doi: 10.14202/vetworld.2017.1118-1128
Share this article on [Facebook] [LinkedIn]
Article history: Received: 24-02-2017, Accepted: 18-08-2017, Published online: 24-09-2017
Corresponding author: Hanaa Mohamed Fadel
E-mail: hanaamohamedfadel@ymail.com
Citation: Fadel HM, Afifi R, Al-Qabili DM (2017) Characterization and zoonotic impact of Shiga toxin producing Escherichia coli in some wild bird species, Veterinary World, 10(9): 1118-1128.Aim: Wild birds are considered silent vectors of some zoonotic water and food borne pathogens of public health significance. Owing to the importance of Shiga toxin producing Escherichia coli (STEC) as the most pathogenic among the emerging diarrheagenic E. coli groups that can infect man; the present study was designed to detect the occurrence of STEC among wild birds in Egypt.
Materials and Methods: A total of 177 intestinal content swab samples originating from five wild bird species were investigated for the presence of E. coli and STEC by standard culture methods. Suspect STEC isolates were further characterized by serotyping, random amplified polymorphic DNA polymerase chain reaction (RAPD PCR), antimicrobial resistance pattern and PCR detection of stx1, stx2, and eae genes.
Results: A total of 30 suspect STEC isolates from 30 positive birds' samples were detected and identified on STEC CHROMagar (semi-captive pigeons, 15; house crows, 8; cattle egrets, 3; moorhens, 2; and house teals, 2). 25 isolates were grouped into 13 serogroups (O:20, O:25, O:26, O:27, O:63, O:78, O:111, O:114, O:125, O:128, O:142, O:153, and O:158), while five were rough strains. The distribution of STEC virulence genes among wild birds was as follows: 16 birds carried stx1 gene only (nine pigeons [28.1%], six crows [7.1%], and one cattle egret [5.6%]). stx1 and stx2 genes together were detected in four birds (one cattle egret [5.6%], two moorhens [6.1%], and one house teal, [10%]). Only one pigeon (3.1%) possessed the three alleles. Disk diffusion test results showed that cefixime was the most effective against STEC serotypes with (93.3%) sensitivity, followed by gentamycin (56.7%), and amoxicillin (50%). On the other hand, all the recovered STEC isolates were resistant to cefotaxime, doxycycline, cephalothin, and sulfisoxazole. RAPD fingerprinting using primers OPA-2 and OPA-9 showed that STEC isolates were heterogeneous; they yielded 30 and 27 different clusters, respectively.
Conclusion: Wild birds carry STEC and may add to the contamination of the surrounding environment.
Keywords: antibiotic, eae, random-amplified polymorphic DNA polymerase chain reaction, Shiga toxin producing Escherichia coli, stx1, stx2, wild birds.
1. WHO. (2016) E. coli Fact Sheet. Available from: http://www.who.int/mediacentre/factsheets/fs125/en. Viewed on 02-02-2017.
2. Espenhain, L.E. (2013) Epidemiology and surveillance of three diarrheagenic Escherichia coli in Denmark between 2000-2012-can surveillance be improved? Master of Public Health Science, Faculty of the Health and Medical Sciences. University of Copenhagen, Denmark.
3. Garcia, A., Fox, J.G. and Besser, T.E. (2010) Zoonotic enterohemorrhagic Escherichia coli: A one health perspective. ILARJ, 51(3): 221-232. [Crossref]
4. Kappeli, U., Hachler, H., Giezendanner, N., Beutin, L. and Stephan, R. (2011) Human infections with non-O157 Shiga toxin-producing Escherichia coli, Switzerland, 2000-2009. Emerg. Infect. Dis., 17(2): 180-185. [Crossref] [PubMed] [PMC]
5. CDC-Centers for Disease Control and Prevention. (2015) Multistate outbreaks of Shiga toxin-producing Escherichia coli O26 infections linked to Chipotle Mexican grill Rrestaurants. Available from: http://www.cdc.gov/ecoli/2015/O26-H11-15/signs-symptoms.html. Viewed on 14-05-2016.
6. Hedican, E.B., Medus, C., Besser, J.M., Juni, B.A., Koziol, B., Taylor, C. and Smith, K.E. (2009) Characteristics of O157 versus non-O157 Shiga toxin-producing Escherichia coli infections in Minnesota, 2000-2006. Clin. Infect. Dis., 49(3): 358-364. [Crossref] [PubMed]
7. Gioia-Di Chiacchio, R.M., Cunha, M.P.V., Sturn, R.M., Moreno, L.Z., Moreno, A.M., Pereira, C.B.P., Martins, F.H., Franzolin, R.M., Piazza, R.M.F. and Knobl, T. (2016) Shiga toxin-producing Escherichia coli (STEC): Zoonotic risks associated with psittacine pet birds in home environments. Vet. Microbiol., 184: 27-30. [Crossref] [PubMed]
8. USDA-United States Department of Agriculture. (2012), Risk profile forpathogenic non-O157 Shiga toxin-producing Escherichia coli (non-O157 STEC). Food Safety and Inspection Service. Available from: http://www.aphis.usda.gov. Viewed on 12-02-2016.
9. Santaniello, A., Gargiulo, A., Borrelli, L., Dipineto, L., Cuomo, A., Sensale, M., Fontanella, M., Calabria, M., Musella, V., Menna L.F. and Fioretti, A. (2007) Survey of Shiga toxin-producing Escherichia coli O157: H7 in urban pigeons (Columba livia) in the city of Napoli, Italy. Ital. J. Anim. Sci., 6: 313-316. [Crossref]
10. CFSPH-The Center for Food Security and Public Health. (2016) Enterohemorrhag ic Escherichia coli and other E. coli causing hemolytic uremic syndrome. Available from: http://www.cfsph.iastate.edu/Factsheets/pdfs/e_coli.pdf. Viewed on 20-02-2017.
11. Cernicchiaro, N., Pearl, D.L., McEwen, S.A., Harpster, L., Homan, H.J., Linz, G.M. and LeJeune, J.T. (2012) Association of wild bird density and farm management factors with the prevalence of E. coli O157 in dairy herds in Ohio (2007-2009). Zoonoses Public Health, 59(5): 320-329. [Crossref] [PubMed]
12. Dutta, P., Borah, M.K., Sarmah, R. and Gangil, R. (2013) Isolation, histopathology and antibiogram of Escherichia coli from pigeons (Columba livia). Vet. World, 6(2): 91-94. [Crossref]
13. Nielsen, E.M., Skov, M.N., Madsen, J.J., Lodal, J., Jespersen, J.B. and Baggesen, D.L. (2004) Verocytotoxin-producing Escherichia coli in wild birds and rodents in close proximity to farms. Appl. Environ. Microbiol., 70(11): 6944-6947. [Crossref] [PubMed] [PMC]
14. Foster, G., Evans, J., Knight, H.I., Smith, A.W., Gunn, G.J., Allison, L.J., Synge, B.A. and Pennycott, T.W. (2006) Analysis of feces samples collected from a wild-bird garden feeding station in Scotland for the presence of verocytotoxin producing Escherichia coli O157. Appl. Environ. Microbiol., 72(3): 2265-2267. [Crossref] [PubMed] [PMC]
15. Persad, A.K. and LeJeune, J.T. (2014) Animal reservoirs of Shiga toxin-producing E. coli. Microbiol. Spectr., 2(4): EHEC-0027-2014.
16. Kobayashi, H., Pohjanvirta, T. and Pelkonen, S. (2002) Prevalence and characteristics of intimin-and Shiga toxin-producing Escherichia coli from gulls, pigeons and broilers in Finland. J. Vet. Med. Sci., 64(11): 1071-1073. [Crossref]
17. Kobayashi, H., Kanazaki, M., Hata, E. and Kubo, M. (2009) Prevalence and characteristics of eae- and stx-positive strains of Escherichia coli from wild birds in the immediate environment of Tokyo Bay. Appl. Environ. Microbiol., 75(1): 292-295. [Crossref] [PubMed] [PMC]
18. Hasan, B., Sandegren, L., Melhus, A., Drobni, M., Hernandez, J., Waldenstrom, J., Alam, M. and Olsen, B. (2012) Antimicrobial drug-resistant Escherichia coli in wild birds and free-range poultry, Bangladesh. Emerg. Infect. Dis., 18(12): 2055-2058. [Crossref] [PubMed] [PMC]
19. Stenkat, J., Krautwald-Junghanns, M.E. and Schmidt, V. (2013) Causes of morbidity and mortality in free-living birds in an urban environment in Germany. Ecohealth., 10(4): 352-365. [Crossref] [PubMed]
20. Koochakzadeh, A., Askari, B.M., Zahraei, S.T., Aghasharif, S., Soltani, M. and Ehsan, M.R. (2015) Prevalence of Shiga toxin-producing and enteropathogenic Escherichia coli in wild and pet birds in Iran. Braz. J. Poult. Sci., 17(4): 445-450. [Crossref]
21. Fukushima, H., Hoshina, K. and Gomyoda, M. (1999) Long-term survival of Shiga toxin-producing Escherichia coli O26, O111, and O157 in bovine feces. Appl. Environ. Microbiol., 65: 5177-5181. [PubMed] [PMC]
22. Neher, S., Hazarika, A.K., Barkalita, L.M., Borah, P., Bora, D.P. and Sharma, R.K. (2016) Isolation and characterization of Shiga toxigenic Escherichia coli of animal and bird origin by multiplex polymerase chain reaction. Vet. World, 9(2): 123-127. [Crossref] [PubMed] [PMC]
23. Pedersen, K. and Clark, L. (2007) A review of Shiga toxin Escherichia coli and Salmonella enterica in cattle and free-ranging birds: Potential association and epidemiological links. Hum. Wildl. Confl., 1(1): 68-77.
24. Guenther, S., Ewers, C. and Wieler, L.H. (2010) Extended-spectrum beta-lactamases producing E. coli in wildlife, yet another form of environmental pollution? Front Microbiol., 2: 246-259.
25. Shobrak, M.Y. and Abo-Amer, E. (2014) Role of wild birds as carriers of multi-drug resistant Escherichia coli and Escherichia vulneris. Braz. J. Microbiol., 45(4): 1199-1209. [Crossref]
26. Veldman, K., van Tulden, P., Kant, A., Testerink, J. and Mevius, D. (2013) Characteristics of cefotaxime-resistant Escherichia coli from wild birds in the Netherlands. Appl. Environ. Microbiol., 79(24): 7556-7561. [Crossref] [PubMed] [PMC]
27. Cole, D., Drum, D.J., Stalknecht, D.E., White, D.G., Lee, M.D., Ayers, S., Sobsey, M. and Maurer, J.J. (2005) Free-living Canada geese and antimicrobial resistance. Emerg. Infect. Dis., 11: 935-938. [Crossref] [PubMed] [PMC]
28. Alcala, L., Alonso, C.A., Simon, C., Gonzalez-Esteban, C., Oros, J., Rezusta, A., Ortega, C. and Torres, C. (2016) Wild Birds, frequent carriers of extended-spectrum β-lactamase (ESBL) producing Escherichia coli of CTX-M and SHV-12 types. Microb. Ecol., 72(4): 861-869. [Crossref] [PubMed]
29. Sabat, A.J., Budimir, A., Nashev, D., Sa-Leao, R., van Dijl, J.M., Laurent, F., Grundmann, H. and Friedrich, A.W. (2013) Overview of molecular typing methods for outbreak detection and epidemiological surveillance. Eur. Surveill., 18(4): 20380-20395. [PubMed]
30. Vogel, L., van Oorschot, E., Maas, H.M.E., Minderhoud, B. and Dijkshoorn, L. (2000) Epidemiologic typing of Escherichia coli using RAPD analysis, ribotyping and serotyping. Clin. Microbiol. Infect., 6(2): 82-87. [Crossref]
31. Mahanti, A., Samanta, I., Bandyopadhyay, S. and Joardar, S.N. (2015) Molecular characterization and antibiotic susceptibility pattern of caprine Shiga toxin producing-Escherichia coli (STEC) isolates from India. Iran. J. Vet. Res., 16(1): 31-35. [PubMed] [PMC]
32. AVMA Guidelines on Euthanasia. (2007) Edition American Veterinary Medical Association 1931 N Meacham Road Schaumburg, IL.
33. USFDA. (2001) United States Food and Drug Administration for Detection, Enumeration and Identification to Species Level of Individual Organisms, Bacteriological Analytical Manual. 8th ed. U.S. Food and Drug Administration, Washington, DC.
34. Andrews, J.M. (2005) BSAC standardized disc susceptibility testing method (version 4). J. Antimicrob. Chemother., 56: 60-76. [Crossref] [PubMed]
35. Krumperman, P.H. (1983) Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Appl. Environ. Microbiol., 46(1): 165-170. [PubMed] [PMC]
36. Luczkiewicz, A., Jankowska, K., Kurlenda, J. and Olanczuk-Neyman, K. (2010) Identification and antimicrobial resistance of Enterococcus spp. isolated from surface water. Water Sci. Technol., 62(2): 466-473. [Crossref] [PubMed]
37. Madico, G., Akopyants, N.S. and Berg, D.E. (1995) Arbitrarily primed PCR DNA fingerprinting of Escherichia coli O157: H7 strains by using templates from boiled cultures. J. Clin. Microbiol., 33(6): 1534-1536. [PubMed] [PMC]
38. Lee, G.Y., Jang, H.I., Hwang, I.G. and Rhee, M.S. (2009) Prevalence and classification of pathogenic Escherichia coli isolated from fresh beef, poultry, and pork in Korea. Int. J. Food Microbiol., 134(3): 196-200. [Crossref] [PubMed]
39. Lopez-Saucedo, C., Cerna, J.F., Villegas-Sepulveda, N., Thompson, R., Velazquez, F.R., Torres, J., Tarr, P.I. and Estrada-Garcia, T. (2003) Single multiplex polymerase chain reaction to detect diverse loci associated with diarrheagenic Escherichia coli. Emerg. Infect. Dis., 9(1): 127-131. [Crossref] [PubMed]
40. Hopkins, K.L. and Hilton, A.C. (2001) Optimization of random amplification of polymorphic DNA analysis for molecular subtyping of Escherichia coli O157. Lett. Appl. Microbiol., 32(3): 126-130. [Crossref]
41. Hassell, J.M., Begon, M., Ward, M.J. and Fevre, E.M. (2017) Urbanization and disease emergence: Dynamics at the wildlife-livestock-human interface. Trends Ecol. Evol., 32(1): 55-67. [Crossref] [PubMed] [PMC]
42. Morabito, S., Dell'Omo, G., Agrimi, U., Schmidt, H., Karch, H., Cheasty, T. and Caprioli, A. (2001) Detection and characterization of Shiga toxin-producing Escherichia coli in feral Pigeons. Vet. Microbiol., 82(3): 275-283. [Crossref]
43. Gould, L.H., Mody, R.K., Ong, K.L., Clogher, P., Cronquist, A.B., Garman, K.N., Lathrop, S., Medus, C., Spina, N.L., Webb, T.H., White, P.L., Wymore, K., Gierke, R.E., Mahon, B.E. and Griffin, P.M. (2013) Increased recognition of non-O157 Shiga toxin-producing Escherichia coli infections in the United States during 2000-2010: Epidemiologic features and comparison with E. coli O157 infections. Foodborne Pathog. Dis., 10(5): 453-460. [Crossref] [PubMed]
44. Friesema, I., van der Zwaluw, K., Schuurman, T., Kooistra-Smid, M., Franz, E., van Duynhoven, Y. and van Pelt, W. (2014) Emergence of Escherichia coli encoding Shiga toxin 2f in human Shiga toxin producing E. coli (STEC) infections in the Netherlands, January 2008 to December 2011. Eur., Surveill., 19(17): 26-32. [Crossref]
45. Awad-Alla, M.E., Abdien, H.M.F. and Dessouki, A.A. (2010) Prevalence of bacteria and parasites in white ibis in Egypt. Vet. Ital., 46(3): 277-286. [PubMed]
46. Byrne, L., Vanstone, G.L., Perry, N.T., Launders, N., Adak, G.K., Godbole, G., Grant, K.A., Smith, R. and Jenkins, C. (2014) Epidemiology and microbiology of Shiga toxin-producing Escherichia coli other than serogroup O157 in England, 2009-2013. J. Med. Microbiol., 63: 1181-1188. [Crossref] [PubMed]
47. Schmidt, H., Scheef, J., Morabito, S., Caprioli, A., Wieler, L.H. and Karch, H. (2000) A new Shiga toxin 2 variant (Stx2f) from Escherichia coli isolated from pigeons. Appl. Environ. Microbiol., 66(3): 1205-1208. [Crossref]
48. Wani, S.A., Samanta, I., Bhat, M.A. and Nishikawa, Y. (2004) Investigation of Shiga toxin-producing Escherichia coli in avian species in India. Lett. Appl. Microbiol., 39(5): 389-394. [Crossref] [PubMed]
49. Grobmann, K.M. (2010) Isolation and Characterization of Shiga Toxin-Producing Escherichia coli (STEC) in Pigeons. Doctoral Thesis. Universitatsbibliothek, Garystr. 39, 14195 Berlin Institutional Repository of the Freie Universitat Berlin.
50. Bonnedahl, J. and Jarhult, J.D. (2014) Antibiotic resistance in wild birds. Ups. J. Med. Sci., 119(2): 113-116. [Crossref] [PubMed] [PMC]
51. Mora, A., Blanco, J.E., Blanco, M., Alonso, M.P., Dhabi, G., Echeita, A., Gonzalez, E.A., Bernardez, M.I. and Blanco, J. (2005) Antimicrobial resistance of Shiga toxin (verotoxin)-producing Escherichia coli O157: H7 and non-O157 strains isolated from humans, cattle, sheep and food in Spain. Res. Microbiol., 156(7): 793-806. [Crossref] [PubMed]
52. Gomes, A.R., Muniyappa, L., Krishnappa, G., Suryanarayana, V.V.S., Isloor, S., Prakash, B. and Hugar, P.G. (2005) Genotypic characterization of avian Escherichia coli by random amplification of polymorphic DNA. Int. J. Poult. Sci., 4(6): 378-381. [Crossref]
53. Kumar, V., Gupta, R.K., Kewalramani, H., Sikhwal, Y., Sharma, M. and Nayar, S. (2015) Genetic differentiation of Escherichia coli strains isolated from the urinary tract infected patients. Int. J. Microbiol. Allied Sci., 2(1): 17-22.
54. Idil, N. and Bilkay, I.S. (2014) Application of RAPD-PCR for determining the clonality of methicillin resistant Staphylococcus aureus isolated from different hospitals. Braz. Arch. Biol. Technol., 57(4): 548-553. [Crossref]
55. Dhanashree, B. and Mallya, S.P. (2012) Molecular typing of enteropathogenic Escherichia coli from diarrheagenic stool samples. J. Clin. Diagn. Res., 6(3): 400-404.
56. Wang, G., Whittam, T.S., Berg, C.M. and Berg, D.E. (1993) RAPD (arbitrary primer) PCR is more sensitive than multilocus enzyme electrophoresis for distinguishing related bacterial strains. Nucleic Acids Res., 21(25): 5930-5933. [Crossref]