Fluoroquinolone-resistant Salmonella sp. in Carcasses.

To the Editor: Fluoroquinolone (FQ)-resistant Salmonella has been isolated from patients in Taiwan (1-7). Recently, a report further indicated that several patients were infected with Salmonella enterica serovar Schwarzengrund with high-level FQ resistance (1). S. Schwarzengrund has never been isolated from food animals in Taiwan.

We report the isolation of FQ-resistant strains from pork and broiler carcasses sampled from 2000 to 2003: 27 in 2000, 3 in 2001, 4 in 2002, and 2 in 2003. These isolates made up 18.85% of the 191 Salmonella strains obtained from pork and broiler carcasses in the study period. Of these isolates, 16 FQ-resistant S. Schwarzengrund strains were further analyzed to elucidate the possible mechanism of FQ resistance. Ciprofloxacin MIC levels in these isolates ranged from 4 to 16 [micro]g/mL, and all had high-level nalidixic acid resistance ([greater than or equal to] 1,024 [micro]g/mL). All of the 16 investigated strains displayed mutations possibly associated with high-level FQ resistance. The mutation sites included 2 sites (Ser83Phe and Asp87Gly) in the quinolone resistance-determining region (QRDR) of gyrA, 2 sites (Thr57Ser and Ser80Arg) in the QRDR of parC, and 1 site (Ser458Pro) in the QRDR of parE, respectively. Four strains had mutations in the QRDR of gyrA and parC only but not in the QRDR of parE (Table).

In conclusion, high-level FQ resistance was detected in S. Schwarzengrund isolated from pork and chicken in Taiwan. Specific mutation sites of gyrA, parC, and parE were associated with high-level FQ resistance in all the isolates investigated. Our results warrant further investigation of the public health consequences of FQ use in food animals in Taiwan.

Yu-Chih Wang, * Kuang-Sheng Yeh, ([dagger]) Chao-Chin Chang, * Shih-Ling Hsuan, * and Ter-Hsin Chen *

* National Chung Hsing University, Taichung, Taiwan; and ([dagger]) Taipei Medical University, Taipei, Taiwan

References

(1.) Baucheron S, Chaslus-Dancla E, Cloeckaert A, Chiu CH, Butaye P. High-level resistance to fluoroquinolones linked to mutations in gyrA, parC, and pare in Salmonella enterica serovar Schwarzengrund isolates from humans in Taiwan. Antimicrob Agents Chemother. 2005;49:862-3.

(2.) Chiu CH, Su LH, Hung CC, Chen KL, Chu C. Prevalence and antimicrobial susceptibility of serogroup D nontyphoidal Salmonella in a university hospital in Taiwan. J Clin Microbiol. 2004;42:415-7.

(3.) Chiu CH, Wu TL, Su LH, Chu C, Chia JH, Kuo AJ, et al. The emergence in Taiwan of fluoroquinolone resistance in Salmonella enterica serotype Choleraesuis. N Engl J Med. 2002;346:413-9.

(4.) Chiu CH, Wu TL, Su LH, Liu JW, Chu C. Fluoroquinolone resistance in Salmonella enterica serotype Choleraesuis, Taiwan, 2000-2003. Emerg Infect Dis. 2004; 10:1674-6.

(5.) Hsueh PR, Teng L J, Tseng SP, Chang CF, Wan JH, Yan JJ, et al. Ciprofloxacin-resistant Salmonella enterica Typhimurium and Choleraesuis from pigs to humans, Taiwan. Emerg Infect Dis. 2004;10:60-8.

(6.) Huang TM, Chang YF, Chang CF. Detection of mutations in the gyrA gene and class I integron from quinolone-resistant Salmonella enterica serovar Choleraesuis isolates in Taiwan. Vet Microbiol. 2004;100:247-54.

(7.) Ko WC, Yan JJ, Yu WL, Lee HC, Lee NY, Wang LR, et al. A new therapeutic challenge for old pathogens: community-acquired invasive infections caused by ceftriaxone- and ciprofloxacin-resistant Salmonella enterica serotype Choleraesuis. Clin Infect Dis. 2005;40:315-8.

Address for correspondence: Ter-Hsin Chen, The Graduate Institute of Veterinary Public Health, College of Veterinary Medicine, National Chung Hsing University, No. 250, Kuo Kuang Rd, Taichung 402, Taiwan; fax: [phone]; email: [e-mail]. edu.tw

Table. Characteristics of ciprof loxacin-resistant Salmonella enterica
serovar Schwarzengrund strains from carcasses * ([dagger])

                                                          Quinolone
                                                            MICs
                                                        ([micro]g/mL)
Strain                  Year      Antimicrobial drug
no.       Origin *    isolated    resistance profile         NAL

A5          B, M        2000           CmSxtTc              1,024
A16         P, E        2000          ApCmNSxtTc            2,048
A17         P, E        2000          ApCmNSxtTc            2,048
A18         P, E        2000          ApCmNSxtTc            2,048
A19         P, E        2000         ApCmCnNSxtTc           1,024
A20         P, E        2000          ApCmNSxtTc            2,048
A29         B, S        2000           CmNSxtTc             1,024
A36         B, S        2000          ApCmSxtTc             1,024
A41         P, S        2000         ApCmCnNSxtTc           1,024
A45         P, S        2000          ApCmNSxtTc            1,024
A51         P, S        2000         ApCmCnNSxtTc           1,024
A56         B, M        2000         ApCmCnNSxtTc           2,048
A61         P, S        2000           CmSxtTc              1,024
A62         P, S        2000         ApCmCnSxtTc            2,048
B16         P, E        2001         ApCmCnCroTc            2,048
B73         P, N        2003         ApCmCnNSxtTc           2,048

           Quinolone MICs             Substitutions in QRDR
            ([micro]g/mL)               ([double dagger])
Strain
no.       FLU    ENR    CIP      gyrA          parC          parE

A5        512    32      8     Ser83Phe;    Thr57Ser;      Ser458Pro
                               Asp87Gly      Ser80Arg
A16       512    32      8     Ser83Phe;    Thr57Ser;      Ser458Pro
                               Asp87Gly      Ser80Arg
A17       512    32     16     Ser83Phe;    Thr57Ser;      Ser458Pro
                               Asp87Gly      Ser80Arg
A18       512    32     16     Ser83Phe;    Thr57Ser;      Ser458Pro
                               Asp87Gly      Ser80Arg
A19       512    32      8     Ser83Phe;    Thr57Ser;      Ser458Pro
                               Asp87Gly      Ser80Arg
A20       512    32      8     Ser83Phe;    Thr57Ser;      Ser458Pro
                               Asp87Gly      Ser80Arg
A29       512    32      8     Ser83Phe;    Thr57Ser;      Ser458Pro
                               Asp87Gly      Ser80Arg
A36       512    32      8     Ser83Phe;    Thr57Ser;      Ser458Pro
                               Asp87Gly      Ser80Arg
A41       512    32     16     Ser83Phe;    Thr57Ser;      Ser458Pro
                               Asp87Gly      Ser80Arg
A45       512    32     16     Ser83Phe;    Thr57Ser;
                               Asp87Gly      Ser80Arg
A51       512    16      4     Ser83Phe;    Thr57Ser;
                               Asp87Gly      Ser80Arg
A56       512    64     16     Ser83Phe;    Thr57Ser;
                               Asp87Gly      Ser80Arg
A61       512    32      8     Ser83Phe;   Thr57Ser;Ser    Ser458Pro
                               Asp87Gly       80Arg
A62       512    64     16     Ser83Phe;    Thr57Ser;
                               Asp87Gly      Ser80Arg
B16       512    32     16     Ser83Phe;    Thr57Ser;      Ser458Pro
                               Asp87Gly      Ser80Arg
B73       512    32     16     Ser83Phe;    Thr57Ser;      Ser458Pro
                               Asp87Gly      Ser80Arg

* QRDR, quinolone resistance-determining region; B, broiler; M, middle
Taiwan; P, pork; E, east Taiwan; S, south Taiwan; N, north Taiwan.

([dagger]) Antimicrobial agents are ampicillin (Ap), chloramphenicol
(Cm), ciprofloxacin (CIP), enrofloxacin (ENR), flumequine (FLU),
gentamicin (Cn), ceflriaxone (Cro), nalidixic acid (NAL),neomycin (N),
trimethoprim/sulfamethoxazole (Sxt), and tetracycline (Tc).

([double dagger]) No gyrB substitutions were detected.