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Salmonella Isolates from Humans in the United States, 1984-1986

Nancy T. Hargrett-Bean, Ph.D., Andrew T. Pavia, M.D., Robert V. Tauxe, M.D., M.P.H., Enteric Diseases Branch and Statistical Services Activity, Division of Bacterial Disease, Center for Infectious Diseases

INTRODUCTION

Since 1962, Salmonella surveillance activity has been conducted jointly by the Association of State and Territorial Epidemiologists, the State Public Health Laboratory Directors, and CDC. This surveillance system is a passive laboratory-based system that receives weekly reports from 49 states and the District of Columbia and receives regular summaries from the Food and Drug Administration and the U.S. Department of Agriculture. The objectives of the surveillance system are 1) to define endemic patterns of salmonellosis, particularly those with interstate ramifications, 2) to identify trends in disease transmission, and 3) to monitor control efforts. The following report is based on data collected by this system in the years 1984-1986. OVERVIEW

The Salmonella isolation rate reported to CDC continues to show a general upward trend (Figure 1). The number of Salmonella isolates from humans (including Salmonella typhi) reported to CDC was 36,061 in 1984, 56,750 in 1985, and 42,028 in 1986. Compared with the number reported in 1983 (38,886), these numbers represent a 7.8% decrease in reported isolates in 1984, a 48.5% increase in 1985, and an 8.1% increase in 1986. GEOGRAPHIC CHANGES

Table 1 shows the Salmonella isolates reported by region. The modest decrease in the number of reported isolates in 1984 was not confined to one state or region.States reporting decreases from 1983 included Arizona, 54% (518 to 239); Louisiana, 38% (892 to 556); Alabama, 34% (734 to 484); Texas, 20% (2,125 to 1,708); and New York, 17% (2,916 to 2,409).

The marked increase in the number of Salmonella isolates reported from 1984 to 1985 was due largely to a massive Salmonella typhimurium outbreak, which accounted for over 16,000 cases in the East North Central Region (1). States reporting large increases included Illinois, 614% (2,699 to 19,292); Indiana, 173% (443 to 1,210); Alabama, 53% (484 to 740); Michigan, 44% (1,403 to 2,026); Montana, 44% (64 to 92); South Dakota, 42% (62 to 88); and Louisiana, 42% (556 to 788).

Although the overall number of isolates reported in 1986 was lower than in 1985, many states reported more isolates in 1986 than in 1985, including Delaware, 138% (26 to 62); Alaska, 50% (119 to 178); Rhode Island, 46% (181 to 264); Washington, 43% (550 to 786); Wisconsin, 45% (630 to 915); Pennsylvania, 34% (2,253 to 3,021); and California, 32% (4,366 to 5,764). CHANGES AMONG COMMON SEROTYPES

In 1984, the 10 most frequently reported serotypes constituted 72% of all reported isolates (Table 2). During this year, reports of all serotypes decreased, except for Salmonella muenchen, which increased 5%, and Salmonella enteritidis, which increased 14%. Reported outbreaks of S. enteritidis occurred in a private home, a hospital, an industrial plant, a nursing home, a school cafeteria, a prison, a restaurant, and a wedding reception. Additional S. enteritidis outbreaks were associated with consumption of sausage in Washington, of rice pilaf in Pennsylvania, and of eggs in New Jersey.

In 1985, the 10 most frequently reported serotypes accounted for 82% of all reports. The number of S. typhimurium isolates increased 121% over the number reported in 1984; more than 16,000 cases were due to a milk-borne outbreak in Illinois and surrounding states. Reported Salmonella hadar isolates increased 357%. Outbreaks of this serotype were reported from Wisconsin, Washington, and New York; no vehicles of transmission were implicated. Reported Salmonella heidelberg isolates increased 45%; outbreaks were associated with consumption of eggs in New Mexico and of barbecue in California. Outbreaks of Salmonella newport, which increased 52%, were associated with consumption of raw hamburger in California and of raw milk in Washington.

In 1986, the 10 most frequently reported serotypes accounted for 82% of all reported isolates. During that year, reported S. typhimurium isolates dropped to the lowest level since 1980. This decrease was more than offset by increases in reported isolates of S. enteritidis, S. heidelberg, and S. hadar. In the period 1976-1986, the New England and the Middle Atlantic regions experienced a fivefold increase in the number of reported S. enteritidis isolates (2). Several reported outbreaks from these areas were associated with eggs and foods containing raw eggs. Reports of S. hadar isolates increased 30% over the number reported in 1985; Georgia reported an outbreak of this serotype. Reported isolates of S. heidelberg increased 8%, and outbreaks were associated with lupine beans in Massachusetts, roast pork in Delaware, frozen pasta in the Northeast, and chicken in Oklahoma, Wisconsin, and Hawaii. Increases in the number of reports of Salmonella saint paul (26% increase) were not confined to any single region. LESS FREQUENTLY REPORTED SEROTYPES

The reported number of Salmonella kottbus isolates increased from four in 1983 to 40 in 1984. California reported 24 of these isolates. The reported number of Salmonella berta isolates increased 127% from 44 to 100; Pennsylvania reported 16% of these isolates. Reports of Salmonella bonariensis increased from two to seven isolates, and reports of Salmonella carrau, from two to 12 isolates; these increases were not confined to any single state. The number of Salmonella braenderup isolates increased from 324 to 414; an outbreak of this serotype was associated with consumption of beef in New Jersey. The number of Salmonella bredeney isolates rose from 140 to 178. New York City reported an outbreak of this serotype that was associated with eating roast beef in a deli. Reported isolates of Salmonella ibadan increased from seven to 15; all reports were from Alabama, Arkansas, and Texas. Salmonella ohio isolates increased from 196 to 249; increases of this serotype were reported from Massachusetts, Hawaii, and California. The reported number of Salmonella brandenburg isolates increased from 58 to 88. Louisiana and New York together reported 20.5% of these isolates. Reported isolates of Salmonella adelaide increased from 45 to 78; Illinois, New York, and Virginia accounted for 51% of these isolates.

During 1985, the reported number of Salmonella poona isolates increased 154% (88 to 224). An outbreak of this serotype occurred in a school in Illinois. The number of S. kottbus isolates increased 208% (40 to 123). Outbreaks of this serotype were reported in Oregon and California. Increases were reported in Salmonella bere (two to 22), S. brandenburg (88 to 171), and Salmonella bovismorbificans (24 to 53); these increases were not confined to one state or region.

In 1986, reported isolates of S. braenderup increased 84% (334 to 616); an outbreak of disease in Illinois caused by this serotype was associated with eating tomatoes. Alabama reported 82% of the Salmonella bardo isolates, which increased from seven to 28 isolates. No single area was associated with the increased isolation of Salmonella alachua (150% increase, from 48 to 120), S. berta (90% increase, 126 to 240), and Salmonella johannesburg (170% increase, 17 to 46). S. TYPHI

In 1984, 458 isolates of S. typhi were reported; 121 were reported to have come from patients with typhoid fever, and 24, from carriers. In 1985, 470 isolates were reported, 71 from patients and 17 from carriers. In 1986, 541 were reported, 115 from patients and 14 from carriers. Patient or carrier status of the remainder of the S. typhi isolates for each of these years was not designated. The median age of patients was 22 years in 1984 and 24 years in 1985 and 1986, and the median age of carriers was 71, 58, and 69 years, respectively. AGE

Figure 2 shows age-specific isolation rates for the years 1970 and 1986. Patient age was reported for 79% of the isolates in the period 1984-1986. The rates of reported Salmonella isolates were highest for 1- to 4-month-old infants, decreased abruptly among early childhood age groups, remained relatively constant through the adult years, and then increased slightly in the age group over 80 years of age. The rates were slightly higher among males under 20 years of age and were slightly higher for females 40-69 years old. The median age of persons from whom isolates were obtained has increased from 6 years in 1970 to 18 years in 1984, 13 years in 1985, and 20 years in 1986. The largest increase in an age-specific isolation rate occurred among the 20- to 39-year-old age groups. COMMENT

This summary is based on the passive laboratory-based Salmonella surveillance activity, and the reports received in this system do not distinguish between symptomatic and asymptomatic infection or chronic carriage, except in the case of S. typhi. Cases of salmonellosis without laboratory confirmation are not included. The system has inherent biases that must be remembered. Many factors, including intensity of surveillance, severity of illness, access to medical care, and association with a recognized outbreak, affect whether an infection will be reported. Infants, the elderly, and severely ill patients are more likely to have stool cultures performed. Reporting of Salmonella isolates is incomplete, and the true incidence of salmonellosis is substantially underestimated. However, these data permit broad comparisons, provide information that may lead to epidemiologic investigations, identify trends, and allow some insight as to the effectiveness of public health interventions.

In general, the overall rate of Salmonella isolation has increased since 1976, with brief decreases in the years 1980 and 1984. During this period no major changes have been recognized in the Salmonella surveillance system, and the increase is limited to certain serotypes. Shigella isolates, reported through a parallel surveillance system, did not show a similar increase during this same period (3). Thus, the increase in the incidence of reported isolations is likely to represent a real increase in the incidence of Salmonella infections in the United States rather than improved reporting. The median age of persons from whom isolates were reported has continued to increase faster than the median age of the general population, and the rate of isolation has increased most among 20- to 39-year-olds. The reasons for this shift in age are unknown but may indicate that foods to which older children and adults are commonly exposed are becoming more important vehicles of transmission.

The increase in specific serotypes is only partially understood. In California a large and ongoing outbreak of S. newport infections was traced to a reservoir in dairy cattle used to make ground beef, and the spread of this epidemic strain to cattle in other states has been documented (4,5). The marked increase in S. enteritidis in the northeastern United States appears to be related to eating raw or undercooked eggs (6). S. heidelberg and S. hadar have been associated with consumption of poultry in the past, but it is not known if the current increases in these serotypes are related to poultry.

The serotyping of Salmonella isolates is critical in recognizing outbreaks and new vehicles of infection. Recently, the application of molecular biologic techniques, such as plasmid profile analysis, to epidemiologic studies has provided additional means to investigate outbreaks caused by common serotypes that may otherwise go unrecognized. Better understanding of the reservoirs and routes of transmission of the major serotypes may lead to specific control measures.

References

  1. Ryan CA, Nickels MK, Hargrett-Bean NT, et al. Massive outbreak of antimicrobial resistant salmonellosis traced to pasteurized milk. JAMA 1987;258:3269-74.

  2. Centers for Disease Control. Update: Salmonella enteritidis infections in the northeastern United States. MMWR 1987;36:204-5.

  3. Centers for Disease Control. Shigellosis--United States, 1984. MMWR 1985;34:600-2.

  4. Spika JS, Waterman SH, Soo Hoo GW, et al. Chloramphenicol-resistant Salmonella newport traced through hamburger to dairy farms: a major persisting source of human salmonellosis in California. N Engl J Med 1987;316:565-70.

  5. Pacer RE, Thurmond ML, Ryan CP, Spika JS, Potter ME. Salmonella newport in cattle: an animal and human health problem. In: Proceedings of the Nineteenth Annual Meeting of the US Animal Health Association, 1986:374-80.

  6. St. Louis ME, Morse DL, Potter ME, et al. The emergence of grade A eggs as a major source of Salmonella enteritidis infections: new implications for the control of salmonellosis. JAMA 1988;259:2103-7.

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