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Bushra Ahmed, E., Ali Abu Groun, E., Saad Almugadam, B., Musa Alobaid Ahmed, Y., Mudawe Nurain Mudawe, A., Abakar Babiker, N., & Abuzeid, N. (2023). Epidemiological Aspects and Antibiotics Susceptibility Patterns of Streptococcus pyogenes Isolated from Subjects with Tonsillitis, Sudan. Sudan Journal of Medical Sciences (SJMS), 18(1), 6–24. https://doi.org/10.18502/sjms.v18i1.12861
https://doi.org/10.18502/sjms.v18i1.12861
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authors
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Elnaim Bushra Ahmed
Elnaim Bushra Ahmed
Department of Microbiology, Faculty of Medical Laboratory Sciences, Omdurman Islamic University, Omdurman, Sudan
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Elsir Ali Abu Groun
Elsir Ali Abu Groun
Department of Microbiology, Faculty of Medical Laboratory Sciences, University of Khartoum, Khartoum, Sudan
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Babiker Saad Almugadam
Babiker Saad Almugadam
Department of Microbiology, Faculty of Medical Laboratory Sciences, University of El Imam El Mahdi, Sudan, Sudan
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Yousif Musa Alobaid Ahmed
Yousif Musa Alobaid Ahmed
Department of Microbiology, Faculty of Medical Laboratory Sciences, University of El Imam El Mahdi, Sudan, Sudan
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Aymen Mudawe Nurain Mudawe
Aymen Mudawe Nurain Mudawe
Delta College of Science and Technology, Omdurman , Sudan
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Nassir Abakar Babiker
Nassir Abakar Babiker
Central Medical Laboratory, Wad Medani Teaching Hospital for Obstetrics & Gynecology, Wad Medani, Sudan
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Nadir Abuzeid
Nadir Abuzeid
Department of Microbiology, Faculty of Medical Laboratory Sciences, Omdurman Islamic University, Omdurman, Sudan
Published Date
- Mar 31, 2023
Epidemiological Aspects and Antibiotics Susceptibility Patterns of Streptococcus pyogenes Isolated from Subjects with Tonsillitis, Sudan
Abstract
Background: Globally, Streptococcus pharyngitis is a major public health challenge. The current study investigates the prevalence of Streptococcal pyogenes among children under 17 years old in ENT Kosti Teaching Hospital and examines the susceptibility of isolated S. pyogenes strains to commonly used antibiotics.
Methods: A total of 384 throat swabs were obtained from children under the age of 17 who attended the Kosti Teaching Hospital between 2019 and 2021. Streptococcus pyogenes was isolated by conventional microbiology procedures. Each S. pyogenes strain was subjected to antibiotic susceptibility testing according to the CLSI guidelines.
Results: Most participants of this study were females 219 (57%) and aged between 5 and 10 years 259 (67.4%). Out of the 384 participants, 134 (34.9%) and 255 (66.4%) suffered from lymphadenopathy and tonsil hyperplasia, respectively. Interestingly, lymphadenopathy and tonsil hyperplasia were more (P 0.05) in the 5–10 age group than those aged 11–16 years. Moreover, 41.4% of the participants were infected by a GAS sore throat. GAS sore throat is significantly associated with lymphadenopathy (AOR: 2.375, 95% CI: 1.479–3.815, P 0.000) and tonsil hyperplasia (AOR: 3.374, 95% CI: 1.939–5.874, P 0.000). Notably, males (AOR: 0.853, 95% CI: 0.549–1.325, P 0.479) and individuals aged 5–10 years (AOR: 0.867, 95% CI: 0.464–1.618, P 0.654) were less likely to have a GAS sore throat. In our study, all isolated strains were sensitive to penicillin. Clindamycin, azithromycin, and erythromycin resistance were observed in 7 (4.4%), 44 (27.7%), and 47 (29.6%) isolates, respectively.
Conclusion: The study displayed the current situation of GAS sore throat in the White Nile state. Penicillin was found to be the effective drug to cure S. tonsillitis but a high rate of resistance to macrolides was noticed which is an alarming sign.
Keywords:
azithromycin, clindamycin, erythromycin, GAS, Streptococcus pyogenes
References
[1] Hurst, J. R., Kasper, K. J., Sule, A. N., & McCormick, J. K. (2018). Streptococcal pharyngitis and rheumatic heart disease: The superantigen hypothesis revisited. Infection, Genetics and Evolution, 61(1), 160–175.
[2] Pfoh, E., Wessels, M. R., Goldmann, D., Lee, G. M. (2008). Burden and economic cost of group A streptococcal pharyngitis. Pediatrics, 121(2), 229–234.
[3] May, P. J., Bowen, A. C., & Carapetis, J. R. (2016). The inequitable burden of group A streptococcal diseases in Indigenous Australians. Medical Journal of Australia, 205(5), 201–203.
[4] Marx, J., Hockberger, R., & Walls, R. (2013). Rosen's emergency medicine: Concepts and clinical practice. Elsevier Health Sciences E-Book: 2-Volume Set.
[5] Danchin, M. H., Rogers, S., Kelpie, L., Selvaraj, G., Curtis, N., Carlin, J. B., Nolan, T. M., & Carapetis, J. R. (2007). Burden of acute sore throat and group A streptococcal pharyngitis in school-aged children and their families in Australia. Pediatrics, 120(5), 950–957.
[6] Choby, B. A. (2009). Diagnosis and treatment of streptococcal pharyngitis. American Family Physician, 79(5), 383–390.
[7] Makthal, N., Vander Wal, A. R., Saavedra, M. O., Olsen, R. J., Musser, J. M., & Kumaraswami, M. (2019). Environmental pH and peptide signaling control virulence of Streptococcus pyogenes via a quorum-sensing pathway. Nature Communications, 10(1), 1–14.
[8] Carapetis, J. R., Currie, B. J., & Kaplan, E. L. (1999). Epidemiology and prevention of group A streptococcal infections: Acute respiratory tract infections, skin infections, and their sequelae at the close of the twentieth century. Clinical Infectious Diseases, 28(2), 205–210.
[9] Bisno, A. L., Rubin, F. A., Cleary, P. P., & Dale, J. B. (2005). Prospects for a group A streptococcal vaccine: Rationale, feasibility, and obstacles—Report of a National Institute of Allergy and Infectious Diseases workshop. Clinical Infectious Diseases, 41(8), 1150–1156.
[10] Carapetis, J. R., Steer, A. C., Mulholland, E. K., & Weber, M. (2005). The global burden of group A streptococcal diseases. The Lancet Infectious Diseases, 5(11), 685–694.
[11] Ralph, A. P., Fittock, M., Schultz, R., Thompson, D., Dowden, M., Clemens, T., Parnaby, M. G., Clark, M., McDonald, M. I., Edwards, K. N., & Carapetis, J. R. (2013). Improvement in rheumatic fever and rheumatic heart disease management and prevention using a health centre-based continuous quality improvement approach. BMC Health Services Research, 13(1), 1–13.
[12] May, P. J., Bowen, A. C., & Carapetis, J. R. (2016). The inequitable burden of group A streptococcal diseases in Indigenous Australians. Medical Journal of Australia, 205(5), 201–203.
[13] Oliver, J. R., Pierse, N., Stefanogiannis, N., Jackson, C., & Baker, M. G. (2017). Acute rheumatic fever and exposure to poor housing conditions in New Zealand: A descriptive study. Journal of Paediatrics and Child Health, 53(4), 358–364.
[14] Parks, T., Smeesters, P. R., & Steer, A. C. (2012). Streptococcal skin infection and rheumatic heart disease. Current Opinion in Infectious Diseases, 25(2), 145–153.
[15] Karacan, M., Karakelleoğlu, C., & Orbak, Z. (2007). Diagnosis of group A beta-hemolytic Streptococcus using the Breese clinical scoring system. Southern Medical Journal, 100(12), 1192–1197.
[16] Dale, A. P., Marchello, C., & Ebell, M. H. (2019). Clinical gestalt to diagnose pneumonia, sinusitis, and pharyngitis: A meta-analysis. British Journal of General Practice, 69(684), e444–e453.
[17] Karmarkar, M. G., Venugopal, V., Joshi, L., & Kamboj, R. (2004). Evaluation & revaluation of upper limits of normal values of anti-streptolysin O & anti-deoxyribonuclease B in Mumbai. Indian Journal of Medical Research, 119, 26–28.
[18] Sharma, Y., Vishwanath, S., & Bairy, I. (2010). Biotype and antibiotic resistance pattern of group A streptococci. Indian Journal of Pathology and Microbiology, 53(1), 187.
[19] Ray, D., Sinha, S., Saha, S., Karmakar, S., Dutta, R. N., Bhattacharya, S., Pal, N. K., & Bhattacharya, B. (2010). A preliminary sentinel surveillance report on antibiotics resistance trend of Streptococcus pyogenes in Kolkata region, India. Al Ameen Journal of Medical Sciences, 3(2), 146–151.
[20] Bourbeau, P. P. (2003). Role of the microbiology laboratory in diagnosis and management of pharyngitis. Journal of Clinical Microbiology, 41(8), 3467–3472.
[21] Zhou, W., Jiang, Y. M., Wang, H. J., Kuang, L. H., Hu, Z. Q., Shi, H., Shu, M., & Wa, C. M. (2014). Erythromycin-resistant genes in group A β-haemolytic Streptococci in Chengdu, Southwestern China. Indian Journal of Medical Microbiology, 32(3), 290–293.
[22] World Health Organization. (2015). The current evidence for the burden of group streptococcal diseases [Discussion papers on Child Health]. Department of Child and Adolescent Health and Development, WHO. http://whqlibdoc.who.int/hq/ 2005/WHO_FCH_CAH_05.07.pdf
[23] Al Fadhil, A. O. O. Bacteriology of sore throats in a Sudanese population.
[24] Abdelwahab, O. I., Eljak, M. A., & Suliman, A. M. (2014). Isolation and identification of Streptococcus pyogenes in patients with sore throat [Doctoral dissertation, Sudan University of Science and Technology].
[25] Mohammed, N. A. (2016). Bacterial isolates associated with tonsillitis in Khartoum (Sudan). African Journal of Medical Sciences, 1(9), 1–5.
[26] Ahmed, E. B., Adam, A. M., Bakhiet, A. A., & Almugadam, B. S. (2018). Association of Streptococcus pyogenes with symptomatic pharyngitis in Kosti City, Sudan. Research & Reviews: Journal of Microbiology and Biotechnology, 7(1), 19–21.
[27] Clinical and Laboratory Standards Institute (CLSI). (2018). Performance standards for antimicrobial susceptibility testing. 28th Ed. Wayne, Pennsylvania: Clinical and Laboratory Standards Institute.
[28] Gherardi, G., Petrelli, D., Di Luca, M. C., De Araujo, F. P., Bernaschi, P., Repetto, A., Bellesi, J., & Vitali, L. A. (2015). Decline in macrolide resistance rates among Streptococcus pyogenes causing pharyngitis in children isolated in Italy. European Journal of Clinical Microbiology & Infectious Diseases, 34(9), 1797–1802.
[29] Bisno, A. L., Brito, M. O., & Collins, C. M. (2003). Molecular basis of group A streptococcal virulence. The Lancet Infectious Diseases, 3(4), 191–200.
[30] Uzodimma, C. C., Dedeke, F. I., Nwadike, V., Owolabi, O., Arifalo, G., & Oduwole, O. (2017). A study of group a streptococcal pharyngitis among 3–15-year-old children attending clinics for an acute sore throat. Nigerian Journal of Cardiology, 14(2), 97.
[31] Sultan, A. M., & Seliem, W. A. (2018). Evaluating the use of dedicated swab for rapid antigen detection testing in group a streptococcal pharyngitis in children. African Journal of Clinical and Experimental Microbiology, 19(1), 24–29.
[32] Osowicki, J., Azzopardi, K. I., Baker, C., Waddington, C. S., Pandey, M., Schuster, T., Grobler, A., Cheng, A. C., Pollard, A. J., McCarthy, J. S., & Good, M. F. ( 2019). Controlled human infection for vaccination against Streptococcus pyogenes (CHIVAS): Establishing a group A Streptococcus pharyngitis human infection study. Vaccine, 37(26), 3485–3494.
[33] Tesfaw, G., Kibru, G., Mekonnen, D., & Abdissa, A. (2015). Prevalence of group A β-haemolytic Streptococcus among children with pharyngitis in Jimma town, Southwest Ethiopia. Egyptian Journal of Ear, Nose, Throat and Allied Sciences, 16(1), 35–40.
[34] Vijayashree, M. S., Viswanatha, B., & Sambamurthy, B. N. (2014). Clinical and bacteriological study of acute tonsillitis. IOSR Journal of Dental and Medical Sciences, 13(1), 37–43.
[35] Singh, A. K., Kumar, A., Agarwal, L., Agarwal, A., & Sengupta, C. )2015(. Prevalence of group A streptococcal pharyngitis among schoolchildren of Barabanki district, Uttar Pradesh, India. Journal of the Academy of Clinical Microbiologists, 17(2), 110.
[36] Le Hello, S., Doloy, A., Baumann, F., Roques, N., Coudene, P., Rouchon, B., & Bouvet, A. )2010(. Clinical and microbial characteristics of invasive Streptococcus pyogenes disease in New Caledonia, a region in Oceania with a high incidence of acute rheumatic fever. Journal of Clinical Microbiology, 48(2), 526–530.
[37] Bahnan, W., Hashwa, F., Araj, G., & Tokajian, S. (2011), Emm typing, antibiotic resistance and PFGE analysis of Streptococcus pyogenes in Lebanon. Journal of Medical Microbiology, 60(1), 98–101.
[38] Wu, P. C., Lo, W. T., Chen, S. J., & Wang, C. C. (2014). Molecular characterization of group A streptococcal isolates causing scarlet fever and pharyngitis among young children: A retrospective study from a northern Taiwan medical center. Journal of Microbiology, Immunology and Infection, 47(4), 304–310.
[39] Khosravi, A. D., Ebrahimifard, N., Shamsizadeh, A., & Shoja, S. (2016). Isolation of Streptococcus pyogenes from children with pharyngitis and emm type analysis. Journal of the Chinese Medical Association, 79(5), 276–280.
[40] Ibrahim, S. B., El-Sokkary, R. H., Elhewala, A. A., El-Anwar, M. W., Awad, W. M., Hamed, A. M., & Badawy, I. I. (2014). Emerging resistance to erythromycin and penicillin among Streptococcus pyogenes isolates in Zagazig, Egypt. International Journal of Current Microbiology and Applied Sciences, 3(10), 750–756.
[41] Kaplan, E. L., Chhatwal, G. S., & Rohde, M. (2006). Reduced ability of penicillin to eradicate ingested group A streptococci from epithelial cells: Clinical and pathogenetic implications. Clinical Infectious Diseases, 43(11), 1398–1406.
[42] Ogawa, T., Terao, Y., Okuni, H., Ninomiya, K., Sakata, H., Ikebe, K., Maeda, Y., & Kawabata, S. (2011). Biofilm formation or internalization into epithelial cells enable Streptococcus pyogenes to evade antibiotic eradication in patients with pharyngitis. Microbial Pathogenesis, 51(1–2), 58–68.
[43] Brook, I., & Gober, A. E. (2008). Failure to eradicate streptococci and beta‐lactamase producing bacteria. Acta Paediatrica, 97(2), 193–195.
[44] Brook, I. (2013). Penicillin failure in the treatment of streptococcal pharyngo-tonsillitis. Current Infectious Disease Reports, 15(3), 232–235.
[45] Karaky, N. M., Araj, G. F., & Tokajian, S. T. (2014). Molecular characterization of Streptococcus pyogenes group A isolates from a tertiary hospital in Lebanon. Journal of Medical Microbiology, 63(9), 1197–1204.
[46] Syrogiannopoulos, G. A., Grivea, I. N., Al-Lahham, A., Panagiotou, M., Tsantouli, A. G., Michoula Ralf René Reinert, A. N., & van der Linden, M. (2013). Seven-year surveillance of emm types of pediatric group A streptococcal pharyngitis isolates in Western Greece. PLoS One, 8(8), e71558.
[47] Sayyahfar, S., Fahimzad, A., Naddaf, A., & Tavassoli, S. (2015).Antibiotic susceptibility evaluation of group A streptococcus isolated from children with pharyngitis: A study from Iran. Infection & Chemotherapy, 47(4), 225–230.
[48] Littauer, P., Caugant, D. A., Sangvik, M., Høiby, E. A., Sundsfjord, A., & Simonsen, G. S. (2006). Macrolide-resistant Streptococcus pyogenes in Norway: Population structure and resistance determinants. Antimicrobial Agents and Chemotherapy, 50(5), 1896–1899.
[49] Villaseñor-Sierra, A., Katahira, E., Jaramillo-Valdivia, A. N., de los Angeles Barajas-García, M., Bryant, A., Morfín-Otero, R., Márquez-Díaz, F., Tinoco, J. C., Sánchez-Corona, J., & Stevens, D. L. (2012). Phenotypes and genotypes of erythromycin-resistant Streptococcus pyogenes strains isolated from invasive and non-invasive infections from Mexico and the USA during 1999–2010. International Journal of Infectious Diseases, 16(3), e178–e181.
[50] Plainvert, C., Doloy, A., Loubinoux, J., Lepoutre, A., Collobert, G., Touak, G., Trieu-Cuot, P., Bouvet, A., Poyart, C., CNR-Strep network. (2012). Invasive group A streptococcal infections in adults, France (2006–2010). Clinical Microbiology and Infection, 18(7), 702–710.
[51] Montes, M., Tamayo, E., Mojica, C., García-Arenzana, J. M., Esnal, O., & Pérez-Trallero, E. (2014). What causes decreased erythromycin resistance in Streptococcus pyogenes? Dynamics of four clones in a southern European region from 2005 to 2012. Journal of Antimicrobial Chemotherapy, 69(6), 1474–1482.
[52] Ksia, S., Smaoui, H., Hraoui, M., Bouafsoun, A., Boutiba-Ben Boubaker, I., & Kechrid, A. (2017). Molecular characteristics of erythromycin-resistant Streptococcus pyogenes strains isolated from children patients in Tunis, Tunisia. Microbial Drug Resistance, 23(5), 633–639.
[53] Huang, C. Y., Lai, J. F., Huang, I. W., Chen, P. C., Wang, H. Y., Shiau, Y. R., Cheng, Y.-W., Hsieh, L.-Y., Chang, S.-C., & Lauderdale, T. L. Y. (2014). Epidemiology and molecular characterization of macrolide-resistant Streptococcus pyogenes in Taiwan. Journal of Clinical Microbiology, 52(2), 508–516.
[54] Sayyahfar, S., Fahimzad, A., Naddaf, A., & Tavassoli, S. (2015). Antibiotic susceptibility evaluation of group A streptococcus isolated from children with pharyngitis: A study from Iran. Infection & Chemotherapy, 47(4), 225–230.
[55] Kim, H.Y., & Uh, Y. (2004). Macrolide resistance in β-hemolytic streptococci: Changes after the implementation of the separation of prescribing and dispensing of medications policy in Korea. Yonsei Medical Journal, 45(4), 591–597.
[56] Michos, A. G., Bakoula, C. G., Braoudaki, M., Koutouzi, F. I., Roma, E. S., Pangalis, A., Nikolopoulou, G., Kirikou, E., & Syriopoulou, V. P. (2009). Macrolide resistance in Streptococcus pyogenes: Prevalence, resistance determinants, and emm types. Diagnostic Microbiology and Infectious Disease, 64(3), 295–299.
[57] Richter, S. S., Heilmann, K. P., Beekmann, S. E., Miller, N. J., Miller, A. L., Rice, C. L., Doern, C. D., Reid, S. D., & Doern, G. V. (2005). Macrolide-resistant Streptococcus pyogenes in the United States, 2002–2003. Clinical Infectious Diseases, 41(5), 599–608.
[58] Sharma, S., Praveen, S., Devi, K. S., Sahoo, B., Singh, W. S., & Singh, T. D. (2014). Prevalance of Streptococcus pyogenes infection in children aged between 5 to 15 years with acute tonsillopharyngitis and its antibiogram. IOSR Journal of Dental and Medical Sciences (IOSR-JDMS), 1(13), 50–55.
[59] Rijal, K. R., Dhakal, N., Shah, R. C., Timilsina, S., Mahato, P., & Thapa, S. (2009). Antibiotic susceptibility of group A Streptococcus isolated from throat swab culture of school children in Pokhara, Nepal. Nepal Medical College Journal, 11(4), 238–240.
[2] Pfoh, E., Wessels, M. R., Goldmann, D., Lee, G. M. (2008). Burden and economic cost of group A streptococcal pharyngitis. Pediatrics, 121(2), 229–234.
[3] May, P. J., Bowen, A. C., & Carapetis, J. R. (2016). The inequitable burden of group A streptococcal diseases in Indigenous Australians. Medical Journal of Australia, 205(5), 201–203.
[4] Marx, J., Hockberger, R., & Walls, R. (2013). Rosen's emergency medicine: Concepts and clinical practice. Elsevier Health Sciences E-Book: 2-Volume Set.
[5] Danchin, M. H., Rogers, S., Kelpie, L., Selvaraj, G., Curtis, N., Carlin, J. B., Nolan, T. M., & Carapetis, J. R. (2007). Burden of acute sore throat and group A streptococcal pharyngitis in school-aged children and their families in Australia. Pediatrics, 120(5), 950–957.
[6] Choby, B. A. (2009). Diagnosis and treatment of streptococcal pharyngitis. American Family Physician, 79(5), 383–390.
[7] Makthal, N., Vander Wal, A. R., Saavedra, M. O., Olsen, R. J., Musser, J. M., & Kumaraswami, M. (2019). Environmental pH and peptide signaling control virulence of Streptococcus pyogenes via a quorum-sensing pathway. Nature Communications, 10(1), 1–14.
[8] Carapetis, J. R., Currie, B. J., & Kaplan, E. L. (1999). Epidemiology and prevention of group A streptococcal infections: Acute respiratory tract infections, skin infections, and their sequelae at the close of the twentieth century. Clinical Infectious Diseases, 28(2), 205–210.
[9] Bisno, A. L., Rubin, F. A., Cleary, P. P., & Dale, J. B. (2005). Prospects for a group A streptococcal vaccine: Rationale, feasibility, and obstacles—Report of a National Institute of Allergy and Infectious Diseases workshop. Clinical Infectious Diseases, 41(8), 1150–1156.
[10] Carapetis, J. R., Steer, A. C., Mulholland, E. K., & Weber, M. (2005). The global burden of group A streptococcal diseases. The Lancet Infectious Diseases, 5(11), 685–694.
[11] Ralph, A. P., Fittock, M., Schultz, R., Thompson, D., Dowden, M., Clemens, T., Parnaby, M. G., Clark, M., McDonald, M. I., Edwards, K. N., & Carapetis, J. R. (2013). Improvement in rheumatic fever and rheumatic heart disease management and prevention using a health centre-based continuous quality improvement approach. BMC Health Services Research, 13(1), 1–13.
[12] May, P. J., Bowen, A. C., & Carapetis, J. R. (2016). The inequitable burden of group A streptococcal diseases in Indigenous Australians. Medical Journal of Australia, 205(5), 201–203.
[13] Oliver, J. R., Pierse, N., Stefanogiannis, N., Jackson, C., & Baker, M. G. (2017). Acute rheumatic fever and exposure to poor housing conditions in New Zealand: A descriptive study. Journal of Paediatrics and Child Health, 53(4), 358–364.
[14] Parks, T., Smeesters, P. R., & Steer, A. C. (2012). Streptococcal skin infection and rheumatic heart disease. Current Opinion in Infectious Diseases, 25(2), 145–153.
[15] Karacan, M., Karakelleoğlu, C., & Orbak, Z. (2007). Diagnosis of group A beta-hemolytic Streptococcus using the Breese clinical scoring system. Southern Medical Journal, 100(12), 1192–1197.
[16] Dale, A. P., Marchello, C., & Ebell, M. H. (2019). Clinical gestalt to diagnose pneumonia, sinusitis, and pharyngitis: A meta-analysis. British Journal of General Practice, 69(684), e444–e453.
[17] Karmarkar, M. G., Venugopal, V., Joshi, L., & Kamboj, R. (2004). Evaluation & revaluation of upper limits of normal values of anti-streptolysin O & anti-deoxyribonuclease B in Mumbai. Indian Journal of Medical Research, 119, 26–28.
[18] Sharma, Y., Vishwanath, S., & Bairy, I. (2010). Biotype and antibiotic resistance pattern of group A streptococci. Indian Journal of Pathology and Microbiology, 53(1), 187.
[19] Ray, D., Sinha, S., Saha, S., Karmakar, S., Dutta, R. N., Bhattacharya, S., Pal, N. K., & Bhattacharya, B. (2010). A preliminary sentinel surveillance report on antibiotics resistance trend of Streptococcus pyogenes in Kolkata region, India. Al Ameen Journal of Medical Sciences, 3(2), 146–151.
[20] Bourbeau, P. P. (2003). Role of the microbiology laboratory in diagnosis and management of pharyngitis. Journal of Clinical Microbiology, 41(8), 3467–3472.
[21] Zhou, W., Jiang, Y. M., Wang, H. J., Kuang, L. H., Hu, Z. Q., Shi, H., Shu, M., & Wa, C. M. (2014). Erythromycin-resistant genes in group A β-haemolytic Streptococci in Chengdu, Southwestern China. Indian Journal of Medical Microbiology, 32(3), 290–293.
[22] World Health Organization. (2015). The current evidence for the burden of group streptococcal diseases [Discussion papers on Child Health]. Department of Child and Adolescent Health and Development, WHO. http://whqlibdoc.who.int/hq/ 2005/WHO_FCH_CAH_05.07.pdf
[23] Al Fadhil, A. O. O. Bacteriology of sore throats in a Sudanese population.
[24] Abdelwahab, O. I., Eljak, M. A., & Suliman, A. M. (2014). Isolation and identification of Streptococcus pyogenes in patients with sore throat [Doctoral dissertation, Sudan University of Science and Technology].
[25] Mohammed, N. A. (2016). Bacterial isolates associated with tonsillitis in Khartoum (Sudan). African Journal of Medical Sciences, 1(9), 1–5.
[26] Ahmed, E. B., Adam, A. M., Bakhiet, A. A., & Almugadam, B. S. (2018). Association of Streptococcus pyogenes with symptomatic pharyngitis in Kosti City, Sudan. Research & Reviews: Journal of Microbiology and Biotechnology, 7(1), 19–21.
[27] Clinical and Laboratory Standards Institute (CLSI). (2018). Performance standards for antimicrobial susceptibility testing. 28th Ed. Wayne, Pennsylvania: Clinical and Laboratory Standards Institute.
[28] Gherardi, G., Petrelli, D., Di Luca, M. C., De Araujo, F. P., Bernaschi, P., Repetto, A., Bellesi, J., & Vitali, L. A. (2015). Decline in macrolide resistance rates among Streptococcus pyogenes causing pharyngitis in children isolated in Italy. European Journal of Clinical Microbiology & Infectious Diseases, 34(9), 1797–1802.
[29] Bisno, A. L., Brito, M. O., & Collins, C. M. (2003). Molecular basis of group A streptococcal virulence. The Lancet Infectious Diseases, 3(4), 191–200.
[30] Uzodimma, C. C., Dedeke, F. I., Nwadike, V., Owolabi, O., Arifalo, G., & Oduwole, O. (2017). A study of group a streptococcal pharyngitis among 3–15-year-old children attending clinics for an acute sore throat. Nigerian Journal of Cardiology, 14(2), 97.
[31] Sultan, A. M., & Seliem, W. A. (2018). Evaluating the use of dedicated swab for rapid antigen detection testing in group a streptococcal pharyngitis in children. African Journal of Clinical and Experimental Microbiology, 19(1), 24–29.
[32] Osowicki, J., Azzopardi, K. I., Baker, C., Waddington, C. S., Pandey, M., Schuster, T., Grobler, A., Cheng, A. C., Pollard, A. J., McCarthy, J. S., & Good, M. F. ( 2019). Controlled human infection for vaccination against Streptococcus pyogenes (CHIVAS): Establishing a group A Streptococcus pharyngitis human infection study. Vaccine, 37(26), 3485–3494.
[33] Tesfaw, G., Kibru, G., Mekonnen, D., & Abdissa, A. (2015). Prevalence of group A β-haemolytic Streptococcus among children with pharyngitis in Jimma town, Southwest Ethiopia. Egyptian Journal of Ear, Nose, Throat and Allied Sciences, 16(1), 35–40.
[34] Vijayashree, M. S., Viswanatha, B., & Sambamurthy, B. N. (2014). Clinical and bacteriological study of acute tonsillitis. IOSR Journal of Dental and Medical Sciences, 13(1), 37–43.
[35] Singh, A. K., Kumar, A., Agarwal, L., Agarwal, A., & Sengupta, C. )2015(. Prevalence of group A streptococcal pharyngitis among schoolchildren of Barabanki district, Uttar Pradesh, India. Journal of the Academy of Clinical Microbiologists, 17(2), 110.
[36] Le Hello, S., Doloy, A., Baumann, F., Roques, N., Coudene, P., Rouchon, B., & Bouvet, A. )2010(. Clinical and microbial characteristics of invasive Streptococcus pyogenes disease in New Caledonia, a region in Oceania with a high incidence of acute rheumatic fever. Journal of Clinical Microbiology, 48(2), 526–530.
[37] Bahnan, W., Hashwa, F., Araj, G., & Tokajian, S. (2011), Emm typing, antibiotic resistance and PFGE analysis of Streptococcus pyogenes in Lebanon. Journal of Medical Microbiology, 60(1), 98–101.
[38] Wu, P. C., Lo, W. T., Chen, S. J., & Wang, C. C. (2014). Molecular characterization of group A streptococcal isolates causing scarlet fever and pharyngitis among young children: A retrospective study from a northern Taiwan medical center. Journal of Microbiology, Immunology and Infection, 47(4), 304–310.
[39] Khosravi, A. D., Ebrahimifard, N., Shamsizadeh, A., & Shoja, S. (2016). Isolation of Streptococcus pyogenes from children with pharyngitis and emm type analysis. Journal of the Chinese Medical Association, 79(5), 276–280.
[40] Ibrahim, S. B., El-Sokkary, R. H., Elhewala, A. A., El-Anwar, M. W., Awad, W. M., Hamed, A. M., & Badawy, I. I. (2014). Emerging resistance to erythromycin and penicillin among Streptococcus pyogenes isolates in Zagazig, Egypt. International Journal of Current Microbiology and Applied Sciences, 3(10), 750–756.
[41] Kaplan, E. L., Chhatwal, G. S., & Rohde, M. (2006). Reduced ability of penicillin to eradicate ingested group A streptococci from epithelial cells: Clinical and pathogenetic implications. Clinical Infectious Diseases, 43(11), 1398–1406.
[42] Ogawa, T., Terao, Y., Okuni, H., Ninomiya, K., Sakata, H., Ikebe, K., Maeda, Y., & Kawabata, S. (2011). Biofilm formation or internalization into epithelial cells enable Streptococcus pyogenes to evade antibiotic eradication in patients with pharyngitis. Microbial Pathogenesis, 51(1–2), 58–68.
[43] Brook, I., & Gober, A. E. (2008). Failure to eradicate streptococci and beta‐lactamase producing bacteria. Acta Paediatrica, 97(2), 193–195.
[44] Brook, I. (2013). Penicillin failure in the treatment of streptococcal pharyngo-tonsillitis. Current Infectious Disease Reports, 15(3), 232–235.
[45] Karaky, N. M., Araj, G. F., & Tokajian, S. T. (2014). Molecular characterization of Streptococcus pyogenes group A isolates from a tertiary hospital in Lebanon. Journal of Medical Microbiology, 63(9), 1197–1204.
[46] Syrogiannopoulos, G. A., Grivea, I. N., Al-Lahham, A., Panagiotou, M., Tsantouli, A. G., Michoula Ralf René Reinert, A. N., & van der Linden, M. (2013). Seven-year surveillance of emm types of pediatric group A streptococcal pharyngitis isolates in Western Greece. PLoS One, 8(8), e71558.
[47] Sayyahfar, S., Fahimzad, A., Naddaf, A., & Tavassoli, S. (2015).Antibiotic susceptibility evaluation of group A streptococcus isolated from children with pharyngitis: A study from Iran. Infection & Chemotherapy, 47(4), 225–230.
[48] Littauer, P., Caugant, D. A., Sangvik, M., Høiby, E. A., Sundsfjord, A., & Simonsen, G. S. (2006). Macrolide-resistant Streptococcus pyogenes in Norway: Population structure and resistance determinants. Antimicrobial Agents and Chemotherapy, 50(5), 1896–1899.
[49] Villaseñor-Sierra, A., Katahira, E., Jaramillo-Valdivia, A. N., de los Angeles Barajas-García, M., Bryant, A., Morfín-Otero, R., Márquez-Díaz, F., Tinoco, J. C., Sánchez-Corona, J., & Stevens, D. L. (2012). Phenotypes and genotypes of erythromycin-resistant Streptococcus pyogenes strains isolated from invasive and non-invasive infections from Mexico and the USA during 1999–2010. International Journal of Infectious Diseases, 16(3), e178–e181.
[50] Plainvert, C., Doloy, A., Loubinoux, J., Lepoutre, A., Collobert, G., Touak, G., Trieu-Cuot, P., Bouvet, A., Poyart, C., CNR-Strep network. (2012). Invasive group A streptococcal infections in adults, France (2006–2010). Clinical Microbiology and Infection, 18(7), 702–710.
[51] Montes, M., Tamayo, E., Mojica, C., García-Arenzana, J. M., Esnal, O., & Pérez-Trallero, E. (2014). What causes decreased erythromycin resistance in Streptococcus pyogenes? Dynamics of four clones in a southern European region from 2005 to 2012. Journal of Antimicrobial Chemotherapy, 69(6), 1474–1482.
[52] Ksia, S., Smaoui, H., Hraoui, M., Bouafsoun, A., Boutiba-Ben Boubaker, I., & Kechrid, A. (2017). Molecular characteristics of erythromycin-resistant Streptococcus pyogenes strains isolated from children patients in Tunis, Tunisia. Microbial Drug Resistance, 23(5), 633–639.
[53] Huang, C. Y., Lai, J. F., Huang, I. W., Chen, P. C., Wang, H. Y., Shiau, Y. R., Cheng, Y.-W., Hsieh, L.-Y., Chang, S.-C., & Lauderdale, T. L. Y. (2014). Epidemiology and molecular characterization of macrolide-resistant Streptococcus pyogenes in Taiwan. Journal of Clinical Microbiology, 52(2), 508–516.
[54] Sayyahfar, S., Fahimzad, A., Naddaf, A., & Tavassoli, S. (2015). Antibiotic susceptibility evaluation of group A streptococcus isolated from children with pharyngitis: A study from Iran. Infection & Chemotherapy, 47(4), 225–230.
[55] Kim, H.Y., & Uh, Y. (2004). Macrolide resistance in β-hemolytic streptococci: Changes after the implementation of the separation of prescribing and dispensing of medications policy in Korea. Yonsei Medical Journal, 45(4), 591–597.
[56] Michos, A. G., Bakoula, C. G., Braoudaki, M., Koutouzi, F. I., Roma, E. S., Pangalis, A., Nikolopoulou, G., Kirikou, E., & Syriopoulou, V. P. (2009). Macrolide resistance in Streptococcus pyogenes: Prevalence, resistance determinants, and emm types. Diagnostic Microbiology and Infectious Disease, 64(3), 295–299.
[57] Richter, S. S., Heilmann, K. P., Beekmann, S. E., Miller, N. J., Miller, A. L., Rice, C. L., Doern, C. D., Reid, S. D., & Doern, G. V. (2005). Macrolide-resistant Streptococcus pyogenes in the United States, 2002–2003. Clinical Infectious Diseases, 41(5), 599–608.
[58] Sharma, S., Praveen, S., Devi, K. S., Sahoo, B., Singh, W. S., & Singh, T. D. (2014). Prevalance of Streptococcus pyogenes infection in children aged between 5 to 15 years with acute tonsillopharyngitis and its antibiogram. IOSR Journal of Dental and Medical Sciences (IOSR-JDMS), 1(13), 50–55.
[59] Rijal, K. R., Dhakal, N., Shah, R. C., Timilsina, S., Mahato, P., & Thapa, S. (2009). Antibiotic susceptibility of group A Streptococcus isolated from throat swab culture of school children in Pokhara, Nepal. Nepal Medical College Journal, 11(4), 238–240.