ONLINE REPORT Global Avian Infuenza Surveillance in Wild Birds: a Strategy to Capture Viral Diversity

ONLINE REPORT Global Avian Infuenza Surveillance in Wild Birds: A Strategy to Capture Viral Diversity

Catherine C. Machalaba, Sarah E. Elwood, which has spilled over repeatedly to humans since its frst Simona Forcella, Kristine M. Smith, report in 1996; and novel avian infuenza A(H7N9) virus, Keith Hamilton, Karim B. Jebara, frst detected in March 2013, which has caused serious hu- David E. Swayne, Richard J. Webby, man infections across China. Wild birds played a role in the Elizabeth Mumford, Jonna A.K. Mazet, evolution of infuenza A(H7N9) virus (3) and might have Nicolas Gaidet, Peter Daszak, William B. Karesh contributed to the spread of this virus to parts of Asia, Eu- rope, and Africa after a 2005 outbreak in birds at Qinghai Wild birds play a major role in the evolution, maintenance, Lake in China (4,5). and spread of avian infuenza viruses. However, surveil- Most recently, wild birds have been considered as hav- lance for these viruses in wild birds is sporadic, geographi- ing a role in the unexpected appearance and spread of infu- cally biased, and often limited to the last outbreak virus. To identify opportunities to optimize wild bird surveillance for enza A(H5N8) virus in Europe in November 2014 and in understanding viral diversity, we reviewed responses to a North America in December 2014; genetically similar lin- World Organisation for Animal Health–administered survey, eages have also been found in South Korea and Japan (6). government reports to this organization, articles on Web of Concern about highly pathogenic avian infuenza viruses has Knowledge, and the Infuenza Research Database. At least generated sporadic attention and investments paired to spe- 119 countries conducted avian infuenza virus surveillance cifc subtypes. For example, alarm about infuenza A(H5N1) in wild birds during 2008–2013, but coordination and stan- virus resulted in short-term spending of hundreds of millions dardization was lacking among surveillance efforts, and of dollars for wild bird–related research globally. Although most focused on limited subsets of infuenza viruses. Given interest and funding has since waned, threats from avian in- high fnancial and public health burdens of recent avian infu- fuenza viruses remain, and H5N1 and H7N9 subtype virus- enza outbreaks, we call for sustained, cost-effective invest- es continue to cause human infections and deaths. ments in locations with high avian infuenza diversity in wild birds and efforts to promote standardized sampling, testing, Wild birds are natural reservoirs for avian infuenza and reporting methods, including full-genome sequencing virus (4,7), host a wide diversity of subtypes, and provide a and sharing of isolates with the scientifc community. dynamic population for viral evolution and transmission to domestic focks and mammals. Most hemagglutinin (HA) and neuraminidase (NA) subtypes have been detected in vian infuenza is a global threat to food animal produc- wild birds, although some infrequently (8,9). Highly patho- tion and distribution systems, as well as human health. A genic avian infuenza viruses of poultry are defned by the However, sustained, comprehensive, and coordinated glob- World Organisation for Animal Health (OIE) as having an al efforts to monitor the continually changing genetic diver- intravenous pathogenicity index >1.2 in 6-week-old chick- sity of avian infuenza viruses circulating in nature are lack- ens and causing ≥75% deaths in 4 to 8-week-old chickens ing (1,2). Two avian infuenza viruses are current pandemic infected intravenously, or H5 or H7 virus isolates with a threats: highly pathogenic avian infuenza A(H5N1) virus, characteristic molecular sequence at the HA cleavage site Author affliations: EcoHealth Alliance, New York, New York, USA (for full defnition, see the OIE Terrestrial Animal Health (C.C. Machalaba, S.E. Elwood, K.M. Smith, P. Daszak, W.B. Code [10]). Although these viruses are rarely detected in Karesh); World Organisation for Animal Health, Paris, France wild birds, they have been found in diverse wild bird spe- (S. Forcella, K. Hamilton, K.B. Jebara, W.B. Karesh); Ministry of cies from disparate locations and can be potentially trans- Environment and Water, Dubai, United Arab Emirates mitted along transcontinental fyways (5). (K.B. Jebara); US Department of Agriculture, Athens, Georgia, Avian infuenza rarely causes widespread deaths in USA (D.E. Swayne); St. Jude Children’s Research Hospital, wild birds, and infuenza caused by H5N1 subtype virus Memphis, Tennessee, USA (R.J. Webby); World Health represents the frst major clinical avian infuenza virus–as- Organization, Geneva, Switzerland (E. Mumford); University of sociated disease recognized in wild birds since the out- California, Davis, California, USA (J.A.K. Mazet); French break of infuenza caused by H5N3 subtype virus in South Agricultural Research Centre for International Development, Africa in 1961 in common terns (Sterna hirundo) (7,11). Montpellier, France (N. Gaidet); International Union for the Thus, limiting surveillance for avian infuenza virus to only Conservation of Nature Species Survival Commission, New York deaths of wild birds provides little insight into the diversity (W.B. Karesh) of avian infuenza virus genotypes circulating globally or risk for future outbreaks in poultry or humans. DOI: http://dx.doi.org/10.3201/eid2104.141415

e1 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 21, No. 4, April 2015 ONLINE REPORT

Programs implemented during sporadic periods of et al. (1) analyzed 191 literature reports of wild bird sur- concern (e.g., the Global Avian Infuenza Network for Sur- veillance initiated during 1961–2007 and identifed needs veillance of Wild Birds after infuenza outbreaks caused by for a coordinated scientifc approach, including refned H5N1 subtype viruses in 2005 [12]) have provided useful sampling and screening strategies. Our analysis incorpo- data on avian infuenza virus diversity for a limited number rates additional surveillance and viral diversity data sourc- of isolates but have missed the opportunity to document es available at a global level and assesses current/recent how diversity changes over time (1). The situation for wild efforts to determine capacity and actions needed for an ef- bird surveillance parallels similar constraints for surveil- fective avian infuenza virus tracking system in wild birds lance of infuenzas circulating in swine, as highlighted in a (online Technical Appendix, http://wwwnc.cdc.gov/EID/ recent review (13). article/21/4/14-1415-Techapp1.pdf). Other sources of in- While focusing on wild birds, we recognize the ben- formation (e.g., in local languages) might provide further efts of globally coordinated surveillance systems for all in- useful information for future analyses. fuenza viruses with the aims of multitype detection, whole- genome sequencing, sharing of virus isolates, and analysis OIE Member Survey of epidemiologic data to highlight changes in circulating Forty-six (25.8%) of 178 OIE member countries respond- virus subtype prevalence. In contrast to our current system, ed to an infuenza surveillance survey (online Technical which largely emphasizes reacting to new avian infuenza Appendix). Eleven (23.9%) of 46 responding countries re- viruses once they are detected in poultry, more upstream ported active (live birds) and passive (dead birds) surveil- tracking of this information could potentially provide a lance activities (whether collected specifcally for the study critical early warning system or at least provide a sense of or by other means [e.g., sampling of hunter collections]); the likely evolution and movement of these viruses so that 14 (30.4%) reported active surveillance only; 14 (30.4%) more proactive action can be taken. conducted passive surveillance only; and the remaining 7 Wild bird surveillance information could directly ben- (15.2%) reported conducting no surveillance activity. Sev- eft human and animal health through understanding of how eral of these countries cited a lack of funding as the imped- avian infuenza virus genes fow into poultry, swine, equine, iment. Of 39 countries that reported surveillance (online and human infuenza viruses and could provide a basis for Technical Appendix), 23 (58.9%) specifed testing for virus strategies that reduce their risk for introduction into agri- subtypes deemed to be a higher pathogenic risk to poultry cultural species and humans. The documented human case and humans (H5, H7, and all highly pathogenic avian in- of infuenza in Taiwan in 2013 caused by an H6N1 subtype fuenza viruses identifed) and 9 (23.0%) reported that they virus (14) points to the potential value of broader avian infu- tested to determine all subtypes found. Only 11 subtype enza virus surveillance in other species because this subtype combinations were reported through the OIE survey from 9 has rarely been included in infuenza surveillance systems. countries during January 2012–March 2013. In recognition of the potential benefts of surveillance, the OIE–Food and Agriculture Organization global OIE–World Animal Health Information network of expertise on animal infuenza (OFFLU) estab- Data Interface lished a working group on wildlife infuenzas in October A total of 116 countries submitted reports during the period 2014; this group has highlighted the need for wild bird sur- examined (2008–2012) (17). Reports indicated that 82 of veillance to understand circulation dynamics of avian infu- those countries conducted some form of avian infuenza vi- enza virus and recommends full-genome sequencing (15). ral surveillance in wild birds (online Technical Appendix). In April 2014, the Strategic Alliances for the Coordination One country reported highly pathogenic avian infuenza vi- of Research on the Major Infectious Diseases of Animals rus (H5N1 subtype), 6 reported low pathogenicity avian in- and Zoonoses identifed avian infuenza surveillance in fuenza during 2008–2012 (including 10 HA segments and wild birds as a top priority for collaboration as part of a 39 subtype combinations), and the remainder reported no 10-year strategic research agenda (16). We review current viruses. The other countries did not report detection. Of the surveillance efforts and provide recommendations toward 682 entries of highly pathogenic and low pathogenicity vi- establishing an effective surveillance program for avian in- ruses detected in wild birds from the 37 countries reporting fuenza in wild birds. detection or suspicion of avian infuenza, 244 entries were at the serotype (HA type or subtype combination) level of Assessing the Current State of information. Wild Bird Surveillance A global look at multiple major data sources on wild bird Infuenza Research Database surveillance for avian infuenza viruses by country has not A total of 39 countries (online Technical Appendix) re- been previously reported. An excellent review by Hoye ported wild bird surveillance. This surveillance, which e2 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 21, No. 4, April 2015 ONLINE REPORT was based on species name, was conducted during January genetic sequences. Finally, analysis of which types of sam- 2008–June 2013. ples yielded more positive results (e.g., cloacal swab versus fecal specimens) is not possible from these data, which Web of Knowledge limits their value in informing future sampling strategies. At least 54 countries reported wild bird surveillance during We recognize that studies have had varied aims that 2008–2013. This surveillance was reported mainly through contribute to differences in surveillance methods. Howev- peer-reviewed literature. er, the lack of standardized, sustained, and targeted surveil- We found that ≥119 countries conducted and reported lance prevents effective tracking of avian infuenza virus some form of avian infuenza virus surveillance in wild diversity over time in the major reservoir for this group of birds during January 2008–January 2013 (online Technical viruses. Opportunities for systematic avian infuenza virus Appendix). We identifed 3 trends in surveillance efforts surveillance could have been readily implemented through and their implications for comparability of data, as well as existing programs. For example, regional guidance through opportunities for refning surveillance strategies to capture the European Union (EU) directives on wild bird surveys diversity of avian infuenza viruses. has promoted some level of comparability of data through The frst trend was sampling method (active versus a required uniform reporting format, which led to exten- passive surveillance; number of birds and species sampled; sive data sharing. In 2006, EU member states reported hav- types of samples collected as cloacal, oropharyngeal/tra- ing tested 120,706 birds (active and passive surveillance) cheal, fecal, blood, or tissue samples; sampling site charac- in ≥330 species of 22 orders (19). Unfortunately, samples terization; frequency and seasonality of sampling) differs were not screened beyond infuenza A virus (or, in some widely across surveillance programs. This fnding is con- cases, H5 or H7 subtype viruses) under the EU directive. sistent with analysis of surveillance efforts of Hoye et al (1) Future regional coordinated efforts could begin to increase conducted during 1961–2007 and suggested that unstan- avian infuenza virus tracking even if only requiring full dardized sampling approaches remain a chronic challenge genome sequencing on a subset of samples. Ongoing sys- for a global avian infuenza virus surveillance system. Sam- tematic surveillance can inform avian infuenza virus ecol- pling methods, although not necessarily a limiting factor in ogy research, going beyond pattern descriptions or experi- identifying the wide range of these viruses circulating in mental conditions by generating long-term data to address nature, pose diffculties in discerning the usefulness of a complex processes around dynamics of host immunity or report and comparing fuctuations in subtype virus preva- viral diversity (2). lence between years or areas. The second trend was that testing and virus character- Capturing Viral Diversity ization protocols vary widely. Some countries or programs Improved understanding of avian infuenza virus need not screen for infuenza A virus, some selectively screen for H5 involve a monumental global effort but requires a shift in and H7 virus subtypes, and some screen only for HA and screening practices to move beyond emphasis on highly NA virus subtypes, but not subtype virus combinations. Al- pathogenic avian infuenza viruses. Where available, ge- though we acknowledge resource and capacity limitations nomic sequencing for detection of avian infuenza virus for analysis, the high level of effort required to capture or may provide more robust subtype fndings. sample wild birds argues for investment to test for virus A recent study detected by sequencing different HA subtypes in addition to those believed to be currently highly subtype viruses that had not been detected by antigenic pathogenic, to sequence as many as economically feasible, subtyping approaches (20). However, we call for a phase and to share samples and genomic data widely. Sequence change in surveillance programs, which includes additional data are needed to effectively track viral diversity, spread, measures to track avian infuenza virus diversity beyond and evolution. subtype, at least in a subset of samples. Capturing informa- The third trend was that critical data are defcient in tion on all 8 avian infuenza virus gene segments by rou- most reporting systems. Measures of sampling effort are tinely sequencing wild bird isolates would enhance under- often absent. None of the data sources reviewed con- standing of avian infuenza virus dynamics even more. For frmed that a country did not conduct surveillance, which example, infuenza A(H7N9) virus that caused respiratory confounded analyses of negative fndings. Approximate disease in humans evolved from genetic contributions of location or date of positive and negative fndings is often ≥4 gene segment origins, including sources from wild birds missing, which hinders spatiotemporal risk analyses. Be- (3). These contributions exemplify complex major genetic cause positive fndings are commonly reported without de- evolution around antigenic drift and gene reassortment, nominator data, especially for H5 and H7 subtype viruses, which subtype characterization alone does not capture. relative risk for spillover is diffcult to assess. Only the In- The 6 less well-studied infuenza virus gene segments fuenza Research Database (18) enables aggregation of full may confer major determinants of infectivity, pathogenicity,

Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 21, No. 4, April 2015 2015 e3 ONLINE REPORT transmissibility, and host species susceptibility (e.g., the effciency and refnement of reporting systems and also en- role of the basic polymerase 2 gene segment in host range sure resource alignment across high-priority surveillance and virulence) (9). Tracking gene segments may be espe- and reporting. Overall, a coordinated surveillance system cially useful for wild birds, given the high reassortment rate should capitalize on global sharing tools to promote access in their avian infuenza virus genome sequences (21) and the to information that will support rapid detection of these vi- unknown potential for transient genomes to become stable rus and ongoing analysis. and pose risks for endemic infections or transmissibility to or pathogenicity in humans. As a long-term goal, surveil- Targeted Country Participation lance should be refned to maximize understanding of trans- A coordinated, annual surveillance system with a global mission factors (e.g., host receptivity and susceptibility, perspective does not necessarily require participation from host dispersal) and ecologic factors (e.g., climate-dependent every country. Rather, resource allocation could be priori- viral persistence, migration timing and range) that drive avi- tized to provide sustained surveillance in a few targeted an infuenza virus prevalence in wild birds (22) and enable locations and in specifc seasons that maximize informa- spillover, emergence, and maintenance (1). tion on viral diversity relevant to potential spread (e.g., Coordinating bodies, such as OFFLU, have an op- high-risk species, species interfaces, major staging and portunity to develop specifc standards for avian infuenza migration stopover sites, and reassortment hotspots [23]). virus diversity-oriented surveillance programs to ensure a Recent analysis of avian infuenza virus subtype diversity clear strategy forward for the scientifc community and its and richness suggests that 75% of HA and NA subtype di- funders. Similarly, funders have a key role in driving ef- versity in wild birds could be captured through targeted forts to track avian infuenza virus diversity but will have to surveillance efforts in the Northern Hemisphere over a embrace sustained screening efforts for highly pathogenic 4-year period (24). and low pathogenicity avian infuenza viruses and promote In addition, fndings recently reported from the larg- the value of increased sharing of negative fndings and re- est avian infuenza surveillance program in wild birds ever quire full-genome sequencing of avian infuenza viruses, implemented (a study by the US Department of Agricul- even if required for only a subset of samples. ture and Department of Interior in collaboration with authorities in Canada and Mexico) suggested that hotspots Reporting Systems of avian infuenza virus in wild birds were primarily lo- Despite benefts of international sharing of avian infuenza cated in the northern latitudes of the United States (25). viruses, regardless of their pathogenicity, there is no stan- These fndings suggest that sites in the Northern Hemi- dardized and comprehensive reporting requirement beyond sphere are high-yield starting locations for viral diversity, highly pathogenic avian infuenza virus and H5 and H7 especially because we found that countries considered subtypes of low pathogenicity avian infuenza viruses, nor as major sources of avian infuenza virus diversity (e.g., adequate reporting incentives. Scientifc journals and on- Canada, China, Germany, Mongolia, Norway, Russia, the line databases enable sharing of information from research United Kingdom, and the United States) have reported projects, as well as from offcial government surveillance, surveillance data since 2008, but to different data portals but these sources inherently underreport negative fndings, (Figure; online Technical Appendix). and the lack of standardization among studies reduces Coordinating extant programs in areas with major value to authorities responsible for prevention and control. roles in avian infuenza virus diversity would be a cost- Online databases, such as the Infuenza Research Database effective frst measure. Although we propose an initial and GenBank, provide forums for detailed and consistent focus on the Northern Hemisphere to leverage current reporting, including sequence data. investments and target surveillance on the basis of prior We urge avian infuenza virus surveillance funders to avian infuenza study fndings reported above (24,25), we require reporting of results to the Infuenza Research Da- do not intend to undermine the role of efforts elsewhere. tabase to drive sharing of metadata and genetic sequence We especially acknowledge that bias in surveillance effort information. This sharing would expand the utility of lo- has limited current knowledge on avian infuenza virus cal- and national-level data to feed into global data analy- diversity in the Southern Hemisphere (4). Surveillance in sis. The limited current comparability of data can inform the Southern Hemisphere, where resources are available, database directors on the need to harmonize data deposi- provides highly useful information on exchange in the tion requirements, improve interoperability, and encourage avian infuenza virus genetic pool through bird migration full reporting of negative and positive results to optimize (migration–shedding dynamics may enable avian infu- tracking potential for avian infuenza viruses. Ongoing enza virus dispersal over extensive distances [5]), poultry discussions between coordinating bodies, such as OFF- trade, and maintenance of some specifc phylogenetic lin- LU, database designers, and funders, might help improve eages of these viruses. e4 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 21, No. 4, April 2015 ONLINE REPORT

Figure. Feasibility of coordinating and improving avian infuenza surveillance in wild birds where viral diversity is highest. Countries in red, orange, and yellow currently self-report some type of avian infuenza surveillance in wild birds (For a country list, see online Technical Appendix, http://wwwnc. cdc.gov/EID/article/21/4/14- 1415-Techapp1.pdf). Country income levels, based on gross domestic product, further suggest fnancial capacity to contribute to a coordinated surveillance system. The polar view emphasizes where most avian infuenza viral diversity is circulating.

Study Limitations this information. Additional relevant papers were likely Our analysis was intended to provide a snapshot of recent available through other databases. avian infuenza virus surveillance effort in wild birds to Non-reporting does not indicate lack of surveillance explore how existing infrastructure could be optimized to and likely increases the number of countries actually con- capture viral diversity. There are limitations of our study, ducting surveillance. We also recognize that reports of including information missed through our data compilation surveillance are not always verifed for accuracy, and sur- methods. Only a subset of OIE member countries respond- veillance at one time point might not indicate current ca- ed to the survey, and some responses were incomplete or pacity. We included sampling effort reported that occurred unclear, which was potentially caused by instructions or during 2008–2013, but not all data sources spanned that language barriers. In addition, because only highly patho- time frame (e.g., the OIE survey only refected 1 year of ac- genic infuenza viruses or infuenza A H5 or H7 subtype vi- tivities). Last, because in some cases it was not possible to ruses are required for reporting to OIE, data for low patho- ascertain the lead institution organizing surveillance efforts genicity avian infuenza viruses were reported voluntarily in a given country (government versus in-country research by countries. Thus, reports to OIE cannot be assumed to organizations or outside institutions), this information was be comprehensive. not compiled. We acknowledge that outside research might We targeted information specifc for wild birds, but it not be indicative of true in-country capacity and might have was not always possible from the data sources reviewed to different implications for reporting. Despite several limi- determine whether animals were truly free-ranging or cap- tations, our fndings suggest that investments have been tive (e.g., data from the World Animal Health Information recently made for surveillance in most countries and thus Data Interface [WAHID] was specifc for wild species but provide a starting infrastructure for capturing avian infu- did not distinguish by setting, which might show different enza virus diversity. dynamics for avian infuenza viruses). Articles reporting surveillance from the Web of Knowledge were reviewed A Cost-effective Surveillance System for specifc parameters (e.g., time frame, wild bird species), Establishing collaborative networks among countries but this method excluded papers not explicitly reporting would be cost-effective, reduce the need for additional

Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 21, No. 4, April 2015 2015 e5 ONLINE REPORT laboratory capacity in regions of interest for surveillance, Acknowledgments and complement and support other surveillance programs We thank the country delegates who responded to the survey in maintaining trained and operational feld teams in tar- administered by the OIE, as well as the Infuenza Research geted locations, instead of rebuilding local capacity and Database team for their guidance. logistics for each new avian infuenza virus threat. A more The concept of this study was developed by W.B.K., C.C.M., robust understanding of virus diversity and changing vi- S.M.E., and K.M.S. in collaboration with K.H. C.C.M. reviewed ral trends might inform biosecurity efforts at the wildlife/ the literature base, infuenza research database, and WAHID domestic animal interface in which virus spillover might reports. S.M.E. reviewed the OIE survey. C.C.M., S.M.E., and occur. This understanding has potential value, given dev- W.B.K. drafted the paper. W.B.K. provided technical guidance astation from the death or culling of millions of birds throughout the data review process. S.F. and K.B.J. designed during 1 outbreak of highly pathogenic avian infuenza and disseminated the survey to OIE delegates and designed and (26), because surveillance provides information on genes collected data from WAHID. D.E.S., R.J.W., and E.M. provide of low pathogenicity avian infuenza viruses that could oversight and editing on surveillance and virology aspects. recombine or mutate to produce high pathogenic avian in- J.A.K.M., N.G., W.B.K, and P.D. contributed to ecology and fuenza viruses (27). feld techniques interpretation and recommendations. All authors Stronger capacity for early detection of changing reviewed the report and provided input. avian infuenza virus dynamics in reservoir populations may provide inputs to support public health and pandemic C.C.M., S.M.E., K.M.S., J.A.K.M., P.D., and W.B.K. were preparedness. These inputs include potentially useful ge- supported by the US Agency for International Development netic material for vaccine development, detection of virus Emerging Pandemic Threats Program PREDICT. origins, refned diagnostic capacity beyond infuenza A Ms. Machalaba is the Program Coordinator for Health screening, improved understanding of molecular determi- and Policy at the EcoHealth Alliance, New York, New York. nants of transmission and pathogenesis from gene segment She serves as Program Offcer for the IUCN Species Survival characterization, and analysis of the potential for virus Commission Wildlife Health Specialist Group and is a doctoral spread through migration and trade (28). student in Public Health at the City University of New York. Her The cost of avian infuenza virus outbreaks in poultry research interests focus on One Health approaches to human, is substantial; outbreaks of infuenza A(H5N1) virus during animal, and environmental health challenges. 2004–2009 caused US $30 billion in damage (29), and the frequency of highly pathogenic avian infuenza outbreaks in poultry appears to be increasing (11). Rather than spo- References radically releasing large amounts of funding for wild bird 1. Hoye BJ, Munster VJ, Nishiura H, Klaassen M, Fouchier RA. Surveillance of wild birds for avian infuenza virus. Emerg Infect Dis. surveillance when specifc avian infuenza viruses emerge, 2010;16:1827–34 and http://dx.doi.org/10.3201/eid1612.100589 sustained national, regional, and global investments can 2. Latorre-Margalef N, Tolf C, Grosbois V, Avril A, Bengtsson D, provide the targeted baseline level of systematic surveil- Wille M, et al. Long-term variation in infuenza A virus prevalence lance we propose. Many countries, especially where avian and subtype diversity in migratory mallards in northern Europe. Proc Biol Sci. 2014;281:20140098 and http://dx.doi.org/10.1098/ infuenza virus diversity in wild birds is highest, are already rspb.2014.0098 investing in some form of avian infuenza virus surveil- 3. Liu D, Shi W, Shi Y, Wang D, Xiao H, Li W, et al. Origin and lance in wild birds. diversity of novel avian infuenza A H7N9 viruses causing Current efforts should be refned by leveling the invest- human infection: phylogenetic, structural, and coalescent analyses. Lancet. 2013;381:1926–32 and http://dx.doi.org/10.1016/ ment roller coaster that has funded subtype-specifc wild S0140-6736(13)60938-1 bird surveillance toward a lower-cost but long-term invest- 4. Olsen B, Munster VJ, Wallensten A, Waldenstrom J, Osterhaus AD, ment in collecting and sequencing wild bird avian infu- Fouchier RA. Global patterns of infuenza a virus in wild birds. enza viruses. 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