Journal of Stored Products Research 45 (2009) 206–211

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Journal of Stored Products Research

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Survival kinetics of Ephestia kuehniella eggs during 46–75  C heat treatment

Ameziane Ben-Ialli a, Jean-Michel Méot b, Philippe Bohuon c, *, Antoine Collignan c
a
Alterbio, UMR QualiSud, Z.I. Saint Charles, rue Levavasseur, 66000 Perpignan, France
b
CIRAD, UMR QualiSud, 40/15, 73 rue Jean François Breton, 34398 Montpellier, Cedex 5, France
c
Montpellier SupAgro, UMR QualiSud, 1101 Avenue Agropolis, CS 24501, 34093 Montpellier Cedex 5, France

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

Article history: The effect of heat treatment on the survival of Ephestia kuehniella eggs was examined. Samples of 60 eggs
Accepted 9 March 2009 were immersed in hot water at constant temperature in the 46–75  C range for 5–1200 s. Following heat
treatment and cooling, the eggs were stored at 24  1  C in a growth chamber for 7 days before survival
Keywords: evaluation. Statistical analysis of the data demonstrated that the thermal survival kinetics were best
Disinfestation represented by a first-order reaction. The rate constant had an Arrhenius-type dependence over the 54–
Thermal death kinetics
75  C temperature range. Kinetic parameters were estimated by non-linear regression. The activation
Arrhenius activation energy
energy (Ea) and rate constant (kref) at the reference temperature (Tref ¼ 64.8  C), were determined as
Pests
Food 102.2  6.2 kJ mol1 and 0.061  0.003 s1, respectively, over the 54–75  C temperature range. A 0.01%
survival rate was obtained after 50 s at 75  C. The data at temperatures below 50  C were not in
accordance with those at higher temperatures. Above this temperature, mortality was likely due to
physiological disorders, as noted on a DSC thermogram.
Ó 2009 Elsevier Ltd. All rights reserved.

1. Introduction technique. Packaging products under modified or controlled

Many plant-based food products (cereals, fresh or dried fruits
and vegetables, etc.) contain insects despite protective measures
taken during the cropping stage. Infestations can be substantially
reduced by procedures such as releasing sterile females or preda-
tors, disseminating pathogens, using pheromone traps or setting up
some form of physical protection to reduce insect access to crops,
but none of these provides total protection (Khoualdia et al., 1996;
Nay et al., 2006). A disinfestation treatment is required to ensure
efficient preservation of the product. Chemical fumigation is the
most common disinfestation process (Taylor, 1994; Fields and
White, 2002). However, due to their toxicity and negative environ-
mental impacts, some of these chemical products can no longer be
produced or used (e.g. methyl bromide from 2005), and regulations
have also been passed to strictly control fumigation conditions.
Consumer awareness of the negative impacts of chemicals on
human health and the environment is increasing, so there is now
high consumer demand for products that have been disinfested by
alternative techniques.
Irradiation (g-rays, X-rays, etc.) is an efficient and inexpensive
alternative when implemented on a large scale (Hallman, 2001),
but consumers often shy away from products treated by this
* Corresponding author. Tel.: þ33 4 67 61 57 26; fax: þ33 4 67 61 57 28.
E-mail address: philippe.bohuon@supagro.inra.fr (P. Bohuon).
atmospheres is another solution (Chervin et al., 1996), but this
technique is costly and thus is mainly only used with high added-
value products. Freezing products at temperatures in the 25  C
range is lethal for most insect larvae (Brokerhof et al., 1993;
Chauvin and Vannier, 1997; Dupuis et al., 2006), but expensive
(initial investment and energy consumption), and can generally
only be used with relatively small product volumes since it takes
several hours to take effect.
Air or water heat treatments have been studied for the disin-
festation of cherries (Feng et al., 2004), oranges (Sharp and
McGuire, 1996), mangoes (Sharp et al., 1989), papayas (Armstrong
et al., 1995), apples (Smith and Lay-Yee, 2000) and persimmons
(Dentener et al., 1997; Lay-Yee et al., 1997). One to several hours are
required for diffusive energy transfer through a fruit to ensure 100%
insect mortality at the required temperature (T  50  C). These
conditions (time, temperature) can sometimes be detrimental to
the overall product quality. Moreover, short high-temperature
treatments using a microwave (Vadivambal et al., 2007) or a high
frequency source (Tang et al., 2000; Vadivambal and Jayas, 2007;
Zhao et al., 2007) may be effective and avoid product quality
degradation. After treatment, insects have a higher temperature
than the food products due to the difference in dielectric properties
(Nelson, 1973), which means that a selective product treatment
could potentially be implemented.
It is essential to know the intrinsic thermal susceptibility of the
target insect before determining the optimal heat treatment

0022-474X/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jspr.2009.03.001
 A. Ben-Ialli et al. / Journal of Stored Products Research 45 (2009) 206–211 207

conditions (time/temperature) for efficient disinfestation of 2.2. Heat treatment procedure

a product. Table 1 provides some examples of egg mortality, along
with the many experimental methods that have been used by
different authors to study egg mortality during heat treatment,
and the heat susceptibility threshold specific to each insect.
Overall, it is clear that as the temperature rises the treatment time
required to obtain the same disinfestation level decreases. Insect
eggs are very susceptible to temperatures above 50  C (Mahroof
et al., 2003; Zhao et al., 2007). However, it is hard to use these
previously published data because the temperature information
provided often corresponds to that of the environment (fruit or
ambient conditions) not to the actual thermal patterns of the eggs.
The temperature of eggs is never measured because of their small
size, i.e. under 500 mm (Cônsoli et al., 1999). During hot air
treatment, the rise in egg temperature is accompanied by dehy-
dration, which contributes to egg mortality. The only way to very
quickly achieve a thermal balance between the eggs and the water
without substantially modifying the egg water content is through
convective heat transfer by plunging the eggs in hot water. Finally,
the very few other cases in which the data were obtained under
known thermal conditions are of minimal value due to the
questionable data quality (lack of replications or small datasets).
The aim of this work was twofold: to experimentally quantify
the survival of Ephestia kuehniella Zeller eggs following heat
treatments in hot water and to develop a kinetic model to describe
and predict their survival in heating situations. The kinetic model
was based on experimental data obtained from constant temper-
ature heat treatment. We discuss the advantages of using high-
temperature/short-time thermal treatments for egg disinfestation
in order to reduce the thermal impact on product quality.
Sealed Plexiglass tubes (10 mm internal diameter by 20 mm
length) filled with 0.5 ml of water were immersed in a 10-l
agitated water bath (Aqualine AL, LAUDA, Neuilly sur Seine,
France; equipped with electronic PID regulation). The bulk water
temperature was controlled at the desired temperature (46, 54, 60,
65, 70 or 75  C) to within 0.5  C. Immediately before treatment,
the water temperature was verified inside the tubes using a PT-100
temperature sensor (AOIP, Ris Orangis, France). Approximately 60
eggs were placed and soaked in water for various immersion times
(5–1200 s). After thermal treatment, the tube was rapidly removed
from the water bath and 1 ml of cool water (25  1  C) was poured
into the tube to immediately decrease the temperature. The tube
was immersed in cool water (25  1  C) for 2 min, then drained
and the eggs were collected on moist CansonÒ paper inside Petri
dishes (33 mm dia.). Each heat treatment condition was replicated
10 times.
2.3. Survival assessment
Petri dishes containing eggs on CansonÒ paper were held in
a growth chamber at 24  1  C for 7 days to ensure that all hatches
were achieved and mortality was evaluated using a binocular
microscope (Paralux, 4–10 magnification). Egg mortality was
based on the presence or absence of an exit rupture in the egg
chorion and calculated by taking the natural mortality of untreated
eggs into account. Egg mortality at time t, denoted M(t), was
calculated as the ratio change of unhatched eggs at time t to the
total treated eggs. The egg survival rate was expressed by
   
SðtÞ ¼ 1  M ðtÞ = 1  Mð0Þ (1)

2. Materials and methods
2.1. Ephestia kuehniella egg supply
Mediterranean flour moth (E. kuehniella) eggs were obtained
from INRA (Antibes, France). Ephestia kuehniella larvae were reared
on hard wheat semolina. Throughout the experiments, insect
cultures were maintained at constant temperature (20  1  C),
under a 14L:10D photoperiod and at 75  5% relative humidity
(r.h.). Recently hatched eggs were shipped in sealed containers
under controlled conditions (15  C at 75% r.h.). The trials were
carried out within 30 h after the eggs arrived at the laboratory. The
hatching rate of these untreated eggs was 972%.
where M(0) is the initial mortality of eggs (control mortality close to
3  2%). Mean values and confidence interval (P ¼ 0.01) were
obtained from 10 replications for each temperature–time combi-
nation. For this experimental regime, control batches of eggs were
run both as untreated and by standing for 1200 s in water at 25  C.
2.4. Thermal analysis of eggs with differential scanning calorimetry
Eggs (25.0  0.1 mg) were hermetically sealed in an aluminium
pan and the heat flow between the sample and an empty reference
pan was measured using differential scanning calorimetry (DSC)
with a Perkin Elmer DSC7 (Norwalk, USA). Samples were heated
from 25 to 150  C at a scanning rate of 5  C min1.

Table 1
Some exposure times (t) for egg mortality at product or medium temperature (T) obtained with different heating methods.

Insect name Infested product Medium and heating method T ( C) t (min) Reference
Ephestia cautella Walker Date palm Hot forced air in test chamber 60 20 Al-Azawi et al. (1983)
Carpophilus hemipterus (L.) Date palm Hot forced air in test chamber 60 5 Al-Azawi et al. (1984)
Ceratitis capitata (Wiedemann) Mango Hot forced air in test chamber 46.5 10 Heather et al. (1997)
No product 30 ml Plexiglass tube in hot water 45–47 63.2–8.8 Jang (1986)
Citrus fruit Hot forced air 43–49 184–1.7 Lurie et al. (2004)
Ectomyelois ceratoniae (Zeller) Date palm Microwave heating (2450 MHz) 63 3 Reynes (1997)
Sitophilus oryzae (L.) Rice Microwave heating (2450 MHz) 55 1.5 Zhao et al. (2007)
Liposcelis bostrychophila Badonnel No product Heating block (air tight) 45–47 900–310 Beckett and Morton (2003)
Liposcelis decolor Pearman No product Heating block (air tight) 45–47 1667–910 Beckett and Morton (2003)
Liposcelis paeta Pearman No product Heating block (air tight) 45–47 6750–288 Beckett and Morton (2003)
Cydia pomonella (L.) No product Temperature ramp in heating block 50–52 6.7–1.9 Wang et al. (2004)
Dacus cucurbitae Coquillett No product 30 ml Plexiglass tube in hot water 45–48 42.17–5.0 Jang (1986)
Dacus dorsalis Hendel No product 30 ml Plexiglass tube in hot water 45–48 51.9–13.1 Jang (1986)
Bactrocera tryoni Froggatt No product 45 ml Plexiglass tube in hot water 42–48 254–5.5 Waddell et al. (2000)
Anastrepha ludens (Loew) No product Hot forced air (50% RH) 52 240 Yahia and Ortega-Zaleta (2000)
208 A. Ben-Ialli et al. / Journal of Stored Products Research 45 (2009) 206–211

Table 2 Table 3
Survival rate of Ephestia kuehniella eggs after time t at several temperatures T. Rate constant for the fit of S(t) ¼ exp(kt) at several temperatures T.

t (s) Survival rate (%) T ( C) k  103 (s1) R2 RMSD

T ¼ 46  C T ¼ 54  C T ¼ 60  C T ¼ 65  C T ¼ 70  C T ¼ 75  C 46 0.4  0.1 0.91 0.033

54 21.3  0.8 0.97 0.065
0 97  2 97  2 97  2 97  2 97  2 97  2
60 32.1  1.7 0.95 0.095
5 nd nd nd nd 67  10 40  11
65 55.2  1.9 0.98 0.051
10 96  5 87  4 81  11 60  7 26  6 42
70 104.0  5.0 0.96 0.078
30 95  2 56  6 45  5 15  2 52 00
75 207.0  11.0 0.97 0.078
60 94  4 22  4 22 00 00
120 92  4 11 00 k-Values  confidence interval (P ¼ 0.01).
180 92  3 00 RMSD, root mean square deviation of S(t).
240 91  5
600 78  5
780 70  6 apparent activation energy of the reaction (J mol1), and the gas
1200 64  4
constant (8.314 J mol1 K1). The rate constant k was estimated by
Values presented as the mean  confidence interval (P ¼ 0.01) with n ¼ 10 per group. non-linear regression (TableCurve2DÒ V2.03, Jandel Scientific
nd, Not determined.
Software) at each temperature from the relationship S(t) and t.
Because of the close correlation between k0 and Ea, a simple rep-
arameterization was achieved by introducing a reference temper-
2.5. Kinetic modelling ature Tref as follows (Van Boekel, 1996)

The purpose of this kinetic modelling was to develop a useful k ¼ kref expðEa XÞ (4)
tool which, associated with a heat transfer model, could predict
where
survival rates of eggs at any location in a solid product exposed to
different heating processes (hot air, hot water, vapour, microwaves,   
kref ¼ k0 exp  Ea = RTref (5)
infrared, etc.), under isothermal or non-isothermal conditions
(heating, maintaining, cooling). Equations are thus presented to
evaluate cumulative effects of any time–temperature history T(t) on 1 
X ¼ 1=T  1=Tref (6)
survival rate of eggs. In order to describe the thermal survival of R
eggs, a kinetic model approach was used in which the reaction
In this reparameterization, the pre-exponential factor kref becomes
order was evaluated. The activation energy, which is related to the
the rate constant at the reference temperature. The reference
temperature dependence of the reaction rate, was identified
temperature was chosen to be in the middle of the studied
(Waddell et al., 2000; Wang et al., 2002). The survival rate of eggs
temperature range as follows:
S(t) during heat treatment was described in terms of first-order
kinetics: n
1X
Tref ¼ T (7)
SðtÞ ¼ expðktÞ (2) n i¼1 i

The rate constant k (s1) varied with the absolute temperature T
(K) of the system according to the Arrhenius law.
k ¼ k0 expð  Ea =ðRTÞÞ
where k0, Ea, and R were, respectively, the pre-exponential factor,
which was assumed to be temperature independent (s1), the
Taking the temperature dependence into account by including the
reparameterized Arrhenius equation (Eq. (4)) at the five or six
heating temperatures simultaneously, the k-values in the proposed
(3)
100

10-1
1.08
75°C
rate constant k (s-1)

Ttrans
Endothermic heat flow (W/g)

1.06
10-2
54°C

1.04

10-3 46°C

1.02

2.8 2.9 3 3.1 3.2

25 50 63 75 100 125 103/T (K-1)
T (°C)
Fig. 2. Arrhenius plot of the rate constant for the survival of Ephestia kuehniella eggs at
Fig. 1. DSC thermogram of Ephestia kuehniella eggs (Ttrans: transition peak). several temperatures T.
 A. Ben-Ialli et al. / Journal of Stored Products Research 45 (2009) 206–211 209

Table 4 short for comparative assessment. Other authors who have

Estimated parameters for the fit of S(t) ¼ exp[kref exp(EaX)t] in several tempera- assessed the effects of heat treatment used a narrower treatment
ture ranges with X ¼ ðð1=TÞ  ð1=Tref ÞÞ=R.
range, i.e. 46–52  C, which was more in line with the quality of their
T ( C) Tref ( C) kref  103 (s1) Ea (kJ mol1) R2 RMSD products (fresh fruit and vegetables) and the applied treatment
46–75 61.6 32.1  3.3 170.7  10.2 0.89 0.020 (Jang, 1986; Moss and Chan, 1993; Wang et al., 2002). Increasing the
54–75 64.8 61.2  3.1 102.2  6.2 0.98 0.021 treatment temperature markedly increased the egg mortality rate,
kref and Ea values  confidence interval (P ¼ 0.01). with 100% mortality achieved after 180, 120, 60, 40 and 30 s at
RMSD, root mean square deviation of S(t). temperatures of 54, 60, 65, 70 and 75  C, respectively. However,
a mortality rate of only 46% was obtained after a treatment time of
model were replaced by Eq. (2) and fitted to all the data at once by 1200 s at 46  C. Neven (2000) explains that this mortality is
non-linear regression (TableCurve3DÒ V1.06, Jandel Scientific generally due to physiological and biochemical modifications
Software). This procedure gives much better precision in final (agglutination of proteins associated with different egg constitu-
estimates than first deriving the rate constants and then fitting ents) that occur within the egg during heat treatment – with the
them to the Arrhenius model (Van Boekel, 1996). mortality rate rising as the extent of modifications increases. At low
temperatures (46  C), the survival rate was much higher, even
with long treatment times. Fig. 1 shows the heat flow pattern in
3. Results and discussion eggs measured by DSC over a time-course. This highlights the egg
thermal susceptibility zone. There was a first shift in the curve at
3.1. Effect of temperature on egg survival 50  C for E. kuehniella eggs, reflecting reactions that induce
a physiological modification within the eggs (Neven, 2000). At this
Table 2 gives the survival rate of E. kuehniella eggs according to temperature, the eggs were partially or totally damaged and
the treatment time and temperature. The baseline egg survival rate became opaque as the treatment progressed. This modification,
used for this study was close to 97  2% due to the natural mortality initiated at 50  C, indicated that the eggs had entered the tempo-
of a small proportion of the eggs. The temperatures studied ranged rary stagnation phase. This phase ended when the temperature
from 46 to 75  C because the treatment had no significant impact peaked (Ttrans) at around 63  C. This peak indicated the onset of
below this range, and above 75  C the treatment times were too major chemical reactions. Above Ttrans, there was a permanent

1 1
T =75°C T =60°C

0.5 0.5

0 0
0 60 120 0 60 120

1 1
T =70°C T =54°C
survival rate S(t)

0.5 0.5

0 0
0 60 120 0 60 120

1 1
T =65°C T =46°C

no fit
0.5 0.5

0 0
0 60 120 600 1200
t (s) t (s)
Fig. 3. Experimental and simulated (54–75  C) survival rate of Ephestia kuehniella eggs after t time at several temperatures T. Error bars show the confidence interval (P ¼ 0.01) of
the experimental data.
210 A. Ben-Ialli et al. / Journal of Stored Products Research 45 (2009) 206–211
stagnation phase that was quickly lethal for eggs, with complete
mortality reached within 60 s, as indicated in Table 2 (Vannier,
1987).
3.2. Rate constant determination
The experimental data in Table 2 were used to determine the
rate constant k at each treatment temperature. Although an order
kinetics of around 0.5 is preferred by several authors (Ikediala et al.,
1999; Wang et al., 2001, 2002), a preliminary analysis of our data
showed that 0.5-order kinetics were not suitable for representing
time-course survival rate variations (0.38  R2  0.74) regardless of
the treatment temperature range used (46–75  C). This discrepancy
could be explained by the fact that distinct insect species had been
treated within a higher temperature range. Another drawback of
using 0.5-order kinetics is that they cannot be used for extrapola-
tions since this survival rate pattern does not integrate the long-
term asymptotic trend. We therefore decided to use first-order
kinetics, which are more robust and in line with the observed
trends. Table 3 shows the rate constants. The determination coef-
ficients associated with the different temperatures show that the
first-order kinetics quite accurately reflect (0.91  R2  0.98) the
time-course survival rate pattern, especially for temperatures
54  C (R2  0.95).
3.3. Activation energy
Fig. 2 shows the rate constant variations according to 1/T. Note
that the five data points are aligned between 75 and 54  C, so the
Arrhenius law is thus relevant. However, there seemed to be
a different reaction behaviour at lower temperatures. The activa-
tion energy values determined with or without the low 46  C
temperature are presented in Table 4. We noted that the activation
energy concept was only valid within the 54–75  C temperature
range, with a correlation coefficient of around 0.98. The identified
activation energy was 102.2  6.2 kJ mol1, which is lower than that
determined by Moss and Chan (1993) for eggs of the Caribbean fruit
fly, Anastrepha suspensa (Loew), (Ea ¼ 440–445 kJ mol1 for
37  C  T  50  C) as well as that determined by Wang et al. (2001)
103
t (s)
102
1
10
54 60 65 70
T (°C)
Fig. 4. Simulated times (t) required to reduce the survival rate of Ephestia kuehniella
eggs from 101 to 105 within the 54–75  C temperature (T) range.
for codling moth eggs (Cydia pomonella (L.)) (Ea ¼ 472 kJ mol1 for
46  C  T  52  C). For three fruit fly species (Ceratitis capitata
(Weidemann), Dacus cucurbitae Coquillett, Dacus dorsalis Hendel,
see Table 1), Jang (1986) determined survival activation energies
ranging from 517 to 957 kJ mol1 in a narrow temperature range
with lower temperatures (T  47  C). These activation energy levels
seem to be out of line with an elementary reaction (Van Boekel,
2008). Moreover, with the values determined for the two kinetic
parameters, i.e. kref and Ea 61.2  103 s1 and 102.2 kJ mol1,
respectively, a close fit between the experimental and simulated
survival data was obtained (Fig. 3). Fig. 4 charts the heat treatment
conditions (t, T) required to reduce the egg survival rate from 10 to
0.001%. Hence, the eggs had to be exposed for less than 70 s at 75  C
or 620 s at 54  C to be able to reduce the survival rate to 0.001%.
With this extent of activation energy (102.2  6.2 kJ mol1), a 21  C
increase thus enabled us to reduce the treatment time by tenfold.
This value seemed to be within the same range as the thermo-
sensitivity of nonenzymatic chemical browning reactions (Villota
and Hawkes, 1992), i.e. a deterioration factor for most fruits.
Moreover, so-called ‘high-temperature/short-time’ treatments
seem to be well adapted for limiting fruit degradation during
disinfestation heat treatments.
4. Conclusion
Information on insect egg heat susceptibility thresholds is
essential for developing a heat disinfestation process. In this study,
the E. kuehniella egg survival rate was measured following a water
immersion heat treatment – this procedure was used to avoid egg
dehydration and ensure an almost instantaneous increase in egg
temperature. The data highlighted two different egg behaviours.
Below 50  C, very long treatment times (>60 min) were required to
achieve 100% mortality. However, treatment times were short
(<3 min) at temperatures over 54  C. The DSC measurements
seemed to confirm that there is a critical temperature (around
50  C) at which reactions begin to occur in eggs and affect their
survival. Variations in the time-course of egg survival rate were
accurately represented by first-order kinetics and the Arrhenius
law. The activation energy obtained (102.2  6.2 kJ mol1) revealed
that the treatment time could be reduced tenfold by increasing the
treatment temperature by 21  C. For instance, a 0.01% survival rate
was obtained after a 50 s treatment at 75  C. Lower survival rate
could be obtained (with the same time–temperature profile) if eggs
suffered from dehydration during the heat disinfestation process,
(e.g. using hot air or infrared). Therefore, using these data deter-
mined from water immersion heat treatment guarantees
a minimum rate of disinfestation for all heat disinfestation
processes. This information on egg reactions could be included in
an energy transfer model (conduction, convection, radiation) for
subsequent assessment of the relevance of high-temperature/
short-time treatments for disinfestation, especially of dry products.
Also, associated with a heat transfer model, we could predict and
10-5 optimize by computer modelling the time–temperature profile of
10-4 heat disinfestation processes. An applicable extension of these
10-3 results would be to predict the behaviour of other insects (e.g. date
or carob moth) during heat disinfestation processes: (i) by direct
10-2 testing, (ii) by identification of a new set of kinetics parameters
based on a limited number of experiments or (iii) by reproducing all
the work.
10-1
75
Acknowledgements
We are grateful to Alterbio (Perpignan, France) and AB-med
(Perpignan, France) for their support and funding, as well as the
 A. Ben-Ialli et al. / Journal of Stored Products Research 45 (2009) 206–211
ANRT association (CIFRE) and the TLR service of Languedoc Rous-
sillon region (France).
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