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Multidrug-resistant Salmonella enterica, Democratic Republic of the Congo.
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MedLine Citation:
PMID:  23017665     Owner:  NLM     Status:  MEDLINE    
Marie-France Phoba; Octavie Lunguya; Daniel Vita Mayimon; Pantaléon Lewo di Mputu; Sophie Bertrand; Raymond Vanhoof; Jan Verhaegen; Chris Van Geet; Jean-Jacques Muyembe; Jan Jacobs
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Publication Detail:
Type:  Letter    
Journal Detail:
Title:  Emerging infectious diseases     Volume:  18     ISSN:  1080-6059     ISO Abbreviation:  Emerging Infect. Dis.     Publication Date:  2012 Oct 
Date Detail:
Created Date:  2012-09-28     Completed Date:  2013-02-19     Revised Date:  2013-07-11    
Medline Journal Info:
Nlm Unique ID:  9508155     Medline TA:  Emerg Infect Dis     Country:  United States    
Other Details:
Languages:  eng     Pagination:  1692-4     Citation Subset:  IM    
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MeSH Terms
Anti-Bacterial Agents / pharmacology
Bacteremia / epidemiology*,  microbiology
Child, Preschool
Democratic Republic of the Congo / epidemiology
Drug Resistance, Multiple, Bacterial*
Microbial Sensitivity Tests
Salmonella Infections / epidemiology*,  microbiology
Salmonella enterica / classification,  drug effects,  genetics
Salmonella enteritidis / drug effects*,  genetics,  isolation & purification
Salmonella typhi / drug effects*,  genetics,  isolation & purification
Salmonella typhimurium / drug effects*,  genetics,  isolation & purification
Reg. No./Substance:
0/Anti-Bacterial Agents

From MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine

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Journal Information
Journal ID (nlm-ta): Emerg Infect Dis
Journal ID (iso-abbrev): Emerging Infect. Dis
Journal ID (publisher-id): EID
ISSN: 1080-6040
ISSN: 1080-6059
Publisher: Centers for Disease Control and Prevention
Article Information
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Print publication date: Month: 10 Year: 2012
Volume: 18 Issue: 10
First Page: 1692 Last Page: 1694
PubMed Id: 23017665
ID: 3471636
Publisher Id: 12-0525
DOI: 10.3201/eid1810.120525

Multidrug-Resistant Salmonella enterica, Democratic Republic of the Congo Alternate Title:Multidrug-Resistant S. enterica
Marie-France Phoba1
Octavie Lunguya1
Daniel Vita Mayimon
Pantaléon Lewo di Mputu
Sophie Bertrand
Raymond Vanhoof
Jan Verhaegen
Chris Van Geet
Jean-Jacques Muyembe
Jan Jacobs
National Institute for Biomedical Research, Kinshasa, Democratic Republic of the Congo (M.-F. Phoba, O. Lunguya, J.-J. Muyembe);
University Hospital of Kinshasa, Kinshasa (M.-F. Phoba, O. Lunguya, J.-J. Muyembe);
Saint-Luc Hospital, Kisantu, Democratic Republic of the Congo (D.V. Mayimona, P. Lewo di Mputu);
Institute of Public Health, Brussels, Belgium (S. Bertrand, R. Vanhoof);
University Hospital Leuven, Leuven, Belgium (J. Verhaegen, C. Van Geet);
and Institute of Tropical Medicine, Antwerp, Belgium (J. Jacobs)
Correspondence: Address for correspondence: Jan Jacobs, Institute of Tropical Medicine, Nationalestraat 155, 2000 Antwerp, Belgium; email:

To the Editor:Salmonella enterica serotype Typhi and the nontyphoid S. enterica (NTS) are leading causes of bacteremia in sub-Saharan Africa, but little information is available from central Africa (1,2). We describe an epidemic increase of S. enterica bacteremia in Kisantu in southwestern Democratic Republic of the Congo (DRC).

The Hospital of Saint Luc in Kisantu is a 274-bed referral hospital serving a community of 150,000 inhabitants. As part of an ongoing microbiological surveillance study in DRC (3), we identified pathogens grown from blood cultures (BacT/ALERT; bioMérieux, Marcy L’Etoile, France) and assessed them for antimicrobial drug susceptibility (Vitek II system; bioMérieux) (4) and serotype (Sifin, Berlin, Germany). We determined MICs for nalidixic acid, ciprofloxacin, and chloramphenicol using the Etest macromethod (bioMérieux). For salmonella isolates, we defined decreased ciprofloxacin susceptibility as an isolate with an MIC >0.064 mg/L (5) and multidrug resistance (MDR) as co-resistance of the isolate to ampicillin, chloramphenicol, and trimethoprim/sulfamethoxazole (6). Screening for mutations causing decreased ciprofloxacin susceptibility included assessment of the quinolone resistance–determining regions of the gyrA, gyrB, and parC genes and the plasmid-mediated qnrA, qnrB, and qnrS genes (7). Multilocus variable-number tandem-repeat analysis was performed on a subset of 37 S. enterica ser. Enteritidis isolates (8).

The pathogens isolated were S. enterica ser. Typhi (n = 17, 14.4%), Enteritidis (n = 79, 67.0%), and Typhimurium (n = 22, 18.6%). The increased incidence of S. enterica bacteremia was caused by an increased incidence of S. enterica ser. Enteritidis infection from 1 and 2 isolates reported in 2008 and 2009, respectively. The rate of infection by serotypes Typhi and Typhimurium had remained constant during this period.

During September 2010–May 2011, the proportion of pathogens isolated from blood cultures increased to 53.2% (197/370), compared with 19.7% (63/319) and 25.2% (85/328) for 2008 and 2009, respectively (p<0.001). S. enterica isolates represented 59.9% (118/197) of pathogens, compared with 53.3% (70/131) and 30.9% (84/272) for the same months during 2008–2009 and 2009–2010, respectively (p<0.001). Of 118 S. enterica samples isolated, 89 (75.4%) were isolated from specimens from children <5 years old and 17 (15.3%) from children 5–10 years old. Clinical signs and symptoms were nonspecific; malaria and gastrointestinal infection were the leading diagnoses on admission. Data for in-hospital deaths (retrieved for 87 patients) revealed case-fatality rates of 23.0% (17/74) for children <5 years old, compared with 1 in 10 patients 5–10 years old. Because of the retrospective nature of the study, it was not possible to assess population incidence rates, and we had no estimates of the number of children who were referred to the hospital but died before reaching the emergency department. There was no apparent geographic clustering, but the epidemic coincided with the onset of the rainy season, which had started late and had unusually heavy rainfall.

All NTS isolates were MDR; 1 (1.3%) S. enterica ser. Enteritidis and 1 (4.5%) S. enterica ser. Typhimurium isolate had additional decreased ciprofloxacin susceptibility. Most (16/17, 94.1%) S. enterica ser. Typhi isolates were resistant to amoxicillin and trimethoprim/sulfamethoxazole, 4 (23.5%) and 7 (41.2%) were MDR and had decreased ciprofloxacin susceptibility, respectively. Three combinations of resistance genes encoding decreased ciprofloxacin susceptibility were found (Table). No resistance to cefotaxime was observed. Multilocus variable-number tandem-repeat analysis typing of the S. enterica ser. Enteritidis isolates revealed 2 major profiles (differing in 3 tandem repeats in 1 locus) and 3 minor profiles (differing from the major profiles by 1 tandem repeat at 1 and 2 loci, respectively). Considering the long sample period, we concluded that 1 clonal type had caused the infections in which S. enterica ser. Enteritidis was isolated.

A recent literature review of bacteremia reported aggregated data from 16 studies from eastern (Kenya, Tanzania), western (the Gambia), and southern Africa (Malawi, Mozambique) (1). S. enterica ser. Typhi and NTS represented 0–42% and 9%–84%, respectively, of associated pathogens. The study reported that most NTS isolated were of the serotypes Enteritidis and Typhimurium. A sequential occurrence of disease caused by NTS serotypes similar to that in this study was recorded in Malawi (6).

The reservoir of NTS in sub-Saharan Africa remains unclear; person-to-person and zoonotic transmissions have been postulated (1,2). The coincidence of the onset of the epidemic described in this study with the start of the rainy season is a known phenomenon and might be related to increased incidences of malaria and malnutrition (9) and to contamination of the surface waters caused by floods after heavy rainfalls (2).

Case-fatality rates in this study were similar to those reported previously from sub-Saharan Africa, describing mortality rates up to 27% (2), irrespective of the serotype involved. The MDR rates among NTS and among S. enterica ser. Typhi in this study are among the highest reported in sub-Saharan Africa (10). The finding of decreased ciprofloxacin susceptibility among isolates in a rural area in DRC highlights the need for surveillance of antimicrobial drug resistance of S. enterica isolates.


1These authors contributed equally to this article.

The antibiotic resistance surveillance project in RD Congo is funded by Project 2.01 of the Third Framework Agreement between, the Belgian Directorate General of Development Cooperation and the Institute of Tropical Medicine, Antwerp, Belgium. M.-F.P. has a scholarship from the Fondation Delacroix, Tienen, Belgium.

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2. . MorpethSC, RamadhaniHO, CrumpJAInvasive non-typhi Salmonella disease in Africa.Clin Infect Dis. Year: 2009;49:606–1110.1086/60355319591599
3. . LunguyaO, PhobaM-F, MundekeSA, BonebeE, MukadiP, MuyembeJJ, et al. The diagnosis of typhoid fever in the Democratic Republic of the Congo.Trans R Soc Trop Med Hyg. Year: 2012;106:348–5510.1016/j.trstmh.2012.03.00622551639
4. . Clinical and Laboratory Standards Institute Standard institute performance standards for antimicrobial susceptibility testing: twenty-first informational supplement (M100–S21). Wayne (PA): The Institute; Year: 2011
5. . European Committee on Antimicrobial Susceptibility Testing Breakpoint tables for interpretation of MICs and zone diameters [cited 2012 Feb 1]
6. . GordonMA, GrahamSM, WalshAL, WilsonL, PhiriA, MolyneuxE, et al. Epidemics of invasive Salmonella enterica serotype Enteritidis and S. enterica serotype Typhimurium infection associated with multidrug resistance among adults and children in Malawi.Clin Infect Dis. Year: 2008;46:963–910.1086/52914618444810
7. . CavacoLM, HasmanH, XiaS, AarestrupFMqnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serotypes Kentucky and Bovismorbificans of human origin.Antimicrob Agents Chemother. Year: 2009;53:603–810.1128/AAC.00997-0819029321
8. . HopkinsKL, PetersTM, de PinnaE, WainJStandardisation of multilocus variable-number tandem-repeat analysis (MLVA) for subtyping of Salmonella enterica serotype Enteritidis.Euro Surveill. Year: 2011;16:1994221871223
9. . GreenSDR, CheesbroughJSSalmonella bacteraemia among young children at a rural hospital in western Zaire.Ann Trop Paediatr. Year: 1993;13:45–537681645
10. . GrahamSMNon-typhoidal salmonellae: a management challenge for children with community-acquired invasive disease in tropical African countries.Lancet. Year: 2009;373:267–910.1016/S0140-6736(09)60073-819150705

[TableWrap ID: T1] Table  MICs and genetic analysis of Salmonella enterica isolates with decreased ciprofloxacin susceptibility, Democratic Rebublic of the Congo
Serotype MIC, mg/L
No. isolates Mutations
Nalidixic acid Ciprofloxacin
Enteritidis 128 0.094 1 Asp82-Asn in gyrA + qnrB
Typhimurium >256 0.125 1 Asp87-Tyr in gyrA + qnrB
Typhi >256 0.19–0.25 7 Ser83-Phe in gyrA

Article Categories:
  • Letters to the Editor
Article Categories:
  • Letter

Keywords: Keywords: Salmonella, bacteria, outbreak, Democratic Republic of the Congo, multidrug resistance, pediatric, epidemic, bacteremia, antimicrobial resistance.
Keywords: Suggested citation for this article: Phoba M-F, Lunguya O, Mayimona DV, Lewo di Mputu P, Bertrand S, Vanhoof R, et al. Multidrug-resistant Salmonella enterica, Democratic Republic of the Congo [letter]. Emerg Infect Dis [Internet]. 2012 Oct [date cited].

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