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we reviewed final reports of nontyphoidal salmonella outbreaks investigated by cdc from 1984 to 2002 .
we excluded outbreaks that occurred in a healthcare setting or outside the united states , including on cruise ships . when antimicrobial susceptibility was not recorded in the final report , we searched cdc microbiology records for susceptibility test results on isolates collected as part of the outbreak .
outbreaks were only included if susceptibility data were available for > 1 isolate . because different laboratories performed susceptibility testing , the antimicrobial agents tested and the methods used varied between outbreaks .
we classified outbreaks as resistant when the outbreak strain was resistant to 1 antimicrobial agent ; other outbreaks were considered pansusceptible .
outbreaks caused by resistant strains were additionally classified as r - type ac / kssut when the outbreak strain was at least resistant to ampicillin , chloramphenicol or kanamycin , streptomycin , sulfamethoxazole , and tetracycline .
outbreaks were additionally classified as resistant to a clinically important agent when the outbreak strain was at least resistant to ampicillin , trimethoprim - sulfamethoxazole , aminoglycosides , fluoroquinolones , or a third - generation cephalosporin .
data from the final investigative reports were used for the analysis . when analyzing data according to outbreaks , we calculated the medians for percentage hospitalized and percentage who died and compared medians with the wilcoxon rank - sum test . when analyzing data according to ill persons , we pooled data from the reports , calculated proportions , and compared proportions with chi - square or , when appropriate , fisher exact test .
the denominators for percentage hospitalized and died varied depending on the number of persons in whom outcome data were ascertained .
data were analyzed by using sas v.9 ( sas institute , cary , nc , usa ) . from 1984 to 2002 , cdc investigated 48 community outbreaks of nontyphoidal salmonella strains in the united states .
of these , 47 ( 98% ) had a final report available for review ( table a1 ) .
we restricted our analyses to the 39 ( 83% ) outbreaks in which data about antimicrobial susceptibility were available .
the largest outbreak occurred in 1985 , in which culture - confirmed s. typhimurium infection associated with milk consumption developed in 16,659 persons ( 11 ) .
strains from 11 ( 28% ) outbreaks were resistant , and 28 ( 72% ) were pansusceptible .
the 11 outbreaks caused by resistant strains involved 18,698 persons . of these 11 outbreaks ,
7 ( 64% ) , involving 17,182 persons , had strains that were at least r - type ac / kssut , and 9 ( 82% ) , involving 17,919 persons , had strains that were resistant to a clinically important agent .
the hospitalization rates were higher for each type of outbreak caused by resistant salmonellae compared with outbreaks caused by susceptible salmonellae ( p<0.01 for each comparison ) ( table ) . to account for differences in the size of outbreaks
, we compared the median proportion of persons hospitalized and compared hospitalization rates after excluding a large salmonella outbreak that occurred in 1985 .
the median proportion hospitalized for each type of outbreak caused by resistant strains ( 26% ) was > 2.5 times higher than the median proportion hospitalized for outbreaks caused by pansusceptible strains ( 10% , p<0.05 for all resistance patterns ) .
the difference in hospitalization rates between outbreaks caused by resistant and susceptible strains was similar after we excluded the large 1985 outbreak of resistant s. typhimurium , in which the percentage hospitalized was 22% .
the results also remained similar after excluding s. enteritidis outbreaks , in which rates of hospitalization and isolate resistance were low . * ac / kssut , ampicillin , chloramphenicol , kanamycin , streptomycin , sulfamethoxazole , tetracycline .
mortality data were available for 24 outbreaks involving 21,927 persons . a greater proportion of persons died in resistant outbreaks than in pansusceptible outbreaks , but the difference was not significant ( 0.1% in outbreaks caused by resistant strains vs. 0.06% in outbreaks caused by pansusceptible strains , p = 0.57 ) ( table ) .
three ( 38% ) outbreaks were due to s. enteritidis and 2 ( 25% ) to s. typhimurium . in the 6 outbreaks for which hospitalization data were available , 70 ( 20% )
of 353 persons were hospitalized . in the 4 outbreaks for which mortality data were available , 7 ( 0.4% ) of 1,708 persons died .
outbreaks caused by antimicrobial - resistant , nontyphoidal salmonellae were associated with an increased rate of hospitalization compared with outbreaks caused by pansusceptible salmonellae .
persons who take antimicrobial drugs for reasons unrelated to gastroenteritis have an increased risk of developing antimicrobial - resistant salmonella infections ; such patients may be taking antimicrobial drugs because they have medical conditions that increase their risk for hospitalization ( 79 ) .
we doubt that this explains the differential hospitalization rate observed in our study , because the outbreaks we studied occurred in diverse community settings .
a second explanation for the higher hospitalization rate is that persons with resistant salmonella infections may fail empiric antimicrobial treatment , and their physicians subsequently hospitalize them for inpatient therapy .
a third explanation is that resistant salmonellae may be more virulent because of some unknown factor . in the united states ,
resistant salmonellae are more often associated with hospitalization and bloodstream infection compared to pansusceptible salmonellae ( 13 ) . in canada and denmark , studies have also found excess death rates associated with resistant salmonella infection ( 14,15 ) . in england and wales ,
a study found no association between resistance and bloodstream infection , but that study had substantial limitations , including the failure to use pansusceptible salmonellae as a referent group and the failure to adjust for confounders , such as age ( 16 ) . since the review of salmonella outbreaks published in 1984 , several changes have occurred in the epidemiology of antimicrobial - resistant salmonellae .
first , s. typhimurium dt104 has emerged as a cause of antimicrobial - resistant salmonella infections .
five outbreaks in this study were caused by s. typhimurium with r - type ac / kssut ; isolates with this resistance pattern are often dt104 ( 2,17 ) .
the hospitalization rate was higher in these 5 outbreaks ( median proportion hospitalized : 17% ) than in 3 outbreaks caused by pansusceptible s. typhimurium , which suggests that resistance or related factors , rather than just serotype , contribute to the differential rates of hospitalization .
second , a strain of s. newport resistant to at least 9 agents and with diminished susceptibility to ceftriaxone recently emerged in the united states ; 1 outbreak in this review was caused by this strain and had a hospitalization rate greater than that seen in most other resistant outbreaks ( 18 ) .
third , s. enteritidis has emerged as a frequent cause of foodborne outbreaks ( 19 ) .
s. enteritidis strains are infrequently resistant to antimicrobial agents , and in this review , s. enteritidis outbreaks were associated with low hospitalization rates . excluding s. enteritidis outbreaks did not change the results of our analysis . the previous analysis by holmberg et al .
found that the rate of death was significantly greater in outbreaks caused by resistant strains ( 4% ) compared with outbreaks caused by pansusceptible strains ( 0.2% ) ( 10 ) .
because this study covered a more recent period , improvements in medical care may explain the overall lower death rates .
studies with larger sample sizes are needed to determine whether antimicrobial resistance is associated with increased fatality rates .
state health departments investigate hundreds of salmonella outbreaks annually . occasionally , state health departments request assistance from cdc in investigating these outbreaks .
the reasons for such requests vary but may be related to size , severity , setting , or other features of the outbreak . while concern about a high hospitalization rate might encourage a state health department to request assistance from cdc in a salmonella outbreak , susceptibility results are usually not known initially and are unlikely by themselves to influence the request for assistance .
another limitation is that our study was based on final reports , not raw data . as a result
, we were unable to adjust for the different patient populations affected , including age , medical condition , and other factors that could affect hospitalization .
excluding outbreaks that occurred in healthcare settings may have reduced some of this bias . adjustment for serotype , which could also affect hospitalization rates , was also not possible because of the small sample size . despite these limitations
, we believe this study adds to the weight of evidence about the health effects of antimicrobial - resistant salmonellae .
the evidence now includes data from outbreaks and sporadic illness in the united states from 1970 to 2002 .
data from sporadic illness and 1 outbreak is also available from denmark ( 14,20 ) . across these diverse studies ,
such data about the adverse human health effects of resistant salmonellae should be incorporated into programs that promote appropriate antimicrobial use in humans and animals .
few studies have evaluated the health consequences of antimicrobial - resistant salmonella strains associated with outbreaks . among 32 outbreaks occurring in the united states from 1984 to 2002 , 
 22% of 13,286 persons in 10 salmonella - resistant outbreaks were hospitalized , compared with 8% of 2,194 persons in 22 outbreaks caused by pansusceptible salmonella strains ( p<0.01 ) .