Emergence of Multidrug-Resistant Salmonella enterica SerotypeTyphimurium DT104 Infections in the United States
M. Kathleen Glynn, D.V.M., M.P.V.M., Cheryl Bopp, M.S., Wallis Dewitt, M.P.H., Paul Dabney, M.S., Mohammad Mokhtar, M.D., M.P.H., and Frederick J. Angulo, D.V.M., Ph.D.
Background Strains of salmonella that are resistant to antimicrobialagents have become a worldwide health problem. A distinct strainof Salmonella enterica serotype typhimurium, known as definitivetype 104 (DT104), is resistant to ampicillin, chloramphenicol,streptomycin, sulfonamides, and tetracycline and has becomea major cause of illness in humans and animals in Europe, especiallythe United Kingdom.
Methods To characterize typhimurium DT104 infections in theUnited States, we analyzed data collected by local and statehealth departments and public health laboratories between 1979and 1996 in national surveys of the antimicrobial-drug resistanceof salmonella. Selected typhimurium isolates with the five-drugpattern of resistance were phage typed.
Results The prevalence of typhimurium isolates with the five-drugpattern of resistance increased from 0.6 percent in 1979–1980to 34 percent in 1996. In 1994–1995, such isolates wereidentified in samples from 36 of the 46 surveillance sites (78percent). Thirty-nine of 43 typhimurium isolates with the five-drugpattern of resistance identified in 1994–1995 and 1996were phage type DT104 or a closely related phage type.
Conclusions Multidrug-resistant typhimurium DT104 has becomea widespread pathogen in the United States. More prudent useof antimicrobial agents in farm animals and more effective diseaseprevention on farms are necessary to reduce the disseminationof multidrug-resistant typhimurium DT104 and to slow the emergenceof resistance to additional agents in this and other strainsof salmonella.
Each year in the United States, there are an estimated 800,000to 4 million salmonella infections, and approximately 500 arefatal.1 Approximately 40,000 of these infections are confirmedby culture; isolates are serotyped at state public health laboratoriesand reported to the Centers for Disease Control and Prevention(CDC).2 Although most salmonella infections are self-limited,bacteremia occurs in 3 to 10 percent of reported, culture-confirmedcases, particularly in cases involving patients at the extremesof age or those who are immunocompromised.3,4,5,6,7 For thesepatients, appropriate antimicrobial-drug therapy can be lifesaving.1,3
In recent years, testing of salmonella isolates in the UnitedStates8,9 and abroad10,11 has shown that an increasing proportionof isolates are resistant to several antimicrobial agents. Inthe United Kingdom, the marked increase in the incidence ofa distinct multidrug-resistant strain of Salmonella entericaserotype typhimurium (hereafter referred to as typhimurium),characterized as definitive type 104 (DT104), that is resistantto five agents — ampicillin, chloramphenicol, streptomycin,sulfonamides, and tetracycline — has been of particularconcern. A recent report from the United Kingdom suggests thatinfections caused by this five-drug–resistant typhimuriummight be associated with greater morbidity and mortality thanother salmonella infections.12 Of further concern, 14 percentof such isolates that were identified in the United Kingdomin 1996 were also resistant to ciprofloxacin, and 24 percentwere resistant to trimethoprim; in each case the level of resistancewas 0 percent in 1991.13 We report on the widespread emergenceof typhimurium DT104 in the United States.
Methods
In the United States, state public health laboratories reportculture-confirmed cases of salmonella to the CDC by means ofthe Public Health Laboratory Information System, a nationwideelectronic reporting system. Information on the antimicrobial-drugresistance of salmonella is available from several sources:the National Antimicrobial Resistance Monitoring System establishedin 1996, the 1995 National Salmonella Antimicrobial ResistanceStudy, and surveys of antimicrobial-drug resistance that wereconducted in sentinel counties in 1979–1980, 1984–1985,1989–1990, and 1994–1995. We examined data collectedby these systems and surveys to identify reports of typhimuriumDT104.
Public Health Laboratory Information System
As a part of routine public health surveillance, most clinicallaboratories in the United States routinely forward salmonellaisolates to state or territorial public health laboratoriesfor serotyping, and state public health laboratories reportculture-confirmed salmonella infections, usually after serotyping,to epidemiologists in their state and to the CDC.2,14
National Antimicrobial Resistance Monitoring System
Salmonella isolates are not usually forwarded to the CDC; theexceptions are atypical or rare isolates sent for confirmatoryserotyping and those included in special surveys of antimicrobial-drugresistance. One such survey, the recently established NationalAntimicrobial Resistance Monitoring System, was begun in January1996 in collaboration with 12 state health departments (California,Colorado, Connecticut, Florida, Georgia, Kansas, Massachusetts,Minnesota, New Jersey, Oregon, Washington, and West Virginia)and 2 local health departments (Los Angeles County and New YorkCity) to monitor prospectively the patterns of antimicrobial-drugresistance of human salmonella isolates received at participatingpublic health laboratories.15 Participants forward every 10thsalmonella isolate to the CDC for testing for susceptibilityto antimicrobial agents. Isolates are tested with a Sensititresystem (Accumed International, Westlake, Ohio), which determinesthe minimal inhibitory concentration for 15 antimicrobial agents:ampicillin, amoxicillin–clavulanic acid, apramycin, ceftiofur,ceftriaxone, cephalothin, chloramphenicol, ciprofloxacin, gentamicin,kanamycin, nalidixic acid, streptomycin, sulfamethoxazole, tetracycline,and trimethoprim–sulfamethoxazole. After testing, a randomsample of typhimurium isolates that are resistant to ampicillin,chloramphenicol, streptomycin, sulfonamides, and tetracyclineare phage typed at the CDC,16 and strains are classified asDT104, DT104 complex (other closely related definitive typesor closely related untypable strains), or unrelated to DT104.
National Salmonella Antimicrobial Resistance Study
The second source of data on the resistance of salmonella toantimicrobial agents was the National Salmonella AntimicrobialResistance Study conducted between July 1, 1994, and June 30,1995. All state and territorial public health laboratories wereasked to forward every 10th salmonella isolate to the CDC forantimicrobial-drug–susceptibility testing. Isolates weretested by the disk–diffusion method for resistance to12 antimicrobial agents: ampicillin, amoxicillin–clavulanicacid, ceftriaxone, chloramphenicol, ciprofloxacin, gentamicin,kanamycin, nalidixic acid, streptomycin, sulfisoxazole, tetracycline,and trimethoprim–sulfamethoxazole.17 A random sample oftyphimurium isolates with resistance to ampicillin, chloramphenicol,streptomycin, sulfonamides, and tetracycline was sent to theDanish Veterinary Laboratory (Copenhagen, Denmark) and the WorldHealth Organization International Center for Enteric Phage Typing(Collindale, United Kingdom) for phage typing16; strains wereclassified as DT104, DT104 complex, or unrelated to DT104.
Periodic Surveys of Antimicrobial-Drug Resistance in Sentinel Counties
The third source of data was a series of surveys conducted inselected counties in the United States. These surveys were conductedevery five years in a volunteer panel of counties, initiallychosen in 1979.18 Trends in antimicrobial-drug resistance overtime were examined with the use of data from the 23 countiesthat participated in each of the surveys, conducted over one-yearperiods from July 1 to June 30 in 1979–1980,18 1984–1985,91989–1990,8 and 1994–1995. The participating countieswere in California, Massachusetts, New Jersey, New Mexico, NewYork, North Carolina, Ohio, Pennsylvania, Rhode Island, Texas,and Vermont. These health departments were asked to send allsalmonella isolates collected in their counties during the surveyperiods to the CDC, except those associated with an outbreak.In each of the surveys, the isolates were tested with the disk-diffusionmethod for resistance to nine antimicrobial agents: ampicillin,chloramphenicol, gentamicin, kanamycin, nalidixic acid, streptomycin,sulfisoxazole, tetracycline, and trimethoprim–sulfamethoxazole.17After testing, typhimurium isolates with the five-drug patternof resistance from the 1979–1980, 1984–1985, and1989–1990 surveys were phage typed at the CDC16; strainswere classified as DT104, DT104 complex, or unrelated to DT104.
Results
Public Health Laboratory Information System
In 1996, a total of 39,032 culture-confirmed salmonella infectionswere reported to the CDC by state public health laboratories.Of the 38,218 isolates that were serotyped, 9566 (25 percent)were classified as S. enterica serotype enteritidis, the mostcommonly identified serotype, and 9501 (25 percent) as typhimurium.Although the percentage of serotyped salmonella isolates thatare identified as S. enterica serotype enteritidis increasedfrom 16 percent in 1987 to 25 percent in 1996, reflecting adecade-long problem associated with contamination of eggs, thepercentage of typhimurium isolates identified during that periodincreased only slightly, from 24 percent to 25 percent.19
National Antimicrobial Resistance Monitoring System
In 1996, 1326 salmonella isolates were received at the CDC throughthe National Antimicrobial Resistance Monitoring System, and1239 (93 percent) were serotyped (Table 1). Three hundred six(25 percent) of the serotyped isolates were classified as typhimurium;103 of the 306 (34 percent) were resistant to ampicillin, chloramphenicol,streptomycin, sulfonamides, and tetracycline. Of 13 isolateswith the five-drug pattern of resistance that were phage typedat the CDC, 9 (69 percent) were identified as DT104, 2 as DT104complex, and 2 as having unrelated phage types. The five-drugpattern of resistance was identified in isolates from 12 of13 sites that submitted typhimurium isolates; more than 50 percentof the typhimurium isolates from California and Connecticuthad this pattern. Among the five antimicrobial drugs, the mostspecific marker for this pattern of resistance was resistanceto chloramphenicol: 103 of the 122 chloramphenicol-resistanttyphimurium isolates (84 percent) were also resistant to ampicillin,streptomycin, sulfonamides, and tetracycline. None of the 306typhimurium isolates were resistant to ciprofloxacin. One isolatewas resistant to nalidixic acid, but it did not have the five-drugpattern of resistance.
Table 1. Characteristics of Typhimurium Isolates Reported in Three Surveys of Antimicrobial-Drug Resistance in Salmonella in the United States, 1979 to 1996.
National Salmonella Antimicrobial Resistance Study
Patterns of resistance to antimicrobial agents were also determinedfor 4008 salmonella isolates received from 51 states or territoriesfrom July 1, 1994, through June 30, 1995, through the NationalSalmonella Antimicrobial Resistance Study, and 3903 (97 percent)were serotyped (Table 1). Of these 3903 isolates, 976 (25 percent)were identified as typhimurium, 275 (28 percent) of which wereresistant to ampicillin, chloramphenicol, streptomycin, sulfonamides,and tetracycline. Isolates resistant to these five drugs wereidentified at 36 of the 46 sites (78 percent) that submittedtyphimurium isolates, with the highest proportional prevalencein the western United States. The states in which more than40 percent of typhimurium isolates had this pattern of resistancewere California, Kentucky, Nevada, Oregon, Utah, and Washington.Thirty of the 275 isolates with the five-drug pattern of resistancethat were submitted to the CDC were phage typed: 25 (83 percent)were identified as DT104, 3 as DT104 complex, and 2 as unrelateddefinitive types.
In this series of isolates, resistance to chloramphenicol wasagain the most specific marker for the five-drug pattern ofresistance: 275 of the 285 chloramphenicol-resistant isolates(96 percent) had this pattern of resistance. None of the 701typhimurium isolates were resistant to ciprofloxacin. Two ofthe 275 isolates with the five-drug pattern of resistance (0.7percent) were also resistant to nalidixic acid, as comparedwith 3 of the 701 isolates (0.4 percent) with other patternsof resistance or no resistance; the median diameters and distributionsof the disk-diffusion zone for nalidixic acid were similar inthe two groups.
Periodic Surveys of Antimicrobial-Drug Resistance in Sentinel Counties
The periodic surveys conducted in the 23 selected counties furtherdemonstrated the emergence of a pattern of resistance to ampicillin,chloramphenicol, streptomycin, sulfonamides, and tetracyclineamong typhimurium isolates in the United States. The prevalenceof this pattern was 0.6 percent (1 of 162 isolates) in 1979–1980,5 percent (7 of 135) in 1984–1985, 7 percent (8 of 108)in 1989–1990, and 19 percent (31 of 166) in 1994–1995(Figure 1). Among the 16 such isolates identified between 1979and 1990, 1 (14 percent) in 1984–1985 and 3 (38 percent)in 1989–1990 were typed as DT104 or DT104 complex.
Figure 1. Prevalence of Resistance to Ampicillin, Chloramphenicol, Streptomycin, Sulfonamides, and Tetracycline among Typhimurium Isolates Identified by Surveys of Antimicrobial-Drug Resistance in Sentinel Counties.
Each survey was conducted from July 1 to June 30.
Discussion
In the past five years in the United States there has been widespreademergence of a strain of typhimurium that is resistant to fivemajor antibiotics: ampicillin, chloramphenicol, streptomycin,sulfonamides, and tetracycline. Although the number of casesof typhimurium infection reported to the CDC by means of thePublic Health Laboratory Information System has remained relativelyconstant over the past 15 years (excluding a large outbreakin 1985), the proportion of isolates with the five-drug patternof resistance has increased from less than 1 percent in 1979–1980to 34 percent in 1996. The great majority of these isolatesare probably DT104; since 1995, 91 percent of such isolatesthat were phage typed were identified as DT104 or as closelyrelated phage types included in the DT104 complex. Using datafrom these surveys, we estimate that of the 40,000 salmonellaisolates reported annually, 3400 are typhimurium with the five-drugpattern of resistance. Since previous studies have shown thatthe number of reported cases of salmonella infection representsonly 1 to 5 percent of the total number of cases,20 we estimatethat between 68,000 and 340,000 cases of infection with typhimuriumwith the five-drug pattern of resistance, most of which areprobably DT104, occur annually in the United States.
The sources of typhimurium DT104 with the five-drug patternof resistance remain to be determined. As early as 1985 andcoincident with its appearance in the United Kingdom, five-drug–resistanttyphimurium DT104 emerged in the United States, particularlyin western states. In contrast to the emergence of S. entericaserotype enteritidis,which was heralded by a dramatic increasein the number of related foodborne outbreaks,21 few outbreaksof typhimurium DT104 have been recognized in the United Statessince the first in 1996.22 In the United Kingdom, DT104 nowappears to be widely distributed in food animals, particularlycattle, and investigations have associated infections in humanswith eating pork sausages, chicken, and meat paste and withcontact with sick animals.12,23 Investigations in the UnitedStates have found associations between typhimurium DT104 infectionsin humans and the consumption of unpasteurized dairy productsand direct contact with livestock.24,25,26
The emergence of antimicrobial-drug resistance in salmonellaisolates is associated with the therapeutic and nontherapeuticuse of antimicrobial agents in food animals.27,28,29 In theface of the rapid emergence of DT104 and other resistant strainsof salmonella, in 1997 a World Health Organization group ofexperts reaffirmed recommendations to minimize the further emergenceof resistance to antimicrobial agents by, among other things,promoting the prudent use of antimicrobial agents in food animalsand ending the use as growth-promoting agents in food animalsof agents used in human medicine, such as penicillin and tetracycline,to which five-drug–resistant typhimuriumDT104 is resistant.30Although 14 percent of the five-drug–resistant typhimuriumDT104 isolates in the United Kingdom in 1996 were also resistantto ciprofloxacin,13 we did not identify any ciprofloxacin-resistantDT104 isolates in the United States. This difference may berelated to the fact that veterinary use of fluoroquinolones,approved in the United States in late 1995, is allowed onlyin poultry, and typhimurium DT104 might not yet be present inpoultry in the United States.
This study has some limitations. Data in the National AntimicrobialResistance Monitoring System and the periodic surveys of antimicrobial-drugresistance were collected from populations that may not be geographicallyrepresentative. Since these data were not, however, collectedspecifically for the study of typhimurium and since the isolatesforwarded to the CDC were randomly selected, any major biasis unlikely from this approach. Also, the appropriateness ofincluding multiple phage lysis patterns as a part of a largerDT104 complex and the epidemiologic importance of the DT104complex are not entirely clear.
Since data on clinical illness were not collected in the antimicrobialsurveys, there remains much to be learned about the spectrumof illness caused by typhimurium DT104. As with most salmonellainfections, treatment of these infections depends on the severityof illness. Antimicrobial-drug therapy is usually not essentialin cases of uncomplicated salmonella gastroenteritis; a fluoroquinolone,such as ciprofloxacin, or an extended-spectrum cephalosporin,such as ceftriaxone, remains the recommended treatment for invasivetyphimurium infections with the five-drug pattern of resistance.30
Typhimurium infections are common in the United States; it isthe second most commonly identified salmonella serotype andaccounted for 25 percent of culture-confirmed, serotyped casesof salmonella in 1996. Because typhimurium is common and fewlaboratories routinely subtype isolates, it is difficult todetect increases in specific strains. Continued and specificsurveillance, including a uniform method of subtyping isolates,is necessary to identify the extent to which DT104 might becontributing to the incidence of typhimurium infection in theUnited States. Currently used methods of subtyping typhimuriumisolates include phage typing, pulsed-field gel electrophoresis,and testing for susceptibility to antimicrobial agents; no onemethod, however, is capable of identifying five-drug–resistanttyphimurium DT104. Phage typing, which requires maintenanceof phage stocks and careful quality control, is available inonly a few public health laboratories in the world and providesno information about the antimicrobial-drug resistance of theorganism. The most common five-drug–resistant DT104 strainin the United States can be identified on the basis of its uniquepattern on pulsed-field gel electrophoresis, but other patternshave been reported, and the various patterns identified in differentlaboratories cannot be compared unless the technique has beencarefully standardized (Barrett T, CDC: personal communication).Testing for susceptibility to antimicrobial agents, particularlyscreening for resistance to chloramphenicol, appears to be agood screening procedure for identifying isolates with the five-drugpattern of resistance, but it is not routinely performed andmay not always be done according to the approved methods ofthe National Committee for Clinical Laboratory Standards.
Further epidemiologic studies are essential to devise a meansof preventing the transmission of five-drug–resistanttyphimurium DT104, a rapidly emerging pathogen in the UnitedStates. Until standardized laboratory procedures have been developed,state and local health departments and other interested personscan use resistance to chloramphenicol as a highly specific markerfor DT104 in order to prioritize the investigation of clustersof typhimurium infections. The sources of typhimurium with afive-drug pattern of resistance and the risk factors for infectionwith the organism must be identified, and the association betweenthe use of antimicrobial agents in food animals and the incidenceand continued emergence of these infections must be addressed.Prudent use of antimicrobial agents in farm animals and moreeffective disease prevention on farms are necessary to reducethe dissemination of five-drug–resistant typhimurium DT104and to slow the evolution of resistance to additional agentsin this and other strains of salmonella.
We are indebted to the participating local and state healthdepartments and public health laboratories in the Sentinel Countysurveys, the National Salmonella Antimicrobial Resistance Study,and the National Antimicrobial Resistance Monitoring System,and to Patricia Griffin, M.D., Laurence Slutsker, M.D., M.P.H.,Balasubr Swaminathan, Ph.D., and Robert Tauxe, M.D., M.P.H.,from the Foodborne and Diarrheal Diseases Branch, Division ofBacterial and Mycotic Diseases, National Center for InfectiousDiseases, Centers for Disease Control and Prevention, for theirassistance and comments in reviewing this article.
Source Information
From the Foodborne and Diarrheal Diseases Branch, Division of Bacterial and Mycotic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta (M.K.G., C.B., W.D., M.M., F.J.A.), and the Food and Drug Administration, Rockville, Md. (P.D.).
Address reprint requests to Dr. Glynn at the Foodborne and Diarrheal Diseases Branch, Centers for Disease Control and Prevention, 1600 Clifton Rd., MS A-38, Atlanta, GA 30333.
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