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Group B streptococcusserotype prevalence in reproductive-age women at a tertiary care military medical center relative to global serotype distribution

  • Danielle L Ippolito1,
  • Wesley A James1,
  • Deborah Tinnemore1,
  • Raywin R Huang1,
  • Mary J Dehart1,
  • Julie Williams1,
  • Mark A Wingerd1 and
  • Samandra T Demons1, 2Email author
BMC Infectious Diseases201010:336

DOI: 10.1186/1471-2334-10-336

Received: 3 June 2010

Accepted: 24 November 2010

Published: 24 November 2010

Abstract

Background

Group B Streptococcus (GBS) serotype (Ia, Ib, II-IX) correlates with pathogen virulence and clinical prognosis. Epidemiological studies of seroprevalence are an important metric for determining the proportion of serotypes in a given population. The purpose of this study was to evaluate the prevalence of individual GBS serotypes at Madigan Healthcare System (Madigan), the largest military tertiary healthcare facility in the Pacific Northwestern United States, and to compare seroprevalences with international locations.

Methods

To determine serotype distribution at Madigan, we obtained GBS isolates from standard-of-care anogenital swabs from 207 women of indeterminate gravidity between ages 18-40 during a five month interval. Serotype was determined using a recently described molecular method of polymerase chain reaction by capsular polysaccharide synthesis (cps) genes associated with pathogen virulence.

Results

Serotypes Ia, III, and V were the most prevalent (28%, 27%, and 17%, respectively). A systematic review of global GBS seroprevalence, meta-analysis, and statistical comparison revealed strikingly similar serodistibution at Madigan relative to civilian-sector populations in Canada and the United States. Serotype Ia was the only serotype consistently higher in North American populations relative to other geographic regions (p < 0.005). The number of non-typeable isolates was significantly lower in the study (p < 0.005).

Conclusion

This study establishes PCR-based serotyping as a viable strategy for GBS epidemiological surveillance. Our results suggest that GBS seroprevalence remains stable in North America over the past two decades.

Background

Streptococcus agalactiae (Group B Streptococcus [GBS]) was first identified as a significant public health concern in maternal fetal medicine in the 1970s. Since this time, more than 7500 cases of GBS-associated neonatal sepsis and meningitis have been reported annually, with a financial burden of more than $350 million per year in neonatal costs [1]. Population-specific surveillance studies provide an important vehicle for evaluating the public health risks posed by changes in distribution of GBS serotypes [2].

Anogenital colonization with GBS is usually asymptomatic in immunocompetent adults [3]. Perinatal transmission of GBS from infected mothers during delivery can cause potentially fatal sepsis and meningitis [4]. Classification of GBS serotype is based on 10 immunologically unique capsular polysaccharides associated with pathogen virulence and encoded in the capsular gene cluster (cps) (Ia, Ib, II-IX) [5]. In the United States civilian population the predominant GBS serotypes are Ia, III, Ib, and V. Current multivalent vaccine development depends on accurate population data of serotype distribution [6]. Thus, epidemiological studies of seroprevalence are important in assessing changes in GBS distribution.

Accurate epidemiological characterization of GBS isolates is dependent on unequivocal classification of serotypes. Molecular methods have improved the accuracy and feasibility of serotyping, but these methods have only recently been applied to large cohorts [7].

Global serotyping distribution studies have documented that the prevalence of a given GBS serotype varies according to geographical location and time of study conductance [2]. Surveillance data in the United States come largely from civilian hospitals, with the Active Bacterial Core surveillance system within the Emerging Infections Program Network providing a mechanism for routine population-based surveillance [8]. Military communities are unique in their demographically diverse population including transients from military bases across the United States and around the world. It is unknown how the geographical mobility of the military might affect GBS seroprevalences in military cohorts.

Madigan Healthcare System (Madigan) is a tertiary care military medical center providing obstetric care to military families, with more than 2100 deliveries reported in 2009. Women between the ages of 18-40 are screened for GBS by urine cultures and vaginal/rectal swabs as standard of care. The objective of this study was to apply a two-tiered polymerase chain reaction (PCR) approach to determine the prevalence and distribution of the GBS serotypes in the Madigan population during the period covering July - December 2009 and to compare Madigan seroprevalences with global distributions.

Methods

Study population

This study was performed with the approval of the Madigan Healthcare System Institutional Review Board. Of the 1129 patients screened during the study period (July 2009 - December 2009), 207 were scored as GBS positive (18.3%). Clinical GBS isolates from these patients were obtained from vaginal/rectal swabs routinely conducted on women of indeterminate gravidity between ages 18-40. GBS isolates were disassociated from any personal health information and assigned a unique study number correlating with the date of specimen collection.

Bacterial culture and banking

GBS isolates were cultured from vaginal/rectal swabs. GBS positive diagnoses were confirmed by conventional morphologic and phenotypic methods. Isolated GBS colonies were obtained taking vaginal/rectal swabs and placing them directly into 5 ml of Lim enrichment broth (Fisher Scientific, Pittsburgh, PA) and grown overnight at 35°C in an 8% CO2 incubator. One microliter loop of culture was quadrant streaked on blood neomycin plates (Fisher Scientific, Pittsburgh, PA) in order to obtain isolated colonies. Single colonies were then inoculated in 5 ml of LB broth and grown overnight under the same conditions stated above. Cultures (700 μl) were placed in 1.5 ml cryovial tubes with 300 μl of 50% glycerol to make glycerol stocks. Samples were then flash frozen with liquid nitrogen and stored at -80°C. Glycerol stocks were streaked overnight onto blood neomycin plates and colonies with a clear zone of hemolysis were selected for PCR amplification.

Serotyping of GBS Isolates

Classification of GBS samples was done by PCR-based restriction fragment length polymorphism (RFLP) capsular typing to distinguish among nine of the ten known GBS serotypes (Ia, Ib, II-IX). We used PCR primers and conditions published by Manning et al (cpsG-F97, cpsL-R200, cpsR8-F40) [9]. These primers were used to amplify DNA fragments using Pure Taq Ready-to-Go PCR Beads (GE Healthcare, Pittsburgh, PA) followed by digestion with DdeI (New England Biolabs, Ipswich, MA) to generate restriction fragments. Digested amplicons were separated on 1.8% agarose gels and analyzed using a Typhoon 9410 variable mode imager (GE Healthcare, Piscataway, NJ). Serotype classification was determined by comparison of the molecular weight banding pattern of the resulting restriction fragment length polymorphisms (RFLPs) with published DNA fragment sizes of the GBS cps gene cluster [9].

Serotyping by multiplex polymerase chain reaction

GBS-specific primers (DLTS) were used to identify those isolates that were nontypeable (NT) by RFLP analysis of the cps gene cluster. Multiplex PCR confirmed serotype classification and serotyped GBS isolates that yielded ambiguous results by the RFLP analysis of the cps gene cluster. Multiplex PCR was performed on single colonies using Pure Taq PCR Ready-to-Go PCR beads using the cps primers and PCR conditions published by Poyart et al [10]. Isolates classified as NT by both methods were serotyped using the primers and methods detailed in Imperi et al [7].

Statistical analysis, systematic review, and multiple comparisons analysis

An a priori power analysis indicated that a minimum of 400 patients should be enrolled in the study, assuming a 20% rate of colonization with 5% error to determine prevalence with a precision (α) of 5% [11]. Based on this estimation, a total of 1129 patients were screened, of which 207 (18.3%) were determined to be GBS positive. To compare the Madigan cohort to the global serotype distributions, a systematic review was conducted of 426 primary literature references evaluating serotype distribution in discrete geographical regions. These studies were identified in a Pub Med keyword search for references reporting population serotyping data for GBS (through February 2010). Studies were excluded if GBS was obtained from normally sterile sites (i.e., blood, synovial fluid, etc.). Studies reporting serodistribution in neonates were likewise excluded. Of the papers surveying predominantly colonized women, we excluded studies predating the emergence of serotype V in the general population. Where raw numbers were available, we confirmed the investigator-reported serotype percentages by our own independent calculations. In two instances, the frequencies we calculated did not match the percentages reported in the article due to obvious typographical errors. We relied solely on data in article abstracts where the full text articles were not written in the English language or if the full text article could not be procured. Meta-data were compiled by calculating proportions of serotype distribution among all GBS-positive diagnoses segregated by geographical region (Table 1). Studies included in the global statistical analysis are presented in systematic review in Table 2 (United States and Canada) [1226] and Table 3 (global data) [11, 2764]. The proportional z-test was used to determine significance between serotype rates of the Madigan cohort and other regions. The statistical significance level was stringently set by the Bonferroni correction method to be p < 0.005.
Table 1

Multiple comparisons analysis comparing the Madigan cohort with global GBS serotype distributions.

  

Serotype Distribution (%)

 

Region

Patients

Ia

Ib

II

III

IV

V

VI

VII

VIII

NT

 

Madigan

207

59

25

25

56

4

35

2

0

0

1

#patients

  

28.50

12.08

12.08

27.05

1.93

16.91

0.97

0.00

0.00

0.48

%

Canada

353

77

35

40

66

5

78

  

1

49

#patients

  

21.81

9.92

11.33

18.70

1.42

22.10

0.00

0.00

0.28

13.88

%

  

0.104

0.512

0.906

0.027

0.918

0.171

   

0.001

p-value

US

7609

2039

618

826

1887

73

1139

26

3

17

869

#patients

  

26.80

8.12

10.86

24.80

0.96

14.97

0.34

0.04

0.22

11.42

%

  

0.642

0.055

0.658

0.511

0.299

0.501

0.364

  

0.001

p-value

Europe

2662

485

329

384

747

98

396

16

16

15

131

#patients

  

18.22

12.36

14.43

28.06

3.68

14.88

0.60

0.60

0.56

4.92

%

  

0.001

0.93

0.407

0.817

0.265

0.492

0.847

  

0.006

p-value

ME, EEu

566

78

24

76

82

17

79

10

7

0

41

#patients

  

13.78

4.24

13.43

14.49

3.00

13.96

1.77

1.24

0.00

7.24

%

  

0.001

0.001

0.709

0.001

0.575

0.363

0.64

  

0.001

p-value

Asia

1521

171

214

132

446

25

266

81

22

48

85

#patients

  

11.24

14.07

8.68

29.32

1.64

17.49

5.33

1.45

3.16

5.59

%

  

0.001

0.502

0.142

0.553

0.987

0.913

0.01

  

0.003

p-value

Africa

260

37

12

22

89

10

82

0

0

0

7

#patients

  

14.23

4.62

8.46

34.23

3.85

31.54

0.00

0.00

0.00

2.69

%

  

0.001

0.005

0.256

0.118

0.349

0.001

   

0.142

p-value

S. Am

113

23

12

28

13

2

6

   

10

#patients

  

20.35

10.62

24.78

11.50

1.77

5.31

0.00

0.00

0.00

8.85

%

  

0.144

0.836

0.006

0.002

0.749

0.005

   

0.001

p-value

Mexico

492

277

 

112

88

     

16

#patients

  

56.30

0.00

22.76

17.89

0.00

0.00

0.00

0.00

0.00

3.25

%

  

0.001

 

0.002

0.009

     

0.057

p-value

Aus, NZ

125

25

24

5

26

4

37

0

 

0

2

#patients

  

20.00

19.20

4.00

20.80

3.20

29.60

0.00

0.00

0.00

1.60

%

  

0.111

0.107

0.022

0.251

0.728

0.01

   

0.655

p-value

NOTE. Bonferroni correction alpha = 0.05/p = 0.005 (two-sided); statistical significance < 0.005 relative to Madigan cohort

Madigan, Madigan Healthcare System; ME, Middle East; EEu, Eastern Europe; S.Am, South America; Aus, Australia; NZ,New Zealand

Table 2

United States and Canada GBS Seroprevalences Relative to Madigan Distribution

       

Prevalence by Serotype (%)

 

Location

Study Interval

Patient Population

Typing method

total # patients

% GBS+

# Total Iso-lates

Iaa

Ib

II

III

IV

V

VI

VII

VIII

NT

Ref

WA (Madigan)

2010

Women

PCR

1129

18.3

207

29

12

12

27

2

17

1

0

0

1

this study

Canada Alberta

1998-2000

Gravidas

OID

NA

NA

118

20

9

9

15

0

28

  

0

20

[15]

Canada Calgary

1998-2000

Gravidas

OID

1207

19.5

235

23

11

13

21

2

19

  

0.4

11

[15]

MA Boston

1999

>94% Women

ELISA

NA

NA

114

25

5

10

24

0

32

0

 

0.9

4

[23]

MA Boston

1962-1963

>90% Women

ELISA

NA

NA

149

46

14

11

22

 

0

  

0

7

[23]

MI

1997-2000

Adults

DB

NA

NA

338

21

12

13

13

1

22

2

0

0.3

12

[20]

MI

1999-2000

Gravidas

LCP

NA

NA

117

18

11

11

19

1

20

2

  

17

[19]

MIc

1999-2000

92% Adults

DB

NA

NA

306

23

12

14

11

3

30

3

0.7

2

1

[12]

MN

1974- 1975

3rd Trimester Gravidas

CP

802

5.6

45

26

13

24

24

     

13

[17]

MN

1993-1999

Adults

NA

NA

NA

138

21

14

16

5

0.7

35

   

9

[24]

OH

2001-2002

Gravidas, urine cultures

LCP

65

2.8

2318

23

4

4

32

2

6

   

30

[21]

OH

2003

  

NA

NA

349

18

9

11

17

 

27

    

[14]

PA Pittsburgh

1993-2002

non pregnant women

IP

NA

NA

2660

34

11

13

25

0.4

15

0.3

0

0.3

2

[16]

PA Pittsburgh

1998-2000

non pregnant women

DB

NA

NA

177b

31

9

15

28

0.6

14

   

3

[22, 26]

TX

1994-1995

Gravidas

AS

546

28

153

24

9

26

24

0

12

   

4

[18]

WA, TX Seattle; Houston

1992-1995

Gravidas

ID

3307

26

856

26

8

18

21

0

21

0.2

  

1

[13]

WV

1999

Females

LA

NA

NA

84

19

13

9

15

4

15

   

9

[25]

a--Ic from earlier studies is grouped with Ia

b--of 270 GBS+ patients, 177 were serotyped

c--mixed population: 267 adults - Michigan, 24 neonates - Houston, TX

Madigan-Madigan Healthcare System, Tacoma, WA

LCP-Lancefield capillary precipitin

OID-Ouchterlony immunodiffusion

DBC-dotblot capsular typing

ID-immunodiffusion with rabbit antisera

IP-immunoprecipitation in agarose

LA-latex agglutination with serotype specific sera

NA-not available

AS-antisera

Table 3

Global GBS Serotype Distribution in Reproductive-Age Adults Relative to Madigan Healthcare System.

       

Prevalence by Serotype (%)

 

Location

Study Interval

Patients

Typing method

# Total Patients

% GBS+

# GBS+ Isolates

Iaa

Ib

II

III

IV

V

VI

VII

VIII

NT

Ref

Madigan, USA

2010

Women

PCR

1129

18.3

207

29

12

12

27

2

17

1

0

0

0.5

this study

Europe

Czech R

2001-2002

Gravidas

IP

586

29.4

172

22

~10

~13

33

0

14

~3

  

1.8

[46]

FranceT

2001

Gravidas

PCR

39

8

500

26

8

8

41

 

18

    

[60]

Germany

1997-1999

Gravidas

EA

NA

NA

146

18

8

15

29

3

13

   

14

[63]

Germany

2001-2003

Gravidas

OID

460

23

104(75)

17

15

21

28

3

16

0

0

0

0

[30]

Greece

2000-2001

Gravidas

LA

1014

6.6

67

19

12

27

22

3

9

3

3

2

 

[58]

Ireland

1998 pub

Women

NA

504

25.6

129

30

 

17

30

1

9

    

[40]

Ireland

1999-2001

Gravidas

IP

NA

NA

20

35

5

0

30

0

20

0

0

0

5

[11]

IrelandD

2003 pub

Gravidac

NA

NA

NA

159

20

19

11

30

2

15

   

4

[32]

Italy P

1993-1995

Gravidas

OID

2300

11.3

260

16

27

22

22

3

5

0

0

5

 

[52]

Italy T

2005-2006

Gravidas

LA

400

18

73

21

7

6

33

8

26

    

[51]

Netherl

1999-2004

Gravidas

LA

NA

NA

92

26

7

13

22

8

15

8

   

[61]

Portugal L

2002-2004

Gravidas

LA

NA

NA

269

16

5

17

22

2

22

0

2

0

14

[44]

Sweden

2005

Women

LA,PCR

1579

25.4

356

11

13

16

24

15

19

0.5

1

0

1

[38]

Sweden

1995-1996

Gravidas

LA, IP

NA

NA

114

13

13

11

32

3

22

   

6

[29]

U.K.

2001-2003

Gravidas

LA

748

21.3

159

26

16

9

26

 

19

   

2

[39]

Eastern Europe/Middle East

Kuwait

2004 pub

Gravidas

AS

847

14.6

124

13

2

8

24

1

22

8

6

0

17

[27]

Iran

2003

Gravidas

NA

110

9.1

1197

          

[49]

Israel

2000

Gravidas

AS

681

12.3

84

18

11

27

20

 

14

    

[43]

Lebanon

2006

Gravidas

 

775

17.7

137

15

7

11

16

1

23

   

29

[53]

Turkey

2000 2001

Gravidas

LA

500

9.2

54

26

4

29

19

2

0

   

20

[34]

UAE

1998-1999

Gravidas

ID

563

10.1

57

21

 

4

18

26

12

   

16

[28]

Asia

IndiaD

1980s

Women

NA

NA

NA

110

 

20

40

30

     

10

[64]

IndiaV

1980s

Women

NA

NA

NA

79

20

41

53

6

      

[64]

Japan

1999-2000

Gravidas

ELISA

48

8.2

583

8

13

8

10

0

6

19

0

27

8

[45]

Japan

1992-2001

Gravidas

IS

   

9

6

2

10

 

9

27

 

32

6

[56]

Japan

1992-1994

Gravidas

E, OID

441

16

71

7

8

0

11

0

4

25

0

36

10

[41]

Korea

2006-2008

Gravidas

LA

2624

8

352

12

10

 

44

 

20

   

2

[42]

Korea

1990-2000

Gravidas

LA

NA

NA

446

10

22

2

37

1

21

4

1

1

1

[59]

Malaysia

2008

Gravidas

LA

NA

NA

200

12

2

6

12

10

19

17

5

2

17

[31]

MyanmarY

1999-2001

Gravidas

CP

226

7.1

14

14

0

36

0

0

36

0

0

0

14

[11]

Taiwan

2000-2005

Gravidas

LA

NA

NA

58

22

9

3

33

0

26

3

   

[61]

PhillipM

1999-2001

Gravidas

CP

200

7.5

15

7

7

27

33

0

13

0

0

7

7

[11]

ThailandBK

1999-2001

Gravidas

CP

400

 

52

17

2

13

17

0

27

0

15

0

8

[11]

Africa

Gambia

1998

Gravidas

AbTyp

136

19.9

27

19

4

26

7

4

37

   

4

[55]

Nigeria

Early 1980s

Women

NA

NA

NA

89

 

12

6

62

     

20

[64]

ZimbabweH

1999-2001

Gravidas

CP

210

11.9

21

10

14

5

24

0

43

0

0

0

5

[11]

Zimbabwe

2000 end

Gravidas

AbTyp

206

31.6

65

11

3

1

42

3

37

   

2

[48]

Zimbabwe

2002 end

Gravidas

AbTyp

  

117

15

5

4

45

5

24

   

2

[47]

South/Central America and Mexico

Argentina

NA

Gravidas

LA

531

3.2

17

          

[57]

Brazil

2003-2004

Gravidas

AS

316

14.6

46

17

24

20

4

7

9

   

17

[54]

Mexico

2000

Gravidas

LA

946

13

123

59

30

6

     

6

[62]

Mexico

2000-2001

Women

LA

  

25

68

4

28

      

[62]

Mexico

1999-2001

Gravidas

LA

691

14

97

62

26

13

      

[36]

Mexico

1988-1998

Gravidas

LA

  

169

44

 

20

30

     

5

[50]

Mexico

 

Gravidas

   

78

68

19

13

      

[36]

Australia/New Zealand

N. Zea

1998-1999

Gravidas

ID; PCR

240

52

22

21

20

6

29

 

20

2

 

2

 

[37]

Australia

1991-1992

Adultsb

LA

  

103

19

19

4

19

4

32

   

1.9

[33]

Italicized countries host US military bases (source: Military.com at http://www.military.com/ )

a--Ic from earlier studies is grouped with Ia

b--genital/urine data only are compiled

c--70% Gravidas

Madigan--Madigan Healthcare System, Tacoma, WA

pub--study publication date; interval not given

LCP-Lancefield capillary precipitin

AbTyp--Antibody typing

OID-Ouchterlony immunodiffusion

DBC-dotblot capsular typing

ID-immunodiffusion with rabbit antisera

IP-immunoprecipitation in agarose

LA-latex agglutination with serotype specific sera

E--ELISA

NA-not available

EA-enzyme extraction

CP-capillary precipitation

Czech R--Czech Republic

FranceT--France (Tours)

IrelandD--Ireland (Dublin) ItalyP--Italy (Perugia)

ItalyT--Italy (Turin)

Netherl--Netherlands

PortugalL--Portugal (Lisbon)

UAE--United Arab Emirates

IndiaD--India (Delhi)

IndiaV--India (Vellore)

MyanmarY--Myanmar (Yangon)

PhilippinesM--Philippines (Manila)

ThailandBK-- (Bankok, Kohn Kaen)

ZimbabweH--Zimbabwe (Harare)

NZ--New Zealand

Results

Four isolates were classified as NT by PCR amplification and DdeI restriction endonuclease digest alone. These isolates were confirmed to be GBS antigen B by GBS-specific primers dlts-F and dlts-R. Isolates were further screened by a multiplex approach to verify CPS serotype [10]. The single isolate not typeable by either method was further screened by GBS IX-specific primers [7], but results were negative. The serotype distribution results of the multi-tiered typing strategies are presented in Figure 1. Our results show that serotypes Ia, III, and V were the most abundant of the screened GBS isolates (28.5%, 27.1%, and 16.9%, respectively), followed by the less prevalent serotypes Ib, II, IV, and VI (12.1%, 12.1%, 1.9%, and 1.0%, respectively). GBS serotypes VII, VIII, and IX were not detected in our population group and one isolate was NT.
https://static-content.springer.com/image/art%3A10.1186%2F1471-2334-10-336/MediaObjects/12879_2010_Article_1316_Fig1_HTML.jpg
Figure 1

Prevalence of GBS serotypes at Madigan Healthcare System July 2009 - December 2009. Serotype was determined for GBS isolates collected from vaginal/rectal swabs from women of indeterminate gravidity at Madigan Healthcare System (Joint Base Lewis-McChord, Washington, USA). Percentages refer to serotype frequency in 207 total isolates screened. Total numbers of patients testing positive for each isolate are listed in parentheses. NT, non-typeable.

A systematic review of the literature compared Madigan seroprevalences with those reported within the rest of the United States (Table 2) and internationally (Table 3). Global proportions were combined by geographical region into a composite multiple comparisons analysis to compare Madigan serotype distributions with the rest of the world (Table 1). Because most studies conducted in Mexico did not segregate serotype I into Ia and Ib, these studies were included in the systematic review (Table 3) but not in the final analysis (Table 1).

Discussion

To determine the serotype of our Madigan population GBS isolates, we used a two-tiered PCR-based approach to identify type-specific capsular polysaccharides (CPS), epidemiologic markers used to classify serotypes according to prevalence for colonization and disease. The most common mechanism for identifying serotypes is serotype-specific latex agglutination analysis, but this method is prohibitively expensive when used on large patient populations [65]. Further, these tests have lower accuracy, and result in numerous NT isolates (Tables 2 and 3). In contrast, the polymerase chain reaction (PCR) based capsular typing techniques used in this study (i.e., RFLP analysis and multiplex PCR) are reproducible, specific, and easy to perform with fewer NT isolates reported [9, 10]. We chose a two-tiered PCR approach, first using a restriction enzyme digest fingerprinting strategy followed by multiplex PCR for serotypes classified as NT by the RFLP methods [9, 10]. There was 100% concordance between the two methods used to screen isolates, confirming accuracy of the classification scheme used in determining seroprevalences at Madigan.

The percentage of NT isolates reported in our study is significantly lower than that reported in international civilian GBS serotype surveillance studies using primarily the serotype-specific latex agglutination method (2-13%; Tables 1, 2, and 3) [6567]. The 0.5% (n = 1 NT isolate) could result from an uncharacterized capsule [68], mutation in the capsular genes [69], or reversible nonencapsular phase variations [70]. Thus, the PCR-based method has proven an effective screening strategy for rapid and effective screening in a military population, and is anticipated to improve typing accuracy in larger cohorts as these methods become more widespread in surveillance studies.

To our knowledge, this is the first GBS serotype surveillance study targeting a population comprised solely of military beneficiaries. The primary mission of infectious disease research initiatives at military operated facilities is to identify and reduce the impact of infectious diseases affecting military populations. In accordance with this objective, this study reports a strikingly similar GBS distribution profile at Madigan relative to United States and Canadian studies (Tables 1 and 2). In comparing seroprevalences in the US with the Madigan cohort, our data suggest that seroprevalences have remained relatively stable in the United States over the past two decades since the emergence of serotype V in the mid-1990s (Table 2). Subtle regional differences in demographic makeup have been reported to affect GBS serodistribution within the same country [31]. Serotypic shifts have been reported in regional distributions in Korean study populations, for example, with a shift in prevalence of serotypes III and V depending on study site [42]. Regional data in early onset invasive GBS strains in neonates in the US indicate that GBS serotypes vary significantly according to study site, with more cases of serotype V reported in New Jersey and New York populations than in Florida, Texas, and Alabama [71]. However, combining study populations by geographical location led to a striking similarity between Madigan and the civilian sector in North America (Tables 1 and 2). It is currently unknown how rapidly seroconversion occurs in the general population. Our data plausibly reflect a stabilization of seroprevalence in the US over the past 15 years. However, very recent data indicate that serotype IV may be increasing in prevalence in the United States (8.4% of the 1160 patients enrolled from 2004 - 2008 in a multi-site United States study) [72].

Relative to global serodistribution studies, our statistical analysis indicates that North American populations have a higher representation of serotype Ia relative to other geographical locations (Tables 1 and 3). Since the emergence of serotype V in the general population, distributions of serotype proportion have shifted to accommodate the rise in serotype V prevalence in recent years in pregnant patients and neonates with invasive GBS disease [73]. Our global surveillance analysis suggests that Africa and South America have significantly greater serotype V representation relative to North American populations (Table 1).

The rate of GBS colonization rate at Madigan is comparable to the civilian-sector United States and Canada but differs from colonization rate reported in global surveillance studies (Tables 2 and 3). Data from the Emerging Pathogens Network places the overall GBS colonization incidence among U.S. women at approximately 10-30% [1, 4]. At Madigan, GBS colonization rate was 18.3% during the study interval. East Asian countries report incidences as low as 0.3-5.9% [42], while African countries such as Zimbabwe report greater than 60% colonization in pregnant patients (Table 3) [74]. Ethnicity could account for some of these differences. African Americans and Hispanic Americans, for example, are GBS-colonized at higher rates than Caucasians [4, 75]. Further, African American heritage is a recognized risk factor for early onset sepsis in neonates born to colonized mothers [1]. Finally, the mode of specimen collection (i.e., vaginal, rectal, or vaginal/rectal) has been reported to vary significantly depending on geographical location [1]. We recognize that mode of collection may bias estimates of global colonization and/or serodistribution.

Besides ethnicity and vertical transmission between colonized mother and neonate, colonization has also been associated with sexual contact and diet [22, 7679]. All modes are relevant to the Madigan population of highly mobile military beneficiaries and could account for the differences in GBS colonization rate observed between the Madigan cohort and the global studies.

Our systematic review and statistical comparison of the Madigan cohort with global epidemiological studies indicates variability in the geographical distribution of GBS serotypes (Tables 1 and 3). Studies with populations originating in Europe, Asia, Africa, Australia, and North and South America have reported significant differences in prevalence and emergence of novel serotypes over time (Table 3). When comparing Madigan seroprevalences with the global distributions, the Madigan cohort most closely resembles studies conducted in the continental United States and Canada (Table 2) [23].

Analysis of Tables 1 and 3 prompts the following conclusions regarding the seroprevalence of GBS in the Madigan cohort relative to international cohorts: (1) Ia is higher in North America relative to the rest of the world; (2) Ia and Ib are considerably higher in Mexico and South America; (3) III is lower in the Middle East and Eastern Europe than North America but higher in Africa and Australia/New Zealand; (4) IV is comparable across continents; (5) V is higher in Africa but much lower in Australia/New Zealand than North American populations; and (6) VI/VIII are most prevalent in Japan while (7) VII is least represented across the globe with occasional isolates reported in the Middle East/Eastern Europe and Asia. Limited population seroprevalance data are available for serotype IX given its very recent emergence in the general population [5, 7]. Given that serotypes III and V (and to a lesser extent Ia) are most commonly associated with late onset neonatal illness, trends in locations such as Korea, Australia/New Zealand, and African countries with proportionally higher III seroprevalences underscore the need for continuing surveillance. An important caveat when interpreting the meta-data is the high NT rate reported in some studies (11.4-13.88%). The molecular methods more accurately assess serotype, potentially biasing the reporting of the serodistribution in the global comparative analyses.

Given the limited data available on GBS transmission [22, 7679], surveillance studies are warranted in military hospitals located in regions reporting unique seroprevalences. Serotypes typical of discrete geographical regions (i.e., VI and VIII) were less prevalent in our Madigan population (Table 1). Serotypes VIII and VI are most prevalent in Japan [41], a country which hosts numerous U.S. military bases and associated military hospitals. However, we report no incidences of VIII and only a small percentage of VI serotypes in our Madigan population. Similarly, neonatal GBS type IV disease has been reported as more prevalent in countries such as the United Arab Emirates than the United States [28]. Interestingly, our serodistribution data indicate that IV is the most stable serotype across all countries in the world, with no statistically significant differences reported (Table 1). Surveillance studies of seroconversion in female military operatives are warranted in military medical facilities located in Japan and the Middle East.

The implementation of CDC guidelines for anovaginal swab screening at 35-37 weeks gestation and subsequent intrapartum chemoprophylaxis in culture-positive individuals has reduced the incidence of GBS disease by 70% [1, 8, 80]. However, more than 25% of women now receive intrapartum antibiotics [81], raising public health concerns over the possibility of increasing antibiotic resistance of other common pathogens affecting neonatal health [2]. Further, although GBS readily succumbs to penicillin regimens, resistance is increasing in antibiotic alternatives such as clindamycin and erythromycin in women with penicillin allergy [82, 83]. One strategy currently underway to combat this problem is the development of multivalent vaccines. Although vaccination efficacy and implementation feasibility remain controversial, understanding serotype distribution as a function of population is recognized as a critical component of vaccine development [6, 84].

Conclusions

In conclusion, the two-tiered molecular approach to GBS serotype analysis proved a viable strategy for assessing GBS serodistribution in the Madigan cohort, with fewer NT isolates than other methods employed in large population serodistribution studies. The ethnic diversity and geographical mobility of the United States military classify the military as a unique epidemiologic unit relative to US regional and global surveillance populations surveyed in our systematic review. However, the serodistributions reported in our study are remarkably comparable to those reported in civilian sector hospitals in the United States and Canada. Significant discrepancies exist between Madigan distributions and global epidemiology. Investigating seroprevalence in US military medical facilities abroad is necessary to determine whether military-specific populations will require specialized risk analysis for emerging GBS pathogens when alternatives to chemoprophylaxis come into clinical practice.

Funding

This project did not receive external financial support.

Abbreviations

GBS: 

Group B Streptococcus

Madigan: 

Madigan Healthcare System

PCR: 

Polymerase Chain Reaction

RFLP: 

Restriction Fragment Length Polymorphism.

Declarations

Acknowledgements

The opinions and assertions contained herein are the private views of the authors and are not to be construed as official or reflecting views of the Department of Defense, or Department of the Army.

We thank Mr. Paul Kulvi, Ms. Nancy Copper, Ms. Barbara Chickering, and SPC Edmond Flores in the Department of Pathology for initial specimen culturing and preparation. We gratefully acknowledge Ms. Cindy Kirker for library consultation and article procurement. We thank Mr. Mike Smith for technical assistance in PCR, bacterial stock preparations. We thank Mr. Troy Patience for statistical consultation and LTC Steven Mahlen and CPT Karen Thomas for critical manuscript review.

Authors’ Affiliations

(1)
Department of Clinical Investigation, Madigan Healthcare System
(2)
Department of Pathology, Madigan Healthcare System

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  85. Pre-publication history

    1. The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2334/10/336/prepub

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