High Carrying Rate of Extended-Spectrum Beta-Lactamase (ESBL) Producing Enterobacteriaceae by Slaughterhouse Workers in Lomé, Togo in 2019

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Amivi Mawussi Godonou
Fifonsi Adjidossi Gbeasor-Komlanvi
Novissi Tsogbale
Fiali Lack
Sika Dossim
Komla Batassé Batawui
Yaovi Agbekponou Ameyapoh
Koumavi Ekouevi
Anoumou Yaotsè Dagnra
Mounerou Salou


Introduction: Extended-spectrum beta-lactamase-producing Enterobacteriaceae (ESBL) represent a real public health concern because of their spread. The role of agri-food chains in transmitting of digestive ESBL-producing bacterial strains in the community, was demonstrated but little work was done in our settings (Togo, west Africa). The aim of this study was to estimate the rate of digestive carrying ESBL producing enterobacteriacae in slaughterhouse workers in Lomé, Togo.

Material and Methods: This was a cross-sectional study carried out in three slaughterhouses in Lomé. Fresh stools of 60 slaughterhouse workers and socio-demographic data were collected during the period of September to October 2019 after obtaining the consent of each participant.

The bacterial strains of interest were isolated on the selective medium Purple Bromocresol + Ceftazidime at 6µg/l. UriselectÒ and API 20E media were used for identification. Antibiotic susceptibility test was performed in Mueller-Hinton agar plate diffusion method (Kirby Bauer technic) and according to CASFM-EUCAST recommendations.

Results: The digestive carriage rate of ESBL producing enterobacteriacae among professionals of three slaughterhouses of Lomé was 80% (n=48/60). Escherichia coli was the main bacteria 78.2% (n = 43/55) followed by Klebsiella pneumoniae 16.4% (n = 9/55) and Enterobacter cloacae 5.4% (n = 3/55). The antibiotic profile of ESBL producing enterobacteriacae showed resistance to Amoxycillin + Clavulanic Acid (26%), Ticarcillin + Clavulanic Acid (86%), Piperacillin + Tazobactam (14%), Cefoxitin (7%) Ciprofloxacin (63%), Levofloxacin (49%), Nalidixic Acid (42%), Chloramphenicol (33%), Gentamicin (21%), Sulfamethoxazole-Trimetoprim (93%). These bacteria were 100% sensitive to Imipenem, Ertapenem, Amikacin and Fosfomycin.

Conclusion: This study revealed a very high carriage rate of ESBL producing Enterobacteriacae among Slaughterhouse Workers in Lomé. It confirmed the major potential role of the agri-food chains in the spread of ESBL producing bacteria in the Community.

Digestive carrying ESBL producing bacteria, workers, slaughterhouse, Lomé.

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How to Cite
Godonou, A. M., Gbeasor-Komlanvi, F. A., Tsogbale, N., Lack, F., Dossim, S., Batawui, K. B., Ameyapoh, Y. A., Ekouevi, K., Dagnra, A. Y., & Salou, M. (2020). High Carrying Rate of Extended-Spectrum Beta-Lactamase (ESBL) Producing Enterobacteriaceae by Slaughterhouse Workers in Lomé, Togo in 2019. Microbiology Research Journal International, 30(11), 30-41. https://doi.org/10.9734/mrji/2020/v30i1130281
Original Research Article


Overdevest I, Willemsen I, Rijnsburger M, Eustace A, Xu L, Hawkey P, et al. Extended-spectrum β-lactamase genes of Escherichia coli in chicken meat and humans, the Netherlands. Emerg Infect Dis 2011;17(7):1216–1222.

Rogers BA, Aminzadeh Z, Hayashi Y, Paterson DL.Country-to-country transfer of patients and the risk of multi-resistant bacterial infection. Clin Infect Dis. 2011;53(1):49–56.

Jouini A, Vinué L, Slama KB, Sáenz Y, Klibi N, Hammami S, et al.Characterization of CTX-M and SHV extended-spectrum β-lactamases and associated resistance genes in Escherichia coli strains of food samples in Tunisia. J Antimicrob Chemother. 2007;60:1137–41.

Leverstein-van Hall MA, Dierikx CM, Cohen Stuart J, Voets GM, van den Munckhof MP, van Essen-Zandbergen A, et al. Dutch patients, retail chicken meat and poultry share the same ESBL genes, plasmids and strains. Clin Microbiol Infect.2011;17:873–80.

Kola A, Kohler C, Pfeifer Y, Schwab F, Kühn K, Schulz K, et al.High prevalence of extended-spectrumbeta-lactamase producing Enterobacteriaceae in organic and conventional retail chicken meat, Germany. J Antimicrob Chemother 2012; 67:2631–2634.

Dohmen W, Bonten MJM, Bos MEH, Marm S , Scharringa J, Wagenaar JAet al. Carriage of extended-spectrum beta-lactamases in pig farmers is associated with occurrence in pigs. Clin. Microbiol. Infect. : The Official Publication of the European Society of Clinical Microbiology and Infectious Diseases. 2015; 21:917–923.

Dierikx C, van der Goot J, Fabri T, Essen-Zandbergen A, Smith H, Mevius D. Extended-spectrum-β-lactamase- and AmpC-β-lactamase-producing Escherichia coli in Dutch broilers and broiler farmers. J Antimicrob Chemother. 2013;68(1):60–67.

Hammerum AM, Larsen J, Andersen VD,Lester CH, Skytte TSS, Hansen F et al.Characterization of extended spectrum beta-lactamase (ESBL)-producing Escherichia coli obtained from Danish pigs, pig farmers and their families from farms with high or no consumption of third- or fourth-generation cephalosporins. J Antimicrob Chemother. 2014; 69(10):2650–2657.

Geser N, Stephan R, Kuhnert P, Zbinden R, Kaeppeli U, Cernela Net al. Fecal carriage of extended-spectrum beta-lactamase-producing Enterobacteriaceae in swine and cattle at slaughter in Switzerland. J Food Prot. 2011; 74(3):446–449.

Agyare C, Boamah VE, Zumbi CN, Osei FB. Antibiotic Use in Poultry Production and Its Effects on Bacterial Resistance. Antimicrobial Resistance—A Global Threat. Intech Open; 2018.

Jasovsky´ D, Littmann J, Zorzet A, Cars O. Antimicrobial resistance-a threat to the world’s sustainable development. Ups J Med Sci. 2016; 121:159–64.

Li B, Webster TJ. Bacteria antibiotic resistance: New challenges and opportunities for implant-associated orthopedic infections. J Orthop Res. 2018; 36:22–32.

Prestinaci F, Pezzotti P, Pantosti A. Antimicrobial resistance: A global multifaceted phenomenon. Pathog Glob Health. 2015;109(7):309–318.

Michael CA, Dominey-Howes D, Labbate M. The antimicrobial resistance crisis: Causes, consequences, and management. Front Public Health. 2014;2(145):1-8

Miles TD, McLaughlin W, Brown PD. Antimicrobial resistance of Escherichia coli isolates from broiler chickens and humans. BMC Vet Res. 2006; 2:7.

Ouedraogo AS, Sanou S, Kissou A, Poda A, Aberkane S, Bouzinbi N, et al. Fecal Carriage of Enterobacteriaceae Producing Extended-Spectrum Beta-Lactamases in Hospitalized Patients and Healthy Community Volunteers in Burkina Faso, Microb Drug Resist. 2016: 1-8.

Mahamat OO, Tidjani A,lounnas M, Hide M, Benavides Jet al. Fecal carriage of extended-spectrum beta-lactamase producing Enterobacteriacae in hospital and community settings in Chad. Antimicrobial Resistance & Infection Control. 2019:169(8).

Michaud C, Seck A, Senghor ML, Richard V, Bercion R. Evaluation du taux de portage digestif des entérobactéries productrices β-lactamase à spectre élargi d’origine communautaire chez les travailleurs et les porcs de la ferme de Bignona. Posters / Médecine et maladies infectieuses 2014 ; (44) : 78-81.

Toudji AG, Djeri B, Karou SD, Tigossou S, Ameyapoh Y, de Souza C. Prévalence des souches d’entérobactéries productrices de bêta-lactamases à spectre élargi isolées au Togo et de leur sensibilité aux antibiotiques. Int. J. Biol. Chem. 2017; 11(3):1165-1177

Salou M, Assimadi K, Wateba IM, Dossim S, Tigossou SD, Dagnra AYet al. Résistance aux antibiotiques des bactéries isolées en 2009 au laboratoire de bactériologie du CHU-Tokoin Lomé-Togo. J Recher Scient UL. 2011 ;13 :151-159.

Bonnet R, Bru JP, Caron F,Cattoir V, Courvalin P, Dubreuil L, et al. Comité de l’antibiogramme de la Société Française de Microbiologie. Recommandations V.1.0 Janvier ; 2019.

Carter MW, Oakton KJ, Warner M, Livermore DM. Detection of extended-spectrum beta-lactamases in klebsiellae with the Oxoid combination disk method. J Clin Microbiol. 2000;38:4228–4232.

Valverde A, Coque MT, Sanchez-Moreno MP, Rollan A, Baquero F, Canton R.Dramatic increase in prevalence of fecal carriage of extended-spectrum b-lactamase-producing Enterobacteriaceae during nonoutbreak situations in Spain. J Clin Microbiol 2004; 42:4769–4775.

Miro´ E, Mirelis B, Navarro F, Rivera A, Mesa RS, Roig MC, et al. Surveillance of extendedspectrum b-lactamases from clinical samples and fecal carriers in Barcelona, Spain. J Antimicrob Chemother 2005; 56:1152–1155.

Garcıa FJC, Seral GC, De la Gandara MP.The epidemiology of ESBL-producing Enterobacteriaceae in hospitalized and ambulatory patients during two non-outbreak periods. Eur J ClinMicrobiol Infect Dis 2007; 26:77-78

Moubareck C, Daoud Z, Hakime´ NI, Hamze M, Mangeney N, Matta H, et al. Country wide spread of community- and hospital-acquired extended-spectrum b-lactamase (CTX-M-15)-producing Enterobacteriaceae in Lebanon. J Clin Microbiol. 2005;43(7):3309–3313.

Rodrigues C, Shukla U, Jog S, Mehta A. Extended-spectrum b-lactamase-producing flora in healthy persons. Emerg Infect Dis. 2005;11(6):981–982.

Kader AA, Kumar A, Kamath KA. Fecal carriage of extended spectrum b-lactamase-producing Escherichia coli and Klebsiella pneumoniae in patients and asymptomatic healthy individuals. Infect Control Hosp Epidemiol 2007; 28:1114–1116.

Luvsansharav U, Hirai I, Nakata A, Imura K, Yamauchi K, Niki M et al. Prevalence of and risk factors associated with fecal carriage of CTX-M b-lactamase-producing Enterobacteriaceae in rural Thai communities. J Antimicrob Chemother 2012;67:1769–1774.

Saleem R, Ejaz H, Zafar A, Younas S, Rathore AW. Phenotypic characterization of extended-spectrum-beta—lactamase producing E. coli from healthy individuals, patients, sewage sludge, cattle, chickens and raw meat. Pak J Med Sci. 2017;33(4):886-890.

DOI : 10.12669/pjms.334.12647

Sasaki T, Hirai I, Niki M, Nakamura T, Komalamisra C, Maipanich W, et al. High prevalence of CTX-M b-lactamase-producing enterobacteriaceae in stool specimens obtained from healthy individuals in Thailand. J Antimicrob Chemother. 2010;65(4):666-668.

Aworh KM, IKwaga J, Okolocha E, Mba N, Thakur S. Prevalence and risk factors for multi-drug resistant Escherichia coli among poultry workers in the Federal Capital Territory, Abuja, Nigeria. PLoS ONE. 2019, 14(11):e0225379.

Nguyen VT, Carrique-Mas JJ, Ngo TH, Ho HM, Ha TT, Campbell JI, et al. Prevalence and risk factors for carriage of antimicrobial-resistant Escherichia coli on household and small-scale chicken farms in the Mekong Delta of Vietnam. J AntimicrobChemother, 2015;70:2144–2152

Goossens H, Ferech M, Stichele RV, Elseviers M, ESAC Project Group. Outpatient antibiotic use in Europe and association with resistance: a cross-national database study. Lancet. 2005; 365(9459):579–587.

Tian SF, Chen BY, Chu YZ, Wang S. Prevalence of rectal carriage of extended-spectrum b-lactamase-producing Escherichia coli among elderly people in community settings in China. Can J Microbiol. 2008;54,781–785.

Dohmen W, Van Gompel L, Schmitt H, Liakopoulos A, Heres L, Urlings BAet al. ESBL carriage in pig slaughterhouse workers is associated with occupational exposure. Epidemiol. Infect., Cambridge University Press. 2017;1-8.

Otter JA, Natale A, Batra R,Auguet OT, Dyakova E, Goldenberg SD, et al. Individual-and community-level risk factors for ESBL Enterobacteriaceae colonization identified by universal admission screening in London. Clin Microbiol Infect. 2019; 25:1259-1265.

Sogaard M, Heide-Jorgensen U, Vandenbroucke JP, Schonheyder HC, Vandenbroucke-Grauls C. Risk factors for extended-spectrum beta-lactamase-producing Escherichia coli urinary tract infection in the community in Denmark: a case-control study. Clin Microbiol Infect. 2017;23(12):952–960.

Chanoine M, Gruson C, Bialek-Davenet S, Bertrand X, Thomas-Jean F, Bert F et al. 10-Fold increase (2006-11) in the rate of healthy subjects with extended-spectrumbeta- lactamase-producing Escherichia coli fecal carriage in a Parisian check-up centre. J Antimicrob Chemother. 2013;68(3):562-568.