fructose and ascorbic acid on the performance of cross-linked fish
gelatin films, Polymers (Basel) 12 (3) (2020) 570.
[159] A. Manikandan, S. Thirupathi Kumara Raja, T. Thiruselvi, A. Gnanamani,
Engineered fish scale gelatin: An alternative and suitable biomaterial for tissue
engineering, Journal of Bioactive and Compatible Polymers 33 (3) (2017)
332–346.
[160] D.Y. Wu, S.S. Wang, C.S. Wu, Antibacterial properties and cytocompatibility of
biobased nanofibers of fish scale gelatine, modified polylactide, and freshwater
clam shell, Int. J. Biol. Macromol. 165 (Pt A) (2020) 1219–1228.
[161] Z. Zhang, J. Wang, Y. Ding, X. Dai, Y. Li, Oral administration of marine collagen
peptides from Chum Salmon skin enhances cutaneous wound healing and
angiogenesis in rats, J. Sci. Food Agric. 91 (12) (2011) 2173–2179.
[162] R.C. Cheung, T.B. Ng, J.H. Wong, Marine peptides: bioactivities and applications,
Mar. Drugs 13 (7) (2015) 4006–4009.
[163] D.-H. Ngo, Z.-J. Qian, B. Ryu, J.W. Park, S.-K. Kim, In vitro antioxidant activity of
a peptide isolated from Nile tilapia (Oreochromis niloticus) scale gelatin in free
radical-mediated oxidative systems, J. Funct. Foods 2 (2) (2010) 107–117.
[164] H. Ohara, H. Iida, K. Ito, Y. Takeuchi, Y. Nomura, Effects of Pro-Hyp, a collagen
hydrolysate-derived peptide, on hyaluronic acid synthesis using in vitro cultured
synovium cells and oral Ingestion of collagen hydrolysates in a guinea pig model
of osteoarthritis, Journal of the Agricultural Chemical Society of Japan 74 (10)
(2010) 2096–2099.
[165] J. Asserin, E. Lati, T. Shioya, J. Prawitt, The effect of oral collagen peptide
supplementation on skin moisture and the dermal collagen network: evidence
D. Qin et al.
from an ex vivo model and randomized, placebo-controlled clinical trials,
J Cosmet Dermatol 14 (4) (2015) 291–301.
[166] C. Liu, J. Sun, Potential application of hydrolyzed fish collagen for inducing the
multidirectional differentiation of rat bone marrow mesenchymal stem cells,
Biomacromolecules 15 (1) (2014) 436–443.
[167] F. Subhan, H.Y. Kang, Y. Lim, M. Ikram, S.Y. Baek, S. Jin, Y.H. Jeong, J.Y. Kwak,
S. Yoon, Fish scale collagen peptides protect against CoCl2/TNF-α-induced
cytotoxicity and inflammation via inhibition of ROS, MAPK, and NF-kappaB
pathways in HaCaT cells, Oxid Med Cell Longev 2017 (2017) 9703609.
[168] S. Vigneswari, V. Murugaiyah, G. Kaur, H.P. Abdul Khalil, A.A. Amirul,
Biomacromolecule immobilization: grafting of fish-scale collagen peptides onto
aminolyzed P(3HB-co-4HB) scaffolds as a potential wound dressing, Biomed.
Mater. 11 (5) (2016), 055009.
[169] S. Arcidiacono, D.L. Kaplan, Molecular weight distribution of chitosan isolated
from Mucor rouxii under different culture and processing conditions, Biotechnol.
Bioeng. 39 (3) (1992) 281–286.
[170] S. Kumari, P.K. Rath, Extraction and characterization of chitin and chitosan from
(Labeo rohit) fish scales, Procedia Mater. Sci. 6 (2014) 482–489.
[171] I.F.M. Rumengan, P. Suptijah, S. Wullur, A. Talumepa, Characterization of chitin
extracted from fish scales of marine fish species purchased from local markets in
North Sulawesi, Indonesia, Earth and Environmental Science 89 (2017), 012028.
[172] K. Karimzadeh, Anticoagulant effects of glycosaminoglycan extracted from fish
scales, International Journal of Basic Science in Medicine 3 (2) (2018) 72–77.
[173] C. Irawan, Y.F. Arifin, R. Marisa, M. Asnia, Biopolymer of chitosan from fish
scales as natural coagulant for groundwater treatment, IOP Conf. Series: Earth
and Environmental, Science 175 (2018), 012028.
22
Chemical Engineering Journal 428 (2022) 131102
[174] F.Z. Aboudamia, M. Kharroubi, M. Neffa, F. Aatab, S. Hanoune, M. Bouchdoug,
A. Jaouad, Potential of discarded sardine scales (Sardina pilchardus) as chitosan
sources, J. Air Waste Manag. Assoc. 70 (11) (2020) 1186–1197.
[175] R. Pobletea, E. Cortesa, J. Bakitb, Y. Luna-Galianoc, Landfill leachate treatment
using combined fish scales based activated carbon and solar advanced oxidation
processes, Process Saf. Environ. Prot. 123 (2019) 253–262.
[176] S.O. Ojwach, J.O. Lalah, C.O. Kowenje, G.O. Achieng, Preparation,
characterization of fish scales biochar and their applications in the removal of
anionic indigo carmine dye from aqueous solutions, Water Sci. Technol. 80 (11)
(2019) 2218–2231.
[177] W.N. Wang, Y. Kaihatsu, F. Iskandar, K. Okuyama, Highly luminous hollow
chloroapatite phosphors formed by a template-free aerosol route for solid-state
lighting, Chem. Mater. 21 (19) (2009) 4685–4691.
[178] I. Demnati, D. Grossin, O. Marsan, G. Bertrand, G. Collonges, C. Combes, M.
Parco, I. Braceras, J. Alexis, Y. Balcaen, C. Rey, Comparison of physical-chemical
and mechanical properties of chlorapatite and hydroxyapatite plasma sprayed
coatings, The Open Biomedical Engineering Journal 9(Suppl 1-M3) (2015) 42-55.
[179] J.S. Cho, D.S. Yoo, Y.-C. Chung, S.-H. Rhee, Enhanced bioactivity and
osteoconductivity of hydroxyapatite through chloride substitution, J. Biomed.
Mater. Res. Part A 102 (2) (2014) 455–469.
[180] C. Piccirillo, R.C. Pullar, D.M. Tobaldi, P.M.L. Castro, M.M.E. Pintado,
Hydroxyapatite and chloroapatite derived from sardine by-products, Ceram. Int.
40 (8) (2014) 13231–13240.
[181] L.A. Cavalcante, L.S. Ribeiro, M.L. Takeno, P.T.P. Aum, Y. Aum, J.C.S. Andrade,
Chlorapatite derived from fish scales, Materials (Basel) 13 (5) (2020) 1129.