1 

FSIS National Antimicrobial Resistance Monitoring System Cecal

Sampling Program, 2014 Salmonella Report

• Summary

• Key Findings

• Introduction

• Results

• Resistance by Slaughter Class

• Resistance by Salmonella Serotype

• Resistance Profiles

• Resistance in Serotypes Associated with Human Illness

• Extremely Resistant Salmonella Isolates

• Conclusion

• Appendix

Summary

The Food Safety and Inspection Service isolates bacteria from the ceca (beginning of the large intestine) 

of swine (market swine and sows), cattle (heifers, steers, beef cows, and dairy cows), and poultry (young 

chickens and young turkeys) for the presence of Salmonella spp., Campylobacter spp., generic 

Escherichia coli, and Enterococcus spp. This is a descriptive report of antimicrobial resistance results for 

Salmonella during calendar year 2014, the first full year of cecal sampling. This report complements the 

findings described in the 2014 NARMS Integrated Report. The isolate level data described in this report 

are available on the Food and Drug Administration (FDA) NARMS website. Additional information on the 

food animal component of NARMS can be found on the on the FSIS NARMS web page. 

Key Findings

Overview

• In 2014, Salmonella was isolated from 21.5% (1,077/5,001) of cecal samples

• Sixty six percent of the Salmonella isolates were pansusceptible (i.e. not resistant to any

antimicrobial drug tested).

• Thirteen percent of the Salmonella isolates were multidrug resistant (MDR) (i.e. resistant to 3 or

more antimicrobial classes).

• Less than 5% of the Salmonella isolates were resistant to each of the antimicrobial drugs

classified by FDA as critically important for human clinical use.

• Among antimicrobial drugs classified by FDA as highly important, tetracycline (28.8%) and

streptomycin (17.9%) had the highest percentage of resistance among the Salmonella isolates.

• Looking at Salmonella serotypes, a notably high proportion of resistant and MDR isolates was

found for Salmonella I 4,[5],12:i:- (89.5% resistant; 68.4% MDR) and Salmonella Typhimurium

(85.5%; 51.6%).
2 

By Commodity

Poultry

• The highest proportion of resistant Salmonella isolates was identified in turkey (76%). 

• The highest proportion of resistant Salmonella Typhimurium isolates was obtained from chicken

(49%). 

• All ten Salmonella Heidelberg isolates were obtained from poultry with seven pansusceptible 

chicken isolates and three MDR turkey isolates.

Swine (Market Swine, Sows)

• All Salmonella I 4,[5],12:i:- isolates (nine isolates) from market swine were resistant to at least 

one antimicrobial drug with 89% having the ampicillin/streptomycin/sulfonamide/tetracycline 

(ASSuT) resistance profile. Half of the sow Salmonella I 4,[5],12:i:- isolates (10 isolates) exhibited 

this resistance profile. In some cases, these isolates were resistant to other antimicrobial drugs 

in addition to ASSuT.

Cattle (Dairy Cow, Beef Cow, Steers, Heifer)

• Nineteen percent of all cattle isolates were resistant to at least one antimicrobial drug. 

• The two most common serotypes among cattle isolates were Salmonella Newport and 

Salmonella Typhimurium. At least half of the cattle isolates for these serotypes exhibited 

resistance (50% and 71%, respectively) and all resistant isolates were MDR.

Introduction

Antimicrobial drugs are used in food-producing animals to prevent illness, treat disease, and limit the 

spread of infection already present in a herd or flock. Animal exposure to antimicrobial drugs can 

promote selection for resistant subpopulations of bacteria that can spread to other animals, the 

environment and humans. FSIS has made it a priority to track changes in antibiotic susceptibility of meat 

and poultry products to reduce the potential of human exposure to harmful resistant pathogens. 

FSIS collects data for the animal arm of NARMS through two programs including: the Pathogen 

Reduction/Hazard Analysis and Critical Control Point (PR/HACCP) verification program and the cecal 

sample program. For PR/HACCP verification sampling, select classes of livestock carcasses (cow/bulls, 

steers/heifers, market hogs, broilers) and raw ground/comminuted product (beef, chicken, and turkey) 

are sampled from federally inspected slaughter and processing plants throughout the United States.1

Carcass samples consist of swabs (beef, turkey, hogs), or rinsates (chicken), and raw 

ground/comminuted product samples collected during processing, wherein in-plant antimicrobial 

interventions may have been applied to reduce bacterial loads either during slaughter or further

processing, or a combination of both. While this approach allows NARMS surveillance to be efficiently 

and economically coupled with FSIS PR/HACCP verification sampling, the historical sampling design 

(risk-based sample collection from 2006-2015) and varying types of product classes targeted under 

 

1 Of note, FSIS suspended scheduling cows/bulls from sampling in 2011 and market hogs, steer, and heifers in 2012 

because of the low number of positive samples.
3

PR/HACCP sampling presented important limitations to analyzing trends and drawing conclusions about 

the occurrence of antibiotic resistance in food animals. In 2014, FSIS began to move from a risk-based 

sampling approach to routine sampling of all establishments that produce commodities included in the 

PR/HACCP verification programs (81 FR at 7285; February 11, 2016). This change enables the Agency to 

better evaluate prevalence and contamination trends over time in these commodities. 

The World Health Organization (WHO) recommends that if on-farm sampling is not possible, samples 

from healthy animals at slaughter may be used to estimate bacterial resistance in food animals.2 Cecal 

samples collected immediately after slaughter may reflect microbial characteristics prior to the 

application of in-plant processing interventions, making them better indicators of pre-harvest 

antimicrobial resistance. Microbiota in the animal cecum also may be affected by the time spent in 

transport and in holding pens prior to slaughter. Therefore, sampling results may reflect gut colonization 

by microorganisms present in these environments.

Since March 2013, FSIS’s cecal sampling has provided a means for monitoring antimicrobial resistance in 

intestinal (cecal) bacteria at slaughter from four food animal species (chickens, turkeys, swine, and 

cattle) and associated slaughter classes (young chicken, young turkey, beef cow, dairy cow, steer, and 

heifer, market swine and sow). In contrast to historical PR/HACCP verification sampling , cecal sampling 

is routinely conducted using a statistical model based on establishment production volume and provides

more nationally representative data on antimicrobial susceptibility among four targeted bacteria 

(Salmonella, Campylobacter, Escherichia coli and Enterococcus)

3 prior to slaughter. 

Salmonella isolates described in this report were recovered by FSIS from cecal samples collected in 

CY2014 as described in FSIS Directive 10,100.1. As with other data collected for NARMS, data generated 

from cecal samples may: facilitate detection of trends in antimicrobial resistance or emerging 

antimicrobial resistance profiles of concern from food animals in the United States; support the 

identification of mitigation steps to limit the spread of resistance to antimicrobial drugs classified as 

critically important; improve the scientific basis for food animal antibiotic use policies and regulations;

and enable risk analysis of foodborne antimicrobial resistant hazards when evaluating a new animal 

antibiotic for safety.

4

The following descriptions of resistance are used in the results section of this report. Pansusceptible 

isolates are susceptible to all antimicrobial drugs included in the NARMS testing panel. Multidrug 

resistance (MDR) is reported as resistance to three or more of the nine antimicrobial classes included in 

the NARMS testing panel. Isolates that are resistant to all or all but one of these classes are considered 

extremely drug resistant (XDR).5 Bacteria that are classified as XDR are epidemiologically significant not 

 2 World Health Organization (2017). Integrated surveillance of antimicrobial resistance: guidance from a WHO 

Advisory Group. Retrieved from: http://apps.who.int/iris/bitstream/10665/255747/1/9789241512411-

eng.pdf?ua=1. 3 CDC, FDA, FSIS (2016). NARMS Integrated Report, 2014. Retrieved from 

http://www.fda.gov/downloads/AnimalVeterinary/SafetyHealth/AntimicrobialResistance/NationalAntimicrobialRe

sistanceMonitoringSystem/UCM528861.pdf. 4 FDA, Antimicrobial Resistance, About NARMS, updated 11/18/2016. Retrieved from: 

http://www.fda.gov/AnimalVeterinary/SafetyHealth/AntimicrobialResistance/ucm059089.htm#Data_usage

5 CDC, FDA, FSIS (2016). NARMS Integrated Report, 2014. Retrieved from 

http://www.fda.gov/downloads/AnimalVeterinary/SafetyHealth/AntimicrobialResistance/NationalAntimicrobialRe

sistanceMonitoringSystem/UCM528861.pdf.
4 

only because of resistance to multiple antimicrobial drugs, but also because of the likelihood of being 

resistant to all, or almost all, clinically approved antimicrobial drugs. 

Results

Resistance by Slaughter Class

Salmonella was isolated from 21.5% (1,077/5,001) of samples, with percent positive ranging within the 

slaughter classes from 2.8% (15/540) in beef cows to 58.1% (328/565) in sows. All isolates were analyzed 

for antimicrobial resistance and 65.6% (707/1,077) exhibited no resistance, while 34.4% (370/1,077) 

were resistant to one or more antimicrobial drugs, and 13.4% (144/1,077) were MDR. XDR was found in 

0.4% (4/1,077) isolates. Figure 1 shows the percentage of cecal samples that were positive for 

Salmonella for each slaughter class. 

Figure 1. Percent cecal samples (N = 5,001 total samples) Salmonella positive, by production class, 2014.
5 

Figure 2 represents the Salmonella isolates by resistance (pansusceptible, resistant to 1-2 antimicrobial 

drug classes, or MDR) within each slaughter class. The highest proportion of resistant isolates was 

identified in turkey (75.6% [34/45] resistant), followed by chicken (53.4% [55/103]), swine (36.0% 

[219/608]), and cattle (19.3% [62/321]). MDR isolates were identified in less than 20% of isolates in all 

slaughter classes except for turkeys (46.7% [21/45]) and market swine (20.7% [58/280]).

Figure 2. Percent cecal Salmonella isolates (n = 1,077 total isolates) pansusceptible, resistant, and MDR, 

within each production class, 2014.

Resistance by Salmonella Serotype

Salmonella serotypes varied by slaughter class. Table 1 summarizes the top 10 serotypes from all 

classes, the proportion of isolates resistant to at least one antimicrobial drug, the proportion of isolates 

that are MDR, and the slaughter class with the most isolates for each serotype. For the following top 10

serotypes, over 75% of isolates were exclusive to one species: Salmonella Cerro (84.4% [76/90] from 

cattle), Salmonella Derby (96.1% [75/78] from swine), Salmonella Johannesburg (97.2% [70/72] from 

swine), Salmonella Infantis (95.1% [58/61] swine), and Salmonella Montevideo (86.7% [52/60] from 

cattle). 
6

Table 1. Top 10 Salmonella serotypes isolated from cecal samples (serotype totals highlighted in grey).

Serotype

No. of isolates

(% total 

isolates§)

No. of resistant 

isolates* (% 

serotype isolates)

No. of MDR isolates

(% serotype isolates)

Primary slaughter class of 

serotype (# of isolates, % 

of serotype)

Anatum 142 (13.2%) 58 (40.8%) 0 (0.0%) Sows (68, 47.9%)

Cerro 90 (8.4%) 5 (5.6%) 0 (0.0%) Dairy (70, 77.8%)

Derby 78 (7.2%) 52 (66.7%) 30 (38.5%) Market Swine (49, 62.8%)

Johannesburg 72 (6.7%) 9 (12.5%) 2 (2.8%) Sows (42, 58.3%)

Typhimurium 62 (5.8%) 53 (85.5%) 32 (51.6%) Chicken (27, 43.5%)

Infantis 61 (5.7%) 3 (4.9%) 2 (3.3%) Sows (36, 59.0%)

Montevideo 60 (5.6%) 10 (16.7%) 2 (3.3%) Dairy (38, 63.3%)

Agona 50 (4.6%) 24 (48.0%) 13 (26.0%) Market Swine (17, 34.0%)

Kentucky 41 (3.8%) 25 (61.0%) 6 (14.6%) Chicken (27, 65.9%)

Muenchen 23 (2.1%) 12 (52.2%) 0 (0.0%) Sows (9, 39.1%)

§

Total isolates: n = 1,077; *Includes MDR isolates

Table 2 shows the Salmonella serotypes with the highest proportion of isolates exhibiting resistance to 

at least one antimicrobial drug. The table includes the percentage of all isolates, percentage of resistant

isolates, percentage of MDR isolates, and the slaughter class where the majority of each serotype was 

identified. The serotypes with higher proportions of resistant isolates include some serotypes that were 

less common overall. Serotypes with a high proportion of resistance in general and MDR included

Salmonella I 4,[5],12:i:- (89.5% [17/19] resistant; 68.4% [13/19] MDR) and Salmonella Typhimurium 

(85.5% [53/62]; 51.6% [32/62]).

Table 2. Salmonella serotypes with highest proportion of resistant isolates (serotypes with ≥ 10 

isolates) (resistant isolate totals highlighted in grey).

Serotype

No. of isolates

(% total 

isolates§)

No. of resistant 

isolates* (% 

serotype isolates)

No. of MDR isolates 

(% serotype isolates)

Primary slaughter class of 

serotype (# of isolates, % 

of serotype)

Hadar 11 (1.0%) 10 (90.9%) 4 (36.4%) Turkey (7, 63.6%)

I 4,[5],12:i:- 19 (1.8%) 17 (89.5%) 13 (68.4%) Sows (10, 52.6%)

Typhimurium 62 (5.8%) 53 (85.5%) 32 (51.6%) Chicken (27, 43.5%)

Schwarzengrund 17 (1.6%) 12 (70.6%) 3 (17.7%) Chicken (8, 47.1%)

Derby 78 (7.2%) 52 (66.7%) 29 (37.2%) Market Swine (49, 62.8%)

Kentucky 41 (3.8%) 25 (61.0%) 6 (14.6%) Chicken (27, 65.9%)

Muenchen 23 (2.1%) 12 (52.2%) 0 (0.0%) Sows (9, 39.1%)

Agona 50 (4.6%) 24 (48.0%) 13 (26.0%) Market Swine (17, 34.0%)

Newport 22 (2.0%) 10 (45.5%) 9 (40.9%) Dairy (15, 68.2%)

Reading 14 (1.3%) 6 (42.9%) 3 (21.4%) Turkey (6, 42.9%)

§

Total isolates: n = 1,077; *Includes MDR isolates

Table 3 shows the Salmonella serotypes with the highest proportion of isolates exhibiting MDR. Only 

two serotypes had the majority of isolates identified as MDR: Salmonella I 4,[5],12:i:- and Salmonella

Typhimurium (68.4% and 51.6% MDR, respectively).
7 

Table 3. Salmonella serotypes with highest proportion of MDR isolates (serotypes with ≥ 10 isolates)

(MDR isolate totals highlighted in grey).

Serotype

No. of isolates

(% total 

isolates§)

No. of resistant 

isolates* (% 

serotype isolates)

No. of MDR isolates

(% serotype isolates)

Primary slaughter class of 

serotype (# of isolates, % of 

serotype)

I 4,[5],12:i:- 19 (1.8%) 17 (89.4%) 13 (68.4%) Sows (10, 52.6%)

Typhimurium 62 (5.8%) 53 (85.5%) 32 (51.6%) Chicken (27, 43.5%)

Newport 22 (2.0%) 10 (45.5%) 9 (40.9%) Dairy (15, 68.2%)

Derby 78 (7.2%) 52 (66.7%) 30 (38.5%) Market Swine (49, 62.8%)

Hadar 11 (1.0%) 10 (90.9%) 4 (36.4%) Turkey (7, 63.6%)

Heidelberg 10 (0.9%) 3 (30.0%) 3 (30.0%) Chicken (7, 70.0%)

Agona 50 (4.6%) 24 (48.0%) 13 (26.0%) Market Swine (17, 34.0%)

Reading 14 (1.3%) 6 (42.9%) 3 (21.4%) Turkey (6, 42.9%)

Saintpaul 22 (2.0%) 8 (36.4%) 4 (18.2%) Market Swine (9, 40.9%)

Schwarzengrund 17 (1.6%) 12 (70.6%) 3 (17.6%) Chicken (8, 47.1%)

§

Total isolates: n = 1,077; *Includes MDR isolates

Salmonella serotypes identified among cecal isolates from each slaughter class varied. For example, the 

majority of chicken isolates were one of two serotypes, Salmonella Typhimurium or Salmonella

Kentucky (both 26.2% [27/103]), while market swine and sow isolates showed greater diversity. 

Salmonella Typhimurium and Salmonella Kentucky isolates from chicken were often resistant (74.1% 

[20/27] and 96.3% [26/27], respectively), but less often MDR (18.5% [5/27] and 29.6% [8/27]). For dairy 

cattle, only two common serotypes (with ≥ 10 isolates) exhibited resistance in a majority of isolates: 

Salmonella Newport and Salmonella Typhimurium (53.3% [8/15] and 90.0% [9/10] MDR, respectively). 

Salmonella Resistance Profiles

All Salmonella isolates with resistance (34.4% [370/1,077]) were resistant to one or more of the 

antimicrobial drugs classified by FDA as highly important or critically important. Figure 3 shows the 

percentage of isolates resistant to each antimicrobial drug. In some cases, a single isolate was resistant 

to more than one of these drugs and is counted more than once in the figure. Streptomycin (17.9% 

[193/1,077]) and tetracycline (28.8% [310/1,077]) were the only antimicrobial drugs classified as highly 

important to which more than 10% of all isolates exhibited resistance. Resistance to each of the 

antimicrobial drugs classified as critically important was less than 5%. Less than 1% of isolates were 

resistant to azithromycin (0.6% [7/1,077]). Table 4 shows the cecal Salmonella serotypes most 

frequently isolated with resistance to each highly important or critically important antimicrobial drugs. 
8

Figure 3. Percent of cecal Salmonella isolates (n = 1,077) resistant to each of the highly important and 

critically important antimicrobial drugs, 2014. Note that of the 370 isolates represented in this figure, 

220 were resistant to more than one of these drugs and thus are counted more than once.

Table 4. Salmonella serotypes resistant to highly important and critically important antimicrobial drugs.

Antimicrobial

drug

Number of 

resistant isolates

Most common serotype (# 

resistant, % of resistant isolates)

Second most common serotype (# 

resistant, % of resistant isolates)

TIO 41 Typhimurium (11, 26.8%) Newport (9, 22.0%)

AXO 43 Typhimurium (11, 25.6%) Newport (9, 20.9%)

CIP 26 Muenchen (9, 34.6%) Anatum (6, 23.1%)

AZI 7 Typhimurium (2, 28.6%)

Agona, Brandenburg, Heidelberg, 

Montevideo, Schwarzengrund (1

isolate each, 14.3% each)

COT 16 Agona (3, 18.8%) Kentucky, Senftenberg (2 isolates 

each, 12.5% each)

GEN 32 Schwarzengrund, Senftenberg (5

isolates each, 15.6% each)

Saintpaul, Typhimurium (4 isolates 

each, 12.5% each)

STR 193 Derby (33, 17.1%) Typhimurium (28, 14.5%)

AMP 94 Typhimurium (26, 27.7%) I 4,[5],12:i:- (13, 13.8%)

AMC 41 Typhimurium (11, 26.8%) Newport (9, 22.0%)

CHL 39 Typhimurium (16, 41.0%) Newport (9, 23.1%)

TET 310 Anatum (56, 18.1%) Derby, Typhimurium (49 isolates each, 

15.8% each)

Figure 4 shows the serotypes identified as exhibiting resistance profiles that are of public health concern

to FSIS. These resistance profiles are listed in Appendix Table 4. They are of interest in part because they 

indicate multidrug resistance, often to multiple critically important or highly important antimicrobial 

drugs. Some have not been previously seen frequently in the United States, however others such as 

ACSSuT and ASSuT have been historically associated with Salmonella Typhimurium DT104 and 

Salmonella I 4,[5],12:i:- respectively. For several of these profiles, the highest proportion of isolates was 

in one or two serotypes. The majority of isolates with ASSuT resistance are Salmonella I 4,[5],12:i:-

(54.2% [13/24]), while the majority of isolates with ACSSuT resistance were Salmonella Typhimurium

(44.1% [15/34]) or Salmonella Newport (26.5% [9/34]). In some cases, the resistance profile of a single 
9 

isolate contained more than one MDR profile of concern, and is counted more than once. 

Figure 4. Salmonella resistance profiles of public health concern (n = 1,077) by serotype, 2014*. 

Similar data are presented in Figure 5, except by slaughter class. Beef cattle and steers each had only 

one cecal isolate with the ASSuT resistance profile, and no cecal isolates from heifers exhibited 

resistance to any of the profiles of public health concern. Market swine and dairy cow cecal samples

made up the highest proportion of isolates with any of the resistance profiles of concern (35.5% [27/76]

and 25.0% [19/76] of the isolates described here, respectively). 

Figure 5. Salmonella resistance profiles of public health concern (n = 1,077) by slaughter class, 2014*. 

Resistance in Salmonella Serotypes Associated with Human Illness

During 2011-2014, Salmonella Enteritidis, Salmonella Heidelberg, Salmonella I 4,[5],12:i:-, Salmonella

Typhimurium, Salmonella Infantis, and Salmonella Newport were serotypes that were associated with 
10

FSIS foodborne illness investigations. A review of these serotypes found that 89.5% (17/19) of 

Salmonella Enteritidis isolates were from chicken and all were pansusceptible. All Salmonella Heidelberg 

isolates (n = 10) were isolated from poultry. Seven of ten (70%) were from chicken and all were 

pansusceptible. The remaining three (30%) were from turkey and were MDR.

The three turkey Salmonella Heidelberg isolates exhibited resistance to the following antimicrobial drug 

classes: 

1. ß-lactam/ß-lactamase inhibitor combinations (AMC), penicillins (AMP), cephems (FOX, TIO, 

AXO), folate pathway inhibitors (FIS), and tetracyclines (TET)

2. ß-lactam/ß-lactamase inhibitor combinations (AMC), penicillins (AMP), cephems (FOX, TIO, 

AXO), aminoglycosides (GEN, STR), and folate pathway inhibitors (FIS)

3. Macrolides (AZI), ß-lactam/ß-lactamase inhibitor combinations (AMC), penicillins (AMP), 

cephems (FOX, TIO, AXO), phenicols (CHL), aminoglycosides (GEN, STR), folate pathway 

inhibitors (FIS, COT), and tetracyclines (TET).

Salmonella I 4,[5],12:i:- isolates were recovered from both swine slaughter classes. All market swine 

Salmonella I 4,[5]12:i:- isolates were resistant to at least one antimicrobial drug, and most were MDR 

with the ASSuT profile (88.9% [8/9]) (some isolates were resistant to additional antimicrobial drugs as 

well). In contrast, 50.0% (5/10) of sow Salmonella I 4,[5],12:i:- isolates were resistant to antimicrobial 

drugs included in the ASSuT profile.

Salmonella Typhimurium isolates were identified across all slaughter classes (Figure 6) with a high 

proportion of isolates resistant or MDR (85.5% [53/62] and 51.6% [32/62], respectively). Heifers and 

steers were the only slaughter classes where all Salmonella Typhimurium isolates were pansusceptible. 

Chicken, market swine, and dairy cows accounted for a majority of resistant isolates (49.1% [26/53], 

18.9% [10/53], and 17.0% [9/53], respectively).

Figure 6. Resistance profiles found in Salmonella Typhimurium isolates by product class, 2014.

Salmonella Infantis was isolated from chicken, market swine, sows, and dairy cow cecal samples. Only 

4.9% (3/61) of Salmonella Infantis isolates exhibited resistance and all were from market swine. The 
11

resistance profiles for market swine identified were: FIS TET (one isolate) and AMP STR TET (two 

isolates). 

Salmonella Newport was recovered primarily from market swine and dairy cow cecal samples. Eight of 

15 (53.3%) Salmonella Newport isolates from dairy cow samples exhibited MDR, all with the 

ACSSuTAuCx resistance profile plus resistance to two additional cephems (FOX, TIO). Two of five (40.0%) 

market swine Salmonella Newport isolates were resistant; one with the MDR profile found in dairy 

cattle isolates and one resistant to tetracycline. The remaining Salmonella Newport isolates from dairy 

cattle and market swine isolates were pansusceptible.

Additionally, Salmonella Dublin is a serotype of concern that appears to have increasing resistance to 

ceftriaxone in clinical, PR/HACCP ground beef and retail ground beef isolates.6 Yet in 2014, only one 

Salmonella Dublin isolate was recovered from FSIS cecal sampling; this isolate was pansusceptible.

Extremely Resistant Salmonella Isolates

Only 4/1,077 (0.4%) of isolates exhibited an XDR resistance profile. These isolates and their resistance 

are as follows:

• Market swine Salmonella Agona isolate and turkey Salmonella Heidelberg isolate: Macrolides 

(AZI), ß-lactam/ß-lactamase inhibitor combinations (AMC), penicillins (AMP), cephems (FOX, TIO, 

AXO), phenicols (CHL), aminoglycosides (GEN, STR), folate pathway inhibitors (FIS, COT), and 

tetracyclines (TET)

• Dairy cow Salmonella Montevideo isolate: Macrolides (AZI), ß-lactam/ß-lactamase inhibitor 

combinations (AMC), penicillins (AMP), cephems (FOX, TIO, AXO), phenicols (CHL), 

aminoglycosides (STR), folate pathway inhibitors (FIS, COT), and tetracyclines (TET)

• Dairy cow Salmonella Typhimurium isolate: ß-lactam/ß-lactamase inhibitor combinations (AMC), 

penicillins (AMP), cephems (FOX, TIO, AXO), phenicols (CHL), quinolones (CIP), aminoglycosides 

(STR), folate pathway inhibitors (FIS), and tetracyclines (TET)

Conclusion

Cecal sampling represents a major addition to NARMS and has resulted, for the first time, in a random 

and nationally representative sampling of antimicrobial susceptibility of all bacteria targeted by NARMS, 

within all four major food animal species. The cecal sampling program establishes representative 

sampling that reflects microbial characteristics prior to the application of in-plant processing 

interventions, and that may serve as indicators of pre-harvest antimicrobial resistance. FSIS PR/HACCP 

regulations require establishments to lower levels of bacteria by ensuring process controls in production 

of animal products. 

This report covers the first full year of cecal sampling and provides initial data on antimicrobial resistant 

Salmonella in cecal samples from animals slaughtered in federally inspected establishments. Notable 

findings include: the high level of resistance in turkey cecal isolates; the isolation of minimal Salmonella 

Dublin isolates; the majority of ASSuT resistance being in swine isolates; and, the low number of XDR 

 

6 CDC, FDA, FSIS (2016). NARMS Integrated Report, 2014. Retrieved from 

http://www.fda.gov/downloads/AnimalVeterinary/SafetyHealth/AntimicrobialResistance/NationalAntimicrobialRe

sistanceMonitoringSystem/UCM528861.pdf. 
12

isolates. Ongoing analysis of isolates collected in this program and the addition of more advanced 

microbial characterization, especially through whole genome sequencing, will enable FSIS to assess how 

AMR profiles in food animals compare with AMR profiles of public health concern. Additionally, 

information from cecal sampling allows surveillance of antimicrobial resistance in isolates recovered 

from different points in the food production system. These analyses will be used to inform sampling

programs, guidelines, and policies; and support policies designed to reduce AMR bacteria in the food 

chain. Through these activities, FSIS is uniquely positioned to contribute science based expertise to 

promote a better understanding of the characteristics and movement of resistant bacteria throughout

the food chain.
13

Appendix

Sampling Protocols

Cecal sampling within slaughter establishments is scheduled at a frequency based on establishment size, 

animal classes slaughtered, and annual slaughter volumes. Establishments are sampled in a tiered, 

randomized fashion based on slaughter volume, resulting in a scheme representative of overall national 

production.

As described in FSIS Directive 10100.1, Section III.A,7

 sampling tasks for the NARMS sampling program 

are assigned at frequencies indicated in Appendix Table 1, using the previous 12 months of slaughter 

data.

Appendix Table 1. NARMS sampling frequencies. 

Slaughter Volume Maximum number of sampling tasks 

per month per sampling project

Top 25% of Slaughter 

Establishments 4 

Second 25% of Slaughter 

Establishments 2 

Lowest 50% of Slaughter 

Establishments 1 

An algorithm sets the number of cecal samples collected per slaughter class each month to reach an 

annual target. Appendix Table 2 shows the maximum numbers of samples that can be assigned per 

NARMS project per month.

Appendix Table 2. NARMS sampling algorithm (number of samples scheduled per class). 

Class Annual Monthly¶

Young Chickens

§ 600 55 (275 birds)

Young Turkeys

§ 300 28 (140 birds)

Dairy Cattle 1200 110

Beef Cattle* 2000 184

Market Hogs 800 74

Sows 800 74

§ Five cecal samples are pooled as one sample in young chickens and young turkeys

*samples divided between steer, heifer, adult beef equally

¶ Including about a 10% overage

Antimicrobial Susceptibility Testing

Minimal Inhibitory Concentrations (MICs) are determined for each isolate. MICs are defined as the 

lowest concentration of an antimicrobial drug that will inhibit the visible growth of a microorganism 

 

7 FSIS (2014). FSIS Directive 10,100.1 FSIS Sampling for the National Antimicrobial Resistance Monitoring System 

(NARMS). Retrieved from: https://www.fsis.usda.gov/wps/wcm/connect/056b7ec7-5456-4325-ae55-

1a73ddd6f348/10100.1.pdf?MOD=AJPERES.
14

after overnight incubation. Breakpoints are set by FDA and Clinical and Laboratory Standards Institute

(CLSI) to categorize bacteria as susceptible or resistant.

When breakpoint changes occur, historical isolates’ MICs are re-evaluated using current criteria to 

facilitate comparisons with historical data. This report uses breakpoints and categories that were 

implemented in January 2014 (Appendix Table 3).

Appendix Table 3. Interpretive criteria used for antimicrobial susceptibility testing of Salmonella1

.

Antimicrobial 

Class

Antimicrobial Drug

Breakpoints (μg/ml)

Susceptible Intermediate Resistant

Aminoglycosides

Gentamicin (GEN) ≤ 4 8 ≥ 16

Streptomycin (STR)1 ≤ 32 N/A ≥ 64

ß-Lactam/ßLactamase 

Inhibitor 

Combinations

Amoxicillin–Clavulanic Acid 

(AMC) ≤ 8 / 4 16 / 8 ≥ 32 / 16

Cephems

Cefoxitin (FOX) ≤ 8 16 ≥ 32

Ceftiofur (TIO) ≤ 2 4 ≥ 8

Ceftriaxone (AXO) ≤ 1 2 ≥ 4

Folate Pathway 

Inhibitors

Sulfisoxazole (FIS) ≤ 256 N/A ≥ 512

Trimethoprim–

Sulfamethoxazole (COT) ≤ 2 / 38 N/A ≥ 4 / 76

Macrolides Azithromycin (AZI)1 ≤ 16 N/A ≥ 32

Penicillins Ampicillin (AMP) ≤ 8 16 ≥ 32

Phenicols Chloramphenicol (CHL) ≤ 8 16 ≥ 32

Quinolones

Ciprofloxacin2 (CIP) ≤ 0.06 N/A ≥ 0.12

Nalidixic acid (NAL) ≤ 16 N/A ≥ 32

Tetracyclines Tetracycline (TET) ≤ 4 8 ≥ 16

1 Breakpoints were adopted from CLSI M100-S26 document (2014), except for streptomycin and azithromycin, 

which have no CLSI breakpoints. 2 In previous reports, resistance to nalidixic acid has been used as a surrogate for quinolone resistance. However 

with the 2012 Clinical Laboratory Standards Institute (CLSI) decision to widen the intermediate susceptibility 

range for ciprofloxacin, we now use decreased susceptibility to ciprofloxacin (DSC, MIC >= 0.12 ug/ml) as an 

indicator of emerging quinolone resistance. For the 2015 report, DSC is incorporated into the definition of 

multidrug resistance (MDR, resistance to 3 or more classes of antimicrobials). Although DSC encompasses both 

resistant and intermediate susceptibility populations, it is more clinically relevant than nalidixic acid resistance. 

In this report, the new MDR definition is retrospectively applied to all NARMS Salmonella data collected before 

2015(Internal Communication).
15

Appendix Table 4. Multidrug resistance profile descriptions.

Profile Abbreviation Resistance Description

AMC AMP FOX TIO AXO Resistance to amoxicillin-clavulanic acid, ampicillin, cefoxitin, ceftiofur, and 

ceftriaxone, with or without resistance to other antimicrobial drugs

GEN STR FIS TET Resistance to gentamicin, streptomycin, sulfamethoxazole/sulfisoxazole, 

and tetracycline, with or without resistance to other antimicrobial drugs

ACSSuT

Resistance to ampicillin, chloramphenicol, streptomycin, 

sulfamethoxazole/sulfisoxazole, and tetracycline, with or without resistance 

to other antimicrobial drugs

ASSuT

Resistance to at least ampicillin, streptomycin, 

sulfamethoxazole/sulfisoxazole, and tetracycline, with or without resistance 

to other antimicrobial drugs, except chloramphenicol

ACSSuTAuCx

Resistance to ampicillin, chloramphenicol, streptomycin, 

sulfamethoxazole/sulfisoxazole, tetracycline, amoxicillin/clavulanic acid, 

and ceftriaxone, with or without resistance to other antimicrobial drugs

ACT/S Resistance to ampicillin, chloramphenicol, and trimethoprimsulfamethoxazole, with or without resistance to other antimicrobial drugs

Categorization of the importance of Antimicrobial Drugs8

Five criteria are used by FDA to rank the importance of antimicrobial drugs in human medicine. The 

criteria are ranked 1 to 5 from most important to least important (Appendix Table 5).

Appendix Table 5. Criteria to rank importance of antimicrobial drugs.

Criterion 1: Antimicrobial drugs used to treat enteric pathogens that cause foodborne disease

Criterion 2: Sole therapy or one of few alternatives to treat serious human disease or drug is 

essential component among many antimicrobial drugs in treatment of human disease

Criterion 3: Antimicrobial drugs used to treat enteric pathogens in non-foodborne disease

Criterion 4: No cross-resistance within drug class and absence of linked resistance with other drug 

classes

Criterion 5: Difficulty in transmitting resistance elements within or across genera and species of 

organisms

The categories of importance for antimicrobial drugs based on these criteria are defined in Appendix 

Table 6, and Appendix Table 7 shows the categorization of important antimicrobial drugs included in AST 

for Salmonella.

 8 FDA (2003). Guidance for Industry #152, Evaluating the Safety of Antimicrobial New Animal Drugs with Regard to 

Their Microbiological Effects on Bacteria of Human Health Concern. Retrieved from 

https://www.fda.gov/downloads/AnimalVeterinary/GuidanceComplianceEnforcement/GuidanceforIndustry/UCM

052519.pdf.
16

Appendix Table 6. Antimicrobial drug categories of importance.

Critically important (C): Antimicrobial drugs which meet BOTH criteria 1 and 2 in Appendix A of the 

FDA Guidance for Industry #152

Highly important (H): Antimicrobial drugs which meet EITHER criterion 1 or 2 in Appendix A of the 

FDA Guidance for Industry #152

Important (I): Antimicrobial drugs which met EITHER criterion 3 and/or 4 and/or 5 in 

Appendix A of the FDA Guidance for Industry #152

Not classified (NC): Antimicrobial drugs which are not given a classification in FDA’s Guidance 

for Industry #152

Appendix Table 7. FDA categorization for antimicrobial drugs of importance highlighted in NARMS 

antimicrobial susceptibility analyses.

Antimicrobial Class Antimicrobial Drug Abbreviation FDA Classification

Cephems Ceftiofur TIO

Critically important (C)

Ceftriaxone AXO

Quinolones Ciprofloxacin CIP

Macrolides Azithromycin AZI

Folate Pathway Inhibitors TrimethoprimSulfamethoxazole COT

Aminoglycosides Gentamicin GEN

Highly Important (H)

Streptomycin STR

Penicillins Ampicillin AMP

Beta-Lactam/BetaLacatamase Inhibitor 

Combinations

AmoxicillinClavulanic Acid AMC or AUG

Phenicols Chloramphenicol CHL

Tetracyclines Tetracycline TET

Cephems Cefoxitin FOX Important (I) Quinolones Nalidixic Acid NAL

Folate Pathway Inhibitors SulfamethoxazoleSulfisoxazole FIS Not Classified (NC)