PMCCPMCCPMCC

Search tips
Search criteria 

Advanced

 
Logo of eidLink to Publisher's site
 
Emerg Infect Dis. 2011 October; 17(10): 1910–1912.
PMCID: PMC3310650

Global Distribution of Shigella sonnei Clones

Abstract

To investigate global epidemiology of Shigella sonnei, we performed multilocus variable number tandem repeat analysis of 1,672 isolates obtained since 1943 from 50 countries on 5 continents and the Pacific region. Three major clonal groups were identified; 2 were globally spread. Type 18 and its derivatives have circulated worldwide in recent decades.

Keywords: Shigella sonnei, molecular epidemiology, global distribution, clones, bacteria, dispatch

Shigella sonnei is the most commonly isolated species among the 4 Shigella species in industrialized countries (1,2). Transmission of S. sonnei across geographic boundaries is frequently linked to international travel and cross-border food trade (3,4). S. sonnei is a monomorphic organism and therefore requires a highly discriminative sequence-based method for investigating its clonal structure and the geographic distribution of clones.

A total of 26 variable number tandem repeats (VNTRs) have been used to type S. sonnei isolates (5). Because VNTRs have a wide range of variability, they are useful markers for investigating clonal relationships among strains that have evolved over different times (6). In this study, we analyzed 1,672 S. sonnei isolates obtained since 1943 from 50 countries on 5 continents (Africa, Asia, Europe, North America, and South America) and the Pacific region by multilocus VNTR analysis (MLVA) to investigate the global epidemiology of S. sonnei.

The Study

Isolates were obtained from 50 countries on 5 continents and the Pacific region (Table A1). Of these isolates, 31 were obtained during 1943–1983 (from Cameroon, Denmark, France, Senegal, and Sweden) and 1,641 were obtained during 1994–2008 from 48 countries. Isolates were lyophilized, kept in stab culture medium, or stored in 15%–20% glycerol at –75°C for long-term storage. The isolates were not repeatedly subcultured before this study. MLVA26, an MLVA assay based on analysis of 26 VNTRs, classified the 1,672 isolates into 620 MLVA26 types. With only 2 exceptions, no common MLVA26 type was shared among isolates from different countries. One isolate from Malaysia (1999) and 2 isolates from Vietnam (2006) shared a common MLVA26 type, and an isolate from Chad and an isolate from France (both isolated in 2007) shared a common MVLA26 type.

The high resolving power of MLVA is primarily caused by highly diverse VNTRs (6). Clustering analysis of the MLVA26 types using a minimum spanning tree (MST) algorithm grouped the 1,672 isolates into 3 large clusters (A, B, and C), 1 small cluster (D), and 1 singleton (E). Each cluster was defined to include MLVA26 types differing at <7 loci among the 26 loci. The 3 large clusters displayed distinct allelic diversity features. Eight loci (SS1, SS3, SS6, SS9, SS10, SS11, SS12, and SS23) had Simpson diversity values >0.5 for >1 of the 3 large clusters (Table). Differences in diversity values >0.3 among the 3 clusters were observed for 9 of the 26 VNTRs. The largest difference was in 2 hypervariable VNTRs (SS1 and SS6). These 2 VNTRs displayed a high degree of allelic diversity in cluster A, but were invariant in cluster B. SS1 was invariant but SS6 displayed a high degree of diversity in cluster C.

Table
Allelic diversity and range of repeats of VNTRs for 3 major Shigella sonnei clonal groups*

Of 1,672 isolates, 66% (1,100) were obtained from patients who acquired infections in Taiwan. Most isolates belonged to an insertion element IS1 interspacer 1 clone (6,7) that had slightly lower diversity values for some VNTRs than diversity values for total isolates obtained from a panel of 620 isolates representing the 620 MLVA26 types. However, a large number of clonal isolates from Taiwan did not affect relative magnitudes of diversity of the 26 VNTRs.

Although highly variable VNTRs are useful markers in distinguishing closely related strains, they are less useful for investigating clonal relationships among strains that have evolved over time (6). MLVA18 profiles, which excluded the data of 8 highly variable VNTRs (SS1, SS3, SS6, SS9, SS10, SS11, SS12, and SS23) from the 26-locus panel, were used to investigate the clonal structure of the isolates. On the basis of 18-locus profiles, 105 MLVA18 types were identified.

A simplified MST was created by analysis of a subset of 200 isolates selected by obtaining 1 MLVA18 type among those identified in each of 50 countries. As shown in the MST (Figure), cluster A was further divided into subclusters A1 and A2 and singleton A3, and cluster C was divided into subclusters C1 and C2.

Figure
Clonal structure of 200 Shigella sonnei isolates. These isolates, representative of the 1,672 isolates analyzed in this study, were selected by obtaining 1 isolate for 1 multilocus variable number tandem repeat analysis (MLVA) 18 type from those identified ...

Cluster A consisted of 46 MLVA18 types, which represented 1,382 isolates obtained since 1943 in 40 countries on 5 continents and the Pacific region (Table A1). Several MLVA18 types within cluster A were widespread. SS18.2 was detected in 23 countries on 5 continents. SS18.2 had 14 single-locus variants (SLVs) at which genotypes differed only at 1 of the 18 loci; 3 (SS18.80, SS18.1, and SS18.60) of the SLVs were detected in 13, 10, and 7 countries, respectively. SS18.2 and its SLVs represented 1,290 isolates obtained in during 1995–2008 from 38 countries on 5 continents. Four MLVA18 types were detected in samples obtained in 1943–1983. These isolates shared identical MLVA18 profiles or differed at 1–2 loci from recently obtained isolates. Subcluster A2 consisted of 4 MLVA18 types found in isolates from Argentina only. Singleton A3, which was found in isolates obtained in Vietnam in 2008, was distantly separate from subclusters A1 and A2.

Cluster B consisted of 12 MLVA18 types representing 75 isolates, which were obtained in 8 countries in Africa, Asia, and Europe. SS18.6 had the highest number of SLVs in cluster B and was detected in 5 countries in Asia and Africa. Five types were detected in isolates obtained in 1943–1974; they shared identical MLVA18 profiles or differed at 1–2 loci from recently recovered isolates.

Cluster C was relatively diverse; it consisted of 44 MLVA18 types, which represented 212 isolates obtained in 21 countries on 5 continents and the Pacific region. SS18.8 had the highest number of SLVs and was found in isolates obtained during 1974–2007 in 8 countries on 5 continents. SS18.4, the largest SLV of SS18.8, was found in isolates from 5 countries on 5 continents. Subcluster C2 consisted of isolates from Argentina obtained in 2002 and Sweden and Denmark in 1943. These isolates emerged in 1943–1974 and were genetically similar to recently obtained isolates. Clusters (clonal groups) A and C were globally spread, and clonal group B was found in countries in Africa, Asia and Europe only.

Cluster D contained 2 isolates obtained in French Guiana and Senegal in 2003. The isolate for singleton E was obtained in Malaysia in 1999.

Conclusions

Genetic analysis using MLVA presented a simple clonal structure for 1,672 S. sonnei isolates obtained since 1943 from 50 countries on 5 continents and the Pacific region. Three large clonal groups were identified; they displayed distinct allelic diversity features, particularly for 2 hypervariable VNTRs (SS1 and SS6). Clonal groups A and C were globally spread. One MLVA18 type (SS18.2) and several of its SLVs were widely distributed over 5 continents in the past 10 years.

Acknowledgments

This study was supported by the Department of Health, Taiwan (grant no. DOH97-DC-2012).

Biography

• 

Dr Filliol-Toutain is deputy director of the National Reference Center for Escherichia coli and Shigella at Institut Pasteur, Paris, France. Her research interests are surveillance of Shigella strains and Shiga toxin–producing E. coli strains circulating in France, detection of outbreaks, surveillance of the circulating serovars, and surveillance of antimicrobial drug resistance.

Table A1

Geographic distribution of Shigella sonnei clones*
Continent and countryYear isolatedNo. isolatesMLVA18 type (no. isolates)
Africa
Algeria2006–20072Cluster A: SS18.60 (1), 80 (1)
Burkina Faso20061Cluster A: SS18.80 (1)
Cameroon1973, 20072Cluster A: SS18.2 (1); cluster C: SS18.102 (1)
Central African Republic20071Cluster A: SS18.60 (1)
Chad20071Cluster A: SS18.1 (1)
Egypt2000, 2002, 20073Cluster A: SS18.2 (2), 80 (1)
Côte d’Ivoire20011Cluster A: SS18.2 (1)
Kenya2003, 20072Cluster A: SS18.45 (2)
Madagascar1998–20076Cluster A: SS18.1 (1), 2 (1); cluster B: SS18.6 (1); cluster C: SS18.4 (1), 8 (2)
Mali2006–20072Cluster A: SS18.60 (2)
Mayotte20041Cluster C: SS18.8 (1)
Morocco2001–20076Cluster A: SS18.1 (2), 2 (1), 42 (1), 87 (1); cluster C: SS18.97 (1)
Nigeria20071Cluster A: SS18. 80 (1)
São Tomé and Principe20081Cluster A: SS18.58 (1)
Senegal1967–200652Cluster A: SS18.2 (36), 14 (6), 15 (5), 59 (1), 66 (1); cluster B: SS18.39 (1); Cluster C: SS18.90 (1); cluster D: SS18.19 (1)
Tanzania20041Cluster C: SS18.4 (1)
Tunisia
2006
1
Cluster A: SS18.15 (1)
Asia
Myanmar20071Cluster A: SS18. 2 (1)
Cambodia2004–20088Cluster A: SS18.2 (1), 3 (5), 64 (1), 65 (1)
People’s Republic of China2003–20076Cluster A: 2 (4), 7 (1), 80 (1)
India2000, 20073Cluster A: SS18.1 (2), 55 (1)
Indonesia2003–200816Cluster A: SS18.60 (15), 85 (1)
Iran2002–200352Cluster A: SS18.1 (21), 2 (25), 62 (1), 63 (1), 66 (2), 80 (2)
Israel1996, 2003, 20073Cluster A: SS18.2 (3)
Malaysia1994–200465Cluster A: SS18.1 (8), 2 (10), 71 (1); cluster B: SS18.6 (17), 35 (1), 36 (1), 38 (1); cluster C: SS18.8 (6), 12 (9), 13 (3), 16 (1), 81 (2), 82 (2), 99 (2); singleton E: SS18.23 (1)
Nepal20072Cluster A: SS18.59 (1), 60 (1)
Pakistan20011Cluster C: SS18.8 (1)
The Philippines20051Cluster B: SS18.37 (1)
Taiwan1996–20081,100Cluster A: SS18.1 (704), 2 (203), 3 (23), 7 (1), 10 (19), 46 (1), 52 (1), 53 (1), 60 (1), 65 (10), 66 (1), 69 (1), 80 (2); cluster B: SS18.6 (22); cluster C: SS18.4 (61), 5 (29), 13 (6), 32 (1), 33 (1), 34 (1), 50 (1), 83 (2), 86 (1), 88 (1), 91 (1), 93 (2), 95 (1), 100 (1), 102 (1)
Thailand2004, 20073Cluster A: SS18.2 (2), 80 (1)
Turkey20021Cluster A: SS18.2 (1)
Vietnam
2004–2008
62
Cluster A: SS18.2 (28), 3 (7), 7 (1), 20 (1), 58 (1), 65 (2), 80 (6); cluster B: SS18.6 (15); cluster C: SS18.96 (1)
Europe
Denmark19431Cluster C: SS18.21 (1)
France1943–200773Cluster A: SS18.1 (5), 2 (17), 26 (1), 41 (1), 54 (1), 58 (1), 59 (1), 60 (3), 61 (1), 67 (1), 68 (1), 80 (4); cluster B: SS18.6 (1), 28 (1), 29 (1), 30 (1), 31 (1), 39 (7), 40 (1); cluster C: SS18.4 (2), 8 (5), 9 (7), 16 (4), 79 (1), 83 (1), 89 (1), 92 (1), 94 (1)
Greece20071Cluster A: SS18.2 (1)
Italy2001–200770Cluster A: SS18.2 (48), 42 (2), 59 (1), 80 (8); cluster C: SS18.9 (8), 79 (1), 101 (1), 103 (1)
Poland20061Cluster A: SS18.1 (1)
Spain20071Cluster A: SS18.2 (1)
Sweden
1943–1947
8
Cluster A: SS18.25 (2); cluster B: SS18.27 (2); cluster C: SS18.9 (1), 22 (1), 104 (1), 105 (1)
North America
Cuba20031Cluster A: SS18.80 (1)
Guatemala20071Cluster C: SS18.16 (1)
Haiti20061Cluster C: SS18.8 (1)
Mexico20071Cluster A: SS18.14 (1)
United States
1995–2007
49
Cluster A: SS18.2 (9), 14 (5), 26 (16), 47 (4), 49 (2), 51 (1), 57 (1); Cluster C: SS18.8 (1), 11 (3), 43 (3), 44 (2), 70 (2)
South America
Argentina2001–200748Cluster A: SS18.1 (10), 2 (4), 48 (1), 58 (1), 66 (2), 72 (2), 73 (1), 74 (1), 75 (2), 76 (2), 78 (1), 80 (9); cluster C: SS18.4 (4), 5 (1), 17 (4), 24 (1), 56 (1), 93 (1)
Brazil20061Cluster C: SS18.98 (1)
French Guiana1998, 2000, 2003, 20064Cluster A: SS18.2 (3); cluster D: SS18.18 (1)
Venezuela
2007
1
Cluster C: SS18.8 (1)
Pacific
New Caledonia19971Cluster A: SS18.77 (1)
Tahiti20071Cluster C: SS18.84 (1)

*MLVA, multilocus variable number tandem repeat.

Footnotes

Suggested citation for this article: Filliol-Toutain I, Chiou C-S, Mammina C, Gerner-Smidt P, Thong K-L, Phung DC, et al. Global distribution of Shigella sonnei clones. Emerg Infect Dis [serial on the Internet]. 2011 Oct [date cited]. http://dx.doi.org/10.3201/eid1710.101486

References

1. Gupta A, Polyak CS, Bishop RD, Sobel J, Mintz ED Laboratory-confirmed shigellosis in the United States, 1989–2002: epidemiologic trends and patterns. Clin Infect Dis. 2004;38:1372–7. doi: 10.1086/386326. [PubMed] [Cross Ref]
2. Kotloff KL, Winickoff JP, Ivanoff B, Clemens JD, Swerdlow DL, Sansonetti PJ, et al. Global burden of Shigella infections: implications for vaccine development and implementation of control strategies. Bull World Health Organ. 1999;77:651–66. [PubMed]
3. Lewis HC, Kirk M, Ethelberg S, Stafford R, Olsen K, Nielsen EM, et al. Outbreaks of shigellosis in Denmark and Australia associated with imported baby corn, August 2007–final summary. Euro Surveill. 2007;12:E071004 2. [PubMed]
4. Ekdahl K, Andersson Y The epidemiology of travel-associated shigellosis–regional risks, seasonality and serogroups. J Infect. 2005;51:222–9. doi: 10.1016/j.jinf.2005.02.002. [PubMed] [Cross Ref]
5. Liang SY, Watanabe H, Terajima J, Li CC, Liao JC, Tung SK, et al. Multilocus variable-number tandem repeat analysis for molecular typing of Shigella sonnei. J Clin Microbiol. 2007;45:3574–80. doi: 10.1128/JCM.00675-07. [PMC free article] [PubMed] [Cross Ref]
6. Chiou CS, Watanabe H, Wang YW, Wang WL, Terajima J, Thong KL, et al. Utility of multilocus variable-number tandem-repeat analysis as a molecular tool for phylogenetic analysis of Shigella sonnei. J Clin Microbiol. 2009;47:1149–54. doi: 10.1128/JCM.01607-08. [PMC free article] [PubMed] [Cross Ref]
7. Chiou CS, Wei HL, Wang YW, Liao JC, Li CC Usefulness of inter-IS1 spacer polymorphisms for subtyping of Shigella sonnei isolates. J Clin Microbiol. 2006;44:3928–33. doi: 10.1128/JCM.01069-06. [PMC free article] [PubMed] [Cross Ref]

Articles from Emerging Infectious Diseases are provided here courtesy of Centers for Disease Control and Prevention