ORIGINAL

Niger J Paed 2013; 40 (4): 389 –394

Owobu AC

Sadoh WE

Oviawe O

Streptococcal throat carriage in a

population of nursery and primary

school pupils in Benin City, Nigeria

DOI:http://dx.doi.org/10.4314/njp.v40i4,8

Accepted: 28th April 2013

Abstract Background: Group A

streptococcus (GAS) is a major

cause of mortality in man. Regu-

lar disease surveillance can be

achieved through evaluation of

throat carriage.

Objectives: To evaluate GAS

throat carriage amongst nursery

and primary schools pupils in

Benin City, Nigeria.

Method: This cross sectional

study was carried out between

September and November 2011.

A multistage random sampling

method was used to recruit the

pupils. Throat swabs were ob-

tained for microscopy and Lance-

fied grouping.

primary and 63(14.8%) in nursery

schools. The subjects were aged 2

to 15years and 203(47.7%) were

males. Of the 426 pupils, 123

(28.9%) had positive throat swabs

for β haemolytic streptococcus

(βHS). None of the isolate was

GAS. The isolates were groups C

(

)

Sadoh WE

Department of Child Health,

University of Benin Teaching Hospital,

PMB 1111, Benin City, Edo State,

Nigeria

E-mail: sadohehi@yahoo.com

Tel: +2348028809710

(50.4%),

(11.4%).

D

(38.2%) and

G

Owobu AC

Department of Paediatrics,

Irrua Specialist Teaching Hospital,

Irrua, Edo State, Nigeria

Conclusion: Although βHS throat

carriage rate in this study is high,

there was no GAS isolate. This

may suggest low prevalence of

GAS related diseases in the com-

munity.

Oviawe O

Institute of Child Health,

University of Benin, PMB 1154,

Benin City, Nigeria

Keywords: group A Streptococ-

cus; throat carriage; school chil-

dren

Results: 426 pupils were recruited

of which 363(85.2) were in

Introduction

Previous studies on GAS throat carriage rate have docu-

mented results as high as 19.5₁%₃ amongst asymptomatic

children aged 5 to 15 years. It has also been found

more recently that children less than 5 years of ag₁₄e may

have high throat carriage rates in Southern Israel, con-

trary to previous documentation that GAS pharyngitis

and chronic sequelae are uncommon in children of this

age group. Some authors have reported throat carriage

rates as high as 8.5%₄ and 17.8% amongst infants and

Group A Streptococcus (GAS) is the ninth major infec-

tious cause of deaths in man globally. It causes several

1

invasive illnesses in children including meningitis, septi-

2

caemia and toxic shock. It is one of the three leading

causes of bacteraemia in children aged less than 90 days

2

in developing countries and acco_,₄unts for 15-30% of

3

cases of pharyngitis in children . Its chronic sequelae

are glomerulonephritis, acute rheumatic fever (ARF),

rheumatic heart disease (RHD) and throat carriage. The

majority of deaths from GAS are caused by RHD, ac-

1

toddlers respectively.

5

counting for 233,000 deaths per year globally. Rheu-

In Nigeria, there is a dearth of data on GAS throat car-

riage. Different authors have reported different throat

carriage₁₅r_-₁a₇tes in previous studies ranging from 0% to

matic heart disease is the_,₇greatest contributor to acquired

6

heart disease in Nigeria. On the other hand, post strep-

tococcal acute glomerulonephritis (PSAGN) is the third

most₈common cause of renal disorders in Nigerian chil-

dren.

32.7% ,

The variations in these results, as well as the

fact that none of these studies evaluated throat carriage

in preschool aged pupils highlights the need for a new

study which will include preschool aged children. This

is particularly important as invasive GAS diseases in

this age group may contribute to high underfive morbid-

ity and mortality rates. In an earlier study in 1999 on

streptococcal throat carriage amongst primary school

pupils in mid-western Nigeria, although a prevalence of

9.87% of βHS was obtained, none of the isolates was

GAS. The absence of GAS may reflect a low GAS

The enormous disease burden arising from GAS empha-

sizes the need for active surveillance of the organism.

Such surveillance may be achieved through evaluating

the p_,r₁e₀valence of GAS throat carriage in the commu-

9

nity. The reservoir of acute GAS disease is the carrier

1

1,12

and this emphasizes its public health signifi-

state

cance.

3

90

activity in the study locale in which the prevalence of

RHD is expected to be high.

by a ratio of the total number of pupils in the ten se-

lected nursery (1,238) and primary (7,879) schools

which was 1:6.36. Thus, 410 was distributed into 56

nursery and 354 primary school pupils. The number of

pupils to be selected from each of the twenty schools

was determined by proportion. The school sample size

The present study set out to evaluate the streptococcal

throat carriage rate amongst primary school pupils in

Egor local government area of Edo State, in mid-

Western Nigeria. It further aimed to evaluate the preva-

lence of βHS throat carriage in children less than five

years which is as yet undocumented in the country to the

best knowledge of the researcher.

w a s

d e t e r m i n e d

u s i n g

t h e

f o r m u l a

N2 =^a^x^N¹

n

2

Where: N = number of pupils re-

cruited from a given nursery or primary school, a =

population of index school, n = total number of pupils in

all the selected nursery or primary schools (i.e. 1,238 for

the nursery schools and 7,879 for the primary schools).

Methods

N

1

= sample proportion calculated above (i.e.57

This cross sectional study was carried out in Egor local

government area (LGA) of Edo State of Nigeria. It is

one of the three LGAs that comprise Benin City, the

capital of Edo State. Benin City is a cosmopolitan city

located in the tropical rain forest belt at 122 metres

above sea level. The LGA has ten (10) political wards.

for the nursery schools and 363 for the primary schools).

In each school, one arm of classes was selected ran-

domly from which pupils were selected. The number of

pupils obtained from the chosen arm in a given school

was calculated using the list of pupils in each arm com-

prising of all the classes in the arm e.g nursery 2 had

two classes. The calculated sample size of each school

Ethical clearance was obtained from the Ethics and Re-

search Committee of the University of Benin Teaching

Hospital. Approval for the study was obtained from the

Edo State Universal Basic Education Board. Written

informed consent was obtained from each of the parents/

guardians of all the pupils that participated in the study.

2

(N ) was distributed among the classes by proportion

N3= ^a^x^N²

b

3

using this formula: where N = Class sample size, a =

Class population (all arms), b = Population of all classes

in the school (either nursery or

1

8

The sample size was determined using the formula

2

primary), N = School sample size (as above).

P(1− P)

d

2

n = Z (1−α )/ 2

2

The first pupil was randomly selected from the list of

pupils in that class by balloting. All subsequent pupils

that were recruited were selected using a sampling

interval. The list of pupils in the class arranged alpha-

betically was used as the sampling frame. The selected

pupils were then given a consent form to take to their

parents/guardians.

where n = minimum

2

Z

(1−α )/ 2

sample size,

= 1.96, P = 9.78% which was

the prevalence of streptococcal throat carriage in the

1

7

Benin study. d = 5% or 0.05. A minimum sample size

of 136 was obtained. For better representation of the

population, the minimum sample size was multiplied by

a factor of 3, thus a final sample size of 410 was used.

The study was carried out between September and

November 2011, when schools were in session.

For each selected pupil, with the aid of a proforma,

information on biodata and household number was

obtained. The socio-econo₉ mic class (SEC) was deter-

1

mined by Olusanya et al method. The pupil’s weight

and height were measured using a Seca digital electronic

and Seca portable stadiometer, using standard methods.

The pupils had a complete physical examination in the

school sick bay. Throat swab was obtained after depress-

ing the tongue to expose the oropharynx with a cotton

swab stick rubbed gently on the posterior pharyngeal

wall. Thereafter, the swab stick was returned into its

sterile container and transported in that manner to avoid

contamination. The swabs were obtained between the

hours of 11am and 1 pm. The younger children were

sampled when the parents/caregivers were available at

the close of school to enlist their cooperation.

The study subjects were nursery and primary school

pupils in Egor LGA of Edo State. The pupils who used

mouthwash on the day of examination and pupils who

had antibiotics during the preceding two weeks of the

study were excluded.

Sampling method

A multistage sampling technique was used to select the

schools in the Egor LGA. In the first stage, one nursery

and one primary school were selected by simple random

sampling technique from each of the ten political wards

in Egor LGA. Twenty schools were thus selected com-

prising of 8 private nursery and 2 public nursery

Processing of throat specimens

schools. This was because there were more private than

public nursery schools. The selected primary schools

comprised of four public and six private schools.

The number of pupils to be selected from nursery and

primary schools was the second stage. It was determined

Within two hours of swabbing the throats, the swab

sticks were taken to the laboratory for gram staining and

culture. Growth with clear zones of haemolysis

2

0

indicated beta haemolytic Streptococcus.

3

91

TM

The Lancefield group was determined using PROLEX

74 (33.2%) were female carriers while 49 (24.1%) were

the male carriers, p = 0.04. Table 2 illustrates the distri-

bution of streptococcal throat carriage amongst the

pupils in the study. Most of the carriers 61 (49.6%) were

in the 9-12 years age group while the least 4 (3.3%)

were between 13-15 years of age. Table 2

STREPTOCOCCAL GROUPING LATEX KIT, China,

which identifies Groups A, B, C, D, F and G strepto-

cocci, according to the manufacturer’s recommendations

The cultures and Lancefield grouping were done in

University of Benin Teaching Hospital, Benin City,

Nigeria by a senior laboratory scientist.

Follow-up of subjects

Table 1: Socio-demographic characteristics of the study popu-

lation

Pupils with positive throat swabs were followed up on a

twice-weekly basis for six weeks, looking out for

features of pharyngitis, PSAGN or ARF.

Characteristic

Male

n(%)

Female

n(%)

Total

N(%)

Age group (years)

2

5

9

1

– 4

– 8

– 12

3 - 15

28(6.6)

60(14.1)

113(26.5) 118(27.7)

2(0.5)

34(8.0)

67(15.7)

62(14.6)

127(29.8)

231(54.2)

6(1.4)

Data analysis

4(0.9)

Data were analysed using Statistical Package for Social

Sciences (SPSS) 16.0 (Chicago IL). Student t test was

used to compare the means of continuous variables.

More than two means were compared using one way

ANOVA. Fisher’s exact test and Pearson’s Chi-square

statistical test of significance were used to determine the

associations between throat carriage and the socio-

demographic variables. The level of significance was set

at p < 0.05.

Nursery (n = 63)

Public

Private

Primary (n = 363)

Public

Private

Socio-economic status

High

Medium

Low

10(2.3)

19(4.5)

11(2.6)

23(5.4)

21(4.9)

42(9.9)

105(24.6)

69(16.2)

111(26.1)

78(18.3)

216(50.7)

147(34.5)

64(34.0)

79(42.0)

45(23.9)

69(33.3)

79(38.2)

59(28.5)

133(33.7)

158(40.0)

104(26.3)

Table 2: Distribution of socio-demographic characteristics of

carriers and non carriers

Results

Characteristics of the study population

Characteristics

carriers

Nn(%)

non-carrier

n(%)

p value

0.04

Four hundred and seventy eight pupils were recruited for

the study, of which 52 were excluded because of antibi-

otics use within the preceding two weeks of the study.

Hence, 426 pupils’ data were analysed. There were 203

Males

Females

49(24.1)

74(33.2)

154(75.9)

149(66.8)

Age group (years)

2

5

9

1

High SEC

Middle SEC

Low SEC

– 4

– 8

– 12

3 – 15

18(14.6)

40(32.5)

61(49.6)

4(3.3)

36(31.6)

46(40.4)

32(28.1)

44(14.5)

87(28.7)

170(56.1)

2(0.7)

97(34.5)

112(39.9)

72(25.6)

(

47.7%) males and 223 (52.3%) females. The mean age

of the subject was 8.0± 2.8 (range; 2-15) years. The

mean age of the female pupils 8.1±2.8 years was not

significantly higher than that of the males 8.0 ± 2.7

years, p = 0.72. The mean age of the nursery pupils was

0.15

0.82

3

.4 ± 0.7 (range; 2-5) years while that of the primary

Household size

school pupils was 8.8 ± 2.1 (range; 5-15) years.

<

7

>

7 persons

– 11

11

58(53.7)

43(39.8)

7(6.5)

162(58.3)

103(37.1)

13(4.6)

0.63

There were 363 pupils from the primary schools and 63

from the nursery schools. Of all the pupils, 216 (50.7)

were in public schools and 147(34.5%) in the private

schools. The SEC distribution of the subjects showed

that 133 (33.7%), 158 (40.0%) and 104 (26.3%) pupils

respectively were from high, middle and low SECs. The

socio-demographic distribution by gender of the study

population is shown in table 1. A total of 396 pupils

provided data on their household sizes. The average

Of the 123 carriers, 46 (40.4%) were of the middle SEC

while 32 (28.1%) and 36 (31.6) were of the low and

high SEC respectively, p = 0.82. The prevalence of

throat carriage among the nursery pupils 19 (30.2%) was

higher than in primary school pupils 104 (28.7%). The

difference was not statistically significant, p = 0.80. The

carriage rate was highest 7 (35.0%) amongst pupils from

households with greater than 11 persons and was least

(

2

range) number of persons per household was 7 (range;

-20). 220 (57.0%) of the pupils were from households

with less than 7 persons while 146 (37.8%) and 20

5.2%) were from households with 7-11 persons and

5

8 (26.4%) amongst those from households with less

than 7 persons, p= 0.63. Seventy two (30.4%) of the 237

public school pupils and 51 (27%) of the 189 private

school pupils were carriers, p= 0.357.

(

greater than 11 persons respectively.

Streptococcal throat carriage

Lancefield group of the isolates

Of the 426 pupils, 123 (28.9%) had positive throat

swabs for βHS. Of the 123 pupils with positive isolates,

Of the 123 β haemolytic Streptococci isolated in the

present study, 62 (50.4%) were of group C, 47 (38.2%)

3

92

1

4

were of group D and 14 (11.4%) were of group G. There

were no group A, group B nor group F isolates. The

mean ages of children with Lancefield groups C, D and

G were 8.5 ± 2.7years , 7.6 ± 2.9 years and 7.5 ± 3.5

years respectively and their mean ages did not differ

significantly, p = 0.21.

dren <5 years while Yagupsky et al reported a carriage

rate of 17.8% amongst toddlers in Southern Israel. In

both of these studies, evaluation was only for GAS im-

plying that the overall βHS would likely have been

higher. The high streptococcal throat carriage rate in the

preschool aged children in the present study may be due

to their early exposure to βHS as a result of early patron-

age of day care facilities and nursery₂₃schools by the in-

creasing number of working mothers.

Table 3: Gender and age group distribution of Lancefield

groups

Characteristics

Lancefield group

There was no GAS isolate in this study. This is similar

to the earlier report by Sadoh and Omokhodion in

1

C(%)

D(%)

G(%)

p value

0.19

17

999 where an absence of GAS was similarly noted in

Gender

Male

Female

Age group

28(58.3) 18(37.5)

2(4.2)

the same Egor L.G.A. This is in contrast to all previous

studie₁₃s_,₂₄w_,₂h₅ich isolated GAS strains in India and Fiji Is-

34(45.3) 29(38.7) 12(16.0)

land.

The absence of GAS in the present study

2

5

9

1

- 4

– 8

– 12

3 – 15

5(27.8)

9(50.0)

20(50.0) 16(40.0)

35(57.4) 21(34.4)

4(22.2)

4(10.0)

5(8.2)

may stem from the preferential use of penicillin antibiot-

0.78

ics for the mana₆gement of acute pharyngitis in children

2

29(93.6)

1(3.2)

in Benin City, which is known to reduce the preva-

lence of GAS throat carriage in susceptible individu-

2

7

Follow-up

als. The widespread antibiotic use may also account

for the high group₁₃_,₁D₇_,₂₁f_,o₂₄u_,₂n₈d in this study compared to

None of the pupils in the study with streptococcal isolate

developed symptoms of pharyngitis, ARF or PSGN

during follow-up.

previous studies,

resulting in change in the

microbiota of the throat, favouring the preferential

growth of group D streptococcus over GAS. This is

possible because group D strepto₂c₉occus is mostly

resistant to penicillin antibiotics.

Discussion

A previous study has demonstrated that low carriage rate

in a community is associated with low prevalence of

rheumatic fever and rheumatic heart disease in the same

community. Another study done during an outbreak of

invasive GAS disease in a community showed that the

The present study noted a βHS carriage rate of 28.9%. A

9

simila₅rly high value of 32.7% was reported by Odigwe

1

et al in Calabar. The latter study evaluated only GAS

strains implying that the overall βHS carriage rate would

have been higher. High βHS carriage rates infer that the

burden of disease such as skin infections and invasive

illnesses attributable to₉_,₁β₀ HS in the community under

study may also be high.

clone responsible for the outbreak was prev₀alent

1

amongst throat carriers in the same community. The

throat carriage rate of the GAS clone was significantly

more amongst school children within the o₀utbreak area

1

than amongst those from other localities. These find-

ings support the usefulness of GAS throat carriage as an

index of GAS disease burden (both acute diseases and

chronic sequelae), thus suggesting that the burden of

GAS may be low in the community where the present

study was carried out since throat carriage was absent.

Some other Nigerian studies however reported lower

βHS throat carriage rates. In 1999, Sadoh and co work-

1

7

er reported a βHS₆ carriage rate of 9.8% in Edo State

1

while Ogunbi et al reported a carriage rate of 13.3% in

1

978 in Lagos State. Studies done in other countries

reveal a wide ra₁nge of βHS carriage₁r₃ates including

A predominance of Lancefield group C and G strepto-

cocci as compared to₁₆G_,₁A₇_,₂S₂_,₂₄is consistent with previous

2

.3% in Croatia, 19.5% in South India and 28.5% in

22

8

Lucknow. These rates may reflect the disparity in dis-

ease burden in the different communities during the pe-

riod of the research.

studies in the tropics.

Groups C and G strepto-

cocci have been implicated in pharyngitis and skin

infections and may cause invasive illnesses in man.

2

8

It is of note that the βHS carriage rate in the present

1

7

study is higher than that of Sadoh and Omokhodion

carried out in the same LGA twelve years earlier. A

plausible explanation is that seasonal factors may have

influenced the results as neither study was carried out all

through the year to accommodate seasonal variations in

carriage rate and disease burden. It may also reflect a

change in the epidemiology of βHS in the LGA over the

years. The high βHS throat carriage rate of 29.0%

amongst the nursery pupils in this study is considerable.

Other workers have earlier reported high βHS throat

carriage rates₅ in preschool aged children. In 2002,

Conclusion

The prevalence of streptococcal throat carriage amongst

nursery and primary school pupils in Egor LGA of Edo

State was 28.9%. This high prevalence rate suggests that

the burden of βHS diseases in Egor LGA may be high.

However GAS was not isolated, which implies a likely

low burden of group A Streptococcal diseases and se-

quelae in the study community. This is more so since a

similar study conducted in the same locale over a decade

1

Odigwe et al reported a carriage rate of 45% in chil-

3

93

ago yielded no GAS isolate. The high streptococcal

throat carriage rate amongst pupils less than 5 years of

age suggests similarly high burden βHS activity in the

age group perhaps because of early exposure.

Authors’ contribution

ACO, WES,OO: Data collection, analysis, interpreta-

tion, Conceptualisation and design of the study

ACO, WES: Writing of the initial draft

Considering the enormous disease burden of invasive

and RHD thought to be associated with the country

where the study was done, this may mean a reduction in

prevalence of GAS related diseases. This possible

change in epidemiology needs further evaluation by

conducting similar studies in other parts of the country

to further describe the current epidemiology of GAS

activity.

ACO, WES, OO: Contribution of intellectual input to

the draft, Approval of the manuscript

Conflict of interest: None

Funding: None

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