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Food Research International 33 (2000) 719±724

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Combined industrial processes with irradiation to assure innocuity


and preservation of food products Ð a review
M. Lacroix *, B. Ouattara
Canadian Irradiation Center (CIC), Research Center in Microbiology and Biotechnology, INRS-Institut Armand-Frappier, 531 Boul. des Prairies,
Laval, QueÂbec, Canada H7V 1B7

Received 15 December 1999; accepted 31 March 2000

Abstract
The desire to assure food safety for consumption requires better food preservation techniques. The presence of parasites, insects,
mites, and micro-organisms, is an important source of problems. In this regard, irradiation is an interesting alternative to be con-
sidered to satisfy quarantine requirements, to control severe losses during transportation and commercialization, and to insure food
safety. This paper reviews some potential applications of irradiation for preserving food products. # 2000 Elsevier Science Ltd. All
rights reserved.
Keywords: Industrial processes; Irradiation; Food safety; Food preservation

1. Introduction has come to ®nd ways to reduce losses in food products,


enhance their shelf life and assure their innocuousness.
At the present time, many procedures such as freezing, Irradiation technology is the answer to these expecta-
smoking and heating are used alone or in combination to tions, since it creates the possibility of putting foods on
preserve food products, but manufacturers are still the market that are ``glowing with freshness, and
faced with heavy losses (Farkas, 1990; 1999). Yearly, exempt of pathogens. This technology was approved in
losses during storage have been estimated to be 10% for 1981 by the FAO/IAEA/WHO joint committee on the
cereal, 40% for vegetable and fruits, 75% for peas and wholesomeness of irradiated food. It was stated that,
beans, and much more for meats, poultry and ®sh due irradiation of food at doses up to 10 kGy introduced no
to their particular sensitivity to enzymatic and microbial special nutritional problem. Currently, more than 26
attacks. These losses are being shouldered by the customers countries are using the process on a commercial scale
who are faced with price increases for the said products. (Stevenson, 1994). When irradiation is used in combi-
Furthermore, society has to cope with many food-borne nation with other preservation methods such as mild
diseases as a result of the development of pathogenic heat treatments, addition of spices and plant extracts,
micro-organisms such as E. coli O157:H7, Campylobacter, the global eciency is reinforced through synergistic
Listeria, Toxoplasma, Trichinella etc. and production of action, and the irradiation doses can be reduced without
toxic substances like enterotoxin, mycotoxin and histamin a€ecting the product quality (Farkas, 1990; Mahrour,
(Cassin, Lammerding, Todd, Ross & McColl, 1998; Lacroix, Nketsa-Tabiri, Calderon & Gagnon, 1998a).
IFT-Expert Panel, 1988). According to the United The irradiation of food products is a physical treatment
Nations report in 1995, over 30% of the mortality rate involving direct exposure to electron or electromagnetic
world-wide is caused by alimentary diseases. The time rays, for their long time preservation and improvement
of safety and quality (Urbain, 1986). 60Cobalt produces
electromagnetic g-rays which are similar to light but
with much higher energy. This source of energy is being
* Corresponding author. Tel.: +1-450-687-5010 ext. 4489; fax: +1-
used for deinsectization, slowing the fruit ripening,
450-687-5792. elimination of pathogenic bacteria and parasites, and
E-mail address: monique.lacroix@iaf.uquebec.ca (M. Lacroix). destruction of micro-organisms. During irradiation
0963-9969/00/$ - see front matter # 2000 Elsevier Science Ltd. All rights reserved.
PII: S0963-9969(00)00085-5
720 M. Lacroix, B. Ouattara / Food Research International 33 (2000) 719±724

treatment, DNA molecules undergo swelling and break experiments was mostly a hot water dip (Gagnon et al.,
alongside the chain, preventing them from functioning 1993). With fresh fruits and vegetables, it is important
normally. As a result, the micro-organisms and parasites to establish the exact parameters such as proper ripen-
that have been a€ected are no longer capable of reprodu- ing stage, proper pre-treatment, post-treatment and
cing themselves and die (Urbain, 1986). Irradiation can transport conditions yielding optimum results.
be performed at ambient or lower temperatures which Combined treatment (low heat with a weak dose of
guarantees better preservation of nutritive values and irradiation) can slow down ripening and reduce losses in
physico-chemical properties of foods. Such advantages fruits. Attempts have been made in our laboratories, to
make irradiation treatment a viable technology for pre- evaluate the possibility of using ionizing radiation in
servation of various food products. The focus of this combination with hot water dip treatment to achieve
review is the use of gamma-irradiation for food pre- longer shelf life of fresh mangoes (Gagnon et al., 1993;
servation and the development of new products for Lacroix et al., 1991; 1993). The results showed that after
edible/biodegradable packaging application. 30 days of storage, the percentages of rotten fruits were
100% for controls, 80%, for samples irradiated at 1
kGy, and 20% for samples treated by hot water dip
2. Irradiation of fruits and vegetables combined with irradiation at 1 kGy. The combined
treatment also delayed the development of ripe skin
Radiation treatment for extension of the shelf life of color. In this study, the hot water treatment and/or the
fresh fruits and vegetables have been widely studied gamma irradiation of mangoes had no adverse e€ects
(Farkas, 1990; Gagnon, Lacroix, Pringsulaka, Latreille, on nutritional and chemical qualities of the mangoes.
Jobin, Nouchpranool, et al., 1993; Lacroix, Jobin, Di€erent studies on Moroccan citrus fruits were also
Latreille, Lapointe & Gagnon, 1991; Lacroix, Gagnon, undertaken at the Canadian Irradiation Center. Results
Pringsulaka, Jobin, Latreille, Nouchpramool et al., obtained from this research demonstrated that washing
1993; Thomas, 1986). The application of irradiation, using with warm water and waxing are treatments that cause a
doses less than 1 kGy or 100 krad (radiation absorbed signi®cant loss in fruits during storage. In contrast,
dose) for vegetables and fruits, inhibits germination, clementines irradiated at 0.3 kGy, and stored at 3 C for
slows ripening of fruits and eliminates insect infestation. a period of 8 weeks, showed <11% losses (Abdellaoui,
Doses between 1 and 3 kGy might eliminate mold. Lacroix, Jobin, Boubekri & Gagnon, 1995).
When used on cereal products, it allows the elimination We also observed that throughout the entire pre-
of insects (doses 41 kGy), reduces and eliminates bacteria servation period, the quantity of vitamin C content in
(doses 52 kGy) and reduces cooking time (vegetable the irradiated clementines was signi®cantly higher.
proteins). Most fruits and vegetables tolerate irradiation Moreover, results of the sensorial evaluation showed
treatments at a minimal dose of 0.25 kGy, without that the organoleptic quality was maintained through-
undergoing a change in their quality. A dose of 2.25 out the entire storing period, especially in irradiated
kGy is usually the optimal dose that fruits and vege- fruits. According to the sensorial evaluators, the taste of
tables may tolerate to keep their quality intact (loss of the irradiated fruits was sweeter than in non-irradiated
®rmness, change in ¯avour/taste, physilogical breakage, fruits (Abdellaoui et al., 1995).
accelerated ripening). Strawberries, for instance, may The e€ect of waxing, hot water dipping and irradia-
tolerate doses as high as 3 kGy. At this dose, the infection tion, on the phenol content and the colour of the oran-
of fruits is eliminated and the quality of the strawberries ges was also veri®ed. These assays demonstrated that
is untouched for a period of 14 days if kept at 5 C. irradiation and storage at 20 C favors the synthesis of
Doses as weak as 0.04 to 0.74 kGy may inhibit the ger- phenolic compounds, such as the ¯avonoids. The research
mination of onions. The use of irradiation as a sole demonstrated that the combined treatment stimulated
treatment for postharvest desease control seems to be the synthesis of these compounds (Oufedjikh, Mahrouz,
limited to only a few commodities, because the doses Amiot & Lacroix, 2000). This phenomenon is related to
required for e€ective control of fungal spoilage frequently a decrease in intensity of the red colouring in favor of a
result in undesirable changes such as tissue or skin more yellowish one. Waxing, however, maintains the
damages, or changes in ¯avour or texture or by a€ecting colour and the concentration of phenolic compounds in
the appearance and normal ripening of fruits (Mahrour oranges (unpublished data).
et al., 1998b). The tolerance to irradiation varies among Among the essential oils in oranges, (D)-limonene
species and varieties and is in¯uenced by ripeness at the seems to be the major compound in the fruit skin. A
time of treatment. Several investigations have demon- dose of 2 kGy stimulated the (D)-limonene synthesis
strated, however, the usefulness of mild treatment prior (Moussaid, Lacroix, Nketsia-Tabiri & Boubekri, 2000).
to low-dose irradiation in extending the shelf life of The control in the concentration of the compounds is
certain fresh fruits without a€ecting their normal quality important for oranges, as the appearance of brown
attributes. The heat treatment employed in these spots in fruits is related to their presence in the tissues in
M. Lacroix, B. Ouattara / Food Research International 33 (2000) 719±724 721

an appreciable amount. These studies showed that this sample. In Iÿ, the higher phenols concentration and
waxing had a protective e€ect on the quality of the the better preservation of whiteness throughout the storage
oranges during irradiation. Moreover, a irradiation period can be explained by diminished activity of poly-
dose up to 1 kGy ensured the innocuity of the product phenols oxidases. However, that hypothesis could not
did not, in any way, a€ect its essential oil content. explain the higher degree of coloration and browning
Mushrooms are a popular food products in the world. found in I+ samples. This e€ect was explained by the
However, the level of loss during marketing could be as electronic microscopy of the cellular membranes which
high as 40%. The loss of mushroom quality is marked revealed a better preserved integrity in Iÿ than in I+.
by brown coloration of its surface, cap opening, stipe The thickening of the membranes observed in I+ which
elongation, cap diameter increase, weight loss and tex- causes a stress to the cell, alters the cell permeability.
ture changes. The enzyme, polyphenol oxidase (PPO) This alteration allows the release of vacuolar phenolic
present in the mushroom cells causes browning when compounds and the entry of molecular oxygen into the
they are subjected to forces that can disrupt cellular cell cytoplasm which creates a synergistic e€ect of
integrity, such as vibrations, rough handling, and ageing. enzymatic and non-enzymatic phenols oxidation. This
PPO oxidizes phenolic compounds present in the mush- theory explains the browning e€ect and the smaller
room such as tyrosine to quinones which condense to concentration of total phenolic compounds observed in
form the brown melanin pigments (Beaulieu, BeÂliveau, I+. This study has shown that the right dose rate should
D'Aprano & Lacroix, 1999). In addition, bacterial be applied for each product. A lower dose rate (2 kGy /
infection (Pseudomonas tolaasii; Mycogone perniciosa h) should be applied for fresh mushrooms (Beaulieu et
magnus) could cause the brown coloration. A low irra- al., 1999).
diation dose in combination with a controlled storage
(temperature and relative humidity) is very e€ective in
controlling the deterioration of fresh mushrooms caused 3. Irradiation of proteinic sources
by senescence and microbial activity. The elimination of
pathogenic bacteria such as Pseudomonas tolaasii and The application of irradiation in meats, poultry and
Mycogone perniciosa can be achieved with 2 kGy dose ®sh, at doses less than 1 kGy, eliminates parasites (Gir-
and increase shelf life from 2 to 8 days when stored at oux & Lacroix, 1998). The intermediate doses of 1±10
10 C (Skou, Beett & Lundsten, 1974). The irradiation kGy eliminates pathogenic bacteria and reduces the
treatment at 1 kGy could extend the shelf life from 2 to number of micro-organisms. Signi®cant progress has
4 days at 10 C by reduction of the micro¯ora, slowing been made in this respect by using irradiation doses
the respiration and the morphological transformation, lower than 10 kGy to control the growth of pathogenic
and lowering PPO activity and browning reaction. A and spoilage bacteria on meat and meat products, such
dose of 2 kGy appears to be necessary for satisfactory as Listeria monocytogenes and Salmonella typhimurium,
prolongation of the shelf life of mushrooms at 10 C. Escherichia coli O157:H7 and Yersinia enterocolitica
However, this can also a€ect some of the physical (Fu, Sebranek & Murano, 1995a, b). Although irradiation
characteristics viz. hyphes contraction and discolora- might have some e€ects on lipids, proteins or vitamins,
tion. Based on these results, treatment at a dose of 2 its bene®cial outcome on protection of food quality
kGy and at dose rates of 4.5 kGy/h (Iÿ) and 32 kGy/h outweighs the former. However, meats are generally
(I+) have been studied to evaluate their e€ects on the susceptible to oxidative deterioration principally due to
overall quality of the mushrooms (Beaulieu et al., 1999). oxidation of polyunsaturated fatty acids present in the
Both the dose rates were e€ective in lowering the number phospholipids. This results in the development of unde-
of yeasts, molds, and bacteria and extend the shelf life sirable ¯avours in irradiated meats (Giroux & Lacroix,
by 6 days (Beaulieu, Lacroix, Charbonneau, Laberge & 1998). Since polyunsaturated fatty acids are oxidized
Gagnon, 1992). However, based on mushrooms whiteness, rapidly, precautions must be taken during the irradia-
I+ and Iÿ showed a respective 2 and 4 days shelf life tion treatment. Oxidative and non oxidative changes in
increase. After a storage of 9 days, the I+ treated mush- lipids can be observed. Ionizing radiation causes the
rooms were signi®cantly (P40.05) darker, and a higher radiolysis of water which is present to a great extent in
L value (whiteness color) was observed in Iÿ. In treated meat. This generates free radicals such as .OHÿ, hydrated
mushrooms, at both dose rates, the PPO activity was electron and H+, all of which react with the food con-
signi®cantly lower (P40.05) as compared to the con- stituents (Merritt, Angelini & Graham, 1978). The most
trol. However, the content of total phenolic compounds susceptible site for free radical attack in a lipid molecule
throughout the storage, was signi®cantly higher is adjacent to the double bonds. The most a€ected lipids
(P40.05) only in case of Iÿ, as compared to I+ and during irradiation are thus the polyunsaturated fatty
control samples. This greater phenolic accumulation is acids that bear two or more double bonds.
in accordance with the better preserved coloration Similar to lipids, protein damage due to irradiation is
observed in Iÿ indicated a diminished oxidation rate in catalyzed by free radicals formed by the radiolysis of
722 M. Lacroix, B. Ouattara / Food Research International 33 (2000) 719±724

water. Sulfur containing amino acids along with aromatic A number of studies reported that free radicals generated
amino acids are also susceptible to irradiation damage. by irradiation can also react with myoglobin or hemo-
The products formed from sulfur-containing amino globin resulting in undesirable color (Kamarei, Karel &
acids in proteins include methyl or ethyl mercaptan, Wierbicki, 1979). The color stabilization would be more
dimethyl disul®de, carbonyl sul®de or hydrogen sul®de. improved if meat and meat products could be incorpo-
When sulfur compounds are submitted to radiation in rated with food additives possessing radical scavenging
the absence of oxygen, hydrogen sul®de and other sul®des properties before irradiation. Furthermore, ascorbic
are formed in large amounts. In the presence of oxygen, acid like many other edible short chain fatty acids has
the production of ammonia and sulfuric acid also been reported to inhibit the growth of many meat-borne
increases (Giroux & Lacroix, 1998). The most radiation pathogenic and spoilage bacteria (Ouattara, Simard,
sensitive amino acids are in fact the ones bearing sulfur Holley, Piette & BeÂgin, 1997). Hence, a study was
notably cystine, methionine and tryptophan. Desulfur- undertaken in our laboratory in which ascorbic acid
ization must thus be considered as one of the principal (0.5%, w/w) was incorporated in half-lean ground beef
e€ects of ionizing radiation on amino acids and pro- before irradiating at 1±4 kGy in order to evaluate the
teins (Singh, Lacroix & Gagnon, 1991). Partmann and combined e€ect of these on microbial characteristics
Keskin (1979) showed that the majority of the amino and color parameters of the meat product. Results
acids in minced lean beef or pork and chicken breast showed that irradiation treatment at a dose of 1 kGy
muscle are stable up to a dose of 5 kGy. Josephson, resulted in signi®cant (p40.05) reduction of total aero-
Thomas and Calhoum (1978) indicated that there was bic plate counts compared to unirradiated samples dur-
no signi®cant destruction of cystine, methionine and ing the entire experimental period (10 days). Increasing
tryptophan up to a dose of 71 kGy. It is also note- irradiation dose led to subsequent improvement of
worthy that there was no loss of lysine by irradiation at antibacterial e€ect. Complete inhibition of microbial
70 kGy and even an increase is detected (Ley, Bleby, growth occurred during a period of 3 and 5 days,
Coates & Patterson, 1969). In comparison, cooking can respectively, in samples treated at 3 and 4 kGy. The shelf
generate up to 40% loss of the essential amino acid life was respectively 1, 5, 7 and 10 days for samples
lysine (Harris, 1983). treated at 0, 1, 2 and 3 kGy. Samples treated at 4 kGy
The minimum irradiation dose (threshold dose) above were still good after 10 days of storage. The results also
which o€-¯avors are detected in irradiated meats was con®rmed the high sensitivity of Enterobacteriaceae to
reported to be 2.5 kGy for poultry and beef (Hanis, irradiation doses. The observation is of great interest
Jelen, Klir, Mnukova, Perez & Pesek, 1989). However, since this group contained many bacteria involved in
doses higher than 2.5 kGy may be required for complete meat borne diseases like E. coli O157:H7, Salmonella
elimination of Salmonella on chicken (Mahrour et al., typhimurium, Yersinia enterocolitica. The results of color
1998b). Natural antioxidants from spices could be analysis showed higher a values and lower hue angle
employed to stabilize fats and control oxidative dete- values in samples containing ascorbic acid, which are
rioration of foods during irradiation. The e€ect of the indicative of more red color. Results of sensorial eva-
combination of irradiation and marinating with rosemary luation also demonstrated that incorporation of the
and thyme extract on the sensitivity of Salmonella and antioxidant in ground beef before irradiation had no
organoleptic characteristics of poultry has also been detrimental e€ect on its odor and taste.
investigated in our laboratory (Mahrour et al., 1998a,
b). The shelf life of chicken irradiated in air, under
vacuum and in combination with marinating was, 4. Irradiation and development of edible coatings
respectively, 10, 11 and 15 days when irradiated at a
dose of 3 kGy. This increased to more than 15 days for Edible coating is a new technology that has been
all samples when irradiated at a dose of 5 kGy. Irradia- introduced in food processing in order to obtain products
tion of fresh chicken pieces with a dose of 3 kGy with longer shelf life. Several applications for meat,
appears to be able to extend the microbiological shelf poultry, and seafoods have been reviewed by Gennadios,
life by a factor of 2 if stored at 4 C. When the chicken is Hanna and Kurth (1997) with particular emphasis on
marinated or when irradiated at 5 kGy, the micro- the reduction of lipid oxidation, weight loss, moisture
biological shelf life was extended by a factor of 7±8. Our loss, microbial load, and volatil ¯avor loss. Studies
results demonstrated that the use of marination before made in our laboratories on calcium caseinate-based
irradiation reduced the dose necessary to eliminate Sal- solutions demonstrated that gamma irradiation improved
monella in poultry from 5 to 3 kGy. edible coating development via the production of cross-
The analysis of fatty acid demonstrated that the mar- links between protein molecules (Brault, D'Aprano &
ination treatment has a better protection e€ect on linoleic Lacroix, 1997; Ressouany, Vachon & Lacroix, 1998).
acid (18:2), linolenic acid (C18:3) and arachidonic acid Based on these results and those obtained for gamma
(C20:4) derived from phospholipids. irradiated foods, studies were undertaken to evaluate
M. Lacroix, B. Ouattara / Food Research International 33 (2000) 719±724 723

the e€ect of combining gamma irradiation of fresh and ®rm bread base with soft moist topping of cheese,
strawberries, beef or prepared foods (pizza) and coating sauce and selected meats and/or vegetables) which
with unirradiated and irradiated (cross-linked) edible makes it more dicult to keep for long periods under
solutions. Strawberry decay resulting from mold growth refrigeration. For example, ingredients such as pork
is a common problem during fruit storage. Rot caused by sausage and pepperoni are highly susceptible to oxida-
Rhizopus sp. and Aspergillus sp. are mainly accountable tion and spoilage by psychrotrophic bacteria such as
for the fruit loss. Because strawberries are especially Pseudomonas and Acinetobacter. Also, ¯avor loss may
sensitive to mold growth, its shelf life is of 2 days when occur in both storage and in cooking process. We have
stored at 15 C. In order to control fruit decay and losses, examined the combined e€ect of irradiation and coating
many studies have been carried out in order to develop with milk protein solutions on the shelf life of pizza
new preservation methods. Among those tested, gamma under refrigeration. Based on microbiological status,
irradiation treatments have proven e€ective in reducing the shelf life of control samples was 5 days, compared to
the number of micro-organisms on fresh strawberries 14 and 16 days for samples irradiated at 1 and 2 kGy,
and were used in combination with hot-water dip treat- respectively. When pizzas were coated before irradiation
ments to inhibit yeasts and increase the storage stability treatment, only 1 kGy was necessary to obtain shelf life
of strawberry yoghurt (Kiss, 1975). We have combined of 21 days. That was expected since gamma irradiation
gamma irradiation with the use of an edible coating in is known to increase the cohesive strength in protein
order to improve the shelf life of fresh strawberries. solution by formation of cross-links (Brault et al., 1997;
Fresh unirradiated and irradiated strawberries were Mezgheni, D'Aprano & Lacroix, 1998; Ressouany et al.,
coated with two types of protein solutions (with or 1998), which in turn reduced water vapor and oxygen
without cross-linking). The results showed that coating barriers properties (unpublished data). Therefore, aerobic
de®nitively delayed mold growth as did gamma irradiation. spoilage microorganism are more inhibited and the
Also, for the unirradiated strawberries, the cross-linked initiation of oxidation activity is delayed. Also, sensorial
coating was more e€ective than the uncross-linked one. evaluation experiments showed that coated and irra-
Almost 50% of the uncoated control strawberries were diated samples had better odor and taste properties
rejected after 8 days while an equal amount of rejected compared to control samples and samples irradiated
fruits was obtained on day 9 for the coated unirradiated only, suggesting that the coating process reduces loss of
control fruits. The self life increased to 11 days for the ¯avor during storage and cooking.
coated control fruits with an irradiated formulation.
Good results were obtained for all types of irradiated
strawberries. In comparison, 50% fruit loss was 5. Conclusion
obtained after 11 days for irradiated strawberries coated
with an unirradiated coating and after 13 days for the Gamma irradiation can be used for many applications
irradiated strawberries without coating or coated with related to food science. Low dose of irradiation can be
an irradiated solution. On that basis, the shelf life of used to prolong the shelf life of many fruits and vege-
fresh strawberries was extended by 5 days by applica- tables by reducing microbial spoilage, reducing the rate
tion of a cross-linked edible coating or by irradiation of respiration and delayed ripening. The use of com-
treatment. No synergistic e€ect was noted between bined treatment with irradiation had a synergistic e€ect
gamma irradiation and coating. However, the use of a reducing the microorganisms load and the irradiation
cross-linked coating was found to be almost as e€ective dose, required to eliminate pathogenic bacteria and also
as gamma irradiation for preventing mold growth. Fol- reducing the rate of unsaturated fatty acid oxidation.
lowing these results, we have submitted these formula- The use of edible coating in combination with gamma
tions to a sensorial analysis to see if the coatings altered irradiation has been proven e€ective for increasing the
in any way the organoleptic properties of the fruits. shelf life of many foods. Our recent research clearly
Statistical analysis con®rmed that the coated strawberries showed the e€ectiveness of the use of gamma irradiation
were not signi®cantly di€erent (P>0.05) from the to generate cross-linked edible coating or biodegradable
uncoated fruits in terms of their texture or taste. Further- packaging. These biodegradable packagings could be
more, the coated strawberries were shinier than the customized for each speci®c product. We also believe
uncoated ones throughout the storage period. These, that these promising ®lms of cross-linking by gamma
thus clearly demonstrated that edible coatings could be irradiation might ®nd application as a support for
applied on strawberries in order to extend their shelf life immobilization of active compounds like ¯avors, anti-
without altering their organoleptic properties. microbial or antioxidant compounds. Moreover, the
Another interest is consumption of oven-ready meals cross-linked ®lms could be used as a support for con-
such as pizzas. Pizza consumption has dramatically trolled release of these compounds from the ®lm to the
escalated in recent years. An inherent problem with food. The combination of irradiation with coating is a
pizza is the contrasting nature of its ingredients (crisp promising path that must be developed in the future.
724 M. Lacroix, B. Ouattara / Food Research International 33 (2000) 719±724

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