Open Access


Research Article

Main Article Content

Kumel Kasongo Kumelundu corresponding author
Berthe Nkema Miwanda
Ronald Ng'etich
Samuel Njoroge
Denis Kakongo Kandolo
Michel Balaka Ekwalanga
Emmanuel Mposhi Malangu
Victor Ndibualonji
Claude Lubobo Kazadi
Philomène Anzwal Lungu
Clément Numbi Kashindi
Prosper Muenze Kalenga
Léon Kafita Cibuabua
John Kiiru
Samuel Kariuki
Jean-Jacques Tamfum Muyembe
Christophe Mukena Nyembo


Background: This study has its foundation following the emergence of the phenomenon of antimicrobial resistance of Salmonella enterica enterica Typhi associated with severe complications, such as intestinal perforations with a significant lethality.
Objectives: Of this antimicrobial resistance, to determine the phenotypic profile, to detect the chromosomal molecular markers (CMMs) such as the class 1 integrons (intl-1) and ESBLs (blaTEM-1, blaOXA-1 and blaCTX-M-1) and to measure the association between the phenotypic profile and CMMs of typhoid isolates in concerned areas.
Methods:  Salmonella Typhi strains of typhoid epidemic areas were confirmed by serotyping tests. The antimicrobial susceptibility testing was conducted by disc diffusion method using the following commercial antimicrobials: Chloramphenicol-C, Ampicillin-AMP, Sulfamethoxazole-RL and Trimethoprim-W (former first-line antimicrobials), Ciprofloxacin-CIP or Cefotaxime-CTX, Ceftriaxone-CRO, Ceftazidime-CAZ (first-line antimicrobials), Tetracycline-TE, Amoxicillin-Potassium clavulanate-AMC, Nalidixic acid-NA, Cefoxitine-FOX, Gentamicin-CN (varied antimicrobials) and FEP-Cefepime (4GC). The phenotypic antimicrobial resistance profile was determined by Kirby-Bauer diffusion method on Mueller-Hinton agar. To perform the molecular characterization, the Salmonella Typhi isolates DNA has been extracted by Sigma Aldrich kit and the CMMs detection was performed by DNA Engine for PCR test. The association between phenotypic profile and CMMs has been measured by Pearson’s chi-square test.
Results: Out of 320 Salmonella Typhi isolates, 50 were identified conform. The phenotypic profile of antimicrobial resistance was 59.5% in all the Western and Southern regions and 61% in the provinces of Kinshasa City and Bas-Congo to the former antimicrobials of first intention and the mean of CMMs rates were 22.5% and 27.4%, respectively. Those isolates showed a significant resistance profile to AMP, C and RL in those last two provinces.
Conclusion: The rate of phenotypic multidrug-resistance of Salmonella Typhi isolates was more than 50% with the predominance of CMMs in Kinshasa and Bas-Congo. This study suggests to give up the use of AMP, C and RL in those two provinces. This may also indicate that the antimicrobial resistance surveillance system would be one strategy to manage food borne pathogens.

multidrug-resistance, Salmonella Typhi, phenotypic profile, chromosomal markers

Article Details

How to Cite
Kumelundu, K., Miwanda, B., Ng’etich, R., Njoroge, S., Kandolo, D., Ekwalanga, M., Malangu, E., Ndibualonji, V., Kazadi, C., Lungu, P., Kashindi, C., Kalenga, P., Cibuabua, L., Kiiru, J., Kariuki, S., Muyembe, J.-J., & Nyembo, C. (2022). Antimicrobial resistance of Salmonella enterica Typhi in the Western and Southern Regions of the Democratic Republic of the Congo: Phenotypic profile and molecular characterization of isolates associated with epidemics of Typhoid Fever. Advances in General Practice of Medicine, 4(1), 28-41.


  1. Buller N, Thomas A and Barton M. Antimicrobial, Animal health Laboratories, Australia and New Zealand Standard Diagnostic Procedures. 2014, 31st Ed. Zealand, 30 P.
  2. Steele AD, Deborah C, Burgess H, et al. Challenges and opportunities for Typhoid Fever control: A call for coordinated action. Clinical Infection Diseases, 2016, 62(S1): S4-S8.
  3. Weill FX La fièvre typhoïde n'est plus aussi simple à soigner. Med Sci Paris, 2010, 26: 969-975.
  4. Mongasale V, Maskery B, Ochai RL, et al. Burden of typhoid fever in low-income and middle-income countries: a systematic literature based update with risk factor adjustment. Lancet Glob Health, 2014, 2: 570-580.
  5. World Health Organization. Background document: The diagnosis treatment and prevention of typhoid fever. Geneva Switzerland Who Department of Vaccines & Biologicals, 2003, 15(6): 460-463.
  6. Al-Emran HM, Eibach D, Krumkamp R, et al. Multicountry molecular analysis of Salmonella enterica serovar Typhi with reduced susceptibility to Ciprofloxacin in Sub-Saharan Africa. Clinical Infection Diseases, 2016, 62(S1): S42-S46.
  7. Kariuki S, Revathi G, Kiiru J, et al. Typhoid in Kenya is associated with dominant multidrug-resistant Salmonella enterica serovar Typhi haplotype that is also widespread in Southeast Asia. Journal of Clinical Microbiology, 2010, 48: 2171- 2176.
  8. Vlieghe ER, Phe T, De Smet B, et al. Azithromycin and Ciprofloxacin Resistance in Salmonella Bloodstream Infections in Cambodian Adults. PLoS, Neglected Tropical Diseases, 2012, 6(12) : e1933.
  9. Rahman BA, Wasfy MO, Maksoud MA, et al. Multi-drug resistance and reduced susceptibility to ciprofloxacin among Salmonella enterica Serovar Typhi isolates from the Middle East and Central' Asia. New Microbes New Infect, 2014, 2: 88-92.
  10. Ohmani F, Khedid K, Britel S, et al. Antimicrobial resistance in Salmonella enterica serovar Enteritidis in Morocco. Journal of Infection in Developing Countries, 2010, 4: 804-809.
  11. Alambedji RB, Akakpo AJ, Teko-Agbo A, et al. Contrôle des résidus: exemple des antibiotiques dans les aliments au Sénégal. Conférence de l'OIE sur les médicaments vétérinaires en Afrique: Harmonisation et amélioration de l'enregistrement de la distribution et du contrôle qualité. Dakar, Sénégal, 2008, 13 : 25-27.
  12. Ahmed AM, Younis EE, Ishida Y, et al. Genetic basis of multidrug resistance in Salmonella enterica serovars Enteritidis and Typhimurium isolated from diarrheic calves in Egypt. Acta Tropica, 2009, 111: 144-149.
  13. Bodering A, Ndoutamia G, Ngandolo BN, et al. Utilisation des antibiotiques et profil de résistance des souches de Salmonella spp. et Escherichia coli isolées des exploitations avicoles des villes de N'Djaména et Doba au Tchad. International Journal of Biological & Chemical Sciences, 2017, 11(4): 1669-1684.
  14. Muyembe TJJ, Veyi J, Kaswa M, et al. An Outbreak of peritonitis caused by multidrug-resistant Salmonella Typhi in Kinshasa, Democratic Republic of Congo. PLoS, Neglected Tropical Diseases, 2009, 7(1): 40-43.
  15. Lunguya O, Phoba MF, Ahuka SM, et al. The diagnosis of typhoid fever in the Democratic Republic of the Congo. Transactions of the Royal Society of Tropical Medicine and Hygiene, 2012a, 106: 348-355.
  16. Kumel Kumelundu K, Samuel Njoroge, Ronald Ng’etic, et al. Antimicrobial Resistance Profiles of Salmonella enterica subspecie enterica serovar Typhi isolates Associated with Typhoid Fever Epidemics in the Democratic Republic of the Congo, 2002-2014. International Journal of Innovative Science and Research Technology, 2018, 3: 117-124.
  17. Dauvergne E. Détection de gènes de résistance aux antibiotiques dans les bactéries isolées des produits de la mer. Microbiologie et Parasitologie, 2018, hal-02010604.
  18. Cambray G, Guerout AM and Mazel D. Integrons. Annual Review of Genetics, 2010, 44: 141-166.
  19. Vong O, Meyer S and Barraud O. Place des intégrons dans la dissémination de la résistance aux antibiotiques en clinique et dans l'environnement. UMR INSERM, 1092, Faculté de Médecine, Université de Limoges, 2020
  20. Bouvier M. integron cassette insertion: a recombination process involving a folded single strand substrate. EMBO Journal, 2005, 24: 4356-4367.
  21. Gillings MR. Class1 integrons as invasive species. Current Opinion in Microbiology, 2017, 38: 10-15.
  22. Guérin E, Cambray G, Da Re S, et al. The SOS Response Controls Integron Recombination. Science, 2009, 324(5930): 1034.
  23. Deylam SM, Ferdosi SE, Yahyapour Y, et al. Integron-Mediated Antibiotic Resistance in Acinetobacter baumannii isolated from intensive care unit patients, Babol, North of Iran. BioMed Research International, 2017, 2017: 1-8.
  24. Rodriguez V and Struelens MJ. Résistance bactérienne par $beta$-lactamases à spectre étendu. Implications pour le réanimateur. Réanimation, 2006, 15: 205-213.
  25. Beval TC Les Bêta-lactamines. DUCIV Lyon, CH Alpes-Léman, 2016, 47.
  26. Ouedraogo AS. Prévalence, circulation et caractérisation des bactéries multirésistantes au Burkina Faso. Médecine humaine et pathologie, Université Montpellier, 2016.
  27. Cherkaoui A, Emonet S, Renzi G, et al. Bêtalactamases à spectre étendu et carbapénémases chez les Enterobacteriaceae. Revue Médicale Suisse, 2014, 10: 2142-2148.
  28. Sadeeq R, Tariq A, Ijaz A, et al. The Growing Genetic and Functional Diversity of Extended Spectrum Beta-Lactamases. BioMed Research International, 2018, ID 9519718, 1-14.
  29. Franklin C, Liolios L and Peleg AY. Phenotypic detection of carbapenem-susceptible metallo-$beta$-lactamase-producing Gram-negative bacilli in the clinical laboratory. Journal of Clinical Microbiology, 2006, 44: 3139-3144.
  30. Makanera A, Arlet G, Gautier V, et al. Molecular epidemiology and characterization of plasmid-encoded beta-lactamases produced by Tunisian clinical isolates of Salmonella enterica serotype Mbandaka resistant to broad-spectrum cephalosporins. Journal of Clinical Microbiology, 2003, 7: 2940-2945.
  31. Kermas R, Touati A, Brasme L, et al. Charaterization of Extended-Spectrum Beta-Lactam-Producing Salmonella entrica Serotype Brunei and Heidelberg at the Hussein Dey Hospital in Algiers (Algeria). Foodborne Pathogens & Disease, 9(9): 803-808.
  32. IBM-SPSS Statistics, 23.0 step by step: A Simple Guide and Reference, 2016, 14è éd, 0134320255, 9780134320250.
  33. Iyer V, Ravalia A, Bhavsar K, et al. Antimicrobial resistance surveillance in typhoidal Salmonella in Ahmedabad in an era of global antimicrobial resistance surveillance systems. Journal of Global Infectious Diseases, 2019, 11(4): 153-159.
  34. Kariuki S. Typhoid fever in sub-Saharan Africa: Challenges of diagnosis and management of infections. Journal of Infection in Developing Countries, 2008, 2(6): 443-447.
  35. Koffi AR, Ouassa T, Dadie A, et al. Sérotypes et profils d'antibiorésistance de Salmonella suspectées d'origine alimentaire et isolées chez des patients diarrhéiques à Abidjan, Côte d'Ivoire. Médecine d'Afrique Noire, 2012, 59(6): 336-342.
  36. Kashosi TM, Muhandule AB, Mwenebitu DL, et al. Antibio-résistance des souches de Salmonella spp isolées d'hémocultures à Bukavu en RD Congo. Pan African Medical Journal, 2018, 29: 42.
  37. WHO Global Antimicrobial Resistance Surveillance System. Geneva, Report on Antimicrobial Resistance, 2018.
  38. White PA, Mciver CJ and Rawlinson WD. Current status of the aad and dfr gene cassette Families. J Antimicrob Chemother, 2001, 47: 495-502.
  39. Koczura R, Przyszlakowska B, Mokracka J, et al. Class1 integrons and antibiotic resistance of clinical Acinetobacter calcoaceticus-baumannii complex in Poznan Poland. Curr Microbiol, 2014, 69: 258-262.
  40. Peterson RP, Kuchenbaecker K, Walters RW, et al. Genome-wide Association Studies in Ancestrally Diverse Populations: Opportunities, Methods, Pitfalls, and Recommendations. Cell, 2019, 179: 589-60.