Detection of zoonotic diarrheagenic pathotypes of Escherichia coli in healthy household dogs
-
Asma Askari
,
Reza Ghanbarpour
,
Baharak Akhtardanesh
,
Mohammad Reza Aflatoonian
,
Hamid Sharifi
,
Maziar Jajarmi
,
Reza Molaei
Abstract
Background and Objectives: Intestinal pathotypes of Escherichia coli belong to the companion animals may poses potential risk to public health following zoonotic transmission. Therefore, this study was proposed to determine the virulence genes associated to diarrheagenic E. coli strains isolated from healthy pet dogs and their owners in the southeast of Iran, Kerman province.
Materials and Methods: Totally 168 E. coli isolates were collected from 49 healthy household dogs and their owners. Seventy isolates were obtained from non-pet owners as control group. Presence or absence of the virulence genes including eae, stx1, stx2, st1, lt1, ipaH, cnf1 and cnf2 were screened by conventional polymerase chain reaction (PCR) and dissemination pattern of the genes were studied among the various hosts.
Results: PCR examinations showed that the most frequent virulence gene was ipaH (6.1%) in dogs followed by eae in dog owners (6.1%) and in controls (8.6%). The most frequent pathotypes in dogs, their owners and controls were EIEC (6.1%), EHEC (4.08%) and EPEC (8.5%), respectively. In one of studied houses, both of dog and its owner harbored E. coli strains with same virulence profile (stx1/eae) and pathotype (EHEC).
Conclusion: These results collectively indicate that healthy household dogs probably are the mild reservoir of potential virulent E. coli strains with possible active transmission to their contact owner. However, even non-pet owners seemed to be a notable source of intestinal pathotypes, especially EPEC, for their environment. Transmission of E. coli pathotypes may occurs by direct contact with the reservoirs or ingestion of contaminated food. These pathotypes are potentially virulent and creates public health hazards. Further studies are needed for better understanding of dissemination mechanisms of E. coli pathotypes among humans and their pets.
1. Hale CR, Scallan E, Cronquist AB, Dunn J, Smith K, Robinson T, et al. Estimates of enteric illness attributable to contact with animals and their environments in the United States. Clin Infect Dis 2012;54 Suppl 5:S472-479.
2. Damborg P, Nielsen SS, Guardabassi L. Escherichia coli shedding patterns in humans and dogs: insights into within-household transmission of phylotypes associated with urinary tract infections. Epidemiol Infect 2009;137:1457-1464.
3. Corzo-Ariyama HA, García-Heredia A, Heredia N, García S, León J, Jaykus L, et al. Phylogroups, pathotypes, biofilm formation and antimicrobial resistance of Escherichia coli isolates in farms and packing facilities of tomato, jalapeño pepper and cantaloupe from Northern Mexico. Int J Food Microbiol 2019;290:96-104.
4. Donnenberg M (2013). Escherichia coli: pathotypes and principles of pathogenesis. Academic Press.
5. Dubreuil JD, Isaacson RE, Schifferli DM. Animal enterotoxigenic Escherichia coli. EcoSal Plus 2016;7:10.1128/ecosalplus.ESP-0006-2016.
6. Persad AK, Lejeune JT (2015). Animal reservoirs of Shiga toxin-producing Escherichia coli. In: Enterohemorrhagic Escherichia coli and other Shiga toxin-producing E. coli. American Society of Microbiology. p:231-244.
7. Pearson JS, Giogha C, Wong Fok Lung T, Hartland EL. The genetics of enteropathogenic Escherichia coli virulence. Annu Rev Genet 2016;50:493-513.
8. Jensen BH, Olsen KEP, Struve C, Krogfelt KA, Petersen AM. Epidemiology and clinical manifestations of enteroaggregative Escherichia coli. Clin Microbiol Rev 2014;27:614-630.
9. Servin AL. Pathogenesis of human diffusely adhering Escherichia coli expressing Afa/Dr adhesins (Afa/Dr DAEC): current insights and future challenges. Clin Microbiol Rev 2014;27:823-869.
10. Croxen MA, Finlay BB. Molecular mechanisms of Escherichia coli pathogenicity. Nat Rev Microbiol 2010;8: 26-38.
11. Mainil J. Escherichia coli virulence factors. Vet Immunol Immunopathol 2013;152:2-12.
12. Croxen MA, Law RJ, Scholz R, Keeney KM, Wlodarska M, Finlay BB. Recent advances in understanding enteric pathogenic Escherichia coli. Clin Microbiol Rev 2013;26:822-880.
13. Vega-Manriquez XD, Ubiarco-López A, Verdugo-Rodríguez A, Hernández-Chiñas U, Navarro-Ocaña A, Ahumada-Cota RE, et al. Pet dogs potential transmitters of pathogenic Escherichia coli with resistance to antimicrobials. Arch Microbiol 2020;202:1173-1179.
14. Markey B, Leonard F, Archambault M, Cullinane A, Maguire D (2013). Clinical veterinary microbiology e-book. Elsevier Health Sciences.
15. Alizade H, Jajarmi M, Aflatoonian MR, Kalantar-Neyestanaki D, Shoja S, Ghanbarpour R. Comparative prevalence of blaCTX-m-15 gene with virulence genes and serotypes in Klebsiella pneumoniae. Jundishapur J Microbiol 2018; 11 (4); e61285.
16. Dashti AA, Jadaon MM, Abdulsamad AM, Dashti HM. Heat treatment of bacteria: a simple method of DNA extraction for molecular techniques. Kuwait Med J 2009;41:117-122.
17. Ghanbarpour R, Aflatoonian MR, Askari A, Abiri Z, Naderi Z, Bagheri M, et al. Domestic and game pigeons as reservoirs for Escherichia coli harboring antimicrobial resistance genes. J Glob Antimicrob Resist 2020;22:571-577.
18. China B, Pirson V, Mainil J. Typing of bovine attaching and effacing Escherichia coli by multiplex in vitro amplification of virulence-associated genes. Appl Environ Microbiol 1996;62:3462-3465.
19. Aranda KRS, Fagundes-Neto U, Scaletsky ICA. Evaluation of multiplex PCRs for diagnosis of infection with diarrheagenic Escherichia coli and Shigella spp. J Clin Microbiol 2004;42:5849-5853.
20. Tóth I, Hérault F, Beutin L, Oswald E. Production of cytolethal distending toxins by pathogenic Escherichia coli strains isolated from human and animal sources: establishment of the existence of a new cdt variant (type IV). J Clin Microbiol 2003;41:4285-4291.
21. Puño-Sarmiento J, Medeiros L, Chiconi C, Martins F, Pelayo J, Rocha S, et al. Detection of diarrheagenic Escherichia coli strains isolated from dogs and cats in Brazil. Vet Microbiol 2013;166:676-680.
22. Torkan S, Bahadoranian MA, Khamesipourc F, Anyanwu MU. Detection of virulence and antimicrobial resistance genes in Escherichia coli isolates from diarrhoiec dogs in Iran. Arch Med Vet 2016;48:181-190.
23. Hammermueller J, Kruth S, Prescott J, Gyles C. Detection of toxin genes in Escherichia coli isolated from normal dogs and dogs with diarrhea. Can J Vet Res 1995;59:265-270.
24. Paula CJS de, Marin JM. Occurrence of non-O157 Shiga toxin-producing Escherichia coli in dogs with diarrhea. Cienc Rural 2008;38:1682-1686.
25. Paula CJS de, Marin JM. Multidrug-resistant Shiga toxin-producing Escherichia coli in dogs with diarrhea. Arq Bras Med Vet Zootec 2009;61:511-514.
26. Koochakzadeh A, Salehi TZ, Fasaei BN, Badouei MA. Detection of verotoxin (Shiga-like toxin)-producing and eae harboring Escherichia coli in some wild captive and domestic Equidae and Canidae. Arch Razi Inst 2014;69:157-163.
27. Salehi TZ, Badouei MA, Gohari IM. Molecular detection and antibacterial susceptibility of enteropathogenic Escherichia coli (EPEC) and shigatoxigenic Escherichia coli (STEC) strains isolated from healthy and diarrhoeic dogs. Comp Clin Path 2011;20:585-589.
28. Ghanbarpour R, Akhtardanesh B, Afsahi E, Sookhtanloo S. Molecular characterization of Escherichia coli pathotypes from diarrheic and healthy dogs. Online J Vet Res 2010;14:316-324.
29. Younis K, Baddour M, Ibrahim MS. Detection of diarrheagenic Escherichia coli in pet animals and its antibiotic resistance in Alexandria governorate. AJVS 2015;45: 113-118.
30. Derakhshandeh A, Eraghi V, Boroojeni AM, Niaki MA, Zare S, Naziri Z. Virulence factors, antibiotic resistance genes and genetic relatedness of commensal Escherichia coli isolates from dogs and their owners. Microb Pathog 2018;116:241-245.
31. Harada K, Niina A, Nakai Y, Kataoka Y, Takahashi T. Prevalence of antimicrobial resistance in relation to virulence genes and phylogenetic origins among urogenital Escherichia coli isolates from dogs and cats in Japan. Am J Vet Res 2012;73:409-417.
32. Stenske KA, Bemis DA, Gillespie BE, D’Souza DH, Oliver SP, Draughon FA, et al. Comparison of clonal relatedness and antimicrobial susceptibility of fecal Escherichia coli from healthy dogs and their owners. Am J Vet Res 2009;70:1108-1116.
33. O’Neil J. Zoonotic infections from common household pets. J Nurse Pract 2018;14:363-370.
34. Miri ST, Dashti A, Mostaan S, Kazemi F, Bouzari S. Identification of different Escherichia coli pathotypes in north and north-west provinces of Iran. Iran J Microbiol 2017;9:33-37.
35. Alizade H, Teshnizi SH, Azad M, Shojae S, Gouklani H, Davoodian P, et al. An overview of diarrheagenic Escherichia coli in Iran: A systematic review and meta-analysis. J Res Med Sci 2019;24:23.
36. Bien J, Sokolova O, Bozko P. Role of uropathogenic Escherichia coli virulence factors in development of urinary tract infection and kidney damage. Int J Nephrol 2012;2012: 681473.
37. Kaper JB, Nataro JP, Mobley HLT. Pathogenic Escherichia coli. Nat Rev Microbiol 2004;2:123-140.
38. Kaper JB. Diarrheagenic Escherichia coli. Clin Microbiol Rev 1998;11:142-201.
2. Damborg P, Nielsen SS, Guardabassi L. Escherichia coli shedding patterns in humans and dogs: insights into within-household transmission of phylotypes associated with urinary tract infections. Epidemiol Infect 2009;137:1457-1464.
3. Corzo-Ariyama HA, García-Heredia A, Heredia N, García S, León J, Jaykus L, et al. Phylogroups, pathotypes, biofilm formation and antimicrobial resistance of Escherichia coli isolates in farms and packing facilities of tomato, jalapeño pepper and cantaloupe from Northern Mexico. Int J Food Microbiol 2019;290:96-104.
4. Donnenberg M (2013). Escherichia coli: pathotypes and principles of pathogenesis. Academic Press.
5. Dubreuil JD, Isaacson RE, Schifferli DM. Animal enterotoxigenic Escherichia coli. EcoSal Plus 2016;7:10.1128/ecosalplus.ESP-0006-2016.
6. Persad AK, Lejeune JT (2015). Animal reservoirs of Shiga toxin-producing Escherichia coli. In: Enterohemorrhagic Escherichia coli and other Shiga toxin-producing E. coli. American Society of Microbiology. p:231-244.
7. Pearson JS, Giogha C, Wong Fok Lung T, Hartland EL. The genetics of enteropathogenic Escherichia coli virulence. Annu Rev Genet 2016;50:493-513.
8. Jensen BH, Olsen KEP, Struve C, Krogfelt KA, Petersen AM. Epidemiology and clinical manifestations of enteroaggregative Escherichia coli. Clin Microbiol Rev 2014;27:614-630.
9. Servin AL. Pathogenesis of human diffusely adhering Escherichia coli expressing Afa/Dr adhesins (Afa/Dr DAEC): current insights and future challenges. Clin Microbiol Rev 2014;27:823-869.
10. Croxen MA, Finlay BB. Molecular mechanisms of Escherichia coli pathogenicity. Nat Rev Microbiol 2010;8: 26-38.
11. Mainil J. Escherichia coli virulence factors. Vet Immunol Immunopathol 2013;152:2-12.
12. Croxen MA, Law RJ, Scholz R, Keeney KM, Wlodarska M, Finlay BB. Recent advances in understanding enteric pathogenic Escherichia coli. Clin Microbiol Rev 2013;26:822-880.
13. Vega-Manriquez XD, Ubiarco-López A, Verdugo-Rodríguez A, Hernández-Chiñas U, Navarro-Ocaña A, Ahumada-Cota RE, et al. Pet dogs potential transmitters of pathogenic Escherichia coli with resistance to antimicrobials. Arch Microbiol 2020;202:1173-1179.
14. Markey B, Leonard F, Archambault M, Cullinane A, Maguire D (2013). Clinical veterinary microbiology e-book. Elsevier Health Sciences.
15. Alizade H, Jajarmi M, Aflatoonian MR, Kalantar-Neyestanaki D, Shoja S, Ghanbarpour R. Comparative prevalence of blaCTX-m-15 gene with virulence genes and serotypes in Klebsiella pneumoniae. Jundishapur J Microbiol 2018; 11 (4); e61285.
16. Dashti AA, Jadaon MM, Abdulsamad AM, Dashti HM. Heat treatment of bacteria: a simple method of DNA extraction for molecular techniques. Kuwait Med J 2009;41:117-122.
17. Ghanbarpour R, Aflatoonian MR, Askari A, Abiri Z, Naderi Z, Bagheri M, et al. Domestic and game pigeons as reservoirs for Escherichia coli harboring antimicrobial resistance genes. J Glob Antimicrob Resist 2020;22:571-577.
18. China B, Pirson V, Mainil J. Typing of bovine attaching and effacing Escherichia coli by multiplex in vitro amplification of virulence-associated genes. Appl Environ Microbiol 1996;62:3462-3465.
19. Aranda KRS, Fagundes-Neto U, Scaletsky ICA. Evaluation of multiplex PCRs for diagnosis of infection with diarrheagenic Escherichia coli and Shigella spp. J Clin Microbiol 2004;42:5849-5853.
20. Tóth I, Hérault F, Beutin L, Oswald E. Production of cytolethal distending toxins by pathogenic Escherichia coli strains isolated from human and animal sources: establishment of the existence of a new cdt variant (type IV). J Clin Microbiol 2003;41:4285-4291.
21. Puño-Sarmiento J, Medeiros L, Chiconi C, Martins F, Pelayo J, Rocha S, et al. Detection of diarrheagenic Escherichia coli strains isolated from dogs and cats in Brazil. Vet Microbiol 2013;166:676-680.
22. Torkan S, Bahadoranian MA, Khamesipourc F, Anyanwu MU. Detection of virulence and antimicrobial resistance genes in Escherichia coli isolates from diarrhoiec dogs in Iran. Arch Med Vet 2016;48:181-190.
23. Hammermueller J, Kruth S, Prescott J, Gyles C. Detection of toxin genes in Escherichia coli isolated from normal dogs and dogs with diarrhea. Can J Vet Res 1995;59:265-270.
24. Paula CJS de, Marin JM. Occurrence of non-O157 Shiga toxin-producing Escherichia coli in dogs with diarrhea. Cienc Rural 2008;38:1682-1686.
25. Paula CJS de, Marin JM. Multidrug-resistant Shiga toxin-producing Escherichia coli in dogs with diarrhea. Arq Bras Med Vet Zootec 2009;61:511-514.
26. Koochakzadeh A, Salehi TZ, Fasaei BN, Badouei MA. Detection of verotoxin (Shiga-like toxin)-producing and eae harboring Escherichia coli in some wild captive and domestic Equidae and Canidae. Arch Razi Inst 2014;69:157-163.
27. Salehi TZ, Badouei MA, Gohari IM. Molecular detection and antibacterial susceptibility of enteropathogenic Escherichia coli (EPEC) and shigatoxigenic Escherichia coli (STEC) strains isolated from healthy and diarrhoeic dogs. Comp Clin Path 2011;20:585-589.
28. Ghanbarpour R, Akhtardanesh B, Afsahi E, Sookhtanloo S. Molecular characterization of Escherichia coli pathotypes from diarrheic and healthy dogs. Online J Vet Res 2010;14:316-324.
29. Younis K, Baddour M, Ibrahim MS. Detection of diarrheagenic Escherichia coli in pet animals and its antibiotic resistance in Alexandria governorate. AJVS 2015;45: 113-118.
30. Derakhshandeh A, Eraghi V, Boroojeni AM, Niaki MA, Zare S, Naziri Z. Virulence factors, antibiotic resistance genes and genetic relatedness of commensal Escherichia coli isolates from dogs and their owners. Microb Pathog 2018;116:241-245.
31. Harada K, Niina A, Nakai Y, Kataoka Y, Takahashi T. Prevalence of antimicrobial resistance in relation to virulence genes and phylogenetic origins among urogenital Escherichia coli isolates from dogs and cats in Japan. Am J Vet Res 2012;73:409-417.
32. Stenske KA, Bemis DA, Gillespie BE, D’Souza DH, Oliver SP, Draughon FA, et al. Comparison of clonal relatedness and antimicrobial susceptibility of fecal Escherichia coli from healthy dogs and their owners. Am J Vet Res 2009;70:1108-1116.
33. O’Neil J. Zoonotic infections from common household pets. J Nurse Pract 2018;14:363-370.
34. Miri ST, Dashti A, Mostaan S, Kazemi F, Bouzari S. Identification of different Escherichia coli pathotypes in north and north-west provinces of Iran. Iran J Microbiol 2017;9:33-37.
35. Alizade H, Teshnizi SH, Azad M, Shojae S, Gouklani H, Davoodian P, et al. An overview of diarrheagenic Escherichia coli in Iran: A systematic review and meta-analysis. J Res Med Sci 2019;24:23.
36. Bien J, Sokolova O, Bozko P. Role of uropathogenic Escherichia coli virulence factors in development of urinary tract infection and kidney damage. Int J Nephrol 2012;2012: 681473.
37. Kaper JB, Nataro JP, Mobley HLT. Pathogenic Escherichia coli. Nat Rev Microbiol 2004;2:123-140.
38. Kaper JB. Diarrheagenic Escherichia coli. Clin Microbiol Rev 1998;11:142-201.
| Files | ||
| Issue | Vol 12 No 6 (2020) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v12i6.5026 | |
| Keywords | ||
| Escherichia coli; Virulence; Dog; Zoonotic enteropathogens | ||
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How to Cite
1.
Askari A, Ghanbarpour R, Akhtardanesh B, Aflatoonian MR, Sharifi H, Jajarmi M, Molaei R. Detection of zoonotic diarrheagenic pathotypes of Escherichia coli in healthy household dogs. Iran J Microbiol. 2020;12(6):522-530.
