- Research note
- Open Access
Asymptomatic pharyngeal carriage rate of Streptococcus pyogenes, its associated factors and antibiotic susceptibility pattern among school children in Hawassa town, southern Ethiopia
BMC Research Notes volume 12, Article number: 564 (2019)
The aim of this study was to determine the asymptomatic pharyngeal carriage rate of S. pyogenes, antimicrobial pattern and related risk factors among school children in Hawassa, southern Ethiopia.
Out of 287 school children’s screened, 35 (12.2%) were colonized with S. pyogenes. The carriage rate was significantly associated with factors such as sex (female p = 0.013) occupational status of mother (p = 0.002), lower income source (500–900 ETB, 1000–1500 ETB) (p = 0.001, and p = 0.042), history of hospitalization (p = 0.00) and residence of the children (p = 0.002). High level resistant to tetracycline and low level to vancomycin were observed, while penicillin, amoxicillin, erythromycin, chloramphenicol, and ceftriaxone were found to be effective.
Streptococcus pyogenes (S. pyogenes) is a species of gram positive, aerotolerant, beta-hemolytic bacterium in the genus Streptococcus. It is classified as Lancefield Group A Streptococcus (GAS). S. pyogenes has continued as a significant human pathogenic organism for centuries. It causes a several diseases in humans including mild skin disease, upper respiratory tract (URT) infections, severe life-threatening conditions such as Rheumatic fever, glomerulonephritis, septicemia, pneumonia and streptococcal toxic shock syndrome .
Infection begins with colonization of the URT or injured skin surfaces. All age group may carry GAS on throat and epidermis of skin, however, children aged 5–15 years old are a major reservoir of pharyngeal carriage of GAS .
GAS is highly communicable and can cause disease in individuals of all ages. School-age children (5–15 years) are considered as the major reservoir of GAS, with a prevalence of 2.5–25% or more depending on the study setting . In Ethiopia, the asymptomatic carriage rate of GAS among healthy school children was 9.7–16.9% [4, 5].
An educational status, employment status of the family, separation of mother and father , sex [7,8,9,10], socioeconomic and environmental factors, lack of awareness of disease transmission are the risk factor for colonization of the S. pyogenes among school children [11, 12].
GAS has not been developed resistance to any of the penicillin’s over the last decades. Nowadays, it is starting to appear antimicrobial drug resistant strain from asymptomatic children  including penicillin . However, in Ethiopia, antimicrobial resistance pattern to the GAS isolated from throat/phalanx were not adequately explicated. Therefore, the present study was aimed to determine the carriage rate of S. pyogenes, associated risk factors and antibiotic susceptibility pattern among school children in Hawassa, South Ethiopia, 2018.
Study area and period
Hawassa is the capital city of the Southern Nation Nationalities and people’s Government. It is located 275 km South of Addis Ababa, and has an altitude of 1665 m above sea level with mean annual temperature and rainfall of 20.9 °C and 997.6 mm, respectively.
A school based cross-sectional study design was conducted from May to October 2018 in Hawassa, South Ethiopia.
All school children who attached governmental primary schools found in Hawassa town during the study period.
All children aged 5–15 years who attend the class in selected schools during the study period and children whose parents had accepted the consent to participate in the study.
All children who were on antibiotics for the last 2 weeks those with any signs and symptoms of respiratory diseases such as fever, soreness and throat, cough and watery nasal discharge were excluded.
A total of 295 school children were enrolled in this study. The study participants were selected by using a multi-stage stratified sampling technique. From the total of 19 governmental primary schools 30% (5 of the schools) were included. Simple random sampling technique was used to select the schools. Proportionate amount of samples were assigned to each selected schools. Then study participants were identified by the lists of students using simple random sampling technique.
The sample was collected from different school children from May to October 2018. The schools were sampled at the same period of time. All the swabs were immediately transferred to Amies transport medium (Oxoid, UK). Each sample was labeled very well. Within 2 h the collected swab were transported to the Microbiology laboratory [9, 14, 15].
Isolation of GAS
The throat swabs were directly inoculated to 5% sheep blood agar plates (Blood agar base, Oxoid UK) by rolling the swab over a small area of the plate and streaking the sample using a sterile loop and incubated at 37 °C with 5% CO2 atmosphere and examined beta-haemolytic colonies after 24 h and 48 h. Beta-haemolytic streptococci were identified by their colony morphology and beta-haemolysis.
All plates with beta-haemolytic colonies were sub-cultured with 0.04 U Bacitracin disks (Oxoid, UK) in blood agar plates similar manner as an earlier. All grams positive, catalase negative and any zone of inhibition around the disk were candidate for Pyrrolidonyl arylamidase (PYR) tests. A purple color in PYR tests were identified as S. pyogenes according to publications [16,17,18].
Antimicrobial susceptibility testing
Antibiotic susceptibility test (AST) was performed on disc diffusion method for all S. pyogenes using penicillin (10 U), erythromycin (15 µg), amoxicillin (10 µg), chloramphenicol (30 µg), ceftriaxone (30 µg), vancomycin (30 µg) and tetracycline (10 µg).
Data management and quality control
Quality of the data was ensured by using pre-structure questionnaire. For laboratory analysis the sterility of the prepared media was checked by incubating 5% by of prepared with in 5% CO2 enriched atmosphere at 37 °C for 24 h before using it. A quality control strain of S. pyogenes (ATCC19615) was used a positive control for each test.
Data processing and analysis
Data entry and analysis was performed by using SPSS version 20. The frequency of variables the prevalence of S. pyogenes, and antibiotic susceptibility pattern was determined. The association between risk factors and S. pyogenes colonization was determined by using logistic regression. A p value < 0.05 at 95% confidence interval (CI) was considered statistically significant.
Out of 295 school children who participated in the present study, 147 (51.2%) were males, 250 (87.8%) were within the age of 5–12 years. About 41.8% of the study participant’s parents/guardian found to have no formal education. A fifty percent of students’ mothers were a house-wife. About 162 (56.4%) of a total children’s parents/guardian had a monthly income between 500 and 900 ETB, 33 (11.5%) had 1000–1500 ETB and 92 (32.1%) had higher than 1500 ETB per month. However, the average income source of this area was 1560.00 ETB.
The prevalence of S. pyogenes
Among 287 school children 35 (12.2%) 95% CI [19–27.8] were confirmed to have S. pyogenes in throat swabs. A colonization rate of S. pyogenes among children who were 5–8 years old, 9–12 years old, 13–15 years old, those who live with employed mother, those who live with poor income source were 12 (17.1%), 18 (10.0%), 5 (13.5%), 8 (17.0%), and 26 (16%), respectively (Table 3).
The prevalence of S. pyogenes was higher among children with employed mother 8 (17.0%) than other occupations. Highest carriage rate was detected in low socioeconomic class 500–900 ETB per month 26 (16.0%) followed by 1000–1500 ETB 4 (12.1%). Among a total of 35 (12.2%) S. pyogenes isolates, the highest carriage rate was observed in student’s family size more than 5 person per house 23 (12.6%).
Out of 35 S. pyogenes isolated in this study, 35 (100%), 26 (74.3%), and 15 (42.9%) were susceptible to penicillin, vancomycin and tetracycline, respectively. About 34 (97.1%) of S. pyogenes isolates were sensitive to erythromycin, chloramphenicol, ceftriaxone and amoxicillin (Tables 1 and 2).
Risk factor analysis for pharyngeal carriage
The possible risk factors such as age, sex, children living status, parents/guardians occupation, parents/guardians education, income of parents, family size, person per bed room sharing, and past history of recurrences of URTI were evaluated for pharyngeal carriage of S. pyogenes. It was observed in bivariate analysis that, female children (COR = 2.212; 95% CI 1.055–0.638; p = 0.013), low income of parents (COR = 3.326; 95% CI 1.231–8.990; p = 0.001), children being with mother(COR = 0.34; 95% CI 0.2–1.6; p = 0.301), and occupational status of mothers (COR = 1.8 (1.2–4.40) 95% CI 1.2–4.40; p = 0.02 were observed.
The female children (AOR = 2.730; 95% CI 1.24–6.037; p = 0.013), and low income of parents (AOR = 11.917; 95% CI 2.729–2.032; p = 0.001) were associated with S. pyogenes carriage. Conversely, Occupational status of mothers (AOR = 100; 95% CI 0.023–0.437; p = 0.002) was associated with reduced likelihood of risk for asymptomatic pharyngeal carriage of S. pyogenes (Table 3).
The overall asymptomatic pharyngeal carriage rate of S. pyogenes among school children was 12.2% which is higher than the reports in Ethiopia 9.7% , in Tunisia 9.0% , in Nigeria 10% , Pemba 8.6% , India 8.4% , and Mangalore 5%  and lower than the report of Ethiopia 16.9% , Turkey 13.9% , Pennsylvania 15.9% , Australia 19.5%  and Turkey 25.9% . The possible explanation for the variation might be due to vaccination status and age differences. Moreover, sample size, seasonal variation and method if used, geography and socio-demographic variation are another possible explanation of the difference [4, 11, 21, 24].
In the present study we assessed different factors that could possibly increase colonization rate of S. pyogenes. Having female children 23 (16.4%) were 2.21 times more risk than male children for S. pyogenes colonization (p = 0.013). Similar result was reported from India , Turkey  and Nepal  and Ethiopia [4, 11, 21, 24]. This is might be due to social attitude towards female children or high contact with the others during supporting their mother in daily tasks.
The detection rate of S. pyogenes were high in children who had illiterate parents 19 (15.8%) (p > 0.05). It was in-lined with study reveled in India 44.9% , and in Iraqi 66.7% . This might be reflects the literate parents had better awareness of the hygiene, hand washing and not sharing utensils than the illiterate parents.
There was clear association of pharyngeal carriage rate and children from low income families in our finding which 26 were (16.0%). It was in accordance with the earlier finding in Ethiopia  and other studies carried out in many parts of the world [7, 25].
The carrier group of S. pyogenes was higher 10.9 times more among children living within families of more than 5 members than less family members in our study (p > 0.05). Similarly, S. pyogenes carriage was significantly higher in large family size as reported in different authors (p < 0.05) [2, 23, 26]. This might be an increasing the number of family members increases the rate of prevalence of many infectious diseases including GAS.
A Children with a history of hospital admission had 4.1 times chance to be colonized with GAS (p = 0.00) which is comparable to other’s studies . A children with history of recurrent pharyngitis show higher incidence 8 (80%) of carrier than those with no history of pharyngitis 16 (17.8%) .
A children from rural resident were 3 times (p = 0.002) more likely to have S. pyogenes carriage. This finding is similar to that the report found in Uganda at Wakiso district . In the current study, a high proportion (12.8%) of previously diseased children was colonized with S. pyogenes even though it was not statistically significant (p > 0.05).
Out of 35 of S. pyogenes isolated in this study, 35 (100%), 26 (74.3%) and 15 (42.9%) were susceptible to penicillin, vancomycin and tetracycline, respectively. However, 34 (97.1%) of S. pyogenes were susceptible to erythromycin, ceftriaxone, chloramphenicol and amoxicillin. The finding is similar as compared with the report found in Ethiopia  and in different parts of the world [7,8,9, 12,13,14, 29,30,31,32,33,34]. About 7 (29.2%) of isolated GAS strains were showed multiple drug resistant (two or more drugs). This is might be due to the ease of availability of antibiotics and misuse of the drugs.
The prevalence of S. pyogenes among school children in this study was high. The gender difference and low income of parents, residence of the children and occupational status of the mother are the prime risk factors associated with the carriage rate. All S. pyogenes isolates were susceptible to penicillin but most isolates were susceptible to chloramphenicol, Erythromycin and Ceftriaxone. Low level of resistant was observed against vancomycin and high level was observed against tetracycline. Further study in the area by using large sample size and all predisposing factors should be investigated.
Limitation of the study
Serotyping of Group A streptococci and ASO titer was not performed due to lack of antisera.
Availability of data
The data used/analyzed during the current study available from the corresponding author on reasonable request.
American type culture control
Ferretti JJ, Stevens DL, Fischetti VA, editors. Streptococcus pyogenes: basic biology to clinical manifestations. Oklahoma: The University of Oklahoma Health Sciences Center; 2016.
Saleh MMS. Carriage state of Gaβhs among Yemeni School children and the upper limit of Normal for ASO in different population groups. Iraqi J Sci. 2010;51(1):63–70.
Revelas A, Taxmazidis O. Group A streptococcal infections in children. S Afr J Epidemiol Infect. 2012;27(3):98–103.
Abdissa A, Asrat D, Kronvall G, Shitu B, Achiko D, Zeidan M, et al. Throat carriage rate and antimicrobial susceptibility pattern of Group A Streptococci (GAS) in healthy Ethiopian school children. Ethiop Med J. 2011;49(2):125–30.
Tewodros W, Muhe L, Daniel E, Schalen C, Kronvall A. One-year study of streptococcal infections and their complications among Ethiopian children. Epidemiol Infect. 1992;109:211–25.
Nabipour F, Tayarzadeh M. Prevalence of beta-hemolytic streptococcus carrier state and its sensitivity to different antibiotics among guidance—school children in Kerman-Iran. Am J Infect Dis. 2005;1(2):128–31.
Chand P, Arvind N, Vishrutha K, Vidyalakshmi K, Shenoy S. Surveillance of Group A Streptococcal throat infections among school children in Mangalore. Int J Biol Med Res. 2013;4(4):3585–9.
Muthusamy D, Boppe A, Suresh SP. The prevalence of the Group A beta haemolytic streptococcal carriers among school children in Coimbatore, South India. J Clin Diagn Res 2012;6(4).
Raza S, Kundu KK, Dutta SK. Prevalence of asymptomatic pharyngeal carriage of (3-hemolytic Group A Streptococcus pyogenes among school going children of age 5–12 years in Bharatpur, Nepal. J Kathmandu Med Coll. 2013;2(3):18–20.
Vijaya D, Sathish JV, Janakiram K. The prevalence of Group A Streptococci carriers among asymptomatic school children. J Clin Diagn Res. 2013;7(3):446–8.
Martin JM, Green M, Barbadora KA, Wald ER. Group A Streptococci among school-aged children: clinical characteristics and the carrier state. Pediatrics. 2004;114:1212–9.
Lloyd CAC, Jacob SE, Menon T. Pharyngeal carriage of group A streptococci in school children in Chennai. Indian J Med Res. 2006;124:195–8.
Dumre S, Sapkota K, Adhikari N, Acharya D, Karki M, Bista S. Asymptomatic throat carriage rate and antimicrobial resistance pattern of Streptococcus pyogenes in Nepalese school children. Kathmandu Univ Med J. 2009;7(28):392–6.
Fatima F, Shubha S. Prevalence survey for assessing intensity of group a beta hemolytic Streptococci (GABHS) Subclinical infection rate in school children: a cross sectional study. Glob J Med Res. 2013;13(3):1–6.
Ozturk E, Yavuz T, Kaya D, Yucel M. The rate of asymptomatic throat carriage of Group A Streptococcus in school children and associated ASO titers in Duzce. Turkey. Jpn J Infect Dis. 2004;57:271–2.
Gheni AI. Detection of Streptococci in the throat swabs from upper respiratory tract infections in Kurdistan Region. J Life Sci. 2014;8(3):283–9.
Agency HP. UK standards for microbiology investigations. Identification of Streptococcus species, Enterococcus species and morphologically similar organisms. UK: Standards Unit; 2011. p. 1–22.
WHO. Basic laboratory procedures in clinical bacteriology. In: J. Vandepitte et al. 2nd ed. Geneva: Switzerland: WHO; 2003. p. 1–188.
Mzoughi R, Selmi H, Ben Said H, Essoussi AS, Jeddi M. Group A streptococci in children with acute pharyngitis in Sousse, Tunisia. East Mediterr Health J. 2004;10:488–93.
Sadoh AE, Omokhodion SI. Streptococcal throat isolates in school children in an urban centre in Nigeria—are there other rheumatogenic strains? Niger J Cardiol. 2007;4:50–5.
Braito A, Galgani I, Mohammed MR, Iozzi C, Ame SM, Haji HS, et al. Epidemiology of Streptococcus Group A in school aged children in Pemba. East Afr Med J. 2004;81:307–13.
Gür E, Akkus S, Arvas A, Güzeloz S, Can G, Diren S, et al. Prevalence of positive throat cultures for Group A beta-hemolytic streptococci among school children in Istanbul. Indian Pediatr. 2002;39:569–73.
McDonald MI, Towers RJ, Andrews RM, Benger N, Currie BJ, Carapetis JR. Low rates of streptococcal pharyngitis and high rates of pyoderma in australian aboriginal communities where acute rheumatic fever is hyperendemic. Clin Infect Dis. 2006;43:683–9.
Kumar R, Vohra H, Chakraborty A, Sharma YP, Shah B, Dhanda V. Epidemiology of group A streptococcal pharyngitis & impetigo: a cross-sectional & follow up study in a rural community of northern India. Indian J Med Res. 2009;130:765–71.
Al-Gabban N, Al-Ani WA, Al-Kinany BJ. B-Haemolytic streptococcal carrier among school age children. Iraqi J Community Med. 2008;21(2):91–5.
Prajapati A, Rai SK, Mukhiya RK, Karki AB. Study on carrier rate of Streptococcus pyogenes among the school children and antimicrobial susceptibility pattern of isolates. Nepal Med Coll J. 2012;14(3):169–71.
Danchin MH, Rogers S, Kelpie L, Selvaraj G, Curtis N, Carlin JB, et al. Burden of acute sore throat and Group A Streptococcal pharyngitis in school-aged children and their families in Australia. Pediatrics. 2007;120:950–7.
Nayiga I, Okello E, Lwabi P, Ndeezi G. Prevalence of group a streptococcus pharyngeal carriage and clinical manifestations in school children aged 5–15 yrs in Wakiso District, Uganda. BMC Infect Dis. 2017;17:248.
Rubio-López V, Valdezate S, Álvarez D, Villalón P, Medina MJ, Salcedo C, et al. Molecular epidemiology, antimicrobial susceptibilities and resistance mechanisms of Streptococcus pyogenes isolates resistant to erythromycin and tetracycline in Spain (1994–2006). BMC Microbiol. 2012;12(215):1–11.
Rijal K, Dhakal N, Shah R, Timilsina S, Mahato P, Thapa PS, et al. Antibiotic susceptibility of Group A Streptococcus isolated from throat swab culture of school children in Pokhara, Nepal. Nepal Med Coll J. 2009;11(4):238–40.
Ksia S, Smaoui H, Kechrid A, Bouvet A. Streptococcus pyogenes isolated in a Tunisian pediatric population: emm types, T types, virulence factors and genes of resistance to macrolide and tetracycline. Malay J Microbiol. 2013;9(1):24–32.
Ibrahim SB, El-Sokkary R, Elhewala AA, El-Anwar MW, Awad WM, Hamed MA, et al. Emerging resistance to erythromycin and penicillin among Streptococcus pyogenes isolates in Zagazig, Egypt. Int J Curr Microbiol App Sci. 2014;3(10):750–6.
Graydon C, McKay R, Patrick D. Antimicrobial resistance trends in the Province of British Columbia. British Columbia Communicable Disease Prevention and Control Services Centre for Disease Control. 2011 AMR trends report, www.bccdc.ca. 2011. p. 1–88.
Devi U, Borah PK, Mahanta J. The prevalence and antimicrobial susceptibility patterns of beta-hemolytic streptococci colonizing the throats of schoolchildren in Assam, India. J Infect Dev Ctries. 2011;5(11):804–8.
We would like to acknowledge data collector, all staff working at kindergarten school that facilitated data collection, Hawassa University College of Medicine and Health Sciences, Jimma University Health Science institute for their support during the study. We would also acknowledge parents who allowed their children to participate in this study.
This study was supported by Jimma University, institute of Health Sciences. The support included payment for data collectors and purchase of materials and supplies required for the study. The support did not include designing of the study, analysis, and interpretation of data, and manuscript preparation.
Ethics approval and consent to participate
This study was ethically cleared from the Institutional Review Board (IRB) of the College of Medicine and Health Sciences, Hawassa University. Official permission was obtained from the study site and written informed consent was obtained from all parents/guardians of the children.
Consent for publication
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Anja, A., Beyene, G., S/Mariam, Z. et al. Asymptomatic pharyngeal carriage rate of Streptococcus pyogenes, its associated factors and antibiotic susceptibility pattern among school children in Hawassa town, southern Ethiopia. BMC Res Notes 12, 564 (2019) doi:10.1186/s13104-019-4601-9
- S. pyogenes
- Nasopharyngeal carriage