Clin Infect DisClin. Infect. DiscidcidClinical Infectious Diseases: An Official Publication of the Infectious Diseases Society of America1058-48381537-6591Oxford University Press22403223369349510.1093/cid/cir1053Supplement ArticlesA Literature Review and Survey of Childhood Pneumonia Etiology Studies: 2000–2010GilaniZunera1KwongYuenting D.2LevineOrin S.3Deloria-KnollMaria3ScottJ. Anthony G.45O’BrienKatherine L.3FeikinDaniel R.36Department of Epidemiology, Bloomberg School of Public HealthSchool of MedicineDepartment of International Health, International Vaccine Access Center, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MarylandKEMRI–Wellcome Trust Research Programme, Kilifi, KenyaNuffield Department of Clinical Medicine, University of Oxford, United KingdomDivision of Preparedness and Emerging Infections, National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GeorgiaCorrespondence: Zunera Gilani, MPH, International Vaccine Access Center, Johns Hopkins Bloomberg School of Public Health, 855 No. Wolfe St, Ste 600, Rangos Bldg, Baltimore, MD 21205 (zgilani@jhsph.edu).0142012014201254Suppl 2Pneumonia Etiology Research for Child HealthS102S108209201120122011© The Author 2012. Published by Oxford University Press on behalf of the Infectious Diseases Society of America.2012This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (http://creativecommons.org/licenses/by-nc-nd/3.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work properly cited. For commercial re-use, please contact journals.permissions@oup.com.

The Pneumonia Etiology Research for Child Health (PERCH) project is the largest multicountry etiology study of childhood pneumonia since the Board on Science and Technology in International Development studies of the 1980s. However, it is not the only recent or ongoing pneumonia etiology study, and even with seven sites, it cannot capture all epidemiologic settings in the developing world. Funding providers, researchers and policymakers rely on the best available evidence to strategically plan programs, new research directions and interventions. We aimed to describe the current landscape of recent pneumonia etiology studies in children under 5 years of age in the developed and developing world, as ascertained by a literature review of relevant studies with data since the year 2000 and a survey of researchers in the field of childhood pneumonia. We collected information on the study population, study design, case definitions, laboratory samples and methods and identified pathogens. A literature review identified 88 studies with child pneumonia etiology results. As of June 2010, our survey of researchers identified an additional 65 ongoing and recently completed child pneumonia etiology studies. This demonstrates the broad existing context into which the PERCH study must be placed. However, the landscape analysis also reveals a multiplicity of case definitions, levels of clinician involvement, facility types, specimen collection, and laboratory techniques. It reinforces the need for the standardization of methods and analyses for present and future pneumonia etiology studies in order to optimize their cumulative potential to accurately describe the microbial causes of childhood pneumonia.

Each year, approximately 1.6 million children die from pneumonia [1]. The Pneumonia Etiology Research for Child Health (PERCH) study is the largest multisite study of childhood pneumonia since the Board of Science and Technology for International Development (BOSTID) studies were done in the 1980s [2]. The goal of PERCH is to identify the expected etiologies of pneumonia in 2015, a time when the burden of the major causes of bacterial pneumonia in the developing world, Streptococcus pneumoniae and Haemophilus influenzae type b (Hib), will likely be significantly reduced by widespread introduction and use of conjugate vaccines. Moreover, PERCH capitalizes upon new molecular diagnostic techniques that were not available 2 decades ago when the BOSTID studies were carried out. Another salient difference between PERCH and the BOSTID studies is that the 7 sites participating in PERCH will follow a highly standardized protocol, which includes standardization of enrollment criteria, specimen collection, and laboratory testing.

Although PERCH is the largest multicountry, childhood pneumonia etiology study in developing countries that has been conducted in the past 2 decades, it is not the only contemporary pneumonia etiology study, and cannot capture the entire complexity of all epidemiologic settings. In recent years, many developed and developing country sites have initiated pneumonia studies that provide etiology data. These studies will provide useful complementary data to the PERCH study that will more fully define and characterize the causes of childhood pneumonia throughout the world. Yet, because the clinical, laboratory and statistical analysis approaches of these studies vary significantly, collating the results of multiple etiology studies will likely prove challenging. Differences in observed etiology can arise not only from epidemiologic differences in the sites and populations studied, which are biologic and epidemiologic attributes relevant to public health decision making, but also from variability in study design. Consideration of how study design can affect the results of etiologic studies is crucial to interpreting such studies in the context of PERCH.

In this paper, we describe the global landscape of sites that are currently studying pneumonia etiology or have recently studied it in the developed and developing world as ascertained by a literature review of studies with data since the year 2000 and a survey of pneumonia researchers. We did not aim to conduct a systematic review of the literature or a meta-analysis of study results. Furthermore, we did not undertake a critical evaluation of the methods or results from the studies we identified. The purpose of this project is limited to a landscape analysis to better describe the breadth of available data on child pneumonia etiology.

METHODSLiterature Review

We conducted a literature review to identify studies with pneumonia etiology data. All searches were conducted in June 2010 using the PubMed database and entering search terms that were key words, MeSH terms, synonyms or truncations. Eight separate search strategies were conducted. Titles and abstracts were screened to identify potential studies with pneumonia etiology data in children under five years old. Eligible studies were abstracted by two trained abstractors (ZG, YDK). Information abstracted included study population, study design, case definitions, body fluid samples, laboratory methods and identified pathogens. The studies were grouped by category, and summary statistics were described using Stata version 10 (College Station, TX); no statistical testing was undertaken on the data.

The inclusion criteria for studies were as follows:

Study of acute community-acquired pneumonia or acute lower respiratory tract infection (ALRI).

Consistent testing for at least one specific etiology in enrolled patients.

Enrollment of children <5 years old (can also include older persons).

Published between June 2005 and June 2010.

Data collection from the year 2000 onwards.

≥10 pneumonia/ALRI cases.

≥1 calendar year of surveillance.

English language.

The exclusion criteria were as follows:

Exclusive enrollment of bronchiolitis patients.

Exclusive enrollment of patients with a specific complication or sequelae of pneumonia (eg, empyema or parapneumonic effusions).

Inability to distinguish the etiology of pneumonia cases from other syndromes (eg, pneumonia cases within a study of invasive pneumococcal disease).

Etiology inferred from the upper airway carriage alone.

Focus only on antibiotic resistance among pneumococcal isolates.

Exclusive enrollment of hospital-acquired pneumonia patients.

Our aim was to identify sites and studies, not publications. When more than one publication was identified from the same study, we designated the publication with the most comprehensive etiology results or methodology details, longest surveillance period, or the oldest reference, as the “main publication.” Results from additional publications supplemented data when possible. When publications referred to a particular surveillance network that included sites in multiple countries, we included a result for the entire surveillance network and individual results for each country if they were published separately.

When studies encompassed other disease syndromes other than pneumonia, such as meningitis and sepsis, we limited results to pneumonia-specific information when possible. Clinical trials were only included if they described methods for etiological diagnoses.

Survey of Pneumonia Researchers

A Web-based survey of researchers who may have conducted pneumonia etiology research was created to capture information regarding unpublished ongoing and recently completed pneumonia etiology studies among children less than five years old (Survey Monkey, Palo Alto, California). This survey was circulated by email on 12 April 2010 to approximately 5000 pneumonia community members that belonged to the email address list of PneumoFOCUS [3], a monthly bulletin providing news about pneumonia, pneumococcal disease, and pneumococcal vaccines that is written and produced by our team at Johns Hopkins School of Public Health. We also contacted researchers who had submitted letters of intent in response to the PERCH Request for Proposals (RFP) for sites, researchers at sites selected to be part of the PERCH study, other known pneumonia surveillance researchers (eg, US Centers for Disease Control and Prevention’s International Emerging Infection Program sites) and researchers identified through word of mouth. We individually contacted researchers to clarify and confirm certain responses. We followed up by email with known pneumonia researchers if they did not respond to our initial survey request.

The survey included questions about the study population, study design, case definitions, body fluid samples, laboratory methods, and identified pathogens. Separate surveys were filled out for each study if more than one study took place in a given geographic site. The studies were grouped by category and summary statistics were described; no statistical testing was undertaken on the data.

RESULTSLiterature Review

Of 2511 titles and abstracts reviewed, 2311 were excluded because they did not meet eligibility criteria. The full text of 200 publications was reviewed, and 88 studies with child pneumonia etiology results were included [410] [1118] [1925] [2630] [3138] [3943] [4451] [5261] [6271] [7280] [8191]. Studies ranged in size from 10 to 21 239 pneumonia patients (median 260 patients). We identified studies in 52 countries (Supplementary Figure 1). Multiple studies were done in 26 countries. Of these, 8 studies were identified in the United States; 7 in each of Bangladesh and India; 6 in Thailand; 5 in South Africa; 4 in each of Brazil, Philippines and Taiwan; 3 in each of China, Hong Kong, Kenya, Korea, Japan, Nepal, Nigeria, and Vietnam; and 2 in each of Argentina, Ethiopia, Finland, Guatemala, Italy, Mexico, Mozambique, Pakistan, Yemen and Zambia. Three studies (3%) in 5 countries (Brazil, Costa Rica, El Salvador, United States and Zambia) reported collecting postmortem specimens [29, 31, 69], and 5 (6%) in 10 counties (Bangladesh, Ecuador, the Gambia, India, Malawi, Mexico, Nigeria, Pakistan, South Africa and Yemen) reported collecting lung aspirates [11, 26, 35, 51, 63]. Seven studies used asymptomatic controls [6, 17, 19, 30, 79, 83, 89]. Additional study characteristics are summarized in Supplementary Table 1.

Survey

We received 81 responses to the survey. A total of 65 studies were identified once we removed responses that did not meet our study criteria. Of the 16 studies excluded from analysis, the reasons for exclusion were the following: the study was not a pneumonia etiology study, the study did not include children less than five years of age or multiple responses were received describing the same study. Studies ranged in size from 12 to 27 778 pneumonia patients (median 780 patients). Among the 65 pneumonia etiology studies, 41 countries were represented (Supplementary Figure 1). There were 16 countries that reported multiple studies. Of these, 6 studies were being conducted in Bangladesh; 5 in each of Brazil, India and Nepal; 4 in Indonesia; 3 in each of Kenya, Mozambique, South Africa, the United States, Australia, Thailand and Spain; and 2 in each of Jordan, Guatemala, China and Israel. Two studies reported that they obtained approval to collect postmortem specimens in their protocols, but neither site had collected any postmortem specimens as of March 2011. Additional study characteristics are reported in Supplementary Table 1.

DISCUSSION

The results of the literature review and survey reveal that many child pneumonia etiology studies have been and are taking place throughout the world since the year 2000, which enable an understanding of PERCH data in the context of a global landscape of ongoing pneumonia research. The large quantity and great depth of the available data highlight the challenges in interpreting various pneumonia etiology studies, particularly when comparing or combining results. Different studies employ different case definitions, levels of clinician involvement, facility types, specimens collected and laboratory tests. The use of a common protocol in a multisite study with broad geographic and epidemiologic representation will enable inferences to be drawn about the similarities and differences from other studies.

Our landscape analysis identified several gaps in the availability of data regarding childhood pneumonia etiology. First, there were few studies identified in Latin America (outside of Brazil, Chile and Argentina), in west and particularly central Africa, and in the Middle East. No studies were identified from Russia or China. This gap may be due in part to our English language inclusion criterion. It is important to have data from places where child pneumonia mortality is the highest [92]. South Asia and parts of Africa, which are regions of the world with the greatest burden of childhood pneumonia deaths, are well-represented in pneumonia etiology studies. Nonetheless, the 5 countries with the highest burden of child pneumonia deaths—India, Nigeria, Pakistan, the Democratic Republic of Congo (DRC) and Afghanistan [1]—are not proportionally represented in our literature review. Our literature review identified only 7 studies conducted in India, 3 in Nigeria, 2 in Pakistan and none in the DRC or Afghanistan. Second, there needs to be more pneumonia etiology studies in countries that have or are currently introducing both the Hib and pneumococcal conjugate vaccines. Such studies will help define the new distribution of pneumonia-causing etiologies in these settings, which will likely have important implications for diagnosis and empiric treatment algorithms. Third, there are few studies that report postmortem results. It is important to understand the spectrum of etiologies for the most severe cases of pneumonia, which will be critical in reducing the still high burden of childhood pneumonia mortality in the world [93]. Although technically and culturally challenging, postmortem studies reveal a different and complementary picture of etiology that is otherwise underestimated or forgotten. This applies particularly to tuberculosis, HIV-associated conditions (eg, lymphocytic interstitial pneumonia, Pneumocystis jiroveci (carinii) pneumonia and cytomegalovirus disease), and to other pathogenic processes that produce a clinical syndrome that mimics pneumonia (eg, severe anemia with heart failure or interstitial lung disease).

Variation in the methods employed by different pneumonia etiology studies can lead to differences in the identified etiologies. For example, the case definition used can influence the distribution of microbial etiologies. Case definitions based on radiologic (eg, alveolar consolidation) and laboratory definitions (eg, left-shift of polymorphonuclear neutrophils) are likely to identify more bacterial than viral pneumonia cases. Alternatively, a simple clinical case definition based on tachypnea (eg, nonsevere pneumonia defined by the Integrated Management of Childhood Illness) or a definition that included wheeze might lead to the identification of relatively more viral infections. Given the association between clinical severity and etiology, the target population and facility type can also determine the spectrum of etiologies. Thus, studies in community-based settings, health centers or outpatient wards may find different ranges of etiologies than studies in referral hospitals. Age is an influential variable and studies that exclude older children and focus on infants are likely to identify more RSV infection, which predominates in infancy. Neonates, in particular, have a distinct set of pneumonia pathogens [92, 94].

Other factors that varied across studies were the type of body fluid specimens collected and the type of laboratory testing done. Detection of bacterial pneumonia is dependent to a large extent on blood culture. While a majority of studies performed blood culture, it is likely that there was considerable variation in the sensitivity of the tests, particularly for Streptococcus pneumoniae, which is a fastidious organism requiring optimal collection and laboratory conditions. There are other factors that may result in an over-representation of viral causes of pneumonia. It was notable that the use of PCR as a diagnostic tool was higher in the studies reported on the survey (68%) than in those already published in the literature (46%). As molecular diagnostics become more widely used, it will be important to disaggregate temporal trends in the epidemiology of viral pneumonia from trends in laboratory practice. The findings of PCR testing of nasopharyngeal and oropharyngeal swabs will need to be interpreted judiciously. The presence of viral nucleic acids in the pharynx does not necessarily mean that the virus is acutely causing pneumonia in the lungs [79, 95]. As PCR use increases, strategies must be used to help interpret these findings. One such strategy is to include control children (ie, those without pneumonia) in whom similar body fluids are collected and tested, which will allow for improved ability to interpret the PCR results [95].

Our landscape analysis had several limitations. In spite of employing multiple search strategies, we likely missed identifying some studies. Of note, we only searched the English language literature and only utilized one literature database (PubMed). This likely biased our findings by excluding studies from certain geographic regions such as China, Spanish-speaking Latin America, Russia and the Middle East where there may be a substantial body of evidence in local language publications. We did not search Embase and thus did not include conference abstracts unless researchers directed us to specific abstracts. Second, some published studies lacked sufficient detail to provide information on particular aspects of the study design that were of interest. Notable missing data were case definitions, facility types, and eligibility determination. Our survey likely suffered from similar limitations as far as incompleteness of data that was provided for some studies. Similarly, we only reached out to researchers who were already identified in the field, which might have led to gaps in those contacted. Third, not all identified studies were intended to be pneumonia etiology studies. Several had other primary objectives, such as to study invasive pneumococcal disease or influenzalike illness, and in that process identified children with pneumonia. As such, these studies are by design not comparable to studies that identify multiple pneumonia pathogens in that their case definitions and patient mix would likely differ. Finally, we were unable to verify survey responses.

In conclusion, the review of the literature and the survey of studies illustrate the context within which the PERCH study will be interpreted. Pneumonia etiologies are likely to continue to evolve as more countries introduce Hib and pneumococcal conjugate vaccines. Vaccines for other major causes of childhood pneumonia such as influenza will likely become more widely used across the globe or may be successfully developed (eg, RSV) over the next decade, and therefore, will further influence the pneumonia burden and remaining etiologies. Improvement in global socioeconomic conditions will also influence the pneumonia etiologic spectrum in the future. One of the goals of PERCH is to create a reference standard for the design, conduct and analysis of pneumonia etiology studies. This will provide a framework within which valid between-site comparisons can be drawn and integrated models can be extended geographically. PERCH will also contribute to a refinement of the case definition of pneumonia and provide evidence for the utility of certain body fluid specimens and laboratory tests. We hope that the definition of a standard, and the publication of the validation processes that were undertaken to create that standard, will encourage investigators to analyze existing studies and design future studies with reference to this standard in order to optimize the epidemiological value of the results.

Supplementary Data

Supplementary materials are available at Clinical Infectious Diseases online (http://www.oxfordjournals.org/our_journals/cid/). Supplementary materials consist of data provided by the authors that are published to benefit the reader. The posted materials are not copyedited. The contents of all supplementary data are the sole responsibility of the authors. Questions or messages regarding errors should be addressed to the authors.

NotesDisclaimer.

The findings and conclusions are those of the authors and do not necessarily represent the views of the US Centers for Disease Control and Prevention.

Financial support.

This work was supported by grant 48968 from The Bill & Melinda Gates Foundation to the International Vaccine Access Center, Department of International Health, Johns Hopkins Bloomberg School of Public Health.

Supplement sponsorship.

This article was published as part of a supplement entitled “Pneumonia Etiology Research for Child Health,” sponsored by a grant from The Bill & Melinda Gates Foundation to the PERCH Project of Johns Hopkins Bloomberg School of Public Health, Baltimore, Maryland.

Potential conflicts of interest.

All authors: No reported conflicts.

All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed.

BlackRECousensSJohnsonHLGlobal, regional, and national causes of child mortality in 2008: a systematic analysisLancet201037519698720466419SelwynBJThe epidemiology of acute respiratory tract infection in young children: comparison of findings from several developing countries. Coordinated Data Group of BOSTID ResearchersRev Infect Dis199012Suppl 8S870882270410PneumoACTION. PneumoFOCUS2011Available at: http://pneumoadip.idfive.com/news/pneumofocus/. Accessed 5 January 2012Addo-YoboEChisakaNHassanMOral amoxicillin versus injectable penicillin for severe pneumonia in children aged 3 to 59 months: a randomised multicentre equivalency studyLancet20043641141815451221AgarwalJAwasthiSRajputATiwariMJainAAtypical bacterial pathogens in community-acquired pneumonia in children: a hospital-based studyTrop Doct2009391091119299299Al-GhizawiGJAl-SulamiAAAl-TaherSSProfile of community- and hospital-acquired pneumonia cases admitted to Basra General Hospital, IraqEast Mediterr Health J2007132304217684843Al-KaabiNSolhZPachecoSMurrayLGabouryILe SauxNA Comparison of group A Streptococcus versus Streptococcus pneumoniae pneumoniaPediatr Infect Dis J20062510081217072122AndradeAOliveiraRVieiraMActive surveillance of invasive pneumococcal disease (IPD) and chest radiograph-confirmed pneumonia (CXR+Pn) in infants and young children in Goiânia, BrazilIn: International Symposium on Pneumococci and Pneumococcal Diseases2010Tel Aviv, Israel: ISPPDAnhDDKilgorePESlackMPSurveillance of pneumococcal-associated disease among hospitalized children in Khanh Hoa Province, VietnamClin Infect Dis200948Suppl 2S576419191620ArifeenSESahaSKRahmanSInvasive pneumococcal disease among children in rural Bangladesh: results from a population-based surveillanceClin Infect Dis200948Suppl 2S1031319191605AsgharRBanajehSEgasJChloramphenicol versus ampicillin plus gentamicin for community acquired very severe pneumonia among children aged 2–59 months in low resource settings: multicentre randomised controlled trial (SPEAR study)BMJ200833680418182412AzzariCMoriondoMIndolfiGMolecular detection methods and serotyping performed directly on clinical samples improve diagnostic sensitivity and reveal increased incidence of invasive disease by Streptococcus pneumoniae in Italian childrenJ Med Microbiol20085712051218809546BaggettHCPeruskiLFOlsenSJIncidence of pneumococcal bacteremia requiring hospitalization in rural ThailandClin Infect Dis200948Suppl 2S657419191621BambaMJozakiKSugayaNProspective surveillance for atypical pathogens in children with community-acquired pneumonia in JapanJ Infect Chemother200612364116506088BanajehSMNutritional rickets and vitamin D deficiency–association with the outcomes of childhood very severe pneumonia: a prospective cohort studyPediatr Pulmonol20094412071519911367BaquiAHRahmanMZamanKA population-based study of hospital admission incidence rate and bacterial aetiology of acute lower respiratory infections in children aged less than five years in BangladeshJ Health Popul Nutr2007251798817985819BaquiAHEl ArifeenSSahaSKEffectiveness of Haemophilus influenzae type B conjugate vaccine on prevention of pneumonia and meningitis in Bangladeshi children: a case-control studyPediatr Infect Dis J2007265657117596795BatuwanthudaweRKarunarathneKDassanayakeMSurveillance of invasive pneumococcal disease in Colombo, Sri LankaClin Infect Dis200948Suppl 2S1364019191609BerkleyJAMunywokiPNgamaMViral etiology of severe pneumonia among Kenyan infants and childrenJAMA20103032051720501927BharajPSullenderWMKabraSKRespiratory viral infections detected by multiplex PCR among pediatric patients with lower respiratory tract infections seen at an urban hospital in Delhi from 2005 to 2007Virol J200968919558656BiiCCKoseJTaguchiHPneumocystis jirovecii and microbiological findings in children with severe pneumonia in Nairobi, KenyaInt J Tuberc Lung Dis20061012869117131790BravoLGonzalesMLimAActive hospital-based epidemiological surveillance to estimate the burden of invasive pneumococcal disease (Ipd) in children in Metro Manila, PhilippinesIn: International Symposium on Pneumococci and Pneumococcal Diseases2010Tel Aviv, Israel: ISPPDBroughtonSSylvesterKPFoxGLung function in prematurely born infants after viral lower respiratory tract infectionsPediatr Infect Dis J20072610192417984809BruceNWeberMAranaBPneumonia case-finding in the RESPIRE Guatemala indoor air pollution trial: standardizing methods for resource-poor settingsBull World Health Organ2007855354417768502CapedingMBrooksDGraySActive hospital-based epidemiological surveillance of invasive pneumococcal disease (IPD) in children in Muntinlupa, PhilippinesIn: World Society for Pediatric Infectious Diseases2009Buenos Aires, Argentina: WSPIDCarrolEDGuiverMNkhomaSHigh pneumococcal DNA loads are associated with mortality in Malawian children with invasive pneumococcal diseasePediatr Infect Dis J2007264162217468652Cevey-MacherelMGaletto-LacourAGervaixAEtiology of community-acquired pneumonia in hospitalized children based on WHO clinical guidelinesEur J Pediatr200916814293619238436CharkalukMLKalachNMvogoHAssessment of a rapid urinary antigen detection by an immunochromatographic test for diagnosis of pneumococcal infection in childrenDiagn Microbiol Infect Dis200655899416530375ChintuCMudendaVLucasSLung diseases at necropsy in African children dying from respiratory illnesses: a descriptive necropsy studyLancet20023609859012383668ChoiSHParkEYJungHLSerum vascular endothelial growth factor in pediatric patients with community-acquired pneumonia and pleural effusionJ Korean Med Sci2006216081316891801ChongDCRaboniSMAbujamraKBRespiratory viruses in pediatric necropsies: an immunohistochemical studyPediatr Dev Pathol2009122111619018665ChistiMJAhmedTFaruqueASAbdus SalamMClinical and laboratory features of radiologic pneumonia in severely malnourished infants attending an urban diarrhea treatment center in BangladeshPediatr Infect Dis J201029174719927041CillaGOnateEPerez-YarzaEGMontesMVicenteDPerez-TralleroEViruses in community-acquired pneumonia in children aged less than 3 years old: high rate of viral coinfectionJ Med Virol2008801843918712820ColesCLBoseAMosesPDInfectious etiology modifies the treatment effect of zinc in severe pneumoniaAm J Clin Nutr20078639740317684211CuttsFTZamanSMEnwereGEfficacy of nine-valent pneumococcal conjugate vaccine against pneumonia and invasive pneumococcal disease in The Gambia: randomised, double-blind, placebo-controlled trialLancet200536511394615794968DareRKFryAMChittaganpitchMSawanpanyalertPOlsenSJErdmanDDHuman coronavirus infections in rural Thailand: a comprehensive study using real-time reverse-transcription polymerase chain reaction assaysJ Infect Dis20071961321817922396DeerojanawongJPrapphalNSuwanjuthaSPrevalence and clinical features of mycoplasma pneumoniae in Thai childrenJ Med Assoc Thai2006891641717128838DonMFasoliLPaldaniusMAetiology of community-acquired pneumonia: serological results of a paediatric surveyScand J Infect Dis2005378061216308213EunBWKimNHChoiEHLeeHJMycoplasma pneumoniae in Korean children: the epidemiology of pneumonia over an 18-year periodJ Infect2008563263118420275FaladeAGLagunjuIABakareRAOdekanmiAAAdegbolaRAInvasive pneumococcal disease in children aged <5 years admitted to 3 urban hospitals in Ibadan, NigeriaClin Infect Dis200948Suppl 2S190619191615FreitasMCasteloAPettyGGomesCECarvalhoEViridans streptococci causing community acquired pneumoniaArch Dis Child2006917798016737994GerberJSCoffinSESmathersSAZaoutisTETrends in the incidence of methicillin-resistant Staphylococcus aureus infection in childre’s hospitals in the United StatesClin Infect Dis200949657119463065HakanssonSKallenKImpact and risk factors for early-onset group B streptococcal morbidity: analysis of a national, population-based cohort in Sweden 1997–2001BJOG20061131452817083655Hamano-HasegawaKMorozumiMNakayamaEComprehensive detection of causative pathogens using real-time PCR to diagnose pediatric community-acquired pneumoniaJ Infect Chemother2008144243219089556HonKLLeungETangJPremorbid factors and outcome associated with respiratory virus infections in a pediatric intensive care unitPediatr Pulmonol2008432758018219695HsiehSCKuoYTChernMSChenCYChanWPYuCMycoplasma pneumonia: clinical and radiographic features in 39 childrenPediatr Int200749363717532837HsiehWYChiuNCChiHHuangFYHungCCRespiratory adenoviral infections in Taiwanese children: a hospital-based studyJ Microbiol Immunol Infect200942371720182665HuangHHZhangYYXiuQYCommunity-acquired pneumonia in Shanghai, China: microbial etiology and implications for empirical therapy in a prospective study of 389 patientsEur J Clin Microbiol Infect Dis2006253697416767484IngarfieldSLCelenzaAJacobsIGRileyTVThe bacteriology of pneumonia diagnosed in Western Australian emergency departmentsEpidemiol Infect200713513768317274861JaspanHBHuangLCCottonMFWhitelawAMyerLBacterial disease and antimicrobial susceptibility patterns in HIV-infected, hospitalized children: a retrospective cohort studyPLoS One20083e326018813340JohnsonAWOsinusiKAdereleWIGbaderoDAOlaleyeODAdeyemi-DoroFAEtiologic agents and outcome determinants of community-acquired pneumonia in urban children: a hospital-based studyJ Natl Med Assoc20081003708518481475KumarMBiswalNBhuvaneswariVSrinivasanSPersistent pneumonia: underlying cause and outcomeIndian J Pediatr2009761223619941090KuypersJMartinETHeugelJWrightNMorrowREnglundJAClinical disease in children associated with newly described coronavirus subtypesPediatrics2007119e70617130280LahtiEPeltolaVWarisMInduced sputum in the diagnosis of childhood community-acquired pneumoniaThorax200964252719052043LehtinenPJarttiTVirkkiRBacterial coinfections in children with viral wheezingEur J Clin Microbiol Infect Dis200625463916819619LindbladeKAArveloWGrayJA comparison of the epidemiology and clinical presentation of seasonal influenza A and 2009 pandemic influenza A (H1N1) in GuatemalaPLoS One20105e1582621209850LiuFCChenPYHuangFTsaiCRLeeCYWangLCRapid diagnosis of Mycoplasma pneumoniae infection in children by polymerase chain reactionJ Microbiol Immunol Infect2007405071218087631LochindaratSSuwanjuthaSPrapphalNMycoplasma pneumoniae and Chlamydophila pneumoniae in children with community-acquired pneumonia in ThailandInt J Tuberc Lung Dis2007118141917609060LuceroMGNohynekHWilliamsGEfficacy of an 11-valent pneumococcal conjugate vaccine against radiologically confirmed pneumonia among children less than 2 years of age in the Philippines: a randomized, double-blind, placebo-controlled trialPediatr Infect Dis J2009284556219483514MadhiSAKlugmanKPA role for Streptococcus pneumoniae in virus-associated pneumoniaNat Med2004108111315247911MartinezMAMillanFGonzalezCChlamydia trachomatis genotypes associated with pneumonia in Chilean infantsScand J Infect Dis2009413131619177260MathisenMStrandTASharmaBNRNA viruses in community-acquired childhood pneumonia in semi-urban Nepal; a cross-sectional studyBMC Med200973519635124McNallyLMJeenaPMGajeeKEffect of age, polymicrobial disease, and maternal HIV status on treatment response and cause of severe pneumonia in South African children: a prospective descriptive studyLancet200736914405117467514MorenoLKrishnanJADuranPFerreroFDevelopment and validation of a clinical prediction rule to distinguish bacterial from viral pneumonia in childrenPediatr Pulmonol200641331716493666MudhuneSWamaeMReport on invasive disease and meningitis due to Haemophilus influenzae and Streptococcus pneumonia from the network for surveillance of pneumococcal disease in the East African regionClin Infect Dis200948Suppl 2S1475219191610NaheedASahaSKBreimanRFMultihospital surveillance of pneumonia burden among children aged <5 years hospitalized for pneumonia in BangladeshClin Infect Dis200948Suppl 2S82919191623Nascimento-CarvalhoCMRibeiroCTCardosoMRThe role of respiratory viral infections among children hospitalized for community-acquired pneumonia in a developing countryPediatr Infect Dis J2008279394118756190NgeowYFSuwanjuthaSChantarojanasririTAn Asian study on the prevalence of atypical respiratory pathogens in community-acquired pneumoniaInt J Infect Dis200591445315840455PaddockCDSandenGNCherryJDPathology and pathogenesis of fatal Bordetella pertussis infection in infantsClin Infect Dis2008473283818558873PerezAHerranzMSeguraMEpidemiologic impact of blood culture practices and antibiotic consumption on pneumococcal bacteraemia in childrenEur J Clin Microbiol Infect Dis2008277172418347821RahmanMHossainSBaquiAHHaemophilus influenzae type-b and non-b-type invasive diseases in urban children (<5 years) of Bangladesh: implications for therapy and vaccinationJ Infect200856191618280571RobertsonSERocaAAlonsoPRespiratory syncytial virus infection: denominator-based studies in Indonesia, Mozambique, Nigeria and South AfricaBull World Health Organ2004829142215654405RocaASigauqueBQuintoLInvasive pneumococcal disease in children<5 years of age in rural MozambiqueTrop Med Int Health20061114223116930265RutmanMSBachurRHarperMBRadiographic pneumonia in young, highly febrile children with leukocytosis before and after universal conjugate pneumococcal vaccinationPediatr Emerg Care2009251719116501SamransamruajkitRHiranratTChieochansinTPrevalence, clinical presentations and complications among hospitalized children with influenza pneumoniaJpn J Infect Dis200861446919050351SandoraTJDesaiRMikoBAHarperMBAssessing quality indicators for pediatric community-acquired pneumoniaAm J Med Qual2009244192719520967ShahASKnollMDSharmaPRInvasive pneumococcal disease in Kanti children’s hospital, Nepal, as observed by the South Asian pneumococcal alliance networkClin Infect Dis200948Suppl 2S123819191607ShahASNisargaRRavi KumarKLHublerRHerreraGKilgorePEEstablishment of population-based surveillance for invasive pneumococcal disease in Bangalore, IndiaIndian J Med Sci20096349850720075551SingletonRJBulkowLRMiernykKViral respiratory infections in hospitalized and community control children in AlaskaJ Med Virol20108212829020513097SungRYChanPKTsenTIdentification of viral and atypical bacterial pathogens in children hospitalized with acute respiratory infections in Hong Kong by multiplex PCR assaysJ Med Virol200981153919031443TajimaTNakayamaEKondoYEtiology and clinical study of community-acquired pneumonia in 157 hospitalized childrenJ Infect Chemother200612372917235643TregnaghiMCeballosARuttimannRActive epidemiologic surveillance of pneumonia and invasive pneumococcal disease in ambulatory and hospitalized infants in Cordoba, ArgentinaPediatr Infect Dis J200625370216567994TumgorGCelikUAlabazDAetiological agents, interleukin-6, interleukin-8 and CRP concentrations in children with community- and hospital-acquired pneumoniaAnn Trop Paediatr2006262859117132293van WoenselJBBosAPLutterRRossenJWSchuurmanRAbsence of human metapneumovirus co-infection in cases of severe respiratory syncytial virus infectionPediatr Pulmonol200641872416850438WalterNDTaylorTHShayDKInfluenza circulation and the burden of invasive pneumococcal pneumonia during a non-pandemic period in the United StatesClin Infect Dis2010501758320014948WatanabeKAnhDDHuong PleTDrug-resistant pneumococci in children with acute lower respiratory infections in VietnamPediatr Int2008505141819143975WilliamsEJThorsonSMaskeyMHospital-based surveillance of invasive pneumococcal disease among young children in urban NepalClin Infect Dis200948Suppl 2S1142219191606WilliamsJVEdwardsKMWeinbergGAPopulation-based incidence of human metapneumovirus infection among hospitalized childrenJ Infect Dis20102011890820446850WolfDGGreenbergDShemer-AvniYGivon-LaviNBar-ZivJDaganRAssociation of human metapneumovirus with radiologically diagnosed community-acquired alveolar pneumonia in young childrenJ Pediatr20101561152019782998XatzipsaltiMKyranaSTsoliaMRhinovirus viremia in children with respiratory infectionsAm J Respir Crit Care Med200517210374015994468ZhangHYLiZMZhangGLDiaoTTCaoCXSunHQRespiratory viruses in hospitalized children with acute lower respiratory tract infections in Harbin, ChinaJpn J Infect Dis2009624586019934539World Health OrganizationConclusions from the WHO multicenter study of serious infections in young infants. The WHO Young Infants Study GroupPediatr Infect Dis J199918Suppl 10S32410530571TurnerGWonodiCLevineOScottJAMurdochDMethodological and practical challenges in post-mortem studies of pneumonia etiologyClin Infect Dis2012In PressCentersfor Disease Control and PreventionDivision of bacterial diseases bulletin2010Winter 2010. Available at: http://www.cdc.gov/ncird/downloads/dbd-bull-winter10-508.pdf. Accessed 27 July 2011RuuskanenOLahtiEJenningsLCMurdochDRViral pneumoniaLancet201137712647521435708