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Postharvest Biology and Technology 101 (2015) 1014

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Postharvest Biology and Technology


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

Preservation of mango quality by using functional chitosanlactoperoxidase systems coatings


Mohamed Ciss a,b, *, Jessica Polidori a , Didier Montet a , Grard Loiseau a ,
Marie Nolle Ducamp-Collin a
a
b

CIRAD, UMR Qualisud, 73 rue Jean Franois Breton, 34398 Montpellier Cedex 5, France
University Peleforo Gon Coulibaly Korhogo, Cote dIvoire

A R T I C L E I N F O

A B S T R A C T

Article history:
Received 20 June 2014
Received in revised form 25 October 2014
Accepted 3 November 2014

Inuence of chitosan coating with or without the active antimicrobial lactoperoxidase system was
studied on postharvest mangoes. Mangoes were treated with three concentrations of chitosan (0.5; 1;
1.5%) containing or not lactoperoxidase with or without iodine as a second electron donor. Coatings
containing 1 and 1.5% chitosan incorporated with lactoperoxidase system efciently inhibited fungal
proliferation and delayed mango ripening. Iodine did not inuence antifungal activity. Ripening
parameters (rmness, respiration, weight loss and color) were not inuenced by the lactoperoxidase
system, but were more inuenced by chitosan concentration. Chitosan coating alone reduced weight loss,
and delayed the decline in rmness and respiration rate. It exhibited a benecial effect on the contents of
total soluble solids (TSS), ascorbic acid, total acidity (TA) and pH.
2014 Elsevier B.V. All rights reserved.

Keywords:
Chitosan
Lactoperoxidase system
Edible coatings
Mango

1. Introduction
Developing countries experience signicant postharvest losses
of fruit and vegetables, and among these agricultural products,
mango is a dominant tropical fruit variety (FAO, 2003). However,
mangoes face problems in storage due to various diseases caused
by fungi and bacteria. The control of these diseases has become
difcult because of strain resistance to fungicides and increasingly
rigorous regulations. These regulations on the use of fungicide
have reduced the ability to develop control strategies based on
chemicals (Johnson and Sangchote, 1994). An alternative to this
problem could be the use of natural compounds that have a broad
antimicrobial spectrum.
The lactoperoxidase system (LPOS) has been described as an
excellent system for ghting pathogenic microorganisms as it has
a broad antimicrobial spectrum. This enzyme system has shown a
bactericidal effect on Gram-negative bacteria and a bacteriostatic
effect on Gram-positive bacteria (Seacheol et al., 2005). In
addition, it has antifungal (Jacob et al., 2000) and antiviral activity
(Pakkanen and Aalto, 1997; Seifu et al., 2005). This system
generates intermediate antimicrobial products such as

* Corresponding author at: BP 1328 Korhogo, Cote dIvoire.


Tel.: +33 4 67615498/225 07082215; fax: +33 4 67615515.
E-mail address: cismorad@yahoo.fr (M. Ciss).
http://dx.doi.org/10.1016/j.postharvbio.2014.11.003
0925-5214/ 2014 Elsevier B.V. All rights reserved.

hypothiocyanite (OSCN ) and hypothiocyanate acid (HOSCN).


These highly reactive products inhibit microorganisms by
oxidation of the sulfhydryl groups of microbial enzymes
(Martnez-Camacho et al., 2010). Presence of iodine in addition
to thiocyanate increases the fungicidal and bactericidal effect
against microbes such as Candida albicans,Escherichia coli and
Staphylococcus aureus (Bosch et al., 2000). LPOS incorporated into
matrix polymers by immobilization, absorption, or trapping has
been operating in the pharmaceutical and food areas. The
effectiveness of incorporation of the LPOS into whey proteins
(Min et al., 2005; Min and Krochta, 2005) and alginate lms (Fatih
et al., 2009) has been demonstrated. Chitosan has multiple
biological and chemical properties. Amino and hydroxyl groups of
the linear polyglucosamine chain are very reactive, and consequently it is amenable to chemical modication. Dissolved in an
acid solution, chitosan has a high positive charge on NH3+ groups
which can form an aggregate with polyanions. This characteristic
provides excellent ionic properties to chitosan gels which give
them remarkable afnity to proteins. In addition, chitosan has
antimicrobial properties and can protect fruit against fungal
deterioration (Atia et al., 2005; Photchanachai et al., 2006).
Chitosan could be used to stabilize LPOS antimicrobial activity for
a long time, and it may also delay the ripening of fruit.
The objective of this study, therefore was to enhance the
effectiveness of LPOS linked to chitosan and thereby extend the
postharvest preservation of mangoes.

M. Ciss et al. / Postharvest Biology and Technology 101 (2015) 1014

2. Materials and methods


Experiments were performed on mangoes (Mangifera indica L.
cv. Kent) imported from Brazil, and purchased in a local
supermarket in Montpellier France. Selected mature green fruit
were uniform in size (591  30 g), with good quality and were free
from injury or disease.
LPOS was composed of lactoperoxidase (LPO; 140 U/mg,
Bioserae, France), glucose oxidase (GO; 158.9 U/mg, Sigma
Aldrich); D (+) glucose (Glu SigmaAldrich), potassium thiocyanate
(KSCN, Bioserae, France), with or without potassium iodide
(KI, Fluka). Chitosan (>90% DDA viscosity 5002000 cps) was
obtained from France Chitin (Marseille, France). Glycerol, used as a
plasticizer to improve coating exibility, was purchased from
Fisher Scientic Inc. (Fair Lawn, NJ). Strains of Colletotrichum
gloeosporioides, Phomopsis sp. RP257, Pestalotiopsis sp. and
Lasiodiplodia Theobromae ngr 05 A were isolated and identied
by CIRAD (Montpellier-France).
2.1. Preparation of solution of LPOS
The weight ratios of the LPOS components were 0.35, 1.00, 1.09,
2.17 and 108.70 respectively for LPO, GO, Glu KSCN, and KI.
The composition was adapted from Min and Krochta (2005). The
components were dissolved separately in 50 mL phosphate buffer
(pH 6.2) and 15.5 mg of LPO was added. LPOS solution was
incubated at 23  2  C for 24 h with shaking at 160 RPM using a
water bath shaker (Julabo SW 20 Silab, France) to increase the
antimicrobial activity of LPOS (Bosch et al., 2000; Min et al., 2007).
Two solutions of the enzyme system were prepared, one with
iodine (LPOSI) and one without (LPOS).

instrument, Italy) for oxygen and GC 1000, Dani, Italy, for carbon
dioxide). The respiratory rate was expressed in mmol kg 1 h 1 in
normal conditions of temperature and pressure.
2.5. Evaluation of the quality of mangoes
Weight loss was determined by daily weighing mangoes with a
balance (Precisa, Switzerland). Weight loss was expressed as a
percentage of initial weight.
Firmness was determined using a TA XT2 texture analyzer
(Instron Co., USA), calibrated at 5 kg and equipped with a 2 mm
diameter probe. Initial grip separation was 30 mm with a stroke
speed of 1 mm/s.
The color of the fruit skin was measured using a Minolta
chromameter (Chroma meter CR 400, Japan). Three determinations were performed on different sides of each fruit and the
average represented the color value. The results were determined
in the color space L*, a* and b*.
Total soluble solids (TSS) concentration were measured with a
digital refractometer Atago PR-101 (Atago Co., Ltd., Tokyo, Japan) at
20  C and expressed as % of dry matter.
Thirty (30) grams of mango pulp were homogenized in 150 mL
of distilled water using a blender for 2 min and then ltered. The
pH was determined with a pH meter (Kyle, USA). Total acidity (TA)
was determined on 10 mL of homogenate pulp by automatic
titration with 0.1 N NaOH up to pH 8.1. The results were expressed
as g citric acid equivalent per 100 g fresh weight. Ascorbic acid
content was determined by colorimetry using 2,6-dichlorophenolindorhenol titration (AOAC, 1984).
2.6. Statistical analysis

2.2. Preparation of chitosan lm-forming solutions

Experimental data were subjected to ANOVA analysis using


Statistica 7. The overall least signicant differences (Student's
procedure, p < 0.05) were calculated and used to detect signicant
differences among treatments. Each trial contained three
replicates of 126 fruit.

Chitosan solutions were prepared by dissolving chitosan akes


(0.5, 1 and 1.5 g) in distilled water (80 mL) containing 0.7 mL of
lactic acid (Sigma) under agitation using a magnetic stirrer,
incubated over night at room temperature (22  C). The pH of the
solution was adjusted to 5.5 with 0.46 M K2HPO4 (SigmaAldrich)
and the solution was made up to 100 mL with distilled water.
Glycerol (25% p/p of chitosan) was added and the solution was
stirred at ambient temperature for 30 min.

3. Results and discussion


3.1. Antifungal activity of different coatings
Uncoated mangoes contaminated with Phomopsis RP257
showed signs of fungal decay (>1 cm) after seven days of storage
whereas those treated with Colletotrichum gloeosporiodes strains
and L. diplodia showed signs of fungal decay after fourteen days.

2.3. Antimicrobial tests


Fruit were sterilized by washing with chlorinated water (1%)
and rinsing with distilled water. Identical lesions (diameter 1 mm
and depth 3 mm) were performed on the two opposite sides of the
fruit with sterile nails. Fruit were then inoculated individually by
immersion for 1 min in the microbial solution (105 spore/mL of
selected mould) and left overnight at room temperature. They
were dipped into the coating solution and then stored at 18  C and
60% RH. Percentages of inhibition of microorganisms by the
different coatings were calculated by comparing with the control
(uncoated mango), when the diameter of the lesions of the latter
exceeded 1 cm. Percentages of inhibition (%) = 1 (DS/DC)  100,
where DS is the diameter of the lesion zone in the coated mango
and DC is the diameter of lesion in the control (uncoated mango)
(Martnez-Camacho et al., 2010).

11

[(Fig._1)TD$IG]

2.4. Respiration rate


Respiratory rate (RR) was determined by individually placing
each fruit in a 3 L glass jar hermetically closed for 3 h. Then 0.5 mL
of gas was withdrawn with a syringe and analyzed to determine
the % of CO2 and O2 by gas chromatography (GC 800, CE

Fig. 1. Antifungal activity of different coatings against pathogenic strains on Kent


mango fruit. Coatings are dened in Section 2.

12

M. Ciss et al. / Postharvest Biology and Technology 101 (2015) 1014

The rapid ability of Phomopsis to infect mangoes indicated that it


was the most virulent of the strains tested.
Fig. 1 shows different sensitivities of strains to different
coatings applied on the mangoes. The concentration of chitosan
in the coating solution and the presence of the enzyme system
affected the fungal decay of the fruit. The percentage of strain
inhibition was improved with the increase of chitosan concentration, and it became higher when the LPOS system was added. The
inhibitory action of chitosan alone has already been demonstrated
in several studies. These studies reported that the antifungal effect
of chitosan was dependent on concentration (El Ghaouth et al.,
1992; Jiang and Li, 2001; Liu et al., 2007). Chitosan with its positive
charges interacts with negatively charged membranes of the cell to
alter cell permeability.
In all the cases, the inhibition by the coatings was improved by
the LPOS. Some strains that showed a resistance to chitosan
became more sensitive to LPOS. Phomopsis was inhibited 58% by
chitosan, 1% alone and in the presence of LPOS, the inhibition
reached about 100%. These results showed that there was a
synergistic effect of chitosan and LPOS.
Inhibitory effects increased with the incorporation of LPOS or
LPOSI in chitosan at 1 or 1.5%. The synergistic effect between the
LPOS with chitosan against C. gloeosporioides strains and L. diplodia
has already been demonstrated by Ciss et al. (2013). They revealed
that this combination was more effective with chitosan at 1 and
1.5%.
No signicant difference was observed during comparison of
the effects of inhibition of LPOS with and without iodine (LPOS and
LPOSI) at the same concentration of chitosan. Presence of iodine in
the enzyme system (LPOSI) did not inuence signicantly the
antifungal activity of LPOS. This result conrmed those found by
Ciss et al. (2013) on mango phytopathogenic strains in vitro.
Effectiveness of the presence of iodine in LPOS has also been
studied also by Bosch et al. (2000) who reported that addition of
iodine with thiocyanate increased the fungicidal and bactericidal
effect against C. albicans, E. coli and S. aureus while Pseudomonas
aeruginosa showed the same inhibition from the lactoperoxidase
system with or without iodide.
3.2. Respiration rate
Table 1 shows O2 consumption and CO2 produced from
uncoated and coated mangoes with 1 and 1.5% of chitosan
incorporated with LPOS or LPOSI. Signicant differences (p < 0.05)
were found with the lowest O2 consumption and highest CO2
production observed for coating mangoes. These results indicated
on the whole that chitosan coating reduced the respiration rate of
mangoes by decreasing O2 and increasing CO2.
Regarding the O2 consumption, there was no signicant
difference between mangoes treated with chitosan at 1% and

1.5%. The presence of the enzyme system (LPOS or LPOSI) did not
affect O2 consumption. These results conrmed these obtained by
Ciss et al. (2012), who demonstrated that the diffusion of O2 could
be reduced by a chitosan lm. The addition of the LPOS with or
without iodine did not alter the permeability of the lm. Other
work has also highlighted the reduction of O2 permeability in
coated fruit by chitosan lms; Thumula (2006) showed that
chitosan could reduce the oxygen consumption of tomatoes.
Concerning CO2 production, there was no signicant difference
observed between coated and uncoated mangoes after two days,
with production from coated mangoes increasing sharply to the
sixth day. The increase in CO2 production of coated fruit may be a
stress response due to the treatment (El Ghaouth et al., 1992). The
strong CO2 production caused by chitosan coatings has been
demonstrated by other authors (El Ghaouth et al., 1992; Thumula,
2006). No signicant difference in CO2 production was observed
between mangoes treated with two concentrations of chitosan
(1% and 1.5%) combined or not with LPOS or LPOSI.
These different behaviors of chitosan coating on O2 consumption and CO2 production of different mangoes showed that
chitosan coating was more selective to CO2 than to O2 permeability.
Edible coatings increase CO2 production and reduce O2 consumption in the coated fruit by lowering respiration rates and
deterioration indexes. This action contributes to extending
the preservation of fruit (Hagenmaier, 2005). High levels of CO2
in the fruit restrict succinic dehydrogenase activity and induce
accumulation of succinic acid, which leads nally to the inhibition
of the Krebs cycle (Deng et al., 2006). Also, the low level of oxygen
suppresses the activity of cytochrome oxidase and plays a role in
the inhibition of the activity of oxidases such as ascorbic acid
oxidase, polyphenol oxidase, and glycolic acid oxidase (zden and
Bayindirli, 2002). Obviously, edible coatings contribute to the
reduction of vital activities, enhancing quality maintenance of fruit
during storage. Thumula (2006) showed also that a coating made
of 1 or 2% chitosan could delay the ripening of tomatoes.
3.3. Weight loss of fruit during storage
Table 2 shows weight loss during storage of uncoated mangoes
compared to coated fruit. All samples underwent a gradual loss of
weight during storage. Loss of weight of uncoated fruit was
signicantly greater than that of coated fruit after 5 days. At the
end of storage, untreated mangoes showed 2.8% loss in weight,
whereas the weight losses of coated samples were around 1.5%.
These results highlight a protective action of coating against
moisture loss, which has also been reported by several authors
(Ali et al., 2011 Vsconez et al., 2009). The reduction in water loss
can be attributed to an additional barrier against diffusion through
the stomata (Paull et al., 1989). As can be observed in Table 2,
incorporation of LPOS with and without iodine into the

Table 1
Respiration rate (RR) of Kent mangoes.
2 days
RR (mmol kg

Uncoated
1% Chit
1% ChitLPOS
1.5% ChitLPOS
1% ChitLPOSI
1.5% ChitLPOSI
1.5% Chit

4 days
1

RR (mmol kg

6 days
1

RR (mmol kg

O2

CO2

O2

CO2

O2

CO2

0.19a  0.04
0.15ab  0.02
0.10b  0.03
0.09b  0.01
0.07b  0.00
0.08b  0.03
0.12ab  0.04

0.41a 0.06
0.48ab  0.05
0.52b  0.06
0.43a 0.06
0.53b  0.02
0.44a 0.05
0.45ab  0.09

0.18a  0.03
0.11ab  0.03
0.08 b  0.02
0.07b  0.01
0.08b  0.00
0.09b 0.03
0.09b  0.02

0.37a 0.03
0.49b  0.12
0.50b  0.06
0.51b  0.09
0.47b 0.06
0.42 b  0.09
0.49b  0.11

0.12a  0.02
0.07b  0.01
0.07b  0.01
0.05b  0.00
0.04b  0.00
0.08b  0.01
0.05b  0.01

0.44a 0.09
0.65b  0.21
0.64b 0.34
0.47ab  0.04
0.47ab  0.07
0.48ab  0.16
0.58ab  0.19

Means are averaged values of three trials. Each trial contained three replicates per treatment. Values within a column with the same letter are not signicantly different
(p > 0.05).

M. Ciss et al. / Postharvest Biology and Technology 101 (2015) 1014

13

Table 2
Effect of coating on the weight loss of Kent mango.
Days
Coating
composition

Uncoated
1% Chit
1.5% Chit
1% ChitLPOS
1.5% ChitLPOS
1% ChitLPOSI
1.5% ChitLPOSI

0.65a  0.01
0.54a  0.08
0.65a  0.06
0.62a  0.06
0.61a  0.07
0.55a  0.01
0.60a  0.000

0.66a  0.06
0.57a  0.01
0.49a  0.04
0.58a  0.18
0.64a  0.10
0.51a  0.03
0.56a  0.11

0.77a  0.09
0.73a  0.01
0.79a  0.06
0.72a  0.06
0.77a  0.03
0.64a  0.07
0.63a  0.31

0.98a  0.07
0.77b  0.15
0.79b  0.09
0.81b  0.04
0.69b  0.06
0.72b  0.08
0.65b  0.35

1.20a  0.06
0.89b  0.08
0.85b  0.10
0.90b  0.05
0.80b  0.06
0.74b  0.02
0.79b  0.44

1.74a  0.02
1.30b  0.03
1.21b  0.07
1.36b  0.03
1.10b  0.10
1.24b  0.04
1.15b  0.56

2.54a  0.12
2.06ab  0.06
1.91b  0.08
1.78b  0.10
1.81b  0.04
1.59b  0.07
1.58b  0.51

Means are averaged values of three trials. Each trial contained three replicates per treatment. Values within a column with the same letter are not signicantly different
(p > 0.05).

lm-forming solution did not have any signicant effect on weight


loss reduction. Thumula (2006) showed also that the presence of
lysozyme in chitosan coatings did not inuence the loss of weight
of tomatoes.

[(Fig._3)TD$IG]

3.4. Changes in color


Color of mango skins is an important selection criterion for
buyers. It can give an indication of the state of fruit ripening. As
shown in Fig 2, noticeable changes in the skin color occurred
during storage. Uncoated mangoes lost their green color (a* > 0)
unlike coated fruit that maintained this color (a* < 0). Chitosan
concentration at 1.5% seemed the best to maintain green color.
The presence of LPOS did not inuence color change, and thus the
action of the coating in slowing ripening was correlated with
the concentration of chitosan and was not dependent on the
presence of the LPOS.
3.5. Firmness
Mango is a soft fruit that suffers a rapid loss of rmness during
ripening which contributes greatly to its short postharvest life.
Fig. 3 shows the changes in esh rmness of control and treated
fruit after eight days of storage. Initial esh rmness decreased for
all treatments, however chitosan coatings retained more initial
esh rmness of fruit in contrast to uncoated fruit. An overall
comparison showed that there was no signicant difference
between chitosan at 1% or 1.5%. This same result was observed with
the use of chitosan incorporating LPOS or LPOSI. LPOS with or
without iodine did not inuence chitosan protection against
rmness lost. These results indicate that fruit rmness is preserved
by chitosan coating and not by the presence of the enzyme system.
Reduction of respiration and water loss could be responsible for the
retention of rmness. Using a suitable coating could maintain that
strength (Tasdelen and Bayindirli, 1998).

[(Fig._2)TD$IG]

Fig. 2. Color properties of Kent mangoes treated with different coating


formulations. Coatings are dened in Section 2.

Fig. 3. Firmness changes in Kent mangoes treated with different coating


formulations. Coatings are dened in Section 2.

3.6. Chemical composition change in fruit


The chemical composition of the fruit pulp is an important
criteria needed for the evaluation of fruit quality. Normally,
biochemical changes of mangoes during ripening include a
reduction of titratable acidity (TA) and increase of pH, ascorbic
acid, and total soluble solids (TSS). The changes in the chemical
composition of mangoes after eight days of storage were studied
(Table 3). Titratable acidity decreased in all the mangoes, both
treated and untreated, and uncoated mangoes had the maximum
fall in acidity. pH increased from the initial value of 3.61 in the
uncoated mangoes (4.88). There was not a signicantly different
change observed between control and coated fruit.
During ripening, TSS increased due to the degradation of
polysaccharides present in the fruit. In this study, there was no
signicant difference between values of coated and uncoated
mangoes and reference values. However uncoated fruit showed a
maximum value of 14.8% TSS after eight days of storage. Initially,
fruit are rich in ascorbic acid but its level usually decreases during
maturation. After eight days of storage, ascorbic acid in uncoated
fruit fell signicantly (5.84 mg/100 mL) compared to coated fruit
(2326 mg/100 mL) (Table 3). Slowing maturation caused by the
coating of chitosan, thus reduced degradation of ascorbic acid.
An overall comparison between chitosan treatments showed
that there was no signicant difference between chitosan
concentrations of 1% and 1.5%. Application of chitosan exhibited
a benecial effect on the contents of TA, TSS, pH and ascorbic acid.
This could be due to low respiration of coated fruit. The presence of
the enzyme system did not inuence chemical composition
changes in the fruit.

14

M. Ciss et al. / Postharvest Biology and Technology 101 (2015) 1014

Table 3
Chemical composition of Kent mangoes.

Reference
Uncoated
1% Chit
1% ChitLPOS
1% ChitLPOSI
1,5% Chit
1.5% ChitLPOS
1.5% ChitLPOSI

pH

Titrable acidity (g/citric acid/100 g of pulp)

T.S.S (%)

ascorbic acid (mg/100 ml)

3.61b  0.11
4.88a  00
4.195b  0.12
4.18b  0.49
3.83b  0.20
4.07b  0.04
3.82b  0.02
4.06b  0.01

1.35a  0.03
0.29b 0.02
0.58c 0.03
0.69cd 0.05
0.76cd 0.13
0.8 d 0.01
0.80d 0.23
0.68cd 0.09

12.56a  0.07
14.875a  0.03
14.65a 0.07
13.425a  0.1
13a  1.13
13,65a  0.78
12.55a  0.35
12.8a  0.42

29.36a 0.35
5.84b  0.14
25.48c  5.2
23.04c  2.6
23.64c  2.09
23.54c  0.5
25.94c  3.45
24.80c  4.56

Means are averaged values of three trials. Each trial contained three replicates per treatment. Values within a column with the same letter are not signicantly different
(p > 0.05). Reference is value before storage.

4. Conclusion
This study demonstrated the effectiveness of chitosan coating
containing LPOS in postharvest conservation of mangoes. Chitosan
has antimicrobial activity which was been strengthened by the
LPOS. A chitosan concentration at 1% containing LPOS was
sufciently effective against microbial contamination and enabled
a delay in fruit ripening without altering quality. If chitosan coating
had an effect on the physico-chemical properties, the presence of
the LPOS did not affect those parameters. Use of chitosanLPOS
could thus be an effective approach in the preservation of tropical
fruit, an alternative in limiting synthetic pesticide use.
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