Serotype distribution and antimicrobial resistance of Streptococcus pneumoniae among children with acute otitis media in Marrakech, Morocco
,
Abstract
Background and Objectives: Streptococcus pneumonia (S. pneumoniae) is one of the most frequent pathogens leading to a variety of clinical manifestations. The effects of S. pneumoniae carriage on acute otitis media (AOM) are poorly studied. The study aimed to assess the serotype’s distribution and antimicrobial susceptibility in children with AOM after the implementation of the pneumococcal conjugate vaccine (PCV) in Morocco.
Materials and Methods: We conducted a prospective study of AOM children aged 6 to 36 months who visited pediatric centers in Marrakesh between January to June 2018. Parents were asked to complete a questionnaire and a swab was collected from each child. The S. pneumoniae strains were further identified (Hemolysis, optochin sensitivity, and agglutination test), serogrouped (IMMULEX PNEUMOTEST agglutination test), serotyped (Real time PCR) and tested for antimicrobial susceptibility.
Results: The S. pneumoniae carriage rate was 49.7% (87/175). As estimated, non-vaccine serotypes (NVT) were most prevalent (51/63; 81%). The most frequent serotypes were 6C/6D (12.7%), 10 (9.5%), and 19B/19C (9.5%). The S. pneumoniae strains that were isolated showed a diminished susceptibility to penicillin G with a rate of 27.5%. Penicillin non-susceptible pneumococci (PNSP) was mostly associated with NVT. More than 90% of S. pneumoniae isolates were susceptible to chloramphenicol (97.5%), clindamycin (97.5%), erythromycin (97.5%), levofloxacin (97.5%), pristinamycin (97.5%), gentamicin (92.5%), and teicoplanin (92.5%).
Conclusion: Important nasopharyngeal carriage prevalence was reported among children with AOM. The study showed that new NVT are emerging, including 6C/6D and 10. Furthermore, susceptibility was significantly higher against all antibiotics tested except for penicillin G and amoxicillin.
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2. Jespersen SI, Demant MN, Pedersen ML, Homøe P. Acute otitis media and pneumococcal vaccination-an observational cross-sectional study of otitis media among vaccinated and unvaccinated children in Greenland. Int J Circumpolar Health 2021; 80: 1858615.
3. Avnstorp MB, Homøe P, Bjerregaard P, Jensen RG. Chronic suppurative otitis media, middle ear pathology and corresponding hearing loss in a cohort of Greenlandic children. Int J Pediatr Otorhinolaryngol 2016; 83: 148-153.
4. Suaya JA, Gessner BD, Fung S, Vuocolo S, Scaife J, Swerdlow DL, et al. Acute otitis media, antimicrobial prescriptions, and medical expenses among children in the United States during 2011–2016. Vaccine 2018; 36: 7479-7486.
5. Ngo CC, Massa HM, Thornton RB, Cripps AW. Predominant bacteria detected from the middle ear fluid of children experiencing otitis media: A systematic review. PLoS One 2016; 11(3): e0150949.
6. Imöhl M, Perniciaro S, Busse A, van der Linden M. Bacterial spectrum of spontaneously ruptured otitis media in a 7-year, longitudinal, multicenter, epidemiological cross-sectional study in Germany. Front Med (Lausanne) 2021; 8: 675225.
7. Bergenfelz C, Hakansson AP. Streptococcus pneumoniae Otitis Media pathogenesis and how it informs our understanding of vaccine strategies. Curr Otorhinolaryngol Rep 2017; 5: 115-124.
8. Loughran AJ, Orihuela CJ, Tuomanen EI. Streptococcus pneumoniae: invasion and inflammation. Microbiol Spectr 2019; 7: 10.1128/microbiolspec.GPP3-0004-2018.
9. Howard LM, Zhu Y, Griffin MR, Edwards KM, Williams J V, Gil AI, et al. Nasopharyngeal Pneumococcal density during asymptomatic respiratory virus infection and risk for subsequent acute respiratory illness. Emerg Infect Dis 2019; 25: 2040-2047.
10. Littorin N, Ahl J, Uddén F, Resman F, Riesbeck K. Reduction of Streptococcus pneumoniae in upper respiratory tract cultures and a decreased incidence of related acute otitis media following introduction of childhood pneumococcal conjugate vaccines in a Swedish county. BMC Infect Dis 2016; 16: 407.
11. Ganaie F, Saad JS, McGee L, van Tonder AJ, Bentley SD, Lo SW, et al. A new pneumococcal capsule type, 10D, is the 100th serotype and has a large cps fragment from an oral streptococcus. mBio 2020; 11(3): e00937-20.
12. Ganaie F, Maruhn K, Li C, Porambo RJ, Elverdal PL, Abeygunwardana C, et al. Structural, genetic, and serological elucidation of Streptococcus pneumoniae serogroup 24 serotypes: discovery of a new serotype, 24C, with a variable capsule structure. J Clin Microbiol 2021; 59(7): e0054021.
13. Quirk SJ, Haraldsson G, Erlendsdóttir H, Hjálmarsdóttir MA, van Tonder AJ, Hrafnkelsson B, et al. Effect of vaccination on pneumococci isolated from the nasopharynx of healthy children and the middle ear of children with otitis media in Iceland. J Clin Microbiol 2018; 56(12): e01046-18.
14. Soysal A, Gönüllü E, Yıldız I, Aydemir G, Tunç T, Fırat Y, et al. Impact of the 13-valent pneumococcal conjugate vaccine on the incidences of acute otitis media, recurrent otitis media and tympanostomy tube insertion in children after its implementation into the national immunization program in Turkey. Hum Vaccin Immunother 2020; 16: 445-451.
15. Wouters I, Van Heirstraeten L, Desmet S, Blaizot S, Verhaegen J, Goossens H, et al. Nasopharyngeal S. pneumoniae carriage and density in Belgian infants after 9 years of pneumococcal conjugate vaccine programme. Vaccine 2018; 36: 15-22.
16. Allemann A, Frey PM, Brugger SD, Hilty M. Pneumococcal carriage and serotype variation before and after introduction of pneumococcal conjugate vaccines in patients with acute otitis media in Switzerland. Vaccine 2017; 35: 1946-1953.
17. Sigurdsson S, Eythorsson E, Hrafnkelsson B, Erlendsdóttir H, Kristinsson KG, Haraldsson Á. Reduction in all-cause acute otitis media in children <3 years of age in primary care following vaccination with 10-valent Pneumococcal Haemophilus influenzae protein-D conjugate vaccine: a whole-population study. Clin Infect Dis 2018; 67: 1213-1219.
18. Altun O, Athlin S, Almuhayawi M, Strålin K, Özenci V. Rapid identification of Streptococcus pneumoniae in blood cultures by using the ImmuLex, Slidex and Wellcogen latex agglutination tests and the BinaxNOW antigen test. Eur J Clin Microbiol Infect Dis 2016; 35: 579-585.
19. Dubois D, Segonds C, Prere MF, Marty N, Oswald E. Identification of clinical Streptococcus pneumoniae isolates among other alpha and nonhemolytic Streptococci by use of the Vitek MS matrix-assisted laser desorption ionization – time of flight mass. J Clin Microbiol 2013; 51: 1861-1867.
20. Bosch AA, Biesbroek G, Trzcinski K, Sanders EA, Bogaert D. Viral and bacterial interactions in the upper respiratory tract. PLoS Pathog 2013; 9(1): e1003057.
21. Li N, Ma WT, Pang M, Fan QL, Hua JL. The commensal microbiota and viral infection: a comprehensive review. Front Immunol 2019; 10: 1551.
22. Ribet D, Cossart P. How bacterial pathogens colonize their hosts and invade deeper tissues. Microbes Infect 2015; 17: 173-183.
23. Enoksson F, Rodriguez AR, Peno C, Lopez CB, Tjernström F, Bogaert D, et al. Niche- and gender-dependent immune reactions in relation to the microbiota profile in pediatric patients with otitis media with effusion. Infect Immun 2020; 88(10): e00147-20.
24. Brugger SD, Kraemer JG, Qi W, Bomar L, Oppliger A, and Hilty M. Age-Dependent dissimilarity of the nasopharyngeal and middle ear microbiota in children with acute otitis media. Front Genet 2019; 10: 555.
25. Satoh C, Toizumi M, Nguyen HAT, Hara M, Bui MX, Iwasaki C, et al. Prevalence and characteristics of children with otitis media with effusion in Vietnam. Vaccine 2021; 39: 2613-2619.
26. Ekinci E, Desmet S, Van Heirstraeten L, Mertens C, Wouters I, Beutels P, et al. Streptococcus pneumoniae serotypes carried by young children and their association with acute otitis media during the period 2016-2019. Front Pediatr 2021; 9: 664083.
27. Lee J, Kim KH, Jo DS, Ma SH, Kim JH, Kim CS, et al. A longitudinal hospital-based epidemiology study to assess acute otitis media incidence and nasopharyngeal carriage in Korean children up to 24 months. Hum Vaccin Immunother 2020; 16: 3090-3097.
28. Korona-glowniak I, Zychowski P, Siwiec R, Mazur E, Niedzielska G, Malm A. Resistant Streptococcus pneumoniae strains in children with acute otitis media – high risk of persistent colonization after treatment. BMC Infect Dis 2018; 18: 478.
29. Falup-Pecurariu O, Leibovitz E, Mercas A, Bleotu L, Zavarache C, Porat N, et al. Pneumococcal acute otitis media in infants and children in central Romania, 2009-2011: microbiological characteristics and potential coverage by pneumococcal conjugate vaccines. Int J Infect Dis 2013; 17(9): e702-e706.
30. Warda K, Oufdou K, Zahlane K, Bouskraoui M. Antibiotic resistance and serotype distribution of nasopharyngeal isolates of Streptococcus pneumoniae from children in Marrakech region (Morocco). J Infect Public Health 2013; 6: 473-481.
31. Dilagui I, Moussair FZ, Loqman S, Diawara I, Zerouali K, Belabbes H, et al. Streptococcus pneumoniae carriage among febrile children at the time of PCV-10 immunization in pediatric emergencies at Mohammed VI university hospital centre in Marrakesh (Morocco). Arch Pédiatr 2019; 26: 453-458.
32. Jroundi I, Mahraoui C, Benmessaoud R, Moraleda C, Munoz Almagro C, Seffar M, et al. Streptococcus pneumoniae carriage among healthy and sick pediatric patients before the generalized implementation of the 13-valent pneumococcal vaccine in Morocco from 2010 to 2011. J Infect Public Health 2017; 10: 165-170.
33. Brotons P, Bassat Q, Lanaspa M, Henares D, Perez-arguello A, Madrid L, et al. Nasopharyngeal bacterial load as a marker for rapid and easy diagnosis of invasive pneumococcal disease in children from Mozambique. PLoS One 2017; 12(9): e0184762.
34. Baggett HC, Watson NL, Knoll MD, Brooks WA, Feikin DR, Hammitt LL, et al. Density of upper respiratory colonization with Streptococcus pneumoniae and its role in the diagnosis of Pneumococcal Pneumonia among children aged < 5 years in the perch study. Clin Infect Dis 2017; 64(supple_3): S317–S327.
35. Cohen R, Varon E, Doit C, Schlemmer C, Romain O, Thollot F, et al. A 13-year survey of pneumococcal nasopharyngeal carriage in children with acute otitis media following PCV7 and PCV13 implementation. Vaccine 2015; 33: 5118-126.
36. Ziane H, Manageiro V, Ferreira E, Moura IB, Bektache S, Tazir M, et al. Serotypes and antibiotic susceptibility of Streptococcus pneumoniae isolates from invasive Pneumococcal disease and asymptomatic carriage in a pre-vaccination Period, in Algeria. Front Microbiol 2016; 7:803.
37. Haile AA, Gidebo DD, Ali MM. Colonization rate of Streptococcus pneumoniae, its associated factors and antimicrobial susceptibility pattern among children attending kindergarten school in Hawassa, southern Ethiopia. BMC Res Notes 2019; 12: 344.
38. Diawara I, Zerouali K, Katfy K, Zaki B, Belabbes H, Najib J, et al. Invasive pneumococcal disease among children younger than 5 years of age before and after introduction of pneumococcal conjugate vaccine in Casablanca, Morocco. Int J Infect Dis 2015; 40: 95-101.
39. Setchanova L, Murdjeva M, Stancheva I, Alexandrova A, Sredkova M, Stoeva T, et al. Serotype changes and antimicrobial nonsusceptibility rates of invasive and non-invasive Streptococcus pneumoniae isolates after implementation of 10-valent pneumococcal nontypeable Haemophilus influenzae protein D conjugate vaccine ( PHiD-CV) in Bulgaria. Braz J Infect Dis 2017; 21: 433-440.
40. Chi H, Chiu NC, Huang FY, Hsu CH, Lee KS, Huang LM, et al. Acute otitis media caused by Streptococcus pneumoniae serotype 19A ST320 clone: epidemiological and clinical characteristics. J Microbiol Immunol Infect 2018; 51: 337-343.
41. Pinto TCA, Neves FPG, Souza ARV, Oliveira LMA, Costa NS, Castro LFS, et al. Evolution of penicillin non-susceptibility among Streptococcus pneumoniae isolates recovered from asymptomatic carriage and invasive disease over 25 years in Brazil, 1990–2014. Front Microbiol 2019; 10: 486.
42. Emgård M, Msuya SE, Nyombi BM, Mosha D, Gonzales-Siles L, Nordén R, et al. Carriage of penicillin-non-susceptible pneumococci among children in northern Tanzania in the 13-valent pneumococcal vaccine era. Int J Infect Dis 2019; 81: 156-166.
43. Moyo SJ, Steinbakk M, Aboud S, Mkopi N, Kasubi M, Blomberg B, et al. Penicillin resistance and serotype distribution of Streptococcus pneumoniae in nasopharyngeal carrier children under 5 years of age in Dar es Salaam, Tanzania. J Med Microbiol 2012; 61: 952-959.
44. Uddén F, Filipe M, Slotved HC, Yamba-Yamba L, Fuursted K, Pintar Kuatoko P, et al. Pneumococcal carriage among children aged 4 – 12 years in Angola 4 years after the introduction of a pneumococcal conjugate vaccine. Vaccine 2020; 38: 7928-7937.
45. Beheshti M, Jabalameli F, Feizabadi MM, Hahsemi FB, Beigverdi R, Emaneini M. Molecular characterization, antibiotic resistance pattern and capsular types of invasive Streptococcus pneumoniae isolated from clinical samples in Tehran, Iran. BMC Microbiol 2020; 20: 167.
46. Horácio AN, Silva-Costa C, Lopes E, Ramirez M, and Melo-Cristino J, Portuguese Group for the Study of Streptococcal Infections. Conjugate vaccine serotypes persist as major causes of non-invasive pneumococcal pneumonia in Portugal despite declines in serotypes 3 and 19A (2012-2015). PLoS One 2018; 13(11): e0206912.
47. Dewé TCM, D’aeth JC, and Croucher NJ. Genomic epidemiology of penicillin-non-susceptible Streptococcus pneumoniae. Microb Genom 2019; 5(10): e000305.
48. Zintgraff J, Gagetti P, Napoli D, Sanchez EluchansN, Irazu L, Moscoloni M, et al. Invasive Streptococcus pneumoniae isolates from pediatric population in Argentina for the period 2006–2019. Temporal progression of serotypes distribution and antibiotic resistance. Vaccine 2022; 40: 459-470.
49. Al-Jardani A, Al Rashdi A, Al Jaaidi A, Al Bulushi M, Al Mahrouqi S, Al-Abri S, et al. Serotype distribution and antibiotic resistance among invasive Streptococcus pneumoniae from Oman post 13-valent vaccine introduction. Int J Infect Dis 2019; 85: 135-140.
50. Houri H, Tabatabaei SR, Saee Y, Fallah F, Rahbar M, Karimi A. Distribution of capsular types and drug resistance patterns of invasive pediatric Streptococcus pneumoniae isolates in Teheran, Iran. Int J Infect Dis 2017; 57: 21-26.
51. Tsai YT, Lee YL, Lu MC, Shao PL, Lu PL, Cheng SH, et al. Nationwide surveillance of antimicrobial resistance in invasive isolates of Streptococcus pneumoniae in Taiwan from 2017 to 2019. J Microbiol Immunol Infect 2022;55:215-224.
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2. Jespersen SI, Demant MN, Pedersen ML, Homøe P. Acute otitis media and pneumococcal vaccination-an observational cross-sectional study of otitis media among vaccinated and unvaccinated children in Greenland. Int J Circumpolar Health 2021; 80: 1858615.
3. Avnstorp MB, Homøe P, Bjerregaard P, Jensen RG. Chronic suppurative otitis media, middle ear pathology and corresponding hearing loss in a cohort of Greenlandic children. Int J Pediatr Otorhinolaryngol 2016; 83: 148-153.
4. Suaya JA, Gessner BD, Fung S, Vuocolo S, Scaife J, Swerdlow DL, et al. Acute otitis media, antimicrobial prescriptions, and medical expenses among children in the United States during 2011–2016. Vaccine 2018; 36: 7479-7486.
5. Ngo CC, Massa HM, Thornton RB, Cripps AW. Predominant bacteria detected from the middle ear fluid of children experiencing otitis media: A systematic review. PLoS One 2016; 11(3): e0150949.
6. Imöhl M, Perniciaro S, Busse A, van der Linden M. Bacterial spectrum of spontaneously ruptured otitis media in a 7-year, longitudinal, multicenter, epidemiological cross-sectional study in Germany. Front Med (Lausanne) 2021; 8: 675225.
7. Bergenfelz C, Hakansson AP. Streptococcus pneumoniae Otitis Media pathogenesis and how it informs our understanding of vaccine strategies. Curr Otorhinolaryngol Rep 2017; 5: 115-124.
8. Loughran AJ, Orihuela CJ, Tuomanen EI. Streptococcus pneumoniae: invasion and inflammation. Microbiol Spectr 2019; 7: 10.1128/microbiolspec.GPP3-0004-2018.
9. Howard LM, Zhu Y, Griffin MR, Edwards KM, Williams J V, Gil AI, et al. Nasopharyngeal Pneumococcal density during asymptomatic respiratory virus infection and risk for subsequent acute respiratory illness. Emerg Infect Dis 2019; 25: 2040-2047.
10. Littorin N, Ahl J, Uddén F, Resman F, Riesbeck K. Reduction of Streptococcus pneumoniae in upper respiratory tract cultures and a decreased incidence of related acute otitis media following introduction of childhood pneumococcal conjugate vaccines in a Swedish county. BMC Infect Dis 2016; 16: 407.
11. Ganaie F, Saad JS, McGee L, van Tonder AJ, Bentley SD, Lo SW, et al. A new pneumococcal capsule type, 10D, is the 100th serotype and has a large cps fragment from an oral streptococcus. mBio 2020; 11(3): e00937-20.
12. Ganaie F, Maruhn K, Li C, Porambo RJ, Elverdal PL, Abeygunwardana C, et al. Structural, genetic, and serological elucidation of Streptococcus pneumoniae serogroup 24 serotypes: discovery of a new serotype, 24C, with a variable capsule structure. J Clin Microbiol 2021; 59(7): e0054021.
13. Quirk SJ, Haraldsson G, Erlendsdóttir H, Hjálmarsdóttir MA, van Tonder AJ, Hrafnkelsson B, et al. Effect of vaccination on pneumococci isolated from the nasopharynx of healthy children and the middle ear of children with otitis media in Iceland. J Clin Microbiol 2018; 56(12): e01046-18.
14. Soysal A, Gönüllü E, Yıldız I, Aydemir G, Tunç T, Fırat Y, et al. Impact of the 13-valent pneumococcal conjugate vaccine on the incidences of acute otitis media, recurrent otitis media and tympanostomy tube insertion in children after its implementation into the national immunization program in Turkey. Hum Vaccin Immunother 2020; 16: 445-451.
15. Wouters I, Van Heirstraeten L, Desmet S, Blaizot S, Verhaegen J, Goossens H, et al. Nasopharyngeal S. pneumoniae carriage and density in Belgian infants after 9 years of pneumococcal conjugate vaccine programme. Vaccine 2018; 36: 15-22.
16. Allemann A, Frey PM, Brugger SD, Hilty M. Pneumococcal carriage and serotype variation before and after introduction of pneumococcal conjugate vaccines in patients with acute otitis media in Switzerland. Vaccine 2017; 35: 1946-1953.
17. Sigurdsson S, Eythorsson E, Hrafnkelsson B, Erlendsdóttir H, Kristinsson KG, Haraldsson Á. Reduction in all-cause acute otitis media in children <3 years of age in primary care following vaccination with 10-valent Pneumococcal Haemophilus influenzae protein-D conjugate vaccine: a whole-population study. Clin Infect Dis 2018; 67: 1213-1219.
18. Altun O, Athlin S, Almuhayawi M, Strålin K, Özenci V. Rapid identification of Streptococcus pneumoniae in blood cultures by using the ImmuLex, Slidex and Wellcogen latex agglutination tests and the BinaxNOW antigen test. Eur J Clin Microbiol Infect Dis 2016; 35: 579-585.
19. Dubois D, Segonds C, Prere MF, Marty N, Oswald E. Identification of clinical Streptococcus pneumoniae isolates among other alpha and nonhemolytic Streptococci by use of the Vitek MS matrix-assisted laser desorption ionization – time of flight mass. J Clin Microbiol 2013; 51: 1861-1867.
20. Bosch AA, Biesbroek G, Trzcinski K, Sanders EA, Bogaert D. Viral and bacterial interactions in the upper respiratory tract. PLoS Pathog 2013; 9(1): e1003057.
21. Li N, Ma WT, Pang M, Fan QL, Hua JL. The commensal microbiota and viral infection: a comprehensive review. Front Immunol 2019; 10: 1551.
22. Ribet D, Cossart P. How bacterial pathogens colonize their hosts and invade deeper tissues. Microbes Infect 2015; 17: 173-183.
23. Enoksson F, Rodriguez AR, Peno C, Lopez CB, Tjernström F, Bogaert D, et al. Niche- and gender-dependent immune reactions in relation to the microbiota profile in pediatric patients with otitis media with effusion. Infect Immun 2020; 88(10): e00147-20.
24. Brugger SD, Kraemer JG, Qi W, Bomar L, Oppliger A, and Hilty M. Age-Dependent dissimilarity of the nasopharyngeal and middle ear microbiota in children with acute otitis media. Front Genet 2019; 10: 555.
25. Satoh C, Toizumi M, Nguyen HAT, Hara M, Bui MX, Iwasaki C, et al. Prevalence and characteristics of children with otitis media with effusion in Vietnam. Vaccine 2021; 39: 2613-2619.
26. Ekinci E, Desmet S, Van Heirstraeten L, Mertens C, Wouters I, Beutels P, et al. Streptococcus pneumoniae serotypes carried by young children and their association with acute otitis media during the period 2016-2019. Front Pediatr 2021; 9: 664083.
27. Lee J, Kim KH, Jo DS, Ma SH, Kim JH, Kim CS, et al. A longitudinal hospital-based epidemiology study to assess acute otitis media incidence and nasopharyngeal carriage in Korean children up to 24 months. Hum Vaccin Immunother 2020; 16: 3090-3097.
28. Korona-glowniak I, Zychowski P, Siwiec R, Mazur E, Niedzielska G, Malm A. Resistant Streptococcus pneumoniae strains in children with acute otitis media – high risk of persistent colonization after treatment. BMC Infect Dis 2018; 18: 478.
29. Falup-Pecurariu O, Leibovitz E, Mercas A, Bleotu L, Zavarache C, Porat N, et al. Pneumococcal acute otitis media in infants and children in central Romania, 2009-2011: microbiological characteristics and potential coverage by pneumococcal conjugate vaccines. Int J Infect Dis 2013; 17(9): e702-e706.
30. Warda K, Oufdou K, Zahlane K, Bouskraoui M. Antibiotic resistance and serotype distribution of nasopharyngeal isolates of Streptococcus pneumoniae from children in Marrakech region (Morocco). J Infect Public Health 2013; 6: 473-481.
31. Dilagui I, Moussair FZ, Loqman S, Diawara I, Zerouali K, Belabbes H, et al. Streptococcus pneumoniae carriage among febrile children at the time of PCV-10 immunization in pediatric emergencies at Mohammed VI university hospital centre in Marrakesh (Morocco). Arch Pédiatr 2019; 26: 453-458.
32. Jroundi I, Mahraoui C, Benmessaoud R, Moraleda C, Munoz Almagro C, Seffar M, et al. Streptococcus pneumoniae carriage among healthy and sick pediatric patients before the generalized implementation of the 13-valent pneumococcal vaccine in Morocco from 2010 to 2011. J Infect Public Health 2017; 10: 165-170.
33. Brotons P, Bassat Q, Lanaspa M, Henares D, Perez-arguello A, Madrid L, et al. Nasopharyngeal bacterial load as a marker for rapid and easy diagnosis of invasive pneumococcal disease in children from Mozambique. PLoS One 2017; 12(9): e0184762.
34. Baggett HC, Watson NL, Knoll MD, Brooks WA, Feikin DR, Hammitt LL, et al. Density of upper respiratory colonization with Streptococcus pneumoniae and its role in the diagnosis of Pneumococcal Pneumonia among children aged < 5 years in the perch study. Clin Infect Dis 2017; 64(supple_3): S317–S327.
35. Cohen R, Varon E, Doit C, Schlemmer C, Romain O, Thollot F, et al. A 13-year survey of pneumococcal nasopharyngeal carriage in children with acute otitis media following PCV7 and PCV13 implementation. Vaccine 2015; 33: 5118-126.
36. Ziane H, Manageiro V, Ferreira E, Moura IB, Bektache S, Tazir M, et al. Serotypes and antibiotic susceptibility of Streptococcus pneumoniae isolates from invasive Pneumococcal disease and asymptomatic carriage in a pre-vaccination Period, in Algeria. Front Microbiol 2016; 7:803.
37. Haile AA, Gidebo DD, Ali MM. Colonization rate of Streptococcus pneumoniae, its associated factors and antimicrobial susceptibility pattern among children attending kindergarten school in Hawassa, southern Ethiopia. BMC Res Notes 2019; 12: 344.
38. Diawara I, Zerouali K, Katfy K, Zaki B, Belabbes H, Najib J, et al. Invasive pneumococcal disease among children younger than 5 years of age before and after introduction of pneumococcal conjugate vaccine in Casablanca, Morocco. Int J Infect Dis 2015; 40: 95-101.
39. Setchanova L, Murdjeva M, Stancheva I, Alexandrova A, Sredkova M, Stoeva T, et al. Serotype changes and antimicrobial nonsusceptibility rates of invasive and non-invasive Streptococcus pneumoniae isolates after implementation of 10-valent pneumococcal nontypeable Haemophilus influenzae protein D conjugate vaccine ( PHiD-CV) in Bulgaria. Braz J Infect Dis 2017; 21: 433-440.
40. Chi H, Chiu NC, Huang FY, Hsu CH, Lee KS, Huang LM, et al. Acute otitis media caused by Streptococcus pneumoniae serotype 19A ST320 clone: epidemiological and clinical characteristics. J Microbiol Immunol Infect 2018; 51: 337-343.
41. Pinto TCA, Neves FPG, Souza ARV, Oliveira LMA, Costa NS, Castro LFS, et al. Evolution of penicillin non-susceptibility among Streptococcus pneumoniae isolates recovered from asymptomatic carriage and invasive disease over 25 years in Brazil, 1990–2014. Front Microbiol 2019; 10: 486.
42. Emgård M, Msuya SE, Nyombi BM, Mosha D, Gonzales-Siles L, Nordén R, et al. Carriage of penicillin-non-susceptible pneumococci among children in northern Tanzania in the 13-valent pneumococcal vaccine era. Int J Infect Dis 2019; 81: 156-166.
43. Moyo SJ, Steinbakk M, Aboud S, Mkopi N, Kasubi M, Blomberg B, et al. Penicillin resistance and serotype distribution of Streptococcus pneumoniae in nasopharyngeal carrier children under 5 years of age in Dar es Salaam, Tanzania. J Med Microbiol 2012; 61: 952-959.
44. Uddén F, Filipe M, Slotved HC, Yamba-Yamba L, Fuursted K, Pintar Kuatoko P, et al. Pneumococcal carriage among children aged 4 – 12 years in Angola 4 years after the introduction of a pneumococcal conjugate vaccine. Vaccine 2020; 38: 7928-7937.
45. Beheshti M, Jabalameli F, Feizabadi MM, Hahsemi FB, Beigverdi R, Emaneini M. Molecular characterization, antibiotic resistance pattern and capsular types of invasive Streptococcus pneumoniae isolated from clinical samples in Tehran, Iran. BMC Microbiol 2020; 20: 167.
46. Horácio AN, Silva-Costa C, Lopes E, Ramirez M, and Melo-Cristino J, Portuguese Group for the Study of Streptococcal Infections. Conjugate vaccine serotypes persist as major causes of non-invasive pneumococcal pneumonia in Portugal despite declines in serotypes 3 and 19A (2012-2015). PLoS One 2018; 13(11): e0206912.
47. Dewé TCM, D’aeth JC, and Croucher NJ. Genomic epidemiology of penicillin-non-susceptible Streptococcus pneumoniae. Microb Genom 2019; 5(10): e000305.
48. Zintgraff J, Gagetti P, Napoli D, Sanchez EluchansN, Irazu L, Moscoloni M, et al. Invasive Streptococcus pneumoniae isolates from pediatric population in Argentina for the period 2006–2019. Temporal progression of serotypes distribution and antibiotic resistance. Vaccine 2022; 40: 459-470.
49. Al-Jardani A, Al Rashdi A, Al Jaaidi A, Al Bulushi M, Al Mahrouqi S, Al-Abri S, et al. Serotype distribution and antibiotic resistance among invasive Streptococcus pneumoniae from Oman post 13-valent vaccine introduction. Int J Infect Dis 2019; 85: 135-140.
50. Houri H, Tabatabaei SR, Saee Y, Fallah F, Rahbar M, Karimi A. Distribution of capsular types and drug resistance patterns of invasive pediatric Streptococcus pneumoniae isolates in Teheran, Iran. Int J Infect Dis 2017; 57: 21-26.
51. Tsai YT, Lee YL, Lu MC, Shao PL, Lu PL, Cheng SH, et al. Nationwide surveillance of antimicrobial resistance in invasive isolates of Streptococcus pneumoniae in Taiwan from 2017 to 2019. J Microbiol Immunol Infect 2022;55:215-224.
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| Files | ||
| Issue | Vol 14 No 1 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v14i1.8801 | |
| Keywords | ||
| Otitis media; Preschool children; Colonization; Streptococcus pneumoniae; 10 valent pneumococcal vaccine; Serotyping; Antibacterial drug resistance | ||
| Rights and permissions | |
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Amari S, Warda K, Elkamouni Y, Arsalane L, Bouskraoui M, Zouhair S. Serotype distribution and antimicrobial resistance of Streptococcus pneumoniae among children with acute otitis media in Marrakech, Morocco. Iran J Microbiol. 2022;14(1):47-55.
