Food Packaging and Shelf Life xxx (xxxx) xxxxxx

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Food Packaging and Shelf Life

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

Postharvest treatments to control physiological and pathological disorders

in lemon fruit

Gins B. Martnez-Hernndeza,b, Francisco Arts-Hernndeza,b, , Perla A. Gmezb, Jorge Bretc,
Benito Orihuel-Iranzoc, Francisco Artsa,b
a
Postharvest and Refrigeration Group, Department of Food Engineering, Universidad Politcnica de Cartagena, Paseo Alfonso XIII, 48, 30203, Cartagena, Murcia, Spain1
b
Institute of Plant Biotechnology, Universidad Politcnica de Cartagena, Campus Muralla del Mar, 30202, Cartagena, Murcia, Spain
c
PRODUCTOS CITROSOL S.A., Partida Alameda Parc. C., 46721, Potres, Valencia, Spain

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

Keywords: Physiological and pathological disorders of lemons (Citrus limon (L.) Osbeck) are the main causes of quality losses
Calcium salts during shelf life leading to high economic losses. This experiment studied the eect of innovative postharvest
2-phenylphenol chemical treatments [Fortisol Ca (1%; FoCa), Fortisol CaPlus (1.5%; FoCaPlus), Philabuster (0.2%; PHI) and
Imazalil Ortocil (1%; ORT)], and their combinations, by immersion (30 s), to control decay, chilling injury and red blotch
Pyrimethanil
in lemon fruit. The inuence of a preharvest application of Fortisol Ca (1%) over the trees was also studied.
Chilling injury
Red blotch
Lemons washed with tap water were used as control fruit (CTRL). Lemons were stored for 33 d at 7 C, which
simulated a long storage and transportation period, followed by 5 d at 22 C of retail sale period, simulating then
a prolonged shelf life. The PHI + ORT treatment completely avoided pathological disorders after both shelf life
periods. FoCa and FoCaPlus reduced chilling injury and red blotch. The incidence of such physiological disorders
was even highly reduced when combined FoCa and FoCaPlus with PHI + ORT treatments were used. In parti-
cular, the combination of PHI + ORT + FoCaPlus completely avoided the incidence of chilling injury and red
blotch. In conclusion, a combined postharvest treatment of PHI + ORT with FoCa/FoCaPlus highly reduced, or
even avoided, physiological disorders (chilling injury and red blotch), minimizing mass losses, in lemon fruit
during long storage and transportation, and retail sale periods extending its shelf life.

1. Introduction
Lemon fruit (Citrus limon (L.) Osbeck) is a fruit consumed worldwide
mostly like a food condiment or ingredient in fruit juices. The external
appearance of lemons is crucial in the fresh market at the time of the
consumer choice. Accordingly, the wasted lemons due to low visual
quality and/or pathological disorders (mainly Penicillium spp.) is esti-
mated to be approximately of 20%. Therefore, the use of postharvest
techniques that preserve the quality of lemons during their postharvest
life is of high interest (Martnez-Hernndez, Arts-Hernndez,
Gmez, & Arts, 2015). The postharvest treatments applied on lemon
can be chemical (calcium and aluminium salts, imazalil, tiabendazole,
2-phenylphenol, natural waxes, phytoalexins, essential oils, etc.), phy-
sical (temperature management, relative humidity, controlled and
modied atmospheres, ozone, heat pretreatments or curing, UV-C ra-
diation, etc.), biological (yeasts, moulds and/or bacteria) or combina-
tions of them (Arts, 1995, 2000; Arts-Hernndez & Arts, 2008; Ben-
Yehoshua et al., 2000; Martnez-Jvega, 2004; Parra, Ripoll, & Orihuel-
Iranzo, 2014). The application of preharvest treatments is also inter-
esting in order to reduce disorders emerged during postharvest life.
Chilling injury and red blotch are physiological disorders of lemons,
which may lead to important economic losses due to low visual quality
of commercialized lemons. Lemon fruit is very sensitive to storage
temperature below 12 C appearing chilling injury symptoms (Arts,
Guilln, & Escriche, 1981; Guilln-Mir, 1978). Such symptoms are
aggravated when fruits are taken out from the refrigerated storage
during retail sale period. The chilling injury is characterized by loca-
lized discoloration of the peel followed by the collapse of the aected
area, which results in depressions on the fruit surface (Arts et al.,
1981; Cohen, Shapiro, Shalom, & Klein, 1994). The primary responses
to chilling injury are thought to be alterations of cell membrane
structures and stability, together with changes in lipid and fatty acids
composition and characteristics (Lado, Rodrigo, Lpez-Climent, Gmez-
Cadenas, & Zacaras, 2016; Sevillano, Sanchez-Ballesta,

Corresponding author at: Postharvest and Refrigeration Group, Department of Food Engineering, Universidad Politcnica de Cartagena, Paseo Alfonso XIII, 48, 30203, Cartagena,
Murcia, Spain.
E-mail address: fr.artes-hdez@upct.es (F. Arts-Hernndez).
1
Web site: www.upct.es/gpostref.

http://dx.doi.org/10.1016/j.fpsl.2017.08.009
Received 13 February 2017; Received in revised form 5 June 2017; Accepted 8 August 2017
2214-2894/ 2017 Elsevier Ltd. All rights reserved.

Please cite this article as: Martnez-Hernndez, G.B., Food Packaging and Shelf Life (2017), http://dx.doi.org/10.1016/j.fpsl.2017.08.009
G.B. Martnez-Hernndez et al.
Romojaro, & Flores, 2009; Wismer, Worthing, Yada, & Marangoni,
1998). Secondary responses to chilling injury have been associated with
oxidative stress in citrus fruit (Lafuente, Sala, & Zacarias, 2004;
Sala & Lafuente, 1999; Sala, 1998).
Red blotch, or adustiosis, is a postharvest physiological disorder
characterized by brown-red stains, which may cover 70% of the lemon
fruit surface in advanced stages. There is no damage to the glandule or
epithelium at initial stages of adustiosis. However, when this physio-
logical disorder is aggravated the cell collapses and necrotizes, moving
later into the albedo tissues. The cause of the red blotch incidence in
lemons is not well known although it is thought to be a result of some
products from fruit respiration such as the alkyl-esters because similar
symptoms have been observed in vitro after application of several esters
such as ethyl-acetate (; Guilln-Mir, 1978).
The main pathological disorder in lemons is caused by Penicillium
spp. The citrus industry usually applies chemical fungicides to reduce
such incidence while other alternative postharvest treatments, as pre-
viously mentioned, are under study.
The objective of this work was to investigate the eects of several
chemical postharvest treatments (calcium salts and fungicides) and
their combinations over the incidence of physiological (chilling injury
and red blotch) and pathological (Penicillium spp.) disorders during
storage and transportation periods at chilling temperature followed by
a retail shelf life period at room temperature. The eect of a preharvest
treatment with calcium salts over the eciency of the above-en-
umerated postharvest treatments was also studied.
2. Material and methods
2.1. Chemical compounds
The chemical compounds used in this study were supplied by
PRODUCTOS CITROSOL S.A. (Valencia, Spain). Such compounds were
Fortisol Ca (35.5% of a mix of water-soluble salts of calcium (CaO),
potassium (K2O) and phosphorous (P2O5)), Fortisol Ca Plus (29.3% of a
mix of water-soluble salts of calcium (CaO), sodium (Na2O) and phos-
phorous (P2O5)), Philabuster 400 SC (PHI; Imazalil 20% w/v + pyr-
imethanil 20% w/v) and Ortocil (ORT; 2-phenylphenol 10% w/v).
2.2. Plant material, preharvest treatments and harvest
The plant material used was lemon (C. limon) cv. Fino over Citrus
macrophylla rootstock from Alhama de Murcia (Spain). Soil, irrigation
water and tree leaves analyses were done by an external laboratory
(Fitosoil S.L., Murcia, Spain) (data not shown). Lemon trees were drip
irrigated and pruned according to Good Agricultural Practices protocols
of the company Frugarva S.A. (Murcia, Spain).
A preharvest treatment with Fortisol Ca (hereinafter F) was con-
ducted on September 2014. Accordingly, Fortisol Ca was diluted in a
tank of 1000 L of water to obtain a nal concentration of 1% v/v.
Subsequently, lemon trees were aspersed with the treatment using
pressure guns until the tree leaves were completely wet. Untreated trees
were used as control treatment (hereinafter C). Three eld replicates
per treatment were used representing three trees each replicate. The
two preharvest treatments were separated leaving one tree line without
treatments between them.
Fruits were manually harvested on February 2015 around 10:00 am
in order to avoid dew and high ambient temperatures. Fruits were
harvested homogenously from all the tree volume. Fruits were placed in
PVC boxes (40 30 25 cm) and then transported by car to the pilot
plant of the Postharvest and Refrigeration Group where postharvest
treatments were immediately applied.
2.3. Postharvest treatments
The harvested lemons were packaged in perforated PVC plastic nets
2
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prior to postharvest treatments. Three replicates were prepared for
every postharvest treatment being every replicate composed by 30
fruits. Postharvest treatments were applied by immersion of lemon nets
in a 100L-tank for 30 s. The postharvest treatments were:
CTRL: tap water
FoCa: Fortisol Ca 1% v/v
FoCaPlus: Fortisol Ca Plus 1.5% v/v
PHI + ORT: 0.2% v/v PHI and 1% v/v ORT
PHI + ORT + FoCa: 0.2% v/v PHI, 1% v/v ORT and 1% v/v
Fortisol Ca
PHI + ORT + FoCaPlus: 0.2% v/v PHI, 1% v/v ORT and 1.5% v/v
Fortisol Ca Plus
After application of the treatments, the nets with treated lemons
were allowed to drain on a plastic pallet. Subsequently, samples were
stored at 7 0.5 C (8085% RH) for 33 d (hereinafter storage and
transportation), simulating long storage and overseas transport, fol-
lowed by a shelf life period of 5 d at room temperature (22 C) (here-
inafter shelf life), which simulated a commercial retail period.
Residues of postharvest plant protection fungicides currently legal
when applied to citrus in the EU (EU, 2005) were evaluated on the fruit
by an external laboratory (Fitosoil S.L., Murcia, Spain).
2.4. Evaluation of mass losses and incidences of physiological and
pathological disorders
Mass losses during storage and transportation, and shelf life periods
were determined with a precision balance. Incidences (%) of chilling
injury, red blotch and pathological disorders were visually scored by
personnel trained on physiological and pathological disorders of lemon.
Lemons with decay observed after storage and transportation period
were discarded after the evaluation in order to avoid increases of the
incidences of physiological and pathological disorders due to the dis-
semination of spores from the aected fruits to the unaected ones.
Such discarded fruits were taking into account for the calculations after
the shelf life period.
2.5. Statistical analyses
The experiment was a one-factor (postharvest treatment) design
subjected to analysis of variance (ANOVA) using Statgraphics Plus
software (vs. 5.1, Statpoint Technologies Inc., Warrenton, USA).
Statistical signicance was assessed at the level p = 0.05, and Tukeys
multiple range test was used to separate means.
3. Results and discussion
3.1. Chemical residues in treated lemons
The residues of pesticides in food is regulated by the Regulation EU
(2005). Accordingly, maximum residue levels (MRL) of application on
the citrus industry area are: 2-phenylphenol (5 mg kg1), imazalil
(5 mg kg1), pyrimethanil (8 mg kg1), FoCaPlus (75 mg kg1), di-
cloran (0.1 mg kg1), myclobutanil (3 mg kg1) and thiabendazole
(5 mg kg1). The chemical residues data regarding to latter regulated
compounds are presented in Table 1. As observed (Table 1), the MRL
limits were no exceeded by any of the samples. Consequently, the ap-
plied concentrations of treatments may not lead to high quantities of
residues on samples ensuring the food safety of the product according to
the European Regulations.
3.2. Mass loss
Mass losses of treated lemons after storage and transportation, and
shelf life periods are shown in Fig. 1A and B, respectively. F-samples did
G.B. Martnez-Hernndez et al. Food Packaging and Shelf Life xxx (xxxx) xxxxxx

Table 1
Chemical residues in Fino lemons with dierent washing treatments. Values are expressed in mg kg1.

Postharvest treats. CTRL PHI + FoCa PHI + FoCaPlus

Preharvest treats. C F C F C F

2-Phenylphenol 0.022 0.033 2.8 2.5 2.4 2.9

Pyrimethanil 0.013 0.045 1.3 1 1.5 1.1
FoCaPlus < 0.5 < 0.5 < 0.5 < 0.5 1.5 2
Dicloran < 0.010 < 0.010 < 0.010 < 0.010 < 0.010 < 0.010
Imazalil < 0.010 < 0.010 1.1 0.95 0.81 1
Myclobutanil < 0.010 < 0.010 < 0.010 < 0.010 < 0.010 < 0.010
Prochloraz < 0.010 < 0.010 < 0.010 < 0.010 < 0.010 < 0.010
Thiabendazole < 0.010 < 0.010 < 0.010 < 0.010 < 0.010 < 0.010

not show signicant (p < 0.05) dierences of mass losses among dif-
ferent postharvest treatments after 33 d at 7 C with levels ranging
among 3.44.1%. Attending to C-samples, a similar mass losses range of
4.04.6%, without signicant (p < 0.05) dierences among post-
harvest treatments, was observed for all postharvest treatments except
FoCa and FoCaPlus. After 33 d at 7 C, these two treatments induced
mass losses of 15.5 and 7.0%, respectively. Such higher water loss in
those fruits dipped in inorganic salt solutions has been hypothesized to
be as a consequence of a change in supercial water potential due to
osmotic stress resulted from the skin residue after the salt dipping
(Larrigaudire, Pons, Torres, & Usall, 2002). However, FoCaPlus coun-
teracted the potassium sorbate-provoked mass losses in Navel oranges
(Parra et al., 2014). However, the higher salts concentration of FoCa-
Plus, compared to FoCa, induced 3.5-fold lower mass losses in those C-
lemons treated with FoCa. Furthermore, the preharvest application of
FoCa (F-samples) avoided the higher mass losses registered in C-sam-
ples after the storage periods.
As expected, the mass losses of lemons were increased during the
shelf life period of 5 d at 22 C. The higher mass losses observed when
lemons were transferred from lower to higher temperature storage have
been previously reported in other citrus fruits (Cohen et al., 1994;
McCollum, 1989). Such mass losses may be associated with a probably
increased water vapor partial pressure decit at such higher storage
temperature together with higher fruit respiration. These cracks origi-
nated by mass losses were studied by make them visible by dipping fruit
in malachite green solution (Cohen, Rosenberger, & Shalom, 1988). C-
samples treated with FoCa showed the highest mass losses as it was
observed after the storage and transportation period. The lowest mass
losses were observed in those samples treated with the combined
treatments with levels of 9.011.6% after the shelf life period.
Besides the sensory quality importance of mass loss in lemons
during shelf life, it may be also used as a non-destructive indicator of
chilling injury before the symptoms of this physiological disorder ap-
pear (Cohen et al., 1994). Accordingly, latter authors reported that the
mass loss increased after removing lemons from cold storage to shelf
life simulation at 20 C. Accordingly, mass loss was proposed as a better
indicator of possible chilling injury incidence than electrolyte leakage
in citrus fruits (Forney & Peterson, 1990; Pantastico, Soule, & Grierson,
1968).
3.3. Chilling injury incidence
CTRL C-lemons showed the highest chilling injury incidence of
41.9% (Fig. 2). However, CTRL F-lemons showed a trend of lower
chilling injury incidence although it was not signicant (p < 0.05).
Accordingly, the preharvest application of FoCa could lead to lower
chilling injury during postharvest life of lemons. Chilling injury of C-
lemons was reduced 3.3-fold when FoCa and FoCaPlus were applied as
postharvest treatments contrary to mass loss data previously discussed.
It is known that calcium plays a role in the maintenance of cell stability,
particularly cell membranes, under stress conditions such as post-
harvest low temperature storage (Roux & Slocum, 1982, Chapter 13).
Accordingly, preharvest and postharvest calcium applications have
been reported to lower the chilling injury in lemons by reducing the cell
wall breakdown, maintaining the membrane function and prolonging
the capacity for signal transduction (Ferguson & Drobak, 1988;
Poovaiah, 1986; Tsantili, Konstantinidis, Athanasopoulos, & Pontikis,
2002). However, the benecial eect of FoCa to reduce chilling injury

Fig. 1. Mass loss of Fino lemons treated with dierent pre and postharvest treatments after storage and transportation period (A; 33 d at 7 C) followed by shelf life period simulation (B;
5 d at 22 C) (n = 3 SD). White and grey bars represent lemons non-treated (C) and treated with FoCa (F) during preharvest phase, respectively. Dierent capital letters denote
signicant dierences (p < 0.05) among postharvest treatments for preharvest C treatment. Dierent lower-case letters denote signicant dierences (p < 0.05) among postharvest
treatments for preharvest F treatment.

3
G.B. Martnez-Hernndez et al.
incidence was not observed when they were applied as postharvest
treatments in lemons (F-samples) that already received this treatment
during preharvest. No signicant dierences of chilling injury incidence
were found between FoCa, FoCaPlus and PHI + ORT samples. A sy-
nergistic eect was observed when PHI + ORT was combined with
FoCa or FoCaPlus leading to the absence of incidence of chilling injury.
PHI + ORT + FoCa and PHI + ORT + FoCaPlus treatments of lemons
completely (or almost for C-samples) avoided chilling injury of samples
after 33 d at 7 C followed by the shelf life period of 5 d at 7 C. The
latter synergistic eect may be explained by the combined eect of the
calcium salts from FoCa and FoCaPlus with the active ingredients 2-
phenylphenol, imazalil and pyrimethanil from PHI + ORT treatment.
4
Food Packaging and Shelf Life xxx (xxxx) xxxxxx
Fig. 2. Chilling injury incidence on Fino lemons treated with dif-
ferent pre and postharvest treatments after storage and transportation
period (33 d at 7 C) followed by shelf life period simulation (5 d at
22 C) (n = 3 SD). White and grey bars represent lemons non-
treated (C) and treated with FoCa (F) during preharvest phase, re-
spectively. Dierent capital letters denote signicant dierences
(p < 0.05) among postharvest treatments for preharvest C treatment.
Dierent lower-case letters denote signicant dierences (p < 0.05)
among postharvest treatments for preharvest F treatment.
Fig. 3. Red blotch incidence on Fino lemons treated with dierent
pre and postharvest treatments after storage and transportation period
(33 d at 7 C) followed by shelf life period simulation (5 d at 22 C)
(n = 3 SD). White and grey bars represent lemons non-treated (C)
and treated with FoCa (F) during preharvest phase, respectively.
Dierent capital letters denote signicant dierences (p < 0.05)
among postharvest treatments for preharvest C treatment. Dierent
lower-case letters denote signicant dierences (p < 0.05) among
postharvest treatments for preharvest F treatment.
Application of hurdle technology using fungicides has been also pre-
viously reported. Accordingly, imazalil and thiabendazole treatments
applied with hot water reduced signicantly the chilling injury sensi-
tivity in lemons, oranges and grapefruit (McDonald, 1989; McDonald,
Miller, McCollum, & Brown, 1991; Wild & Hood, 1989). Particularly,
hot imazalil was even more eective than tiabendazole to reduce
chilling injury (McDonald et al., 1991).
3.4. Red blotch incidence
The incidence of red blotch in treated lemons after storage and
transportation period followed of shelf life period is shown in Fig. 3.
G.B. Martnez-Hernndez et al.
Fig. 4. Penicillium spp. incidence on Fino lemons treated with dierent pre and postharvest treatments after storage and transportation period (A; 33 d at 7 C) followed by shelf life
period simulation (B; 5 d at 22 C) (n = 3 SD). White and grey bars represent lemons non-treated (C) and treated with FoCa (F) during preharvest phase, respectively. Dierent capital
letters denote signicant dierences (p < 0.05) among postharvest treatments for preharvest C treatment. Dierent lower-case letters denote signicant dierences (p < 0.05) among
postharvest treatments for preharvest F treatment.
The higher red blotch incidences of 61.963.7% were observed in CTRL
lemons after storage and transportation period followed by shelf life
period. Samples treated with FoCa and FoCaPlus showed intermediate
red blotch incidences of 31.439.4%. There were no dierences
(p < 0.05) between C and F-samples for any of the postharvest treat-
ments. Accordingly, application of FoCa in preharvest did not have any
benet over red blotch while the postharvest application of FoCa and
FoCaPlus reduced the red blotch incidence by 1.82.0-fold after storage
and transportation period followed by shelf life period. Furthermore,
the incidence of red blotch was even reduced when PHI + ORT was
included as postharvest treatment leading to even no detected red
blotch in PHI + ORT + FoCaPlus samples. Similar to chilling injury,
the calcium salts from latter postharvest treatments could lead to the
maintenance of cell stability avoiding the damage of epidermal lemon
cells from the red blotch physiological disorder.
3.5. Pathological disorders
The main pathological disorder observed was Penicillium spp. CTRL
and FoCa samples showed the highest Penicillium spp. incidences of
2.73.2% after storage and transportation period (Fig. 4). The Peni-
cillium spp. incidence augmented to 3.84.9% in CTRL, FoCa and Fo-
CaPlus treated samples after shelf life period without signicant
(p < 0.05) dierences among them. In general, no dierences on Pe-
nicillium spp. incidence among both preharvest treatments were ob-
served during storage and transportation, or shelf life periods. No Pe-
nicillium spp. incidence was observed in samples treated with PHI
+ ORT at any postharvest sampling time.
The samples with higher chilling injury also showed higher
Penicillium spp. incidence since the damaged epidermal cells are
priority entrances for the fungal attack. Furthermore, the observed
cracks on epidermal lemon tissue aected with chilling injury have
been hypothesized to facilitate penetration of certain pathogens like
Penicillium spp. (Guilln-Mir, 1978; Schimann-Nadel et al., 1980).
4. Conclusions
The single or combined application of calcium salts-based treat-
ments (FoCa and FoCaPlus) and dierent fungicides on Fino lemon
during a low temperature storage and transportation period (33 d at
7 C) followed by a shelf life (5 d at 22 C) that simulated the retail sale
period are rstly here reported. The preharvest application of FoCa on
trees did not show an advantage to reduce mass losses or Penicillium
5
Food Packaging and Shelf Life xxx (xxxx) xxxxxx
spp. incidence, or prevent the incidence of physiological disorders like
chilling injury and red blotch. However, postharvest treatments with
FoCa and FoCaPlus reduced chilling injury and red blotch incidences in
lemons after storage and transportation period followed by a shelf life
period. Furthermore, the treatments including the fungicides, which
avoided the Penicillium spp. incidence, even reduced the incidence of
latter physiological disorders even to undetected presence for the
treatment PHI + ORT + FoCaPlus. Conclusively, a combined post-
harvest treatment of PHI + ORT with FoCa/FoCaPlus highly reduces,
or even avoids, the pathological and physiological disorders (chilling
injury and red blotch), together with mass losses, in Fino lemon after
the storage and transportation periods followed by the shelf life period
considered.
Acknowledgments
Authors are grateful to Spanish CDTI for nancial support through
project 3835/14IAEA-P. We also thank to Frugarva S.A. for providing
plant material and qualied personal for harvesting.
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