Informe sobre resistencias antimicrobianas en Salmonella y Campylobacter en 2010 en EE.UU.

Publicado 27 julio 2012

Mirada Internacional, Novedades

El Sistema Nacional de Seguimiento de Resistencias Antimicrobianas de EE.UU. (NARMS) acaba de publicar un informe donde se presentan los resultados de prevalencia de serotipos y de resistencias antimicrobianas de Salmonella y Campylobacter aislados en humanos, animales para consumo y sus derivados durante el año 2010.

II. Summary of the NARMS 2010 Executive Report

Highlights from results of testing of Salmonella and Campylobacter strains isolated from humans, retail meats, and food animals in 2010 are described below. For more information, including a description of changes in surveillance methods over time, refer to other sections of this report and individual agency NARMS 2010 reports for human, retail meat, and food animal isolates.

Non-Typhoidal Salmonella

A total of 3,947 non-typhoidal Salmonella isolates were tested, consisting of 2,474 from humans, 400 from retail meats, and 1,073 from healthy food animals at slaughter. Among retail meats, Salmonella was isolated from 15% of ground turkey samples, 13% of chicken breast samples, 1.5% of pork chop samples, and 0.5% of ground beef samples. Some key findings about serotype distribution and antimicrobial resistance are described below.

Serotype Frequencies

Some of the most common serotypes among isolates from humans were also common among food isolates, particularly isolates from poultry sources.

  • Among isolates from humans, Enteritidis (21%), Typhimurium (15%), and Newport (12%) remained the three most common serotypes, followed by Javiana (7.2%), I 4,[5],12:i:-(3.1%), and Heidelberg (2.5%).
  • The four most common serotypes among retail chicken breast isolates were Typhimurium (46%), Enteritidis (16%), Heidelberg (12%), and Kentucky (12%); the four most common serotypes among isolates from chickens at slaughter were Kentucky (43%), Enteritidis (27%), Typhimurium (10%), and Heidelberg (4.4%).
  • Hadar and Saintpaul remained among the top three serotypes recovered from retail ground turkey (10% and 24% of retail ground turkey isolates, respectively) and from turkeys at slaughter (20% and 14% of turkey isolates, respectively). Serotypes Heidelberg and IIIa 18:z4,z23:- increased in prevalence from 2009, and were two of the top four serotypes isolated from retail ground turkey (8.4% and 11% of all serotypes, respectively) and turkeys at slaughter (9.3% and 7.3%, respectively).
  • Montevideo (25%) and Dublin (17%) remained the predominant serotypes among isolates from cattle at slaughter. The proportion of cattle isolates that are serotype Dublin has steadily increased since 1997. This serotype is associated with invasive salmonellosis in humans (Jones et al., 2008).

Resistance to nalidixic acid is correlated with decreased susceptibility to fluoroquinolones (Crump et al., 2003), a class of drugs important for treating complicated Salmonella infections in humans (Pegues and Miller, 2010). In the United States, fluoroquinolones are approved for the treatment of certain respiratory infections in swine and cattle (Animal Drugs @ FDA), but these agents are not currently approved for use in poultry.

  • Nalidixic acid resistance has remained <3% from all sources since 2004. In 2010, 2.0% of human Salmonella isolates were resistant to nalidixic acid. Enteritidis was the most common serotype (55%) among the nalidixic acid-resistant isolates from humans. Among the serotype Enteritidis isolates tested from humans, 5.2% were resistant. Enteritidis isolates were rarely resistant to the other agents tested.
  • Nalidixic acid resistance was rare in retail meat and animal isolates. It was found only in seven isolates from cattle (2.8%), one isolate from turkey (0.7%), and one from retail ground turkey (0.5%) in 2010. Of the seven cattle isolates, six were serotype Dublin. Both the turkey and retail ground turkey isolates were serotype Albert.

Ceftriaxone, an extended-spectrum cephalosporin, is important for treating complicated Salmonella infections in humans (Pegues and Miller, (010). Ceftiofur, a closely related antimicrobial agent, is licensed for use in food animal production (Animal Drugs@ FDA).

  • Among all isolates from humans, ceftriaxone resistance has been relatively stable since 2004 (<4%). In 2010, 2.8% of isolates were resistant. Newport (31%), Typhimurium (26%), and Heidelberg (21%) were the most common serotypes among the ceftriaxone-resistant isolates.
  • Ceftriaxone resistance was found in 35% of retail chicken breast isolates in 2010, after rising from 16% in 2007 to 38% in 2009. Typhimurium (81%) was the predominant serotype among these ceftriaxone-resistant isolates. Among retail ground turkey isolates, ceftriaxone resistance rose from 5.7% in 2009 to 16% in 2010, the highest since testing began in 2002.
  • Among isolates from food animals at slaughter, resistance to ceftriaxone was 22% among isolates from cattle, 15% among isolates from turkeys, and 12% among isolates from chickens. Only 2 isolates (1.8%) from swine were ceftriaxone resistant. Resistance in isolates from cattle and turkeys was the highest observed since testing began in 1997. Dublin was the predominant serotype (55%) among ceftriaxone-resistant isolates from cattle. Heidelberg (22%), Brandenburg (13%), and Schwarzengrund (13%) were the most common serotypes among ceftriaxone-resistant turkey isolates. Kentucky (55%), Typhimurium (24%) and Heidelberg (12%) were the most common serotypes among the ceftriaxone-resistant chicken isolates.
  • Among serotype Newport isolates from humans, ceftriaxone resistance declined to 7.2% after peaking at 26% in 2001. A decline was also observed among cattle isolates; resistance declined to 60% (3/5) in 2010 after peaking at 82% (22/27) in 2005.
  • Among serotype Typhimurium isolates from humans, ceftriaxone resistance declined from 6.5% in 2009 to 4.9% in 2010. Among retail chicken breast isolates, resistance steadily rose from 44% in 2007 to 61% in 2010.
  • Human infections with serotype Heidelberg are associated with invasive disease (Jones et al., 2008). Although the percentage of serotype Heidelberg among all Salmonella isolated from humans and poultry has declined, ceftriaxone resistance has increased. Among human strains, ceftriaxone resistance increased from 8.0% in 2008 to 21% in 2009 and 24% in 2010.
  • Among retail chicken breast isolates, resistance rose from 17% in 2008 to 32% in 2009 then declined to 24% in 2010. Among isolates from chickens at slaughter, ceftriaxone resistance increased from 8.5% in 2008 to 18% in 2009 and rose to 32% in 2010. Resistance in isolates from retail ground turkey and turkeys at slaughter increased from 3.5% and 13% in 2008 to 10% and 33% in 2009, and rose to 24% and 36% in 2010, respectively.

No Resistance Detected
. In 2010, 85% of isolates from humans had no resistance to any antimicrobial agents tested, an increase from 74% in 1999.
. Among isolates from retail meats and food animals at slaughter, the percentage that had no resistance to any antimicrobial agents tested was highest in bovine sources (61% in cattle and 57% in retail ground beef) and lowest in turkeys (25% in turkeys at slaughter and 31% in retail ground turkey).
Multidrug Resistance

  • Among isolates from humans, resistance to .3 antimicrobial classes was 9.1%, the lowest since 1996. However, among serotype Heidelberg isolates, resistance to .3 antimicrobial classes increased from 17% in 2007 to 28% in 2008 and 34% in 2010. Similarly, among serotype I 4,[5],12:i:- isolates, resistance to .3 antimicrobial classes increased from 5.5% in 2007 to 13% in 2009 and 22% in 2010. Typhimurium (44%) was the most common serotype among isolates resistant to .3 classes.
  • Among retail chicken breast isolates, resistance to .3 antimicrobial classes declined to 43%, after a steady increase from 24% in 2006 to 49% in 2009. Typhimurium (81%) was the predominant serotype among isolates with resistance to .3 classes.
  • Among retail ground turkey isolates, resistance to .3 antimicrobial classes was found in34%, a decline from the peak resistance of 52% in 2008. Similarly, the percentage of Heidelberg isolates resistant to .3 classes declined to 65% from the peak of 83% in 2008. Heidelberg (16%), Saintpaul (16%), and I 4,[5],12:r:- (13%) were the most common serotypes among isolates resistant to .3 classes.
  • Among isolates from turkeys at slaughter, resistance to .3 antimicrobial classes increased from 30% in 2008 to 37%. Hadar (16%), Heidelberg (14%), Saintpaul (11%) and Schwarzengrund (11%) were the most common serotypes among isolates resistant to .3 classes.
  • Among isolates from cattle at slaughter, resistance to .3 antimicrobial classes increased from 22% in 2007 to 28%. Dublin was the predominant serotype (55%) among isolates with resistance .3 antimicrobial classes.

An important multidrug resistance (MDR) pattern in Salmonella is resistance to ampicillin, chloramphenicol, streptomycin, sulfonamides, and tetracycline (ACSSuT). This pattern is associated with invasive disease in humans (Varma et al., 2005a; Varma et al, 2005b). Another important MDR pattern linked to severe illness in humans is resistance to ACSSuT with additional resistance to amoxicillin-clavulanic acid and ceftriaxone (ACSSuTAuCx) (Gupta, 2003).

  • Among isolates from humans, resistance to at least ACSSuT declined to 4.3%, the lowest since testing began in 1996. Typhimurium (64%) and newport (21%) were the most common serotypes among isolates with this resistance pattern. ACSSuT resistance was detected in 19% of Typhimurium and 7.2% of Newport isolates.
  • Among isolates from retail poultry and poultry at slaughter, ACSSuT resistance remained low (<5%). In 2010, 7.3% of isolates from swine at slaughter were resistant to ACSSuT, a decline from the peak resistance of 13% in 2009.
  • Among isolates from cattle at slaughter, resistance to at least ACSSuT was 19%. Dublin (52%) and Typhimurium (15%) were the most common serotypes among cattle isolates with this resistance pattern. ACSSuT resistance was 59% among Dublin and 40% among Typhimurium isolates.
  • In 2010, 1.3% of isolates from humans were resistant to at least ACSSuTAuCx. Newport (67%) and Typhimurium (21%) were the most common serotypes among isolates with this resistance pattern. Resistance was 7.2% among Newport isolates and 1.9% among Typhimurium isolates.
  • Resistance to ACSSuTAuCx among isolates from retail poultry, poultry at slaughter, and swine remained low (<4.5%), as it has been since testing began.
  • ACSSuTAuCx resistance among cattle isolates from slaughter was 16%, an increase from 9.5% in 2009. Serotype Dublin accounted for 55% of isolates with this pattern. Fifty-four percent of serotype Dublin isolates from cattle were resistant to at least ACSSuTAuCx.

A total of 2,136 Campylobacter isolates were tested, including 1,310 from humans, 518 from retail meats (505 from chicken breasts and 13 from ground turkey) and 308 from chickens at slaughter. Poultry are a major source of human C. jejuni infections. All sources except retail
ground turkey yielded higher proportions of C. jejuni than C. coli. The distribution of these predominant species varied by source: 88% C. jejuni and 9% C. coli among isolates from humans; 70% C. jejuni and 29% C. coli among retail chicken breast isolates; 39% C. jejuni and 54% C. coli among retail ground turkey isolates; 68% C. jejuni and 32% C. coli among chicken isolates. Resistance to three important antimicrobial classes highlighted below was mostly higher among C. coli than among C. jejuni isolates from all sources. Some key antimicrobial resistance findings are described below.

The macrolides, erythromycin and azithromycin are important antimicrobial agents for the treatment of severe campylobacteriosis in humans (Allos and Blaser, 2010). Macrolides are also authorized for use in food-producing animals (Animal Drugs @ FDA).

  • Erythromycin resistance in C. jejuni isolated from humans, retail chicken breasts, and chickens at slaughter has remained below 4.0% since testing began.
  • Erythromycin resistance was 4.3% among C. coli isolates from humans; it ranged from 0% to 10% during 1999.2009 with no apparent pattern.
  • Erythromycin resistance was 4.1% among C. coli recovered from retail chicken breasts and 4.0% among C. coli from chickens at slaughter, both the lowest since 2002.

The fluoroquinolone ciprofloxacin is an alternative therapy for treating campylobacteriosis (Allos and Blaser, 2010). FDA approvals of the two poultry fluoroquinolones, sarafloxacin and enrofloxacin, were withdrawn in April 2001 and September 2005, respectively, due to resistance
concerns. See

  • Ciprofloxacin resistance among C. jejuni recovered from humans (253/1,158), retail chicken breasts (80/355) and chickens at slaughter (48/208) remained .20%.
  • Among C. jejuni isolated from humans, ciprofloxacin resistance increased from 12% in 1997, peaked at 26% in 2007, and was detected in 22% in 2010. Among human C. coli isolates, ciprofloxacin resistance was 31% in 2010.
  • Ciprofloxacin resistance in C. jejuni isolated from retail chicken breasts increased from 17% in 2006 to 23% in 2010 and declined in C. coli from 22% to 14% during that time.
  • Ciprofloxacin resistance in C. jejuni isolated from chickens at slaughter increased from 22% in 2007 when the first full year of risked-based sampling by FSIS was implemented, peaked at 32% in 2008, and declined to 23% in 2010. Among C. coli isolates, ciprofloxacin resistance was 22% in 2010.

Gentamicin is categorized as a highly important antimicrobial agent for human medical therapy according to criteria outlined in FDAfs guidance on evaluating the safety of antimicrobial new animal drugs (FDA, 2003). It is used in humans for the treatment of severe infections, including
Campylobacter, that may be transmitted from food animal sources (Allos and Blaser, 2010).
Gentamicin is also used in chickens, where it can be injected in day-old chicks for the prevention of early mortality associated with bacterial infections (Animal Drugs @ FDA).

  • Gentamicin resistance among C. jejuni isolates from humans, retail chickens and chickens at slaughter was <1%.
  • Between 2007 and 2010, gentamicin resistance among C. coli increased from 0% to 11% among isolates from humans, 0.7% to 13% among isolates from retail chicken breasts, and 1.3% to 5.0% among isolates from chickens at slaughter.

Allos BM, Blaser MJ. Campylobacter jejuni and related species. In: Mandell GL, Bennett JE, and Dolin R, editors. Mandell, Douglas, and Bennettfs Principles and Practice of Infectious Diseases, 7th ed. Philadelphia, PA: Churchill Livingstone; 2010. p. 2793.2802.

Animal Drugs @ FDA: Available at

Crump JA, et al. (2003). Reevaluating fluoroquinolone breakpoints for Salmonella enterica serotype Typhi and for non-Typhi Salmonellae. Clinical Infectious Diseases, 37:75.81.

FDA Center for Veterinary Medicine Guidance for Industry #152, Evaluating the Safety of Antimicrobial New Animal Drugs with Regard to Their Microbiological Effects on Bacteria of Human Health Concern.

Gupta A, et al. (2003). Emergence of multidrug-resistant Salmonella enterica serotype Newport infections resistant to expanded-spectrum cephalosporins in the United States. Journal of Infectious Diseases, 188:1707-16.

Jones TF, et al. (2008). Salmonellosis outcomes differ substantially by serotype. Journal of Infectious Diseases, 198:109-14.
Pegues DA, Miller SI. Salmonella species, including Salmonella Typhi. In: Mandell GL, Bennett JE, and Dolin R, editors. Mandell, Douglas, and

Bennettfs Principles and Practice of Infectious Diseases, 7th ed. Philadelphia, PA: Churchill Livingstone; 2010. p. 2887.2903.
Varma JK, et al. (2005a). Hospitalization and antimicrobial resistance in Salmonella outbreaks, 1984-2002. Emerging Infectious Diseases, 11:943-6.

Varma JK, et al. (2005b). Antimicrobial-resistant nontyphoidal Salmonella is associated with excess bloodstream infections and hospitalizations. Journal of Infectious Diseases, 191:554-61.

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