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The goal of syndromic surveillance is the earlier detection of epidemics, allowing a timelier public health response than is possible using traditional surveillance methods. Syndromic surveillance application for public health purposes has changed
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  The remarkable adaptability of syndromicsurveillance to meet public health needs Beverley J. Paterson  a,b, * , David N. Durrheim  a,b,c a Hunter Medical Research Institute, University of Newcastle, Newcastle, Australia b Private Bag 10, Wallsend, 2287 NSW, Australia c Hunter New England Population Health, Newcastle, Australia Received 13 June 2012; received in revised form 11 December 2012; accepted 18 December 2012Available online 20 January 2013 KEYWORDS Syndromic surveillance;Outbreaks;International HealthRegulations;Infectious diseases;Public health Abstract  The goal of syndromic surveillance is the earlier detection of epidemics,allowing a timelier public health response than is possible using traditional surveil-lance methods. Syndromic surveillance application for public health purposes haschanged over time and reflects a dynamic evolution from the collection, interpreta-tion of data with dissemination of data to those who need to act, to a more holisticapproach that incorporates response as a core component of the surveillance sys-tem. Recent infectious disease threats, such as severe acute respiratory syndrome(SARS), avian influenza (H5N1) and pandemic influenza (H1N1), have all highlightedthe need for countries to be rapidly aware of the spread of infectious diseases withina region and across the globe. The International Health Regulations (IHR) obligationto report public health emergencies of international concern has raised the impor-tance of early outbreak detection and response. The emphasis in syndromic surveil-lance is changing from automated, early alert and detection, to situationalawareness and response. Published literature on syndromic surveillance reflectsthe changing nature of public health threats and responses. Syndromic surveillancehas demonstrated a remarkable ability to adapt to rapidly shifting public healthneeds. This adaptability makes it a highly relevant public health tool. ª  2013 Ministry of Health, Saudi Arabia. Published by Elsevier Ltd. All rightsreserved. 1. Introduction Syndromic surveillance provides an indication ofdisease patterns, a method for detecting aberra-tions in health data, or a signal that an event ofpublic health concern is occurring. Syndromic sur-veillance systems have been implemented sincethe 1990s, initially with a focus on bioterrorismevent detection.Last (2001) [1] defines a syndrome as: ‘‘A symp-tom complex in which the symptoms and/or signscoexist more frequently than would be expected 2210-6006/$ - see front matter  ª  2013 Ministry of Health, Saudi Arabia. Published by Elsevier Ltd. All rights reserved.http://dx.doi.org/10.1016/j.jegh.2012.12.005* Corresponding author at: Private Bag 10, Wallsend, 2287NSW, Australia. Tel.: +61 49246275. E-mail address:  Beverley.Paterson@hnehealth.nsw.gov.au(B.J. Paterson).Journal of Epidemiology and Global Health  (2013)  3 , 41  –  47 http:// www.elsevier.com/locate/jegh  by chance on the assumption of independence.’’ Insurveillance terms,   syndromic   relates to a specificset of symptoms not requiring laboratory confirma-tion for diagnosis. Common examples of syndromesused for syndromic surveillance include: acute flac-cid paralysis (AFP), a syndrome potentially indica-tive of poliomyelitis; influenza-like-illness (ILI); oracutefeverandrash,asyndromepotentiallyindica-tive of measles.Syndromic surveillance captures a spectrum ofapproaches ranging from fully automated systems,using sophisticated statistical algorithms, to simplemanual systems. It includes very specific case def-initions for syndromes such as AFP to the genericcounting of over-the-counter medications forcoughs and colds. As it is based on clinical syn-dromes rather than laboratory confirmation, it isalso potentially useful in settings where there islimited timely access to laboratories, includingmany developing countries [2]. As an approach,syndromic surveillance incorporates elements ofdata collection and analysis of specific syndromesor indicators (to detect disease), verification (thatdisease actually exists), information sharing (tothose who need to know in order to respond), feed-back to those who collected the data (to confirmthat an action is occurring), and, in many recentcases, response and control measures to mitigateglobal health security threats.Recent infectious disease threats such as SARS,avian influenza (H5N1) and pandemic influenza(H1N1) have highlighted the need for governmentsand public health agencies to rapidly learn of poten-tialinfectiousdiseasethreatstofacilitatetimelyandappropriate public health responses. The require-ment for improved early warning and response sys-tems may be   reshaping   global health surveillance[3]. The published literature on syndromic surveil-lance reflects the changing nature of these threatsand responses. Over time, syndromic surveillancehas been applied to a remarkable range of publichealth issues using a wide variety of data sources.Notonlyhasitbeenusedtocollectdataonparticulardisease syndromes, butithas also been usedtomon-itor the public  s health following, or during, naturaldisasters,suchastheIcelandicashcloud,massgath-erings, heat waves, floods or pandemics.This paper documents the evolution of syn-dromic surveillance from bioterrorist detectionsystems to those implemented for outbreak detec-tion and response. By characterising the changingapproaches used in syndromic surveillance, andthe drivers for this change, it demonstrates theencouraging adaptability of syndromic surveillanceand the important role it plays in public health. 2. Methodology An analysis of published articles on syndromic sur-veillance was undertaken in published English-lan-guage literature to examine the evolution ofsyndromic surveillance. MEDLINE, EMBASE, Scopusand Web of Science databases were searched usingthe term ‘‘syndromic surveillance’’ for English lan-guage studies published prior to February 2012.After removing duplicates and non-English languagearticles, 415 records were obtained. Citations weredownloaded into Endnote X4. Reference lists werethen hand searched to obtain further relevant addi-tional published articles and a total of 769 articleswere thus included in the study.To identify trends in the publication of syn-dromic surveillance articles, PubMed was searchedfor all articles with the term   syndromic surveil-lance   in the title or abstract, as published in Pub-Med prior to 20 February, 2012; 214 articles wereobtained and were downloaded into Endnote X4.This database was then searched to identify publi-cation year for each article and the number of arti-cles published each year. The database was furthersearched using the terms   bioterrorism   and   influ-enza   to identify articles published each year onthese topics. Keywords assigned to these articleswere extracted for the periods 2001–2004, 2005–2008, and 2009–2011, based on visual changes inthe data, and these were imported into NVivo 9.Each of these time-periods was queried and a tagcloud created. Tag clouds represent by size the fre-quency of a particular word in a document, or inthis case the frequency of keywords used in syn-dromic surveillance publications. The tag cloudused a Word search for the 100 most frequentwords with the following characteristics: a mini-mum length of six characters; matching set to in-clude stemmed words; and used the followingStop words – epidemiology, methods, statistics,and numerical – to reduce visual confusion in thetag cloud results. 3. Results and discussion In this study, published literature was examined toassess the evolving usage of syndromic surveillancefor public health purposes.While generally acknowledged as a simplifiedview of the many approaches used in syndromicsurveillance, predominantly two different ap-proaches were commonly reported in the litera-ture. The first is based on networked systems andencompasses the timely, automated extraction,42 B.J. Paterson, D.N. Durrheim  using syndromic algorithms from an individual ormultiple data sources, with alerts generated whenthere is an exceedance of a baseline thresholdusing statistical methods. The emphasis in this ap-proach is on the timely, automated collection ofdata; the application of a syndromic algorithm toclinical or non-clinical data; the use of statisticalmethods to recognise that the data are exceedinga defined threshold or to monitor trends; and thegeneration of alerts to those who need to knowso that a response can be implemented. This formof syndromic surveillance is traditionally associ-ated with systems designed to rapidly detect biot-errorism events. An example is the Essence(Electronic Surveillance System for the Early Notifi-cation of Community-Based Epidemics), a bio-surveillance system used in the United States whichuses aberration detection algorithms of syndromegroups, extracted from ICD-9 classification groups,to detect whether the observed count is above orbelow the expected count [4].The second approach involved the regular,timely reporting of syndromic activity, based onagreed case definitions, at sentinel sites; detectionof outbreaks, either based on an exceedance of his-torical data, or the reporting of syndromic cases inexcess of the number clinicians would usually ex-pect (which may include the reporting of unusualmedical events); proportionate investigation andresponse; and regular feedback to concerned par-ties. The emphasis here was on both detectionand response, with low technological requirementsmaking it suitable for use in developing regions. Anexample of this is the syndromic surveillance sys-tem established in the Pacific Island Countriesand Territories (PICT) [5]. 3.1. Early application of syndromicsurveillance in public health The different approaches reflect the flexibility ofsyndromic surveillance to adapt to changing publichealth requirements and, while not truly linear intime, noticeable trends or themes are apparentin the literature. An exploration of the literaturerevealed that while public health surveillance wasbeing discussed and implemented from the early1960s, based on the visionary work of Langmuir[6] and Raska [7], with many of the principles developed then still applicable, the term syn-dromic surveillance only regularly entered peer-re-viewed literature at the beginning of the twentiethcentury.In the 1980s, the goal of global eradication ofpolio resulted in acute flaccid paralysis (AFP) sur-veillance being implemented globally as the keysurveillance measure for the eradication of polio[8]. T. Jacob John also established a novel, dis-trict-level disease surveillance system in SouthernIndia [9], which sought to control and limit diseaseoutbreaks through early detection (described by astandardised set of symptoms); regular reportingand response; and would be termed a syndromicsurveillance system if implemented today. Thismodel included elements of data collection, analy-sis, confirmation, feedback and response – all keyelements of modern-day syndromic surveillance.This approach was later further adapted in a ruralAfrican setting with a focus on rural hospitalsreporting presentations of nine core clinical syn-dromes, including cholera and meningitis-like dis-ease [10].In the 1990s, the STD and HIV literature docu-mented the value of syndrome-based diagnosisand treatment for case management purposes[11,12]. There were also some early examples ofoutbreak surveillance systems based on syndromesin developed countries. Among other examples,New York City implemented a syndromic surveil-lance system to detect outbreaks of waterborne ill-ness using surveillance for diarrhoeal illness, stoolsubmissions in laboratories and over-the-counter(OTC) pharmacy sales [13]; and public health offi-cials in England compared data collected througha call centre (NHS Direct), using an algorithm forinfluenza-like symptoms, to routinely available sur-veillance data to assess the usefulness of syn-dromic surveillance for influenza surveillance [14]. 3.2. Syndromic surveillance application inresponse to the bioterrorism threat In the literature there was an apparent surge ininterest in syndromic surveillance following theterrorist events in the United States of America,the United Kingdom and Spain, as well as the2001 anthrax outbreak [15]. The word syndromicwas applied because the majority of such systemsmonitored syndromes which might herald the earlystages of epidemics [16]. Fig. 1 presents a graphic representation of the adaptability of syndromicsurveillance as public health requirements forinformation have changed. A review of the pub-lished literature on syndromic surveillance showsthe rapid growth in publications following the ter-rorist attacks, with the number of publicationspublished each year peaking in 2004, after theemergence of SARS. These events appear to haveaccelerated the development of syndromic surveil-lance as a tool for the early identification of unex-pected biological events [17].The remarkable adaptability of syndromic surveillance to meet public health needs 43  3.3. Syndromic surveillance and emerginginfectious disease threats Fig. 1 demonstrates that from 2005 there was a de-crease in the number of publications addressingbioterrorism and a shift in focus to emergent dis-eases and pandemics (with   influenza   used hereas a proxy indicator). A second wave of interestin syndromic surveillance is apparent from 2008after the emergence of avian influenza and the2009 influenza pandemic. Tag clouds, as shown inFig. 2, highlight the predominance of bioterrorismas a keyword in syndromic surveillance publicationsfrom 2001 to 2004, and its lessening importanceover time. In contrast, influenza and outbreaks in-crease in importance reflecting increasing publichealth activities in these two areas from 2005 to2011.Many recent emergent pathogenic infectious dis-eases have signalled their emergence through casespresenting with particular syndromes, such asencephalitis, influenza-like-illness (ILI) or severeacute respiratory syndrome (SARS), emphasisingthe importance of surveillance for syndromes as amethod of detecting emergent diseases. The highlypathogenic Nipah and Hendra viruses presented asan encephalitic syndrome with a high case fatalityrate [18,19]. The arrival of SARS in 2003 focusedthe world  s attention on emerging infectious dis-eases (EID) [16], the potential for an EID to cause‘‘significant social and economic disruption,’’ andthe need for early identification to limit furtherspread [20]. SARS was the first infectious diseaseevent in modern times that confirmed how rapidlya deadly disease could spread across the globe andthe subsequent cost to infected individuals and af-fected countries   economies [21]. More recently, asyndromic approach first signalled a disturbing,unusual event occurring in Jordan when an appar-ent cluster of cases and fatalities from an unknowndisease presented as a SARS with renal complica-tions. It was only when this disease was finally iden-tified, in a later case, as a novel coronavirus thatthe mystery behind the unusual cluster was solved[22]. Enhanced syndromic surveillance for furtherSARS presentation due to this novel coronavirushas currently been recommended at the global le-vel by the World Health Organization [23].The advent of SARS in 2003 led public healthofficials in developed economies to appreciatethe potential benefits of syndromic surveillanceto public health beyond bioterrorism and the possi-bility that it could be used to detect unusual dis-ease clusters [24,25]. The influenza pandemic(H1N1) in 2009 also highlighted the need for sur-veillance systems able to provide early detectionof first cases through the identification of patientswith an ILI syndrome [26]. It also had value laterduring the pandemic; Elliott (2009) noted thatwhen countries changed phase to   containment  ,and were no longer able to laboratory confirm eachcase, then ‘‘syndromic surveillance takes prece-dence as the primary means of estimating the com-munity burden of pandemic influenza infections[27].’’ As a result of the pandemic, and in an effortto improve public health surveillance, the CDC sta-ted that it was ‘‘expanding and automating syn-dromic surveillance [28].’’ 3.4. Syndromic surveillance and theInternational Health Regulations The 2005 IHR revision required all countries to de-velop certain minimum core public health capaci-ties, including the ability to detect and respondto communicable disease outbreaks, and the rapidreporting of public health emergencies of interna-tional concern to the World Health Organization(WHO) [29]. Included in the IHR core capacityrequirements are: ‘‘surveillance, reporting, notifi-cation, verification, response and collaborationactivities [29].’’ The IHR obligation to report pub-lic health emergencies of international concernhave raised the importance of early outbreakdetection and response.Standardised approaches to data collection,analysis, reporting, outbreak investigation and re-sponse are necessary for a surveillance system toeffectively serve as an early warning system forbiological, chemical or radiological threats. Evalu-ations of syndromic surveillance systems are neces-sary to confirm that they are able to meet publichealth requirements and obligations by adequately Figure 1  Trends in syndromic surveillance publica-tions, 2001–2011. 44 B.J. Paterson, D.N. Durrheim  identifying outbreaks when they are occurring and,when an outbreak is detected, that there is anappropriate public health response [30,31].For developing countries, where there are oftenlong delays in laboratory confirmation, the imple-mentation of simple syndromic surveillance sys-tems may provide the opportunity to ensure acountry  s early warning and response capacity[32]. The Pacific Island Countries and Territories(PICT) have developed a syndromic surveillancesystem to respond to an identified need for afunctional surveillance system, capable of identify-ing and responding to outbreaks in a systematicmanner, while taking account of limited local Figure 2  Tag clouds for keywords extracted from published literature on syndromic surveillance, 2001–2011. The remarkable adaptability of syndromic surveillance to meet public health needs 45
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