- Email: [email protected]
Molecular epidemiology of CTX-M-type extended-spectrum β-lactamase-producing Proteus mirabilis isolates in Taiwan
International Journal of Antimicrobial Agents 45 (2015) 84–95
Contents lists available at ScienceDirect
International Journal of Antimicrobial Agents journal homepage: http://www.elsevier.com/locate/ijantimicag
Letters to the Editor Molecular epidemiology of CTX-M-type extended-spectrum -lactamase-producing Proteus mirabilis isolates in Taiwan Sir, Enterobacteriaceae producing extended-spectrum lactamases (ESBLs) are a worldwide problem. The most frequently encountered ESBLs belong to TEM-, SHV- and CTX-M-type -lactamases [1]. The CTX-M-type -lactamases are the predominant ESBL type among Proteus mirabilis in Taiwan [2,3]. The present study aimed to determine the prevalence, characterisation and molecular epidemiology of ESBLs in P. mirabilis isolates in central Taiwan. From January to August 2009, a total of 140 P. mirabilis isolates were collected from five district hospitals in central Taiwan. Among them, 28 isolates (20.0%), named Pm1–Pm28, respectively, exhibited non-susceptibility to cefotaxime, with a significant reduction in the minimum inhibitory concentration (MIC) (≥3 log2 dilution)
by clavulanic acid [Clinical and Laboratory Standards Institute (CLSI), 2010], confirming the ESBL phenotype (Table 1). Of these 28 ESBL-producers, 26 (92.9%) exhibited high-level resistance to cefotaxime (MIC ≥256 g/mL). ESBL-producing P. mirabilis isolates were found in all five hospitals submitting isolates, including 19 isolates recovered from urine, 4 from sputum and 5 from pus. Twenty-four (85.7%) of the isolates were isolated from inpatients. The antimicrobial susceptibility patterns of these isolates were also examined. All ESBL-producing isolates were susceptible to imipenem, and 27 (96.4%) and 24 (85.7%) isolates exhibited susceptibility to tazobactam/piperacillin and cefoxitin, respectively. In addition, 13 (46.4%), 11 (39.3%) and 8 (28.6%) ESBLproducing isolates were susceptible to amikacin, ciprofloxacin and ampicillin/sulbactam, respectively. Most ESBL-producing isolates were intermediate or resistant to gentamicin (27; 96.4%), ceftazidime (25; 89.3%), ceftriaxone (25; 89.3%) and sulfamethoxazole/trimethoprim (24; 85.7%). All ESBL-producing isolates were non-susceptible (resistant or intermediately susceptible) to ampicillin and cefazolin (Table 1).
Table 1 Characteristics of 28 extended-spectrum -lactamase (ESBL)-producing Proteus mirabilis isolates in this study. Strain
MIC (g/mL) CTX
Pm1 Pm2 Pm3 Pm4 Pm5 Pm6 Pm7 Pm8 Pm9 Pm10 Pm11 Pm12 Pm13 Pm14 Pm15 Pm16 Pm17 Pm18 Pm19 Pm20 Pm21 Pm22 Pm23 Pm24 Pm25 Pm26 Pm27 Pm28
>256 >256 >256 >256 >256 >256 >256 >256 >256 >256 >256 >256 >256 >256 >256 256 128 >256 >256 >256 >256 >256 >256 >256 >256 >256 >256 64
-Lactamase gene(s)
Antimicrobial resistance pattern
PFGE pattern (hospital)
TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, SHV-1, CTX-M-14, CMY-2, DHA-1 TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, CTX-M-14, DHA-1, OXA-10, OXA-13 TEM-1, CTX-M-14 TEM-1, CTX-M-14 CTX-M-14 TEM-1, SHV-1, CTX-M-14, OXA-10 TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, CTX-M-9 TEM-1, CTX-M-14 TEM-1, CTX-M-14, CMY-2 TEM-1, CTX-M-14 TEM-1, CTX-M-14, CTX-M-3 TEM-1, CTX-M-3 TEM-1, VEB-1
AMP-CEZ-GEN-CAZ-CRO-SAM-CIP-AMK AMP-CEZ-GEN-CAZ-SXT-CRO-SAM AMP-CEZ-GEN-CAZ-SXT-CRO-SAM AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-CIP-AMK AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-CIP-AMK AMP-CEZ-GEN-CAZ-SXT-CRO-CIP-AMK AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-CIP-AMK AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-CIP-AMK AMP-CEZ-GEN-CAZ-SXT-CRO-CIP-AMK AMP-CEZ-GEN-CAZ-SXT-CRO AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-CIP-AMK AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-CIP-AMK AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-CIP-AMK AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-FOX AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-CIP AMP-CEZ-GEN-CAZ-SXT-CRO AMP-CEZ-GEN-CAZ-SXT-CRO-CIP AMP-CEZ-GEN-CAZ-SXT-CRO-CIP AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-AMK AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-CIP-AMK-FOX AMP-CEZ-GEN-SAM AMP-CEZ-GEN-CAZ-SXT-CRO-FOX AMP-CEZ-GEN-CAZ-SXT-CRO-CIP AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-AMK-FOX AMP-CEZ-CAZ-CRO-SAM-CIP-TZP AMP-CEZ-GEN-SAM AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-CIP-AMK AMP-CEZ-GEN-SXT-SAM-AMK
A (I) B (I) B (I) C (II) C (II) C (III) C (III) C (I) D (I) B (I) C (I) C (II) C (II) E (III) F (II) B (I) C (IV) C (IV) G (I) H (V) C (I) I (I) B (V) J (I) C (I) K (V) L (V) M (V)
CTX/CLA <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 0.25 <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 16 <0.25 <0.25 <0.25 <0.25
MIC, minimum inhibitory concentration; CTX, cefotaxime; CLA, clavulanic acid; PFGE, pulsed-field gel electrophoresis; AMP, ampicillin; CEZ, cefazolin; GEN, gentamicin; CAZ, ceftazidime; CRO, ceftriaxone; SAM, ampicillin/sulbactam; CIP, ciprofloxacin; AMK, amikacin; SXT, trimethoprim/sulfamethoxazole; FOX, cefoxitin; TZP, piperacillin/tazobactam. 0924-8579/© 2014 Elsevier B.V. and the International Society of Chemotherapy. All rights reserved.
Letters to the Editor / International Journal of Antimicrobial Agents 45 (2015) 84–95
Detection of genes encoding -lactamases was performed by PCR amplification with previously described primers [2,4,5]. The presence of TEM-1 was detected in 27 isolates (96.4%; all strains except for Pm17), SHV-1 in 2 isolates (7.1%; strains Pm10 and Pm18), OXA-10 in 2 isolates (7.1%; strains Pm14 and Pm18), OXA13 in 1 isolate (3.6%; strain Pm14), VEB-1 in 1 isolate (3.6%; strain Pm28), CTX-M-9-cluster in 26 isolates (92.9%) and CTX-M-1 cluster in 2 isolates (7.1%). The most common type of class A ESBLs identified was CTX-M-14 (n = 25; all strains except for Pm22, Pm27 and Pm28). Genes encoding CTX-M-9 (n = 1; strain Pm22) and CTX-M-3 (n = 2; strains Pm26 and Pm27) were also detected. Genes encoding DHA-1 and CMY-2 AmpC -lactamases were detected in 2 isolates (7.1%; strains Pm10 and Pm14) and 2 isolates (7.1%; strains Pm10 and Pm24), respectively. The bla gene of PER and GES enzymes as well as members of the CTX-M-2, CTX-M-8 and CTX-M-25 clusters were not detected in this survey (Table 1). The relationship between the 28 ESBL-producing strains was studied by pulsed-field gel electrophoresis (PFGE). Based on the PFGE pattern, the 28 clinical ESBL-producing isolates were classified into 13 different PFGE patterns (patterns A–M) (Table 1; Supplementary Fig. S1). Two major epidemic clones with intrahospital and interhospital distribution were recognised, including 12 isolates (42.9%) of pattern C (hospitals I, II, III and IV) and 5 isolates (17.9%) of pattern B (hospitals I and V). The remaining 11 profiles (patterns A, D, E, F, G, H, I, J, K, L and M) were unique. In this study, 20.0% (28/140) of the P. mirabilis isolates were ESBL-producers. Compared with a survey in 2005 [2], the prevalence of ESBL-producing P. mirabilis in Taiwan has increased approximately three-fold from 6.2% to 20%, whilst a 2003 survey reported 30.6% of P. mirabilis isolates as ESBL-producers [3]. In this study, SHV-1, VEB-1, OXA-10 and OXA-13 -lactamases were also detected in P. mirabilis isolates. However, these -lactamases were not identified in two previous studies in Taiwan. As far as we know, this is the first report of P. mirabilis producing VEB- and OXA-type ESBLs in Taiwan. Another notable result was that two ESBL-producing P. mirabilis (strains Pm10 and Pm14) isolates all carried five ESBL genes. Two earlier studies in Taiwan showed that most ESBL-producing P. mirabilis isolates only harboured two or three ESBLs [2,3]. This result revealed that the ESBL gene epidemic trend appears to have a more and more complicated phenomenon, worthy of clinical staff attention. In summary, these data indicated that the incidence of ESBLproducing P. mirabilis has increased due to the dissemination of bla genes encoding CTX-M enzymes in Taiwan. Furthermore, these isolates are characterised by reduced susceptibility to many -lactam and non--lactam agents. Acknowledgments The authors thank all of the contributing hospitals that provided isolates for this study. Funding: This work was supported by grants from the 100 annual cooperation programs of Central Taiwan University of Science and Technology and Feng Yuan Hospital [FYH1000305-100.04] and the Taichung Tzu Chi Hospital [TTCRD101-23]. Competing interests: None declared. Ethical approval: Not required.
References [1] Pitout JD, Laupland KB. Extended-spectrum -lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis 2008;8: 159–66. [2] Wu JJ, Chen HM, Ko WC, Wu HM, Tsai SH, Yan JJ. Prevalence of extendedspectrum -lactamases in Proteus mirabilis in a Taiwanese university hospital, 1999 to 2005: identification of a novel CTX-M enzyme (CTX-M-66). Diagn Microbiol Infect Dis 2008;60:169–75. [3] Wu LT, Wu HJ, Chung JG, Chuang YC, Cheng KC, Yu WL. Dissemination of Proteus mirabilis isolates harboring CTX-M-14 and CTX-M-3 -lactamases at 2 hospitals in Taiwan. Diagn Microbiol Infect Dis 2006;54:89–94. [4] Kim JY, Park YJ, Kim SI, Kang MW, Lee SO, Lee KY. Nosocomial outbreak by Proteus mirabilis producing extended-spectrum -lactamase VEB1 in a Korean university hospital. J Antimicrob Chemother 2004;54: 1144–7. [5] Navon-Venezia S, Chmelnitsky I, Leavitt A, Carmeli Y. Dissemination of the CTX-M-25 family -lactamases among Klebsiella pneumoniae, Escherichia coli and Enterobacter cloacae and identification of the novel enzyme CTXM-41 in Proteus mirabilis in Israel. J Antimicrob Chemother 2008;62: 289–95.
Chien-Wen Huang 1 Division of Chest Medicine, Feng Yuan Hospital, Ministry of Health and Welfare, Executive Yuan, Taiwan, ROC Ju-Huei Chien 1 Department of Laboratory Medicine, Tzu Chi Hospital, Taichung Branch, Taichung, Taiwan, ROC Ru-Yan Peng 1 Institute of Biotechnology, Central Taiwan University of Science and Technology, Taiwan, ROC De-Jiun Tsai Ming-Hsien Li Department of Medical Laboratory Science and Biotechnology, Central Taiwan University of Science and Technology, No. 660 Buzih Road, Beitun District, Taichung City 40601, Taiwan, ROC Hsien-Ming Lee Institute of Biotechnology, Central Taiwan University of Science and Technology, Taiwan, ROC Chuen-Fu Lin 2 Department of Medical Laboratory Science and Biotechnology, Central Taiwan University of Science and Technology, No. 660 Buzih Road, Beitun District, Taichung City 40601, Taiwan, ROC Mong-Chuan Lee Institute of Biotechnology, Central Taiwan University of Science and Technology, Taiwan, ROC Chao-Tsai Liao ∗ Department of Medical Laboratory Science and Biotechnology, Central Taiwan University of Science and Technology, No. 660 Buzih Road, Beitun District, Taichung City 40601, Taiwan, ROC ∗ Corresponding
author. Tel.: +886 4 2239 1647x7056; fax: +886 4 2239 6761. E-mail address: [email protected] (C.-T. Liao)
1
Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at http://dx.doi.org/10.1016/j.ijantimicag. 2014.09.004.
85
2
These authors contributed equally to this work.
Present address: Department of Veterinary Medicine, National Chiayi University, Chiayi City 60004, Taiwan, ROC. 25 April 2014
http://dx.doi.org/10.1016/j.ijantimicag.2014.09.004
Contents lists available at ScienceDirect
International Journal of Antimicrobial Agents journal homepage: http://www.elsevier.com/locate/ijantimicag
Letters to the Editor Molecular epidemiology of CTX-M-type extended-spectrum -lactamase-producing Proteus mirabilis isolates in Taiwan Sir, Enterobacteriaceae producing extended-spectrum lactamases (ESBLs) are a worldwide problem. The most frequently encountered ESBLs belong to TEM-, SHV- and CTX-M-type -lactamases [1]. The CTX-M-type -lactamases are the predominant ESBL type among Proteus mirabilis in Taiwan [2,3]. The present study aimed to determine the prevalence, characterisation and molecular epidemiology of ESBLs in P. mirabilis isolates in central Taiwan. From January to August 2009, a total of 140 P. mirabilis isolates were collected from five district hospitals in central Taiwan. Among them, 28 isolates (20.0%), named Pm1–Pm28, respectively, exhibited non-susceptibility to cefotaxime, with a significant reduction in the minimum inhibitory concentration (MIC) (≥3 log2 dilution)
by clavulanic acid [Clinical and Laboratory Standards Institute (CLSI), 2010], confirming the ESBL phenotype (Table 1). Of these 28 ESBL-producers, 26 (92.9%) exhibited high-level resistance to cefotaxime (MIC ≥256 g/mL). ESBL-producing P. mirabilis isolates were found in all five hospitals submitting isolates, including 19 isolates recovered from urine, 4 from sputum and 5 from pus. Twenty-four (85.7%) of the isolates were isolated from inpatients. The antimicrobial susceptibility patterns of these isolates were also examined. All ESBL-producing isolates were susceptible to imipenem, and 27 (96.4%) and 24 (85.7%) isolates exhibited susceptibility to tazobactam/piperacillin and cefoxitin, respectively. In addition, 13 (46.4%), 11 (39.3%) and 8 (28.6%) ESBLproducing isolates were susceptible to amikacin, ciprofloxacin and ampicillin/sulbactam, respectively. Most ESBL-producing isolates were intermediate or resistant to gentamicin (27; 96.4%), ceftazidime (25; 89.3%), ceftriaxone (25; 89.3%) and sulfamethoxazole/trimethoprim (24; 85.7%). All ESBL-producing isolates were non-susceptible (resistant or intermediately susceptible) to ampicillin and cefazolin (Table 1).
Table 1 Characteristics of 28 extended-spectrum -lactamase (ESBL)-producing Proteus mirabilis isolates in this study. Strain
MIC (g/mL) CTX
Pm1 Pm2 Pm3 Pm4 Pm5 Pm6 Pm7 Pm8 Pm9 Pm10 Pm11 Pm12 Pm13 Pm14 Pm15 Pm16 Pm17 Pm18 Pm19 Pm20 Pm21 Pm22 Pm23 Pm24 Pm25 Pm26 Pm27 Pm28
>256 >256 >256 >256 >256 >256 >256 >256 >256 >256 >256 >256 >256 >256 >256 256 128 >256 >256 >256 >256 >256 >256 >256 >256 >256 >256 64
-Lactamase gene(s)
Antimicrobial resistance pattern
PFGE pattern (hospital)
TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, SHV-1, CTX-M-14, CMY-2, DHA-1 TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, CTX-M-14, DHA-1, OXA-10, OXA-13 TEM-1, CTX-M-14 TEM-1, CTX-M-14 CTX-M-14 TEM-1, SHV-1, CTX-M-14, OXA-10 TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, CTX-M-14 TEM-1, CTX-M-9 TEM-1, CTX-M-14 TEM-1, CTX-M-14, CMY-2 TEM-1, CTX-M-14 TEM-1, CTX-M-14, CTX-M-3 TEM-1, CTX-M-3 TEM-1, VEB-1
AMP-CEZ-GEN-CAZ-CRO-SAM-CIP-AMK AMP-CEZ-GEN-CAZ-SXT-CRO-SAM AMP-CEZ-GEN-CAZ-SXT-CRO-SAM AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-CIP-AMK AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-CIP-AMK AMP-CEZ-GEN-CAZ-SXT-CRO-CIP-AMK AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-CIP-AMK AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-CIP-AMK AMP-CEZ-GEN-CAZ-SXT-CRO-CIP-AMK AMP-CEZ-GEN-CAZ-SXT-CRO AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-CIP-AMK AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-CIP-AMK AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-CIP-AMK AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-FOX AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-CIP AMP-CEZ-GEN-CAZ-SXT-CRO AMP-CEZ-GEN-CAZ-SXT-CRO-CIP AMP-CEZ-GEN-CAZ-SXT-CRO-CIP AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-AMK AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-CIP-AMK-FOX AMP-CEZ-GEN-SAM AMP-CEZ-GEN-CAZ-SXT-CRO-FOX AMP-CEZ-GEN-CAZ-SXT-CRO-CIP AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-AMK-FOX AMP-CEZ-CAZ-CRO-SAM-CIP-TZP AMP-CEZ-GEN-SAM AMP-CEZ-GEN-CAZ-SXT-CRO-SAM-CIP-AMK AMP-CEZ-GEN-SXT-SAM-AMK
A (I) B (I) B (I) C (II) C (II) C (III) C (III) C (I) D (I) B (I) C (I) C (II) C (II) E (III) F (II) B (I) C (IV) C (IV) G (I) H (V) C (I) I (I) B (V) J (I) C (I) K (V) L (V) M (V)
CTX/CLA <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 0.25 <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 <0.25 16 <0.25 <0.25 <0.25 <0.25
MIC, minimum inhibitory concentration; CTX, cefotaxime; CLA, clavulanic acid; PFGE, pulsed-field gel electrophoresis; AMP, ampicillin; CEZ, cefazolin; GEN, gentamicin; CAZ, ceftazidime; CRO, ceftriaxone; SAM, ampicillin/sulbactam; CIP, ciprofloxacin; AMK, amikacin; SXT, trimethoprim/sulfamethoxazole; FOX, cefoxitin; TZP, piperacillin/tazobactam. 0924-8579/© 2014 Elsevier B.V. and the International Society of Chemotherapy. All rights reserved.
Letters to the Editor / International Journal of Antimicrobial Agents 45 (2015) 84–95
Detection of genes encoding -lactamases was performed by PCR amplification with previously described primers [2,4,5]. The presence of TEM-1 was detected in 27 isolates (96.4%; all strains except for Pm17), SHV-1 in 2 isolates (7.1%; strains Pm10 and Pm18), OXA-10 in 2 isolates (7.1%; strains Pm14 and Pm18), OXA13 in 1 isolate (3.6%; strain Pm14), VEB-1 in 1 isolate (3.6%; strain Pm28), CTX-M-9-cluster in 26 isolates (92.9%) and CTX-M-1 cluster in 2 isolates (7.1%). The most common type of class A ESBLs identified was CTX-M-14 (n = 25; all strains except for Pm22, Pm27 and Pm28). Genes encoding CTX-M-9 (n = 1; strain Pm22) and CTX-M-3 (n = 2; strains Pm26 and Pm27) were also detected. Genes encoding DHA-1 and CMY-2 AmpC -lactamases were detected in 2 isolates (7.1%; strains Pm10 and Pm14) and 2 isolates (7.1%; strains Pm10 and Pm24), respectively. The bla gene of PER and GES enzymes as well as members of the CTX-M-2, CTX-M-8 and CTX-M-25 clusters were not detected in this survey (Table 1). The relationship between the 28 ESBL-producing strains was studied by pulsed-field gel electrophoresis (PFGE). Based on the PFGE pattern, the 28 clinical ESBL-producing isolates were classified into 13 different PFGE patterns (patterns A–M) (Table 1; Supplementary Fig. S1). Two major epidemic clones with intrahospital and interhospital distribution were recognised, including 12 isolates (42.9%) of pattern C (hospitals I, II, III and IV) and 5 isolates (17.9%) of pattern B (hospitals I and V). The remaining 11 profiles (patterns A, D, E, F, G, H, I, J, K, L and M) were unique. In this study, 20.0% (28/140) of the P. mirabilis isolates were ESBL-producers. Compared with a survey in 2005 [2], the prevalence of ESBL-producing P. mirabilis in Taiwan has increased approximately three-fold from 6.2% to 20%, whilst a 2003 survey reported 30.6% of P. mirabilis isolates as ESBL-producers [3]. In this study, SHV-1, VEB-1, OXA-10 and OXA-13 -lactamases were also detected in P. mirabilis isolates. However, these -lactamases were not identified in two previous studies in Taiwan. As far as we know, this is the first report of P. mirabilis producing VEB- and OXA-type ESBLs in Taiwan. Another notable result was that two ESBL-producing P. mirabilis (strains Pm10 and Pm14) isolates all carried five ESBL genes. Two earlier studies in Taiwan showed that most ESBL-producing P. mirabilis isolates only harboured two or three ESBLs [2,3]. This result revealed that the ESBL gene epidemic trend appears to have a more and more complicated phenomenon, worthy of clinical staff attention. In summary, these data indicated that the incidence of ESBLproducing P. mirabilis has increased due to the dissemination of bla genes encoding CTX-M enzymes in Taiwan. Furthermore, these isolates are characterised by reduced susceptibility to many -lactam and non--lactam agents. Acknowledgments The authors thank all of the contributing hospitals that provided isolates for this study. Funding: This work was supported by grants from the 100 annual cooperation programs of Central Taiwan University of Science and Technology and Feng Yuan Hospital [FYH1000305-100.04] and the Taichung Tzu Chi Hospital [TTCRD101-23]. Competing interests: None declared. Ethical approval: Not required.
References [1] Pitout JD, Laupland KB. Extended-spectrum -lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis 2008;8: 159–66. [2] Wu JJ, Chen HM, Ko WC, Wu HM, Tsai SH, Yan JJ. Prevalence of extendedspectrum -lactamases in Proteus mirabilis in a Taiwanese university hospital, 1999 to 2005: identification of a novel CTX-M enzyme (CTX-M-66). Diagn Microbiol Infect Dis 2008;60:169–75. [3] Wu LT, Wu HJ, Chung JG, Chuang YC, Cheng KC, Yu WL. Dissemination of Proteus mirabilis isolates harboring CTX-M-14 and CTX-M-3 -lactamases at 2 hospitals in Taiwan. Diagn Microbiol Infect Dis 2006;54:89–94. [4] Kim JY, Park YJ, Kim SI, Kang MW, Lee SO, Lee KY. Nosocomial outbreak by Proteus mirabilis producing extended-spectrum -lactamase VEB1 in a Korean university hospital. J Antimicrob Chemother 2004;54: 1144–7. [5] Navon-Venezia S, Chmelnitsky I, Leavitt A, Carmeli Y. Dissemination of the CTX-M-25 family -lactamases among Klebsiella pneumoniae, Escherichia coli and Enterobacter cloacae and identification of the novel enzyme CTXM-41 in Proteus mirabilis in Israel. J Antimicrob Chemother 2008;62: 289–95.
Chien-Wen Huang 1 Division of Chest Medicine, Feng Yuan Hospital, Ministry of Health and Welfare, Executive Yuan, Taiwan, ROC Ju-Huei Chien 1 Department of Laboratory Medicine, Tzu Chi Hospital, Taichung Branch, Taichung, Taiwan, ROC Ru-Yan Peng 1 Institute of Biotechnology, Central Taiwan University of Science and Technology, Taiwan, ROC De-Jiun Tsai Ming-Hsien Li Department of Medical Laboratory Science and Biotechnology, Central Taiwan University of Science and Technology, No. 660 Buzih Road, Beitun District, Taichung City 40601, Taiwan, ROC Hsien-Ming Lee Institute of Biotechnology, Central Taiwan University of Science and Technology, Taiwan, ROC Chuen-Fu Lin 2 Department of Medical Laboratory Science and Biotechnology, Central Taiwan University of Science and Technology, No. 660 Buzih Road, Beitun District, Taichung City 40601, Taiwan, ROC Mong-Chuan Lee Institute of Biotechnology, Central Taiwan University of Science and Technology, Taiwan, ROC Chao-Tsai Liao ∗ Department of Medical Laboratory Science and Biotechnology, Central Taiwan University of Science and Technology, No. 660 Buzih Road, Beitun District, Taichung City 40601, Taiwan, ROC ∗ Corresponding
author. Tel.: +886 4 2239 1647x7056; fax: +886 4 2239 6761. E-mail address: [email protected] (C.-T. Liao)
1
Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at http://dx.doi.org/10.1016/j.ijantimicag. 2014.09.004.
85
2
These authors contributed equally to this work.
Present address: Department of Veterinary Medicine, National Chiayi University, Chiayi City 60004, Taiwan, ROC. 25 April 2014
http://dx.doi.org/10.1016/j.ijantimicag.2014.09.004