Research Article: Characterization of Invasive Salmonella Serogroup C1 Infections in Mali

Date Published: February 26, 2018

Publisher: The American Society of Tropical Medicine and Hygiene

Author(s): Fabien J. Fuche, Sunil Sen, Jennifer A. Jones, Joseph Nkeze, Jasnehta Permala-Booth, Milagritos D. Tapia, Samba O. Sow, Boubou Tamboura, Aliou Touré, Uma Onwuchekwa, Mamadou Sylla, Karen L. Kotloff, Sharon M. Tennant.


Nontyphoidal Salmonella (NTS) are the leading cause of foodborne infections worldwide and a major cause of bloodstream infections in infants and HIV-infected adults in sub-Saharan Africa (SSA). Salmonella Typhimurium (serogroup B) and Salmonella Enteritidis (serogroup D) are the most common serovars in this region. However, data describing rarer invasive NTS serovars, particularly those belonging to serogroups C1 and C2, circulating in SSA are lacking. We previously conducted systematic blood culture surveillance on pediatric patients in Bamako, Mali, from 2002 to 2014, and the results showed that serovars Typhimurium and Enteritidis accounted for 32% and 36% of isolates, respectively. Here, we present data on 27 Salmonella serogroup C1 strains that were isolated during this previous study. The strains were typed by serum agglutination and multilocus sequence typing (MLST). Sixteen strains were Salmonella Paratyphi C, four were Salmonella Colindale, and two were Salmonella Virchow. Interestingly, five strains were identified as the very rare Salmonella Brazzaville using a combination of serum agglutination and flagellin gene typing. Phenotypic characterization showed that Salmonella Brazzaville produced biofilm and exhibited catalase activity, which were not statistically different from the gastroenteritis-associated Salmonella Typhimurium sequence type (ST) 19. All tested Salmonella Paratyphi C strains were poor biofilm producers and showed significantly less catalase activity than Salmonella Typhimurium ST19. Overall, our study provides insight into the Salmonella serogroup C1 serovars that cause invasive disease in infants in Mali. In addition, we show that MLST and flagellin gene sequencing, in association with traditional serum agglutination, are invaluable tools to help identify rare Salmonella serovars.

Partial Text

Nontyphoidal Salmonella (NTS) are the leading cause of foodborne infections worldwide and a major cause of gastroenteritis and bloodstream infections. Of the 94 million cases and 155,000 deaths attributed to NTS every year worldwide, sub-Saharan Africa (SSA) bears the highest burden with 193–338 disability-adjusted life years per 100,000 individuals, compared with 50 and 67 for Europe and North America, respectively.1 In particular, invasive NTS (iNTS) disease, in which bacteria invade the bloodstream and cause life-threatening disseminated infections, is a leading cause of morbidity and mortality among infants and HIV-positive adults in SSA, with up to a 30% mortality rate.2,3

Of the 27 Salmonella strains that agglutinated with O:6 antisera and which were isolated from the blood of infants and children at l’Hôpital Gabriel Touré, Bamako, Mali, between 2002 and 2014, all were determined to be O:6,7 (serogroup C1) by agglutination with antisera and by MLST (Table 1). Sixteen isolates were identified as S. Paratyphi C (O:6,7;c;1,5), and all were Vi-positive. MLST revealed that although two strains belonged to ST146, the majority (14/16) belonged to the less common ST114.12 Five isolates were serovar Brazzaville (O:6,7;b;1,2) based on O- and H-agglutination. The H-type was confirmed by sequencing the fliC and fljB genes. We were not able to determine the ST as there was no entry for this combination of allele types in the Salmonella MLST database. The combination of alleles for all seven loci tested was identical for all five S. Brazzaville strains (Table 2), indicating that all five isolates of this serovar belonged to the same ST. Finally, four isolates were identified as S. Colindale (ST584) and two as S. Virchow (ST121 and ST755).

The data presented here provide insight into the Salmonella serogroup C1 serovars that cause invasive disease in Mali. The predominance of S. Paratyphi C is particularly intriguing, as this serovar is rarely reported, either in African countries or in industrialized countries such as the United States where only 13 cases were reported between 1995 and 2012. Here, we described the identification of 16 isolates of this serovar from four different areas within Bamako, Mali, over a period of seven years (from 2002 to 2008), suggesting a widespread presence rather than a transient, localized outbreak. Historically, S. Paratyphi C has been associated with metastatic, suppurative infections. However, of the 16 S. Paratyphi C cases, only one had osteomyelitis. We hypothesize that the patients had atypical clinical presentations of S. Paratyphi C because of their immunocompromised status and other comorbidities. Children who are admitted to l’Hôpital Gabriel Touré can have malaria (highly prevalent), HIV (low prevalence), and/or are malnourished (very common). Six patients had malaria and one of these patients also had HIV. Interestingly, the most common ST was ST114, which differs from what Achtman et al. reported after analyzing 51 isolates of S. Paratyphi C from around the world: 34 were ST146 and only 3 were ST114.12 Similarly, the MLST database EnteroBase shows that the majority of S. Paratyphi C strains belong to ST146 (92 strains of 165 isolates deposited in the database).27 The situation in Mali is therefore unusual, both because of the number of cases in the surveillance period and in the distribution of the STs.




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