Antimicrobial drug resistance of Salmonella isolates from meat and humans, Denmark.We compared 8,144 Salmonella salmonella Any of the rod-shaped, gram-negative, non-oxygen-requiring bacteria that make up the genus Salmonella. Their main habitat is the intestinal tract of humans and other animals. isolates collected from meat imported to or produced in Denmark, as well as from Danish patients. Isolates from imported meat showed a higher rate of antimicrobial antimicrobial /an·ti·mi·cro·bi·al/ (-mi-kro´be-al) 1. killing microorganisms or suppressing their multiplication or growth. 2. an agent with such effects. drug resistance, including multidru9 resistance, than did isolates from domestic meat. Isolates from humans showed resistance rates lower than those found in imported meat but higher than in domestic meat. These findings indicate that programs for controlling resistant Salmonella spp. are a global issue. ********** Salmonella spp. are among the most common causes of human bacterial gastroenteritis
Bacterial gastroenteritis is an inflammation of the stomach and intestines caused by bacteria or bacterial toxins. worldwide, and food animals are important reservoirs of the bacteria (1). In recent years, an increase in the occurrence of antimicrobial drug-resistant Salmonella spp. has been observed in several countries (2-5). Fatality rates fa·tal·i·ty rate n. See death rate. fatality rate see case fatality rate. are higher for patients with infections caused by drug-resistant Salmonella spp., and these patients are more likely to require hospitalization hospitalization /hos·pi·tal·iza·tion/ (hos?pi-t'l-i-za´shun) 1. the placing of a patient in a hospital for treatment. 2. the term of confinement in a hospital. and to be hospitalized for longer periods than are patients with infections caused by antimicrobial drug susceptible Salmonella spp. (6,7). Antimicrobial drug resistance of Salmonella spp. isolated from food animals in Denmark has so far been relatively low (8). However, an estimated 30% of all poultry, 10% of all pork, and 50% of all beef sold in Denmark is imported (9). Imported meat is therefore an important potential source of human infection with drug-resistant Salmonella spp. We compared antimicrobial drug resistance of Salmonella isolates from both imported meat and meat produced within Denmark (domestic meat), as well as from outpatients with diarrhea diarrhea (dīərē`ə), frequent discharge of watery feces from the intestines, sometimes containing blood and mucus. It can be caused by excessive indulgence in alcohol or other liquids or foods that prove irritating to the stomach or . Salmonella isolates from humans and meat were obtained from July 1998 through June 2002. Isolates from domestic poultry, pork, and beef were obtained through the national Salmonella control program (10), and isolates from imported poultry, pork, and beef were obtained from the Denmark import control and from the regional food control units. Human salmonellosis salmonellosis (săl'mənĕlō`sĭs), any of a group of infectious diseases caused by intestinal bacteria of the genus Salmonella, is a notifiable disease no·ti·fi·a·ble disease n. A disease that must be reported to public health authorities at the time it is diagnosed because it is potentially dangerous to human or animal health. Also called reportable disease. in Denmark, and all human Salmonella spp. isolates are collected at the Statens Serum Institute. The serovars included were restricted to S. Typhimurium, S. Hadar, S. Dublin, S. Saintpaul, S. Enteritidis, S. Virchow, and S. Newport because these were the serovars of which a sufficient number of isolates had been tested for antimicrobial drug susceptibility susceptibility the state of being susceptible. Refers usually to infectious disease but may be to physical factors such as wetting or to psychological factors such as harassment. . Data on 4,081 Salmonella isolates from humans were included in the study. Identification, serotyping, phage phage: see bacteriophage. phage - A program that modifies other programs or databases in unauthorised ways; especially one that propagates a virus or Trojan horse. See also worm, mockingbird. The analogy, of course, is with phage viruses in biology. typing, and susceptibility testing susceptibility test Antimicrobial susceptibility test, see there were done as described (8,11,12). Susceptibility to the following antimicrobial agents Antimicrobial agents Chemical compounds biosynthetically or synthetically produced which either destroy or usefully suppress the growth or metabolism of a variety of microscopic or submicroscopic forms of life. was determined: ampicillin ampicillin (ăm'pĭsĭl`ĭn), a penicillin-type antibiotic that is effective against both gram-negative microorganisms and gram-positive microorganisms such as Escherichia coli. , ceftiofur, chloramphenicol chloramphenicol (klōr'ămfĕn`əkŏl'), antibiotic effective against a wide range of gram-negative and gram-positive bacteria (see Gram's stain). It was originally isolated from a species of Streptomyces bacteria. , ciprofloxacin ciprofloxacin /cip·ro·flox·a·cin/ (sip?ro-flok´sah-sin) a synthetic antibacterial effective against many gram-positive and gram-negative bacteria; used as the hydrochloride salt. cip·ro·flox·a·cin n. , co-amoxiclav, colistin colistin /co·lis·tin/ (ko-lis´tin) an antibiotic produced by Bacillus polymyxa var. colistinus, related to polymyxin and effective against many gram-negative bacteria; used as the sulfate salt. , florphenicol, gentamicin gentamicin /gen·ta·mi·cin/ (jen?tah-mi´sin) an aminoglycoside antibiotic complex isolated from bacteria of the genus Micromonospora, , nalidixic acid nalidixic acid /nal·i·dix·ic ac·id/ (nal-i-dik´sik) a synthetic antibacterial agent used in the treatment of genitourinary infections caused by gram-negative organisms. na·li·dix·ic acid n. , neomycin neomycin (nē'ōmī`sĭn), broad spectrum antibiotic effective against both gram positive and gram negative bacteria (see Gram's stain). , streptomycin streptomycin (strĕp'tōmī`sĭn), antibiotic produced by soil bacteria of the genus Streptomyces and active against both gram-positive and gram-negative bacteria (see Gram's stain), including species resistant to other , sulfamethoxazole sulfamethoxazole /sul·fa·meth·ox·a·zole/ (-meth-ok´sah-zol) a sulfonamideantibacterial and antiprotozoal, particularly used in acute urinary tract infections. sul·fa·me·thox·a·zole n. , tetracycline tetracycline (tĕ'trəsī`klēn), any of a group of antibiotics produced by bacteria of the genus Streptomyces. They are effective against a wide range of Gram positive and Gram negative bacteria, interfering with protein , and trimethoprim trimethoprim /tri·meth·o·prim/ (-meth´o-prim) an antibacterial closely related to pyrimethamine; almost always used in combination with a sulfonamide, primarily for the treatment of urinary tract infections. . Statistical analyses were performed using S-PLUS version 6.2 (Insightful Corp., Seattle, WA, USA). The trend in the occurrence of resistant isolates over time, the occurrence of multidrug-resistant isolates over time, and the occurrence of nalidixic acid resistant isolates were investigated by fitting a logistic-regression model with origin (domestic/imported), time (year), product type (beef, pork, poultry), and all 2-way interactions as explanatory ex·plan·a·to·ry adj. Serving or intended to explain: an explanatory paragraph. ex·plan variables. The regression models were reduced by using a likelihood ratio test. Significance in all 2-by-2 tables (only tables with minimum 30 domestic and 30 imported samples) was tested by a Pearson [chi square chi square (kī), n a nonparametric statistic used with discrete data in the form of frequency count (nominal data) or percentages or proportions that can be reduced to frequencies. ] test with continuity correction In probability theory, if a random variable X has a binomial distribution with parameters n and p, i.e., X is distributed as the number of "successes" in n independent Bernoulli trials with probability p ; if the number in any cell in the contingency table contingency table n. A statistical table that shows the observed frequencies of data elements classified according to two variables, with the rows indicating one variable and the columns indicating the other variable. was <5, Fisher exact test was applied. All tests were done on a 5% significance level (p<0.05). No correction for multiple testing was done. An isolate was considered multidrug resistant if the isolate was resistant to [greater than or equal to] 4 antimicrobial agents. Salmonella spp. were isolated from 1,078 (11.8%) of 9,135 samples from imported poultry, pork, and beef and 2,985 (1.4%) of 213,214 samples from domestic poultry, pork, and beef. Among the isolates from domestic meat, the serovars S. Typhimurium, S. Infantis, and S. Derby were the 3 most frequently isolated; in imported meat, the 3 most frequently isolated serovars were S. Heidelberg, S. Typhimurium, and S. Hadar (Table 1). In isolates from domestic meat originating from pigs and poultry, S. Typhimurium was the most frequently isolated serovar; in beef isolates, S. Dublin was most common. Among isolates from imported meat, S. Typhimurium was the most frequently isolated serovar from pork and beef, while S. Heidelberg was the most frequently isolated serovar from poultry. A significantly higher ([chi square], p<0.001) proportion of the Salmonella spp. isolates from imported meat (58%) were resistant to [greater than or equal to] 1 antimicrobial agents compared with isolates from domestic meat (26%) (Table 1). A significant difference ([chi square], p<0.001) was also observed between the proportions of multidrug-resistant isolates from domestic (4%) compared with imported (28%) poultry, pork, and beef. The regression results (Table 2) showed a significant increase in the proportion of resistant (p<0.001) and multidrug-resistant (p = 0.015) isolates over time and an increase in odds per year of 27% (corresponding to an increase in probability of 5% per year) and 14% (corresponding to an increase in probability of 3% per year), respectively (Figure 1). Furthermore, the probability for isolating a resistant and a multidrug-resistant isolate from imported meat compared with domestic meat was significant, with an odds ratio of [approximately equal to] 5. The probability of isolating a resistant isolate differed between product types; pork had the highest probability, followed by poultry and beef. [FIGURE 1 OMITTED] A high proportion of resistant and multidrug-resistant isolates was found among S. Hadar, S. Newport, S. Typhimurium, and S. Heidelberg in imported meat (Table 1). Among S. Typhimurium, antimicrobial drug resistance was particularly prominent in the phage types DT104, DT170, DT193, DT120, DT208, DT107, U302, and DT135 (Table 3). Multidrug-resistant DT104, DT120, 2and DT193 were found in both domestic and imported poultry, pork, and beef, whereas multidrug-resistant DT107, DT170, and DT208 were more common in domestic meat, and multidrug-resistant U302 was more common in imported meat (Table 3). Resistance to nalidixic acid was higher among isolates from imported meat (26%) compared with isolates from domestic meat (4%) ([chi square], p<0.001, odds ratio = 6.54, Table 3), with an increase over time in the proportion of domestic nalidixic acid resistant isolates (p = 0.004, data not shown). Furthermore, the probability of isolating a nalidixic 2acid-resistant isolate differed between product types; poultry (domestic 14%, imported 30%) had the highest probability, followed by pork (domestic 1%, imported 3.2%) and beef (domestic 1%, imported 0%). Nalidixic acid resistance among Salmonella spp. from imported products was highest among S. Hadar, S. Newport, S. Kottbus, and S. Virchow (Table 1). For S. Typhimurium, S. Hadar, and S. Virchow, the proportion of resistant and multidrug-resistant isolates was much higher among isolates from humans than among isolates from domestic meat (Table 1, Figure 2). For S. Dublin and S. Enteritidis, the proportion of resistant and multidrug-resistant isolate did not differ between the meat sources and the human isolates, whereas for S. Saintpaul and S. Newport the rates of resistance and multidrug resistance multidrug resistance, n the adaptation of tumor cells or infectious agents to resist chemotherapeutic agents. were lower for isolates from humans than from both domestic and imported meat. [FIGURE 2 OMITTED] S. Hadar, S. Virchow, S. Newport, and S. Heidelberg were frequently found in imported products but rarely found in domestic products. Isolates that belong to these serovars are common causes of human salmonellosis in Denmark (13). Overall, a significantly higher number of resistant and multidrug-resistant Salmonella isolates were found among isolates from imported poultry, pork, and beef compared with domestic products. This finding implies that consumers in Denmark are more likely to be exposed to drug-resistant Salmonella spp. when eating imported compared with domestic meat. An increase in the occurrence of resistance over time was also observed among isolates from both domestic and imported meat; this is in agreement with observations worldwide (2-5). Antimicrobial agents might not be essential for treatment of gastroenteritis gastroenteritis: see enteritis. gastroenteritis Acute infectious syndrome of the stomach lining and intestines. Symptoms include diarrhea, vomiting, and abdominal cramps. caused by Salmonella spp., but they are essential for treatment of patients with invasive infections. In particular, the frequent occurrence of resistance to quinolones is a matter of concern because these compounds are often used for first treatment of serious human infections, before the results of susceptibility testing are available. International trade of food products is expected to increase in the future. Thus, endeavors to improve food safety must take into account the importance of resistant Salmonella spp. in imported food products and, through international agreements, limit contamination with antimicrobial drug-resistant Salmonella spp. at the primary production site. Acknowledgement We thank the Danish Veterinary and Food Administration for providing import control data. This study was supported by the National Food Institute, Copenhagen. Dr Skov is senior researcher in the Research Unit for Clinical Microbiology Clinical microbiology The adaptation of microbiological techniques to the study of the etiological agents of infectious disease. Clinical microbiologists determine the nature of infectious disease and test the ability of various antibiotics to inhibit or kill at the University of Southern Denmark As a national institution the University of Southern Denmark (SDU) comprises five faculties – Humanities, Science, Engineering, Social Sciences and Health Sciences totaling 32 departments, 11 research centers and a university library. . Her main research interests are the epidemiology epidemiology, field of medicine concerned with the study of epidemics, outbreaks of disease that affect large numbers of people. Epidemiologists, using sophisticated statistical analyses, field investigations, and complex laboratory techniques, investigate the cause and genotyping Genotyping refers to the process of determining the genotype of an individual with a biological assay. Current methods of doing this include PCR, DNA sequencing, and hybridization to DNA microarrays or beads. of foodborne Salmonella spp. References (1.) Humphrey TJ. Public-health aspects of Salmonella infections. In: Wray C, Wray A, editors. Salmonella in domestic animals. Wallingford (England): CABI CABI Commonwealth Agricultural Bureaux International (UK) CABI Centre for Agriculture and Biosciences International (UK) CABI Colorado Association of Business Intermediaries CABI California Birth Index Publishing; 2000. (2.) Cailhol J, Lailler R, Bouvet P, La Vieille S, Gauchard F, Sanders San´ders n. 1. An old name of sandalwood, now applied only to the red sandalwood. See under Sandalwood. P, et al. Trends in antimicrobial resistance phenotypes in non-typhoid salmonellae from human and poultry origins in France. Epidemiol Infect infect /in·fect/ (in-fekt´) 1. to invade and produce infection in. 2. to transmit a pathogen or disease to. in·fect v. 1. . 2006;134:171-8. (3.) Hoge CW, Gambel JM, Srijan A, Pitarangsi C, Echeverria P. Trends in antibiotic resistance antibiotic resistance, n the ability of certain strains of microorganisms to develop resistance to antibiotics. antibiotic resistance among diarrheal pathogens isolated in Thailand over 15 years. Clin infect Dis. 1998;26:341-5. (4.) Davis MA, Hancock DD, Besser TE, Rice DH, Gay JM, Gay C, et al. Changes in antimicrobial resistance among Salmonella enterica Salmonella enterica is a rod shaped, flagellated, Gram-negative bacterium, and a member of the genus Salmonella.[1] Serovars S. enterica has an extraordinarily large number of serovars serovar Typhimurium isolates from humans and cattle in the Northwestern United States Noun 1. northwestern United States - the northwestern region of the United States Northwest western United States, West - the region of the United States lying to the west of the Mississippi River , 1982-1997. Emerg Infect Dis. 1999;5:802-6. (5.) van Duijkeren E, Wannet WJ, Houwers DJ, van Pelt van Pelt is the surname of several people: People
(6.) Helms M, Vastrup P, Gerner-Smidt P, Molbak K. Excess mortality associated with antimicrobial drug-resistant Salmonella Typhimurium Salmonella ty·phi·mu·ri·um n. A bacterium that causes food poisoning. . Emerg Infect Dis. 2002;8:490-5. (7.) Varma JK, Molbak K, Barrett TJ, Beebe JL, Jones TF, Rabatsky-Ehr T, et al. Antimicrobial-resistant nontyphoidal Salmonella is associated with excess bloodstream blood·stream n. The flow of blood through the circulatory system of an organism. bloodstream the blood flowing through the circulatory system in the living body. infections and hospitalizations. J Infect Dis. 2005;191:554-61. (8.) Aarestrup FM, Bager F, Jensen NE, Madsen M, Meyling A, Wegener HC. Resistance to antimicrobial agents used for animal therapy in pathogenic-, zoonotic- and indicator bacteria Each gram of human feces contains approximately 10 billion (109) bacteria, among them may include pathogenic bacteria, such as Salmonella, associated with gastroenteritis. In addition, feces may contain pathogenic viruses, protozoa and parasites. isolated from different food animals in Denmark: a baseline study for the Danish Integrated Antimicrobial Resistance Monitoring Programme (DANMAP). APMIS APMIS Acta Pathologica, Microbiologica et Immunologica Scandinavica APMIS Automated Project Management Information System APMIS Automated Project Management System . 1998;106:745-70. (9.) Alban L, Olsen A-M A-M Alternating Maximization (algorithm) , Granly Koch A. Food safety risk assessment for imports of meat. In: Proceedings of the 18th International Pig Veterinary Society Congress, 27 June-1 July, 2004, Hamburg Hamburg, city, Germany Hamburg (häm`b  rkh), officially Freie und Hansestadt Hamburg (Free and Hanseatic City of Hamburg), city (1994 pop. , Germany.
Hamburg: The Society; 2004. p. 667.
(10.) Wegener HC, Hald T, Lo Fo Wong D, Madsen M, Korsgaard H, Bager F, et al. Salmonella control programs in Denmark. Emerg Infect Dis. 2003;9:774-80. (11.) Aarestrup FM, Lertworapreecha M, Evans MC, Bangtrakulnonth A, Chalermchaikit T, Hendriksen RS, et al. Antimicrobial susceptibility and occurrence of resistance genes among Salmonella enterica serovar Weltevreden from different countries. J Antimicrob Chemother. 2003;52:715-8. (12.) Baggesen DL, Sandvang D, Aarestrup FM. Characterization A rather long and fancy word for analyzing a system or process and measuring its "characteristics." For example, a Web characterization would yield the number of current sites on the Web, types of sites, annual growth, etc. of Salmonella enterica serovar typhimurium DT104 isolated from Denmark and comparison with isolates from Europe and the United States United States, officially United States of America, republic (2005 est. pop. 295,734,000), 3,539,227 sq mi (9,166,598 sq km), North America. The United States is the world's third largest country in population and the fourth largest country in area. . J Clin Microbiol. 2000;38:1581-6. (13.) Annual reports on zoonoses Zoonoses Infections of humans caused by the transmission of disease agents that naturally live in animals. People become infected when they unwittingly intrude into the life cycle of the disease agent and become unnatural hosts. in Denmark, 2000-2003. Copenhagen: Ministry of Agriculture, Food and Fisheries fisheries. From earliest times and in practically all countries, fisheries have been of industrial and commercial importance. In the large N Atlantic fishing grounds off Newfoundland and Labrador, for example, European and North American fishing fleets have long ; 2001-2004. [cited 2007 15 Feb]. Available from http://www.dfvf.dk/Default.aspx? ID=9606 Address for correspondence: Frank M. Aarestrup, National Food Institute, 27 Bolowsvej, DK-1790 Copenhagen V, Denmark; email: faa@ food.dtu.dk Marianne N. Skov, * Jens Strodl Andersen, ([dagger]) Soren Aabo, ([dagger]) Steen Ethelberg, ([double dagger double dagger n. A reference mark (  ) used in printing and writing. Also called diesis.Noun 1. ]) Frank M. Aarestrup, ([dagger]) Anders Hay Sorensen, ([dagger]) Gitte Sorensen, ([dagger]) Karl Pedersen, ([dagger]) Steen Nordentoft, ([dagger]) Katharina E.P. Olsen, ([double dagger]) Peter Gerner-Smidt, ([double dagger]) and Dorte L. Baggesen ([dagger]) * University of Southern Denmark, Odense, Denmark; ([dagger]) National Food Institute, Copenhagen, Denmark; and ([double dagger]) Statens Serum Institut Statens Serum Institut (English: the State Serum Institute), or SSI for short, is a Danish sector research institute located on the island of Amager in Copenhagen. , Copenhagen, Denmark
Table 1. Number and proportion of susceptible (S), resistant (R),
multidrug-resistant (M), and nalidixic acid-resistant (Nal) Salmonella
spp. isolates within different serotypes isolated from meat and humans,
Denmark, July 1998-July 2002 *
Domestic meat
No.
Serotype tested S, % R, % M, % Nal
Typhimurium ([double dagger]) 1,508 73 21 6 1
Infantis ([double dagger]) 184 94 4 2 2
Derby ([double dagger]) 163 55 44 1 1
Heidelberg 6 67 33 0 17
Hadar ([double dagger]) 38 74 26 0 11
Enteritidis ([double dagger]) 91 90 9 1 4
Indiana ([double dagger]) 94 95 4 1 0
Newport 2 0 100 0 100
Kottbus 26 81 19 0 15
Dublin 71 99 1 0 1
Anatum 50 100 0 0 0
Saintpaul 9 11 0 89 22
Regent 47 0 100 0 100
Virchow 3 100 0 0 0
Bredeney 3 100 0 0 0
Other ([double dagger]) 690 71 24 5 5
Total 2,985 74 22 4 4
Imported meat
No.
Serotype tested S, % R, %
Typhimurium ([double dagger]) 138 34 24
Infantis ([double dagger]) 50 84 10
Derby ([double dagger]) 34 32 59
Heidelberg 157 49 13
Hadar ([double dagger]) 113 1 53 ([section])
Enteritidis ([double dagger]) 50 84 16
Indiana ([double dagger]) 40 45 43 ([section])
Newport 78 28 51
Kottbus 49 6 90
Dublin 4 100 0
Anatum 12 75 8
Saintpaul 39 31 8
Regent 1 0 100
Virchow 39 44 36
Bredeney 38 34 0
Other ([double dagger]) 256 56 24
Total 1,078 42 30
Imported meat
Serotype M, % Nal
Typhimurium ([double dagger]) 42 ([section]) 9 ([section])
Infantis ([double dagger]) 6 8 ([section])
Derby ([double dagger]) 9 ([section]) 3
Heidelberg 38 4
Hadar ([double dagger]) 46 ([section]) 81 ([section])
Enteritidis ([double dagger]) 0 10
Indiana ([double dagger]) 13 ([section]) 3
Newport 21 60
Kottbus 4 92
Dublin 0 0
Anatum 17 0
Saintpaul 62 15
Regent 0 0
Virchow 21 49
Bredeney 66 11
Other ([double dagger]) 20 17
Total 28 26
Humans ([dagger])
No.
Serotype tested S, % R, % M, % Nal
Typhimurium ([double dagger]) 1,886 61 20 19 3
Infantis ([double dagger])
Derby ([double dagger])
Heidelberg
Hadar ([double dagger]) 189 26 71 3 58
Enteritidis ([double dagger]) 1,706 92 7 0 4
Indiana ([double dagger])
Newport 59 88 7 5 5
Kottbus
Dublin 88 95 5 0 2
Anatum
Saintpaul 58 72 9 19 7
Regent
Virchow 95 35 56 9 62
Bredeney
Other ([double dagger])
Total 4,081 73 17 9 7
* Only serotypes with [greater than or equal to] 40 isolates are
included.
([dagger]) Only subsets of selected serovars are routinely tested for
susceptibility to antimicrobial agents.
([double dagger]) Indicates serotypes with >30 samples from Danish
produced meat and >30 samples from imported meat, which were
statistically tested.
([section]) Indicates clinical significance.
Table 2. Results from the reduced logistic regression models *
Variable OR (95% CI)
Resistance vs. nonresistance
Intercept 0.164 (0.129 to 0.207)
Origin 5.08 (4.19 to 6.18)
Year 1.27 (1.19 to 1.35)
Cattle vs. poultry 0.400 (0.230 to 0.662)
Pork vs poultry 1.26 (1.06 to 1.51)
Multidrug resistance vs. resistance
Intercept 0.141 (0.0976 to 0.201)
Origin 4.98 (3.87 to 6.44)
Year 1.14 (1.03 to 1.27)
Nalidixic acid resistance vs. non-nalidixic acid resistance
Intercept 0.0611 (0.0333 to 0.107)
Origin 6.54 (3.45 to 12.8)
Year 1.41 (1.18 to 1.69)
Origin and year 0.732 (0.587 to 0.909)
Cattle vs. poultry 0.0404 (0.00229 to 0.182)
Pork vs. poultry 0.0668 (0.0425 to 0.101)
Variable Estimate (95% CI)
Resistance vs. nonresistance
Intercept -1.81 (-2.05 to -1.57)
Origin 1.62 (1.43 to 1.82)
Year 0.235 (0.174 to 0.297)
Cattle vs. poultry -0.917 (-1.47 to -0.413)
Pork vs poultry 0.233 (0.0553 to 0.414)
Multidrug resistance vs. resistance
Intercept -1.96 (-2.33 to -1.60)
Origin 1.61 (1.35 to 1.86)
Year 0.133 (0.0259 to 0.240)
Nalidixic acid resistance vs. non-nalidixic acid resistance
Intercept -2.80 (-3.40 to -2.24)
Origin 1.88 (1.24 to 2.55)
Year 0.342 (0.167 to 0.526)
Origin and year -0.311 (-0.532 to -0.0956)
Cattle vs. poultry -3.21 (-6.08 to -1.70)
Pork vs. poultry -2.71 (-3.16 to -2.29)
Variable SE (Est.) p value
Resistance vs. nonresistance
Intercept 0.121
Origin 0.0988 <0.00001
Year 0.0313 <0.00001
Cattle vs. poultry 0.268 <0.00001
Pork vs poultry 0.0916
Multidrug resistance vs. resistance
Intercept 0.185
Origin 0.129 <0.00001
Year 0.0547 0.0148
Nalidixic acid resistance vs. non-nalidixic acid resistance
Intercept 0.296
Origin 0.334
Year 0.0914
Origin and year 0.111 0.00448
Cattle vs. poultry 1.01 <0.00001
Pork vs. poultry 0.220
* OR, odds ratio; CI, confidence interval; SE, standard error;
Est., estimated.
Table 3. Number and proportion of susceptible (S), resistant (R), and
multidrug-resistant (M) meat isolates within Salmonella Typhimurium
phage types, Denmark, July 1998-July 2002 *
Domestic meat
Serovar/phage type M, % R, % S, % Total no.
All S. Typhimurium isolates 6 21 73 1,508
DT104 70 13 17 23
DT170 3 68 29 97
DT193 13 37 51 63
DT120 16 29 55 38
DT208 57 40 3 30
DT107 5 55 41 22
U302 0 33 67 6
DT135 6 56 38 16
Other S. Typhimurium 5 21 74 1,213
Salmonella other than Typhimurium 3 22 75 1,477
Total 4 22 74 2,985
Imported meat
Serovar/phage type M, % R, % S, % Total no.
All S. Typhimurium isolates 42 24 34 138
DT104 88 7 5 43
DT170 0 0 0 0
DT193 50 17 33 6
DT120 57 43 0 7
DT208 0 57 43 7
DT107 0 0 0 0
U302 38 31 31 13
DT135 0 100 0 2
Other S. Typhimurium 21 32 47 60
Salmonella other than Typhimurium 26 31 43 940
Total 28 30 42 1,078
Serovar/phage type Total no.
All S. Typhimurium isolates 1,646
DT104 66
DT170 97
DT193 69
DT120 45
DT208 37
DT107 22
U302 19
DT135 18
Other S. Typhimurium 1,273
Salmonella other than Typhimurium 2,417
Total 4,063
* Not all S. Typhfmurfum isolates from humans were phage typed.
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