ORIGINAL ARTICLE. B.S.M. Mahmoud. Abstract

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1 Letters in Applied Microbiology ISSN -5 ORIGINAL ARTICLE Inactivation effect of X-ray treatments on Cronobacter species (Enterobacter sakazakii) in tryptic soy broth, skim milk, low-fat milk and whole-fat milk * B.S.M. Mahmoud Costal Research and Extension Center, Mississippi State University, Pascagoula, MS, USA Keywords Cronobacter (E. sakazakii), low-fat milk, skim milk, whole-fat milk, X-ray. Correspondence Barakat S.M. Mahmoud, Coastal Research & Extension Center, Mississippi State University, 311 Frederic St., Pascagoula, MS 3957, USA. bm57@msstate.edu * This paper is journal article of the Mississippi Agriculture and Forestry Experiment Station. 9 7: received April 9, revised 1 July 9 and accepted July 9 doi:1.1111/j.17-75x.9.7.x Abstract Aims: To determine the inactivation effect of X-ray treatments on Cronobacter (E. sakazakii) in tryptic soy broth (TSB), skim milk (% fat), low-fat milk (1% and %) and whole-fat milk (3Æ5%). Methods and Results: X-rays were produced using the RS generator system (Rad Source Technologies Inc.). Cronobacter (in TSB), inoculated skim milk (% fat), low-fat milk (1% and % fat) and whole-fat milk (3Æ5% fat) were treated with Æ, Æ1, Æ5, Æ75, 1Æ, Æ, 3Æ, Æ, 5Æ and Æ kgy X-ray doses. Surviving bacteria in the TSB and inoculated milk, before and after treatment, were enumerated using plating method onto trypticase soy agar. Greater than 7Æ-log CFU reduction in Cronobacter population was observed with Æ, 5Æ, Æ, Æ and Æ kgy X-ray in the TSB, skim milk, 1% fat milk, % fat milk and 3Æ5% fat milk, respectively. Conclusions: Treatment with X-rays significantly (P <Æ5) reduced Cronobacter to less than detectable limits (<1 log CFU ml )1 ) in skim milk at 5Æ kgy and milk with 1% fat content and greater at Æ kgy dose levels. The D-value for Cronobacter in TSB was significantly (P <Æ5) lower than those in milk samples. Significance and Impact of the Study: Treatment with X-rays could be an effective and safe alternative technology to control pathogenic bacteria (Cronobacter) in the dairy industry. Introduction Milk and other dairy products are healthy foods that provide us with high-quality protein, minerals (calcium, phosphorous, magnesium, iodine and zinc), vitamins (B1, A, C and riboflavin) and omega-3 fatty acids (Wiley 5; Adebamowo et al. ). The nutritional value of these foods is such that, as part of a healthy diet, it is recommended that three servings of dairy products such as milk, yogurt and cheese be eaten every day (Popkin et al. ; Adebamowo et al. ). Cronobacter (E. sakazakii) is a gram-negative, nonspore-forming bacterium, a foodborne pathogen that has been associated with serious illness and death among the elderly and immunocompromised adults (Iversen et al. ; Osaili et al. a). Among foods in which it is has been found are milk and other dairy products, including cheese milk powder and ultra-high temperature processed milk (Lai 1; Lee et al. ; Osaili et al. 7; ; Shaker et al. 7). Because of its potential virulent effects, the possibility of Cronobacter in foods that make up an important part of our daily diet raises important concerns regarding food safety and the need to control the presence of this and other harmful food pathogens. Ionizing radiation is one of the most effective technologies for controlling pathogens in food (Farkas 199; Molins et al. 1; Lacroix et al. ; Osaili et al. a,b; Mahmoud 9a,b; Mahmoud and Burrage 9). The Centers for Disease Control and Prevention, along with the World Health Organization and many other health organizations, encourage the use of irradiation as an 5 Journal compilation ª 9 The Society for Applied Microbiology, Letters in Applied Microbiology 9 (9) 5 57

2 B.S.M. Mahmoud Inactivation effect of X-ray treatments effective technology that could protect public against foodborne pathogens. Like pasteurization and canning, irradiation technology is a safe and effective food processing technology. Several reports have demonstrated that irradiation is effective in eliminating foodborne pathogens in several products including meat and poultry (Tauxe 1; Manas and Pagan 5). Applications of ionizing radiation up to a dose level of 1 kgy can be used to eliminate or greatly reduce spoilage and pathogenic organisms without causing any toxicological hazard to human consumption (WHO 191, 1999). Previous work has shown irradiation (gamma rays) to be an effective method of inactivating foodborne pathogens in milk and milk products (Bougle and Stahl 199; Cecchi et al. 199; Tsiotsias et al. ; Adeil Pietranera et al. 3). An advantage of this approach is that it provides a means of treating large volumes or amounts of product with virtually no effect on quality or interruption of production and shipment. Despite this, there remains a question regarding the effectiveness of this method for addressing contamination by specific pathogens that have shown to be resistant to many methods of pathogenic control. X-ray has advantages over other current approved ionizing irradiation used in the food industry, such as gamma rays, as the X-ray irradiator does not have a radioactive source (Janatpour et al. 5). The present study was conducted to evaluate the inactivation effect of X-ray on E. sakazakii in TSB, skim milk (% fat), low-fat milk (1% and %) and whole-fat milk (3Æ5%). Materials and methods Milk samples Fresh pasteurized milk samples with different fat contents [(skim (% fat), low-fat (1%), reduced-fat (%) and whole-fat milk (3Æ5%)] were purchased from a local grocery market in Pascagoula, MS and kept at C until use. Bacterial strains and culture conditions Six strains of Cronobacter (E. Sakazakii 71, 7, 75, 7, 79 and 713) were provided by Dr Salam Ibrahim, North Carolina A&T State University. These strains were kept at ) C in tryptic soy broth (TSB) with % glycerol. Strains were activated by transferring 5 ll of the stock into 5 ml of TSB and incubated at 37 C for 1 h. All working cultures were kept at C on tryptic soy agar slants. Each strain culture was grown separately in 1 ml TSB and incubated at 37 C for 1 h with continuous agitation (1 rev min )1 ) on a MaxQ platform shaker (Barnstead Lab-line, Melrose, IL, USA). The cultures were streaked onto individual plates of TSA and incubated at 37 C for 1 h. To prepare an inoculum, a single colony from each strain was transferred to separate 1-ml Erlenmeyer flasks containing 5 ml of sterile TSB and incubated at 37 C for h. Preparation of mixture strains Bacterial strains were combined at equal volumes (5 ml each) in a sterilized empty 5-ml Erlenmeyer flask. Strain mixture was then centrifuged at 11 g (BD 1 Dynac III Centrifuge; Aria Medical Equipment, San Antonio, TX, USA) for 15 min. The supernatant was discarded, and the cell pellet was washed twice in peptone water (PW) and finally resuspended in 1 ml of sterile TSB, skim milk, 1% fat milk, % fat milk and 3Æ5% fat milk to achieve a mixture strains with a final population of approximately CFU ml )1. Description of the RS radiator and generation of X-ray Specific irradiation doses (Æ1, Æ5, Æ75, 1Æ, Æ, 3Æ, Æ, 5Æ and Æ kgy) were generated using the RS industrial cabinet X-ray irradiator (Rad Source Technologies, Inc., Alpharetta, GA) according to Mahmoud (9a). Briefly, at higher currents (ma), more electrons leave the filament. The electrons gather energy, equal to the potential difference; the higher the potential difference, the more energy the electrons gather. When the electrons reach the gold target plated inside the inner tube, they interact with the gold atoms and emit photons called X-rays. The X-ray doses in the treatment chamber were determined using a dosimeter (Rad Source Technologies). Treatment of inoculated Cronobacter in TSB and milk samples with X-ray Four sets of glass tubes (1 15 mm), each containing 1 ml of either TSB, skim milk, 1% fat milk, % fat milk or 3Æ5% fat milk inoculated with the Cronobacter were prepared as described earlier. Two of the tubes from each media type were used to determine the initial numbers of viable cells (control). The other two tubes were placed in the cardboard irradiation canister inside the exposure chamber and subjected to one of the following X-ray doses: Æ1, Æ5, Æ75, 1Æ, Æ, 3Æ, Æ, 5Æ and Æ kgy. Also, negative controls (uninoculated and untreated; to determine background microflora and pathogen levels, if they were present) were prepared and tested for any growth on TSA, for TSB, skim milk, 1% fat milk, % fat milk and 3Æ5% fat milk, which were always negative to any growth on TSA). Journal compilation ª 9 The Society for Applied Microbiology, Letters in Applied Microbiology 9 (9)

3 Inactivation effect of X-ray treatments B.S.M. Mahmoud Microbial enumeration At each examined dose, two tubes of TSB, skim milk, 1% fat milk, % fat milk and 3Æ5% fat milk were removed from the exposure chamber. Serial 1-fold dilutions were prepared in PW. Appropriate dilution was then spread plated onto TSA plates and incubated at 37 C for h. Colonies were counted, and results expressed as log CFU ml )1. D 1 -value determination A first-order kinetic model (linear model) was used to analyse the data for log of surviving organisms per treatment dose (Mahmoud et al. 7). The D 1 -values (X-ray dose required for a 9% reduction) were determined using survival data for, Æ1, Æ5, Æ75, 1Æ, Æ, 3Æ, Æ, 5Æ and Æ kgy X-ray during treatment. D 1 -values analyses were performed using Microsoft Excel (Microsoft Windows XP). Statistical analysis All experiments were replicated three times using two samples per experiment for a total of six data points per treatment. Data were pooled, and the mean values and standard deviations were determined using a Student s t-test with Microsoft Excel (Microsoft Windows XP). Determination of significance was set at P < Æ5. Results Inactivation of Cronobacter in TSB Figure 1(a) shows the effect of X-ray doses on the inactivation of Cronobacter in TSB. The initial population was Æ9 ±Æ1 CFU ml )1. However, the population was reduced to 7Æ3 ±Æ CFU ml )1 with Æ1 kgy dose and continued to be reduced further with higher doses. The population Cronobacter in TSB was reduced to Æ ±Æ, 5Æ ±Æ3, 3Æ9 ±Æ, Æ ±Æ1 and 1Æ1 ±Æ log CFU ml )1 after treatment with Æ5, Æ75, 1Æ, Æ and 3Æ kgy doses of X-rays, respectively (Fig. 1a). All X-ray treatments had significant (P <Æ5) effect on the reduction in the population of Cronobacter. Exposure to Æ kgy X-ray reduced the population of Cronobacter in laboratory medium to below detection limits (<1Æ log ml )1 ). The D 1 -value of inoculated Cronobacter in TSB was Æ1 ± Æ1 kgy (Table 1). Inactivation of Cronobacter in skim milk Figure 1(b) shows the effect of X-ray doses on the inactivation of Cronobacter in skim milk samples. The population of Cronobacter was slightly decreased with Æ1 kgy X-ray treatment. Further bacterial population reduction was recorded with higher X-ray doses. Cronobacter population was significantly (P < Æ5) reduced from Æ ± Æ1 to 7Æ ±Æ1, 7Æ5 ±Æ1, Æ5 ±Æ1, 3Æ7 ±Æ and Æ9 ±Æ1 CFU ml )1 after treatment with Æ5, Æ75, 1Æ, Æ (c) 1 (a) 1 R = R = 977 (b) R = (d) R = (e) R = Figure 1 Microbial survival curves for inoculated Cronobacter species in tryptic soy broth (a), skim milk (b), 1% fat milk (c) % fat milk (d) and 3Æ5% fat milk (e) by X-ray. Error bars represent standard error. Each value represents the mean of three replications. 5 Journal compilation ª 9 The Society for Applied Microbiology, Letters in Applied Microbiology 9 (9) 5 57

4 B.S.M. Mahmoud Inactivation effect of X-ray treatments Table 1 D 1 -values (kgy) for inoculated Cronobacter (Enterobacter sakazakii) in tryptic soy broth (TSB), skim milk, low-fat milk (1% and %) and whole-fat milk (3Æ5%) D 1 -values (kgy) TSB Skim milk 1% fat milk % fat milk 3Æ5% fat milk Æ1 ± Æ1 a Æ5 ± Æ b Æ5 ± Æ c Æ71 ± Æ3 c Æ7 ± Æ3 c Mean values with different letters are significantly different (P < Æ5). and 3Æ kgy doses of X-rays, respectively (Fig. 1b). Exposure to Æ kgy X-ray reduced the population of Cronobacter to 1Æ9 ±Æ1 CFU ml )1. Treatment with 5Æ kgy was required to achieve reduction in Cronobacter population below detection limits (<1Æ log ml )1 ). This indicates that skim milk provide some protection against X-ray compared to laboratory medium (TSB). The D 1 -value of inoculated Cronobacter in skim milk was Æ5 ± Æ kgy (Table 1). Inactivation of Cronobacter in low- (1%) and reduced (%)-fat milk Figure 1(c,d) shows the effect of X-ray doses on the inactivation of Cronobacter in low-fat and reduced-fat milk samples. The population of Cronobacter reduced from the initial population of Æ9 ±Æ1 to 7Æ ±Æ5, 7Æ ±Æ1, Æ ±Æ1, 3Æ7 ±Æ3, Æ3 ±Æ3 and 1Æ9 ±Æ1 log CFU ml )1 after treatment with Æ75, 1Æ, Æ, 3Æ, Æ and 5Æ kgy doses of X-rays, respectively (Fig. 1c) in low-fat milk samples and to 7Æ ±Æ1, Æ ±Æ1, 3Æ ±Æ3, 3Æ ±Æ1 and Æ3 ±Æ log CFU ml )1 in reduced-fat (%) milk samples (Fig. 1d). Exposure to Æ kgy X-ray was required to reduce the population of Cronobacter below detection limits (<1Æ log ml )1 ). The D 1 -values of inoculated Cronobacter in 1% fat milk and % fat milk were Æ5 ± Æ and Æ71 ± Æ3 kgy, respectively (Table 1). Inactivation of Cronobacter in whole-fat milk (3Æ5%) Figure 1(e) shows the effect of X-ray on the reduction in Cronobacter population in whole-fat milk. Cronobacter tend to become more resistant to X-ray in whole-fat milk samples compared to other samples tested in this study. There was slight reduction in Cronobacter population with up to Æ75 kgy doses. A significantly bacterial cell reduction was observed with 1Æ kgy (P <Æ5). The population was reduced to 7Æ ±Æ1 log CFU ml )1. The population was further reduced to Æ ±Æ1, 3Æ ±Æ, 3Æ ±Æ and Æ ±Æ1 log CFU ml )1 when samples exposed to Æ, 3Æ, Æ and 5Æ kgy doses of X-rays, respectively (Fig. 1e). Exposure to Æ kgy X-ray reduced the population of Cronobacter in pure culture to below detection limits (<1Æ log ml )1 ). The D 1 -value of inoculated Cronobacter in whole-fat milk was Æ7 ± Æ3 kgy (Table 1). Discussion In the recent years, the social perception of irradiation is changing, and consumers are more aware of this technology. Therefore, the use of such nonthermal technology in several food applications needs to be determined to ensure safe and high-quality products. A major advantage of irradiation over other technologies is that milk products can be irradiated within their packaging and products remain protected until reach consumer. This practice would prevent cross-contamination, a major factor responsible for foodborne pathogens. X-ray irradiation is an alternative that has certain advantages over other current approved ionizing irradiation used in the food industry, such as gamma rays. The X-ray irradiator does not have a radioactive source (Janatpour et al. 5). X-ray irradiation is an effective treatment and has successfully been used to sterilize several food products including oysters and shrimps (Mahmoud 9a,b; Mahmoud and Burrage 9). The use of X-ray to improve the microbiological safety of milk and milk products is relatively new technology that has not been investigated. As expected increasing X-ray doses increased the inactivation effect on Cronobacter in pure culture and milk samples. These findings are in the same trend as those reported by Mahmoud 9a,b and Mahmoud and Burrage 9;. Cronobacter showed a significant resistance to X-ray treatment than other pathogenic bacteria. A greater than Æ-log reduction in V. parahaemolyticus and V. vulnificus population was observed with Æ75 kgy X-ray in TSB (Mahmoud 9a,b; Mahmoud and Burrage 9). Cronobacter was more resistant to X-ray treatments in the milk samples than in the pure culture (fat, proteins, lactose and minerals may have influence on bacterial reduction). These findings are in agreement with those obtained by Osaili et al. (7) who found that the D-values for Cronobacter treated with gamma rays ranged from Æ1 to Æ9 kgy, Æ to Æ37 kgy and 1Æ to 1Æ71 kgy in brain heart infusion broth, rehydrated infant milk formula and dehydrated infant milk formula, respectively. This study examined the effect of milk composition (% fat) on the inactivation effect of X-ray against Cronobacter. The X-ray dose needed to reduce the population of Cronobacter in skim milk was significantly lower than those needed to reduce the population of Cronobacter in 1%, % and 3Æ5% fat milk. The X-ray dose needed to reduce the population of Cronobacter in 1% fat milk samples was similar to those needed for % and 3Æ5% fat Journal compilation ª 9 The Society for Applied Microbiology, Letters in Applied Microbiology 9 (9)

5 Inactivation effect of X-ray treatments B.S.M. Mahmoud milk. Earlier studies have also shown that milk protein protect bacterial cells against several stresses including heat, cold and starvation stresses. Wiebe et al. (1993) reported that the growth response at low temperatures depended on the availability of nutrients. Addition of milk protein could provide nutrients and energy sources that promote the survival and growth of E. coli O157:H7 in milk samples. Rubin (195) reported that in high caesein dairy products such as cheese, survival of pathogens might be due to the protective action of casein micelles. Kinetic models are used for the development of food preservation processes and to understand the mechanism of microbial survival and inactivation. D 1 -value information helps processors develop appropriate treatment doses to reduce pathogen levels and reduce risk from consumption of dairy products. In this study, we determined the death rate of Cronobacter as influenced by X-ray using D 1 -value. In the TSB, low X-ray doses was needed to cause high reduction in the bacterial population (R =Æ91). In the milk samples, higher X-ray doses was required to achieve higher population reduction (R =Æ95 Æ9). D 1 -value for Cronobacter in TSB was Æ1, where as in skim milk the D 1 -value was Æ5. These values increased to Æ5, Æ71 and Æ7 in 1%, % and full-fat milk sample respectively. These results are in the same trend as those found by Osaili et al. (a) who studied the effect of gamma radiation on stressed Enterobacter sakazakii in powdered infant milk formula (PIMF). The authors found that the D 1 -values for the stressed E. sakazakii strains were ranged from Æ to 1Æ95 kgy. Also, Osaili et al. (b) studied the effect of extended dry storage of PIMF on susceptibility of Enterobacter sakazakii to ionizing radiation. They found that the D-value for E. sakazakii in PIMF was Æ9 kgy. More than kgy was required to kill 1Æ5 log g )1 of the same strain that had survived 1 months in dry PIMF. Lee et al. () studied the effect of gamma irradiation on Enterobacter sakazakii in TSB and dehydrated powdered infant formula. The D 1 -values for Enterobacter sakazakii in TSB and dehydrated powdered infant formula were Æ7 and Æ7 kgy, respectively. The quality of treated products by ionizing radiation is very important for both consumers and industry. The main purpose of this study was to evaluate the effect of X-ray in the survivability of Cronobacter in different fat milk. So, the author did not determine the effect of X-ray treatment on the quality of treated milk. There are a few reports regarding the effect of ionizing radiation on the quality of treated dairy products. Bierman et al. (195) reported that treatment with high voltage cathode rays (ranged from 7 to 5 rep) induced off-flavour in cream and various types of whole-fat and skim milk, depending on the product. In conclusion, this is the first report that describes inactivation of inoculated Cronobacter in skim milk, low-fat (1% and %) and whole-fat milk (3Æ5%) by X-ray. Treatment with 5Æ, Æ and Æ kgy X-ray doses significantly (P < Æ5) reduced the population of Cronobacter in skim, low-fat and whole-fat milk samples to less than the detectable limit (<1Æ log CFU ml )1 ), respectively. The D-value for Cronobacter in skim milk (Æ5 ± Æ b ) was significantly (P <Æ5) lower than those in 1% (Æ5 ± Æ c ), % (Æ71 ± Æ3 c ) and 3Æ5% (Æ7 ± Æ3 c ) milk samples. These results revealed that treatment with X-ray could be a good alternative to current techniques for disinfections of milk and dairy products for the dairy industry. Additional research is needed to determine the effect of X-ray treatment on the quality and shelf-life of treated milk. References Adebamowo, C.A., Spiegelman, D., Berkey, C.S., Danby, F.W., Rockett, H.H., Colditz, G.A., Wrillett, W.C. and Holmes, M.D. () Milk consumption and acne in teenage boys. J Am Acad Dermatol 5, Adeil Pietranera, M.S., Narvaiz, P., Horak, C. and Kairiyama, K. (3) Irradiated ice creams for immunosuppressed patients. Radiat Phys Chem, Bierman, G.W., Proctor, B.E. and Goldblith, S.A. (195) Radiation preservation of milk and milk Products. II. Off-flavors in milk and cream induced by ionizing radiations as judged by Organoleptic tests. J Dairy Sci 39, 379. Bougle, D.L. and Stahl, V. (199) Survival of Listeria monocytogenes after irradiation treatment of camembert cheeses made from raw milk. J Food Prot 57, Cecchi, L., Brasca, M., Lodi, R., Batteli, G., Nicosia, P. and Soldini, G. (199) Irradiation of dairy products: I. Sensitivity of different microorganisms. Latte, 9. Farkas, J. (199) Irradiation as a method for decontaminating food A review. Int J Food Microbiol, 19. Iversen, C., Mullane, M., McCardell, B., Tall, B.D., Lehner, A., Fanning, S., Stephan, R. and Joosten, H. () Cronobacter gen. nov., a new genus to accommodate the biogroups of Enterobacter sakazakii, and proposal of Cronobacter sakazakii gen. nov., comb. nov., C. malonaticus sp. nov., C. turicensis, sp. nov., C. muytjensii sp. nov., C. dublinensis sp. nov., Cronobacter genomospecies 1, and of three subspecies. C. dublinensis sp. nov. subsp. dublinensis subsp. nov. C. dublinensis sp. nov. subsp. lausannensis subsp. nov., and C. dublinensis sp. nov. subsp. lactaridi subsp. nov. Int J Syst Evol Microbiol 5, Janatpour, K., Denning, L., Nelson, K., Betlash, B., Mackenzie, M. and Holland, P. (5) Comparison of X-ray vs. gamma irradiation of CPDA-1 red cells. Vox Sang 9, Lacroix, M., Ouattara, B., Saucier, L., Giroux, M. and Smoragiewicz, W. () Effect of gamma irradiation in 5 Journal compilation ª 9 The Society for Applied Microbiology, Letters in Applied Microbiology 9 (9) 5 57

6 B.S.M. Mahmoud Inactivation effect of X-ray treatments presence of ascorbic acid on microbial composition and TBARS concentration of ground beef coated with an edible active coating. Radiat Phys Chem 71, Lai, K.K. (1) Enterobacter sakazakii infections among neonates, infants, children, and adults. Medicine, Lee, J.W., Oh, S.H., Kim, J.H., Yook, H.S. and Byun, M.W. () Gamma radiation sensitivity of Enterobacter sakazakii in dehydrated powdered infant formula. J Food Prot 9, Mahmoud, B.S.M. (9a) Reduction of Vibrio vulnificus in pure culture, half shell and whole shell oysters (Crassostrea virginica) by X-ray. Int J Food Microbiol 13, Mahmoud, B.S.M. (9b) Effect of X-ray treatments on inoculated E. coli O157: H7, Salmonella enterica, Shigella flexneri and Vibrio parahaemolyticus in ready-to-eat shrimp. Food Microbiol (In press) doi: 1.11/ j.fm Mahmoud, B.S.M. and Burrage, D. (9) Inactivation of Vibrio parahaemolyticus in pure culture, whole live and half shell oysters (Crassostrea virginica) by X-ray. Lett Appl Microbiol, Mahmoud, B.S.M., Bhagat, A.R. and Linton, R.H. (7) Inactivation kinetics of inoculated Escherichia coli O157:H7, Listeria monocytogenes and Salmonella enterica on strawberries by chlorine dioxide gas. Food Microbiol, Manas, P. and Pagan, R. (5) Microbial inactivation by new technologies of food preservation. J Appl Microbiol 9, Molins, R.A., Motarjemi, Y. and Käferstein, F.K. (1) Irradiation: a critical control point in ensuring the microbiological safety of raw foods. Food Control 1, Osaili, T.M., Shaker, R.R., Abu Al-Hasan, A.S., Ayyash, M.M. and Martin, E.M. (7) Inactivation of Enterobacter sakazakii in infant milk formula by gamma irradiation: determination of D 1 -Value. J Food Sci 7, 5. Osaili, T., Al-Nabulsi, A., Shaker, R., Ayyash, M., Olaimat, A., Abu Al-Hasan, A., Kadora, K. and Holley, R. (a) Effect of environmental stresses on the sensitivity of Enterobacter sakazakii in powdered infant milk formula to gamma radiation. Lett Appl Microbiol 7, 79. Osaili, T., Al-Nabulsi, A., Shaker, R., Ayyash, M., Olaimat, A., Abu Al-Hasan, A., Kadora, K. and Holley, R. (b) Effects of extended dry storage of powdered infant milk formula on susceptibility of Enterobacter sakazakii to hot water and ionizing radiation. J Food Prot 71, Osaili, T., Shaker, R., Ayyash, M.M., Al-Nabulsi, A. and Forsythe, S.J. (c) Survival and growth of Cronobacter species (Enterobacter sakazakii) in wheat-based infant follow-on formulas. Lett Appl Microbiol, 1. Popkin, B.M., Armstrong, L.E., Bray, G.M., Caballero, B., Frei, B. and Willett, W.C. () A new proposed guidance system for beverage consumption in the United States. Am J Clin Nutr 3, Rubin, H.E. (195) Protective effect of casein toward Salmonella Typhimurium in acid-milk. J Appl Bacteriol 5, Shaker, R., Osaili, T., Al-Omary, W., Jaradat, Z. and Al-Zuby, M. (7) Isolation of Enterobacter sakazakii and other Enterobacter sp. from food and food production environments. Food Control 1, Stabel, J.R., Waldren, C.A. and Garry, F. (1) Gamma-radiation effectively destroys Mycobacterium paratuberculosis in milk. J Dairy Sci, 7. Tauxe, R.V. (1) Food safety and irradiation: protecting the public from foodborne infections. The Centers for Disease Control and Prevention. Emerg Infect Dis 7, Tsiotsias, A., Savvaidis, I., Vassila, A., Kontominas, M. and Kotzekidou, P. () Control of Listeria monocytogenes by low-dose irradiation in combination with refrigeration in the soft whey cheese anthotyros. Food Microbiol 19, Wiebe, J.W., Sheldon, M. and Pomeroy, L.R. (1993) Evidence for an enhanced substrate requirement by marine mesophilic bacterial isolates at minimal growth temperatures. Microb Ecol 5, Wiley, A.S. (5) Does milk make children grow? Relationships between milk consumption and height in NHANES 1999 Am J Hum Biol 17, 5 1. World Health Organization (191) Wholesomeness of Irradiated Food. WHO Technical Reports Series 59. Geneva: World Health Organization. World Health Organization (1999) High-dose Irradiation: Wholesomeness of Food Irradiated With Doses Above 1 kgy. WHO Technical Reports Series 9. Geneva: World Health Organization. Journal compilation ª 9 The Society for Applied Microbiology, Letters in Applied Microbiology 9 (9)

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