MAJOR ARTICLE Tonsillopharyngitis Caused by Foodborne Group A Streptococcus: A Prison-Based Outbreak Michael Levy,1 Christine G. Johnson,2 and Ed Kraa3 1 Population Health, Corrections Health Service, Matraville, 2Discipline of Microbiology, Hunter Area Pathology Service, Newcastle, and Food Inspection and Surveillance, Food Branch, New South Wales Health Department, North Sydney, Australia 3 An outbreak of tonsillopharyngitis due to Streptococcus pyogenes occurred among inmates of a rural correctional center in New South Wales, Australia. A total of 72 (28%) of 256 inmates became ill in December 1999. S. pyogenes type M-75, T-25, which was opacity factor positive, was isolated from throat swab specimens obtained from 5 of 57 inmates with primary cases and from 4 of 15 inmates with secondary cases, as well as from specimens obtained from the hand wounds and throat of one of the food handlers. The consumption of curried egg rolls (i.e., curried egg salad sandwiches) was the most likely association with this outbreak. The presumed source of the food contamination was the food handler who had infected hand wounds. There has been only one other outbreak of streptococcal pharyngitis reported from a prison. Other outbreaks have been reported from military bases, nursing homes, and community picnics. Foodborne outbreaks of group A streptococcal disease are relatively rarely reported. We report a moderatesized outbreak in an institutional setting and present a review of the reports of previous outbreaks. The correctional center at which the outbreak occurred is a rural minimum-security prison in New South Wales, Australia, located 300 km northwest of Sydney, Australia. Meals for the inmates came from 2 sources. Bread rolls (i.e., sandwiches) for lunch were prepared on site, whereas “cook-chill” evening meals were prepared in a central kitchen in a correctional center in Sydney. There were 256 male inmates in the prison on 17 December 1999, the date when a small number of inmates presented with tonsillopharyngitis. These patients were treated symptomatically for a presumed viral illness. By the next day, there were 11 cases of tonsillopharyngitis, and inmates with new cases continued Received 21 June 2002; accepted 8 October 2002; electronically published 7 January 2003. Reprints or correspondence: Dr. Christine G. Johnson, Discipline of Microbiology, Hunter Area Pathology Service, Locked Bag 1, Hunter Region Mail Centre, 2310, Australia ([email protected]). Clinical Infectious Diseases 2003; 36:175–82 2003 by the Infectious Diseases Society of America. All rights reserved. 1058-4838/2003/3602-0006$15.00 to present until 21 December, with a peak of 26 cases diagnosed on 18 December. On 19 December, the presumptive diagnosis was changed to bacterial tonsillopharyngitis. Throat swab specimens were obtained from 6 of the new patients, and a policy of providing empirical treatment with penicillin for all additional cases was introduced. Antibiotics were also offered to inmates who had previously sought care. Five of the throat swab specimens were subsequently found to be positive for group A b-hemolytic streptococcus. On 22 December, no additional cases were diagnosed, but 15 additional inmates had bacterial tonsillopharyngitis diagnosed from 23 through 26 December. PATIENTS AND METHODS Definitions and case ascertainment. A “case patient” was defined as an inmate of the correctional center who had culture-proven group A streptococcal throat infection or clinically purulent tonsillopharyngitis diagnosed between 18 and 26 December. Case patients who received their diagnosis on or before 21 December (i.e., patients who presented within 72 h of the time of presentation of the first case patient) were regarded as having primary cases. Those who presented on or after December 23 were regarded as having secondary cases. Foodborne Group A Streptococcus • CID 2003:36 (15 January) • 175 from workers in the central kitchen at the correctional center in Sydney were cultured at the Centre for Infectious Diseases and Microbiology, Institute of Clinical Pathology and Medical Research (Westmead, Australia). Analysis of survey results. Data were entered into Epi Info software, version 6.04b (US Centers for Disease Control and Prevention; Atlanta, GA). Analysis was done using the same program. Literature search. A literature search of MEDLINE was performed using various combinations of the search terms “group,” “streptococcus,” “streptococcal,” “outbreak,” and “foodborne.” The references found by this search were used to locate additional reports. Figure 1. Epidemic curve of cases of tonsillopharyngitis due to foodborne group A streptococcus in an outbreak among 256 inmates of a rural correctional center in New South Wales, Australia. The number of cases diagnosed was determined from clinic records, and the epidemic curve was constructed using the date of diagnosis as the time referent. Investigation of meal arrangements at the correctional center. Information about the usual routine for meals at the prison was obtained by interviewing the inmates who worked in the kitchen as well as the custodial staff who supervised them. Information from the menus for 15–17 December were used to prepare a questionnaire, which, on 22 December, was administered to 154 inmates; the inmates completed the questionnaire either during a face-to-face interview or on their own. Kitchen inspections. The on-site kitchen was inspected on 21 December, and the kitchen staff was interviewed. Throat swab specimens were obtained from the 5 inmates who worked in the kitchens. Skin lesions present on the hands of one member of the kitchen staff were also swabbed to obtain specimens for bacterial culture. The kitchen at the correctional center in Sydney that supplied the cook-chill meals was inspected on 22 December. Throat swab specimens were also obtained from some of the kitchen staff in Sydney. Laboratory investigations. The Division of Microbiology, Hunter Area Pathology Service (Newcastle, Australia), cultured the swab specimens obtained from inmates of the rural correctional center. By use of Streptex (Murex Biotech) reagents, characteristic b-hemolytic colonies on horse blood agar were identified as being of Lancefield group A. Emm gene determination, T-protein typing, and testing for the serum opacity factor were performed at the Institute of Environmental Science and Research Limited in Porirua, New Zealand. The emm gene was amplified by PCR, and the product of the amplification was subjected to restriction fragment–length polymorphism analysis. Those isolates that yielded a distinct pattern, as well as a representative subset of the isolates that yielded an identical pattern, were sequenced. The throat swab specimens obtained 176 • CID 2003:36 (15 January) • Levy et al. RESULTS Time course and clinical features of the outbreak. The 72 case patients presented in 2 distinct groups: 57 (79%) presented from 18 through 21 December, and 15 (21%) presented from 23 through 26 December. The median date of presentation was 19 December (figure 1). For tonsillopharyngitis, the primary and secondary attack rates were 22% and 8%, respectively. The denominator used for the calculation of the secondary attack rate was 199 (the total no. of inmates [256] minus the total no. of inmates with primary cases [57]); 15 secondary cases were identified. Inmate survey results. A total of 154 (60%) of 256 questionnaires were completed, but 67 were unsuitable for analysis. The responses to the remaining 87 questionnaires were analyzed (table 1). The only association with streptococcal tonsillopharyngitis was consumption of the curried egg rolls served at lunch on 15 December; however, this association did not reach statistical significance (P p .06 ; risk ratio, 1.50; 95% CI, 1.05–2.14). Meal arrangements at the correctional center and findings of kitchen inspections. Breakfast consisted of cereal provided in single-serving packets and toast. There were limited on-site kitchen facilities that were used to prepare lunch, which consisted of bread rolls. Five inmates who were assigned to work in the kitchen prepared bread rolls with 2 different fillings each day. Two teams of kitchen workers each prepared bread rolls for half of the inmates and handled both of the fillings. For curried egg rolls (i.e., curried egg salad sandwiches), the eggs were boiled and then stored in a refrigerator overnight. The next morning, the shells were removed and the eggs mashed. Curry powder and mayonnaise from a bulk storage container were added, and the mixture was spread onto a buttered bread roll. Although disposable gloves were available, gloves were not being worn by the food handlers at the time of the kitchen inspection. It was not possible to determine whether gloves had been worn when the eggs were prepared on 15 December, Table 1. Association of consumption of various foods with cases of streptococcal illness occurring during an outbreak among 256 inmates at a rural correctional center in New South Wales, Australia. a Food (date consumed) Devon/tomato roll (15 Dec 1999) Risk ratio (95% CI) 1.13 (0.08–1.59) Curried egg roll (15 Dec 1999) b 1.50 (1.05–2.14) Vegetarian meal (15 Dec 1999) 0.58 (0.02–5.78) Lamb stew (15 Dec 1999) 1.10 (0.78–1.55) Chicken/cheese roll (16 Dec 1999) 1.13 (0.86–1.50) Baked beans roll (16 Dec 1999) 1.08 (0.60–1.95) Beef pasta (16 Dec 1999) 1.23 (0.89–1.70) Vegetarian meal (16 Dec 1999) 0.58 (0.07–4.71) Tuna roll (17 Dec 1999) 1.13 (0.71–1.77) Corned beef roll (17 Dec 1999) 1.05 (0.70–1.59) Tempura fish (17 Dec 1999) 0.93 (0.63–1.38) Vegetarian meal (17 Dec 1999) 4.50 (0.80–25.20) NOTE. Association was determined on the basis of responses to a questionnaire administered to all inmates. The questionnaire was created using information from the menus for 15–17 December. Data from 87 of the 256 questionnaires administered were analyzable. a b “Roll” denotes a sandwich. Curried egg salad sandwich. whether the usual routine had been followed, or whether there were any temperature-time violations of safe food-handling practices. All members of the kitchen staff denied having any lesions on their hands. However, the clinic staff remembered dressing 5-day-old wounds for 1 of the 5 food handlers earlier that day. The worker was removed from kitchen duty, and swab specimens of the 2 hand wounds were obtained. Since August 1999, there had been a cook-chill meal service for the hot evening meals. These meals were prepared at a correctional center in metropolitan Sydney and delivered twice a week (journey length, ∼4 h) in a refrigerated truck. During a visit to the facility in Sydney that prepared the cook-chill meals, the hands of all workers present were examined for skin lesions, and the workers were also asked about recent wounds on their hands. There were no hand wounds evident, nor were any reported by the kitchen workers from the previous week. Throat swab specimens were obtained from 5 of the food handlers. Results of microbiological testing. Streptococcus pyogenes was isolated from 5 of the 6 throat swab specimens obtained on 19 December. These isolates were all found to be the same type (M75, T25). Group A streptococcus was isolated from the throat and skin lesions of one member of the kitchen staff, and these isolates were also type M75, T25. A second member of the kitchen staff also had a throat swab specimen that was positive for group A b-hemolytic streptococcus, but the isolate recovered was of a different type (M68, T nontypeable). Four throat swab specimens with positive results were obtained from patients who presented from 23 through 26 December. The isolates recovered from these specimens were all type M75, T25. Isolates recovered from the throat swab specimens obtained from 4 patients who presented 2 weeks later were M type 87. Group A b-hemolytic streptococcus was not detected in any of the throat swab specimens obtained from the kitchen staff that prepared cook-chill evening meals Literature search. Twenty-six of the reports published in English-language journals were obtained for review (table 2). It was determined that at least 10 additional outbreaks have been reported in non–English-language articles. These were not reviewed. DISCUSSION Outbreaks of milkborne streptococcal tonsillopharyngitis were not uncommon before the introduction of pasteurization [36–44], and they were of such magnitude that they were recognized in the wider community setting. There have been only ∼30 foodborne outbreaks described in the English-language literature, and most of these have been recognized in institutional settings or in association with community events (table 2). It is likely that other foodborne outbreaks occur but go unrecognized because the victims are widely dispersed in the community. Incubation periods (median time until onset of disease) of 32–52 h are frequently reported, with the first case patients developing symptoms as early as 6–8 h after exposure [21, 25, 31, 33]. In other outbreaks, the median time until onset has been as long as 96 h, with the first case patients presenting 2 days after the probable exposure [10]. A longer incubation period may be the result of a lower inoculum in the contaminated food. However, determination of the incubation period is influenced by the data used to construct the epidemic curve. In calculating the incubation period, use of the date of presentation for medical attention can delay the apparent onset of the outbreak up to 24–32 h, compared with use of the time to development of symptoms [5, 14]. Both the definition of secondary cases as those that occurred either 172 h after the onset of the first case or 172 h after consumption of the implicated food and the exclusion of these cases from the aforementioned calculation also influence the apparent incubation period. Nevertheless, all of the reported foodborne outbreaks have had a median incubation period of 1–4 days [44]. As in the outbreak that we report here, the limitations of the investigation may preclude a definitive conclusion regarding the source (and time) of exposure, rendering estimates of the incubation period tentative. In some outbreaks, illness among people consuming leftovers has provided supportive evidence and has made it possible to distinguish between several possible foods as causes Foodborne Group A Streptococcus • CID 2003:36 (15 January) • 177 Table 2. Reference Previous reports of foodborne outbreaks of group A streptococcal infection. Date of outbreak Location Setting No. of cases 178 [1] Jul 1941 Massachusetts, US Church lunch Jun 1942 Western US Army base [3] Nov 1942 United Kingdom Air Force base [4] Nov 1943 North Carolina, US Army base [5] Sep 1951 Army base [6] Mar 1952 Cambridge, United Kingdom Army camp 43 [7] Feb 1957 Maryland, US Charity lunch [8] Sep 1965 Buffalo, US University cafeteria — [9] Apr 1968 Colorado, US Air Force Academy ∼1200 [10] Jul 1973 Arizona, US Community picnic– Indian Reservation 255 Potato salad (included a sliced eggs) Four food handlers, 1 of whom had a son with pharyngitis T3/13/B3264 [11] Aug 1974 Florida, US Prison 290 Egg salad sandwich One of 5 inmates who peeled the eggs had a fever and a sore throat; a throat swab specimen was positive for the outbreak strain M9, T9 [12] Apr 1975 Perm, Russia [13] 1976 Ashdod, Israel [14] May 1980 Israel Military base 41 Boiled egg salad One of the kitchen workers had tonsillitis 3 days before the outbreak; he and 5 other kitchen workers were positive for the outbreak strain M3 [15] May 1981 Oregon, US Microbiology conference ∼300 No specific food identified Four of 10 food handlers had positive throat swabs, and 3 had skin lesion swabs positive for group A streptococcus M–nontypeable, T9, SOR⫹ [16] Jul 1982 Private party 34 — A food handler, who was asymptomatic, had a positive throat swab; a household contact had acute pharyngitis shortly before the party M–nontypeable, T12, SOR⫹ [17] Nov 1983 Tennessee, US Charity luncheon 20 Rice dressing [18] 1983 [19] Mar 1984 Missouri, US New Hampshire, US Japan — Factory ∼300 89 Ham Typing of Streptococcus isolates Status of food handlers [2] Northern Germany 102 Food that was the presumed cause of the outbreak One of 2 cooks had an early stage of scarlet fever Griffith 2 Not identified — Griffith 15 Tinned milk Cook in charge of preparation of tinned milk was infected with streptococci Type 9 125 Creamed eggs No findings despite thorough investigation M5 265 Not identified Thirty cooks; no specific findings Custard (the “skin”) One of the food handlers had a cough at the time of custard preparation; a throat swab specimen obtained 2 days later had a positive result Egg salad Food handlers had positive results of testing done Type 25 6 days after food preparation Shrimp salad Three food handlers who prepared the shrimp salad had negative throat swab specimens 500–600 Tuna salad that contained Thirty persons present at the salad preparation; boiled eggs 1 of 6 of those involved in egg preparation was throat swab positive 185 Sour cream — 447 Egg salad — — — Conference luncheon 60 — Mousse (most probably) and macaroni salad (less likely) — Type 9 Not typed (coinfection with S. flexneri) M–nontypeable, T12 — M-nontypeable, T12 Person who had prepared the implicated dish had M–nontypeable, T8/25, SOR⫹ had pharyngitis 3 weeks earlier and was culture positive at the time of the outbreak — One food handler reported a sore throat; 5 food handlers had negative throat swabs and no visible hand lesions (8 days later) — — 179 [20] Aug 1984 Puerto Rico Private party [21] Jul 1986 Venice, Italy 5 Banquets in the same restaurant [22] 1988 Turkey [23] Jun 1988 Israel [24] 1989 Russia [25] Apr 1990 Israel [26] May 1990 Sweden [27] 1990 Sweden [28] Feb 1991 Israel [29] — Military bases with a central kitchen — Military base Church party 179 58 439 Conch salad Four food handlers had negative throat swab specimens and were asymptomatic M–nontypeable, T12, SOR⫹ Prawn cocktail in banSix of 18 staff members (5 of whom were from quet 1, squills and custhe manager’s family) and 3 other children of tard cake in banquets the manager were positive for epidemic strain 2–4, and no identified b food in banquet 5 M28, T28 Bean salad with boiled egg M11, T3/13/B3264 No specific food identified — Two of 12 asymptomatic food handlers had throat swab specimens positive for group A streptococcus (not typed) — — — 61 Boiled egg salad, cabbage salad, and probably egg salad Two of 19 food handlers were symptomatic; both had throat swab specimens positive for the epidemic strain 122, including Sandwiches, including 1 death egg Probable M29 variant, T-nontypeable — M-nontypeable, T12 Six of 7 food handlers had positive throat swab Fifty-one of 58 were T28; 5 of 58 were specimens; 5 of these 6 attended the party and T28/4; 2 of 58 were autoagglutinin. ate the food. The one who did not attend the The strain from the deceased and 4 party had nasal symptoms 2 days before the random specimens were positive for party and peeled eggs the day before the party; erythrogenic toxins B and C. a second food handler was symptomatic on the day of the party. — — Military base 75 Cabbage salad Three soldiers were symptomatic before the implicated meal; one was the cook who was throat swab positive for the outbreak strain M56, T28 May 1991 Louisiana, US School banquet 71 Macaroni with cheese sauce Food handlers had negative throat swab specimens; 1 food handler had a positive result of culture of a hand lesion M9, T5/9 [30] 1991 Djibouti Military base [31] Apr 1992 Israel Air Force base [32] May 1993 [33] May 1996 Aichi Prefecture, Japan [34] 1997 Fukuoko Prefecture, Japan — — — — — [35] 1997 Ibaragi Prefecture, Japan — — — — — NOTE. a b c — 23 — — — 197 White cheese — — Food handler was asymptomatic but was throat swab positive; he did not taste the cheese and was absent at the time of the outbreak — M-nontypeable, T11 M-nontypeable, T 8/25/Imp19 Military unit 162 Butter — T11 Sports meeting 244 Boiled eggs, boiled fish paste, fried chicken, c and wakame-gohan — T1 (PFGE identical) S. flexneri, Shigella flexneri; SOR⫹, serum opacity factor positive; US, United States. Culture positive for epidemic strain. A chopping board was also found to be culture positive. All culture positive. of the outbreak [7, 10, 26, 31, 33]; however, at the same time, it has confounded the study of secondary spread of the illness. Illness among people eating a meal as guests in an institutional setting may provide useful supporting evidence as to which meal—if not which item of food—was associated with the outbreak [23, 25]. Reported attack rates of tonsillopharyngitis due to foodborne group A streptococcus vary from 10% to 85%. The level of preexisting immunity to the outbreak strain in the exposed group of people is an important influence on the attack rate, as is the level of contamination of the food. In the outbreak reported by Getting et al. [1], increasing attack rates were seen among groups of people consuming leftover food later in time, and this was attributed to the ongoing multiplication of the organism. In our investigation, as in the outbreak reported by Boissard and Fry [6], it is possible that only half of the incriminated food was likely to be infective; this possibility not only reduces the ability to demonstrate an association but, also, reduces the apparent attack rate. The choice of denominator used to calculate the attack rate also influences the result. In most reports, the total number of attendees at the meal or function associated with the outbreak has been used, but the proportion of attendees who consumed the contaminated item varied significantly. In instances in which data collection was relatively complete and in which the attack rate was calculated with a denominator denoting the number of attendees who consumed the suspect food, attack rates as high as 80% have been reported. The attack rate also depends on whether asymptomatic subjects with throat swab specimens found to be positive for the outbreak strain are included in the case definition. This increases the apparent attack rate associated with outbreaks in which microbiological sampling of the entire exposed cohort is able to be performed [28]. Secondary cases of streptococcal tonsillopharyngitis that occur in the context of a foodborne outbreak are believed to be a result of the usual mode of spread via respiratory droplets. Of major practical importance in outbreaks that occur in institutional settings is the question of whether secondary spread would be expected to be of sufficient magnitude to warrant prophylaxis. Guided by the only other report of an outbreak in a custodial setting [11] and some of the reports of recent outbreaks in military settings [25, 28, 31], in which the incidence of secondary cases was as low as 2%–5%, we did not offer prophylaxis to asymptomatic inmates. The secondary attack rate of 8% among asymptomatic inmates was higher than expected, although it was approximately half that described in some other outbreaks [4, 9, 10]. In several outbreaks, cases presenting 172 h after the onset of the first case were onequarter to one-third of the total number of cases. A variety of factors influence the potential for secondary 180 • CID 2003:36 (15 January) • Levy et al. spread, and the study of secondary spread is difficult. In an institutional setting, “evidence of secondary spread of streptococcal infections after a foodborne epidemic is frequently obscure because of the difficulty of observing an adequate population which is exposed only to secondary infection and not to the primary source” [4, p. 194]. Some of the later cases, rather than being the result of secondary spread, may be either primary cases in which infection has resulted from a lower inoculum of the organism or cases caused by infection occurring at subsequent meals (if there is further contamination by the same infected cook or contaminated utensils). Evidence for the latter possibility is provided in the report by Claesson et al. [26], in which an apron cultured 6 days after the meal was found to be positive for the epidemic strain of group A streptococcus, and, also, in the report by Gallo et al. [21], in which attendees at 5 separate banquets were infected, different foods were implicated for different cohorts, and the outbreak strain was isolated from a chopping board as well as from members of the restaurant staff. In the community setting, ascertainment of secondary cases is incomplete, and determination of a denominator for calculation of the attack rate is impossible. In closed communities, the potential for secondary spread is partially determined by the proportion of individuals who were not exposed to an infective inoculum in the first instance. In the outbreak we have described, it is possible that as few as one-quarter of the inmates may have had primary exposure (if only half of the inmates had chosen curried egg rolls and only half of the curried egg rolls were contaminated). In most military outbreaks, ill soldiers were separated from unaffected soldiers immediately after presentation, which would have limited the opportunity for secondary infection. It is unclear whether infected inmates were segregated during the outbreak in the Florida jail reported by Ryder et al. [11], but penicillin therapy was initiated within 2 h of presentation. The length of time that may elapse prior to initiation of penicillin therapy before such therapy loses its effectiveness in preventing secondary spread of illness is unknown. In many of the reported outbreaks, the epidemic strain has been isolated from throat swab specimens obtained from ⭓1 food handler. In some instances, the cook was symptomatic at the time of food preparation [3, 6, 19, 25, 28]. More frequently, the cook was asymptomatic, although some of the asymptomatic cooks had household contacts with a recent clinical illness. One cook had had follicular tonsillopharyngitis 3 weeks previously but had received antibiotic therapy for only 3 days [14]. Skin lesions on the hands have also been implicated as a source of group A streptococcus [29], although coexisting pharyngeal colonization may also be present [15]. The types of foods implicated in foodborne outbreaks of streptococcal tonsillopharyngitis suggest that contamination of the hands with respiratory secretions is an important means of infecting the food. Eggs, crustaceans, sandwiches, and salads, all items that involve significant hand contact during preparation, account for 15 of 21 outbreaks in which a specific food was identified. In addition, in virtually all of the reported outbreaks, there were time-temperature violations of safe foodhandling practices that would have allowed for multiplication of the organism in the food incriminated in the outbreak. The majority of reported outbreaks have occurred in the warmer months. The severity of the clinical illness has been reported to be mild in some outbreaks [28] and severe in others, with myalgia and prostration [5, 6, 9, 20, 26]. In some studies, gastrointestinal symptoms have been prominent, with up to 20% of patients reporting diarrhea, vomiting, or both [7, 11, 17, 21, 25, 33]. Getting et al. [1] demonstrated production of an enterotoxin by the causative organism associated with an outbreak at a church reunion. Although the rate of complications usually is low, serious complications do occur. In several of the outbreaks reported during the first half of the 20th century, scarlet fever occurred in a significant percentage of patients. In the outbreak that occurred at Fort Bragg in 1943 [4], there were 3 definite and 2 possible cases of rheumatic fever in a group of 100 patients with tonsillopharyngitis. A 45-year-old man died in a outbreak due to an isolate that produced pyrogenic exotoxins B and C [26]. 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