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

    This information is current as of January 4, 2007

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    rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.Grove Village, Illinois, 60007. Copyright 2006 by the American Academy of Pediatrics. Alland trademarked by the American Academy of Pediatrics, 141 Northwest Point Boulevard, Elkpublication, it has been published continuously since 1948. PEDIATRICS is owned, published,PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly

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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

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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

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