Population structure of group B streptococcus from a low-incidence region for invasive neonatal disease

Naiel Bisharat1, Nicola Jones2, Dror Marchaim3, Colin Block4, Rosalind M. Harding5, Pablo Yagupsky3, Tim Peto6 and Derrick W. Crook2

1 Department of Medicine C, Ha'Emek Medical Center, Afula, Israel
2 Department of Microbiology, Nuffield Department of Clinical Laboratory Sciences, John Radcliffe Hospital, University of Oxford, Oxford, UK
3 Departments of Bacteriology and Infectious Diseases, Soroka Medical Center, Faculty of Health Sciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel
4 Clinical Microbiology Unit, Department of Clinical Microbiology and Infectious Diseases, Hadassah-Hebrew University Hospital, Jerusalem, Israel
5 The Oxford Centre for Gene Function, University of Oxford, Oxford, UK
6 The Academic Department of Microbiology and Infectious Disease, John Radcliffe Hospital, University of Oxford, Oxford, UK

Correspondence
Naiel Bisharat
bisharat_na{at}clalit.org.il


   ABSTRACT
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
 
The population structure of group B streptococcus (GBS) from a low-incidence region for invasive neonatal disease (Israel) was investigated using multilocus genotype data. The strain collection consisted of isolates from maternal carriage (n=104) and invasive neonatal disease (n=50), resolving into 46 sequence types. The most prevalent sequence types were ST-1 (17·5 %), ST-19 (10·4 %), ST-17 (9·7 %), ST-22 (8·4 %) and ST-23 (6·5 %). Serotype III was the most common, accounting for 29·2 % of the isolates. None of the serotypes was significantly associated with invasive neonatal disease. BURST analysis resolved the 46 sequence types into seven lineages (clonal complexes), from which only lineage ST-17, expressing serotype III only, was significantly associated with invasive neonatal disease. Lineage ST-22 expressed mainly serotype II, and was significantly associated with carriage. The distribution of the various sequence types and lineages, and the association of lineage ST-17 with invasive disease, are consistent with the results of analyses from a global GBS isolate collection. These findings could imply that the global variation in disease incidence is independent of the circulating GBS populations, and may be more affected by other risk factors for invasive GBS disease, or by different prevention strategies.


Abbreviations: CI, confidence interval; GBS, group B streptococcus; MLEE, multilocus enzyme electrophoresis; MLST, multilocus sequence typing; NT, non-typable; OR, odds ratio; ST, sequence type

The work was done at the microbiology laboratory, Nuffield Department of Clinical Laboratory Sciences, John Radcliffe Hospital, University of Oxford, UK.


   INTRODUCTION
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
 
Over the last three decades, group B streptococcus (GBS) has become the leading cause of neonatal meningitis and septicaemia in North America, western Europe and Australia, causing considerable rates of morbidity and mortality (Baker, 2001; Isaacs et al., 1995; Schrag et al., 2000). The increasing incidence of invasive neonatal GBS disease has prompted measures to reduce its prevalence in the USA (American Academy of Pediatrics Committee on Infectious Diseases and Committee on Fetus and Newborn, 1997), Australia (Isaacs & Royle, 1999), and recently in the UK (www.hpa.org.uk/infections/). Interestingly, reports from many developing countries and some developed countries show rates of invasive neonatal GBS disease that are much lower than those reported from North America (Chong et al., 1993; Mayon-White, 1985; Schuchat, 1995; Stan et al., 2001; Stoll, 1997; Tsolia et al., 2003). An explanation for such variation is not apparent, and has not been systematically investigated. Low rates of GBS carriage among pregnant women have been suggested as a possible explanation, yet reports from developing countries have shown that, despite significant geographical variation in the proportion of GBS carriage, the range of colonization is similar to that identified in North America (Stoll & Schuchat, 1998). Others have speculated that since virulence is associated with a subset of GBS serotype III strains, low maternal carriage of the more virulent GBS serotype III may explain the low rates of invasive neonatal GBS disease (Suara et al., 1994).

Estimates of maternal GBS carriage and invasive neonatal disease from the western world range between 5 and 35 %, and 0·2 and 3·0 per 1000 live births, respectively (Baker, 2001; Embleton et al., 1999; Jeffery & Moses Lahra, 1998; Schrag et al., 2000; Schuchat & Wenger, 1994; Zangwill et al., 1992). The best estimate of invasive neonatal GBS disease in Israel shows an incidence ranging from 0·08 for 1000 live births in the 1980s (Weintraub et al., 1983) to 0·38 per 1000 live births in the late 1990s (Bromiker et al., 2001). A recent report from southern Israel showed a maternal carriage rate of 12·3 %, with an incidence of 0·095 per 1000 live births (Marchaim et al., 2003a).

A possible explanation for such a low incidence of invasive neonatal GBS disease, despite the substantial carriage rate, is that invasive disease may be caused by a few virulent lineages (clones) within the total GBS population, such that measurement of the total GBS colonization rates may be misleading as to the true size of the population at risk. Secondly, virulent lineages may account for a different proportion of the vaginal GBS population in different geographical locations, giving rise to dissimilarities between total GBS colonization rates and disease incidence. Characterizing the population structure of GBS isolate collections from a region with a low incidence for invasive neonatal disease could provide important insights into the epidemiology and pathogenesis of neonatal GBS disease.

Until recent years, multilocus enzyme electrophoresis (MLEE) was applied to study the population structure of many bacterial pathogens; however, with the advent of automated sequencing, MLEE has given way to multilocus sequence typing (MLST) (Maiden et al., 1998). MLST is conceptually similar to MLEE: isolates are characterized by indexing variation based on genetic diversity within neutral genes that are under stabilizing selection, i.e. housekeeping genes. MLST is highly discriminatory, since it detects all the nucleotide polymorphisms within a gene, rather than just those that alter the amino acid composition (nonsynonymous changes), as in MLEE. MLST has become a key molecular technique in the descriptive epidemiology of bacterial pathogens, as it provides much insight into the population biology of some important human bacterial pathogens, including Neisseria meningitidis (Maiden et al., 1998), Streptococcus pneumoniae (Enright & Spratt, 1998) and Staphylococcus aureus (Enright et al., 2000). Analysis of MLST data collected from a global GBS isolate collection showed that a single homogeneous lineage of capsular serotype III GBS (lineage ST-17) was significantly associated with cases of invasive neonatal disease (Jones et al., 2003). The existence of highly invasive neonatal lineages of GBS had been suggested by other investigators (Bohnsack et al., 2001; Musser et al., 1989; Takahashi et al., 1998).

The aim of the present study was to characterize, using MLST, the population structure of GBS isolate collections from maternal carriage and invasive neonatal disease from a low-incidence region for invasive neonatal disease (Israel), and to identify the major lineages involved in invasive neonatal disease in this region.


   METHODS
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
 
Bacterial strains.
The GBS isolates (n=154) were collected from healthy asymptomatic pregnant women in the 35th to 37th week of gestation (n=104), and from invasive neonatal disease (n=50). The carriage isolates (n=104) included 73 isolates that had been obtained during a prospective study conducted between January and October 2000 to determine the maternal carriage rate of GBS in southern Israel, and they have been previously characterized in detail (Marchaim et al., 2003a, b). Another 31 carriage isolates were obtained from northern Israel, where the incidence of invasive neonatal GBS disease is 0·18 per 1000 live births (N. Bisharat, unpublished data). The invasive isolates (n=50) were obtained from multiple geographical locations: southern Israel (n=9); the Hadassah hospitals in Jerusalem (n=25); northern Israel (n=3); and the central governmental laboratories, Ministry of Health, Jerusalem (n=13), representing isolates obtained from invasive neonatal disease from various hospitals around the country during the last 15 years. The ethnic background of the pregnant women (carriage isolates) and neonates (invasive isolates) was similar (data not shown, and Marchaim et al., 2003b), reflecting the multicultural nature of the Israeli population.

Identification of GBS, DNA extraction and MLST.
Methods for identification of GBS, DNA extraction and MLST were carried out as previously described (Jones et al., 2003). Briefly, fragments of 400–500 bp from seven housekeeping genes were PCR-amplified, and sequenced in both directions. The genes used for the MLST scheme are adhP, encoding alcohol dehydrogenase; pheS, encoding phenylalanyl tRNA synthetase; atr, encoding amino acid transporter; glnA, encoding glutamine synthetase; sdhA, encoding serine dehydratase; glcK, encoding glucose kinase; and tkt, encoding transketolase. For each locus, every different sequence was assigned a distinct allele number in order of identification; these were internal fragments of the gene, which contained an exact number of codons. Each isolate was therefore designated by a seven-integer number (the allelic profile), which corresponds to the allele numbers at the seven loci, in the order adhP, pheS, atr, glnA, sdhA, glcK and tkt. These designations conform to the general GBS MLST database. Isolates with the same allelic profile were assigned to the same sequence type (ST), and these were numbered in the order of their identification (ST-1, ST-2, etc.). The data have been deposited in a database accessible at http://sagalactiae.mlst.net. STs were grouped into lineages or clonal complexes using the program BURST (based upon related sequence types) (START version 1.05) (Jolley et al., 2001). Lineages were named according to the predominant constituent ST within the group. STs were grouped into the same lineage if they were identical at five or more loci.

Capsular serotyping was carried out using the latex assay (Statens Serum Institute, Copenhagen, Denmark), as described by the manufacturer's recommendations (Slotved et al., 2003).

Estimation of the invasiveness of lineages and serotypes.
An empirical odds ratio (OR) or invasive ratio was calculated to compare the probability of invasive disease due to individual lineages (clones) or serotypes. The OR was calculated by reference to all the other lineages or serotypes, using a method published elsewhere (Brueggemann et al., 2003; Smith et al., 1993), as follows: OR=(ad)/(bc), where a is the number of invasive A lineages or serotypes, b is the number of carriage A lineages or serotypes, c is the number of invasive non-A lineages or serotypes, and d is the number of carriage non-A lineages or serotypes.

An OR of 1 indicated that the lineage was equally likely to be recovered from invasive disease or from carriage, an OR >1 indicated an increased probability for a lineage (or serotype) to cause invasive disease, and an OR <1 indicated a reduced probability for a lineage (or serotype) to cause invasive disease. ORs and 95 % confidence intervals (CIs) were calculated using SAS (version 8.2; SAS Institute).


   RESULTS
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
 
Genotypes identified
The 154 Israeli GBS isolates resolved into 46 STs. The most common ST was ST-1, accounting for 27 isolates (17·5 %). Other common STs were ST-19 (10·4 %), ST-17 (9·7 %), ST-22 (8·4 %) and ST-23 (6·5 %). These STs accounted for 52·5 % of the whole isolate collection. Twenty-five STs were identified only once in the dataset. Twelve STs were identified among carriage and invasive isolates. ST-1 was found in 22 and 15·4 % of the invasive and carriage isolates, respectively (P=0·36). ST-19 was identified in equal proportions among invasive and carriage isolates (10 and 10·6 %, respectively). ST-17 was identified in 16 % of the invasive isolates, and 6·7 % of the carriage isolates (P=0·08). The characteristics of the genotypes identified in the dataset are shown in Table 1.


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Table 1. Characteristics of GBS isolates according to ST and serotype

 
Capsular serotyping
Serotype III was the most common serotype, accounting for 29·2 % of the isolates (38 and 25 % of invasive and carriage isolates, respectively) (Table 2). Serotypes II and V were equally common, each accounting for 17·5 % of the isolates. Serotype Ia and Ib accounted for 14·3 and 7·1 % of the isolates, respectively. Twenty-one isolates were non-typable (NT; 13·6 %). None of the different serotypes was found to be significantly associated with invasive disease (Table 2). However, serotype II was significantly associated with carriage, with an OR of 0·3, and a 95 % CI of 0·09–0·9.


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Table 2. The invasive ratio (or odds ratio, OR) of the different serotypes

An OR >1 indicates increased invasive disease potential, and an OR <1 indicates decreased invasive potential. None of the calculated ORs was statistically significant.

 
Relationship between lineage, serotype and lineage-specific OR
The 46 STs resolved by BURST into seven lineages or clonal complexes (Table 3). ST-4 and ST-172 could not be assigned to any of the seven lineages. Lineage ST-17, which included ST-17, ST-31, ST-170 and ST-171, was the only lineage found to be significantly associated with invasive disease (OR 3·9, 95 % CI 1·5–10·4) (Table 3), and all its 19 isolates expressed capsular serotype III. No other lineage was found to be significantly associated with invasive disease. Lineage ST-1 was the most prevalent, and its members expressed various serotypes, with serotype V being the most common. Lineage ST-19 was mainly associated with serotype III. Lineage ST-23 and lineage ST-22 were mainly associated with serotypes Ia and II, respectively. Almost two-thirds of the NT isolates belonged to lineage ST-1.


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Table 3. Distribution of the major lineages (clones), serotype identity, and lineage-specific OR

 

   DISCUSSION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
 
MLST data analyses of GBS populations from a low-incidence region for invasive neonatal disease have shown that a single homogeneous lineage, ST-17, was the only lineage found to be significantly associated with invasive neonatal disease. These findings are consistent with data analysis of global isolate collections (Bisharat et al., 2004; Jones et al., 2003).

The most prevalent STs found in the present study were ST-1, ST-17, ST-19, ST-22 and ST-23. Excluding ST-22, these STs were also the most prevalent in the global collection analysis (Jones et al., 2003). Almost two-thirds of the invasive isolates resolved into one of the three major lineages, i.e. ST-1, ST-17 and ST-19 (Table 3). However, only lineage ST-17 (expressing capsular serotype III) was found to be significantly associated with invasive disease (Table 3). The finding that a subset of GBS isolates is significantly associated with invasive neonatal disease has been suggested by others (Bohnsack et al., 2001; Musser et al., 1989). The other major lineage expressing mainly serotype III was lineage ST-19; however, this lineage was not significantly associated with invasive disease. This could suggest that the increased invasive potential of lineage ST-17 is probably independent of the serotype identity.

The calculated invasive ratio for lineage ST-1 (the most prevalent in the dataset; Table 3) was not statistically significant (OR 1·38, 95 % CI 0·6–2·9). This heterogeneous lineage, expressing multiple serotypes, was almost equally represented among carriage and invasive isolates. Analyses of the main homogeneous subset of this lineage, expressing serotype V only, and consisting of 23 isolates, were also not significantly associated with invasive disease (data not shown).

The distribution of the different sequence types and lineages, and the association of lineage ST-17 with invasive neonatal GBS disease are consistent with observation from global isolate collection analysis (Bisharat et al., 2004; Jones et al., 2003). Furthermore, the carriage rate of the hyperinvasive lineage ST-17 among pregnant Israeli women living in the southern part of Israel, where the incidence of invasive neonatal GBS disease is 0·095 per 1000 live births, was 8·2 % (Marchaim et al., 2003a; and data not shown), similar to figures found among pregnant British women living in Oxfordshire, UK, where the incidence of invasive neonatal disease is approximately 10 times higher (0·9 per 1000 live births) than in southern Israel (N. Jones, unpublished data). These findings argue against previous speculations that variation in disease incidence may be attributed to low carriage rates of the more virulent strains (Suara et al., 1994).

Epidemiological data from the developing world reveal inconsistencies in disease incidence, ranging from non-existent (Daoud et al., 1995), low to moderate (Almuneef et al., 2000; Miura & Martin, 2001; Yossuck & Preedisripipat, 2002), to rates similar to those found in the USA prior to the implementation of preventive measures (2–3 per 1000 live births; Ali, 2004). Similar observations are evident in Europe, with disease incidence ranging from 0·26 per 1000 live births in Greece (Tsolia et al., 2003), 0·4 per 1000 in Switzerland (Stan et al., 2001), 0·5–1·15 per 1000 in the UK (Beardsall et al., 2000; Embleton et al., 1999; Halliday et al., 2000; Heath et al., 2004; Moses et al., 1998; Oddie & Embleton, 2002), 1·9 per 1000 in The Netherlands (Trijbels-Smeulders et al., 2002), and 2·4 per 1000 in Spain (Hervas et al., 1993). In view of the similarities in the structure of GBS populations from geographically diverse locations, it is reasonable to postulate that exposure to the organism is similar among pregnant women from the developing and the developed world. Therefore, the observed differences in disease incidence in many developing countries compared with those in most of the developed world are truly intriguing. It has been speculated that these differences could be attributed to differences in clinical disease manifestation (Schuchat, 1999). In the developing world, GBS-related morbidity manifesting as preterm delivery may not be identified as such because infants may not survive to develop confirmed sepsis, while in the developed world the level of care available for preterm infants could allow them to survive and develop full clinical sepsis. Nevertheless, these speculations do not explain the variable incidence within western European countries. It is possible that the relative contribution of other risk factors for invasive GBS disease (i.e. GBS genital inoculum, preterm delivery, premature rupture of membranes, intrauterine fetal monitoring, chorioamnionitis, intrapartum fever, GBS bacteriuria, and low levels of capsular serotype-specific IgG), and prevention strategies for invasive neonatal GBS disease, may differ from one region to another, and may better explain the observed differences in disease incidence.

In conclusion, the population structure of GBS from a low-incidence region for invasive neonatal disease exhibits a similar pattern to those described among globally diverse GBS isolate collections. This could suggest that the global variation in disease incidence may be independent of the circulating GBS populations.


   ACKNOWLEDGEMENTS
 
This work was funded by the Wellcome Trust, grant number 067147/Z/02/Z. N. B. is the recipient of a grant from the Wellcome Trust Travelling Research Fellowships. We thank Raul Colodner (Ha'Emek Medical Center, Afula, Israel) and Dan Miron (Rivka Zeeve Medical Center, Zfat, Israel) for providing bacterial strains.


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INTRODUCTION
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RESULTS
DISCUSSION
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Received 11 December 2004; revised 28 February 2005; accepted 21 March 2005.



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