Food Protection Trends - May/June 2014 - 154

a food safety assessment, a specialized and comprehensive
investigation of the establishment's food safety system
decisions, design, and controls, from April to May 2011;
FSIS issued a Notice of Intended Enforcement (NOIE)
in early May 2011 to Company A. An NOIE is issued for
noncompliance that does not pose an imminent threat to
public health but may warrant a withholding or suspension
action if not corrected. Among other findings, the issuance
cited lack of validated cooking instructions.
FSIS worked with the Centers for Disease Control and
Prevention (CDC) to monitor PulseNet for new casepatients with indistinguishable PFGE patterns for the next
60 days to determine whether the scope of the recall was
adequate. The FSIS Consumer Complaint Monitoring
System (CCMS) logged several illness-related complaints
related to Company A turkey burgers during this time.
Leftover product from two complainants' homes was tested
for Salmonella. Neither of the samples was positive for the
outbreak strain.
DISCUSSION
lthough a small number of cases were identified during
this specific outbreak investigation, previous studies
have demonstrated an estimated 38.6 cases of salmonellosis
for each culture-confirmed case (20). Among those in the
cluster exposed to Company A turkey burgers within a week
of illness onset, FSIS was concerned by the unusually high
proportion of hospitalized case-patients and the multidrug
resistance of the Salmonella involved. It is not known whether
the multidrug resistance of this strain resulted in treatment
failure for any of the hospitalized case-patients; such

information would be useful for further understanding of the
public health impacts of MDR Salmonella infections.
A number of factors affect the susceptibility of poultry
to Salmonella colonization, including age, serotype, dose
level, stress, feed additives, and genetic background (1, 12).
Additionally, in high-density production environments
such as in poultry settings, the potential for disease spread
increases. In a 2010 NARMS survey of Salmonella Hadar
from 1996 to 2008, 41.8% of isolates from retail meat
were resistant to three or more antimicrobial classes.
Among Salmonella Hadar isolates from the food animals at
slaughter, 19.4% were MDR (17). It is important to note
that these resistance results are less striking than the 73.9%
of Salmonella Hadar MDR PR/HACCP samples found at
Company A.
Based on recent FSIS nationwide microbiological baseline
data collection, new, stricter Salmonella standards were
implemented by FSIS in July 2011. Following these
standards, an establishment passes Salmonella verification
testing if no more that five samples are positive in a
51-sample set for young chickens and if no more than four
samples are positive in a 51-sample set for turkeys. FSIS
estimates that 20,000 illnesses will be avoided under the
revised standards, which are set at 7.5 and 1.7 percent
Salmonella positive in young chicken (broilers) and young
turkey, respectively, compared to the former standards of
20 and 19 percent positive (5, 16, 19). This investigation,
which resulted in the first-ever FSIS raw poultry recall due to
contamination with MDR Salmonella in the United States,
would not have been possible without extensive coordination
among public health partners, including regulatory agencies.

REFERENCES
2008-0008. Available at: http://www.fsis.usda.
gov/ OPPDE/rdad/FRPubs/2008-0008.htm.
Accessed 1 December 2013.

1. Bailey, J. S. Integrated colonization control
of Salmonella in poultry. 1988. Poult. Sci.
67:928-932.
2. Behravesh, C. B., M. Lynch, and J. Schlundt.
2008. Salmonellosis, p. 534-540. In D. L.
Heynmann (ed.), Control of Communicable
Diseases Manual. American Public Health
Association, Washington, D.C.
3. Cavaco, L. M., H. Korsgaard, G. Sorensen,
and F. M. Aarestrup. 2008. Plasmid-mediated
quinolone resistance due to qnrB5 and qnrS1
genes in Salmonella enterica serovars Newport,
Hadar, and Saintpaul isloated from turkey
meat in Denmark. J. Antimicrob. Chemother.
62:632-634.
4. Eswarappa, S. M., K. K. Panguluri, M. Hensel,
and D. Chakravortty. 2008. The yejABEF
operon of Salmonella confers resistance to
antimicrobial peptides and contributes to its
virulence. J. Microbiol. 154:666-678.
5. Federal Register Vol. 76, No. 134, July 13,
2011, Department of Agriculture Food Safety
and Inspection Service Docket No. FSIS-

154

Food Protection Trends

6. Fluit, A. C. Towards more virulent and
antibiotic-resistant Salmonella? 2005. FEMS
Immunol. Med. Microbiol. 43:1-11.
7. FSIS recall release FSIS-RC-041-2009.
Available at: http://www.fsis.usda.gov/
wps/portal/ fsis/topics/recalls-and-publichealth-alerts/recall-case-archive. Accessed 13
January 2014.
8. FSIS recall release FSIS-RC-039-2009.
Available at: http://www.fsis.usda.gov/
wps/portal/ fsis/topics/recalls-and-publichealth-alerts/recall-case-archive. Accessed 13
January 2014.
9. Gebreyes, W. A., S. Thakur, P. Dorr,
D. A. Tadesse, K. Post, and L. Wolf. 2009.
Occurrence of spvA virulence gene and clinical
significance for multidrug-resistant Salmonella
strains. J. Clin. Microbiol. 47:777-780.

May/June

10. Ground Poultry and Food Safety. Available at:
http://www.fsis.usda.gov/wps/ portal/fsis/
topics/food-safety-education/get-answers/
food-safety-fact-sheets/poultry-preparation/
ground-poultry-and-food-safety/ct_index.
Accessed 13 January 2014.
11. Le Hello, S., R. S. Hendriksen, B. Doublet,
I. Fisher, E. M. Nielsen, J. M. Whichard,
B. Bouchrif, K. Fashae, S. A. Granier, N.
Jourdan-Da Silva, A. Cloeckaert, E. J. Threlfall,
F. J. Angulo, F. M. Aarestrup, J. Wain, and
F. X. Weill. 2011. International spread of an
epidemic population of Salmonella enterica
serotype Kentucky ST198 resistant to ciprofloxacin. J. Infect. Dis. 204:675-684.
12. McEwen S. A., and P. J. Fedorka-Cray. 2002.
Antimicrobial use and resistance in animals.
CID 34: S93-S106.
13. National Antimicrobial Resistance Monitoring
System. NARMS 2008 animal ARM annual report. Available at: https://www.ars.usda.gov/
SP2UserFiles/Place/66120508/ NARMS/
NARMS2008/Table4A.pdf. Accessed 1
December 2013.

Food Protection Trends - May/June 2014

Table of Contents for the Digital Edition of Food Protection Trends - May/June 2014