Antimicrobial susceptibility and serovars of Salmonella from chickens and humans in Ibadan, Nigeria

Journal of Infection in Developing Countries

Volumn 4, Issue 8, 2010, Pages 484-494

  Fashae, Kayode ^a   Ogunsola, Folasade ^c   Aarestrup, Frank M ^b   Hendriksen, Rene S ^b  

^a UNIVERSITY OF IBADAN   (Nigeria)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c UNIVERSITY OF LAGOS   (Nigeria)

Author keywords

Antimicrobial resistance; Bacteriaemia; Chicken; Human; Nigeria; Plasmid mediated quinoline resistance; Salmonella

Indexed keywords

AMOXICILLIN PLUS CLAVULANIC ACID; AMPICILLIN; APRAMYCIN; CEFOTAXIME; CEFTIOFUR; CHLORAMPHENICOL; CIPROFLOXACIN; FLORFENICOL; GENTAMICIN; NALIDIXIC ACID; NEOMYCIN; SPECTINOMYCIN; STREPTOMYCIN; SULFAMETHOXAZOLE; TETRACYCLINE; TRIMETHOPRIM;

ANIMAL EXPERIMENT; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENE; BACTERIUM ISOLATE; BLOOD SAMPLING; FECES ANALYSIS; FEMALE; HOST RANGE; HUMAN; MAJOR CLINICAL STUDY; MALE; NIGERIA; NONHUMAN; PHENOTYPE; POULTRY FARMING; PREVALENCE; QNR BACTERIAL GENE; SALMONELLA; SALMONELLA APAPA; SALMONELLA DUBLIN; SALMONELLA ENTERITIDIS; SALMONELLA JUKESTOWN; SALMONELLA MOUSCHAUI; SALMONELLA ONIREKE; SALMONELLA ORITAMERIN; SALMONELLA TYPHI; SALMONELLA TYPHIMURIUM; SALMONELLA VIRCHOW; SALMONELLOSIS; SEROTYPE;

GALLUS GALLUS; SALMONELLA; SALMONELLA ENTERITIDIS; SALMONELLA TYPHI; SALMONELLA TYPHIMURIUM;

EID: 78649262376     PISSN: 20366590     EISSN: 19722680     Source Type: Journal    
DOI: 10.3855/jidc.909     Document Type: Article

References (70)

1. Grimont PAD, Weill FX (2007) Antigenic formulae of the Salmonella serovars, 9th edition. Paris: WHO Collaborating Center for Reference and Research on Salmonella at Institut Pasteur in France 150 p.
2. Uzzau S, Brown DJ, Wallis T, Rubino S, Leori G, Bernard S, Casadesus J, Platt DJ, Olsen JE (2000) Host adapted serotypes of Salmonella enterica. Epidemiol Infect 125: 229-255.
3. Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS, Shapiro C, Griffin PM, Tauxe RV (1999) Food-related illness and death in the United States. Emerg Infect Dis 5: 607-625.
4. Adak GK, Long SM, O'Brien SJ (2002) Trends in indigenous foodborne disease and deaths, England and Wales: 1992 to 2000. Gut 51: 832-841.
5. Hald T, Lo Fo Wong DM, Aarestrup FM (2007) The attribution of human infections with antimicrobial resistant Salmonella bacteria in Denmark to sources of animal origin. Foodborne Pathog Dis 4: 313-326.
6. Braden CR (2006) Salmonella enterica serotype Enteritidis and eggs: a national epidemic in the United States. Clin Infect Dis 43: 512-517.
7. Hohmann EL (2001) Nontyphoidal salmonellosis. Clin Infect Dis 32: 263-269.
8. Jones TF, Ingram LA, Cieslak PR, Vugia DJ, Tobin-D'Angelo M, Hurd S, Medus C, Cronquist A, Angulo FJ (2008) Salmonellosis outcomes differ substantially by serotype. J Infect Dis 198: 109-114.
9. Morpeth SC, Ramadhani HO, Crump JA (2009) Invasive non-Typhi Salmonella disease in Africa. Clin Infect Dis 49: 606-611.
10. Hendriksen RS, Bangtrakulnonth A, Pulsrikarn C, Pornruangwong S, Noppornphan G, Emborg HD, Aarestrup FM (2009) Risk factors and epidemiology of the ten most common Salmonella serovars from patients in Thailand: 2002-2007. Foodborne Pathog Dis 6: 1009-1019.
11. Gordon MA (2008) Salmonella infections in immunocompromised adults. J Infect 56: 413-422.
12. Vandenberg O, Nyarukweba DZ, Ndeba PM, Hendriksen RS, Barzilay EJ, Schirvel C, Bisimwa BB, Collard JM, Aidara KA, Aarestrup FM (2010) Microbiologic and Clinical Features of Salmonella Species Isolated From Bacteremic Children in Eastern Democratic Republic of Congo. Pediatr Infect Dis J. 29: 504-10.
13. Kingsley RA, Msefula CL, Thomson NR, Kariuki S, Holt KE, Gordon MA, Harris D, Clarke L, Whitehead S, Sangal V, Marsh K, Achtman M, Molyneux ME, Cormican M, Parkhill J, Maclennan CA, Heyderman RS, Dougan G (2009) Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome Res 19: 2279-2287.
14. Sire JM, Garin B, Macondo EA (2008) Low-level resistance to ciprofloxacin in non-Typhi Salmonella enterica isolated from human gastroenteritis in Dakar, Senegal (2004--2006). Int J Antimicrob Agents 31: 581-582.
15. Gordon MA, Graham SM, Walsh AL, Wilson L, Phiri A, Molyneux E, Zijlstra EE, Heyderman RS, Hart CA, Molyneux ME (2008) Epidemics of invasive Salmonella enterica serovar Enteritidis and S. enterica serovar Typhimurium infection associated with multidrug resistance among adults and children in Malawi. Clin Infect Dis 46: 963-969.
16. Usha G, Chunderika M, Prashini M, Willem SA, Yusuf ES (2008) Characterization of extended-spectrum beta-lactamases in Salmonella spp. at a tertiary hospital in Durban, South Africa. Diagn Microbiol Infect Dis 62: 86-91.
17. Alausa KO, Montefiore D, Sogbetun AO, Ashiru JO, Onile BA, Sobayo E (1977) Septicaemia in the tropics. A prospective epidemiological study of 146 patients with a high case fatality rate. Scand J Infect Dis 9: 181-185.
18. Hendriksen RS, Mikoleit M, Carlson VP, Karlsmose S, Vieira AR, Jensen AB, Seyfarth AM, DeLong SM, Weill FX, Wong DM, Angulo FJ, Wegener HC, Aarestrup FM (2009) WHO Global Salm-Surv external quality assurance system for serotyping of Salmonella isolates from 2000 to 2007. J Clin Microbiol 47: 2729-2736.
19. Ameh JA, Kwari HD, Abubakar YM (2001) Prevalence and antibiotic susceptibility of Salmonella Enteritidis in chicken meat sold in Maiduguri. Nigeria Res J Sci 33-37.
20. Raufu I, Hendriksen RS, Ameh JA, Aarestrup FM (2009) Occurrence and characterization of Salmonella Hiduddify from chickens and poultry meat in Nigeria. Foodborne Pathog Dis 6: 425-430.
21. McDermott PF (2006) Antimicrobial Resistance in notyphoidal Salmonellae. In: Antimicrobial Resistance in Bacteria of Animal Origin. Aaretrup FM Editor, Washington DC: ASM Press. 293-314.
22. Collignon P, Powers JH, Chiller TM, Aidara-Kane A, Aarestrup FM (2009) World Health Organization ranking of antimicrobials according to their importance in human medicine: A critical step for developing risk management strategies for the use of antimicrobials in food production animals. Clin Infect Dis 49: 132-141.
23. Hendriksen RS, Mikoleit M, Kornschober C, Rickert RL, Duyne SV, Kjelso C, Hasman H, Cormican M, Mevius D, Threlfall J, Angulo FJ, Aarestrup FM (2009) Emergence of Multidrug-Resistant Salmonella Concord Infections in Europe and the United States in Children Adopted From Ethiopia, 2003-2007. Pediatr Infect Dis J 28: 814-818.
24. Hoa NT, Diep TS, Wain J, Parry CM, Hien TT, Smith MD, Walsh AL, White NJ (1998) Community-acquired septicaemia in southern Viet Nam: the importance of multidrug-resistant Salmonella Typhi. Trans R Soc Trop Med Hyg 92: 503-508.
25. Cowan ST, Steel KJ (1974) Manual for the Identification of Medical Bacteria. Cambridge. University Press: 28-106.
26. Cruickshank R, Duguid JP, Marmion BP, Swainr HA (1975) The Practice of Medical Microbiology. Edinburgh. Churchill Livingstone: 171-191.
27. Hendriksen RS, Bangtrakulnonth A, Pulsrikarn C, Pornreongwong S, Hasman H, Song SW, Aarestrup FM (2008) Antimicrobial resistance and molecular epidemiology of Salmonella Rissen from animals, food products, and patients in Thailand and Denmark. Foodborne Pathog Dis 5: 605-619.
28. Cavaco LM, Hasman H, Xia S, Aarestrup FM (2009) qnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serovar Kentucky and Bovismorbificans strains of human origin. Antimicrob Agents Chemother 53: 603-608.
29. Wang M, Guo Q, Xu X, Wang X, Ye X, Wu S, Hooper DC, Wang M (2009) New plasmid-mediated quinolone resistance gene, qnrC, found in a clinical isolate of Proteus mirabilis. Antimicrob Agents Chemother 53: 1892-1897.
30. Ghiorghis B, Geyid A, Haile M (1992) Bacteraemia in febrile out-patient children. East Afr Med J 69: 74-77.
31. Brent AJ, Oundo JO, Mwangi I, Ochola L, Lowe B, Berkley JA (2006) Salmonella bacteremia in Kenyan children. Pediatr Infect Dis J 25: 230-236.
32. Sigauque B, Roca A, Mandomando I, Morais L, Quinto L, Sacarlal J, Macete E, Nhamposa T, Machevo S, Aide P, Bassat Q, Bardaji A, Nhalungo D, Soriano-Gabarro M, Flannery B, Menendez C, Levine MM, Alonso PL (2009) Community-acquired bacteremia among children admitted to a rural hospital in Mozambique. Pediatr Infect Dis J 28: 108-113.
33. Bahwere P, Levy J, Hennart P, Donnen P, Lomoyo W, Dramaix-Wilmet M, Butzler JP, De MP (2001) Community-acquired bacteremia among hospitalized children in rural central Africa. Int J Infect Dis 5: 180-188.
34. Walsh AL, Phiri AJ, Graham SM, Molyneux EM, Molyneux ME (2000) Bacteremia in febrile Malawian children: clinical and microbiologic features. Pediatr Infect Dis J 19: 312-318.
35. Galanis E, Lo Fo Wong DM, Patrick ME, Binsztein N, Cieslik A, Chalermchikit T, Aidara-Kane A, Ellis A, Angulo FJ, Wegener HC (2006) Web-based surveillance and global Salmonella distribution, 2000-2002. Emerg Infect Dis 12: 381-388.
36. Brent AJ, Oundo JO, Mwangi I, Ochola L, Lowe B, Berkley JA (2006) Salmonella bacteremia in Kenyan children. Pediatr Infect Dis J 25: 230-236.
37. Graham SM, Molyneux EM, Walsh AL, Cheesbrough JS, Molyneux ME, Hart CA (2000) Nontyphoidal Salmonella infections of children in tropical Africa. Pediatr Infect Dis J 19: 1189-1196.
38. Kariuki S, Revathi G, Kariuki N, Kiiru J, Mwituria J, Muyodi J, Githinji JW, Kagendo D, Munyalo A, Hart CA (2006) Invasive multidrug-resistant non-typhoidal Salmonella infections in Africa: zoonotic or anthroponotic transmission? J Med Microbiol 55: 585-591.
39. Ojeniyi AA, Montefiore DG (1986) Food poisoning outbreak in Ibadan, Nigeria, due to a new phage type of Salmonella Typhimurium. Scand J Infect Dis 18: 551-552.
40. Oboegbulam SI, Oguike JU, Gugnani HC (1995) Microbiological studies on cases diagnosed as typhoid/enteric fever in south-east Nigeria. J Commun Dis 27: 97-100.
41. Orji MU, Onuigbo HC, Mbata TI (2005) Isolation of Salmonella from poultry droppings and other environmental sources in Awka, Nigeria. Int J Infect Dis 9: 86-89.
42. Ricosse JH, Saliou P, Albert JP, Menard M, Le MG, Schollhammer G, Trotobas J, Morvan D, Meyran M (1979) Current aspects of human salmonellosis in Upper Volta. Study carried out at Centre Muraz (Bobo-Dioulasso) from 1966 to 1977: isolation of 1,013 Salmonella strains. Med Trop Mars 39: 381-394.
43. Maguire H, Cowden J, Jacob M, Rowe B, Roberts D, Bruce J, Mitchell E (1992) An outbreak of Salmonella Dublin infection in England and Wales associated with a soft unpasteurized cows' milk cheese. Epidemiol Infect 109: 389-396.
44. Allerberger F, Liesegang A, Grif K, Prager R, Danzl J, Hock F, Ottl J, Dierich MP, Berghold C, Neckstaller I, Tschape H, Fisher I (2002) Occurrence of Salmonella enterica serovar Dublin in Austria. Euro Surveill 7: 65-70.
45. Vaillant V, Haeghebaert S, Desenclos JC, Bouvet P, Grimont F, Grimont PA, Burnens AP (1996) Outbreak of Salmonella Dublin infection in France, November-December 1995. Euro Surveill 1: 9-10.
46. Anonymous (2009) The Community summary report on trends and sources of zoonotic agents in the European Union in 2007. The EFSA Journal 2009, Parma, Italy.
47. Collard P, Sen R (1956) Isolation of Salmonellae from cattle in Ibadan. West Afr Med J 5: 118-120.
48. Collard P, Sen R (1962) Salmonellosis at Ibadan, Nigeria. (5. Strains isolated during 1956-1960). West Afr Med J 11: 106-112.
49. Cooke FJ, De PE, Maguire C, Guha S, Pickard DJ, Farrington M, Threlfall EJ (2009) First report of human infection with Salmonella enterica serovar Apapa resulting from exposure to a pet lizard. J Clin Microbiol 47: 2672-2674.
50. Bertrand S, Rimhanen-Finne R, Weill FX, Rabsch W, Thornton L, Perevoscikovs J, van PW, Heck M (2008) Salmonella infections associated with reptiles: the current situation in Europe. Euro Surveill 13: 1-6.
51. Milstone AM, Agwu AG, Angulo FJ (2006) Alerting pregnant women to the risk of reptile-associated salmonellosis. Obstet Gynecol 107: 516-518.
52. Carlquist PR, Coates MS (1947) Salmonella Monschaui-A New Type. J Bacteriol 53: 249.
53. Collard P, Sen R (1960) Serotypes of Salmonella at Ibadan, Nigeria, with special note of the new serotypes isolated in Nigeria. J Infect Dis 106: 270-275.
54. Sharma VK, Rohde R, Garg DN, Kumar A (1977) Toads as natural reservoir of Salmonella. Zentralbl Bakteriol Orig A 239: 172-177.
55. Pedersen K, Lassen-Nielsen AM, Nordentoft S, Hammer AS (2009) Serovars of Salmonella from captive reptiles. Zoonoses Public Health 56: 238-242.
56. Mermin J, Hutwagner L, Vugia D, Shallow S, Daily P, Bender J, Koehler J, Marcus R, Angulo FJ (2004) Reptiles, amphibians, and human Salmonella infection: a population-based, case-control study. Clin Infect Dis 38: 253-261.
57. Bradley T, Angulo F, Mitchell M (2001) Public health education on Salmonella spp and reptiles. J Am Vet Med Assoc 219: 754-755.
58. Oboegbulem SI, Iseghohimhen AU (1985) Wall Geckos (Geckonidae) as reservoirs of Salmonellae in Nigeria: problems for epidemiology and public health. Int J Zoonoses 12: 228-232.
59. Mascher F, Reinthaler FF, Sixl W (1988) Serotyping of Salmonella strains in south-west Nigeria: epidemiological aspects. Geogr Med 18: 171-174.
60. Parry CM, Threlfall EJ (2008) Antimicrobial resistance in typhoidal and nontyphoidal salmonellae. Curr Opin Infect Dis 21: 531-538.
61. Elgroud R, Zerdoumi F, Benazzouz M, Bouzitouna-Bentchouala C, Granier SA, Fremy S, Brisabois A, Dufour B, Millemann Y (2009) Characteristics of Salmonella contamination of broilers and slaughterhouses in the region of Constantine (Algeria). Zoonoses Public Health 56: 84-93.
62. Anonymous (2009) Annual report on zoonoses in Denmark 2007. National Food Institute, Technical University of Denmark, Copenhagen, Denmark.
63. Bertrand S, Weill FX, Cloeckaert A, Vrints M, Mairiaux E, Praud K, Dierick K, Wildemauve C, Godard C, Butaye P, Imberechts H, Grimont PA, Collard JM (2006) Clonal emergence of extended-spectrum beta-lactamase (CTX-M-2)-producing Salmonella enterica serovar Virchow isolates with reduced susceptibilities to ciprofloxacin among poultry and humans in Belgium and France (2000 to 2003). J Clin Microbiol 44: 2897-2903.
64. Weinberger M, Solnik-Isaac H, Shachar D, Reisfeld A, Valinsky L, Andorn N, Agmon V, Yishai R, Bassal R, Fraser A, Yaron S, Cohen D (2006) Salmonella enterica serotype Virchow: epidemiology, resistance patterns and molecular characterisation of an invasive Salmonella serotype in Israel. Clin Microbiol Infect 12: 999-1005.
65. Weill FX, Lailler R, Praud K, Kerouanton A, Fabre L, Brisabois A, Grimont PA, Cloeckaert A (2004) Emergence of extended-spectrum-beta-lactamase (CTX-M-9)-producing multiresistant strains of Salmonella enterica serotype Virchow in poultry and humans in France. J Clin Microbiol 42: 5767-5773.
66. Ammari S, Laglaoui A, En-Nanei L, Bertrand S, Wildemauwe C, Barrijal S, Abid M (2009) Isolation, drug resistance and molecular characterization of Salmonella isolates in northern Morocco. J Infect Dev Ctries 3: 41-49.
67. Tibaijuka B, Molla B, Hildebrandt G, Kleer J (2003) Occurrence of Salmonellae in retail raw chicken products in Ethiopia. Berl Munch Tierarztl Wochenschr 116: 55-58.
68. Adetosoye AI (1980) Infective drug resistance among Escherichia coli isolated from clinically healthy domestic livestock. Vet Microbiol 333-342.
69. Lee HY, Su LH, Tsai MH, Kim SW, Chang HH, Jung SI, Park KH, Perera J, Carlos C, Tan BH, Kumarasinghe G, So T, Chongthaleong A, Hsueh PR, Liu JW, Song JH, Chiu CH (2009) High rate of reduced susceptibility to ciprofloxacin and ceftriaxone among nontyphoid Salmonella clinical isolates in Asia. Antimicrob Agents Chemother 53: 2696-2699.
70. Garcia-Fernandez A, Fortini D, Veldman K, Mevius D, Carattoli A (2009) Characterization of plasmids harbouring qnrS1, qnrB2 and qnrB19 genes in Salmonella. J Antimicrob Chemother 63: 274-281.