**3.2** *Salmonella* **from meats**

226 Salmonella – A Dangerous Foodborne Pathogen

analog – florfenicol, most sulphonamides, and penicillin, and susceptible to 7 antimicrobials including the cephalosporin – ceftiofur, the quinolone – enrofloxacin some aminoglycosides, and ampicillin (Table 5). *Salmonella* Worthington was resistant to 14 of 20 antimicrobials (70% resistance), including macrolides (erythromycin, tilmicosin, tylosin), tetracyclines (chlortetracycline, oxytetracycline), chloramphenicol analog – florfenicol, some sulphonamides, and penicillins (penicillin and ampicillin), and susceptible to 6 antimicrobials including the cephalosporin – ceftiofur, the quinolone - enrofloxacin and some aminoglycosides (Table 5). Except for ampicillin, both *Salmonella* isolates were resistant to similar antimicrobials (Table 5). None of the *Salmonella* isolates were resistant to

**Antibiotics 18S 24S 53S** 

S S S R

S R R R

S

S

R

R

S R

R R

R R R

R

Table 5. Antibiotic sensitivity and resistance of *Salmonella* isolates from a bison herd

*Salmonella* **Isolates** 

S S S S

S S S I

S

S

R

R

R R

S S

R R R

R

S S S R

S R R R

S

S

R

R

R R

R R

R R R

R

clinically important antimicrobials.

 Sulphadimethoxime Sulphachloropyridazine

**Quinolones/Fluoroquinolones** 

 Sulphathiazole **Cephalosporins**  Ceftiofur

 Enrofloxacin **Pleuromutilins**  Tiamulin

 Ampicillin Penicillin **Tetracyclines** 

**Penicillins** 

**Macrolides** 

**Misc.** 

**Chloramphenicol Analog**  Florfenicol

 Chlortetracycline Oxytetracycline

 Erythromycin Tilmicosin

Clindamycin

Tylosin (Tartrate/Base)

R = Resistant S = Susceptible I-Intermediate

**Sulphanamides/Potentiated Sulphonamides**  Trimethoprim/Sulphamethoxazole

**Aminoglycosides**  Apramycin Gentamycin Neomycin Spectinomycin In the Khaitsa et al (2007b) study, 2.4% (23/959) of the samples were contaminated with *Salmonella*; with 5% (16/329), and 1% (7/607) of the raw and ready to eat meat samples testing positive for *Salmonella*, respectively. There was a significant difference in recovery of *Salmonella* (*P* < 0.05), between meat type (raw vs RTE; OR =4.2, 95% CI = 1.6, 10.8); and sampling time (OR = 0.4, 95% CI = 0.2, 0.7). Retail store and product brand did not affect *Salmonella* recovery. The twenty three *Salmonella* isolates recovered from meat products were confirmed to belong to 6 different serotypes; the predominant one being *S. hadar* followed by *S. Heidelberg, S.* typhimurium var Copenhagen, *S. newport*, *S. saintpaul* and *S. agona.*  Overall, *Salmonella* isolates from raw turkey products exhibited a higher antimicrobial resistance rate (53%) compared to those from RTE products (33%). Multidrug resistance was exhibited by 54% of the *Salmonella* isolates with the majority (62%) originating from RTE meats compared to 45% from raw ones.

In the Kegode et al (2008) study the distribution of samples that tested positive for *Salmonella* by meat type and meat part is summarized in Table 6. *Salmonella* was recovered from turkey breast (1/8, 13%), ground turkey breast (1/15, 7%), and turkey drumsticks (1/20, 5%) (Table 6). For chicken products *Salmonella* (2/5, 40%) were recovered from whole chicken. Thirteen *Salmonella* isolates recovered from the meat samples were confirmed by NVSL to belong to eight different *Salmonella enterica* serotypes (Table 7). The predominant serotype was *S*. *enterica s*erotype Heidelberg recovered from turkey from which *S.* Typhimurium, *S.* Newport, *S.* Saintpaul and *S.* Senftenberg were also recovered. *S*. Kentucky, *S.* Typhimurium var Copenhagen, *S.* Blockley, and one undetermined serotype were recovered from chicken.

In the study by Tumuhairwe et al, 2007) that investigated the temporal and spatial distribution of 1465 salmonellosis outbreaks involving 49/50 states in the US, turkey meat associated outbreaks (TMAOs) were reported by 24 states, mostly from California and New York. Additionally, turkey meat was implicated in 4.2% of outbreaks, sea-foods (5.8%), pasta (8.3%), milk-products (8.6%), chicken (13.4%), red-meats (15.4%), eggs (21.3%), and freshproduces (22.9%). Most outbreaks were at restaurants and private-homes for TMAOs (23.2% and 21%). The major serotypes were: S. Enteritidis, S. Heidelberg, S. Reading and S. Newport for TMAOs,

In the study by Tumuhairwe et al (2008), there were 45 different serotypes that were recovered from 71.8% (277/386) of the salmonellosis cases in North Dakota (2000 to 2005). The four major ones contributing over 70% of the cases were: *S.* Typhimurium (93, 33.1%), *S.*  Enteritidis (40, 14.2%), *S.* Heidelberg (33, 11.7%) and *S.* Newport (32, 11.4%). The rest of the serotypes were: *S.* Saintpaul and *S.* Montevideo from eight cases each, *S.* Thompson was recovered from five cases, *S.* Hadar from four cases, *S.* Stanley*, S.* Poona*, S.* Mbandaka, *S.*  Javiana, *S.* Braenderup, and *S.* Bredeney from three patients each. *S.* Reading, *S.*  Oranienburg, *S.* Hillington, *S.* Derby, *S.* Urbana, and *S.* Albany were each recovered from 2 cases. One case each was diagnosed with *S.* Agona, *S.* Berta, *S.* Bleadon, *S.* Blockley, *S.*  Chameleon, *S.* Ealing, *S.* Edinburgh, *S.* Havana, *S.* Ibadan, *S.* Indiana, *S.* Infantis, *S.* Istanbul, *S.* Lexington, *S.* Litchfield, *S.* Manhattan, *S.* Marina, *S.* Miami, *S.* Mississippi, *S.* Muenchen, *S.* Newport, *S.* Othmarschen, *S.* Sandiego, *S.* Schwarzengrund, *S.* Senftenberg, *S.* Sepsis, *S.*  Syrsis, *S.* Tripoli, *S.* Uppsala, and *S.* Weltevereden.

Antimicrobial Drug Resistance and Molecular Characterization

United States metropolitan area, 2005.

**swine, turkeys, elk and bison) 3.3.1** *Salmonella* **serotypes** 

from NDDoH (Table 8).

of *Salmonella* Isolated from Domestic Animals, Humans and Meat Products 229

*Salmonella* **serotypes** n (%) Chicken Turkey

*S.* Heidelberg 4 (30.8) 0 4 *S.* Kentucky 2 (15.4) 2 0 *S.* Typhimurium (Copenhagen) 1 (7.7) 1 0 *S.* Typhimurium 1 (7.7) 0 1 *S*. Blockley 1 (7.7) 1 0 *S.* Newport 1 (7.7) 0 1 *S.* Saintpaul 1 (7.7) 0 1 *S.* Senftenberg 1 (7.7) 0 1 Unknown 1 (7.7) 1 0 Total 13 (100) 5 8

Table 7. *Salmonella enterica* serotypes recovered from retail meats in the Midwestern

**3.3** *Salmonella* **from clinical cases of humans and animals (cattle, chicken, ducks,** 

A total of 434 isolates were serotyped, including the 255 (58.8%) isolates from NDSU (from apparently healthy cattle, sick or dead animals and meat products) and 179 (41.2%) isolates

Serotypes Cattle Human Chicken Ducks Swine Turkey Bison Elk Others Total

Agona - 3(0.7) - - - 1(0.2) - - - 4(0.9) Anatum - 1(0.2) - - - 2(0.5) - - - 3(0.7) Arizona 3 (0.7) - - - - - - - - 3(0.7) Blockley - - 2(0.5) - - - - - - 2(0.5) Braenderup - 1(0.2) - - - - - - - 1(0.2) Brandeberg - 2(0.5) - - - - - - - 2(0.5) Bredeney - 2(0.5) - - - - - - - 2(0.5) Derby - - - - 2(0.5) - - - - 2(0.5) Dublin 2 (0.5) - - - - - - - - 2(0.5) Ealing - 1(0.2) - - - - - - - 1(0.2) Enteritidis - - - 1(0.2) - - - - - 1(0.2) Give 4 (0.9) - - - - - - - - 4(0.9) Hadar - - - - - 10(2.3) - - - 10(2.3) Havana - 1(0.2) - - - - - - - 1(0.2) Heidelberg - 5(1.2) - - - 9(2.1) - - - 14 (3.2) Indiana - 2(0.5) - - - - - - 2(0.5)


Table 6. Number and percentage of retail meat samples that tested positive for *salmonella* by store and meat type, 2005 (n = 456).


United States metropolitan area, 2005.

228 Salmonella – A Dangerous Foodborne Pathogen

Store/Meat Type *Salmonella* 

whole chicken 0 ground turkey 1 turkey breast 1 Total 2 2/97 (2%)

turkey drumstick 1 chicken drumstick 1 chicken thigh 0 whole chicken 2 Total 4 4/108 (4%)

chicken breast 0 chicken thigh 0 chicken wings 0 whole chicken 0

breast <sup>1</sup> Total 1 1/95 (1.1%)

ground turkey 4 chicken thigh 1 whole chicken 0 chicken wings 0 turkey thigh 0 Total 5 5/93 (5.4%)

 chicken breast 1 Total 1 1/63 (1.6%) Grand Total (n =456) 13 13/456 (2.9%)

Table 6. Number and percentage of retail meat samples that tested positive for *salmonella* by

Store A (n=97)

Store B (n=108)

Store C (n=95)

ground turkey

Store D (n = 93)

Store E (n = 63)

store and meat type, 2005 (n = 456).

Table 7. *Salmonella enterica* serotypes recovered from retail meats in the Midwestern

#### **3.3** *Salmonella* **from clinical cases of humans and animals (cattle, chicken, ducks, swine, turkeys, elk and bison) 3.3.1** *Salmonella* **serotypes**

A total of 434 isolates were serotyped, including the 255 (58.8%) isolates from NDSU (from apparently healthy cattle, sick or dead animals and meat products) and 179 (41.2%) isolates from NDDoH (Table 8).


Antimicrobial Drug Resistance and Molecular Characterization

isolates with similar PFGE profile were recorded after (Table 9).

Fig. 2. PGFE profile of the commonly serotypes isolated from domestic animals or their

provided in Table 8.

**3.3.2 PFGE Results** 

products and humans.

of *Salmonella* Isolated from Domestic Animals, Humans and Meat Products 231

from sick or dead animals submitted to the NDSU-VDL. Of the 42 serotypes involved in animal and human infection, human isolates were highly diverse with 32 serotypes involved compared to cattle (9), turkeys (8), chickens (2), bison (2), swine (2), ducks (1) and elk (1). The detailed distribution of the different serotypes between different host species is

The initial 434 *Salmonella* isolates were grouped into 113 distinct PFGE profiles at 85% similarity (Tables 9, 10, 11; Figure 2). The 179 human isolates were distributed within the 98 of the 113 PFGE fingerprint patterns or profiles at the same level of similarity. A detailed examination of the 273 isolates from serotypes commonly isolated from man (n=90) and domestic animals (n=183), revealed that 40 of the human and 55 animal isolates were distributed amongst 8 distinct (i.e. with 100% similarity) PFGE fingerprint profiles. The 40 isolates from the human cases were linked to 2 serotypes – *S. Typhimurium Copenhagen* and *S. Heidelberg* that shared indistinguishable genetic fingerprint patterns (100% homology) with some animal isolates. The biggest clonal group involving *S. Typhimurium Copenhagen* with 100 % similarity in the PFGE fingerprint patterns involved 22 isolates from cattle, 17 Humans and 1 from a sick swine (Figure 2). The second PFGE profile involved 19 isolates of *S. Typhimurium Copenhagen* with indistinguishable fingerprints, isolated from 7 feedlot cattle, 2 range cattle and 10 human cases (Figure 2). The third profile had 10 cattle and 4 humans, fifth profile had 1 human, 1 swine and 1 turkey, sixth profile was identified as *S. Heidelberg* form human (1) and turkey meat (1), seventh profile had *S. Typhimurium Copenhagen* from cattle (4), human (5) and chicken (1) and the eighth profile had S. *Heidelberg,* isolated from human (1) and turkey meat (1). Figure 2 shows details of human and domestic animal serotypes in the eight distinct profiles each with indistinguishable PFGE fingerprint patterns. The isolation of serovars with similar PFGE patterns in cattle preceded those in humans. Most outbreaks were recorded in 2004 (58%), while a few turkey


Table 8. *Salmonella* serotypes isolated from different animal species and human cases in North Dakota.

The total number of isolates that were common between domestic animals and humans were 183 (42.2%) and 90 (20.7%) respectively (Table 8). *S. Typhimurium* was the predominant serotype in both humans (13.4%, n=58) and domestic animals (34.3%, n= 159), followed by Newport with 11 (2.6%) and 17(3.9%) isolated in animals and human, respectively. *S. Arizona* (n=3, 0.7%)*, S. Give* (n=4, 0.9%) *and S. Muenster* (n=15, 3.5%) were isolated mostly from sick or dead animals submitted to the NDSU-VDL. Of the 42 serotypes involved in animal and human infection, human isolates were highly diverse with 32 serotypes involved compared to cattle (9), turkeys (8), chickens (2), bison (2), swine (2), ducks (1) and elk (1). The detailed distribution of the different serotypes between different host species is provided in Table 8.
