2022, Volume 10, Issue 3
Engineering >> 2022, Volume 10, Issue 3 doi: 10.1016/j.eng.2021.01.015
Molecular Epidemiology of Klebsiella pneumoniae from Clinical Bovine Mastitis in Northern Area of China, 2018–2019
a Beijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China
b China Institute of Veterinary Drug Control, Beijing 100081, China
c College of Veterinary Medicine, Hunan Agricultural University, Changsha 410125, China
d Research and Innovation Office, Murdoch University, Murdoch 6150, Australia
e China Australia Joint Laboratory for Animal Health Big Data Analytics, College of Animal Science and Technology, Zhejiang Agricultural and Forestry University, Hangzhou 311300, China
Next Previous
Abstract
Klebsiella pneumoniae (K. pneumonia, KpI) is a predominate inducement of bovine mastitis, which is associated with high mortality and milk yield reduction. However, data is lacking on the molecular characteristics of bovine K. pneumoniae, limiting the risk assessment of its transmission through the food chain. Herein, we investigated the prevalence of K. pneumoniae in 6301 clinical mastitis (CM) milk samples from dairy cattle in northern area of China. In total, 183 K. pneumoniae isolates were recovered, with detection rates of 3.0% and 2.8% in 2018 and 2019, respectively. Like human clinical K. pneumoniae, all CM K. pneumoniae isolates belonged to one of three phylogroups: KpI (n = 143), Klebsiella quasipneumoniae subsp. similipneumoniae (KpII-B) (n = 37), and Klebsiella variicola (KpIII) (n = 3). We detected the extendedspectrum β-lactamase-encoding genes blaSHV-2a, blaCTX-M-14, and blaCTX-M-15, as well as clpC, lpfA, lacI, lacZ, lacY, and the fecABDEIR operon in the KpI isolates, which may contribute to their pathogenicity and host adaptability in cows. The high prevalence of KpI in dairy farms may be problematic, as it showed relatively higher rates of antibiotic resistance and virulence gene carriage than the KpII-B and KpIII isolates. Furthermore, we observed distinct differences in population structure between CM- and human infection-associated KpI isolates, with the genes associated with invasive infection in humans rarely being observed in bovine isolates, indicating that few CM-associated K. pneumoniae isolates pose a threat to human health. Nevertheless, bovine KpII-B isolates shared a high level of nucleotide sequence identity with isolates from human infections and frequently carried the nitrogen-fixation gene nif, suggesting an association between KpII-B isolates from cattle and humans, and plant-derived bacteria.
Keywords
Clinical mastitis ; Klebsiella pneumonia ; Molecular characteristics ; Population structure ; Antimicrobial resistance
SupplementaryMaterials
Figures
Fig. 1
Fig. 2
Fig. 3
Fig. 4
References
[ 1 ] Podschun R, Ullmann U. Klebsiella spp. as nosocomial pathogens: epidemiology, taxonomy, typing methods, and pathogenicity factors. Clin Microbiol Rev 1998;11(4):589–603. link1
[ 2 ] Fuenzalida MJ, Ruegg PL. Molecular epidemiology of nonsevere clinical mastitis caused by Klebsiella pneumoniae occurring in cows on 2 Wisconsin dairy farms. J Dairy Sci 2020;103(4):3479–92. link1
[ 3 ] Jamali H, Barkema HW, Jacques M, Lavallée-Bourget E-M, Malouin F, Saini V, et al. Invited review: incidence, risk factors, and effects of clinical mastitis recurrence in dairy cows. J Dairy Sci 2018;101(6):4729–46. link1
[ 4 ] Halasa T, Huijps K, Østerås O, Hogeveen H. Economic effects of bovine mastitis and mastitis management: a review. Vet Q 2007;29(1):18–31. link1
[ 5 ] Hertl JA, Schukken YH, Bar D, Bennett GJ, González RN, Rauch BJ, et al. The effect of recurrent episodes of clinical mastitis caused by gram-positive and gram-negative bacteria and other organisms on mortality and culling in Holstein dairy cows. J Dairy Sci 2011;94(10):4863–77. link1
[ 6 ] Cha E, Bar D, Hertl JA, Tauer LW, Bennett G, González RN, et al. The cost and management of different types of clinical mastitis in dairy cows estimated by dynamic programming. J Dairy Sci 2011;94(9):4476–87. link1
[ 7 ] Cha E, Hertl JA, Schukken YH, Tauer LW, Welcome FL, Gröhn YT. The effect of repeated episodes of bacteria-specific clinical mastitis on mortality and culling in Holstein dairy cows. J Dairy Sci 2013;96(8):4993–5007. link1
[ 8 ] Roberson JR, Warnick LD, Moore G. Mild to moderate clinical mastitis: efficacy of intramammary amoxicillin, frequent milk-out, a combined intramammary amoxicillin, and frequent milk-out treatment versus no treatment. J Dairy Sci 2004;87(3):583–92. link1
[ 9 ] Brisse S, Verhoef J. Phylogenetic diversity of Klebsiella pneumoniae and Klebsiella oxytoca clinical isolates revealed by randomly amplified polymorphic DNA, gyrA and parC genes sequencing and automated ribotyping. Int J Syst Evol Microbiol 2001;51(3):915–24. link1
[10] Haeggman S, Lofdahl S, Paauw A, Verhoef J, Brisse S. Diversity and evolution of the class a chromosomal beta-lactamase gene in Klebsiella pneumoniae. Antimicrob Agents Chemother 2004;48(7):2400–8. link1
[11] Brisse S, Passet V, Grimont PAD. Description of Klebsiella quasipneumoniae sp. nov., isolated from human infections, with two subspecies, Klebsiella quasipneumoniae subsp. quasipneumoniae subsp. nov. and Klebsiella quasipneumoniae subsp. similipneumoniae subsp. nov., and demonstration that Klebsiella singaporensis is a junior heterotypic synonym of Klebsiella variicola. Int J Syst Evol Microbiol 2014;64(Pt 9):3146–52. link1
[12] Rosenblueth M, Martínez L, Silva J, Martínez-Romero E. Klebsiella variicola, a novel species with clinical and plant-associated isolates. Syst Appl Microbiol 2004;27(1):27–35. link1
[13] Podder MP, Rogers L, Daley PK, Keefe GP, Whitney HG, Tahlan K, et al. Klebsiella species associated with bovine mastitis in Newfoundland. PLoS ONE 2014;9 (9):e106518. link1
[14] Yang Y, Higgins CH, Rehman I, Galvao KN, Brito IL, Bicalho ML, et al. Genomic diversity, virulence, and antimicrobial resistance of Klebsiella pneumoniae strains from cows and humans. Appl Environ Microbiol 2019;85(6). e02654- 18. link1
[15] Maatallah M, Vading M, Kabir MH, Bakhrouf A, Kalin M, Naucler P, et al. Klebsiella variicola is a frequent cause of bloodstream infection in the stockholm area, and associated with higher mortality compared to K. pneumoniae. PLOS ONE. 2014;9(11):e113539..
[16] Berry GJ, Loeffelholz MJ, Williams-Bouyer N, Ledeboer NA. An investigation into laboratory misidentification of a bloodstream Klebsiella variicola infection. J Clin Microbiol 2015;53(8):2793–4. link1
[17] Holt KE, Wertheim H, Zadoks RN, Baker S, Whitehouse CA, Dance D, et al. Genomic analysis of diversity, population structure, virulence, and antimicrobial resistance in Klebsiella pneumoniae, an urgent threat to public health. Proc Natl Acad Sci U S A 2015;112(27):E3574–81. link1
[18] Paulin-Curlee GG, Singer RS, Sreevatsan S, Isaacson R, Reneau J, Foster D, et al. Genetic diversity of mastitis-associated Klebsiella pneumoniae in dairy cows. J Dairy Sci 2007;90(8):3681–9. link1
[19] Bengtsson B, Unnerstad HE, Ekman T, Artursson K, Nilsson-Öst M, Waller KP. Antimicrobial susceptibility of udder pathogens from cases of acute clinical mastitis in dairy cows. Vet Microbiol 2009;136(1-2):142–9. link1
[20] de Jong A, Garch FE, Simjee S, Moyaert H, Rose M, Youala M, et al. VetPath Study Group. Monitoring of antimicrobial susceptibility of udder pathogens recovered from cases of clinical mastitis in dairy cows across Europe: VetPath results. Vet Microbiol 2018;213:73–81. link1
[21] Cheng J, Qu W, Barkema HW, Nobrega DB, Gao J, Liu G, et al. Antimicrobial resistance profiles of 5 common bovine mastitis pathogens in large Chinese dairy herds. J Dairy Sci 2019;102(3):2416–26. link1
[22] Timofte D, Maciuca IE, Evans NJ, Williams H, Wattret A, Fick JC, et al. Detection and molecular characterization of Escherichia coli CTX-M-15 and Klebsiella pneumoniae SHV-12 b-lactamases from bovine mastitis isolates in the United Kingdom. Antimicrob Agents Chemother 2014;58(2):789–94. link1
[23] Locatelli C, Scaccabarozzi L, Pisoni G, Moroni P. CTX-M1 ESBL-producing Klebsiella pneumoniae subsp. pneumoniae isolated from cases of bovine mastitis. J Clin Microbiol 2010;48(10):3822–3. link1
[24] Editorial Committee of China Dairy Yearbook. China Dairy Association: 2017. Beijing: China Agriculture Press; 2018. Chinese. link1
[25] He W, Ma S, Lei L, He J, Li X, Tao J, et al. Prevalence, etiology, and economic impact of clinical mastitis on large dairy farms in China. Vet Microbiol 2020;242:108570. link1
[26] Verbeke J, Piepers S, Supré K, De Vliegher S. Pathogen-specific incidence rate of clinical mastitis in Flemish dairy herds, severity, and association with herd hygiene. J Dairy Sci 2014;97(11):6926–34. link1
[27] He T, Wei R, Zhang L, Sun L, Pang M, Wang R, et al. Characterization of NDM-5- positive extensively resistant Escherichia coli isolates from dairy cows. Vet Microbiol 2017;207:153–8. link1
[28] Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals–4th edition. CLSI document VET08. Wayne (PA): Clinical and Laboratory Standards Institute; 2018..
[29] Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing–28th edition. CLSI document M100. Wayne (PA): Clinical and Laboratory Standards Institute; 2018..
[30] The European committee on antimicrobial susceptibility testing (EUCAST). EUCAST guideline for the detection of resistance mechanisms and specific resistances of clinical and/or public health importance. The European committee on antimicrobial susceptibility testing. 2018;156142–6..
[31] Ma S, Sun C, Hulth A, Li J, Nilsson LE, Zhou Y, et al. Mobile colistin resistance gene mcr-5 in porcine Aeromonas hydrophila. J Antimicrob Chemother 2018;73 (7):1777–80. link1
[32] Inouye M, Dashnow H, Raven L-A, Schultz MB, Pope BJ, Tomita T, et al. SRST2: rapid genomic surveillance for public health and hospital microbiology labs. Genome Med 2014;6(11):90. link1
[33] Ferreira ML, Araújo BF, Cerdeira LT, Toshio C, Ribas RM. Genomic features of a clinical ESBL-producing and colistin-resistant hypermucoviscous K. quasipneumoniae subsp. similipneumoniae from Brazil. Braz J Infect Dis 2019;23(3):207–9. link1
[34] Beghain J, Bridier-Nahmias A, Le Nagard H, Denamur E, Clermont O. ClermonTyping: an easy-to-use and accurate in silico method for Escherichia genus strain phylotyping. Microb Genom 2018;4(7):000192. link1
[35] Bush K, Bradford PA. Epidemiology of b-lactamase-producing pathogens. Clin Microbiol Rev 2020;33(2):33. link1
[36] Treangen TJ, Ondov BD, Koren S, Phillippy AM. The Harvest suite for rapid coregenome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol 2014;15(11):524. link1
[37] Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014;30(14):2068–9. link1
[38] Page AJ, Cummins CA, Hunt M, Wong VK, Reuter S, Holden MTG, et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 2015;31 (22):3691–3. link1
[39] Brynildsrud O, Bohlin J, Scheffer L, Eldholm V. Rapid scoring of genes in microbial pan-genome-wide association studies with Scoary. Genome Biol 2016;17:238. link1
[40] Chelius MK, Triplett EW. Immunolocalization of dinitrogenase reductase produced by Klebsiella pneumoniae in association with Zea mays L. Appl Environ Microbiol 2000;66(2):783–7. link1
[41] Gao J, Barkema HW, Zhang L, Liu G, Deng Z, Cai L, et al. Incidence of clinical mastitis and distribution of pathogens on large Chinese dairy farms. J Dairy Sci 2017;100(6):4797–806. link1
[42] de Melo MES, Cabral AB, Maciel MAV, da Silveira VM, de Souza Lopes AC. Phylogenetic groups among Klebsiella pneumoniae isolates from Brazil: relationship with antimicrobial resistance and origin. Curr Microbiol 2011;62(5):1596–601. link1
[43] Oliver SP, Murinda SE, Jayarao BM. Impact of antibiotic use in adult dairy cows on antimicrobial resistance of veterinary and human pathogens: a comprehensive review. Foodborne Pathog Dis 2011;8(3):337–55. link1
[44] Cha MK, Kang CI, Kim SH, Chung DR, Peck KR, Lee NY, et al. High prevalence of CTX-M-15-type extended-spectrum b-lactamase among AmpC b-lactamaseproducing Klebsiella pneumoniae isolates causing bacteremia in Korea. Microb Drug Resist 2018;24(7):1002–5. link1
[45] Hausherr A, Becker J, Meylan M, Wüthrich D, Collaud A, Rossano A, et al. Antibiotic and quaternary ammonium compound resistance in Escherichia coli from calves at the beginning of the -fattening period in Switzerland (2017). Schweiz Arch Tierheilkd 2019;161(11):741–8. link1
[46] Rosen DA, Hilliard JK, Tiemann KM, Todd EM, Morley SC, Hunstad DA. Klebsiella pneumoniae FimK promotes virulence in murine pneumonia. J Infect Dis 2016;213(4):649–58. link1
[47] Magill SS, Edwards JR, Bamberg W, Beldavs ZG, Dumyati G, Kainer MA, et al. Emerging Infections Program Healthcare-Associated Infections and Antimicrobial Use Prevalence Survey Team. Multistate point-prevalence survey of health care-associated infections. N Engl J Med 2014;370 (13):1198–208. link1
[48] Qin X, Wu S, Hao M, Zhu J, Ding BYang Y, et al. The colonization of carbapenem-resistant Klebsiella pneumoniae: epidemiology, resistance mechanisms, and risk factors in patients admitted to intensive care units in China. J Infect Dis 2020;221:S206–14. link1
[49] Shu L, Lu Q, Sun R, Lin L, Sun Q, Hu J, et al. Prevalence and phenotypic characterization of carbapenem-resistant Klebsiella pneumoniae strains recovered from sputum and fecal samples of ICU patients in Zhejiang Province, China. Infect Drug Resist 2019;12:1211–8. link1
[50] Bialek-Davenet S, Criscuolo A, Ailloud F, Passet V, Jones L, Delannoy-Vieillard A-S, et al. Genomic definition of hypervirulent and multidrug-resistant Klebsiella pneumoniae clonal groups. Emerg Infect Dis 2014;20(11): 1812–20. link1
[51] Struve C, Roe CC, Stegger M, Stahlhut SG, Hansen DS, Engelthaler DM, et al. Mapping the evolution of hypervirulent Klebsiella pneumoniae. MBIO 2015;6 (4). e00630-15. link1
[52] Gunaratnam G, Tuchscherr L, Elhawy MI, Bertram R, Eisenbeis J, Spengler C, et al. ClpC affects the intracellular survival capacity of Staphylococcus aureus in non-professional phagocytic cells. Sci Rep 2019;9(1):16267. link1
[53] Zhou M, Ding X, Ma F, Xu Y, Zhang J, Zhu G, et al. Long polar fimbriae contribute to pathogenic Escherichia coli infection to host cells. Appl Microbiol Biotechnol 2019;103(18):7317–24. link1
[54] Keane OM. Genetic diversity, the virulence gene profile and antimicrobial resistance of clinical mastitis-associated Escherichia coli. Res Microbiol 2016;167(8):678–84. link1
[55] Dogan B, Rishniw M, Bruant G, Harel J, Schukken YH, Simpson KW. Phylogroup and lpfA influence epithelial invasion by mastitis associated Escherichia coli. Vet Microbiol 2012;159(1–2):163–70. link1
京公网安备 11010502051620号
