Open Access
Research (Published online: 22-01-2019)
17. Bacterial isolation from internal organs of rats (Rattus rattus) captured in Baghdad city of Iraq
Nagham Mohammed Ayyal, Zainab Abdulzahra Abbas, Abdulkarim Jafar Karim, Zainab Majid Abbas, Karima Akool Al-Salihi, Jenan Mahmood Khalaf, Dunya Dhafir Mahmood, Eman Abdullah Mohammed, Rawaa Saladdin Jumaa and Dhuha Ismaeel Abdul-Majeed
Veterinary World, 12(1): 119-125

Nagham Mohammed Ayyal: Unit of Zoonotic Diseases, College of Veterinary Medicine, University of Baghdad, Baghdad, Iraq.
Zainab Abdulzahra Abbas: Unit of Zoonotic Diseases, College of Veterinary Medicine, University of Baghdad, Baghdad, Iraq.
Abdulkarim Jafar Karim: Unit of Zoonotic Diseases, College of Veterinary Medicine, University of Baghdad, Baghdad, Iraq.
Zainab Majid Abbas: Department of Pathological Analysis, Babylon Technical Institute, Al-Furat Al-Awsat Technical University, Babylon, Iraq.
Karima Akool Al-Salihi: Department of Internal and Preventive Medicine, College of Veterinary Medicine, Al-Muthanna University, Al-Muthanna, Iraq.
Jenan Mahmood Khalaf: Department of Internal and Preventive Medicine, College of Veterinary Medicine, University of Baghdad, Baghdad, Iraq.
Dunya Dhafir Mahmood: Unit of Zoonotic Diseases, College of Veterinary Medicine, University of Baghdad, Baghdad, Iraq.
Eman Abdullah Mohammed: Department of Parasitology, College of Veterinary Medicine, University of Baghdad, Baghdad, Iraq.
Rawaa Saladdin Jumaa: Department of Microbiology, College of Veterinary Medicine, University of Baghdad, Baghdad, Iraq.
Dhuha Ismaeel Abdul-Majeed: Department of Microbiology, College of Veterinary Medicine, University of Baghdad, Baghdad, Iraq.

doi: 10.14202/vetworld.2019.119-125

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Article history: Received: 10-08-2018, Accepted: 07-12-2018, Published online: 22-01-2019

Corresponding author: Abdulkarim Jafar Karim

E-mail: karimjafar59@yahoo.com

Citation: Ayyal NM, Abbas ZA, Karim AJ, Abbas ZM, Al-Salihi KA, Khalaf JM, Mahmood DD, Mohammed EA, Jumaa RS, Abdul-Majeed DI (2019) Bacterial isolation from internal organs of rats (Rattus rattus) captured in Baghdad city of Iraq, Veterinary World, 12(1): 119-125.
Abstract

Aim: Rats are accused in disseminating many zoonotic diseases. This study aimed to isolate and identify bacteria from internal organs of rats captured in Baghdad City, Iraq.

Materials and Methods: A total of 120 black rats (R. rattus) were trapped from different areas in Baghdad city. Rats were kept in individual plastic cages for 3 h before euthanizing. Deep pharyngeal swab, intestinal content, urine, and pieces of the liver and spleen, lung, kidney, and brain were obtained aseptically. The specimens were inoculated into peptone water and incubated at 37°C for 24 h for enrichment. A loopful of each specimen was then subcultured onto MacConkey Agar, Blood Agar, and Mannitol Salt Agar. CHROMagar O157 H7 and CHROMagar Listeria were used to detect Escherichia coli 157:7 and Listeria spp., respectively. Biochemical tests on analytical profile index, microscopic examination, and commercial kit for latex agglutination test for serotyping E. coli O157:H7 were used.

Results: Mixed bacterial isolates were recorded as 116, 52, 36, 28, 18, 6, and 4 from intestinal contents, deep pharyngeal, liver and spleen, urine, lung, brain, and kidney, respectively. Microorganisms included E. coli, Staphylococcus aureus, Streptococcus spp., Bacillus spp., Pseudomonas aeruginosa, Citrobacter freundii, Proteus vulgaris, E. coli O157:H7, Enterobacter cloacae, Listeria spp., Klebsiella spp., Ochrobactrum anthropi, Aeromonas spp., Brucella spp., Pseudomonas fluorescens, Escherichia fergusonii, Micrococcus spp., Morganella spp., Proteus mirabilis, Pseudomonas luteola, and Streptobacillus spp. The highest bacterial prevalence (88; 73.33%) was recorded for E. coli, where 68 isolates were identified from the intestinal contents. Of these, four isolates were E. coli O157:H7.

Conclusion: Rats are important carriers and transmitters of a number of pathogens and can disseminate these microorganisms to humans and animals.

Keywords: bacteria, different organs, Escherichia coli O157:H7, Pseudomonas aeruginosa, rat, urine.

References

1. Fayenuwo, J.O., Olakojo, S.A., Akande, M., Amusa, N.A. and Olujimi, O.A. (2007) Comparative evaluation of vertebrate pest damage on some newly developed quality protein maize (QPM) varieties in southwestern Nigeria. Afr. J. Agric. Res., 2(11): 592-595.

2. Edman, J.C., Kovacs, J.A., Masur, H., Santi, D.V., Elwood, H.J. and Sogin, M.L. (1988) Ribosomal RNA sequence shows Pneumocystis carinii to be a member of the fungi. Nature, 334(6182): 519-522. [Crossref] [PubMed]

3. Laudisoit, A., Falay, D., Amundala, N., Akaibe, D., de Bellocq, J.G., Van Houtte, N. and Socolovschi, C. (2014) High prevalence of Rickettsia typhi and Bartonella species in rats and fleas, Kisangani, Democratic Republic of the Congo. Am. J. Trop. Med. Hyg., 90(3): 463-468. [Crossref] [PubMed] [PMC]

4. Yan, Y., Zhao, Z., Wan, H., Wu, R., Fang, J. and Liu, H. (2014) A novel fungus concentration-dependent rat model for acute invasive fungal rhinosinusitis: An experimental study. BMC Infect. Dis., 14(1): 3856. [Crossref]

5. Mohebali, M., Zarei, Z., Khanaliha, K., Kia, E.B., Motavalli-Haghi, A., Davoodi, J. and Rezaeian, M. (2017) Natural intestinal protozoa in rodents (Rodentia: Gerbillinae, Murinae, Cricetinae) in Northwestern Iran. Iran. J. Parasitol., 12(3): 382-388. [PubMed] [PMC]

6. Psaroulaki, A., Antoniou, M., Toumazos, P., Mazeris, A., Ioannou, I., Chochlakis, D., Christophi, N., Loukaides, P., Patsias, A., Moschandrea, I. and Tselentis, Y. (2010) Rats as indicators of the presence and dispersal of six zoonotic microbial agents in Cyprus, an Island ecosystem: A seroepidemiological study. Trans. R. Soc. Trop. Med. Hyg., 1049(6): 733-739. [Crossref] [PubMed]

7. Zahedi, A., Paparini, A., Jian, F., Robertson, I. and Ryan, U. (2016) Public health significance of zoonotic Cryptosporidium species in wildlife: Critical insights into better drinking water management. Int. J. Parasitol. Parasites Wildl., 5(1): 88-109. [Crossref] [PubMed] [PMC]

8. Wullenweber, M. (1995) Streptobacillus moniliformis a zoonotic pathogen. Taxonomic considerations, host species, diagnosis, therapy and geographical distribution. J. Lab. Anim. Dis., 29(1): 1-16. [Crossref] [PubMed]

9. Cleri, D.J., Varnaleo, J.R., Lombardii, L.J., Rabbat, M.S., Mathew, A., Marton, R. and Reyelt, M.C. (1997) Plague pneumonia caused by Yersinia pestis. Semin. Respir. Infect., 12(1): 12-23. [PubMed]

10. Burriel, A.R., Kritas, S.K. and Kontos, V. (2008) Some microbiological aspects of rats captured alive at the port city of Piraeus, Greece. Int. J. Environ. Health Res., 18(2): 159-164. [Crossref] [PubMed]

11. Guenther, S., Grobbel, M., Beutlich, J. and Guerra, B. (2010) Detection of pandemic B2-O25-ST131 Escherichia coli harbouring the CTXM-9 extended-spectrum beta-lactamase type in a feral urban brown rat (Rattus norvegicus). J. Antimicrob. Chemother., 65(3): 582-584. [Crossref] [PubMed]

12. Nkogwe, C., Raletobana, J., Stewart-Johnson, A. and Suepaul, S. (2011) Frequency of detection of Escherichia coli, Salmonella spp., and Campylobacter spp. In the faeces of wild rats (Rattus spp.) in Trinidad and Tobago. Vet. Med. Int., 2011(20): 1-7. [Crossref] [PubMed] [PMC]

13. Adesiyun, A.A., Stewart-Johnson, A. and Thompson, N.N. (2009) Isolation of enteric pathogens from bats in Trinidad. J. Wildl. Dis., 45(4): 952-961. [Crossref] [PubMed]

14. Gopee, N.V., Adesiyun, A.A. and Caesar, K. (2000) A longitudinal study of Escherichia coli strains isolated from captive mammals, birds, and reptiles in Trinidad. J. Zoo Wildl. Med., 31(3): 353-360. [Crossref]

15. Desvars-Larrive, A., Pascal, M., Gasqui, P., Cosson, J.F., Benoit, E., Lattard, V., Crespin, L., Lorvelec, O., Pisanu, B., Teynie, A., Vayssier-Taussat, M., Bonnet, S., Marianneau, P., Lacote, S., Bourhy, P., Berny, P., Pavio, N., Le Poder, S., Gilot-Fromont, E., Jourdain, E., Hammed, A., Fourel, I., Chikh, F. and Vourc'h, G. (2017) Population genetics, community of parasites, and resistance to rodenticides in an urban brown rat (Rattus norvegicus) population. PLoS One, 12(9): e0184015. [Crossref]

16. Tsakmakidis, I., Angelopoulou, K., Dovas, C.I., Dokianakis, E., Tamvakis, A., Symeonidou, I., Antoniou, M. And Diakou, A. (2017) Leishmania infection in rodents in Greece. Trop. Med. Int. Health, 22(12): 1523-1532. [Crossref] [PubMed]

17. Struck, M.B., Andrutis, K.A., Ramirez, H.E. and Battles, A.H. (2011) Effect of a short-term fast on ketamine-xylazine anesthesia in rats. J. Am. Assoc. Lab. Anim. Sci., 50(3): 344-348. [PubMed] [PMC]

18. Chow, V.T.K., Inglis, T.J.J. and Peng-Song, K. (2006) Diagnostic clinical microbiology. In: Kun, L. Y., editor. Microbial Biotechnology. World Scientific Publishing Co. Pte. Ltd., Singapore. p539-593. [Crossref]

19. Islam, N.N., Akter, M., Farzana, Z. and Bin Kader, A. (2014) Detection of Staphylococcus aureus in frozen chicken rinse through bacteriological and Nuc gene-specific PCR methods and their drug resistance patterns in Southern Chittagong, Bangladesh. Res. J. Microb., 9(5): 251-264. [Crossref]

20. Gakuya, F.M., Kyule, M.N., Gathura, P.B. and Kariuki, S. (2001) Antimicrobial resistance of bacterial organisms isolated from rats. East Afr. Med. J., 78(12): 646-649. [Crossref]

21. Karmali, M.A., Gannon, V. and Sargeant, J.M. (2010) Verocytotoxin producing Escherichia coli (VTEC). Vet. Microbiol., 140(3-4): 360-370. [Crossref] [PubMed]

22. Moine, V.L., Vanner, P. and Jestin, A. (1987) Microbiological studies of wild rodents in farms as carriers of pig infectious agents. Prev. Vet. Med., 4(5-6): 399-408. [Crossref]

23. Savini, V., Catavitello, C., Talia, M., Manna, A., Pompetti, F., Favaro, M., Fontana, C., Febbo, F., Balbinot, A., Di Berardino, F., Di Bonaventura, G., Di Zacomo, S, Esattore, F. and D'Antonio, D. (2008) Multidrug-resistant Escherichia fergusonii: A case of acute cystitis. J. Clin. Microbiol., 46(4): 1551-1552. [Crossref] [PubMed] [PMC]

24. Funke, G., Hany, A. and Altwegg, M. (1993) Isolation of Escherichia fergusonii from four different sites in a patient with pancreatic carcinoma and cholangiosepsis. J. Clin. Microbiol., 31(8): 2201-2203. [PubMed] [PMC]

25. Mahapatra, A. and Mahapatra, S. (2005) Escherichia fergusonii: An emerging pathogen in South Orissa. Ind. J. Med. Microbiol., 23(3): 204-208. [Crossref]

26. Gaastra, W., Boot, R., Ho, H.T.K. and Lipman, L.J.A. (2009) Rat bite fever. Vet. Microbiol., 133(3): 211-228. [Crossref] [PubMed]

27. Oh, J.Y., Kang, M.S., An, B.K., Shin, E.G., Kim, M.J. and Kwon, J.H. (2012) Isolation and epidemiological characterisation of heat labile enterotoxin producing a from healthy chickens. Vet. Microbiol., 160(1-2): 170-175. [Crossref] [PubMed]

28. Simmons, K., Rempel, H., Block, G., Forgetta, V., Vaillancourt, R. and Malouin, F. (2014) Duplex PCR methods for the molecular detection of Escherichia fergusonii isolates from broiler chickens. Appl. Environ. Microbiol., 80(6); 1941-1948. [Crossref] [PubMed] [PMC]

29. Herraez, P., Rodriguez, A.F., de los Monteros, A.E., Acosta, A.B., Jaber, J.R., Castellano, J. and Castroa, A. (2005) Fibrinonecrotic typhlitis caused by Escherichia fergusonii in ostriches (Struthio camelus). Avian Dis., 49(1): 167-169. [Crossref] [PubMed]

30. Hariharan, H., Alfonso, L., Gary, C., Mada, C. and Tammy, M. (2007) Isolation of Escherichia fergusonii from the feces and internal organs of a goat with diarrhea. Can. Vet. J., 48(6): 630-631. [PubMed] [PMC]

31. Wragg, P., La Ragione, R.M., Best, A., Reichel, R., Anjum, M.F. and Mafura, M. (2009) Characterisation of Escherichia fergusonii isolates from farm animals using an Escherichia coli virulence gene array and tissue culture adherence assays. Res. Vet. Sci., 86(1): 27-35. [Crossref] [PubMed]

32. Weiss, A.T.A., Lubke-Becker, A., Krentz, M. and van der Grinten, E. (2011) Enteritis and septicemia in a horse associated with infection by Escherichia fergusonii. J. Equine Vet. Sci., 31(7): 361-364. [Crossref]

33. Aklilu, E., Zunita, Z., Hassan, L. and Chen, H.C. (2010) Phenotypic and genotypic characterization of Methicillin-resistant Staphylococcus aureus (MRSA) isolated from dogs and cats at University Veterinary Hospital, Universiti Putra Malaysia. Trop. Biomed., 27(3): 483-492. [PubMed]

34. Kato, Y., Matsunaga, S., Misuna, Y., Ushioda, H. and Yamamoto, T. (1995) Isolation and characterization of Staphylococcus aureus in rats trapped at restaurants in buildings in downtown Tokyo. J. Vet. Med. Sci., 57(3): 499-502. [Crossref]

35. AL-Edany, O.S. (2015) Isolation and Identification of Zoonotic Bacteria from Wild Rats and Mice. MSc Thesis. College of Veterinary Medicine-University of Baghdad. Baghdad-Iraq.

36. Khalaf, S.K., Nagham, M.A., Abdulkarim, J.K. and Jenan, M.K. (2015) Isolation of Methicillin-resistant Staphylococcus aureus (MRSA) from Rattus rattus from Adhamiyah district in Baghdad governorate. MRVSA, 4(3): 9-23.

37. Bouchiat, C., Curtis, S., Spiliopoulou, I., Bes, M., Cocuzza, C., Codita, I., Dupieuxm, C., Giormezis, N., Kearns, A., Laurent, F., Molinos, S., Musumeci, R., Prat, C., Saadatian-Elahi, M., Tacconelli, E., Tristan, A., Schulte, B., Vandenesch, F. (2017) MRSA infections among patients in the emergency department: A European multicentre study. J. Antimicrob. Chemother., 72(2): 372-375. [Crossref] [PubMed]

38. Al Jalaf, M., Fadali, H., Alanee, R., Najjar, F., Al Deesi, Z., Seliem, R.M. and Nilles, E.J. (2018) Methicillin-resistant Staphylococcus aureus in emergency department patients in the United Arab Emirates. BMC Emerg. Med., 18(1): 12. [Crossref]

39. Elliott, S.P. (2007) Rat bite fever and Streptobacillus moniliformis. Clin. Microbiol. Rev., 20(1): 13-22. [Crossref] [PubMed] [PMC]

40. Meerburg, B.G., Singleton, G.R. and Kijlstra, A. (2009) Rodent-borne diseases and their risks for public health. Crit. Rev. Microbiol., 35(3): 221-270. [Crossref] [PubMed]

41. Verbist, L. (1993) Epidemiology and sensitivity of 8625 ICU and hematology/oncology bacterial isolates in Europe. International Study Group. Scand. J. Infect. Dis., 91(1): 14-24.

42. Agodi, A., Barchitta, M., Cipresso, R., Giaquinta, L., Romeo, M.A. and Denaro, C. (2007) Pseudomonas aeruginosa carriage, colonization, and infection in ICU patients. Intensive Care Med., 33(7): 1155-1161. [Crossref] [PubMed]

43. Kerr, K.G. and Snelling, A.M. (2009) Pseudomonas aeruginosa: A formidable and ever-present adversary. J. Hospital Infect., 73(1): e338-e344. [Crossref]

44. Lee, J.R., Bang, H., Dadhania, D., Hartono, C., Aull, M. J., Satlin, M. and Muthukumar, T. (2013) Independent risk factors for urinary tract infection and for subsequent bacteremia or acute cellular rejection: A single center report of 1166 kidney allograft recipients. Transplantation, 96(8): 10. [Crossref]

45. Badamchi, A., Masoumi, H., Javadinia, S., Asgarian, R. and Tabatabaee, A. (2017) Molecular detection of six virulence genes in Pseudomonas aeruginosa isolates detected in children with urinary tract infection. Microb. Pathog., 107(22): 44-47. [Crossref] [PubMed]

46. Breidenstein, E.B., de la Fuente-Nu-ez, C. and Hancock, R.E. (2011) Pseudomonas aeruginosa: All roads lead to resistance. Trends Microbiol., 19(8): 419-426. [Crossref] [PubMed]

47. Rybtke, M.T., Jensen, P.O., Hoiby, N., Givskov, M., Tolker-Nielsen, T. and Bjarnsholt, T. (2011) The implication of Pseudomonas aeruginosa biofilms in infections. Inflamm. Allergy Drug Targets, 10(2): 141-157. [Crossref]

48. Hsueh, P.R., Teng, L.J., Pan, H.J., Chen, Y.C., Sun, C.C., Ho, S.W. and Luh, K.T. (1998) Outbreak of Pseudomonas fluorescens bacteremia among oncology patients. J. Clin. Microbiol., 36(10): 2914-2917. [PubMed] [PMC]

49. Anaissie, E.J., Penzak, S.R. and Dignani, M.C. (2002) The hospital water supply as a source of nosocomial infections: A plea for action. Arch. Int. Med., 162(13): 1483-1492. [Crossref]

50. Connor, B.J., Kopecky, R.T., Frymoyer, P.A. and Forbes, B.A. (1987) Recurrent Pseudomonas luteola (CDC group Ve-1) peritonitis in a patient undergoing continuous ambulatory peritoneal dialysis. J. Clin. Microbiol., 25(6): 1113-1114. [PubMed] [PMC]

51. Chihab, W., Alaoui, A.S. and Amar, M. (2004) Chryseomonas luteola identified as the source of serious infections in a Moroccan university hospital. J. Clin. Microbiol., 42(4): 1837-1839. [Crossref] [PMC]

52. Casalta, J.P., Fournier, P.E., Habib, G., Riberi, A. and Raoult, D. (2005) Prosthetic valve endocarditis caused by Pseudomonas luteola. BMC Infect. Dis. X, 5(7): 82. [Crossref]

53. Su, S.Y., Chao, C.M. and Lai, C.C. (2014) Peritoneal dialysis peritonitis caused by Pseudomonas luteola. Perit. Dial. Int., 34(1): 138-139. [Crossref] [PubMed] [PMC]

54. Arnold, F., Sciortino, C. and Riede, K. (2004) New associations with Pseudomonas luteola bacteremia: A veteran with a history of tick bites and a trauma patient with pneumonia. Internet J. Infect. Dis., 4(2): 9005.

55. OIE. (2016) The 5th Global Animal Health Conference. Available from: http://www.healthforanimals.org/resources-and-events/resources/news/25-global-animal-health-conference-addresses-regulatory-barriers.html. Last accessed on 25-04-2018.

56. Saha, M., Debnath, C. and Pramanik, A.K. (2015) Listeria monocytogenes: An emerging foodborne pathogen. Int. J. Curr. Microbiol. App. Sci., 4(11): 52-72.

57. Farber, J.M. and Peterkin, P.I. (1991) Listeria monocytogenes, a food-borne pathogen. Microbiol. Rev., 55(3): 476-511. [PubMed] [PMC]

58. Yoshida, T., Tomoaki, S., Moritoshi, S. and Katsuya, H. (2000) Incidence of Listeria monocytogenes in wild animals in Japan. J. Vet. Med. Sci., 62(6): 673-675. [Crossref]

59. Ryu, C.-H., Igimi, S., Inoue, S. and Kumagai, S. (1992) The incidence of Listeria species in retail foods in Japan. Int. J. Food Microbiol., 16(2): 157-160. [Crossref]

60. Inoue, S., Tanikawa, T., Kawaguchi, J., Iida, T. and Morita, C. (1992) Prevalence of Listeria spp in wild rats captured in the Kanto area of Japan. J. Vet. Med. Sci., 54(3): 461-463. [Crossref]

61. Moore, C.G. and Schnurrenberger, P.R. (1981) A review of naturally occurring Brucella abortus infections in wild mammals. J. Am. Vet. Med. Assoc., 179(1): 1105-1112. [PubMed]

62. Zheludkov, M.M. and Tsirelson, L.E. (2010) Reservoirs of Brucella infection in nature. Biol. Bull., 37(7): 709-715. [Crossref]

63. Islam, M.A., Khatun, M.M. and Baek, B.K. (2012) Rats born to Brucella abortus-infected mothers become latent carriers of Brucella. J. Infect. Dev. Ctries., 6(3): 256-261. [Crossref]

64. Shuster, K.A., Hish, G.A., Selles, L.A., Chowdhury, M.A., Wiggins, R.C., Dysko, R.C. and Bergin, I.L. (2013) Naturally occurring disseminated Group B Streptococcus infections in postnatal rats. Comp. Med., 63(1): 55-61. [PubMed] [PMC]

65. Cohen-Poradosu, R. and Kasper, D.L. (2007) Group A streptococcus epidemiology and vaccine implications. Clin. Infect. Dis., 45(7): 863-865. [Crossref] [PubMed]

66. Ralph, A.P. and Carapetis, J.R. (2013) Group A streptococcal diseases and their global burden. Curr. Top. Microbiol. Immunol., 368(1): 1-27. [PubMed]

67. Parks, T., Barrett, L. and Jones, N. (2015) Invasive streptococcal disease: A review for clinicians. Br. Med. Bull., 115(1): 77-89. [Crossref] [PubMed]

68. Hamada, S. and Slade, H.D. (1980) Biology, immunology, and cariogenicity of Streptococcus mutans. Microbiol. Rev., 44(2): 331-384. [PubMed] [PMC]

69. Drucker, D.B. and Melville, T.H. (1971) The classification of some oral streptococci of human or rat origin. Arch. Oral. Biol., 16(8): 845-853. [Crossref]

70. Zhu, H., Willcox, M.D.P. and Knox, K.W. (2000) A new species of oral Streptococcus isolated from Sprague-Dawley rats, Streptococcus orisratti Sp. Nov. Int. J. Syst. Evol. Microbiol., 50(1): 55-61. [Crossref] [PubMed]

71. Schaffer, J.N. and Pearson, MM. (2015) Proteus mirabilis and urinary tract infections. Microbiol. Spectr., 3(5): 1-66. [Crossref]

72. Guentzel, M.N. (1996) Escherichia, Klebsiella, Enterobacter, Serratia, Citrobacter and Proteus. In: Baron S, editor. Medical Microbiology. 4th edition. University of Texas Medical Branch, Galveston (TX). [PubMed]

73. Flores-Mireles, A.L., Walker, J.N., Caparon, M. and Hultgren, S.J. (2015) Urinary tract infections: Epidemiology, mechanisms of infection and treatment options. Nat. Rev. Microbiol., 13(5): 269-284. [Crossref] [PubMed] [PMC]

74. Badger, J.L., Stins, M.F. and Kim, K.S. (1999) Citrobacter freundii invades and replicates in human brain microvascular endothelial cells. Infect. Immun., 67(8): 4208-4215. [PubMed] [PMC]

75. Coonrod, J.D. (1981) Pulmonary opsonins in Klebsiella pneumoniae Pneumonia in Rats. Infect. Immun., 33(2): 533-539. [PubMed] [PMC]

76. Sleger, T., Gangl, E., Pop-Damkov, P., Krause, K.M., Laud, P.J., Slee, A.M. and Nichols, W.W. (2018) Efficacy of ceftazidime-avibactam in a rat intra-abdominal abscess model against ceftazidime- and meropenem-resistant isolate of Klebsiella pneumoniae carrying blaKPC-2. J. Chemother., 30(2): 95-100. [Crossref] [PubMed]

77. Darby, A., Lertpiriyapong, K., Sarkar, U., Seneviratne, U.I. and Fox, J.G. (2014) Cytotoxic and pathogenic properties of Klebsiella oxytoca isolated from laboratory animals. PLoS One, 9(7): e100542. [Crossref]

78. Bleich, A., Kirsch, H.P., Sahly, H., Fahey, J., Smoczek, A., Hedrich, H. J. and Sundberg, J.P. (2008) Klebsiella oxytoca: Opportunistic infections in laboratory rodents. Lab. Anim., 42(3): 369-375. [Crossref] [PubMed]

79. Berendt, R.F., Long, G.G., Abeles, F.B., Canonico, P.G., Elwell, M.R. and Powanda, M.C. (1977) Pathogenesis of respiratory Klebsiella pneumoniae infection in rats: Bacteriological and histological findings and metabolic alterations. Infect. Immun., 15(2): 586-593. [PubMed] [PMC]

80. Dong, F., Wang, B., Zhang, L., Tang, H., Li, J. and Wang, Y. (2012) Metabolic response to Klebsiella pneumoniae infection in an experimental rat model. PLoS One, 7(11): e51060. [Crossref]

81. Shatzkes, K., Singleton, E., Tang, C., Zuena, M., Shukla, S., Gupta, S., Dharani, S., Onyile, O., Rinaggio, J., Connell, N.D. and Kadouri, D.E. (2016) Predatory bacteria attenuate Klebsiella pneumoniae burden in rat lungs. MBio, 7(6): e01816-e01847. [Crossref]

82. Schaufler, K., Nowak, K., Dux, A., Semmler, T., Villa, L., Kourouma, L., Bangoura, K., Wieler, L.H., Leendertz, F.H. and Guenther, S. (2018) Clinically relevant ESBL-producing K. pneumoniae ST307 and E. coli ST38 in an Urban West African rat population. Front Microbiol., 9: 150. [Crossref] [PubMed] [PMC]

83. Sanders, W. and Sanders, C.C. (1997) Enterobacter Spp.: Pathogens poised to flourish at the turn of the century. Clin. Microbiol. Rev., 10(2): 220-241. [Crossref] [PubMed] [PMC]

84. Khan, F.A. (2004) Meningitis due to Enterobacter aerogenes subsequent to resection of an acoustic neuroma and abdominal fat graft to the mastoid. Braz. J. Infect. Dis., 8(5): 386-388. [Crossref]

85. Chauhan, S., Noor, J., Yegneswaran, B. and Kodali, H. (2016) Enterobacter meningitis and challenges in treatment. J. Clin. Diag. Res., 10(12): 10-11. [Crossref]

86. Hunter, C.J., Singamsetty, V.K., Chokshi, N.K., Boyle, P., Camerini, V., Grishin, A.V., Upperman, J.S. and Prasadarao, N.V. (2008) Enterobacter sakazakii enhances epithelial cell injury by inducing apoptosis in a rat model of necrotizing enterocolitis. J. Infect. Dis., 198(4): 586-593. [Crossref] [PubMed] [PMC]

87. Mahmood, M.S., Sarwari, A.R., Khan, M.A., Sophie, Z., Khan, E. and Sami, S. (2000) Infective endocarditis and septic embolization with Ochrobactrum anthropi: Case report and review of literature. J. Infect., 40(3): 287-290. [Crossref]

88. Stiakaki, E., Galanakis, E., Samonis, G., Christidou, A., Maraka, S., Tselentis, Y. and Kalmanti, M. (2002) Ochrobactrum anthropi bacteremia in pediatric oncology patients. Pediatr. Infect. Dis. J., 21(2): 72-74. [Crossref]

89. Falagas, M.E., Kavvadia, P.K., Mantadakis, E., Kofteridis, D.P., Bliziotis, I.A., Saloustros, E., Maraki, S. and Samonis, G. (2006) Morganella morganii infections in a general tertiary hospital. Infection, 34(6): 315-321. [Crossref] [PubMed]

90. Nadjar, D., Labia, R., Cerceau, C., Bizet, C., Philippon, A. and Arlet, G. (2001) Molecular characterization of chromosomal class C beta-lactamase and its regulatory gene in Ochrobactrum anthropi. Antimicrob. Agents Chemother., 45(8): 2324-2330. [Crossref] [PubMed] [PMC]

91. Stratev, D. and Odeyemi, O.A. (2016) Antimicrobial resistance of Aeromonas hydrophila isolated from different food sources: A mini-review. J. Infect. Public Health, 9(2): 535-544. [Crossref] [PubMed]

92. Janda, J.M. and Abbott, S.L. (1998) Evolving concepts regarding the genus Aeromonas: An expanding Panorama of species, disease presentations, and unanswered questions. Clin. Infect. Dis., 27(2): 332-344. [Crossref]

93. Lee, I.K. and Liu, J.W. (2006) Clinical characteristics and risk factors for mortality in Morganella morganii bacteremia. J. Microbial. Immunol. Infect., 39(4): 328-334. [PubMed]

94. Custovic, A. and Hadzic, S. (2008) Epidemiology of bacterial intrahospital infections in newborns. Med. Arh., 62(5-6): 294-297. [PubMed]

95. Lin, T.Y., Chan, M.C., Yang, Y.S., Lee, Y., Yeh, K.M., Lin, J.C. and Chang, F.Y. (2015) Clinical manifestations and prognostic factors of Morganella morganii bacteremia. Eur. J. Clin. Microbiol. Infect. Dis., 34(2): 231-236. [Crossref] [PubMed]

96. Plummer, J.L., Ossowicz, C.J., Ilsley, A.H. and De La M Hall, P. (2000) Influence of intestinal flora on the development of fibrosis and cirrhosis in a rat model. J. Gastroenterol. Hepatol., 15(11): 1307-1311.

97. Muller, H.E. (1986) Occurrence and pathogenic role of Morganella-proteus-providentia group bacteria in human feces. J. Clin. Microbiol., 23(2): 404-405. [PubMed] [PMC]

98. Moyer, N.P. (1987) Clinical significance of Aeromonas species isolated from patients with diarrhea. J. Clin. Microbiol., 25(11): 2044-2048. [PubMed] [PMC]

99. El-Feki, M., Awad, E.M., Amin, H.M. and Mahmoud, A.M. (2001) Immunological evaluation of Aeromonas infection in albino rat. Egypt. J. Biol., 3(2): 96-101.

100. Munir, M.B., Hashim, R., MohdNor, S.A. and Marsh, T.L. (2018) Effect of dietary prebiotics and probiotics on snakehead (Channa striata) health: Haematology and disease resistance parameters against Aeromonas hydrophila. Fish. Shellfish. Immunol., 75(3): 99-108. [Crossref] [PubMed]

101. Moreillon, P., Overholser, C.D., Malinverni, R., Bille, J. and Glauser, M.P. (1998) Predictors of endocarditis in isolates from cultures of blood following dental extractions in rats with periodontal disease. J. Infect. Dis., 157(5): 990-995. [Crossref]

102. Jemilehin, F.O., Ogunleye, A.O., Okunlade, A.O. and Ajuwape, A.T.P. (2016) Isolation of Salmonella species and some other gram negative bacteria from rats cohabitating with poultry in Ibadan, Oyo State, Nigeria. Afr. J. Microbiol. Res., 10(29): 1104-1110. [Crossref]