Figure 26–1 Salmonellosis cases (per 100,000 population) United States, 1970–2000 Centers for Disease Control and Prevention, 2002 622 Modern Food Microbiology Foodborne Gastroenteritis Caused by Salmonella and Shigella 623 Food Products Salmonellae have been found in commercially prepared and packaged foods with 17 of 247 products examined being positive.1 Among the contaminated foods were cake mixes, cookie doughs, dinner rolls, and cornbread mixes These organisms have been found in coconut meal, salad dressing, mayonnaise, milk, and many other foods In a study of health foods, none of plant origin yielded salmonellae, but from two of three lots of beef liver powder from the same manufacturer were isolated S Minnesota, S Anatum, and S Derby.54 See Chapters 4–7 and Growth and Destruction of Salmonellae These organisms are typical of other Gram-negative bacteria in that they are able to grow on a large number of culture media and produce visible colonies well within 24 hours at about 37◦ C They are generally unable to ferment lactose, sucrose, or salicin, although glucose and certain other monosaccharides are fermented, with the production of gas Although they normally utilize amino acids as N sources, in the case of S Typhimurium, nitrate, nitrite, and NH3 will serve as sole sources of nitrogen.43 Although lactose fermentation is not usual for these organisms, some serovars can utilize this sugar The pH for optimum growth is around neutrality, with values above 9.0 and below 4.0 being bactericidal A minimum growth pH of 4.05 has been recorded for some (with HCl and citric acids), but depending on the acid used to lower the pH, the minimum may be as high as 5.5.15 The effect of acid used to lower the pH on minimum growth is presented in Table 26–2 Aeration was found to favor growth at the lower pH values The parameters of pH, water activity (aw ), nutrient content, and temperature are all interrelated for salmonellae, as they are for most other bacteria.56 For best growth, the salmonellae require a pH between 6.6 and 8.2 The lowest temperatures at which growth has been reported are 5.3◦ C for S Heidelberg and 6.2◦ C for S Typhimurium.38 Temperatures of around 45◦ C have been reported by several investigators to be the upper limit for growth Regarding available moisture, growth inhibition has been reported for aw values below 0.94 in media with neutral pH, with higher aw values being required as the pH is decreased toward growth minima Unlike the staphylococci, the salmonellae are unable to tolerate high salt concentrations Brine above 9% is reported to be bactericidal Nitrite is effective, with the effect being greatest at the lower pH values This suggests that the inhibitory effect of this compound is referable to the undissociated HNO2 molecule The survival of Salmonella spp in mayonnaise was studied by Lerche,34 who found that they were destroyed in this product if the pH was below 4.0 It was found that several days may be required for destruction if the level of contamination is high, but within 24 hours for low numbers of cells S Thompson and S Typhimurium were found to be more resistant to acid destruction than S Senftenberg With respect to heat destruction, all salmonellae are readily destroyed at milk pasteurization temperatures Thermal D values for the destruction of S Senftenberg 775W under various conditions are given in Chapter 17 Shrimpton et al.50 reported that S Senftenberg 775W required 2.5 minutes for a 104 –105 reduction in numbers at 54.4◦ C in liquid whole egg This strain is the most heat resistant of all salmonellae serovars This treatment of liquid whole egg has been shown to produce a Salmonella-free product and destroy egg α-amylase (see Chapter 17 for the heat pasteurization of egg white) It has been suggested7 that the α-amylase test may be used as a means of determining the adequacy of heat pasteurization of liquid egg (compare with the pasteurization of milk and the enzyme phosphatase) In a study on the heat resistance of S Senftenberg 775W, Ng et al.42 found this strain to be more heat 624 Modern Food Microbiology sensitive in the log phase than in the stationary phase of growth These investigators also found that cells grown at 44◦ C were more heat resistant than those grown at either 15◦ C or 35◦ C With respect to the destruction of Salmonella in baked foods, Beloian and Schlosser5 found that baked foods reaching a temperature of 160◦ F or higher in the slowest heating region can be considered Salmonella free These authors employed S Senftenberg 775W at a concentration of 7,000–10,000 cells/ml placed in reconstituted dried egg With respect to the heat destruction of this strain in poultry, it is recommended that internal temperatures of at least 160◦ F be attained.40 Although S Senftenberg 775W has been reported to be 30 times more heat resistant than S Typhimurium,42 the latter organism has been found to be more resistant to dry heat than the former.21 These investigators tested dry heat resistance in milk chocolate The destruction of S Pullorum in turkeys was investigated by Rogers and Gunderson,47 who found that it required hours and 55 minutes to destroy an initial inoculum of 115 million in 10- to 11lb turkeys with an internal temperature of 160◦ F, and for 18-lb turkeys with an initial inoculum of 320 million organisms, hours and 20 minutes were required for destruction The salmonellae are quite sensitive to ionizing radiation, with doses of 5–7.5 kGy being sufficient to eliminate them from most foods and feed The decimal reduction dose has been reported to range from 0.4 to 0.7 kGy for Salmonella spp in frozen eggs The effect of various foods on the radiosensitivity of salmonellae is shown in a study by Ley et al.35 These investigators found that for frozen whole egg, kGy gave a 107 reduction in the numbers of S Typhimurium, whereas 6.5 kGy was required to give a 105 reduction in frozen horsemeat, between and 7.5 kGy for a 105 –108 reduction in bone meal, and only 4.5 kGy to give a 103 reduction of S Typhimurium in desiccated coconut More extensive information on the effect of irradiation on salmonellae is presented in Chapter 15 Table 26–2 Minimum pH at Which Salmonellae Would Initiate Growth under Optimum Laboratory Conditions Acid Hydrochloric Citric Tartaric Gluconic Fumaric Malic Lactic Succinic Glutaric Adipic Pimelic Acetic Propionic pH 4.05 4.05 4.10 4.20 4.30 4.30 4.40 4.60 4.70 5.10 5.10 5.40 5.50 Note: Tryptone–yeast extract–glucose broth was inoculated with 104 cells per milliliter of Salmonella Anatum, S Tennessee, or S Senftenberg Source: From Chung and Goepfert,15 copyright c 1970 by Institute of Food Technologists Foodborne Gastroenteritis Caused by Salmonella and Shigella 625 In dry foods, S Montevideo was found to be more resistant than S Heidelberg when inoculated into dry milk, cocoa powder, poultry feed, meat, and bone meal.29 Survival was greater at aw 0.43 and 0.52 than at aw 0.75 The Salmonella Food-Poisoning Syndrome This syndrome is caused by the ingestion of foods that contain significant numbers of non-hostspecific species or serotypes of the genus Salmonella From the time of ingestion of food, symptoms usually develop in 12–14 hours, although shorter and longer times have been reported The symptoms consist of nausea, vomiting, abdominal pain (not as severe as with staphylococcal food poisoning), headache, chills, and diarrhea These symptoms are usually accompanied by prostration, muscular weakness, faintness, moderate fever, restlessness, and drowsiness Symptoms usually persist for 2–3 days The average mortality rate is 4.1%, varying from 5.8% during the first year of life, to 2% between the first and 50th year, and 15% in persons over 50 years Among the different species of Salmonella,S Choleraesuis has been reported to produce the highest mortality rate—21% (see Chapter 22) Although these organisms generally disappear rapidly from the intestinal tract, up to 5% of patients may become carriers of the organisms upon recovery from this disease Numbers of cells on the order of 107 –109 /g are generally necessary for salmonellosis That outbreaks may occur in which relatively low numbers of cells are found has been noted.18 From three outbreaks, the numbers of cells found were as low as 100/100 g (S Eastbourne in chocolate) to 15,000/g (S Cubana in a carmine dye solution) In general, minimum numbers for gastroenteritis range between 105 and 106 /g for S Bareilly and S Newport to 109 –1010 for S Pullorum.8 Salmonella Virulence Properties Although an enterotoxin and a cytotoxin have been identified in pathogenic salmonellae, they seem to play only a minimal (if any) role in the gastroenteritis syndrome The virulence mechanisms of the salmonellae continue to be unravelled, and summaries of what is known are presented in Chapter 22 along with other Gram-negative foodborne pathogens A synopsis of the early history of salmonellae pathogenesis can be found in the previous edition of this text Incidence and Vehicle Foods The precise incidence of salmonellae food poisoning in the United States is not known However, the two largest recorded outbreaks of salmonellosis occurred under rather unusual circumstances The largest occurred in 1994 and it involved more than 224,000 persons.23 The vehicle food was ice cream produced from milk that was transported in tanker trucks that had previously hauled liquid eggs The serovar was S Enteritidis, and cases were seen in at least 41 U.S states The next largest outbreak occurred in 1985 and involved close to 200,000 persons.48 (See Fig 26–1 and Fig 26–2.) The vehicle was 2% milk produced by a single dairy plant in Illinois, and S Typhimurium was the etiological agent (see Figures 26–1 and 26–2) The third largest outbreak occurred in 1974 on the Navajo Indian Reservation, when 3,400 persons became ill.26 The vehicle food was potato salad served to about 11,000 individuals at a barbecue It was prepared and stored for up to 16 hours at improper holding temperatures prior to serving; the serovar isolated was S Newport It may be noted from Figure 26–2 that S Typhimurium has been the single most Figure 26–2 Reported isolates of Salmonella by serotype and year, United States, 1975–2000 (Data from Public Health Laboratory Information System, PHLIS, Centers for Disease Control and Prevention, 2002) 626 Modern Food Microbiology ...Foodborne Gastroenteritis Caused by Salmonella and Shigella 623 Food Products Salmonellae have been found in commercially prepared and packaged foods with 17 of 247 products examined being... in baked foods, Beloian and Schlosser5 found that baked foods reaching a temperature of 160◦ F or higher in the slowest heating region can be considered Salmonella free These authors employed S... largest occurred in 1994 and it involved more than 224,000 persons.23 The vehicle food was ice cream produced from milk that was transported in tanker trucks that had previously hauled liquid eggs