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Growth of <I>Aeromonas Hydrophila</I> in the Whey Cheeses Myzithra, Anthotyros, and Manouri During Storage at 4

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Growth of <I>Aeromonas Hydrophila</I> in the Whey Cheeses Myzithra, Anthotyros, and Manouri During Storage at 4 308 Journal of Food Protection, Vol. 69, No. 2, 2006, Pages 308±314 Copyright Q, International Association for Food Protection Growth of Aeromonas hydrophila in the Whey Cheeses Myzithra, Anthotyros, and Manouri during Storage at 4 and 128C DEMETRIOS K. PAPAGEORGIOU,* DIMITRIOS S. MELAS, AMIN ABRAHIM, AND APOSTOLOS S. ANGELIDIS Laboratory of Milk Hygiene and Technology, Department of Food Hygiene and Technology, School of Veterinary Medicine, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece MS 05-340: Received 15 July 2005/Accepted 19 September 2005 ABSTRACT Downloaded from http://meridian.allenpress.com/jfp/article-pdf/69/2/308/1677981/0362-028x-69_2_308.pdf by guest on 02 October 2021 The fresh whey cheeses Myzithra, Anthotyros, and Manouri were inoculated with Aeromonas hydrophila strain NTCC 8049 (type strain) or with an A. hydrophila strain isolated from food (food isolate) at levels of 3.0 to 5.0 3 102 CFU/g of cheese and stored at 4 or 128C. Duplicate samples of cheeses were tested for levels of A. hydrophila and pH after up to 29 days of storage. At 48C, A. hydrophila grew in Myzithra and Anthotyros with a generation time of ca. 19 h, but no growth was observed in Manouri. In Myzithra, average maximum populations of 8.87 log CFU/g (type strain) and 8.79 log CFU/g (food isolate) were recorded after 20 and 22 days of storage at 48C, respectively. The average maximum populations observed in Anthotyros stored at 48C were 6.72 log CFU/g (food isolate) and 6.13 log CFU/g (type strain) and were observed after 15 and 16 days of storage, respectively. A. hydrophila grew rapidly and reached high numbers in cheeses stored at 128C. The average generation times were 3.7 and 3.9 h (Myzithra), 4.1 and 6.1 h (Anthotyros), and 8.0 and 9.2 h (Manouri) for the type strain and the food isolate, respectively. Among the different whey cheese trials, the highest A. hydrophila population recorded (10.13 log CFU/g) was in Myzithra that had been inoculated with the food isolate after 8 days of storage at 128C. To prevent A. hydrophila growth in whey cheeses, efforts must be focused on preventing postprocessing contamination and temperature abuse during transportation and storage. Aeromonas spp. are gram-negative facultative anaero- in raw milk in Greece as well as in the Greek whey cheeses bic rod-shaped bacteria widely distributed in nature (20, 31, Anthotyros and Manouri (30). A high frequency of A. hy- 38). Aeromonas spp. are widespread in foods and the en- drophila isolation has also been reported from the Italian vironment and were recognized as pathogens of aquatic and whey cheese Ricotta (45). Upon postprocessing contami- amphibian animals long before they were considered path- nation, these cheeses are susceptible to bacterial prolifera- ogenic for humans (3, 6, 19). Aeromonas spp. are com- tion because of their high moisture content (up to 70%) and monly isolated from water, fresh vegetables, and foods of their high pH (6.1 to 6.5). Therefore, the objective of this animal origin such as seafood, meat, raw milk, and cheese study was to determine the potential of growth for A. hy- (8, 11±13, 23, 25, 28, 30, 33, 39, 44, 45). Refrigeration of drophila in the whey cheeses Myzithra, Anthotyros, and these foods is not adequate for control of Aeromonas, as Manouri stored at 4 and 128C. some of the strains isolated from foods can grow at refrig- eration temperatures and produce enterotoxins, cytotoxins, MATERIALS AND METHODS or hemolysins (5, 7, 18, 21, 22, 26, 41). Bacterial strains and preparation of inocula. Two A. hy- The taxonomy of Aeromonas spp. is an area of ongoing drophila strains were used in this study. One was the strain A. research (1, 15, 43) and, to date, there are 14 recognized hydrophila NTCC 8049, provided by the Irish National Food Cen- species within the genus Aeromonas (16). Only ®ve species ter (Qunsined, Dublin, Ireland), and the other was an A. hydro- are thought to be of clinical importance to humans, and of phila strain isolated from raw ewe's milk (food isolate) in our these, two species and one biotype of another species laboratory (30). Freeze-dried A. hydrophila cultures were regen- (Aeromonas hydrophila, Aeromonas caviae, and Aeromon- erated in brain heart infusion broth, which was incubated aero- bically at 288C for 18 h. Intermediate cultures were then prepared as veronii biovar sobria) account for more than 85% of all by transferring the regenerated cultures to brain heart infusion clinical isolates (14, 15, 42). Gastroenteritis due to Aero- broth (288C for 18 h), and working cultures were prepared by monas spp. is primarily a problem in young children, the transferring 0.3 ml of the intermediate culture into 200 ml of ster- elderly, and the immunocompromised (2, 10, 14, 19). ile skim milk in screw-top Erlenmeyer ¯asks, which were incu- A. hydrophila has been incriminated for 16.3% of 881 bated aerobically at 288C for 18 h. For each trial, the appropriate cases of diarrhea in children in Greece between 1991 and volume of a working culture was added to the cheese to generate 1993 (24). Previous work in our laboratory has documented an initial inoculum of ca. 3.0 to 5.0 3 102 CFU/g. the presence of A. hydrophila and other motile aeromonads Inoculation and storage of Myzithra, Anthotyros, and Manouri. All three types of whey cheese used in the experiments * Author for correspondence. Tel: 130 2310 999806; Fax: 130 2310 (Myzithra, Anthotyros, and Manouri) were manufactured in a 999803; E-mail: [email protected]. commercial dairy facility in central Macedonia, Greece, by a pro- J. Food Prot., Vol. 69, No. 2 GROWTH OF A. HYDROPHILA IN WHEY CHEESES 309 cedure described elsewhere (36). For each of the three whey RESULTS AND DISCUSSION cheeses, eight experimental trials were performed (8 3 3 5 24 trials total). Four trials (two for each strain) were prepared and Composition of whey cheeses. The Greek regulatory stored at 48C, and an additional four trials were prepared and standards for whey cheeses specify that the moisture con- stored at 128C for up to 29 days. For each trial, ca. 3 kg of whey tent of Myzithra (standard version) and Anthotyros must cheese was inoculated. The inoculation was performed in a grad- not exceed 70% and that the fat in dry matter (FDM) of ual and sequential manner to ensure optimum distribution of A. these products must not be less than 50 and 65%, respec- hydrophila cells in the cheese: 0.5 kg of whey cheese was inoc- tively. Manouri must not contain more than 60% moisture ulated with a calculated volume of A. hydrophila culture and or less than 70% FDM. The addition of salt is allowed in mixed thoroughly for 3 min in a sterile 14-liter open-mouth round- these cheeses, and commercially produced whey cheeses in glass container. The metal stirring rods of the mixer had been also Greece usually contain 1 to 2% salt, but no standards are sterilized. A second 0.5-kg portion of whey cheese was next added in place to regulate its concentration. Myzithra can be found to the glass container and mixed thoroughly for 4 min; then, two in the market as a dry, salted cheese. However, it is also more 1-kg portions were added. After each 1-kg addition of manufactured as a low-fat, fresh cheese, without the addi- Downloaded from http://meridian.allenpress.com/jfp/article-pdf/69/2/308/1677981/0362-028x-69_2_308.pdf by guest on 02 October 2021 cheese, the mixture was thoroughly mixed for 5 min. The inoc- ulated cheese was distributed (in ca. 50-g portions) into each of tion of salt (17). Low-fat, salt-free, fresh Myzithra (as in 60 sterilized 90-g plastic urine-collection containers (Latex Inc., the experiments) is preferred by consumers because of con- Arnea, Greece). The containers' well-®tted plastic caps prevented temporary nutritional practices. The moisture content, moisture loss. Each ®lled container was sealed and kept refriger- FDM, SWP, and pH of the whey cheeses used in the ex- ated until the last container had been prepared (for each trial, the periments are presented in Table 1. The chemical compo- entire packaging process was completed within 30 min), and then sition of Manouri and Anthotyros cheeses used in this study the sealed containers were stored at 4 or 128C. were in accordance with the Greek standards with respect to moisture and FDM. We purposely chose the low-fat, un- Sampling schedule and enumeration of A. hydrophila. Pri- salted version of Myzithra for our experiments to evaluate or to the inoculation of cheeses, duplicate 10-g cheese samples the response of A. hydrophila in a whey cheese that is sub- from all 24 trials were checked for the presence of A. hydrophila stantially different from the other two Greek whey cheeses by means of direct plating and cold enrichment (78C for 72 h) as previously described (30, 34). The lower detection limit of direct in terms of its chemical composition. plating was 10 CFU/g (0.2 ml from the 102l dilution spread onto The average initial pH values of Myzithra, Anthotyros, each of ®ve plates), and that of cold enrichment was less than 1 and Manouri at the beginning of the experiments (time 0) CFU/10 g. From each container, duplicate samples were used for were 6.31, 6.56, and 6.10, respectively (Table 1). In the the enumeration of A. hydrophila and the determination of pH Myzithra trials, the pH of cheese remained relatively con- immediately postinoculation and thereafter at 24-h intervals (48C stant throughout the experiments, with an overall minor de- trials) or at 12- to 24-h intervals (128C trials).
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