Food Protection Trends - May/June 2014 - 152

in ground turkey (14). Antimicrobial-resistant Salmonella
strains may be more virulent than antimicrobial-sensitive
salmonellae (4, 6, 9), though this is still a topic of debate.
In 2008, 51% of all Salmonella isolates were MDR (14). From
2002 to 2007, MDR Salmonella (resistant to three or more
antimicrobial classes) ranged from 20.3% to 42.6% among
isolates in ground turkey (14). Importantly, fluoroquinolone
resistance has rarely been reported in Salmonella Hadar in the
United States (14) as well as in Salmonella Hadar isolated from
turkey meat in Denmark (3). Fluoroquinolone resistance also
is an emerging issue in Salmonella Kentucky, another serotype
common in poultry (11).
The United States Department of Agriculture, Food Safety
and Inspection Service (FSIS) has recalled products because
of contamination with MDR Salmonella associated with
human illness. In 2009, a cluster of 42 MDR Salmonella
Newport illnesses in 11 states was linked to consumption of
ground beef; the investigation resulted in a recall of 825,769
lbs of ground beef (7). Also in 2009, a cluster of 15 MDR
Salmonella Typhimurium illnesses in Colorado was linked
to consumption of ground beef, which resulted in a recall of
466,236 pounds of ground beef (8). This report describes the
investigation that resulted in the first FSIS raw poultry recall
due to contamination with MDR Salmonella.
MATERIALS AND METHODS
linical laboratories send Salmonella isolates from casepatients to state public health laboratories for serotyping
and Pulsed-Field Gel Electrophorsis (PFGE) subtyping (18).
State public health laboratories submit PFGE subtyping
results to the national molecular subtyping network for
foodborne disease surveillance (PulseNet) database for
rapid detection of disease clusters. In this investigation,
the Wisconsin State Laboratory of Hygiene (WSLH)
additionally performed antimicrobial susceptibility testing
on the Salmonella Hadar clinical isolates, using Clinical and
Laboratory Standards Institute (CLSI) protocols. Also using
CLSI automated protocols, but testing a different panel of
antimicrobials, a Colorado hospital laboratory performed
antimicrobial susceptibility testing on a single Salmonella
Hadar clinical isolate.
A case was defined as a in a person with laboratory-confirmed
Salmonella Hadar infection with PFGE Xbal pattern
indistinguishable from the outbreak strain isolated between
December 27, 2010 and March 29, 2011. FSIS worked with
10 health departments in states with cases in the cluster.
State and local health departments conducted case-patient
interviews concerning poultry consumption in the seven
days prior to diarrheal onset, including type of product and
brand. Case-patients (or their families) also were asked
about hospitalization. Findings from these interviews were
provided to FSIS.
The Wisconsin Department of Agriculture Trade and
Consumer Protection-Bureau of Laboratory Services

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May/June

(DATCP-BLS) conducted culture and isolation from
the product purchased in Wisconsin. The product isolate
was sent to the WSLH for serotyping, PFGE subtyping,
and susceptibility testing (using Clinical and Laboratory
Standards Institute (CLSI) protocols). The Colorado
Department of Public Health and Environment Laboratory
Services Division (CDPHE) performed culture, isolation,
serotyping, and PFGE subtyping from the product consumed
by the Colorado case-patient. Susceptibility testing was
performed at USDA Agricultural Research Service (ARS)
using National Antimicrobial Resistance Monitoring
System (NARMS) sensititre methods for the Colorado and
Wisconsin product isolates.
FSIS reviewed historic Salmonella Pathogen Reduction/
Hazard Analysis and Critical Control Points (HACCP)
verification sampling results for Salmonella Hadar at
the Company A processing establishment and at the
slaughter establishments that supplied the source products.
Establishments use PR/HACCP to identify where potential
hazards are likely to occur and take steps to prevent,
eliminate, or mitigate these hazards to ensure product safety.
FSIS verifies that establishments are operating effectively
under their PR/HACCP plan. In addition, FSIS requested
PFGE and NARMS data from the USDA Agricultural
Research Service, Bacterial Epidemiology and Antimicrobial
Resistance research unit (ARS-BEAR) to determine historic
Salmonella trends at Company A.
RESULTS
n mid-January 2011, the Minnesota Department of
Agriculture's retail food sampling program detected
Salmonella Hadar in a turkey and gravy product produced by
Company A, a corporation with nationwide distribution. A
Minnesota case-patient with infection of the same serotype
and indistinguishable PFGE pattern reported turkey
consumption; however, the product had been purchased and
then frozen six months prior to consumption. Additional
product traceback information was not available from
this case-patient. At approximately the same time, two
clinical Salmonella Hadar isolates with indistinguishable
PFGE results were uploaded in Wisconsin. FSIS asked the
Wisconsin Department of Health Services (WDHS) for the
dietary histories of the case-patients; one case-patient was
lost to follow-up and a reliable food history could not be
obtained from the other case-patient.
On February 11, 2011, WDHS notified FSIS of another
case-patient with Salmonella Hadar infection with an
indistinguishable PFGE pattern. The case-patient reported
consuming Company A turkey burgers in the seven days
prior to illness onset. During a follow-up interview, the casepatient reported having unopened, individually wrapped
Company A turkey burger product that was from the same
box as the product that had been consumed prior to illness.
The case-patient's family was willing to have it tested. WDHS

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