Salmonella enteritidis in broiler chickens, United States, 2000-2005.US Department of Agriculture Food Safety and Inspection Service The United States Department of Agriculture's Food Safety and Inspection Service (FSIS) is charged with ensuring that all meat, poultry, and processed egg products in the United States are safe to consume and accurately labeled. (FSIS FSIS Food Safety and Inspection Service FSIS Food Safety Information System (of Malaysia) FSIS Fixed-Size Importance Sampling FSIS Functional Support Information Systems FSIS Fire Support Interface Specification ) data on Salmonella enterica Salmonella enterica is a rod shaped, flagellated, Gram-negative bacterium, and a member of the genus Salmonella.[1] Serovars S. enterica has an extraordinarily large number of serovars serotype serotype /se·ro·type/ (ser´o-tip) the type of a microorganism determined by its constituent antigens; a taxonomic subdivision based thereon. se·ro·type n. See serovar. v. Enteritidis in broiler broiler a young (about 8 weeks old) male or female chicken weighing 3 to 3.5 lb. chicken carcass carcass, carcase 1. the body of an animal killed for meat. The head, the legs below the knees and hocks, the tail, the skin and most of the viscera are removed. The kidneys are left in and in most instances the body is split down the middle through the sternum and the vertebral rinses collected from 2000 through 2005 showed the annual number of isolates increased >4-fold and the proportion of establishments with Salmonella Enteritidis-positive rinses increased nearly 3-fold (test for trend, p<0.0001). The number of states with Salmonella Enteritidis Salmonella en·ter·it·i·dis n. Gärtner's bacillus. in broiler rinses increased from 14 to 24. The predominant phage phage: see bacteriophage. phage - A program that modifies other programs or databases in unauthorised ways; especially one that propagates a virus or Trojan horse. See also worm, mockingbird. The analogy, of course, is with phage viruses in biology. types (PT) were PT 13 and PT 8, 2 strains that a recent Foodborne Diseases Active Surveillance Network (FoodNet) case-control study case-control study, n an investigation employing an epidemiologic approach in which previously existing incidents of a medical condition are used in lieu of gathering new information from a randomized population. associated with eating chicken. FSIS is directing more sampling resources toward plants with marginal Salmonella control to reduce prevalence in products including broilers. The policy targets establishments with common Salmonella serotypes of human illness, including Salmonella Enteritidis. Voluntary interventions should be implemented by industry. ********** During the 1990s, Salmonella enterica serotype Enteritidis briefly surpassed S. Typhimurium as the predominant Salmonella serotype isolated from humans in the United States United States, officially United States of America, republic (2005 est. pop. 295,734,000), 3,539,227 sq mi (9,166,598 sq km), North America. The United States is the world's third largest country in population and the fourth largest country in area. (1). Eggs were frequently implicated im·pli·cate tr.v. im·pli·cat·ed, im·pli·cat·ing, im·pli·cates 1. To involve or connect intimately or incriminatingly: evidence that implicates others in the plot. 2. as the cause of outbreaks of human infection (2,3), and the outbreak strain was often detected in the implicated egg production flock (4). After egg producers implemented quality assurance programs in the late 1990s, human Salmonella Enteritidis infection rates decreased by [approximately equal to] 50% (1). Recently, 2 US case-control studies in Foodborne Diseases Active Surveillance Network (FoodNet) sites identified eating chicken as a risk factor for sporadic human Salmonella Enteritidis infection (5,6), replicating findings of a case-control study performed in England in the late 1980s (7). While the overall incidence of human salmonellosis salmonellosis (săl'mənĕlō`sĭs), any of a group of infectious diseases caused by intestinal bacteria of the genus Salmonella, in FoodNet sites was lower in 2005 than in the mid-1990s, the incidence of Salmonella Enteritidis infections was [approximately equal to] 25% higher (8). We present US Department of Agriculture (USDA USDA, n.pr See United States Department of Agriculture. ) Food Safety and Inspection Service (FSIS) Salmonella testing program data collected from 2000 to 2005 that suggest a need for interventions to prevent the emergence of this Salmonella serotype in broiler chickens in the United States. Methods FSIS Salmonella Testing Program As of January 2000, an FSIS performance standard for Salmonella was set for all establishments that slaughter US broiler chickens (9). Establishments that slaughtered >20,000 chickens per year were eligible for FSIS regulatory Salmonella testing. These establishments accounted for >95% of raw poultry marketed in the United States. The sampling frame for the present study included all eligible FSIS-inspected establishments. Each month, eligible facilities were randomly selected for Salmonella testing to begin in the following month. In each broiler slaughter setting that was tested, 1 broiler chicken carcass rinse (hereafter referred to as broiler rinse) was collected per day for 51 days of operation. The 51 broiler rinses constitute a "Salmonella set." Sets were scheduled approximately once a year. When a plant did not meet the Salmonella performance standard, a follow-up set was scheduled. To limit bias, this report does not include data from follow-up sets. Carcasses were collected after they exited the chiller chill·er n. 1. One that chills. 2. A frightening story, especially one involving violence, evil, or the supernatural; a thriller. chiller Noun 1. , downstream from the slaughter line. The chiller is designed to bring carcass temperatures down to the refrigeration refrigeration, process for drawing heat from substances to lower their temperature, often for purposes of preservation. Refrigeration in its modern, portable form also depends on insulating materials that are thin yet effective. range. The postchill collection site was selected as the sampling site because interventions for pathogen Pathogen Any agent capable of causing disease. The term pathogen is usually restricted to living agents, which include viruses, rickettsia, bacteria, fungi, yeasts, protozoa, helminths, and certain insect larval stages. reduction are generally located before this point. Broiler Rinse Collection Carcasses were collected after they exited the chiller and aseptically placed in a sterile bag. A 400-mL volume of buffered peptone peptone /pep·tone/ (pep´ton) a derived protein, or a mixture of cleavage products produced by partial hydrolysis of native protein.pepton´ic pep·tone n. water was added to the carcass in the bag. Half the volume was poured into the interior cavity and the other half over the skin. The carcass was rinsed with a rocking motion for 1 minute at a rate of [approximately equal to] 35 cycles per minute. After the carcass was removed from the bag, the rinse was poured into a sterile container and shipped on a freezer pack by overnight mail to 1 of 3 FSIS laboratories (Athens, GA; Alameda, CA; St. Louis, MO, USA) for analysis (10). Microbiologic Testing Testing of broiler rinses for Salmonella was performed by using standard FSIS isolation methods (11). Before October 2003, an immunoassay Immunoassay An assay that quantifies antigen or antibody by immunochemical means. The antigen can be a relatively simple substance such as a drug, or a complex one such as a protein or a virus. system (Assurance polyclonal polyclonal /poly·clo·nal/ (-klon´'l) 1. derived from different cells. 2. pertaining to several clones. polyclonal derived from different cells; pertaining to several clones. enzyme immunoassay, BioControl bi·o·con·trol n. See biological control. biocontrol See biological control. Systems, Inc., Bellevue, WA, USA) was used to screen enrichment broths for Salmonella. Beginning in October 2003, Salmonella gene amplification Gene amplification The process by which a cell specifically increases the copy number of a particular gene to a greater extent than it increases the copy number of genes composing the remainder of the genome (all the genes which make up the genetic machinery (BAX System PCR PCR polymerase chain reaction. PCR abbr. polymerase chain reaction Polymerase chain reaction (PCR) Assay, DuPont Qualicon, Wilmington, DE, USA) was performed on lysed cells after overnight incubation in buffered peptone broth (35[degrees]C). Broiler rinses that tested positive on the screening test were cultured for Salmonella with standard methods (i.e., selective enrichment, plating, serologic se·rol·o·gy n. pl. se·rol·o·gies 1. The science that deals with the properties and reactions of serums, especially blood serum. 2. and biochemical confirmation). Three presumptive pre·sump·tive adj. 1. Providing a reasonable basis for belief or acceptance. 2. Founded on probability or presumption. pre·sump Salmonella colonies with the predominant colony form were selected from each plate for biochemical and serologic confirmation. One confirmed Salmonella isolate was sent to the National Veterinary Services Laboratories (NVSL NVSL National Veterinary Services Laboratories (United States Department of Agriculture) NVSL Northern Virginia Swimming League , USDA-APHISVS, Ames, IA, USA) for Salmonella serotyping (12). Beginning in 2001, isolates of Salmonella Enteritidis were phage typed at NVSL (13). Because the predominant Salmonella Enteritidis phage types were clonal (6,14) and pulsed-field gel electrophoresis gel electrophoresis n. Electrophoresis performed in a gel composed of agarose, polyacrylamide, or starch. and antimicrobial antimicrobial /an·ti·mi·cro·bi·al/ (-mi-kro´be-al) 1. killing microorganisms or suppressing their multiplication or growth. 2. an agent with such effects. susceptibility patterns were not available on all isolates during the study period, no further characterization of the isolates was performed for this report. Analysis Analysis was restricted to Salmonella sets performed in calendar years 2000-2005. A [chi square chi square (kī), n a nonparametric statistic used with discrete data in the form of frequency count (nominal data) or percentages or proportions that can be reduced to frequencies. ] test (2-sided) was used to test trends for annual percent of Salmonella Enteritidis isolates among Salmonella-positive broiler rinses and all analyzed broiler rinses, respectively. A [chi square] test for trend was also performed to assess the percent of establishments tested annually with Salmonella Enteritidis-positive broiler rinses, with subanalyses by establishment size. Approximately two thirds of establishments were large ([greater than or equal to] 500 employees), one fourth were small (<500 but [greater than or equal to] 10 employees), and 5% were very small (<10 employees). In addition, a [chi square] test for trend was performed on the number of isolates per Salmonella Enteritidis-positive establishment, by year (SAS (1) (SAS Institute Inc., Cary, NC, www.sas.com) A software company that specializes in data warehousing and decision support software based on the SAS System. Founded in 1976, SAS is one of the world's largest privately held software companies. See SAS System. version 9.1, SAS Institute SAS Institute Inc., headquartered in Cary, North Carolina, USA, has been a major producer of software since it was founded in 1976 by Anthony Barr, James Goodnight, John Sall and Jane Helwig. , Inc., Cary, NC, USA). The number of positive broiler rinses per state was plotted on a US map that showed the geographic density of broiler chicken production by county for the year 2002 (15). Results were plotted for 2 periods: calendar years 2000-2002 and 2003-2005. Phage types of isolates were tabulated by year. The present study preceded a new FSIS policy to control Salmonella. The new policy emphasizes improvement in Salmonella control in product classes that have not reduced Salmonella prevalence in the past decade, such as broilers, and focuses on plants that test positive for common serotypes of human illness, such as Salmonella Enteriditis (16). Results During the 6-year study period, 280 (0.5%) Salmonella Enteritidis isolates were recovered from 51,327 broiler rinses (Table 1). From 2000 to 2005, the proportion of Salmonella isolates that were Salmonella Enteritidis increased (test for trend, p<0.0001). The percentage of all broiler rinses that tested positive also increased (test for trend, p<0.0001). Overall, 90 establishments tested positive from 2000 through 2005. The number of establishments testing positive increased from 17 (9%) of 197 in 2000 to 47 (25%) of 187 in 2005 (test for trend, p<0.0001, Table 2). The increase in the number of positive establishments per year remained significant after stratification by large versus small establishment size. While most establishments with Salmonella Enteritidis--positive broiler rinses were large, in most years, a higher proportion of the small establishments that were tested had positive rinses. During the 6-year study period, the proportion of Salmonella Enteritidis--positive establishments with multiple positive broiler rinses per year also increased significantly (p<0.01, test for trend, Figure 1). In addition, the proportion of establishments with [greater than or equal to] 4 positive broiler rinses per year (of 51 broiler rinse tests per set) increased, beginning in 2002. [FIGURE 1 OMITTED] From 2000 to 2002, Salmonella Enteritidis was isolated from broiler rinses in 14 states, compared with 24 states from 2003 to 2005 (Figure 2). Phage type (PT) 13 was predominant, accounting for half of all isolates, followed by Salmonella Enteritidis PT 8, which accounted for more than one third of isolates (Table 3). In 2005, the number of isolates that were PT 8 increased >3-fold compared with 2004. [FIGURE 2 OMITTED] Discussion The principal finding of this study was a significant increase in the number of broiler chicken slaughter establishments with Salmonella Enteritidis--positive broiler rinses in the years from 2000 through 2005. The 90 slaughter establishments with positive rinses were dispersed across 24 states, reflecting the geographic distribution of the US broiler industry. During the study period, increases were seen in the proportion of both large and small establishments that had such positive broiler rinses. Some caution is warranted when interpreting our findings. The purpose of the FSIS Salmonella program is to assess performance of individual establishments. The program is not designed to estimate national prevalence of poultry contamination because it does not fully account for production volume or regional or seasonal effects. Furthermore, samples are collected after slaughter processes that are intended to reduce carcass contamination. Nonetheless, the apparent emergence of Salmonella Enteritidis in broilers is noteworthy given the increase in human Salmonella Enteritidis infection rates in the United States (8) and recent findings that eating chicken is a new and important risk factor for sporadic infection (5,6). Additional epidemiologic studies epidemiologic study A study that compares 2 groups of people who are alike except for one factor, such as exposure to a chemical or the presence of a health effect; the investigators try to determine if any factor is associated with the health effect are recommended to further elucidate e·lu·ci·date v. e·lu·ci·dat·ed, e·lu·ci·dat·ing, e·lu·ci·dates v.tr. To make clear or plain, especially by explanation; clarify. v.intr. To give an explanation that serves to clarify. the role of contaminated contaminated, v 1. made radioactive by the addition of small quantities of radioactive material. 2. made contaminated by adding infective or radiographic materials. 3. an infective surface or object. chicken in human Salmonella Enteritidis infections and estimate the extent of illness attributable to chicken. Retail food surveillance and laboratory subtyping studies (6) may also be valuable because they enable comparisons of human and poultry strains. In this report, 2 Salmonella Enteritidis phage types, PT 8 and PT 13, accounted for most isolates from broiler rinses. In a recent FoodNet study, the association between Salmonella Enteritidis infection and eating chicken strengthened in analyses restricted to patients infected with these 2 phage types (6). The possible emergence of these phage types in broiler chickens suggests that industry should implement appropriate Salmonella Enteritidis controls for broiler chickens (17,18). The present study preceded a new FSIS policy to control Salmonella in broilers that emphasizes common serotypes of human illness (16). As part of this effort, FSIS held 2 public meetings on Salmonella in broilers: 1 in Athens, Georgia Athens-Clarke County is a unified city-county in Georgia, U.S., in the northeastern part of the state, at the eastern terminus of Georgia 316. The University of Georgia is located in this college town and is responsible for the initial creation of Athens and its subsequent growth. , in August 2005 on controls before slaughter (preharvest), and another in Atlanta, Georgia, in February 2006 on controls in the slaughter plant (postharvest). Information from these meeting was used to prepare guidelines to help broiler plants control salmonellae (19). The agency is also monitoring progress of meat and poultry plants in controlling this organism. If, in July 2007, most plants (e.g., 90%) that manufacture a specific product (e.g., broiler carcasses) have not reduced the percentage of Salmonella tests that are positive to at least half the FSIS performance standard, the agency will consider actions to improve control of salmonellae. One option that FSIS is considering is to post Salmonella results on the web for product classes that have not made sufficient progress, listing data by plant name. In the 1990s, successful voluntary quality assurance programs to control Salmonella Enteritidis were developed by the egg industry and state poultry health officials (20). Many of the interventions are adaptable to the control of this organism in broilers. For example, control points for the organism in broilers are likely to include monitoring and sanitation of breeding flocks, hatcheries, broiler flocks, and slaughter establishments. Serotype data that FSIS provides to plants on each isolate as part of its new Salmonella policy (16) may also assist plant officials to make informed SE risk management decisions. Acknowledgments We thank the FSIS headquarters, inspection, and laboratory personnel and APHIS laboratory personnel who made the report possible. References (1.) Patrick ME, Adcock PM, Gomez TM, Altekruse SF, Holland BH, Tauxe RV, et al. Salmonella Enteritidis infections, United States, 1985-1999. Emerg Infect Dis. 2004;10:1-7. (2.) St Louis ME, Morse DL, Potter ME, DeMelfi TM, Guzewich JJ, Tauxe RV, et al. The emergence of grade A eggs as a major source of Salmonella Enteritidis infections. New implications for the control of salmonellosis. JAMA JAMA abbr. Journal of the American Medical Association . 1988;259:2103-7. (3.) Trepka MJ, Archer JR, Altekruse SF, Proctor ME, Davis JP. An increase in sporadic and outbreak- associated Salmonella Enteritidis infections in Wisconsin: the role of eggs. J Infect Dis. 1999; 180:1214-9. (4.) Altekruse S, Koehler J, Hickman-Brenner F, Tauxe RV, Ferris K. A comparison of Salmonella Enteritidis phage types from egg-associated outbreaks and implicated laying flocks. Epidemiol Infect. 1993;110:17-22. (5.) Kimura AC, Reddy V, Marcus R, Cieslak PR, Mohle-Boetani JC, Kassenborg HD, et al. Chicken consumption is a newly identified risk factor for sporadic Salmonella enterica serotype Enteritidis infections in the United States: a case-control study in FoodNet sites. Clin Infect Dis. 2004;38(Suppl 3):S244-52. (6.) Marcus R, Varma JK, Medus C, Boothe EJ, Anderson BJ, Crume T, et al. Re-assessment of risk factors for sporadic Salmonella serotype Enteritidis infections: a case-control study in five FoodNet sites, 2002 2003. Epidemiol Infect. 2006;7:1-9. (7.) Cowden JM, Lynch D, Joseph CA, O'Mahony M, Mawer SL, Rowe B, et al. Case-control study of infections with Sahnonella Enteritidis phage type 4 in England. BMJ BMJ n abbr (= British Medical Journal) → vom BMA herausgegebene Zeitschrift . 1989;299:771-3. (8.) Centers for Disease Control and Prevention Centers for Disease Control and Prevention (CDC), agency of the U.S. Public Health Service since 1973, with headquarters in Atlanta; it was established in 1946 as the Communicable Disease Center. . Preliminary FoodNet data on the incidence of infection with pathogens transmitted commonly through food--10 states, United States, 2005. MMWR MMWR Morbidity & Mortality Weekly Report Epidemiology A news bulletin published by the CDC, which provides epidemiologic data–eg, statistics on the incidence of AIDS, rabies, rubella, STDs and other communicable diseases, causes of mortality–eg, Morb Mortal Wkly Rep. 2006;55:392-5. (9.) Food Safety and Inspection Service. Pathogen reduction; hazard analysis A hazard analysis is a process used to characterize the elements of risk. The results of a hazard analysis is the identification of unacceptable risks and the selection of means of controlling or eliminating them. and critical control point (HACCP HACCP hazard analysis critical control points. ) systems; Final Rule. Fed Regist. 1996;61:38805-55 [cited 2006 Oct 11]. Available from http://www.fsis.usda.gov/OPPDE/rdad/FRPubs/93-016F.htm (10.) Food Safety and Inspection Service. FSIS directive 10,230.5: Self-instruction guide for collecting raw meat and poultry product samples for Salmonella analysis. February 4, 1998. [cited 2006 Oct 11]. Available from http://www.fsis.usda.gov/OPPDE/rdad/FSIS Directives/10230-5.pdf (11.) Food Safety and Inspection Service. Microbiology laboratory guidebook. August 17, 2006 [cited 2006 Oct 11]. Available from http://www.fsis.usda.gov/Science/Microbiological_Lab_Guidebook (12.) Ewing E, editor. Edwards and Ewing's identification of Enterobacteriaceae. 5th ed. London: Elsevier; 1986. (13.) Ward LR, de Sa JD, Rowe B. A phage-typing scheme for Salmonella Enteritidis. Epidemiol Infect. 1987;99:29l-4. (14.) Laconcha I, Baggesen DL, Rementeria A, Garaizar J. Genotypic genotypic emanating from or pertaining to genotype. genotypic selection selection of breeding stock on the basis of known inherited characteristics. characterisation by PFGE PFGE Pulsed-Field Gel Electrophoresis of Salmonella enterica serotype Enteritidis phage types 1, 4, 6, and 8 isolated from animal and human sources in three European countries. Vet Microbiol. 2000;75:155-65. (15.) USDA National Agricultural Statistics Service. Number of broilers and other meat-type chickens sold: 2002 [cited 2006 Oct 11]. Available from http://www.nass.usda.gov/research/atlas02/ Livestock/Poultry/Number%20of%20Broilers%20and%20Other%20 Meat-Type%20Chickens%20Sold.gif (16.) Food Safety and Inspection Service. Salmonella verification sample result reporting: agency policy and use in public health protection. Fed Regist. 2006;71:9772-7. (17.) Gast RK, Holt PS. Experimental horizontal transmission horizontal transmission n. Transmission of infection by contact. horizontal transmission Epidemiology The transmission of an infection from one to another person of the same generation in the same population. of Salmonella Enteritidis strains (phage types 4, 8, and 13a) in chicks. Avian avian /avi·an/ (a´ve-an) of or pertaining to birds. a·vi·an adj. Of, relating to, or characteristic of birds. Dis. 1999;43:774-8. (18.) McIlroy SG, McCracken RM, Neill SD, O'Brien JJ. Control, prevention and eradication of Salmonella Enteritidis infection in broiler and broiler breeder breeder 1. a person with an animal enterprise involving the multiplication of the herd, flock or group. 2. a female animal used basically for the production of saleable young. flocks. Vet Rec. 1989;125:545-8. (19.) Food Safety and inspection Service. Compliance guideline for controlling Salmonella in poultry. 1st ed. August 2006 [cited 2006 Oct 11]. Available from http://www.fsis.usda.gov/PDF/Compliance_ Guideline_Controllin_Salmonella_Poultry.pdf#search=%22Compli ance%20guideline%20for%20controlling%20Salmonella%20in%20 poultry%22 (20.) Mumma GA, Griffin PM, Meltzer MI, Braden CR, Tauxe RV. Egg quality assurance programs and egg-associated Salmonella Enteritidis infections, United States. Emerg Infect Dis. 2004; 10:1782-9. Dr Altekruse is a veterinary epidemiologist in the Public Health Service assigned to the USDA Food Safety and Inspection Service. His research interests include characterization of Salmonella isolates from meat and poultry and reductions in indicator and pathogen counts during slaughter. Sean F. Altekruse,* Nathan Bauer, ([dagger]) Amy Chanlongbutra,* Robert DeSagun,* Alecia Naugle,* Wayne Schlosser, ([dagger]) Robert Umholtz,* and Patricia White ([double dagger double dagger n. A reference mark (  ) used in printing and writing. Also called diesis.Noun 1. ]) * US Department of Agriculture Food Safety and Inspection Service, Washington, DC, USA; ([dagger]) US Department of Agriculture Food Safety and Inspection Service, College Station, Texas College Station is a city in Brazos County, Texas, situated in Central Texas. It is located in the heart of the Brazos Valley. The city is located within the most populated region of Texas, near to three of the 10 largest cities in the United States - Houston, Dallas, and San , USA; and ([double dagger]) US Department of Agriculture Food Safety and Inspection Service, Omaha, Nebraska “Omaha” redirects here. For other uses, see Omaha (disambiguation). Omaha is the largest city in the State of Nebraska, United States. It is the county seat of Douglas County.GR6 As of the 2000 census, the city had a population of 390,007. , USA Address for correspondence: Sean F. Altekruse, USDA Food Safety and Inspection Service, Office of Policy, Program, and Employee Development, 300 12th St SW, Rm 412, Washington, DC 20250, USA; email: sean.altekruse@fsis.usda.gov
Table 1. Salmonella Enteritidis (SE) isolates per year as a
proportion of Salmonella-positive broiler rinses and total broiler
rinses, 2000-2005
No. SE Salmonella-positive SE as a proportion of
Year isolates rinses all salmonellae (%)*
2000 23 914 2.5
2001 17 1,065 1.6
2002 33 1,059 3.1
2003 29 828 3.5
2004 58 957 6.1
2005 120 1,559 7.7
Total 280 6,382 4.4
No. rinses SE-positive rinse as a
Year tested proportion of all rinses *
2000 10,057 0.2
2001 8,955 0.2
2002 9,183 0.4
2003 6,468 0.5
2004 7,072 0.8
2005 9,592 1.3
Total 51,327 0.5
* Test for trend, p < 0.0001; SE isolates as a proportion of
Salmonella isolates and all broiler rinses by year.
Table 2. Establishments with Salmonella Enteritidis (SE)--positive
broiler rinses, by establishment size, * 2000-2005
All * Large ([dagger])
Year No. tested SE positive (%) No. tested SE positive (%)
2000 197 17 (9) 128 9 (7)
2001 186 15 (8) 111 10 (9)
2002 185 22 (12) 123 17 (14)
2003 143 25 (17) 103 17 (14)
2004 160 25 (16) ill 16 (14)
2005 187 47 (25) 126 32 (25)
Small ([double dagger])
Year No. tested SE positive (%)
2000 60 8 (13)
2001 61 5 (8)
2002 53 5 (9)
2003 37 8 (22)
2004 43 9 (21)
2005 48 15 (31)
* Establishment size: large [greater than or equal to] 500, small
[greater than or equal to] 10 to <500; very small <10 employees.
(SE was not isolated in the 54 sets from very small establishments.)
Ninety establishments had SE-positive broiler rinses; 63 (70%) were
large and 27 (30%) were small.
([dagger]) Test for trend, p < 0.0001.
([double dagger]) Test for trend, p < 0.01.
Table 3. Salmonella Enteritidis (SE) phage types from broiler rinses,
2001-2005 *
Phage type
Year SE isolates no. PT 13 no. (%) PT 8 no. (%)
2001 17 11 (65) 4 (24)
2002 33 12 (36) 8 (24)
2003 29 13 (45) 14 (48)
2004 58 37 (64) 15 (26)
2005 120 56 (47) 50 (42)
Total 257 129 (50) 91 (35)
Phage type
Year Other ([dagger]) No data ([double
no. (%) dagger]) no. (%)
2001 1 (6) 1 (6)
2002 5 (15) 8 (24)
2003 1 (3) 1 (3)
2004 4 (7) 2 (3)
2005 9 (8) 5 (4)
Total 20 (8) 17 (7)
* Phage type (PT) data were not available for 2000. Row percents do
not sum to 100 because of rounding.
([dagger]) Other phage types: 13a (7); PT 23 (7), PT 28 (3); PT 2 (2);
PT 14B (1).
* No phage type data were available for 17 isolates.
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