American Journal of Microbiological Research
ISSN (Print): 2328-4129 ISSN (Online): 2328-4137 Website: https://www.sciepub.com/journal/ajmr Editor-in-chief: Apply for this position
Open Access
Journal Browser
Go
American Journal of Microbiological Research. 2024, 12(4), 98-105
DOI: 10.12691/ajmr-12-4-4
Open AccessArticle

Prevalence and Characteristics of Intestinal Carriage of Multidrug-Resistant Enterobacteriaceae in Outpatients in Abidjan

Kofi Kobina Amandzé Adams1, 2, , Koffi Kouadio Stéphane2, 3, Yapi Ivane Alexia3, Dine Mourtada3, 4, Obouayeba Nguessan Djaman Carole1, Guessend Nathalie5, Kra Adou Koffi Mathieu1 and Kacou-N’douba Adèle3

1Laboratoire de Biologie et Santé, Université Félix Houphouët Boigny, Abidjan, Côte d’Ivoire

2Laboratoire de Bactériologie-Virologie, Centre Hospitalier Universitaire de Treichville, Abidjan, Côte d’Ivoire

3Département Sciences Fondamentales et bio-cliniques, Unité de Formation et de Recherches Sciences Médicales, Université Félix Houphouët Boigny, Abidjan, Côte d’Ivoire

4Service des Maladies Infectieuses et Tropicales, Centre Hospitalier Universitaire de Treichville, Abidjan, Côte d’Ivoire

5Centre National de Référence des Antibiotiques, Institut Pasteur de Côte d’Ivoire

Pub. Date: September 12, 2024

Cite this paper:
Kofi Kobina Amandzé Adams, Koffi Kouadio Stéphane, Yapi Ivane Alexia, Dine Mourtada, Obouayeba Nguessan Djaman Carole, Guessend Nathalie, Kra Adou Koffi Mathieu and Kacou-N’douba Adèle. Prevalence and Characteristics of Intestinal Carriage of Multidrug-Resistant Enterobacteriaceae in Outpatients in Abidjan. American Journal of Microbiological Research. 2024; 12(4):98-105. doi: 10.12691/ajmr-12-4-4

Abstract

Background: The growing threat of antibiotic resistance poses a major challenge to global public health as it could lead to up to 10 million deaths annually by 2050, particularly in low-income countries. The COVID-19 pandemic has further worsened the issue of multidrug-resistant bacteria, particularly extended-spectrum β-lactamase-producing Enterobacteriaceae (ESBL-PE). In Africa, data on intestinal carriage on ESBL-PE are scarce. This study aimed to assess the prevalence and risk factors associated with ESBL-PE intestinal carriage among outpatients at Treichville University Hospital. Method: This study was conducted from July to December 2023 at Treichville University Hospital. Rectal swabs were collected from patients attending the general medical consultation ward selected by systematic random sampling. Enterobacteriaceae strains were identified by conventional methods and antibiotic susceptibility testing was carried out in accordance with the CA-SFM EUCAST 2022 guidelines. Data were analysed using R studio software version 4.0.3. Results: Rate of intestinal carriage with resistance Enterobacteriaceae was 54.55%. Prevalence of ESBL-PE in intestinal carriage was 30.90%. Among ESBL-PE carriers, the predominant age group was between 40 years and older; with a sex ratio of 1.26 (55.88% male). Escherichia coli and Klebsiella pneumoniae were the common ESBL producer species at 43.33% and 11.67% respectively. According to observed resistance patterns and predefined multidrug resistance categories, 94.60% of Escherichia coli strains and 100.00% of Klebsiella pneumoniae strains were identified as Multidrug-resistant. Only 5.40% of Escherichia coli strains were identified as Extensively drug-resistant. No isolates were classified as Pandrug- resistant. Risk factors like size of household living in a single room, presence of children under 15 years old, previous hospitalization (less than 6 months), antibiotic use (less than 3 months) and chronic medical diseases were significantly associated with ESBL-PE intestinal carriage (p<0.05). Conclusion: High rate of ESBL-PE in intestinal carriage was observed. The knowledge of factors associated with Multi-resistant Enterobacteriaceae carriage helps to identify patients at risk to combat the spread of resistant bacteria within the healthcare system.

Keywords:
intestinal carriage antibiotic resistance enterobacteriaceae ESBL Low-income contry Côte d’Ivoire

Creative CommonsThis work is licensed under a Creative Commons Attribution 4.0 International License. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

References:

[1]  O’Neill J., Review on antimicrobial resistance: tackling drug-resistant infections globally: final report and recommendations, Government of the United Kingdom Publisher, 2016.
 
[2]  Shrivastava S. R., Shrivastava P. S., Ramasamy J., “World health organization releases global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics”, Journal of Medical Society, 32 (1). 76-77. April 2018.
 
[3]  Rello J., Kalwaje E. V., Lagunes L., Alves J., Wunderink R. G., Conway-Morris A., Rojas J.N., Alp E., Zhang Z., “A global priority list of the TOp TEn resistant Microorganisms (TOTEM) study at intensive care: a prioritization exercise based on multi-criteria decision analysis”, Eur J Clin Microbiol Infect Dis, 38 (2). 319-323. February 2019.
 
[4]  Shaikh S., Fatima J., Shakil S., Rizvi S.M., Kamal M.A., “Antibiotic resistance and extended spectrum beta-lactamases: Types, epidemiology and treatment”, Saudi J Biol Sci, 22 (1). 90-101. January 2015.
 
[5]  Pitout J. D. D., Laupland K. B., “Extended-spectrum β-lactamase-producing Enterobacteriaceae: an emerging public-health concern”, Lancet Infect Dis, 8 (3). 159-166. March 2008.
 
[6]  Bradford P. A., “Extended-spectrum β-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat”, Clin Microbiol Rev, 14 (4). 933–951. October 2001.
 
[7]  Rai S., Das D., Niranjan D. K., Singh N. P., Kaur I. R., “Carriage prevalence of carbapenem-resistant Enterobacteriaceae in stool samples: A surveillance study”, Australas Med J, 7 (2). 64-67. February 2014.
 
[8]  Woerther P.L., Burdet C., Chachaty E., Andremont A., “Trends in human fecal carriage of extended-spectrum β-lactamases in the community: toward the globalization of CTX-M”, Clin Microbiol Rev, 26 (4). 744–758. October 2013.
 
[9]  Karanika S., Karantanos T., Arvanitis M., Grigoras C., Mylonakis E., “Fecal colonization with extended-spectrum beta-lactamase–producing Enterobacteriaceae and risk factors among healthy individuals: a systematic review and metaanalysis”, Rev Infect Dis, 63 (3). 310–318. August 2016.
 
[10]  Bezabih Y.M., Sabiiti W., Alamneh E., Bezabih A., Peterson G.M., Bezabhe W.M., Roujeinikova A., “The global prevalence and trend of human intestinal carriage of ESBL-producing Escherichia coli in the community”, J Antimicrob Chemother, 76 (1). 22-29. January 2021.
 
[11]  Sallem R. B., Slama K. B., Estepa V., Cheikhna E. O., Mohamed A. M., Chairat S., Torres C., “Detection of CTX-M-15-producing Escherichia coli isolates of lineages ST410-A, ST617-A and ST354-D in faecal samples of hospitalized patients in a Mauritanian hospital”, Journal of Chemotherapy, 27 (2). 114-116. February 2015.
 
[12]  Djuikoue I.C., Woerther P.L., Toukam M., Burdet C., Ruppé E., Gonsu K.H., Fokunang C., El Mniai A., Larissa K., Pieme A.C., Mboupaing M.G., Kakam C.M., Fogang H.K., Andremont A., Ngogang J., “Intestinal carriage of Extended Spectrum Beta-Lactamase producing E. coli in women with urinary tract infections, Cameroon,”. J Infect Dev Ctries, 10 (10). 1135-1139. October 2016.
 
[13]  Lontsi N. G., Houcke S., Matheus S., Nkontcho F., Pujo J.M., Higel N., Ba A., Cook F., Gourjault C., Mounier R., “Impact of Antibiotic Consumption on the Acquisition of Extended-Spectrum β-Lactamase Producing Enterobacterales Carriage during the COVID-19 Crisis in French Guiana”. Antibiotics, 12(1). 58-65.  December 2022.
 
[14]  Emeraud C., Figueiredo S., Bonnin R.A., Khecharem M., Ouzani S., Leblanc P-E, Jousset A.B., Fortineau N., Duranteau J., Dortet L., “Outbreak of CTX-M-15 Extended-Spectrum β-Lactamase-Producing Klebsiella pneumoniae ST394 in a French Intensive Care Unit Dedicated to COVID-19”, Pathogens, 10 (11). 1426-1437. October 2021.
 
[15]  Mai H.T.T., Espinoza J.L., “The Impact of COVID-19 Pandemic on ESBL-Producing Enterobacterales Infections: A Scoping Review”, Antibiotics, 12 (6). 1064-1073. June 2023.
 
[16]  Livermore D.M., Mushtaq S., Doumith M., Jamrozy D., Nichols W.W., Woodford N., “Selection of mutants with resistance or diminished susceptibility to ceftazidime/avibactam from ESBL- and AmpC-producing Enterobacteriaceae”, J Antimicrob Chemother, 73 (12). 3336-3345. Decembre 2018.
 
[17]  Ouattara M. B., Guessend K.N., Koffi N.R., Koffi S., Ouattara G. D., Gbonon V., Tiekoura K.B., Fay-Kette H., Dosso M., “Evaluation of Drigalski agar supplemented with ceftazidime (2 mg/L) for selective isolation of extended-spectrum beta-lactamase (ESBL) producing Enterobacteria”, African J Microbiol Res, 8 (29). 2758–2765. July 2014.
 
[18]  Lal A., Cheeptham N., “Eosin-methylene blue agar plates protocol” American Society for Microbiology Publisher, 2007.
 
[19]  Harrigan W. F., McCance M. E., “Laboratory methods in microbiology”, Sciences, June 2014.
 
[20]  Comité de l’antibiogramme de la Société Française de Microbiologie Recommandations 2022 V.1.0 Mai.
 
[21]  Magiorakos A.P., Srinivasan A., Carey R.B., Carmeli Y., Falagas M.E., Giske C.G., Harbarth S., Hindler J.F., Kahlmeter G., Olsson-Liljequist B., Paterson D.L., Rice L.B., Stelling J., Struelens M.J., Vatopoulos A., Weber J.T., Monnet D.L., “Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance”, Clin Microbiol Infect, 18 (3). 268-281. March 2012.
 
[22]  Sahraoui H. L., Quasmaoui A., Charof R., Mennane Z., “Detection methods of Enterobacteriaceae producing extended spectrum betalactamase”, Int J Innov Appl Stud, 15 (2). 232-239. April 2016.
 
[23]  Jeon K., Jeong S., Lee N., Park M-J., Song W., Kim H-S., Kim H.S., Kim J-S., “Impact of COVID-19 on Antimicrobial Consumption and Spread of Multidrug-Resistance in Bacterial Infections”, Antibiotics, 11 (4). 535-542. April 2022.
 
[24]  Livermore D. M., “Antibiotic resistance during and beyond COVID-19”, JAC Antimicrob Resist, 3 (1). 5-16. June 2021.
 
[25]  Antimicrobial Resistance Collaborators., “Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis”, Lancet. 12 (10325). 629-655. February 2022
 
[26]  Ouattara M.B., Wognin A. S., Anatole T. A., Carole G. M. V., Gédeon K. K., Bertin G. K., Bertin T. K., Fernique K. K., Innocent K. K., Kpoda D. S., Ayayi A., Ali K., Kouadio G. N., Alphonse K., Mireille D., “Role of Healthy Human Gut Microbiota in the Emergence and Dissemination of Extended-Spectrum β-lactamase-Producing Enterobacteriaceae and Genes Associated with β-lactam Resistance in Community Settings in Abidjan, Côte d’Ivoire”. Microbiology Research Journal International, 33 (7). 27–37. September 2023.
 
[27]  Lautenbach E., Mosepele M., Smith R.M., Styczynski A., Gross R., Cressman L., Jaskowiak-Barr A., Alby K., Glaser L., Richard-Greenblatt M., Cowden L., Sewawa K., Otukile D., Paganotti G.M., Mokomane M., Bilker W.B., Mannathoko N., “Risk Factors for Community Colonization With Extended-Spectrum Cephalosporin-Resistant Enterobacterales (ESCrE) in Botswana: An Antibiotic Resistance in Communities and Hospitals (ARCH) Study”, Clin Infect Dis, 77 (1). 89-96. July 2023.
 
[28]  Mandal D.K., Sah S.K., Mishra S.K., Sharma S., Kattel H.P., Pandit S., Yadav P.K., Laghu U., Lama R., Sah N.P., Sherchand J.B., Parajuli K., Bastola A., Pun S.B., Rijal B.P., Pokharel B.M., “Carriage of Extended-Spectrum-β-Lactamase- and AmpC-β-Lactamase-Producing Enterobacteriaceae (ESBL-PE) in Healthy Community and Outpatient Department (OPD) Patients in Nepal”, Can J Infect Dis Med Microbiol, Article ID 5154217. 9 pages. February 2020.
 
[29]  Obeng-Nkrumah N., Hansen D. S., Awuah-Mensah G., Blankson N. K., Frimodt-Møller N., Newman M. J., Krogfelt K., “High level of colonization with third-generation cephalosporin-resistant Enterobacterales in African community settings, Ghana”, Diagnostic Microbiology and Infectious Disease, 106 (1). Article ID 115918. 10 pages. May 2023.
 
[30]  Mahamat D. D., Sore S., “Faecal carriage of extended-spectrum beta-lactamase-producing Enterobacteriaceae in healthy volunteers and hospitalized patients in Ouagadougou, Burkina Faso: prevalence, resistance profile, and associated risk factors”, International Journal of Infectious Diseases, 116 (1). 15-16, March 2022.
 
[31]  Mustapha A., Chidiebere O., Bata M., Ali Z. D., Victor F. I., Yakubu M. N., David A. S., “Fecal carriage rates of extended-spectrum Β-lactamase-producing Escherichia coli of inpatients and outpatients attending Yobe State Teaching Hospital, Damaturu, Nigeria.” Microbes and Infectious Diseases, 4 (4). 1173-1177. November 2023.
 
[32]  Lewis J. M., Lester R., Garner P., Feasey N. A., “Gut mucosal colonisation with extended-spectrum beta-lactamase producing Enterobacteriaceae in sub-Saharan Africa: a systematic review and meta-analysis”, Wellcome Open Res, 4 (1). 160-178. October 2020.
 
[33]  Herfst S., Böhringer M., Karo B., Lawrence P., Lewis N. S., Mina M. J., Menge C., “Drivers of airborne human-to-human pathogen transmission”, Current opinion in virology, 22 (1). 22-29. February 2017.
 
[34]  Godijk N. G., Bootsma M. C. J., Bonten M. J. M., “Transmission routes of antibiotic resistant bacteria: a systematic review,” BMC Infect Dis, 22 (1). 482- 497. May 2022.
 
[35]  Guessennd N.K., Kacou-N’douba A., Gbonon V., Yapi D., Ekaza E., Dosso M., Courvalin P., “Prévalence et profil de résistance des Entérobactéries productrices de beta lactamases a spectre élargi (BLSE) à Abidjan côte d’ivoire de 2005 à 2006”, J. sci. pharm. Biol, 9 (1). 63-70, April 2008.
 
[36]  Ouedraogo A.-S., Sanou M., Kissou A., Sanou S., Solaré H., Kaboré F., Poda A., Aberkane S., Bouzinbi N., Sano I., “High prevalence of extended-spectrum ß-lactamase producing enterobacteriaceae among clinical isolates in Burkina Faso”, BMC Infect. Dis, 16 (1). 326-335. June 2016.
 
[37]  Mahamat O.O., Tidjani A., Lounnas M., Hide M., Benavides J., Somasse C., Ouedraogo A.S., Sanou S., Carrière C., Bañuls A.L., Jean-Pierre H., Dumont Y., Godreuil S., “Fecal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae in hospital and community settings in Chad”. Antimicrob Resist Infect Control, 8(1). 169-176. October 2019.
 
[38]  Ventola C.L., ‘’The antibiotic resistance crisis: part 1: causes and threats’’. Pharmacy and Therapeutics, 40 (8). 277-83. April 2015.
 
[39]  Fatoumata K.M., Anatole A.T., Victoire G., Valerie G.M., Fernique K.K., Bertin K.G., Ouattara M.B., Tiekoura K., Nathalie G., Mireille D., “Detection of qnr Genes That Mediate Fluoroquinolone Resistance in Gram-Negative Bacilli in Abidjan, Côte d’Ivoire” Am J Microbiol Res, 11 (3). 79–82, October 2023.
 
[40]  Guessennd N., Bremont S., Gbonon V., Kacou-Ndouba A., Ekaza E., Lambert T., Dosso M., Courvalin P., “Qnr-type quinolone resistance in extended-spectrum beta-lactamase producing enterobacteria in Abidjan, Ivory Coast”, Pathol Biol, 56 (8). 439-44. December 2008.
 
[41]  TahouJ. E., Guessennd N. K., Sokouri P. D., Gbonon V., Konan F., Kouadio J., Gba K. K., Ouattara B. M., N’guetta S.P. A., “Antimicrobial Resistance of Klebsiella pneumoniae -ESBL Producing Strains Isolated from Clinical Specimens in Abidjan (Cote de Ivoire)”, Microbiology Research Journal International, 20 (2). 1–7. June 2017.
 
[42]  Carattoli A. “Plasmids and the spread of resistance”. Int J Med Microbiol, 303(6-7). 298-304. August 2013.
 
[43]  Partridge S.R., Kwong S.M., Firth N., Jensen S.O., “Mobile Genetic Elements Associated with Antimicrobial Resistance”, Clin Microbiol Rev. 31(4). 17-88. August 2018.
 
[44]  Tzouvelekis L. S., Markogiannakis A., Piperaki E., Souli M., Daikos G. L., “Treating infections caused by carbapenemase-producing Enterobacteriaceae”, Clinical Microbiology and Infection, 20 (9). 862–872. September 2014.
 
[45]  Nordmann P., Naas T., Poirel L., “Global spread of carbapenemase-producing Enterobacteriaceae”, Emerg Infect Dis, 17 (10). 1791-1799. October 2011.
 
[46]  Van den Bunt G., Liakopoulos A., Mevius D. J., Geurts Y., Fluit A. C., Bonten M. J. M., Mughini-Gras L., Van Pelt W., “ESBL/AmpC-producing Enterobacteriaceae in households with children of preschool age: prevalence, risk factors and co-carriage”, Journal of Antimicrobial Chemotherapy, 72 (2). 589-595. February 2017.
 
[47]  Otter J.A., Natale A., Batra R., Tosas Auguet O., Dyakova E., Goldenberg S.D., Edgeworth J.D.,”Individual- and community-level risk factors for ESBL Enterobacteriaceae colonization identified by universal admission screening in London”, Clinical Microbiology and Infection, 25 (10). 1259-1265. March 2019.
 
[48]  Cocker D., Sammarro M., Chidziwisano K., “Drivers of Resistance in Uganda and Malawi (DRUM): a protocol for the evaluation of One-Health drivers of Extended Spectrum Beta Lactamase (ESBL) resistance in Low-Middle Income Countries (LMICs)”, Wellcome Open Res, 7 (1).55-69. 2022.
 
[49]  Farra A., Frank T., Tondeur L., Bata P., Gody J.C., Onambele M., Rafaï C., Vray M., Breurec S., “High rate of faecal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae in healthy children in Bangui, Central African Republic”, Clin Microbiol Infect. 22 (10). 891-895. October 2016.
 
[50]  Cocker D., Chidziwisano K., Mphasa M., Mwapasa T., Lewis J.M., Rowlingson B., Sammarro M., Bakali W., Salifu C., Zuza A., Charles M., Mandula T., Maiden V., Amos S., Jacob S.T., Kajumbula H., Mugisha L., Musoke D., Byrne R., Edwards T., Lester R., Elviss N., Roberts A.P., Singer A.C., Jewell C., Morse T., Feasey N.A., “Investigating One Health risks for human colonisation with extended spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae in Malawian households: a longitudinal cohort study”, Lancet Microbe. 4 (7). 534-543. July 2023.