Online paper

Vol 44, No. 4;Apr 2014

301 Pretoria, South Africa

Application of microwave as an alternative home

pasteurization method for camel milk; microbiological,

physiochemical and biochemical study.

Ali Alkaladi1, Mohamed Afifi1,2* and Rania Kamal3

1Department of Biological Sciences, Faculty of Science, King Abdulaziz University, North

Campus, PO Box 11508, Jeddah, 21463, Saudi Arabia. 2Department of Biochemistry, Faculty of Veterinary Science, Zagazig University, Egypt. 3Food Control Department, Faculty of Veterinary Medicine, Zagazig University, Egypt.

* Corresponding Author

Mohamed Afifi

e-mail [email protected], [email protected]

tel. 00966509562637 Statement of novelty: This work was conducted to study the application of microwave in

pasteurization of the camel milk. For the first record the treatment of camel milk for 40s in microwave

is sufficient for complete pasteurization of it without adversely affect it's properties and components.

Abstract The present study aimed to compare the efficacy of microwave treatments of camel milk

with the standard milk heat pasteurization method in the terms of microbiological,

physiochemical and biochemical components changes. Fifty camel’s milk samples were

divided into 7 parts for each, one part examined raw the other was pasteurized 62.3 °C for 30

min and the rest were exposed to microwave for 10, 20 ,30, 40 and 50S. The results indicated

the insufficiency of heating camel milk at 62.3 °C for 30 m especially when it has a high

initial microbial count. Contrarily, microwave treatment at 40 seconds was enough to

destruct all tested microbial content of examined camel milk. Unfortunately, both heat

treatment and microwave adversely affect the vital component of the camel's milk as vitamin

C, E, glutathione (GSH), insulin and Immunoglobulin G, in addition to elevation of the

oxidative products as molondialdehyd (MDA) and nitric oxide

Keywords: Camel milk, Pasteurization, Microwave, microbiological and biochemical

properties

Introduction Peoples in many world countries are widely consuming camel milk especially in the arid and

semi-arid zones for its nutritional value, medicinal properties and availability. Many reports

had reported many health associated benefits of camel milk. It was found that camel milk

contains good qualities of lactoferrin, lactoperoxidase, lysozyme and other antibacterial and

antiviral protective proteins, which make it more superior over cow milk (Elagamy, 2000;

Mal & Pathak, 2010). Camel milk is considered to have anti-carcinogenic (Magjeed, 2005), a

protective effect against cisplatin-induced nephrotoxicity (Afifi, 2010), hypo-allergic (Shabo

et al., 2005) and anti-diabetic properties (Agrawal et al., 2003). A high content of

unsaturated fatty acids contributes to its overall dietary quality (Konuspayeva et al., 2008).

The low quantity of ß-casein and the lack of ß-lactoglobulin are linked to the hypo-allergic

Vol 44, No. 4;Apr 2014


effect of camel milk (Konuspayeva et al., 2007). Camel’s milk is different from other

ruminants’ milk; having low cholesterol, low sugar, high minerals (sodium, potassium, iron,

copper, zinc and magnesium), high vitamin C, B2, A and E, low protein and high

concentrations of insulin. Moreover, camel milk can be consumed by lactase deficient

persons and those with weak immune systems (Afifi, 2010).

Since camel milk possess the all required nutrients for microbial growth, it required an

effective method for controlling microorganism before consumption. Pasteurization is the

process that uses relatively mild heat treatment to kill pathogens, and inactivate vegetative

bacteria and enzymes. Heat treatment of milk aims to extend the shelf life and improve the

quality of this complex biological fluid by reducing the microbial load and thus, minimizing

the risk of food borne infections (McKinnon et al., 2009).

Despite that pasteurized camel milk is produced and sold in a few countries including

Saudi Arabia, United Arab Emirates, Kazakhstan and Mauritania, (Wernery et al., 2005)

camel milk still to be widely consumed in its raw state. Therefore, this study aimed to find an

effective ways to pasteurize camel’s milk and assess their impact on the physiochemical,

nutritional, immunological, biochemical and microbial properties of camel’s milk.

Materials and methods Row milk supply

Fifty camel's milk samples (1750 mL each ) were collected under aseptic conditions in sterile

plastic bottles from different camels farms at Sharkia province, Egypt and transported in ice

poxes to the milk hygiene laboratory at Faculty of Veterinary Medicine, Zagazig University,

where every sample was divided into seven parts (250 ml each). The first part was untreated

to serve as control, the 2nd part was aseptically exposed to indirect heat treatment in water

path at 62.3 °C for 30 min then cooled directly to 10 degrees, the 3rd, 4th, 5th, 6th and 7th parts

were exposed to microwave (Triple Distribution System, model ME732K, Samsung,

Selangor, Malaysia) treatment for 10, 20, 30, 40 and 50 seconds respectively. After

treatment, each sample was thoroughly mixed before further analysis.

Microbiological examination

Fresh and treated samples were decimally diluted using peptone water before inoculation

onto plates. 3MTM petrifilmTM plates were used in this study to determine the total bacterial,

Staphylococcus aureus (St. aureus), total coliform and Escherichia coli (E. coli) and total

yeast and mold counts (3M Corporate Headquarters; St. Paul, MN, USA) (AOAC, 2003).

Briefly, 1 ml of appropriate dilution was inoculated onto petrifilm plate and the inoculum

was evenly distributed with a sterile plastic spreader. After one minute at ambient

temperature, each petrifilm plate was incubated aerobically according to manufacturer

recommendations, of each tested group. Following incubation, corresponding colonies on

each plate were counted according to the manufactures’ instructions.

Physiochemical examination of milk

pH values were determined using pH meter (Model HI, Hanna Instruments, Latina, Italy),

titrable acidity, specific gravity, total solids and ash contents were determined according to

the method of Association of Official Analytical Chemists (AOAC, 1990a,b,c,e). Fat content

was analyzed by Gerber method as described by James (1995). Protein content was estimated

according the method of British Standards Institution (BSI, 1990), Lactose content was

determined by the method of Lynch et al. (2007).

Biochemical assays

Vol 44, No. 4;Apr 2014


Vitamin A was determined using Enzyme immunoassay kit (VitaKit ATM; SciMed

Technologies, Inc., Catalogue No. KTSP-71051), vitamin C was assayed colorimetric, firstly

the milk samples was cleared by mixing 600 µL milk with 100 µL 6N HCl, centrifuged for 5

min at 14,000 rpm, then 300 µL supernatant was neutralized with 50 µL 6 N NaOH, and the

supernatant was used for assay of vitamin C according to the method described by Arya

(2002), vitamin E was determined colorimetrically using the method of Rutkowski et al.

(2007). Zn and Se were determined by Flame atomic absorption spectrometric method in

accordance with BSI 11813 (2010), Malodialdehyde (MDA) and nitric oxide and reduced

glutathione were assayed using methods of Okhawa (1979), Montgomery and Dymock

(1961) and Sedlak and Lindsay (1968). IgG was determined by ELISA according to the

method described by Erhardt et al. (1992) and insulin was determined using ultraviolet-visible

absorption spectroscopy, according to Royatvand et al. (2013).

Statistical analysis

The data were statistically analyzed by SPSS version 20 statistical packages (IBM 1 New

Orchard Rd Armonk, NY 10504, USA). Data were presented as a mean ± SD, n = 10.

Statistical differences between groups were performed using student's t-test. Differences

considered significant when P < 0.05.

Results and Discussion Camel's milk has invaluable nutritional and medicinal values, as it contains high levels of

vitamins C, A, B2 and E; and very rich in magnesium and other trace elements as Se and Zn

(Afifi, 2010). Camel milk represents a good nutrition source for peoples live in hard

conditions as desert; as well, it contains a high concentration of non-specific low molecular

weight immunoglobulin G (IgG) which help in protecting them against different pathogens.

It contains high level of insulin that resist acidity, proteolysis and encapsulated in

nanoparticles (lipid vesicles) that make possible its passage through stomach and entry into

circulation (Ajamaluddin et al., 2012). Camel's milk is usually consumed raw, which

certainly constitutes a prominent health hazards for transporting many zoonotic milk-borne

pathogens. Heat treated camel milk sold on a limited scale in some countries as Kingdom of

Saudi Arabia, United Arab Emirates, Mauritania and Khazakhastan (Wernery et al., 2005). In

this study, we tested two ways for the camel's milk pasteurization. The first one is a

modification of the known pasteurization method where the milk is indirectly heated in a

water bath up to 62.3 °C for 30 min, and the second one is microwave treatment, using the

household device (2450MHZ), where the milk samples were exposed to ordinary

microwaves for 10, 20, 30, 40 and 50 seconds. Following treatments, microbiological,

physiochemical and biochemical properties of the milk were examined.

Microbiological parameters

There is no doubt that the major goal of milk heat treatment is making it safe for

consumption. Process of pasteurization can not kill all pathogens through elevated

temperature. Obtained results of the heat treated group of camel milk were in conformity

with the major goals of milk pasteurization. As at 62.3 °C/30 min, highly significant

reductions of all examined microbiological parameters were obtained (Table 1), although,

total elimination was not achieved. Staphylococcus aureus and coliform could be detected

after heat treatment at 62.3 °C/30m, in addition to a total bacterial count. This may be

attributed to high initial value of contaminating microorganisms. The automatic milking

Vol 44, No. 4;Apr 2014


system of dairy cows is mostly responsible for the lower levels of contaminating

microorganisms which can get entrance to milk, and since she-camel milking is still

depending on hand milking, high initial level of contaminating microorganism is usually a

common phenomenon. Heating camel milk at 62.3 °C for 30 min has reduced total microbial,

coliforms, St. aureus, yeasts and molds counts with about 2 logs. E. coli was found to be

completely inactivated with this treatment. These findings proved that this kind of heat

treatment could not fit for camel milk especially with high microbial counts.

Table 1. Effect of heat and microwave treatment on bacterial and mold contents in

camel milk

Microwave treated groups

Heat

treated

group Control

group

Microbiologic

al parameters

50s 40s 30s 20s 10s 62.3°C/30

m

0 0 1.89 ±

0.88 3.31 ± 2.8 4.56 ±3.39* 2.5 ± 1.1

4.77 ±

3.32* TBC (cfu/ml)

0 0 0 2.88 ±

1.89 3.6 ± 2.4*

1.58 ±

0.78

3.8 ±

2.18*

Coliform

(cfu/ml)

0 0 0 0 1.63 ± 0.17 0 2.68 ±

1.48 E. coli (cfu/ml)

0 0 0 2.44 ±

1.14 3.6 ± 2.06* 1.6 ± 0.65

3.6 ±

2.48*

St. aureus

(cfu/ml)

0 0 0 2.58 ± 0.9 3.61 ±

1.95*

1.52 ±

1.18

3.73 ±

1.89*

Yeast and mold

(cfu/ml)

TBC: total bacterial count, St. aureus: Staphylococcus aureus.

Values at the same raw and carry the same symbol not differ statistically.

Results are the mean of three independent replicates and expressed as log10 CFU/ml.

While regarding microwave treatments of camel milk, to the best of our knowledge, this is

the first trail of using microwave pasteurization for camel milk. Moreover, scarce number of

published articles regarding microwave treatment for bovine milk made discussion of our

results accordingly very difficult. Anyhow, microwave treatments of camel milk have

promising results in the term of microbiological quality. In this study, we treated camel milk

sample with microwave at different exposure intervals. Whilst a 10 seconds of microwave

exposure had no significant effect on many microbiological parameters (TBC, coliform, St.

aureus, yeast and mold counts, Table 1), it has a significant reducing effect against E. coli

count (nearly 1 log reduction). Extended exposure of camel milk samples to microwave

treatment for 20 seconds had significantly alter all microbiological parameters positively

especially for E. coli count, whereas it could not be detected after this exposure time. Despite

the significant reduction of coliform, St. aureus and yeast and molds counts after the 20

seconds microwave treatment, they still to represent prominent hazards. Moreover, total

bacterial count reduction value could not be acceptable even with more than 65% reduction

percentage. On further extension of the exposure time to 30 seconds, none of examined

microbiological groups could be detected, except for the total bacterial count which has been

Vol 44, No. 4;Apr 2014


reduced significantly (one log reduction). 40 seconds microwave exposure has reached with

microbiological quality of camel milk to nearly a sterile stage, as none of tested microbial

groups has yielded any count. Same phenomenon of microbial elimination was also

encountered at 50 seconds microwave exposure time. While there is no any work on

microwave pasteurization of camel's milk, its application for caw's milk was studied in the

last few years by some researches (Soler et al., 1995; Sieber et al., 1996; Asaad et al., 2013).

Microwave pasteurization of cow’s milk to reach 72°C for 15 seconds has reduced total

bacteria, psychotropic bacteria counts, E. coli ( Asaad et al., 2013). Microwave energy

inactivated milk pathogens as Yersinia enterocolitica, Listeria monocytogenes

Campylobacter jejuni, and, Enterococcus faecalis in cow's milk (Choi et al., 1993 a,b) and

decrease the count of milk spoilage bacteria (Géczi et al., 2013). Nasri et al. (2013)

investigated the lethal effect of microwave against Salmonella enterica serovar typhimurium

and found that microwave has a bactericidal effect and this would be explained by high

energy absorption by vital cell components (Rougier, 2003). Another theory (Khalil &

Villota, 1989) was linked to change in chemical structure of cellular lipids and protein.

Similar bactericidal effect was also reported against St. aureus and E. coli (Pothakamury et

al.,1995), Clostridium perfringens (Blanco & Dawson, 1974), Listeria monocytogenes

(Farber et al., 1998) and Lactobacillus plantarum (Shin and Pyun, 1997). Interestingly,

bactericidal effect of microwave in Nasri et al. (2013) trails was more prominently achieved

at 40 seconds exposure. These findings augmented our findings as the total elimination

(bactericidal effect) of microwave treatments was met at 40 seconds exposure. In another

study, Villamiel et al. (1996) used microwave to heat both bovine and ovine milk and they

recorded reduction in the total bacterial count (less than 2 log cfu/ml) using different

temperature/time combination. Clare et al. (2005) have reached to a sound conclusion based

on their bovine milk microwaving (continuous flow microwave system) and they stated that

microwave is a suitable sterilization method as milk was kept for 1 year without any sign of

microbial growth.

Physiochemical properties

Many parameters were chosen in this study to assess different treatments on camel milk

physicochemical properties. Heat and microwave treatments were found to have different

patterns of efficacy against these selected parameters. Results listed in table (2) show that

there were some constant parameters (pH, acidity %, lactose %, fat % and total protein %)

which had not significantly changed during either heat treatment at 62.3 °C for 30 min, or

microwaving at different exposure intervals. Although, other parameters had changed

significantly. Mainly, total solids % had increased significantly during heat treatments, and

this certainly attributed to the concomitant evaporation of moisture during heating. Similar

pattern of increase in total solids was also noticed during microwaving. This also is due to

elevated temperature with prolonged exposure time. Total solids’ increase had in turn

significantly affected specific gravity, which showed a similar elevation during either heat

treatment or microwaving of camel milk. Wernery et al. (2003) reported that whey protein in

camel’s milk is more heat resistant than those of cow’s milk, as the degree of denaturation

varied in camel’s milk from 32 to 35% at 80ºC for 5 min, and pasteurization at 72ºC for 5

min revealed no losses in camel’s milk. The thermal treatment of camel milk was found to

have significant impact on milk components especially ash, total solids, and proteins which

showed increase during heat treatment, whilst fat content was not affected (Hattem et al.,

Vol 44, No. 4;Apr 2014


2011). Previous study showed that pasteurization of camel milk had very little effects on its

constituent (fat and protein) with slight increase in ash content (Wernery et al., 2005). Thus,

based on earlier report, which revealed that foodstuffs are less damaged with microwave

rather than regular heat treatments, microwave pasteurization looks promising for camel milk

(Albert et al., 2009).

Table 2. Physiochemical characters of camel milk

Microwave treated groups Heat

treated

group

Control

group

Paramet

ers

50s 40s 30s 20s 10s 62.3°C/30

m

6.3 ±

0.35

6.5 ±

0.5

6.2 ±

0.15

6.5 ±

0.3 6.3 ± 0.22 6.5 ± 0.21 6.4± o.2 pH

0.13 ±

0.011

0.14 ±

0.01

0.137 ±

0.12

0.13 ±

0.01

0.127 ±

0.02

0.12 ±

0.015

0.127 ±

0.015 Acidity

1.0197

± .007a

1.019 ±

.006ab

1.017 ±

0.006bc

1.016 ±

0.005cd

1.016 ±

0.001cd

1.016 ±

0.001cd

1.015 ±

0.002d

Specific

Gravity

0.7 ±

0.01a

0.69 ±

0.005ab

0.68 ±

0.01abc

0.67 ±

0.006bc

0.66 ±

0.005c

0.66 ±

0.03c

0.66 ±

0.02c Ash %

4.6 ±

0.09

4.57 ±

0.13

4.54 ±

0.17

4.5 ±

0.15 4.56 ± 0.1 4.5 ± 0.08

4.4 ±

0.09

Lactose

%

3.45 ±

0.06

3.42 ±

0.07

3.43 ±

0.06

3.41 ±

0.11

3.41 ±

0.052 3.47 ± 0.05 3.43 ±

0.06 Fat %

4.29 ±

0.1

4.25 ±

0.09

4.24 ±

0.1

4.2 ±

0.17

4.25 ±

0.06 4.16 ± 0.07

4.23 ±

0.06 Protein %

13.6 ±

2.5a

13.4 ±

1.3a

12.9 ±

1.5b

12.8 ±

1.3bc

12.5 ±

1.5cd 12.5 ± 1.3cd 12.3 ±

1.5d

Total

Solid

Each value represents M± SE of 10 samples. Means within the same raw carrying

different subscript (a,b,c,d) are significant at P˂0.05 Antioxidant and free radicals

Very little is known about the effect of heat on the antioxidant vitamins, minerals and thiol-

containing substances concentration of camel's milk. As it can be seen in table (3), vitamin C

and reduced glutathione are the most susceptible to degradation by heat. They were hardly

decreased in heat treatment in comparison to fresh milk. This degradation was certainly

attributed to either primary to oxidative effect or secondary to heat treatment (Wernery et al.,

2005). Conversely to Albert et al. (2009), the damage in vitamin C and GSH by microwave

pasteurization is less than that of heat treatment, may be due to less exposure time to heat in

microwave pasteurization. Fat-soluble vitamins A and E are relatively resistant to heat

treatment. A slight reduction was occurred in vitamin E in both treatment and this may be

caused by oxidation (Renner, 1983). While regarding mineral contents of camel milk, heat

generally has very little effect on camel's milk mineral content with exception of Cu and Zn

(Safaa et al., 2013; Wernery et al., 2003). Both Zn and Se were increased in our results by

heat or microwave treatment. Autoxidation may occur for milk lipids during processing with

formation of aldehyds, ketons and lactons (Frankel et al., 1987), trans fatty acids (Semma,

2002). Heat treatments significantly increased the concentrations of the oxidation markers as

Vol 44, No. 4;Apr 2014


MDA in cow's milk compared to the fresh raw milk and correlated to the heating temperature

(Meshref & Al-Rowaily, 2008). Lipid peroxidation represented by MDA and protein

oxidation measured as nitric oxide were significantly increased by heat treatment and

correlated to the heating temperature in comparison with fresh raw milk, and the highest

increase was observed in microwave-pasteurized milk. MDA values for the microwave

heated milk was significantly different from all other heating methods (Meshref & Al-

Rowaily, 2008).

Table 3. Effect of heat and microwave treatment on camel milk antioxidants, free

radicals, insulin and IgG contents.

Microwave treated groups Heat

treated

group

Control

group

Parameter

s

50s 40s 30s 20s 10s 62.3°C/30

m

31 ±

2.9b

31.8 ±

3.3b

35.6 ±

2.2b

40.8 ±

3.2a

45.4 ±

4.6a

35.8 ±

3.2b

46.2 ±

9.7a

Vit.C

(mg/dl)

0.122

±0.0 3

0.124 ±

0.03

0.12 ±

0.007

0.128 ±

0.02

0.122 ±

0.022

0.126 ±

0.015

0.136 ±

0.0 2

Vit. A

(mg/L)

0.48 ±

0.02b

0.48 ±

0.01b

0.49 ±

0.02b

0.52 ±

0.02a

0.53 ±

0.01a

0.5 ±

0.02b

0.54 ±

0.03a

Vit. E

(mg/L)

112.3 ±

2.5c

125.7 ±

2.5b

130.3 ±

4ab

133 ±

16.5ab

140 ±

7.9a

132.3 ±

2.5ab

142.7 ±

3a

GSH

(μmol/ml

4.9 ±

0.7a

4.6 ±

0.6a

4.4 ±

0.7a

4.3 ±

0.7a 4 ± 0.6a 4.2 ±

0.64a

3.1 ±

0.23b Zn (PPM)

136.3 ±

1.5a

130 ±

4.5ab

127.3±

2.5ab

124.3 ±

1.5ab

123.7 ±

4.7ab

115.7 ±

12b

113.3 ±

20b Se (PPM)

0.46 ±

0.05a

0.41 ±

0.03b

0.38 ±

0.03bc

0.38 ±

0.02bc

0.352 ±

0.02c

0.22 ±

0.015e

0.172 ±

0.03f

MDA

(nmol/L)

0.55 ±

0.04a

0.49 ±

0.015b

0.40 ±

0.015cd

0.38 ±

0.01de

0.37 ±

0.015de

0.37 ±

0.01de

0.36 ±

0.01e

NO

(μmol/ml

37.4 ±

1.9a

37.6 ±

1.1a

38.8 ±

2a

39.2 ±

2.8a

40 ±

2.7a 40.4 ± 2a 41.2 ±

5.7a

Insulin

(μU/ml)

723.3 ±

25b

800 ±

43.6a

805 ±

43.6a

820 ±

10a

816.7 ±

15a

823.3 ±

25a

850 ±

50a IgG (μg/ml)

MDA; Malondialdehyde, GSH; Reduced glutathione, NO; Nitric Oxide. Each value

represents M± SE of 10 samples. Means within the same raw carrying different subscript (

a,b,c,d) are significant at P˂0.05

Insulin

Camel milk contains high levels of insulin (52 μU/ml) than cow milk (16.32 μU/ml) and

similar to human milk (60.23±41.05 μU/ml), so camel milk can be used for Diabetes mellitus

control (Agrawal et al., 2003). However, Wernery et al. (2006) reported that the insulin

content in camel milk is only slightly higher than in cow milk. Amel et al. (2012) found that

the pasteurization condition (63°C/30 min) not affected insulin level and its anti-diabetic

effect, but it decreased by boiling (100°C/30 min). At this study, insulin level was not

Vol 44, No. 4;Apr 2014


affected by microwave pasteurization (Table 3), which certainly due loser expositor time.

Pasteurization, freeze drying or storage of camel milk at 4°C for 4 days as well as freezing at

-20 °C resulted in a statistically significant reduction in insulin concentrations; however, this

was minimal (Wernery et al., 2006).

Immunoglobulin G (IgG)

The importance of IgG in camel's milk has been emphasized by many authors to explain the

health related effects of camel milk (Farah, 1993; Konuspayeva et al., 2004). On average,

IgG concentration in camel colostrum seemed to be higher than that in other species (El-

Hatmi et al., 2006). Camel milk was found to be the richest source of IgG (Conesa et al.,

2008). Lactoproteins such as lactoferrin and IgG are known as health factors that play an

important role for milk consumers. In particular, camel milk, which is consumed in many

countries for its medicinal virtues, is renowned for being richer in some lactoproteins

compared with cow's milk (Konuspayeva et al., 2007). Camel milk IgG is a heat labile

compound and its denaturation midpoints for the mature milk heated for 30 min is 67·2°C

(Didier et al., 2006). The concentration of IgG in camel milk was slightly decreased during

heating at 62.3 °C for 30 mints. Whilst the detrimental effect of microwave treatment was

encountered only at exposure time for 50s (Table 3). Microwave pasteurization of milk was

reported to result in lower levels of denaturation of whey proteins compared to conventional

thermal processes and the denaturation of_ß-lactoglobulin was almost similar in both

processes (Villamiel et al., 1996). In general, Elagamy (2000) found that camel IgG is more

resistant to heating up to 100°C than that of cow’s milk.

Conclusion Microwave treatment at 40 sec can be used as an alternative pasteurization tools for camel

milk. Despite that microwave treatment likely affect the physiochemical properties of the

milk by the same degree as regular heat pasteurization, but the microwave method is more

advantageous in affecting the vital components in camel's milk.

Acknowledgments This work was funded by the Deanship of Scientific Research (DSR), King Abdulaziz

University, Jeddah, under grant No (965-005-D1434). The authors, therefore, acknowledge

with thanks DSR technical and financial support.

Author disclosures Ali Alkaladi, Mohamed Afifi, and Rania Kamal declare that they have no conflict of interest

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