National Antimicrobial Resistance Monitoring System (NARMS)
1998 Annual Report
Report Summary
Table of Contents
SUMMARY
In 1998, there were 1476 Salmonella isolates, 315 E. coli O157:H7
isolates, and 382 Campylobacter isolates from humans submitted to the
National Antimicrobial Resistance Monitoring System:Enteric Bacteria (NARMS).
Twenty-seven percent of Salmonella isolates were resistant to one or
more antimicrobial agents. Among Salmonella Typhimurium isolates, 53%
were resistant to one or more antimicrobial agents. Thirty-two percent of Salmonella
Typhimurium isolates had the multi-drug resistant pattern characteristic of
DT104. One Salmonella isolate was resistant to ciprofloxacin. The percentage
of Salmonella isolates with ciprofloxacin minimum inhibitory concentrations
(MICs) >0.25 increased from 0.4% in l996 to 0.7% in l998. Among E. coli O157:H7
isolates, 7.3% were resistant to one or more antimicrobial agents. Among Campylobacter
isolates, 55.0% were resistant to one or more antimicrobial agents; 13.3% were
resistant to ciprofloxacin.
NARMS was launched in l996, within the framework of CDC’s Emerging Infections Program’s Epidemiology and Laboratory Capacity Program and the Foodborne Disease Active Surveillance Network (FoodNet) as a collaboration between CDC, Food and Drug Administration-Center for Veterinary Medicine (FDA), United States Department of Agriculture- Food Safety and Inspection Service and Agricultural Research Service (USDA), and 14 state and local health departments to prospectively monitor the antimicrobial resistance of human non-typhoid Salmonella and Escherichia coli O157:H7 isolates. In 1998, there were 16 NARMS health department partners (CA, CO, CT, FL, GA, KS, Los Angeles County, MD, MN, MA, NJ, New York City, New York State, OR, WA, and WV), representing approximately 97 million persons (37% of the United States population). In 1998, seven states (CA, CT, GA, MD, MN, NY, and OR) also monitored antimicrobial resistance among human Campylobacter isolates (Table 1, Figure 1).
NARMS participating public health laboratories select every tenth Salmonella and every fifth E. coli O157:H7 isolate received at their laboratory, and forward the isolates to CDC for susceptibility testing. At CDC, a semi-automated system (Sensititre, Trek Diagnostics, Westlake, OH) is used to determine the MICs for 17 antimicrobial agents: amikacin, ampicillin, amoxicillin-clavulanic acid, apramycin, ceftiofur, ceftriaxone, cephalothin, chloramphenicol, ciprofloxacin, gentamicin, kanamycin, nalidixic acid, streptomycin, sulfamethoxazole, tetracycline, trimethoprim-sulfamethoxazole, and ticarcillin (Table 2). Public health laboratories from seven states also select and forward the first Campylobacter isolate received each week to CDC for susceptibility testing. For Campylobacter, the E-test system (AB BIODISK, Solna, Sweden) is used to determine the MICs for 8 antimicrobial agents: azithromycin, chloramphenicol, ciprofloxacin, clindamycin, erythromycin, gentamicin, nalidixic acid, and tetracycline (Table 2). After confirmation to genus level, identification of Campylobacter to species level is performed using dark field motility, oxidase test, and hippurate test, and for hippurate-negative Campylobacter isolates, polymerase chain reaction.
For all three pathogens in this report, MIC results are dichotomized, and isolates with intermediate susceptibility are categorized as sensitive. Breakpoints are determined using, when available, National Committee for Clinical Laboratory Standards (NCCLS). In l998, a validation of MIC results obtained by the CDC Sensititre system and the USDA Sensititre system was performed by both laboratories. Twelve samples from each laboratory were tested in both laboratories for MICs to all 17 antimicrobial agents; results from both systems were analyzed for consistency.
RESULTS
Salmonella
A total of 1476 Salmonella isolates were received at CDC in 1998; 1466/1476
(99.3%) were viable upon receipt and tested for antimicrobial susceptibility.
The antimicrobial agents with the highest prevalence of resistance were tetracycline,
sulfamethoxazole, streptomycin, and ampicillin; 295/1466 (20.1%) were resistant
to tetracycline, 283/1466 (19.3%) isolates were resistant to sulfamethoxazole,
273/1466 (18.6%) were resistant to streptomycin, and 241/1466 (16.4%) were resistant
to ampicillin (Table 3, Figure 2). Correlation between ampicillin resistance
and ticarcillin resistance was very high; 234/241 (97.1%) of isolates resistant
to ampicillin were resistant to ticarcillin. All ticarcillin-resistant Salmonella
isolates were also resistant to ampicillin. One (0.1%) isolate (S. Schwarzengrund)
was resistant to ciprofloxacin; twenty (1.4 %) isolates were resistant to nalidixic
acid. Ten (0.7%) isolates were resistant to ceftriaxone. No isolates tested
were resistant to amikacin (Table 3, Figure 2). MICs of all antimicrobial agents
for Salmonella are shown in Figure 3.
Frequency of resistance among different serotypes of Salmonella is shown in Table 4. Among Salmonella isolates, 397/1466 (27.1%) were resistant to one or more agents, and 346/1466 (23.6%) were resistant to two or more agents. Among serotypes with >22 isolates tested, the serotypes with the greatest resistance were Hadar, Typhimurium, Heidelberg, and Agona. Among Salmonella isolates tested, 245/1466 (16.7%) were serotype Enteritidis and 380/1466 (25.9%) were serotype Typhimurium (includes serotype Typhimurium var. Copenhagen) (Table 4). Among S. Enteritidis isolates, 30/245 (12.2%) were resistant to one or more antimicrobial agents. Among S. Typhimurium isolates, 200/380 (52.6%) were resistant to one or more antimicrobial agents (Table 4). Resistance to each antimicrobial agent among specific serotypes of Salmonella is shown in Figure 4.
In recent years, a multidrug-resistant strain of S. Typhimurium (DT104) has been identified. Among 380 S. Typhimurium isolates tested, 120 (31.6%) were resistant to the five antimicrobial agents, ampicillin, chloramphenicol, streptomycin, sulfamethoxazole, and tetracycline (ACSSuT), to which S. Typhimurium DT104 is commonly resistant (Table 5, Figure 6). Of the 120 S. Typhimurium isolates with the ACSSuT resistance pattern, 17 (14.2%) were also resistant to kanamycin, 8 (6.7%) were also resistant to cephalothin, 8 (6.7%) were also resistant to amoxicillin-clavulanic acid, 5 (4.2%) were also resistant to ceftiofur, and 4 (3.3%) were also resistant to ceftriaxone (Table 6). S. Typhimurium with the ACSSuT resistance pattern were somewhat more frequently isolated from blood (5/120, 4.2%) than were other S. Typhimurium isolates (9/260, 3.5%) (Table 7).
A second penta-resistant pattern, resistance to ampicillin, kanamycin, streptomycin, sulfamethoxazole, and tetracycline (AKSSuT), has also emerged among Salmonella Typhimurium. These strains are not DT104 by phage typing. Among 380 Salmonella Typhimurium isolates tested, 47/380 (12.4%) had the AKSSuT resistance pattern (Table 5). Of the 47 S. Typhimurium isolates with the AKSSuT resistance pattern, 17 (36.2%) were also resistant to chloramphenicol, 9 (19.1%) were also resistant to cephalothin, and 4 (8.5%) were also resistant to amoxicillin-clavulanic acid (Table 6). S. Typhimurium with the AKSSuT resistance pattern were more commonly isolated from blood (4/47, 8.5%) than were other S. Typhimurium isolates (9/260 or 3.5%) (Table 7).
Salmonella isolates with the ACSSuT or AKSSuT resistance pattern were also often additionally resistant to other antimicrobial agents, as shown in Table 8.
One Salmonella isolate (0.1%) was resistant to ciprofloxacin. The percentage of Salmonella isolates with ciprofloxacin MICs >0.25 increased from 0.4% (5/1326) in 1996 to 0.7% (10/1465) in 1998 (Figure 3). Serotypes of Salmonella isolates with reduced susceptibility or resistance to ciprofloxacin included S. Enteritidis (7/21 or 33.3%) and S. Typhimurium (3/21 or 14.3%)(Table 9 ). The percentage of Salmonella isolates resistant to nalidixic acid (MIC >32) increased from 0.4% (5/1326) in 1996 to 1.4% (20/1466) in 1998 (Figure 3 ). Serotypes of Salmonella isolates with resistance to nalidixic acid included S. Enteritidis (12/35 or 34.3%) and S. Typhimurium (6/35 or 17.1%) (Table 10).
E. coliO157:H7
A total of 315 E. coli O157:H7 isolates were received at CDC in 1997;
313/315 (99.4%) were tested for antimicrobial sensitivity. Among E. coli
O157:H7 isolates, 23/313 (7.3%) were resistant to one or more antimicrobial
agents and 19/313 (6%) were resistant to two or more agents. The most common
resistance among E. coli O157:H7 isolates was to sulfamethoxazole (18/313
or 5.8%) or tetracycline (14/313 or 4.5%) (Table 11). None of the E. coli
O157:H7 isolates tested were resistant to amikacin, amoxicillin/clavulanic acid,
apramycin, ceftiofur, ceftriaxone, cephalothin, ciprofloxacin, gentamicin, or
nalidixic acid (Table 11, Figure 7). The MICs for E. coli O157:H7 are
shown in Figure 8.
Campylobacter
A total of 382 Campylobacter isolates were collected in 1998 and forwarded
to CDC; 346/382 (91.0%) were viable upon receipt and tested for antimicrobial
susceptibility (Table 1, Figure 1). Among tested isolates, 332/346 (96%) were
C. jejuni, 9/346 (2.6%) were C. coli, 2 were C. upsaliensis,
1 was C. lari, and 2 were undetermined. Among Campylobacter jejuni
isolates, 181/332 (54.5%) were resistant to one or more antimicrobial agents,
and 52/332 (15.6%) were resistant to two or more agents. The most common resistance
among Campylobacter jejuni isolates was to tetracycline (46.4%) followed
by nalidixic acid (15.1%), and ciprofloxacin (13.3%) (Table 12, Figure 9). The
MICs for Campylobacter jejuni are shown in Figure 10. Among Campylobacter
coli isolates, 5/9 (56%) were resistant to one or more antimicrobial agents,
and 3/9 (33%) were resistant to two or more agents. The most common resistance
among Campylobacter coli isolates was to nalidixic acid (55.6%)
, followed by tetracycline (44.4%), chloramphenicol (22.2%), and ciprofloxacin
(11.1%) (Table 12).
SENSITITRE VALIDATION STUDY OVERALL
355/408 (86%) of MIC results obtained in CDC and USDA laboratories were identical. Of the 53 (14%) results which differed, 52/53 (98%) differed by one dilution. In the 53 instances of disagreement, CDC had the higher MIC 17 times. The disagreements involved gentamicin (3/17), apramycin (3/17), cephalothin (2/17), streptomycin (2/17), tetracycline (2/17), ciprofloxacin (2/17), ticarcillin (1/17), amoxicillin-clavulanic acid (1/17), and trimethoprim-sulfamethoxazole (1/17). The one instance with >1 dilution disagreement involved ticarcillin (3 dilutions higher). Overall, there was a 99% agreement rate with respect to interpretation of Sensititre results obtained by CDC and USDA laboratories.
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