Abstract
Streptococcus pyogenes remains one of the top ten causes of mortality from infectious diseases. Children in low-income nations have high carrier rates of Streptococcus pyogenes, which can serve as a source of infections, including simple superficial infections that may lead to invasive and post-streptococcal diseases, particularly among schoolchildren. This study aimed to assess the prevalence of Streptococcus pyogenes, associated factors, and antimicrobial susceptibility profiles among urban and rural public schoolchildren in Gondar City, Northwest Ethiopia. A school-based comparative cross-sectional study was conducted via a multistage sampling technique among elementary schoolchildren from April to June 2022 in Gondar City. Sociodemographic and clinical data were collected via a pretested structured questionnaire. Standard microbiological methods were used to collect and process throat swabs to isolate Streptococcus pyogenes. An antimicrobial susceptibility test was performed via the disk diffusion method. Epi-Info version 7.2.5 was used to enter the data, which were then exported to SPSS version 25 for analysis. Logistic regression analysis was used to determine the strength of associations between variables, and p < 0.05 was considered statistically significant. The overall prevalence of Streptococcus pyogenes in 438 children was 11.2% (n = 49), with 71.43% (35/49) being urban and 28.57% (14/49) being rural. Low-income parents, hospital admission history, and cigarette smoking in the home were found to be substantially linked with Streptococcus pyogenes carriage among students (p < 0.05). All the Streptococcus pyogenes isolates were susceptible (100%) to penicillin and cefotaxime, but 18.8% and 12.25% of the isolates were resistant to amoxicillin and tetracycline, respectively. The prevalence of Streptococcus pyogenes throat carriage among was intermediate. All the isolates were sensitive to penicillin and cefotaxime, but 18.8% and 12.25% of the isolates were resistant to amoxicillin and tetracycline, respectively. Thus, regular screening and surveillance of Streptococcus pyogenes among schoolchildren should be conducted to minimize carriage or infections and maintain the rational use of antimicrobials. Health education about cigarette smoking in the house also needs to be provided to and the community.
Supplementary Information
The online version contains supplementary material available at 10.1038/s41598-024-82009-2.
Keywords: Streptococcus pyogenes, Schoolchildren, Antimicrobial susceptibility profile
Subject terms: Microbiology, Health care, Medical research
Introduction
Streptococcus pyogenes (S. pyogenes) is a facultative anaerobe, gram-positive, β-hemolytic bacterium arranged in chains1, and a major human-specific bacterial pathogen2. Poverty increases the risk of all S. pyogenes infections because living conditions facilitate the organism’s spread and make prevention and control initiatives less likely to be effective3.
The human skin and mucous membranes are the only reservoirs of S. pyogenes in nature and first colonize the oropharynx and skin, from which it can progress to severe disease4. It affects people of any age, but children are the most likely to be affected5. S. pyogenes is responsible for various infections, ranging from superficial to more serious disorders, such as streptococcal toxic shock syndrome (STSS) necrotizing fasciitis, and meningitis. In addition, it also causes autoimmune diseases such as acute rheumatic fever (ARF) that can lead to rheumatic heart disease (RHD)6,7. These serious disease is caused by a wide range of surface antigens, toxins, and enzymes8.
Streptococcus pyogenes is the most common cause of pharyngitis in schoolchildren and is considered a “hazard” in school-aged children9. It is responsible for 616 and 111 million cases of pharyngitis and pyoderma in children, respectively10. Approximately 18 million people suffer from severe S. pyogenes-related diseases worldwide, with 1.78 million new cases and at least 517,000 deaths occurring each year11. More than 660,000 people suffer from invasive S. pyogenes infections, which result in more than 160,000 deaths annually across the globe. A more recent analysis of data concerning the worldwide burden of ARF and RHD in Africa revealed that 15.6–19.6 million people have RHD, of which 2.4 million are children between the ages of 5 and 14, with 1 million living in Sub-Saharan Africa12. Children from low- and middle-income nations are at risk for invasive and RHD infections13. Ethiopia is a country with a high prevalence of ARF and RHD, accounting for 50–64% of children’s RHD14.
The carriage rate of S. pyogenes in asymptomatic school-aged children is estimated to be 15–20% worldwide. On the other hand, its prevalence was reported to be 8.4–12.9% in children from high-income nations15. The carriage rate in Ethiopia was 9.7%15, and a current study in Hawasa, Ethiopia, found 22.9% in urban and 8.8% in rural areas16. Untreated S. pyogenes infections can progress to ARF, and inappropriate antibiotic prescriptions based on inaccurate data can lead to the emergence and spread of antibiotic-resistant bacteria17.
The factors that promote resistance are misuse, overuse, and poor infection prevention practices and empirical treatment practices18. Diseases caused by S. pyogenes and their post-infection sequelae, which mostly affect children, have considerable impacts on public health and the economy19. The carriage rate of S. pyogenes is directly related to children’s crowding, low socioeconomic status, limited medical access, and residence9. S. pyogenes is highly contagious, and school settings provide excellent conditions for its transmission due to close contact among children20. Individuals who have this organism on their pharynx but show no symptoms may contribute to infection in households and public areas, including offices, schools, and daycare centers21. Evidence showed that S. pyogenes carriers have the potential to cause reinfection and may develop life-threatening conditions22.
Although S. pyogenes poses serious issues, there is limited data in Ethiopia3,21 and only a few studies have been conducted in the past, specifically in Gondar City, northwest Ethiopia23. Data on S. pyogenes carriage rate-associated factors and antimicrobial susceptibility profiles among schoolchildren in Ethiopia are needed, particularly in the study area. Thus, this study aimed to evaluate and fill the knowledge gap concerning antibiotic susceptibility patterns, current throat carriage rates, and related risk factors for S. pyogenes among students attending elementary schools in Gondar City. It will also serve as preliminary data for further research and to highlight preventative and control strategies in the broader population.
Methods and materials
Study area and period
The study was conducted in six urban and six rural governmental elementary schools from April to June 2022 in Gondar City. The city is located in the Central Gondar Zone of the Amhara Regional State, 748 km northwest of Addis Ababa, Ethiopia’s capital, and approximately 180 km from Bahir Dar, the Amhara Regional State’s capital. Gondar is Ethiopia’s fourth largest city, with an estimated population of 378,000 residents24. During the study period, the city had 44 elementary schools, of which 23 were urban (29,582 students) and 21 were rural (12,863 students), with a total of 42,445 students. Among these, 20,742 were males and 21,703 were females, according to the Gondar City education department.
Study design and population
A school-based comparative cross-sectional study was conducted. A lottery system was used to choose students at random from six urban and six rural government elementary schools. Participants’ parents supplied written informed consent and oral assent (7–11 years), while children ≥ 12 years old provided written assent.
Study population
All who attended in the selected government elementary schools in Gondar City, during the study period.
Inclusion and exclusion criteria
Schoolchildren aged 7–15 years old selected from each classroom of the selected schools who attended the class during the study period were included.
However, children who have been on antibiotic treatment for the last 2 weeks and at the time of data collection, children with throat infections or any related signs and symptoms of pharyngitis, children who were unable to give sociodemographic information and nasal samples, and those who were involuntary to participate in the study due to different reasons were excluded.
Sample size determination and sampling technique
The double population proportion formula was used by considering the following statistical assumption: 95% CI, taking the prevalence of S. pyogenes, p1 = 22.9% in urban areas and p2 = 8.8% in rural areas from the previous study21.
By considering a 10% non-response rate and design effect 2: 102 × 2 = 204, 204 × 0.1 = 20.4 ≈ 21,
n1 = 204 + 21 = 225.
Therefore, the final calculated sample size was 225 for each area and the total sample size was 450.
Sampling procedure and sampling technique
Twelve12 elementary schools were picked at random from a total of 44 using a lottery system. The selected schools were then assigned a proportionate percentage of the study’s finalized sample size. Children were identified using a random sampling procedure. To include study participants, a multistage sampling procedure was used. Children whose parents agreed to participate were sampled until the sample size was attained at each chosen school.
Sample collection and transport methods
A predesigned structured questionnaire based on prior research3,21,25 was used to collect information on the socio-demographic characteristics of the parents/guardians and children, as well as the children’s clinical history. The interviews were administered by a qualified nurse, and two skilled laboratory workers collected a sample of the child’s throat using cotton swabs. The throat swab samples were labeled, put in Amies transport media (Oxoid, England), and transferred via cold chain to the Microbiology Laboratory at the University of Gondar’s College of Medicine and Health Sciences in less than two hours.
Laboratory investigation
The throat sample was cultured on 5% sheep blood agar plates (Blood Agar Base, Oxoid UK) by rolling the swab over a small area of the plate, streaking the sample with a sterile loop, and then incubating at 37 °C in a 5% CO2 atmosphere for 24 h. All plates with beta-hemolytic colonies were microbiologically processed and S. pyogenes were identified by conventional methods (colony morphology, hemolysis pattern, catalase test, Gram stain, and morphological observation). All catalase-negative and gram-positive cocci were sub-cultured for 24 h. at 37 °C on 5% fresh blood agar plates with a Bacitracin disk in a 5% CO2 condition to identify further colonies suspected of S. pyogenes26.
Antimicrobial susceptibility testing
The antimicrobial susceptibility test was conducted via a disk diffusion technique utilizing Muller Hinton Agar (MHA) supplemented with 5% sheep blood. The colony suspension was prepared by mixing normal saline (0.85% NaCl) with the equivalent of 0.5% McFarland standard from grown overnight colonies (18–24 h.) on sheep blood agar plates. Then, the suspension was streaked on an MHA plate with 5% sheep blood, and the following antibiotic disks were dispensed.
Antibiotic disks containing penicillin (P = 10 U), ampicillin (AMP = 10 µg), clindamycin (DA = 2 µg), erythromycin (E = 15 µg), chloramphenicol (C = 30 µg), tetracycline (TE = 30 µg), vancomycin (VA = 30 µg), azithromycin (ATH = 15 µg), ceftriaxone (CRO = 30 µg), cefotaxime (CTX = 30 µg), and cefepime (FEP = 30 µg) were used. The preparation was incubated at 37 °C in a candle jar for over 18–24 h. Finally, the sensitivity pattern is read and interpreted.
These antibiotics were selected following the Ethiopian Drug Administration standard guidelines for health centers and control authorities27 and the Clinical Laboratory and Standard Institute (CLSI) 2021 guidelines28. The antibiotic sensitivity pattern was determined by measuring the zone of inhibition via a ruler and interpreted as sensitive, intermediate, or resistant according to the diameter of inhibition established by the CLSI guidelines28.
Data quality control
All methods were performed in accordance with the relevant guidelines and regulations. To ensure consistency, the questionnaire was initially written in English, translated into Amharic, and then back into English. The questionnaire was pretested before the start of the real data collection. To assess the sterility of every produced media batch in a laboratory setting, 5% of the culture media was incubated for 24 h. at 37 °C in an atmosphere enriched with 5% CO2. Streptococcus pyogenes (ATCC 19615) and Streptococcus agalactiae (ATCC 12386), were used for positive and negative controls of the Bacitracin disk test, respectively28.
Data entry and analysis
The data were coded and entered into Epi Info version 7.2.5, and its completeness and clearness were checked to ensure the recorded data’s validity. The data were subsequently exported to SPSS version 25 for analysis. Descriptive statistics and frequency tables were used to summarize the data. Logistic regression analysis determined the association between each independent variable and the outcome variable.
All variables with P ≤ 0.20 in the bivariate analysis were included in the final model of the multivariate analysis to identify factors associated with the throat carriage of S. pyogenes. The direction and strength of the statistical associations were measured via odds ratios with a 95% confidence intervals. An adjusted odds ratio with a 95% CI was estimated, and a P value < 0.05 was considered statistically significant.
Results
Sociodemographic characteristics of the study participants
A total of 438 study participants were included in this study, with a response rate of 97.33%. The data revealed that 240 (54.8%) and 280 (63.93%) participants were females and urban dwellers, respectively. The study participants ranged in age from 7 to 15 years, with a median of 12 years (IQR ± 3). Two hundred eighty-nine (66%) study participants were 11 to 15 years of age. Furthermore, 232 (53%) of the study participants were from families with more than five members. Approximately 183 (41.8%) of the study participants had a history of sore throat before two weeks, and 83 (18.9%) had a history of sore throat in their families (Table 1).
Prevalence of streptococcus pyogenes
The overall throat carriage rate of S. pyogenes was 11.2% (n = 49, 95% CI 8.4–14.2) among SSchil438 study participants. Of the forty-nine S. pyogenes isolates, 35/49 (71.43%) were recovered from urban, and 28.57% (14/49) were from rural. The carriage rate in females was 11.67% (28/240). A higher carriage rate was observed within an age group of 7–10 year, 13.86% (Table 1).
Table 1.
Frequency (%) of the S. pyogenes concerning the sociodemographic and clinical variables among urban and rural elementary schoolchildren in Gondar City, Northwest Ethiopia, 2022.
| Variables | category | Frequency n (%) |
Culture result () | |||||
|---|---|---|---|---|---|---|---|---|
| Pos (N=49) n (%) n (%) |
Neg (N=389) | Urban (N=280) Pos(N=35) | Neg(N=245) | Rural (N=158) Pos(N=14), | Neg (N=144) | |||
| Age | 7-10 years | 149 (34) | 20 (13.42) | 129 (86.58) | 14/101 (13.86) | 87/101 (86.14) | 6/48 (12.5) | 42/48 (87.5) |
| 11-15 years | 289 (66) | 29 (10.03) | 260 (89.97) | 21/179 (11.73) | 154/179(86.03) | 8/110(72.27) | 102/110(92.72 | |
| Sex | male | 198 (45.2) | 21(10.6) | 177 (89.4) | 13/120 (10.38) | 107/120(89.16 | 8/78(10.26) | 70/78 (89.74) |
| Female | 240 (54.8) | 28 (11.67) | 212 (88.33) | 22/160(13.75) | 138/160(86.25) | 6/80 (7.5) | 74/80 (92.5) | |
| Students’ educational status | 1-4 grades | 225 (51.37) | 29 (12.9) | 196 (88.1) | 21/154(13.64) | 133/154(86.36) | 8/71(11.2) | 63/71(88.8) |
| 5-8 grades | 213 (48.63) | 20 (9.40) | 193 (90.1) | 14/126(11.11) | 112/126(88.89) | 6/87(6.8) | 81/87 (93.2) | |
| Households (n) | 2-5 | 232 (53) | 23(9.9) | 209 (90.1) | 19/162(11.73) | 102/162(88.27) | 4/60(6.67) | 56/60(93.33) |
| Greater than 5 | 206 (47) | 26 (14.44) | 180 (85.56) | 16/118(13.56) | 102/118(85.44) | 10/98(10.20) | 88/98(89.8) | |
| Children living with non- | Family | 424 (96.8) | 43 (10.14) | 381 (89.86) | 30/270 (11.11) | 240/270 (88.89) | 13/154(8.44) | 121/154(91.56 |
| immediate family | 14 (3.2) | 6 (42.86) | 8 (57.14) | 5/10 (50) | 5/10 (50) | 1/4(25) | 3/4(75) | |
| Sharing sleeping bed | 1-2 | 319 (72.8) | 31(9.7) | 288 (90.3) | 20/215(9.3) | 195/215(90.7) | 11/104 (10.5) | 97/104(89.5) |
| above 2 | 119 (27.2) | 18(15.13) | 101(84.87) | 15/65(23) | 50/65(77) | 3/54 (5.5) | 52/54(94.5) | |
| No. of students in a class | ≤50 | 207 (47.3) | 17(8.2) | 190 (91.8) | 15/158(9.5) | 143/158(90.5) | 2/49 (4.1) | 47/49(96) |
| above 50 | 231(52.7) | 32 (14.5) | 199 (85.5) | 20/122(16.4) | 102/122(83.6) | 12/109 (11.0) | 97/109(89) | |
| Parent Education status | unable to read &write | 93 (21.2) | 13 (13.98) | 80 (86.02) | 8/56 (14.3) | 48/56(85.7) | 5/43(11.63) | 37/43(88.37) |
| primary school complete | 196 (44.7) | 23(11.73) | 173(88.27) | 19/160 (11.87) | 139/160(88.13) | 4/36(11.11) | 32/36(88.89) | |
| secondary school complete | 46(10.5) | 7(15.2) | 39(84.8) | 5/29(17.24) | 24/29(82.76) | 2/17(11.76) | 15/17(88.24) | |
| college/university | 103(23.5) | 6(5.82) | 97 (94.18) | 3/64 (4.7) | 61/64(95.3) | 3/39(7.7) | 36/39(92.3) | |
| Parents’ occupation | Gov.t employment | 119 (27.2) | 7(5.9) | 112 (94.1) | 4/57(7.1) | 53/57(92.9) | 3/62 (4.5) | 59/62(95.5) |
| Private employment | 101 (23.1) | 9(8.91) | 92 (91.09) | 7/89(7.86) | 82/89 (92.14) | 2/12(16.67) | 10/12(83.33) | |
| merchant | 151(34.7) | 24(15.89) | 127 (84.11) | 20/105(19.05) | 85/105(80.95) | 4/46 (8.7) | 42/46(8/3) | |
| others | 66(15.1) | 9(13.63) | 57 (86.37) | 4/29 (13.8) | 25/299(86.2) | 5/37 (13.51) | 32/37(86.49) | |
| Family’s monthly income | ≤2000 EBR | 95 (21.7) | 23(19.5) | 95 (80.5) | 14/64(21.9) | 50/64(62.5) | 9/31(29.03) | 22/31(70.97) |
| 2001-5000EBR | 259 (59.1) | 21(7.5) | 259 (92.5 | 16/161 (9.94) | 145/161(90.06) | 4/98(4.1) | 94/98(95.9) | |
| >5000 EBR | 84 (19.2) | 5 (5.62) | 84 (94.38) | 35/280(12.5) | 1/29(3.4) | 1/29(3.4) | 28/29(96.6) | |
| History of chronic disease | Yes | 17 (3.9) | 5 (29.41) | 12 (70.59) | 3/9 ( 33.33) | 6/9(66.7) | 2/8 (25) | 6/8 ( 75) |
| No | 421(96.1) | 44(10.45) | 377(89.55) | 32/271(11.8) | 239/271(88.2) | 12/150(8) | 138/150(92) | |
| History of health institution visits | Yes | 44 (10) | 5 (11.36) | 39 (88.64) | 4/35 (11.43) | 31/35(88.57) | 1/9 (11.11) | 8/9(88.89) |
| No | 394(90) | 44(11.1) | 350(88.83) | 31/245(12.65) | 214/245(87.35) | 13/149(8.72) | 136/149(81.28 | |
| Hx. of antibiotic use without prescription | Yes | 91 (20.8) | 8 (8.79) | 83 (91.21) | 3/35(8.57) | 33/35(91.43) | 5/56(8.93) | 51/56(91.17) |
| No | 347 (79.1) | 41(11.82) | 306 (88.18) | 32/245(13.6) | 213/245(86.4) | 9/102(8.82) | 93/102(91.18) | |
| Hx. Of cigarette smoker in the house | Yes | 26 (5.9) | 10 (38.46) | 16 (61.34) | 7/18(38.88) | 11/18(61.12) | 3/8 (37.5) | 5/8(62.5) |
| No | 412 (94.1) | 39 (9.5) | 373 (90.5) | 28/262(10.68) | 234/262(89.32) | 11/150(7.3) | 139/150(92.7) | |
| Hx of hospitalization to any case | Yes | 26 (5.9) | 9 (34.6) | 17 (96.54) | 6/15(40) | 9/15(60) | 3/11(27.3) | 8/11(72.7) |
| No | 412 (94.1) | 40 (9.71) | 372 (90.29) | 29/265(11) | 36/265(89) | 11/1477.5) | 136/147(92.5) | |
| History of heart disease | Yes | 120 (27.4) | 15 (13.16) | 99 (86.84) | 11/85 (13) | 74/85(87) | 4/35 (11.43) | 31/35(88.57) |
| No | 318 (72.6) | 34 (10.5) | 290 (89.5) | 24/195(12.31) | 171/195(87.69 | 10/123(8.13) | 113/123(91.87) | |
| Hx. of headache | Yes | 114 (26) | 15 (13.16) | 99 (86.84) | 9/66(13.64) | 57/66(84.36) | 6/48(12.5) | 42/48(87.5) |
| No | 324 (74) | 34 (10.5) | 290 (89.5) | 26/214(12) | 188/214(88) | 8/10(80) | 2/10(20) | |
|
Repeated of URTI w/in six months in the past |
Yes | 136 (31.1) | 21(15.44) | 115 (84.56) | 15/82(18.3) | 67/82(81.7) | 6/54(11.11) | 49/54(88.89) |
| No | 302 (68.9) | 28 (9.27) | 274 (90.73) | 20/198(10.10) | 178/198(89.9) | 8/104(7.7) | 96/104(92.3) | |
| Hx. of lymphadenopathy | Yes | 113 (25.8) | 18 (15.93) | 95 (84.17) | 11/54(20.37) | 43/54(79.63) | 7/59(11.86) | 52/59(88.14) |
| No | 325 (74.2) | 31(9.54) | 294 (90.46) | 24/226(10.62) | 202/226(89.38 | 7/99(7.10) | 92/99(92.9) | |
| Hx. of body temperature | ≥38 | 122 (27.9) | 14 (11.48) | 108 (88.52) | 11/80(13.75) | 69/80(86.25) | 3/42(7.10) | 39/42(92.9) |
| <38 | 316 (72.1) | 35 (10.07) | 281 (89.89) | 24/200(12.0) | 176/200(88) | 11/116(9.5) | 105/116(90.5) | |
| Hx. of respiratory instrument use while admission | Yes | 12 (2.74) | 2 (16.67) | 10 (83.33) | 2/9(22.22) | 7/9(77.78) | 0/3(0) | 3/3(100) |
| No | 426 (97.26) | 47 (11.03) | 379 (88.87) | 33/271(12.17) | 238/271(87.83 | 14/155(9) | 141/155(91) | |
| Hx. of sore throat before two weeks | Yes | 183 (41.8) | 28 (15.3) | 155 (84.7) | 19/113(16.8) | 94/113(83.2) | 9/70(12.86) | 61/70 (87.14) |
| No | 255 (58.2) | 21(8.24) | 234 (91.76) | 35/280(12.5) | 245/280(87.5) | 5/88(5.7) | 144/158 (91.14) | |
| Hx. of sore throat in family members | Yes | 83 (18.9) | 13(15.66) | 70 (84.34) | 9/49(18.4) | 40/49(81.6) | 4/34(11.76) | 30/34(88.24) |
| No | 355 (81.1) | 36 (10.14) | 319 (89.86) | 26/231(11.26) | 205/231(88.74) | 10/124(8) | 114/124(92) | |
Key: URTI upper respiratory tract infection, Hx history, Pos positive, Neg Negative, EBR Ethiopian birr.
In urban elementary schoolchildren, the carriage rate was 12.5% (35/280), whereas in rural schoolchildren, it was 8.86% (14/158) (Table 1). In this study, the distribution of S. pyogenes differed among schoolchildren. For example, the carriage rate of S. pyogenes at one urban elementary school, Edigetfeleg, was 22.22% (8/36) (Fig. 1), whereas at another rural school, Deresgie, the carriage rate was 45.5% (5/11) (Fig. 2). Children who lived with non-immediate families had the highest carriage rate, 42.86% (6/14), followed by children who lived with a cigarette smoker in the family, 38.46% (10/26) (Table 1).
Fig. 1.
Frequency of S. pyogenes among study participants in urban elementary schoolchildren (N = 280), Gondar, Northwest Ethiopia, 2022.
Fig. 2.
Frequency of S. pyogenes among study participants in rural elementary schoolchildren (N = 158), Gondar, Northwest Ethiopia, 2022.
Factors associated with streptococcus pyogenes colonization
Among the variables analyzed via bivariate logistic regression, those with a P value ≤ 0.20 were eligible for inclusion in the multivariable analysis. In the multivariable analysis, parents’ income 2000EBR (P = 0.003; AOR = 5.56; CI: (1.76, 17.57), history of hospital admission (p = 0.000; AOR = 7.25; CI: (2.61, 20.17) and cigarette smokers in the house (p = 0.000; AOR = 6.9; CI: (2.49, 19.10) were significant predictors of the S. pyogenes carriage rate among schoolchildren (Table 2).
Table 2.
Bivariate and multivariate logistic regression analyses of sociodemographic and clinical variables associated with S. pyogenes among urban and rural schoolchildren in Gondar city.
| Variable | Category | S. pyogenes | COR(95%CI) P-value | AOR (95% CI) | P-value | |
|---|---|---|---|---|---|---|
| Yes (n=49) | No (n=389) |
|||||
| Residence | Urban | 35 | 245 | 1.47(0.66,2.82) 0.248 | 1.38(0.65-2.94) | 0.406 |
| Rural | 14 | 144 | 1(ref.) | 1 | ||
| Households(n) | 2-5 | 23 | 209 | 1 | 1 | |
| Greater than 5 | 26 | 180 | 0.76 (0.42-1.38) 0.371 | 1.06 (0.51-2.45) | 0.25 | |
|
Parent income/month (EBR) |
≤2000 | 23 | 72 | 5.05(1.82-13.98) 0.009 | 5.56(1.76-17.57) | 0.003* |
| 2001-5000 | 21 | 238 | 1.4(0.05-3.82) 0.820 | 1.26 (0.35-4.58) | 0.722 | |
| >5000 | 5 | 79 | 1 | 1 | ||
| Children living condition with | Family | 42 | 381 | 1 | 1 | |
|
Non imme- diate family |
6 | 9 | 6.05 (2.20-20.05) 0.001 | 3.37(0.74-15.29) | 0.115 | |
| Number of person per bed | 1-2 | 31 | 288 | 1 | 1 | |
| >2 | 18 | 101 | 1.66(0.9-3.1) 0.113 | 1.15(0.54-2.45) | 0.722 | |
| Number of students per class | ≤50 | 17 | 190 | 1 | 1 | |
| >50 | 32 | 199 | 1.8(0.97-3.34) | 1.60 (0.77-3.33) | 0.21 | |
| History of hospital admission | Yes | 9 | 17 | 4.92(2.06-11.77) 0.001 | 7.25(2.25-20.17) | 0.001* |
| No | 40 | 372 | 1 | |||
| History of sore throat before two week | Yes | 28 | 155 | 2.01(1.10-3.67) 0.023 | 1.02(0.36-2.88) | 0.975 |
| No | 21 | 234 | 1 | 1 | ||
| Repeated URTI in the past six month | Yes | 21 | 115 | 1.79(0.98-3.28) 0.061 | 1.56(0.56-4.38) | 0.394 |
| No | 28 | 274 | 1 | 1 | ||
| History of tender cervical lymphadenopathy | Yes | 18 | 95 | 1.797(0.96-3.36) 0.066 | 0.702(0.24-2.02) | 0.511 |
| No | 31 | 294 | 1 | 1 | ||
| History of chronic disease | Yes | 5 | 12 | 3.57(1.20-10.61) 0.022 | 3.03(0.86-10.69) | 0.085 |
| No | 44 | 377 | 1 | 1 | ||
| Family member with sore throat | Yes | 13 | 70 | 1.65(0.83-3.264) 0.154 | 1.22(0.54-2.75) | 0.635 |
| No | 36 | 319 | 1 | 1 | ||
| Cigarette smoker in the house | Yes | 10 | 16 | 5.98(2.54-14.1) 0.001 | 6.9 (2.49-20.73) | 0.001* |
| No | 39 | 373 | 1 | 1 | ||
| Cleanness of the class | Yes | 9 | 112 | 1 | 1 | |
| No | 40 | 277 | 1.80 (0.44-3.83) 0.128 | 2.01 (0.86-4.71) | 0.107 | |
COR crude odds ratio, AOR Adjusted odds ratio, URTI Upper respiratory tract infection.
* Associations between independent variables and the S. pyogenes carriage rate.
Antimicrobial susceptibility pattern of Streptococcus pyogenes
All 49 S. pyogenes isolates identified were susceptible to penicillin and cefotaxime. The majority of these strains were susceptible to azithromycin (97.96%), ampicillin and ceftriaxone (95.9%), chloramphenicol (93.87%), clindamycin (93.87%), ceftriaxone (95.9%), vancomycin (93.87%), and erythromycin (87.75%). Relatively low activity was observed for amoxicillin (79.6%) among isolates recovered from rural schoolchildren. Two (4.1%) of the 49 isolates were multidrug-resistant to amoxicillin, tetracycline, and erythromycin (Table 3).
Table 3.
Antimicrobial susceptibility patterns of S. pyogenes isolates among urban and rural elementary schoolchildren in Gondar City, Northwest Ethiopia, 2022.
| Antimicrobial Agents |
Urban schools | Rural schools | |||||
|---|---|---|---|---|---|---|---|
|
n =35
S n (%) |
I
n (% ) |
R
n (%) |
n=14
S n (%) |
I
n (%) |
R
n (%) |
Total | |
| Penicillin 10 μg | 35 (100) | - | - | 14 (100) | - | - | 49 (100) |
| Ampicillin 10 μg | 34 (97.14) | - | 1(2.86) | 13 (92.86) | - | 1(7.14) | 47 (95.9) |
| Amoxicillin 10 μg | 29 (82.85) | - | 6 (17.14) | 10(71.43) | 1(7.14) | 3(21.43) | 39 (79.6) |
| Cefotaxime 30 μg | 35 (100) | - | - | 14 (100) | - | - | 49 (100) |
| Ceftriaxone 30 μg | 34 (97.14) | - | 1 (2.86) | 13 (92.86) | - | 1 (7.14) | 47 (95.9) |
| Chloramphenicol 30 | 33 (94.3) | - | 2 (5.7) | 13(92.86) | - | 1(7.14) | 46(93.87) |
| Clindamycin 2 μg | 34 (97.14) | - | 1 (2.86) | 13(92.86) | - | 1(7.14) | 46(93.87) |
| Azithromycin 15μg | 35 (100) | - | - | 13(92.86) | - | 1(7.14) | 48 (97.96) |
| Vancomycin 30 μg | 33 (94.3) | - | 2 (5.7) | 13(92.86) | - | 1(7.14) | 46 (93.87) |
| Erythromycin 15μg | 30 (85.71) | 1(2.86) | 4 (11.42) | 12(85.71) | - | 2(14.28) | 43 (87.75) |
| Tetracycline 30 μg | 32 (91.43) | 2 (5.71) | 2 (5.7) | 11(78.57) | - | 3(21.43) | 43 (87.75) |
Key: S Sensitive, I Intermediate, R Resistance.
Discussion
S. pyogenes throat carriage is an important public health issue, as the infection leads to post-streptococcal sequelae and individuals colonized with S. pyogenes can serve as a source of infections to others29. Evidence showed that S. pyogenes carriers have the potential to cause reinfection and may develop life-threatening conditions22. S. pyogenes infections can lead to acute rheumatic fever (ARF) and, subsequently, rheumatic heart disease (RHD) through a process known as molecular mimicry. Initial infection usually starts with pharyngitis (strep throat) or skin infections caused by S. pyogenes. The body mounts an immune response to clear the bacteria. However, due to similarities between bacterial antigens and human tissue antigens, some antibodies produced during this response can mistakenly target the body’s tissues, particularly the heart, joints, skin, and central nervous system30. Certain proteins on the surface of S. pyogenes resemble human proteins, especially those found in heart muscle and connective tissues. This cross-reactivity leads to an autoimmune response. Repeated episodes of ARF can cause chronic damage to the heart valves, leading to RHD31.
In the current study, the overall throat carriage rate of S. pyogenes was 11.2% (95% CI; 8.4–14.2). This finding was in line with study reports from Nepal (10.8%)32, Sana’a, Yemen (12.8%)33, Argentina (14%)34, the United Arab (10%)35, Indonesia (13.9%)25, Kenya (9.5%)9, Pakistan (11.5%)36 and Ethiopia, such as Hawasa (12.2%)21 and Jijiga (10.6%)3. In contrast, the results of this study were higher than the S. pyogenes carriage rates reported in Gondar Ethiopia (8.3%)23, Nepal (5.4%)37, Iran (3–6%)38, India (1.9%)39, Côte d’Ivoire (4.6%)40, and Nigeria (3.3%)22. On the other hand, the findings of this work revealed a lower prevalence of S. pyogenes throat carriage than reported in Yemen (39.03%)41, Kerala, India (23.1%)42, Uganda (16%)43, and Egypt (16%)44. The difference might be due to variations in the control of respiratory infections, hygiene practices, geographical location, population density, and sample size37,40.
In the present study, females had a slightly higher carriage rate (11.67%) than did males (10.6%), which is consistent with research conducted in Nepal32,45 and Pakistan36. This may be due to social attitudes toward females or high contact with objects or others while supporting their mothers in daily tasks, which may contribute to upper respiratory infections. A higher prevalence of S. pyogenes was recorded in the age group of 7–10 years (13.42%), which is supported by studies in Argentina34 and Jijiga Ethiopia3. This might be due to poor personal and hand hygiene practices and low immunity status.
Urban children had a higher S. pyogenes carriage rate (12.5%) than did rural children (8.86%), which is similar to the findings of studies conducted in Hawasa21 and Uganda43. This could be due to overcrowding and the presence of several governmental and nongovernmental health care facilities, such as hospitals and health centers/clinics, which attribute overcrowding and a higher level of social contact in these settings to the urban community rather than the rural community46.
Several studies have shown that sociodemographic characteristics and risk factors contribute greatly to the throat carriage rate of S. pyogenes3,21,22,33,43,47. In the present study, we assessed different factors that could increase the colonization rate of S. pyogenes. There was no significant connection of S. pyogenes carriage rate between urban and rural areas, or between females and males. Children living with parents earning less than 2000 EBR were 5.56 times more likely to get S. pyogenes colonization than children earning more than 5000 EBR. This finding was consistent with studies in Hawasa Ethiopia21, Indonesia47, and Kenya46. Possible factors could be inadequate health care and housing conditions, low household income, poor personal hygiene, and inadequate nutrition46. Children who had a history of hospitalization were 7.25 times more likely to have a carriage rate of S. pyogenes than those who had no history of hospitalization. This result was in line with the findings of a study from Hawasa21. Since hospitals are common areas that are overcrowded and exposed to S. pyogenes, they increase the spread of bacteria.
Children living with cigarette smokers in the house had a 6.9 times increased likelihood of carrying S. pyogenes than children living in houses without cigarette smokers. This result was in agreement with reports from Ethiopia such as Bahir Dar48 and Adama49. Smoking may disrupt and reduce the commensal population of normal flora, providing opportunities for pathogenic microorganisms and affecting both innate and adaptive immunity by intensifying the pathogenic immune response or attenuating defensive immunity50.
All the S. pyogenes isolates were sensitive to penicillin and cefotaxime, which is in line with studies reported in many nations, such as Ethiopia3,21, Nepal32,37, India42, Egypt44, southern Nigeria22, Indonesia25, Pakistan36, Argentina34, and Kerala, India42. Ampicillin demonstrated 95.9% activity against S. pyogenes, which was in line with the findings of research conducted in Nepal32.
Amoxicillin and tetracycline slightly reduced activity (71.43% and 78.57%, respectively) among rural schoolchildren compared with urban children, which was comparable to the findings of a study in Argentina34. The possible reason might be that children from rural areas have weak experience using health institution services, and they may even misuse antibiotics. The isolates presented the same level of sensitivity to clindamycin, chloramphenicol, and vancomycin (93.87%). This finding was similar to the report found in Pakistan36. In the present study, the isolates were sensitive to tetracycline and erythromycin (87.75%), azithromycin (97.96%), and ceftriaxone (95.9%). These findings were almost identical to earlier studies in Ethiopia, such as Hawassa21 and Jijiga3, as well as other studies carried out in Pakistan36.
Limitations of the study
Some of the children who were categorized as colonized might have been ill or experienced recall bias. The pyrrolidonyl aminopeptidase (PYR) test is more specific (100%) than bacitracin (87.5%), but it was not performed because of its unavailability. Confirming the use of antibiotics in the two weeks preceding the study was often challenging for some of the younger children.
Conclusion
The prevalence of S. pyogenes throat carriage among schoolchildren was intermediate in this study. However, it still poses a threat to children and the community. Parents who had low income, a history of admission to a hospital, and cigarette smokers in the house were significant predictors of throat carriage of S. pyogenes among schoolchildren. Penicillin and cefotaxime were fully active against all the isolates, but erythromycin and amoxicillin had relatively reduced activity in rural schoolchildren. Large community-based studies and continuous surveillance in antimicrobial resistance of S. pyogenes are paramount in elementary schools, and carriers shouldn’t be underestimated to decrease the spread and burden of S. pyogenes infection and its sequelae among children.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Acknowledgements
We would like to thank all participants of this research, all the study participants, and the directors of each elementary school for their active and voluntary participation and cooperation. We also thank all individuals who have in one way or another contributed to the completion of this research.
Abbreviations
- ARF
Acute rheumatoid fever
- CLSI
Clinical laboratory and standard institute
- IQR
Interquartile range
- IPA
Isopropanol
- RHD
Rheumatoid heart disease
- SPSS
Statistical package for the social sciences
- S. pyogenes
Streptococcus pyogenes
- STS
Streptococcal toxic shock syndrome
Author contributions
Yalewayker Gashaw contributed to the conception of the research idea, data collection, laboratory work, analysis, and interpretation, thesis preparation, and preparation of the manuscript. Baye Gelaw contributed to the conception of the research idea, supervision, thesis preparation, and review of the manuscript. Alem Getaneh contributed to the analysis and interpretation, supervision, thesis preparation, and review of the manuscript. Desie Kasew contributed to the analysis and interpretation, thesis preparation and supervision and Mitkie Tigabie contributed to the laboratory work, and review of the manuscript. All authors read and approved the final manuscript.
Data availability
The data sets generated during and/or analyzed during the current study are available from the corresponding authors upon reasonable request.
Declarations
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Data Availability Statement
The data sets generated during and/or analyzed during the current study are available from the corresponding authors upon reasonable request.