Pharyngitis in Low-Resources Settings. a Pragmatic Clinical Approach to Reduce Unnecessary Antibi

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DOI:10.1542/peds.2006-10252006;118;1607-1611Pediatrics

Aguiar, Jean Vanderpas and Anne VergisonPierre Robert Smeesters, Dioclcio Campos, Jr, Laurence Van Melderen, Eurico de

Reduce Unnecessary Antibiotic UsePharyngitis in Low-Resources Settings: A Pragmatic Clinical Approach to

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ARTICLE

Pharyngitis in Low-Resources Settings: A PragmaticClinical Approach to Reduce UnnecessaryAntibiotic Use

Pierre Robert Smeesters, MDa,b, Dioclecio Campos, Jr, MD, PhDa, Laurence Van Melderen, PhDc, Eurico de Aguiar, MDd,

Jean Vanderpas, MD, PhDe, Anne Vergison, MDb,e

aServico de Pediatria, Hospital Universitario de Bras lia, Universidade de Bras lia, Braslia, Brazil; bDepartement des Maladies Infectieuses, Hopital Universitaire des Enfants

Reine Fabiola, cLaboratoire de Genetique des Procaryotes, Institut de Biologie et de Medecine Moleculaire, and eUnite depidemiologie et dhygiene hospital iere, Hopital

Brugmann, Universite Libre de Bruxelles, Brussels, Belgium; dServico de Microbiologia, Hospital Regional da Asa Sul, Bras lia, 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

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 non group A streptococcus pharyngitis.

PATIENTS AND METHODS. We prospectively included children with pharyngitis in 3 public

hospitals of Brazil during 9 months in 2004. We filled 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,

specificity, positive likelihood ratio, and posttest probability of non group 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 specificity of the score

for nongroup 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.

www.pediatrics.org/cgi/doi/10.1542/

peds.2006-1025doi:10.1542/peds.2006-1025

Key Words

pharyngitis, practice guidelines, antibiotic

use, developing countries

Abbreviation

GASgroup A streptococcus

Accepted for publication Jul 11, 2006

Address correspondence to Pierre Robert

Smeesters, MD, Departement des Maladies

Infectieuses, Hopital Universitaire des Enfants

Reine Fabiola, Av JJ Crocq 15, 1020 Bruxelles,

Belgium. E-mail: [email protected]

PEDIATRICS (ISSNNumbers:Print, 0031-4005;

Online, 1098-4275). Copyright 2006by the

AmericanAcademy of Pediatrics

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THE GLOBAL BURDEN of antimicrobial resistance is par-ticularly pressing in developing countries.1 The levelof antibiotic resistance is correlated clearly to antibiotic

consumption.26 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 occidentalones, 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 dailypractice, 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 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.

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 Sao Sebastiao, 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-

fined as viral signs; or (2) fever38.5C, 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 37C 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, Biomerieux, France), and a commercially

available method following the manufacturers recom-

mendations (MicroScan, Dade Behring, Sao 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

e1608 SMEESTERS et alby on January 4, 2007www.pediatrics.orgDownloaded from


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best results with our data. The outcome measures were

sensitivity, specificity, 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 thebacteriologic 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 coeffi-

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 classification 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/benefit ratio. The discriminative

ability of the model at the cutoff value 8 was calculated

according to sensitivity, specificity, positive likelihood

ratio, and posttest probability in Table 4.

We designed 2 different decision rules depending on

the accessibility to microbiologic diagnosis. A clinical

score8 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

give a posttest probability for non-GAS pharyngitis of88%. 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 refined 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

Age? 35 mo 20

3659 mo 6

60 mo 2

Viral signs? No sign 0

1 sign 7

2 signs 10

Bacterial signs? No sign 10

1 sign 2

2 signs 4

Total score

Viral signs were defined as conjunctivitis, coryza, cough, diarrhea, and viral-like exanthema.

Bacterial signs were defined as tender cervical node, headache, petechia on the palate, fever

38.5C,abdominalpain,and suddenonset(12hours).Thetotalscorewillbedeterminedby

summingthevaluesattributedtoageandpresenceorabsenceofviralandbacteriologicalsigns

and will determine the therapeutic option as shown in Table 2.

TABLE 2 Treatment Decision Rule Accordingto Total Clinical Score

in 2 Different Situationsof Availability of Microbiological

Resources

Total Score MicrobiologicalDiagnosis

Treatment

Bacteriological diagnosis is

unavailable

8 Symptomatic

8 Antibiotic

Limited bacteriological diagnosis

is available

8 No Symptomatic

57 Yes Antibiotic if positive culture

5 No Antibiotic

TABLE 3 Classification of Pharyngitis Accordingto the Total Score,Throat Culture Result(GAS Negative

or GASPositive),and Age

Total

Score

No. of Cases

(%)

Throat Culture Age, mo

GAS

Negative

GAS

Positive

035 3659 60

8 76 (34) 67 9 20 25 31

57 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.



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and would require a microbiologic diagnostic confirma-

tion. A score result 5 indicates an antibiotic treatment

without bacteriologic confirmation. 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 significant 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-

nificant impact given the high prevalence of pharyngitisin children. As in most cases, the children were given a

benzathine penicillin G shot; this would also mean a

significant reduction of the pain associated with this

treatment and a decrease of the financial 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, first, 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 specificity 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 efficacy of

primary prevention of rheumatic fever by antibiotic

treatment of GAS pharyngitis has not been demon-

strated firmly.22 Some studies showed a positive effect of

this prevention, but design flaws 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 justified 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 Diagnosisfor the Identification of

Non-GAS Pharyngitis With a Cutoff of>8

Sensitivity

(95% CI)

Specificity

(95% CI)

LHR

(95% CI)

Posttest Probability

(95% CI)

0.41(0.330.48) 0.84(0.750.94) 2.6 (1.54.9) 0.88(0.790.95)

Sensitivity isdefinedas theproportionof childrenwho havenon-GAS pharyngitisand a score of

8. Specificity is the proportion of children who do not have non-GAS pharyngitis and have a

score of8. The positive likelihood ratio (LHR) expresses the ratio of the probability that a

score result would be expected in children with non-GAS pharyngitis as opposed to children

withGAS-positiveculture. Thepretestprobabilityis 0.74(163of 220). Theposttestprobabilityis

theproportionof childrenwhohave thatparticularscoreresultand non-GASpharyngitis.Those

results are expressed with a 95% confidence interval (CI).

TABLE 5 Children WhoWouldNot Have Been Treated With

Antibiotic if theClinicalDecision Rule HadBeen Used

Age, y Viral Signs Bacterial Signs

3 Cough Fever38.5C and tender cervical node

4 Cough Fever38.5C and petechia

5 Coryza and cough Headache, sudden onset (12 h)

6 Coryza and cough Absent

6 Coryza and cough Headache, fever

38.5C, tender cervicalnode, abdominal pain, and sudden onset

(12 h)

7 Coryza and cough Absent

8 Absent Absent

8 Coryza and cough Fever38.5C and tender cervical node

9 Coryza and cough Fever38.5C

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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 specificity theoretically could

be more efficient in terms of antibiotic reduction.

There are several limitations to our study. First, thenumber 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 publicpediatric 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 qualifie du Fonds National de la

Recherche Scientifique.

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DOI:10.1542/peds.2006-1025

2006;118;1607-1611PediatricsAguiar, Jean Vanderpas and Anne Vergison

Pierre Robert Smeesters, Dioclcio Campos, Jr, Laurence Van Melderen, Eurico deReduce Unnecessary Antibiotic Use

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

This information is current as of January 4, 2007

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Pharyngitis in Low-Resources Settings. a Pragmatic Clinical Approach to Reduce Unnecessary Antibi