Received: 29 June 2023 Revised: 21 September 2023 Accepted: 25 October 2023

DOI: 10.1111/1750-3841.16831

ORIGINAL ARTICLE
Fo o d E n g i n e e r i n g , M a t e r i a l s S c i e n c e , & Na n o t e c h n o l o g y

Antifungal edible coatings for fruits based on zein and

chitosan nanowhiskers
Carolina L. Almeida1 Lucas R. F. Figueiredo2 Diego V. M. Ribeiro1
Adillys M. C. Santos3 Evandro L. Souza4 Kataryne A. R. Oliveira4
Juliano E. Oliveira5 Eliton S. Medeiros2
1 Postgraduate Program in Materials Science and Engineering, Federal University of Paraíba (UFPB), João Pessoa, Brazil
2 Materials and Biosystems laboratory (LAMAB), Center of Technology (CT), Federal University of Paraíba (UFPB), João Pessoa-PB, Brazil
3 Center for Science and Technology in Energy and Sustainability, Federal University of Recôncavo da Bahia, Feira de Santana-BA, Brazil
4 Laboratory of Food Microbiology, Department of Nutrition, Health Science Center (CCS), Federal University of Paraíba (UFPB), João Pessoa-PB,
Brazil
5 Materials and Biosystems laboratory (LAMAB), Department of Engineering, Federal University of Lavras, Lavras-MG, Brazil

Correspondence
Eliton S. Medeiros, Materials and Abstract: Fresh produce have a more limited shelf life than processed ones.
Biosystems laboratory (LAMAB), Center Their sensory attributes such as appearance and surface texture are important
of Technology (CT), Federal University of
Paraíba (UFPB), CEP 58051–900 João features in consumer perception and liking. The decomposition of fresh pro-
Pessoa-PB, Brazil. Email: duce, which is caused by enzymes, chemical reactions, and microbial infections,
[email protected]
often caused by Colletotrichum species, is inevitable. However, it can be slowed
Funding information down. Several materials have been developed for this purpose, with an empha-
Coordenação de Aperfeiçoamento de sis on active coatings using nanomaterials. In this study, the protective effects
Pessoal de Nível Superior; Conselho
of a zein coating containing chitosan nanowhiskers (CSW) for the maintenance
Nacional de Desenvolvimento Científico e
Tecnológico; Scientific and Technological of fruit quality were investigated using guava (Psidium guajava L.) as a model
Development National Research Council, fruit. CSW were previously characterized, and their antifungal effects against dis-
Grant/Award Numbers: 306.447/2018-5,
305880/2021-7, 405.802/2022-6,
tinct Colletotrichum species (Colletotrichum asianum, Colletotrichum tropicale,
406.973/2022-9, 305.065/2022-0; Colletotrichum gloeosporioides, and Colletotrichum brevisporum) were proven.
Coordination for the Improvement of Coatings were characterized by thermogravimetric analysis, optical profilome-
Higher Education Personnel (CAPES); the
Minas Gerais state funding agency, try, and mechanical properties. Total soluble solids, pH, mass loss, and visual
Grant/Award Numbers: APQ-00153-23, inspection of uncoated and coated guava fruits were also verified during 9 days.
BPD-00406-22
Results show that CSW length and aspect ratio decreased for longer extraction
times. A similar behavior was found for x-ray diffraction in which peak inten-
sity decreases under the same conditions. CSW degradation (ca. 250–400◦ C) also
depends on extraction time in which more crystalline whiskers are the most ther-
mally stable ones. The addition of CSW did not significantly (p < 0.05) modify the
homogeneity and continuity of coating but prevented microbial growth assuring
fruit quality during storage. In summary, coatings protected guava fruits from
post-harvest spoilage while preserving quality and extending shelf life.
Practical Application: Fresh foods such as fruits and vegetables have a more
limited shelf life than processed ones.

J. Food Sci. 2023;1–15. wileyonlinelibrary.com/journal/jfds © 2023 Institute of Food Technologists. 1

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2 ANTIFUNGAL EDIBLE COATINGS FOR FRUITS

KEYWORDS
antifungal, chitosan nanowhisker, coating, fruit preservation, nanotechnology

1 INTRODUCTION packaging can be an alternative to overcome many of the

abovementioned problems.
Food quality has emerged as a strong competitive factor, Active packaging based on films and coatings need to
owing to its indispensability in meeting consumer expec- present adequate properties for their use, as significant
tations. The globalization of production, combined with losses in quality can occur due to the transfer of mois-
the increase in consumer awareness and demands from ture, gases, aroma, flavor, or even color to the surrounding
government agencies, have made food quality and safety a environment (Bankier et al., 2019). One of the most exten-
key factor in food industries. Food quality can be evaluated sively employed natural film-forming materials is zein, a
by the decrease in the sensory characteristics of products, hydrophobic protein derived from corn endosperm (Yang
such as texture, flavor (taste), aroma, and visual aspects, et al., 2021). Zein is a good candidate for the develop-
according to the needs and satisfaction of consumers (Amit ment of edible food coatings due to its biodegradability
et al., 2017). Frequently, a significant amount of time and biocompatibility. On the other hand, chitosan (CS) is
elapses from the harvesting of a product until it finally a natural polymer obtained from the chemical deacetyla-
reaches the consumer, involving lengthy transportation tion of chitin (CT), which is the second most abundant
processes along the way. In this context, it becomes impera- polysaccharide in nature. This polymer has been used in
tive to implement quality control measures throughout the the food industry because of its biocompatibility, non-toxic
food chain. This necessity has led to a growing demand nature, and antimicrobial properties, especially when used
for investments in research and development, aimed at in the form of nanowhiskers due to their high surface area
discovering innovative tools that can enhance the effec- (Confederat et al., 2021; Corradini et al., 2014; Ibrahim &
tiveness of quality control, ultimately reducing food losses El-Zairy, 2015; Morin-Crini et al., 2019; Pereira et al., 2020;
and minimizing waste (Cattaneo et al., 2021). Spirescu et al., 2021).
Fresh foods are the most challenging as they have a In the present study, zein-based films for coating
shorter shelf life (Jideani et al., 2017). In recent years, the guava (Psidium guajava L.) with addition of chitosan
search for a good diet with the consumption of unpro- nanowhiskers (CSW) were developed, different fruit
cessed or minimally processed foods, brings continuous quality parameters were analyzed, and their physical,
demands to develop new preservation techniques for per- mechanical, and antimicrobial properties were evaluated
ishable products (Giannakourou & Tsironi, 2021; Jideani against Colletotrichum strains (Colletotrichum asianum,
et al., 2017). One of the main problems in food preservation Colletotrichum tropicale, Colletotrichum gloeosporioides,
is the presence of microorganisms that can rapidly degrade and Colletotrichum brevisporum).
food quality. In recent years, the necessity for the effec-
tive control of anthracnose caused by the distinct species
of the phytopathogenic fungi Colletotrichum has become a 2 MATERIALS AND METHODS
key point for producers, as these infections sharply reduce
the quality and shelf life of the fruits and affects the market 2.1 Materials
value and consumer acceptance (Danh et al., 2021; Wang
et al., 2023). Chitin (Sigma-Aldrich/C7170, Barueri/SP, Brazil), sul-
Application of natural bioactive molecules is an alter- furic acid PA (Química Moderna Indústria e Comér-
native to the use of synthetic fungicides to control post- cio, Barueri/SP, Brazil), and tubular cellulose membrane
harvest disease in edible fruits (Demartelaere et al., 2017; (Sigma-Aldrich, Barueri/SP, Brazil) were used for the
Zakaria, 2021). Edible polymers with the incorporation of extraction and dialysis of nanowhiskers from chitin.
nanometric structures by emulsion or simple dispersion Sodium hydroxide PA (Química Moderna Indústria e
have largely been used in coating not only for the preser- Comércio, Barueri/SP, Brazil) and sodium borohydride
vation of the sensory properties of fruits but also to exert (Sigma-Aldrich, 99%, Barueri/SP, Brazil) were used to
antimicrobial effects to avoid post-harvest losses caused obtain CSW. Zein (Sigma-Aldrich, Z3625, Barueri/SP,
by microorganisms (Bautista-Baños et al., 2017; Guimarães Brazil) and acetic acid (VWR Chemicals - 100%, Lisboa,
et al., 2020; Wang et al., 2017). Moreover, the use of active Portugal) were used to produce the edible coatings.
 17503841, 0, Downloaded from https://ift.onlinelibrary.wiley.com/doi/10.1111/1750-3841.16831 by Universidade Federal Da Paraiba, Wiley Online Library on [29/11/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
ANTIFUNGAL EDIBLE COATINGS FOR FRUITS 3

Guava fruits (P. guajava L.), Paluma variety, were 2.3.2 Crystallinity by XRD
obtained directly from a local market in the city of João
Pessoa (Paraiba, Brazil). Fruits were with the first signs To measure the crystallinity of nanowhiskers, x-ray diffrac-
of skin yellowing (stage 1 of ripening) and selected based tion (XRD) spectra were recorded using a Cu Kα radiation
on size and skin uniformity, and absence of mechanical diffractometer (λ = 1.5406 Å) under a 45 kV anode volt-
and/or physiological injuries. age and 40 mA current. Previously dried samples were
pressed between two 1 mm patterned-glass slides and XRD
patterns were performed between 2θ = 5◦ and 2θ = 40◦
2.2 Extraction of CSW at a scan rate of 2◦ /min. XRD data were smoothed using
10-point smoothing in a second-order regression based
CSW were prepared following the method proposed by on the Savitzky–Golay filter (Microcal Origin™ 8.0). The
Pereira (Pereira et al., 2014) from the deacetylation of chitin crystallinity index (CI) was calculated as:
nanowhiskers in 50% (w/v) aqueous sodium hydroxide
(NaOH) solution, containing 0.5% (w/v) sodium borohy- 𝐴𝑐
CI (%) = 𝑥100 (1)
dride (NaBH4 ), used as the reducing agent to prevent 𝐴𝑡
extensive depolymerization of chitosan. The proportion
of chitin nanoparticles in the aqueous solution of NaOH where, Ac is the crystalline, and At the total, amorphous
was 1 g/10 mL at 120◦ C for 20 min. The product obtained and crystalline area under the curve between 2θ = 5◦ and
was diluted with ice-cold distilled water and centrifuged 30◦ . Diffraction curves were deconvoluted based on a
at 10,000 rpm for 10 min. This process was repeated three Gauss or Lorentzian functions using Microcal Origin™
times. The suspension was dialyzed in distilled water for 3 8.0 software for the description of individual signals.
days until pH reached 6.0. Suspension homogeneity was Crystallite size was estimated using the Scherrer equation.
further achieved with the aid of an ultrasound bath for
5 min. The resulting suspension was filtered to remove 𝑑ℎ𝑘𝑙 = 0.9 𝜆 𝛽1∕2 𝑐𝑜𝑠𝜃 (2)
residual aggregates and kept refrigerated (5 ± 0.5◦ C) before
further use. This extraction process was carried out for 30, where, dhkl is the crystal dimension perpendicular to the
60, 90, and 120 min, and samples coded, respectively, as diffraction plane with Miller hkl indices, λ is the x-ray radi-
CSW30, CSW60, CSW90, and CSW120. ation with wavenumber (λ = 0.154 nm), and β1/2 the full
width at half maximum (FWHM) of the diffraction peak
(Pereira et al., 2014).
2.3 Characterization

2.3.1 Morphological characterization of 2.3.3 Fourier Transform Infrared

CSW by AFM and DLS Spectroscopy
Chitin and CSW morphology were accessed using a SPM A spectrometer (IRAffinity−1 /SHIMADZU) was used to
9600 (Shimadzu, Japan) atomic force microscope (AFM) characterize the CSW in pressed KBr disks. Fourier trans-
operating in the tapping mode. Nanowhiskers were dis- form infrared spectroscopy (FTIR) spectra were recorded
persed in deionized water at a concentration of 0.1 mg/mL, between 4000 and 400 1/cm with a resolution of 4 1/cm in
and a 50 µL aliquot was deposited on a freshly cleaved mica a 128-scan transmittance mode at room temperature.
surface and kept at room temperature for 24 h until com-
plete solvent evaporation. The length and aspect ratio of
the nanowhiskers were determined for all treatments with
the aid of Image J software (NIH, Bethesda, MD, USA). 2.3.4 Thermogravimetric analysis
The hydrodynamic radius of CSW was measured by
dynamic light scattering (DLS) using a ZetaSizer (Malvern, Thermogravimetric analysis (TGA) of chitin and CSW
ZS90 nanoseries). All dispersions were diluted to a con- were carried out in a temperature range from 25 to 600◦ C
centration of 0.1% nanowhisker using HCl to set pH to 1.0. under a heating rate of 10◦ C/min using 5 mg of sample, in
Zeta potential was measured from pH 1 to 12 using a 0.01% a controlled atmosphere of nitrogen at 30 mL/min, with a
NaOH as the titrant solution. TGA-50 thermogravimetry analyzer (Shimadzu).
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4 ANTIFUNGAL EDIBLE COATINGS FOR FRUITS

F I G U R E 1 Atomic force microscope micrographs of chitosan nanowhiskers extracted for: (a) 30 min, CSW30; (b) 60 min, CSW60; (c)
90 min, CSW90; and (d) 120 min, CSW120.

2.3.5 Antifungal activity University of Pernambuco, Recife, Brazil). Initially, an agar

plug (5 mm in diameter) containing the mycelia of each
The effects of CSW under different extraction conditions strain was taken from the edge of a 7-day culture grown in
were tested for the inhibition of the radial mycelial growth potato dextrose agar (PDA) at 25◦ C, then transferred to the
of distinct Colletotrichum strains (C. asianum CCM 4057, center of a Petri dish containing PDA supplemented with
C. tropicale CMM 4071, C. gloeosporioides CMM 320, and C. CSW at distinct concentrations (8, 6, 4, and 2 mg/mL), fol-
brevisporum CMM 1936) using the poisoned substrate tech- lowed by incubation at 25◦ C in the dark. For reliability of
nique (dilution in solid medium). These strains have been results, commercial chitosan, without whisker production
associated with the development of anthracnose in fruit (pH 5.6), was similarly tested for negative control. Radial
and were gently provided by Culture Collection of Phy- mycelial growth was measured daily for 10 days or when
topathogenic Fungi, Prof. Maria Menezes (Federal Rural the negative control Petri dish was completely covered.
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ANTIFUNGAL EDIBLE COATINGS FOR FRUITS 5

depth, where solutions evaporated at 40◦ C for 24 h in an

oven. Moreover, spin-coated films were prepared (Ji et al.,
2017). Solutions (150 µL) were slowly cast onto glass slides
(22 × 22 mm) at 1000 rpm and retention time of 30 s.

2.4.2 Morphological studies

The edible coatings were produced in an aqueous solution

of acetic acid (3:1), in triplicate, by spin coating to deter-
mine thickness and roughness. Spun-coated films on glass
slides were measured for roughness by optical profilometry
(Taylor Hobson, CCI/MP). Film thickness was measured
F I G U R E 2 X-ray diffraction of chitosan nanowhisker under after the formation of a step between the coating and the
different treatments. glass slide.

The radial growth diameter (mm) of each strain colony 2.4.3 Thermogravimetric analysis
was measured in two perpendicular directions, and the
average colony diameter was obtained. The percentage of The TG characterization tests for this step followed the
mycelial growth inhibition (MGI%) was calculated using same procedures described in Section 2.3.4.
the formula:

𝐶−𝑇
MGI (%) = 𝑥100 (3) 2.4.4 Mechanical properties
𝐶

where C is the diameter of the colony in the control Mechanical properties of the coatings were evaluated on
assay, and T is the diameter of the colony growing in PDA specimens cast from Teflon molds. Tests samples were
supplemented with CSW (Oliveira et al., 2023). 50 mm in width and 80 mm in length, and about 0.2 mm in
The combinations of concentration (8, 6, 4, and thickness. Tests were carried out according to the Ameri-
2 mg/mL) and extraction time of the CSW (30, 60, 90, can Society for Testing and Materials (ASTM 882-02) using
and 120 min) were tested to verify the inhibitory effects a universal testing machine (Instron - 3300) analyzed
on the tested Colletotrichum strains. The experiments were by Bluehill software to determine the maximum tensile
performed in triplicate on three distinct occasions. Data strength, elongation at break, and elastic modulus at a
were submitted to analysis of variance, applying the Tukey speed of 1 mm/min.
test at 5%, and polynomial regression for significant sim-
ple effects. The Excel program (Microsoft Corporation) was
used for the statistical analysis of the data using the Pop 2.4.5 Coating studies
tools macro. In addition, photographs of the fruits were
recorded during storage for a better visual understanding After inspection and selection, the guava fruits were san-
of the results. itized with a neutral detergent, immersed in a 100-ppm
chlorine solution for 3 min, and dried at room tempera-
◦
ture (25 C). The fruits were then separated in groups of 18
2.4 Edible coatings fruits and subjected to treatment by immersion in the coat-
ing solution for 60 s, that is, uncoated (U), coated with zein
2.4.1 Film preparation (Z), and zein + 1% chitosan (Z + CSW) nanowhiskers. After
immersion, the coating excess was drained, and the fruits
For preparation of the coating films, powdered zein was were placed on rigid polystyrene trays for normal ripen-
gradually dissolved in an aqueous acetic acid solution ing at 26◦ C and 65% humidity for 10 days. Three randomly
(4:1/3:1/2:1/1:1) under constant agitation until reaching a chosen fruits were then picked out every 3 days for the
final concentration of 20 g/100 mL. The coating suspen- analysis.
sions were kept under agitation until complete solubiliza- Total soluble solids were determined by refractome-
tion. Films were prepared with the aid of Teflon casting try using a manual refractometer model 107BP Biobrix,
molds of approximately 5 cm in length and 1 mm in with readings expressed in ◦ Brix. The analysis of mass
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6 ANTIFUNGAL EDIBLE COATINGS FOR FRUITS

T A B L E 1 Chitosan nanowhisker dimensions by dynamic light TA B L E 2 Peak assignments of chitin, chitosan, and CSW.
scattering and atomic force microscope image measurements. Wavelength (cm−1 ) Attributes
a
Sample DLS (nm) AFM (nm) Aspect ratio 3450 Stretching O—H
CSW30 634 510 ± 144 203 ± 52 3260 Stretching N—H
CSW60 489 360 ± 104 169 ± 40 2900–2800 Vibration C—H
CSW90 336 244 ± 73 129 ± 32 1660 Stretching C=O (Amide I)
CSW120 311 198 ± 45 95 ± 25 1560 Vibration N—H (Amide II)
a
Measured by atomic force microscope. 1380 Symmetrical deformation CH3
1160 Asymmetric stretch of C—O—C and
stretching C—N
loss (Mass variation = Initial fruit mass − Fruit mass at
1070 Vibration C—O
sampling time) was performed using an analytical bal-
ance with a precision of 0.01 g. The pH was measured in
aqueous extract with readings performed in a bench poten-
tiometer. The experiments were performed in triplicate on et al., 2015), TEM (Sriupayo et al., 2005), and AFM (Liu
three distinct occasions. Data were submitted to analysis et al., 2015).
of variance, applying the Tukey test at 5% and polynomial
regression for significant simple effects. The Excel program
(Microsoft Corporation) was used for the statistical analy- 3.1.2 XRD
sis of the data. In addition, photographs of the fruits were
recorded during storage for a better visual understanding Figure 2 presents the diffraction patterns of pure chi-
of the results. tosan (CS) samples, CSW30, CSW60, CSW90, and CSW120,
which peaks at 2θ = 9.4◦ , 19.2◦ , 20.7◦ , 23.2◦ , and 26.3◦ ,
respectively, which are related to the crystallographic
3 RESULTS AND DISCUSSION planes (020), (110), (120), (310), and (013), therefore,
in agreement with literature data and consistent with
3.1 Morphological characterizations of the structure of chitosan (Pereira et al., 2014; Wijesena
CSW et al., 2015; Zhang et al., 2015). The extraction time of
nanowhisker from chitin influenced the intensity of the
3.1.1 AFM peaks, as indicated by the increase in the peak at 2θ = 19.2◦ ,
ascribed to the crystalline plane (110). However, the peak
Figure 1 shows AFM images of CSW deposited on mica intensity at 2θ = 19.2◦ for 90 min of extraction decreases
sheets. Whiskers were acicular in shape and had wide when compared to 120 min. This occurs because, for longer
size distribution for all treatments: CSW30 (a); CSW60 (b); extraction times, the severely acidic medium not only
CSW90 (c), and CSW120 (d). These data are corroborated attacks the amorphous chains but also start destroying
by other authors that mention chitin and CSW to have a some highly crystalline whiskers, therefore causing a bal-
similar shape (Ji et al., 2017; Liu & Niyongira, 2017; Qin ance between the amorphous and the crystalline regions,
et al., 2015). which ultimately leads to a leveling-off in both peak inten-
The average lengths for nanoparticles were determined sity and crystalline fraction. The crystalline fraction of
from Figure 1, which were 510, 360, 244, and 198 nm for pure chitosan without undergoing any extraction treat-
CSW30, CSW60, CSW90, and CSW120, respectively. The ment (CS) was found to be 13% and increased to 49%, 49%,
aspect ratio showed the same tendency to decrease with 55%, and 55% for CSW30, CSW60, CSW90, and CSW120,
increasing extraction time, their average values were 203, respectively. This shows that hydrolysis predominantly
169, 129, and 95 as shown in Table 1. Table 1 also shows removes amorphous regions during the initial acid attack
the average particle size of CSW under different extrac- and for longer times a balance can be reached (De Moura
tion times, determined by DLS and AFM imaging. CSW30 et al., 2011; Pangon et al., 2016; Rubentheren et al., 2015).
sample underwent the shortest extraction time and the
largest particle size (ca. 634 nm). Thus, CSW60, CSW90,
and CSW120 suspensions presented hydrodynamic radii 3.1.3 FTIR
of 489, 336, and 311 nm, respectively, showing the same
trend observed for the aspect ratio. CSW dimensions are Table 2 shows the peaks assigned to the studied materi-
therefore in agreement with those found in the literature, als. The FTIR spectra of pure chitin (CT) and chitosan
determined by DLS (Chantarasataporn et al., 2013; Qin (CS) were slightly similar (Figure 3a), but a difference can
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ANTIFUNGAL EDIBLE COATINGS FOR FRUITS 7

This observation aligns with the trend observed in peak

intensity in XRD studies carried out by other authors (Qin
et al., 2015). Phongying et al. (2007) described that CSW
deacetylation is likely to cause a decrease or disappear-
ance of the bands associated with the amide II groups
(1560 cm−1 ).

3.1.4 Thermogravimetry

Figure 4a,b shows the TGA curves for pure chitin (CT)
and chitosan (CS) flakes. Samples started to lose weight
between 50 and 60◦ C, leading to the release of volatile
compounds and moisture. The second event with greater
mass loss, starting at approximately 250◦ C, is related to the
beginning of the CT and CS decomposition. These data are
corroborated by the literature (Pereira et al., 2014; Sriupayo
et al., 2005; Wijesena et al., 2015). TGA data for CSW30,
CSW60, CSW90, and CSW120 (Figure 4c,d) show an event
with an onset around 60◦ C, related to loss of volatile
compounds and moisture. For the different treatments,
the samples CSW30 and CSW60 showed a decomposition
peak at 358◦ C. With an increase in extraction time, the
CSW90 sample exhibited a notable shift in this peak to
388◦ C, indicating its superior thermal stability among all
the studied nanowhiskers. With a higher degradation rate
at 370◦ C, CSW90 and CSW120 showed that the loss of its
F I G U R E 3 Fourier transform infrared spectroscopy (a) of original composition did not start at the same tempera-
chitin and chitosan without treatment and (b) of chitosan ture (Pereira et al., 2015). Although Wijesena et al. (2015)
nanowhisker under different treatment times. described a higher degradation rate at 403◦ C for pure chi-
tosan and found values of 260 and 350◦ C for chitin and
CSW, respectively.
be seen in the region corresponding to the range of 3500
to 2800 cm−1 . This behavior is assigned to axial deforma-
tion of the O—H and N—H groups and indicates a smaller 3.1.5 Antifungal activity
amount of acetamide groups (Watthanaphanit et al., 2010).
The 1700 to 1500 cm−1 range is assigned amide I and Table 3 shows the percent of radial mycelial growth inhibi-
II vibrational modes. The vibrations between 3600 and tion caused by the CSW against the distinct Colletotrichum
3000 cm−1 are attributed to the elongation vibrations of strains. For C. asianum, the extraction time influenced the
the OH and NH groups involved in the molecule’s hydro- antifungal effects with a variation of mycelial growth inhi-
gen bonds. The range between 2900 and 2800 cm−1 is bition percent values decreasing from 23.9% to 19.1% with
characteristic of the symmetrical and antisymmetric elon- the concentration of 8 mg/mL and from 23.6% to 8.5% with
gation vibrations of the CH3 group. Absorption bands the concentration of 2 mg/mL. Also, the concentration did
at 1660 cm−1 related to the elongation of the C=O of not influence the antifungal activity of CSW30 sample, but
the amide group I (Chantarasataporn et al., 2013; Pereira there was a significant decrease in the inhibitory effects
et al., 2014; Qin et al., 2015; Watthanaphanit et al., when compared to other CSW samples.
2010). For C. tropicale, extraction time also influenced signifi-
CSW displayed no noticeable alterations in their struc- cantly (p < 0.05) the antifungal effects of CSW. The largest
tures post-deacetylation, except for the 1560 cm−1 peak difference stands out with values from 22.42% to 12.7% in
associated with N—H bending vibrations of amide groups the concentration of 8 mg/mL, with the smallest decrease
II. Under these conditions, most of these groups under- with 2 mg/mL, which showed values ranging from 13.0%
went conversion to amine groups, exhibiting comparable to 10.6%. There was a significant decrease (p < 0.05) in the
vibrational modes, albeit with slightly reduced intensity. antifungal effects for the different tested concentrations,
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8 ANTIFUNGAL EDIBLE COATINGS FOR FRUITS

F I G U R E 4 (a) Thermogravimetric analysis and (b) DTG of untreated chitin and chitosan. (c) TG and (d) DTG of chitosan nanowhisker
under different treatments.

except for CSW120 for which these effects ranged from distinct Colletotrichum species, it has been reported that
12.7% to 10.6%. the extraction of nanoparticles from plant and animal
The inhibitory effects of all CSW samples against C. materials can present changes in its functionality due to
gloeosporioides are influenced significantly (p > 0.05) by structural modifications, such as the loss of active amor-
the extraction time, but the greatest decrease was verified phous structures caused by such extraction treatments
with 8 mg/mL (i.e., 25.6% to 16.9%), while the inhibitory (Mahapoka et al., 2012; Pereira et al., 2015; Rubentheren
effects caused by 4 mg/mL was the most uniform among et al., 2015).
the tests. According to the concentrations used, it is veri- The activity of CSW against Colletotrichum was early
fied that in all tests there was a decrease in the antifungal reported to be around 25%, and by increasing the extraction
effects. time there is a considerable loss of this activity. There-
For C. brevisporum, it is seen that the inhibitory effects fore, CSW can exert inhibitory effects against distinct
of CSW are influenced by the extraction time (p > 0.05), Colletotrichum species capable of causing anthracnose in
as the longer the extraction time the lower the inhibition various fruits (e.g., mango, banana, and papaya) even
rate, especially for the concentration of 4 mg/mL with applying extraction treatments. Camatari et al. (2018)
values ranging from 16.4% to 4.3%. The inhibitory effects reported the efficacy of commercial chitosan to inhibit
caused by 8 mg/mL were less variable. For the concen- five distinct of Colletotrichum species (C. asianum, Col-
trations used, it was observed that, except for the CSW30 letotrichum fructicola, C. tropicale, Colletotrichum dianesei,
treatment, concentration below 6 mg/mL had reduced and Colletotrichum karstii) with mycelial growth inhibi-
antifungal effects. tion ranging from 73.2%, 30.0%, 35.8%, 37.4%, and 24%,
Considering the properties of CSW under different syn- respectively. With respect to the synergy of commercial
thesis times and concentrations to inhibit the growth of chitosan with essential oil, Oliveira et al. (2013) found
 17503841, 0, Downloaded from https://ift.onlinelibrary.wiley.com/doi/10.1111/1750-3841.16831 by Universidade Federal Da Paraiba, Wiley Online Library on [29/11/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
ANTIFUNGAL EDIBLE COATINGS FOR FRUITS 9

T A B L E 3 Percent (%) of radial mycelial growth inhibition of chitosan nanowhisker on Colletotrichum asianum, Colletotrichum tropicale
Colletotrichum gloeosporioides, and Colletotrichum brevisporum.
Concentration (g/mL) Colletotrichum asianum
CMM 4057
CSW30 CSW60 CSW90 CSW120
8 23.88 ± 1.27 Aa
23.61 ± 0.48 Aa
23.63 ± 0.90 Aa
19.09 ± 0.90Ba
6 24.16 ± 1.44Aa 23.03 ± 0.48Aa 18.61 ± 1.04Bb 15.15 ± 1.04Bb
4 22.50 ± 0.83 Aa
17.50 ± 0.83 Bb
13.63 ± 0.90 Bc
12.72 ± 1.81Bc
2 23.61 ± 0.48Aa 18.61 ± 1.27Bb 11.51 ± 0.57Bd 8.48 ± 1.04Cd
Concentration (g/mL) Colletotrichum gloeosporioides
CMM 320
CSW30 CSW60 CSW90 CSW120
8 25.55 ± 0.48 Aa
20.67 ± 1.27 Ba
18.33 ± 0.83 Ca
16.94 ± 0.96Cb
6 20.27 ± 1.27 Ab
16.38 ± 0.48 Bb
16.66 ± 0.83 Ba
20.00 ± 0.83Aa
4 21.11 ± 0.48Ab 17.22 ± 0.48Bb 17.50 ± 1.66Ba 17.50 ± 1.44Bb
2 21.66 ± 0.83 Ab
16.11 ± 0.96 Bb
11.94 ± 0.48 Cb
14.16 ± 0.83Bc
Concentration (g/mL) Colletotrichum tropicale
CMM 4071
CSW30 CSW60 CSW90 CSW120
8 22.42 ± 0.52 Aa
18.78 ± 0.90 Ba
14.24 ± 0.52 Ca
12.72 ± 2.52Ca
6 19.69 ± 1.38 Ab
12.72 ± 0.90 Bb
10.90 ± 0.90 Cb
10.00 ± 1.81Ca
4 19.69 ± 1.04Ab 9.69 ± 1.04Bc 10.90 ± 0.90Bb 10,60 ± 0.54Ba
2 13.03 ± 0.52 Ac
9.39 ± 0.52 Bc
9.09 ± 0.00 Bb
10.60 ± 0.52Ba
Concentration (g/mL) Colletotrichum brevisporum
CMM 1936
CSW30 CSW60 CSW90 CSW120
8 16.06 ± 2.28Aa 12.12 ± 0.52BCa 10.49 ± 0.53Ca 13.88 ± 1.60Ba
6 15.15 ± 0.52 Aa
10.00 ± 0.90 Bb
9.56 ± 0.53 Bb
11.11 ± 1.85Bb
4 16.36 ± 0.00Aa 9.39 ± 0.52Bb 9.87 ± 1.06Bb 4.32 ± 0.53Cd
2 14.84 ± 1.38 Aa
9.09 ± 0.00 Bb
8.33 ± 0.92 Bc
8.33 ± 0.92Bc
Notes: Results are expressed as the percentage of radial mycelial growth inhibition rates compared to the control treatment (0 mg/mL).
Means in the same column with different lowercase letters are significantly different (p < 0.05) according to Tukey’s test.
Means on the same line with different capital letters are significantly different (p < 0.05) according to Tukey’s test.

mycelial growth inhibition values of 73.2%, 30.0%, 35.8%, 3.2.1 Morphology

37.4%, and 24%, respectively, against C. asianum, Col-
letotrichum siamense, C. fructicola, C. tropicale, and C. Table 4 shows thickness values with coating sample
karstii. The antifungal activity of chitosan in its integral codes. Higher concentrations of the solution are found
form against Colletotrichum species in post-harvest of to produce a thicker and less rough coating, which are
common bean, banana, and pepper with inhibition growth corroborated by Figure 5a,b. CSW were added to the
of 70.0%, 53.3%, and 35.0%, respectively, were also verified coatings (Figure 5c,d) causing and increase in film thick-
(Silva et al., 2021). ness to 2.67 um. Thickness is an essential parameter, as
it is closely linked to the uniformity and transparency
of food coatings. Another important factor is the rough-
3.2 Zein coating with CSW ness, where the system containing CSW showed higher
roughness with a value of 1.84 µm. There is also the pos-
For this experiment, samples of CSW60 were used (concen- sibility of a better release of functional agents through
trations of 0.25%, 0.5%, and 1% w/w), since they presented the thinner films, as the diffusion pathway is shorter
the best results concerning the antifungal effects against in order to reach the desired tissue (Sidorov et al.,
Colletotrichum species. 2013).
 17503841, 0, Downloaded from https://ift.onlinelibrary.wiley.com/doi/10.1111/1750-3841.16831 by Universidade Federal Da Paraiba, Wiley Online Library on [29/11/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
10 ANTIFUNGAL EDIBLE COATINGS FOR FRUITS

TA B L E 4 Thickness and roughness of coatings by optical profilometry.

Sample coatings Thickness (µm) Roughness [Ra] (nm)
Ac4:1 1.91 ± 0.22 A
20.3 ± 0.18A
Ac3:1 1.84 ± 0.24 A
24.7 ± 0.14A
Ac2:1 2.16 ± 0.34B 13.7 ± 0.14B
CSW 2.67 ± 0.39 B
184 ± 0.22C
Note: Means in the same column with different capital letters are significantly different (p < 0.05) according to Tukey’s test.

F I G U R E 5 Surface of coatings. (a) Control coating profile; (b) Control coating roughness; (c) Composite coating profile; (d) Roughness
of the composite coating.

3.2.2 Mechanical and thermal properties of when compared to the control (zein only). CSW addition
coatings increased tensile strength and modulus of elasticity when
compared to zein films without nanowhiskers. Moura et al.
The addition of CSW to the zein coating improved the (2011) showed that the proper use of coatings for food
tensile strength of the films (Table 5), which went from mostly depends on favorable mechanical factors and that
20.78 to 38.19 MPa when adding CSW at 0.25% w/w. Also, the addition of CSW significantly improves the properties.
the elastic modulus of sample with 0.5% w/w of CSW Figure 6 shows TGA curves for the CSW60 coatings at
was found to be 589.50 MPa. The percentage of elonga- concentrations (0.25%, 0.5%, and 1%). Samples containing
tion of zein coatings under the addition of CSW showed CSW presented an onset of the first event around 150◦ C
a significant decrease when compared to the control, vary- when compared to the control without CSW due to the
ing from 53.6% to values of 36.0%, respectively. Elongation lower thermal stability of the high surface of whiskers.
at break of the coatings reinforced with CSW decreased However, thermal stability is still within the range required
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ANTIFUNGAL EDIBLE COATINGS FOR FRUITS 11

T A B L E 5 Mechanical properties of composite coatings coated (Z), and coated with chitosan nanowhisker (CSW) (Z + CSW), as a
function of nanowhisker content.
Coating type Tensile strength (MPa) Elastic modulus (MPa) Elongation at break (%)
Z 20.78 ± 1.69A 494.20 ± 2.45A 53.6 ± 1.90A
Z + CSW0.25% 38.19 ± 1.22 B
550.35 ± 2.79 B
37.7 ± 1.65B
Z + CSW0.5% 36.62 ± 1.78B 589.50 ± 3.01C 36.0 ± 1.73B
Z + CSW1% 23.33 ± 2.43 A
549.45 ± 3.12 B
38.0 ± 2.01B
Note: Means in the same column with different capital letters are significantly different (p < 0.05) according to Tukey’s test.

FIGURE 6 (a) TGA and (b) DTG of the coatings under different treatments.

for coating materials that must not degrade before to 100◦ C may have delayed the ripening aspects of the guava during
(Gorrasi & Vertuccio, 2016). There is another significant the storage period.
mass loss between 275 and 400◦ C, the active pyrolysis The pH levels of guava were noticeably affected by the
region. These results can be compared to those found in storage time in the case of uncoated guava fruits, par-
the literature (Gorrasi & Vertuccio, 2016; Park et al., 2013; ticularly after the ninth day of incubation, when the pH
Trujillo-de Santiago et al., 2014). reached a value of 3.98 from an initial 3.39. Guava samples
coated solely with zein showed relatively consistent pH
levels, ranging from 3.39 to 3.55, with no significant vari-
3.2.3 Application on guava ations observed. Similarly, guava fruits coated with zein
and CSW displayed pH values within the range of 3.39 to
The total soluble solids content, pH, and loss of weight of 3.50. This trend may be attributed to the fruit’s respiratory
the guava fruits coated and uncoated with films were mon- process during post-harvest ripening, where organic acids
itored over a period of 9 days, as shown in Table 6. These are consumed, tending to shift pH values toward neutrality,
parameters served as quality indicators assessed in relation which is generally considered undesirable.
to the applied treatments in this study. The guava fruits A decrease in fruit weight during the storage days for all
coated with Z and Z + CSW consistently maintained their evaluated fruits was also observed. However, guava fruits
values throughout the entire monitored storage period. In that underwent coating treatment with zein (Z) and zein +
contrast, the control group of uncoated fruits (U) experi- CSW (Z + CSW) showed a better ability to maintain their
enced a notable increase of two ◦ Brix points in their values. integrity. The variation in weight loss of control fruits on
Pereira et al. (2014) described that altered values for this the last day of storage was 21.54%, a significant variation
parameter can be attributed to the accumulation of sugars for the fruit to become unsuitable for human consump-
due to the natural ripening process of fruits, even if on a tion. Kader (2002) reported that the quality reference is the
small scale. Based on this quality parameter, the coatings loss of 10% of the fruit mass, so that it becomes unfit for
 17503841, 0, Downloaded from https://ift.onlinelibrary.wiley.com/doi/10.1111/1750-3841.16831 by Universidade Federal Da Paraiba, Wiley Online Library on [29/11/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
12 ANTIFUNGAL EDIBLE COATINGS FOR FRUITS

F I G U R E 7 Shelf life of guava (Psidium guajava L.) on the first (I), second (II), sixth (III), and ninth (IV) day for uncoated (U), coated (Z),
and coated chitosan nanowhisker (CSW) samples (Z + CSW) at 25◦ C. Observe that despite the color change, fruit integrity is maintained
together with the absence of surface scars.

consumption. Weight loss behavior of coated guava fruits presence of visible damage and/or deterioration in their
was different, that is, 9.49% and 8.47%, respectively, for surface area. This figure also shows the images of the fruit
samples coated only with zein, and zein + CSW, showing during its storage from the first day (I) to the last (IV).
that the treatments were effective throughout the storage, It is important to highlight the difference in the appear-
which according to this quality parameter, the guava is ance of the fruits during storage. After the third day (II), it
classified as suitable for consumption even after 9 days at becomes visible that the control fruits (left) had rot signs on
room temperature. their surfaces that could be linked to undesirable microbial
Fruit integrity is an important factor in its market value growth, since these same characteristics were accentuated
and consumer preference. Figure 7 shows the evolution on the sixth day (III). On the ninth day of storage, the
of uncoated (U), coated (Z), and CSW (Z + CSW) coated control fruits had signs of contamination and accentuated
guava fruits. The evaluation was carried out to determine degradation, which is not seen in coated samples and in
the time required for the fruit to be discarded due to the samples treated with CSW. The importance of applying the
 17503841, 0, Downloaded from https://ift.onlinelibrary.wiley.com/doi/10.1111/1750-3841.16831 by Universidade Federal Da Paraiba, Wiley Online Library on [29/11/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
ANTIFUNGAL EDIBLE COATINGS FOR FRUITS 13

T A B L E 6 Values of total soluble solids in ◦ Brix of guava fruits during 9 days of storage uncoated (U), coated (Z), and coated with
chitosan nanowhisker (CSW) (Z + CSW).
Sample Total soluble solids (◦ BRIX)
0 3 6 9
Aa Aa Aa
U 11 11 11 13Bb
Aa Aa Aa
Z 11 11 11 11Aa
Z + CSW 11Aa 11Aa 11Aa 11Aa
Sample pH
0 3 6 9
U 3.39 ± 0.04 Aa
3.41 ± 0.03 Aa
3.45 ± 0.05 Aa
3.98 ± 0.09Bb
Z 3.39 ± 0.04 Aa
3.43 ± 0.06 Aa
3.44 ± 0.03 Aa
3.55 ± 0.11Aa
Z + CSW 3.39 ± 0.03Aa 3.44 ± 0.04Aa 3.46 ± 0.03Aa 3.50 ± 0.10Aa
Sample Weight loss (%)
0 3 6 9
U 0 .0 4.00 11.07 21.54
Z 0.0 3.78 6.82 9.49
Z + CSW 0.0 3.57 6.45 8.47
Note: Means followed by the same capital letter in the row do not differ statistically from each other by the F test at 5% and means followed by the same lowercase
letter in the column do not differ statistically from each other by the Scott–Knott test at 5% (means followed by the same capital letter in line do not differ
significantly, according to F test [p < 0.05] and means followed by the same tiny letter in the column do not differ significantly, according to Scott–Knott’s test
[p < 0.05]).

coating is fundamental for the quality control of this fruit, tion. Juliano E. Oliveira: Supervision; conceptualiza-
as the treatment with CSW (Z + CSW) on the last eval- tion; writing—review and editing; project administration.
uated day was efficacy to keep the fruit surface integrity Eliton S. Medeiros: Supervision; writing—review and
characteristics. editing; conceptualization; methodology; project adminis-
tration.

4 CONCLUSIONS AC K N OW L E D G M E N T S
The authors are grateful to the Scientific and Techno-
CSW were successfully obtained and later incorporated logical Development National Research Council (CNPq,
into zein to form antifungal coatings to increase fruit shelf grant nos. 306.447/2018-5, 305880/2021-7, 405.802/2022-6,
life. CSW60 showed the greatest antifungal effects against 406.973/2022-9, and 305.065/2022-0), Coordination for the
C. asianum, C. fructicola, C. tropicale, C. dianesei and C. Improvement of Higher Education Personnel (CAPES),
karstii, in addition to presenting the best morphological and the Minas Gerais state funding agency (FAPEMIG,
characteristics. Furthermore, addition of CSW did not sig- grant nos. APQ-00153-23 and BPD-00406-22) for funding
nificantly (p < 0.05) modify the coating surface, preserving this research.
its homogeneity and continuity after coating guava fruits.
In turn, the protective coating prevented microbial growth C O N F L I C T O F I N T E R E S T S TAT E M E N T
and maintained the parameters indicative of fruit quality The authors declare no conflicts of interest.
during storage.
ORCID
AU T H O R CO N T R I B U T I O N S Carolina L. Almeida https://orcid.org/0009-0009-4383-
Carolina L. Almeida: Writing—review and editing; 9643
formal analysis; resources; investigation; data curation. Evandro L. Souza https://orcid.org/0000-0003-4927-
Lucas R. F. Figueiredo: Supervision; investigation; 9383
writing—review and editing; data curation. Diego V. M.
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