Please wait a minute...
Journal of Integrative Agriculture  2012, Vol. 12 Issue (1): 116-121    DOI: 10.1016/S1671-2927(00)8517
ANIMAL SCIENCE · VETERINARY SCIENCE Advanced Online Publication | Current Issue | Archive | Adv Search |
Detection and Characterization of β-Lactam Resistance in Haemophilus parasuis Strains from Pigs in South China
 GUO Li-li, ZHANG Jian-min, XU Cheng-gang, REN Tao, ZHANG Bin, CHEN Ji-dang , LIAO Ming
1.Key Laboratory of Animal Disease Control and Prevention, Ministry of Agriculture/Key Laboratory of Zoonoses Prevention and Control of Guangdong, College of Veterinary Medicine, South China Agricultural University, Guangzhou 510642, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  To characterize the β-lactam resistance in veterinary clinical isolates of Haemophilus parasuis, 115 isolates were examined for the β-lactam resistance, the possession of β-lactamase, and the presence of β-lactamase genes. The genetic relationship among isolates was evaluated by pulsed-field gel electrophoresis (PFGE). Overall, the commonly detected resistance phenotypes were resistant to ampicillin (26.09%), penicillin (22.61%), amoxicillin (21.74%), cefazolin (14.78%), cefaclor (12.17%), and cefotaxime (6.96%). These strains showed high minimal inhibitory concentration (MICs) to oxacillin. 20.87% strains produced β-lactamase, and 4.35% strains showed extended-spectrum b-lactamase (ESBL) phenotype. Moreover, 19 strains harboured bla genes including TEM-1 (n=5), TEM-116 (n=10), and ROB-1 (n=5). Significantly, one strain possessed both TEM-1 and ROB-1, and displayed resistance to cefotaxime (MIC=8 mg L-1). The epidemiological analysis of PFGE revealed high genetic diversity among bla-positive isolates. This work shows that TEM- and ROB-type β-lactamases are prevalent in H. parasuis isolates in China.

Abstract  To characterize the β-lactam resistance in veterinary clinical isolates of Haemophilus parasuis, 115 isolates were examined for the β-lactam resistance, the possession of β-lactamase, and the presence of β-lactamase genes. The genetic relationship among isolates was evaluated by pulsed-field gel electrophoresis (PFGE). Overall, the commonly detected resistance phenotypes were resistant to ampicillin (26.09%), penicillin (22.61%), amoxicillin (21.74%), cefazolin (14.78%), cefaclor (12.17%), and cefotaxime (6.96%). These strains showed high minimal inhibitory concentration (MICs) to oxacillin. 20.87% strains produced β-lactamase, and 4.35% strains showed extended-spectrum b-lactamase (ESBL) phenotype. Moreover, 19 strains harboured bla genes including TEM-1 (n=5), TEM-116 (n=10), and ROB-1 (n=5). Significantly, one strain possessed both TEM-1 and ROB-1, and displayed resistance to cefotaxime (MIC=8 mg L-1). The epidemiological analysis of PFGE revealed high genetic diversity among bla-positive isolates. This work shows that TEM- and ROB-type β-lactamases are prevalent in H. parasuis isolates in China.
Keywords:  Haemophilus parasuis      β-lactamase genes      resistance      pulsed-field gel electrophoresis  
Received: 03 December 2010   Accepted:
Fund: 

This work was supported by the Program for New Century Excellent Talents in University, China (NCET-06-0752), and the Guangdong Technology Planning Committee, China (2006B0152 and 2009A0201006).

Corresponding Authors:  Correspondence LIAO Ming, Tel: +86-20-85280240, Fax: +86-20-85285282, E-mail: mliao@scau.edu.cn   
About author:  GUO Li-li, E-mail: gll2004203746@126.com

Cite this article: 

GUO Li-li, ZHANG Jian-min, XU Cheng-gang, REN Tao, ZHANG Bin, CHEN Ji-dang , LIAO Ming. 2012. Detection and Characterization of β-Lactam Resistance in Haemophilus parasuis Strains from Pigs in South China. Journal of Integrative Agriculture, 12(1): 116-121.

[1]Aarestrup F M, Seyfarth A M, Angen O. 2004. Antimicrobial susceptibility of Haemophilus parasuis and Histophilus somni from pigs and cattle in Denmark. Veterinary Microbiology, 101, 143-146.

[2]Ahmed A M, Furuta K, Shimomura K, Kasama Y, Shimamoto T. 2006. Genetic characterization of multidrug resistance in Shigella spp. from Japan. Journal of Medical Microbiology, 55, 1685-1691.

[3]Aragon V, Cerda-Cuellar M, Fraile L, Mombarg M, Nofrarias M, Olvera A, Sibila M, Solanes D, Segales J. 2010. Correlation between clinico-pathological outcome and typing of Haemophilus parasuis field strains. Veterinary Microbiology, 142, 387-393.

[4]Cai X, Chen H, Blackall P J, Yin Z, Wang L, Liu Z, Jin M. 2005. Serological characterization of Haemophilus parasuis isolates from China. Veterinary Microbiology, 111, 231-236.

[5]National Committee for Clinical Laboratory Standards. 2002. Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals. Approved Standard M31-A2. 2nd ed. Wayne, PA, USA. Clinical and Laboratory Standards Institute. 2009. Performance Standards for Antimicrobial Susceptibility Testing. M100-S19.

[6]Wayne, PA, USA. de la Fuente A J M, Tucker A W, Navas J, Blanco M, Morris S J, Gutierrez-Martin C B. 2007. Antimicrobial susceptibility patterns of Haemophilus parasuis from pigs in the United Kingdom and Spain. Veterinary Microbiology, 120, 184-191.

[7]Hu G Z, Chen H Y, Si H B, Deng L X, Wei Z Y, Yuan L, Kuang X H. 2008. Phenotypic and molecular characterization of TEM-116 extended-spectrum betalactamase produced by a Shigella flexneri clinical isolate from chickens. Federation of European Materials Societies Microbiology Letters, 279, 162-166.

[8]Kang M, Zhou R, Liu L, Langford P R, Chen H. 2009. Analysis of an Actinobacillus pleuropneumoniae multi-resistance plasmid, pHB0503. Plasmid, 61, 135-139.

[9]Li J X, Jiang P, Wang Y, Li Y F, Chen W, Wang X W, Li P. 2009. Genotyping of Haemophilus parasuis from diseased pigs in China and prevalence of two coexisting virus pathogens. Preventive Veterinary Medicine, 91, 274-279.

[10]Li X Z, Mehrotra M, Ghimire S, Adewoye L. 2007. β-Lactam resistance and β-lactamases in bacteria of animal origin. Veterinary Microbiology, 121, 197-214.

[11]Liao W, Jiang J, Xu Y, Yi J, Chen T, Su X, Pan S, Wei X, Li Y. 2010. Survey for beta-lactamase among bacterial isolates from Guangzhou, China hospitals between 2005-2006.

[12]The Journal of Antibiotics (Tokyo), 63, 225-229.

[13]Oliveira S, Galina L, Pijoan C. 2001. Development of a PCR test to diagnose Haemophilus parasuis infections. Journal of Veterinary Diagnostic Investigation, 13, 495-501.

[14]Perez-Perez F J, Hanson N D. 2002. Detection of plasmidmediated AmpC β-lactamase genes in clinical isolates by using multiplex PCR. Journal of Clinical Microbiology, 40, 2153-2162.

[15]San Millan A, Escudero J A, Catalan A, Nieto S, Farelo F, Gibert M, Moreno M A, Dominguez L, Gonzalez-Zorn B. 2007. β-Lactam resistance in Haemophilus parasuis is mediated by plasmid pB1000 bearing blaROB-1. Antimicrobial Agents and Chemotherapy, 51, 2260-2264.

[16]Sun Y, Zeng Z, Chen S, Ma J, He L, Liu Y, Deng Y, Lei T, Zhao J, Liu J H. 2010. High prevalence of bla (CTX-M) extended-spectrum beta-lactamase genes in Escherichia coli isolates from pets and emergence of CTX-M-64 in China. Clinical Microbiology and Infection, 16, 1475-1481.

[17]Sutton L D, Biedenbach D J, Yen A, Jones R N. 1995. Development, characterization, and initial evaluations of S1. A new chromogenic cephalosporin for β-lactamase detection. Diagnostic Microbiology and Infectious Disease, 21, 1-8.

[18]Tang X B, Zhao Z Q, Hu J Y, Wu B, Cai X W, He Q G, Chen H C. 2009. Isolation, antimicrobial resistance, and virulence genes of Pasteurella multocida strains from swine in China. Journal of Clinical Microbiology, 47, 951-958.

[19]Touati A, Achour W, Ben Hassen A. 2009. Phenotypic and molecular characterization of β-lactam resistance and capsular typing of colonizing Haemophilus influenzae strains isolated from neutropenic patients in Tunisia. Pathologie Biologie (Paris), 57, 353-357.

[20]Wissing A, Nicolet J, Boerlin P. 2001. The current antimicrobial resistance situation in Swiss veterinary medicine. Schweizer Archiv für Tierheilkunde, 143, 503-510.

[21]Yuan L, Liu J H, Hu G Z, Pan Y S, Liu Z M, Mo J, Wei Y J. 2009. Molecular characterization of extended-spectrum β-lactamase-producing Escherichia coli isolates from chickens in Henan Province, China. Journal of Medical Microbiology, 58, 1449-1453.

[22]Zhou X, Xu X, Zhao Y, Chen P, Zhang X, Chen H, Cai X. 2010. Distribution of antimicrobial resistance among different serovars of Haemophilus parasuis isolates. Veterinary Microbiology, 141, 168-173.

[23]Zuo B, Liu Z H, Wang H P, Yang Y M, Chen J L, Ye H F. 2006. Genotype of TEM-and SHV-type beta-lactamase producing Klebsiella pneumoniae in Guangzhou area. National Medical Journal of China, 86, 2928-2932. (in Chinese)
[1] Yunchuan He, Yang Gao, Qiulin Chen, Zheyi Shi, Hainuo Hong, Jiamei Geng, Ying Zhou, Zengrong Zhu. Field identification of cowpea variety resistance against Megalurothrips usitatus and the metabolomics-based resistance mechanism[J]. >Journal of Integrative Agriculture, 2026, 25(4): 0-.
[2] Jiaqi Wang, Biao Zhao, Dan Liu, Fumeng He, Chong Du, Yunzhu Che, Zengli Zhang, Xu Feng, Xue Wang , Yingnan Wang, Fenglan Li. StCOMT1 enhances potato resistance to Fusarium sporotrichioides by regulating coumarin-related substance accumulation and the ROS system[J]. >Journal of Integrative Agriculture, 2026, 25(3): 1020-1035.
[3] Hao Wu, Wenjiang Jing, Yajun Zhang, Ying Zhang, Weilu Wang, Kuanyu Zhu, Weiyang Zhang, Junfei Gu, Lijun Liu, Jianhua Zhang, Hao Zhang. Optimized application strategy of controlled-release nitrogen improves grain yield, nitrogen use efficiency and lodging resistance of rice[J]. >Journal of Integrative Agriculture, 2026, 25(3): 903-917.
[4] Jie Shuai, Qiang Tu, Yicong Zhang, Xiaobo Xia, Yuhua Wang, Shulin Cao, Yifan Dong, Xinli Zhou, Xu Zhang, Zhengguang Zhang, Yi He, Gang Li. Silence of five Fusarium graminearum genes in wheat host confers resistance to Fusarium head blight[J]. >Journal of Integrative Agriculture, 2026, 25(3): 1051-1063.
[5] Shuangxi Zhang, Xinlin Wei, Rongbo Wang, Hejing Shen, Hehuan You, Langjun Cui, Yi Qiang, Peiqing Liu, Meixiang Zhang, Yuyan An. Nicotinamide mononucleotide confers broad-spectrum disease resistance in plants[J]. >Journal of Integrative Agriculture, 2026, 25(3): 1064-1073.
[6] Xiqiang Li, Yuhong Gao, Zhengjun Cui, Tingfeng Zhang, Shiyuan Chen, Shilei Xiang, Lingling Jia, Bin Yan, Yifan Wang, Lizhuo Guo, Bing Wu . Optimized nitrogen and potassium fertilizers application increases stem lodging resistance and grain yield of oil flax by enhancing lignin biosynthesis[J]. >Journal of Integrative Agriculture, 2026, 25(2): 659-670.
[7] Xiaowei Zhu, Min Wang, Xiang Tai, Panling Lu, Hang Gui, Jinxiu Chen, Tianyue Bo. Candidate gene analysis of cabbage head-splitting resistance based on QTL mapping and omics profiling[J]. >Journal of Integrative Agriculture, 2026, 25(2): 709-720.
[8] Chaohui Yan, Juexi Liu, Xiaoxuan Wang, Yunfei Wang, Yuejin Wang, Jiaping Liang, Qiliang Yang. VqMAPK3–VqERF1B–VqPRs module confers resistance against Erysiphe necator in grapevine[J]. >Journal of Integrative Agriculture, 2026, 25(2): 682-693.
[9] Shuo Ma, Tong Li, Ziquan Feng, Yali Zhang, Han Jiang, Yuanyuan Li. MdXTH30, an apple gene encoding endotransferase/hydrolase for xyloglucan, enhances plant resistance to drought, salt and pathogenic stresses[J]. >Journal of Integrative Agriculture, 2026, 25(1): 127-137.
[10] Yijuan Ding, Yaru Chai, Sen Li, Zhaohui Wu, Minghong Zou, Ling Zhang, Rana Kusum, Wei Qian. SsBMR1 as a putative ABC transporter is required for pathogenesis by promoting antioxidant export and antifungal resistance in Sclerotinia sclerotiorum[J]. >Journal of Integrative Agriculture, 2026, 25(1): 166-179.
[11] Yang Sun, Yu Liu, Li Zhou, Xinyan Liu, Kun Wang, Xing Chen, Chuanqing Zhang, Yu Chen. Activity of fungicide cyclobutrifluram against Fusarium fujikuroi and mechanism of the pathogen resistance associated with point mutations in FfSdhB, FfSdhC2 and FfSdhD[J]. >Journal of Integrative Agriculture, 2025, 24(9): 3511-3528.
[12] Weiqi Guo, Di Wang, Xinyu Wang, Zhiyang Wang, Hong Zhu, Jiangang Hu, Beibei Zhang, Jingjing Qi, Mingxing Tian, Yanqing Bao, Na Li, Wanjiang Zhang, Shaohui Wang. Identification and characterization of a plasmid co-harboring blaCTX-M-55 and blaTEM-141 in Escherichia albertii from broiler in China[J]. >Journal of Integrative Agriculture, 2025, 24(8): 3212-3221.
[13] Chenyang Wang, Yinuo Zhang, Qiming Sun, Lin Li, Fang Guan, Yazhou He, Yidong Wu. Species-specific evolution of lepidopteran TspC5 tetraspanins associated with dominant resistance to Bacillus thuringiensis toxin Cry1Ac[J]. >Journal of Integrative Agriculture, 2025, 24(8): 3127-3140.
[14] Wei Wang, Chuxiao Lin, Yirong Zhang, Shiyan Liu, Jiali Liu, Xinnian Zeng. Four signal chemicals can non-destructively induce enhanced resistance to Asian citrus psyllids in Citrus sinensis while maintaining balanced plant growth and development[J]. >Journal of Integrative Agriculture, 2025, 24(7): 2732-2748.
[15] Jiazhi Sun, Bingyun Yang, Lingmin Xia, Rui Yang, Chaoyang Ding, Yang Sun, Xing Chen, Chunyan Gu, Xue Yang, Yu Chen. Amino acid substitutions in succinate dehydrogenase complex conferring resistance to the SDHI fungicide pydiflumetofen in Cochliobolus heterostrophus causing southern corn leaf blight[J]. >Journal of Integrative Agriculture, 2025, 24(7): 2670-2685.
No Suggested Reading articles found!