Public Health Agency of Canada
www.publichealth.gc.ca
C-EnterNet 2007 Annual Report
National Integrated Enteric Pathogen Surveillance Program
4. Salmonella
4.1 Human Cases
In 2007, in Sentinel Site 1, a total of 130 cases of salmonellosis were reported (26.2/100,000 person-years). Of these 130 cases, 25% (33) were travel-related, 0.8% (1) were outbreak-related and 74% (96) were classified as endemic (19.3/100,000 person-years). In comparison, the annual incidence rates for salmonellosis in 2006 in Canada and Ontario were 14.9/100,000 and 16.1/100,000, respectively.5
The age, gender and seasonal distributions fit patterns that have been historically observed for Salmonella (Figures 4.1 and 4.2).
FIGURE 4.1: Incidence rates of endemic salmonellosis cases by gender and age group in Sentinel Site 1 in 2007
There were 27 different serotypes detected among the 96 endemic cases, for which the serotype was known. The top three serotypes, Typhimurium (36), Enteritidis (18), and Heidelberg (5), encompassed 62% of isolates that were serotyped (Table 4.1). Comparison of travel versus endemic Salmonella cases indicated that Typhimurium (36/39), Heidelberg (5/5), and Newport (2/2) serotypes were primarily of domestic origin, while over one third of the Enteriditis (10/28) cases were travel-related.
Potential exposure information for the three days prior to onset of illness was collected for 90% (86/96) of the reported endemic Salmonella infections (Appendix B). Few meaningful risk factors were identified from the case-case comparison; however, household pet exposure did appear to be a risk factor for Salmonella cases.
4.2 Exposure Surveillance
Retail
Salmonella was commonly detected on raw skin-on chicken breasts but rarely found on raw pork chops and ground beef (Table 4.1). Only low levels of Salmonella were detected on the positive retail samples (Appendix C).
The three most frequent serotypes found on chicken meat included: Kentucky, Heidelberg and Hadar (Table 4.1). The top two serotypes found on pork chops were Typhimurium and Give, while the single beef isolate was Enteritidis PT13.
On-Farm
The prevalence of Salmonella in pooled manure samples from swine, beef and dairy farms in 2007 was 33%, 10%, and 13%, respectively (Table 4.1). Broiler chicken farm sampling was initiated late in the year (October). During the three months of sampling on broiler chicken farms, Salmonella was detected in 72% of the samples. Hadar (6), Heidelberg (5) and Kentucky (5) were the most common serotypes isolated on broiler chicken farms. On swine farms, Typhimurium (15) and Agona (7) were the most frequently isolated Salmonella serotypes (Table 4.1). The most frequently isolated Salmonella serotypes from dairy operations were Kentucky (6) and Typhimurium (3). On beef farms, Typhimurium (2), Kentucky (2) and Uganda (2) were the most frequently isolated Salmonella serotypes.
Water
The prevalence of Salmonella contamination in untreated surface water samples was lower for the culture-based method (10%) than the molecular method (35%) (Table 4.1). Of the 13 isolates cultured, Salmonella Thompson was the most frequently detected serotype. Salmonella was most frequently detected at sample site E (close to a waste water treatment effluent point on the Grand River) by both culture and molecular methods.
TABLE 4.1: Salmonella detection and serotyping data from the integrated surveillance activities in Sentinel Site 1 in 2007
| Human | Retail Food | Food Animals (Manure) | Untreated Surface Water | |||||||
|---|---|---|---|---|---|---|---|---|---|---|
| Endemic Cases | Pork | Chicken | Beef | Swine | Broiler Chickens | Beef Cattle | Dairy Cattle | Grand River | ||
| Pork chop | Skin-on breast | Ground beef | 5 sample points on Grand River | |||||||
| Detection | Culture | Molecular | ||||||||
| # tested | Unknown | 187 a | 187 a | 187 a | 120 a | 36 a | 80 a | 112 a | 134 a | 129 b |
| # positive | 96 a | 6 | 61 | 1 | 40 | 26 | 8 | 14 | 13 | 45 |
| % positive | 3% | 33% | 1% | 33% | 72% | 10% | 13% | 10% | 35% | |
| Subtyping # subtyped |
95 | 6 | 61 | 1 | 40 | 26 | 8 | 14 | 13 | |
| Adelaide | 2 | |||||||||
| Agona | 2 | 7 | 1 | |||||||
| Berta | 1 | 1 | 1 (E) | |||||||
| Bovismorbificans | 1 | 1 | ||||||||
| Brandenburg | 1 | 1 (C) | ||||||||
| Branderup | 3 | |||||||||
| Cerro | 2 | |||||||||
| Derby | 2 | |||||||||
| Enteritidis | 6 | |||||||||
| Enteritidis PT 13 | 2 | 2 | 1 | 1 | 2 | |||||
| Enteritidis PT4 | 1 | |||||||||
| Enteritidis PT6 | 1 | |||||||||
| Enteritidis PT6a | 1 | |||||||||
| Enteritidis PT8 | 4 | 1 | 1 | |||||||
| Enteritidis PT8a | 1 | |||||||||
| Enteritidis PT21 | 1 | |||||||||
| Enteritidis PT911 | 1 | |||||||||
| Enteritidis Atypical | 1 | |||||||||
| Give | 2 | 1 | ||||||||
| Group B | 2 | |||||||||
| Hadar | 1 | 5 | 2 | 6 | ||||||
| Hartford | 2 | |||||||||
| Heidelberg | 5 | 16 | 5 | |||||||
| I:4,5,12:b:- | 1 | 2 (B, E) | ||||||||
| I:4,12:i:- | 2 | |||||||||
| I:ROUGH-O:-:- | 1 | 2 | ||||||||
| Infantis | 3 | 1 | 1 | 1 | ||||||
| Javiana | 2 | |||||||||
| Kentucky | 1 | 28 | 5 | 2 | 6 | 1 (D) | ||||
| London | 1 | 1 | ||||||||
| Mbandaka | 1 | 1 | ||||||||
| Newport | 2 | |||||||||
| Ohio | 1 | 1 | ||||||||
| Oranienberg | 2 | |||||||||
| Schwarzengrund | 1 | 1 | ||||||||
| Thompson | 4 | 1 | 3 | 2 (B) | ||||||
| Typhimurium | 11 | 1 (A) | ||||||||
| Typhimurium DT104c | 2 | 4 | 1 | 2 | ||||||
| Typhimurium DT104ac | 1 | |||||||||
| Typhimurium 3 | 3 | |||||||||
| Typhimurium 12 | 1 | |||||||||
| Typhimurium 21 | 1 | |||||||||
| Typhimurium 28c | 2 | 1 | 1 | |||||||
| Typhimurium 41c | 1 | |||||||||
| Typhimurium 46 | 1 | |||||||||
| Typhimurium 82 | 2 | |||||||||
| Typhimurium 97 | 2 | |||||||||
| Typhimurium U285 | 1 | |||||||||
| Typhimurium U302c | 1 | 2 | ||||||||
| Typhimurium U310 | 1 | |||||||||
| Typhimurium UT1c | 1 | |||||||||
| Typhimurium 108 | 9 | 1 | ||||||||
| Typhimurium 110c | 1 | |||||||||
| Typhimurium 120 | 1 | |||||||||
| Typhimurium 151c | 1 | |||||||||
| Typhimurium 194c | 2 | |||||||||
| Typhimurium 208c | 2 | |||||||||
| Typhimurium Untypable c | 1 | |||||||||
| Typhimurium Atypical | 1 | |||||||||
| Uganda | 1 | 2 | ||||||||
| Worthington | 2 | |||||||||
| Other d | 6 | 3 | 2 | 5 | ||||||
| Serotype ranking within each component |
|
|---|---|
| most frequent serotype | |
| second most frequent serotype | |
| third most frequent serotype | |
aCulture method. bMolecular method. cIncludes var5-. dSerotypes that were identified once in a single component are listed below and are NOT listed in TABLE 4.1:
Human: Anatum, Choleraesuis, I:4,5,12-,I:4,5,12.6-, Java, Virchow. Chicken meat: Indiana, Kiambu, Tumodi. Swine operations: I:6,7,14:r.-, Krefeld. Untreated water: Alachua (C), I:6,7:-;enz15 6,7:-215 (E): I:ROUGH-O:z10:enz15 -:z10:z15 (E);!:10:-:1,5 10:-:5(E), Kiambu (E).
Water Sampling Locations in Grand River Watershed: A- Canagagigue Creek. B- Conestogo River. C- Upper Grand River. D-Grand River, near drinking water intake. E- Grand River, near one wastewater treatment plant effluent point.
TABLE 4.2: PFGE results for the most common Salmonella serotypes for all components, including human travel-related cases in Sentinel Site 1 in 2007 (values in brackets refer to 2006 and 2005 data for comparisons)
| Non-travel Cases a | Travel-related Cases | Pork | Chicken | Beef | Swine | Broiler Chickens | Beef Cattle | Dairy Cattle | Grand River | |
|---|---|---|---|---|---|---|---|---|---|---|
| Pork chop | Skin-on breast | Ground beef | 5 sample points on Grand River | |||||||
| Typhimurium | ||||||||||
| # samples with PFGE result | 24 (15) | 1 | 2 (1) | 3 (4) | 0 | 16 (32) | 0 | 2 | 3 (2) | 1 (4) |
| STXAI.0001 | 2 (2) | (1) | 4 (7) | 2 | 3 (1) | (1) | ||||
| STXAI.0006 | 1 | |||||||||
| STXAI.0013 | (1) | |||||||||
| STXAI.0027 | (1) | (1) | 3 (13) | |||||||
| STXAI.0029 | (4) | |||||||||
| STXAI.0044 | (1) | |||||||||
| STXAI.0067 | 4 | |||||||||
| STXAI.0098 | (1) | (1) | ||||||||
| STXAI.0193 | 3 | |||||||||
| STXAI.0195 | (1) | (2) | ||||||||
| STXAI.0203 | (1) | |||||||||
| STXAI.0214 | 1 (1) | |||||||||
| STXAI.0233 | (2) | |||||||||
| STXAI.0239 | (1) | |||||||||
| STXAI.0243 | 1 | 1 | ||||||||
| STXAI.0269 | (1) | |||||||||
| STXAI.0270 | (1) | |||||||||
| STXAI.0286 | 1 | (1) | ||||||||
| STXAI.0312 | 8 (3) | 2 (2) | ||||||||
| STXAI.0314 | 1 | |||||||||
| STXAI.0339 | (1) | |||||||||
| STXAI.0349 | (1) | |||||||||
| STXAI.0361 | (1) | (1) | (1) | |||||||
| STXAI.0362 | (1) | |||||||||
| STXAI.0364 | 3 (1) | |||||||||
| STXAI.0376 | 1 | |||||||||
| STXAI.0406 | 1 | |||||||||
| STXAI.0425 | 1 | 1 | ||||||||
| STXAI.0434 | 2 | |||||||||
| STXAI.0436 | 1 | |||||||||
| STXAI.0440 | 1 | |||||||||
| STXAI.0441 | 1 | |||||||||
| STXAI.0444 | 1 | |||||||||
| STXAI.0452 | 1 | |||||||||
| STXAI.0479 | 1 | |||||||||
| Enteritidis | ||||||||||
| # samples with PFGE result | 12 (14) | 6 (19) | 0 | 3 (5) | 1 | 1 | 4 | 0 | 0 | 0 |
| SENXAI.0001 | 2 | 3 (14) | ||||||||
| SENXAI.0002 | (1) | (1) | ||||||||
| SENXAI.0003 | 4 (2) | 1 | 2 | |||||||
| SENXAI.0004 | 2 | 1 (1) | ||||||||
| SENXAI.0008 | 2 | |||||||||
| SENXAI.0009 | 1 | |||||||||
| SENXAI.0038 | 3 (11) | 2 (5) | 1 | 1 | 2 | |||||
| SENXAI.0079 | (1) | |||||||||
| SENXAI.0093 | (1) | |||||||||
| SENXAI.0123 | (1) | |||||||||
| Heidelberg | ||||||||||
| # samples with PFGE result | 3 (5) | 0 | 0 | 16 (11) | 0 | 0 | 5 | 0 | 0 | 0 (2) |
| SHEXAI.0001 | 1 | 8 (4) | 5 | (1) | ||||||
| SHEXAI.0006 | (1) | (5) | (1) | |||||||
| SHEXAI.0009 | (4) | |||||||||
| SHEXAI.0011 | 2 | 2 (1) | ||||||||
| SHEXAI.0015 | (1) | |||||||||
| SHEXAI.0020 | 4 | |||||||||
| SHEXAI.0187 | 1 | |||||||||
| SHEXAI.0194 | 1 | |||||||||
| Kentucky | ||||||||||
| # samples with PFGE result | 1 | 1 | 0 (1) | 28 (26) | 0 | 0 | 5 | 2 | 6 (12) | 1 (5) |
| KenXAI.0005 | 1 | 7 (9) | 2 | |||||||
| KenXAI.0012 | 2 (3) | |||||||||
| KenXAI.0013 | 15 (12) | 3 | ||||||||
| KenXAI.0016 | (1) | 2 | 6 (11) | 1 (5) | ||||||
| KenXAI.0023 | (1) | |||||||||
| KenXAI.0024 | (1) | |||||||||
| KenXAI.0025 | (1) | |||||||||
| KenXAI.0029 | 2 | |||||||||
| KenXAI.0030 | ||||||||||
| KenXAI.0032 | 1 | |||||||||
| KenXAI.0033 | 1 | |||||||||
| KenXAI.0034 | 1 | |||||||||
| Thompson | ||||||||||
| # samples with PFGE result | 3 (1) | 2 (1) | 0 (2) | 1 | 0 | 0 | 3 | 0 | 0 (1) | 2 (6) |
| STHXAI.0001 | 3 | (1) | (2) | |||||||
| STHXAI.0002 | 1 | 1 | 1 (1) | |||||||
| STHXAI.0011 | (1) | |||||||||
| STHXAI.0046 | 1 | 1 | (3) | |||||||
| STHXAI.0056 | 1 | |||||||||
| STHXAI.0060 | (1) | |||||||||
| STHXAI.0062 | (2) | |||||||||
aNon-travel includes endemic and outbreak cases.
The PFGE patterns of Salmonella isolated by C-EnterNet during 2007 were compared to the PulseNet Canada National Databases, which contain clinical isolates uploaded by provincial public health labs between 2000 and 2008 during routine laboratory-based surveillance6. The C-EnterNet PFGE results described below refer to isolates from 2007 only. For comparison purposes, we have included PFGE results for isolates from 2005 and 2006, in parentheses, in Table 4.2.
The most frequently occurring PFGE patterns of Salmonella Typhimurium, Enteritidis, Heidelberg, Thompson, and Kentucky among human clinical isolates in the PulseNet Canada database were represented in C-EnterNet isolates.
There were 52 Typhimurium isolates with PFGE results representing 22 distinct patterns collected by C-EnterNet in 2007. Three of the PFGE patterns (STXAI.0001, STXAI.0243, STXAI.0312) were isolated from more than one source in 2007. Two represent the most common patterns in the PulseNet Canada database (STXAI.0001, STXAI.0312); however, pattern STXAI.0243 (isolate from a human case and from untreated surface water) is an uncommon pattern for Typhimurium (Table 4.2). The PFGE patterns STXAI.0027 and STXAI.0001 were most commonly identified in non-human sources and both were also found in human cases. Most of these were from pooled swine manure samples.
The 27 isolates of Enteritidis from C-EnterNet in 2007 comprised 6 distinct PFGE patterns, a lower diversity compared to Typhimurium and consistent with the overall diversity of PFGE patterns for Enteritidis in the PulseNet Canada database. Three patterns of Enteritidis were isolated from more than one category. The 12 endemic S. Enteritidis cases had 5 PFGE patterns, whereas the six travel-related ones were distributed among three patterns, two being identical to patterns identified in endemic cases (SENXAI.0001 and SENXAI.0004) (Table 4.2). The nine non-human isolates were distributed among two patterns, SENXAI.0003 and SENXAI.00038, which were also seen in endemic cases but not travel-related cases. The PFGE patterns SENXAI.0001, SENXAI.0038, SENXAI.0003, SENXAI.0008, found among C-EnterNet samples, represent the vast majority of Enteritidis isolates in PulseNet Canada.
Of the 24 isolates of S. Heidelberg that were isolated by C-EnterNet and characterized by PFGE in 2007; 5 distinct patterns were found. The PFGE pattern SHEXAI.0001, which was recovered in C-EnterNet retail chicken, broiler chicken manure, and from a human case, is the most frequently occurring PFGE pattern for Heidelberg in the PulseNet Canada database (over 40% of all cases). Similarly, SHEXAI.0011 was also recovered from both C-EnterNet retail chicken and from human cases; this pattern is the second most frequently occurring Heidelberg pattern in PulseNet Canada. Chicken retail isolates were distributed among four other patterns not seen in any other components.
Seven of the S. Kentucky patterns were detected in the 28 retail chicken isolates, and two were predominant (KenXAI.0013 and KenXAI.0005). These two patterns were also detected in broiler chicken manure. KenXAI.0005 was the only S. Kentucky pattern isolated from an endemic case. KenXAI.0016 was detected on dairy cattle farms, beef farms and in untreated surface water samples. PFGE patterns from the few S. Thompson isolates in Sentinel Site 1 in 2007 were not specific to any particular pattern, but scattered across various ones (Table 4.2). The majority of C-EnterNet S. Kentucky and S. Thompson samples comprised the most frequently occurring PFGE patterns in the PulseNet Canada database.
Generally, when looking at these five Salmonella serotypes, PFGE patterns associated with travel-related cases were rarely found in the sources tested (1/6) whereas patterns associated with endemic cases were more frequently found in the sources tested (9/22). Also, about half of the PFGE patterns associated with travel-related cases were also associated with endemic cases.
4.3 Seasonal Trends in Exposure Sources
There are no obvious seasonal trends in the Salmonella exposure sources evaluated in Sentinel Site 1 (Figure 4.2). Among human cases, there appears to be a seasonal increase in summer months, which matches trends observed in 2006.
FIGURE 4.2: Temporal distribution of Salmonella detected in human endemic cases, untreated surface water and retail meat samples in Sentinel Site 1 in 2007
4.4 Summary of Salmonella Results
- Typhimurium was the most commonly detected Salmonella serotype in human cases and on swine and beef farms, and the second most commonly detected serotype on dairy farms in Sentinel Site 1.
- Salmonella Enteritidis was the second most commonly detected serotype in human cases and the third most commonly detected serotype in broiler chicken manure. The only retail ground beef isolate identified was S. Enteritidis. A third of the Salmonella Enteritidis cases were travel-related.
- In Sentinel Site 1, the prevalence of S. Enteritidis phagetype 13 has decreased in 2007 from 2006 in human cases and retail chicken meat. However, it was detected in retail ground beef and on swine and broiler chicken farms in 2007. This pattern was identified whether you consider the phagetype (PT13) or the PFGE pattern (SENXAI.0038).
- Salmonella Heidelberg was the third most commonly detected serotype in human cases and the second most commonly detected serotype in retail chicken meat and on broiler chicken farms (tied for second with S. Kentucky). PFGE patterns identified in human cases this year (SHEXAI.0001 and SHEXAI.0011) are the most frequently occuring Heidelberg patterns in PulseNet Canada. These patterns were detected in retail chicken meat and SHEXAI.0001 was also found on broiler chicken farms in 2007.
- The most common serotype detected on broiler chicken farms was S. Hadar. All five S. Hadar isolates recovered from retail chicken had the same PFGE pattern (SHAXAI.0001). This PFGE pattern was also found on one swine and one broiler chicken farm in Sentinel Site 1. This PFGE pattern was not found in any of the human cases in Sentinel Site 1, but is a common pattern identified in human cases across Canada.
- Salmonella Kentucky was the most commonly detected serotype on retail chicken meat, manure from dairy cattle, and beef farms, and tied for second on manure from broiler chicken farms with S. Heidelberg. It was isolated in one endemic and one travel-related human case. The single endemic human case isolate (PFGE pattern KENXAI.0005) matched isolates recovered from retail chicken meat and broiler chicken farms in Sentinel Site 1.
5 National Notifiable Disease representative (Carole Scott) 2007 [personal communication]. Note: 2006 numbers contain travel and endemic cases and are preliminary and subject to change.
6 PulseNet Canada, National Microbiology Laboratory, Public Health Agency of Canada (Celine Nadon) 2008 [personal communication].
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