PEDIATRICS Vol. 120 No. 5 November 2007, pp. 950-957 (doi:10.1542/peds.2006-3368)
ARTICLE |
Burden of Acute Sore Throat and Group A Streptococcal Pharyngitis in School-aged Children and Their Families in Australia
a Department of Paediatrics
d School of Population Health, University of Melbourne, Melbourne, Australia
c Department of General Medicine, Royal Children's Hospital, Melbourne, Australia
e Menzies School of Health Research, Charles Darwin University, Darwin, Australia
b Murdoch Children's Research Institute, Parkville, Australia
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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OBJECTIVE. The objective of this study was to determine the incidence, transmission, carriage, and risk factors for group A streptococcal pharyngitis in school-aged children and their families.
METHODS. A 16-month, prospective, family-based cohort study was undertaken from August 2001 through December 2002 in Melbourne, Australia. A total of 202 families (853 people) with at least 1 child aged 3 to 12 years were randomly selected from 3 primary care practices across suburban Melbourne to collect surveillance data for acute group A streptococcal pharyngitis, including serology for index and secondary cases and intermittent carriage data. Cohort retention was 97% for 16 months.
RESULTS. The incidence of acute sore throat, group A streptococcal swab–positive pharyngitis, and serologically confirmed group A streptococcal pharyngitis was 33, 13, and 8 per 100 child-years, respectively, for school-aged children (5–12 years) and 60, 20, and 15 per 100 family-years, respectively. Sore throat was less common in adults than children, but adults with sore throat were as likely as children to have group A streptococcal culture–positive or serologically proven pharyngitis. In families who had a primary case, 43% had at least 1 secondary case, and in family members who were at risk, 13% contracted a secondary case. The spring, summer, and winter carriage rates for children were 13%, 8%, and 16%, respectively, and for adults the rate was 2% across all seasons.
CONCLUSIONS. Group A streptococcal pharyngitis is still common, and the peak incidence occurs in school-aged children. However, the incidence in adults is higher than expected, and the number of secondary cases in families may be an important factor when considering the potential benefits of treatment.
Key Words: acute pharyngitis • group A streptococci • incidence • transmission • carriage • serology • school-aged children
Abbreviations: GAS—group A Streptococcus • SES—socioeconomic status • ASO—antistreptolysin O • ADB—anti-DNase B • ULN—upper limit of normal • CI—confidence interval • RR—relative risk
Sore throat remains one of the most common presentations to primary care providers,1 and group A Streptococcus (GAS) is arguably the only cause of sore throat that needs treatment.2 The potential aims of treatment are symptom reduction, prevention of transmission, and prevention of suppurative and nonsuppurative streptococcal sequelae, particularly acute rheumatic fever. In developed countries, where the incidence of acute rheumatic fever is low, the role of antibiotics in the treatment of acute pharyngitis is a continuing source of controversy.
Most recent studies3–7 of sore throat reported numbers of presentations to primary care, the proportion of sore throats from which GAS can be recovered on throat swabs, or response to antibiotic treatment. Since the 1960s, very few population-based studies have reported the incidence of sore throat or GAS culture–positive sore throat, and no studies have reported the incidence of true GAS pharyngitis (ie, GAS culture–positive sore throat with serologic evidence of recent streptococcal infection). Such data are critical in determining the most appropriate approach to management and in preparing for the arrival of GAS vaccines, which are in clinical trials.8,9
We conducted a prospective study to determine the burden of sore throat, GAS culture–positive sore throat, and serologically proven GAS pharyngitis in suburban Melbourne, Australia. We included all family members in the cohort to assess secondary transmission of GAS within the household.
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METHODS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Design
We undertook a 16-month, prospective, family-based cohort study, which was community based, using family medicine practitioners to collect the surveillance data. The Royal Children's Hospital Ethics in Human Research Committee approved the study.
Setting
Families were resident in 3 diverse geographic and socioeconomic regions of metropolitan Melbourne. Deer Park, Essendon North, and Nepean are in the western, northern, and southern areas of Melbourne, respectively. Deer Park has a diverse mix of ethnicities and a lower socioeconomic status (SES) than the other 2 areas. The median weekly individual income for men in Deer Park was $500 to $599 (Australian dollars) ($255–$305 US dollars) in contrast to Essendon North and Nepean, where the most common weekly individual income for men was $1000 to $1499 (Australian dollars) ($510–$760 US dollars).10
Data Collection
Families with at least 1 child aged 3 to 12 years, the peak age of incidence of GAS pharyngitis, were randomly selected and recruited through 3 practices, 1 in each region. Deidentified lists of all families seen within the past 5 to 10 years by the practice were obtained. Initially, 250 families from each practice were selected using random number allocation by computer. Parents were sent a letter signed by the general practitioner, requesting their participation in the study. The remaining families in the practice database were contacted in subsequent mailings, and nonresponders received a second letter until a sufficient number families were recruited. Interested families were contacted, and enrollment visits were arranged. Baseline demographic data were collected, and each family member had a throat swab to determine baseline carriage of GAS.
Families were asked to attend the practice when any member developed a sore throat plus 
1 of the Centor criteria11: a history of fever, tender anterior cervical lymph nodes, pharyngeal exudate, or an absence of cough. Because these criteria were not developed for children, parents were encouraged to bring in their children with a broader set of symptoms, including headache, abdominal pain, vomiting, cough, coryza, and hoarseness. The general practitioner performed a throat swab, recorded the clinical details, and treated the patient as dictated by their usual practice. When the culture isolated GAS, the family was visited at home 1 to 2 weeks later to obtain blood and additional data from the index patient and swabs from family members. The family was visited 2 weeks after the initial blood draw (3–4 weeks after the positive culture) for repeat serology on the index patient, serology on any culture-positive family members, and repeat throat swabs from family members. All participants also had throat swabs taken every 3 or 4 months to assess upper respiratory tract carriage of GAS. To receive a swab at one of these carriage clinics, the participant had to be asymptomatic. Serology was not performed at this time because of logistic (need for paired titers on well individuals) and cost constraints.
Definitions
Children were aged 1 to 18 years, and adults were aged >18 years. The family included all members who were living in the household for the duration of the study period and included all household contacts. A primary case was a symptomatic episode of GAS culture–positive sore throat or serologically confirmed GAS pharyngitis in any family member when all other family members had been asymptomatic for the preceding 2 weeks. A secondary case was an episode of culture-positive or serologically confirmed GAS pharyngitis in a family member that was detected within the 2 weeks of onset of an index patient in the family and was classified as symptomatic or asymptomatic (because all family members had swabs taken once a primary patient was identified in the family). A new episode of pharyngitis was differentiated from a previous episode by a 5-day interval asymptomatic period. A relapse of GAS pharyngitis was defined as a recurrent GAS culture–positive episode of sore throat within 30 days of a previous episode with isolation of the same emm type at both episodes (discussed later).
Pharyngitis was classified using 3 categories of increasing specificity: all sore throat, culture-positive GAS pharyngitis, and serologically confirmed GAS pharyngitis. Serologically confirmed cases included unequivocal and likely serologically confirmed GAS pharyngitis. Unequivocal GAS pharyngitis was any patient with a positive GAS culture and >0.2 log-10 rise in antistreptolysin O (ASO) or anti-DNase B (ADB) titer between acute and convalescent sera. Both titers were performed to increase the chance of detecting evidence of GAS infection, because there is often no clear concordance between the ASO and ADB titers. Likely serologically confirmed GAS pharyngitis included any other case in which the acute serum was taken >7 days after the onset of symptoms (by which time a serologic response was already likely to have been mounted12,13) and in which the ASO titer and/or ADB titer was greater than the upper limit of normal (ULN) for age. We used ULN values determined recently in Melbourne children14 because the ULN values for ASO and ADB titers can vary between populations and within different age groups. When unqualified, the term "serologically confirmed GAS pharyngitis" refers to unequivocal and likely cases together. GAS carriage was defined as the presence of GAS in the upper respiratory tract without an antibody response.15 GAS typing, which is mainly based on the M protein, includes serotyping (Lancefield serologic typing) and emm sequence typing (genotyping of the amino-terminal portion of the M protein gene).
Microbiology
All swabs were placed in Amies transport medium, plated within 24 hours on horse blood agar, and incubated at 37°C in 5% CO2 aerobically for up to 24 hours.16,17 Beta-hemolytic streptococcal colonies were grouped (A, C, or G) by using latex agglutination (Streptex Kit; Oxoid, Basingstoke, United Kingdom). Senior scientist Wayne Devenish performed the ASO and ADB titers using the routine method of hemolysin neutralization at the Royal Children's Hospital.18
Sample Size
On the basis of previous estimates, we expected a 10% incidence of GAS culture–positive sore throat per year in our population. A sample size of 160 families (
240 children), with an intracluster correlation of 0.2, provided an expected width of a standard 95% confidence interval (CI) of ±4% around a 10% point estimate of cumulative incidence and ±5.3% interval around a 20% point estimate. To accommodate up to a 20% dropout rate during the year, we aimed to enroll 200 families, divided evenly among the 3 regions.
Statistical Analysis
Categorical variables were compared between subgroups by using 
2 or Fisher's exact test as appropriate. Univariate Poisson and logistic regression were used to assess potential risk factors for GAS pharyngitis. Data analysis was performed using Stata 7 (Stata Corp, College Station, TX).
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Demographics
A total of 202 families were recruited (853 people), 196 families (828 people) of which completed the study, resulting in a retention rate of 97% for both individuals and families (Table 1). Of the 3 regions, Deer Park had the families with the lowest and Nepean had the families with the highest SES and educational status.
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Sore Throat Episodes
One third of all participants, 16% of adults and 41% of children, reported experiencing a sore throat during the study period (Table 2).
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Primary and Secondary GAS Culture–Positive Sore Throat
There were 54 primary and 32 secondary cases of GAS culture–positive sore throat (Table 3). Of the sore throat episodes in children, 20% were GAS culture positive compared with 26% in adults, but the proportion of GAS culture–positive sore throat episodes was slightly higher in the 5- to 12-year age group (25%); therefore, although adults were 48% less likely to experience a sore throat compared with children (relative risk [RR]: 0.52 [95% CI: 0.4–0.7]; P < .0001), they were just as likely to have a GAS culture–positive throat swab once the sore throat had occurred (RR: 1.2 [95% CI: 0.7–2.0]; P = .44).
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More than half of the secondary cases were in 5- to 12-year-old children (Table 3). Of the secondary cases, 41% were symptomatic and two thirds occurred in children who were aged 5 to 12 years. Within families who experienced a primary case of GAS pharyngitis, the risk for secondary infection was 1.8 times greater than that of primary infection in the community (RR: 1.8 [95% CI: 1.3–2.4]; P = .003).
Serologically Confirmed GAS Culture–Positive Pharyngitis
Nineteen primary episodes were unequivocal GAS pharyngitis, and 16 episodes were likely serologically confirmed GAS pharyngitis (total 35 serologically confirmed cases; Table 3). Of the 19 unequivocal primary cases, 15 (32%) had a rise in ASO titer and 10 (21%) had a rise in ADB titer. The geometric mean initial ASO for the unequivocal group (those with a rise in titer) was 350 U, whereas the mean initial ASO for the likely group (those without a rise in titer) was 733 U. Of the 32 secondary cases, there were 9 unequivocal episodes and 12 likely episodes (total 21 serologically confirmed episodes). There were 3 negative and 8 missing serology episodes. The secondary cases were detected a mean of 8 days after the primary case.
Incidence of Sore Throat, GAS Culture–Positive Pharyngitis, and Serologically Confirmed GAS Pharyngitis
The incidence of acute sore throat, GAS culture–positive pharyngitis, and serologically confirmed GAS pharyngitis were 33, 13, and 8 per 100 person-years, respectively, in children aged 5 to 12 years and 14, 5, and 3 per 100 person-years for adults. The incidence of at least 1 episode of acute sore throat, GAS culture–positive pharyngitis, and serologically confirmed GAS pharyngitis in each family was 60, 20, and 15, respectively, per 100 family-years (Table 2). The estimated incidence of symptomatic GAS culture–positive pharyngitis, including primary and secondary cases, was 10 and 4 per 100 person-years for children aged 5 to 12 years and for adults, respectively (Table 4).
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Risk Factors for GAS Culture–Positive Sore Throat
When examined by Poisson regression, both age and season were independent risk factors for GAS pharyngitis. Children experienced more episodes of sore throat and pharyngitis, both culture and serologically confirmed, compared with adults, and there was a bimodal seasonal pattern peaking in winter/spring and autumn. The SES markers of income, education, and location showed no evidence of association with risk for GAS pharyngitis, which was also not associated with gender. There was no clear association with household crowding, the type of facility attended (child care, preschool, or kindergarten), the hours attended, or the class size and incidence of primary cases in children (Table 5).
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Transmission of GAS Culture–Positive Pharyngitis
Of the families who had a primary case of GAS pharyngitis, 43% had at least 1 secondary case (18 of 42). Of the families who had a secondary case, more than half (11 of 18) had at least 2 secondary cases. Of all people who were at risk (all family members except the index patient), 13% contracted a secondary case (95% CI: 9–18). The emm type of 81% (26 of 32) of the secondary GAS culture–positive isolates was determined, and 96% (25 of 26) of secondary cases in the family had the same emm type as the primary case.
Seasonal Carriage Rates
The GAS carriage rates for children over the 3 seasons were 13%, 8%, and 16% for spring, summer, and winter, respectively. The rate for adults was 2% for each season.
emm Types of Pharyngeal and Carriage Isolates
There were 22 emm types identified, and the most common pharyngeal emm types were 1, 75, and 28. In contrast, the most common carriage emm types were 12, 28, and 1. The most common emm types of the secondary isolates were 4, 1, and 3.2.
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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This is the first prospective, population-based study of the incidence of GAS pharyngitis in a nonindigenous population in an industrialized country since the 1960s and indicates that the incidence of GAS pharyngitis in these settings is essentially unchanged in 50 years. The incidence of GAS culture–positive sore throat in children aged 5 to 12 years (13% per person-year) was very similar to the incidences of 15% and 18% per person-year for children found in 2 studies in suburban American families during the 1950s and 1960s.19,20 Higher estimates have been reported in more crowded, lower SES settings. The incidence of GAS culture–positive sore throat in children who lived in institutions during the 1950s and 1960s was 23% per person-year in the United Kingdom21 and 26% per person-year in the United States.22 In more recent studies of Maori and Pacific Island children in New Zealand and from India and Egypt, the incidence was 50%, 95%, and 30% per person-year, respectively.3,4,23
This is also the first study to include presence of symptoms, throat swab culture findings, and serologic confirmation to determine the relative incidences of sore throat, GAS culture–positive sore throat, and true, serologically confirmed GAS pharyngitis. All published studies used clinical criteria and culture to make the diagnosis of GAS pharyngitis except for 1,23 which used culture and serology but no clinical criteria. We found that one quarter of all people (one third of school-aged children) experienced a sore throat every year, that approximately one third of these were GAS culture positive (in all ages), and that approximately two thirds of GAS culture–positive cases were serologically confirmed GAS pharyngitis. The GAS culture–positive rate was similar to other studies in affluent populations, where rates between 24% and 36% have been reported in school-aged children.24–27 Our finding of a similarly high proportion of GAS culture–positive cases in adults suggests that, although sore throat is less common in adults than children, the chance that an adult who has a sore throat will have culture- or serologically confirmed GAS pharyngitis is similar to that of a school-aged child.
We believe that our definition of serologically confirmed GAS pharyngitis, combining unequivocal and likely cases, gives a more accurate representation of true GAS pharyngitis than unequivocal cases alone. The ideal study would include paired serology on all cases, with the first sample taken at the time of first presentation with symptoms. This was not possible in our cohort study, in which the need to minimize unnecessary blood-taking meant that we had to wait for a positive culture result before approaching participants, which was often followed by logistic delays in arranging for home visits. Therefore, the first sample was sometimes taken 8 days after the onset of sore throat, by which time antistreptococcal antibody titers would already have started rising in true GAS pharyngitis.13 Moreover, most children received antibiotics before the culture results, which is known to reduce the magnitude of the antibody response to GAS extracellular antigens.28–30 Our combined definition ensured that the gold standard, rising antibody titers, was used in all cases in which this could reasonably be assessed (ie, those with first samples taken within 7 days of symptom onset) and that a sensitive but less specific definition, based on population-specific ULN values (which were higher than have previously been used in this population), was used for cases in which the first specimen was delayed. Although this may have resulted in a slight overestimation of the incidence of true GAS pharyngitis, the alternative, rejecting these "likely" cases, would have resulted in a dramatic underestimation.
We found a high incidence of secondary cases, which often affected >1 family member. When exposed, an individual was nearly twice as likely to experience a secondary case in the family than a primary case in the community. This suggests that a single episode of GAS pharyngitis within the family has broader implications in terms of extra cost of medication and time off school and work for additional family members, which should be considered in the management of the index case.
We also found that 20% of children who were younger than 5 years experienced a secondary case of GAS pharyngitis. Higher rates of GAS pharyngitis are becoming increasingly common in younger children, presumably since the advent of child care. A study from Israel surveyed 866 children who were younger than 2 years in 1999, 371 of whom had symptoms, and 98 (26%) of these were positive for GAS.31 In a child care study in the United States in 1989, 18 (27%) of 66 children who were aged <3.5 years and had symptoms were found to be GAS positive.32
The incidence rates of sore throat and GAS pharyngitis did not seem to be influenced by SES or household crowding; however, like most other studies, there was a lack of extremes of these indicators in our study population, making it difficult to examine them as independent risk factors. A lack of association with economic indicators was found in predominantly middle class American families in the 1960s19,25,33,34 and in homogeneously poor families in India.4 The much higher incidence of GAS pharyngitis in children in India4 and from Maori or Pacific Island families in New Zealand3 than was found in our study and others in affluent populations suggests that there may be an association between low SES and higher GAS infection rates, although ethnic differences may also have an influence. Most cohort studies were conducted in small to moderately sized families and were unable to demonstrate an association with crowding,4,35,36 probably because the level of crowding present in military studies that demonstrated an effect of close proximity of beds on acquisitions of GAS37 was of a greater magnitude than has been found in family studies.
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CONCLUSIONS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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This study provides the first reliable, population-based data on the burden of sore throat and GAS pharyngitis in an affluent population for several decades. We have confirmed that GAS pharyngitis remains as common now in school-aged children as it was 50 years ago. Our study also highlights the higher-than-expected proportion of culture-positive GAS pharyngitis in adults and the potentially important role of intrafamilial transmission. We also propose that future cohort studies use our combined definition of serologically proven GAS pharyngitis when there are substantial numbers of cases for which the first blood specimen is delayed.
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ACKNOWLEDGMENTS |
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This work was funded by a 2002–2004 National Health and Medical Research Council (Australia) project grant.
We acknowledge the family medicine practitioners, Dr Michael Howson, Dr Peter Rankin, and Dr Robert Vorich, for assistance in the cohort study and Kris Jamsen for assistance with statistical analysis and data processing.
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FOOTNOTES |
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Accepted May 21, 2007.
Address correspondence to Margaret H. Danchin, PhD, Murdoch Children's Research Institute, Department of Paediatrics, Flemington Road, Parkville 3052, Australia. E-mail: margie.danchin{at}rch.org.au
The authors have indicated they have no financial relationships relevant to this article to disclose.
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