Acta Vet. Brno 2020, 89: 273-282
https://doi.org/10.2754/avb202089030273
A complex approach to a complex problem: the use of whole-genome sequencing in monitoring avian-pathogenic Escherichia coli – a review
References
1. E-M, Glodde S, Li G, Sharifi R, Homeier T, Laturnus C, Diehl I, Bethe A, Philipp H-C, Preisinger R, Wieler LH, Ewers C 2008: The chicken as a natural model for extraintestinal infections caused by avian pathogenic Escherichia coli (APEC). Microb Pathogen 45: 361-369
<https://doi.org/10.1016/j.micpath.2008.08.005>
2. J, Mlynárčik P, Procházková P, Röderová M, Mezerová K, Kolář M 2018: Occurrence of bacteria with a dangerous extent of antibiotic resistance in poultry in the Central Region of Moravia. Acta Vet Brno 87: 165-172
<https://doi.org/10.2754/avb201887020165>
3. O, Christenson JK, Denamur E, Gordon DM 2013: The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylogroups. Environ Microbiol Rep 5: 58-65
<https://doi.org/10.1111/1758-2229.12019>
4. C, Kemmett K, Williams N, Wigley P 2014: Is the concept of avian pathogenic Escherichia coli as a single pathotype fundamentally flawed? Front Vet Sci 1: 1-4
<https://doi.org/10.3389/fvets.2014.00005>
5. G, Woodward MJ, Wu H, Alanazi M, Wallis T, La Ragione RM 2016: Comparative genomics of European avian pathogenic E. coli (APEC). BMC Genom 17: 960
<https://doi.org/10.1186/s12864-016-3289-7>
6. ML, Reid CJ, Roy Chowdhury P, Bushell RN, Esbert N, Tivendale KA, Noormohammadi AH, Islam S, Marenda MS, Browning GF, Markham PF, Djordjevic SP 2019: Whole genome sequence analysis of Australian avian pathogenic Escherichia coli that carry the class 1 integrase gene. Microb Genom 5: e000250
7. MPV, Saidenberg AB, Moreno AM, Ferreira AJP, Vieira MAM, Gomes TAT, Knöbl T 2017: Pandemic extra-intestinal pathogenic Escherichia coli (ExPEC) clonal group O6-B2-ST73 as a cause of avian colibacillosis in Brazil. PLoS One: 12, e0178970-e0178970
<https://doi.org/10.1371/journal.pone.0178970>
8. WD, Ferreira A, Brocchi M, Maria de Hollanda L, Pestana de Castro AF, Tatsumi Yamada A, Lancellotti M 2002: Biological characteristics and pathogenicity of avian Escherichia coli strains. Vet Microbiol 85: 47-53
<https://doi.org/10.1016/S0378-1135(01)00482-5>
9. K, Projahn M, Semmler T, Roesler U, Friese A 2017: Extended-spectrum beta-lactamase-/AmpC beta-lactamase-producing Enterobacteriaceae in broiler farms: transmission dynamics at farm level. Microb Drug Resist 24: 511-518
<https://doi.org/10.1089/mdr.2017.0150>
10. AP, Woodford N 2015: Extra-intestinal pathogenic Escherichia coli (ExPEC): Diseae, carriage and clones. J Infect 71: 615-626
<https://doi.org/10.1016/j.jinf.2015.09.009>
11. A, Fischet EAJ, van der Goot J, Stegeman A, Mevius D 2019: Transmission routes of ESBL/pAmpC producing bacteria in the broiler production pyramid, a literature review. Prevent Vet Med 162: 136-150
<https://doi.org/10.1016/j.prevetmed.2018.12.002>
12. M, Fairbrother JM 1999: Avian pathogenic Escherichia coli (APEC). BMC Vet Res 30: 299-316
13. U 2005: (Patho-)Genomics of Escherichia coli. Inter J Med Microbiol 295: 357-371
<https://doi.org/10.1016/j.ijmm.2005.07.009>
14. Z, Kmet V 2013: Prevalence of β-lactam and fluoroquinolone resistance, and virulence factors in Escherichia coli isolated from chickens in Slovakia. Biologia 68: 11-17
<https://doi.org/10.2478/s11756-012-0142-6>
15. F, Hauser H, Connor TR, van Diemen PM, Prescott G, Langridge GC, Eckert S, Chaudhuri RR, Ewers C, Mellata M, Mukhopadhyay S, Curtiss R 3rd, Dougan G, Wieler LH, Thomson NR, Pickard DJ, Stevens MP 2013: Sequencing and functional annotation of avian pathogenic Escherichia coli serogroup O78 strains reveal the evolution of E. coli lineages pathogenic for poultry via distinct mechanisms. Infect Immun 81: 838-849
<https://doi.org/10.1128/IAI.00585-12>
16. C, Janßen T, Kießling S, Philipp HC, Wieler LH 2005: Rapid detection of virulence-associated genes in avian pathogenic Escherichia coli by multiplex polymerase chain reaction. Av Dis 49: 269-273
<https://doi.org/10.1637/7293-102604R>
17. C, Li G, Wilking H, Kieβling S, Alt K, Antáo E-M, Laturnus C, Diehl I, Glodde S, Homeier T, Böhnke U, Steinrück H, Philipp HC, Wieler LH 2007: Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli: How closely related are they? Inter J Med Microbiol 297: 163-176
<https://doi.org/10.1016/j.ijmm.2007.01.003>
18. C, Antão EM, Diehl I, Philipp HC, Wieler LH 2009: Intestine and environment of the chicken as reservoirs for extraintestinal pathogenic Escherichia coli strains with zoonotic potential. Appl Environ Microbiol 75: 184-192
<https://doi.org/10.1128/AEM.01324-08>
19. TF, Fávaro C, Ingberman M, Beirao BCB, Inoue A, Gomes L, Caron LF 2013: Effect of spray Escherichia coli vaccine on the immunity of poultry. Av Dis 57: 671-675
<https://doi.org/10.1637/10456-112612-ResNote.1>
20. CA, Benham ML, Adams LM, Whithear KG, Bettelheim KA, Crabb BS, Browning GF 2000: Colonization of the respiratory tract by a virulent strain of avian Escherichia coli requires carriage of a conjugative plasmid. Infect Immun 68: 1535-1541
<https://doi.org/10.1128/IAI.68.3.1535-1541.2000>
21. D, Campagnari E, Ruffoni LS, Pesente P, Ortali G, Furlattini V 2005: Avian pathogenic Escherichia coli transmission from broiler breeders to their progeny in an integrated poultry production chain. Av Pathol 34: 313-318
<https://doi.org/10.1080/03079450500179046>
22. R, Schouler C 2015: Avian colibacillosis: still many black holes. FEMS Microbiol Lett 362
23. PM, Graat EA, van Hoek AH, Veenman C, de Jong MC, van Duijkeren E 2016: Transmission dynamics of extended-spectrum beta-lactamase-producing Escherichia coli in a broiler flock without antibiotic use. Prev Vet Med 131: 12-19
<https://doi.org/10.1016/j.prevetmed.2016.07.001>
24. RA, Cryer TL, Lafi SQ, Basha EA, Good L, Tarazi YH 2019: Identification of Escherichia coli from broiler chickens in Jordan, their antimicrobial resistance, gene characterization and the associated risk factors. BMC Vet Res 15: 159
<https://doi.org/10.1186/s12917-019-1901-1>
25. JR, Russo TA 2005: Molecular epidemiology of extraintestinal pathogenic (uro-pathogenic) Escherichia coli. Inter J Med Microbiol 295: 383-404
<https://doi.org/10.1016/j.ijmm.2005.07.005>
26. TJ, Siek KE, Johnson SJ, Nolan LK 2005: DNA Sequence and comparative genomics of pAPEC-O2-R, an avian pathogenic Escherichia coli transmissible R plasmid. Antimicrob Agents Chemother 49: 4681-4688
<https://doi.org/10.1128/AAC.49.11.4681-4688.2005>
27. TJ, Siek KE, Johnson SJ, Nolan LK 2006: DNA sequence of a ColV plasmid and prevalence of selected plasmid-encoded virulence genes among avian Escherichia coli strains. J Bacteriol 188: 745-758
<https://doi.org/10.1128/JB.188.2.745-758.2006>
28. TJ, Kariyawasam S, Wannemuehler Y, Mangiamele P, Johnson SJ, Doetkott C, Skyberg JA, Lynne AM, Johnson JR, Nolan LK 2007: The genome sequence of avian pathogenic Escherichia coli strain O1:K1:H7 shares strong similarities with human extraintestinal pathogenic E. coli genomes. J Bacteriol 189: 3228-3236
<https://doi.org/10.1128/JB.01726-06>
29. TJ, Wannemuehler Y, Doetkott C, Johnson SJ, Rosenberger SC, Nolan LK 2008: Identification of minimal predictors of avian pathogenic Escherichia coli virulence for use as a rapid diagnostic tool. J Clin Microbiol 46: 3987-3996
<https://doi.org/10.1128/JCM.00816-08>
30. TJ, Jordan D, Kariyawasam S, Stell AL, Bell NP, Wannemuehler YM, Alarcón CF, Li G, Tivendale KA, Logue CM, Nolan LK 2010: Sequence analysis and characterization of a transferable hybrid plasmid encoding multidrug resistance and enabling zoonotic potential for extraintestinal Escherichia coli. Infect Immun 78: 1931-1942
<https://doi.org/10.1128/IAI.01174-09>
31. TJ, Wannemuehler Y, Kariyawasam S, Johnson JR, Logue CM, Nolan LK 2012: Prevalence of avian-pathogenic Escherichia coli strain O1 genomic islands among extraintestinal and commensal E. coli isolates. J Bacteriol 194: 2846-2853
<https://doi.org/10.1128/JB.06375-11>
32. K, Humphrey T, Rushton S, Close A, Wigley P, Williams NJ 2013: A longitudinal study simultaneously exploring the carriage of APEC virulence associated genes and the molecular epidemiology of faecal and systemic E. coli in commercial broiler chickens. PLoS ONE 8: e67749
<https://doi.org/10.1371/journal.pone.0067749>
33. K, Williams NJ, Chaloner G, Humphrey S, Wigley P, Humphrey T 2014: The contribution of systemic Escherichia coli infection to the early mortalities of commercial broiler chickens. Av Pathol 43: 37-42
<https://doi.org/10.1080/03079457.2013.866213>
34. T, Kollarcikova M, Crhanova M, Karasova D, Cejkova D, Sebkova A, Matiasovicova J, Faldynova M, Pokorna A, Cizek A, Rychlik I 2019: Contact with adult hen affects development of caecal microbiota in newly hatched chicks. PLoS ONE 14: e0212446
<https://doi.org/10.1371/journal.pone.0212446>
35. H, Friese A, von Salviati C, Guerra B, Kasbohrer A, Kreienbrock L, Roesler U 2013: Longitudinal monitoring of extended-spectrum-beta-lactamase/AmpC-producing Escherichia coli at German broiler chicken fattening farms. Appl Environ Microbiol 79: 4815-4820
<https://doi.org/10.1128/AEM.00856-13>
36. C, Mahjoub-Messai F, Dupont D, Caro V, Diancourt L, Bingen E, Bidet P, Bonacorsi S 2013: A conserved virulence plasmidic region contributes to the virulence of the multiresistant Escherichia coli meningitis strain S286 belonging to phylogenetic group C. PLoS ONE 8: e74423
<https://doi.org/10.1371/journal.pone.0074423>
37. CM, Stegger M, Aziz M, Johnson TJ, Waits K, Nordstrom L, Gauld L, Weaver B, Rolland D, Statham S, Horwinski J, Sariya S, Davis GS, Sokurenko E, Keim P, Johnson JR, Price LB 2018: Escherichia coli ST131-H22 as a foodborne uropathogen. mBio 9: e00470-18
38. T, Petkau A, Knox N, Graham M, Van Domselaar G 2016: A primer on infectious disease bacterial genomics. Clin Microbiol Rev 29: 881-913
<https://doi.org/10.1128/CMR.00001-16>
39. RP, Logue CM, Casas MRT, Meng T, Guastalli EAL, Rojas TCG, Montelli AC, Sadatsune T, de Carvalho Ramos M, Nolan LK, da Silveira WD 2014: Overlapped sequence types (STs) and serogroups of avian pathogenic (APEC) and human extra-intestinal pathogenic (ExPEC) Escherichia coli isolated in Brazil. PLoS ONE 9: e105016
<https://doi.org/10.1371/journal.pone.0105016>
40. AR 2016: Escherichia coli and urinary tract infections: the role of poultry-meat. J Clin Microbiol Infect 22: 122-129
<https://doi.org/10.1016/j.cmi.2015.11.010>
41. VG, de Pace F, Carlos C, Mistretta Pires M, Amabile de Campos T, Nakazato G, Guedes Stheling E, Logue CM, Nolan LK, Dias da Silveira 2011: Subpathotypes of avian pathogenic Escherichia coli (APEC) exist as defined by their syndromes and virulence traits. Open Microbiol J 5: 55-64
<https://doi.org/10.2174/1874285801105010055>
42. AJ, Peirano G, Pitout JDD 2015: The role of epidemic resistance plasmids and international high-risk clones in the spread of multidrug-resistant Enterobacteriaceae. Clin Microbiol Rev 28: 565-591
<https://doi.org/10.1128/CMR.00116-14>
43. H, Chantziaras I, Iguer-Ouada M, Moula N, Garmyn A, Martel A, Touati A, Smet A, Haesebrouck F, Boyen F 2016: Presence of antimicrobial resistance in coliform bacteria from hatching broiler eggs with emphasis on ESBL/AmpC-producing bacteria. Av Pathol 45: 493-500
<https://doi.org/10.1080/03079457.2016.1167837>
44. RD, Boyle CR, Lenarduzzi TA, Jones, LS 1999: Consequences to chicks hatched from Escherichia coli inoculated embryos. Av Dis 43: 553-563
<https://doi.org/10.2307/1592656>
45. A, López C, Dabhi G, Blanco M, Blanco JE, Alonso MP, Herrera A, Mamani R, Bonacorsi S, Moulin-Schouleur M, Blanco J 2009: Extraintestinal pathogenic Escherichia coli O1:K1:H7/NM from human and avian origin: detection of clonal groups B2 ST95 and D ST59 with different host distribution. BMC Microbiol 9: 132
<https://doi.org/10.1186/1471-2180-9-132>
46. A, Viso S, López, C, Alonso MP, García-Garrote F, Dabhi G, Mamani R, Herrera A, Marzoa J, Blanco M, Blanco JE, Moulin-Schouleur M, Schouler C, Blanco J 2013: Poultry as reservoir for extraintestinal pathogenic Escherichia coli O45:K1:H7-B2-ST95 in humans. Vet Microbiol 167: 506-512
<https://doi.org/10.1016/j.vetmic.2013.08.007>
47. M, Répérant M, Laurent S, Brée A, Mignon-Grasteau S, Germon P, Rasschaert D, Schouler C 2007: Extraintestinal pathogenic Escherichia coli strains of avian and human origin: link between phylogenetic relationships and common virulence patterns. J Clin Microbiol 45: 3366-3376
<https://doi.org/10.1128/JCM.00037-07>
48. K, Cook JKA, Frazier JA, Narita M 1992: Escherichia coli multiplication and lesions in the respiratory tract of chickens inoculated with infectious bronchitis virus and/or E. coli. Av Dis 36: 881-890
<https://doi.org/10.2307/1591546>
49. K, Ueda H, Tanimura T, Noguchi K 1994: Effect of mixed live vaccine (Newcastle disease and infectious bronchitis) and Mycoplasma gallisepticum on the chicken respiratory tract and on Escherichia coli infection. J Compar Pathol 111: 33-42
<https://doi.org/10.1016/S0021-9975(05)80109-4>
50. Nolan LK, Barnes HJ, Vaillancourt JP, Abdul-Aziz T, Logue CM. Colibacillosis. In: Swayne DE, Glisson JR, et al. (Eds). Diseases of Poultry. Ames, Iowa, USA: John Wiley & Sons, Inc., 2013: pp. 751-805
51. PE, Pohjola LK, Pietola ES, Heikinheimo A 2019: Direct vertical transmission of ESBL/pAmpC-producing Escherichia coli limited in poultry production pyramid. Vet Microbiol 231: 100-106
<https://doi.org/10.1016/j.vetmic.2019.03.001>
52. RH, Christensen H, Bisgaard M 2012: Comparative genomics of multiple plasmids from APEC associated with clonal outbreaks demonstrates major similarities and identifies several potential vaccine-targets. Vet Microbiol 158: 3-4
<https://doi.org/10.1016/j.vetmic.2012.03.008>
53. OO, Thomson RG, Carlson HC 1978: Aerosol exposure of ammonia, dust and Escherichia coli in broiler chickens. Canadian Vet J 19: 187-193
54. A, Masarikova M, Valcek A, Senk D, Cejkova D, Jahodarova E, Cizek A 2020: Genomic analysis of Escherichia coli strains isolated from diseased chicken in the Czech Republic. BMC Vet Res 16: 189
<https://doi.org/10.1186/s12917-020-02407-2>
55. A, Christensen JP, Kuhnert P, Bisgaard M, Olsen JE 2006: Vertical transmission of a fluoroquinolone-resistant Escherichia coli within an integrated broiler operation. Vet Microbiol 116: 120-128
<https://doi.org/10.1016/j.vetmic.2006.03.015>
56. M, Irrgang A, Roschanski N, Brenner MG, Hamprecht A, Rieber H, Käsbohrer A, Schwarz S, Rösler U, Kreienbrock L, Pfeifer Y, Fuchs S, Werner G, RESET Study Group 2018: Whole genome analyses of CMY-2-producing Escherichia coli isolates from humans, animals and food in Germany. BMC Genom 19: 601
<https://doi.org/10.1186/s12864-018-4976-3>
57. LL, Thofner I, Bisgaard M, Christensen JP, Olsen RH, Christensen H 2017: Longitudinal study of transmission of Escherichia coli from broiler breeders to broilers. Vet Microbiol 207: 13-18
<https://doi.org/10.1016/j.vetmic.2017.05.029>
58. LL, Kudirkiene E, Jorgensen SL, Djordjevic SP, Cummins ML, Christensen JP, Christensen H, Bisgaard M, Thofner I 2020: Whole genome sequence comparison of avian pathogenic Escherichia coli from acute and chronic salpingitis of egg laying hens. BMC Vet Res 16: 148
<https://doi.org/10.1186/s12917-020-02369-5>
59. SA, Boulianne M, Martineau-Doizé B, Dozois CM, Desautels C, Fairbrother JM 1997: Dynamics of Escherichia coli infection in experimentally inoculated chickens. Av Dis 41: 221-233
<https://doi.org/10.2307/1592463>
60. M, Daehre K, Roesler U, Friese A 2017: Extended-spectrum-beta-lactamase- and plasmid-encoded cephamycinase-producing enterobacteria in the broiler hatchery as a potential mode of pseudo-vertical transmission. J Appl Environ Microbiol 83: e02364-16
<https://doi.org/10.1128/AEM.02364-16>
61. M, Daehre K, Semmler T, Guenther S, Roesler U, Friese A 2018: Environmental adaptation and vertical dissemination of ESBL-/pAmpC-producing Escherichia coli in an integrated broiler production chain in the absence of an antibiotic treatment. Microb Biotechnol 11: 1017-1026
<https://doi.org/10.1111/1751-7915.13040>
62. M, Potter RF, Ferreiro A, Wallace MA, Rahim A, Ali Malik A, Siddique N, Abbas MA, D’Souza AW, Burnham C-AD, Ali N, Dantas G 2020: Genomic characterization of antibiotic resistant Escherichia coli isolated from domestic chickens in Pakistan. Front Microbiol 10: 3052
<https://doi.org/10.3389/fmicb.2019.03052>
63. KE, Giddings CW, Doetkott C, Johnson TJ, Nolan LK 2005: Characterizing the APEC pathotype. Vet Res 36: 241-256
<https://doi.org/10.1051/vetres:2004057>
64. T, Stegger M, Olsen RH, Sekse C, Nordstoga AB, Pohjanvirta T, Lilje B, Lyhs U, Andersen PS, Pedersen K 2017: Spread of avian pathogenic Escherichia coli ST117 O78:H4 in Nordic broiler production. BMC Genomics 18: 13
<https://doi.org/10.1186/s12864-016-3415-6>
65. J, Wu Z, Davies H, van Diemen PM, Milicic A, La Ragione RM, Kaiser P, Stevens MP, Dziva F 2015: Immune responses associated with homologous protection conferred by commercial vaccines for control of avian pathogenic Escherichia coli in turkeys. Vet Res 46: 5
<https://doi.org/10.1186/s13567-014-0132-5>
66. C, Schaeffer B, Brée A, Mora A, Dahbi G, Biet F, Oswald E, Mainil J, Blanco J, Moulin-Schouleur M 2012: Diagnostic strategy for identifying avian pathogenic Escherichia coli based on four patterns of virulence genes. J Clin Microbiol 50: 1673-1678
<https://doi.org/10.1128/JCM.05057-11>
67. JA, Johnson TJ, Johnson JR, Clabots C, Logue CM, Nolan LK 2006: Acquisition of avian pathogenic Escherichia coli plasmids by a commensal E. coli isolate enhances its abilities to kill chicken embryos, grow in human urine, and colonize the murine kidney. Infect Immun 74: 6287-6292
<https://doi.org/10.1128/IAI.00363-06>
68. WJ, Carnaghan RBA 1961: Escherichia coli infections in poultry. Res Vet Sci 2: 340-352
<https://doi.org/10.1016/S0034-5288(18)34938-5>
69. M, Cameron-Veas K, Badiola I, Dolz R, Majó N, Dahbi G, Viso S, Mora A, Blanco J, Piedra-Carrasco N, González-López JJ, Migura-Garcia L 2015: Diversity of multi-drug resistant avian pathogenic Escherichia coli (APEC) causing outbreaks of colibacillosis in broilers during 2012 in Spain. PLoS ONE 10: e0143191
<https://doi.org/10.1371/journal.pone.0143191>
70. KA, Logue CM, Kariyawasam S, Jordan D, Hussein A, Li G, Wannemuehler Y, Nolan LK 2010: Avian-pathogenic Escherichia coli strains are similar to neonatal meningitis E. coli strains and are able to cause meningitis in the rat model of human disease. Infect Immun 78: 3412-3419
<https://doi.org/10.1128/IAI.00347-10>
71. A, Stromberg ZR, Mellata M 2017: A recombinant multi-antigen vaccine with broad protection potential against avian pathogenic Escherichia coli. PLoS ONE 12: e0183929
<https://doi.org/10.1371/journal.pone.0183929>
72. AHAM, Veenman C, Florijn A, Huijbers PMC, Graat EAM, de Greeff S, Dierikx CM and van Duijkeren E 2018: Longitudinal study of ESBL Escherichia coli carriage on an organic broiler farm. J Antimicrob Chemother 73: 3298-3304
73. D, De Herdt P, Laevens H, Pasmans F 2004: Colibacillosis in caged layer hens: characteristics of the disease and the aetiological agent. Av Pathol 33: 117-125
<https://doi.org/10.1080/03079450310001642149>
74. VL, Crosa JH 1991: Colicin V virulence plasmids. Microbiol Rev 55: 437-450
<https://doi.org/10.1128/MMBR.55.3.437-450.1991>
75. DG, Dho-Moulin M, Wilson RA, Whittam TS 1993: Clonal relationships and variation in virulence among Escherichia coli strains of avian origin. Microb Pathogen 14: 399-409
<https://doi.org/10.1006/mpat.1993.1039>
76. TS, Wilson RA 1988: Genetic relationships among pathogenic strains of avian Escherichia coli. Infect Immun 56: 2458-2466
<https://doi.org/10.1128/IAI.56.9.2458-2466.1988>
77. A, Alborali GL, Bardotti M, Candotti P, Guadagnini PF, Anna Martino P, Stonfer M 2000: Severe Escherichia coli O111 septicaemia and polyserositis in hens at the start of lay. Av Pathol 29: 311-317
<https://doi.org/10.1080/03079450050118430>
78. S, Maurer JJ, Hubert S, De Villena JF, McDermott PF, Meng J, Ayers S, English L, White DG 2005: Antimicrobial susceptibility and molecular characterization of avian pathogenic Escherichia coli isolates. Vet Microbiol 107: 215-224
<https://doi.org/10.1016/j.vetmic.2005.01.021>
79. S, Wang C, Chang S, Tsai Y, Chou C 2019: Characterization of Escherichia coli isolated from day-old chicken fluff in Taiwanese hatcheries. Av Dis 63: 9-16
<https://doi.org/10.1637/11935-072318-Reg.1>
80. Ge X, Jiang J, Pan Z, Hu L, Wang S, Wang H, Leung FC, Dai J, Fan H 2014: Comparative genomic analysis shows that avian pathogenic Escherichia coli isolate IMT5155 (O2:K1:H5; ST complex 95, ST140) shares close relationship with ST95 APEC O1:K1 and human ExPEC O18:K1 strains. PLoS ONE 9: e112048
<https://doi.org/10.1371/journal.pone.0112048>
