Original Article
Quinolone-Resistant Campylobacter jejuni Infections in Minnesota, 1992–1998
N Engl J Med 1999; 340:1525-1532May 20, 1999
- Abstract
Background
Increasing resistance to quinolones among campylobacter isolates from humans has been reported in Europe and Asia, but not in the United States. We evaluated resistance to quinolones among campylobacter isolates from Minnesota residents during the period from 1992 through 1998.
Methods
All 4953 campylobacter isolates from humans received by the Minnesota Department of Health were tested for resistance to nalidixic acid. Resistant isolates and selected sensitive isolates were tested for resistance to ciprofloxacin. We conducted a case-comparison study of patients with ciprofloxacin-resistant Campylobacter jejuni isolated during 1996 and 1997. Domestic chicken was evaluated as a potential source of quinolone-resistant campylobacter.
Results
The proportion of quinolone-resistant C. jejuni isolates from humans increased from 1.3 percent in 1992 to 10.2 percent in 1998 (P<0.001). During 1996 and 1997, infection with quinolone-resistant C. jejuni was associated with foreign travel and with the use of a quinolone before the collection of stool specimens. However, quinolone use could account for no more than 15 percent of the cases from 1996 through 1998. The number of quinolone-resistant infections that were acquired domestically also increased during the period from 1996 through 1998. Ciprofloxacin-resistant C. jejuni was isolated from 14 percent of 91 domestic chicken products obtained from retail markets in 1997. Molecular subtyping showed an association between resistant C. jejuni strains from chicken products and domestically acquired infections in Minnesota residents.
Conclusions
The increase in quinolone-resistant C. jejuni infections in Minnesota is largely due to infections acquired during foreign travel. However, the number of quinolone-resistant infections acquired domestically has also increased, largely because of the acquisition of resistant strains from poultry. The use of fluoroquinolones in poultry, which began in the United States in 1995, has created a reservoir of resistant C. jejuni.
Media in This Article
Figure 2
Reported Cases of Quinolone-Resistant Campylobacter jejuni Infection among Minnesota Residents Who Did Not Use a Quinolone before Stool-Specimen Collection, Whose Infection Was Not Associated with an Outbreak, and Who Were Index Patients in Identified Clusters of Cases, According to Month and History of Foreign Travel, 1996–1998.Figure 1
Percentage of Campylobacter jejuni Isolates Obtained from Minnesota Residents and Submitted to the Minnesota Department of Health That Were Resistant to Nalidixic Acid (Top Panel) and Total Number of C. jejuni Isolates from Minnesota Residents Submitted (Bottom Panel), According to the Year and the Quarter, 1992–1998.Article Activity
- Article
Campylobacter jejuni is the most commonly recognized cause of bacterial gastroenteritis in the United States.1,2 When antibiotics are indicated for the treatment of campylobacter gastroenteritis, erythromycin or a fluoroquinolone such as ciprofloxacin is the drug of choice.3-5 Fluoroquinolones are frequently prescribed empirically for diarrheal illness, including traveler's diarrhea, because of their effectiveness against a range of enteric bacteria.3-7 Since the late 1980s, the resistance of campylobacter isolates to fluoroquinolones has been increasing, especially in Europe.8 Poultry is a major source of campylobacter infections in humans, and some European investigators have proposed a causal relation between the use of fluoroquinolones in animals and the increase in fluoroquinolone-resistant campylobacter infections in humans.8
Current trends in antibiotic-resistant campylobacter infections in the United States have not been well documented. In the United States, fluoroquinolones were first licensed for use in poultry in 1995. Therefore, we conducted a study of campylobacter isolates obtained from humans during the period from 1992 through 1998 as part of statewide surveillance activities to analyze recent trends in quinolone-resistant campylobacter infections, risk factors for infection with resistant organisms, and poultry as a potential source of resistant organisms.
Methods
Surveillance and Characterization of Isolates
Cases of illness caused by campylobacter have been reportable in Minnesota since 1979. The Minnesota Department of Health Public Health Laboratory serves as a statewide reference laboratory for the confirmation and identification of campylobacter infections.9 In 1995, the rules for reporting disease were changed to require the submission of isolates as part of the reporting process.
We screened all isolates received since 1992 for resistance to the quinolone antibiotic nalidixic acid with a preliminary disk-diffusion test.10 We also tested every fifth isolate, all resistant isolates, and all sensitive isolates from the 1996 portion of our case-comparison study for resistance to nalidixic acid by a standardized disk-diffusion test11 and for resistance to ciprofloxacin by the E test with use of a modification of the methods of Huang et al.12 We tested 20 randomly selected ciprofloxacin-resistant isolates from 1997 for resistance to grepafloxacin, levofloxacin, and trovafloxacin (by the E test) and to the veterinary fluoroquinolones enrofloxacin (by the E test) and sarafloxacin (by the disk-diffusion test). We tested 28 isolates from 1992 and 1993 and every fifth isolate from 1994 through 1997 for resistance to erythromycin and tetracycline by the E test.
E-test strips (AB Biodisk, Piscataway, N.J.) were applied to agar plates prepared from a Mueller–Hinton base (Difco, Detroit), supplemented with 5 percent lysed sheep's blood, and incubated at 37°C for 48 hours in a microaerophilic atmosphere (CampyPak, BBL Microbiology Systems, Cockeysville, Md.). We used interpretive criteria for Enterobacteriaceae and quality-control guidelines established by the National Committee for Clinical Laboratory Standards.13 Our definition of resistance to trovafloxacin, enrofloxacin, and sarafloxacin was the same as that of resistance to ciprofloxacin (a minimal inhibitory concentration of ≥4 μg per milliliter). Resistance to erythromycin was defined as a minimal inhibitory concentration greater than 8 μg per milliliter. Campylobacter isolates from 1996 and 1997 were subtyped by restriction-fragment–length polymorphism of the flagellin gene amplified by the polymerase chain reaction (PCR-RFLP).14
Comparison of Cases of Quinolone-Resistant and Quinolone-Sensitive C. jejuni Infection
Isolates obtained from Minnesota residents with C. jejuni infection during the period from 1996 through 1997 were classified as quinolone-sensitive or quinolone-resistant. A quinolone-resistant isolate was defined as having resistance to nalidixic acid on the standardized test; all resistant isolates were also resistant to ciprofloxacin. We matched each patient with a resistant isolate to two patients with sensitive isolates; patients were matched for age (within 10 years), residence (in the seven-county Minneapolis–St. Paul metropolitan area vs. elsewhere in Minnesota), and date of specimen collection.
Each patient answered a standardized questionnaire that included questions about clinical history, use of antibiotics after and during the month before the onset of illness, recent diarrheal illness and the use of antibiotics in household contacts, history of food consumption, contact with animals, and travel history. The period of interest for potential exposure, unless noted otherwise, was the seven days before the onset of illness. When patients could not answer questions about their use of antibiotics, we contacted their health care providers.
Evaluation of Retail Chicken Products
During the period from September 8 to November 3, 1997, we purchased 91 domestic chicken products in the Minneapolis–St. Paul metropolitan area from 16 retail markets representing 11 franchises. These products came from 15 poultry-processing plants in nine states. The products were various fresh or thawed items with and without the skin.
We cultured all chicken products for campylobacter,15 and we tested isolates for resistance to nalidixic acid and ciprofloxacin as described previously. For 76 products, we tested for resistance isolates from each product that was positive, using 3 to 10 campylobacter colonies from each product. The other 15 product samples were concentrated quantitatively, and serial dilutions were made in Mueller–Hinton broth (BBL Microbiology Systems). The samples were plated on Campy-BAP medium (BBL Microbiology Systems) in the presence of 8 μg of nalidixic acid per milliliter and in its absence. The concentration of agar was increased to 1.7 percent. We evaluated 1 nalidixic acid–resistant colony and 1 susceptible colony from each broth culture and 5 colonies of each from a dilution plate with 15 to 150 colonies. Isolates were subtyped by PCR-RFLP, and a random sample of ciprofloxacin-resistant isolates was tested for resistance to additional fluoroquinolones as described previously.
Statistical Analysis
Population estimates were obtained from Minnesota Health Statistics, 1994. 16 We determined univariate matched odds ratios, P values for tests for trend, and exact 95 percent confidence intervals with Epi Info software (version 6.04a, Centers for Disease Control and Prevention, Atlanta).17 Mantel–Haenszel chi-square tests were used in univariate matched analyses.17 We determined multivariate odds ratios and exact 95 percent confidence intervals with PC-SAS software (version 6.12, SAS Institute, Cary, N.C.) using exact conditional logistic regression with a forward, stepwise approach.18 Variables with a P value of 0.1 or less in univariate analysis were included in the multivariate model. Variables independently associated with the outcome variable were included in the final multivariate model. The Kruskal–Wallis test was used to compare groups of patients with respect to the duration of diarrhea.17 All reported P values are two-sided.
An outbreak was defined as two or more cases of campylobacter infection in separate households with a common epidemiologic exposure. A case cluster was defined as two or more cases occurring within two weeks of one another among members of the same household. Only the isolate from the first case in each outbreak was included in analyses of resistance to antibiotics. All outbreak-associated cases were excluded from the case-comparison study, and only the index case from identified clusters was included in the case-comparison study.
Results
Surveillance of Campylobacter and Resistance to Quinolones
During the period from 1992 through 1998, 6674 cases of campylobacter infection among Minnesota residents were reported to the Minnesota Department of Health. The median number of cases reported annually was 946 (range, 785 to 1181), with a median annual incidence of 20.7 cases per 100,000 population (range, 17.2 to 25.8). During the period from 1992 through 1998, 4953 viable campylobacter isolates from various patients (74 percent of all reported cases) were submitted to the Minnesota Department of Health; from 1996 through 1998, 91 percent of all isolates were submitted. C. jejuni constituted 95 percent of all campylobacter isolates. Seven outbreaks of C. jejuni infection were identified; six occurred during 1992, 1993, 1994, 1995, or 1998 and involved 71 C. jejuni isolates, all of which were sensitive to nalidixic acid. An outbreak in October 1997 among personnel of the Minnesota Army National Guard who were returning from training in Greece accounted for 29 C. jejuni isolates; all were resistant to nalidixic acid and ciprofloxacin.
After we excluded all except the initial case in each identified outbreak, the annual percentage of C. jejuni isolates that were resistant to nalidixic acid on the preliminary disk-diffusion test increased from 1.3 percent in 1992 to 10.2 percent in 1998 (chi-square for linear trend, 75.3; P<0.001) (Figure 1Figure 1
Percentage of Campylobacter jejuni Isolates Obtained from Minnesota Residents and Submitted to the Minnesota Department of Health That Were Resistant to Nalidixic Acid (Top Panel) and Total Number of C. jejuni Isolates from Minnesota Residents Submitted (Bottom Panel), According to the Year and the Quarter, 1992–1998.). The prevalence of nalidixic acid–resistant isolates exhibited a marked seasonality characterized by peaks during the first quarter and valleys during the third quarter of each calendar year (Figure 1).Ciprofloxacin resistance was confirmed in 285 C. jejuni isolates from the study period: 1 in 1993, 16 in 1994, 41 in 1995, 44 in 1996, 98 in 1997 (excluding all but the first isolate from the outbreak), and 85 in 1998. The minimal inhibitory concentration of ciprofloxacin was at least 32 μg per milliliter in the case of 274 of the ciprofloxacin-resistant isolates (96 percent). With use of the E test for resistance to ciprofloxacin as the standard, testing of 1230 isolates by the preliminary test for resistance to nalidixic acid resulted in a sensitivity of 99.6 percent, a specificity of 98.4 percent, a positive predictive value of 94.9 percent, and a negative predictive value of 99.9 percent.
All 20 ciprofloxacin-resistant C. jejuni isolates from 1997 that we tested were also resistant to grepafloxacin, trovafloxacin, enrofloxacin, and sarafloxacin. Seventeen of 20 isolates were resistant to levofloxacin; the other 3 isolates had intermediate levels of resistance. Minimal inhibitory concentrations of at least 32 μg per milliliter were noted for grepafloxacin (20 isolates), enrofloxacin (17 isolates), trovafloxacin (12 isolates), and levofloxacin (12 isolates). Eighteen of 827 clinical isolates (2 percent) obtained during 1992 through 1997 were resistant to erythromycin, and 501 (61 percent) were resistant to tetracycline. There were no significant changes in the proportion of isolates that were resistant to either of these antibiotics during the study period.
Comparison of Cases of Quinolone-Resistant and Quinolone-Sensitive C. jejuni Infection
Of the patients who had had a C. jejuni isolate submitted to the Minnesota Department of Health during the period from 1996 through 1997, 142 had quinolone-resistant isolates (including only the first patient in the 1997 outbreak), 1576 had quinolone-sensitive isolates, and 2 had isolates that were resistant to nalidixic acid on the preliminary test but that were not available for confirmation. Of the patients with quinolone-resistant C. jejuni infection, 130 (92 percent) were enrolled in the case-comparison study, along with 260 matched patients with quinolone-sensitive C. jejuni infection. Of the 12 patients with quinolone-resistant infection who were not enrolled, 6 patients were not the index patient in five household clusters, 1 patient was the first patient associated with the 1997 outbreak, and 5 patients could not be contacted.
The risk factors that were identified by univariate analysis are shown in Table 1Table 1
Potential Risk Factors for Infection with Quinolone-Resistant Campylobacter jejuni as Compared with Quinolone-Sensitive C. jejuni among Minnesota Residents, 1996–1997.. According to the multivariate analysis, the only variables independently associated with resistant C. jejuni infection were foreign travel, foreign travel to specific regions, and the use of a quinolone beginning one or more days before the collection of stool specimens (Table 1). Among patients who did not use quinolones before the collection of stool specimens, 78 of 133 patients (59 percent) who traveled abroad had a resistant isolate, whereas 24 of 222 patients (11 percent) who did not travel abroad had a resistant isolate.The use of a quinolone beginning one or more days before the collection of stool specimens occurred in 26 of the 130 patients with resistant C. jejuni infection (20 percent) and did not differ significantly according to the year or travel status (Table 2Table 2
Number of Patients in Minnesota with Quinolone-Resistant Campylobacter jejuni Infection Who Used a Quinolone before Culture, According to Foreign-Travel Status and Year, 1996–1997.). Twenty-four patients began treatment with a quinolone after the onset of illness but before the collection of stool specimens, and two patients took prophylactic ciprofloxacin while traveling. When patients were grouped according to their history of foreign travel, the use of a quinolone before the collection of stool specimens remained a significant risk factor for patients with resistant C. jejuni infection who had a history of foreign travel (matched odds ratio, 6.0; 95 percent confidence interval, 2.3 to 18.5) and those who did not (matched odds ratio, 16.0; 95 percent confidence interval, 2.2 to 710). Among patients who used a quinolone before the collection of stool specimens, the use began a median of 5 days (range, 1 to 30) before culture.Overall, 110 of the 130 patients with resistant C. jejuni infection (85 percent) were treated with an antibiotic, as compared with 212 of the 260 patients with sensitive C. jejuni infection (82 percent). Of the patients with resistant C. jejuni infection who were treated with an antibiotic, we identified the antibiotic used for 106 patients; 69 patients (65 percent) received a fluoroquinolone, and 26 patients (25 percent) received a macrolide. Of the 212 patients with sensitive C. jejuni infection who were treated, we identified the antibiotic used for 182; 115 patients (63 percent) received a fluoroquinolone, and 45 patients (25 percent) received a macrolide. Of the patients identified during 1997 who were treated with a fluoroquinolone after the collection of stool specimens, the duration of diarrhea was longer for the patients with quinolone-resistant C. jejuni infections (median, 10 days) than for the patients with quinolone-sensitive C. jejuni infections (median, 7 days; P=0.03).
Quinolone-Resistant Infections Acquired Domestically, 1996 to 1998
Figure 2Figure 2
Reported Cases of Quinolone-Resistant Campylobacter jejuni Infection among Minnesota Residents Who Did Not Use a Quinolone before Stool-Specimen Collection, Whose Infection Was Not Associated with an Outbreak, and Who Were Index Patients in Identified Clusters of Cases, According to Month and History of Foreign Travel, 1996–1998. shows the reported cases of quinolone-resistant C. jejuni infection during the period from 1996 through 1998 among Minnesota residents who did not use a quinolone before the collection of stool specimens, whose infection was not associated with an outbreak, and who were index patients in identified clusters of cases. When these criteria were used in the analysis, the percentage of confirmed C. jejuni infections that were resistant to quinolones and acquired domestically increased from 0.8 percent in 1996 to 3.0 percent in 1998 (chi-square for linear trend, 9.8; P=0.002). In 1998, 75 of 80 patients with quinolone-resistant infections (94 percent) did not use a quinolone before culture; when the data were combined with the data from 1996 and 1997, 179 of 210 patients with quinolone-resistant infections (85 percent) did not use a quinolone before culture.Evaluation of Retail Chicken Products
Of the 91 retail chicken products obtained, campylobacter was isolated from 80 (88 percent), including C. jejuni from 67 (74 percent) and C. coli from 19 (21 percent). Ciprofloxacin-resistant campylobacter was isolated from 18 products (20 percent), including resistant C. jejuni from 13 (14 percent) and resistant C. coli from 5 (5 percent). The minimal inhibitory concentration of ciprofloxacin was at least 32 μg per milliliter for all resistant isolates. Products that yielded resistant isolates were purchased at 11 retail markets representing eight franchises. They originated in seven poultry-processing plants in five states (Florida, Georgia, Minnesota, Missouri, and Ohio).
Eight of 11 campylobacter-positive chicken products (73 percent) tested quantitatively yielded a combination of species and types of resistance to ciprofloxacin; for example, 1 product yielded sensitive C. jejuni, sensitive C. coli, and resistant C. coli. Of eight ciprofloxacin-resistant C. jejuni isolates from chicken products, all were also resistant to grepafloxacin, trovafloxacin, enrofloxacin, and sarafloxacin; six isolates were resistant to levofloxacin, and the other two had intermediate levels of resistance.
Molecular Subtyping of C. jejuni Isolates from Humans and Retail Chicken Products
We identified 45 subtypes on PCR-RFLP among 269 typable C. jejuni isolates from patients in the case-comparison study of 1996 and 1997. Among the isolates from 1997, 5 subtypes were detected among quinolone-resistant isolates only, 24 among quinolone-sensitive isolates only, and 12 among both resistant and sensitive isolates.
Twelve subtypes were identified on PCR-RFLP among C. jejuni isolates from 13 positive chicken products. Three subtypes were detected among quinolone-resistant isolates only; five among quinolone-sensitive isolates only; and four among both resistant and sensitive isolates. Up to three subtypes were identified per product. Six of seven subtypes of quinolone-resistant C. jejuni identified among isolates from retail chicken products were also identified among quinolone-resistant C. jejuni isolates from humans. Among patients with infection in 1997 and excluding those who used a quinolone before culture, patients with quinolone-resistant C. jejuni infection that was acquired domestically were more likely to have a C. jejuni subtype that was also found among quinolone-resistant C. jejuni from chicken products than were patients with sensitive C. jejuni infection that was acquired domestically (12 of 13 vs. 40 of 90; odds ratio, 15.0; 95 percent confidence interval, 1.9 to 322) or patients with resistant C. jejuni infection that was associated with foreign travel (12 of 13 vs. 14 of 40; odds ratio, 22.3; 95 percent confidence interval, 2.5 to 508).
Discussion
Our study had six major findings. First, we documented an increase in quinolone resistance among human C. jejuni isolates, from 1.3 percent in 1992 to 10.2 percent in 1998. Second, seasonal peaks in quinolone resistance occurred that were primarily related to foreign travel during winter. Third, the rate of resistant infections that were acquired domestically also increased significantly from 1996 through 1998. Fourth, domestic chicken products obtained from retail markets in 1997 had high rates of contamination with ciprofloxacin-resistant C. jejuni. Fifth, we identified an association between molecular subtypes of resistant C. jejuni strains that were acquired domestically in humans and those found in chicken products. Poultry has been documented repeatedly as a major food reservoir of campylobacter for infections in humans2 and our data suggest that poultry is an important source of quinolone-resistant infections as well. Finally, the use of a quinolone before culture, shown previously to be capable of selecting for resistance in campylobacter,8 contributed to the increase in resistant isolates; however, this mechanism could account for a maximum of only 15 percent of resistant cases identified here.
The significant increase from 1996 through 1998 in quinolone-resistant C. jejuni infections that were acquired domestically is temporally associated with the recent licensure of fluoroquinolones (sarafloxacin in 1995 and enrofloxacin in 1996) for use in poultry in the United States. Published epidemiologic and laboratory data from other countries also provide evidence that the use of fluoroquinolones in poultry has had a primary role in increasing resistance to quinolones among C. jejuni isolates from humans.19-26 Treatment with enrofloxacin of broiler chickens infected with quinolone-sensitive C. jejuni does not eradicate the organism; rather, it selects for quinolone resistance in C. jejuni. 19 Enrofloxacin was introduced in the Netherlands for veterinary use in 1987 and has been used extensively as a therapeutic agent in poultry since that time.20 An increase in ciprofloxacin-resistant human campylobacter isolates in the Netherlands from 0 percent through 1985 to 11 percent in 1989 closely paralleled the increase in ciprofloxacin-resistant campylobacter isolates from retail poultry products.20 In Spain, an increase in the percentage of ciprofloxacin-resistant human campylobacter isolates from 0 to 3 percent in 1989 to 30 to 50 percent in 1991 coincided with the licensure of enrofloxacin for veterinary use in 1990.21-23 Ciprofloxacin-resistant campylobacter has also been isolated from retail poultry products in Spain,24 Taiwan,25 and the United Kingdom.26 These ecologic data support the selective pressure created by veterinary use of fluoroquinolones in increasing the reservoir of resistant campylobacter. Because the use of fluoroquinolones in poultry in the United States began only recently, we are probably documenting the early emergence of quinolone-resistant campylobacter in this country. Curtailing such use may reverse or slow this trend. It may be suggested that the increasing use of quinolones among humans is responsible for the increase in resistance among campylobacter isolates from humans. However, the association with poultry found by us and researchers in other countries is a more biologically plausible mechanism for the increase, especially when one considers that person-to-person transmission of campylobacter is not important epidemiologically.
Other researchers have associated fluoroquinolone-resistant campylobacter infections with travel or military deployment to many countries in Africa, Asia, and the Mediterranean.26-31 In our study, Mexico was the most frequent destination for patients with resistant C. jejuni infection. In Mexico, the amount of poultry meat produced increased from 0.77 billion kg (1.7 billion lb) in 1990 to 1.45 billion kg (3.2 billion lb) in 1997.32 Sales of quinolones in Mexico for use in poultry, including the fluoroquinolones ciprofloxacin, enrofloxacin, and danofloxacin, increased by a factor of approximately four from 86 million liters in 1993 to 326 million liters in 1997.33 Thus, the use of fluoroquinolones in poultry in Mexico may be an important contributor to infections with resistant C. jejuni among travelers to that country.
Fluoroquinolones shorten the duration and severity of symptoms caused by campylobacter gastroenteritis,34,35 and our data indicate that ciprofloxacin is frequently prescribed to treat this condition in Minnesota. In our small sample of 20 human isolates, ciprofloxacin-resistant isolates were also generally resistant to the newer fluoroquinolones used in human medicine. Tetracyclines, cited as an alternative choice for treatment,3-5 should not be used to treat campylobacter infections because of the high prevalence of resistance. In our study, the rates of resistance to erythromycin stayed low; therefore, this antibiotic may remain the most prudent choice for the treatment of campylobacter gastroenteritis.
Our findings highlight broader concern about the use of antibiotics in animals used for food and the development of resistant enteric pathogens. Partly because of the development of resistance to ciprofloxacin among multidrug-resistant Salmonella typhimurium definitive type 104 (DT104) in the United Kingdom36 and the presence of DT104 in the United States,37 in August 1997 the Food and Drug Administration banned the off-label use of fluoroquinolones in animals used for food. We believe that this ban is an appropriate and important measure for public health. In 1998, enrofloxacin was licensed for use in beef cattle in the United States. The use of fluoroquinolones in beef cattle should be monitored closely to detect any quinolone resistance in foodborne bacterial pathogens that may result from this practice. Despite these efforts, measures of control implemented in the United States alone will not be sufficient to curtail the development of quinolone resistance in foodborne bacterial pathogens. A well-coordinated international program is needed to assess worldwide use of antibiotics in animals used for food and to ensure appropriate limitations of such use if it is shown to be deleterious to human health.
Supported in part by a cooperative agreement (U50/CCU511190) with the Centers for Disease Control and Prevention as part of the Emerging Infections Program and through the Foodborne Diseases Active Surveillance Network (FoodNet) of the Emerging Infections Program. FoodNet is also supported by the Food and Drug Administration and the Department of Agriculture.
Source Information
From the Acute Disease Epidemiology Section (K.E.S., C.W.H., J.B.B., J.H.W., B.P.J., K.A.M., M.T.O.) and the Division of Public Health Laboratories (J.M.B., F.T.L.), Minnesota Department of Health, Minneapolis; and the Epidemic Intelligence Service, Epidemiology Program Office, Centers for Disease Control and Prevention, Atlanta (K.E.S.).
Address reprint requests to Dr. Smith at the Acute Disease Epidemiology Section, Minnesota Department of Health, 717 Delaware St. SE, Minneapolis, MN 55440-9441.
Members of the investigation team are listed in the Appendix.
Appendix
Members of the investigation team were Seth Baker, David Boxrud, Ami Buikema, Larry Carroll, Pamela Chapman, Craig Grimes, Jennifer Hall, Becky Huebner, John Hunt, Michelyn Jones, Peter Lynch, Carlota Medus, Tracy Miller, Kim Moore, Megha Mungekar, Megan Ryan, Kendra Schmidt, Scott Seys, Dana Soderlund, Dana Stephens, Maureen Sullivan, Ellen Swanson, and Charlott Taylor at the Minnesota Department of Health, Minneapolis; and Norman Danner, Mimi Derry, Demetria Downs, David Grussing, Henry Keizer, and Kevin Vought at the Minnesota Department of Agriculture, St. Paul.
- References
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Michael E. Ginevan. (2002) Assessment of the national antimicrobial resistance monitoring system (NARMS) and its value in critical decision-making. International Journal of Infectious Diseases 6, S8-S15
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Ronald L. Coulter, Mary K. Coulter, Jim L. Murrow. (2002) The Food Animal Supply and Its Related Concerns. Journal of Food Products Marketing 8:2, 33-64
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Janet G. Salisbury, Terence J. Nicholls, Anna M. Lammerding, John Turnidge, Michael J. Nunn. (2002) A risk analysis framework for the long-term management of antibiotic resistance in food-producing animals. International Journal of Antimicrobial Agents 20:3, 153-164
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David Tilman, Kenneth G. Cassman, Pamela A. Matson, Rosamond Naylor, Stephen Polasky. (2002) Agricultural sustainability and intensive production practices. Nature 418:6898, 671-677
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Eric J. Kasowski, Gary D. Gackstetter, Trueman W. Sharp. (2002) Foodborne illness: New developments concerning an old problem. Current Gastroenterology Reports 4:4, 308-318
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Michael Barza, Karin Travers. (2002) Excess Infections Due to Antimicrobial Resistance: The “Attributable Fraction”. Clinical Infectious Diseases 34:s3, S126-S130
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Wang-Huei Sheng, Yee-Chun Chen, Jann-Tay Wang, Shan-Chwen Chang, Kwen-Tay Luh, Wei-Chuan Hsieh. (2002) Emerging fluoroquinolone-resistance for common clinically important gram-negative bacteria in Taiwan. Diagnostic Microbiology and Infectious Disease 43:2, 141-147
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B. M. Allos. (2002) Reply. Clinical Infectious Diseases 34:5, 720-721
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Glenn S Tillotson. (2002) Natural might not be healthier. The Lancet Infectious Diseases 2:3, 136
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(2002) Policy Statements Adopted by the Governing Council of the American Public Health Association, October 24, 2001. American Journal of Public Health 92:3, 451-483
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(2002) Urinary Tract Infections and a Multidrug-Resistant Escherichia coli Clonal Group. New England Journal of Medicine 346:7, 535-536
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Billy Bourke. (2002) Campylobacter infection: small bowel and colon. Current Opinion in Gastroenterology 18:1, 4-9
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Douglas Steinke, Peter Davey. (2001) Association between Antibiotic Resistance and Community Prescribing: A Critical Review of Bias and Confounding in Published Studies. Clinical Infectious Diseases 33:s3, S193-S205
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Xilin Zhao, Karl Drlica. (2001) Restricting the Selection of Antibiotic‐Resistant Mutants: A General Strategy Derived from Fluoroquinolone Studies. Clinical Infectious Diseases 33:s3, S147-S156
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David C. Hooper. (2001) Minimizing Potential Resistance: The Molecular View—A Comment on Courvalin and Trieu‐Cuot. Clinical Infectious Diseases 33:s3, S157-S160
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David M. Bell. (2001) Promoting Appropriate Antimicrobial Drug Use: Perspective from the Centers for Disease Control and Prevention. Clinical Infectious Diseases 33:s3, S245-S250
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Edward C. Oldfield, Mark R. Wallace. (2001) THE ROLE OF ANTIBIOTICS IN THE TREATMENT OF INFECTIOUS DIARRHEA. Gastroenterology Clinics of North America 30:3, 817-835
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D. Guillemot, P. Courvalin, . (2001) Better Control of Antibiotic Resistance. Clinical Infectious Diseases 33:4, 542-547
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A. Sundsfjord, G. Skov Simonsen, P. Courvalin. (2001) Human infections caused by glycopeptide-resistant Enterococcus spp: are they a zoonosis?. Clinical Microbiology and Infection 7:4, 16-33
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Iruka N. Okeke, Robert Edelman. (2001) Dissemination of Antibiotic‐Resistant Bacteria across Geographic Borders. Clinical Infectious Diseases 33:3, 364-369
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Sherri Turnipseed. 2001. Drug Residues in Meat. .
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John W. Sanders, David R. Tribble. (2001) Diarrhea in the returned traveler. Current Gastroenterology Reports 3:4, 304-314
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D. Acheson, B. M. Allos. (2001) Campylobacter jejuni Infections: Update on Emerging Issues and Trends. Clinical Infectious Diseases 32:8, 1201-1206
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A. D. Harris, T. B. Karchmer, Y. Carmeli, M. H. Samore. (2001) Methodological Principles of Case-Control Studies That Analyzed Risk Factors for Antibiotic Resistance: A Systematic Review. Clinical Infectious Diseases 32:7, 1055-1061
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Irving Nachamkin. (2001) Campylobacter enteritis and the Guillain-Barré syndrome. Current Infectious Disease Reports 3:2, 116-122
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Pramil Singh. 2001. Does Low Meat Consumption Contribute to Greater Longevity?. , 135-170.
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Andrea G. Winquist, Aaron Roome, Roger Mshar, Terry Fiorentino, Patricia Mshar, James Hadler. (2001) Outbreak of Campylobacteriosis at a Senior Center. Journal of the American Geriatrics Society 49:3, 304-307
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Debra D. Poutsiaka. (2001) Antimicrobial Resistance in the Chronically Critically Ill Patient. Clinics in Chest Medicine 22:1, 87-103
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(2001) Policy statements adopted by the Governing Council of the American Public Health Association, November 15, 2000. American Journal of Public Health 91:3, 476-521
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(2001) Expanded family and medical leave. American Journal of Public Health 91:3, 477-478
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(2001) Support for a new campaign for universal health care. American Journal of Public Health 91:3, 490-491
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(2001) Drinking water quality and public health (position paper). American Journal of Public Health 91:3, 499-500
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(2001) Effective public health assessment, prevention, response, and training for emerging and re-emerging infectious diseases, including bioterrorism. American Journal of Public Health 91:3, 500-501
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(2001) Confirming need for protective national health-based air quality standards. American Journal of Public Health 91:3, 501-502
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(2001) Public health role of the National Fire Protection Association in setting codes and standards for the built environment. American Journal of Public Health 91:3, 503-504
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(2001) Raising income to protect health. American Journal of Public Health 91:3, 504-505
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(2001) Eliminating access barriers in public health meetings. American Journal of Public Health 91:3, 507-508
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(2001) Ensuring optimal vision performance in visually at risk drivers. American Journal of Public Health 91:3, 510-511
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(2001) Establishment of a Medicare prescription drug benefit. American Journal of Public Health 91:3, 519-519
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(2001) Condemnation of pharmaceutical manufacturers' retaliatory tactics. American Journal of Public Health 91:3, 521-521
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(2001) Joint resolution in support of National Public Health Performance Standards Program. American Journal of Public Health 91:3, 505a-506
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(2001) International trade policy and issues of improving access to drugs for HIV/AIDS and other life-threatening and disabling diseases. American Journal of Public Health 91:3, 505b-505
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(2001) International Digest of Health Legislation. American Journal of Public Health 91:3, 506a-507
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(2001) The need for continued and strengthened support for immunization programs. American Journal of Public Health 91:3, 506b-506
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(2001) International multilateral and bilateral debt relief. American Journal of Public Health 91:3, 508b-508b
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(2001) Resolution to improve the social conditions that contribute to health. American Journal of Public Health 91:3, 518b-518b
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(2001) Participation of health professionals in capital punishment. American Journal of Public Health 91:3, 520a-521a
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(2001) Support the framework for action on oral health in America: a report of the Surgeon General. American Journal of Public Health 91:3, 520c-520c
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Christopher J. Gill, Davidson H. Hamer. (2001) Foodborne illnesses. Current Treatment Options in Gastroenterology 4:1, 23-38
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R. L. Guerrant, T. Van Gilder, T. S. Steiner, N. M. Thielman, L. Slutsker, R. V. Tauxe, T. Hennessy, P. M. Griffin, H. DuPont, R. Bradley Sack, P. Tarr, M. Neill, I. Nachamkin, L. B. Reller, M. T. Osterholm, M. L. Bennish, L. K. Pickering. (2001) Practice Guidelines for the Management of Infectious Diarrhea. Clinical Infectious Diseases 32:3, 331-351
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John C. Christenson, Philip R. Fischer, Devon C. Hale, Debbie Derrick. (2001) Pediatric Travel Consultation in an Integrated Clinic. Journal of Travel Medicine 8:1, 1-5
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Andrew Gorske, Charles McQueen. (2001) Treatment of gastrointestinal infections. Current Opinion in Gastroenterology 17:1, 46-51
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Mary D. Barton. (2000) Antibiotic use in animal feed and its impact on human healt. Nutrition Research Reviews 13:02, 279
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E.John Threlfall, Linda R Ward, Jennifer A Frost, Geraldine A Willshaw. (2000) The emergence and spread of antibiotic resistance in food-borne bacteria. International Journal of Food Microbiology 62:1-2, 1-5
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EUGENE LEIBOVITZ, JACOB JANCO, LOLITA PIGLANSKY, JOSEPH PRESS, PABLO YAGUPSKY, HEINZ REINHART, IRIT YANIV, RON DAGAN. (2000) Oral ciprofloxacin vs. intramuscular ceftriaxone as empiric treatment of acute invasive diarrhea in children. The Pediatric Infectious Disease Journal 19:11, 1060-1067
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Burke A. Cunha. (2000) ANTIBIOTIC RESISTANCE. Medical Clinics of North America 84:6, 1407-1429
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Gerald Zirnstein, Leta Helsel, Yu Li, Bala Swaminathan, John Besser. (2000) Characterization of gyrA mutations associated with fluoroquinolone resistance in Campylobacter coli by DNA sequence analysis and MAMA PCR. FEMS Microbiology Letters 190:1, 1-7
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R. Carnevale, K. Molbak, F. Bager, F. M. Aarestrup. (2000) Fluoroquinolone Resistance in Salmonella: A Web Discussion. Clinical Infectious Diseases 31:1, 128-130
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Ryan, Edward T., Kain, Kevin C., . (2000) Health Advice and Immunizations for Travelers. New England Journal of Medicine 342:23, 1716-1725
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Donald S McLaren. (2000) A trawl through the current nutrition literature. Nutrition 16:2, 158-160
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D. C. Hooper. (2000) New Uses for New and Old Quinolones and the Challenge of Resistance. Clinical Infectious Diseases 30:2, 243-254
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Subhas Banerjee, J.Thomas LaMont. (2000) Treatment of gastrointestinal infections. Gastroenterology 118:2, S48-S67
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Abinash Virk, James M. Steckelberg. (2000) Clinical Aspects of Antimicrobial Resistance. Mayo Clinic Proceedings 75:2, 200-214
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Hilpi Rautelin, Maria-Liisa Hanninen. (2000) Campylobacters: the most common bacterial enteropathogens in the Nordic countries. Annals of Medicine 32:7, 440-445
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David W.K. Acheson. (1999) Foodborne infections. Current Opinion in Gastroenterology 15:6, 538
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Michael C. Powanda. (1999) Persons and pathogens: Consequences of co-existence. Inflammopharmacology 7:3, 199-205
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Gerald L. Mandell. (1999) Rational antibiotic use: Simple and not so simple. Current Infectious Disease Reports 1:3, 210-211
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