Pharyngitis in Low-Resources Settings: A Pragmatic Clinical Approach to

Reduce Unnecessary Antibiotic Use

Pierre Robert Smeesters, Dioclécio Campos, Jr, Laurence Van Melderen, Eurico de
Aguiar, Jean Vanderpas and Anne Vergison
Pediatrics 2006;118;1607-1611
DOI: 10.1542/peds.2006-1025

This information is current as of December 11, 2006

The online version of this article, along with updated information and services, is
located on the World Wide Web at:
http://www.pediatrics.org/cgi/content/full/118/6/e1607

PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly

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ARTICLE

Pharyngitis in Low-Resources Settings: A Pragmatic

Clinical Approach to Reduce Unnecessary
Antibiotic Use
Pierre Robert Smeesters, MDa,b, Dioclécio Campos, Jr, MD, PhDa, Laurence Van Melderen, PhDc, Eurico de Aguiar, MDd,
Jean Vanderpas, MD, PhDe, Anne Vergison, MDb,e

aServiço de Pediatria, Hospital Universitário de Brası́lia, Universidade de Brası́lia, Brası́lia, Brazil; bDépartement des Maladies Infectieuses, Hôpital Universitaire des Enfants

Reine Fabiola, cLaboratoire de Génétique des Procaryotes, Institut de Biologie et de Médecine Moléculaire, and eUnité d’épidémiologie et d’hygiène hospitalière, Hôpital
Brugmann, Université Libre de Bruxelles, Brussels, Belgium; dServiço de Microbiologia, Hospital Regional da Asa Sul, Brası́lia, Brazil

The authors have indicated they have no financial relationships relevant to this article to disclose.

ABSTRACT
OBJECTIVE. Existing scoring systems for the diagnosis of group A streptococcus phar-
yngitis are insensitive or inapplicable in low-resources settings. Bacterial cultures
www.pediatrics.org/cgi/doi/10.1542/
and rapid tests can allow for antibiotic prescription abstention in high-income peds.2006-1025
regions. These techniques are not feasible in many low-resources settings, and doi:10.1542/peds.2006-1025
antibiotics often are prescribed for any pharyngitis episode. However, judicious
Key Words
antibiotics prescription in the community also is of concern in low-income coun- pharyngitis, practice guidelines, antibiotic
tries. The objective of this study was to develop a clinical decision rule that allows use, developing countries
for the reduction of empirical antibiotic therapy for children with pharyngitis in Abbreviation
GAS— group A streptococcus
low-resources settings by identifying non– group A streptococcus pharyngitis.
Accepted for publication Jul 11, 2006
PATIENTS AND METHODS. We prospectively included children with pharyngitis in 3 public Address correspondence to Pierre Robert
Smeesters, MD, Département des Maladies
hospitals of Brazil during 9 months in 2004. We filled out clinical questionnaires Infectieuses, Hôpital Universitaire des Enfants
and performed throat swabs. Bilateral ␹2 (2-tailed test) and multivariate analysis Reine Fabiola, Av JJ Crocq 15, 1020 Bruxelles,
Belgium. E-mail: psmeeste@ulb.ac.be
were used to determine score categories. The outcome measures were sensitivity,
PEDIATRICS (ISSN Numbers: Print, 0031-4005;
specificity, positive likelihood ratio, and posttest probability of non– group A Online, 1098-4275). Copyright © 2006 by the
streptococcus infection with the clinical approach as compared with throat culture. American Academy of Pediatrics

RESULTS. A total of 163 of the 220 children had non– group 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 specificity of the score
for non– group A streptococcus pharyngitis was ⬎84%.
CONCLUSION. Such a clinical decision rule could be helpful to reduce significantly
unnecessary antibiotic prescriptions for pharyngitis in children in low-resources
settings.

PEDIATRICS Volume 118, Number 6, December 2006 e1607

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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.2–6 In Western Europe and North America,
modifications 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.13–15 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 modified clinical decision rules with a higher sensi-
tivity and adequate specificity. 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.
e1608 SMEESTERS et al
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METHODS
Patients
All children (0 –15 years) who attended the emergency
department of 3 public hospitals of Brazil (Academic
hospital of Brası́lia, Regional Hospital of the south wing
of Brası́lia, and Medical Unit of São Sebastião, 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-
dren’s 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-
fined as viral signs; or (2) fever ⬎38.5°C, tender cervical
node, headache, petechia on the palate, abdominal pain,
and sudden onset (⬍12 hours), features suggestive of
GAS as causative agent and defined as bacterial signs.9
The pediatricians filled 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 37°C for 24 to 48 hours. GAS
were identified by a ␤ hemolysis on blood agar, colony
morphology, Gram stain, catalase reaction, sensitivity to
0.04-U bacitracin disk, latex agglutination (Slidex,
strepto A, Biomérieux, France), and a commercially
available method following the manufacturer’s recom-
mendations (MicroScan, Dade Behring, São 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 findings 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 significant 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 coefficients and optimized for
 TABLE 1 Scoring System under the same roof was 2.2 (range: 1– 8 children).
Question Answer Value Among the 220 patients, 163 (74%) had no GAS isolated
Age? ⱕ35 mo 20
from their throat, whereas 57 (26%) had a pharyngeal
36–59 mo 6 positive culture. A GAS-positive culture was recovered
ⱖ60 mo 2 in 0%, 18%, and 33% of children who were 0 to 36
Viral signs? No sign 0 months of age, 37 to 59 months of age, and older than 59
1 sign 7 months, respectively (P ⫽ .003). All children were
ⱖ2 signs 10
Bacterial signs? No sign 10
treated empirically with antibiotics independent of the
1 sign ⫺2 bacteriologic result. Most (83%) received intramuscular
ⱖ2 signs ⫺4 benzathine penicillin. Other treatments included amoxi-
Total score cillin (9%), macrolides (3%), cephalexin (3%), and
Viral signs were defined as conjunctivitis, coryza, cough, diarrhea, and viral-like exanthema. amoxicillin with clavulanate (2%).
Bacterial signs were defined as tender cervical node, headache, petechia on the palate, fever
⬎38.5°C, abdominal pain, and sudden onset (⬍12 hours). The total score will be determined by
summing the values attributed to age and presence or absence of viral and bacteriological signs Clinical Decision Rule
and will determine the therapeutic option as shown in Table 2.
The 3 questions (age, viral signs, and bacterial signs) of
our decision rule had a ␤ value of the regression coeffi-
TABLE 2 Treatment Decision Rule According to Total Clinical Score cients of 2.8, 0.8, and 1.0, respectively. The scoring
in 2 Different Situations of Availability of Microbiological system is presented in Table 1, and the decision rule to
Resources apply according to the score is shown in Table 2.
Total Score Microbiological Treatment The classification of our children in our study accord-
Diagnosis ing to this clinical approach and the result of the throat
Bacteriological diagnosis is culture is shown in Table 3. A cutoff of 8 was chosen as
unavailable
having the optimal risk/benefit ratio. The discriminative
ⱖ8 Symptomatic
⬍8 Antibiotic ability of the model at the cutoff value ⱖ8 was calculated
Limited bacteriological diagnosis according to sensitivity, specificity, positive likelihood
is available ratio, and posttest probability in Table 4.
ⱖ8 No Symptomatic We designed 2 different decision rules depending on
5–7 Yes Antibiotic if positive culture
the accessibility to microbiologic diagnosis. A clinical
⬍5 No Antibiotic
score ⱖ8 suggests a symptomatic treatment with an 84%
specificity for non-GAS pharyngitis. Those children had
a likelihood ratio for non-GAS pharyngitis of 2.6, which
best results with our data. The outcome measures were
give a posttest probability for non-GAS pharyngitis of
sensitivity, specificity, positive likelihood ratio, and post-
88%. Nine (16%) of 57 children with a score ⱖ8 nev-
test probability of non-GAS infection with the clinical
ertheless had a GAS-positive culture. The clinical char-
approach as compared with throat culture.
acteristics of these children are shown in Table 5. In
medical settings where bacteriologic diagnosis is unavail-
RESULTS
able, the application of that recommendation would
General Data have reduced the antibiotic prescription by 41%.
A total of 220 patients were included during the study In medical settings where limited bacteriologic diag-
period. The mean ⫾ SD age was 6.6 ⫾ 2.8 years, and nosis is available, a score ⬍8 can be refined into 2
56% were male. An antimicrobial treatment had been distinct situations. In case of a score result from 5 to 7, an
prescribed in the past 6 months for 80 (36%) patients. antibiotic treatment would be recommended if the cul-
Most (90%) of them had received benzathine penicillin ture were positive for GAS. Only 16% of the children of
or amoxicillin. The mean number of children who lived our population would fall into this intermediate category

TABLE 3 Classification of Pharyngitis According to the Total Score, Throat Culture Result (GAS Negative
or GAS Positive), and Age
Total No. of Cases Throat Culture Age, mo
Score (%)
GAS GAS 0–35 36–59 ⱖ60
Negative Positive
ⱖ8 76 (34) 67 9 20 25 31
5–7 35 (16) 22 13 0 0 35
⬍5 109 (50) 74 35 0 31 78
Total 220 (100) 163 57 20 56 144
The number of children with positive and negative GAS culture and the age repartition are shown for 3 different score results.

PEDIATRICS Volume 118, Number 6, December 2006 e1609

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 TABLE 4 Accuracy of the Clinical Diagnosis for the Identification of onstrated with GAS.19,20 We assume, until validation and
Non-GAS Pharyngitis With a Cutoff of >8 with the present epidemiology, that the absence of GAS
Sensitivity Specificity LHR⫹ Posttest Probability in children who were younger than 3 years in our data
(95% CI) (95% CI) (95% CI) (95% CI) could justify the symptomatic treatment of all of these
0.41 (0.33–0.48) 0.84 (0.75–0.94) 2.6 (1.5–4.9) 0.88 (0.79–0.95) children.
Sensitivity is defined as the proportion of children who have non-GAS pharyngitis and a score of A 41% to 55% sparing of antibiotic prescriptions by
ⱖ8. Specificity is the proportion of children who do not have non-GAS pharyngitis and have a use of our clinical decision rule would represent a sig-
score of ⬍8. The positive likelihood ratio (LHR⫹) expresses the ratio of the probability that a
nificant impact given the high prevalence of pharyngitis
score result would be expected in children with non-GAS pharyngitis as opposed to children
with GAS-positive culture. The pretest probability is 0.74 (163 of 220). The posttest probability is in children. As in most cases, the children were given a
the proportion of children who have that particular score result and non-GAS pharyngitis. Those benzathine penicillin G shot; this would also mean a
results are expressed with a 95% confidence interval (CI).
significant reduction of the pain associated with this
treatment and a decrease of the financial cost related to
TABLE 5 Children Who Would Not Have Been Treated With
the antibiotic injection.
Antibiotic if the Clinical Decision Rule Had Been Used
The posttest probability for non-GAS pharyngitis was
high (corresponding to a theoretical positive predictive
Age, y Viral Signs Bacterial Signs
value of 88.1%), even without taking into account the
3 Cough Fever ⬎38.5°C and tender cervical node
4 Cough Fever ⬎38.5°C and petechia
GAS carriers among these children. The use of that prag-
5 Coryza and cough Headache, sudden onset (⬍12 h) matic approach in our population would have resulted
6 Coryza and cough Absent in antibiotic abstention for 9 (16%) children with phar-
6 Coryza and cough Headache, fever ⬎38.5°C, tender cervical yngitis that was associated with a GAS-positive culture.
node, abdominal pain, and sudden onset However, this seems acceptable because, first, 16% is
(⬍12 h)
7 Coryza and cough Absent
lower than the general pediatric GAS carriage rates
8 Absent Absent (20%–50%).10 Second, the sensitivity of throat culture is
8 Coryza and cough Fever ⬎38.5°C and tender cervical node limited to a maximum of 90% in study settings (this
9 Coryza and cough Fever ⬎38.5°C 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
and would require a microbiologic diagnostic confirma- this study, and we do not know whether these 9 chil-
tion. A score result ⬍5 indicates an antibiotic treatment dren were infected by GAS or only carriers. In an addi-
without bacteriologic confirmation. The application of tional validation study, the capacity of this scoring sys-
this recommendation would have reduced the antibiotic tem to discriminate between carriage and infection will
prescription by 55%. be investigated in the patients with high score and pos-
itive culture. The true specificity of our clinical decision
DISCUSSION rule could be underestimated in the present study if such
The prevalence of pharyngitis associated with GAS-pos- patients were carriers.
itive culture was similar (26%) to previous reports.9 Rheumatic fever still is highly prevalent in many
Therefore, at least 74% of the children were treated developing countries (one third of the Brazilian heart
unnecessarily with antibiotics. The presence of GAS in surgeries in 2004).21 In pediatric patients, the efficacy of
the throat sample depended on the age of the children. primary prevention of rheumatic fever by antibiotic
As shown previously,9 the incidence of GAS pharyngitis treatment of GAS pharyngitis has not been demon-
was lower in children who were younger than 5 years strated firmly.22 Some studies showed a positive effect of
than in older children. However, a significant proportion this prevention, but design flaws and use of atypical
of children had a GAS-positive culture in the 37- to populations limit the applicability of these studies to
59-month age group. This would lead us to propose a children in developing countries.23 However, a careful
lower age limit (3 years) for considering a GAS cause for attitude has been favored and antimicrobial treatment of
pharyngitis as chosen for the Canadian sore throat score GAS pharyngitis probably can be justified in countries
and in contrast with the 5-year cutoff chosen by the with a high prevalence of rheumatic fever. Nevertheless,
Infectious Diseases Society of America. In children who the hypothetical prevention of rheumatic fever has to be
were younger than 36 months, no GAS was isolated in balanced against the development of antimicrobial resis-
our study. This result differs from other studies that tance and its consequences.
showed the presence of GAS in the throat of children Another scoring system was constructed for use in
who were younger than 3 years.17,18 However, the pro- children from Cairo (Egypt).16 The use of this score
portion of GAS infections (or colonization?) in children would have allowed for a 37.5% reduction of unneces-
who are younger than 3 years is lower and is well sary antibiotic therapy with 9% of missed streptococcal
correlated to age in this young age group. Epidemiologic cases in the study population of Cairo. When we applied
variations over time and location also have been dem- this Egyptian score to our Brazilian children population,

e1610 SMEESTERS et al
Downloaded from www.pediatrics.org by on December 11, 2006
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 specificity theoretically could
be more efficient 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 Kid’s
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 André 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 qualifié du Fonds National de la
Recherche Scientifique.
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PEDIATRICS Volume 118, Number 6, December 2006 e1611
 Pharyngitis in Low-Resources Settings: A Pragmatic Clinical Approach to
Reduce Unnecessary Antibiotic Use
Pierre Robert Smeesters, Dioclécio Campos, Jr, Laurence Van Melderen, Eurico de
Aguiar, Jean Vanderpas and Anne Vergison
Pediatrics 2006;118;1607-1611
DOI: 10.1542/peds.2006-1025
This information is current as of December 11, 2006

Updated Information including high-resolution figures, can be found at:

& Services http://www.pediatrics.org/cgi/content/full/118/6/e1607
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