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Published in: BMC Pediatrics 1/2012

Open Access 01-12-2012 | Research article

Detection of group A Streptococcus in tonsils from pediatric patients reveals high rate of asymptomatic streptococcal carriage

Authors: Amity L Roberts, Kristie L Connolly, Daniel J Kirse, Adele K Evans, Katherine A Poehling, Timothy R Peters, Sean D Reid

Published in: BMC Pediatrics | Issue 1/2012

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Abstract

Background

Group A Streptococcus (GAS) causes acute tonsillopharyngitis in children, and approximately 20% of this population are chronic carriers of GAS. Antibacterial therapy has previously been shown to be insufficient at clearing GAS carriage. Bacterial biofilms are a surface-attached bacterial community that is encased in a matrix of extracellular polymeric substances. Biofilms have been shown to provide a protective niche against the immune response and antibiotic treatments, and are often associated with recurrent or chronic bacterial infections. The objective of this study was to test the hypothesis that GAS is present within tonsil tissue at the time of tonsillectomy.

Methods

Blinded immunofluorescent and histological methods were employed to evaluate palatine tonsils from children undergoing routine tonsillectomy for adenotonsillar hypertrophy or recurrent GAS tonsillopharyngitis.

Results

Immunofluorescence analysis using anti-GAS antibody was positive in 11/30 (37%) children who had tonsillectomy for adenotonsillar hypertrophy and in 10/30 (33%) children who had tonsillectomy for recurrent GAS pharyngitis. Fluorescent microscopy with anti-GAS and anti-cytokeratin 8 & 18 antibodies revealed GAS was localized to the tonsillar reticulated crypts. Scanning electron microscopy identified 3-dimensional communities of cocci similar in size and morphology to GAS. The characteristics of these communities are similar to GAS biofilms from in vivo animal models.

Conclusion

Our study revealed the presence of GAS within the tonsillar reticulated crypts of approximately one-third of children who underwent tonsillectomy for either adenotonsillar hypertrophy or recurrent GAS tonsillopharyngitis at the Wake Forest School of Medicine.

Trial Registration

The tissue collected was normally discarded tissue and no patient identifiers were collected. Thus, no subjects were formally enrolled.
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Literature
1.
go back to reference Bisno AL, Gerber MA, Gwaltney JM, Kaplan EL, Schwartz RH: Practice guidelines for the diagnosis and management of group A streptococcal pharyngitis. Infectious Diseases Society of America. Clin Infect Dis. 2002, 35 (2): 113-125.CrossRefPubMed Bisno AL, Gerber MA, Gwaltney JM, Kaplan EL, Schwartz RH: Practice guidelines for the diagnosis and management of group A streptococcal pharyngitis. Infectious Diseases Society of America. Clin Infect Dis. 2002, 35 (2): 113-125.CrossRefPubMed
2.
go back to reference Casey JR, Pichichero ME: Higher dosages of azithromycin are more effective in treatment of group A streptococcal tonsillopharyngitis. Clin Infect Dis. 2005, 40 (12): 1748-1755.CrossRefPubMed Casey JR, Pichichero ME: Higher dosages of azithromycin are more effective in treatment of group A streptococcal tonsillopharyngitis. Clin Infect Dis. 2005, 40 (12): 1748-1755.CrossRefPubMed
3.
go back to reference Pichichero ME, Green JL, Francis AB, Marsocci SM, Murphy AM, Hoeger W, Noriega C, Sorrento A, Gootnick J: Recurrent group A streptococcal tonsillopharyngitis. Pediatr Infect Dis J. 1998, 17 (9): 809-815.CrossRefPubMed Pichichero ME, Green JL, Francis AB, Marsocci SM, Murphy AM, Hoeger W, Noriega C, Sorrento A, Gootnick J: Recurrent group A streptococcal tonsillopharyngitis. Pediatr Infect Dis J. 1998, 17 (9): 809-815.CrossRefPubMed
4.
go back to reference Pichichero ME, Marsocci SM, Murphy ML, Hoeger W, Green JL, Sorrento A: Incidence of streptococcal carriers in private pediatric practice. Arch Pediatr Adolesc Med. 1999, 153 (6): 624-628.CrossRefPubMed Pichichero ME, Marsocci SM, Murphy ML, Hoeger W, Green JL, Sorrento A: Incidence of streptococcal carriers in private pediatric practice. Arch Pediatr Adolesc Med. 1999, 153 (6): 624-628.CrossRefPubMed
5.
go back to reference Tarlow MJ: Macrolides in the management of streptococcal pharyngitis/tonsillitis. Pediatr Infect Dis J. 1997, 16 (4): 444-448.CrossRefPubMed Tarlow MJ: Macrolides in the management of streptococcal pharyngitis/tonsillitis. Pediatr Infect Dis J. 1997, 16 (4): 444-448.CrossRefPubMed
6.
go back to reference Bisno AL: Streptococcus pyogenes. 1995, New York, N.Y.: Churchill Livingstone, 4, Bisno AL: Streptococcus pyogenes. 1995, New York, N.Y.: Churchill Livingstone, 4,
7.
go back to reference Pichichero ME, Casey JR, Mayes T, Francis AB, Marsocci SM, Murphy AM, Hoeger W: Penicillin failure in streptococcal tonsillopharyngitis: causes and remedies. Pediatr Infect Dis J. 2000, 19 (9): 917-923.CrossRefPubMed Pichichero ME, Casey JR, Mayes T, Francis AB, Marsocci SM, Murphy AM, Hoeger W: Penicillin failure in streptococcal tonsillopharyngitis: causes and remedies. Pediatr Infect Dis J. 2000, 19 (9): 917-923.CrossRefPubMed
8.
go back to reference Group A Streptococcal Infections. Edited by: Pediatrics AAo. 2009, Elk Grove Village, IL: American Academy of Pediatrics, 28 Group A Streptococcal Infections. Edited by: Pediatrics AAo. 2009, Elk Grove Village, IL: American Academy of Pediatrics, 28
9.
go back to reference Kaplan EL, Huew BB: The sensitivity and specificity of an agglutination test for antibodies to streptococcal extracellular antigens: a quantitative analysis and comparison of the Streptozyme test with the anti-streptolysin O and anti-deoxyribonuclease B tests. J Pediatr. 1980, 96 (3 Pt 1): 367-373.CrossRefPubMed Kaplan EL, Huew BB: The sensitivity and specificity of an agglutination test for antibodies to streptococcal extracellular antigens: a quantitative analysis and comparison of the Streptozyme test with the anti-streptolysin O and anti-deoxyribonuclease B tests. J Pediatr. 1980, 96 (3 Pt 1): 367-373.CrossRefPubMed
10.
go back to reference Dajani A, Taubert K, Ferrieri P, Peter G, Shulman S: Treatment of acute streptococcal pharyngitis and prevention of rheumatic fever: a statement for health professionals. Committee on Rheumatic Fever, Endocarditis, and Kawasaki Disease of the Council on Cardiovascular Disease in the Young, the American Heart Association. Pediatrics. 1995, 96 (4 Pt 1): 758-764.PubMed Dajani A, Taubert K, Ferrieri P, Peter G, Shulman S: Treatment of acute streptococcal pharyngitis and prevention of rheumatic fever: a statement for health professionals. Committee on Rheumatic Fever, Endocarditis, and Kawasaki Disease of the Council on Cardiovascular Disease in the Young, the American Heart Association. Pediatrics. 1995, 96 (4 Pt 1): 758-764.PubMed
11.
go back to reference Kaplan EL, Gastanaduy AS, Huwe BB: The role of the carrier in treatment failures after antibiotic for group A streptococci in the upper respiratory tract. J Lab Clin Med. 1981, 98 (3): 326-335.PubMed Kaplan EL, Gastanaduy AS, Huwe BB: The role of the carrier in treatment failures after antibiotic for group A streptococci in the upper respiratory tract. J Lab Clin Med. 1981, 98 (3): 326-335.PubMed
12.
go back to reference Osterlund A, Engstrand L: An intracellular sanctuary for Streptococcus pyogenes in human tonsillar epithelium--studies of asymptomatic carriers and in vitro cultured biopsies. Acta Otolaryngol. 1997, 117 (6): 883-888.CrossRefPubMed Osterlund A, Engstrand L: An intracellular sanctuary for Streptococcus pyogenes in human tonsillar epithelium--studies of asymptomatic carriers and in vitro cultured biopsies. Acta Otolaryngol. 1997, 117 (6): 883-888.CrossRefPubMed
13.
go back to reference Osterlund A, Popa R, Nikkila T, Scheynius A, Engstrand L: Intracellular reservoir of Streptococcus pyogenes in vivo: a possible explanation for recurrent pharyngotonsillitis. Laryngoscope. 1997, 107 (5): 640-647.CrossRefPubMed Osterlund A, Popa R, Nikkila T, Scheynius A, Engstrand L: Intracellular reservoir of Streptococcus pyogenes in vivo: a possible explanation for recurrent pharyngotonsillitis. Laryngoscope. 1997, 107 (5): 640-647.CrossRefPubMed
14.
go back to reference Tanz RR, Shulman ST: Chronic pharyngeal carriage of group A streptococci. Pediatr Infect Dis J. 2007, 26 (2): 175-176.CrossRefPubMed Tanz RR, Shulman ST: Chronic pharyngeal carriage of group A streptococci. Pediatr Infect Dis J. 2007, 26 (2): 175-176.CrossRefPubMed
15.
go back to reference Doern CD, Roberts AL, Hong W, Nelson J, Lukomski S, Swords WE, Reid SD: Biofilm formation by group A Streptococcus: a role for the streptococcal regulator of virulence (Srv) and streptococcal cysteine protease (SpeB). Microbiology. 2009, 155 (Pt 1): 46-52.CrossRefPubMedPubMedCentral Doern CD, Roberts AL, Hong W, Nelson J, Lukomski S, Swords WE, Reid SD: Biofilm formation by group A Streptococcus: a role for the streptococcal regulator of virulence (Srv) and streptococcal cysteine protease (SpeB). Microbiology. 2009, 155 (Pt 1): 46-52.CrossRefPubMedPubMedCentral
16.
go back to reference Roberts AL, Connolly KL, Doern CD, Holder RC, Reid SD: Loss of the group A Streptococcus regulator Srv decreases biofilm formation in vivo in an otitis media model of infection. Infect Immun. 2010, 78 (11): 4800-8.CrossRefPubMedPubMedCentral Roberts AL, Connolly KL, Doern CD, Holder RC, Reid SD: Loss of the group A Streptococcus regulator Srv decreases biofilm formation in vivo in an otitis media model of infection. Infect Immun. 2010, 78 (11): 4800-8.CrossRefPubMedPubMedCentral
18.
go back to reference Fux CA, Costerton JW, Stewart PS, Stoodley P: Survival strategies of infectious biofilms. Trends Microbiol. 2005, 13 (1): 34-40.CrossRefPubMed Fux CA, Costerton JW, Stewart PS, Stoodley P: Survival strategies of infectious biofilms. Trends Microbiol. 2005, 13 (1): 34-40.CrossRefPubMed
19.
go back to reference Gilbert P, Das J, Foley I: Biofilm susceptibility to antimicrobials. Adv Dent Res. 1997, 11 (1): 160-167.CrossRefPubMed Gilbert P, Das J, Foley I: Biofilm susceptibility to antimicrobials. Adv Dent Res. 1997, 11 (1): 160-167.CrossRefPubMed
20.
go back to reference Donlan RM: Biofilm formation: a clinically relevant microbiological process. Clin Infect Dis. 2001, 33 (8): 1387-1392.CrossRefPubMed Donlan RM: Biofilm formation: a clinically relevant microbiological process. Clin Infect Dis. 2001, 33 (8): 1387-1392.CrossRefPubMed
21.
go back to reference Kania RE, Lamers GE, Vonk MJ, Huy PT, Hiemstra PS, Bloemberg GV, Grote JJ: Demonstration of bacterial cells and glycocalyx in biofilms on human tonsils. Arch Otolaryngol Head Neck Surg. 2007, 133 (2): 115-121.CrossRefPubMed Kania RE, Lamers GE, Vonk MJ, Huy PT, Hiemstra PS, Bloemberg GV, Grote JJ: Demonstration of bacterial cells and glycocalyx in biofilms on human tonsils. Arch Otolaryngol Head Neck Surg. 2007, 133 (2): 115-121.CrossRefPubMed
22.
go back to reference Clark MA, Wilson C, Sama A, Wilson JA, Hirst BH: Differential cytokeratin and glycoconjugate expression by the surface and crypt epithelia of human palatine tonsils. Histochem Cell Biol. 2000, 114 (4): 311-321.PubMed Clark MA, Wilson C, Sama A, Wilson JA, Hirst BH: Differential cytokeratin and glycoconjugate expression by the surface and crypt epithelia of human palatine tonsils. Histochem Cell Biol. 2000, 114 (4): 311-321.PubMed
23.
go back to reference Nave H, Gebert A, Pabst R: Morphology and immunology of the human palatine tonsil. Anat Embryol (Berl). 2001, 204 (5): 367-373.CrossRef Nave H, Gebert A, Pabst R: Morphology and immunology of the human palatine tonsil. Anat Embryol (Berl). 2001, 204 (5): 367-373.CrossRef
24.
go back to reference Perry ME: The specialised structure of crypt epithelium in the human palatine tonsil and its functional significance. J Anat. 1994, 185 (Pt 1): 111-127.PubMedPubMedCentral Perry ME: The specialised structure of crypt epithelium in the human palatine tonsil and its functional significance. J Anat. 1994, 185 (Pt 1): 111-127.PubMedPubMedCentral
25.
go back to reference Pegtel DM, Middeldorp J, Thorley-Lawson DA: Epstein-Barr virus infection in ex vivo tonsil epithelial cell cultures of asymptomatic carriers. J Virol. 2004, 78 (22): 12613-12624.CrossRefPubMedPubMedCentral Pegtel DM, Middeldorp J, Thorley-Lawson DA: Epstein-Barr virus infection in ex vivo tonsil epithelial cell cultures of asymptomatic carriers. J Virol. 2004, 78 (22): 12613-12624.CrossRefPubMedPubMedCentral
26.
go back to reference Connolly KL, Roberts AL, Holder RC, Reid SD: Dispersal of Group A Streptococcal Biofilms by the Cysteine Protease SpeB Leads to Increased Disease Severity in a Murine Model. PLoS One. 2011, 6 (4): e18984-CrossRefPubMedPubMedCentral Connolly KL, Roberts AL, Holder RC, Reid SD: Dispersal of Group A Streptococcal Biofilms by the Cysteine Protease SpeB Leads to Increased Disease Severity in a Murine Model. PLoS One. 2011, 6 (4): e18984-CrossRefPubMedPubMedCentral
27.
go back to reference Chole RA, Faddis BT: Anatomical evidence of microbial biofilms in tonsillar tissues: a possible mechanism to explain chronicity. Arch Otolaryngol Head Neck Surg. 2003, 129 (6): 634-636.CrossRefPubMed Chole RA, Faddis BT: Anatomical evidence of microbial biofilms in tonsillar tissues: a possible mechanism to explain chronicity. Arch Otolaryngol Head Neck Surg. 2003, 129 (6): 634-636.CrossRefPubMed
28.
go back to reference Brodsky L, Moore L, Stanievich J: The role of Haemophilus influenzae in the pathogenesis of tonsillar hypertrophy in children. Laryngoscope. 1988, 98 (10): 1055-1060.CrossRefPubMed Brodsky L, Moore L, Stanievich J: The role of Haemophilus influenzae in the pathogenesis of tonsillar hypertrophy in children. Laryngoscope. 1988, 98 (10): 1055-1060.CrossRefPubMed
29.
go back to reference Stjernquist-Desatnik A, Prellner K, Schalen C: Colonization by Haemophilus influenzae and group A streptococci in recurrent acute tonsillitis and in tonsillar hypertrophy. Acta Otolaryngol. 1990, 109 (3-4): 314-319.CrossRefPubMed Stjernquist-Desatnik A, Prellner K, Schalen C: Colonization by Haemophilus influenzae and group A streptococci in recurrent acute tonsillitis and in tonsillar hypertrophy. Acta Otolaryngol. 1990, 109 (3-4): 314-319.CrossRefPubMed
30.
go back to reference Casselbrant ML: What is wrong in chronic adenoiditis/tonsillitis anatomical considerations. Int J Pediatr Otorhinolaryngol. 1999, 49 (Suppl 1): S133-135.CrossRefPubMed Casselbrant ML: What is wrong in chronic adenoiditis/tonsillitis anatomical considerations. Int J Pediatr Otorhinolaryngol. 1999, 49 (Suppl 1): S133-135.CrossRefPubMed
31.
go back to reference Brodsky L, Moore L, Stanievich JF, Ogra PL: The immunology of tonsils in children: the effect of bacterial load on the presence of B- and T-cell subsets. Laryngoscope. 1988, 98 (1): 93-98.PubMed Brodsky L, Moore L, Stanievich JF, Ogra PL: The immunology of tonsils in children: the effect of bacterial load on the presence of B- and T-cell subsets. Laryngoscope. 1988, 98 (1): 93-98.PubMed
32.
go back to reference Stjernquist-Desatnik A, Prellner K, Schalen C: High recovery of Haemophilus influenzae and group A streptococci in recurrent tonsillar infection or hypertrophy as compared with normal tonsils. J Laryngol Otol. 1991, 105 (6): 439-441.CrossRefPubMed Stjernquist-Desatnik A, Prellner K, Schalen C: High recovery of Haemophilus influenzae and group A streptococci in recurrent tonsillar infection or hypertrophy as compared with normal tonsils. J Laryngol Otol. 1991, 105 (6): 439-441.CrossRefPubMed
Metadata
Title
Detection of group A Streptococcus in tonsils from pediatric patients reveals high rate of asymptomatic streptococcal carriage
Authors
Amity L Roberts
Kristie L Connolly
Daniel J Kirse
Adele K Evans
Katherine A Poehling
Timothy R Peters
Sean D Reid
Publication date
01-12-2012
Publisher
BioMed Central
Published in
BMC Pediatrics / Issue 1/2012
Electronic ISSN: 1471-2431
DOI
https://doi.org/10.1186/1471-2431-12-3

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