DOI:10.1542/peds.

2006-1025
2006;118;1607-1611 Pediatrics
Aguiar, Jean Vanderpas and Anne Vergison
Pierre Robert Smeesters, Dioclcio Campos, Jr, Laurence Van Melderen, Eurico de
Reduce Unnecessary Antibiotic Use
Pharyngitis in Low-Resources Settings: A Pragmatic Clinical Approach to
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ARTICLE
Pharyngitis in Low-Resources Settings: A Pragmatic
Clinical Approach to Reduce Unnecessary
Antibiotic Use
Pierre Robert Smeesters, MD
a,b
, Diocle cio Campos, Jr, MD, PhD
a
, Laurence Van Melderen, PhD
c
, Eurico de Aguiar, MD
d
,
Jean Vanderpas, MD, PhD
e
, Anne Vergison, MD
b,e
.
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ABSTRACT
OBJECTIVE. Existing scoring systems for the diagnosis of group A streptococcus phar-
yngitis are insensitive or inapplicable in low-resources settings. Bacterial cultures
and rapid tests can allow for antibiotic prescription abstention in high-income
regions. These techniques are not feasible in many low-resources settings, and
antibiotics often are prescribed for any pharyngitis episode. However, judicious
antibiotics prescription in the community also is of concern in low-income coun-
tries. The objective of this study was to develop a clinical decision rule that allows
for the reduction of empirical antibiotic therapy for children with pharyngitis in
low-resources settings by identifying nongroup A streptococcus pharyngitis.
PATIENTS AND METHODS. We prospectively included children with pharyngitis in 3 public
hospitals of Brazil during 9 months in 2004. We lled out clinical questionnaires
and performed throat swabs. Bilateral
2
(2-tailed test) and multivariate analysis
were used to determine score categories. The outcome measures were sensitivity,
specicity, positive likelihood ratio, and posttest probability of nongroup A
streptococcus infection with the clinical approach as compared with throat culture.
RESULTS. A total of 163 of the 220 children had nongroup A streptococcus phar-
yngitis (negative culture). We established a 3-questions decision rule (age and viral
and bacterial signs) with 3 possible answers. The use of this score would prevent
41%to 55%of unnecessary antimicrobial prescriptions. The specicity of the score
for nongroup A streptococcus pharyngitis was 84%.
CONCLUSION. Such a clinical decision rule could be helpful to reduce signicantly
unnecessary antibiotic prescriptions for pharyngitis in children in low-resources
settings.
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Key Words
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T
HE GLOBAL BURDEN of antimicrobial resistance is par-
ticularly pressing in developing countries.
1
The level
of antibiotic resistance is correlated clearly to antibiotic
consumption.
26
In Western Europe and North America,
modications of prescribing practice have been attained
with diagnosis and prescribing guidelines.
7
These strate-
gies have not been evaluated in developing countries,
where health care systems differ greatly from occidental
ones, so locally validated interventions are needed.
8
Acute pharyngitis is 1 of the most common childhood
illnesses. Viruses are responsible for 80% of them, and
group A Streptococcus (GAS) accounts for 15% of
these infections.
9
In cases of GAS as the cause, antibiotics
are prescribed frequently.
9
Recent studies underlined the
high proportion (20%50%) of GAS carriers among
children, and distinguishing between carriers with viral
pharyngitis and real GAS pharyngitis is impossible in
general practice.
10
In low-income regions, there is no access to microbi-
ologic diagnosis of common GAS infections such as phar-
yngitis. Presumptive diagnosis relies on clinical signs
only, although the positive predictive value of clinical
signs and symptoms has been shown to be extremely
low.
11
The World Health Organization clinical decision
rule for streptococcal pharyngitis suggests treating chil-
dren who are younger than 5 years when pharyngeal
exudate plus enlarged, tender cervical nodes are found.
The evaluation of this approach was performed in Brazil,
Egypt, and Croatia and presented a very low sensitivity
(3.6%8.5%).
12
Some clinical scores, developed in med-
ical settings where microbiology is available in the daily
practice, have already been published.
1315
Because of the
unavailability of microbiologic testing in low-income re-
gions, clinicians often empirically treat all pharyngitis
with antibiotics. In these settings, there clearly is a need
for modied clinical decision rules with a higher sensi-
tivity and adequate specicity. To our knowledge, only 1
interesting study proposed a clinical decision rule that
is designed for the management of streptococcal phar-
yngitis in low-incomes regions (Egypt).
16
However, it
has not yet been validated clinically, and we have no
data so far that it could be applied in other low-income
settings.
Bacterial culture and rapid tests are not available for
common infections in public hospitals of Brazil (for
structural and cost reasons). Like many other public
institutions in developing countries, all children with
clinical pharyngitis are treated empirically with antibiot-
ics. We developed a clinical decision rule that allows for
a reduction in empirical antibiotic therapy for children
with pharyngitis in Brazil, as an example of a low-
resource settings. We directed our clinical analysis for
best identifying non-GAS pharyngitis rather than GAS
pharyngitis.
METHODS
Patients
All children (015 years) who attended the emergency
department of 3 public hospitals of Brazil (Academic
hospital of Braslia, Regional Hospital of the south wing
of Braslia, and Medical Unit of Sa o Sebastia o, with 250,
180, and 40 beds, respectively) with signs and symptoms
of acute pharyngitis from February 1 to October 31,
2004, were enrolled prospectively in the study. This
study was approved by the ethical board of all partici-
pant hospitals. Exclusion criteria were current antimi-
crobial treatment or refusal to participate in the study. A
written informed consent was obtained from the chil-
drens parents or guardian. A predesigned questionnaire
that comprised general data (date of birth, gender, anti-
microbial treatment in the past 6 months, and the pre-
scribed treatment for current episode), demographic in-
formation (number of children living under the same
roof), and description of infection was used for data
collection. Signs and symptoms of pharyngitis were de-
rived from the practice guidelines of the Infectious Dis-
eases Society of America and included the presence of
(1) conjunctivitis, coryza, cough, diarrhea, and viral-like
exanthema, features suggestive of viral cause and de-
ned as viral signs; or (2) fever 38.5C, tender cervical
node, headache, petechia on the palate, abdominal pain,
and sudden onset (12 hours), features suggestive of
GAS as causative agent and dened as bacterial signs.
9
The pediatricians lled out the questionnaire, measured
the weight and height, and collected the throat secretion
samples using sterile cotton-tipped swabs. Physicians
were trained to standardize the swabbing technique.
Laboratory Analysis
The swabs were plated on 5% sheep blood agar plates
that were incubated at 37C for 24 to 48 hours. GAS
were identied by a hemolysis on blood agar, colony
morphology, Gram stain, catalase reaction, sensitivity to
0.04-U bacitracin disk, latex agglutination (Slidex,
strepto A, Biome rieux, France), and a commercially
available method following the manufacturers recom-
mendations (MicroScan, Dade Behring, Sa o Paulo, Bra-
zil).
Statistical Analysis
We used the data that were collected in this study to
develop the clinical decision rule. The association of
clinical ndings with negative throat culture was as-
sessed with the use of a bilateral
2
(2-tailed test). Con-
tinuous variables also were assessed using a t test anal-
ysis (Gaussian distribution). The 3 more signicant items
(age, viral signs, and bacterial signs) were retained for
multivariate analysis (using SPSS 11.0; SPSS, Chicago,
IL). The weighting of each question was based on the
value of the regression coefcients and optimized for
e1608 ||||| c| .|
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best results with our data. The outcome measures were
sensitivity, specicity, positive likelihood ratio, and post-
test probability of non-GAS infection with the clinical
approach as compared with throat culture.
RESULTS
General Data
A total of 220 patients were included during the study
period. The mean SD age was 6.6 2.8 years, and
56% were male. An antimicrobial treatment had been
prescribed in the past 6 months for 80 (36%) patients.
Most (90%) of them had received benzathine penicillin
or amoxicillin. The mean number of children who lived
under the same roof was 2.2 (range: 18 children).
Among the 220 patients, 163 (74%) had no GAS isolated
from their throat, whereas 57 (26%) had a pharyngeal
positive culture. A GAS-positive culture was recovered
in 0%, 18%, and 33% of children who were 0 to 36
months of age, 37 to 59 months of age, and older than 59
months, respectively (P .003). All children were
treated empirically with antibiotics independent of the
bacteriologic result. Most (83%) received intramuscular
benzathine penicillin. Other treatments included amoxi-
cillin (9%), macrolides (3%), cephalexin (3%), and
amoxicillin with clavulanate (2%).
Clinical Decision Rule
The 3 questions (age, viral signs, and bacterial signs) of
our decision rule had a value of the regression coef-
cients of 2.8, 0.8, and 1.0, respectively. The scoring
system is presented in Table 1, and the decision rule to
apply according to the score is shown in Table 2.
The classication of our children in our study accord-
ing to this clinical approach and the result of the throat
culture is shown in Table 3. A cutoff of 8 was chosen as
having the optimal risk/benet ratio. The discriminative
ability of the model at the cutoff value 8 was calculated
according to sensitivity, specicity, positive likelihood
ratio, and posttest probability in Table 4.
We designed 2 different decision rules depending on
the accessibility to microbiologic diagnosis. A clinical
score 8 suggests a symptomatic treatment with an 84%
specicity for non-GAS pharyngitis. Those children had
a likelihood ratio for non-GAS pharyngitis of 2.6, which
give a posttest probability for non-GAS pharyngitis of
88%. Nine (16%) of 57 children with a score 8 nev-
ertheless had a GAS-positive culture. The clinical char-
acteristics of these children are shown in Table 5. In
medical settings where bacteriologic diagnosis is unavail-
able, the application of that recommendation would
have reduced the antibiotic prescription by 41%.
In medical settings where limited bacteriologic diag-
nosis is available, a score 8 can be rened into 2
distinct situations. In case of a score result from 5 to 7, an
antibiotic treatment would be recommended if the cul-
ture were positive for GAS. Only 16% of the children of
our population would fall into this intermediate category
TABLE 1 Scoring System
Question Answer Value
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.no .||| oc|c|u|nc ||c ||c|.ocu||. oo||on . |o.n |n .||c 2
TABLE 2 Treatment Decision Rule According to Total Clinical Score
in 2 Different Situations of Availability of Microbiological
Resources
Total Score Microbiological
Diagnosis
Treatment
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TABLE 3 Classication of Pharyngitis According to the Total Score, Throat Culture Result (GAS Negative
or GAS Positive), and Age
Total
Score
No. of Cases
(%)
Throat Culture Age, mo
GAS
Negative
GAS
Positive
035 3659 60
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109 (0, /4 ? 0 ?1 /8
o|.| 220 (100, 1o? / 20 o 144
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and would require a microbiologic diagnostic conrma-
tion. A score result 5 indicates an antibiotic treatment
without bacteriologic conrmation. The application of
this recommendation would have reduced the antibiotic
prescription by 55%.
DISCUSSION
The prevalence of pharyngitis associated with GAS-pos-
itive culture was similar (26%) to previous reports.
9
Therefore, at least 74% of the children were treated
unnecessarily with antibiotics. The presence of GAS in
the throat sample depended on the age of the children.
As shown previously,
9
the incidence of GAS pharyngitis
was lower in children who were younger than 5 years
than in older children. However, a signicant proportion
of children had a GAS-positive culture in the 37- to
59-month age group. This would lead us to propose a
lower age limit (3 years) for considering a GAS cause for
pharyngitis as chosen for the Canadian sore throat score
and in contrast with the 5-year cutoff chosen by the
Infectious Diseases Society of America. In children who
were younger than 36 months, no GAS was isolated in
our study. This result differs from other studies that
showed the presence of GAS in the throat of children
who were younger than 3 years.
17,18
However, the pro-
portion of GAS infections (or colonization?) in children
who are younger than 3 years is lower and is well
correlated to age in this young age group. Epidemiologic
variations over time and location also have been dem-
onstrated with GAS.
19,20
We assume, until validation and
with the present epidemiology, that the absence of GAS
in children who were younger than 3 years in our data
could justify the symptomatic treatment of all of these
children.
A 41% to 55% sparing of antibiotic prescriptions by
use of our clinical decision rule would represent a sig-
nicant impact given the high prevalence of pharyngitis
in children. As in most cases, the children were given a
benzathine penicillin G shot; this would also mean a
signicant reduction of the pain associated with this
treatment and a decrease of the nancial cost related to
the antibiotic injection.
The posttest probability for non-GAS pharyngitis was
high (corresponding to a theoretical positive predictive
value of 88.1%), even without taking into account the
GAS carriers among these children. The use of that prag-
matic approach in our population would have resulted
in antibiotic abstention for 9 (16%) children with phar-
yngitis that was associated with a GAS-positive culture.
However, this seems acceptable because, rst, 16% is
lower than the general pediatric GAS carriage rates
(20%50%).
10
Second, the sensitivity of throat culture is
limited to a maximum of 90% in study settings (this
could be lower in the day-to-day medical practice), and
the culture does not distinguish between carriage and
infection. Serologic examinations were not performed in
this study, and we do not know whether these 9 chil-
dren were infected by GAS or only carriers. In an addi-
tional validation study, the capacity of this scoring sys-
tem to discriminate between carriage and infection will
be investigated in the patients with high score and pos-
itive culture. The true specicity of our clinical decision
rule could be underestimated in the present study if such
patients were carriers.
Rheumatic fever still is highly prevalent in many
developing countries (one third of the Brazilian heart
surgeries in 2004).
21
In pediatric patients, the efcacy of
primary prevention of rheumatic fever by antibiotic
treatment of GAS pharyngitis has not been demon-
strated rmly.
22
Some studies showed a positive effect of
this prevention, but design aws and use of atypical
populations limit the applicability of these studies to
children in developing countries.
23
However, a careful
attitude has been favored and antimicrobial treatment of
GAS pharyngitis probably can be justied in countries
with a high prevalence of rheumatic fever. Nevertheless,
the hypothetical prevention of rheumatic fever has to be
balanced against the development of antimicrobial resis-
tance and its consequences.
Another scoring system was constructed for use in
children from Cairo (Egypt).
16
The use of this score
would have allowed for a 37.5% reduction of unneces-
sary antibiotic therapy with 9% of missed streptococcal
cases in the study population of Cairo. When we applied
this Egyptian score to our Brazilian children population,
TABLE 4 Accuracy of the Clinical Diagnosis for the Identication of
Non-GAS Pharyngitis With a Cutoff of >8
Sensitivity
(95% CI)
Specicity
(95% CI)
LHR
(95% CI)
Posttest Probability
(95% CI)
041 (0??048, 084 (0/094, 2o (149, 088 (0/909,
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.||| /oo|||vc .u||u|c |c o|c|c| o|o|.|||||, | 0/4 (1o? o| 220, |c oo||c| o|o|.|||||, |
||c o|ooo|||ono| .|||o|cn.|o|.vc ||.| o.|||.u|.| .o|c |cu|| .nonon/ o|.|,nj||| |oc
|cu|| .|c co|cco .||| . 9 .onocn.c |n|c|v.| (|,
TABLE 5 Children Who Would Not Have Been Treated With
Antibiotic if the Clinical Decision Rule Had Been Used
Age, y Viral Signs Bacterial Signs
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we obtained only a 20% reduction of unnecessary anti-
biotic therapy with 12.5% missed streptococcal cases.
This variability could be attributable to epidemiologic
differences between Cairo and Brazil. However, a scor-
ing system directed for best sensitivity to non-GAS phar-
yngitis with an acceptable specicity theoretically could
be more efcient in terms of antibiotic reduction.
There are several limitations to our study. First, the
number of included children was small. Second, this
clinical decision rule has to be validated on a large pop-
ulation of children who attend different medical settings.
Third, the acceptability of this scoring system by the
general physician and pediatricians has to be evaluated
in the daily practice. The validation also should include
bacterial serology and viral culture and serologies to
improve distinction between carriage and infection.
CONCLUSIONS
This clinical decision rule for pharyngitis management
was constructed on the basis of the reality of public
pediatric practice in Brazil, which could be representa-
tive of many emerging countries of the developing
world. Clinically based and locally designed guidelines in
such setting could be a potent incentive for physicians to
modify their prescribing practice.
ACKNOWLEDGMENTS
Dr Smeesters is supported by a grant of the Belgian Kids
Foundation. The Medcorp society supported us for the
bacteriologic diagnosis (MicroScan).
We thank Maria Custodia Machado Ribeiro, Denise
Nogueira, Joceleia de Lira, Maria Gloria Andrade,
Daniela de Sales M. dos Santos, Marne Rodrigues, Am-
abel Fernandes Correia, Marina Sancha Queiroga, Jeane
Bezerra Rodrigues, Francisca Moura de Oliveira, Maria
do Carmo Teixeira, Divina Maria Dias, Georges Casimir,
and Andre Kahn for help in the realization of this study.
We thank Philippe Lepage for critical proofreading of the
manuscript. We thank all of the professionals of the 3
participating hospitals for kind collaboration. Dr Van
Melderen is chercheur qualie du Fonds National de la
Recherche Scientique.
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DOI:10.1542/peds.2006-1025
2006;118;1607-1611 Pediatrics
Aguiar, Jean Vanderpas and Anne Vergison
Pierre Robert Smeesters, Dioclcio Campos, Jr, Laurence Van Melderen, Eurico de
Reduce Unnecessary Antibiotic Use
Pharyngitis in Low-Resources Settings: A Pragmatic Clinical Approach to
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