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Multidrug-resistant Salmonella enterica, democratic Republic of the Congo.

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; bioMerieux, Marcy L'Etoile, France) and assessed them for antimicrobial drug susceptibility (Vitek II system; bioMerieux) (4) and serotype (Sifin, Berlin, Germany). We determined MICs for nalidixic acid, ciprofloxacin, and chloramphenicol using the Etest macromethod (bioMerieux). 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 variablenumber 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 Ty phimurium (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; personto-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.

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.


Marie-France Phoba, [1] Octavie Lunguya, [1] Daniel Vita Mayimon, Pantaleon Lewo di Mputu, Sophie Bertrand, Raymond Vanhoof, Jan Verhaegen, Chris Van Geet, Jean-Jacques Muyembe, and Jan Jacobs

Author affiliations: 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)

[1] These authors contributed equally to this article.


(1.) Mtove G, Amos B, van Seidlein L, Hendriksen I, Mwambuli A, Kimera J, et al. Invasive salmonellosis among children admitted to a rural Tanzanian hospital and a comparison with previous studies. PLoS ONE. 2010;5:e9244. http://dx.doi. org/10.1371/journal.pone.0009244

(2.) Morpeth SC, Ramadhani HO, Crump JA. Invasive non-typhi Salmonella disease in Africa. Clin Infect Dis. 2009;49:606-11.

(3.) Lunguya O, Phoba M-F, Mundeke SA, Bonebe E, Mukadi P, Muyembe JJ, et al. The diagnosis of typhoid fever in the Democratic Republic of the Congo. Trans R Soc Trop Med Hyg. 2012;106:348-55.

(4.) Clinical and Laboratory Standards Institute. Standard institute performance standards for antimicrobial susceptibility testing: twenty-first informational supplement (M100-S21). Wayne (PA): The Institute; 2011.

(5.) European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters [cited 2012 Feb 1] http://www. EUCAST_files/Breakpoint_tables/Breakpoint_table_v_2.0_120221.pdf

(6.) Gordon MA, Graham SM, Walsh AL, Wilson L, Phiri A, Molyneux E, 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. 2008;46:963-9. http://dx.doi. org/10.1086/529146

(7.) Cavaco LM, Hasman H, Xia S, Aarestrup FM. qnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serotypes Kentucky and Bovismorbificans of human origin. Antimicrob Agents Chemother. 2009;53:603-8. http://

(8.) Hopkins KL, Peters TM, de Pinna E, Wain J. Standardisation of multilocus variable-number tandem-repeat analysis (MLVA) for subtyping of Salmonella enterica serotype Enteritidis. Euro Surveill. 2011;16:19942.

(9.) Green SDR, Cheesbrough JS. Salmonella bacteraemia among young children at a rural hospital in western Zaire. Ann Trop Paediatr. 1993;13:45-53.

(10.) Graham SM. Non-typhoidal salmonellae: a management challenge for children with community-acquired invasive disease in tropical African countries. Lancet. 2009;373:267-9. http://dx.doi. org/10.1016/S0140-6736(09)60073-8

Address for correspondence: Jan Jacobs, Institute of Tropical Medicine, Nationalestraat 155, 2000 Antwerp, Belgium; email: jjacobs@
Table. MICs and genetic analysis of Salmonella enterica isolates
with decreased ciprofloxacin susceptibility, Democratic Rebublic
of the Congo

              MIC, mg/L

              Nalidixic                     No.
Serotype        acid      Ciprofloxacin   isolates    Mutations

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
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Title Annotation:LETTERS
Author:Phoba, Marie-France; Lunguya, Octavie; Mayimon, Daniel Vita; di Mputu, Pantaleon Lewo; Bertrand, Sop
Publication:Emerging Infectious Diseases
Article Type:Letter to the editor
Geographic Code:60SUB
Date:Oct 1, 2012
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