Outbreaks of Typhoid Fever in the United States, 1960–99

Home , Asymptomatic carrier

Epidemiol. Infect. (2003), 130, 13–21. f 2003 Cambridge University Press DOI: 10.1017/S0950268802007598 Printed in the United Kingdom

Outbreaks of typhoid fever in the United States, 1960–99

S. J. OLSEN 1,2*, S. C. BLEASDALE1,A.R.MAGNANO1, C. LANDRIGAN1, B. H. HOLLAND 1,R.V.TAUXE1,E.D.MINTZ1 AND S. LUBY1

1 Foodborne and Diarrheal Diseases Branch, Division of Bacterial and Mycotic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, 1600 Clifton Road, Atlanta, GA 30333 2 Epidemic Intelligence Service, Division of Applied Public Health Training, Epidemiology Program Oﬃce, Centers for Disease Control and Prevention, 1600 Clifton Road, Atlanta, GA 30333

(Accepted 17 July 2002)

SUMMARY Although the incidence of typhoid fever in the United States has been low since the 1940s, Salmonella Typhi continues to cause outbreaks. We reviewed reported outbreaks of typhoid fever from 1960 to 1999. There were 60 outbreaks; in 54, exposure occurred within the United States. These 54 outbreaks accounted for 957 total cases (median 10) and 4 deaths. In 36 (67%) outbreaks the route of transmission was identified, and in 16 (62%) of the 26 foodborne outbreaks an asymptomatic carrier was identified by culture or serology. The median incubation period was 2 weeks. Isolates from 10 (40%) of 25 outbreaks were phage type E1. The average frequency of outbreaks decreased from 1.85/year during 1960–79 to 0.85/year during 1980–99 (P=0.0001). S. Typhi outbreaks in the United States are generally small in size but can cause significant morbidity, and are often foodborne, warranting thorough investigation.

INTRODUCTION [2]. Since then, the majority of the approximately 250 infections in the United States reported to the Centers Infection with Salmonella enterica subspecies enterica for Disease Control and Prevention (CDC) each year serotype Typhi (S. Typhi) causes an enteric fever are sporadic, that is, not related to a recognized out- better known as typhoid fever [1]. Typhoid fever was break. Most of these infections are acquired abroad; endemic in the United States in the late 19th and early from 1985 to 1994, 72% of persons with S. Typhi 20th centuries and remains endemic in many devel- infection reported travelling outside the United States oping countries. In the United States, several public within the 30 days preceding their illness onset [3]. health actions, including widespread chlorination of Infection with S. Typhi, when not diagnosed and drinking water supplies, pasteurization of milk, better treated promptly, can cause severe illness and death. shellfish sanitation, and improved sewage disposal The dramatic decrease in the incidence of typhoid practices, led to a dramatic decline in the incidence of fever in the United States has resulted in a population S. Typhi infections in the early and mid-20th century that is immunologically susceptible to S. Typhi infection. Since outbreaks of typhoid fever have become * Author for correspondence: CDC Box 68, American Embassy, relatively rare [3], the vast majority of local and state APO AP 96546. Current affiliations: S. Olsen, International Emerging Infections public health authorities have little or no experience in Program, CDC, Bangkok, Thailand. S. Bleasdale, Rush Presby- investigating them. Moreover, certain characteristics terian St. Luke’s Medical Center, Chicago, IL, USA. A. Magnano, of S. Typhi infection, including the prolonged incuba- Columbia Presbyterian Hospital, New York, NY, USA. C. Lan- drigan, Children’s Hospital, Boston, MA, USA. tion period and the prolonged asymptomatic carrier 14 S. J. Olsen and others state, pose peculiar challenges to investigators. From Outbreaks with exposure within the United States a clinical perspective, typhoid fever is becoming Clinical and epidemiologic description more difficult to treat as antimicrobial resistance in- creases [4]. In the 54 outbreaks with exposure within the United We reviewed S. Typhi outbreaks over the last 40 States, the total number of persons ill was 957 (me- years to characterize epidemiologic patterns and dian 10, range 2–210). The median number of persons trends in the United States. These data help to with culture-confirmed infection was 7 (range 1–180). better define the ongoing risk of S. Typhi outbreaks In 15 outbreaks for which ages were reported, the for the US population. median age of patients was 26 years (range 0–89 years). Of the 18 outbreaks for which gender was reported, 231 (44%) of 531 patients were female. Of the 38 out- METHODS breaks for which hospitalization was reported, the We abstracted data on all reported S. Typhi out- median number of persons hospitalized was 5 (range breaks in the United States from 1960 to 1999. Out- 0–170). The median hospitalization rate was 79% breaks were identified through a review of CDC’s (range: 0–100%). There were 4 reported deaths, 1 each National Salmonella Surveillance System, Foodborne in 1964 and 1979, and 2 in 1971, yielding an overall . Disease Outbreak Surveillance System, and Morbid- case fatality rate of 0 4%. ity and Mortality Weekly Report, and through a Pub- For 36 outbreaks in which route of transmission Med Medline query using the key words ‘typhoid’ was identified, 26 (72%) were foodborne, 6 (17%) and ‘outbreak’ and limiting the results to English. were attributed to contaminated water or ice, and 4 All outbreaks had laboratory confirmation (culture (11%) were attributed to either food or water (Table or serology) of Salmonella Typhi. Data abstracted 1). Only one of these outbreaks, in 1999, was caused included date, location, and duration of the outbreak, by a food product contaminated before final prep- number of persons affected, exposure information, aration [5]. In 16 (62%) of the 26 foodborne out- incubation period, and the antibiotic resistance pat- breaks, 1 (17%) of the 6 waterborne, and 3 (75%) of tern and phage type of outbreak isolates. Possible the food- or waterborne outbreaks an asymptomatic outbreaks for which there were laboratory data but carrier was identified by either culture or serology as no corresponding descriptive data by which to estab- the likely source. Outbreaks with a determined route lish an epidemiologic link were not included in this of transmission were statistically significantly larger review. in size than those without (median number of persons . Attack rates were calculated by dividing the num- ill: 11 vs. 5, respectively, P=0 0008). ber of persons who became ill by the total number The median incubation period for seven outbreaks of exposed persons. Outbreaks were grouped into with a known exposure date and sufficient data on geographic region using the nine divisions established onset dates was 14 days (range of individual incuba- by the US Census Bureau. tion periods, 4–33 days) (Table 1). The median attack . The incidence of laboratory-confirmed S. Typhi in- rate was 23% (range 0 3–80%) for the 28 outbreaks fections was calculated using reports from state health in which the number of persons exposed was known. departments to CDC through the Public Health Lab- There were too few outbreaks with sufficient data to oratory Information System (PHLIS) and US Census examine the relationship between median incubation data as the denominator. Incidence rates were calcu- period and attack rate or median incubation and route lated per 100 000 000 persons per year. Means were of transmission (e.g. food vs. water). The median time compared using analysis of variance and the Kruskal– from onset of illness in the first patient until investi- Wallis test for non-parametric data. gation of the outbreak was 27 days (range 0–161). The median duration of an outbreak was 1 month (range 9–150 days). RESULTS Temporal and geographic distribution Sixty outbreaks of typhoid fever in the United States were reported from 1960 to 1999; 54 outbreaks were The 60 outbreaks occurred from 1964 to 1998 (Fig. 1). caused by an exposure within the United States and A median of one outbreak occurred per year (range the remaining 6 were travel-related (Table 1). All but 0–6). From 1970 to 1999, the annual incidence of 1 of the 60 outbreaks had been reported to CDC. reported laboratory-confirmed S. Typhi infections, Typhoid fever outbreaks in the United States 15 including outbreak-associated and sporadic cases, de- age of the carrier was known, the median age was creased from 261 to 129/100 000 000 persons (Fig. 1). 61 years (range 16–89) and in the 18 outbreaks where Fifty-eight percent of outbreaks occurred from May the sex of the carrier was known, 89% were female. to August, while only 9% occurred from January to In the 10 outbreaks in which country of birth of the April (Fig. 2). Outbreaks were reported in all regions carrier was known, 8 (80%) were foreign born. In the of the country: 11 (20%) occurred in the South Atlantic 9 outbreaks in which a travel history for the carrier region; 9 in Mid-Atlantic; 6 each in East South Central, was known, 7 (78%) reported travelling outside the West South Central and Mountain; 5 in Pacific; 4 each United States and 3 of those had travelled within the in New England and East North Central; and 3 in previous year. None were known to be carriers before West North Central regions. There was no association the outbreak; however, in the 17 outbreaks in which between month of onset and region. the carrier was asked about a history of typhoid fever, We examined the 54 outbreaks in which exposure 5 (29%) reported having had typhoid fever. Overall, occurred in the United States by 20-year time periods, 13 (62%) of 21 were either foreign born, reported trav- 1960–79 and 1980–99. The average number of out- elling outside the United States within the last year, breaksper year decreased significantly from 1.85/year or had a history of typhoid fever. In 16 (62%) of 26 between 1960 and 1979 to 0.85/year between 1980 foodborne outbreaks, an asymptomatic carrier was and 1999 (P=0.0001). During these two time periods identified; in 7 outbreaks the carrier prepared food for the median number of persons ill increased from 7 to family or friends, in 6 outbreaks the carrier was em- 16, respectively (P=0.10), but the median attack rate ployed as a commercial foodhandler, in 2 outbreaks decreased from 25 to 14% respectively (P=0.14); the carrier was a relative of the main food preparer, and neither difference was statistically significantly. The in 1 outbreak the carrier probably served the food. proportion of outbreaks in which the route of transmission was identified increased significantly from Laboratory results 49% (18/37) in 1960–79 to 88% (15/17) in 1980–99 The phage type of S. Typhi isolates from 25 (46%) of . (P=0 006). the 54 outbreaks was known (Table 1). Ten (40%) were phage type E1, 3 were B3, 2 each were F1 and 35 Setting and source of outbreaks and 38, and 1 each were B1, B2, C1, E9, F3, T, react A variety of different food vehicles were identified, but does not conform (RDNC), and degraded Vi. and cooked and non-cooked foods were both promi- Antimicrobial susceptibilities of S. Typhi isolates nent (Table 1). Of the 26 foodborne outbreaks, from eight outbreaks were reported. In three out- 9 were linked to fresh salad or produce, 4 to seafood breaks, all occurring after 1979, isolates were resistant or shellfish, 4 to meat, 7 to various other foods, and to ampicillin, chloramphenicol, and trimethoprim– 2 were unknown. There was only one incident of sulphamethoxazole. In two outbreaks which occurred a commercial food contaminated before final pre- in 1975 and 1981, isolates were resistant to ampicillin paration [5]. Of the 26 foodborne outbreaks, in 13 and chloramphenicol. In two outbreaks which occur- outbreaks the food was prepared in a restaurant or red in 1973 and 1978, isolates were resistant to ampi- commercial enterprise, in 11 outbreaks it was pre- cillin only, and in one outbreak in 1986, isolates were pared in a home, and in 2 the setting was unknown. resistant to chloramphenicol only. There were six outbreaks in which contaminated water was the most likely vehicle. In three of these Outbreaks with exposure outside the United States outbreaks there was apparent sewage contamination; In 6 reported outbreaks exposure occurred outside in four outbreaks the water system was a well. All of the United States, 2 in Mexico, 2 in Europe, 1 in Haiti, these outbreaks occurred before 1975. and 1 in Canada (Table 1). Three of the six outbreaks involved persons from more than one state, and Characteristics of carriers the median number of persons ill was 4 (range 2–9). In 21 (39%) outbreaks, an asymptomatic carrier In three outbreaks for which data were available, whose infection was confirmed by culture or serology the median rate of hospitalization was 67% (range was identified as the source; in one outbreak two car- 5–100%). In four outbreaks with outcome data, there riers were identified. Only one carrier was confirmed were no reported deaths. Four of the outbreaks occur- by serology alone. In the 12 outbreaks in which the red in August and one each in July and November. 6S .Osnadothers and Olsen J. S. 16

Table 1. Epidemiologic and laboratory characteristics of Salmonella Typhi outbreaks, United States, 1960–99

Onset month*/ Incubation# Phage No. year State(s) Setting [reference] Presumed source No. ill Attack rate (days) type

1$ 7/64 NE Mexico Unknown 2 2 8/64 NY Neighbours Watermelon ﬁshed from Hudson River 10 56% (10/18) T 3 8/64 GA Neighbours Unknown (possible carrier as food handler) 14 E1 4 12/64 NM Wedding reception Chicken salad made by carrier (+) 44 22% (44/200) 19.5F1 5 12/66 LA Home Unknown 8 80% (8/14) B2 6 2/67 CO Luncheon Food prepared by carrier (+) 11 20% (11/55) 7 5/67 CA Fraternity house [19] Food prepared by carrier (+)or 26 38% (26/68) B1 water contaminated with sewage 8$ 8/67 OR Canada, lake resort Water contaminated with sewage 3 9 8/68 MO Church camp [20] Food or ice handled by carrier (+) 25 13% (25/189) 18 C1 10 7/69 CT Restaurant Meatball sandwiches made by carrier (+)4 F1 11 11/69 NM Home Well water 4 12 11/70 MD Home Well water contaminated with sewage 4 31% (4/13) 13 11/70 WI Community Unknown 6 14 6/71 PA Unknown Unknown 3 15 7/71 PA Church supper Food, possibly eggs contaminated by carrier (+) 33 25% (33/130) F1 16$ 8/71 VA, AL Europe, student tour Possibly water 8 Degraded Vi 17$ 8/71 NY, NJ, Spain, school tour Possibly water 5 CO 18 9/71 VA Playground Sewage contamination, possible carrier 11 37% (11/30) 19 ?/71 MI Nursing home Unknown 3 20 11/71 MI Cruise ship Unknown 19 56% (19/34) 21 4/72 WA Home Well water contaminated with sewage, 4 80% (4/5) neighbour carrier 22 6/72 AL Several families Unknown (visit from carrier in Ohio) 7 23 7/72 MA Home Unknown (carrier) 3 23% (3/13) 24 1/73 FL Migrant farm camp [21] Well water with carrier (+) 210 15% (210/1400) E1 25 6/73 MO Family Unknown 3 50% (3/6) 26 7/73 AL Home Unknown 5 27$ 8/73 AK, ID Mexico Unknown 3 28 9/73 AZ Extended family Unknown 7 2% (7/315) E1 29 10/73 AL Unknown Unknown 2 50% (2/4) 30 11/73 NJ Church supper Fish whiting 25 24% (25/105) 31 5/74 NY Family Unknown (grandmother known carrier) 3 32 5/74 WA Community Water and possible carrier 5 33 5/74 MS Unknown Unknown (grandmother known carrier) 3 34$ 11/74 CT Haiti Unknown 9 35 5/75 FL Concession stand Snow cones (food or ice) 5 RDNC· 36 6/75 TX Restaurant [22] Salad with guacamole made by carrier (+)19 37 9/75 LA Private reception Homemade pies made in household of 517 with caterer carrier (+) 38 12/75 NY Restaurant [23] Mashed potatoes 28 5% (28/572) 14 B3 39 6/76 FL Factory Peruvian cheese and potato dish made 9 20% (9/45) 8.5 35, 38 by carrier (+) 40 5/77 WA Outdoor camp Unknown 4 41 9/77 TN Unknown Barbecue beef 26 42 7/78 NY Two parties [24] Cake 11 10% (11/110) F3 43 8/79 MS Homes of distant relatives Unknown with carrier (+)4 44 5/80 MO Social functions Food served by carrier (+) 11 31% (11/36) E9 45 8/80 TX Camp Tossed salad made by ill cook 16 4% (16/449) B3 46 4/81 AZ Birthday party [25] Chicken with chilli and potato salad made 613 by carrier (+) 47 8/81 TX Restaurant [26, 27] Cows’ head (barbacoa) made by carrier (+)80 B3 48 10/81 MI Luncheon [28] Food or ice handled by carrier (+) 17 7% (17/257) E1 49 10/83 TX University cafeteria Unknown 10 <1% (10/3000) E1 50 8/86 MD Restaurant [29] Shrimp salad handled by carrier (+) 10 Degraded Vi

51 5/87 NH Restaurant Fried clams from Spain not thoroughly cooked 2 17 States United the in outbreaks fever Typhoid 52 6/89 NY Hotel [30] Orange juice handled by carrier (+) 68 42% (68/163) E1 53 3/90 MA Home/restaurant Raw shellﬁsh (lappas) 4 E1 54 5/90 AZ Restaurant Guacamole made by carrier(s) (+) 21 12 35, 38 55 6/90 WA, CA Party at community Potato salad made by carrier (+) 18 6% (18/293) E1 centre [31] 56 8/90 MD Family picnic [32] Potato salad made by carrier (+) 24 40% (24/60) 57 10/90 NY Baptismal party Potato salad made by carrier (+) 7 21% (7/34) 58 9/93 FL Community Unknown 18 E1 59 11/96 FL Neighbours Homemade cheese from Mexico 9 60 12/98 FL Community [5] Frozen mamey from Guatemala 16

* Month of ﬁrst onset of illness. # Median. $ Travel-related outbreak. · React but does not conform. (+) Asymptomatic carrier identiﬁed by culture or serology. 18 S. J. Olsen and others

Number of outbreaks Incidence per 100000000 8 350 Outbreaks with exposure within the United States

7 Outbreaks with exposure outside the United States 300

6 250

5 200 4 150 3

100 2

1 50

0 0 1960 1962 1964 1966 1968 1970 1972 1974 1976 1978 1980 1982 1984 1986 1988 1990 1992 1994 1996 1998 Year Fig. 1. Number of Salmonella Typhi outbreaks and incidence per 100 000 000 persons per year, United States, 1960–99.

Percentage of outbreaks 25

20 Outbreaks with exposure within the United States Outbreaks with exposure outside the United States

0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Month Fig. 2. Percent of Salmonella Typhi outbreaks by month, United States, 1960–99.

No information on incubation period was available since this trend coincides with an overall decrease and no carriers were identified. Isolates from only in the incidence of laboratory-confirmed S. Typhi one outbreak were available for testing. The phage infections. Although the reasons for the decline are type was degraded Vi, but the antimicrobial resist- unknown, several factors, including more wide- ance pattern was not determined. spread use of the typhoid vaccine among travellers [3], thorough outbreak investigations, and aggressive identification and treatment of carriers, may have DISCUSSION contributed to the decline in sporadic cases and Outbreaks of typhoid fever continue to occur oc- outbreaks. Interestingly, the proportion of reported casionally in the United States, although with de- infections that are outbreak-associated has remained creasing frequency. This likely reflects a true decline fairly constant at 9% except in 1990, a year with five Typhoid fever outbreaks in the United States 19 outbreaks, when 25% of infections were outbreak- contact and adequate hand washing with warm water associated (CDC, unpublished data). and soap, especially for professional foodhandlers Although we identified only 60 reported outbreaks, and for any person who prepares foods that will be the long and variable incubation period for typhoid eaten raw. fever and the intermittent excretion of S. Typhi by Although outbreaks in the United States are small chronic asymptomatic carriers makes it likely that in size, a large proportion of infected individuals are more outbreaks went unrecognized and unreported. hospitalized, reflecting the severity of typhoid fever In the United States, typhoid outbreaks affect a small and the need for prompt diagnosis and treatment. In number of persons and are most frequently caused addition, increasing antimicrobial resistance among by foodborne transmission. In this review, 85% of S. Typhi isolates in the United States [13] may lead to outbreaks were associated with contaminated food. treatment failure. Treatment of carriers is also critical This finding supports recent estimates that as much to prevent future spread; carriers can excrete S. Typhi as 80% of S. Typhi infections in the United States for many years after the initial infection [8]. are caused by foodborne transmission [6]. The ma- Prompt recognition and investigation of typhoid jority of these foodborne outbreaks are caused by an fever outbreaks is often difficult because of the asymptomatic chronic carrier employed as a food unusually long incubation period, which is longer preparer. and more variable than the incubation period for Similar to other reports [7, 8], carriers identified in other bacterial foodborne enteric pathogens, and the these outbreaks tended to be older women. S. Typhi is additional delay before an outbreak is brought to the well adapted to colonize the gallbladder, where it attention of public health officials and an investi- causes no acute symptoms and, even when recog- gation is launched. The paucity of outbreaks traced nized, is difficult to eradicate [8]. Older women are to commercial food products, and the small size of also at an increased risk of having gall stones [9], recognized outbreaks, suggest that processes used by and it has been suggested that the two conditions commercial food suppliers are effective in preventing may be related. Carriers were also frequently foreign- the introduction of S. Typhi to the food supply in the born. Although the place of birth was not consistently United States. However, food handled and processed reported for carriers identified through outbreak inves- in other countries may be at greater risk of S. Typhi tigations, the majority of those reported were from contamination. The single outbreak in this data set developing countries where typhoid fever has been caused by a commercial food product occurred in common (e.g. Mexico, Central America and Lebanon), Florida in 1998 and 1999 and was associated with and approximately one-third reported a history of eating frozen mamey fruit that was commercially typhoid fever. The two states that reported the most peeled, crushed, and processed in Guatemala [5]. outbreaks, New York and Florida, also rank second The recent increase in the proportion of fresh and fourth in net international migration [10], and thus fruits, vegetables, and processed food imported from may be likely to have a relatively high rate of carriers low-income countries [14] highlights the need for [7]. Nationwide, the percent of the population that continued attention to possible contamination of com- is foreign-born has doubled during 1970–98 (5–10%), mercial products. In addition, risk of infection in- and the percent of foreign-born persons that are from creases with international travel [3], as evidenced by Asia, an area of high S. Typhi endemnicity, has risen the recent outbreak among persons on a cruise ship steadily from 9% in 1970 to 27% in 1997 [11]. who were exposed to contaminated food during a stop As with outbreaks of many foodborne enteric in Papua New Guinea [15]. pathogens, including E. coli O157:H7, outbreaks of Routine vaccination against S. Typhi is not recom- S. Typhi infection increase in the warmer months [12]. mended in the United States and since there are Although the reasons for this are largely unknown, few infections, there is little natural exposure. As a seasonal factors, such as food cooking, handling, and result, the population is immunologically susceptible consumption behaviours may contribute to these dif- to infection and thus at risk for outbreaks. How- ferences. A variety of foods were implicated, reflecting ever, despite a constant influx of S. Typhi carriers contamination by hand contact and growth of bac- and occasional outbreaks, the small size of the out- teria in cooked foods left out for prolonged periods. breaks and their limited duration suggest that they are To prevent transmission, public health messages easily contained and do not spread into the broader should stress the importance of minimizing hand susceptible population [3]. This is further supported 20 S. J. Olsen and others by the decreasing incidence of infection in the United REFERENCES States [3]. In the early 1900s, massive multistate outbreaks of 1. Brenner FW, Villar RG, Angulo FJ, Tauxe R, Swami- typhoid fever due to untreated drinking water and nathan B. Salmonella nomenclature. J Clin Microbiol 2000; 38: 2465–7. oysters harvested in sewage-contaminated beds were 2. Tauxe RV. Salmonella: a postmodern pathogen. J Food common occurrences in the United States [16]. 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