Natural Resources Defense Council, Inc. et al v. United States Food and Drug Administration et al

Filing 33

DECLARATION of Jennifer A. Sorenson in Support re: 19 MOTION for Summary Judgment.. Document filed by Center For Science In The Public Interest, Food Animal Concerns Trust, Natural Resources Defense Council, Inc., Public Citizen, Inc., Union Of Concerned Scientists, Inc.. (Attachments: # 1 Exhibit A, # 2 Exhibit B, # 3 Exhibit C, # 4 Exhibit D, # 5 Exhibit E, # 6 Exhibit F, # 7 Exhibit G, # 8 Exhibit H, # 9 Exhibit I, # 10 Exhibit J, # 11 Exhibit K, # 12 Exhibit L, # 13 Exhibit M, # 14 Exhibit N, # 15 Exhibit O, # 16 Exhibit P, # 17 Exhibit Q, # 18 Exhibit R, # 19 Exhibit S, # 20 Exhibit T, # 21 Exhibit U, # 22 Exhibit V, # 23 Exhibit W, # 24 Exhibit X, # 25 Exhibit Y, # 26 Exhibit Z, # 27 Exhibit AA, # 28 Exhibit BB, # 29 Exhibit CC, # 30 Exhibit DD)(Sorenson, Jennifer)

EXHIBIT V
TO DECLARATION OF
JENNIFER A. SORENSON
National Antimicrobial Resistance Monitoring System
2009 Retail Meat Report

TABLE OF CONTENTS

Abbreviations…….......……………………………………………..………………………………………………………4
Acknowledgements…...……………………………………………………………………………………………………5
Introduction & Summary………….…………………………………………………………………………………………
6-9
Surveillance and Laboratory Testing Methods…………….…………………………………………………………… 10-13
Interpretive Criteria…………………………………………………………………………………………………………14-15
PREVALENCE DATA
Percent Positive Samples
Site and Bacterium, 2002-2009...……………....…………………………………………………………………………
16-19
Bacterium and Meat Type, 2002-2009….……….......……………………………………………………………………
20
Salmonella & Campylobacter by Meat Type, 2002-2009….….…………………………………………………..……
21
SALMONELLA DATA
Salmonella by Serotype and Meat Type, 2009……………………………………………………………………..……
22
Trends in Resistance
Salmonella by Meat Type, 2002-2009
23-27
By Top Serotypes within Meat Type, 2009..…………………………………………………….……………………… 28
Resistance to Multiple Antimicrobial Agents
Multidrug Resistance Patterns, 2002-2009………………………………………………………………………………29
Resistance to Multiple Classes by Meat Type, 2002-2009…………………………………………………………… 30
MIC Distributions
Chicken Breast, 2002-2009….…………………………………………………………………………………………… 31-32
Ground Turkey, 2002-2009…………………………………………………………………………………………………
33-34
Ground Beef, 2002-2009.………………………………………………………………………………………………… 35-36
Pork Chop, 2002-2009………………………………………………………………………………………………………
37-38
CAMPYLOBACTER DATA
Campylobacter Species by Meat Type, 2002-2009………………………………………………………………...… 39
Campylobacter jejuni and C. coli Isolated by Month from Chicken Breast, 2002-2009……………………..…….40
Trends in Resistance
Campylobacter Species by Meat Type, 2002-2009……………………….………………………………….
41
Campylobacter jejuni and C. coli from Chicken Breast, 2002-2009………………………………………………… 42-44
Resistance to Multiple Antimicrobial Agents
Campylobacter jejuni and C. coli Resistant to Multiple Classes by Meat Type, 2002-2009……..…………………
45
MIC Distributions in Chicken Breast
Campylobacter jejuni , 2002-2009…………………………………………………………………………………………
46
Campylobacter coli , 2002-2009……………………………………………………………………………………………
47

2

ENTEROCOCCUS DATA
Enterococcus Species by Meat Type, 2002-2009.………………………………………………………..……………48
Trends in Resistance
Enterococcus by Meat Type, 2002-2009…………………………………………………………………………………
49-53
Enterococcus faecalis by Meat Type, 2002-2009……………………………………………………….………………
54
Enterococcus faecium by Meat Type, 2002-2009………………………………………………………………………55
Enterococcus hirae by Meat Type, 2002-2009…………………………………………………………………………56
Resistance to Multiple Antimicrobial Agents
Enterococcus faecalis Resistant to Multiple Classes by Meat Type, 2002-2009……………………………………
57
Enterococcus faecium Resistant to Multiple Classes by Meat Type, 2002-2009……………………………………
58
MIC Distributions by Species
Chicken Breast, 2009……………………………………………………………………………………...……………… 59
Ground Turkey, 2009………………………………………………………………………………………...…..…………
60
Ground Beef, 2009……………………………………………………………….………………………..…..……………
61
Pork Chop, 2009……………………………………………………………………………………....………………….…
62
ESCHERICHIA COLI DATA
Escherichia coli Prevalence by Meat Type, 2002-2009………………………..………………………………………63
Trends in Resistance
Escherichia coli by Meat Type, 2002-2009

64-68

Resistance to Multiple Antimicrobial Agents
Multidrug Resistance Patterns, 2002-2009………………………………………………………………………………69
Resistance to Multiple Classes by Meat Type, 2002-2009…………………………………………………………… 70
MIC Distributions
Chicken Breast, 2009………………………………………………………………………………………………………71-72
Ground Turkey, 2009……………………………………………………………………………………………………..…
73-74
Ground Beef, 2009…………………………………………………………………………………………………………75-76
Pork Chop, 2009..……………………………………………………………………………………………………………
77-78
APPENDICES
PFGE Profiles For Salmonella Isolates………………………………………………………...…………………………
79-89
Log Sheet Example………..…………………………………………………………………………………...………...…
90

3

ABBREVIATIONS USED IN THE REPORT, 2009
General Abbreviations
AR
Antimicrobial Resistance
BAP
Blood Agar Plate
CCA
Campy-Cefex Agar Plate
CDC
Centers for Disease Control and Prevention
CLSI
Clinical and Laboratory Standards Institute
CVM
Center for Veterinary Medicine
EAP
Enterococcosel Agar Plate
EIP
Emerging Infections Program
EMB
Eosin Methylene Blue
FDA
Food and Drug Administration
FoodNet
Foodborne Diseases Active Surveillance Network
MIC
Minimum Inhibitory Concentration
NARMS
National Antimicrobial Resistance Monitoring System
PCR
Polymerase Chain Reaction
PFGE
Pulsed Field Gel Electrophoresis
PulseNet
National Molecular Subtyping Network for Foodborne Disease Surveillance
QC
Quality Control
RVR10
Rappaport-Vassiliadis Medium
USDA
United States Department of Agriculture
XLD
Xylose Lysine Deoxycholate
Antimicrobial Abbreviations
AMC Amoxicillin/Clavulanic Acid
AMI Amikacin
AMP Ampicillin
AXO Ceftriaxone
AZI Azithromycin
CHL Chloramphenicol
CIP Ciprofloxacin
CLI Clindamycin
COT Trimethoprim/Sulfamethoxazole
DAP Daptomycin
DOX Doxycycline
ERY Erythromycin
FFN Florfenicol
FIS Sulfisoxazole
FOX Cefoxitin

GEN
KAN
LIN
LZD
NAL
NIT
PEN
QDA
STR
TEL
TET
TGC
TYL
TIO
VAN

Gentamicin
Kanamycin
Lincomycin
Linezolid
Nalidixic Acid
Nitrofurantoin
Penicillin
Quinupristin/Dalfopristin
Streptomycin
Telithromycin
Tetracycline
Tigecycline
Tylosin
Ceftiofur
Vancomycin

Meat Types Abbreviations
CB
Chicken Breast
GB
Ground Beef

GT
PC

Ground Turkey
Pork Chop

State Abbreviations
CA
California
CO Colorado
CT
Connecticut
GA
Georgia
MD Maryland
MN Minnesota

NM
NY
OR
PA
TN

New Mexico
New York
Oregon
Pennsylvania
Tennessee

4

NARMS Retail Meat Working Group
U.S. Food and Drug

Participating State and Local

Administration

Health Departments

Jason Abbott
Sherry Ayers

California

Minnesota

Pennsylvania

Sonya Bodeis-Jones

Richard Alexander

John Besser

Michael Nageotte

Kristin Cooley

Melody Hung-Fan

Craig Braymen

Stanley Reynolds

Sharon Friedman

Maribel Rickard

Karen Everstine

Deepanker Tewari

Gary Horvath

Anthony Russell

Stuart Gaines

Colorado

David Heller

Joe Gossack

Billie Juni

Ann Rosenberg

Claudia Lam

Dee Jae Dutton

Fe Leano

Carol Sandt

Patrick McDermott

Dave Heltzel

Stephanie Meyer

Lisa Dettinger

Shawn McDermott

Hugh Maguire

Kirk Smith

Susan Johnston

Leeann Johnson

Nkuchia M. M’ikanatha

Sadaf Qaiyumi

Connecticut

Emily Tong

Aristea Kinney

Niketta Womack

Mona Mandour

Adreiena Armijo

Parvin Arjmandi

Shenia Young

Ruthanne Marcus

Lisa Butler

Samir Hanna

Shaohua Zhao

Michael A. Pascucilla

Carlos Gonzales

Henrietta Hardin

Laurn Mank

Cindy Nicholson

Tim Jones

Diane Barden

Nicole Espinoza

Ryan Mason

Erica Swanson

Sheri Roberts

Centers for Disease

Georgia

New Mexico

Tennessee

Control and Prevention

James Benson

Paul Torres

John Dunn

Fred Angulo

Cherie Drenzek

Frederick Gentry

Stephanie Estes

Ezra Barzilay

Tameka Hayes

Jennifer Hollander

Kenneth Mitchell

Olympia Anderson

Lynett Poventud

Sharon Greene

Elizabeth Franko

Dale Morse

Bobby Price

Felicita Medalla

Mary Hodel

Marsha Peck

Henry Davis

Mahin Park

Timothy Root

Julie Montgomery

Melissa Tobin-D’angelo

Shelley Zansky

Maryland
David Blythe
Beverly Jolbitado

New York

Robyn Atkinson

Ariel Endlich-Frazier
Suzanne Solghan
Oregon

Jennifer Kiluk

Elizabeth Baldwin

Kirsten Larson

Emilio DeBess

Amanda Palmer

Helen Packett

Many thanks to Denise

Patricia Ryan

Robert Vega

Benton and Laura Alvey

Chengru Zhu

Veronica Williams

for providing outstanding

Marianna Cavanaugh

web support to the

Dawn Daly

NARMS program.

Barbara Olson
Vicki A. Hafits
5

NARMS Retail Meat Annual Report 2009
Introduction
The primary purpose of the NARMS retail meat surveillance program is to monitor the
prevalence of antimicrobial resistance among foodborne bacteria, specifically, Salmonella,
Campylobacter, Enterococcus and Escherichia coli. The results generated by the NARMS retail
meat program serve as a reference point for identifying and analyzing trends in antimicrobial
resistance among these organisms.
NARMS retail meat surveillance is an ongoing collaboration between the U.S. Food and
Drug Administration/Center for Veterinary Medicine (FDA/CVM), the Centers for Disease
Control and Prevention (CDC), the 2009 FoodNet laboratories and an additional State
Department of Public Health Laboratory: California, Colorado, Connecticut, Georgia, Maryland,
Minnesota, New Mexico, New York, Oregon, Tennessee, and Pennsylvania. From January to
December, each site purchased approximately 40 food samples per month, which are
comprised of 10 samples each from chicken breast, ground turkey, ground beef, and pork
chops. All sites culture the meat and poultry samples for Salmonella and only poultry samples
are cultured for Campylobacter. In 2009, 3 of the 10 participating FoodNet laboratories
(Georgia, Oregon, and Tennessee) also cultured meat and poultry samples for E. coli and
Enterococcus. Bacterial isolates were sent to FDA/CVM for confirmation of species and
serotypes, antimicrobial susceptibility testing, and genetic analysis.
As a public health monitoring system, the primary objectives of NARMS are to:
•

Monitor trends in antimicrobial resistance among foodborne bacteria from humans,
retail meats, and animals

•

Disseminate timely information on antimicrobial resistance to promote interventions
that reduce resistance among foodborne bacteria

•

Conduct research to better understand the emergence, persistence, and spread of
antimicrobial resistance

•

Assist the FDA in making decisions related to the approval of safe and effective
antimicrobial drugs for animals

6

What is New in the NARMS Retail Meat Report for 2009
A total of 5,280 meat samples were collected in 2009, compared with 5,236 in 2008.
The Pennsylvania Department of Public Health Laboratory joined the NARMS retail meat
surveillance program in 2008 but was only testing meat samples for Salmonella. As of 2009,
Pennsylvania has increased their testing to include Campylobacter isolation from poultry
samples.
In 2008, both CMV2AGPF and CMV3AGPF SensititreTM plates were used for
Enterococcus testing and the smaller range from either plate was used in the report. In 2009,
all Enterococcus testing were performed using the CMV3AGPF SensititreTM plate. Resistance
data for flavomycin was excluded from this report as the new CMV3AGPF plate does not
include this antimicrobial. Flavomycin resistance data can be found in prior NARMS Retail Meat
Reports. The CMV3AGPF range of dilutions tested expanded for daptomycin, erythromycin,
penicillin, quinupristin-dalfopristin and tetracycline, while ranges decreased for lincomycin and
vancomycin.
Prior to 2009 NARMS reports used ceftiofur (an extended-spectrum cephalosporin used
in food animals) to represent resistance to third-generation cephalosporins in the multidrug
resistance patterns. In 2009 ceftriaxone replaced ceftiofur in the multidrug resistance patterns
presented in this report, resulting from revised ceftriaxone breakpoints where ceftriaxone
resistance (MIC ≥ 4 μg/ml) is nearly identical to ceftiofur resistance.
A new table (Table 6.) was added to the Salmonella multidrug resistance section of this
report. This table highlights the number of resistant isolates by Salmonella serotype for each
retail meat. This table is very useful for comparing the distribution of Salmonella serotype
specific resistance among the different classes of antimicrobials. Salmonella antigenic formulas
I 4,12:i:- and I 4,5,12:i:- were included with serotype I 4,[5],12:i:- to correspond with the NARMS
Executive Report.

7

Highlights of the NARMS Retail 2009 Report
Salmonella 1
Salmonella serotypes Typhimurium, Saintpaul, and Heidelberg account for 53% of retail
meat isolates (Table 4). S. Typhimurium and S. Saintpaul increased markedly from an
average of 11.4% and 8.9% from 2002–2008 to 25.6% and 16.4% in 2009, respectively.
In 2009 S. Saintpaul became the most common serotype in ground turkey. Also never
seen before was a higher prevalence of S. Heidelberg among chicken breast over
ground turkey. S. Heidelberg prevalence among all retail meat continued to decrease
from 22.8–11.5% from 2002–2009.
First-line antimicrobial agents recommended for treating salmonellosis are ciprofloxacin,
ceftriaxone and trimethoprim-sulfamethoxazole. 2
o

o
o
o
o

o

Quinolones - Resistance to nalidixic acid corresponds to decreased fluoroquinolone
susceptibility; however, fluoroquinolone resistance has never been detected in
Salmonella recovered from any retail meat since the program began in 2002. Only
0.8% of Salmonella (4/489) were nalidixic acid resistant (Table 5). Nalidixic acid
resistance was detected for the first time in ground beef and 2 of 3 ground beef
isolates resistant to nalidixic acid were also ceftriaxone resistant.
Cephalosporins – Third-generation cephalosporin resistance rose in all retail meats
compared to 2008, with > 10% increases detected in chicken breast.
There were highly significant increases in ampicillin resistance among chicken breast
(16.7–45.8%) and ground turkey isolates (16.2–57.9%) from 2002 to 2009.
Trimethoprim-Sulfamethoxazole - Resistance to this antimicrobial is extremely rare
and 6 (of 489) isolates were resistant in 2009 compared to only 1 in 2008.
Multidrug Resistance – 48.4% of chicken breast isolates were resistant to ≥ 3
antimicrobial classes in 2009 compared to 26.3% in ground turkey, which is an
increase in chicken breast from previous years (ranging 20–38.2%). More than 30%
of chicken breast isolates showed resistance to ≥ 5 classes in 2009 (Table 8), to
which S. Typhimurium accounts for more than half of them (Table 6).
Salmonella isolates susceptible to all antimicrobials (Table 8) decreased in chicken
breast (45.7–29.2%), ground beef (79.2–57.1%), and pork chops (65.2–50%) from
2008 to 2009. Meanwhile, Salmonella pansusceptibility slightly increased among
ground turkey (20.8–22.1%) isolates.

Campylobacter 3
More than 90% of Campylobacter are recovered from chicken breast each year and of
those isolates, the proportion of C. jejuni to C. coli is about 2:1 (Table 10).
Macrolides and fluoroquinolones are used in the treatment of Campylobacter infections.
It is well known that C. coli tend to be more resistant than C. jejuni regardless of source,
and this is reflected in the 2009 NARMS retail data with the exception of quinolones and
tetracycline.
o

Macrolide resistance in chicken breast isolates was seen in 4.5% of C. coli and 1%
of C. jejuni in 2009, with no significant changes over time (Table 13).

1

Nearly all salmonellae were recovered from poultry. Due to the low recovery from ground beef and pork
chops (< 2%), statistical analysis of trends in resistance from these sources should be considered with
caution.
2
IDSA, Practice Guidelines for the Management of Infectious Diarrhea. Clinical Infectious Diseases 2001;
32:331–50.
3
Ground beef and pork chop samples are no longer cultured for Campylobacter, due to their low recovery
(<0.5%) from 2002–2007.

8

o

o
o
o

Ciprofloxacin resistance in C. coli from chicken breast rose from 10% in 2002 to its
highest peak of 29.1% in 2005. Since the fluoroquinolone ban in September 2005,
ciprofloxacin resistance in C. coli has decreased to 18.4% in 2009 (Table 13), while
C. jejuni significantly increased from 15.2–21.1% from 2002 to 2009 (p=0.0296).
Tetracycline resistance decreased in both C. jejuni (49.8–46.2%) and C. coli (46.4–
38%) compared to 2008.
Gentamicin resistance in C. coli has increased with 5.6% in 2009, up from 1.7% in
2008 (p<0.0001).
Multidrug resistance is rare in Campylobacter. There were only 9 (of 606)
Campylobacter isolates resistant to ≥ 3 antimicrobial classes in 2009 (Table 14).

Enterococcus
E. faecalis (67.6% [884/1307]) was more prevalent than E. faecium (27% [353/1307]) in
2009 (Table 16). Chicken breast was the only meat type where E. faecium was more
prevalent than E. faecalis.
Enterococcus is used as a sentinel for antibiotic selection pressures by compounds with
gram-positive activity. This spectrum of activity is exhibited by many antimicrobials used
in food animal production; and the same classes of antibiotics are also used to treat
human infections.
o

o
o

o

No isolates were resistant to vancomycin or linezolid. These classes of compounds
are critically important in human medicine but are not used in food animal production
(Table 17).
Since 2002, streptogramin resistance has decreased in ground beef (46.2–13%) and
pork chop (27.2–11.4%) but has remained above 50% in poultry isolates.
E. faecalis from poultry showed markedly higher aminoglycoside and macrolide
resistance than E. faecium, with exception of streptomycin. E. faecium had much
higher resistance to nitrofurantoin, penicillin and ciprofloxacin from all sources
compared to E. faecalis (Table 18a-b).
Multidrug resistance from 2002–2009 was highest in E. faecium isolates from poultry
which more than doubled the amount of multidrug resistant E. faecalis (Table 19a-b).

Escherichia coli
E. coli are common in all retail meat products tested in NARMS. Nearly 71% of the
1,440 retail meats tested in 2009 were culture positive for E. coli, with pork chops having
the lowest prevalence (40.8%) and chicken breasts the highest (87.5%).
o

o
o

o

o

Ceftriaxone resistance among E. coli isolates from chicken breast is consistently
higher than any other retail meat tested. Chicken breast (7.8–12.4%), Ground turkey
(1.3–6.9%), and pork chop (0.5–6.8%) had statistically significant trends in
ceftriaxone resistance from 2002–2009 at the p < 0.05 level (Table 22).
Ciprofloxacin resistance remained low (< 1.0%) among E. coli isolates (Table 22).
From 2002–2005, nalidixic acid resistance in E. coli from chicken breast increased
from 2.8–6.6% and increased in ground turkey from 4.3–10.4%. Since the
fluoroquinolone ban in September 2005, resistance has decreased to 2.9% in
chicken breast and 2.6% in ground turkey (Table 22). Nalidixic acid resistance in
ground beef and pork chops remains < 2%.
Gentamicin resistance is much higher in retail poultry isolates (> 20%) than ground
beef and pork chop isolates (< 5%), with a statistically significant increase among
chicken breast at the p < 0.05 level (Table 22).
A highly statistically significant trend (p<0.0001) in ampicillin resistance was seen
among ground turkey with 56.2% resistance in 2009, up from 31.3% in 2002.

9

Table 3. Percent Positive Samples by Bacterium and Meat Type, 2002-2009
2002
Bacterium (A)

Chicken Breast

Ground Turkey

N

N

Campylobacter (2513)
Salmonella (2513)
Enterococcus (1574)
Escherichia coli (1574)

616
616
390
390

2004
Bacterium (A)

Chicken Breast

Ground Turkey

N

n

(%)

N

1172
1172
476
476

706
157
466
400

(60.2)
(13.4)
(97.9)
(84.0)

1165
1165
466
466

Campylobacter (4699)
Salmonella (4699)
Enterococcus (1900)
Escherichia coli (1900)

2006
Bacterium (A)
Campylobacter (4766)
Salmonella (4769)
Enterococcus (1893)
Escherichia coli (1884)

2008
Bacterium (A)

n

(%)

288 (46.8) 642
60 (9.7) 642
381 (97.7) 395
282 (72.3) 395

n

(%)

Ground Beef
N

4
(1.0) 642
74 (11.5) 642
387 (98.0) 399
304 (77.0) 399

n

(%)

n

(%)

Pork Chop
N

613
9
(1.4) 613
383 (96.0) 390
295 (73.9) 390

Ground Beef
N

12 (1.0) 1186
142 (12.2) 1186
437 (93.8) 480
376 (80.7) 480

n

(%)

Ground Turkey

Ground Beef

N

n

(%)

N

N

1193
1196
478
475

572
152
469
418

(47.9)
(12.7)
(98.1)
(88.0)

1185
1185
465
466

Chicken Breast
N
n
(%)

(%)

24 (2.0) 1196
159 (13.4) 1196
435 (93.5) 478
388 (83.3) 471

Ground Turkey
N
n
(%)

n

(%)

5
(0.8)
10 (1.6)
369 (94.6)
184 (47.2)

n

(%)

3
(0.3)
11 (0.9)
404 (84.5)
232 (48.5)

Pork Chop
N

n

1192
19 (1.6) 1192
438 (91.6) 472
295 (62.6) 472

Ground Beef
N
n
(%)

(%)

Pork Chop
N

1176
14 (1.2) 1176
448 (93.3) 478
338 (70.4) 478

Chicken Breast

n

n

N

(%)

3
(0.3)
8
(0.7)
389 (82.4)
182 (38.6)

Pork Chop
n
(%)

Campylobacter (2379) 1190 510 (42.9) 1189 31 (2.6)
Salmonella (5236)
1310 199 (15.2) 1309 245 (18.7) 1310 24 (1.8) 1307 23 (1.8)
Enterococcus (1440)
360 346 (96.1) 360 345 (95.8) 360 336 (93.3) 360 310 (86.1)
Escherichia coli (1440) 360 306 (85.0) 360 300 (83.3) 360 250 (69.4) 360 146 (40.6)

2003
Bacterium (A)

Chicken Breast

Ground Turkey

N

N

Campylobacter (3533)
Salmonella (3533)
Enterococcus (1873)
Escherichia coli (1873)

897
897
477
477

2005
Bacterium (A)

Chicken Breast

Ground Turkey

N

n

(%)

N

1190
1194
470
468

554
153
457
393

(46.6)
(12.8)
(97.2)
(84.0)

1195
1195
470
470

Campylobacter (4777)
Salmonella (4781)
Enterococcus (1880)
Escherichia coli (1871)

2007
Bacterium (A)
Campylobacter (4278)
Salmonella (4282)
Enterococcus (1407)
Escherichia coli (1379)

2009
Bacterium (A)

n

(%)

469 (52.3) 857
83 (9.3) 857
466 (97.7) 447
396 (83.0) 447

n

(%)

Ground Beef
N

5
(0.6) 880
114 (13.3) 880
418 (93.5) 470
333 (74.5) 470

n

(%)

n

(%)

Pork Chop
N

1
(0.1) 899
10 (1.1) 899
432 (91.9) 479
311 (66.2) 479

Ground Beef
N

20 (1.7) 1196
183 (15.3) 1196
452 (96.2) 470
396 (84.3) 468

n

(%)

Ground Turkey

Ground Beef

N

N

N

1070
1072
351
342

(%)

475 (44.4) 1065
99 (9.2) 1066
342 (97.4) 348
299 (87.4) 338

Chicken Breast
N
n
(%)

n

(%)

34 (3.2) 1071
190 (17.8) 1071
341 (98.0) 352
315 (93.2) 343

Ground Turkey
N
n
(%)

n

(%)

4
(0.4)
5
(0.6)
426 (88.9)
218 (45.5)

n

(%)

2
(0.2)
9
(0.8)
409 (87.0)
205 (44.1)

Pork Chop
N

n

5
(0.5) 1072
13 (1.2) 1073
336 (95.5) 356
256 (74.6) 356

Ground Beef
N
n
(%)

(%)

Pork Chop
N

1196
8
(0.7) 1196
447 (95.1) 470
316 (67.5) 465

Chicken Breast
n

n

N

(%)

4
(0.4)
18 (1.7)
313 (87.9)
152 (42.7)

Pork Chop
n
(%)

Campylobacter (2640) 1320 582 (44.1) 1320 24 (1.8)
Salmonella (5280)
1320 277 (21.0) 1320 190 (14.4) 1320 14 (1.1) 1320 8
(0.6)
Enterococcus (1440)
360 349 (96.9) 360 328 (91.1) 360 327 (90.8) 360 303 (84.2)
Escherichia coli (1440) 360 315 (87.5) 360 306 (85.0) 360 247 (68.6) 360 147 (40.8)

A = Total number of meat sampled
N = Number of samples tested
n = Number of isolates
Where % = Number of isolates (n) / number of samples per meat type (N)
Dashes indicate no positive isolates.
Gray area indicates not tested.

20

Table 5. Trends in Antimicrobial Resistance among Salmonella by Meat Type, 2002-20091
Aminoglycosides
AMI
Meat Type

Chicken
Breast

Ground
Turkey

Ground
Beef

Pork
Chop

Year (N)
2002 (60)
2003 (83)
2004 (157)
2005 (153)
2006 (152)
2007 (99)
2008 (199)
2009 (277)
Z Statistic
3
P Value
2002 (74)
2003 (114)
2004 (142)
2005 (183)
2006 (159)
2007 (190)
2008 (245)
2009 (190)
Z Statistic
P Value
2002 (9)
2003 (10)
2004 (14)
2005 (8)
2006 (19)
2007 (13)
2008 (24)
2009 (14)
Z Statistic
P Value
2002 (10)
2003 (5)
2004 (11)
2005 (9)
2006 (8)
2007 (18)
2008 (23)
2009 (8)
Z Statistic
P Value

GEN

KAN

STR

(MIC ≥ 64) (MIC ≥ 16) (MIC ≥ 64) (MIC ≥ 64)

–
–
–
–
–
–
–
–
N/A4
N/A
–
–
–
–
–
–
–
–
N/A
N/A
–
–
–
–
–
–
–
–
N/A
N/A
–
–
–
–
–
–
–
–
N/A
N/A

10.0%
6.0%
3.8%
3.3%
9.2%
6.1%
7.0%
3.6%
0.7344
0.4627
14.9%
22.8%
20.4%
26.8%
28.9%
24.7%
27.8%
18.4%
-0.7436
0.4571
–
–
–
25.0%
–
7.7%
8.3%
14.3%
-1.5925
0.1113
30.0%
–
–
–
50.0%
5.6%
13.0%
–
0.7698
0.4414

6.7%
4.8%
11.5%
4.6%
9.9%
5.1%
10.6%
15.2%
-2.8960
0.0038
18.9%
27.2%
18.3%
20.2%
15.1%
23.7%
18.0%
6.8%
3.1403
0.0017
–
–
–
25.0%
5.3%
–
8.3%
14.3%
-1.4143
0.1573
10.0%
–
9.1%
–
25.0%
5.6%
–
12.5%
0.4114
0.6808

AMP

β-Lactamase Inhibitor
Combinations
AMC

(MIC ≥ 32)

(MIC ≥ 32)

(MIC ≥ 32) (MIC ≥ 4) (MIC ≥ 32) (MIC ≥ 512) (MIC ≥ 4)

16.7%
33.7%
30.6%
26.8%
22.4%
18.2%
29.2%
45.8%
-3.9729
<0.0001
16.2%
28.9%
20.4%
26.8%
25.8%
42.6%
50.6%
57.9%
-9.5415
<0.0001
22.2%
40.0%
21.4%
25.0%
10.5%
–
12.5%
28.6%
1.1473
0.2513
40.0%
40.0%
9.1%
22.2%
25.0%
5.6%
13.0%
37.5%
1.2488
0.2117

10.0%
25.3%
24.8%
21.6%
19.1%
16.2%
22.6%
37.2%
-3.8154
0.0001
12.2%
11.4%
7.7%
8.7%
5.0%
5.3%
5.3%
5.8%
2.7790
0.0055
22.2%
40.0%
14.3%
–
–
–
8.3%
14.3%
1.9680
0.0491
20.0%
20.0%
–
–
–
–
–
25.0%
1.0744
0.2827

10.0%
25.3%
24.8%
20.9%
19.1%
16.2%
22.6%
36.8%
-3.7823
0.0002
8.1%
2.6%
4.9%
7.1%
5.0%
5.3%
4.5%
5.8%
0.1584
0.8741
22.2%
40.0%
14.3%
–
–
–
8.3%
14.3%
1.9680
0.0491
20.0%
20.0%
–
–
–
–
–
25.0%
1.0744
0.2827

Penicillins

28.3%
26.5%
28.0%
30.1%
36.2%
30.3%
23.6%
23.1%
1.6064
0.1082
37.8%
45.6%
34.5%
44.3%
40.9%
45.8%
58.8%
27.9%
-0.6484
0.5167
22.2%
40.0%
14.3%
25.0%
10.5%
–
20.8%
28.6%
0.4633
0.6431
70.0%
40.0%
27.3%
33.3%
25.0%
16.7%
13.0%
37.5%
2.7069
0.0068

Cephems
TIO

AXO
10.0%
26.5%
24.8%
21.6%
19.1%
16.2%
22.6%
37.5%
-5.2988
<0.0001
8.1%
2.6%
5.6%
7.1%
5.0%
5.8%
4.5%
5.8%
0.2268
0.8206
22.2%
40.0%
14.3%
–
–
–
8.3%
14.3%
1.9680
0.0491
20.0%
20.0%
–
–
–
–
–
25.0%
1.0744
0.2827

FOX
10.0%
25.3%
24.8%
20.9%
18.4%
15.2%
21.6%
32.5%
-2.7345
0.0062
8.1%
2.6%
4.9%
7.1%
5.0%
5.3%
4.5%
5.8%
0.1584
0.8741
22.2%
40.0%
14.3%
–
–
–
8.3%
14.3%
1.9680
0.0491
20.0%
20.0%
–
–
–
–
–
25.0%
1.0744
0.2827

Folate Pathway
Inhibitors
COT
FIS2
16.7%
14.5%
28.7%
17.0%
23.0%
25.3%
39.2%
48.0%
-7.7961
<0.0001
20.3%
33.3%
28.2%
34.4%
32.1%
34.7%
27.4%
20.0%
1.3050
0.1919
22.2%
40.0%
14.3%
25.0%
10.5%
7.7%
20.8%
35.7%
0.0221
0.9823
70.0%
40.0%
18.2%
33.3%
75.0%
16.7%
30.4%
37.5%
1.5624
0.1182

–
–
–
–
1.3%
–
–
0.4%
-0.5376
0.5909
1.4%
–
–
0.5%
–
0.5%
0.4%
1.6%
-1.1119
0.2662
–
–
7.1%
–
–
–
–
–
0.9210
0.3571
20.0%
–
–
11.1%
50.0%
5.6%
–
25.0%
0.3396
0.7341

Phenicols
CHL
(MIC ≥ 512)

–
2.4%
1.9%
0.7%
2.6%
1.0%
0.5%
–
1.8103
0.0702
1.4%
0.9%
2.8%
0.5%
0.6%
1.6%
1.6%
1.6%
-0.2226
0.8238
22.2%
40.0%
14.3%
12.5%
5.3%
–
12.5%
21.4%
1.2510
0.2109
40.0%
40.0%
18.2%
22.2%
–
–
–
12.5%
3.7087
0.0002

Quinolones
CIP

NAL

(MIC ≥ 4) (MIC ≥ 32)

–
–
–
–
–
–
–
–
N/A
N/A
–
–
–
–
–
–
–
–
N/A
N/A
–
–
–
–
–
–
–
–
N/A
N/A
–
–
–
–
–
–
–
–
N/A
N/A

–
1.2%
–
0.7%
0.7%
–
–
0.4%
0.5126
0.6082
8.1%
4.4%
–
1.1%
–
2.6%
0.4%
–
3.9396
<0.0001
–
–
–
–
–
–
–
14.3%
-1.9480
0.0514
–
–
–
–
–
–
–
–
N/A
N/A

Tetracyclines
TET
(MIC ≥ 16)

33.3%
27.7%
46.5%
43.8%
46.7%
41.4%
46.7%
59.9%
-4.9733
<0.0001
55.4%
39.5%
56.3%
39.9%
56.0%
67.4%
66.1%
65.3%
-5.5360
<0.0001
22.2%
40.0%
14.3%
12.5%
21.1%
–
20.8%
42.9%
-0.2929
0.7696
70.0%
80.0%
54.5%
55.6%
25.0%
50.0%
34.8%
37.5%
2.2864
0.0222

1

Dashes indicate 0.0% resistance to antimicrobial. Where % resistance = (# isolates resistant to antimicrobial per meat type) / (total # isolates per meat type).
Sulfisoxazole replaced Sulfamethoxazole on NARMS panel in 2004.
3
P value for percent resistant trend was calculated using the Cochran-Armitage Trend Test method.
4
N/A = No Z statistic or P value could be calculated.
2

23

Table 8. Multidrug Resistance among Salmonella Isolates by Antimicrobial Class, 2002-20091
Year

2002

Number of Isolates
Tested by Source
2

Resistance Pattern
1. No Resistance
Detected

Chicken Breast
Ground Turkey
Ground Beef
Pork Chop

Chicken Breast
Ground Turkey

Pork Chop
Chicken Breast
Ground Turkey
Ground Beef
Pork Chop

3. Resistant to ≥ 4
Antimicrobial Classes

Chicken Breast
Ground Turkey
Ground Beef
Pork Chop

4. Resistant to ≥ 5
Antimicrobial Classes

Chicken Breast
Ground Turkey
Ground Beef
Pork Chop

5. Resistant to ≥ 6
Antimicrobial Classes

2006

2007

2008

2009

153
183
8
9

152
159
19
8

99
190
13
18

199
245
24
23

277
190
14
8

51.7%
31
37.8%
28
77.8%
7
20.0%
2
20.0%
12
20.3%
15
22.2%
2
60.0%
6
5.0%
3
13.5%
10
22.2%
2
40.0%
4
3.3%
2
12.2%
9
22.2%
2
40.0%
4

45.8%
38
34.2%
39
60.0%
6
20.0%
1
30.1%
25
29.0%
33
40.0%
4
40.0%
2
16.9%
14
24.6%
28
40.0%
4
40.0%
2
13.3%
11
14.0%
16
40.0%
4
40.0%
2
4.8%
4
3.5%
4
40.0%
4
40.0%
2

40.1%
63
28.9%
41
78.6%
11
45.5%
5
34.4%
54
26.1%
37
14.3%
2
18.2%
2
24.2%
38
12.7%
18
14.3%
2
18.2%
2
22.3%
35
4.9%
7
14.3%
2
9.1%
1
5.7%
9
2.8%
4
14.3%
2

46.4%
71
30.1%
55
75.0%
6
44.4%
4
25.5%
39
29.0%
53
25.0%
2
22.2%
2
18.3%
28
7.7%
14
12.5%
1
22.2%
2
17.7%
27
2.7%
5
12.5%
1
22.2%
2
3.9%
6
2.2%
4

38.8%
59
17.6%
28
73.7%
14
25.0%
2
24.3%
37
24.5%
39
10.5%
2
25.0%
2
15.1%
23
8.2%
13
5.3%
1
25.0%
2
14.5%
22
3.1%
5
5.3%
1

47.5%
47
15.3%
29
92.3%
12
44.4%
8
25.3%
25
42.6%
81

45.7%
91
20.8%
51
79.2%
19
65.2%
15
38.2%
76
51.0%
125
20.8%
5
17.4%
4
23.1%
46
15.1%
37
12.5%
3
13.0%
3
19.1%
38
2.9%
7
12.5%
3

–

29.4%
81
22.1%
42
57.1%
8
50.0%
4
48.4%
134
26.3%
50
35.7%
5
50.0%
4
34.7%
96
12.1%
23
35.7%
5
25.0%
2
31.4%
87
3.7%
7
14.3%
2
25.0%
2
11.2%
31
2.6%
5
14.3%
2
12.5%
1

–

Ground Turkey

10.8%
8
22.2%
2
20.0%
2

Pork Chop

2

2005

157
142
14
11

Chicken Breast

Ground Beef

1

2004

83
114
10
5

Isolate Source

Ground Beef

2. Resistant to ≥ 3
Antimicrobial Classes

2003

60
74
9
10

–2
5.6%
1
13.1%
13
14.7%
28
–
5.6%
1
12.1%
12
3.2%
6
–

–

–

–

5.9%
9
1.9%
3

4.0%
4
2.1%
4

–

–

–

4.0%
8
2.0%
5
8.3%
2

–

–

–

–

Dashes indicate 0.0% resistance.
Cephem class includes Cephalothin for 2002 and 2003.

30

Table 13. Trends in Antimicrobial Resistance among Campylobacter Species from Chicken Breast, 2002-20091
Aminoglycosides

Ketolides Lincosamides

Macrolides

Phenicols

Quinolones

Tetracyclines2

CLI
(MIC ≥ 8)

AZI
(MIC ≥ 8)

ERY
(MIC ≥ 32)

FFN3
(MIC > 4)

CIP
NAL
(MIC ≥ 4) (MIC ≥ 64)

TET
(MIC ≥ 16)

–

Not Tested

Not Tested

Not Tested

–

Not Tested

30 (15.2) Not Tested

76 (38.4)

2003 (325)

1 (0.3)

Not Tested

Not Tested

Not Tested

–

Not Tested

47 (14.5) Not Tested

132 (40.6)

2004 (510)
C. jejuni

Year (N)

TEL
(MIC ≥ 16)

2002 (198)

Species

GEN
(MIC ≥ 8)

–

2 (0.4)

2 (0.4)

4 (0.8)

4 (0.8)

–

77 (15.1)

77 (15.1)

256 (50.2)

–

2 (0.5)

2 (0.5)

2 (0.5)

2 (0.5)

–

61 (15.1)

60 (14.9)

187 (46.4)

2005 (403)
2006 (426)

n (%R4)

–

3 (0.7)

3 (0.7)

4 (0.9)

4 (0.9)

–

71 (16.7)

71 (16.7)

201 (47.2)

2007 (332)

–

2 (0.6)

2 (0.6)

2 (0.6)

2 (0.6)

–

57 (17.2)

57 (17.2)

161 (48.5)

2008 (329)

–

1 (0.3)

3 (0.9)

4 (1.2)

4 (1.2)

–

48 (14.6)

48 (14.6)

164 (49.8)

2009 (403)

–

1 (0.2)

2 (0.5)

4 (1.0)

4 (1.0)

–

85 (21.1)

85 (21.1)

186 (46.2)

Z Statistic

6

1.2403
0.2149

0.4375*
0.6617

-0.5290*
0.5968

-0.7058*
0.4803

-1.9629
0.0497

N/A
N/A

-2.1757
0.0296

-2.0382*
0.0415

-1.8933
0.0583

2002 (90)

–

Not Tested

Not Tested

Not Tested

7 (7.8)

Not Tested

9 (10.0)

Not Tested

40 (44.4)

2003 (142)

–

Not Tested

Not Tested

Not Tested

10 (7.0)

Not Tested

19 (13.4) Not Tested

72 (50.7)

2004 (196)

–

16 (18.2)

14 (7.1)

18 (9.2)

18 (9.2)

–

32 (16.3)

32 (16.3)

91 (46.4)

2005 (151)

–

12 (7.9)

13 (8.6)

15 (9.9)

15 (9.9)

–

44 (29.1)

44 (29.1)

64 (42.4)

–

7 (4.8)

7 (4.8)

8 (5.5)

8 (5.5)

–

32 (22.1)

30 (20.7)

68 (46.9)

1 (0.7)

10 (7.0)

7 (4.9)

9 (6.3)

9 (6.3)

–

37 (25.9)

37 (25.9)

57 (39.9)

2008 (181)

3 (1.7)

14 (7.7)

9 (5.0)

18 (9.9)

18 (9.9)

–

37 (20.4)

37 (20.4)

84 (46.4)

2009 (179)

10 (5.6)

8 (4.5)

6 (3.4)

8 (4.5)

8 (4.5)

–

33 (18.4)

33 (18.4)

68 (38.0)

Z Statistic

-4.8698
<0.0001

1.1070*
0.2683

2.0125*
0.0442

1.3466*
0.1781

0.8853
0.3760

N/A
N/A

-2.1215
0.0339

0.2090
0.8344

1.6998
0.0892

P Value

C. coli

5

2006 (145)

n (%R)

2007 (143)

P Value
1
2

Dashes indicate 0.0% resistance.
Results for 2002 and 2003 are for Doxycycline.

3

Percent non susceptible is reported rather than percent resistant as no CLSI breakpoint has been established. NARMS breakpoint established to determine resistance.
% R = the number of resistant isolates (n) / the number of positive isolates (N).
5
P value for percent resistant for trend was calculated using Cochran-Armitage trend test method.
6
N/A = Z Statistic and P value could not be calculated due to insufficient data or no resistance observed.
∗
Z statistic and P value calculated based on 6 years data.
4

42

Table 22. Trends in Antimicrobial Resistance among Escherichia coli by Meat Type, 2002-20091
Aminoglycosides
AMI
Meat Type

Chicken
Breast

Ground
Turkey

Ground
Beef

Pork
Chop

Year (N)
2002 (282)
2003 (396)
2004 (400)
2005 (393)
2006 (418)
2007 (299)
2008 (306)
2009 (315)
Z Statistic
4
P Value
2002 (304)
2003 (333)
2004 (376)
2005 (396)
2006 (388)
2007 (315)
2008 (300)
2009 (306)
Z Statistic
P Value
2002 (295)
2003 (311)
2004 (338)
2005 (316)
2006 (295)
2007 (256)
2008 (250)
2009 (247)
Z Statistic
P Value
2002 (184)
2003 (218)
2004 (232)
2005 (205)
2006 (182)
2007 (152)
2008 (146)
2009 (147)
Z Statistic
P Value

GEN

KAN

STR

(MIC ≥ 64) (MIC ≥ 16) (MIC ≥ 64) (MIC ≥ 64)

–
–
–
–
–
–
–
–
N/A3
N/A
–
–
–
–
–
–
–
–
N/A
N/A
–
–
–
–
–
–
–
–
N/A
N/A
–
–
–
–
–
–
–
–
N/A
N/A

23.1%
29.3%
30.0%
37.7%
37.3%
34.4%
34.0%
34.3%
-1.8718
0.0612
27.0%
29.7%
29.3%
27.5%
29.6%
27.0%
37.0%
37.9%
-3.1541
0.0016
0.3%
1.0%
0.6%
–
4.1%
–
2.0%
0.8%
-1.4761
0.1615
1.1%
1.4%
1.3%
–
1.1%
1.3%
1.4%
4.1%
-1.7338
0.0829

6.0%
6.8%
6.8%
7.1%
11.5%
9.0%
6.9%
5.4%
-0.4489
0.6535
13.2%
16.8%
16.0%
11.4%
14.7%
15.6%
19.0%
20.6%
-2.3795
0.0173
2.4%
2.9%
2.4%
0.6%
4.7%
1.6%
4.0%
2.0%
-0.4190
0.6752
5.4%
8.7%
8.2%
7.3%
6.0%
4.6%
6.2%
6.1%
0.8817
0.3779

AMP

β-Lactamase Inhibitor
Combinations
AMC

TIO

AXO

(MIC ≥ 32)

(MIC ≥ 32)

(MIC ≥ 32)

(MIC ≥ 4)

(MIC ≥ 32) (MIC ≥ 512) (MIC ≥ 4)

21.6%
25.3%
17.0%
24.7%
20.1%
18.1%
23.5%
22.2%
0.2597
0.7951
31.3%
35.7%
33.2%
38.1%
42.0%
48.3%
58.0%
56.2%
-9.2751
<0.0001
6.1%
5.1%
5.3%
3.5%
9.2%
6.6%
6.4%
4.9%
-0.4781
0.6326
13.6%
13.3%
15.1%
16.1%
15.9%
15.8%
15.1%
11.6%
-0.0126
0.9900

12.1%
13.6%
10.0%
12.2%
11.5%
7.4%
11.8%
13.3%
0.4139
0.6789
5.6%
3.0%
5.3%
3.8%
6.7%
6.3%
8.3%
9.8%
-3.6245
0.0003
2.0%
2.3%
3.9%
1.3%
2.4%
0.8%
2.4%
1.6%
0.9595
0.3373
5.4%
5.1%
5.6%
2.9%
2.2%
0.7%
3.4%
6.8%
0.9516
0.3413

7.1%
7.6%
5.8%
8.7%
8.6%
6.0%
10.8%
11.7%
-2.5399
0.0111
1.0%
0.3%
1.1%
1.8%
3.1%
6.0%
3.7%
6.2%
-5.8556
<0.0001
–
0.3%
0.9%
0.6%
1.0%
0.8%
1.6%
0.8%
-1.8333
0.0668
0.5%
0.9%
0.4%
–
–
0.7%
3.4%
6.8%
-4.5868
<0.0001

7.8%
9.1%
6.5%
10.2%
9.1%
6.4%
11.1%
12.4%
-1.9681
0.0491
1.3%
0.3%
1.3%
2.3%
3.1%
6.0%
3.7%
6.9%
-5.7139
<0.0001
–
0.3%
1.5%
1.9%
1.7%
0.8%
1.6%
0.8%
-1.2963
0.1949
0.5%
0.9%
0.4%
0.5%
0.6%
0.7%
3.4%
6.8%
-4.4349
<0.0001

11.0%
9.3%
8.3%
11.2%
11.2%
7.4%
11.8%
13.3%
-1.3229
0.1859
3.3%
1.2%
4.5%
3.3%
6.2%
6.3%
6.3%
7.8%
-4.2615
<0.0001
1.4%
0.3%
1.2%
1.0%
2.0%
0.8%
2.4%
1.6%
-1.3887
0.1649
3.3%
2.3%
2.2%
1.5%
1.6%
0.7%
3.4%
6.8%
-1.4454
0.1483

Penicillins

49.3%
56.1%
56.8%
50.6%
48.1%
46.8%
43.8%
38.1%
5.0655
<0.0001
57.6%
54.7%
49.2%
43.4%
43.8%
44.8%
57.3%
57.5%
0.0369
0.9705
9.5%
9.0%
11.8%
5.4%
14.2%
6.3%
10.4%
8.1%
0.4405
0.6596
22.3%
19.7%
21.1%
13.2%
13.7%
13.8%
19.9%
19.7%
1.2484
0.2119

Cephems
FOX

Folate Pathway
Inhibitors
COT
FIS2

32.3%
38.4%
41.3%
48.1%
46.9%
42.1%
39.2%
40.6%
-1.7099
0.0873
48.0%
51.7%
48.4%
48.0%
48.5%
48.9%
51.0%
53.9%
-1.0620
0.2882
9.8%
10.3%
13.0%
7.0%
12.5%
9.4%
11.6%
7.7%
0.5706
0.5683
12.5%
15.1%
19.4%
14.2%
20.3%
11.8%
16.4%
14.3%
-0.1036
0.9175

3.6%
7.1%
4.3%
7.4%
8.9%
5.0%
3.6%
2.2%
1.4534
0.1461
4.0%
6.9%
3.7%
5.1%
8.0%
7.9%
5.3%
5.9%
-1.3181
0.1874
0.7%
0.3%
0.6%
0.6%
1.4%
1.2%
2.0%
2.0%
-2.5432
0.0110
1.1%
2.8%
3.9%
1.5%
2.2%
1.3%
6.2%
2.7%
-1.1923
0.2332

CHL

CIP

NAL

Tetracyclines
TET

(MIC ≥ 512)

(MIC ≥ 4)

(MIC ≥ 32)

(MIC ≥ 16)

0.7%
–
1.8%
0.5%
2.6%
2.0%
1.0%
0.6%
-1.0737
0.2830
0.3%
3.6%
0.8%
4.0%
2.3%
2.9%
3.7%
3.3%
-2.1290
0.0333
1.0%
2.3%
3.6%
1.6%
1.4%
3.9%
0.8%
2.4%
-0.2672
0.7893
1.6%
4.1%
4.3%
3.4%
6.6%
3.9%
3.4%
4.8%
-1.0975
0.2724

–
–
–
–
–
–
–
0.3%
-1.6400
0.1010
–
0.3%
0.8%
–
0.5%
0.3%
–
0.7%
-0.4651
0.6419
–
–
–
–
–
–
–
–
N/A
N/A
–
–
–
–
–
–
–
–
N/A
N/A

2.8%
4.0%
7.0%
6.6%
5.0%
3.0%
2.9%
2.9%
1.4100
0.1585
4.3%
11.7%
10.6%
10.4%
5.2%
2.2%
3.7%
2.6%
4.7865
<0.0001
–
1.0%
1.5%
1.3%
0.7%
0.4%
0.4%
0.4%
0.5612
0.5747
0.5%
0.5%
–
1.5%
0.5%
–
–
–
0.9618
0.3362

46.1%
42.9%
48.0%
46.6%
50.5%
40.5%
43.8%
41.6%
1.1513
0.2496
77.0%
77.8%
74.2%
78.0%
76.5%
80.0%
85.7%
82.0%
-3.0311
0.0024
30.9%
25.1%
22.8%
16.5%
25.4%
21.9%
24.0%
18.6%
2.5861
0.0097
52.7%
46.3%
56.0%
45.9%
52.7%
50.0%
54.8%
46.9%
0.1653
0.8687

Phenicols

Quinolones

1

Dashes indicate 0.0% resistance to antimicrobial. Where % resistance = (# isolates resistant to antimicrobial per meat type) / (total # isolates per meat type).
Sulfisoxazole replaced Sulfamethoxazole on the NARMS panel in 2004.
3
N/A = No Z statistic or P value could be calculated.
4
P value for percent resistant trend was calculated using the Cochran-Armitage Trend Test method.
2

64

1

Table 24. Multidrug Resistance among Escherichia coli Isolates by Antimicrobial Class, 2002-2009
Year

2002

Number of Isolates
Tested by Source
2

Resistance Pattern
1. No Resistance
Detected

Chicken Breast
Ground Turkey
Ground Beef
Pork Chop

Chicken Breast

Ground Beef
Pork Chop
Chicken Breast
Ground Turkey
Ground Beef
Pork Chop
3. Resistance to ≥ 4
Antimicrobial Classes

Chicken Breast
Ground Turkey
Ground Beef
Pork Chop

4. Resistance to ≥ 5
Antimicrobial Classes

Chicken Breast
Ground Turkey
Ground Beef
Pork Chop

5. Resistance to ≥ 6
Antimicrobial Classes

Chicken Breast
Ground Turkey
Ground Beef
Pork Chop

1
2

2004

2005

2006

2007

2008

2009

396
333
311
218

400
376
338
232

393
396
316
205

418
388
295
182

299
315
256
152

306
300
250
146

315
306
247
147

27.0%
76
16.8%
51
63.1%
186
41.3%
76

20.5%
81
14.7%
49
66.9%
208
44.5%
97

20.8%
83
19.1%
72
73.1%
247
37.9%
88

20.6%
81
16.2%
64
80.4%
254
48.8%
100

23.7%
99
16.0%
62
71.5%
211
42.9%
78

29.1%
87
13.0%
41
77.0%
197
48.0%
73

33.3%
102
8.3%
25
73.2%
183
43.8%
64

34.3%
108
11.8%
36
78.1%
193
51.0%
75

36.2%
102
55.6%
169
10.2%
30
17.4%
32

42.2%
167
55.6%
185
7.4%
23
17.9%
39

35.3%
141
51.9%
195
10.4%
35
21.1%
49

45.0%
177
52.8%
209
5.4%
17
16.1%
33

43.3%
181
55.2%
214
11.5%
34
15.9%
29

33.8%
101
57.5%
181
9.0%
23
15.1%
23

36.6%
112
63.7%
191
11.2%
28
17.8%
26

37.5%
118
66.3%
203
6.9%
17
15.0%
22

13.8%
39
23.0%
70
1.7%
5
5.4%
10

13.6%
54
30.0%
100
4.2%
13
6.9%
15

12.5%
50
24.5%
92
4.7%
16
7.8%
18

12.2%
48
24.2%
96
1.9%
6
4.9%
10

14.6%
61
25.8%
100
5.8%
17
7.7%
14

10.4%
31
27.0%
85
4.7%
12
3.3%
5

13.7%
42
32.3%
97
4.4%
11
7.5%
11

13.7%
43
38.9%
119
3.6%
9
10.9%
16

6.0%
17
9.2%
28
0.3%
1
3.3%
6

7.3%
29
14.7%
49
2.6%
8
2.8%
6

6.0%
24
6.9%
26
2.7%
9
2.2%
5

5.9%
23
6.3%
25
1.0%
3
1.5%
3

7.4%
31
5.7%
22
2.4%
7
3.3%
6

5.7%
17
4.1%
13
0.4%
1
1.3%
2

8.2%
25
6.3%
19
2.0%
5
4.1%
6

6.3%
20
7.8%
24
1.2%
3
5.4%
8

3.9%
11
2.6%
8
0.3%
1
1.6%
3

3.5%
14
4.2%
14
1.3%
4
1.8%
4

3.3%
13
3.2%
12
2.1%
7
0.4%
1

3.6%
14
1.8%
7
0.6%
2
0.5%
1

5.3%
22
3.1%
12
1.7%
5
1.1%
2

3.3%
10
2.9%
9

6.2%
19
4.0%
12
1.6%
4
2.1%
3

4.4%
14
3.6%
11
0.4%
1
4.1%
6

Isolate Source

Ground Turkey

2. Resistance to ≥ 3
Antimicrobial Classes

2003

282
304
295
184

–2
0.7%
1

Dashes indicate 0.0% resistance.
Cephem class includes Cephalothin for 2002 and 2003.

70