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Surface decontamination of whole-shell eggs using far-infrared radiation
Accepted Manuscript Title: Surface Decontamination of Whole-Shell Eggs Using Far-Infrared Radiation Author: Gunseli ¨ Bobus¸ Alkaya Ferruh Erdogdu A. Kadir Halkman H. Ibrahim Ekiz PII: DOI: Reference:
S0960-3085(16)00032-8 http://dx.doi.org/doi:10.1016/j.fbp.2016.02.006 FBP 689
To appear in:
Food and Bioproducts Processing
Received date: Revised date: Accepted date:
23-10-2015 15-2-2016 23-2-2016
Please cite this article as: Alkaya, G.B., Erdogdu, F., Halkman, A.K., Ekiz, H.I.,Surface Decontamination of Whole-Shell Eggs Using Far-Infrared Radiation, Food and Bioproducts Processing (2016), http://dx.doi.org/10.1016/j.fbp.2016.02.006 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Far-infrared surface decontamination of whole-shell eggs... Highlights: -
Infrared processing for surface pasteurization of whole shell eggs were investigated.
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Surface temperature changes were related with the microbial reduction
Changes in the physical properties of the eggs after infrared processing
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-
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data.
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were investigated.
Applicability of infrared processing for surface pasteurization was
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demonstrated.
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Far-infrared surface decontamination of whole-shell eggs...
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Surface Decontamination of Whole-Shell Eggs Using Far-Infrared Radiation Günseli Bobuş Alkaya1, Ferruh Erdogdu2*,
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M
an
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A. Kadir Halkman2 and H. Ibrahim Ekiz1
Department of Food Engineering
University of Mersin
Department of Food Engineering
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2
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33343 Ciftlikkoy-Mersin, Turkey
Ankara University
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06110 Diskapi-Ankara, Turkey * Corresponding Author e-mail:
[email protected] [email protected]
Tel:
+90-533-812-0686
Fax:
+90-312-317-8711
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Far-infrared surface decontamination of whole-shell eggs...
Abstract Shell eggs from healthy chickens are assumed sterile inside, but numerous microorganisms might be present on the shell. While warm water and controlled
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microwave applications are some common whole egg pasteurization processes, surface decontamination might be a feasible process since majority of
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microorganisms are located over the shell. With infrared application`s direct
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influence on the surface, similar to the case of pulsed light and ultra-violet applications, the objective of this study was to determine its potential for surface
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decontamination of whole-shell eggs. For this purpose, shell eggs were inoculated with E. coli ATCC 25922 strain, considering its similar resistance
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compared to Salmonella Enteritidis to heat, and processed under infrared conditions from 180 to 350 °C. Processing at 250 °C for 110 s resulted in 3.37 log
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cycle reduction without causing any denaturation in albumen and adverse effects
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in yolk index, Haugh unit, albumen pH and foaming capacity. These results demonstrated the potential of infrared heating for surface decontamination of
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whole shell eggs as a possible industrial application. Key words: whole shell eggs; surface decontamination; infrared processing
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Far-infrared surface decontamination of whole-shell eggs...
Introduction Eggs are one of the most important economic and balanced protein source available in daily diet, and 540 billion eggs are consumed in the world annually.
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USDA risk assessment studies indicated the possibility of 1 in 20,000 fresh eggs might contain Salmonella Enteritidis (Mermelstein, 2001), and eggs are reported
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to be most frequently involved with Salmonella outbreaks (Hiero et al., 2009;
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EFSA, 2009; Martelli and Davies, 2012). Salmonella is at the top of the CDC list for foodborne illness estimates resulting deaths in the USA (CDC, 2014). It might be
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inside the eggs (Centers for Disease Control and Prevention, 2005) due to vertical (trans-ovarian transmission in utero to developing pre-ovulatory
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follicles or trans-shell transmission through shell pores; Hou et al., 1996) or horizontal transmission (contamination of shell after it has formed either during
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ovipostion or from environment following the oviposition; Jones et al., 1995;
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Chousalkar et al., 2013). While the latter has higher possibility assuming eggs are obtained from healthier chickens, contamination of eggs and eggshells have been
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identified as one of the major causes of foodborne Salmonella problems (Howard et al., 2012; Whiley and Ross, 2015). Besides the presence of Salmonella over the
shell, possible shell contamination with other aerobic bacteria and Enterobacteriaceae (Jones et al., 2004; Musgrove et al., 2005) is also a possible risk factor. Storage temperature has a certain effect on penetration (Al-Nataour et al., 2012) of the microorganisms to the interior of the eggs, and possible contamination of egg contents might also occur via breaking shell for process purposes through the production line.
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Far-infrared surface decontamination of whole-shell eggs... Various methods have been proposed for egg surface decontamination (FDA, 2009) such as dry cleaning or washing (Hierro et al., 2009; Chousalkar et al., 2013) with alternative approaches for surface pasteurization: ultra-violet irradiation (Scott, 1993; Kuo et al., 1997; De Reu et al., 2006), pulsed light
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treatment (Hierro et al., 2009; Lasagabaster et al., 2011), hot-air application (Manfreda et al., 2010; Pasquali et al., 2010), pulsed ultra-violet light (Keklik et
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al., 2010) and non-thermal atmospheric gas plasma (Ragni et al., 2010). For
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surface decontamination purposes, James et al. (2002) determined the applicability of hot-air, hot-water, infra-red radiation and atmospheric steam
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reporting the requirement of further studies on this subject. Besides surface decontamination approaches, there are also studies in the literature for
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decontamination of the whole shell eggs. Hot-water based heat treatment (Davidson, 2003), irradiation and ultrasonic treatment (Hou et al., 1996) and
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controlled microwave (Erasmus and Rossouw, 2012) are possible methods for
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this purpose. In decontamination of shell eggs, loss of functional properties (foaming, coagulation, emulsification) due to protein denaturation even at low
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temperatures (e.g., below 60 C) might be observed (Perry et al., 2011).
Therefore, considering the higher possibility of horizontal transmission, surface decontamination without any further damages to the egg constituents would be a preferred way.
Infrared (IR) radiation is one of the oldest ways for processing agricultural products. It is classified into near- (NIR; 0.78 to 1.4 μm), mid- (MIR; 1.4 to 3 μm) and far-infrared (FIR; 3 to 1000 μm) regions. Rastogi (2012) emphasized the efficient heat transfer by IR heating with less process time and energy cost while Sawai et al. (2000) demonstrated that the FIR heating was 5 Page 5 of 36
Far-infrared surface decontamination of whole-shell eggs... more effective in eliminating vegetative cells compared to thermal conductive heating. Besides, lower temperature of the emitters in this region, compared to the case of NIR and MIR regions, enables an effective process control. IR processing was applied for surface decontamination of various food products
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including strawberries (Scheerlinck et al., 2004; Tanaka et al., 2007); turkey frankfurtes (Huang, 2004), hotdogs (Huang and Sites, 2007), fig fruit (Hamanaka
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et al., 2011), cumin (Erdogdu and Ekiz, 2011), black pepper (Erdogdu and Ekiz,
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2011), oregano (Eliasson et al., 2014) and Gorgonzola cheese rinds (Bernini et al., 2015).
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Exposing eggs to IR heating results in an increase in shell temperature (due to the shorter wavelength, IR does not have the ability to penetrate deeply),
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and heat is conducted to interior by conduction. With low thermal conductivity (0.55-0.61 W/m-K; Almonacid et al., 2007; Erdogdu et al., 2007; Fabbri et al.,
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2012) and high viscosity of albumen (0.0304 Pa-s; Kemps et al., 2010, e.g, ≈30
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times higher than water), heat transfer rate (mainly dominated by conduction) inside tends to be rather slow compared to the case of a natural convection
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heating in a low viscosity liquid product. If the exposure time is then properly controlled, shell temperature can be preferentially raised to a degree that a target microorganism can be inactivated without substantially increasing the interior temperature.
Therefore, the objectives of this study were to evaluate the potential of IR application for surface decontamination of whole shell eggs and compare the possible changes in the quality attributes of the IR processed eggs with the fresh ones. Materials and Methods 6 Page 6 of 36
Far-infrared surface decontamination of whole-shell eggs... Through the course of this study, commercial grade ‘A’ fresh unfertilized table chicken eggs (medium size, 53-63 g) were purchased from a local market and used through inoculation and IR processing experiments. The eggs were stored in refrigerated conditions through the study and kept at room temperature for
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one night before their use for inoculation and IR processing studies. Based on the given objectives, this study was carried out in 3-stages. In
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the first stage, culture preparation and surface inoculation over the egg shells
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were completed, and this was followed by infrared treatment at various time temperature combinations. In the last stage, certain physical properties (changes
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in yolk index, Haugh unit, albumen pH and foaming capacity) of the IR processed eggs were determined to compare the results with the fresh ones.
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Culture preparation and surface inoculation:
E. coli ATCC 25922 strain, a useful surrogate for E. coli O157:H7, was used to
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determine the IR effect on the surface decontamination of whole shell eggs for
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surface penetration studies. Various studies in the literature also demonstrated that the E. coli ATCC 25922 strain might be used as a surrogate for E. coli
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O157:H7 (Elben et al., 2005; Kim and Harrison, 2009). Hence, E. coli ATCC 25922
strain was used through the culture preparation and shell inoculation stages. To prepare the culture preparation for egg shell inoculation, activated E. coli ATCC 25922 pure culture strain was grown in a 250 ml TSB (Triptic Soy Broth, Merck) at 37 °C for 18 h to have 109 CFU/mL of strain in the culture. This culture was then used in the shell inoculation. For the inoculation, the eggs were weighed and brushed with soap first. After rinsing out with warm water, they were dipped into 70% ethanol for one minute and washed again with sterile and warm water. These eggs were then 7 Page 7 of 36
Far-infrared surface decontamination of whole-shell eggs... located in a sterile laminar air flow cabinet and allowed to dry for 30 min. The shell-dried eggs were then placed in the TSB culture for 10 min under orbital shaking at 200 rpm. Following the inoculation step, the eggs were left to dry for 40 min again in the laminar air flow cabinet prior to the IR processing at various
Far infrared processing for surface decontamination:
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times and temperatures.
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Far infrared processing for surface decontamination was carried out after half an
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hour following the IR heating unit temperature reached to the process
temperature. The infrared heating unit (Fig. 1 demonstrates the schematic
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representation) was designed with flat electrically operated ceramic emitters, of 650 W with maximum surface temperature of 553 °C (Ceramicx, Cork, Ireland)
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working under far-infrared conditions. Under the given temperature range, minimum wavelength obtained from the ceramic emitters was 3.507 µm based
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on the Wien`s displacement law (Eq. 1):
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2897.6 3.507 m 553 273.15
(1)
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Where λ is the wavelength. Considering that the surface temperatures of the heating elements would be lower than the given maximum value, the resulting wavelenghts are expected to be higher falling into the far infrared region. The emitters were installed within aluminum reflectors. Since the
infrared heaters radiated in all directions, they were specifically placed within aluminum reflectors to focus as much of the radiation as possible uniformly onto the processed eggs. This unit consisted of 48 ceramic infrared heaters located on side walls enabling the product inside the tunnel to be heated from all surfaces. To control the process temperature, the infrared unit was assembled with four 8 Page 8 of 36
Far-infrared surface decontamination of whole-shell eggs... thermocouples located between the infrared emitters (2 at the top and 2 at the bottom left and right part of the system – Fig. 1). After setting the process temperature of the system, temperature equilibration was monitored before conducting the experiments.
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During the IR processing experiments, the eggs were placed at the center line of the conveyor belt of the system – right at the centerline of the infrared
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system - for a given time for infrared processing at a given process temperature.
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Far-infrared treatment time and process temperatures were determined in preexperiments based on the initialization of denaturation in egg albumen and
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reported in Table 1. In the pre-experiments, the eggs, processed for various times under the given IR heating conditions, were broken into a Petri dish to
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observe the changes in the albumen and determine the denaturation initialization point. The required maximum process time at a given IR processing
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temperature was then determined based on the visual observation of the initial
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denaturation point in the albumen (Fig. 2). While three inoculated and unprocessed eggs were used as control, three
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eggs were processed for each given time - temperature combination (Table 1). Following the IR process, the eggs were transferred into a beaker, containing 70 mL dilution liquid (0.85 % NaCl + 0.1 % Tween 80) for 10 min. The spread method was used to evaluate the number of surviving E. coli ATCC 25922 cells
where the inoculums were spread by a sterile Drigalski-spatula and inoculated (Hierro et al., 2009; Pasquali et al., 2010; Herigstad et al., 2011; Bote-Salo et al., 2012 and Gole et al., 2014). The colonies were counted following the incubation period.
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Far-infrared surface decontamination of whole-shell eggs... For the IR processed eggs, surface temperature measurement was carried out during processing using an IR camera (FLIR Systems AB, FLIR-I50, Sweden). The temperature measurement was carried out through an observation hole located on top of the unit. The field of view on the shell from the viewing distance
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of 50 cm (from the observation point to the egg surface) was scanned with the IR camera. The IR images provided a partial temperature map of the shell from the
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view angle, and these surface images were processed to determine and report
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the average surface temperature changes of the field of view by using the Flir Quickreport software (V1.2 SP1). In the image analysis, thermal emissivity of the
Changes in the physical properties:
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shells was set to be 0.9 as also applied by Van Brecht et al. (2002).
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Changes in some physical properties (yolk index, Haugh unit, albumen pH and foaming capacity) of the IR processed eggs were determined for the effect of
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temperature on the egg quality as reported by Manfreda et al. (2010). At each
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time-temperature combination, 3 eggs processed, and the results were compared with the case of non-processed eggs. Yolk index (YI), Haugh unit (HU), albumen
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pH and foaming capacity were determined after the IR process. The yolk index was calculated as the height of the yolk divided by the width (Stadelman, 1990), measured with a digital micrometer (Mitutoyo Corp., Absolute digimatic CD15CPX). Albumen pH was measured with a pH meter (Hanna, HI 98103), and Haugh unit was calculated using the empirical equation given by Perry et al. (2011). This equation was based on the height of egg albumen to the mass of the unbroken egg: HU 100 log h 0.01 5.6745 30 m 0..37 100 1.9
(2)
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Far-infrared surface decontamination of whole-shell eggs... Where h is the height of egg albumen and m is mass of unbroken egg. Besides these three quality attributes, change in the foaming capacity of the processed eggs were also demonstrated to indicate the possible effect in the functional properties of the egg proteins. The foaming capacity was determined applying
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the methodology applied by Monfort et al. (2013) where the volume of the egg albumens were measured and 15% solutions were prepared with distilled water.
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These solutions were then whipped with a mixer (Arzum Soprano Max Model
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AR161, max 700W, Turkey) at the max speed in a 1 L beaker for 2 min, and the foam volume was measured with a digital micrometer. The foaming capacity,
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percentage of the increase in the foam volume, was then calculated using the following equation:
V2 V1 100 V1
(3)
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% FC
respectively.
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Where the V1 and V2 were the foam volumes of the initial the whipped solutions,
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While Haugh unit and yolk index were indicators of the egg quality,
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foaming capacity showed its functional property. Any decrease in these values were assumed to be deteriorate to the quality. Perry et al. (2011) also used Haugh unit and yolk index to test quality changes of pasteurized shell eggs with heat and heat-ozone combination during extended storage, and the foaming capacity was recently used by Monfort et al. (2013) to demonstrate the effect of liquid whole egg ultra-pasteurization on the functional properties. The albumen pH was also checked for any significant increase in the pH. Possible pH increase of the egg albumen is temperature dependent and related with CO2, which is linked to the decrease in the in the shelf life.
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Far-infrared surface decontamination of whole-shell eggs... The results for these properties were reported to be the average ± standard deviation. The effect of IR processing on the changes of yolk index, Haugh unit and albumen pH was then analyzed using a single factor ANOVA at 95% confidence interval to compare the control group and processed eggs`
Results and Discussion
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Surface decontamination:
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physical properties at each process temperature.
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E. coli ATCC 25922 strain was used to determine the IR treatment effect on the surface decontamination of the whole shell eggs. Eblen et al. (2005) studied the
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growth and survival characteristics of 15 nonpathogenic generic E. coli strains and one nonpathogenic E. coli O157:H43 strain in five different growth media.
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These strains’ growth and survival characteristics (at 60°C) were reported to be similar to the pathogenic Salmonella and E. coli O157:H7 strains. Among these
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strains, E. coli ATCC 25922 had the most similar thermal - kinetic properties to
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Salmonella and E. coli O157:H7 (Eblen et al., 2005). Kim and Harrison (2009) used non-pathogenic E. coli and pathogenic E. coli O157:H7 strains based on their
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similarities in cryotolerance, cell surface characteristics (hydrophobicity, zeta potential, and morphology) and connection to the lettuce. The results of this study indicated that E. coli ATCC 25922 was a useful surrogate for E. coli O157:H7 for surface penetration studies. Jin et al. (2008) also demonstrated that non-pathogenic E. coli K12 might serve as a surrogate for pathogenic Salmonella Enteritidis in liquid egg for validation of a pasteurization process. Hence, E. coli ATCC 25922 strain was chosen in the current study through the culture preparation and shell inoculation stages. The activated E. coli ATCC 25922 culture density was prepared to have 109 CFU/mL while maximum 12 Page 12 of 36
Far-infrared surface decontamination of whole-shell eggs... loading on the egg shell was 105 CFU/cm2. Pasquali et al. (2010) achieved a similar bacterial load on the shell eggs ranging between 104 and 105 CFU/eggshell. Fig. 3 shows the change in E. coli ATCC 25922 cells by infrared treatment
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from 180 to 350 °C. The infrared treatment at 250 °C for 110 s resulted in the maximum reduction (3.37 log cycle) over the shell while there was no
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denaturation observed in the albumen at the given process times at each IR
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processing temperature. The denaturation start was assumed to be a significant index to conclude the pasteurization process since a partial albumen coagulation
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would be indication of a decay in the egg quality (Fabbri et al., 2012). Start of denaturation in the albumen indicates the conformational changes in the protein
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structure, and the denaturation point for albumen is given by Donovan et al. (1975) in the range of 60 – 65 °C. Other infrared processing conditions at 180°C
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– 200 s; 300 °C – 60 s and 350 °C – 20 s led to log-reductions of 1.63; 2.66 and
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1.7, respectively. Fabrri et al. (2012) also obtained a 1.9 log reduction in the number of S. Enteritidis cells using a hot-air treatment of egg shell surface and
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emphasized that the significance of even this level of reduction without causing any significant changes in the eggs` quality attributes leads to ≈99% decrease in the number of the cells of S. Enteritidis. Fig. 4 shows the average surface average temperature change of the
eggshell during far-infrared processing at 250 and 300 °C (the results were the average of the 3-replicates) while Fig. 5 shows the surface temperature distribution over the egg surface during infrared processing at 250 oC at 110 s and 300 oC at 60 s. Since the highest number of microbial reductions was obtained at these time-temperature combinations, the resulting surface average 13 Page 13 of 36
Far-infrared surface decontamination of whole-shell eggs... temperature change (calculated based on the view angle of the IR camera) was reported. After the infrared processing at 250 °C for 110 s processing, surface average temperature reached just below 60 °C (58.7 °C) while it was just above 60 °C (62.7 °C) at 300 °C – 60 s processing (Fig. 4). The reason that the lower
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reduction was obtained at higher temperature processing was due to the longer processing time at the lower temperature of 250 °C leading to a possible
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temperature uniformity throughout the whole shell surface (Fig. 5).
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As indicated, there was a significant non-homogenous temperature distribution over the shell (Fig. 5). Besides, the overall microbial change
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throughout the shell was reported rather than a certain portion where the infrared temperature image was obtained since the experimental set-up choice
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was preferred to resemble the actual technological process. Scattered results, as also demonstrated in Fig. 3, was the result of the non-homogeneous temperature
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and resulting non-homogeneous microbial reduction distribution.
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If the accumulative effect of temperature to reduce the number of a given microorganism (z- -values for Salmonella Enteritidis strain 13076 and E. coli K12
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in liquid whole egg, reported by Jin et al., 2008, were 4.07 min and 0.17 min, respectively) were calculated based on the temperature increase obtained over the shell (Eq. 3), that would result in 1.32 and 0.39 min of decontamination values for Salmonella Enteritidis and 1.38 and 0.51 min E. coli K12 at the process temperatures of 250 and 300 °C (the reference temperature for these calculations were 60 °C). This would also explain the reason why higher reductions are obtained at a lower process temperature. As indicated above, that is due to the effect of process time – temperature combination, and the higher process time (due to the 14 Page 14 of 36
Far-infrared surface decontamination of whole-shell eggs... earlier start of local denaturation at higher temperatures) at a lower process temperature of 250 °C. This was not the case for the process temperature of 180 °C due to the shorter time and resulting limited increase of the surface temperature. T t Tref z
dt
0
(4)
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t
F 10
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Where Tref (°C)is the reference temperature, T is the average surface
temperature (°C), and z is the z-value (°C), and F might be defined to be the
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decontamination value for this study.
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The applied process time – temperature combination and the evolved temperature over the shell (with increase in the albumen temperature), infrared
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process at 250 °C for 110 s (where the average shell surface temperature was 58.7 °C) did not result in any significant changes in the albumen. As indicated by
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Ramachandran et al. (2011), USDA reported that the minimum temperature without affecting the physical properties of albumen is 55.6 °C with a minimum
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holding time of 6.2 min. This combination resulted in the highest number of
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microbial reductions due to the well-balanced temperature distribution over the shell as explained above. For other IR processing conditions, temperature changes revealed that the
maximum egg surface temperature was almost 50 °C after processing for 200 s at 180 °C leading to 1.63 log cycle reduction. This level of reduction, almost 50% less compared to the case at 250 °C for 110 s, did not account for a proper decontamination condition. Besides, at this low level of reduction, significant albumen denaturation was observed at 200 s due to the local over-heating points through the shell as a result of the longer processing time. The IR surface images 15 Page 15 of 36
Far-infrared surface decontamination of whole-shell eggs... also revealed the non-uniformity in the surface temperature distribution of the eggs processed at higher temperatures. As explained, 3.37 log cycle reduction was obtained under far infrared processing at 250 °C for 110 s. However, as reported by Silva and Gibbs (2012),
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for food products containing poultry, a minimum process resulting in 7 log cycle reduction is suggested for Salmonella by Canadian Food Inspection Agency
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(CFIA, 2005). Besides, USDA risk assessment studies report the possibility of 1 in
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20000 fresh eggs might contain Salmonella Enteritidis (Mermelstein, 2001) leading to the requirement of 5 log cycle reduction. Based on these, IR surface
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treatment might be suggested to be a possible pre-process for an additional pasteurization method to reach 5 to 7 log cycle reduction or a possible
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decontamination technique rather than a proper pasteurization method. In the production of pasteurized liquid egg products, for example, IR decontamination
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methodology might also be a possible pre-process to reduce the risk of
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contamination during shell breaking process and to prevent the violations of the following pasteurization norms. Isolation of Salmonella from ready-to-eat
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pasteurized liquid egg products as a pasteurization-resistant bacteria or due to contamination (Gurtler et al., 2015) also supports this suggestion. Howard et al. (2012) reported the significance of obtaining a possible 3-log
cycle reduction in the number of Salmonella Enteritidis in a decontamination
process. It was stated that this kind of reduction rate might result in 70% decrease in the eventual Salmonella related illnesses. James et al. (2002) also applied IR heating at 210 °C for 30 s on shell egg while the exterior temperature of the shell was reported to be 88 °C with internal surface temperature of 52 °C. There were no visible damage to the shell or no visible denaturation of albumen 16 Page 16 of 36
Far-infrared surface decontamination of whole-shell eggs... observed following this process. As a result, the infrared treatment was theoretically be justified to reduce a certain number of microorganisms on the shell eggs without causing changes on albumen and other quality factors. There have been various studies to reduce the Salmonella Enteritidis on shell eggs
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(Stadelman et al. 1996; Hou et al. 1996; Pasquali et al. 2010; James et al. 2002), and heat treatments are reported to be the mostly used processes even though
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there might be possible quality losses in egg components especially due to egg
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albumen denaturation observed at rather lower temperatures of less than 60 °C (Hou et al., 1996). Pasquali et al. (2010) also used a hot air apparatus to
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pasteurize the shell eggs with the initial loads of 104 to 105 CFU/egg-shell. Two shots of hot air at 600 °C for 8 s with a 30 s cold air break were applied, and 1.9
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log cycle reduction in the number of Salmonella Enteritidis was obtained with no significant quality changes. They have also indicated the significance of 1 log
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cycle reduction due to the corresponding foodborne risk reduction of Salmonella
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Enteritidis for human health. Stolz et al. (2015) also obtained 2.4 log cycle of reduction, conforming 99.6% of the initial Salmonella Enteritidis population
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using non-thermal atmospheric plasma. The given conclusion with the maximum 3.37 log cycle reduction obtained
at 250 °C for 110 s was reported based on the results where the IR exposure time was determined not to affect the initial denaturation in the egg albumin. It is expected and the pre-experiments also demostrated that the further increase of the exposure at the given maximum process times (Table 1) would give a start in the albumin denaturation. However, it might be possible to apply a variable process temperatures to eliminate the initialization of the denaturation while increasing the effect of IR temperature to lead to at least 5-log cycle reductions 17 Page 17 of 36
Far-infrared surface decontamination of whole-shell eggs... for surface pasteurization purposes without affecting the physical properties of the egg constituents. Changes in the physical properties: Table 2 reports the changes in the physical properties of the infrared processed
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and control group eggs. Regarding the comparison between control group and processed eggs` physical properties at each process temperature, a single factor
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ANOVA test was applied at 95% confidence intervals to determine any
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significant effect of processing time. There were no significant differences determined (p>0.05) as a function of processing time at a given process
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temperature even though standard deviation of the foaming capacity values with respect to the average changed in a significant matter. The differences among the
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IR temperatures were not tested since the objective was just to determine whether the processed temperature had any significant on a quality parameter.
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Besides these physical properties, there were also no mass losses observed
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during the IR processing.
Conclusions
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External contamination of egg shell by Salmonella and Enterobacteriaceae is a major concern in industry as a health hazard. Besides the effects on health issues, [resence of these microorganisms might even violate the pasteurization norms in the production of, for example, pasteurized liqud egg. In this study, IR application was demonstrated to be a feasible process for surface decontamination of shell eggs with its major advantage of directly influencing the surface. Processing at 250 °C for 110 s resulted in 3.37 log cycle reduction of E. coli ATCC 25922 strain (used in the experimental methodology as a surrogate for Salmonella Enteritidis)
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Far-infrared surface decontamination of whole-shell eggs... without causing any denaturation in albumen and adverse effects in yolk index, Haugh unit, albumen pH and foaming capacity. Further optimization studies are suggested for proper design of an infrared processing system to obtain a uniform temperature and heat flux distribution through the surface of the eggs for an
Acknowledgement
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effective heat transfer.
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The authors gratefully acknowledge the Scientific Research Foundation,
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University of Mersin, Turkey for supporting this project (Project No: 2015-TP31164). Besides, upon the start of this study, Dr. Erdogdu was also affiliated with
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the Department of Food Engineering at the University of Mersin.
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Far-infrared surface decontamination of whole-shell eggs...
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Botey-Salo, P., Anyogu, A., Varnam, A.H. and Sutherland, J. P. 2012. Survival of
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inoculated Salmonella on the shell of hens’ eggs and its potential
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activity, color and volatile compounds. Journal of Food Science. 79: E2447-
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Huang, L. 2004. Infrared surface pasteurization of turkey frankfurters. Innovative Food Science and Emerging technolgoies. 5: 345-351.
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Huang, L. and Sites, J. 2007. Elimination of Listeria monosytogenes on hotdogs by infrared surface treatment. Journal of Food Science. 73: M27-M31.
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James, C., Lechevalier, V. and Ketteringham, L. 2002. Surface pasteurization of shell eggs, Journal of Food engineering. 53:193-197.
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Jin, T., Zhang, H., Boyd, G. and Tang, J. 2008. Thermal resistance of Salmonella
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Jones, F.T., Rives, D.V. and Carey, J.B. 1995. Salmonella contamination in commercial eggs and egg production facility. Poultry Science. 74: 753-757.
Jones, D.R., Musgrove, M.T. and Northcutt, J.K. 2004. Variations in external and internal microbial populations of shell eggs during extended storage. Journal of Food Protection. 67: 2657-2660. Keklik, N.M., Demirci, A., Patterson, P.H. and Puri, V.M. 2010. Pulsed UV light inactivation of Salmonella Enteritidis on eggshells and its effects on egg quality. Journal of Food Protection. 8: 1408-1590.
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Far-infrared surface decontamination of whole-shell eggs... Kemps, B.J., Bamelis, F.R>, Mertens, K., Decuypere, E.M., De Baerdemaeker, J.G. and De Ketalaere, B. 2010. The assessment of viscosity measurements on the albumen of consumption eggs as an indicator for freshness. Poultry Science. 89: 2699-2703.
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Kim, J.K. and Harrison, M.A. 2009. Surrogate selection for Escherichia coli O157:H7 based on cryotolerance and attachment to romaine lettuce.
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Kuo, F-L., Carey, J.B. and Ricke, S.C. 1997. UV irradiation of shell eggs: effect on populations of aerobes, molds and inoculated Salmonella typhimurium.
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Lasagabaster, A., Arboleya, J.C., de maranon, I.M. 2011. Pulsed light technology
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for surface decontamination of eggs: impact on salmonella inactivation and
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egg quality. Innovative Food Science and Emerging Technologies. 12: 124-
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Manfreda, G., Cevoli, C., Lucchi, A., Pasquali, F., Fabbri, A. and Franchini, A. 2010. Hot air treatment for surface decontamination of table eggs incfected with
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Salmonella, Literia and Escherichia coli. Veterinary Research Communications. 34 (Supplement 1): S179-S182.
Martelli, F. and Davies, R.H. 2012. Salmonella serovars isolated from table eggs: an overview. Food Research International. 45: 745-754.
Mermelstein, N.H. 2001. Pasteurization of shell eggs. Food Technology. 55(12): 72-73, 79. Monfort, S., Sagarzazu, N., Condon, S., Raso, J. and Alvarez, I. 2013. Liquid whole egg ultrapasteurization by combination of PEF, heat and additives. Food and Bioprocess Technology. 6: 2070-2080. 24 Page 24 of 36
Far-infrared surface decontamination of whole-shell eggs... Musgrove, M.T., Jones, D.R., Northcutt, J.K., Cox, N.A. and Harrison, M.A. 2005. Shell rinse and shell crush methods for the recovery of aerobic microorganisms and Enterobacteriaceae from shell eggs. Journal of Food Protection. 68: 2144-2148.
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Pasquali, F., Fabbri, A., Cevoli, C., Manfreda, G. and Franchini, A. 2010. Hot air treatment for surface decontamination of table eggs. Food Control. 21:431-
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Perry, J.J., Rodriguez-Saona, L.E. and Yousef, A.E. 2011. Quality of shell eggs pasteurized with heat or heat-ozone combination during extended storage.
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Ragni, L., Berardinelli, A., Vannini, L., Montanari, C., Sirri, F., Guerzoni, M.E. and
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Guarnieri, A. 2010. Non-thermal atmospheric gas plasma device for surface decontamination of shell eggs. Journal of Food Engineering. 100: 125-132.
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Ramachandran, R., Malhotra, D., Anishaparvin, A. and Anandharamakrishnan, C.
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2011. Computational fluid dynamic simulation studies on pasteurization of egg in stationary and rotation modes. Innovative Food Science and
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Emerging Technologies. 12: 38-44.
Rastogi, N.K. 2012. Recent trends and developments in infrared heating in food processing. Critical Reviews in Food Science and Nutrition. 52: 737-760.
Sawai, J., Sagara, K., Kasai, S., Igarashi, H., Hashimoto, A., Kokugan, T., Shimizu, M. and Kojima, H. 2000. Far-infrared irradiation-induced injuries to Escherichia coli at below the lethal temperature. Journal of Industrial Microbiology and Biotechnology. 24: 19-24.
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Far-infrared surface decontamination of whole-shell eggs... Scheerlinck, N., Marquenie, D., Jancsok, P.T., Verboven, P., Moles, C.G., Banga, J.R. and Nicolai, B.M. 2004. A model-based approach to develop periodic thermal treatments for surface decontamination of strawberries. 34: 39-52. Scott, T.A. 1993. The effect of UV-light and air filtering system on embryo
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viability and microorganism load on the egg shell. Journal of Applied Poultry research. 2: 19-25.
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Stadelman, W.J. 1990. Quality identification of shell eggs. In Egg Science and
Haworth Publishing Co., Binghamton, N.Y.
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Technolgy (Eds. Stadelman, W.J. and Cotterill, O.J.). 3rd ed. Pp. 37-61.
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Stadelman, W.J., Singh, R.K., Muriana, P.M. ve Hou, H. 1996. Pasteurization of eggs in the shell. Poultry Science. 75: 1122-1125.
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Stolz, N., Weihe, T., Stachowiak, J., Braun, P., Schluter, O. and Ehlbeck, J. 2015. Decontamination of shell eggs by using non-thermal atmospheric pressure
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plasma. 15th International Conference on Biomedical Engineering and
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Technology (ICBET 2015). 81: 81-84. Tanaka, F., Verboven, P., Scheerlinck, N., Morita, K., Iwasaki, K. and Nicolai, B.
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2007. Investigation of far infrared radiation heating as an alternative technique for surface decontamination of strawberry. 79” 445-452.
Van Brecht, A., Aerts, J.M. Degraeve, P. and Berckmans, D. 2002. Quantification of the spatio-temporal eggshell temperature and convection coefficient by infrared thermography. Transactions of the ASAE. 45: 1951-1957. Whiley, H. and Ross, K. 2015. Salmonella and eggs: from production to plate. International Journal of Environmental Research and Public Health. 12: 2543-2556.
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Far-infrared surface decontamination of whole-shell eggs... Zhang, W., Zheng, J-X. and Xu, G-Y. 2011. Toward better control of Salmonella contamination by taking advantage of the egg`s self-defense system: a
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pt
ed
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an
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review. Journal of Food Science. 76: R76-R81.
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Far-infrared surface decontamination of whole-shell eggs...
Figure Captions: Figure 1. A schematic representation of the infrared processing unit (the lengths are reported in cm).
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Figure 2. Demonstration of the denaturation initialization in the egg albumen. Figure 3. The decrease in the number of E.coli ATCC25922 cells by infrared
treatment (a) 180 ˚C – 200 s (b) 250 ˚C – 110 s (c) 300 ˚C – 60 s and
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(d) 350 ˚C – 20 s.
Figure 4. Surface average temperature change (calculated based on the view processing at 250 and 300 ˚C.
Surface temperature images of the shell eggs infrared processed at (a)
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Figure 5.
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angle of the IR camera) of the egg shells during far infrared
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pt
ed
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250 ˚C for 90 s (b) 300 ˚C for 60 s.
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Far-infrared surface decontamination of whole-shell eggs... Table 1. Experimental conditions for far infrared treatment time and temperatures. Process time (s)
180
0 – 120 – 150 – 180 - 200
250
0 - 30 - 60 - 90 - 100 - 110
300
0 – 30 – 45 - 60
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Infrared process temperature (oC)
350
0 – 5* - 10 – 15* - 20
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* This data were only used in the microbiological analysis results to observe the decreasing trend.
29 Page 29 of 36
Far-infrared surface decontamination of whole-shell eggs...
Table 2. Effect of infrared processing time – temperature on yolk index, haugh unit and albumen pH. Foaming Capacity (%)
Control
9.43 ± 0.05
0.27 ± 0.03
48.5 ± 7.7
111.5 ± 19.1
120
9.35 ± 0.01
0.24 ± 0.02
37.4 ± 17.9
126..6 ± 30.5
150
9.41 ± 0.13
0.26 ± 0.03
31.6 ± 1.4
123.0 ± 13.6
180
9.47 ± 0.06
0.24 ± 0.02
44.7 ± 12.0
99.1 ± 13.6
200
9.34 ± 0.08
0.28 ± 0.05
59.6 ± 17.4
91.7 ± 29.9
Control
9.16 ± 0.04
0.37 ± 0.03
72.5 ± 6.5
111.5 ± 19.1
30
9.29 ± 0.04
0.32 ± 0.04
61.3 ± 10.0
110.0 ± 31.4
60
9.32 ± 0.02
90
9.23 ± 0.17
100
9.12 ± 0.09
110
9.07 ± 0.16
350 °C
an
us
cr
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Haugh Unit
0.33 ± 0.03
62.6 ± 2.4
93.8 ± 18.9
0.34 ± 0.01
59.1 ± 14.4
100.3 ± 7.8
0.34 ± 0.01
60.9 ± 8.1
131.0 ± 26.4
0.36 ± 0.03
71.7 ± 8.1
130.6 ± 10.8
Control
9.43 ± 0.05
0.27 ± 0.02
56.8 ± 10.4
111.5 ± 19.1
30
9.46 ± 0.21
0.30 ± 0.04
60.1 ± 12.0
147.1 ± 27.1
45
9.39 ± 0.14
0.33 ± 0.03
57.1 ± 5.1
113.8 ± 15.2
60
9.20 ± 0.24
0.34 ± 0.03
69.0 ± 5.7
119.2 ± 45.8
Control
9.43 ± 0.05
0.27 ± 0.02
56.8 ± 10.4
10
9.45 ± 0.05
0.23 ± 0.01
41.9 ± 11.3
20
9.39 ± 0.32
0.29 ± 0.04
63.2 ± 4.8
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300 °C
Yolk Index
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250 °C
Albumen pH
ed
180 °C
Process time (s)
pt
Infrared process temperature
-
30 Page 30 of 36
d
M
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us
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Far-infrared surface decontamination of whole-shell eggs...
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te
Figure 1. A schematic representation of the infrared processing unit (the lengths are reported in cm).
Page 31 of 36
te
d
M
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Far-infrared surface decontamination of whole-shell eggs...
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Figure 2. Demonstration of the denaturation initialization in the egg albumen.
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4.5 4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 0.0 50
200
250
(a)
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7.0 6.0
d
5.0 4.0
te
Log (N)
100 150 Process Time (s)
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0
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Log (N)
Far-infrared surface decontamination of whole-shell eggs...
3.0
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2.0 1.0 0.0
0
20
40
60 80 Process Time (s)
100
120
(b)
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Far-infrared surface decontamination of whole-shell eggs...
7.0 6.0
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4.0
3.0
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Log (N)
5.0
2.0
us
1.0 0.0 20
6.0
50
60
70
(c)
d
5.0
te
4.0 3.0
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Log (N)
30 40 Process Time (s)
an
10
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0
2.0 1.0 0.0
0
5
10 15 Process Time (s)
20
25 (d)
Figure 3. The decrease in the number of E.coli ATCC25922 cells by infrared treatment (a) 180 ˚C – 200 s (b) 250 ˚C – 110 s (c) 300 ˚C – 60 s and (d) 350 ˚C – 20 s.
Page 34 of 36
Far-infrared surface decontamination of whole-shell eggs...
60
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50
40
250 °C
30
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300 °C
20 10 0 0
20
40
60
80
100
120
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an
Process Time (s)
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Average Surface Temperature (°C)
70
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te
d
Figure 4. Surface average temperature change of egg shell during far infrared processing at 250 and 300 ˚C.
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(a)
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te
d
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Far-infrared surface decontamination of whole-shell eggs...
(b)
Figure 5. Surface temperature images of the shell eggs infrared processed at (a) 250 ˚C for 90 s (b) 300 ˚C for 60 s.
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S0960-3085(16)00032-8 http://dx.doi.org/doi:10.1016/j.fbp.2016.02.006 FBP 689
To appear in:
Food and Bioproducts Processing
Received date: Revised date: Accepted date:
23-10-2015 15-2-2016 23-2-2016
Please cite this article as: Alkaya, G.B., Erdogdu, F., Halkman, A.K., Ekiz, H.I.,Surface Decontamination of Whole-Shell Eggs Using Far-Infrared Radiation, Food and Bioproducts Processing (2016), http://dx.doi.org/10.1016/j.fbp.2016.02.006 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Far-infrared surface decontamination of whole-shell eggs... Highlights: -
Infrared processing for surface pasteurization of whole shell eggs were investigated.
-
Surface temperature changes were related with the microbial reduction
Changes in the physical properties of the eggs after infrared processing
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-
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data.
-
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were investigated.
Applicability of infrared processing for surface pasteurization was
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pt
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demonstrated.
1 Page 1 of 36
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Far-infrared surface decontamination of whole-shell eggs...
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Surface Decontamination of Whole-Shell Eggs Using Far-Infrared Radiation Günseli Bobuş Alkaya1, Ferruh Erdogdu2*,
1
M
an
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A. Kadir Halkman2 and H. Ibrahim Ekiz1
Department of Food Engineering
University of Mersin
Department of Food Engineering
pt
2
ed
33343 Ciftlikkoy-Mersin, Turkey
Ankara University
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06110 Diskapi-Ankara, Turkey * Corresponding Author e-mail:
[email protected] [email protected]
Tel:
+90-533-812-0686
Fax:
+90-312-317-8711
2 Page 2 of 36
Far-infrared surface decontamination of whole-shell eggs...
Abstract Shell eggs from healthy chickens are assumed sterile inside, but numerous microorganisms might be present on the shell. While warm water and controlled
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microwave applications are some common whole egg pasteurization processes, surface decontamination might be a feasible process since majority of
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microorganisms are located over the shell. With infrared application`s direct
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influence on the surface, similar to the case of pulsed light and ultra-violet applications, the objective of this study was to determine its potential for surface
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decontamination of whole-shell eggs. For this purpose, shell eggs were inoculated with E. coli ATCC 25922 strain, considering its similar resistance
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compared to Salmonella Enteritidis to heat, and processed under infrared conditions from 180 to 350 °C. Processing at 250 °C for 110 s resulted in 3.37 log
ed
cycle reduction without causing any denaturation in albumen and adverse effects
pt
in yolk index, Haugh unit, albumen pH and foaming capacity. These results demonstrated the potential of infrared heating for surface decontamination of
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whole shell eggs as a possible industrial application. Key words: whole shell eggs; surface decontamination; infrared processing
3 Page 3 of 36
Far-infrared surface decontamination of whole-shell eggs...
Introduction Eggs are one of the most important economic and balanced protein source available in daily diet, and 540 billion eggs are consumed in the world annually.
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USDA risk assessment studies indicated the possibility of 1 in 20,000 fresh eggs might contain Salmonella Enteritidis (Mermelstein, 2001), and eggs are reported
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to be most frequently involved with Salmonella outbreaks (Hiero et al., 2009;
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EFSA, 2009; Martelli and Davies, 2012). Salmonella is at the top of the CDC list for foodborne illness estimates resulting deaths in the USA (CDC, 2014). It might be
an
inside the eggs (Centers for Disease Control and Prevention, 2005) due to vertical (trans-ovarian transmission in utero to developing pre-ovulatory
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follicles or trans-shell transmission through shell pores; Hou et al., 1996) or horizontal transmission (contamination of shell after it has formed either during
ed
ovipostion or from environment following the oviposition; Jones et al., 1995;
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Chousalkar et al., 2013). While the latter has higher possibility assuming eggs are obtained from healthier chickens, contamination of eggs and eggshells have been
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identified as one of the major causes of foodborne Salmonella problems (Howard et al., 2012; Whiley and Ross, 2015). Besides the presence of Salmonella over the
shell, possible shell contamination with other aerobic bacteria and Enterobacteriaceae (Jones et al., 2004; Musgrove et al., 2005) is also a possible risk factor. Storage temperature has a certain effect on penetration (Al-Nataour et al., 2012) of the microorganisms to the interior of the eggs, and possible contamination of egg contents might also occur via breaking shell for process purposes through the production line.
4 Page 4 of 36
Far-infrared surface decontamination of whole-shell eggs... Various methods have been proposed for egg surface decontamination (FDA, 2009) such as dry cleaning or washing (Hierro et al., 2009; Chousalkar et al., 2013) with alternative approaches for surface pasteurization: ultra-violet irradiation (Scott, 1993; Kuo et al., 1997; De Reu et al., 2006), pulsed light
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treatment (Hierro et al., 2009; Lasagabaster et al., 2011), hot-air application (Manfreda et al., 2010; Pasquali et al., 2010), pulsed ultra-violet light (Keklik et
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al., 2010) and non-thermal atmospheric gas plasma (Ragni et al., 2010). For
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surface decontamination purposes, James et al. (2002) determined the applicability of hot-air, hot-water, infra-red radiation and atmospheric steam
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reporting the requirement of further studies on this subject. Besides surface decontamination approaches, there are also studies in the literature for
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decontamination of the whole shell eggs. Hot-water based heat treatment (Davidson, 2003), irradiation and ultrasonic treatment (Hou et al., 1996) and
ed
controlled microwave (Erasmus and Rossouw, 2012) are possible methods for
pt
this purpose. In decontamination of shell eggs, loss of functional properties (foaming, coagulation, emulsification) due to protein denaturation even at low
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temperatures (e.g., below 60 C) might be observed (Perry et al., 2011).
Therefore, considering the higher possibility of horizontal transmission, surface decontamination without any further damages to the egg constituents would be a preferred way.
Infrared (IR) radiation is one of the oldest ways for processing agricultural products. It is classified into near- (NIR; 0.78 to 1.4 μm), mid- (MIR; 1.4 to 3 μm) and far-infrared (FIR; 3 to 1000 μm) regions. Rastogi (2012) emphasized the efficient heat transfer by IR heating with less process time and energy cost while Sawai et al. (2000) demonstrated that the FIR heating was 5 Page 5 of 36
Far-infrared surface decontamination of whole-shell eggs... more effective in eliminating vegetative cells compared to thermal conductive heating. Besides, lower temperature of the emitters in this region, compared to the case of NIR and MIR regions, enables an effective process control. IR processing was applied for surface decontamination of various food products
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including strawberries (Scheerlinck et al., 2004; Tanaka et al., 2007); turkey frankfurtes (Huang, 2004), hotdogs (Huang and Sites, 2007), fig fruit (Hamanaka
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et al., 2011), cumin (Erdogdu and Ekiz, 2011), black pepper (Erdogdu and Ekiz,
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2011), oregano (Eliasson et al., 2014) and Gorgonzola cheese rinds (Bernini et al., 2015).
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Exposing eggs to IR heating results in an increase in shell temperature (due to the shorter wavelength, IR does not have the ability to penetrate deeply),
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and heat is conducted to interior by conduction. With low thermal conductivity (0.55-0.61 W/m-K; Almonacid et al., 2007; Erdogdu et al., 2007; Fabbri et al.,
ed
2012) and high viscosity of albumen (0.0304 Pa-s; Kemps et al., 2010, e.g, ≈30
pt
times higher than water), heat transfer rate (mainly dominated by conduction) inside tends to be rather slow compared to the case of a natural convection
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heating in a low viscosity liquid product. If the exposure time is then properly controlled, shell temperature can be preferentially raised to a degree that a target microorganism can be inactivated without substantially increasing the interior temperature.
Therefore, the objectives of this study were to evaluate the potential of IR application for surface decontamination of whole shell eggs and compare the possible changes in the quality attributes of the IR processed eggs with the fresh ones. Materials and Methods 6 Page 6 of 36
Far-infrared surface decontamination of whole-shell eggs... Through the course of this study, commercial grade ‘A’ fresh unfertilized table chicken eggs (medium size, 53-63 g) were purchased from a local market and used through inoculation and IR processing experiments. The eggs were stored in refrigerated conditions through the study and kept at room temperature for
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one night before their use for inoculation and IR processing studies. Based on the given objectives, this study was carried out in 3-stages. In
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the first stage, culture preparation and surface inoculation over the egg shells
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were completed, and this was followed by infrared treatment at various time temperature combinations. In the last stage, certain physical properties (changes
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in yolk index, Haugh unit, albumen pH and foaming capacity) of the IR processed eggs were determined to compare the results with the fresh ones.
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Culture preparation and surface inoculation:
E. coli ATCC 25922 strain, a useful surrogate for E. coli O157:H7, was used to
ed
determine the IR effect on the surface decontamination of whole shell eggs for
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surface penetration studies. Various studies in the literature also demonstrated that the E. coli ATCC 25922 strain might be used as a surrogate for E. coli
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O157:H7 (Elben et al., 2005; Kim and Harrison, 2009). Hence, E. coli ATCC 25922
strain was used through the culture preparation and shell inoculation stages. To prepare the culture preparation for egg shell inoculation, activated E. coli ATCC 25922 pure culture strain was grown in a 250 ml TSB (Triptic Soy Broth, Merck) at 37 °C for 18 h to have 109 CFU/mL of strain in the culture. This culture was then used in the shell inoculation. For the inoculation, the eggs were weighed and brushed with soap first. After rinsing out with warm water, they were dipped into 70% ethanol for one minute and washed again with sterile and warm water. These eggs were then 7 Page 7 of 36
Far-infrared surface decontamination of whole-shell eggs... located in a sterile laminar air flow cabinet and allowed to dry for 30 min. The shell-dried eggs were then placed in the TSB culture for 10 min under orbital shaking at 200 rpm. Following the inoculation step, the eggs were left to dry for 40 min again in the laminar air flow cabinet prior to the IR processing at various
Far infrared processing for surface decontamination:
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times and temperatures.
cr
Far infrared processing for surface decontamination was carried out after half an
us
hour following the IR heating unit temperature reached to the process
temperature. The infrared heating unit (Fig. 1 demonstrates the schematic
an
representation) was designed with flat electrically operated ceramic emitters, of 650 W with maximum surface temperature of 553 °C (Ceramicx, Cork, Ireland)
M
working under far-infrared conditions. Under the given temperature range, minimum wavelength obtained from the ceramic emitters was 3.507 µm based
ed
on the Wien`s displacement law (Eq. 1):
pt
2897.6 3.507 m 553 273.15
(1)
Ac ce
Where λ is the wavelength. Considering that the surface temperatures of the heating elements would be lower than the given maximum value, the resulting wavelenghts are expected to be higher falling into the far infrared region. The emitters were installed within aluminum reflectors. Since the
infrared heaters radiated in all directions, they were specifically placed within aluminum reflectors to focus as much of the radiation as possible uniformly onto the processed eggs. This unit consisted of 48 ceramic infrared heaters located on side walls enabling the product inside the tunnel to be heated from all surfaces. To control the process temperature, the infrared unit was assembled with four 8 Page 8 of 36
Far-infrared surface decontamination of whole-shell eggs... thermocouples located between the infrared emitters (2 at the top and 2 at the bottom left and right part of the system – Fig. 1). After setting the process temperature of the system, temperature equilibration was monitored before conducting the experiments.
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During the IR processing experiments, the eggs were placed at the center line of the conveyor belt of the system – right at the centerline of the infrared
cr
system - for a given time for infrared processing at a given process temperature.
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Far-infrared treatment time and process temperatures were determined in preexperiments based on the initialization of denaturation in egg albumen and
an
reported in Table 1. In the pre-experiments, the eggs, processed for various times under the given IR heating conditions, were broken into a Petri dish to
M
observe the changes in the albumen and determine the denaturation initialization point. The required maximum process time at a given IR processing
ed
temperature was then determined based on the visual observation of the initial
pt
denaturation point in the albumen (Fig. 2). While three inoculated and unprocessed eggs were used as control, three
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eggs were processed for each given time - temperature combination (Table 1). Following the IR process, the eggs were transferred into a beaker, containing 70 mL dilution liquid (0.85 % NaCl + 0.1 % Tween 80) for 10 min. The spread method was used to evaluate the number of surviving E. coli ATCC 25922 cells
where the inoculums were spread by a sterile Drigalski-spatula and inoculated (Hierro et al., 2009; Pasquali et al., 2010; Herigstad et al., 2011; Bote-Salo et al., 2012 and Gole et al., 2014). The colonies were counted following the incubation period.
9 Page 9 of 36
Far-infrared surface decontamination of whole-shell eggs... For the IR processed eggs, surface temperature measurement was carried out during processing using an IR camera (FLIR Systems AB, FLIR-I50, Sweden). The temperature measurement was carried out through an observation hole located on top of the unit. The field of view on the shell from the viewing distance
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of 50 cm (from the observation point to the egg surface) was scanned with the IR camera. The IR images provided a partial temperature map of the shell from the
cr
view angle, and these surface images were processed to determine and report
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the average surface temperature changes of the field of view by using the Flir Quickreport software (V1.2 SP1). In the image analysis, thermal emissivity of the
Changes in the physical properties:
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shells was set to be 0.9 as also applied by Van Brecht et al. (2002).
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Changes in some physical properties (yolk index, Haugh unit, albumen pH and foaming capacity) of the IR processed eggs were determined for the effect of
ed
temperature on the egg quality as reported by Manfreda et al. (2010). At each
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time-temperature combination, 3 eggs processed, and the results were compared with the case of non-processed eggs. Yolk index (YI), Haugh unit (HU), albumen
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pH and foaming capacity were determined after the IR process. The yolk index was calculated as the height of the yolk divided by the width (Stadelman, 1990), measured with a digital micrometer (Mitutoyo Corp., Absolute digimatic CD15CPX). Albumen pH was measured with a pH meter (Hanna, HI 98103), and Haugh unit was calculated using the empirical equation given by Perry et al. (2011). This equation was based on the height of egg albumen to the mass of the unbroken egg: HU 100 log h 0.01 5.6745 30 m 0..37 100 1.9
(2)
10 Page 10 of 36
Far-infrared surface decontamination of whole-shell eggs... Where h is the height of egg albumen and m is mass of unbroken egg. Besides these three quality attributes, change in the foaming capacity of the processed eggs were also demonstrated to indicate the possible effect in the functional properties of the egg proteins. The foaming capacity was determined applying
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the methodology applied by Monfort et al. (2013) where the volume of the egg albumens were measured and 15% solutions were prepared with distilled water.
cr
These solutions were then whipped with a mixer (Arzum Soprano Max Model
us
AR161, max 700W, Turkey) at the max speed in a 1 L beaker for 2 min, and the foam volume was measured with a digital micrometer. The foaming capacity,
an
percentage of the increase in the foam volume, was then calculated using the following equation:
V2 V1 100 V1
(3)
M
% FC
respectively.
ed
Where the V1 and V2 were the foam volumes of the initial the whipped solutions,
pt
While Haugh unit and yolk index were indicators of the egg quality,
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foaming capacity showed its functional property. Any decrease in these values were assumed to be deteriorate to the quality. Perry et al. (2011) also used Haugh unit and yolk index to test quality changes of pasteurized shell eggs with heat and heat-ozone combination during extended storage, and the foaming capacity was recently used by Monfort et al. (2013) to demonstrate the effect of liquid whole egg ultra-pasteurization on the functional properties. The albumen pH was also checked for any significant increase in the pH. Possible pH increase of the egg albumen is temperature dependent and related with CO2, which is linked to the decrease in the in the shelf life.
11 Page 11 of 36
Far-infrared surface decontamination of whole-shell eggs... The results for these properties were reported to be the average ± standard deviation. The effect of IR processing on the changes of yolk index, Haugh unit and albumen pH was then analyzed using a single factor ANOVA at 95% confidence interval to compare the control group and processed eggs`
Results and Discussion
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Surface decontamination:
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physical properties at each process temperature.
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E. coli ATCC 25922 strain was used to determine the IR treatment effect on the surface decontamination of the whole shell eggs. Eblen et al. (2005) studied the
an
growth and survival characteristics of 15 nonpathogenic generic E. coli strains and one nonpathogenic E. coli O157:H43 strain in five different growth media.
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These strains’ growth and survival characteristics (at 60°C) were reported to be similar to the pathogenic Salmonella and E. coli O157:H7 strains. Among these
ed
strains, E. coli ATCC 25922 had the most similar thermal - kinetic properties to
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Salmonella and E. coli O157:H7 (Eblen et al., 2005). Kim and Harrison (2009) used non-pathogenic E. coli and pathogenic E. coli O157:H7 strains based on their
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similarities in cryotolerance, cell surface characteristics (hydrophobicity, zeta potential, and morphology) and connection to the lettuce. The results of this study indicated that E. coli ATCC 25922 was a useful surrogate for E. coli O157:H7 for surface penetration studies. Jin et al. (2008) also demonstrated that non-pathogenic E. coli K12 might serve as a surrogate for pathogenic Salmonella Enteritidis in liquid egg for validation of a pasteurization process. Hence, E. coli ATCC 25922 strain was chosen in the current study through the culture preparation and shell inoculation stages. The activated E. coli ATCC 25922 culture density was prepared to have 109 CFU/mL while maximum 12 Page 12 of 36
Far-infrared surface decontamination of whole-shell eggs... loading on the egg shell was 105 CFU/cm2. Pasquali et al. (2010) achieved a similar bacterial load on the shell eggs ranging between 104 and 105 CFU/eggshell. Fig. 3 shows the change in E. coli ATCC 25922 cells by infrared treatment
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from 180 to 350 °C. The infrared treatment at 250 °C for 110 s resulted in the maximum reduction (3.37 log cycle) over the shell while there was no
cr
denaturation observed in the albumen at the given process times at each IR
us
processing temperature. The denaturation start was assumed to be a significant index to conclude the pasteurization process since a partial albumen coagulation
an
would be indication of a decay in the egg quality (Fabbri et al., 2012). Start of denaturation in the albumen indicates the conformational changes in the protein
M
structure, and the denaturation point for albumen is given by Donovan et al. (1975) in the range of 60 – 65 °C. Other infrared processing conditions at 180°C
ed
– 200 s; 300 °C – 60 s and 350 °C – 20 s led to log-reductions of 1.63; 2.66 and
pt
1.7, respectively. Fabrri et al. (2012) also obtained a 1.9 log reduction in the number of S. Enteritidis cells using a hot-air treatment of egg shell surface and
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emphasized that the significance of even this level of reduction without causing any significant changes in the eggs` quality attributes leads to ≈99% decrease in the number of the cells of S. Enteritidis. Fig. 4 shows the average surface average temperature change of the
eggshell during far-infrared processing at 250 and 300 °C (the results were the average of the 3-replicates) while Fig. 5 shows the surface temperature distribution over the egg surface during infrared processing at 250 oC at 110 s and 300 oC at 60 s. Since the highest number of microbial reductions was obtained at these time-temperature combinations, the resulting surface average 13 Page 13 of 36
Far-infrared surface decontamination of whole-shell eggs... temperature change (calculated based on the view angle of the IR camera) was reported. After the infrared processing at 250 °C for 110 s processing, surface average temperature reached just below 60 °C (58.7 °C) while it was just above 60 °C (62.7 °C) at 300 °C – 60 s processing (Fig. 4). The reason that the lower
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reduction was obtained at higher temperature processing was due to the longer processing time at the lower temperature of 250 °C leading to a possible
cr
temperature uniformity throughout the whole shell surface (Fig. 5).
us
As indicated, there was a significant non-homogenous temperature distribution over the shell (Fig. 5). Besides, the overall microbial change
an
throughout the shell was reported rather than a certain portion where the infrared temperature image was obtained since the experimental set-up choice
M
was preferred to resemble the actual technological process. Scattered results, as also demonstrated in Fig. 3, was the result of the non-homogeneous temperature
ed
and resulting non-homogeneous microbial reduction distribution.
pt
If the accumulative effect of temperature to reduce the number of a given microorganism (z- -values for Salmonella Enteritidis strain 13076 and E. coli K12
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in liquid whole egg, reported by Jin et al., 2008, were 4.07 min and 0.17 min, respectively) were calculated based on the temperature increase obtained over the shell (Eq. 3), that would result in 1.32 and 0.39 min of decontamination values for Salmonella Enteritidis and 1.38 and 0.51 min E. coli K12 at the process temperatures of 250 and 300 °C (the reference temperature for these calculations were 60 °C). This would also explain the reason why higher reductions are obtained at a lower process temperature. As indicated above, that is due to the effect of process time – temperature combination, and the higher process time (due to the 14 Page 14 of 36
Far-infrared surface decontamination of whole-shell eggs... earlier start of local denaturation at higher temperatures) at a lower process temperature of 250 °C. This was not the case for the process temperature of 180 °C due to the shorter time and resulting limited increase of the surface temperature. T t Tref z
dt
0
(4)
ip t
t
F 10
cr
Where Tref (°C)is the reference temperature, T is the average surface
temperature (°C), and z is the z-value (°C), and F might be defined to be the
us
decontamination value for this study.
an
The applied process time – temperature combination and the evolved temperature over the shell (with increase in the albumen temperature), infrared
M
process at 250 °C for 110 s (where the average shell surface temperature was 58.7 °C) did not result in any significant changes in the albumen. As indicated by
ed
Ramachandran et al. (2011), USDA reported that the minimum temperature without affecting the physical properties of albumen is 55.6 °C with a minimum
pt
holding time of 6.2 min. This combination resulted in the highest number of
Ac ce
microbial reductions due to the well-balanced temperature distribution over the shell as explained above. For other IR processing conditions, temperature changes revealed that the
maximum egg surface temperature was almost 50 °C after processing for 200 s at 180 °C leading to 1.63 log cycle reduction. This level of reduction, almost 50% less compared to the case at 250 °C for 110 s, did not account for a proper decontamination condition. Besides, at this low level of reduction, significant albumen denaturation was observed at 200 s due to the local over-heating points through the shell as a result of the longer processing time. The IR surface images 15 Page 15 of 36
Far-infrared surface decontamination of whole-shell eggs... also revealed the non-uniformity in the surface temperature distribution of the eggs processed at higher temperatures. As explained, 3.37 log cycle reduction was obtained under far infrared processing at 250 °C for 110 s. However, as reported by Silva and Gibbs (2012),
ip t
for food products containing poultry, a minimum process resulting in 7 log cycle reduction is suggested for Salmonella by Canadian Food Inspection Agency
cr
(CFIA, 2005). Besides, USDA risk assessment studies report the possibility of 1 in
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20000 fresh eggs might contain Salmonella Enteritidis (Mermelstein, 2001) leading to the requirement of 5 log cycle reduction. Based on these, IR surface
an
treatment might be suggested to be a possible pre-process for an additional pasteurization method to reach 5 to 7 log cycle reduction or a possible
M
decontamination technique rather than a proper pasteurization method. In the production of pasteurized liquid egg products, for example, IR decontamination
ed
methodology might also be a possible pre-process to reduce the risk of
pt
contamination during shell breaking process and to prevent the violations of the following pasteurization norms. Isolation of Salmonella from ready-to-eat
Ac ce
pasteurized liquid egg products as a pasteurization-resistant bacteria or due to contamination (Gurtler et al., 2015) also supports this suggestion. Howard et al. (2012) reported the significance of obtaining a possible 3-log
cycle reduction in the number of Salmonella Enteritidis in a decontamination
process. It was stated that this kind of reduction rate might result in 70% decrease in the eventual Salmonella related illnesses. James et al. (2002) also applied IR heating at 210 °C for 30 s on shell egg while the exterior temperature of the shell was reported to be 88 °C with internal surface temperature of 52 °C. There were no visible damage to the shell or no visible denaturation of albumen 16 Page 16 of 36
Far-infrared surface decontamination of whole-shell eggs... observed following this process. As a result, the infrared treatment was theoretically be justified to reduce a certain number of microorganisms on the shell eggs without causing changes on albumen and other quality factors. There have been various studies to reduce the Salmonella Enteritidis on shell eggs
ip t
(Stadelman et al. 1996; Hou et al. 1996; Pasquali et al. 2010; James et al. 2002), and heat treatments are reported to be the mostly used processes even though
cr
there might be possible quality losses in egg components especially due to egg
us
albumen denaturation observed at rather lower temperatures of less than 60 °C (Hou et al., 1996). Pasquali et al. (2010) also used a hot air apparatus to
an
pasteurize the shell eggs with the initial loads of 104 to 105 CFU/egg-shell. Two shots of hot air at 600 °C for 8 s with a 30 s cold air break were applied, and 1.9
M
log cycle reduction in the number of Salmonella Enteritidis was obtained with no significant quality changes. They have also indicated the significance of 1 log
ed
cycle reduction due to the corresponding foodborne risk reduction of Salmonella
pt
Enteritidis for human health. Stolz et al. (2015) also obtained 2.4 log cycle of reduction, conforming 99.6% of the initial Salmonella Enteritidis population
Ac ce
using non-thermal atmospheric plasma. The given conclusion with the maximum 3.37 log cycle reduction obtained
at 250 °C for 110 s was reported based on the results where the IR exposure time was determined not to affect the initial denaturation in the egg albumin. It is expected and the pre-experiments also demostrated that the further increase of the exposure at the given maximum process times (Table 1) would give a start in the albumin denaturation. However, it might be possible to apply a variable process temperatures to eliminate the initialization of the denaturation while increasing the effect of IR temperature to lead to at least 5-log cycle reductions 17 Page 17 of 36
Far-infrared surface decontamination of whole-shell eggs... for surface pasteurization purposes without affecting the physical properties of the egg constituents. Changes in the physical properties: Table 2 reports the changes in the physical properties of the infrared processed
ip t
and control group eggs. Regarding the comparison between control group and processed eggs` physical properties at each process temperature, a single factor
cr
ANOVA test was applied at 95% confidence intervals to determine any
us
significant effect of processing time. There were no significant differences determined (p>0.05) as a function of processing time at a given process
an
temperature even though standard deviation of the foaming capacity values with respect to the average changed in a significant matter. The differences among the
M
IR temperatures were not tested since the objective was just to determine whether the processed temperature had any significant on a quality parameter.
ed
Besides these physical properties, there were also no mass losses observed
pt
during the IR processing.
Conclusions
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External contamination of egg shell by Salmonella and Enterobacteriaceae is a major concern in industry as a health hazard. Besides the effects on health issues, [resence of these microorganisms might even violate the pasteurization norms in the production of, for example, pasteurized liqud egg. In this study, IR application was demonstrated to be a feasible process for surface decontamination of shell eggs with its major advantage of directly influencing the surface. Processing at 250 °C for 110 s resulted in 3.37 log cycle reduction of E. coli ATCC 25922 strain (used in the experimental methodology as a surrogate for Salmonella Enteritidis)
18 Page 18 of 36
Far-infrared surface decontamination of whole-shell eggs... without causing any denaturation in albumen and adverse effects in yolk index, Haugh unit, albumen pH and foaming capacity. Further optimization studies are suggested for proper design of an infrared processing system to obtain a uniform temperature and heat flux distribution through the surface of the eggs for an
Acknowledgement
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effective heat transfer.
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The authors gratefully acknowledge the Scientific Research Foundation,
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University of Mersin, Turkey for supporting this project (Project No: 2015-TP31164). Besides, upon the start of this study, Dr. Erdogdu was also affiliated with
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pt
ed
M
an
the Department of Food Engineering at the University of Mersin.
19 Page 19 of 36
Far-infrared surface decontamination of whole-shell eggs...
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ip t
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Guarnieri, A. 2010. Non-thermal atmospheric gas plasma device for surface decontamination of shell eggs. Journal of Food Engineering. 100: 125-132.
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Rastogi, N.K. 2012. Recent trends and developments in infrared heating in food processing. Critical Reviews in Food Science and Nutrition. 52: 737-760.
Sawai, J., Sagara, K., Kasai, S., Igarashi, H., Hashimoto, A., Kokugan, T., Shimizu, M. and Kojima, H. 2000. Far-infrared irradiation-induced injuries to Escherichia coli at below the lethal temperature. Journal of Industrial Microbiology and Biotechnology. 24: 19-24.
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Far-infrared surface decontamination of whole-shell eggs... Scheerlinck, N., Marquenie, D., Jancsok, P.T., Verboven, P., Moles, C.G., Banga, J.R. and Nicolai, B.M. 2004. A model-based approach to develop periodic thermal treatments for surface decontamination of strawberries. 34: 39-52. Scott, T.A. 1993. The effect of UV-light and air filtering system on embryo
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viability and microorganism load on the egg shell. Journal of Applied Poultry research. 2: 19-25.
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Stadelman, W.J. 1990. Quality identification of shell eggs. In Egg Science and
Haworth Publishing Co., Binghamton, N.Y.
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Stadelman, W.J., Singh, R.K., Muriana, P.M. ve Hou, H. 1996. Pasteurization of eggs in the shell. Poultry Science. 75: 1122-1125.
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Stolz, N., Weihe, T., Stachowiak, J., Braun, P., Schluter, O. and Ehlbeck, J. 2015. Decontamination of shell eggs by using non-thermal atmospheric pressure
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Technology (ICBET 2015). 81: 81-84. Tanaka, F., Verboven, P., Scheerlinck, N., Morita, K., Iwasaki, K. and Nicolai, B.
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2007. Investigation of far infrared radiation heating as an alternative technique for surface decontamination of strawberry. 79” 445-452.
Van Brecht, A., Aerts, J.M. Degraeve, P. and Berckmans, D. 2002. Quantification of the spatio-temporal eggshell temperature and convection coefficient by infrared thermography. Transactions of the ASAE. 45: 1951-1957. Whiley, H. and Ross, K. 2015. Salmonella and eggs: from production to plate. International Journal of Environmental Research and Public Health. 12: 2543-2556.
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Far-infrared surface decontamination of whole-shell eggs... Zhang, W., Zheng, J-X. and Xu, G-Y. 2011. Toward better control of Salmonella contamination by taking advantage of the egg`s self-defense system: a
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review. Journal of Food Science. 76: R76-R81.
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Far-infrared surface decontamination of whole-shell eggs...
Figure Captions: Figure 1. A schematic representation of the infrared processing unit (the lengths are reported in cm).
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Figure 2. Demonstration of the denaturation initialization in the egg albumen. Figure 3. The decrease in the number of E.coli ATCC25922 cells by infrared
treatment (a) 180 ˚C – 200 s (b) 250 ˚C – 110 s (c) 300 ˚C – 60 s and
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(d) 350 ˚C – 20 s.
Figure 4. Surface average temperature change (calculated based on the view processing at 250 and 300 ˚C.
Surface temperature images of the shell eggs infrared processed at (a)
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Figure 5.
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angle of the IR camera) of the egg shells during far infrared
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250 ˚C for 90 s (b) 300 ˚C for 60 s.
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Far-infrared surface decontamination of whole-shell eggs... Table 1. Experimental conditions for far infrared treatment time and temperatures. Process time (s)
180
0 – 120 – 150 – 180 - 200
250
0 - 30 - 60 - 90 - 100 - 110
300
0 – 30 – 45 - 60
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Infrared process temperature (oC)
350
0 – 5* - 10 – 15* - 20
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* This data were only used in the microbiological analysis results to observe the decreasing trend.
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Far-infrared surface decontamination of whole-shell eggs...
Table 2. Effect of infrared processing time – temperature on yolk index, haugh unit and albumen pH. Foaming Capacity (%)
Control
9.43 ± 0.05
0.27 ± 0.03
48.5 ± 7.7
111.5 ± 19.1
120
9.35 ± 0.01
0.24 ± 0.02
37.4 ± 17.9
126..6 ± 30.5
150
9.41 ± 0.13
0.26 ± 0.03
31.6 ± 1.4
123.0 ± 13.6
180
9.47 ± 0.06
0.24 ± 0.02
44.7 ± 12.0
99.1 ± 13.6
200
9.34 ± 0.08
0.28 ± 0.05
59.6 ± 17.4
91.7 ± 29.9
Control
9.16 ± 0.04
0.37 ± 0.03
72.5 ± 6.5
111.5 ± 19.1
30
9.29 ± 0.04
0.32 ± 0.04
61.3 ± 10.0
110.0 ± 31.4
60
9.32 ± 0.02
90
9.23 ± 0.17
100
9.12 ± 0.09
110
9.07 ± 0.16
350 °C
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Haugh Unit
0.33 ± 0.03
62.6 ± 2.4
93.8 ± 18.9
0.34 ± 0.01
59.1 ± 14.4
100.3 ± 7.8
0.34 ± 0.01
60.9 ± 8.1
131.0 ± 26.4
0.36 ± 0.03
71.7 ± 8.1
130.6 ± 10.8
Control
9.43 ± 0.05
0.27 ± 0.02
56.8 ± 10.4
111.5 ± 19.1
30
9.46 ± 0.21
0.30 ± 0.04
60.1 ± 12.0
147.1 ± 27.1
45
9.39 ± 0.14
0.33 ± 0.03
57.1 ± 5.1
113.8 ± 15.2
60
9.20 ± 0.24
0.34 ± 0.03
69.0 ± 5.7
119.2 ± 45.8
Control
9.43 ± 0.05
0.27 ± 0.02
56.8 ± 10.4
10
9.45 ± 0.05
0.23 ± 0.01
41.9 ± 11.3
20
9.39 ± 0.32
0.29 ± 0.04
63.2 ± 4.8
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300 °C
Yolk Index
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250 °C
Albumen pH
ed
180 °C
Process time (s)
pt
Infrared process temperature
-
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Figure 1. A schematic representation of the infrared processing unit (the lengths are reported in cm).
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Figure 2. Demonstration of the denaturation initialization in the egg albumen.
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4.5 4.0 3.5 3.0 2.5 2.0 1.5 1.0 0.5 0.0 50
200
250
(a)
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7.0 6.0
d
5.0 4.0
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Log (N)
100 150 Process Time (s)
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Log (N)
Far-infrared surface decontamination of whole-shell eggs...
3.0
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2.0 1.0 0.0
0
20
40
60 80 Process Time (s)
100
120
(b)
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Far-infrared surface decontamination of whole-shell eggs...
7.0 6.0
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4.0
3.0
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Log (N)
5.0
2.0
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1.0 0.0 20
6.0
50
60
70
(c)
d
5.0
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4.0 3.0
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Log (N)
30 40 Process Time (s)
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10
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0
2.0 1.0 0.0
0
5
10 15 Process Time (s)
20
25 (d)
Figure 3. The decrease in the number of E.coli ATCC25922 cells by infrared treatment (a) 180 ˚C – 200 s (b) 250 ˚C – 110 s (c) 300 ˚C – 60 s and (d) 350 ˚C – 20 s.
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Far-infrared surface decontamination of whole-shell eggs...
60
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50
40
250 °C
30
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300 °C
20 10 0 0
20
40
60
80
100
120
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Process Time (s)
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Average Surface Temperature (°C)
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Figure 4. Surface average temperature change of egg shell during far infrared processing at 250 and 300 ˚C.
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(a)
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Far-infrared surface decontamination of whole-shell eggs...
(b)
Figure 5. Surface temperature images of the shell eggs infrared processed at (a) 250 ˚C for 90 s (b) 300 ˚C for 60 s.
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