2020, Volume 6, Issue 1
Engineering >> 2020, Volume 6, Issue 1 doi: 10.1016/j.eng.2019.10.014
Association between the Phenotypes and Genotypes of Antimicrobial Resistance in Haemophilus parasuis Isolates from Swine in Quang Binh and Thua Thien Hue Provinces, Vietnam
a State Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University, Wuhan
430070, China
b Faculty of Animal Science and Veterinary Medicine, University of Agricultural and Forestry, Hue University, Hue 53000, Vietnam
c MienTrung Institute for Scientific Research, Vietnam Academy of Science and Technology, Hue 53000, Vietnam
d Guangdong Provincial Key Laboratory of Marine Biology, Shantou University, Shantou 515063, China
e Cooperative Innovation Center of Sustainable Pig Production, Wuhan 430070, China
f International Research Center for Animal Diseases, the Ministry of Science and Technology, Wuhan 430070, China
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Abstract
Haemophilus parasuis (H. parasuis) is one of the bacterial pathogens of great concern as it causes huge economic losses to the swine industry worldwide. One of the reasons why the control of H. parasuis has failed is the increase in antimicrobial resistance (AMR). Vietnam, a country has the second-largest pig production in Asia. However, there is still a lack of data about the AMR prevalence of H. parasuis in Vietnam. The purpose of this study is to investigate the prevalence of AMR and analyze the association between AMR and AMR genes (ARGs). The H. parasuis strains used in this research were isolated from swine in the Quang Binh and Thua Thien Hue Provinces, Central Vietnam, as reported in our previous study. All of the strains were tested for AMR against 25 antibacterial agents using the broth microdilution method and for the presence of ARGs using the polymerase chain reaction (PCR) method. The tested strains were shown to have a high frequency of resistance to trimethoprim/sulfamethoxazole (94.6%), followed by resistance to colistin, chloramphenicol, gentamicin, penicillin, lincomycin, and amoxicillin. The most prevalent ARGs in these strains were blaTEM-1 (94.6%), int (76.8%), gyrA (58.9%), and rmtD (50.0%). Cefuroxime, chloramphenicol and tobramycin resistances were strongly correlated with the presence of the ARGs blarob-1 (odds ratio (OR) = 26.3, 95% confidence interval (CI) 2.7–255.7, p = 0.002), catl (OR = 25.1, 95% CI 2.4–258.9, p = 0.004), and strB (OR = 23.5, 95% CI 2.6–212.6, p = 0.001),
respectively. This study reveals for the first time the current situation of H. parasuis AMR in Central Vietnam, which is helpful for the clinical control of this disease, as well as for the development of policies and clinical practice guidelines to reduce AMR in swine production in Central Vietnam.
References
[ 1 ] Oliveira S, Pijoan C. Diagnosis of Haemophilus parasuis in affected herds and use of epidemiological data to control disease. J Swine health produc 2002;10 (5):221–5. link1
[ 2 ] Oliveira S, Pijoan C. Haemophilus parasuis: new trends on diagnosis, epidemiology and control. Vet Microbiol 2004;99(1):1–12. link1
[ 3 ] Bouchet B, Vanier G, Jacques M, Gottschalk M. Interactions of Haemophilus parasuis and its LOS with porcine brain microvascular endothelial cells. Vet Res 2008;39(5):42. link1
[ 4 ] Howell KJ, Weinert LA, Peters SE, Wang J, Hernandez-Garcia J, Chaudhuri RR, et al. ‘‘Pathotyping” multiplex PCR assay for Haemophilus parasuis: a tool for prediction of virulence. J Clin Microbiol 2017;55(9):2617–28. link1
[ 5 ] Rúbies X, Kielstein P, Costa L, Riera P, Artigas C, Espuña E. Prevalence of Haemophilus parasuis serovars isolated in Spain from 1993 to 1997. Vete Microbiol 1999;66(3):245–8. link1
[ 6 ] Cu HP, Nguyen NN, Nguyen TH, Au XT, Nguyen BT, Vu NQ, et al. Determination the causes of respiratory disease in pigs rearing at some different provinces in the North Vietnam. Vet Sci Tech 2005;7(4):23–32. Vietnamese. link1
[ 7 ] Cai X, Chen H, Blackall PJ, Yin Z, Wang L, Liu Z, et al. Serological characterization of Haemophilus parasuis isolates from China. Vet Microbiol 2005;111(3):231–6. link1
[ 8 ] Smart NL, Miniats OP, Rosendal S, Friendship RM. Glasser’s disease and prevalence of subclinical infection with Haemophilus parasuis in swine in southern Ontario. Can Vet J 1989;30(4):339–43. link1
[ 9 ] Cromwell GL. Why and how antibiotics are used in swine production. Ani Biotechnol 2002;13(1):7–27. link1
[10] Blake DP, Humphry RW, Scott KP, Hillman K, Fenlon DR, Low JC. Influence of tetracycline exposure on tetracycline resistance and the carriage of tetracycline resistance genes within commensal Escherichia coli populations. J Appl Microbiol 2003;94(6):1087–97. link1
[11] Roca I, Akova M, Baquero F, Carlet J, Cavaleri M, Coenen S, et al. Corrigendum to ‘‘The global threat of antimicrobial resistance: science for intervention”. New Microb New Infec 2015;8(1):175. link1
[12] Aarestrup FM. Association between the consumption of antimicrobial agents in animal husbandry and the occurrence of resistant bacteria among food animals. Int J Antimicrob Agents 1999;12(4):279–85. link1
[13] Brogden S, Pavlovic´ A, Tegeler R, Kaspar H, De Vaan N, Kehrenberg C. Antimicrobial susceptibility of Haemophilus parasuis isolates from Germany by use of a proposed standard method for harmonized testing. Vet Microbiol 2018;217(1):32–5. link1
[14] Aarestrup FM, Seyfarth AM, Angen O. Antimicrobial susceptibility of Haemophilus parasuis and Histophilus somni from pigs and cattle in Denmark. Vet Microbiol 2004;101(2):143–6. link1
[15] De la Fuente AJM, Tucker AW, Navas J, Blanco M, Morris SJ, Gutiérrez-Martín CB. Antimicrobial susceptibility patterns of Haemophilus parasuis from pigs in the United Kingdom and Spain. Vet Microbiol 2007;120(1):184–91. link1
[16] Zhou X, Xu X, Zhao Y, Chen P, Zhang X, Chen H, et al. Distribution of antimicrobial resistance among different serovars of Haemophilus parasuis isolates. Vet Microbiol 2010;141(1–2):168–73. link1
[17] Zhao Y, Guo L, Li J, Huang X, Fang B. Characterization of antimicrobial resistance genes in Haemophilus parasuis isolated from pigs in China. PeerJ 2018;6(1):e4613. link1
[18] Guo LL, Zhang JM, Xu CG, Ren T, Zhang B, Chen Jd, et al. Detection and characterization of b-lactam resistance in Haemophilus parasuis strains from pigs in South China. J of Integrati Agri 2012;11(1):116–21. link1
[19] Hu Z, Li J, Hu S, Wang Y, Yuan X, Xu L. Phenotype and genotype analysis of antibiotic resistance of Haemophilus parasuis isolated from the scaled pig farms in Zhejiang Province. Acta Agri Boreali Sin 2013;28(4):228–33. Chinese. link1
[20] Zhang Q, Zhou M, Song D, Zhao J, Zhang A, Jin M. Molecular characterisation of resistance to fluoroquinolones in Haemophilus parasuis isolated from China. Inter J Anti Agen 2013;42(1):87–9. link1
[21] Van CN, Thanh TVT, Zou G, Jia M, Wang Q, Zhang L, et al. Characterization of serotypes and virulence genes of Haemophilus parasuis isolates from Central Vietnam. Vet Microbiol 2019;230(1):117–22. link1
[22] Clinical and Laboratory Standards Institute. Performance Standards for antimicrobial susceptibility testing. 26th ed. Wayne: Clinical and Laboratory Standards Institute; 2016. link1
[23] Lanz R, Kuhnert P, Boerlin P. Antimicrobial resistance and resistance gene determinants in clinical Escherichia coli from different animal species in Switzerland. Vet Microbiol 2003;91(1):73–84. link1
[24] Doi Y, Arakawa Y. 16S ribosomal RNA methylation: emerging resistance mechanism against aminoglycosides. Clin Infect Dis 2007;45(1):88–94. link1
[25] Dayao D, Gibson JS, Blackall PJ, Turni C. Antimicrobial resistance genes in Actinobacillus pleuropneumoniae, Haemophilus parasuis and Pasteurella multocida isolated from Australian pigs. Aust Vet J 2016;94(7):227–31. link1
[26] Guo L, Zhang J, Xu C, Zhao Y, Ren T, Zhang B, et al. Molecular characterization of fluoroquinolone resistance in Haemophilus parasuis isolated from pigs in South China. J Antimicrob Agents Chemother 2011;66(3):539–42. link1
[27] Keyes K, Hudson C, Maurer JJ, Thayer S, White DG, Lee MD. Detection of florfenicol resistance genes in Escherichia coli isolated from sick chickens. J Antimicrob Agents Chemother 2000;44(2):421–4. link1
[28] Kehrenberg C, Schwarz S. Distribution of florfenicol resistance genes fexA and cfr among chloramphenicol-resistant Staphylococcus isolates. J Antimicrob Agents Chemother 2006;50(4):1156–63. link1
[29] Chen LP, Cai XW, Wang XR, Zhou XL, Wu DF, Xu XJ, et al. Characterization of plasmid-mediated lincosamide resistance in a field isolate of Haemophilus parasuis. J Antimicrob Agents Chemother 2010;65(10):2256–8. link1
[30] Gow SP, Waldner CL, Harel J, Boerlin P. Associations between antimicrobial resistance genes in fecal generic Escherichia coli isolates from cow-calf herds in western Canada. Appl Environ Microbiol 2008;74(12):3658–66. link1
[31] Rosengren LB, Waldner CL, Reid-Smith RJ. Associations between antimicrobial resistance phenotypes, antimicrobial resistance genes, and virulence genes of fecal Escherichia coli isolates from healthy grow-finish pigs. Appl Environ Microbiol 2009;75(5):1373–80. link1
[32] Nedbalcová K, Kucˇerová Z. Antimicrobial susceptibility of Pasteurella multocida and Haemophilus parasuis isolates associated with porcine pneumonia. Acta Vet Brno 2013;82(1):3–7. link1
[33] Du X-D, Wu C-M, Liu H-B, Li X-S, Beier RC, Xiao F, et al. Plasmid-mediated ArmA and RmtB 16S rRNA methylases in Escherichia coli isolated from chickens. J Antimicrob Agents Chemother 2009;64(6):1328–30. link1
[34] Ohnuki T, Imanaka T, Aiba S. Self-cloning in Streptomyces griseus of an str gene cluster for streptomycin biosynthesis and streptomycin resistance. J Bacteriol 1985;164(1):85–94. link1
[35] Sundin GW, Bender CL. Dissemination of the strA–strB streptomycin-resistance genes among commensal and pathogenic bacteria from humans, animals, and plants. Mol Ecol 1996;5(1):133–43. link1
[36] Hollingshead S, Vapnek D. Nucleotide sequence analysis of a gene encoding a streptomycin/spectinomycin adenylyltransferase. Plasmid 1985;13(1):17–30. link1
[37] Clark NC, Olsvik O, Swenson JM, Spiegel CA, Tenover FC. Detection of a streptomycin/spectinomycin adenylyltransferase gene (aadA) in Enterococcus faecalis. J Antimicrob Agents Chemother 1999;43(1):157–60. link1
[38] San Millan A, Escudero JA, Catalan A, Nieto S, Farelo F, Gibert M, et al. b-lactam resistance in Haemophilus parasuis is mediated by plasmid pB1000 bearing bla (ROB-1). J Antimicrob Agents Chemother 2007;51(6):2260–4. link1
[39] Belmahdi M, Bakour S, Al Bayssari C, Touati A, Rolain JM. Molecular characterisation of extended-spectrum b-lactamase- and plasmid AmpCproducing Escherichia coli strains isolated from broilers in Bejaia, Algeria. J Glob Antimicrob Resist 2016;6(1):108–12. link1
[40] Tayh G, Ben Sallem R, Ben Yahia H, Gharsa H, Klibi N, Boudabous A, et al. First report of extended-spectrum b-lactamases among clinical isolates of Klebsiella pneumoniae in Gaza Strip, Palestine. Microb Drug Resist 2017;23(2):169–76. link1
[41] Majlesi A, Kakhki RK, Mozaffari Nejad AS, Mashouf RY, Roointan A, Abazari M, et al. Detection of plasmid-mediated quinolone resistance in clinical isolates of Enterobacteriaceae strains in Hamadan, West of Iran, Saudi. J Biol Sci 2018;25 (3):426–30. link1
[42] Akiko T, Naomi K, Yukano K, Kikutarou E, Mitsuhiro O, Eiji Y, et al. Mutational analysis of reduced telithromycin susceptibility of Streptococcus pneumoniae isolated clinically in Japan. FEMS Microbiol Lett 2010;307(1):87–93. link1
[43] Vo ATT, Van Duijkeren E, Gaastra W, Fluit AC. Antimicrobial resistance, class 1 integrons, and genomic island 1 in Salmonella isolates from Vietnam. PLoS ONE 2010;5(2):e9440. link1
[44] Lancashire JF, Terry TD, Blackall PJ, Jennings MP. Plasmid-encoded Tet B tetracycline resistance in Haemophilus parasuis. J Antimicrob Agents Chemother 2005;49(5):1927–31. link1
[45] Amato R, Lim P, Miotto O, Amaratunga C, Dek D, Pearson RD, et al. Genetic markers associated with dihydroartemisinin-piperaquine failure in Plasmodium falciparum malaria in Cambodia: a genotype-phenotype association study. Lancet Infect Dis 2017;17(2):164–73. link1
[46] Witkowski B, Duru V, Khim N, Ross LS, Saintpierre B, Beghain J, et al. A surrogate marker of piperaquine-resistant Plasmodium falciparum malaria: a phenotype-genotype association study. Lancet Infect Dis 2017;17(2):174–83. link1
[47] Winokur PL, Vonstein DL, Hoffman LJ, Uhlenhopp EK, Doern GV. Evidence for transfer of CMY-2 AmpC b-lactamase plasmids between Escherichia coli and Salmonella isolates from food animals and humans. J Antimicrob Agents Chemother 2001;45(10):2716–22. link1
[48] Travis RM, Gyles CL, Reid-Smith R, Poppe C, McEwen SA, Friendship R, et al. Chloramphenicol and kanamycin resistance among porcine Escherichia coli in Ontario. J Antimicrob Agents Chemother 2006;58(1):173–7. link1
[49] Boerlin P, Travis R, Gyles CL, Reid-Smith R, Janecko N, Lim H, et al. Antimicrobial resistance and virulence genes of Escherichia coli isolates from swine in Ontario. Appl Environ Microbiol 2005;71(11):6753–61. link1
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