The antibiotic resistance study of Enterobacteriaceae, Yersiniaceae and Morganellaceae bacteria isolated from broilers (outside veterinary control) in western Algeria
Keywords:
Antibiogram, Antibiotic resistance, Enterobacteriaceae, Yersiniaceae, Morganellaceae
Abstract
In the context of our study of the animal side, especially in broiler chickens, the breeding of the latter requires the use of antibiotics for treatment and prophylaxis purpose; to give a closer look at the antibiotic resistance status of broiler chickens in Western Algeria. The bacteria Enterobacter, Escherichia coli, Proteus, Salmonella, Serratia were present and showed a high multidrug-resistance at a percentage of 67.14%, 63.64%, 60%, 57.27%, 50% respectively. The forty-nine bacteria identified belong to different families of Enterobacteriaceae, Yersiniaceae and Morganellaceae have shown an overall resistance of 61.22%. Presented resistance to cefazolin 91.84%, flumequine 89.80%, neomycin 83.67%, ceftiofur 79.59%, ampicillin 73.47%, trimethoprim 73.47%, aztreonam 57.14%, colistin 48.98 %, nadilixic acid 32.65%, streptomycin 30.61%, gentamicin 12.24%. To study the sensitivity, critical values to antibiotics a statistical Student's t-test was used. All bacteria were significantly resistant (P ≤ 0.05) to the following antibiotics: flumequine, neomycin, cefazolin, trimethoprim, ampicillin, and ceftiofur. However, a low sensitivity was also noted to gentamicin, nalidixic acid, streptomycin (P ≤ 0.05). Some isolated bacteria were resistant to many antibiotics, with resistance from 3 to 10 antibiotics simultaneously. The highest percentage of all bacteria (28.57%) were resistant to 8 antibiotics, while the lowest percentage of all bacteria (2.04%) were resistant to 3 and 10 antibiotics.
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References
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34. Dandachi I, Sokhn ES, Dahdouh EA, Azar E, El-Bazzal B, Rolain J-M, Daoud Z. Prevalence and characterization of multi-drug-resistant Gram-negative bacilli isolated from Lebanese poultry: A nationwide study. Frontiers Microbiol. 2018; 9: 550.
35. Nandi SP, Sultana M, Hossain MA. Prevalence and characterization of multidrug-resistant zoonotic Enterobacter spp. in poultry of Bangladesh. Foodborne Pathog Dis. 2013; 10(5): 420-427.
36. Arhin RE, Hackman HK, Sa-eed A. Antibiotic prophylaxis and cloacal carriage of resistant zoonotic bacteria in commercially-bred poultry. Eur J Animal Health. 2019; 1(1): 1-13.
37. Ezekiel C, Olarinmoye A, Jnr JO, Olaoye O, Edun A. Distribution, antibiogram and multidrug resistance in Enterobacteriaceae from commercial poultry feeds in Nigeria. Afr J Microbiol Res. 2011; 5(3): 294-301.
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40. Lenchenko E, Blumenkrants D, Vatnikov Y, Kulikov E, Khai V, Sachivkina N, et al. Poultry Salmonella sensitivity to antibiotics. Syst Rev Pharmacy. 2020; 11(2): 170-175.
41. Sepehri G, Akbarpour P, Nekoobin M. Microbial resistance of broiler poultry samples to the commonly used antibiotics in Kerman. Int J Vet Res. 2008.
42. Wajid M, Awan AB, Saleemi MK, Weinreich J, Schierack P, Sarwar Y, Ali A. Multiple drug resistance and virulence profiling of Salmonella enterica serovars Typhimurium and Enteritidis from poultry farms of Faisalabad, Pakistan. Microb Drug Resist. 2019; 25(1): 133-142.
43. Begum K, Mannan SJ, Ahmed A. Antibiotic resistance, plasmids and integron profile of Salmonella species isolated from poultry farm and patients. Dhaka Univ J Pharmac Sci. 2016; 15(2): 209-214.
44. Djeffal S, Bakour S, Mamache B, Elgroud R, Agabou A, Chabou S, Hireche S, Bouaziz O, Rahal K, Rolain J-M. Prevalence and clonal relationship of ESBL-producing Salmonella strains from humans and poultry in northeastern Algeria. BMC Vet Res. 2017; 13(1): 132.
45. Suresh Y, Kiranmayi CB, Rao TS, Srivani M, Subhashini N, Chaitanya G, et al. Multidrug resistance and ESBL profile of Salmonella serovars isolated from poultry birds and foods of animal origin. 2019.
46. Nahar A, Siddiquee M, Nahar S, Anwar KS, Islam S. Multidrug resistant-proteus mirabilis isolated from chicken droppings in commercial poultry farms: Bio-security concern and emerging public health threat in Bangladesh. J Biosaf Health Educ. 2014.
47. Nemati M. Antimicrobial resistance of Proteus isolates from poultry. Eur J Exp Biol. 2013; 3(6): 499-500.
48. Shawish RR, El-Bagory A-RM, Elnahriry SS, Wafy HA, Sayed HH. Incidence of antibiotic resistant coliforms in poultry meat in Menoufia Governorate, Egypt. PSM Microbiol. 2020; 5(1): 7-13.
49. Adelowo OO, Ojo FA, Fagade OE. Prevalence of multiple antibiotic resistance among bacterial isolates from selected poultry waste dumps in Southwestern Nigeria. World J Microbiol Biotechnol. 2009; 25(4): 713-719.
50. Sala C, Morar A, Colibar O, Morvay AA. Antibiotic resistance of gram negative bacteria isolated from meat surface biofilm. Rom Biotech Lett. 2012; 17(4): 7483-92.
51. Kilonzo-Nthenge A, Rotich E, Nahashon S. Evaluation of drug-resistant Enterobacteriaceae in retail poultry and beef. Poultry Sci. 2013; 92(4): 1098-1107.
52. Faife SL, Zimba T, Sekyere JO, Govinden U, Chenia HY, Simonsen GS, Sundsfjord A, Essack SY. β-lactam and fluoroquinolone resistance in Enterobacteriaceae from imported and locally-produced chicken in Mozambique. J Infect Develop Countries. 2020; 14(05): 471-478.
53. Okorafor ON, Anyanwu MU, Nwafor EO, Anosa GN, Udegbunam RI. Multidrug-resistant enterobacteria colonize commercial day-old broiler chicks in Nigeria. Vet World. 2019; 12(3): 418-423.
54. Yulistiani R, Praseptiangga D, Raharjo D, Shirakawa T. Prevalence of antibiotic-resistance enterobacteriaceae strains isolated from chicken meat at traditional markets in Surabaya, Indonesia. MSE. 2017; 193(1): 012007.
55. Lei C-W, Zhang A-Y, Liu B-H, Wang H-N, Guan Z-B, Xu C-W, et al. Molecular characteristics of Salmonella genomic island 1 in Proteus mirabilis isolates from poultry farms in China. Antimicrob Agents Chemother. 2014; 58(12): 7570-7572.
56. Pan Y-s, Yuan L, Liu J-h, Hu G-z, Mo J. Isolation, Identification and Antimicrobial Susceptibility of Escherichia coli and Proteus mirabilis Isolated from Chicken [J]. Acta Agricult Jiangxi. 2009; 12.
57. Zhang L, Fu Y, Xiong Z, Ma Y, Wei Y, Qu X, et al. Highly prevalent multidrug-resistant Salmonella from chicken and pork meat at retail markets in Guangdong, China. Frontiers Microbiol. 2018; 9: 2104.
58. Ziech RE, Lampugnani C, Perin AP, Sereno MJ, Sfaciotte RAP, Viana C, et al. Multidrug resistance and ESBL-producing Salmonella spp. isolated from broiler processing plants. Braz J Microbiol. 2016; 47(1): 191-195.
59. Ojo OE, Ogunyinka OG, Agbaje M, Okuboye JO, Kehinde OO, Oyekunle MA. Antibiogram of Enterobacteriaceae isolated from free-range chickens in Abeokuta, Nigeria. Vet Arhiv. 2012; 82(6): 577-589.
2. Hammoudi A, Mouats A, Halbouche M. Sérotypes, antibiorésistance et identification de gènes de virulence des Escherichia coli pathogènes dans les élevages avicoles en Algérie. Actes des 1ères JE-RGAL, Mostaganem,23-24 Juin 2009. 2009.
3. Castanon J. History of the use of antibiotic as growth promoters in European poultry feeds. Poultry Sci. 2007; 86(11): 2466-2471.
4. Elhani D. L’émergence de la résistance aux antibiotiques annonce-t-elle le retour des âges sombres? Ann Biol Clinique. 2011; 69(6): 637-646.
5. Chaslus-Dancla E, Guillot JF, Lafont JP. Evolution de l'antibiorésistance bactérienne dans des élevages avicoles. Ann Recherches Vét. 1979; 10(1): 77-86.
6. Laxminarayan R, Duse A, Wattal C, Zaidi AK, Wertheim HF, Sumpradit N, Vlieghe E, Hara GL, Gould IM, Goossens H. Antibiotic resistance - the need for global solutions. Lancet Infect Dis. 2013; 13(12): 1057-1098.
7. Agyare C, Boamah VE, Zumbi CN, Osei FB. Antibiotic use in poultry production and its effects on bacterial resistance, in antimicrobial resistance-a global threat, 2018; IntechOpen.
8. OIE MT. Partie i. Information générale. Sectioni. 1. Chapitres d’introduction-chapitre 1.1.1. Méthodes d’échantillonnage. World Organisation for Animal Health. 2005: 1-15.
9. Alamargot J. Manuel d'anatomie et d'autopsie aviaires. 1982: E'ditions du Point Vétérinaire.
10. Maryvonne D, Mouline C. Analyse qualitative et quantitative de la flore bactérienne dans la trachée du poulet sain. Ann Recherches Vét. 1983; 14(3): 189-194.
11. Cohen N, Karib H. Risque hygiénique lié à la présence des Escherichia coli dans les viandes et les produits carnés: Un réel problème de santé publique? Technol Lab. 2006; 1(1).
12. Leboffe MJ, Pierce BE. Microbiology: laboratory theory and application. 2012: Morton Publishing Company.
13. Abeid AO, Mennane Z, Hassan O, Ouhssine M. Etude microbiologique et identification des souches isolés à partir du poisson (Mugil cephalus) séché-pilé «Lekhlia» (Microbiological Study and identification of strains isolated from the fish (Mugil cephalus) dried-pounded «Lekhlia»). 2015.
14. Bertrand S, Nicolas MLG, la Faim AC, Luc MM. Recherche de VibrioCholerae dans l’environnement hydrique. 2011; Version n 1 du 21/07/2011.
15. Elhamzaoui S, Benouda A, Allali F, Abouqual R, Elouennass M. Sensibilité aux antibiotiques des souches de Staphylocoques aureus isolées dans deux hôpitaux universitaires à Rabat, Maroc. Méd Maladies Infect. 2009; 39(12): 891-895.
16. Schouten A, Tenberge KB, Vermeer J, Stewart J, Wagemakers L, Williamson B, Van Kan JA. Functional analysis of an extracellular catalase of Botrytis cinerea. Molecular Plant Pathology. 2002; 3(4): 227-238.
17. CA-SFM/EUCAST. Comité de l'antibiogramme de la société française de microbiologie /European Committee on Antimicrobial Susceptibility Testing. Vol. V.1.0 Janvier, 2019.
18. CA-SFM. Recommandations 2018 du comité del'antibiogramme de la société française de microbiologie. Groupe de Travail Antibiogramme Vétérinaire. 2018: 1-16.
19. Benameur Q, Tali-Maamar H, Assaous F, Guettou B, Benklaouz MB, Rahal K, Ben-Mahdi M-H. Characterization of quinolone-resistant Enterobacteriaceae strains isolated from poultry in Western Algeria: First report of qnrS in an Enterobacter cloacae. Vet World. 2018; 11(4): 469.
20. El-Demerdash AS, Aggour MG, El-Azzouny MM, Abou-Khadra SH. Molecular analysis of integron gene cassette arrays associated multi-drug resistant Enterobacteriaceae isolates from poultry. Cell Mol Biol. 2018; 64(5): 149-156.
21. Gay E, Chazel M, Danielle M, Haenni M, Calavas D, Jy M, Jouy E. Apport du Résapatha la problématique de l’antibiorésistance en santé animale: analyse des données recueillies en 2008 sur Escherichia coli dans les différentes filieres animales. Bull Epidémiol AFSSA. 2010; 36: 6-9.
22. Benklaouz MB, Aggad H, Benameur Q. Resistance to multiple first-line antibiotics among Escherichia coli from poultry in Western Algeria. Vet World. 2020; 13(2): 290.
23. Halfaoui Z, Menoueri NM, Bendali LM. Serogrouping and antibiotic resistance of Escherichia coli isolated from broiler chicken with colibacillosis in center of Algeria. Vet World. 2017; 10(7): 830.
24. Shecho M, Thomas N, Kemal J, Muktar Y. Cloacael carriage and multidrug resistance Escherichia coli O157: H7 from poultry farms, eastern Ethiopia. J Vet Med. 2017; 2017: 8264583.
25. Asai T, Masani K, Sato C, Hiki M, Usui M, Baba K, Ozawa M, Harada K, Aoki H, Sawada T. Phylogenetic groups and cephalosporin resistance genes of Escherichia coli from diseased food-producing animals in Japan. Acta Vet Scand. 2011; 53(1): 52.
26. Tansawai U, Walsh TR, Niumsup PR. Extended spectrum ß-lactamase-producing Escherichia coli among backyard poultry farms, farmers, and environments in Thailand. Poultry Sci. 2019; 98(6): 2622-2631.
27. Yassin AK, Gong J, Kelly P, Lu G, Guardabassi L, Wei L, et al. Antimicrobial resistance in clinical Escherichia coli isolates from poultry and livestock, China. PloS One. 2017; 12(9): e0185326.
28. He J, Li C, Cui P, Wang H. Characterization of Tn7-like transposons and its related antibiotic resistance among Enterobacteriaceae from livestock and poultry in China. 2020.
29. Siemon CE, Bahnson PB, Gebreyes WA. Comparative investigation of prevalence and antimicrobial resistance of Salmonella between pasture and conventionally reared poultry. Avian Dise. 2007; 51(1): 112-117.
30. Chatellet M-C. Modalités d’utilisation des antibiotiques en élevage bovin: enquête en Anjou. 2007, Thèse de doctorat, Faculté de médecine de Créteil, Créteil, France.
31. Meguenni N, Chanteloup N, Tourtereau A, Ahmed CA, Bounar-Kechih S, Schouler C. Virulence and antibiotic resistance profile of avian Escherichia coli strains isolated from colibacillosis lesions in central of Algeria. Vet World. 2019; 12(11): 1840.
32. Nguyen NT, Nguyen HM, Nguyen CV, Nguyen TV, Nguyen MT, Thai HQ, et al. Use of colistin and other critical antimicrobials on pig and chicken farms in southern Vietnam and its association with resistance in commensal Escherichia coli bacteria. Appl Environ Microbiol. 2016; 82(13): 3727-3735.
33. Rahmatallah N, Nassik S, El Rhaffouli H, Lahlou Amine I, El Houadfi M. Détection de souches multi-résistantes d’Escherichia coli d’origine aviaire dans la région de Rabat Salé Zemmour Zaer. Revue Maroc Sci Agronom Vét. 2016; 5(2).
34. Dandachi I, Sokhn ES, Dahdouh EA, Azar E, El-Bazzal B, Rolain J-M, Daoud Z. Prevalence and characterization of multi-drug-resistant Gram-negative bacilli isolated from Lebanese poultry: A nationwide study. Frontiers Microbiol. 2018; 9: 550.
35. Nandi SP, Sultana M, Hossain MA. Prevalence and characterization of multidrug-resistant zoonotic Enterobacter spp. in poultry of Bangladesh. Foodborne Pathog Dis. 2013; 10(5): 420-427.
36. Arhin RE, Hackman HK, Sa-eed A. Antibiotic prophylaxis and cloacal carriage of resistant zoonotic bacteria in commercially-bred poultry. Eur J Animal Health. 2019; 1(1): 1-13.
37. Ezekiel C, Olarinmoye A, Jnr JO, Olaoye O, Edun A. Distribution, antibiogram and multidrug resistance in Enterobacteriaceae from commercial poultry feeds in Nigeria. Afr J Microbiol Res. 2011; 5(3): 294-301.
38. Abdi RD, Mengstie F, Beyi AF, Beyene T, Waktole H, Mammo B, et al. Determination of the sources and antimicrobial resistance patterns of Salmonella isolated from the poultry industry in Southern Ethiopia. BMC Infect Dis. 2017; 17(1): 352.
39. Andoh LA, Dalsgaard A, Obiri-Danso K, Newman M, Barco L, Olsen JE. Prevalence and antimicrobial resistance of Salmonella serovars isolated from poultry in Ghana. Epidemiol Infect. 2016; 144(15): 3288-3299.
40. Lenchenko E, Blumenkrants D, Vatnikov Y, Kulikov E, Khai V, Sachivkina N, et al. Poultry Salmonella sensitivity to antibiotics. Syst Rev Pharmacy. 2020; 11(2): 170-175.
41. Sepehri G, Akbarpour P, Nekoobin M. Microbial resistance of broiler poultry samples to the commonly used antibiotics in Kerman. Int J Vet Res. 2008.
42. Wajid M, Awan AB, Saleemi MK, Weinreich J, Schierack P, Sarwar Y, Ali A. Multiple drug resistance and virulence profiling of Salmonella enterica serovars Typhimurium and Enteritidis from poultry farms of Faisalabad, Pakistan. Microb Drug Resist. 2019; 25(1): 133-142.
43. Begum K, Mannan SJ, Ahmed A. Antibiotic resistance, plasmids and integron profile of Salmonella species isolated from poultry farm and patients. Dhaka Univ J Pharmac Sci. 2016; 15(2): 209-214.
44. Djeffal S, Bakour S, Mamache B, Elgroud R, Agabou A, Chabou S, Hireche S, Bouaziz O, Rahal K, Rolain J-M. Prevalence and clonal relationship of ESBL-producing Salmonella strains from humans and poultry in northeastern Algeria. BMC Vet Res. 2017; 13(1): 132.
45. Suresh Y, Kiranmayi CB, Rao TS, Srivani M, Subhashini N, Chaitanya G, et al. Multidrug resistance and ESBL profile of Salmonella serovars isolated from poultry birds and foods of animal origin. 2019.
46. Nahar A, Siddiquee M, Nahar S, Anwar KS, Islam S. Multidrug resistant-proteus mirabilis isolated from chicken droppings in commercial poultry farms: Bio-security concern and emerging public health threat in Bangladesh. J Biosaf Health Educ. 2014.
47. Nemati M. Antimicrobial resistance of Proteus isolates from poultry. Eur J Exp Biol. 2013; 3(6): 499-500.
48. Shawish RR, El-Bagory A-RM, Elnahriry SS, Wafy HA, Sayed HH. Incidence of antibiotic resistant coliforms in poultry meat in Menoufia Governorate, Egypt. PSM Microbiol. 2020; 5(1): 7-13.
49. Adelowo OO, Ojo FA, Fagade OE. Prevalence of multiple antibiotic resistance among bacterial isolates from selected poultry waste dumps in Southwestern Nigeria. World J Microbiol Biotechnol. 2009; 25(4): 713-719.
50. Sala C, Morar A, Colibar O, Morvay AA. Antibiotic resistance of gram negative bacteria isolated from meat surface biofilm. Rom Biotech Lett. 2012; 17(4): 7483-92.
51. Kilonzo-Nthenge A, Rotich E, Nahashon S. Evaluation of drug-resistant Enterobacteriaceae in retail poultry and beef. Poultry Sci. 2013; 92(4): 1098-1107.
52. Faife SL, Zimba T, Sekyere JO, Govinden U, Chenia HY, Simonsen GS, Sundsfjord A, Essack SY. β-lactam and fluoroquinolone resistance in Enterobacteriaceae from imported and locally-produced chicken in Mozambique. J Infect Develop Countries. 2020; 14(05): 471-478.
53. Okorafor ON, Anyanwu MU, Nwafor EO, Anosa GN, Udegbunam RI. Multidrug-resistant enterobacteria colonize commercial day-old broiler chicks in Nigeria. Vet World. 2019; 12(3): 418-423.
54. Yulistiani R, Praseptiangga D, Raharjo D, Shirakawa T. Prevalence of antibiotic-resistance enterobacteriaceae strains isolated from chicken meat at traditional markets in Surabaya, Indonesia. MSE. 2017; 193(1): 012007.
55. Lei C-W, Zhang A-Y, Liu B-H, Wang H-N, Guan Z-B, Xu C-W, et al. Molecular characteristics of Salmonella genomic island 1 in Proteus mirabilis isolates from poultry farms in China. Antimicrob Agents Chemother. 2014; 58(12): 7570-7572.
56. Pan Y-s, Yuan L, Liu J-h, Hu G-z, Mo J. Isolation, Identification and Antimicrobial Susceptibility of Escherichia coli and Proteus mirabilis Isolated from Chicken [J]. Acta Agricult Jiangxi. 2009; 12.
57. Zhang L, Fu Y, Xiong Z, Ma Y, Wei Y, Qu X, et al. Highly prevalent multidrug-resistant Salmonella from chicken and pork meat at retail markets in Guangdong, China. Frontiers Microbiol. 2018; 9: 2104.
58. Ziech RE, Lampugnani C, Perin AP, Sereno MJ, Sfaciotte RAP, Viana C, et al. Multidrug resistance and ESBL-producing Salmonella spp. isolated from broiler processing plants. Braz J Microbiol. 2016; 47(1): 191-195.
59. Ojo OE, Ogunyinka OG, Agbaje M, Okuboye JO, Kehinde OO, Oyekunle MA. Antibiogram of Enterobacteriaceae isolated from free-range chickens in Abeokuta, Nigeria. Vet Arhiv. 2012; 82(6): 577-589.
Published
2021-03-08
How to Cite
(1)
Yahya, M.; Hammadi, K.; Faiza, F. The Antibiotic Resistance Study of Enterobacteriaceae, Yersiniaceae and Morganellaceae Bacteria Isolated from Broilers (outside Veterinary Control) in Western Algeria. European Journal of Biological Research 2021, 11, 217-233.
Section
Research Articles
This work is licensed under a Creative Commons Attribution 4.0 International License.
