|Year : 2020 | Volume
| Issue : 1 | Page : 23-30
Prevalence and pattern of beta-haemolytic streptococcal throat infections among primary school children in a rural community in rivers state
Department of Paediatrics, Rivers State University Teaching Hospital, Port Harcourt, Nigeria
|Date of Submission||26-Nov-2019|
|Date of Acceptance||29-Jan-2020|
|Date of Web Publication||30-Apr-2020|
Department of Paediatrics, Rivers State University Teaching Hospital, 6-8 Harley Street, Forces Avenue, Old GRA, Port Harcourt
Source of Support: None, Conflict of Interest: None
Background: Group A beta-haemolytic Streptococcus (GABHS) remains a major cause of morbidity and mortality in humans where it causes symptomatic pharyngitis and the non-suppurative sequelae of acute rheumatic fever and post-streptococcal acute glomerulonephritis. Regional evaluation of streptococcal throat infections may be helpful in disease surveillance. The aim of this study was to evaluate the prevalence and pattern of GABHS throat infections among primary school children in a rural community in Rivers State, Nigeria.
Methodology: This cross-sectional study was carried out between May and July 2015 in Emohua local government area of Rivers State, Nigeria. Pupils were recruited using a multistaged random sampling technique. Throat swabs obtained were cultured using sheep blood and sent for microscopy and Lancefield grouping.
Results: A total of 456 pupils aged 6–12 years were recruited, of which 54 (11.8%) had a positive throat culture of beta-haemolytic Streptococcus (BHS). The isolates were Lancefield Groups B (23; 42.6%), A (18; 33.3%), D (9; 19.6%), C (3; 5.6%) and F (1; 1.8%). No Group G BHS was isolated. Age, sex, socioeconomic class, classroom and household overcrowding did not significantly influence the prevalence of BHS throat infections.
Conclusion: The prevalence of BHS throat infections in this rural community was similar to that in the urban areas in Nigeria. There was no significant difference between the prevalence of BHS in symptomatic and asymptomatic pupils.
Keywords: Beta-haemolytic Streptococcus, Group A beta-haemolytic Streptococcus, primary school children, rural community, throat infection
|How to cite this article:|
Wonodi W. Prevalence and pattern of beta-haemolytic streptococcal throat infections among primary school children in a rural community in rivers state. Port Harcourt Med J 2020;14:23-30
|How to cite this URL:|
Wonodi W. Prevalence and pattern of beta-haemolytic streptococcal throat infections among primary school children in a rural community in rivers state. Port Harcourt Med J [serial online] 2020 [cited 2020 Jun 6];14:23-30. Available from: http://www.phmj.org/text.asp?2020/14/1/23/283651
| Introduction|| |
The presence of Group A beta-haemolytic Streptococcus (GABHS) in the human respiratory tract is of major public health importance as the World Health Organization estimates that it causes about 616 million cases of symptomatic pharyngitis annually; over 550 million (89%) of these cases occur in the less developed countries.In addition, the late non-suppurative sequelae of streptococcal pharyngitis, including acute rheumatic fever (ARF) and post-streptococcal acute glomerulonephritis (PSAGN), may follow GABHS-associated pharyngitis, after 1–4 weeks.,,, The high prevalence of acute rheumatic fever (ARF)is particularly of public health concern, especially in developing countries, which carries a substantial burden of the global annual morbidity and mortality of rheumatic heart disease (RHD).,
RHD remains the most common acquired heart disease in Nigerian children and is reportedly responsible for about 35.8%–58% of cases of acquired heart disease.,, Up to two-thirds of the patients with RHD have a history of sore throat some 1–4 weeks before the onset of the disease. In addition, PSAGN is currently the third most common cause of renal disorders in Nigerian children; 32%–66.6% of such cases follow acute streptococcal pharyngitis.,, Clearly, systematic surveillance and a prompt treatment of GABHS pharyngitis, particularly through school-based programmes, are evidently crucial to the primary prevention of RHD and renal disorders due to PSAGN.,,,
GABHS infection refers to the multiplication of the infectious agent within the body. This can result in a carrier or disease state. In the carrier state, the person has an asymptomatic infection that can be transmitted to a susceptible host while the disease is said to be present if the bacteria or immunologic reactions to their presence cause sufficient harm or damage to the person that will manifest with the relevant clinical symptoms and signs. The reservoir of active GABHS disease is the carrier state, emphasising its public health importance.
In Nigeria, there is a dearth of studies on beta-haemolytic Streptococcus (BHS) throat infections, with varying rates being reported (0%–32.7%).,,, These reported previous studies in Nigeria were, however, all carried out in urban communities.,,, Hence, the present study was set up to document the burden of GABHS in a rural community in Rivers State, Nigeria. The enormous disease burden of GABHS emphasises the need for active surveillance, which may be achieved through evaluating the prevalence of GABHS throat infections in a community. GABHS throat infections are usually community acquired, via droplets, thus further emphasising their public health significance.,,,
The present study evaluated the prevalence and pattern of BHS throat infections among primary schoolchildren in Rivers state. It further evaluated this in a rural community, which is yet undocumented in the country to the best knowledge of the researcher.
| Methodology|| |
This study was carried out in Emohua local government area (LGA), situated in the rural part of Rivers State. Most of the inhabitants are peasant farmers, hunters and fishermen. There is generally a lack of industries and basic infrastructures such as pipe-borne water, electricity and good roads. The LGA has 14 political wards divided into two constituencies: 1 and 2.
Ethical clearance was obtained from the Ethics Committee of the University of Port Harcourt Teaching Hospital (UPTH) as well as the Rivers State Ministry of Education. Written informed consent was obtained from the parents/guardians of the participants. A written informed assent was also obtained from each participant.
The sample size was calculated based on the following formula: where n = minimum sample size, e = margin of sample error tolerated at 5% = 0.05, e = 0.0025, z = 1.96 at 95% confidence limit, therefore z = 3.8416 and P = prevalence rate of positive throat culture of BHS among primary schoolchildren in South-South Nigeria, which is 32.7%. Therefore, the minimum calculated sample size was 408.
The study participants were pupils aged 6–12 years attending primary schools within Emohua LGA. Pupils who used mouthwash on the day of sample collection, had received antibiotics in the preceding 2 weeks and whose parents refused to give consent were excluded from the study. The study was carried out between May and July 2015 When the schools were in session.
The stratified multistage sampling method was used to select the pupils for the study. The list of government-approved primary schools in Emohua LGA was used as the sampling frame. The 54 approved primary schools were first stratified into the two constituencies. Constituency one had 30 schools, whereas constituency two had 24 schools, giving a ratio of 5:4.
The schools in each constituency were then stratified into public and private schools. Constituency one had 27 public and three private schools, whereas constituency two had 24 schools, all public schools. Based on the ratio of schools in each constituency, a total of nine schools were selected, five from constituency one (four public and one private) and four public schools from constituency two by simple balloting.
Each school was stratified into six classes (primary one to six). In schools with more than one arm of a class, an arm was chosen by balloting to represent others, whereas in those with only one arm, that arm was chosen. Ten pupils were then randomly selected from each class, using the class register as the sampling frame.
For each selected pupil, a study questionnaire was used to obtain information on his/her demographic characteristics and associated risk factors for BHS throat infection such as sex, age, socioeconomic class (SEC) of the family as well as household and classroom overcrowding. The SEC was determined based on the social classification scheme developed by Oyedeji in 1985, whereby the occupation and educational attainment of the parents were used to determine the socioeconomic index scores of the pupils. Household overcrowding was defined as more than five persons sleeping in the same room with the child, whereas classroom overcrowding was defined as more than 35 pupils in a classroom.
The study questionnaire also assessed the clinical status of the pupils using the McIsaac's streptococcal score, which considers the possibility of a sore throat being caused by GABHS in children aged 6–12 years. The questionnaire was also designed to elicit the history of recent illness and use of antibiotics in the 2 weeks preceding the study. For the purpose of this study, the clinical feature suggestive of BHS throat infections was defined as the presence of sore throat.
Collection and processing of throat swab specimens
The throat was examined next by asking the child to slightly tilt his/her head back and open the mouth as wide as possible while saying 'aaah'. This usually exposed the tonsils, but in addition, a spatula was used to further expose the tonsils in some children, and a pen torch was used for more lighting. A pre-labelled sterile swab stick was introduced into a well-exposed mouth with the tongue depressed by a wooden spatula, where necessary. The pharynx and the tonsils were swabbed, while contact with the teeth, tongue and gum was avoided. The swab stick was immediately placed in the Amies transport media 108C (Copan Transystem™, Brescia, Italy), which ensures viability of the organism for up to 8 h at room temperature or 72 h if refrigerated at 2°C–8°C. At the end of swab collection each day, all swab sticks in the transport media were sent to the Medical Microbiology Laboratory, UPTH, where they were analysed within 2 h of arrival.
In the laboratory, each swab was plated on 5%–7% sheep blood agar in a Petri dish. Identification of BHS was made based on standard microbiological techniques which included identifying the presence of clear zones of haemolysis.,,,,, Thereafter, Gram staining was done with BHS identified as round organisms in chains that retained the crystal violet colour of the primary stain.,,,, The Lancefield grouping of the BHS isolated was determined using the IMMULEX™ Streptococcus Group KIT (REF 73265, Lot group TL3, expiration date 2017-08-01) produced by Statens Serum Institut Diagnostica, Hillerod, Denmark. This Streptococcal Latex Group kit identifies Lancefield groups A, B, C, D, F and G by introducing antibodies to the group-specific streptococcal carbohydrate antigen, resulting in a visible agglutination reaction. The culture, Gram staining and Lancefield grouping were done by a senior laboratory scientist and the researcher at UPTH microbiology laboratory.
Classification and follow-up of the pupils
The pupils with positive throat cultures were grouped into two categories: symptomatic and asymptomatic. The symptomatic group consisted of those pupils with complaints of sore throat, whereas the asymptomatic group consisted of those without sore throat. Each child in the symptomatic group with a positive culture of BHS was promptly given a referral letter to the closest government hospital for prescription of antibiotics and further investigations.
Data from the study were collated and analysed using the Statistical Package for Social Sciences version 21.0 developed in 2012 by IBM (International Business Machines) Corporations in Armonk, New York, USA. Chi-square test, or the Fishers' exact test, was used, as appropriate, to test the significance of the association between the prevalence of BHS and the risk factors of age, sex, SEC, household overcrowding and classroom overcrowding. Means were compared using Student's t-test and proportions using Chi-square test or Fisher's exact test, as appropriate. In all cases, P < 0.05 was considered statistically significant.
| Results|| |
Characteristics of the study population
A total of 497 pupils were initially recruited for the study. Forty-one (8.2%) pupils were subsequently excluded because they had had antibiotics within the 2 weeks preceding the study. Thus, 456 pupils were ultimately studied. Of the 456 pupils, 221 (48.5%) were male, whereas 235 (51.5%) were female, giving a male: female (M:F) ratio of 1:1.1. The ages of the pupils ranged from 6 to 12 years, with a mean age of 9.40 ± 1.83 years. The mean age was 9.43 ± 1.85 years for males and 9.37 ± 1.81 years for females. The difference in the mean age of males and females was not statistically significant (t = 0.35, P = 0.727). Forty-one (9.0%) pupils belonged to the upper SEC, 277 (60.7%) to the lower SEC, whereas the remaining 138 (30.3%) belonged to the middle class. Of the 54 classrooms in the nine schools from where pupils were surveyed, 12 (22.2%) were overcrowded. The number of pupils per classroom (mean ± standard deviation; range) was 28.2 ± 7.3; 15–50 pupils. Of the 456 pupils recruited, 299 (65.6%) lived in overcrowded household, whereas 157 (34.4%) were from households which were not overcrowded.
Prevalence of positive beta-haemolytic Streptococcus throat culture
Fifty-one (12.5%) of the 408 pupils from public schools had a positive culture compared with 3 (6.3%) of the 48 pupils from the private school. The difference was not statistically significant (χ = 1.61, P = 0.205). Of the 214 pupils aged 6–9 years, 25 (11.6%) had BHS isolates, compared with 29 (11.9%) pupils aged 10–12 years. This difference was not statistically significant (χ = 0.01, P = 0.920). Among the 221 males, 28 (12.7%) had a positive culture, whereas among the females, 26 (11.1%) had a positive culture. This difference was not statistically significant (χ = 0.28, P = 0.596). The culture was positive in 34 (12.3%) of the 277 pupils from the lower SEC, compared with 20 (11.2%) of the 178 from the middle SEC. Only one (2.4%) of the 41 pupils from the higher SEC had a positive culture. This difference in prevalence between SEC was not statistically significant (χ = 3.95, P = 0.139). Thirty-nine (13%) of the 299 pupils from households with overcrowding versus 15 (9.6%) of the 157 pupils from non-crowded homes had a positive culture. The difference was not statistically significant (χ = 1.20, P = 0.273). Of the 40 pupils sampled from overcrowded classrooms, 4 (10.0%) had positive BHS cultures compared to the 50 (12.1%) of the 416 pupils whose classrooms were not overcrowded. The difference was also not statistically significant (Fisher's exact test = 1.00, P = 0.705).
Of the 37 symptomatic children with a sore throat, 2 had a positive throat culture for BHS, giving a prevalence of 5.4%. Of the 419 asymptomatic pupils without a sore throat, 52 pupils had a positive throat culture and the prevalence was 12.4%. The difference in the prevalence of positive throat culture in the symptomatic pupils, compared with the prevalence in the asymptomatic pupils, was not statistically significant (χ = 1.60, P = 0.206).
Lancefield group of the isolates
Lancefield Groups A and B made up 76% of the isolates. as shown in [Figure 1]. No group G BHS was isolated.
|Figure 1: Distribution of Lancefield groups of beta-haemolytic Streptococcus isolates in the study|
Click here to view
| Discussion|| |
The prevalence of BHS among primary school children in the present study was identified as 11.8%. The result of the current study is comparable to the prevalence of 13.3% reported earlier by Ogunbi et al. in Lagos. Although the Lagos study had a commendably large sample size of 12,755, collected over a 3-year period and was conducted about three and a half decades before the current study, comparable prevalence values were recorded in both studies. It is possible that similarities in the age of the study participants, as well as the use of similar methods of identification of BHS, might have accounted for this observation.
The result of the current study is also comparable to the 9.8% prevalence rate reported by Sadoh and Omokhodion in Benin City. This is not surprising considering the similarities in the age of the participants studied, the similar sample size as well as the geographical proximity of the study area in the South-South geopolitical zone of Nigeria.
Evidently, this burden of BHS throat carriage is lower than the 28.9% obtained earlier by Owobu et al. in Benin City. In addition, the prevalence of BHS carriage in the present study is evidently lower than the corresponding value of 32.7% recorded in Calabar. Although all these studies used similar methods of identification of positive BHS throat culture, the studies in Benin and Calabar included children aged <6 years. Odigwe et al. had earlier reported the highest prevalence of positive BHS throat culture in children below 5 years, whereas Owobu et al. had reported a high contribution of about 30% of the total prevalence in the same age group. Our current study did not however include under-five children. This may have accounted for the difference between the overall prevalence of BHS throat culture positivity.
In the present study, the highest age prevalence was recorded among those aged 10–12 years. This is similar to the reports of a peak age of 11 years seen earlier by Nandi et al. in South India and 9–12 years' peak age by Sadoh and Omokhodion in Benin City. The comparable demographic characteristics of these developing nations may account for the current similarities in the peak prevalence of BHS throat colonisation. In addition, with increasing age, the pupils mixing freely with other pupils and making more stable friends in school, a more prolonged contact with infected person(s), was a plausible explanation for the similarities in the peak age prevalence of BHS colonisation. Again, the methodology-related (logistic) exclusion of under-five pre-schoolchildren may have accounted for this observation. However, a possible reason for the high prevalence rate in these 'young children in school' may be their early exposure to BHS as a result of early patronage of day-care facilities in contemporary times. It is also possible that a higher chance of infections could result from a greater exposure from increased contact in day care and indeed, a lower immunity occasioned by age.
With regard to the gender-related distribution of BHS colonisation, a higher prevalence was recorded among males in the present study, as was the case in the studies by Tewodros et al. in Ethiopia, Noel et al. in Grenada and Shrestha et al. in Nepal. The naturally higher level of activity of males at school age, coupled with an increase in the number of social contacts, could account for this observation.
Although the present study did not show a significant association between SEC and the prevalence of BHS, the BHS colonisation was higher among pupils with lower SEC. This was similar to the findings by Owobu et al. in Benin City, Nigeria, and Nandi et al. in Chandigarh, India. The higher BHS prevalence in the low SEC could be ascribed to possible overcrowding and poor sanitation both at home and in school.
Furthermore, the reason for the absence of a significant difference between BHS prevalence rate and SEC of pupils in the current study may be ascribed to the apparently small number of pupils from the upper SEC in the present study.
With regard to other domestic variables, household overcrowding did not affect the prevalence of positive BHS throat culture in the present study. Whereas this study used the number of persons sleeping in a room as the index in its definition of overcrowding in the household, the study by Owobu et al. and Saleh used the number of persons in a household/family as the index, while the number of rooms irrespective of the number of persons in the household constituted the 'yardstick' for defining overcrowding by Factor et al. These differences in the defining criteria would make a valid comparison of the results of the present study with those of earlier ones difficult. However, for a better comparison between studies, an international definition of household overcrowding in developing countries is required.
Classroom overcrowding, which also constitutes an important risk factor for the transmission of BHS, did not appear to influence BHS prevalence in the present study. This is at variance with the findings in reports by Emel et al. in Istanbul, as well as with that of Sadoh and Omokhodion in Benin City. This difference could be accounted for by the higher number of pupils per class in the report by Emel et al., as was the case for the earlier finding by Sadoh and Omokhodion. Unlike the present study in which the average number of pupils in a class was 28, the corresponding average number of pupils in the earlier reports, was 43.
There was no significant difference between the rate of isolation of BHS from symptomatic and asymptomatic pupils in the present study. This is similar to what was found in Tunisia. The exposure of these children to similar pathogens and, indeed, the comparable environmental risk factors, may account in part for this observation. The asymptomatic pupils, also known as carriers, may, however, pose formidable public health challenges, as they constitute an important pool for the transmission of BHS to other pupils. Indeed, these asymptomatic carriers may also develop one or the other of the non-suppurative sequelae of RHD or PSAGN, despite the absence of antecedent pharyngitis symptoms. As regards the findings with respect to symptomatic pupils, the rate of isolation of BHS of 5.4% from pupils with sore throat in this study was lower than that obtained earlier by Odigwe et al. The difference in the isolation rates could be accounted for by a high prevalence among the under-five children in the study by Odigwe et al. as previously discussed.
Lancefield Group B Streptococcus (GBS) and GABHS were the most frequently isolated in the current study. Furthermore, the fact that GBS accounted for 42.6% of the total BHS isolates underscores the significant contribution of GBS as an important throat flora. Indeed, this group of streptococci (GBS) constituted the single-most important potential bacterial agent of BHS-associated pharyngitis and its sequelae in this rural study population. In addition, the proportion of GBS among the isolates is higher in the present study than in those of earlier studies in Nigeria., In those earlier reports,, GBS accounted for 0.9% and 6%, respectively, of the total isolates. The comparatively poorer domestic sanitation in rural areas,,, could possibly enhance the transfer of the organism from the anal region, and hence the higher prevalence recorded in the present study. It may also be implied that in Rivers State, GBS is indeed the peculiar variant of Streptococcus associated with pharyngitis. Further studies are, however, required to confirm this finding. In the Western world, GBS remains the dominant Gram-positive agent of neonatal sepsis.,, Furthermore, the high proportion of GBS in the present study may suggest that GBS could be an important potential contributor to neonatal sepsis in the study locale.
The 33.3% proportion of GABHS among the isolates in the present study is higher than the 14.7% by Emel et al. in Istanbul. It was also higher than the 22.8% rate in Lagos by Ogunbi et al. and the 32.7% rate by Odigwe et al. in Calabar. It is noteworthy that two earlier studies in Benin, Nigeria (by Sadoh and Omokhodion, as well as Owobu et al.), did not isolate GABHS, presumably because human blood, as against sheep's blood, was used in the agar preparation. It is also possible that the consistent paucity of GABHS in the Benin locality may be due to a truly low carriage rate of the pathogen. With the high proportion of GABHS in the present study, it is possible that the prevalence of its sequelae such as PSAGN, ARF and RHD may be high in the locality. Ujuanbi et al. have recently reported a higher RHD prevalence of 6.5/1000 students among primary schoolchildren in Rivers State as against the 0.08/1000 prevalence reported earlier by Ogunbi et al. in Lagos. The present study was, however, not designed to address the subsisting disease burden of RHD and PSAGN. Hence, the need for further studies to address the issue of the disease burden of RHD and PSAGN is self-evident.
Group D BHS was isolated in the present study as well as in a previous study by Owobu et al. in Benin City. Group D BHS, although a normal flora of the human gut and commensal in the pharynx, has been implicated in nosocomial infections and community-acquired infections, especially urinary tract infections in children.,,, While the reason (s) for the high contribution of Group D BHS in the current study as well as in earlier Nigerian studies remain(s) unclear, this observation may indeed be indicative of a truly high burden of Group D streptococcal disease, or perhaps its importance as a commensal in the study locale.
In the present study, the proportion of Group C BHS was relatively low when compared to the earlier reported 27.7% by Ogunbi et al., 38% by Sadoh and Omokhoidion and 50.4% by Owobu et al. It is, however, noteworthy that Group C BHS had earlier been categorised as one of the most common BHS isolated in the tropics, including Nigeria.,, The same 'variant' of BHS has also been implicated as a common cause of pharyngitis. Hence, its lower prevalence in the current study may suggest a low burden of Group C BHS-associated morbidities including pharyngitis. Group F BHS was also isolated in the present study, as was the case in the study by Sadoh and Omokhoidion. Group F BHS was distinctly an uncommon isolate, as was the observation in some earlier Nigerian studies., However, as Group F BHS rarely affects human, its finding in both studies appears to suggest that it may indeed be a true commensal. Clearly, more studies are needed to unveil the reason(s) behind its isolation. With regard to Group G, its absence in the current study is at variance with those of some earlier studies.,, In addition, the paucity of this (streptococcal) group in the present study may suggest that the burden of Group G BHS diseases is truly low in the study community.
Finally, the present study has shown a high prevalence of BHS throat infections in a rural community of Rivers State, Nigeria, with the most prevalent Lancefield group type being Group B BHS. It can also be validly deduced from the present study that the symptomatic streptococcal throat infection rate was lower than the asymptomatic carriage rate in the study population. Age, sex, SEC, household overcrowding and classroom overcrowding did not appear to have influenced BHS throat infections in the present study.
Limitations of the study
- Some of the data in the study such as the history of sore throat and antibiotic use were based on information by parents and guardians of the pupils, with the well-known limitation of recall-related bias. Obviously, recruiting a child who had had antibiotics in the study would most likely give a negative throat culture result, thereby reducing the number of culture-positive results. On the other hand, parents/guardians forgetting to give the history of sore throat would have misled the researcher to a wrong classification of the pupil as asymptomatic
- Viral studies could not be carried out on those children with a sore throat.
| Conclusion|| |
The prevalence of BHS throat infections among primary school children in a rural area of Rivers State is 11.8%, and this is comparable to what was obtained in some urban areas. Group B BHS is the most prevalent Lancefield group in primary schoolchildren in the rural study population of Rivers State, Nigeria. Lancefield Group G BHS is a rare throat isolate in primary school children (asymptomatic or otherwise) in the rural study population of Rivers State, Nigeria.
Age, sex, SEC, classroom overcrowding and household overcrowding did not significantly influence the prevalence of BHS in the throats of primary schoolchildren in the rural study population of Rivers State. There was no significant difference between the prevalence of positive BHS throat culture among symptomatic and asymptomatic pupils.
The Author would like to thank Dr. Nneka Dublin-Green, Dr. Onyinyechi Amadi, Dr. Victor Abel, Dr. Ihundah Etitinwo, Dr. Kelechi Udochu and Dr. Elizabeth Ogbuagu without which the field work would have been overwhelming.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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