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      Avian Influenza Virus (H11N9) in Migratory Shorebirds Wintering in the Amazon Region, Brazil

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          Abstract

          Aquatic birds are the natural reservoir for avian influenza viruses (AIV). Habitats in Brazil provide stopover and wintering sites for water birds that migrate between North and South America. The current study was conducted to elucidate the possibility of the transport of influenza A viruses by birds that migrate annually between the Northern and Southern Hemispheres. In total, 556 orotracheal/cloacal swab samples were collected for influenza A virus screening using real-time RT-PCR (rRT-PCR). The influenza A virus-positive samples were subjected to viral isolation. Four samples were positive for the influenza A matrix gene by rRT-PCR. From these samples, three viruses were isolated, sequenced and characterized. All positive samples originated from a single bird species, the ruddy turnstone ( Arenaria interpres), that was caught in the Amazon region at Caeté Bay, Northeast Pará, at Ilha de Canelas. To our knowledge, this is the first isolation of H11N9 in the ruddy turnstone in South America.

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          Influenza A viruses of migrating wild aquatic birds in North America.

          Surveillance of North America's wild ducks and shorebirds for 26 and 16 years, respectively, revealed differences in the prevalence of orthomyxoviruses between these hosts. Shorebirds had a high frequency of influenza A virus isolation during their northern migration, while wild ducks had high virus isolation frequencies during their southern migration. Some subtypes of influenza occurred regularly in both hosts with a 2-year periodicity, whereas others rarely occurred. Hemagglutinin subtypes H1 through H12 occurred in both hosts; H13 occurred only in shorebirds; and H14, H15, and influenza B and C never were detected. Shorebirds manifested a broader range of subtypes suggesting that shorebirds are the leading source of some viruses (such as H5) which are isolated less frequently from wild ducks. The viruses reported in this study are available for genomic study to determine whether prediction of host range or pandemic potential is possible.
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            Surveillance of Wild Birds for Avian Influenza Virus

            Avian influenza virus (AIV) gained a high profile after the unprecedented bird-to-human transmission of highly pathogenic AIV (HPAIV) subtype H5N1 in 1997. Originating in Asia, HPAIV (H5N1) subsequently caused widespread deaths among wild and domestic birds in Southeast Asia and westward throughout Europe and Africa in 2005 and 2006. After ≈50 years of research in wild birds, a wide range of low-pathogenicity AIV (LPAIV) subtypes is known to circulate in numerous species (1,2–5), and LPAIVs are believed to perpetuate in aquatic bird populations (6). In contrast, outbreaks of HPAIV are extremely rare in wild birds (7). Although the role of wild birds in HPAIV maintenance remains controversial (8), the magnitude of the subtype H5N1 epidemics increased the demand for early recognition of potential threats to humans and poultry and an understanding of the natural history of AIV in wild birds. Consequently, surveillance of aquatic bird populations surged (9). Although surveillance for AIV often uses state-of-the-art storage, transport and diagnostics, these must be underpinned by appropriate survey design, sampling, and interpretation in the context of the host population. In the wake of such rapid growth in surveillance, we reviewed the literature to determine a scientifically and statistically sound approach to the design, conduct, and interpretation of surveillance for AIV and other wildlife diseases. Current Surveillance We reviewed 191 published reports of surveillance in wild birds (Technical Appendix). The number of studies initiated per year rapidly increased after the first reports of HPAIV (H5N1) in Asia (Figure 1). All studies addressed 4 major lines of investigation: 1) early detection of HPAIVs; 2) ecology and epidemiology of LPAIV in host populations; 3) diversity and evolution of viral strains within wild birds; and 4) identification of the pathogens that infect individual birds or populations, often as part of multipathogen surveillance. Multiple aims can, and often are, addressed within the same surveillance program, albeit in a post hoc manner. However, identifying the aims in advance is vital, because what, when, and where to sample will critically depend on the purpose of the survey (10,11). Figure 1 Average number of surveys of avian influenza in wild birds initiated per year in different awareness periods: each decade from the first discovery in 1961 until the outbreak of highly pathogenic avian influenza virus (HPAIV) (H5N1) in Asia in 1997; the period after the first outbreak, 1997–2004; and the period after mass deaths of wild birds from HPAIV (H5N1) (2005–2007). Black bar sections indicate studies citing the detection of contemporary HPAIV strains as one of the main aims of their survey are indicated in black; white bar sections indicate studies investigating other aspects of the wild bird–avian influenza system without mention of monitoring HPAIV. Early Detection of HPAIV More than half of the studies reviewed, and all but a handful initiated since the mass bird deaths in 2005–2006, cited early detection of HPAIV as one of the main goals of conducting the research (Figure 1). Such early warning systems question whether HPAIV exists in a population at a given location and point in time. The global rarity of HPAIV in wild birds and apparent clustering of such cases (7) present additional challenges to addressing this aim. Ecology and Epidemiology Greater understanding of transmission cycles, reservoirs, and the role of wildlife in the dynamics of AIV invoke questions related to the epidemiology and ecology of the virus, including host range and spatial and temporal variation in infection (12,13). Elucidating such questions requires investigating not just presence or absence of infection in a specific host, but also prevalence over space and time. Viral Diversity Influenza viruses are highly diverse and capable of rapid genetic alteration. Understanding the pathogenic and antigenic properties of AIVs circulating in the host population and the rate and direction of genetic alterations could become a powerful tool for identifying transmission parameters, reservoir populations (14), viral maintenance in the face of host immunity (12,15), and factors promoting disease emergence (10). Such information also facilitates compilation of comprehensive diagnostic reference panels and generation of potential vaccines (13). Investigation of variation in the viral population requires isolates that represent the entire circulating virus pool. Host Health Almost 15% of the studies reviewed aimed to ascertain whether certain individuals or populations had been infected with AIV as part of broader health surveys within the context of conservation programs, or in an attempt to understand causes of death. Although these studies often have a predefined host population of interest, they are likely to be sensitive to the underlying spatial and temporal patterns of disease. Critical Assessment To characterize the specific features required for rigorous wildlife disease surveillance, it is critical to highlight methods that encumber our current approach. Our assessment therefore aims to foster the development of more objective and scientifically sound disease surveillance networks. Maximizing Viral Yield A successful surveillance program is often perceived as one that identifies a high number of positive samples. Moreover, exploitation of spatial, temporal, phylogenetic, and demographic differences in viral prevalence have been advocated to maximize the proportion of positive samples collected (12,16). Minimizing the number of negative samples is expedient from a laboratory perspective, particularly when labor-intensive virus isolation techniques are being used. However, a key tenet of surveillance is that the sampling scheme is representative: infection characteristics of the host population and genetic diversity of the viral population are sufficiently captured, and results can be interpreted on the basis of statistical probability (11,17). A study designed to maximize the number of positive samples by sampling historically high cohorts, populations, times, and locations can confirm the presence of the disease in the sampled cohort. However, such samples cannot be used to conclude the absence of AIV in the population or to estimate prevalence or diversity of circulating viral strains (17). Host Range Although AIVs have been isolated from >100 species, several species from the orders Anseriformes (ducks, geese, and swans) and Charadriiformes (shorebirds) are thought to act as the reservoir community for AIV (6), primarily because AIVs have been most frequently isolated from these groups (9). Yet, surveillance is rarely representative of the diversity of wild birds or their relative abundance at the time and location of sampling. Considerable bias exists toward species that are easily caught or are present in accessible areas at high concentrations (9,13). Surveys that have included a wide range of species often obtained samples in a highly opportunistic manner, resulting in few species being sampled in reasonable numbers (12–13). For instance, despite sampling >56,000 birds in the Netherlands from 1998 to 2009, only 20 of the 174 species were sampled >300 times. Moreover, prevalence in a given species may vary over space and time. Although passerines have often been found negative for AIV, recent evidence suggests that, when sampled in or near waterfowl-rich bodies of water, a high proportion of individuals from 8 different passerine families show infection (18,19). Current surveillance may, therefore, overlook many potential reservoir or transient host species and their role in the introduction, transmission, maintenance and diversity of AIV. Temporal and Spatial Patterns The prevalence of AIV infection has long been recognized to vary over time and space. Viruses have been most frequently isolated from duck populations in North America and Europe in late summer and early autumn (5,15,20), a pattern attributed to high concentrations of susceptible juvenile birds on premigratory staging grounds (4,6). Less frequent isolations from wintering populations have prompted suggestions that prevalence rapidly decreases over the course of autumn migration (21,22); thus, premigratory staging grounds in late summer and early autumn are considered the optimal time and location for conducting surveillance among waterfowl (16,23). Yet when samples have been collected elsewhere, high numbers of AIVs have been isolated in winter (21,24), spring (20), and summer (25). Several positive samples from birds in the tropics (26) have also been found, including unexpectedly high numbers in tropical Africa (27). The temporal and spatial bias in existing surveillance may therefore result in delayed detection of novel strains or an incomplete understanding of AIV transmission, maintenance, diversity, and evolution. Age-dependent Patterns Pioneering work by Hinshaw et al. (4) found significantly higher prevalence of AIV infection among juvenile birds than among contemporaneously sampled adult birds, leading to the suggestion that immunological naivety may make juvenile birds a high-risk group within waterfowl populations. Emphasis has subsequently been placed on sampling juvenile birds; accounting for ≈80% in some recent surveys. However, wild bird populations are rarely composed of >80% juvenile birds, and numerous infected adults have also been found (4,24). Given that recent experimental results indicate that age at the time of infection might also affect the extent of viral shedding (28), different age cohorts may play different roles in the introduction, transmission, maintenance, and diversity of AIVs. Site of Infection AIVs replicate in the gastrointestinal tract (sampled by swabbing the cloaca or collecting droppings) and in the respiratory tract (sampled by swabbing the oropharynx) (16). Individual mallards (Anas platyrhynchos) have historically shown higher detection probability from cloacal c.f. oropharyngeal swabs (29; Figure 2). Accordingly, 61% of studies investigating contemporary infection sampled the gastrointestinal tract alone. However, the site of infection may differ between species. As part of ongoing surveillance (21,29), free-living Eurasian wigeons (Anas penelope) showed no difference in detection probability between the cloacal and oropharyngeal swabs (p>0.05, McNemar test; Figure 2). In contrast, white-fronted geese (Anser albifrons) were roughly 2× as likely to have infection detected in the oropharynx (6.58%; 95% confidence interval 6.57–6.59) than in the cloaca (3.13%; 95% confidence interval 3.13–3.14; p 10,000 species of birds worldwide, careful selection of a local target population is critical to the design of any surveillance program. Because the prevalence of infection is generally low (requiring large sample sizes) and can vary over time and between locations within a species, it is difficult to make an initial assessment of the most important species to target on the basis of virus detection alone. Each of the surveillance aims outlined above may be most appropriately addressed by considering 1) populations with evidence of previous infection, or ecologic potential for infection (32), on the basis of not only existing literature and conventional monitoring but also serosurveillance in a large number of locally and regionally abundant species; and 2) Evidence of contemporary AIV infection in populations that were identified in step 1, and species in which AIV has historically been detected (for comparative purposes). Surveillance for emergent HPAIV may also benefit from targeting species displaying natural histories of interest, including species that link wild and human/agricultural populations or disparate locations. Serologic studies have great potential for enhancing wildlife disease surveillance and understanding. However, in isolation, cross-sectional observations of seroprevalence provide insufficient information to interpret the degree to which a population has been infected with AIV. Without age specificity, high seroprevalence may indicate a recent outbreak of infection or long-term antibody maintenance rather than persistence of AIV infection in the population (14,16). Moreover, low seroprevalence may result from a high mortality rate among infected birds, a long time interval between infection and sampling, or species-specific differences in the sensitivity or specificity of the antibody diagnostics. Explicit interpretation of seroprevalence calls for age-specific sampling, longitudinal observations, understanding of the underlying epidemiologic dynamics, and experimental validation of antibody diagnostics. Individual Birds within Populations Within each species, infection may depend on multiple factors, including age and prior exposure to AIV (4), gender (33), and even nutrition or social status (8). Given that most capture methods inherently result in biases within these cohorts, a population should ideally be sampled to account for these differences. Experimental validation of such interindividual differences in infection could greatly enhance the design and interpretation of surveillance. When, Where, and How Often to Sample? When and where sampling is conducted will critically depend on the question at hand and should be representative of the biology of the hosts of interest. Single time or location studies may be sufficient to inform of novel incursions of HPAIV (Table) and may therefore be best matched to times/locations with a high risk for wild bird–poultry interaction. Changes in climatic conditions, host population dynamics, and host population immunity are likely relevant to understanding the ecology, epidemiology, and evolution of AIV in its natural host(s) (34). Enhancing our knowledge in these areas will require information from before, during, and after infection from ecologically connected populations (35), often over longer periods and across large spatial scales when studying migratory birds (36). Coordinated local surveys, both along flyways and over time, will greatly enhance these efforts. Table Data requirements for assessment of major questions regarding avian influenza in wild birds* Aim Type of question Geographic range Temporal range Frequency Early detection of HPAIV Presence/absence Local/regional Period when birds present Approximately weekly (average infection duration) Ecology and epidemiology Comparative prevalence Local to flyway, depending on the process in question 1 to many epidemic seasons (multiple times/year) Weekly to monthly (multiple times before, during, and after an epidemic) Diversity and evolution Comparative prevalence (of viral strains) Flyway to global Decades (multiple times/year repeated for multiple years) Monthly to seasonally *Larger-scale studies can be compiled over large geographic areas from relevant local surveys that are methodologically comparable and over long periods from relevant annual surveys that are likewise methodologically comparable. HPAIV, highly pathogenic avian influenza virus. How Many Individual Birds Should Be Sampled? As prevalence decreases, an increasingly large number of birds need to be sampled to detect contemporary infection (Figure 3, Figure 4). Deciding just how many is critically dependent on the study aim, with a clear distinction between surveys that aim to substantiate freedom from infection (presence or absence), and those that are designed to provide an estimate of disease prevalence. Figure 3 Probability of detecting >1 individual bird infected with avian influenza virus from a given number of samples selected at random from an extremely large population in which individual birds are infected at random at different prevalence levels. Although this nominal minimum detectable prevalence assumes binomial sampling, it can also be used for gaining a rough quantitative estimate of the minimum number of samples required before embarking on a surveillance program. Figure 4 The 95% confidence intervals for prevalence in an independent population for a given number of samples, derived from the binomial distribution. Confidence intervals depend on the number of samples taken and unbiased prevalence of infection; they should be calculated and reported along with prevalence estimates when reporting surveillance results. Presence/Absence In practice, it is not possible to confirm disease freedom in a large population by any direct observational method. Instead, appropriate sampling and analysis can demonstrate that at that time and location, prevalence was below a nominal detection threshold (Technical Appendix) (17). Although this nominal minimum detectable prevalence assumes binomial sampling, it can also be used for gaining a rough quantitative estimate of the minimum number of samples required before embarking on a surveillance program (Figure 3; Technical Appendix). Given that information on the absence of pathogens is crucial to understanding disease dynamics (10), postsurveillance reporting of such maximum undetected prevalence is highly desirable for all studies with negative findings. Prevalence The proportion of positive findings among a given number of samples is rarely sufficiently precise to inform population prevalence. Thus, the confidence intervals of any observed proportion should be calculated and reported alongside any prevalence estimates when reporting surveillance results. Such confidence limits depend on the number of samples taken and the underlying true (unbiased) prevalence of infection (Figure 4). Achieving Effective Surveillance Each of the points above highlight the need for surveillance that captures the underlying temporal, spatial, demographic, and phylogenetic variation in the wild bird population, often requiring detailed information on host population size, density, demographic structure, rates of recruitment and attrition, habitat utilization, and species composition. However, wildlife surveillance is also faced with substantial logistical and financial constraints. Effective surveillance, therefore, requires a compromise between sampling that is based on probability and the constraints of sample collection, transport and analysis, the details of which will depend on the specific objectives of the survey. To this end, it is critical to have active, investigator-defined surveillance designs based on probability on a larger scale while using convenience sampling within these units (11). For instance, probability methods could be used to plan the species, locations, and months of the year to sample, and a certain number of individual birds within these units could be sampled by ornithologists and hunters, with additional top-up sampling where necessary. Such convenience-within-probability surveillance could provide statistically valid estimates of disease absence and prevalence by reducing the effect of bias generated by sampling on a first-come-first-served basis. It facilitates stipulation of an upper limit to the use of convenience samples, allowing targeted allocation of limited sampling, diagnostic, and financial resources. To employ such convenience-within-probability surveillance, samples will often need to be collected from times, places, and species that are not currently covered by ornithologists and hunters. Preferably, individual birds should be sampled to confirm species, gender, age, and body mass, and sampling of digestive and respiratory tracts. However, when it is logistically and/or financially difficult to capture live birds several alternatives exist. Swabbing of fresh, species-specific feces is 1 method for collecting a regulated number of samples (16). Species should be identified through careful presampling observation of flocks, or, when sampling mixed-species flocks, through DNA barcoding of the fecal samples (37). Given that AIV can be detected from the same nucleic acid extract used in species identification (37), and substantially more samples can be collected at a much higher frequency than traditional trapping methods, dropping samples may greatly enhance our capacity to detect AIV in the population. Other, more proximate surveillance methods include sampling surface water that is, has been, or is about to be inhabited by wild birds (16), as well as regular sampling of sentinel species (38). Both methods are likely to yield insight into infection in the broader host population (16), although their usefulness for understanding infection in specific populations must be carefully assessed. Conclusions Surveillance for wildlife diseases is an inherently arduous task. However, as the vanguard of our understanding of these diseases, surveillance warrants a scientific approach. To make major inroads into the broader understanding of AIV ecology, epidemiology, and evolution, as well as risks associated with HPAIV, an integrated sampling strategy with clearly defined aims and appropriate methods is required. The financial and logistical constraints of covering vast spatial and temporal scales call for concerted efforts among our combined virologic, ecologic, and genetic expertise. Supplementary Material Technical Appendix Source References and Formulas for Estimating Minimum Detectable Prevalence.
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              Is the gene pool of influenza viruses in shorebirds and gulls different from that in wild ducks?

              Evidence is presented for a second major gene pool of influenza A viruses in nature. Shorebirds and gulls harbor influenza viruses when sampled in the spring and fall. Approximately half of the viruses isolated have the potential to infect ducks but the remainder do not. The hemagglutinin subtypes that are prevalent in wild ducks were rare or absent in shorebirds and gulls.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                16 October 2014
                : 9
                : 10
                : e110141
                Affiliations
                [1 ]BSL3+ Laboratório de Virologia Clínica e Molecular do Instituto de Ciências Biomédicas (ICB-II), Universidade de São Paulo, São Paulo, Brazil
                [2 ]Departamento de Biologia da Universidade Federal Rural de Pernambuco, Pernambuco, Brazil
                [3 ]CIRAD-ES, UR AGIRS, Montpellier, France
                [4 ]Department of Infectious Diseases, St. Jude Children's Research Hospital, Memphis, Tennessee, United States of America
                [5 ]Agência de Defesa Agropecuária do Estado do Pará- ADEPARA, Pará, Brazil
                [6 ]SFA-PA- Superintendência Federal de Agricultura no estado do Pará. Ministério da Agricultura Pecuária e Abastecimento (MAPA), Distrito Federal, Brasília, Brazil
                [7 ]Biologia Animal da Universidade Federal de Pernambuco, Pernambuco, Brazil
                [8 ]Centro de Ciências Tecnológicas da Terra e do Mar, Universidade do Vale do Itajaí (UNIVALI), Santa Catarina, Brazil
                [9 ]Centro Nacional de Pesquisa e Conservação das Aves Silvestres (CEMAVE), Cabedelo, Paraíba, Brazil
                Australian National University, Australia
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: JA SMAJ JOB ELD RGW. Performed the experiments: JA SMAJ RFH DW LMT TO MMMS RR DG AMMR ACS LLB MAM MEL JOB PS ISN NG JF RW ELD. Analyzed the data: JA SMAJ RFH DW LMT TO MMMS NG RW ELD. Contributed reagents/materials/analysis tools: JA SMAJ RFH DW LMT TO NG JF RW RGW ELD. Wrote the paper: JA SMAJ DW LMT TO MMMS NG RW RGW ELD.

                Article
                PONE-D-14-00407
                10.1371/journal.pone.0110141
                4199675
                25329399
                e18aedfb-4e9d-4b6d-b979-520024dd3b1e
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 6 January 2014
                : 16 September 2014
                Page count
                Pages: 10
                Funding
                This work has been funded in part by the Fundacão de Amparo a Pesquisa do Estado de São Paulo (FAPESP), Conselho Nacional de Desenvolvimento a Pesquisa (CNPq), Ministério da Agricultura, Pecuária e Abastecimento (MAPA), the Wildlife Conservation Society (WCS) and the National Institute of Allergy and Infectious Diseases of the National Institutes of Health, under contract number HHSN266200700005C and ALSAC. The funders had no role in the study design, data collection and analysis, decision to publish or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Veterinary Science
                Animal Types
                Wildlife
                Veterinary Diseases
                Veterinary Virology
                Animal Influenza
                Zoonoses
                Veterinary Microbiology

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