Variations in the frequency of streptococcal tonsillopharyngitis among children after COVID-19

Öz

Aim: Comprehensive data on the variations in the frequency of Streptococcus pyogenes (GAS) tonsillopharyngitis before and after the Coronavirus disease 2019 (COVID-19) pandemic are still insufficient. This study aimed to investigate the changes in the frequency of GAS in children before, during, and after the COVID-19 period. Material and Methods: This retrospective study included 13,061 patients diagnosed with a pre-diagnosis of bacterial tonsillopharyngitis based on clinical findings, between June 2018 and June 2023. All patients were administered the Strep A antigen test, and throat swab samples were collected. Patients were divided into three groups based on their hospital admission dates. Group 1, pre-COVID-19 pandemic period (1 January 2018 – 10 March 2020); Group 2, during the COVID-19 pandemic when strict measures were enforced (11 March 2020 – 30 June 2021); and Group 3, the period after the lifting of COVID-19 pandemic measures (1 July 2021 – 30 June 2023). Results: The prevalence of GAS in the entire population was 23.2% (n=3024). Among the groups, Group 3 had the highest ratio of GAS cases, followed by Group 1, and then Group 2 (Group 1: 18.1%, Group 2: 6.0%, Group 3: 29.6%, p < 0.001). During the period characterized by stringent measures against the COVID-19 pandemic, a significant reduction in the frequency of GAS was observed in comparison to the pre-COVID-19 era. However, with the relaxation of COVID-19-related restrictions, particularly in the last quarter of 2022 and the spring of 2023, there was a marked increase in the frequency of GAS. Conclusion: In children, the frequency of GAS significantly decreases with COVID-19 isolation measures. However, a rebound increase is observed following the relaxation of these isolation measures.

Anahtar Kelimeler

• Group A β-hemolytic streptococcus
• COVID-19
• strep A rapid test
• tonsillopharyngitis

Proje Numarası

Decision No: 23-48, Date: 22.09.2023

Etik Beyan

Çalışma Helsinki Bildirgesi'ne uygun olarak yapıldı ve Hisar Hospital Intercontinental Etik Kurulu tarafından onaylandı (Tarih: 22.09.2023, Karar No: 23-48).

Çocuklarda COVID-19 sonrası streptokokal tonsillofarenjit sıklığındaki değişiklikler

Öz

Amaç: Koronavirus hastalığı 2019 (COVID-19) pandemisi öncesi ve sonrasında Streptococcus pyogenes (GAS) tonsillofarenjit sıklığında yaşanan değişikliklere ilişkin kapsamlı veriler yetersizdir. Bu çalışmada, COVID-19 dönemi öncesi, sırası ve sonrasında çocuklarda GAS sıklığında meydana gelen değişiklikleri incelemeyi amaçlanmıştır. Gereç ve Yöntemler: Bu retrospektif çalışmaya, Haziran 2018 ile Haziran 2023 tarihleri arasında klinik bulgularla bakteriyel tonsillofarenjit ön tanısı alan 13,061 çocuk hasta dahil edildi. Tüm hastalara Strep A antijen testi yapılmış ve boğaz sürüntü örnekleri toplanmıştır. Hastalar, hastaneye başvuru tarihlerine göre üç gruba ayrıldı: Grup 1, COVID-19 pandemisi öncesi dönem (1 Ocak 2018 - 10 Mart 2020); Grup 2, COVID-19 pandemisi sırasında sıkı önlemlerin uygulandığı dönem (11 Mart 2020 - 30 Haziran 2021); ve Grup 3, COVID-19 pandemisi önlemlerinin kaldırıldığı dönem (1 Temmuz 2021 - 30 Haziran 2023). Bulgular: Tüm popülasyonda GAS prevalansı %23.2 (n=3024) idi. Gruplar arasında, Grup 3 en yüksek GAS sıklığına sahipken, bunu Grup 1 ve ardından Grup 2 izledi (Grup 1: %18.1, Grup 2: %6.0, Grup 3: %29.6, p < 0.001). COVID-19 pandemisine karşı katı önlemlerin alındığı dönemde, COVID-19 öncesi döneme kıyasla GAS sıklığında önemli bir azalma gözlemlendi. Ancak, COVID-19 ile ilişkili kısıtlamaların gevşetilmesiyle, özellikle 2022'nin son çeyreği ve 2023 ilkbaharında, GAS sıklığında belirgin bir artış saptandı. Sonuçlar: Çocuklarda, GAS sıklığı COVID-19 izolasyon önlemleriyle önemli ölçüde azaldı. Ancak, bu izolasyon önlemlerinin gevşetilmesinin ardından ani bir artış gözlemlendi.

Anahtar Kelimeler

• Grup A Beta-Hemolitik Streptokok
• COVID-19
• hızlı strep A testi
• tonsillofarenjit

Proje Numarası

Decision No: 23-48, Date: 22.09.2023

Etik Beyan

The study was performed in accordance with the Declaration of Helsinki, and was approved by the Hisar Intercontinental Hospital Ethics Committee (Date: 22.09.2023, Decision No: 23-48).

Kaynakça

1. Mustafa Z, Ghaffari M. Diagnostic methods, clinical guidelines, and antibiotic treatment for Group A Streptococcal Pharyngitis: A narrative review. Front Cell Infect Microbiol. 2020;10:563627.
2. Shaikh N, Leonard E, Martin JM. Prevalence of streptococcal pharyngitis and streptococcal carriage in children: a meta-analysis. Pediatrics. 2010;126:e557-564.
3. Walker MJ, Barnett TC, McArthur JD, et al. Disease manifestations and pathogenic mechanisms of Group A Streptococcus. Clin Microbiol Rev. 2014;27:264-301.
4. Smith KL, Hughes R, Myrex P. Tonsillitis and tonsilloliths: Diagnosis and management. Am Fam Physician. 2023;107:35-41.
5. Avire NJ, Whiley H, Ross K. A Review of Streptococcus pyogenes: Public health risk factors, prevention and control. Pathogens. 2021;10:248.
6. Windfuhr JP, Toepfner N, Steffen G, Waldfahrer F, Berner R. Clinical practice guideline: Tonsillitis I. Diagnostics and nonsurgical management. Eur Arch Otorhinolaryngol. 2016;273:973-987.
7. Herrera AL, Huber VC, Chaussee MS. The association between invasive Group A Streptococcal diseases and viral respiratory tract infections. Front Microbiol. 2016;7:342.
8. Morens DM, Fauci AS. The 1918 influenza pandemic: insights for the 21st century. J Infect Dis. 2007;195:1018-1028.

9. Zakikhany K, Degail MA, Lamagni T, et al. Increase in invasive Streptococcus pyogenes and Streptococcus pneumoniae infections in England, December 2010 to January 2011. Euro Surveill. 2011;16:19785.
10. Jean C, Louie JK, Glaser CA, et al. Invasive Group A streptococcal infection concurrent with 2009 H1N1 influenza. Clin Infect Dis. 2010;50:e59-62.
11. Prasad N, Rhodes J, Deng L, et al. Changes in the incidence of invasive bacterial disease during the COVID-19 pandemic in the United States, 2014-2020. J Infect Dis. 2023;227:907-916.
12. Cobo-Vazquez E, Aguilera-Alonso D, Carrasco-Colom J, Calvo C, Saavedra-Lozano JPed GASnWG. Increasing incidence and severity of invasive Group A streptococcal disease in Spanish children in 2019-2022. Lancet Reg Health Eur. 2023;27:100597.
13. Abo YN, Oliver J, McMinn A, et al. Increase in invasive Group A Streptococcal disease among Australian children coinciding with northern hemisphere surges. Lancet Reg Health West Pac. 2023;41:100873.
14. WHO. Increased incidence of scarlet fever and invasive Group A Streptococcus infection – multi-country. 15 December 2022 [cited 2024 15 January]; Available from: https://www.who.int/emergencies/disease-outbreak-news/item/2022-DON429.
15. Johannesen TB, Munkstrup C, Edslev SM, et al. Increase in invasive Group A Streptococcal infections and emergence of novel, rapidly expanding sub-lineage of the virulent Streptococcus pyogenes M1 clone, Denmark, 2023. Euro Surveill. 2023;28:2300291.
16. van der Putten BCL, Vlaminckx BJM, de Gier B, Freudenburg-de Graaf W, van Sorge NM. Group A Streptococcal meningitis with the M1UK variant in the Netherlands. JAMA. 2023;329:1791-1792.
17. Shulman ST, Bisno AL, Clegg HW, et al. Clinical practice guideline for the diagnosis and management of Group A Streptococcal pharyngitis: 2012 update by the Infectious Diseases Society of America. Clin Infect Dis. 2012;55:1279-1282.
18. Solvik UO, Boija EE, Ekvall S, et al. Performance and user-friendliness of the rapid antigen detection tests QuickVue Dipstick Strep A test and DIAQUICK Strep A Blue Dipstick for pharyngotonsillitis caused by Streptococcus pyogenes in primary health care. Eur J Clin Microbiol Infect Dis. 2021;40:549-558.
19. Barlas G, Ozturk H, Pehlivanturk G, Aydin S. Turkey's response to COVID-19 pandemic: strategy and key actions. Turk J Med Sci. 2021;51:3150-3156.
20. Ilhan MN, Tuzun H, Kilic R, Yildirim N. Nonpharmaceutical interventions in Turkey and worldwide during COVID-19 pandemic. Turk J Med Sci. 2021;51:3207-3214.
21. Sidell D, Shapiro NL. Acute tonsillitis. Infect Disord Drug Targets. 2012;12:271-276.
22. Yilmaz F, Karabay O, Ince NK, Ekerbicer H, Kocoglu E. [Effectiveness of rapid antigen test with throat gargle in detecting Group A beta-hemolytic streptococci]. Kulak Burun Bogaz Ihtis Derg. 2008;18:280-283.
23. Candan ED, Neslihan İ, Taner A. Factors affecting the incidence of Group A Β-Hemolytic Streptococci isolated from throat culture. Hacettepe Journal of Biology and Chemistry. 2022;50:25-30.
24. Yücel S, Güdücüoğlu H, Parlak M, Bayram Y. The frequency of Group A Beta-Hemolytic Streptococci (AGBHS) growing in throat cultures by years. Van Sağlık Bilimleri Dergisi. 2021;14:258-263.
25. Ozkaya-Parlakay A, Uysal M, Kara A. Group A Streptococcal tonsillopharyngitis burden in a tertiary Turkish hospital. Turk J Pediatr. 2012;54:474-477.
26. Furuncuoğlu Y, Başar M, Alici Ö, Bayiz Ü. The incidence of Group A Beta Hemolytic Streptococci in patients with acute exudative tonsilitis in Istanbul a 14-year period. Journal of Istanbul Faculty of Medicine. 2016;79:16-18.
27. Boyanton BLJ, Snowden JN, Frenner RA, Rosenbaum ER, Young HLKennedy JL. SARS-CoV-2 infection mitigation strategies concomitantly reduce Group A Streptococcus pharyngitis. Clin Pediatr (Phila). 2023;62:683-687.
28. Flores-Perez P, Gerig N, Cabrera-Lopez MI, et al. Acute bronchiolitis during the COVID-19 pandemic. Enferm Infecc Microbiol Clin (Engl Ed). 2022;40:572-575.
29. Cohen JF, Rybak A, Werner A, et al. Surveillance of noninvasive group A Streptococcus infections in French ambulatory pediatrics before and during the COVID-19 pandemic: a prospective multicenter study from 2018-2022. Int J Infect Dis. 2023;134:135-141.
30. Rybak A, Levy C, Angoulvant F, et al. Association of nonpharmaceutical interventions during the COVID-19 pandemic with invasive pneumococcal disease, pneumococcal carriage, and respiratory viral infections among children in France. JAMA Netw Open. 2022;5:e2218959.
31. Mangioni D, Fox V, Saltini P, et al. Increase in invasive Group A Streptococcal infections in Milan, Italy: A genomic and clinical characterization. Front Microbiol. 2023;14:1287522.
32. Wolters M, Berinson B, Degel-Brossmann N, et al. Population of invasive Group A streptococci isolates from a German tertiary care center is dominated by the hypertoxigenic virulent M1(UK) genotype. Infection. 2023. Epub ahead of print. doi: 10.1007/s15010-023-02137-1.
33. Cohen R, Ashman M, Taha MK, et al. Pediatric Infectious Disease Group (GPIP) position paper on the immune debt of the COVID-19 pandemic in childhood, how can we fill the immunity gap? Infect Dis Now. 2021;51:418-423.
34. Lu Q, Yu D, Yang Y. Group A Streptococcus is still at large. J Clin Med. 2023;12:2739.
35. Wrenn K, Blomquist PB, Inzoungou-Massanga C, et al. Surge of lower respiratory tract Group A Streptococcal infections in England in winter 2022: Epidemiology and clinical profile. Lancet. 2023;402:93.
36. Guy R, Henderson KL, Coelho J, et al. Increase in invasive group A streptococcal infection notifications, England, 2022. Euro Surveill. 2023;28:2200942.
37. Kennis M, Tagawa A, Kung VM, et al. Seasonal variations and risk factors of Streptococcus pyogenes infection: a multicenter research network study. Ther Adv Infect Dis. 2022;9:20499361221132101.
38. Lamagni TL, Darenberg J, Luca-Harari B, et al. Epidemiology of severe Streptococcus pyogenes disease in Europe. J Clin Microbiol. 2008;46:2359-2367.
39. Taylor A, Whittaker E. The changing epidemiology of respiratory viruses in children during the COVID-19 pandemic: A Canary in a COVID time. Pediatr Infect Dis J. 2022;41:e46-48.
40. Mponponsuo K, Church DL, Lu SJ, et al. Age and sex-specific incidence rates of Group A Streptococcal pharyngitis between 2010 and 2018: a population-based study. Future Microbiol. 2021;16:1053-1062.
41. Yildiz I, Gonullu E, Soysal A, Oner CN, Karabocuoglu M. The epidemiology of influenza virus infection and Group A Streptococcal pharyngitis in children between 2011 and 2018 in an outpatient pediatric clinic. Cureus. 2023;15:e33492.