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United States Department of Agriculture

Agricultural Research Service

Research Project: Monitoring of Antimicrobial Resistance in Food Animal Production

Location: Bacterial Epidemiology and Antimicrobial Resistance

Title: Highlights of the NARMS 2009 Executive Report

item Mcdermott, Patrick -
item Whichard, Jean -
item Cray, Paula
item Tate, Heather -
item Karp, Beth -
item Haro, Jovita
item Plumblee, Jodie

Submitted to: World Wide Web
Publication Type: Research Technical Update
Publication Acceptance Date: September 7, 2011
Publication Date: September 7, 2011
Citation: McDermott, P., Whichard, J., Cray, P.J., Tate, H., Karp, B., Haro, J.H., Plumblee, J. 2011. Highlights of the NARMS 2009 Executive Report. Available:

Technical Abstract: Salmonella Isolates by Source During 2009, NARMS tested 2,192 isolates of non-typhoidal Salmonella from humans, 489 from retail meats, and 992 from food animals. • The most common serotypes in humans, in order of frequency were Enteritidis (18.7%), Typhimurium (16.9%), Newport (10.8%), Javiana (4.8%), Heidelberg (3.9%), and I 4,[5],12:i:- (3.3%). • The percent of retail chicken breast (CB) samples that tested positive for Salmonella increased from 9.2% in 2007 to 15.2% in 2008, and then to 21% in 2009. The proportion of CB isolates that carried serotype Typhimurium rose from 13.8% in 2006 (the lowest prevalence since testing began) to 44.4% in 2009. • The percent of ground turkey (GT) isolates that were serotype Saintpaul increased from 12% to 40% between 2008 and 2009, while serotypes Hadar and Saintpaul decreased. Antimicrobial Resistance-Salmonella The NARMS 2009 Executive Report provides detailed data on resistance to clinically important antimicrobial agents. Resistance to three antimicrobial classes important for treating Salmonella infections in humans is highlighted below. Cephems • Ceftriaxone resistance increased in CB isolates between 2007 and 2009, from 16.2% to 37.6%, following a steady decline from 26.5% in 2003 to 16.2% in 2007. • In humans, 32% of the ceftriaxone-resistant Salmonella isolates were serotype Typhimurium; 24% were Heidelberg; 20% were Newport; and 6.7% were Infantis. • The percentage of ceftriaxone-resistant Heidelberg isolates more than doubled in humans and chickens and almost doubled in CB between 2008 and 2009. • In chickens and CB, ceftriaxone resistance was found predominately in serotypes Kentucky, Typhimurium and Heidelberg, whereas ceftriaxone-resistant cattle isolates were mostly serotypes Newport, Dublin, and Typhimurium. Quinolones Resistance to nalidixic acid, an elementary quinolone, is correlated with decreased susceptibility to fluoroquinolones, a class of drugs important for treating salmonellosis. • In 2009, all Salmonella isolated from GT, pork chops (PC), chickens and swine were susceptible to nalidixic acid. Among the other sources, nalidixic acid resistance was less than 2%, with the exception of ground beef (GB) which had low isolation of Salmonella. • Among nalidixic acid-resistant isolates from humans, Enteritidis was the most common serotype (38.5%), followed by Typhimurium (20.5%). Potentiated Sulfonamides • Resistance to trimethropim-sulfamethoxazole has remained low (<5%) over the years in isolates from all sources, except for PC which had low isolation. Multidrug Resistance • In 2009, 83.2% of human Salmonella isolates were not resistant to any antimicrobial agent tested, increasing steadily from 66.1% in 1996. • Among retail meats and food animals, the percentage of isolates with no resistance detected was highest in bovine (68.5% for cattle and 57.1% for GB) and lowest in turkeys (19.8% in turkeys and 22.1% in GT). • Among CB in 2009, there was no resistance detected in 29.2% of isolates; the lowest it’s been since retail testing began in 2002. An important multidrug resistance pattern in Salmonella is the combined resistance to ampicillin, chloramphenicol, streptomycin, sulfonamides, and tetracycline (ACSSuT). This pattern is associated with more severe and invasive disease in humans. • In human Salmonella isolates, ACSSuT resistance declined from 10.1 % in 2001 to 5.1% in 2009. The most common serotypes among ACSSuT-resistant isolates were Typhimurium (64.3%) and Newport (13.4%). This decline may reflect in part the decline in Salmonella ser. Typhimurium DT104, an ACSSuT-resistant strain of Salmonella that emerged in the late 1980s and has caused several outbreaks. • In cattle isolates, the ACSSuT pattern declined from 18.1% in 2008 to 15.0% in 2009, and was most common in serotypes Typhimurium and Newport. • In swine, ACSSuT resistance increased from 8.1% in 2008 to 13.3% in 2009. Typhimurium and Agona were the most common serotypes among ACSSuT-resistant isolates. • ACSSuT resistance remained low in poultry (<5%). In some isolates the ACSSuT pattern is linked with decreased susceptibility to additional beta-lactam drugs, including ceftiofur, ceftriaxone, amoxicillin-clavulanic acid, and cefoxitin. Over the years, NARMS has detected this phenotype (designated ACSSuTAuCx) among Salmonella from all sample sources tested. In the U.S., the addition of extended spectrum cephalosporin resistance (e.g. ceftriaxone) is usually conferred by blaCMY-2 genes that reside on plasmids that frequently contain additional resistance genes. • In 2009, 1.4% of human Salmonella isolates were resistant to at least ACSSuTAuCx; isolates resistant to this pattern were most commonly serotypes Newport (50%) and Typhimurium (20%). • Similar to ACSSuT, among poultry (both retail and carcass rinsates at slaughter) has remained <5% since testing began. • Approximately 9.5% of cattle isolates showed resistance to ACSSuTAuCx, the lowest since 2000. In cattle, 42% of the ACSSuTAuCx-resistant Salmonella isolates were serotype Newport and 21% were serotype Dublin. • ACSSuTAuCx resistance in swine isolates has remained low since testing began. Of increasing concern are the evolution and spread of bacteria resistant to all classes of antibiotics. • In 2009, two Salmonella isolates from humans and two from GB were resistant to all eight classes of antimicrobials currently tested in NARMS. Campylobacter Isolates by Source During 2009, NARMS tested 1,159 Campylobacter isolates from humans, 541 from retail poultry, and 106 from chickens at slaughter. • The major Campylobacter species recovered from humans were jejuni (91.0%) and coli (8.7%). • C. jejuni was more commonly isolated than C. coli from CB (64.5% vs. 35.5%) and chickens at slaughter (73.6% vs. 26.4%). Antimicrobial Resistance-Campylobacter Resistance to the two antimicrobial classes important for treating Campylobacter infections in humans is highlighted below. Quniolones Quinolones such as the fluoroquinolone, ciprofloxacin, are effective treatments for human campylobacteriosis. Fluoroquinolones were first approved for used in poultry in the United States in 1995 for control of mortality associated with E. coli. Because of concerns about increasing fluoroquinolone resistance among Campylobacter in both animal and human hosts, approvals for sarafloxacin and enrofloxacin use in poultry were withdrawn in April 2001 and September 2005, respectively. See • In 2009, ciprofloxacin resistance in C. jejuni from humans was 23%, a slight decrease from a peak of 25.8% in 2007, but still higher than 2005 (21.5%) when enrofloxacin approval was withdrawn. • The percentage of ciprofloxacin-resistant C. jejuni from CB increased from 14.6% in 2008 to 21.1% in 2009. This is the first notable increase since withdrawal of enrofloxacin use in poultry. • Ciprofloxacin resistance of C. jejuni isolates from chickens at slaughter declined from 32.1% in 2008 to 19.7% in 2009. The lowest resistance was in 2005 (8.8%). • In C. coli isolates from humans, resistance to ciprofloxacin was 21.7% in 2009, a decline from 30% in 2008. • In chicken isolates, ciprofloxacin resistance increased from 14.3% in 2008 to 22.2% in 2009. Resistance decreased in the three previous years (2006-2008), following enrofloxacin withdraw. • Ciprofloxacin resistance in C. coli isolates from CB declined to 18.4% in 2009 from 20.4% in 2008. The lowest resistance observed since the FDA’s withdrawal of enrofloxacin approval. Macrolides • Erythromycin resistance in C. jejuni from humans has remained below 3% since testing began. • In retail poultry and chickens at slaughter, erythromycin resistance has remained relatively low in C. jejuni. • Among retail poultry and chickens at slaughter, erythromycin resistance is generally higher in C. coli than in C. jejuni.

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