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Running conditions consisted of 1 phase from 2. All isolates from Denmark and Thailand and 7 of the food isolates from the United States were typed at the Danish Institute for Food and Veterinary Research; the remaining isolates from the United States were typed by PulseNet-participating state and local health departments, with the PFGE patterns submitted to the PulseNet database.

Nalidixic acid resistance was not found in pig, pork, or turkey meat isolates Table. All nalidixic acid—resistant isolates from Denmark also displayed reduced susceptibility to ciprofloxacin. All nalidixic acid—resistant isolates from Thailand also exhibited reduced susceptibility to ciprofloxacin; 12 isolates 10 from persons and 2 from chickens were resistant to ciprofloxacin.

Mutated bases are shown in boldface. All nalidixic acid—resistant isolates from the United States also showed decreased susceptibility to ciprofloxacin; 16 of the 17 nalidixic acid—resistant isolates from persons and the isolate from an imported dehydrated whole chili from Thailand were resistant to ciprofloxacin. The most common pattern 58 isolates, JM6X The second most common pattern 44 isolates, JM6X The third most common pattern 34 isolates, JM6X Two additional patterns are noteworthy.

One pattern 18 isolates, JM6X Another pattern 14 isolates, JM6X This is the pattern from the previously described outbreak of ciprofloxacin-resistant S. Schwarzengrund infections in medical facilities in Oregon 9. Of these, 11 were found among 14 human isolates, 10 among the 26 isolates from pigs and pork, 7 among the 19 chicken meat isolates, and 4 among the 9 turkey meat isolates. Forty-three different PFGE types were found among the isolates from Thailand; 25 of these were found among the 57 human isolates and 25 among the 48 chicken meat isolates.

Four of the 6 PFGE types, involving 7 of the 14 isolates found among persons and chickens in Denmark, were also observed among persons and chicken meat in Thailand. Both ill persons in Denmark who reported travel to Thailand in the 30 days before specimen collection were infected with 1 of the PFGE types common in Denmark and Thailand.

These 4 PFGE types included the most common type among persons and chickens in Denmark and the 2 most common types among persons and chickens in Thailand. Among the isolates from the United States, different PFGE types were found; of these were found among the human isolates and 12 among the 13 food and food animal isolates.

All 8 food isolates with types also found in persons were found in foods imported to the United States, including food imported from Thailand. Foodborne diseases caused by nontyphoidal Salmonella spp.

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In the United States nontyphoidal Salmonella spp. Historically, Salmonella serotypes Enteritidis and Typhimurium have been the most important causes of nontyphoidal salmonellosis. Schwarzengrund is a less common cause of human salmonellosis worldwide. In recent years, however, the relative incidence of this serovar seems to have increased 6 , 8. It now ranks among the 20 most frequently identified Salmonella serovars in several countries, including Slovakia, New Zealand, Venezuela, and Thailand; is among the 40 most frequently identified serovars in Denmark and the United States; and was the fifth most common serovar isolated from retail meat in the United States in , associated exclusively with poultry products.

Other studies also suggest that poultry could be the most common reservoir 6 , 28 , This study showed a high frequency of antimicrobial drug resistance, including an unusually high prevalence of nalidixic acid resistance, among S. Schwarzengrund isolates from chickens in Denmark, persons and chickens in Thailand, and food products imported into the United States. In contrast, the frequency of resistant isolates from pigs and turkey meat in Denmark was low.

The prevalence of resistance among isolates from persons in Denmark was intermediate compared with the high level in persons and chickens in Thailand and the low level in Danish food animals. Schwarzengrund from chickens to persons in Thailand, and transmission from chickens, pigs, and turkeys to persons in Denmark. Schwarzengrund isolates. Fluoroquinolone ciprofloxacin resistance among Salmonella spp. These positions, located in the quinolone resistance—determining region of gyrA , are commonly reported among numerous bacterial species, including Salmonella isolates with a high-level of ciprofloxacin resistance 30 — A ciprofloxacin-resistant strain of S.

Schwarzengrund recently caused a nosocomial outbreak involving 2 nursing homes and 1 hospital in Oregon 9. The index patient in the Oregon outbreak was initially hospitalized in the Philippines. In many countries, including Denmark, fluoroquinolones are the drugs of choice for treating complicated gastrointestinal infections.

Thus, resistance to this group of antimicrobial agents is especially critical, both for management of salmonellosis and because of the association of resistance with increased illness and death 19 , To our knowledge, this is the first study of the molecular epidemiology of S. The study demonstrated a substantial diversity in PFGE patterns of this serotype with the presence of several common international clones. The PFGE types of isolates from persons and chicken meat in Thailand formed overlapping populations, with more than half of the isolates from both sources belonging to shared types.

This supports the involvement of chicken meat as a reservoir for human S. Schwarzengrund infections in Thailand. The epidemiology of S. Schwarzengrund infections in Denmark is complicated. Although some PFGE types were only found among isolates from pigs, several PFGE types were shared among isolates from persons and pigs; persons, chicken meat, and turkey meat; and persons and chicken meat.

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This suggests that chicken meat, pork, and turkey meat are sources of S. Schwarzengrund infections for persons in Denmark. Because modern trade and distribution of food products makes it difficult to determine the country of origin of meat samples sold retail in Denmark, the sources of the chicken meat, pork, and turkey meat included in this study are not completely known.

However, Denmark has been importing an increasing amount of chicken meat, and much of this imported chicken is from Thailand. In addition, S. Schwarzengrund has, to our knowledge, not been detected in the Danish production of chicken. These data, with the identification of identical PFGE types from persons and chickens in both Denmark and Thailand, support the possibility that some persons in Denmark acquired S. Schwarzengrund from imported chicken meat from Thailand.

A limited number of isolates from food and food animals in the United States were included in this study.


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The prevalence of S. Schwarzengrund in retail meat was low in , with only 3 isolates recovered. In addition, PFGE data on isolates from food animals were not available for comparison in this study. The study would have benefited from additional isolates, especially from food and food animals in the United States. Nevertheless, a high proportion of these available isolates from food and food animals shared PFGE patterns with human isolates. In addition, several patterns found among human isolates in the United States were also present among human isolates in Denmark and Thailand, which suggests an international spread of these clones.

Specifically, 1 PFGE type that was frequently ciprofloxacin resistant was found in a person in Denmark, in persons and chicken meat in Thailand, and in persons and the dehydrated whole chili imported from Thailand to the United States. Another PFGE type that was nalidixic acid—resistant was found in persons and chicken meat in Denmark, persons in the United States, and in catfish imported from Thailand to the United States. In our study and other studies, Salmonella isolates from imported food in Denmark had a higher frequency of resistance than was found in domestically produced meats A study from the United States also reported a high frequency of antimicrobial drug resistance among Salmonella isolates from imported food Food is an important vehicle for the national and international dissemination of Salmonella spp.

This study supports the conclusion that multidrug-resistant, including nalidixic acid—resistant, S. Schwarzengrund was likely disseminated internationally by chicken products from Thailand. Because antimicrobial drug resistance among Salmonella isolates from food animals commonly reflects antimicrobial drug use in food animals, efforts are needed to ensure appropriate use of antimicrobial agents in food animals and to improve food safety to reduce dissemination of Salmonella spp.

Pulsed-field gel electrophoresis types among Salmonella enterica serovar Schwarzengrund isolates from various sources in Denmark, Thailand, and the United States. We are grateful to Christina Svendsen for technical assistance, Ole A. Jensen for providing strains and data for infections in persons in Denmark.

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His main research interest is the evolution and spread of antimicrobial-resistant bacteria in the food chain. International spread of multidrug-resistant Salmonella Schwarzengrund in food products. Emerg Infect Dis [serial on the Internet]. Europe PMC requires Javascript to function effectively. Recent Activity. The snippet could not be located in the article text.