Effects of ultraviolet light on biogenic amines and other quality indicators of chicken meat during refrigerated storage C. A. Lázaro,*†1 C. A. Conte-Júnior,† M. L. G. Monteiro,† A. C. V. S. Canto,† B. R. C. Costa-Lima,† S. B. Mano,† and R. M. Franco† *Faculty of Veterinary Medicine, Universidad Nacional Mayor de San Marcos, Av. Circunvalación Cdra. 28 s/n, PO Box 03-5137, San Borja, Lima, Perú; and †Department of Food Technology, Faculty of Veterinary, Universidade Federal Fluminense, Vital Brazil Filho 64, CEP: 24230-340, Niterói, Rio de Janeiro, Brazil ramine, cadaverine, and putrescine contents (P < 0.05). The highest UV-C intensity (1.95 mW/cm2) promoted a decrease in the initial bacterial load, and extended the lag phase and the shelf life. The groups irradiated with 1.13 and 1.95 mW/cm2 exhibited a more stable b* value than the other groups; similar trends for L*, a*, pH, and TBA reactive substance values were observed among all groups. The UV-C light was demonstrated to be an efficient alternative technology to improve the bacteriological quality of chicken meat without negatively affecting the physical and chemical parameters of chicken breast meat. Nonetheless, the increases on the biogenic amines content should be considered as an effect of the UV processing and not as an indicator of bacterial growth.

Key words: biogenic amine, poultry, quality indicator, storage, ultraviolet 2014 Poultry Science 93:2304–2313 http://dx.doi.org/10.3382/ps.2013-03642

INTRODUCTION In the poultry industry, the application of critical control points for chicken meat processing is important to control and decrease the risk of introduction and spread of spoilage and pathogenic microorganisms in the final product, and to improve the food safety (Barker et al., 2004). Bacterial contamination occurs mainly through surface contact (skin and carcass cavity) and represents the major source of meat contamination during processing (Kondjoyan and Portanguen, 2008). The increase in the consumer demand for high-quality food products has stimulated the meat industry to develop technologies to decrease the surface contamination of meat products. Several methods have been reported as potential decontamination technologies including gamma irradiation, continuous and pulsed ©2014 Poultry Science Association Inc. Received September 21, 2013. Accepted May 11, 2014. 1 Corresponding author: [email protected]

UV light, high hydrostatic pressure, infrared technology, electro-magnetic fields, sonication, and microwaves (Barbut, 2004). Ultraviolet light discharges and translocates energy in the form of waves or particles through space without inducing radioactivity. Ultraviolet light ranges from 100 to 400 nm and is divided into UV-A (315–400 nm), responsible for human skin tanning; UV-B (280–315 nm), which can cause skin burning and eventually lead to skin cancer; UV-C (200–280 nm), recognized as the germicidal range because it effectively inactivates bacteria and viruses; and the vacuum UV range (100–200 nm), in which almost all substances can absorb it, and thus is only transmitted in vacuum (Koutchma et al., 2009). Ultraviolet-C light injures microorganisms directly by damaging the DNA or indirectly by forming free radicals during water radiolysis (Byelashov and Sofos, 2009). In contrast to thermal processing, this nonthermal technology reduces the microbial load without significantly changing the nutritional and sensory characteristics of vegetables (fruits and roots) products, as

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ABSTRACT Radiation from UV-C has been demonstrated as a potential surface decontamination method in addition to several advantages over regular sanitation methods. However, UV-C radiation possibly affects the physicochemical properties of meat products. To determine the optimum exposure time for bacterial reduction, 39 chicken breasts, inoculated with a pool of Salmonella spp., were submitted to 3 levels of UV-C intensities (0.62, 1.13, and 1.95 mW/cm2) for up to 120 s. After the optimum exposure time of 90 s was determined, changes in the biogenic amines, total aerobic mesophilic bacteria, Enterobacteriaceae, lipid oxidation, pH, and instrumental color were evaluated in 84 chicken breasts that were irradiated (0.62, 1.13, and 1.95 mW/cm2) and stored at 4°C for 9 d. The groups treated with UV-C radiation exhibited an increase in ty-

EFFECTS OF ULTRAVIOLET LIGHT ON CHICKEN MEAT QUALITY

MATERIALS AND METHODS Trial 1: Exposure of Inoculated Chicken Meat to UV-C Irradiation A pooled suspension of Salmonella Enteritidis (ATCC 13076), Salmonella Typhi (ATCC 19214), Salmonella Typhimurium (ATCC 14028), Salmonella Gallinarum (ATCC 9184), and Salmonella Arizonae (ATCC 13314), serotypes obtained from the Fiocruz Institute (Rio de Janeiro, Brazil), was prepared according to Sant’Ana et al. (2012). The lyophilized serotypes were individually rehydrated in brain heart infusion broth, and incubated at 37°C for 24 h, twice. The live cultures were centrifuged at 1,000 × g at 4°C for 15 min and the pellet

was washed 3 times with PBS. Aliquots representing equal amounts of each strain were combined to obtain a mixed inoculum solution. The bacterial concentrations (1 mL = approximately 5.0 × 108 cells) were determined using a UV spectrophotometer (Smartspec Plus, BioRad, Hercules, CA) at 600 nm. To determine the most efficient time of UV-C exposure to reduce the bacterial load, 39 frozen chicken breast tenderloins (M. pectoralis profundus) were purchased from a retail market in Niteroi, Brazil. All samples exhibited absence of Salmonella spp. before the inoculation. The chicken meat was thawed at 4°C for 24 h, then the breast tenderloins were individually packaged in 20 × 15 cm, 0.16 µm thickness polyvinyl chloride film (ECO-N-VAC, Deltaplam Ltda., Paraná, Brazil). The PVC film was initially tested and exhibited proper physicochemical properties for the UV-C irradiation. One milliliter of the inoculum was spotted onto the surface of each breast, spread using a sterile Drigalski glass spatula, and then the packages were sealed (TECMAQ, AP 450, Sao Paulo, Brazil) and held at 20°C for 15 min before being exposed to the UV-C irradiation. Inoculated chicken meat samples were randomly distributed into 13 groups with 3 replicates. The experimental design included the exposure of 3 UV-C light intensities (0.62, 1.13, and 1.95 mW/cm2) for 4 times (30, 60, 90, and 120 s) and 1 control (inoculated and no UV-C exposure). Following the UV-C exposure, Salmonella spp. content was determined. For that, 25 g of meat from the inoculated surface were homogenized with 225 mL of 0.1% peptone water using a stomacher (Stomacher 80, Seward, London, UK), followed by an 8-fold serial dilution in peptone water. Aliquots of 0.1 mL were inoculated in duplicate on Salmonella-Shigella agar (HiMedia, Mumbai, India) using the spread plate technique. The plates were incubated at 37°C for 48 h, and the results were expressed as log cfu per gram (APHA, 2001).

Trial 2: Effect of UV-C Irradiation on Quality Attributes The effects of UV-C irradiation on biogenic amine content, bacteriological load, pH, lipid oxidation, and color parameters of chicken meat storage at 4°C were determined. Chicken breast tenderloins were purchased, conditioned, and packed in the same conditions related in trial 1. Eighty-four chicken breasts were assigned into 3 groups: T1 (0.62 mW/cm2), T2 (1.13 mW/cm2), and T3 (1.95 mW/cm2) and submitted for 90 s based on the results of the first trial. In addition, a control group received no UV-C irradiation. All groups were evaluated with 3 replicates. Samples were stored for 9 d, and values of biogenic amines, bacteriological load, pH, lipid oxidation, and color parameters were performed at d 0, 3, 5, 6, 7, 8, and 9. Biogenic Amine Quantification. The method was conducted according to Lázaro et al. (2013). Chicken breast (5 g) was homogenized with perchloric acid

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well as meat (fish and chicken) products (Guerrero-Beltrán and Barbosa-Cánovas, 2004). The beneficial effect of UV-C light on chicken meat has already been evaluated (Wallner-Pendleton et al., 1994; Kim et al., 2002; Lyon et al., 2007). The aforementioned authors reported that UV light efficiently decreased the pathogenic bacterial load on the carcass surface without negatively affecting carcass color or meat lipid oxidation. On the other hand, Koutchma et al. (2009) determined that UV light potentially affects food products due to free radical generation via a wide variety of organic photochemical reactions. Possible undesirable effects include oxidation of vitamins, lipids and proteins, degradation of antioxidants, changes in texture and color, and formation of off-flavors and aromas. Biogenic amines are low molecular weight products of specific amino acid decarboxylation reactions promoted by bacterial enzymes during storage (Silla Santos, 1996). The formation of biogenic amines depends on the free amino acid profile present in the food matrix and the identity of the microorganisms; thus, biogenic amines potentially indicate microbial development (Vinci and Antonelli, 2002). Balamatsia et al. (2006) observed that some biogenic amines and bacterial groups (total viable count and Enterobacteriaceae) increased in chicken meat during refrigerated storage. These authors proposed the sum of putrescine, cadaverine, and tyramine as bacteriological quality indicators. Although there is limited information regarding the effects of UV-C light on biogenic amines, other technologies such as gamma irradiation promoted changes such as fragmentation, coagulation, cross-linking, and oxidation on proteins and amino acids; this could be a reason why irradiation increases the content of certain biogenic amines (Min et al., 2007). The objectives of this study were to determine: 1) the most efficient UV-C exposure time for bacterial load reduction in chicken meat inoculated with Salmonella serotypes and 2) the effect of UV-C light on biogenic amines, total aerobic mesophilic bacteria, Enterobacteriaceae, pH, lipid oxidation, and instrumental color parameters in chicken meat during the storage at 4°C.

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lyzed using a CR-400 Chroma Meter (Minolta, Osaka, Japan) at 3 different locations on the skin side of the breast tenderloins, and expressed as CIE L* (lightness), a* (redness), and b* (yellowness; Canto et al., 2012).

UV-C Equipment Specifications A stainless steel barrel-shaped chamber was constructed to perform the experiments (Figure 1). Twelve UV-C lamps (6 of 30 W and 6 of 55 W; OSRAM HNS, OFR, Munich, Germany) were placed longitudinally around the chamber’s inner surface using a balanced pattern. Samples were placed at the geometrical center of the chamber using the aid of a nylon net. Two electrical switches were installed to control each lamp power individually. The evaluated intensities were 0.62 mW/cm2 (30 W lamps), 1.13 mW/cm2 (55 W lamps), and 1.95 mW/cm2 (30 and 55 W lamps); these values were determined using an UV radiometer (MRUR-203, Instrutherm Ltda., São Paulo, Brazil) placed inside the polyvinyl film used to package the chicken meat. Different locations inside the irradiation chamber throughout the nylon net were tested by the UV radiometer to determine the highest radiance spot. The UV-C irradiation was performed in a dark room to minimize the bacterial photo reactivation. Each breast was placed in a central area (10 × 40 cm2) of the nylon net 14 cm from the UV-C sources.

Statistical Analysis For the first trial (UV-C intensities × time of exposure), the statistical differences in Salmonella species reduction were conducted with ANOVA at a 5% confidence level for the Tukey test. For the second trial, variances in all parameters tested (biogenic amines, color values, lipid oxidation, pH, TAMB, and Enterobacteriaceae) were carried out according to UV-C intensity levels (control, 0.62, 1.13, and 1.95 mW/cm2), days of storage (0, 3, 5, 6, 7, 8, 9), and interaction between the variables with ANOVA at a 5% confidence level for the Tukey test. All analyses were performed using GraphPad Prism 5 (Graphpad Software Inc., San Diego, CA). Bacterial growth parameters (lag phase and generation time) were assessed using the Baranyi and Roberts (1994) model performed in DMFit predictive microbiology software (available at http://www. combase.cc).

RESULTS AND DISCUSSION Time of UV-C Exposure in Inoculated Chicken Meat Our data demonstrated that the increase on the UV-C intensity and the exposure time promoted an increase on the bacterial log reduction (Table 1). All intensities tested for 90 and 120 s increased (P < 0.05) the log reduction on Salmonella spp. inoculated on chicken meat.

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5%, following alkalization with NaOH (pH > 12), and then derivatized with benzoyl chloride (40 μL). The mixture was extracted using diethyl ether and concentrated through nitrogen evaporation. The dry extract was dissolved in 1,000 μL of mobile phase (42:58 of acetonitrile:water) and stored at 4°C. The chromatographic system consisted of a Shimadzu Prominence UFLC apparatus (Shimadzu, Kyoto, Japan) equipped with a DGU-20A5 degasser, a SIL20AC auto sampler, a LC-20AD quaternary pump, a CTO-20A column oven, a SPD-M20A diode array detector, and a CBM-20A communication bus module. Amine separations were performed on a C18 Spherisorb ODS2 (15 × 0.46 cm i.d., 5 μm, Waters) column equipped with a Supelco Ascentis C18 (2 × 0.40 cm, i.d. 5 μm) guard column, under isocratic conditions. The mobile phase consisted of 42:58 (vol/vol) of acetonitrile (Tedia) and ultrapure water (Simplicity-Millipore, Molsheim, France), previously degassed in an ultrasonic bath (Cleaner USC 2800 A, São Paulo, Brazil). The chromatography conditions were 1 mL/min of flow rate, 20 µL of injection volume, and column temperature of 20°C. Benzoylated polyamines were detected using UV absorption at 198 nm after a total run time of 15 min. A 10 min cleaning step between each injection was performed using 100% acetonitrile. The biogenic amines were identified by their specific retention time and quantified by peak area using external standards. Bacteriological Analysis. All analyses were conducted using standard microbiological methods (APHA, 2001). Total aerobic mesophilic bacteria (TAMB) and Enterobacteriaceae were evaluated using serial dilutions of 25 g of sample homogenized with 225 mL of 0.1% peptone water. Plate count agar and violet red bile glucose agar were used to determine TAMP and Enterobacteriaceae contents, respectively. Results were expressed as log cfu per gram. pH. Ten grams of each sample were homogenized with 90 mL of distilled water, and then the pH values were determined using a digital pH meter (Digimed DM-22) equipped with a DME-R12 electrode (Digimed; ConteJúnior et al., 2008). Lipid Oxidation. Determination of the lipid oxidation was performed using the distillation method of 2-TBA reactive substances (TBARS) according to Tarladgis et al. (1960) and modified by Monteiro et al. (2012). Briefly, 10 g of meat was added to a solution of 97.5 mL of distilled water and 2.5 mL of HCl (4 N) following homogenization and distillation. Five milliliters of the distillate was added to 5 mL of 0.02 M TBA and heated in water bath 100°C for 35 min. The solutions were cooled and the absorbance was measured at 528 nm on a Smartspec Plus spectrophotometer (BioRad, Hercules, CA). The results were expressed as milligrams of malondialdehyde (MDA) per kilogram of sample (mg of MDA/kg). Instrumental Color. Breast samples were held at 20°C for 30 min for color blooming before the measurement. The instrumental color parameters were ana-

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Typhimurium using 82.5 mW/cm2 for 60 s. Based on the results from trial 1 (Table 1), 90 s of exposure time was the most efficient irradiation duration.

Despite the limited capacity to penetrate the product surface, UV-C is a feasible germicidal technology to reduce pathogenic bacteria (Guerrero-Beltrán and Barbosa-Cánovas, 2004). Our results are in agreement with Sommers et al. (2010), who reported a log reduction between 0.4 and 0.6 of Salmonella spp. using 2 to 4 J/cm2 doses in boneless skinless chicken breasts and chicken drumsticks. In addition, Haughton et al. (2011) documented that chicken meat irradiated with UV-C at 6 mW/cm2 for 32 s exhibited a reduction of 1.34 log cfu/g of Salmonella Enteritidis. Nonetheless, WallnerPendleton, Sumner, Froning and Stetson (1994) irradiated broiler whole carcasses with UV-C irradiation and reported a reduction of 0.5 log cfu/g of Salmonella

Effect of UV-C Irradiation on Chicken Meat During Storage Time at 4°C Biogenic Amines. All groups showed similar (P > 0.05) values for tyramine content up to d 6 of storage, from which T2 and T3 exhibited an increase (P < 0.05) compared with the other groups (Table 2). These differences were maintained during the rest of the storage time. Values of putrescine were less than 1 mg/ kg for the first 3 d of storage in all groups (P > 0.05);

Table 1. Log reductions1 (mean ± SD) of bacterial mix (Salmonella Enteritidis, Salmonella Typhi, Salmonella Typhimurium, Salmonella Gallinarum, and Salmonella Arizonae) inoculated in chicken breast meat after different UV-C intensities and time of exposures2,3 Treatment time (s) UV-C intensity (mW/cm2) 0.62 1.13 1.95 a–cAt

30 0.14 ± 0.18 ± 0.34 ±

0.01c 0.04b 0.03b

60 0.34 ± 0.28 ± 0.42 ±

0.03b 0.01ab 0.02b

90 0.38 ± 0.33 ± 0.60 ±

0.03ab 0.07ab 0.03a

120 0.48 ± 0.04a 0.36 ± 0.02a 0.57 ± 0.01a

the same intensity (row), values not followed by the same letter are significantly different (P < 0.05). of inoculated sample non-UV treated – log of inoculated sample UV treated. 2Chicken meat inoculated and non-UV treated = 7.28 ± 0.02 log cfu/g. 3Results are the average of 3 samples. 1Log

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Figure 1. Layout of UV-C instrument. (a) Stainless-steel irradiation chamber. (b) Internal dispositions of UV-C lamps. (c) Nylon net used to put the samples. All dimension values in centimeters.

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To the best of our knowledge, there is a lack of information regarding the evaluation of the behavior of biogenic amines in meat irradiated with UV-C. Still, our results were compared with other reports that adopt biogenic amines as a quality indicator for meat. Balamatsia et al. (2006) observed a constant increase in tyramine (0.02–4 mg/kg), putrescine (58–409 mg/kg), cadaverine (19–252 mg/kg), and histamine (not determined to 19 mg/kg) contents in chicken meat during 17 d of refrigerated storage at 4°C. Bacteriological Analysis. During the refrigerated storage, T3 (1.95 mW/cm2) was the only group that exhibited an effect (P < 0.05) on TAMB and Enterobacteriaceae content. Groups T1 (0.62 mW/cm2), T2 (1.13 mW/cm2), and control demonstrated a decline phase after d 7, whereas T3 (1.95 mW/cm2) continued to increase (Figure 2A). Similar results were observed on Enterobacteriaceae content in all UV-C intensities in which the irradiation promoted a similar log phase up to d 8; after that, T1, T2, and control groups exhibited a decline phase, whereas T3 continued to increase (Figure 2B). The growth curves for both bacteria groups were fitted on the Baranyi growth model to estimate the shelf life, lag phase, generation time, and number of cells in the stationary phase (Baranyi and Roberts, 1994). According to our data (Table 3), only T3 (1.95 mW/ cm2) exhibited a slight decrease in the lag phase, and an increased generation time on both bacterial groups. Considering 7 log cfu/g value as the maximum limit for the product shelf life (Senter et al., 2000), only T3 (1.95 mW/cm2) promoted an extension on the shelf life of chicken breast samples stored at 4°C. The effects of UV light on microorganism populations depend on several parameters such as species, strain, growth media, composition of the food, and density of microorganisms (Guerrero-Beltrán and Barbosa-Cánovas, 2004). Ultraviolet irradiation is only effective on the bacteria present at the surface of the product; thus, the bacteria present inside the food matrix are shielded against the UV-C light and are not affected by this type of treatment. Korhonen et al. (1981) evaluated the effect of brief exposure of high intensity UV-C light on the microbial survivability on beef and observed that the irregular surface provides physical protection against irradiation. Our results are in agreement with Yndestad et al. (1972) who evaluated the effect of 10 mW/cm2 at 12.8 s on chicken carcasses and observed that UV-C light had an immediate effect on the bacterial reduction present at the surface. Huang and Toledo (1982) showed an initial reduction of 2 to 3 log microbial content on mackerel fish irradiated with 0.3 mW/cm2 for 16.6 min, and 120 to 180 mW/cm2 for 40 s, promoting an extension on the product’s shelf life. Lipid Oxidation. The TBARS values increased from 0.14 to 016 to 0.38 to 0.40 mg of MDA/kg during refrigerated storage in all treatments (P < 0.05; Table

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after that, a slight increase (4–6 mg/kg) was observed. Concentrations rapidly increase at d 6, 7, and 8 for T1 and T2, control, and T3, respectively. All groups had a steady increase on putrescine content until the end of storage (P < 0.05). Similarly, cadaverine contents were less than 1 mg/kg at the first 5 d of storage in all groups. Groups irradiated with UV-C exhibited a dramatic increase at d 6, whereas in the control group a similar increase started at d 7. Based on these data, all groups demonstrated an increase (P < 0.05) of cadaverine content until the end of storage. The UV-C irradiation promoted an increase on the initial values of spermidine. In addition, during the storage these values gradually increased in control, T1 (0.62 mW/cm2), and T2 (1.13 mW/cm2) groups (P < 0.05), whereas T3 (1.95 mW/cm2) exhibited a slight decrease (P < 0.05). Furthermore, initial values of histamine and spermine decreased (P < 0.05) in T2 (1.13 mW/cm2) and T3 (1.95 mW/cm2). Because biogenic amines are products of specific amino acid decarboxylation reactions with bacterial enzymes during storage, it was expected that reducing bacteria loads due to UV-C light exposure would lead to lower levels of biogenic amines. Controversially, in our study some biogenic amines exhibited an increase. These results are potentially associated with other effects of UV irradiation such as interaction with free amino acids. Koutchma et al. (2009) documented that UV light promoted degradation of essential amino acids (histidine, phenylalanine, and tryptophan), and influenced protein due to complex photochemical reactions leading to changes on solubility, heat sensitivity, mechanical properties, and hydrolysis. Based on this statement, UV-C irradiation potentially increased the availability of free amino acids. Løvaas (1991) proposed another interesting hypothesis for the biogenic amine increase. He concluded that the cellular stress state influences the polyamine activity as antioxidatives. Polyamines have the ability to scavenge superoxide and hydroxyl radicals produced by UV-C exposure. Their participation in cell membrane stabilization, cell proliferation, and protein synthesis has been already documented (Stadnik and Dolatowski, 2010). Although the effect of UV-C on biogenic amines is yet to be studied in meat, its effect has already been reported in plants (Kondo et al., 2011), in which the putrescine and spermine contents increased in apples irradiated with UV-C; it showed the role of polyamines in protection against oxidative stress. Values of spermine and spermidine usually remain stable or gradually decrease during storage. Some authors justify this observation as these polyamines are naturally present in fresh meat (Hernández-Jover et al., 1997; Ruiz-Capillas and Jiménez-Colmenero, 2004). In addition, polyamines are a source of nitrogen for microorganisms (Bardócz, 1995). Nonetheless, this pattern was not observed in our experiment as both amines showed an increase.

± ± ± ±

± ± ± ±

± ± ± ±

± ± ± ±

± ± ± ±

0.32 0.69 0.65 0.77

0.01 0.11 0.05 0.01

0.47 2.08 2.03 1.94

3.35 2.48 0.46 1.01

2.02 0.37 0.10 0.07

0.23 0.67 0.53 1.08 0.46 0.37 0.17 0.86 0.36 0.01 0.01 0.10 0.66 2.70 2.22 1.46 5.61 5.68 1.82 1.66 2.02 0.02 0.01 0.01

0.54B,d 0.12B,d 0.02B,d 0.05A,c

0.01A,f 0.06A,f 0.15A,e 0.09A,f

0.01A,f 0.13A,d 0.07A,d 0.01A,f

0.02B,c 0.37A,e 0.12A,c 0.01A,a

0.06A,d 0.28A,e 0.16C,d 0.04B,f

0.01A,c 0.15B,bc 0.00C,d 0.00C,c

  0.06C,d 0.03B,d 0.00B,d 0.28A,c   ± 0.18A,f ± 0.04A,f ± 0.00A,f ± 0.25A,f   ± 0.29A,e ± 0.00A,e ± 0.00A,d ± 0.11A,f   ± 0.26C,c ± 0.01A,c ± 0.01A,b ± 0.08B,c   ± 0.57A,c ± 0.02A,d ± 0.08B,c ± 0.41B,e   ± 0.01A,c ± 0.00B,d ± 0.00B,e ± 0.01B,c

± ± ± ±

3

2.14 0.36 0.26 0.15

6.06 6.14 2.04 2.33

2.04 2.11 2.11 1.64

0.78 0.29 0.02 0.36

5.18 4.10 6.64 6.38

3.17 2.30 2.68 4.23

  0.91A,c 0.18A,c 0.41A,c 0.93A,b   ± 0.30A,e ± 0.15A,e ± 0.25A,d ± 0.20A,e   ± 0.17A,e ± 0.06A,d ± 0.01A,d ± 0.03A,e   ± 0.08A,b ± 0.10A,e ± 0.01A,c ± 0.04B,b   ± 0.04A,c ± 0.13A,c ± 0.04B,c ± 0.21B,e   ± 0.03A,b ± 0.06B,c ± 0.01C,c ± 0.04D,b

± ± ± ±

5

2.13 0.37 0.82 0.11

6.04 6.48 5.89 3.06

2.91 2.55 2.35 1.64

67.10 355.43 457.70 217.19

15.68 123.37 141.45 17.03

2.74 2.67 5.91 5.80

  ± 0.04B,c ± 0.62B,c ± 0.13A,b ± 0.04A,b   ± 0.42C,d ± 0.52B,d ± 7.16A,c ± 0.15C,d   ± 1.36C,d ± 1.27B,c ± 1.87A,c ± 15.59C,d   ± 0.03A,a ± 0.01A,d ± 0.06A,ab ± 0.16B,bc   ± 0.03B,c ± 0.10A,c ± 0.10C,b ± 0.00D,d   ± 0.05A,b ± 0.23C,bc ± 0.11B,a ± 0.00C,b

6

2.17 0.25 0.92 0.35

17.17 15.26 5.52 5.41

2.05 3.91 2.94 1.73

643.73 515.27 693.03 503.20

275.50 139.52 196.15 66.51

3.16 3.75 7.42 5.58

  ± 0.16C,bc ± 0.03C,b ± 1.25A,b ± 0.40B,b   ± 3.46A,b ± 0.32C,c ± 0.23B,b ± 12.98D,c   ± 5.62B,c ± 17.32C,b ± 2.74A,b ± 3.81C,c   ± 0.65C,b ± 0.18A,b ± 0.21B,a ± 0.25C,bc   ± 1.56A,b ± 0.75A,b ± 0.16B,b ± 0.00B,c   ± 0.06A,b ± 0.14C,c ± 0.03B,a ± 0.05C,a

7

followed by different uppercase letters in the same column and different letters in the same row are significantly different (P < 0.05). (0.62 mW/cm2), T2 (1.13 mW/cm2), and T3 (1.95 mW/cm2).

± ± ± ±

0.42 0.49 0.51 1.07

0

Storage time (d)

1.98 0.45 0.75 0.34

27.67 17.89 17.55 15.59

1.97 4.34 2.96 1.11

723.29 549.93 701.58 892.98

255.41 144.47 196.15 320.93

3.74 3.50 10.20 9.39

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1T1

A–D,a–fValues

Tyramine   Control (0.00)   T1 (0.62)   T2 (1.13)   T3 (1.95) Putrescine   Control (0.00)   T1 (0.62)   T2 (1.13)   T3 (1.95) Cadaverine   Control (0.00)   T1 (0.62)   T2 (1.13)   T3 (1.95) Spermidine   Control (0.00)   T1 (0.62)   T2 (1.13)   T3 (1.95) Histamine   Control (0.00)   T1 (0.62)   T2 (1.13)   T3 (1.95) Spermine   Control (0.00)   T1 (0.62)   T2 (1.13)   T3 (1.95)

Group1 (mW/cm2)   ± 0.62B,bc ± 0.17B,b ± 0.15A,a ± 0.45A,a   ± 7.81B,c ± 0.35D,b ± 0.23C,b ± 2.18A,b   ± 15.26B,b ± 12.20C,b ± 6.15B,b ± 19.12A,b   ± 0.28C,b ± 0.26A,ab ± 0.11B,a ± 0.01D,d   ± 0.91A,a ± 0.29B,b ± 1.72BC,a ± 0.42C,b   ± 0.22A,c ± 0.07BC,b ± 0.28B,ab ± 0.04C,a

8

Table 2. Changes in biogenic amines (mg/kg) of chicken meat subjected to different UV-C intensities (90 s exposure) and storage during 9 d at 4°C

2.92 0.74 0.66 0.41

30.07 25.65 18.84 18.77

2.12 4.71 2.83 1.23

767.13 894.44 1,084.11 1,029.60

304.49 537.10 646.19 577.78

6.94 6.70 10.76 8.99

  ± ± ± ±   ± ± ± ±   ± ± ± ±   ± ± ± ±   ± ± ± ±   ± ± ± ±

9

0.18A,a 0.08B,a 0.08B,b 0.01C,a

1.22A,a 2.40B,a 0.22C,a 0.95C,a

0.18C,b 0.04A,a 0.49B,a 0.14D,d

4.18D,a 0.68C,a 9.77A,a 24.86B,a

2.81D,a 1.27C,a 2.35A,a 2.85B,a

0.78B,a 0.43B,a 1.33A,a 1.39A,a

EFFECTS OF ULTRAVIOLET LIGHT ON CHICKEN MEAT QUALITY

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Table 3. Shelf life and growth parameters of microorganisms in chicken breast meat submitted 90 s to UV-C light during the storage Total aerobic mesophilic bacteria Group1 (mW/cm2) Control (0.00) T1 (0.62) T2 (1.13) T3 (1.95)

Enterobacteriaceae

Shelf life2

Lag phase (d)

Stationary phase3

Generation time (h)

Shelf life2

Lag phase (d)

Stationary phase3

Generation time (h)

6.40 6.40 6.40 7.10

3.66 3.69 3.89 3.47

8.39 8.20 8.36 8.08

0.10 0.10 0.09 0.13

6.90 6.90 7.30 7.60

4.24 4.26 4.38 4.38

8.49 7.99 7.97 8.11

0.13 0.13 0.13 0.15

1T1

(0.62 mW/cm2), T2 (1.13 mW/cm2), and T3 (1.95 mW/cm2). to reach 107 cfu/g. 3Number of cells (log cfu/g) at the stationary phase. 2Days

on the initiation of lipid autoxidation, including the presence of oxygen, transition metals, peroxides, free radicals, light irradiation, heat, and enzymes such as

Figure 2. Effect of different UV-C intensities for 90 s on bacterial load in chicken meat storage at 4°C during 9 d. Values in parentheses correspond to UV-C intensities expressed in milliwatt per centimeter2.

Downloaded from http://ps.oxfordjournals.org/ at Purdue University Libraries ADMN on September 1, 2014

4). No difference (P > 0.05) was observed on TBARS values among the groups for most of the analyzed days (P > 0.05). Several factors are potentially involved

  0.1A,b 0.0B,c 0.0A,a 0.0A,a   ± 0.03A,a ± 0.02A,a ± 0.01A,a ± 0.02A,a 0.36 0.38 0.39 0.40

  0.0A,ab 0.0A,a 0.0B,b 0.0C,c   ± 0.01A,b ± 0.01A,b ± 0.00A,b ± 0.01A,ab A–C,a–dValues

followed by different uppercase letters in the same column and different lowercase letters in the same row are significantly different (P < 0.05).

0.30 0.31 0.32 0.34 0.27 0.28 0.30 0.31 0.19 0.21 0.26 0.27 0.13 0.14 0.16 0.16 0.01B,d 0.02A,dc 0.01A,d 0.02A,c ± ± ± ± 0.11 0.17 0.18 0.19 0.01A,cd 0.01A,d 0.02A,d 0.01A,c ± ± ± ± 0.14 0.14 0.16 0.16

6.0 6.3 5.9 6.3   0.0A,a 0.0A,a 0.0B,b 0.0B,a ± ± ± ± 6.5 6.4 6.3 6.3

pH   Control (0.00)   T1 (0.62)   T2 (1.13)   T3 (1.95) TBARS (mg of malondialdehyde/kg)   Control (0.00)   T1 (0.62)   T2 (1.13)   T3 (1.95)

± ± ± ±

  0.0B,d 0.0A,bc 0.0B,d 0.0A,a

6.1 6.1 6.2 6.2

± ± ± ±

  0.0B,c 0.0B,d 0.0A,c 0.0A,b   ± 0.01A,d ± 0.01A,d ± 0.02A,d ± 0.01A,c

6.2 6.2 6.3 6.2

± ± ± ±

  0.0B,c 0.0B,c 0.0A,b 0.0B,b   ± 0.01B,c ± 0.01B,c ± 0.01A,c ± 0.01A,b

6.2 6.3 6.3 6.1

± ± ± ±

  0.0B,c 0.0A,ab 0.0A,b 0.0C,c   ± 0.01A,b ± 0.00A,b ± 0.01A,b ± 0.04A,b

6.4 6.4 6.3 6.0

± ± ± ±

8 7 6 5 3 0 Group (mW/cm2)

Storage time (d)

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lipooxygenases (Namiki, 1990). Nonetheless, our results demonstrated that UV-C irradiation did not affect the TBARS values, potentially because the exposure periods were not enough to promote oxidation. Our results were similar to other reports that evaluated the effect of UV-C light. Wallner-Pendleton, Sumner, Froning and Stetson (1994) documented that after d 10 of refrigerated storage at 7°C, the UV treated chicken thigh meat exhibited 1.3 mg of MDA/kg of TBARS values, whereas the control samples had 1.7 mg of MDA/kg. Similarly, Chun et al. (2010) observed that the TBARS value of the chicken breasts slowly increased during storage, regardless of the UV-C dose applied. Furthermore, lipid oxidation occurs during storage regardless of the UV-C light. Lázaro et al. (2012) observed that chicken meat from different rearing systems exhibited a gradual increase in TBARS values during 18 d of refrigerated storage at 4°C; the values did not exceed 0.5 mg of MDA/kg at the end of the experiment. Alasnier et al. (2000) documented low initial levels of lipid oxidation (0.03 mg of MDA/kg) followed by a linear increase to 0.30 mg of MDA/kg in chicken breast meat at d 14 of refrigerated storage. pH. According to our data (Table 4), UV-C treatments exhibited slight pH value variations during refrigerated storage. The T1 (0.62 mW/cm2) and control groups had greater pH values on d 1 than T2 (1.13 mW/cm2) and T3 (1.95 mW/cm2) groups (P < 0.05). At the end of the storage, whereas most groups did not demonstrate changes on their pH values, T1 (1.95 mW/ cm2) samples exhibited a decrease in their pH values (P < 0.05). Chun et al. (2010) reported no increase in the initial pH values (ranging from 6.24 to 6.45) among the UV-C irradiated chicken meat. Instrumental Color. At the beginning of the experiment only the T3 (1.13 mW/cm2) treatment exhibited greater L* values than the other groups (P < 0.05; Table 5). Groups T2 (1.13 mW/cm2) and T3 (1.95 mW/cm2) promoted a decrease in the L* values (P < 0.05) after d 9 of refrigerated storage. The different intensities of UV-C irradiation did not affect the initial a* values (P > 0.05). However, during the refrigerated display all treatments exhibited a slight decrease in a* values compared with the initial values (P < 0.05). Initial b* values in groups T2 (1.13 mW/cm2) and T3 (1.95 mW/cm2) were lower than T1 (0.62 mW/cm2) and control groups (P < 0.05). All treatments exhibited a gradual decrease on the b* values during storage (P < 0.05). Color is an important sensory characteristic of foods and often indicates the quality and freshness of a food product (Meilgaard et al., 2007). Our results were similar to those documented by Wallner-Pendleton et al. (1994), who also reported a slight effect on b* values in chicken meat during 10 d of refrigerated storage. In addition, Lyon et al. (2007) observed a small effect on a* values in breast chicken fillets after d 7 of UV-C exposure (1,000 μW/cm2 for 5 min). Nonetheless, Chun et al. (2010) reported that UV-C irradiation promoted

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Table 4. Changes in pH and TBA reactive substances (TBARS) of chicken submitted 90 s to different UV-C intensities and storage during 9 d at 4°C

6.3 6.1 6.4 6.3

± ± ± ±

9

EFFECTS OF ULTRAVIOLET LIGHT ON CHICKEN MEAT QUALITY

± ± ± ± 10.22 10.00 12.55 13.37

15.43 15.28 16.27 15.57

± ± ± ±

  1.78AB,ab 1.27A,a 0.73B,ab 0.31B,b   0.25B,b 0.30B,b 0.14A,b 0.29B,b   0.51C,c 0.24C,c 0.15B,b 0.64A,b   0.62A,a 1.01A,a 2.71B,b 0.68AB,b   ± 1.05B,b ± 1.58B,b ± 0.93A,b ± 1.03A,ab   ± 0.05B,c ± 0.98B,c ± 0.81A,ab ± 0.55A,b 13.60 14.45 12.20 13.62

15.74 15.26 16.94 16.98

12.58 15.76 13.90 15.60

16.02 15.28 15.09 15.40

14.00 16.29 13.69 14.37

15.76 15.10 16.52 16.42

15.27 16.78 14.19 15.25

15.59 15.74 15.70 15.94

16.78 16.08 14.72 15.40

18.35 17.68 19.01 18.20

followed by different uppercase letters in the same column and different lowercase letters in the same row are significantly different (P < 0.05). A–C,a–cValues

9.68 10.80 12.75 13.79

14.66 14.20 16.63 16.36

  1.46B,ab 1.03A,a 1.54B,b 1.36B,b   ± 0.43B,b ± 0.76B,b ± 1.45AB,b ± 0.25A,ab   ± 0.94A,b ± 0.35A,b ± 0.49B,b ± 0.79A,b   2.67A,b 0.68A,b 0.50A,b 0.58A,b   ± 0.61A,b ± 0.39A,b ± 0.85A,b ± 0.51A,b   ± 0.73B,b ± 0.97A,a ± 0.98AB,a ± 0.68A,b L*   Control (0.00)   T1 (0.62)   T2 (1.13)   T3 (1.95) a*   Control (0.00)   T1 (0.62)   T2 (1.13)   T3 (1.95) b*   Control (0.00)   T1 (0.62)   T2 (1.13)   T3 (1.95)

55.66 56.51 57.20 58.30

± ± ± ±

  0.19B,a 1.04AB,a 2.43AB,a 1.53A,a   ± 1.02A,a ± 0.75A,a ± 0.48A,a ± 1.67A,a   ± 0.54A,a ± 0.22AB,a ± 0.48C,a ± 0.51BC,a

53.31 53.12 55.67 53.96

± ± ± ±

  1.74A,ab 0.62A,b 0.96A,a 1.59A,b   ± 0.64A,b ± 0.82A,ab ± 0.35A,b ± 0.71A,b   ± 0.70A,b ± 0.22A,a ± 0.91A,ab ± 0.73A,a

53.43 51.21 53.98 53.83

± ± ± ±

  0.92A,ab 1.30A,b 1.12A,ab 0.92A,b   ± 0.26A,b ± 0.79A,b ± 0.70A,b ± 0.82A,ab   ± 0.55B,b ± 0.15A,a ± 0.56B,a ± 0.12A,a

50.93 51.16 52.33 53.35

± ± ± ±

6 5 3 0 Group (mW/cm2)

Storage time (d)

52.53 56.91 51.27 51.91

± ± ± ±

7

55.20 54.37 51.34 53.88

± ± ± ±

8

54.12 55.47 52.68 53.36

± ± ± ±

9

Lázaro et al.

an increase on the a* values of chicken breast after d 6 of refrigerated storage. Based on our results, the intensity of 1.95 mW/cm2 decreased the levels of pathogenic bacteria and can be used as a nonthermal technology to improve the superficial quality of packed poultry meat without promoting relevant changes on some quality indicators. The use of biogenic amines as a freshness indicator in meat subjected to UV-C light must be further studied as this technology promoted the increase of some amines. Thus, it is not suitable to evaluate product freshness based only biogenic amines values on chicken meat irradiated with UV-C. Further studies should be conducted to determine the effect of the ratio between intensity and exposure time to develop a feasible technology for industry production.

ACKNOWLEDGMENTS The authors are thankful for the financial support of the Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ, Rio de Janeiro, Brazil), process numbers E-26/111.610/2010 and E-26/103.003/2012. The authors C. A. Lázaro, A. C. V. C. S. Canto, B. R. C.Costa Lima were supported by the scholarships provided by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil). The author M. L. G. Monteiro was supported by the scholarship provided by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil). Finally, grateful acknowledgments are made to I. Y. Yanque Tomasevich (Department of Electrical Engineering/COPPE, Federal University of Rio de Janeiro, Brazil) for the assistance drawing Figure 1.

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Table 5. Changes in Commission Internationale d’Eclairage color (lightness, L*; redness, a*; yellowness, b*) of chicken meat submitted for 90 s to different UV-C intensities and storage during 9 d at 4°C

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