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Over prescription of antibiotics for adult pharyngitis is prevalent in developing countries but can be… Palla, Amber H; Khan, Rafeeq A; Gilani, Anwar H; Marra, Fawziah Nov 24, 2012

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RESEARCH ARTICLE Open AccessOver prescription of antibiotics for adultpharyngitis is prevalent in developing countriesbut can be reduced using McIsaac modificationof Centor scores: a cross-sectional studyAmber Hanif Palla1,2, Rafeeq Alam Khan3, Anwar H Gilani2 and Fawziah Marra4*AbstractBackground: Although Group A beta hemolytic streptococcus (GABHS) can cause bacterial pharyngitis, the mostcommon etiology is viral; despite this viral etiology, antibiotics are commonly prescribed for this infection inindustrialized countries. We investigated the prevalence of GABHS in adult pharyngitis patients from lowersocioeconomic settings in Karachi, Pakistan, how often antibiotics are prescribed for pharyngitis and if appropriateagents were used in a developing world setting. Finally, we wanted to see the usefulness of modified McIsaacscores in predicting positive cultures.Methods: Adult patients were recruited from three local hospital outpatient dispensaries (OPDs). All patients aged14–65 years who were suspected of having bacterial pharyngitis had throat swabs taken. Laboratory results forGABHS pharyngitis were then compared with their prescriptions. Appropriateness (using the World HealthOrganization’s definition) and type of antibiotic prescribed were assessed.Results: Of 137 patients, 30 patients each were studied for scores of 0, 1, 2 and 3; 17 patients were studied forscore 4. Although 6 (4.4%) patients were GABHS+, for a prevalence of 43.8 per 1000 population, antibiotics wereprescribed to 135 patients (98.5%). Of these, only 11.1% received appropriate antibiotics while 88.9% receivedinappropriate antibiotics. Penicillins were prescribed most (34.1%), especially amoxicillin/clavulanate; followed bymacrolides (31.1%), especially the second-generation agents, and fluoroquinolones (14.8%). McIsaac scores werefound to be 100% sensitive and 68.7% specific, giving a positive predictive value (PPV) of 12.7% and a negativepredictive value (NPV) of 100%.Conclusions: Antibiotics were prescribed irrationally to adult pharyngitis patients, as most cultures were negativefor bacterial infection. McIsaac modification of Centor scores related directly to culture results. We would thereforehighly recommend its use to help family physicians make treatment decisions for adult pharyngitis patients.Keywords: Antibiotics, Pharyngitis, McIsaac-modified Centor score, Antibiotic prescribing, Pakistan* Correspondence: fawziah.marra@ubc.ca4Faculty of Pharmaceutical Sciences, University of British Columbia,Vancouver, CanadaFull list of author information is available at the end of the article© 2012 Palla et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the CreativeCommons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, andreproduction in any medium, provided the original work is properly cited.Palla et al. BMC Pulmonary Medicine 2012, 12:70http://www.biomedcentral.com/1471-2466/12/70BackgroundGroup A beta hemolytic Streptococcus (GABHS) is com-monly implicated in bacterial pharyngitis [1]. Startingtreatment with antibiotics for GABHS infection, withinthe first 24–48 hours of illness, when a bacterial cause ishighly suspected, has been found to decrease duration ofsymptoms, such as sore throat, fever and adenopathy byapproximately one day [2], and prevent complications ofGABHS pharyngitis, particularly rheumatic fever andrheumatic heart disease [3]. However, the majority ofpharyngitis cases in adults are of viral etiology [4]; only5–15% of cases suffer from bacterial pathogens that re-quire prompt antibiotic treatment [5,6].The World Health Organization (WHO) defines anappropriate prescription as “administration of the rightdrug indicated for the disease, in the right dose, throughan appropriate route of administration, for the right dur-ation” [7]. When these criteria are not fulfilled, the pre-scription is considered inappropriate. Inappropriateantibiotic prescriptions for treatment of pharyngitis havecontributed to the emergence of resistant strains of oro-pharyngeal human flora [8] which in turn, haveincreased morbidity, mortality, and health-care costs [9].Approximately three quarters of pharyngitis patientshave received inappropriate antibiotic prescriptions, byreceiving antibiotics for viral infections or otherwise notadhering to the WHO definition [10-12].First-line agents for treatment of bacterial pharyngitisinclude penicillin, ampicillin or amoxicillin.13 Alternativeoptions include erythromycin (especially in patients witha non-life-threatening allergy to penicillin) and first-generation cephalosporins (CG) [1]. Both erythromycinand cephalosporins are also considered reasonable alter-natives to penicillin in patients who fail to respond topenicillin or continue to become re-infected followingpenicillin therapy [13-15]. As GABHS is the most im-portant pathogen causing infection, fluoroquinolones,and sulfamethoxazole/trimethoprim that do not coverGram-positive pathogens very well are not recom-mended. Although amoxicillin-clavulanate, clarithromy-cin, azithromycin and second-generation cephalosporinswork very well against GABHS infection, they are con-sidered third-line alternatives due to their broaderspectrum of action and potential for causing resistance.Throat swab and culture is the gold standard for diag-nosis of pharyngitis. A rapid antigen detection test(RADT) can also give relatively specific diagnosis in aphysician’s office. Although a WHO technical reportstates that there is less possibility of false-positive resultswith RADT, RADT kits vary in sensitivity, which rangesfrom 31–95%. Therefore, RADT cannot be substitutedfor standard blood agar cultures [3]. Because antibioticstreatment should occur fairly promptly, diagnosis ofpharyngitis is often based on clinical symptoms; throatswabs are not always taken [16]. Thus to improve thediagnostic criteria, several scoring systems have beendeveloped to predict, on a clinical basis, whetherpatients have bacterial or viral pharyngitis [17,18].Among the many devised clinical scores, the Centorcriteria are reliable predictors of GABHS pharyngitis.They include evaluating patients for tonsillar exudates,tender anterior cervical lymphadenopathy or lymph-adenitis, absence of cough, and history of fever (oraltemperature greater than 38.3°C; 101°F) [19]. More re-cently, the Centor score was modified by incorporatingpatient's age, which allows the physician to placepatients in low-, moderate-, or high-risk groups. The useof the McIsaac Modified Centor score has helped in de-creasing inappropriate antibiotic use by almost 88% [18].Several guidelines have been published on diagnosisand treatment of streptococcal pharyngitis in adults;however, not all are in agreement. The American Collegeof Physicians’ (ACP) guideline endorsed by Centre forDisease Control (CDC), American Academy of FamilyPhysicians and the American Society of Internal Medi-cine, recommend that patients with low Centor scores of0 or 1 (i.e., low risk for streptococcal pharyngitis) do notrequire any testing or treatment with antibiotics. Forpatients with Centor scores of 2 or, 3, the guidelines sug-gest using a RADT, which would give a sensitivity of >80% for accurate diagnosis of GABHS infection, and pre-scribing antibiotics to patients with positive tests [20,21].Empirical treatment with antibiotics is recommendedfor patients with Centor scores of 3 or 4 [22]. However,practice guidelines issued by the American Heart Asso-ciation [23], American Academy of Pediatrics [24], andInfectious Diseases Society of America (IDSA) [25] rec-ommend microbiologic confirmation by throat cultureor RADT to diagnose all adults with pharyngitis priorto antibiotic prescribing, regardless of their Centorscores. IDSA and others are of the opinion that if pres-tigious organizations like AAFP and CDC endorse theoption of not culturing at all for any given score, itwould be unlikely that physicians would opt for eitherRADT or culture [26].These concerns were addressed by McIsaac whopointed out that missed infections are not due solely toscore approaches, as physicians do not obtain a throatswab for every case of sore throat [27]. Therefore, treat-ment decisions based on clinical judgment would alreadymiss 50% of GABHS infections, while 20–40% of the lar-ger number of non-GABHS sore throat presentationswould be identified as needing antibiotics [19,28].Given the controversy in clinical guidelines and notknowing how physicians in Pakistan generally treat theiradult pharyngitis patients, we investigated whether anti-biotics are prescribed appropriately for primary treat-ment of pharyngitis within a developing world settingPalla et al. BMC Pulmonary Medicine 2012, 12:70 Page 2 of 7http://www.biomedcentral.com/1471-2466/12/70and under low socio-economic conditions. We also eval-uated the sensitivity and specificity of McIsaac ModifiedCentor scores in predicting GABHS pharyngitis in ourpatient populations. Finally, we evaluated whether thechoice of antibiotic to treat pharyngitis was appropriate,in terms of antibiotic class, dose, and duration of ther-apy. Our study did not address use of antibiotics for sec-ondary prevention of pharyngitis or asymptomaticcarrier state.MethodsStudy settingThe study was conducted in three tertiary care hospitals—the Jamal Noor hospital, Zubaida Medical Centre andthe Civil Hospital, within two different areas of Karachi(Dhoraji and Bander Road) where outpatient dispensar-ies (OPD) were available. The clinical ethics committeesof all three hospitals gave their approval. Before startingthe study, educational sessions were set up at the clinicsto describe the study and consent process to clinicnurses and physicians. Informed consent was obtainedfrom all study participants by the clinic physician.Patient recruitmentAll patients between the ages of 14 and 65 years of age,suspected of having bacterial pharyngitis were asked toparticipate in the study between March and October2005. Patients who were younger than 14 years, im-munocompromised (i.e., had autoimmune diseases in-cluding HIV/AIDS or were on immunosuppressiveagents), or had been on antibiotics 24–48 hours beforewere not included in the study.Patients who agreed to participate were categorizedaccording to the McIsaac Modified Centor System intoscores 0, 1, 2, 3 and 4 [27]. One point was assigned toeach of the following symptoms: tonsillar exudates, ten-der anterior cervical lymphadenopathy or lymphadenitis,absence of cough, and history of fever (oral temperaturegreater than 38.3°C; 101°F), and one point was deductedif the patient was older than 45 years.MicrobiologyA throat swab was collected by the clinic physician usinga sterile swab from the posterior pharynx, tonsils and/orinflamed areas. These swabs were transported to themicrobiological laboratory facility of Zubaida MedicalCenter, which is an ISO 2001 certified laboratory andfollows the Monica Cheesbrough “District laboratorypractice in tropical countries” guidelines [29] for speci-men testing, and the Clinical and Laboratory StandardsInstitute (CLSI) guidelines [30] to perform the cultures.Each specimen was cultured on a sheep blood agarplate and a chocolate agar plate in anaerobic environ-ment at 35°–37°C for 18–24 hours before reading forGABHS, and then in CO2 rich atmosphere 35°C for 24hours. A colony grown on blood agar plate and chocolateagar was taken, and streaked on the nutrient agar plate.A bacitracin disc, and penicillin, ampicillin, amoxicillin,amoxicillin-clavulanate, cephradine, clarithromycin anderythromycin, were then placed on the plate and wereincubated for 24 hours. Based on zones of inhibition,they were graded as sensitive, intermediate or resistant.Testing methodology was same for all patients.DefinitionsInappropriate treatment was defined as per the WHO,which suggests that administration of the right drugindicated for the disease, in the right dose, through anappropriate route of administration, for the right dur-ation [6]. Thus, both infected (GABHS+) patients whodid not receive antibiotics, and uninfected (GABHS–)patients who did receive antibiotic prescriptions wereconsidered to receive inappropriate treatment.A second aspect of appropriate antibiotic prescriptionwas whether the choice of antibiotic for GABHS+ pha-ryngitis was from a recommended class, in the rightdose and for the right duration. When evaluating a phy-sician’s choice of antibiotics, we assumed that allpatients who received antibiotics were infected; prescrip-tions were then considered appropriate if they pre-scribed an accurate dose and duration of first-line agentsor second-line alternative agents. Prescriptions wereconsidered inappropriate if patients received inappropri-ate doses or duration of first- or second-line agents, orthird- line agents or antibiotics that are not recom-mended for pharyngitis infection.First-line antibiotics included penicillin (oral penicillinV 500 mg every 8 hours for 10 days; benzyl penicillin0.6–1.2 million units IM once; oral ampicillin 500 mgevery 6 hours for 10 days; oral amoxicillin 500 mg every8 hours for 10 days) [20]. Appropriate alternativesecond-line agents included cephalexin (500 mg every12 hours for 10 days) and other first-generation cepha-losporins, cefaclor (500 mg every 8 hours orally for10 days), a second-generation cephalosporin [31] anderythromycin for penicillin-allergic patients (250 mg p.o.every 6 hours or 500 mg every 12 or 6 hours for 10 days).Third-line agents were considered inappropriate, becausethey are too broad-spectrum, or do not have adequateactivity. Broad-spectrum agents included amoxicillin-clavulanate (500–875 mg orally every 12 hours for10 days), second-generation macrolides such as clarithro-mycin (250 mg orally every 12 hours for 5 days), azithro-mycin (500 mg orally on day 1; 250 mg on days 2–5 for5 days) and roxithromycin (150 mg orally every 12 hoursor 300 mg once daily for 10 days), broader-spectrum sec-ond-generation cephalosporins like cefuroxime (250 mgor 500 mg every 12 hours for 5–10 days) and third-Palla et al. BMC Pulmonary Medicine 2012, 12:70 Page 3 of 7http://www.biomedcentral.com/1471-2466/12/70generation cephalosporins like cefixime (400 mg orallydaily for 5 days). Use of erythromycin for non-penicillinallergic patients was also considered inappropriate. Fi-nally, antibiotics not recommended for Gram-negativepathogens were also considered to be inappropriateor third-line agents; these included fluoroquinolones(e.g., ciprofloxacin, levofloxacin and ofloxacin); sulfona-mides such as sulfamethoxazole/trimethoprim and tetra-cyclines (e.g., doxycycline, minocycline, tetracycline, andoxytetracycline).Study outcomes and statisticsThe primary outcome was the prevalence of GABHS in-fection in the adult pharyngitis patients from a lowsocioeconomic setting. Secondary outcomes included 1)number of prescriptions used for adult pharyngitis; 2)appropriateness of prescribed antibiotics; and 3) diag-nostic accuracy of the Modified Centor criteria.By comparing patients’ culture results, we could deter-mine the prevalence of infection. To determine whetherpatients received appropriate or inappropriate prescrip-tions, culture results were compared with antibiotic pre-scriptions. Sensitivity, specificity, positive predictive andnegative predictive value of the McIsaac score approachwas determined by ratios of false positives, true posi-tives, false negatives and true negatives.ResultsTable 1 shows the demographics of the study population.Of the 137 patients, the average age of the study popula-tion was 26 years old while the median age was 23 years.There were more males than females who presentedwith symptoms of pharyngitis (66% male vs 34%females). Thirty patients each with scores 0, 1, 2 and 3,and 17 patients with score 4 were evaluated for bacterialpharyngitis (N= 137); of these patients, only 6 wereGABHS+ but 135 were treated with antibiotics. Thus,the prevalence of bacterial pharyngitis in our populationwas 43.8 per 1000 population. Penicillin was the mostfrequently prescribed antibiotic class (34.1%). Withinthis class, the majority of prescriptions were foramoxicillin-clavulanate (26.6%), a broad-spectrum peni-cillin. Approximately 15% of the prescriptions were forcephalosporins (14.8%), with the third-generation cepha-losporins accounting for 9.6% of the usage, second-generation cephalosporins accounting for 3.7%, andfirst-generation cephalosporins accounting for 1.4% oftotal antibiotic usage. Macrolides (31.1%), quinolones(14.8%), sulfonamide (3.0%), tetracyclines (2.2%) werealso prescribed for patients.Antibiotics were prescribed inappropriately to adultpharyngitis patients; we saw no association between anti-biotic use and culture confirmation results (P = 0.75).When cross tabulated, of the patients who were givenantibiotics, only 4% patients were GABHS+; 96% ofpatients were GABHS– (Table 2).A total of 135 patients received antibiotics, but only15/135 (11.1%) received appropriate antibiotics; 120/135 (88.9%) who received inappropriate antibiotics, notrecommended by current guidelines. Table 3 shows thebreakdown of the antibiotics received by the patients.Only 8/135 (5.8%) of the patients received first-lineagents for treatment of pharyngitis; most patientsreceived second-line agents (7/135; 5.2%) and third-lineagents (120/135; 88.9%). Of the inappropriate antibio-tics prescribed, macrolides (42/135; 31.1%) were pre-scribed most, including erythromycin for non-penicillinallergic patients, clarithromycin and roxithromycin;followed by broad-spectrum penicillin; amoxicillin-clavulanate (36/135; 26.7%), the third-generation ceph-alosporin cefixime (13/135; 9.6%) and fluoroquinolones(20/135; 14.8%).Antibiotics were prescribed by brand names to 96.2%of patients. Irrespective of which class of antibiotic wasprescribed, only 45% (61/135) of patients were pre-scribed antibiotics at appropriate doses and durations,whereas 55% (74/135) received prescriptions for in-appropriate doses and/or durations.Table 4 shows an even distribution of patients in eachof the 4 score groups (30 in each group), except forgroup 4 (17 patients). The McIsaac score system wasfound to be 100% sensitive and 68.7% specific, giving aTable 1 Patient demographicsVariables N (%)Total number of patients in study 137Males, N (%) 91 (66.4%)Females, N (%) 46 (33.5%)Mean age ± SD 26 ± 10.71Median age ± SD 23 ± 10.71Antibiotics prescribed by physiciansPenicillin 46 (34.1%)Macrolides 42 (31.1%)Cephalosporins 20 (14.8%)Quinolones 20 (14.8%)Sulfonamide/Trimethoprim 4 (3.0%)Tetracyclines 3 (2.2%)Table 2 Appropriateness of antibiotic prescribing whencompared to culture resultsCulture fromthroat swabAntibiotic prescribed TotalYes NoPositive, N (%) 6 0 6 (4.4%)Negative, N (%) 129 2 131 (95.6%)Total, N (%) 135 2 137 (100%)Palla et al. BMC Pulmonary Medicine 2012, 12:70 Page 4 of 7http://www.biomedcentral.com/1471-2466/12/70positive predictive value (PPV) of 12.7% and a negativepredictive value (NPV) of 100%.DiscussionThis is the first study to look at appropriate antibioticuse for adult pharyngitis in a developing world setting.Our study showed that much antibiotic use isunnecessary for patients who have pharyngitis—probablybecause most such patients have viral, rather than bac-terial, infections. In fact, only 4.3% of the patients in oursample were found to be GABHS+; the rest were likelyviral infections.Furthermore, even when antibiotics are used, physi-cians are prescribing broader class agents for treatment,Table 3 Antibiotics prescribed by physicians for adult pharyngitis patientsAPPROPRIATE ANTIBIOTICSClass Name Numbers (%)Appropriate first-line agentsPenicillin Ampicillin 3 (2.2%)Amoxicillin 5 (3.7%)Total 8 (5.8%)Appropriate alternative second-line agentsFirst-generation cephalosporins Cefadroxil 1 (0.7%)Cephradine 1 (0.7%)Second-generation cephalosporins Cefaclor 5 (3.7%)Total 7 (5.2%)NON-RECOMMENDED ANTIBIOTICSInappropriate or third-line agentsBroad spectrum penicillins Amoxicillin-Clavulanate 36 (26.7%)Ampicillin-Cloxacillin 2 (1.5%)Macrolides Erythromycin for patients not reported with penicillin allergy 14 (10.5%)Clarithromycin 27 (20.0%)Roxithromycin 1 (0.7%)Third-generation cephalosporins Cefixime 13 (9.6%)Quinolones Ciprofloxacin 2 (1.5%)Levofloxacin 18 (13.3%)Sulfonamides Sulfamethoxazole/trimethoprim 4 (3.0%)Tetracyclines Oxytetracycline 3 (2.2)Total 120 (88.9%)Table 4 Cross tabulation of McIsaac modification of Centor score and cultureMcIsaac modification of Centor score Culture positivity (N = 137) Total TN3 TP3 FP3Score 0 0 (0%) 30 (100%) 30 30 – 0Score 1 0 (0%) 30 (100%) 30 30 – 0Score 2 0 (0%) 30 (100%) 30 30 – 0Score 3 1 (3.4%) 29 (96.6%) 30 0 1 29Score 4 5 (29.4%) 12 (70.6%) 17 0 5 12Sensitivity4 100% (95% CI: 0.5–1)Specificity4 68.7% (95% CI: 0.54–0.7)PPV3,1 12.7% (95% CI: 0.05–0.26)NPV3,2 100% (95% CI: 0.9–1)1 Yes = Number of patients GABHS+ in culture / Total number of patients with respective score.2 No = Number of patients not found GABHS+ in culture.3 TN = True negative; TP = True positive; FP = False positive; PPV = positive predictive value; NPV = negative predictive value.4 Sensitivity and specificity of scores 0 to 4.Palla et al. BMC Pulmonary Medicine 2012, 12:70 Page 5 of 7http://www.biomedcentral.com/1471-2466/12/70such as amoxicillin/clavulanate or macrolides, ratherthan using the simple narrow-spectrum agents such aspenicillin or amoxicillin/ampicillin; even when the anti-biotic choice was appropriate, doses and durations ofthose antibiotics mostly were not. Although benzathinepenicillin is recommended by the WHO, we did not seeits usage in our study. Our investigation did not interro-gate physicians’ motives; however, we speculate that theypreferred the ease and lower cost of oral antibiotics tobenzathine penicillin, which costs more and requiresintramuscular injection.Although our findings are similar to those of otherstudies conducted in western countries, the enormity ofthe problem seems to be much larger in Pakistan due tothe large numbers of patients seeking medical attentionfor pharyngitis [32,33]. Many factors could have contrib-uted to inappropriate prescribing of antibiotics for pha-ryngitis. Quality of health care is constrained by costs indeveloping countries like Pakistan. Therefore, for a com-mon ailment like sore throat, a costly throat swab andculture is not a routine practice. Furthermore, RADT isnot an option in our setting because of its unavailabilityand high cost. Finally, patients generally expect to getthe maximum benefit from a physician visit so that theydo not have to pay the cost of the next visit. As a result,physicians are burdened with patients’ expectation ofproviding all care during the patient’s first and only visit.The results of our study would be generalizable to otherlow income countries such as India, Afghanistan andBangladesh.Our study showed that it would be useful for cliniciansin Pakistan to use the McIsaac Modified Centor score asit is not costly, and is sensitive and specific enough toreduce unnecessary antibiotic prescriptions. Based onour study, we recommend that the score-only approachwould save antibiotics prescriptions for most patients, asmost adult patients with pharyngitis had scores of 0, 1or 2. Although without a RADT test option, more anti-biotics would be prescribed for patients with a score of 3or 4, this percentage is better than the percentage ofpatients getting inappropriate antibiotics without clinicalscore-based screening at all. This modified Centor clin-ical prediction rule holds more importance in our set-ting because RADT is not widely available in ourcountry; given their high cost and varied sensitivity(31–95%) of the different RADT kits, their use will belimited [3]. During the course of our study, we sawthat affordability of RADT testing was the major con-cern in this setting, which resulted in almost 99% ofpatients being prescribed antibiotics. Following a scoreapproach would significantly reduce unnecessary anti-biotics prescriptions.Our study implies that, as with developed countries,clinicians in low socioeconomic countries need furthereducation on appropriate antibiotics to use for GABHSinfection, particularly the proper dose and duration ofthose antibiotics and possible repercussions of inappro-priately prescribed antibiotics. Education shouldemphasize the higher prevalence of viral etiology, use ofthe McIsaac modified Centor scoring system, and pub-lished guidelines on treatment of pharyngitis [8,14]. Thisis particularly important as India and Pakistan have beenfound to be among the initial sites of extremely resistantorganisms such as Escherichia coli and Klebsiella pneu-monia with the carbapenem-resistance gene blaNDM-1,[34] which may have resulted from uncontrolled andexcessive use of antibiotics in these countries. Inappro-priate use of antibiotics in developing regions has conse-quences for everyone; microbes have no country.Sensitivity to this issue needs to be renewed by creatingawareness that should be well supported by data.This study has several limitations. This patient samplewas very small with representation of few selected set-tings where the influx of patients is from lower- andmiddle-class families. A larger sample with patients fromdifferent areas of Karachi in future studies would offerbetter-supported conclusions about city-wide prescribingpractices, and about the prevalence of GABHS infectionin adults. The McIsaac–Centor score has been validatedfor use in industrialized countries, where prevalence ofrheumatic heart disease is < 1 per 1000 population, com-pared to >10 per 1000 in Pakistan /Asia [35]. Thus,using the McIsaac modified score as a routine clinicaltool may also mean that more cases of rheumatic feverare being prevented, given the higher prevalence ofrheumatic fever in Pakistan compared to the industria-lized nations.ConclusionsIn Pakistan, antibiotics are prescribed for most cases ofadult pharyngitis when in fact, the majority of the cul-tures are negative for bacterial infection. Furthermore, itwas alarming for us to discover the high use of secondgeneration macrolides and cephalosporins rather thanthe recommended narrower spectrum agents. McIsaacmodification of Centor score directly related to cultureresults. We therefore highly recommend its use to helpfamily physicians evaluate appropriate use of antibiotics.Competing interestsThe authors declare that they have no competing interests.Authors’ contributionsMs. AHP designed the study, obtained ethics approval, collected andanalyzed the data, created initial manuscript draft and subsequent revisions.Dr. FM assisted with statistical analysis, helped with the initial manuscriptdraft and revised all subsequent drafts. Drs RAK and AHG commented onstudy design and all manuscript drafts. All authors read and approved thefinal manuscript.Palla et al. BMC Pulmonary Medicine 2012, 12:70 Page 6 of 7http://www.biomedcentral.com/1471-2466/12/70AcknowledgementsWe thank Dr. Ashraf Ibrahim, Dr. Shahab Abid, Dr. Saleem Marfani, Dr. Aafia,Dr. Afshan, Dr. Uzma, Dr. Nisar Rao and Mr. Hanif Palla for providing thefacilities to gather the data. We also thank Dr. Afia Zafar for her input indesigning the data collection form.Author details1Department of Pharmacology, University of Karachi, Karachi, Pakistan.2Department of Biological and Biomedical Sciences, Aga Khan UniversityMedical College, Karachi, Pakistan. 3Department of Basic Medical Sciences,College of Medicine, King Saud bin Abdul-Aziz University for Health Sciences,King Abdul-Aziz Medical City, Jeddah 21423, KSA. 4Faculty of PharmaceuticalSciences, University of British Columbia, Vancouver, Canada.Received: 17 May 2012 Accepted: 26 October 2012Published: 24 November 2012References1. Bertrand E, Gerard R: Comparison of hospital prevalence of rheumaticheart diseases and acute rheumatic arthritis in France and Africa. ArchMal Coeur Vaiss 1993, 86:291–295.2. Krober MS, Bass JW, Michels GN: Streptococcal pharyngitis: placebo-controlled double-blind evaluation of clinical response to penicillintherapy. JAMA 1985, 253:12714.3. 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National Committee for Clinical Laboratory Standards: Performancestandards for antimicrobial susceptibility testing, 14th informationalsupplement M100-S14. Wayne: PA:NCCLS; 2004.31. Hayes CS, Williamson H: Management of Group A Beta-HemolyticStreptococcal Pharyngitis. Am Fam Physician 2001, 63:1557–1565.32. Aalbers J, Brien K, Chan WS, et al: Predicting streptococcal pharyngitis inadults in primary care: a systematic review of the diagnostic accuracy ofsymptoms and signs and validation of the Centor score. BMC Medicine2011, 9:67.33. Gill JM, Fleishchut P, Haas S, et al: Infections in Outpatient Settings:A National Ambulatory Network Study. Fam Med 2006, 38:349–54.33.34. Kumarasamy KK, Toleman MA, Walsh TR, et al: Emergence of a newantibiotic resistance mechanism in India, Pakistan, and the UK:a molecular, biological, and epidemiological study. Lancet Infect Dis 2010,10:597–602.35. Seckeler MD, Hoke TR: The worldwide epidemiology of acute rheumaticfever and rheumatic heart disease. Clin Epidemiol 2011, 3:67–84.doi:10.1186/1471-2466-12-70Cite this article as: Palla et al.: Over prescription of antibiotics for adultpharyngitis is prevalent in developing countries but can be reducedusing McIsaac modification of Centor scores: a cross-sectional study.BMC Pulmonary Medicine 2012 12:70.Submit your next manuscript to BioMed Centraland take full advantage of: • Convenient online submission• Thorough peer review• No space constraints or color figure charges• Immediate publication on acceptance• Inclusion in PubMed, CAS, Scopus and Google Scholar• Research which is freely available for redistributionSubmit your manuscript at www.biomedcentral.com/submitPalla et al. BMC Pulmonary Medicine 2012, 12:70 Page 7 of 7http://www.biomedcentral.com/1471-2466/12/70

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