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Evaluating the effect of storage conditions on

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DOI: 10.1016/j.lwt.2017.03.027

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 LWT - Food Science and Technology 80 (2017) 523e530

Contents lists available at ScienceDirect

LWT - Food Science and Technology

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

Evaluating the effect of storage conditions on the shelf life of cape

gooseberry (Physalis peruviana L.)
Mary-Luz Olivares-Tenorio a, b, *, Matthijs Dekker a, Martinus A.J.S. van Boekel a,
Ruud Verkerk a
a
Wageningen University & Research, Food Quality and Design Group, Bornse Weilanden 9, 6708 WG, Wageningen, The Netherlands
b
Fundacio
, Colombia

n Universitaria Agraria de Colombia UNIAGRARIA, Calle 170, No. 54a e 10, Bogota

a r t i c l e i n f o a b s t r a c t

Article history: Cape gooseberry is the fruit of the plant Physalis peruviana L. and has gained commercial and scientific
Received 8 November 2016 interest for its contents of health-promoting compounds. An integral approach to estimate shelf life of
Received in revised form cape gooseberry was conducted taking into account physicochemical, microbiological and nutritional
13 March 2017
changes and consumer acceptance. The experiments were performed for 5 independent harvest times
Accepted 13 March 2017
during two years (2014e2015). The conditions of storage were temperatures of 4, 8 and 12
C and a
relative humidity of 80%. Fruit with (Y) and without calyx (N) were packed into polyethylene tere-
phthalate (PET) trays and polypropylene (PP) baskets, respectively. The experiment was conducted for a
Keywords:
Ascorbic acid
total of 76 d or shorter when the fruit was spoilt earlier. Fruit with the calyx showed a longer shelf life,
b-carotene while 8
C was the temperature that gave longer shelf lives irrespective of the calyx presence. The critical
Fungal growth quality attribute of shelf life without calyx was fungal growth, which determined consumer acceptance;
Modelling weight loss was the most critical quality attribute for the fruit with calyx. Studying various quality at-
Survival analysis tributes in an integral way appeared to give a better understanding of the shelf life.
Shelf life © 2017 Published by Elsevier Ltd.

1. Introduction
Shelf life is defined as the time during which a food product
remains safe, retains desired sensory, chemical, physical and
microbiological characteristics and complies with any label decla-
ration of nutritional data when stored under recommended con-
ditions (IFST, 1993). This time also implies that the food remains of
an acceptable quality to the consumer. Thus, all the above param-
eters should be taken into account when assessing the shelf life of a
food product (Hough & Garitta, 2012). Shelf life estimation of a
fresh food can be evaluated from a product and/or a consumer
perspective; a product view is related to changes occurring in the
fruit, such as microbiological, physical, chemical, biochemical
changes, and the consumer point of view is based on sensory
evaluation (Van Boekel, 2009). Food safety aspects have the priority
when setting shelf life times. Nevertheless, according to the nature
of the food product, sometimes food safety hazards do not occur
* Corresponding author. Wageningen University & Research, Food Quality and
Design Group, Bornse Weilanden 9, 6708 WG, Wageningen, The Netherlands.
E-mail addresses: maryluz.olivarestenorio@wur.nl, maryluzolivares@hotmail.
com (M.-L. Olivares-Tenorio).
before other changes in the food, altering the quality and causing
rejection by the consumer. Between the available techniques for
consumer acceptance, survival analysis has emerged as a relatively
simple methodology to determine shelf life of foods (Hough &
Garitta, 2012; Hough, Luz Calle, Serrat, & Curia, 2007). Survival
analysis has been used before in fresh foods like lettuce and broc-
coli, conducting the current data methodology, where a consumer
evaluates a single sample (Araneda, Hough, & De Penna, 2008;
Garitta, Hough, & Chaves, 2013; Libertino, Osornio, & Hough,
2011). The combination of both perspectives (product and con-
sumer) avoids the bias caused by the ‘arbitrary’ choices when
deciding about shelf life based only on the product point of view;
ultimately, it is the consumer who decides what is tolerated for
consumption or not (Guerra, Lagazio, Manzocco, Barnab a, &
Cappuccio, 2008; Hough & Garitta, 2012). An integral approach to
study shelf life of foods based on combination of perspectives
complies better with the quality definition of satisfying consumer
needs (Luning & Marcelis, 2009).
Cape gooseberry is the fruit of the plant Physalis peruviana L.
that belongs to the Solanaceae plant family and the genus Physalis.
This fruit has a diameter of approximately 1.25e2.50 cm, 4e10 g of
weight, orange yellow skin and a juicy pulp containing numerous

http://dx.doi.org/10.1016/j.lwt.2017.03.027
0023-6438/© 2017 Published by Elsevier Ltd.
524 M.-L. Olivares-Tenorio et al. / LWT - Food Science and Technology 80 (2017) 523e530
small seeds. The berry is contained in a bladder-like calyx (Fischer,
1995). Cape gooseberry contains health-promoting compounds,
especially ascorbic acid and b-carotene (Olivares-Tenorio, Dekker,
Verkerk, & van Boekel, 2016). Few studies on postharvest behav-
iour of cape gooseberry have been reported (Alvarado, Berdugo, &
Fischer, 2004; Lanchero, Velandia, Fischer, & Varela, 2007), never-
theless, shelf life estimations have not been conducted so far.
The present study aims to evaluate the effect of storage condi-
tions such as temperature (4, 8 and 12
C) and presence (Y) or
absence (N) of calyx on the shelf life of cape gooseberry under 80%
RH. This study brings an integrated approach that involves not only
physicochemical and microbiological changes of the fruit as has
been worked traditionally, but also incorporates the evaluation of
health-promoting compounds (ascorbic acid and b-carotene) and
consumer acceptance assessed by a survival analysis. This approach
is an attempt to give a more holistic view of the quality attributes
changes that affect the shelf life of foods and allows making more
accurate estimations based on product and consumer perspectives.
2. Materials and methods
2.1. Fruit material
Cape gooseberry (Physalis peruviana L. Ecotype Colombia) fruit
grown in Pasca, Cundinamarca, Colombia (2180 m.a.s.l.) were har-
vested from February to March 2014 and from March to April 2015
according to Table 1. After harvesting, fruit were selected, choosing
category I and extra with ripeness state No. 4 (for all experiments)
according to the Colombian standard for cape gooseberry NTC 4580
(ICONTEC, 1999), see appendix 1. Fruit subjected to be studied with
calyx were immediately placed into a dry chamber to reduce the
humidity of the calix (36 h at 18
C) and stored according to the
experimental conditions described below. Fruit subjected to be
studied without calyx were pealed after selection and packed in
trays with approximately 300 g of berries each and immediately
stored according to the experimental conditions described below.
2.2. Experimental design and storage conditions
A full 2  3 factorial design was used. Factors: calyx (presence: Y
and absence: N) and temperatures (4, 8, and 12
C). Relative hu-
midity (RH) was set at 80%. Two different package conditions were
used, one for each presentation of fruit as explained in appendix 2.
The set of experiments is depicted in Table 1. Samples were taken
for physicochemical, phytochemical and fungal growth analyses
every 12 d until the fruit was visually spoilt. Samples subjected to
HPLC analyses were treated according to the procedure in appendix
2. All five experiments were independent. For consumer evaluation,
samples were taken weekly until reaching approximately 95% of
consumer rejection. One survival study was done for each year.
2.3. Physicochemical analyses
Blended and filtered fruit was used to measure titratable acidity
against 0.1 mol L1 NaOH. The same juice was used to measure pH
Table 1
Set of experiments conducted for shelf life evaluation of cape gooseberry.
Year Harvest time Storage temperature (
C) Physicochemical Phytochemical
2014 March 8,12 x x
2014 April 8,12 x x
2014 May 8,12 x x
2015 March 4,8,12 x x
2015 April 4 x x x
(HANNA instruments, inc, USA) and total soluble solids TSS with a
refractometer (Brixco, 0e32) at 20
C. Different extraction methods
were performed separately for organic acids content and sugars
content, and both analyses were conducted by HPLC (Dionex Ulti-
mate 3000 RS diode array detector). Maturity index corresponds to
the ratio of TSS/titratable acidity, according to NTC 4580 (ICONTEC,
1999), see appendix 1. Weight loss was assessed with gravimetric
analysis, taking as reference day 0 weight. Colour and firmness of
the berries were analysed directly with a colorimeter (Konica
Minolta Chroma Meter Chroma Meters CR-400) and texture ana-
lyser (Brookfield Engineering Laboratories, Inc, USA). Detailed
methods are given in appendix 2. All measurements were per-
formed in duplicate or triplicate of samples.
2.4. Fungal growth
Two methods were used to assess fungal growth. Mould count
and level of mycelium growth according to methods described in
appendix 2.
2.5. Ascorbic acid and b-carotene
Ascorbic acid content was determined according to the pro-
cedure described by Herna
ndez, Lobo, and Gonz
alez (2006) with
modifications, see appendix 2 (Herna
ndez et al., 2006). The b-
carotene content in cape gooseberry fruit was determined
following the procedure described by Bushway (1986) with modi-
fications, see appendix 2 (Bushway, 1986). Measurements were
performed in duplicate of fruit and extracts and results were
expressed in g kg1 of ascorbic acid or b-carotene on fresh weight
basis.
2.6. Consumer evaluation: survival analysis
A preliminary study was conducted to set the conditions of the
survival analysis, see appendix 3. The consumer study based on
survival analysis was conducted for samples of cape gooseberry
without calyx placed in PET trays. The consumers recruited were
located in different places of the northern part of Bogot

a, Colombia.
For 2014, fruit stored at 8 and 12
C were evaluated by 798 con-
sumers (from 20 to 60 years old with gender equality 50%/50%) over
8 weeks (56 d). The whole consumer study was repeated in 2015. In
this year the PET trays were stored at 4, 8 and 12
C and samples
from two independent fruit batches were evaluated at 4
C (See
Table 1). The same locations as in the 2014 study were selected and
914 consumers participated in the study (from 20 to 60 years old
with 52%/48% male/female) over 9 weeks (63 d). Every week, the
same trays (one for each temperature/experiment) were evaluated
visually by different consumers in the two studies. Consumers were
asked the question ‘are you willing to consume this fruit?’ for every
sample. Each consumer had to evaluate two (in 2014) and four
samples (in 2015) and simply respond ‘yes’ or ‘no’ for every sample,
according to their willingness to consume, based only on the gen-
eral appearance (Libertino et al., 2011). The number of weekly re-
spondents was changed deliberately in order to increase the
Microbiological Consumer Study
x One survival analysis study for 2014 (8 and 12
C)
e
e
x One survival analysis for 2015 (4, 8 and 12
C)
 M.-L. Olivares-Tenorio et al. / LWT - Food Science and Technology 80 (2017) 523e530
number of responses when the rejection rate was increasing, so
when getting close to final shelf life (Hough et al., 2007). The
studies were conducted until the time when more than 90% of the
consumers rejected the fruit.
2.7. Statistical analysis
Analyses of variance (ANOVA) between years, between harvest
times, between temperatures and between presence of calyx (Y, N)
during the studied period were evaluated with the statistical
package SPSS statistics 22 IBM® and using a confidence coefficient
of 95% (a ¼ 0.05). Data related to organic acids content, TSS, sugars,
ascorbic acid and b-carotene contents were corrected for weight
loss in order to avoid bias in results interpretation. Parameter
estimation and simulations of rejection rate of samples by con-
sumers were conducted with the Solver Add-in of Excel Microsoft
Office®.
3. Results and discussion
3.1. Physicochemical changes
Physicochemical results of the five independent experiments
conducted in 2014 and 2015 (Table 1) did not vary significantly,
therefore the combined data were analysed for the effect of tem-
perature and storage time. Titratable acidity, organic acids content,
pH, TSS, sugars content, and colour did also not change significantly
when the fruit contained the calyx or not (P > 0.05), therefore also
these combined data were analysed.
3.1.1. Titratable acidity, organic acids and pH
A reduction in titratable acidity was found over storage time for
all three temperatures (P  0.05) from 2.1 to 0.8% citric acid
equivalent. Storage temperature had an effect on this reduction
(P  0.05). At higher temperatures, a larger reduction of titratable
acidity was observed. The main organic acid identified in the fruit
was citric acid with 16.8 ± 1.6 g kg1 at day 0, which decreased over
the storage time to 9.7 ± 2.0 g kg1 (P  0.05), affected equally as
the titratable acidity by the storage temperature. Malic acid and
tartaric acid were also found but in lower concentrations,
1.8 ± 0.3 g kg1 and 1.7 ± 0.3 g kg1, respectively, at day 0. Malic
acid and tartaric acid acids remained stable during storage time at
the three studied temperatures (P > 0.05). Oxalic acid was not
detected within our samples. In line with the decreased acidity, the
pH of cape gooseberries showed a significant increase at all three
temperatures in storage time from 3.8 (day 0) up to 4.7 after 76 d at
12
C (P  0.05).
3.1.2. TSS and sugars content
TSS decreased for all three storage temperatures (from
13.4% ± 0.3e9.6% ± 0.9) and after day 60 showed a slight increase
(until 11.3% ± 1.0). The sugars identified in cape gooseberry fruit
were sucrose, glucose and fructose, in accordance with a previous
report (Fischer & Lüdders, 1997; Fischer, Ebert, & Lüdders, 2007).
Results of sucrose, glucose and fructose contents in g kg1 for the
three temperatures during storage are shown in Table 2. Univariate
ANOVA for every sugar showed that glucose and fructose increased
slightly during the first 20 d of storage P  0.05 and then remained
stable, while sucrose decreased P  0.05.
3.1.3. Maturity index
The calculated maturity index (Ratio TSS/titratable acidity)
increased over the storage period for all samples P  0.05. In
Appendix 4 a plot is given that shows the continued ripening
process of the fruit during its storage time. Storage at 12
C showed
525
the most rapid ripening of the fruit, followed by 8 and 4
C. This
trend follows the climacteric behaviour as reported for cape
gooseberry by other authors (Galvis, Fischer, & Gordillo, 2005, pp.
165e190; Lanchero et al., 2007). At lower temperature, the ripening
process was slower (P  0.05).
3.1.4. Weight loss
Weight loss was affected by temperature during storage time
(P  0.05) as shown in Fig. 1. After 76 d of storage at 12
C, fruit lost
about 17% of weight. Results in Fig. 1 are presented combined for
fruit with and without calyx because no significant differences
were found (P > 0.05).
Our results were comparable to weight loss reported previously
for Physalis ixocarpa without calyx and Physalis peruviana L.
(Balaguera-lo
pez, C, & Herrera-are
valo, 2014; Benito-Bautista,
Arellanes-Jua
rez, & Pe
rez-Flores, 2016). For the fruit with calyx
(Y), weight loss was one the most important quality attributes that
denoted loss of quality, at least, it was the attribute that changed
most rapid. Considering 6% as a commercial standard limit for
weight loss, the fruit stored at 4
C reached that level at approxi-
mately day 38, while at 8 and 12
C, it took approximately 62 and
24 d respectively.
3.1.5. Colour
The colour expressed as CIELAB values did not change signifi-
cantly with temperature nor with presence or absence of calyx (Y,
N) (P > 0.05). Differences in colour were noticed over storage time:
L* decreased (from 57.1 to 50.7, P  0.05), a* remained stable
(z10.0) and b* decreased (from 47.3 to 35.4, P  0.05). This a* and
b* behaviour indicates a colour change from yellow to orange which
might be related to b-carotene synthesis. Pearson's correlation
coefficients of b-carotene contents and a* and b* indicate that b*
values and b-carotene contents are negative correlated R2 ¼ 0.414,
N ¼ 84, P ¼ 0.000. a* and b-carotene are not correlated R2 ¼ 0.269,
N ¼ 84, P ¼ 0.13. Colour values were similar to earlier reported data
on the colour of cape gooseberry (Lo
pez et al., 2013).
3.1.6. Firmness
Firmness was affected by temperature (P  0.05) and the pres-
ence or absence of calyx (Y, N) (P  0.05) as shown in appendix 4.
Firmness decreased over time, this decrease was faster at higher
storage temperature. In the fruit without the calyx (N) the firmness
decreased faster because of the lack of protection from environ-
mental conditions that the calyx gives to the berry. The mechanism
behind firmness decrease of cape gooseberry fruit is a co-ordinated
series of enzymatic activities, where after the start of ethylene
synthesis, respiratory rate increases associated with an increased
level of polygalacturonase activity resulting in pectin trans-
formation from insoluble to soluble, leading to a gradual softening
of the cape gooseberry fruit (Majumder & Mazumdar, 2002;
Pressey, Hinton, & Avants, 1971).
3.2. Fungal growth
The microbiological problem most strongly associated to cape
gooseberry was the development of fungus on the fruit. Although,
berries can be subjected to several handling steps that might lead to
other type of microbiological contamination, for the purpose of this
study, the fruit was manipulated according to good agricultural
practices. Fungus development varied drastically with the presence
(Y) or absence (N) of the calyx and the harvest time (year)
(P  0.05). Fig. 2 depicts the growth of fungi expressed as the mould
count (CFU g1) and the level of mycelium growth (%), visually
assessed, in experiments with fruit without calyx (N). As statistical
differences were detected at 8 and 12
C and between harvest times
526 M.-L. Olivares-Tenorio et al. / LWT - Food Science and Technology 80 (2017) 523e530

Table 2
Sugars content (g kg1) of cape gooseberry during storage time at three temperatures and 80% RH.

Storage temperature Storage time (days) na Sucroseb Confidence interval 95% Glucosec Confidence interval 95% Fructosed Confidence interval 95%

Lower bound Upper bound Lower bound Upper bound Lower bound Upper bound


4 C 0 8 26.6 23.3 30.0 16.3 13.6 19.0 8.9 6.8 10.9
24 8 17.4 14.1 20.8 20.8 18.1 23.5 15.7 13.7 17.8
35 16 16.2 13.9 18.6 21.4 19.5 23.3 14.0 12.6 15.5
44 8 14.3 11.0 17.7 19.7 17.1 22.4 14.6 12.6 16.7
55 8 14.2 10.8 17.6 21.0 18.4 23.7 14.9 12.9 17.0
76 8 18.6 15.2 21.9 19.7 17.0 22.3 15.9 13.9 18.0
8
C 0 16 52.5 49.1 55.8 25.9 23.2 28.6 23.7 21.6 25.7
24 12 36.4 33.0 39.7 31.0 28.4 33.7 28.9 26.9 31.0
35 24 31.9 29.6 34.3 28.4 26.5 30.2 28.1 26.7 29.6
44 12 23.0 19.7 26.4 32.9 30.2 25.6 31.3 29.3 33.4
55 12 30.5 27.2 33.9 25.7 23.0 28.4 26.9 24.9 29.0
76 8 24.7 21.4 28.1 24.6 21.9 27.3 28.0 26.0 30.1
12
C 0 16 47.7 45.3 50.0 24.7 22.9 26.6 23.0 21.5 24.4
12 12 33.6 30.2 36.9 26.7 24.0 29.3 26.1 24.0 28.1
24 8 24.0 19.3 28.8 26.7 22.8 30.3 26.6 23.7 29.5
35 24 24.2 21.9 26.6 28.5 26.7 30.4 29.8 28.3 31.2
44 4 24.2 19.4 28.9 32.5 28.7 36.2 35.8 32.9 38.7
55 12 23.4 20.1 26.8 22.0 19.3 24.6 24.3 22.3 26.4
76 8 21.5 18.1 24.9 18.6 16.0 21.3 21.7 19.7 23.8
a
n values vries because of the differences in number of experiments and samples for each temperature as the analyses were not conducted after the fruit was spoilt.
b
Univariate ANOVA Between-subject effects:Sucrose (Temperature): F(2,175) ¼ 151.641 P ¼ 0.000Sucrose (Time): F(6,175) ¼ 66.734 P ¼ 0.000Sucrose (Time, Temperature):
F(10,175) ¼ 6.069 P ¼ 0.000.
c
Univariate ANOVA Between-subject effectsGlucose (Temperature): F(2,175) ¼ 72.472 P ¼ 0.000Glucose (Time): F(6,175) ¼ 7.789 P ¼ 0.000Glucose (Time, Temperature):
F(10,175) ¼ 1.330 P ¼ 0.219.
d
Univariate ANOVA Between-subject effectsFructose (Temperature): F(2,175) ¼ 433.524 P ¼ 0.000Fructose (Time): F(6,175) ¼ 21.239 P ¼ 0.000Fructose (Time, Temper-
ature): F(10,175) ¼ 5.379 P ¼ 0.000.

Fig. 1. Effect of temperature (4
C, ; 8
C, ; 12
C, ) and time on weight loss of cape gooseberry fruit at 80% RH (P  0.05). Vertical bars represent standard deviation Weight loss vs
time (n ¼ 4e16)*; Weight loss vs Temperature (n ¼ 36e52)*.
*
n values varies because of the differences in number of experiments and samples for each temperature as the analyses were not conducted after the fruit was spoilt.

Fig. 2. (A) Effect of temperature and time on fungal growth in cape gooseberry without calyx ‘N’ at 80% RH. CFU colony forming-unit g1 (n ¼ 3) (4
C -2015-1, ; 4
C-2015-2, ; 8
C-
2014, ; 8
C-2015, ; 12
C-2014, ; 12
C-2015, ) (P  0.05) and (B) Level of mycelium growth (LMG) (%) (n ¼ 3) (4
C -2015-1, ; 4
C-2015-2, ; 8
C-2014, ; 8
C-2015, ; 12
C-
2014, ; 12
C-2015, ) (P  0.05).
 M.-L. Olivares-Tenorio et al. / LWT - Food Science and Technology 80 (2017) 523e530
(P  0.05), all harvest times were plotted. Fungal growth of samples
with calyx was negligible during the storage time studied.
Fungal growth appeared to be the most critical attribute for the
shelf life of cape gooseberry without calyx (N). Higher temperature
resulted in higher counts at shorter time when comparing samples
stored at 8 and 12
C. Mould count in samples stored at 4
C
remained stable during time up to 55 d. The reduction in CFU at
12
C at day 24e30 CFU might be due to the complexity of fungus
quantification that makes mould counts not to be the most suitable
method to evaluate fungal growth (Gibson and Hocking, 1997).
Therefore, in the present study these results were combined with
the level of mycelium growth that has been used extensively to
monitor fungal growth (Jiang & Li, 2001). Mycelium growth
showed a different pattern for 4 and 8
C. At 4
C, in contrast with
the results of the mould count, the mycelium was visible earlier. At
8
C, there was a large difference between the harvest years. The
harvest of 2014 presented visible mycelium and growth sooner
than the harvest of 2015 (Fig. 2B). In contrast to the harvest of 2014,
in 2015 storage at 4 or 8
C did not show differences in the level of
mycelium growth over time. The fruit stored at 4
C, for the two
experiments conducted in both years presented a wet surface,
which could be a result of chilling injury of the fruit that disrupt
cells, increasing humidity, and the growth of fungi (Cantwell,
Flores-Minutti, & Trejo-Gonza
lez, 1992). Besides, we noticed visu-
ally when preparing samples for analyses, that after calyx removal,
a terpene covering substance (Chirinos et al., 2009; Valencia, 1985)
on the fruit increased significantly the moisture, making a good
substrate for microbial growth during storage time. The presence of
fungi is related to cultivation conditions rather than contamination
during storage time because they are associated to diseases, pest
and weeds of the plant Physalis peruviana L. (Fischer, Almanza-
Mercha
n, & Miranda, 2014). Nevertheless, enzymatic changes of
pectin in plant cell walls and cape gooseberry pH, makes the fruit
more vulnerable to fungal infection (Wubben, ten Have, van Kan, &
Visser, 2000).
3.3. Ascorbic acid and b-carotene
Because the presence (Y) or absence (N) of calyx as well as
harvest times and years (2014 and 2015) did not show a significant
effect on the ascorbic acid content (P > 0.05), the results are shown
combined in appendix 4. Ascorbic acid increased at the three
temperatures until a certain period of storage time, thereafter
degradation took place at 12
C. At 4 and 8
C, after reaching a peak,
the ascorbic acid remained stable during the studied storage time.
Decrease of ascorbic acid at 12
C after day 44 probably can be due
to oxidation processes. Our findings related to the increase of
ascorbic acid during storage are similar to what has been reported
for Physalis ixocarpa (husk tomato) and tomato (Solanum lyco-
persicum, also from Solanaceae family (Cruz-Alvarez,
Martínez-
Damia
n, Rodríguez-Pe
rez, Colinas-Leo

n, & Moreno-Pe
rez, 2012;
Giovanelli, Lavelli, Peri, & Nobili, 1999). On the contrary, in cape
gooseberry, ascorbic acid decreased rapidly during storage at 20
C
after the calyx was removed (Valdenegro, Fuentes, Herrera, &
Moya-Leo
n, 2012), probably because the higher temperature pro-
moted degradation of ascorbic acid.
b-carotene did not change significantly between harvest times
(P > 0.05), therefore data are presented combined (appendix 4).
Effects of temperature and presence (Y) or absence (N) of the calyx
were found (P  0.05). b-carotene increased at 12
C, at 8
C first
increased and then decreased; and at 4
C it remained stable. The
presence of the calyx played a role in b-carotene development.
When the fruit was removed from the calyx, b-carotene increased
at 8 and 12
C, at 4
C there was no significant change. Experiments
on cape gooseberry have shown an increase of b-carotene related to
527
ripening stages (Olivares-Tenorio et al., 2016).
3.4. Consumer acceptance evaluation: survival analysis
Survival analysis was made by the evaluation of consumer
rejection probabilities calculated from the data obtained for the
fruit without calyx (N), at different storage times, evaluated tem-
peratures and harvest years, according to Table 1. The Weibull
distribution model (equation (1)) was selected to model the sur-
vival analysis (Hough, Subramaniam, Narain, & Beeren, 2013).
 
lnðtÞ  m
FðtÞ ¼ Fsev (1)
s
Fsev represents the survival function of the smallest extreme value
distribution and m and s are the model's parameters shown in
Table 3 (Araneda et al., 2008; Gime
nez, Ares, & Ares, 2012). Fig. 3
shows the data and the model. As mentioned, surveys were con-
ducted for fruit stored at three temperatures (4, 8 and 12
C) and
80% RH without calyx only. To estimate shelf life, authors usually
choose a rejection probability of 50% (FðtÞ ¼ 0.5) (Araneda et al.,
2008; Cardelli & Labuza, 2001; Gacula Jr & Singh, 1984). From
this, shelf lives of cape gooseberry were calculated based on the
value and the estimations as shown in Table 3.
In 2014, no differences between the rejection rate of fruit stored
at 8
C and 12
C were found. For 2015, shorter shelf life was ob-
tained at 12
C with 10.9 ± 1.1 d. At 4
C, the shelf life was 23.0 ± 1.4
and 21.8 ± 1.5 d and at 8
C, 56.1 ± 1.0 d. These variations between
rejection rates are related to fungal growth, one of the most rapid
noticeable change in the fruit (by consumers). Although the differ-
ence between harvest times is evident, the storage temperature that
showed better results from the consumer point of view was 8
C.
3.5. Shelf life estimations
As this study integrates evaluations of quality from different
perspectives, Figs. 4 and 5 represent shelf lives estimations based
on the measured parameters of cape gooseberry quality and/or
consumer acceptance. Fig. 4 depicts quality attributes that denoted
loss of quality more rapid for fruit with calyx (Y). Weight loss and
firmness were the most important changes in the fruit with the
calyx (Y). Considering a 6% of weight loss (commercially used) a
limit for delivering fruit quality, 8
C gives longest shelf life values
(approx. 62 d), followed by 4
C (approx. 38 d) and 12
C (approx. 24
d). Cape gooseberry with calyx is sensitive to storage temperature,
when the temperature is low (4
C) it might suffer chilling injury,
increasing weight losses and loss of firmness. At higher tempera-
ture (12
C), transpiration processes take places more rapid, stim-
ulating these changes as well.
Fig. 5 shows the level of mycelium growth (LMG) and the con-
sumer rejection probability (CRP), which were the critical factors in
shelf life of fruit without the calyx (N). As previously mentioned,
consumer rejection was the parameter determining shelf life in this
presentation. Since fungal growth had a close relation with con-
sumer rejection, they are both plotted. For fruit stored at 4
C, the
rejection of consumers starts before the fungal growth is visible
because of the chilling injury of the fruit that increased the mois-
ture of the surface of the fruit. Shelf lives values were already given
in Table 3.
Ascorbic acid and b-carotene, at the three evaluated tempera-
tures and with and without calyx are still present at the end of the
shelf life of cape gooseberry and at any stage of the storage time.
The amounts of these compounds are high contents in comparison
with other fruit sources (USDA, 2014, 2016). Results are in Table 4
based on data presented in appendix 4.
528 M.-L. Olivares-Tenorio et al. / LWT - Food Science and Technology 80 (2017) 523e530

Table 3
The parameters m and s of the Weibull model for the experimental data and Confidence intervals CI (95% confidence) and shelf life values estimated of cape gooseberry with
50% probability of rejection by consumer's data and Confidence intervals CI (95% confidence).

Temperature/harvest time m ± CI s ± CI Shelf life values (days) Confidence interval 95%

Lower bound Upper bound

8 Ce2014 3.51 ± 0.05 0.09 ± 0.06 32.5 31.7 33.3
12
Ce2014 3.57 ± 0.08 0.17 ± 0.11 33.4 31.9 34.9
4
C - 2015-1 3.33 ± 0.16 0.54 ± 0.26 23.0 21.6 24.4
4
C - 2015-2 3.29 ± 0.17 0.56 ± 0.28 21.8 20.3 23.3
8
Ce2015 4.07 ± 0.04 0.12 ± 0.06 56.1 55.1 57.1
12
Ce2015 2.64 ± 0.20 0.67 ± 0.28 10.9 9.8 12.0

Fig. 3. (A) Consumer rejection probability CRP as a function of storage time for studies 2014 (8
C, ; 12
C, ) and (B) 2015 (4
C-1, ; 4
C-2, ; 8
C, ; 12
C, ). Lines represent
Weibull models and points are experimental data.

▪
Fig. 4. Shelf lives of cape gooseberry with calyx ‘Y’ at 4 (A), 8 (B) and 12
C (C) (firmness, ; weight loss, ). Horizontal dashed lines represent the cut-off point ( ) of 6% as the
acceptance limit of weight loss and relate cut-off point with shelf life. Vertical dashed lines related cut-off point con firmness values. All data from 2014 to 2015 are presented
combined.

▪
Fig. 5. Shelf lives of cape gooseberry without calyx ‘N’ at (A) 4
C (2015-1, 2015-2), (B) 8
C (2014) and 12 (C) 12
C (2014). Horizontal dashed lines represent the cut-off point ( ) of
0.5 as the acceptance limit Consumer Rejection Probability (CRP, ) and relate cut-off point with Level of Mycelium growth (LMG, ). Vertical dashed lines relate cut-off point with
shelf life. Shelf life estimations for fruit without the calyx (N) are depicted (4
C 2015 and 8 and 12
C of 2014 as examples).
 M.-L. Olivares-Tenorio et al. / LWT - Food Science and Technology 80 (2017) 523e530
Table 4
Estimation of ascorbic acid and b-carotene contents in cape gooseberry with and without calyx, stored at 4, 8 and 12
C, at the end of shelf life.
Temperature/Harvest time Presentation
4
C - 2015- 1-2 Calyx (Y)
8
C - 2014e2015 Calyx (Y)
12
C - 2014e2015 Calyx (Y)
8
C - 2014 No calyx (N)
12
C - 2014 No calyx (N)
4
C - 2015-1 No calyx (N)
4
C - 2015-2 No calyx (N)
8
C - 2015 No calyx (N)
12
C - 2015 No calyx (N)
a
Values taken from the closest data point in time (appendix 3).
4. Conclusions
Cape gooseberry (Physalis peruviana L.) is a climacteric fruit with
difficulties to retain an acceptable level of quality attributes. An
integrated approach to shelf life estimation showed that storage
temperature has a large effect on the shelf life of the fruit. Presence
of calyx did not play a big role in the ripening process in storage
time. Nevertheless, the removal of calyx is the crucial factor in
fungal growth because it stimulated the increase of the fruit surface
moisture, promoting the growth of fungi. Consumer rejection due
to signs of fungal growth determined shelf life of cape gooseberry
without the calyx.
In summary, 8
C is the most suitable temperature to store cape
gooseberry in comparison with 4 and 12
C, either with calyx (Y) or
without (N) under the studied conditions (80% RH). The shelf life is
longer when the calyx is not removed. The consumption of cape
gooseberry during the times estimated in this research is safe when
the conditions of handling meet the good agricultural practices.
Contents of ascorbic acid and b-carotene are still relevant at the end
of the shelf life of cape gooseberry.
The use of an integral approach to estimate the shelf life of cape
goosebery is a suitable methodology to understand the changes of
the product form different perspectives because it permits to
correlate quality attributes changes with consumer acceptance. The
use of survival analysis allows to have more insights about con-
sumer acceptance since the number of consumers participating in
the study is higher than in trained panels. Besides, the fact that they
are actual consumers gives more reliability to shelf life estimations.
The only use of sensory evaluation for the estimation of shelf life
does not mean that the food safety regulation should not be
considered. Thus, before starting a study on shelf life estimation,
the nature of the food must be assessed in terms of what quality
attributes might be limiting the shelf life and their relation to the
food safety requirements.
Acknowledgments
This work was supported by NUFFIC Netherlands Universities
Foundation for International Cooperation (NFP-PhD.11/830) and
COLCIENCIAS Administrative department of science, technology
and Innovation of Colombia (Agreement 268-2014). The authors
gratefully acknowledge FLP Fresh fruit and vegetables for their lo-
gistic collaboration in offering information and providing cape
gooseberry fruit in Colombia and The Netherlands; Sandra Bar-
acaldo and Elena Escobar for their collaboration in data gathering;
and Dr. Guillermo Hough for his inputs in the development of the
survival analysis study.
Appendix A. Supplementary data
Supplementary data related to this article can be found at http://
dx.doi.org/10.1016/j.lwt.2017.03.027.
529
Estimated Shelf life values (days) Ascorbic acida g kg1 b-carotenea g kg1
38.0 0.33e0.34 0.013e0.014
62.0 0.44e0.47 0.016e0.021
24.0 0.32e0.36 0.015e0.024
32.5 0.42e0.46 0.013e0.019
33.4 0.33e0.39 0.013e0.019
23.0 0.29e0.31 0.010e0.012
21.8 0.29e0.31 0.010e0.012
56.1 0.44e0.47 0.016e0.021
10.9 0.27e0.30 0.006e0.007
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